A Dictionary of Birds 9781472597458, 9781408138403, 9781408138380

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A DICTIONARY OF BIRDS

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A Dictionary of Birds Edited by BRUCE CAMPBELL and ELIZABETH LACK Published for The British Ornithologists' Union

T & A D POYSER · Calton

First published 1985 by T & AD Poyser Ltd Print-on-demand and digital editions published 2010 byT & AD Poyser, an imprint of A&C Black Publishers Ltd, 36 Soho Square, London W1D 3QY www.acblack. com Copyright © 1985 The British Ornithologists' Union ISBN (print) 978-1-4081-3840-3 ISBN (epub) 978-1-4081-3839-7 ISBN (e-pdf) 978-1-4081-3838-0 A CIP catalogue record for this book is available from the British Library All rights reserved. No part of this publication may be reproduced or used in any form or by any means - photographic, electronic or mechanical, including photocopying, recording, taping or information storage or retrieval systems - without permission of the publishers. This is a print-on-demand edition produced from an original copy. It is produced using paper that is made from wood grown in managed sustainable forests. It is natural, renewable and recyclable. The logging and manufacturing processes conform to the environmental regulations of the country of origin. Printed in Great Britain by Martins the Printers, Berwick upon Tweed

Contents Prefaces

VII

Editorial Introduction

IX

Note on Classification followed, contributed by K.H. Voous

X

Avian Anatomical Nomenclature, contributed by }.}. Baumel

X

Table of Classification, including list of major articles on bird groups

Xl

List of Contributors

XIX

1-670

Dictionary: A-Z

v

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Prefaces By the President of the British Ornithologists' Union In 1964 the 'New Dictionary', as it became so well known, was termed a comprehensive book of reference on birds on a world-wide basis both by its editor and creator, Sir Landsborough Thomson, and by R.E. Moreau, then President of the BOU. The present volume is no different in this respect, but it has been very widely revised, a great part of it re-written, much fresh material added, and it forms a new and important almost encyclopaedic work, written and illustrated by several hundred experts. Once again the co-operation of authors, artists and photographers has been given unstintedly, nearly all of it in an honorary capacity, and to them all the Union owes much gratitude and praise. To the great expertise and ability of the senior editor, Dr Bruce Campbell, and to his tireless assistant Elizabeth Lack, has fallen the task of organizing and completing this ambitious work with the help of a panel of advisors, of whom Dr David Snow must be especially mentioned. They have given readily of their time, thought and knowledge for over five years and the Union is indeed grateful. Our publisher also earns generous thanks, for he has given patient and sympathetic help all through and has worked well beyond the limits to which most publishers in his position would go. A New Dictionary of Birds was in part a tribute to the memory of Professor Alfred Newton F.R.S., whose original A Dictionary of Birds was the inspiration behind Sir Landsborough Thomson's project for the Union's Centenary. A New Dictionary ofBirds has been an important source of reference for 20 years and it so remains. That it needs this new volume to update it in so comparatively short a time is a measure of the immense output of present research into a subject for which Professor Newton did so much to originate respect and esteem. The Union that he helped to found has here been provided with a worthy successor to the two previous works. J.F. MONK

By the President of the American Ornithologists' Union The American Ornithologists' Union congratulates the British Ornithologists' Union for the publication of this major new work in our field. The completion in 1985 of A Dictionary ofBirds continues and extends the service to ornithology provided first in 1896 by Alfred Newton's dictionary and then in 1964 by A. Landsborough Thomson's new dictionary. Because ornithology is expanding and diversifying so fast, the importance of having an up-to-date, comprehensive reference work of its terms is even greater now than it was at the time of Thomson's work. That work was initiated to mark the Centenary of the British Ornithologists' Union. This new dictionary was being prepared at the time that the American Ornithologists' Union celebrated its own centennial in 1983. We are particularly indebted to the editors and to all the other people involved in its production for the role the dictionary will play in fostering communication among nations. For students it will serve as an entrance to the present status of the field. For scientists it will serve as a research tool and a bridge between disciplines. We are also glad that many of our members were able to serve as contributors to such a worthy cooperative project. FRANCES C . JAMES

vii

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Editorial Introduction Dr D.W. Snow has made an outstanding contribution, not only as the author of 17 articles and numerous short entries, but with invaluable help and advice on the text, and later when reading the proofs. Drs L.G. Grimes, E.K. Dunn and P.J.K. Burton advised on the revision of many articles, and I.C.J. Galbraith was a generator of several short entries. We must also make special mention of the part played by Prof. K.H. Voous, whose classification the panel decided to adopt, (though authors have sometimes expressed their own views). Professor Voous wrote or revised all of the relevant articles, and answered many questions from us in his immaculate handwriting. Many authors, outside the scope of their own contributions, gave us help from time to time and, outside the list of authors, we should like to record our gratitude to Dr N.P. Ashmole, Prof. P.P.G. Bateson, N.J. Ball, A. Bell, Prof. R.J. Berry, Dr L. Birch, Dr R.I. Bowman, Mrs E. Brooks, A.R.M. Campbell, R.N. Campbell, S. Cowdrey, N.C. Davidson, Prof. J. Dorst, S. Digby Firth, Dr J.A. Gibb, Dr J. Horsfall, Dr P. Hudson, Dr I. Keymer, L. Kunzemann, Dr A.J. Lack, C.M. Lack, Dr P.C. Lack, Prof. A.M. Lucas, Dr P. Marler, K.T. Marsland, H. Mayer-Gross, Dr R.V. Melville, P.J.S. Olney, J.L.F. Parslow, Dr M.G. Ridpath, Prof. R.K. Ringer, F.N. Robinson, Dr R. Schodde, Dr J. Sincock, D. Smallwood, Dr H.N. Southern, J.K. Terres, Prof. H.B. Tordoff, M.W. Tweedie, Dr M.A. Vince, P. Ward (died 1979), P. Wayre, M.G. Wilson, I. Wyllie and Dr M. Yasuda. Dr J.F. Monk, as President of the BOU, gave us welcome support and encouragement in all stages of production, while our publishers, Trevor and Anna Poyser, have continuously helped and co-operated all through our years of work on the dictionary, and we must record our warmest gratitude and thanks to them. Amendment. In a work of this kind, freedom from error is unobtainable, and it has obviously been impossible to include all new information accruing during the years of preparation. The Editors welcome any intimation of necessary corrections or additions.

The Dictionary consists of articles on general subjects relating to birds, and on different kinds of birds mainly treated by families. The arrangement is alphabetical with cross-references in small capitals, so the dictionary constitutes its own index. The short entries define special terms, applications of names, or are merely cross-references to the relevant major article. No attempt has been made to provide a glossary of words that can be found in an ordinary dictionary. Language. Scientific terms formed from classical languages do not appear as entry headings unless they are in such common use as to be practically anglicized, or unless they have no satisfactory equivalents in common speech. Synonyms in modern foreign languages are also generally excluded. The English names of birds chosen as entry headings are those in use by British ornithologists; the inclusion of dialect or archaic names is limited to those most widely occurring. North American names and others used in the English-speaking world have also been covered as far as practicable. Scientific names of groups above generic level have been used in headings; families are treated under their English names. Scientific names of genera are not used as entry headings except where they are also the English substantive names. References. These are generally in English and mainly limited to books, monographs or important papers, which contain fuller accounts of particular subjects. Such publications will usually give references to the international literature. In a few cases we have added references which have been too recently published to be made use of in the articles concerned. Illustrations. The photographs have been chosen to illustrate different activities of birds. We are indebted to E.J. Hosking for advising us and for his help in collecting suitable subjects from a number of leading photographers. The drawings of birds, normally one to each family, have been assembled for us by Robert Gillmor and executed by 18 artists. The diagrammatic text figures have been supplied mainly by the authors of the articles to which they refer, but a number have been redrawn by J.W.N. Turner. We are very grateful to all of them. Collaboration. The wide subject cover has been made possible by enlisting contributions from. 280 ornithological and other specialists, drawn from every continent and from 29 countries. Artists and photographers bring the total to well over 300. The articles on general subjects are mostly by authors in the UK and the USA; the articles on bird groups are by authors from throughout the world. To all of them we are most grateful. During the long course of the preparation of the dictionary we have had the assistance of an advisory panel which has met at intervals. Its members were Sir Hugh Elliott, BOU President in January 1979 when the project was begun, S. Cramp (part-time), R. Gillmor (part-time), E.J. Hosking, Dr J.R. Krebs, Dr J.F. Monk (part-time), Dr R.J. O'Connor, P.j.S. Olney (part-time), Dr C.M. Perrins, T. Poyser and Dr D.W. Snow.

Full general references: Campbell B. & Lack, E. (eds). 1985. A Dictionary of Birds. Calton (Poyser) and Vermillion (Buteo). Abbreviated references: Campbell, B. & Lack, E. (eds). 1985. Diet. Birds, Calton & Vermillion. Reference to a contributed article: Evans, P.R. 1985. Article 'Migration'. In Campbell, B. & Lack, E. (eds). Diet. Birds. Calton & Vermillion.

ix

Note on the Classification Followed Other notable contributions to the recognition, sequence and relationship of higher taxa have been included in the table of classification and in the specific articles. In this situation of uncertainty and hopeful expectation it will be understood that it has not been possible to follow all of the recently proposed changes in the classification of birds. More time is needed for their evaluation, before they are accepted and incorporated into standard lists and handbooks. Here, the starting point has been K.H. Voous's List ofRecent Holarctic Bird Species (1973, 1977), which was augmented for world-wide use for this occasion. Throughout, Morony, Bock and Farrand's Reference List of the Birds of the World (1975) and additions by Bock and Farrand (1980) can be recommended as a sound base for tackling any problems of taxonomy, sequence and literature reference at the specific, generic, familial and ordinal levels relating to the comparative systematics of living birds.

The classification followed in this work, down to familial level, is shown in the succeeding table. It deviates from the classification used in the 1964 Dictionary, which for the non-passerine groups was mainly that of volumes 1-7 of the Check-list of Birds of the World (1931-1951) by the late ].L. Peters, which itself was essentially based on the well-known Wetmore system. The families of songbirds, by 1964 not yet fully treated by Peters' successors, followed the so-called Basle sequence with 'crows last' (Mayr and Greenway 1956), as opposed to the 'crows first' sequence of Wetmore. The first paragraph of the note on classification followed in the 1964 edition closes with the words: 'It seems likely that the Check-list, when completed, will be widely accepted as an international standard for general purposes of ornithology'. This turns out to have been a wish rather than a reality, for suddenly the study of the interrelationships, and hence the sequence of orders and families of birds, has found itself in such a turbulent state of development that at present nobody can foresee where it will all end. This has been caused not only by a general renewal of interest but also by the development of new methods, especially biochemical, a resurgence of morphological studies, and the discovery of new fossil material, with the additional stimulus of the availability of a deductive method known as Hennigian systematics or CLADISTICS (see also CLASSIFICATION). The use of chemical properties of egg-white proteins throughout the whole class of birds by Charles G. Sibley and collaborators, and of the other biochemical characters by other authors, has revolutionized basic and often traditional thoughts on relationships at the familial level (e.g, Sibley 1970, Sibley and Ahlquist 1972; cf. Voous 1980). The rapids turned into waterfalls after Sibley and his staff started to investigate chemical properties of the genetic material (DNA x DNA hybridization), the first results of which have recently been published and are summarized by Sibley and Ahlquist (1984). Particularlyenigmatic have become the relationships of passerine groups endemic to Australia and New Zealand at the generic, familial and nearordinal levels. Morphological studies on the bony stapes (ear-bone) in pre-, proto- and recent Passeriformes by Alan Feduccia (1975, 1977) have upset what had been thought well established ideas on the relationships among these birds, including the distinction between non-oscine and oscine songbirds. Careful study of new fossil material has led to noteworthy progress in the understanding of the relationships of certain groups, e.g. the Gruiformes.

K.H.

voous

NOTE: the publication of the Check-list of North American Birds 1983 (6th edn) came too late for all pertinent revisions to be incorporated in the articles, but some amendments were made in proof where practicable. (Eds). Bock, W.J. & Farrand, J. 1980. The number of species and genera of recent birds: a contribution to comparative systematics. Am. Mus. Novit. 2073: 1-29. Feduccia, A. 1975. Morphology of the bony stapes (columella) in the Passeriformes and related groups: evolutionary implications. Univ. Kansas Mus. Nat. Hist, Misc. Publ. 63: 1-34. Feduccia, A. 1977. A model for the evolution of perching birds. Syst, Zoo1. 26: 19-31. Mayr, E. & Greenway, J.C. 1956. Sequence of passerine families (Aves). Breviora, Mus. Compo Zoo1. 58: 1-11. Morony, J.J., Bock, W.J. & Farrand, J. 1975. Reference List of the Birds of the World. Am. Mus. Nat. Hist., New York. Sibley, C.G. 1970. A comparative study of the egg-white proteins of passerine birds. Bull. Peabody Mus. Nat. Hist. 32: 1-131. Sibley, C.G. & Ahlquist, J.E. 1972. A comparative study of the egg white proteins of non-passerine birds. Bull. Peabody Mus. Nat. Hist. 39: 1-276. Sibley, C.G. & Ahlquist, J.E. 1984. The phylogeny and classification of the passerine birds, based on comparisons of the genetic material, DNA. Proc. XVIII Int. Orn. Congr. Voous, K.H. 1973. List of recent holarctic bird species. Non-passerines, Ibis 115: 612-638. Voous, K.H. 1977. List of recent holarctic bird species. Passerines. Ibis 119: 223-250, 376-406. Voous, K.H. 1980. New developments in avian systematics: a summary of results. Proc. XVII Int. Orn. Congr.: 1232-1234. See also references under CLASSIFICATION.

Avian Anatomical Nomenclature Avian Anatomical Nomenclature (ICAAN). The Committee adopted the universally acceptable language of Latin, codifying prevailing usage of satisfactory names, doing away with duplicate terms and defining ambiguous ones. New names were produced where none were previously available or those in use were grossly defective. The terminology of NAA has generally been followed throughout this Dictionary and ornithologists are urged to employ it in their publications. The use of officialLatin anatomical terms will help to establish a standard avian terminology.

The recently published Nomina Anatomica Avium (Baumel et al 1979) is an annotated, illustrated anatomical dictionary of birds. It is a codification of the names for the anatomical parts of birds which was formulated and agreed upon by some 80 eminent avian scientists from around the world. NAA is the first such system of anatomical names to be developed for birds, even though mammalian models have long been in existence. Avian anatomy has suffered from a diversity of terminologies in the literature. Multiple and inappropriate names for the structures have caused confusion. NAA evolved during nearly a dozen years of discussion within the International Committee on

J.J. BAUMEL

x

Table of Classification

ORDER STRUTHIONIFORMES Suborder Struthiones Suborder Rheae Suborder Casuarii Suborder Apteryges

ORDER TINAMIFORMES

Families

Articles

Struthionidae Aepyomithidae (extinct) Rheidae Dromaiidae Casuariidae Dinomithidae (extinct) (incl.. Anomalopteryginae, Dinornithinae) Apterygidae

OSTRICH

Tinamidae

TINAMOU

ORDER PROCELLARIIFORMES

ELEPHANT-BIRD RHEA EMU CASSOWARY MOA

KIWI

PETREL

Diomedeidae Procellariidae Hydrobatidae Pelecanoididae

(AIbatross) (Shearwater) (Petrel) (Diving Petrel)

ORDER SPHENISCIFORMES

Spheniscidae

PENGUIN

ORDER GAVIIFORMES

Gaviidae

DIVER

ORDER PODICIPEDIFORMES

Podicipedidae

GREBE

Phaethontidae

TROPICBIRD

Sulidae Phalacrocoracidae Anhingidae Pelecanidae Fregatidae

GANNET

Ardeidae Scopidae Ciconiidae Balaenicipitidae Threskiomithidae

HERON; BITTERN

ORDER PHOENICOPTERIFORMES

Phoenicopteridae

FLAMINGO

ORDER ANSERIFORMES Suborder Anhimae Suborder Anseres

Anhimidae Anatidae

SCREAMER

ORDER PELECANIFORMES Suborder Phaethontes Suborder Pelecani Superfamily Suloidea

Superfamily Pelecanoidea Suborder Fregatae ORDER CICONIIFORMES Suborder Ardeae Suborder Scopi Suborder Ciconiae

I

xi

CORMORANT DARTER PELICAN FRIGATEBIRD

HAMERKOP STORK SHOEBILL IBIS; SPOONBILL

DUCK

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Table of Classification

ORDER CATHARTIFORMES ORDER ACCIPITRIFORMES Suborder Accipitres

Suborder Sagittarii ORDER FALCONIFORMES ORDER GALLIFORMES Suborder Galli

Cathartidae

VULTURE (2)

Accipitridae Pandionidae Sagittariidae

HAWK; VULTURE (1)

SECRETARY-BIRD

Falconidae

FALCON

Megapodiidae Cracidae Phasianidae

MEGAPODE

Tetraoninae, Odontophorinae Phasianinae Numidinae Meleagridinae Suborder Opisthocomi ORDER MESITORNITHIFORMES ORDER GRUIFORMES Suborder Turnices

Suborder Grues Superfamily Ralloidea Superfamily Gruoidea

Suborder Suborder Suborder Suborder Suborder

Heliornithes Rhynocheti Eurypygae Cariamae Otides

ORDER CHARADRIIFORMES Suborder Charadrii Superfamily Jacanoidea Superfamily Charadrioidea

Superfamily Thinocoroidea Superfamily Chionidoidea

HAWK

(Osprey)

CURASSOW

GROUSE PHEASANT GUINEAFOWL TURKEY

Opisthocomidae

HOATZIN

Mesitornithidae

MESITE

Turnicidae Pedionomidae

BUTTONQUAIL

Rallidae Aramidae Psophiidae Gruidae Heliornithidae Rhynochetidae Eurypygidae Cariamidae Otididae

jacanidae Rostratulidae Haematopodidae Ibidorhynchidae Recurvirostridae Dromadidae Burhinidae Glareolidae Charadriidae Scolopacidae Pluvianellidae Thinocoridae Chionidae

PLAINS-WANDERER

RAIL LIMPKIN TRUMPETER CRANE FINFOOT KAGU SUNBITTERN SERIEMA BUSTARD

JACANA PAINTED SNIPE OYSTERCATCHER IBISBILL AVOCET CRAB-PLOVER THICKKNEE COURSER; PRATINCOLE PLOVER (1) SANDPIPER; PHALAROPE MAGELLANIC PLOVER SEEDSNIPE SHEATHBILL

Table of Classification xiii

Suborder Lari

Suborder Alcae

Stercorariidae Laridae Stemidae Rynchopidae Alcidae

SKUA GULL TERN SKIMMER AUK

ORDER PTEROCLIDIFORMES

Pteroclididae

SANDGROUSE

ORDER COLUMBIFORMES

Columbidae Raphidae (Dodo, extinct) Pezophapidae (Solitaire, extinct)

DODO

ORDER PSITTACIFORMES

Psittacidae

PARROT

ORDER CUCULIFORMES Suborder Musophagae Suborder Cuculi

Musophagidae Cuculidae

CUCKOO

ORDER STRIGIFORMES

ORDER CAPRIMULGIFORMES Suborder Steatornithes Suborder Caprimulgi

ORDER APODIFORMES Suborder Apodi

Tytonidae Strigidae

Steatomithidae Podargidae Aegothelidae Nyctibiidae Caprimulgidae

PIGEON

TURACO

OWL

OILBIRD FROGMOUTH OWLET-FROGMOUTH POTOO NIGHTJAR

(Hemiprocnidae)

Hemiprocnidae Apodidae Trochilidae

SWIFT

ORDER COLIIFORMES

Coliidae

MOUSEBIRD

ORDER TROGONIFORMES

Trogonidae

TROGON

ORDER CORACIIFORMES Suborder Alcedines Superfamily Alcedinoidea Superfamily Momotoidea Superfamily Todoidea Suborder Meropes Suborder Coracii Superfamily Coracoidea

Alcedinidae Momotidae Todidae Meropidae

Suborder Trochili

Superfamily Leptosomatoidea Suborder Bucerotes Superfamily Phoeniculoidea Superfamily Bucerotoidea

Coraciidae Brachypteraciidae Leptosomatidae Phoeniculidae Upupidae Bucerotidae

SWIFT; SWIFTLET HUMMINGBIRD

KINGFISHER MOTMOT TODY BEE-EATER

ROLLER GROUND-ROLLER CUCKOO-ROLLER WOOD-HOOPOE HOOPOE HORNBILL

xiv

Table of Classification

ORDER PICIFORMES Suborder Galbulae Superfamily Galbuloidea Superfamily Capitonoidea

Suborder Pici

ORDER PASSERIFORMES Suborder Deutero-Oscines Infraorder Eurylaimi

Infraorder Furnarii

Infraorder Tyranni

Infraorder Pittae

Galbulidae Bucconidae Capitonidae Indicatoridae Ramphastidae Picidae

JACAMAR PUFFBIRD BARBET HONEYGUIDE TOUCAN WOODPECKER

Eurylaimidae Eurylaiminae Calyptomeninae Philepittidae Philepi ttinae Neodrepaninae

BROADBILL

Furnariidae Furnariinae Synallaxinae Philydorinae Dendrocolaptidae F ormicariidae Rhinocryptidae Cotingidae Pipridae Tyrannidae Elaeniinae FIuvicolinae Tyranninae Oxyruncidae Phytotomidae Pittidae

OVENBIRD (1)

ASITY

WOODCREEPER ANTBIRD; GNATEATER TAPACULO COTINGA MANAKIN FLYCATCHER (2)

SHARPBILL PLANTCUTTER PITTA

Suborder Oscines or Passeres

AUSTRALIAN AND NEW ZEALAND PRIMITIVE SPECIALISTS Scrub Birds and Lyrebirds Atrichomithidae Menuridae New Zealand Wrens Acanthisittidae

SCRUB-BIRD LYREBIRD

WREN (3)

ISOLATED GROUPS Larks

Alaudidae

LARK

Hirundinidae

SWALLOW

Swallows

Table of Classification

OLD WORLD INSECT EATERS AND RELATED FAMILIES Pipits and Wagtails

Motacillidae

WAGTAIL

Campephagidae Pycnonotidae Chloropseidae

CUCKOO-SHRIKE

Ptilogonatidae Bombycillidae Bornbycillinae Hypocoliinae Dulidae

SILKY FLYCATCHER

Cinclidae Troglodytidae Mimidae Prunellidae Turdidae Turdinae Enicurinae Sylviidae Sylviinae Polioptilinae Muscicapidae Rhipiduridae Monarchidae Pachycephalidae Timaliidae

DIPPER

Aegithalidae

TIT, LONG-TAILED

Maluridae Acanthizidae Acanthizinae Mohouinae Ephthianuridae Neosittidae Climacteridae

WREN (2)

Paridae Sittidae Tichodromadidae Certhiidae Remizidae

TIT

Rhabdomithidae Salpornithidae

CREEPER, PHILIPPINE

Bulbuls and Allies BULBUL LEAFBIRD

Waxwings and Allies

WAXWING HYPOCOLIUS PALMCHAT

Primitive Insect Eaters WREN (1) MOCKING-THRUSH ACCENTOR THRUSH

WARBLER (1); SILKTAIL GNATCATCHER FLYCATCHER (1) FANTAIL MONARCH FLYCATCHER THICKHEAD BABBLER; RAIL-BABBLER; PARROTBILL

Old Australian Endemics WARBLER, AUSTRALIAN

CHAT, AUSTRALIAN SITTELLA TREECREEPER (2)

Titmice, Nuthatches, and Treecreepers NUTHATCH WALLCREEPER TREECREEPER (1) PENDULINE TIT

Uncertain Status CREEPER, SPOTTED

xv

xvi

Table of Classification

Old World Nectar Eaters

Nectariniidae Dicaeidae Dicaeinae Pardalotinae Zosteropidae Promeropidae Meliphagidae

CROWS, BIRDS OF PARADISE AND RELATED FAMILIES Orioles, Shrikes and Allies Oriolidae Irenidae Laniidae Laniinae Malaconotinae Prionopidae Vangidae Pityriasididae Dicruridae Australian and New Zealand Crow-like Birds and Crows Callaeidae Grallinidae Corcoracidae Artamidae Cracticidae

SUNBIRD FLOWERPECKER

WHITE-EYE (1) SUGARBIRD HONEYEATER

ORIOLE (1) FAIRY-BLUEBIRD SHRIKE

HELMET-SHRIKE VANGA BRISTLEHEAD DRONGO

WATTLEBIRD (2) MAGPIE-LARK CHOUGH (2) WOOD-SW ALLOW BUTCHERBIRD (2); MAGPIE (2); CURRAWONG

Turnagridae Paradisaeidae Cnemophilinae Paradisaeinae Ptilonorhynchidae Corvidae

THRUSH, NEW ZEALAND BIRD-OF-PARADISE

BOWERBIRD CROW (1)

Starlings, Weaverbirds and Allies

Sturnidae Sturninae Buphaginae Passeridae Passerinae Plocepasserinae

STARLING OXPECKER

SPARROW (1) SPARROW-WEAVER AND SCALY-WEAVER

Ploceidae Bubalornithinae Ploceinae Estrildidae Viduidae

WEAVER

ESTRILDID FINCH WHYDAH (1)

Table of Classification

NINE-PRIMARIED ASSEMBLAGE Vireos

Vireonidae Cyclarhinae Vireolaniinae Vireoninae Finches and New World Insect Eaters, Fruit Eaters and Granivores Fringillidae Fringillinae Carduelinae Drepanididae Parulidae Coerebidae Thraupidae Thraupinae

PEPPER-SHRIKE SHRIKE-VIREO VIREO

FINCH; DARWIN'S FINCHES

HAWAIIAN HONEYCREEPER WARBLER (2) CONEBILL; BANANAQUIT TANAGER HONEYCREEPER FLOWERPIERCER SWALLOW-TANAGER

Catamblyrhynchinae Emberizidae Emberizinae Cardinalinae Icteridae

FINCH, PLUSH-CAPPED BUNTING CARDINAL GROSBEAK ORIOLE (2)

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List of Contributors Authorship of major articles is indicated by initials at the end of each contribution. Many articles which appeared in A New Dictionary of Birds have been substantially revised. In such instances the initials of the original author are within brackets followed by the initials of the revising author. In the case of minor revisions, the revisor's initials are within the brackets after those of the author.

AUTHORS D.G.A. T.A. R.McN.A. S.A. P.L.A. C.J.A. M.B.A. G.L.A.-W. P.J.B. A.S.B. J.C.B. C.J.B.(I) I.A.G.B. G.A.B. L.A.B. I·J.B. J.H.B. M.B. C.W.B. B.C.R.B. C·I·B.(2) M.E.B. T.R.B. C.R.B.

David G. Ainley, B.S. (Dickinson)., Ph.D. (Johns Hopkins). Point Reyes Bird Observatory, California, USA. PENGUIN (Pygoscelis). Thomas Alerstam, Fil.dr. (Lund). Department of Animal Ecology, University of Lund, Sweden. RADAR. Robert McNeill Alexander, M.A., Ph.D. (Cambridge), D.Sc. (Wales). Professor of Zoology, University of Leeds, England, LOCOMOTION, TERRESTRIAL. Salim Ali, Hon. D.Sc. (Aligarh, Delhi, Andhra). President, Bombay Natural History Society, Bombay, India. ORIENTAL REGION. Peter L. Ames, M.Sc., D.Phi!. (Yale). Senior Ecologist, Harza Engineering Co., Chicago, USA. SYRINX. Charles J. Amlaner, B.Sc., M.A. (Andrews University, Michigan), D.Phi!. (Oxford). Department of Biology, Walla Walla College, Washington, USA. RADIO TRACKING AND BIOTELEMETRY; SLEEP. Malte Borje Andersson, Ph.D. (Gothenburg). Department of Zoology, University of Gothenburg, Sweden. FOOD STORING. George Laidley Atkinson- Willes, Frocester, Gloucestershire, England. Organizer, National Wildfowl Counts 1950-1983. COUNT. Philip John Bacon, B.Sc. (Birmingham), D.Phil. (Oxford). Institute of Terrestrial Ecology, Merlewood, Cumbria, England. ROOSTING. Anne Susan Baker, B.Sc. (Newcastle upon Tyne). Department of Zoology, British Museum (Natural History), London, England. ECTOPARASITE (with T. Clay and A.M. Hutson). Jon C. Barlow, M.Sc., Ph.D. (Kansas), Curator, Department of Ornithology, Royal Ontario Museum; Professor of Zoology, University of Toronto, Canada. VIREO. Christopher John Barnard, B.Sc. (Liverpool), D.Phi!. (Oxford). Lecturer in Zoology, University of Nottingham, England. PIRACY. John Anthony Godsmark Barnes, M.A. (Oxford). President, Lancaster and District Bird-Watching Society, England. TIT. George A. Bartholomew. Professor of Biology, University of California, Los Angeles, USA. TORPIDITY. Leo Adrian Batten, B.Sc., Ph.D. (London). Ornithological Advisor, Nature Conservancy Council, Peterborough, England. CENSUS. Julian J. Baumel, Ph.D. (Florida). Professor of Anatomy, Creighton University, Nebraska, USA. HEART; LYMPHATIC SYSTEM; TAIL (with A.L. Thomson); VASCULAR SYSTEM. Jan Hendrik Beeking, M.Sc., D.Phil. (Leiden). Research Institute, Ministry of Agriculture and Fisheries, Wageningen, Netherlands. BROOD-PARASITISM; EDIBLE NESTS; EGGSHELL, ULTRASTRUCTURE OF; SWIFTLET. Marc Bekoff. Professor, University of Colorado, Boulder, USA. PLAY. Constantine W. Benson, O.B.E., M.A. Formerly Department of Zoology, Cambridge University, England. Died 1982. ASITY; MALAGASY REGION; MESITE; CUCKOO-ROLLER; GROUND-ROLLER; VANGA. Brian Colin Ricardo Bertram, B.A., Ph.D. (Cambridge). Curator of Mammals, Zoological Society of London, Regent's Park, London, England. OSTRICH. Colin J. Bibby, M.A., Ph.D. Senior Research Biologist, Royal Society for the Protection of Birds, Sandy, England. MEASUREMENT. Michael Edward Birkhead, B.Sc. (Newcastle upon Tyne) , D.Phi!. (Oxford). Formerly Post-Doctoral Fellow, Edward Grey Institute of Field Ornithology, University of Oxford, England. ACCENTOR. Timothy Robert Birkhead, B.Sc. (Newcastle upon Tyne) , D.Phil. (Oxford). Lecturer in Zoology, University of Sheffield, England. AUK. Charles Robert Blem, B.S. (Ohio), M.S., Ph.D. (Illinois). Professor of Biology, Virginia Commonwealth University, Richmond, USA. ENERGETICS. xix

xx

List of Contributors

J.H.R.B.

Jeffrey Hugh Richard Boswall. Producer, Natural History Unit, BBC, Bristol, England.

HUMAN IMITATION

OF BIRD SOUNDS; SOUND RECORDING; TOOLS, USE OF.

W.R.P.B. R.K.B. J.P.B.-L. A.B. M.D.B. D.B. D.M.B. H.B. P.J.K.B. E.J.M.B. W.A.C. B.C. R.C.(I) P.G.C. R.C.(2) R.J.S.C. C.K.C. A.S.C. C.A.J.C.

William Richmond Postle Bourne, M.A., M.B., B.Chir. (Cambridge). Honorary Research Fellow, Department of Zoology, University of Aberdeen, Scotland. OIL POLLUTION; PETREL. Richard K. Brooke. FitzPatrick Institute of African Ornithology, Cape Town, South Africa. OXPECKER (with W.R. Siegfried). John Philip Brooke-Little, C.V.O., K.St.J., M.A. (Oxford), F.S.A. Norroy and Ulster King of Arms, College of Arms, London, England. Chairman, Heraldry Society and Harleian Society; Hon Editor-inChief, The Coat of Arms. HERALDIC BIRDS. Andre Brosset, Dr.Sc. Director of Research, CNRS, Museum National d'Histoire Naturelle, Paris, France. MAMMALS, ASSOCIATION WITH. Murray Duncan Bruce. Turramurra, NSW, Australia. PITTA. Donald Bruning. Dr. Curator, Department of Ornithology, New York Zoological Society, New York, USA. BUTTONQUAIL. David Murray Bryant, B.Sc., Ph.D. (London). Senior Lecturer, Department of Biological Science, University of Stirling, Scotland. SWALLOW. Hans Bub. Vogelwarte Helgoland, Wilhelmshaven, Germany. AVOCET; IBISBILL. Philip John Kennedy Burton, B.Sc., Ph.D. (London). Principal Scientific Officer, British Museum (Natural History), Tring, England. HOMOLOGY; LEG; MUSCULATURE; SKULL; TONGUE; WOOD-SWALLOW (with B. E. Smythies). Edward John Mawby Buxton, M.A. (Oxford). East Tytherton, Wiltshire, England. Emeritus Fellow, New College, Oxford. OYSTERCATCHER; POETRY, BIRDS IN. William Alexander Calder III, B.S. (Georgia), M.S. (Washington State), Ph.D. (Duke). Professor of Ecology and Evolutionary Biology, University of Arizona, USA. SIZE. Bruce Campbell, O.B.E., Ph.D. (Edinburgh). Woodstock, Oxford, England. CONGRESSES (with A.L. Thomson); OOLOGY; NEST SITES, MAN-MADE (with D. E. Glue). Robert Carrick, B.Sc. (Glasgow), Ph.D. (Edinburgh). Dornoch, Scotland. Formerly Division of Wildlife Research, CSIRO, Australia. MAGPIE (2). Peter Guernsey Caryl, M.A., Ph.D. (Cambridge). Department of Psychology, University of Edinburgh, Scotland. AGGRESSION; AMBIVALENCE; RITUALIZATION. Richard Carrington. London, England. FABULOUS BIRDS. Richard J.S. Cassels, M.A. (Cambridge). Curator, Manawatu Museum, Palmerston North, New Zealand. MOA (with P.R. Millener). Clive Kenneth Catchpole, B.Sc., Ph.D. (Nottingham). Lecturer in Zoology, University of London, England. VOCALIZATION. Anthony Stephen Cheke, M.A. (Cambridge). Oxford, England. Leader BOU Mascarene Islands Expedition, 1973-75. DODO. Clifford A.J. Christie. Banbury Bird Hospital, Middleton Cheney, Oxon., England. CARE OF SICK, INJURED AND ORPHANED BIRDS.

T.C. M.H.C. N.J.C. N.E.C. C.T.C P.J.C.(I) F.C. C.J.F.C. J.C.(I)

Theresa Clay, B.Sc., D.Sc. (Edinburgh). London, England. Formerly Deputy Keeper, Department of Entomology, British Museum (Natural History). ECTOPARASITE (with A.M. Hutson and A.S. Baker). Mary Heimerdinger Clench, M.Sc., D.Phil. (Yale). Adjunct Curator of Birds, Florida State Museum, Gainesville, Florida, USA. PTERYLOSIS. Nigel James Collar, B.A. (Cambridge), Ph.D. (East Anglia). Compiler, International Committee for Bird Preservation, Cambridge, England. BUSTARD; CRANE. Nicholas Elias Collias, B.Sc., Ph.D. (Chicago). Professor of Zoology, University of California, Los Angeles, USA. SPARROW-WEAVER AND SCALY-WEAVER. Charles Thompson Collins, B.A. (Amherst College), M.S. (Michigan), Ph.D. (Florida). Professor of Biology, California State University, Long Beach, USA. SWIFT. Peter John Conder, O.B.E., Hon. M.A. (Open University). Cambridge, England. Formerly Director, Royal Society for the Protection of Birds, Sandy, Bedfordshire, England. BIRD-WATCHING. Fred Cooke, M.A., Ph.D. (Cambridge). Professor of Biology, Queen's University, Kingston, Ontario, Canada. HARDY-WEINBERG LAW; POLYMORPHISM. Charles John Franklin Coombs, M.A., M.B., B.Ch. (Cambridge). Truro, Cornwall, England. President, Cornwall Bird-Watching and Preservation Society. CROW. John Cooper, B.Sc. (London). Antarctic Research Officer, Percy FitzPatrick Institute, University of Cape Town, South Africa. PENGUIN (Spheniscus).

List of Contributors xxi

H.B.C.

Hugh Bamford Cott, D.Sc. (Glasgow), Sc.D. (Cambridge). Beaminster, Dorset, England. Formerly Lecturer in Zoology and Strickland Curator, University of Cambridge, England. COLORATION, ADAPTIVE;

j.C.C. j.C.(2)

John C. Coulson, D.Sc. Zoology Department, University of Durham, England. RED TIDE. Joel Cracraft, Dr. Department of Anatomy, University of Illinois at Chicago, USA. EARLY EVOLUTION

PALATABILITY OF BIRDS AND EGGS.

OF

BIRDS.

C. D.W.T.C.

T.M.C. j.P.C. P.J.C.(2) N.B.D. S.j.j.F.D. M.S.D. W.R.J.D. J.T.D. R.deN. P.J.D. A.W.D. H.J. de S.D. R.H.D. R.J.D. C.j.D. H.-R.D. E.K.D. R.F.D. j.D. C.E. E.E. H.F.I.E. j.A.E. M.D.E. J.T.E.

Earl of Cranbrook, M.A. (Cambridge), Ph.D. (Birmingham). Great Glemham, Suffolk, England. Formerly Senior Lecturer in Zoology, University of Malaya, Kuala Lumpur, Malaysia. GUANO, CAVE. David William Thomasson Crompton, M.A., Sc.D. (Cambridge). Lecturer in Parasitology, University of Cambridge, England, and Adjunct Professor, Division of Nutritional Sciences, Cornell University, New York, USA. ALIMENTARY SYSTEM; DROPPINGS. Timothy Michael Crowe, B.A. (Mass/Boston), M.Sc. (Chicago), Ph.D. (Cape Town). Senior Research Officer, FitzPatrick Institute, University of Cape Town, Rondebosch, South Africa. GUINEAFOWL. John Patrick Croxall, B.A. (Oxford), Ph.D. (Auckland). Head, Birds and Mammals Section, British Antarctic Survey, Cambridge, England. ANTARCTIC; PENGUIN. Peter James Curry, B.Sc. (Wales), M.Agr.Sc. (Melbourne). Rangeland Management Branch, Department of Agriculture, South Perth, W.A., Australia. EMU. Nicholas Barry Davies, M.A. (Cambridge), D.Phil. (Oxford). Department of Zoology, University of Cambridge, England. FLYCATCHER (1); TERRITORY; WAGTAIL. Stephen John James Frank Davies, B.A., Ph.D. (Cambridge). Director, Royal Australasian Ornithologists' Union, Moonee Ponds, Victoria, Australia. BUTCHER-BIRD (2); CASSOWARY; CURRAWONG; NEST FUNCTION. Marian Stamp Dawkins, B.A., D.Phil. (Oxford). Fellow, Somerville College, University of Oxford, England. SEARCH IMAGE. William Richard John Dean. Associate Member, Transvaal Museum, South Africa. ORIOLE (1). Jean Theodore Delacour, Lie. Sci. (Lille and Paris). In charge of the Zoological Survey of French Indochina 1923-1940. Director Los Angeles County Museums 1951-1966. Cleres, France. PHEASANT (with M.W. Ridley). Rene de Naurois, M.C., Hon. Professor, Universite Libre de Toulouse; Correspondant du Museum National d'Histoire Naturelle, Paris, France. KAGU (with I-No Neyrolles). Pierre J. DeviUers, Ph.D. Institut Royal des Sciences Naturelles de Belgique, Bruxelles, Belgium. GULL. Antony William Diamond, B.A. (Cambridge), M.Sc., Ph.D. (Aberdeen). Canadian Wildlife Service, Ottawa, Canada. AFROTROPICAL REGION; HONEYGUIDE; MOUSEBIRD. Henry John de SufJren Disney, M.A. (Cambridge). Berowra, NSW, Australia. Formerly Curator of Birds, The Australian Museum, Sydney, Australia. RAIL-BABBLER; THICKHEAD (both with L.G. Grimes). Richard H. Donaghey, B.Sc. (Sydney), M.Sc. (Alberta), Ph.D. (Monash). Burnie Technical College, Tasmania, Australia. BOWERBIRD (with C.B. Frith, A. Lill). Robert Joseph Dooling, B.Sc. (Omaha, NE, USA), D.Phil. (St. Louis, Mo, USA). Associate Professor, Psychology Department, University of Maryland, College Park, MD, USA. HEARING AND BALANCE. Christopher John Duncan, B.Sc., Ph.D. (London). Professor of Zoology, University of Liverpool, England. SMELL. Hans-Rainer Duncker, Dr. rer. nat. (Kiel), Dr. med. (Hamburg). Professor of Anatomy, Institute of Anatomy and Cell Biology, justus-Liebig-University, Giessen, Germany. RESPIRATORY SYSTEM. Euan Kennedy Dunn, B.Sc. (Aberdeen), Ph.D. (Durham). Editor, 'Birds of the Western Palearctic'. Oxford, England. CONTROL (3); TERN. Roger F. Durman. Balerno, Midlothian, Scotland. OBSERVATORY, BIRD. Jan Dyck, Cand.polyt. and mag.scient. (Copenhagen). Reader, Institute of Population Biology, University of Copenhagen, Denmark. FEATHER; PLUMAGE. Carl Edelstam, Ph.D. (Stockholm). Curator of Vertebrates, Swedish Museum of Natural History, Stockholm, Sweden. MIMICRY. Eugene S.B. Eisenmann. Formerly Research Associate, American Museum of Natural History, New York, USA. Died 1982. TROGON. Sir Hugh F.I. Elliott, Bt., O.B.E., M.A. (Oxford). Oxford, England. Overseas Civil Service (Tanganyika) 1937-1961; President BOU 1975-1979. FINFOOT. John A. Endler, B.A. (Berkeley, California), Ph.D. (Edinburgh). Professor of Biology, University of Utah, Salt Lake City, USA. SPECIATION; SPECIES. M. Derrick England, O.B.E. Late of Norwich, England. Died 1980. BARBET. Jonathan Thor Erichsen, B.A. (Harvard), D.Phil. (Oxford). Research Assistant Professor, Department of

xxii List of Contributors

Neurobiology and Behavior, State University of New York, Stony Brook, New York, USA.

IRIS

COLORATION; VISION.

P.R.E. S.M.E. ].B.F. C.I.F.

A.F.

Peter Richard Evans, M.A., Ph.D. (Cambridge), D.Phil. (Oxford). Reader in Estuarine Ecology, Department of Zoology, University of Durham, England. MIGRATION; MOULT; PLOVER (1). Stewart Martin Evans, B.Sc., Ph.D. (Bristol). Senior Lecturer, Department of Zoology, University of Newcastle upon Tyne, England. DOMINANCE (2). J. Bruce Falls, Dr. Department of Zoology, University of Toronto, Canada. PLAYBACK. Christopher John Feare, B.Sc., Ph.D. (Leeds). Ministry of Agriculture, Fisheries and Food, Worplesdon, Surrey, England. CRAB-PLOVER; PESTS, BIRDS AS; STARLING. Alan F. Feduccia, B.Sc. (Louisiana State), M.Sc., D.Phil. (Michigan). Professor and Associate Chairman, Department of Biology, University of North Carolina, Chapel Hill, USA. FLIGHTLESSNESS; OVENBIRD (1); WOODCREEPER.

I.].F.-L. P.N.F. R.S.R.F. B.M.F. I·W.F.

].].M.F.

Ian James Ferguson-Lees. Rode, Bath, England. Formerly Executive Editor, BritishBirds; Past President, British Trust for Ornithology. BITTERN; TREE CREEPER (1). Peter Norman Ferns, B.Sc. (Manchester), Ph.D. (Exeter). Senior Lecturer, Zoology Department, University College, Cardiff, Wales. YAWNING. Richard Sidney Richmond Fitter, B.Sc. (Econ.) (London). Chairman, Fauna and Flora Preservation Society, London, England. Chairman Steering Committee, Species Survival Commission, International Union for Conservation of Nature. NATURALIZED BIRDS. Brian Michael Fitzgerald, B.Sc. (New Zealand), M.Sc. (Canterbury), Ph.D. (Berkeley, California). Ecology Division, Department of Scientific and Industrial Research, Lower Hutt, New Zealand. WREN (3). John W. Fitzpatrick, B.A. (Harvard), Ph.D. (Princeton). Head, Division of Birds, Field Museum of Natural History, Chicago, Illinois, USA. FLYCATCHER (2). James J.M. Flegg, B.Sc. Ph.D., A.R.C.S. (Imperial College). Head of Zoology Department, East MaIling Research Station, Kent, England. Formerly Director, British Trust for Ornithology. NUMBERS; ORNITHOLOGICAL SOCIETIES; ORNITHOLOGY.

C.A.F. B.K.F. H.A.F. E.T.B.F. C.B.F. H.].F. C.H.F. R.W.F.

Sir Charles Alexander Fleming, K.B.E., D.Sc. (New Zealand), F.R.S. Research Associate, National Museum of New Zealand, Wellington, New Zealand. THRUSH, NEW ZEALAND. Brian Keith Follett, B.Sc., Ph.D. (Bristol), D.Sc. (Wales), F.R.S. Professor of Zoology, University of Bristol, England. ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM (with A.R. Goldsmith). Hugh A. Ford, Ph.D. Professor of Zoology, University of New England, Armidale, N.S.W., Australia. AUSTRALASIAN REGION (with D.L. Serventy); HONEY EATER (with F. Salomonsen). Eric Thomas Brazil Francis, B.Sc. (London), Ph.D. (Reading). Formerly Reader in Vertebrate Zoology, Sheffield University, England. EXCRETORY SYSTEM. Clifford Brodie Frith. Ornithologist and photographer, Paluma via Townsville, Queensland, Australia. BIRD-OF-PARADISE; BOWERBIRD (with R.F. Donaghey, A. Lill); SILKTAIL. Harry J. Frith, D.Sc. Agr. (Sydney). Formerly Chief, Division of Wildlife Research, CSIRO, Canberra, Australia. Died 1982. MEGAPODE; PLAINS-WANDERER. Charles Hilary Fry, M. A. (Cambridge), Ph.D. (Ahmadu Bello). Senior Lecturer in Zoology, University of Aberdeen, Scotland. BEE-EATER; HOOPOE; KINGFISHER; ROLLER. Robert William Furness, B. Sc., Ph. D. (Durham). Lecturer in Zoology, University of Glasgow, Scotland. SKUA.

I.C.].G. E.F·I·G. P·I·G.(l)

A·I·G.

Ian Courtney Julian Galbraith, M.A. (Oxford). Head of Sub-department of Ornithology, British Museum (Natural History), Tring, England. MUSEUM. Ernest Francis John Garcia, B.Sc. (London), D.Phi!. (Oxford). Head of Biology Department, George Abbot County Secondary School, Guildford, England. WARBLER (1). Peter Jeffrey Garson, B.Sc. (Edinburgh), D.Phil. (Oxford). Lecturer, Zoology Department, University of Newcastle upon Tyne, England. WREN (1). Anthony J. Gaston, B.A., D.Phil. (Oxford). Canadian Wildlife Service, Ottawa, Canada. BABBLER; CO-OPERATIVE BREEDING; TIT, LONG-TAILED.

M·I·G. F.B.G. D.E.G. A.R.G.

Michael John Gentle, B.Sc., Ph.D. (London). Principal Scientific Officer, Poultry Research Centre, Roslin, Midlothian, Scotland. TASTE. Francis B. Gill, B.Sc., Ph.D. (Michigan). Curator of Ornithology, Academy of Natural Sciences, Philadelphia, Pa. USA. SUNBIRD. David Edward Glue, B.Sc. (London). Nest Record Officer, British Trust for Ornithology, Tring, England. NEST SITES, MAN-MADE (with B. Campbell); PELLET. Arthur Richard Goldsmith, B.Sc. (Wales), Ph.D. (Leicester). SERC Advanced Fellow, Department of Zoology, University of Bristol, England. ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM (with B.K. Follett).

List of Contributors xxiii

D.G. A.F.G.

Derek Goodwin, Petts Wood, Kent, England. Formerly Principal Scientific Officer, British Museum (Natural History). PIGEON. Arthur Frederic Gotch. Late of West Wittering, Chichester, Sussex, England. Died 1983. NAMES, SCIENTIFIC.

P.R.G. R.E.G. J.J.D.G. P.J.G.(2)

Peter Raymond Grant, B.A. (Cambridge), Ph.D. (British Columbia). Professor of Biological Sciences, University of Michigan, USA. DARWIN'S FINCHES. Rhys E. Green, Dr. Royal Society for the Protection of Birds, Sandy, England. LARK. Jeremy John Denis Greenwood, B.A. (Oxford), Ph.D. (Manchester). Lecturer in Biological Sciences, University of Dundee, Scotland. EVOLUTION; NATURAL SELECTION; SEXUAL SELECTION. Paul John Greenwood, M.A. (Cambridge), M.Sc. (Durham), D.Phil. (Sussex). Lecturer in Zoology, Department of Adult and Continuing Education, University of Durham, England. DISPERSAL; FREQUENCY DEPENDENT SELECTION.

L.G.G. T.C.G. A.G. J.L.G.

Llewellyn George Grimes, B.Sc., Ph.D. (Bristol), M.Sc. (Aberdeen). Warwick, England. BULBUL (with A.I. Ivanov); HELMET-SHRIKE; HORNBILL (with A.C. Kemp); SHRIKE; WEAVER; RAIL-BABBLER; THICKHEAD (both with H.J. de S. Disney); TURACO (with D.A. Turner). Thomas Christman Grubb, Jr., B.A. (Swarthmore), M.A., Ph.D. (Wisconsin). Professor, Department of Zoology, Ohio State University, Columbus, Ohio, USA. WEATHER AND BIRDS. Alfredo Guillet, Dott. (Torino). Percy FitzPatrick Institute of African Ornithology, University of Cape Town, S. Africa. SHOEBILL (with A.L. Thomson). James L. Gulledge. Director, Library of Natural Sounds, Cornell University, Ithaca, New York, USA. MOCKING-THRUSH.

E.G. J.H. W.G.H. J.M.H.-C. T.R.H. N.H.H. C.J.O.H. J.G.H.

Eberhard Gwinner, Dr. rer. nat. Professor, Head of Vogelwarte fur Verhaltensphysiologie, Federal Republic of Germany. RHYTHM AND TIME MEASUREMENT. Jiirgen HafIer, Dr. rer. nat. (Gottingen), Petroleum Geologist, Exploration Manager, DEMINEX Egypt Branch, Cairo (Central Office: Essen, West Germany). GEOLOGICAL FACTORS. William G. Hale, Ph.D.. Professor of Biology, Liverpool Polytechnic, England. SANDPIPER. Joan Margaret Hall-Craggs (nee Johnston), L.R.A.M. (Perfs.), Sub-Department of Animal Behaviour, University of Cambridge, England. MUSIC, BIRDS IN (with R.E. Iellis). Timothy Richard Halliday, M.A., D.Phil. (Oxford). Senior Lecturer in Biology, The Open University, Milton Keynes, England. ENDANGERED BIRDS. Nicholas H. Hammond. Head of Publications, Royal Society for the Protection of Birds, Sandy, Bedfordshire, England. ILLUSTRATION, BIRD. Colin James Oliver Harrison, Ph.D. (Reading). Sub-Department of Ornithology, British Museum (Natural History), Tring, England. PLUMAGE, ABNORMAL. Jeffrey Graham Harrison, M.B., B.Chir. (Cambridge). Late of Sevenoaks, Kent, England. Died 1978. LEG; (TONGUE); WING.

P.H.T.H. F.H. K.J.H. R.A.H. G.J.M.H. D.G.H. E.J.H. D.C.H. R.W.H.

The Venerable Peter Harold Trahair Hartley, M.A. (Oxford), B.Sc. (London). Framlingham, Suffolk, England. FEEDING HABITS; PREDATION. Francois Haverschmidt, M.A. (Utrecht). Omen, Netherlands. POTOO; TRUMPETER. Kenneth J. Hill, D.V.Sc., M.R.C.V.S. Unilever Research, Bedford, England. EXCRETION, EXTRARENAL. Robert Aubrey Hinde, D.Phil. (Oxford), Sc.D. (Cambridge), F.R.S. Royal Society Research Professor and Honorary Director of the M.R.C. Unit on the Development and Integration of Behaviour, Madingley, Cambridge, England. COPULATION; COURTSHIP FEEDING; DISPLAY; NEST BUILDING; PAIR FORMATION. Graham James Michael Hirons, B.Sc. (Wales), D.Phil. (Oxford). Hartley Research Fellow, Department of Biology, University of Southampton, England. RODING. Dominique G. Homberger, Dr Phil. II (Zurich). Associate Professor, Department of Zoology and Physiology, Louisiana State University, Baton Rouge, Louisiana, USA. PARROT. Eric J. Hosking, O.B.E., F.R.P.S., F.I.I.P. London, England. PHOTOGRAPHY (with G.K. Yeates.) David Charles Houston, B.Sc. (Bristol), D.Phii. (Oxford). Lecturer, Department of Zoology, University of Glasgow, Scotland. VULTURE (1). Robert William Hudson. Research Officer, British Trust for Ornithology, Tring, England. RANGE CHANGES.

H.G.H. A.M.H.

K.I.

Henry George Hurrell, M.A. (Cambridge). Late of South Brent, Devon, England. Died 1981. DIPPER. Anthony Michael Hutson. Formerly in Department of Entomology, British Museum (Natural History), London, England. ECTOPARASITE (with T. Clay and A.S. Baker). Klaus Immelmann, Dr. rer. nat. (Mainz). Professor of Biology, Department of Ethology, University of Bielefeld, W. Germany. BEHAVIOUR, DEVELOPMENT OF; ESTRILDID FINCH.

xxiv

List of Contributors

I.R.I. A.I.I.

J.}.

Ian R. Inglis, B.Sc. (London), Ph.D. (Bristol). Principal Scientific Officer, Ministry of Agriculture, Fisheries and Food, Worplesdon, Surrey, England. SCARING. Alexandr Ivanovich Ivanov, S.D. (Leningrad). Professor. Curator of Birds, Zoological Institute, Leningrad, USSR. BULBUL (with L.G. Grimes). jurgen Jacob, Dr. rer. (Bonn). Professor (Hamburg); Director (Biochemistry Division) Institute for Environmental Carcinogens, Ahrensburg, and Zoological Institute, University of Hamburg, W. Germany. OIL GLAND.

O.}.}.

OUi Juhani Jarvinen, M.Sc., D.Phil. (Helsinki). Professor of Zoology, University of Helsinki, Finland.

}.R.}.

Joseph R. Jehl jr., A.B. (Cornell), Ph.D. (Michigan). Assistant Director, Hubbs-Sea World Research Institute, San Diego, California, USA. MAGELLANIC PLOVER. Rosemary Elston Jellis, M.A. (Oxford). Late Senior Producer, British Broadcasting Corporation. Died 1983. MUSIC, BIRDS IN (with }.M. Hall-Craggs). Donald A. jenni, B.S. (Oregon State), M.S. (Utah State), Ph.D. (Florida). Professor of Zoology, University of Montana, Missoula, USA. JACANA. Arthur Ramsden Jennings, M.A. (Cambridge), D.V.Sc. (Liverpool), M.R.C.V.S. Connel, Argyll, Scotland. DISEASE. Paul Austin johnsgard, B.S. (North Dakota State), M.S. (Washington State), Ph.D. (Cornell). Foundation Professor of Life Science, University of Nebraska, Lincoln, USA. GROUSE. Eric Lionel Jones, B.A. (Nottingham), M.A., D .Phil. (Oxford). Professor, School of Economics, La Trobe University, Victoria, Australia. UTILIZATION BY MAN. Peter J. Jones, Ph.D. (Oxford). Department of Forestry and Natural Resources, University of Edinburgh, Scotland. CROP MILK; HEAT REGULATION; ITINERANT BREEDING; METABOLISM; NUTRITION; QUELEA CON-

DISTRIBUTION, GEOGRAPHICAL.

R.E.}. D.A.}.

A.R.}. P.A.}. E.L.}. P.}.}.

TROL.

G.C.A.}. }.K.(I) }.A.K. A.C.K. R.K. R.E.K. A.K.K. C.B.K. }.K.(2)

A.G.K. }.R.K. }.A.K. L.L. J.H.L. I.L.

George Christoffel Alexander Junge, D.Sc. (Amsterdam). Formerly Curator of Birds, Rijksmuseum van Natuurlijke Historie, Leiden, Netherlands. Died 1962. NIGHTJAR (with J. Marshall). Janet Kear, B.Sc. (London), Ph.D. (Cambridge). Assistant Director, Wildfowl Trust, Martin Mere, Lancashire, England. FLAMINGO; FOOD SELECTION; ODOUR. James Allen Keast, B.Sc., M.Sc. (Sydney), M.A., Ph.D. (Harvard). Professor of Biology, Queen's University, Kingston, Ontario, Canada. ADAPTATIONS, ENVIRONMENTAL. Alan Charles Kemp, B.Sc., Ph.D. (Rhodes). Head, Department of Birds, Transvaal Museum, Pretoria, South Africa. HORNBILL (with L.G. Grimes); SECRETARY-BIRD. Robert Kennedy. Department of Zoology, Washington State University, USA. CREEPER, PHILIPPINE (with R. Orenstein). Robert Eyres Kenward, B.A., D.Phil. (Oxford). Institute of Terrestrial Ecology, Furzebrook, Dorset, England. FALCONRY. Angela Kay Kepler, B.A. (Canterbury, New Zealand), M.S. (Hawaii), Ph.D. (Cornell). Kula, Hawaii, USA. TODY. Cameron Bradford Kepler, B.A., M.A. (California), Ph.D. (Cornell). Biologist-in-charge, Maui Field Station, Patuxent Wildlife Research Center, US Fish and Wildlife Service, USA. HAWAIIAN HONEYCREEPER. Jiro Kikkawa, D.Sc. (Kyoto). Professor of Zoology, University of Queensland, Australia. WHITE-EYE (1). Alan Glasgow Knox, B.Sc., Ph.D. (Aberdeen). Sub-Department of Ornithology, British Museum (Natural History), Tring, England. KERATIN. John Richard Krebs, M.A., D.Phil. (Oxford), F.R.S. Lecturer, Edward Grey Institute of Field Ornithology, University of Oxford, England. E.P. Abraham Fellow in Zoology, Pembroke College, Oxford. BEHAVIOUR, HISTORY OF; and COUNTING; IMPRINTING; LEARNING; MIMICRY, VOCAL (with W.H. Thorpe). James A. Kushlan, B.S., Ph.D. (Miami). Adj. Associate Professor, University of Miami, Coral Gables, Florida, USA. HERON. Lionel Lambourne, B.A. (Nottingham). Assistant Keeper, Department of Paintings, Victoria and Albert Museum, London, England. ART, BIRDS IN. John Hartley Lawton, B.Sc., Ph.D. (Durham). Reader in Biology, University of York, England.

ECOLOGY.

Ingvar Lennerstedt, Fil.dr. (Lund, Sweden). Department of Zoology, University of Lund, Sweden.

FOOT

PAPILLAE AND PADS.

}.D.L.

A.L.

J. David Ligon, B.Sc. (Oklahoma), D.Phil. (Michigan). Professor, Department of Biology, University of New Mexico, Albuquerque, New Mexico, USA. WOOD HOOPOE. Alan Lill, B.Sc. (Bristol), Ph.D. (Edinburgh). Senior Lecturer, Departments of Psychology and Zoology, Monash University, Australia. BOWERBIRD (with R.F. Donaghey, C.B. Frith); LYREBIRD.

List of Contributors

H.L.

Hans Lohrl, Dr. phil. (Munchen). Egenhausen, West Germany. Formerly Vogelwarte Radolfzell. NUTHATCH; WALLCREEPER.

R.L.

Rosemary Low. Deputy Editor, 'Cage and Aviary Birds'. New Barnet, Herts, England.

AVICULTURE; CAGE

BIRD.

J.C.McL. G.L.M.

John Charles McLachlan, B.Sc. (Glasgow), Ph.D. (London). Lecturer, Department of Anatomy and Experimental Pathology, University of St. Andrews, Scotland. DEVELOPMENT, EMBRYONIC. Gordon Lindsay Maclean, B.Sc., Ph.D. (Rhodes), D.Sc. (Natal). Professor, Department of Zoology, University of Natal, Pietermaritzburg, South Africa. COURSER; DRINKING; PRATINCOLE; SANDGROUSE; SEEDSNIPE.

R.McN. P.H.M.-B.

Raymond McNeil, B.Sc., M.Sc., Ph.D. (Montreal). Director, Centre de recherches ecologiques de Montreal, Universite de Montreal, Canada. FOOTEDNESS. Sir Philip Henry Manson-Bahr, C.M.G., D.S.O., M.D. (London). Died 1966. England. Formerly Chairman, British Ornithologists' Club, and Vice-President, British Ornithologists' Union. MECHANICAL SOUNDS.

S.M. M.B.M. J.M. L.D.M. G.V.T.M. E.M. C.J.M. H.M. P.R.M. C.D.T.M. D.W.M. N.W.M. R.A.M.

Stephen Marchant, B.A. (Cambridge). Moruya, NSW, Australia. NEST. Miles Berkeley Markus, B.Sc., M.Sc. (Pretoria), M.Sc., D.I.C., Ph.D. (London). Professor, Department of Zoology, University of the Witwatersrand, Johannesburg, South Africa. FEATHERS, NUMBER OF. Joe T. Marshall, Jr. Division of Birds, U.S. National Museum, Washington DC, USA. NIGHTJAR (with G.C.A. Junge). Larry Dean Martin, B.S., M.S. (Nebraska), Ph.D. (Kansas). Curator, Vertebrate Paleontology, Museum of Natural History, and Professor, Systematics and Ecology, University of Kansas, Lawrence, Kansas, USA. ARCHAEOPTERYX. Geoffrey Vernon Townsend Matthews, M.A., Ph.D. (London). Deputy Director, Wildfowl Trust, Slimbridge, Gloucester, England. HOMING PIGEON; NAVIGATION. Ernst Mayr, Ph.D. (Berlin). Alexander Agassiz Professor Emeritus, Museum of Comparative Zoology, Harvard University, Cambridge, Mass., USA. NEARCTIC REGION; NEOTROPICAL REGION. Christopher John Mead, M.I.Biol. Head of Ringing and Migration Section, British Trust for Ornithology, Tring, England. AGE; PENDULINE TIT; WING FORMULA; WING SPAN. Heimo Mikkola, Ph.D. (Kuopio). M.Sc. (Oulu), D.Phii. (Kuopio). Fisheries Specialist, Africa Development Bank, Ivory Coast, Africa. OWL. Philip R. Millener, B.Sc., Ph.D. (Auckland). National Museum of Natural History, Smithsonian Institution, Washington DC, USA. MOA (with R.J.S. Cassels). Clive D.T. Minton, Ph.D. IMI Australia, Melbourne, Australia. TRAPPING. Douglas Wayne Mock, B.S. (Cornell), M.S., Ph.D. (Minnesota). Associate Professor, Department of Zoology, University of Oklahoma, Norman, Ok, USA. COLONIALITY. Norman Wilfred Moore, M.A. (Cambridge), Ph.D. (Bristol). Swavesey, Cambridge, England. Formerly Chief Advisory Officer, Nature Conservancy Council. HABITAT; TOXIC CHEMICALS. Robert Andrew Morgan, B.Sc. (Wales). British Antarctic Survey, Madingley Road, Cambridge, England. NEST RECORDS; THICKKNEE.

D.H.M. G.M. J.B.N. LN.

J-N.N. R.J.O'C. J.C.O.

Douglas Hathaway Morse, B.S. (Bates College), M.S. (Michigan), Ph.D. (Louisiana State). Professor of Biology and Chairman, Section of Population Biology and Genetics, Brown University, Providence, Rhode Island, USA. FLOCKING. Guy Mountfort, O.B.E. Lyndhurst, Hants, England. Past President B.O.U. BILL. Joseph Bryan Nelson, B.Sc. (St. Andrews), D.Phil. (Oxford). Reader in Zoology, University of Aberdeen, Scotland. GANNET; GUANO. Ian Newton, B.Sc. (London), D.Phil., D.Sc. (Oxford). Institute of Terrestrial Ecology, Monks Wood, Abbots Ripton, Huntingdon, England. FALCON; FINCH; HAWK; IRRUPTIONS. Jean-Noel Neyrolles. Paris, France. KAGU (with R. De Naurois). Raymond Joseph O'Connor, B.Sc. (National University of Ireland), D.Phil. (Oxford). Director, British Trust for Ornithology, Tring, England. BIOSTATISTICS; EGG; GROWTH; PARENTAL CARE; and DEVELOPMENT, EMBRYONIC (Embryonic thermoregulation). John C. Ogden. Senior Staff Scientist, Condor Research Center, Ventura, California, USA. IBIS; SPOONBILL; STORK; VULTURE (2).

R.O.

Ronald Isaac Orenstein, B.Sc., M.Sc. (Toronto), Ph.D. (Michigan), LL.B. (Toronto). Canada. CREEPER, (with R. Kennedy); CREEPER, SPOTTED; ELEPHANTBIRD; EXTINCT BIRDS; SITTELLA; TREE(with D.L. Serventy). Gordon H. Orians, B.S. (Wisconsin), Ph.D. (UC, Berkeley). Director, Institute for Environmental Studies, and Professor of Zoology, University of Washington, Seattle, Washington, USA. ORIOLE (2).

PHILIPPINE CREEPER (2)

G.H.O.

xxv

xxvi List of Contributors

M.O. R.S.P. S.A.P. K.C.P. D.T.P. C.P. R.B.P.

Myrfyn Owen, B.Sc. (Wales), Ph.D. (Leeds). Assistant Director (Research), The Wildfowl Trust, Slimbridge, Gloucestershire, England. WILDFOWL. Ralph S. Palmer, B.A. (Maine), Ph.D. (Cornell). Research Associate, Smithsonian Institution, Washington, DC, USA. CARDINAL GROSBEAK; COLOUR STANDARDIZATION; LIMPKIN. Shane Alwyne Parker, B.Sc. (Adelaide). Curator of Birds, South Australian Museum, Adelaide, South Australia. CHAT, AUSTRALIAN; FANTAIL; MONARCH FLYCATCHER; WARBLER, AUSTRALIAN; WREN (2). Kenneth Carroll Parkes, B.Sc., M.Sc., Ph.D. (Cornell). Chief Curator, Life Sciences, and Curator of Birds, Carnegie Museum of Natural History, Pittsburgh, Pennsylvania, USA. WARBLER (2). David Thomas Parkin, B.Sc. (Durham), Ph.D. (Manchester). Senior Lecturer, Department of Genetics, University of Nottingham, England. GENETICS. Colin Patterson, B.Sc., Ph.D. (London). Senior Principal Scientific Officer, Department of Palaeontology, British Museum (Natural History), London, England. CLADISTICS. Robert Berkeley Payne, B.S. (Michigan), Ph.D. (University of California, Berkeley). Museum of Zoology and Division of Biological Sciences, University of Michigan, Ann Arbor, Michigan, USA. CUCKOO; WHYDAH (1).

C.J.P. C.M.P. D.E.P. A.P. W.F.P. I.P. J.P. R.P.P.-J. E.P. J.D.P. D.A.R. J.M.V.R.

Colin James Pennycuick, M.A. (Oxford), Ph.D. (Cambridge). Maytag Professor of Ornithology, University of Miami, Florida, USA. FLIGHT. Christopher Miles Perrins, B.Sc. (London), D.Phii. (Oxford). Director, Edward Grey Institute of Field Ornithology, University of Oxford, England. BREEDING SEASONS; CLUTCH-SIZE. Derek Edmund Pomeroy, M.A. (Cambridge), Ph.D. (Adelaide). Professor of Zoology, Makerere University, Uganda. BILL ABNORMALITIES. Adolf Portmann, Ph.D. (Basel), Dr. h.c. (Aix-Marseille; Freiburg i Br.). Formerly Professor, Director, Zoological Institute, University of Basel, Switzerland. HATCHING (with W.H. Stingelin). William Frank Porter, B.A. (Northern Iowa), M.S., Ph.D. (Minnesota). Associate Professor, Department of Environmental and Forest Biology; Director, Adirondack Ecological Center, State University of New York, Syracuse, New York, USA. PARTHENOGENESIS; TURKEY. Ian Prestt, M.Sc., (Liverpool), F.I. BioI. Director, Royal Society for the Protection of Birds, Sandy, Bedfordshire, England. CONSERVATION. Jesu Prevost, Ph.D. Professor, Faculty of Sciences, University of Limoges, France. PENGUIN (Aptenodytes). Robert Parton Prys-jones, B.Sc. (Nottingham), D.Phii. (Oxford). Research Officer, Percy FitzPatrick Institute of African Ornithology, University of Cape Town, Rondebosch, South Africa. BUNTING. Erkki Pulliainen, Ph.D. Professor of Zoology, University of Oulu, Finland. WAXWING. John David Pye, B.Sc. (Wales), Ph.D. (London). Professor of Zoology, School of Biological Sciences, Queen Mary College, Mile End Road, London, England. ECHOLOCATION; (MECHANICAL SOUNDS). Derek Almey Ratcliffe, B.Sc., D.Sc. (Sheffield), Ph.D. (Wales). Chief Scientist, Nature Conservancy Council, Peterborough, England. EGGSHELL THINNING. Jeremy Mark Verrinder Rayner, M.A., Ph.D. (Cambridge). Department of Zoology, University of Bristol, England. FLIGHT, SPEEDS OF.

R.E.R.

Reginald Elson Rewell, M.D. (London), M.R.C.P. Formerly Pathologist, Zoological Society of London, England. BLOOD.

J.F.R.

John Frank Reynolds, M.A. (Oxford). Head of Biology, Rastrick Grammar School, Yorkshire, England. BELLY-SOAKING.

A.S.R. M.R.

Andrew Stephen Richford, B.Sc. (Edinburgh), D.Phii. (Oxford). London, England. PAINTED SNIPE. Mark Ridley, M.A., D.Phii. (Oxford). New College, Oxford. ALTRUISM; E.S.S.; FACILITATION, POSTURAL; FACILITATION, SOCIAL; FITNESS; SEXUAL DIMORPHISM; SOCIOBIOLOGY.

M.W.R. S.D.R.

The Hon. Matthew White Ridley, B.A., D.Phii. (Oxford). Science editor, The Economist, London, England. PHEASANT (with J.T. Delacour). S. Dillon Ripley, K.B.E., Sc.D. Secretary, Smithsonian Institution, Washington, DC, USA. RAIL; THRUSH.

R.B.R. I.C.R.R. F.S. L.S.

Richard B. Root, B.S. (Michigan), Ph.D. (Berkeley). Professor, Section of Ecology and Systematics,

Cornell University, Ithaca, New York, USA. GNATCATCHER.

Ian Cecil Robert Rowley, B.Agr.Sci. (Melbourne). Senior Principal Research Scientist, CSIRO, Helena Valley, Western Australia. CHOUGH (2). Finn Salomonsen, Ph.D. (Copenhagen). Formerly Keeper of Bird Department, Zoological Museum, Copenhagen, Denmark. Died 1983. FLOWERPECKER; HONEYEATER (with H.A. Ford). Luc Schifferli, Lie. Zool. (Basel, Switzerland), D.Phii. (Oxford). Schweizerische Vogelwarte (Swiss Ornithological Institute), Sempach, Switzerland. GRIT.

List of Contributors xxvii

R.P.S. J.S. D.K.S. P.S. D.L.S. J.T.R.S. L.L.S.

Roberto Pablo Schlatter, Med. Vet. (U. de Chile, Santiago), Ph.D. (Johns Hopkins, USA). Professor, Institute of Zoology, Faculty of Sciences, Universidad Austral de Chile, Valdivia, Chile. PLANTCUTTER. J. SchwartzkopfI, Professor Dr. Ruhr-Universitat Bochum, Germany. TOUCH. Dafila Kathleen Scott, B.A. (Oxford), Ph.D. (Cambridge). Scientist at the Wildfowl Trust, Welney, Norfolk, England. RECOGNITION, INDIVIDUAL. Sir Peter Markham Scott, K.B.E., D.S.C., M.A. (Cambridge). Founder and Director, Wildfowl Trust, Slimbridge, Gloucestershire, England. DECOY; DUCK; GAMEBIRDS. Dominick Louis Serventy, B.Sc. (W. Australia), Ph~D. (Cambridge). Formerly Principal Research Officer, CSIRO Division of Wildlife Research, Nedlands, Western Australia. AUSTRALASIAN REGION (with H.A. Ford); FROGMOUTH; OWLET-FROGMOUTH; TREECREEPER (2) (with R. Orenstein). John Timothy Robin Sharrock, B.Sc., Ph.D. (Southampton). Managing Editor, 'British Birds', Blunham, Bedford, England. ATLAS. Lester LeRoy Short, B.Sc., D.Phil. (Cornell). Chairman and Curator, Ornithology Department, American Museum of Natural History, and Professor, City University of New York, USA. HYBRID; HYBRIDIZATION, ZONE OF SECONDARY; INTROGRESSION; WOODPECKER.

A.S. C.G.S.

Aharon Shulov, D.Sc. Nat. (Naples). Emeritus Professor of Zoology, Hebrew University of Jerusalem, Israel. Founder and first Director of Jerusalem Biblical Zoological Garden. BIBLE, BIRDS OF THE. Charles Gald Sibley, Ph.D. (California). William Robertson Coe Professor of Ornithology; Curator of Birds, Peabody Museum of Natural History, Yale University, New Haven, Conn. USA. DNA AND PROTEINS AS SOURCES OF TAXONOMIC DATA.

H.S.

Helmut Sick, Ph.D. (Berlin). Academia Brasileira de Ciencias, Rio de Janeiro, Brazil. CURASSOW;

HOATZIN;

SERIEMA; TAPACULO; TINAMOU.

W.R.S. K.E.L.S. S.S. A.F.S.

Walter Roy Siegfried, B.Sc., Ph.D. (Cape Town). Director, Percy FitzPatrick Institute of African Ornithology, University of Cape Town, Rondebosch, South Africa. HAMERKOP; OXPECKER (with R.K.Brooke); SUGARBIRD. Kenneth Edwin Laurence Simmons, M.Sc., Ph.D. (Bristol). Honorary Visiting Fellow, Department of Psychology, University of Leicester, England. ANTING; COMFORT BEHAVIOUR; DISTRACTION BEHAVIOUR; DUSTING; GREBE; SMOKE BATHING; SUNNING, and PARENTAL CARE (Protection of eggs). Sverre Sjolander, Dr. Zoologiska Institutionen, University of Stockholm, Sweden. DIVER. Alexander Frank Skutch, A.B., Ph.D. (Johns Hopkins University). San Isidro de El General, Costa Rica. JACAMAR; MOTMOT; PUFFBIRD; SHRIKE-VIREO; SILKY-FLYCATCHER; SUNBITTERN; TANAGER; TOUCAN.

T.S. P.J.B.S. G.T.S. N.G.S.

Tore Slagsvold, D.Phil. Zoologisk Avdeling, University of Trondheim, Norway. NEST SITE SELECTION. Peter James Bramwell Slater, B.Sc., Ph.D., D.Sc. (Edinburgh). Professor of Natural History, University of St. Andrews, Scotland. DISPLACEMENT ACTIVITY. Graeme Talbot Smith, B.Sc., Ph.D. (ANU). Senior Research Scientist, Division of Wildlife and Rangeland Research, CSIRO, Midland, Western Australia. SCRUB-BIRD. Neal Griffith Smith, D.Phil. (Cornell). Smithsonian Tropical Research Institute, Balboa, Panama. NESTING ASSOCIATIONS; SHARPBILL.

B.E.S. B.S.

Bertram Evelyn Smythies, B.A. (Oxford). Merstham, Surrey, England. Formerly Forest Service in Burma and Sarawak. CUCKOO-SHRIKE; WOOD-SWALLOW (with P.J.K. Burton). Barbara Katherine Snow, B.Sc. (Reading). Wingrave, Bucks, England. Formerly of Trinidad. HUMMINGBIRD.

D.W.S.(l)

David William Snow, M.A., D.Phil., D.Sc. (Oxford). Wingrave, Bucks, England. Formerly Senior Principal Scientific Officer, British Museum (Natural History). BANANAQUIT; CHARACTER DISPLACEMENT; COEVOLUTION; CONEBILL; COTINGA; FINCH, PLUSH-CAPPED; HONEYCREEPER; HYPOCOLIUS; LEK; MANAKIN; MATING SYSTEM; OILBIRD; PEPPER-SHRIKE; POLYANDRY; POLYGYNY; SEED DISPERSAL; SWALLOW-TANAGER.

E.J.L.S.

E.J. Lawson Soulsby, M.A. (Cambridge), Ph.D., M.R.C.V.S., D.V.S.M. (Edinburgh). Professor of Animal Pathology and Head, Department of Clinical Veterinary Medicine, University of Cambridge, England. ENDOPARASITE.

R.S.

Robert Spencer, B.A., M.Sc. (Durham). Cockermouth, Cumbria, England. Formerly head of Ringing and Migration Section, and Director of Services, British Trust for Ornithology, Tring, England. MARKING.

D.W.S.(2)

David William Steadman, B.Sc. (Edinboro State College), M.Sc. (Florida), D.Phil. (Arizona). Research Associate, Division of Birds, Smithsonian Institution, Washington, DC, USA. FOSSIL BIRDS. Werner Hugo Stingelin, Ph.D. (Basel). Zoological Institute, University of Basel, Switzerland. HATCHING (with A. Portmann). Bernard Stonehouse, B.Sc. (London), M.A., D.Phil. (Oxford). Scott Polar Research Institute, Cambridge, England. FRIGATEBIRD; SHEATHBILL; TROPICBIRD.

W.H.S.

B.S.

xxviii

List of Contributors

R.W.S. }.G.S. D.S.-S.

Robert W. Storer, A.B. (Princeton), M.A., Ph.D. (California). Professor of Zoology and Curator of Birds, Museum of Zoology, University of Michigan, Ann Arbor, Michigan, USA. SWIMMING AND DIVING. Joseph G. Strauch, Jr. Ph.D. Adjoint Curator, University Museum (Zoology), University of Colorado, USA. SKELETON, POST-CRANIAL. James Denis Summers-Smith, B.Sc. (Glasgow), Ph.D. (Reading). Guisborough, Cleveland, England. SPARROW (1).

A.L.T.

W.H.T.

N.T. S.R.T.

Sir (Arthur) Landsborough Thomson, C.B., D.Sc. (Aberdeen). President XI Orne Int. Congr., Basel 1954. Editor, A New Dictionary of Birds, 1964. London, England. Died 1977. AVES; CONGRESSES (with B. Campbell); CROCODILE-BIRD; FAMILY; NAME, ENGLISH; NOCTURNAL HABITS; NOMENCLATURE; TAIL (with }.}. Baumel); SHOEBILL (with A. Guillet); TAMENESS; TAXONOMY; TOPOGRAPHY; YOUNG BIRD. William Homan Thorpe, M.A., Ph.D., Sc.D. (Cambridge), F.R.S. Emeritus Profesor of Animal Ethology, University of Cambridge, England; Past President, British Ornithologists' Union; Past President, Association for the Study of Animal Behaviour. COUNTING; IMPRINTING; LEARNING (all with} .R. Krebs); (MIMICRY, VOCAL). Nikolaas Tinbergen, Ph.D. (Leiden), M.A. (Oxford), F.R.S. Oxford, England. Formerly Professor of Experimental Zoology, University of Leiden, Netherlands; Formerly Reader in Animal Behaviour, University of Oxford, England. RECOGNITION; REDIRECTION; SIGN STIMULUS. Susan Rhonda Tingay, B.A. (Adelaide), Ph.D. (Western Australia). Stoneville, West Australia. MAGPIELARK.

L.T. S.G.T. D.A.T. G.E.S.T. E.K.U. G.F.v.T. H.G.V. K.H.V. F.V. }.W. K.E.W. M.W.W. D.R.W.

Ludwik Tomialoic, B.Sc., Dr., Dr. habil. (Wroclaw). Museum of Natural History, University ofWroclaw, Poland. URBANIZATION. Stephen Graham Tullett, B.Sc., Ph.D. (Bath). Senior Scientific Officer, Department of Reproductive Physiology, Agricultural and Food Research Council's Poultry Research Centre, Roslin, Midlothian, Scotland. INCUBATION; LAYING. Donald Arthur Turner. East African Natural History Society, Nairobi, Kenya. TURACO (with L.G. Grimes). Geoffrey Eric Slade Turner, M.A. (Oxford). Formerly Secretary, Science Area Delegacy, University of Oxford, England. Died 1984. (FOLKLORE); (OMENS, BIRDS AS); ORNAMENTATION, BIRDS IN HUMAN. Emil Karl Urban, B.Sc., Ph.D. (Wisconsin), M.A. (Kansas). Professor and Chairman, Department of Biology, Augusta College, Augusta, Georgia, USA. PELICAN. Gerard Frederick van Tets, B.A., M.A., Ph.D. (British Columbia). Principal Research Scientist, CSIRO Division of Wildlife and Rangelands Research, Canberra, Australia. CORMORANT; DARTER. Henry Gwynne Vevers, M.B.E., M.A., D.Phil. (Oxford). Formerly Assistant Director of Science, The Zoological Society of London, England. COLOUR. Karel Hendrik Voous, D.Sc. (Amsterdam). Emeritus Professor of Systematic Zoology and Zoogeography, Free University, Amsterdam; Formerly Deputy Director, Zoological Museum, University of Amsterdam, Netherlands. CLASSIFICATION; ORDER; PALEARCTIC REGION. Francois Vuilleumier, Lie. es sciences naturelles (Geneva), Ph.D. (Harvard). Curator, Department of Ornithology, American Museum of Natural History, New York, USA. ZOOGEOGRAPHY. John Warham, B.Sc. (Durham), Ph.D. (New Zealand). Reader, Department of Zoology, University of Canterbury, Christchurch, New Zealand. PENGUIN (Eudyptes). Keith Edward Webster, B.Sc., Ph.D., M.B., B.S. (London). Professor of Anatomy, King's College, University of London, England. NERVOUS SYSTEM. Milton W. Weller, A.B., M.A., D.Phil. (Missouri). Professor, Caesar Kleberg Chair in Wildlife Ecology, Texas A & M University, College Station, Texas, USA. SCREAMER. David R. Wells, Ph.D. (Malaya). Department of Zoology, University of Malaya, Kuala Lumpur, Malaysia. BROADBILL; FAIRY-BLUEBIRD; LEAFBIRD.

G.R.M.

E.O.W.

Gordon R. Williams, B.Sc. (Sydney), M.Sc. (New Zealand), Ph.D. (Canterbury). Formerly Professor of Entomology, Lincoln College, Canterbury, New Zealand, and Director of New Zealand Wildlife Service. Died 1983. KIWI. Edwin O'Neill Willis, B.S. (Virginia Polytechnic Institute), M.S. (Louisiana State), Ph.D. (California). Professor Colaborador, Departamento de Zoologia, Universidade Estadual Paulista, Sao Paulo, Brazil. ANTBIRD.

R.F.W.

Raffael Felix Winkler, Dr. Phil. (Basel). Curator of Birds, Natural History Museum, Basel, Switzerland. PNEUMATIZATION OF BONE.

L.L.W. M.W.

Larry Louis Wolf, B.S. (Michigan), Ph.D. (California). Professor, Department of Biology, Syracuse University, Syracuse, NY, USA. POLLINATORS. Martin Wedgwood Woodcock. Staplehurst, Kent, England.

DRONGO; PARROTBILL.

List of Contributors

D.G.M.W.-G. E.N.W. V.C.W.-E. G.K.Y. V.Z. R.L.Z.

David Grainger Marcus Wood-Gush, B.Sc. (Rand), Ph.D. (Edinburgh). Honorary Professor, Edinburgh School of Agriculture, University of Edinburgh, Scotland. DOMESTICATION. Ernest Nuttall Wright, B.Sc. (Birmingham). Head of Mammals and Birds, Ministry of Agriculture, Fisheries and Food, Worplesdon, Surrey, England. REPELLENTS, CHEMICAL. Vero Copner Wynne-Edwards, D.Sc. (Oxford), F.R.S. Torphins, Aberdeenshire, Scotland. Emeritus Professor of Natural History, University of Aberdeen, Scotland. OCEANIC BIRDS; PHALAROPE. George Kirkby Yeates, B.A. (Oxford). Harrogate, Yorkshire, England. PHOTOGRAPHY (with E.J. Hosking). Vinzenz Ziswiler, D.Phil. Zoolog Museum d'Universitat, Zurich, Switzerland. PALATE. Richard Laurence Zusi. B.A. (Northern University), M.Sc. (Michigan). Curator of Birds, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA. SKIMMER.

Additional authors whose articles in A New Dictionary of Birds (1964) have been revised, sometimes extensively, in the present work. D. Amadon (Starling); R.J. Andrew (Behaviour, Development of); E.A. Armstrong (Folklore, Birds in; Wren (1)); D.A. Bannerman (Wood Hoopoe); I.P. Barclay-Smith (Oil Pollution); A. d'A. Bellairs (Palate; Skeleton, Post-Cranial; Skull); E.R. Blake (Oriole (2)); H.J. Boyd (Swimming and Diving); L.H. Brown (Falcon; Flamingo; Hawk); Prof. A.J. Cain (Genetics; Natural Selection); Prof. Sir G. de Beer (Archaeopteryx); H.G. Deignan (Parrotbill); E.A.R. Ennion (Trapping); Prof. P.G. 'Espinasse (Feather); R.A. Falla (Moa); J. Fisher (Extinct Birds); J .A. Gibb (Nest Site Selection); Prof. F. Goldby (Nervous System); J.W.D. Goodall (Plantcutter); J.C. Greenway, Jr. (Palmchat); F. Gudmundsson (Diver); F.N. and F. Hamerstrom (Grouse); J.M. Harrison (Moult; Plumage); T.H. Harrison (Edible Nests; Omens, Birds as); W.C.O. Hill (Musculature); D. Lack (Swift); J.D. Macdonald (Museum); Colonel R. Meinertzhagen (Crab-plover; Grit; Palearctic Region; Piracy); Prof. A.H. Miller (Mocking-thrush); R.E. Moreau (Oriole (2); Weaver; White-eye (1)); R.C. Murphy (Guano); Prof. R.J. Pumphrey (Hearing and Balance); A.L. Rand (Bird-of-paradise; Cuckoo-roller; Mesite; Vanga); B.B. Roberts (Antarctic); A.G.O'C. Scott (Falconry); E.R. Sutter (Buttonquail); K. Tansley (Vision); R.O. Tudor (Art, Birds in); E.G. Turbott (Wren (3)); C. Vaurie (Bunting); U. Weidmann (Laying); A. Wetmore (Seriema); A.N. Worden (Alimentary System).

ARTISTS

Arlott, N.A., Norfolk, England Burton, P.J.K., Hertfordshire, England Busby, J., East Lothian, Scotland Coombs, C.J.F., Cornwall, England Cusa, N.W., Norfolk, England Gillmor, R., Berkshire, England Harris, A., Essex, England Kikkawa, N., Queensland, Australia Payne, K., Michigan, USA

Pearson, B., Bedfordshire, England Scott, Sir Peter, Gloucestershire, England Shackleton, K., London, England Talbot-Kelly, C.E., London, England Thelwell, D.A., Hampshire, England Watson, D., Kirkcudbrightshire, Scotland Wood, K.J., Surrey, England Woodcock, M., Kent, England Yule, M., Lancashire, England

PHOTOGRAPHERS

Andreev, A.V., USSR Becking, Dr J.H., Wageningen, Netherlands Bottomley, J.B. & S., Cornwall, England British Antarctic Survey, Cambridge, England

Buchanan, I., Oxfordshire, England Burton, Jane, Surrey, England Carlson, K., Norfolk, England Carlson, Dr R.J., Norfolk, England

xxix

xxx List of Contributors

Chandler, Dr R.J., Kent, England Christiansen, A., Copenhagen, Denmark Croxall, Dr J.P., Cambridge, England Grenfell, H.E., Swansea, Wales Harper, W.G., Edinburgh, Scotland Holliday, M., Humberside, England Hosking, D., London, England Hosking, E.J., London, England Huseby, B. Konnerud, Norway Jehl, Dr J.R. Jr., California, USA Karavaev, A.A., USSR Knystautas, Dr A., Vilnius, Lithuanian SSR Krechmar, A.V., USSR Maclean, Prof. G.L., Natal, South Africa Moffett, A.T., Staffordshire, England Moon, G., Auckland, New Zealand Munsterman, P., Haarlem, Netherlands Omelko, M.A., USSR

Pennycuick, Prof. C.J., Florida, USA Polking, F., Greven, Germany Pop, R., Vlaardingen, Netherlands Prevost, Prof. J., Limoges, France Rankin, N. (deceased) Reynolds, Dr J.F., Yorkshire, England Rue, L.L. Jr., New Jersey, USA Schouten, H., Haarlem, Netherlands Shibnev, V.B., USSR Shiota, T., Osaka, Japan Siokhin, V., USSR Swanberg, Dr P.O., Falkoping, Sweden Taylor, J., Berkshire, England van Swelm, N., The Hague, Netherlands van Tets, Dr G.F., Canberra, Australia Warham, Dr J., Christchurch, New Zealand Wood, Dr M.S. (deceased) Zonfrillo, B., Glasgow, Scotland

A ABDOMEN: the 'belly', being the part of the body containing the excre-

tory, reproductive, and main digestive organs (see ALIMENTARY SYSTEM; ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM; EXCRETORY SYSTEM); applied also to the ventral surface of the same region (see TOPOGRAPHY).

ABDUCTOR: see MUSCULATURE. ABMIGRATION: an anomalous migratory movement of a particular

type (see MIGRATION).

ABNORMALITIES: see BILL ABNORMALITIES;

PLUMAGE, ABNORMAL.

ABRASION: the effect of wear on the vane of a feather, involving some reduction of the tips of the barbs or their barbules; where these tips are coloured differently from the rest of the vane, their loss may substantially change the pattern and hue of the plumage generally (see PLUMAGE). ABUNDANCE: see NUMBERS. ACANTHISITTIDAE: a family of PASSERIFORMES, suborder Oscines; alternative name for the Xenicidae; see WREN

(3).

ACANTHIZIDAE; ACANTHIZINAE: a family and subfamily of PASSERIFORMES,

suborder Oscines;

WARBLER, AUSTRALIAN.

ACCENTOR: former generic name used as substantive for most species of Prunellidae (Passeriformes, suborder Oscines); in plural, general term for the family, which comprises 12 species placed in the single genus Prunella. Characteristics. They are small birds (14-18 em) with rufous or brownish-grey upperparts, streaked in most species; and with greyish underparts, usually marked in places with rufous. The general size and appearance are like those of a sparrow Passer, but the bill is more slender and pointed. The sexes are similar in plumage but males have longer wings and are heavier. Anatomically the Prunellidae have the fringillid character of a true crop and a muscular gizzard, adapted to a diet of seeds at some seasons. Their systematic position among the Oscines had been long debated, but recent evidence from DNA-hybridization indicates that they are closest to the ploceine weavers (see DNA AND PROTEINS AS SOURCES OF TAXONOMIC DATA). (Sibley and Ahlquist 1981). Distribution and habitat. The family is exclusively Palearctic, widely distributed from western Europe to Japan. The Alpine Accentor P. collaris is the most widespread species, its disjunct occurrence in high mountains having resulted in the evolution of many races; 8 subspecies are currently recognized. The Himalayan Accentor P. himalayana breeds as high as 5,000 m. The Robin Accentor P. rubeculoides is also found at high altitudes in central Asia, showing a preference for dwarf rhododendrons and other scrub, or for willows and sedges in damp meadows. The Siberian Accentor P. montanella breeds in the Siberian mountains and also along the lower courses of the Siberian rivers well north of the Arctic Circle. The best-known species, the Dunnock (formerly Hedge Sparrow) P. modularis, breeds mainly in mountains in central and eastern Europe, but is a familiar bird of gardens and cultivation, as well as woodland and scrub, in the west. Movements. Some accentors are migratory, while others move to lower altitudes in winter. The Dunnock is sedentary in mild parts of its range, migratory in the north, and makes altitudinal movements in mountains. Food. Accentors are unobtrusive ground feeders, often creeping about with a mouse-like action. They are mainly insectivorous in summer, and in winter subsist largely on seeds. In winter quarters some accentors regularly forage in flocks. Behaviour. The Dunnock, the only species investigated in detail, has a complex and highly variable social organization (Birkhead 1981; Davies and Lundberg 1984, Snow and Snow 1982). Female ranges are largely

exclusive. Males set up song territories in spring and compete to monopolize females. Depending on their ability to monopolize one or more females, the resulting mating systems range from polygyny (a male with two or three females) through simple pairs to polyandry (a female with two or three males) or even 'polygynandry' (several males associated with several females). The commonest mating systems are pairs and 'trios' (a female with two males). When two males share a female, one is dominant and the other subordinate. The dominant male guards the female closely, and the subordinate male mayor may not succeed in mating. Only if he does, does he help in feeding the young. The likelihood that a similar social system may occur in other species is suggested by the report of two males and a female feeding the young in an Alpine Accentor nest (Dyrcz 1977). The Dunnock's precopulatory display and method of mating are most unusual. The male pecks the female's cloaca for up 2 minutes before mating, which he does with extraordinary rapidity, jumping towards her at a slight angle and making cloacal contact for only a fraction of a second. During the precopulatory display the female's cloaca makes strong pumping movements and sometimes, at least, she ejects a small droplet of sperm. The male is very interested in the droplet, looks at it, and then immediately copulates. In view of the complex mating system, often including polyandry, this display may have evolved because it increases the male's chances of paternity (Davies 1983). From the little evidence available it seems that the Alpine Accentor's mating behaviour is similar. Voice. The Dunnock has a complex song consisting of a succession of rapid modulated notes and trills. Males include in their songs extensive passages copied exactly from their neighbours. Females very occasionally sing. The Alpine Accentor has a longer song of similar structure and regularly sings in flight. Other calls include sharp high-pitched alarm and contact notes (Dunnock) and a rippling trill (Alpine Accentor). Breeding. The nest, built by the female, is an open cup of plant fragments and moss, lined with hair, wool or feathers, and placed in low tree branches, shrubs, rock crevices, or on the ground. The 3-6 unmarked eggs range from blue to light bluish green. Two or three broods are normal for the Dunnock, two for the Alpine Accentor. Incubation is by the female alone in the Dunnock, but both sexes are reported to incubate in the Alpine Accentor. The incubation and fledging periods are each about 12-13 days in the Dunnock, but probably average somewhat longer in the high montane species. M.E.B. Birkhead, M.E. 1981. The social behaviour of the Dunnock. Ibis 123: 75-84. Davies, N.B. 1983. Polyandry, cloaca-pecking and sperm competition in Dunnocks. Nature 302: 33~336. Davies, N .B. & Lundberg, A. 1984. Food distribution and a variable mating system in the dunnock, Prunella modularis. J. Anim. Ecol. 53: 895-912. Dyrcz A. 1977. Nest-helpers in the Alpine Accentor Prunella collaris. Ibis 119: 215. Sibley, C.G. & Ahlquist, J.E. 1981. The relationships of the accentors (Prunella) as indicated by-DNA-DNA hybridization. J. Orne 122: 369-378.

Dunnock Prunella modularis. (D. W.).

2

Accidental

Snow, B.K. & Snow, D.W. 1982. Territory and social organization in a population of Dunnocks Prunellamodularis. J. Yamashina Inst. Orn. 14: 281-292. Snow, D.W. & Snow, B.K. 1983. Territorial song of the Dunnock Prunella modularis. Bird Study 30: 51-56.

ACCIDENTAL (SPECIES): see VAGRANT. ACCIPITER: sometimes used in North America as a vernacular term for Accipiter spp., 'hawk' having there a wider connotation than in Britain (see HAWK).

ACCIPITRES: alternative ordinal or subordinal name (see ACCIPITRIFORMES).

ACCIPITRIDAE: see ACCIPITRIFORMES;

HAWK.

ACCIPITRIFORMES: an order, alternatively'Accipitres' , comprising 2 suborders: Accipitres, Sagittarii; 3 families: Accipitridae (HAWK), Pandionidae (OSPREY), Sagittariidae (SECRETARY-BIRD). The order is a cosmopolitan one and contains all birds-of-prey in the strict sense, such as hawks, kites, harriers and eagles, but not the cathartid vultures (see VULTURE (2) and the falcons and caracaras (see FALCONIFORMES). The Old World vultures, sometimes treated as Aegypiinae, are included in the Accipitridae, whereas the Osprey Pandum haliaetus is given family rank Pandionidae, as in Wetmore's system. All species are generally characterized by hooked beak and sharp curved claws, used as talons in seizing living prey. The large number of species have developed an astonishingly wide ecological radiation and an impressive variety of wing shapes and flight methods, depending on habitat and hunting techniques. The order includes the largest known fossil and Recent flying land birds, some of the former with enormous wingspan. Food ranges from small insects to relatively large terrestrial and arboreal mammals, such as small deer, sloths, and monkeys. Some have turned to feeding on carcasses of large ungulates, others to plant material including oily fruits. ACCLIMATION: the process of adjusting to changed environmental circumstances, often with respect to temperature. Often used as a synonym of acclimatization but strictly refers to experimentally induced changes whilst the latter term is appropriate to natural change. ACETABULUM: the hollow in the pelvic girdle, on each side, into which the head of the femur fits (see SKELETON, POST-CRANIAL). ACQUIRED CHARACTERS: those arising during the life of the individual as the result of environmental or functional influences, as distinct from those expressing genetic constitution (see EVOLUTION; NATURAL SELECTION).

ACROMION: anterior projection of the scapula (see SKELETON,

POST-

CRANIAL).

ACROMYODI: see PASSERIFORMES. ACROPODIUM: the dorsal surface of the toes. ACROTARSAL: pertaining to the anterior surface of the tarsus. ACUTIPLANTAR: having the hinder aspect of the tarsus coming to an angle (applied to oscine Passeriformes); opposite of LATIPLANTAR (in general, see LEG). AD APTATI0 N: the production of fitness for a particular function, the term being also applied to a character (structure, behaviour, etc.) specially providing such fitness (see EVOLUTION; NATURAL SELECTION). 'Adaptive radiation' denotes divergence in the characters of related forms that enables them to exploit different kinds of opportunity. 'Convergence' denotes the adaptation of unrelated forms to similar functions, often giving rise to superficial resemblance (see CONVERGENCE). The term 'preadaptation' is used in cases where, coincidentally, a character existed in advance of the opportunity to which it proved particularly suited. ADAPTATIONS, ENVIRONMENTAL: the production of fitness for particular functions.

The make-up of the bird, especially warm-bloodedness and capacity for flight, pre-adapt it for certain ways of life, ecological roles, life-zones, and habitats. Warm-bloodedness and feathery insulation permit birds to thrive at high latitudes and altitudes, fly annually to exploit habitats thousands of kilometres apart, utilize temporary habitats, as well as patchily distributed resources, and feed at different levels. Many seeming adaptations are thus really pre-adaptations. Every aspect of the bird's life is adaptive: adaptations to the physical environment, habitat, prey and predators, and other bird species. Adaptations to the various aspects of reproduction alone are bewildering in their diversity and complexity. In this broad review it is not possible to cite the cross references involved. Within the avian framework some of the most important adaptations to different living areas involve modification to the annual cycle: the more or less stereotyped annual sequence of breeding-moulting-outward migration-moulting-return migration-breeding. Basically the annual cycle is structured around reproduction in the spring, this usually being the time of optimum food resources. In those parts of the world with significant annual day-length changes, breeding is initiated by the changing photoperiod, a threshold being passed in the lengthening process that, via the pituitary pathway, triggers enlargement of the reproductive organs. Other phases of the annual cycle, moulting and migration, are also linked in most species to the changing photoperiod. Each phase of the annual cycle represents a major energy drain on the bird, and may be the basis of adaptive modification. Breeding entails the setting up and defence of territory, courtship, nest-building, incubation, and the raising of the young. The moult (Payne 1972) represents the massive replacement of the body and flight feathers. Migration (Berthold 1975)may entail flights of thousands of kilometres: it is characteristically preceded by the laying down of layers of body fat (premigratory fat) to be used as fuel during the flight. Breeding and moulting are almost invariably sequential and do not overlap. In high latitude breeding species the former commonly occupies 4-8 weeks. Erratic and unpredictable environments may necessitate modifications to the control and timing of breeding and moulting (Serventy 1971; Immelmann 1971). For example, in the interior of Australia breeding may be linked with rainfall, and only partly to the photoperiod. In such an environment, when conditions are optimal for only a brief period, there may be some overlap of breeding and moulting, and moulting may be very protracted so that it never represents a major energy-drain (Keast 1968). Migration is, of course, very much a feature of the higher latitudes and altitudes. Whilst in most species the moult precedes migration, in a minority it is post-migratory. Presumably in such cases better resources are available in the wintering ground; or it is advantageous to leave the breeding grounds early. An alternative to the north-south (or south-north) migration of the higher latitude birds is the seasonal nomadism found in many inhabitants of warmer savanna and desert areas. Nomadism is a more random form of seasonal movement than 'true' migration and is of shorter amplitude. It brings the birds to areas where resources improve seasonally (e.g. winter rainfall areas, areas of fruiting or flowering), with the end point of the movement varying somewhat from year to year. Nomadic journeys may have a directional component (as in some African hawks and Australian interior birds) so that whether a movement be regarded as nomadic or migratory is a matter of choice. Presumably nomadic movements are usually less demanding on the bird than a 1,000km migratory journey. There may be one, or two, moults. Most bird species have only one, the 'complete' moult of late summer or early autumn. This post-reproductive moult entails a complete replacement of the flight, tail, and contour feathers. In a minority of species, mostly those with distinct breeding plumages, there is a prenuptial moult that is partial, involving the body feathers only. These different patterns of moulting are doubtless adaptive. Just as some races of species, but not others, are migratory so there may, or may not, be a prenuptial moult. The component parts of the avian annual cycle are under neurendocrine control. As yet, however, despite intensive research, most of the finer control mechanisms remain unknown. The control of breeding (and of the various aspects of breeding behaviour) is well understood, but the same is not true of the moult. Whilst the thyroid is clearly linked to the moult in many species, in others this link is much less clear-cut. Little is known of the antagonistic/synergistic effects of the hormones on the pituitary, reproductive organs, and thyroid, in the control of the moulting process.

Afrotropical Region 3

The link between hormones and migration is also inadequately understood. Species inhabiting extreme environments often share common adaptations to those environments. Those of Arctic birds include migration, heavy body insulation, and sometimes white winter plumage. The small minority of species that over-winter in the far north commonly avoids freezing by spending the night in hollows (sometimes communally), or by burying themselves in the snow. Desert adaptations include nomadism; breeding after rain; avoiding breeding in bad years; breeding at an early age (permitting rapid population build-up); mechanisms for restricting water-loss; evaporative cooling, and modifying the effects of heat; ability to survive on a minimum of water or to drink semi-saline water; and being cryptically coloured (Serventy 1971; Immelmann 1971; Dawson 1980). Gloger's Rule (that races living in arid areas are pale-coloured) has wide application in birds, as does Bergmann's Rule (races occupying colder latitudes are larger than those inhabiting warmer areas). At the finer level, within avifaunas and bird communities, it is now appreciated that individual species show complex ecological, behavioural, and structural adaptations for specific ways of life. These also serve to channel species within communities into different roles, thus permitting a diversity of different species to live together. There is a general link between body and bill size, and prey or food particle size (e.g. Hespenheide 1971). Migratory races of species have longer and more tapering wings than resident ones. Species living close to the ground or in thickets (e.g. quails) have rounded wings, a shape presumably linked to rapid vertical take-off. In warblers, minor differences in tarsal structure have been shown to be related to different perching habits (Leisler 1980; Osterhaus 1962). Species interactions could be a significant factor in consolidating ecological specializations. Recent studies on migration (e.g. papers in Keast and Morton 1980) reveal not only a great diversity of adaptations associated with overwintering patterns but also a high adaptational plasticity amongst the migrants. These birds not only occupy different habitats in winter and summer but some may change their diets (e.g. from insect-eater to frugivore). Again, they art: able to operate effectively in quite different J.A.K. bird communities in summer and winter. Berthold, P. 1975. Migration: control and metabolic physiology. In Farner, D.S. & King, J.R. (eds.). Avian Biology V: 77-128. New York. Dawson, W. 1980. Adjustments of Australian birds to thermal condition and water scarcity in arid zones. In Keast, A. (00.). Ecological Biogeography of Australia. The Hague. Hespenheide, H.A. 1971. Food preference and the extent of overlap in some insectivorous birds, with special reference to the Tyrannidae. Ibis 113: 59-72. Immelmann, K. 1971. Ecological aspects of periodic reproduction. In Farner, D.S. & King, }.R. (eds). Avian Biology I: 342-391. New York. Keast, A. 1968. Moult in birds of the Australian dry country relative to rainfall and breeding. J. Zoo!' ISS: 185-200. Keast, A. & Morton, E.S. 1980. Migrant birds in the Neotropics. Ecology, Behaviour, Distribution and Conservation. Washington. Leisler, B. 1980. Morphology and habitat utilization in Acrocephalus in Europe. Proc. XVII Int. Orn. Congr. Berlin. Osterhaus, M.R. 1962. Adaptive modifications in the leg structure of some North American Warblers. Am. MidI. Nat. 68: 474-486. Payne, R.B. 1972. Mechanisms and control of molt. In Farner, D.S. & King, J.R. (eds.). Avian Biology II: 104-157. New York. Serventy, D.L. 1971. Biology of desert birds. In Farner & King (eds). Avian Biology I: 287-341. New York.

ADAPTIVE RADIATI 0 N: denotes divergence in the characters of related forms that enables them to exploit different kinds of opportunity (see ECOLOGY).

ADDLED: term applied to egg in which the developing embryo has died, as opposed to an infertile egg in which no development has taken place. ADDUCTOR: see MUSCULATURE. ADENOSINE TRIPHOSPHATE (ATP): the source of energy for, inter alia, muscular contraction (see METABOLISM). ADJUTANT: also 'Adjutant-bird' or 'Adjutant Stork', substantive name of species of Leptoptilos (see STORK).

ADRENAL GLAND: see

ENDOCRINOLOGY AND THE REPRODUCTIVE

SYSTEM.

ADULT: theoretically, a bird that has reached its fullest development; in practice, however, a term difficult to define precisely. Size is no criterion, as a bird is virtually full-grown at a very early age (see also YOUNG BIRD). The implication is that the bird has attained, appropriately to season, definitive plumage (see PLUMAGE; MOULT); and also that it is capable of breeding (see MATURITY). For most purposes, plumage provides the only practicable criterion. Difficulties are that many species breed, some even more than once, before acquiring their best plumage; and that others do not breed in the first year of wearing it (see AGE). ADVERTISING DISPLAY: see DISPLAY. AEGITHALIDAE: see under PASSERIFORMES, suborder Oscines;

TIT,

LONG-TAILED.

AEGITHOGNATHOUS: see PALATE. AEGOTHELIDAE: see CAPRIMULGIFORMES;

OWLET-FROGMOUTH.

AEGYPIINAE: see VULTURE (1). AEPYORNITHIDAE: see under STRUTHIONIFORMES; EARLY EVOLUTION OF BIRDS; ELEPHANT BIRD; EXTINCT BIRDS. AERATION: see RESPIRATORY SYSTEM. AETHINI: see AUK. AETIOLOGY: the science of causation, especially the causes of disease (see DISEASE). AFFERENT: carrying inwards i.e, towards the centre; applied especially to nerves, in respect of the direction in which they transmit impulses----contrasted with EFFERENT (see NERVOUS SYSTEM). AFRICA: see PALEARCTIC

Madagascar).

AFROTROPICAL REGION (for Africa south of the Sahara); REGION (for North Africa); MALAGASY REGION (for

AFROTROPICAL REGION: one of the six major zoogeographical regions (see DISTRIBUTION, GEOGRAPHICAL), consisting essentially of Africa south of the Sahara but excluding Madagascar (see MALAGASY REGION) and the Comoro Islands while including the islands of Zanzibar, Pemba, Mafia and the Gulf of Guinea. Previously known as the Ethiopian Region until the former state of Abyssinia changed its name to Ethiopia and necessitated a revision of the regional name. In the north it abuts the southern border of the Palearctic Region, which runs from about 21°N in the west to 22!ON at the Red Sea, skirting to the south of the Ahaggar and north of the Air and Ennedi massifs. The south-west corner of Arabia has sometimes been included; it contains enough Palearctic elements to exclude it from the Afrotropical Region but enough Afrotropical elements to exclude it from the Palearctic. The total area of the region is about 21 million km 2 of which about 1~ million km 2 are south of the tropics; the southern limit is at about 35°S. The distribution of Afrotropical birds is closely related to that of vegetation types, which in turn are influenced by climate and topography, and, within a vegetation type, to its history. A useful account of the habitats of Africa, with special reference to birds, is given in Brown et al (1982). The most recent authoritative study of the vegetation is incorporated in the map by White (1982), which recognizes 18 floristic divisions and about 75 vegetation types. An important feature is the extent of vegetation types that are transitional between others, or are a mosaic of different types existing side by side; together, transitions and mosaics account for about 36°;0 of the area of the Afrotropical region. The most conspicuous avifaunal changes coincide approximately with the boundaries of major vegetational types. Bird distribution patterns analyzed by Crowe and Crowe (1982) could be divided into 31 avifaunal zones, arranged in a 3-tier hierarchy from sub-regions through provinces to districts; of these, the boundaries of the 10 provinces coincide most closely with the boundaries of phytochoria (floristic zones) in White's map. The most important

4 Afrotropical Region

distinction in the avifauna remains that between forest and non-forest species, as stressed by Moreau (1966), even though more forest species are now known to occur in other habitats as well. The geographical pattern of vegetation types is essentially a series of latitudinal belts becoming progressively more arid and open away from the Equator. This basic pattern is complicated by topography; east of 300E and south of about 8 much of the land surface is 1,000 m or more above sea level and is too cool and dry for the development of the lowland rain-forest that is found at lower altitudes. On these raised plateaus, woodland, savanna and grassland or scrub replace the forest found further west and north. About 37% of the Afrotropical Region lies at altitudes of 1,000m or more, compared, for example, with less than 170/0 of the Neotropical Region; the relatively small proportion of lowland must go some considerable way towards explaining the impoverishment of the Afrotropical Region compared with other parts of the tropics. Lowland rain forest occupies the equatorial lowlands to about 10° north and south, and east to about 28°E; it is bordered broadly by a transitional zone consisting of a mosaic of woodland, forest and grassland maintained by the burning and stock-grazing activities of man. The zone as a whole is characterized by high rainfall-ISO em a year or more-and the lack of a marked dry season; but few if any parts of the Region receive the high and dependable rainfall found in many parts of the lowland rain forests of South America or South-East Asia. There is little or no undisturbed primary rain-forest remaining in Africa, but those areas that approach this condition most nearly are dominated by tall trees with few side branches beneath the canopy at 30-50 m, festooned with epiphytes and Hanes.Below these tall emergent trees are several layers of tree canopy that between them shade the ground so darkly that the vegetation there is a sparse one of scattered herbs and saplings with very few grasses. Natural breaks in the canopy, caused by falling trees, watercourses or landslips, are important because they admit the light to lower levels and so allow the growth of a dense luxuriant undergrowth. This understorey is characteristic of much African forest where man has crudely mimicked the effects of natural breaks in the canopy. Rich forest extends also along rivers, whose water allows the trees to survive far outside the climatic limits of forest set by rainfall; these 'gallery' or riverine forests are often only a few trees deep but may be important dispersal routes for forest birds. The stratification of the forest plants into layers is often confused; the ground layer, understorey and uppermost canopy are clearly recognizable but it is often impossible to distinguish other separate strata. Characteristic birds of the ground layer and understorey are thrushes and babblers; the upper layers are far richer, abounding in cuckoos, turacos, trogons, hornbills, barbets, starlings and weavers. Flycatchers, warblers and bulbuls range widely at all levels of the forest. Woodlands and grasslands. Beyond about 8° north and south of the Equator, the transitional mosaic of forest, woodland and grassland gives way to more uniform expanses of woodlands and wooded grasslands. The chief distinction between these and the forest habitats is that here the trees are often more widely scattered, are deciduous and have a lighter, more airy canopy, allowing enough light to reach the ground to support a luxuriant growth of perennial grasses. The term 'savanna' is often used for some of these habitats but for a variety of reasons is now to be avoided. A wide belt between about gO-lOON and 100 - 1 6 ° S is dominated by the wettest of these habitats, a closed deciduous woodland consisting chieflyof Brachystegia spp.,]ulbernardia spp. and, especially north of the Equator, I soberlinia spp.; much of this, especially in the south, is often referred to as MIOMBO. The grassier, more open habitats are characterized by frequent dry-season fires; the trees are characteristically thick-barked and fireresistant, the grasses grow in dense clumps with roots and stems protected deep in the soil. The characteristic birds of the grassier habitats are grasswarblers Cisticola, weavers (Ploceidae) and estrildid finches (Estrildidae). Semi-arid bushlands and deserts. Drier vegetation with small scrubby trees and bushes, and scattered annual herbs and grasses, dominate three areas-a belt along the southern edge of the Sahara (the Sahel), a block in the north-east from the Gulf of Aden to northern Tanzania, and another block centred on Namibia in the south-west. Trees and shrubs are predominantly species of Acacia and Commiphora, while baobab trees Adansonia are conspicuous at low altitudes in the east. The vegetation is so sparse that for most of the year the appearance of the landscape is dominated by the colour of the soil. Characteristic birds are coursers, bustards and larks, but the avifauna of the trees is also quite rich and these habitats support many Eurasian migrants. The birds show a variety of adaptations to the extreme conditions, including paler plumage than rela0S,

tives in moister environments, and less sedentary behaviour; some species undertake regular migrations of many hundred kilometres south from the Sahel, notably Abdim's Stork Ciconia abdimii and the Grasshopper Buzzard Butastur rufipennis, True desert is found in the Sahara, in the Chalbi Desert of northern Kenya, along the shore of the Red Seaand in the Namib Desert of the south-west. Montane regions. Between about 1,000m and 3,SOOm, the forest on most African mountains changes continuously in its species composition and in the growth form of its trees. The sharp division between lowland and montane forest so firmly stressed by Moreau (1966) and others is less widely accepted now (Diamond and Hamilton 1980). On isolated small mountains, and those near the coast (such as the Usambaras where Moreau worked), vegetation changes occur at lower altitudes, and possibly more sharply, than in forests nearer the centre of the continent. Above the tree-line there is often a zone of heathy bushes and low trees which merges into a more open moorland community of tussock-grasses, rushes, and, on the highest mountains, giant lobelias and ragworts. The 'Afromontane' zone of White (1982) contains many endemic plants and is recognized as a distinct floristic division, occurring on the scattered mountains of the Region in an archipelago-like distribution. Many bird species are common to this zone wherever it occurs, except in Ethiopia where the montane forest avifauna is notably depauperate. Moreau (1966) interpreted the disjunct distribution of these montane species as indicating that montane forest was previously much more widespread, but present historical evidence does not support this (see below). History. Two major historical phenomena have shaped the present Afrotropical avifauna. Widespread volcanic and tectonic activity in the Miocene period, ending about 7 million years ago, raised the eastern and southern parts of the continent a thousand metres or so and generated most of the volcanic massifs there; it also broke the previous connection between the forests of Africa and those of Asia, a connection that is reflected in the affinities of the non-passerine forest avifauna (Snow 1980). The Quaternary period, from about 2 million years ago, has shown continued volcanic activity but has also suffered dramatic climatic changes related to the ice ages at higher latitudes. The classic description of the effects of these changes on the Afrotropical avifauna by Moreau (1966and references therein) needs to be modified in at least two chief respects. First, the assumption that the distinction between lowland and montane forest is determined by temperature did not take into account the very major influence of moisture; second, the cold periods coinciding with the glacial maxima of the ice-ages were not also wet in Africa, as Moreau supposed-the so-called 'pluvials'-but extremely arid. The combined effects of these two points lead to the conclusion, which is supported by a variety of evidence from deep-sea cores to pollen diagrams, that montane forest was not continuous over much larger areas of Africa than it is now, as Moreau supposed was necessary to explain the occurrence of similar species on widely-separated mountains, but is probably as extensive now (apart from its recent reduction by man) as at any time in the last hundred thousand years (Diamond and Hamilton 1980 and references therein). The increased aridity of glacial periods confined forests to the most climatically stable areas; these 'refuges' are identifiable now as centres of endemism and species diversity within areas of apparently homogeneous habitat. During arid periods, the Sahara desert extended as far as SOOkm south of its present boundary, and the Kalahari Desert occupied most of the area now occupied by the lowland rain-forest of Zaire and reached as far east as Victoria Falls as recently as 10,000 years ago. Characteristic forms. Endemic Afrotropical taxa are few above the generic level: they include one order, the mousebirds, and 5 families-Hamerkop, Secretary-bird, guineafowl, turacos and wood-hoopoes, as well as the Ostrich (Struthionidae) which has become endemic, as it were, only by recent extinction elsewhere. The Region is particularly rich in francolins, bustards, barbets, honeyguides, larks, grass-warblers Cisticola, helmet-shrikes, shrikes and estrildid finches (Ploceidae and Estrildidae). The 2 species of oxpecker (Buphaginae) are of special interest because they have evolved as symbionts of the spectacular African fauna of large herbivorous mammals. On the other hand, the Region is poor in parrots and woodpeckers, and the number of species in the Region as a whole is substantially fewer than in the Neotropical Region. One of the most dramatic features of the Afrotropical avifauna is the enormous influx of migrants from the Palearctic region in the northern winter (Moreau 1972). About a third of all Palearctic species winter wholly or mainly in the Region, occupying every habitat except lowland rainforest and some reaching as far south as the Cape. Several species

Age 5

occasionally breed in their African 'winter' quarters, and the close affinity of many species of the southern grasslands with Palearctic species suggests that other African taxa may have originated in this way (Snow 1980). See also MIGRATION. A.W .D . Bannerman, D.A. 1930--1949. Birdsof TropicalWestAfrica. 8 vols. London. Benson, C.W. et all973 (revised edn.). The Birdsof Zambia. London. Benson, C.W. & Benson, F.M. 1977. The Birdsof Malawi. Limbe. Britton,P.L. (00.). 1980. Birdsof EastAfrica. Nairobi. Brown, L.H. , Urban, E.K. & Newman, K. 1982. The Birds of Africa, vol. I. London. Chapin, J.P. 1932-1956. Birds of the Belgian Congo. Parts 1-4. Bull. Am. Mus. Nat. Hist. 65, 75, 75A, 75B. Crowe, T.M. & Crowe, A. 1982. Patternsofdistribution, diversityand endemism in Afrotropical birds. J. Zool. Lond. 198: 417-442. Diamond, A.W. & Hamilton,A.C. 1980. The distribution of forest passerine birds and Quaternary climatic change in tropical Africa. J. Zool. Lond. 191 : 379-402. Hall, B.P. & Moreau, R.E. 1970. An Atlasof Speciation in African Passerine Birds. Brit. Mus. (Nat. Hist.), London. Mackworth-Praed,C.W. & Grant, C.H.B. 1952-1973. African Handbook of Birds, Series 1,2,3. 6 vols. London. McLachlan, G.R. & Liversidge, R. 1978 (revised edn.). Roberts' Birds of South Africa. CapeTown. Moreau, R.E. 1966. TheBirdFaunasofAfrica and its Islands. London& NewYork. Moreau, R.E. 1972. The Palaearctic-African BirdMigration System. London. Penny, M. 1977 (revised edn.). The Birdsof Seychelles and the Outlying Islands. London. Serle, W., Morel, G.J. & Hartwig, W. 1977. A Field Guide to the Birdsof West Africa. London. Snow, D.W. (ed.), 1978. An Atlas of Speciation in African Non-passerine Birds. Brit. Mus.(Nat. Hist.), London. Snow, D.W. 1980. The affinities of African non-passerine birds to the Oriental and Palaearctic avifaunas. Proc. IV Pan-African Om. Congr.: 71-76. White,C.M.N. 1960--1965. (Revised check-lists, separately titled, of African bird families). Lusaka. White,F. 1983. Vegetation Mapof Africa. UNESCOIAEFTAT. Williams, J.G. & Arlott, N. 1980. AFieldGuideto theBirdsofEastAfrica. London.

AFTERFEATHER: (also called aftershaft). This is a structure resem-

bling a feather in miniature attached to the underside of a feather at the superior umbilicus. Six types may be recognized of which the most developed is that found in Casuariiformes, where the afterfeather closely resembles the main feather , so that each feather appears double. In its simplest type the afterfeather lacks an aftershaft (hyporachis) and merely consists of a row of barbs (an aftertuft) attaching to the rim of the superior umbilicus. It is found in the New World vultures (Cathartinae). Several groups entirely lack afterfeathers, e.g. Ostrich Struthio, pigeons, cuckoos and swallows. Most workers assume that the function of afterfeathers is to increase the thermal insulating property of the feathers . This is supported by the facts, (I ) that they nearly always have a downy structure, (2) that they are best developed on body feathers , especially down and semiplumes , but small or lacking on remige s and rectrices , and (3) that some birds, e.g. ptarmigans Lagopus, have larger afterfeathers in the winter than in the summer plumage. See FEATHER; FEATHERS, NUMBERS OF. AGAMI: Agamia agami (see HERON) .

AGE: elapsed time, since hatching, of a live bird. Analogous to age in human beings but only able to be measured accurately for bird s for those individually marked as nest lings (see MARKING ) . In studies of populations (see ECOLOGY) the age of first breeding is particularly important: for small temperate zone passerines it is generally during the first summer but may be deferred for several years in larger species (averages ninth year for Fulmar Fulmarus glacialis). Even when breeding has started, age may have a significant effect on productivity as demonstrated by Coulson and White (1958) for the Kittiwake Rissa tridactyla. Older Kittiwakes were generally in better condition, returned to the colonies earlier in the breeding season, occupied the 'best' sites , laid larger eggs and produced bigger clutches which gave rise to more and healthier young than recent recruits to the breeding population. Such age-effects have now been demonstrated for a wide variety of birds, including small passerines, and are a very significant feature in the population ecology of many species. The age composition of any population of birds depends on the species' mortality which is the fractional part of the population alive at the beginning of a period but dead by its end . Similarly the survival is the fractional part still alive at the end of the period, and so S = I - M where Sand M

Wandering Albatross Diomedea exulans male 30 years old. (P hoto: J .P . Croxall).

are the survival and mortality rates expres sed as proportions. In many studies these figures are calculated over a year but they may also be calculated monthly or over a particular phase of the bird 's life e.g. breeding season mortality. The earliest calculations of mortality were made by Lack (1943), who used reports of birds ringed so long before the analysis that no further reports could be expected; this is known as the Lack or complete data method. Later Haldane (1955) devised a maximum likelihood analysis allowing for the effects on the mortality estimate of ringed birds which were still alive: this enables the incomplete data to be included in the calculation . Both methods assume that the annual mortality rate of adult birds remains constant from year to year. Later methods, often involving detailed modelling and computer analysis, have attempted to allow both for variation in mortality rates from year to year (for instance changes related to the severity of winter weather) and for variation with the age of the bird. The sample of dead birds found is much more likely to include birds dying through inexperience (e.g. dead on road, brought in by cat or stunned against a window ) than those dying under more natural circumstances (e.g. egg-bound on the nest , at a secluded roost or on migration). In fact most birds die through inexperience, for they are constantly at risk from predators, disease , accident and food shortage. Newly independent fledglings are at greatest risk and mortality gradually decreases as the birds become more experienced. For many species mortality seems to be least just after the birds have bred for the first time , and is fairly constant thereafter. The two graphs (Fig . 1) show the gradual loss of individuals from a cohort of youngsters reared in the same year--one species (solid line) is long-lived with a delay of several years before breeding and the other (broken line) is a short-lived passerine breeding in its first summer. A few analyses show that particularly old birds are less likely to survive : this was first demonstrated for the Common Tern Sterna hirundo with increased mortality from the 19th year onwards. Where the species concerned has been studied intensively, the results of mortality analyses can be compared with known productivity and population figures . Mortality estimates computed from dead ringed birds are often high when related to such figures although survival estimates, from repeated sightings of live marked birds, are often compatible with productivity and population figures. Hence the sample of dead birds found is probably biassed towards younger rather than older individuals. Mortality may vary between the sexes. Females are particularly at risk during the breeding season when they must produce and lay the clutch and generally undertake the major share of incubation duties. On the other hand, in some species the males have 'dangerous' displays, including conspicuous song-flights and the regular use of song-posts which may put them at risk; and territorial chases may result in their death from traffic accidents or other collisions . In species with marked sexual dimorphism, size or colour differences may also be responsible for differences in mortality. If a steady annual adult mortality is assumed it is possible to calculate the Expectation of Further Life of an adult bird . The simplest formula is 2 - M/2M where M is the annual adult mortality. This gives the expected further life-span of a bird on reaching adulthood. However, for many

6

Age

100 \

\ \

\

30

\\

Q; > ~

c: 10 .2

"0 3

\

\

- - Seabird species \

\

\

\ \

a.

tf

\

\

3

\

,

\-,-Passerine species

,

\

\

1-+-...,.......,r--r....,--r-1--.--+.,......,-r....,-.,......,-,--r-.,......,--.-.......,......,--.-,-r-'T--r-,-,.......--.--r-~.,

o

5

10

15 20 Age in years

25

30

35

Fig. 1. The decay of two bird populations of 100 individuals at fledging. The solid line is of a seabird with 65% first year mortality, 15% p,a. for 4 pre-breeding years and 10% p.a. thereafter. On average one bird will live to 32 years of age. The broken line is for a passerine with 750/0 first year mortality and 35% p.a. thereafter: one of these would, on average, last into its ninth year. N .B. the vertical scale (population) is logarithmic.

small passerine species in the northern temperate regions, 90% or more of all eggs laid may fail to produce young that attain adulthood. Indeed, for a bird population to remain stable, each adult that breeds needs only to replace itself. Thus each adult needs, on average, only to rear two young to maturity during its life as a breeding bird-two need to be reared as each breeding attempt involves an adult of each sex. The huge changes in life expectation as mortality rates vary are evident from the following examples: Bird

Small passerine Woodpigeon Columba palumbus Swift Apus apus Yellow-eyed Penguin M egadyptes antipodes Royal Albatross Diomedea epomophora

Annual adult mortality

Expectation offurther life ofan adult

0.9 year 2.0 years 4.5 years 9.5 years 32.8 years

Longevity records (examples of extreme old age) provide concrete evidence of age-span but may be difficult to interpret. Species for which many recoveries have been reported are more likely to include a particularly old individual rather than those rarely marked or from parts of the world where ringing has only recently been introduced. The two tables of longevity records show the maximum recorded elapsed time between ringing and recovery of wild birds. Most have been taken from Rydzewski (1978, 1979) with additional data from British ringing files. The tables are in descending order of age and include, if available, one record (maximum three) for each main family or group. Clearly the larger birds can be expected to live longer than the smaller ones when species are compared. Lindstedt and Calder (1976) investigated the relationship between longevity records (4.08-38 years) and body mass (3.5-12,200 g) of 152 species in the wild. They obtained a good correlation between the two and showed that longevity was roughly proportional with the fifth root of body mass-L 17.6Mo. 2owhere L is longevity in years and M body mass in kg. Thus, on average, a doubling of body mass would lead to 15% greater longevity and body mass has to increase 32-fold for a doubling in longevity (e.g. Blue Tit Parus caeruleus to Tawny Owl Strix aluco). The non-passerine list shows that waders and terns survive well despite being relatively light species. Ducks, game-birds and kingfishers mostly appear in the lower part of the table and generally lay large clutches. Among the passerines the larger temperate species head the list because very large files of recoveries are available, but it is likely that tropical passerine species will eventually be shown to be much longer lived than temperate ones (Fry 1980). Extreme longevity is symptomatic of K-SELECTION and poor longevity OfR-SELECTION (see also ECOLOGY). The records from bird collections and zoos show that captive birds live much longer than those in the wild. London Zoo in 1982 had two birds in its collections which had been resident for 50 years: a Common Caracara Polyborus plancus since 1932 and a Sulphur-crested Cockatoo Cacatua galerita since 1925. The cockatoo had been with its previous owner since about 1902 and was certainly more than 80 years old. This may be the

oldest bird ever reliably recorded. Also 75% of London Zoo's Night Herons Nycticorax nycticorax were still alive at an age (about 8 years) when 990/0 of wild Grey Herons Ardea cinerea would have died (no data were available for Night Herons in the wild). In normal circumstances there is no possibility of accurately measuring the age of a wild bird without marking it but instances exist of individually recognizable birds, e.g. albino waders, frequenting the same place for a decade or more. Detailed work on Bewick's Swan Cygnus columbianus has shown that individuals can be recognized, over periods of many years, by their bill patterns (see DUCK). One individual, Lancelot, was recorded over 19 winters. However it is often necessary to describe the age of a bird in the field or in the hand, in so far as it can be assessed. For nestlings growth is so rapid that measurements of bill, tarsus and primaries may often be used to estimate the age to within a day or so from hatching (see GROWTH) but, after fledging, a bird's age can usually be estimated only within broad limits, generally on the basis of age-specific plumages (see PLUMAGE; MOULT), from the colour and growth of the bare parts or, for young birds, from the incomplete ossification of the skull. Birds pass through a sequence of plumages and age has normally been recorded by a simple description of the bird's current plumage phase. The progression for a northern temperate passerine is as follows: Month 6 7 8 9 10 11 12 1 2 3 4 5 6 7 8 9 10 11 12 1 2 3 4 Moult Major Minor Complete Minor Juvenile

First winter

First summer

Adult

First winter and first summer may be combined into First year. Adult is used for the rest of the bird's life as it has reached its definitive adult plumage.

These simple descriptions of age for free-flying birds are liable to confusion, especially between different groups of workers, and are, in any case, not adequate for large non-passerine species with a long sequence of identifiable immature plumages spanning several years. Bird ringers, in the Holarctic, now use a precise code based on the calendar year:

Longevity records-i-Non-passennes Oystercatcher Haematopus ostralegus + Royal Albatross Diomedea epomophora + Arctic Tern Sterna paradisaea + Guillemot Uria aalge Black-headed Gull Larus ndibundus Osprey Pandion haliaetus Mallard Anas platyrhynchos Honey Buzzard Pernis apivorus Spoonbill Platalea leucorodia Long-eared Owl Asio otus Black-throated Diver Gavia arctica White Stork Ciconia ciconia Manx Shearwater Puffinus puffinus + Purple Heron Ardea purpurea Northern Fulmar Fulmarus glacialis Blue-faced Booby Sula dactylatra Pink-footed Goose Anser brachyrhynchus Mute Swan Cygnus olor Swift Apus apus + Shag Phalacrocorax aristotelis

Red-bellied Woodpecker Melanerpescarolinus Leach's Petrel Oceanodroma leucorhoa Little Blue Penguin Eudyptula minor + Coot Fulica atra Arctic Skua S tercorarius parasuicus + Mourning Dove Zenaida macroura Kestrel Falco tinnunculus White Pelican Pelecanus erythrorhynchus Kea Nestor notabilis Little Grebe Tachybaptus ruficollis + Cuckoo Cuculus canorus Kookaburra Dacelo nouaeguineae + Capercaillie T etrao urogallus Quail Coturnix coturnix Ruby-throated Hummingbird Archilochus colubris +

years

36.0* 35.9 33.9* 32.1 * 32.1 31.2 29.0*

28.9* 28.2*

27.7* 27.0 26.2*

26.0 25.5* 23.0 22.9* 22.1 21.7

21. 1* 20.6* 20.4

19.9 18.9* 18.3

18.1* 17.1* 16.2*

16.1* 14.1

13.1 12.9* 12.3 9.3 * 7.6

5.0

Aggression

R inger's age categories

Europ ean code

Free flying: age unknown Hatched this year Hatched before this year Hatched last year Hatched before last year Hatched the year before last Hatched earlier still

2 3 4

5 6 7

8

7

A merican code

U (Unknown) HY (Hatching Year) AHY(After Hatching Year) SY(Second Year) ASY(After Second Year) TY (Third Year) ATY (After Third Year)

Important manuals cont aining age (an d sex) information on northern hemisphere birds are Svensson (1984) for European pa sser ines , Wood (198 1) for North American species and Prater, March ant and Vuorinen (1977) for Holarctic waders . C.] .M. Coulson, J.C. & White, E. 1958. The effect of age on the breeding biology of the KiuiwakeRissa tridactyla , Ibis 100: 40-5 1. Fry, C.H. 1980. Survival and longevity among tropical land birds. Proc. IV Pan-Afr. Om. Congr.: 333-343 . Haldane, J.B.S. 1955. The calculation of mortality rates from ringing data. Acta XI Congr. Int. Orn .: 454-458 . Lack, D. 1943. The Life of the Robin. London. Lindstedt, S.L. & Calder, W.A. 1976. Body size and longevity in birds. Condor 78: 91-94 .

Prater, A.J., Marchant, J.H . & Vuorinen, J. 1977. Guide to the identification and ageing of Holarctic waders. BTO Guide 17. Tring. Rydzewski, W. 1978. The longevity of ringed birds. The Ring 96--97: 218-262. Rydzewski, W. 1979. The longevity of ringed birds. The Ring 98- 99: 8. Svensson, L. 1984. Identification Guide to European Passerines. Stockholm. Wood, M. 1981. A Bird-Bander's Guide to Determination ofAge and Sexof Selected Species. Pennsylvania State University, Pennsylvania. AGGRESSION: threatening behaviour and attack. Overt aggre ssion , in the form of pure ph ysical assault, is usuall y int er mingled with or overlain by a variety of postures, movements and vocalizations which serve as threat, repelling or intimidating the oppo nent without actual combat. A general term for thi s mixture of attack, threat and withdrawal is 'agonistic

L ongevity records-Passerines

Blackbird Turdus merula Starling S tum us v ulgaris Rook Coru us f rugilegus Bullfinch Pyrrhula pyrrhula Swallow Hirundo rustica Great Tit P arus major Golden Oriole Onolus oriolus Common Grackle Quisealus quiscula + Red-winged Blackbird A gelaius phoeniceus Cardinal Cardinalisc ardinalis + Brown-headed Cowbird Molothrus ater + Robin E nthacus rubecula White·crowned Sparrow Z onotnchia leucoph rys Waxwing B omby eilla garrulus White-browed Babbler Pomatostomus superciliosus + House Sparrow Passerdomesticus Brown-throated Sunbird A nthreptes malaeensis + Olive-winged Bulbul Pycnonotus plumosus + Black and White Warbler Mn iotilta varia Reed Warbler Acrocephalus scirpaceus + Silvereye Z osterops lateralis + Skylark Alauda arvensis Warbling Vireo Vireo gilvu s + Pied Wagtail M otacilla alba + Blue-gray Tanager Thraupi s episcop us White·breasted Nuth atch S illa carolinensis + Pied Flycatcher F ieedula hy poleuca + Dunnock Pru nella modulans Dipper Ci nclus cinclus + Long-tailed Tit Aegithalos caudatus + Bay-backed Shrike L anius villalUS + Wood Thrush Hy/ocichla mustelina Goldcrest R egulus regulus Treecreeper Certhia fam iliaris House Wren T roglodytes aedon +

years 20 .3 20 .0 19 .9'

17.5 16.0' 15.0 14.9'

14.7 14.2'

13.5' 13.0 12.9'

Great Skua S tercorarius skua aggressive display. (P hoto: E .]. Hoskin g). behaviour' . Certain behaviour mu st be distingu ished from true aggression or the category becomes so diffu se as to be usel ess. For example, bird song ma y induce withdrawal and thus make unnecessa ry the physical defence of a territory, but its motivation is d istinct from that of attack or threat. Raptor ial killing is separa ted from true aggr essive behaviour for similar reasons. Whilst m ost aggressive behaviour occurs within a species, true aggressive behaviour does occur between members of d ifferent species where the se compete for resources. In wild birds, fighting is rarely prolonged and threat is often used rather than overt fighting . This is because fighting involves costs: ph ysical combat is exhausting, carrying a risk of injury and an increased risk of predation. Set against these costs ar e the benefits of gaining or own ing the contested item . The theory of natural selection indicates that the level of aggress ion shown will depend on th e balance between these benefits and the costs involved . Although it is difficult to quantify these it has , for example, been po ssible to measure the greater yield of flower s within th e territory of sun birds Nectarinia reichenowi co m pared with the undefended flower s outside . Aggressive int eractions ma y lead to the formation of a DOMI NANCE hierarchy, within a group of birds, although spe cies d iffer in the readiness with which this occurs. The hierarchy is best regarded as a way of reducing the detrimental effects of freq uent aggressive interactions, rather than a desirable feature of social stru ct ure, but its presen ce may have important implications for population dynamics (see ECOLOGY) . In some species, dominance rank in winter flocks is related to earlier territorial boundaries,

12.8 12 .6

12.1 12.0

11.7 11.7' 11.1 11.0

10.7 10.1'

10.0 9.9 9.4

9.4 9.2' 9.0 8.4' 8. 1 7.9 7.8

7.0 6 .8'

6.2

White.billed Diver Gavia adamsii aggressive display. (P hoto: A .V . Kr echmar).

8

Aggression

Pheasant Phasianus colchicus two males fighting. (P hoto: F . P olking). an illustration of the links between aggression in different contexts. Aggression has sometimes been regarded as an inborn drive which must be suppressed or re-channelled for successful social life. But since it enables birds to compete for food, nesting and roosting sites and mates, and spaces them out appropriately, its occurrence can be better understood in most instances in terms of the benefit it brings to the individual involved . Aggression cannot be a unitary phenomenon across such a wide range of contexts, but it appears to share causal factors in different contexts, so that its subdivision into several distinct categories is inappropriate. Outside the reproductive season, one common factor is physical proximity. Factors such as hunger, which increases fighting over food, produce this effect by bringing birds together rather than by increasing their aggressiveness. Whilst most non-reproductive fighting can thus be explained in terms of defence of the individual distance (a small defended area, centred on the bird ), reproductive fighting may involve defence of a larger , fixed territory. In the Chaffinch Fringilla coelebs, intermediate stages between defence of the individual distance and defence of the territory can be found . The gradual modification of the defended area in this species, under the influence of androgens and experience during the spring, demonstrates close links between reproductive and winter fighting. But in the weaver bird Quelea quelea, the hormone which stimulates individual distance fighting (luteinizing hormone) is not the same as that which stimulates fighting over nest materials (testosterone). Thus the control of aggressive behaviour may differ in detail in different contexts, and generalizations must be made with due care. Androgens such as testosterone are important in the control of aggression in many species, and female phalaropes Phalaropus spp ., which set up and defend the territory whilst

Snow Goose Anser caerulescens aggressive display. (P hoto: A. V . Krechmar).

the males incubate, have high levels of androgen. Other hormones which modify aggressive and defensive behaviour in various species are oestrogens, proge sterone, prolactin and follicle stimulating hormone (FSH), but the details of such hormonal effects will probably depend on the reproductive cycle of the species concerned. Although most aggressive behaviour can be understood in terms of benefit to the individuals involved, the effects of pain and frustration (which increase the probability of aggression ) have not yet been explained in this way. Demonstrations of this effect of frustration in pigeons Columba livia , hens Gallus gallus, and Quail Cotumix co/urnix have all involved frustration of feeding , and so it is possible that the effect could be understood in terms of the tactics of feeding in a flock. Some examples of the 're-direction of aggression ' , for instance where a Chaffinch which has just lost a fight attacks a feeding subordinate without provocation , may also be explicable in this way, rather than implying that aggression must be discharged once it has been aroused, as the term 're-direction' suggests. In a reproductive context , behaviour which was once described as redirected 'aggression' (the 'swoop and soar' performance of the Blackheaded Gull LaTUS ridibundus ) has proved to be purely sexual in motivation, and need not be explained in terms of the re-channelling of aggressive motivation aroused by the mate . Most aggressive behaviour is triggered by external stimuli. Despite the fact that fighting cocks will work for the opportunity to threaten a rival in the laboratory, there is little evidence that wild birds show appetitive behaviour for fighting , except as a consequence of learning . The European Robin Eruhacus rubecula , for instance, will go specifically to places at which it has recentl y had fights when patrolling its territory, and may even

Galapagos Hawks Buteo galapagoensis fighting. (P hoto: F . Polking).

AJcae

attack an imaginary opponent if the effect of previous experience is very intense . External stimuli from the territory, the mate and the family may all playa part in triggering aggression in different species, but stimuli from the opponent are of greatest importance. Many aspects of the form, posture and bearing of a bird determine whether it will be attacked, but some features are so important that they are termed RELEASERS , for instance the red breast of the European Robin . (Some features, such as the nape band of the Kittiwake chick Rissa tridactyla, have the opposite effect, inhibiting attack). Such badges on the plumage also modify the way in which birds respond to aggression by the bearer . In the Red-winged Blackbird Agelaiusphoeniceus experimental concealment of the male's red epaulets reduced the ability of the subjects to win contests and retain their territories, since their opponents refused to submit . Birds use a variety of postures in threat; in many species these contain intention movements of attack, and have evolved from behaviour reflecting ambivalence towards the opponent. The effect of threat postures has been analysed by noting what posture is shown in an interaction, and correlating this with the opponent's response, and also by presenting dummies mounted in a particular posture and noting the response. Threat postures may produce withdrawal without the need for physical attack . There has been dispute over whether they do this by providing informa-

9

Maynard Smith , J . 1979. Game theory and the evolution of behaviour . Proc. Roy. Soc. Lond . B 205:475-488.

AGONISTIC : term applied to behaviour relating to combat (see AGGRESSION ) .

AIGRETTE : see PLUME . AILUROEDINAE : see BOWERBIRD . AIR.PASSAGES; AIR -SACS: see RESPIRATORY SYSTEM . AIR SPEED: see FLIGHT, SPEEDS OF . AKALAT: substantive name used in West Africa for Malacocincla ('Illadopsis') spp . (for subfamily see BABBLER) , and in East Africa for chats of the genus Sheppardia (for subfamily see THRUSH) . AKEPA : Loxopscoccinea (see HAWAIIAN HONEYCREEPER). AKIALOA : Hemignathus obscurus, also called 'Sicklebill' (see HAWAIIAN HONEYCREEPER) .

AKIAPOLAAU: Hemignathus wilsoni (for family see HAWAIIAN

HONEY-

CREEPER) .

ALA MEMBRAN A: the wing membrane, on the posterior margin of the forewing and manus , from which the remiges grow (see WING) . ALAR: pertaining to the wing. ALARM : expressed, like WARNING , either visually or vocally, with the distinction that there is not necessarily a warning function, although this may be the effect on other individuals.

House Martin Delichon urbica attacking Swallow Htrundo rusllca wnen collecting nest mater ial (mud) . (Photo: H . Schouten).

tion about the signaller's intention to attack (statements of intention would be open to cheating), and the processes involved in the interaction are not yet understood . Aggressive elements are also visible in the form of many courtship and parental displays in birds, but the role of aggression in courtship is not fully understood (see AMBIVALENCE) . The development of aggression has been studied in detail in only a few species, including the ]unglefowl Gallus g. spadiceus. Its adult aggressive behaviour is only gradually built up from components which appear independently in the young bird . Although the process appears to allow opportunities for learning in the integration of these motor components, isolation during rearing disturbs not the form of the motor patterns , but rather the way in which the aggressive behaviour is used. For example, isolation-reared cocks do not switch from aggression to sexual behaviour when the hen crouches . This evidence that individuals require social experience during rearing to show normal aggressive behaviour parallels that for many higher animals, but we cannot yet explain the details of its P.G .C. pattern of development. See photo DISPLAY . Andersson , M. 1976. Social behaviour and communication in the Great Skua. Behaviour 58:40-77. Dun can, I.J .H . & Wood-Gush, D .G .M . 1971. Frustration and aggression in the domestic fowl. Anim . Behav. 19:500-504. Galusha, J .G. & Stout, J .F . 1977. Aggressive communication by Lams glaucescens Part IV: Experiments on visual communication . Behaviour 62 :222-235 . Kruijt , J .P . 1964. Ontogen y of social behaviour in the Burme se Red Junglefowl (Gallusgallusspadiceus) Bonnaterre. Behaviour Suppl. 12: 1-201. Marler , P. & Hamilton , W.J . 1966. Mechanisms of Animal Behaviour , Chapter 5. New York.

Great Spotted Woodpecker Dendrocopos major juvenile showing alarm . (Photo: A .T. Moffett).

ALA SPURIA: the alula or BASTARD WING (see WING) . ALAUDIDAE: a family of the

PASSERIFORMES,

suborder Oscines; see

LARK.

ALAUWAHIO : Loxops maculata also called Hawaiian Creeper (for family see HAWAIIAN HONEYCREEPER) . ALBATROSS: see PETREL. See photos

AGE; DISPLAY; FLIGHT.

ALBINO; ALBINISM : see PLUMAGE, ABNORMAL. ALBUMEN: see

DNA AND PROTEINS AS SOURCE S OF TAXONOMIC DATA;

EGG.

ALCAE: see under CHARADRIIFORMES;

AUK.

10 Alcedines; Alcedinidae

ALCEDINES; ALCEDINIDAE: seeCORACIIFORMES; KINGFISHER. ALCEDIN 0 IDEA: see under CORACIIFORMES; KINGFISHER. ALCIDAE: see underCHARADRIIFORMES; AUK. ALE THE: generic name used as substantive common name for speciesof chats (see THRUSH). ALIMENTARY SYSTEM: consists essentially of (1) the buccal apparatus (bill, mouth, tongue, salivary glands and sensory receptors), (2) the oesophagus (and crop if present), (3) stomach (proventriculus and ventriculus), (4) the small intestine (duodenum and ileum), (5) the large intestine (caeca, colon and cloaca) and (6) various glands and organs including the liver, biliary system and gall-bladder, the pancreas and the bursa of Fabricius. Most of the these components are derived from the endoderm during the development of the bird in the egg. During the course of evolution, modern birds have acquired mechanisms for the regulation of body temperature, a high metabolic rate, powered flight and a world-wide distribution. Consequently birds feed on relatively large quantities of a great variety of substances including fish, flesh, carrion, fruit, roots, leaves, seeds, pollen, nectar and all kinds of invertebrates (see FEEDING HABITS). Their diets may change as they mature, as the seasons change or as a result of migration. Nevertheless, unless wild birds are markedly different from their domesticated relatives, we may assume that the food of any bird must supply about forty chemical compounds to provide the energy and nutrients for growth, activity, reproduction and general maintenance (see NUTRITION). The alimentary system has become adapted to obtain and process the food and extract the nutrients. Several features of the avian alimentary system are probably related to the fact that most birds are supremely modified for powered flight. For example, the relatively heavy cephalic apparatus of many mammals is not present in modern birds. Instead, trituration occurs, when necessary, in the ventriculus or gizzard, which is located deep in the body where equilibrium will not be disturbed during flight. Other features of the tract are assumed to be functional adaptations for the digestion of a particular diet (see below). Morphology and structure. Some general information about the form of the alimentary tract is given in Figs 1 to 20. Details of the bill are given elsewhere (see BILL). The mouth accommodates the tongue, which is as varied in form as the bill (see TONGUE), and the salivary glands. The oesophagus leads out of the mouth and enters the proventriculus (Fig. 1). In some birds, a thin-walled pouch, called the crop or ingluvies (Figs 4, 6 and 8), extends from the ventral wall of the oesophagus. The oesophageal lining consists of longitudinally-folded stratified squamous epithelium which is capable of considerable distension (Fig. 5). The stomach comprises the secretory or glandular proventriculus and the muscular ventriculus or gizzard (Fig. 1). The degree of development of the secretory and muscular tissue can often be correlated with the nature of the diet (Figs 9 and 11). Much of the thickness of the proventricular wall is due to the proventricular glands consisting of secretory cells some of which produce mucus while others (oxyntico-peptic cells) secrete both hydrochloric acid and pepsinogen (pepsin precursor). The ventriculus, in birds which ingest hard or fibrous food, is generally very muscular and may contain grit or other abrasive material so that it functions not unlike a ball mill. The ventricular lumen is lined by a polysaccharide-protein substance known as koilin which protects the tissues from acidic and abrasive damage. The pylorus connects the stomach with the small intestine which consists of the duodenum and ileum (Fig. 1). The pancreas is usually located between the descending and ascending limbs of the duodenum and its digestive secretions usually enter the small intestine at the caudal end of the ascending limb near the entry of the bile ducts. This point may be taken as the end of the duodenum and the start of the ileum. Most birds possess a gall-bladder, which is usually embedded to some extent in the right lobe of the liver. There are usually two bile ducts which carry bile either directly from the liver or in a more concentrated form from the gall-bladder into the small intestine (Fig. 2). The length of the ileum, which is often smaller in diameter than the duodenum, appears to be related to the nature of the diet. Carnivorous birds tend to possess relatively short intestines and herbivorous birds usually have long ones. The large intestine, consisting of the paired caeca, colon and cloaca, extends from the ileo-caeco-colic junction to the vent

(Fig. 1). The caeca are variable in size and shape; some birds (herons) possess one caecum and not two (Figs. 12-18) while others (kingfishers) do not seem to have any obvious caeca. The complex cloaca receives and discharges intestinal and caecal faeces and urine from the bird (Fig. 3) (see DROPPINGS). In young birds, a small diverticulum called the bursa of Fabricius extends from the mid-dorsal wall of the cloaca. The bursa has an important immunological function similar in some respects to that of the thymus. Throughout its length, the alimentary tract is made up of concentric layers known, in the small intestine, as the mucosa, submucosa, muscularis and serosa (Fig. 19). The mucosa consists mainly of villi which are formed from a layer of epithelial cells enclosing the lamina propria (Fig. 20). The lamina contains blood vessels, connective tissue and many white corpuscles which contribute to the immune responses of the bird. Numerous white corpuscles are to be found in the caecal tissues and the caecal tonsil, which is located near the ileo-caeco-colic junction and is reminiscent of a lymph node. The surfaces of many of the epithelial cells are composed of numerous microvilli. The effect of this enormous elaboration of intestinal surface membrane, together with the increase in surface area due to the villi, is to provide a very large surface area for the absorption of nutrients from the contents of the intestinal lumen. Goblet cells, which produce mucus, are also located in the epithelium. There are usually more goblet cells in the posterior small intestine and the caecathan in the duodenum. The submucosa is similar in appearance to the lamina propria although the white corpuscles may be found in discrete colonies and more connective tissue is present in addition to nerve fibres and larger blood vessels. The muscularis consists of a relatively thick coat of circular muscle and a thinner layer of longitudinal muscle (Fig. 19). The outer serosal layer is formed from connective tissue. The principal blood vessels of the post-pyloric part of the tract of the domestic fowl are illustrated in Fig. 1. Most blood is supplied to this part of the tract by the coeliac, anterior and posterior mesenteric arteries which originate from the dorsal aorta. The blood leaves the small intestine along the veins of the hepatic portal system which transports recently absorbed nutrients directly to the liver (see METABOLISM). The tract receives an extensive autonomic or sympathetic innervation which is partially responsible for regulation of the variable motility of the tract. Physiology of digestion. Digestion involves the sequential mechanical and chemical breakdown of food into components which are in a suitable condition for absorption. The alimentary tract provides not only the agents for this process but also the physico-chemical conditions for their efficient action. The intestinal motility serves to move the food along the tract, to mix the food and agents of digestion for the optimum time and to present the products of digestion to the absorptive surface of the small intestine. Fig. Fig. Fig. Fig.

1. Stomach and intestine of a domestic fowl Gallus gallus. 2. Gall-bladder and bile ducts of a domestic fowl. 3. Cloaca of a domestic fowl. 4. Crop of Hooded Vulture Necrosyrtes monachus.

Fig. S. Extensible oesophagus of Red-tailed Hawk Buteo jamaicensis. Fig. 6. Crop of Bobwhite Quail Colinus virginianus. Fig. 7. Oesophagus of Ruby-throated Hummingbird Archilochus colubris. Fig. 8. Crop of Rock Dove Columba liuia. Fig. 9. Stomach region of Double-crested Cormorant Phalacrocorax auruus. Fig. 10. Stomach region of American Woodcock Scolopax minor. Fig. 11. Stomach region of Pink-footed Goose Anser brachyrhynchos. Fig. 12. Caeca of Yellow-billed Cuckoo Coccyzus amencanus. Fig. 13. Caeca of Coot Fulica atra. Fig. 14. Caeca of Great Horned Owl Bubo virginianus. Fig. 15. Rudimentary caeca of Chestnut-sided Warbler Dendroica pensyluamea. Fig. 16. Caeca of Snipe Gallinagogallinago. Fig. 17. Caecum of Heron Ardea cinerea. Fig. 18. Caeca of Great Black-backed Gull Larus marinus. Fig. 19. Transverse section of part of the ileum. Fig. 20. Detail of the structure of a villus from the ileum (see inset on Fig. 19).

Alimentary system

\\

v

b.b

Figs 1-20. Diagrammatic representations of aspects of the morphology of the avian alimentary tract. In all figures, the scale bar represents about 20 mm and the solid arrows show the usual direction of intestinal flow. Abbreviations: b.b. brush border; b.v. blood vessel; c. caecum; cl,

cloaca; co. colon; d. duodenum; e.c. epithelial cell; g.c. gland cell; i. ileum; l. lumen; l.p. lamina propria; m. mucosa; sm. submucosa; mu, muscularis; p. pancreas; pv. proventriculus; s. serosa; u. ureter; v. ventriculus.

11

12 Alimentary system

In birds food is moistened and swallowed quickly. The salivary glands undoubtedly produce mucus, but evidence suggests that the secretion of salivary amylase varies from species to species. The lining of the oesophagus also produces a lubricant and the food may pass straight into the proventriculus or be diverted and stored in the crop or in the extensible oesophagus. The period for which food is retained in the crop. is. very variable but microbial fermentation processes may occur when It ISdelayed fo; several hours. The crop of the HOATZIN Opisthocomus ho~tzin is muscular and is capable of squeezing the sap out of the leaves on which the bird feeds. The control of motility in the anterior part of the tract allows the direction to be reversed and regurgitation is an important process in many birds (see PARENTAL CARE; PELLET). On entering t~e p~oventriculu~, the food is soon mixed with more mucus, hydrochlonc acid and pepsm which begins the digestion of protein. This phase of digestion continues in the ventriculus where the muscular contractions break up the food and ensure a thorough mixing of pepsin with its substrate. The activity of pepsin depends on a low hydrogen ion concentration (c. < pH 3.5); the hydrogen ion concentration in the oesophagus and post-pyloric portion of the tract is usually maintained at about pH 6.5 to 7.5 which favours the activity of the other enzymes involved in digestion. . The partially digested food or chyme is forced out of the ventnculus through the pylorus into the duodenum where the main phase of chemical digestion begins. Under hormonal control, pancreatic juice and bile e.nter the intestinal lumen. Pancreatic juice contains a large amount of bicarbonate, which neutralizes the proventricular acid, and several enzymes including (in the domestic fowl) amylase, cholesterol esterase, esterase, lipase, phospholipase, trypsin and chymotrypsin. Bile contains the sodium salts of cholic, chenodeoxycholic and lithocholic acids. These salts are detergents which emulsify fats prior to enzymic hydrolysis by esterases, lipases and phospholipases, and also facilitate the abs~rptio? of the end products of fat digestion. Pancreatic amylase together with vanous disaccharidases synthesized by the mucosa hydrolyse certain carbohydrates to their constituent sugars which are then absorbed. Simultaneously, the hydrolysis of the polypeptides, which were .liberated by t~e action of pepsin, to amino acids is completed by the trypsm, chymotrypsin and peptidases. The chyme continues to be propelled rather more slowly along the tract and gradually indigestible materials accumulate posteriorly. Cellulose and other complex carbohydrates often form the major proportion of the contents of the large intestine together with many micro-organisms. Some of the indigestible material together with urine from the cloaca (Fig. 3) are forced by retroperistalsis into the caeca where as many as lOll microbial cells per g of caecal contents may be found. The caecal bacteria of some birds, particularly galliforms, degrade plant products to volatile fatty acids which may contribute significantly to the energy budget of the bud. In other respects, the evidence for the contribution of the intestinal flora to the nutrition of the bird is equivocal; birds given an adequate diet can be reared in isolators in a germ-free state. Similarly, the functions of the caeca are not fully understood. Caecal tissue may be involved in water reabsorption which also occurs in the colon, and in the immune responses. However, domestic birds continue to grow and develop normally in the laboratory after surgical removal of the caeca. Certain parts of the anterior alimentary tract have acquired secondary functions during the evolution of some birds. The cells of the crop lining in both sexes of pigeons liberate a nutrititive substance which is regurgitated and fed to the squabs (see CROP MILK). The cell~ of the P!Oventriculus in some species of PETREL probably produce the oily secretion which is vomited and considered to have a defensive function. Secretions from the salivary glands are used to build the nests of various species of cave swiftlet (see EDIBLE NESTS). Generalizations about the form and function of the avian alimentary tract are difficult to make. First, the ecological relationships and diets of birds are very diverse. Secondly, most knowledge of digestive physiology in birds has been obtained from studies on the domestic fowl. Thirdly, for any given species we may expect that the amount of food and water consumed, the motility of the tract and the digestive and absorptive processes will depend on (1) the bird's age, sex and metabolic rate, (2) its nutritional, physiological and reproductive status, (3) the availability of food, (4) the physical and chemical properties of the food and (5) various environmental factors. (A.N.W.) D.W.T.C. Crompton, D.W.T. & Nesheim, M.e. 1976. Host-parasite relationships in the alimentary tract of domestic birds. Adv. Parasit. 14: 95-194. Dorst, J. 1971. The Life of Birds, 1. London.

Sturkie, P.D. 1976. In Sturkie, P.O. (ed.), Avian Physiology, (3rd ed.): 185-209. New York. Welty,J.C.1962. The Life of Birds. Philadelphia and London. Ziswiler, V. & Farner, D.S. 1972. In Farner, D.S. & King, J.R. (eds.). Avian BiologyII: 343-430. New York & London.

ALLANTOIS: see DEVELOPMENT, EMBRYONIC. ALLELE: see GENETICS. ALLELOMIMETIC: term sometimes applied to similar behaviour on

the part of two or more individuals when some element of mutual stimulation is involved.

ALLELOMORPH: sometimes abbreviated to 'allele' (see GENETICS). ALLEN'S RULE: that among the forms of a polytypic species, exten-

sions of the body (in birds, chiefly bill) tend to be longer in the warmer parts of the total range and shorter in the cooler parts. It is ge~erally accepted that the adaptive basis for this rule is reduction of heat loss In cold climates (see ADAPTATIONS, ENVIRONMENTAL; ENERGETICS).

ALLOCHRONIC: existing at different levels of geological time (applied to two or more forms)--contrasted with

SYNCHRONIC.

ALLOCRYPTIC: adventitious concealing coloration, as distinct from 'cryptic' coloration adapted to the purpose.

ALLOMETRY: the differential growth of one part of the body in relation to the whole or to other parts (see SIZE). ALLOPATRIC: mutually exclusive geographically (usually applied to taxonomically related populations}-contrasted with SYMPATRIC; also used in the substantive form, ALLOPATRY. Species whose geographical ranges are closely contiguous but do not overlap are generally referred to as PARAPATRIC.

ALLOPREENING: term that has been introduced (with 'autopreening' as antonym) for preening of one bird by another bird, usually of the same species and commonly a mate-often mutual (see COMFORT BEHAVIOUR).

Allopreening of white-eyes Zosterops. (N. Kikkawa).

ALLOSEMATIC: see under SEMATIC. ALLOSPECIES: one of the constituent species of a SUPERSPECIES. ALLOTYPE: term sometimes applied to a paratype of the opposite sex from the holotype (see TYPE

SPECIMEN).

ALPHA-CHLORALOSE: see PESTS,

BIRDS AS; TOXIC CHEMICALS.

AL TERNATE PLUMAGE: in species which have two different plumages a year, the alternate plumage is usually that worn during the breeding

Ambivalence

season. The term is modern American usage, its equivalent in classical terminology is nuptial plumage (see PLUMAGE).

AMAKIHI: Loxops virens (for family see HAWAIIAN

ALTITUDINAL DISTRIBUTION: distribution in accordance with height above sea-level in a particular area. See also MONTANE.

PARROT).

13

HONEYCREEPER).

AMAZON: substantive name of Neotropical Amazona spp. (see

ALTITUDINAL MIGRATION: a local movement in which the displacement is principally a matter of altitude. ALTRICIAL: helpless when hatched (see YOUNG BIRD). AL TRUISM: in its biological usage defined as an act that has the effect of increasing the chance of survival (or more precisely, FITNESS) of another individual, but decreases the chance of survival of the altruist. Avian examples of altruism include any form of care of the young, whether the 'parent' in question is the young bird's genetic parent, a foster parent (see BROOD-PARASITISM) or some other bird (as occurs when there are helpers at the nest; see CO-OPERATIVE BREEDING). An altruistic act may be purely behavioural, such as feeding or protecting the young, or it may involve some physiological or anatomical trait. A bee's sting, for example, is an altruistic adaptation, for the bee dies after stinging, but benefits its colony. In its everyday usage for describing human behaviour, altruism not only means that some benefit is transferred to the recipient at a cost to the altruist, but also that the altruist intended to be kind. The subjective motive of the altruist is ignored in biology, and there is no reason to suppose that an animal intends to produce a biologically altruistic effect when it does so. If a cuckoo's foster parent really knew the effects of its action, it would probably stop feeding the cuckoo. Evolution. The existence of altruism is a paradox for the Darwinian theory of evolution, which claims that those individuals that reproduce most will come to prevail in the population. This theory predicts that altruism, in which by definition the recipient reproduces more than the altruist, should not exist. Four solutions to the paradox have been suggested, of which three are at present thought valid. One solution is the theory of GROUP SELECTION. Although altruism is not beneficial to the individual altruist, it does benefit the group of altruists and recipients as a whole; therefore a group containing altruists would produce more offspring in all than a group that lacked altruists. So by inter-group selection, altruism could come to prevail. Group selection is thought not to have much effect in nature because, when modelled precisely, it is found to require conditions that are unlikely to exist very often, and it is very open to 'cheating' . The three mechanisms that can account for altruism are named kin selection, reciprocal altruism and manipulation. KIN SELECTION, an idea mainly developed by W.D. Hamilton, can explain altruism between genetically related individuals. Parents are selected to feed their young because by doing so they are helping an individual that is genetically similar. Altruism between other kinds of genetic relatives can be selected for exactly the same reason. So kin selection has probably been important in the evolution of some species with helpers at the nest. In some of these it has been confirmed that the helpers are close relatives. Reciprocal altruism can explain altruism between genetically unrelated as well as related individuals. If an individual can expect to be repaid in the future for acting altruistically now, then it would be selected to be altruistic. Reciprocal altruism will only be favoured by natural selection in species which are sufficiently intelligent to recognize particular individuals. In other species, cheaters (who receive altruism but do not repay) will not be discriminated against, and the system will break down. This theory cannot account for the initial spread of an altruistic trait, since the mechanism relies on an altruist encountering a reciprocator. The altruism of some birds to brood parasites is presumably explained by manipulation. The parasite is in some way able to deceive, or manipulate, its foster-parent into feeding it. Although these mechanisms by which altruism might evolve have been identified, few cases of altruism have been studied in sufficient detail for it to be known which mechanism was responsible for its evolution. M.R. Dawkins, R. 1976. The Selfish Gene. Oxford.

ALULA: see WING. AMADINI: see ESTRILDID FINCH.

AMBIENS: a muscle of the leg (see MUSCULATURE). The presence or absence of this has been used as a taxonomic character. Garrod (1874) even proposed to divide birds into two subclasses, Homalogonatae ('typicallykneed', i.e. ambiens present) and Anomalogonatae (ambiens absent), but his classification produced too many inconsistencies in relation to other characters and was soon abandoned. The ambiens is a reptilian feature and, broadly speaking, is present in what we regard as the more primitive groups of birds and absent from the more highly developed, including the Apodiformes and the Passeriformes. It may be noted that the ambiens is present in the Falconiformes but not in the Strigiformes; and also that differences in this respect occur within certain groups, notably the Psittacidae and the Columbidae. AMBIVALENCE: term applied to behaviour that is the outcome of two (or more) conflicting tendencies, such as approach and avoidance, or attacking and copulating with the partner. Ambivalent motivation is present in many social interactions. For instance, among Gannets Sula bassana, in which the male is exceptionally aggressive towards the female even in well established pairs, the male bites the female's nape during copulation, revealing the presence of aggressive as well as sexual tendencies during this act. During phylogeny, ambivalent behaviour has given rise to social displays used in communication. Some displays are a mosaic of elements of the conflicting tendencies. The 'upright posture' of the Herring Gull Larus argentatus, used in threat, includes a downward pointing bill and upward stretched neck (preparations for a pecking attack) and raised carpal joints (preparation to deliver a wing blow) combined with signs of fear, a withdrawn neck and flattened plumage. Since the posture combines elements of both tendencies, it is termed formally ambivalent. Where the elements of the conflicting tendencies are shown in rapid alternation (for instance in 'pendulum fights' of songbirds at a territorial boundary) the term successive ambivalence may be used. Where behaviour involves only the elements which are common to both conflicting tendencies, the term compromise activity is used. For example, in a conflict between flying towards and sidling towards an object, buntings (Emberiza spp.) show tail flicks, a component of both flying and sidling. The motivation of an ambivalent movement may be inferred firstly by scoring the overt behaviour shown in rapid alternation with it ('time score method'). For instance, agonistic postures tend to alternate with attack and escape rather than with feeding or preening; but where displays alternate with other displays, this method is not helpful. Secondly, the context in which the behaviour is shown can be examined. If stimuli for two incompatible types of behaviour are known to be present, it is likely that the behaviour seen is ambivalent, and both 'natural experiments' and laboratory experiments can provide evidence of this sort. Thirdly, the orientation adopted during the act may also provide an indication of subtle variations in motivation. Finally, where a movement is formally ambivalent, the form itself may provide clues to its motivation, although the possibility that the movement has become divorced from its original motivation during the course of evolution must be considered. (Comparisons between species using this type of evidence provided the first indications of the importance of ambivalence in social behaviour.) Physiological work, in which areas of the brain were stimulated electrically, had been expected to provide a further line of evidence, but has proved difficult to interpret; it has not provided unequivocal support in any instance for analyses based on the behaviour alone. The generality of the actual behavioural tendencies involved may vary considerably. Some agonistic postures depend specifically on the arousal of attack and escape tendencies, others on the arousal of the tendency to attack together with any incompatible tendency. 'Beak hiding' in the Kittiwake Rissa tridactyla occurs when fear interacts with any tendency towards approach or staying. In the buntings described above, the conflict was between tendencies to move towards the object in alternative ways. The presence of ambivalence in some social interactions (for instance, during a fight) is easy to understand, but the reasons for its presence in others (such as mating) are less obvious. One possibility is that it is a consequence of the evolutionary origin of the signal postures used, which constrains future evolution much as the pentadactyl limb constrains the

14 America

ANI: substantive name ofCrotophaga spp. (see CUCKOO).

evolution of wings or flippers. Alternatively, it may represent a compromise between conflicting selection pressures on the individual. For example, aggressive courtship by the male dove Streptopelia roseogrisea (= 'risoria') delays ovulation, but may confer advantages in preventing cuckoldry. (N.T.) P.G.C.

ANIMAL KINGDOM: in the perspective of the Animal Kingdom as a

Baerends, G.P. 1975. An evaluation of the conflict hypothesis as an explanatory principle for the evolution of displays. In: Baerends, G.P., Beer, C. & Manning, A. (eds.). Function and Evolution in Behaviour. Oxford. Blurton-Jones, N.G. 1968. Observations and experiments on causation of threat displays of the Great Tit (Parus major). Anim. Behav. Monographs 1:75-158. Delius, J.D. 1973. Agonistic behaviour of juvenile gulls, a neuroethological study. Anim. Behav. 21:23~246.

Parker, T.J. & Haswell, W.A. 1962. Text-book of Zoology. Vol. 2 (7th edn, revised by Marshall, A.J.). London. Young, J.Z. 1981 (3rd edn.). The Life of Vertebrates. Oxford.

AMERICA: see NEARCTIC REGION; NEOTROPICAL REGION. Note that the term 'Middle America' is now much used to designate the area comprising Mexico, Central America, and Panama (the last being by political history part of South America), and sometimes including the West Indies. This usage has the consequence that 'North America' is often used in ornithologicalliterature as excluding Mexico.

ANIANIAU: Loxops parva (see HAWAIIAN HONEYCREEPER). whole, the taxonomic position of birds may be defined as: Sub-kingdom Metazoa, Phylum Chordata, Subphylum Vertebrata, Class Aves (see AVES).

ANISODACTYL: having three toes directed forwards and one (hallux) backwards (see LEG).

ANKLE: the intertarsal joint-sometimes popularly mistaken, in birds, for the knee (see LEG; SKELETON, POST-CRANIAL).

ENGLISH.

ANKYLOSIS: a stiffening or fixed union of a joint, a natural feature of development in some joints, but also occurring as a pathological condition of joints that are normally movable (see SKELETON, POST-CRANIAL).

AMETHYST: Philodicemitchellii(for family see HUMMINGBIRD).

ANOMALOGONATAE: seeAMBIENS.

AMINO-ACIDS: see ENERGETICS.

ANOMALOPTERYGIDAE: see STRUTHIONIFORMES; MOA.

AMNION: see DEVELOPMENT, EMBRYONIC.

ANOSMATIC: without olfactory sense (see SMELL).

AMNIOTA: term embracing reptiles, birds, and mammals.

ANSERANATINAE: see DUCK.

AMNIOTIC CLOSURE: term for the protective sealing of the eyes and ears during the first few days of life in some birds, the function being analogous to that earlier performed for the embryo by the amnion (see GROWTH; YOUNG BIRD).

ANSERES: see below.

AMERICAN USAGE: as regards vernacular names, see under NAME,

AMPHIRHIN AL: see NARIS. AMPULLA: term for a vesicle, among other things the dilated end of a semicircular canal in the labyrinth of the ear (see HEARING AND BALANCE).

ANABOLISM: see ENERGETICS. ANALOGUE: a structure adaptively similar to another but of basically different nature-compare HOMOLOGUE. ANATIDAE: see under ANSERIFORMES; DUCK. The family comprises birds variously designated as 'ducks', 'geese', and 'swans'; but the application of these primary English names cuts across the taxonomic arrangement. For all, see under DUCK.

ANATOMY: bodily structure; also the science of this. By derivation, the term relates to internal structure as revealed by dissection, as contrasted with external form (see MORPHOLOGY); but the two terms have come to be used almost synonymously. Special branches of anatomy, such as osteology, deal with particular systems of the body; 'histology' refers to the microscopic structure of the tissues; 'morbid anatomy' is diseased structure, or the branch of pathology dealing with this. The structure of birds is dealt with in this work under the names of the systems, organs, and tissues of the body, and under other special heads.

ANCONEAL: pertaining to the elbow; sometime used with reference to the whole dorsal surface of the wing. ANGEL: see RADAR. ANGULAR: a paired bone of the lower jaw (see SKULL).

ANHIMAE; ANHIMIDAE: see under ANSERIFORMES; SCREAMER. ANHINGA: used (America) as vernacular name of Anhinga anhinga (see

DARTER).

ANHINGIDAE: see under PELECANIFORMES; DARTER.

ANSERIFORMES: an order, alternatively 'Anseres', comprising 2 suborders: Anhimae, Anseres; 2 families: Anhimidae (SCREAMER), Anatidae (DUCK). Although these groups show affinities in their anatomy, they are very different in external appearance and mode of life. Among the most obvious characters common to both are the unspotted eggs and the nidifugous young clad in thick down. In the Anseres (in the subordinal sense) the front 3 toes are connected by a web and the small hind-toe is placed high; in the Anhimae there is only a slight web, and the hind-toe is long and on the same level as the others. In the Anseres the bill and tongue have special characteristics. ANTAGONISTIC DISPLAY: see DISPLAY. ANTARCTIC: usually defined as the continent of Antarctica (including

the Antarctic Peninsula), its offlying islands, sea ice and surrounding ocean and islands northwards to the Antarctic Convergence, the circumpolar boundary where north-flowing Antarctic surface water sinks beneath warmer, south-flowing sub-Antarctic water. At the water surface this shows as a zone in which temperature changes by 3°C in half a degree of latitude and whose mean position is usually constant to within 100 km, roughly following the 500S parallel in the Atlantic and Indian Oceans but lying between 55°S and 62°S in the Pacific Ocean. Biologically the Antarctic can be divided into several regions. The continental Antarctic region comprises the central high plateau and coastal fringe zones, the latter including Peter I 0ya, Scott and Balleny Islands and the east coast of the Antarctic Peninsula south of c. 64°S. The maritime Antarctic region includes the west coast of the Antarctic Peninsula and its offshore islands to c. 70oS, Bouveteya and the South Shetland, South Orkney and South Sandwich Islands. The sub-Antarctic region includes South Georgia and Heard Islands, lying just south and Kerguelen and Macquarie Islands lying just north, of the Convergence. lIes Crozet and the Prince Edward Islands, although further north, are close enough to the Convergence for the sinking cold Antarctic water to upwell against them. Still further north (and not far south of the sub-tropical Convergence, the northern limit of sub-Antarctic surface water) are the temperate oceanic islands of the Tristan da Cunha group (including Gough Island) and St. Paul and Amsterdam Islands; these have much.in common with the New Zealand shelf islands (e.g. Auckland, Campbell and Chatham Islands) and the Falkland Islands.

Antarctic

Land climate and vegetation. Of the 14.3 million km 2 surface of the Antarctic Continent most is covered with a thick sheet of glacial ice at a mean elevation of about 2,000 m with peaks rising to 5,140 m. Only about 8,OOOkm2 of rock and soil are exposed, mainly on the Antarctic Peninsula and around the edge of the continent. Of this much is either too inhospitable or too far from the sea to be suitable for birds, which principally use rock ledges, rock debris, shingle beaches and fast sea ice for breeding. The continental climate is cold, dry and windy. Temperatures on the continental plateau rarely exceed - 20°C in summer and the world's lowest temperature record of -89.2°C was made at an inland site. However, mean annual temperatures at coastal sites range from -10°C to -12°C (summer means -1°C to - 3°C; winter means 16°Cto 17°C).Precipitation is virtually all as snow and rarely more than 40 em yr- 1 on the coast, less inland where some areas are complete deserts. Winds are strong and reach a mean velocity of 72 km hr " ! on the Adelie Coast with gusts of over 240kmhr- 1• In the maritime Antarctic region the climate is milder, being cold, wet and windy. Mean temperatures from December to March may be at or just above freezing, precipitation reaches 100em yr- 1 and mean wind velocity rarely exceeds 30 km hr- 1• In protected areas at low altitudes a modified feldmark vegetation exists, dominated by mosses and lichens, the former developing, under favourable conditions, into moss peat banks over I m deep. Numerous crevices and ledges are available for birds but the ground is unsuitable for burrowing although storm petrels are often abundant in scree and debris slopes. Rocky promontories and beaches provide many breeding sites, especially for penguins. At the sub-Antarctic islands mean monthly air temperature remains above freezing for at least half the year (annual range - 2°C to goC). Precipitation is usually between 100-150 em, mostly as rain in summer, and often as snow in winter, and cloudy, windy weather with frequent mist and low cloud is typical. The Atlantic and Indian Ocean sectors are generally colder than the Pacific at the same latitude, partly due to the eccentric position of the Antarctic Continent. At these islands moss and lichen communities are abundant on higher ground (which rises to 2,900m at South Georgia) but at lower elevations thick vegetation and often deep, peaty soilsprovide shelter, nest sites and nest material for both surface and burrow-dwelling birds. The most important vegetation type is tussock grassland, usually dominated by species of Poa, which may form a continuous cover to 2 m high. Short grass and rush tundra meadows are frequent on flat land and carpets of large-leaved perennial herbs may occur in sheltered places. Peat bogs, usually with small lakes and ponds, are present. In contrast to more southerly areas where ice abrasion and other factors result in a biologicallyimpoverished intertidal zone, sub-Antarctic islands have a rich intertidal fauna, and luxuriant coastal kelp beds also contribute to tideline debris. Oceanography. One important feature is the Antarctic Convergence where Antarctic surface and sub-Antarctic intermediate water meet. Below the latter is a southward flowing layer of warm circumpolar deep water. This rises close to the surface not far from the edge of the Antarctic Continent, in the area of the Antarctic Divergence, the boundary between the east flowing currents near the continent and the west flowing currents of the main Antarctic Ocean. This divergence is a major upwelling area and the abundant nutrients brought to the surface there facilitate vast phytoplankton blooms in the austral summer. Although the waters to the south of.the Antarctic Convergence are generally considerably richer than temperate waters, and coastal waters exceptionally so, there are areas of the open ocean, especially in the Pacific, that are of low productivity. The key organism nourished in the highly productive regions is krill, a collective term for crustaceans of the genus Euphausia, particularly E. superba. As the food either directly, or indirectly through many fish and squid, of most Antarctic whales, seals and birds, it is the hub of the Antarctic food web and a vital factor in sustaining the vast animal biomass of the Antarctic Ocean in summer. Avifauna. The birds are dominated by representatives of those two most marine of all orders, the PENGUINS and PETRELS. Within the Antarctic' zone and at the islands near the Antarctic Convergence the breeding species comprise 7 penguins (Spheniscidae), 6 albatrosses (Diomedeidae), 18 petrels (Procellariidae), 3 storm-petrels (Hydrobatidae), 2 diving petrels (Pelecanoididae), 2 shags Phalacrocorax, 2 skuas Stercorarius, 2 terns Sterna, 1 gull Larus and 2 sheathbills Chionis plus 4 ducks Anas (2 at South Georgia, one each at Kerguelen and Macquarie), a pipit Anthus antarcucus (South Georgia only), Starling Stumm vulgaris (self-introduced), Redpoll Carduelis flammea and an introduced rail

15

Gallirallusaustralis at Macquarie Island (where another rail Hypotaenidia macquariensis and a parakeet Cyanorhamphus nouaezelandiae erythrotis became extinct by 1894 and 1911 respectively). Farther north at the temperate sub-Antarctic islands a number of other birds occur, principally shearwaters Puffinus, other gadfly petrels Pterodroma and additional land birds, particularly at the Tristan da Cunha group and the Chatham Islands. The most important boundaries affecting seabird distribution are the Antarctic Convergence and the northern limit of pack ice. However, as there are relatively few suitable breeding sites for seabirds in Antarctic areas, few species are confined, even in the breeding season, to only one of the resulting circumpolar zones. Thus as a breeding species only the Antarctic Petrel Thalassoica antarctica is restricted to the cold Antarctic sub-zone although the Adelie Penguin Pygoscelis adeliae, Snow Petrel Pagodroma nivea, and particularly the Antarctic Skua Catharacta maccormicki and Emperor Penguin Aptenodytes forsteri have by far their greatest concentrations here. Only II species have been recorded breeding in this zone; the 5 mentioned above, plus Chinstrap Penguin Pygoscelis antarctica, Southern Giant Petrel Macronectes giganteus, Antarctic Fulmar Fulmarus glacialoides, Cape Pigeon Daptum capense, Antarctic Prion Pachyptila desolata and Wilson's Storm Petrel Oceanites oceanicus. The maritime Antarctic sub-zone (Antarctic Peninsula and adjacent islands) provides a bridge along which Antarctic and sub-Antarctic species have been able to move on a north-south axis. Chinstrap Penguin and probably Black-bellied Storm Petrel Fregetta tropica are at their most abundant here and at some sites 4 penguins, 5 petrels, 2 storm petrels and 2 skuas occur (together with a sheathbill, shag, gull and tern). At the sub-Antarctic islands, in addition to abundant King Aptenodytes patagonicus, Gentoo Pygoscelis papua and Crested Eudyptes spp. Penguins, the well vegetated areas are extensively colonized by large surface-nesting species (albatrosses and giant petrels Macronectes spp.) and by many species of burrowing petrels. lIes Crozet has the richest avifauna (34 breeding 30 0

300

·Macq •CampbellIs \ SOo_ _ ·AucklandIs Ice edge Sep·Oct Ice edge March

,,

e: '\

rl\~ALANO

~35~---

1500

12QO

W 1800E

(>

AUSTRALIA 1500

Fig. 1. The Antarctic and Sub-tropical Convergences, and apparent mean position of the ice edge in summer and winter.

16 Antarctic

species, including 16 burrowing species), followed by Kerguelen (30 species) and South Georgia and the Prince Edward Islands (26 species). Zonal (i.e. latitude-based) speciation is much more marked than longitudinal (i.e. island-based) differentiation. Thus, except for the large and small forms of Snow Petrel, none of the species of the Antarctic zone shows regional differentiation within this zone. In the sub-Antarctic zone the only clear example is the existence of the Royal Penguin E udyptes chrysolophus schlegeli at Macquarie Island and Macaroni Penguin E.c. chrysolophus at the other cold sub-Antarctic islands. However, part of the taxonomic complexity of the prions Pachyptila is due to the occurrence of morphometrically distinguishable populations at most breeding sites. In contrast there are distinct races of Rockhopper Penguin Eudyptes chrysocome moseleyi, Wandering Albatross Diomedea exulans dabbenena, Cape Pigeon Daption capense australe, White-chinned Petrel Procellaria aequinoctialis conspicillata and Black-bellied Storm Petrel Fregetta tropica melanoleuca at the temperate sub-Antarctic sub-zone islands and wellmarked (but probably essentially clinal) disjunctions in Gentoo Penguin and Wilson's Storm Petrel farther south. There are also several examples of species which doubtless evolved in adjacent zones and which show largely non-overlapping circumpolar distributions but with varying degrees of coexistence. Thus Sooty Phoebetria fusca and Light-mantled Sooty P. palpebrata Albatrosses, Yellow-nosed Diomedea chlororhynchos and Grey-headed D. chrysostoma Albatrosses, Northern Macronectes halli and Southern Giant Petrels, Rockhopper and Macaroni Penguins, Thinbilled Pachyptila belcheri and Antarctic Prions are all respectively northerly and southerly replacement species, although the penguins and giant petrels co-exist fairly extensively at the cold sub-Antarctic islands. Antarctic and Brown Stercorarius lonnbergi Skuas are another 'species pair', with a zone of hybridization in the central Antarctic Peninsula and King Phalacrocorax albiuenter and Blue-eyed P. atriceps Shags are basically zonal taxa which hybridize in southern South America; the status of the Kerguelen Shag P. uerrucosus is uncertain. The New Zealand subAntarctic islands are an important centre of speciation for small albatrosses and crested penguins. Breeding habitat. Most of the seabirds in the region are basically colonial, except for Light-mantled Sooty Albatross and the skuas, gull, terns and sheathbills, which defend isolated nest territories and, in the case of sheathbills and skuas, often feeding territories in penguin colonies. On the Antarctic Continent and Peninsula the smaller petrels are crevice nesters, larger ones using sheltered ledges, while the penguins often choose very exposed sites (including flat sea-ice by Emperor Penguin) as these are frequently associated with wind-assisted early break-out of pack-ice in summer, thus improving access to breeding sites. At the sub-Antarctic islands the tussock grasslands are used by nearly all species: large albatrosses, giant petrels, and Gentoo Penguins in flatter areas, smaller albatrosses usually on steep slopes and burrowing petrels underground in a wide range of conditions of slope, aspect and general topography. Storm petrels mainly nest in cliff crevices, boulder scree and moss banks and the South Georgia Diving Petrel Pelecanoides georgicus only in fine consolidated scree. King Penguins favour flat land usually near glacier moraines, the other penguins utilizing a wide variety of rock and boulder slopes or beaches. General biology. The breeding biology of most Antarctic birds (see especially PENGUIN, PETREL, SHEATHBILL, SKUA) is basically very similar to that of their more temperate relatives. With the short duration of summer in high latitudes most species show high synchrony of breeding events within populations although this is least true of some inshore feeding species (e.g. Gentoo Penguin, Blue-eyed Shag, Antarctic Tern Sterna vittata, some storm petrels). Even so, most larger species, with correspondingly long incubation and fledging periods, commence breeding in early spring and only finish at the end of April, when food stocks are first starting to diminish. Smaller species can be more flexible in their timing and there are several cases of similar species having mutually exclusive chick-raising periods (e.g. Common Pelecanoides urinatrix and South Georgia P. georgicus Diving Petrels, Blue Petrel Halobaena caerulea and Fulmar Prion Pachyptila crassirostris as opposed to all other prions, Antarctic and Kerguelen Sterna virgataTerns). The fulmarine petrels (e.g. Snow, Antarctic and Cape Petrels, Antarctic Fulmar Fulmarusglacialoides and giant petrels) have especially short incubation and fledging periods and this may have been an important factor in determining why most members of this group and not other Procellariidae became successful colonists of the Antarctic Continent. A small number of Antarctic species consistently breed in winter. These are two burrowing petrels of more

northerly sites, Great-winged Petrel Pterodroma macroptera and Grey Petrel Procellaria cinerea, which thus avoid times when their congeners are active, Wandering Albatross, with Royal Albatross Diomedea epomophora the only albatrosses with this strategy, and Emperor Penguin. King Penguin chicks, although remaining in the colony over winter, are only fed very occasionally and this species is essentially a summer breeder. The Emperor Penguin, however, raises its chick through the high Antarctic winter, under the most extreme conditions of any bird, and a number of ecological, physiological and behavioural adaptations combine to make this possible. Most other Antarctic seabirds show fewer special adaptations to cope with the rigorous environmental conditions of the region. Like seabirds elsewhere they have thick layers of subdermal fat and these are especially well developed in penguins, which also have a particularly dense covering of overlapping feathers and a highly developed vascular heat exchange system in the flippers and legs. Selection of nest sites that are sheltered but not prone to blockage with snow is often critical. Climatic factors also strongly influence breeding success, either causing chick loss directly through chilling in very cold weather or indirectly by causing poor feeding conditions for adults or delaying the onset of breeding so that adults feed and chicks fledge at less favourable times. Native predators are of much less importance although locally sheathbills and skuas may be responsible for appreciable losses of eggs and small chicks. Burrowing petrels, however, have been drastically affected on many sub-Antarctic islands by introduced rats (taking eggs and chicks) and on some islands by cats (taking chicks and adults). In many areas, particularly on Macquarie Island (where erosion induced by rabbits is also a problem) and parts of lIes Crozet and Marion Island, burrowing petrels are virtually restricted to offshore predator-free islands. On South Georgia the pipit and South Georgia Pintail Anas georgica have been similarly affected by rats in many areas. For many species the full rigours of the Antarctic climate are avoided by moving north in winter, whether to the pack-ice edge (Adelie Penguin, Snow and Antarctic Petrel) or, like most species, to between the Antarctic and Sub-tropical Convergences, with several species (e.g. giant petrels, Wandering Albatross, Black-browed Albatross Diomedea melanophris) reaching at least 35°S, particularly off coastal South America and South Africa and in the Tasman Sea. Juvenile dispersal is wide, and best documented for albatrosses and giant petrels where birds reach low latitudes in all Southern Hemisphere oceans. In many species both immatures and adults probably not infrequently encircle the globe in the zone ofthe West Wind Drift. A few species are transequatorial migrants: Sooty Shearwater Puffinusgriseus, Great Shearwater Puffinusgravisand Mottled Petrel Pterodroma inexpectata all from mainly temperate sub-Antarctic sites, and Wilson's Storm Petrel and also, in the reverse direction, Arctic Tern Sterna paradisaea which is a widespread austral summer visitor to the Antarctic Ocean. Population dynamics. Antarctic seabirds, like those elsewhere, are generally long-lived and delay breeding until several years old. Mean annual survival of breeding adults of Antarctic seabirds so far studied is around 90-95%, the main exceptions so far being diving petrels (700/0), and most penguins (70-85%). Young birds clearly sustain high losses in the first year or so of life, but even so 45% of an age group of Wandering Albatrosses survive to 5 years of age. Mean life expectancy is correspondingly high and may reach 10-15 years for smaller petrels and 25 years for albatrosses and giant petrels. Maximum values are uncertain but there are proven field records of 16 year old Adelie Penguins, Wandering Albatrosses over 30 and Snow Petrels over 35 years of age. Most petrels commence to breed from age 4-6 but diving petrels do so from age 2 and Wilson's Storm Petrel from age 3, whereas albatrosses may commence at age 4-9, depending on species and location. Adelie and Emperor Penguins breed from age 3, King Penguins from age 4 but Royal Penguins not until 5. One interesting feature of some Antarctic seabirds is their inability to breed in a season following that in which they raised a chick. This is not unexpected in King Penguins, Wandering and Royal Albatrosses which take nearly a year (or more) to raise a chick, but also occurs in Grey-headed (but not Black-browed), and both Phoebetria albatrosses. In these latter cases it is believed also to relate to the very long chick fledging period, itself probably a result of dietary restrictions. Diet and feeding ecology. Terrestrial (and!or tideline-s-especially in winter) invertebrates are important to ducks, sheathbills (particularly Lesser Sheathbills Chionis minor), passerines (especially South Georgia Pipit), Southern Black-backed Gull Larus dominicanus and Kerguelen

Antbird

Tern. Giant petrels, sheathbills and skuas scavenge extensively, particularly in penguin colonies; some Antarctic Skuas, however, take fish or krill at sea. The remaining species are exclusively marine and 4 main types of prey are taken; fish (especially Nototheniidae and Myctophidae), squid, krill and other, smaller crustaceans (amphipods, copepods). Fish are eaten extensively by inshore feeders like Gentoo Penguin and shags, the latter frequenting coastal kelp beds where many fish mature, but more pelagic species, like some albatrosses and Blue Petrel, also take much fish. King and Emperor Penguins, many albatrosses, Procellaria and Pterodroma petrels chiefly eat squid although some Antarctic species are considerably less nutritious than fish or krill. Krill predominates in the diet of most remaining species, especially penguins, and is also taken by many fish- and squid-eating seabirds. Small crustaceans are taken mainly by smaller seabirds e.g. diving petrels, storm petrels and particularly Antarctic Prion which (like the Broad-billed Prions Pachyptila vittata) has a broad, deep bill with a comb-like lamella fringing the upper mandible through which water is expelled to filter out small organisms. Apart from such specialized feeding adaptations, most Antarctic seabirds are either pursuit divers (penguins, shags and, near the surface, diving petrels) or surface feeders. This is done either by pattering along the surface like storm petrels, swooping down like gadfly petrels, plunging (chiefly terns) or, like most species, seizing prey while sitting on the surface. Most of the last type of feeding is probably done at night when krill and its associated predators reach the surface. Even for the rich and diverse seabird concentrations at sub-Antarctic islands, differences in diet, feeding technique and foraging range appear to act to reduce direct competition for food in summer, especially between related species. In winter, those that remain in high latitudes are chiefly fish and squid eaters as crustacean prey is greatly reduced in availability. In terms of biomass and consumption penguins are the dominant Antarctic group with vast Adelie Penguin colonies around the coast of Antarctica, huge Chinstrap Penguin concentrations on the Antarctic Peninsula and adjacent islands and great numbers of crested penguins at the sub-Antarctic islands (there may be 10 million Macaroni Penguins in the South Georgia population alone). As most eat krill, it is not surprising that penguins may account for 75% of food consumed by Antarctic seabirds and in total this may approximate to krill consumption by present day Antarctic whale stocks and be not too far short of that by Antarctic seals; seabirds are thus important predators of the marine resources of Antarctic seas. (B.B.R.) I.P.C. Ainley, D. G., O'Connor, E. F. & Boekelheide, R.J. 1984. The marine ecology of birds in the Ross Sea, Antarctica. Ornithological Monographs, No. 32. A.O.U. Carrick, R. & Ingham, S.E. 1970. Ecology and population dynamics of Antarctic seabirds. In Holdgate, M.W. (ed.), Antarctic Ecology: 505-525. London & New York. Croxall, J.P. 1983. Seabirds. In Laws,R.M. (ed.), Antarctic Ecology. vol. II. London & New York. Watson, G.E. 1975. Birds of the Antarctic and Sub-Antarctic. American Geophysical Union. Washington.

ANTBIRD: substantive name, referring to the habit of following army ants, of some of the 236 species of 53 genera in the large Neotropical family Formicariidae (Passeriformes, suborder Tyranni); in the plural, general name for the family. Species of this family have radiated so as to fill many forest niches, occupied by many different families on other continents. 'Gnateaters' (9 species, 1 genus, sometimes placed in the family Conopophagidae-see GNATEATER) are rotund and short-tailed little birds that hop or cling on or near the forest floor much like small 'antpittas' (38 species, 5 genera). 'Ant-thrushes' (9 species, 2 genera) walk rail-like on or near the forest floor, pounding their lifted tails as they go. Other formicariids, from warbler-like tiny 'antwrens' and small 'antvireos' to hook-beaked large 'antshrikes,' occur from the forest floor to the canopy. Characteristics. Antbirds vary in size from 8 to 36 em, the longest and perhaps largest being the 154 g Giant Antshrike Batara cinerea. Most have dark red eyes, becoming bright vermilion in 'fire-eyes' (Pyriglena). A few have pale or yellow eyes. Bare green, blue or red areas (the last in P hlegopsis, the 'bare-eyes') sometimes surround the eye and form giant 'eye-spots', which glow like eyes of huge mammals in the forest undergrowth. One species (Gymnocichla nudiceps) has a bare blue crown and forehead as well as face. Colour patterns are frequently striking, being varied combinations of black, brown, rufous, white, or greenish to yellowish. Females are often duller than males, with white or brown replacing black areas; but sexes are usually alike in bare-eyes, ant-thrushes, and antpittas, Nestling fire-eye

17

Black-faced Ant-thrush Formicarius analise (C.E.T.K.).

males are black, females brown; but most small young look like adult females or have a dull plumage. Some young males take on the female plumage for nearly a year. The body plumage is usually loose and sparse, becoming long and silky on the lower back and rump; the forecrown is plush and dense in fire-eyes, while several antbirds have erectile crests and one, the White-plumed Antbird Pithys albifrons, a white crest and beard. Many species have concealed white back or shoulder patches, exposed mainly during disputes. The wings are rounded, with 10 primaries, and functional for short flights in dense vegetation rather than for long-distance travel in the open. Tails are short to medium in length, square or rounded, with 12 feathers (8 or 10 in some species). The slender to thick dark bill is often hooked, and is swollen slightly rather than pointed. One 'bushbird' (Clytoctantes alixi) has a laterally flattened bill with semicircular lower mandible, used for slitting stems of banana-like plants; another (Neoctantes niger) has a similar bill that tears into rotten logs in swamps. Legs and feet are slender or strong, pale or dark, while claws are very sharp and curved in forms that cling crosswise on vertical saplings near the forest floor. Habitat. Antbirds live mostly in lowland tropical forests, and 30--50 species can be found in many equatorial forests of the Amazon valley. N umbers of species decline greatly as one goes to more open tropical or subtropical environments, or into swamps or up mountains. Antpittas, however, are more diverse in the Andes than in the lowlands. Except when sunning in a ray of sunlight, antbirds almost never leave the shade even when they live in the forest canopy; at midday few will cross a wide road through the forest, and different species or subspecies occur on the opposite banks of some wide rivers in the Amazon Valley. A few (such as Myrmochanes hemileucus) occur primarily on species-poor islands in the middle of the Amazon and other large rivers, and fly from one island to another without staying on the nearby shores. Others live only in swampy forest or scrub of the seasonally flooded varzeas of the Amazon, and apparently cross rivers readily. Distribution. Neotropical; antbirds range from north-eastern Mexico to Argentina, but are absent from Chile and from the Antilles other than Trinidad and Tobago. Only two species are restricted to Central America; other species that occur there also occur in South America. Populations. Some antbirds, such as the Slaty Antshrike Thamnophilus punctatus in Panama, occupy a hectare or less per pair. Others are less common, for instance the White-plumed Antbird at 1-2 pairs per km 2 near Manaus in central Brazil. All disappear rapidly when forest or other vegetation is cut, so that certain antbirds of south-eastern Brazil (the Slender Antbird Rhopomis ardesiaca, for instance) are threatened with extinction. Probably many other species of antbird will disappear as forests are cut and isolated; some antbird species have already disappeared from one forest reserve, Barro Colorado Island in central Panama. Movements. Hudson reported that the Rufous-capped Antshrike Thamnophilus ruficapillus leaves Argentina in winter, but most species are nonmigratory. Young birds of most species wander locally, while adult

18 Antbird

birds tend to stay on territories. Young females and females that have lost their mates sometimes wander widely. In many species that follow army ant colonies, pairs have large and overlapping home ranges; Whiteplumed Antbirds wander 2-3 km or more through forests at Manaus. Often the pair or individual is dominant over neighbours only in the central area of its home range, an area that corresponds to the territory in less vagile related antbirds (ones that need not follow nomadic ants so widely). Food. Antbirds for the most part capture small insects, spiders, lizards, frogs, and similar animals. Gleaning and short-distance sallies to the lower sides of foliage are common, less often rummaging in dense dead leaves or tossing fallen leaves with swipes of the side of the bill or by picking them up with the bill. Scratching with the feet is not recorded. Giant Antshrikes have been seen attacking small birds in mist nets. Gnateaters occasionally eat small fruit, but fruit-eating is rare in the family. Ants are rarely eaten, except larvae taken when ants flee a nest at the approach of army ants; in this case the adult ants are thrown away and the larvae they carry are retained. Only a few antbirds (notably Cinereous Antshrike Thamnomanes caesius) are good flycatchers, but sometimes individuals capture winged ants flying from a nest. Some 28 species regularly follow army ants for prey flushed by them. Many other antbirds, as well as many species in other bird families, occasionally follow army ants. Sometimes an antfollowing bird follows domestic pigs or herds of white-lipped peccaries; and one Bicoloured Antbird Gymnopithys bicolor came to follow the Costa Rican naturalist Alexander Skutch when he stirred the leaf litter with a stick. The two ant species followed regularly are both 'swarm raiders,' which form wide phalanxes on the forest floor or up tree trunks in lowland Neotropical forest: Eciton burchelli and Labidus praedator. Swarm raiders flush large numbers of cockroaches, spiders, and other small animals that are snapped up by waiting birds. Typically the ant-following aritbirds cling crosswise on slender vertical saplings just above the ants and dart briefly to the ground for prey. Some antbirds, such as hopping Blackcrowned Antpittas Pittasoma michleri and walking ant-thrushes Fonnicarius spp., wander on the ground on the outskirts of an advancing swarm. The Scale-backed Antbird Hylophylax poecilmota of equatorial South America can cling horizontally to vertical thick trunks, a type of perch usually occupied only by ant-following woodcreepers, and hence finds places over ants despite the aggression of larger antbird species. Behaviour. Most antbirds form pairs that last for life, with rarely a divorce. White-plumed Antbird females, however, rapidly leave mates to care for single young, and find another male so as to start a new nest. Young birds occasionally stay with their parents for some months or years, although none are known to help with later nestings. Clan formation in Ocellated Antbirds Phaenostictus mcleannani involves the occasional association of sons and grandsons with a pair, the male offspring bringing back mates from other clans. At times the members of a clan cooperate briefly in attacking intruders from another clan. Antbirds form the centres of many of the mixed-species flocks of insectivorous birds that wander through Neotropical forests. These flocks, unlike the flocks around army ants, do not feed at concentrated food sources. Fifty species or more may be present, including 20-30 species of antbirds. Each species forages differently, some peering in dead curled-up leaves and others in green foliage. Some stay in the canopy, others in the subcanopy, midlevels, lower midlevels, lower levels, or on the ground. Others occupy only dense foliage, such as around vine tangles; and the whole flock is likely to slow down and search intensively in the dense foliage around a light gap where a forest tree has fallen. If a hawk appears, alarm calls from the most alert flycatchers warn even the species that forage inside dense foliage or in dead leaves. Certain flycatching antshrikes (Thamnomanes spp.), centres of Amazonian flocks, are extremely alert and noisy and hence are followed by other species, which then flush food for the antshrikes. Regular flock members often have the same territories (but defend only against their own species when meeting a neighbouring flock), roost together, and preen together. Other species join the flocks less readily or wander between one flock and another. Ground and low-level ant birds tend to ignore flocks, apparently depending on protective coloration because they forage too slowly to keep up with birds gleaning through sparser foliage high above the ground. Antbirds usually scratch the head over the wing. Alarm behaviour often produces upward 'flicking' of the tail or downward 'pounding' of the tail, depending on the species. Voice. Antbirds have simple songs, mostly resonant series of whistles or chattering notes. Both sexes sing; the female sometimes has a song unlike

that of the male. Some, such as the Ferruginous Antbird Mynnecizaferruginea, have pleasant short warbles. The strangest vocalization is that of the White-plumed Antbird, a series of several hundred buzzy zee notes

given for up to 3 min while performing a wing-waving display. Call notes of antbird species tend to be very varied. There is often a sharp chipping note of alarm, a buzzy rattle or churr at a nuisance (like a human), and a thin whistle at distant hawks. Faint songs and chirps go to mates and young. Snarling and bugling notes, as well as songs and billsnapping and growls, may accompany aggressive fluffing to show concealed white back, crown, or wing patches at intruders. Whimpering peeps signify subordinate status, commonly associated with hangdog fluffing or wing-quivering submissive display. Young birds peep song-like phrases and squeak when fed. Breeding. Courtship feeding by the male often precedes copulation; mutual grooming and pair association are regular. (Aggressive displays have at times been incorrectly interpreted as courtship.) Antbird pairs work together at building simple nest cups or oven-shaped nests, the last on the ground by fire-eyes and above the ground by Brown-bellied Antwrens Mynnotherula gutturalis. Some nests resemble piles of debris, others are sunk in tree cavities or in the ground at the base of a tree. Ant-thrushes of the genus Fonnicarius lay white eggs deep in cavities of saplings, but most antbird eggs are speckled with brown, purple, or other colours. Blue eggs occur in some antpittas of the genus Grallaria, perhaps because such eggs look like the scattered foliage of the montane understorey where most live. Buff ground colour is known in some gnateaters, resembling the brown leaf litter just below their cup nests. Two eggs are the normal clutch, rarely 3; eggs are laid 2 days apart. Incubation, about 14-20 days, is by both sexes during the day and by the female at night. She fluffs out and, with her beak in her back, looks like a tuft of feathers. Eggs are covered most of the day, but White-flanked Antwrens Mynnotherula axillaris are off the nest 25-50% of the day despite pair cooperation. Young are brooded and fed by both parents for 9-18 days, and can hop and flutter actively on leaving the nest. Long incubation or brooding spells are the rule, as is infrequent feeding with large insects. Rufous Gnateaters Conopophaga lineata, however, feed small insects rapidly. Droppings are eaten or carried off by parents. Long incubation and nestling periods are found mainly in cavity-nesting species, notably the Black-faced Ant-thrush Formicarius analis with 20 days incubation and 18 days nestling period. Young Blackfaced Ant-thrushes are covered with down at hatching, unlike the naked young of most other antbirds. Injury feigning has been recorded for some species nesting on or near the ground, and for canopy species (Terenura spodioptilai when young have fluttered to the ground. If2 young survive, the male often cares for one and the female for the other. Young depend on their parents for food 1-2 months, then forage with them or wander away. Rufous Gnateater pairs leave corners oftheir territories for independent young, but young are driven away when they gain adult colour in Bicoloured Antbirds. Several broods may be reared in a season, and because of repeated nest destruction some pairs may nest 6 or more times per year. Breeding seasons of pairs may be short, 3-6 months, in equatorial regions as well as far from the equator; other species in the same areas nest 10 months or so per year. Some species apparently have two breeding seasons per year, while others nest all year or only during rainy seasons. (S.M.) E.O.W. Marchant, S. 1960. The breeding of some S.W. Ecuadorian birds. Ibis 102: 346-382,584-589. Munn, C.A. & Terborgh, l.W. 1979. Multi-species territoriality in neotropical foraging flocks. Condor 81: 338-347. Skutch, A.F. 1969. Life Histories of Central American Birds, III. Pacific Coast Avifauna 35: 580pp. Willis, E.O. 1967. The behavior of Bicolored Antbirds. Univ. Calif. Publ. Zool. 79: 1-132. Willis, E.O. 1972. The behavior of Spotted Antbirds. A.O.U. Monographs 10: 1-162. Willis, E.O. 1973. The behavior of Ocellated Antbirds. Smithsonian Contr. to Zool. 144: 1-57. Willis, E.O. 1974. Populations and local extinctions of birds on Barro Colorado Island, Panama. Ecol. Monog. 44: 153-169. Willis, E.O. & Oniki, Y. 1978. Birds and army ants. Ann. Rev. Ecol. Syst. 9: 243-263.

ANTCATCHER: obsolete (and misleading-see ANTBIRD) formerly applied to some medium-sized antbirds. ANT-CHA T: substantive name of Mynnecocichla spp. (see THRUSH).

Antwren

19

ANTCREEPER: substantive name of some species of Formicariidae, e.g. Mynnoborus spp . (see ANTBIRD) . ANTEPISEMATIC : see under EPISEMATIC. ANTHROPOMORPHISM: denotes, in the biological context, the fallacy of describing or interpreting the actions of animal s, other than Man, in terms of human actions and mental processes. ANTIBODIES: see BLOOD; DNA AND PROTEINS AS SOURCES OF TAXQNOMIC DATA.

ANTICOELOUS: see ALIMENTARY SYSTEM. ANTICRYPTIC: see under CRYPTI C. ANTIGEN: see DNA AND PROTEINS AS SOURCES OF TAXONOMIC DATA; SEROLOGICAL CHARACTERS. ANTING : highly specialized, stereotyped behaviour of passerine birds, whereby certain areas of plumage are treated with the defence and other body fluids of worker ants, chiefly of two non-stinging subfamilies, the Fortnicinae, which squirt fortnic acid from the tip of the gaster, and the Dolichoderinae, which exude sticky droplets of a repugnatory nature from the anal glands . Between 200 and 250 species of passerine birds, representing some 40 families or subfamilies, have been recorded using ants, though other insects and invertebrates producing similar fluids may be used occasionally. In addition, and especially in captivity, 'anting' has been observed with a variety of substances, mainly pungent, and in the presence of smoke (see SMOKE-BATHING) . True anting has been claimed for a few non-passerines, but such records remain to be substantiated; some may be due to misap prehension of other behaviour (see also COMFORT BEHAVIOUR) . Birds ant mainly in two ways: (I) directly by applying ants in the bill to the feathers ('active anting'); (2) indirectly by pertnitting ants to invade the plumage ('passive anting'). The direct manner, by far the commoner, is typical of babblers, starlings, tanagers, and weavers (Ploceidae) . They apply ants with quivering or stroking movements, characteristically with the wing partly open and lifted out at the side and the spread tail thrust sideways. The ant fluids, often mixed with copious saliva, mainly reach the ventral tips of the primaries and to a lesser extent the head (via the wing) and the undersurface of the tail near the vent. A small minority of species, including certain crows, drongos and New World orioles, practise a more extended form of direct anting, by applying ants to other areas, sometimes with preening action s. The ants are generally used singly but, notably by many starlings and some corvids, may be collected up progressively into a wad; then eaten or discarded afterwards. Birds anting in the indirect manner are mainly larger species of thrushes and crows (Corvidae) , but the tiny waxbills and allies (Estrildidae) also do so. While some crows (Corous spp.) will lie spread-eagled among the ants, most indirect anters squat in a special posture with both wings thrust forward in front of the body, allowing the ants to ascend the plumage while discharging their defence fluids. The birds may stir up the insects by repositioning themselves, by shuddering their wings among the ants, e.g. the Jay Garrulus glandarius, or even by quivering the tail, e.g. the Red-billed Magpie Cissa erythrorhyru:ha. Many species only use one or other of the two main methods but some also apply ants directly in the bill while anting 'passively', or as in the case of the Jay, the estrildine finches and the Grey Thrush Turdus cardis, just go through the motions without actually picking up ants . A few, notably Turdus thrushes, e.g. the Blackbird T . merula, ant in one way or the other on different occasions . All members of the same family or subfamily may use the same method but some taxa, notably the crows, show great variation even among closely related species . There is still controversy over the function of anting, but evidence points to it being a form of COMFORT BEHAVIOUR. It may help with feather maintenance, especially of the wings, perhaps to combat feather ectoparasites or remove stale or excess lipids (see DUSTING). Fortnic acid and anal fluids are insecticidal, and certain organic fluids from ants are essential oils, perhaps supplementing the bird's own preen oil. Preening often follows anting, and some birds also bathe and oil. Most anting is reported during the period when the post-breeding and juvenile moult occurs , at least in the Northern Hemisphere, but specula-

Jay Gatrulus glandarius in 'passive' anting position. (P hoto: Jane Burton ).

tion that birds ant to soothe the skin during feather replacement seems ill-founded. The correlation is more likely to be with the weather and seasonal factors that produce the maximum activity of the ants, most records being at swarms of ant s, especially those related to the nuptial flights of the royal castes. Theories on the auto-erotic or self-stimulating effects of anting appear to be misguided; nor is anting a mean s of removing distasteful liquids from the ants before eating them. See also COMFORT BEHAVIOUR; DUSTING ; SUNNING. K .E .L.S. Chisholm , A.H . 1959. The history of anting . Emu 59: lOI-130. Poulsen, H . 1956. A study of aming-behaviour in birds . Dansk Om. Foren . Tids skr. 50:267-298. Sinunons, K.E .L. 1957. A review of the aming -behaviour of passerine birds . Brit. Birds 50:401-424. Sinunons, K.E.L. 1966. Aming and the problem of self-stimulation . J. Zoo!., London 149:145-162. Whitak er, L.M. 1957. A resume of anting, with particular reference to a captive Orchard Oriole. Wilson Bull. 69: 195-262.

ANTIPHONAL SONG: 'duetting' (see VOCALIZATION) . ANTI-PREDATOR REACTIONS : see PARENTAL CARE. ANTPECKER: substantive name of estrildid Parmoptila jamesoni (see ESTRILDID FINCH).

ANTPIPIT: substantive name of the 2 species of Corythopis, small and superficially pipit-like birds that forage close to the ground in the Amazonian and other forests east of the Andes in South America . They were formerly placed with the GNATEATERS in a small family, Conopophagidae, but it has recently been shown that gnateaters are specialized members of the ANTBIRD family, while the antpipits are probably aberrant members of the tyrant-flycatcher family (see FLYCATCHER (2». ANTPITTA : substantive names of species of Pittasoma, Grallaria, Hylopezus, Mynnothera and Grallaricula (see ANTBIRD) . ANTRORSE: directed forwards ; applied, e.g., to rictal bristles that do not conform with the usual backward direction of plumage elements. ANTSHRIKE: substantive name of Taraba major, Thamnophilus spp ., Sakespharus spp ., and other large antbirds (see ANTBIRD) . ANT-TANAGER : substantive name of Habia spp . (see TANAGER). ANT-THRUSH: substantive name of Formicarius and Chamaeza spp . (see ANTBIRD); and of Neocossyphus spp . (for subfamily see THRUSH) ; sometimes used also for species ofPittidae (see PITTA) . ANTVIREO: substantive name of Dysuhamnus spp . and allies (see ANTBIRD) .

ANTWREN: substantive name of Myrmotherula spp ., Terenura spp ., Microrhopia s quixensis, and other small antbirds (see ANTBIRD) .

20

Anvil

ANVIL: stone or hard object used for smashing snail shells. ANVIL-HEAD: name sometimes used for Scopus umbretta (see HAMERKOP).

AORTIC ARCH: see DEVELOPMENT, EMBRYONIC; VASCULAR SYSTEM. APALIS: generic name used as substantive name ofApalis spp. of Africa (for subfamily see WARBLER (1).

APAPANE: Himatione sanguinea (see HAWAIIAN HONEYCREEPER). APODI; APODIDAE: see below. APODIFORMES: an order comprising 2 suborders: Apodi, Trochili; 3 families: Hemiprocnidae (CRESTED SWIFT), Apodidae (SWIFT; SWIFTLET), Trochilidae (HUMMINGBIRD). The suborders Apodi and Trochili do not at first sight seem very similar, but in the structure of the wings and the extreme shortness of the legs they are much alike, in both the number of rectrices is 10 (not 12, as in most other birds), and they show similarities of cranial structure which are unlikely to be the result of convergence. Wing movements are very rapid in both groups. Swifts are cosmopolitan, while hummingbirds are exclusively American, with remarkable specific radiation in all altitudinal zones of northern South America. APONEUROSIS: a flattened tendon for the insertion of a muscle (see MUSCULATURE).

APOSEMATIC: having a protective role-applied particularly to coloration. 'Proaposematic' means that the protection is in the form of a warning (e.g. of unpalatability); 'pseudaposematic' means that the warning is a bluff (protective mimicry); 'synaposematic' means that the warning signal is shared in common with other species. Compare EPISEMATIC; and, in general, see COLORATION, ADAPTIVE; MIMICRY.

APOSTLEBIRD: Struthidea cinerea (see under CHOUGH (2). APPENDICULAR SKELETON: the part of the skeleton consisting of the pectoral and pelvic girdles and the limbs; contrasted with the AXIAL SKELETON (see SKELETON, POST-CRANIAL).

APPETITIVE BEHAVIOUR: 'the variable introductory phase of an instinctive behaviour pattern or sequence' (Thorpe 1951)--compare CONSUMMATORY ACT (see BEHAVIOUR, HISTORY OF). APPLIED ORNITH0 LOGY: the application of ornithological know-

ledge to human activities concerned with birds (see especially AVICULTURE; CONSERVATION; DOMESTICATION; FALCONRY; GAMEBIRDS; GUANO; UTILIZATION BY MAN, with cross-references thereunder).

APTERIUM (plural APTERIA): an area of skin bare of contour feathers, lying between pterylae. Apteria may be feathered with semiplumes, down or powderdown (see PTERYLOSIS).

APTERYGES; APTERYGIDAE: seeSTRUTHIONIFORMES; KIWI. AQUATIC HABIT: for adaptations to this see SWIMMING AND DIVING; SKULL; VISION.

AQUINTOCUBITALISM: or 'diastataxis' (see WING). ARA.24 o ~20

110 120 100 Wing length (rnrnl

:J

lot

Fig. 3. fa. bi-modal distribution typical of a mixture of two distinct sample populations, here of male (long-winged birds) and female (short-winged birds) Skylarks Alauda arvensis trapped at Gibraltar Point (England) bird observatory. (After Davies 1981, Ringing & Migration).

their shape may be easily assimilated. There are two conventional ways of presenting the material. Where discrete variables are involved, so that only certain values may be found, a bar-diagram is used for the display (Fig. 1). Note that the bars do not touch one another, thereby indicating the non-continuity of the variable. Where the data are continuous, on the other hand, they can be presented as a histogram (Fig. 3), the height of each bar indicating the frequency, and the width of each bar indicating the class interval. To construct such a histogram the values of the continuous variable are tallied into specified class intervals defined by specified upper and lower limits, the upper limit of one class serving as the lower limit of the adjacent class. The class interval is usually held constant across the histogram, except perhaps at the beginning and final steps, but its width may be chosen according to convenience. Typically there are 12-20 classes displayed on a histogram. Descriptive statistics. The first task of biostatistics is to provide some form of summary description of the data. If one measures 200 bird weights it is impracticable to describe the population by quoting the raw data: some form of summary is required. For an ordered frequency distribution two descriptive statistics are particularly important: a measure of central tendency, and a measure of dispersion. If appropriately chosen, these statistics more economically describe the data than do the histograms or bar charts previously presented. Statistics of location or of central tendency indicate the whereabouts of the distribution as a whole (Fig. 4). The figure shows the position of three separate measures of central tendency, the mode, the median, and the mean. Which measures may best be used depend on the nature of the data (whether nominal, ordinal or continuous). The mode is the most frequently represented value within the histogram or bar chart, i.e. there are more observations at that value than at any other, whether the value be discrete or that of a class interval. It is

...... rll'lcl"1llnn

32

12

8

4

o 36

39

42

45

48 51 54 Weight (g)

57

60

63

Fig. 4. An example of a skew distribution, here of weights of female Corn Buntings Miliaria calandra, showing the effect of the (here positive) 'tail' in moving the mean value away from the median and modal values (which are themselves separated). (Modified from Boddy & Blackburn 1978, Ringing & Migration).

1971

90

90

75

75

60

60

45

45

30

30 15

15

o

1972

0

April 90

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1973

April 90

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45

30 15

30

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1974

15

o

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Fig. S. Annual distributions of egg-laying dates in a New Forest (England) population of Lapwing Vanellus vanellus showing year-to-year variation in distribution width ('dispersion'). (After Jackson & Jackson 1975, Ringing & Migration).

Biostatistics

tially in their apparent 'width' independent of their central location (Fig. 5). Some measure of the width of the distribution is therefore desirable. The range is the simplest form of characterizing distributions and is calculated as the difference between the largest and the smallest item in the sample. This measure is obviously sensitive to outliers and is therefore only an approximate measure of the dispersion. It is worth noting in particular that as sample size increases the probability of detecting an observation with a still more extreme value increases, thereby increasing the range. The standard deviation is the most widely used measure of dispersion for symmetrically distributed data. It is computed as

s= !(X-X)2 n-l or equivalently as

where x is an observed value, x is the average of all values in the sample, and n is the sample size. The former version shows that the standard deviation is a root mean square index of dispersion. That is, it is calculated by computing the deviations of each point from the mean, squaring them, weighting them for sample size and taking their square root. The squaring procedure ensures that positive and negative deviations are given equal weight and avoids the problems caused by the average deviation being zero; the squaring process has other advantages on mathematical grounds. The use of the factor (n - 1) in the denominator instead of dividing by n to compute an average mean square deviation has been shown by statisticians to be necessary to obtain an unbiased estimate of the spread of the population from which the sample has been drawn. The term variance is used to describe the square of the standard deviation. The coefficient of variation is a statistic which expresses dispersion (in the form of standard deviation) as a percentage of the sample mean. That is, CV=100s/m where s is standard deviation and m is sample mean. This measure of relative variation allows for the fact that large animals are more likely to vary individually by any absolute amount than small animals: a Wren Troglodytes troglodytes will not show the same absolute variation in measurement as will an Ostrich Struthio camelus. The coefficient of variation provides a scale of relative variation with which meaningful comparisons between species of different size can be attempted. Statistical significance. Because animals are inherently variable as to the characteristics ornithologists may wish to measure, statements about them are necessarily expressed (at least in principle) in probabilistic terms. That is, we are rarely in a position to assert that, say, males are larger than females; what we must say, in strict pedantry, is that males are more likely to be larger than females. Were there no convention amongst scientists as to how a phrase such as 'more likely' is to be interpreted there would be considerable variation in individual ornithologists' interpretations of its meaning. Conventionally, therefore, such results are assessed in terms of statistical significance, meaning the probability that a particular result would have arisen by chance were the supposed hypothesis untrue. In the example of the male-female weight difference, for example, we start with the assumption or null hypothesis that there is no difference between males and females. We then compute the probability that two samples drawn from this common pooled male/female population would in fact differ by the amount found in the samples actually taken. If these chances are low enough we regard the probability of the male and the female sample having been drawn from a common pool as being so low as to be unlikely and prefer the alternative hypothesis that there are in fact differences between male and female. What is 'low enough' in this context? The conventional probability for scientific purposes is 0.05, meaning that we have five chances in a hundred of getting the two Cor more) samples drawn from the 'common pool yielding a difference as big as that observed. Two points must be made about this limit. First, it is a purely conventional limit accepted as a working tool by scientists. Secondly, in working to this conventional

53

value one is accepting a one in twenty chance of a sampling artefact, there really being no difference between the male and female distributions. When there is great importance attached to getting the results correct a one-in-twenty chance of error may be too high and it is possible to work to higher levels of significance, such as 0.01 or 0.001, meaning respectively a one-in-a-hundred and a one-in-one-thousand risk of falsely asserting the existence of a difference between the two samples. This approach to testing hypotheses has a further consequence. If one conducts 100 tests of differences between males and females on the basis of a 5% significance level, as many as five of these tests are likely to yield 'significant' results by chance alone. Consequently, where repeated testing of samples is involved, it is necessary to avoid such a 'Type I' error by working to a higher level of significance than would otherwise be appropriate. On the other hand, such an approach to probability testing of hypotheses is more likely to fail to recognize real differences between male and female samples as the significance level is raised (a failure known as Type II error). That is, in protecting ourselves against the chances of falsely asserting the presence of a male/female difference, whilst the samples were in fact drawn from distributions similar for males and females, we are increasing our chances of failing to detect sex differences when male and female distributions are not identical. Testing a significance level. How does one assess the probability of two samples drawn from a common distribution in fact differing by the amount observed in the experimental samples? One approach is to draw repeatedly from a model population with the desired characteristics, and to examine the differences between the two samples of pseudo-males and pseudo-females drawn from this population. Such a course would be extremely tedious and one normally has recourse instead to certain test statistics whose critical values are conveniently tabulated. As these test statistics have been computed only for distributions obeying certain assumptions, it is important that the data under test also obey these distributions. Thus, a test statistic calculated for a normally distributed population is inappropriate to a population whose distribution is nonnormal. To accommodate the wide variety of problems regularly encountered, statisticians have evolved a number of test statistics meeting particular problems. The rationale behind these test statistics is that they represent quantities which can be calculated for samples repeatedly taken from some underlying distribution. Corresponding to repeated sampling from the population will be a distribution of values of these test statistics, the distribution being defined either analytically or, in the case of complex population distribution, by computer simulations. It is therefore possible to examine these distributions and to establish values of the test statistic corresponding to, say, 50% of all observations lying between the chosen values, 90% of all observations lying between the specified values, 95% lying between them, etc. Of particular interest are the values corresponding to 95% of the observations defined by the critical values since this corresponds to the conventional 0.05 significance level. Were two samples drawn from a single underlying population and the corresponding test statistic computed, 95% of the drawings would yield test values within the specified critical values. Were the computed value outside these limits, one would be dealing with the rare set of 5% of the drawings from a common population. Given real samples for which such a test statistic value was calculated, one has a nineteen to one chance against the value being derived from samples belonging to the distribution concerned. Such critical values will vary according to the size of the samples drawn. Consequently, it is possible to tabulate these values as a function of sample size. Armed with such a table, an ornithologist faced with a real sample or samples can compute the same test statistic and enquire whether the value exceeds the conventional 5% significance level. Confidence limits. The aim in sampling is to describe the population by inferring from the observations which were taken as a sample. How good is the resulting inference? Suppose one is interested in the weights of individuals of a species just before migration. If one could weigh all individuals of the species one would know the 'true mean' eM) and the 'true variance' (0 2) for the population. In practice one has a sample of these birds with some average weight x and sample variance S2. One may set confidence limits to the estimated average x to allow statements of the form 'The probability that limit 1 < x < limit 2 is at least 950/0' by using certain statistical methods to calculate the lower confidence limit limit 1 and the upper confidence limit limit 2. Such statements claim that conventional statistical procedures have been followed and that estimates of the

54 Biostatistics

confidence limits would encompass the true mean in at least 95% of the experiments analysed with such procedures. The theory behind such statements is complicated but an understanding of the methods may be obtained as follows. Suppose we took, as before, a sample of observations from the parent distribution of all observations and computed some test statistic for the sample. We could repeat this process as often as we wish, tabulating the resulting values of the test statistic for each drawing of the sample. After, say, 1,000 such samples, we would have a good idea as to the distribution of the test statistic scores and, in particular, what values of the statistic would arise in only 50/0 (or 1% or 0.10/0, as we wish) of the samples. If we now examined a sample of real observations satisfying certain criteria (discussed below) we could likewise compute a sample test statistic. If this were so extreme as to arise in 5% or fewer of the sample drawings just discussed it would be rather improbable that these real data belonged to the parent distribution. Note that we have reached a conclusion-that the real data do not belong to the parent distribution-on the basis of comparing a computed test statistic for the sample with a critical value (for 5%, 10/0, etc.) already established by simulated drawings from the parent population. These critical values depend on the size of the sample used but it is nevertheless possible to prepare tables of these critical values, both with respect to different significance levels and with respect to sample size. If these tables had to be prepared from the results of large numbers of sample drawings as outlined above, with different procedures for each different problem, the tables would be excessively voluminous. In practice analytical expressions for the distribution of particular test statistics can be formulated and many problems can be analysed in such a way as to generate such a statistic. Examples of widely used statistics of this type include Student's t, the variance ratio F, and chi-squared (,r). Parametric and non-parametric statistics. Test statistics based on analytical expressions necessarily make assumptions about the distribution of the population sampled. If these assumptions are correct, the test statistic will be correctly calculated and the conclusions valid; if incorrect, the statistic is inappropriate and the conclusions invalid. Since the population assumptions turn on values given to parameters within their algebraic expressions these methods are called parametric. Many statistical techniques more recently in fashion are independent of such assumptions and are called distribution-free or non-parametric methods. These techniques are particularly valuable with ordinal and categorical data, which fail to satisfy parametric assumptions. These techniques may also prove helpful with skew or otherwise unsatisfactory distributions of continuous variables. In many instances non-parametric procedures result in an evaluation of the exact probability of getting as extreme an event as that observed. That is, this probability is directly calculated rather than inferred via a statistic subject to assumptions. This is especially valuable with very small samples, for which the validity of assumptions as to distribution is difficult to check. They are also useful in testing differences between populations known to differ in distribution. The main drawback of non-parametric methods is that they require rather larger samples than do equivalent parametric tests for which all assumptions are satisfied. Statistical testing. Siegel (1956) summarizes the process of statistical testing into six stages: (1) state the null hypothesis; (2) choose an appropriate statistical test with its associated statistical model; (3) specify the target significance level and sample size; (4) find (or assume) the sampling distribution of the statistical test for the assumption that the null hypothesis is correct; (5) define region of rejection; and (6) compute the value of the test for the sample data and accept or reject the null hypothesis accordingly. The null hypothesis is one temporarily assumed for the purposes of the statistical test. Since it is impossible to prove a negative we try to recast the problem as a positive; e.g. the surest way to prove that a colourringed Blackbird Turdus merula is not breeding in a particular forest is to show that it is breeding somewhere else; otherwise, however well one searched the forest one has always a residual possibility of having missed the bird. For a null hypothesis, therefore, we assume the absence of what we expect to find and seek to establish the presence of a consequential discrepancy. The choice of statistical test depends primarily on (a) the validity of the assumptions to be made if the chosen test is to be used and (b) the type of data involved, particular tests being inapplicable to certain types of data (see above).

The level of significance associated with a test is necessitated by the variation inevitably associated with random sampling. Repeated sampling on the same question will give different results on different occasions, with the extent of the variation determined by measurement errors and by the natural variation of biological populations. Consequently, the results of a test are only probabilities, not determinants, and one is at risk both of falsely deciding in favour of and of falsely deciding against one's hypothesis. By convention-and one must emphasize it is convention, not an inescapable rule-we accept at maximum a one-in-twenty risk of incorrectly rejecting the null hypothesis (and thus of falsely concluding in favour of the research hypothesis under test). For some purposes we may wish to reduce this risk (a so-called 'Type I' error) to one in a hundred or even to one in a thousand. This is equivalent to demanding stronger evidence for the research hypothesis and therefore carries increasing risk of making the alternative ('Type II') error, of falsely accepting the null hypothesis and concluding one's research hypothesis is wrong. In general the chance of correctly rejecting the null hypothesis increases with sample size. Glossary of some common statistical tests. It is not possible to describe within the scope of the present article how to conduct the various statistical tests available. For information on these readers are referred to the references below. What follows is a brief glossary of some of the commoner statistical tests, primarily to indicate their respective functions.

AnaO'sis of variance A general class of statistical tests used for assessing the significance of differences between two or more samples. The principle used is to compare the between sample and within sample variances: if the average differences between samples are large enough relative to the variation within each sample, it is likely that biological effects are present. The implementation of this principle varies, however, according to the assumptions that one can (or must) make about relationships between the individual birds measured in each sample. For an excellent introduction see the book by Parker. ANOVA (Anova) A synonym of analysis of variance. Bartlett's testof homogeneity of variances A test of whether three or more samples are equally variable (see F-test for two sample case) Binomial test A test for whether in a sample the number of birds possessing some particular attribute corresponds to the proportion expected (according to some quantitative, e.g. genetical-hypothesis) to have that attribute. Chi-square (x5 while if pressure is to maximize distance flown (migration, flying to feeding site) it will fly at V mr- In some situations reducing time becomes important (escape from predation, foraging to feed young), and the bird will then fly as fast as possible. Typical flight speeds relative to the power curve for different flight conditions are summarized in Fig. 1. Migration. Perhaps the most important situation demanding best possible flight performance is migration. As a contribution to the animal's annual energy budget the extra flight energy consumed must be more than balanced by improved energy intake in the more favourable habitat, and by the associated increase in reproductive fitness. The large distances involved place strong pressure for a strategy that minimizes total energy for the distance covered, and migrants can be expected to fly (in still air) at speed V mr- If the bird is influenced by wind, as is often the case in migration, ground speed and air speed will not correspond, and air speed must be adjusted so that ground distance is as large as possible. Theory suggests that in head winds air speed should be increased by about 300/0 of wind speed (up to the maximum set by metabolism, beyond which forward progress is impossible), while in tail winds the bird should reduce air speed by the same amount. Several migrants (e.g, Chaffinch F ringilla coelebs) have been observed to respond in this way when the wind is parallel to the flight path and does not drift the bird to the side of its goal. In crosswinds the situation is more complex, but one possible response is for the bird to fly at high altitude in a strong wind without compensation for drift or wind speed until abreast of its goal, then to descend to lower altitudes where the winds are weaker and to fly direct to its destination: in this way the total energy needed can be minimized. The large fuel reserves stored as fat at the start of migration by many small birds also affect flight strategy: as the flight proceeds, fuel is

225

assumed maxi mum aerobic power

cruise flight and migration bounding small n"c~c:ol,..il'"\C: typical minimum take off speed, greater in larger birds hover feeders (hummingbirds, kingfishers) optimal wind speed for stationary hunters (kestrels, buzzards, terns) roosting flight (swifts) aerial hunting (hcrriera.owls] aerial insect ivores (swifts, swallows, night jars) foraging to feed young non - powered flight typical glide and dive speeds

Fig. 1. Typical graph of power against speed for level flapping flight in birds, showing characteristic speeds Vmp and Vmre together with the likely ranges of flight speed in different flight conditions, as they are related to the characteristic speeds and to the shape of the curve. Morphology adapts so that power is minimum at the appropriate SPeed range.

consumed and mass decreases, and speed should be reduced: at all times, however, the bird should fly at V mr (with appropriate compensation for wind etc.), and the change in mass alone dictates the change in speed. Morphology. The active selection of flight speed according to the demands of performance allows a bird to optimize flight behaviour, but the speeds available to it are dictated by the aerodynamic features of the animal and by the size and shape of the wings. Selection favours the development of wings specialized for the type of flight pattern associated with the animal's behaviour and ecology, and as the design of wings becomes more extreme, allowing less flexibility in flight behaviour, so the animal becomes more specialized not only in its flight but also in ecology and ethology. Wing size is described by wing loading (weight supported by unit wing area), and wing shape by aspect ratio (wing span squared, divided by area), and the major trends of flight adaptations may be distinguished with these parameters. Measurements of air speed in level flapping flight for a number of species are shown in Table 1, together with body mass, wing loading and aspect ratio. The considerable variation in speed even between birds of the same mass is the effect of wing morphology: speed rises with both mass and wing loading since higher speeds become necessary if lift is to be sufficient to support weight, while speed shows a slight decrease as aspect ratio rises since longer wings are more efficient. Birds which fly slowly or hover while foraging (e.g. Kestrel, terns, kingfishers, hummingbirds), and aerial insectivores (swifts, swallows), have long, high-aspect-ratio wings so that V mp (and also V mr) is low and power at that speed is as small as possible, even though the penalty of low maximum speed is unavoidable. On the other hand divers, ducks, geese and some waders have short, highaspect-ratio wings allowing high speeds without unduly high power, because their feeding behaviour is dramatically influenced by weather and tide, and high speeds are of great importance to their success, as many of these species breed in arctic latitudes where the season is short and weather can be unfavourable. Many small passerines have short, rounded wings of large area and low aspect ratio. The low wing loading permits the large increases in weight prior to migration without flight becoming impossible, and these birds compensate for the high wing drag

226 Flight, speeds of

Table of speeds offlight for a sample of birds, with average mass and wing morphology for each species.Speeds, obtained from radar measurements from a variety of sources, are cruise speed (V mr) in light winds or still air. Mass

Aspect ratio

(kg) Red-throated Diver Wandering Albatross Wilson's Petrel Grey Heron Bewick's Swan Barnacle Goose Whitefronted Goose Mallard Eider Duck Sparrowhawk Osprey Kestrel Pheasant Crane Oystercatcher Dunlin Herring Gull Common Tern Woodpigeon Swift (roosting) Swift (migrating) Swallow BlueTit Chaffinch House Sparrow Starling Crow

Wing loading

Speed

(N/m

(m/s)

2

Gavia stellata Diomedea exulans Oceanites oceanicus A rdea cinerea Cygnus columbianus bewickii Branta leucopsis Anser albifrons Anas platyrhynchos S omateria mollissima Accipiter nisus P andion haliaetus Falco tinnunculus Phasianus colchicus Grus grus H aematopus ostralegus Calidris alpina Larus argentatus Sterna hirundo Columba palumbus Apus apus

0.96 8.7 0.038 1.32 6.2 1.15 1.72 1.01 2.18 0.188 1.1 0.200 1.2 4.8 0.42 0.045 1.0 0.121 0.461 0.042

12.2 15 8 7.8 9.2 10.1 10.8 9.1 8.4 6.5 8.9 7.9 5.5. 7.3 9.7 8.6 10 13.2 6.6 10.5

106 140 19.4 39.8 147 98 92 113 194 28.1 38.5 30.7 123 85 64 29.8 49.9 24.5 57.5 29.1

H irundo rustica Parus caeruleus Fringilla coelebs Passer domesticus Sturnus vulgaris Corvus corone

0.022 0.010 0.022 0.028 0.076 0.46

8 6.8 5.9 5.5 7.2 6.8

16.1 16.8 20.2 26.4 36.6 36.7

by adopting bounding flight, in which the wings are closed for about half the time they are airborne, and speed is rather higher than V mr ' In every flying bird morphology is best adapted to suit performance largely so that speed and energy are optimized: flight is so demanding on energy consumption that selection will ensure that no resources are wasted and that food is gathered in the optimum way. Speed measurement. In view of the numerous factors involved in the selection of flight speed and the great difficulties inherent in measuring it, it is hardly surprising that published bird speed records show little coherence. Many methods have been used with remarkably little success; techniques such as triangulation or pacing from cars, trains or aircraft are particularly unlikely to produce meaningful data. The best method is probably low-range Doppler radar tracking of a known individual; with tracking radars the bird may not be accurately identified, and exact wind strength and direction are rarely known. High-speed cinematography can be valuable if the camera used and distances are accurately calibrated, but with every technique it is vital to record wind velocity and to take note of what the bird is trying to achieve. Because many observers have been prevented from doing this, published speed records, such as those tabulated by Meinertzhagen, are often misleading and inaccurate. Table 1 lists recent radar measurements of cruise (usually migration) flight speeds in still air or light winds. These are believed to be reliable, and in most cases represent flight at or near V mr ' Considerable popular interest is devoted to records such as the 'fastest' bird, and to this end many fanciful estimates of speed have been published. Comparisons of this kind between species are invidious, but from the table it can be seen that speeds rarely exceed 20 m/ s (72 km/h), and doubt must be expressed over air speeds for steady powered flight much in excess of this. The fastest speed for any type of flight probably occurs during the stoop of the Peregrine Fa/co peregrinus, but no accurate determination of speed has been made, and it is probably no more than about 50 m/s (180 km/h), In steady flight the fastest bird reliably clocked as yet is the Eider Somateria mollissima at 21 m/s (76km/h); this bird has the highest recorded wing loading. Contrary to popular opinion, swifts are among the slowest of birds, as is consistent with their long, thin wings; speeds for the Common Swift Apus apus in foraging (6.5 m/s, 23 km/h) are slightly higher than V mp> at the expected optimum for an

)

17 15 11 12 20 19 15 18 21 12 13 9 15 19 14-16 13 1~11

9-12 17 6.5 11 9 8 1~14

8-11 9-10 14

(km/h) 61 54 40 43 72 68 54 65 76 43 47 32 54 68 5~58

47 36--40 32-43 61 23 40 32 29 36--50 29-40 32-36 50

aerial insectivore; in migration they fly at about 11 m/s (40km/h), that is at V mr • J.M.V.R. Alerstam, T. 1982. The courseand timingof bird migration. Semin. Ser. Soc. Exp. BioI. 13: 9-54. Meinerizhagen, R. 1955. The speed and altitude of bird flight. Ibis 97: 81-117. Norberg, U .M. 1981. Flight, morphology and the ecological niche in some birds and bats. Symp. Zool. Soc. Lond. 48: 173-197. Pennycuick, C.J. 1969. The mechanics of bird migration. Ibis 111: 525-556. Rayner,J.M.V. 1979. A newapproach to animalflight mechanics. J. Exp. BioI. 80: 17-54.

Rayner, J.M.V. 1982. Avian flight energetics. A. Rev. Physiol. 44: 109-119.

FLIPPER: term applied to the modified wing in the Spheniscidae (see PENGUIN; SWIMMING AND DIVING).

FLOCK: see

ASSEMBLY, NOUN OF.

FLOCKING: term for the positive social behaviour of individual birds that results in their joining into groups (flocks), as distinguished from aggregations of animals resulting from the influence of ecological factors alone. Characteristics of flocks. Flocks may consist of one to several species, the latter usually referred to as mixed-species flocks. Dominance hierarchies may exist in both single and mixed-species flocks, and an individual's ranking may affect its access to food. In the tropics flocks exist year-round, while at higher latitudes they are confined to the nonbreeding season and to non-breeding birds. Flocks range in size from a few birds to thousands of individuals, as seen in some icterid or finch flocks. Many flocks are constantly on the move, showing a loosely coordinated, unidirectional movement that distinguishes them from chance aggregations. They may cover as much as several hundred metres within an hour, even when their individuals are successful in finding food. Members of compact open-country flocks frequently exhibit conspicuous 'leap-frog' movements, in which birds at the rear fly over and land in front of the other members. In this way they minimize the probability of encountering just-exploited areas. Although flocks result in a large-scale clumped distribution of birds, at

Flocking

a smaller scale these birds are evenly spaced. Members of open-country flocks are usually spaced much more closely than those of forest-dwelling flocks, sometimes not over a body-length apart . Birds in forest-dwelling flocks usually remain at least several metres apart, but their minimal tolerated distances (individual distances) vary among species or at different times. Half of the advances by Black-capped Chickadees Parus atricapillus to within 3 m of a conspecific resulted in a supplanting action or retreat ; in Blue Tits Parus caeruleus, the corresponding distance was one metre. Flock members may either roost communally or apart. Icterid and starling flocks sometimes remain as units within large roosts. Members of forest-dwelling flocks, however, usually roost in holes or other sites independently of each other and join shortly after becoming active in the following morning . Flock members obtain one or more general advantages: feeding, predator-avoidance, and reproductive. In most cases, reproductive advantages (sensu stricto) may be separated from the others and they will not be further discussed here (see NATURAL SELECTION ) . Bird flocks bear many functional similarities to fish schools and mammal herds or troops. Feeding advantages. Foraging flocks are a common phenomenon among birds. Hypothetically, birds may obtain several food-related advantages while in them . Facilitation of food-finding. Probably the most frequently suggested feeding advantage is that participating in a group facilitates food-finding. One bird may observe another foraging and join it if the original forager is successful. For this to be advantageous, food must be so abundant that one individual can not consume it all quickly. Alternatively, an individual may simply forage at a site similar to one where another individual is foraging successfully. The only experimental evidence supporting either alternative is from the laboratory studies using Great Tit s Parus major. Several field studies have also produced evidence consistent with this advantage. Rather than increasing the amount of food that an individual will find, flocking may lessen the danger of an individual going without food for long periods . Given the severe conditions often experienced by birds at high latitudes during the winter, and the tendency for flocking to increase as climatic conditions grow more severe, this hypothesis has merit . Minimizing duplication of effort. If flock members deplete an area other birds must avoid that site. The y may obtain this advantage by watching the movements of others, although little direct evidence exists that they do this. This pattern would be advantageous if food were evenly distributed in parcels too small for more than one individual to exploit. Success from numbers. Individuals may have access to certain resources by sole virtue of their numbers. If Cedar Waxwings Bombycilla cedrorum

Oystercatchers Haematopus ostralegus flocking . (photo : H .E. Grenfell ).

227

enter a Mockingbird Mimus polyglottos territory, the Mockingbird will attempt to drive them out, but if their flock consists of several score individuals, the Mockingbird may be able to evict only a small minority of them . In this way the Waxwings can exploit the rich berry sources often defended by a Mockingbird during the winter. Beating. It is often suggested, particularly in the older literature, that a major advantage of flocking lies in the insects that are flushed (and subsequently captured) by the participants. Some individuals may so benefit when insects are active; however, the advantage cannot occur in all cases, since flocks of small insectivorous birds are most prominent at high latitudes during winter , when insects are inactive. Further, unless birds can capture flying insects, they are unlikely to benefit. For beating to be a direct advantage of flocking, rather than an advantage only to certain members, more flushed prey must be captured by birds when in groups than when alone, and this advantage must hold for all members. Such conditions are not met in most flocks of small insectivorous birds, and certainly not in flocks that feed on non-motile prey. However, Cattle Egrets Bubulcus ibis feeding in groups may obtain this advantage, although their foraging success is lower than when they follow cattle. Flocks of pelicans, cormorants and mergansers may also drive schooled fishes into shallow water where these birds can capture their prey more readily than in deep water. Predator-avoidance advantages. Flock members may enhance their ability to escape predators in several ways. Increased awareness of predators. Individuals should be apprised of predators more rapidly in groups, because many eyes are present. Predation is less severe on members of wader and Woodpigeon Columba palumbus flocks than on single individuals. Vulnerability decreases as flocks become larger up to a certain point. In the case of waders and corvids, detailed observations have shown that more birds were taken from larger flocks than from smaller ones. If flocks become too large, an individual on one side of the flock may not see a predator approaching from the other. Alternatively, individuals might get in each other's way during an escape. Evidence on these points is not available for most bird flocks, and some workers have argued that the increased conspicuousness of flock members may negate any advantages. Members of many flocks call nearly continuously , including notes that may not be given at other times. Thus, although the percentage of successful attacks might decline, the number of attacks might increase. Confusion effect. A mass response, whether a sudden flight or calling, may confuse a predator, at least temporarily, giving flock members the opportunity to escape. When confronted with many simultaneous stimuli, a predator may find it impossible to separate out a single individual. When attacking a flock, a predator's typical strategy is to separate an

228 Flocking

individual if possible. Many, although not all, flocking species give characteristic calls upon detecting a predator. These calls have been considered difficult to localize because of their acoustical properties. However, at least some avian predators can localize them; but in any case the fact that it is calling means that the flock member is aware of the predator. As a consequence, the predator may not attempt to capture it. Discouraging predators. Some animals may repel predators as a consequence of their numbers, by posing a threat. Flocks in flight tighten their formation, thereby providing a target that may be dangerous to any predator that attempts to fly into the middle of it. Starling Sturnus vulgaris and Red-winged Blackbird Agelaius phoeniceus flocks may even turn on their attackers, forcing them on to the ground or into the water. Alternatively, if being in a flock makes individuals more difficult to capture, it may not be worth the predator's efforts to attack, though no data known to the writer support the existence of this effect in bird flocks. Cover-seeking. A given flock member might obtain protection from predators by hiding behind other members, or at least by positioning itself so that one or more flock members lie between it and the predator. This behaviour would favour central individuals over peripheral ones and would tend to result in a compact group. Little direct evidence exists for this in birds. In flocks with widely-spaced individuals, such as mixedspecies insectivorous flocks, such a hypothetical advantage would seem confined to maintaining a core position, thus keeping other individuals between the actor and the periphery, from which an attack would normally come. However, even if these effects were demonstrated, they could not be considered a primary advantage of flocking, unless all members benefited from it. Thus, if peripheral individuals suffered increased predation as a consequence, they would be continually peeled off the outside. More likely, peripheral individuals would stop flocking before severe predation ever took place. Decreasing the probability of discovery. Several workers have suggested from mathematical formulations that animals in groups should be discovered less frequently than if they were solitary. However, it is questionable whether such advantages exist in the real world. These models assume random movement on the part of the flocks and predators and do not account for possible behavioural changes of members between solitary and social situations. Flock members and their predators, at least when in heterogeneous habitats, concentrate their activities in certain places. Further, they perform various behavioural patterns that are not typically given by solitary individuals. For instance, tits in flocks regularly produce calls that are not given elsewhere. If a flock member becomes temporarily separated from other individuals, it often calls loudly from a conspicuous perch. Both these behaviours make flocks conspicuous to human observers, and probably to flock predators as well. Single-species and mixed-species flocks. Both single-species and mixed-species flocks may share the non-reproductive advantages discussed above. However, differences should exist in the magnitude of advantages obtained. Although members of mixed-species flocks overlap with each other in foraging, this overlap is lower than that among members of the same species. Thus, if food is scarce, individuals of different species would not be disadvantaged as greatly as members of the same species. However, any food-related advantages should not be as great as those obtained in a single-species flock. If the energetic stakes are lower in mixed-species flocks than in single-species flocks, some other factor should account for the existence of mixed-species, as opposed to single-species, flocks. Anti-predator advantages should be relatively greater in mixed-species flocks, by virtue of the greater variety of eyes brought to bear, the wider range of locations often exploited at a given time, and the larger size often possible in mixed-species groups, a probable consequence of lowered competition. Certain species often sound anti-predator warnings first. Carolina Chickadees Parus carolinensis usually sound the warning in mixed-species forest flocks in eastern USA. It is not clear whether they are thus being parasitized by other species, or whether the sentinels obtain special advantages in return. However, species sharing relatively little foraging similarity to other members of flocks sometimes move with them for considerable distances. For instance, Eastern Bluebirds Sialia sialis, Dark-eyed Juncos Junco hyemalis, and Chipping Sparrows Spizella passerina often follow tit flocks through open woodlands, spending much of their time foraging on the ground. If individuals in the trees sound warnings, these 3 species fly rapidly to cover. They probably take advantage of the others' elevated locations to lessen the danger of being

captured unaware. If so, this relationship is a commensal one; that is, one in which they benefit and the other members are unaffected. Migrants in flocks. Flock function has been little studied during migration, although migrants often move in groups or join other flocks between their flights. Migrants might find rich food sites or protection from predators by following resident groups. Since migrants are unfamiliar with their surroundings, their potential reward from joining residents should be large. Evolution of flocking. Many workers have argued that either foraging or anti-predator advantages are responsible for the evolution of flocking. These arguments are fraught with danger, because it is unlikely that either advantage will exist in the absence of adaptations associated with the other. Thus, if individuals commenced to form flocks that enhanced foraging, they would quickly become vulnerable to predation, unless they simultaneously developed anti-predator adaptations lowering predation at least to a point where feeding advantages outweighed the increased risk of predation. Alternatively, if individuals formed flocks that enhanced avoidance of predators, they would be likely to incur feeding disadvantages as a consequence. Strong pressure would consequently develop to minimize foraging disadvantages. In either case, if one capability develops, the other should quickly follow. Flock size. A close relationship may exist between energetic conditions, aggression levels, predation pressure, and consequent flock size. When energetic demands are stringent, foraging occupies so much of flock members' time that they have little time left to fight. This might happen at a time of deteriorating food supply, or when cold weather makes high energetic demands. Flocks increase in size and cohesion at such times, and individuals simultaneously decrease their frequency of scanning for predators, permitting an increased proportion of time to be spent searching for food, presumably with no added danger of predation. If conditions become less stringent, more time is available for fighting. Flock size declines at such times, probably because subordinate birds are harassed so frequently that it no longer benefits them to participate in the flock. However, certain reports are not consistent with these observations. For instance, increased fighting for food accompanies extremely severe conditions in corvid and tit flocks. Whether or not flock sizes in extremely large groups follow this pattern remains to be explored. The flocks discussed here are of modest size, within the range in which individual recognition remains possible. Other groupings. In practice it may be difficult to distinguish between flocks and other groupings (see ROOSTING; COLONIALITV). Some of the flocks discussed above have clearly-defined commensals attached to them, such as the bluebirds Sialia and sparrows (Emberizidae) that follow tit flocks. It is not a great jump from these associations to two-species feeding associations, such as those between grebes and ducks or coots, in which the former obtain food dislodged by the latter. Similar associations may even form between birds and other animals, such as squirrels that follow bird flocks, or monkeys that follow hornbills. See photos FACILITATION, SOCIAL; ROOSTING. D.H.M. Caraco, T. 1979. Time budgeting and group size: a test of theory. Ecology 60: 618-627. Herrera, C.M. 1979. Ecological aspects of heterospecific flock formation in a Mediterranean passerine bird community. Oikos 33: 85-96. Krebs, j.R., MacRoberts, M.H. & Cullen, j.M. 1972. Feeding and flocking in the Great Tit Parus major-an experimental study. Ibis 114: 507-530. Morse, D.H. 1977. Feeding behavior and predator avoidance in heterospecific groups. Bioscience 27: 332-339. Morse, D.H. 1980. Behavioral Mechanisms of Ecological Interaction. Cambridge, Mass.

FLORA: the total plant life of an area (contrasted with

FAUNA);

see

HABITAT.

FLORICAN: substantive name (also spelt 'floriken') of 2 Indian species of Otididae (see BUSTARD). FLOWERPECKER: substantive name of some species of Dicaeidae (Passeriformes, suborder Oscines); in the plural, general term for the family. This is a group of small or (rarely) medium sized arboreal birds (7.5-19 em long) of Oriental and Australasian distribution.

Flowerpecker

Mistletoebird Dicaeum hirundinaceum, female (left) and male. (C.B. T.K.).

Characteristics. Most (40 out of 55 species) are grouped within the 2 widely distributed genera Prionochilus and Dicaeum. These typical flowerpeckers are small birds, with a wing length in adult individuals of 4.0--7.5em, and with short, stumpy tails. The bill, in which the edges of the distal third are serrated, is short, varying in structure between a stout and blunt type like that of tits (Paridae) and a thin, attenuated, more or less decurved type like that of warblers (Sylviinae) or short-billed sunbirds (Nectariniidae). The short tongue has, in its deeply cleft distal half, the edges curled to form two slender semitubular tips; this somewhat resembles the tongue structure in sunbirds and is probably an adaptation to nectar feeding. The plumage coloration in some species is plain, similar in both sexes; in other species the males are brightly coloured, often with contrasting patches of red and with glossy areas, the females as a rule being more dully coloured. The outermost (tenth) primary is well-developed in Prionochilus, but vestigial in Dicaeum except in D. melanoxanthum. Habitat. Habitat selection is very varied. Some species frequent lowland rain-forest, others the montane mossy forests, and Paramythia montium ascends even to the stunted trees of the timberline. Many species prefer second growth, bamboo groves, and cultivated areas, and may, as in the case of the Scarlet-backed Flowerpecker Dicaeum cruentatum of Burma and Malaya, be common inhabitants of village and town gardens. The New Guinean endemic genera mainly frequent forest understory. The Mistletoebird Dicaeum hirundinaceum of Australia occurs in diverse habitats, ranging from rain-forest to arid Acacia woodland. Distribution. The distribution of the family covers the whole Oriental Region westwards to the drier parts of India, and the Australasian Region (not New Zealand) eastwards to the Solomon Islands. Two species, Dicaeum ignipectus and D. melanoxanthum, range into the Palearctic parts of the Himalayan area and south-western China. Richest in species are the Philippines (13 species, of which 11 are endemic) and New Guinea (11 species, all endemic). The New Guinean genera Melanocharis (with 5 species) and Rhamphocharis (monotypic) are more primitive and have a rather simple structure of the tongue, but in many ways show relationship to PrionochiIus. The New Guinean mono typic genera Oreocharis and Paramythia, as well as the Australian genus Pardalotus (pardalotes or diamond-birds) with 7 species inhabiting the Australian continent and Tasmania, are more aberrant, and their relationship with the typical flowerpeckers is obviously remote. They share with Dicaeum the vestigial outer primary, but differ in having simple tongue structure and in lacking the serration of the bill. Even in habits they differ strikingly. The Tit Berrypecker Oreocharis arfaki resembles a large tit, while the Crested Berrypecker Paramythia montium is the size of a thrush Turdus. The pardalotes come nearest to the typical flowerpeckers in appearance. They are small birds with short tails, tit-like bills, and a variegated plumage in which a spotted pattern is very conspicuous and has given rise to the common names. Nevertheless, the pardalotes may probably belong to a separate family, the Pardalotidae, as protein analysis indicates they are closer to other

those of the family Loranthaceae), nectar, and insects. The pardalotes are almost entirely insectivorous, while the 4 New Guinean endemic genera are fruiteaters. Behaviour and voice. The typical flowerpeckers resemble sunbirds in appearance and general habits. They usually frequent high trees, where they fly restlessly around in search of food, their favourite hunting grounds being flowering epiphytes, strangling figs, or, particularly, clumps of parasitic plants growing high up in the branches. They are energetic and noisy birds that turn and twist about in every kind of attitude and constantly twitter when feeding. During flight they utter rather sharp call notes that can be rendered as chip, chip. Some species have modest warbled songs. The flowerpeckers are not especially gregarious, but appear in pairs or family parties. Breeding. The pendent, domed nests of the typical flowerpeckers are similar to those of sunbirds. They are pear-shaped structures, suspended by the stalk from a twig, with the entrance high on one side, built of vegetable fibres, rootlets, grass, and cobwebs, lined with silky down. The nest of the Thick-billed Flowerpecker Dicaeum agile (Indo-Malayan) differs in its peculiar felt-like fabric. The pardalotes place their nests in holes in trees or hollows or crevices in the ground, or in a tunnel excavated by the birds themselves, usually in the side of a bank. The nest itself is elaborately built of bark and grass, and is usually cup-shapedbut domed in some species. Nests of the endemic New Guinean Paramythia and Melanocharis are cup-shaped and placed in dense bushes. Most flowerpeckers lay white eggs, only Paramythia, Melanocharis and a few species of Dicaeum have spotted eggs. The clutch size is 1--4 (usually 2) in Dicaeum and Prionochilus; 2 in Melanocharis, one only in Paramythia while Pardalotus lays 2-5, usually 4. In the species investigated the female alone builds the nest and incubates the eggs, while both sexes participate in the feeding of the young. In Pardalotus it is known that the excavating of the nesting tunnel is shared by both sexes. Ecological relations. A close association exists between certain flowerpeekers and the mistletoes (chiefly Loranthaceae: Amyema, Lysiana, Muellerina, Dendrophthoe, Viscum). Many species among the typical flowerpeckers feed almost exclusively on the fruits of these plants (apart from insects), and at the same time they constitute by far the most effective disseminators of the mistletoe seeds. In this way a mutual dependency, highly specialized, has evolved between the plants and the birds. In spreading these harmful parasitic plants, which are a serious pest in many areas, the flowerpeckers become important birds from an economic point of view. The method of eating the mistletoe berries differs according to the structure of the bill. The thick-billed species, such as Dicaeum agile, use the bill to separate the fleshy epicarp from the seed, swallowing the former and getting rid of the latter by scraping it off on a twig. The thin-billed species, such as Tickell's Flowerpecker Dicaeum erythrorhynchos of India, swallow the berries whole and void the viscous seeds after an astonishingly short time, usually a few minutes. The seeds are able to germinate in both cases, i.e. whether they have passed through the alimentary canal of the birds or not. The extraordinary rapidity with which the mistletoe fruits pass through the intestines is due partly to the laxative effect of the berries, but mainly to a special structure of the stomach. The muscular stomach has developed into a blind sac with a sphincter at its opening, which construction allows the easily digestible

Australian families than to the Dicaeidae.

Movements. All flowerpeckers are sedentary in high degree, except the Mistletoebird Dicaeum hirundinaceum, which has nomadic habits and is a powerful flyer with long swallow-like wings. Food. The food of the typical flowerpeckers consists of berries (chiefly

229

Red-browed Pardalote Pardalotus rubricatus. (C.E. T.K.).

230

Flower-piercer

berries to pass directly from the oesophagus to the intestine without entering the stomach; on the other hand, insects and spiders, which need grinding and a more thorough treatment before the digestible parts can be assimilated, are not prevented from entering the muscular stomach. The alimentary canal of Melanocharis and Paramythia is not so specialized, but more closely resembles that in other fruit-eating passerines. Owing to their nectar feeding, many flowerpeckers are of importance as pollinators of various flowers, but in this respect playa lesser role than honey eaters (Meliphagidae), sunbirds (Nectariniidae), and some other groups (see POLLINATORS; SEED DISPERSAL.) F.S. Ali, Salim. 1931. The role of sunbirds and flowerpeckers in the propagation and distributionof the tree-parasite, Loranthus longiflorus Dest., in the Konkan (W. India). J. Bombay Nat. Hist. Soc. 35: 114-149. Keast, A. 1958. The influence of ecology on variation in the Mistletoe-bird Dicaeum hirundinaceum. Emu 58: 195-206.

Mayr, E. & Amadon,D. 1947. A review of the Dicaeidae. Amer. Mus. Novit. No. 1360: 1-32.

Parker, S.A. 1963. Nidification of the genusMelanocharis Sclater; Dicaeidae. Bull. Br. Orn. Club. 83: 109-112. Salomonsen, F. 1960--61. Notes on flowerpeckers (Aves, Dicaeidae). Amer. Mus. Novitates: nos. 1990: 1-28; 1991: 1-38; 2016: 1-36; 2057: 1-35; 2067: 1-24; 2068: 1-31.

van Leeuwen, W.M. 1954. On the biology of someJapanese Loranthaceae and the roles the birds play in their life histories. Beaufortia 4: 105-205.

FLOWER-PIERCER: substantive name of Diglossa spp., a group of specialized Neotropical passerine birds (suborder Oscines) formerly included in the family Coerebidae but now treated as members of the tanager subfamily, Thraupinae (see HONEYCREEPER (1); TANAGER). Relationships within this large passerine assemblage are still uncertain, and future research may well modify the arrangement adopted here. The most striking character of the flower-piercers is the form of the bill and associated feeding method. The upper mandible has a sharply hooked tip and is notched along the cutting edge, while the lower mandible, which is a little shorter, ends in a very sharp point. Flower-piercers extract nectar from flowers by hooking the upper mandible round the corolla tube, thus holding it in position while the lower mandible pierces the tube and the tongue, which is unusually long and V-shaped in cross-section, is inserted into the slit. By this means flower-piercers are able to visit and take the nectar from small flowers in very rapid succession, as well as extracting more slowly the more copious nectar from larger flowers. Since they do not come into contact with the reproductive parts of the flower they are 'nectar thieves' rather than pollinators, and where they coexist with hummingbirds they may be important ecological competitors. On occasion, however, they may also extract nectar in the 'legitimate' manner, by inserting the bill into the mouth of the corolla tube if the mouth is wide enough. Not all species of flower-piercers are equally specialized; in some the bill is less highly modified and fruit may be an important part of the diet. Probably all the species also take insects. Distribution. The flower-piercers have their centre of abundance in the Andes, where they are a characteristic element in the avifauna of woodland and shrubby country at subtropical and temperate levels. One species extends to the highlands of Central America, and 2 endemic species occur in the isolated highlands of southern Venezuela. The total number of species of Diglossa is problematical, as there. has evidently been much recent diversification of populations isolated in different parts of the Andes, and it is in several cases not clear whether the isolates have diverged sufficiently to qualify as separate species; 11 species are currently recognized. Characteristics and breeding. Flower-piercers are mainly dull-plumaged birds, largely slaty grey or black in the male and paler grey and olive in the female; but dark shining blue plumage occurs in some species, and in another the black plumage is set off by a conspicuous tuft of white feathers on each flank. Their voices are generally weak and high-pitched. The nest of the only species that has been well studied, the Slaty Flower-piercer D. baritula in Central America, is a substantial cup placed in a shrub or sapling, and the 2 eggs are bright blue spotted with brown. The nestlings are fed by regurgitation, and receive the food into a large protuberant crop, in which respect they resemble the hummingbirds. D.W.S.(l) Skutch,A.F. 1954. Lifehistoriesof CentralAmerican birds. Pacific Coast Avifauna No. 31. Vuilleumier, F. 1969. Systematics and evolution in Diglossa (Aves, Coerebidae). Am. Mus. Novit. No. 2381.

FLUKES: see

ENDOPARASITE.

FLUSH: disturb bird, usually into flight. FLUVICOLINAE: subfamily of Tyrannidae (see

FLYCATCHER (2)).

FLYCATCHER (1): substantive name of the family Muscicapidae (Passeriformes, suborder Oscines), comprising about 150 species distributed throughout the Old World. Characteristics. The species in this large group are very variable in plumage and behaviour but most are about 10-20 em in length and are characterized by broad, flattened bills surrounded by rictal bristles and short, weak legs that are used mainly just for perching. Most of the larger species have long wings and are good fliers, feeding by hawking flying insects in mid-air or by diving from a perch on to insects on the ground. Some of the smaller species feed like warblers (Sylviidae), hopping amongst vegetation and picking insects from the foliage. In the New World the flycatcher ecological niche is occupied by the tyrant-flycatchers of the family Tyrannidae (see FLYCATCHER (2)). Habitat and distribution. The family includes the Ficedula and Muscicapa flycatchers of Europe, Africa and Asia, the Melaenornis and Bradornis flycatchers from Africa, and the Niltava and Eumyias flycatchers from Asia. The habitats occupied come under two broad categories related to foraging behaviour. Some species inhabit parks, orchards, gardens and woodland edges where they sally forth from prominent perches and capture flying insects or prey on the ground, often returning to the same perch again after a capture attempt (e.g. Spotted Flycatcher Muscicapa striata and Verditer Flycatcher Eumyias thalassina). Other species inhabit woodland where they capture insects on the wing amongst the branches or pick up prey from the foliage in the canopy (e.g. Pied Flycatcher Ficedula hypoleuca). Some species may join mixed-species flocks in the foliage of forest trees. In the Himalayas, for example, the Rufous-bellied Niltava Niltava sundara, is frequently seen with small parties of tits, warblers and babblers, snapping up small insects disturbed by the flock as it moves through the trees. Populations and movements. As might be expected from their specialized insect diet, flycatchers are migratory. All the Palearctic species winter in the tropics. The Pied and the Collared Flycatcher F. albicollis winter in Africa south of the Sahara, probably mainly in evergreen forest in the canopy and along forest edges. The Spotted Flycatcher winters from Kenya south to the Cape in thorn country, forest edges and gardens. The Red-breasted Flycatcher F. parua winters in India and Sri Lanka. Species breeding in the Himalayas show altitudinal migration, moving down into the valleys in winter. In the breeding season the Pied Flycatcher inhabits deciduous, and sometimes coniferous, woodland in western and northern Europe. In south-eastern Europe it is replaced by the very similar Collared Flycatcher and there is an area of overlap in central and eastern Europe and on the island of Gotland in the Baltic where the 2 species occasionally interbreed. On Gotland, the Collared Flycatcher is 10 times as abundant as the Pied Flycatcher and the 2 species hybridize (4% of all matings) at frequencies less than predicted for random mating (13 % ) . Mixed pairs produce just as many offspring as same-species pairs but fewer hybrids breed than would be expected from the proportion of hybrid fledglings in the population, probably due to poorer survival after fledging and also, perhaps, to the inefficiency of hybrids at mate attraction. Food. Pied and Collared Flycatchers feed their young on both adult and larval insects, particularly caterpillars collected from the tree canopy. The Spotted Flycatcher takes mainly large flying insects, especially Diptera (Muscidae, Calliphoridae, Scatophagidae, Syrphidae), Lepidoptera and Coleoptera. They also eat bees (Bombus) and wasps (Vespula) and beat these against a perch to remove the stings before swallowing them or giving them to their nestlings. Early in the morning or during cold, wet days, when large flying insects are scarce, they feed up in the tree canopy on swarms of small insects, especially Chironomidae and Aphididae. During the egg laying stage the female seeks out calcium-rich prey including snails (Mollusca) and woodlice (Isopoda) presumably to help her form the egg shells. These prey are also given to the nestlings, probably to help bone growth. Nestlings are given larger prey than the adults eat themselves because it is more economical to carry large prey back to the nest.

Flycatcher

231

In both the Pied and the Collared Flycatcher, some males are successively bigamous and some first year males fail to breed. A male increases his reproductive success through polygamy but his second female suffers because only the first female gets the male's help with chick feeding. A male goes a long way from his first nest site (up to 3.5 km) in order to attract a second female, perhaps to deceive her into thinking that he is unmated. In Britain, the Spotted Flycatcher is one of the last summer visitors to arrive and breed, usually laying at the end of May. This is probably because it is not until fairly late in the summer that there is a guaranteed supply of large flying insects on which this species feeds its young, N.B.D.

Spotted Flycatcher Muscicapa striata. (R.G.).

Behaviour. Most species are territorial in the breeding season. Pied Flycatchers defend their nest holes and Spotted Flycatchers defend their nest sites and favourite feeding perches presumably to avoid interference in prey capture from conspecifics. Male and female within a pair may also avoid interference by feeding in different parts of the territory. Other species, including the Pied Flycatcher, defend feeding territories even during the short stop-overs on migration when they spend a week or so fattening up prior to the Sahara crossing. In the breeding season the nest defence behaviour of the Pied Flycatcher is beautifully adapted to the dangers presented by particular predators. Woodpeckers and squirrels, which are only a threat to the brood, are attacked with swooping dives accompanied by snarling calls. Owls and Red-backed Shrikes Lanius collurio on the other hand prey upon both the adults and the young and are merely mobbed from a safe distance. Experiments with hand-reared, naive birds showed that recognition of these predators is innate. The Spanish population of the Pied Flycatcher, F. hypoleuca iberiae, reacts to owls but not to Red-backed Shrikes, which are absent from Spain. Therefore geographical variation in enemy recognition matches the occurrence of the predators. Voice. Some species have songs consisting of musical warbles but in others the song is very weak and is just a few thin, squeaky notes. Many species utter loud alarm calls, much heard when the young have fledged. Breeding. Some species build neat, open cup-shaped nests in crevices in walls or against tree trunks (Spotted Flycatcher). Others breed in holes in trees (Pied and Collared Flycatchers) and will regularly occupy nest boxes. The Black and Orange Flycatcher, Ochromela nigrorufa, of southern India builds an enclosed nest of moss, with a side entrance, under tree roots on the forest floor. Sometimes the old nests of other species are used, for example old thrush and blackbird Turdus nests (Spotted Flycatcher), old weaver bird nests (Swamp Flycatcher Alseonax aquaticus) and old woodpecker holes (Pied Flycatcher). The eggs of flycatchers are blue, brown, red, yellow or white in background with spots and mottling. In tropical or subtropical species the clutch is usually 2-3 eggs but in temperate regions it is larger (usually 5-7 but up to 10 in the Pied Flycatcher and usually 4-5 in the Spotted Flycatcher). In Ficedula spp. it is usually the female who incubates alone but in other species both sexes take part. Both parents feed the young. Incubation and nestling periods are both about 10-15 days. In the Spotted Flycatcher the male may provide up to 30% of the female's food by courtship feeding during the egg-laying period and he also feeds her while she is incubating on the nest. In the Pied Flycatcher the male may provide the incubating female with half her food requirements. There have been several detailed population studies of the Pied Flycatcher with densities of up to 4 nests per hectare. Early broods are more successful than late broods, reflecting the decline in the abundance of the caterpillar food for the young. There is a seasonal decline in clutch size; for example in the Forest of Dean in England, mean clutch size is 7.5 at peak in May and 4.5 in the middle of June.

Alatalo, R.V., Carlson, A., Lundberg, A. & Ulfstrand, S. 1981. The conflict between male polygamy and female monogamy: the case of the pied flycatcher Ficedula hypoleuca. Am. Nat. 117: 738-753. Alatalo, R.V., Gustafsson, L. & Lundberg, A. 1982. Hybridization and breeding success of Collared and Pied Flycatchers in the Island of Gotland. Auk 99: 285--291. Bibby, C.}. & Green, R.E. 1980. Foraging behaviour of migrant Pied Flycatchers, Ficedula hypoleuca, on temporary territories. J. Anim. Ecol. 49: 507-521. Campbell, B. 1955. A population of Pied Flycatchers, Muscicapa hypoleuca. Proc. XI Int. Orne Congr: 428-434. Curio, E. 1975. The functional organization of antipredator behaviour in the Pied Flycatcher. A study of avian visual perception. Anim. Behav. 23: 1-115. Davies, N.B. 1977. Prey selection and the search strategy of the Spotted Flycatcher, Muscicapa striata: a field study on optimal foraging. Anim. Behav. 25: 1016-1033. Lack, D. 1966. Population Studies of Birds. Oxford. von Haartman, L. 1949, 1951, 1954. Der Trauerfliegenschnapper. Acta zool, Fenn. 56: 1-104; 67: 1-60; 83: 1-92.

FLYCATCHER (2): substantive name of most species of Tyrannidae (Passeriformes, suborder Deutero-oscines, infraorder Tyranni); in the plural forms 'tyrant-flycatchers' or 'New World flycatchers', general name for the family; a diverse assemblage of 375 species in about 90 genera, entirely restricted to the New World, predominantly the Neotropical realm where it is numerically the dominant land-bird family. Other major substantive names for members of the family include 'tyrant', 'tyrannulet', 'kingbird', 'phoebe', 'pewee', 'flatbill', and 'elaenia'. Systematics. Closely related to Cotingidae and Pipridae, with which its taxonomic boundaries have been enigmatic. Presently considered to contain at least 3 subfamilies, Elaeniinae, Fluvicolinae, and Tyranninae; by some authors, a fourth subfamily, Tityrinae, is provisionally moved to this family from Cotingidae. The family is defined primarily by cranial, syringeal, and tarsal characters. Characteristics. In its great diversity of body forms and foraging styles, the family replaces numerous Old World families, principally the Muscicapidae (see FLYCATCHER (1)). The family includes ecological counterparts of warblers, wrens, vireos, jays, shrikes, pipits, thrushes, and certain icterids, as well as many sorts of aerial flycatching species of various families. Body sizes range from the smallest passerine species (Short-tailed Pygmy-Tyrant Myiornis ecaudatus; total length 5 em, wing length (3.0-3.5 em) up to medium-sized birds in the genera Agriornis, Xolmis, Tyrannus and their relatives (wing lengths 11-14cm). Body weights span from 4.5-80 g. Sexual dimorphism in size is minor, males averaging slightly the larger. Variation in body form is primarily associated with the diversity of foraging styles. Wings are short and rounded among the tody-tyrants iTodirostrum, Hemitriccus, and related genera), which glean prey with short hops in dense foliage. Wings are long and pointed in the many genera that forage with powerful aerial sallies in open places, such as the kingbirds Tyrannus spp. and pewees Contopus spp. Deeply forked and greatly elongated tails occur in many of these 'aerial hawkers', including the genus Tyrannus (contains Scissor-tailed T. forficatus and Fork-tailed T. savana Flycatchers, formerly genus Muscivora), in the Streamer-tailed Tyrant Gubemetes yetapa, Long-tailed Tyrant Colonia colonus, and others. Tarsi vary from extremely short in the Cliff Flycatcher Hirundinea ferruginea, to long and strong in several terrestrial genera such as Muscisaxicola, Muscigralla and Machetornis. Bills tend to be broad at the base, but great variation is evident in this character as well; the longest and broadest bill is that of the Boat-billed Flycatcher Megarhynchus pitangua; specialized, wide and spatulate bills occur in the spadebills Playtrinchus spp., flatbills Rhynchocyclus spp., and relatives; narrow, warbler-like bills occur in several genera (e.g. Ornithion, Camptostoma, Inezia) that probe and glean for insects without sallying from perches.

232 Flycatcher

Rictal bristles are in general well developed, excessively so in Onychorhynchus, Myiobius spp. and relatives; in species that are either heavily frugivorous (e.g. Elaenia spp.) or do not sally while foraging (e.g. Southern Beardless Flycatcher Camptostoma obsoletum), rictal bristles are reduced or absent. Overall coloration typically is drab; the most common pattern is olive-green above, bright or pale yellow to whitish below, with or without pale superciliary eye rings, stripes, or wingbars. Other colours include browns, greys, black and white. Bright colours besides yellow are rare, and blue is virtually absent. Eight tyrannine genera share a common colour pattern of bright yellow underparts, dull olive back, and contrasting black or grey and white stripes on the crown. Many species show slight to well developed crests. Semi-concealed red, orange, yellow, or white crown patches occur in 30 of the 90 genera. The most extreme crown ornamentation is a long, erectile crest of brilliant orange feathers tipped iridescent blue, in the Royal Flycatcher Onychorhynchus coronatus. Pronounced sexual dimorphism in plumage is rare except in one group of fluvicoline genera, in which males typically are black or black-and-white, and females are brownish (e.g. Knipolegus, Fluvicola, Alectrurus). The male Vermilion Flycatcher Pyrocephalus rubinus is predominantly brilliant scarlet, unique in the family. The Many-coloured Rush Tyrant Tachuris rubigastra, a marsh-dwelling species of Argentina and the high Andes, shows a harlequin pattern of reds, yellows, blue, green and black. Habitat. Foliage-gleaning species, which predominate, occur in all vegetation types from temperate woodlands and tropical desert scrubs to dense deciduous and evergreen forests, from treeline to sea-level. Aerial hawking flycatchers occupy open, forest-edge habitats, water margins, and cliff faces. Terrestrial species, such as the Cattle Tyrant Machetornis rixosus and various ground-tyrants (genus Muscisaxicola), predominantly occupy savanna or bare, rocky alpine habitats. Many species dwell along stream, river, and lake margins, where they may take aerial prey (e.g. Black Phoebe Sayornis nigricans), aquatic prey from the surface (e.g. Lesser Kiskadee Pitangus lietor) or even from underwater (e.g. Greater Kiskadee Pitangus sulphuratus, a frequent fish-eater). Distribution. Found virtually throughout the New World, tyrantflycatchers occur from the taiga of Alaska and northern Canada (where all species are migratory) south through the Americas and West Indies to the southern tip of South America and adjacent islands, including the Galapagos Archipelago (2 species). Only about 30 species occur north of Mexico. Greatest diversity is reached in the Amazonian and eastern Andean forests. More than 70 species have been found together at several localities in western Amazonia. Many lowland species occur throughout the forested Neotropics. Certain open-country species such as the Tropical Kingbird Tyrannus melancholicus and Vermilion Flycatcher occur from southern North America south to central Argentina. Others, especially those inhabiting cloud forests or oceanic islands, show greatly restricted distributions. Movements. All species that breed in North America are at least partially migratory, wintering primarily in Central and northern South America. In some species only the northernmost populations migrate. The Eastern Kingbird Tyrannus tyrannus migrates in huge flocks from as far north as Alaska and northern Canada south as far as Bolivia and northern Argentina. Many long-distance migrants, such as the Eastern Wood Pewee Contopus virens, maintain exclusive territories on their wintering grounds. Many, perhaps most, of the temperate-zone species of Patagonia, southern Argentina, and even southern Brazil migrate northward to equatorial latitudes. The Piratic Flycatcher Legatus leucophaius migrates entirely within tropical latitudes, apparently in response to seasonal patterns of fruiting by tropical forest trees. Local movement patterns within tropical forest regions by Olive-striped and Ochre-bellied Flycatchers and relatives (Mionectes spp.) have been recently documented, but remain poorly understood. Food. Feeding habits vary enormously within the family, but nearly all species are predominantly insectivorous. Insects of all kinds are eaten, most frequently snatched from the air or from leaf surfaces during a rapid, sudden flight (sally) from a stationary perch. Some species, like the shrike-tyrants Agriornis spp. and the monjitas Xolmis spp., drop to the ground from exposed perches in the manner of bluebirds (Sialia). Others, mentioned above, take various invertebrates while walking on the ground. The larger species, especially the Greater Kiskadee, frequently feed on fish, tadpoles, frogs and lizards as well as large moths, orthopterans and other arthropods. Many tropical species regularly eat fruit from vines, mistletoes, or trees. The Piratic Flycatcher and several

Eastern Kingbird Tyrannus tyrannus. (R.G.)

species of Elaenia and relatives are almost entirely frugivorous during much of the year. Behaviour. Most species live as monogamous pairs on territories, in a relatively simple social structure. Some migratory species, such as the Variegated Flycatcher Empidonomusvarius, and the Fork-tailed Flycatcher Tyrannus savana, congregate in flocks of up to several hundred individuals during the non-breeding season, but no true coloniality is known to occur in any species. Intra- and interspecific communal roosting occurs among some tyrannine species. Helpers at the nest occur in a few species, especially the White-bearded Flycatcher Conopias inornatus, but this, too, is uncommon. The Piratic Flycatcher breeds within large colonies of caciques (Icteridae), whose nests it takes over through harassment. Members of the genus Mionectes (incl. 'Pipromorpha' spp.) are known to exhibit loose LEK behaviour in their forested habitats, associated with their highly frugivorous diet. Some sexually dimorphic grassland species, especially the Cock-tailed Tyrant Alectrurus tricolor, may be polygynous. This and numerous related species have peculiar and highly stereotyped aerial displays. The Spectacled Tyrant Hymenops perspicillata, in which the all-black male has wide, fleshy yellow eyerings, performs spectacular aerial loops and somersaults over its marshy habitat during courtship. Tail flicking or pumping is common, particularly among terrestrial forms such as the Masked Water Tyrant F luvicola nengeta. The tail is cocked and spread like a fan during active foraging by Myiobius spp. Wing-stretching, flicking, whirring or buzzing are featured in the territorial or courtship displays of almost all species. The Common Tody-Flycatcher Todirostrum cinereum cocks its tail vertically and hitches sideways along a perch during such a display. Voice. Tyrant-flycatcher vocalizations are notably simple and weak, with only a few exceptions. Most species whistle uncomplicated single syllables, phrases, or short trills. These include some of the least conspicuous advertising songs of any species of Passeriformes. The most remarkable vocal feature of the family is the propensity of nearly all its members to utter repetitive 'dawn songs', at or before first light during breeding seasons. These typically include more extended and complicated versions of the simple, daytime advertising songs, but in some species certain vocal patterns are restricted to this period of active calling. Thus, in the Neotropics, flycatchers of many species are frequently the first birds to be heard vocalizing as dawn breaks. Aerial displays are accompanied by special flight songs in some fluvicoline species and in the kingbirds. Breeding. Nest structure varies considerably. Most typical is a simple cup placed in a forked twig or stem, as in the genera Empidonax and and Tyrannus. Cups may be elaborately decorated with mosses and lichens, as in Contopus and Elaenia. Bulky, ball-shaped globular nests of grasses and twigs are built by Greater Kiskadee, Masked Water Tyrant, Social Flycatcher Myiozetetes similis, and others. Pendulous, purse-shaped nests with side entrances characterize the tody-flycatchers (Todirostrum) and

Folklore, birds in

numerous related genera. All members of the genus Myiarchus nest in natural cavities, and line their nests with soft animal matter, virtually always including pieces of shed snake skin. Other cavity-nesters include the genera Rhytiptema, Attila, Myiodynastes, Machetornis, and the Whiteringed Flycatcher Conopias parva. Clutch size varies from 3-5 in North America (but up to 8 in Great Crested Flycatcher Myiarchus crinitus), and is usually 2-3 in the Neotropies. Incubation time typically ranges from 14-20 days, followed by nestling periods of 14-23 days. Independent young of many tropical species remain with their parents to form family groups for nearly a year after fledging. With rare exceptions, both sexes construct the nest and feed the young. Only females incubate eggs or brood young. Many species regularly attempt more than one brood in a single season. (S.M.) J.W.F. Fitzpatrick, J.W. 1980. Foraging behavior of Neotropical tyrant flycatchers. Condor 82: 43-57. Fitzpatrick, J.W. 1980. Wintering of North American tyrant flycatchers in the Neotropics. In Keast, A. & Morton, E.S. (eds.). Migrant Birds in the Neotropies: Ecology, Behavior, Distribution, and Conservation. Symp. Nat. Zool. Park, Smithsonian Inst., Washington, D.C. Traylor, M.A., Jr. 1977. A classification of the tyrant flycatchers (Tyrannidae). Bull. Mus. Compo Zool. 148: 129-184. Traylor, M.A., Jr. & Fitzpatrick, J.W. 1982. A survey of tyrant flycatchers. Living Bird 19: 7-50.

FLYCATCHER-SHRIKE: alternative substantive name of some species of Campephagidae (see CUCKOO-SHRIKE). FLYCATCHER, SILKY: see SILKY

FLYCATCHER.

FLYCATCHER-WARBLER: name sometimes given to Seicercus spp. (see WARBLER (1)). FLYEATER: Getygone sulphurea, the only south-east Asian member of the predominantly Australian genus Gerygone (see WARBLER, AUSTRALIAN).

FLYW AY: a major route for birds on migration (see MIGRATION). FODI; FODY: substantive name of Foudia spp. (see WEAVER). FODITANY: substantive name applied to two Madagascan BULBULS of the genus Phyllastrephus, and to the aberrant Madagascar BABBLER Oxylabes madagascariensis. FOLIAGE-GLEANER: substantive name of species in several genera (e.g. Automolus) of Furnariidae (see OVENBIRD (1)). FOLKLORE, BIRDS IN: folklore is a term of somewhat imprecise application, mingling as it does with myth, legend, fable and oral literature, and reaching out toward magic and religion. For present purposes bird folklore may be defined as the total corpus of beliefs, half-beliefs, tales and sayings, fanciful or otherwise, orally transmitted and of undetermined authorship, which are referable to genuine species. (For discussion of wholly invented or composite species see FABULOUS BIRDS.) Its origins lie in observation as well as imagination, with misinterpretation in between. It may be assumed that birds have been the concern of men for as long as humankind has existed: on the material side as a food source for the hunter and later as a competitor for food with the farmer; as a supplier of plumage for adornment and for warmth, and of such accessories as feathers for arrows and bones for beads and whistles; and as practice targets for apprentice hunters (see ORNAMENTATION, BIRDS IN HUMAN). Although true domestication has been accepted by very few species, the keeping of birds as pets may go back to the remote past, to judge by the fondness of 20th century Stone Age peoples in Amazonia for their shoulder-tame macaws Ara ararauna, or the young cassowaries Casuarius spp. running loose in Papuan villages. On the non-material side, the readiness of men to ascribe human characteristics to other creatures is with us yet. In the minds of preliterate peoples, for whom the barrier between natural and supernatural hardly exists, all animals and often plants must needs live on the spiritual as well as the earthly planes. Thus a bird that is notably wily or swift or cruel or nutritious must possess particular powers, to be courted, countered, revered or borrowed; and upon such relationships myths are built. The antiquity of this preoccupation is illustrated by palaeolithic cave-paintings of bird-men (whether

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gods, decoys, disguised hunters or all three is not always clear), and its refinement by Horus the Hawk God of dynastic Egypt, who personified the rising sun. Some myths have the force of religious tenets. For the Hebrews a dove discovered dry land after the Flood, and for the Crow Indians in Montana diving ducks sent down by the Creator brought up mud from below the primaeval waters to make the Earth-to give but two examples of a widespread theme. Over much of native North America rainfall is controlled by the Thunderbird, conceived of usually as an eagle but sometimes as a hawk, and in the interior of British Columbia as a grouse. In all cases it is the flashing eye that generates lightning and the flapping wings that reverberate. As has been said, other creatures besides birds have their mythic roles and, despite his luxuriant plumage, Quetzalc6atl the Plumed Serpent, god of wind and scholarship in ancient Mexico, appears to have been a reptilian rather than an avian mutant. He is much, much older than the eagle with a serpent in its talons which was the sign for the 14th century Aztecs that they had reached their Promised Land. Not all bird lore is so portentous. Tales told purely for entertainment have abounded in both Old and New Worlds, wherein birds appear as protectors, tricksters or comics. A favourite genre, echoed in Kipling's Just So Stories, recounts the origins of particular shapes or plumages: in Europe the Robin Erithacus rubecula scorched its breast bright red while stealing fire from the sun, and the Crossbill Loxia curvirostra twisted its beak on the nails of the Cross; in Manitoba the Sapsucker Sphyrapicus varius acquired its many hues as consolatory gifts from other birds because it had been too tipsy on birch juice to attend the official distribution of colours. In the Orient some birdlike beings of no clear faunal affinity have entrenched themselves in the great religions (see FABULOUS BIRDS). In the West the bird spirits have been banished by Christianity or diminished, sometimes by way of witchcraft, into mere harbingers of good or bad luck. The dove (when not pronounced 'pigeon') and the crowing cock have maintained an odour of reasonable sanctity, and the Swift Apus apus has about lived down a reputed collusion with the Devil, but the superstitious still know that any bird-especially a black-as-night corvid-that strikes at a window is summoning a human soul to the grave. Attitudes to birds as expressed in British folklore are not always consistent. The Wren Troglodytes troglodytes, which shares with the Goldcrest Regulus regulus and Firecrest R. ignicapillus a variety of ironic European names denoting petty kingship (Regulus, Latin; Roitelet, French; Reyezuelo, Spanish-sometimes downgraded to Abadejo, petty abbot), is traditionally killed and paraded on St Stephen's Day in England and Ireland to a satirical refrain dubbing it King of All Birds. This despite the West Country warning that 'Who kills a Robin or a Wran, shall never prosper, boy or man', and similar minatory verses current in Scotland. The Magpie Pica pica likewise enjoys a mixed reputation, 'One for sorrow' offset by 'One's a wish'. Owls, highly regarded in Classical Athens and relied upon to deflect lightning in England as in China, are associated with the black arts in both hemispheres and can still induce the crossing of fingers in the role of Shakespeare's 'fatal bellman, that gives the stern'st goodnight'. Perhaps darkness has something to do with it; by daylight the wise old owl is among the most popular of avian symbols. An important branch of bird folklore is that which may be classed as alternative ornithology, based on day-to-day observation, but leaning heavily on conjectural explanations of what was not, in pre- 'scientific' conditions, observable. The empirical approach has engendered some sound proverbs or 'country' sayings; the hypothetical conclusions have been shrivelled by science. It is probably good if expensive husbandry to plant one bean for the rook and one for the crow in addition to the one to grow. It is certainly true that the first Swallow Hirundo rustica may arrive in England before the last cold snap, so that one alone does not indeed make a summer. On the other hand it is no longer averred that swallows spend the winter dormant beneath the streams they skim over in autumn; that the Cuckoo Cuculuscanorus and the Merlin Falco columbarius are the summer and winter phases of one and the same species; that the 14 halcyon days during which the seas remain calm are those needed by the Kingfisher or Halcyon Alcedo atthis to safeguard the eggs in its floating nest of fish bones; nor yet that the cirriped barnacle is the embryo of the Barnacle Goose Branta leucopsis. Vicariously related to bird lore proper are the Gabriel Hounds, the nocturnal pack whose funereal baying overhead has been explained away as the flight calls of Brent Geese Branta bernicla. The ominous function of

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FoUicle, feather

some other species, notably owls and corvids, has been touched on above; the institutionalized role of birds in augury in S.E. Asia is treated in detail under a separate heading (see OMENS, BIRDS AS). A wealth of perception, imagination, whimsy and onomatopeia resides in English local or folk-names of birds, and some of it is intriguing. The erroneous reason for calling the Nightjar Caprimulgus europaeus a Goatsucker is familiar enough, but why also Corpse-hound (a distinction shared with the Whimbrel Numenius phaeopus)? The Wryneck Jynx torquilla is Cuckoo's Mate because it arrives a day or two ahead to prepare the way for the Cuckoo-s-which name itself, amended with the pejorative termination '-old', bespeaks the bird's involvement with fertility. Association with wet weather belongs equally, for differing reasons, to the Green Woodpecker Picus viridis and the Red- and Black-throated Divers Gavia stellata and G. aretica, which are Rain-bird and Rain-geese respectively. The Hooded Crow Corvus corone cornix is called a Kentish Crow in Norfolk, an Isle of Wight Crow in Sussex, a Danish Crow in East Anglia and a Dutch Crow in Yorkshire; the North Country's Wetwang Greyback sounds less discriminatory. Storm Witch for the Storm Petrel or Mother Carey's Chicken Hydrobates pelagicus reflects the mariner's belief that the bird lived totally invisible until the onset of tempest. The stripling Oxfordshire cronies who taught me Bumbarrel for the Longtailed Tit Aegithalos caudatus cared naught for semantics. It is very desirable that ornithologists who come across any local or traditional sayings, stories or customs to do with birds should make sure that they are, or that they already have been, recorded. As a counterbalance to the histogram, folklore provides insights both valuable and entertaining into Man's long association with the world of birds. Mainly, to be sure, as it has been in the past-but Her Britannic Majesty's Government still takes precautions against the disaster that would befall the realm were the Tower of London to lose its Ravens Corvus corax. (E.A.A.) G.E.S.T. Armstrong, E.A. 1958. The Folklore of Birds. London. Jackson, C.E. 1968. British Names of Birds. London. Lockwood, W.B. 1984. The Oxford Book of British Bird Names. Oxford & New York.

FOLLICLE, FEATHER: see FEATHER. FOLLICLE, OVARIAN: see ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM. FOLLOWING RESPONSE: see under IMPRINTING. FOOD: see FEEDING HABITS; FOOD SELECTION; PARENTAL CARE; PIRACY; PREDATION; also ALIMENTARY SYSTEM; GRIT; METABOLISM; NUTRITION; PELLET. FOOD, BIRDS AS HUMAN: see UTILIZATION BY MAN. FOOD CHAIN: see ECOLOGY. FOOD DEFICIENCY: see DISEASE. FOOD PASS: aerial food presentation by the male raptor to the female, usually taking place during the periods of courtship, incubation, and brooding of the young. FOOD SELECTION: an aspect of behaviour (see FEEDING HABITS), of interest also from the evolutionary and ecological points of view in that closely related species living in the same habitat do not compete for food (as postulated first by D. Lack and now generally accepted). Although some avian species are specialized for selecting a particular type of food, e.g. the FLAMINGOS, many are rather catholic in their choice and take a variety of items. This wide range of food items is apparently due to an initial response to a few generalized stimulus situations, each characteristic of a variety of objects. The effective stimuli are later narrowed by learning, the course of which is determined not only by the food within the environment, but also by the behaviour patterns, sense organs and body structures available for finding it. Distantly related species may show marked innate differences in the stimuli that elicit their feeding responses. Between closely related species, however, such innate differences are often more difficult to detect. Sometimes competition is avoided by differences in habit selection or in the selection of the feeding niche within the habitat. In other

cases, small differences in behavioural or physical characteristics prevent overlap in diet. Thus tits, but few other species, learn to open milk bottles because they have the necessary motor patterns; and the size of seeds taken by finches is determined in large part by the size of the bill-each species learning to take the most suitable seeds. The ability of many birds-including Jays Garrulus glandarius, Magpies Pica pica, some finches and tits-to use the foot with the bill is often characteristic of the species, but learning helps towards its perfection. It enables food sources to be tapped that would otherwise be unavailable: thus Magpies pull down and stand on grass stems while they peck out the seeds, and Goldfinches Carduelis carduelis use both bill and foot to feed on thistle seeds. The BILL and other structures used in feeding are adapted to conditions in the localities inhabited by the species. Populations adapted to different conditions and meeting later may therefore select different diets, not because of innate differences in responsiveness, but because they learn to eat those foods to which they are structurally adapted (Hinde 1959). The first appearance of pecking in the young of nidifugous birds is not dependent on learning: they may peck at a number of different items, provided that they contrast with the background, and accuracy improves with experience. Should the object be of a suitable size, it may be swallowed. If the effect is not then unpleasant, the action may be repeated and the animal comes to distinguish the edible from the inedible. In the food selection of most birds, the visual sense is paramount; TASTE and TOUCH are also important, but the other senses less so (although nocturnal birds such as owls hunt by sound, and at least the kiwis and Oilbird Steatornis caripensis use an ability to detect ODOUR-see also SMELL). The stimuli that elicit the greatest pecking response have been tested in a variety of birds. In particular, the newly-emerged young of species that hatch with their eyes open have been found to peck selectively at objects that differ in size, shape, height and in speed of movement. Young birds with little visual experience and no opportunity for direct learning have been tested also for their differential response to colour. It is known that closely-related species tend to have similar colour preferences, and in many cases these preferences have selective advantages. Hence gulls and terns peck at red and orange, and these colours often, but not always, appear on the parents' bill at which the young bird pecks for food. The chicks of the Oystercatcher H aematopus ostralegus and Moorhen Gallinula chloropus also select red, as does the Coot Fulica atra although the adult bill is white. In studies of young ducks and pheasants, which obtain their own food from the start, it has been shown that almost all species prefer green. The preferences of some adult birds can be inferred through a study of bird-pollinated flowers and bird-distributed fruit (see POLLINATORS; SEED DISPERSAL). Some 84% of the former are red or orange, while red, orange and black berries are vastly more common than those of any other colour. The Browers (1964) suggest that food has a variety of flavours that conveys no information to the naive bird who will accept initially a wide range of items. If the animal eats and then vomits, it will associate the taste of the food being expelled through the mouth with an uncomfortable 'gut reaction'. Originally a gourmand, the bird is now a gourmet, and taste will thereafter convey useful information. Once conditioned, the bird judges potential food by taste. Obviously the next, more efficient, stage is to recognize prey by sight alone before it needs to be caught and tasted. The complexity of food selection is illustrated by the work of Krebs (1978) among others, on OPTIMAL FORAGING (see also OPTIMALITY THEORY). The hypothesis here is that an animal searching for food must make decisions that maximize its rate of food absorption: it must decide which type of food it will eat, where it will hunt, and what search path it will adopt. Any item eaten has a cost in terms of time taken to find, catch and consume it, and a benefit in terms of net nutritional intake. Predators should (a) prefer more nutritious (profitable) prey, (b) be more selective when such profitable prey items are uncommon and (c) should ignore unprofitable items no matter how common they are. These predictions have been tested and it can be shown that (c) does not apply if the time taken to recognize unprofitable prey lowers the overall rate of food intake. Thus caged Great Tits Parus major do not completely ignore unprofitable items if they are abundant and mixed at a high density with profitable ones. Either the birds require time to recognize prey or they need to sacrifice a certain amount of efficiency to acquire information by 'sampling' the relative nutritional value of each food type. Active birds

Food storing

will search where food is clumped or patchy in distribution but, again, the need to collect information through sampling may cause them to deviate from optimal behaviour . In considering the search path that the foraging bird will take, it can be predicted that a non-random route is most likely, at least in situations where the prey is not replenished rapidly, if only so that the bird does not waste time crossing its own path . Blackbirds Turdus merula, for instance , will alternate left and right turns in their search path, but after finding an earthworm, tend to make successive turns in the same direction. In a fluctuating environment (and most environments do change with time), the bird's problem is to update continually its estimates of capture rate and availability so that it can always make the 'best' decisions. Many temperate-latitude species are known to change their diet with the seasons, coinciding with the onset of breeding, migration, the feeding of young, the moult and a changing climate. To some extent this is a matter of food availability, but preferences are governed by internal changes. Domestic hens can learn to select food so as to correct for some deficiencies, and Red Grouse Lagopus lagopus scoticus have been found to prefer 3-4 year old heather that is richer in nitrogen and phosphorus . Parental example and social experience are likely to affect food selection, the latter especially in flocking species. Most parent birds provide potential dietary guidance . Duck s and geese lead their young to suitable feeding grounds , and most gallinaceous birds pick up and drop a morsel of food apparently to draw it to their chicks' attention . Young rails follow their parents and are fed from their bills, and even sometimes obtain food from juveniles of the previous brood. In many other species, the parents bring food to their offspring. The importance of this early experience is not known; in parasitic species, at least, it sometimes appears to be slight. Cuckoos and honeyguides do not parasitize host species that give 'unsuitable' foods or cannot collect enough . Eggs laid by female Cuckoos Cuculus canorus 'taken short' in the nests of 'wrong' species often hatch but the young one seldom fledges. Yet no host brings the food that makes the diet of adult cuckoos and honeyguides unique: hairy caterpillars on the one hand and beeswax on the other. The feeding behaviour of flocking species may be influenced by companions in three ways: by SOCIAL FACILITATION, by imitation and by what has been called 'local enhancement'. Social facilitation usually affects the quantity offood that the individual takes and , apart from vocal mimicry, there is not a lot of evidence for direct imitation in birds. Normally it is 'local enhancement' that accounts for the spread of new feeding habits among birds: one bird happens upon a previously untapped food source and others are led in that direction . Examples are the opening of milk bottles by tits and the appearance of Great Spotted Woodpeckers Dendrocopos major at bird tables. Often prolonged severe weather and food scarcity seem to encourage searching and lead to the discovery of new food supplies. Such novel behaviour patterns perhaps originate with young birds during the first year of life; their actions are observed by other juveniles and eventually by their offspring. Thus new habits become traditional, without the usual limits of acquired behaviour that disappears with the death of the individual. The tendency for new feeding behaviour to arise varies from species to species and differences in adaptability seem to be genetic in origin. Possibilities for interaction between the members of a flock are obviously influenced by the proximity of feeding individuals. Crook (1965) showed how the social organizations of birds are related to the type of food eaten and to its dispersion within the habitat. Food that is scattered or cryptic, difficult to find and difficult to catch, must be searched for by stealth, speed and skill. Birds dependent on this type of food, such as birds-of-prey (Accipitriformes, Falconiformes), are solitary feeders because any gregarious behaviour interferes with individual methods of acquisition, and their feeding methods in consequence tend to be stereotyped. If food is commoner in some parts of the environment than in others, congregation by the birds may be advantageous in increasing the ability to locate and exploit it effectively. In this group are swifts and many nectar-feeders, insectivores with broad diets such as tits, and ground-feeders. These birds normally tolerate other feeding individuals close by, although a change of feeding habit (to feed young, for instance) may change the closeness of foraging, and territorial behaviour develops. It is when food is found sporadically in patches within the habitat and does not require skill to catch it that the greatest gregariousness occurs. Foraging in a flock prevents repeated sampling of areas already covered and this may be of especial value when food is scarce. A member of the flock, by the very act of feeding, indicates where there is

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food and other birds move towards it-a precise example of 'local enhancement'. This applies especially to fruit-eating birds, such as many parrots, whose frequently bright colours and raucous voices indicate to their own and other species the locality of clumps of ripe fruit which are shared. It is in these social groups that the greatest possibility for change J.K.(l ) in food selection by demonstration exists. Brower, L.P. & Brower, J.V.Z . 1964. Birds, butterflies and plant poisons, a stud y in ecological chemistry . Zoologica New York 49: 137-159. Crook, J.H. 1965. The adaptive significance of avian social organisations. Symp. Zoo!' Soc. Lond . 14: 181-218. Hailmann, J.P. 1967. The ontogeny of an instinct : the pecking response in chicks of the Laugh ing Gull (Larus atricilla L. ) and related species. Behaviour Supp!. IS. Hinde , R.A. 19S9. Behaviour and speciation in birds and lower vertebrates . Bio!. Rev. 34: ins-no. Kear, J. 1972. Feeding habits of birds . In Fiennes , R.N .T .W. (ed.). The Biology of Nu trition. Oxford . Krebs , J .R . 1978. Opt imal foraging : decision rules for predators. In Krebs, J.R . & Davies, N .B. (eds.), Behavioural Ecology. Oxford .

Nutcracker Nucifragacaryocatactes digging in the snow for nuts that it has hidden. (Photo; P .O. Swanberg).

FOOD STORING: temporary storing ('hoarding') of food in sites other than where it was collected. The time between storing an item and eating it may vary between a few hours in tits and up to a year in certain woodpeckers and corvids. Storing in different forms is well developed among several bird families, notab ly crows and their allies, tits, nuthatches, shrikes, woodpeckers and also among certain diurnal raptors and owls. For example, Thick-billed Nutcrackers Nucifraga c. caryocatactes during autumn collect large numbers of hazelnuts Corylus avellana several km from their nesting territories in coniferous forest, storing loads of 15-20 nuts in many different locations on the ground, and carefully covering the sites with vegetation . During winter and spring, the Nutcrackers subsist and raise their young on the stored nuts, which they recover with great precision . Swanberg (1951) found that 86% of the attempts at digging up nuts through thick snow-cover were successful, and the precision did not decrease over the winter . Nutcrackers hence memorize the storing sites, and also which caches they have previously emptied . Food storing is also important in N . c. macrorhynchos, and in the North American Clark's Nutcracker N . columbianus. Another species with advanced food storing is the Acorn Woodpecker Melanerpes formicivorus . Territorial groups of up to a dozen birds store large numbers of acorns in a few granary trees, in which the woodpeckers have excavated suitable storage holes. The group members communally defend the 'larders' against food competitors of the same and other species. The social organization of Acorn Woodpeckers is related to the feasibility of acorn storage: when food cannot be hoarded in sufficient quantity, the birds do not form social groups but nest in solitary pairs and migrate during winter , a remarkable social flexibility. Ecological factors promoting hoarding. The survival value of food storing should usually increase with, among other things, the likelihood that (a) food withstands extended storing without decay; (b) food will be less abundant in the period ahead, or the forager will then require more food, for example during reproduction; (c) the storing individual itself will be able to recover the food. Hoarding seems to fit such a pattern. (a) The most commonly stored items are energy-rich seeds or nuts with protective cover, which are sometimes preserved for over one year without serious decay. Bird's eggs are often hoarded by crows, foxes and martens . Tits store insects mainly during autumn, and low temperatures during the following winter may

236

Food storing

Great Spotted Woodpecker Dendrocopos major storing cones. (P hoto:

H . Schouten ).

retard their decay, but it is doubtful whether hoarded insects remain unused for such a long period . Raptors and owls store small mammals and bird s for short periods of usually a few days, both outside and during the breeding period; so do certain shrikes with insect s and small vertebrates. (b) Most storing species occur in North Temperate areas, with great differences in food abundance between the autumn storing season and the recovery period during winter and spring. The few known cases of storing in the tropics occur among highland species, for which food abundance may vary due to seasonal fluctuations in rainfall. Further studies in the tropics are needed to test whether hoarding is less common in stable environments with little seasonal variation. Nesting raptors , owls and shrikes which store food over brief periods might gain two advantages: ( I) buffering against temporary food short age due to, for example, inclement weather which impedes hunting; (2) boosting the growth of chicks when their food requirements are highest and they consume food faster than the parents can gather it. (c) The chances that the hoarder itself will recover the food should be greatest in sedentary species with individual or pair territories. Food storing seems to be crucial for the non-migratory habit in the Acorn Woodpecker. Most hoarding birds are resident species which forage on individual, pair , or group territories. Among colonially nesting birds , the Rook Corvus frugilegus regularly and the Jackdaw C . monedula sometimes hoard food. Scatterhoarding and larderhoarding. 'Scatterhoarding' the food in numerous small and dispersed caches, and hiding it in the ground, below vegetation, in bark crevices or tree holes is common among hoarding birds, also among species which live in groups. Scatterhoarding reduces the risk that competitors will discover and consume the stored food . ' Larderhoarding' of food in concentrated, more conspicuous stores occurs in some species which are well equipped to chase away food competitors. Acorn woodpeckers, where the members of a social group store thousands of acorns in one or two prepared trees, jointly defend the larders. Shrikes and birds of prey are morphologically well adapted to protect their larders from other species. Recovery of stored food. Careful hiding of food reduces the risk that

competitors will find it, but also makes recovery by the hoarder more difficult. In some species , this problem is solved by a remarkable memory: several hundred or even thousand storing sites spread over sometimes more than 10 ha are remembered fairly precisely for more than half a year by Thick-billed Nutcrackers and European Jays Garrulus glandarius. The jays use conspicuous objects such as sapling s and tree trunks as beacons in recovering food. There is strong evidence that the birds do not use smell, but rely on visual cues in recovering stored food. Nutcrackers and jays, like most birds, appear to have poor sense of smell . Hoarding in groups. Tits, Rook, Clark 's Nutcracker, Pinyon Jay Gymnorhinus cyanocephalus and several other species hoard in conspecific groups in 'communal areas' where the group members tolerate each other. Hoarding in such situations raises a special problem. Since harvesting and storing food requires time and energy , it has a certain cost which a group member might avoid by refraining from hoarding , yet exploiting the food stored by other group members. When stored food is easily available to each group member, as in the Acorn Woodpecker, such 'cheating' seems particularly likely . In this species all group members except yearlings hoard, but there is no quantitative study of the distribution of storing and consumption of the food among the different members. In group-living birds which scatterhoard and hide food , cheating may not be advantageous if the hoarder of an item is more likely than any other group member to recover it. This could come about either if individuals remember their own caching sites , or if individuals differ in preferred types of sites . Among group-living tits , both mechanisms may operate. Individual Mar sh Tits Parus palustris differ in their types of hoarding sites, and have a fairly precise memory of the storing places during at least 24 hours. Contrary to what has been suggested, stored food in many group-living species may not therefore be 'communal property' which all group members have equal chances to eat ; the hoarder of an item is often most likely to recover it. Therefore, KIN SELECTION is not necessar y for the evolution of hoarding in groups. After juvenile dispersal in late summer, groups of food-storing tits consist of genetically unrelated individuals. But kin selection has possibly been important in other hoarding, group-living birds , as it has apparently been for the evolution of advanced food-storing among bees and other hymenopterous insects . Evolution of food storing. Among species which do not hoard , a bird, after finding a food item , may move to eat it in a more convenient or protected place, for instance to reduce the risk of discovery by predators or competitors. Food-storing may have evolved from such transportation of food . Woodpeckers and nuthatches often fix their food in holes or bark crevices to make eating easier. Fixation of more food than is immediately needed should be a further easy step in evolution. Many predators may continue hunting even when they have just eaten and will not consume more food. 'Surplus killing ' is common among carnivorous mammals, and some birds of prey continue to hunt and store food after they are satiated. Coevolution of hoarders and food plants. There are several beautiful examples of mutualism and coadaptation between hoarding birds and their food plants. The latter offer the animal a rich food source, while the hoarder 'pays back' by dispersing the seeds (see SEED DISPER SAL). Since the hoarder does not recover all stored seeds, it helps propagate the plant . In some well developed hoarder-plant systems, the bird has evolved a specialized bill and an extensible oesophagus or sublingual pouch for efficient seed transport, and the plant has evolved seeds or fruits which are large, nutritious, easily available, protected against mould by a cover, and otherwise suitable for hoarding. Two examples are Clark's Nutcracker-Pinon Pine Pinus edulis and European Ja y-Pedunculate Oak Quercus robur. But the habits of hoarders are not always advantageous for their food plants; Acorn Woodpeckers and other melanerpine species seldom drop Pinon seeds or acorns, and store them in sites unsuitable for germination. These woodpeckers may therefore be 'parasites' on mutualistic systems developed between other hoarding birds and plants. M.A. Bossema, r. 1979. Jaysand oaks: an eco-ethologicalstudy ofa symbiosis. Behaviour 70: 1-117.

Cowie, R.J., Krebs, J.R. & Sherry, D.F. 1981. Food storing by marsh tits. Anim. Beh. 29: 1252-1259 . MacRoberts, M.H. & MacRoberts, B.R. 1976. Social organizationand behaviorof the acorn woodpecker in central coastal California. Ornithol. Monogr. 21. Roberts, R.C. 1979. The evolution of avian food-storing behavior. Amer. Natur. 114: 418-438.

Foot papillae and pads

Stacey, P.B. & Bock, C.E. 1978. Social plasticity in the acorn woodpecker. Science 202: 129S-1300. Swanberg, P.O. 1951. Food storage, territory and song in the Thick-billed Nutcracker. Proc. X Int. Orn. Congr., Uppsala: 545-554. Tomback, D.F. 1978. Foraging strategies of Clark's Nutcracker. Living Bird 16: 123-161. Vander Wall, S.B. & Balda, R.P. 1981. Ecology and evolution of food-storage behaviour in conifer-seed-caching Corvids. Z. Tierpsychol. 56: 217-242.

FOOD-WEB: see ECOLOGY. FOOL HEN: popular name for the Spruce Grouse Dendragapus canachiies (see GROUSE). FOOT: see under

LEG; SKELETON, POST-CRANIAL.

FOOTEDNESS: a physiological dominance of one foot over the other, comparable with right-handedness or left-handedness in human beings. There is some evidence of this in a few groups of birds. In 7,259 landings of 11 Domestic Pigeons Columbia livia, 7 used the right foot, 3 the left foot, and one showed no particular preference for either (Fisher 1957); biometric analysis revealed a slight departure from bilateral symmetry in the leg bones of the pigeon (McNeil and Martinez 1967). The right leg as a whole, and most of the right limb segments, are significantly longer than the left. In the Accipitriformes, Bond (1942) found that a young Goshawk Accipiter gentilis would sleep on both feet, but would hold its food with the left talon. Hosking (1943) describes the same behaviour for several species of hawks and owls. The parrots manifest a similar type of handedness. Of 20 birds belonging to 7 genera and 16 species observed using right or left foot to bring food to the beak (Friedmann and Davis 1938), the percentage of left-handedness exhibited by the birds as a whole was 72.2%; 3 individuals of Brotogeris jugularis were 1000/0 left-handed. Of the genus Amazona, 7 species showed 66.97% left-handedness, while the 10 individuals involved were 70.5% left-handed. In Amazona amazonica, which is 750/0 left-handed, McNeil and Martinez showed a significant predominance in the length of the left limb as a whole and in most of the left limb segments. A similar type of left-handedness was reported for the Carolina Parakeet Conuropsis carolinensis (Allen 1939). It may be concluded that many genera and species of Psittacidae are left-handed. However, observations on 56 individuals of Aratinga pertinax when bringing food to the beak (McNeil et a11971) showed that half the birds were left-handed and half were right-handed. A biometric analysis revealed a slight departure from bilateral symmetry in hindlimbs as a whole and hindlimb segments in close relationship with handedness (left and right). Among Passeriformes, the occurrence of foot preferences is not well documented. It has been reported (Dobie 1936, and others) that in the Crossbill Loxia curvirostra the use of a particular foot to hold a cone is correlated with the direction of crossing of the mandibles. If the lower mandible twists to the right, then the left foot is used and vice versa. When the cone is held with both feet, if the lower mandible twists to the right, the base of the cone lies under the left foot and its tip under the right foot and vice versa. Great Tits Parus major showed marked preferences, about half the birds being right- and half left-footed, when holding insect food (Vince 1964). The preferences were however more marked in some individuals than others and broke down in the more complex task of string-pulling. There is no evidence to show whether such foot preferences are individually acquired or not. A close relationship between skeletal bilateral asymmetry and footedness has been shown but the results do not demonstrate any causal relationship. McNeil and Martinez (1967) believe that bilateral symmetry in external organs (limbs and sense organs) may be interpreted as a locomotor adaptation in the sense that it would make it easier for an animal to reach its goal directly, while departures from bilateral symmetry may have other functions in, for example food handling or prey catching. R.McN. Allen, F.H. 1939. Left-handedness in the Carolina Parroquet, Auk 56: 476--477. Bond, R.M. 1942. Development of young Goshawks. Wilson Bull. 54: 81-88. Dobie, W.H. 1936. Crossbill's method of feeding. Br. Birds. 30: 43-44. Fisher, H.J. 1957. Footedness in domestic pigeons. Wilson Bull. 69: 170-178. Friedmann, H. & Davis, M. 1938. Left-handedness in parrots. Auk 55: 478-480. Hosking, E.J. 1943. Some observations on the Marsh Harrier. Br, Birds 37: 2-9. McNeil, R. & Martinez, M.A. 1967. Asymetrie bilaterale des os longs des membres

237

du pigeon Columbalivia et du perroquet Amazona amazonica. Rev. Can. Biol, 26: 273-386. McNeil, R., Rodriguez, S., Figuera, B. & D.M. 1971. Handedness in the Brown-throated Parakeet Aratinga pertinax in relation with skeletal asymmetry. Ibis 113: 494-499. Vince, M.A. 1964. Use of the feet in feeding by the Great Tit Parus major. Ibis 106: 50S-529.

FOOT-PADDLING: see FEEDING

HABITS.

FOOT PAPILLAE AND PADS: thickenings of plantar skin; pads are covered with papillae and are separated from other pads by furrows. In various birds pads and papillae, making contact with the substrate, show great variety in structure as adaptations to the way of living. The papillae are often called scales or reticulate scales. In embryonic studies they are called radially symmetrical scales in contrast to the overlapping scales of tarsometatarsus and toes. The morphology, histology, and function of papillae deviate from scales and justify the term papilla. Embryonic development. Pads, furrows, and papillae develop by three separate processes in the embryo (see Fig. 1). The furrows develop through a thickening of epidermal cells, followed by a folding; they appear during days 10-12 of the domestic chick's embryo development. Pads swell by cell proliferation in the deep dermis; the large pad in the centre of the foot appears on day 8 of the embryo, and the pads in the toes on days 10-12. The papillae develop through a condensation of dermal cells close to a thickening of epidermal cells; they appear on days 11-14. The embryonic development of papillae shows similarities to that of scales and feathers; factors in the dermis control the differentiation of the skin. Papillae. Tree-living birds often have papillae with the microscopic structure shown in Fig. 2. The primary dermal papilla is divided into several secondary dermal papillae. This implies an increased surface of

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238 Foot papillae and pads

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Ground-living birds such as waders, bustards, cranes, grouse and storks have a similar connection of papillae to a skin plate, although the surface of the papillae is flat. Parrots have separate papillae. Many papillae have Herbst sensory corpuscles in the dermis. The free papillae and the sensory corpuscles indicate a touch function of the papillae, comparable to the touch function of the epidermal ridges in primates. Birds-of-prey have separate or connected papillae. The stratum germinativum is often thin and the stratum corneum is thick, indicating a different condition of wear and renewal. Herbst sensory corpuscles are sparse and scattered in the dermis of owls Asio and buzzard Buteo. The Osprey Pandion and the fishing owls Ketupa and Scotopelia have pointed, spiny papillae adapted to grasping slippery fishes. Palearctic passerines wintering within the region have generally few and large papillae, whereas passerines of similar size wintering in tropical Africa have many and small papillae. The Redpoll Carduelis flammea and the Goldcrest Regulus regulus have exceptionally few papillae, but some of them are very large and the stratum corneum is thick. This reduces the area of contact with the substrate during cold winter conditions. Some birds wintering in temperate climates have a thicker stratum corneum in winter than in summer, an insulative acclimatization. Passerines living on the ground such as the Skylark Alauda arvensis also have few papillae. Pads. The pads are defined by the furrows: gaps between the papillae, which open and close when the digits are bent. Some furrows are developed in the early embryo and occur in every individual of the species; other furrows develop later in the embryo or early in the nestling, and they show individual variation in occurrence. The pads in the toes are anchored by connective tissue to the phalanges or to the joints and are therefore termed phalanx pads and joint pads. One pad in the central part of the foot is close to the trochleas of the tarsometatarsus: the central pad. Figure 3 shows the feet of 6 birds. The Grey Heron Ardea cinerea has small joint pads and long narrow phalanx pads. This pattern occurs in

----d sg

se

c Fig. 2. Diagrams of papilla in (a) a passerine, (b) a parrot, and (c) an owl. The skin consists of the dermis (d), which projects into the papilla with a primary dermal papilla (pdp) and several secondary dermal papillae (sdp). The epidermis has a basal cell layer (bc) where mitotic activity renews the epidermis, the cells moving through the stratum germinativum (sg) and the stratum corneum (sc) to be worn off at the surface. Many papillae in parrots have Herbst sensory corpuscles (He), Scales 0.1 mm.

contact between dermis and epidermis and space for a large number of basal epidermal cells, which divide and renew the epidermis. Papillary arteries and veins branch from a network of blood vessels in the dermis and continue as capillaries to the top of the secondary dermal papillae. Arteriovenous anastomoses occur at the base, regulating the blood flow to the papilla. There is obviously a heat exchange between arteries and veins, generating a temperature gradient in the papilla. The pads and papillae of tree-living birds are often subjected to strong external forces when the bird lands or grasps a branch. They are connected to each other by a thick layer of stratum corneum, forming a thick skin which covers the pad. This skin is flexible but only slightly stretchable. The distal end of the papillae in some birds projects and is pointed, suitable to penetrate roughnesses in the substrate.

Fig. 3. Pads in the feet of 3 ground-living birds (upper row) and 3 tree-living birds (lower row): (a) Grey Heron Ardea cinerea; (b) Ringed Plover Charadrius hiaticula; (c) Kori Bustard Choriotis kori; (d) Roller Coracias garrulus: (e) Redstart Phoenicurus phoenicurus; (f) Sparrowhawk Accipiter nisus. Each pad is represented by a line showing the margin of the pad. Black areas at the side of the digit show the position of joints. Scales lcm.

Fossil birds

many ground-living birds such as waders and gamebirds. Some of them, such as the Ringed Plover C haradrius hiaticula, walking mostly on hard substrates, have phalanx and joint paids about equal in size. This also occurs in the Little Bustard Otis tetrax. The great Kori Bustard Ardeotis kori has only 4 pads: one in the centre of the foot and one in each of the anterior toes, the latter being fusions of several pads. Similar fusions of pads occur in sandgrouse and in flightless birds such as the Ostrich Struthio camelus. Many ducks and gulls have joint pads and a central pad but lack furrows. The Eider Somateria mollissima has a large phalanx pad at the base of the second toe, obviously important in standing. The Scaup Aylhya marila and the divers have only a central pad and no sign of pads in the toes. The papillae and pads of the petrels are very similar to these groups. The Roller Coracias garrulus has phalanx and joint pads; some phalanx pads in the distal part of second and third toe are divided into 2 or 3 pads. Kingfishers and other birds with toes connected by skin have fewer pads due to fusions. Pigeons and doves have pads comparable to those in the Roller, but certain species have fewer pads. Passerines, e.g. the Redstart Phoenicurus phoenicurus, have a basic pattern of 12 phalanx pads and one central pad. The joint pads are reduced to folds, which have a few papillae or a smooth skin surface without any papillae. Certain joints may even lack folds. Woodpeckers and cuckoos have prominent phalanx pads and small folds at many joints. Many diurnal raptors have phalanx and joint pads, but not so many as in the Roller. The Sparrowhawk Accipiternisus has some projecting joint pads in the third and fourth toe adapted to penetrate the feathers of its prey. The owls have joint pads, but the furrows are unclear or absent. Pads and papillae are mostly characteristic of the species. In fragments of birds including the leg, e.g. from a raptor's prey, the species may sometimes be recognized by comparison with wet-prepared museum specimens. I. L. Lennerstedt, I. 1975. Pattern of pads and folds in the foot of European Oscines (Aves, Passeriformes). Zoo!' Scr. 4: 101-109. Lennerstedt, I. 1975. A functional study of papillae and pads in the foot of passerines, parrots, and owls. Zool, Scr. 4: 111-123. Lucas, A.M. & Stettenheim, P.R. 1972. Avian anatomy, integument. Parts I-II. Agricultural Handbook 362. U.S. Dep. Agr., Washington. Sawyer, R.H. 1979. Avian scale development: effects of the scaleless gene on morphogenesis and histogenesis. Develop. Biol. 68: 1-15. Vollmerhaus, B. & Hegner, D. 1963. Korrosionsanatomische Untersuchungen am Blutgefassystem des Huhnerfusses. Morph. [ahrb. 105: 139-184.

FOSSIL BIRDS: any members of the class Aves whose remains have been preserved in a palaeontological context. Fossil birds range in age from the Jurassic Period up to only several hundred years old and may be taken to include all avian remains that are not accompanied by written historical documentation. Bone, both mineralized and unmineralized, is the most common and the most important type of avian fossil, although feathers, feather impressions, eggshells, gizzard stones, footprints, and mummified skin and bare parts have also contributed to our knowledge of birds of the past. Chronological framework. A clear understanding of geological time and its associated biological events is essential to interpret the fossil record of birds. Recent years have witnessed great advances in geochronology and biochronology, especially through the application of radiometric and palaeomagnetic dating methods to many fossil localities. Figures 1 and 2 present a synthesis of much recent information on MILLIONS OF YEARS BEFORE PRESENT ERA 65

70

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FORAMEN: an aperture (plural 'foramina') in a bone or other bodily structure (see SKELETON, POST-CRANIAL). FOREHEAD: see TOPOGRAPHY.

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Growth

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263

Table of temperature regulation in recently-hatched young of various species when experimentally kept in ambient temperatures of 10 e for 20 minutes. (Data were estimatedfrom the graphicalpresentation of Koskimies, J. & Lahti, L. (1964 A uk 81: 0

281-307).)

Drop in body temp.,oC Goldeneye Bucephala clangula Mallard Anas platyrhynchos Teal Anas crecca Blackcock Tetrao tetrix Capercaillie Tetrao urogallus Lesser Black-backed Gull Larus fuscus Herring Gull Larus argentatus Pheasant Phasianus colchicus Black-headed Gull Larus ridibundus Willow Ptarmigan Lagopus lagopus Domestic Pigeon Columba livia

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Fig. 6. Cooling curves of nestling Ovenbirds Seiurus aurocapillus exposed to ambient temperatures (shown on each curve) outside the nest on various days following birth on 9 July, showing how nestlings progressively improve temperature regulation with age. (After Hann 1937).

generally a high intercept, but adults of the two groups have rather similar final energy densities. Fat deposits in nestlings are primarily around the abdomen, reflecting the absorption of the yolk sac lipids, but amongst older nestlings the other major depots-cervical and subscapular-are equally important. Calcium is probably the mineral component of growth that is of most importance to birds. In young thrushes calcium concentration (mg/IOOmg lean dry weight) more than trebles between hatching and fledging, its accumulation over this period being more or less sigmoid in time. This high intake of calcium (it has been estimated at 20-30 mg per gram of dietary protein) must underlie the frequently recorded habits of altricial species feeding their young fragments of shell and other sources of extraneous calcium. Development of thermoregulation. Body temperatures. Young nestlings are initially unable to regulate their body temperatures to a constant level and in the absence of parental brooding cool towards ambient temperatures (Fig. 6). Both nestling insulation and the abilities of the young birds to produce heat are involved here. Figure 6 shows that older nestlings were more able to resist heat loss than were younger birds and to do so more effectively at warmer temperatures than at colder. If such nestlings are tested experimentally at these temperatures for prolonged periods their abilities to maintain even this degree of temperature control are lost and they become torpid. Similar results are obtained when the nestlings are exposed to particularly low temperatures, so they are unable to compensate for the rate of heat loss from their bodies. Much of the variation in the timing of thermoregulation is associated with the specific growth rate of the nestling, with fast-growing species becoming thermally independent sooner than slow-growing species. But amongst species with a given growth rate, those with the longer nestling period attain thermoregulation somewhat later. Amongst precocial species the onset of thermoregulation is harder to define, given the independence of such young. However, there are a number of obvious gradients with ecological factors (Table). The diving ducks were the most resistant to cold stress, followed by dabbling ducks, then the gallinaceous species and semi-altricial gulls. This sequence basically reflects the normal exposure to cold. Amongst the auks young Guillemots show temperature control at 10-12°C from about 3 days of age and Puffins Fratercula arctica by fr.7 days of age. However, these are experimental findings and in the wild the chicks are in fact brooded at these temperatures until 5-6 days from hatching. Amongst young waders thermoregulatory abilities seem poorly developed, with various sandpiper chicks averaging 37.2°C when actively brooded but averaging 3° lower when actively feeding and becoming quite torpid when crouching in response to adult alarm calls (see also HEAT REGULATION).

Metabolic rate and body weight. Metabolic output of young birds is a power function of their body weight at any age but the exponent is greater than amongst adults. There are significant differences between passerines and non-passerines in the speed with which they reach adult levels of metabolic intensity, the latter achieving this level sooner. There is a similar difference in passerine embryos, their weight-specific metabolism averaging about one-quarter to one-third the levels shown by adults of the same weight, whilst a non-passerine's metabolic intensity is nearly one-half of the adult level. Body temperatures can be regulated either by controlling body conductance (the resistance offered by the body to the loss of heat produced internally) or by regulating heat production. Because their plumage is initially inadequate, young birds at first thermoregulate by producing excessive amounts of heat, only later reducing this rate of heat production with improvements in their body conductance. Figure 7 shows the pattern of oxygen production in Blue Tit Parus caeruleus nestlings of different ages. In the youngest birds oxygen consumption is directly proportional to the prevailing temperatures, whilst in the oldest young the pattern of respiration approaches that of 8

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Fig. 7. Age changes in the metabolic rate of Blue Tit Parus caeruleus nestlings exposed to various ambient temperatures, showing the development of the nestlings' ability to produce heat. (After O'Connor, 1984).

264 Growth

the adult, with the inverse relationship between temperature and metabolic output. At intermediate ages the situation is more complex, the birds elevating their heat production in response to lower temperatures over a range of the warmer ambients but losing heat too rapidly and becoming torpid at the lower temperatures. These patterns of thermoregulatory development in nestlings are associated with concomitant changes in the physiology and morphology of the young bird. As it increases in size its surface to volume ratio decreases, reducing the rate at which heat is lost from the body. Secondly, air sacs-functional in adult respiration-do not develop fully until some days into the nestling period and thus contribute increasingly to the metabolism of oxygen later. A third change involves the circulatory system, for the heart increases slightly in relative size and there are major increases in the erythrocyte concentration of the blood and in haemoglobin concentration. These changes contribute to the ability of the circulatory system to transport oxygen to the lungs. Carbohydrates form the main energy reserve for short-term responses to cold stress and their concentration in the body increases with age. Chemical thermoregulation by the young is also promoted (at least in domestic fowl) by injection with such hormones as noradrenalin, and thyroid hormones also contribute to cold stress responses. Thyroid activity peaks in altricial nestlings a day or so before the onset of full homeothermy. Finally, development in heat production by shivering under nervous system control contributes to heat production, appearing 3 or 4 days into the nestling period but increasing efficiency of heat production for sometime thereafter. In precocial species very similar processes are apparent, though some of the responses, e.g., muscle tremor, begin shortly before the embryos hatch. Another way in which young birds can regulate their heat loss to the environment operates by way of a lower body temperature than is shown by the adult bird. By doing this, the thermal gradient between bird and environment is reduced, with consequential reduction in the rate of cooling. Nestlings of several species have been shown to increase their equilibrium body temperature with age in this fashion. Evaporative cooling and hyperthermia are the main defences available to nestlings subjected to heat stress. Hyperthermia operates to cool the nestling by elevating its body temperature above the ambient temperature, thus creating a temporary gradient down which heat can flow from the nestling to the now cooler environment. Conversely, in extremely hot conditions elevation of temperature reduces the rate at which further heat 30 House Sparrow

25

-~

GEL

20

.s

-0 u

DEB = 1.353 WO. 8 14 (Kendeigh et al 1977), showing a faster increase with weight (exponent = 0.814) than would be the case amongst adults (exponent = 0.67). The young thus expend more energy per day than would an adult of the same weight, probably the result of the inferior insulation afforded by feathers whose shafts are vascularized until late in development. The different life-styles of altricial and precocial species result, however, in different proportions of their energy intake being devoted to maintenance costs. Despite these differences, though, there are no major differences in the proportion of energy consumed which is eventually converted into growth (see also ENERGETICS). R.] .O'C. Kendeigh, S.C., Dolnik, V.R. & Gavrilov, V.M. 1977. Avian energetics. In Pinowski, J. & Kendeigh, S.C. (eds.). Granivorous Birds in Ecosystems. Cambridge, Mass. O'Connor, R.J. 1984. Growth and Development of Birds. Chichester. Ricklefs, R.E. 1973. Patterns of growth in birds. II. Growth rate and mode of development. Ibis 115: 177-201. Ricklefs, R.E. 1983. Avian postnatal development. Pp. 5-83. In Farner, D.S., King, J.R. & Parkes, K.C. (eds.). Avian Biology. VII. New York. Skutch, A.F. 1976. Parent Birds and their Young. Austin.

GRUES; GRUIDAE: see

>a ~ 15 ~

.::J:.

can flow into the nestling. Thermal ability of this type is more marked in very young birds than in older birds: 3-day-old House Wren Troglodytes aedon nestlings can safely withstand temperatures as high as 45.5°C but nestlings 11-16 days old can withstand high temperatures only to 42.1°C. Evaporative cooling also serves nestlings faced with heat stress. Each millilitre of water evaporated carries with it 580 cal of latent heat. Consequently a nestling can work, e.g., by panting, to evaporate water and thereby lose more heat through evaporation than is produced by the extra effort of panting. Even quite young nestlings are able to pant when exposed to heat, and in tropical species regularly exposed to high temperatures this cooling can be enhanced by gular flutter. Energetics of growth. The pattern of energy used during growth differs between altricial and precocial species (Fig. 8). Gross energy intake is higher in altricial species than in precocial species. In the House Sparrow the amount of energy spent on basic existence and maintenance costs rises to nearly twice the adult level before declining, thus implying that the young nestling is less efficient than an adult in its use of energy for maintenance costs. Precocial and altricial young alike have higher gross energy intakes than adults, but the excess is larger and increases virtually until fledging in precocial species. The energy expended in this way comes from the metabolization of food ingested and in the altricial House Sparrow food assimilation efficiency is at first below adult levels but reaches these after 4-5 days. In the precocial Black-bellied Tree Duck Dendrocygna autumnalis this efficiency varies little during the first part of postnatal life. The daily energy requirements (Kcal/bird/ day) of young birds increases with body weight according to the equation

10

5

O~-----.~--.......------r-----.---.......------r-----.""'1~

o

2

6

8

10

12

1L.

Ad

Age (days)

Fig. 8. Changes in energy budgets of House Sparrow Passer domestic us nestlings with age, showing changes in gross energy intake (GEl), in daily energy budget after assimilation (DEB), and in existence energy (EM). (From Myrcha, Pinowski & Tomek, 1972. In Kendeigh & Pinowski, (eds). Productivity, Population Dynamics and Systematics of Granivorous Birds. (PWN) Warsaw).

GRUIFORMES; CRANE.

GRUIFORMES: an order comprising 7 suborders: Turnices, Grues, Heliornithes, Rhynocheti, Eurypygae, Cariamae, Otides; 11 families: Turnicidae (BUTTONQUAIL), Pedionomidae (PLAINS-WANDERER), Rallidae (RAIL), Aramidae (LIMPKIN), Psophiidae (TRUMPETER), Gruidae (CRANE), Heliornithidae (FINFOOT), Rhynochetidae (KAGU), Eurypygidae (SUNBITTERN), Cariamidae (SERIEMA), Otididae (BUSTARD) . Of the assemblage as a whole, it may be said that it consists essentially of ground-living birds-ground-feeding and mainly ground-nesting; many of them seldom fly, and a few never. The Heliornithidae and some of the Rallidae, e.g., coots (Fulicinae) and gallinules of various genera, are adapted to an aquatic life; many others frequent marshes or the margins of water. Of the families, the Rallidae include a large number of genera; 4 of the families are monotypic. Only the Gruidae and Rallidae are cosmopolitan, although the Turnicidae and Otididae are widespread in the Old World; the others have restricted distributions. GUACHARO: alternative name of Steatornis caripensis (see

OILBIRD).

GUAIABERO: substantive name of the Philippine species Bolbopsiuacus lunulatus (Psittacinae) (see PARROT). GUAN: substantive name of some species of Cracidae (see CURASSOW).

Guano, cave

GUANO: the excreta of seabirds, dried to a crusty, rock-like or rough powdery consistency. Huanu is an Incan (Quechuan) word and its derivative is now widely used and applied, also, to other animal excreta such as 'bat guano' from caves (see also GUANO, CAVE). Guano, the Inca's 'secret' (see The Royal Commentaries of the Incas (1609) by Garcilaso de la Vega), introduced to the modern world by Alexander von Humboldt, has been extensively used as organic fertilizer, that from Peru giving rise to scandalous 19th-century commercial and political machinations. As Murphy wrote: 'Small though the Chinchas (Peruvian guano islands) are, their name is known in the farthest seaports of the world and their share in making fortunes and abetting calamities, in debauching men and demoralizing administrations, and in serving as the inanimate cause of greed, cruelty, extravagance, economic ruin and wars has given them a historic place quite out of proportion to their size.' Guano is formed over many years where huge and densely packed colonies of seabirds breed on arid, flattish islands. Guanay Cormorants Phalacrocorax bougainvillei nest at a density of 3 pairs per m 2 whilst Cape Gannets Sula capensis have been recorded at 6.8 nests per m 2 though 3 or 4 is more usual. Many guano islands at times hold more than a million birds and some hold several millions (Central Chincha, maximum estimate 6 million). Necessarily, these colonies are situated in or near to enormously productive upwelling areas which support inconceivable numbers of fish (the catch of anchovies by Peru, 1969/70, contained more than 10 trillion). The Peruvian guano islands adjacent to the Humboldt current, those off SW Africa in the region of the Benguela and the seabird islands in the Gulf of California in the region of the California current are the best examples. Global wind and current systems are such that the cold and nutrient-laden upwellings are on the western seaboards of land masses (North America, South America, South Africa, India, Australia). These areas are also dry, the cold upwelling accentuating aridity by delivering cold moist air to a hot land mass, thus preventing precipitation (the moisture is retained in the warm air as mist). Pelecaniforms, especially cormorants (Phalacrocorax bougainvillei in Peru; P. capensis in South Africa), sulids (Sula variegata and marginally S. nebouxii in Peru, S. capensis in South Africa) and pelicans (Pelecanus occidentalis thagus) produce most guano, partly because they are most numerous and also because some species tend to withhold their excreta until they are at the breeding site, where they deposit it to form the nest. Cape Gannets (average nest weight 1,770 gm) have been shown to reproduce more successfully where ample guano was artificially provided than in otherwise comparable areas. Guano can be used as nest material only in a dry climate; otherwise it would become sticky and coat the egg and chick. A Guanay Cormorant deposits on land, throughout its life, a minimum dry weight of 1kg of guano per month. In addition to the 3 main guano-producing species, penguins (Peruvian Penguin Spheniscus humboldti in Peru and Jackass Spheniscus demersus in South Africa) and diving petrels (Pelecanoides garnotii in Peru) have been significant contributors, whilst the Gulf of California and islands off Mexico were seriously investigated as the potential basis for a guano industry, to which the Blue-footed Booby Sula nebouxii would have been the main contributor. Seabird excreta leached by moisture lose nitrogen and leave calcium phosphate minerals, called phosphatic guano. This is less nutritious to plants than the original high-grade nitrogenous guano. The calcium phosphate from the Indian Ocean Christmas Island (apatite ore for conversion into superphosphate fertilizer in Australia and New Zealand) is said to be modified guano, but if this is so, vast changes in topography, climate and seabird population have occurred since its deposition. In some parts of the world, low-grade 'guano' is collected, consisting of annual increments of excreta scraped up together with much substrate and nest material. Peruvian guano contains approximately 210/0 water, 53°/0 organic material capable of being burnt off, 1.70/0 insoluble materials (silicon dioxide, etc.), 3.5°/0 sodium oxide, 2.5°/0 potassium oxide, between 3 and 11°/0 calcium oxide, 0.5°/0 magnesium oxide, between 7 and 11°10 phosphorus pentoxide, 2°1o chlorine, 0.3°/0 sulphur trioxide and 0.9°/0 of a complex of aluminium and ferric phosphate (Hutchinson 1950). Although the guano caps of the islands were up to 90 m thick, this represented the deposits of no more than 2-3,000 years. However, C l 4 dating has indicated a much greater age for at least one deposit. Earlier guano caps may have been washed away by periods (measured in scores or hundreds of years) during which a wetter climate prevailed. Indeed, the distribution of guano-birds has changed within (relatively) recent

265

times. There are extensive and old (fossil) guano deposits in Peru/Chile well south of the present concentrations of guano birds and the 'modern' deposits of guano. This southern area evidently became uninhabitable whilst the northern one became attractive, having presumably been climatically unsuitable previously. The factors which led to the decline of guano birds in the south may have been oceanographic (change in currents and distribution of food fish and in sea level, submerging many islands off Chile). Between 1848 and 1875 more than 20 million tons of guano were shipped from Peru, mainly to Europe, USA and Britain. This was the era of total exploitation, both of the resource (including the seabirds) and the labour force. In 1909, the Guano Administration instituted protection for guano birds, the single most effective measure being the stationing of officialwardens at the main breeding stations to control human and other animal predators (foxes, gulls, Condors Vultur gryphus and Turkey Vultures Cathartes aura). Since 1945 extra nesting areas have been provided on Peruvian coastal headlands. Peninsulas have been isolated by high concrete walls, nesting areas enlarged and sites created. Up until 1956 these measures dramatically increased the mainland population and in 1962 headlands held some 4,500,000 guano birds. Other regulations, though rarely enforced, oblige boats to remain at least 3 km away from the islands holding breeding colonies, fishing boats to refrain from operations within a 5-km belt around all stations (8 km around some) and planes to fly over stations at a height no lower than 500 m. Harvesting of guano takes place every second or third year on a rotating basis; the maximum yield per year is in the region of 300,000 tons. Harvesting inevitably disrupts breeding cycles and may be partly responsible for the considerable movements of birds between nesting islands, although shifts in the distribution of anchovies may also be involved. The populations of Peruvian guano birds (mainly Phalacrocorax bougainvillei, Sula variegata and Pelecanus thagus), and also the proportions of each, fluctuate massively. Little can be inferred about changes prior to the 20th century though Vogt (1942) suggested that there had been a massive decline due to climatic changes and/or disease. However, this century the population has fluctuated between less than 3 and more than 20 millions of individuals. When estimated from the amount of guano deposited (a surprisingly accurate method), the highest figure is 28 million. The population crashes periodically. The cold upwelling fails, anchovies Anchoveta engraulis avoid the warm surface layers and become inaccessible and guano birds starve en masse. Until recently recovery was rapid but overfishing by the Peruvians, for example an officialcatch of 11 million metric tons in 1969/70, largely for the manufacture of fish meal, has apparently reduced stocks and/or altered the age composition of the anchovy population. Presumably as a result of this, recovery from the most recent crashes (1965, 1972/3, and 1983/4) has been greatly retarded. In addition, in the 1960s, many thousands of breeding guano birds were killed by fishermen. At the present time, after a period during which anchovy stocks remained low, some recovery in them and the seafowl has taken place, the boobies having fared better than the cormorants and pelicans. In South Africa declining catches by fishermen has led, as in Peru, to requests for an official policy of killing off seabirds. Apart from the fact that the seabirds catch fish and interfere with the nets, it has been argued that man can convert fish into meal more efficiently (at 5: 1) than birds can convert it into guano (at 9.7: 1). But birds not only produce a better and cheaper product, they also remain in a stable relationship with their ecosystem. Man should learn to do the same. And a colony of guano birds is more beautiful than a stinking fishmeal factory. (R.C.M.) J.B.N. Hutchinson, G.E. 1950. Survey of contemporary knowledge of biogeochemistry. 3. The biogeochemistry of vertebrate excretion. Bull. Amer. Mus. Nat. Hist. 96: i-xviii, 1-544. Levin, j.V, 1960. The Export Economies: Peru in the Guano Age. Cambridge, Mass. Murphy, R.C. 1936. Oceanic Birds of South America. 2 vols. New York. Nelson, j.B. 1978. The Sulidae: Gannets and Boobies. Oxford. Paulick, E.j. 1970. Anchovies, birds and fishermen in the Peru Current. In Murdock, W.W. (ed.). Environment, Resource, Pollution and Society. Stamford. Vogt, W. 1942. Aves guaneras. Bol. Compo Admin. Guano 18: 3-132.

GUANO, CAVE: of avian origin, occurs in limestone caves in South.. east Asia occupied by swiftlets of the genera Collocalia and Aerodramus

266 Guiding line

(see EDIBLE NESTS). Droppings gathering below nest sites are quickly reduced, by a rich fauna of coprophagic arthropods, to a dark brown material with the consistency of damp sawdust. This is composed chiefly of organic matter and normally contains 6-10% phosphate and 3-9% nitrogen. In undisturbed dry caves this fresh guano is underlain by deposits, which can be several metres thick, of a compact, powdery 'fossil' guano containing 10-45% phosphate by weight (characteristically as collophanite, 3CaOPzOsHzO), often with other minerals, and 10-300/0 organic matter. Despite low nitrogen and unpredictable phosphate yield, both types of guano are locally popular as fertilizer. Most accessible caves in the region have already been stripped down to bedrock. C.

GUIDING LINE: less appropriate alternative term (translating 'Leitlinie') for

LEADING LINE

(see

MIGRATION).

GUILLEMOT: substantive name of Uria spp. ('murre' in American usage) and Cepphus spp. (also called 'tystie')---see AUK. Although origi-

nally a French word, it is now pronounced in English with the final syllable as in 'hot'.

GUINEAFOWL: substantive name of species of Numidinae (Galliformes, family Phasianidae); a group of sedentary terrestrial gamebirds. There are 6-7 species, assigned to 4 genera, 2 of which are superspecies. Characteristics. The major external feature of guineafowl is a largely unfeathered head and neck, which is adorned with cartilaginous gape wattles and areas of richly pigmented, sometimes folded skin. Some species have a well-developed casque or feathered crest surmounting the crown, and cartilaginous bristles or warts at the cere. These structures provide some of the most useful specific and subspecific taxonomic characters, and presumably play important roles in species and individual recognition, and possibly in thermoregulation. Patterns of geographic variation in these and other morphological features of guineafowl correlate well with, and may be adaptively related to, variation in the thermal and moisture environments. All guineafowl species show little sexual dimorphism, with males averaging slightly larger than females, range 45-60 ern. Size among the various species appears to be inversely related to the density of the vegetation in which they live. The smallest guineafowl are Agelastes spp. (mean wing length 20.4 em), which inhabit dense, virgin, tropical rain-forest. Among the guineafowl with feathery crests (Guttera spp.) G. plumifera, which inhabits dense forest, is smaller (mean wing length 22.5 em) than G. pucherani(range of mean wing length among subspecies 24.5-26.0 em), which lives in secondary and riparian forest, and along the forest edge. Larger still is the Helmeted Guineafowl Numida meleagris (range of mean wing length among subspecies 25-28 em), which lives in relatively open savanna vegetation and mixed savanna-bush. The Vulturine Guineafowl Aeryllium uulturinum is the largest of the guineafowl (mean wing length 29.5 em), and frequents the semi-desert steppe of the Horn of Africa. Distribution and habitat. The ancestral guineafowl is thought to have arisen from an Asian, savanna-living, francolin-like phasianid which colonized Africa during the mid to late Miocene, and radiated into terrestrial biotopes which were relatively unexploited. With the exception of an isolated population in Morocco, guineafowl now occur naturally only in sub-Saharan Africa. Distribution patterns of species and subspecies correlate well with the present-day distribution of vegetation, so that nearly every African biome and biotope has an associated guineafowl species or subspecies. However, guineafowl evolution at all taxonomic levels has been influenced by past changes in the distribution of forest, savanna and desert during geological time (see AFROTROPICAL REGION). One species, Numida meleagris, has been domesticated (probably several times independently), and/or captured and introduced widely throughout the world (see DOMESTICATION). This accounts for its presence in south-western Arabia, the Malagasy Republic and on offshore African islands. Food. They consume varying amounts of grit, and appear to be opportunistic omnivores, probably favouring insects when they are abundant. The bill of the Helmeted Guineafowl N umida meleagris is arched, and therefore well-suited to digging for underground bulbs, which are a favoured food item during dry periods and may be an important supplementary source of water. Social behaviour. With the exception of Agelastes spp., which appear to associate in small (family?) parties, all guineafowl species are highly

Helmeted Guineafowl Numida meleagris. (M.W.).

gregarious in the non-breeding season, and flocks of 50 birds or more are not uncommon sightings, All species roost in trees at night. At least 3 species (N. meleagris, G. pucherani and A. vulturinum) exhibit courtship feeding, and this behaviour is highly ritualized in A. vulturinum. These 3 species are monogamous in their breeding habits, although males may attempt to copulate with unattended females. Voice. As with size, the pitch of the rattling alarm calls given by guineafowl species is inversely related to habitat vegetation density. Thus the desert-living Aeryllium has the highest pitched, while Guuera spp. and Agelastes spp. have the lowest-pitched calls. Numida meleagris and Aeryllium vulturinum females, especially when separated from their mates during the breeding season, emit a characteristic two-noted buck-wheat call, to which their cocks respond antiphonally with a single note. Breeding. The nests of Agelastes spp. have not been described, but those of all other guineafowl are well-concealed shallow scrapes in the ground, which may be thinly lined with grass. The eggs of all species are pitted, creamy or buff in colour, remarkably thick shelled, blunt at one end and pointed at the other. Nests with 12 or more eggs are not uncommon. Sometimes several hens may lay in the same nest. The incubation period for the various species ranges from 23 days (for Guttera spp. and Aeryllium) to 27-28 days (for Numida). At 15-20 days old, Numida chicks can fly up to roosts 2 m above ground. Specific distribution. The most widely distributed and well-studied member of the family is the Helmeted Guineafowl Numida meleagris. This open-country, polytypic species has a virtually unfeathered head and neck, with the exception of the hindneck, which is covered by a concentration of short, downy, or long, hair-like feathers. The bill is heavy, a bony helmet (see CASQUE) with a horny sheath surmounts the crown, and a pair of long wattles hangs from the gape. The nostrils are exposed, and are rimmed with cartilaginous bristles or warts in subspecies which live in hot, arid biotopes. The blood vessels which supply the wattles, cere and upper hindneck are finally interwoven into retia, which may promote counter-current heat exchange, and thereby assist in the regulation of brain temperature through convective cooling of warm arterial blood coming from the heart. The iris of the chick is grey, but changes to brown by the age of 20 weeks. The tarsus is unspurred, and the legs are long and powerful, as befits a species which relies on running as its primary means of escape, and on scratching in the soil for much of its food. The ground colour of the plumage is black, with white spots intermeshed with a network of similarly-coloured vermiculation. The spots on the outer margins of the secondaries merge to form bars

(perpendicular to the rachis), which also have intervening vermiculation. The degree of vermiculation is most intense in subspecies which live in hot and arid biotopes, and may afford some degree of camouflage. There are 9 well-marked subspecies of N. meleagris, which fall into 3 groups: the West African, East African and Central-Southern African subspecies groups. These groups are separated by relatively narrow zones of intergradation, and hence have been regarded as semispecies. The West African subspecies group (N. m. galeata and N. m. sabyi) consists of

Guira

small- to medium-sized birds, with very short helmets (i.e., less than 1em tall), a naked cere, a grey to blue-grey mantle, rounded red wattles, very pale blue facial skin, and long hair-like feathers confined to the mid-dorsal line of the hindneck. Since N. m. sabyi, the isolated Moroccan subspecies, differs relatively little from N. m. galeata, the hundreds of kilometres of desert which presently separate the 2 subspecies are likely to be a relatively recent development on a geological time scale. The domesticated guineafowl is derived from N. m. galeata, and artificial selection has significantly modified its external morphology. Since domesticated guineafowl have been bred to be broilers, they are 20-25% heavier than their wild counterparts, which weigh about 1,300 g. They have thicker tarsi, which are orange and not black as in wild stock. The colour of the face, and that of the plumage of some breeds, is entirely white, and the wattles and helmet are 30-500/0 larger. There are no qualitative differences in displays, social and maintenance behaviour between wild and domesticated guineafowl. Even wild populations of this species can be more or less commensals of man, since the distribution and numbers of Helmeted Guineafowl have increased markedly when critical resources, e.g., water (bore holes and dams), roosts (telephone poles, exotic trees), and food (maize, wheat, lucerne, etc.) have been provided. The East African subspecies group (N. m. meleagris and N. m. somaliensis) are medium-sized guineafowl (mean wing length 26.5 em) with short helmets (mean height 1.2 ern), a cere with long bristles (up to 2.5 ern), a finely barred mantle, rounded blue (or with small red tips) wattles, cobalt blue facial skin, and a blanket of short downy feathers covering the hindneck. The Central-Southern African subspecies group (N. m. reichenowi, N. m. mitrata, N. m. marungensis, N. m. papillose, and N. m. coronata) consists of relatively large birds, with tall helmets (i.e., greater than 1.8 ern), a naked cere (except N. m. papillosa which has its cere rimmed by warts), a finely barred mantle, triangular-shaped blue wattles with red tips (except N. m. reichenowi which has rounded red wattles), cobalt blue facial skin, and varying amounts of long hair-like feathers confined to the mid-dorsal line of the hindneck. Although N. meleagris is virtually sexually monomorphic, the sex of live birds can be determined accurately by cloacal examination, and through study of individual behaviour. During the breeding season, males develop a cloacal protuberance, which is easily discovered by gently everting the cloaca. Males, again mainly during the breeding season, display laterally to each other, and to hens, in a 'hump-backed' posture (i.e., with the wings raised and laterally compressed against their bodies), and run on the tips of their toes. In this 'hump-backed' posture all important taxonomic characters of this species are displayed to their fullest. Closely allied to Numida is the Vulturine Guineafowl Acryllium vulturinum. In captivity the 2 species will hybridize to produce sterile offspring. However, encounters between these 2 guineafowl in the wild are rare, since they segregate according to habitat where they are sympatric. The bare skin of the head and neck of Acryllium is blue-grey, and the only plumage thereon is a band of short, downy chestnut feathers which stretches across the occiput from ear to ear. The wattles are rudimentary, and the iris a brilliant crimson. The most striking field characters for this species are well-developed hackles, and a pair of long central tail feathers. The former consist of long, narrow, pointed feathers striped longitudinally with black and white, and margined with cobalt blue. The breast and abdomen are also extensively covered by cobalt blue plumage. The remainder of the plumage resembles that of Numida except that the outer margins of the secondaries are lilac, and the inter-spot vermiculation is much denser. The only external feature which shows obvious inter-individual variation is the tarsal adornment, which is a series of degenerate, rounded spurs or 'bumps'. No two individuals have both the same number (up to 6) and size of 'bumps', and there is even variation in 'bump' arrangement between legs. As with important characters in Numida, this species' characteristic features are displayed to their fullest in aggressive and courtship postures. The first guineafowl encountered as one enters forest biome is the Crested Guineafowl Gutterapucherani. Most taxonomic treatments recognize 2 species of these 'forest-edge' birds, but breeding experiments with captive individuals have demonstrated complete interfertility between

'species', and morphological intermediates have been identified among museum specimens collected in zones of contact. Nevertheless, all subspecies attributed to G. pucherani are much more well-marked than are those for N. meleagris, which supports the idea that forest-dwelling

267

guineafowl have been more effectively isolated in refugia during the geological past than have savanna species. The body plumage of G. pucherani is similar to that of N umida and Acryllium except that the spots are tinged with blue, and there is no vermiculation between them. The outer margin of the secondaries is white, and the tarsus is unspurred. The crown is surmounted by a crest of curly, downy feathers; gape wattles are rudimentary; there is a well-developed fold of skin at the occiput and, in all but one subspecies, at the base of the neck; and the skin of most of the head and neck is dull blue-grey. A striking feature of the internal anatomy of this species is the hollow furcula of the clavicle through which passes the trachea. This feature may act as a resonant organ which allows the broadcasting of calls over relatively long distances. The 5 subspecies attributed to G. pucherani can be divided into 3 groups: the West-Central, East and Southern African subspecies groups. These groups can be distinguished through differences in the morphology of the head, neck and mantle. Subspecies of the West-Central African group (G. p. verreauxi and G. p. sclateri) have red throats and brown irides. Those of the Southern African group (G. p. edouardi and G. p. barbata) have dull blue-grey throats and red irides. The Kenyan Crested Guineafowl G. p. pucherani has a red throat and red irides, and differs further from other subspecies in having virtually no black feathers in the mantle (all other subspecies have a distinct black 'collar'), and a ring of red skin around the eye. Moving deeper into forest biome, the next guineafowl which may be encountered is the Plumed Guineafowl Guttera plumifera. This species and G. pucheraniform a superspecies. The body plumage of G. plumifera is similar to that of G. pucherani, except that there is little or no tinge of blue to the spots, and the entire mantle is spotted (i.e., lacks a 'collar' of black feathers). Other characteristic features of G. plumifera are: a tall crest of straight bristly feathers, brown eyes, long gape wattles, and a rudimentary occipital skin fold. Like G. pucherani, G. plumifera has a hollow furcula, but it is much less well-developed. Although the Congo forest (to which this species is confined) stretches relatively uninterrupted from the Atlantic coast to Uganda, there are 2 subspecies of G. plumifera. One subspecies (G. p. plumifera) is confined to the western reaches, the other (G. p. schubotzi) to the eastern portion of the forest. The major difference between the 2 subspecies is that G. p. schubotzi has patches of orange-yellow skin at the base of the nape and just anterior to the ear, while the head of G. p. plumifera is entirely dull blue-grey. The fact that this relatively uninterrupted forest can harbour more than one subspecies of forest-dwelling bird suggests that it was formerly fragmented into island-like refugia. Deeper still in virgin tropical rain-forest live the Turkey Guineafowl Agelastes meleagrides and the Black Guineafowl A. niger. There is only fragmentary or anecdotal information on the natural history of these forest guineafowl, and this has already been summarized above. These species differ conspicuously from other guineafowl in having a wholly unspotted body plumage. That of A. niger is uniformly blackish-brown, and that of A. meleagrides blackish-brown with fine grey vermiculation. The bare skin of the heads of both species is red, brighter in A. meleagrides. The head of A. meleagrides is unfeathered, and that of A. niger is surmounted by a crest of short feathers which extends from the base of the bill to the occiput. The mantle and breast of A. meleagrides are snowy white. Both species have brown irides and well-developed spurs on their tarsi. T.M.C. Ghigi, A. 1936. Galline di Faraone e Tacchini. Milano. Skead, C.]. 1962. A study of the Crowned Guineafowl Numida meleagns coronata Gurney. Ostrich 33: 51-65. Crowe, T.M. 1978. The evolution of guineafowl (Galliformes, Phasianidae, Numidinae) Taxonomy, phylogeny, speciation and biogeography. Ann. S. Afr. Mus. 76: 43-136. Crowe, T.M. & Snow, D.W. 1978. Numididae. In: Snow, D.W. (ed.). An Atlas of Speciation in African Non-passerine Birds. London. Crowe, T.M. & Crowe, A.A. 1979. Anatomy of the vascular system of the head and neck of the Helmeted Guineafowl Numida meleagris. J. Zool. Lond, 188: 221-233. Crowe, T.M. 1979. Adaptive morphological variation in Helmeted Guineafowl Numida meleagris and Crested Guinea-fowl Guttera pucherani. Ibis 121: 313-320. Crowe, T.M. & Withers, P.C. 1979. Brain temperature regulation in Helmeted Guineafowl. S. Afr. J. Sci. 75: 362-365.

GUIRA: Guira guira (see

CUCKOO).

268 Gular

GULAR: pertaining to the throat (see

TOPOGRAPHY).

GULAR FLUTTER: rapid oscillation of the thin floor of the mouth and upper throat (see HEAT REGULATION). GULL: substantive name of nearly all the species of the family Laridae (Charadriiformes, suborder Lari); in the plural, general term for the family. The other families of the suborder are the Sternidae (see TERN), Rynchopidae (see SKIMMER), and Stercorariidae (see SKUA). Characteristics. All species are medium to large (length 31-76 em) and have relatively long and narrow wings (span 64-165 em), with 10 functional primaries and one vestigial. The tail of 12 rectrices is usually almost square and of moderate length, generally 35-45% of the length of the closed wing. The bill is usually stout, sometimes slightly hooked, with a tapering nail, and a marked gonydeal angle. The tarsus is rather long and slender, the 3 front toes webbed, the hind toe very small or in a few species vestigial. The plumage of adults is basically white and grey. Head, underparts, rump, tail and underwings are white, sometimes washed grey to a variable degree, the head often covered for part of the year by a dark brown or black hood, leaving contrasting white marks above and below the eye, the tail adorned in a few species by a subterminal black band. Mantle and upper wing-coverts are grey, white in one species, black in a few. The tips of the primaries are usually patterned with black or black and white. Irides are usually brownishblack, sometimes white or pale yellow. The fleshy eye-ring is usually red or deep red tending to black, but yellow or purple in a few species. The bill is usually red, reddish-black or black, sometimes yellow with black or red distal marks or entirely yellow. Legs and feet are red to black, but yellow, bluish, greenish or flesh-coloured in a few groups of species. Adults have an annual complete moult, starting during or immediately after the breeding season, but, in a few species, after the autumn migration, and in the Ivory Gull Pagophila eburnea before the breeding season. A second moult, not involving, except in a very few species, the wings and tail, takes place before the breeding season. Breeding and non-breeding plumages differ in most species. Downy chicks are usually grey or buff, variously patterned with dark brown stripes and spots. Juveniles of almost all species are brown and buff with strongly patterned mantle and upper wing-coverts, dark remiges and rectrices. This plumage is replaced after a few weeks to a few months by a usually distinct first-winter dress. Adult plumage is acquired after as long as 4 or more years in some large species, through a succession of plumage stages reached by moults which generally take place earlier in the year than those of adults. Systematics. The morphological uniformity of the family has made the construction of phylogenies difficult. The principal revisions are those of Dwight (1925), based entirely on structure and plumage, and Moynihan (1959), based partly on behaviour. The present arrangement is derived from these but more recent information on behaviour, morphology and distribution is taken into account. Pelagic gulls. A small number of species, pelagic or semi-pelagic when not breeding, differs sharply from the core of typical gulls in voice, behaviour, proportions, tail-shape (either forked or wedge-shaped) and several adult and juvenile plumage characters. When hooded, they lack the white eye marks characteristic of gulls. Many of their characters are primitive within larids and they probably represent early offshoots near the common ancestors of typical gulls and terns. Their originality is best expressed by placing them in several small genera. The Swallow-tailed Gull Creagrus furcatus is a large species with long forked tail, slaty breeding hood and prominent wing pattern. Three small species, Sabine's Gull Xema sabini, Ross's Gull X. rosea and the Little Gull X. minuta have similar juvenile plumage. X. sabini and X. minuta have dark breeding hoods, without white eye marks, while X. sabini and X. rosea share unique black neck rings, bordering the slaty hood in sabini. The 2 kittiwakes, Black-legged Rissa tridactyla and Red-legged R. brevirostris, have juvenile plumages, which are reduced versions of those of Creagrus and Xema, and a shallowly forked tail. They are white-hooded in summer. It is unclear whether the peculiar Ivory Gull, white when adult, spotted brown in juvenile plumage, belongs near these primitive species. All other gulls may be placed in a single genus Larus, subdivided into 5 main groups. Central Eurasian gulls. The Great Black-headed Gull Larus ichthyaetus, Mediterranean Gull L. melanocephalus and Relict Gull L. relictus, breeding on the inland seas and lakes of Eurasian steppes are much alike in

downy and juvenile plumages and, when adult, differ mostly in size and mantle shade. They are hooded in breeding plumage and have a characteristic auricular bridle in non-breeding dress. The agonistic behaviour of the Mediterranean Gull is very un-Larus-like, while that of the Relict Gull seems to have similarities with those of possibly primitive species in other groups such as Audouin's Gull L. audouinii or the Slender-billed Gull L. genei, so that the central Eurasian gulls may well occupy a position near the centre of evolution of the Larus gulls. Masked gulls. The relatives of the Black-headed Gull L. ridibundus form a successful homogeneous group, best characterized by the presence of a conspicuous white triangle along the leading edge of the wing, dark underside to the primaries, and the development of the Forward Display in the Long-Call performance. They are hooded or not in breeding plumage, differ in wing-tip pattern, but generally have a characteristic double band across the top of the head in non-breeding or immature plumage. The core species are the Black-headed Gull, the Grey-headed L. cirrocephalus, the Brown-headed L. maculipennis, the Andean L. serranus, the Silver L. novaehollandiae, Buller's Gull L. bulleri, and Hartlaub's Gull L. hartlaubii. Somewhat more distantly related seem to be Bonaparte's Gull L. philadelphia which lacks the dark underwing, the Slender-billed which lacks the Forward Display, the Indian Blackheaded Gull L. brunnicephalus and Saunders' Gull L. saundersi. The masked gulls seem to represent the top of one evolutionary line among Larus gulls, perhaps derived from the previous group. Herring gulls. This is also a large, homogeneous, successful group, probably at the summit of another evolutionary line; all species are large, with patterned or white wing tips, a white head in breeding dress, and usually a streaked hood in winter. Their legs are yellow or flesh-coloured, their bills usually with a red gonydeal patch, a unique pattern in Larus. The group comprises many closely related species, of almost identical behaviour, e.g., Glaucous L. hyperboreus, Iceland L. glaucoides, Thayer's L. thayeri, Glaucous-winged L. glaucescens, Western L. occidentalis, Yellow-footed L. livens, Dominican L. dominicanus, Slaty-backed L. schistisagus, Vega L. vegae, Great Black-backed L. marinus, Herring L. argentatus, Yellow-legged L. cachinnans, Lesser Black-backed L. fuscus, Armenian L. armenicus and California Gull L. californicus. American hooded gulls. The Laughing Gull L. atricilla and Franklin's Gull L. pipixcan are very similar in adult breeding plumage and almost identical in voice and behaviour. They are unquestionably closely related. The Lava Gull L. fuliginosus, endemic to the Galapagos, is an obvious dark derivative of the Laughing Gull. The affinities of the group with other gulls are not entirely clear but may be with the central Eurasian gulls on the one hand, the 'black-tails' (see below) and their allies on the other. Black-tailed gulls and allies. The Pacific Gull L. pacificus, Olrog's L. atlanticus, Belcher's L. belcheri and Japanese Gull L. crassirostris have a black band in the tail of the adult plumage, plain black wing-tips, a white head in breeding plumage; they approach the herring gulls in their ritualized behaviour, their juvenile and downy plumages, the yellow bill with a red or black and red tip, and the yellow legs; they may constitute an early offshoot of the line that leads to the argentatus group. A few fairly isolated species, the Grey L. modestus, Scoresby's L. scoresbii, Sooty L. hemprichii, White-eyed L. leucophthalmus, Audouin's and Heermann's Gull L. heermanni may all be related, more or less distantly, to the black-tailed gulls. Common and Ring-billed gulls. These 2 species are difficult to place and have usually been considered related. The Ring-billed L. delawarensis closely resembles the herring gulls in plumage but its behaviour seems to differ more from them than it does from some members of the blacktailed group. The Common Gull L. canus differs more from the herring gulls in downy and juvenile plumages, recalling the Laughing Gull or some 'black-tails', and is behaviourally isolated. Habitat. Most gulls are coastal throughout their life cycle. A few (the kittiwakes, Swallow-tailed and Sabine's Gulls) are truly pelagic during the non-breeding season, others (Ivory, Ross's Gull) frequent the edge of ice, or (Little Gull, Mediterranean Gull) offshore waters. A few feed inland in open terrain, away from water. For breeding most species resort to flat or fairly flat open ground near water, often on islands. A few (the kittiwakes, Swallow-tailed, Ivory and Thayer's Gulls) breed on cliffs and have developed a series of adaptations to minimize the risk of eggs or young falling (Cullen 1957, Hailman 1964). Others breed in coastal or inland marshes (e.g., the Black-headed, Grey-headed and Franklin's Gulls) where they may build floating platforms (Burger 1974). Bona-

Gyrfalcon

Great Black-backed Gull Larus marinus. (B.P.).

parte's Gull breeds in trees in wooded tundra, the Grey Gull in total desert far from the sea (Howell et al 1974). A few species (e.g. , Black-legged Kittiwake, Herring, Yellow-legged and Dominican Gulls) have adapted in some areas to nesting on man-made structures. Distribution. Worldwide, but with a scarcity of species in the tropics. Main centres of differentiation, with several original and isolated species, seem to exist in South America and in central Eurasia, while a more recent radiation of the herring gulls has given the northern shores a wealth of closely related forms. Populations. Many species are numerous and some, in association with man, are increasing at remarkable rates. These belong mostly to the herring and masked groups. A few species, however, are uncommon with a restricted range and thus vulnerable. Examples are the solitary Lava Gull of the Galapagos, the very local Olrog's Gull of the coast of Argentina and the Mediterranean Audouin's Gull. Movements. No gull is completely sedentary, and most species undertake migratory movements of at least restricted amplitudes, often along the coasts they frequent. These generally take the form of a post-breeding movement to lower latitudes, but a few species disperse to higher latitudes (Heermann's Gull and the Yellow-footed in western North America, the Yellow-legged Gull in Europe) and some populations shift longitudinally (the Mediterranean Gull from the Black Sea to the Mediterranean and the Atlantic, Ross's Gull from Siberia east in the Arctic Ocean). Three species regularly perform trans-tropical or transequatorial movements, the Lesser Black-backed Gull from northern Europe and western Siberia to Africa and India, Franklin's Gull from the northern American prairie to South America, reaching Tierra del Fuego, Sabine's Gull from the Arctic as far as the open seas off South Africa and South America. Food. Many species feed on marine invertebrates in the intertidal zone. A few, such as the Slender-billed or Grey Gulls (when feeding young) are specialized fish predators; pelagic gulls take fish and invertebrates. Many species feed for at least part of the year on freshwater or even terrestrial invertebrates. Some (e.g., Great Black-backed, Glaucous and Dominican Gulls) are predators of mammals and birds. Fishing and hunting techniques include probing and prying, actively chasing on foot (e.g., Grey Gull), pecking at the surface of the water, up-tilting, quartering, hovering and snatching, plunging. Many species are scavengers, some specializing in robbing eggs, young or spilled food at sea-bird colonies, or in associating with marine mammals (Scoresby's Gull). Piracy on terns or smaller gulls is widespread, as is association with flocks of fishing mergansers Mergus, cormorants Phalacrocorax or divers Gavia. Many species, notably of the herring and masked gull groups, also Franklin's Gull, exploit human refuse and fishing activities. Behaviour and voice. Gulls are almost completely diurnal, though some migrate at night; the Grey Gull undertakes at night the long flights

269

between the sea and the desert where it feeds its young and the Swallow-tailed Gull is mostly nocturnal, at least on the breeding grounds. Almost all species are highly gregarious, often breeding in large, dense colonies, roosting in vast multispecific roosts, and feeding socially. They have thus developed a rich repertoire of both visual and auditory social signals, the significance of which has been best described by Howell et ale The form taken by the expression of self-advertisement, anxiety, threat, intention to flee or attack, dominance, and submissiveness differs somewhat from species to species, though along consistent lines. It has been studied in detail for several species, representing most groups, and comparative, partial summaries have been made, for example by Tinbergen (1959a) and Moynihan (1962). Among the most important, widespread, and conspicuous displays are the silent Upright, indicating anxiety or aggression, the aggressive Choking, the begging Head-toss, and the Long Call, a usually ringing and far-carrying vocal utterance, accompanied by a complex posture and proclaiming a readiness to interact either aggressively or amicably. Besides the Long Call and Long Call notes, the most often heard vocalizations are the guttural alarm notes, the cat-like mewing, and the whining soliciting calls of females and juveniles. The Swallow-tailed Gull has a peculiar 'rattle and whistle' alarm call, which has been correlated with the threat from frigate-birds (Fregatidae) (Snow and Snow 1968). Breeding. Most gulls breed upon assuming adult plumage, at 1-5 years old. The pair-bond is normally monogamous, and fidelity to colony, nest-site and partner is high in established breeders. Pair formation may occur at the nest-site or in 'clubs' of non-breeders, which are characteristic of some species. The breeding cycle of most species is annual but 2 broods a year are known in some populations of the Silver Gull (Nicholls 1964) and Hartlaub's Gull. The Swallow-tailed Gull breeds throughout the year. Gulls' nests are sometimes extremely rudimentary, sometimes bulky and sometimes untidy. One to 4, mostly 2 to 3 brown, olive, blue or grey, heavily mottled eggs are laid. The incubation period is from 3-4 weeks; both parents incubate and care for the young. The chicks are alert at birth and are fed in or near the nest for 2-3 weeks, usually until fledging at ~S weeks and, in the herring gulls, sometimes for several weeks thereafter. See photos: COLORATION ADAPTIVE; CONSERVATION; DRINKING; FEEDING HABITS; MOBBING; NOCTURNAL HABITS; PARENTAL CARE; PIRACY; RITUALIZATION.

P.o.

Burger, J. 1974. Breeding adaptations of Franklin's Gull (Larus pipixcan) to a marsh habitat. Anim. Behav. 22: 521-567. Cullen, E. 1957. Adaptations in the Kittiwake to cliff-nesting. Ibis. 99: 275-302. Dwight, J. 1925. The gulls of the world. Bull. Amer. Mus. Nat. Hist. 52: 63-401. Hailman, J.P. 1964. The Galapagos Swallow-tailed Gull is nocturnal. Wilson Bull. 76: 347-354. Howell, T.R., Araya, B. & Millie, W.R. 1974. Breeding biology of the Gray Gull, Larus modestus. Univ. Calif. Publ. Zool. 104: 1-57. Moynihan, M. 1959. A revision of the family Laridae (Aves). Amer. Mus. Novitates 1928: 1-42. Moynihan, M. 1962. Hostile and sexual behavior patterns of South American and Pacific Laridae. Behav. Suppl. 8: 1-365. Nicholls, C.A. 1964. Double-broodedness in the Silver Gull Larus novaehollandiae. W. Austral. Nat. 9: 73-77. Snow, B.K. & Snow, D.W. 1968. Behavior of the Swallow-tailed Gull of the Galapagos. Condor 70: 252-264. Stout, J.F. 1975. Aggressive communication by Larus glaucescens, III. Behaviour 55: 181-208. Tinbergen, N. 1959. The Herring Gull's World. London. Tinbergen, N. 1959a. Comparative studies of the behaviour of gulls (Laridae): a progress report. Behaviour 15: 1-70.

GULLET: the anterior part of the oesophagus (see

ALIMENTARY

SYSTEM).

GUT: the alimentary tract, from mouth to cloaca (see SYSTEM).

GYMNORHINAL: see

NARIS.

GYNANDROMORPHISM: see GYPAETINAE: see

PLUMAGE, ABNORMAL.

VULTURE (1).

GYRFALCON: Falco rusticolus (see

FALCON).

ALIMENTARY

H

The relatively simple habitat requirements of birds have an important bearing on their conservation. It is possible to create suitable habitats for many species of birds simply by digging ponds, flooding fields or planting trees and bushes, whereas many plant and invertebrate species, with their more exacting requirements, are unable to colonize these places for many years and so can only be conserved by retaining their existing habitats. N.W.M. Diamond, J.M. 1975. Assembly of species communities. In Cody, M.L. & Diamond, J .M. (eds.). Ecology and Evolution of Communities. Cambridge, Mass. pp. 342-444. Elton, C.S. 1966. The Pattern of Animal Communities. London. Fuller, R.J. 1982. Bird Habitats in Britain. Calton. Lack, D. 1971. Ecological Isolation in Birds. Oxford. Reynolds, J.F. 1980. In Britton, P.L. (ed.). Birds of East Africa. Nairobi. Southwood, T.R.E. 1977. Habitat, the templet for ecological strategies? J. Anim. Eco!. 46: 337-365.

HABITAT: the particular environment inhabited by a particular living organism. The environment thus described comprises the whole complex of flora, fauna, soil and climatic factors to which the organism is adapted. The term has been extended to cover the particular environment inhabited by a community of organisms. When it is used like this, the emphasis moves from the relationship with an organism to the biological nature of an area, and hence the term becomes virtually synonymous with BIOTOPE. The meaning of the word 'habitat' is further confused because at one time it could also mean the geographical distribution or range of a species. The habitat of a bird species can only be determined by field studies in which the full range of opportunities and constraints in nature is related to the adaptive characteristics of the bird. Much is known about the general requirements of different species and their general adaptations, but very little about the exact constraints, and so it is not yet possible to describe the habitat requirements of most birds definitively. For example, the distribution of many species can be fitted to isotherms, but it is not usually known whether temperature is operating directly or through food supply or some other component of the environment. In some cases limited food or nesting site requirements clearly limit the species' habitat. For example, the Snail or the Everglades Kite Rostrhamus sociabilis is restricted by the distribution of the freshwater Apple Snail Pomacea on which it is almost entirely dependent for food. The Golden-shouldered Parrot Psephotus chrysopterygtus is dependent for nesting on the large termite mounds found in parts of the Cape York Peninsula of Australia. Nest sanitation of this species depends upon its symbiotic relationship with larvae of the moth N eossiosynoeca scatophaga. The timing of nesting of a particular bird species may indicate its dependence on a particular food species, for example, the nesting of the White-cheeked Honeyeater Phylidonyris niger coincides with the peak flowering of Banksia ericifolia, the beak of the Honeyeater being adapted to obtain the nectar from the Banksia flowers. In general the more specialized species are found in stable tropical habitats (see ECOLOGY). At the other extreme, highly adaptable opportunist species (the 'r' species) such as House Sparrows Passer domesticus and Starlings Sturnus vulgaris can live in numerous kinds of biotopes throughout the world. Most species appear to be intermediate in their habitat requirements: they are confined to major botanical formations, e.g. temperate broad-leaved woodland, but not restricted by the distribution of particular plant or animal species. In some birds the breeding habitat is very different from the wintering one. For example, in Europe the Chiffchaff Phylloscopus coilybita breeds in light broadleaved woodland and coniferous forests but winters in dry savanna in Northern Africa. The Little Auk Plautus aile breeds on Arctic sea cliffs and mountains, but is largely pelagic in winter, and the Black Tern Chlidonias niger breeds in freshwater marshes and lagoons but spends the winter on tropical sea coasts. In some species the habitat differs in different parts of its range. For example in Britain the Dartford Warbler Sylvia undata is confined to areas dominated by tall heather Cailuna, thick gorse Ulex or mixtures of the two, but in North Spain it also occurs in open pinewoods. Sudden changes in habitat requirements have been observed from time to time. These have enabled the species concerned to enlarge its range, as when the Little Ringed Plover Charadrius dubius, whose principal original habitat was sand banks in large rivers, extended its range by colonizing gravel pits. The habitats of birds (and mammals) tend to be much wider than those of insects. This reflects their more catholic feeding habits and more plastic behaviour. Structure of habitat is usually more important to birds than the plant species which form it. Therefore it is possible to devise quite simple classifications of bird habitats, for example that of J.F. Reynolds, which has 16 basic categories consisting of easily identified structural types of vegetation (e.g. grassland, bushed grassland, wooded grassland etc.).

HACK: term used in

FALCONRY.

HACKLE: a long slender feather on the neck; such feathers are found, especially,: in various species of Galliformes. HADADA: Hagedashia hagedash (see HAEMATOPODIDAE:

see

IBIS).

under

CHARADRIIFORMES;

OYSTER-

CATCHER.

HAEMOGLOBIN: see

BLOOD.

HAGGARD: term for a hawk caught as an adult and trained (one caught as full-grown but in its first plumage is a 'passage hawk')-see FALCONRY.

HALCYON: poetic name for

KINGFISHER.

HALLUX: the first toe, usually 'opposed' (i.e. directed backwards) in birds and often much reduced (sometimes absent)-see LEG; SKELETON, POST -CRANIAL.

HAMERKOP: name, alternatively 'Hammer-headed Stork' or 'Anvilhead', of Scopus umbrella, sole genus and species of the Scopidae (Ciconiiformes, suborder Ciconiae). In the past a relationship to the Charadriiformes has been proposed for Scopus as it shares with them 2 genera of Mallophaga and only one with the Ciconiidae, but its egg-white protein suggests it may be related to the storks. However, Kahl (1967) found its behaviour quite different from either the storks or herons and concluded that it has no 'particularly close relationship with any other living bird so far studied'. Many legends are centred about the bird and they receive some protection from the taboos that have developed. One common native legend is that other birds bring nesting material to their remarkably structured nest (see below). Characteristics. The Hamerkop is a rather heavy-looking bird (c. 56 ern long), with short legs, a moderately long bill that is laterally compressed and slightly hooked, and rather long wings and tail. The conspicuous feature is a long backward-pointing crest which, together with its bill, produces an anvil shaped head from which it gets its common names. The plumage, which is the same for both sexes, is dark chocolate-brown, and the bill and legs are black, giving it a sombre appearance. Powder-down patches are lacking, but the middle toe is pectinated as in herons, and the 3 forward toes are connected by a partial web. Hamerkops are very agile fliers and their relatively large, rounded wings give them an owl-like shape when in flight. During normal flapping flight the head is only partially retracted on the shoulders but, when soaring or gliding, both less frequent than in storks, it usually extends its neck fully. Habitat and distribution. It is found throughout the Afrotropical region and its range extends also to Madagascar and south-western Arabia. The birds inhabiting the coast of West Africa belong to a dwarf race. Hamerkops may be found in a wide variety of wetlands including estuaries, mangrove creeks, swamps, rice fields and ponds provided these are bordered generously with trees and/or cliffs. Because of taboos the birds are often tame and found in villages. Food. A variety of small fish, shrimps and insects may be taken, but 270

Harrier-hawk

the principal food is frogs of the genus Xenopus and their tadpoles, which also form a major part of the nestling diet. When foraging, the bird usually walks along the edge of a pool or stream or wades in shallow water. In muddy water the Hamerkop probes repeatedly for prey, whereas in clear water the prey are snatched from the water surface. In both cases, it uses its feet to disturb prey from the substrate. Hamerkops pick tadpoles from off the surface by flapping low over the water and flying at low speed into the wind with very deep wing strokes. Behaviour. Social gatherings, sometimes involving up to 20 birds, are common away from nesting areas; the most demonstrative displays take place in groups when they feed. Several displays have been described by Kahl (1967), one of the more bizarre being the false mounting display. This may occur outside the breeding season and consists of one bird jumping on to the back of another as if intending to copulate, and standing there while beating its wings and giving a specific series of calls. Either sex may assume the top position and often the birds may alternate positions a number of times. This behaviour often occurs between mates but is not confined to mated pairs, and may occur on a tree, on the ground or on top of a nest. There are some preliminary displays that precede the false-mounting display and also precede true copulation. Paired birds indulge in a wing-flapping and bowing display while uttering braying calls. Hamerkops are apparently monogamous and birds may remain paired for several years, but co-operative nest building has been observed (Gentis 1976). Although active during the day, Hamerkops become more active at dusk and are semi-nocturnal in their habits. They often use the backs of hippopotamuses as perches. Voice. When 3 or more birds are together they generally join in mutual calling displays; the calls start with a series of loud, high pitched yips, becoming more rapid until they run together into a trilling note. These notes also accompany the false-mounting and other displays. Sometimes when a pair is flying together the birds keep in mutual contact by means of a few soft kep notes. Breeding. The Hamerkop, a non-colonial nester, builds a remarkable enclosed nest of sticks, grass and mud placed 5-12 m up in the fork of a tree (often over water) or, less commonly, on the ground or on a cliff face. It may take a few months to build and measures about 1m in diameter. Inside is a carefully shaped internal chamber, which is about 30-50 em in diameter and height. The entrance tunnel (c. 13-18 em in diameter and c. 40-60 em long) is heavily plastered with mud to give it a smooth surface. The 3-6 eggs are chalky white; the incubation period is about 21 days, and the nidicolous young, fed by both parents, spend about 7 weeks in the nest before fledging. The initial plumage of the young is brown apart

271

from white on the head, neck, back and wings, but by the time they leave the nest they are brown all over. W.R.S. and L.G.G. Gentis, S. 1976. Co-operative nest building by Hammerkops. Honeyguide 88: 48. Kahl, M.P. 1967. Observations on the behaviour of the Hammerkop Scopus umbrella in Uganda. Ibis 109: 25-32.

HAMMERHEAD: see

HAMERKOP.

HAMULUS: a hooked barbicel (see

FEATHER).

HANDBOOK: see regional articles. HANDEDNESS: see FOOTEDNESS. HANDSAW: see HERNSHAW. HANGNEST: name sometimes applied, in North America, to Icterus spp. (for family see ORIOLE (2)). HAPLOOPHONAE: see under

PASSERIFORMES.

HARDY-WEINBERG LAW: a law of population genetics, established in 1908 by G.H. Hardy and W. Weinberg, which relates mathematically the frequency of alleles in a population at a particular genetic locus to the frequency of genotypes at that locus. In its simplest form the law states that if at a particular locus there are 2 alleles A and AI, and if the frequency of A p and the frequency of A! = q (such that p + q = 1), then the frequency of the 3 genotypes AA, AAI and AlA I will be p2: 2pq :q2. This is the binomial expansion of the expression (p + q)2. Thus if a population is in Hardy-Weinberg equilibrium, it means that there is a predictable and defined ratio between the 3 genotypes. The law is only true if a number of stringent conditions apply. These are (1) that the population must be large enough for sampling errors to be ignored, (2) that there is no mutation, migration or differential selection, and (3) that mating among individuals of the different genotypes be random. The law is valuable to population biologists in two ways. Firstly, if a polymorphism is suspected to have a genetic basis, then it defines the expected relative frequencies of the distinct phenotypes. For instance, if it is suspected that the 3 morphs of the Arctic Skua Stercorarius parasiticus, dark, intermediate and light, are determined respectively by 3 genotypes AA, AAI and AlAI, then at equilibrium the 3 morphs will occur in a predictable ratio dependent only upon the frequencies of the 2 alleles A and AI. If as an example 36% of the population (p2) were dark, 48% (2 pq) should be intermediate and 160/0 (q2) light. The law is also useful when the genetic basis for the polymorphism is already known. If then the genotypes are not in the predicted frequencies, it may be suspected that one or more of the conditions stated above are not holding. Deviations from the Hardy-Weinberg equilibrium have been used as a crude first indication that selection is occurring or that a population is not mating at random (see also GENETICS.) F.C. HAREM POLYGAMY: see

POLYGAMY.

HARLEQUIN: sometimes used by itself for the Harlequin Duck Histrionicus histrionicus (see DUCK). HARPY: sometimes, at least formerly, used alone for the Harpy Eagle Harpia harpyja (see under HAWK). See also FABULOUS BIRDS. HARRIER: substantive name of Circus spp.; in the plural, general term for the subfamily Circinae of the Accipitridae. HARRIER EAGLE: substantive name, alternatively 'serpent eagle', of species of Circaetinae (Accipitridae); in the plural, general term for the subfamily (see HAWK). HARRIER-HAWK (1): substantive name of species of Polyboroidinae (Accipitridae); in the plural, general term for the subfamily (see HAWK).

Hamerkop Scopus umbrella. (R.G.).

HARRIER-HAWK (2): sometimes used as the substantive name, alternatively 'forest falcon' (Brown and Amadon), of Micrastur spp.; in the plural, serves as a general term for the Herpetotherinae (see FALCON).

272 Hatching

eggshell by movements alone . The shell is always weaker after incubation through the loss of mineral substances dissolved out of it, transported by the blood and used to prepare the first ossification of the skeleton. The hatching of different eggs in a clutch may be almost synchronous or there may be a considerable interval between first and last. In many species the parents remove the fragments of eggshell from the nest ; but those with nidifugous young tend to leave them in situ. See also BEHAvIOUR, DEVELOPMENT OF; DEvELOPMENT, EMBRYONIC; EGG; GROWTH; INCUBATION; PARENTAL CARE ; YOUNG BIRD. See photo PARENTAL CARE. A.P. and W.S . Oppenheim. R.W. 1972. Prehatching and hatching behaviorin birds: a comparative study of altricial and precocial species. Anim. Behav. 20: 644--655. Oppenheim, R.W. 1973. Prehatching and hatching behavior: comparative and physiological considerations. In Gottlieb, G. (ed .) , Behavioral Embryology. New York. Romanoff, A.L. 1960. The Avian Embryo: Structural and Functional Development. New York. HATCHLING : term sometimes applied to a newly hatched bird (see YOUNG BIRD).

Whimbrei Numenius phaeopus chicks hatching. (P hoto: E.] . Hosking ). HATCHING: emergence of the developed chick from the egg after incubation ; the term is applied both to the egg and the chick, e.g. the eggs 'hatch', the young 'are hatched ' or 'hatch out' . Eggs showing the first cracks in the shell are 'pipped', 'chipping' or 'starred' . Hatching is prepared for by several synchronized processes. It often takes some hours, but may be reduced to about half an hour in small birds. The young bird has to change from breathing in the amniotic fluid to respiration in air, and it must break the hard eggshell by its own means . The time of hatching is fixed for each species by an innately determined series of events. Some days before it breaks the shell , the embryo starts swallowing the amniotic liquid . The tissues, particularly the muscles, thus acquire a very high water content at birth, but this diminishes rapidly . The contents of the albumen-sac go the same way . The yolk-sac is driven into the body cavity by movements of the abdominal musculature. The new-born bird always has an internal yolk-sac, of which the mass varies from 25% of the birth weight in the Ostrich Struthio camelus to c. 5% in small passerines. The yolk mass vanishes rapidly in the first 6 days after hatching. During incubation a constant water loss by evaporation produces an air chamber between the two shell-membranes (at the blunt pole of the egg). An aerated space is thus formed, into which the embryo penetrates. This moment marks the beginning of air respiration and is often announced by the cheeping of the baby bird, 2 or even 3 days before hatching. The blood supply of the allantois is still functioning and provides the necessary oxygen, the air-chamber being rich in carbon dioxide and insufficient for the needs of the young bird . Very soon partial respiration by the lungs is started, the eggshell is opened, and the rapid drying up of the allantois begins. The vessels of the allantois are functional until the last moment before the navel is closed . At the moment of hatching the adult type of breathing is firmly established . Immediately before the bill enters the air-chamber, the embryo changes from a transverse position into a longitudinal one , thus directing its bill towards the air space . This movement permits the use of a special tool for hatching , the egg-tooth on the tip of the maxilla . The formation of this structure, present in the great majority of birds, begins about the sixth day of incubation (domestic fowl, duck) . It is horny , without any mineral substance. In some birds a corresponding thickening is produced also at the tip of the lower mandible. The egg-tooth produces the first openings; stretching of the head and movements of the legs help to burst the shell. Sooner or later after hatching the shell-breaking tool is lost, in some groups, such as the penguins, not for some weeks. No egg tooth is formed in the Ostrich and the megapodes, but it is not known whether this condition is primitive or secondary; the young of these birds are very far developed and strong enough to break the

HAWAIIAN HONEYCREEPER: substantive name for species of the family Drepanididae (Passeriformes, suborder Oscines). This family, treated by some as the subfamily Drepanidinae of the family Fringillidae, is endemic to the Hawaiian Archipelago including 63 ha Nihoa Island and Laysan Atoll in the North-western Hawaiian Islands. The recent discovery of the Poo-uli Melamprosops phaeosoma on Maui (Casey and Jacobi 1974) brings the total number of described species to 23. To this at least 15 recently discovered fossil species, as yet undescribed, must be added (Olson and James 1982). Geographic isolation within the archipelago has produced impressive variation-40 taxa are currently recognized. Evolution, morphology and characteristics. The Hawaiian honeycreepers are supposed to have been derived recently from cardueline finches : Telespyza c. cantans on Laysan and T . c. ultima on Nihoa are most similar to the founder species (Raikow 1977). The subfamilv is best known for its remarkable adaptive radiation. Bill shapes (Fig. i) range from powerful seed-cracking cones (Grosbeak Finch Psiuirostra kona ) to attenuate, decurved probes 6.6 em long, one third the bird 's length (K auai Akialoa Hemignathus procerus). Between these extremes are found bills shaped like those of parrots (Maui Parrot bill Ps eudonestor xanthophrys) a?d warblers tLaxops parva , Paroreomyza maculata ), and the unique bill of the Akiapolaau Hemignathus wilsoni, whose upper mandible , long and decurved, is nearly twice the length of the stout , straight lower mandible . Despite this diversity in bill structure, the Drepanididae have very similar appendicular myology , much like that of cardueline finches . The similarity of the tubular tongues of the nectarivores to New World 9-primaried oscines is due to convergence . Plumage colours include black, brown , white , green, yellow, red, and da zzling orange. Sexes are alike in colour in some species, unlike in others. Overall lengths

Fig. I. Bills of some Hawaiian honeycreepers : (a) Psittirostra bailleui; (b) Hemignathu s wilsoni ; (c) Hemignathus procerus; (d ) Loxops coccinea; (e) Vestiaria coccinea.

Hawk

range from 10em (Anianiau Loxops parva) to nearly 20 em (Greater Koa Finch Psittirostra palmeri and Hawaii Mamo Drepanis pacifica). Habitat. The majority of the extant drepanidids are presently confined to wet (rainfall up to 1,164cm per year) montane forests dominated by Ohia Metrosideros collina or Koa Acacia koa. On the island of Hawaii several species inhabit the much drier Mamane Sophora chrysophyllaNaio Myoporum sandwichense forests up to 3,000 m elevation. The family was formerly widespread in dry lowland forests, but these habitats, and their fauna, have been largely destroyed in the islands. Food. The Hawaiian honeycreepers feed upon a diversity of foods. Some, like the Apapane Himatione sanguinea, Iiwi Vestiaria coccinea, and Crested Honeycreeper Palmeria dolei are primarily nectarivorous, while others feed upon fruit (Ou Psittirostra psittacea) or green seeds (Palila Psittirostra bailleui). Most species, however, are primarily insectivorous. The omnivorous Nihoa Finch includes seabird eggs in its varied diet. The Apapane and Iiwi undertake daily migrations, often of many kilometres, in search of patchily distributed but locally abundant Ohia flowers, their primary source of nectar. Perhaps as a result of this mobility, they are monomorphic in the main islands (one other widespread species, the Ou, is undifferentiated between islands), and the Apapane reached Laysan Island, about 1,125 km north-west of Kauai, where it was represented by a local race that is now, unfortunately, extinct. Voice. Song is highly variable within the family, ranging from disconnected squeaky notes to melodic trills. The Apapane sings a bewildering variety of songs that vary within, and between, islands. Breeding. The breeding season extends from February to June for most species. Chasing is an important part of courtship, and often directly precedes copulation. Nests of only half the family have been described (Scott et al 1980). Most are open cups composed of twigs and lined with fine materials, such as mosses, tree fern scales, and other fibres (Berger 1972). They are generally placed within the canopy and are well hidden within terminal leaf clusters. Clutch size ranges from 1--4 eggs; 2 or 3 is the usual complement. Normally only the female incubates; she is fed away from the nest by the male. Nests of 3 species have been found in tree cavities; 2 species are known to use rock cavities, the Nihoa Finch preferentially so. The Laysan Finch nests in grass tussocks. Current status. It is tragic that of 40 described taxa, 16 are recently extinct and an additional 17 endangered. Their demise has resulted from a number of interrelated stresses that began with the first Polynesian settlement. Habitats have been vastly altered by man, and introduced mammals, notably pigs, goats, cattle, sheep, and Axis Deer Axis axis have devastated additional thousands of hectares. The Hawaiian honeycreepers proved highly susceptible to introduced diseases, especially avian malaria and pox, which were transmitted to them by an introduced mosquito Culex quinquefasciatus (Warner 1968). Predation by cats and rats may have also been important (Atkinson 1977), and competition with introduced forest birds, many now quite common, may have produced additional stress. Many of these factors remain uncontrolled, and more species may be lost unless vigorous corrective action is taken. A programme that successfully eradicated feral sheep from Mauna Kea in 1982 should help restore the essential habitat of the Palila. Similar programmes in prime rain-forest sites throughout the state could do much to improve the outlook for these fascinating birds. C.B.K. Amadon, D. 1950. The Hawaiian Honeycreepers (Aves, Drepanididae), Bull. Am. Mus. Nat. Hist. 95: 151-262. Atkinson, LA.E. 1977. A reassessment of factors, particularly Rattus rauus L., that influenced the decline of endemic forest birds in the Hawaiian Islands. Pac. Sci. 31: 109-133. Baldwin, P.H. 1952. Annual cycle, environment and evolution in the Hawaiian honeycreepers (Aves: Drepanididae). Univ. Calif. Pub!. Zoo!' 52: 285-398. Berger, A.J. 1972. Hawaiian Birdlife. Honolulu. Casey, T.L.C. & Jacobi, J.D. 1974. A new genus and species of bird from the island of Maui, Hawaii (Passeriformes: Drepanididae). Dec. Papers B.P. Bishop Mus., XXIV (12): 216-226. Olson, S.L. & James, H.F. 1982. Prodromus of the fossil avifauna of the Hawaiian Islands. Smithson. Contr. Zool. 365: 1-59. Raikow, R.J. 1977. The origin and evolution of the Hawaiian honeycreepers (Drepanididae). Living Bird 15: 95-117. Scott, J.M., Sincock, J.L. & Berger, A.J. 1980. Records of nests, eggs, nestlings, and cavity nesting of endemic passerine birds in Hawaii. Elepaio 40: 163-168. Warner, R. 1968. The role of introduced diseases in the extinction of the endemic Hawaiian avifauna. Condor 70: 101-120.

273

HA WAIIAN ISLANDS: a mid-oceanic archipelago having an avifauna largely related to the Nearctic Region but with elements of Australasian affinities (see AUSTRALASIAN REGION; DISTRIBUTION, GEOGRAPHICAL; HAWAIIAN HONEYCREEPER).

Peterson, R.T. 1961. A Field Guide to Western Birds. 2nd ed. Boston, Mass.

HAWFINCH: substantive name of Coccothraustes coccothraustes and of Eophona spp.; used without qualification for the first mentioned (see FINCH).

Hawfinch Coccothraustes coccothraustes. (D.A. T.).

HAWK: substantive name, or part of the substantive name, of many members of the Accipitridae (Accipitriformes, suborder Accipitres)-in North America the name is given to species of Accipitridae that in British usage have special substantive names (e.g. 'buzzard', 'harrier'), and is even applied to some species of Falconidae (see FALCON); in the plural, general term for the Accipitridae, the subject of this article except that the several genera of Old World vultures are separately treated (see VULTURE (1). Apart from the vultures, the family is often divided into subfamilies: the Accipitrinae (true hawks, including accipiters, buzzards, and eagles), Circaetinae (harrier eagles or serpent eagles), Circinae (harriers), Polyboroidinae (harrier-hawks in one sense), Milvinae (true kites and fish eagles), Perninae (honey-buzzard etc.), Elaninae (whitetailed kites), and the monotypic Machaerhamphinae (Bat-hawk). For convenience this grouping is followed here, but K.H. Voous regards all but one of these suggested subfamilies as united in a single group constituting the Accipitridae; and the monotypic Pandionidae as a separate family. Characteristics. The birds in this large and varied assemblage range from small sparrowhawks Accipiter spp. to huge and powerful eagles, those of the genera Harpia, Pithecophaga, and Haliaeetus being among the largest and strongest birds of prey in the world and among the largest of flying birds. Several of these large eagles exceed 6 kg in weight, 1m in body length and 2 m in wingspan. In almost all birds-of-prey the female of the species is larger than the male; she is often duller and browner in colour, and immature birds may be quite different in appearance from the adults. The degree of size dimorphism between the sexes is correlated with feeding habits, as species which specialize on snails, insects, reptiles, mammals or birds respectively show progressively greater dimorphism (Newton 1979). In some extreme bird-feeders, such as the European Sparrowhawk Accipiternisus, the female weighs almost twice as much as the male. The family has the characteristics of the order, of which the most obvious are the decurved and pointed bill, with base covered by a cere in which the external nares are situated,and the powerful gripping feet with strong sharp claws. Leaving aside the carrion-eating Old World vultures, they are-with some exceptions-hunters of live prey; the latter ranges from birds in flight to fish, and from sizeable mammals to insects. Unlike many of the owls, which have similar adaptations of bill and foot by convergence, they are diurnal in their habits-occasionally crepuscular (Machaerhamphus).

274 Hawk

Habitat and distribution. The Accipitridae are represented on all continents except Antarctica and in all kinds of habitat from thick forest to open grassland and desert. As expected of predators, these birds live at relatively low densities, and mostly in individual territories or home ranges, which include feeding areas. Under natural conditions, small species occur at densities up to about 1 pair/km", but larger ones are very much sparser. The large African Martial Eagle Polemaetus bellicosus occurs at one pair per 125-300 km-, with 30-40 km between pairs, and is thus one of the most thinly-spread birds in the world. However, in 'developed' regions, most species have been much reduced in numbers by human activities, especially habitat destruction, direct persecution and pesticide use. In consequence, many species which were numerous a century ago are now quite scarce, and some are among the most endangered of all birds. Where undisturbed, some species show extreme stability in breeding population, with the numbers over large areas changing by no more than 10% of the mean over long periods of years (e.g. Golden Eagle Aquila chrysaetosi. Such species usually feed on a wide spectrum of prey species, and thus have fairly stable food-supplies. Other species, which have restricted diets based on cyclic prey, fluctuate greatly in numbers from year to year, depending on their prey (e.g. Rough-legged Buzzard Buteo lagopus which feeds on lemmings and other rodents). Movements. From northern regions many species migrate south for the winter. The broad-winged types, such as buzzards and eagles, travel by soaring and gliding, and are thus dependent on updraughts or thermals. They form narrow migration streams along routes where conditions are favourable, such as north to south mountain chains or narrow sea crossings. In Europe, many thousands of individuals en route to Africa circumvent the Mediterranean each year via the Straits of Gibraltar in the west and the Bosphorus or Dardanelles in the east. In North America similar concentrations occur along mountain ranges, of which the most famous for observation is Hawk Mountain in Pennsylvania. Voice. Different species of the Accipitridae have screaming, yelping, mewing or cackling cries, which are heard mainly in the breeding season. Such vocalization is used primarily for communication between the sexes, but also in some species for territorial advertisement. Many call loudly when the nest area is invaded by a human or other predator. Behaviour and breeding. These rap tors have mainly aerial displays, involving soaring over the nesting area, diving or undulating flights, which probably serve to advertise possession of the territory. Other displays, early in the breeding cycle, are centred on nest-sites. Most species breed in trees, either making their own nests or sometimes adopting the nests of others; some eagles and buzzards breed on crags. The nests are built of sticks and are often lined with green leaves, sometimes with grass, rags, and oddments. The larger species build huge structures to which they return year after year. The main trends in breeding within the group are related to body-size. The larger the species: (1) the later the age at which breeding begins, (2) the longer each successful attempt takes, and (3) the fewer the young produced with each attempt (Newton 1979). Small clutches of 1-2 eggs are typical of large eagles, but the smaller species may lay 3-5 or even more. Incubation times vary from about 28 days in small sparrowhawks to 49 days in large eagles, and fledging periods from 28 days to 120 days. After leaving the nest, the young continue to be fed by their parents for another 21 days in small accipiters to several months in large eagles. In one or two eagle species, breeding cycles may be so long as to prevent breeding in successive years: the largest species are long-lived, slow-breeding birds. While breeding, there is a clear division of labour between the sexes, the male providing the food and the female incubating the eggs and tending the young. Only when the young are large enough to be left does the female help with the hunting. The young themselves could be described as 'semi-precocial' in that they hatch with a full covering of down and with their eyes open, in contrast to most other nidicolous birds. Initially the mother tears up small pieces of meat for them, which they take from her bill, but before fledging they learn to tear up prey for themselves. True hawks and eagles. The Accipitrinae are the largest and most varied subfamily, containing most of the world's hawks (in the strict sense), buzzards, and eagles. They may conveniently be divided into several smaller groupings. First, the genera Accipiter, Melierax, and Urotriorchis are small to medium-sized hawks of swift flight, generally inhabiting woodlands or forests, and preying upon birds, small mam-

mals, and reptiles. Of these only Accipiter occurs in the New World, while the others (Urotriorchis being monotypic) are confined to the Ethiopian Region. Three other genera, to be mentioned later, also belong to this group. The genus Accipiter contains the true sparrowhawks and is the largest of all the genera of the birds-of-prey, cosmopolitan in distribution, and with representative members in any woodland ecotype, from the pine forests of the far north to the most luxuriant tropical rain-forests and the thorn-scrub of Africa. All are broad-winged, long-tailed hawks, with rather long thin legs; they fly from tree to tree in the forest, and when hunting adopt methods of stealthy approach behind cover, culminating in a short, fast attack. Few of them can fly down birds in the open, but they are adept at catching them in thick vegetation. The largest member of the genus, the Goshawk Accipiter gentilis, is about 48-62 em long, grey above and white barred grey below, with a fierce yellow eye; it has been trained for falconry, as have several others of the genus, and is capable of killing birds as large as a Pheasant Phasianus colchicus and mammals up to the size of a hare (see FALCONRY). At the other extreme is the tiny African Little Sparrowhawk Accipiter minullus, about the size of a thrush, and living to a considerable extent on insects; these it catches in a short sortie after the manner of a flycatcher (Muscicapinae). Between these two extremes are hawks of every intermediate size, but all bold and aggressive, all inhabiting woodlands, and all living mainly on birds, with mammals and reptiles as side-lines. Close to the genus Accipiter is Melierax (including 'Micronisus'); these are birds of the open African thorn-bush, grey above, with white undersides barred with grey. The two chanting goshawks Melierax spp. are large birds (length 35-50 em) capable of killing guineafowl, but living chiefly on insects and lizards, which they often catch on the ground, running about like small editions of the Secretary-bird Sagittarius serpentarius. The Gabar Goshawk Melierax gabar is like a sparrowhawk in its habits. Finally there are the Long-tailed Hawk Urotriorchis macrourus, a strange dark-coloured hawk, black above with chestnut below and a long tail ornamented with white dots, which inhabits dense forests in West Africa and lives chiefly on arboreal squirrels and birds; 2 Australasian genera, Erythrotriorchis and Megatriorchis, of large and powerful hawks; and the Lizard Buzzard Kaupifalco monogrammicus, which preys chiefly on lizards and is found in east and southern Africa. The next subdivision of the Accipitrinae comprises large hawks with soaring flight, inhabiting woodlands or open country, and preying upon mammals and reptiles caught on the ground, with birds forming a minor part of the diet. The genus Buteo (including 'Rupornis' and 'Asturina'), containing the true buzzards, is the largest of this group, and is cosmopolitan in distribution save for Australasia and Malaysia. The genera Heterospizias, Leucopternis, Parabuteo, Buteogallus, and Busarellus are confined to Central and South America, and Butastur to Africa, India, and the East. Butastur spp. (e.g. the Grasshopper Buzzard B. rufipennis of Africa) are the least like buzzards of the whole group, having more the habits of harriers (Circinae). All these birds are large, with a body length of 50-65 em, and a wing-spread of 1-1.5 m. They all can soar, but they perch a great deal on trees, telegraph posts, or rocks, and catch their prey on the ground. Some frequent lowland swamps, others mountainous country; the Augur Buzzard Buteo rufofuscus occurs in Africa up to 5,500 m, and the Mexican Black Hawk Buteogallus anthracinus is found in swampy areas or tropical forest regions at low altitudes. They are mainly brown in colour when immature, but as adults often develop handsome plumages of brown, white, and red-brown, or black and white. Females are generally only slightly larger than males. Some are migratory, e.g. the Rough-legged Buzzard Buteo lagopus, which is also one of the few members of the group with the tarsus feathered to the toes. Others remain in their haunts all the year round, the tendency being for those that live in the far north to migrate, while most tropical and subtropical species do not. The third subdivision of the Accipitrinae consists of large or very large birds-of-prey, with wing-spread of up to 2.5 m and weight of 1-7 kg, generally called eagles. They include the following American genera: Harpyhaliaetus, Spizastur, Oroaetus, Morphnus, and Harpia. Stephanoaetus and Polemaetus inhabit Africa, and Ietinaetus, Harpyopsts, and Puhecophaga occur only in India and the Far East. The genera Aquila, Spizaetus, and Hieraaetus are of wider distribution. Aquila in particular is found in all regions of the world except South America and the Malaysian area, being represented in Australia by Aquila audax. All these birds are both large and aggressive, preying on large and small mammals, birds,

Hawk

and reptiles. Some eagles, especially Aquila spp., eat carrion; the Tawny Eagle A. rapax (length 65-77 em) pursues and robs other raptors of their prey. Although some are hardly bigger than buzzards, they are in general fiercer and more active than the birds of that group. They vary in size from small, active hawk-eagles of the genera Spizaetus and Hieraaetus to huge and powerful birds-of-prey iStephanoaetus, Polemaetus, Aquila, Harpyopsis, Pithecophaga, and Harpia). Aquila, Spizaetus, Spizastur, Hieraaetus, Stephanoaetus, Polemaetus, Oroaetus, and Ictinaetus have feathered tarsi, the rest bare tarsi. The largest and most powerful of all is the Harpy Eagle Harpia harpyja, inhabiting tropical South America; and scarcely smaller is the Philippine Monkey-eating Eagle Pithecophaga jeffetyi, which has unusual blue eyes. The smaller members of the group include Ayres' Hawk-eagle Hieraaetus ayresi, a rare bird of Africa which is like a sparrowhawk in its habits, living on birds of the tree-tops, and the very handsome Hieraaetus kieneri of India. Those that live in open country (Aquila, Polemaetus) tend to live principally on mammals and gallinaceous birds, caught upon the ground but often seized in spectacular fashion. All these birds are capable of beautiful soaring flight, and some of them are probably as fast as or, faster than, any other birds-of-prey, although they may appear, by reason of their large size, to move more slowly than some falcons. Their plumage varies from dull brown (Aquila) through various patterns of grey and white and black and white to very rich and beautiful combinations of black, buff, chestnut, and white (Stephanoaetus and Spisaetus ornatus). Two, Verreaux's Eagle Aquila verreauxi and the Black Eagle Ictinaetus malayensis, are mainly black, with white on the rump; the former lives almost entirely on hyraxes Procavia and Dendrohyrax; the latter species has the peculiar habit of feeding upon the eggs of other birds, taken in the nest. Snake eagles. The snake eagles, serpent eagles and harrier eagles are sometimes placed in a subfamily Circaetinae; they live principally on snakes and other reptiles and have feet specially adapted, with short rough toes of immense power, for grasping and holding this prey. Circaetus, Terathopius, and Dryotriorchis are African genera, the latter two monotypic and the first with one of its species, the Short-toed Eagle C. gallicus (length 62-68 em) extending over the warmer parts of Europe, Asia, and Africa. The crested serpent eagles Spilornis spp. occur from India to the Philippines, and Eutriorchis astur inhabits Madagascar. The habits of these birds in the field are much like those of other large eagles. They are given to soaring for long periods, or to perching on outstanding trees and rocks whence they can see their prey; the Short-toed Eagle can hover like a Kestrel Falco tinnunculus, although relatively large (see FALCON). They drop on their prey and either snatch it in the air or kill it on the ground. When eating snakes, they crush the head first, afterwards swallowing the rest of the body whole. They inhabit open country, forests, and bushland. The most remarkable of the whole group is the Bateleur Terathopius ecaudatus (length 80-85 em) of Africa, which has exceptionally long wings (wing span 170-180 em) and a very short tail (8-10 em). Birds of this species fly perhaps 300km on most days of their lives, canting from side to side and occasionally performing astonishing aerobatics. They eat carrion and mammals as well as reptiles, and will pursue and attack other carrion birds in the hope of making them disgorge. The Serpent Eagle Dryotriorchis spectabilis of West Africa is a strange bird of dense tropical forests and has large eyes that perhaps help it to see in poor light. Harriers. The subfamily Circinae, cosmopolitan in distribution, contains the harriers Circus spp., a very characteristic genus inhabiting open country, cultivations, or swampy land. They are either mainly brown in colour or, in some species, the males are grey and the females and juveniles brown; two species, Circus maurus of South Africa and C. melanoleucus breeding in north-eastern Asia, are black and white. All harriers are slender, long-winged, long-tailed birds with long legs, and rather owlish heads, ranging between 40-56 em in body length. They spend most of the day on the wing but also perch on posts and hillocks. Their habits are similar all over the world: they fly low over the ground, systematically quartering to and fro, and dropping on prey in the grass. Unlike most birds-of-prey, they both roost and breed on the ground; and the male, when bringing prey, characteristically passes it to the female in flight, a little way from the nest. One species, the Spotted Harrier C. assimilis of Australia, nests in trees. Some of the species are migratory, the Palearctic Pallid Harrier C. macrourus being one of the commonest birds-of-prey in the plains of Africa and India in winter. On migration they tend to be gregarious, and they roost in company in 'forms' in the grass (Pallid Harrier and Marsh Harrier C. aeruginosus). Some tend to

275

concentrate in swampy localities and others in dry open plains or steppe, but they never frequent woodland country for long. They live on small mammals, frogs, and some insects and reptiles, but occasionally also take birds on the ground. Harrier-hawks. The subfamily Polyboroidinae contains the harrierhawks, curious long-tailed, long-legged birds the size of a buzzard, grey and black in plumage with yellow legs and bare skin on the face; they inhabit Africa and Madagascar, usually in wooded country. The South American genus Geranospiza is probably closely related. The African continental species is the Harrier-hawk Polyboroides typicus. They are unable to kill any large prey, and have buoyant, rather erratic flight. They feed largely on the young of other birds, and in attacking weaver-bird (Ploceidae) broods, they often hang head downwards with flapping wings. The double-jointedness of their legs enables them more easily to extract nestlings from tree-holes and other enclosed nests. They are also fond of the fruits of the Oil Palm Elaeis guineensis. The term 'harrier-hawks' is also applied to certain Neotropical Falconidae (see FALCON).

True kites and fish eagles. The Milvinae are a large and varied subfamily of cosmopolitan distribution, containing the genera Milvus, Lophoictinia, Hamirostra, Haliaeetus, Ichthyophaga, Haliastur, Rostrhamus, Harpagus, and Ictinia. The Black Kite Milous migrans (length 55-60 em), in its many races, is one of the commonest and most obvious birds-ofprey in the warmer parts of the Old World, scavenging in hundreds in towns and villages of the East. It is migratory throughout its range to a greater or lesser extent, and decidedly gregarious on migration. However, it was apparently the Red Kite M. milvus (length 60-66 em) that was formerly a common scavenger in London. Haliaeetus and I chthyophaga are 2 genera of large or very large birds-of-prey living mostly on fish. Haliaeetus, comprising the fish eagles and sea eagles, is nearly cosmopolitan in distribution and contains some of the largest and finest of all birds-of-prey, among them the European Sea Eagle H. albicilla (length 70-90cm), the American Bald Eagle H. leucacephalus (length 70-90 em), Steller's Sea Eagle H. pelagicus (length 80-100 em) of north-eastern Asia and the Fish Eagle Haliaeetus oocifer (length 74-84 em) of tropical Africa. The smaller fishing eagles I chthyophaga spp. inhabit inland lakes, rivers, and ponds in southern Asia and live on fish amongst other food. Haliasturis a genus of2 species, inhabiting India, the Far East, and Australia, and in places very common; the Brahminy Kite H. indus, regarded as sacred in India, inhabits swampy areas, and lives on frogs and offal. The American genera Rostrhamus, Harpagus, and Ictinia are rather unlike the Old World kites in their general habits, and their members are considerably smaller. The Snail or Everglade Kite R. sociabilis breeds in colonies and feeds exclusively on snails, which it extracts from the shell with the long point of its upper mandible. Rostrhamus hamatusalso has a remarkably long and sickle-shaped bill. The genus I ctinia contains small grey kites, in appearance very unlike the typical Milvus spp. of Europe and Asia; they live in open country, feed largely on insects, spend a great deal of time on the wing, and are capable of remarkable aerial evolutions; they are migratory and tend to be gregarious on migration. Honey-buzzards. The subfamily Perninae contains a variety of genera difficult to relate to others--Leptodon, Chondrohierax, and Elanoides in America, Pernis and Aviceda in Europe, Asia, and Africa, and Henicopemis in New Guinea and nearby islands. The Honey-buzzard Pemis apiuorus (length 52-60 cm) of Europe and Asia is a medium-sized buzzard-like bird which feeds chiefly on the grubs in bees' and wasps' nests. It is a migrant, moving south from Europe in numbers to Africa, and from northern Asia to India and farther east. The Swallow-tailed Kite Elanoides forficatus of America (not to be confused with the African bird of the same English name, mentioned below) is a very beautiful bird, with black back, tail, and wings, the rest of the plumage being white; it has remarkable powers of flight, and on account of its beauty has been much persecuted. The so-called cuckoo-falcons Aviceda spp. are widespread in Africa, India, and the Far East, one reaching Australia. Superficially rather like sparrowhawks, but distinguished by having two notches on the upper mandible, they are crested and generally conspicuously patterned in plumage; the Black Baza A. leuphotes of northeastern India and Malaysia is a very striking black-and-white bird, while other members of the genus are grey or brown above and often handsomely barred below. They are generally insectivorous, and in most parts of their range rather rare. They were formerly placed close to Harpagus, to which they have certain similarities.

276 Hawk

Craighead, J.J. & Craighead, F .C. 1956. Hawks, Owls and Wildlife. Pennsylvania. Newton, I. 1979. Population Ecology of Raptors. Berkhamsted. Swann, H.K. 1924-1945. (ed. Wetmore, A.). Monograph of the Birds of Prey (Order Accipitres). 2 vols (1930, 1945). London.

HA WK-EAGLE: substantive name of species of Spizaetus, Hieraaetus, and allied genera (Accipitrinae)--see HAWK. HAWKING: synonymous with FALCONRY; also used to describe the behaviour of a bird of any kind flying in search or pursuit of prey. HEAD: see

TOPOGRAPHY;

also

BILL.

HEADING: the direction in which a bird is flying through the air, as distinct (in a wind) from its 'track' relative to the earth's surface (see MIGRATION; TRACK).

Osprey Pandion haliaetus. (K.]. W.).

White-tailed kites. The Elaninae are a nearly cosmopolitan subfamily of small or very small birds-of-prey (length 30--35 ern), inhabiting open country. Elanus spp. occur in America and the warmer parts of Europe, southern Asia, Africa, and Australia; examples are the White-tailed Kite E. leucurus of America and the Black-shouldered Kite E. caeruleus widespread in the Old World. All members of the genus are small grey-and-white hawks, superficially like falcons, with black markings at the fore edge of the wing. They are attractive birds, perching constantly on telegraph posts or tall trees, dropping on insects and small mammals in the grass. They can hover very gracefully, like the Kestrel. The other two members of the subfamily are very small and beautiful birds-of-prey in monotypic genera, the Pearl Kite Gampsonyx swainsoni of America and the Swallow-tailed Kite Chelictinia riocourii of northern tropical Africa. The Pearl Kite is one of the smallest birds-of-prey, and is blackish above, with rufous on head and back, and white below; it has well developed powder-down tracts. Chelietinia is an exquisitely graceful little bird with swallow-like forked tail, grey and white plumage, and a flight so buoyant that it resembles a tern rather than a bird-of-prey. It is gregarious, migratory, and breeds in small colonies, sometimes associated with larger birds-of-prey; it feeds on insects. Bat-hawk. The subfamily Machaerhamphinae contains a single species, the Bat-hawk Machaerhamphus alcinus, which inhabits Africa and parts of the Far East and has the remarkable habit of catching bats as they emerge from caves or buildings at dusk; this prey is commonly swallowed in flight. In general appearance like a large falcon, the Bat-hawk has a wide gape and very large eyes adapted to its habits; it flies extremely swiftly, looking up, down, and sideways when hunting. It requires an open space such as a large pool in a river, a station platform, or an open lawn to be successful, and in addition to bats it eats swallows and martins (Hirundinidae); it spends the day in shady trees, and it is a rare bird, solitary in habit, throughout its range. Osprey. The Pandionidae comprise only the Osprey Pandion haliaetus (length 55-58 ern) a bird of almost cosmopolitan distribution, absent only from South America as a breeding species but occurring even there on migration. It feeds exclusively on fish, catching them with a tremendous headlong dive in which it often completely submerges, throwing its feet forward at the last moment before entering the water so as to grasp the prey. The feet are specially adapted, with a spiny rough surface, for holding such prey. Where it is common it breeds in colonies, notably on the coasts of North America and on islands in the Red Sea. It is commoner on sea coasts but occurs also on inland lakes. It is frequently robbed of its prey by eagles of the genus Haliaeetus. In parts of the range it declined in the 1960s through pesticide poisoning. See photos AGGRESSION; FLIGHT. (L.H.B.) LN. Bent, A.C. 1937-38. Life Histories of North American Birds of Prey. New York. Brown, L. 1976. Birds of Prey: their Biology and Ecology. London. Brown, L. 1976. Eagles of the world. London. Brown, L.H. & Amadon, D. 1968. Eagles, Hawks and Falcons of the World. London.

HEARING AND BALANCE: senses here treated together because in both cases the sensory apparatus is in the ear. Ear. As with other vertebrates, the ear may be functionally divided into outer, middle, and inner parts. The outer ear of birds usually includes specialized feathers covering the opening of a short auditory canal. An enlarged ear funnel has developed in some species, especially the owls, and in some instances these ear funnels are movable. The ear funnels in owls are asymmetrical, aiding in sound localizations. The ear canal in some diving birds can be closed by muscle contraction. The middle ear cavity is composed of several cranial bones and this air filled cavity communicates with other air filled cavities of the skull. Thus, the middle ear cavities are not acoustically isolated from one another and sound impinging on the external surface of one typanic membrane is transmitted through the skull and affects the interior surface of the opposite tympanic membrane (Rosowski and Saunders 1980). This may provide a special mechanism by which birds with small heads can localize sounds in the frequency region of 1-8 kHz. Impedance matching from the tympanic membrane to the oval window is accomplished by the columella, extracolumellar cartilage, supporting ligaments, and middle ear muscle. The movements of the columella during sound stimulation are probably more complex than was earlier thought and may involve rotational forces. The inner ear of birds is a short, slightly curved tube consisting of three fluid filled cavities similar to mammals. The receptor surface, the basilar papilla, was first thought to contain a homogeneous cell population (Retzius 1884). Now it appears that a complex scheme exists consisting of tall, intermediate, and short hair cells which also differ on the basis of shape, cuticular plate dimensions, and innervation. Efferent nerve fibres form extensive networks from which many branches are given off to the hair cells. The basilar papilla is shorter and wider than the mammalian basilar membrane. There are no rods or tunnels of Corti and thus no division between inner and outer hair cells. As many as 40 hair cells can be seen across the width of the basilar papilla and it appears that the cilia may be more firmly inserted into the tectorial membrane than is the case in the mammalian cochlea. The scala vestibuli is not welldeveloped in birds and there is some question whether the two perilymphatic canals communicate by means of a helicotrema, as is seen in mammals. The size of the helicotrema influences low frequency sensitivity in mammals and the lack of a similar structure in birds may provide a mechanism for enhanced sensitivity to low frequency sounds. Hearing. Birds as a group hear best in the frequency rage of 1-5 kHz. Within this range, absolute sensitivity approaches the levels reported for man. Sensitivity declines dramatically for frequencies above this range and most birds show a high frequency hearing limit of about 10kHz. Owls show slightly better high frequency sensitivity with a hearing limit around 12kHz. Even those birds which are known to echolocate utilize signals in the frequency region of 2-8 kHz (Konishi and Knudsen 1979). Below 1kHz sensitivity decreases gradually but there is evidence in some birds (Rock Dove Columba livia) of a special sensitivity to infra-sound. Since infra-sound travels great distances, it is hypothesized that sensitivity to these sounds may aid in navigation. Discrimination of acoustic signals by birds is of considerable interest due to their use of complex vocal signals. Within the frequency region of 1-5 kHz, birds are almost as sensitive as man to changes in the frequency, duration, or intensity of simple pure tones (R. Dooling 1982). On more sophisticated measures of frequency resolving power such as masking, at least one species (Budgerigar Melopsittacus undulatus) consistently out-

Heart

performs man. It may be that the auditory system is especially tuned to complex acoustic signals in this frequency region. On several measures of temporal resolving power, birds have shown levels of sensitivity similar to those reported for other mammals, suggesting that the bird ear may not be specialized for a high speed of response as once thought. Sound localization abilities in 0~71s and other avian predators are extremely well-developed both in azimuth and elevation (Knudsen 1980). The cues for sound localization in these species are interaural arrival time and interaural spectrum. For common bonds with un specialized auditory systems both the cues and the mechanisms for sound localization are less clear. Behavioural studies indicate that birds localize high and low frequencies better than mid-range frequencies and broad band noise better than pure tones. The complexity of avian vocalizations probably provides a rich source of potential cues for sound localization and it is clear that birds can and do localize the sounds of conspecifics. But the existence of an interaural pathway in birds suggests that the mechanism for sound localization in birds is considerably different from that used by man and other mammals. Balance. As with other vertebrates, the three semi-circular canals lie in nearly orthogonal planes and function to indicate the angular motion of the head. The receptors of the superior division of the labyrinth consist of the ampullary crests, utricular macula, and the papilla neglecta. The inferior division, in addition to the basilar papilla, consists of the saccular macula and the lagenar macula. No data are available on the function of this complex system but common observation of the flying skills of most birds would suggest a highly developed system with a short time constant. Differences in labyrinth structures across species do indeed show a correlation with flying ability. (R.].P.) R.].D.

277

Rosowski, J. J. & Saunders, J. C. 1980. Sound transmission through the avian interaural pathways. J. Compo Physiol. 136: 183-190. Schwartzkopf, J. 1963. Morphological and physiological properties of the auditory system in birds. Proc. XIIIth Int. Orn. Congr., Ithaca, N.Y., 1962: 1059-1068.

Dooling, R.J. 1.982. Auditory perception in birds. In Kroodsma, D. & Miller, E. (eds). Acoustic Communication in Birds, vol 1. New York. Knudsen, E.!. 19~0. Sound localization in birds. In Popper, A.W. & Fay, R.R. (eds). Comparative Studies of Hearing in Vertebrates. New York. Konishi, M. & Knudsen, E.!. 1979. The oilbird: hearing and vocalization. Science 204: 425-427. Pumphrey, R.J. 1961. Sensory organs: hearing. In Marshall, A.J. (ed.). Biology and Comparative Physiology of Birds vol. 2. New York. Retzius, G. 1884. Das Gehororgan der Wirbelthiere. Stockholm.

HEART: in its pericardial sac the heart occupies the cranial part of the thoracic cavity, its apex pointing caudoventrally. Its pulmonary surface (or base) lies below the lungs, trachea, and proventriculus. The dorsal ventricular portion of the heart lies against the liver. Nearly its entire ventral aspect rests on the body of the sternum. Surface features (Fig. 1). The heart consists of cardiac muscle (myocardium) invested with the shiny layer of epicardium; its lining of endocardium is continuous with endothelium of vessels entering and leaving the heart. The grooves between the heart chambers are often obscured by subepicardial fat (Fig. IA). The cone-shaped heart is truncated in some species, elongated in others. The wide cranial end of the .heart is formed by the two atria and their ear-shaped appendages, the auricles. The pulmonary trunk and the ascending aorta intervene between the atria. The coronary sulcus separates atria and ventricles. The shallow ventral interventricular (I-V) sulcus extends obliquely between the short right ventricle and the longer left ventricle and is continuous with the dorsal I-V sulcus of the hepatic surface of the heart. . Skeleton ~nd musculature. The skeleton of the heart is composed of rmgs (annuli) of fibrous connective tissue that surround the atrioventricular (A-V) openings (ostia) and the openings of the aorta and pulmonary trunk. The annuli support the cusps of the valves of these ostia and prevent collapse of the ostia during valve closure. The annuli serve as origin and insertion of atrial and ventricular myocardium. The smooth-walled parts of the atria are thin; the thicker rib-like pectinate muscles of the auricles stand out in relief. Certain pectinate muscles coalesce into prominent median and transverse arches. The bundles of ventricular myocardium sweep spirally from the annuli toward the apex then back toward the bases of the ventricles. This arrangement causes the wringing of the ventricles during their contraction. Ventricular walls are much thicker than those of the atria. Heart chambers. The adult heart of some birds (ratites) retains the foetal heart chamber, the sinus venosus. The three caval veins empty into

Fig. 1. Heart of the goose, Anser. (From Ghetie et al 1976). (A) Dorsal aspect of heart and great vessels. Upper half of figure is the base or pulmonary surface. Note that the right cranial vena cava has a greater ca~lbre tha? the. left, reflecting the greater dimensions of the right jugular vem prevailing m most birds. 1 ascending aorta; 2 aortic arch; 3,4 brachiocephalic aa.; 5,6 common carotid aa.; 7 pulmonary trunk and aa.; 8 right cranial vena cava; 9 caudal vena cava; 10,11 pulmonaryaa.; 12 left cranial vena cava; 13 right atrium; 14,15 left and right auricles; 16 coronary (atrioventricular) sulcus covered with fat; 17,18 left and right ventricles.

(B) Sternal surface of heart and great vessels, right ventricle opened. 1 asce.nding aorta; 2 aortic arch; 3,4 brachiocephalic aa.; 5 pulmonary aa.; 5.' ostium o.fpulmonary trunk; 6 right cranial vena cava; 7 right auricle; 8 nght ventricle; 9 interventricular septum; 10 right atrioventricular valve (muscular); 11 left ventricle; 12 valve of pulmonary trunk; 13 trabeculae carneae.

278 Heart

this chamber which communicates with the right atrium via the slit-like sinu-atrial (S-A) opening. In other birds (e.g. Gallus) the sinus receives only two caval veins, the left cranial vena cava emptying directly into the right atrium. In most birds that have been studied the three caval veins open individually into the right atrium (Fig. lA); no definitive sinus venosus is present. Most of the foetal sinus becomes incorporated into the right atrium; remnants of the S-A valve persist. The right atrium receives venous blood from all parts of the body and the heart wall itself. The inflow ostia of the right atrium are those of the huge caval veins (or sinus venosus) and the cardiac veins; the single outflow opening is the right A-V ostium. The main part of the interior of the right atrium, including the interatrial septum, is smooth-walled and communicates with the subchamber of the auricle. Another feature of the interior is a cul-de-sac, the left recess of the right atrium. The right ventricle is short and wide. The entrance of the right ventricle is equipped with the right A-V valve, a crescent-shaped muscular fold with its free edge projecting into the ventricle. During ventricular contraction (systole) the valve clasps the interventricular septum, preventing regurgitation of blood into the atrium. Blood entering the ventricle passes apically, then flows into the conus arteriosus, the funnel-shaped subchamber of the right ventricle. Its outflow opening is the pulmonary trunk, where the pulmonary valve is located. Blood then travels via the pulmonary arteries to the lungs for aeration. The avian I~V septum is a curved partition between the ventricles; almost two-thirds of the circumference of the left ventricle is enveloped by the free wall of the right ventricle (Fig. 1). The left heart receives blood from the lungs and propels it throughout the arterial tree to all parts of the body. The paired pulmonary veins (Fig. l A) enter the left atrium independently ot become confluent (Fig. 1). The cavity of the left atrium is partitioned by a transverse fold known as the valve of the pulmonary vein, which directs blood into the left A-V ostium. The left ventricle forms the apical one-third of the heart. Its wall is 2-3 times thicker than that of the right ventricle, reflecting its function as a high pressure pump. One or more papillary muscles project from the wall of the left ventricle. The left A-V ostium is rounded in contrast to the semilunar one of the right A-V ostium. The left A-V valve differs from the right one in that its two or three cusps are membranous. The cusps are restrained by tendinous cords from the papillary muscles or ventricular wall. The vestibule of the aorta lies between the septal cusp of the valve and the interventricular septum and leads to the outflow channel, the aorta. Blood supply and drainage. The right and left coronary arteries originate from the aortic sinuses, enlargements at the base of the aorta, just distal to the aortic valve. Ordinarily each coronary artery divides into superficial and deep rami. Unlike the mammalian heart, most of the blood to the myocardium of the avian heart is distributed via deep rather than surface arteries. The superficial rami course in the coronary sulcus, supplying atria and ventricles. The deep rami course within the I-V septum, gradually inclining toward the surface. The major venous trunks course just beneath the epicardium; generally the veins do not accompany coronary artery branches. The smallest cardiac (luminal) veins carry some of the myocardial blood directly into the heart chambers. Conducting system. The cardiac conducting system initiates and carries the impulses that bring about the co-ordinated contraction sequence of the heart muscle required for pumping blood through the pulmonary and systemic circuits. This impulse-conducting system is derived from transformed cardiac muscle cells (or fibres), and forms impulse-conducting chains. The terminal network is partly subendocardial and partly periarterial around branches of the coronary arteries. The terminal rami branch further, ultimately becoming contiguous end-toend or side-to-side with contractile myocardial cells. The cardiac impulse is automatically generated in the nodal tissue, then transmitted over the bundles, branches, and terminal rami. The rami excite the myocardial fibres, bring about their contraction, the wave of excitation passing to adjacent myocardial fibres. Cell-to-cell transmission is electrical, conducted from one cell to the next over nexuses (gap junctions), low resistance zones of continuity between adjacent cells. The compact S-A node ('pace-maker') is located in the right atrial wall somewhere near the apical end of the right S-A valvule or its vestige. The A-V node is embedded in the caudodorsal part of the interatrial septum. The A-V node continues apically as the A-V bundle of His which enters

the I-V septum and divides into its right and left crura that travel on each side of the septum. From the region of its bifurcation the A-V bundle gives off its Ramus recurrens (truncobulbar fasciculus). The ramus then joins the ventral extremity of the right A-V annulus. Here the truncobulbar node is reported to be present in adult heart of Gallus. The right A-V annulus courses in the right A-V valve; its dorsal extremity arises directly from the A-V node. Atrial musculature is not continuous with ventricular musculature. Both are 'insulated' from one another by attachment to the nonconducting skeleton of the heart. The only direct connections between the two muscle groups are by way of the bundles of conducting tissue. Heart innervation. The innervation to the heart modulates the activity of the conducting tissue. The most densely innervated regions of the avian heart are the S-A node, right atrium, and the A-V node. The periarterial and subendocardial conducting tissue of the ventricles also receives a double innervation of interacting (autonomic) nerves. In general the cholinergic vagal efferent nerves produce effects that slow the heart beat. On the other hand, the thoracolumbar (sympathetic) adrenergic nerves from the lowest of the cervical paravertebral ganglia accelerate the beat. The vagal afferent fibres are involved in cardiac reflexes. The direct innervation of the heart muscles probably modifies their response to stimulation from the conducting system, adrenergic innervation enhancing the force of their contraction and cholinergic innervation the reverse. Coronary arteries also receive a double innervation of noradrenergic and cholinergic fibres for regulation of coronary blood flow. Heart size. The weights of avian hearts, as a percentage of body weight (B.W.), range from 1.4--2 times larger than mammals of comparable size. Species living at high altitudes have larger hearts than the same species at lower altitudes. The ratio of heart size to body weight is significant for flight, i.e. birds with large hearts but only modestly developed flight muscles can fly for long periods. Thus, although the tinamous (Tinamiformes) have powerfullimb muscles and extremely large flight muscles, they are capable only of explosive flight over short distances. Their hearts are relatively the smallest of all birds (0.19-0.25% of B.W.), which appears to limit prolonged flight effort. Compare this with flying abilities of pigeons (Columbidae) whose flight muscle weights are equivalent to those of tinamous while the heart ratio is greater (0.93-1.29% of B.W.). Since the avian heart rate is so high (see below) the relatively large heart in birds may provide the means for quickly increasing heart output by utilizing the reserve portion of the blood not ejected from the ventricles at each beat during moderate activity. Large hearts requiring a relatively reduced degree of muscle shortening may facilitate adequate filling of the chambers at the high rate prevailing in birds. Heart rate. Normal heart rates for resting birds (e.g. pigeon, chicken, duck) range from 150-350 beats per min. The resting rate in the ostrich (Struthio) is 60--70 per min, in a small passerine (Black-capped Chickadee Parus atricapillus) 500 per min, in hummingbirds (Trochilidae) up to 1,000 per min. During excitement, stress, or sustained flight the above rates more than double. For example, during flight the heart rate of small birds (10--20g) is 2.4 times that at rest; in large birds (500-1,000 g), the flight rate is 3 times resting rate. In diving birds the heart rate is slowed reflexly about 50% during the dive. Some coupling of heart rate to wing beat frequency in flight has been observed: in some forms 1 : 1, in others 1: 2. It has been suggested that the pectoral muscles of small birds in flight may operate as a venous pump in order to maintain adequate venous return to the heart, compensating for high cardiac output. (E.T.B.F.) J.J.B. Akester, A.R. 1971. The blood vascular system. In Bell, D.J. & Freeman, B.M. (eds.). Physiology and Biochemistry of the Domestic Fowl. vol. 2, pp. 783-839. London. Baumel, J.J. 1971. Aves. Heart and blood vessels. In Getty, R. (ed.). Sisson & Grossman. The Anatomy of the Domestic Animals, vol. 2. Philadelphia. Baumel, J.J. 1979. Systema cardiovasculare. In Baumel, J.]', King, A.S., Lucas, A.M., Breazile, J .E. & Evans, H.E. (eds.). Nomina Anatomica Avium. An Annotated Anatomical Dictionary of Birds. London. Ghetie, V., Chitescu, St., Cotofan, V. & Hillebrand, A. 1976. Anatomical Atlas of Domestic Birds. Bucharest. Jones, D.R. & Johansen, K. 1972. The blood vascular system of birds. In Farner, D.S. & King, J.R. (eds.). Avian Biology, vol. 2. London.

HEATH FOWL: antique term (in British game laws) for Black Grouse Tetrao tetrix-contrasted with 'Moor Fowl' for Red Grouse Lagopus

Heat regulation

279

Ostrich Struthio camelus showing exposed bare skin to reduce heat , sexual dimorphism and male giving distraction display. (P hoto: J .F. Reynolds).

lagopus scoticus (see

GROUSE) .

HEA TH HEN: name of the now extinct nominate race of the Greater Prairie Chicken Tympanuchus cupido (see GROUSE; EXTIN CT BIRDS). HEAT REGULATION: also called thermoregulation; the process by which a bird maintains a stable body temperature, irrespective of variations in the surrounding temperature. Birds are endothermic animals (= warm-blooded or homoiothermic ), that maintain a high body temperature of 40 ± 2°C. Their body heat is generated metabolically by the oxidation of absorbed nutrients (see METABOLISM) and accounts for a large proportion of the total energy metabolized by the body. Apart from species that can go torpid (see TORPIDITY) body temperature shows only a small daily variation; in diurnal birds the daytime core temperature may be 42°C, dropping to 39cC at night ; in nocturnal birds the cycle is reversed . In an inactive bird metabolic heat production is normally never less than the Basal Metabolic Rate (see ENERGETICS ) and when the bird is active it may be much more. To maintain a stable body temperature it is necessary that heat production is balanced by heat loss. At low to moderate ambient temperatures this is achieved mainly by conduction and radiation and at high temperatures by the evaporation of water. The rate at which heat is lost by conduction and radiation is proportional to the temperature difference between the body core and the outside, thus Rate of heat loss = C(T body - Tambient)' where C represents the heat conductance (Joules ·sec - l ·cm- 2 . cC -' ) of the body and plumage (its reciprocal is the insulation ). Over a range of ambient temperatures known as the thermoneutral zone the heat production of an inactive bird is able to remain constant at the Basal Metabolic Rate, because changes in ambient temperature, which would alter the rate of heat loss, are compensated by changes in the thermal conductance (or insulation) of the body. By a complex neuromuscular arrangement connecting adjacent feather follicles, the ptilomotor system, a bird can fluff out its feathers to their maximum extent, so trapping a greater amount of still air between them and greatly increasing the insulation value of the plumage . Conversely, the feathers can be sleeked back to

increase the conductance. Birds may also make postural changes to alter heat loss; to reduce heat loss the face may be hidden under the scapulars and the feet withdrawn up into the feathers, or (especially on ice or in water) the bird may stand on one leg. Heat loss through the feet may be reduced by an arrangement of the blood vessels in the upper leg that acts as a counter-current heat exchanger. Warm arterial blood from the body passes through fine arteries in close contact with the veins returning cold blood from the feet. The venous blood is thus warmed before it can return and cool the body, while the arterial blood is cooled before it can lose its heat to the exterior . A gull with its feet in ice water may lose only I. 5% of its metabolic heat through its feet because of the efficiencyof the heat exchange. Even so the feet cannot be allowed to freeze; below freezing point additional heat is supplied to the feet to prevent freezing and heat loss is therefore increased . If the insulation is already maximized, but the ambient temperature drops still further, heat loss increases in proportion to the increasing temperature difference (T, - T a) . A stable body temperature can then be maintained only by increased heat production in the body core. The ambient temperature at which this occurs is the lower criticaltemperature and marks the lower end of the thermoneutral zone. It is generally much lower in well-insulated Antarctic and Arctic species (and hence the thermoneutral zone is wider) than in temperate or tropical birds. The lower critical temperature may vary seasonally in some species, being lower in winter than in summer. The lower winter value may be due to a better insulating plumage, or a higher basal heat production, or both (see ENERGETICS ). As ambient temperature decreases, metabolic heat production increases more rapidly in poorly insulated tropical species than in well-insulated Arctic ones. Small birds are doubly disadvantaged because their size preven ts them from carrying as thick a plumage as large birds, as well as requiring them to increase their heat production more rapidly with falling temperature, since the area of the body surface, through which the heat is lost, is proportionately greater than the volume of the body core, where heat is produced . All species, however, are eventually limited by the maximum additional metabolic heat that they can produce. The maximum heat production determines the minimum ambient temperature below which hypothermia and death result .

280

Hedgesparrow

At high ambient temperatures heat may be lost by increased blood circulation to the periphery, particularly to the legs and to any bare, well-vascularized patches of skin. The wings may be partly spread, e.g. in coursers, allowing radiation from the sparsely-feathered under surface of the wing. Incubating birds, e.g. plovers, may sit with their backs to the wind and raise the mantle feathers, allowing the wind to break the insulating boundary layer of air trapped in the plumage. However, as ambient temperature approaches that of the body, conduction and radiation become less effective at dissipating heat and cooling by the evaporation of water becomes increasingly important. Since birds do not possess sweat glands, water is usually evaporated through the respiratory tract, where the rate of evaporation is greatly increased by panting or, in some non-passerines, by gular flutter, a rapid oscillation of the thin floor of the mouth and upper throat. Nevertheless among birds, unlike mammals, evaporative water loss at high ambient temperatures rarely dissipates more than half the total heat production. Some species, e.g. incubating Fairy Terns Gygis alba, reduce heat production by slowing the heart rate and reducing the basal metabolic rate. Others, particularly some desert birds, e.g. the American Mourning Dove Zenaidura macroura, allow the body temperature to rise above normal to 45°C, thus re-establishing a temperature gradient to their surroundings so that heat loss by conduction and radiation can continue. The temperature at which this occurs is the upper critical temperature and marks the upper limit of the thermoneutral zone. Where the environment is hotter than body temperature, the bird absorbs heat. Small birds are again at a disadvantage compared with large ones; they already have a high basal metabolic heat production and their surface area being large relative to body volume causes them to gain heat faster from their surroundings. Small birds seek shade to lessen the heat intake from solar radiation and large soaring birds take to the wing to reach cool air at high altitude; but birds can cope with heat stress only for as long as they have an adequate supply of water that they can evaporate fast enough. Some large birds may even excrete down their legs to provide an additional site for evaporative cooling. The capacity for evaporative cooling determines the ambient temperature at which body temperature begins to rise (the upper critical temperature). As hyperthermia proceeds, the metabolic heat production, which is temperature dependent, also increases, resulting in an explosive heat rise and death at body temperatures of 4&-48°C. See photos BELLY SOAKING; ENERGETICS; INCUBATION. P.}.}.

HEDGESPARROW: name (misnomer), alternatively 'Dunnock', of

Prunella modularis (see ACCENTOR).

HEEL PAD: a callosity behind the intertarsal joint in nestlings of some piciform and other birds (see

LEG).

HELIGOLAND TRAP: see

BIRD OBSERVATORY; TRAPPING.

HELIORNITHES; HELIORNITHIDAE: see under GRUIFORMES; FINFOOT.

HELL-DIVER: popular American name for the Pied-billed Grebe

Podilymbus podiceps (see GREBE).

HELMET: an ornament, usually composed of feathers, on the top of the head, as in helmet-shrikes (Prionopinae)---compare CASQUE. HELMETBIRD: Euryceras prevostii (see VANGA). HELMETCREST: Oxypogon guerinii (for family see

HUMMINGBIRD).

HELMET-SHRIKE: substantive name of most species ofPrionopidae

(Passeriformes, suborder Oscines); in the plural general term for the family; formerly considered a subfamily of the shrikes (Laniidae) by Rand (1960). The helmet-shrikes, all endemic to the Afrotropical region, have bills that are hooked and notched near the tip, similar to the true shrikes (Laniidae). The wing has 10 primaries and the tail 12 rectrices. Legs and feet are strong and claws sharp for catching prey. Lengths range from 18-25 em. They are unusual in having a tarsus scutellated on both side and front, and most species have specialized head feathering and eye-wattles that are distinctively coloured. The feathers on the forehead are stiff and project forward, covering the nostrils. Two genera

Common Helmet-shrike Pnonops plumata. (M. W.).

are recognized, following Hall and Moreau (1970), Prionops (7 species) and Eurocephalus (2 species); others place some species of Pnonops in a separate genus Sigmodus, and place Eurocephalus in the Laniidae. The sexes are alike. Field characteristics, habitat and distribution. The species of Prionops fall into two groups, 3 black-billed species and 4 red-billed. Of the black-billed species the Common Helmet-shrike Prionops plumata has the widest distribution in savanna and light woodland throughout the Afrotropical region; 5 races are recognized by Hall and Moreau. It is a black, grey and white bird, with orange eye-wattles. The Grey-crested Helmet-shrike P. poliolopha differs from it in having no eye-wattles and replaces it in the Kenya highlands and in drier areas further south. The Yellow-crested Helmet-shrike P. alberti, closely related to poliolopha, is confined to land above 1,400 m in the eastern Congo and is wholly black with a yellow crest and orange eye-wattle. Of the red-billed species one, the Red-billed Shrike P. caniceps, is restricted to the West African and Congo forest block. It has a black back, throat and tail, whitish head and white and chestnut underparts, but no eye-wattle. Another, the smallest of the family, is the Chestnutfronted Helmet-shrike P. scopifrons (length 18em) which has a blue eye-wattle and is confined to a narrow forest belt along the eastern sea-board of Africa. The White-crowned Shrikes, Eurocephalus anguitimens and E. rueppelli, sometimes considered conspecific, are brown and white and inhabit acacia steppe in southern Africa and north-eastern Africa respectively. Their white heads and rumps are conspicuous in flight which resembles that of a large butterfly. Movements. There are no ringing data to confirm the presence or absence of movements; observations suggest that local movements may occur in some populations of the Common Helmet-shrike. Food. Helmet-shrikes search trunks, branches and leaves mainly for insects, each species foraging systematically in a group much like tits. Behaviour. All species are intensely sociable, occurring in groups numbering &-12 birds or more, throughout the year. Nothing is known about the permanency of the pair bond. Only the Common Helmetshrike has been studied using colour-ringed birds. All group members co-operate in nest-building, incubation and feeding young; in addition, clumping and allopreening occur. A group normally has only one active nest used by one female but occasionally (8 cases in 225 recorded in Zimbabwe) 2 females may lay complete clutches in the same nest; pairs sometimes nest close to each other in neighbouring trees. In Retz's Red-billed Shrike P. retzii some pairs (1 in 36 recorded in Zimbabwe) breed alone. The 2 Eurocephalus species appear to breed only in pairs, although outside the breeding season they are found in groups of up to 10 birds. Group territorial defence and predator attack have been recorded in the Curly-crested Helmet-shrike P. cristata and may be common to the genus. Helmet-shrikes are often accompanied by other bird species when feeding. Their flight is buoyant, much like jays, and they are usually silent on the wing.

Heraldic birds

Voice. Although helmet-shrikes have a variety of calls, of which the most frequently listed are repeated whistles or flute-like notes, they are usually located in the field through the noisy chattering of a mobile flock. In addition, bill snapping is characteristic of the group. Breeding. The nests of the helmet-shrikes are inconspicuous but neatly formed shallow cups, either secured to a horizontal branch or placed in a fork of a tree or thicket from 2-7 m above the ground. Materials used include tendrils, spider webs, lichen, rootlets, grass and bark fibre. The normal clutch is 3 or 4; eggs have a range of ground colours, variously described as white, greyish-white, pale blue grey, blue, greenish blue, and pale pinkish. The eggs are either streaked, speckled or blotched with various shades of brown, purple-brown and chestnutbrown, the markings being concentrated usually at the large end. Incubation periods are in the range 12-14 days, nestling periods in the range 16-20 days. The breeding seasons are prolonged and overlap both the dry and wet seasons. L. G.G. Hall, B.P. & Moreau, R.E. 1970. An Atlas of Speciation in African Passerine Birds. London. Rand, A.L. 1960. Family Laniidae. In Mayr, E. & Greenway, J.C. Jr (eds.). Check-list of Birds of the World, vol. 9.

HELPERS AT THE NEST: see

CO-OPERATIVE BREEDING.

HEMIPODE: alternative substantive name of species of Turnicidae and Pedionomidae, and also used as a general term for the suborder Turnices (see BUTTONQUAIL; PLAINS-WANDERER). HEMIPROCNIDAE: see

APODIFORMES; SWIFT.

HEMISPINGUS: substantive name of South American the genus Hemispingus.

TANAGERS

of

HEN: a female bird; applied without qualification to the female of the domestic fowl (compare COCK). Special terms apply to the females of some species, e.g. PEN, GREYHEN, PEAHEN, REEVE. The names of certain species have also a special use as terms for the female, e.g. DUCK, GOOSE, FALCON; but note that in North America the female of any duck species is the 'hen'. HERALDIC BIRDS: avian symbols used as charges in armorial

bearings. In heraldry the animals fall into roughly the same classes as in zoology, but with the addition of heraldic monsters. The four main classes are beasts, monsters, fishes, and birds. Most books on heraldry deal fairly fully with beasts; monsters can be studied in the many excellent beastiaries and books of monsters; Thomas Moule's Heraldry of Fish (1842) is the last word on that subject; but birds have been neglected. It is, therefore, particularly pleasant to be able to remedy here, if only in some slight measure, this deficiency. Heraldry is a form of hereditary personal symbolism in which the basic medium for the display of the devices used is the shield. It is European in conception and application, just post-Conquest in time of origin and, to a great extent, dependent for much of its early symbolism and many of its conventions on the Crusades, jousts, and tournaments. Two symbols are used, the arms borne upon the shield and the crest. The crest is a device which was originally modelled on top of the helmet and which, together with the mantling which flows from it, is often shown in pictorial representations of arms. That heraldry was from its inception at once utilitarian and also pictorial and decorative accounts for the fact that crests are often absurdly impracticable and could never have been in actual use, but only engraved upon seals and otherwise used pictorially. It is not surprising that birds are to be found in early heraldic symbolism, when it is considered how frequently they appear in more ancient symbolisms. The eagle on the standard of a Roman legion is well known; perhaps less familiar in this regard is the owl, which in a most heraldic form graced the reverse of an Athenian tetradrachmon minted about the time of the Persian Wars. In Christian symbolism the dove holds pride of place as a symbol of the Holy Spirit and His attributes of peace (see also ART, BIRDS IN). If only for this reason, it has always been a favourite heraldic charge, whilst the pelican as a type of Christ is popular in the heraldry of ecclesiastics. In early heraldry she is often drawn more like an eagle, and is almost invariably depicted 'in her piety', i.e. on a nest and pecking her breast to

281

feed her young with her own blood. The ongm of this fable of self-wounding may lie in the habit of resting the pouched bill upon the breast. A well-known example of the pelican in heraldry occurs in the arms of Richard Foxe, Bishop of Winchester, Azure a Pelican wings elevatedand addorsed Or vulning herselfproper. Foxe, who died in 1528, founded Corpus Christi College, Oxford, in 1515, and his arms still form part of the cumbersome coat borne by his foundation. An early arrival in the heraldic aviary was the martlet. This bird has always been shown sans legs and looking perhaps rather more like a fat swallow than anything else. Indeed, to preserve the obvious pun, it is described as an hirondelle (swallow) in the arms of Arundell (Sable six hirondelles 3, 2, and 1 Argent): variants of these arms are used by both the East Sussex and West Sussex County Councils. Most heraldic writers state that 'martlet' is a synonym for 'martin' , a bird which has such short legs that it relies upon them but little, and is therefore always depicted heraldically without legs, albeit it is almost invariably shown 'close' and not in flight. Other writers assert that it represents a swift, for these birds are found in great numbers in the Holy Land and crusaders may have come to associate these elegant yet sturdy (and apparently legless) creatures with their own exploits in the Near East and adopted them as symbols of speed and endurance, as well as a reminder to others that the bearers had fought for the Faith. It is amusing to note that the martlet is used to denote a fourth son in heraldry. The story is that the first son inherited, the second became a soldier, and the third entered the church; but for the fourth there was nothing, so he flew away to seek his fortune. That the martlet is of great antiquity in heraldry is borne out by its presence in a great many of the coats depicted in 'Glover's Roll' (c. 1255). It was a common mediaeval practice to show in arms not only military but also sporting symbols. Thus one finds hunting horns, greyhounds, and, of course, hawks. These last are usually shown belled and jessed, and sometimes hooded. The hawk is drawn in a somewhat stylized way and indifferently called a 'hawk' or 'falcon', except where a pun is required or where for some special reason a particular species was chosen for a charge. Then the hawks may be found looking much like any other, but blazoned a 'goss-hawk', 'sparrowhawk', 'gerfalcon', 'marlion', or 'hobbey'. See also FALCONRY. The birds so far mentioned are to be found in heraldry principally owing to the qualities which they symbolize. Very many other kinds of bird grace armorial bearings, but principally because they pun on the name of the bearer of the arms. There is no need to mention what birds are to be found in the arms of Larkins, Bustard, Sparrow, Hancock, Cobbe, and Storke, to mention but a few. Whilst it is often apparent why a certain bird appears in a certain coat of arms, as the pheasant which is found in the crest of the Worshipful Company of Cooks, this is not always the case. In 1550 one William Strickland, of Yorkshire, was granted arms and a crest, the latter consisting of A Turkey Cock Argent beaked and legged Sable combed and wattled Gules. The reason for this grant is that William Strickland was said to have introduced turkeys into England from North America; the sketch which is part of the docquet of this grant must therefore be one of

Fig. 1. Pelican; in the arms of Richard Foxe (as Bishop of Bath and Wells), from College of Arms Ms. L. 10.

282 Herbst's corpuscles

HERMIT THRUSH: Catharus guttatus, a North American THRUSH, noted for its outstandingly beautiful song. HERN; HERNSHAW: obsolete or dialect names, in Britain, for the

Heron Ardea cinerea-the latter variously spelt, including 'handsaw' in Shakespeare.

HERODIONES: see

Fig. 2. Turkey; an early drawing in the records of the College of Arms. the first ever made of a turkey in Britain-indeed, one look at the sketch lends support to this view! The arms of the Worshipful Company of Musicians are full of royal emblems, and this might suggest that the swan in the arms is a royal swan; however, the reason for its appearance is almost certainly an allusion to the legend that the soul of Apollo, the god of music, passed into a swan when it was at the point of death, thus enabling the bird to sing a beautiful song before it died. The swan deserves particular mention as it was the famous badge of the powerful family of Bohun, Earls of Hereford and Essex, and the crest of the Beauchamps, Earls of Warwick, and from these families it percolated through to many others. Why these and other families adopted the swan is uncertain. It has been suggested that the reason is to be found in the fact that they can all trace descent from the house of Boulogne, connected in legend with the Knight of the Swan. This theory is carefully examined by A.R. Wagner in his essay 'The Swan Badge and the Swan Knight' (Archaeologia 97: 127). It is interesting to consider how legend and romance were mirrored in an heraldic charge which, because it was adopted by one or two powerful families, soon found its way into the heraldry of smaller families, as representing either consanguinity with, or feudal dependence upon, these early magnates. Although birds are seen to best advantage as crests and charges in arms they are also used as supporters. It is a privilege of peers and certain grades of knight to have supporters on either side of the shield. Although a bird is a rather unsteady supporter, compared with a beast or a human being, it is becoming increasingly popular. Birds have become increasingly popular as heraldic charges and particularly as crests during the present century. Although unspectacular birds frequently appear, they are not so popular as the more exotic breeds; unornithological Kings of Arms tend not to distinguish between, say, a blackbird, thrush and starling. Thus if a starling is granted as a crest, someone wanting a thrush will be unlucky as it will be dubbed 'the same sort of bird'. A glance through the recent grant books at the College of Arms has revealed hummingbirds, albatrosses, many cormorants, a rockhopper penguin, a Canada goose, many red cardinals, moas and sedge warblers. When the Zoological Society of London was granted arms in 1959, it was desired to represent different classes of creature. Therefore, to the principal charge of a lion were added two zebra as supporters (Lord Zuckerman's idea) and a crest consisting of an osprey with a fish in its talons, as suggested by Sir Landsborough Thomson, and effected by the J.P.B-L. writer of this article.

HERBST'S CORPUSCLES: see HERD: see

TOUCH.

ASSEMBLY, NOUN OF.

HEREDITY: see

GENETICS.

HERITABILITY: the proportion of total variation in a population which is due to genetic causes (see GENETICS).

HERMIT: substantive name of species of HUMMINGBIRDS of the genera Ramphodon, Glaucis, Phaethornis and sometimes of Threnetes, so-called because of their generally sombre plumage colours.

CICONIIFORMES.

HERON: substantive name for most species of the Ardeinae (typical herons), one of 2 subfamilies of Ardeidae (Ciconiiformes); in Britain commonly used without qualification for the sale native species, the Grey Heron Ardea cinerea; in the plural, a general term for the Ardeinae and the Ardeidae. The substantive name 'egret' is used for several species. The other subfamily is the Botaurinae (see BITTERN). The Boat-billed Heron Cochlearius cochlearius was previously placed in a separate family. Characteristics. Herons are medium to large birds, ranging from the Zigzag Heron Zebrilus undulatus, 30 em long, to the Goliath Heron Ardea goliath, 140 em long. Particularly in the day herons, the body is slender and neck and legs relatively long. Night herons are stouter with shorter necks. Long-necked herons keep their heads retracted in prolonged flight. A kink in the neck is caused by the structure of the relatively long sixth cervical vertebra. Toes are long and slender; the inner toe IS shorter than the outer and is attached to the middle toe by a short basal web; the hind toe is lengthened and level with the inner toe; a pectinated middle toe nail is used for grooming. Bill structure ranges from very long and thin in the Chestnut-bellied Heron Agamia agami, to broad and thickened in the Boat-billed Heron. The tail is short, usually with 12 rectrices. Wings are long, broad, with 10 primaries, 9 in the Boat-billed Heron. Flight is slow but strong. Herons assume an erect or semi-crouched posture when active and retract their neck when resting. The plumage of herons is loose, the basic colours emphasizing black, brown, blue, grey, and white. Colour patterns may be complex, especially in cryptic species. The head is completely feathered except the lares. Some species, especially day herons, have lanceolate or filamentous display plumes on their head, neck, breast, or back. Sexes of most species are alike in plumage, but polymorphism occurs in several. Down is confined to apteria; feather tracts are extremely narrow (see PTERYLOSIS). Powder-down patches, characteristic of herons, occur in pairs on the breast and rump. Additional pairs are located on the back and thighs of some species. Powder down is used during preening (see COMFORT BEHAVIOUR). Moult and plumage development patterns are complex and variable, seasonally and with age. Juvenile may differ from adult plumage, the night herons being cryptically barred and the Little Blue Heron Egretta caerulea white. Habitat. Herons are adapted for walking about in water and are with ibises and storks often referred to by the descriptive name of wading birds. They characteristically inhabit shallow marshes and swamps, the shores of rivers and lakes. Small herons tend to frequent dense marshes; larger species tend to forage in the open. The amount of wetland habitat available directly influences population size. Terrestrial habitats are frequented by many typically aquatic species and used extensively by Cattle Egrets Bubulcus ibis and the Black-headed Heron Ardea melanocephala. Many species use shallow marine habitats, but several are marine specialists. Taxonomy and distribution. The Ardeinae are divided into 3 tribes, the tiger herons Tigriornithini, night herons Nycticoracini, and day or typical herons Ardeini. Herons as a group are cosmopolitan, but most species are tropical. The Tigrionithini are considered to be the most primitive group (but see Payne and Risley (1976)). The secretive and solitary tiger herons, including 6 species in 4 genera, 3 of which are monotypic, have a discontinuous apparently relict distribution. The New Guinea Tiger Heron Zonerodius heliosylus is confined to Papua-New Guinea. Its nearest relative, the White-crested Tiger Heron Tigriornis leucolophus inhabits the equatorial rain forest of West Africa. The Zigzag Heron, the least known ardeid, occurs in South America in forest pools and streams. The 3 Tigrisoma herons are Neotropical, occurring in swamps and along streams from Mexico to Argentina, with the Bare-throated Tiger Heron T. mexicanum confined to Central America. The Nycticoracini are medium-sized herons that typically, but not universally, feed at night. In general they are stockier, shorter-legged, and heavier-billed than day herons. The 8 species in 3 genera have

Heron

Black-crowned Night Heron Nycticorax nycticorax. (R.G.).

distinctive skeletal differences from the day herons. The 4 oriental night herons Gorsachius are PalaeotropicaL The Black-crowned Night Heron Nycticorax nycticorax is found on all continents but Australia and on many islands. It is replaced in Australia by the closely related Nankeen Night Heron N. caledonicus. The Neotropical Boat-billed Heron is distinguished by its peculiarly widened bill, 7.5 em long by 5 em wide, and by its exceptionally large eyes. It has diverged from other herons in its display repertoire and has 3 rather than 4 powder-down patches. It resembles night herons in plumage and frequently feeds at night. Some believe that the unusual bill primarily serves a display function. It seems more likely to be a feeding adaptation. The Ardeini include the well known, typically day-feeding herons and egrets. Many species nest colonially and forage in aggregations. The day heron group of 35 species is cosmopolitan. The little known Capped Heron Pilherodius pileatus has a distribution centred in the Amazon basin of South America. Considered in the past to be a night heron, taxonomic and field studies indicate it to be a typical heron, characteristic of forested stream edges. The Whistling Heron Syrigma sibilatrix has a disjunct distribution in northern and southern South America. Its whistling calls, duck-like flight, and complex social behaviour are distinctive. It is a bird of the tropical savannas. The pond herons Ardeola include 6 diminutive, short-legged Old World herons of shallow, reedy marshes. In several species breeding and non-breeding plumage differ markedly. The Cattle Egret is primarily a terrestrial heron that forages in commensal association with African buffalo, domestic cattle, other large animals, and even agricultural equipment. In Africa this mostly white bird favours seasonally-flooded plains. Both Indian and African races have expanded their ranges markedly within historic times, probably taking advantage of changing agricultural practices. The Cattle Egret had become established in South America by the late 1800s, in Australia by the early 1900s, and in North America and Europe by the early 1950s. The Green Heron Butorides striatus includes 3 small, dark herons previously considered to be separate species. The most distinctive population, on the Galapagos, includes individuals that are almost entirely dark grey. Green Herons are secretive, often foraging under the cover of trees along the shores of rivers and lagoons. The Galapagos form typically feeds on rocky shores. The genus Egretta includes 13 species, the medium sized white Little Egret E. garzetta of Europe, Africa, and Australia being typical. The Little Egret has a mainly inland distribution and breeds in mixed-species colonies. The Snowy Egret E. thula of North and South America is similar but has different breeding plumes. Two polymorphic reef herons E. gularis and E. sacra tend to replace the Little Egret along the coast in

283

Africa and in Asia to Australia, respectively. But see a recent discussion in The Herons Handbook (p. 132). Another similar heron, Swinhoe's Egret E. eulophotes, is now confined to China and Korea. Three New World forms are similar in habitats to the Old World reef herons. The Pied Heron E. picata has a patchy distribution in Australia to New Guinea. Two more occur in Africa, and the Intermediate Egret E. intermedia, larger than the Little Egret, has a discontinuous distribution from Africa and Asia to Australia. The Great White Egret E. alba is cosmopolitan, occurring in many habitats on all continents. The genus Ardea includes 11 species of medium to very large dark-plumaged herons. The Grey Heron and Purple Heron A. purpurea are widely distributed in Eurasia and Africa. The Grey Heron forms a natural, mutually allopatric, group with the North American Great Blue Heron A. herodias and the South American Cocoi Heron A. cocoi. The White-necked Heron A. pacifica replaces these species in Australia. The White-faced Heron A. novaehollandiae is a medium-sized species of Australia, which has been introduced and has spread in New Zealand. The African Black-headed Heron is characteristically terrestrial, feeding in cultivated areas and open grassland. Finally, there are 4 very large herons of allopatric distribution: the Malagasy Heron A. humbloti of the Malagasy Republic, the Goliath Heron of Africa and Asia, the Imperial Heron A. imperialis of South Asia, and the Sumatran Heron A. sumatrana from Malaya to Australia. The Agami or Chestnut-bellied Heron is a peculiarly attractive neotropica1species of uncertain affinity. It has a long neck and bill and brilliant dark green, chestnut, and pale blue plumage. It occurs along stream banks in deep forests. Populations. Over their known history many populations have been reduced by hunting and by habitat loss. Extensive surveys in North America have assembled information on nesting colonies in recent years. The Grey Heron is the best known species, colonies in the United Kingdom being tallied as early as 1872 and the nesting population of England and Wales being censused annually since 1928. The population decreases markedly after hard winters. Movements. Herons demonstrate several types of population movements. In temperate latitudes, regular seasonal migrations are undertaken by many species. Herons of the eastern Palearctic move toward Malaysia and Indonesia; western Palearctic herons migrate on a broad front to central Africa and also to India; Nearctic herons move to southern North America with eastern birds moving through Florida and western birds moving through Central America; southern African herons and southern South American herons undoubtedly migrate northward but their routes require additional study; Australasian herons appear to migrate as far north as New Guinea. Nearly all herons show postbreeding dispersals of juveniles, and of adults after nesting failure. Such dispersing birds may be moving from areas where food is scarce. Dispersals before migration bring many birds as late summer visitors to localities well away from their breeding range. Intra-regional movements, nomadic responses to seasonally variable food resources, have also been documented for various species. Food. Herons are almost entirely carnivorous, depending heavily on aquatic prey. Diets are broad and variable in time and place and reflect seasonal flushes of prey. Exploiting seasonal prey abundances is of critical importance to many populations, affecting nesting success, movements, migration, and food choice. The foraging behaviour of herons can be as simple as standing motionless in the shallows or at the water's edge until a potential prey approaches, as is typical of the largest and smallest species. Food is commonly sought by walking stealthily in the water or on dry ground, or by more active behaviours. A bird may combine walking with running or hopping in a repetitive sequence, as is characteristic of Reddish Egrets E. rufescens. Use of the feet is common, particularly in species with distinctively coloured toes. Aerial feeding methods are used by several species. Special wing actions characterize actively foraging species. The Black Heron E. ardesiaca, stands with its wings extended completely over its head forming a canopy that appears to attract prey and may increase their visibility. Prey are grasped or, less frequently, impaled by a quick thrust. Dead or slow-moving prey are grabbed or picked up. When bill thrusts are directed into the water, herons must compensate for refraction. Herons may tilt or cock their heads to improve visibility. Captured prey are mandibulated by bites or stabbing if they are large or possess counteradaptations such as spines, hard bodies, or violent post-capture be-

284 Herpetotherinae

haviour. Pellets of undigested material are disgorged. Smaller herons take longer to handle large prey, which may affect their choices. The New World Yellow-crowned Night Heron Nycticorax violaceus specializes in feeding on crustaceans. Most herons feed diurnally, but some species, e.g. the night herons, characteristically feed nocturnally or crepuscularly, while others, e.g. Great Blue Heron, may do so at times. Behaviour. Some herons, such as the tiger herons, are typically solitary; others forage in isolation but nest colonially. Some species, such as the Cattle Egret, feed in flocks and nest in large colonies. Others are socially flexible, and individuals may alternately feed alone or in an aggregation. Social foraging provides opportunities for complex interactions, including aggression, commensalism, competition, and prey robbing. Territorial behaviour on the feeding grounds is common, and individual territories may be occupied over long periods. Individual distances are always maintained. Many herons form mixed-species communal roosts in protected sites, often after assembling at staging locations. Nesting in groups on isolated sites confers some degree of protection. Herons may also use colony associates to obtain information on the direction of available food resources. Pair formation behaviours are varied and elaborate, including aerial and non-aerial elements. Pair-bonding begins at the colony, with intensive displays by males. Three types of pair formation are distinguishable. A succession of females may visit a displaying male at his future nest site (Grey Herons). Several females may visit a male on one or more temporary display sites (Cattle Egrets). Both males and females may move as a group around the colony (Little Egrets). A male typically initiates courtship by advertising calls, defends his site, and attracts a female with various displays. In many species lores, irides, bill, legs, or feet change colour during courtship. Often the colour remains for only a few days. Coloration may vary among populations, such as in the Great White Egret. The irides and feet of the Green Heron turn from yellow to orange; bills of the European Great White Egret turn yellow; and bills of the Squacco Heron Ardeola ralloides turn blue. Colour changes appear to be partly a result of the deposition of pigments (see COLOUR) and partly of increased vascularization. Voice. Herons have a limited repertoire of guttural honks, frarnks, coos, and growls. Tiger herons and oriental night herons have booming bittern-like calls. The Whistling Heron has high-pitched calls. Calls are most frequent during agonistic encounters and early in pair formation. Bill-snapping also produces sounds. Acoustic signals are emphasized by species such as the Boat-billed Heron which occur in dense vegetation. Breeding. Nesting generally occurs during the local spring and summer or when the rainfall cycle produces optimal foraging conditions. Some tropical herons nest year-round. Nests typically are stick platforms in trees, reeds, or on the ground. They are built by the female from sticks brought by the male. The 3-7 eggs are usually unmarked white, buff, or pale blue. Both the parents incubate the eggs for 16-30 days. The altricial, nidicolous young are fed regurgitated food. Young may leave the nest in as little as a week, returning to be fed. At this time both parents forage simultaneously. Young become progressively more independent and are seldom fed away from the nest site. See photos CREST; DISPLAY; FEEDING HABITS; RITUALIZATION; SUNNING. ].A.K. Hancock, j. & Kushlan, J. 1984. The Herons Handbook. London. Kushlan, j.A. 1978. Feeding ecology of wading birds. In Sprunt, A., Ogden, j.C. & Winckler, S. (eds.). Wading Birds. Nat. Audubon Soc. Research Report 6: New York. Kushlan, j.A. 1981. Resource use strategies of wading birds. Wilson Bull. 93: 145-163. Milstein, P.le S., Prestt, I. & Bell, A.A. 1970. The breeding cycle of the Grey Heron. Ardea 58: 171-257. Mock, D.W. 1976. Pair formation displays of the Great Blue Heron. Wilson Bull. 88: 185-230. Payne, R.B. & Risley, C.]. 1976: Systematics and evolutionary relationships among the herons (Ardeidae). Misc. Pub1. Mus. Zoo1. Univ. Michigan, no. 150.

HERPETOTHERINAE: see

FALCON.

HESPERORNITHIFORMES: an order erected to.include such fossil forms as H esperornis, H argeria, E naliomis (provisional placing) and B aptornis (see FOSSIL BIRDS).

HESSE'S RULE: that among warm-blooded animals the forms living in cold regions have relatively higher heart weights than those living in 'warm regions. Hartman, F.A. 1955. Heart weight in birds. Condor 57: 221-238. Hesse, R. 1921. Das Herzgewicht der Wirbeltiere. Zoo1. jahrb. (AUg. Zoo1.) 38: 243-264.

HETEROCHROISM: see

PLUMAGE, ABNORMAL.

HETEROCOELOUS: term for a type of vertebra (see

SKELETON,

POST-CRANIAL).

HETERODACTYL: see under

ZYGODACTYL.

HETEROGYNISM: term introduced by Hellmayr for a situation in which the taxonomic characters distinguishing closely related species (often geographically replacing each other) are more strongly marked in the females than in the males (see SEXUAL DIMORPHISM). HETEROSIS: 'hybrid vigour'; see under

HYBRID.

HETEROZYGOUS: see GENETICS. HIBERNATION: spending the winter in a state of reduced animation. It is common in some classes of animals; but it is scarcely known to occur in birds, although formerly fabled to do so as a regular event. (see ENERGETICS; TORPIDITY).

HILL: special term for the display ground (court) of the Ruff Philomachus pugnax (see LEK). HILL-PARTRIDGE: substantive name of some species of Arborophila (for family see PHEASANT). HILLSTAR: substantive name of Oreotrochilus spp. and Urochroa bougueri (for family see HUMMINGBIRD). HINDNECK: see

TOPOGRAPHY.

HIND TOE: see LEG. HIPPOBOSCID: see ECTOPARASITE. HIRUNDINIDAE: a family of the Passeriformes, suborder Oscines; SWALLOW.

HISTOGRAM: see HOARDING: see

BIOSTATISTICS.

FEEDING HABITS.

HOATZIN: Opisthocomus hoatzin, sole member of the Opisthocomidae (Galliformes, suborder Opisthocomi). It is an inhabitant of the flooded forested borders of quiet streams in Amazonia, one of the most peculiar birds evolved in this greatest river system in the world. Local names are 'Cigana' (gypsy, because of its extravagant dress) and 'Catingueiro' (musk-smelling). Characteristics. The Hoatzin resembles in general appearance the guans and chachalacas (Cracidae, see CURASSOW). Its total length is some 60 em but it weighs little more than 810 g as the body is quite small. The sexes are almost alike. The remarkably small head on its long, thin neck bears a long, erect and bristly crest. The short but heavy bill is operated by strong muscles and the upper mandible is articulated with the skull and so is moveable, a feature found in the parrots (Psittacidae) and some other groups (see BILL). The wings are very large in relation to the body but are weak owing to the reduced flight muscles (see below). The tail is both long and broad, the legs and toes are stout. The plumage of the upper parts is dark brown, spotted with white in places; the crest is reddish brown, and the bare facial skin is brilliant blue. The under parts are reddish yellow, the belly rust-coloured. Systematically the Hoatzin poses a still unsolved problem. Since 1837 it has been tentatively linked with 8 different orders, usually with the Galliformes, but also with the Cuculiformes (Musophagidae), Columbiformes, Gruiformes (Rallidae) and others. Primitive characteristics occur

Holorhinal

285

"

'.

alongside specializations (crop, nasal fossa, wing-claws of the chick, syrinx). The comparative study of the egg-white proteins by Sibley and Ahlquist (1973) indicated that the Hoatzin was most closely allied to the Guirine cuckoos (Crotophagidae), but immunological data (Brush 1979) suggest a closer relationship with the Galliformes and it is retained here in a sub-order of its own. No systematic clues are given by the bird's parasites: the feather lice of the Hoatzin are allied to those of the Green Ibis Mesembrinibis cayennensis, found in the same habitat. A curious anatomical feature is the wing structure of the chick; it recalls that of Archaeopteryx and led to the idea that the Hoatzin itself was an archaic relict. The first and second digits carry large claws, moveable by special muscles. These aid it to grasp branches like a climbing reptile, a technique that Archaeopteryx may well have used. Correspondingly, the development of the flight feathers is retarded, contrary to what happens in gallinaceous birds generally. As the young grow, they lose their wing-claws and the ability to swim and dive, but continue to use the spread wings to help them awkwardly about the branches, often breaking their primaries in the process. Another very peculiar morphological character is the digestive tract. While in other vegetarian birds the food is broken up in the gizzard, the crop of the Hoatzin performs this function; it is of unusual size and consists of a number of separate sections which squeeze out and break up the food. To do this, the crop has thick muscular walls and a horny internal layer, whereas the true gizzard is much reduced. The size and weight of the full crop makes the Hoatzin top-heavy and when crouching on branches it keeps its balance by leaning on its sternum, which is covered by a specially-developed callosity. The pectoral girdle is totally transformed by the size of the crop. When the bird jumps from branch to branch, it maintains its equilibrium by spreading its wings and flapping its tail. The feet do not provide a sufficient grip on the branches, unlike the curassows' which can cling firmly even on thin branches. Hoatzins have a musky odour varying in intensity with the individual and the season (hence the name 'stinking bird'). There is a widespread notion that the flesh also has this smell, which has caused the natives to leave the birds alone, except to use them as bait for fishing. Sometimes they are used for medicinal purposes. The eggs are always much in demand and Hoatzins are rapidly diminishing near human settlements. Habitat and food. The Hoatzin occurs from Guyana and Brazil to Ecuador and Bolivia, in permanently flooded forests along the overgrown shores of the Amazon, the Orinoco and rivers of the Guyanas; it can only exist where certain marshy plants are available as food; these include the great Montrichardia (Araceae) and the arboreal White Mangrove Avicennia. The birds feed on the tough, caustic leaves, flowers and fruit of these plants. Occasionally they take small animals, including fish and crabs, which they catch in the mud or shallow water under hanging vegetation. While so occupied they sometimes fall into the water, or even jump into it when shallow. Behaviour. Hoatzins are sedentary; they consort in pairs but live in flocks of 10-20 (numbers up to 30 or more were formerly recorded). They are most active in the morning and evening and on moonlit nights. They like to climb to the tops of low trees along the shore, whence they look about them and fly clumsily across small bays and creeks, frequently gliding. During the hottest part of the day they rest hidden in the shadow of the dense woodland. The Hoatzin has a very conspicuous display: it raises its enormous wings vertically, showing a big black area against a whitish background and contrasting sharply with the deep reddish colour of the rest of the wing and the flanks. It is a kind of 'eye effect', although the area is not round but square. Voice. Their loud, hoarse cries and hissing sounds make their presence known from afar. The name 'Hoatzin' is said to be Indian and onomatopoeic, based on some of their cries. When calling, the birds usually spread wings and tail. Breeding. Hoatzins breed more or less throughout the year in colonies and make their nests on branches 2-6 m above the water. The nest is flat, of dry twigs, loosely entwined. There are 2-4 eggs, relatively small, yellowish with pink spots; their shape varies considerably; the average size is 46 x 33 mm. The young hatch after about 4 weeks and have two successive down plumages. Although they stay in the nest for some weeks, they soon become adventurous and start making excursions, using their wings as hands. As, at that time, they also have a good grip with feet and bill, like parrots, they are able to clamber about without mishap. This method of locomotion is an excellent adaptation to the

Hoatzin Opisthocomus hoatzin, (K.]. W.).

mangrove jungles. When danger threatens, the chicks let themselves fall into the water, where they dive and swim off, using both wings and feet. Afterwards they climb out again and continue their way through the branches. The parents feed the young from the crop, the chick putting its head well into the widely gaping bill of the adult. As at times there are more than two mature birds visiting a nest and females exceed males in collections, some authors have suspected polygamy. H.S. Beebe, W. 1909. A contribution to the ecology of the adult Hoatzin. Zoologica (N.Y.) 1: 45-66. Brush, A.H. 1979. Comparison of egg-white proteins: effect of electrophoretic conditions. Biochem. Syst. and Ecology 7: 155-165. Parker, W.K. 1891. On the morphology of a reptilian bird, Opisthocomus cristatus. Trans. Zoo1. Soc. 13 II. Sibley, C.G. & Ahlquist, J.E. 1973. The relationships of the Hoatzin. Auk 90: 1-13. Stegmann, B.C. 1978. Relationships of the Superorders Alectoromorphae and Charadriomorphae: a comparative study of the avian hand. Pub1. Nuttall Ornith. Club 17: 1-119.

HOBBY: substantive name of certain small Falco spp.; used without qualification, in Britain, for F. subbuteo (see FALCON). HOLARCTIC REGION: the Palearctic and Nearctic Regions combined-see DISTRIBUTION, GEOGRAPHICAL; NEARCTIC REGION; PALEARCTIC REGION.

HOLDING: using the feet to grasp food or other objects (except perches-see PERCHING). Most birds do not use the feet in this way, 'manual' functions devolving entirely on the bill (see BILL). Some birds indeed have feet obviously incapable of a prehensile function, e.g. when adapted to running or swimming (see LEG). Among the exceptions, parrots are specially notable, often using a foot very much as a hand when feeding. Birds-of-prey and owls make much use of the feet in seizing, killing, holding, and dismembering their food. To some extent this is true also of some of the 'minor raptors' , such as figure prominently in the list of families given below. Tits Parus spp. not only hold food with the foot but can learn to pull up a hanging string with food at the end of it, the pulling being done with the bill but the successive lengths being secured on the perch with the feet. Further examples of use of the feet for holding food and so on are to be found among the toucans, nuthatches, shrikes, pepper-shrikes, shrike-vireos, drongos, wattle-birds, bell-magpies, and crows; this list is not necessarily exhaustive-the Purple Gallinule Porphyrio porphyria (in Africa) is, rather unexpectedly, described as holding food up to its bill while it bites pieces off. In at least some of these cases the held object may be carried in flight (see CARRYING).

HOLORHINAL: see

NARIS.

286 Holothecal

HOLOTHECAL: see

BOOTED; LEG.

HOLOTYPE: see TYPE

SPECIMEN.

HOMALOGONATAE: birds with an ambiens muscle (Garrod)-see MUSCULATURE.

HOME RANGE: the area occupied by an individual, a pair or a group of birds. When the area is defended, it is referred to as a TERRITORY. HOMING PIGEON: a domestic pigeon Columba Livia var. used for 'homing', either as a carrier of messages or in the sport of pigeon racing. Pigeons have been used to convey messages since the days of the ancient Egyptians, and were much used by the Greeks and in the Roman Empire and generally throughout the Middle East. Regular pigeon-posts were established and military operations were supported. The most famous siege use of pigeons was in Paris in 1870-1871, when 150,000 officialand a million private messages (microphotographed) were passed. With the advent of telegraphy and wireless the civilian use of pigeon-post disappeared, but in both World Wars much use was made of them. In the 1939-45 war some 200,000 birds were supplied by private breeders to the British Services and 50,000 were reared by the US Army; nearly 17,000 were parachuted to the Resistance in German-occupied Europe and 2,000 returned safely. Many airmen owed their lives to the SOS messages , carried by pigeons released when aircraft crash-landed at sea. To fit pigeons for close support of modern warfare, birds were trained to home to mobile lofts, moved a short distance each day; only moderate success was obtained with intense training, and the birds were particularly likely to go astray if they were required to cross old flight lines, as in a retreat. Attempts were also made to establish a two-way message service by feeding the birds in one place and giving them grit, water, and roosts in another; this was useful only over short distances. Drastic selection provided pigeons that would fly short distances at night, up to 2Skm. All these specialized techniques of training laid heavy emphasis on the birds being given an intimate knowledge of the country in which they were to fly. Pigeons sent long distances and returning to an established base were trained by a series of releases, at increasing distances, in the direction from which they would eventually have to return. Directional training of that kind is also the basis of pigeon racing. This is an important sport and there are perhaps 100,000 pigeon fanciers in Britain alone, with something like 2 million pigeons in their lofts. The sport developed with the advent of the railways, which provided swift transport to distant release points. The first pigeon race over 150km was held in 1818 in Belgium, and similar races had been established in England by 1875. Such distances are nowadays considered suitable for young birds of the year; yearlings will fly races of 480 km, and older birds up to 800 km. Because of heavier losses at sea-crossings the longer races, 1,000-1,300km from the Faeroe Islands in the north and from San Sebastian (Spain) in the south, are seldom flown. In continental North America races of 1,600 km are often flown, although no birds return in one day. Only a small fraction, perhaps 1 in 20, of pigeons come through all the initial stages and return from the long-distance races. Elaborate precautions are taken to ensure correct timing and to eliminate fraud. Before release a temporary rubber leg-band with a code number is put on each bird by officials. On its return the owner removes the band and drops it into a sealed time-check clock which marks the hour and minute of arrival. The distance from the release point to the home loft is measured to the nearest yard on a great circle, and the speed of the bird expressed in yards per minute. In good conditions homing speeds of 1,200 y.p.m. are common, while with tail winds they may be in excess of 2,000 y.p.m, Birds may, apparently, fly for up to 16 hours a day. Competition is within clubs and within area federations; prize money is relatively modest but is increased by systems of 'pooling' for the big national races. Birds that have been successful in such races are much in demand as breeders and can command extremely high prices. Much attention is paid to pedigrees, but there is general agreement that the only real test of an individual is its performance in races. Various fads about body shape and colour come and go; there is a school of thought that stresses 'eye-sign', the configuration of the ciliary muscle of the pupil, and in view of the overriding importance of the eye it is not impossible that there may be something in this idea. There are also numerous techniques that are supposed to increase the speed of homing, but little agreement as to whether, for instance, cocks or hens home faster or

whether they should preferably be incubating eggs or feeding young. The 'widowhood' system seeks to send cocks off to a race in a frenzy of sexual passion. Although pigeon races are essentially one-directional, the direction selected being that which gives the longest runs to the home area, it is well known that good homers can return, although not so swiftly or certainly, from other than the training direction. This indication of a more advanced form of navigational ability has been seized upon in testing theories of bird navigation (see NAVIGATION). The pigeon is certainly a bird readily amenable to experimental treatment, but a great deal of confusion has resulted from the use of birds of inferior stock. There is a wide range of individual variation in homing ability. Other species have been used for message carrying. The Romans used swallows (Hirundinidae) to convey the winning colours of chariot-races, but these were wild birds caught at their nests on the day required. Pacific islanders, however, have tamed frigatebirds Fregata sp. and use them for inter-island communication. In a different category were the 'shore-sighting' birds carried by ships of olden times. The technique was known in countries as far apart as Scandinavia and Ceylon. Ravens Corvus corax were particularly favoured and were released when land should be near; if the bird made off, it not only confirmed the presence of land but indicated its direction. G.V.T.M. Levi, W.M. 1951. The Pigeons. Columbia, S.C.

HOMOIOTHERMAL: 'warm-blooded', as contrasted with 'poikilothermal' or 'cold-blooded'; other spellings and alternative terminations are sometimes used (see ENERGETICS; HEAT REGULATION). HOMOLOGUE: a structure basically equivalent to another (but possibly adapted in a different way)-compare ANALOGUE. HOMOLOGY: a fundamental concept in comparative evolutionary studies, whether of morphological or behavioural features. Bock (1969) gives the following definition: 'Homologous features (or conditions of features) in two or more organisms are those that can be traced back phylogenetically to the same feature (or condition) in the immediate common ancestor of these organisms'. 'Analogy' is often taken as the opposite term but, as this term is used in a variety of other senses, Bock advocates the term 'non-homology' where attributes in two or more organisms cannot be traced phylogenetically to the same attribute in their immediate common ancestor. Discrimination of homologous features becomes a problem in morphologically uniform groups such as many bird taxa, and Bock has proposed the term 'pseudohomology' for some of the closely similar features or conditions that may arise independently in two or more members of such groups. P.].K.B. Bock, W.J. 1963. Evolution and phylogeny in morphologically uniform groups. Amer. Natur. 97: 265-285. Bock, W.J. 1969. The concept of homology. Ann. N.Y. Acad. Sci. 167: 71-73. Bock, W.J. 1974. The avian skeletomuscular system. In Farner, D.S. & King, J.R. (eds.). Avian Biology, vol. IV. New York.

HOMONYM: see

NOMENCLATURE.

HOMOZYGOUS: see GENETICS. HONEY-BUZZARD: name of Pemis apivorus and allies (see HAWK). HONEYCREEPER: substantive name of some species of Thraupinae (see TANAGER), which were formerly combined with the BANANAQUIT, ORANGEQUIT, CONEBILLS and FLOWER-PIERCERS in the family Coerebidae (Passeriformes, suborder Oscines). In this older classification, 'honeycreepers' was the general term for the family. This term is inappropriate for the family Coerebidae as here recognized, since none of the 3 genera now included, Coereba (Bananaquit) and Conirostrum and Oreomanes (conebills), are generally known as honeycreepers. In what follows, the term 'honeycreeper' is restricted to the thraupine genera Cyanerpes, Chlorophanes, Dacnis and Xenodacnis, the last a little known genus represented by one species in the Andes and perhaps not closely related to the others. The 4 genera comprise 15 species, all confined to the American tropics. The honeycreepers represent a line of specialization within the large assemblage of tanagers leading, from the typical tanagers' diet of insects

Honeyeater

and fruit, to nectar-eating. In Da cnis the bill is sharp, slightly decurved, and quite short, and thu s not very different from that of some typical tanagers. Chlorophanes has a longer , more curved bill, and the extreme is reached in the Pu rple Honeycreeper Cya nerpes caeruleus, in which the bill is very long and curved and nectar and fruit juices are important elements in the diet. Together with the bill, the tongue is progressively modified into a tubular struct ure adapted for sucking. Even the most specialized honeycreepers, however, feed also on insects and small whole fruits, the long bill enabling them to pr obe for insects and to extract the arillate seeds from the splitting capsules of such plants as Clusia. Male honeycreepers are brilliantly coloured , with unrivalled shades of deep blue, turqu oise-blue and blue-green; the females are much duller , predominantly greenish. The male Blue (or Red-legged) Honeycreeper Cyanerpes cyaneus is peculiar in moulting, at least in parts of its range, into a female-type plumage dur ing the non-breeding season. Honeycreepers are typically birds of forest and forest-edge , doing most of their foraging in the forest canopy; but cultivation with trees forms a suitable habitat for several species. In general behaviour they are typical TANAGERS; they live in pairs, have poorly developed , unmu sical vocalizations, and build cup-shaped nests in trees and shrubs. D .W .S. (I) Skutch, A.F. 1962. Life histories of honeycreepers. Condor 64: 92- 116.

HONEYCREEPER , HAWAIIAN: see

HAWAII AN HON EYCREEPER .

HONEYEATER: substantive name of many species of Meliphagidae (Passeriformes, suborder Oscines); in the plural, general term for the family. Th is is a group of mainly arboreal, nectar-, insect- and fruiteating birds of Australasian distribution. Characteristics. The most striking family character is the brushtongue, an adaptation to nectar feeding, but in its structure notably different from that of other major nectar-feeding groups of bird s. T he tongue is prolonged and protru sible. The basal part is curled up on each side, forming two long grooves. Th e distal part is deeply cleft into 4 parts, which on their edges are delicately frayed and together form the 'brush' which licks up the nectar. Th e tongue is extended into nectar, or other liquids, about 10 times per second and liquid is taken up by capillary action. The tongue is then withdrawn into the beak which is closed, and projections on the roof of the beak appear to compress liquid from the brush along the groove to the throat. In spite of much variation and secondary changes, the basic characters of the tongue are present in all members of the family. A more rud imentary bru sh-tongue is found in other birds which feed on nectar less frequently e.g. silvereyes Zosterops, wood-swallows (Artarnidae) and Australian chats (Ephthianuridae). Other characters widespread in the family are the pervious nostrils, and the tendency to absence of feather s from parts of the face, on which develop bare spaces, or even lobes, wattles, or other appendages . Th e plumage is in most species rather dull , greenish, greyish brown , or streaked; the sexes being similar . Th e most notable exception to this is in several species of My zomela, which possess contrasting patches of sanguineous red in the plumage and display a pronounced sexual dimorphism. In many honeyeaters ther e is a conspicuous yellow, golden or white patch on the posterior part of the ear region; this character is particularly well developed in the members of the large genus M eliphaga. The honeyeaters display extraordinary variation in structure (lengths 9.5-32 em), bill form , body proport ions, and even mode of life. The y include birds resembling goldcrests R egulus spp., other warblers (Sylviinae), and thru shes (T urdinae); species that could be mistaken for sunbirds (Nectariniidae) or hummingbirds (T rochilidae); species with falcate bills like Hawaiian honeycreepers (Drepanididae) or bee-eaters (Meropidae); larger species approaching the appearance of orioles (Oriolidae), jays and magpies (Corvidae); and even birds looking very similar to tits (Paridae), nuthatches (Sitt idae), babblers (Timaliidae) and flycatchers (Muscicapinae). Thi s extreme variation has been compared with that of the marsupials among mammals; and , although this may be exaggerated, there is obviously a striking parallelism in history and evolution in these two group s. Habitat. In such a large and diversified group as the honeyeaters, ecology and behaviour are of course extremely varied. Common to almost all honeyeaters is their arboreal habit. Only a few descend to the ground for feeding e.g. Ma norina and the T awny-crowned Honeyeater Phylidonyris melanops and not a single species places its nest on the ground , although the latter species make s use of high grassy tussocks as nesting sites. Honeyeaters are mainly bird s of forests and heathlands, where they

287

Tu i Prosthemadura 1Iln.'ot's....landia e. (C. E .T .K .) .

frequent tree-tops and flowering trees and shrubs. Several species, most of them inhabiting the continent of Australia, have become adapted to the more open and arid woodlands. No species can exist in completely treeless country, however, but a single species, the Singing Honeyeater M eliphaga virescens, ranges right to the coastal sand-dunes and also inhabits the small islands off the barren south and west coasts of Australia. Many species are attached to the mangrove swamps, savannas, heathland and mallee, a few even to the mulga scrub, while in the desert-like spinifex country in the interior of Australia only one species, the Pied Honeyeater Certhionyx variegatus, is occasionally encountered. There is a tendency for different species in some genera, Me liphaga, M elithreptus, M anorina , to occur in separate, though often neighbouring habitats. Several species are restricted to the high mount ains of New Guinea (M elipoces, M elidectes and others), while some, most of them belonging to the genera My zomela and L ichmera, are inhabitants of small oceanic islands. Distribution. Honeyeaters belong to the Australasian region, where they are widely distributed and form one of the most characteristic bird groups. Only one species, the Brown Honeyeater Lichmera indistincta, has crossed Wallace's Line and settled in Bali; another species, Apalopteron f amiliaris, inhabits the Bonin Island s, which are regarded as belonging to the Palearctic Region . T o the east the range of the honeyeaters includes the greater part of Micronesia, Melanesia, Polynesia (east to Samoa and Tonga ), the Hawaiian Island s, and the New Zealand islands. Th e 167 species of honeyeater s (including a total of about 450 sub-species) are divided among 38 genera, of which 14 are rnonotypic. Th e largest genera are M eliphaga (36 species), Myzomela (24 species), and Philem on (16 species). New Guinea and the Australian mainland form the centres of distribution and are inhabited by an almost equal number of species--New Guinea (with satellite island s) by 63 species, Australia (with Tasmania) by 68 species. The New Guinea honeyeaters are generally more primitive and unspecialized, while the Australian (and New Zealand) forms include a great number of specialized and derivative types. Food. Nectar and insects form the major part of the diet of most honeyeaters. In addition, many of the larger honeyeaters feed also on fruits and berries and may do some damage in Australian orchards. The tropical rainforest species are predominantly frugivorous. Pollen is consumed but probabl y not digested . Hone ydew from scale insects, manna (sugary granul es from damaged eucalypt leaves) and lerp (coats of sap-sucking insects) also form an impo rtant part of the diet of some species. Behaviour and movements. Honeyeater s are more or less gregarious; no species is solitary. The y tend to move around in small parties, especially outside the breeding season, and under certain conditions large swarms concentrate around flowering trees. Some open-country species are markedly nomadic ; a few subtropical-temperate species make regular seasonal movements, whereas in many other species the movements are more complex and appear less regular. The flight may be swift in smaller species, and more clumsy and undulating in the larger species, almost like that of the Magpie Pica pica. Voice. The vocal utterances differ widely. Many of the smaller species

288 Honeyeater

are excellent songsters, while the larger ones are not so musical and utter various harsh and noisy babbling sounds, usually characteristic of the genus. The Bell Miner Manorina melanophrys has a peculiar song, resembling the tinkling of a silver bell; the song of the New Zealand Bellbird Anthornis melanura, a distant ally, is somewhat similar. The strange Tui Prosthemadura novaeseelandiae, also of New Zealand, a glossy bluish-green bird like a Starling Sturnus sp. with 2 tufts of white curled feathers on the lower throat, is known to be an excellent mimic of other birds' songs. A few species frequenting open country have song-flights. Some of the species inhabiting dense rainforests are silent. Breeding. The nest is a cup-shaped, sometimes pendulous, structure, varying considerably in composition and situation. It is placed in trees or bushes, often high up. In several species the nests are placed on branches overhanging water, along rivers or lake borders. Group nesting, in colonies up to 20 or more, is a rather frequent phenomenon, at least in Australian species. Many species of Meliphaga and probably all species of Meluhreptus and Manorina are co-operative breeders with several adults, probably chiefly males, feeding the nestlings and fledglings from each nest. The Noisy Miner Manorina melanocephala has a particularly complex breeding system. The breeding season of honeyeaters in southern Australia is extended and late winter is the peak for the more nectarivorous species and spring for the more insectivorous ones. Breeding in autumn is quite frequent. A peculiar habit is developed in some species of Melithreptus and Meliphaga: to obtain nest material they habitually pull hairs off cows, larger marsupials (possums), and even man. The species of Ramsayornis are unique among honeyeaters in building closed nests, dome-shaped with a side entrance. The Blue-faced Honeyeater Entomyzon cyanotis of Australia differs from all other honeyeaters in using deserted nests of babblers (Timaliinae), preferably those of Pomatostomus temporalis, and it is known sometimes to oust the legitimate owners by force. The eggs are spotted, most often with reddish brown. The clutch consists, in the tropical species, of 1 or 2 eggs, in the subtropical of 2, occasionally 3 eggs, in the larger species often of 4 eggs; and in the temperate species (in New Zealand) also usually of 4 eggs. The participation of the male in nest building and incubation differs widely, and in many species the female alone performs these duties. On the other hand, both sexes share in feeding the young. Incubation periods are from 12-16 days; and fledging periods 10-16 days. Ecological relations. Many species of honeyeaters (e.g. Phylidonyris, Acanthorhynchus and Anthochaera) are dependent on the nectar of blossoms of trees and shrubs for a large part of the year. Insects are taken primarily as a source of protein. Others (e.g. Meliphaga and Melithreptus) feed more on insects, though they readily take nectar, especially in winter in southern Australia, and alternative sources of sugar (honeydew etc.). The species belonging to the Australian genus Conopophila have mostly given up nectar feeding and are mainly insectivorous, capturing their prey in the air like flycatchers (Muscicapinae). One species, the Painted Honeyeater C. pieta, has specialized on mistletoe berries, apart from insects. The members of the New Guinean genus Melipotes have also become fruit-eaters; their tongue structure has been secondarily simplified. The 6 species of Melithreptus are tit-like, active birds, of which the Strong-billed Honeyeater M. validirostris of Tasmania has developed food habits and even a bill-form almost like that of a nuthatch Sitta sp. It runs up trunks, taking insects from under the bark, which it pulls off with its powerful bill. The O-o-aa Moho braccatus of Hawaii is predominantly insectivorous and searches for food by climbing the boles of trees like a woodpecker (Picidae), aided by its stiff tail-feathers. The spine-bills Acanthorhynchus spp. of Australia have long and extremely thin decurved bills, and during nectar feeding are able to hover in front of the blossoms like hummingbirds. The 4 miners Manorina spp. are jay-like, noisy, and inquisitive birds. The friar-birds or leatherheads Philemon spp. generally resemble jays or jackdaws (Corvidae) but have parts of the head naked and inky black, and many species have a horny protuberance on the bill. They are strange in appearance and utter loud and querulous chatterings. The wattle-birds Anthochaera have a pendent wattle on each side of the head, longest and most conspicuous in the Yellow Wattle-bird A. paradoxa of Tasmania; they utter peculiar guttural notes, resembling coughing or barking. All 3 New Zealand honeyeaters feed on nectar, insects and fruit. The large Tui takes much nectar, often defending flowers from the 2 smaller species. The rare Stitch bird Notiomystis cincta, now only found on Little Barrier Island, visits the flowers of shrubs, while the Bellbird is more

insecti vorous. Blossoms of trees and shrubs constitute the main feeding place of most honeyeaters. Owing to this fact they are very efficient pollinators; in fact they form, together with certain parrots, the most important agents in the fertilization of the greater part of the indigenous Australian tree and shrub flora, such as members of the Myrtaceae, Proteaceae, Epacridaceae, Loranthaceae, Rutaceae, Myoporaceae and Haemodoraceae (see POLLINATORS). An intimate connection exists between the plants and the honeyeaters, and the ornithophilous flowers have developed a number of adaptations to bird visits, just as the honeyeaters in their anatomy demonstrate striking adaptations to nectar feeding; this is true of the tongue, as mentioned above, and also of the alimentary tract. The intestinal canal is rather short and wide, the opening of the oesophagus into the stomach and that of the intestinal canal (pylorus) are placed very closely together, in a little chamber partly separated from the stomach proper. This structure permits nectar and other easily digestible matter to pass directly from the oesophagus to the intestines, while insect food can be retained in the stomach for the necessary period of digestion there. The structure of the flowers visited by honeyeaters varies from simple and cup-shaped in Eucalyptus to long and gullet-shaped as in Eremophila and Anigozanthos. Pollen is chiefly deposited on the forehead and throat, but also on the crown and even the back, and the pollen of the Epacrids sticks to the beak and nostrils. Areas where nectar is abundant frequently attract large numbers of individuals and species of honeyeaters. Competition for nectar is often severe. Under these conditions larger species may defend territories around rich nectar sources, forcing smaller species into less rich areas. Sugarbirds. The 2 sugarbirds Promerops spp. of South Africa, which are characterized by a long, curved bill and a prolonged, drooping tail, agree with the honeyeaters in most structural characters as well as in life-habits (nest, eggs, feeding). They have, therefore, been incorporated in the Meliphagidae until recently, but must for other reasons (for instance, electrophoresis) be regarded as a special family, not least on account of their remote breeding range (see SUGARBIRD (1)). F.S. and H.A.F. Craig, J.L., Stewart, A.M. & Douglas, M.F. 1981. The foraging of New Zealand honeyeaters. N.Z. J. Zool. 8: 87-91. Dow, D.D. 1977. Reproductive behavior of the Noisy Miner, a communally breeding honeyeater. Living Bird 16: 163-185. Ford, H.A. 1979. Interspecific competition in Australian honeyeaters--depletion of common resources. Australian Journal of Ecology 4: 145-164. Ford, H.A. 1980. Breeding and moult in honeyeaters near Adelaide, South Australia. Australian Wildlife Research 7: 453-463. Ford, H.A., Paton, D.C. & Forde, N. 1979. Birds as pollinators of Australian plants. N.Z. Journal of Botany 17: 509-519. Gravatt, D.]. 1971. Aspects of habitat use by New Zealand Honeyeaters, with reference to other forest species. Emu 71: 65-72. Keast, J.A. 1976. The origin of adaptive zone utilizations and adaptive radiations, as illustrated by the Australian Meliphagidae. Proc. XVI Int. Orn. Congr., Canberra: 71-82. Paton, D.C. 1980. The importance of manna, honeydew, and lerp in the diets of honeyeaters. Emu 80: 213-226. Paton, D.C. & Ford, H.A. 1977. Pollination by birds of native plants in South Australia. Emu 77: 73-85. Pyke, G.H. 1980. The foraging behaviour of Australian honeyeaters: a review and some comparisons with hummingbirds. Australian Journal of Ecology 5: 343370. Recher, H.F. 1977. Ecology of co-existing White-cheeked and New Holland Honeyeaters. Emu 77: 136-142.

HONEYGUIDE: substantive name of the species of Indicatoridae (Piciformes, suborder Galbulae); in the plural, general term for the family. The family contains Ifr-19 species, depending on controversial taxonomic decisions exacerbated by inadequate knowledge of the biology of most forms; one (Melignomoneisentrauti) discovered as recently as 1965. Characteristics. All honeyguides are small, 10-20 ern long and weighing 10-55 g. Plumage is dull and inconspicuous, generally olive, grey or brownish above, sometimes obscurely streaked, and lighter below, with dark or dull-coloured bill, legs and feet; Indicator xanthonotus has the forehead and rump orange. Most species have pale sides to the tail, often with a pale rump patch, and 2 species have yellow patches on the wing-coverts. Some species have a white spot on the lores and a black malar streak. Sexual dimorphism is usually slight, except in I. indicator

Hoopoe

Greater Honeyguide Indicator indicator. (C.E.T.K.).

where the female is typically dull-coloured but the breeding male has the head boldly marked with white cheeks and black throat, and has yellow shoulder patches and a pink bill. The bill is typically stout and blunt, with raised edges around the nostrils except in the 3 small flycatcher-like Prodotiscus species which have a fine pointed bill. The legs are short, toes zygodactyl, with strong hooked claws. The wings are pointed, the flight rapid and often weakly undulating. The tail is graduated in most species; in Melichneutes it is lyre-shaped. The skin of some species is notably thick, possibly as a defence against insect stings. Habitat and distribution. All 4 genera (Indicator, Prodotiscus, Melignomon and Melichneutes) inhabit evergreen forest or forest edge, the first 2 also occurring in more open woodland. All but 2 of the species are confined to Africa south of the Sahara; the 2 exceptions (both Indicator) are Oriental, one occurring in south-east Asia, the other in the Himalayas. Most of the African species form closely related groups whose members are so similar that taxonomic treatment remains controversial, especiallyas the groups themselves are very similar to each other. Within each group, there is a trend towards darker-plumaged species inhabiting evergreen forest and paler species occupying more open woodland. Three or more sibling species may be sympatric, and it is not known how they remain segregated. Populations and movements. No information for any species. Food. All the species whose food is known eat insects, but a characteristic peculiarity of the family is that they also eat wax, usually as bee comb but also, in Prodotiscus spp., as waxy scale-insects. Some species have been seen eating comb at bees' nests but in others 'cerophagy' (eating wax) is inferred from the presence of wax in the digestive system of collected specimens. Two species (I. indicator and I. minor) have been shown experimentally to digest wax and to survive for around 4 weeks on wax alone; I. indicator can also survive without wax for several months. It is not yet entirely clear whether the wax is digested by symbiotic bacteria, as one experiment suggests, or by an enzyme unique to honeyguides. The parts of the honeycomb most commonly eaten by I. indicator in captivity are the larvae and the wax; the honey that contributes to the family name, the pupae and adult bees are taken rarely or not at all. Bees' nests may be detected at least partly by scent since honeyguides can be attracted by the smoke from burning wax. The habit of feeding on bee comb is associated in the 2 largest species, I. indicator and I. variegatus, with that of guiding man and other mammals to bees' nests. This behaviour is best known in I. indicator; the bird, usually alone, draws attention to itself by a distinctive chattering call, and then flies a short distance towards a bees' nest. This behaviour is repeated until the nest is reached, when the bird sits quietly nearby, coming down to feed at any comb that may be left after the follower has opened the nest. The usual follower apart from man is the Ratel or Honey-Badger Mellivora capensis, but baboons Papio and even mongooses (Herpestinae) may also respond. Tribesmen in many parts of Africa use honeyguides to lead them to bees' nests, but the habit seems to be declining as alternative sources of sugar become more available. The evolution and development of this complex symbiotic behaviour, especially surprising in a nest parasite, remain obscure. Behaviour. So far as is known all honeyguides are solitary, individuals aggregating chiefly for mating or at localized food sources. Voice. Poorly known; in several species the male song is a simple monotonous one repeated from an elevated song post. The guiding chatter of I. indicator is distinctive, and a variety of generally rather simple calls, often nasal or squeaky, is recorded from several species. Some species show vigorous vocal interactions with potential hosts even

289

when hosts are not breeding. Breeding. Of the 7 species whose breeding habits are known, 6 are certainly parasitic but I. xanthonotus of the Himalayas apparently is not; it may be significant that this species lacks the white outer tail feathers typical of honeyguides, supporting the possibility that these may be used in luring hosts away from their nest. An observation of an adult Prodotiscus insignis feeding a recently-fledged juvenile raises the intriguing possibility that parasitism may not always be complete even in habitually parasitic species (Brosset 1981). Most species parasitize holenesting birds, especially barbets, woodpeckers, hoopoes and woodhoopoes, kingfishers, rollers, bee-eaters and starlings; but the small flycatcher-like Prodotiscus species (P. insignis, P. zambesiae) parasitize open-nesters such as white-eyes, and P. regulus parasitizes hosts with closed nests such as swallows, swifts and some Cisticola warblers. The mating system is known only in I. xanthonotus. Males defend territories centred around bees' nests, to which they allow access only to females with which they have mated and their attendant young; this mating system has been described as 'resource-based non-harem polygyny'. Other species have been assumed to be promiscuous, but males of several species have been observed accompanying females attempting to enter host nests, a behaviour unlikely in a promiscuous species. No other honeyguide is known to defend either food sources or mating sites. In I. indicator and probably other species, males sing from a conspicuous 'stud post' where females come for mating, which is preceded by rudimentary courtship behaviour and may be followed in I. indicator by the male executing a dramatic circling flight in which a loud rattling noise is made by the wing feathers. In Melichneutes the lyre-shaped tail apparently also makes a distinctive sound. This may also be connected with courtship behaviour, which includes a display flight above the forest canopy. Honeyguide eggs are normally thick-shelled and white, except in P. zambesiae where they are sometimes blue like those of the Zosterops host. Usually only one egg is laid in each nest but there are a few records of 2 honeyguides being reared in one nest. The incubation period is known only for P. zambesiae (less than 13 days) and I. minor (12 days). The fledging period is about 38 days for I. minor, 40 days for I. indicator. The chicks of several species bear on each mandible a hook, which is used to destroy host eggs or chicks. The chick is fed exclusively by the hosts at least until fledging; the begging call of nestling I. indicator resembles the combined calls of several chicks. A.W.D. Archer, A.L. & Glen, R.M. 1969. Observations on the behaviour of two species of honey-guides. L.A. County Mus. Contrib. Sci. 160: 1-6. Brosset, A. 1981. Observation de l'Indicateur parasite Prodotiscus insignis nourissant un jeune de son espece, L'Oiseau et R.F.O. 51: 59-61. Cronin, E. W. & Sherman, P.W. 1975. A resource-based mating system: the Orange-rumped Honeyguide. Living Bird 15: 4-32. Friedmann, H. 1955. The honey-guides. U.S. Natl. Mus. Bull. 208. Friedmann, H. 1970. Further information on the breeding biology of the honeyguides. L.A. County Mus. Contrib. Sci. 205: 1-5. Friedmann, H. & Kern, J. 1956. The problem of cerophagy or wax-eating in the honeyguides. Quart. Rev. BioI. 31: 19-30. Fry, C.H. 1974. Vocal mimesis in nestling Greater Honey-guides. Bull. B.O.C. 94: 58-59. Fry, C.H. 1977. Relation between mobbing and honey-guiding. Br. Birds 70: 268-269. Short, L.L. & Horne, J.F.M. 1979. Vocal displays and some interactions of Kenya honeyguides (Indicatoridae) with barbets (Capitonidae). Amer. Mus. Novitates 2684.

HONKER: name applied in North America to the Canada Goose Branta canadensis (see under DUCK). HOOD: an area of distinctive colour, in some plumage patterns, covering a large part of the head (see TOPOGRAPHY). HOOKBILL: Ancistrops strigilatus (see OVENBIRD

(1).

HOOPOE: Upupa epops, sole species of the family Upupidae (Coraciiformes, suborder Coracii), found in some 9 subspecies throughout most of the Palearctic, Afrotropical and Oriental Regions. The Hoopoe is such a striking and unmistakable bird that it has a long pedigree in human culture: it was used as a hieroglyphic in ancient Egypt, figured prominently in Aristophanes' The Birds, features widely in folklore, and has long been celebrated in literature. Both of the scientific names, and the vernacular names in several languages including English, are onomatopoeic.

290 Hoopoe

Hoopoe Upupa epops africana. (N.A.).

Characteristics. Hoopoes are hole-nesting, ground-foraging, insectivorous birds with a long thin decurved beak, short legs and rather weak feet, and plumage of predominant hue varying geographically from pinkish through cinnamon to chestnut. The sexes, and the fledgling, look much alike. There is a long, black-tipped crest which is usually flat, but is opened into a conspicuous fan when the bird alights or is excited. The rump is white and the tail broad and black, with an inverted white chevron across it. The wings are rounded, black, with 1-4 broad bands of white across the secondaries and greater coverts and in some races a further white band crossing both primaries and secondaries subperipherally. Flight is distinctive, with erratic, butterfly-like flapping, the wings closed at each beat; it appears weak and indecisive, but Hoopoes are in fact strong fliers. They are about 31 em long and weigh 50-60 g (range 40-70 g). The mutual affinities of coraciiform and piciform families remain controversial (Sibley and Ahlquist 1972). But there is wide agreement that the Hoopoe's closest relatives are the Phoeniculidae (WOOD-HOOPOE), with which it agrees in feather structure (except the absence of an aftershaft), pterylosis, tongue, anatomy, egg-white proteins, visceral and skeletal characters; and there is good evidence also for allying these 2 families closely with the Bucerotidae (HORNBILL). However, Upupa differs from all other coraciiform birds in the absence of the expansor secondarium muscle, and in some characters it converges with passerine birds. Hoopoes being migratory, at certain seasons and places 2 or more subspecies occur together. Where they are distinguishable in the field, it has led to them being treated as specifically distinct (e.g. U. senegalensis, U. africana and U. epops in Africa); but in the absence of breeding sympatry it accords better with current systematic practice to treat Hoopoes as a single polytypic species. Distribution, habitat and movements. Hoopoes occur in open country in virtually the whole of Africa and Madagascar, and the Oriental and Palearctic Regions north to the Gulf of Finland, the Sakmara River, the southern shores of Lake Baikal, the middle Amur and Khungari Rivers. They breed in the Canaries and most Mediterranean islands, but only exceptionally in Britain and Scandinavia. In south-east Asia they breed throughout Sri Lanka, Indochina and Taiwan but rarely further south in the Malayan peninsula than Pattani, Borneo has only one record, probably a migrant; but a few may nest in northern Sumatra. They do not occur in Korea or Japan. Throughout their breeding range, they prefer open land with scattered trees and some short grass sward or bare soil: pastures, parkland, orchards, steppe, dry and wooded savannas, and broken ground with scattered shrubs to an altitude of 2,500 m. In Africa, drier regions are favoured and lush evergreen woods and forests are shunned. West Palearctic Hoopoes winter in sub-Saharan Africa south to 10oS,and central and east Palearctic populations winter in south Asia from Mesopotamia to southern India and south China. African races are migratory within the tropics. The bird is a diurnal migrant, and over

the Mediterranean commonly falls prey to falcons. Food. Mainly small insects, particularly soft larvae; cockchafers and smaller beetles (larvae and imagines), grasshopper nymphs, caterpillars, ants, flies, termites, earwigs, ant-lions. Also spiders, occasionally earthworms and woodlice, and rarely larger items like centipedes, which have to be broken up before being eaten. Evidently Hoopoes do not regurgitate pellets, but void arthropod sclerites with the faeces. They feed mainly on the ground, walking over turf, dusty or moist soil, pecking and probing assiduously, and may insert the beak full-length into soft soil and dig small holes with the beak to extract prey. Sometimes Hoopoes hawk flying insects, and search the ground beneath flicked-over refuse and dry cow-pats. Behaviour and voice. Hoopoes are monogamous, and territorial when breeding. No winter territories appear to be held. They occur in pairs or solitarily, but immigrants to breeding grounds form parties up to 9 before reproductive behaviour commences. The young do not feed themselves at all for 6 days after fledging, and thereafter remain in loose family parties with their parents for some weeks. Sexual behaviour is heralded by males beginning to call even when still in pre breeding flocks-a far-carrying, dove-like hoohoo(2-4 notes) given inside or on top of a tree. As territories are established, favoured song-posts are adopted and rival males advertise from 300 m or more apart. 'Swizzle' and 'rattle' calls are given during male-male and male-female chases, and these and other calls during courtship feeding and nest-hole-demonstration by the male to the female (Hirschfeld and Hirschfeld 1973; Skead 1950). There is no additional courtship display; and copulation takes place on the ground. Nestlings defend themselves by: hissing; rapid upward poking of the head with beak-clapping; a single rapid wing-strike; a stinking secretion of the preen gland (Lohrl 1977); and by the aimed spraying of excreta. Adults have a striking defence posture with the wings and tail widespread on the ground, the head thrown back and the beak upward. Breeding. Hoopoes nest in holes in trees and walls, or crevices in boulders and old buildings; sometimes in nest-boxes. Nest holes are found and cleared by the male. Sometimes no nest material is used (although droppings accumulate) but at others a distinct bed of grassbents is made. The whitish eggs are laid daily, clutch sizes being 4-7 in the tropics and 5-8, exceptionally 12, in Europe. The female incubates and is fed by the male, occasionally emerging to feed herself too. She remains in the nest for about a week after the last egg hatches, then both parents provide food. The incubation period is 17 days and the nestling period 26-32 days (South Africa). Nest sanitation is primitive. The species is double, possibly treble, brooded. C.H.F. Hirschfeld, H. & Hirschfeld, K. 1973. Zur Brut- und Ernahrungsbiologie des Wiedehopfes, Upupa epops L., unter Berucksichtigung seiner Verhaltensweisen. Beitr. Vogelkd. 19: 81-152. Lohrl, H. 1977. Zum Brutverhaltern des Wiedehopfes Upupa epops. Vogelwelt 98: 41-58. Sibley, C.G. & Ahlquist, J.E. 1972. A comparative study of the egg white proteins of non-passerine birds. Peabody Mus. Nat. Hist. Bull. 39: 1-276. Skead, C.]. 1950. A study of the African Hoopoe. Ibis 92: 434-463.

HOOTING: term applied, where appropriate, to the calling of certain birds, especially owls (Strigiformes). HOPPING: see

LEG; LOCOMOTION, TERRESTRIAL.

HORIZONTAL AND VERTICAL CLASSIFICATION: a horizontal system of CLASSIFICATION is one that includes only birds existing at the same level of geological time. A system thoroughly phylogenetic in its scope must, however, take into account also those fossil forms that produce a vertical arrangement in which, so to speak, time is a dimension. Such an arrangement can be depicted as a branching tree. HORMONES: internal secretions having specific physiological actions (see ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM).

HORNBILL: substantive name of all members of Bucerotidae (Coraciiformes, suborder Bucerotes). A discrete and distinctive family, most closely allied to the hoopoes (Phoeniculidae, Upupidae), but not related to the toucans (Ramphastidae) of the New World, although they may be their ecological counterpart. Characteristics. Hornbills have fused axis and atlas vertebrae, and are noted for their long, heavy bills, each with a casque on top. In some

Hornbill

species the bill has ridges or notches on its sides. The casque is light and hollow, supported internally by thin bony struts, and may be elaborately shaped and as large as the bill. Hornbills have long eyelashes, short legs with syndactylous toes and broad soles, broad, rather short wings, and long tails which are graduated in some species. The flight is direct and consists of bouts of flapping and gliding, and is often noisy as air rushes through the bases of the flight feathers not covered by stiff coverts. Most species hop on the ground, but a few terrestrial ones walk. The plumage is white, black or brown, sometimes with a metallic sheen. Bare areas of skin on the face and throat, the eyes, and the bill and casque are often brightly coloured, the colours changing with age. Differences in these colours also occur between the sexes which are dimorphic, to a greater or lesser extent, through size (males being slightly larger than females), through differences in plumage, and through the shape and size of the casque. All hornbills (apart from 2 ground horn bills in Bucorvus) seal the entrance of their nesthole. These characteristics have made horn bills mystical birds. Some African tribes place Bucorvus heads on their own heads as camouflage when hunting game, and many taboos exist about who may eat hornbills, when and for what reasons. Asian and Polynesian tribes use tail feathers of the large hornbills for head-dress and cloak ornamentation. In Borneo the Rhinoceros Hornbill Buceros rhinoceros is revered, the recurved casque being symbolized as spirals on large carved effigies, and it forms the centre-piece of the coat-of-arms of Sarawak. Ivory from the casque of the Helmeted Hornbill Rhinoplax vigil is intricately carved as earrings, belt buckles and other trinkets, and has been a highly valued export from the region to China since at least the 12th century. As a result hornbills are being protected, legally or by taboo, in many areas. (See also ORNAMENTATION, BIRDS IN HUMAN.)

Systematic characteristics. The 45 species of horn bills are usually placed in 14 genera; Tockus (14), Rhyticeros (7), Bycanistes (5), Anthracoceros (4), Buceros (3), Penelopules (2), Bucorvus (2), Ceratogymna (2), and the monotypic genera Aceros, Anorrhinus, Berenicornis, Ptilolaemus, Rhinoplax and Tropicranus. As far as is known all nestlings of Tockus, Anthracoceros, Penelopides, Anorrhinus,Berenicornis, Ptilolaemus and Tropicranus have pink skin on hatching and this remains pink, whereas in the remaining genera the pink coloration changes to a deep purple-black within a few days of hatching. Hornbills vary in size from the relatively small Tockus species (c. 38-46 em), through the medium-sized species in Anorrhinus, Anthracoceros, Berenicornis, Ptilolaemus and Tropicranus (range c. 68-92 em), to the very large species in Aceros, Buceros, Bucorvus and Rhinoplax (c. 116-126cm). The African Tockus species and the closely related Long-crested Hornbill Tropicranus albicristatus, with its white crest and long graduated tail, are the only horn bills that bring single items of food to the nest. The others, apart from the ground hornbills, regurgitate food at the nest, item by item, from the gullet. The Asian species of Tockus may deserve their own genus for they differ from the African species in having young with yellow bills, as do other Asian genera, and when calling do not display, whereas the African species are very vocal and do display. They appear to be linked to the poorly defined Anthracoceros genus, most of which have very large casques in both sexes, but differ among themselves in calls, behaviour and breeding biology. Although the Bushy-crested Hornbill Anorrhinus galeritus and the Brown-backed Hornbill Ptilolaemus tickelli have similar calls and share their own genus of louse, they are kept in monotypic genera as their colour and breeding biology are different. Sexual dimorphism is pronounced in the White-crested Hornbill Berenicornis comatus, Penelopides spp., the Rufous-necked Hornbill Aceros nipalensis and in Rhyticeros spp. In the last 2 genera the head and neck are brown and white in males and black in females, and the immatures are like adult males. In most species their tails are short and white. Each species of Rhyticeros has a distinctive casque shape, variously wreathed and wrinkled, and the bare areas on the face are often extensive and colourful. The White-crested Hornbill has a long crest and a long graduated tail. Little is known about it, and it may be related to Anorrhinus and Ptilolaemus. The Penelopides species, one highly polymor-

orange coloration is applied using a special tuft of feathers that surrounds the gland. All Buceros species and the Helmeted Hornbill have brightly coloured feet, greenish-yellow in Buceros, reddish-brown in Rhinoplax and usually dark slate grey in other genera, white tails with a black band, and elaborate and large casques. The Helmeted Hornbill differs in having extensive bare skin on the head and neck, greatly elongated tail feathers, and the front of the casque composed of solid 'ivory' so that its skull is 10% of the body mass. These 3 genera also share a unique genus of louse, although Buceros and the Helmeted Hornbill are arboreal while Bucorous species are terrestrial. The ground horn bills are aberrant: in addition to the differences already mentioned, they have an extra cervical vertebra (IS instead of 14), long tarsi and a short tail, and extensive and inflatable facial skin areas. They walk on the tips of their toes, and scrape and dig the ground with their bills in search of food. They are the only hornbills that excavate their own nest hole if required, and show no nest sanitation. They also deliver the food to the nest as a collection of items in the bill. Seven species in the genera Bycanistes and Ceratogymna are closely allied. Immatures resemble adult females in having brown on the head and neck, and males have greatly enlarged casques. Bycanistes species are distinguishable by their white rumps, and Ceratogymna species by the throat wattles of loose skin. Habitat. All but II of the 45 species occupy forest of one type or other, although some of these (in Tockus, Bycanistes and Anthracoceros) show wide habitat tolerance and may be found along forest edge and in riparian woodland extending into savanna areas. The savanna species (9 Tockus, 2 Bucorvus) are found in habitat ranging from woodland to arid grassland and even semi desert in south-west Africa where Monteiro's Hornbill Tockusmonteiri occurs. All are confined to Africa except the Indian Grey Hornbill Tockus birostris. Distribution. There are 22 horn bills in the Afrotropical region, 19 in the Oriental region and 4 species in the Australasian region. The genera Tropicranus, Bycanistes, Ceratogymna, and Bucorvus are African. The majority of Tockus species are African but 2, not considered closely related, are Oriental. The remaining genera are Oriental, with representative species in Rhyticeros (3) and Penelopides (1) extending into the Australasian region. Two species of Rhyticeros (the Narcondam Hornbill R. narcondami and Sumba Hornbill R. everetti) have a very restricted range, each confined to a South East Asian island. A fossil hornbill is known from Germany. Movements. Most species seem to be sedentary and territorial throughout the year. Some savanna Tockus species form into flocks in the non-breeding season, moving locally in search of food, and these movements may entail regular local or altitudinal migrations in some areas. In Nigeria, the resident population of the Grey Hornbill Tockus nasutus in the Sudan zone (1IO-13°N) is joined by immigrants from the

phic, have similar calls and tail patterns to Anorrhinus and both may be

closely linked. Several species of horn bills, the Helmeted Hornbill Rhinoplax vigil, Buceros, and Bucoruus, have oil glands which provide cosmetic coloration for bills, casques and white areas of plumage. In Buceros the yellow and

291

Yellow-billed Hornbill Tockus flavirostris. (N.A.).

292 HornbiU

Guinea zone (8°-11 ON) after breeding there. Frugivorous species in forest, such as Bycanistes, Ceratogymna and Rhyticeros, may never hold territories, ranging randomly over a wide area in search of fruiting trees. Food. Most species are omnivorous, eating fruit as well as small animals. Tockus and Tropicranus species are largely insectivorous, some of them following army ants or troops of monkeys for the insects they disturb. The ground hornbills appear to be entirely carnivorous, catching reptiles, including large and venomous snakes, birds, squirrels, rodents and animals the size of hares. Tortoises are dug out of their shells as well as fossorial toads and beetles from the ground. Their main diet, however, is insects, especially grasshoppers and beetles. Most of the forest species rely on fruit as their main diet but supplement it with any small animal disturbed in the foliage. Many are known to increase the amount of animal prey during the breeding season but this is minimal for Bycanistes and Ceratogymna species. During the nesting period of the Silverycheeked Hornbill Bycanistes brevis, it has been estimated that the male makes 1,600 deliveries of food with average loads of 15 fruits. Food is simply picked up or plucked where found, the long bill being an effective pair of forceps to handle sticky or dangerous items. Some species dig out their food, and the more aerial species hawk or capture food while in flight. Limited observations suggest that Rhinoplax may use its bill in the manner of a giant woodpecker. Only Ceratogymna species have been recorded drinking water and then only twice, once in natural habitat and the other in a zoo. Behaviour. Most species are sedentary and live as pairs within their territory, which ranges from 10ha in small Tockus species to 10,000ha in Bucorous. Some species form flocks during the non-breeding season but these break up into pairs at the beginning of the breeding season. In a few species there are social groups which defend a common territory and breed co-operatively, a breeding pair being assisted throughout the year by other members in defence of the territory and in bringing food to the nest. This is known to occur in Anorrhinus and Bucorous species and probably in some Berenicornis, Buceros and Tockus species. Hornbills display threat by raising the bill and exposing the throat, which is often coloured distinctively, at other times by beating on a log, and occasionally by bill-grappling and fighting. Submission is shown by bowing the head, and often leads on to ALLOPREENING between pairs or group members. Dominance within a group may be mediated by gestures either of food acceptance or its refusal. Several species have special warming postures. Bathing in standing water is unknown, but several species bathe in wet foliage or in rain and so become soaked. The majority of species sunbathe regularly with outstretched wings. Voice. Hornbills are very vocal and have a variety of calls. Most of the smaller species, which are probably the most primitive, utter a series of clucks with the head bowed. They also use high pitched cries and whistles while raising their heads and pointing their bills vertically upwards. These vocal displays are often accompanied either by wingflapping or flicking movements of the tail or head, or by fanning the tail over the back as found in Hemprich's Hornbill Tockus hemprichii and Aceros, 2 unrelated birds. The larger species utter soft hoots (Berenicornis), short barks (Rhyticeros and Aceros), a variety of whistles, wails, clicks and brays (Bycanistes and Ceratogymna), and deep booming noises, usually before dawn, which may be heard at 5 km distance (Bucorvus). Calls of Buceros species and Rhinoplax vigil are given often as duets. The latter has a most striking call, an accelerating series of hoots, breaking into maniacal laughter, which makes it one of the never-to-be-forgotten noises of the Asian forests. Breeding. Apart from the ground hornbills, it is usual for a pair of hornbills to select a natural hole in a tree, sometimes in a rock face, as a nest site. The entrance is sealed to form a vertical slit. In most species this is the task of the female, although males in some species may assist, and in Bycanistes and Ceratogymna they supply the female with specially prepared sealing material. The sealing proceeds in stages, often initially with mud from the outside, until the female is just able to enter the nest hole. The timing of the final entrance of the female, before she seals herself in, is probably determined to some extent by the amount of food she receives from the male during courtship. The male may now pass lining, such as leaves and bark, through the slit to the female and mollusc shells that may be important as a source of calcium for egg production. The sealed nest protects the female and chicks from predators, but, in addition to this, most nests have a long funk-hole above them into which the female and chick can crawl out of reach. Ventilation in the nest is maintained by convection.

Egg-laying may be delayed for several days after the female has sealed herself in, but once started occurs at intervals of a day in Tockus species but at longer intervals in the larger species. Females of Bycanistes, Ceratogymna and Bucorvus species do not moult while breeding but have a normal successive replacement of feathers as do males and non-breeding females. They are, therefore, able to fly at all times and this may be a result of an unpredictable food supply or predation risk, both making flight necessary at times. Although not thoroughly studied, many breeding females of other genera, possibly all, are flightless within a few days of laying because of a rapid moult of rectrices followed by the remiges. A staggered moult of the body feathers also begins. By the time the females leave the nest, their flight feathers are renewed. The breeding of many species is little known and only a few species have been studied thoroughly. Incubation of the white eggs, which are oval and rather pitted, begins with the first egg, and the incubation period ranges from 25 days (Tockus) to 40 days (Bucorvus). Some species lay 1 or 2 eggs, usually 2, but others may lay more (Anthracoceros 3-4, Aceros 3, Penelopides 4, Asian Tockus species 4, and Ptilolaemus 5) and African Tockus species may lay up to 7. The nestling periods range from 45 days (Tockus) to 86 days (Bucorvus). The long breeding periods exclude second broods except in some forest species, which have no fixed breeding season and show co-operative breeding behaviour. Females of Bycanistes remain in the nest with the young and they all emerge together after a period of 4 months or more. In Tockus, Tropicranus, some Anthracoceros and Buceros species the females emerge before the chicks are full grown. In Bucorous the female, when incubating or brooding, is brought food by the male or group members and only leaves the nest 3 or 4 times a day, mainly to defaecate. The chicks hatch at intervals, are naked and blind at hatching, and their upper mandibles are markedly shorter than the lower. Their legs develop rapidly and this enables them to sit and beg for food from the male, rather than from the female inside, and lift their anus, as does the female, to the entrance in order to squirt out their droppings. The nest is kept clean of food remains and debris by throwing these out through the slit; any left is eaten by insects. The feathers on the chicks remain for some time in quill, giving a porcupine-like appearance but, when they burst out, the feathers develop rapidly. In species where the female emerges before the chicks, the nestlings re-seal the entrance themselves (without help from the parents) using their own droppings. The chicks fly as soon as they leave the nest and do not return there. Food is brought to the nest entirely by the male except in those species where the female emerges from the nest before the chick. In Bucorvus members of the group bring food to the nest in addition to the male. Smaller chicks often die of starvation and this seems to be obligatory in Bucorvus and may be so in the other species (Bycanistes, Ceratogymna, Buceros and Rhyticeros) which lay 2 eggs but rear only 1 chick. A.C.K. and L.G.G. Kemp, A.C. 1976. A study of the ecology, behaviour and systematics of Tockus horn bills (Aves: Bucerotidae). Transvaal Mus. Memoir 20. Kemp, A.C. 1979. A review of the hornbills: biology and radiation. Living Bird 17: 105-136. Kemp, A.C. & M.I. 1980. The biology of Bucorous leadbeateri (Vigors) (Aves: Bucerotidae). Ann. Transvaal Mus. 32(4): 65-100. Sanft, K. 1960. Bucerotidae (Aves/Upupae), Tierreich 76: 1-176.

HORNERO: South American substantive name of the true ovenbirds Furnarius spp., especially F. leucopus, now used also as English substantive name (see OVENBIRD (I)). HOST: see BROOD-PARASITISM;

ECTOPARASITE; ENDOPARASITE.

HOT SEARCHING: term used to describe finding nests by working vegetation so as to flush the sitting bird; sometimes after watching it back to the nest area; contrasted with 'cold searching', when the nest is found by close examination of likely habitat. HOUBARA: sometimes used alone as the name of the Houbara Bustard Chlamydotis undulata (see BUSTARD). HOVERING: see FLIGHT. HUET-HUET: Pteroptochos tamii (see TAPACULO). HUlA: Heteralocha acutirostris (see WATTLEBIRD

(2); EXTINCT BIRDS).

Hummingbird

HUMAN IMITATION OF BIRD SOUNDS: for a number of reasons and by a variety of means. Perhaps the commonest form is onomatopoeia, when we speak bird names that are intended to sound like the sounds of the birds, e.g. Cuckoo Cuculus canorus, Chiffchaff Phylloscopus collybita, Killdeer Charadrius oociferus and Bobwhite Colinus virginianus. The human vocal cords can be employed to copy, for example, the song of the male Cuckoo. Imitation may be otherwise effected by whistling through the lips, 'spishing' through the teeth or 'squeaking' by sucking in air between lips held against the back of the hand. By cupping the hands together and blowing between thumbs held parallel and against the lips, calls such as those of the Tawny Owl Strix aluco and the Cuckoo can be reproduced. Among the various 'bird-calls', the commonest is the whistle or pipe. The simplest design is a tube with a mouth aperture and a single outlet hole. Some whistles may have a 'pea' inside or may incorporate a reed. The pipe known as the 'Nightingale' (and used in the music of Scarlatti and Haydn) involves blowing through a container partly filled with water. The small thin circular instruments used, for example, to copy the distinctive wheooo! of the drake Wigeon Anas penelope are sucked rather than blown. Diaphragm callers (e.g. for Wild Turkeys Meleagris gallopavo) are held inside the mouth against the palate. A few whistles have bellows (e.g. the French Quail Coturnix cotumix pipe); or a compressible bulb (the British Quail pipe) both of which are operated with the hands. In the case of a large bellows (as in the American 'Scotch' make of Mallard Anas platyrhynchos call) a foot may be used (thus leaving two hands free for a gun?). Quite different instruments are those that rely on friction for the creation of sound. An Irish Corncrake Crex crex caller comprises two mammalian rib bones; one has saw-teeth, across which the other bone is rhythmically drawn to reproduce the rasping 'song'. The'Audubon' bird call consists of a small cylindrical piece of birch wood into which is inserted (and then turned) a resined small pewter plug; its high-pitched squeaks are reputed to attract song birds. A common design of Wild Turkey call involves scraping a piece of wood across a slate. Box calls are operated by hand; one side of the box is pivoted at one end and elongated at the other to form a handle and its flat side is drawn across an upright edge, the box acting as a resonator. These are used mainly for Wild Turkeys and wild geese. One French company sells 25 different birdcalls, a Brazilian one, 40. Although 'electronic callers' are not strictly relevant they do represent the reproduction of bird sounds by human agency and they have come to replace earlier manual callers. These consist of recordings of real birds reproduced from a disc or tape on a portable battery-operated gramophone or player. The use of this method for hunting is now illegal in the USA and Britain. Siffleurs use a sifHer-'a song whistle' with a moveable 'plunger'-to give generalized impressions of bird song accompanying music. The copying of birds in human music is done with conventional instruments, or (recently) with synthesizers for radiophonic music. One recent and highly original example of human imitation of bird voice combines the simplest with the most sophisticated technique: human vocal mimicry recorded on tape and then electronically enhanced to increase its verisimilitude before being published on disc and cassette as an identification aid for birdwatchers (Ward et al 1980). Primitive peoples imitate birds, either in their ceremonies, or to locate or decoy them. For example, the American Indians of the north-west Pacific coast have a dance in which they imitate the voice and the actions of the Raven Corvus corax. The Cree Indians use callers to decoy Canada Geese Branta canadensis. The Esquimo of the Canadian Belcher Islands attract them vocally. There is a published recording of the Kayabi tribe of the Paranatinga River in the Matto Grosso of Brazil mimicking 4 species of bird. Tribespeople in Laos use a bird-call fashioned from bamboo to attract the Bamboo Partridge Bambusicolafytchii within range of a weapon. Whistles made from bone and found in a few prehistoric sites in Europe, and more commonly across North America, may well have been used for the purpose of attracting birds. Indeed, whistles similar to those found by archaeologists in New Mexico were still used by the Pueblos to lure Wild Turkeys in the early 20th century. Present day hunters use a variety of means to decoy their quarry, but nowhere more elaborately than in North America, where the sales of duck and goose calls and, most of all, of Wild Turkey calls must be considerable. Schorger (1966) gives a detailed account of turkey calling from prehistoric times to the present day. Not only are the food species decoyed, so too are so-called 'vermin'. Hunters may copy the species they

293

are pursuing or they may attract them by mimicking a predator that the birds assemble to mob. Thus plumage hunters in Trinidad used to call up hummingbirds by mimicking the call of a local owl. Human imitations are usually intended to attract the birds but, in the case of dove calling, they merely cause the bird to answer from its perch and thus give away its location to the hunter. Bird-trappers on the south-west coast of France, and no doubt elsewhere, lure birds to the catching areas of their clap nets with a decoy whistle. For bird-watchers to call up owls for a better view is comparatively simple, and in North America 'spishing' and 'squeaking' are commonly employed, usually to put wild birds on view for the purpose of identification, and occasionally to census (Smith 1975, Tucker 1978). The reproduction in the field of tape recordings is widely used, e.g. for censusing and ringing. For example, Swallows Hirundo rustica approaching a roost location before sunset can be very effectively drawn in the direction of the ringer and his mist net by playing the 'Swallow roost twitter' recording. Even more remarkable is the success achieved by reproducing from coastal headlands at night the purring call of the Storm Petrel Hydrobates pelagicus. Although well away from nesting colonies, 3 workers in 6 years mist-netted 16,000 birds (Fowler et al1982). The use of tape PLAYBACK in the breeding season, particularly with rare species, needs scientific investigation to determine how easily, if at all, harm may be done. Bird impressionists--notably in mid 20th century Britain, Percy Edwards--provided entertainment on stage, radio and television. Gramophone records of avian imitators have been issued surprisingly often since the earliest one in 1891 (Copeland and Boswall 1983). Mechanical birds that sang from little French enamel boxes appeared in the late 18th century in France, and 'automaton' mechanical caged birds were no doubt a familiar sight in Victorian drawing-rooms. Two of the jewelled eggs of Imperial Russia were designed by Faberge to feature birds (a Nightingale Luscinia megarhynchos and a cockerel) that appeared by clockwork to offer the world mechanical utterances. The direct imitation by human composers dates from the 13th century and is dealt with in detail under MUSIC, BIRDS IN. See also SCARING and VOCALIZATION. J.H.R.B. Becker, A.C. 1972. Game and Bird Calling. South Brunswick. Boswall, J. & Barton, R. 1983. Human imitation of bird sound. Recorded Sound 83: 57-73. Copeland, P. & Boswall, J. 1983. A discography of human imitation of bird sound. Recorded Sound 83: 73-100. Fowler, J.A., Okill, J.D. & Marshall, B. 1982. A retrap analysis of Storm Petrels tape-lured in Shetland. Ringing and Migration 4(1): 1-7. Humphreys, J. 1979. Hides, Calls and Decoys. London. Schorger, A.W. 1966. The Wild Turkey. Oklahoma. Smith, N. 1975. 'Spishing' noise: biological significance of its attraction and non-attraction by birds. Proc. Nat. Acad. Sc. USA 72(4): 1411-1414. Tucker, J. 1978. Swishing and squeaking. Birding 10(2): 83-87. Ward, J., Haven, A. & Bland, B. 1980. Big Jake Calls the Waders. LP or tape cassette.

HUMERUS: a bone of the fore-limb (see SKELETON, POST-CRANIAL; The flight feathers ('tertials') borne on this part of the limb are sometimes called 'humerals',

WING).

HUMIDITY: see WEATHER

AND BIRDS.

HUMMINGBIRD: substantive name of many species of Trochilidae (Apodiformes); in the plural general term for the family. The name derives from the noise made by the wings when hovering. Characteristics. All hummingbirds feed by extracting nectar from flowers with their specialized tongues and usually elongated bills and nearly all hover while doing so. This feeding method accounts for the most striking characteristics of the family. These are: wings adapted for hovering both forwards and backwards, long bills, and very small legs and feet. In addition most hummingbirds have brilliant glittering or iridescent plumage. Hummingbirds are mostly small (6-13 em long) and range in weight between 2 and 9 g. Two genera with specialized bills, Ensifera and Eutoxeres, are larger (12-13 g), and the substantially larger Giant Hummingbird Patagona gigas weighs 20 g. The wing structure of hummingbirds differs from other birds, except swifts, by a great reduction in length of the humerus, radius and ulna and an elongation of the hand bones to which the flight feathers are attached. This modified wing moves freely in all directions at the shoulder

294 Hummingbird

attachment so that a rotary movement is possible. The wing-beat rates of hummingbirds vary between 22 and 78 per second (Greenewalt 1962); and they have a forward speed in level flight of about 45 km/h. The high wing-beat rate, small size and high temperature (39-42°C) means that hummingbirds have a high rate of metabolism, requiring the frequent intake of energy-rich food. In order to conserve energy, hummingbirds are capable of becoming torpid at night when their temperature falls close to that of the surrounding air. Most hummingbirds show striking sexual dimorphism, the females having a relatively plain, and the males a more brilliant, plumage, with glittering patches particularly on the throat and crown. In some species males have other special adornments, such as elongated and brilliant tail feathers and crests. In most of the hermit hummingbirds, sometimes placed in a separate subfamily Phaethorninae, the sexes are the same or only slightly different in plumage; this is also true of the violet-ears Colibri and many emeralds Amazilia. The 320 species of hummingbird have been placed in 112 genera, 63 of which are represented by only a single species. Eighty-eight genera occur in South America and 24 additional genera occur to the north, mostly in middle America but also the Caribbean islands and North America. Habitat. Hummingbirds occupy a wide range of habitats from the open paramos of the Andes, over 4,000 m, to the tropical forests of Amazonia, arid scrublands and coastal mangrove swamps. Most species are resident, but a few migrate to breed in such diverse habitats as the deserts of Arizona and the coniferous forests of Canada and Alaska. The essential ingredient of all these habitats is a sufficient abundance of nectar-secreting flowers to supply the energy which the birds need. Although a large and variable proportion of insect food is taken by hummingbirds, most habitats are soon deserted when flowers become scarce. While most hummingbird nests are small simple cups which may be sited in almost any vegetation and even on overhead electric wires, a few species have more exact nest-site requirements. Thus the hillstars Oreotrochilus of the high Andes require a cave roof or a rocky overhang on which to affix their pendent nests. The long-billed hermit hummingbirds of the forests (Phaethorninae) attach their pendent nests to the underside of large tapering leaves such as palms or the wild banana H eliconia spp, While this type of leaf is abundant in unaltered forest habitat, it may be absent from areas highly modified by man so that they become largely unsuitable for the Phaethorninae. Distribution. Hummingbirds occur only in the New World, where they range from Alaska and Labrador in the north to Tierra del Fuego in the south, and from Barbados in the east to the Juan Fernandes group of islands 650 km from the western seaboard of Chile. Very few species, however, occur at high latitudes, the Green-backed Firecrown Sephanoides sephanoides in the south (to c. 54°S) and the Rufous Hummingbird Selasphorus rufus (c. 600 N ) and the Ruby throat Archilochus colubris (c. 54°N) in the north. The great majority of species inhabit the latitudes between lOON and 25°S, with the greatest diversity in Colombia and Ecuador. Of the 88 South American genera, 5 genera with 8 species occur in the arid coastal zones of the western and northern seaboards, 41 genera with 119 species occur mainly at tropical levels (sea level to 1,525m), 15 genera with 26 species occur mainly at subtropical levels (1,525-2,580 m, also including 4 genera inhabiting subtropical habitats due to latitude), and 19 genera with 62 species occur mainly at temperate levels (2,5803,500 m) with the monotypic S ephanoides occupying a temperate habitat due to latitude. The number of species decreases sharply in the paramo and puna zones (from the tree line up to the snow line); here 3 genera, Oreotrochilus, Oxypogon and Chalcostigma, show special adaptations to high altitudes (Carpenter 1976) but some temperate-zone species make seasonal visits. This breakdown of species by habitat shows the importance of the Andean mountain range for hummingbird speciation; no other bird family is represented by so many species at temperate levels in the Andes as are the Trochilidae. Within the Trochilidae there is great variation in the geographical range of different species. The Brown Violetear Colibri delphinae, for example, is nowhere abundant but ranges from Guatemala to Bolivia at subtropical and tropical levels. Others have extremely restricted ranges, such as the Spatule-tail Loddigesiamirabilis which is known only from the temperate zone of one valley in Peru. Further species with restricted ranges may yet be discovered. As recently as the 1970s, a new species of sunangel, Heliangelus regalis, was discovered at subtropical levels in one

locality in N. Peru and a metaltail, M etallura odomae, at temperate levels in one range in N. Peru. Movements. The few hummingbird species that breed at high latitudes undertake long migrations. The Ruby throat of eastern N. America migrates for the winter to middle America, reaching as far as Panama. For some populations this journey includes a 1,000 km crossing of the Gulf of Mexico. The Rufous Hummingbird, which breeds attfar north as Alaska, winters in southern Mexico 3,500 km away. The Green-backed Firecrown, which breeds as far south as the Straits of Magellan, moves north in the southern winter, some birds at least as far as 23°S. Besides long-distance movements, many species of hummingbird make more local movements in response to the flowering season of nectar-rich flowers. This has been well documented for the Anna Hummingbird Calypte anna in the Santa Monica mountains of California, with its winter breeding season in the chaparral linked to the flowering of a species of Ribes, followed by a movement in mid-summer to the high mountain meadows. In the highlands of Costa Rica (2,950-3,200m) 4 species of hummingbird breed, but only one, Panterpe insignis, is present in large numbers throughout the year; the other 3 species make seasonal movements related to flower abundance (Wolf et al 1976). At much higher altitudes around 4,000 m on the altiplano of Peru the Sparkling Violetear Colibri coruscans is present only in the summer and migrates to lower altitudes in the winter (Carpenter 1976). In rain forest at tropical levels most hummingbird species appear to be sedentary. This has been proved by marking individuals of the Hairy Hermit Glaucis hirsuta and Guy's Hermit Phaethornis guy in Trinidad, and the Long-tailed Hermit P. superciliosus in Costa Rica. Food. The diet of hummingbirds consists of nectar supplemented with insects and sometimes spiders. This is true of all species that have been studied in any detail but the proportion of insect to nectar food, the method of capturing insects, the flowers from which nectar is extracted and the behavioural factors which secure this nectar supply, are extremely varied. This variation allows a very large range of feeding niches, which must be the major factor accounting for the large number of hummingbird species. The structure of hummingbird flowers, especially the length and shape of the corolla tube, is in many cases adapted to permit exploitation by particular kinds of hummingbirds, which pollinate the flowers while feeding at them. A large number of plant genera in the Americas have flowers adapted for pollination by hummingbirds, among the most important being Heliconia, Passifiora and many genera in the families Bromeliaceae and Gesneriaceae. In several plant genera there is a clear distinction between insect-pollinated species (presumed to be the primitive condition) and species with longer, usually red, corolla tubes adapted for pollination by hummingbirds. (See also POLLINATORS. )

One of the major divisions in feeding methods is between territorial and trap-line feeding. For territorial behaviour to develop, a flower species must provide sufficient nectar to fulfil the energy needs of an individual hummingbird in an area small enough to defend from other nectar feeders. Medium-sized hummingbirds with medium-length bills, such as the emeralds Amazilia at tropical levels and the sunangels Heliangelus and pufflegs Eriocnemis at subtropical and temperate levels, are typical territorial feeders. Trap-line feeders do not defend a nectar resource but travel round visiting scattered flowers rich in nectar. Typically they are hummingbirds with long bills which may be curved, and most show a high degree of co-evolutionary development with the flowers they visit, which have correspondingly long or curved corolla tubes. The hermit hummingbirds are typical trap-line feeders. An advanced degree of co-evolutionary development is shown between 2 hummingbird genera with the most extreme bills, the Swordbill Enstfera with a bill length which may exceed 100mm and the sicklebills Eutoxeres with extremely curved bills, and the flowers they visit, which have respectively extremely long and extremely curved corollas. The nectar in such flowers is not available to other hummingbirds if they use the legitimate corolla aperture, but a few genera, e.g. Heliothryx, have evolved short and exceptionally sharp bills and habitually pierce long or curved corolla tubes to gain access to the nectar. In addition to the relatively large, long-billed trap-line feeders, many small hummingbirds, with relatively small unspecialized bills, trap-line feed at insect-pollinated flowers or the less specialized hummingbird flowers which are too scattered to be defended by territorial hummingbirds.

Hummingbird

In North America 4 species of hummingbird are known to take sap from trees where it is made available by sap-sucking woodpeckers (Picidae); and hummingbirds have also been recorded taking juice from ripe fruit. Hummingbirds employ 2 methods of capturing insects: hawking insects in flight, and gleaning resting insects and spiders from the vegetation and from spider's webs. The hermit hummingbirds, nearly all of which have curved bills, employ the gleaning method almost entirely, hovering to search the undersides, edges and tips of leaves low down in the forest or in the middle canopy. A specialized form of insect gleaning while clambering over the ground is employed by 3 species of hummingbirds inhabiting the high Andes, where the bare hillsides are suitable for such methods and the energetic cost of hovering in the thin cool air is particularly heavy. Hawking for airborne insects has been observed in many straight -billed species, some of which also glean for resting insects in the same way as hermit hummingbirds. Hawking is especially prevalent among species with relatively long wings and short bills such as the Green-tailed Trainbearer Lesbia nuna and the Buff-tailed Coronet Boissonneaua flavescens. Methods and vantage points for hawking vary between species, some species using high exposed perches above the canopy, and others lower perches near or within vegetation or in the open. Some species catch a single flying insect at a sally, others make a number of captures per sally or attempt to do so. Behaviour. Hummingbirds are polygamous, the males advertising themselves by song and display either at traditional leks (singing assemblies) or at more scattered song posts or at their feeding territories. Spectacular aerial diving displays are characteristic of species that inhabit open country, as in North America. The female's visits to advertising males culminate in copulation. In all except one of the species that have been studied, the female builds, incubates the eggs and rears the young unaided by the male. The exception is the Sparkling Violetear. Males of this species are reported to guard the nest, and one took over incubation when the female was shot at the nest (Moore 1947). At another nest 2 adults shared incubation; one of them the observer believed to be the male (Schafer 19'54). A LEK mating system is usual among species, such as many of the hermits, that feed by trap-lining. The size of leks varies greatly; T.A.W. Davis noted assemblies of 100 or more Long-tailed Hermits in Guyana, while a lek of the same species in Costa Rica censused for 5 years varied between 14 and 23 males (Stiles and Wolf 1979). Leks of the Reddish Hermit Phaethornis ruber may consist of only 5 males, and the Barbthroat Threnetes ruckeri may sing at solitary perches or within sound of 1 or 2 conspecifics. Within a hermit hummingbird's lek, each male defends several song perches, which are slender horizontal twigs in the undergrowth. Song, display, territorial encounters with other males and copulation take place on or near these perches. During courtship and other encounters, the plain-coloured hermits nearly all display their brightly coloured gapes. The many species with brilliant plumage and iridescent patches display these, usually when airborne. In the Purple-throated Carib Eulampis jugularis mating takes place within the male's feeding territory where the female is permitted to feed prior to copulation (Wolf 1975). The male Hairy Hermit forms loose pair-bonds with one or two females that nest along a section of stream side which he defends from other hermits (Snow and Snow 1973). Prior to mating, the female Andean Hillstar Oreotrochilus estella feeds the male in her territory. In this species only females hold territories in the breeding season. Voice. Both male and female hummingbirds call in flight. Flight calls are usually monosyllabic, lasting about half a second; they are uttered by a bird flying alone and not near leks or assemblies. It is characteristic of hummingbirds which defend floral feeding territories to utter a brief monosyllabic note between feeding probes. Many species utter a chase call, a chattering series of rapid notes uttered when attacking and chasing intruders at their feeding territories or at lek territories. There are strong aggressive elements in these two calls, which may be employed by either sex, are particular to a species and appear to be innate. Most hummingbird advertising song is short and simple, lasting from a fraction of a second to 11/2 s. These short songs are frequently repeated, the brief monosyllabic ones typically up to 70 times a minute and the

longer 1-}l/2 s phrases some 30 times a minute. The songs are often of high frequency and sound squeaky and thin to human ears. Some species sing longer more musical songs with longer intervals between them: the Barbthroat has a warbling song lasting 4-5 s and the Wine-throated

295

Ruby throat Archilochus colubris. (N.A.).

Hummingbird Atthis ellioti has a song of nearly a minute's duration. Many species, particularly the Phaethorninae, are extremely persistent singers, and sing throughout much of the day and throughout the often long breeding season. An extremely low-volume continuous warbling sub-song has been heard from many species; recently fledged birds and adults of both sexes may sing this sub-song. Some displays are accompanied by vocalizations not heard at other times. Duet singing, with first the male then the female uttering a phrase, occurs in the Hairy Hermit. All evidence indicates that the advertising song of males is not innate but learnt, becoming fixed in young males probably in their first year. Abnormal songs may apparently be developed by individuals that learn from the wrong species. Skutch (1974) reported a striking example, of a male Amazilia amabilis which for 7 years sang the song of Amazilia tzacatl but at the tempo usual to his own species. In the lek-forming hermit hummingbirds, young males learn the song form of their closest neighbours. Even when the song is a monosyllabic note lasting less than a quarter of a second, as in the Long-tailed Hermit, many audibly distinct forms are sung. One lek of 20 males had 4 distinct song forms, adjacent males all singing alike. Breeding. The unaided female builds the nest, incubates the eggs and rears the young. Throughout the Trochilidae the clutch consists of 2 eggs which are always white and of an elongated shape; there is normally a 48-hour interval before the second egg is laid. In two hermit hummingbird genera Glaucis and Threnetes, nests with 3 or 4 eggs are not uncommon; these are apparently attributable to more than one female. There are 2 basic nest-types. The commoner, built by all species except the Phaethorninae and some cave-nesting species, is a small compact open cup placed astride a stem or twig. The nest is composed of .vegetable down and sometimes moss and is bound together and to its support with cobweb. The Phaethorninae build pendent nests which are fastened by cobweb to the underside of a blade-shaped leaf or strip of leaf, so that the leaf forms the inner wall. The nest tapers to a tail, to which twigs and debris are attached to act as a balancing weight. Species that nest in caves and buildings, such as the hillstars, have thick-walled pendent nests attached to the rock by a glue. The only known nest of the Blue-fronted Lancebill Doryfera johannae was also pendent and attached by cobweb to a rocky overhang near the bottom of a 75 m shaft. Normally hummingbirds nest solitarily except those that need specialized nest-sites such as caves. Incubation begins when the second egg is laid and ranges from 14-19 days. The altricial young are sparsely covered with down at hatching, and are brooded frequently, but by 8-12 days brooding ceases even at night. Small nestlings defaecate in the nest and the female removes the droppings, older nestlings defaecate over the rim of the nest. The female regurgitates food to the young, inserting her bill into their throats. Fledging periods vary between 18 and 28 days. H.O. Wagner, studying the Green Violetear Colibri thalassinus in Mexico, found the fledging period varied from season to season with different weather conditions. The female continues to feed the young after they have fledged, the longest recorded period being 41 days (Skutch 1974). Hummingbird breeding seasons are linked with the flowering seasons of their main sources of nectar. In the far north and south of their range the main flowering seasons have a simple relationship with day length and temperature, corresponding to the northern and southern summers. At 34°N in California, 2 migratory species have a typical northern breeding season starting MarchiApril with a peak in May, while the nonmigratory Anna Hummingbird has a peak of breeding from January to March coinciding with the peak of precipitation in this dry region and the peak flowering season of 2 species of Ribes (Stiles 1973).

296 Hunger trace

In the humid tropics and subtropics the hummingbirds which build open cup nests liable to saturation do not nest at the peak of the rainy seasons when day-long rain may occur. This group of hummingbirds breeds mainly in the dry season, but not towards the end of a long or severe one when flowers become scarce. The beginning and end of rainy seasons, when both sun and rain are usually intermittent, are important breeding periods as hummingbirds are well able to protect the nest and its contents for limited periods of rain. The nests of hermit hummingbirds are protected from rain by the living leaf to which they are attached, so excessive rain is not a limiting factor of the breeding season. Thus at 600-900 m in Costa Rica the Hairy Hermit and the Barbthroat nest almost entirely in the rainy season (Skutch). In the lowlands of Costa Rica the Long-tailed Hermit breeds from January to August, well into the wet season. In Trinidad the Hairy Hermit also breeds from January to August, which spans the main dry season, but with a peak of laying in the first 2 months of the wet season. Nests of Guy's Hermit in the same locality were found in all months except August to October. All these hermit breeding seasons show correlations with the flowering of the mainly herbaceous plants on which these species feed. Individual female Hairy Hermits and Guy's Hermits in Trinidad may make 3 nesting attempts in a season, as deduced from the reuse of repaired nests. A female Anna Hummingbird in California successfully raised 2 broods in a season, as did a Black-throated Mango Anthracothorax nigricollis in Trinidad. B.K.S. See photo FEEDING HABITS. Carpenter, F.L. 1976. Ecology and evolution of an Andean hummingbird (Oreotrochilus estella). Univ. Calif. Publ. Zool. No. 106. Grant, K.A. & Grant, V. 1968. Hummingbirds and their Flowers. New York. Greenewalt, C.H. 1962. Dimensional relationships of flying animals. Smithson. Misc. ColI. 144: 1-46. Moore, R.T. 1947. Habits of male hummingbirds near their nests. Wilson Bull. 59: 21-25. Schafer, E. 1954. Sobre la biologia de Colibri coruscans. Bol. Soc. Venez. Ci. Nat. IS: 153-162. Scheithauer, W. 1967. Hummingbirds. London. Skutch, A.F. 1974. The Life of the Hummingbird. London. (Includes references to earlier work.) Snow, D.W. & Snow, B.K. 1973. The breeding biology of the Hairy Hermit Glaucis hirsuta in Trinidad. Ardea 61: 106--122. Stiles, F.G. 1973. Food supply and the annual cycle of the Anna Hummingbird. Univ. Calif. Publ. Zool. No. 97. Stiles, F.G. & Wolf, L.L. 1979. Ecology and evolution of lek mating behavior in the Long-tailed Hermit Hummingbird. Orn. Monogr. (A.O.V.) No. 27. Wolf, L.L. 1975. Female territoriality in the Purple-throated Carib. Auk 92: 511-522. Wolf, L.L., Stiles, F.G. & Hainsworth, F.R. 1976. Ecological organization of a tropical highland hummingbird community. J. Anim. Ecol. 45: 349-379.

HUNGER TRACE: see HUNTING: see

genetically distinct subspecies; the hybrids are variable, occurring in a hybrid zone that both genetically connects and geographically separates the parental SUBSPECIES. Generally, the more distantly related 2 species are, the more dissimilar they are genetically and hence the less likely they are to hybridize. Under captive conditions, and in the wild at borders of the ranges of species where choice of mates may be restricted, barriers to interbreeding can break down, resulting occasionally in hybridization. Another factor that promotes hybridization is mating systems in which pair formation occurs rapidly and males take no part in the nesting effort, as in many ducks, birds-of-paradise and hummingbirds (see also PAIR FORMATION). Hybrids between species that manage to interbreed, despite behavioural or other factors tending to reduce mixed pairing, may be eliminated at various stages of development, from the period of fertilization onward. There is usually reduced fertility of the eggs of hybridizing individuals, and hybrid embryos often fail to develop to hatching. Anomalies often occur in hybrids that do hatch, reducing their chances of survival and breeding. Those hybrids that survive vary greatly in their degree of viability. They may be intermediate in their morphological, behavioural and other characteristics between those of their parents, but often show a variable array of traits, some like one or other parent, some intermediate, and others occasionally unlike either parent. Hybrids that do survive may exhibit 'hybrid vigour', being larger, or stronger, or faster growing, or more aggressive than either parental species, but as they usually have reduced viability, this prevents or limits introgression (passage of genes from the gene pool of one species into that of another). Fertile interspecific hybrids seem more frequent in some orders of birds than in others, and certain large genera such as Anas, that contain a number of relatively closely related species, show numerous natural hybrids as well as hybrids produced under captive conditions. Although hybrids are of behavioural, physiological and genetic interest they are of little significance in terms of evolution unless they exhibit some degree of fertility and backcrossing occurs. Frequent hybridization with backcrossing is significant in an evolutionary sense to the degree that the interbreeding allows gene flow, giving the gene pool of each parental species some access to favourable genes and gene combinations of the other species. There is no more recent list of bird hybrids than that of A.P. Gray (1958), although reports treating various aspects and occurrences of hybrids and hybridization are frequent in ornithological literature. Mayr and Short (1970) analyzed the North American avifauna of 516 breeding non-marine birds and found 24 cases of interspecific hybridization and 30 instances of intraspecific hybridization involving a total of 73 species, roughly 10% of all North American species. L.L.S. Gray, A.P. 1958. Bird Hybrids: a Check-list with Bibliography. Farnham Royal. Mayr, E. & Short, L.L. 1970. Species taxa of North American birds: a contribution to comparative systematics. Publ, Nuttall Ornith. Club, No.9, pp. 1-127.

PLUMAGE, ABNORMAL.

FEEDING HABITS.

HWAMEI: Garrulax canorus (see

BABBLER).

HYBRID: term used to denote the product of a cross between individuals of unlike genetic constitution, usually distinct morphologically. It is often restricted to a cross between individuals of different species, but this begs the question of the taxonomic status of the forms before one can designate the products of their crossing. Genetically the term denotes a first generation product but in practice it is impossible under field conditions to distinguish such F 1 hybrids from second generation hybrids (resulting from a cross between hybrids) and from backcross products, i.e. individuals resulting from crossing hybrids with individuals of the parental forms (see GENETICS). Interspecific and intraspecific hybrids are generally uncommon but may involve some 10% of the world's bird species. Interspecific hybrids between distantly related species that occur sympatrically are rare, but are usually easily distinguishable, and readily come to the attention of ornithologists. More common are hybrids between closely related species, either in zones of parapatry (where their ranges meet) or in zones of overlap and hybridization between geographically replacing allospecies that together form a superspecies (see HYBRIDIZATION, ZONE OF SECONDARY; INTROGRESSION; SPECIATION). Intraspecific hybridization results in zones of secondary contact between morphologically and

HYBRIDIZATION, ZONE OF SECONDARY: an area in which 2 or more closely related forms contact and interbreed with backcrossing, having earlier differentiated under conditions of geographical isolation (see SPECIATION). It is not clear that the isolation need be complete, as strong selection could counter gene flow if the contact between the differentiating forms is restricted. Such zones are characterized by great individual variability. Short (1969) classed these zones into 2 types: a zone of overlap and hybridization, and a hybrid zone. The zone of overlap and hybridization involves forms that hybridize to a greater or lesser degree, but the hybridization is incomplete, both parental forms occurring along with the hybrids. In this case the 2 forms remain sympatric and the continued occurrence and in some instances the preponderance of parental-type individuals indicate the presence of some barrier to interbreeding, or hybrid breakdown-the forms are considered to represent hybridizing species, designated allospecies, and together these allospecies form a superspecies (Amadon 1966). The hybrid zone is an area of greater or lesser extent populated entirely by hybrids between well-differentiated but freely interbreeding forms. This type of zone both genetically connects and geographically separates the parental forms, which are conspecific. The conspecific hybridizing forms often are so distinct that they have been considered full species at one time or another, and Amadon and Short (1976) have designated such differentiates as 'megasubspecies'.

Hypocolius

297

Examples of zones of overlap and hybridization are rather numerous and include those involving the Rose-breasted Grosbeak Pheucticus ludovicianus and Black-headed Grosbeak P. melanocephalus, and the Mallard Anas platyrhynchos and the American Black Duck A. rubripes in North America, and the Azure Tit Parus cyanusand Blue Tit P. caeruleus in Europe. Hybrid zones occur between the megasubspecies cafer and auratus of the North American Northern Flicker Colaptes auratus, and between the megasubspecies cornix and corone of the Carrion/Hooded Crow Corvuscorone, of Eurasia. The extent of these zones depends upon a variety of factors, not the least of which is the availability of characters used in defining the zone. When characters are few, as in the case of the crows, the zone defined by the one or two characters may be narrow. The use of other, especially biochemical characters may show that the zones actually are broader than they appear, as has been found in lizards and other animals. Topographical and ecological factors may severely limit the possibility of contact and thus affect the size of the zone. There are several cases of range expansion that increase the area of a zone of overlap and hybridization, in the course of which hybridization is prevalent mainly at the edge of the range of the expanding species, followed by lessened interbreeding in the area of overlap, as in Parus caeruleus-cyanus, and in the European Syrian Woodpecker Dendrocopos (Picoides) syriacus, and Great Spotted Woodpecker D. major. Another peculiar situation is that of a range extension with very frequent hybridization accompanying it, followed by replacement of one species by the other, the example here being that of the Blue-winged Warbler Vermivora pinus, hybridizing with and largely or entirely replacing the Golden-winged Warbler V. chrysoptera in eastern North America (see also

by the propensity of the Herring Gull to interbreed with the Glaucouswinged Gull L. glaucescens in western North America, with the Glaucous Gull L. hyperboreus in Iceland, and with the Slaty-backed Gull L. schistisagus in eastern Siberia. The matter of hybridization is of great interest and is directly involved in the matter of defining species (see SPECIATION). Many of the situations are highly dynamic and subject to modification through man's effects on habitats. Mayr and Short (1970) note that many hybridizing species of temperate regions seem biologically very successful, even in the face of man's activities. L.L.S.

RANGE CHANGES).

HYPAXIAL: see MUSCULATURE.

A few situations are so complex as to defy any attempt to categorize them. The Rufous-sided Towhee Pipilo erythrophthalmus, and Collared Towhee P. ocai, are 2 strikingly differently plumaged finches, the former occupying much of North America and the latter inhabiting highlands of Mexico. In Mexico there is generally an ecological and altitudinal separation of the 2 forms, but they meet in many places with varying outcomes. In a few small areas they occur together, overlapping in range without interbreeding. In many areas they hybridize apparently freely, forming hybrid zones. Some entirely hybrid populations are geographically isolated, forming 'hybrid swarms' totally out of genetic contact with their parental forms. Certain of the hybrid swarm populations show by their distribution and gradation of their average characters the effects of a hybrid zone, but with geographical gaps among the isolated populations. The diverse situations probably reflect differences in the time of occurrence of the contacts relative to the development of reproductive isolating mechanisms, although some may have occurred as the result of a local breakdown in reproductive isolation. The Crimson Rosella Platycercus elegans of wet eastern and southeastern Australian woodlands and the Yellow Rosella P. flaveolus of the interior Murray River system meet and sporadically hybridize west and north of Australia's Great Dividing Range. The range involved is massively modified by man's activities, but at least one tenuous hybrid zone exists between them along the Murrumbidgee River. In South Australia's Adelaide Hills and the Flinders Range occurs a variable population that clearly represents a huge hybrid swarm; often treated as a species, the 'Adelaide' Rosella P. adelaidae, this population interbreeds freely but narrowly with the Yellow Rosella, destruction of habitat limiting the contact possibilities near the lower Murray River. There is no extant contact between the'Adelaide' Rosella and the Crimson Rosella but 'Adelaide' Rosellas grade from yellowish in the north to red in the south, tending strongly toward P. elegans. This situation has been regarded by some as a 'ring' in which the extremes ({laveolus and elegans) are connected by an intermediate population but do not interbreed at the ends of their ranges (in the east). Actually the 'ring' is broken in the lack of contact of 'adelaidae' with elegans, and elegans and flaveolus do hybridize in eastern Australia, so they appear to represent well-differentiated megasubspecies. A true ring of races appears to exist between the Herring Gull Larus argentatus and the Lesser Black-backed Gull L. fuscus. These are sympatric in parts of northern Europe, and usually do not interbreed. However, from eastern Europe across Siberia to North America occur connecting, interbreeding populations, and thus the northern European situation would seem to represent the non-interbreeding ends of a chain of genetically connected populations. All of the connections have not been thoroughly studied and the complexity of this problem is enhanced

Amadon, D. 1966. The superspecies concept. Syst, Zool. 15: 245-249. Amadon, D. & Short, L.L. 1976. Treatment of subspecies approaching species status. Syst. Zool. 25: 161-167. Gill, F.B. 1980. Historical aspects of hybridization between Blue-winged and Golden-winged warblers. Auk 97: 1-18. Mayr, E. & Short, L.L. 1970. Species taxa of North American birds. A contribution to comparative systematics. Publ. Nuttall Ornith. Club, No.9, pp. 1-127. Short, L.L. 1969. Taxonomic aspects of avian hybridization. Auk 86: 84-105. Sibley, C.G. 1954. Hybridization in the Red-eyed Towhees of Mexico. Evolution 8: 252-290.

HYDROBATIDAE: see under

PROCELLARIIFORMES; PETREL.

HYLIA: substantive name of Hylia prasina, an African warbler-like bird of uncertain affinities. HYOID: see MUSCULATURE;

SKELETON, POST-CRANIAL; TONGUE.

HYPHENS: as regards their use in vernacular or scientific names of birds, see NAME, ENGLISH; NOMENCLATURE. HYPOCOLIINAE: see BOMBYCILLIDAE; and below. HYPOCOLIUS: generic name used as common name of Hypocolius ampelinus, sole member of subfamily Hypocoliinae of the Bombycillidae (Passeriformes, suborder Oscines); an aberrant species placed near the waxwings (see under BOMBYCILLIDAE). Its home is south-western Asia, whence irregular migrations take place to north-western India and perhaps casually to north-eastern Africa. Characteristics. The plumage is pale grey, tinged blue on the back and buff on the forehead and underparts. A black band extends from the bill through the lores and round the back of the neck, where it can be erected into a small crest. The primaries are black, tipped white; the tail is grey, tipped black. Females lack the black on face and neck. Juveniles are buffy-brown without black markings, except for the tips of the rectrices; the tips of the remiges are marked buff as well as white. The Hypocolius is about 23 cm in length with a long tail and short, broad, slightly hooked bill; the feet and legs are short and strong. The wings are relatively short and rounded; the tenth primary is relatively

Hypocolius Hypocolius ampelinus. (C.E.T.K.).

298 Hypocolius

longer than in the waxwings. The flight is strong, swift and direct, not undulating, but the birds are sluggish, shy and sociable except in the breeding season. Fruits and berries are staple foods, although insects are also taken. Voice. Vocalizations include mewing calls, associated with pair formation, and a continuous loud kimkimkim, uttered by pairs during courtship flights over the nesting territory. Breeding. Nests have been found in the Tigris-Euphrates valley of Iraq and in south-western Arabia. Large and loosely built of twigs, they are lined with soft vegetable matter and sometimes hair, like those of waxwings; they are usually well hidden among the leaves of palm trees, but sometimes in other bushy trees. The 4--S eggs are laid in mid-June and the parents are prone to desert if disturbed. The eggs are very pale slaty grey, with darker blotches and spots at the larger end; occasionally (J.e.G. Jr). D.W.S. (1) these form a ring or cover the whole egg.

Bunni, M.K. & Siman, H.Y. 1979. Pair formation and courtship activities in Grey Hypocolius, HypocoliusampelinusBonaparte. Bull. Nat. Hist. Res. Centre, Univ. Baghdad 7(3): 73-82. Delacour, J. & Amadon, D. 1949. The relationships of Hypocolius. Ibis 91: 427-429. Meinertzhagen, R. 1954. Birds of Arabia. Edinburgh.

HYPOPHYSIS: the pituitary gland (see

ENDOCRINOLOGY AND THE

REPRODUCTIVE SYSTEM).

HYPORACHIS: see AFTERSHAFT. HYPOSITTIDAE: a monotypic family separated by some authors, but of doubtful affinities and now provisionally merged with the Vangidae (for family see VANGA). HYPOTHALAMUS: part of the forebrain (see

NERVOUS SYSTEM).

I IBIDORHYNCHIDAE: see

CHARADRIIFORMES; IBISBILL.

IBIS: substantive name for most of the approximately 23 species and 16 genera in the subfamily Threskiornithinae of the family Threskiornithidae (Ciconiiformes, suborder Ciconiae). Characteristics. Ibises are medium-sized water or terrestrial birds, about 50 to 100em in total length, including medium to long legs, long necks, and long, decurved bills. All species have heads that are partially or wholly bare, and some species are crested or have other modified feathers. The wings are relatively long and broad, and the tail is short. The flight is strong and rapid with neck extended. Among the more gregarious species, flocks often fly in long lines or V's with all birds flapping or gliding in unison. Sexes are similar except that the males of some species are slightly larger than the females. Immature birds are often darker than adults, and may be more extensively feathered on the head. Systematic characteristics and distribution. Ibises are widespread in the warmer parts of the world, with 9 genera restricted to the Old World, 6 to the New World, and one that is cosmopolitan. In the Old World, the genus Threskiomis contains 4 species, the Sacred Ibis T. aethiopicus occurring primarily in Africa south of the Sahara, the Straw-necked Ibis T. spinicollis of Australia, the Australian White Ibis T. molucca found between Indonesia and Australia, and the similar Oriental White Ibis T. melanocephalus in southern Asia. The species of Threskiornis are primarily black and white in colour, with entirely bare heads and upper necks. Also in Asia is the Black (or White-shouldered) Ibis Pseudibis papillosa of India, south-eastern Asia and southern China, the Giant Ibis Thaumatibis gigantea of Indo-China, and the Crested Ibis Nipponia nippon of Japan, China, and Korea. The Black and Giant Ibises are dark species, the former having a patch of red papillae on the bare skin of the crown, and the latter characterized by its large size and barred nape and hind neck. The Crested Ibis is white, with the anterior half of the head bare red skin, and a crest of elongate white feathers at the nape. In addition to the Sacred Ibis, 7 other species occur entirely or in large part within Africa. The endangered Waldrapp Geronticus eremita survives as a breeding bird of Morocco and Turkey, while the Bald Ibis G. calvus is restricted to mountains of South Africa. Both are large, dark ibises with strong metallic sheens to their plumage, red bills and entirely bare heads and upper necks. Three crested species are the Olive (or Green) Ibis Lompribis olivacea, the Spotted-breasted Ibis L. rara and the Crested Wood Ibis Lophotibis cristata, endemic to Malagasy. The Hadada H agedashia hagedash, widespread in Africa south of the Sahara, is a broadwinged, all dark bird, and the Wattled Ibis Bostrychia carunculata in the Afrotropical Region, also a dark species, has a wattle hanging from the throat. In the New World are 2 species of Eudocimus, the American White Ibis E. albus, a mostly white species with bare red face, which occurs between the south-eastern United States and northern South America, and the Scarlet Ibis E. ruber with a brilliant red plumage, found along the north-eastern coast of South America and in Trinidad. Immatures of both species are dark brown above. Six species belonging to monotypic genera are essentially South American. The Plumbeous Ibis Harpiprion caerulescens, occurring in the southern continent east of the Andes, is a slaty grey bird with a bushy crest, while the Buff-necked Ibis Theristicus caudatus, found throughout tropical South America, is a grey and white species with buffy head and neck and large white wing patches. Four mostly blackish species are the Green Ibis Mesembrinibis cayennensis and the Bare-faced Ibis Phimosus infuscatus, both ranging throughout most of tropical South America, the Sharp-tailed Ibis Cercibis oxycerca, occurring from eastern Colombia to northern Brazil, and the Puna Ibis Plegadis ridgwayi, a high altitude species of the central and southern Andes. All 4 have feathered heads

with varying amounts of bare skin on the face or chin, which is red on the Sharp-tailed and Bare-faced and dark in the other two. The one cosmopolitan species is the Glossy Ibis Plegadis falcinellus, occurring in warmer regions of Eurasia, Africa, Australia and the New World, although the population that breeds from South America to the western United States is separated by some taxonomists as P. chihi, the White-faced Ibis. The Glossy Ibis is a dark, chestnut-coloured bird, glossy green on the wings, and with the head mostly feathered. Habitat. Most ibises feed in a broad range of shallow, wetland habitats, primarily freshwater or estuarine, including swamps, marshes, rain-flooded agricultural lands, rice fields and river and lake edges. Exceptions include the 2 Geronticus species, the Buff-necked Ibis and the Black Ibis, which feed in dry pastures, savannas or other open, upland habitats. Most ibises place their nests in patches of low woody or herbaceous vegetation in either permanently or seasonally flooded sites, although Geronticus nests on ledges of cliffs or in piles of boulders, and the Crested Ibis and Black Ibis nest in large trees near water. Population. Although several species of ibis are known to have experienced slow and persistent declines in numbers and some loss of range, in part due to habitat loss, shooting and pesticide problems, most species remain fairly common in large portions of their ranges. Two species, however, have become seriously threatened with extinction. The last 5 remaining Crested Ibis in Japan were live-trapped in 1981 in an attempt to increase numbers through a captive breeding programme; the species has become extremely rare in other parts of its range. Waldrapps had disappeared from their central European range by the 17th century, and declined in north Africa and the Near East until less than 300 nesting pairs remained by the late 1970s. On the other hand, the Glossy Ibis in North America has experienced a tenfold increase in numbers and has greatly extended its breeding range along the Atlantic Coast since the 1940s. Movements. In more tropical regions, ibises are generally nonmigratory. Instead, they may be resident or perform somewhat irregular movements apparently regulated by the influence which rainfall patterns and water levels have upon food resources and nesting sites. Ibises that nest in temperate regions, including populations of Glossy Ibis, American White Ibis and Crested Ibis, are migratory, and move into warmer regions during winter. Post-breeding dispersals, including northward movements in some North Temperate populations, are also characteristic of ibises, especially among younger age-classes. Food. In aquatic habitats, ibises feed primarily on crustaceans, molluscs, aquatic insects, and insect larvae, small fish and frogs. Prey taken at upland sites includes numerous grasshoppers, locusts, beetles, ants and other insects, spiders, molluscs, reptiles, and occasionally carrion, bird and reptile eggs or small rodents. Most food is captured by probing the long bill along the bottom in shallow flooded areas or in terrestrial sites. Feeding sites may be some distance from nesting or roosting locations, entailing flights of 10-25 km each way. Voice. Ibises utter a variety of harsh, guttural or grunting calls, usually when in flight or during social interactions in colonies. Most species are otherwise quiet, although an exception is the Hadada, which is extremely loud and vociferous. Behaviour. Ibises tend to be highly gregarious, although the degree of social behaviour varies between species. Roosting and feeding occur in small to large flocks, although some tropical species such as the Sharptailed and Green Ibis in South America and Black Ibis in India are usually seen as pairs or in small groups of less than 10 birds. Breeding. Most species nest in colonies, either single-species or mixed with other species of long-legged water birds. Nesting colonies vary considerably in size, depending upon local habitat conditions and the species of ibis, with colonies of a few nests to several hundred the most common. The extremes are represented by the Crested Ibis which once nested as single pairs in the eastern USSR, to the American White Ibis which forms colonies containing tens of thousands of pairs covering many hectares of swampland forest. In the few species whose breeding behaviour has been studied, pair bonds are monogamous and of seasonal duration. Pairing occurs at the nesting site, and may include a display with head and neck stretched low and forward by one or both adults, and intertwining of the head and neck by the pair. During incubation, nest exchanges may include mutual billing and allopreening. Pairs defend immediate nest sites only. Both sexes participate in incubation and care of the young. Nesting occurs on an annual cycle in temperate zones, but on less

299

300 Ibisbill

ICHTHYORNITHIFORMES: order erected to include such fossil forms as Ichthyornis and Apatornis (see FOSSIL BIRDS). ICTERIDAE: a family of the Passeriformes, suborder Oscines;

ORIOLE

(2).

IIWI: Vestiaria coccinea (see HAWAIIAN

HONEYCREEPER).

ILEUM: the posterior part of the small intestine (see

ALIMENTARY

SYSTEM).

ILIUM: a paired bone of the pelvic girdle, partly fused with the other elements (see SKELETON, POST-CRANIAL). ILLADOPSIS: substantive name of African Trichastoma, in West Africa known as Adalats.

Sacred Ibis Threskiornis aethiopicus. (R. G.).

well-defined cycles in tropical regions where local water conditions may greatly influence its timing. Pairs generally are single-brooded during each breeding cycle. Clutch size generally ranges from 2-5 eggs, incubation starting with the first egg in the Glossy Ibis and Waldrapp, and with the last egg laid by the American White Ibis and Sacred Ibis. Incubation lasts from 21-29 days. Nestlings are nidicolous and semi-altricial, and are fed by regurgitation either directly between adult and nestling or into the nest bottom. Nestlings are brooded for the first 5-7 days after hatching, begin to move away from the nest by 14-21 days, but will return to it to be fed, and are capable of full flight between 30 and 50 days of age. Nesting success in individual colonies ranges from complete failure when rapid deterioration of feeding conditions occurs, to as high as 80% of nests producing 1 or more young in years of good feeding conditions. Young ibises of most species apparently reach maturity by at least 3 years of age. J.C.O. Carrick, R. 1959. The food and feeding habits of the Straw-necked Ibis Threskiornis spinicollis (Jameson) and the White Ibis T. molucca (Cuvier), in Australia. CSIRO Wildl. Res. 4: 69-92. Dement'ev, G.P. & Gladkov, N.A. 1951. Birds of the Soviet Union. Vol. 2. Israel Prog. for Scientific Translations, Jerusalem, 1968. Kushlan, J.A. 1977. Populations energetics of the American White Ibis. Auk 94: 114-122. Palmer, R.S. (ed.) 1962. Handbook of North American Birds. Vol. 1. New Haven.

IBISBILL: Ibidorhyncha struthersii, sole member of the family Ibidorhynchidae (Charadriiformes, suborder Charadrii). Formerly grouped with avocets and stilts in the Recurvirostridae, this aberrant wader of the high plateaux of central Asia, from Turkestan to Kashmir and northern Burma, is rather over 17 em in length, greyish brown above, bluish grey to white below, with a black face and broad black gorget. The decurved bill, 7-8 em long, is bright red, the legs are blood red, the eyes dark red. Small parties of birds remain by the slower-flowing reaches of mountain streams all the year, but a few descend into the foothills in winter. They feed, both on the banks and by wading deep into the water or swimming, on a variety of invertebrate animals. In the light elegant flight the neck is stretched out and white patches show on the wings, and a repeated whistling call is uttered. The Ibisbill breeds from the end of March to early June according to the season. A shallow scrape is made among stones and shingle and the clutch of 4 eggs, brown-spotted on a grey ground, is incubated by both parents for an as yet unknown period. H.B. Grzimek, B. 1972. Grzimek's Animal Life Encyclopaedia: Birds II, vol. 8. New York. Etchecopar, R.D. & Hue, F. 1978. Les Oiseaux de Chine. Non-passereaux. Tahiti.

IBIS, WOOD-: see

STORK; WOOD-IBIS.

ICE-BIRD: sailors' name for some prions Pachyptila spp. (see PETREL). Note, however, that the German name 'Eisvogel' applies to the Kingfisher Alcedo atthis.

BABBLERS

of the genus

ILLUSTRATION, BIRD: the pictorial representation of birds. Birds were among the first subjects to be drawn by Neolithic man on the walls of his cave. It is thought that these pictures of birds and other animals may have had some mystical significance, being sympathetic or restitutive magic, shamanism, totemism or a representation of the duality of male and female. It is even possible that they may have been just home decoration or Art for its own sake. Representations of birds were found in several ancient cultures, but most notable must be those from Ancient Egypt. These usually depicted recognizable species. On the fresco of the tomb of Ne-Few-Maat at Medum are very life-like illustrations of Bean Goose Anser fabalis, Red-breasted Goose A. ruficollis and White-fronted Goose A. albifrons. Each bird has a specific JIZZ, suggesting that the artist, working at least as long ago as 3,000 BC, was familiar with his subjects. It was not until the Middle Ages that the first didactic bird illustrations appeared in medieval bestiaries. The monastic manuscripts also contained accurate representations of species that are recognizable today. There are excellent marginal decorations of birds in De Arte Venandi cum Avibus (c. 1248) by the German Emperor Frederick II (see also FALCONRY). Probably the best representations of this period are to be found in the Sherborne Missal (c. 1400). Of the 170 decorations, two-thirds are identifiable and cover 40 species. The invention of printing brought bird illustrations to a wider readership. Notable among the earliest printed books to contain bird pictures were Das Buch der Natur (Augsburg, 1475) and De Proprietatibus Rerum of Bartholomaeus Anglicus, printed in England by Wynkyn de Worde (c. 1495). A third significant book at this period was Hortus Sanitatis, printed by Jacob Meydenbach at Mainz in 1491, which contained 103 figures of birds. The first book that can be described as an 'ornithological treatise' was by Pierre Belon of Le Mans, whose Histoire de La Nature des Oyseaux was published in Paris in 1555. The 160 woodcut illustrations were described by the author as 'simple portraits of birds, the nature of which no one else has illustrated before'. More accurate and sophisticated woodcuts by the Strasbourg artist Lukas Schan are to be found in Conrad Gesner's Historia AnimaLium (Zurich, 1565), the third volume of which was devoted to birds. Gesner, in describing Schan as equally skilled in painting and in fowling, summed up the essential truth that the best bird illustrators know as much about birds as they do about painting and drawing. It was not until 1676 that the first illustrated text book of birds appeared in England, when Willughby and Ray's Ornithologiae Libri Tres, was published. It was significant because in it the authors attempted a scientific classification of birds. The illustrations were not of a very high quality, but they were attempts at clear representations of birds. Engraving on metal, which had begun to supersede wood towards the end of the 16th century enabled the artist to achieve finer detail. This development coincided with the great 17th and 18th century voyages of

discovery, which gave rise to books with magnificent, hand-coloured plates. Excellent examples of these are Mark Catesby's Natural History of Carolina (2 volumes, London 1731-43) and Eleazer Albin's Natural History of Birds (1738). In France the work of Buffon had provoked enormous interest with the publication of the collection of plates of animals drawn and engraved under Buffon's supervision by F.N. Martinet. Work began in 1765 and by 1783 1,000 plates had been published, 973 of which contained figures

IUustration, bird

of birds. This comprehensive ornithological iconography is usually referred to as Les Planches Enluminees, Executees par Daubenton IeJeune or Buffon's Planches Enluminees. This was the period of the de luxe monograph in France. Works of great beauty, such as Oiseaux Dotes (Paris 1800-2) by J.D. Audebert, F. Levaillant's Histoire Naturelle des Perroquets (1801-5) with figures by J. Barraband, and A.G. Desmarest's Histoire Naturelle de Tangaras (1805-7) with plates by Barraband's pupil, Pauline de Courcelles, made the Empire the golden age of ornithological illustration in France. The foremost bird illustrator at this time was Thomas Bewick, who by 1800 was developing wood engraving. By cutting into the end grain he obtained from the wood the delicacy of shadowing that only intaglio copperplates had achieved before. He also attempted by means of detailed backgrounds to indicate the bird's habitat. Bewick was a major influence on both wildlife illustration and the art of engraving. The first and, arguably, the finest of the great colour-illustrated books of the 19th century was The Birds of America, a four-volume elephant folio illustrated with 435 aquatint engravings. This book was the work of John James Audubon, who as well as being the greatest 19th century bird illustrator must also have been the most romantic. He was born in Haiti, son of a Creole woman and a French sea captain who later made a considerable fortune as a merchant. Educated in France, he went to live in the United States at the age of 18 and it was only after various business ventures had failed that he thought of publishing a book. Unable to interest American publishers, he sought subscribers in Europe and The Birds of America was published in London. The carefully composed plates often contain several birds and are full of action, showing that as well as being a very skilled artist, Audubon was a skilful observer of bird behaviour. The invention of lithography brought a means of reproducing tone successfully and one of the pioneers of the process was Edward Lear, whose illustrations of the Family Psittacidae (1830-32) contains 42 large lithographic plates 'drawn from life and on stone'. These plates were beautifully and laboriously coloured by hand. Lear was one of a stable of artists used by John Gould to prepare plates for his books. Gould's first book A Century of Birds from the Himalaya Mountains was published in 1832 and when he died in 1881 he had published more than 40 illustrated books. Although he prepared preliminary sketches and completed some very fine finished drawings, most of the illustrations were the work of his wife Elizabeth, Edward Lear, Joseph Wolf, William Hart, H.C. Richter and, latterly, J.G. Keulemans and Joseph Smit. The portraits of birds in the school of Gould showed an adult or, especially in the case of sexually dimorphic species, two adults in the foreground with a scene suggesting the habitat or an interesting aspect of the species's habits. This formula for composition became accepted and was used by many artists for many years after Gould's death. The paintings for exhibition or commission by Joseph Wolf and others were on an heroic scale, the fashionable obsession with the macabre and with the Scottish Highlands producing many dramatic paintings of Golden Eagles Aquila chrysaetos feeding on dead Red Deer Cervus elaphus or harrying Ptarmigan Lagopus mutus. The invention of chromolithography meant that colour illustrations could be produced in greater quantities than before. One of the earlier bird books to take advantage of this development was Lord Lilford's Coloured Figures of Birds of the British Islands (1891-98). The chromolithographs were made from drawings by Keulemans and Archibald Thorburn with a small number by G.E. Lodge and W. Foster. These illustrations must have been seen by hundreds of thousands of birdwatchers, because they subsequently appeared in all 3 volumes of T .A. Coward's The Birds of the British Isles and Their Eggs, which was almost continuously in print for 40 years from 1920 and The Observer's Book of Birds, published in 1937. Thorburn in his own British Birds, published in 4 volumes in 1915-16, produced plates in which several species could be compared. On one plate there might be up to 11 species seen in appropriate habitat. With his illustrations for the first two volumes of E.D. Cumming's The Bodley Head Natural History (1913) J.A. Shepherd suggested that it might be possible to identify birds from illustrations that show them as living and moving animals. Noone else has tried to do this as an aid to identification, but Shepherd's work has influenced some of today's leading British illustrators, particularly John Busby. Generally, North American bird artists of the early part of this century

301

were more adventurous in approach than the Europeans. Louis Agassiz Fuertes, for example, showed great understanding of light and shade and his gallery paintings were the equal of any European contemporary, with the possible exception of Bruno Liljefors. Fuertes was then, and still is, a major influence on American bird art and his death at the age of 53 in 1927 was a tragedy. At this time other leading North American bird artists included Lynne Bogue Hunt, Bruce Horsfall, Francis Lee Jaques and two Canadians, Allan Brooks and Frank Hennessy. All were among the exhibitors at the Cooper Ornithological Club's 1926 Annual Meeting in Los Angeles. Among the newcomers was an eighteen-year-old who was to revolutionize bird watching with his system of illustrating for identification. His name was Roger Tory Peterson. Peterson in AField Guide to the Birds set a pattern which was to be followed for 40 years at least. In this revolutionary book he showed birds in profile with an arrow indicating diagnostic characters. Peterson, with Guy Mountfort and P.A.D. Hollom, did the same for European birds in A Field Guide to the Birds of Britain and Europe, published by Collins in 1954. These field guides have set a format for books on birds of various parts of the world as well as for those about other classes of animals. Although there have been imitators of Peterson, none has been able to better his technique. Two artists, however, have developed further dimensions to illustration for identification by recognizing that not all birds present their watchers with a perfect profile. They are Peter Hayman, whose illustrations for The Birdlife ofBritain (Mitchell Beazley, 1976) and What's That Bird? (RSPB, 1979) show birds in a variety of postures and Lars Jonsson, a Swedish artist, whose Fdglar i Naturen series of identification guides, first published in Sweden from 1977 to 1980, effectively capture the jizz of birds. As well as book illustrations, Thorburn produced paintings for exhibitions. These often portrayed gamebirds and birds of prey, for it was sportsmen rather than ornithologists who made up the greatest market for bird paintings at the beginning of the century. These pictures showing birds in landscapes were much less dramatic (and, despite his reputation, less accurate) than the oil paintings of his Swedish contemporary, Bruno Liljefors, whose knowledge of birds and other animals and creative ability must make him one of the greatest of all wildlife painters. Other excellent bird painters, who both illustrated books and painted pictures for the private collector at this period, included Winifred Austen, G.E. Lodge, Allen W. Seaby and Frank Southgate. Thorburn died in 1935, Liljefors 2 years later, by which time the paintings of Peter Scott had become popular, both as illustrations to his books and also reproduced as prints. This work as an artist, together with his conservation activities, helped to create a fertile ground in which the post-war interest in birds could grow. Among other books published in the 1930s were R.B. Talbot Kelly's The Way of Birds (1937) and Mary Priestley's A Book ofBirds (1937) with illustrations by C.F. TunniclifIe, who later wrote and illustrated several significant books of his own, notably Shorelands Summer Diary (1957). R.B. Talbot Kelly's distillation of birds to a few lines and flat colours and Eric Ennion's outstanding ability to catch the movement of birds and commit it to paper have influenced several of today's leading wildlife artists. C.F. Tunnicliffe had first come to notice as an etcher of country subjects and then as a wood engraver, illustrating the nature books of Henry Williamson. Another expert wood-engraver still working is the Swiss, Robert Hainard, all of whose prints, often in several colours, are based on events that he has seen. Print-making is not popular among bird illustrators today, but Robert Gillmor has made strong lino-cut prints and Robert Greenhalf uses birds in landscapes as subjects for his etchings. While European bird art has become freer, in North America there seems to be a vogue for minutely accurate, often rather romanticized portrayals of birds. There is certainly work of a high ornithological standard from Roger Tory Peterson, George Miksch Sutton, Don Eckeiberrry, Guy Coheleach and Al Gilbert, and Canada has produced two first-class bird artists in Robert Bateman and J. Fenwick Lansdowne. Australasia has produced several artists in the realistic genre; perhaps the most notable are Peter Trusler, William Cooper and Raymond Harris Ching, a New Zealander whose skilful drawing shows to great advantage when he tackles subjects with which he is familiar. The contribution of bird illustrators to the creation of an interest in birds and their conservation has always been considerable, but in the last 50 years this contribution has been particularly impressive. The wide

302 Image-fighting

popularity of the work of Peter Scott and Roger Tory Peterson, the illustrations of Don Eckelberry, the vast commercial output of C.F. Tunnicliffe, the paintings and prints by Keith Shackleton and the book illustrations, calendars and cards by Robert Gillmor have all been notable. Never has the demand for bird illustrations been so great nor have there been so many illustrators. However, not all the published bird illustrations are as accurate as they might be. The wonderfully detailed studies by David Reid Henry have yet to be matched by any living wildlife artist. While the growth of nature photography has encouraged some artists to adopt a more abstract approach, photographs have had the unfortunate effect of providing a source for other artists to copy. Sadly, some also use as models mounted specimens which they faithfully reproduce with all their unpreened feathers, shrunken soft parts and sometimes unrealistic poses. However, thanks to the Society of Wildlife Artists, whose inaugural exhibition was held in 1964, standards are improving. The SWLA and in the USA the Society of Animal Artists mount annual ornithological exhibitions and, with conservation societies holding exhibitions and a growing number of privately run galleries, there is plenty of opportunity for bird watchers to acquire original work. With an increasing number of bird books being published and the decorative opportunities presented by the use of birds on gifts and cards there has never been such wide scope for bird artists to have their work used. N.H. Anker, J. 1938. Bird Books and Bird Art. Copenhagen. Jackson, C.E. 1975. Bird Illustrators. London. Jackson, C.E. 1978. Wood Engravings. London. Kelly, R.B. Talbot. 1955. Birdlife and the Painter. London. Harris, H. 1926. Examples of recent American bird art. Condor, 28: 191-206. Niall, I. 1980. Portrait of a Country Artist. London. Norelli, Martina R. 1975. American Wildlife Painting. New York. Yapp, B. 1981. Birds in Medieval Manuscripts. London.

IMAGE-FIGHTING: term used to describe attacks by a bird against its reflection in a window, mirror or other reflecting surface, e.g. the hub-cap of a motor-car. The attacks may be brief and not repeated or become an obsession, persisting over months, and are usually but by no means always made by male birds, presumably against a territorial 'rival'. Attacks by a number of passeriform species, notably crows Corvus and wagtails Motacilla, are on record; also by game-birds such as the Capercaillie Tetrao urogallus. So far the phenomenon has not attracted more than anecdotal attention. IMITATION: see under FOOD SELECTION; MIMICRY, VOCAL.

HUMAN

COMFORT BEHAVIOUR; FACILITATION, SOCIAL; IMITATION OF BIRD SOUNDS; LEARNING;

IMMATURITY: see under

YOUNG BIRD.

IMMIGRATION: migration into an area (see MIGRATION; and

IRRUP-

TION).

IMPENNES: a superorder recognized by some authorities (see under CLASS; PENGUIN).

IMPERVIOUS: as applied to nostrils, see IMPING: a technique in

NARIS.

FALCONRY for mending broken feathers, also useful for rehabilitating flight-impaired birds. There are 3 main methods. (1) The broken feather's calamus is severed at the widest, most distal, hollow part; a whole moulted feather is cut at the same point, and a shaped wooded plug glued into the vane of each to join them. (2) The broken feather's calamus is cut as in (1) and the 'new' feather's calamus is not cut but trimmed to fit inside the original calamus, retained by glue and a thread tie. This method has been used to attach small transmitters (see RADIO-TRACKING AND BIOTELEMETRY). (3) The rachis is severed proximal to the break, a moulted feather cut to match, and a needle, pointed at each end, inserted with glue to make the join. Severely bent but unbroken feathers can be similarly mended by pushing the needle into the distal rachis at the bend, and ventrally slitting the proximal rachis to insert the needle lengthways.

IMPRINTING: a special case of exploratory or latent learning that has particular relevance for the student of ornithology (see also LEARNING). Like latent learning and insight learning, it is characterized by the absence of any reward in the usual sense of something which satisfies one of the primary physiological needs of the animal. The name 'imprinting' (T'ragung' in German) was originally given to a type of learning characteristic of the development of the following response of the young of nidifugous birds such as geese and ducks and rails. Heinroth, in 1910, found that young geese reared from the egg in isolation reacted to their human keepers, or to the first relatively large moving objects that they saw, by following them as they would their parents. In extreme cases it seems that this need happen perhaps for only a few minutes for the young bird to come to accept a human being as its proper associate and to retain for the rest of its life a tendency to regard human beings as fellowmembers of its species. Thus a bird, as a result of this first experience, may when it becomes mature-months or years later-be found to be irreversibly fixated sexually to human beings; and Lorenz (1935) assumed from his work on geese that this was characteristic of imprinting. Subsequent investigation seems to show that such fixations based solely on the experience of the first few hours or days of life are extremely rare. Although many examples have been reported, it is evident that in almost all cases there has been a long subsequent history of rearing and attending by human keepers, so that there has been continual opportunity for the bird to learn to respond to human beings as a result of other types of LEARNING. The important point emerges, however, that when the young bird first follows the parent or substitute parent the attachment is not to an individual (although this will usually come later as a result of conditioning) but to the 'species' in a very general manner. Thus, we can sum up the characteristics of the process of imprinting, in the sense originall y proposed by Lorenz, as: (1) A learning process confined to a very definite and brief period of the individual life. (2) One that, once accomplished, is often very stable and perhaps in some rare cases irreversible. (3) A process that is often completed long before the various specific reactions to which the imprinted pattern will ultimately become linked are established. (4) Learning that is generalized in the sense of leading to an ability to respond to the broad characteristics of the species. On the whole, subsequent research has tended to emphasize the importance of conclusion (1) and to suggest that (2) and (3) apply only in exceptional cases. Recent developments concerning conclusion (4) will be discussed later. As regards the first point, it has been shown that the critical age for imprinting Mallard Anas platyrhynchos ducklings, by the process of following, is between 13 and 16 hours; and that if the first experience is delayed beyond the latter age then the percentage of ducklings that can be imprinted falls rapidly to zero (Figure). It is known, however, that by holding the birds in complete isolation, or by giving doses of drugs such as meprobamate that reduce metabolism and act as muscle relaxants, the critical age for imprinting can be extended (E.H. Hess). Similar evidence for the existence of a critical period early in life has been found in chicks and goslings, as well as in the young of Tufted Duck Aylhya fuligula, Moorhen Gallinula chloropus, Coot Fulica atra, and others. The importance of internal processes of maturation in determining the start of the sensitive period is indicated by the observation that the start is more closely related to developmental age (time since conception) than to time since hatching. A wide variety of stimuli will elicit a following response in ducklings and domestic chicks, ranging from a slowly walking person to a flashing light. The optimal stimulus in terms of colour and size varies from species to species, and the efficacy of a particular stimulus is influenced by the rearing environment. P.P.G. Bateson, for example, found that exposure of chicks to a colour pattern in their home pens subsequently facilitated imprinting to that pattern. As the young bird becomes attached to one stimulus, a tendency to avoid other stimuli develops. In part, the onset of avoidance of new stimuli is a consequence of the imprinting process itself: when one object becomes familiar, others, by definition are unfamiliar and avoided. Thus the sensitive period is to some extent self-terminating and by depriving young birds the chance to become imprinted (e.g. by rearing them in diffuse light) the sensitive period can be extended. However it cannot be extended indefinitely, so it seems likely that the endogenous maturation

Incubation

individual, species-specific chararacters. P. P. G. Bateson has shown that Quail prefer to mate with partners that differ slightly in plumage pattern from those with which they have been reared. This preference for slight novelty may prevent inbreeding, while ensuring that a mate of the correct species is chosen. The flexibility of learning may be better suited to cope with this compromise than a genetically fixed rule. Other kinds of imprinting. Although most of the research on imprinting has been concerned with filial and sexual imprinting, analogous forms of learning (latent learning in a sensitive period) are known to influence other kinds of behaviour, for example, food preferences and habitat selection. The concept of a sensitive period also emerges from studies of song development in birds (see VOCALIZATION): young Chaffinches Fringilla coelebs are capable of learning songs during their first year of life, but not subsequently. In this case the termination of the sensitive period seems to be under the hormonal control-gonadectomized Chaffinches have a greatly extended learning period. W.H.T. and J.R.K.

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Bateson, P.P.G. 1979. How do sensitive periods arise and what are they for? Anim. Behav. 27: 470-486. Chalmers, N. 1983. The development of social relationships. In Halliday, T.R. & Slater, P.J.B. (eds). Animal Behaviour, vol. 3. Genes, development and learning. Pp. 114-148. Oxford. Heinroth, O. 1910. Beitrage zur Biologie, namentlich Ethologie und Physiologie der Anatiden. Verh. V. Internal. Orne Kongr., Berlin 1910: 589-702. Lorenz, K. 1935. Der Kumpan in der Umwelt des Vogels. J. Orne 83: 137-214; 289-413.

INCA: substantive name of some Coeligena spp. (for family see Fig. 1. Critical age for imprinting in Mallards Anas platyrhynchos expressed as a percentage of positive responses. (Redrawn from Hess 1957).

of 'fear' also plays a role in terminating it. More detailed investigations of the stimuli eliciting the following response have shown that in fact the most effective stimulus for an imprinted chick is one that is very slightly different from the original imprinting stimulus; for example a chick imprinted on a yellow flashing light, and then offered the choice between approaching yellow or orange lights, prefers the orange. Thus there is a trade-off between familiarity and novelty and slight novelty provides the optimal stimulus. Imprinting is not restricted to visual stimuli. In the cavity-nesting Wood Duck A ix sponsa exposure to sound signals can lead to a subsequent preference for that sound; further, this imprinted response to sound is not altered or reinforced by visual stimuli. This fits well with the natural life of the Wood Duck, since the first response of the young ducklings inside the dark nest cavity to their mother must be based on auditory rather than visual stimuli. Sexual imprinting. For Lorenz, one of the key characteristics of imprinting was that later sexual preference could be determined by a rather brief exposure in early life. Subsequent work has shown that sexual imprinting does occur, but that it requires longer exposure to the imprinting stimulus than does so-called filial imprinting of the young bird on its parent. Once established, however, imprinted sexual preference can be very strong. In one experiment Zebra and Bengalese Finches (Poephila guuata and Lonchura striata) were cross-fostered and then maintained with their own species for a number of years. Even though the cross-fostered birds bred with their own species, when eventually given a choice between their own and their foster species, they strongly preferred to court the latter. Sexual imprinting, does, however, seem to be biassed towards the animal's own species. When the two finch species referred to above are raised by a mixed pair, they always imprint on their own species. The sexual imprintability of the two sexes may differ in some cases. F. Schutz, for example, reported that in sexually dimorphic duck species only the males show sexual imprinting as a result of cross-fostering, while in the monomorphic Chilean Teal Anas flavirostris both sexes imprint. The biological significance of imprinting. Why should the chancy business of learning be used instead of a fixed genetic instruction to determine filial and sexual preference? One proposal for filial imprinting is that the young bird sees its parent from so many different angles and distances that it would be hard to programme a genetic instruction for recognizing the parent under all conceivable circumstances: learning is more flexible. A second idea refers primarily to sexual imprinting. Recent work with Japanese Quail Coturnix coturnix japonica has shown that sexual imprinting is not, after all, simply a matter of learning supra-

HUM-

MINGBIRD).

INCA-FINCH: substantive name of Andean finches of the genus

Incaspiza (for family see BUNTING).

INCA-TERN: see

TERN.

INCERTAE SEDIS: term used in taxonomy to mean 'of uncertain taxonomic position'. INCUBA.TION: the process whereby the heat necessary for embryonic development is applied to an egg after it has been laid. Such heat is usually derived from the body of one or both of the parent birds although species in several groups use foster parents (see BROOD-PARASITISM). The Megapodiidae utilize natural sources of heat such as solar radiation, volcanoes or the heat of fermentation of decaying organic matter (see MEGAPODE).

In the majority of birds heat transfer is effected by the close application to the eggs of the incubation or brood patch. Some birds have a single patch that covers all the eggs whilst others have a discrete patch for each egg. Generally this area on the ventral surface of the bird becomes denuded of feathers, and becomes oedematous and highly vascular through the action of steroid hormones in conjunction with prolactin (for reviews see Lofts and Murton 1973, Drent 1975). The release of these hormones appears to be related to the onset of breeding behaviour, e.g. the manipulation of nest material and stimulation by the mate during courtship. In some species, e.g. pigeons and doves (Columbidae), the incubation patch is an area naturally devoid of feathers and is bare the year round whilst in waterfowl there are no true incubation patches but the feathers in an area on the ventral surface are often plucked out by the parent. There are numerous observations on the way the incubation patch is brought into the right relationship with the eggs. The 'resettling' movements performed when a bird sits on the eggs include ruffiing or lowering of the abdominal feathers to expose the patch and a waggling or quivering action as or after the bird lowers itself to adjust the tightness of sit. Some birds lack incubation patches (e.g. pelicans Pelecanus spp.) and in the Sulidae (gannets and boobies) the cradling of the egg in the webs of the feet has led to the suggestion that these birds incubate with their feet. The ventral body surface, although lacking an incubation patch, probably contributes to the warming of the egg for, as Drent points out, blood flow through the feet is usually highly variable since the legs and feet are used as heat dissipators for thermoregulation (see HEAT REGULATION). Kendeigh (1952) surveyed a large body of data collected from all groups on such points as the division of labour between the parents and the patterns of attentiveness and inattentiveness i.e. intervals spent on and off the nest. Almost all the possible arrangements are exemplified from equal sharing of incubation between the sexes (most birds) to either

304 Incubation

-;

Magellanic Plover Pluuianellus socialis incubating. (P hoto: J .R. Jehl Jr. ). female (e.g. Galliformes, Strigiformes) or male (e.g. phalaropes, Tinami formes) taking sole charge . Incubating males generally develop incubation patches (e.g. phalaropes and passerines-Skutch 1957) although several exceptions are listed by Lofts and Murton and by Drent . There are numerou s examples of adaptive specialization, for instance, species in which only one member of a pair incubates are in many cases sexually dimorphic; the incubating bird is coloured cryptically and its mate conspicuously. In bisexual incubation the eggs are generally attended at all times by one or the other parent except , for example , when the weather is mild. In single sex intermittent incubation the time is divided between attending the eggs and inattentive periods usually spent foraging; the nests of these species are usually of complex structure providing good heat retention during the inattentive period s. Periods spent sitting on the eggs vary enormously between species (Lack 1968), from less than one hour in many passerines e.g. European Robin Eruhacus rubecula, to a few hours in most seabirds which feed inshore , e.g. gulls and terns , between 2 and 12 days in offshore feeding seabirds, e.g. shearwaters, storm-petrels (Procellariidae), spells of 2 ~ to 3 weeks in the albatro sses Diomedea nigripes and D. immurabilis and the 64 days of the male Emperor Penguin Aptenodytes [orsteri . Incubating bird s do not adjust their heat production to regulate egg temperatures, but instead adjust the amount of time they spend in contact with the eggs. Consequently adjustments in the time (number and/ or duration of sitting spells) spent attending the eggs are related to the ambient air temperature, degree of nest insulation, and the time requir ed for foraging (White and Kinney 1974). The time spent off the nest foraging is reduced in some cases by the non-incubating member feeding its sitting mate. When the parent leaves the nest to forage, the eggs lose heat at a rate dependent on their size, arrangement in the nest , degree of nest insulation , ambient temperature, and possibly egg colour. Resistance of the embryo to chilling has been demonstrated clearly in the Procellariiformes and seems to be a feature of bird embryos in general. In the latter half of incubation, when embryonic metabolism is increasing, the heat so produced , whilst not able to maintain the egg temp eratur e, may at least slow its rate of decrease when the parent leaves the nest. Drent points out that in the energy budget for incubation not only is the rate of cooling of the eggs important , but the time required to reheat the eggs when the parent returns may also influence the pattern of foraging. In birds with open nests on the ground the eggs may be exposed to the danger of overheating due to solar radiation when the parents leave the nest. Many of these species, however, have cryptic egg coloration as a protect ion against predators, and the pigments responsible for the markings tend to reflect the potentially harmful near-infrared rays and thus minimize solar heating . The bright blue eggs of some tree-nesting species also show high reflectance in the near-infrared . In some instances the ambient /egg temperature may be so high that cooling of the eggs by shading , wetting of the abdominal feathers (see BELLY-SOAKING) or

Double-banded Courser Cursorius africanus incubating. (P hoto: G .L. Mac-

lean).

through the brood-patch, with or without accompanying panting or gular flutter , may be necessary. Such species tend additionally to locate their nests to take advantage of prevailing shade and cooling winds and to orient their sitting posture to minimize insulation and maximize cooling by breezes. The definitive incubation temperature (generally between 34 and 39°C depending on the species) is achieved only after a warm-up period , the length of which may be related to the tightness of sit and the time required for the incubation patch to become fully functional. Maintaining an adequate incubation temperature is, however, only one ingredient in the recipe for successful incubation, for it is clear from a consideration of the artificial incubation of eggs that other criteria must be satisfied through the behaviour of the incubating bird , the particul ar nest environment or adaptation of the egg. Thus, most eggs irrespect ive of size lose about 15% of their fresh weight during incubation (due to the loss of water from the content s across the porou s shell) which suggests either a regulation of the nest humidity or an adaptation of shell porosity to the humidity conditions characteri stic of the species. Control of water loss from the egg may be obligatory if the water content of the hatchling is to be similar to that of the fresh egg and successful hatching maximal. Thus, for example, the eggs of coots Fulica , divers (Gaviidae) and grebes have a shell of high porosity as an adaptation to the humidity pertaining in the nest. Species nesting at altitude have a reduced eggshell porosity compared to their sea-level counterparts to compensate for the changes that would result in embryonic respiratory gas exchange and water loss from the egg as a consequence of the lower baromet ric pressure (for these and other examples see Rahn and Paganelli 1981). Nest ventilation (achieved presumably during the frequent rising and shufiling by the incubating parent ) is important to maintain an optimum gaseous environment and egg turning, 'poking' or 'shifting' behaviour is important for a number of reasons. For example, it helps counteract the temperature gradients which occur in the nest and during early incubation it prevents premature adhesions between the extra-embryon ic membranes and the shell membranes . These may result in distortions in subsequent development, with the embryo perhaps dying during incubation or finding itself in a position from which it is unable to escape when hatching . During the latter part of incubation the egg develops an asymmetrical distribution of weight so that in spite of egg-turning by the parent the egg probably resettles in a particular attitude. This may facilitate attainment of a correct pre-hatching position by the embryo (Drent; see HATCHING) . The incubation period is strictly defined as the time which, with regular uninterrupted incubation, elapses from the laying of the last egg in a clutch to the hatching of that egg. Accurate determination of the period of incubation demand s marking of the eggs and vigilant observation and many docum ented periods have not been assessed according to the definition above. Incubation periods vary from 11 days in some of the smaller passerines (egg weight below 1g) to about 80 days in the Royal

Insessores

305

INDIGENOUS: term applied to species, etc., meaning native to the area under reference. INDIGO-BIRD: substantive name, alternatively 'indigo-finch' or 'combassou' , used in East Africa for Hypochera spp . (for family see WHYDAH ( 1» .

INDIGO BUNTING: Passerina cyanea of North America (see

CAR-

DINAL GROSBEAK) .

INDIRECT HEAD SCRATCHING: see COMFORT

BEHAVIOUR.

INDIVIDUAL DISTANCE: the minimum distance at which an individual will tolerate the presence of another (usually, conspecific) individual. The term was introduced into ornithology by Conder (1949), who defined it widely so as to include the distance maintained between individuals in various other circumstances; but it is now most often applied to resting, or otherwise inactive, birds . Individual distance tends to be a specific characteristic; it is perhaps most obvious in gregarious birds roosting or perching together, for example on a telegraph line. Conder, P.J. 1949. Individual distance. Ibis 91: 649-655. Water Rail Rallus aquaticus moving egg during incubation. (Photo: K.] . Carlson).

Albatross Diomedea epomophora (egg weight about 450 g). There exists a general relationship between egg weight and incubation period : each doubling of species egg weight increases incubation time by 16% on average. However, various factors have been suggested that modulate the relationship . Some of these are the egg temperature during incubation, stage of the development of the chick at hatching, relative risk of predation, type of nest, climate , season and food supply, with the result that there is a wide range of incubation period about any given egg weight. Nice (1954), reviewing these factors, concluded that the crucial one was the rate of development of the embryo . This rate of development is a product of natural selection and ultimate causes may be located in the bird's ecological relationships e.g. the availability of food and growth rate of the young. Thus Lack, commenting on the correlation between the fledging period and incubation period, suggested that the easiest or perhaps the only way to evolve a particular growth rate of the young was to alter the whole rate of development including that of the embryo in the egg (see DEVELOPMENT, EMBRYONIC; GROWTH ). See photos BELLY SOAKING; COLONIALITY ; COLORATION, ADAPTIVE; ENERGETICS . S.G.T. Drent, R.H. 1975. Incubation. In Farner, D.S. & King, j.R. (eds.). Avian Biology V. London. Kendeigh, S.c. 1952. Parental careand itsevolution in birds. Illinois BioI. Monog. 22(1-3): 1-356.

Lack, D. 1968. Ecological Adaptations for Breeding in Birds. London. Lofts, B. & Murton, R.K. 1973. Reproduction in birds. III Farner, D.S. & King, j .R, (eds.). Avian Biology III. London. Nice, M.M. 1954. Problems of incubation in North American birds. Condor 56: 173-197.

Rahn, H. & Paganelli, C.V. 1981. GasExchange in Avian Eggs. Buffalo. Skurch, A.F. 1957. The incubation patternsof birds. Ibis 99: 69-93 . White, F.N. & Kinney, J.L. 1974. Avian incubation. Science 186: 107-115. INCUBATOR BIRD: see MEGAPODE.

INDEX: term sometimes applied to the second digit of the manus, but by a few authors to the first (see WING ) .

INDICATORIDAE: see

INFESTATION: see

ECTOPARASITE; ENDOPARASITE.

INFORMATION CENTRE: a phrase coined by P. Ward and A. Zahavi (following J. Fisher) to refer to the idea that birds nesting in colonies or gathering in communal roosts may learn from each other about the location of good feeding sites. The idea is that unsuccessful foragers could follow more successful individuals on their next trip . It has generated a considerable amount of data and theoretical controversy. Most of the evidence pertaining to the idea is inconclusive. INFRA-ORDER: a systematic category between suborder and superfamily (if used) or family. The use of this category is not obligatory and the grouping of presumed families into a suborder in fact is rather subjective . INFRA-SOUND: sounds of too low frequency to be detected by the human ear: below 20-30 Hz (waves per second). Recent experiments have shown that pigeons can detect sounds down to 0.05 Hz (1 wave in 20 s). If this proves to be common in birds, it may be related to the presence in their coclilea of a third otolith, the lagena, which has been lost in mammals . It has been suggested that natural infra-sound, which carries for very long distances, may give pigeons cues that help them in homing (see HOMING PIGEON; ULTRASOUND) . INGLUVIES: the crop (see

ALIMENTARY SYSTEM).

INHAMBU: name used in Latin America for Crypturellus spp. (see TINAMOU) .

INHERITANCE: see GENETICS. INJURED BIRDS: see CARE

INDETERMINATE LAYER: species in which the number of eggs laid in a clutch can be altered by the addition or removal of eggs during laying (see LAYING).

INDIAN REGION: alternative name for

INFECTION: see DISEASE.

ORIENTAL REGION .

PICIFORMES; HONEYGUIDE.

INDICATOR SPECIES: species whose ecological requirements are such that their presence more or less guarantees the existence of particular environmental conditions . It may then be easier to observe the presence or the absence of the indicator species than to measure the environmental conditions themselves .

INJURY FEIGNING: see

OF SICK, INJ URED AND ORPHANED BIRDS.

DISTRACTION BEHAVIOUR.

INNATE BEHAVIOUR: see

BEHAVIOUR , HISTORY OF.

INNER TOE: see LEG. INSECTICIDES: see TOXIC

CHEMICALS .

INSECTIVOROUS: insect-eating ; usually assumed to include other terrestrial arthropods. INSESSORES: former ordinal name , applied to an assemblage of so-called 'perching birds ' comprising the Passeriformes of today and various other groups .

306 Inshore habitat

INSHORE HABITAT: see under

INTESTINE: the posterior part of the gut or digestive tract, comprising the small intestine (duodenum and ileum) and the large intestine (rectum)-see ALIMENTARY SYSTEM.

OCEANIC BIRDS.

INSIGHT: see LEARNING. INSTINCT: an innate capacity for forms of behaviour that do not have to be learnt by the individual-a word falling into disuse as a scientific term because it represents an over-simplified concept and has acquired a variety of meanings. INSTRUMENTAL SOUNDS: see MECHANICAL

SOUNDS.

INTEGUMENTARY STRUCTURES: outgrowths from the skin (see SKIN). Of these the chief are feathers (see FEATHER; PLUMAGE), the rhamphotheca covering the bill, sometimes with horny excrescences or extensions such as casques and frontal shields (see BILL), the podothecae covering the feet (see LEG), and the oil gland (see OIL GLAND); these are dealt with elsewhere, as indicated. So also are the claws growing on the toes and sometimes on the digits of the manus, and the spurs that are present on the tarsus or on the carpal joint in some species (see LEG; WING). There remain to be considered various accessory structures found in certain species, especially about the head and neck; these are of several kinds. See photo BELLY-SOAKING. Combs, Wattles, and Lappets. These are unfeathered flaps or appendages, usually of a fleshy texture and brightly coloured. Their function must lie in display and recognition; they often show sexual dimorphism; and their state may be subject to hormonal control. They are included in the general term 'caruncle'. A familiar example of a comb-an erect process situated longitudinally on the crown-is that of the domestic fowl, largest in the cock; the name derives from the serrated margin. Wattles are often pendulous from the angles of the mouth ('rictal lappets'), and there may be more than one on each side. Or they may be harder, more warty excrescences, variously situated-rictally, frontally, near the eye, or anywhere on the patches of bare skin found in some species, chiefly on the face and neck. Some of these, as with others adorning the bill, are moulted seasonally (see MOULT). Wattles are found in many species, particularly among the pheasants, turkeys, plovers, jacanas, cotingas, honeyeaters, starlings, and wattle-birds. The Turkey Meleagris gallopauo has a varied assortment, comprising a distensible frontal caruncle, tubercles on head and neck, and a throat wattle. Pouches and Sacs. These are of different kinds. The gular pouches of pelicans and, less markedly, of cormorants playa part in the capture and swallowing of prey. Others are ornamental, such as the long red pouch depending from the almost naked neck of the Marabou Leptoptilos crumeniferus; or the inflatable sac, covered with bright red skin, on the front of the throat in male frigatebirds Fregata spp. Others again are concealed by feathers and are used in the production of booming calls, such as that uttered in spring by the male Prairie Chicken Tympanuchus cupido with the aid of two inflatable sacs on the sides of the neck. INTELLIGENCE: a term without precise connotation for the study of bird behaviour, its place being taken by 'insight learning' (see LEARNING; also NERVOUS SYSTEM). INTENTION MOVEMENTS: the incomplete initial phases of a behaviour pattern. For example when a bird is about to take off it crouches, withdraws its head and raises its tail, and then reverses these movements as it takes off. Such incomplete movements may be repeated several times as the bird prepares to take off, in particular if the bird is in a conflict about whether to fly or not. The primary interest of intention movements to students of bird behaviour is that they are thought to be the raw material from which some courtship and threat displays have evolved by RITUALIZATION. INTERBREEDING: see GENETICS;

HYBRID; HYBRIDIZATION, ZONE OF SECONDARY; ISOLATING MECHANISM; REPRODUCTIVE ISOLATION; SPECIATION.

INTERMEWED: term used in

FALCONRY.

INTERNATIONAL CODE; INTERNATIONAL COMMISSION: see NOMENCLATURE. INTERSPECIFIC: between two or more species.

INTRASPECIFIC: within a single species. INTRODUCTION, ARTIFICIAL: see

NATURALIZED BIRDS.

INTROGRESSION: gene flow between genetically divergent populations, often used technically for gene flow occurring only between species, but that usage begs the question of the exact taxonomic status of the two populations before one can employ the term, and such taxonomic determination is not always easy. In cases of avian hybridization in nature there is frequently little difference between introgression affecting species and that affecting subspecies, although theoretically greater introgession is to be expected between genetically more similar conspecific subspecies than between genetically more divergent species. One complication is that evaluation of hybridization and introgression is usually based upon a few morphological or other traits representing but a small fraction of genetic determinants which may be linked, and hence possibly biased (the fewer the characters studied the more difficult it is to appreciate actual gene flow). Other complications include intrinsic factors such as various reproductive isolating mechanisms, population structure, heterosis, selection for or against certain alien genes and gene combinations, and extrinsic factors such as topography or gene flow in one direction or another (see GENETICS; HYBRID; HYBRIDIZATION, ZONE OF SECONDARY). Biochemical and other sophisticated techniques applied to cases involving hybridization usually disclose greater introgession than is super.. ficially apparent from analysis of plumage and other morphological traits. Not only are different traits apt to show different degrees of introgression in a given case, but introgression may affect one population more than another. In the Northern Flicker Colaptesauratus of North America there is extensive hybridization between the eastern ('yellow-shafted') and western ('red-shafted') subspecies groups: traits such as shaft colour and colour of the facial moustache of males show extensive introgression into the eastern populations, whereas restriction of the nape patch shows little introgression beyond the hybrid zone. Also, the western populations show much more introgression than do the eastern populations. Other notable cases of introgression involve the Yellow-rumped Warbler Dendroica coronata, and the Blue-winged Warbler Vermivora pinus and Golden-winged Warbler V. chrysoptera in North America, the House Sparrow Passer domesticus and Spanish Sparrow P. hispaniolensis of Europe, and the Pale-headed Rosella Platycercus adscitus and Eastern Rosella P. eximius of Australia. Introgression is suspected as a cause of observed variation when hybridization is known to occur between two populations, and the variation encountered shows gradients for traits within each population that involve characteristics of the other population and run toward the area of contact and hybridization between the two populations. Often the gradients in each population, with their gradual increase in characteristics of the other population toward the region of their interbreeding, run counter to all other patterns of clinal variation within each of them.

L.L.S.

INVASION: a term best reserved for an expansion of range into a new area; but sometimes used as synonymous with IRRUPTION. lORA: substantive name of Aegithina spp. (see LEAFBIRD). IRENIDAE: a family of the Passeriformes, suborder Oscines;

LEAF-

BIRD.

IRIS: a thin, opaque annulus of tissue in front of the lens of the eye, which by its state of contraction determines the size of the aperture

(pupil) in its centre (plural 'irides'; see VISION). As in reptiles, but in

contrast to mammals, the musculature of the bird iris is striated.

IRIS COLORATION: often a noticeable character of the living bird at close range or of the newly dead specimen, but lost in the museum skin and not always accurately represented by the artificial eyes of mounted exhibits. The character may show SEXUAL DIMORPHISM, and changes with age and sometimes with season. Even more rapid colour changes are reported to occur in the eyes of some species, perhaps corresponding to

Irruption 307

different emotional states. Although eye colour sometimes matches the coloration of the head, possibly in order to camouflage the eye, brilliant lipochrome pigments in the irides of many birds often make the eye more conspicuous. The function of iris coloration is unclear; as in other vertebrates, the iris of birds is opaque, and its colour can apparently have no effect on vision. In different birds, eye colour may be used for sex or age recognition, in display behaviour, or simply as an integral part of the head plumage coloration. The pigment of the iris epithelium in birds is brown, but there are nearly always stromal pigment cells (i.e. chromatophores in the stromal connective tissue of the iris) containing various amounts of melanin and/ or coloured oils. The iris coloration is the result of both pigmentary factors and differential absorption or reflection by the different layers of the iris (see COLOUR); the red or reddish eyes observed in many species may be due (as in the Rock Dove Columba Livia) more to richness of the superficial blood vessels than to pigmentation of the iris itself. On close examination, iris coloration may often be seen to be variegated and, interestingly, the iris of most birds has a black edge which may seem to make the pupil appear larger. Among birds a brown iris coloration, resembling that found in mammals, is very common especially among song birds. In general, the irides of birds of prey are often yellow while many herons, parrots and pheasants have reddish eyes due to oil droplets of different refractions. Dark (brown or black) eyes are even reported to be especially common in birds that fly fast or feed on the wing (Worthy 1978). Despite these generalizations, however, a wide variety of colours occurs in many kinds of birds. Some examples of birds showing various colours other than brown may be mentioned. Yellow irides are found, for instance, in most owls (Strigiformes), some 'waders' (Charadrii), some pigeons, and some herons, but also in many other groups. The Jackdaw Corvus monedula is a familiar example of a species in which the iris is almost white (pearl-grey in the adult). In adult Budgerigars Melopsutacus undulatus the iris is white peripherally, and chocolate-brown with white concentric lines in the pupillary part. In the Honey Buzzard Pernis apivorus a layer of guaninecontaining cells in the yellow iris makes the latter appear brilliant white in reflected light. An example of a bird in which the irides are green-a relatively infrequent colour-is the Cormorant Phalacrocorax carbo. Blue irides are found in, for example, the Oilbird Steatornis canpensis, the Blue-eyed Shag Phalacrocorax atriceps, the Ariel Toucan Ramphastos vitellinus ariel, and the Monkey-eating Eagle Pithecophaga jefferyi. Many groups include red-eyed birds, e.g. rails, pigeons, grebes, herons, coucals (Centropinae), barbets, puftbirds, vireos, and mockingthrushes; the White-winged Cough Corcorax melanoramphos (Grallinidae) has a bright red eye. Sexual dimorphism in iris coloration is not infrequent. In Brewer's Blackbird Euphagus cyanocephalus (Icteridae), the iris is white in the male and dark in the female; whereas in two species of finfoots (Heliornithidae), it is dark brown in the male and bright yellow in the female. In the Wood Duck Aix sponsa the iris is orange-red in the male and dark brown in the female. A striking case is that of the Saddlebill Ephippiorhynchus senegalensis (Ciconiidae); the brown eye of the male tones with the dark plumage of the head, while the chrome yellow iris of the female is a conspicuous character. Iris coloration often varies with age. The iris usually begins as blue, grey, grey-brown, brown or yellow, but in many species gradually changes after fledging to reddish-brown, brown, red, orange, yellow, white or green. These age-related changes in iris coloration in birds usually take place over a relatively short period. In the Gannet Sula bassana, for example, the iris is dark brown in the nestling, grey-blue in the juvenile, and nearly white-with a fine black outer ring-in the adult. In certain hawks, however, iris coloration may continue to change for several years. There may sometimes be seasonal change; for instance in the Rockhopper Penguin Eudyptes crestatus the colour of the iris, with that of the bill, varies from red to yellow with the seasons (see also HERON). As in fish, more rapid changes in iris coloration may sometimes accompany changes in emotional state. For example, the yellow irides of the Eagle Owl Bubo bubo are reported to turn red when the bird becomes agitated. To be distinguished from iris coloration is the colour of the orbital ring of bare (sometimes hardened) skin around the eye in some species, e.g. among the cormorants, or in any circular pattern in the plumage in that

posinon. The white-eyes (Zosteropidae) take their name from a white J.T. E. ring around the eye. Duke-Elder, W.S. 1958. System of Ophthalmology. Vol. I. The Eye in Evolution. London. Walls, G.L. 1942. The Vertebrate Eye. Bull. 19. Cranbrook Inst. Sci., Michigan. (pp. 543-551). Worthy, M. 1978. Eye color, size and quick-versus-deliberate behavior of birds. Percep. Motor Skills, 47: 60-62.

IRRUPTION: a form of MIGRATION in which the proportion of birds leaving the breeding range, and the distance travelled, varies greatly from year to year. Noted mainly in northern regions, irruptions occur in responses to annual, as well as to seasonal, fluctuations in food. Most migrations are regular, taking place at the same season each year, with individuals moving between fixed breeding and wintering areas. In irruptions, individuals may breed or winter in widely separated areas in different years. Regular migrations are associated with regular and predictable food supplies, whereas irruptions are associated with sporadic food supplies, which are much more plentiful in certain years than in others, or are plentiful in one region in one year and in a different region the next (Newton 1972). Strictly the term 'irruption' (or invasion) is applicable only to the region receiving the birds, whereas 'eruption' is often applied to the region losing them, but for general discussion it is convenient to use a single term. Typically, irruptive species have diets based on one or two food types, which fluctuate from year to year. They include certain finches and other fruit-eating birds of boreal regions, certain rap tors and owls that depend on cyclic prey, and a few steppe species, which occasionally experience extreme food shortages through drought (Table 1). All these species appear in strength in particular areas only in certain years. Seed-eaters. The seed crops of trees vary enormously from year to year, and in some years fail completely. The cropping depends partly on the natural rhythm of the trees themselves, and partly on the weather. Most trees require more than one year to accumulate the reserves necessary to produce fruit, and crop at longer intervals towards the north, where the growing seasons are shorter. Spruce, for example, tends to crop well every 2-3 years in central Europe, every 3-4 years in southern Sweden, and less frequently further north. For a good crop, the weather must also be fine and warm in the preceding autumn when the fruit buds form, and again in the spring when the flowers set; otherwise the crop is delayed for another year. In anyone area, most of the trees of a species fruit in phase with one another because they come under the same weather, and often those of a different species also crop in phase. The result is an enormous profusion of fruits in certain years, and practically none in others. The trees in widely separated areas may be on different cropping regimes, partly because of regional variations in weather, so good crops in some areas may coincide with poor crops in others. Usually each productive area extends over thousands or millions of km", and is separated from the next by terrain which, in that year, is almost devoid of seeds. In some years, moreover, the productive patches are plentiful and widespread, and in others few and far between, so that the total production of seeds over a continent varies greatly from year to year. The birds that depend on such seeds generally concentrate wherever their food is plentiful at the time. The majority of individuals migrate regularly in spring and autumn, but may breed and winter in different areas in successive years. Their local populations therefore fluctuate greatly from year to year in parallel with local seed crops. In winter quarters, too, populations range between total absence in years when appropriate tree seeds are lacking, to thousands of birds per km 2 in years when such seeds are plentiful. The bird species involved seem to move each autumn only until they find areas rich in food, then settle there. In consequence, the distance travelled by the bulk of the migrants varies from year to year, according to where the crops are good, and only when the migrants are exceptionally numerous, or their food is generally scarce, do they reach the furthest parts of their wintering range, as an irruption. Often several species irrupt in the same years, coinciding with the simultaneous failure of their respective food-plants (Bock and Lepthien 1976). The food shortage which leads to a long and heavy migration is accentuated if the birds are especially numerous at the time. This situation is frequent, because good seed crops are usually followed by

308 Irruption

poor ones. The good crops in the first year lead to high survival among the birds over winter and to a large breeding population the next summer, and these same birds and their young then encounter the widespread poor crops in the next autumn, so have to move further than usual then. How far irruptive species move northward in spring also depends partly on how much food they meet on the way. The Mealy Redpoll Carduelisf. fiammea provides the most striking example, for this subspecies curtails its usual migration by up to several hundred km to breed in southern Fennoscandia in years when the spruce crop there is good. Compared with other migrants in autumn, irruptive finches tend to show more spread in their departure directions, and birds from a particular breeding area may spread over a large part of Europe on migration. Bullfinches Pyrrhula pyrrhula ringed in Fennoscandia have been recovered the following winter anywhere between south-west, through south, to east of their breeding place in the previous summer, and similar but less marked trends have been noted in other species. Individuals breeding or wintering in widely separated areas in different years have been confirmed by ringing. For example, one Siskin Carduelis spinus was found in successive breeding seasons at places 120 km apart, and 2 Mealy Redpolls were found at places 280 and 550 km apart. Wintering recoveries are even more striking, and Bramblings Fringilla montifringilla and Siskins have been caught in Belgium in one winter and as far east as Turkey and the Balkans in a later one. Another Siskin was ringed in Germany one February and recovered 2,200 km to the east in Russia the next, and a Bullfinch was recovered one winter in Russia 2,000 km to the west of where it had been ringed in the winter of the previous year. Three Mealy Redpolls are known to have wintered in different years at places 1,300, 1,500 and 1,800 km apart. Similarly, a Waxwing Bombycilla garrulus ringed in Poland one February was recovered in the next winter 4,500 km further east in Siberia, and a Cedar Waxwing B. cedrorum ringed in California in April was recovered in Alabama 3,000 km to the east two years later. Presumably all these birds had returned to the breeding range in the meantime, and took quite different directions in the two years. The extent to which an irruptive finch will wander for food is well shown by the North American Evening Grosbeak H espenphona uespertina, which breeds in conifer forests and moves south or south-east in autumn. This species feeds mainly on large, hard tree-fruits, but also visits feeding trays for sunflower seeds, a habit which makes it easy to catch. Over 14 winters, 17,000 Grosbeaks were ringed at a site in Pennsylvania. Of these, only 48 were recovered at the same place in subsequent winters, yet 451 others were scattered among 17 American states and 4 Canadian provinces. Another 348 birds that had been ringed elsewhere were caught at this same locality, and these had come from 14 different states and 4 provinces. These recoveries show both how widely individual Grosbeaks range and how weak is their tendency to return to the same place in later years. The wide wintering range, less rigid directional tendencies, and the poor homing shown by irruptive species are all ways of coping with a

II

c.c·1 P.C.

TC. 1110

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I II I III II UI II II DDIIIII IIUII I I

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1820 1825

0

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Fig. 1. The dates of crossbill invasions into south-west Europe. Filled blocks show large invasions, open blocks small ones. P.C., T.C. and C.C. refer to Parrot Crossbill Loxia pytyopsillacus, Two-barred Crossbill L. leucoptera and Common Crossbill L. curvirostra.

sporadic food supply. They contrast with the marked directional tendencies, narrow migration routes and strong homing shown by birds which feed on more predictable food supplies. The most famous of the irruptive migrants are the crossbills, which feed almost entirely on conifer seeds, and leave the boreal region in large numbers only in exceptional years. Between 1800 and 1965, Common Crossbills Loxia curvirostra irrupted into south-west Europe at least 67 times; sometimes they came in successive years, and at other times at intervals up to 11 years (Newton 1972). Parrot L. pytyopsittacus and Two-barred Cross bills L. leucoptera often came in the same years as Common Crossbills, though less frequently. The ultimate cause (adaptive value) of mass emigration is presumably to avoid food shortage on the regular range, but while some authors have speculated that food shortage is the proximate factor releasing the flight (Svardson 1957), others believe that over-population and crowding present the stimulus to leave (Lack 1954). The hypothesis that best fits the facts is that high numbers are necessary for eruptive migrations of crossbills, but the size of the food crop modifies this (Newton 1972). Once the population is high, emigration probably occurs in response to the first inadequate crop, and only an exceptionally good crop over a wide area will prevent the flight. Once on the move, some birds reach the extreme south-west of Europe, some 4,000 km from their breeding range. Such mass movements by crossbills were formerly regarded as 'death-wanderings', because most birds failed to find areas of suitable food. However, ringing has now confirmed that some individuals return successfully to the boreal forests in a later year. Moreover, those emigrants which find areas with conifers often stay for a year or two and breed, if the cone crops permit. In many irruptive species, the young predominate in invading flocks, and among the adults females outnumber males. This has given rise to the ideas (a) that irruptions follow good breeding seasons, (b) that the young emigrate in greater proportion than the adults, and (c) that more adult hens than cocks leave. In general, this is probably true, as in many regular migrants, but recent information on the composition of irruptive flocks is conflicting. While some certainly contain a high proportion of young, others do not, suggesting that not all movements follow good breeding. Some authors have suggested a cyclic rhythm to the irruptions of seed-eating species, but in most cases there is little evidence for this. This is in contrast to the owls and raptors discussed below. Owls and raptors. Irruptive movements are known from those species which feed on cyclic prey, mass emigration occurring in the 'low' years, when prey are scarce (Newton 1979). Two main cycles are recognized: (a) an approximately 4-year cycle of small rodents on the northern tundras and temperate grasslands; and (b) an approximately 10-year cycle of Snowshoe Hares Lepus americanus in the boreal forests of North America. Some grouse-like birds are also involved, but whereas in some regions they follow the 4-year rodent cycle, with peaks in the same years, in others they follow the 10-year hare cycle. The populations of these various animals do not reach a peak simultaneously over their whole range, but the peak may be synchronized over tens or many thousands of km/. Why such prey species fluctuate with fairly regular periodicity is uncertain, but there is no question that they cause mass movements by their avian predators. Among owls and raptors, the majority of individuals stay in the north of the wintering range in years when prey is plentiful there, and move further south in years when prey is scarce. As in the finches, the food shortage caused by a crash in the prey population is often accentuated because the predators themselves tend to be numerous at such times, as a result of good breeding and survival in the previous few years, when prey was abundant. The main invasions by the Rough-legged Buzzard Buteo lagopus occur at about 4-year intervals, whereas those of the Goshawk Acciptergentilisin North America occur roughly every 10 years, corresponding with the 4-year and 10-year prey cycles respectively. Invasions may occur in only one autumn, or in two successive ones if prey remains sparse. Invasions by Rough-legged Buzzards often occur in the same years as those by Snowy Owls Nyctea scandiaca (both species eat rodents), while in parts of North America the invasions by Goshawks show a similar periodicity to those by Horned Owls Bubo virginianus (both eat hares and grouse). Since the lows in prey populations are not synchronized over the whole range, invasions by anyone species tend to come in different years in different regions. Those by the Rough-legged Buzzard and Snowy Owl are also more marked in North America than in Europe, presumably because the birds are more numerous in North America, having a greater area of breeding habitat (tundra) on that continent.

Italics

Preferred Food

Distri bution

SEED-EATERS Great Spotted Woodpecker Dendrocopos major Waxwing Bombycilla garrulus Cedar Waxwing B. cedrorum Pine Grosbeak Pinicola enucleator Fieldfare Turdus pilaris Coal Tit Parus ater Black-capped and Boreal Chickadees Parus atricapillus and P. hudsonicus littoralis Nuthatch Sitta europaea (Siberian populations) Red-breasted Nuthatch S. canadensis Brambling Fringilla montifringilla Siskin C arduelis spinus Pine Siskin Carduelis pinus Northern Bullfinch Pyrrhula pyrrhula Evening Grosbeak H esperiphona vespertina Redpoll Carduelis fiammea Arctic Redpoll C. hornemanni Purple Finch Carpodacus purpureus Crossbill Loxia curvirostra Two-barred Crossbill L. leucoptera Parrot Crossbill L. pytyopsittacus Jay Garrulus glandarius Thick-billed Nutcracker N ucifraga caryocatactes macrorhynchos Thin-billed Nutcracker N. c. caryocatactes Clark's Nutcracker N. columbiana

Spruce, Pine and other seeds Berries, especially Rowan Berries Conifer seeds, berries Berries Spruce seeds, insects Various seeds, insects Spruce seeds Pine, Spruce seeds Beech seeds Birch, Alder and Conifer seeds Conifer, Birch and Alder seeds Various tree-seeds and berries Maple and other tree-seeds Birch seeds Birch seeds Various tree-seeds Spruce and other Conifer seeds Larch and other Conifer seeds Pine seeds Oak fruits Hazel fruits Arolla Pine seeds Whitebark Pine and other Conifer seeds

Palearctic Holarctic Nearctic Holarctic Palearctic Palearctic Nearctic Siberia Nearctic Palearctic Palearctic Nearctic Palearctic Nearctic Holarctic Holarctic Nearctic Holarctic Holarctic Europe Palearctic Scandinavia Siberia Nearctic

RAPTORS AND OTHER PREDATORS Goshawk Accipiter gentilis Rough-legged Buzzard Buteo lagopus Snowy Owl Nyctea scandiaca Horned Owl Bubo virginianus Short-eared Owl Asio fiammeus Great Grey (or Northern) Shrike Lanius excubitor

Various Grouse and Hares Lemmings, Voles Lemmings, Voles Varying Hares Voles Voles

Palearctic Holarctic Holarctic Nearctic Holarctic Holarctic

Agriophyllum gobicum

Central Asia Turkestan

Some Irregular Migrants of the Northern Hemisphere

STEPPE BIRDS Pallas's Sandgrouse S'yrrhaptes paradoxus Rosy Pastor S turnus (' Pastor') roseus

Many individual raptors must winter in widely separated areas in different years, as in the finches. On their breeding grounds, too, some rodent-eating species concentrate to breed wherever food is plentiful at the time, so that their local populations fluctuate greatly from year to year. This implies that at least some individuals breed (as well as winter) in widely separated areas in different years. So far, however, ringing recoveries of owls and raptors lend no support to this idea because they nearly all refer to birds handled only once as adults. Steppe species. The Rosy Pastor Sturnus roseus is a regular migrant to India from the Asian steppes, but it is sporadic in its breeding, as thousands of birds may settle in a suitable locality, breed and then desert it again. It feeds its young on locusts, and its irruptions occur in spring and early summer, presumably on occasions when it returns on its normal spring migration to find a failure of the locust hatch. The movements of Pallas's Sandgrouse Syrrhaptes paradoxus are probably caused by prolonged drought. Major invasions of sandgrouse into western Europe occurred in 1863, 1872, 1876, 1888 and 1908, and there have been a few other occurrences. Breeding was recorded in Britain in 1888-89 following an irruption. It seems probable that irregular migration is far more widespread than is generally supposed. There is every gradation between irruption and conventional migration, and even species which are normally fairly sedentary perform irruptive movements on occasion. Unexpected movements of this type have been noted, for example, among Blue Tits Parus caeruleus and Bearded Tits Panurus biarmicus. They tend to occur when the birds are especially numerous, or in obvious imbalance with their food-supply. LN. Bock, C.E. & Lepthien, L.W. 1976. Synchronous eruptions of boreal seed-eating birds. Am. Nat., 110: 559-71. Lack, D. 1954. The Natural Regulation of Animal Numbers. Oxford. Newton, I. 1972. Finches. London. Newton, I. 1979. Population Ecology of Raptors. Berkhamsted. Svardson, G. 1957. The 'invasion' type of bird migration. Br. Birds, 50: 314-43.

Locusts (in breeding season)

309

ISCHIUM: a paired bone of the pelvic girdle, partly fused with the other elements (see SKELETON, POST-CRANIAL). ISLAND BIOGEOGRAPHY: see

DISTRIBUTION, GEOGRAPHICAL.

ISOCHRONAL LINE: a line joining geographical localities at which the same event occurs simultaneously; applied, notably, to the mean date of arrival of a given migratory species (see MIGRATION). ISOLATING MECHANISM: a difference between species, or populations of a species, that tends to prevent cross-mating and so to maintain reproductive isolation; such differences are often in factors concerned in recognition, i.e. in appearance (plumage) or behaviour (display, voice). An isolating mechanism is said to be 'specific' when it is adaptively built up between two populations that are genetically capable of interbreeding and of producing fertile hybrids; this can occur only when there is some contact between the two populations, with the production of hybrids that are at a selective disadvantage as compared with the parent stocks. Such specific isolating mechanisms often play an important part in speciation (see SPECIATION; also HYBRID; HYBRIDIZATION, ZONE OF SECONDARY; RECOGNITION; REPRODUCTIVE ISOLATION; VOCALIZATION).

ISOPHENE: a geographical line along which a character of a polytypic species has the same value; 'a line of equal phenotype'. Isophenes run roughly at right angles to the direction of a CLINE. ISOTHERM: a line connecting points of equal air temperature (commonly in terms of the mean temperature for a stated day or month of the year)--see

WEATHER AND BIRDS.

ITALICS: as regards their use in printing scientific names of birds (represented by single underlining in manuscript or typescript), see NOMENCLATURE.

310 Itinerant breeding

ITINERANT BREEDIN G: a series of breeding attempts by the same individual in two or more different geographical areas during the course of the same annual reproductive period, and recurring year after year as a normal event in the annual cycle of the species. The seasonal movement between the successive breeding areas has been termed the 'breeding migration' . Conclusive proof of itinerant breeding, e.g. from ringed individuals, is still lacking but circumstantial evidence points to its occurrence in several tropical and temperate species. The phenomenon was first recognized in the European Quail Coturnix cotumix, where females arriving in Italy in June and July, apparently to breed, often showed regressing incubation patches from a recent breeding attempt and were frequently accompanied by young no more than 2 months old. These young must have hatched from clutches begun in March but at so early a date breeding could have been possible only in North Africa. Reports of a general exodus of Quail from Tunisia in spring after breeding support this and birds ringed there in May and early June have been recovered in Italy and Albania 2-3 months later. It has been suggested that late clutches laid in Britain and northern Europe in August and September could result from an influx in midsummer of birds that have already bred around the Mediterranean. Among tropical species the most suggestive evidence for itinerant breeding is for the Red-billed Quelea Quelea quelea of Africa. The different races of queleas perform migrations whose patterns are determined by the movements of rainfronts across the continent. The birds congregate during the dry season in certain areas where they subsist on the dry grass seed produced during the previous rains. When the next rains break, however, this abundance of dry seed suddenly germinates and is unavailable as food, forcing the birds to leave the area. Queleas are normally able to perform an 'early-rains migration' to areas over which the rainfront has already passed some two months previously and where the new grass has already set seed. The new seed and insects associated with the growing vegetation enable some birds to begin their first breeding attempt straight away, while others begin the slow return movement, the 'breeding migration'. This follows the course taken by the rainfront at the start of the wet season, in the wake of which is now

developing a 'front' of seeding grasses. By remaining within this slowly shifting zone of seeding grass all birds soon reach breeding condition, halt the migration, and establish colonies. Feeding conditions suitable for rearing young do not last long, however, and despite an abbreviated breeding schedule of only 5 weeks, there is not time to rear 2 broods in the same place. The adults abandon the young at 3 weeks old with enough fat reserves to ensure their survival, and continue the 'breeding migration'. On catching up once more with the zone of seeding grasses it is thought that the adults can begin a second breeding attempt, perhaps some hundreds of km from the site of the first, and almost certainly with a different mate. The evidence is circumstantial but compelling; many females begin developing the yolks of a second clutch while still feeding the first brood, yet do not breed again in the vicinity, and in those regions where colonies are likely to contain a majority of birds breeding for the second time on the 'breeding migration', most adults arrive in already very worn plumage, consistent with a previous breeding attempt. In West and southern Africa there is time in wet years for up to 3 broods to be raised in different places along a 'breeding migration' and in East Africa up to 5, though it is unknown if these maxima could often be achieved. It is likely that itinerant breeding will be found amongst other birds living in seasonal environments which offer local opportunities for breeding for too limited a period for more than one brood to be reared. Such species may nevertheless be multibrooded if, by performing a 'breeding migration', they can utilize in turn adjacent regions that become suitable at different times during the annual reproductive period. Prerequisites for such a breeding strategy would be a short breeding schedule with early independence of the young. Species that require a long period of territorial establishment, or which undertake prolonged postfledging parental care, would not be expected to be itinerant breeders. P.J.J. Moreau, R.E. 1951. The British status of the Quail and some problems of its biology. Br. Birds 44: 257-276. Ward, P. 1971. The migration patterns of Quelea quelea in Africa. Ibis 113: 275-297.

J

a

JABIRU: Jabiru mycteria of South America; in the Old World t~e name is sometimes applied to the Saddlebill E phippiorhynchus senegalensisor the Black-necked Stork E. asiaticus. For all these species of Ciconiidae see STORK.

JACAMAR: substantive name of species of Galbulidae

jacamar Galbalcyrhynchus leucotis of Amazonia. Its plumag~ is l~rgely dark chestnut, with white or chestnut ear coverts. A lo?g, thick, pink or whitish bill and short tail give it a topheavy aspect. Plainest and smallest of the jacamars are the 4 species of Brachygalba, which have .largely brown or dusky plumage with white on the under parts, short tails, and . long, sharp, usually black bills. Food. [acamars appear to be wholly insectivorous and, at least In the best-known genera, Galbula and Brachygalba? their 'prey is captur~d on the wing. They rest on an exposed perch, turning their heads from SIde to side, until they spy a suitable flying insect, which. they o~e~take ~y means of rapid sally. Morphos and large swallow-~atls Paptlla,. which .m~st flycatching birds eschew, are often captured by Ja~amars. WIth .the vlc~lm fluttering in its slender bill, the captor retu~ns to ItS ~e~ch, against which it beats the insect long and loudly until the bnlha~1t WIngs flut~er earthward, after which the body is swallowed. Skipper butterflies (Hesperiidae), dragonflies (Odonata), wasps and bees (Hyme~optera), beetles (Coleoptera), and other insects are also c~ptured In la:ge numbers; heliconian butterflies (Heliconiinae) are avoided. The feeding habits of jacamars have been compared to those of Old World bee-eaters. Voice. The Rufous-tailed jacamar is a voluble bird whose sharp calls, sounding afar through the woodland, suggest that it lives ~t a high pitch of excitement. When mated birds are together, and especially when two males compete for a female, their animated vocal performances i~clude an accelerated series of high-pitched notes that may merge Int~ ~ prolonged, clear, soft trill. The Pale-headed jacarnar B.rachygalba ¥oenngl has a similarly elaborate song, but in a weaker VOIce. At their best, jacamars' songs are delightfully melodious. .. Behaviour and breeding. Solitary rather than colonial, jacamars nest chiefly in burrows, which they dig in roadside or streamside banks, in steep wooded hillsides, or in the wall-like root-plate of a gre~t fallen tree. Breeding in cavities in termites' nests has been observed In the G~eat jacamar and several species of Galbula, including the RUfous-tatle~ Jacamar, which usually nests in earthen ?urrows. Both se.xes of this species loosen the soil with fine-pointed bills, and remove It from .the tunnel by kicking vigorously backwards as they enter. The Rufous-tailed Iacamars' burrows range from about 28-50 em in length. At the inner end, they dilate into a chamber that is not lined. The same burrow may be occupied in successive years. The Rufous-tailed jacamar lays 2-4 white, glossy eggs. Few records are available for other species. The Rufous-tailed female incubates through the night, and by day she and her mate sit alternately. Interv~ls of neglect are short, and the eggs are almost constantly attended '. ~hde sitting, the parents regurgitate many shards of beetles and other ChItInoUS parts of insects, which accumulate on the floor of the chamber. The incubation period is 20-23 days. . . . In contrast to the perfectly naked nestlings of most picIfor~ buds, newly hatched jacamars bear copious, long, whitish down. T~eu heels are covered with prominent callous pads that are nearly smooth lI~stead of strongly papillate like those of woodpeckers, to~cans and other bIr~s that breed in unlined holes in trees. Both parents bring the young a variety of insects, but they fail to cl:an the n~st. As they. grow old~r, the l~quaci~us nestlings repeat weak-VOIced versions of then parents calls, Inc.luding pleasant little trills. They leave the burrow when from 19 to (In wet weather) 26 days of age, wearing plumage much like that of adults of t~e same sex. Fledgling Rufous-tailed jacamars seem never to return to their natal burrow; but 4 juvenile Pale-headed jacamars continued fo~ sever~l months to return each evening to sleep with both parents In their 79cm-Iong burrow in a vertical bank. A.F.S.

(Pi~iforme~,

suborder Galbulae): in the plural, general term for the family. ThIS consists of 5 genera and 15 species of small or middle-sized birds (15-31 em long). Characteristics, distribution and habitat. Jacamars are confined to the wooded regions of continental tropical America, chiefly at low altitudes. [acamars have long, pointed, usually slender bills. Their legs are short and in the 4-toed species 2 toes are directed backward. The inner hind toe of the Three-toed jacamar Jacamaralcyon tridactyla has been lost. The more typical species have glittering metallic plumage and, with their long, thin bills, are reminiscent of overgrown humming?ir~s. Perhaps even more than hummingbirds, they seem charged with vitality and intensely alive. They are among the most exciting of all birds to meet. One of the most widespread and familiar members of the family is the Rufous-tailed Jacamar Galbula ruficauda, which ranges from southern Mexico to north-eastern Argentina. Its upper plumage, including the wings and central feathers of the long tail, is glittering metallic green, over which play golden, coppery, and bronzy glints. A broad green band across the chest separates the white throat from the rufous-chestnut of the posterior underparts and the outer tail feathers. The female differs from the male only in having the throat pale buff instead of white. In both sexes, the long, sharp bill is black. Galbula, the largest genus, cont~in~ 7 other species, including the lovely Paradise Jacamar G. dea, distinguished by narrow, greatly elongated central tail feathers. The stoutest member of the family is the Great Jacamar J acamerops aurea, a long-tailed bird (in all 30 ern in length) that ranges from Costa Rica to the Amazon valley. The top of the male's head is bright metallic green, which merges into rich metallic golden or reddish-bronze on the back and shoulders; this in turn becomes bright golden-green on the rump and central tail feathers. The outer tail feathers are violet-blue. The sides of the head and upper throat are metallic green, the lower throat is white, and the remaining under plumage is rufous-tawny. The female is like the male, except that her throat is tawny instead of white. The black bill is only moderately long and slightly curved. A less graceful and glittering member of the family is the Chestnut

Burton, P.J.K. 1976. Feeding behavior of the Paradise jacamar and the Swallowwing. Living Bird 15: 223-238. Sclater, P.L. 1882. A Monograph of the Iacamars and Puff-birds, of the Families Galbulidae and Bucconidae. London. Skutch, A.F. 1937. Life history of the Black-chinned jacamar. Auk 54: 135-14~. Skutch, A.F. 1963. Life history of the Rufous-tailed jacamar Galbula ruficauda In Costa Rica. Ibis lOS: 354-368. Skutch, A.F. 1968. The nesting of some Venezuelan birds. Condor 70: 66-82.

JACANA: name applied to species of th~ Jacanidae

(Charadriifor~es,

suborder Charadrii). African and Australian forms are also called lilytrotters or lotus-birds. The name Iacana is an Anglicized form of the Portuguese name 'jacana' a transliter.ation.of a native Br~zilian name for the bird. The precise systematic relationship of the jacanidae to the other Charadrii is not clear. Superficial resemblances to the Rallidae are due to convergence.

Paradise jacamar Galbula dea. (P.].K.B.).

311

312 Jacana

African jacana Actophilornis afncanus. (C.E.T.K.). Characteristics. Conspicuous adaptations for walking on floating vegetation include long, mostly bare tibia and extremely elongated toes and nails. jacanas are of moderate size (16.5-53 ern). Adult Northern jacanas (Jacana spinosa) weigh only 8~170 g, but their feet cover an area as large as 12 x 14cm. In the Northern [acana sharp spurs on the wrist commonly reach 16 mm; other jacanas also have carpal spurs or knobs. In breeding populations Northern jacana females average 161 g while males average only 91 g. Sexes are monochromatic in all species. The plumage is basically dark reddish or blackish-brown. Five species have white or pale yellow on lower neck, throat and head. Several have pale yellowish primaries and secondaries. The African jacana Actophilomis africanus reportedly moults its flight feathers simultaneously, but the Northern jacana has a gradual moult and is never flightless. Several species have fleshy frontal shields and/or lappets. The downy chicks are striped. Habitat. Jacanas are never found on salt water. All species establish territories and breed on floating, low profile, aquatic vegetation in swamps, marshes, and along streams. In addition to feeding in their territories they may feed in dense emergent aquatic vegetation, wet meadows and short-grass uplands. Outside the breeding' season jacanas may form flocks of up to several hundred birds that feed in meadows, irrigated farmland or other wet areas. Distribution. This circum-tropical family occasionally extends into the sub-tropics (Houston, Texas; Peking). jacanas are found from sea-level to 2,400 m in Kenya, 3,600 m in outer Himalayas. The African [acana occurs throughout sub-Saharan Africa; A. albinucha is found only on Madagascar. The Lesser Jacana M icroparra capensis is found in eastern Africa. The Bronze-winged [acana Metopidius indicus occurs from India through south-eastern Asia, while the Pheasant-tailed [acana Hydrophasianus chirurgus is found from Pakistan east into south-east Asia, southern China, Taiwan, and the Philippine Islands. The Comb-crested jacana or Lotus-bird Irediparra gallinacea occurs in Indonesia and Australia. The Northern or American jacana, which occurs from western Panama northward into Mexico, southern Texas and the Caribbean Islands, is regarded by some as conspecific with the Southern or Wattled Iacana Jacana jacana found from western Panama south to northern Argentina. Populations. Local breeding populations vary from one pair to several hundred. Territory sizes vary depending on the quality and shape of habitat. Territories along streams tend to be linear. Territories of the

Northern jacana average 0.15 ha for males and 0.35 ha for females. Movements. No regular migrations or patterns of movement have been reported. In some areas jacanas occupy territories year-round and breed in any month. In areas with prolonged dry seasons movement to permanent wet lands must occur but no detailed reports are available. In western Costa Rica flocks of 200 to 300 jacanas arrive on the breeding marshes at the beginning of the season; absence of reports of regular movements suggest these are local birds. Food. jacanas feed primarily by gleaning insects from floating vegetation. They also take small frogs, fish and invertebrates from just beneath the surface. Sometimes they turn rooted, floating plants upside down and remove invertebrate prey from amongst the roots. Stomach contents often include plant matter. Northern Jacanas occasionally feed on the ovules of water-lilies. Behaviour. Four species of jacanas are polyandrous. Mating systems in the other species remain unknown. In the Northern Jacana, the bestknown species, males defend small territories from which they exclude all other males. Females defend the territories of one to four adjacent males (polyandrous populations average 1.8-2.4 males per female). The pair co-operates in excluding intruders of both sexes, but the small males cannot exclude persistent females without help. Where jacanas breed year-round, both sexes are replaced by new birds on an individual basis. Deserted territories are promptly occupied by new, previously nonbreeding birds. Neighbouring females sometimes take over an abandoned male and his territory. A new female that attacks and drives a territory owner from her territory is invariably larger than the female she replaces. Where Northern jacanas breed seasonally, courtship and territory establishment occur simultaneously. Initial bonding occasionally occurs between one female and two adjacent males; additional males settle next to existing pairs or interpolate themselves between existing territories and become bonded to the already established females. In continuously breeding populations young sometimes stay on parental territory for more than a year. Where the marsh dries, young and adults leave when the chicks are 4-5 months old. Over short distances the flight appears slow and laboured, with the feet dangling. Sustained flight is stronger and smoother with the legs extending out behind. Although capable of swimming, adult African and Northern [acanas climb out of water as soon as possible. Small chicks of the Lotus-bird regularly dive beneath the surface to hide from predators. Voice. Northern [acana chicks give simple peeps similar to domestic chicks. Adults produce a relatively soft call consisting of very short, wide-frequency notes clustered in repeated groups of 3 to 4 notes. This call is used in non-threatening situations. In response to intruders or predators, adults produce a wide variety of squawks and calls that vary greatly in duration and inter-note interval. Breeding. Breeding continues throughout the rainy season and may be year-round under uniformly wet conditions. Where they occupy territories, year-round bonds between females and their one to four males persist. Where suitable breeding sites are occupied only during the rainy season, new bonds are established each year. Courtship consists primarily of female aggression and male submission and is relatively subtle. Pre-copulatory displays include calling, posturing, nest building, wing raising and other conspicuous acts. Nests are built on floating vegetation, and construction by the Northern Jacana is primarily by the male. He grasps aquatic vegetation in his bill and either tosses it over his shoulder or backs up over the nest site where he drops it. Material is packed in place with the feet. Nests vary but are usually flimsy. Incubation is by the male and lasts 28 days in Northern jacana. The clutch of 4 eggs is laid on consecutive days in the nest of one male. The eggs are glossy with dark markings on a brownish or bronze background, unmarked in Pheasanttailed jacana. The female may start laying a replacement clutch or a clutch for one of her other males 7 days after completing the first clutch. A polyandrous female Northern jacana may copulate with all her mates in less than half an hour, but she does not copulate with a male who is incubating or caring for young chicks. Although females feed in and help defend the territories of all their males they do not necessarily visit every male every day. In the Pheasant-tailed Jacana similar interactions occur between the sexes and they are probably also simultaneously polyandrous. Bronze-winged and African [acanas are less well known, but polyandrous mating groups have been reported. Mating systems in other species are not known, but the larger female size suggests polyandry. Male Northern [acanas usually provide all direct care for chicks. Male African, Northern and Comb-crested [acanas all pick up young chicks

Jynginae

between the wings and body to shelter them from heavy rains. African and Comb-crested males also carry chicks under their wings. In the Northern jacana the female occasionally broods the young. While the male is away feeding, females often stay near chicks where they can detect potential predators. The precocial chicks develop slowly and are dependent on the male for 3-4 months. Young chicks feed when accompanied by their male parent and may actually starve in his absence. D.A.J. Hoffmann, A. 1949. Uber die Brutpflege des polyandrischen Wasserfasans, Hydrophasianus chirurgus (Scop.). Zoo!' [ahrb. (Syst.) 78: 367-403. Hopcraft, J.B.D. 1968. Some notes on the chick-carrying behavior in the African jacana. Living Bird 7: 85-88. Jenni, D.A. & Betts, B.J. 1978. Sex differences in nest construction, incubation and parental behavior in the polyandrous American Iacana (Jacana spinosa). Anim. Beh. 26: 207-218. Ienni, D.A. & Collier, G. 1972. Polyandry in the American jacana (Jacana spinosa). Auk 89: 743-769.

JACANIDAE: see under

CHARADRIIFORMES; JACANA.

JACKASS, LAUGHING: alternative name of the Kookaburra Daeelo novaeguineae, while the Blue-winged Kookaburra D. leaehii is sometimes called the 'Howling Jackass' (see KINGFISHER). JACKDAW: Corvus monedula; also applied to one related species (see CROW (1)). See photos CARE OF SICK, INJURED AND ORPHANED BIRDS. JACOBIN: substantive name of Florisuga mellivora and Melanotrochilus fuscus (for family see HUMMINGBIRD). JAEGER: substantive name, in American usage, for skuas of the genus Stereorarius (as contrasted with Catharaeta-not separated by all authors)-see SKUA. JAW: see BILL;

SKULL.

JAY: substantive name of many species of Corvidae, in various genera; used without qualification, in Britain, for Garrulus glandarius (see CROW (1)). 'Blue Jay' is a misnomer in India for Coraeias benghalensis (see ROLLER). For 'jay-thrushes' (Garrulax) see BABBLER. See photo BROODING.

JERY: substantive name of Neomixis spp. (see JESS: term (plural 'jesses') used in

313

BABBLER).

FALCONRY.

JEWELFRONT: substantive name of the

HUMMINGBIRD

Polyplaneta

aurescens.

JIZZ: combination of characters which identify a living creature in the field, but which may not be distinguished individually. A word coined by T.A. Coward (1922. Bird Haunts and Nature Memories. London). JOURNALS: see

ORNITHOLOGICAL SOCIETIES.

JUGAL: a paired bone of the

SKULL.

JUGGING: sleeping place of Partridge Perdix perdix, where they jug or nestle together; also used of their call when jugging (Oxford English Dictionary). JUGULUM: the foreneck (see TOPOGRAPHY). JUNCO: substantive name of Junco spp. (see

BUNTING).

JUNGLE BABBLER: substantive name of the tribe Pellorneini (see PASSERIFORMES; BABBLER).

JUNGLEFOWL (1): substantive name of Gallus spp. (see PHEASANT; DOMESTICATION).

JUNGLEFOWL (2): name used in Australia for Megapodiusfreycinet; in the plural, serves as a general term for this and allied genera (some also called 'scrubfowl')-see MEGAPODE. JUVENAL; JUVENILE: term of which the first spelling is usual in America, the second in Britain (see under YOUNG BIRD). JYNGINAE: see under

WOODPECKER.

K

and seek a mate when they are about 2 years of age. }.-N.N. and R. de N. Greenway, J.C., Jr. 1967. Extinct and Vanishing Birds of the World. New York. Sibley, C.G. 1972. A comparative study of the egg white proteins of non-passerine birds. Bulletin 39, Peabody Museum of Natural History, Yale.

KAKA: Maori name used for Nestor meridionalis (see

PARROT).

KAKAPO: alternative name (Maori) of the Owl Parrot Stngops habroptilus (see PARROT). KAKARIKI: substantive name used for the Cyanoramphus spp. (Psittacinae, Platycercini) (see PARROT). KAKELAAR: alternative name of Phoeniculus purpureus (see

WOOD-

HOOPOE).

KALIJ: substantive name of some Lophura spp. (see KEA: Maori name used for Nestor notabilis (see KEEL: the carina of the sternum (see

PHEASANT).

PARROT).

SKELETON, POST-CRANIAL;

and

CARINATE).

KERATIN: the main structural protein found in the horny parts of the skin, scales, beaks and feathers of birds. It is also found in the skin and epidermal structures of mammals, reptiles and to a lesser extent lower vertebrates. There are two main types of avian keratin: hard keratin, found in claws, beaks and feathers, and soft keratin, found in the skin. Most research into avian keratin has used hard keratin, especially feathers. Structure. Keratin is a generic name for several groups of closely related proteins which are characterized by their strength, flexibility and resistance to most common solvents and proteolytic enzymes. Avian hard keratins are extremely small and light; they comprise chains of about 100 amino acids, and have molecular weights (MWs) of c. 10,500 daltons (feather keratins) or 14,500 daltons (beak and claw keratins). By comparison, mammalian hard keratins are larger and much more variable; they are usually divided into two main groups, one with a high sulphur content and MWs of 10,500-28,000 daltons and the other with a low sulphur content and MWs of 45,000-50,000+ daltons. Reptile scales appear to be made up of two layers, one mammal-like and the other avian-like, with MWs in the range 10,000-85,000 daltons. All hard keratins are unusually rich in the di-amino acid cystine, which comprises two molecules of the amino acid cysteine. The strength and relative insolubility of keratin structures are due to the formation of strong disulphide bonds between the cysteine molecules in adjacent keratin chains. Sections of feathers studied using the electron microscope show an ultrastructure of parallel rod-like microfibrils in an amorphous matrix. The best model for the molecular structure of feather keratin suggests that the central third of each keratin molecule is folded into a pleated sheet, and that two chains of these pleated sheets are wound helically around a central axis, forming the microfibrils seen with the electron microscope. The ends of the keratin molecules (the other two-thirds) contain most of the cysteine amino acids and are believed both to form the amorphous matrix of the feather structure and to be the sites of the inter-molecular disulphide bonds. Development and keratinization. Keratin is not detectable in chicken embryonic feathers until about the 12th day of incubation, by which stage the feathers are nearing completion of their morphological development. Keratins rapidly then become more abundant and account for most protein synthesis in the feather at 14 days. By 19 days nearly all the protein present in the feather is keratin. The onset of keratinization and the rate of its progress appear to be limited by the amount of keratin messenger-RNA (mRNA) in the embryonic feather cells. Keratinization begins within the cell cytoplasm with the formation of bundles of microfibrils which increase in size until they start to coalesce. Other cellular materials are then reabsorbed from the cells and the bundles finally pack together, trapping a certain amount of cellular debris in the matrix as the cell shrinks and dehydrates. The fully keratinized cell is a totally dead, solid structure. Heterogeneity. Feather keratins are usually made soluble for chemical analysis by reducing (breaking) the disulphide bonds with thioglycollic

Kagu Rhynochetus jubatus. (C.].F.C.).

KAGU: native name, adopted as English, for the mono typic species Rhynochetosjubatus endemic to New Caledonia and sole member of the Rhynochetidae (Gruiformes, suborder Rhynocheti). Although some have considered it close to the Ardeidae, it is probably more closely allied to the Eurypygidae (see SUNBITTERN) or to some other gruiform group (Sibley 1972). Characteristics. The overall colour is slate grey but there is a conspicuous pattern of white, reddish and black bars on the broad, rounded wings (length 29 em) which is visible when they are spread. The head has a long loose crest which is raised during threat displays. The powerful bill (length 6.3 em) is slightly decurved and reddish-orange. The reddish-orange legs and feet are strong, enabling it to run fast. Although flightless, the bird is able to glide down slopes. The sexes are alike but females weigh less than males. The total length is about 60 em. Habitat. The few hundred remaining birds survive in forests which have well developed undergrowth. These are found mainly in the central mountains on the eastern (wetter) side of the island, between 400 and 1,000 m, often close to rivulets. Only occasionally is the Kagu found in primary forest and in savanna. Food. The Kagu eats invertebrates, particularly earthworms. It searches for food by tapping the surface of the ground. When a food item is located under the soil, the Kagu digs it up using its strong bill. Behaviour. Birds move in loose flocks in search of food. Prior to breeding, prs move to higher altitudes. Contrary to earlier reports, the Kagu is active during the day and is only nocturnal when incubating. It has a characteristic habit of running rapidly and then standing motionless; captive birds have been observed whirling round holding the tip of the tailor wing in the bill, but the significance of these antics is unknown. Voice. The Kagu has a variety of harsh, rattling call notes and, in addition, a powerful and solemn predawn 'song' which is a beautiful, melodious succession of notes and pauses; the female answers the male's song. Breeding. The nest consists of a thin layer (10 mm) of dead leaves carefully placed on the ground. Occasionally 3 or 4 active nests per ha have been ocated. The single egg has red-brown and grey blotches on a yellow or creamy ground colour. Eggs are laid in the drier months (May to December); the incubation period is 35 days. The downy young is cryptically marked with black and yellow streaks. The young bird is strong enough at 15 days of age to run rapidly for short distances, and shows some independence in about the 10th week of life when it has half the body weight of an adult (about 900 gm); but the semi-dependent phase lasts until the 14th week or even later. At this age young birds compete partially with the parents for food and the latter begin to be aggressive towards their progeny. Family units break up when the young Kagu is between 6 and 12 months old. Young Kagus defend a territory 314

Kingfisher

acid and preventing them reforming with iodoacetic acid, giving S-carboxymethyl keratin (SCMK). Using electrophoretic techniques the SCMK produces a pattern with many bands showing it to be a complex mixture of many different SCMK molecules (monomers). There is good evidence that each SCMK monomer is a separate gene product; up to 35 different types have been found in many of the feather keratin electrophoretic patterns examined. This agrees well with an experimental estimate of 25-35 keratin mRNAs in chick embryonic feathers. There are believed to be 100-240 keratin genes in the whole chick genome. Such a multiplicity of genes probably arose following repeated duplication of an ancestral keratin gene and a subsequent slight divergence in the sequence of the coding nucleotides in the original DNA and the resulting copies. This has given rise to a large family of slightly different genes, each producing a slightly different protein. Some of the protein amino acid sequences within a species differ by only one in the hundred or so amino acids that make up the keratin monomers. Different parts of each feather (e.g., rachis, barbs) contain different subsets of the complete pool of keratin monomers and therefore give different electrophoretic patterns, but the way these monomers combine to produce the complex structure of a feather is unknown. Corresponding parts of different feathers of the same main type (e.g., flight, contour) from the same bird share the same subsets of SCMK monomers, and there is little or no intra-specific variation in electrophoretic patterns of SCMK from comparable feather parts from different individuals. However, using techniques of adequate resolution, differences have been found between all the species and some of the subspecies examined so far. These differences are of use in taxonomic studies. For example, analysis of SCMK electrophoretic patterns has been used to investigate the relationships of the African Halcyon kingfishers, suggesting, among other things, that the morphological similarity between H. chelicutiand H. pyrrhopygia is probably due to convergence and that the former is more closely related to the H. albioentns-leucocephala-pileata subgenus. Other studies have shown that Bonasa bonasiaand B. umbel/us(Tetraonidae) are not at all closely related despite being treated as congeneric, and that the Palm Cockatoo Probosciger aterrimus is an extremely aberrant member of the subfamily Cacatuinae. The technique has also been used to show that a unique museum skin of a cotinga belonged to a new species and to suggest affinities with other taxa. The availability in museums of feather samples of practically all the extant and many extinct species of birds of the world, together with the refined analytical techniques now available, has made feather keratin a potentially important source of taxonomic information. A.G.K. Brush, A.H. 1978. Feather keratins. In Brush, A.H. (ed.). Chemical Zoology 10. New York. Knox, A.G. 1980. Feather protein as a source of avian taxonomic information. Compo Biochem, Physiol. 65B: 45-54.

KESTREL: substantive name of certain Falco spp.; used without qualification, in Britain, for F. tinnunculus (see FALCON). See photo FLIGHT.

KIDNEY: see EXCRETORY

SYSTEM.

KILLDEER: Charadrius vociferus (see PLOVER

(1».

KINESIS (I): movement of the upper mandible in relation to the SKULL

(see BILL).

KINESIS (2): 'locomotory behaviour not involving a steering reaction

but in which there may be turning, random in direction' (Thorpe)-compare TAXIS.

KINGBIRD: substantive name of Tyrannus spp. (see FLYCATCHER

(2».

KING-CROW: Dicrurus macrocercus (see DRONGO). KINGFISHER: substantive name of all species (except kookaburras Dacelo) of Alcedinidae (Coraciiformes, suborder Alcedines); in the plural, general name for the family; applied without qualification in Britain to Alcedo auhis. A diverse family of 86 species, almost cosmopolitan, but with most species in the Paleotropics and only a few in the Palearctic and the New World. Most are generalized predators of arthropods, small lizards and fish, and inhabit rainforests and woodlands, usually near but often far from water. Three subfamilies are customarily

315

recognized on the basis of morphological (Miller 1912) and biological (Fry 1982) characteristics: Daceloninae (tree-kingfishers, 55 species), Alcedininae (22 small species of insect- and fish-eaters), and Cerylinae (9 species, most large and piscivorous). Generic boundaries have been controversial, but the following genera and numbers of species are now recognized. Daceloninae: Tanysiptera, 6, Papuan subregion; Actenoides(formerly Halcyon), 6, Malaysia to Solomon Is.; the monotypic Cutura (Sulawesi), Lacedo (Thailand to Wallace's Line), Melidora and Clytoceyx (both New Guinea); Dacelo, 4, New Guinea and Australia; and Halcyon (including Pelargopsis), 35, Paleotropics. Alcedininae: Ceyx, 8, Paleotropics; Corythomis, 3, Afrotropics; and Alcedo, 11, Old World. Cerylinae: Chlorocetyle, 4, Neotropics; Megaceryle, 4--one Oriental, one African, one Neotropical and one Nearctic; and the monotypic Ceryle of the Paleotropics. Characteristics. Kingfishers range from 10cm in length and 8 g in weight (Ceyx lecontei) to 46 cm and 500 g tDacelo gigas), but the majority of species weigh between 20 g and 100g. They are large-headed birds with long, strong beaks, the maxilla straight and pointed (hooked in some) and the mandible straight and narrow or deep, wide, and recurved. They are short-necked, short-tailed, and round-winged; the legs are short and the feet weak and syndactyl-the second, third and fourth toes being united basally and the third and fourth for much of their length. The second toe is vestigial in Ceyx fallax and absent in some species of Ceyx and Alcedo, The Alcedinidae is rather a distinctive family, and all of the members show an unmistakable general similarity. The most aberrant is Clytoceyx rex, a large drab bird probably distantly allied with kookaburras (and like them having a shining azure rump); it eats earthworms and the beak is short, broad and deep with scoop-shaped mandibles. Plumages are generally striking and colourful, dominantly non-iridescent dark blue and rufous, with shining azure rumps, and black or scarlet beaks and legs. Cerylines have no blue, but are pied or rufous with grey or oily green. The sexes are alike or nearly so, but in cerylines and a few dacelonines they differ recognizably in the field. Juveniles are generally like adults, but duskier. Kingfishers are territorial, and only 3 are at all gregarious. Dacelonines have loud songs and conspicuous territorial displays; otherwise many kingfishers are rather quiet and inconspicuous birds" seen mainly in fast, direct and nonundulatory flight. Habitat. The interior of tropical rainforest in all strata, its canopy and edges; mangroves; lowland forests with a few species as high as 2,000m; tropical savanna woodlands, farms and gardens; swamps, paddyfields, wooded or grassy margins of rivers and lakes; arid thorn-bush; seashores in tropical and temperate zones, from wooded estuaries to treeless beaches and coral islands. The few species in the Palearctic and Nearctic can be found by almost any waters, particularly in winter (Megaceryle alcyon, M. lugubns, Alcedo atthis) or in any open countryside and woodland (Halcyon pileata, H. coromanda). They perch freely in vegetation, often concealed from view, but also on treetops and any open vantage points from which they can scan the ground or water for prey. A few species regularly forage on the ground, rooting in litter and topsoil for invertebrates, but most perch on the ground only transiently when feeding or nesting. Fishing species use such man-made vantage points as posts, boats and quays. Distribution. The greatest number and diversity of dacelonine species is in the Papuan subregion, and of alcedinine species in that subregion with the adjoining part of the Oriental region. The Papuan subregion has 16 dacelonines of which 13 are endemic there, including some of the most remarkable kingfishers, such as Clytoceyx rex and Melidora macrorhina which have unusual feeding habits (see below). Both subfamilies extend north to Japan and south to Tasmania; alcedinines do not occur east of the Solomon Is. but several dacelonines are endemic to Pacific islands, from the Caroline Is. to the Marquesas Is. To the west alcedinines range to the Atlantic seaboards of Europe and Africa and dacelonines to the Near East and Africa including the Cape Verde Is. Of the cerylines, the 4 green kingfishers Chloroceryle are sympatric in the Neotropics, and Ceryle rudis is widespread in Africa and the Orient (for the range of Megaceryle, see above). Several species are endemic to a small island; for instance Halcyon gambieri is restricted to Niau Is. in the Tuamotu Archipelago and numbers only 400-600 birds. The most widespread kingfisher is Alcedo auhis, breeding from the Baltic to the Cape (treating A. semitorquata as conspecific) and from Morocco to Japan and the Solomon Is.

316 Kingfisher

Movements. Most kingfisher species are sedentary, but the temperatezone ones are migratory at least from more northerly latitudes, and several insectivorous species are intra-tropical migrants. Halcyon leucocephala is migratory throughout its African range and in Nigeria has a two-stage vernal movement northwards (pre-breeding and post-breeding), and one return migration after the rains. Its allospecies H. pileata in the Orient migrates from Korea to equatorial latitudes. Food. The dacelonines are all sit-and-wait predators on a variety of arthropods and small vertebrates taken from the ground, tree-trunks and foliage and the surface of water. They eat insects, spiders, centipedes, scorpions, shrimps, frogs, lizards and, among Halcyon species, some fish, occasionally taking insects by flycatching, and in some cases evidently specializing on crabs (Halcyon (Pelargopsis) capensis) and snails (H. coromanda). Clytoceyx rex subsists largely on earthworms and other invertebrates caught at the surface of the forest floor by foraging in leaf-litter, worms being extracted in the manner of thrushes. Melidora macrorhina, which is evidently nocturnal or at least crepuscular, and at least 2 species of Halcyon sometimes feed on worms likewise, ploughing loose soil with their beaks. These kingfishers, and in particular the largest 2 of the 4 kookaburras, are formidable predators of vertebrates and catch snakes and some birds. Among the Alcedininae, Ceyx species are dry-land insectivores but also take some prey from water. Corythornis (a genus of 1 forest and 2 savanna species intermediate between Ceyx and Alcedo) eat small dry-land and aquatic arthropods and vertebrates; and Alcedo feed almost entirely from water, on arthropods nearly as much as on fish. In the Cerylinae, Chloroceryle and Ceryle are almost exclusively piscivorous, Megaceryle maxima subsists largely on river crabs and M. alcyon takes fish and in addition mussels, clams, oysters, salamanders, young landbirds, mice, a variety of insects (including butterflies taken on the wing) and even, exceptionally, plant matter. Dacelonines capture land prey by swooping down to seize it in the beak and alighting on the ground or a perch to immobilize it by beating. They usually take aquatic prey in much the same way, a splash-and-grab at the surface with subsequent beating at a perch. Species of alcedinines and cerylines (closely related subfamilies) can be arranged in a sequence suggesting evolutionary change from such swooping to more proficient diving and ultimately to reliance on more specialized diving. Evident correlates are a shift from forest floor to forest waterway to open-water habitats and from insectivory to piscivory. Moreover, those species which hunt farthest from the shore are the ones which eat the most fish, and the fish are caught in dives not only from perches but also from hovering flight: A lcedo atthis, A. semitorquata, C hloroceryle amazona, C. americana, Megaceryle alcyon, the marine Halcyon saurophaga , and-the extreme case-Ceryle rudis. No kingfisher other than these 7 is known to hover; and no other species regularly fishes open waters. M. alcyon and C. rudis are spectacular fishers; they scan the water by hovering as high as 12m and make a straight or spiral dive directly downward, but how far they can submerge is not known. Ceryle rudis fishes up to 3 km offshore and in choppy conditions it makes 4 times as many dives from hovering flight as from perches. It can catch 2 fish at once, and swallow a small fish without having to return to a perch to beat it. Voice and behaviour. Detailed accounts have been published for some dozen species; little is known about most others and nests of a few have not yet been described. Breeding biology is apparently rather uniform. Kingfishers are monogamous and territorial. A group of African and Asian Halcyon species maintain their territories by the frequent repetition of a far-carrying song delivered from a tree-top-a loud initial note and a series of evenly-spaced notes on the same or a falling pitch-accompanied by a highly conspicuous display. The bird perches erect with cocked tail, and flicks the wings to show a bold ventral pattern of chestnut, black and white. H. senegalensis pivots rapidly from side to side, holding the wings fully outstretched and vibrating. Mates may display and call together, and duetting occurs in H. chelicuti, an African arid-zone bird in which 20%

of territories are occupied and defended by a mated pair with a

helper. Helpers occur also in Ceryle rudis and Dacelo gigas. Nearly all other kingfishers live in pairs or, after dependent fledglings have dispersed, solitarily; but C. rudis, with up to 5 adult helpers at a nest, is quite gregarious and D. gigas, with helpers at more than half the nests, lives in pairs or perennial groups of 3-6. Kookaburras are obtrusive on account of their permanent occupancy of a socially defended territory and of their infectious 'laughing jackass' song. Alcedinines and cerylines are much less conspicuous in defence of their territories; cerylines are vocal,

Pied Kingfisher C eryle rudis. eN.A.).

but songs and displays among alcedinines are weak or non-existent. Breeding. All kingfishers are hole-nesters, lay sub-spherical white eggs and have no nest sanitation. Dacelonines nest in tree-holes, often expropriated from other birds, remodelling the chamber, and they commonly use holes in termitaria on the ground or high in trees; some, notably the African and Asiatic halcyons, regularly nest also in earth banks, excavating the tunnel themselves. Alcedinines excavate their own nest holes in earth banks by water. Soil is loosened by the beak and kicked out backwards by the legs. The tunnel is horizontal, straight or a little curved, 0.75-1.5 m long, and ends in an oval egg-chamber. Kingfishers never line the nest chamber. Incubation begins with the first egg laid, so the brood is staggered in size. The sexes incubate alternately in a cycle varying from 3-24 hours (Chloroceryle amazona, with the female incubating all night) and even 48 hours (Megaceryle torquata, with each sex taking 24-hour spells of incubation). During incubation the egg chamber becomes fouled with the pungent, watery excrement and with trodden-down pellets of regurgitated insect sclerites or fish bones. Clutches vary from one egg (rarely in Dacelo gigas) to 10 (rarely in Alcedo atthis), with specific means of about 3 to 4 eggs in the tropics and 6 to 7 in the temperate zone. Many species lay second and replacement clutches. The hatchling is naked and prognathous, the mandible projecting up to 2.5 mm beyond the maxilla. Nestlings stand on the heel, not the toes, and have rugose heel-pads. In most species fledglings have the same plumage as their adults, and they continue to be fed by adults for 10 weeks or more. Incubation and nestling periods are not known; incubation has been estimated as 14-16 days for Corythornis; 10-21 days for Alcedo; and about 14 days for Halcyon. The nestling period for Corythornis is at least 25 days. See photo COMFORT BEHAVIOUR. C.H.F. Fry, C.H. 1980. The origin of Afrotropical kingfishers. Ibis 122: 1-17. Fry, C.H. 1982. The evolutionary biology of kingfishers (Alcedinidae). The Living Bird 18 (1981): 113-160. Miller, W . DeW. 1912. A revision of the classification of the kingfishers. Bull. Am. Mus. Nat. Hist. 31: 239-311. Parry, V. 1973. The auxiliary social system and its effect on territory and breeding in kookaburras. Emu 73: 81-100. Reyer, H.-V. 1980. Flexible helper structure as an ecological adaptation in the Pied Kingfisher (Ceryle rudis rudis L.). Behav. Ecol. Sociobiol. 6: 219-227.

KINGLET: in American usage, substantive name of Regulus spp. (see WARBLER (1)).

KINKIMAVO: substantive name of the Madagascar endemic Tylas

eduardi (for family see BULBUL).

KIN SELECTION: the operation of natural selection, not directly on the individual under consideration but indirectly, on related individuals who share a proportion of his genes. Kin selection is one of the mechanisms that have been invoked to explain the evolution of ALTRUISM (see also SOCIOBIOLOGY).

Koklass

KIOEA: the Hawaiian

HONEYEATER

Chaetoptila angustipluma.

KIRITIKA: substantive name of the endemic Madagascar warbler Thamnornis chloropetoides (for family see WARBLER (1)). KISKADEE: substantive name of Pitangus spp. (see FLYCATCHER

(2)).

KITE: substantive name of species of Milvinae, and used also for members of the Elaninae (for both these subfamilies of the Accipitridae see HAWK). KITTIWAKE: substantive name of 2 species of Laridae; used without qualification in Britain for Rissa tridactyla (alternatively, Black-legged Kittiwake), the other species being the Red-legged Kittiwake R. brevirostris of the Bering Sea (see GULL). KIWIS: the smallest and most aberrant of the RATITES and endemic to New Zealand. They are generally regarded as being most closely related to the MOAS (also endemic to New Zealand), each group being given the status of an order, or-as here-together making up the suborder Apteryges, one of the 4 suborders of the Struthioniformes. There are yet other alternative schemes for classifying the ratites, perhaps the most common recent ground for agreement being that they are monophyletic in origin. Both kiwis and MOAS are regarded as being descendants of the Gondwanaland fauna and thus the most ancient elements of New Zealand's recent avifauna. There are 3 species: Apteryx australis the Brown-or Common-Kiwi (subspecies, A. a. australis South Island, A. a. mantelli North Island and A. a. lawryi Stewart Island); Apteryx oweni the Little Spotted Kiwi (North and South Islands, no subspecies); Apteryx haasti the Great Spotted Kiwi (South Island only, no subspecies). No recently exinct species are known and the earliest fossil kiwi (Pseudapteryx gracilis) dates from the Quaternary. However, footprints attributed to the family have been found in Upper Miocene mudstone. Characteristics. Kiwis are 35-55 em long. Distinctive features include a long and slightly decurved bill with nostrils near the tip, a cone-shaped body tapering markedly to a strong neck and comparatively small head, small eyes, large ear apertures and many long tactile bristle-like feathers about the face and base of the bill, powerful muscular legs (which make up about one-third of the body weight), large feet with stout claws, and very small virtually bare wings (4-5 em in length) which end in a claw and are hidden in the plumage. There is no external tail. The plumage is brown or grey, loose and hair-like, and does not change in form throughout life. Its neotenous characteristic of having weak barbs and lacking aftershafts gives the birds a shaggy appearance. The largest kiwis (the Stewart Island race) have females weighing at least 3.5 kg, the smallest (Little Spotted) about 1.2 kg. Females are about 20% heavier than males and their bills 25-30% longer. With the exception of the Stewart Island race (which is also active during the early morning and evening) kiwis are nocturnal and uncomfortable in broad daylight. Habitat. Though primarily birds of the indigenous forests (kauri, podocarp or southern beech), kiwis may also occur in scrub, native

317

grasslands and even in exotic forests and pastures. Among critical environmental factors may be soil texture, its humus content, atmospheric humidity and dense vegetation overhead; certain combinations of which may be essential for kiwis to burrow and feed in and for the development of a suitable soil fauna for food. Nothing reliable is known about differences in habitat requirements that separate the 3 species. Distribution and populations. Originally Brown and Little Spotted Kiwis had a wide distribution on both main islands and D'Urville Island (which is separated from the South Island by a shallow strait only about 1 km wide and of post-glacial origin). Apart from the Stewart Island race of A. australis, they are not known to have occurred on any other islands. Now, they have gone from the east coast of the South Island (subfossil records only) and the southern and south-eastern parts of the North Island. The Little Spotted Kiwi has apparently been extinct in the North Island for about a century and is thought to be extinct in the South Island and survives only on Kapiti I. where it was introduced in 1913. The Great Spotted Kiwi is now found, apparently in good numbers, on the western side of the Southern Alps, mainly north of 43°S. More detailed information is needed on the distribution of all kiwis, especially to determine the extent to which overlap, spatial as well as ecological, occurs. Kiwis have been successfully' introduced to offshore islands and will readily breed in captivity, so the ultimate survival of all species and subspecies seems assured. They have no native predators, and do not seem to be unduly sensitive to predation by the various introduced mammals (rats, mustelids and cats), though the Little Spotted Kiwi may be an exception. However, many are maimed or killed by being caught in traps set for the introduced Australian possum or by being burnt or crushed in forestry or land-clearing operations. Nevertheless, kiwis have long been fully protected by law and have added protection where they occur in national parks or similar reserves. Food. All 3 species have the same general food habits but little is known in detail. Earthworms are the principal item of diet, though woodlice, millipedes, centipedes, slugs, snails, spiders, a wide range of insects, seeds and berries are also taken. The highly developed sense of smell is apparently important in finding food. Voice. Although each species and subspecies has contact calls of characteristic quality, all are essentially similar-males utter a shrill and prolonged whistle with a slightly ascending and then brief descending pitch (from which the species' name is derived); females have a hoarser and lower cry. These are heard at dusk, during the night and near dawn. When alarmed or aggressive, kiwis growl, hiss and loudly snap their mandibles. The other common noise is a loud snuffling made by expelling air forcibly through the nostrils while feeding. Breeding. It is not known what stimulates breeding-the egg-laying period extends from July (late winter) to February (late summer). A functional right ovary is always present but only the left oviduct. The age of sexual maturity is unknown, but is likely to be at least 2 years. Studies of captive kiwis have shown that after about 2 months of burrowing or otherwise preparing a nest site, mainly by the male, the first egg is laid. Captive females may lay up to 5 eggs in a continuous series with a mean interval of 33 days between each; but in the wild clutches contain 1, 2 or rarely 3 eggs (each 18-25% of the female's body weight, depending on the species). The heavily yolked (61%) white-shelled egg is incubated almost entirely by the male for some 74-84 days before the chick hatches active, open-eyed and fully feathered. G.R.W. Cracraft, J. 1974. Phylogeny and evolution of the ratite birds. Ibis 116: 494-521. Reid, B. & Williams, G.R. 1975. The kiwi. Pp. 301-330. In Kuschel, G. (ed.). Biogeography and Ecology in New Zealand. The Hague.

KLEPTOPARASITISM: see

FEEDING HABITS; PIRACY.

KNEE: for both the true knee and for a popular misconception on the subject see LEG. KNOT: substantive name of Calidris canutus and one congener (see SANDPIPER).

KOEL: Eudynamys scolopacea (see

CUCKOO).

KOKAKO: Callaeas cinerea (see WATTLEBIRD Brown Kiwi Apteryx australis. (N. W.C.).

KOKLASS: Pucrasia macrolopha (see

(2».

PHEASANT).

318 Koloa

KOLOA: alternative name (indigenous) for the Hawaiian Duck Anas 'WjJviliiana (for family see DUCK). KOOKABURRA: substantive name of Dacelo spp. (see

KORI: Ardeotis kori (see KRONISM: see

BUSTARD).

CRONISM.

KINGFISHER).

KORHAAN: substantive name of some South African species of Eupodotis (see BUSTARD).

K-SELECTION AND r-SELECTION: see graph).

ECOLOGY

(final para-

L L. LINN. LINNAEUS: see

NOMENCLATURE.

LABYRINTH: part of the ear (semicircular canals)--see HEARING AND BALANCE.

LAGENA: part of the cochlea, in the inner ear (see

HEARING AND

BALANCE).

LAGGAR: Falco jugger (see

FALCON).

LAMELLAE: in birds, fine hair-like structures lining the bills of some species, enabling them to filter small food particles (see BILL; FEEDING HABITS).

LAMINIPLANTAR: having the horny sheath of the tarsus undivided on its posterior surface, although scutellate on the anterior surface (see LEG); compare BOOTED.

open spaces. They rarely perch on vegetation to feed although some species do so regularly to sing. Like pipits and some buntings which also spend much time on the ground, larks have long, generally straight claws on their hind toes. Larks differ structurally from other Passeriformes in lacking an ossified pessuius in the syrinx and in having the posterior surface of the tarsus covered by scutes rather than an unbroken lamina. Most larks have cryptic brown or buff plumage with dark streaks. The sexes are usually similar in appearance though in a few cases (e.g., Melanocorypha yeltoniensis, some Eremopterix) they differ, with the male being more strikingly marked though not in bright colours. Many species have a marked size dimorphism, the males being larger than females. Habitat. Larks live in open country including hot and cold deserts, tundra, moors, grasslands, steppe, savanna and farmland. Nests are always on the ground so the abundance of trees and bushes is not important in determining the availability of nesting cover. However, sympatric species often differ in the preferred density of trees and bushes in the habitat. Skylarks Alauda arvensis tend not to feed near tall hedges or woodland even when food is abundant there. Woodlarks Lullula arborea are superficially similar but are less averse to feeding near cover and live in areas with scattered trees or by woodland edges. The colour of the soil is an important habitat feature for some desert-dwelling larks (Ammomanes, Mirafra, Certhilauda, Eremopterix) which tend to live in areas with soil similarly coloured to their plumage. In some species birds avoid landing on ground with contrasting soil colour even when driven over it. This matching is presumably an adaptation providing concealment from avian predators (see COLORATION, ADAPTIVE).

Distribution. A predominantly Old World family with one species, the Shore Lark Eremophila alpestris, in the Americas. Three-quarters of the 76 species occur in Africa and over half are only found there. Only one species (Mirafra javanica) occurs in Australia and New Guinea. Populations. Larks generally occur at lower population densities than are typical of similarly sized woodland or scrub-dwelling passerines, which is probably due to the simple vegetation structure and low productivity of their preferred habitats. However, suitable habitat often covers vast tracts of land (e.g., deserts, tundra, arable farmland) so total populations may be very large. For example, the tundra dwelling Shore Lark is one of the world's most numerous birds. Population densities of Skylarks are 10-50 pairs/km/ on arable farmland in England and up to 70 pairs/km/ on coastal dunes. Woodlarks also occur at fairly low densities with territories 5ha or more in extent. Population densities of desertdwelling larks are very variable in space and time, since many species are nomadic, and are also usually low, though pockets with densities up to 1,250 pairs/km/ can occur in Eremopterix spp. where rain has fallen. The average annual mortality rate for adult Skylarks is about 33% which is low for a temperate small passerine. Movements. The family includes long distance and partial migrants and sedentary species. All North Temperate larks are at least partially migratory. Some species living in arid areas are nomadic, moving between areas of localized rainfall and abundant food. In the Kalahari desert granivorous species such as Calandrella conirostris and Eremoptenx spp. are nomadic, while larks which include more arthropods in their diet are mainly sedentary. In the short term, frequent movements are made by some larks (e.g., Eremopterix) to waterholes to drink while other desert species appear to derive sufficient water from dew and food. There may be a correlation with diet; species feeding on arthropods and green vegetation being less likely to need to fly to water than those taking dry seeds. Food. As a family, larks feed on a great variety of foods including seeds, flowers, buds, leaves, seedling cotyledons, molluscs and arthropods. A large proportion of species take a broad range of foods but some are specialized in feeding on insects or seeds. Omnivorous species have a conical, straight bill (e.g., Alauda, Galerida) while seed-eating specialists such as Eremopterix, Melanocorypha and Calandrella have deeper, finchlike bills. The Hoopoe Lark Alaemon alaudipes and some other species have thin decurved bills which they use to dig for soil arthropods. All larks search for food by walking. The Skylark is an omnivorous species with an unspecialized bill. On arable farmland it feeds on grain, weed seeds, leaves and cotyledons and insects, particularly beetles. Grain and seeds are not hulled as they are by finches and buntings since the bill lacks the grooves within the upper mandible used to hold the seed by these groups. Although Skylarks may feed almost entirely on leaves of cereals in midwinter, they have a short intestine and lack the large caeca of larger

LAMMERGEIER: name, alternatively 'Bearded Vulture', of Gypaetus barbatus (see VULTURE (1)). LANCEBILL: substantive name of Doryfera spp. (for family see HUMMINGBIRD) .

LANCEOLATE(D): spear shaped. LAND-BRIDGES: see

GEOLOGICAL FACTORS.

LANDRAIL: alternative name (probably obsolescent) for the Corncrake Crex crex (see RAIL). LANGERHANS, ISLETS OF: see ENDOCRINOLOGY AND THE

REPRO-

DUCTIVE SYSTEM.

LANIIDAE: a family of the

PASSERIFORMES;

suborder Oscines;

SHRIKE.

LANNER: Falco biannicus (see

FALCON).

LAPAROTOMY: the minor surgical process used to assess the state of the internal organs of an animal. Typically involves making a small opening (1-2 mm) between the ribs and then using a powerful light source to look into the body cavity. General or sometimes a local anaesthetic is used. Valuable in sexing birds. LAPPET:

a

wattle,

particularly

one

at

the

gape

(see

IN-

TEGUMENTARY STRUCTURES).

LAPWING: substantive name of some Vanellus spp., others being called 'plover'; used without qualification for V. vanellus; in the plural, general term for plovers of this genus (split by some authors into several genera constituting a subfamily Vanellinae)--see PLOVER (1). LARDER: a collection of prey items impaled on thorns or barbed wire by shrikes (Laniidae) and some other birds. LARI: see under

CHARADRIIFORMES.

LARIDAE: see under

CHARADRIIFORMES; GULL.

LARK: substantive name of the species of the family Alaudidae (Passeriformes, suborder Oscines). Characteristics. Larks are small (11-19 em) ground-feeding birds of 319

320 Lark

at the beginning and end. Incubation is for 10-12 days by the female alone or by both sexes in some species. The young are fed by both parents and leave the nest well before they can fly, usually at about 10 days old. The down of the nestlings is cryptically coloured. Leaving the nest early is probably an anti-predator adaptation, reducing the risk of loss of a whole brood collected at one place, although movement of the young may also be beneficial in reducing the distance the adults have to carry food; the feeding areas are sometimes far from the nest. Losses of nests and young to predators are often high, 80% of eggs failing to produce fledglings for 7 species in the Kalahari and 90% of eggs failing to give rise to independent young for Skylarks on coastal dunes in England. Breeding is annual in temperate and arctic larks but is initiated after rainfall in many desert species. Skylarks begin to breed in the year after hatching. R.E.G.

Skylark Alauda arvensis. (D. W.).

herbivorous birds. Larks which take green leaves probably select plant species and growth stages rich in nutrients. Skylarks feed on weed and crop seedlings with high-protein levels. Stark's Lark Spizocorys starki in the Namib desert feeds on grass seedlings soon after germination. Gray's Lark Ammomanes grayi and Stark's Lark also select the tender basal node of grasses, discarding less digestible parts. Most larks feed their young on insects though some feed seeds by regurgitation (e.g., Eremopterix leucotis). On arable farmland Skylarks collect weevils, click beetles, grasshoppers, caterpillars and sawfly larvae for their young from rough grass and weeds at field edges. Desert-dwelling larks in southern Africa exploit ant and termite colonies, particularly when these are producing sexuals, and also locust nymphs. Behaviour. Most larks breed on dispersed territories and are monogamous. Breeding territories are defended by song and chasing. Skylarks sing and visit the territory for much of the year in England as do some Mirafra larks in southern Africa. Nomadic desert species such as Stark's Lark may only be territorial and sing when breeding. Song and territory may function more to attract a mate than to maintain a feeding area which may be more important in sedentary species. Skylarks tend to remain faithful to a breeding site from year to year. In the Namib desert Gray's Lark lives in small groups throughout the year; territoriality is not strongly developed, with courtship and mating sometimes taking place within the group. Many lark species associate in flocks when not breeding. In southern Africa nomadic species form the largest and most cohesive flocks. Skylarks and Shore Larks migrate in flocks. In hot deserts larks show behavioural adaptations to avoid overheating. Karroo Larks Certhilauda albescens and Stark's Larks become inactive and sit in shade during the hottest part of the day while Spike-heeled Larks Certhilauda albofasciata and Gray's Larks, foraging partly in the shade around the entrance of rodent burrows, are able to remain active. Larks roost on the ground and do not roost communally. Voice. Song is well developed and long in many species, often delivered during a song flight or from a prominent perch. The song flight incorporates a rapid dive to the ground in several species. the wings and sometimes the tail are used in sound production in some larks, especially Mirafra, though these also sing. Flight calls are uttered by single and flocking birds. In the Skylark single birds usually call chir-r-rup while those in cohesive flocks call seep. Breeding. All larks nest on the ground. Often the nest is a scraped cup but on hard substrates a foundation may be built to support the sides of the cup. The cup is often lined with grass grass fibre. Sand larks (Ammomanes) and finch-larks (Eremopterix) build a rampart of pebbles on the windward side of the nest. This may act as a windbreak and prevent the nest filling with sand. Shore Larks also collect pebbles and other objects around the nest. In hot deserts lark nests are often built close to a stone or tuft of grass which shades the nest during the hottest part of the day. Nest ramparts may also contribute to shading the nest as well as perhaps partly concealing the nest from predators at ground level. The eggs are usually cryptically streaked or spotted. Clutch-sizes are larger in arctic and temperate larks (average about 4 eggs) than in tropical Africa (2-3 eggs). In Africa clutch-size tends to be larger in species living in more arid, less wooded habitat. Skylarks in England show a seasonal variation in clutch-size with mid-season clutches being larger than those

or

Delius, J.D. 1965. A population study of Skylarks Alauda arvensis. Ibis 107: 46fr.492. Green, R.E. 1978. Factors affecting the diet of farmland skylarks Alauda arvensis J. Anim. Ecol. 47: 913-928. MacLean, G.L. 1970. The biology of the larks (Alaudidae) of the Kalahari sandveld. Zoologica Africana 5: 7-39. Willoughby, E.J. 1971. Biology of larks (Aves: Alaudidae) in the central Namib desert. Zoologica Africana 6: 133-176.

LARK, MAGPIE: see

MAGPIE-LARK.

LARK, MEADOW: see

MEADOWLARK; ORIOLE (2).

LARK-QUAIL: name, alternatively 'quail-plover' (misnomer), of Ortyxelos meiffrenii (see BUTTONQUAIL). LARK, SONG-: see

SONGLARK.

LARO-LIMICOLAE: Stresemann's order equivalent, in the classification here followed, to the order Charadriiformes less the families Jacanidae, Thinocoridae, and Alcidae. LARYNX: see

RESPIRATORY SYSTEM; SYRINX; TRACHEA.

LA TEBRA: core of fluid white yolk at the centre of an LATENT LEARNING: see

LEARNING.

LATEROSPHENOID: a paired bone of the LATIN NAME: see

EGG.

SKULL.

NOMENCLATURE.

LATIPLANTAR: having the hinder aspect of the tarsus flat (applied to oscine Passeriformes); opposite of ACUTIPLANTAR (in general, see LEG). LAVEROCK: archaic name for the Skylark Alauda arvensis (see LARK). LA YING: the deposition of the egg; the act of oviposition. Oviposition. At ovulation the ovary releases a yolk (ovum) into the body cavity. Within half-an-hour it is engulfed by the upper end of the oviduct, the infundibulum, and it then passes through three further regions of the oviduct (see ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM). In the 'magnum', the chalazae and the thick albumen are added; in the 'isthmus', inner and outer shell membranes are formed; and in the 'uterus' or shell-gland, where the egg remains for 20-24 hours, it undergoes a 25% osmotic increase in volume, the chalky shell is deposited, and (mainly in the last hour before laying) pigment and the cuticle may be formed (see EGG). The times given apply to the domestic hen, in which the whole process from ovulation till laying takes about 24-27 hours. The method by which the egg is carried through the oviduct has not been demonstrated conclusively. Some maintain that it is moved entirely by ciliary action, and others that it is propelled by peristaltic movements of the oviduct (Gilbert 1971). In the oviduct the egg lies with its pointed end towards the cloaca and in many species, e.g., domestic pigeon, eggs are correspondingly laid pointed pole first. In other species, e.g., Black-headed Gull Larus ridibundus, domestic hens and ducks, eggs are quite often laid blunt end first; this happens in 29% of the eggs of Khaki-Campbell domestic ducks. By using X-rays, it has been shown

Laying

that such eggs undergo a quick 180 rotation (in a horizontal plane) an hour before they are laid. On rare occasions this rotation precedes the formation of pigment spots; the latter then collect round the pointed pole of the egg. Rotation is more frequent in some individuals than in others, and its incidence increases with age, presumably because the uterus wall becomes more stretched with repeated layings. How the egg is actually released from the body has for long been a matter of controversy. Some maintained that the whole uterus (with contained egg) prolapses through vagina and cloaca to the exterior, where the uterine wall everts, thus unwrapping the egg and leaving it outside. Sykes (1953), however, observed, in laparotomized hens, that the uterus is not everted during oviposition; instead, the egg passes from the uterus into the vagina and is then pushed out by peristaltic action of the vaginal muscles. In intact birds he showed, also, that the distension of the vagina by the egg evokes a ventroflexion of the legs and erection of the feathers surrounding the vent, as well as 'bearing down' contractions of the abdominal muscles and increased respiratory movements causing a rise in the abdominal pressure. The egg may be expelled after a period of bearing down lasting 1-3 minutes. In social parasites, e.g., cowbirds Molothrus spp. and cuckoos (Cuculinae), the process is a matter of seconds. A Bobwhite Quail Colinus virginianus needs from 3-10 minutes at the nest to lay an egg, whereas Turkeys Meleagris gallopavo and geese Anser spp. are reported to labour for 1-2 hours. A bird that cannot lay its egg is called egg-bound; this condition may be caused by inflammation, stricture, or tumour in the oviduct; sometimes a malformed, oversized, or soft-shelled egg may be responsible. An egg that is ready for laying can be held back; a Cuckoo Cuculus canorus is thus able to wait until the nest-owner has left the nest (see BROOD-PARASITISM). Many song-birds postpone laying while quickly constructing a new nest when the old one has been damaged or removed. For review of the hormone and neural control of oviposition, see Gilbert (1971), Sturkie and Mueller (1976). Age of bird. Captive Quail Coturnix coturnix reproduce at 6 weeks of age, some individuals laying as early as 38 days (Science 129: 267). Most breeds of domestic hen begin laying at 5-7 months; most passerines, pigeons (Columbidae), and ducks Anas spp., etc., many gallinaceous birds, and some owls (Strigiformes) at one year; geese, many gulls (Laridae), and birds-of-prey, some waders (Charadriidae), and a few passerines at 2 years; cormorants (Phalacrocoracidae), divers (Gaviidae), and the larger gulls at 3 years; the large birds-of-prey and storks (Ciconiidae) when 4-6 years old, and the Royal Albatross Diomedea epomophora not until it is at least 8 years old. In many of these species the age at which breeding first occurs may vary with the individual. These differences are often explained by stating that larger birds require longer to mature than those of smaller size. More convincing is Lack's suggestion that breeding imposes a strain on the parents that may have been too great for the young individuals in some species, thus leading to adaptive retardation of the breeding age (Lack 1968). This is particularly the case for species with specialist feeding techniques, for themselves or for their young. For example, neither Arctic Tern Sterna paradisaea nor the Puffin Fratercula arctica breed before 3 years, rather later than do land birds of equivalent size. Breeding also takes place earlier in low-density populations with little adult competition than it does in more crowded ones, as expected if inexperienced females find it easier to collect enough food for egg formation when fewer birds are present. Time of year. Like other reproductive activities, egg-laying is restricted \.0 particular seasons of the year in most birds (see BREEDING SEASON). In general it is so timed that the young grow up when their food is most abundant, or when the female can find enough food to form eggs (Perrins 1970). In temperate and cold climates, the proximate factors controlling the time of egg-laying are increase in day-length in late winter and warm temperatures in early spring. In the tropics the rainy season determines the onset of breeding in many passerines. In special cases other factors and adaptations may be involved; thus the Great Crested Grebe Podiceps cristatus does not normally breed until the vegetation supporting its floating nest has grown up. Eiders Somateria mollissima, Common Gulls Larus canus, and Herring Gulls L. argeniatus in the Arctic are reported to postpone breeding on islets until the surrounding ice has melted, which may be an adaptation against robbing by Arctic Foxes Alopex lagopus. The date of laying of the first egg varies somewhat from year to year and between individuals; in many species, birds laying for the first time tend to do so a few days later than older ones. According to one view, birds of a colony influence one another's reproductive activities 0

321

in such a way that bigger colonies lay earlier in the season and within fewer days, i.e., are more closely synchronized, than small ones. Other studies do not support either statement, but it appears that small colonies may lay later in the season because they include a larger proportion of young birds than bigger colonies. Time of day. Some birds lay only at a particular time of day; many song-birds such as finches (Fringillidae), wrens (Troglodytidae), tanagers (Thraupinae), wood-warblers (Parulidae), and hummingbirds (Trochilidae) around sunrise; pigeons (Columbidae) early in the afternoon; pheasants (Phasianidae) in the evening. In a flock of domestic hens, 56% of the eggs were laid between 9 am and 1 pm. Successive eggs may not be laid at the same time of day; in the domestic pigeon the second egg appears 44-46 h after the first and is thus laid earlier in the day. The laying pattern, i.e., the time interval between the laying of successive eggs, is characteristic for a species. This interval is 20-24h for most but not all passerines and for many ducks; 24-28 h for the domestic hen; 24-72 h, with an average of 40 h, for the Black-headed Gull; 2 days for the Raven Corvus corax, Ostrich Struthio camelus, and Rhea Rhea americana; 3 days for cassowaries C asuarius spp; 5 days for the Condor Vultur gryphus; and for the Masked ('Blue-faced') Booby Sula dactylatra a 6-7 day interval has been reported. The interval probably corresponds to the time necessary for the formation of the various layers of the egg. It is known that in the domestic hen ovulation usually follows the laying of the previous egg within about 30 minutes, except when the previous egg is laid late in the afternoon-in which case ovulation is delayed until the next morning. Number of eggs. Most birds lay eggs in a clutch-they lay a few eggs in sequence, then stop and incubate. The domestic hen is a notable exception, laying continuously for a large part of the year. Here cycles of 3, 4 or more days of uninterrupted laying are separated from one another by one or a few days of non-laying. The annual output declines steadily with increasing age and so does the length of the laying season; 351 eggs in one year and 1,515 eggs laid within 8 years by a single hen have been recorded. The number of eggs in a clutch (clutch-size) varies with the species. Some lay only 1 egg; others regularly have clutches of 2, 3, or 4; others show more variability, especially where the number is large (such as 10-20 for the Partridge Perdix perdix). In many species clutch-size varies between populations, with the individuals of a population, and even for one individual in different years. The average clutch-size of a population has been shown to be delicately adjusted to yield the maximal number of successfully reared young (Lack 1968). It is influenced by such factors as the age of the parents, seasonal influences responsible for the availability of food later in the year, and population density (see EGG; CLUTCH-SIZE). Determinate and indeterminate layers. Little is known about how the regulation takes place-what are the climatic (or other) indicators of abundance of food later in the season, and by what means they affect the activity of the ovary. A further complication arises from the fact that 2 types of egg-laying mechanism may have to be distinguished; in some birds (indeterminate layers) the number of eggs laid can be changed by adding or removing eggs during or just before the time of laying; in other birds (determinate layers) this has no influence. In the latter case, presumably, the ovary produces only as many yolks as eggs will be laid. Experimental addition of eggs to the first egg of the clutch may reduce the number of eggs laid subsequently, e.g. in the Tricolored Blackbird Agelaius tricolor of North America. In many other species, e.g., Swallow Hirundo rustica, pigeons, gulls, and the Lapwing Vanellus vanellus, this has no effect; but if eggs are presented a few days earlier in some of these, egg-laying may be suppressed fully or partially-thus a Black-headed Gull sitting on model eggs for 2-8 days before laying its first egg may lay only 2 or 1. Removal of eggs, so as to leave only one or a few in the nest, increases the number to be laid in many species. Such protracted laying occurs, e.g., in the Yellow-shafted Flicker Colaptes auratus (where one female laid 71 eggs within 73 days) and in other woodpeckers (Picidae); a Mallard Anas platyrhynchos is reported to have laid 80-100 eggs when one was removed daily, and a House Sparrow Passer domesticus laid up to 50 eggs in succession (of which 12-19 were laid on consecutive days) instead of the usual clutch of 4-5. These and many other birds thus qualify as indeterminate layers. In a few others, e.g., Swallow, Magpie Pica pica, Gentoo Penguin Pygoscelis papua, Lapwing, and gulls, this procedure has no influence on the number of eggs laid. Nevertheless some of these have been shown to be indeterminate layers; they will lay additional eggs at normal intervals if the first egg

322 Leading line

is taken as well, i.e., if all eggs are removed as soon as they are laid. In these circumstances the Lapwing and Gentoo Penguin will lay one and gulls 3 more additional eggs. In pigeons, egg-laying could not be protracted in this way (Poulsen 1953). In the ovary of an indeterminate layer more oocytes may enter the final phase of growth than are normally laid, and tactile or visual stimuli from the eggs in the nest are responsible for the cessation of laying. In some species, e.g., gulls, the end of laying is determined not by a definite number of eggs in the nest but by the opportunity for the bird to incubate. Only a limited number of eggs are laid after the onset of incubation, which causes all oocytes under a critical size in the ovary to degenerate. In species that do not incabate before the clutch is complete this explanation cannot apply. Here it is the critical number of eggs in the nest that stops the growth or causes the degeneration of superfluous oocytes. In neither case can laying be protracted once the reserve follicles have started to degenerate, i.e., one or more days after the onset of incubation. N umber of clutches. Many wild birds normally lay only one clutch in each year, but there are others that have two or more broods in a season. The domestic pigeon may lay up to 10 clutches a year. In most species (but not the domestic pigeon) the number of eggs tends to decrease with each successive clutch. In Megapodiidae there may be no clutch in the ordinary sense; the eggs, often very numerous, are laid at intervals throughout several months, and there is no synchronization of incubation and hatching (see MEGAPODE).

Most birds with only one brood annually, and all of those with more than one, are able to replace the clutch when it is lost (repeat laying); a Black-headed Gull will lay again 8-12 days after the loss. Exceptions are some big vultures (Aegypiinae) and most Procellariiformes. Repeat clutches tend to be smaller than the first one. (V.W.) S.G.T. Gilbert, A.B. 1971. Transport of the egg through the oviduct and oviposition. In Bell, D.]. & Freeman, B.M. (eds.). Physiology and Biochemistry of the Domestic Fowl. Vol. III. London. Lack, D. 1968. Ecological Adaptations for Breeding in Birds. London. Perrins, C.M. 1970. The timing of birds' breeding seasons. Ibis 112: 242-255. Poulsen, H. 1953. A study of incubation responses and some other behaviour patterns in birds. Vidensk. Medd. Dansk Naturh. Foren. 115: 1-131. Sturkie, P.D. & Mueller, W.]. 1976. Reproduction in the female and egg production. In Sturkie, P.D. (ed.). Avian Physiology 3rd ed. New York. Sykes, A.H. 1953. Some observations on oviposition in the fowl. Quart. J. Exp. Physiol. 38: 61-68.

LEADING LINE: see

MIGRATION.

LEAD POISONING: see

DISEASE.

LEAFBIRD: substantive name of the species of the genus Chloropsis of the Chloropseidae (Passeriformes, suborder Oscines). Members of a second genus, Aegithina, are called ioras. There is no accepted collective in English. Characteristics. Small to medium-sized, wholly arboreal passerines 12-19cm long in the weight-range 1{}-40g, with small toes, tarsi slender in ioras, short and thick (similar to bulbuls) in leafbirds; bill medium to fairly long and slender, terminally decurved to hooked and finely notched; wing and tail of moderate length. All have ample, fluffy body plumage, long on the rump. Leafbirds resemble fairy-bluebirds (Irenidae) and bulbuls (Pycnonotidae) in profusely shedding feathers when handled. During flight the white flank feathers of some ioras conspicuously overlay the rump, and all except A. lafresnayei also have two white wing-bars. All chloropseids are predominantly green or green and yellow (or orange). Most male leaf birds combine intense black and glossy blue on the throat and a proportion of the males of some ioras (not A. viridissima) tend to be black rather than green above, which character often varies clinally. Black is lacking in the body plumage of most females and apart from some south-east Asian island leaf birds most chloropseids show well-marked sexual dichromatism. Juveniles resemble females, and some populations of non-forest ioras acquire a brighter breeding plumage by moult. Leafbirds superficially resemble and behave like some bulbuls, with which all chloropseids have at times been merged. A possible link with Meliphagidae has also been suggested. Distribution and habitat. The 12 species constitute 1 of only 2 bird

families endemic in the Oriental biogeographical region, chloropseids being found to its full limits. Northern congeners tend to be segregated by biotope and maximum co-occurrent diversity is reached in Sundaic dipterocarp forests where up to 5 species in both genera can be found together. Philippine congeners are allopatric by island. Only Aegithina has non-forest representatives. The familiar A. tiphia everywhere inhabits thinly wooded environments (locally also mangrove), its range being almost that of the family. In evergreen forests of the Sunda and Indochinese subregions it is replaced respectively by viridissima and the larger lafresnayei (which also occurs in the Malay Peninsula but is scarce there away from forest-edge). A close relative, nigrolutea, replaces it in the driest scrub of north-west India and Pakistan. Leafbirds are purely forest dwellers. C. aurifrons inhabits northern deciduous forest, others evergreen forest though C. cochinchinensis comes to quite open edge. The continental montane species is nearly everywhere the colourful C. hardwickii. Its place in the mountains of Sumatra is taken by an isolated form of aurifrons (possibly with the little insular endemic, venusta), and in Borneo by an upland subspecies of cochinchinensis. Movements. Non-migratory, but in its Himalayan range C. hardwickii makes seasonal shifts of altitude. Food. Ioras are mostly insectivorous. Leafbirds have mixed insect/fruit diets and some at times visit flowers, reputedly for nectar. A role in the pollination biology of certain forest trees is conceivable. The main foraging mode of both genera is leaf-searching, often acrobatic and frequently in dense foliage. Non-forest and forest-edge species hunt at all levels, forest species largely in the continuous canopy (from which A. viridissima regularly visits the crowns of tall emergents). Behaviour. Ioras and leaf birds forage alone, in pairs or small, loose groups, and in forest frequently attend mixed-species gatherings. At flowerings or fruitings in extensive forest the northern leafbirds congregate in considerable numbers but show no flock cohesion, such gatherings being strictly temporary. Voice. A. tiphia has numerous sharp or drawn-out and repeated whistles, loud and with spectacular shifts of pitch. Leafbirds have liquid, whistling songs, most sustained and melodious in C. hardwickii and C. aurifrons. Some are also considerable mimics of other birds. Breeding. Some ioras have elaborate courtship displays involving vertical leaps and parachuting flight by males. A. tiphia builds a neat compact cup of fine grass and plant fibre felted into a branch fork with cobweb. The few known leaf bird nests are loose cups of fine twigs variously mixed with grass and bryophytes, felted with cobweb and suspended by the rim from outer branchlets. A. tiphia eggs are pale pinkish with purple-brown blotches zoned in some populations round the longest circumference. Known leaf bird eggs are pale buff-cream to pinkish-white speckled, or speckled and hairlined, reddish or purple-black. Chloropseid clutches average 2 eggs, rising to 3 only in some outer tropical forms. A. tiphia fosters the cuckoo Cacomantis sonneratii (see BROOD-PARASITISM). D.R.W. Ali, S. & Ripley, S.D. 1971. Handbook of the Birds of India and Pakistan, Vol. 6. Bombay. Dunn, D.F. 1974. Zoogeography of the Irenidae (Aves: Passeres). Biotropica 6: 165-174. Medway, Lord & Wells, D.R. 1976. The Birds of the Malay Peninsula, Vol. 5. London. Smythies, B.E. 1953. The Birds of Burma (2nd edn.). Edinburgh. Smythies, B.E. 1981. The Birds of Borneo (3rd edn.). Kuala Lumpur.

LEAFLOVE: used as a substantive name for some species of Pycnonotidae (see BULBUL). LEAFSCRAPER: substantive name of Sclerurus spp. (see

(1)).

LEAF WARBLER: see

OVENBIRD

WARBLER (1).

LEAP-FROG MIGRATION: migration by a northern breeding population to winter quarters which lie further to the south than those occupied by a southern breeding population of the same species; or the corresponding return migration to the breeding quarters. LEARNING: best defined as 'the production of adaptive changes in individual behaviour as a result of experience'. There has been considerable difference of opinion as to whether the term 'adaptive' should be

Learning

included in the definition (Thorpe 1956); the word is used here to prevent the term 'learning' from including such changes in behaviour as those resulting from fatigue, sensory adaptation, and the effects of injury (surgical or otherwise). This is important, because it is generally agreed that learned behaviour is to be carefully distinguished from changes in behaviour caused by physiological or structural damage to the system. Many workers have considered that a more or less frequent repetition of a stimulus or of a changed situation is necessary for learning, but so many examples are now known of learning as a result of a single experience that this contention can no longer be maintained. There are 6 different categories of learning that are found to be useful in describing behaviour of birds and the higher vertebrates generally, one of which is discussed in a separate article (see IMPRINTING; see also BEHAVIOUR, DEVELOPMENT OF).

Habituation. This is, in some respects, the simplest type of learning found in the Animal Kingdom. It consists of 'the waning of a pre-existing response as a result of repeated stimulation when this is not followed by any kind of reward or punishment' (reinforcement). It is most evident in nature in relation to avoiding action to more generalized and simple stimuli such as loud sounds, sudden movements, any stimulus or situation that is strange, and any familiar stimulus at an unusually high intensity. Many species of birds, also, have the inborn ability to recognize, and immediately take appropriate avoiding action or other response in regard to certain types of predator, such as hawks and owls that are particularly dangerous to their species; but such an inherited response is hardly likely to have been evolved except in response to dangers that are of primary significance to the particular species. To have such an instinctive response to every kind of predator, and to every and any danger, would be out of the question. Therefore instead of, or in addition to, such specific responses, practically all animals show this ability to become habituated to stimuli that experience shows to be harmless. Obviously, if the response to such stimuli as sudden movements and sounds were completely automatic and unvarying, the life of the animal would become impossible since it would be continually taking cover from the flicker of a leaf and from every passing shadow. Habituation is thus that very simple form of learning which saves an animal from wasting its energies in response to stimuli that experience shows to be of no significance. Habituation is obviously of prime importance in the process of taming birds and other animals, constituting as it does the first step in accepting the abnormal conditions of captivity. The term 'habituation' is used in a general way for any type of response decrement shown by animals. It is, however, important to distinguish between habituation and the alternative processes, sensory adaptation and muscular fatigue. An example of how these can be distinguished refers to the withdrawal response of the marine worm Nereis pelagica. This animal, which lives in a burrow, withdraws into its home in response to a stimulus such as a shadow or a touch from a small rod, but repeated presentations of such stimulus lead to a waning of the withdrawal response. The worm's muscles are not fatigued, because a change in stimulus immediately elicits complete withdrawal. Nor have the worm's sense organs adapted to the stimulus (in much the same way as we adapt to bright light after emerging from a dark room), because the worm, even though it does not withdraw when prodded, shows other responses such as turning towards the rod. Therefore the change in the withdrawal response is due to habituation. In vertebrates, habituation is probably a result of a process in the central nervous system, although not many examples have been studied at the neurophysiological level. Associative learning. The great majority of studies of animal learning by experimental psychologists have focused on two kinds of associative learning, in which the animal learns an association between a reward or reinforcement and another event. Two main categories of associative learning are recognized. (a) Classical or Pavlovian conditioning (named after the great Russian scientist I. Pavlov) in which the animal learns an association between two stimuli. One stimulus is motivationally significant, such as the sight of food (this acts as the reinforcer) and the other is a neutral arbitrary stimulus such as light or a buzzer. In Pavlov's classic experiment a dog learned to associate the light or buzzer with food" so that eventually it would respond by salivating whenever the light or buzzer was presented. (b) Operant or instrumental conditioning, in which the animal learns an association between a reward and a response. In a typical experiment an animal has to perform a response (e.g., pecking at a key), to get a reward

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in the form of food. In both kinds of associative learning, then, the experimenter arranges a set of contingencies--in classical conditioning between a stimulus and reward, in operant conditioning between a response and reward. Adaptive value of operant and classical conditioning. The two kinds of associative learning obviously play a major adaptive role in the life of birds. The ability of birds to learn to go to good feeding sites and to stay away from places where predators are likely to attack are examples of operant conditioning. An adaptive advantage of classical conditioning is that it allows an animal to anticipate the onset of a biologically significant event: by learning to associate the start of a rain shower with the emergence of worms birds might get to the feeding site ahead of competitors. The role of associative learning can also readily be seen in the process of DEVELOPMENT OF BEHAVIOUR. For example, pecking movements of young chicks, or the ability of young Great Tits Parus major to deal with food items held under the feet are both examples of feeding skills that improve with performance. A chick's first pecks are poorly co-ordinated and inaccurate, but within a few days precision and control has improved greatly; the young Great Tit is clumsy and inept when it first handles food with its feet, but it soon learns to do the job skilfully and without errors. In these cases the process of instrumental conditioning is serving to modify the animal's natural behaviour to improve efficiency at obtaining rewards. In this kind of learning the animal gradually selects successful (in terms of reward-getting efficiency) manoeuvres and rejects less successful ones, suggesting an analogy between natural selection over many generations and learning within the lifetime of an individual. Both processes involve the selection of successful variants and discarding others. A similar point is made by K. Lorenz who has dubbed instrumental associative learning 'trial-and-success' (as opposed to the more usual term 'trial-and-error'). Although animals in the laboratory can be taught rather arbitrary responses to obtain food (e.g., raising a leg, pressing a lever, putting a coin in a slot), such instrumental conditioning proceeds more readily if there is some natural association between the response and the reinforcer. In fact what appears to be an arbitrary response to get food may be based on a natural feeding movement: rats 'pressing a bar' to get a food reward may often, on closer inspection, be gnawing at the bar as though engaged in normal appetitive behaviour for feeding. Latent learning and perceptual learning. In the types of learning so far described the performance is established or stereotyped as a result of the attainment of some kind of reward, e.g., food, drink, effective nest building, or control of flight movements. It has long been recognized that in some animals another type of learning can be discerned which is independent of reward in the ordinary, physiological sense of the term. The classical experiment is as follows: a litter of young rats is divided into two groups, one of which is placed for a period every day for 10 days in a particular maze of a particular pattern and allowed to explore this maze at random; the others are given no such experience. If, then, both groups of rats are given identical training in such a maze by being rewarded in the normal manner by finding food in the food box on completion of the run, it will be found that those rats which had had the chance to explore the maze previously (but without being rewarded in it) had, in fact, learnt a great deal about its layout and showed a striking decrease both in errors and time of running as compared with the control group. A simple maze may in this way be entirely mastered through random exploration, but this learning is latent in that it cannot be demonstrated until the introduction of a reward. Latent learning can thus be defined as 'the association of indifferent stimuli or situations (i.e. situations without reward)'. One cannot conveniently train pigeons in mazes, but there is little doubt that latent learning is a laboratory version of what is a very general feature of animals that in nature have to find their way about. There is no doubt that a great deal of the learning displayed by birds in getting to know territory, individual habitat, migration routes, and so on, resembles latent learning in that the learning achieved is not immediately rewarded in the ordinary physiological sense. Also, like latent learning, it implies a tendency to explore the environment and to learn as a result the characteristic features and their special relation to one another. Perceptual learning is essentially similar to latent learning: prior exposure to a stimulus improves later learning abilities. For example, rats reared with circles and triangles on the walls of their cages may subsequently be able to learn to discriminate these stimuli more rapidly than control animals. Perceptual learning, therefore, involves building

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up a set of descriptions of the critical features of a stimulus situation. Song learning in birds (see VOCALIZATION) and IMPRINTING are examples of perceptual learning. Insight and other complex forms of learning. There are some examples of learning which at least at first sight appear to go beyond the processes of habituation and associative learning. In the early part of this century the psychologist W. Kohler made the classic observations of insight learning in Chimpanzees Pan troglodytes. He saw that they could pile boxes on top of one another to make a 'ladder' to reach bananas hanging from the ceiling, and piece together sections of bamboo pole to make a 'rake' which they used to collect food outside their cage. According to Kohler the chimpanzees were perceiving objects in their environment in a new way-in a flash of insight the animals saw that sticks could be used as a rake, boxes as a ladder. An analogous form of learning is the ability of some animals to work out a short-cut through a maze, having been taught only a devious route. The extent to which these examples of learning should be viewed as qualitatively different from associative learning is not clear. For example, during the course of their normal play behaviour Chimpanzees will manipulate sticks and even fit them together or pile boxes up and climb on them without using the behaviours to obtain food. What Kohler saw as a flash of insight may in fact have simply been a reflection of the Chimpanzees' normal behaviour patterns. Among birds there are examples, along the same lines, of tool using in the normal process of food acquisition (see TOOLS, USE OF). Imitation is another class of learning which has sometimes been viewed as being more complex than associative learning. In birds a famous example is the ability of titmice Paridae to peck open milk-bottle tops to drink the cream. It is likely that relatively few individuals learned the trick de novo and that others acquired the novel feeding method by watching those that had already learnt it. In this way milk-bottle opening spread as a cultural behaviour tradition. The ability of birds to learn by watching others seems widespread. Experiments have shown that an individual can learn to avoid certain distasteful foods, to obtain food from a novel hiding place, and to mob an artificial 'predator' stimulus simply by observing another bird doing the same thing. It is sometimes suggested that the various learning abilities of animals can be expressed in terms of a single dimension of intelligence. However, as yet this term is not very useful to the student of animal behaviour since it is hard to define precisely and as we have seen, learning phenomena are diverse in nature. It is also becoming increasingly apparent that different species may have different specialized learning abilities to cope with their particular way of life. W.H.T. and J.R.K. Dickinson, A. 1980. Contemporary Animal Learning Theory. Cambridge. Halliday, T.R. & Slater, P.J.B. 1983. Animal Behaviour, Vol. 3. Genes, Development and Learning. Oxford. Hinde, R.A. 1954. Changes in responsiveness to a constant stimulus. Brit. J. Anim. Behav. 2: 41-55. Mackintosh, N.J. 1974. The Psychology of Animal Learning. London. Staddon, J.E.R. 1983. Adaptive Behavior and Learning. Cambridge, Mass. Thorpe, W.H. 1956. Learning and Instinct in Animals. London (2nd edn. 1963). Thorpe, W.H. 1959. Learning. Ibis 101: 337-353.

LEATHERHEAD: substantive name, alternatively 'friar-bird', of Philemon spp, (see HONEYEATER). LECTOTYPE: see TYPE

SPECIMEN.

LEG: the paired hind limb; but the term 'leg' is variously used, in different contexts, for the whole limb or for the ordinarily visible part of it and to include or exclude the 'foot', itself an inexact term for the extremity. The main components are the thigh, the lower leg (equivalent to shin), the so-called tarsus, and the toes-corresponding osteologically with the femur, the tibiotarsus plus fibula, the fused tarsometatarsus (with one free metatarsal where there are four toes), and the digit phalanges (see SKELETON, POST-CRANIAL). The joints between these components are the knee, the inter-tarsal joint or ankle, and the joints of the toes; as most birds stand on their toes, the raised ankle is often popularly mistaken for a knee (the real knee being concealed in the plumage) although it bends in the reverse direction. Birds are dependent upon their limbs for locomotion on land or on water, and there are a number of adaptations to meet these varying conditions. When the bird is standing, the leg is situated just behind the bird's centre of gravity, balance being maintained by the toes. The legs

are set farther back in swimming species; this is particularly true of the divers (Gaviidae), in which walking becomes almost impossible, so that on land they rest on their tarsi and wriggle on their stomachs--as sometimes do penguins (Spheniscidae), although these can also walk or hop in the upright position; the grebes (Podicipedidae) can run on their toes in emergency. The thigh, knee, and upper part of the lower leg are completely hidden by the flank feathers and it is only the lower part of the lower leg, the ankle joint, the tarsus, and the toes that are visible. The relative length of the limb is extremely variable. Birds that walk or run, such as the Ostrich Struthio camelus, have long legs, whereas most small birds hop and have relatively shorter legs (see LOCOMOTION, TERRESTRIAL). In passerine birds that run, e.g., larks and wagtails, the young initially hop. Similarly, wading birds, particularly flamingos and the Stilt Himantopus himantopus, have long legs and can thus go far into the water without wetting their plumage. The Secretary-bird Sagittarius serpentarius is an example of a long-legged hawk-like bird that both evades snakes and preys on them by springing in the air and killing them by striking. The shortest legs are seen in those species that seldom walk, such as the swifts and the kingfishers; but such short legs are capable of digging-the Bee-eater Merops apiaster leans on its wings while it digs with its feet. Relative strength depends upon function. Birds-of-prey possess powerful limbs for striking and holding their quarry; swimming species, particularly those that are not assisted in the water by their wings, possess massive thighs (see SWIMMING AND DIVING); whereas those that scratch the ground for food, such as the gallinaceous birds, have heavy tarsi and toes. See also CARRYING; HOLDING; PERCHING. Covering of tarsi and toes. In some birds, the tarsi and even the toes are covered with feathers or bristles. This may be protective against the cold, e.g., Pallas's Sandgrouse Syrrhaptes paradoxus, in which the feathers extend to the upper surface of the toes only, and the Ptarmigan Lagopus mutus, in which the under surface of the toes is also feathered. Feathering in other species, including the owls (Strigiformes) and the House Martin Delichon urbica, cannot be accounted for in this way. Feathering may therefore be primitive, a scaly covering being a secondary transformation of feathers. These scales may be shed annually (see MOULT), and occasional variants of the Buzzard Buteo buteo possess feathered tarsi, similar to those of the Rough-legged Buzzard Buteo lagopus. Man has produced feathered tarsi by selective breeding in domestic pigeons and fowls. The part of the limb lacking feathers is covered with a thickened, hardened structure, the podotheca. This may be corneous (horny) as in land birds or softer and more 'leathery' as in water birds. The surface may be scutellate (scaly), reticulate (covered with polygonal plates), granulate (covered with small tubercles), cancellate (covered with cross lines, as on the webs of water birds). If the podotheca is undivided or has only a few scales close to the toes, the bird is said to be 'booted' or holothecal, a condition found in most passerines (but when young these have scutellae that disappear by fusion). The young of certain Piciformes, Coraciiformes, and Trogonidae possess 'heel' pads, at the back of the intertarsal joint, that are shed when the birds leave the nest. These pads are in most cases strongly papillate, but smooth in Galbulidae. In some grouse (Tetraonidae) with unfeathered toes these are laterally pectinated (for pectinate claws see below). (See also FOOT PAPILLAE AND PADS.) Tarsal shape. In most species the tarsus is rounded in cross section, but in many swimming species it is compressed laterally to reduce water friction when the leg is brought forward, the foot folding neatly to the same shape. This is most highly developed in divers and grebes, where the tarsus resembles a knife blade. Spurs. These consist of a bony core covered with a pointed horny sheath and are situated on the posterior and inner surface of the tarsus. They are used with skill in battles that can well prove fatal, and are possessed by cock birds of polygamous species such as pheasants and peacocks and turkeys. The peacock-pheasants Polyplectron spp. have up to 4 full-sized spurs on each leg (see also COCK-FIGHTING). Number and arrangement of toes. No bird has more than 4 toes: some have only 3, the hallux having been lost (vestigial in some others), and one species has only 2, as noted below. Their arrangement depends upon function. The majority have 3 forward toes and one, the 1st toe or hallux, behind (anisodactyl). This was the position in Archaeopteryx of the Jurassic period (see ARCHAEOPTERYX). Exceptions are as follows: (a) All 4 toes may point forwards, as in the swifts. (b) The 1st toe may be capable of turning backwards or forwards, as in

Leg

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One-wattled Cassowary Casuarius unappendiculatus, may be concerned with balance when running. In the iacanas all 4 claws are long, in association with long thin toes; this remarkable adaptation enables the birds to walk over floating vegetation. In grebes the claw is flattened and is incorporated into the paddle. The herons, night jars, and pratincoles Glareola spp., have a serrated edge or 'comb' on the inner border of the 3rd claw, which, in the herons at least, has a special function in plumage-maintenance (see COMFORT BEHAVIOUR).

Fig. 1. Foot (right) of Ostrich Struthio camelus, with toes uniquely reduced to two. One-fifth natural size. (M. Yule).

the mousebirds (Coliidae); this and the preceding case have been termed the pamprodactyl foot. (c) The outer forward toe (4th) may be capable of turning backwards or forwards, as in most owls (Strigiformes) and the Osprey Pandion haliaetus. (d) The toes may be permanently in pairs, 2 in front and 2 behind-the

zygodactyl or 'yoke-toed' foot. This occurs in woodpeckers, toucans, cuckoos, parrots, and others. These have the 1st and 4th toes pointing backwards, but in the trogons it is the 1st and 2nd that do so (sometimes called 'heterodactyl'). In some Picidae, e.g. the Three-toed Woodpecker Picoides tridactylus, the 1st toe has been lost; in a few others (Campephilus etc.) the 1st and 4th toes are, during climbing, rotated into an external lateral position (ectropodactyl). (e) The 3rd and 4th toes may be partly united, with a single broad sole-the syndactyl foot of the kingfishers, hornbills, and the Cock-ofthe-rock Rupicola rupicola. In swift-running species it may be advantageous to lessen the surface of contact with the ground. Thus the 1st toe becomes raised and tends to disappear, as in some plovers (Charadriidae). The extreme is seen in the Ostrich, which has only 2 forward toes, one poorly developed and both possessing a soft elastic cushion on the sole to prevent sinking into soft sand. In sandgrouse the 3 forward toes are united by a membrane holding them close together. Claws. Claws are specialized scales, and in ptarmigan Lagopus spp. are moulted in winter. Their shape is variable; sharp, well-curved claws are used for gripping firmly and are seen in such birds as the treecreepers (Certhiidae), the Wallcreeper Tichodroma muraria, woodpeckers, and the birds-of-prey (excepting the carrion-feeding vultures (Aegypiinae) and the Honey-buzzard Pemis apivorus, in which the claws are weaker and straighter). The claws of oxpeckers Buphagus spp. are extremely sharp. Strong, blunt claws are associated with species that scratch the ground in search of food, while exceptionally long claws, such as the hind claws of some larks and pipits Anthus spp., and the long 2nd claw of the

Fig. 2. Some perching and clinging feet (right): (a) Starling Stumus vulgaris, anisodactyl; (b) Senegal Parrot Poicephalus senegalensis, zygodactyl; (c) Swift Apus apus, with all 4 toes directed forwards; (d) Kingfisher Alcedo atthis, syndactyl. Natural size. (M. Yule.)

Types of foot. Although there are many transitional forms, three main functional patterns have been evolved. 1. Perching (a) In the passerine foot all the toes are free and mobile, the hind toe being highly developed and 'opposable' to produce a firm grip. (For an exception see PARROTBILL (1).) (b) The zygodactyl foot with 2 'opposable' toes provides an even surer grip. Parrots use the foot like a hand in feeding. The 'semizygodactyl' variant, typified in Turacus fischeri, has been defined by R.E. Moreau 'as having a fourth (outside) toe that can be brought back to form an angle of about 70° with the first toe, and forward until it almost touches the third toe, but normally is held at right angles to the main axis of the foot'.

Fig. 3. Some walking and wading feet (right); (a) Lapwing Vanellus vanellus; (b) Avocet Recurvirostra avosetta, webbed; (c) Lesser Lily-trotter or jacana Microparra capensis; (d) Ptarmigan Lagopus mutus, in winter plumage with feathered toes ('snowshoes'). Two-thirds natural size. (M. Yule).

(c) In the raptorial foot the toes are widely spread and possess sharp, highly curved claws. The under surface of the toes has bulbous and roughened pads, which in the Osprey carry spines to fix the slippery fish. This type of foot has great grasping and holding powers. 2. Walking and wading. In general the foot has tended to lose its power of gripping. The hind toe may become elevated to lose contact with the ground and has become reduced in size-or it may be lost, as in the Kittiwake Rissa tridactyla. In some wading birds the toes are partially or completely webbed, for example the flamingos, storks, and avocets Recurvirostra spp.; walking over soft ground is thus facilitated, and such species can swim well on occasion. The rails have developed long toes and claws as an adaptation for walking over soft ground; this type reaches its extreme form, as already mentioned, in the jacanas, which are thus able to distribute their weight over a large surface area. The feathered foot of the Ptarmigan increases the weight-bearing surface when walking on snow in winter. The American Ruffed Grouse Bonasa umbellus in winter develops 'snow shoes' in the form of a row of scales along each side of the toes. 3. Swimming. Many unrelated birds such as the petrels, gulls, auks, ducks and geese, have developed along similar lines to transform the foot into a paddle.

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developed, and unmodified except in diving ducks, in which it is lobulate. The Hawaiian Goose Branta sandvicensis possesses a partially palmate foot and is an example of a goose that has reverted to a more terrestrial life. In the totipalmate variation characteristic of the Pelecaniformes, all 4 toes are webbed to provide the perfect swimming foot, the outer toe being the longest and the hind toe pointing slightly forward. Unfeathered legs and feet, particularly webbed feet, are a potential source of heat loss. Irvine and Krog have shown in gulls Larus spp., however, that there is not only a reduced blood flow at low external temperatures but also some kind of vascular heat exchange, so that blood flowing into the unfeathered part of the leg does so at a very low temperature. This can be appreciated by feeling the cold web of any water bird. Serious heat loss is thus eliminated; and, in extremes, loss can be further reduced if the bird sits on its legs, covering them with its feathers (see also HEAT REGULATION). Abnormalities. Supernumerary limbs and toes occur as genetic variants (except in domestication, the Dorking Fowl possessing a constant supernumerary toe on each foot). Very rarely a toe may be missing due to a congenital defect; frequently the toes are crooked, in association with inbreeding. Survival has been recorded in a wild Pheasant Phasianus colchicus after both feet had been accidentally amputated through the tarsi. Partial or total loss of one or both feet is not uncommon in water or wading birds and there is evidence that this is caused by fishes and molluscs. Loss of toes in a Moorhen Gallinula chloropus has followed a tuberculous arthritis. Normal embryonic development may be altered by radiation or drug administration. J.G.H.

Fig. 4. Some swimming feet (right): (a) Coot Fulica atra, lobate; (b) Mallard Anas platyrhynchos, palmate; (c) Cormorant Phalacrocorax carbo, totipalmate. Half natural size. (M. Yule).

Beebe, C.W. 1907. The Bird-Its Form and Function. New York. Bock, W.J. & Miller, W.D. 1959. The scansorial foot of the woodpeckers, with comments on the evolution of perching and climbing feet in birds. Amer. Mus. Novit. no. 1931: 1-45. Goslow, G.E. 1972. Adaptive mechanisms of the raptor pelvic limb. Auk 89: 47-64. Thomson, J.A. 1923. The Biology of Birds. London.

LEITLINIE: original German term, best translated as 'leading line'

(see In the lobate variation, each toe carries independent webs, examples being the coots Fulica spp., phalaropes, the grebes, and the three remarkably grebe-like species of finfoot, thought to be of gruiform affinity. In grebes, the tibiotarsus is held in extreme external rotation when the bird is swimming; the foot is pale on its inner surface and dark on its outer surface, so that, as the latter is uppermost in swimming, the normal countershading is maintained. In the palmate variation the 3 forward toes are united by a web, typical examples being the gulls, petrels, and ducks. The hind toe is free, poorly

Fig. 5. Foot (right) of Golden Eagle Aquila chrysaetos, adapted for grasping. Half natural size. eM. Yule).

MIGRATION).

LEK: a communal display ground (sometimes called 'arena') where males congregate for the sole purpose of attracting and courting females and to which females come for mating. The term is sometimes applied to the group of males congregating at such an area, and seems to be derived from Swedish 'leka', 'to play', which can have a sexual connotation. In resident species leks are usually traditional, their location remaining unaltered year after year; but in some migratory species the position of leks may change yearly, and even within seasons. Lek displays constitute one of several categories of polygynous mating systems (see MATING SYSTEM; POLYGYNY), their most important distinguishing feature being that the males do not defend any resource needed by the female (nest-site or food) but compete directly among themselves for the attention of females, those of the highest status doing most of the mating. It is the rule for each male to occupy and defend his own display area (a cleared or trampled area, usually known as a 'court' if it is on the ground, or a special perch or group of perches if it is in a tree) within the lek. Mating normally takes place at the lek, on the successful male's court or display perch, after a stereotyped display sequence. Detailed studies of lek displays have shown that some males, usually those whose courts are centrally placed within the lek, attract most females and do most of the mating, while peripheral males are relatively or completely unsuccessful. It is assumed that even peripheral males nevertheless have a better chance of mating than they would have if they attempted to court females away from the lek, and that this is so for two reasons. First, because the males stimulate and enhance each other's displays, a group of n males will be more than n times as effective in attracting females as a single male displaying alone, and secondly, peripheral males have a chance to succeed to central positions in a lek when these fall vacant. Evidence for the first of these assumptions, which are crucial to explaining the evolution of lek displays, is very difficult to obtain; but there is a considerable amount of evidence that peripheral males in a lek take every opportunity to claim more central positions and regularly succeed in doing so. It is not always possible to draw a clear distinction between true leks (in the sense used above) and those in which males display in a looser

Lek

group within a circumscribed area , often out of sight but within earshot of one another. The term 'dispersed lek' or 'expl oded lek' has been used for such cases. In some species the spatial organization of displaying males probably varies according to population den sity. Closely related species within the same genu s (e.g. manakins of the genus Pipra) may show example s of different degrees of spacing. In many species with lek displays the inten se inter-male competition has led to the evolution of striking male ornamentation; display postures and movements are typically both striking and highl y stereotyped. In some groups of lek birds, however , most notabl y the hermit hummingbird s, male and female differ hardly at all in plumage. It is noteworthy that the most refined elaborations of plumage , as in the Great Argus Pheasant Argusianus argus, Peacock P avo cristatus and Lyrebird Menura novaehollandia e, are found in species in which the males display solitarily or in 'd ispers ed leks' . There is generall y a clear distin ction between displays which serve to attract females from a distance (loud calls, and very striking visual displays , especially flight displays) and those that presumably stimulate females at close quarters (the more elaborate and refined, often static, visual displays). Lek displays, being performed by birds belonging to several different families in which monogamy is probably the primitive condition, exemplify evolutionary convergence in behaviour. An important predisposing

Male Ruffs Ph ilomachus pugnax displaying and fightingat a lek with (lower photo) females, 'reeves', in attendance. (P hotos: A . C hristiansen).

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cond ition is that the male is eman cipated from nest-attendance and parental care. This probably explain s why lek displays have evolved only in birds with precocial young and, among bird s with altricial young, only in some fruit-eating, nectar-eating and seed-eating groups (for further explanation, see MATING SYSTEM). The following is a systematic summary of the main known cases of lek behaviour. Game-birds. The grouse family (Tetraonidae) includes several species with highly developed lek displays , the Black Grouse Tetrao tetrix and Sage Grouse Centtocercus urophasianus being well-studied example s. True lek displays apparently do not occur in the largest of the game-bird families, the Phasianidae, but males of the Great Argus and some other species occupy isolated display areas within earshot but not within sight of one another ('dispersed leks' ). Bustards, The Great Bustard Otis tarda has a lek display ; in other species, so far as known, the males display solitarily . Waders. The Ruff Philomachus pugnax is one of the most outstanding and best known of lek birds. Ruffs arc unique in having highly polymorphic male display plumage, no two individuals being exactly alike . There are two main types of male : independent males, with mainly dark display plumage, which occupy and defend courts within the display grounds (known, in this species , as 'hills '); and satellite males, with largely white display plumage, which lack aggressive behaviour and are tolerated at the courts of the independent males. The Ruff is exceptional among lek birds in being silent at the 'hill' , but the courts may be only c. 0.5 m from each other, the area is open and frequented year after year , and conspicuousness is increased by corporate flights . Two other waders, the Buff-breasted Sandpiper Ttyngites subruficollis and the Great Snipe Gallinago media , have lek displa ys. Unlike the Ruff, they show little sexual dimorphism in plumage. The display of the Great Snipe, which takes place mostly at night , is accompanied by loud vocalization s; the Buff-breasted Sandpiper's displays are made conspicuous by showing off the satin-white underside of the raised wings. Parrots. It is reliably reported that the little-known, and gravely endangered, Kakapo or Owl Parrot Stngops habroptilus of New Zealand is a lek species . The males congregate in restricted display areas, where each bird adverti ses itself with a booming call. Hummingbirds. Many , perhaps all, of the hermit hummingbirds of the genu s Phaethomis displa y in leks. They are dull-coloured for hummingbirds, and the sexes are nearl y or quite alike in plumage. Th e males advertise themselves on their display perches by constant singing; displays directed toward s intruding males and females are similar , mating being elicited bf appropriate behaviour on the part of receptive females. Singing assemblies of some other tropi cal hummingbirds, which may qualify as leks, nave been less studied . It seems that the evolution of lek behaviour in the hermit hummingbirds is connected with the fact that they are 'trap-lining' hummingbirds and do not defend their nectar sources (see HUMMtNGBtRD). A 'resource-based' mating system, such as is found in some other hummingbirds, is therefore not possible, and males establish their status by direct competitive interaction. Manakins (Pipridae). This Neotropical family of small forest-living bird s contains a number of species with highly developed lek displays , notably the White-bearded Manakin Manacus manacus (and its ncar relatives), several species of Pipra , and the 4 species of Chiroxiphia . Manacus species display on cleared courts on the forest floor, Pipra species on perches in under-storey trees , and Chiroxiphia on low, more or less horizontal vines and other stems within a few metres of the ground. The displa y behaviour of Chiroxiphia is unique in that 2, or in one species 3, males take part in a perfe ctly coordinated joint dance in front of a female but only one, apparently the dominant male of the group , mates with her . In one closely related group of P ipra species , including the Wire-tailed Manakin P . filicauda , the owning (or dominant) male on a display perch is regularly joined by a visiting (or subordinate) male in the absence of a female, and the two birds carry out an elaborate series of coordinated displa y flights and other movements . Cotingas. This family, closely related to the manakins but containing mainly larger forest bird s and , like the manakins, largely frugivor ous, contains many species with extravagantly ornamented males which have elaborate displays, but only a few of them are known to display at leks, most notably the 2 cocks-of-the-rock Rupicola spp . Several species, including the bellbirds Procnias, have dispersed leks. The Screaming Piha Lipaugus vociferans parallels the hermit hummingbirds in that the sexes are alike and dull-coloured, and the males advertise them selves by per sistent calling from their display perches within a well-defined lek.

328 Lens

LEY DIG CELLS : see ENDOCRINOLOGY AND THE REPROD UCTIVE SYSTEM.

L ICE : see ECTOPARASITE . LIF E , EXPECTAT ION O F: see AGE. LIFE Z ONE : an area defined , for ecological purposes, in term s of temperature and humidity rather than of nature of ground and vegetation (cont rast BlOME ) . L I G AM E N T : band of connective tissue , tough and flexible, uniting two bone s (see SKELETON , POST-CRANIAL) or supporting an organ . LIGHT : considered as an environmental factor-see PHOTOPERIODISM ; also under BREEDING SEASON; MIGRATION ; NOCTURNAL HABITS; RHYTHMS AND TIME MEASUREMENT ; ROOSTING; VISION .

L IL Y-TRO TTER : substantive name most commonly used for African species of jacanidae (see JACANA) . LIME, BIRD : a viscous substance (made from holly bark , etc .) used for smearing on twigs or other perches in order to catch small bird s. The term is sometimes popularly misapplied to the residual excrement adhering to trees , rocks, buildings, and the like much frequented by bird s. L I MICOL AE : formerl y used as th e nam e of an order equivalent to the suborder Charadrii of the Charadriiformes (see also LARO-LIMICOLAE) .

Jackson's Whydah Euple ctes jacksoni male displaying at a lek, showing developmentof 'ornamental' features often found in birds with this type of behaviour. (p hoto: ] .F. R eynolds). Weavers. Among weavers , Jack son 's Wh ydah Euplectes ja cksoni is unique in having a lek displa y, the females nesting away from the display area (not within the male' s displa y territory , as in the typical polygynou s weavers). Birds -of-paradise. Several of the bird s-of-paradise, notab ly the species of Paradisaea, display at leks ; in others the males have a system of disper sed leks or disp lay solitarily. In all these, the males are extravagantly ornamented. Other species are monogamous, and show much less sexual dimorphism. As in the manakins and cotinga s, the evolution of lek display s seems to be related to frugivory. D .W .S. (1) Bradbury, J.W. 1981. Evolution of leks. In Alexander, R.D. & Tinkle, D. (eds.). Natural Selection of Social Behavior: 138-169. New York. Hogan-Warburg, A.J. 1966. Social behavior of the Ruff, Ph ilamachus pugnax (L. ). Ardea 54: 109-229. Kruiit, J.P. & Hogan, I.A. 1967. Social behavior on the lek in the Black Grouse, Lyrurus tetnx tetnx (L. ). Ardea 55: 203--240. Lemmell, P.A. 1978. Social behaviour of the Great Snipe Capella media at the arena display. am. Scand. 9: 146-163 . Lill, A. 1974. Sexual behavior of the lek-forrning White-bearded Manakin (M anacus manacus trinitatis Hartert), Z. Tierpsychol. 36: 1-36. Snow, B.K. & Snow, D.W. 1979. The Ochre-bellied Flycatcher and the evolution of lek behavior. Condor 81: 286-292. Snow, D.W. 198 1. The Cotingas. London. Stiles, F.G. & Wolf, L.L. 1979. Ecology and evolution of lek mating in the Long-tailed Hermit Hummingbird. am. Monogr. (A.O.V.), no. 27. Wiley, R.H. 1978. The lek mating system of the Sage Grouse. Sci. American 238: 114-125 .

L E NS : part of the eye (see VISION). LEPTO S OMATIDAE: see CORACII FORMES; CUCKOO-ROLLER. L ESS ER COVERTS: see TOPOGRAPHY . LEUCISM: see PLUMAGE , ABNORMAL. L E U COCYTE : see BLOOD.

Limpkin Aramus guarauna. (C .] .F. C .). LIMPKIN: A ramus guarauna , sole species in the New World family Aramidae (Gruiform es, suborder Grues ). It has certain osteological and pterylographical characters that are crane-like (i.e. as in Gruidae) and a digestive system like that of the rails . Cha ra cteristics. In general appearance the Limpkin is like a very large rail (length 58-71 em). The sexes are similar in size and appearance. The bill is long, laterall y compressed, and slightly decurved. The neck is long and slender; the wings are very broad and rounded; the tail is short and broad; the legs are long , with tibia e partly bare . The general coloration is glossy brownish olive, quite finely streaked with white on the neck and with broader broken streaks on the body. Fledged young closely resemble adults, but have shorter bills. Ne stlings are dark brownish, evenly coloured. The feet are not webbed, but it is an efficient swimmer. It is seldom seen in flight. It stands on the ground or perches at any heigh t, including the tops of tall trees . H ab ita t. Although it is a wading bird , usually occurring in wooded

Locomotion, terrestrial

swamps or shaded places where there is a lush growth of woody or herbaceous vegetation, it has been found in areas of arid brush in the West Indies. Distribution and movements. The Limpkin is a sedentary species. It occurs from Georgia and Florida through Central America and on various islands, south in South America east of the Andes to central Argentina. Four subspecies are recognized. Food. The Limpkin feeds almost exclusively on large snails, mainly Pomacea ('Ampullaria'), obtained in water of wading depth. The bird walks ashore or to very shallow water with its prey, extracts the snail, and discards the undamaged shell; a perching place is sometimes littered with these. Behaviour. Although, where not protected, it is considered to be crepuscular and nocturnal in its habits, it is notably unwary and diurnal (as well as nocturnal) at certain localities in Florida where it is responding to full protection. Voice. The Limpkin is best known for its voice and is often called 'wailing bird' or 'crying bird'. Its varied wailing, screaming, and assorted clucking notes are heard most frequently at night. Breeding. Relatively little is known about its breeding habits. The rather flimsy shallow nest, of sticks and dry vegetation, is built in a shaded spot on the ground near water or even as high as a few metres up in a bush or tree. The 4-8 eggs are pale buff, spotted or blotched with various light browns. Incubation is by the sexes in turn for an unknown period. Both parents tend the precocial young for an unknown length of time. Either the nesting season (in Florida) is very prolonged or else the species is double-brooded. The young out of the nest, even for some weeks after they have attained flight, approach from behind and reach forward between a parent's legs for food; the snail (in shell) is taken from the bill of the parent and swallowed whole. R.S.P.

329

LOBATE; LOBED: having the toes separately fringed by lobes, as distinct from webs connecting the toes (see LEG). LOCAL ENHANCEMENT: see FACILITATION,

SOCIAL.

LOCOMOTION, TERRESTRIAL: birds use three gaits, the walk and run in which the feet move alternately and the hop in which they move together. In walking, each foot is on the ground for more than half the stride so there are times when both are on the ground. In running, each foot is on the ground for less than half the stride so there are times when both are off the ground. Gait and energy cost. Turkeys, ducks, rheas and probably many other birds use the gait known as the stiff walk, which is also used by man. In it, energy is saved by the principle of the pendulum. The potential energy of a pendulum increases and decreases as the bob rises and falls, and its kinetic energy increases and decreases as the bob accelerates and decelerates. Very little work is needed to keep the pendulum swinging because kinetic energy increases as potential energy decreases and vice versa: energy is shuttled back and forth between the two forms. In the stiff walk, the leg is kept rather stiff while the foot is on the ground so the bird's centre of mass rises as it goes from position (a) to position (b) (Fig. 1). At the same time the force exerted by the ground on the foot, acting along the leg, slows the bird down a little. Thus potential energy increases and kinetic energy decreases as the bird goes from (a) to (b). The reverse changes occur between (b) and (c). There is a maximum speed which depends on the length of the leg, above which it is impossible to make the potential energy changes compensate for the kinetic energy changes, and the stiff walk loses its advantage. The Wild Turkey Meleagris gallopavo uses the stiff walk at speeds below 1.5 mls but runs to go faster.

Nesbitt, S.A. et al. 1976. Capturing and banding Limpkins in Florida. Bird Banding 47(2): 164-165. Snyder, N. & H. 1969. A comparative study of mollusc predation by Limpkins, Everglade Kites and Boat-tailed Grackles. Living Bird 8: 177-223.

LINCOLN INDEX: the formula of a sampling method used in population studies (and see PREDATION), viz.:

MxS Population = - m where 'M' is the number of marked animals released in a given area; 'S' is the number of animals captured in a sample taken after the dispersal of the marked animals from the release point; and 'm' is the number of marked animals in the sample S.

Fig. 1. Successive positions of a bird performing the stiff walk. The broken line represents the path of the centre of mass.

Lincoln, F.C. 1930. Calculating waterfowl abundance on the basis of banding returns. Circ. U.S. Dept. Agric. no. 118: 1-4.

LINE TRANSECT: see CENSUS. LINKAGE: see GENETICS. LINNET: Carduelis cannabina (see FINCH). LIOCICHLA: substantive name sometimes used for laughing thrushes of the genus Liocichla (for family see BABBLER). LIVER: a large unpaired organ associated with the digestive tract (see ALIMENTARY SYSTEM). In addition to secreting bile into the duodenum by way of the hepatic duct or ducts (gall-bladder present or absent), it is the site of important metabolic changes in substances brought to it by the portal vessels (see VASCULAR SYSTEM) and also to some extent a storage depot, e.g., of glycogen (see METABOLISM). LIVER (with long 'i' as in 'diver'): name derived from that of the city of Liverpool and applied since the 17th century to a bird imaginatively portrayed in the municipal coat-of-arms, originally intended to be the eagle of St John the Ecclesiastic but now changed out of recognition (see, in general, HERALDIC BIRDS). LLANO: an environment of savanna type characteristic of parts of tropical South America (see SAVANNA). LOAFING: see ROOSTING.

Fig. 2. Successive positions of a running bird. The broken line represents the path of the centre of mass.

In running, energy may be saved by the principle of the bouncing ball. The centre of mass is lowest when the bird is moving most slowly (Fig. 2b) so kinetic and potential energy have their lowest values at the same time. However, the force on the foot is largest at this time and tendons in the leg are stretched, storing elastic strain energy. Kinetic and potential energy are converted to elastic strain energy between (a) and (b), and restored by elastic recoil between (b) and (c). This mechanism is most effective at high speeds, when the feet are on the ground for only a small fraction of the stride and the forces on them are correspondingly large. Calculations based on films and dissections seem to show that tendon elasticity saves a lot of energy in the fast running of Ostriches Struthio camelus, but it is not certain that it is important in smaller birds. It may also save energy in hopping. Most small passerines and some other birds hop. Most of those that do are small or arboreal in habits or both. Hopping seems a particularly

330 Locomotion, terrestrial

Sanderling Calidris alba in winter plumage, running. (P hoto: J .B. & S.

Large Pied Wagtail Motacilla maderaspatensis walking. (P hoto: T . Shiota ).

Bottomley) ,

Rook Corvus frugilegus walking. (P hoto: H .E. Grenf ell ).

Lesser Yellowlegs Tringa flavip es wading. (P hoto: ].B. & S. Bottomley).

useful gait in tree s where supports for the feet are sparse (in comparison with solid ground) but where the feet can always be placed side-by-s ide on the branch . Some families (for instance, the Corvidae) include species which hop and others which walk or run . Some species (for instance the Blackbird and American Robin , both species of Turdus) sometimes hop and sometimes run . The Magpie Pica pica walks to travel slowly and hop s to go faster , but its hop is a peculiar asymmetrical gait with the left and right feet out of phase . Vultures use a similar asymmetrical hop. Birds have been trained to run on a conveyor belt, so that they remain stationary while the belt moves under them . This technique has made it possible to measure the rate at which they use oxygen as they run , and so to estimate their energ y consumption. Ostriches use oxygen at about the same rate as ponies of the same weight , running at the same speed. Similarly roadrunners Geococcyx use oxygen at about the same rate as ground squirrels of similar weight at the same speed . However, bird s whose style of walking looks clums y (for instance, geese and penguins) use oxygen up to three times as fast as more graceful species of similar weight at the same speed . Ostriches seem to run a little faster than typical antelopes but most birds are slow runners, compared to mammals of similar size. Ostriches have a much larger proportion of leg muscle in the body than flying bird s. Measurements of oxygen consumption of kangaroo s have shown that their hopping uses more energy than the running gaits of other mammals of similar size, except at high speeds . Measurements on smaller hopping mammals (for instance, kangaroo rat s) show that they use oxygen about as fast as similar-sized running mammals, at all speeds. There is no evidence that hopping can give any energetic advantage, for any size of mammal, and no measurements seem to have been made on birds. Penguins slide down slopes on their bellies and presumably save energy that way, but this technique of locomotion seems not to have been closely studied. The mechanics of wading have also been neglected by zoologists .

Balance. The hips of birds are far posterior to the centre of mass of the body, but standing and walking without overbalancing are only possible if the average position of the feet is directly below the centre of mass. Most birds stand and walk with the thigh s nearly horizontal, so that the knees are alongside the centre of mass. They move their thighs only a little as they walk or run, and swing the legs mainly from the knees . Penguins and auks have thigh s too short for this, and bring the centre of mass over the feet by standing with the trunk erect. Head bobbing. A bobbing movement of the head is characteristic of the gaits of many birds, including pigeon s. The head moves backwards and forwards relative to the body in every step. There is a stage in the step when the head is moving backwards relative to the body and is more or less stationary relative to the ground. It is believed that having the head even briefly stationary relativ e to the surroundings may make it easier for the bird to detect moving object s visually . In support of thi s idea , pigeon s do not bob their head s when walking on a conveyor belt so as to be stationary relative to their surroundings. R.McN .A. Alexander, R.McN. & Goldspink, G. (eds.). 1977. Mechanics and Energetics of Animal Locomotion. London. Alexander, R.McN., Maloiy, G.M.O., Njau , R. & Jayes, A.S. 1979. Mechanics of running of the ostrich (S muhio camelus). J. Zoo!. , Lond. 187: 169-178. Cavagna, G.A., Heglund, N.C. & Taylor, C.R. 1977. Mechanical work in terrestrial locomotion: twobasicmechanisms for minimizingenergyexpenditure. Am. J. Physio!. 233: R243--R261. Dagg, A.!. 1977. The walkof the Silver Gull (L arus nuvaehollandiae) and of other birds. J. Zoo!., Lond. 182: 529-540. Fedak, M.A. & Seeherman, H.J. 1979. Reappraisal of energetics of locomotion shows identical cost in bipeds and quadrupeds including ostrich and horse. Nature, Lond. 282: 713-6 . Frost, B.J. 1978. The optokinetic basisof head-bobbing in the pigeon. J. expoBio!. 74: 187-195.

Lymphatic system

LOCUS: of a gene (plural 'loci')-see

particular species within range; also a form of bait used by falconers to recover their charges (see FALCONRY).

GENETICS.

LOCUST-BIRD: name applied in parts of Africa to various species of birds that congregate to feed on locust swarms, e.g. the Black-winged Pratincole Glareola nordmanni as an off-season visitor to South Africa. LOGGERHEAD: name applied in the Falkland Islands to steamer ducks Tachyeres spp.; and in North America to the Loggerhead Shrike Lanius ludovicianus.

LOGRUNNER: substantive name of Orthonyx spp. (see

RAIL-

BABBLER).

LONGBILL: substantive name of the 2 New Guinea the genus Toxorhamphus.

HONEYEATERS

LONGCLAW: substantive name of Macronyx spp. (see under

of

WAG-

TAIL).

LONGEVITY: see

AGE.

LONGSPUR: substantive name, in North America, of Calcarius spp., including the Lapland Bunting C. lapponicus (see BUNTING). LONGTAIL: substantive name of Urolais epichlora, and an alternative substantive name for prinias Prinia spp. (see WARBLER (1)). LOOMERY: term which has been applied to breeding colonies of guillemots (Uria)-see AUK. LOON: substantive name used in North America for all the species of Gaviidae (see DIVER). LOOP MIGRATION: see

MIGRATION.

LORE: the area between the base of the upper mandible and the eye, on each side (plural 'lores'; adjective 'loral')-see TOPOGRAPHY. LORICULINAE: see LORIINAE: see

PARROT.

PARROT.

LORIKEET: substantive name used sometimes for the smaller species of lories (Loriinae) (see PARROT). LORY: substantive name of the species of the Loriinae; in the plural (lories), general term for the subfamily (see PARROT). LOTUS-BIRD: name in Australia for Irediparra gallinacea (see JACANA).

LOURIE: alternative substantive name of some species of Musophagidae (see TURACO). LOUSE-FLIES: see

ECTOPARASITE.

LOVEBIRD: substantive name of the African Agapomis spp. (Psittacinae, Psittaculini); sometimes applied to the Budgerigar Melopsittacus undulatus (Psittacinae, Platycercini) (see PARROT). LOWAN: name, alternatively 'Mallee Fowl', of Leipoa ocellata (see MEGAPODE).

LUMPER: a taxonomist who prefers a nomenclature that recognizes broad groupings, and hence emphasizes relationships-in contrast to a SPLITTER, who prefers a nomenclature that recognizes fine distinctions. Workers interested primarily in wider evolutionary problems tend to be lumpers, while specialists in narrower fields of research tend to be splitters; but this distinction should not be pushed too far. LUNG: see

331

RESPIRATORY SYSTEM.

LURE: instrument used in imitating bird-calls to attract birds of the

LUTEIN: a yellow, fat-soluble, carotenoid pigment (C4oHs602) found in many plant and animal materials; for example, in yolk of eggs, fat cells, corpus luteum, and feathers. LYMPHATIC SYSTEM: much of the fluid part of blood, with its protein, that escapes from the blood capillaries into the tissue spaces is retrieved by lymphatic capillaries, collected in lymphatic vessels and ultimately returned to the venous system. Thus the lymphatic vessels function in the maintenance of the fluid balance of the body. Throughout the body are accumulations of lymphoid tissue, the cells of which provide immunity to antigens such as microorganisms, toxins, foreign cells and tissues. Embryologically, lymphoid tissue and lymphatic vessels originate independently. Lymphatic vessels. The lymphatic capillaries are blind endothelial tubules forming plexuses which drain into collecting vessels that are tributaries of the main transporting lymphatic vessels. Lymphatic vessels accompany blood vessels, usually veins. Generally the lymphatics are paired and flank their veins. Most of the lymph flow of the body converges on the 'venous angles' at the confluence of the jugular and subclavian veins where the major transporting trunks (thoracoabdominal, jugular, and subclavian) empty individually, their orifices guarded by valves. Dual thoracoabdominal trunks (thoracic ducts) are tightly applied to each side of the descending aorta, and communicate extensively with one another. The jugular trunks, usually two on each side, descend the neck adherent to the jugular veins. Lymph is propelled by compression of the vessels brought about by muscle contraction and body movements, backflow prevented by the valves interspersed along the vessels. In most mature birds lymph hearts are absent. A pair of contractile hearts have been reported in some ratites, anseriforms, storks, and grebes, located in the pelvic region. In birds lymph vessels, especially cutaneous vessels, and their valves are more sparse than in mammals. Most of the lymph is produced by the alimentary canal and the liver. Lymphoid tissue. Most of the lymphoid tissue is found in the wall of the alimentary canal, cloacal bursa, thymus, spleen as well as in numerous small nodules and foci scattered throughout many organs and tissues, including the lymphatic vessels themselves. The lymphoidtissue is in the form of solitary or aggregated nodules, consisting largely of lymphocytes and organized into diffuse masses with germinal centres. Birds generally lack lymph nodes which function as filters of lymph. Avian lymph nodes somewhat resembling those of mammals are reported to occur in adults of some anseriforms, the Coot Fulica atra and the Herring Gull Larus argentatus. In these forms only 4 nodes are present: a pair of cervicothoracic nodes located on the jugular lymphatic trunks and a pair of lumbar nodes located on the thoracoabdominal trunks in the pelvic region. The avian node is a fusiform structure grafted on to the vessel with an irregular central sinus, a central zone of lymphoid tissue, and a peripheral meshwork of reticular fibres into which the sinus spaces open, allowing some filtration of the lymph. The main sinus space is central rather than peripheral as in mammalian nodes. Accumulations of lymphoid tissue occur abundantly on the lymphatic vessels of all species examined so far. These are the mural lymphoid nodules which are embedded in one side of the vessel, protruding into the lumen. Nodules apparently have no filtration capacity. Birds, especially the chicken, have been important research subjects in the elucidation of much basic information on adaptive immunity since it was discovered that the cloacal bursa possesses an immunological function. The bursa and the thymus are intimately connected with the development of immunity. In the early life of these organs are found the primary sources of immunologically competent cells which are seeded to other connective and epithelial tissues, where they form secondary centres of lymphoid tissue. The bursa and thymus programme the cells, which are sent elsewhere to proliferate and respond to antigens. The cloacal bursa (of Fabricius) is unique to birds. A diverticulum of the proctodeal part of the cloaca, it rests on the dorsal wall of the cloaca. Th~ bursa has a central space; its walls contain numerous lobules (follicles) of lymphoid tissue. The bursa begins to regress with onset of sexual maturity, diminishing in size and undergoing fibrosis. The bursa-dependent line of cells is represented morphologically by larger lymphocytes of the germinal centres and by plasma cells. These cells bear

332 Lyrebird

surface immunoglobulins which appear to function as antibody receptors for various antigens. The thymus consists of a series of lobes stretched out along each jugular vein. Each lobe contains lobules of lymphoid tissue which also regress at onset of sexual maturity. The thymus-dependent line of cells is represented morphologically by the smaller lymphocytes of the circulation and the diffuse type of lymphoid tissue. These cells which carry no antibodies on their surfaces are concerned with the development of cellular immunity such as graft-versus-host, homograft, and delayed hypersensitivity reactions. The spleen is a small, brownish-red organ located near the junction of proventriculus and gizzard. The spleen of birds has little or no function as a blood reservoir. It produces red blood cells only in foetal life and lymphocytes throughout adult life. As a lymphoid organ the spleen contains both thymus-dependent (diffuse) lymphocytes and bursa-dependent (germinal centres and plasma cells) lymphocytes in the white pulp and loose lymphocytes in the red pulp. The main functions of the adult spleen are destruction of red blood cells in the red pulp, production of lymphocytes in the white pulp, and uptake of antigens and antibody production by lymphocytes in both types of splenic pulp. J.J.B. King, A.S. 1975. Aves. Lymphatic System. In Getty, R. (ed.). Sisson and Grossman's The Anatomy of the Domestic Animals. Vol. 2. 5th ed. Philadelphia. Payne, L. N. 1971. The Lymphoid System. In Bell, D.}. & Freeman, B.M. (eds.). Physiology and Biochemistry of the Domestic Fowl. Vol. 2. London.

L YREBIRD: name applied to the 2 species of Menuridae (Passeriformes, suborder Oscines). The name stems from the supposed close resemblance of the male Superb Lyrebird's tail to a Greek lyre. Lyrebirds rank among the largest passerines and are renowned for their spectacular courtship display and vocal mimicry. The origin, affinities and even the specific name of one of the species are controversial. On the basis of their simple syringeal musculature, the aberrant lyrebirds and their distant relatives the SCRUB-BIRDS, Atrichornithidae, have long been considered suboscine and grouped together in the suborder Menurae. Lyrebirds and scrub-birds have 3 pairs of intrinsic syringeal muscles whereas the suborder Oscines usually have 4. This suboscine classification has naturally led some authors (e.g. Cracraft 1973) to propose a southern, Gondwanaland origin for the Menurae, even though most of the extant Australian avifauna, except possibly the ratites, is probably of northern origin. Recently, C.G. Sibley proposed on the basis of a review of anatomical and egg white protein comparisons that lyrebirds and scrub-birds are oscine and allied to the bird-of-paradise-bowerbird assemblage. He advocates dropping the suborder Menurae and placing lyrebirds and scrub-birds next to Ptilonorhynchidae in Passeres. He thus considers lyrebirds part of the 'corvine assemblage' and probably of Asian origin. While the morphology of the stapes (see SKULL) also supports the affinities with the oscines (Feduccia 1975), the alleged close relationship with bowerbirds and birds-of-paradise is not reflected in the appendicular myology (Raikow 1978). Nonetheless a more distant sister-group relationship with this assemblage remains possible. Characteristics. Lyrebirds have weak powers of flight but run swiftly. Flying is limited to downhill gliding and short, clumsy flights of a few metres between tree branches. Despite this, they roost high in the forest canopy (especially males), ascending by jumping from branch to branch and gliding. They are very 'shy' and difficult to approach and observe. The Superb Lyrebird Menura novaehollandiae is mainly dark brown dorsally and grey-brown ventrally. The Albert Lyrebird Menura alberti is more rufous-brown above and has rufous rather than grey undertail coverts. Both species have long legs and large feet equipped with big claws, and are sexually dimorphic in size and tail plumage. Male Superb Lyrebirds (80-90 em long) have highly modified rectrices comprising 2 outer lyrates, 2 medians and 12 filamentaries. The lyrates are's'-shaped with one vane greatly reduced; their upper surfaces are dark brown edged with black, their under surfaces white (except in the race edwardi).

The broad vane has a black tip and many transparent notches edged with rufous on the underside. The medians have very narrow vanes, while the filamentaries, black above and white below, have widely spaced distal barbs which lack barbules. The smaller female has unspecialized rectrices, except for the outermost 2 which have transparent notches like male lyrates. Male Albert Lyrebirds also have unspecialized lyrates but their tails are otherwise like those of male Superb Lyrebirds. Distribution and habitat. Lyrebirds are endemic to Australia and

Superb Lyrebird Menura novaehollandiae. (N. w.e.).

restricted to the mountains and foothills of the south-eastern seaboard. The Superb Lyrebird ranges from southern Victoria to south-eastern Queensland, inhabiting mainly wet sclerophyll eucalypt forest and temperate rainforest dominated by beeches N othofagus. However, it also occurs in sub-tropical rainforest and the edwardi race is restricted to drier, open forest in the granite country of southern Queensland. The Albert Lyrebird has a much more restricted range, occurring only in subtropical rainforests in a narrow belt in north-eastern New South Wales and southern Queensland. In 1934 the Superb Lyrebird was introduced to Tasmania where it now has a restricted range in wet sclerophyll and temperate rainforest. Food. Lyrebirds eat mainly soil-dwelling invertebrates which they expose by digging with powerful feet capable of removing large obstructions such as stones and roots with comparative ease. In southern Victoria, Superb Lyrebirds typically catch about 13-17 prey per minute of foraging and dig to a maximum depth of approximately 12em. Invertebrates living in fallen, rotting logs are also secured by ripping away the covering bark and outer layers with the claws. The adult diet has not been quantitatively documented, but widely overlaps that of the nestling whose principal foods are earthworms, amphipods, spiders, millipedes, centipedes, isopods and fly and beetle larvae. Superb Lyrebirds regularly drink from streams and surface pools. Behaviour and mating system. Both lyrebird species probably exhibit sexual bimaturism (deferred male maturity). Male Superb Lyrebirds gradually acquire adult-type rectrices from age 2-5, 6 or 7 years. They frequently associate in pairs or trios characterized by much mutual aggression and display during their early development. Shortly before or when the full adult tail has developed, they become territorial and begin to show courtship behaviour; females are thought to commence breeding at a much earlier age. Adult males occupy marginally overlapping territories averaging 2.5-3.5 ha throughout the year and defend them by displaying, chasing and singing. In southern Victoria, males are fairly evenly dispersed throughout suitable habitat. However, they often have a

preferred singing area within the territory, and since those of some neighbours are commonly adjacent across a shared boundary, temporary clustering sometimes occurs during display and countersinging. Lyrebirds exhibit arena behaviour. Male Superb Lyrebirds clear and maintain many earth mounds 1-1.5 m in diameter on their territories and spend up to 50% of daylight singing and displaying on them, as well as on the ground, on fallen trunks and in trees, during the mating season. Male Albert Lyrebirds display on well-concealed platforms of criss-crossing

Lyrebird

vines and/or fallen branches on scratched ground (Curtis 1972). Copulation is probably largely restricted to the mounds and platforms. Male Superb Lyrebirds are polygamous, probably promiscuous, and take no part in caring for the young (see POLYGAMY). In southern Victoria, 2-3 female breeding territories lie within or partially overlap each male territory and some females visit more than one displaying male immediately prior to laying. Heterosexual association between adults is limited and typically brief (LiB 1979a), so that pair-bonding seems to be absent. However, some hens have been recorded copulating with the same male in successive seasons (see Reilly 1970 and Kenyon 1972 for other interpretations of the parental care and mating systems). Voice. The territorial song of the Superb Lyrebird contains a loud, species-typical component lasting about 5-6 s, audible from 1km under minimal wind conditions and exhibiting marked local dialects. But up to 800/0 of territorial song is composed of extended bouts of mimicry of the vocalizations of a wide range of co-habiting bird species (see MIMICRY, VOCAL). There is some evidence that these are learned in part from conspecifics rather than the models themselves. The mimicked sounds include the antiphonal duetting of whip birds Psophodes, kookaburras Dacelo and magpies Gymnorhina and the wing-beats and calls of flying flocks of Rosella parrots. A quieter type of singing occurs during close pursuit and courtship of hens away from the mounds. This often contains mimicked bird calls rarely heard in territorial song, as well as mimicry of dogs barking and, reputedly, occasionally sounds made by inanimate objects. Females can produce full territorial song including mimicry but do so infrequently. Superb Lyrebirds also give 3 distinct species-typical calls during courtship display and emit loud whistles when alarmed. The Albert Lyrebird also has a loud territorial song and a softer courtship song, but its mimicry is restricted largely to only 4 or 5 avian models (Smith 1976). Display. In full courtship display, the singing male Superb Lyrebird holds the rectrices horizontally over the back so that they form a fan spread over and in front of the bird. The white undersurfaces of the lyrates and filamentaries are thus strikingly exposed. When a female visits the mound, however, the rectrices are held forward but close together and rapidly quivered. Courtship climaxes in rapid circling and jumping displays. Away from the mounds and main display area, courtship involves quiet song, wing-lowering and tail-shaking. The display of the male Albert Lyrebird has been less well described but is broadly similar. Breeding. Both species commence breeding in winter. The nest of the Superb Lyrebird is a large chamber with a side entrance and averages 14kg. The base and sides are built of sticks, the interstices being packed with moss and bark strips. The chamber is lined and roofed with fine rootlets and sometimes a little green vegetation is placed on the roof. Immediately before laying, some body feathers are added to the chamber floor. Nests are constructed from ground level to 22 m, the preferred range being up to 2 m. The principal nest sites are on earth banks and rock faces, in trees and grass and sedge clumps, and on boulders. Nestbuilding is usually protracted over several months (Reilly 1970, Lill 1980).

333

The clutch-size is one and re-Iaying is uncommon. The egg is grey with dark brown markings and averages 62 g when fresh. The full incubation rhythm takes up to 18 days to develop and even then daytime attentiveness averages only 45%. Throughout incubation the egg is continuously deserted for 3-6 hours each morning, during which time embryonic temperature falls to and remains at the prevailing ambient level of less than 10°C and development is presumably interrupted. Consequently the incubation period is unusually long, averaging 50 days (Lill 1979b). The newly-hatched chick with its incomplete dorsal cover of black down is brooded for a gradually diminishing percentage of daylight hours until it is effectively homeothermic at about 10 days old. However, it also chills appreciably during maternal absences in the first few days after hatching. In the post-brooding stage, the nestling is fed about 3 times per hour, the mother storing collected food in a gular sac. During the 47-day nestling period the chick's weight increases roughly 12-fold to an average fledging weight which is 63% of adult female body weight. Available nesting success estimates vary widely from 11-20% to 65-790/0 and introduced mammals and native birds have been implicated as the major nest predators (LiB 1980). Fledglings leave the nest in October and November and accompany and are partly fed by the mother for up to 8 months. Although the breeding biology of the Albert Lyrebird is less well known, the main features are similar. Lyrebirds were slaughtered in great numbers in the 19th century for their tail plumage. Nowadays both species have protected status and are quite common in suitable habitat. The impact of introduced predators on recruitment is difficult to assess; probably the main threat to lyrebirds' survival is continuing large-scale clearance of wet forests for commercial purposes. A.L. Cracraft, 1. 1973. Continental drift, paleoclimatology, and the evolution and biogeography of birds. 1. Zoo!' Lond. 169: 455-545. Curtis, H.S. 1972. The Albert Lyrebird in display. Emu 72: 81-84. Feduccia, A. 1975. Morphology of the bony stapes in the Menuridae and Acanthisittidae; evidence for oscine affinities. Wilson Bull. 87: 418-420. Kenyon, R.F. 1972. Polygyny among Superb Lyrebirds in Sherbrooke Forest Park, Kallista, Victoria. Emu 72: 70-76. Lill, A. 1979a. An assessment of male parental investment and pair bonding in the polygamous Superb Lyrebird. Auk 96: 489-498. Lill, A. 1979b. Nest inattentiveness and its influence on development of the young in the Superb Lyrebird. Condor 81: 225-231. Lill, A. 1980. Reproductive success and nest predation in the Superb Lyrebird, Menura superba. Aust. Wildt. Res. 7: 271-280. Raikow, R.J. 1978. The appendicular myology and its taxonomic significance in the passerine suborder Menurae. Amer. Zoot. 18: 377. Reilly, P.N. 1970. Nesting of the Superb Lyrebird in Sherbrooke Forest, Victoria. Emu 70: 73-78. Robinson, F.N. 1975. Vocal mimicry and the evolution of bird song. Emu 75: 23-27. Robinson, F.N. & Frith, HiI. 1981. The Superb LyrebirdMenura nouaehollandiae at Tidbinbilla. ACT. Emu 81: 145-157. Smith, G.T. 1976. Ecological and behavioural comparisons between the Atrichornithidae and Menuridae. Proc. XVI Int. Orne Congo 1974: 125-136.

male has a white nape and rump, which are variably greyish in the slightly smaller female. The males of the White-backed G. t. hypoleuca and Western G. t. dorsalis are pure white-backed and the females are mottled grey-backed, darker in dorsalis. In first-year birds the pied effect is reduced by grey or buff fringes to all the feathers; this varies in degree so that some individuals are much lighter and others darker than average. Most second-year plumages resemble the adult, but some lighter individuals are difficult to distinguish from darker one-year-olds. The bill of first-year birds is dark and the pale bluish base develops in the second year until only a dark tip remains in the fully adult bird. The Western Magpie is longer-billed than the others. Habitat. The preferred habitat is open savanna woodland, with pasture for feeding and trees for nesting, roosting and shelter. Australian magpies are most abundant, and prominent visually and vocally, in settled areas, rural and urban. Distribution. The Black-backed Magpie occurs throughout New South Wales (except the southern border) and Queensland, becoming sparse across the north into Western Australia and southern New Guinea. The White-backed Magpie covers Tasmania, South Australia into the centre of the continent, Victoria and across its northern border into New South Wales, with further penetration and increasing scarcity northward along the Great Dividing Range and Pacific coast, finally petering out in south-eastern Queensland. Black-backed and White-backed forms interbreed, producing plumage intergrades which breed successfully. The White-backed Magpie is well established by introduction to both islands of New Zealand, where variable dark-backed birds also occur. The Western Magpie is confined to the south of Western Australia. Food. Magpies are versatile ground feeders, taking mainly beetles and other insects, earthworms, ants and spiders, and a few frogs and lizards; they hawk for adult scarabs and grasshoppers in season, and survive on grain during frost and drought. Voice and behaviour. The loud melodious carolling throughout the year, with social groups calling in antiphonal chorus between neighbouring territories, especially at dawn, is one of the most popular Australian bird sounds. The birds often become quite tame, and the adult male can be embarrassingly aggressive to humans near the nest. By contrast, in the outback they are shy and distant. The habitat is divided into permanent territories of about 8 ha strongly held all year by small social groups of Black-backed and White-backed Magpies; larger groups of Western Magpies hold larger areas. In the first two, non-territorial and therefore non-breeding birds form loose flocks, which feed in open treeless pasture by day and roost in denser woodland up to several km distant; in Western Magpies, all birds are in territorial groups. Top-quality habitat contains all requirements for survival and breeding within each territory, often in excess of needs; it is held most strongly and permanently, and birds so ensconced never leave their territory so long as the group remains intact to defend it. At all seasons there is intense competition by groups and individuals to improve their habitat and social status; groups pre-formed in the flock continually seek entry to breeding habitat, and familiarity with the voices of neighbouring birds enables vacancies to be exploited at once. In dry country, where food may be less abundant or seasonally unreliable, territories are enormous. Breeding. In treeless country, magpies nest on telegraph poles, low bushes, and even the ground. The nest of twigs lined with grass or wool contains 3-5 mottled eggs during July to October, and is usually obvious in the outer canopy of a gum tree. The hen does all the building and incubation, and often alone rears the nestlings for 4 weeks, while their plaintive insistent food-begging calls can be heard for another 2 months or more. The males police the territory, and the females assist to repel invaders of their own sex. Polygamy is common, and a sex hierarchy of dominance within the group leads to subordinate hens breeding later or not at all. In exceptional cases, where older hens are unusually tolerant or the younger ones can escape their attention, one-year-old females have bred, but most are 2 or 3 years old at first breeding. They are single-brooded and productivity is low; only 1 young for every 2 adult hens in permanent territories survives to independence, and none at all in poorer territories. A detailed large-scale study of individually-marked Black-backed Magpies during 1955-1966 (Carrick 1972) showed that social groups of 2-10 birds consisted mainly of monogamous and bigamous adults plus immatures, but all ratios up to 3 adults of each sex occurred. Territory boundaries and size remain fairly constant despite wide fluctuations in the number of occupants. Individual advancement

MACAW: substantive name of the Neotropical Ara spp. and Anodorhynchus spp. (Psittacinae, Arini). (see PARROT). MACHAERAMPHINAE: see

HAWK.

MACHAIR: florally rich turf on leeward side of dunes on north-west Scottish coast and especially in the Hebridean islands. MACROCHIRES: name formerly used for the order

APODIFORMES;

SW"IFT.

MACROSMATIC: having a highly developed olfactory sense (see SMELL).

MADAGASCAR: see

MALAGASY REGION.

MAGELLANIC PLOVER: Pluvianellus socialis, sole member of the Pluvianellidae (Charadriiformes, suborder Charadrii). Characteristics. The superficially dove-like Magellanic Plover is a small grey wader, c. 20 em long, with a white belly. It has a short straight bill, stout legs and feet, and a bright coral red iris. Though formerly classified with the plovers (Charadriidae), its closest relatives are the sheathbills (Chionididae). Habitat and distribution. It breeds along gravel shores of small fresh-water ponds in Patagonia and northern Tierra del Fuego, and winters in sheltered bays and estuaries on the coast of Argentina north to Chubut Province. During the breeding season it is sparsely distributed and the entire population may not exceed several hundred individuals. Food. Magellanic Plovers feed exclusively on invertebrates which they obtain by walking slowly along the shore or upper beach and pecking at the surface. In a unique behaviour, they also stand in one spot and spin, phalarope-like, using their feet to excavate shallow holes in areas of rotting vegetation where fly larvae are common. Breeding. During the breeding season, they are invariably found in pairs, whereas in winter they form small flocks and often associate with Two-banded Plovers (Charadrius falklandicus) and other waders. Although at least 10 distinct vocalizations have been documented, the birds are quiet and inconspicuous at all seasons. Nesting begins in September. Linear territories are established along the lake shore and are defended in a complicated display involving both members of the pair. The clutch consists of 2 relatively small unspotted eggs, laid in a nest-scrape lined with a few pebbles and incubated by both parents. Apparently only one chick is raised. Both parents feed the chick by regurgitation. The chick grows slowly and makes its first flight at 28 days of age. It remains with the parents, and is still being fed by them, at least until day 40. See photo INCUBATION. J.R.J.Jr. jehl, J.R., Jr. 1975. Pluvianellus socialis: biology, ecology, and relationships of an enigmatic Patagonian shorebird. San Diego. Soc. Nat. Hist., Transactions, 18(3): 35-74.

MAGNETIC SENSE: see

NAVIGATION.

MAGPIE (1): substantive name of the two species in several genera of Corvidae; used without qualification, in Britain, for Pica pica (the 'Black-billed Magpie' of North America)-see CROW (1). MAGPIE (2): substantive name of the two Gymnorhina spp. in the family Cracticidae (Passeriformes, suborder Oscines). Characteristics. These similar crow-like birds of upright stance, about 25 em high, have boldly pied plumage, with black underparts, wings (with white flashes) and head; the tail is white with a terminal black band. In the Black-backed Magpie Gymnorhina tibicen the back is black and the 334

Malagasy region

335

takes precedence over group loyalty. Birds established in good territories are long-lived, and the main mortality occurs in the slightly nomadic flocks. Australian magpies are aggressive capitalists, and very sedentary birds indeed; even non-breeding individuals move only a few km throughout life. R.C. (1) Carrick, R. 1972. Population ecology of the Australian Black-backed Magpie, Royal Penguin, and Silver Gull. Population Ecology of Migratory Birds: A Symposium. U.S. Dept. Interior: Wildlife Research Report 2: 41-99. Robinson, A. 1956. The annual reproductory cycle of the Magpie, Gymnorhina dorsalis Campbell, in south-western Australia. Emu 56: 235-336.

MAGPIE-LARK: substantive name of Grallina cyanoleuca, one of the 2 species in the family Grallinidae (Passeriformes, suborder Oscines), the other being the Torrentlark G. bruijni of New Guinea (see Schodde 1975 and CHOUGH (2)). Alternative English names for the group are 'mudlark' and 'mud nest-builders'. Characteristics. The Australian Magpie-lark, 26-30 em long, is a medium-sized boldly pied bird, showing conspicuous sexual dimorphism in head and throat patterning. The relatively long legs are black, the beak and iris creamy white. The male's crown and throat are black, with white eyebrow and cheek patches. The female's crown and breast are black, but a black vertical stripe runs through the eye and joins them; forehead, throat and sides of the head are white. Juveniles have the black forehead and white eyebrow of the male and the white throat and chin of the female. They moult into adult plumage after about 3 months. Distribution and habitat. Widespread throughout mainland Australia, but rare in Tasmania. It prefers open areas such as water margins, open woodland and cleared paddocks and rarely penetrates closed forest or dense scrub. Agricultural development, with the provision of water in dams and bores, has led to considerable extension of the bird's original range. Its wide distribution, conspicuousness and the readiness with which it has adapted to city suburbs have made it among the best known Australian birds. Food. Magpie-larks are ground-feeders, their varied diet consisting mainly of insects, but also spiders, pond snails, small frogs and seeds. Behaviour. Adult Magpie-larks live in monogamous pairs in allpurpose territories of 4-8 ha. Both partners actively defend the territory and share nesting duties. The pair-bond and territory probably endure for the lifespan of the birds. Aggression is mostly confined to encounters between birds of the same sex, and is most intense against single intruders. This suggests that year-round territoriality not only protects resources but, with the persistent pair-bond, has adaptive advantage for a species so dependent on rainfall for opportunistic breeding. Unlike the adults, young birds are relatively wide-ranging. After leaving the parental territory at about 3 months old, they join local flocks of their peers, moult into adult plumage, develop song and eventually form pairs. These leave the flock, which may number from 50--3,000 individuals, at the start of the next breeding season, and set up their own territories. Ringing studies have shown that adults are sedentary and that flocks are mainly composed of first-year birds. Voice. Magpie-larks communicate through a large and varied repertoire of strident calls, often accompanied by striking displays. These are used for communicating with the mate, while a few universal calls are reserved for contact with the young, with rivals or to warn of predators. The most interesting feature of the vocal behaviour is antiphonal singing in exact alternation. This helps to keep the partners together and the territory intact. Breeding. The local distribution of the Magpie-lark is related to the availability of fresh surface water, since breeding depends on a source of mud for nest-building. A typical bowl-shaped mud nest was 15em across, 9 em deep, with walls 2 em thick and weighed 950 g (Serventy and Whittell 1967). Nests are built far out on bare horizontal branches often over water. Wads of grass are collected with the mud to strengthen the construction and the finished nest is lined with dry grass, feathers or wool. Clutch-size ranges from 1-4, commonly 3 eggs, white with violet or purplish brown blotches. Breeding takes place during the wet season (summer in the north, winter in the south and at variable times inland) and its success seems to depend upon an adequate spell of favourable rainfall conditions. Breeding may be stopped or interrupted in dry or unusually wet years, but birds will rear 2, or rarely 3, broods if the wet season is consistent and long-lasting. Also, rainfall outside the normal nesting season can stimulate successful breeding (Serventy and Marshall 1957). Both parents incubate and tend the young, which are downy when

Magpie-lark Grallina cyanoleuca, juvenile (top), adult female and male (bottom). (N. w.e.).

hatched and fledge in c. 20 days. Torrentlark. The Torrentlark has a pied plumage like the Magpie-lark and also shows marked sexual dimorphism. The legs are blackish, the iris dark brown and the bill greyish white. The male has a black face, chin, throat and upper abdomen, with a white superciliary stripe. The female is distinguished by her white forehead and breast and a more pronounced eyebrow. The Torrentlark is restricted to montane habitats where it feeds on insects along fast-flowing streams. The cup-shaped nest is made of mud and rootlets. Little is known of the species' biology and behaviour. (A.K.) S.T. Robinson, A. 1947. Magpie-larks: a study in behaviour. Emu 46: 265-281, 382-391; 47: 11-28, 147-153. Schodde, R. 1975. Interim List of Australian Songbirds, Passerines. Melbourne. Serventy, D.L. & Marshall, A.J. 1957. Breeding periodicity in Western Australian birds: with an account of un seasonal nesting in 1953 and 1955. Emu 57: 99-126. Serventy, D.L. & Whittell, H.M. 1967. Birds of Western Australia. Perth. Tingay, S. 1974. Antiphonal song of the Magpie-Lark. Emu 74: 11-17. Tingay, S. 1981. The social behaviour and vocalizations of Australian Magpie Larks (Grallina cyanoleuca) in south-western Australia. Ph.D. thesis, Univ. of W. Australia.

MAGPIE-ROBIN: substantive name of Copsychus spp. (see THRUSH). MAINTENANCE ACTIVITY: see

COMFORT BEHAVIOUR.

MAJOR MITCHELL: the Australian cockatoo Cacatua leadbeateri, formerly known as Leadbeater's Cockatoo (see PARROT). MALACONOTINAE: see

SHRIKE.

MALAGASH: alternative name of the Cape Gannet Sula capensis (see GANNET).

MALAGASY REGION: the faunal region formed by Madagascar (adjective Malagasy) and outlying islands, east to the Mascarenes, north to the granitic Seychelles. Although Madagascar, the putative main source of the avifauna of the outlying islands, is separated from Africa at the nearest point by only some 400 km, its fauna is so unique that it is now widely accepted as distinct from the AFROTROPICAL REGION. Madagascar was probably separated from Africa in the late Cretaceous. If the

336 Malagasy region

fossil remains found in Africa are correctly attributed to the Aepyornithidae, which is questionable (see ELEPHANT-BIRD; FOSSIL BIRDS), it would follow that their dispersal to Madagascar pre-dated this separation. Most of the remainder of the avifauna may have arrived later by flying and, as might be expected, has an African origin. Nevertheless, there is a distinct Asian element, including 3 genera unknown in Africa, viz. Ninox, Hypsipetes (=Ixos) and Copsychus. Apart from the Aepyornithidae, which may have survived until 400 years ago, there are 3 families endemic to Madagascar, the Mesitornithidae (3 species in 2 genera), Brachypteraciidae (5 species in 3 genera) and the suboscine Philepittidae (4 species in 2 genera): see MESITE, GROUND- ROLLER and ASITY. The Leptosomatidae (1 species) are only otherwise known from the Comoros: see CUCKOO-ROLLER. The Vangidae (14 species in 11 genera, including the Coral-billed Nuthatch Hypositta corallirostris, formerly placed in its own family, the Hyposittidae) are only represented outside Madagascar by one of these species in the Comoros: see VANGA. Of the c. 180 breeding land birds (including 2 only discovered since 1970), 67% are endemic, even 94% in the passerines. Specific differentiation is so marked that the genera average less than 1.3 species each (in passerines as low as 1.1 as against 3.5 for the Afrotropical Region). Nevertheless, there is striking evidence of evolutionary radiation in the Vangidae and in the endemic genus Coua (see CUCKOO), with 10 species. Ecological diversity is strongly marked. Eastern Madagascar is very wet (rainfall per annum up to 350 em in the north-east); the original vegetation dense evergreen forest, much of it cleared for cultivation, but perhaps 3,000 km 2 still standing. A spine of highlands runs down the middle, mostly at 1,600 m, but rising in places to c. 3,000 m. This area, where habitat destruction has been worst, has largely degenerated into eroded grassland. The much drier west consists of more or less wooded savannas, with subdesert scrub in the south-west (rainfall less than 50 em per annum). While some species range practically throughout (but often showing well-marked subspecific differentiation), others are very restricted. Thus, of the 10 Coua spp., 4 are only known from evergreen forest, one from subdesert scrub. A figure of 180 breeding land birds is small in comparison to the Afrotropical Region. The comparable figure for Zambia exceeds 600. The water birds make up 30%, as against 16% Afrotropical (some not even subspecifically distinguishable between the two regions, but 1 in 3 in the former is endemic). Yet the Malagasy passerines account for 340/0 only, as against 48%. They are deficient in fruit eaters---only 1 starling (Sturnidae) and 1 bulbul (Pycnonotidae, but 6 others possibly wholly insectivorous)---and in seed-eaters, 1 lark (Alaudidae), 4 weavers (Ploceidae) and 1 mannikin (Estrildidae). According to Cheke (1985), the volcanic Mascarenes developed a highly endemic and bizarre avifauna in the absence of any native mammalian ground predators. The Dodo and solitaires (see DODO), and the large rails Aphanapteryx spp. were flightless. There were also several endemic genera of parrots and starlings, and endemic species of ducks, raptors, pigeons, owls, swifts, and at least 8 families of passerines. The introduction of rats, monkeys, pigs, cats and other animals by man took their toll of the flightless birds soon after the islands were discovered and settled (16th and 17th centuries), and hunting followed by extensive habitat destruction has left only 16 survivors from the 40-45 known endemic species. The affinities of the Mascarene avifauna are with Madagascar and Asia, a pattern also shown by the native bats and reptiles. The 4 Comoro Islands, also volcanic (Grand Comoro, still active, rising to 2,560 m), have an avifauna predominantly Malagasy, but with some Afrotropical transitional elements. The number of species of land birds (excluding water birds, few in number) is c. 30 per island. Endemism is considerable (1 genus, c. 8 species). North-eastward, towards the granitic Seychelles, there are many low-lying islets, some important for breeding sea birds, but few with more than 2 species of land bird. By far the largest and least disturbed is the elevated limestone atoll of Aldabra, rising 10m above sea level, and 36km long. The number of species of land (excluding water) birds attains the relatively high figure of 12, including 2 endemics, while even among the 7 water birds there are 2 endemic subspecies (6 among the land birds), one of the 2 being a flightless form of rail. The Aldabra avifauna is predominantly Malagasy-derived. The Seychelles, possibly a continental relic, are nevertheless oceanic from the ornithological aspect. At the height of a glacial epoch c. 18,000 years ago, with sea levels c. 150m lower than now, they would have

formed a single land mass. There were at least 14 species of land bird, and 4 water birds (3 herons, Moorhen Gallinula chloropus) still breed. Endemic, very well marked, subspecies of parakeet Psittacula eupatria and white-eye Zosterops mayottensis apparently became extinct in the 1890s. Several of the 12 surviving land birds, under special protection, are on the upgrade from near extinction. There is no endemic genus, but 7 endemic species. As to be expected, the Asian element is more pronounced than in Madagascar and the Comoros. C.W.B. Benson, C.W., Colebrook-Robjent, J.F.R. & Williams, A. 1976-1977. Contribution a l'ornithologie de Madagascar. L'Oiseau & R.F.O. 46: 103-134, 209-242, 367-386. 47: 41-64, 167-191. Cheke, A.S. 1985. An ecological history of the Mascarene Islands, with particular reference to extinctions and introductions of land vertebrates. In Diamond, A.W. (ed.). Studies of Mascarene Island Birds. Cambridge. Cracraft, J. 1974. Phylogeny and evolution of the ratite birds. Ibis 116: 494-521. Dorst, J. 1972. The evolution and affinities of the birds of Madagascar. In Biogeography and Ecology in Madagascar. The Hague. Hachisuka, M. 1953. The Dodo and Kindred Birds, or the Extinct Birds of the Mascarene Islands. London. Keith, G.S. 1980. Origins of the avifauna of the Malagasy Region. Proc. IV Pan-Afro Orn. Congr. Pp. 99-108. Milon, Ph., Petter, J.-J. & Randrianasolo, G. 1973. Faune de Madagascar, 35, Oiseaux. Tananarive, Paris. Staub, J.J.F. 1976. Birds of the Mascarenes and Saint Brandon. Port Louis, Mauritius. Stoddart, D.R. (ed.) In press. Biogeography and Ecology of the Seychelles Islands. The Hague.

MALAR: pertaining to the area on the side of the throat immediately below the base of the lower mandible (see

TOPOGRAPHY).

MALEO: Dutch name (sometimes used as English) in Indonesia for Megacephalon maleo (see MEGAPODE). MALIA: Malia grata, an endemic

BABBLER

of Celebes (Sulawezi).

MALIMBE: sometimes used as substantive name of certain Malimbus

spp. (see

WEAVER).

MALKOHA: substantive name of Rhopodytes spp. (see CUCKOO). MALLARD: Anas platyrhynchos, the common 'wild duck', but originally applied only to the male (a usage now obsolete)---see DUCK. MALLEE: an environment, consisting of Eucalyptus scrub, characteristic of Australia.

MALLEE FOWL: name, alternatively 'Lewan', of Leipoa ocellata (see MEGAPODE).

MALPIGHIAN BODY: see EXCRETORY

SYSTEM.

MALPIGHIAN LAYER: the basal layer of the epidermis (see SKIN). MALURIDAE: family of PASSERIFORMES, suborder Oscines;

WREN (2).

MAMMALS, ASSOCIATION WITH: occurs as a regular habit of

various avian species, chiefly in relation to the quest for food (see FEEDING The most frequent role of mammals, wild or domesticated, is that of a beater, disturbing insects or other prey for birds, as they move through the herbage or foliage. Cattle Egrets Bubulcus ibis find food more rapidly when they are associated with mammals than when they hunt alone. Similar associations are shown by such familiar birds as the Starling Stumus vulgaris associating with cattle in Europe, or by the Piapiac Philostomus afer with domestic stock and wild grazing mammals in tropical Africa; its habit of perching on the Elephant Loxodonta africana is well known, and most remarkable, because elephants do not tolerate the attentions of oxpeckers Buphagus spp. Examples of such associations between birds and mammals of many species, in various parts of the world, are too numerous to cite at length. Often, the attendant bird will perch on the mammal. Aquatic and wading birds of many species habitually perch on the backs of an almost submerged Hippopotamus Hippopotamus amphibius: cormorants (Phalacrocorax sp.) are characteristic in this role. Sometimes the animal provides the bird with a vantage point for fishing, as in the case of HABITS).

Manakin

Great Tit P arus major attacking field M .S. Wood ).

mouse A podemus. (P hoto:

Hamerkop S copus umbrella on the lookout for frogs; in other instances , it may be no more than a convenient resting place. Sometime s bird s find some part of the ir food on the beast itself, as the Common Sandpiper Actitis hypol eucos on the hipp o's hide . The 2 oxpeckers have a closer , rather symbiotic, relation with the mammals that they frequent , feeding upon the ticks in the hide (see OXPE CKER ) . Another special case is the strange association on the part of HONEYGUIDES (Indicatoridae) with Ratels Mellivora capensis and man . In tropical forests, association of mixed bird partie s with squirrels is frequent, sometimes to mob a snake or an owl, more often to catch the insects which the mammal flushes out of the foliage. The same type of association exists with duikers C ep halop hus and various rodents. The most remarkable case is the constant association of the Hornbill Tropicranus albocristatus with Cercopithecus monkey s in tropical Africa. Tropicranus apparently possesses anatomical and behavioural adaptations which have evolved in connection with its constant association with monkey s. Nesting associations with mammal s are rare. The only perfect case seems to be that the Miner Geositta cunicularia of South Ameri ca, which nests only in the burrow of the Vizcacha Lagostromus trichodactylus. All associations between birds and mammals are initiated by the bird s, and are for the ir own benefit. Ne verthele ss, in some cases, the presence of the bird s obviously favours the security of th e mammal s; for example , at the approach of a potential enem y, the roving troop of C ercopithecus is alerted by a special call of Trop icranus, which is followed by modification in th e behaviour of the monkeys. A.B. For associations with mankind , see also TAMENESS. MAMMAL SIMULATION: also 'rode nt run ' (see

DISTRACTIO N

BEHAVIOUR) .

MAN AKIN: substantive name of species of Pipridae (Passeriformes, infraorder Tyranni}-not to be confused with MANNIKI N ; in the plural , general term for the family. This Neotropical group of some 50 species is allied to the cotingas (Cotingidae) and, less closely, to the tyrantflycatchers (T yrannidae).

337

White Wagtail M otacilla alba and pig. (P hoto: F . PO/king). Characteristics. Manakins are small, stocky bird s the size of tit s (Paridae) 9-15 em long , usually with short wings and tail , and with short bills rather broad at the base and slightly hooked at the tip . In most species the sexes are strik ingly different , the males being predominantly black with patches of brilliant red , orange, blue and other colours, and the females greenish. In several specie s the males have some of the flight feathers modified for making mechanical sounds . In one species, the Wire-tailed Manakin Pipra fili cauda, the tail feathers are prolonged into curved wire-like structures. In a few species, supposed to be primitive, the sexes are alike and mainly green or brown . It is, however , doubtful whether some of these , for example the Thrush-like Manakin S chiffornis turdinus, are really closely related to the typical manakins. Habitat and distribution. Manakins are distributed throughout the lowland forests of South and Central America ; few of them extend up into subtropical montane forest s. Most are bird s of primary forest , but some species are regular in secondary growth. They feed mainly on small fruits which the y pluck on the wing ; insects are also taken in small quantities by the adults , and form a major part of the food of the young. As far as known , all species are sedentary. Behaviour. Manakins are especially notable for their elaborate courtship behaviour, which appears to have evolved under conditi ons of intense sexual selection . They are polygynous, the males taking no part in attending the nest. In the White-bearded Manakin Manacus mana cus (a member of a widely distributed assemblage of forms, including Gould 's Manakin which is sometimes treated as a separate species, M . vi tellinus), the males display in LEKS. Each clears for itself a small 'court' on the floor of the forest , taking away all leaves and twigs that are small enough to be carried , and dropping them a few metres away. Each court contains a vertical sapling that serves as the main display perch , and one or more other sapling s. On and around his court the male execute s astonishing jumps and evolutions of a highly stereotyped nature . Variou s loud snapping and whirring noises are made with the wing feather s, the secondaries having much thickened shafts and a special musculature, while the outer primaries are thin, stiff and curved. The females visit the males at their courts and take part in a joint dance with them . Mating in

338 Manakin

White-bearded Manakin Manacus manacus. (R.G.).

this genus, as in the other species studied, takes place on the main display perch. Several Pipra species that have been studied display on horizontal perches between about 2 and 15 m up in trees or saplings, below the main forest canopy. Their displays consist of various elements: a swift flight to the perch from a distance, often accompanied by vocal or mechanical sounds; 'sliding' movements along the perch (in fact, very short and rapid steps); raising of the wings and spreading of the tail; rapid about-turns on the perch; and quick to-and-fro flights between the main perch and an adjacent perch, accompanied by mechanical wing-noises. Some Pipra species, e.g., the Golden-headed Manakin P. erythrocephala, display in typical leks, while in others the males are dispersed more widely, within sound but not in sight of one another. In a group of 3 closely related species that includes the Wire-tailed Manakin, the owner of a display perch is regularly joined by a visiting, or subordinate, male, and the two perform beautifully coordinated joint displays. The Wiretailed Manakin has a unique display that makes use of its modified tail: the male faces away from his display partner, elevates his tail, and with a rapid twisting movement of his body brushes the other bird's throat with the wire-like tips of his tail-feathers. This display is little used in the joint displays of males (mentioned above), but is the main element of the male's display to a female. The displays of several species are remarkable, but little known. In 2 species of M achaeropterus the male hangs head downwards on a vertical perch and rapidly turns the body from side to side while making a grasshopper-like reeling sound. It is noteworthy that, in Machaeropterus and some other species, observers have found it extremely difficult to determine whether certain sounds accompanying the displays are vocal or mechanical in origin. In Corapipo gutturalis the male is described as crouching on the ground and, with wings fully spread, moving towards the female in a laboured undulating crawl, an action strikingly like that described for the bowerbird Archboldia sanfordi (see BOWERBIRD). The 4 species of Chiroxiphia have perhaps the most remarkable behaviour in that 2, or in C. caudata 3, males take equal parts in various joint displays that serve to attract and stimulate the female, after which one male only (apparently always the dominant male of the group) takes part in the final phase of courtship and copulation. The most striking of the joint displays is a 'catherine wheel' dance. When a female comes to the display perch the males face her; the front bird then jumps up and, hovering, moves backwards through the air while the other (in C. caudata, the next) bird hops up into his place and in his turn jumps as the first bird lands. The dance is accompanied by a rhythmic twanging, consisting of alternating calls uttered by each bird as it hovers. Breeding. Except for Schiffomis, which builds a bulky cup nest composed chiefly of leaves (and may not be at all closely related to the typical manakins), all manakins whose nests are known build thinly woven cup nests slung in a horizontal fork of a tree branch, sapling or fern, at heights ranging from less than a metre to as much as 15 m above the ground. The clutch normally consists of 2 eggs. The eggs are pale grey, brown or beige in ground colour, mottled and spotted with darker brown. Recorded incubation periods are mostly 17-19 days, and fledging periods 13-15 days. The female alone builds, incubates, and cares for the young. D.W.S. (1)

Foster, M.S. 1976. Nesting biology of the Long-tailed Manakin. Wilson Bull. 88: 400-420. Foster, M.S. 1977. Odd couples in manakins: a study of social organization and cooperative breeding in Chiroxiphia linearis. Am. Nat. Ill: 845-853. Lill, A. 1974. Sexual behavior in the lek-forming White-bearded Manakin (M. manacus trinitatis Hartert). Z. Tierpsychol. 36: 1-36. LilI, A. 1976. Lek behavior in the Golden-headed Manakin, Pipra erythrocephala in Trinidad (West Indies). Z. Tierpsychol., Beiheft 18. Schwartz, P. & Snow, D.W. 1979. Display and related behavior of the Wire-tailed Manakin. Living Bird 17: 51-78. Sick, H. 1967. Courtship behavior in manakins (Pipridae): a review. Living Bird 6: 5-22. Skutch, A.F. 1969. Life histories of Central American birds III. Pacific Coast Avifauna no. 35 (Cooper Ornithological Society). Snow, D.W. 1963. The evolution of manakin displays. Proc. XIII Int. Orn. Congr.: 553--561. Snow, D.W. 1976. The Web of Adaptation: Bird Studies in the American Tropics. New York & London. Snow, D.W. 1977. Duetting and other synchronised displays of the blue-backed manakins, Chiroxiphia spp. Pp. 239-251. In Stonehouse, B. & Perrins, C. (eds.). Evolutionary Ecology. London.

MANDARIN: substantive name, often used instead of Mandarin Duck, of Aix galericulata, a highly ornamental Chinese duck now naturalized in Britain (see DUCK). MANDIBLE: term sometimes used without qualification for the lower jaw (compounded of several bones--see SKULL) and its horny covering (see BILL), and in this sense contrasted with 'maxilla'; in another usage applied to either jaw, with the adjective 'upper' or 'lower' (see also MAXILLA; MUSCULATURE).

MANGO: substantive name of Anthracothorax spp. (for family see HUMMINGBIRD).

MANGROVE SWAMP: a specialized type of environment widely distributed in tropical parts of the world and bordering areas of the sea, tidal rivers, or saline marshes; it consists of mangrove trees (several species) growing closely together out of water and liquid mud, presenting a most formidable obstacle to human ingress. MANNIKIN: substantive name of various Lonchura spp.; in the plural, general term for a tribe (Amadini) of the Estrildidae (see ESTRILDID FINCH). Not to be confused with MANAKIN. MAN 0' WAR BIRD: sailors' name for Fregata spp. (see

FRIGATE-

BIRD).

MANTLE: see

TOPOGRAPHY.

MANUBRIUM: forward process of the sternum (see

SKELETON,

POST-CRANIAL).

MANUCODE: substantive name of species of Manucodia and Phony-

gammus (see BIRD-OF-PARADISE).

MANUS: the 'hand' (see

SKELETON, POST-CRANIAL; WING).

MAO: Gymnomyza samoensis, a MAPPING: see

HONEYEATER

endemic to Samoa.

CENSUS.

MARABOU: also 'Marabou Stork', Leptoptilos crumeniferus (see STORK). MARGARORNITHINAE: see

OVENBIRD (1).

MARGINAL COVERTS: see TOPOGRAPHY. MARISMA: Spanish word applied to marshy country, notably in the delta of the Guadalquivir (an important bird habitat). MARKING: a term initially confined in its application to what is now known as 'bird ringing' or 'banding', but conveniently extended as a comprehensive term for all techniques used to mark birds. All forms of

Marking

•

339

spri'19/~ummer (April-JUly)

• autumn /winter (AUJust-March)~ If?

*

:3-f ,. t

* * •

r-

2,8~. 1--

i:[t5 .. 5

. ~

2

0~

7

Fig. I. Recovery localities of Common Whitethroat Sylvia communis ringed in Great Britain. The British population of this species migrates slightly west of south to its wintering area in West Africa. There is a major autumn stop-over area in northern Portugal.

marking have in common a basic purpose: to make a bird recognizable, either as an individual or else as a member of a class, e.g., a brood, a colony or an age group. The many techniques now in use may be divided into two categories: the extensive system, generally organized on a national or even Continental basis, in which public co-operation is normally important or essential, and the intensive or private systems, in which the marks are meaningful only to the operator, or to those he initiates. The main-almost the only----extensive technique is known as bird ringing, the term 'banding' being preferred in North America and Australasia. The private or intensive techniques include colour ringing or marking in various forms, tagging, radiotelemetry, undertaken for reasons of research, and closed ringing for captive birds (see CAGE BIRD). Bird ringing. The essential feature of bird ringing, as here defined, is that each ring carries, in addition to a unique serial number, a postal address to which any finder of the ring is invited to write. Usually both number and address appear on the outside of the ring, but in North America, on the smallest sizes, the return address may be on the inside. The rings are bands of metal which are fixed around the tarsus (or, occasionally, tibia) of the bird. They range in size from an inside diameter of 1.8mm to one of 30mm. Aluminium or aluminium alloys are used for small sizes. Large sizes are frequently of modern alloys such as monel, incoloy or stainless steel. Most rings are supplied in the shape of a 'C', which is closed to form a circle round the leg. In some countries the largest rings are secured by having the two ends brought together and bent over to form a clip. The rings may be fitted on nestlings, as soon as the legs and feet are sufficiently developed, or on fully-grown birds caught specially for ringing (see TRAPPING). As a part of their bird-ringing scheme, certain issuing authorities have also used wing-clips. These resemble small safety-pins, the pin being passed through the PATAGIUM and secured in the cap, upon which are marked the usual inscriptions of address and serial number. Wing clips are especially used for marking young

* .spiLJ1!J/summer (April-July)

- autumn/winter (Ai{qust-March)

•

Fig. 2. Recovery localities of Lesser Whitethroat Sylvia curruca ringed in Great Britain. The British population migrates south east to winter in East Africa. The recoveries indicate staging posts in northern Italy and, probably, the Nile Delta in autumn and in Asia Minor during the spring.

Anatidae, which may be very difficult to catch by the time their legs have grown sufficiently to retain an ordinary ring (but see next paragraph). Their chief disadvantage is that they are inconspicuous when partly concealed by the feathers and hence produce proportionately fewer recoveries than do rings. A technique developed in Latvia temporarily reduces the inside diameter of rings with soft plasticine or florist's wax, thus permitting ducklings to be marked at a much earlier age and obviating the need for wing tags. The growing tarsus squeezes out the plasticine or wax so that the inside diameter is automatically adjusted to the diameter of the tarsus. The details of species, race, age, and sex (if ascertainable), date and locality are recorded for each ring used and the bird is released or returned to the nest. The ringing data are entered on schedules which are filed at the headquarters of each scheme for reference. Objects. Two broad categories of study may be recognized, migration and vital statistics, including life histories. The more spectacular nature of migration studies attracted attention from the outset (see MIGRATION), whereas the use of ringing for population studies and similar investigations began rather later and new methods of interpretation are still being developed. Results. Ringing data, based on the accumulation of individual case histories, provide generally more precise information than other migration study techniques. Limitations arise from the small proportion of birds recovered and the fact that the geographical distribution of these recoveries may not be fully representative. Effectiveness in determining the summer and winter distribution of migratory species tends to bear a

340 Marking

close relationship to the density of the human populations in the areas concerned, their literacy, and, their hunting traditions. Thus, for the Anatidae wintering in Britain, with a breeding range extending northwards and eastwards across Europe, the recovery rate may exceed 20% for some species and is generally over 10% • In contrast, small passerines wintering in Africa may show a recovery rate of less than 0.50/0. Common British garden birds have recovery rates in the range 1-4%, although the figure for particular species may vary appreciably between rural and suburban areas. Because of the high human population and the high level of ringing activity, ringers operating in countries like Britain and the Netherlands tend to enjoy much higher recovery rates for non-quarry species than do ringers in other parts of the world. Furthermore, improved catching efficiency, associated especially with mist nets and cannon nets (see TRAPPING), is leading to further improvement. For many species, ringers can now rely on re-capturing far more of their ringed birds than will be reported by the public-a factor of obvious importance in the development of population studies. For species with low recovery rates, there are generally still too few records to permit detailed analysis of summer and winter distribution. Recoveries providing data about migration are more numerous and may be used to determine such features as the direction and sometimes the speed of migration, and time of arrival of passage migrants in given areas. Only ringing can provide quantitative data for the study of partial migration and abmigration, and the presence of ringed birds in 'wrecks' and other weather movements is often a valuable guide to the origin of the populations involved. For species which may be at risk, as for example, auks from oiling, raptors from pesticides, terns from persecution, the policy of keeping a proportion of the population ringed at all times provides a sensitive monitoring system. Locally, ringing has proved effective as a means of studying the gathering area for communal roosts and the feeding ranges of colonial nesters. In the study of population dynamics, ringing data have been used to establish the age at which breeding begins; age structures of populations; annual, seasonal, and regional variations in mortality; common causes of death. The value of such data depends on the fate of the recovered birds being representative of what happens to all birds. This may be almost impossible to prove, but allowance can be made for recognized sources of bias, and recovery data are generally regarded as valid (see ECOLOGY). In long-lived species, including many seabirds, longevity studies were for a time handicapped by the weakness of the aluminium rings. The harder modern alloys, first introduced in the late 1950s, are beginning to produce more realistic survival figures (see AGE). History. Although there had been sporadic attempts and a few schemes (in Great Britain from 1890) of limited scope, the first ornithologist to undertake systematic large-scale ringing was Christian Mortensen of Viborg (Denmark), who commenced his experiments in 1899. Germany was quick to take up the study (1903) and the pioneer 'Vogelwarte' at Rossitten, on the Baltic, did much to establish the value of ringing. The practice soon gathered impetus: Hungary (1908), Great Britain (1909), Yugoslavia (1910), Holland (1911), Sweden (1911), Denmark (1914) and Norway (1914) all had effective schemes before the 1914--1918 war. Between the two World Wars there was a rapid growth in the number of ringing schemes, especially in Europe, at least 15 being established between 1918 and 1930, and a further 8 by 1939. In North America the start was later, for although an American Bird Banding Association was founded in 1909 (and Jack Miner was marking wildfowl before 1914 with rings carrying Biblical quotations instead of serial numbers), the two main centres, at Washington and Ottawa, were not established until 1920 and 1922 respectively; but the growth of activities was rapid and the scale of ringing soon outpaced work of individual European centres. Outside Europe and North America, ringing has been on a small scale, and generally of recent development, as is shown by the following dates of commencement: Japan (1924), Egypt (1937), New Zealand (1947), Tasmania (1947), Union of South Africa (1948), Australia (1953), and Zaire (1954). Marking has also been done in the Antarctic (e.g., by the UK, USA, France, Australia and New Zealand) and from time to time on various oceanic islands. In Britain, H.F. Witherby in London and A. Landsborough Thomson in Aberdeen both started comprehensive schemes in 1909. The latter scheme came to an end during the First World War, but the former developed steadily under the guidance of its founder until 1937, when responsibility for the organization was handed over to the British Trust for Ornithology, and a special Bird Ringing Committee was appointed to

control actrvines, with headquarters at the British Museum (Natural History). Although the scheme was for many years financially selfsupporting, since 1954 it has required a subsidy, currently from the Nature Conservancy Council. In 1963, the headquarters moved to Tring in Hertfordshire (see also OBSERVATORY, BIRD). In Europe a major obstacle to full use of ringing data has been the dispersed housing of the results, with over 30 different ringing schemes holding data and working autonomously. To meet this problem EURING, the European Union for Bird Ringing, was established in 1963 to standardize both methodology and terminology throughout the continent. The advent of computer facilities permitted the inauguration of an international data bank of European recoveries, at Arnhem in the Netherlands. This now stores recovery data for more than half the birds ringed in western Europe. Even in western Europe not all countries contribute to the Data Bank, while data from eastern Europe are as yet very unevenly represented. In North America a single banding scheme covers the entire continent. The main direction of effort has been towards birds of economic importance and the high annual intake of recoveries necessitated early use of computers to facilitate analysis. Sophisticated capture-recapture techniques have been evolved for use in population studies, while in the field of passerine migration annual corporate studies were introduced under the code name 'Operation Recovery'. Intensive or private techniques. The aim of most intensive marking techniques is to permit the recognition of individual birds at a distance, and there is little point in so marking birds unless the research worker is prepared to spend long hours of observation or to publicize widely a request for sightings. National and international discipline in the launching of colour marking programmes is essential to prevent inadvertent duplication of codes, but is too often lacking. Most early studies used celluloid rings, but these rarely incorporate light-fast pigments so that the colours fade in a year or two. For a time anodized aluminium was used, but modern plastics such PVC and Darvic have proved more satisfactory. 'Traditional' colour ringing usually involves the use of several different rings on each bird: for example yellow over blue left leg, yellow over red right leg. On bigger birds this has generally been superseded by the use of large laminated plastic rings engraved with large figures and/or letters. On geese, in favourable conditions, the detailed combination of letters and numbers may be read by telescope at distances up to 300 m. Other devices. For species which spend much time in the water, engraved leg rings may be of limited use. This has led to the development of neck collars, chiefly used on geese and swans, of nasal discs, used on ducks and of small plastic patches temporarily cemented to the plumage of head or wing. For the easier identification of birds on the wing, tags have been developed. Most are attached by a stainless steel pin, passed either through the patagium or elsewhere in the wing; some wrap round the wing, overlying the scapulars. Tags may be colour-coded or carry a combination of letters and figures. Radiotelemetry has been used to facilitate the tracking of birds by aeroplane, but is chiefly (and increasingly) employed for very intensive local studies. The equipment permits detailed, round-the-clock monitoring of movements, but despite advances in the miniaturization of both transmitter and battery, the weight factor still renders the technique unsuitable for use on small birds. The high unit cost of the equipment, which is often lost, means that few individuals can be marked in anyone programme (see RADIO TRACKING AND BIOTELEMETRY). Radio-isotopes, bonded to conventional metal rings, have been used to obtain round-the-clock records of the incubation roles of male and female seabirds. Web tags. In detailed studies of Anatidae it may be important to recognize the young as individuals from soon after hatching, at which stage their legs and feet are much too tiny to take a ring appropriate to a fully-grown bird. As an alternative to the wing clip already described, which is used as a permanent mark, small tags may be passed through the web of the foot, a conventional ring being substituted at a later date. Work in the United States has demonstrated that the same end can be achieved by the use of a variously placed tiny hole in the web. Plumage dyeing has been much used on pale-coloured birds ranging in size from small waders to swans. Dye offers a short-term approach, being lost with the first moult, but because of its conspicuousness at long range it has proved invaluable in tracing the migratory paths of birds such as Bewick's Swan Cygnus columbianus bewickii.

Maxilla

Close ringing. This technique differs from the others in that the rings are not split but are true rings. Their use is confined to nestlings, which are marked while the foot is still small enough to permit the rings to be slipped on; once the foot is fully grown the ring cannot be removed. Close rings are of little value to ornithologists, but aviculturists and pigeon-fanciers use them extensively to establish individual identity and ownership; and in the law of several countries a correctly fitted close ring is taken as proof that the bird was bred in captivity (see CAGE BIRD). In recent years the high-value, often illegal, trade in birds of prey has led to much research into a tamper-proof ring which can be 'locked' on to the leg of a bird for life. It is too soon to say whether designs evolved will successfully fulfil their function. R.S. Mead, C.I. 1974. Bird Ringing: BTO Guide 16. Tring. Stonehouse, B. (ed.). 1977. Animal Marking: Recognition Marking of Animals in Research. London.

MARROW: see BLOOD;

SKELETON, POST-CRANIAL.

MARSH-BIRD: substantive name of 2 South American icterids of the genus Pseudoleistes (for family see ORIOLE (2)). MARTIN: substantive name of some species of Hirundinidae (see SWALLOW).

MAR TLET: archaic and heraldic name for a bird which may have been either the House Martin Delichonurbica (or other hirundine) or the Swift Apus apus, perhaps used for both (see HERALDIC BIRDS). MATE: either member of a pair in relation to the other (see PAIR). MATING: see COPULATION. MATING SYSTEM: that part of the social organization of a species

that involves the relationship between the sexes, especially copulation and the subsequent events of the breeding cycle. In the great majority of birds-over 900/0 of all species--more or less long-lasting pairs are formed (see PAIR FORMATION), which usually persist through the breeding season and in some birds for life. The minority, which do not form simple pairs, show a great variety of mating systems, mostly involving some form of polygamy. Because of its prevalence in most families of birds it is generally thought that monogamy is the primitive condition in birds, and that polygamous systems are later specializations. There are two main forms of polygamy: polygyny (the mating of one male with two or more females) and polyandry (the mating of one female with two or more males). Both polygyny and polyandry may be simultaneous, when a bird has several mates at the same time, or successive (serial), when a bird has several mates in quick succession. A clear-cut classification of mating systems is difficult because they are not necessarily mutually exclusive; thus in some species polygyny is combined with successive polyandry. Some species, especially those with LEK displays, seem to be promiscuous in their mating; but detailed study is needed in order to establish this, and it is unlikely that both sexes will be equally promiscuous. Thus in some lek species which had been thought to be promiscuous, observation of marked birds indicates that females show well-marked attachments to particular males. In general it will be expected that males will be more promiscuous than females, because of the very different parental investment in each mating by the male and female. Males invest very little in each mating, and there is no great disadvantage to them in a mating which is unsuccessful in its outcome; but females invest a great deal in each reproductive attempt, and choice of a suitable mating partner is important. Some ecological correlates of the different mating systems are clear. Monogamy is usual when the conditions in which a species breeds are such that both parents are needed for the successful rearing of the young; polygamy and promiscuity are possible only when one parent is able to rear the young single-handed. Hence, polygamy and promiscuity are found mainly in birds with precocial young, especially if the young find their own food, and in birds with altricial young if their food is plentiful or easily found. It is probably for this reason that polygyny is found in several groups of seed-eating, fruit-eating and nectar-eating birds, and very rarely in insectivorous birds. Other factors are, however, important. For instance frugivorous birds that nest in holes tend to live strictly in

341

pairs, probably because both parents are needed to guard the nest-hole. Another predisposing condition for the evolution of polygyny is that a proportion of the males can occupy all the suitable nesting territories, the other males being relegated to suboptimal or unsuitable territories. If females of such species make their choice mainly on the basis of the quality of the male's territory, a small proportion of the males may acquire most of the females. This kind of system has been demonstrated in some American marsh-breeding icterids (see ORIOLE (2)) and may also apply to some weaver-birds and in less extreme form to some arctic sandpipers. A related system, apparently rare, involves the male's domination over an essential food resource. Male Orange-rumped Honeyguides Indicator xanthonotus defend the huge combs of the honeybee Apis dorsata: the females mate only with comb-holding males, and they and their offspring have access to the combs of the males with which they have mated. In some hummingbirds a similar system probably obtains, the resource in this case being a clump of flowers held by a territorial male. Several species of waders that breed in the far north, or in montane areas, have mating systems ('rapid multi-clutch systems'-Graul 1974) enabling them to make the fullest possible use of the short period that is suitable for nesting. The essence of such a system is that the female lays two or more clutches in quick succession; it may be combined with monogamy, the male incubating the first clutch and rearing the young and the female taking charge of the second clutch (e.g. Temminck's Stint Calidristemminckii, Mountain Plover Charadrius montanus), or with serial polyandry, the female laying clutches for two or more males (e.g., Dotterel Eudromias morinellus, Spotted Sandpiper Actitis macularia). For details of the various forms of polygamy, and of the groups in which they occur, see POLYGYNY and POLYANDRY (see also CO-OPERATIVE BREEDING). D.W.S. (1) Cronin, E.W. & Sherman, P.W. 1976. A resource-based mating system: the Orange-rumped Honeyguide. Living Bird 15: 5-32. Crook, I.H. 1965. The adaptive significance of avian social organizations. Symp. Zoo!. Soc. London 14: 181-218. Emlen, S.T. & Oring, L.W. 1977. Ecology, sexual selection, and the evolution of mating systems. Science 197: 215-223. Graul, W.D. 1974. Adaptive aspects of the Mountain Plover social system. Living Bird 12: 69-94. Lack, D. 1968. Ecological Adaptations for Breeding in Birds. London. Orians, G.H. 1969. On the evolution of mating systems in birds and mammals. Am. Nat. 103: 589-603. Oring, L.W. 1982. Avian mating systems. In Farner, D.S., King, I.R. & Parkes, K.C. (eds.). Avian Biology, Vol. VI: 1-91. New York. Pitelka, F.A., Holmes, R.T. & Maclean, S.F. 1974. Ecology and evolution of social organization in arctic sandpipers. Am. Zoo!' 14: 185-204.

MATURATION: literally 'ripening'; in physiology, applied par-

ticularly to completion of the development of the germ-cells (see in ethology, the development of a behaviour pattern in a young bird without performance, i.e., without learning through practice (see BEHAVIOUR, DEENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM);

VELOPMENT OF).

MATURITY: attainment of the age at which the bird is capable of reproduction (although breeding condition is a seasonal phenomenon); in practice, the criterion is usually the acquisition of full adult plumage (for immaturity see under YOUNG BIRD). In highly seasonal environments many small species first breed in their first summer, when they are just under a year old but in non-seasonal environments they may start breeding at 6-8 months of age, e.g., Zebra Finches Poephila guuata in Australia (see under LAYING). The term has occasionally been restricted to mean the age at which maximum breeding capability is attained, usually one or more years after the age of first breeding. MAVIS: popular name, in Britain, for the Song Thrush Turdus philomelos (see THRUSH). MAXILLA: osteologically, a slender paired bone of the SKULL, between

the jugal and the premaxilla; sometimes used more generally as a term for what is otherwise called the 'upper mandible', i.e., the upper jaw (of which the premaxillae are the chief bones) and its horny covering (see BILL); in the latter usage the term mandible is restricted to the lower part (see MANDIBLE).

342 Meadowlark

MEADOWLARK: substantive name of Stumella spp. (see ORIOLE

(2)).

MEAN, ARITHMETIC: equivalent to 'average' in the sense in which the latter word is most exactly used-the sum of the recorded values divided by the number of observations in the sample. In a perfectly symmetrical distribution the arithmetic mean coincides with the median and modal values (see BIOSTATISTICS). MEASUREMENT: here confined to the sense of recording the lengths of external features of birds. Measurements may be used to give a general indication of size or for a variety of taxonomic, ecological or other purposes (see also SIZE). Within a population of a species, significant differences in measurements may occur between the sexes, age classes or seasons, the latter reflecting feather growth and wear. Differences between populations may correlate with local environmental factors and over the range of a species may vary clinally or disjointedly according to subspeciation. Individual birds from the same population and agel sex group vary in size and correlated behavioural features may be found. Similar species can sometimes be separated most reliably by measurement (see also WING FORMULA). For scientific purposes, millimetres are conventionally preferred to centimetres, but centimetres are often used in general descriptions. Care should be taken to avoid measuring feathers shortened by undue abrasion and fracture or not fully grown during moult. Innumerable features of birds can be and have been measured but the 6 described below are in most common use. Wing. This is the most widely taken measurement, being a fair indicator of size of an individual within a species. It is easy to measure on a live bird. Wing-length is taken on the naturally folded wing from the carpal joint to the tip of the longest primary using a ruler with an end-stop. If the curvature of the wing is not corrected in any way, a 'minimum chord' is obtained. One of the two curvatures can be eliminated by pressing at the greater coverts to flatten the wing on to the ruler to give a 'flattened chord'. Most of both curvatures can be removed by flattening the wing as above and then straightening the primaries along the ruler with a firm stroking action to give a 'maximum chord' wing-length. Maximum chords can be measured most reliably and repeatedly and are to be preferred. The difference between the maximum and minimum chord can easily be 10% and thus as great as most other differences that might be being studied, so beware of published winglengths without the method stated. Beware too of measurements of skins which might, apart from the effect of shrinkage, be harder to flatten and straighten if this has even been attempted. In Britain, the maximum chord method is advocated by the British Trust for Ornithology for use by bird-ringers. Tail. Tail-length is generally taken as the measurement from the point of emergence of the feathers to the tip of the longest, but may instead be of a stated pair. Measurement can be made with an unstopped ruler, dividers or vernier callipers and taken from above or below the tail. The roundedness or forkedness of a tail is taken as the distance between the tips of the central and outer feathers measured directly from an unfanned tail. Bill. Bill-length is probably the second most widely used measurement after wing-length and is of particular interest in some seabirds, wildfowl and waders which show intraspecific variation with race and latitude. Bill-length can be measured to the cere (owls and birds of prey), to the start of the feathering, to the base of the skull or less commonly to the nares or the gape, so it is vital to note the method used in any published data. Other bill dimensions may be of ecological interest. Tarsus. The bone is measured from the depression at the rear of its upper joint to the end of the last complete scale before the toes diverge at the front. Dividers or callipers may be used. Total length. This is taken from bill to tail by laying the live or freshly dead bird on its back along a ruler and straightening it out. The measurement is difficult to take consistently, is of no taxonomic or ecological use and consequently is often expressed in inches in British literature. Total length is used in identification books to convey a general impression of size, though as such it is not very helpful because of the misleading influence of long bills or tails. Wing-span. Wing-span is measured from tip to tip by straightening the wings of a live or freshly dead bird as far as they will go without undue force. Like total length, it is not easy to measure consistently and is mainly used to give an approximate idea of size especially of larger

birds. Wing-span is, however, of use in flight performance models derived' from aerodynamic theory (see FLIGHT). Documentation. Measurements quoted in standard reference works are generally of museum skins which because of shrinkage will be lower than those obtained, as most now are, from live birds in the field. Many such published data are further inadequate because the method by which they were taken is not stated and the statistical necessity of giving the sample size and standard deviation is overlooked (see BIOSTATISTICS). There is thus an outstanding need for the collection and publication of standard measurements even of species which are common and frequently handled by bird-ringers. C.} .B. (2) MEATUS: an opening, particularly of the ear (see

HEARING AND

BALANCE).

MECHANICAL SOUNDS: non-vocal sounds, made by the bill, wings, or tail, as contrasted with vocal utterances (see VOCALIZATION). The 3 types may be considered separately. Bill sounds. Some of these, perhaps to be regarded as adventitious, are made by two birds together. Various clattering noises are made in the course of bill-fencing and bill-sparring in a wide range of birds, such as grebes, herons, auks, pigeons, kingfishers, woodpeckers, waxwings, thrushes, crows, and some finches. Bill-crossing and bill-tapping are common in the sexual display of albatrosses (Diomedeidae); the whetting together of the bills of a pair of Laysan Albatross Diomedea immutabilis has been described as producing a whistling sound. Bill-rattling by a single bird, producing a noise like that of a nutmeg-grater, occurs among frigatebirds as an alarm note, and also as an entreaty for food on the part of the chicks. The bill-clapping of storks is well known. In the White Stork Ciconiaciconia it is a sign of recognition between members of a pair or group; the head is thrown down and back between the legs, to the accompaniment of raising and flapping of wings and spreading of tail. The chick, when sufficiently strong, exhibits similar behaviour towards its parents, recognizing them and soliciting food. Other species of stork also clap, but less loudly. The Shoebill Balaeniceps rex clatters its massive mandibles, but without posturing, as a note of alarm and an entreaty for food. Bill-snapping as a defensive threatening sound is made by most owls and is particularly loud in such large species as the Eagle Owl Bubo bubo and the Snowy Owl Nyctea scandiaca. In a different category are sounds made by the bill in contact with various objects. Some of these are adventitious effects of feeding or nesting actions, for example among tits, nuthatches and woodpeckers. On the other hand, specialized bill-drumming-beating a tattoo on the wood of a tree-is practised by many woodpeckers and has been most studied in the Great Spotted Woodpecker Dendrocopos major. In this species both sexes produce a loud, harsh vibrating sound by an extremely rapid rain of blows at a selected point, most commonly near the end of a broken or dead branch, but exceptionally on some quite different sort of sounding-board such as the lead-covered top of a wireless mast. The sound produced depends upon the resonant properties of the branch; the normal duration is about a second, and the normal frequency may exceed 20 blows per second. At the higher rates the human ear runs the sounds together to form a continuous vibration which may be audible at distances up to 1 km. The strength diminishes after the first or second blow, and the rate accelerates steadily from 15 per second to 25 per second so that the sounds tend to die away and rise in pitch. The drumming period extends in Britain from the end of February to the first week in May; the sound serves to attract mates, and both birds drum before coition. In the Lesser Spotted Woodpecker D. minor, the sound tends to be less powerful and higher in pitch, and may last for 2 s at a frequency of 22 blows per second; both sexes drum before performing the sexual 'butterfly dance'. The Northern Flicker Colaptes auratus of North America beats a rolling tattoo on dead branches in spring, and sometimes uses metal telegraph poles for the purpose. Wing Sounds. The normal flight of some birds is inaudible except when there is a dense flock within close range. Owls are particularly silent, even at ultrasonic frequencies audible only to their prey, due to special adaptations of their feathers (these are absent in the fishing owl, Scotopelia peli). The flight of other birds may make a considerable noise. Ducks produce rather musical sounds with their wings when flighting; the audible intensity of the sound depends to a great extent on atmo... spheric conditions and wildfowlers are agreed that it reaches its maxi-

Mechanical sounds

WhiteStorks Ciconia ciconia bill-clappering at nest. (P hoto: E.]. Hosking). mum effect on still, frosty mornings. Teal Anas crecca, especially in planing down, make a metallic -sounding 'swoop', and among other surface-feeding species the Shoveler Anas clypeata stands out for the amount of sound emitted during level flight-as , in a different group, does the Shelduck Tadoma tadoma . On the whole, however, it is the diving ducks that make most sound, and notably the Goldeneye Bucephala clangula--commonly known in America as the 'Whistler ' because of the penetrating sound made by its wings , especially in the case of old drakes . The Mute Swan Cygnus olor, alone among its kind , produces a high-pit ched harp-like note from its primaries on the downbeat. Various gallinaceous birds have noisy flight. Flying Pheasants Pha sianus colchicus create a musical high-p itched whistle with their wings; and the 'whirr' of wings of Red Grouse Lagopu s lagopus scoticus and Partridge Perdix perdix are familiar. The American Wood Stork Myceena americana makes a most amazing noise as the air rushes through the wings when it dives from a height to its feeding grounds. The Rhinoceros Hornbill Buceros rhinoceros has been described as making a sound 'like that of a chugging steam locomotive' with its wings . Hummingbirds are so called because of the sound made by the extremely rapid vibration of their wings; it reminded Salvin of a piece of machinery actuated by a powerful spring. The humming sound is produced by wing-beats as fast as 80 to the second (although the largest species, the Giant Hummingbird Pacagona gigas beats its wings only 8-10 times per second). As originally noted by Darw in , different species produce a different 'hum' . In the male Broadtail S elasphorus platycercus the primary feathers taper at the tips and the air filtering through the openings produces a distinctive rattling whistle , whereas the female has normally shaped feathers and hovers with the usual humming or buzzing sound . The foregoing examples relate to ordinary flight, although the sounds are in some cases not heard under all conditions. There are other instances where a characteristic sound is emitted only at special times , and usually as an element of display ; these include cases where the sound is the result of wing-clapping, although that can happen also in other circumstances. This last point is particularly relevant to the pigeons; wing-clapping is common in dome stic pigeons, notably tumblers, and many wild species stan with a few clapping strokes when taking off-the sound varies considerably from one species to another. In the Woodpigeon Columba palumbus the male , near the top of its display flight, makes 1-3 vigorous claps with its wings; the sound has been attributed to forcible downstrokes analogous to the crack of a whip , but as in other cases it is more likely to be due to the wings striking each other.

343

Even the silent-flying owls do this . In the breeding season the Short-eared Owl A sio flamm eus will circle on extended wings with only occasional beats, and from time to time will drop like a stone for some distance clapping its wings 4-6 times in rapid succession beneath its body ; the wing-tips appear to meet only at the first clap, but contact at the carpal region is said to take place throughout the clapping. Clapping is also used when the nest is threatened. The Long-eared Owl A. otus performs zig-zag flights between the tree-trunks, and then rises above the tree-tops clapping its wings beneath the body at the end of each beat ; both sexes do this, the female less frequently, and again the action is also used when the nest is threatened. Similar habits have been descr ibed for other owls. In the breeding season the male Night jar Caprimulgus europaeus produces a series of wing-claps ; the tips do not appear to meet , but possibly the carpal joints do. The male may clap as many as 2S times in succession while gliding with tail spread and wings raised obliquely. The female also claps, and apart from the mating season has been observed to do so when accompanied in flight by her two young in early September. In America the Common Nighthawk Chord eiles minor indulges in 'skycoasting ', and, when the bird makes the turn , the air rushing through the primaries produces a booming sound such as one might imitate by blowing across the bung-hole of an empty barrel. The Ruffed Grou se B onasa umbellus of North America 'booms' , while at rest , by striking its wings against its brea st. It is a great performer in the mating season , and both sexes 'b oom ' before coition . The sound has been described as a deep-toned thump , like the muffled beating of a great heart, followed by a quickly accelerating drumming roll like distant thunder. Various other gallinaceous bird s have similar, if less notable , performances; for instance, the crowing of the cock Pheasant Phasianus colchicus in spring is associated with flapping and thumping. Both sexes of the Red-throated Diver Gavia stellata produce a loud rushing noise with their wings when, in May and June, they volplane down to the loch uttering wild raucous cries. The American Woodcock Scolopax minor has the first 3 primaries modified and attenuated as a musical instrument used during the nuptial flight; the writer observed this at twilight in March , when the birds produced a cadence of musical whistling during the rapid descent following the upward spiral. Various plovers in the breeding season make wing noises during flight ; thus the male Lapwing Van ellus uanellus makes a 'zooming' noise. Among the passerines, mention may be made of the bird s-of-paradi se; those species with specialized wings and drooping tails, such as Prince ss Stephanie's Bird-of-paradise Astrapia stephaniae, produce an attractive sound comparable with ru stling silk . The Neotropical manakins (Pipridae) perform peculiar dance s with both buzzing sounds and clashes that resemble loud thumb-snappings; their outer primaries are strikingly attenuated in some species , and some also have modified secondary feathers (see MANAKIN ) . Other examples include the wing sounds made by flappet larks Mirafra spp. and todies Todus spp . Finally, a case of wing-sound made by two birds : in courtship flight the drake Pintail Anas acuta passes beneath the duck so closely that their wings clatter together with a loud noise like a football rattle . Tail sounds. Of these the chief are the 'drummings' or 'bleatings' of snipe Gallinago spp . during aerial evolutions in the breeding season . The Common Snipe G. gallinago produces a resonant, tremulous sound lasting about a couple of seconds and sometimes frequently repeated ; both sexes do it, but chiefly the male . The sound accompanies a rapid descent at an angle from a considerable height. Experiments have provided definite proof that the sound is a result of vibration of the outer pair of rectrice s, which-when the tail is spread fanwise-are detached from the remaining 6 pairs; but that the wavering element is due to the action of the wings in intermittently deflecting air against the tail. The sound can be artificially reproduced by variou s devices, such as attaching the musical feathers in the appropriate position to a cork and whirling it at the end of a string ; the latter imparts a vibratory motion and serves (as a rigid stick will not ) to simulate the tremulous effect naturally derived from wing movements. The mus ical feather s, the outermost rectric es (7th pair), show a specialized struc ture, the essent ial feature s of which are comparable with those of a harp. The outer web is narrow and formed of stiff rami that can be easily separated. The inner web is very broad and formed of long, stiff rami making an acute angle with the shaft and having radii and hamuli so arranged that the whole web is strongly locked together. The adjacent

344 Median coverts

feathers (6th pair) show something approaching the same structure, whereas the 5 central pairs are soft and unmusical. In some other species of snipe that make similar sounds the total number of rectrices is greater-16, 18,20, or even 26-28; this last occurs in the Pintail Snipe G. stenura of Asia, in which 8-9 on each side are attenuated, the outermost so much so that they resemble pins. The number showing specialization varies considerably with species; in G. nobilis of northern South America there are 3 on each side. The quality of the sound also varies; in Latham's Snipe G. australis it is more voluminous-a tremendous rushing noise-and in the Auckland Island Snipe Coenocorypha aucklandica the bleat is high-pitched. The Great Snipe Gallinago media and Jack Snipe Lymnocryptes minimus possess no musical feathers, and the same is true of the European Woodcock Scolopax rusticola and the American Woodcock S. minor. A sound made by the Lyre-tailed Honeyguide Melichneutes robustus, in the course of elaborate flying evolutions, is thought to be produced by vibration of the outer rectrices, as in the Snipe. P.M.-B. (J.D.P.)

MEDIAN COVERTS: see TOPOGRAPHY. MEDULLA: for that of the adrenal glands see

ENDOCRINOLOGY AND

THE REPRODUCTIVE SYSTEM.

MEDULLA OBLONGATA: part of the hindbrain (see

NERVOUS

SYSTEM).

MEGAGEA: see under

ARCTOGAEA; DISTRIBUTION, GEOGRAPHICAL.

MEGAPODE: substantive name of species of Megapodiidae (Galliformes, suborder Galli); in the plural, general term for the family. Alternative English names, given to species found in Australia, are 'Scrubfowl', 'Brush-turkey'-and in one instance 'Mallee Fowl' or 'Lowan'. Such general terms as 'mound-birds', 'mound-builders', and 'incubator birds'-this last a common American usage-have been applied to the group. The family is a small one. The members are characterized by their habit of not incubating their eggs. Instead they lay them in holes in the ground or in mounds of rotting vegetable matter and leave them to be incubated by natural heat. The family comprises 6 genera, which can be divided into 3 ecological groups, viz., scrubfowl (Megacephalon and Megapodius), brush-turkeys (Alectura, Aepypodius, and Talegalla), and the MaBee Fowl (Leipoa). Of these Megacephalon, Alectura, and Leipoa are monotypic, the species being M. maleo, A. lathami, and L. ocellata. The genus Aepypodius includes 2 species, A. arfakianus and A. bruijnii; and Talegalla includes 3, T. cuvieri, T. fuscirostris, and T. jobiensis. Peters recognized 9 species, including 28 subspecies, of Megapodius, but E. Mayr reviewed the genus and reduced these to 3 species-M. freycinet, M. laperouse, and M. pritchardii. Some later authors have increased the number of species but not convincingly. Characteristics. With the exception of Megacephalon maleo which is more colourful, scrubfowl are dull brownish birds with sombre plumage and small crests. M. maleo is distinguished by having a black tail, black wings, and pink underparts, and its head bears a prominent casque. All are about 50 em in total length. The brush-turkeys are black, with vertically folded tails, and are longer than scrubfowl, being 66-71 em in total length. Their heads and necks are bare, except for numerous coarse hairs. Similar in size to the brush-turkeys, the Mallee Fowl is coloured brown in keeping with the red-brown soils of its habitat, and each feather of the wing coverts bears a prominent white spot edged with black. Megapodes are ground-living birds. Scrubfowl and brush-turkeys are very active, although secretive, and seldom fly unless hard pressed. They are quite vocal, particularly in the evenings. According to K.H. Bennett, the Mallee Fowl's 'actions are suggestive of melancholy, for it has none of the liveliness that characterizes almost all other birds, but it stalks along in a solemn manner as if the dreary nature of its surroundings and its solitary life weighed heavily on its spirits'. Habitat. The brush-turkeys are generally restricted to tropical rainforest, both lowland and highland, but in a few places in Australia Alectura extends into drier, more inland scrubs. The scrubfowl are also mostly found in rain-forest but also are common in monsoon forest and gallery forest in riverine locations. The Mallee Fowl is unique in inhabiting a semi-arid environment. It is

Brush Turkey Alectura lathami. (N. w.e.).

confined to the dry scrubs of inland Australia; it is characteristic of, but by no means confined to, mallee scrub, which consists of several species of dwarf eucalyptus. The only extension of its range from the inland area occurs in Western Australia, where it is found in a narrow strip of heath land on the south-western coastline. Distribution. Of the brush-turkeys, Aepypodius spp. and Talegalla spp. are confined to New Guinea, and Alectura lathami to the eastern coast of the Australian mainland. Megapodius freycinet, with many subspecies, extends from the Nicobar Islands in the west to central Polynesia in the east, and from the Philippines in the north to the tropical northern coasts of Australia. Included in this range are coral islands with little vegetation, heavily vegetated continental islands, and mainland jungles. The birds are found in all these habitats but rarely extend far inland. M. pritchardii and M. laperouse have a similar habitat, but more restricted ranges, in central Polynesia and the Mariana Islands respectively. The Maleo Megacephalon maleo is found in Sulawesi. Populations. Eggs of megapodes are used as food by indigenous peoples and, in places, traded for other goods in the markets. In New Britain and some other places the harvesting of eggs of M. freycinet is the prerogative of certain clans and age-groups and some ceremony is attached to it. Prayers are said to ensure that the birds return in good numbers to the breeding ground each season. In some cases, because of access to firearms and to a cash economy involving the eggs, the traditional methods are now upset and predation could be a serious population problem, but in the past the rituals were, in effect, a primitive but effective programme of harvest regulation and management. The present position is that due to habitat destruction, perhaps accelerated utilization of the birds and their eggs and also perhaps because of declining volcanic heat in some regions, some megapodes have declined in this century. Concern has been expressed especially for Megacephalon maleo and Megapodius pritchardii but detailed data are lacking. The 3 species in Australia, Leipoa ocellata, Megapodius freycinet and Alectura lathami, are still in a strong position despite clearing of habitat in the interests of agriculture and, in Leipoa, the competition for food imposed by grazing stock and rabbits. Movements. Australian populations of Megapodius freycinet, Alectura lathami and Leipoa ocellata. are sedentary. There are no precise data on other species but, although some populations make roosting flights to off-shore islands, there seems to be no doubt that all are essentially sedentary. Food. There are no precise data on the food of any megapode, but general observations suggest all are omnivorous. The food mostly consists of insects, small animals, seeds and fruits. The food of the Mallee Fowl is better known than that of other members of the family and

Melipotes

consists largely of the seeds of the Acacia, Cassia and Beyeria, and the flowers of several ephemeral herbs as well as ground-living insects and small lizards. The Mallee Fowl is apparently independent of free water, but will drink if water is available. Behaviour. The brush-turkeys and the Mallee Fowl are solitary to the extent that, except when eggs are to be laid, the male drives the female from the mound. The other species, where there have been observations, live in pairs and, with mound-building species, two or more pairs can use the one mound but visit it at different times so that confrontation is avoided. Voice. There is no detailed description of the repertoire of sounds of any megapode. The male Mallee Fowl possesses a very loud, booming call and the female a high-pitched crow. The brush-turkeys have gobbles and loud grunts and the scrubfowl loud cries that are likened to gurgles and shouts. Breeding. The simplest type of incubation is found in Megacephalon, and some populations of Megapodius freycinet. The birds simply lay each egg in a pit dug on a beach or in sandy soil exposed to the sun. The hole is filled in and the eggs are hatched by heat conducted from the soil surface. The site is not visited again, and so no temperature control is exercised. A suitable incubation temperature is apparently achieved by careful selection of the location of each egg-pit. On some islands in the Pacific, the Solomons and in New Britain, the egg-pits of Megapodius species are dug into soil heated by volcanic action, the eggs being incubated by that agency. On Dunk Island, off the Queensland coast, some M. freycinet lay their eggs in fissures in rocks exposed to the sun, the heat-retaining capacity of the rock ensuring a relatively constant temperature by day and night. In other places, particularly in denser jungles, Megapodius freycinet constructs large mounds of earth up to 11m in diameter and 5 m high, including a variable amount of vegetable material which, by fermentation, supplements the heat of the sun. The eggs are laid in tunnels up to 1m long dug into the mound. The amount of vegetable material in the mound varies according to its location. Some mounds are built of almost pure soil and others of almost pure vegetable material, and all intermediate stages exist. Several pairs of birds participate in the construction of these mounds. Apparently the exact composition is determined by the local air temperature and amount of insolation; heavily shaded mounds require a greater supplement of heat of fermentation than those exposed to direct sunlight. Studies of M. freycinet in north Queensland have shown that in a large leafy mound the temperature fluctuated from 30-38°C but the egg was always laid in the warmer parts of the mound. There was evidence that the birds were conscious of the temperatures in the mound but it cannot be said if they exercised any control over it. There is no such variation in the nesting mounds of the brush-turkeys, all of which construct mounds composed mainly of plant material; these are commonly about 4 m in diameter and 1m high. In the warm, moist jungles the mound ferments rapidly and generates much heat. The males regularly test the temperature of the mound by probing with their bills; the temperature-perceiving organ is not known but is possibly the tongue. In the first burst of fermentation the temperature of mounds rises to a high level, and the male exercises some control over it by digging into the top and turning over and mixing the material. Not until the temperature is declining does he permit the female to approach and lay eggs. Throughout the incubation period the male remains in charge of the mound. In captive birds it has been shown that the temperature does fluctuate but the egg is always placed in the warmer parts of the mound. It is suspected, but not proved, that the male exercises some control over mound temperature. It has also been suggested that digging in the mound is important in controlling the oxygen supply available to the embryo. In its arid inland habitat the Mallee Fowl must adopt more complicated methods to secure a suitable incubation temperature. The air temperature fluctuates widely during the day and the year; accordingly, the soil does not keep a suitable constant temperature. Leaf mould does not form on the ground, litter is sparse, and fallen leaves dry and wither and do not ferment. To provide the proper constant temperature, the birds dig a hole in the ground up to 5 m in diameter and 1-1.5 m deep. During the winter they fill the hole with vegetable material swept up from the ground over a radius of some 45 m, and when it is moistened by a shower of rain the

345

whole is covered by a layer of sandy soil 50 cm or more thick. Sealed from the dry air, the vegetable material ferments and generates heat, which later in the season is supplemented by solar heat. It has been shown that in the spring fermentation heat is the more important and the birds need to open the mound frequently to allow heat to escape, so as to maintain the incubation temperature of 34°C. In midsummer the thickness of the soil cover is increased so as to slow the penetration of the sun's heat into the mound; by then the sun is the most important source of heat and is greater than is needed. In autumn the sun's heat is less and the fermentation heat has been exhausted. Then the birds open and flatten the mound daily to allow the sun's rays to penetrate it and warm the eggs. The result of all of this is a very uniform temperature in the mound for several months. Details of egg laying have been recorded for only one megapode, the Mallee Fowl. The number of eggs laid varies from 5 to 35. Variation in clutch size is very great, both between different females in one year and in the same female in different years. The eggs are laid at intervals of several days, the length of the interval being apparently determined by the nutritional state of the female. As many as 35 eggs have been laid by a female Alectura lathami in captivity. Up to 20 eggs have been taken from pits of M. freycinet in New Britain, but in north Queensland one female, watched quite regularly, laid 12 or 13 in the one season. Each egg begins to incubate as soon as it is laid and, as the eggs are laid throughout a period of several months, the first eggs are hatched and the chicks have left the mound long before the last eggs are laid. The chicks, on hatching, dig their way unaided to the surface of the mound and run into the scrub. They are capable of running very swiftly within a few hours of hatching and can fly within 24 hours. They never see their parents and live completely independent and solitary lives. H.I.F. Baltin, S. 1969. Zur Biologic und Ethologie des Talegalla-Huhns (Alectura lathami Gray) unter besonderer Berucksichtigung des Verhaltens wahrend der Brutperiode. Z. Tierpsychol. 26: 524-572. Crome, F.H.J. & Brown, H.E. 1979. Notes on social organization and breeding of the Orange-footed Scrubfowl Megapodius reinwardt. Emu 79: 111-119. Fleay, D.H. 1937. Nesting habits of the Brush Turkey. Emu 36: 153-163. Frith, H.J. 1956. Breeding habits in the family Megapodiidae. Ibis 98: 620-640. Frith, H.J. 1956. Temperature regulation in the nesting mounds of the Mallee Fowl Leipoa ocellata Gould. CSIRO Wild. Res. I: 79-95. Frith, H.J. 1956. Breeding of the Mallee Fowl Leipoa ocellata Gould. CSIRO Wild. Res. 4: 31-60. Frith, H.J. 1962. The MaBee-Fowl: the Bird that Builds an Incubator. Sydney.

MEGAPODIIDAE: see GALLIFORMES;

MEGAPODE.

MEGASUBSPECIES: a subspecies or group of subspecies which is considered almost to deserve the status of an ALLOSPECIES. The status of such a geographically representative form may be represented typographically. For instance, if the Red Grouse of Scotland, scoticus, is considered to be merely a distinct subspecies of the continental Willow Grouse Lagopus lagopus, it is represented by a simple trinomial, L. lagopus scoticus. As a megasubspecies it may be shown as L. (lagopus) scoticus. As an allospecies it may either be represented simply as a species L. scoticus; or its relationship to L. lagopus may be indicated by the use of square brackets, L. [lagopus] scoticus. Amadon, D. & Short, L.L. 1976. Treatment of subspecies approaching species status. Syst. Zool. 25: 161-167.

MEIOSIS: division of a germ-cell involving reduction in the number of chromosomes (see CELL; GENETICS). MELAMPITTA: substantive name of the 2 species of Melampitta of New Guinea (for family see RAIL-BABBLER). MELANIN: see COLOUR. MELANISM: see PLUMAGE,

ABNORMAL.

MELEAGRIDINAE: see under

GALLIFORMES;

and

TURKEY.

MELIPHAGIDAE: a family of the Passeriformes, suborder Oscines; HONEYEATER; SUGAR-BIRD (1).

MELIPOTES: substantive name of the 3 species of Melipotes of New Guinea (for family see HONEYEATER).

346 Membrane bone

MEMBRANE BONE: one that, in the course of development, ossifies directly without going through a cartilaginous stage (see SKELETON, POST-CRANIAL).

MEMBRANES, FOETAL: see DEVELOPMENT,

EMBRYONIC.

MEMBRANES, SHELL: see EGG. MENDELIAN INHERITANCE: see GENETICS. MENTUM: chin (see TOPOGRAPHY). MENURAE; MENURIDAE: see PASSERIFORMES, suborder Oscines; LYREBIRD.

MERGANSER: substantive name of Mergus spp. (see DUCK). MERGINI: see DUCK. MERISTIC: a statistical term for data values that vary in whole units, such as the number of eggs in a clutch. In contrast, 'linear' values vary continuously, as in the measurement of wing length, where precision is limited only by the precision of measurement (see also BIOSTATISTICS). MERLIN : Falco columbarius (see FALCON). MEROBLASTIC: the type of embryonic development found in birds (see DEVELOPMENT, EMBRYONIC). MEROPES; MEROPIDAE: see CORACIIFORMES; MERRYTHOUGHT: the

FURCULA;

and see

BEE-EATER. SKELETON,

POST-

CRANIAL.

MESENTERY: a fold of peritoneum in the abdominal cavity, enclosing part of the intestine together with blood vessels and nerves supplying it (see ALIMENTARY SYSTEM). MESETHMOID: bony interorbial septum (see SKULL). MESIA: substantive name of the Silver-eared Mesia Leiothrixargentauris (see BABBLER). MESITE: name used for 2 of the 3 species (Monias being the other) of the family Mesitornithidae, sole member of the order Mesitornithiformes. The family is endemic to Madagascar. Although placed here in its own order, its systematic position is by no means certain. At one time or another it has been considered as galliform, gruiform, ranine or even passerine, specimens reminding at least one student of ground-babblers of the genus Eupetes (family Timaliidae, subfamily Orthonychinae). Characteristics. The 3 species are c. 30cm long, with long and broad tails, short wings and moderate-sized feet. The bill is short and straight in Mesitornis, longer and curved in Monias. There are 5 pairs of powderdown patches. The Brown Mesite Mesitomis unicolor is rufous brown above, with a single white stripe along the sides of the neck, somewhat paler, more greyish below. The sexes are alike. The White-breasted Mesite M. variegata is longer billed, but with a shorter tarsus. It also differs in having the sides of the head streaked with whitish, rufous and blackish, the throat and chest whitish spotted with black. The Monias (alternatively Bensch's Rail) Monias benschi, unlike the 2 Mesitornis spp., shows well-marked colour dimorphism. Both sexes are greyish above, with a white superciliary streak. The male, however, is whitish on the throat and chest, the latter spotted with black, whereas the female has this whole area heavily marked rufouschestnut. Habitat. All 3 species are strongly terrestrial. M esitomis unicolor inhabits evergreen forest; M. variegata thick woodland relatively clear of underbrush; and Monias benschi subdesert scrub with a shady substrate covered thickly with leaf litter. Distribution. Mesuornis unicolor is known from widely scattered localities in the humid east, but M. oariegata is only known from Ankarafantsika, some 100km south-east of Majunga, and from near Tsarakibany, in the extreme north. Monias benschi is confined to the

Brown Mesite Mesuomis unicolor. (C.E.T.K.).

coastal south-west, from north of Tulear to the Mangoky River. Populations. Due to habitat destruction, the status of all 3 species is a matter for deep concern; particularly of Mesuornis variegata, so localized. Movements. All may be assumed to be extremely sedentary. Food. Nothing is known about the diet of the Mesitornis spp., but Monias benschi feeds on fleshy fruits and insects. Behaviour. Monias benschi runs with quick, pigeon-like steps, bobbing the head and depressing the tail at each step. It is capable of flying short distances, but does so only rarely. It tends to be gregarious, and has even been recorded in groups of up to 20. There is no information regarding Mesitornis unicolor or variegata, except that the latter has been recorded in pairs. Probably in all respects they resemble Monias benschi. Voice. A variety of calls, including a 'choral song', have been described for Monias benschi, but the most typical one is nak-nak-nak- - -; hence the local name 'naka', Mesitomis variegata is said to emit a brief tsik, but nothing at all is on record for unicolor. Breeding. The nest of all 3 species is placed in a shrub or small tree within 2 m of the ground, in such a situation that it could be reached without flying (in the case of Monias benschi a kind of inclined 'ramp' has been noted). It is a flat, thin platform of twigs with some lining of grass, leaves and other soft material, scantily constructed. The eggs are nearly oval, whitish, somewhat glossy, spotted with brown, tending to form a wreath at one end. The chicks are covered with down at the time of hatching. In Monias benschi the down is rufous brown on the upperparts, white on the underparts, but in the Mesitornis spp. it is said to be entirely black. All 3 species have been claimed to be nudifugous, although for Monias benschi the age at which the young leave the nest is positively stated to be unknown. Two nests of Mesitornis unicolor each contained a single egg being incubated by a female, which allowed herself to be caught on the nest. For M. oariegata, however, the clutch-size is said to be 2 or 3, and possibly more than one female is involved. At all events, one nest of Monias benschi contained 2 eggs, apparently laid by different females, associated with a single male. Incubation was by the male and at least one female. In the case of another nest, the family consisted of one male, one female and 2 young, which were fed by both parents. (A.L.R.) C. W.B. Appert, O. 1968. Beobachtungen an Manias benschi in sudwest-Madagaskar. J. Orn, 109: 402-417. King, W.B. 1978. Red Data Book. Morges. Lavauden, L. 1937. Histoire de Madagascar. 12, Oiseaux. Suppl. Paris. Rand, A.L. 1951. The nest and eggs of Mesoenas unicolor of Madagascar. Auk 68: 23--26. Sibley, C.G. & Ahlquist, J.E. 1972. A comparative study of the egg white proteins of non-passerine birds. Bull. 39. Peabody Mus. Nat. Hist.

MESITORNITHIDAE: see MESITORNITHIFORMES;

MESITE.

MESITORNITHIFORMES: an order, comprising the sole family Mesitornithidae (see MESITE). In Wetmore's system treated as a suborder Mesitornithes of the order Gruiformes. MESOBLAST: the middle layer of the embryo, developing between

Metabolism

the epiblast and endoblast that are formed at a very early stage (gastrulation)-see DEVELOPMENT, EMBRYONIC.

MESOENATIDES: alternatively 'Mesoenades' and 'Mesitornithes' (see MESITORNITHIFORMES). MESOGYROUS: see MESOMYODI: see

The central metabolic reactions (often called intermediary metabolism) are those involving carbohydrates, fats and proteins (Fig. 1) but we may also speak of the metabolic reactions of individual elements, especially of minerals, e.g. calcium metabolism (see EGG). Metabolic reactions are all catalyzed by specific enzymes under hormonal control (see ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM).

ALIMENTARY SYSTEM.

PASSERIFORMES.

MESOPTILE: term applied to the second of two nestling down plumages, in cases where there is such a sequence, the first then being called 'protoptile' (see PLUMAGE). METABOLISM: the processes of biochemical breakdown and synthesis of nutrients that take place within the cells of all body tissues. Catabolic processes provide the energy necessary for the maintenance of body temperature and for muscular work, as well as supplying precursor compounds for the anabolic processes of growth and body maintenance.

The biochemical breakdown of carbohydrate and fat (and in some circumstances protein) liberates energy partly as heat, which contributes to thermoregulation (see ENERGETICS; HEAT REGULATION), and partly as chemical energy by the formation of a high-energy compound, adenosine triphosphate (ATP), which fuels many other metabolic reactions and is itself utilized directly by muscle cells to perform work. Carbohydrate metabolism. The breakdown of carbohydrates ultimately involves their complete oxidation to carbon dioxide and water but the initial stages of this process (glycolysis) can occur anaerobically (in the absence of oxygen) to yield small but useful amounts of energy as ATP. Under anaerobic conditions the end point of glycolysis is lactic acid. Cells cannot tolerate excessive amounts of lactic acid, however, so that heavily working muscle can obtain sufficient energy from ATP produced in this

CARBOHYDRATE

PROTEIN

LIPID

+

GLYCOGEN

GLUCOSE

~

~1+PhoSPhate

triglycerides

/\

glucose 6 phosphate

~ fructose 1,6 diphosphate t glyceraldehyde 3 phosphate +

1

KETOGENIC AMINO ACIDS

GLYCOGENIC AMINO ACIDS

• methionine • valine • arginine glutamine • histidine ornithine proline

fatty acids

dihydroxyacetone phosphate

1 ,3 diphosphoglycerate ~

12ATPI

phosphoenol pyruvate

t

~~14ATPI

}

*'" ~

~

• PhenYlalanine} tyrosine ~ • isoleucine

/

glycerol

2 ATP I - - 1

alanine cysteine • glycine serine • threonine aspartate asparagine

347

}

~ malate ~

fumarate

~

"'E~------~"~acetyl ~ acetoacetate

pyruvate

/

~ oxaloacetate

~KREBS

¥ CYCLE 30 ATP

succinate./'

~

~glutam~

~~

lactate

\

J

citrate

CoA

1

KETOGENIC AMINO ACIDS

• isoleucine • threonine • tryptophan

()(ketoglutarate

Fig. 1. Biochemical pathways of intermediary metabolism. Essential amino acids are marked •.

• leucine • phenylalanine tyrosine • lysine • tryptophan

348 Metabolism

pathway for only a limited period before fatigue due to lactic acid build-up develops. The lactic acid accumulation constitutes an 'oxygen debt' since it must eventually be removed by oxidation. Anaerobic glycolysis with lactic acid as an end-point releases only 7% of the energy of a glucose molecule. However, in the presence of oxygen, lactic acid is not formed and complete oxidation can occur, trapping some 37% of the total energy of one glucose molecule as ATP. The remainder is liberated as heat. Glucose or other intermediate stages of glycolysis essential for energy production must sometimes be provided from non-carbohydrate sources. The enzymes for this occur primarily in the liver and are particularly important in the embryo because yolk contains very little carbohydrate. These enzymes decrease markedly after hatching in granivorous birds with a high carbohydrate diet, but carnivorous species retain them. Carbohydrate metabolism is controlled by the pancreatic hormones insulin, glucagon and avian pancreatic polypeptide. Insulin lowers blood glucose, promoting the synthesis of glycogen in the liver, while glucagon stimulates the breakdown of liver glycogen. Fat metabolism. Birds store lipid as an energy reserve for overnight metabolism and in large amounts for long-distance MIGRATION. Lipid has almost twice the energy value as the same dry weight of carbohydrate and, unlike carbohydrate, can be stored without large amounts of additional water. The weight saving is obviously advantageous for flight. Some fat is taken in the diet but birds also convert large amounts of dietary carbohydrate to lipid before use, which is consistent with the low Respiratory Quotients (RQ values of 0.75-0.80) measured in birds (see ENERGETICS). In birds the liver is the main site of lipid synthesis and is 20 times more active than other sites in the body, whereas in mammals adipose tissue itself is important in lipid synthesis. A product of glycolysis, pyruvate, is the normal starting point for lipid synthesis, being converted first to fatty acids and then to triglycerides. Since the liver has only limited storage capacity, the triglycerides are liberated into the bloodstream to be transported either to target tissues and metabolized, or to fat depots and stored. Mobilization of stored fat involves hydrolysis to free fatty acids and glycerol. Fatty acids are readily oxidized inside muscle cells, the later stages of oxidation occurring along the same pathways as the breakdown of carbohydrate. The complete breakdown of fatty acids enables 41% of the total energy stored as lipid to be trapped by ATP and then used by the muscle cell, a figure agreeing well with that obtained by the complete combustion of carbohydrate. The structure of bird flight muscle reflects which metabolic pathway normally provides energy. 'White' muscle has few mitochondria (cell structures where oxidation occurs), few lipid inclusions, and is poorly oxygenated. It is, however, rich in carbohydrate (glycogen) which can be rapidly metabolized anaerobically. Such muscle is adapted to shortduration bursts of hard work, for example during take-off. In contrast, 'red' muscle has little glycogen but is rich in fat, myoglobin (the oxygen-carrying pigment responsible for the red colour), mitochondria and the enzymes for fatty acid oxidation, all of which enable the muscle to sustain energy output for steady prolonged flight. Protein metabolism. Proteins enter the metabolic pathways as amino acids. Two processes, transamination and deamination, are central to protein metabolism. Transamination involves the transfer of an amino group, - NHz, to another carbon skeleton, so that all amino acids, other than a few 'essential' amino acids (see NUTRITION), can be interconverted. The deaminated carbon chains of some amino acids may be metabolized by pathways leading to intermediates in carbohydrate metabolism and so take part in carbohydrate synthesis or oxidation (the glycogenic amino acids); others may take part in fatty acid synthesis (ketogenic amino acids). Glutamate plays a central role in regulating nitrogen metabolism; it can be deaminated or synthesized without involving a receptor or donor amino acid and it can give up an amino group as waste ammonia, NH 3 • In mammals this waste ammonia is detoxified by conversion to urea. However, this requires the enzyme carbamylphosphate synthetase, which birds lack. Instead birds form uric acid (see EXCRETORY SYSTEM), a nearly insoluble compound whose particular advantage is that, as the waste product of embryonic metabolism, it can be stored harmlessly within the egg. Protein metabolism is under hormonal control; indeed, hormones are often classified as anabolic or catabolic with respect to protein. Adrenal corticosteroids increase protein mobilization and insulin and glucagon also directly affect amino acid transportanc metabolism. P.J.J. Sturkie, P.D. (ed.). 1976. Avian Physiology. New York.

METACARPUS (adj. metacarpal): name of certain bones of the 'hand'

(see

SKELETON, POST-CRANIAL).

METAL- TAIL: substantive name of

HUMMINGBIRDS

of the genus

Metallura.

METAPATAGIUM: a membranous fold of skin between the body and the posterior margin of the upper wing (see MUSCULATURE; WING). METATARSUS (adj. metatarsal): name of bones of the foot, 3 of

them fused together in birds, and at their upper ends with the distal row of tarsals, to form the TARSOMETATARSUS (see also LEG; SKELETON, POST-CRANIAL).

METEOROLOGY: see

BIRDS AND WEATHER.

MEW: archaic or poetic name, also 'sea-mew', for a gull (Laridae sp.), cf. German 'Mowe'; also, in American usage, adjectival name of LaTUS canus (see GULL). MEWS: term used in

FALCONRY.

MICROECA: substantive name of most species of Microeca, a genus of Australasian flycatchers (see

FLYCATCHER (1».

MICROPODIFORMES: name formerly used for the order

APODI-

FORMES; SWIFT.

MICROPSITTINAE: see

PARROT.

MICROSMATIC: with poorly developed olfactory sense (see SMELL). MIGRATION: term used hitherto in ornithology for only those

movements of bird populations occurring at predictable times of each year, between breeding and one or more non-breeding areas, and therefore involving flights in predictable directions. Movements which do not include an obligatory return journey or preferred directions of flight have been classed as 'DISPERSAL', 'nomadism', 'emigrations' and 'IRRUPTIONS' rather than 'true' migrations. But the functions of all these types of movement may be similar: to allow exploitation of different geographical areas at different stages of the annual cycle and in response to seasonal changes in population density and in the environment (see below). They may also follow from vegetational changes in an area, resulting from plant succession. This long-established classification has resulted from emphasis on populations rather than individuals. Thus DISPERSAL has been distinguished from migration because only the latter need involve a change in the geographical centre of distribution of the population. Each individual, however, that takes part in the outward dispersive movement, from e.g., a seabird colony, might in fact fly in a preferred direction rather than at random; but different individuals would have to move in different preferred directions if the centre of distribution were not to change. Since dispersals usually occur at predictable times of year, and since, especially in seabirds, the individuals of the species concerned may reassemble at the breeding locality in the following year, the difference from 'true' migration lies only in the degree of unanimity amongst individuals concerning the preferred direction of departure. In the more specific terminology of Berndt and Sternberg (1968), dispersals are movements that lead to observed dispersions (locations in space) of individuals of a population. Their terminology was developed for comparisons of the locations of individuals in successive breeding seasons, later termed 'natal dispersal' and 'breeding dispersal' by Greenwood (1980). Such studies consider only the resultant distances and directions involved, and not the routes by which the changes in breeding locations occur, which mayor may not involve long-distance return migrations between breeding seasons. Even in 'true' migrations, the routes, and therefore directions, by which individuals of a species return to their breeding areas are not necessarily the reverse of those followed on the outward journey. For example, the Pied Flycatcher F icedula hypoleuca returns from Africa to its northern breeding range by a more easterly route. Fidelity to a previously used breeding site occurs commonly in long-distance migrants, and fidelity to a wintering site is found regularly in some wildfowl,

Migration

especially geese, and estuarine waders. Some marked individual passerines have returned to the same 'wintering' area in Africa (Moreau 1972), but fidelity to a non-breeding locality may be the exception rather than the rule amongst passerines. This is especially true for species whose foods outside the breeding season occur unpredictably either in space (e.g., fruit and berry crops) or time (e.g., mass emergence of insects). Indeed, although some northern European thrushes, such as the Redwing Turdus iliacus, are generally considered to be 'true' migrants, the movements of individuals within the wintering range are best described as itinerancy (sensu Moreau 1972). It is but a short step further to include within the class of 'true' migrants species that may shift their breeding localities, within a year, e.g., Quail Coturnix coturnix, or between years, e.g., Crossbill Loxia curvirostra, and which also move about within their 'wintering' range. The difference from nomadism, which refers to movements of species that do not normally revisit either breeding sites or non-breeding areas, is thus one of degree and not kind. Migration has also been defined in terms of a change of habitat, but in birds this does not always occur, e.g., Oystercatchers Haematopus ostralegus may move several hundred km between coastal breeding sites on sandy beaches in northern Britain and similar wintering habitats in southern Britain. On the other hand, the definition adopted by Baker (1978) in an attempt to find one which applies to individuals of all animal species---namely 'the act of moving from one spatial unit to another'-is too general, although it avoids the need to define habitat boundaries. It would be better to exclude unintentional movements (birds blown outside their normal range) and those used in everyday foraging and roosting behaviour by restricting the term migration to movements leading to a change of home range. In bird species whose migrations involve long non-stop flights, physiological as well as behavioural changes usually occur before departure. The most marked behavioural changes occur in nocturnal migrants, particularly small passerines, which develop an additional activity rhythm during the hours of darkness, when they normally roost. Methods of observation. Information on the daily and seasonal timing of migration of species, populations and individuals, on directions, routes and distances of flight, and on flight performance has been collected by the following methods. (1) Direct observation usually of visible migration but sometimes of audible movements also (especially at night). Under favourable weather conditions for migration, many birds pass too high to be seen with the naked eye, but flights at moderate altitudes can be detected with the aid of binoculars, a method pioneered in the Netherlands to study diurnal migration of Chaffinches Fringilla coelebs. The directions of flights at lower altitudes are often influenced heavily by topography and thus may change frequently; hence it is difficult to establish preferred directions with accuracy from direct observations. (2) Seasonal timings of migration may be established by noting dates of arrival at, and departure from, the breeding and non-breeding areas. This method gives reliable information on first arrivals and last departures, but continued passage through possible breeding or wintering areas may not be detected. However, at intermediate stopovers on migration routes it has been used successfully for determining the duration of passage, particularly of night migrants. (3) Radar observations using long-range surveillance equipment, have proved complementary to those visual observations which record only low-altitude flights. They have been particularly useful for measurements of flight directions over long distances and uninfluenced by topography. Data on seasonal patterns of movement have been established chiefly for groups of species with similar flight characteristics. Recognition of individual species has not often been possible. The most detailed studies of the influence of weather on migratory departures and flight behaviour have been made with the aid of RADAR. (4) Direction offlight can be determined by watching the silhouettes of migrants crossing the face of the full (or nearly-full) moon. The method demands prolonged observation of the moon's disc through a telescope or binoculars. Identification of migrants to the specific level is rarely possible. As the method can be used effectively for at most 7 days each month, it cannot provide much information on seasonal patterns of movement and has been largely superseded by the use of radar. It has been used most successfully in the USA (Lowery and Newman 1966). In northern Europe, cloud associated with the flow of maritime air from the Atlantic often renders observation at full-moon periods impossible. (5) Marking of birds, with numbered metal rings, combinations of

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coloured rings, or plumage dyes, all of which can be used on a large scale, has provided a considerably quantity of data on migration routes, destinations and (less precisely) timing of movements. Bias in the regularity and reliability of reports from different parts of the world, however, requires results to be interpreted with caution. Nonetheless, the results can be assigned unambiguously to particular species. (6) Radiotelemetry has given detailed information on the flight tracks and movements ·of individual birds. By the early 1980s, the weight of transmitter and power pack had been reduced sufficiently to permit attachment to birds of the size of Starlings Sturnus vulgaris for migration studies, and further miniaturization of transmitters and batteries is to be expected. Because of the restricted range of frequencies that may be used and the high cost of radio-tags, most studies to date concern only 20-30 individual birds. Limited detection range also restricts the value of the technique for migration studies, but radio-tags promise to give useful data on the behaviour of migrants immediately before departure, even if the birds cannot be followed thereafter (see RADIO TRACKING AND BIOTELEMETRY) .

(7) Automated recordings of daily activity patterns of captive migrants can show when nocturnal migratory behaviour develops and for how long it continues. When the directional components of total activity have been separated, information has been obtained on preferred directions of departure of different species, and on cues for obtaining compass information (see NAVIGATION). Patterns of migration 1. Time of day. Most long-distance passerine migrants, travelling from temperate or arctic breeding areas to tropical non-breeding areas, depart an hour or two after sunset, as recorded by radar in several parts of the Northern Temperate Zone. Although they fly chiefly at night and usually land at dawn, some make non-stop flights of several days' duration over inhospitable habitats, e.g., Blackpoll Warbler Dendroica striata from North to South America over the Western Atlantic Ocean. Many primarily nocturnal migrant passerines are insectivorous during the breeding season, but they may also feed on fruits before and, in daytime pauses, during autumn migration. Most short-distance passerine migrants travelling chiefly within the Northern Temperate Zone, fly by day, often departing slightly before sunrise. But, in contrast to nocturnal migrants, they move for only a few hours in a morning before stopping to feed, unless they are aerial feeders such as Swallows Hirundo rustica, which may continue to migrate all day, feeding as they travel. Many diurnal migrants are primarily seed- or fruit-eating species, especially outside the breeding season in northern latitudes. A few of these species also migrate by night, e.g., Brambling Fringilla montifringilla. Soaring birds, including the White Stork Ciconia ciconia, and birds of prey such as the Black Kite M ilvus migrans, move chiefly during the middle of the day when thermals which assist their flight are most active. Shorebirds (Charadrii) may depart at any time of day or night, since their activity patterns are also governed by the tidal cycle. Their departures often coincide with those times when they would normally fly to high-water roosts. Exceptionally, nocturnal migrants may not leave until the middle of the night. Wave-like migratory departures from roosts several hours after dusk have been recorded by radar; they refer to Starlings leaving Britain in spring to return to breeding areas in continental Europe. Several advantages have been suggested for migration at night: the availability of more than one astronomical cue to assist navigation so that migrants may obtain directional information from fixed patterns of stars, rather than from the changing position of the sun in the sky; reduced likelihood of predation, particularly important at the end of a flight when the migrant's speed may have fallen; and improved atmospheric conditions for detection of sound signals, which may give information about terrain below the bird, or about the positions of conspecifics; also the daylight hours become available for feeding. 2. Patterns of migration in species, populations or individuals moving each year. 2a. Distances and directions. The most prominent and extensive move-

ments of land birds occur in a north-south direction. Most passerines breeding at high latitudes in the western Palearctic move towards equatorial regions of Africa during the Northern Hemisphere autumn, whereas those breeding in eastern Siberia move chiefly towards southeast Asia and Australasia (Moreau 1972). In the New World, extensive southward movements occur in autumn towards central and South America, though many species do not travel further than the southern

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states of the USA. The same pattern is broadly true of waterfowl movements in the New World, whereas in the Palearctic most species move further west than south to spend the (northern) winter in countries bordering the North Sea and the Mediterranean, and in West Africa. Autumn movements of several arctic-breeding wader species in the New World involve long south-eastward flights overland to the east coast near the Canadian/USA border, followed by southward flights to South America; others migrate southwards along the west coast of North America or make long overwater flights to 'wintering' areas on the Pacific Islands, the most spectacular flight being that of the Lesser Golden Plover Pluvialis dominicafulua from Alaska to Hawaii, a distance of about 4,000 km. Waders from Greenland fly south-east to Europe and then southwards to West and South Africa; many from Siberia, even from longitudes far to the east, move westwards in autumn to the western European seaboard. Some then continue southwards to north-west Africa. Others may fly overland from Siberia via the Caspian Sea to South Africa, whereas yet other species from eastern Asia move southwards to Australasia. Many of these long-distance routes approximate to great circles--the shortest distance between two points on the earth's surface. Seabird movements are more complex still. Within the Atlantic region, many species move primarily on a roughly north/south axis, which may also involve crossing from the western side of the North Atlantic off Canada to the western side of Africa (Arctic Tern Sterna paradisaea), or from the eastern side of the North Atlantic off the British Isles to the eastern coast of South America (Manx Shearwater Puffinus puffinus). The tern continues its movements beyond southern Africa into the Antarctic Ocean, thereby flying some 25,OOOkm on the round-trip from and to its breeding grounds. Conversely some seabirds breeding in the southern Atlantic spend the non-breeding season in Northern Hemisphere waters, e.g., the Great Shearwater Puffinus gravis, which breeds on the Tristan da Cunha group of islands and congregates during the northern summer to moult off the Newfoundland coast. Similar extensive movements occur within the Pacific, e.g., those of the Mutton Bird or Short-tailed Shearwater Puffinus tenuirostris from breeding sites in southern Australia to moulting areas in the Bering Straits. This migration follows an almost circular route, at first north and westwards to Japan and later south and eastwards along the western coast of the USA before crossing back to Australasia. Migrant land birds breeding at mid-latitudes in the Northern Hemisphere often do not move as far south in autumn as those from higher latitudes. In western Europe, the directions of most movements of passerines lie between south and west, to wintering areas in the British Isles, the Iberian Peninsula and the Mediterranean coasts and islands. In the Southern Hemisphere, which lacks extensive ice-free land masses further south than those at mid-latitudes in South America and southern Africa, most migrant species move northwards after breeding but rather few cross the Equator and none enter the Northern Temperate Zone. Some of the most extensive movements are made by aerial feeders, such as the Brown-cheeked Martin Phaeoprogne tapera from Argentina to Venezuela and central America. Within the tropics, generalizations about directions of migration are hardly possible, since many movements are associated with the alternation between wet and dry seasons. These result from the seasonal movements of air masses and accompanying belts of rains, often in different directions in different parts of the tropics. Associated with each of these weather systems, which affect flowering and fruiting of plants, may be a separate migration system, as has been documented by Ward (1971) for Quelea quelea in different parts of Africa. Short-distance movements between different altitudes also tend to occur in a variety of directions, dependent on the alignment of mountain ridges such as the Andes and the Alps. For example, the Grey-flanked Cinclodes Cinclodes oustaleti nests in the Chilean Andes above an altitude of 3,500 m and spends the non-breeding season along the sea coasts nearby. 2b. Time of year. Amongst species that migrate every year, major differences in seasonal timing occur, according to the feeding requirements of each species on the breeding grounds, the climatic zones crossed during their migrations and the timing of other events, such as moult and reproduction, in their ecophysiological cycles. Generalizations are difficult to make. Land-birds nesting in the high Arctic, north of the tree-line, usually depend upon the emergence of insects for successful reproduction; they must arrive in the Arctic late in the spring (Mayor June) and so pass through the lower latitudes well after many, including

their own, species have begun nesting there. The lower-latitude breeding species usually do not move such long distances after the breeding season, and may still be present on their breeding grounds when the higher-latitude species return in late summer and early autumn. The lower-latitude species often have protracted migration periods. Of more general relevance are situations leading to variations in timing of movements within a species. An observer may notice the occurrence of several periods of passage of the same species during a single season through a refuelling area on the migration route. These can arise in autumn in several different ways: (1) Different breeding populations may reach the same place at different dates, e.g., Dunlin Calidris alpina from Iceland and Greenland pass through the British Isles in August and September, en route for north-west Africa, whereas those from northern Russia reach the end of their migration route in the British Isles, arriving from mid-September onwards. (2) Young birds, particularly of species deserted by their parents soon after hatching, may leave arctic breeding areas many weeks after the adults. Adult Grey Plovers Pluvialis squatarola move from their breeding areas in Siberia to moulting grounds in western Europe 4-5 weeks before their juveniles reach the same areas. (3) Males and females may migrate at different times. This occurs in many shorebirds, in some of which males (and in others females) leave the breeding grounds first; also amongst certain wildfowl in which males take no part in care of their young and desert their mates once they have begun incubation, e.g., Eiders Somateria mollissima, in which males move to moulting grounds well before females. (4) Young of later broods may migrate later than those from first broods, e.g., House Martins Delichon urbica, whose second broods may not fledge until September. Indeed a higher proportion of young from later broods may be migratory, as in Great Tits Parus major in northern parts of continental Europe. (5) In single-brooded species with long periods devoted to incubation and care of the young, failed breeders may migrate earlier than successful breeders, e.g., European Shelduck Tadoma tadoma moving to their moulting grounds in north-west Germany. In addition to these situations which lead to several waves of passage, the duration of a single migratory wave may be prolonged in species with a wide spread in dates of laying, particularly those in which birds breeding for the first time do so later than experienced breeders. Some of these temporal patterns of movements are noticeable also in spring. Different breeding populations often occur at a locality on passage on different dates. Indeed, departures of different populations from a common wintering ground may take place in different months, as in the case of the races of Yellow Wagtails Motacilla flava wintering in Zaire. Males of species that defend territories during the breeding season usually return to the breeding grounds before females. Birds attempting to breed for the first time may migrate later than older birds. Indeed in some waders, e.g., Bar-tailed Godwit Limosa lapponica, immature birds may migrate towards the breeding grounds not only later than potential breeding birds, but also without completing the journey. Migrations of species within the tropics may be less predictable on a calendar basis, since the timing of the wet and dry seasons is also less predictable than that of the seasons at higher latitudes. Amongst the smaller insectivorous passerines, several species contain partially migratory populations, particularly at higher latitudes. These comprise some individuals that leave their breeding grounds each autumn and return each spring and others that are resident. In mild winters, the residents survive better than the migrants, which suffer mortality not only on the more southerly wintering grounds but also during migration; in cold winters on the breeding grounds the residents survive worse (e.g., Goldcrests Regulus regulus in Finland). Partial migrants tend to move south later in autumn but return earlier in spring than long-distance migrants breeding in the same areas (e.g. Willow Warbler Phylloscopus trochilus). 3. Patterns ofmigrationin species, populations, or individuals movingonly in someyears. Amongst the types of migrants falling into this category, the most prominent are those taking part in IRRUPTIONS. Others include those populations in which certain individuals are partial .migrants, moving in some years but not in others, or different distances in different years, albeit along the same preferred direction. The British race of RedpoUs Carduelis flammea cabaret, which utilizes the seeds of birch Betula in winter, comes into this category. Large seabirds, such as albatrosses, that attempt to breed only every other year but move away from the breeding colony between attempts, may also be considered as irregular migrants.

Migration

Finally, some species, particularly those that feed by probing in damp earth or picking prey from the surface in short grasslands (see PLOVER) may move in response to the onset of freezing conditions. These 'hard-weather migrants', like the Lapwing Vanellusvanellus and Skylark Alauda arvensis, move in directions most likely to lead them to unfrozen feeding areas, i.e., between west and south. In mild winters, no such movements take place; in other years, their timing is dictated by the occurrence of the severe weather. Functions of migration. Successful migration enhances the lifetime reproductive output of an individual, either by increasing its chances of survival or by allowing it to breed where it can rear more young than if it remained resident in another site, or for both reasons. In some species migration allows colonization of areas in which individuals could not survive throughout the year. In relation to increased reproductive performance, migration to higher latitudes provides longer hours of daylight, between the spring and autumn equinoxes, in which young can feed or be fed. This is particularly important to species such as the passerines that forage visually and not by touch, and thus are dependent upon daylight feeding. Disturbance and predation pressures from mammals may also be less at higher latitudes, since few predatory mammals can survive there through the winter. This may permit greater nesting success for ground-nesting species, e.g., shorebirds. The chances of survival of migrant individuals during the breeding season are greater in temperate and arctic areas than they would have been in the (often tropical) non-breeding areas, for reasons considered above and later. Against this must be balanced the costs of the journey. A similar equation can be drawn up for seasonal movements within tropical regions according to the timing of wet and dry seasons. In many cases, food is more abundant or more predictable in the breeding area, particularly once nesting has begun, than it would have been in the non-breeding area at the same time of year. 'Moult migrations' are also concerned with enhancing the chances of survival of the individual-in this case, normally a waterfowl. Aggregations of certain species, or sex- or age-groups, of ducks and geese occur in areas of plentiful food and/or improved protection from mammalian predators when they are at their most vulnerable, having shed all their flight feathers in rapid succession. For many species breeding in the North Temperate or Arctic regions and migrating southwards in autumn, the clemency of weather they face in the non-breeding area increases, the further it lies from the breeding area. Taken to its extreme in trans-equatorial migration, movement can eliminate the hazards of severe weather, except on the flight itself, by taking birds from the northern summer to the southern summer and back again in a single year. In species whose average life expectancy is more than a few years, individuals would be expected to produce most offspring during their lifetimes by devoting resources chiefly to survival in the early years of life and to reproductive efforts later. The longerdistance migrations of young, of species such as Black-headed Gulls Larus ridibundus from central and northern Europe, to less severe winter conditions than encountered by adults agree with such a prediction. Theoretical considerations of reproductive investments by males and females may explain why the non-breeding areas of the two sexes sometimes differ. For example, in waterfowl, females often move to safer places; in some terrestrial species, males may attempt to stay on or close to breeding territories whilst females migrate to more favourable climates. Dingle (1980) has suggested that most migrants may be 'fugitive' species, which cannot compete successfully with residents, and are displaced into marginal habitats, whose resources are less predictable in space and time than are those occupied by the residents. As in insects, successful utilization of marginal habitats can be achieved only by mobility (a biological response to adversity), so fugitive species of birds have been pre-adapted to take advantage of seasonally available resources in mid- and high-latitudes. The habitats occupied by passerine migrants in the non-breeding season tend to have transient resources-hence the itinerancy reported by Moreau (1972) in Africa. Evolution. Long-distance migration must have evolved many times in many species. Most of the migration patterns seen today, in all their variety and complexity, must have altered considerably in the last 10,000 years, since the last glaciations. (Intra-tropical movements may, however, have existed relatively unaltered for a much longer period.) The glaciations were not responsible for the origin of migrations, only for

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modifying distances moved. Many existing routes bear no relation to the geographical patterns of advance and retreat of the glaciers. However, the movement patterns of several species appear conservative. For example, although the Wheatear Oenanthe oenanthe has spread as a breeding species from the Palearctic eastwards into Alaska and westwards into Greenland, the non-breeding area has remained within Africa and birds from the outlying breeding areas rejoin those from the Palearctic on their way south in autumn. Although easier achievement of energy balance; by migrating from severe climates, may be an important advantage for some present-day migrants from high-latitude breeding areas, other species have evolved adaptations which permit survival through the worst weather in those same areas, e.g., the resident Scandinavian Yellowhammers Emberiza citrinella have thicker plumage than the migratory Ortolan Buntings E. hortulana. Hence, migration need not have evolved solely for energetic reasons. In Africa, central America and other areas used by non-breeding passerine migrants, resident and migrant species are often segregated by habitat or microhabitat. This has been taken as evidence for competition and shortage of food in the non-breeding areas, but such a deduction ignores the differences in the types of habitat used by the two groups of species. Migrants are usually found in habitats where they can utilize superabundant but erratically distributed food resources, both in time and in space. These habitats are probably unsuitable for breeding attempts for most species, unless food concentrations remain for long enough to enable completion of a breeding cycle at least once every few years. Migration may thus have evolved in the non-breeding areas by colonization of, or displacement of species into, habitats that provided adequate food for survival of nomadic individuals but were insufficiently predictable for successful reproduction; followed by further movements to temperate and higher latitudes where productivity at certain seasons was sufficiently great and predictable. These generalizations may apply only to passerines. Myers (1981) points out that both migrant and resident shorebirds present during the southern summer in coastal areas of Argentina use dependable food resources, albeit erratically distributed in space. He suggests that the migrant sandpipers that evolved in the Northern Hemisphere have failed to establish themselves as breeding species in Argentina chiefly because their densities there are so high that behavioural and competitive interactions do not allow sufficient time and resources for successful breeding. The few local breeding species of shorebirds are taxonomically and ecologically distinct from the migrants. Preparation for migration. In longer-distance migrants, two distinct phases of preparation can be identified. The first, termed Zugdisposition, is concerned with physiological preparation for the energy demands of migratory flight. The second, Zugstimmung, leads to the behavioural changes needed to initiate and maintain prolonged flight. It may involve a change in the daily rhythm and orientation of activity, under hormonal control. In caged birds, Zugstimmung is expressed as Zugunruhe (migratory restlessness), a phenomenon which has been exploited in studies of orientational preferences. Field studies of the behaviour of migrants at a refuelling area (Rappole and Warner 1976) have highlighted differences in behaviour between birds in Zugdisposuion ('feeders') and those in Zugstimmung ('flyers') within the same species. Feeders attempted to acquire territories and did not gain weight unless they did so; flyers foraged in groups and gained little weight. Flyers flocked to assist in synchronizing their departures. Physiological preparation. Fat is the main fuel used for extended flights by birds. Weight for weight, it provides more than twice as much energy when oxidized as does glycogen, the carbohydrate fuel used by many (but not all) species of migrant insects. Before migration, fat is stored chiefly in subcutaneous and visceral deposits, sometimes known as fat pads. Increase in the mass of a pad results from accumulation of fat within existing adipocytes (fat storage cells), rather than from proliferation in the number of such cells. In general terms, the mass of fat stored before a migratory flight is related to the distance to be flown, especially in terrestrial birds making obligatory sea- or desert-crossings. In species, such as the Ruby-throated Hummingbird Archilochus colubris, that migrate across the Gulf of Mexico, fat may form about 50% of the total mass of a bird before its departure. A similar load is carried by some Sedge Warblers Acrocephalus schoenobaenus migrating from the British Isles towards West Africa in autumn and by some waders leaving Britain

352 Migration

for the high Arctic in spring. The extent, if any, of the safety margin of fat carried by different species, above that required for flight to the destination in calm air, is not known. Possibly some species rely on flight with following winds to make a successful journey. Not all species begin migration with the maximum fat load they are known to carry. In spring in the North Temperate areas, many songbird migrants that move up to a few thousand km in a series of relatively short flights may set out from their 'wintering grounds' with rather small deposits of fat. This may be an adaptation to link the rate of their movement northwards with the timing of improvement in weather conditions. In autumn, long-distance migrants begin to move southwards from their breeding grounds with small fat stores, but build up reserves en route towards geographical barriers. For songbirds that change diet to include ripe berries in late summer, it becomes progressively easier for them to increase their rate of food intake, as they move south, if they start soon enough, since most fruits ripen earlier at lower latitudes. Glycogen is not an important source of energy for long flights. The chief storage organ is the liver, and the maximum quantity that has been recorded represents less than 10/0 of the total mass of a bird. However, although this and other components of the lean mass of a migrantskeleton, water and protein (chiefly muscle and gut)-do not change measurably during fat deposition in some migrant species, there are definite increases in flight muscle mass before migration in a few passerines and shorebirds, e.g., Dunlin, and of decreases in flight muscle mass, to below 'normal' levels, in several shorebirds after flights from Europe to Mauritania, W. Africa (Dick and Pienkowski 1979). Such changes in muscle mass would be expected if migrants attempted to fly at optimum speeds (see below), which should be high when they first depart and are heaviest, but decrease as they use up their fuel during flight (Pennycuick 1978). A reduction in flight speed without a change in wing-flapping rate could be achieved by reducing power output, i.e., by reducing muscle mass. Control of fat deposition. In birds, fat is synthesized in the liver and transported to the storage sites in the blood as low-density lipoproteins. The source of the increase in the rate of fat synthesis before migration is chiefly an increase in daily food intake. If food is restricted, fat deposition can be prevented in captive birds. Metabolic changes which would allow greater availability of materials for fat storage without an increase in food intake-namely, a reduction in maintenance energy, more efficient assimilation of the normal diet, or change to an 'energy-rich' diet-are not of general importance, though they have been claimed as important additional factors for a few species. Most laboratory studies have revealed that an increase in food intake precedes, or is independent of, the timing of onset of nocturnal activity in captive migrants, so that an independent means of control of food intake must be sought. Prolactin has been implicated as the hormone most heavily involved both in stimulating appetite and in increasing the rate of fat synthesis in the liver. Its effects are dependent on the time of day at which it is administered to captive birds, and circadian rhythms of prolactin release are known to occur in free-living birds. Once fattening has begun, it may produce gains of body weight of as much as 5% per day in small warblers Acrocephalus (Gladwin 1963). However, rates of use of fat during flight are much faster. Hence, unless migration is accomplished in a single non-stop flight, pauses for 'refuelling' must separate periods of flight by several days at least. Control of the timing of migration. I. Ultimate factors. Migration must be timed to bring individuals to potential breeding areas at the most appropriate times (see BREEDING SEASON). Movement away from the breeding area may be timed by the need to moult at a particular site, or to reach a certain refuelling site as soon as possible before its food resources have been depleted, or to establish a feeding site in the non-breeding area. Thus the timings of movements are ultimately controlled by the influence of seasonal fluctuations in the availability of food on reproductive success and survival. 2. Proximate factors. Since long-distance movements cannot be undertaken without adequate preparation, both physiological and behavioural, certain timing factors must operate to initiate these processes in advance of the dates when migration 'should' take place. For transequatorial migrants, the timing of start of fat deposition and migratory restlessness at the end of the non-breeding season and after breeding is controlled chiefly by an internal circannual rhythm, synchronized perhaps by changes in daylength on the breeding grounds (see

For migrants wintering in the Northern Temperate Zone, preparation for spring migration is initiated chiefly by the increase in daylength beyond a certain threshold. Preparation for autumn migration in these species may be timed as a 'carry-over' effect from the spring, since many species lose their sensitivity to photostimulation in late summer after breeding. Alternatively, they may rely on a circannual rhythm for timing of fat deposition and changes in behaviour in autumn, as presumably must the juveniles of such species. Once initiated, the rate of development of migratory condition can be modified by secondary timers such as temperature, particularly in spring. In intra-tropical migrants, whose movements are related to the alternation between wet and dry seasons, rainfall, or its indirect effects on food abundance, is most likely to act as the proximate timer. Once adequate levels of fat deposition have been achieved, weather conditions provide the 'fine tuning' to the timing of a migratory flight. There exists an interplay between the degree of physiological preparedness and the favourability of the weather in determining whether or not a migrant will depart. The effects of weather on migration have been reviewed by Richardson (in Alerstam et alI978). Particularly in spring, the rate of advance of passerine migrants is closely correlated with the northward movements of certain isotherms, which suggests that temperature, as well as the presence of following winds, may exert an important influence on departures. Once migration is underway, if migrants then land with low fat reserves, their migratory behaviour may be suppressed temporarily whilst they regain weight. However, such physiological inhibition of migration in individuals may be over-ridden by social factors in species that fly in flocks by day or that feed upon the wing. Flight performance. Pennycuick (1969, 1975) has predicted from models of the mechanics of bird flight that each individual should migrate at a speed which maximizes the range it can achieve for each gram of fat oxidized. For migrants carrying large loads of fat on departure, the maximum-range speed should decrease as fuel is used up. This awaits confirmation by radar observations. So also do a series of predictions concerning rates of climb and altitudes of flight, published by Pennycuick (1978). Body temperatures of flying birds normally lie above those of resting birds, so that cooling of the bird during migration can be considered a major problem. This is achieved by two routes-direct loss of heat by convection from the surfaces of the flight muscles and underwings, and evaporative cooling via the respiratory system. It has been claimed that water requirements rather than the size of energy reserves may limit the flight range of many migrants, but conclusive evidence is lacking. Migrants may alter the relative importance of the two routes of heat loss by adjusting the altitude at which they fly: direct convective loss increases at the lower temperatures found at higher altitudes. However, many other features are involved in choice of flight altitude. Most passerines fly at altitudes of less than 1,500 m, but at the end of a long flight over the western Atlantic birds have been recorded as high as 6,800m above the sea. It is not known whether they had adopted a 'cruise-climb' strategy on the flight from the north-eastern USA. Migrant shorebirds have been recorded at greater altitudes. Canada Geese Branta canadensis have been seen by radar to fly over the Canadian Rockies on migration. The altitudes chosen by passerines may be affected by the favourability of the wind direction if this varies with height above ground (see also FLIGHT; FLIGHT, SPEEDS OF). Most migration of songbirds takes place on a broad front, especially by night. By day, concentrations of migrants may form along 'leading lines'-topographical features marking the boundaries between habitats. Particularly effective are coastlines, if the preferred migration directions would lead landbirds over the sea. Such 'leading lines' are followed primarily when migration occurs into a headwind, for birds fly low under these conditions. Other concentrations may occur along escarpments, which may provide shelter for small passerines, or mountain ridges which provide updrafts to assist soaring birds on migration. Other groups of species may follow narrow migration routes because their areas of origin are restricted. For example, shorebirds congregate on estuaries as refuelling areas during migration. These are often well separated geographically. They then depart on narrow routes for the next section of their long-distance journeys. Flocking of migrants occurs chiefly by day-possibly as an antipredator adaptation. Although large numbers of birds migrate by night, evidence for tightly-bunched flocks is scarce, though individuals of many species call in flight, which may serve to keep loose groupings together, RHYTHMS AND TIME MEASUREMENT).

Mimicry, vocal

perhaps to assist in maintenance of the preferred direction. Even if migrants prepare adequately for flight, choose appropriate weather conditions for departure, and fly at suitable altitudes, longdistance migration will be successful for an individual only if it chooses an appropriate direction of flight. The mechanisms of orientation and navigation are dealt with elsewhere (see NAVIGATION). Two points are relevant here: (1) weather conditions at the time of departure restrict the orientational cues available for use-for example, the stars are obscured by total cloud cover; and (2) weather conditions during flight determine whether or not a migrant can maintain its preferred flight track. Strong side or headwinds may force a small slow-flying songbird to abandon its track and allow itself to be blown off course (see DRIFT). See photo RADAR. P.R.E. Most of the papers quotedin the text are referred to in: Gauthreaux, S.A., Jr. (ed.), 1980. Animal Migration, Orientation and Navigation.

New York.

Otherimportant reviewsare provided by: Alerstam, T., Enckell, P.H. & Ulfstrand, S. (eds.). 1978. Currentbird migration research. Oikos 30(2). Baker, R.R. 1978. The Evolutionary Ecology of Animal Migration. London. Berthold, P. 1975. In Farner, D.S. & King, J.R. (eds.). Avian Biology, Vol. 5.

New York. Moreau, R.E. 1972. The Palaearctic-African Bird Migration System. NewYork. Myers, J.P. 1981. In Keast, A. & Morton, E.S. (eds.). Migrant Birds in the Neotropics. Washington, D.C. Pienkowski, M.W. & Evans, P.R. 1985. In Sibley, R. & Smith, R.H. (eds.), Behavioural Ecology. Oxford.

MIGRATORY RESTLESSNESS: the unsettled behaviour of birds immediately before they are due to depart on migration, also called 'pre-migratory restlessness' or (using a German term) 'Zugunruhe' (see MIGRATION).

MILK, CROP: see CROP

MILK.

MILK, PIGEON: see CROP

MILK.

MILLERBIRD: Acrocephalus familiaris of the Hawaiian Islands (for subfamily see WARBLER (1)). MILVINAE: see HAWK. MIMESIS: same as

MIMICRY

(adjective 'mimetic').

MIMICRY: the resemblance, by evolutionary convergence, of one species to another for mutual or one-sided benefit. This phenomenon is widespread among insects but rare in birds where, however, it has not been searched for in a systematic manner. Mimicry in birds commonly involves plumage and shape, sometimes also posture, movements or voice. Cases of alleged mimicry must be carefully evaluated before drawing conclusions regarding their functional and evolutionary basis. Interspecific resemblance may be simply the expression of close relationship, or of parallel adaptations to a common environment and shared specializations. Defensive mimicry. A docile and palatable animal may evolve a resemblance to a pugnacious or unpalatable one in order to achieve protection from enemies (Batesian Mimicry). From encounters with the unpleasant species, predators learn to avoid it and, in the process, will avoid similar species, whether unpleasant or not; avoidance may also be innate. The two African forest flycatchers Stizorhina resemble almost to perfection the two ant-thrushes Neocossyphus, presumably shunned by predators because of the smell of formic acid transferred to them from their food. The 'snake mimicry' of cornered Wrynecks Jynx includes 'scaly' plumage pattern, undulating movements of the extended neck, and hissing. Brooding titmice Parus may move their necks, feign attacks and hiss like snakes toward an intruder from the darkness of their nest cavity (hence no plumage mimicry is required). In other cases, association with a pugnacious model may be a prime selective force. Examples are 5 Moluccan-New Guinea orioles Oriolus which are more dull-coloured than their continental congeners but which resemble, species for species, 5 pugnacious honeyeaters Philemon with which they share feeding sites; and 2 African black flycatchers Melaenornis, which resemble 2 pugnacious drongos Dicrurus with which they frequently associate.

353

The benefit obtained by a mimic will increase as the model becomes relatively more common. Should a model become rare, the advantage gained by the mimic will decrease, as will selection pressure in favour of resemblance. However, a highly deterrent model need not present itself very often to maintain its beneficial influence on the mimic. Several cuckoos of the genus Cuculus have evolved a striking resemblance to specific birds of prey which as a rule do not markedly outnumber the cuckoos. The main purpose of this resemblance is thought to be protection from other raptors, Whether it confers any net advantage to the cuckoos in their parasitic activities remains uncertain. Another form of defensive mimicry (called Mullerian) implies that several 'unpleasant' species converge in appearance in order mutually to reinforce their deterrent effect on a predator-a situation well known from butterflies but so far not demonstrated in birds. The concept of 'social mimicry' advocated by some authors may, however, include aspects of this kind. Aggressive mimicry. The model in this case mayor may not be a victim of the mimic. Eggs of parasitic cuckoos usually mimic those of locally preferred foster-parents. Nestling whydahs Vidua have gape patterns of the same shape and colour as their foster-siblings, species by species, which will elicit feeding by fosterers and prevent the parasite from being ejected. Similarly, nestlings of some parasitic cuckoos (the Drongo Cuckoo Sumiculus lugubris, the koels Eudynamis, the Channelbilled Cuckoo Scythrops nooaehollandiae and various Clamator species) have a plumage resembling their most frequent foster-siblings, usually drongos or crows; and young Parasitic Weavers Anomalospiza imberbis are said to mimic the plumage of young Cisticola warblers, a frequent host genus. There may also be cases where a raptor resembles an abundant innocuous species, enabling it to approach its prey unnoticed. The white morph of the Indo-Australian Goshawk Accipiter nouaehollandiae probably evolved in response to the presence in great numbers of white cockatoos Cacatua galerita. On islands where goshawks occur but not cockatoos, the white morph is absent. In this instance, the model presumably is not affected by its role in the interaction between predator and prey, since the latter does not include cockatoos. The occasional adoption by hunting Merlins Falco columbarius of a 'passerine' flight mode has also been interpreted as aggressive mimicry. The dangers of interpretation are highlighted by the case of the Zone-tailed Hawk Buteo albonotatus, whose resemblance in silhouette, flight, and plumage to the innocuous Turkey Vulture Cathartes aura may have originated as an aggressive disguise but may now serve mainly as a means of avoiding being mobbed by passerines (see also BROOD-PARASITISM; COLORATION, ADAPTIVE; MIMICRY, VOCAL). C.E. Anon. (Wallace, A.R.). 1867. Mimicry and other adaptive resemblances among animals. Westminster Review N.S. 32: 1-43. Diamond, J.M. 1982. Mimicry of friarbirds by orioles. Auk 99: 187-196. Edelstam, C. (in prep.). Mimicry in young and adultcuckoos of thegenusCuculus. Nicolai, J. 1974. Mimicry in parasitic birds. Sci. Amer. 231/4: 92-98. Sibley, C.G. 1955. Behavioral mimicry in the titmice (Paridae) and certain other birds. Wilson BulL 67: 128-132. Wickler, W. 1%8. Mimicry in Plants and Animals. London. MIMICRY, VOCAL: imitation by birds of sounds other than their specifically characteristic vocalizations. The place that the ability to imitate sounds plays in the development of the vocalizations of a species is dealt with to a certain extent elsewhere (see LEARNING; VOCALIZATION). However, the vocal performances of those birds that can not merely imitate sounds characteristic of their own species or of other species of birds but can even imitate the human voice and other sounds of non-avian origin, pose problems of quite a different order for students of animal behaviour and of phonetics. Consonant and vowel sounds. Roughly speaking, there are two types of consonant sound in human speech, the plosives (of which p, b, t, and d are examples) and the fricatives (which include f, v, and varieties of s, z, and ch sounds, all on the whole of relatively high frequency). The first group, the plosives, really involve different ways of stopping and starting sounds more or less suddenly, with more or less explosive force, and with greater or less infusion of high frequencies. Since birds in the course of producing their normal vocalizations are obviously capable of stopping and starting their sounds with extreme suddenness, we should expect them to be able to produce something like our consonants; but since their tongue, larynx, and mouth cavity are so different from ours, and since the

354 Mimicry, vocal

overall size of the vocal organs of most birds is so much smaller than ours, we should not expect sound-spectrograms of birds' voices to show more than a slight and very general resemblance between the stopped sounds of birds and those which we ourselves produce. Thus we find that the sound-spectrograms of normal bird voices do not give us any very clear evidence of distinguishing between, say, p and b, or t and d. When we come to the fricatives we find that the resemblances are a good deal closer, and we can distinguish in bird vocalizations sounds that are closely similar to a number of our own fricative consonants; it is for this reason that, when we attempt to represent the sounds of small birds in words, we find ourselves making such lavish use of the letters f, v, s, x, and z. Thus, the closest similarities between human consonants and the sounds made by birds as part of their normal repertoire are found amongst those that depend on the range and relative intensity of the higher frequencies present. When we come to the vowels, the problems posed by bird vocalizations are of peculiar interest to the phonetician. Twenty-three different vowels or vowel-like sounds are recognized in human speech. These are the incidental results of the fact that we have more than one resonator. Vowels occur whenever our throats and mouth cavities are stirred into resonance simultaneously, whether this is due to vocal cords (as in speech and song, when the sound is said to be 'voiced') or whether it is merely due to the airstream passing through both cavities, as in whispering. Four types of modulation occur in speech: (i) start-stop, (ii) vocal cord, (iii) frictional, and (iv) cavity modulation. Of these, (i) and (iii) affect the flow of air from our lungs, (ii) and (iii) convert it into audible sound waves, while (iv), broadly speaking, varies the quality of the sound. The different types of consonants discussed above are produced by differing combinations of these types of modulation but always contain (i) or (iii) or both. When pure vowels or vowel-like sounds are produced in ordinary speech, only (ii) and (iv) occur. The vocal resonances that give the vowel sounds their characteristic qualities are determined by the shapes and sizes of the resonators and are under very precise control by the movements of the lips, jaw, tongue, and soft palate; but it stands to reason that this cavity modulation will affect the sounds produced by the vocal cords very much more than those produced by frictional modulation, since the sounds produced by the vocal cords arise behind the cavities concerned whereas those produced frictionally arise in front. Talking birds. At first sight the vocal equipment of birds does not appear to have the cavities necessary to enable them to produce anything at all similar to our vowels, and examination of sound-spectrograms of bird vocalizations often shows that when we think we hear a particular vowel we may be deceiving ourselves. In some cases all that the bird seems to be doing is to change the overall pitch of the sound in the same general manner as we may change pitch during vowel production, but without producing the characteristic human resonance patterns. However, there is no doubt that some species of birds, particularly those such as parrots Psittacidae and mynahs Acridotheres spp., which can be taught to produce plausible imitations of human speech, do in fact do something more than this and can, in a manner not yet by any means understood, produce a surprisingly accurate copy of the vocal resonances hitherto regarded as peculiar to human speech. A great deal more anatomical and physiological research will be necessary before it will be possible to account fully for the talking abilities of birds, and until this further knowledge is available speculation is apt to be profitless. Quite apart from the physiological problems arising in connection with bird imitation of human speech, there are other questions concerning the evolution and biological function of this mimetic ability. Talking birds are so familiar to us that the significance of the performance has often been overlooked. No satisfactory evidence is available that either parrots or mynahs ever use their remarkable powers of imitation in the wild; these seem to lie completely latent. Within the primates we find a great variety of vocal mechanism which, it would seem, should enable some of these apes to produce excellent imitations of human speech, yet not even the chimpanzee can be taught to do this. That the birds with their entirely different and apparently much inferior vocal equipment can on occasion overcome almost perfectly the problems of phonation posed by human speech is indeed mysterious. Why these birds should learn to imitate human speech when kept in captivity is perhaps a little more understandable. Many birds such as Budgerigars Melopsutacus undulatus and mynahs learn to talk best when they are kept in close contact with human beings but away from their own kind. This is probably because, as they develop a social attachment

to their human keepers, they learn that vocalizations on their part tend to retain and increase the attention that they get, and as a result vocal production, and particularly good vocal imitation, is quickly rewarded by social contact. This seems an obvious explanation of the fact that a parrot when learning will tend to talk more when its owner is out of the room or just after he has gone out-as if he is attempting, by his talking, to bring him back. If this theory about the psychology of talking birds is correct, it makes their process of learning appear very similar to that of the human infant in its first attempts to talk. Mowrer (1950), in advancing this hypothesis, has suggested that birds and babies make their first efforts at reproducing words and other sounds because these sounds seem good to them-they are, in fact, self-stimulatory. Mothers often talk or croon to babies when attending to them, and so the sound of the mother's voice has become associated with comfort-giving measures. So it is to be expected that, when the child, alone and uncomfortable, hears its own voice, this will likewise have a consoling, comforting effect. In this way Mowrer supposes that the human infant will be rewarded for his own first babbling and jabbering without any necessary reference to the effects that these sounds produce upon others. Before long, however, he will learn that if he succeeds in making the kind of sound his mother makes he will get more interest, affection, and attention in return; and so the stage is set for the first steps in the learning of human language. In spite of all the differences, it seems hard not to believe that something of the same sort is happening in the learning of human speech by pet birds. Mimicry in wild birds. While many birds learn their songs, or at least some phrases of them, by imitation from others of their own species, it is well known that some species incorporate into their songs sounds copied from completely alien species or even sounds of non-avian origin. This tendency to mimic a wide variety of sounds can probably be regarded as a special development of the ability to learn songs from the parents or other conspecifics. It has been shown that some species that show no traces of imitation of alien sounds in their songs nevertheless include quite a number of such sounds in their sub-songs. When these sub-songs are transformed at the beginning of the breeding season into the true songs, all the sounds of alien origin are omitted. This fact will perhaps give a clue to the development of this faculty of general mimicry, for it is significant that sub-songs seem to have little or no communicatory function, whereas the songs themselves, atleast in territorial species and probably in many others too, are important in transmitting information to other members of the species about the circumstances of the singer, e.g., whether mated or not, whether established in a territory, and sometimes also constituting an individual recognition mark. There is no doubt that a very large number of species occasionally imitate alien sounds, but only very few species are good general mimics. Even in those which are renowned for their mimicry, such as the Starling Stumus vulgaris, the Marsh Warbler Acrocephalus palustris, and the Mockingbird M imus polyglottos, it is far from easy to make any estimate of how much of the vocal repertoire has been picked up in this way. It is estimated that an average male Marsh Warbler mimics 76 species (range 63-84). Of particular note is the observation that about half the mimicked species are from the Marsh Warbler's breeding area in Europe, while the other half are from its wintering grounds in Africa. As regards the percentage of total song that consists of mimicry, for Mockingbirds estimates are from s%r-18% , for Starlings about 10% and for White-eyed Vireos Vireo griseus about 53%. The robin chats Cossypha spp. are said to include some of the best mimics among African birds. Cossypha dichroa seems to interact vocally with the models: it tends to match vocalizations of species it mimics in direct response to their songs. In Australia, the bowerbirds Ptilonorhynchidae, the lyrebirds Menuridae, and the scrub-birds Atrichornithidae are all renowned as mimics; and Chisholm (1937) has pointed out that it is the ground-living members of these and a number of other families in Australia that are most skilled and persistent in their mimicry. Marshall (1950) points out that most vocal mimics in Australia are strongly territorial (although not necessarily using their vocalizations in territorial defence), and that most of them carry out much of their mimicry near the ground in wooded country where visibility is limited. He suggests that the lack of visibility places a premium on communication by sound. A number of hypotheses have been put forward to account for the biological significance of mimicry, all of which may be correct, since mimicry probably serves a variety of functions in different species. (a) Mimicry is a method of acquiring a large repertoire. There is some evidence that variety in bird song is attractive to females (an 'acoustic

Moa

peacock's tail') and mimicry may simply be a way of increasing repertoire size. In one study of Mockingbirds there was some evidence that individuals with larger repertoires paired earlier. (b) Mimicry is important in interspecific territoriality. Some species mimic many of their competitors (e.g. Cossypha dichroa) and may use their mimicked song in interspecific territoriality. (c) Mimicry as a form of deception. The Thick-billed Euphonia Euphonia laniirostris is reported to mimic the mobbing calls of other species nesting near its breeding site, thus inducing them to mob predators while the Euphonia retreats to a safe distance. It is possible that there are other examples of mimicry used to deceive competitors, rivals or predators, but as yet there is no convincing evidence for this. (d) Mimicry in reproductive isolation. The parasitic Paradise Whydah Vidua paradisea learns part of its song by mimicking>that of the host species Pytilia. Song in Vidua plays a role in mate attraction, and it appears that a female prefers to approach Vidua males singing the song of the fosterspecies by which she was reared. Thus song learning ensures that the brood parasites selectively mate with individuals reared by the same hosts, thereby maintaining host-specific reproductively isolated parasite species. W.H.T. (J.R.K.) Baylis, J.R. 1982. Avian vocal mimicry: its function and evolution. In Kroodsma, D.E. & Miller, E.H. (eds.). Acoustic Communication in Birds, vol. 2. Pp. 51-83. New York. Chisholm, A.H. 1932. Vocal mimicry among Australian birds. Ibis (13 ser.) 2: 605-624. Chisholm, A.H. 1937. The problem of vocal mimicry. Ibis (14 ser.) 1: 703-721. Dobkin, D.S. 1979. Functional and evolutionary relationships of vocal copying phenomena in birds. Z. Tierpsychol. 50: 348-363. Dowsett-Lemaire, F. 1979. The imitative range of the song of the Marsh Warbler Acrocephalus palustris with special reference to imitations of African birds. Ibis 121: 453-468. Harcus, J.J. 1977. The function of mimicry in the vocal behaviour of the chorister robin. Z. Tierpsychol. 44: 178-193. Marshall, A.J. 1950. The function of vocal mimicry in birds. Emu 50: 5-16. Morton, E.S. 1976. Vocal mimicry in the thick-billed euphonia. Wilson Bull. 88: 485-487. Mowrer, a.H. 1950. Learning Theory and Personality Dynamics. New York. Robinson, F.N. 1975. Vocal mimicry and the evolution of bird song. Emu 75: 23-27. Thorpe, W.H. 1961. Bird Song: the Biology of Vocal Communication and Expression. Cambridge.

MIMICS: sometimes used as a general term for the Mirnidae. MIMIDAE: a family of the Passeriformes, suborder Oscines; MOCKINGTHRUSH.

MINER.: substantive name of Manorina spp. (see HONEYEATER).

MINER (alternatively MINERA): substantive name of Geositta spp. (see OVENBIRD (1)).

MINERAL REQUIREMENTS: see NUTRITION. MINIVET: substantive name of Pencrocotus spp. (see CUCKOO-SHRIKE). MINLA: substantive name of the 2 species of Minla of south-east Asia (see BABBLER). MIOMBO: an environment, consisting of sparse leguminous woodland (Brachystegia), characteristic of large parts of south-central Africa. MIRROR: a white spot on the otherwise black wing tip of certain species of gulls (Laridae). MISTLETOEBIRD: Dicaeum hirundinaceum (see FLOWERPECKER). MIST NET: see TRAPPING. MITES: see ECTOPARASITE. MITOSIS: ordinary cell-division, without reduction in the number of chromosomes (see CELL). MOA: substantive name of the species, all extinct, of the family Dinornithidae, order Struthioniformes, suborder Apteryges.

355

The moas were wingless, cursorial birds, of moderate to very large size, endemic to New Zealand; a moa bone found in Australia is now believed to have been taken there from a New Zealand site by man (Scarlett 1969); fossil remains are extremely rare, virtually all the abundant material so far discovered being of Post-Glacial age; the living birds were hunted by the prehistoric Maoris, and extinction became complete only within the last few centuries. Examples of the largest species, Dinornis maximus, estimated to have stood more than 3m high, were the tallest, though not the heaviest, birds ever known, being exceeded in mass by the largest Dromornithids and some Aepyornithids. Discovery. In the early years of European exploration in New Zealand there is no unequivocal evidence that the Maoris had any memory of the former existence of giant birds, or that they had a name for them, although the archaeological record proves that their ancestors were hunting moas only a few hundred years previously. The name 'moa' did feature, but only very rarely, in a few Maori traditions, but there was no clear indication of what it meant, beyond that it implied some kind of monster, man or bird. After Europeans had found bones of giant, extinct birds, the name 'moa' (the widespread Polynesian word for 'chicken') was applied to these birds. Specimens of moa bones were first exhibited and described by Richard Owen, who was shown, in 1839, the shaft of a femur brought to England by Dr John Rule. Owen's verdict was that the femur indicated the existence in New Zealand of a large struthious bird, probably as large as the Ostrich Struthio camelus. With more material received in the next few years, he was soon able to elaborate his descriptions and referred to his genus, Dinornis, 6 distinct species. These descriptions were further elaborated over a period of nearly 40 years (Owen 1879). Notable subsequent reviews are those of Hutton (1892), Archey (1941) and Oliver (1949) who listed 27 species in 7 genera. Cracraft (1976) suggested a considerable reduction to 13 in 6 genera. Acceptance of this proposal depends largely on whether marked variations in skeletal size reflect real specific differences or simply sexual dimorphism. More recently Millener (1981, 1982) has merged 2 of the species admitted by Cracraft, thus indicating that only 12 species should be considered valid. All classifications have agreed in regarding moas as 'ratite' birds (see EARLY EVOLUTION OF BIRDS), and this assumption has not been challenged except by theoretical inference. Despite earlier suggestions of a polyphyletic origin for the group, there is now overwhelming evidence for monophyly (reviewed in Sibley and Frelin 1972). Within the ratites the moas appear to be most closely related to the kiwis (Apterygidae) and perhaps more distantly to the Aepyornithidae (see ELEPHANT-BIRD). Their closest non-ratite relatives are possibly the Galliformes (Cracraft 1973). Evolution. The ancestry as well as virtually the entire evolutionary history of the moas is largely speculative, as their fossil record is sparse. The most abundant remains are Holocene in age, some are undoubtedly Pleistocene, but none are, other than tentatively, of Pliocene age or older. It can be reasonably assumed, however, that the moas developed from volant ancestors of southern continental (Gondwanaland) distribution and that flightless ancestors of the moas were present (see FLIGHTLESSNESS) on the New Zealand landmass at the time of its late Cretaceous (c. 80 million years BP) separation from Gondwanaland. Adaptive radiation in the moa lineage presumably began in the earliest Tertiary but, as noted by Cracraft (1976), the remarkably diverse Holocene assemblages most probably resulted from a later, Pleistocene, radiation. The changes in landform, climate and vegetation during the Pleistocene, more marked and more rapid than any in the Tertiary, while stimulating adaptive radiation, must almost certainly have effected extinctions amongst the Tertiary forms. The radiation of the moas, obviously strongly favoured by the absence of mammalian predators, is paralleled by the faunas of a number of other oceanic islands and indeed within New Zealand by a number of other avian families, notably the Rallidae. Deposits. The oldest known moa remains are a very few, isolated bones found in marine deposits of ?Pliocene and Pleistocene ages. The oldest radiometrically dated remains in terrestrial deposits are of late Pleistocene age (McCulloch and Trotter 1979). All recognized species, however, occur in Holocene deposits. The largest deposits of moa bones are found in situations that indicate death from natural causes, accumulation having continued over a long period. The richest deposits have been found in swamps where huge mixtures of bones prevented much identification of individual skeletons,

356 Moa

and attempts to assemble them resulted in many mistakes in the early descriptions of supposed species. An important swamp deposit found in 1937 at Pyramid Valley, Canterbury, has provided numerous individual moa skeletons associated with 3. considerable variety of other avian remains. Sand dune deposits, especially in the far north of the North Island, have yielded abundant moa and associated faunal remains of Holocene age. Caves have frequently provided well-preserved individual skeletons while those in drier regions have also produced dried integument and feathers (Buller 1888). Significant finds, especially of moa footprints, have been made in river deposits and in the early days of European settlement, when large areas of forest and scrub were being cleared, skeletons were found on the surface of the ground. The wealth of material from these predominantly Holocene deposits is such that it is likely that all those species of moa which survived the Pleistocene are now known. We still, however, know nothing of the earlier Tertiary forms. Moa bones are common in early archaeological sites from one end of the country to the other. They are, however, rarely intact, having been broken up by the Maoris to make bone fishhooks and other artefacts. The largest, and greatest number, of these 'moa-hunting' sites are along the coast, especially at river mouths, but sites also occur inland, even in the high country of the South Island. At least two early prehistoric rock drawings in Canterbury show birds that can be identified as moas with reasonable certainty. Reconstruction. Interpretation of plentiful bones, quantities of eggshell, a few unbroken eggs, a few feathers and pieces of skin, some gizzard contents, occasional footprints and, of course, associated faunal and floral remains provide substantial clues to the habits and habitats of moas. The general robustness of the bones of moas and especially the relative lengths of their hind limb elements indicate that most were sturdy and slow-moving. Even the most lightly-built would appear to have been far more ponderous than any of the extant savanna-dwelling ratites. Superficially the birds probably had the looped neck stance of emus Dromaius and cassowaries (Casuariidae) rather than the erect carriage of the Ostrich and rheas (Rheidae). Surviving feathers, at least of Megalapteryx, are less 'degenerate' than the norm for struthious birds. They have aftershafts but no barbules and some show vane pigmentation (purplish black centres with golden buff edges). Eggshell, which is usually white and occasionally pale green, is not abnormally thick for the size of the eggs. Moa nests, presumed to be those of Anomalopteryx, were discovered by Hartree in two North Island districts. All contained single eggs or chicks in scoop nests on sheltered ledges or cavities. Buller, however, produced evidence of a brood of 4 in Dinornis robustus. Ecology. Whenever moa remains have been found, the associated fauna and flora are indicative of a forest habitat, as is only to be expected in the light of New Zealand's vegetational history (see Fleming 1979). Only in alpine and recently active volcanic zones and, during the Pleistocene, in isolated periglacial regions, can there have existed extensive grassland. Moas appear to have been entirely herbivorous, berries, seeds and shoots of a wide variety of forest trees having been found as gizzard contents (Burrows 1980), suggesting a close analogy to the browsing, forest-dwelling cassowaries of New Guinea and north-eastern Australia. Collections of gizzard stones of various, most frequently quartzose, lithologies have been found. Distribution. Five of the 6 moa genera, but only 4 of the 20 or so species were common to both North and South islands. This dichotomy, into what are in many cases North Island-South Island 'species-pairs', is doubtless the result of the two islands having been effectively isolated from each other since the Post-Glacial inundation of Cook Strait some 10,000 years ago. On neither island, however, does anyone species appear to have been restricted to a particular altitudinal or geographic zone, although both Megalapteryx and Anomalopteryx have not commonly been found in coastal sites, and some of the larger species are rare in steeper country. Generally, however, moa bone deposits, wherever they occur, yield a considerable variety of species. The finding of moa remains predominantly in lowland or coastal sites (both natural and archaeological) has led to the assumption that moas were most abundant in these regions. It is more probable that this distribution simply reflects the distribution of sites in which moa remains were most readily preserved. Indeed there were probably few areas in

New Zealand, except perhaps the most mountainous, that were not at some time inhabited by moas. The occurrence of the remains of many different species of moas in a single site has, on the assumption that all were deposited at essentially the same time, been taken to indicate that these many species shared the same habitat. However, the time it may have taken for such deposits to accumulate has been a factor all too often overlooked. As a result, excessive estimates of population density and extravagant theories of catastrophism have often been invoked to explain accumulations which more probably have resulted from prolonged and intermittent deposition. Extinction and the impact of man. All the moa genera known have been found in archaeological sites, so that moas clearly were widespread when New Zealand was first colonized by prehistoric Man from East Polynesia about 1,000 years ago. All the moas were extinct or extremely rare by the time of European settlement which occurred in the years following Cook's first visit of 1769. The exact date of moa extinction will always be hard to define, but the latest radiocarbon dates for archaeological sites containing any number of moa skeletons suggest that the 15th century AD was the last time that moas were at all numerous; and that by 1800 AD they were extinct or virtually so. Because all the known moa genera became extinct in the short period of prehistoric settlement, it is likely that the arrival of man was an important factor in their demise. It is clear from archaeological evidence, particularly in the South Island, that moas were hunted extensively. Moas must also have been seriously affected by the widespread burning of forest which accompanied the spread of the prehistoric population. However, large areas in the remoter parts were never seriously disturbed by prehistoric hunting or burning, so that the disappearance of the moa cannot everywhere be ascribed to the direct effect of man. It is possible that natural environmental changes were also detrimental, although the fluctuations of the Holocene were never as drastic as those of the Pleistocene, which the moas had previously survived. The prehistoric introduction of the Polynesian rat Rattus exulans and the domestic dog may also have affected the moas. Possible survival into the 19th century. The discovery, in an excellent state of preservation, of bones of an individual Megalapteryx in an open fireplace in a rock shelter near Lake Te Anau led to the suggestion that this bird was hunted by Maoris in the period after European settlement. In the absence of radiocarbon dating this conclusion is highly speculative, as the state of preservation of bones cannot be taken as a reliable guide to age. It is quite clear that none of the largest species were ever seen by Europeans, but there is a possibility that at least one of the smaller ones, Megalapteryx didinus, still survived in the southern province of Otago into the early part of the 19th century. Sealers from Foveaux Strait were in the habit of spending many months in the south-western fiords and living off the land. Most of the birds they described to F. Strange in 1852 are recognizable, except a larger one which they called 'the fireman', because of a call reminiscent of the wooden rattles carried by firemen on duty. Maori informants about the same time frequently referred to kiwis and to a larger bird which they called the Roa. European lexicographers have since attached this name to one of the larger kiwis, Apteryx haasti, but this species does not and apparently did not occur in the south-western area, and there is a possibility that the Roa was in fact a small moa. Among reported direct observations by Europeans, one of the most arresting is that given in her later years by a Mrs Alice McKenzie of South Westland. As a child of 7, about the year 1880, she claimed to have seen a large bird of dark bluish plumage standing close to her. It was about 1m in height, and her clearest recollection was of its large protruding eyes, broad beak, and powerful scaly legs. Classification. The following classification, adapted from Archey (1941), Oliver (1949), and Scarlett (1972), represents the more traditional diagnosis of the group. Order DINORNITHIFORMES Family Dinornithidae Genus Dinomis Owen-6 species, 3 in each island. Family Emeidae Subfamily Anomalopteryginae Genus Anomalopteryx Reichenbach-2 species, the larger in both islands, the smaller only in the North Island.

Mocking-thrush

Genu s Me galapreryx Haast-2 species, the larger in both islands but very rare in the North Island. The smaller, rare and confined to the South Island . Genus Pachyomis Lydekker--4 species, the largest in both islands alth ough very rare in the North Island ; 2 confined to the North Island and the fourth known only from the unique South Island holotype . Subfamily Emeinae Genus E17UW Reichenbach-I species, prob ably confined to the South Island . Genus Euryapteryx Haast--4 species, the largest in both main islands and from cultural deposits onl y on Stewa rt Island , th e others confined to the No rth Island .

In the classification proposed by Cracraft (1973, 1976), a single order , Palaeognathiformes, encompasses the tinamous and ratites , with the moas occupying 6 genera within a single family (Dinornithidae). Cracraft admits only 4 species in Dinomis, 2 each in Anomalopteryx, Megalapteryx, P achy om is and Eu ryapteryx ; and one in E meus. Millener (1981, 1982) has shown that only the one species A. didiformis is admissable in the genus Anomalopteryx , (R.A.F.) R.].S .C. and P.R.M . Archey, G. 1941. The Moa , a stu dy of the Dinornithiforme s. Bulletin of the Auckland Institute and Museum No. I: 1-145 . Buller, W .L. 1888. A History of the Bird s of New Zealand . 2nd edn , London . Burr ows, C.] . 1980. Some empirical information concerni ng the diet of moas. New Zealand Journa l of Ecology 3: 125-130 . Cracraft , ] . 1973. Phylogeny and evoluti on of the ratite birds. Ibis 116: 494-521. Cracraft, [ . 1976. The Species of Moas. Smithsonian Contributions to Palaeobiology 27: 189- 205. Fleming, C. A. 1979. T he Geological History of New Zealand and its Life. Auckland . Hu tton , F .W . 1892. The moas of New Zealand. Tr ansactions of the New Zealand Institute 24: 9~J72 . McCulloch , B. & T rotte r, M.M . 1979. Some radiocar bon dates for moa remains from natural deposits. New Zealand Journal of Geology and Geoph ysics 22(2): 277-279. Millener , P.R. 1981. The qu aternary avifauna of the No rth Island , New Zealand . Ph .D. thesis Univ ersi ty of Auckland . Millener , P.R . 1982. And then there were twelve: the taxonomic status of Anomalopteryx oweni (Aves: Dinorn ith idae). Noto rnis 29(3): 165-168. Oliver , W .R.B. 1949. T he moas of New Zealand and Austr alia. Bulletin of th e Dominion Museum No . IS: 1- 206. Owen, R . 1879. Memoirs on the Extin ct Wingless Bird s of New Zealand . 2 vols. London (Collected paper s of 1843 et seq. ). Scarlett , R.] . 1%9 . On th e alleged Queensland Moa, D inom is queenslandiae de Vis. Memoirs of the Queensland Museum 15(3): 207-2 12. Scarlett , R.] . 1972. Bones for the Archa eologist. Canterbury Museum Bulletin 4: 1-68. Sibley, C.G. & Frelin, C. 1972. Th e egg-whit e pr otein evidence for Ratite affinities. Ibis 114(3): 377-387 .

MOBBING : term used for collective and noisy demonstration (see DISTRACTION BEHAVIOUR) against a predator by birds of one or several

Herring Gull Larus argenuuus mobb ing White Stork s Giconia ciconia . (P hoto: E.] . Hosk ing ).

357

species. Thi s behaviour is typically shown when small passerines surround a perched owl in daytime and when a part y of hirundines pursue a hawk. Only rarely is the predator actually struck by the mobbing birds. MOCKINGBIRD : see MOCKING-THRUSH. MOCKING-THRUSH: general term for the 33 species comprising the Mirnidae (Passeriformes, suborder Oscines), consisting of the mockingbirds and their allies, though not used as the substantive name of any of the species. (D onaeobius atricapillus, formerl y known as the Blackcapped Mocking-thrush, is now considered to be an aberrant wren (see WREN ( I) ) . The name 'mockingbird' is used for the 13 members of the genus M imus (including N esomimus), the 2 blue mockingb irds of the genus Melanotis and the monotypic genus Mimodes. The name 'thrasher' is used for the 10 members of the genu s Toxostoma as well as the 2 members of the genus Margarop s, and the monotypic genera Rhamphoeinelus, and Oreoscoptes. The members of the monotypic genera Dumetella and Melanoptila are known as 'catbirds'. The monotypic C ineloeerthia is known as the 'trembler', owing to its habit of vigorously quivering its wings during most intra- and inter specific social interactions. Characteristics. This New World group is related to the thrushes (T urdinae), and nearly all are suggestive of them in appearance , especially the 2 Margarops thrashers and the 2 catbirds. The y range from 20-33 em in length . The y have rounded , short wings characteristic of birds that do not fly extensively. The relatively long-winged arboreal Margarops thra shers are exceptions. Most have long tails. The bill is strong, medium to long, and in many species, especially the thra shers of the genus Toxostoma , is slightly to strongly decurved. Most species are shades of white, grey and/ or brown, the exceptions being the blue mockingbirds and the iridescent Black Catbird M elanoptila glabrirosrris. Many have white areas in the wings and on the tips of the tail feathers. Dark spots are found on the vent ral surfaces of various thrashers and several of the mockingbird s. The crissum (under tail coverts) of several species exhibits contrasting coloration, ranging from the chestnut of the Grey Catbird Dumetella earolinensis and the Crissal Thrasher Toxo sroma erissale to various shades of reddish-brown in other thrashers and mockingbirds. The mocking-thrushes are very varied in ecological adaptation for such a small number of species. Several, notably the 2 catbirds, are structurally quite like many other unspecialized brush-dwelling insectivorousfrugivorous thrushes. However , the group also includes the Trembler C incloeerthia ruficauda, which with its elongated cranial structures, short legs, reduced sternum, narrow interorbital structures, and eyes oriented for close binocular vision, is adapt ed to probing arboreal epiphyte s. The Margarops thrashers have developed powerful pectoral systems adapting them for much flying in their arboreal habitat. A particularly interesting group of specializations is found in the 10 Toxostoma thrashers. Evolutionary stages leading to powerful pelvic systems, reduction of the pectoral system, including the length of the wings, and modification of skull structural relationships, including lengthening and increased curvature of the bill, have been demon strated. The species exhibiting the least degree of modification are the Brown, Long-billed and Cozumel Thrashers (T . rufum , T . longirostre, and T . guttatum ). The most extreme modifications are found in the Le Conte 's, Crissal and California T hrashers T . lecontei , T . erissale, and T . redivivum ), species which are weak flyers, and are specialized to search for invertebrates by hoeing soft desert soils and litter with their long decurved bills. Habitat. T ypical member s of the group are either largely terrestrial or dwellers of thickets , brush or low trees. Distribution. The mocking-thrushes can be divided into 2 major groups. The larger includes the mockingbirds of the genus Mimus , which range from southern Canada through northern Central America, the West Indies , through non-rain-forest areas of South America to T ierra del Fuego , and the Galapagos Archipelago where the 4-member endemic superspecies M imus (formerly Nesomimus) trifa sciatus is found. Thi s first group also includes 2 rnonorypic genera, Oreoscoptes montanus of western North America and Mimodes gray soni, found only on Socorro Island in the Revillagigedo Archipelago off the west coast of Mexico. Evidence suggests that both these species are closely related to M imus and the English name of the latter has been changed to Socorro Mockingbird. Also included in this section of the family are the 10 thrashers of the genus Toxostoma which are confined to the United States and Mexico, the

358 Mocking-thrush

performed by the female. In some, the male assists. Both parents feed the young, which fledge in about 13 days. In some species, nest helpers have been observed. Social organization during the breeding season is monogamous and territorial. (A.H.M.) I.L.G. Engels, W.L. 1940. Structural adaptations in thrashers. Univ. Calif. Pubs. Zool. 42: 341-400. Grant, P.R. & Grant, N. 1979. Breeding and feeding of Galapagos Mockingbirds, Nesomimusparoulus. Auk 96: 723-736. Gulledge, ].L. 1975. A study of phenetic and phylogenetic relationships among the mockingbirds, thrashers and their allies. Unpub. Ph.D. thesis, City Univ. N.Y., N.Y. Univ. Micro. 75-21328. Michener, H. & Michener, ] .R. 1935. Mockingbirds, their territories and individualities. Condor 37: 97-140. Zusi, R.L. 1969. Ecology and adaptations of the trembler on the island of Dominica. Living Bird 8: 137-164.

MODE: see BIOSTATISTICS. MOHO: alternative name of the Oriole Babbler Hypergerus atriceps (for subfamily see BABBLER). MOHOUINAE: see WARBLER,

AUSTRALIAN.

MOLLYMAUK: sailors' name, with several variants, for the smaller species of Diomedeidae (see PETREL); also applied to some other sea birds. Northern Mockingbird Mimus polyglottos, (R.G.).

MOLT: American spelling of MOULT.

Grey Catbird of North America, and the Black Catbird which is found only in coastal Central America from Yucatan to Honduras. The second group includes the Blue Mockingbird Melanotis caerulescens of Mexico, the Blue and White Mockingbird M. hypoleucus of southern Mexico and Central America, and 3 West Indian endemic species, the Pearly-eyed Thrasher M argarops fuscatus, the Scaly-breasted Thrasher M. fuscus and the Trembler Cinclocerthia ruficauda. The endangered West Indian endemic species, Ramphocinclus brachyurus, although clearly a mocking-thrush, cannot unequivocally be associated with either of the two major groupings. Movements. Migration is well developed in some species that breed in temperate zones. Food. Invertebrates and various fruits are the principal foods. Behaviour. During the non-breeding season, some species (Mimus paruulus and Ramphocinclus brachyurus) move about in small groups, possibly families. Group territories are sometimes defended. Individual Northern Mockingbirds Mimus polyglottos will often defend a favourite food source during winter months. Mockingbirds are often extremely aggressive in defending the area about the nest, vigorously attacking and striking predators in their efforts to drive them away. Voice. The mocking-thrushes are renowned for vigorous and versatile song. Nearly all are continuous singers. In most, the songs consist of a wide variety of syllables which are assembled into species-characteristic phrases, the detailed patterns of which are often highly varied. Some members of the group, especially the mockingbirds and notably the Northern Mockingbird, are excellent mimics. The degree of mimicry varies widely among individuals, ranging from slight in many birds to extensive in a few. Mockingbirds typically incorporate mimicked sounds, syllables, and songs into their own species-characteristic song patterns. The Northern Mockingbird, for example, usually repeats the model 2-4 times as it does its own sounds. Night singing is prominent during the breeding season and, in members of the genus Mimus, song may continue as the bird flies up and flutters above its song perch. The Sage Thrasher Oreoscoptes montanus sings on the wing as it circles over its treelees sagebrush plain habitat. Breeding. Nests are typically placed in bushes or dense trees and are open cup-like structures, sturdily built of twigs, often incorporating leaves, and lined with rootlets and hair. The Pearly-eyed Thrasher prefers holes in forest trees. Eggs number 2-5, rarely more, the greater numbers occurring in some individuals of species living in high latitudes, the smaller numbers occurring in tropical species. The ground colour of the eggs ranges from pale whitish-blue to intense blue-green. The mockingbirds (Mimus and Mimodes), the Sage Thrasher, and the Toxostoma thrashers generally have spotted eggs. The eggs of all others are unmarked. In most species, incubation lasts about 13 days and is

MOMOTIDAE: see CORACIIFORMES;

MOTMOT.

MONAL: substantive name of Lophophorus spp. (see PHEASANT). MONARCH: substantive name of several species of monarchine flycatchers (see MONARCH FLYCATCHER).

Black-faced Monarch Monarcha melanopsis. (N. w.e.).

MONARCH FLYCATCHER and allies: substantive name of family Monarchidae (Passeriformes, suborder Oscines). This group, though in the main distinctive, remains to be clearly circumscribed and defined, particularly in anatomical terms. Boles (1981) regarded it as a subfamily, Myiagrinae, of the Pachycephalidae, together with the Australo-Papuan robin-flycatchers (Petroica spp.) and whistlers, Pachycephalinae. The nucleus of the group consists of the Indo-Pacific and Australian genera Monarcha, Arses, Pomarea, Neolalage, Clytorhynchus, Chasiempis, Metabolus, Mayromis, Myiagra, Hypothymis and Philentoma, the African 'Trochocercus' (probably an artificial genus) and the Afro-Indian Terpsiphone, some 87 species. To these have been added the African fantail-like Elminia and Erythrocercus (Traylor 1970); the fantails themselves, Rhipi-

Moon-watching

359

duridae, are here given family status but see Beecher (1953), Boles (1979). Other genera that have been referred to this group include the somewhat drongo-like Peltops of New Guinea, the Indo-Malaysian Hemipus (currently in the Campephagidae), the mudnest-building Pomareopsis and Grallina (Grallinidae), and the egregious Fijian Silktail Lamprolia. The association with the monarchs of the Australo-Papuan boat-billed flycatchers Machaerirhynchus has been questioned by Storr (1958). Certain other African genera included in the Monarchidae have been removed by Traylor (1970), Platysteira, Batis and relatives to the Platysteirinae, and Hyliota and Stenostira to the Sylviidae (see also Pocock 1966, and Beecher 1953). Characteristics. The body is of general passerine proportions (overall length I2.5-20cm, but see Terpsiphone, below), though with a tendency for relatively short tarsi and a relatively long tail. The wings are moderately long and pointed, the tail squared or rounded (strongly graduated in Machaerirhynchus, forked in Peltops); the tarsal envelope laminiplantar; the bill with a tendency in some species for dorsoventral flattening (pronounced in Machaerirhynchus and Myiagra ruficollis), with slight terminal hook and subterminal notch usually present on upper mandible, and gape usually armed with rictal bristles. The nostril is rounded, usually exposed, and open (slightly lidded in Peltops). Other modifications to external morphology include crests or incipient crests (e.g. Terpsiphone, 'Trochocercus", Hypothymis), nuchal frills (Arses), long streamer-like median rectrices (Terpsiphone) and blue eye-wattles (Arses, Terpsiphone, Hypothymis). The plumage is most often in combinations of grey, blue, black (often glossed), white, rufous and brown, though sometimes largely or wholly one of these; less frequent combinations include black and yellow (Monarcha chrysomela), black, white, olivegreen and yellow (Machaerirhynchus) and black, white and red tPeltops). Many species are strongly sexually dimorphic; the young are wholly or largely unspotted. Legs and bills are grey-blue to blackish and blackishbrown, irides usually dark brown (orange or red in Peltops). Distribution, habitat and movements. The typical monarchs inhabit the Oriental, Australasian and Afrotropical regions; they are notably well-represented in the Pacific, where several endemic genera occur. Habitats range from primary rain-forest and second-growth through open woodland to shrub savanna. Tropical and subtropical populations may be sedentary or, in the case of higher-altitude breeders, descend to the lowlands after breeding; some populations of high latitudes migrate to lower latitudes after breeding, e.g., southern Australian populations of the Leaden Flycatcher Myiagra rubecula and Black-faced Monarch Monarcha melanopsis, and northern Indian populations of the Paradise Flycatcher Terpsiphone paradisi. Food. Chiefly insects: dragonflies, termites, grasshoppers, bugs (including cicadas and lerps), beetles, flies, butterflies and moths (including caterpillars), bees and ichneumon wasps, also spiders. In addition the Shining Flycatcher Myiagra (Piezorhynchus) alecto of waterside thickets takes isopod crustaceans, tiny shellfish and crabs, the Restless Flycatcher M. (Seisura) inquieta worms and centipedes, and the Spectacled Monarch Monarcha trivirgata small snails. Behaviour. Monarch flycatchers are usually solitary or in pairs, sometimes family groups; some species also noted in mixed feeding parties. Most species hunt by moving briskly through the foliage of trees, shrubs or herbage, flicking wings and fanning tail in the manner of FANTAILS, presumably to dislodge their prey; many also catch flying insects in aerial sallies (a habit not pronounced in Monarcha, however). Variations of these methods occur. The 2 species of frilled monarchs (Arses), for instance, habitually climb up and down the trunks of trees flushing insects from bark-crevices; the Shining Flycatcher has been observed creeping along near the ground among mangrove roots or swamp-litter; and the Restless Flycatcher hunts mainly by flying slowly over open ground and hovering above its prey before pouncing. As in the fantails, prey too large to be swallowed whole may be held under the foot and eaten piecemeal. Displays are not well-documented. Species with crests, incipient crests, nape-tufts or nuchal frills will raise these when excited. Courtship display observed in male Paradise Flycatcher consists of a slow rising and dropping flight with long tail-streamers undulating. Group-displays

Azure Monarch Hypothymis azurea); songs of others are described as a series of simple whistles (Myiagra), slow rattled ringing trills (Arses), a musical jumble of loud mellow notes and fluting whistles (Monarcha) and a low pleasant rising and falling warble (Terpsiphone). Breeding. Nests are cup-shaped, mainly of vegetable matter, often bound with spiderweb and adorned with cocoons, lichen and bark; usually supported from beneath, on a horizontal branch (e.g., Myiagra) or in a vertical fork (e.g., Monarcha, Mayrornis) at heights from I-20m, exceptionally partly or wholly suspended by rim (Arses, Erythrocercus, and apparently, Machaerirhynchus and Peltopsi. The 2-4 eggs are whitish or very pale pastel shades, spotted and blotched with reds, greys and browns, in two chief types of distribution: (a) marked more or less uniformly over the shell, e.g., Monarcha, (b) markings concentrated in wreath, e.g., Myiagra, Elminia. Whether this variation is of taxonomic significance remains to be determined. Incubation lasts 14-17 days; the young fledge after 12-18 days according to species. Where information is available, both sexes build the nest, incubate, and feed the young; in some the female does most of the nest-building and incubating, but the male has been recorded as doing most of the building in Machaerirhynchus jlaviventer. S.A.P.

observed in Arses and Machaerirhynchus. Voice. Calls are short and simple, the quality variously described as dry, grating, harsh, rasping, buzzing or scolding, the notes often with a rising inflexion. Some species are not recorded as possessing a song (e.g.,

necessary to the performance of a given course of instinctive behaviour' (W.H. Thorpe).

involving repeated chasing or following within a restricted area have been

Beecher, W.J. 1953. A phylogeny of the oscines. Auk 70: 270-333. Boles, W.E. 1979. The relationships of the Australo-Papuan flycatchers. Emu 79: 107-110. Boles, W.E. 1981. The subfamily name of the monarch flycatchers. Emu 81: 50. Iredale, T. 1956. Birds of New Guinea, 2. Melbourne. Olson, S.L. 1980. Lamprolia as part of a South Pacific radiation of monarchine flycatchers. Notornis 27: 7-10. Pocock, T.N. 1966. Contributions to the osteology of African birds. Ostrich Suppl. 6: 83-94. Storr, G.M. 1958. On the classification of the Old World flycatchers. Emu 58: 277-283. Traylor, M.A. 1970. Notes on African Muscicapidae. Ibis 112: 395-397.

MONARCHIDAE: family of

PASSERIFORMES,

suborder Oscines;

MONARCH FLYCATCHER.

MONIAS: Monias benschi, sometimes misnamed 'Bensch's Rail' (see MESITE).

MONJITA: substantive name of most species of Xolmis, a genus of tyrant-flycatchers inhabiting open country in South America (see FLYCATCHER (2)).

MONKLET: substantive name of the small lanceolata of tropical America.

PUFFBIRD

Micromonacha

MONOCULAR VISION: see VISION. MONOPHYLETIC: of a single evolutionary ancestry (contrasted with POLYPHYLETIC).

MONOSPECIFIC: in reference to a genus containing only one species. MONOTYPIC: term applied to a taxon that has only one unit in the immediately subordinate category, e.g., a genus comprising only one species, or a species not divisible into subspecies--contrasted with POLYTYPIC.

MONOTYPY: see under TYPE

SPECIES.

MONTANE: appertaining to mountains; term applied particularly to the avifaunas of elevated areas in which the bird-life is strikingly different from that of adjacent areas of less altitude. The contrast tends to be especially pronounced at high levels in low latitudes; and it has been one of the puzzles of ornithology that particular sedentary species, sometimes not even showing subspecific differentiation, are found on isolated tropical mountain ranges separated by wide areas of unsuitable country in which such birds are never encountered (see AFROTROPICAL REGION). MOOD: 'the preliminary state of "charge" or "readiness for action"

MOON-WATCHING: see MIGRATION.

360 Moor fowl

MOOR FOWL: antique term (in British game laws) for the Red Grouse Lagopus lagopus scoticus; cf. HEATH FOWL. MOORHEN: substantive name of Gallinula spp.; applied without qualification, in Britain, to G. chloropus (see RAIL). MOORUK: native name in New Guinea, sometimes used as English, for Bennett's Cassowary Casuarius bennetti (see CASSOWARY). MOPOKE: popular name, also written 'more-pork', used in Australia for Podargus strigoides (see FROGMOUTH), and both there and in New Zealand for subspecies (or related forms) of Ninox novaeseelandiae (see OWL). The name purports to represent the call. MORILLON: British fowler's name (probably obsolescent) for immature Goldeneye Bucephala clangula, once thought to be a different species (see DUCK). MORPH: term introduced (I.S. Huxley 1955) to replace the less precise 'phase', denoting anyone of the different forms of a species population subject to polymorphism (including dimorphism, where there are only two morphs)--see POLYMORPHISM. MORPHOLOGY: literally, the science of form or shape; nowadays commonly extended to cover all external characters, including coloration, or even used synonymously with 'anatomy' (literally, internal structure as revealed by dissection); and it may be applied not only to the study but to its subject matter, as a collective term for the 'morphological' characters of a taxon. MORTALITY: see AGE. MOSAIC EVOLUTION: see under

ARCHAEOPTERYX.

MOSSIE: or Cape Sparrow, Passer melanurus (see MOTACILLIDAE: a family of the

SPARROW (1)).

PASSERIFORMES,

suborder Oscines;

WAGTAIL.

MOTHER CAREY'S CHICKEN: sailors' name (from 'Mater cara') for storm-petrels of various species (Hydrobatidae)--see PETREL. MOTIVATION: see

AMBIVALENCE; BEHAVIOUR, HISTORY OF.

MOTMOT: substantive name of species of Momotidae (Coraciiformes, suborder Alcedines); in the plural, general term for the family. The motmots are allied to the kingfishers (Alcedinidae) and even more closely to the todies (T odidae). The 6 genera and 9 species of motmots (Momotus, Electron, and Baryphthengus have 2 each) are confined to continental tropical America, chiefly at low altitudes; but the family was once far

Blue-diademed Motmot MomolUS momota. (N.A.).

more widely distributed, as the fossil bird Protornis glarniensis from the lower Oligocene of Switzerland is now ascribed to it. Characteristics, distribution and habitat. At the present time, the Momotidae are best represented in northern Central America and southern Mexico, where in certain regions of lighter vegetation these birds are abundant and conspicuous. Among the noteworthy structural peculiarities of the motmots are the serrated edges of their broad bills, which are about as long as their heads and downcurved at the end, and their feet, of which the outer toe is united to the middle one for most of its length and only one toe is directed backward, as in kingfishers. These beautiful birds (16-50 em in total length) are clad in softly blended shades of green, olive-green, and rufous rather than in brilliant spectral colours; although the head is often adorned with bright blue, and a black patch is usually present on the chest or throat. The most arresting feature of motmots is the tail, which is long and strongly graduated. In typical motmots, the central rectrices far exceed the others in length, and, when they first expand, the vanes may be narrower in the subterminal region than elsewhere. In this subterminal portion the barbs are loosely attached and fall away as the bird preens, and probably also in consequence of rubbing against the vegetation through which it moves, leaving a length of naked shaft which supports a spatulate or raquetlike tip where the vanes remain intact. The length of denuded shaft varies considerably from genus to genus, and in some genera it is lacking. While perching, motmots often swing their tails, pendulum-wise, from side to side, and sometimes hold them tilted sideways. When they about-face on a perch, they lift the tail over it with a graceful flourish. One of the most beautiful members of the family is the Turquoisebrowed Motmot Eumomota superciliosa, which is found from southern Mexico to northern Costa Rica in semi-arid country and in clearings in rain forest. Well over half of its 35 em is accounted for by its long tail. As in other motmots, the sexes are alike in coloration. The upper plumage is largely bright olive-green, with a patch of cinnamon-rufous in the centre of the back. Above each eye is a broad band of pale turquoise, the bird's brightest colour. The lores and ear tufts are black; and on the throat is an elongated, wedge-shaped patch of black, bordered on each side with turquoise. The remaining under plumage is greenish olive and cinnamonrufous. The middle feathers of the greenish-blue tail have a much greater length of denuded shaft than in other motmots, so that the spatulate, blue and black ends hardly appear to be connected with the rest of the bird. This makes the Turquoise-browed Motmot more airily graceful than its relatives. The largest member of the family is the Rufous Motmot Baryphthengus martii, which inhabits heavy forests from Nicaragua to Amazonia and western Ecuador. This 46-cm bird has the head, neck, and most of the underparts tawny, the back and rump and undertail coverts green. There is a black patch on each side of the head and one in the centre of the chest. Each of the central tail feathers has a short length of naked shaft. At the other extreme of size is the Tody Motmot Hylomanes momotula, an elusive, little-known inhabitant of forests from southern Mexico to northwestern Colombia. About 17em long, clad in dull green and rufous, with black ear-tufts, this small motmot has a short tail without racquet tips. An aberrant member of the family is the Blue-throated Motmot Aspatha gularis, which in northern Central America and extreme southern Mexico inhabits forests of oaks, pines, and cypress from about 1,200 to 3,000 m above sea level. Here it resides throughout the year, despite the severe frosts of the winter months. About 28 em long, this motmot is almost wholly clad in green, with a blue throat, black ear-tufts, and a black patch on the foreneck. The feathers of the long tail are strongly graduated, but the central ones have continuous webs rather than racquet tips. Habits and food. When foraging, motmots perch motionless until their keen eyes detect a beetle, caterpillar, spider, butterfly, cicada, small frog, lizard, or snake, on foliage, on the ground, or in the air. Then they dart swiftly, seize the victim, and carry it to a perch, against which, if large, they beat it before gulping it down. Small fruits, including those of palms, plucked while the bird hovers, enter conspicuously into the diets of some of the bigger motmots. These large species often forage with the mixed flocks that follow the army ants Eciton, catching small fugitive insects and other creatures rather than the ants themselves. Voice. Although the utterances of motmots are all structurally simple, they vary immensely in tone from species to species. The Turquoisebrowed Motmot voices a dull, wooden cawaak cawaak. The call of the

Moult

widespread Blue-diademed Motrnot MotmoluS momOla is a full, froglike, not unmelodious COOl COOl . At dawn, the rain-forest of southern Caribbean Central America is filled with the hollow hooting of the Rufous Motrnot, a mysterious sound often difficult to trace to its source , for these motrnots stay high in trees . The most melodious of the motrnots is the Blue-throa ted, whose delightfully clear and mellow notes are heard chiefly at dawn, when the members of a pair often sing in unison just after they emerge from the burrow where they slept. Behaviour. In courtship, two or more motmots call back and forth, often continuing for surprisingly long intervals. Sometimes, while so engaged, they hold pieces of green leaf or other fragments of vegetation in their bills-a puzzling habit, since such material is not carried into the nest burrow. The Blue-diademed, or Blue-crowned Motmot dust-bathes, sometimes on roadways in the evening twilight. Breeding. Motmots nest chiefly in burrows, which are dug by both sexes of the species for which information is available. They loosen the earth with their bills and remove it by kicking backward with their feet each time they enter to resume digging . The female Turquoise-browed Motrnot seems to do the greater share of the work, but her mate sometimes gives her an insect. Often the burrow is in the vertical bank of a watercourse or road ; but the Blue-diaderned Motrnot may dig its tunnel in the side of a mammal's burrow or a narrow pit in level ground, which makes its nests very difficult to find. In this species, as in the Bluethroated Motmot, the burrow may be crooked, with one or several sharp turns; but that of the Turquoise-browed Motmot is often only slightly curved . Motrnots' tunnels up to 4.3 m long have been recorded, but most are much shorter. Along the bottom of an occupied tunnel are two distinct parallel grooves, made by the birds' short legs as they shuffle in and out. In limestone regions, motmots sometimes nest in caverns or in niches in the sides of wells. Two to 4, rarely more , broad , roundish , pure white eggs are laid on the bare floor of the enlarged chamber at the end of the burrow. They are incubated by both parents. One member of a pair of Blue-diademed or Broad-billed Motmots enters the burrow early in the morning and sits for 6-8 hours, rarely longer. At midday or later, the other replaces it and remains in the burrow until the following dawn . While incubating, motrnots regurgitate many chitinous fragments from their insect food and an occasional seed, all of which are trampled into the floor of their chamber. The incubation period of the Blue-throated Motrnot is 21-22 days; that of the Turquoise-browed Motrnot, 15-19 days. Nestling motrnots, hatched blind and with no trace of down on their pink skins, are brooded and fed by both parents, who do not try to keep the nest clean. Young Blue-throated and Turquoise-browed Motmots leave the burrow at 28--31 days of age, and young Blue-diademed Motrnots at 29-38 days, but those of the small Broad-billed Motrnot fly when only 24-25 days old . They remain in the nest until they are well feathered, much in the pattern of the adults, and fly well. Their stubby tails, of course, still lack the racquet tips. Blue-diademed Motrnots and Turquoise-browed Motrnots are single-brooded. Turqoise-browed Motrnots start to dig their burrows as the spring or early summer breeding season approaches. Blue-diademed Motmots often begin in the autumn to dig burrows in which they will breed 4 or 5 months later . Blue-throated Motmots dig their burrows even earlier, in June or July, soon after their young are fledged . These tunnels are soon finished, and are then used as dormitories by the constantly mated pair throughout the winter months, when nights are cold and frosty . Even after eggs are laid in these old burrows in the following spring, both parents continue to sleep in them, as they do with the nestlings. After the latter emerge , they do not return to sleep in the burrow; but the parents sometimes continue to lodge in it unt il a new burrow is completed nearby. The motrnots of the lowlands, however, appear not to use their burrows as dormitories, and only one parent sleeps with the eggs and young, until the latter are about 5 days old . A.F.S. Orejuela, J.E. 1977. Comparative biology of Turquoise-brewed and Blue-crowned Motmotsin the Yucatan Peninsula, Mexico. Living Bird 16: 193-208. Skutch, A.F. 1945. Life history of the Blue-throated Green Motmot. Auk 62:

489-517. Skurch, A.F. 1947. Life history of the Turquoise-brewed Motmot. Auk 64: 201-217. Skutch, A.F. 1964. Life history of the Blue-diademed Motmot Momotus momota, Ibis 106: 321-332. Skutch, A.F. 1971. Life history of the Broad-billed Motmot, with notes on the Rufous Motmot. Wilson Bull. 83: 74-94 .

361

King Penguins Aptenadytespatagonicus (left) after and (right) duringmoult. (Photo: N . Rankin). MOULT: or 'molt' in American usage, the periodic shedding and replacement of plumage, and , in some species , of certain accessory structures of epidermal origin, e.g ., tarsal scales and horny sheaths of the bill (see FEATHER; PLUMAGE; BILL); the term is also applied to the period during which moulting occurs. The extent of moult and its timings during the year are adaptively integrated with the othe r main events of the ecophysiological cycle, name ly reproduction and migration (if this occurs)-see BREEDING SEASON; MIGRATION . Function. Periodic replacement of feathers is needed to maintain a high level of flight performance; to assist in regulation of body temperature by modifying the rate of heat loss from the skin; to maintain the waterproof nature of the plumage of some species ; and to allow seasonal changes in appearance, often associated with reproduction (though such changes may occur through abrasion of feather edgings; see later). Mechanism. Feathers grow from follicles in the skin . During the whole life of a bird, a series of feathers are produced from each follicle. At certain times, the dermal papilla at the base of the follicle is stimulated and in turn activates growth of the epidermis to produce a new feather. This pushes the old feather out of the follicle (Watson 1963). Stimulation of the papilla is usually under internal physiological control, but may occur in response to loss of a feather by plucking or by 'fright moult', the simultaneous shedding of large numbers of feathers from certain parts of the body, a phenomenon that sometimes occurs when birds are frightened by a potential predator. Pattern. Within each pteryla or tract of feathers (see PTERYLOSIS), feather loss and replacement proceeds in a regular sequence. In general, within tracts of contour feathers, waves of moult pass outwards from the mid-line and downwards towards the tail. Moult of flight feathers begins from certain foci in each tract, often proceeding in both directions with sequential loss of adjacent feathers, but sometimes in only one direction, as in moult of the primary feathers of most passerine birds, in which the short innermost primary is shed first and moult proceeds steadily towards the longer outermost feathers. Members of several other orders of birds, e.g . Procellariiformes, Accipitriformes, normally follow the pattern of 'descendent' moult of the primaries found in the passerines. However, in the Falconiformes, moult commences with loss of primary 4 (and in the parrots with primary 5) and then progresses sequentially both inwards and outwards from this focus. In the budgerigar Melopsittacus undulatus, for example, before the tenth primary has completed growth, primary 5 may have been shed again, at the start of the next moult, so that two 'waves' of mou lt are present

362 Moult

briefly in the same bird. The presence of more than one cycle of moult within the same set of primaries has been termed 'Staffelmauser' (= stepwise moult) by E. Stresemann and occurs in some terrestrial non-passerines and in many seabirds, particularly the larger species in which the onset of breeding is delayed for several years. The pattern is established gradually during the first few years of life. One of the most complicated patterns of moult of the primaries discovered so far occurs in cuckoos, e.g. Guculus canorus in which primaries 1-4 moult descendently but the remaining set of feathers moults ascendently and alternately, i.e. 9-7-5-10-8-6; the relative timing of the moult of these two sets of primaries is not fixed. The pattern of moult of secondary feathers of large terrestrial and large seabird species is also highly irregular. The pattern of moult in all feather tracts should be considered as adaptive. Since the distribution of pterylae and apteria (areas of skin that are bare or covered only by semiplumes or downs; see FEATHER) is important in the control of body temperature (Clench 1970), growth of new body feathers starting from the centre of each tract ensures minimum loss of skin cover during moult. Similarly, replacement of primaries from the innermost outwards allows most passerines to fly during wing moult, even though several adjacent feathers may be growing at anyone moment. By means of this sequence, the innergrowing primaries are also protected by the old outermost feathers. A similar protective function of old feathers is shown in the sequence of tail moult of woodpeckers, in which the long inner pair of feathers---used for support in climbing-are retained until the other pairs have been replaced. In most other families, tail feathers are shed sequentially from the innermost outwards, or vice versa. Control. Many experiments have been undertaken on captive birds to establish the hormonal control mechanisms leading to the activation of feather follicles. Most of these have involved hormone injections, but changes in photoperiodic regime or nutrition, known or thought to affect hormone levels, have also been used. The results and relevance of these experiments need to be viewed against the known patterns of moult of different feather tracts. Few experimental treatments have led to sequential moult of feathers in a tract at rates corresponding to what happens in the wild. It is clear from wild birds that the focus or foci at which moult begins in each tract are the same in successive (complete) moults. Miller (1941) suggested that the first feathers to be shed may be those with increased blood supply, but this has yet to be confirmed. Alternatively, or additionally, the follicles at the foci may have lower thresholds of response to hormonal or other stimuli than other feathers in each tract. Once moult has begun, the sequential shedding of feathers could arise by stimulation of growth in one follicle by the growth of an adjacent feather, perhaps by improvements in blood supply. Alternatively, follicles in a sequence could require progressively higher levels of hormones to elicit their growth responses; or each follicle could be time-programmed to begin growth slightly out-of-phase with its neighbour (Ashmole 1968). There is some support from experiments of the concept of local (spatial) variations in sensitivity of follicles to hormonal stimuli, but long-term time-programming of responsiveness of follicles may also be involved, since different levels and combinations of hormones can elicit moult in the domestic fowl according to the number of months since the previous (natural) moult. In general, hormonal treatments of wild birds with androgens and oestrogens inhibit moult, but the species investigated so far include chiefly those whose schedules of breeding and moult do not overlap in the annual cycle. Although breeding, moult and migration are often mutually exclusive, many species are known in which overlap of these events occurs (see later). Levels of gonad-stimulating hormones show no seasonal variations that can be correlated exclusively with moult, rather than breeding, and any inhibitory actions of the hormones FSH and LH on moult that have been demonstrated are probably attributable to the results of increased production of androgens and oestrogens. Similarly, there are no clear-cut relationships between seasonal prolactin levels and the initiation of moult. The results of direct treatments with prolactin are equally diverse, any positive effects probably occurring indirectly through alteration of androgen and oestrogen levels. Almost all the experiments involving the hormones mentioned so far were carried out before any real appreciation existed of the circadian rhythms of release of hormones from the pituitary, of circadian rhythms of sensitivity of target sites, and of seasonal variations in these rhythms. The involvement of the thyroid in the control of moult has been the

subject of extensive research, much of it summarized by Voitkevich (1966). This work, and more recent studies, have been reviewed critically by Payne (1972) who concludes that it is uncertain whether thyroid activity is directly involved in the control of the start and patterns of moult in wild birds. Of external stimuli that might alter hormone balances and so initiate moult, changes in photoperiod have been studied most extensively. Most experiments have involved species that breed in northern temperate latitudes. In these, exposure to artificially long photoperiods, after exposure to natural short winter daylengths, usually leads to development of reproductive condition, and, in those species that moult into a special plumage for the breeding season, to feather replacements. However, the timing of this moult, relative to the timing of fat deposition for migration (if any) and of gonadal enlargement, may not parallel exactly the situation in wild populations. Other experiments have sought to prolong reproductive condition by maintaining birds on artificially lengthened photoperiods after the end of the normal breeding season. Eventually gonadal regression occurs, and the normal complete moult after breeding is usually postponed in these experimental birds until this time. Taken together, all the photoperiodic experiments indicate an effect of gonadal hormones (usually inhibitory) on the time of the start of moult. Day-length may not be important in controlling the timing of events in the annual cycle in equatorial regions, and its importance at higher latitudes may also have been overstressed. Many species show circannual rhythms of breeding, moult and preparation for migration if held in conditions of constant photoperiod, temperature and humidity for several years. In most species these rhythms persist for more than one year, and so are not simply an autonomous sequence of events triggered each spring by an external stimulus. The circannual period length (between successive events of the same type) may differ for moult and reproduction, indicating that there is no obligatory connection between the start of a moult and the stage of breeding (see, for example, Gwinner and Dorka 1976). Energy and nutrient requirements. The additional energy required for feather production during moult by Chaffinches Fringilla coelebs has been measured as 140kCal. spread over 70 days (Dolnik and Gavrilov 1979). This was required to produce 1.4 g of feathers, whose energy content (if burnt in oxygen) would be only about 7.7 kCaL Unlike this experiment, which was carried out at 26°C, within the thermoneutral zone, most measurements of additional energy requirements during moult have been carried out at lower temperatures and so include not only the energetic costs of feather production but also an element for the increased costs of maintenance of body temperature during the period of greater rates of heat loss, from surfaces with growing feathers. Measurementsofthecosts offeatherproduction in House Sparrows Passerdomesticus have been made for two geographical populations and are slightly higher than the 100kCal/g estimated for Chaffinches---namely 185kCal for 1.7 g and 218kCai for 2.0g of plumage in the USA and USSR respectively. Measurements of increased energy requirements during moult in captive birds held at natural temperatures indicate an increase in metabolic rate of around 30% in many passerines. However, the duration of moult in captives has often been longer than in wild birds of the same species, so the increase in metabolic rate may have been over-estimated. It is also not known to what extent wild birds compensate for the added energy costs of moult by reducing their energy expenditure on activities such as flight and foraging. Quite possibly their daily food requirements during moult are not much higher than before moult begins. Feather KERATIN contains higher proportions of sulphur amino-acids, particularly cystine, than those present in most animal and (particularly) plant proteins. It has often been suggested that the cystine content of birds' food during moult might be limiting, rather than the energy content. Dolnik and Gavrilov (1979) have concluded that during the first part of the complete moult of Chaffinches, the increase in food consumption by captive birds chiefly provides the required amounts of the sulphur amino-acids, and that heat production from the daily food intake exceeds that required for thermoregulation at this period. Most species maintain feather growth by both day and night even though they feed only by day. This may result in the transfer of amino-acids from muscles to growing feathers either in the short-term (overnight, as in some passerines) or the longer term (several weeks, as in the Canada Goose Branta canadensis, in which the wing, but not the leg, muscles atrophy during the flightless period).

Moult

Moulting during breeding. Since moulting does require extra energy, and therefore extra food intake unless activity can be reduced, the separation of moulting and breeding could be adaptive on energetic grounds, particularly in species that feed their young in the nest and therefore cannot 'afford' to reduce energy expenditure on foraging. One might expect most overlap of breeding with moult in species in which feather replacement spans a long period of the year, so that the extra energetic demands are small at anyone moment, and in those living in tropical areas where thermoregulatory energy requirements should not be increased by moult. The first of these generalizations is broadly correct, but the second is not. Many tropical species show seasonal breeding, and moult is often delayed until the end of the reproductive period. In those species that utilize foods whose abundance does not vary seasonally, moult may be protracted and overlap with breeding. Other species may vary the timing of breeding from year to year, but show consistency in the timing of onset of moult. This leads in some years to separation but in others to overlap between breeding and moult, and occurs especially in arid-zone birds which breed whenever droughts are broken by irregular rainfalls. The multitude of different schedules and degrees of overlap of breeding and moult in different species are reviewed thoroughly by Payne (1972). Duration of moult of flight feathers. Amongst European passerines, few species renew their primary feathers in less than 5 weeks. In closely related species, e.g., the finches, migratory species take less time to complete primary moult than do sedentary ones. This is true even within a species, e.g., the wagtail Motacilla alba, in which Finnish populations of the migratory M. a. alba complete moult in 45-50 days, whereas the sedentary British M. a. yarrellii take 76 days, on average, to grow new primaries. Wing-moult of the sedentary species often commences later in the year than that of related migratory species. Suspended moult. Under certain circumstances, birds that have begun feather growth may interrupt their moult, growing feathers being completed but feathers next in sequence to be moulted being retained until a later date. This occurs in some species that breed irregularly; moult is interrupted during breeding. (Others, with protracted moults, may continue to moult during breeding, as detailed earlier.) Moult of flight feathers may commence before migration in some species, particularly those breeding in the arctic, but may be interrupted during migration itself. A few species may undertake short migrations with incompletely grown outer primaries. Flightlessness. Some birds lose the power of flight during moult. This occurs for part of the moult period in certain arctic passerines that migrate south soon after breeding and compress moult of the flight feathers into a 5-6-week period. More than 5 adjacent primaries may be growing at anyone time and all pairs of tail feathers may be shed simultaneously (Haukioja 1971). Individuals of the same species, e.g., Willow Warbler Phylloscopus trochilus, breeding at more temperate latitudes, spread their wing moult over a slightly longer period and do not lose completely the ability to fly. Nevertheless, most passerine species become less active and less conspicuous during moult, in part to avoid avian predators (Newton 1966) but presumably also to reduce daily existence energy requirements. In 11 families of birds, many comprising fairly large-sized species, for example the ducks, geese and swans, divers and grebes, all flight feathers are shed simultaneously, and individuals are unable to fly for a period of a month or more. Because they are vulnerable to mammalian as well as avian predators at this period, some species spend the moult on large lakes, offshore islands or the open sea. This may require a 'moult-migration' from the breeding area to a relatively safe moulting site. Most northern European Shelduck Tadorna tadoma gather to moult in July and August on the sandbanks in the Heligoland Bight; many species of arctic-nesting geese undertake such migrations, those involving nonbreeding individuals often leading them to still higher latitudes (Salomonsen 1968). Eclipse plumage. In some groups the full adult plumage, in which the birds breed, is replaced at the end of the reproductive season by a dull 'eclipse' plumage that is worn for only a very few months before a fresh adult plumage is acquired; this is found among the ducks, cuckooshrikes, sunbirds, and weavers. It is particularly striking in the males of typical duck species, which lose their very distinctive plumage early in the breeding season and become more like the cryptically coloured females. In these birds, the body plumage is lost before the wing feathers are

363

replaced, and the second moult of the body plumage, into the colourful breeding plumage once again, may commence before the wing feathers are fully grown. Therefore, although the drakes are protectively coloured during most of their flightless period, it would appear that the advantage of reacquiring the colourful breeding plumage early, in terms of enhancing their chances of successful matings, outweighs the value of prolonging the period in which they are protectively coloured, even though this may increase each individual's chances of survival. Frequency. All birds moult at least part of their plumage once a year, many species twice, and a few thrice. If breeding and moult do not overlap, the main function of the 'postnuptial' moult is the renewal of worn and faded plumage; it is therefore general and almost always complete. In some groups, such as birds-of-prey and swallows, the moult of the remiges and rectrices may be delayed until mid-winter. This adaptation seems to be correlated with migration, during which birds of the two named groups are often in close association. The 'prenuptial' moult, when present, is usually partial. It intensifies the secondary sexual characters by brighter colours or by adding plumes or other adornments (e.g., the facial warty excrescences in the Ruff Philomachus pugnax). This moult tends to be more evident in males than in females; exceptions include the phalaropes. Part of the colour change apparent at this season is in some species due to abrasion of the edges of feathers. Miller (1961) found that the Andean Sparrow Zonotrichia capensis has two complete moults annually, each of two months' duration. In the Ptarmigan Lagopus mutus there is a partial moult during the late summer and autumn, when an admixture of the grey breeding dress and the brownish autumn plumage is observable before the birds pass into the white plumage of winter. Assumption of this winter plumage has been shown to depend on a fall in temperature; this, by responsively increasing metabolism and acting through the endocrine system, suppresses melanin production (Salomonsen). The prenuptial moult in spring, later in males than in females, brings the birds into breeding dress (see also COLORATION, ADAPTIVE). The moult can be a purely local and normal condition, as in the case of defeathering of the incubation patch area which is initiated by the hormone prolactin, prior to the increased vascularity, epithelial hypertrophy, and oedema in preparation for incubation (Bayley 1952). Terminology. From the beginning of the 20th century, the terminology used to describe moults and plumages was based on temperate-zone passerine birds, in which breeding and moult are usually separated in time. This led to use of terms such as 'pre-' and 'post-nuptial' moult, which are difficult to apply to many tropical birds and to others in which there is total overlap or no constant relationship between the timings of moult and reproduction. Humphrey and Parkes (1959) reviewed the then-existing descriptive systems and proposed one of their own which is now widely used. They recognized that new 'aspects' (plumages) arise from new feather generations in at least some of the feather tracts, and that since new feathers push out old (except in fright moult or defeathering of the incubation patch), moults should therefore be named with reference to the incoming generation. These generations are named in a way that avoids seasonal, reproductive or age criteria. The first covering of true feathers is named the juvenal feather generation, and this plumage never recurs after later moults. At some later stage, the incoming feather generation in a particular tract is identical in appearance with one that has developed at an earlier time in that same tract. The interval between these moults is known as a cycle, and is normally of 12-months' duration. If only one feather generation is produced within a cycle, it is termed basic; if two, the second is termed alternate; in those rare cases in which three generations are produced in a single feather tract during one cycle, the third is termed supplemental. The moults are described as pre-basic, pre-alternate, etc. The appearance of a bird can be deduced from knowledge of the feather generations (basic, alternate, juvenal, etc.) present in each feather tract at the time in question. Moult of accessory structures. These cases can be divided into three classes. First, there are those that come under the heading of secondary sexual characters accompanying and supplementing the prenuptial moult, being developed expressly for the breeding season and being

discarded at its end. Typical examples are found in the auks, the Puffin

Fratercula arctica providing a familiar instance; in this species the highly coloured parts of the bill, the two small supraorbicular excrescences, and the puffy 'rosettes' at the angles of the gape are shed. Also, the Hornbill Auk Cerorhinca ('Ceratirhina') monocerata moults the internaral pro-

364 Moult migration

tuberance. A further example is the 'bill-horn' of the males of the American White Pelican Pelecanus etythrorhynchus, the horn falling off at the end of the breeding season. Secondly to be mentioned is the moulting of the claws in ptarmigan Lagopus spp. It is very probable that the tarsal scutellae are also moulted regularly; evidence in support of this is provided by the case of a Song Thrush Turdusphilomelos with abnormal cutaneous horns on its head and on one leg, these being cast each time the bird moulted. Probably this applies to all pathological structures arising from tissues of epidermal origin, including those of the uropygeal OIL GLAND (which in certain circumstances can produce a 'horn' that is moulted regularly). Th~ third category consists of structures that serve a temporary funct~on only. In the Hoatzin Opisthocomus hoazin the young have functional claws on the 1st and 2nd digits of the manus for the first week of life only; these are shed and during after life the claws are represented by minute callosities. A further instance of structure of this nature is afforded by the 'heel' pads of woodpeckers and wrynecks, toucans, and scansorial barbets, this structure falling off when the birds leave the nest. (J.M.H.) P.R.E. Most papers quoted in the text are included in oneof thefollowing three reviews: In Farner, D.S. & King, j.n. (eds.). 1972. Avian Biology. Vol. 2. New York. Palmer, R.S. Patterns of molting. Chapter 2. Payne, R.B. Mechanisms and control of molt. Chapter 3. Stettenheim, P. The integument of birds. Chapter 1.

Also mentioned were: Dolnik, V.R. & Gavrilov, V.M. 1979. Bioenergetics of molt in the Chaffinch Fringilla coelebs. Auk 96: 253-264. Ginn, H.B. & Melville, D.S. 1983. Moult in Birds. BTO Guide No. 19. Tring. Gwinner, E. & Dorka, V. 1976. Endogenous control of annual reproductive rhythms in birds. Proc. XVI Orn. Congr. pp. 223-234. Haukioia, E. 1971. Flightlessness in some moulting passerines in Northern Europe. Ornis Fennica 48: 101-116. Salomonsen, F. 1968. The moult migration. Wildfowl 19: 5-24.

MOULT MIGRATION: a regular movement by certain birds to and from an area where they moult (see MIGRATION; MOULT). MOUND-BIRDS; MOUND-BUILDER: see MEGAPODE. MOUNTAINEER: Oreonympha nobilis(for family see HUMMINGBIRD). MOUNTAIN-GEM: substantive name of Lampomis spp. (for family see HUMMINGBIRD). MOUPINIA: substantive name of the 2 species of Moupinia of southeast Asia (for family see BABBLER). MOURNER: substantive name of species of Laniocera and Rhytipterna (for family see FLYCATCHER (2)). MOUSE-BABBLER: substantive name of the 3 species of Crateroseelis of New Guinea (for family see RAIL-BABBLER). MOUSEBIRD: substantive name, alternatively 'coly', of the species of Coliidae (sole family of the Coliiformes); in the plural ('mousebirds,' 'colies'), general term for the family. The family contains 6 species, all very similar to each other and so specialized in character that the family is generally placed in an order of its own-the only order endemic to Africa. Characteristics. All are small-bodied, weighing 38-68 g, two-thirds of the length of 30-36 em contributed by the characteristically long graduated tail. The plumage is drab grey or brown relieved in most species by a patch of red, blue or white on the head, neck or rump or by barring or speckling. The body feathers are soft and hair-like with remarkably long aftershafts, and are poorly waterproof. The wings are short and rounded, with 10 primaries and 10 secondaries. All species have a pronounced crest which is normally carried erect. The sexes are alike. The bill is short, slightly downcurved, and strong. The 4 toes are normally all directed forward, but the outer toe on each side can also point backwards. The usual perching attitude is with the feet and shoulders at about the same level, the belly hanging down exposed between the legs, but mousebirds occasionally perch normally too. On the ground they can hop, run or walk surprisingly fast. The flight normally consists of alternate bursts of flapping and gliding but can be fast and direct; often a flock will fly

Blue-naped Mousebird Colius macrourus. (N.A.).

straight into the centre of a bush. They are highly gregarious, and probably as similar to each other in behaviour and ecology as in structure. Habitat. Most of the wooded and bushy environments of Africa south of the Sahara, avoiding open plains and forest interiors. Distribution. Throughout the Afrotropical region. The 4 species of the Colius striatus group include the widely distributed C. striatus, the allopatric C. castanotus, the partly sympatric C. colius and the almost completely sympatric C. leucocephalus; none of these species extends west of the River Niger. The members of the C. macrourus superspecies replace each other geographically, C. macrourus in the north and northwest to the Atlantic coast and in the east, C. indicus south of about 80S; some authors put these 2 species in the genus Urocolius (e.g. Schifter 1972). Populations. Mousebirds are often extremely numerous, especially around small-scale cultivations; although several species are widely sympatric, normally one is noticeably commoner than the others in any particular locality. Movements. Mousebirds are highly sedentary; movements are probably confined to feeding and roosting flights. Food. Mousebirds are almost exclusively vegetarian; nearly half the diet in some populations is leaves, the rest fruit, seeds and nectar with little if any animal matter. In gardens and on small fruit and vegetable farms they may be serious pests locally, but they do not adapt well to large-scale monocultures and so are of little importance agriculturally except to small-scale farming. Their diet is notable for the high proportion of plant species containing toxins or irritants. Mousebirds drink pigeon-fashion, sucking water up with the head lowered. Behaviour. Mousebirds are gregarious at all times of year, moving in parties of normally up to 30 birds, roosting in tight huddles, sunbathing and dustbathing together, and often nesting in close proximity. Allopreening is common. Roosting birds cluster tightly together in trees and bushes, sleeping with the head upright but withdrawn into the shoulders; suggestions that they are incompletely homoiothermic are unfounded, but heavy rain can impair their insulation to the extent that they die of cold. Courtship-behaviour is poorly known, but C. indicus and C. macrourus have a perch-jumping display in which one or both birds bounce up and down, sometimes with one wing held up. Voice. They are highly vocal birds, whistling and chattering almost incessantly. Flight and alarm calls are hard or buzzing; C. macrourus has a clear whistle on the wing. Breeding. Nests may be solitary or loosely clumped, shallow cups or open platforms in bushes; some are built on top of old nests of the same or other species, and most are ornamented with fresh green leaves. Eggs are dull creamy white, immaculate in some species, speckled and blotched in others. Clutch size is normally 3 but ranges from 1 to 8, the

Musc~ature

larger clutches often caused by more than one female laying in the same nest. Eggs weigh 2.7-2.9g. Both sexes incubate, for 11-14 days. Chicks are fed by regurgitation, by both sexes, and fledge after 15-20 days. Adults incubate and brood very tightly. Moult. Birds may begin moulting as early as 2 months after fledging. Moult is protracted; it is normally serially descendent but ascendent and stepwise moults have also been recorded. A.W.D. Rowan, M.K. 1967. A study of the colies of southern Africa. Ostrich 38: 63-115. Schifter, H. 1972. Die Mausvogel (Coliidae). Die Neue Brehm-Bucherei No. 459. Wittenberg Lutherstadt.

MOUSTACHIAL: applied to a streak, in some plumage patterns, running back from the base of the bill. MOUTH: see BILL;

TONGUE;

also ALIMENTARY

SYSTEM; RESPIRATORY

SYSTEM.

MUD-HEN: popular name for the American Coot Fulica americana (see RAIL). MUDLARK: see MAGPIE-LARK. MUDNEST·BUILDERS: see MAGPIE-LARK. MULE: aviculturist's term for a hybrid between a Canary and another species of finch. MULGA: name for a type of bush country in Australia, characterized by Acacia aneura. MULLERIAN MIMICRY: see MIMICRY. MULTI·BROODED: see CLUTCH-SIZE. MUNIA: substantive name in Asia of various species of Estrildidae; in the plural, sometimes used as a general term for the group (see ESTRILDID FINCH).

MURRE: alternative substantive name (preferred in American usage) of guillemots of the genus Uria (Alcidae)-see AUK. MURRELET: substantive name of species of Brachyramphus and Synthliboramphus (see AUK). MUSCICAPIDAE: a family of PASSERIFORMES, suborder Oscines, forming part of a group of 12 families of Primitive Insect Eaters, the main body of which consists of the so-called Muscicapid assemblage. This embraces an exceptionally large number and wide variety of largely insectivorous, mainly Old World, ten-primaried song-birds in which bright coloration and conspicuous patterns and structures are scarce. Hence, the group is treated in Peters Check-list of Birds of the World on reasonable grounds as one family, Muscicapidae, comprising the subfamilies Turdinae, Timaliinae, Cinclosomatinae, Paradoxornithinae, Polioptilinae, Sylviinae, Malurinae, Muscicapinae, and Pachycephalinae. Most of these had been treated as families by most authors. Though the differences seem trivial in some cases, particularly in many species of the Old World tropics, the lumping of these groups obscures such differences as do exist and results in a family which (at least in bird systematics) is very large and unwieldy. In the classificatory system used here the Muscicapid assemblage includes the families Turdidae (THRUSH), Sylviidae (WARBLER (1)), Muscicapidae (FLYCATCHER (1), Rhipiduridae (FANTAIL), Monarchidae (MONARCH FLYCATCHER), Pachycephalidae (THICKHEAD), Timaliidae (BABBLER), and Aegithalidae (TIT, LONGTAILED). The general opinion is that the members of these families are closely related and probably more so to each other than to the remaining families of the group of Primitive Insect Eaters with the exception of the

Mimidae (MOCKING-THRUSH) which on recent evidence may be very close to the Turdidae.

MUSCLE: see MUSCULATURE.

365

MUSCULAR CONTRACTION: see ENERGETICS. MUSCULATURE: the system of muscles, which are the specialized organs for effecting movement. Collectively these form the 'flesh', which in an average bird constitutes almost half the total body weight. . Characters of muscular tissue. The essential feature of muscular tissue is its specialization for contraction, in the course of which force is developed. Muscle tissue in birds and other vertebrates occurs in three principal forms. Unstriated ('smooth' or 'involuntary') muscle consists of quite short fusiform cells in which longitudinal filaments may be discerned with appropriate techniques, but little else. Striated or voluntary muscle consists of very much longer multinucleate fibres, which show a characteristic pattern of crossbanding. Cardiac muscle, found only in the heart (see HEART), consists of a network of fibres showing some distantly spaced crossbars. Unstriated muscles occur mainly in such situations as the gut, viscera, glandular ducts or feather bases; they are innervated by autonomic nerves (see NERVOUS SYSTEM) and are not normally under the control of the will. Striated muscles occur principally in association with the skeleton (see SKULL; SKELETON, POST-CRANIAL), hence their alternative name of skeletal muscles. They are innervated by cranial and spinal nerves and are under the control of the will. It is with these that the remainder of this article is concerned. For a fuller review of the structure and properties of avian skeletal muscles, the reader is referred to Bock (1974). Contraction. A muscle exerts force only when contracting, and has no intrinsic means of lengthening; stretching of a muscle can only be brought about by an external force, usually that of another muscle. Muscle contraction can take place without shortening if the force it develops is equalled by an opposing external force; 'isotonic contraction' refers to contraction involving change in length, and 'isometric contraction' to the situation when the muscle produces force without changing in length. Many muscles function primarily through isometric contraction, providing holding or stabilizing forces, e.g., in the maintenance of body posture. However, all muscles play some part in this, exhibiting a low level of contraction ('muscle tone') even when apparently at rest. Fibre types. Striated muscle fibres show important variations in structure and histochemical properties which are correlated with physiological differences, though the details of the relationship are very imperfectly understood at present. Two main sets of types of fibre are recognized in avian muscles: red and white muscle fibres, distinguished by myoglobin content, and twitch and tonus fibres, distinguished by innervation and structural details. Red and white fibres may eventually prove to be simply the extremes of a continuum, but the dichotomy is a familiar one, since muscles consisting largely of white fibres (e.g., the breast muscles of a chicken) are very obviously different from those composed mainly of red (e.g., the same muscles in a pigeon). No bird possesses muscles composed entirely of white fibres, though the pectoral muscles of hummingbirds appear to consist entirely of red. Apparently red fibres fatigue more slowly, but white fibres can produce a higher rate of work over a short period. Twitch and tonus fibres also show some differences in rate of fatigue, but should not be equated with white and red; there appears to be no simple correlation between the two types. Twitch fibres respond to a stimulus with a rapid contraction which ends almost immediately the stimulus ceases. Tonus fibres respond to stimuli with a contraction which builds up more gradually, and falls off very slowly after stimulation stops. Most bird muscles that have been studied consist of a mixture of the two types, but in varying proportions. Probably a high proportion of tonus fibres indicates a postural function, while a high proportion of twitch fibres suggests a more active role. Muscle architecture. In describing the gross structure of a muscle it is usual to refer to the attachments of its two ends as 'origin' and 'insertion'. The origin is strictly the end attached to a stationary bone, while the insertion is the attachment on a bone which is moved by the muscle's contraction. In practice, very often both bones are moved by the muscle, but the terms are still employed, if arbitrarily, for convenience. The arrangement of fibres within the muscle-its architecture-is of great importance in understanding its action and adaptations. Two basic arrangements are generally recognized. In parallel-fibred

muscles, the fibres are oriented along the line of action of the muscle, and run from origin to insertion; hyoid muscles such as M. stylohyoideus or M. cleidohyoideus furnish good examples. Pinnate muscles are those in which fibres are attached, at least at one end, to a tendon-a structure

366

~usc~ature

composed largely of collagen, which functions to transmit the force of the fibres to a bone. The simplest type of pinnate arrangement (unipinnate) is with fibres attached at one end to one surface of a tendon or aponeurosis (tendinous sheet), and at the other to a bone. Bipinnate muscles have fibres attached to either surface of an aponeurosis, and multipinnate muscles have several internal aponeuroses ('raphes'), usually arising alternately from origin and insertion, and interdigitating. The functional properties of parallel-fibred and pinnate muscles differ in important ways, stemming basically from the length and number of fibres in the muscle. Fibre length affects only the speed and range of shortening of a muscle, while the force that it can develop depends fundamentally on fibre number. In general, parallel-fibred muscles can have much longer fibres, but the number that can be accommodated is much less than that possible with pinnate architecture. Pinnate muscles are generally to be found in situations requiring the development of large forces, but relatively little shortening ('excursion'). Extremes of pinnate development, with several raphes and large angles of pinnation commonly occur in muscles sited very close to an articulation, such as the jaw muscle M. adductor mandibulae externus caudalis, or other situations involving little or no excursion, such as with the Mm. intertransversarii linking adjacent cervical vertebrae. One- and two-joint muscles. An important distinction should be made in regard to the siting of muscles. One-joint muscles are those which arise on one bone and insert on the next in succession, spanning a single articulation. Two-joint muscles arise on one bone, miss the next and attach on the third in the series, thus spanning two articulations. (Three or more joint muscles also exist but, with the exceptions of some neck muscles, their forces are usually redirected via tendons traversing pulley or sling devices---a feature of avian limb systems which enables the weight of major muscle masses to be concentrated closer to the bird's centre of gravity.) Two-joint muscles minimize energy expenditure for many actions and, due to their length, can shorten faster than one-joint muscles. Disadvantages are that they cannot individually control the forces about each articulation, and lack the stability for holding the system under static conditions. Thus, in most major systems such as limbs or jaws, two-joint muscles provide a large part of the force, with just sufficient one-joint muscles for precise control of movement at each joint, and for stability. Nomenclature. Muscles may be named after site, shape or action, or on the basis of presumed homologies (see HOMOLOGY). Complications have been caused by attempts to homologize bird muscles with those of mammals, producing conflicting terminologies. The Nomina Anatomica Avium (Baumel et al 1979) should resolve this confusion, and its nomenclature is followed here. For a detailed survey of bird muscles see George and Berger (1966). Subcutaneous muscles. These are thin sheets or bands of muscle lying under the skin, and often adhering to it. The presence or absence of M. biceps brachii, pars propatagialis, is of significance in the diagnoses of several major groups. Subcutaneous muscles are striated, with the exception of M. expansor secundariorum, the only non-striated muscle specifically mentioned in this account (see Muscles of the wing). Cranial muscles 1. Ocular muscles. These are the small muscles concerned with moving the eyeball, and differ little from those in other vertebrates. Included here also is the levator muscle of the upper eyelid and the muscles (M. pyramidalis and M. quadratus) responsible for the movements of the nictitating membrane (see VISION). 2. Jaw muscles. Although only 8 in number, these muscles have attracted the attention of many investigators, since they show extensive variation among birds, correlated at least in part with differences in food and feeding techniques. Present terminology is based on the detailed study by Lakier (1926). The action of these muscles includes not only opening (depression) and closing (adduction) of the lower jaw as in mammals, but also extensive movements of the upper jaw. Muscles which raise the lower jaw fall into two groups. Those which originate on the skull (M. adductor mandibulae externus and M. pseudotemporalis superficialis) are two-joint muscles, frequently of multipinnate architecture; those which arise on the quadrate (M. pseudotemporalis profundus and M. adductor mandibulae caudalis) are one-joint muscles, which, with M. pterygoideus arising on the pterygoid, bring about retraction as well as adduction. M. pseudotemporalis profundus is absent in parrots, many kingfishers, and various other birds. M. pterygoideus is a muscle of

considerable complexity. In many birds, especially passerines, it has a slip (M. retractor palatini) attached to the skull base, thus acting solely to retract the palate. M. pterygoideus has also given rise in parrots to a unique muscle, M. ethmomandibularis, which originates on the interorbital septum, and acts purely as an adductor of the lower jaw. Protraction of the upper jaw is effected by M. protractor quadrati et pterygoidei, and depression of the lower by M. depressor mandibulae. Striking enlargement of one or both of these muscles is seen in birds whose feeding habits involve opening the bill against resistance, e.g., M. protractor in Gallinago or M. depressor in Heteralocha (Burton 1974a and b). ~uscles of the tongue and hyoid apparatus. Like the jaw muscles, these show much variation related to feeding adaptations, and are often also of taxonomic interest. Extremes of complexity are encountered in groups with highly modified tongues, notably parrots and woodpeckers. The tongue and hyoid muscles may be grouped into two categories: Extrinsic muscles have an attachment at one end to the lower jaw, and are responsible for large-scale movements of the entire tongue and hyoid apparatus. They include M. branchiomandibularis, with its insertion wrapped around the hyoid 'horn', which pulls the whole apparatus forward, and M. stylohyoideus which retracts it. Intrinsic tongue muscles have both origin and insertion within the hyoid apparatus, and permit finer control and more delicate movements; for example, M. ceratoglossus flexes the tongue downwards relative to the basihyal, while M. hypoglossus obliquus returns it to the resting position. Muscles of the trachea, larynx and syrinx. Opening and closing of the laryngeal slit or glottis (e.g., when swallowing food) are brought about by two small intrinsic muscles (M..dilator and M. constrictor glottidis). An additional muscle eM. cricohyoideus) connects the larynx and hyoid apparatus. Tracheal muscles show much variation, but one present in most birds is M. tracheolateralis, which adheres closely to the side of the trachea, and inserts on the syrinx. In the highly developed vocal apparatus of passerines (especially oscines), however, a number of additional syringeal muscles are present (see SYRINX). Neck muscles. The detailed comparative review by Boas (1929) has been the basis for most subsequent studies. Muscles of the vertebral column generally are grouped into an epaxial series, situated dorsally, and a hypaxial, providing lateral and ventral components. Six neck muscles, originating principally on the first neck segment, are inserted on the skull. Four are of epaxial origin, acting to raise or turn the head; and include M. complexus, which plays an important, if indirect, part in emergance from the egg. Two hypaxial muscles eM. rectus capitis lateralis and ventralis) act as head flexors. The muscles of the neck proper include some of the most complex to be found in the avian body, spanning many articulations, with individual slips to several vertebrae. The principal epaxial system is that of M. longus colli dorsalis, including long multijoint components as well as shorter ones traversing only one or two vertebrae. Their principal actions are to straighten neck segments I and III, and to flex segment II upwards. Still more intricate is the hypaxial M. longus colli ventralis, the bulk of which consists of long slips arising posteriorly, but each one linked by individual short slips to the vertebrae it passes; its actions are the reverse of M. longus colli dorsalis. Hypaxial muscles also include lateral components, which contribute to lateral bending, as well as providing overall stability; they include both short muscles interconnecting successive vertebrae, notably Mm. intertransversarii and Mm. inclusi, and longer muscles linking 3 or more vertebrae, such as M. cervicalis ascendens. Muscles of the trunk and tail. Within the body region, spinal mobility is much reduced, and consequently, fewer muscles that interconnect vertebrae are required. However, the axial skeleton of the trunk also provides origin for several muscles of the wing and body wall. The chief vertebral series comprises the epaxial muscles M. longus colli dorsalis, pars thoracicus, and M. iliocostalis et longissimus dorsi, the latter including M. thoracicus ascendens. Some of the slips of M. iliocostalis insert on the posterior surface of the bases of true ribs; upon their anterior faces are inserted the hypaxial series of Mm. levatores costarum. Anteriorly, M. scalenus inserts on the cervicodorsal ribs. From the hypaxial musculature are also derived lateral flank muscles and a rectus sheet enclosing the body wall ventrally. The lateral system is largely supported by the ribs, consisting principally of the internal and external intercostal muscles; in the abdominal region, where ribs are lacking, this system provides the external and internal oblique muscles, and M. transversus abdominis. Ventrally, M. rectus abdominis runs from the

Musculature

pubis to the rear edge of the sternum. Posteriorly, a specialized set of muscles of axial origin controls movements of tail and cloaca. Muscles of the wing. The rigorous demands of flight impose rather narrow limits on the variability of the wing muscles. As a result, attempts to use these muscles for taxonomic purposes have generally been less fruitful than in the case of the hind limb. The largest muscle of the wings, and indeed of the whole bird's body, is M. pectoralis, averaging some 15% of the total body weight. It forms the bulk of the fleshy mass on the breast, arising from the body and keel of the sternum and surrounding areas, and attaching by a stout tendon on the crista pectoralis of the humerus. A layered or modified bipinnate structure has been described in many birds. Deep to M. pectoralis is a smaller-but still large-muscle, M. supracoracoideus. It springs also from the keel and body of the sternum, with additional origin from the coraco-clavicular membrane. Its tendon passes through the foramen triosseum, and then over the shoulder-joint to insert on the head of the humerus. Its action is to elevate the humerus, while M. pectoralis depresses it, providing the powerful downstroke of the wing. Overlying the shoulder prominence are M. deltoideus major and minor, the latter apparently absent in some hummingbirds and cuckoos. M. tensor propatagialis pars longa forms the support for the free margin of the propatagium; receiving slips from various other muscles, its tendon attaches in the carpal region. The muscle also includes a pars brevis, which inserts by various arrangements, often considered of taxonomic significance. Pars brevis is absent in several flightless birds. On the dorsal side, M. latissimus dorsi, a broad triangular sheet, arises by aponeurosis from neural spines of posterior cervical or anterior dorsal vertebrae, and inserts on the upper side of the humerus. Deep to it lies M. rhomboideus, which originates in a similar way, but inserts on the scapula. The Mm. serrati, arising on anterior ribs, also insert on the scapula. Derivatives of M. latissimus and Mm. serrati act on the metapatagium. The elbow joint is operated by flexor and extensor groups, the former including M. biceps brachii and M. branchialis, and the latter M. triceps brachii. The presence or absence of a 'biceps slip' (pars propatagialis) has been used in distinguishing major avian groups. Muscles controlling forearm movements include besides M. pronator superficialis and profundus ventrally whose combined action is to pronate the radius and thus depress the leading edge of the wing, and also the dorsal M. supinator which elevates it. In the upper arm region in addition is situated the interesting muscle M. expansor secundariorum, an unstriated muscle of dermal origin, which inserts fleshily on the bases of several proximal secondary quills. Typically it originates by a long tendon from the axillary region via a pulley device, and by a shorter tendon, absent in passerines and several other groups, from the vicinity of the elbow. This muscle has been frequently included in taxonomic diagnoses, but on present evidence is of doubtful value for such purposes. The humerus also provides origin for some long two- or three-joint muscles acting on the carpus or carpometacarpus. Among these is M. flexor carpi ulnaris, whose long tendon passes through the humeroulnar pulley, a ligamentous loop at the elbow. Finally, muscles operating the digits are of great importance in controlling the movements of primaries and alula in flight; they were inadequately studied prior to Stegmann's (1978) detailed account, which has yielded valuable evidence on the relationships of several major groups. Muscles of the hind limb. Leg muscles exhibit considerably greater variability than those of the wing, reflecting the wide range of adaptive modifications shown by the hind limb among birds. An excellent functional study is that by Cracraft (1971) on Columba livia-a species possessingall but one (M. iliofemoralis externus) of the 'formula' muscles (see below). One-joint muscles arising on the pelvic girdle and axial skeleton include femoral protractors, such as M. iliofemoralis internus, retractors (such as M. flexor cruris lateralis) and rotators, such as M. ischiofemoralis and M. obturatorius. The two-part M. caud-ilio-femoralis probably functions mainly to produce lateral tail movements. Two-joint muscles with pelvic origin include extensors of the tibiotarsus (e.g., M. iliotibialis, M. ambiens) and flexors (e.g., M. biceps femoris). Muscles originating on the femur itself are predominantly two-joint or multi-joint. Of the former may be mentioned M. gastrocnemius, which acts partly as an extensor of the tarsometatarsus, and M. tibialis cranialis, a flexor. Multi-joint muscles arising from the distal end of the femur all act as flexors of the digits, and are considered in more detail below. The

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tibiotarsus provides ongm for some single-joint muscles such as M. peroneus brevis, which flexes the tarsometatarsus, and M. peroneus longus which acts to extend it, as well as some additional multi-joint muscles acting on the digits. Finally, the tarsometatarsus itself provides origin mainly for a number of single-joint muscles which act as extensors of the digits, and in some cases provide lateral movement as well. The foundation for taxonomic applications of hind limb myology was laid in the 19th century by Garrod. In the thigh region, he stressed the presence or absence of M. ambiens, and set up a formula in which the presence of components of M. caud-ilio-femoralis and M. flexor cruris lateralis was denoted using letters as symbols. Garrod's original formula, using the letters A, B, X and Y, has been expanded by later workers, and is now made up as shown below. Although most recent pelvic musculature studies use many additional characters, amenable to multivariate or other types of analysis, the formulae are still useful as a shorthand when compiling diagnoses of avian groups. In general, the presence of 'formula' muscles is regarded as a primitive state, and their loss as derived (see CLADISTICS); large complements occur among groups regarded as phylogenetically old (e.g., Galliformes, Gruiformes), while groups of more recent origin mostly show a reduced complement. ACEFMNXY is probably typical of most passerines, while drastic reduction occurs among the Apodiformes (e.g., AEN in Chaetura pelagica), related to that of their hind limbs in general. The 'formula' muscles and their symbols are as follows: A M. caudofemoralis B M. iliofemoralis C = M. iliotrochantericus medius D = M. iliofemoralis externus E = M. iliofemoralis internus F = M. plantaris G = M. popliteus M = M. fibularis (peroneus) longus N = M. fibularis (peroneus) brevis X = M. flexor cruris lateralis, pars pelvica Y = M. flexor cruris lateralis, pars accessoria Am M. ambiens V Vinculum between tendons of Mm. flexor perforatus digiti III and M. flexor perforans et perforatus digiti III.

Garrod also drew attention to the variable arrangements of the deep plantar tendons in birds, and these, too, have been much used in systematic studies. There are three principal sets of long flexors each of which may be represented by several muscles, the hallux having but one, digits II and III having three each, and digit IV two. Inserting tendons pass to the bases of Ist, 2nd, 3rd and terminal phalanges of the toes. Those inserting on the proximal phalanx are perforated, just prior to insertion, by tendons inserting on the 2nd and 3rd phalanges and these in turn are perforated by the tendons to the terminal phalanges, so that we speak of flexores perforati, flexores perforantes et perforati and flexor perforans, the latter being tendinous branches of M. flexor digitorum longus. Mm. flexores perforati digitorum II, III and IV arise in various fashions, separately or partly fused, either from the intercondylar region of the femur or more distally from ligaments around the knee, or the upper part of the tibia and fibula, and from the tendon of M. ambiens. Mm. flexores perforantes et perforati digitorum II and III arise in similar fashion, except for the connection with M. ambiens. In many cases, the tendon to digit III receives a tendinous connection (vinculum) from that of M. flexor perforatus, denoted by 'V' in the muscle formula. M. flexor digitorum longus ('perforans') is the deepest-lying stratum, with extensive origin on the back of the tibia and fibula. Its stout tendon passes deep to the preceding tendons over the intertarsal joint, and divides into three slips that proceed to the three anterior toes. The hallux has its own deep flexor, M. flexor hallucis longus, also arising distally on the femur; this bifurcates in the metatarsal region, one part forming a vinculum to the adjacent tendon of M. flexor digitorum longus, while the other goes on to insert on the terminal phalanx of the hallux. This vinculum (not to be confused with that between the flexors of digit III) ensures that flexion of the hind toe is automatically accompanied by flexion of the other toes, although these can, through their own deep flexors, contract without involving the hind toe. Where the hind toe is absent, the tendon of M. flexor hallucis longus fuses with that of M. flexor digitorum longus. (W.e.O.H.) P.I.K.B. Boas, J.E.V. 1929. Biologisch-anatomische Studien tiber den Hals der Vogel. K.

368 Museum

danske Vidensk. Selsk. Skr., Naturvidenskab. Math. Afdel., Sere9, 1: 102-222. Bock, W.J. 1974. The avian skeletomuscular system. In Farner, D.S. and King, j.R. (eds.). Avian Biology, vol. IV. New York. Burton, P.l.K. 1974a. Feeding and the Feeding Apparatus in Waders. London. Burton, P.J .K. 1974b. Anatomy of head and neck in the Huia (Heteralocha acutirostris) with comparative notes on other Callaeidae. Bull. Br. Mus. Nat. Hist. (Zool.) 27: 3-48. Cracraft, J. 1971. The functional morphology of the hind limb of the domestic pigeon, Columba Livia. Bull. Amer. Mus. Nat. Hist. 144: 171-268. George, J.C. & Berger, A.J. 1966. Avian Myology. New York. Lakier, T. 1926. Studien tiber die Trigeminus-versorgte Kaumuskulatur der Sauropsiden. Copenhagen. Stegmann, B.C. 1978. Relationship of the superorders Alectoromorphae and Charadriomorphae (Aves): a comparative study of the avian hand. Pubis. Nuttall Orne Club, 17.

MUSEUM: an institution having nowadays the main function of preserving, for study and display, collections of specimens relating to particular subjects. Study collections of birds are usually to be found in museums or departments of natural history. The size of the museum largely determines its aims. In the largest, these may be to preserve as representative a sample as possible of the birds of the world, and to display every aspect of bird biology suited to display by exhibits; whereas in small museums the object may rather be to show mounted specimens of local species. Such local exhibits often fill in details for which there is no room in the more comprehensive displays. Public interest is catered for by the education and recreational side of a museum's functions. The objects, captions and graphics of a traditional exhibit allow a visitor wide latitude in depth and speed of study, which is reduced when recorded talks are used. This tendency may be carried much further by reactive displays which put over effectively a limited number of concepts. The information constantly available may be supplemented by guided tours, lectures, demonstrations, classes and film programmes, while portable exhibits may be circulated to schools and other institutions. While display and teaching are the chief concerns of most museums, the great natural history museums are primarily research institutions in which much more extensive specialized collections, supported by libraries and technical facilities, provide unique opportunities for research by their own staffs and visiting workers. Early collections were mainly received from individuals, since the first 'cabinets of curiosities' were founded by wealthy private collectors; but eggshells are now the only bird specimens subject to the collector's mania, and those who collect other material do so for the furtherance of knowledge. Most private collections have now found their way into museums, and collecting is increasingly purposive, whether as a technique of research or to fill gaps in the museum's own collections. Improving the retrieval of information through better arrangement of the specimens has been a powerful impetus to research into natural classifications (see CLASSIFICATION; SYSTEMATICS; TAXONOMY), which is one of the principal fields for study in natural history museums. Much staff time is spent in protecting the collections from physical and biological injury, which has resulted in the application of new techniques, and in refining their arrangement and documentation for the benefit of research workers. Research specimens of birds used to consist almost entirely of study skins, simply stuffed in the field and presenting little more than the external appearance, but carrying essential field information on their labels. Though laborious to prepare, skins are easy to transport, store and examine. With their data, they have been of the greatest importance for studies on classification, variation, seasonal changes and distribution; and are still the principal material for investigating relationships at the species level. Other techniques, such as freeze-drying, for producing comparable specimens offer great advantages, but technical difficulties have so far prevented their widespread use in the field. Since at the species level the classification of birds is uniquely well founded, the emphasis is now on higher classification for which anatomical specimens are more important. Collections of disarticulated study skeletons and of birds preserved in fixatives, though still small in comparison with skin collections, are now growing much more rapidly. New techniques of research (see DNA AND PROTEINS AS SOURCES OF TAXONOMIC DATA) can involve the formation of what are effectively new types of museum collection, like that of egg-whites at Yale. Archives of recorded bird calls, as at Cornell, are primary research material rather than libraries, and important for taxonomic as well as other studies.

The promising new technique of electrophoresis using feather proteins enables the large skin collections to be used for biochemical taxonomy with little damage. Other types of bird specimen are mainly important to aspects of biology other than taxonomy. Eggshells with their data show where and when a species has bred, and can provide material for the analysis of changing pollution. Nests encapsulate the movements used in building them. Preserved gut contents and gonads contribute to knowledge of diets and of breeding cycles. The maintenance of such a range of collections adds to the problems of curation, yet it may be desirable to maintain parallel collections even for a single type of specimen. For example, TYPE SPECIMENS may be segregated from the general skin collection because of their unique importance to nomenclature, as may the skins of extinct and endangered birds. Much taxonomic research concerns variation, whether for its own interest or to establish norms. Birds of one population vary individually between age classes and sexes, and from season to season and may also be polymorphic. Populations of most species vary geographically, and sometimes with altitude. Clearly, to be able to provide a reasonable statistical sample of (say) adult males in fresh breeding plumage from each of many sample areas, over the whole range of one of the 9,000 bird species, requires very large total collections. The material in one museum is often insufficient for a particular study, and the natural history museums of the world are continuously engaged in lending specimens for research. Large collections have been made for special studies, but this method may be wasteful and better replaced by the recording of data from birds which are captured and released. Some museums accept extensive data for permanent preservation. Though anatomical variation is potentially important, its study has scarcely begun because anatomical collections are still comparatively small. Besides their use for modern studies, skeleton collections are essential for the interpretation of older material. Fragments from archaeological sites and Quaternary deposits provide information on former distributions; but it is the rapidly increasing knowledge of bird fossils from the Tertiary which is resulting in fundamental reassessments of evolutionary history and higher classification. Museums became important as more than mere cabinets of curiosities towards the end of the 18th century, when great national collections such as the Museum National d'Histoire Naturelle in Paris and the Riiksmuseum van Natuurlijke Historie in Leiden were dominant. In Britain this was the era of the wealthy private collector, and the British Museum's natural history collections (separated as the British Museum (Natural History) about 1881) only gradually achieved pre-eminence as a result of amateur and official collecting throughout the Empire. Today the United States have the bulk of the specimens in the world, held in dozens of national, state, university and independent museums, whose ornithological staffs comprise the majority of all avian systematists. However, there are important collections and active research staffs throughout the developed world, while many developing countries are actively enlarging or founding their own. In numbers of specimens, the largest collections are those of the British Museum (Natural History) and American Museum of Natural History, since they each have about a million study skins, while the United States National Museum of Natural History is actively expanding exceptional anatomical collections. Several British museums have important research collections of British birds, while for the birds of the world the most important after the BM(NH) are probably the Manchester Museum, Merseyside County Museum, National Museum of Wales, Royal Scottish Museum, and University Museum of Zoology, Cambridge. Some local museums have been designated as biological records centres under a national organization. While some of the functions of this organization are already carried out, for birds, by ornithological and natural history societies, the local centres should make a valuable contribution to planning and conservation. (J.D.M.) I.C.J.G. Banks, R.C., Clench, M.H. & Barlow, J.C. 1973. Bird collections in the United States and Canada. Auk 90: 136-170. Parkes, K.C. 1963. The contribution of museum collections to knowledge of the living bird. Living Bird 2: 121-130. Steward, J.D. 1980. A summary of local environmental record centres in Britain. Museums J. 80: 161-164. Zusi, R.L. 1969. The role of museum collections in ornithological research. Proc. Biol. Soc. Wash. 82: 651-662.

Music, birds in

MUSIC, BIRDS IN: regarded here as an avian element in human culture. There are two other articles on this subject: Fisher (1966) and Scholes(1970). These between them list most of the references to birds in the musical repertoire to the end of the 19th century but few more recent ones. This article, therefore, while offering a necessarily selective survey of bird-inspired western music, treats later developments more fully. Musical inspiration derives from: (1) songs and calls; (2) line and movement; (3) literary sources; and (4) fabulous and mechanical birds. Treatment may be direct sound-imitation; symbolic; impressionistic. In the last few decades, (5) 'concrete' bird music (recorded bird sounds in intact or modified form combined to create musical works) has evolved into a category of its own. Of the three methods of treatment possible in vocal or instrumental music, direct sound imitation, though present in even the earliest works, has perhaps made the greatest progress and impact in recent years. When birds are used as symbols, there may be no obvious reference but an appropriate 'atmosphere' is generated. Impressionistic treatment, despite its lack of definition, is probably the best vehicle for inducing a felicitous response, especially in the ornithologist who may justifiably be irritated by the inadequacy of human voices and instruments when they attempt to imitate all but the simplest bird calls. All these three musical approaches have, however, appealed to composers of all periods, whatever the source of their inspiration (apart from the line and movement of birds which can only be treated impressionistically). Indeed, they are often combined in the same work. The four voices of the 13th century canon 'Sumer is icumen in', the earliest known English secular composition, imitate the Cuckoo's call and it has been musically echoed down the centuries. Ianequin's 'Song of the birds' from the early 16th century combines a realistic Cuckoo together with trilled rrr's and fast staccato notes which merely hint at their living sources. Orlando Gibbons, a century later, in his madrigal 'The Silver Swan' takes this mute bird, which dying 'unlocks her silent throat' in wise utterance, as a symbol and the gravely flowing vocal lines mirror the slow, dignified movement of a swan floating on placid water: the beginning of a long tradition of symbolic swan music. Impressionistic use of bird sounds and movement has been continuously represented in instrumental works from, say, Vivaldi's 'Four Seasons' in the early 17th century, to Vaughan Williams's 'The Lark Ascending' and the compositions of Edward Cowie and Trevor Hold in the 20th. 1. Songs and calls. An index of species shows a great variety, with several favourites. The Cuckoo, with its familiar diatonic intervals, is the obvious point of departure for a composer wishing to introduce a pastoral flavour; Beethoven, in his Sixth Symphony, the most notable among them. But the bird also stimulated a number of compositions exclusively devoted to it: Couperin, Pasquini, Vivaldi and Daquin in the 17th and early 18th centuries, for example. The Nightingale, another favourite but more difficult to represent, had Janequin and Couperin among its early devotees and Rameau (16831764) included an 'Air du Rossignol' in his opera 'Hippolyte et Aricie' with both vocal and instrumental imitation. Handel (1685-1759) made the bold attempt to combine Cuckoo and Nightingale in an organ concerto, and these two species and others.are thought to be represented in Haydn's (1732-1809) Ope 33, no. 3, nicknamed the 'Bird Quartet'. In the famous Toy Symphony, formerly attributed to Haydn, Quail, Cuckoo and Nightingale figure on the toy instruments. It is now known that this composition is part of a work by Leopold Mozart; the toy instruments added, possibly by Joseph's younger brother Michael Haydn. Later admirers of the Nightingale have included Glinka, Mendelssohn, Liszt, Balakirev, Grieg, Granados, Ravel and Milhaud. Respighi (1879-1936) arranged some 17th and 18th century works in his orchestral suite 'The Birds' whose subjects are Cuckoo, dove, hen and Nightingale. Doves, specific or unspecified, are numerous (see below) but the domestic hen is less usual, though one of Haydn's symphonies is called 'La Poule'. Humperdinck (1854-1921) in 'Hansel and Gretel' has a cock which diverts us with ki-ke-ri-ki in the English translation; he also has a vociferous Cuckoo and a Skylark, but this is a bird of vocal whimsy. Larks, too, go through the centuries from Ianequin to Messiaen. Other passerine species less commonly represented include the Goldfinch (Vivaldi), Linnet (Couperin, Haydn, Rachmaninov), Robin (Lalo and Peter Warlock), Swallow (Dvorak, Pierne, Tschaikovsky), Wagtail (Britten) and, exotically, the Scarlet Tanager (Dvorak's American String Quartet). Remarkably, the Blackbird attracted little attention until the present century. An unpromising species, the Magpie, is the subject of a

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Mussorgsky song; and the side-drum roll in Rossini's 'La Gazza ladra' could be an imitation of Magpie chatter. Among non-passerines, there are songs about 'A greedy hawk' and 'Compel the hawk to sit' by William Byrd (1543-1623); and Thomas Weelkes (c. 1575-1623) composed the madrigal 'A Sparrowhawk proud'. Haydn has a song about a Blackcock; Beethoven (Sixth Symphony) and Schubert (C major Quintet) have Quails, and Mussorgsky an escaped parrot in the fifth act of 'Boris Godunov'. Prokofiev, in 'Peter and the Wolf', asks an oboe to give a duck squawk. Numerous other nonpasserine species used by composers are treated more fully below. Finally, in this summary of species representation, Boccherini (17431805) has a collection in 'The Aviary'-the title of a string quartet. From the late 19th century to the mid-20th, continental Europe produced several fine composers of large-scale works whose careers overlapped and all of whom to some extent mirrored in their music the countryside of their birth. The great Austrian symphonist Anton Bruckner (1824-1896) was said to 'reflect ... the voice of Nature itself' in his Fourth Symphony. The only overt imitation occurs in the first movement; this is a song (more likely two song-types strung together) of a Great Tit. Of all direct imitations of bird song this is one of the most authentic and appealing, yet it emerges as an integral part of the movement, never a mere decorative accessory. But it is true to say, as of others among these composers, that Bruckner's music is informed by natural sounds, including birds, rather than formed from them. Mahler (1860-1911) made use of birds, although their singing so distracted him when composing that he was known to shoot them. Yet his musical ear appreciated the Chaffinch call zink zink, thus transcribed in his own poem for one of his 'Songs of a Wayfarer'. A Cuckoo, singing a perfect 4th rather than the ubiquitous major and minor 3rds, pervades much of his First Symphony along with some unspecified bird song. Another Cuckoo and a somewhat capricious Nightingale turn up in the Third Symphony. The slow section of 'The Drunkard in Spring' from 'Das Lied von der Erde' includes bird calls and chirrups to tell the Drunkard of the arrival of spring and the last movement, 'The Departure', contains music strongly evocative of the natural scene in which the two friends say farewell. Although Sibelius (1865-1957) was particularly responsive to bird sounds, he made little explicit use of them in his music. Yet he describes the call of the Crane as 'The leitmotiv of my life' and noted on Villa-Lobos's music 'One can hear that he was brought up in a quite different bird world from me' (Levas 1972). His devotion to swans is evident in the enraptured poignancy of his 'Swan of Tuonela' whose long lament is played by the cor anglais. Most swan music represents the Mute Swan Cygnus olor, a species not established in Finland until 1934. 'The Swan of Tuonela' was composed in 1893 and it was the migrating Whooper Swans C. cygnus that Sibelius used to greet each year when they were resting on a lake near his home. In the incidental music from Kuolema (where we also find the wellknown Valse Triste) there is a 'Scene with Cranes' in which the birds' calls are imitated by two clarinets; and the concert suite from his music for Strindberg's 'Swanwhite' includes 'Peacock' and 'Listen, the Robin sings'. The Danish composer Carl Nielsen (1865-1931) and Bela Bartok (1881-1945), deeply committed to his native Hungary (though his birthplace is now in Romania), were likewise musicians with an informed appreciation of bird sounds who mostly made implicit rather than explicit use of their carefully studied material. Nielsen chose an unusual avian model in his 'Song of the Siskin' for chorus. 'The First Lark' and 'Springtime on Fyn' are other choral works with bird associations and there is a hint of a Cuckoo in the 'Helios' overture. Basically, however, the loving perception he accords to birds, in his description of their special 'accents' on his native island of Fyn (in his essays 'Living Music'), is transmuted into orchestral colours and time-patterns, especially perhaps in his Wind Quintet. Bartok produced his most overt nature music only after he had left Hungary for permanent exile in the United States. Biographers testify to his exact knowledge of all natural sounds and his unusually acute hearing. A buzzing, humming sound as of insects is often his way of suggesting a natural background. In 1943, already suffering from his terminal illness, he was sent to relax at Asheville, North Carolina, where he went for long walks and painstakingly noted down the songs of an avifauna that was new to him. When he came to write his last work, the

370 Music, birds in

Third Piano Concerto, this material was transformed (particularly in the second movement) into the seemingly inexhaustible flow of motifs in this splendid work. In contrast, Olivier Messiaen (b. 1908) brought precise bird vocalizations to the musical masses. A prolific composer and a good ornithologist, he has incorporated the songs or calls of 260 species from six faunal regions in at least 10 of his major works. It is notable, however, that when he contrasts his skilfully contrived overt imitations with impressionistic settings of the habitat-as in the 7-volume 'Catalogue d'Oiseaux' for solo piano-attention and imagination are stimulated. But in those works composed entirely of songs and calls, for example 'Reveille des Oiseaux' for piano and orchestra, attention is taxed to the point of confusion because of the polyphonic nature of the work, wherein as many as 21 species are presented simultaneously at the climax of the dawn chorus. From such complexity, Messiaen turns to extreme simplicity in his 'Merle Noir' for solo flute with piano accompaniment. This does not aim at complete fidelity: the duration of the pauses between the phrases must be reduced to achieve continuity when there is no answering bird or background song; but it is a distillation of the species' song and a convincing work of art. Messiaen's other works devoted to, or incorporating bird sounds include Oiseaux Exotiques, La Fauvette des [ardins, Chronochromie, Couleurs de la Cite Celeste, Et Expecto Resurrectionem Mortuorum, La Transfiguration and Meditations sur la mystere de la Sainte Trinite. In 1974 Messiaen completed 'Des Canyons aux Etoiles', a 96-minute work which incorporates the songs of 60 species from Utah and the Hawaiian Islands. There is a long tradition of bird song representation in French music and Messiaen's immediate predecessor and, maybe, his inspirational springboard, Maurice Ravel (1875-1937), has received little credit for his imaginatively unique contribution to it. In the scene 'Lever de Jour' from the ballet 'Daphnis and Chloe', three solo violins, piccolo and flute evoke the unspecified birds who greet the rising sun. They are followed by two shepherds playing pipes (piccolo and E flat clarinet). In no other musical work are we so delicately reminded of the tenuous borderline between avian and human music. 'L'enfant et les Sortileges', a brief, bewitching opera, ends with a garden scene at night with only a child and the animal denizens taking part. Ravel, master of orchestration, requires a slide flute for his Tawny Owl. He abandons most of the conventional but inaccurate trills dealt out to Nightingales and gives his bird (piccolo) repeated notes and tremolo effects. When a soprano voice sings another Nightingale part there is little attempt at imitation and the bird has a lyrical descant above the other animal voices. In 'Ma Mere l'Oye', a suite of piano duets subsequently extended and orchestrated for a ballet, some unorthodox little birds cheep (complex violin harmonics) as they peck up the trail of crumbs laid by Tom Thumb, and a very orthodox Cuckoo calls in the same piece. Ravel's most serious essay in bird vocalization is his impressionistic 'Oiseaux Tristes' for piano-an evocation of 'birds lost in the torpor of a forest during the most torrid hours of summer'. No other composer has achieved such a convincing representation of the sounds of birds in conditions where they tend to be vocally quiescent. The only firm evidence about species comes from the report of a friend which tells how Ravel went to the forest to listen to a Blackbird. In this work it sings precisely as Blackbirds do in such circumstances---sporadically and tending to repeat a single phrase. All else is implied, but the pairs of slowly repeated single notes can only be a Turtle Dove: a sudden explosion of alarm calls suggests a Chaffinch, followed closely by a single abbreviated Wren song as elicited by disturbance. Repeated drooping major and minor thirds suggest a slow and indeed a 'sad' Cuckoo. A three-line cadenza near the end of the work hints at subsong from several species and merges finally into the continued murmuring of the Turtle Dove. Four birds appear in Ravel's song cycle 'Histoires Naturelles'. The noble, if vain, demeanour is depicted in 'The Peacock'; contrary motion black key glissandi represent the spreading tail; and the harsh cry is sung Leon, Leon with a properly dissonant accompaniment. 'The Swan' looks back to Saint-Saens' (and Pavlova's) famous bird, but with sophistication and irony. Twenty-three bars of pianissimo writing express the awe and delight of a fisherman whose rod is graced by 'The Kingfisher'. And in conclusion and contrast 'The Guinea-fowl' is conjured up, irascible and raucous, scratching in the soil and bathing in the dust. Yorkshire-born Frederick Delius (1862-1934) lived not far from Ravel

at Grez-sur- Loing. He remarked to Elgar that the song of the birds was the greatest music of all, an explanation, perhaps, for his uniquely tender treatment of the subject of 'On Hearing the First Cuckoo in Spring'. Even greater was his love and sympathy for the pair of Mockingbirds and all that they symbolize in Walt Whitman's 'Sea Drift'. This setting for baritone, chorus and orchestra must be the most extended (24 minutes) eulogy for a living, singing bird and threnody for a dead bird-the singer's mate-ever conceived. Much bird music has come from the pen of Benjamin Britten (1913-1976). In the children's opera 'The Little Sweep' their voices give vivid renderings of Chaffinch call notes, the Heron, Tawny Owl and Turtle Dove. The Turtle Dove appears again (flutter tonguing on recorder) when Noah launches it from the ark in 'Noyes' Fludde', and yet again in one of Polly's airs in his realization of 'The Beggar's Opera'. In another air the flight of the Swallow is cleverly suggested by the flute. 'The Spring Symphony' has a merry Cuckoo and a quire of birds; piccolos represent the flight of the Skylark in 'A Midsummer Night's Dream'; and the fluttering of an unspecified wagtail comes in 'Winter Words': a cycle of Hardy poems which also includes 'Proud Songsters'. There is music for wild geese in the operetta 'Paul Bunyan' and an evocative reiterated Curlew motif in 'Curlew River'. 'Our Hunting Fathers' contains an angry 'Dance of Death' for Ravenscroft's 'Hawking for the Partridge'. Amongst British composers, Trevor Hold (b. 1939) has published a study of bird vocalizations and their notation (Hold 1970) and has also used songs and calls, both explicitly and implicitly, in his works. Those in the first category include 'The Unreturning Spring', a song cycle for two voices and small orchestra wherein the Interlude before the final song has a 'mobile' of Song Thrush (flute), Corn Bunting (oboe), Reed Bunting (clarinet), Nightjar (bassoon) and Tawny Owl. Implicit (unspecified) song abounds in his instrumental and orchestral works, notably 'The Blue Firedrake', 'Calendar', 'Time Passes', 'Belfry Music' and 'Clare's Ghost'. In Hold's 'Signs of Winter', based on John Clare's poem, a solo horn represents ducks flying up from a pond. Edward Cowie (b. 1943) has found inspiration in the environment of north-west Lancashire for several works composed in the 1970s. 'Gesangbuch' (Song book), in two versions, a series of four tableaux for voices and instruments is, in Cowie's words, a response to 'particular aural and visual signals' of these open, often marshy expanses. In one of them, 'Hest Bank' (1974), fragments of bird names and landscape features occur in his own text for the voice parts. Of contemporary music derived from bird vocalizations obtainable only on disc or tape, outstanding is 'Calling Down the Flevo Spirit' by Kees Hazevoet and Aan Bennink (Snipe Records, 7678, Amsterdam). There is no score because the performers improvise brilliantly and imitate six species with some startling verisimilitude; the titles are Stone Chattin', The Woodcock, King of Saxony, The Roller, Snipe Drumming and Mot-mot. Beyond Europe, Radio New Zealand leads with a disc (and cassette) of distinction: 'Children of Tane'. Tane is the Maori God of Nature and the birds are his children. Music, words and performance are all by Sydney (Hirimi) Melbourne, a member of the Tuhoe tribes (the people of the mist). Fourteen songs emerge from recordings of the birds' own voices and epitomize native mythology and imitation in the Maori tongue-ideal for the purpose with its many vowel sounds and soft delivery. 2. Line and movement. Sources of inspiration in the shapes and forms of birds at rest, hovering or in flight, and the visual satisfaction they offer, are more difficult to identify than aural sources. Perhaps Vivaldi, in his Flute Concerto '11 Gardellino' , was not as much stimulated by the Goldfinch's twittering, musical song, as by its rapid movements. Certainly Vaughan Williams in 'The Lark Ascending' was particularly sensitive to flight. In some 19th century ballet music, composers (notably Tchaikovsky) were concerned not only to represent birds in movement but to support the dancers when the choreography required emulation of flight. Few can remain unmoved by the artistry achieved by Tchaikovsky and Petipa in the 4-act 'Swan Lake'. But slighter bird works arising from the same composer-choreographer collaboration may arouse even stronger associative feelings on account of their light, delicate texture and the formal scaling down to size and rapidity of movement more compatible with our apperception of birds in general. In 1964 a one-act ballet was based upon courtship display. Entitled simply 'The Display' its subject is the Lyrebird with music by the Australian Malcolm Williamson (b. 1931), Master of the Queen's

Music, birds in

Musick, and choreography by Robert Helpmann. Another recent ballet 'Eagle's Nest' (music by Kamen and choreography by Falco) had its premiere at La Scala, Milan. The eagle portrayed therein is reminiscent of the magnificent Golden Eagle interpretation by the Indian dancer, Ram Gopal, in the 1940s. These are but a few examples from a field worthy of greater consideration; others will be found in section 4. Much 'descriptive music', when birds are used as symbols or to create the atmosphere of a woodland, a particular season or time of day, is evidently inspired by visual as well as aural impressions of birds. Most 'swan' music, for instance, derives from the bird's literary and legendary appearances and the solemn atmosphere created by composers as diverse as Orlando Gibbons, Wagner, Ravel, Sibelius and Prokofiev seems to pay homage to the visible majesty of this great bird. Prokofiev's 'White Swan', composed in 1910 but not given its first performance until 1980 in a version edited by Rozhdestvensky, is a setting for female voices, horn and strings of a poem by Konstantin Bal'mont. In a few minutes of grave, gentle music, it presents the swan as 'a serene symbol of feminine beauty'. Richard Strauss (1864-1949), in his 'Four Last Songs', incidentally illustrates the impossibility of strict categorization of bird-inspired music. In these settings of poems by Hesse and von Eichendorff, two Skylarks rise, hover and ultimately bring '1m Abendrot' (In the Evening Glow) to a close with their tremulous music and flight. The words of Fruhling (Springtime) refer merely to 'bird song'-at which point the vocal line soars above the orchestra in a long melisma. 3. Literary sources. These include all vocal settings of poetry as well as folk tales, legends and stories in which actual (as opposed to fabulous) bird species figure: many works of literary inspiration have been discussed in section 1. Whether poem or legend was the first source of inspiration or whether the composer was attracted to it by an interest in birds is open to argument, or biographical evidence, in individual cases. After the Bible, the earliest inspirational text is probably 'The Birds' of Aristophanes (455-375 Be), treated by at least seven composers. Many legends have contributed to opera plots or tone poems, and forest or pastoral episodes in an even wider range of operas and ballets demand impressionistic treatment of bird sounds and movement as part of the orchestral scene-setting. Neatly spanning the main period of European musical development 'The Suffolk Owle', originally a madrigal by Nicholas Vauter (born c. 1590), has a modern setting in the cantata 'Voices of Night' by Franz Reizenstein (1911-1968). Cock crows dramatically break into the sombre Passion music in the oratorios of Schlitz and Bach and biblical inspiration also evoked bird music in Haydn's 'The Creation'. Handel, in 'Acis and Galatea' and in many pastoral themes in his operas and masques, shows his awareness of bird song, and is said to have 'imported live birds into his operas'. (A 20th century Ashton ballet to music by Messager also brings real birds on stage to supplement the dancers of 'The Two Pigeons'.) German lieder, so many of them settings of 'open air' poetry, are less productive. Only an occasional hint of bird song, perhaps a grace note in the accompaniment, is used by Schubert and Brahms. Wagner (18131883), drawing on medieval legends for his opera plots, gives us the swan symbolism of 'Parsifal' and 'Lohengrin' but it is 'The Ring' cycle and the Siegfried Idyll that bear the strongest testimony to the enrichment of his music by recreated experience of bird sounds. Liszt (1811-1886) also turned to legend in his pianistic tribute to St. Francis of Assisi preaching to the birds. Trills and arpeggio passages punctuated by brief, often staccato motifs represent the birds which are temporarily silenced by a gentle tenor recitative suggesting the voice of the Saint; this appears in the bass at a climactic point, then a long diminuendo leads back to bird song which drifts into near silence at the close. The impression of song and flight may owe inspiration to the Larks (or in one source the Swallows) which are said to have comprised much of the flock at St. Francis' sermon (see Armstrong 1973). Dvorak (1841-1904) was constantly and openly inspired by bird song (using it thematically, for example, in two quartets and the 8th Symphony). He was a pigeon fancier but the species of his symphonic poem 'The Wild Dove' (Czech Holoubek) must be the Stock Dove, whose persistent cooing above her husband's grave drives an erring young widow to suicide. The complex orchestration-flutes, oboe, high repeated notes on harp and some muffled drumstick strokes on a cymbalis peculiarly apt, as is Alec Robertson's description of the dove as 'self-righteous'! (Robertson 1964). The Skylark, Cuckoo, Swallow and

371

House Sparrow are subjects of some of Dvorak's songs. Schoenberg (1874-1951) was also inspired by dove song. The species of his 'Song of the Wood Dove' from the great choral-orchestral work 'Gurrelieder' seems to be the Woodpigeon if judged by the time patterning of fragments in the introduction and coda. But the mezzosoprano's line is suffused with dove-like conjunct intervals as she declaims the death of Tove, tragic figure of Danish legend. (It appears to be fortuitous that the German gurren means to coo.) Schoenberg is again sensitive to birds in his setting of Petrarch's 'When little birds weep'. Leos Janacek (1854-1928), from Moravia, was steeped in the music of animal sounds which he notated as meticulously as he did the lines of human speech. Hence it is not surprising that in his captivating nature opera 'The Cunning Little Vixen' birds are prominent: there are a Cuckoo, Raven, woodpecker (xylophone), a Barn Owl, a Jay and a flock of Starlings. A domestic cock presides over his harem which clucks conventionally while their leader astonishes us and, no doubt, her sister hens with egg-inspiring trills and embellishments! 'Katya Kabanova' has bird music which evokes song, flight and the beating of clipped wings. In his last opera 'The House of the Dead' (set in a Siberian prison camp and based on Dostoyevsky's novel) Janacek introduces, ironically, a Cuckoo and, symbolically, an eagle: the Czar of the forest. The captive, wounded bird, its early attempts to fly and ultimate flight to freedom, symbolize the plight and hopes of the prisoners. Among his small choral works are 'The Dove' (Holubicka) and 'The Wild Duck'. 'The Screech (Barn) Owl' and 'They Chatter like Swallows' are included in the piano suite 'The Overgrown Path'. Rimsky-Korsakov (1844-1908), like Janacek, carefully notated bird vocalizations and was so scrupulous as to explain that the song of his pet Bullfinch had to be transposed down a tone 'for the convenience of the violin harmonics'. This bird's song and other bird voices can be heard in his operas 'The Snow Maiden' and 'Mlada'. Further 20th century illustrations of literary inspiration (apart from the Britten works referred to in section 1) include Carl Orff's 'Carmina Burana', drawing on medieval sources, in which a Swan (again! but this time dead and roasted) finds tenor voice to lament its fate; and, in strong contrast, Peter Warlock's setting of Yeats' poem 'The Curlew' has an evocative flute line as part of the accompaniment. 4. Fabulous and mechanical birds. These are sparse in the musical repertoire wherein Schumann's (181~1856) 'Prophet Bird' is probably the best known. Oddly, the Phoenix attracted little early attention, though there is an unaccompanied concerto for 4 bassoons by Michel Corrette (1709-1795). In the last 20 years, the bird has given its name to several works, including 'The Phoenix and the Turtle' , an opera by Thea Musgrave (b. 1928). A near approach to the Phoenix is Stravinsky's (1881-1971) 'Firebird', composed for Diaghilev's Russian Ballet and choreographed by Fokine. The same composer based his opera 'Le Rossignol' on Hans Andersen's 'The Emperor and the Nightingale'. Subsequently, Diaghilev had it adapted as a ballet 'Le Chant du Rossignol' in which the 'real' Nightingale takes fright at the crude humming of the mechanical bird but ultimately returns to revive the dying emperor with its song. Rimsky-Korsakov's 'Golden Cockerel', yet another creation for Diaghilev's Russian Ballet, approaches the fabulous (as does Wagner's Forest Bird), in its superavian abilities, although its crowing sounds real enough. Maeterlinck's (1862-1949) play 'The Blue Bird' also inspired works by Humperdinck and Norman O'Neill. In Ravel's opera 'L'Heure Espagnole' there is a fabulous bird 'L'Oiseau des lIes' (played by the piccolo) and a mechanical one: a little toy cock whose diminutive but shrill crowing is reproduced by the reed alone when removed from a sarrusophone. This work, set in a clockmaker's shop in Toledo and concerned with the amorous escapades of the wife of the absent owner, also gave Ravel double-edged scope for Cuckoos, both vocal and instrumental! In the very different tradition of Brazilian folk music and legend, Deitor Villa-Lobos (1887-1959) composed his early symphonic poem 'Uirapuni': an enchanted and enchanting bird, worshipped as the King of Love. The story, of his own compiling from several legends, tells how the mellifluous nightly song of the bird lures people into the forest in search of it. An arrow-shot through the heart from a beautiful maiden transforms the bird into a handsome young man. But he, shot once again by an ancient Indian nose-flute player, turns back into a bird and flies away, singing, into the forest depths. The rich orchestration, which includes Latin American percussion instruments and violinophone (a

372 Music, birds in

violin with a horn attached) exploits fully the dramatic episodes of the story and the peaceful, rippling phrases of Uirapuni's song. In the Paul Schwartz recording this elusive bird has an exquisite and varied song such as Villa-Lobos could not have heard. S. Concrete music. This most recent development, only possible since the advent of the tape recorder, demands a brief separate section because bird voices not only fire the composer's imagination but are the music itself. However, contemporary composers had a predecessor in Respighi who, in his tone poem 'The Pines of Rome', presented an early gramophone record of a real Nightingale song. His treatment is so subtle as to debase neither the music nor the song of the bird. In America, James Fassett created his 'Symphony of Birds' entirely from recorded vocalizations (Stillwell Recordings, Ficker, USA). Less ambitious is 'Symphony of the Birds' by johan Dalgas Frisch (MGM Records, New York) which comprises recordings of Brazilian birds, with background music which mayor may not please the listener. But predictably Swedish Radio, and the composer Karl-Birger Blomdahl (1916-1968), take precedence with 'Altisonans'. Blomdahl's ideas originated from an observation by the physicist Ludvik Liszka that certain satellite signals exactly resemble the song of the Redwing. The composer then blended unmodified bird voice recordings with 'space' sounds: satellite signals and magnetic storms re-recorded at various playback speeds. The result is impressive and appropriately unearthly. Coincidentally, 'Children of Tane' (see Section 1), otherwise so different in conception, incorporates thunder storms. Finally, and to solace the mind which may recoil from some contemporary bird music, there is a slender vignette by Percy Buck (18711947): 'The Blackbird's Song', a three-part setting for female voices of Henry Kingsley's poem. Only its unashamed romanticism in an age of rampant eclecticism can explain its neglect for, within melodic and harmonic enchantment graced with delicate traces of its song, the bird pleads for the forgiveness of man's sins and in so doing sings itself to sleep. J .H-C. and R.E.J. Armstrong, E.A. 1973. Saint Francis: Nature Mystic. Berkeley. Fisher, J. 1966. The Shell Bird Book. London. Hold, T. 1970. The notation of bird-song: a review and a recommendation. Ibis 112: 151-172. Levas, S. 1972. Sibelius: A Personal Portrait. London. Robertson, A. 1964. Dvorak. London. Scholes, P. 1970. Oxford Companion to Music. London.

MUSKEG: an environment, consisting of grassy bog, characteristic of much of northern Canada. MUSOPHAGAE: MUSOPHAGIDAE: suborder and family of (see TURACO).

CUCULIFORMES

MUTATION: see

GENETICS.

MUTTON-BIRD: local name for various species of petrel (Procellariidae); applied in New Zealand to the Sooty Shearwater Puffinus griseus, and on the southern coasts and islands of Australia to the Short-tailed Shearwater P. tenuirostris (see PETREL). The young of both species are in these areas collected commercially in large numbers for human consumption. The latter species is known as the Whale-bird in Alaska, which it visits during the northern summer. MYCTERIINI: see STORK. MYIASIS, WOUND: the presence of maggots in a wound on a living bird. MYNAH: substantive name of various Asian species of Acridotheres, Gracula, and Sturnus (see STARLING). MYOCARDIUM: see

HEART.

MYOLOGY: the scientific study of muscles (see MUSCULATURE). MYTHICAL BIRDS: see

FABULOUS BIRDS.

MYZA: substantive name of the 2 species of Myza of Celebes (Sulawezi) (for family see HONEYEATER). MYZOMELA: substantive name of some species of Myzomela, a large genus of Australasian and Pacific island HONEYEATERS. MYZORNIS: substantive name of Myzornis pyrrhoura of south-east Asia (see BABBLER).

N

common speech. Such names, if unsatisfactory, are more susceptible of deliberate change. In particular, it seems to be good practice to displace such a name in favour of one that is widely current in some part of the world where the bird is well-known; thus what was once the 'Buffbacked Heron' Bubulcus ibis of earlier British bird books was known to English-speaking people in Africa and Asia (more appropriately) as 'Cattle Egret' and this has become common usage. Again, in the British Isles, the English names used in North America may well be preferred for species that are merely stragglers from that continent. Names for species and subspecies. English names are primarily the names of species. This follows naturally from the fact that subspecific forms are usually indistinguishable in the field, except in some cases by skilled observers; they can therefore have no names in common speech. Where it is desired to refer to a subspecies (or race) by an English name, this should consist of the name of the species prefaced by a qualifying adjective or adjectival phrase. Such compounded names for races are nearly all of comparatively recent origin; and indeed the desirable occasions for using them seem to be much fewer than some current practice would suggest. Subspecies can be referred to either by their scientific names, as befits a technical concept, or by such expressions as 'Northern race' in relation with the English name of the species. There are a few inevitable exceptions, where subspecies are so distinct in appearance that they have acquired separate English names in common speech. If such names are firmly embedded in the language, as where 2 races of M otacilla alba are known respectively as 'Pied Wagtail' and 'White Wagtail', it seems impossible to do otherwise than accept the situation. Unfortunately, this means that there is no English name covering the species as a whole; and this in turn involves the invention of additional English names for any forms of it other than the 2 in question. Initial capitals. Whether or not to use capitals for the initial letters of the English names of species is a controversial point. Ordinary literary usage would prefer small letters, and some ornithological publications follow this. More commonly it is felt that, for scientific purposes, there are advantages in the use of capital letters. For one thing, references to particular species can be more easily picked out on a page. For another, certain ambiguities are avoided; thus, 'a Little Gull' can refer only to LaTUS minutus, whereas 'a little gull' might mean a gull of any small species. When initial capital letters are preferred, they are used for each main term of the name but not for the second element of a hyphenated compound. Capital letters are in any event not given to English names when these are used in a general rather than a specific sense, e.g. 'gulls'. Hyphenation. It has in the past been a frequent practice in ornithological publications to hyphenate two elements of a name where this consists of a noun preceded by a noun used as an adjective; but not to insert a hyphen between a true adjective and a following noun. This is a tiresome convention, because it involves e.g., for various tits Parus spp., writing 'Marsh-Tit' on the one hand and 'Blue Tit' on the other. Moreover, an exception tends to be made when the adjectival noun is the proper name of a place, as in 'Sandwich Tern', and this further complicates the procedure. There seems to be nothing in ordinary English usage of the present day to demand such a rule as that mentioned above. 'The hyphen is not an ornament; it should never be placed between two words that do not require uniting and can do their work equally well separate' (Fowler). The present tendency happily seems to favour the suppression of all unnecessary hyphens, including especially those that have been inserted merely because the word before it, used adjectivally, happens to be a noun. A hyphen is unnecessary between any two words of which the second would naturally be used for indexing. On the other hand, some hyphens are made necessary by the sense, unless the two elements can be written as a single word; 'Oyster-catcher' is a case in point, as 'catcher' here means nothing by itself. Other necessary hyphens are those between elements of a compound adjective, e.g, 'Black-headed'. It seems desirable, however, to encourage a tendency to go further and to make single words out of properly hyphenated pairs when the sense allows. 'The conversion of a hyphenated word into an unhyphenated single one is desirable as soon as the novelty of the combination has worn off, if there are no obstacles in the way of awkward spelling, obscurity or the like' (Fowler). We already have many compound names such as 'Redpoll', 'Bullfinch', and 'Blackbird' that are always spelt as single words; and others that usually or sometimes are, such as 'Oystercatcher', 'Yellowhammer', and 'Hedge-

NAIL: a horny plate-like structure, shaped like a shield, found at the tip of the upper mandible of all species of wildfowl. NALOSPI: the distance between the forward edge of a bird's nostril and the tip of the bill; term derived from the German NAsenLOchSPItze. NAME, COLLECTIVE: see ASSEMBLY,

NOUN OF.

NAME, COMMON: sometimes used as an equivalent of 'vernacular name' or 'popular name' (see NAME, VERNACULAR). 'Common name' is subject to the slight ambiguity that it is also the translation of the nomen triviale of Linnaeus, which had the meaning of 'specific name' (see NOMENCLATURE).

NAME, ENGLISH: the name ('vernacular name', 'popular name') of a species or category of birds in the English language. English names, especially those of familiar birds, are part of the living language; as with other words, they are thus governed by usage, and this may change with time or differ between one English-speaking country and another. Unlike scientific names, which are based on international agreement among zoologists to accept certain conventions (see NOMENCLATURE), English names can be subject to no fixed rules, and their application may cut across taxonomic beundariesj also, they are usually not of international significance apart from the English-speaking world. Nevertheless, it is expedient that there should be some approach to uniformity-by consensus of opinion-in the practice of ornithologists with regard to English names, at least during one period of time and in the same country. Clearly, a standard should be sought along the lines of determining the best current usage and of encouraging general adherence to it on the part of ornithologists. Some of these may have strong minority views that it would be improper to stigmatise as necessarily incorrect; but it seems probable that most of the diversity of practice is accidental rather than deliberate. Admittedly, there are in many cases alternative names to those given greatest acceptance by ornithologists-names that have also had substantial currency, and may even have been preferred at earlier dates, or that may be found in poetry or literary prose. There are also dialect names, locally or widely used, that have a place in the popular speech of the countryside and in writings embodying that. Some ornithologists and others actively seek to influence usage by reviving older names or by introducing new ones because these are considered to be more pleasing or more appropriate. One may think that such attempts to change English names, widely used outside the realm of ornithology, may lead to confusion. On the other hand, it would be unreasonable to deny some latitude in the use of alternative names for which a case can be made (e.g. 'Dunnock'). There are certain tendencies in common usage that may well be encouraged by ornithologists. There is, notably, a welcome trend in the direction of shortening cumbersome compound names, such as the 'Golden-crested Wren' (a misnomer at that) of a few decades ago, now 'Goldcrest', The prefix 'Common' likewise now tends to be omitted in many instances where it is really unnecessary, and the redundant second term to be dropped in 'Fulmar Petrel', 'Eider Duck', and others. Similarly, ornithologists may help to mould general usage by showing preference for the more appropriate of alternative names both in common use, e.g. 'Willow Warbler' rather than 'Willow Wren'. In the case of birds familiar on both sides of the Atlantic, it is impracticable in the face of differing common usage to secure complete uniformity in English names as between the British Isles and North America, two areas with many birds in common (see below). Similar considerations apply to names used by English-speaking people in various other parts of the world. On the other hand, many English names have been invented by British ornithologists for birds that are not ordinarily found in their country and that are therefore nameless in 373

374

Name, English

sparrow'. There also seems to be no reason against adjectives such as 'Blackheaded' being written as single words; but there are instances where the result would be aesthetically disagreeable or not immediately intelligible. A few hyphens are inescapable on account of awkward spelling, notably 'Bee-eater'-to write 'Bee Eater' (indexing as 'Eater, Bee'!) would be wrong; to write 'Beeeater' would be absurd. Fabricated Names. Where common usage does not operate, ornithologists are free to invent English names (if these are considered necessary in the circumstances); Eisenmann and Poor (1946) have suggested certain principles, as follows. There should be an appropriate name for every species, applicable to the whole species and forming the latter part of the name of each included subspecies. A name should give no false impression of taxonomic relationship. The name of a species should not be formed from a geographical name, or any name from a personal one. The adjectives 'common' (at best of only local relevance), 'least' (or 'little'), and 'great', should be used with extreme care. A name should not be given that is identical with one already well established elsewhere for another species. American usage. The English names used in the United States and Canada, even without going beyond those currently recognized by the American Ornithologists' Union, show some unavoidable differences from British ornithological practice. The same name may be differently applied; or different names may be used for the same species or group. It may be convenient to draw attention here to the instances over which confusion is most likely to arise. The following collective names are applied in the respective hemispheres to birds that have superficial features in common but belong to different taxonomic groups: 'vulture', 'quail', 'flycatcher', 'warbler', 'oriole' , and 'sparrow'-see entries under the several names and others to be mentioned below. The names 'hawk' and 'bunting' have a wider application in the New World. Among names for species, applied quite differently, the following are outstanding examples: British Application Blackbird Robin Redstart Tree Sparrow

Turdus merula E rithacus rubecula P hoenicurus spp. Passer montanus

American Application

Agelaius spp. Turdus migratorius Setophaga ruticilla Spizella arborea

The name 'Great White Heron' is given to Ardea herodias occidentalis in America but was until recently applied in British bird books to Egretta alba, now designated an 'egret' with varying adjectives. There are of course many instances in which the same name is applied to closely related birds, with or without distinguishing adjectives apt to be omitted in ordinary use. Among unofficial American names, there are such uses as 'buzzard' for vulture (New World family) and 'yellowhammer' for a species of woodpecker. Special American names for groups include 'loon' instead of 'diver', 'jaeger' instead of 'skua' for Stercorarius spp. (not Catharacta), 'murre' instead of 'guillemot' for Uria spp. (not Cepphusi, and 'goatsucker' instead of 'nightjar' . The most important instances of different substantive names for the same species are: British Usage Long-tailed Duck Goosander Hen Harrier Little Auk Sand Martin Lapland Bunting

American Usage Oldsquaw Common Merganser Northern Harrier Dovekie Bank Swallow Lapland Longspur

There are many other instances in which a different adjectival name is used although the birds are at most subspecifically distinct, e.g. 'Kentish Plover' becomes 'Snowy Plover' in America, 'Grey Phalarope' becomes 'Red Phalarope' (refers to breeding plumage), and 'Common Gull' becomes 'Mew Gull'. Some American names such as 'Duck Hawk' for 'Peregrine' and 'Pigeon Hawk' for 'Merlin' are no longer the official preferences. Finally, there are many cases in which a species is known in Britain by its substantive name without qualification, but an adjective is added in

America for distinction from related species there, e.g. 'Rock Ptarmigan', 'Barn Swallow', 'Winter Wren'. Other Usages. In the more widely divergent avifaunas of Australia and New Zealand, differences arise chiefly from the use of names familiar in Britain for birds that are not even closely related, e.g. 'chough', 'magpie', 'robin', 'treecreeper', 'warbler', and 'wren'-again see entries under the several names. In other parts of the world, even where English is largely spoken, this tendency is less noticeable; on the other hand, many compound names are merely ornithological fabrications, without roots in common speech and often varying from author to author. Sometimes a name from an indigenous language is adopted and more or less anglicized; or a scientific generic name (currently used or obsolete) does duty as an English substantive name. A.L.T. American Ornithologists' Union. 1983. Check-list of North American Birds. (6th edn). Eisenmann, E. 1955. The species of Middle American birds. Trans. Linn. Soc. N.Y. 7: 1-128. Eisenmann, E. & Poor, H.H. 1946. Suggested principles of vernacular nomenclature. Wilson Bull. 58: 210--215. Lockwood, W.B. 1984. The Oxford Book of British Bird Names. Oxford. Macleod, R.D. 1954. Key to the Names of British Birds. London. Swann, H. Kirke. 1913. A Dictionary of English and Folk Names of British Birds. London.

NAME, POPULAR: recognized equivalent of

NAME, VERNACULAR.

NAME, SCIENTIFIC: Carl Linnaeus (1707-1778) named many animals in addition to plants. The Swedes have a saying: 'God made the plants and animals, Linnaeus named them'; some scientists and evolutionists may not agree with the first part of this saying, but nobody can disagree with the second part. He was certainly the author of the Binominal (sometimes Binomial) System as in use today, and he proposed there must be two names, in Latin or 'Latinized' Greek so that they could be used throughout the world (see NOMENCLATURE). Of course many scientific names (popularly known as Latin names) have been given and recognized by zoologists since Linnaeus's time. In some cases the scientific name of an animal has the generic name repeated as the specific name, for example, the Red Kite Milvus milvus. This is known as a tautonym, for tauton (Gr) the same, and onoma (Gr) a name; and has come about because of a change in the generic name; the International Code states that the specific name may not be changed, even though it results in a tautonym. The ruling has been modified for botanical names and tautonyms are not used for plants. The Wren was among the birds that Linnaeus himself named, and he called it Motacilla troglodytes. Under his genus Motacilla he included a number of small birds which ornithologists have now split up into several genera, reserving M otacilla for the wagtails. In naming the American wren-like birds in the first decade of the 19th century, Vieillot chose the Linnaean specific name troglodytes (troglodyte or cave-dweller, by reference to the form of the nest) as a generic name. Later it was found that the European Wren was so closely allied to these that it must go in Vieillot's genus, so it became 'Troglodytes troglodytes' (Tweedie 1963). The Code states that the name of the nominate subspecies (race) must have a subspecific name that is the same, i.e. it must repeat, the specific name; the result was that the nominate subspecies of the Wren had to be named Troglodytes troglodytes troglodytes, and this ridiculous and lengthy name for such a little bird became something of a joke. Veteran zoologists, who were classical scholars, thoroughly disliked this: there were heated interchanges of correspondence and they refused to use these 'monstrosities'; however they passed from the scene and the rules were finally accepted. Although Linnaeus used the name M otacilla for the wren, he took the name from Marcus Varro, the Roman scholar and author, to whom this Latin word is accredited; Varro died in 27 Be and this name must have been in use since about that time. Motacilla does not really mean 'wag-tail', from motator, a mover, and cilia, a tail, because cilla does not mean a tail, and in fact there is no such word. Motacilla is a Latin word, using -illa a diminutive suffix, and means 'little mover'; when Varro explained this name he said: Quod semper movet caudam (which is always moving its tail), when he might have been expected to say: Quod semper movet cillam, but he did not; one cannot help thinking that Linnaeus was well aware of this when he used the name for the Wren. This wrong interpretation must have started long ago, and still persists among some ornithologists; for example we are quite happy to interpret

Naturalized birds

Haliaeetus albicilla as the White-tailed Eagle; the specific name was supposed to mean 'white-tailed', but it does not. Names taken from Greek mythology were often used by Linnaeus and later zoologists; the generic name Halcyon for a kingfisher is an interesting example. There were strange legends about the kingfishers; the ancient Greeks thought they mated (conceived) at sea and built floating nests, and so at this time the gods favoured them and kept the sea calm. The Greek word for kingfisher, alkuon, is derived from hals the sea, and kuo I conceive, hence 'halcyon days', calm days, kingfisher days. An example of an apparently foolish name is a subspecies of the Great Tit, Parusmajor minor. In 1848 Temminck and Schlegel named a new tit from Japan Parusminor. Later it was considered to be an eastern member of the 30 or so races of P. major, so the subspecific name had to be P. major minor. Sometimes in an effort to give a new species a generic name that almost certainly had not already been used, a zoologist resorted to an anagram, for example Daptioncapensis, the Cape Petrel; the generic is an anagram of Pintado, the Portuguese name for this petrel. The scientific name of an animal might originate from the naturalist who first discovered it, or from a zoologist working in a laboratory, and studying its anatomy; the specific name is quite often given in honour of a well-known person, or the collector who found it. The kiwis have the generic name Apteryx, which is derived from the Greek a-, a prefix meaning not, or there is not, and pterux (Gr) a wing. The wings of a kiwi are rudimentary, hidden by the body feathers, and useless for flight; the Great Spotted Kiwi Apteryx haastiwas named in honour of Sir Julius von Haast, the New Zealand explorer. Col. R. Meinertzhagen, evidently in a flippant mood, took advantage of the now forbidden hyphen to name a babbler subspecies after his friend William Payn: Argyafulvus billypayni. A.F.G.

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nasal cavities in the SKULL. The anterior or external nares (nostrils) pierce the rhamphotheca of the upper mandible at varying distances from its base (uniquely at the tip in kiwis Apteryx spp.)-see BILL; the passages continue through apertures in the bones (premaxillae) into the nasal cavities. The posterior or internal nares (also called 'choanae') lead from the nasal cavities into the buccal cavity. For the nasal cavities and their functions see RESPIRATORY SYSTEM and SMELL; for the nasal glands see EXCRETION, EXTRARENAL. The external nares are of various shapes, from round to linear; sometimes there is a central tubercle in each naris. Usually they are exposed (gymnorhinal); but in some birds they are concealed by frontal feathers, e.g. in crows and grouse. Sometimes each naris is protected by a flap (operculum), which in tapaculos is movable. In the Procellariiformes (Tubinares) the nostrils are carried in a double horny tube on top of the bill. The internasal septum, separating the right and left passages, is imperforate in most birds but perforate in a few. Although the nostrils remain open (pervious) in most birds, they are or become secondarily closed (impervious) in some Pelecaniformes; in such cases, entry to the nasal cavities is only from the mouth through the choanae, which may be quite large, and respiration is through 'secondary external' nares at the angle of the mouth. The shape of the bony aperture of the nostril has been used as a taxonomic character. It is 'holorhinal' when the posterior margin is rounded, 'schizorhinal' when it forms a slit; 'pseudoschizorhinal' is a term applied to a modification of the holorhinal type; and 'amphirhinal' signifies that there are two bony apertures (one behind the other) on each side. In Sulidae (see above) even the bony aperture is blocked.

NARROW FRONT MIGRATION: see MIGRATION under Flight

performance. Tweedie, M.W.F. 1963. Those Latin names. Animals 2(22): 593.

NAME, SUBSTANTIVE: term used throughout this work for a

noun that is the chiefelement in the English name of a number of species distinguished from each other by qualifying adjectives (including nouns and participles used adjectivally). Either or both elements of the full name may be compound, and each of them, unless written as a single word, should preferably be hyphenated (being indissoluble); on the other hand, the adjectival and substantive names should not be joined by a hyphen. For a few species a single word serves as a complete name, e.g, Brambling, Dodo. In other cases the substantive name may ordinarily be used alone where there is no other species with the same substantive name in the area, but in a wider context an adjectival name must be added. Occasionally there may be two independent (not hyphenated) qualifying names, e.g. Great Crested Grebe, Lesser Spotted Woodpecker. There is a certain analogy between an English substantive name and a scientific generic name, but this must not be pressed; unrelated species may have the same substantive name, and closely related species may have different ones. See NAME, ENGLISH.

NAME, TRIVIAL: see NOMENCLATURE-but also sometimes used in the sense of NAME, VERNACULAR. NAME, VERNACULAR: 'the name ofa taxon in any language other

than the language of zoological nomenclature' (International Code)-see NOMENCLATURE; 'popular name' is a recognized equivalent. 'Vernacular name', however, is sometimes used in the restricted sense of a name in a local dialect or in the native language of a country foreign to the writer or speaker; this ambiguity can be avoided by using an adjective denoting the particular language. The vernacular names given in this work are, unless otherwise indicated, 'English names' (see NAME, ENGLISH). For names in other European languages see the works cited below. Cramp, S. et ai. 1977-19-. The Birds of the Western Palearctic, Oxford. (Dutch, French, German, Russian, Spanish, Swedish.) J0rgensen, H.I. 1958. Nomina Avium Europaearum. (Rev. Edn) Copenhagen. Devillers, P. 1976-19-. Projet de Nomenclature Francaise des Oiseaux du Monde. Gerfaut, published in parts. (French, world Iist.)

NANDU: alternative name for species of Rheidae (see RHEA).

NAPE: see TOPOGRAPHY. NARIS: usually in the plural ('nares'), for the paired openings of the

NASAL: a paired bone of the SKULL. NASAL CAVITY: see NARIS; RESPIRATORY SYSTEM; SKULL; SMELL; and EXCRETION, EXTRARENAL. NATIVE COMPANION: alternative name for the Australian Crane Grus rubicunda (see CRANE). NATIVE HEN: substantive name, in Australia, of Tribonyx spp, including the flightless Tasmanian Native Hen T. mortieri (for family see RAIL). NATURALIZED BIRDS: species that have been introduced by human agency, direct or indirect, into areas where they either had not yet spread by natural means or had become extinct, and that have successfully established themselves and are now breeding regularly as wild birds. Mere acclimatization in captivity, or even the casual escape of captive individuals, is excluded from the definition. Extensive man-made changes have taken place in the world distribution of certain bird species within the past hundred years or so. The House Sparrow Passer domesticus, for instance, was a native of Europe and parts of Asia and North Africa but has been spread to the remaining continents by human agency. It now occupies almost the whole of North America, large parts of South Africa, as well as New Zealand, Cuba, Hawaii, New Caledonia, the Falklands, and many other islands. It has been estimated that within the past century largely man-made extensions have doubled the natural world range of the House Sparrow, which was over lS,OOO,OOOkm 2, so that it now occupies one-quarter of the earth's surface. The Starling Stumus vulgaris has been artificially spread almost as widely, as will be further mentioned. Introductions may be either deliberate or more or less accidental. Deliberate introductions have been made for three main reasons. In western Europe and in North America excessive shooting of game stocks has led to widespread and prolonged introductions of game-birds; this has sometimes, as with the Grey Partridge Perdix perdix from Hungary to Britain, been to supplement stocks of native species, but more often, as with the Pheasant Phasianus colchicus in both Europe and North America, to diversify the native game stocks with completely alien birds. Nostalgia for the sights and sounds of the home country led to large-scale and often highly successful introductions of western European song-birds into North America, South Africa, Australia, and New Zealand. In the

376

Naturalized birds

British Isles especially, the desire to increase the amenities of country estates led to the importation of large numbers of ornamental waterfowl, the progeny of which have sometimes been neither pinioned nor wingclipped and have thus escaped to found feral populations. Some more or less domesticated birds have also been able to escape from captivity and establish themselves in the wild. In the British Isles, despite attempts to introduce upwards of 100 bird species (mostly during the past hundred years), only 4 completely alien birds have become thoroughly naturalized over a wide area; the Pheasant from various parts of Asia, the Red-legged Partridge Alectoris rufa from southern Europe, the Little Owl Athene noctua from western Europe, and the Canada Goose Branta canadensis from North America. In addition, the Mandarin Duck Aix galericulata and the Golden and Lady Amherst's Pheasants Chrysolophus pictus and C. amherstiae, all 3 from China, and the Ruddy Duck Oxyura jamaicensis from North America are naturalized in limited areas; the Capercaillie Tetrao urogallus, after becoming extinct in the Scottish Highlands about 1785, was successfully reintroduced there from Sweden in 1837-39; the Gadwall Anas strepera became naturalized in two small areas in southeastern England at the same time as an apparently natural colonization from the Continent took place in Scotland; and the widespread presentday populations of both the Mute Swan Cygnus olor and the feral domestic pigeon Columba livia var. represent escapes from more or less domesticated stocks. Of these 12 species, 5 were introduced to supplement game stocks, 4 were ornamental waterfowl, 2 were formerly kept for food, and the Little Owl was introduced as an aesthetic whim of a handful of bird-loving 19th century landowners. The Ring-necked Parakeet Psiuacula krameri, an escaped cage bird, appears to be established in one or two British localities, as it is in parts of the Middle East and Lower Egypt. In France, on the other hand, the numerous introductions of birds over the past hundred years have resulted in only one additional species becoming established-Reeves's Pheasant Syrmaticus reevesii joining the already naturalized Phasianus colchicus. This is no doubt largely due to the fact that a continental area tends to have fewer vacant ecological niches than an island. In North America the 2 most successful and widespread naturalized birds have been the House Sparrow and the Starling from Europe. The House Sparrow has now occupied the whole of the cultivated area of the United States and Canada. The Starling has spread, since 1891, over the whole continent north to the Gulf of St Lawrence and west to the Rocky Mountains; it also occurs in Jamaica as a result of a separate introduction in 1903. Small local populations of naturalized Grey Partridges, Pheasants, Goldfinches Carduelis carduelis, and Tree Sparrows Passer montanus from Europe have also been added to the avifauna of North America. More recently the Monk Parakeet Myiopsitta monachus from southern South America and the Mexican House-finch Carpodacus mexicanus have become widely naturalized and a number of escaped cage-birds, especially parrots and doves, have become locally naturalized around Los Angeles, California, and Miami, Florida. Honolulu, Hawaii, has its own special constellation of introduced species. The Greater Bird-of-paradise Paradisaea apoda, of the Aru Islands and New Guinea, was successfully introduced into Little Tobago, West Indies, in 1909. Of the numerous European song-birds introduced into Australia and New Zealand by homesick emigrants, mainly in the 1860s, 8 are now naturalized in Australia and 13 in New Zealand. The Skylark Alauda arvensis, Song Thrush Turdus philomelos, Blackbird T. merula, Greenfinch Carduelis chloris, Goldfinch, House Sparrow, and Starling are found in both countries today. In New Zealand an interesting by-product has been the interbreeding of subspecies of the Redpoll Carduelis flammea from different parts of Europe, and perhaps also of the Yellowhammer E mberizacitrinella. Asian birds naturalized in Australia include the Indian Spotted Dove Streptopelia chinensis suratensis, the Common Myna Acridotheres tristis (also naturalized in Hawaii and New Zealand), and the Red-whiskered Bulbul Pycnonotus jocosus. All the birds of the last-named species now at large in New South Wales and Victoria are said to derive from some that either escaped or were liberated from an aviary in Sydney, a city where they are now plentiful in the parks and threaten to become a pest to fruit-growers. From Africa, the Ostrich Struthio camelus was introduced into South Australia under domestication and has become feral in one or two areas. Non-European birds naturalized in New Zealand, in addition to the Common Myna, include the California Quail Callipepla califomica, the Canada Goose, which is now locally abundant, the Black Swan

Cygnusatratusfrom Australia, and the White-backed Magpie Gymnorhina hypoleuca (Cracticidae) also from Australia. Success in deliberate attempts at naturalization is quite haphazard, as the British record shows. Animal species are well adapted to their native environment but, if they are to establish themselves firmly in a completely different part of the world, a whole complex of factors, such as climate, food supply, and cover for both nesting and roosting, must be suited to them; nor must pressure from predators be too great. A.C. Twomey has pointed out that imported European birds became naturalized in the United States only in regions with temperature and rainfall corresponding to those in their native breeding places. In New Zealand the introduced European species have completely supplanted native birds over most of the cultivated area, being for the most part pre-adapted to the habitat created by the destruction of the native vegetation and the substitution of imported crop plants. No doubt the native New Zealand birds would in time have adapted themselves to the areas cultivated by man, but the presence of the European birds has deprived them of the chance. Several other island archipelagos also have their inhabited and cultivated areas dominated by introduced species, notably the Seychelles in the Indian Ocean, where the 3 commonest land birds are the Common Myna, the Peaceful Dove Geopelia striata, and the Cardinal or Madagascar Fody Foudia madagascariensis. The dove, called also Barred Crown Dove and Zebra Dove, has a very involved history. A native of South-east Asia and Australia, it was first introduced to Mauritius (where it is still common) by Indian traders, and thence to the Seychelles. Some 30 introduced species of birds are also at least locally established in the Hawaiian archipelago, out of well over 100 that have been liberated at one time or another. Theoretically, its own fecundity is the only limit to the increase of an introduced bird population in a suitable new habitat, until it comes up against the natural ceiling that the environment imposes on it. The expansion of the Starling and House Sparrow populations in North America bears this out well; so does the increase, from 2 cocks and 6 hens to 1,898 birds in 5 years, of a population of Pheasants on a small island off the western coast of North America. When populations build up to their natural ceiling on an island, the surplus may attempt to spread oversea, as is suggested by the fact that, as Williams (1953) has shown, many of the small birds naturalized in Australia and New Zealand began to appear by the end of the century on the small islands that lie mostly 320-880 km to the southward of the two main landmasses. There can be little doubt that most of them were blown there by the wind. Campbell Island, for instance, 700km south of Dunedin, now has breeding Blackbirds, Song Thrushes, Starlings, Redpolls, Chaffinches F ringilla coelebs, and Dunnocks Prunella modularis, all almost certainly self-introduced-but from stocks naturalized in a secondary area. No highly migratory species have succeeded in keeping their migratory habit while becoming naturalized in a new country. Most of the European birds that have been so successful in other parts of the world are at most partial migrants in Europe. The Canada Goose in Britain, however, provides an instance of a migratory bird population that has lost its urge to migrate during a period of captivity and has become wholly sedentary in its secondary home, apart from a moult migration between some English breeding populations and the Beauly Firth in Scotland. The Pheasant, on the other hand, is normally a wholly sedentary bird but has shown some signs of acquiring a migratory habit in the harsher climate of Sweden, while Swedish Canada Geese winter in Germany and the Netherlands. Bird introductions have on the whole proved less disastrous than introductions of mammals and insects, but the examples of the Starling in North America and perhaps of the Red-whiskered Bulbul in Australia are there to point the dangers of irresponsible introductions. R.S.R.F. Etchecopar, R.D. 1955. L'Acclimatarion des oiseaux en France au cours des 100 dernieres annees. Terre et Vie 102: 42-53. Fitter, R.S.R. 1959. The Ark in our Midst. London. Gabhardt, E. 1959. Europaische Vogel in uberseeischen Landern, Bonn. Zool. Beitr. 3/4: 310-342. Lever, C. 1977. The Naturalized Animals of the British Isles. London. Niethammer, G. 1963. Die Einbiirgerung von Saugetieren und Vogeln in Europa. Hamburg. Penny, M. 1974. The Birds of the Seychelles and the Outlying Islands. London. Peterson, R.T. 1961. A Field Guide to Western Birds. Boston, Mass. (Hawaiian introduced birds at pp. 332-336).

Natural selection

Walker, A.F.G. 1970. The moult migration of Yorkshire Canada geese. Wildfowl 21: 99-104. Williams, G.R. 1953. The dispersal from New Zealand and Australia of some introduced European passerines. Ibis 95: 676-692.

NATURAL SELECTION: all those factors that lead to systematic differences between various genetic forms in a population in their rates of survival or reproduction. Such differences lead to differences in fitness-the relative contribution each genotype makes to the next generation. Natural selection is the main factor bringing about evolution, as first suggested by Darwin and Wallace and confirmed by subsequent studies, particularly in genetics and ecology, and by the development of the mathematical theory of population genetics. Genetical variation within populations is the pre-requisite of natural selection. Such variation is abundant. Although about two-thirds of the genetic material carried by each individual is identical in most members of the majority of animal and plant populations, the remaining one-third varies from individual to individual-i.e. the alleles at each locus are not the same in all members of the population (see GENETICS). This variation may be manifest in various ways in the characters of the organism. A characteristic may vary continuously from one extreme to another, with no division into distinct classes (e.g. body-weight) or with such division being imposed merely by the integral nature of the characteristic (e.g. CLUTCH-SIZE). Alternatively, variation may be discontinuous, with sharply distinct classes (e.g. the bridled and unbridled forms of the Guillemot Uria aalge. See POLYMORPHISM). Variation is found in all types of characters (morphological, physiological, biochemical, behavioural) and all types may be subject to natural selection. Natural selection in birds was first clearly demonstrated by H.C. Bumpus in 1898. He studied 136 House Sparrows Passer domesticus found exhausted after a severe snowstorm: 72 survived and 64 died. The mean total length of the survivors was 158.7 mm, while that of those that died was 160.5 mm. Thus there was strong and significant selection against longer birds. Studies of predation by birds on the peppered moth Biston betularia provide an illustrative example of natural selection. This species is typically pale in colour with darker markings that render it highly cryptic on the lichen-covered tree-trunks on which it rests by day. There is a melanic variety of the species that is conspicuous in such locations. Direct observations of moths on tree-trunks show that birds tend to find the melanic variety much more readily that the typical form. As a result, the survival rate of melanics is much less than that of the typicals. Converse results have been obtained in areas affected by atmospheric pollution. There the tree-trunks present a dark background, having few epiphytes, and the melanic moths appear less conspicuous than the typicals. As expected, birds find the typicals more easily than the melanics in such places and the resultant mortality rate of the typicals is higher than that of the melanics. Natural selection often results in the maintenance of the statusquo with regard to the genetical constitution of populations. Thus most Biston betuLaria of rural areas are of the typical form. Melanics occur, as a result of mutation (see GENETICS) or of immigration from polluted regions, but their frequency is kept extremely low because the birds find them more easily than they find the typical ones. Another example of stabilizing selection is found in Bumpus's study of House Sparrows. Humerus lengths were significantly more variable among the dead birds than among the survivors, though the mean lengths were the same: this means that birds with extreme humerus lengths, whether long or short, survived less well than birds with humeri of average length. Such elimination of the extremes is commonly found in studies of selection acting on continuously varying characters. In general, stabilizing selection is likely to occur whenever a population has been living in a fairly constant environment for some time. When environmental conditions change, the relative fitnesses of the genotypes in the population may change. A form which previously survived relatively well may survive relatively poorly in the changed conditions. The result of this will be that its frequency in the population will decline. The resultant gradual change in the genetic composition of the population is the basis of evolution. Thus prior to the industrial revolution most areas that now suffer atmospheric pollution did not do so and the trees growing in them supported abundant epiphytic lichens. At that time, melanic B. betularia were universally rare. The pollution consequent upon industrialization killed the lichens and so changed the

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direction of selection, the melanics subsequently surviving better than the typical moths. As a result, the frequency of the melanics rose from about 0% to over 90% in 50 years in many industrial centres in Britain. At first sight one might expect that selection would tend to eliminate all genotypes except the one with the highest fitness and thus give rise to genetic uniformity. That this is not always true is demonstrated by the large amount of genetic variation to be found within natural populations. This variation originates by mutation and by the continual production of new combinations of genes that results from sexual reproduction (see GENETICS). It is maintained in populations by various forms of natural selection. One such form is selection in which rarer genotypes have relatively high fitnesses by virtue of their rarity. Such selection may arise in various ways. For example, experiments with various birds and other animals have shown that when they are feeding on food of more than one type, they tend to overlook the rarer forms of food, so that they not only take an absolutely larger number of the commoner forms but also a disproportionately larger number. In nature, if the different forms of food are the different genotypes of a single species then, because each genotype is selectively advantageous when rare but disadvantageous when common, a variety of genotypes is preserved in the population. FREQUENCY-DEPENDENT SELECTION of this form may be of great importance in the maintenance of genetic variation. Selection may vary with frequency in ways that do not conserve genetic variation. If the fitness of each genotype is greater when that genotype is commoner, then rare genotypes are rapidly eliminated and eventually only a single type remains. This occurs when some birds feed on prey which are packed closely together, such as Goshawks Accipiter gentiLis feeding on flocks of Domestic Pigeons CoLumba Livia: they take more light birds from flocks that are mainly dark and vice versa. Selection is measured as fitness, which may be most precisely defined by example. Suppose that one has a population in which there are simply two genotypes, A and B. Consider the newly-fertilized eggs of one generation and the birds developing from them: some will not survive long enough to reproduce themselves; of those that do survive, some may have only a few offspring while others may have many. Suppose that the average number of newly-fertilized eggs of the next generation to which an egg of this generation contributes is a if the egg is of genotype A and b if it is of genotype B. Suppose that A is the fitter genotype, i.e. a is greater than b. Then, by convention, the fitness of genotype A is 1 and the fitness of genotype B is bla. Thus the fitness of a genotype is the average contribution made by an individual of that genotype to the next generation, measured relative to the fitness of that genotype which contributes most (which has a fitness of 1 by convention), with the point of measurement in each generation being the newly-fertilized egg stage. The definition of fitness in terms of average contributions of genotypes clarifies an important point. To say that natural selection, in the form of predation by birds, favours melanic Biston betularia over typicals in industrial areas means not that the birds eat none of the melanics and all of the typicals but that they eat a higher proportion of the typicals. Nor is the fact that many of the deaths are 'accidental', i.e. unrelated to the genotype of the individual, important: so long as there is some systematic difference in average rates of survival and reproduction, natural selection is occurring. Since fitness is a relative measure, based on comparisons within a single population, one cannot validly speak of the fitness of a whole population. The mean fitness of a population is a mathematical abstraction, quite unrelated to the potential growth-rate, size, or competitive ability of the populations. It cannot, therefore, be used for comparing the probability of survival of different populations. A source of confusion is that 'fitness' is a technical term with a precise meaning but is also a word in general use with other meanings. An Olympic athlete may be fit in the evolutionary sense, but not necessarily: 'physical fitness' is only one factor in genetic fitness. In evolutionary biology, the latter is of prime importance, so 'fitness' should only be used in its technical sense in evolutionary discussions. The fitness of the individual is an insufficient explanation for the phenomenon of parental care, manifest more in birds than in any other class of animals. A genotype that produced large numbers of eggs but which failed to care for them, so that none survived, would rapidly disappear from a population. Genotypes that produced fewer eggs but which cared for them, so that some survived to adulthood, would prevail in evolutionary time. Thus it is not just the fitness of the individual that must be taken into account but the fitness of its offspring. However,

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because of the biparental nature of sexual reproduction, only half of the genetic material in an offspring is received from each of its parents. Thus, for the potential genetic contribution to future generations, the fitness of an individual's offspring is only half as important as the fitness of the individual itself. To take an extreme and simplified example, a genotype that lays down its own life to ensure the survival of more than two offspring to reproductive age will tend to prevail in evolution whereas a genotype that lays down its life to ensure the survival of less than two offspring to reproductive age will not. Individuals share part of their genetic endowment not only with their offspring but also with all their relatives: brothers and sisters have half their genetic endowment in common, full first-cousins have one-eighth in common, half-brothers have one-quarter, etc. Thus genotypes that have characteristics benefitting their relatives will prevail in evolution, so long as the characteristics do not cause too great a loss of fitness to the individual. The DISTRACTION BEHAVIOUR of ground-nesting birds provides an example of this: it increases the probability of survival of the eggs or chicks without involving a great risk to the parent. W.D. Hamilton has analysed the theory underlying this idea and has shown that the important factor, in terms of evolution, is the 'inclusive fitness' of an individual-i.e. its own fitness (defined as above) plus the fitnesses of all its relatives, weighted according to their degree of relatedness. In mobile species in which individuals have no great tendency to live near their relatives, the characteristics of an individual will be largely irrelevant to the fitness of its relatives. Thus only offspring need to be considered in calculating inclusive fitness. But in species where individuals tend to associate with their relatives, inclusive fitness in a broad sense is important and selection must be considered in terms of the relatives of the individual as well as the individual itself-KIN SELECTION. The Tasmanian Native Hen Tribonyxmortierii provides an example. The sex-ratio is biased, with an excess of males. Some birds breed in pairs but others form trios of two males and a female, each male obtaining about half the copulations and probably fathering about half the offspring. Such an arrangement is extremely rare: in most species two males display or fight until one gains sole possession of the female. The wife-sharing in T. mortieni is facilitated by the two males usually being brothers. Thus although each male only fathers half the offspring, he is uncle to the other half. This reduces the selective pressure on males to fight for sole possession of the female. Competition between members of one sex for access to members of the other gives rise to a particular type of natural selection known as SEXUAL SELECTION. As a result of natural selection, organisms have characters which aid their survival in their particular ecological niches-they are adapted to their environments. The study of adaptations is a key area of evolutionary biology. In studying the evolutionary forces that have resulted in a particular character, one is in a sense studying the function of the character (without implying that the evolution that produced it was orientated to the goal of producing it). The study of adaptation has, therefore, been named teleonomy by analogy with, and to distinguish it from, Aristotelian teleology. The particular form of any teleonomic study depends on the character being studied but the aim is always to identify, and if possible measure, the selection pressures responsible for the evolution and maintenance of the character. The evolutionary forces responsible for the origin of a character may be considered the 'ultimate causes' of that character, in contrast to the processes occurring during the individual's development that result in the character being formed, the 'proximate causes'. Thus the ultimate cause of flipper-like wings in penguins is that penguins use their wings for submarine locomotion; the proximate cause is that the developmental pathway of the penguin's wing is deflected somewhat from that found in typical birds. The existence of two levels of causative explanation, as a result of evolution by natural selection, is one of the unique features of biology. (A.J.C.) J.J.D.G. Curio, E. 1973. Towards a methodology ofteleonomy. Experientia 29: 1045-1058. Ford, E.B. 1975. Ecological Genetics. (4th edn). London. Lewontin, R.C. 1974. The Genetic Basis of Evolutionary Change. New York. Wilson, E.O. & Bossert, W.H. 1971. A Primer of Population Biology. Stamford.

NAVIGATION: here used in the sense that a bird may be considered to have navigational ability if it is able to orientate its flight path in the absence of landmarks previously known to it. The orientation may be simply in a fixed compass direction, or towards a particular area (homing), from any direction.

Many birds appear simply to shuttle back and forth between summer and winter quarters. To reach the latter the only requirement for the young, naive bird, when not accompanied by experienced adults, is for it to be innately programmed to fly for a certain distance in a given direction, distance-and-bearing navigation in sailors' parlance. If young migrants are held captive in an unchanging, artificial environment when they would normally be migrating, they show periodic bouts of fluttering and hopping, migration-restlessness. It is found that longdistance migrants continue to show this activity for much longer than closely related species migrating only short distances. Since the time spent in flying (if they were free) would determine the distance covered, one element of the migration programme is thus established. See MIGRATION. The restlessness of caged migrants also has a directional component which can be automatically registered on a circle of pressure-sensitive perches. The scatter this produces about a mean direction is generally wide, but if the mean of each day (or night) is calculated and the means over, say, a month are examined, they are found to cluster in the general direction of the seasonal migration. Anomalous directions may also be taken up and these 'nonsense orientations', unrelated to migration or home direction, have been studied especially in Mallard Anas platyrhynchos, using free-flying birds and examining the cluster of bearings on which individually released birds vanish from sight when observed through powerful binoculars. The sun is the primary basis for compass-orientation, with an element of time-compensation to allow for its apparent movement round the sky. Caged birds change orientation as the sun position is deflected by mirrors, change their angle to a fixed, artificial sun throughout the day and switch through 90° if their internal 'clocks' are shifted by 6 hours by being kept in an artificial day out of phase with the normal (see RHYTHMS AND TIME MEASUREMENT). A 12-hour shift produces a 180°switch when the artificial and normal days overlap. If the birds are released by day when their shifted clocks register night-time, various directions are taken up. These have been interpreted as showing that the mechanism changing their flight angle to the sun by 15°/h during the day goes into reverse during the night. There are indications that the position of sunset is an important clue to birds migrating later in the night. But Mallard, released long after the sunset glow has gone, orientate well if the moon is the only visual clue (the stars being obscured by cloud). Time-shifting modifies this orientation, but it is not clear if the same 'clock' is involved as for sun-compass orientation. If the stars alone are visible, compass orientation is shown which is not influenced by imposed time-shifts. This leads to the interpretation that it is the shape of the constellations and their relation to the fixed point (north) marked by Polaris that are the clues used. This concept has been explored in detail using caged passerines under the domes of planetaria. The naive young bird learns firstly the point of least rotation in the night sky and the relation constellation patterns (which need not be ones occurring in nature) bear to this. Subsequently the constellations themselves are used to find the north, much as we do ourselves. The circumpolar constellations which are above the horizon at night throughout the year are the important ones. The constellations farther from the pole can be blotted out without loss of orientation. Seasonal changes, in which different non-polar constellations become visible at night, do not determine the migratory direction taken up. This depends on the bird's physiological condition, governed primarily by photoperiod. Migration predominately occurs under clear or partly-clouded skies. However, field evidence, particularly from radar observations, has shown that well-orientated flights occur when astronomical clues are not available, even when birds are flying between cloud layers. This has reawakened interest in orientation with reference to the earth's magnetic field. Marginal orientations in the appropriate migratory directions have been shown by caged migrants confined in closed rooms. These orientations have been switched by artificially moving the magnetic pole. Moreover birds appear to determine the direction of the magnetic field through its tilt from the horizontal, the downward pole being taken as north. Some evidence suggests that the magnetic compass is actually used to calibrate the sun-compass and the constellation compass, i.e. it is the 'primitive' compass. The mechanism whereby the magnetic field could be detected is baffling, though crystals of magnetite, found in the heads of birds, may be the intermediary. Great difficulty has been experienced in demonstrating a direct sensitivity to magnetism, one exception being a training experiment in which pigeons had to make their choices while

Nearctic Region

actually in flight. When migrants have been displaced laterally, by wind drift or by experiment, the young birds on their first migration tend to proceed in the programmed direction. Older birds, with experience of at least one migration, tend to correct for the displacement and 'home' to the normal winter-quarters. This implies a much more advanced form of navigation than a simple distance-and-bearing procedure. Most homing experiments have been carried out on breeding birds, since their urge to return is strong and only a small area round the nest need be kept under observation. Those breeding in colonies offer obvious advantages in this respect. Many migratory species have homed from remarkable distances. The longest flights on record are those of a Manx Shearwater Puffinus puffinus which homed 4,910km in 121 days, and of Laysan Albatrosses Diomedea immutabilis which covered 5,150 km in 10 days and 6,630 km in 32 days. These, and many shorter journeys, are done in times indicative of more or less straight line flight rather than of random wandering in search of known landmarks. Homeward orientation has also been demonstrated while the birds are still in sight of the observer. Indeed the bulk of experimental work has concentrated on the scatter of vanishing points of individually released birds. The distance to which birds may be followed has been increased, in some researches, by the attachment of minute radio-beacons on their backs. Overwhelmingly the domestic pigeon Columba livia has been the preferred species, because of the ease with which large numbers can be reared and kept under precisely known conditions. Although originating from nonmigratory stock, pigeons have been selected over many generations to the point that many will home rapidly from hundreds of kilometres away. It is argued that if pigeons can undertake some navigational task, longdistance migrants could surely do better. Homeward orientation within a few kilometres of the home site may reasonably be ascribed to visual recognition of previously known landmarks, though there is some argument about this. Farther away from home, several workers have found a zone of disorientation and it is not until about 80 km that consistent homeward orientation reappears, possibly improving with distance thereafter. This apparent requirement for a minimal displacement has led to the concept of a navigational 'grid' (or, as some would have it, 'map'). This visualizes at least two physical features varying more or less regularly in a quantitative way across the earth's surface, but with their gradients crossing each other. The values of these factors at the release point (if sufficiently far away) will be detectably different from those at home and so indicate their relative positions on the 'grid', and thus the direction in which the bird must fly to regain home. The bird will also need to know how the 'grid' relates to local topography-the grid may indicate home is to the north but it must know which direction is north. The compass mechanisms discussed earlier would suffice for this; the real problem is what are the bases for the 'grid'. The common observation that homeward orientation, and homing, were much better in conditions of broken cloud, led to the examination of possible astronomical bases. Homeward orientation has not been demonstrated in free-flying birds under a night sky and some supposedly positive evidence from caged migrants is now treated with caution. A vast amount of experimentation has been undertaken to test whether a sophisticated interpretation of the sun's position in the sky is open to a bird, much as it is for human navigators. The simplest method would be to observe the sun at its highest point (local noon) enabling a time comparison to give the change in longitude. The sun's angle of elevation at that time, and comparison with the home value, would give the change in latitude. However, birds can orientate towards home at various times of day, not only at noon. They would therefore have to detect the movement of the sun and, in effect, compare with the remembered condition at home at that time. Alternatively the bird might extrapolate the observed portion of the sun arc to guesstimate the highest elevation and make comparison at that point. This would require much less of its memory. Most field experiments have indicated that the sun's only role in the homing process is as a compass, though there are some exceptions. The most positive support has come from experiments with pigeons held rigidly and exposed to variations in the position of an artificial sun or to the real sun being apparently shifted by the use of prisms. The birds' responses indicated that they could detect movement slower than that of the normal sun, remember its position to within half a diameter for 24 hours, and react to changes in its elevation as if they were due to changes

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in latitude. The evidence for time-comparison ability is much more nebulous. However, biological clocks with very precise periods (±2 min in 24 h) have been demonstrated. Mostly these have periods slightly more than or less than 24 hours and so slide out of phase if not subject to regular checks against sunrise/sunset. But for a really constant 'chronometer', natural selection has only to favour a 24.0 hour clock-period. Where pigeons experience prolonged overcast conditions and are only flown in such conditions, homeward orientation is demonstrated in the absence of astronomical clues. Homeward orientation has also been found in pigeons where eyesight has been severely restricted by cloudy contact lenses. These results have led to the search for other possible components of the navigational grid, especially those concerned with the earth's magnetism. Homeward orientation of pigeons flying below overcast is disrupted by attached magnets and can be turned about by changing the tilt of the field imposed by electrical coils mounted on the birds' heads. But this evidence does not suggest that more than a magnetic compass is involved. Some disruptions of orientation by magnetic anomalies or storms are slightly more indicative of a magnetic grid. A long range of experiments, mostly in Italy, suggests that olfaction may play a part in homing. This was affected by surgical or other interference with the nerve tracts and olfactory organs, or by diverting the direction of the winds impinging on the birds at home. The theory is that the pigeon builds up an olfactory map around home, associating one smell with one direction, another with the opposite, and so forth. There is conflicting evidence, and at best such a system could not be effective any great distance from home. Inertial navigation, whereby every change of direction and acceleration during the outward journey is recorded and integrated to give the overall angular displacement from home, has often been proposed. But imposition of highly complicated, irregular accelerations, in a revolving drum, had no effect on homing ability. Nor did surgical interference with the inner ear mechanism, most likely site of such a mechanism. Experimenters should remember that the whole bird is the flying machine and that it is capable of flying skills that would defeat a human aviator. In summary then, there are two main forms of navigation shown by birds; a simple distance-and-bearing type programmed innately in inexperienced birds, and a more complex displacement-correcting mechanism in older, experienced birds. The compass element in the former can be based on clues from sun, moon, stars and the earth's magnetism. The 'grid' needed in the latter may involve the sun's position (at least its elevation), magnetic information or even olfactory clues, but the evidence is still far from clear. G.V.T. M. Baker, R.R. 1984. Bird Navigation: the Solution of a Mystery? London. Emlen, S.T. 1975. Migration: orientation and navigation. In Farner, D.S. & King, J.R. (eds.). Avian Biology, vol. V. New York. Keeton, W.T. 1974. The navigation and orientational basis of homing in birds. In Advances in the Study of Behavior. Vol. 5. New York. Galler, S.R., Schmidt-Koenig, K., Jacobs, G.}. & Belleville, R.E. (eds.). 1972. Animal Orientation and Navigation. Washington DC. Matthews, G.V.T. 1968. Bird Navigation. (2nd edn). Cambridge. Papi, F. & Wallraff, H.G. (eds). 1982. Avian Navigation. Berlin. Schmidt-Koenig, K. 1979. Avian Orientation and Navigation. London. Schmidt-Koenig, K. & Keeton, W.T. (eds.). 1978. Animal Migration, Navigation and Homing. Proceedings in Life Sciences. Berlin.

NEARCTIC REGION: the usual designation in zoogeography for DISTRIBUTION, GEOGRAPHICAL). North America north of the tropics The borders are the Arctic Ocean in north, the Bering Strait and the Pacific Ocean in the west, and the Atlantic Ocean in the east. A border in the south is more difficult to draw; it is usually placed through Mexico, along the northern edge of the tropical rain-forest (see NEOTROPICAL REGION). Thus defined, the Nearctic Region extends from about 83°N to about 20oN. Physiography. In this vast area almost the entire range of possible climates is encountered. The major geographical features of North America, in contrast to Europe, extend longitudinally. The west consists of parallel mountains, the Rocky Mountains and related chains, extending from Alaska southward into Mexico and Central America and continuing into the Andes of South America. The interior of North America is occupied by plains extending from the Gulf of Mexico northward into Canada, where they comprise the vast Canadian Shield. In the east a minor chain of mountains, the Appalachians, extends from Georgia and Alabama into Pennsylvania and continues in several more or

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N earctic Region

less isolated mountain ranges in New York, Vermont, New Hampshire, Maine, and the Maritime Provinces of Canada. This essentially longitudinal arrangement of the major geographical features is, to a large extent, responsible for some of the otherwise puzzling features of the North American bird-life. Many attempts have been made to subdivide the Nearctic Region into local provinces, from the life zones of Merriam to the biotic provinces of recent authors. Since all these zones intergrade insensibly, none of the attempts can be considered fully successful. On the whole, bird-life and landscape change latitudinally, with the climatic and vegetational belts becoming increasingly better defined northward. A circumpolar tundra belt north of the tree-line is well defined. A 'Canadian' coniferous belt with its characteristic avifauna is fairly well defined. Both extend southwards along the mountains. Farther south there is a less well defined series of belts of deciduous forest, limited to areas of higher rainfall. Between the Mississippi Valley and the Rocky Mountains lie extensive plains ('prairies'); and in northern Mexico and the southwestern states are extensive arid areas, some of them true deserts. The bird-life of each of these vegetational areas differs more or less drastically from that of other areas. History of the avifauna. The composition of the North American bird fauna is best understood in the light of its history. The North American continent was connected with Europe (via Greenland) in the early Tertiary when the Atlantic Ocean was much narrower; it has had intermittent connections with Asia across the Bering Strait bridge; and it was separated from South America, at least from the early Eocene to the late Pliocene, by a series of Central American water-gaps cutting through what are now Nicaragua, Panama, and north-western Colombia. This history of the North American landmass explains the composition of its avifauna. After the late Eocene separation from Europe the fauna evolved in isolation from both Eurasia and South America, but there has been opportunity for a limited amount of faunal exchange across the Bering Strait bridge and the 'stepping-stones' in the Panamanian gap. During the first half of the Tertiary the southern half of North America was humid and tropical as far north as latitudes 38°-40°, as shown by the palaeo-botanical record. This permitted the evolution of a tropical North American fauna rather distinct from the tropical fauna of South America. The two tropical faunas intermingled when the Panamanian land-bridge was established near the end of the Tertiary (late Pliocene). In the meantime there had been a steady process of cooling and reduction of rainfall in North America, in part caused by the rising of the mountain ranges in the western parts. This resulted in the development of deserts, subsequently populated by colonists from the adjacent, more humid habitats. In addition to sea birds and world-wide taxa, the North American avifauna consists essentially of four elements: (1) an old indigenous one that developed during the Tertiary isolation; (2) a less old Holarctic element dating back to the Eocene trans-Atlantic connection with Europe; (3) more recent Holarctic immigrants from Asia; and (4) immigrants from South America. The fauna as a whole is thus somewhat intermediate between that of South America and that of Eurasia. Even though there is some ambiguity in any faunal analysis, it is fairly easy to determine to which of the four stated faunas most genera and families of North American birds belong. Indigenous elements. Five families of songbirds can be considered indigenous North American elements. The wrens (Troglodytidae) have more genera north of the Tertiary gap through Central America than they have in South America, but more species south. The large number of endemic species and genera in the arid, subtropical zone of Mexico and the south-western United States is further proof of Nearctic origin. A single species, the well-known Winter Wren Troglodytes troglodytes, has crossed into Eurasia. Other well-known North and Central American species are the House Wren Troglodytes aedon, the Carolina Wren Thryothorus ludooicianus, the Marsh Wren Cistothorus palustris, and the Rock Wren Salpinctes obsoletus, Wrens are found in nearly every habitat from the most desolate desert to marshes and the tropical rain-forest. The mocking-thrush family (Mimidae) contains many well-known North American birds of gardens, woodlands, and open country, such as the Gray Catbird Dumetella carolinensis, the Brown Thrasher Toxostoma rufum, and the Mockingbird Mimus polyglottos; the family is restricted essentially to the areas south of the coniferous forest belt. The vireos (Vireonidae), a family of small, mostly greenish, insect-eating birds of the leafy canopy of trees and bushes, are particularly well represented in the

southern United States, Central America, and the West Indies, but there are also many South American species; the Red-eyed Vireo Vireo oliuaceus is perhaps the most common North American woodland bird, the polytypic species extending as far south as southern South America. The American wood-warblers (Parulidae) are a group of colourful but structurally little diversified warbler-like birds well represented also in the northern coniferous belt, and 2 species have indeed crossed over into eastern Siberia; the northern species are highly migratory, and their passing through the United States in spring and fall, in enormous numbers, is one of the most spectacular aspects of bird-life in North America. Although the general pattern of distribution, as well as the number of endemic genera, indicates that tertiary North America was the home of these 4 families, all of them have crossed over into South America rather early, and have there produced a secondary radiation of species. The fifth family consists of the buntings or American sparrows (Emberizidae), This family is highly diversified in the New World, so much so that it is difficult to delimit it against the tanagers (Thraupinae) and other finch-like birds. Well-known North American species are the Song Sparrow Melospiza melodia with over 30 subspecies extending from the Aleutians and Alaska south to Mexico, the Field Sparrow Spizella pusilla, the White-throated Sparrow Zonotrichia albicollis, and the Rufous-sided Towhee Pipilo erythrophthalmus. These buntings, like their Eurasian counterparts, are largely birds of the open country, from deserts to prairies and marshes; but many other species are typical of the undergrowth of the forest, particularly in the tropics. Some small families or subfamilies that are presumably indigenous North American elements are the dippers (Cinclidae), the gnatcatchers (Polioptilinae), the waxwings (Bombycillinae), the silky flycatchers (Ptilogonatinae), the mostly tropical motmots (Momotidae), the West Indian todies (Todidae) (known from North America as fossils), and the Palmchat (Dulidae). Several families of non-passerine birds are perhaps indigenous North American elements, such as the New World vultures (Cathartidae) represented by the Turkey Vulture Cathartes aura, Black Vulture Coragyps atratus, and California Condor Gymnogyps californianus, The American quails (Odontophorinae) are derived from the pheasants and partridges (Phasianinae) of the Old World. Two species of turkey (Meleagris) are the most spectacular gallinaceous birds of the New World. Old World element. Since North America and Europe were a single continent up to the Eocene, permitting considerable faunal interchange across the transatlantic connection, it is impossible to determine the exact area of origin of the older Holarctic element, such as cranes (Gruidae), pigeons (Columbidae), cuckoos (Cuculidae), certain owls and nightjars, kingfishers (Alcedinidae), the bluejay group (Corvidae pt.), Cardueline finches, and certain thrushes (Turdidae). The grouse subfamily (Tetraoninae), with numerous woodland species but also birds of the open country such as the extinct Heath Hen (an eastern subspecies of the surviving Greater Prairie Chicken Tympanuchus cupido) and the spectacular Sage Grouse Centrocercus urophasianus, apparently originated in the Old World, but had a rapid radiation in North America in the late Tertiary. A more recent Palearctic element evidently came across the Bering Strait bridge. This includes larks (Eremophila), creepers (Certhia), pipits (Anthus), nuthatches (Sitta), wren tit (Chamaea), some Corvidae (Perisoreus, Pica, Corvus, Nucifraga), Paridae (Parus, Auriparus, Psaltriparus), kinglets (Regulus), Barn Owl Tyto alba, and some Hirundinidae (Riparia, Hirundo, Petrochelidoni. E.M. American Ornithologists' Union. 1983 (6th edn.). Check-list of North American Birds. Lawrence, Kansas. Cook, R.E. 1969. Variation in species density of North American Birds. Syst. Zool, 18: 63-84. Edwards, E.P. 1978 (revised edn.). A Field Guide to the Birds of Mexico. Sweet Briar, USA. Godfrey, W.E. 1966. The Birds of Canada. Nat. Mus. Canada Bull. No. 203: 1-428. Mayr, E. 1964. Inferences concerning the Tertiary American bird faunas. Proc.

Nat. Acad. Sci. US 51: 280-288. Mayr, E. & Short, L.L. 1970. Species Taxa of North American Birds. Publ. Nuttall Orn. Club. No.9. Cambridge, Mass. Palmer, R.S. (ed.), 1962-1976. Handbook of North American Birds. vols, 1-3. New Haven. Peterson, R.T. 1980 (revised edn.), A Field Guide to the Birds. Birds of North America East of the Rockies. Boston. Robbins, C.S., Bruun, B. & Zim, H.S. 1966. Birds of North America: a Guide to Field Identification. New York.

Neotropical Region

Terres, J.K. 1980. The Audubon Society Encyclopaedia of North American Birds. New York. See also Neotropical Region.

NECK: see TOPOGRAPHY. NECTAR-FEEDERS: birds that feed on the sugary liquid in the calyces of some flowers. The habit has been evolved in several unrelated families in different parts, mainly tropical, of the world. The principal groups are the hummingbirds and honeycreepers of the New World, the sunbirds of Africa and southern Asia, the honeyeaters and flowerpeckers found chiefly in Australasia, and the Hawaiian honeycreepers (Drepanididae). NECTARINIIDAE: a family of the PASSERIFORMES, suborder Oscines, SUNBIRD.

NEDDICKY: name, in South Africa, of Cisticola fulsncapilla (for family see WARBLER (1)). NEGRITO: substantive name of Lessonia rufa, a South American tyrant-flycatcher (see FLYCATCHER (2)). NEGRO-FINCH: substantive name of Nigrua spp. (see

ESTRILDID

FINCH).

NEMATODE: see ENDOPARASITE. NE-NE: Hawaiian vernacular name, widely adopted, for the Hawaiian Goose Branta sanduicensis (see under DUCK). NEOGAEA: see under

ARCTOGAEA; DISTRIBUTION, GEOGRAPHICAL.

NEOGNATHAE: a superorder (see under NEOGNATHOUS: see PALATE;

CLASS).

SKULL.

NEOMORPHINAE: see CUCKOO. NEONATE: a newly hatched bird. NEONTOLOGY: the study of geologically recent forms of life (contrasted with PALAEONTOLOGY). NEORNITHES: a subclass (see under CLASS). NEOSITTIDAE: a family of

PASSERIFORMES,

suborder Oscines,

SITTELLA.

NEOSSOPTILE: term applied to the natal down plumage (where present), as contrasted with 'teleoptile' (see PLUMAGE). NEOTENY: persistence of embryonic characters into adult life. NEOTROPICAL REGION: usual designation in zoogeography for tropical America and the non-tropical parts of South America, together with the West Indies and other islands near South America (see DISTRIBUTION, GEOGRAPHICAL). South America is the real home of the Neotropical fauna, while Central America and the West Indies occupy a special position discussed below. The Neotropical Region extends from the northern edge of the tropical rain-forest in Mexico, about 200 N (see NEARCTIC REGION), south to Cape Horn, in about 57°S. Physiography. South America is characterized by numerous geographical superlatives. The Andes, forming the western edge of the continent throughout its length, are the longest mountain range in the world, extending through 80° of latitude. The Amazon is the world's greatest river. The region is dominated by tropics and subtropics, and the southern third of the continent is so narrow that it leaves only little space for a temperate zone fauna. There are two areas of mountains east of the Andes-the isolated Guiana-Venezuela highlands (with Mt Roraima and Mt Duida), and the eastern Brazilian mountains. There are some extensive savannas ('llanos') north of the River Amazon, particularly in

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the upper Orinoco basin of Venezuela and north-eastern Colombia, and more extensive ones from the Matto Grosso south into Patagonia. Very arid country, some of it true desert, extends from the Pacific coast of southern Ecuador south through coastal Peru and Chile to about Valparaiso, southwards extending increasingly far into the mountains and encroaching in northern Argentina beyond the foot of the eastern Andes. As Wallace said, the Neotropical Region 'is distinguished from all the other great zoologicaldivisions of the globe by the small proportion of its surface occupied by deserts, by the large proportion of its lowlands, and by the altogether unequalled extent and luxuriance of its tropical forests'. History of the avifauna. The avifauna of South America not only is the richest in the world but is also remarkably uniform throughout the continent. There are no latitudinal barriers anywhere east of the Andes, and the Andes themselves have served as a distributional pathway, permitting the colonization of the lower latitudes by many temperate zone elements. The south temperate avifauna is characterized more by the paucity of its elements than by its distinctiveness. There are, however, a number of endemic genera, some of them, such as the seedsnipe (Thinocoridae), forming an endemic family. The Rhinocryptidae are of largely temperate zone distribution. Although South America is now in land connection with North America across the isthmus of Panama, the two continents were isolated for most of the Tertiary Period and perhaps for much longer. Three major water-gaps ('portals') are known to have existed during this period; one across Nicaragua, one across Panama, and the third across north-western Colombia. These water-gaps were bridged by insular 'stepping-stones' for those faunal elements capable of island-hopping. The last of the portals (between Panama and Colombia) did not close until the Pliocene, presumably about 3 million years ago. There is no ornithological evidence for any connection with Africa. Prior to the break-up of the Gondwana plate South America was connected (directly or by stepping-stones) with Antarctica-Australia. The ratites are the only element in Australia clearly a remnant of this former connection. South America has acquired several species from Africa by recent transoceanic colonization such as that demonstrated by the Cattle Egret Bubulcusibis, the Green-backed Heron Butorides striatus, 2 whistling ducks Dendrocygna spp., and a pochard Netta erythrophthalma. Indigenous element. The old indigenous South American element includes a number of small families (the number of included species is indicated in parentheses), such as the rheas (Rheidae) (2), screamers (Anhimidae) (3), hoatzin (Opisthocomidae) (1), trumpeters (Psophiidae) (3), sunbittern (Eurypygidae) (1), seed-snipe (Thinocoridae) (4), potoos (Nyctibiidae) (5), and oilbird (Steatornithidae) (1). Fossil rheas are known as far back as the Eocene, while for the 8 other families the assumption of a South American origin is based on inference (absence from all other continents, either living or as fossils). Five other nonpasserine families are much richer in species in South America than anywhere else, and for them a South American origin is hardly in doubt: tinamous (Tinamidae) (47), hummingbirds (Trochilidae) (300), puffbirds (Bucconidae) (33), jacamars (Galbulidae) (14), and toucans (Ramphastidae) (37). They include some of the most characteristic elements of the South American avifauna. South America is characterized, even better than by these nonpasserines, as the home of the Clamatores (= suborder Tyranni) the true mesomyodian passerines. All the families of this suborder are Neotropical (except for a few Old World genera with simplified syringeal musculature, which may well have acquired this similarity by convergence). The South American Clamatores are divisible into two main branches, the Tracheophonae (= Superfamily Furnarioidea) and the Haploophonae Superfamily Tyrannoidea). The Tracheophonae, in whichthe syrinx entirely tracheal, consist of the tapaculos (Rhinocryptidae) (26), gnateaters (Conopophagidae) (10), antbirds (Formicariidae) (221), ovenbirds (Furnariidae) (212), and woodcreepers (Dendrocolaptidae) (47). This group, including more than 500 species, forms a dominant element in the South American avifauna. The antbirds are particularly characteristic of the undergrowth in the tropical rain-forest, while some of the genera of ovenbirds contribute conspicuous species to the temperate zone fauna of the continent, both in the southern latitudes and at the higher altitudes of the Andes. In the haploophone Clamatores, the syrinx muscles are tracheobronchial, but are attached only at one end of the bronchial rings. This includes the tyrant-flycatchers (Tyrannidae) (366), the manakins (Pipri-

382

Neotropical Region

dae) (51), cotingas (Cotingidae) (61), and the plantcutters (Phytotomidae) (3). This group thus comprises nearly 500 species. Indeed, the 2 groups of Clamatores combined contain nearly one-eighth of all the known species of birds of the world. Most of the indigenous South American bird families, like their mammalian counterparts, have been poor colonizers. Only the hummingbirds and the tyrant-flycatchers, among the truly South American elements, seem to have colonized North America across the Central American stepping-stones to develop subtropical and temperate zone representatives in the North American fauna. The other families crossed into Central America late in the Tertiary, most of them apparently only after a complete land connection had been established. Nearctic element. The stepping-stones between North and South America were used much more actively by North American elements to carry on a steady colonization. The earliest of these immigrants-the tanagers and honeycreepers (Thraupinae), cardinals (Cardinalinae), and troupials (Icteridae)-settled there such a long time ago that, except for their evident relationships with North American elements, they have acquired all the characteristics of South American families. The Emberizidae should perhaps be included in this group. Much of the adaptive radiation of these families took place in South America. Other immigrants radiating secondarily in South America were contributed by such pantropical groups as the parrots, the trogons, the barbets, and one or two smaller groups. Other somewhat later arrivals from North America include the guans (Cracidae), the American quail (Odontophorinae), pigeons (Columbidae), jays (Corvidae), and thrushes (Turdidae). Typically North American families, such as the wrens (Troglodytidae), vireos (Vireonidae), wood warblers (Parulidae), and motmots (Momotidae), invaded South America presumably prior to the closing of the water-gap, because certain genera speciated there quite actively, having now more species in South America than in North America. The Andean chain, through Central America in almost continuous mountainous connection with the North American Rocky Mountains, has permitted the immigration of some typically Holarctic elements into South America, such as pipits Anthus spp., the Horned (or Shore) Lark Eremophila alpestris, and the Short-eared Owl Asio fiammeus. Needless to say, the South American continent has a rich fauna of fresh-water birds, consisting essentially of cosmopolitan families but with many endemic genera and species. Among the more characteristic of these the following may be mentioned: torrent ducks Merganetta spp., the Coscoroba Swan Coscoroba coscoroba, the South American sheld-geese Chloephaga spp. and the steamer ducks Tachyeres spp. (mostly salt water). Subdivisions and Islands. Attempts to subdivide the Neotropical Region into subregions have been unsuccessful as far as the area south of Panama is concerned. The 'Guianan' and 'Brazilian' districts are occupied by some different species and genera, but the total character of the local faunas depends more on climate and vegetation than on historical features. Central America, 'tropical North America' as Wallace quite rightly called it, contains a strongly mixed fauna-an old indigenous element and numerous post-Pliocene invaders from South America. The West Indies have an unbalanced and impoverished avifauna, indicating that they received their fauna by transoceanic dispersal; this is confirmed by studies of mammals, reptiles, fishes, and insects. Most of the avian immigrants came from tropical Central America, for a long period before and after the closing of the Panamanian gap. Typical for the West Indies are certain thrushes, mocking-thrushes (Mimidae), vireos, wood warblers, tanagers, finches (Fringillidae), icterids, and the peculiar Palmchat Dulus dominicus (related to Bombycilla), some tyrant flycatchers, the endemic family Todidae, some trogons, some hummingbirds (including the smallest bird in the world), some parrots, pigeons, and some hawks, to mention the more important. Other islands, such as the Galapagos, the Falklands, and the Juan Fernandez group, received most of their fauna from the adjacent parts of South America. E.M. Blake, E.R. 1977. Manual of Neotropical Birds, vol. I (to be completed in 4 vols). Chicago. Bond, J. 1978. Derivations and continental affinities of Antillean birds. Pp. 119-128. In Zoogeography in the Caribbean. Acad. Nat. Sci. Philadelphia, Special Publication 13. Bond, J. 1979 (revised edn.). Birds of the West Indies: Greater Antilles, Lesser Antilles, Bahama Islands. London. Davis, L.I. 1972. A Field Guide to the Birds of Mexico and Central America. Austin, USA.

ffrench, R. 1980 (revised edn.). A Guide to the Birds of Trinidad and Tobago. Newton Square, USA. Haffer, J. 1974. Avian speciation in tropical South America. Publ. Nuttall Orn. Club 14. Harris, M.P. 1982 (revised edn.). A field guide to the Birds of Galapagos. London. Haverschmidt, F. 1968. Birds of Surinam. Edinburgh. Hilty, S.L. & Brown, W.L. 1985. A guide to the Birds of Colombia. Princeton. Johnson, A.E. 1965 (vol. I), 1967 (vol. II). The Birds of Chile. Buenos Aires. Meyer de Schauensee, R. 1971. A Guide to the Birds of South America. Edinburgh. Meyer de Schauensee, R. & Phelps, W.H. 1978. A Guide to the Birds of Venezuela. Princeton, USA. Olrog, C.C. 1959. Las Aves Argentinas. Tucuman. Peterson, R.T. & Chalif, E.L. 1973. A Field Guide to Mexican Birds: all species found in Mexico, Guatemala, Belize and EI Salvador. Boston. Reichholf, J. 1975. Biogeographie und Oekologie der Wasservogel in subtropischtropisch Sudamerika, Anz. Orn. Ges. Bayern 14: 1-69. Ridgely, R.S. 1976. A Guide to the Birds of Panama. Princeton. Short, L.L. 1975. A zoogeographical analysis of the South American chaco avifauna. Bull. Am. Mus. Nat. Hist. 154: 163-352. Woods, R.W. 1982. Falkland Island Birds. Oswestry.

NEOTYPE: see

TYPE SPECIMEN.

NEPHRON: an excretory unit of the kidney (see EXCRETORY

SYSTEM).

NERVOUS SYSTEM: in birds, built on the same plan as in vertebrates generally; it resembles that of reptiles, especially the Crocodilia and certain lizards, very closely. The difference from reptiles is chiefly one of relative size; in a bird the brain is 10 or more times larger than the brain of a reptile of similar body weight. See also DEVELOPMENT, EMBRYONIC; GROWTH.

Central and peripheral systems. The nervous system consists of a central nervous system (C.N.S., the brain and spinal cord) and a peripheral nervous system (the cranial and spinal nerves, and the visceral or autonomic nerves and ganglia). The peripheral nerves are made up of nerve fibres that can be divided into two main categories; those that conduct impulses from the special sense organs such as eyes or from the skin and deeper tissues to the C.N.S. (afferent or sensory fibres); and others that conduct impulses from the C.N.S. to the muscles, causing them to contract and produce movements (efferent or motor fibres)-see also MUSCULATURE. Viscera such as the heart, blood-vessels, glands, and the alimentary canal are supplied by efferent nerve fibres that are classed as autonomic or visceral and are further subdivided into sympathetic and parasympathetic. Viscera usually have a double nerve supply, sympathetic and parasympathetic; these are in general functionally antagonistic-for example, parasympathetic stimulation slows the rate of the heart beat, whereas sympathetic causes acceleration. Viscera are also supplied by many afferent fibres. Functions. It is the general function of the C.N .S. to integrate the information reaching it in the form of afferent or sensory impulses from all parts of the body and from the outside world, into patterns significant in the life of the animal. It must also be capable of storing this information selectively, so that it can form the basis of memory and learning; but the physical form in which information is stored in the C.N.S. is not known. The C.N.S. must also have motor functions; on the basis of the information reaching it at any particular time, combined with what has been stored from previous experiences, it must integrate or co-ordinate outgoing efferent impulses to the muscles and viscera so that useful movements and patterns of behaviour result. To a large extent the particular kind of behaviour that can be integrated by the nervous system depends on its intrinsic structure, its 'built-in' characteristics (which are inherited). Such behaviour is activated automatically in response to appropriate sensory stimuli and is called reflex or instinctive. The extent to which it can be modified or added to as a result of experience varies in different vertebrates (see LEARNING). In birds it is limited, and much avian behaviour consists of complex but relatively stereotyped patterns, as is well seen in the reproductive cycle (mating, nest building, and so on). Patterns of behaviour depending on inherited structure are not so conspicuous in mammals, where the nervous system is less rigidly organized and shows greater plasticity in its functions: behaviour in consequence depends to a larger extent on learning and the storage of information. However, the learning ability of birds is certainly superior to that of many mammals: pigeons, for example, in some circumstances perform rather better than domestic cats. These differences between birds and mammals are

Nervous system

reflected in fundamental differences in the structure of the nervous system, particularly in the part called the fore-brain (see below). The functions of the nervous system in co-ordinating and activating patterns of behaviour can also be strongly influenced by chemical substances, hormones, circulating in the blood. These are produced by the endocrine glands (see ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM), some of which (the pituitary and the suprarenal glands) are closely associated anatomically with the nervous system. The effect is well illustrated in sexual behaviour. When, as in the male animal, male sex hormones are predominant, the behaviour integrated by the nervous system will be that appropriate for the male; experimentally the same nervous system can be shown to be capable of integrating female sexual behaviour under the influence of female sex hormones. Although such effects can be demonstrated in mammals, they are particularly characteristic of birds, where 'built-in' mechanisms form a more important part of the nervous system. Olfactory bulb

Pineal---+--'" Cerebellum( body)-Cerebellum(auricular) lobe Medulla oblongata-·-

- - Cerebral hemisphere Diencephalon

It---+-----

Optic lobe

Cervical

t 1

Thoracic

I!

lumbo-Sacral

Coccygeal

Rhomboid sinus

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Fig. 2. Transverse section through lumbo-sacral region of the spinal cord of a pigeon Columba to show the rhomboid sinus. (Modified from Kappers, Huber & Crosby 1936).

reptiles. The spinal cord is connected by well developed ascending and descending tracts with the medulla oblongata (see below) and the cerebellum; the latter is largely concerned with the maintenance of equilibrium, a particularly important function during flight. Other connections with the brain are much less well developed, and the spinal cord possesses considerable autonomy. It is able to co-ordinate the movements of the wings in flight, or the legs in running, with little assistance from the brain; it is well known that movements of this kind are often carried out actively for a short time after decapitation. Brain stem. As the spinal cord enters the skull it enlarges to form the medulla oblongata, from which most of the cranial nerves arise (Figs. I, 3, and 4). In the same region the central canal enlarges to form a cavity called the 4th ventricle. The parts of the brain stem surrounding this ventricle belong to a subdivision of the vertebrate nervous system known as the hind-brain; it includes the pons in mammals (small in birds) and the cerebellum (see below) as well as the medulla oblongata. Except in detail the medulla oblongata of birds does not differ markedly from the usual vertebrate pattern. Its expanded cranial end is continuous with the next part of the brain stem, the mid-brain, which is characteristically specialized. It possesses two more or less spherical swellings, the optic lobes, which develop on its dorsal aspect and remain in that situation in all other vertebrates; in birds they are displaced laterally and ventrally by the backward enlargement of the cerebral hemispheres (Figs. 1, 3, and 4). Cerebellum. The cerebellum (Figs. 1 and 3) is large, and situated on the dorsal aspect of the hindbrain. The main part, the corpus or body, is somewhat compressed from side to side and elongated cranio-caudally; it corresponds with the vermis in mammals and there is only rudimentary representation of the lateral extensions that form the mammalian cerebellar hemispheres. The body is divided by transverse furrows into anterior, middle, and posterior lobes, corresponding closely with the same subdivisions in mammals. These lobes are further divided by secondary furrows into folia; the most caudal of these is the nodule, and, strictly speaking, should not be included in the body of the cerebellum. On each side the nodule gives rise to a lateral extension which varies in size in different birds. This is the auricular lobe (Fig. 3), corresponding to the Olfactory bulb Cerebral hemisphere Eye

Fig. L Diagram of the nervous system of a bird (Columba). (Modified from Kappers, Huber & Crosby 1936).

Spinal cord. The spinal cord (Fig. 1) is co-extensive with the vertebral column, as in most other vertebrates except mammals, and contains a narrow channel throughout its length known as the 'central canal'. The cervical and lumbo-sacral regions are long, the thoracic and coccygeal relatively short; there are well marked cervico-thoracic and lumbo-sacral enlargements where the nerves to the wings and legs arise. A feature peculiar to birds is the 'rhomboid sinus'; this is a mass of gelatinous tissue, rich in lipids and glycogen, which separates the dorsal parts of the lumbo-sacral region of the spinal cord (Fig. 2); its significance is unknown. In the same region collections of nerve cells situated superficially on the lateral aspects of the cord form the 'nuclei of Hoffmann'. Somewhat similar but less conspicuous marginal nuclei are present in

383

Optic lobe Cerebellum (body) Cerebellum ----.,,.........,..-f-/ (auricular lobe) Medulla oblongata Spinal cord-

Fig. 3. Lateral aspect of the brain of a bird, shown in relation to the eye and the outline of the head.

384

Nervous system

flocculus of mammals. The whole complex (the nodule with its lateral extension) is called the auriculo-nodular lobe, corresponding to the mammalian flocculo-nodular lobe, and is a primitive part of the cerebellum that receives many connections from the vestibular division of the 8th cranial nerve. Functionally the cerebellum is essential for the maintenance of posture and equilibrium and for regulating the range and force of movements. It may be thought of as acting like an 'automatic pilot', maintaining stability and direction during flight, and it is noteworthy that the tracts connecting it with the centres in the spinal cord through which bodily movements are controlled are well developed in birds. The absence of cerebellar hemispheres is also understandable; they are a characteristic feature of the mammalian brain, where they are concerned in the regulation of learnt skilled movements, particularly of the limbs, and movements of this kind play little part in the behaviour of birds. Fore-brain. The cranial end of the brain stem, the mid-brain, is continuous with a complex mass of nervous tissue, the fore-brain. This consists of a median part, the diencephalon, directly continuous with the mid-brain, and bilateral expansions forming the cerebral hemispheres (Fig. 1). The whole forebrain is hollow, the median cavity of the diencephalon being called the 3rd ventricle. It is continuous caudally through the mid-brain and the 4th ventricle of the hind-brain with the central canal of the spinal cord. On each side the cavity of the 3rd ventricle extends into the cerebral hemisphere to form small lateral ventricles (Fig. 4). Olfactory bulb & cranial nerve I

2

cerebral hemisphere

3

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?Jb~c

5

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Fig. 4. Ventral aspect of the brain of a pigeon, to show the roots of the cranial nerves.

The median diencephalic part of the fore-brain is concealed from view by the cerebral hemispheres (Fig. 1). On each side it contains complex masses of nerve cells, the thalami, which are similar in their organization to the same parts in reptiles. Ventral to the thalami and forming the floor of the 3rd ventricle is the hypothalamus, another complex of nuclei, connected by a thin stalk to the pituitary gland (Fig. 4). On the dorsal aspect of the diencephalon the pineal apparatus is found; it is vestigial, and no parietal eye is present as in some reptiles. The cerebral hemispheres are rounded and smooth, lacking the convolutions characteristic of the mammalian brain. The olfactory bulbs (Figs. 1 and 4) attached to the anterior poles of the hemispheres are generally small and sometimes fused together. The olfactory sense is correspondingly poorly developed, so that most birds are classed as microsmatic; most vertebrates have a well developed sense of smell and are classed as macrosmatic. In a number of avian species, however, e.g. ducks, the domestic fowl, and most markedly the kiwis Apteryx spp., the bulbs are quite well developed; but, with the possible exception of the kiwis, it is doubtful if any birds could be described as macrosmatic (see SMELL).

In all vertebrates the cerebral hemispheres are divided into dorsal and ventral parts forming the roof and floor respectively of the lateral ventricles. In the dorsal part the extensive superficial cortex so characteristic of mammals is formed; the ventral part forms the basal ganglia of the hemisphere.

Lateral Ventricle Wulst {of the External Striatum) (solid black)

Fig. 5. A section through the cerebral hemispheres of a pigeon. On the left, the subdivision of the basal ganglia into internal and external striatal segments is indicated. On both sides, the complicated subdivision of the external striatum is easily seen. 'E' is the ectostriatum.

In birds the most immediately striking features are the small and rudimentary character of the cortex proper, and the relatively enormous development and complex differentiation of the basal ganglia (Fig. 5). This appearance is, however, deceptive. The 'basal ganglia' of birds can in fact be divided into two parts, the internal striatum and the external striatum. The smaller of these, the internal striatum, corresponds to the corpus striatum of mammals and is concerned with the control of movement. The larger external striatum is more sensibly grouped with the rudimentary cortex, since, like the cerebral cortex of mammals, it receives sensory information (especially from the eyes, the ears and, to a lesser degree, that related to the sense of touch) relayed, just as in mammals, through the thalamus of the diencephalon. A part of the external striatum may correspond to the mammalian 'motor cortex' , in as far as it sends nerve fibres directly to the spinal cord. It seems that during evolution birds, like reptiles, failed to find the mechanism for expanding these forebrain masses into a sheet-like cortex. This evolutionary failure perhaps accounts for the lesser evolutionary success of birds in the production of types capable of the very flexible and adaptable behaviour patterns characteristic of higher mammals. In one respect though, birds outdo mammals in this all-important area of plasticity: in song birds there are collections of neurons in the external striatum which control the production and pattern of song. These neurons are remarkable in that they change their structure with the seasons and circumstances, corresponding to the natural seasonal variation of song pattern in these species. There is no doubt that the large basal ganglia are functionally concerned with the integration of the instinctive behaviour of birds, and it is probable that the hyperstriatum is of particular importance in relation to the activities of the breeding cycle. These neural mechanisms are very sensitive to facilitation or inhibition by hormones. The hypothalamus of the diencephalon is closely associated with the pituary gland. It is mainly concerned in the integration of visceral and metabolic activities and has been described as the head ganglion of the autonomic nervous system. In mammals its functions are not purely neural, and it can secrete hormones that pass down the stalk to the pituitary, so that it is very closely associated with the endocrine system; it probably has similar functions in birds. Centres for the regulation of the excretion or retention of water, for temperature regulation, for a general inhibition resulting in sleep, and a number of other functions have been identified in the hypothalamus, which is a very important part of all vertebrate brains. Cranial nerves. The 12 pairs of cranial nerves (Fig. 4) characteristic of higher vertebrates are all present in birds. The Ist (olfactory) are slender (see above). The 2nd (optic) are particularly large and decussate completely in a chiasma or crossing. They discharge to the optic lobes of the mid-brain, which contain what is probably the most highly differentiated neural tissue in the avian nervous system. The size of the nerves and the complexity of the optic lobes is associated with the great importance and high degree of development of the visual sense in birds (see VISION). The visual system is organized in the same way as that of all vertebrates: the optic nerves discharge directly to both the optic lobes of the midbrain and to the thalami of the fore-brain. The optic lobes also send information to the thalami, and from this structure all the visual information passes to the cerebrum. In mammals, the connection from the eyes to the midbrain is relatively smaller than that made directly with the thalami: the ultimate target for the information is the cerebral cortex.

Nest

In birds, although the main visual centres are undoubtedly in the midbrain (the optic lobes send fibres to the brain stem and so are able to control many motor responses to visual information in a reflex way), optic nerve fibres certainly do run directly to the thalami. There is evidence that the appreciation of the nature of seen objects requires the cooperation of those parts of the avian external striatum (the Wulst or hyperstriatum, and the ectostriatum-E in Fig. 5) which are the destination of visual informmation from the thalami. The 3rd (oculomotor), 4th (trochlear), and 6th (abducens) nerves are all purely efferent and supply the ocular muscles as in vertebrates generally. The 12th (hypoglossal) is also efferent and supplies the tongue muscles; it gives a branch to the muscles of the syrinx, which are therefore not comparable with laryngeal muscles (supplied by the vagus)-see SYRINX. The 5th (trigeminal), 7th (facial), 9th (glossopharyngeal), 1Oth (vagus), and 11th (accessory) form the usual series of branchial or visceral arch nerves. They contain, of course, no component from lateral line organs as in aquatic vertebrates, and only a few special avian features need be mentioned. The 5th nerve is well developed and supplies complex sensory corpuscles, such as those of Grandry and Herbst, which are often associated with the bill; while usually considered to be tactile, their function is not fully understood (see TOUCH). Fibres serving the sensation of taste are present in the 7th and possibly in the 9th nerves, but are very few in number on account of the poor development of this particular sense in birds (see TASTE). The 11th nerve (accessory) is small and constitutes one of the caudal roots of the vagus; there is no spinal component as in mammals. There remains only the 8th nerve, which has both auditory and vestibular divisions with connections in the brain stem resembling those of mammals rather closely. The auditory division (from the lagena) is comparatively small, but the vestibular is well developed, as would be expected in animals where the maintenance of equilibrium is a particularly important function (see HEARING AND BALANCE). Spinal and autonomic (sympathetic and parasympathetic) nerves. These are arranged on the same general plan as in mammals and reptiles, but there are many detailed differences related to the different proportions of the parts and organs of the body. The roots of the spinal nerves are shown attached in series to the spinal cord in Fig. 1. They are enlarged opposite the wing and the hind limb, where they form the brachial (wing) plexus and the lumbo-sacral plexus respectively, as in all tetrapoda. Autonomic nerves are not shown: they arise from ganglia (collections of nerve cells), outside the C.N.S., that are classified in two categories, sympathetic and parasympathetic (see above). The former are arranged in two regular chains, approximately one pair of ganglia for each segment of the body, on each side of the vertebral column; the latter are more irregularly scattered, usually close to the viscera they supply. Both sympathetic and parasympathetic ganglia are connected to the C.N.S. through spinal or cranial nerves, so that their activity is centrally regulated and integrated. Differences among Birds. There are great variations among birds in the size of the brain and in the proportions between its parts. In general the gallinaceous birds show primitive characteristics, with relatively small cerebral hemispheres and well developed olfactory bulbs, and the same may be said of pigeons and plovers. Crows, owls, and parrots are at the opposite extreme, with particularly large cerebral hemispheres. (In all birds the cerebral hemispheres comprise a relatively larger part of the brain than in reptiles. Indeed, in this feature birds vie with many mammals.) The 'ratite' birds tend to have relatively large olfactory bulbs, and among them the kiwis have already been mentioned as possibly macrosmatic; these birds also have the large cerebellum typical of birds generally, suggesting that they are descended from ancestors able to fly (see EARLY EVOLUTION OF BIRDS). In the fossil Archaeopteryx, the earliest known bird, the endocranial cast indicates that the brain was essentially reptilian in form; the cerebral hemispheres were elongated, possibly with long olfactory peduncles as in a typicallacertilian brain, and there is no evidence of enlargement of the cerebellum or of ventral displacement of the optic lobes (see ARCHAEOPTERYX). The evidence from endocranial casts of fossil forms is always to be accepted with caution, since it cannot be known with certainty how completely the cranial cavity was filled by the brain. In modern birds (unlike reptiles) the cranium does in fact fit closely around the brain, so that a cast gives an accurate representation of its form and proportions. It is of interest that in the fossil flying reptiles (Pterosauria) there seems to have been a similar close relationship between the cranium and the brain, which is shown by endocranial casts to resemble that of modern birds closely, perhaps more closely than is the

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case with Archaeopteryx. Some small birds, notably the hummingbirds, have a particularly large brain/body weight ratio. In spite of this, the cerebral hemispheres are very primitive and reptile-like, so that their claim to be neurologically advanced depends chiefly on the cerebellum and mid-brain. Most of the differences between the brains of different birds can be related to differences in their mode of life; they do not seem to have much systematic relationship to taxonomic subdivisions, since quite large differences may be found between birds not widely separated in taxonomy. (F.G.) K.E.W. Pearson, R. 1972. The Avian Brain. London. Portmann, A. 1950. Systeme nerveux. In Grasse, P.-P. (ed.). Traite de Zoologie vol. IS. Paris. (Good general account of avian nervous system, with many references.) Portmann, A. & Stingelin, W. 1961. Central nervous system. In Marshall, A.J. (ed.). Biology and Comparative Physiology of Birds vol. 2. New York. Kappers, C.D.A., Huber, C.C. & Crosby, E.C. 1936. The Comparative Anatomy of the Nervous System in Vertebrates. New York. (Details of fibre tracts and cellular structure, with full references to the older literature.) Edinger, T. 1929. Die fossilen Gehirne. Berlin. (Accounts of endocranial castsalso same author, 1941, Amer. J. Sci. 239a: 665-682.) Webster, K.E. 1979. Some Aspects of the Comparative Study of the Corpus Striatum. In Divac, I. & Oberg, G.E. (eds.). The Neostriatum. Oxford. Wright, P., Caryl, P.G. & Vowles, D.M. (eds.). 1975. Neural and Endocrine Aspects of Behaviour in Birds. Amsterdam.

NEST: popularly the word 'nest' implies a structure, made by a bird, in which eggs are laid and incubated; it is perhaps usually thought of as shaped like an open bowl; to ornithologists this meaning is inadequate. Many birds make no nest; others excavate or use holes without nest material; still others make structures but do not incubate the eggs. Further, though eggs are normally incubated in one spot till they hatch, the Black Vulture Coragyps atratus of the New World may move its eggs for appreciable distances during incubation, as may some night jars. Thus, a comprehensive definition of 'nest' would be: a structure built or excavated by a bird or already in existence, or a spot or area, in which eggs are laid and remain till they hatch (after incubation by the species concerned or by some other means). The only exceptions are broodparasites, such as Old World cuckoos (Cuculidae), cowbirds (Icteridae) of the New World and some others that make no nests of their own (see BROOD-PARASITISM), and some penguins, e.g. Emperor Aptenodytes lorsteri and King A. patagonicus, that incubate the single egg between belly and tarsi or feet and may move about with it thus held, so having nothing that can be called a nest. (See also NEST BUILDING; NEST FUNCTION; NESTING ASSOCIATIONS.)

Nests are often specifically distinct in materials or site or both. For instance, the tyrant-flycatcher Tachuris rubrigastra of Argentina makes a beautifully felted cup of yellow plant-down attached to a single reed; the Paradise Riflebird Ptiloris paradiseus of Australia often decorates its nest with a discarded snake-skin; and the Crested Bellbird Oreoica gutturalis, also of Australia, customarily puts hairy caterpillars on the rim of, or inside, its nest. Moreover, closely related species tend to make similar nests and place them in similar sites, so that the nest has some practical value for taxonomy; thus woodpeckers excavate holes in trees and make no nest inside, the anis Crotophaga spp. line their untidy nests with fresh green leaves and buzzards Buteo spp. and other raptors decorate theirs throughout occupation with some fresh material. However, though auks mostly nest on ledges or in crevices on cliffs near the sea, the Marbled Murrelet Brachyramphus marmoratus has recently been found to nest high in branches of tall conifers and Kittlitz's Murrelet B. brevirostris lays its egg on bare ground above the tree-line and far from the sea. Similar remarkable exceptions occur among parrots, which can be said to nest generally in holes of one sort or another; several pairs of Monk Parakeets Myiopsitta monachus build their nests of thorny twigs together at the ends of branches, finally forming large structures made up of separate nests, and the Australian Ground Parrots Pezoporus wallicus and Night Parrots Geopsittacus occidentalis construct nests of grasses in or under tussocks. The greatest complexity and variation of construction occur among passerine birds. Non-passerines mostly build simple structures of sticks, reeds, etc., place their eggs on the ground or make holes for themselves, without adding material. In contrast, passerines that nest on the ground or in holes make more or less substantial nests. The earliest birds probably had the simplest nest-making habits, placing their eggs on the ground or in cavities without any material; later birds came to build

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simple structures or excavate holes. Presumably ground- and holenesting passerines adopted these habits secondarily. Non-passerine birds. Though non-passerines mostly have rather crude nests, there are interesting contrasts and exceptions. Some hummingbirds build the smallest known nests, 2 cm across and 2-3 em tall, whereas a long-established nest of the Osprey Pandion haliaetus or White-bellied Sea-Eagle Haliaeetus leucogaster may be a metre or more across and 2m tall. Also, the perfectly felted cups of plant-down and cobweb made by hummingbirds contrast extremely with the imperfect platforms of sticks made by some pigeons, though the frail nests of some doves (Columbina spp.) become consolidated and built up by the excreta of the young to form substantial structures. Incubation mounds. The Australasian MEGAPODES have the remarkable habit of 'artificial' incubation. They make big mounds of sand, earth and leaves, in which the eggs are hatched by the heat of decaying vegetable matter, or lay the eggs in sand and crevices where they are incubated by the heat from the sun or from volcanic emanations. The Malleefowl Leipoa ocellata, and perhaps other species, carefully control the temperature in the mound during incubation. Use ofsaliva. Swifts are interesting because many species use saliva for building and stick their nests in the shape of half cups on the sides of caves, in hollow trees or elsewhere. The Palm Swift Cypsiurus parous of Africa sticks its nest to the underside of palm leaves. In the Far East species of Aerodramus nest in huge numbers in caves and provide edible nests, being the only birds of economic importance in this respect (see EDIBLE NESTS). The Cayenne Swift Panyptila cayennensis makes a remarkable cylinder, about 70 em long, open at the bottom, of plant material and feathers felted together with saliva, the outside being left rough and plastering being done only from inside; about half-way up inside, a small shelf is made, where the eggs are laid; thus, like most other swifts, the bird nests in a hole, but it constructs its own hole. Though swifts are well-known users of saliva in building, they are probably not the only group of birds to do so. The Australian scrub-birds Atrichornis spp, line their nests with masticated wet plant material, which dries out into a cardboard-like substance and in which saliva may playa part. Some cuckoo-shrikes (Campephagidae) probably use saliva to bind together plant material for nests or to make the nests adhere better to airy forks of branches where they are placed but this needs confirmation. Aquatic nests. Grebes make pads of vegetation floating on water but attached to a plant; jacanas often make nests of rushes on the floating leaves of water-lilies or lotus; some rails and Chlidonias terns make simple nests of reeds and water-plants over water but usually in less open situations and not truly floating. Ground-nesting. Other non-passerines may be roughly divided into ground-nesters, hole-nesters and builders of simple nests in trees. Simple ground-nesting without any material is characteristic of the Ostrich Struthio camelus (though other ratites may assemble some material in their nests), sand-plovers Charadrius spp., thickknees, sandgrouse and nightjars. Interestingly, the Egyptian Plover Pluvianus aegyptius (Glareolidae), the KentishPlover Charadrius alexandrinus and at least some other species of Charadrius in Australasia bury their eggs in sand, though it is not entirely certain whether all do so by design rather than by accident, and cover them with sand when leaving the nest, Apart from auks (see above), most other Charadriiformes make some nest of plant material on the ground, often substantial as in the Black-winged Stilt Himantopus himantopus, and many gulls; yet the Green Sandpiper Tringa ochropus habitually uses the old nests of other species in trees. Albatrosses (Diomedeidae) build big mounds of soil and vegetation, and flamingos, mounds of mud. Other ground-nesters are some penguins (e.g, Adelie Pygoscelis adeliae and Chinstrap P. antarctica), making a scrape lined with pebbles; most ducks and geese (Anatidae), which are unique in using their own down as lining (though it is curious that lyrebirdsMenura spp. add their own body-feathers to the lining of their nests during incubation); pheasants and their allies (Galliformes), which usually line their scrapes with leaves and grass; buttonquail, which make a partly domed nest of grasses; and cranes and rails (Gruiformes), which make substantial structures of plant material. Hole-nesting. Non-passerines nesting in holes in the ground include shearwaters (Procellariidae), storm-petrels (Hydrobatidae), some kingfishers, motmots and bee-eaters, the last 3 making their own holes (often of considerable length) in banks or on flat ground, whereas the others are less liable to dig their own burrows. Groups that generally use existing holes in cliffs, trees or buildings are parrots, owls, trogons,

rollers and hoopoes. Hornbills also do so, with the interesting modification that the entrance is usually restricted with plaster of some sort, the female helping to immure herself. Woodpeckers and barbers mostly make their own holes in trees but some do so in ants' or termites' nests and one woodpecker lays on the ground. Stmple structures. Pelecaniformes (cormorants, pelicans, frigatebirds), Ciconiiformes (herons, storks), birds of prey, Cuculiformes (cuckoos, turacos) and pigeons mostly make simple, if large, nests in trees but many, especially among birds of prey, use the old nests of other species, or nest on ledges or even on the ground. Among the Ciconiiformes, the Hamerkop Scopus umbrella of Africa is remarkable for making a big dome of sticks cemented with mud about a metre high and with the entrance at the side. Passeriformes. In spite of great variety of form and building skill, most' passerines make simple cup-shaped nests. The range of size and materials may be represented by crows Corvus spp. with big nests of sticks lined with finer plant material and wool, and by many small birds (e.g. fantails Rhipiduridae) with small neat cups of the finest plant material and cobweb. Nevertheless, small birds may make huge nests, the Firewood Gatherer Anumbius annumbi (Furnariidae) of Argentina being the classic example; it makes a nest about 70 em deep and 30 em across of big sticks with the entrance at the top and a crooked passage leading down to the nest cavity. On the other hand, some species make such flimsy nests that the contents are visible from below, e.g, the Ecuadorian Finch Sporophila peruviana, the Rufous Whistler Pachycephala rufiventris of Australia and even some honeyeaters (Meliphagidae). Most simple nests are supported in forks or on branches but open cups may be slung by the rims from supporting twigs, often at the inaccessible ends of branches; this habit seems more prevalent in the tropics and Australasia than in the Northern Hemisphere and is characteristic of some antbirds (Formicariidae), vireos (Vireonidae), crombecs (Sylvietta spp.) of Africa, orioles (Oriolidae) and many honeyeaters. Reed warblers Acrocephalus spp. customarily bind their nests to two or three upright supports. Enclosed nests. Spherical nests of various sorts are common. Domed nests built of interlaced plant material with a large side entrance are characteristic of such low-nesting birds as warblers of the genus Phylloscopus (Sylviinae), pittas, lyrebirds, acanthizids of the genus Sericornis, fairy-wrens (Maluridae) and even some icterids, e.g. the Long-tailed Meadowlark Stumella loyca. Others are neater, more felted structures of fine plant material and moss with small entrances at the side, as in some wrens (Troglodytidae), tyrant-flycatchers (Camptostoma spp.), becards (Tyrannidae), though these typically make flat tops to their nests, and acanthizids of the genera Acanthiza and Gerygone. The Yellow-rumped Thornbill Acanthiza chrysorrhoa has the extraordinary and unexplained habit of building an ordinary cup-shaped structure on top of, or near, its rather bulky and untidy domed nest, the entrance of which may be hard to find. Some warblers of the genus Cisticola achieve a similar result by binding in growing grass as a partial dome. Perfect ovoid nests with a small side entrance towards the top are built of moss and lichen by the Long-tailed Tit Aegithaloscaudatusand even more perfect nests, felted out of fineplant down to the texture of surgical lint, are made by penduline tits Anthoscopus spp. of Africa and the Mistletoebird Dicaeum hirundinaceum of Australia. Untidy pendent structures, up to a metre or more long and often with a beard of material hanging down from the bottom and a projecting porch over the entrance, are made by some sunbirds. The African broadbills Smithomis spp. also make nests with a beard and the Common Tody-flycatcher Toduostrum cinereum constructs a long streamer of hanging material, in the centre of which it later works an aperture for the nest cavity. Ovoid, retort-shaped or bottle-shaped nests, occasionally on the ground, are made by estrildid finches of interlaced grasses, and individuals of some species (Estrildamelpoda, E. troglodytes, E. atricapillai attach a semi-covered upper story or extension, apparently used for roosting. More striking are the large retort-shaped nests of spinetailsSynallaxis spp, (Furnariidae), which make big spheres of thorny twigs measuring about 45 by 30 em, enclosing a large nest chamber, with a long winding narrow tunnel as an entrance. Tailorbirds (Orthotomus spp., Sylviinae) in Asia and allied forms in Africa bind leaves together with cobweb or other material and build a nest in the pocket so formed. Woven nests. Weavers (Ploceidae) of the Old World make various sorts of woven nests, from the globular structure of Village Weavers Ploceus cucullatus, which weave it rather carelessly out of strips of palm leaves, making an entrance near the top covered with a small porch, to the

Nest building

inverted sock of some species of Malimbus, neatly made from the fibres of palms with a tubular hanging entrance as much as 70cm long and 10cm wide. The culmination of this habit is shown by the Social Weaver Philetairus socius (Ploceipasserinae) of South-West Africa, which first constructs a roof of coarse straws in a large tree or on a telephone pole and then makes many nest chambers below, the whole forming a single huge mass. In contrast, the Icteridae (oropendolas, caciques and New World orioles) weave pendent bags with an entrance through a slit at or near the top. These bags may be a metre or so long in larger species and, because the birds usually nest colonially, a nesting tree may seem to be laden with monstrous fruit ; however, some icterids (e.g. Icterus rnesornelas and I . graceannae) make small, more conventional woven cups, pendent from their rims. Mud nests. Perhaps the most remarkable mud-nest among passerine birds is that of the ovenbird Furnarius leucopus of South America, which makes a thick-walled domed structure on branches with an entrance at the side leading by a corridor into the nest chamber . The rockfowl Picathartes spp . of West Africa make mud structures plastered on rockfaces. Simple, though large and heavy, mud cups are made by the White-winged Chough Corcorax melanorhamphos and Apostlebird Struthidea cinerea (Corcoracidae) and magpie-larks (Grallinidae) of Australasia. Some thrushes (e.g. Song Thrush Turdus philornelos and Blackbird T . rnerula) and some corvids (e.g. Magpie Pica pica ) use mud as a lining or foundation in more conventional nests as do phoebes Sayornis. Many swallows also use mud either for simple half-cups plastered to some support or for more complex flask-shaped nests. Hole- and ground-nesting. The passerines with these nesting habits need no special mention, because the peculiarities of their nests are more often those of site rather than structure. However, it is interesting that pardalotes (Dicaeidae) make domed nests within the cavities where they nest. Also nuthatches Siua spp. tend to restrict the entrance to their nests with mud . The Sand Martin (or Bank Swallow) Riparia riparia is notable for burrowing tunne ls up to a metre in length. S.M. NESTBOX: see

NEST SIT ES, MAN-MADE.

NEST BUILDING: behaviour concerned with the excavation or construction of nests. Most species of birds lay their eggs in a previously constructed nest , which may be anyth ing from a mere scrape in the ground to a highly elaborate structure, the building of which involves complex patterns of behaviour and the use of many different materials (see NEST) . Construction is usually by the female, but the male often helps and in some polygamous species he may do nearly all the work (see POLYGYNY).

Nest building may involve the selection of a site (see NEST SITE its preparation, the collection of material, the carrying of that material to the site, and the actual construction of the nest . Preparation of the site is usually unnecessary in species which build open cup-nests, but in hole-nesters it may involve excavation or the cleaning out of a pre-existing cavity. Many ground-nes ting birds first make a depression in the earth or sand. In most simple nests, and in some complex ones, only one type of material is employed; but usually there are a number, some being used for the outside and some for the lining. Thus the Long-tailed Tit Aegithalos caudatus uses mainly moss, spiders' silk, lichen, and feathers. If more than one type of material is used, which type is brought to the nest may be dictated either by the internal state of the female or by stimuli from the partially completed nest . In domesticated Canaries Serinus canaria the change-over from collecting grass for the cup to feathers for the lining depends in part on stimuli from the partially constructed nest, and in part on an internal, possibly hormonal, change in the female (Hinde 1958). A variety of relatively stereotyped patterns of behaviour may be used in collecting the material and preparing it for use. Thus weavers (Ploceidae) tear up grass leaves longitudinally (Crook 1960) and Canaries sometimes mandibulate material in water. Nest building by the Wren Troglodytes troglodytes is stimulated by rain, the function of this apparently lying in the increased flexibility of the material (Armstrong 1955). The material is usually carried in the bill; in some cases special movements make it more easily transportable (e.g. Parus spp.). Some love-birds Agapornis spp . carry material in the rump feathers (Moreau 1948). Nest construction involves the integration of a number of stereotyped SELECTION) ,

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Redpoll Carduelis flammea collecting thistledown as nest material. (PhOlO: K .J. Carlson). movements characteristic of the species. Closely similar movements are often characteristic of a wide range of related species. Amongst passerines, common movements are 'pulling and weaving', in which loose strands projecting from the rim arc pulled towards the breast and pushed down into the cup; 'scrabbling', in which the female presses down into the cup and pushes back hard with each leg alternately; and 'turning', in which she turns round while sitting in the nest and thus shapes the cup . Sometimes quite complex movement patterns appear; thus some weavers knot strands round twigs with half-hitches. The appearance of each activity involved in nest building depends both on a certain internal state and on external stimuli. Thus all the nest-building activities of Canaries are increased by injections of oestrogen: the behavioural effectiveness of oestrogen is augmented by longer daylengths and by male song (Hi nde and Steel 1966, 1978). In addition each nest-building activity is elicited by a particular stimulus situation (e.g. collecting by stimuli from the material, scrabbling by stimuli from the nest cup). For the construction of a nest, these various patterns of behaviour may be integrated into functional sequences . The principal processes involved are: (i) The various behaviour patterns of nest building share common causal factors, e.g. certain hormonal states. (ii) Nevertheless, the various activities may appear at different threshold levels of these factors: thus as a female passerine comes into reproductive condit ion, she first shows gathering , then carrying, and then the stereotyped movements of nest construction. (iii) Often each activity brings the bird into the stimulus situation where the next one is evoked; thus, gathering leads to carrying, carrying to placing material in the nest, and so on. (iv) The performance of each activity is associated with a decreased tendency to continue or repeat that activity; thus the change-over from gathering to carrying , or from sitting building in the nest-cup to gathering again, depends not only on the stimuli presented as a consequence of the first activity, but also on a decreased internal tendency to continue it . (v) Stimuli from the partially constructed nest may influence subsequent behaviour; thus a decrease in the size of the nest-cup may cause Canaries to bring a high proportion of lining material, and to bring material less often . In this way stimuli from the near-completed nest are instrumental in causing building to cease. (vi) Although, in all species so far studied , the various constituent activities appear in individuals reared away from their parents and even away from the species-characteristic nest , learning may play an important role in nest construction. Thus the location of suitable sources of material must be learnt: Canaries kept withou t material learn to pull out their own feathers. (vii) W.H . Tho rpe has suggested that learning plays an essential role in the fine integration of the activities of nest building. Thus he suggests that, while building, the bird is responsive to stimuli similar to those

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Armstrong, E.A . 1955. The Wren . Lond on. Collias, N.E . & Collias, E.C. (eds.) 1976. External Construction by Animals. New York. Crook , J.H. 1960. Nest form and construc tion in cert ain West African weaverbird s. Ibis 102: 1-25. Hinde , R.A. 1958. The nest-bu ilding behaviour of domesticated canaries. Proc. Zool. Soc. Lond . 131: 1-48. Hinde , R.A. & Steel, E. 1966. Integ ration of the reprodu ctive behaviour of female Canaries . In Nervou s and Hormonal Mechan isms of Integration . Cambr idge. Hinde , R.A . & Steel, E. 1978. The influence of daylength and male vocalizations on the estrogen-dependent behavior of female canaries and budgerigars, with discussion of data from other species. In Rosenblatt, R. , Hinde , R.A. , Beer, C. & Busnel, M.-C. (eds.). Advances in the Stud y of Behavior 8: 39- 73. Moreau , R.E. 1948. Aspects of evolution in the parrot genus Agapomis. Ibis 90: 206-239 . Noble , G.K. & Wurm, M. 1940. The effect of testosterone propionate on the Black-crowned Night Heron. End ocrinology 26: 837- 850. Stresemann, E. 1927-34. In Kiikenthal , W. & Krumbach, T . (eds.) . Handbuch der Zoologie vol. 7 Pt . 2. Berlin. Thorpe, W.H . 1956. Learning and Instinct in Animals. London . Warren , R.P . & Hinde, R.A . 1959. The effect of oestrogen and progesterone on the nest-building of domesticated canaries. Anim. Behav. 7: 209-213 .

NEST, COCK: term sometimes applied (also 'cock's nest' ) to extra nests or nest-like structures, not used for laying eggs, although the birds may roost in them . The male Wren Troglodytes troglodytes is well known to build as many as 8 of these unlined but otherwise substantial nests in a season. The female may choose one or more for lining and laying eggs in, sometimes in a subsequent year.

Crombec Syluieua brachyura building nest. (P hoto: K. Carlson).

which would be provided by a perfect nest; actions which make the existing structure approximate more closely to a finished nest are reinforced and thu s repeated. Existing evidence shows (a) that the performance of the constituent activities of nest building has some reinforcing value (e.g. the Canaries deprived of material, cited above, whose abnormal behaviour involved the movements of nest building but never led to the construction of a nest ); (b) since the abnormal patterns seen in Canaries deprived of material do not appear in undeprived birds, it seems that the construction of the species-characteristic nest is learnt in preference to the mere performance of constituent activities which do not lead to a completed nest; (c) stimuli characteristic of the finished nest produce a decrease in building behaviour. All these points are in harmony with Thorpe's view, but experimental evidence in support of it is still lacking. The hormonal basis of nest building probably differs between species. Oestrogens are primarily responsible in Canaries, but in some species androgens may be important (Noble and Wurm 1940). The behavioural effectiveness of a given hormone level may vary with external factors (Hinde and Steel). In many species there is a close link between nest building and courtship, and the peaks of nest building and copulation may coincide . The nest is of obvious functional significance: the differences even between the nests of closely related species may be adaptive. Thus the nest form amongst West African weavers is more closely related to habitat than to systematic relationships, and each nest type has special protective functions in its environment (Crook). Some species decorate their nests; thus tits place fragments of torn leaves round the nest cup, and Starlings Sturnus vulgaris gather flowers; the significance of this is not understood. Little is known of the evolution of nest building . It has been suggested that some of the shaping movements are derived from copulatory movements, and the collection of material from aggressive movements redirected on to grass stems, but there is no evidence to support these views. See also BEHAVIOUR, DEVELOPMENT OF. See photo ECTOPARASITE . R.A.H.

NEST FUNCTION: the common statement that a bird's nest is built to hold eggs does less than justice to its other functions. Among the thousands of species of birds there are many different types of nest : ColIias (1964) and Goodfellow (1977) give good descriptive accounts of the range of nests built by birds. In the following discussion the word 'function' has been given a broader meaning than that adopted by some authorities, who would allow no functions for a bird 's nest other than those of holding the eggs and chick s. Protecting the eggs. Nests act to protect birds ' eggs, both from environmental conditions and from predators. The temperature inside the nest of the Sociable Weaver Philetairus socius (see SPARROW -WEAVER AND SCALY-WEAVER ) is as much as 23°C above the external temperature in winter in the Kalahari. Village Weavers Plo ceus cucullatus spend less time incubating the eggs at high ambient temperatures than at low ones. Furthermore, the attentive periods of Village Weavers incubating in well-insulated nests are shorter than those of the same species incubating in less well-insulated nests. The Malleefowl Leipoa ocellata (see MEGAPODE) builds a nest that is also an incubator, a mound that not only passively protects the eggs from fluctuations in ambient temperatures, but one that is modified by the birds' behaviour to ensure that the two fluctuating heat sources, rotting vegetation and solar radiation, do not overheat the mound and that the heat lost to the environment does not cool it too much . The bird works daily to achieve a balance between these heating and cooling factors so that the temperature of that part of the mound where the eggs lie remains between 32° and 35°C throughout the 6 months when the eggs are in the nest. ColIias documents studies which indicate that some aspects of nesting behaviour and of the construction of birds ' nests function to protect the nests , eggs and chicks from predation. Stimulating the female. Experimental work has indicated an important stimulatory consequence of birds ' nests, in addition to other, better documented, functions . Hinde (1967 ) and Hinde and Steel ( 1978) showed that, as the time of egg-laying approached in the domestic Canary Serinus canaria, the female's abdomen became increasingly sensitive to tactile stimuli (see NEST BUILDING). Further, they were able to show that ovulation could be induced by providing the birds with a nest of such shape that it fitted the female's body neatly and therefore stimulated her increasingly sensitive abdomen as much as possible . They concluded that the nest acted as an integrator of reproductive behaviour, especially as egg-laying approached, and that its structure was important in providing stimulation to the female which led to the secretion of secondary reproductive hormones, the development of the oviduct and ovulation itself. Working in America with another species, the Ring (or Barbary ) Dove Streptopelia risoria, Lehrman et al (1961) were able to show that egg-

Nesting associations

laying occurred faster in females given mates and nesting material than in those given mates but no nesting material. The significance of these experimental results may provide the key to understanding the bewildering variety of types of nests and at the same time offer an explanation of the frequency with which false nests are built before egg-laying, the considerable time spent by females of some species sitting in nests for some days before an egg is laid, the very small size of some nests compared with the size of the brood they eventually need to protect, and the structural differences between nests built before laying and those built or reconstructed at laying. Hinde and Steel reported that male Canaries were less likely to sing when the female was engaged in nest-building than when she was not. Davies (1974) in a study of the Ring Dove concluded that much of the male's display and calling led to seating the female in a nest or potential nest site, and that once she was sitting on the nest, calling and display ceased. Unless it was crucial for the male to draw the female to the nest, it seems puzzling to risk directing the attention of predators to the nest even before the lengthy incubation period started. Davies suggested that the male had made a major contribution to the success of the breeding attempt if he got the female to sit in a nest, and thereby to receive tactile stimulation on her abdomen that would lead to rapid ovulation. Skutch (1961) has reviewed the use made by birds of nests as roosting sites. He lists 79 species in which he found evidence of this behaviour, and it is now possible to add many more. In Skutch's study of roosting, the nests of some species were specially built to serve as roosts and in others the birds used old breeding nests, but in some species the birds used the nest for roosting only during the period shortly before the eggs were laid in it, and then, especially those in which only the female roosted, the nest may have been acting to stimulate her to ovulate as well as acting as a roosting site. Although this interpretation ought not to be generalized uncritically to apply to all species, nests have been reported to be regularly used as the focus of courtship by 43 species from 26 families, indicating that their nests may have an important function in the pre-egg-Iaying phase of the breeding cycle as well as in the protection of eggs and young. In a number of species one of the ritual displays given before egg-laying directs the attention of the female to a nest or potential nest site, and it is interesting to note that males of 349 species from 66 families have been observed to assist with nest-building, even if they take little other part in the parental care of their offspring. The use of the nest in courtship and the male's assistance with nest-building are more conspicuous in some avian families than in others. In the Anhingidae, Ardeidae, Ciconiidae, Columbidae, Diomedeidae, Fregatidae, Pelecanidae, Procellariidae, Scolopacidae, Spheniscidae, Sulidae and Threskiornithidae the use of the nest as a focus of courtship is probably widespread, although it has been documented in only one or two species of each. In most of these families, as well as the Accipitridae, Gaviidae and Picidae, the male is the principal nest-builder, especially in the early part of the breeding cycle. The use of the nest in courtship is probably less common in the passerines but is widespread in the Paridae, Ploceidae and Tyrannidae. On the other hand in 156 species from 24 families of pas-

Fig. 1. Various nests of Magpie Geese Anseranassemipalmata, showing A-C roosting and courting forms, and D-F after egg laying.

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serines the male has been recorded assisting the nest-building, sometimes taking a major role, as in the Corvidae, Emberizidae, Icteridae, Parulidae, Troglodytidae and Tyrannidae, so that his interest in the nest during the courtship period is manifest. The involvement of the male in nest-building among the passerines has recently been reviewed by Verner and Wilson (1969) who conclude that males of most North American species assist with nest-building. Magpie Geese Anseranas semipalmata (see DUCK) illustrate the multiple role of birds' nests well. They build many, increasingly complex nests before egg-laying (Fig. 1) (Davies 1962). The convex types are used for roosting and courting. When the first egg is laid on one of these, uprooted vegetation is dragged onto it and it is converted into a concave cup which contains the eggs securely. Males undertake twice as much of the nest-building as the females in this species. Many species are known to build and sit on false nests before egg-laying occurs, but the behaviour is well documented in the Magpie Goose. Brockway (1969) has described the behaviour of captive Budgerigars Melopsutacus undulatus in detail. She has shown that females enter the nest box in response to a male giving the soft warble call and interprets this to mean that the call itself stimulates the female to ovulate. But if the sojourn of the female in the nestbox stimulates her to ovulate, the sequence of behaviour is then analogous to that of the male and female Barbary Dove described above. Bowerbirds. If the nest is such an important part of the male's contribution to the breeding success, then the BOWERBIRDS present a particularly interesting case. The males build and attend a bower, a nest (in the widest sense of the word) which is never used as an egg nest at all. The bower can be viewed as a supranormal nest built by the male to stimulate the female to ovulate and accept copulation. The bower itself, of the avenue builders at least, is nest-like in structure, and careful study of the nests of the Satin Ptilonorhynchus violaceus and Spotted Chlamydera maculata Bowerbirds shows them to have flimsy bower-like walls. Many of the objects collected by the birds to decorate the bowers match the colours of the species' eggs and may therefore add to the effect of the bower as a supranormal nest. Summary. The nests of birds hold the eggs and shelter them from some environmental hazards; they protect eggs, young and parents from predators; they serve as roosts and they act to co-ordinate the behaviour and physiology of the birds before egg-laying. The structure which is the characteristic nest of each species will represent a compromise that best serves each of these functions without damaging its usefulness in fulfilling the others. S. J.J.F. D. Brockway, B.F. 1969. Roles of budgerigar vocalizations in the integration of breeding behaviour. In Hinde, R.A. (ed.). Bird Vocalizations: 131-158. London. Collias, N.E. 1964. The evolution of nests and nest-building in birds. Am. Zoo!' 4: 175-190. Davies, S.l.J.F. 1962. The nest-building behaviour of the Magpie Goose Anseranas semipalmata. Ibis 104: 147-157. Davies, S.J.J.F. 1974. Studies of the three coo calls of the male Barbary Dove. Emu 74: 18-26. Goodfellow, P. 1977. Birds as Builders. London. Hinde, R.A. 1967. Interaction of internal and external factors in integration of canary reproduction. In Beach, F.P. (ed.). Sex and Behaviour: 381-415. New York. Hinde, R.A. & Steel, E. 1978. The influence of daylength and male vocalizations on estrogen-dependent behavior of female canaries and budgerigars, with discussion of data from other species. In Rosenblatt, R., Hinde, R.A., Beer, C. & Busnel, M.-C. (eds.). Advances in the Study of Behavior 8: 39-73. Lehrman, D.S., Brody, P.N. & Wortis, R.P. 1961. The presence of the nests and of nesting material as stimuli for the development of incubation behavior and for gonadotrophin secretion in the Ring Dove Streptopelia risoria. Endocrinology 68: 507-516. Skutch, A.F. 1961. The nest as a dormitory. Ibis 103a: 50-70. Verner, J. & Wilson, H.F. 1969. Mating systems, sexual dimorphism and the role of male North American passerine birds in the nesting cycle. AOO Orn. Monog. 9: 1-76.

NESTING ASSOCIATIONS: the term includes all instances of one bird species often or habitually placing its nests singly or in colonies near those of other species or near habitations or structures of other living organisms. In many cases, these associations may be regarded as true symbioses. Excluded here are instances of organisms, usually insect larvae, which often are found in birds' nests. The following types of associations have been described.

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Nesting associations

With other birds. A. Monospecific aggregations, or mixed species colonies of two or more often related species, e.g. gulls and terns, herons, icterids (see ORIOLE (2», weaverbirds (Ploceidae). B. One species nesting, singly or in scattered pairs, among pure or mixed colonies of other birds, e.g. Long-tailed Duck or Oldsquaw Clangula hyemalis and Sabine's Gull Xema sabini in colonies of the aggressive Arctic Tern Sterna paradisaea; the Turnstone Arenaria interpres among gulls and terns, and the Black-necked Grebe Podiceps nigricollis moving its nests with the yearly movements of Black-headed Gulls Larus ridibundus. C. Groups of non-aggressive species near nest site of an aggressive, usually raptorial species, e.g. Starlings Stumus vulgaris and House Sparrows Passer domesticus breeding on the fringes of the nest of an Imperial Eagle, Aquila heliaca, many African weavers building near a Black Kite Milvus migrans or a Marabou Stork Leptoptilus aumeniferus nest; species of tundra-breeding birds like geese (Anatidae) and waders (Scolopacidae) nesting with Snowy Owls Nyctea scandiaca and auks with Peregrines Falco peregnnus. D. Single pairs of different species, e.g. Redshanks Tringa totanus near the alarm-giving Lapwing Vanellus vanellus; Yellow Warbler Dendroica petechia near aggressive Red-winged Blackbirds Agelaiusphoeniceus or the Grey Catbird Dumetella carolinensis, both of which repel the brood-parasite, the Brown-headed Cowbird Molothrus ater, E. Two bird species in the same nest, as in BROOD-PARASITISM, which is normally considered disadvantageous to the host species; but at least one species association, that of the Giant Cowbird Scaphidura oryzivora, a parasitic icterid and its icterid hosts, results under certain conditions in a peculiar symbiosis in which nests having one host chick and one cowbird have better host fledging success than nests having one or two host chicks but no cowbirds. Only 13°/0 of all birds are colonial nesters, but 930/0 of all marine birds nest in colonies, often mixed. Monospecific coloniality usually, but not always, evolves when a species exploits a food resource which is not defensible. This permits the evolution of nest aggregations. But the apparent converse does not always follow, i.e, even if food is defensible within a nest territory, coloniality may on occasion evolve, as in the marsh-dwelling blackbirds (Icteridae) of the New World. The selective forces producing multispecies associations appear to be (1) nest site availability, (2) food availability and exploitation, and (3) predator pressure. In most associations, all three are involved to varying degrees. Aside from the aggressivity of the species involved, large numbers of birds simply nesting together can result in a swamping effect on predators. The earlier idea that some species are innately sociable is no longer tenable. With insects. A. Nest cavity in structure made by insects, particularly both ground and arboreal termitaria. The habit is widespread, particularly in the tropics in trogons, puffbirds, kingfishers, iacamars; apparently habitual in the Buff-spotted Woodpecker Campethera nivosa of Africa and in the parrot genera Aratinga and Brotogeris in South America. In the cases involving some trogons, puffbirds, and parrots, the birds co-habit with the termites. The Neotropical White-tailed Trogon Trogon viridis habitually nests inside large nests of polybiine wasps. The wasps usually, but not always, desert their invaded nest. The woodpecker M icroptemus brachyurus regularly nests in the spherical papiermache-like nests of certain ants (Crematogaster) in South America. B. Nesting near structures of stinging or biting social hymenoptera (wasps, bees, and ants), is widespread, particularly in the tropics in many passerine families e.g. Tyrannidae, Troglodytidae, Nectariniidae, Icteridae, Ploceidae, Fringillidae. Some raptors and storks also place their nests near aggressive ants or wasps. With vertebrates. Birds have not formed strongly developed associations with many vertebrates other than that with man; some exceptions are: A. The Water Thickknee Burhinus oermiculatus is said to place its nest near crocodile nests which are usually guarded by the female reptile, presumably against predators. Other associations consist of the use either by the bird or its associates of one or the other's burrows in the earth, e.g. the Tuatara lizard Sphenodon punctatus in the burrows of the New Zealand shearwaters, Puffinus cameipes and P. bulleri, the furnariid Geosuta cunicularia nesting in the burrows of the Chinchillid rodent Lagostomus maximus in the Argentine pampas, and the Blue-and-White Swallow N otiochelidon cyanoleuca which in turn uses the abandoned nestholes of Geosuta.

B. With man, commensalism is marked in several groups such as swallows (Hirundinidae) which use buildings as nest sites, storks (Ciconiidae), pigeons Columbalivia, Jackdaws Corvusmonedula, Rooks Corvus frugilegus, and various sparrows and weavers, especially Passer and Ploceus. That one or more of the partners in most mixed associations is aggressive or offers efficient predator alarm argues that the antipredator function is a very strong selective component. That these associationsare not more widespread also suggests that there are disadvantages as well. This has been documented in certain oropendolas and caciques (colonialnesting Neotropical icterids), some species of which almost always nest in association with stinging wasps iProtopolybia, Stelepolybia, etc.) or stingless but biting bees (Trigona). Some species have colonies which traditionally associate with such insects and colonies which do not. A chief source of death in their chicks results from ectoparasitism by botflies (Philornis spp.). But colonies associated with wasps or bees suffer significantly less from botflies than do those without. The hymenoptera repel the flies in a manner which is not yet clear. Removal of the wasps and bees results in an almost immediate high incidence of botfly attacks. Similarly, colonies with wasps or bees suffer less from predation by opossums, toucans, and snakes (Spilotes,Pseustes) than do colonieswhich lack the hymenoptera. But because of apparent seasonal vicissitudes affecting the insects, colonies associating with wasps or bees have a short breeding season and but one chance per year to reproduce while those not associating have a relatively longer breeding period and may have two or three chances per year. An additional disadvantage is that branch breakage is common because of the weight of the bird nests surrounding the insect's nest. Oropendola and cacique nests in colonies lacking bees or wasps have a high incidence of brood-parasitism by the Giant Cowbird, with its advantages and disadvantages. The cowbird chick is fed by the host female and in turn eats ectoparasitic botfly larvae from the host's chick which results in lower mortality of the host chicks (see above). The oropendola chicks do not reciprocate. The advantage conferred by a single cowbird to its host sib is apparently lost in nests having 2 or more cowbird chicks because food competition between cowbird siblings is then involved. While the evolutionary advantages to this association may be clear, the proximate mechanisms are not. Oropendolas and caciques, or any bird that habitually associates with bees, ants, or wasps, are attacked, especially at the initiation of the association, but the Hymenoptera quickly habituate to them. Both visual and olfactory components may be involved. Many birds which habitually associate with stinging or biting Hymenoptera have a rather strong musty body odour, apparently lacking in close relatives which do not form such associations. The nature of this odour is unknown; naked chicks lack it and feathered adults possess it even after death. It is apparently not the same odour in different species-it is significant that almost all species in such associations build covered nests, presumably to cover the chicks from wasp or bee attacks. A current hypothesis is that the odour is not a repellent, but is rather a recognition signal promoting habituation in the aggressive insects. It must be emphasized that it is the birds which join the aggressive insects, not the reverse. However, docile wasps and bees often join the association after its initiation for much the same reasons as did birds. Lack of knowledge of the chronology and behaviour of these subsequent joiners has confused the issue of the evolutionary significance of the association. This is not to say that the aggressive insects do not receive an advantage. The birds often vigorously defend their colony site against anteaters (Tamandua spp.) which are enemies of stingless bees and against the caracaras Daptrius ater and D. americanus (Falconidae) which are enemies of both wasps and bees. The nesting associations here described do not confer equal advantages to all the partners nor complete protection to any. But that they do so more often than not, on the average, is the reason for their existence. (S.M.) N.G.S. Clark, K.L. & Robertson, R.j. 1979. Spatial and temporal multi-species nesting aggregations in birds as anti-parasite and anti-predator defenses. Behavioral Ecology and Sociobiology 5: 359-371. Durango, S. 1949. The nesting associations of birds with social insects and with birds of different species. Ibis 91: 140-143. Janzen, D.H. 1969. Birds and the ant x acacia interaction in Central America with notes on birds and other myrmecophytes. Condor 71: 240-256. Larson, S. 1960. On the influence of the arctic fox Alopex lagopus on the distribution of arctic birds. Oikos 11(2): 276-305. Maclaren, P.I.R. 1950. Bird-ant nesting associates. Ibis 92: 564-566. Maclean, G.L. 1973. The sociable weaver, Part 4: Predators, parasites and symbionts, Ostrich 44: 241-253.

Nest site selection

McCrae, A.W.R. & Walsh, J.F. 1974. Associations between nesting birds and polistine wasps in north Ghana. Ibis 116: 215-217. Moreau, R.E. 1936. Bird-insect nesting associations. Ibis 78: 460-471. Moreau, R.E. 1942. The nesting of African birds in association with other living things. Ibis 84: 240-263. Myers, J.G. 1929. The nesting together of birds, wasps and ants. Proc, Royal Ent. Soc. of London 4: 80-88. Myers, J.G. 1935. Nesting associations of birds with social insects. Trans. Royal Ent. Soc. of London 83: 11-22. Smith, N.G. 1980. Some evolutionary, ecological, and behavioral correlates of communal nesting by birds with wasps or bees. Proc. XVII Int. Om. Congr. (Berlin).

NESTING BASKET: see NESTLING: see under

NEST SITES, MAN-MADE.

YOUNG BIRD.

NESTORINAE: see PARROT. NEST PARASITISM: see BROOD-PARASITISM. NEST RECORDING: the central collection of avian breeding information by voluntary contributors using standardized recording cards. The accumulation of sufficient cards allows the analysis of particular aspects of breeding in different years, habitats and geographical regions. History. The idea of a central collection of cards containing breeding data came from Sir Julian Huxley after his analysis of the detailed nest histories of the birds using nestboxes erected at Whipsnade Zoological Park, Bedfordshire, England in 1936. With J. Fisher, Huxley designed recording cards for the Hatching and Fledging Inquiry, as it was then called, and these were distributed to members of the British Trust for Ornithology in 1939. Observers were asked to concentrate on certain common species and the principal object of the Inquiry was to collect data on incubation and fledging periods, as well as clutch sizes of British birds. In the first year some 600 cards were returned and this total doubled in 1948 when the present name Nest Records Scheme was adopted and a new recording card design used. During the 10 years 1970-1980 the annual intake rose to between 22,000 and 30,000 cards. The first full time organizer of the BTO Nest Records Scheme was appointed in March 1960 following the award of a grant from the Nature Conservancy. A number of countries have started nest record schemes based on the original BTO format. Among the earliest were the USA and Canada, Germany, Switzerland and Finland by 1948, South Africa by 1951 and New Zealand by 1959. Many European countries now have schemes operating, including Belgium, Czechoslovakia, Denmark, Hungary, Iceland, the Netherlands, Italy, Spain and Sweden, while further afield schemes have been started in Australia, Zambia and Zimbabwe. Objects. The objects of nest recording are to collect as complete a picture of the nesting cycle of the bird as possible by utilizing the often incomplete nest histories recorded by amateur birdwatchers, so amassing breeding information impossible to collect in any other way except at immense cost. Each card on its own tells very little but when several thousand are available for analysis the sample containing useful information becomes meaningful. The card is designed so that one half contains boxes which give information on the species, observer, year, geographical locality, altitude, habitat, nest site and height of nest above ground. The other half of the card enables the observer to complete one line for each visit made to the nest, giving the date, time, number of eggs and/or young and a brief note on the observation if necessary: for example, whether eggs are warm or cold, female or male sitting and age of young. There is also a space for evidence of the success or failure of the nest. In the case of colonial species, special colony sheets may be provided. The value of nest record cards is that they provide, in the case of common species, large annual samples coming from a wide geographical area and selection of habitats. Many birdwatchers are naturally interested in looking for nests and a lot of potentially useful information would be lost in individual notebooks if no standardized recording scheme existed. The most important information which the observers record is the date on which the first egg was laid, clutch size, number of eggs hatched and number of young reaching an advanced stage such that there is a good likelihood of their leaving the nest successfully. To record these it is unnecessary and undesirable to visit the nest every day and observers are

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encouraged to plan their VISItS to collect the maximum amount of information with the minimum of disturbance. Uses of the data. The nest record cards provide data on the basic breeding biology of each species. The main parameters that can be extracted are those for laying dates, clutch size and breeding success. If sufficient records are available, the effects of weather, habitat, latitude and altitude can be determined. Some nest record schemes now use computer facilities for the input of annual samples of cards for selected species so that any marked effect on breeding performance caused by environmental changes, such as the introduction of new agricultural chemicals, can be detected. Certain types of bias are inherent in the nest record data and the analyst needs to be aware of them. Observers tend to search more vigorously early in the breeding season (in Britain) when the vegetation cover is least dense and nests are easier to find. The recording of nesting success has two main types of bias. Firstly, it is much easier to record a failure than a success and, secondly, nests found at later stages of the nesting cycle are biased towards success. Therefore various methods of analysing the data have been devised to eliminate as much of these biases as possible. R.A.M. Burton, J. & Mayer-Gross, H. 1965. The first 25 years of the Nest Record Scheme. Bird Study 12: 100--107. Mayer-Gross, H. 1970. The Nest Record Scheme. BTO Field Guide No. 12. Tring. Mayfield, H. 1975. Suggestions for calculating nest success. Wilson Bull. 87: 456-466. Myres, M.T. 1955. The breeding of the Blackbird, Song Thrush and MistleThrush in Great Britain. Bird Study 2: 2-23. Newton, I. 1964. The breeding biology of the Chaffinch. Bird Study 11: 47-68. Snow, D. W. 1955. The breeding of the Blackbird, Song Thrush and Mistle Thrush in Great Britain. Bird Study 2: 72-83, 169-178.

NEST SANITATION: see PARENTAL

CARE.

NEST SCRAPE: a small hollow excavated by a bird in soil, sand or shingle and which it may line with pieces of grass or similar material. NEST SITE SELECTION: an aspect of behaviour the study of which involves such considerations as the season when birds select their nest sites, the interval between nest site selection and the start of building, the share of the sexes, and the factors that may influence birds in selecting nest sites. For the variety of sites used see NEST. In some species the availability of nest sites may be a critical factor in habitat selection (see HABITAT and TERRITORY). The selection procedure Time. Although the nest site is generally selected shortly before breeding, birds may also show interest in such sites in the preceeding autumn (as some birds of prey) or even several years before breeding (as the Fulmar Fulmarus glacialis). Mild spells in late winter can initiate song, courtship, and even nest site selection, in species that will not begin to build until several weeks later. There is thus often an appreciable interval between selection and building, from several weeks or months down to a day or less. A bird that has lost an early nest, or is proceeding to a second brood, may condense its nest site selection and building time in the urgency to breed. The pre-laying period is also short at high latitudes where the spring and summer seasons are short. In Norway the spring arrival time of the Brambling Fringilla montifringilla is about 3 weeks after the Chaffinch F. coelebs, but the onset of nest building is only separated by a few days in areas in which the two species breed sympatrically. Perhaps species with a more southern distribution, like the Chaffinch, have a long pre-building period in order to obtain an optimal territory in the more crowded southern areas, and also in order to locate suitable and well-hidden nest sites. Nest predation is more severe at low latitudes. Shares of sexes. A survey of some 170 representative British breeding species (C. and D. Nethersole-Thompson 1943, 1944) included none in which the male and about 30 in which the female normally takes sole charge in nest site selection; in the remaining species both sexes participate, with males taking the initiative rather less often than females. This pattern is repeated in most orders of birds, although in the Anatidae and Galliformes the males evidently take little or no active part. In some species (as in the Sylvia warblers) the male arrives before the female and builds several uncompleted nests, so that the female later on can choose which of them she prefers. The male Pied Flycatcher Ficedula hypoleuca also arrives before the female and defends a nest hole which the

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Nest site selection

turning his head sideways to display the white cheeks; he may also tap at the entrance. If the female responds by approaching the hole , she shivers her wings, increasingly the nearer she comes, and then normally enters the hole, sometimes preceded by the male ; she may remain inside for a few minutes. If the female does not respond, the male usually returns to her and repeats the performance at the same or another hole. Thus he suggests a number of sites to the female, one of which she is likely to accept . Gulls and waders. Contrasting with the elaborate routine of many hole-nesting species is the nest site selection of gulls and waders (Charadrii). The male and female Herring Gull Laru s argentatus indulge in frequent preliminaries to nest building, moving from one possible site to another. The final selection and beginning of an actual nest at one or other of the sites seems quite haphazard. In the Red-necked Phalarope P halaropus lobatus both sexes together spend several days making scrapes in the soil more or less at random. Then, about an hour before laying, the female revisits man y of the scrapes and apparently lays in whichever scrape she happens to be at when the egg appears . There are exceptions, of course, to this seemingly casual pattern, such as in the Greenshank Tringa nebularia, which prefers to nest close to some small landmark such as a log or large stone in the otherwise rather featureless landscape (C. and D . Nethersole-Thompson).

Galahs Cacalua roseicapilla looking out of nest hole. (P hoto: J . Warham). female, in turn, may accept. The suggestion , based on observations at other stages in the breeding cycle, that in species in which the males take the initiative they are more brightly plumaged than the females, seems not to hold for males taking an active part in nest site selection , e.g. it holds for the Pied Flycatcher but not for the Sylvia warbler s. Titmic e. In general , the bird 's routine tends to be elaborate in species with special requirements, as in tits . They mostly nest in holes and may frequently be seen inspecting the holes from September to April, most actively just before nest building in spring, but also exhibiting a lesser peak of activit y in October and November. Since tits also roost in holes in winter, their activity in autumn could equally be roost site selection; but as winter roosts are often used later for breeding, this distinction may be unimportant (see ROOSTING ). In spring, hole inspection is most frequent in the morning and tails off markedly in mid-afternoon. Tits commonly deposit nest material in several holes before eventually lining and laying in one of them . In a typical hole inspection by the Great Tit Parus major, the male flies to the hole, leaving the female near by, and peers inside, Nuthatch Siua europaea at nest hole, reduced by mud plaster. (Pharo: E .J . Hosking).

Fairy Tern Gygis alba egg in site on branch. (P hoto: N . van S welm).

Open-nesting song-birds. Nest site selection by the majority of these comes somewhere between the elaborate procedure of the hole-nesters and the casual choice of most gulls and waders . In Scottish Crossbills Loxia scotica, for example, the nest site is usually chosen in a distinctive tour by both sexes, during which the female brood s in various crotches ; this is accompanied by frequent snatches of such irrelevant behaviour as bill-wiping, 'false feeding ' , and preening (see DISPLACEMENT ACTIVITY). The final choice of site is the female's . Survival value. Nest predation. Birds prefer to nest in sites which are not easily accessible to predators, e.g. holes, on cliffs, and on small islands. Certain tropical birds nest in close association with wasps' nests ; and Bramblings often nest in colonies of Fieldfares Turdus pilaris, which are especially active in defence of their nesting area, and Tufted Ducks Aythya fuligula

Nest sites, man-made

in mixed colonies of terns and gulls (see NESTING ASSOCIATION). The Redwing Turdus iliacus builds its nest higher up in trees and bushes early in the season before the vegetation develops than later on, probably in order to reduce nest predation. Cover. Birds select sites which provide shelter against rain, wind, and sunshine. The White-crowned Sparrow Zonotrichia leucophrys builds its nest above the ground in those years when there is a lot of snow. Competition. Competition for nest sites is generally keenest among birds with specialized requirements; in the Swift Apus apus, for example, exceptionally prolonged struggles for the possession of nestboxes have been described. Competition between members of the same species may be, to some extent, avoided by the territorial systems of some birds. Competition for nesting space is especially marked in densely colonial species, e.g, among seabirds, each species demanding a special type of ledge or other support for its nest, the presence of which may govern the birds' local distribution in the breeding season. Building effort. Purple Martins Progne subis prefer apartments which have not been cleaned out after a previous occupancy. In open-nesting species the same nest may sometimes be used for subsequent nestings, within the same season (as in the Blackbird Turdus merula) and in successive years (as in the Fieldfare). This habit is rather unusual among song-birds, but is the rule among many birds-of-prey. Eyries of the Golden Eagle Aquila chrysaetos may be occupied (by succeeding generations) for centuries, although the birds often ring the changes on two or more alternative sites. By using an old nest as a basis, less energy is needed in building. An old nest may also be an indication of a safe site: the nest is not likely to fall down. For such species the breeding population size may occasionally be increased by providing artificial nest sites (as for the Osprey Pandion haliaetus). The Green Sandpiper Tringa ochropus is remarkable among waders for laying in old nests, mostly of the Song Thrush Turdus philomelos. Some birds appropriate freshly completed or occupied nests of other species; thus the House Sparrow Passer domesticus habituatly evicts the House Martin Delichon urbica; and a pair of the American Parasitic Flycatcher Legatus leucophalus sometimes causes the rightful owners of several occupied nests to desert before settling on one of them. Nest appropriation has evolved independently in a number of different groups of birds throughout the world; it has perhaps reached its most refined form in wholly parasitic species such as the Cuckoo Cuculus canorus (see BROOD-PARASITISM). Food. Nests are placed at convenient sites according to the food resources. For example, Great Tits collect food closer to the ground than Blue Tits Parus caeruleus, and also prefer lower nest sites. Species which defend a feeding range often build the nest at the centre of the territory. See photo COLONIALITY. (J.A.G.) T.S. Jackson, J.A. & Tate, J. Jr. 1974. An analysis of nest box use by purple martins, house sparrows and starlings in eastern North America. Wilson Bull. 86: 435-439. Nethersole-Thompson, C. & D. 1943-44. Nest-site selection by birds. Brit. Birds 37: 88-94, 108-113.

NEST SITES, MAN-MADE: a wide range of types of artificial structures designed to attract and provide safe nesting places for birds. Most are nest 'boxes' suitable for species normally breeding in holes and cavities; others include ledges, excavated holes, artificial islands, floating platforms and the rearrangement of natural vegetation. The nestbox derives originally from the clay flasks first recorded in the late Middle Ages in Holland-they can be seen in F. van Valkenborch's Kirchmessfest (IS97)-and from wooden cistulae (flasks) used in Silesia. Both were utilitarian: the first broods of sparrows Passer spp. and Starlings Sturnusvulgaris hatched in them were taken for food; sowere the eggsof the Goldeneye Bucephala clangula 'farmed' in Lapland, at first by means of improved natural sites and later in boxes. (In recent years colonization of Scotland by this species has been largely effected by the provision of nestboxes.) In 1782 Gilbert White recorded that his brother had nailed up several large scallop shells under the eaves of his house in South Lambeth, London, and that they were immediately occupied by House Martins Delichon urbica, but Charles Waterton, the early 19th century Yorkshire squire, is believed to have been the first naturalist to put up numbers of boxes simply to encourage birds, and their use for this purpose developed during the century; by 1897 J.R.B. Masefield knew of 20 species that had occupied boxes or artificial platforms in Britain. Nestboxes were first applied on a large scale to attract and increase the numbers of 'beneficial' insectivorous birds in forests by Baron von

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Berlepsch in Germany; by about 1905 all the 300 boxes in his park, and 90% of some 2,000 boxes in his woods, were occupied by birds of 14 different species. Soon afterwards it was realized that whole populations of certain species could be induced to use nestboxes if enough were provided, and could thus be studied in many aspects of their population structure. Pioneer studies were those of S.P. Baldwin and W.W. Bowen on the House Wren Troglodytes aedon in the USA, begun in 1915, and of K. Wolda and his associates on the Great Tit Parus major in Holland, begun in 1920. But the species most suited to nestbox studies is probably the Pied Flycatcher Ficedula hypoleuca; since L. von Haartman began work on it in Finland in 1941, populations have been 'emboxed' in all the European countries where it breeds commonly, and tens of thousands of birds have been ringed. The 19th century nestbox was made of wood, with a round entrance hole and a fixed lid, and was designed primarily to attract tits, Nuthatches Siua europaea, redstarts Phoenicurus spp. and Pied Flycatchers. Von Berlepsch favoured a hollowed-out section of log, resembling as closely as possible the nest-hole of the Great Spotted Woodpecker Dendrocopos major which these small birds were accustomed to use under natural conditions. It has since been found, however, that the shape and external appearance of the box matter very little and that those made of planed boards are quite as effective as 'rustic' boxes with bark-covered sides. Certain rules nevertheless govern the correct construction and maintenance of safe and durable nestboxes and these have been described in a field guide published by the British Trust for Ornithology. For example, the entrance hole should be sufficiently high up the side or front panels of the box to make it hard for larger predators to reach the contents of the nest; the roof or lid should overlap the sides to keep off raindrops; and there should be no perches or ledges on which predators can get a grip. Towards the middle of the 20th century nestboxes in materials other than wood were developed; plastics, cement and sawdust, cement bricks, hardboard, and tin all found advocates. Their advantage over wood lies in superior resistance to weather and to attacks by squirrels and Great Spotted Woodpeckers which became increasingly a nuisance in Britain in the 1950s. Their disadvantages include expense, brittleness, liability to overheating in exposed sites, excessive condensation, and in some instances weight. The Russians have experimented with bottle gourds as the cheapest form of artificial nest cavity; but it is apparently not possible to inspect the contents. Nestboxes should normally be sited on the side of a tree or wall away from the hottest sun. H.N. Kluiiver pointed out that on trees in western Europe this makes them vulnerable to the maximum flow of water after a rainstorm, but some compromise position can usually be found. In woods the main consideration is to site boxes away from twigs and branches which can be used by predators; an open approach for the nesting bird is also important. Provided that they are securely attached to a trunk or branch, nestboxes need not be rigid; in closed canopy woodland they can be fixed to branch snags by a wire loop and lifted down by the loop for inspection. In Britain, the Nature Conservancy Council conducted an experiment to find out the height preferred by small birds using nestboxes, but the results after 5 years were inconclusive; it seems probable that most species have little or no preference. However, boxes in most localities have to be sited at least 3 m above the ground to avoid human damage. Ideally, a nestbox should have a fixed roof and open at the front for inspection; but where it is desired to catch the parent birds in the box for ringing and examination, a movable lid is preferable. Various devices have been developed for retaining adult birds in the box, from small external spring nets to internal treadles that release a shutter. In Britain, J.A. Gibb adapted the automatic swinging door used by racing pigeon owners in their lofts. This was followed by non-automatic shutters remotely operated by means of a fishing line passing under the lid and over the side of the box; J.H. Jenkins and P.A. Banks were responsible for ingenious variations of this idea. After capture in the box, the birds are most easily removed through a detachable version of the sleeve used in the catching boxes of Heligoland and other large traps (see TRAPPING). The traditional design of nestbox has been adapted to attract various species: there have been boxes with narrow entrances and with entrances at the back, both intended for treecreepers Certhia spp.; multiple boxes for the Purple Martin Progne subis; boxes filled with wood chippings, sawdust, balsa wood or polystyrene blocks for birds like Chickadees Parus atricapillus, Willow Tit P. montanus and Great Spotted Woodpecker to excavate. D. Lack evolved elongated boxes with holes opening

394

Netting

downward to embox a colony of Swifts Apus opus; others have taken this idea further to counterfeit the burrows of Sand Martins Riparia riparia, Wheatear Oenanthe oenanthe and Madeiran Petrels Oceanodroma castro; while artificial nests for Swallows Hirundo rustica and House Martin Delichon urbicahave been successful in Switzerland and Britain. Removal of half the front panel converts the traditional nestbox into a covered tray or ledge suitable for Spotted Flycatchers Muscicapa striata, Robins Erithacusrubecula, and many other species. By increasing the size, owls, Kestrels Falco tinnunculus, Jackdaws Corvus monedula, Stock Doves Columba oenas, and ducks can be attracted. For the Tawny Owl Strix aluco a quite distinct chimney design was used most successfully by H.N. Southern, who slung it by wire bands under an upward sloping bough; an inspection mirror was fastened to the mouth of the chimney and a perforated floor allowed drainage. Similar but narrower boxes slung from horizontal boughs are attractive to Little Owls Athene noctua. As well as nest boxes and their obvious derivatives, many other artificial means have been used to encourage nesting; the cart-wheels or platforms put up on houses in Holland and elsewhere for the White Stork Ciconia ciconia are one of the oldest devices and have been copied in the USA to attract Ospreys Pandion haliaetus. Woven baskets for Mallards Anas platyrhynchos are another Dutch idea, while in Iceland stone 'houses' are built for Eiders Somateria mollissima. Egg collectors used to 'farm' Greenshanks Tringanebularia in Scotland by providing ideal nest sites for them, .and other ground-nesting birds have been catered for in the same way. Von Berlepsch suggested tying twigs together to make better than natural forks for bush-nesting birds, 'nesting substrates' have been used by several species in America, and man-made stick nests taken by Long-eared Owls Asio otus in woods devoid of the old nest platforms of other large birds. The creation of bare ground patches or tunnels in dense ground vegetation have provided suitable nest sites for Nightjar Caprimulgus europaeus and Shelduck Tadorna tadorna respectively. More elaborately, artificial banks have been built up, in which Kingfishers Alcedo atthis were attracted to burrow. The main development of the nestbox up to the middle of the 20th century took place in Europe and North America, although it was still not proved that large numbers of boxes did more than concentrate the birds using them. For example, in the Forest of Dean (Gloucestershire, England) as many as 189 out of 200 nestboxes spread over 24 ha were occupied in 1949; but no control data are available for the area before boxes were first put up there in 1942. In Russia, large-scale attempts to attract birds to forests involved over 10,000 nestboxes in 9 areas in 1953; they were occupied by nearly 4,000 pairs of 18 species. Partially successful attempts were also made to transfer both adults and nestlings to newly afforested areas. Foresters in India began putting up boxes in the 1950s, but the great variety of tropical species nesting in holes and cavities offer further opportunities for nestbox techniques. Water bodies such as reservoirs and gravel-pits which lack natural nesting places like graded banks, spits and small islands can be improved through the creation of rafts and raised islands providing nesting places for grebes, ducks and geese, waders, gulls, terns, rails, even passerines like the Reed Bunting Emberiza schoeniclus. See photo CONSERVATION. B.C. and D.E.G. Bowczynski, M. & Sokolowski, J. 1953. Influence of nesting boxes on the distribution of some forest birds. Ochrona Przyrody, 21: 160-192. Buttiker, W. 1960. Artificial nesting devices in southern Africa. Ostrich 31: 39-48. Carter, J. 1971. Artificial Nesting Rafts. WAGBI Report and Yearbook. 1970-71, 43-46. Cave, A. 1968. The breeding of the Kestrel, Falcotinnunculus L., in the reclaimed area Oostelyk Flevoland. Netherlands J. Zool. 18: 313-407. Flegg, J.J.M. & Glue, D.E. 1971. Nestboxes, (British Trust for Ornithology Field Guide no. 3) Tring. Harrison, J. 1970. Creating a wetland habitat. Bird Study, 17: 111-122. Hiesemann, M. 1908. How to Attract and Protect Wild Birds (English edition). London. Johnson, W. 1931. Gilbert White's Journals. London. Masefield, J.R.B. 1897. Wild Bird Protection and Nesting Boxes. Leeds. Mason, C.R. & Reed, P.C. 1950. Provide your birds a nesting place. BulL Massachusetts Audubon Soc. 34: 1-16. Stresemann, E. 1948. Geschichte des Starenkastens. Ornithologische Beobachter 45: 169-179.

NETTING: see TRAPPING. NEUTRAL CATEGORIES: in taxonomy, categories that can be

used as terms without commitment to a view of the status of the subject matter, e.g, FORM; GROUP; COMPLEX.

NEW GUINEA SUBREGION: see AUSTRALASIAN REGION. NEWTONIA: substantive name of the 4 species of Newtonia, a genus of flycatchers endemic to Madagascar (for family see FLYCATCHER (1)). NEW ZEALAND SUBREGION: a division of the Australasian Region, but by some zoogeographers regarded as a separate minor region (see AUSTRALASIAN REGION; DISTRIBUTION, GEOGRAPHICAL). NICATOR: substantive name of the 2 species of Nicator, an African genus formerly placed in the shrike family but now considered to be closer to the BULBULS. NICHE: a term, often used loosely, referring to the ecological role that a species plays within a community; or, more rigorously, to the full range of environmental conditions within which it can survive. See ECOLOGY. NICHE EXPANSION: an increase in the places where a population will breed or feed, or an increase in the kinds of food members of the population will eat. Niche expansion is most often discussed in the context of a change in the feeding ecology of a population of one species in the absence of one or more species with which it normally competes. The population may then be able to exploit a food resource or a feeding site previously used by the competitor. DENSITY COMPENSATION is a likely consequence of niche expansion. Niche expansion may also happen in the absence of any change in the competitive environment, when a population learns to exploit a new food resource or nesting site. NICTITATING MEMBRANE: a transparent fold of skin, present in birds, which can be drawn across the eye to form a third eyelid (see VISION). NIDICOLOUS: young birds that remain in the nest after hatching. See YOUNG BIRD. NIDIFUGOUS: young birds that leave the nest immediately or soon after hatching. See'YOUNG BIRD. NIGHTHAWK: substantive name of various New World species of Caprimulgidae; in the plural, general term for the subfamily Chordeilinae (see NIGHTJAR). NIGHTINGALE: substantive name of some Luscinia spp.; used without qualification, in Britain, for L. megarhynchos (see under THRUSH). See photo VOCALIZATION. NIGHTJAR: substantive name of the Old World species of Caprimul .. gidae (Caprimulgiformes, suborder Caprimulgi); in the plural, a general term for the family, but American usage prefers 'goatsuckers and nighthawks'; some species have special names derived from the calls. About 70 species are known, generally grouped in 18 genera. On the basis of anatomical differences the family can be divided into 2 subfamilies, the Chordeilinae (nighthawks) and the Caprimulginae (goatsuckers), Characterstics. Nightjars are mainly 16-41 cm long, up to 78 em in a few species with greatly elongated tail feathers. The plumage is soft and is buffish, rufous, greyish, or nearly black. The upper parts are in general strongly mottled and vermiculated; the under parts are mostly barred or spotted and often with white patches on chin and throat, on the wings and on the tips of the tail feathers. In some species both a grey and a more rufous phase occur (see POLYMORPHISM). The sexes are normally somewhat different in colour. The tail is rather long; the wings are long and pointed; and the flight is silent and easy. The skull is flattened, with the bill short and weak. The gape, which is extremely wide, and in most species provided with strong bristles, enables the bird to catch insects (the main food) during flight. The eyes are large. The feet are commonly very short, with a feathered tarsus in some species; the toes are small, the middle toe possessing a pectinated claw. Most species are crepuscular or nocturnal in habit. During the day the birds lie up closely and are difficult to detect owing to their cryptic

Nocturnal habits

coloration. Normally the birds perch on the ground or lengthwise on a branch. Habitat. Some species frequent desert areas, others are inhabitants of open spaces in wooded districts, and some of forests. Distribution and movements. This homogeneous family has a nearly world-wide distribution, but it is not represented in the most northern parts of America and Eurasia, in southern South America, or in New Zealand and many oceanic islands. The North Temperate Zone species migrate southwards for the winter. Food. Insects are the main food of all night jars. Breeding. Generally no nest is made, the eggs being laid on the bare ground. These number 1 or 2, rarely 3. They are white to pinkish buff, beautifully marbled or blotched with black, brown or violet. Both parents incubate and care for the young, which are nidicolous and covered with protective (buff or greyish) down. Chordeilinae. The nighthawks are restricted to the New World; the species lack rictal bristles. In North America the Common Nighthawk Chordeiles minorand the very similar Lesser Nighthawk C. acutipennis are well-known representatives. The first frequents open country or forest borders and is also found in the Greater Antilles; the latter, which is somewhat smaller and darker, ranges also over the greater part of tropical South America and is an inhabitant of desert areas or open sandy savannas. In both species the males are slightly larger than the females, and they have· a white wing-patch and a subterminal tail-bar that are absent or smaller in the other sex. Both species are known to breed sometimes on the flat roofs of houses. The Lesser Nighthawk prefers to roost on the horizontal branches of low bushes. Other species are the white-bellied Sand-coloured Nighthawk C. rupestris and the small Least Nighthawk C. pusillus. Both are distributed in the northern part of South America. The remaining 3 genera, which are monotypic, are likewise found in South America. The Nacunda Nighthawk Podager nacunda has a white belly and throat-patch, rather long unfeathered tarsi, and a melancholy voice; it is an inhabitant of the savannas and is known to migrate northwards. Caprimulginae. More than half of the known species in the whole family belong to the typical genus Caprimulgus, of which many species are rather alike in plumage. The European Nightjar Caprimulgus europaeus is found from Great Britain and northern Africa far into Asia, and in winter migrants reach South Africa; the 'churring' or jarring note is the origin of the name. In eastern Asia the related jungle Nightjar C. indicus occurs, and it is also distributed over India, in winter reaching the Greater Sunda Islands; the males differ from the European Nightjar in having subterminal white spots on the outer 4 pairs of tail feathers instead of on the outer 3 only. In the same area, from India and southern China through Indonesia to northern Australia, the Large-tailed Nightjar C. macrurus is widely distributed; it is distinguished from C. europaeus by the fact that the 4, instead of the 3 outer primaries show a white spot. In southern Europe and the western parts of North Africa, the Red-necked Night jar C. ruficollis, with a yellow-rufous collar, is found. The paler and sandier coloured Egyptian Nightjar C. aegyptius inhabits the desert areas of south-western Asia and northern Africa. Different species occur in Africa, but the habits of many are not yet very well known, although mostly these seem not to differ greatly from those of the other members of the family. Some perform regular intertropical migrations (see MIGRATION). Some species, such as the Fiery-necked Nightjar C. fervidus, inhabiting the southern part of Africa, hunt from a fixed perch during the night instead of hawking over longer distances as do most of the other species. Different types of churring sounds are made by various species, while others have whistling calls. North American representatives include the Whip-poor-will Caprimulgus vociferus, ranging from northern North America to well into Middle America; the closely related C. noctitherus from Puerto Rico had long been regarded as extinct, but has recently been rediscovered. Another species named from the call is the Chuck-will's-widow C. carolinensis; it is a somewhat larger species frequenting wooded marshes and rocky hills in the western parts of the United States and wintering in the West Indies and Middle America. Other species inhabit South America, such as the beautiful Cayenne Nightjar C. cayennensis with throat white, and sides of face and abdomen and the lateral tail feathers mainly white; another is the Dark Nightjar C. nigrescens, also found in northern South America. The species of the genus Eurostopodus are distributed from southeastern Asia through the Philippine and Indonesian archipelagoes to Australia. They lack the rictal bristles and have ear-tufts. Most species

395

Large-tailed Nightjar Caprimulgus macrurus. (C.E. T.K.).

are rather large and dark, showing much black and dark brown but with a white throat-patch. The White-necked Nighthawk Nyctidromus albicollis is an inhabitant of Middle and South America; it breeds under the cover of bushes, and the eggs are deposited on a thick layer of dead leaves. The Common Poorwill Phalaenoptilus nuttallii is a rather small species with a relatively short tail, occurring in North America. In winter birds of this species hibernate in rock niches and may return to the same hole every winter. During this winter dormancy the birds remain in a state of torpidity with an exceedingly low body temperature, 18°-19°C (64°-66°F) as against' 40°-4l oC (104°-106°F) normally (see TORPIDITY). In some species the males show a remarkable elongation of certain feathers of wings or tail. In middle Africa the Standard-winged Night jar Macrodipteryx longipennis is found; it is a rather dark species, in which the males have, during the breeding season, the shaft of the second primary (numbered from inside) greatly elongated, with the terminal portion vaned. In courtship the male flies very slowly, with wings stiffly bowed and vibrating, low over or around the female, with its standards held straight up above the wing and the shaft and terminal vane vibrating with the wing. In the southern part of Africa occurs the rather large Pennant-winged Nightjar Semeiophorus vexillarius; its second primaries are extraordinarily prolonged and ribbon-like. In the small Long-tailed Nightjar Scotornis climacurus, inhabiting middle Africa, the central tail feathers are greatly elongated. The males of the South American genera Uropsalis and Macropsalis are distinguished by a forked tail with much elongated lateral feathers. In Hydropsalis, from South America; the outermost as well as the central tail feathers are prolonged. G.C.A.j. (j.M.) NIGHTJAR, OWLET: see OWLET-FROGMOUTH. NIGHTJAR, TREE: see

POTOO.

NILTAVA: substantive name of species of Niltava, a large mainly south-eastern Asian genus of flycatchers (for family see FLYCATCHER (1)). NITROGEN METABOLISM: see

EXCRETORY SYSTEM; METABOL-

ISM.

NOCTURNAL HABITS: characteristic of a minority of bird species, the great majority being entirely diurnal. Outstanding examples of special adaptations to activity in minimal light intensities are found in the Strigiformes, Steatornithidae, and the Apterygidae (see, respectively, OWL; OILBIRD; KIWI); but some of the owls--although all show the main adaptations to nocturnal habits--are in fact diurnal, or largely so. Other birds, notably' the Caprimulgidae (see NIGHTJAR), are crepuscular in habits, being active in the dim light of dusk and dawn rather than in full night or day; the Bat-hawk Machaerhamphus alcinus is a special case (see HAWK). Others again are nocturnal in their nesting activities but to a large extent diurnal in their search for food; examples are many of the petrels (Procellariiformes), e.g. ManxShearwater Puffinus puffinus, and a few penguins (Spheniscidae), e.g. Little Penguin Eudyptula minor (see PETREL; PENGUIN). Further, many aquatic and wading birds (e.g. Anatidae and Charadrii), in particular, are partly nocturnal as well as mainly diurnal, showing considerable activity on nights that are not too dark on the water or open ground. Even among birds that are as a rule strictly diurnal, many migrate by night, e.g. numerous small species of the Passeriformes (see MIGRATION). This may be largely or wholly an adaptation to the need for using the day for feeding.

396

Nocturnal habits

Short-tailed Shearwaters Puffinus tenuirostris waiting to take off from a vantage point, ascended before dawn. (P hoto: ] . Warham ). As the counterpart of nocturnal activity, quiescence during the day calls for concealment. This may be achieved in dense foliage or ground vegetation, or by virtue of cryptic coloration in more open situations. In many instances, however , the birds spend the day in holes or burrows used for nesting, and sometimes also for roosting outside the breeding season . This is true of various owls. Petrels that nest in burrows tend to have their comings and goings during the hours of darkness, and in the

daytime are either underground or out at sea. The Little Penguin, mentioned above , is similarly nocturnal to a large extent when ashore at its breeding places . The Oilbird Steatomis caripensis nests, and has its daytime roosts, in the utter darkness far inside great caves, where it finds its way by echolocation; similar nesting and navigational habits are found in certain SWIFrLETS , but these birds are otherwise diurnal. Nocturnal habits constitute a form of concealment, and like other

Swallow-tailed Gull Creagrus fur catus; the large eyes indicate the habits of the only nocturnalgull. (P hOlO: E .]. Hosking).

Tawny Frogmouth P odargus strigoides at night. Note the largeeyes, placed for binocular vision, as in owls. (P hoto: ] . Warham ).

forms may be either defen sive or aggressive . The flightless kiwis feed at night; and the oceanic petrels safeguard their unavoidable visits to land, for breeding, by resort there to nocturnal habits. On the other hand, owls use darkness--and their silent flight-for hunting; at the same time they exploit a particular source of food in animals that are themselves nocturnal. Likewise, the crepuscular night jars feed on insect s that fly in the twilight; and the case of the Bat-hawk is self-explanatory. In contrast, the Oilbird is frugivorous--the only nocturnal bird that is. The activities of shore birds are often governed more by the state of the tide than by the alternation of night and day . For sensory adaptations to nocturnal activit y see ECHOLOCATION; A.L.T. VISION . NODDY: substantive name (plural 'noddies') of Anous spp . (see TERN ) .

Nomenclature

NOMADISM: term used to describe movements of species that do not normally revisit either breeding site or non-breeding areas (see MIGRATION).

NOMEN: with adjectives conservandum, dubium, novum, nudum, oblitum, and triviale (see below). NOMENCLATURE: the scientific naming of species and subspecies, and of the genera, families, and other categories in which species may be classified (see TAXON). Scientific names are necessary because there must be names that are internationally understood, and also because vernacular names, where such indeed exist in common speech, are governed by popular usage and are thus liable to be inexact in their application or to change in meaning with the passage of time (see NAME, various entries). In practice, scientific nomenclature has fallen short of the ideal, for reasons partly inevitable and partly arising from human wilfulness and negligence. The only hope of uniformity lies in the subordination of individual views or prejudices to the generally accepted code and authority; to regard nomenclature as more than a means to an end is pedantry, and to take a minority course in a matter of convention is merely a nuisance. International code. So far as the Animal Kingdom is concerned, the practice of scientific naming is governed by the International Code of Zoological Nomenclature, and no other code has validity in any branch of zoology. The International Code is a system of rules and recommendations originally authorized by the International Congresses of Zoology. The current (third) edition of the Code (formerly 'Rules') is that provisionally approved by the Division of Zoology of IUBS (the International Union of Biological Sciences) at Helsinki (1979) and published in 1984. 'The object of the Code is to promote stability and universality in the scientific names of animals, and to ensure that the name of each taxon is unique ana distinct. All its provisions and recommendations are subservient to these ends, and none restricts the freedom of taxonomic thought or action.' Two points in the earlier history of international rules are of particular ornithological interest. The first set of rules to be generally accepted was that adopted by the V International Congress of Zoology in 1901; the British representative on the small drafting committee was an ornithologist, P.L. Sclater. Among earlier codes was that prepared, with special reference to birds, by the American Ornithologists' Union in 1885. Notable predecessors were the Strickland Code adopted by the British Association for the Advancement of Science in 1842, and the Dall Code published by an American zoologist in 1877. Binominal system. The Code embodies in legislative form the methods used by Linnaeus (Linne) and first consistently applied in the Tenth Edition of his Systema Naturae. These constitute the Binominal System (sometimes 'binomial' or 'binary'); and this has as its temporal starting point 1 January 1758, the year in which the edition was published. The essence is that every species is placed in a genus, and that the name of a species is a binominal combination, or 'binomen' (plural, 'binomina'), consisting of the name of the genus and a second word denoting the particular member of it; the first term of the binomen is the 'generic name', the second the 'specific name' (formerly 'specific trivial name'-the nomen triviale of Linnaeus himself). The name of a genus is used alone to designate that taxon as such. The specific name of a species has no meaning in isolation. Trinominal system. This is a more recent extension (Schlegel 1844)of the Binominal System and is coveted by the same rules. Where a species is divisible into subspecies (sometimes called 'races'), the binomen constituting the name of the species is for each of them extended by a third term, the 'subspecific name'; the 'trinomen' thus formed is the name of the subspecies. The species as a whole is nevertheless still referred to by its binomen. The subspecies that contains the namebearing type of its species is the 'nominotypical subspecies' , and the third term of its name is a repetition of the second. The International Code expressly does not provide for the nomenclature of infrasubspecific forms, e.g. 'varieties'; nor does it extend to the naming of HYBRIDS. Further, when a number of geographical populations described as separate subspecies are found to intergrade, more or less continuously, the CLINE (although of great importance in reality) is not itself a nomenclatural entity. Groups of taxa. The Code in its most recent form recognizes three basic taxa-the species, the genus, and the family. On these it founds

397

what it calls (for purely nomenclatural purposes) the 'species group' of taxa, comprising species and subspecies; the 'genus group' of taxa, comprising genus and subgenus; and the 'family group' of taxa, comprising superfamily, family, subfamily, tribe, 'and any supplementary categories required'. The names used for taxa within each group are 'co-ordinate', and are subject to the same particular rules (additional to the general rules applicable to all names). The names of taxa in the genus group and family group are single words. (For the other meaning of the term see SPECIES GROUP (1)). The Code expressly excludes provision for the nomenclature of taxa above the rank of superfamily. This is 'because the practice of zoologists in regard to them is not sufficiently uniform to permit the formulation of rules covering them at this time'. The taxa most commonly used at this level are class, subclass, superorder, order, and suborder; of these, class and order may be regarded as basic (see TAXON). Availability of names. The first requirement of a name is that it should be made 'available' for the purposes of nomenclature. This is done by proposing it, for a particular use, in a publication. The form of the name, the information about its proposed use, the circumstances of proposal, and the method of publication must be in accordance with the conditions laid down in the Code. These conditions have been made progressively more stringent in respect of names proposed after certain dates-1930, 1950, 1960; the conditions applied to names proposed earlier (from 1758 onwards) are necessarily in more general terms. A name once duly made available, even if it is or becomes invalid for reasons mentioned later, retains a permanent status in nomenclature; generally speaking, it can be used (at the same group level) only for its original purpose----except that the availability of a specific or subspecific name in one genus does not affect the use of an identical name in another. A name proposed in a manner or circumstances that do not make it 'available' acquires no such status and is not thereby barred for the future; such a name is called a nomen nudum or (if it failed in respect of uncertain application) nomen dubium. Priority; validity of names. 'Priority is the basic principle of zoological nomenclature. Its application may be moderated however, under conditions specified in the Code, to preserve a long-accepted name in its accustomed meaning.' Accordingly, the valid name of a taxon is the oldest available name applied to it, provided (i) that it is not invalidated by any provision of the International Code, e.g. those relating to homonymy (next section); (ii) that it has not been suppressed by the International Commission (mentioned later); (iii) that it has not become a forgotten name (defined below); and (iv) that it has not been superseded by the Commission's express grant of precedence to some other name (which thereby becomes what is sometimes called a nomen conservandum). The exceptional use of what are known as 'plenary powers' by the Commission, in the suppression and validation of names, is no new thing. Such a 'forgotten name' is one that 'has remained unused as a senior synonym of a name in general current use for more than 50 years', and it cannot be brought into use except by direction of the Commission. This provision should discourage the kind of antiquarian research that has too often led to instability of nomenclature by reviving names of overlooked priority discovered in old works, sometimes of indifferent merit. Preoccupation; Homonyms. A name that has been made available is automatically invalidated if found to be preoccupied by an earlier use, either in the identical form (for species-group names) or in some very close approximation to it (as defined in the Code). The rule is that a name of supraspecific rank must be unique in the Animal Kingdom; a name of specific or subspecific rank must be unique in the particular genus. Identical names for different taxa are 'homonyms' of each other; a difference of a single letter, except where dependent on a variable spelling of the original word, is sufficient distinction (i.e. 'Apus' and 'Apis' are not homonyms). The name in its oldest use is the 'senior homonym', in any other use a 'junior homonym'. The 'law of priority' operates here also; the 'senior homonym' is valid, if other conditions are satisfied, while junior homonyms are invalid. They must be replaced, by a junior synonym, if one exists, or by a 'new replacement name' (nomen novurn) if there is none-the term does not apply to a name for a new species. 'Primary homonyms' are those that were in fact homonymous from the outset, although possibly not detected as such until later. 'Secondary homonyms' are those that have become so as the result of taxonomic change-identical specific names may properly exist in related genera, but if these genera are later merged the two specific names become homonyms and one is invalidated; similarly, the splitting of a genus may

398

Nomenclature

validate a name that had hitherto been a junior homonym. Synonyms. Whereas 'homonyms' are identical names proposed for different purposes, 'synonyms' are different names proposed for the same purpose. The operation of the 'law of priority' in respect of synonyms has already been noted, but some points of terminology remain to be mentioned. The oldest of a set of synonyms is the 'senior synonym', and is the valid name if other conditions are satisfied; the remainder are 'junior synonyms' and are invalid, except that the next in order of priority will be promoted if for any reason the existing senior synonym is invalidated (e.g. through being or becoming a junior homonym). Synonyms are 'objective' (sometimes 'absolute' or 'nomenclatural') when they expressly refer to the same 'type' (see later), so that there can be no doubt about the identity of their meaning; they are 'subjective' (sometimes 'conditional' or 'zoological') when the identity of meaning is a matter of opinion and could thus be disputed. Loosely, 'synonym' without qualification is often applied to any junior synonym, as distinct from the valid name. A list of the names given by various authors to a particular taxon is known as the latter's 'synonymy'; this includes authors' names and publication dates, sometimes with full bibliographical references. The term may also be used for the relationship between different names for the same taxon. The type concept. It has become a fundamental principle of nomenclature that a name is firmly attached to a 'type'. However the subjective limits of a nominal taxon may be altered, the name stays with the objective type, i.e. with the part of the original taxon that includes it. 'The name-bearing type provides the objective standard of reference by which the application of the name it bears is determined, no matter how the boundaries of the taxon may change.' The type of a species-group taxon is a 'type specimen', originating from a 'type locality' (see TYPE SPECIMEN; and TYPE LOCALITY). The type of a genus-group taxon is a 'type species'. The type of a family-group taxon is a 'type genus'. Within a group the type of any taxon is also the type of its nominotypical subordinate taxon, if any. A type species must nowadays be expressly designated by the author of the name of a genus-group taxon; for older nominal taxa there are various methods of selecting a type for a genus if no designation was originally made (see TYPE SPECIES). A type genus is that on which the name of a family-group taxon is based-the names of such taxa are purely derivative, not invented ad hoc. The type genus is not necessarily the one with the oldest name; and there are provisions to obviate changes in the names of the family-group taxa with changes in generic names. Form of names. Scientific names must be either Latin or so formed that they can be deemed to be Latin; they are often derived from classical Greek, or formed from modern personal and geographical names or the like-and may even be arbitrary fabrications (thus, e.g. 'Dacelo' is an anagram of 'Alcedo' (see NAME, SCIENTIFIC)). They must be single words-two single words in a binomen, three in a trinomen; if a compound word is used, the parts must be united without a hyphen (subject to one rare exception probably not occurring in ornithology). Names must be written entirely in Latin or neo-Latin letters; and no figure, diacritic mark, apostrophe, or diaeresis may be used. The printing of linked vowels as diphthongs is now deprecated. Pre-existing names that do not conform with the-requirements are to be treated as incorrect original spellings and (like inadvertent errors) corrected; the corrected form keeps the date and authorship of the original. If the name consisted of two parts, these are to be united and any hyphen or apostrophe eliminated; if one part was in contracted form, the implication is that this should be written in full to make union possible. Diacritic marks are simply omitted, except that when the German umlaut sign is deleted the letter 'e' is to be inserted after the vowel that was modified. To give examples: novae hollandiae, clot-bey, l'herminieri, st. thomae, and riippellu respectively become novaehollandiae, clotbey; lherminieri, sanctithomae, and rueppellii; to some extent usage had been tending in this direction before the 1961 Code made the changes mandatory. Certain recommendations concerning the formation of new names are appended to the Code. Species-group names. A specific or subspecific name ('species-group' name in this sense-see SPECIES GROUP (1)) must be an adjective in the nominative singular agreeing in gender with the generic name, and changing in this respect if necessary; or a noun in the nominative singular standing in apposition to the generic name; or a noun (or, in some circumstances, an adjective used as a noun) in the genitive case. The genders and proper declension of non-classical names may often be

difficult to determine, but the Code gives detailed guidance. A specific or subspecific name is always spelt with a small (lower case) initial letter. Genus-group names. A generic or subgeneric name must be a noun in the nominative singular or be treated as such. It is always spelt with a capital initial letter. A subgeneric name does not form part of the binomen or trinomen, and except in taxonomic works it need not usually be shown at all; when required.Jiowever, the subgeneric name is given in parenthesis between the generic name and the specific name. (This practice must not be confused with that of showing a familiar but discarded generic name in parenthesis or brackets after the generic name actually used; such a name should be distinguished, within its parenthesis, by some such expression as ' ... formerly known as X-us'.) Use of italics. Generic, subgeneric, specific, and subspecific names are preferably printed in a typeface different from that of the text, usually in italics. This does not apply to the names of higher taxa. Family-group names. The names of family-group taxa are nouns in the nominative plural, and are always spelt with initial capital letters. They are formed from the name of the type genus, with the termination '-idae' (the 'i' is short) in the case of families and '-inae' in the case of subfamilies; the terminations '-oidea' and '-ini' are recommended in the case of superfamilies and tribes respectively. Names of higher taxa. As already mentioned, the names of taxa above the level of superfamilies are not governed by the International Code, and even within the ornithological field there is variation of practice. One convention (followed in the present work) is to derive the name of an order or suborder from that of an included family, adding the termination '-iformes' in an ordinal name, and using a normal Latin plural for a subordinal name; when this is not done, there may be confusing identity between an ordinal name of one author and a subordinal name of another (see ORDER). In a different convention, ordinal names may be independent fabrications, e.g. 'Tubinares'. The type concept does not, in any event, apply at these higher levels. Emendations. A scientific name, once established, cannot be rejected or altered simply because it is found to be inappropriate or even misleading. The stability of the conventional labels of which the system consists is more important than the accuracy of the meanings that prompted their adoption, e.g. than whether maximus is indeed the largest, or sinensis is characteristically Chinese. Further, a specific name cannot be rejected because it is a tautonym of the generic name, at one time thought by some to be objectionable. It is, however, permissible to correct a lapsus calami or a copyist's or printer's error in a name as originally proposed (and mandatory to remedy detects in form such as the intrusion of a hyphen or apostrophe). Otherwise, the original spelling must be retained even if it is demonstrably erroneous in some respect. Subsequent misspellings of an original name-as distinct from deliberate 'emendations' within the permitted limits-have no nomenclatural significance. Authorship. When the name of a genus (or subgenus) is mentioned by itself, the name of the author who first proposed it may be added; it is not usual to do this in respect of names of higher taxa. When the binomen constituting the name of a species is given, the name of the author who first proposed the specific name may be added; if he originally named the species in a different nominal genus, his own name is placed within parentheses to denote that he did not use the present combination in its entirety. A similar convention applies to the names of the authors of subspecific names, shown after trinominal combinations. The year of publication, or even the complete reference, may follow the author's name if the nature of the subject calls for this. Unless there is special reason to fear ambiguity in the use of a scientific name, however, authors' names are seldom necessary except in systematic publications. International Commission. The International Commission on Zoological Nomenclature is a permanent body that originally derived its powers from the International Congresses of Zoology (now succeeded by IUBS). It makes recommendations to successive 'Congresses' for the clarification or modification of the Code. Between 'Congresses' it makes provisional amendments to the Code in the form of 'Declarations', and it gives 'Opinions' and 'Directions' on nomenclatural matters not involving changes in the Code. It exercises 'plenary powers' to suspend the application of provisions of the Code in particular cases where stability or universality seems likely to be disturbed; among other things, it can annul or conserve any name. On the basis of the Opinions rendered, it compiles 'Official Lists' of accepted, and 'Official Indices' of rejected, names and works. The International Trust for Zoological Nomenclature

Numbers

is an administrative body acting for the Commission in matters of property and publication. The Standing Committee on Ornithological Nomenclature, appointed by the International Ornithological Congresses, has no powers of decision but makes recommendations to the International Commission with regard to names in the Class Aves. A.L.T. Jeffrey, C. 1977. Biological Nomenclature (2nd edn.) London. Mayr, E. 1969. Principles of Systematic Zoology. New York.

NOMINAL TAXON: the taxon, as objectively defined by its type, to which a given name applies (see NOMENCLATURE). A nominal taxon persists as a nomenclatural entity even if it has ceased to correspond with any taxon currently recognized for other purposes. NOMINATE: obsolete equivalent of

NOMINOTYPICAL.

NOMINOTYPICAL: adjective applied to a subordinate taxon, denoting that it contains the type of a subdivided higher taxon and bears the same name as that taxon (amended in suffix in family-group names, according to rank). Thus, every subdivided species has a nominotypical subspecies, in the trinomen of which the second and third terms are identical; every genus subdivided into subgenera has a subgenus with the same name as itself; and (for example) every family divided into subfamilies has a subfamily with the same name as itself (apart from ending in '-inae' instead of '-idae'). On the other hand, the definition (by its reference to types) excludes a species of which the specific name happens to be a tautonym of the generic name, and a genus with a name providing the stem of family-group names. It should be noted that the concept is purely nomenclatural; a nominotypical subspecies has no inherent pre-eminence over its fellows, and the term 'typical subspecies' is ambiguous as an equivalent. See NOMENCLATURE; TAUTONYMY; TYPE. NON -BREEDER: an individual which does not nest in a particular breeding season. NONPAREIL: cage-bird dealers' name for the Painted Bunting Passerina ciris (see BUNTING). NONSENSE ORIENTATION: see NAVIGATION. NON-VOCAL SOUNDS: see MECHANICAL

SOUNDS.

NOSTRIL: see NARIS. NOTOGAEA: see under

ARCTOGAEA; DISTRIBUTION, GEOGRAPHICAL.

NUCHAL: pertaining to the nape (see TOPOGRAPHY). NUCLEUS: see CELL. NUKTA: name used in India for the Comb Duck Sarkidiornis melanotos (see DUCK). NUKUPUU: H emignathus lucidus (for family see

HAWAIIAN HONEY-

CREEPER).

NULL HYPOTHESIS: see BIOSTATISTICS. NU MBERS: the number of different kinds of birds in the world, and their distribution by zoogeographical regions; the numbers of individuals of anyone kind in some stated area; the total of birds of all kinds in a given area; the grand total (so far as even an intelligent guess is practicable) of birds of all kinds in the whole world; also the number of individual birds constituting spectacular assemblies or taking part in great migratory movements. See also CENSUS; CLUTCH-SIZE; COUNT; DISTRIBUTION GEOGRAPHICAL; ECOLOGY; QUELEA CONTROL.

Number of species. Mayr (1963) estimated the number of living bird species at about 8,600. More recently a somewhat larger number is generally accepted, as there has been a tendency for some widespread polytypic forms to be subdivided and a number of new species have been discovered; a recent authoritative list (Morony et al 1975) recognizes 9,016 species. The new species discovered in successive recent decades are listed and discussed in a series of papers by Mayr and others (most

399

recently, Mayr and Vuilleumier 1983). The number of new species found in the Peruvian Andes, including some very distinct birds of uncertain taxonomic affinities, has been especially striking. Geographical incidence. No uniformly comparable estimates are available of the numbers of species in different zoogeographical regions. Obviously there is considerable overlap from region to region, and there is also the question of reckoning the sea birds, more readily grouped by ocean than by landmass. With such reservations in mind, general indications can be given: the number of breeding species in the Palearctic Region is about 950, in the Nearctic Region about 750. The Afrotropical Region may have over 1,500 species, Australasia (including New Guinea) about 1,100, seasonal migrants apart. The richest avifauna of all is found in the Neotropical Region-South America has been called the 'bird continent'-which is credited with some 2,500 breeding species. Size of species populations. Accurate estimates of population size are usually extremely difficult to obtain. Large, spectacular birds which are easily identifiable and have a very limited range (like the California Condor Gymnogyps californianus) are relatively easy, as are those species restricted to just one or two islands; next come colonial seabirds with a limited number of colonies and a definite breeding season, so that expeditions may count occupied nests at each colony; thereafter the problems, and the errors in estimates, inevitably increase. A further hazard is that bird populations are dynamic in time, space and numbers: distributions may change and numbers may increase or diminish start1ingly (in human terms) as part of a natural series of fluctuations. Nevertheless, such estimates as are available are of interest. Small populations. Fisher (1960) listed nearly 100 species in danger of extinction or with populations of less than 2,000 birds. The IUCN Red Data Book documents many of these which must be on the verge of extinction. There were just 12 Japanese Crested Ibis Nipponia nippon in 1965, 22 in 1984; and the California Condor population, estimated at below 50 birds in 1975, had fallen to about 20 in 1983. The case of the Hawaiian Goose or Nene Branta sandvicensis is hearteningly different. Fisher listed only 50 birds remaining in 1946, but an intensive and skilfully managed rearing programme centred on the Wildfowl Trust at Slimbridge, Gloucestershire, and later in collections elsewhere, has raised this number sufficiently for several hundreds of captive-reared young to be liberated on a reserve specially purchased for them on the Hawaiian island of Maui. The Whooping Crane Grus americana had a world population of 33 in 1959, 50 in 1968; by 1980, partly as a result of cross-fostering, the eggs being incubated and the chicks reared by other crane species, this had risen to 120. The wild population in 1984 was about 100. Some larger populations. In 1939, Fisher and Vevers surveyed 19 out of 22 known Gannet Sula bassana colonies, and believed that there were then about 165,600 Gannets breeding in the world. Since then, such large increases have occurred that the 1939 world population was almost doubled by the 1969 British and Irish 'Operation Seafarer' census of 138,000 pairs (Cramp et aI1974). The most recent estimate, in 1976, puts the world Gannet population at about 213,000 site-holding pairs, plus about 70,000 non-breeding birds (Nelson 1978). On a more parochial scale, the Great Crested Grebe Podiceps cristatus can be taken as an example of the handful of species in Britain for which regular census figures are available. From less than 100 birds in the latter half of the 19th century, the 1931 census showed about 2,800 adult birds. A repeat in 1965 showed an increase to about 4,500, and a further repeat in 1975 showed the increase to have continued, with between 6,000 and 7,000 adult birds counted. Possibly this increase arises in part from bird protection legislation, but more likely it is based on the tremendous boom in sand and gravel extraction for building purposes and the consequent creation of new stretches of suitable water. Even so, the grebes have had to contend with increasing chemical pollution of the water and disturbance from various recreational activities. Whilst the threat of extinction may be an effective stimulus to count scarce species, the financial threat posed by some birds to agricultural crops has provoked censuses of potentially damaging species. Thus the US Fish and Wildlife Service was able to document the results of state wide Red-winged Blackbird Agelaius phoeniceus roost surveys during the winter 1976/77 in Tennessee and Kentucky, which showed 2S roosts containing in excess of one million birds each and a total of 47 million birds for the two states. Also in North America, maximum annual wildfowl bags are established each year on the basis of population estimates. Regular counts of

400

Numbers

the Greater Snow Goose Anser caerulescens have shown a dramatic change in status from rarity to pest during this century. In 1900, the autumn population lay between 2,000 and 3,000; in 1921 between 5,000 and 6,000; in 1941 at about 20,000 and in 1966 about 80,000. Then the real expansion began, following a series of summers with good weather and successful breeding. A peak of almost 230,000 was reached in 1975, and numbers have since fluctuated about 200,000. The commonest bird in the world. Darwin suggested that the Fulmar Fulmarusglacialis was the commonest bird, pehaps basing his view on his encounters with Fulmars at sea in the North Atlantic. Fisher disagreed and proposed that another predominantly Arctic-breeding bird, the Little Auk Aile aile, might exceed the Fulmar in numbers. Difficult though such numbers are to estimate, or indeed comprehend in Britain where only a handful have been seen, there may be more than 100 million of the Antarctic-breeding Wilson's Petrel Oceanites oceanicus. It is possible also to guess at the most numerous Iand-bird. It could be either the House Sparrow Passer domesticus or the Starling Sturnus vulgaris, both now world-wide in scope, partly because of introductions. One of the weaver birds, the Red-billed Dioch or Quelea Quelea quelea, widespread in tropical Africa, in which single flocks may be over 1,000,000 strong, is an even more powerful contender. Quelea causes serious damage to cereal crops, and it is recorded (Crook and Ward 1968) that in the Republic of South Africa devastation of crops continued even after the slaughter by aerial spraying of over 100 million Quelea in one year. Considering that this estimate is only of the proportion of dead birds from only a proportion of Quelea's vast range, this is likely to be the world's most numerous bird. Some local populations. At least three attempts have been made to estimate the summer land-bird breeding population of Britain. The first was by E.M. Nicholson, who in 1932 arrived at a figure of about 80 millions. J. Fisher calculated about 100 millions in 1939, revising this to about 120 millions in 1946. These estimates were based on randomly taken sample counts from various habitats at various times, but since 1961 most census work has been carried out by members of the British Trust for Ornithology, on a greatly expanded and properly organized basis in the Common Birds Census (CBC). Using figures available from the annual census returns, and Ministry of Agriculture land-usage statistics, Fisher and Flegg (1974) arrived at a figure of about 134 millions for 1972. Bird population density varies widely with habitat: rough figures derived by Fisher and Flegg from the CBC indicate that with 17 birds/hectare, scrub is the richest habitat, closely followed by suburban and woodland areas, with a considerable gap to farmland at 6 birds/hectare, water areas 2.5 and most barren, moorland and hill grassland with about 1 bird/hectare. Obviously, the numbers of the various species differ greatly. Of about 500 species on the British list, only about 100 contribute significantly in numbers, and the great bulk-about 75°/o-is made up by less than 50 species. Fisher (1940) calculated that the most numerous birds in England and Wales were the Chaffinch F ringilla coelebs and the Blackbird Turdus merula with about 10 million each, followed by the Starling and the Robin Erithacus rubecula with 7 million each and the House Sparrow with 3 millions. Fisher and Flegg (1974) produced new estimates, with the Blackbird at 15 million, a newcomer, the Wren Troglodytes troglodytes in second place at 10.5 million, the Robin at 10 million, Chaffinch and Dunnock Prunella modularis at 8 million, and the Willow Warbler Phylloscopus trochilus, the most numerous summer migrant, with 6 million. An interesting contrast comes from Merikallio (1958), who carried out a comprehensive study of the birds of Finland. Most numerous was the Willow Warbler, with about 11.4 million, followed by Chaffinch (10.6), Tree Pipit Anthus trivialis (3.3), Willow Tit Parus montanus (2.8) and Spotted Flycatcher Muscicapa striata (1.9). Assemblies and movements. Some of the most spectacular manifestations of bird-life are to be seen at the breeding places of colonial nesters. Even the enormous gannetries of Grassholm, Bass Rock and St Kilda in Britain are dwarfed by the Antarctic rookeries of the Adelie Penguin Pygoscelis adeliae with over one million pairs or Sooty Tern Sternafuscata colonies on oceanic islands estimated at 1-10 million pairs. Perhaps the most spectacular feeding concentration of all must be the million or more Lesser Flamingos Phoeniconaias minor gathering on Lake Nakuru in Kenya. Roosts, too, hold large numbers. City centres like Trafalgar Square in London attract huge Starling flocks, but reed-bed roosts of millions of Sand Martins Riparia riparia and in the USA of the

Red-winged Blackbird Agelaiusphoeniceus may contain birds at a density exceeding 2.5 million birds/hectare. Birds on migration often travel in vast flocks, though as so many are night migrants, these tend to be more often observed by radar. Perhaps the most spectacular sights are at the short sea-crossings beloved by soaring birds, at the Bosphorus and the Straits of Gibraltar, where countless thousands of raptors and storks cross to Africa in spirals vanishing from sight into the sky. Looked at on a wider scale, the figures are even more impressive. Moreau (1961) gave his reasons for supposing that about 600 million European birds perform the MediterraneanSaharan transmigration each autumn. This means that 150,000 birds per km of longitude enter North Africa, an average of 2,500 per km daily (A.L.T.) J.J.M.F. over 2 months. Cramp, S., Bourne, W.R.P. & Saunders, D. 1974. The Seabirds of Britain and Ireland. London. Crook, J.H. & Ward, P. 1968. The Quelea problem in Africa. In Murton, R.K. & Wright, E.N. (eds.), The Problems of Birds as Pests. London. Fisher, J. 1940. Watching Birds. Harmondsworth. Fisher, J. 1960. Bird species in danger of extinction. In Jarvis, C. & Morris, D. (eds.). International Zoo Yearbook. London. Fisher, J. & Flegg, J. 1974. Watching Birds. Berkhamsted, Fisher, J. & Vevers, H.G. 1943-44. The breeding distribution, history and population of the North Atlantic Gannet (Sula bassana). J. of Anim, Ecol. 12: 173-213; 13: 49-62. Mayr, E. 1963. Animal Species and Evolution. Cambridge, Mass. Mayr, E. & Vuilleumier, F. 1983. New species of birds described from 1966 to 1975. J. Orn. 124: 217-232. Merikallio, E. 1958. Finnish birds, their distribution and numbers. Fauna Fennica no. 5. Helsinki. Moreau, R.E. 1961. Problems of Mediterranean-Saharan migration. Ibis 103: 373-427; 580-623. Morony, J.J., Bock, W.J. & Farrand, J. 1975. Reference list of the birds of the world. Am. Mus. Nat. Hist. New York. Nelson, B. 1978. The Gannet. Berkhamsted.

NUMBER SENSE: see

COUNTING.

NUMERICAL TAXONOMY: see CLASSIFICATION. NUMIDINAE: see GUINEAFOWL. NUN: substantive name of some mannikins Lonchura spp. (see ESTRILDID FINCH).

NUNBIRD: substantive name of Monasa spp. (see

PUFFBIRD).

NUNLET: substantive name of Nonnula spp. (see

PUFFBIRD).

NUPTIAL: pertaining to the breeding season, a term applied especially to plumage and display. NUTCRACKER: substantive name of the 2 species of Nucifraga; used without qualification, in Britain, for N. caryocatactes (see CROW (1)). See photo FOOD STORING. NUTHATCH: substantive name of the more typical species of Sittidae (Passeriformes, suborder Oscines); used in Britain without qualification for the common European species; in the plural, general term for the family. The family is widely distributed. Characteristics. Nuthatches are small birds, mostly c. 14cm long, but some up to 20 em. They are all similar in form; a compact body with a short tail, very long sturdy toes and claws, and a long symmetrically tapered bill. In many species a black stripe runs through the eye, and some have a black cap. The upper parts are blue-grey in most of the typical species, blue-green in 3 found in southern Asia. The under parts are white, grey, reddish brown, or chestnut. Sexual dimorphism is already evident in the juvenile plumage of some species. All members of the family are climbing birds that seek their food on trees, or in a few cases on rocks. Instead of using the tail for support when clinging to a tree trunk, like woodpeckers or treecreepers, they climb obliquely, with one foot high to hang from, and the other low for support. They can climb down a tree, head foremost, by the same method.

Nutrition

401

hence the name 'nuthatch' (nut hack). Many species store food, especially seeds, by hiding them singly in cracks or under bark, if possible hiding them so that they are not visible. Behaviour. Nuthatches are strongly territorial, and some defend a territory even in winter, when, however, some are social and form flocks. Voice. There are various calls, but the song mostly consists of repeated single notes that often sound like a trill. The songs of several species can be imitated by whistling. Breeding. Members of the genus Suta mostly nest in natural hollows in trees, but some small species make holes for themselves in dead wood; 2 species nest in crevices in rocks. Several species reduce the size of the entrance with mud and fill up all cracks; one fills up cracks only. Two rock nuthatches wall up a semi-enclosed hollow and constructs an entrance tube. The 6-10 eggs are white with reddish spots. Incubation takes 14-15 days. The young usually remain in the nest for 22-24 days and when fledged are fully capable of flying and climbing; in a further 8-12 days they are independent. See photo NEST SITE SELECTION. H.L.

Nuthatch Sitta europaea. (D. W.). Habitat. The great majority of the true nuthatches Sitta inhabit broadleaved, coniferous or mixed woodland, either lowland or montane, though the rock nuthatches S. neumayer and S. tephronota are found typically on rock faces or on buildings, as is the European S. europaea occasionally. Distribution. The family is predominantly Holarctic, with 4 species in North America and the rest in Asia and Europe. The family is not represented in South America, Australia or New Zealand. So far as is known nuthatches are non-migratory, except for individuals of the Red-breasted Nuthatch Sitta canadensis. The most widely distributed species is S. europaea, of which the many races range through the whole of Europe and northern Asia to the limit of tree growth, with a small population in Africa across from Gibraltar. The recently discovered S. ledanti is restricted to one mountain in Algeria. S. europaea is particularly adaptable, not specialized but capable of utilizing most kinds of trees and of seeds, making caches of the latter in autumn. The Chestnut-bellied Nuthatch S. castanea of southern Asia is similar, but differs in voice and in showing marked sexual dimorphism. The Eastern Rock Nuthatch S. tephronota, specialized as regards habitat, is found in the warmer parts of Asia; in Persia it occurs along with Neumayer's Rock Nuthatch S. neumayer, which reaches its western limit at the Adriatic. The Giant Nuthatch S. magna is restricted to the mountains of central Burma, northern Thailand, and Yunnan; it is as large as a Great Spotted Woodpecker Dendrocopos major and flies like a member of that family (Picidae). Other species in eastern Asia are the White-tailed Nuthatch S. himalayensis, the Yunnan Nuthatch, S. yunnanensis, and the Chinese Nuthatch S. villosa. Very similar is the Corsican Nuthatch S. whiteheadi, once thought to be conspecific with the Red-breasted Nuthatch of North America. In the Near East is found the rather unusually coloured Kriiper's Nuthatch S. krueperi. In the southern part of North America are found 2 closely related forms, the Pygmy Nuthatch S. pygmaea and the Brown-headed Nuthatch S. pusilla. In the mountain ranges of Afghanistan and Kashmir dwells the White-cheeked Nuthatch S. leucopsis; very similar but somewhat larger is the White-breasted Nuthatch S. carolinensis of North America. In southern Asia there are 3 brightly coloured species: the Velvet-fronted Nuthatch S. frontalis (coral-red bill in some races), the Azure Nuthatch S. azurea (confined to Indonesia) and the Beautiful Nuthatch S. formosa (Sikkim to eastern Assam). Food. Insects, spiders, and other small invertebrate animals are eaten. The birds inhabiting northern or mountainous areas feed largely on seeds in winter, and some small species are specialized for eating the seeds of conifers. Seeds and all larger prey species are hammered into cracks and are there either broken into small pieces or opened up by strong pecks. The European species is able to open even hazel-nuts,

Gao,W. 1978. On the breeding behaviour and feeding habits of the Black-headed Nuthatch, Sitta villosa Verreaux. Acta Zool. Sinica 24: 26~268. Garter, W. & Mattes, H. 1979. Zur Populationsgrosse und Okologie des neuentdeckten Kabylenkleibers Sitta ledanti Vielliard 1976. J. Orn. 120: 390-405. Lohrl, H. 1958. Das Verhalten des Kleibers (Sitta europaea caesia Wolf). Z. Tierpsychol. 15: 191-252. Lohrl, H. 196~61. Vergleichende Studien tiber Brutbiologie und Verhalten der Kleiber Sitta whiteheadi Sharpe und Sitta canadensis L. J. Orn. 101: 245-264; 102: 111-132. Norris, R.A. 1958. Comparative biosystematics and life historyof the Nuthatches Sitta pygmaea and Sitta pusilla. Univ. Calif. Pub. Zool. 56: 119-300. Vielliard, J. 1976. Le DjebelBaboret sa Sittelle, Sitta ledanti Vielliard 1976. Alauda 46: 1-42. Voous, K.H. & van Marie, J.G. 1953. The distributional historyof the Nuthatch Sitta europaea L. Ardea 41: 1-68. NUTHATCH, CORAL-BILLED: see

VANGA.

NUTRITION: the qualitative and quantitative aspects of diet. An adequate diet must supply a bird with (1) sufficient energy for activity and thermoregulation and (2) specific nutrients, such as amino acids, vitamins and minerals that are essential for body growth and maintenance. Energy requirements have been extensively studied in many domestic and wild species under a variety of environmental conditions (see ENERGETICS) but the detailed requirements for specific nutrients of most birds are still poorly known. Energy. Energy-yielding compounds are usually required in daily amounts of several grams per kilogram body weight. For many bird species the major energy-rich component of the diet is carbohydrate in the form of starch and sugars derived from vegetable foods such as seeds, fruit and foliage, though some seeds and fruit are also rich in fats. Cellulose and lignin are not digested by most birds, though those with large gut caeca, e.g. the subfamily Tetraoninae, may do so (see ALIMENTARY SYSTEM). Animal prey provides fats and some carbohydrates as a direct energy source. Usually, however, the large proportion of protein in animal food must also provide energy by the deamination (removal of the nitrogen group) of its constituent amino acids. The resulting organic acids can then be metabolized in the same way as the breakdown products of fats and carbohydrates (see METABOLISM). In the long term the energy expenditure of a bird is balanced by an equal intake of energy as food. If food intake is temporarily insufficient the remaining energy requirement is supplied by the consumption of body reserves, primarily fat, e.g. during overnight fasting, during incubation, or to sustain long-distance migration. If food intake exceeds the immediate energy requirement the surplus may be stored as fat, irrespective of the nature of the food. Water. Water comprises about 70% of non-fat body tissue. Small birds lose water more rapidly than large ones so that the daily rate of water intake is inversely related to body size. However, the minimum water requirement to avoid dehydration is considerably less than the ad lib consumption. Some desert birds may not need to drink at all, maintaining their water balance by concentrating their urine and by efficient conservation of the free water in their food (even dry seed contains some free water), together with water produced chemically by oxidation of the food.

402

Nutrition

Specific nutrients. While an adequate energy balance may be maintained by the breakdown of a wide variety of fats, carbohydrates and proteins, other essential metabolic processes demand the inclusion in the diet of minimum quantities of specific nutrients. Protein and amino acids. The maintenance of life requires a basal rate of nitrogen metabolism adequate for the continual renewal of body tissues. Additional nitrogen is required for processes such as growth, moult and reproduction. In the chicken on a nitrogen-free diet the basal rate of nitrogen excretion is about 2 mg per calorie basal energy expenditure but is double this amount when dietary nitrogen is freely available. In chickens and in the American Tree Sparrow Spizella arborea the latter rate of nitrogen excretion is obtained on a diet containing about 7% protein. The form in which dietary protein is ingested is of great importance. The amino acids from which new protein is constructed cannot all be synthesized in the body from other nitrogen sources. Certain essential amino acids (arginine, glycine, histidine, isoleucine, leucine, lysine, methionine, phenylalanine, threonine, tryptophan and valine) must therefore be present in the food, usually in daily amounts of about 0.1 g per kg of body weight or less. Not all are essential at all stages of the life cycle, e.g. histidine is not required for maintenance yet is essential during growth and reproduction, whereas glycine is necessary during growth only. The synthesis of large amounts of feather keratin during moult requires an abundant supply of the non-essential sulphur-containing amino acid cystine, which is not required in such quantities by other body tissues. Most birds, whose moult is prolonged over many weeks, can nonetheless meet this extra demand from the diet or by synthesis from other amino acids (Newton 1968). The seasonal dietary changes observed in wild birds will frequently indicate changes in requirement for protein, or for particular amino acids. For example, while the seed food of granivorous birds may provide an adequate balance and quantity of amino acids for moult, it may be inadequate for egg production and chick growth. In particular seeds are deficient in lysine, so that the diet during breeding, particularly of laying females and growing chicks, is supplemented by insects that are rich in lysine. An interesting temporary dietary specialization is shown by parent Great Tits Parus major, which feed their nestlings between 5-8 days old with large numbers of spiders (Royama 1970). Presumably spiders, which are otherwise unprofitable food, contain a nutrient essential at that stage of growth, which is scarce in other food. Minerals. As well as the main structural elements (calcium and phosphorus) and elements essential for maintaining homeostasis in body fluids (sodium, potassium, chlorine), other trace elements are required in much smaller amounts (magnesium, manganese, zinc, iron, copper, selenium and iodine). Compared with the organic constituents of the diet, minerals show a much higher degree of recycling within the body. Iron (for haemoglobin synthesis), iodine (for thyroid hormone synthesis)

and calcium are all recycled to some extent, so that the daily maintenance requirements may be difficult to determine. Calcium is particularly important during growth for bone formation and during laying for eggshell production. The maintenance requirement for calcium in hens is about 100 mg per day. Some of the calcium for eggshell formation is stored prior to use in medullary bone but many species supplement this to a large extent from dietary calcium, often collected specially in the form of snail shell, bone fragments or calcareous grit on the days when the eggs are receiving their shells in the oviduct. Calcium has been thought to limit reproduction in vultures, which feed only on the soft portions of carcasses. Various diseases of poultry are known to result from deficiencies of trace elements such as zinc, copper, manganese and selenium. Vitamins. Vitamins are required daily in the diet in only microgram quantities per kg of body weight but their absence can cause severe deficiency diseases. The water-soluble vitamins (e.g. the B vitamins thiamine, biotin, riboflavin and folic acid; vitamin C) function as coenzymes in specific metabolic reactions that occur widely in the body. Deficiencies of several B vitamins result in various leg disorders, at least in poultry, where they may develop rapidly despite the synthesis of all the B vitamins in the gut by microbial action. Many birds synthesize vitamin C in the kidney or liver or both, while others require a dietary source, e.g. the Red-vented Bulbul Pycnonotus cafer. The fat-soluble vitamins (A, D, E and K) act only at restricted locations in the body. Vitamin A is essential in the formation of visual pigments in the retina. It may be obtained directly in the diet or by the ingestion of f3-carotene from plant food, which is converted to vitamin A in the intestinal wall. Carotenoids are also important in the diet as precursors of many feather pigments, e.g. the yellow of orioles Onolus spp. and the reds of bush -shrikes Laniarius spp. and the Scarlet Ibis Eudocimus ruber. An adequate dietary supply of vitamin D 3 is important to laying hens since this has to be stored in the egg to ensure proper bone mineralization in the chick. Vitamin K stimulates the normal clotting of blood and deficiency, to which poultry are particularly susceptible, leads to haemorrhaging. P.J.J. Fisher, H. 1972. The nutrition of birds. In Farner, D.S. & King, ].R. (eds.). Avian Biology, Vol. 2. London. Newton, I. 1968. The temperatures, weights and body composition of molting Bullfinches. Condor 70: 323-332. Royama, T. 1970. Factors governing the hunting behaviour and selection of food by the Great Tit (Parus major L.). ]. Anim. Ecol. 39: 619-668.

NYCTIBIIDAE: see under NYCTICORACINI: see NYE: see

CAPRIMULGIFORMES; POTOO.

HERON.

ASSEMBLY, NOUN OF.

o

the observation of Scandinavian raptor passage. Ringing stations, too numerous to name individually, are now operating observatory techniques in most Western European Countries. In North America bird observatories are fewer than in Europe, but tend to be far larger establishments, each with permanent scientific staff. The Manomet Observatory in Plymouth, Massachusetts, and Point Reyes Observatory in California both research bird migration and are important ringing stations. These observatories are also concerned with wider ecological studies, especially on marine mammals. In Canada, Long Point Observatory is located on the north shore of Lake Erie. The observatory provides accommodation for both amateur naturalists and professional biologists and additionally Long Point administers two local summer field stations where visitor accommodation is also available. R.F.D.

OBSERVATORY, BIRD: an establishment, usually on a coastal headland or off-shore island, maintained primarily for the study of bird migration by observation and ringing (see MARKING; TRAPPING). In Britain, the mainland observatories tend to operate throughout the year whilst most island observatories confine activities from early spring to late autumn. The opportunity of handling large numbers of birds caught for ringing is used for various associated studies. Some observatories have experienced full time wardens, whilst others rely entirely on voluntary manning. Visitors are accommodated at most observatories. The prototype observatory was established on the North Sea Island of Heligoland in the mid-19th century when Heinrich Gatke commenced systematic recording of migrants. In addition to collecting specimens, which included many vagrants previously unknown in Western Europe, Gatke introduced a daily survey and estimation of numbers of migrant birds, which he continued until 1887. The daily census of birds present within a defined area is now standard practice at all British bird observatories and at many on the continent of Europe. The modern bird observatory at Heligoland was established by Weigold in 1909, when large scale trapping and ringing of migrants in specially designed wire-netting traps (still universally known as 'Heligoland traps') largely replaced the collection of specimens. In the early years of the present century, pioneering work in the British Isles was carried out by W. Eagle Clarke who spent substantial periods at such vantage points as Fair Isle, St Kilda, the Kentish Knock Lightship and the Eddystone Lighthouse. The repeated visits by Misses E.V. Baxter and L.]. Rintoul to the Isle of May (Firth of Forth) and of C.]. Patten to various Irish lighthouses were in the same tradition. Regular observatories came later, and their development has been a marked feature of non-professional ornithological endeavour since 1945. In Britain only two observatories were in operation before 1945: on the island of Skokholm (Dyfed) founded by R.M. Lockley, and on the Isle of May. Following the war disruption, both observatories reopened and others were started by local interests, often at locations where ornithologists of an earlier generation had found observation and collecting profitable. Observatories have always remained autonomous, but have enjoyed very close links with the British Trust for Ornithology which has co-ordinated their activities and regularly published their findings. Most observatories have produced detailed annual or bi-annual reports, and considerable analyses have been carried out, using the voluminous logs containing daily counts. Published results have shown the timing and scale of visible migration and, in many cases, the different migratory patterns of birds originating from different geographical areas. Furthermore, the daily counts of migrants covering a period of past decades are being used as crude indicators of the fluctuations of bird populations. The present English observatories are Dungeness and Sandwich Bay, both in Kent, Portland Bill in Dorset, Lundy Island off Devon, Walney Island in Cumbria, and on the east coast Holme in Norfolk, Gibraltar Point, Lincolnshire, and Spurn Point, Yorkshire. Bardsey Island, Gwynedd, is the main Welsh observatory following the termination of ringing at Skokholm in 1976. The Calf of Man is located just south of the Isle of Man. In Scotland, Fair Isle, Shetland, is especially famous for rare vagrants and the Isle of May is situated in the Firth of Forth. Cape Clear in south-west Ireland is an outstanding observatory for recording seabird migration. An observatory is established on Copeland Island off the east coast of Northern Ireland. Observatories elsewhere in Western Europe record visible migration

Brockie, K. 1984. One Man's Island [Isle of May]. London. Durman, R.F. (ed.) 1976. Bird Observatories in Britain and Ireland. Berkhamsted. Eggeling, W.]. 1960. The Isle of May: A Scottish Nature Reserve. Edinburgh. Ennion, E.A.R. 1959. The House on the Shore. London Riddiford, N.]. & Findley, P.W.]. 1981. Seasonal Movements of Summer Migrants. Tring. Williamson, K. 1965. Fair Isle and its Birds. Edinburgh.

OCCIPUT: the back of the head (adjective 'occipital')-see TOPOGRAPHY. OCEANIC BIRDS: birds capable of supporting themselves by feeding at a distance from land. Species confined to inshore waters such as divers and ducks are not usually included among seabirds, and it seems logical to exclude from the oceanic category the diving petrels, cormorants, darters, pelicans, skimmers, and about two-thirds of the terns and gulls as well, which rarely or never feed as far as 20 km from land. Distributions of inshore feeders are based on the geography of the land, and oceans tend to be barriers to their spread, whereas the distributions of the most pelagic species (e.g. albatrosses Diomedeidae) are based on the geography of the oceans and correspond, e.g. with those of whales. This restriction leaves a total of about 175 oceanic species, belonging to 13 families in 4 orders: (1) SphenisciformeS-PENGUINS; (2) Procellariiformes-albatrosses, shearwaters, PETRELS, storm-petrels; (3) Pelecaniformes-boobies, GANNETS, FRIGATEBIRDS; (4) Charadriiformes-PHALAROPES, SKUAS, GULLS, TERNS and AUKS. Feeding ecology. All sea-feeding birds have enlarged nasal glands, capable of excreting brine through the nostrils or mouth (see EXCRETION, EXTRARENAL) and thus ridding the body-fluids of excess salt. Oceanic birds have no need of fresh water; and none are dependent on plant foods. As on land, species frequenting the same feeding areas (habitats) tend to occupy different niches, separated by the nature of the foods they eat and/or their feeding methods (Ashmole 1971; Murphy 1936; and Fig. 1). Bird habitats at sea are defined by less familiar variables than those on land. Primary production in the ocean depends on microscopic green plants which live within 50-100 m of the surface (the euphotic layer); at greater depths there is not enough light for photosynthesis. The limit to productivity is set by the amount of nutrients available (especially nitrates and phosphates) and the rate at which they circulate through the food chain. The plants are eaten by small herbivores, mostly crustacea, and these by one or more tiers of carnivores. The cycle is completed by microbes which decompose dead organic matter and return the nutrients to the water; but there is a tendency for some of it to fall out of the euphotic layer before decomposition is complete, and thus gradually remove the nutrients from the system. Over the continental shelf productivity is generally high because, in comparatively shallow water, nutrients are fairly quickly restored to the surface by tidal and other water movements. This constitutes the neritic province, and in it living food of suitable size for birds is often abundant, not only at the surface but in mid water and on the bottom. One finds surface-feeders like gulls, and diving birds like cormorants, penguins, auks and ducks, some of which can go right to the bottom at 100m or more. In high latitudes plant productivity falls low in winter when the days are short, and some parts of the sea are covered with pack-ice, but

and operate ringing stations, especially in the Baltic Countries. In 1903,

many of the animals (including fish) survive in undiminished numbers, in

ringing commenced at Rossitten-a location then German but now renamed Rybachi and still operating as an observatory under its Russian staff. In southern Sweden, vast migrations are continuously recorded at Ottenbyand Falsterbo, the latter being a particularly famous location for

more or less quiescent states. Zooplankton is greatly reduced. Some of the birds migrate towards or even beyond the tropics, but many temperate neritic species are able to stay broadly in the same waters throughout the year. 403

404 Oceanic birds ~Uaha"Y;nglem

AERIAL PURSUIT - arctic skue chasing phalarope

______~

.: ,

~

DIPPING - frigate-bird chasing flying-fish

PATTERING-

~~ _SIOi"e~~::;;;~~&ar

noddy tern

SKIMMING - skimmer

SCAVENGING - giant petrel

HYDROPLANING pnon -s-

SURFACE PLUNGING - tern.

peticen.

tropic bird.

gannet.

booby

~URSUIT

PLUNGING - sneerweter

--------

---

t("

. d...

•

.~...

f"'IIlIllll.~ _.

~

'SURFACE SEIZING - phalarope,

_

albatross

~ BOTTOM FEEDING - scaups. eider

PURSUIT DIVING (FEET) - cormorant

(WINGS) - diving petrel. penguin, auk

Fig. 1. Seabird feeding methods. (After Ashmole in Nelson 1978, The Gannet).

Outside the continental edge lies the deep-water pelagic province. At the higher latitudes the plankton is again seasonal, often with a major burst of plant cells in the spring. Much of the abundant dead matter falls straight into the depths below and its nutrients are lost, at least for the rest of the season; they are only restored to the surface mainly through water-mixing in winter storms. The annual productivity of bird foodsmainly fish, squids and shrimps-is only a half to a third what it is in neritic waters on the same parallel; but a dozen or so transequatorial migrants among the shearwaters and storm-petrels manage to enjoy summer feeding twice a year. Seasonal changes are less marked in the subtropical and tropical waters. A very warm and therefore light and stable stratum, floating on top in the absence of strong winds, tends to prevent mixing. Productivity, although continuous, is therefore low, of the order of 1% of that in temperate neritic waters. The dearth of living organisms makes the water clear and blue, and deepens the euphotic layer; but what nutrient cycling there is, is efficient in the sense that little organic matter is lost into the abyss (Cushing 1975). The squid and fish that support the birds are sparse and keep down out of reach by day. Nevertheless this is the habitat of many gadfly-petrels and storm-petrels, tropic- and frigate-birds, boobies and sooty terns, all remarkably adapted to search for scarce food. Most feed from the air by dipping or quick-plunging (swimming under water evidently does not pay; the water being so clear, taking prey by surprise may be impossible). Their opportunities come when they find and follow schools of dolphins or tunnies, which drive flying-fish and other prey to the surface; or in the dusk and darkness when the plankton migrates to the top; or in places where the productivity is higher. High productivity in tropical waters is confined to local areas where nutrient-rich water has upwelled from below, as it does on a vast scale in the Canary and Benguela currents, and the California and Peru currents, which flow towards the Equator along the western coasts of Africa and the Americas. Trade-winds blowing offshore (and Coriolis force) roll the currents over to seaward, bringing up richer water on the landward side in which the plankton quickly starts to 'bloom'. Productivities can rise as high or higher than any found in temperate neritic seas, as off Peru with its once vast anchoveta fishery and its teeming guano birds. In some places the water drifts out to the westward in a tongue for hundreds of kilometres before the effect has completely waned, and so provides a large fertile enclave, isolated at a great distance from the nearest

comparable habitat. As a result, while low-latitude pelagic birds tend to have wide if not pantropical ranges, the upwelling specialists typically include endemics. The Humboldt-Peru current has most, including the Peruvian Booby Sula variegata, but the Benguela quite closely resembles it in having an endemic penguin and two salt-water cormorants, all diving in the turbid waters. Upwellings cause water to spread out on the surface, creating a 'divergence'. Winds can also drive two currents together, and force the denser water-mass to dive under the lighter, at a 'convergence'. The movements, though sometimes vast, are slow, so that anything carried on the surface stops when it reaches the sinking front and stays there. The front is soon marked by flotsam and a slick of oil (at least in part of biological origin) and immediately below the surface there is a similar pile-up of plankton buoyant or active enough to remain at the top and escape going under. This attracts fish and squids, and they attract birds sometimes in hundreds, hour after hour, at what may be the only place in a day's flight where they can feed to repletion and pick up a load for a far-away chick. Many such convergences (and divergences too) are local and transient, being produced by the swirls where currents meet. They occur in all seas, attracting terns, storm-petrels and phalaropes among other birds, but their importance diminishes in the higher latitudes where food is easier to find. In the global patterns of ocean circulation, particular water masses tend to perpetuate their own special characteristics of temperature, salinity and productivity. Recent exploration, e.g. the International Indian Ocean Expedition in the 1960s, has served to emphasize how responsive oceanic birds can often be to small differences in these characteristics, and the extent to which the birds have exploited them to diversify the number of pelagic niches. Many pairs of related species can be listed which avoid the costs of interspecific competition by becoming specialized to live in subtly different ocean habitats and thus promoting their own mutual exclusion. Wind drift. The wind must also playa part in differentiating habitats. Oceanic birds range from sparrow-sized storm-petrels to the great albatrosses weighing 7-12 kg. A wind strength of 100km/h is enough to blow spume off the combers, and the smallest swimming birds risk hurtling with it, unable to hold on. Wrecks of Leach's Storm-petrels Oceanodroma leucorhoa are well known in Britain, when migrant individuals have been caught in autumn gales and driven exhausted ashore. Less commonly phalaropes are similarly overtaken, and also Dovekies or

Odour

405

Little Auks AIle aIle although they, being able to dive, are less vulnerable. Normally the boreal storm-petrels and phalaropes complete their passage south before the gales, and they winter in calmer climes. Some terns make non-stop ocean flights but are not necessarily in danger when driven ashore. The larger pelagic species can often use the wind to advantage, e.g. to increase their hunting range. Sooty Shearwaters Puffinus griseus breed in the southern hemisphere and winter in the temperate westerlies of the North Pacific and North Atlantic. The majority of them direct their northward flight to reach the windward side of either ocean, thereby providing for the maximum leeward travel before they eventually return south to breed, thus completing a wide loop. The Short-tailed Shearwater P. tenuirostns does the same, but only in the Pacific. Many ringing recoveries of young Giant Petrels Macronectes giganteus prove that the majority leave their birthplace downwind, and that some survivors are capable of circling the southern ocean in 12months (J. W.H. Conroy); this may be a normal though perhaps not inevitable routine. Some Wandering Albatrosses Diomedea exulans evidently do the same (J.L. Mougin et aZ). A yearly circuit on the 50th parallel would require a mean leeward drift of 70 km/ day, a trifling distance to these untiring travellers. Oceanic birds show by their ability to get back, after long absences, to remote islands that are dots in the ocean, and to their nests, when experimentally removed and released at distances exceeding 1,000km, that they have superb navigational powers. These resemble in their effectiveness those exercised by a mariner with his sextant, chronometer and almanac. They may also be the same in principle, because physics seems to offer no feasible alternative (see NAVIGATION). Flight. Albatrosses and large shearwaters rival the vultures as economical fliers. They obtain free 'lift' from the combination of wind and waves. Waves tend to run with the wind but less fast, so that the overtaking air-stream flows up the back of each swell. Borne on its long stiff wings the bird alternately rises and falls, sweeping down into a wave-trough across the wind, turning steeply to windward to rise into the updraft above the on-coming wave, which carries it slanting up to a height of 10--15 m where the air-stream levels out. It then uses its height to glide off in the desired direction. The manoeuvre is endlessly repeated, 10--15 times a minute, the rate varying with the size of bird, wave and wind. P. Idrac found that albatrosses could glide indefinitely, given a surface wind of 18 km/h or more; a Fulmar needed at least 22-25 km/h, Calm weather tends to impose insupportable costs on an albatross and may force it to stay on the water. For this reason most species keep out of the tropical doldrums, though the Waved Albatross D. irrorata is endemic to Galapagos, which is on the Equator. Most if not all oceanic birds habitually fly by night as well as day. More remarkably, frigatebirds are known to reach 1,000 km from land at times, and Sooty terns Sterna fuscata can turn up almost anywhere in the tropical oceans, without ever resting on the water at all. Neither of them have waterproof plumage. Sooty terns experimentally prevented from taking off became waterlogged in as little as 25 min and were unable to rise until they were dried. Frigatebirds take longer to soak but are equally averse to swimming; they are big birds but astonishingly light, patrolling from a height as they ride on thermals and eddies. The Sooties beat their buoyant wings like other terns, and are not known to alight except on land at their breeding places. Indisputable facts have finally eroded disbelief, and the conclusion first published by the pioneer behaviourist J.B. Watson in 1908, that they can remain airborne, feeding by dipping to the surface, for months at a time has finally won the day. It is not inconceivable that they could doze at times, holding their posture, altitude and course by subconscious perception and control. Many oceanic birds will land unafraid on floating objects including bergs and sea-ice, though they will not alight on unfamiliar ground or, in the case of terns, on the water. Population ecology. The southern hemisphere, with vaster oceans, supports far more species than the northern. The largest taxon, the Procellariiformes (see PETREL), comprises nearly 100 species of which well 'Over half breed in the South Temperate and Antarctic zones, about aquarter in the tropics, and only the remaining sixth in the North Temperate and Arctic. Oceanic birds generally nest colonially. The

ODOUR: not noticeable in most birds, but some species give off a characteristic smell. The latter is often, for widely unrelated species, described as 'musky' , but in the absence of any systematic study it cannot be assumed that the realities so named are similar. The male Musk Duck Biziura lobata in the breeding season is said to be inedible because of its musky odour. The mature Muscovy Duck Cairina moschata smells musky and so does the adult Magpie Goose Anseranas semipalmata.

evolved in response to low and irregular rates of food intake. Most lay only one egg or rear only one chick from c/2. Incubation and fledging periods are prolonged, the former for reasons unknown, the latter presumably because the requisite amount of food may often take long to

marked are the Hoatzin Opisthocomus hoazin, Bald or Waldrapp Ibis Geronticus eremita, Puffin FratercuLa arctica, Hoopoe Upupa epops, several Hawaiian honeycreepers (Drepanididae) and most, if not all, of the Procellariiformes. The comparatively odourless state of the intact body of

pelagic foragers especially have frugal, protracted life-styles presumably

provide, even for one chick. Although parents and chick are both inured to fasting, nestling losses are often high. Such slow reproduction must necessarily be matched by longevity; thus a Fulmar Petrel Fulmarus glaciaLis (the best attested example), if it survives to breed, will live on average to about 44 years of age, showing how remarkably the risks to survival can be avoided. Predators lurk in the water, not in the air, which may partly explain the value of perpetual flight, as an alternative to speed in the water. Another common trait is long adolescence, often exceeding 5 and sometimes 10 years, which holds an unusually large segment of the population as non-breeders, permanently at sea or annually visiting the breeding colonies just to prospect. The reproductive rate is so low, even at best, that it needs only minor misfortune to put mortality ahead. The equilibrium would be unstable were it not for this great reserve of recruits, built up in good years, ready for the chance to fill gaps in the breeding establishment. Being colonial birds as well, the breeders must be prone to occasional wholesale destruction from local disasters. A standing reserve appears to be an essential stabilizing element in the long-life, slow-breeding strategy. An added benefit is that, except in emergencies, all new breeders will already have survived an arduous test of fitness (Wynne-Edwards 1962). Efforts to study the oceanic distribution of seabirds and its seasonal changes, go back to about 1920. Bird densities are still measured and compared by counting the numbers seen per unit time, in strip-transects from moving ships or (rarely) from light aircraft. Because there are specific differences in bird size, conspicuousness, and behaviour towards ships, it is difficult to convert the data into absolute densities per unit area. A few estimates of biomass, food consumption and energy flow have, however, been attempted (see Sanger 1972 and Furness 1978 for further references). See photo AGE. V.C.W-E. Ashmole, N.P. 1971. Sea bird ecology and the marine environment. In Farner, D.S. & King, J.R. (eds). Avian Biology, vol. 1. New York. Brown, R.G.B. 1980. Birds as marine animals. In Burger, J., OlIa, B.L. & Winn, H.E. (eds). Behaviour of Marine Animals, vol. 4. New York. Cushing, D.H. 1975. Marine Ecology and Fisheries. Cambridge. Furness, R.W. 1978. Energy requirements of seabird communities: a bioenergetics model. J. Anim. Ecol. 47: 39-53. Harrison, P. 1983. Seabirds, an Identification Guide. London. Murphy, R.C. 1936. Oceanic Birds of South America, 2 vols. New York. Pocklington, R. 1979. An oceanographic interpretation of seabird distributions in the Indian Ocean. Marine Biology 51: 9-21. Sanger, G.A. 1972. Preliminary standing stock and biomass estimates of birds in the subarctic Pacific region. In Takenouti, A.Y. (ed.). Biological Oceanography of the North Pacific Ocean. Tokyo. Wynne-Edwards, V.C. 1962. Animal Dispersion in Relation to Social Behaviour. Edinburgh.

OCELLA: eye-like pattern on plumage, e.g. in the train of a Peacock Pavo sp, OCREATE: same as 'holothecal' (see BOOTED). ODONTOGLOSSAE: former ordinal name of the Phoenicopteri (see under CICONIIFORMES; FLAMINGO). ODONTOGNATHAE: a superorder of extinct birds (see under CLASS).

ODONTOPHORINAE: see PHEASANT. ODONTOPTERYGES: see under

FOSSIL BIRDS.

Among other birds in which a characteristic odour is commonly re-

406

Oesophagus

most birds, as contrasted with mammals, can be related to the scarcity of cutaneous glands. Glands in the ear secrete a wax and others around the vent of some birds produce a mucus, but when an odour is present it is usually ascribed to the fatty acids of the uropygial or oil gland (see OIL GLAND; SKIN). Such compounds may enable colonial procellariiform birds to identify by smell their own burrows, chicks and mates. Grubb (1979) found that breeding Leach's Storm Petrels Oceanodroma leucorhoa walked upwind to their burrows after dark, and that plugging the nares or olfactory nerve prevented return. The functions of any scents from the uropygial glands of other birds have not been examined. One species where the oil gland does not seem to be implicated in a noticeable odour is the Crested Auklet Aethia cristatella where the bill plates have been described as smelling like tangerine oranges. Offensive odours may be emitted by ejecta from either end of the alimentary canal, both vomiting and defaecation being common reactions to threat of danger. In certain species these seem to have a repellent role. The wax esters in the stomach oil of Procellariiformes (see PETREL) have been shown to be dietary in origin and not the result of proventricular secretion as was thought. Regurgitation is more frequent and appears to be under greater control in the chicks of surface-nesters than of hole-nesters, suggesting that the squirting of stomach oil is a defence mechanism in the former. Many female ducks produce offensive excreta while incubating, and are apt to defaecate over their eggs when suddenly flushed. In the Eider Somateria mollissima, the faecal matter is particularly foul-smelling. Its unusual nature is probably due to the absence of food in the gut (incubating females sit for 26 days without eating) and the activity there of many anaerobic bacteria. The presence of the excreta with its foul odour has been shown to give the eggs protection against egg-eating mammals such as rats, and against Crows Corvus corone. Faeces from non-breeding Eiders do not have the same deterrent effect. The nesting and roosting places of some species become highly odorous through the accumulation of droppings and food refuse. The nests of many sea birds, raptors, and coraciiform species are cases in point. For the olfactory sense of birds, see SMELL; see also PALATABILITY OF BIRDS AND EGGS. (A.L.T.) 1.K. (1) Grubb, T.C. 1979. Olfactory guidance of Leach's Storm Petrel to the breeding island. Wilson Bull. 91: 141-143. Imber, M. 1976. The origin of petrel stomach oils-a review. Condor 78: 366-369. McDougall, P. & Milne, H. 1978. The anti-predator function of defaecation on their own eggs by female Eiders. Wildfowl 29: 55-59. Quay, W.B. 1967. Comparative survey of the anal glands of birds. Auk 84: 379-389.

OESOPHAGUS: consisting of the gullet and, where present, the crop (see ALIMENTARY SYSTEM). OESTROGEN: see ENDOCRINOLOGY

AND THE REPRODUCTIVE SYSTEM.

OFFSHORE HABITAT: see OCEANIC BIRDS. OILBIRD: Steatorniscaripensis, sole member of the Neotropical family Steatornithidae (Caprimulgiformes, suborder Steatornithes). It is known also as 'Guacharo' and, in Trinidad, 'Diablotin'. Although the Oilbird is generally placed in the order Caprimulgiformes, usually in a suborder of its own, its affinities are still not clear; in any event it occupies a very isolated position. Anatomically it is in general closest to the caprimulgiform birds, but in some characters it resembles the owls (Strigiformes) more closely. In its ecology and behaviour it differs strikingly from the other caprimulgiform birds, and indeed from all other birds. It is the only nocturnal fruit-eating bird. The Oilbird (length c. 35 em) is in appearance something between a large night jar (Caprimulgidae sp.) and a hawk (Accipitridae sp.). It has a powerful hooked bill surrounded by long vibrissae, long wings with a span of just over 1m, an ample tail, and short weak legs. The plumage is rich brown, barred with black and with a scattering of white spots that are especially conspicuous on the wing coverts. Oilbirds are gregarious, cave-living, nocturnal birds; they spend all the day crouched on ledges in the caves that they inhabit, flying out at night to feed on the fruit of various forest trees, chiefly palms and members of the Lauraceae. The fruit is plucked on the wing by means of the strong hooked bill; in intervals between feeding the birds have been reported to perch on bare branches, but so far very little is known about their behaviour outside the

Oilbird Steatomis caripensis. (C.E.T.K.).

caves. Fruit is brought back whole to the caves, apparently in the stomach (as there is no crop), and digested there during the day. The seeds are regurgitated and fall on the lower ledges and floor of the caves, forming a deep rich humus in which etiolated seedlings sprout but soon wither through lack of light. In addition to the clicking sounds which enable Oilbirds to navigate in pitch-dark caves (see ECHOLOCATION), they utter extremely loud screaming and snarling calls, which from a chorus of several hundred birds in a large cave become almost deafening. When flying at night outside the caves they utter occasional harsh cries, but not the echo-locating clicks. As their eyes are rather large and very sensitive to light, it seems probable that it is by sight that they orientate themselves outside the caves. It is probable that scent plays an important part in the locating of food trees. Many of them are notably spicy or aromatic, and the Oilbird's olfactory apparatus is very well developed. The nest is a bulky structure with a shallow saucer-shaped depression, placed on a ledge usually high up on the cave wall. It is made predominantly of regurgitated fruit of paste-like consistency applied directly from the side of the bill, but disgorged seeds and to a lesser extent the bird's own excreta also contribute to the structure. Nests are used year after year and grow in height as more material accumulates. The tempo of breeding is extremely slow. The eggs, usually 2-4 in a clutch, are laid at intervals of several days; incubation lasts about 33 days; and the young remain in the nest for up to 120 days. Both parents incubate the eggs. The young are hatched with a little sparse down, grow a second coat of down after about 3 weeks, and then the adult plumage. They become very fat, reaching a weight half as great again as the adult's by about the 70th day and then gradually losing the excess weight as the feathers grow. Because of the great amount of fat, which when boiled down yields an odourless and durable oil, young Oilbirds used to be, and to some extent still are, collected by the natives of the regions where they occur-hence their name. In Trinidad, eggs may be found at any time; but most clutches are laid in the early months of the year. Oilbirds occur from western Guyana through Venezuela and Colombia, to Ecuador and Peru, and in Trinidad. They are everywhere very local, depending on the presence of suitable caves. Most of these are in mountainous country, but in Trinidad there are some colonies in sea-caves along the rocky north coast. D.W.S.(I) Snow, D. W. 1961-62. The natural history of the Oilbird, Steatomis canpensis, in Trinidad, W.I. Zoologica (N.Y.) 46: 27-48; 47: 199-221.

OILED BIRDS: see OIL

POLLUTION.

OIL GLAND (alternatively 'uropygial gland'): an externally secreting organ located at the rump in the dorsal caudal tract at the bottom of the tail feathers. The uropygial gland (other synonyms: preen gland, glans uropygialis) is a symmetrical bilobed organ, the halves of which are separated by an interlobular septum which ends in a muscular isthmus in the papilla. Each lobe possesses a large number of tubules in which fat cells are produced. The decay of these cells (holocrine type of secretion) forms the greasy gland secretion which then enters into a cavity whence it leaves the gland through two or more orifices. The exterior of the gland, although concealed by overlapping plumage, may be bare but surrounded by a circlet of small feathers or covered by down. The gland may be more or less well developed in different groups of birds; swimming and diving species, however, generally possess large

Oil pollution

glands (e.g, penguins, grebes, petrels, gulls, ducks). It is also very large in the Osprey Pandion haliaetus. But even passeriform birds have comparatively large preen glands. The relatively heaviest glands (in percentage of body weight) were found in the Little Grebe Tachybaptus ruficollis (0.61%) and the Wren Troglodytes troglodytes (0.58%); the lightest (0.02%) in the fruit-doves iDucula, Ptilinopus). Small or very small glands are found in pigeons, night jars, parrots and herons. It seems that originally all birds possessed an uropygial gland, but some species lost it during evolution. Actually, a gland can be recognized in the embryonic stages of birds which lack a gland in the adult form (bustards, rheas, emus). Except for some small glands in the external ear passages, the uropygial gland is the only entirely developed skin gland in birds in contrast to the numerous sebaceous glands in mammals. Nevertheless, there exist numerous fat-producing loci in the integument of birds. The uropygial gland secretion predominantly consists of monoester waxes composed of more or less highly branched fatty acids and alcohols. The qualitative patterns vary significantly at the ordinal, or in some cases even at the family level. Thus relationships among birds can be studied by comparing these patterns (Chemotaxonomy); e.g. penguins and petrels exhibit very similar patterns and the wax profiles are consistent within the Anseriformes. Although early speculations on the function of the uropygial gland secretion agreed that it serves as a water repellent and preserves the bird against wetting, recent investigations make other functions more likely. Besides making the feathers flexible, the secretion seems to play an important role in plumage hygiene, since some of its constituents possess bacteriostatic and fungistatic properties; in the female Mallard Anas platyrhynchos fungistatic fatty acids are produced exclusively during the pre-incubation period and disappear thereafter. Regarding the often strong smell of preen gland secretions (especially in petrels) which is supposed to originate from the free wax constituents after lipolysis (the waxes themselves are odourless), it has been claimed that they are involved in chemical communication (pheromonal activity). Recent findings support this at least for geese. Experimental evidence has been presented that in some birds (e.g. the domestic chicken) the secretion applied to the plumage may have an antirachitic function enabling vitamin D to be synthesized under the influence of sunlight. These findings, however, could not be reconfirmed with pullets or pigeons, and it is thus very doubtful that the uropygial gland generally provides birds with vitamin D. Gland-ectomizing experiments have been performed with various species. No adverse effects were observed after the removal of the gland in pigeons, sparrows and chicken. Experiments on ducks, however, mostly agree in the observation that the plumage condition degenerated after gland removal, feathers becoming rough, dry and (A.L.T.) J.J. disordered.

OILING: see COMFORT BEHAVIOUR;

OIL GLAND.

OIL POLLUTION: the discharge of petroleum oils at sea became a serious problem when ships were converted from burning coal to oil during the second decade of the 20th century. Adverse publicity followed by legislation in the industrialized countries led to some improvement between the wars, but the problem recurred in a newform after the second world war when oil was no longer refined on the fields and tankers carrying it to users started to wash the waxy residues out of their tanks at sea afterwards. This has now been controlled to a large extent by the provision of reception facilities for waste oil at tanker ports, but they are still lacking in some ports used by cargo vessels while 'flag of convenience' fleets in particular are still notoriously careless. The great increase in size of tankers in recent years has also led to some spectacular wrecks, starting with the Torrey Canyon off Cornwall in March 1967, while during 1979 an oil-well began to leak off the east coast of Mexico. Oil floats on water and presents a special hazard to social aquatic birds which are accustomed to react to hazards by diving rather than flying, such as penguins, auks, divers, grebes, cormorants and sea duck. It varies in composition and has a variety of actions. Initially it may contain toxic compounds which may be inhaled by birds or get on their exposed parts and be ingested while preening, and these may cause local inflammation, pneumonia, enteritis and systemic poisoning, notably damage to the liver and kidneys, though it is not clear to what extent this is also due to stress, exposure, hypothermia, dehydration and electrolyte disturbances. These toxic compounds may be lost from the oil by

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evaporation and solution and it then becomes inert and causes its worst damage through contamination of the plumage and destroying its buoyant and insulating properties. The birds are no longer able to fly or feed, exhaust themselves swimming and keeping warm and die of exposure. Quite a small amount of oil may be sufficient to kill them or contaminate eggs. In recent years there has been a growing number of investigations of oil pollution. Light crude oils soon evaporate, while heavy ones are reduced to solid inert tar-balls, and the worst damage is caused by refined residual fuel oils which remain liquid longer and may contain toxic substances. The movement of the oil is most markedly influenced by the wind, and travels at about 3.3 % of its speed; bird bodies drifting after the oil at about 2.2% of the wind's speed, so the extent to which spilt oil and bird bodies come ashore depends on the wind. The amount of damage caused to bird populations depends mainly on whether the oil happens to drift into areas such as feeding grounds, the waters off breeding colonies, or estuaries frequented by large concentrations of social swimming species. The damage tends to be very much worse in hard weather during the winter in high latitudes, probably because the oil remains fluid longer at low temperatures and large numbers of birds then tend to accumulate in vulnerable places. Investigations have shown that the mortality which is usually under one dead bird per km of beach surveyed may then reach tens or hundreds of birds per km. Disasters involving thousands of birds are not infrequent and they may at times involve tens of thousands, but while mortalities running into hundreds of thousands have been claimed they have still to be proved. It is also still debatable whether oil pollution causes permanent harm to bird populations. It has been claimed that oil is responsible for a decline of auks along the southern periphery of their range all round the Northern Hemisphere, but in: western Europe at least the decline began in the eastern English Channel before the onset of serious oil pollution. While massive oil pollution certainly caused a temporary decline of auks and especially Puffins Fratercula arctica on the most important French colony on the Sept Iles off Brittany, it remains to be seen whether the damage is permanent. Similarly, while it has been reported that oil pollution has caused a decline of sea-duck, especially Long-tailed Duck or Oldsquaws Clangula hyemalis wintering in the Baltic, the reliability of the figures is questionable. While the permanence of the damage caused by oil to bird populations is questionable, there is no doubt whatsoever that oil pollution presents a humanitarian problem. Oiled birds are very conspicuous along the shore and attract vast public sympathy. Continual attempts are made to rescue them, often with little success. Recent research indicates that the main problems are that they often cannot be secured until they are moribund, and that people then have difficulty in feeding and cleaning them adequately. To achieve the best results the fittest birds must be selected and they then need to be fed and if necessary tube- or force-fed appropriate foods, usually small fresh fish (except for ducks), until they have at least regained their natural weight; they do better if they exceed it. When fit they need to be washed very thoroughly with a mild detergent or soap and rinsed continually until their plumage spontaneously regains its normal fluffy quality, after which they must be kept clean. The Royal Society for the Prevention of Cruelty to Animals is now obtaining a 1/3 success rate with auks in Britain, and the South African National Committee for the Care of Coastal Birds (SANCCOB) a 2/3 success rate with penguins. The procedure is hardly economic, but could be sufficient to save small threatened bird populations. It is better to avoid pollution. Ornithologists were largely responsible for securing the first legislation by the United Kingdom in 1922 prohibiting the discharge of waste oil in territorial waters. Other countries took similar action, but it was soon recognized as an international problem. An international conference was held in Washington in 1926 when it was debated whether to prohibit discharges entirely, or restrict them to specified zones; a convention to observe zones was never ratified though some shipping companies observed it. An Advisory Committee on Oil Pollution of the Sea was set up on the initiative of the British Section of the International Council for Bird Preservation to bring together all the interests in the countries affected in 1952. This committee organized another international conference the following year; the UK convened an inter-governmental conference in 1954 which agreed on a new convention. Among other things it provided for extensive zones where pollution was prohibited, for the installation of separators to remove oil from discharged ballast-water, and for reception facilities for

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Oil, stomach

the oil in ports. After it had been accepted by 10 nations this Convention came into force for tankers in 1958 and dry-cargo ships in 1961, by which time 15 nations supported it. It was the precursor of many further measures. In recent years the aim has been to prevent pollution entirely by increased care, enforced by severer sanctions and the development of a growing series of procedures for cleaning ship's tanks and then purifying any water that is discharged, and ultimately to keep ballast water in separate tanks away from contaminants. There has also been growing research into means of clearing up spilt oil, though these remain extremely inefficient and expensive. A growing number of nations is now also taking measures to regulate the condition and movements of shipping. It has become clear that the easiest way to control this persistent problem is through strict supervision of oil-handling procedures to prevent leaks, though regrettably it seems unlikely that they will ever be eliminated entirely. The results of individual incidents appear to be purely temporary, and despite a great deal of discussion and some research no remote consequences of pollution by the commoner petroleum compounds have yet been proved though persistently repeated pollution certainly leads to a local deterioration of the environment. (P.B.-S.) W.R.P.B. Bourne, W.R.P. 1976. Seabirds and pollution. In Johnston, R. (ed.). Marine Pollution. London. Croxall, J.P. 1975. The effect of oil on nature conservation, especially birds. In Petroleum and the Continental Shelf of North-west Europe, vol. 2, Environmental Protection. London. Ohlendorf, H.M., Risebrough, R.W. & Vermeer, K. 1978. Exposure of marine birds to environmental pollutants. US Department of the Interior, Fish and Wildlife Service, Wildlife Research Report 9. University of Newcastle upon Tyne, 1972. Recommended Treatment of Oiled Seabirds. Newcastle upon Tyne. Vermeer, K. & Vermeer, R. 1974. Oil pollution of birds-an abstracted bibliography. Can. Wildl. Servo Man. Rep. 29.

OIL, STOMACH: see PETREL. OLDSQUAW: American name (spelt as one word in AOD list) for the Long-tailed Duck Clangula hyemalis (see DUCK). OLD WORLD WARBLER: see WARBLER (1). OLFACTION: see SMELL. OLFACTORY BULBS: parts of the forebrain (see NERVOUS SYSTEM; SMELL).

OLIGOTROPHIC: see

EUTROPHIC.

OLIVE-BACK: alternative substantive name of some waxbills Estrilda spp. (see ESTRILDID FINCH). OMAO: or Hawaiian Thrush Phaeornis obscurus (for subfamily see THRUSH).

OMENS, BIRDS AS: the use of birds in augury (ornithomancy) or, more loosely, as omens individually (see FOLKLORE, BIRDS IN). This can be traced back into many parts of the Ancient World, where, for instance, birds were among the sacrificial creatures in whose entrails portents were 'read'. Indeed, the very word 'augury' refers to divination by means of birds, the first syllable, au-, deriving from Latin avis; similarlyauspex, whence our 'auspicious', denoted a man who watched birds (for divinatory purposes). In recent times organized omenist systems have survived in vigorous form only in south-eastern Asia, where in some places they constitute a full-scale 'animist pagan' system of ethics. This system is strongest among the inland peoples of Borneo, all of whom have versions of belief by which actions of a few selected species of mammals, reptiles and' especially birds are taken to indicate metaphysical conditions favourable or otherwise to currentor intended enterprises. Birds generally form between half and three-quarters of the animist code. Identification between birds and man is easy enough, in a pre-Darwinian context where man seldom feels superior and often regards other life around him, e.g. the munias (Estrildidae) which threaten his rice crops each year, as nearly co-equal. The position of the bird in relation to the observer, and its movements

or calls in flight, are the principal factors in interpreting the augury. A bird crossing one's path from left to right may be dangerous, from right to left very encouraging. Variants are innumerable, methods of propitiation numerous. In extreme conditions of persistent bad omens a group may even abandon their whole longhouse village; among the remote Sabans and Muruts of central north Borneo, to abandon a rice-field painfully cleaned from virgin jungle is not at all uncommon. Elaborate bird usages have lately disappeared from all but the remotest areas. Bird beliefs remain deeply engrained, however, associated with the part omen and other birds play in folklore, notably as ancestral demigods and mighty warriors. Bird augury was based largely on fertility and associated beliefs linked to head-hunting and war, and augurs were deliberately consulted before any such operations could be undertaken. The cessation of head-hunting in this century invalidated some of the basic premises. Yet the greatest ceremony over a large part of Borneo today is still 'Gawai Burong', the Feast of the Birds, now in effect a peaceful secular continuation of a once blood-marked rite of rejuvenation and continuity, symbolized in the great birds. A feature of bird augury is the variability of the birds selected. Thus the Sea Dayaks of south Borneo use one of the medium-sized woodpeckers and a tiny one Sasia abnormis, a rare jungle kingfisher Lacedo pulchella, the noisy Crested Jay Platylophus galericulatus, two rather uncommon and quiet trogons (Trogonidae), and a beautifully voiced shama Copsychus sp. The Land Dayak, Maloh, Kenyah, and Kayan peoples, however, put dominant emphasis on noisy, small, very common spider-hunters Arachnothera spp. and determine much of their daily and nightly lives thereby-whereas the Sea Dayaks ignore these. The Sea Dayak omen birds are all regarded as interchangeable bird-man deputies for their ancestor hero, Sengalang Burong (HornbillKite), and his brave sons-in-law. Related ideas were held in ancient Greece, northern India, and modern Africa; Sir James Frazer wrote in The Golden Bough: 'When the Nandi men are away on a foray, nobody at home may pronounce the names of the absent warriors; they must be referred to as birds'. All the Borneo omen birds are resident species; but it does not follow that all were originally so in the lands whence these peoples came in protohistorical times. Certainly, there is another important sequence of thought-notably in China and Borneo--centred on migratory birds. It is not difficult to see how this could lead directly to an omenist system. In China such beliefs persist even under Communism. The 'Red Bird of the South' ('teng huang'), a frequent phoenix-like form in Chinese art for over 2,000 years, is a symbolic bisexual conglomerate of several birds-the quail, coming to north China from the south as a portent of summer all along the mighty Yellow River, the peafowl, pheasant, junglefowl, eagle, and flying dragon. At the other end of the scale, in the remotest hinterland of central Borneo, the Kelabits determine their crucial rice-planting cycle by the arrival of a series of migrating birds reaching the Equator from the far north, indicating to man the sequence of clearing and planting, bedding, weeding, protecting, and harvesting the vital rice padi. These birds, which give their names to the months, are an eastern race of the Yellow Wagtail M otacilla flaua, Brown Shrike Lanius cristatus, Japanese Lesser Sparrowhawk Accipiter gularis, and Siberian Pale Thrush Turdus pallidus; all 'winter' above 900 m in the Bornean uplands and return north during March-April, after the rice crop has been gathered in. (T.H.) G.E.S.T.

OMNIVOROUS: having a varied and unspecialized diet.

o NTOGENY :

the developmental history of the individual (see DEalso BEHAVIOUR, DEVELOPMENT OF). This is contrasted with the evolutionary history of the species (or other taxon)--see PHYLOGENY. VELOPMENT, EMBRYONIC; GROWTH;

0-0: see HAWAIIAN

HONEYCREEPER.

OOCYTE: a cell in the sequence leading to the formation of an ovum (see ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM). OOLOGY: the scientific study of the eggs of birds, with particular reference to external characters such as shape and size, texture and coloration of shell, and number in clutch (see EGGS). Extension beyond this overlaps the more general field of reproductive physiology and behaviour (see, for example, BREEDING SEASON; CLUTCH-SIZE; IN-

Oriental Region

The study of the contents of the egg, and of the developing chick within it is covered by DEVELOP-

CUBATION; LAYING; BROOD-PARASITISM). MENT, EMBRYONIC.

The main descriptive phase of oology as a form of systematic work has been completed for most parts of Europe and North America; but in some parts of the world there is still very much to be learnt, the eggs of many species being as yet either wholly unknown or the subject of only meagre information. Regrettably, scientific oology is obscured by controversy over egg-collecting, now illegal in many countries except under licence, but still rife in Britain. B.C.

OPENBILL: also 'Open-billed Stork' Anastomus spp. (see STORK). OPEN SEASON: period when certain birds may legally be shot for sport. OPERCULUM: a covering flap, as over the anterior nares or the external auditory meatus in some birds (see BILL; NARIS; OWL). OPISTHOCOMI; OPISTHOCOMIDAE: see under

GALLIFORMES;

HOATZIN.

OPTIC LOBES: parts of the brain (see NERVOUS SYSTEM). OPTIC NERVE: see

VISION; NERVOUS SYSTEM.

OPTIMAL FORAGING THEORY: the application of OPTIMALITY to the study of how animals search for and exploit food. In this approach it is hypothesized that foraging behaviour can be described by mathematical models which assume that the animal is designed (by natural selection) to maximize some aspect of foraging success such as energy intake, protein intake or balance of nutrients. Such models can be tested, thus revealing whether the particular design criteria and constraints embodied in the model are correct. THEORY

OPTIMALITY THEORY: a body of mathematical theory concerned with the analysis of the 'best way' to allocate 'scarce resources' among various alternatives. Although originally developed in the context of engineering and economics, optimality models have been applied to biology in an attempt to understand how organisms have been designed by natural selection. For example, many features of living organisms, from the biochemical to the behavioural level of organization, can be accounted for by the hypothesis that the maximal energetic efficiencyis a design criterion. It is sometimes mistakenly thought that optimality models are used to test the idea that organisms are optimal. This is not so. They allow one to test whether the design criteria and constraints embodied within the models are realistic. Optimality models are used as an analytical tool because of the conviction that natural selection favours good design. ORANGEQUIT: Euneornis campestris, a small Jamaican passerine bird of uncertain affinities, tentatively placed in the subfamily Thraupinae (see TANAGER). It has a sharply pointed, decurved bill and feeds largely on nectar. ORANGETHROAT: Luscinia pectardens (for subfamily see THRUSH). ORBIT: see SKULL. ORBITAL: applied to a distinctive area, in some plumage patterns, round the eye. ORBITOSPHENOID: a paired bone of the

SKULL.

ORDER: a primary taxonomic category, a sub-division of a class, and a grouping of families; other categories may be interpolated between these primary ones to build up a more elaborate hierarchical system, especially subclass and superorder on the one hand, suborder and superfamily on the other (see CLASSIFICATION; TAXON). In accordance with the International Code of Zoological Nomenclature every ordinal name ends in '-iformes'; earlier use favoured '-morphae'. Whereas the family is the most convenient group for most general purposes, the aim of ordinal grouping is to express a supposed phylo-

409

genetic relationship between families. At this level, however, the suppositions tend to become very uncertain and highly speculative; the content of orders has therefore not only changed greatly with advancing knowledge but is also the subject of differing views. Authorities who are sceptical about evidence of relationships naturally tend to preserve a greater number of separate orders of limited content; those who are bolder place more families together and thus reduce the number of orders. Authors who adhere to cladistic systematics must by necessity use either a relatively large number of orders or an almost infinite number of taxonomic subdivisions or do both. Nevertheless, many orders are not in serious dispute. Some of these comprise only a single family, and the ordinal rank merely expresses the view that the family does not appear to have any known near relationships; others comprise a few families that are generally accepted as being more related to each other than to other families. The greatest difference of opinion concerns the large assemblages of families regarded by some as gruiform and coraciiform respectively. Even the Order Passeriformes, generally accepted as having ordinal characteristics clearly separating it from all the other groups, has been treated in a cladistic system as two orders of supposedly independent phylogenetic origin: Tyranniformes and Passeriformes sensu stricto (Feduccia 1975, 1977). In listing orders it is customary to begin with those that are believed to be the most primitive and to proceed towards the most highly developed, the Passeriformes. The placing of the orders is obviously speculative in high degree; any list must be arbitrary in that no linear arrangement could adequately express four-dimensional relationships grown in space and in time. The classification of orders followed here is that proposed by Voous and represents in some way a combination of the well-known systems of Wetmore and Stresemann. It can be found in the Table of Classification in the preliminary pages. Suborder. The suborder is a secondary taxonomic category, a subdivision of an order and a grouping of superfamilies (if any) and families. Not all orders are divided into suborders, the category being used only when required; its necessity depends on the philosophy of the classification system followed and is greatest in cladistic systematics. Other systems may tend to give independent ordinal rank to what are considered suborders elsewhere. Names of suborders end in ordinary Latin plural forms ('-i, '-ae', '-es'). As some authors end their ordinal names in the same way, these can be identical with the subordinal names of others. The International Code of Zoological Nomenclature does not apply at this level. For superorder see under CLASS; for superfamily see under FAMILY. K.H.V. Feduccia, A. 1975. Morphology of the bony stapes (columella) in the Passeriformes and related groups: evolutionary implications. Univ. Kansas Mus. Nat. Hist. Misc. Publ. 63: 1-34. Feduccia, A. 1977. A model for the evolution of perching birds. Syst. Zool. 26: 19-31. Stresemann, E. 1959. The status of avian systematics and its unsolved problems. Auk 76: 269-280. Voous, K.H. 1973. List of recent Holarctic bird species. Non-passerines, Ibis 115: 612-638. Voous, K.H. 1977. List of recent Holarctic bird species. Passerines. Ibis 119: 223-250, 376-406. Wetmore, A. 1960. A classification for the birds of the world. Smithsonian Misc. CoIl. 139 (11): 1-37.

ORGANO-CHLORINE: see TOXIC

CHEMICALS.

ORIENTAL REGION: one of the main zoogeographical divisions of the Earth (see DISTRIBUTION, GEOGRAPHICAL); also known as the Indian Region, although that adjective is better retained for the subregion covering the greater part of continental and peninsular India, with Sri Lanka. Boundaries. The Oriental Region lies mainly between 68° and 135°E and between 100S and 32°N, therefore largely within the tropics. Its northern boundary, dividing it from the Palearctic Region, runs from the Hindu Kush Mountains in the west along the entire length of the Himalaya, and farther east to include Yunnan and Szechuan. It continues roughly south of the basin of the Yangtze Kiang to form an indeterminate frontier with the Manchurian Subregion of the Palearctic till it reaches the East China Sea in the neighbourhood of Ning-po in c. 30 From its western extremity the boundary trends south-west, excluding Afghanistan and Baluchistan, and may conveniently be taken as the valley of the 0N.

410

Oriental Region

Fig. 1. Transitional zone at boundary with the Australasian Region. The classical Wallace's Line (dots) approximates to the western limit of this zone-J Java (part), B = Bali, L = Lombok; Weber's Line (dashes) represents its median, where the two faunas are more nearly balanced. The islands between Wallace's Line and New Guinea are sometimes collectively termed 'Wallacea'.

Indus down to its mouth near Karachi in Pakistan. South of the Asian mainland, the Oriental Region includes the continental islands of Taiwan and Hainan as well as the greater part of the Indonesian Archipelago, the Philippines, Borneo, Sulawesi, and the Greater and Lesser Sunda Islands east to Timor. There are curious clear-cut divisions as well as close intermingling between the characteristic Oriental and Australian faunas on many of the islands in this area, and the line of demarcation from the Australasian Region is not easy. In the last century, since Wallace first postulated the boundary between the islands with a mainly Indo-Malayan fauna and those with the AustraloPapuan type, a succession of investigators (including many ornithologists) have conducted intensive faunal studies on the islands to determine their correct biogeographical status. The demarcation originally proposed by Wallace-'Wallace's Line' as Huxley named it----on the basis of the presence or absence of certain typical bird and other animal groups of the Oriental and Australasian Regions at first enjoyed a wide measure of acceptance from zoologists on account of the truly remarkable examples of clear-cut divergence which it showed, e.g. as between the islands of Bali and Lombok, separated by a deep and narrow strait (only 25-30 km wide), and as between Borneo and Sulawesi. Many dominant Oriental bird groups, e.g. the barbets (Capitonidae), range as far east as Bali and then suddenly break off, being completely absent from Lombok and beyond. Woodpeckers (Picidae), abundant in the Oriental Region as far east as Borneo, Java, and Bali, are very poorly represented (by only 4 or 5 species) in Lombok, Sulawesi, and eastward up to the Moluccas, being absent over the rest of the Australasian Region. On the other hand, many typically Australian groups, e.g. honeyeaters (Meliphagidae) and cockatoos (Cacatuinae), reach westward as far as Lombok, but there end abruptly. The faunal differences on the opposite sides of the Strait of Macassar, between Borneo and Sulawesi, are superficially even more striking; they are not confined to birds but extend to mammals and other animal groups. The line, as postulated by Wallace, passed between Bali and Lombok in a north-easterly direction, through the Macassar Strait separating Sulawesi from Borneo, and then on ENE between Mindanao and Sangi Islands, passing west of the Marianas or Ladrones group. Huxley's proposed modification, by drawing it north from the Macassar Strait to pass between Palawan and Mindoro Islands, excluded the Philippines from the Indo-Malayan Subregion. On statistical analyses of the extensive data accumulated by investigators since Wallace's time, on a percentage basis of typically Oriental and typically Australasian faunal elements present or absent on the various islands, it was realized that a more rational boundary between the two regions would be one that showed a faunal balance, i.e. with the Oriental and Australasian elements in more or less equal proportions. A line of

this nature can of course be only arbitrary, since the 50: 50 balance does not hold good for all taxonomic groups. Such a line of faunal balance between the Oriental and Australasian faunas was first demonstrated by Weber, in 1902, to exist much farther east than Wallace's Line. As modified by subsequent investigations, Weber's Line runs roughly along the Molucca Passage between Sulawesi and the northern Moluccas, southward between Sula Islands in the west and Obi Islands in the east, swings west of Buru, and, leaving Timorlaut Islands on its east, curves WSW along the edge of the Sahul Shelf to include Timor in the Indo-Malayan Subregion. Thus, on consensus of current views, all the islands in the intermediate zone between Wallace's Line and its eastern counterpart-the 'Wallacea' of some zoologists-belong to the IndoMalayan Subregion. Characteristic groups. One bird family is peculiar to the Oriental Region, the leafbirds (Irenidae), and is in fact confined chiefly to the IndoChinese Subregion. The Oriental Region shares with the Afrotropical Region, either exclusively or overwhelmingly, the passerine families Eurylaimidae, Pycnonotidae, Nectariniidae, and Ploceidae. The typical Ethiopian family of the honeyguides (Indicatoridae) is represented here (but in no other region) by the common genus Indicator. Many genera, e.g. Harpactes (Trogonidae), Nyctiornis (Meropidae), Psiuacula and Loriculus (Psittacidae), Acridotheres and Gracula (Sturnidae), and Pericrocotus (Campephagidae), are confined to it and do not occur at all outside its limits. The family Phasianidae is particularly well developed in the Oriental Region, the spectacular genera Pavo, Gallus, Lophura, Pucrasia, Catreus, Argusianus, Polyplectron, and Rollulus being peculiar to it. Subregions. The region is readily divisible into the following three main subregions upon the general spectrum of their avifauna and other animal groups: 1. The Indo-Chinese Subregion (= 'Himalo-Chinese' of H.J. Elwes and H.F. Blanford) 2. The Indo-Malayan or Malaysian Subregion (= 'Malayan' of above authors) 3. The Indian Subregion The first two are essentially very similar in regard to their physiography, being covered largely with tropical and subtropical vegetation, the result of heavy monsoon rainfall and high humidity. Nevertheless, they each exhibit marked peculiarities in many of their plant and animal manifestations, the first subregion showing an affinity with the Palearctic in its temperate zone forms, e.g. the Fringillidae, while the second possesses elements with distinctly Australo-Papuan affiliations. The Indo-Ckinese Subregion. This includes the southern aspect of the entire Himalayan Range (up to the tree-line-3,000 to 4,000m elevation), particularly the section that lies east of the Arun- Kosi River in eastern Nepal. Beyond, its boundary extends into north-western and eastern China, marching with the Palearctic Region. Many typically eastern genera, e.g. Paradoxornis, terminate in Sikkim and Nepal, but the avifauna of the Himalaya westward of the division indicated retains its overall Indo-Chinese character in diminishing degree. This tendency is well illustrated by many other timaliine genera, e.g. Garrulax, abundantly represented in Yunnan and the eastern Himalaya, but sparsely in the western. Besides the Himalaya, this subregion includes Assam, Burma, Thailand, and Indo-China (Vietnam), i.e. the entire portion of the Oriental Region lying on the Asian mainland east of the Ganges delta, with the exception of the Malay Peninsula. It also includes the islands of the Andamans group, as well as Taiwan and Hainan. The Indo-Malayan or Malaysian Subregion. This lies for the most part within a tropical belt 10° on either side of the Equator and includes the Malay Peninsula south of the Isthmus of Kra, together with all the islands of the Archipelago west of Weber's Line. The Nicobar Islands, off the western tip of Sumatra, show closer avifaunal affinities with this subregion than with the Andamans, which are spatially nearer to Burma. This subregion is more exclusively tropical and forested than either of the others. Its avifauna lacks all traces of Ethiopian affinities, so noticeable in the Indian Subregion. It also lacks temperate zone forms of the Himalaya with Palearctic affiliations, such as the rose finches (Fringillidae). The Indian Subregion. This stretches southward from the foot of the Himalaya to include the entire peninsula and Sri Lanka. Its western boundary is that of the Oriental Region-the Indus Valley-while on the east the deltas of the Ganges and Brahmaputra rivers demarcate it from the Indo-Chinese Subregion. Two clear-cut 'provinces' are recognizable which, for convenience, may be termed

Oriole

(a) The Peninsular Province, covering all India and Sri Lanka except the portions under (b); (b) The South-western Province, the tropical humid, heavy-rainfall zone commencing at the northern extremity of the Western Ghats in Khandesh and the Surat Dangs, but more properly south from about Goa (c. 15°30' N) including western Karnataka, the Nilgiri and Palni Hills, and Kerala, together with its virtual extension in south-western Sri Lanka-the so-called 'Low-country Wet' and 'Central Hill' zones. The avifaunal character of the Peninsular Province is largely Palearctic and Ethiopian. A typical example of the latter is the cursoriid genus Rhinoptilus (currently merged in Cursorius) with several species in Africa but only a single one, C. buorquatus, in peninsular India. There is an almost complete absence of characteristic east-oriental genera of birds in this province, as there also is in the Afrotropical Region. The South-western Province, although much smaller, is one of the most interesting areas, from the biogeographical point of view, by virtue of the very striking similarities and parallelisms its fauna and flora exhibit with those of the far-flung Indo-Chinese and Malaysian subregions. It constitutes the western terminal of what is known as the 'Indo-Malayan Are' or 'Horseshoe' of animal distribution: Malaya-Burman-eastern Himalaya-Sri Lanka. Several typical sedentary birds inhabiting its two extremities (e.g. Chrysocolaptes lucidus, Buceros bicornis) are morphologically inseparable, even at subspecific level. These remarkable 'relict populations' of south-western India, now cut off from their nearest neighbours in the Himalaya by up to 2,500 km, have received special attention from zoologists in recent years. Much interest has been aroused by the very attractive 'Satpura hypothesis' of the Indian zoologist, S.L. Hora, which seeks to explain the history, route, and mechanics by which freshwater hill-stream fishes, and other specialized hygrophilous fauna of the Indo-Chinese Subregion, reached Kerala and Sri Lanka. This hypothesis postulates a once continuous mountain trend from the eastern Himalaya and Garo Hills, across peninsular India over the Rajmahal Hills and the Satpura Mountains, and then southward over the Sahyadris or Western Ghats to Kerala and Sri Lanka. Sri Lanka, which was alternately joined to and separated from peninsular India during various geological epochs, bears evidence of having received distributional faunal wavesfrom the mainland. Under periods of prolonged isolation, many endemic races (or species, as some ornithologists consider them) have developed on the island. The avifauna of the humid South-western Province contains one monotypical muscicapine genus, Ochromela (now Muscicapa), peculiar to its mainland section. Numerous examples can be cited of birds not occurring in the adjoining Peninsular Province, but having close affinity, or even identity, with forms living in the eastern Himalaya and in the Indo-Chinese and Indo-Malayan Subregions generally. Prominent among such are laughing thrushes Garrulax spp., Fairy-bluebird Irena puella, woodpeckers of the genera Dinopium, Hemicircus, Dryocopus, and Picumnus, Great Hornbill Buceros bicornis, spinetail swifts Chaetura spp., Broadbilled Roller Eurystomus orientalis, Malabar Trogon Harpactes fasciatus, Frogmouth Batrachostomus moniliger, and the falconid genus Aviceda. Some of these birds, e.g. Dryocopus, Hemicircus, Picumnus, Buceros, curiously enough, are not found in Sri Lanka: the complete absence of vultures Gyps spp., so common and abundant on the Indian mainland, is another anomaly not easily explained considering the powerful flight and far-ranging capabilities of these birds. S.A. Ali, S. & Ripley, S.D. 1968-1974. Handbook of the Birds of India and Pakistan. Bombay. Boonsong, L. & Cronin, E.W. 1974 (revised edn.). Bird Guide of Thailand. Bangkok. Bruce, M.D. 1980. A Field List of the Birds of the Philippines. Sydney. Cheng, Tso-Hsin. 1973. A Distribution List of Chinese Birds. Peiping. Delacour, J. & Iabouille, P. 1931. Les Oiseaux de l'Indochine Francaise. Paris. DuPont, J.E. 1971. Philippine Birds. Greenville. Fleming, R.L., Fleming, R.L. Jr & Bangdel, L.S. 1979 (revised edn.). Birds of Nepal: with Reference to Kashmir and Sikkim. Kathmandu. Henry, G.M. 1979 (revised edn.). Guide to the Birds of Ceylon. Bombay. King, B.F., Woodcock, M. & Dickinson, E.C. 1975. Field Guide to the Birds of South-East Asia, covering Burma, Malaya, Thailand, Cambodia, Vietnam, Laos and Hong Kong. London. Medway, Lord & Wells, D.R. 1976. The Birds of the Malay Peninsula, vol. 5. London. Smythies, B.E. 1953 (2nd edn.), The Birds of Burma. Edinburgh. Smythies, B.E. 1981 (3rd edn.). The Birds of Borneo. Kuala Lumpur. Stresemann, E. 1939. Die Vogel von Celebes. Zoogeographie. J. Orn. 87: 312-425. Woodcock, M.W. 1980. Collins Handguide to the Birds of the Indian Subcontinent. London.

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ORIENTATION: see NAVIGATION. ORIGIN OF BIRDS: see EARLY EVOLUTION

OF BIRDS.

oRI 0 LE

(1): substantive name of most species of Oriolidae (Passeriformes, suborder Oscines); in the plural, and in an Old World context, general term for the family Oriolidae. This is a homogeneous group of about 28 species placed in 2 genera, 24 species in Oriolus and the remainder in Sphecotheres. Tentatively classified with the orioles is the little known Kinkimavo Tylas eduardi of Madagascar, and it has recently been suggested that the 2 FAIRY-BLUEBIRDS, Irena cyanogaster and I. puella of the Oriental region may be aberrant orioles. The family name is from the Old French oriol, which in turn was probably derived from the Latin aureolus, meaning golden or yellow, and applied originally to the Golden Oriole Oriolus oriolus. Characteristics. The orioles differ from the New World orioles (Icteridae) by having 10 primary feathers (see ORIOLE (2)). Old World orioles are robust birds ranging in size from about 20-30 ern in length, and have decurved bills. The wings are long and pointed; the tail has 12 feathers. Habitat, distribution and movements. The family Oriolidae occurs in forests and woodlands throughout Africa south of the Sahara, across Asia, the Philippines, Malaysia to New Guinea and Australia (though not in New Zealand) with one species, the well-known Golden Oriole O. oriolus ranging right across the southern Palearctic region as well as into India, but wintering exclusively south of the Sahara. Other non-forest inhabiting species are to some extent migratory. Speciation has been most active in the eastern quarter of the family's range, where there are so many islands. Most species of Oriolidae occur in the tropics or sub-tropics. Distribution and characteristics. The Golden Oriole, 5 closely related African species, and some of the Oriental species have the male plumage patterned brilliant yellow and black, with black usually on the head, primary and secondary wing feathers and on the upper tail coverts. One species, O. chlorocephalus, limited to a few montane forests in eastern Africa, has the combination of clear yellow and rich olive-green. The 2 Australian species are much duller, greenish and streaky. Several Oriental species are predominantly black, with patches of rich crimson; e.g. the Maroon Oriole O. traillii; while the Black Oriole O. hosii is almost wholly black except for chestnut under tail coverts. As a rule, those orioles that have yellow pigment in the plumage have bills coloured a dull red or pink, while those with crimson in the plumage have the bills horn-coloured or bluish. The 4 species of figbird placed in the genus Sphecotheres occur in the forests and open woodlands of the Timor-New

Black-naped Oriole Oriolus chinensis. (D.A.T.).

412

Oriole

Guinea-Australia area. They are distinguished by bare skin around the eye and an exceptionally short bill. Figbirds are duller in plumage than other orioles, and have dull yellow, green, brown, grey and white in their plumages. Bills are black and legs are red in males; females have both bills and legs reddish-brown. In at least one species, S. vieilloti, the red colour of the bare skin of the adult male apparently fades after the eggs have hatched. Throughout the family the females are, with very few exceptions, duller or more streaked-or both-than the males. Juveniles resemble females. The orioles provide some typical examples of evolution on small islands. O. crassirostris of Sao Tome in the Gulf of Guinea has lost most of the brilliant yellow so prominent in the African species from which it was probably derived, and it has an abnormally short and rounded wing. In the Moluccas, O. bouroensis and its relatives have lost both black and lipochrome to such an extent that they have become dull brownish birds (see MIMICRY). Food. All the species are exclusively arboreal, feeding on insects and fruit. In the Sphecotheres spp., commonly known as figbirds, fruit is the major component of the diet. The African Blackheaded Oriole O. larvatus also takes nectar by probing into flowers. Voice. Certain features of the voice are widespread in the family, namely the sweet, fluting and liquid songs and calls, and also a harsh growling or bleating note. The figbirds have a chattering call and appear to be more noisy than Oriolus spp., particularly when feeding. Breeding. The typical nest of Oriolus spp. is a deep cup, closely woven of beard lichens or grass, and slung in a horizontal fork on a lateral branch high above ground. Nests of Sphecotheres spp. are not woven and are small untidy cups placed in horizontal forks in foliage and may be up to 20 m above ground. The eggs of Oriolus spp. have rich dark blotches or spots on a white, buff or pink ground. Eggs of the figbirds are greenish, from a pale apple-green to a dull olive-green, with dark markings. The nests and eggs of several species of Oriolidae remain to be described. In the European Golden Oriole care of the eggs and young is shared by both adults of the pair (incubation and fledging periods each c. 14-15 days), but very few detailed studies of any of the other species have been made. (R.E.M.) W.R.J.D. Greenway, J.C. Jr 1962. Family Oriolidae. In Mayr, E. & Greenway, J.C. Jr (eds.). Checklist of Birds of the World, vol. 15. Cambridge, Mass.

ORIOLE (2): substantive name of Icterus spp.; in the plural form 'American orioles', general term for the family Icteridae (Passeriformes, suborder Oscines). This strictly New World assemblage of 9-primaried song birds is derived from emberizine stock and forms a remarkably heterogeneous family of medium-sized birds that includes such diverse natural groups as the oropendolas, caciques, grackles, American blackbirds, American orioles or troupials, cowbirds and meadowlarks. Characteristics. The approximately 90 species in this family range in size from IS-53 em in length. All have unnotched conical bills that are usually pointed and not longer than the head; rictal bristles are lacking or obsolescent. In some of the larger species, especially oropendolas and caciques, the culmen is expanded or swollen basally, especially among males, to form a conspicuous frontal shield or casque. The predominant body colour in the family is black, but some species lack black entirely, and in most the basic colour is conspicuously patterned with red, orange, yellow or brown. Iridescent gloss is characteristic of the black of many species. Many species, particularly those with non-monogamous mating systems, are strongly sexually dimorphic in size and behaviour. Plumage dimorphism is also common, especially at high latitudes, but most of the tropical forest species are monochromatic. In many species with pronounced sexual dichromatism there is a first-year male plumage, typically intermediate between that of the female and the adult male, which may be highly variable. Streaked plumage is present in both sexes of grassland species such as meadowlarks (Stumella, Leistes) and among females of many marsh (some Agelaius) and wet grassland (Bobolink Dolichonyx oryzivorus) species. In most species the non-breeding plumage is identical with the breeding plumage, but males of some black species acquire brown tips to their feathers during the post-breeding moult, the full black plumage being acquired gradually through wearing of the feather tips. The male Bobolink undergoes a striking change of plumage during the winter, acquiring the drab, streaked plumage of the female. Distribution. American orioles are best represented in the lowland tropics, but there are common species at temperate latitudes and in tropical montane habitats. One species, the Rusty Blackbird Euphagus

Yellow-headed Blackbird Xanthocephalus xanthocephalus. CD.A. T.).

carolinus, breeds north of the Arctic Circle, while the Austral Blackbird Curaeus curaeus breeds to the southern limits of land in Tierra del Fuego. Icterids are found in virtually every type of vegetation in the New World except tundra. The largest number of species is found in tropical forests, especially disturbed areas, but these birds are among the dominant species in savannas, grasslands and marshes. In the western Amazon basin, up to 12 species can be found in a single habitat. Populations. Because many icterids are found in disturbed habitats, they have often benefited from human-induced environmental changes. Many species have readily adapted to croplands and grazed pastures. The Red-winged Blackbird Agelaius phoeniceus is one of the most abundant breeding birds in North America. The Brown-headed Cowbird Molothrus ater has undergone enormous expansion in both range and population size in North America during the past half century. Its southern counterpart, the Shiny Cowbird M. bonariensis, is also rapidly expanding its range northward through the West Indies. Some species, such as Red-winged Blackbirds, cowbirds and grackles Quiscalus, have become crop pests. None of the species, except for a few on the West Indian islands, appear to be declining in abundance or in danger of extinction. Movements. Most tropical species of icterids are sedentary or undergo only limited seasonal movements in response to changing patterns in availability of fruit and insects or vegetation disturbance. There is one interhemispheric migrant, the Bobolink, which breeds in southern Canada and northern United States and winters primarily in the pampas of Argentina. Most of the North Temperate breeding species migrate south for the winter, but few penetrate farther than Central America, and many winter as far north as snow-free ground is usually available. In South America, where there is so little temperate land mass and climates are maritime, there is relatively little northward movement for the winter. Some species, such as the Yellow-headed Blackbird Xanthocephalus xanthocephalus, which depend on large populations of emerging aquatic insects for breeding, change breeding locations substantially between years, whereas others are highly sedentary and show great local variations in plumage and voice. Food. The key to the evolution of the icterids lies in their ability to open their bills forceably against considerable pressure. Most species in the family use such gaping movements extensively during feeding and this behaviour reveals food not available to species that must find it on the surface. Gaping is used to extract food from epiphytes on trees, especially bromeliads (oropendolas, caciques, orioles and the endemic Jamaican blackbird Nesopsari, flowers (many genera), dead branches and crevices in bark (caciques), the bases of clumps of grasses (meadowlarks), pine

needles (orioles), the ground (meadowlarks), under rocks and cowpats (many blackbirds, cowbirds) and fruit (orioles, caciques and oropendolas). Some, such as grackles, also have powerful muscles for closing the bill and are able to crush large seeds. The nestlings of most species are fed primarily on arthropods, but many species are partially frugivorous (tropical species) or granivorous (most temperate species) during the non-breeding season. Many icterids are highly adapted for foraging on the ground and progress by walking. Marsh-nesting species are able to

Ornamentation, birds in human

forage efficiently in the dense vertical growth of those habitats, often by straddling between stems with their legs extending laterally from their bodies. Many are adept at holding prey in their feet while subduing and dissecting it with the bill. Ground-foraging species are also able to expose hidden food by scratching, usually using both feet in a rapid backward movement, one foot being moved slightly after the other. A common pattern of movement employed by flocking species feeding in open grassland and cropland is one in which birds at the rear of the flock fly over their flockmates to the front and feed in a fixed spot until they are at the rear, when they repeat the movement again. When viewed from a distance such a flock appears to 'roll' across the field. Behaviour. Diversity of social organization is one of the most notable characteristics of the American orioles. Some species are monogamous and defend large, exclusive territories during the breeding season (meadowlarks, Dives, most orioles, some caciques), others are monogamous but colonial (Quiscalus, Euphagus, Curaeus), some are territorial but polygynous (some Agelaius, Xanthocephalus, Dolichonyx), some are colonial and polygynous (oropendolas, some caciques, some grackles, especially Cassidix). An unusual form of breeding is found in the cowbirds, most of which do not build their own nests but lay their eggs in the nests of other species. Only the Bay-winged Cowbird Molothrus badius of temperate South America incubates its own eggs and feeds its own young. Some of the cowbirds are highly host-specific, usually within the family Icteridae. For example the Screaming Cowbird M. rufoaxillaris apparently parasitizes only the Bay-winged Cowbird, while the Giant Cowbird Scaphidura oryzivora parasitizes only oropendolas and caciques. Even the more catholic species, such as Brown-headed and Shiny Cowbirds, heavily parasitize other members of the family. Occasional bigamous matings have been reported in normally monogamous species, presumably the result of local imbalances in sex ratios, but the welldeveloped non-monogamous mating systems are not due to sex ratio imbalances. Sex ratios of nestlings at the time of fledging are close to 1: 1 in those few species that have been studied intensively. There are substantial populations of non-breeding males, usually younger birds, in the polygynous species. These non-breeders may obtain territories when numbers of older birds are low, and can be induced to take over territories by the removal of established adults. Voice. Icterids produce a wide variety of notes ranging from harsh and guttural to very musical. In general the monogamous, territorial species are excellent songsters and some species, such as the Melodious Blackbird Dives dives, the Shiny Cowbird and the Chopi Blackbird Gnorimopsar chopi, are highly prized as cage birds in Latin America. Among tropical species that remain permanently paired on territories, it is common for both sexes to sing, probably because individuals of both sexes must seek replacement mates with approximately equal frequency. In a few species, most notably the Melodious Blackbird, this has been developed into a complex and precisely timed duetting in which each member of the pair sings a different part of the complex song. Song is restricted to males in most migratory monogamous species. Among monogamous species song rates drop strikingly as soon as pairing takes place, but song rates of polygynous males remain high through much of the breeding season. Males of many species sing regularly in autumn and winter flocks, often in loud choruses, but the function of that singing is obscure. In general, species with colonial breeding systems have more vocalizations than territorial species and, among polygynous species, males have many more vocalizations than females. In some polygynous species, females defend space within the territories of the males and may use specific vocalizations and displays to exclude other females. Breeding. The nests of icterids are among the most varied of any avian family. Terrestrial species build well-concealed but simple (Bobolink) or domed (meadowlarks) nests on the ground. The marsh-breeding species build most of their nests in the emergent aquatic vegetation while savanna and scrubland nesting species build their nests in bushes and trees. Orioles suspend their woven, sack-like nests from the tips of the branches of trees where they are inaccessible to most mammalian and reptilian predators. The colonial oropendolas and caciques nest in large, usually isolated trees, and build their remarkable hanging nests, that may measure up to 11/ 2 m in length, in large groups. In most species, nests are built entirely by the females, who also perform incubation unaided by their mates for 11-14 days. Clutches of 2-3 are characteristic of tropical species while 4-6 eggs are usual for the higher latitude species. Nestling periods range from about 10 days in the smallest to about 5 weeks in the largest species. In the monogamous species both sexes share in the

413

feeding of the young, but in some polygynous ones only the female brings food. In these species the males continue to defend territories and attempt to attract additional females. The evolution of these differences appears to be related to the value to the males of differing patterns of investments. In the Yellow-headed Blackbird, for example, where breeding is highly synchronous, most males do feed nestlings, preferentially at the first nest to hatch on their territories. In the Red-winged Blackbird, however, where new females are attracted over a much longer period of time, most males do not feed nestlings, but many feed fledglings later in the season when the probability of attracting additional females is low. Many species are single-brooded, but double broods are raised by at least part of the population in a few species. In most species, renesting occurs if the first nest is destroyed. Helpers at the nest are known in several species (Bay-winged Cowbird, Austral Blackbird, Brown-and-yellow Marshbird Pseudoleistes virescens), but the genetic relationships between nest owners and helpers are unknown. However, helping does occur in species that do not remain as family units on territories during the non-breeding season. (E.R.B.) G.H.O. Beecher, W.J. 1951. Adaptations for food-gettingin the American Blackbirds. Auk 68: 411-440.

Bent, A.C. 1958. Life Histories of North American Blackbirds, Orioles, Tanagers and Allies. Bull. US Nat. Mus. 211. Friedmann, H., Kiff, L.L. & Rothstein, S.1. 1977. A further contribution to knowledge of the host relations of the parasitic cowbirds. Smithson. Contr. Zoo!' 235.

Hellmayr, C.E. 1937. Catalogue of Birdsof the Americas and the Adjacent Islands. Fieldiana 13: part 10, Icteridae. Orians, G.H. 1980. Some Adaptations of Marsh-nesting Blackbirds. Monographs in Population Biology 14. Princeton. Selander, R.K. & Giller, D.R. 1961. Analysis of sympatry of Great-tailed and Boat-tailed Grackles. Condor 63: 29-86.

ORIOLIDAE: a family of the

PASSERIFORMES,

suborder Oscines;

ORIOLE (1).

ORNAMENTATION, BIRDS IN HUMAN: Gilbert's lines in The Gondoliers, 'I wonder whether she'd wear a feather-I rather think she

should!' reflected the fashion of the age. They appeared in 1889, the very year that saw the foundation of the [Royal] Society for the Protection of Birds to combat the plumage trade. Appalling numbers of egret (e.g. Egretta) plumes (commercially misnamed 'ospreys'), as well as hummingbird (Trochilidae) and bird-of-paradise (Paradisaeidae) corpses, were being imported for the ornamentation of fashionable ladies, and it was not until the 1920s that legislation and the vagaries of La mode put a virtual end to the slaughter. Today in Britain some men's hats are still sold with a small gamebird feather in the band, but about 1950 hatters ceased to stock the sprays or 'mounts' of feathers that could be transferred from one hat to another. In the western world the wearing of feathers is nowadays restricted mainly to those who fulfil certain conditions. Ostrich Struthio camelus feathers adorn some official cocked hats, the bonnets of bagpipers, and until recently the coiffures of debutantes. Raptor plumes are thought proper to the bonnets of certain Highland chiefs, and the Black Watch wear the Red Hackle of feathers dyed to match the blood spilt by the regiment at Fontenoy. Here the aesthetic appeal of the feather is complemented by its function as a signal of rank, privilege, or group membership. The same is true in much of the 'primitive' world. To peoples without chemical dyes feathers offer a source of bright colour equalled only by flowers, and much less fragile; but some birds too have qualities that a man would wish to share, such as keen sight or skill in taking prey, and which he may acquire by donning their plumage. Dissociation of the purely decorative from the symbolic or the sacred in this field is difficult and will not be attempted here. For whatever motive, Man's use of feathers goes far back into prehistory and is, on varying levels of frequency, world-wide, attaining its most noteworthy development in the Americas and Oceania. In North America eagle feathers were highly valued, especially the white, dark-tipped tails of the immature Golden Eagle Aquila chrysaetos. A few tribes kept caged eagles, but among some Plains Indians the birds were hand-caught by men concealed under carrion-baited screens of foliage and released minus tail. The feathers were hung from weapons, pipes and bridles, and especially worn in the hair of warriors to indicate, by a precise code of notches, painting and angle, the wearer's deeds. Originally only Plains men of outstanding valour might aspire to the now familiar eagle-plume 'war bonnet', which in its earlier forms was much

414

Ornamentation, birds in human

less stylized both in shape and in the feathers employed. Various species contributed to the simpler crowns and circlets worn in the eastern and southern Woodlands, where the Wild Turkey Meleagris gallopauo was favoured. Among other uses, turkey feathers were tied into fibre netting to produce mantles both warm and decorative. Nineteenth century traders found an avid market for turkey feathers among the Upper Missouri tribes, outside the bird's normal range. The sedentary Pueblo Indians of Arizona and New Mexico used feathers mainly as altar decorations and aspergilla, and for pahos, the wooden pegs with a single pendant downy feather embodying a prayer and used somewhat in the manner of votive candles. Certain Pueblo ceremonies, however, called for topknots of scarlet parrot feathers, obtained from live birds traded north from Mexico. The most imaginative North American featherwork developed in California, in the form of ceremonial kilts and elaborate head-dresses of brilliant passerine feathers, sometimes dominated by long black plumes from the Condor Gymnogyps californianus. The Porno made exquisite coiled baskets studded with crests of quail (Lophortyx sp.), scalps of woodpeckers and flickers (Picidae), and hummingbird feathers. Red feathers from the Pileated Woodpecker Dryocopus pileatus served both for ornamentation and as currency. Birds were important to the Indians of the North Pacific Coast but their heraldic carvings of eagle, raven and hawk belong most properly to art. Feathers were little used here, but at the numerous formal feasts the bark head-rings of the participants must be filled with loose white down; and puffin beaks (Fratercula corniculata or F. cirrhata) were strung together for rattles and fringes. In the Subarctic (especially) bird quills were split and dyed for use in the ornamentation of moccasins and equipment, as a supplement to the more usual porcupine-quill embroidery. The Eskimo combined utility with decorative effect by piecing together the feathered skins of sea ducks and divers (Anatidae, Gaviidae) into garments, or turned them singly into pouches (as did the Swedish Lapps). Native American featherwork reached its apogee in classical Mexico, the land of the Feathered Serpent. Little has survived, but one or two brilliant examples of feather mosaic may still be seen in museums, and precolumbian codices and sculpture show both Maya and Aztec nobles wearing stupendous headgear based on the plumage of the Quetzal Pharomachrus mocinno and theXiuht6totl (Cotinga sp.). The sacred quetzal plumes bulked large in the tribute exacted from subject tribes. The textile-orientated civilizations of the Andes made no great use of feathers, although the reigning Inca wore above his brow, in life and in death, a pair of sacred plumes taken possibly from a fork-tailed nighthawk, Uropsalis lyra or U. segmentata. It is in the forest areas of tropical South America that naked or near-naked peoples wed fine craftsmanship to controlled aesthetic sense to produce a variety of resplendent chaplets and diadems. Important among the many species exploited are the toucans (Ramphastidae), parrots and macaws (Psittacidae), curassows (Cracidae), and the Harpy Eagle Harpia harpyja. Feathers are also worn on arms, legs and necks, and thrust through perforated ears, lips, cheeks and the nasal septum. In coastal Brazil the Scarlet Ibis Eudocimus ruber was semidomesticated to supply feather mantles. Sixteenth century travellers in the same region saw prospective victims of cannibal rituals whose skin was coated with crushed blue eggshell; the same cosmetic is worn today by girls in the Xingu tribal refuge, without culinary connotations. More widespread is the adornment of the body, overall or in patterns, with down or chopped feathers glued on with resin or latex. Amazonia is the home of a process, known to ethnologists as tapirage, for altering the pigment of living birds. Typically, green parrots are partially plucked and the bared skin rubbed with the venomous secretions of the Giant Toad Bufo marinus or frogs, Dendrobates spp., sometimes mixed with a vegetable dye (usually Bixa orellana). The next growth of feathers is yellow or red. The biochemistry of the method is unclear, and made more so by the variety of unguents used in marginal areas, including fish fat, or dye alone, but its effectiveness is unquestionable. Feather ornaments of more sober hue were worn south of the tropics, right to the tip of Tierra del Fuego, where a scrap of birdskin served as a pubic covering for Yahgan women. Here too bird-bone beads were worn. On the pampa feathers of rheas, Rhea americana and Pterocnemia pennata, and of herons (Ardeidae) took precedence. Tribal Africa is in general much less feather-conscious than America. Predictably the Ostrich holds pride of place, its plumes decking heads and shields in East and South Africa, most strikingly in the great face-encircling feather 'manes' of such warrior tribes as the Masai and Emberre (who mixed

them with those of the guinea-fowl Acryllium vulturinum), and surviving most extravagantly in the attire ofmodern Kaffir rickshaw boys. Ceremonial feather fans from the West African emirates recall those of dynastic Egypt. The wearing of ostrich feathers may indeed have been continuous from the ancient world to the modern, radiating from the Mediterranean and supplied until recently from birds in the North African-Middle Eastern range. About 1870 the European vogue for feathers led to the large-scale farming of ostriches in South Africa, soon carried over into Australia and the USA; early in this century ostrich feathers ranked fourth in value among South African exports. Despite vicissitudes, ostrich farming continues, reinforced by a steady demand for skins, which are converted into fine leather goods. Beads of ostrich-egg shell, ground into button-like discs, are worn up and down Africa, and appear in Libyan graves dated at 700 Be. The Peacock Pavo cristatus and other phasianids are high on the list of species whose plumage is used for dress accessories and the like in the Orient. Flexible peacock feather shafts, stripped of the rami, are stitched into Indian embroideries; forewings of eagles (Haliaeetus leucocephalus and Aquila clanga) make fans in Manchuria-as in North America (A. chrysaetos); and cheap metal jewellery set with bright feathers is popular in China. The Naga tribesmen in Assam greatly value rectrices of the Racket-tailed Drongo Dicrurus paradiseus, and it is here that we first meet a preoccupation with the hornbills (Bucerotidae) which recurs at intervals to the limits of Indonesia. The bold black and white tail feathers are worn in the hair and on the war-coats of Dayak headhunters in Borneo, and the solid casque of the Helmeted Hornbill Rhinoplax vigil is carved into ornaments which include ear-plugs denoting the taking of a head. Wooden representations of hornbills, variously conventionalized, are important in Bornean ceremonial life. (See also HORNBILL). A more significant focus on bird exploitation is found in New Guinea, where both men and women delight in disguising themselves behind startling face-paint, pig tusks and shells, topped by enormous structures built up of hair, fur, leaves and feathers-of eagle (Harpyopsis novaeguineae) , parrots and lorikeets (Psittacidae), cassowary Casuarius bennetti, and above all birds-of-paradise. Cassowary plumes are thrust into pierced nostrils as well as through the septum, and cassowary-bone spatulae through the ears. Live cassowaries are kept for their plumage, and change hands as bride-wealth. Across the Torres Strait the northern Aborigines make some use of the Australian species, C. casuarius, along with Emus Dromaius novaehollandiae and smaller species, but featherwork is not prominent. Bird down is worn at corroborees, affixed sometimes with the wearer's blood. Patriotic plumes for regimental slouch hats seem to be the emu's one tiny contribution to white Australian adornment. In the western Pacific featherwork, tasteful generally, achieved a brilliant climax on Hawaii. Its most characteristic manifestation everywhere is the feather cloak. The New Zealand Maoris make them of Kiwi Apteryx australis feathers tied into a groundwork of native flax, and may trim them with those of the New Zealand Pigeon H emiphaga novaeseelandiae, Kea Nestor notabilis, and others. Chiefs used to supplement the cloak with one or two tail feathers of the extinct Huia Heteralocha acutirostris in the hair. The most precious sources of feathers in Polynesia however were the honeyeaters (Meliphagidae) and Hawaiian honeycreepers (Drepanididae). On Santa Cruz Island fibre belts over 6 m long, covered with the scarlet body feathers of the Cardinal Honeyeater Myzomela cardinalis, were currency. On the Hawaiian group half a dozen species contributed splendour to the high-born in the form of leis, plumed staves, helmets and, most notably, robes. Leis were feather garlands more durable than those of flowers which are draped over modern tourists. The official staves, kahili, were emblems of authority. The helmets, mahiole, were astonishingly like Graeco-Roman models in outline, with high, broad keels, but made of wicker and entirely covered with tiny feathers set almost as closely as on the bird itself. So too were the robes, ahuula, varying in size from shoulder capes to full-length cloaks. The basic colour was normally yellow, counterpointed by triangles or lozenges of red or black. The yellow came from the small axillary tufts of the mainly black 0-0 Moho nobilis, red from the Iiwi Vestiaria coccinea and Apapane H imatione sanguinea, and black and orange from the Mamo Drepanis pacifica; some other species were utilized to a lesser extent. To make a robe, tufts of up to 20 tiny feathers were tied in so thickly and evenly that the foundation of Touchardia fibre is quite invisible. A full-sized robe may have some 100,000 such tufts. Examples of this work survive to dazzle the eye and the imagination,

Ornithology

but no more can be made; 0-0 and Mamo, like the New Zealand Huia, have gone, killed off not by feather-hunters (the rarer birds were released to grow new feathers) but by the destruction of habitats. Elsewhere however conscience has prevailed over commerce in time to save the egrets and birds-of-paradise, and the taking of eagles for latterday Indian festival gear in the USA is forbidden by laws which the Indians brand as discriminatory. This article is based mainly on a long acquaintance with museum collections. The subject is touched on in innumerable ethnographies but the 4 books listed below are particularly relevant. The present tense used herein may soon, or already, be rendered inappropriate in some contexts by the advance of Progress and denim; feather ornaments are worn often in inverse ratio to the amount of other covering, in the jungle just as in the cabaret. G.E.S.T. Bisilliat, M., with Vilas-Boas, O. & C. 1979. Xingu. London. Bingham, W. T. 1899. Hawaiian Feather Work. Honolulu. Steward, I.H. (ed.). 1946--50. Handbook of South American Indians, vols. 1-6. Washington, D.C. Strathern, A. & M. 1971. Self-decoration in Mount Hagen. London.

ORNIS: Greek word (plural 'ornithes') for bird, used scientifically (in the singular)-but seldom nowadays-in the sense of AVIFAUNA. ORNITHIC.: pertaining to birds. ORNITHICHNITE: geological term for a bird's footprint preserved in stone. ORNITHOGAEA: name for a zoogeographical region (not one of the classical divisions) considered to include New Zealand and Polynesia. Reasons are given elsewhere for treating New Zealand as a subregion of the Australasian Region, and for excluding oceanic islands from any such scheme (see AUSTRALASIAN REGION; DISTRIBUTION, GEOGRAPHICAL). ORNITHOLITE: geological term for the fossilized remains of a bird (see FOSSIL BIRDS). ORNITHOLOGICAL SOCIETIES: organized groups of ornithologists with a collective interest in watching, studying or enjoying birds; or in their protection and conservation (see BIRD-WATCHING; CONSERVATION; ORNITHOLOGY).

Probably more than in any other branch of zoology, progress in ornithology depends on wide participation. Trained scientists in universities, museums and similar foundations and research institutes play their part, especially in more complex fields such as physiology or behaviour, but many studies of distribution, biology, ecology and migration are founded on this general enthusiasm for collective participation by amateurs, pursuing ornithology as a hobby. Typifying the potential scientific achievement of such collaborative effort is the Atlas of Breeding Birds in Britain and Ireland, published in 1976 (see ATLAS). The project to map the breeding season distribution, based on survey visits to the 10km squares of the British National Grid, was initiated by the British Trust for Ornithology (BTO) and Irish Wildbird Conservancy (IWC) and ran for the 5 years 1968-1972. It has been estimated that up to 15,000 observers took part, contributing immeasurable hours of field-work to visit everyone of 3,862 squares, resulting in an invaluable Atlas of a precision unthinkable by any other approach. The senior ornithological body in Britain is the British Ornithologists' Union founded in 1858, a learned society publishing the journal Ibis and devoting some of its subscription income to supporting ornithological expeditions, research and publications in Britain and overseas. Concerned with the practicalities of the study of all types of birds is the BTO (founded 1933; journals Bird Study, BTO News, Ringing and Migration), whose members are able to participate actively in a wide and ever-changing spectrum of censuses, surveys, biological studies and bird ringing. The extensive data collected from these co-operative ventures is analyzed either by an amateur enthusiast or by the Trust's professional headquarters staff. The Wildfowl Trust (journal Wildfowl), founded by Sir Peter Scott, has a network of reserves directed at waterfowl conservation but is better known internationally as a centre of waterfowl research, ranging from population estimation, movements and ecology to the captive breeding of the Ne-ne Branta sandvicensis.

415

In Scotland the Scottish Ornithologists' Club (SOC) with its journal Scottish Birds, and in Ireland the Irish Wild bird Conservancy (journal Irish Birds) fulfil national roles, often co-operating with the BTO and the Royal Society for the Protection of Birds (RSPB; magazine Birds) in research covering all Britain and Ireland. There is as well a remarkable regional and local network of societies. In 1982, excluding branches of the RSPB, there were 170 organizations devoted to birds against only 46 catering for all other aspects of zoology. Most counties have their own society, providing meetings and excursions to inform and interest their members and maintaining records of the status of the county avifauna. Most countries in northern Europe have an infrastructure of regional and local societies and clubs broadly similar to, but rarely so extensive as the network in Britain. There are 3 major scientific ornithological societies in North America: American Ornithologists' Union (journal Auk), Wilson Ornithological Society (journal Wilson Bulletin), and Cooper Ornithological Society (journal Condor). The National Audubon Society provides leadership in conversation issues. There are also many state and province societies. In Australia, the Royal Australasian Ornithologists' Union publishes Emu. In Europe, most countries now have a national society (for example, Societe Ornithologique de France, journal L'Oiseau; Nederlandsche Ornithologische Vereenigung, journal Ardea; Deutsche Ornithologen Gesellschaft, Journal fur Ornithologie). The oldest society in Asia, the Bombay Natural History Society, celebrated its centenary in 1983. (The journal British Birds, published monthly since 1907, is an exception in not being the organ of a particular society or institute.) These periodical journals are the prime means of disseminating ornithological information and it is generally within their pages that additions to our knowledge of birds are published. Relatively little is found in more general journals connected with animal ecology, physiology or behaviour, a situation distinct from most other disciplines save perhaps entomology. Many of the specialist journals are now regularly abstracted by the various international biological data retrieval systems, and an annual guide to the past contents of the majority can be found in the Zoological Record published by the Zoological Society of London. Of the 36 most-cited journals devoted to birds, 13 are specifically named after birds. J.J.M.F.

ORNITHOLOGY: the scientific study of birds; that branch of Zoology concerned with the Class Aves. (See AVES; BIRD-WATCHING; CONGRESSES, INTERNATIONAL; ORNITHOLOGICAL SOCIETIES; and articles on general subjects.) Birds are fascinating objects for scientific study: their feathers, respiratory and circulatory systems are unique and extremely effective in relation to their great mobility. Flight has opened up new horizons in the form of migration, but has also imposed some strictures. The forelimb is given over to flight, so the food-gathering 'hand' has been lost, but this in turn has led to the enormous adaptive radiation shown by birds' BILLS. Research on birds may be considered under main discipline headings, though, as in all branches of Natural Science, the boundaries between disciplines are not clearly defined: indeed one may often augment another. Systematics. Deals with the identity and relationships of birds, both of the present time and those of the fossil record, and is based largely on anatomy but with an increasing input from elsewhere e.g. protein analysis. There is a natural connection to studies of evolution. Anatomy and physiology. Birds as a Class are regarded by general zoologists as remarkably uniform compared with other animal groups. Thus the subtle distinctions between the different anatomical and physiological adaptations that fit each species or group to its way of life are particularly interesting. Ecology and distribution. Studies which relate birds to their total environment, for example in terms of food or population dynamics, come under this heading. So too does MIGRATION, an ability widely and well developed in birds, and a fertile study area where several key questions remain unanswered. Behaviour (or ethology) and vocalization. Deal with the habits, e.g. courtship and aggressive displays, of birds and their songs and calls, including their causation and biological function. Applied ornithology. Deals with the interactions between birds and men. At one extreme fall the economic aspects of bird damage to crops and its prevention, and at the other lie studies of species threatened by habitat loss or pollution at man's hand. Between lies the role of bird populations as indicators of environmental change.

416

Omithomancy

While ornithology has benefited widely from research in other branches of zoology-for example from studies of migrating fish-there are many cases where ornithological investigations have been the foundation stones of research throughout zoology. Charles Darwin's studies of the Galapagos finches (see DARWIN'S FINCHES) contributed to the formulation of his theories on the ways in which new species originate-views that were to revolutionize all subsequent biological thinking. P.L. Sclater's work on the geographical distribution of birds, propounded in 1858, opened this field of study to all zoologists, and Sclater's zoogeographical regions were largely adopted by Alfred Russel Wallace, 18 years later, for animals in general. More recently, V.C. Wynne-Edwards and David Lack have been pioneering theorists at the forefront of studies of the factors regulating animal populations. ].].M.F. ORNITHOMANCY: divination from observations of the flight of birds-the words 'augury' and 'auspice' both owe their origin to this superstitious practice, being derived from the Latin 'avis' (see OMENS, BIRD AS).

ORNITHOPHILOUS: botanical term applied to plants fertilized through the intermediacy of birds (see POLLINATORS). ORNITHOSCOPY: same as

ORNITHOSIS: term (plural 'ornithoses') applied to diseases identical with, or closely related to, psittacosis (occurring in birds not necessarily of psittacine species)-see PSITTACOSIS. OROPENDOLA: substantive name of species in the tropical genus (Psarocolius) of Icteridae (see ORIOLE (2)). ORPHANED BIRDS: see

CARE OF SICK, INJURED AND ORPHANED

BIRDS.

ORTHONYCHINAE: see

RAIL-BABBLER.

ORTOLAN: name, alternatively 'Ortolan Bunting', of Emberiza hortulana (for subfamily see BUNTING); the gastronomic application of the name is wider than its specific one. ORTSTREUE: fidelity to home area, used especially for the tendency of migrants to return to a previous breeding or wintering area. A German term that has been widely used in English publications. See DISPERSAL. OSCINES: see under

PASSERIFORMES.

OSPREY: Pandion haliaetus, in America often called 'Fish-hawk' (see Also a plumage trade misnomer for egrets (Ardeidae).

HAWK).

OSSIFICATION: see

Ostrich Struthio camelus. eK.]. W.).

ORNITHOMANCY.

AGE; SKELETON, POST-CRANIAL; SKULL.

OSSIFRAGE: archaic name for the Lammergeier Gypaetus barbatus (see VULTURE (1); also BIBLE, BIRDS OF THE). OSTRICH: the largest living bird, Struthio camelus, the only species of the Struthionidae (Struthioniformes), which are placed in the group of large flightless birds known as 'ratites'. Now confined to some of the more arid areas of Africa; 'American ostrich' is an outdated term for the RHEA.

Characteristics. Adult Ostriches stand about 2.5 m high and weigh up to 150 kg. The eyes are large, surrounded by conspicuous eyelashes, and give very acute vision. The neck is flesh-coloured and appears bare, being covered only with minute downy feathers. It and the bare thighs develop a bright red or blue colour (depending on the race) in breeding males. The feathers covering the body lack barbules, giving them a soft appearance. The adult male is jet black, with beautiful white primary plumes in the wings and tail, although the latter usually become stained dark, perhaps deliberately. The female is grey or grey-brown all over, and is slightly smaller than the male. The legs are long and powerful, ending uniquely in only two toes; they can carry the ostrich at a running speed of up to about 50 km/h.

Habitat. Ostriches inhabit a range of open habitats from desert to savanna; they do not occur in thick bush or forest. They occasionally reach densities of more than 1 per krn", but in most places they are much less abundant. Distribution. Only 4 races of Ostrich are now both recognized and still extant. The nominate race S.c. camelus, the North African ostrich, stretches along the southern side of the Sahara from Morocco to Ethiopia. The so-called Dwarf Ostrich S.c. spatzi from Mauritania was mistakenly classified on inadequate information. In the Horn of Africa lives the Somali Ostrich S.c. molybdophanes, the males of which have bright blue-grey skin on neck and thighs. There is very slight hybridizing and overlap in eastern Kenya with its southern neighbour, the Masai Ostrich S.c. massaicus, which has bright red skin during the breeding season. This race stretches south as far as the Katavi plain in south-west Tanzania. The South African Ostrich S.c. australis is found south of the Zambesi river in suitable open arid country. The Arabian Ostrich S.c. syriacus once abundant, has become extinct since 1941 (or possibly 1966). Populations elsewhere are declining in range, but are generally not unduly persecuted or threatened. At Oudtshoorn, in the Cape Province of South Africa, Ostriches have been farmed as domesticated birds since 1860, originally for the feathers only but now also for leather, meat and tourism. Hybridization with imported North African Ostriches at the end of the last century improved the quality of the feathers of the domestic stock; this mongrel variety has been released and become feral in parts of South Africa and Australia (see DOMESTICATION).

Movements. In the less arid regions of East Africa, ostriches are largely resident, the same individuals remaining in the same area throughout the year. In desert regions they are reported to migrate more, and probably cover considerable distances in search of food and water. Food. Ostriches are clearly well adapted to feeding on scarce highquality foods-they can stride effortlessly over a sparsely vegetated landscape, lowering the beak on the end of the long neck to pluck off selected food items. They are almost entirely herbivorous, choosing leaves, flowers and seeds of a wide variety of plants. There are only occasional reports of their eating insects and other animals in the wild, despite their well-deserved reputation in captivity for swallowing anything. When feeding, the food from many pecks is stored at the top of the neck and then all visibly passes as a single large bolus down the elastic neck. Behaviour. The groupings of Ostriches vary with race, place and season. They are often seen singly, often in pairs, and often in small groups of up to 5 or 6 birds. In arid regions larger aggregations may occur at particular feeding or drinking places. The small groups typically seen in East Africa are loose and temporary, as individuals join and depart from others in an apparently casual way. Their exceedingly acute eyesight, and their conspicuousness, especially of the males, clearly helps them to locate other members of their species.

Ovenbird

Within the loose groups, both or all the individuals tend to be engaged on roughly the same activity at the same time-feeding, standing alert, walking, preening, or dustbathing. Preening is a frequent activity, but apparently directed as much towards snapping at pestering flies as towards care of the feathers. Motivation and dominance relations are expressed by different body postures and wing movements. During aggressive encounters, males draw themselves up to their full extent, erect the body feathers, raise the tail, and flap their wings up and down on each side alternately. Much time is spent on threats and chases between breeding adult males, but actual fights are rare. The feet are their only, but extremely effective, weapon; an ostrich can deliver a fearsome forward kick at its opponent's chest. Threat or mild aggression towards a group member is accompanied by raising both wings and opening the beak wide. Voice. During the breeding season, male Ostriches utter a loud 3-note booming sound, which has been likened by Livingstone and others to the roar of a lion. It is used in proclaiming ownership of a territory and attracting females. Breeding. In East Africa, Ostriches breed during the dry season, but in more arid regions elsewhere, at the onset of the rains. The males' necks acquire their bright coloration, and territorial defence begins. The males boom, chase out intruding males, and court any females which come through their large territory. The courtship display is spectacular. The male draws himself up high, raises and erects his tail, and approaches the female at a trot. Suddenly he drops to a squat and rocks from side to side, his black and white wings extended and waving in the air alternately. Meanwhile his neck, even brighter red (or blue, according to subspecies) than usual, writhes from side to side. He may wave his wings as many as 70 or more times in front of the female, who is usually in the submissive or soliciting posture with head and both wings lowered and quivering. The male stands, approaches the female, raises both his wings high above his back, and mounts the squatting female. The mating itself is accompanied by further wing waving. The male prepares a number of shallow scrapes somewhere within his territory. One of these is accepted by a female (the 'major' hen) who lays the first egg in it and continues to lay there at regular 2-day intervals. Up to 5 other females (the 'minor' hens) lay in the same nest, also on alternate days. The male has usually mated with these minor females, and he leads them to the nest with a wing-lowered display like that of submissive females. The eggs are almost round, usually between 1,300 and 1,900 g in weight. The shell is about 2 mm thick, pitted with small pores, and shiny creamy white in colour. Nest destruction is frequent, caused by Egyptian Vultures Neophron percnopterus which throw stones at the eggs, and by jackals and hyaenas. After the first few days, an adult ostrich may attend the nest to protect it against both heat and nest predators. The major female lays about 10 eggs in her nest before incubation begins, and the minor hens may between them have laid between 10 to as many as 30 or more eggs there. At the start of incubation, the major hen pushes out a number of surplus eggs into an outer ring 1-2 m away where they are not incubated and are doomed. She rarely pushes out any of her own eggs, but retains them among the 20 or so which she can cover and incubate in the centre of the nest. Incubation takes about 42 days. It is done by the major female during the day and by the male at night. The minor females take no part in it. The chicks are nidifugous, and leave the nest with the adult pair soon after hatching. Over the next few weeks the brood often merges with the broods from other successful nests, resulting in large aggregations of chicks attended by only one set of adults. The chicks grow very fast and are almost full height within a year. They reach sexual maturity at 3--4 years old, and probably live for at least 40 years. See photo HEAT REGULATION. B.C.R.B. Bertram, B.C.R. 1979. Ostriches recognize their own eggs and discard others. Nature 279: 233-234. Bertram, B.C.R. 1980. Vigilance and group size in ostriches. Anim. Behav. 28: 278-286. Bertram, B.C.R. 1980. Breeding system and strategies of ostriches. Proc. XVII Int. Orne Congr.: 890-894. Hurxthal, L.M. 1979. Breeding behaviour of the Ostrich Struthio camelus massaicus Neumann in Nairobi Park. Ph.D. thesis, Nairobi University. Sauer, E.G.F. & Sauer, E.M. 1966. The behavior and ecology of the South African Ostrich. The Living Bird 5: 45-75. Smit, D.}.V.Z. 1963. Ostrich Farming in the Little Karoo. Pretoria.

OTIDES; OTIDIDAE: see under GRUIFORMES; ing 'Otidae' is patently erroneous.) OU: Psittirostra psiuacea (for family see OUTER TOE: see

BUSTARD.

417

(The spell-

HAWAIIAN HONEYCREEPER).

LEG.

OUZEL: substantive name, also spelt 'ousel', of the Ring Ouzel Turdus torquatus, but formerly applied to the Blackbird T. merula (cf. German 'Amsel')-see THRUSH. 'Water-ouzel' is a popular name in Britain for Cinclus cinclus (see DIPPER). OVARY: female gonad, in birds usually developed only on the left side (see ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM). OVENBIRD (1): substantive name of several species of Furnariidae (Passeriformes, infraorder Furnarii); in the plural, serves as a general term for the family but applies particularly to the nominate subfamily. The woodcreepers or woodhewers (Dendrocolaptidae) are often treated as a subfamily of the Furnariidae, but are here treated as a distinct family. The family is purely Neotropical and predominately South American; and it comprises about 221 species, in 58 genera, although many genera are considerably oversplit. The Furnariidae are probably more diverse than any other avian family. Most systematists recognize subfamilies and these groupings may be usefully introduced here. The Furnariinae (confined to South America), besides true ovenbirds or horneros of the genus Furnarius (which build a mud nest like an old fashioned earth oven and thus give the family its name), include a variety of divergent genera such as the miners (Geobates, Geositta), the groundcreeper (C libanornis), the earthcreepers (Upucerthia), the Tococo (Chilia), and shaketails or cinclodes (Cinclodes). Next and equally important are the Synallaxinae or spinetails, typified by the genera Synallaxis, Cranioleuca and Asthenes, which are rather less variable and tend to be characterized by peculiar tail structure and the building of relatively enormous enclosed nests, for this reason sometimes being called castle-builders. The genera of treerunners (Margarornis) and the Barbtail (Premnoplex) are often placed in a separate subfamily Margarornithinae, but are perhaps best included with Synallaxinae. The third large and diverse subfamily, the Philydorinae, includes treerunners (Pygarrhichas), treehunters (Thripadectes), Hookbill (Ancistrops), Pointed-tail (Berlepschia) , cachalotes (Pseudoseisura) , xenops or recurved-bills (Megaxenops and Xenopsi, and the foliage-gleaners (Philydor, Automolus, etc.). The Philydorinae represent the ovenbird subfamily closest to the woodcreepers (Dendrocolaptidae) and may be considered with certainty to represent a transitional group to the woodcreepers. The affinities of the Sclerurinae, genera Sclerurus (leafscrapers) and Lochmias (Streamcreeper), are uncertain. Characteristics. Most of the family consists of small brown birds which is as much as can be said by way of generalization. The largest members are about 25 em in total length, e.g. cachalotes, species of Pseudocolaptes, and the large Cinclodes. The colour of nearly all members of the Furnariinae is dull, being shades of brown sometimes tending to rufous or chestnut or with rufous parts, usually paler or even white below, and often with a striking wing bar. The miners, earthcreepers, and shaketails, which are all grey-brown or dark brown birds, perhaps paler and somewhat mottled below or with a white wing bar (Cinclodes) , reach the acme of drabness. The true Ovenbird Furnarius leucopus ('El Hornero' of the South Americans) differs in being essentially bright chestnut above and white below. The spinetails tend to be less drab and uniformly coloured, being mostly variegated on the upper parts with brown, chestnut, and almost black, and sometimes with dark streaking on the throat and breast (otherwise usually almost white). Some members even have some bright colour, e.g. the White-cheeked Spinetail Schoeniophylax phryganophila with a bright yellow chin, and Asthenesspp. with a touch of reddish chestnut on the throat. Species of Margarornis are rufous above and dark olive below, heavily marked with pear-shaped drops of light buff, somewhat resembling a woodcreeper. Similarly, the Sclerurinae are generally dark coloured and may be scalloped with white below. Many of the Philydorinae resemble woodcreepers, again, with their characteristic streaking on head and under parts, e.g. Berlepschia rikeri and Pseudocolaptes spp., while the genus Philydor has bright orange underparts.

418 Ovenbird

The wing is as variable as other features of the family, from soft, short, and rounded, to long and somewhat pointed. The tail may be normal, or rather short as in Furnarius and Geosiua, but is remarkably diverse among the spinetails. In that subfamily there is a tendency for it to be graduated or forked, long and attenuated, with the feather barbs breaking down and the webs becoming degenerate so that the naked quills project. For instance, Leptasthenura spp. have long tails with tapering rectrices, and Synallaxis spp. have graduated tails with the ends of the rectrices frayed and broken down so that the shafts project. Most remarkable of all is Des Murs' Spinetail Sylviorthorhynehus desmursii, with a tail 2 or 3 times as long as the rest of the bird, of very thin feathers with poorly developed webs. On the other hand, 'softtails'-Metopothrix and Xenerpestes-have normally developed rectrices, but with the shafts not at all strong, while the rectrices of Berlepschia are sharply tapered. Those forms which resemble dendrocolaptids (Pseudocolaptes, Syndactyle, Anabacerthia, and Philydor, Xenops, etc.) are distinguished from members of that family by not having the shafts of the rectrices stiffened. A very few species are crested, such as the Plainrunner Coryphistera alaudina and the Brown Cachalote Pseudoseisura lophotes. The bill is mostly rather short, straight and pointed, and is normally wide; but many variations occur, the bill being long and decurved in Upucerthia, short and slightly curved in Geosuta, moderate in both respects in Furnarius, long and straight in Sclerurus, laterally compressed in Xenoetistes, and short, wedge-shaped with upturned mandible in Xenops. The legs and feet are usually medium to short, but are strongly developed in terrestrial forms such as the true ovenbirds and cachalotes. Habitat, ecology and behaviour. Most genera and species inhabit thickly wooded habitats or areas with plenty of good cover, and this applies particularly to those within the tropics (where the majority of the family live); but even so there are differences in habitat and behaviour. The foliage-gleaners (Anabaeerthia, Automolus) are birds of the canopy and forest trees, where they hunt through the leaves like warblers (Sylviinae), Heliobletus contaminatus has the habits of a treecreeper (Certhiidae) or woodcreeper (Dendrocolaptidae), as have the treerunners. The leafscrapers inhabit the densest undergrowth, are great skulkers, and have the habit of rooting through leaves and tossing them in the air in their search for food. The Sharp-tailed Streamcreeper Lochmiasnematura is equally unobtrusive, and it shows such a preference for sewage effluent that the Brazilians have aptly named it 'president of filth'. More widely distributed birds such as the true ovenbirds and many spinetails are inhabitants of less densely wooded areas; the former, being largely terrestrial, prefer fairly open country yet with plenty of trees, while spinetails characteristically skulk unobtrusively in thickets or low cover even in treeless lands. In the southern part of its range, and to a limited extent in the Andean highlands as far north as Colombia, the family shows the greatest measure of adaptive radiation. In the open pampa of Argentina and the mountainous fjord areas of Chile, different genera and species have invaded every possible habitat. The miners and earth creepers are entirely terrestrial and typical both of barren mountainous country and of the flat pampa. The Patagonian Earthcreeper U'pucerthia dumetaria is even unwilling to fly, preferring to escape by running. The Brown Cachalote is also largely terrestrial and tends to run off behind trees and other obstacles rather than fly when disturbed. Species of Cinelodes occupy the niche of dippers (Cinclidae) and are always found near water, from mountain torrents in the high Andes down to sea level; they are even known to feed off-shore on the floating masses of giant kelp. The White-throated Treerunner Pygarrhichas albogularis of Chile and Argentina fills the niche of a nuthatch (Sittidae). The Black-faced Spinetail is a bird of the marshes, as is the Curved-billed Reedrunner Limnornis curvirostris. Aphrastura and Leptasthenura are arboreal genera. For the most part, members of the family are active yet unobtrusive birds, even in open country, keeping well to cover, constantly creeping about in bushes, reeds, or thick grass, and even running off like mice rather than flying; and they show a great tendency to remain in pairs. The Greater Thorn-bird Phacellodomus ruber in Argentina is exceptional in being not at all restless and never making an effort to hide. Distribution. The family, like the Formicariidae (see ANTBIRD), ranges from the montane and lowland forests of southern and central Mexico through Central to South America; likewise it reaches Trindad and Tobago, but is not found in the Antilles. In the south its range is greater than that of the antbirds, being over the whole of the continent to Cape Horn and Tierra del Fuego, as well as the Falkland Islands, with a

tremendous Andean radiation. Many specialized forms have developed in the open, barren lands of the extreme south, and the monospecific genus Chilia is confined to Chile, where it inhabits semi-arid country. In Argentina a few species, such as the Black-faced Shaketail Cinclodes fuseus and perhaps the Patagonian Earthcreeper, are said to be migratory. As with the antbirds, no comprehensive account of the family has ever been written, and the majority of species are known only by their appearance. Food. Most species are insectivorous, but Cinclodes spp. also take small crustacea and aquatic animals, as would be expected, while some miners and the Tococo feed on seeds and vegetable matter. Voice. Like all other characters, the voice varies considerably. Generally, the spinetails and many other genera have short, harsh, rattling and jarring calls; but miners have clear ringing reiterated cries, likened to the laughing of a child; the Ovenbird F umarius leucopus has a sequence of clear, resonant notes produced as a duet or harmonious singing; the Black-faced Spinetail Phleocryptes melanops gives wooden-sounding raps and creaks; Hudson's Spinetail Astheneshudsonihas a plaintive four-note song audible for 900 m or more; and the cachalotes are especially noisy with jay-like screams (Brown Cachalote) or a piercing chorus (Whitethroated Cachalote P. gutturalis). Breeding. The breeding habits are known mostly from species inhabiting the open lands of the southern parts of South America, but even within these limits the diversity is astonishingly great. The only constant feature is that all lay white eggs-except the Black-faced Spinetail, which lays bright blue eggs, and a few others which lay slightly bluish or off-white eggs. Clutch size is usually 3--5, but as many as 9 eggs are mentioned for the White-throated Spinetail Synallaxis albeseens, and tropical species probably tend to have smaller average clutches. Terrestrial forms such as miners and earthcreepers nest in holes in the ground, either natural cavities or tunnels dug by the birds themselves or by mammals, e.g. the Common Miner Geositta eunicularia nesting in the burrows of the Vizcacha Octomys mimax on the Argentinian pampa. Cinelodes spp. nest in rock cavities or dig their own holes. Leafscrapers and the Streamcreeper also nest in holes or burrows in banks, and the leafscrapers have an odd habit of flying out of the hole and clinging to a tree-trunk when flushed from the nest. Aphrastura and Leptasthenura nest either in holes in trees, behind bark, or in the abandoned nests of such birds as Asthenes spp. In contrast, the true ovenbirds build very substantial, domed mud-ovens on the branches of trees well above the ground. The spinetails in general build vast nests, remarkable for such small birds. The Firewood-gatherer Anumbiusannumbi(a bird about 21 ern long) makes its big structures oflarge twigs, even in tall trees to which it may have difficulty in carrying up the material. The White-throated Cachalote perhaps makes the largest nest of the family, an enclosed structure with a cavity big enough for an eagle or vulture, and strong enough for aman to stand upon without damaging it; the Brown Cachalote also makes a nest the size of a barrel. The Black-faced Spinetail makes a perfectly roofed nest, domed and impervious to the wet, with entrance near the top, out of grasses and leaves daubed together with mud and probably saliva. Species of Phaeellodomus place their castlesat the ends of branches that are at first several m from the ground, but as the structure grows the boughs bend down and the nest may eventually rest on the ground. Hudson's Spinetail makes domed nests on the ground under the thickest cover, such as the giant cardoon thistles. On the other hand, the Striped-crowned Spinetail Cranioleuea pyrrhophia and the Wren-like Spinetail Spartonoica maluroides make open cup-shaped nests, which is quite exceptional for the Synallaxinae. Owing to the impossibility of observing the nests of most species of Furnariinae and Synallaxinae without destruction or excessive disturbance (the nests of these 2 subfamilies are much better known than those of the rest of the family), breeding details are virtually unknown in spite of the fact that these huge nests are such a conspicuous feature of the countryside in the open parts of South America. The incubation and nestling periods are very superficially known, for only 6 species, being 15-20 days and 13-18 days respectively. The abandoned castles of the spinetails and the ovens of El Hornero are often used by other birds such as cowbirds (Icteridae), swallows (Hirundinidae), wrens (Troglodytidae), and parrots (Psittacidae); sometimes the owners are even expropriated after building their nest. (S.M.) A.F. Feduccia, A. 1970. Natural history of the avian families Dendrocolaptidae (woodhewers)and Furnariidae (ovenbirds). Jour. Grad. Res. Center, S.M.U. 38: 1-26.

Owl

419

Feduccia, A. 1973. Evolutionary trends in the Neotropical Ovenbirds and Woodhewers. Ornithological Monographs, No. 13. Meyer de Schauensee, R. 1970. A Guide to the Birds of South America. Wynnewood, Pa. Skutch, A.F. 1952. Life history of the Chestnut-tailed Automolus. Condor 54: 93--100. Vaurie, C. 1971. Classification of the Ovenbirds (Furnariidae). London. Vaurie, C. 1980. Taxonomy and geographical distribution of the Furnariidae (Aves, Passeriformes). Bull. Am. Mus. Nat. Hist., 166. Wetmore, A. 1972. The Birds of the Republic of Panama, 3, Smithson. Misc. Collect. 150: 56--120.

OVENBIRD (2): Seiurus aurocapillus (see WARBLER

(2)).

OVERFLOW ACTIVITY: a behaviour pattern appearing in the absence of the usual external triggering stimuli, e.g. Canaries in the appropriate physiological state will show nest building responses even in the absence of nest material. Overflow activities (also called vacuum activities) have been interpreted as evidence for spontaneous generation of behaviour patterns in the nervous system. (See BEHAVIOUR, HISTORY OF).

OVERSHOOTING: movement beyond the normal limits of a bird's area of distribution by continuance in the usual direction of migration beyond the proper destination. OVERWINTERING: see OVIDUCT: see

MIGRATION.

ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM;

LAYING.

OVIPARITY: the characteristic of laying eggs in which the embryos develop outside the maternal body; universal in birds. See also under DEVELOPMENT, EMBRYONIC; EGG; LAYING.

OVIPOSITION: see

LAYING.

OVOTESTIS: in virtually all birds only the left ovary is functional. The right ovary remains minute but if the left one is removed, or destroyed by disease, it can develop. Depending upon when this occurs the right gonad may turn into an ovary or a testis, or on occasion into a structure combining the germ cells of both sexes: an ovotestis. In such situations seminiferous tubules are visible in one part of the organ whilst the other contains growing follicles. The potentially ambisexual nature of birds is not confined to one group but is most well known in chickens. Sex changes were described by Aristotle and up to this century were often thought to be associated with the supernatural. OVULATION: see also LAYING.

ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM;

OVUM: the female germ-cell (plural 'ova')-see EMBRYONIC; GENETICS.

EGG;

DEVELOPMENT, ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM;

OWL: substantive name of all species of Strigiformes and in the plural, general term for the order. With very few exceptions owls look like nothing but owls, i.e. they are soft-plumaged, short-tailed, big-headed birds with large forward-facing eyes, surrounded by a broad facial disc. Owls probably have the most frontally situated eyes of all birds. This, together with their ability to blink with the upper eyelids, gives owls a semi-human appearance, in which lies much of their appeal to man. Owls have often been regarded as nocturnal counterparts of the diurnal birds-of-prey (Accipitriformes and Falconiformes), but most likely the Caprimulgiformes (oilbirds, potoos, nightjars and nighthawks) are the owls' nearest living relatives, which have evolved from a common, nocturnal ancestor, perhaps not more than 100 million years ago. General and systematic characteristics. Although the members of the Strigiformes may be easily distinguished from members of other orders, the familial, subfamilial and generic relationships within the order are much less certain. According to present knowledge there are about 134 species divided between 25 living genera and 2 families: the typical owls,

Barn Owl Tyto alba. (K.]. W.).

the Strigidae, and the barn owls, the Tytonidae. The barn owls differ only in minor osteological details from typical owls. Barn owls have proportionately smaller eyes and are easily recognizable by the heartshaped facial disc and the long slender legs. The family comprises 10 species: genus Tyto consisting of 8 species and genus Phodilus 2 species, one occurring in south-east Asia (Oriental Bay Owl P. badius) and the other in Africa (African Bay Owl P. prigoginei). The facial disc of the Strigidae is circular and the legs are usually rather strong and in most cases thickly feathered. This family contains about 124 species, distributed over about 23 genera, of variable size, coloration, and habits. However, owl taxonomy is currently in a state of flux, and anything approaching a final tally of species or genera must await revision now in progress. Owls are mostly birds of medium size with some species fairly large or fairly small. The largest are some eagle owls Bubo spp., reaching 73 em in length, and the smallest the Least Pygmy Owl Glaucidium minutissimum, 12-14cm long. Like many birds of prey the female is often larger than the male (see SEXUAL DIMORPHISM). Owls have dense, soft plumage which makes them look much bigger than they are and helps to keep them warm during long periods of inactivity between hunting forays. The colour of the plumage is often cryptic, which makes the bird less conspicuous when it is resting during the day. Woodland owls tend to be brown or grey in basic coloration; owls living in open habitats are typically paler and those inhabiting desert country are distinctly sandy-coloured (e.g. Hume's Desert Owl Strix butleri). In many species, markedly different colour phases occur, e.g. the most common British owl, Tawny Owl Strix aluco, is typically brown but also has a rarer grey phase (see POLYMORPHISM). Sexual colour dimorphism is usually absent but there are a few exceptions; for example, the female of the Snowy Owl Nyetea scandiaca, is barred, whereas the male is pure white. Differences between juvenile and adult plumage are normally slight, but many species tend to become paler or more whitish in old age (e.g. Short-eared Owl Asio flammeus). Most owls have relatively large, rounded wings, shorter in those species which hunt in cover and much longer in those which hunt in open country or are migratory. Owls are light in relation to their wing area (in aeronautical terms they have a low wing-loading) which explains why they can fly buoyantly and effortlessly, with relatively little wing-flapping (see FLIGHT). Owls show a number of adaptations which enable them to operate with outstanding efficiency as nocturnal predators. First of all they have well-adapted eyes to hunt their prey in poor light; in absolute darkness they cannot see. The huge eyes are shaped like tapering cylinders to provide the largest possible expanse of retina, and a notably thickened cornea acts as an additional lens (see VISION). Forward-facing eyes give a considerable degree of binocular vision, but the eyes themselves are almost immobile. The owl must turn its whole head to look sideways, but it has an exceptional ability to rotate its head; the head of the Long-eared Owl Asio otus has been reported to be capable of turning through at least

420 Owl

Tawny Owl Strix aluco. (K.]. W.).

270 The number of light-sensitive elements (mostly rods) in the retina is very high, particularly in definitely nocturnal species such as the Tawny Owl, and these species sometimes appear to be blinded by very strong sunlight. But many owls are able to hunt in daylight, and none is really helpless during the day. This is made possible by an exceptional range of aperture (pupil size) controlled by the iris. It is always difficult to prove whether an animal can perceive colour. As owls have some cones in their retina, it seems likely that they can do so when the light is good. Experiments on the crepuscular Little Owl Athene noctua have shown that it can perceive at least yellow, green and blue; red and the darkest grey were confused (see VISION). The owl's sense of hearing is no less remarkable than its exceptional sight. The inner ear of owls is very large, and the auditory region of the brain is provided with many more nerve cells than in other birds of comparable size. Aural abilities are aided by a wide outer ear tube and in some species by the presence of large conchae, which, surrounded by the feathers of the facial disc, can be erected at will. In some species a striking asymmetry in the shape and relative position of the external part of the ear, including the bones surrounding the tympanic region and the operculum, has been described. Asymmetrical ear openings are thought to help the owls to locate the source of sound with precision. In laboratory experiments Barn Owls Tyto alba have been capable of locating and striking an unseen living prey in complete darkness, using only their acute sense of hearing (see HEARING AND BALANCE). The high frequency squeals of small prey and the rustle of dry leaves contain all the information the owl needs to locate its intended prey. Assertions that the owl is visually sensitive to infra-red radiation given out by the body of a prey animal have been proved incorrect. Also in the wild many owls rely only on their remarkable auditory powers, at least in hunting rodents and shrews during the winter when these mammals often move under the snow cover. The Great Grey Owl Strix nebulosa is able to localize from the air invisible small mammals and to catch them blindly on the right spot below the snow-surface. Those owl species not having the ears so highly developed can always combine their acute visual and aural abilities, because there is never total darkness in a place where an owl is likely to hunt. The 'ear tufts' which many species possess have nothing to do with the auditory organ; they express mood and act as night-time recognition signals, and may also be an aid to camouflage by breaking up the outline of the owl's head. Softened flight feathers together with the low wing loading help an owl to move silently through the air-to hear other sounds while flying itself, and to avoid giving alarm to its prey. Fishing owls of the genera Ketupa in Asia and Scotopelia in Africa do not fly soundlessly, but, as they take underwater prey, the noisy wing beats do not seem to be of importance. The bill and claws of owls are clearly suited to their predatory way of life. The bill is hooked, usually short and not conspicuously strong, directed downwards-a modification to reduce obstruction of the already limited visual field. As in the diurnal birds-of-prey, the nostrils are placed in a soft cere at the base of the bill, which is partly hidden by the feathers 0

•

of the facial disc. The feet are always 4 toed, with the fourth toe reversible. The legs and toes are usually feathered, a protection against possible bites from prey. The fish-eating owls, Scotopelia and Ketupa, have bare legs and feet with rough spiny soles. All owls have sharp, strongly hooked, raptorial claws. Habitat. As a group of birds owls are able to occupy all kinds of habitats: tundra, deserts, grasslands, marshes, swamps, woods, luxuriant rain forests, mountains and islands, but the majority of the species live in woodlands or forest edges. Only a few species, like the Arctic Snowy Owl and the desert-living species of North America (e.g. Elf Owl M icrathene wkitneyi) prefer habitats where trees cannot grow. Some species are terrestrial and live in flat country or among rocks. Longlegged terrestrial species are known both in the Tytonidae (Common Grass Owl Tyto capensis, found in Africa and from India to Australia) and in the Strigidae (Burrowing Owl Athene cunicularia, found in North and South America). The recent decline of many owls with arboreal habits can be associated with the destruction of forest habitat. Some insular owls, e.g. Madagascar Owl Tyto soumagnei, Seychelles Owl Otus manadensis insularis, Sokoke Scops Owl Otus ireneae (living in a fairly small 'island' of inland forest on the Kenya coast), Anjuan Scops Owl Otus rutiluscapnodes and Forest Little Owl Athene blewitti, are even threatened with total extinction, because of habitat destruction now occurring. Distribution. On the whole, owls are successful birds, which have dispersed to all continents except Antarctica and several remote oceanic islands. The great majority of species occur in the tropics and subtropics. North America and the Palearctic zone of the Old World are inhabited by 33 species of owls, of which 8 species occur in both North America and Eurasia. The most common owl in the world is probably the Barn Owl which has almost world-wide distribution with at least 34 recognizable geographical forms. Barn Owls have been released in some Indian Ocean islands to control rats, and recently they have also colonized Malayan oil palm plantations. The Short-eared Owl is the other owl with a very wide range, mainly inhabiting boggy and marshy places in open country. The Marsh Owl Asio capensis is an ecological equivalent of the Short-eared Owl in Africa. The Snowy Owl is distributed throughout the Arctic tundra regions of the Northern Hemisphere. Throughout the zone of boreal coniferous forests of Europe, Asia and North America quite a number of other species are found; some of them are restricted to this zone, such as the Great Grey Owl, the Hawk Owl Surnia ulula, Tengmalm's Owl Aegolius funereus (known in North America as the Boreal Owl), the Ural Owl Strix uralensis, the Long-eared Owl, and the Pygmy Owl Glaucidium passerinum. The last two have a number of closely related forms in tropical America and Africa. The Eagle Owl Bubo bubo of Europe and Asia, ranging from the cold northern forests to the hot southern deserts, has allied species also in America (Great Horned Owl B. virginianus) and in Africa (Cape Eagle Owl B. capensis and Spotted Eagle Owl B. africanus). The Little Owl has a mainly Palearctic distribution, the Burrowing Owl from the steppe and desert regions of America being its present closest relative. The Little Owl has been introduced into Great Britain and New Zealand. The Tawny Owl and European Scops Owl Otus scops have both only Old World distribution. The Tawny Owl belongs to a widely distributed genus Strix which is absent only from Australia. Otus scops is the only European representative of the scops owls, which form a widespread group of about 33 species mostly living in the tropical regions of the world, except in Australasia where the genus is replaced by the hawk owls Ninox spp. Populations. Studies of the territorial Tawny Owl (Southern 1970) have shown that there is a limit to the owl density in a given habitat, this being determined by territorial behaviour. In England Tawny Owl pairs had a territory of about 13 ha in closed woodland and 20 ha in mixed woodland and open ground (see TERRITORY). Fluctuations in food resources did not lead to changes in the number of adult owls in the woods. Failure to breed, the laying of fewer eggs than potentially possible, failure to hatch laid eggs, and mortality of the young in autumn and winter were the main factors keeping the numbers virtually constant from one year to the next. But quite the opposite population dynamic applies to the nomadic species. For instance, the Short-eared Owl alters the size of its territory from month to month according to the abundance of its main prey, Microtus voles. If food is scarce the species becomes nomadic and seeks new breeding and hunting areas. Movements. Owls are mainly sedentary; regular migrations are known in respect of only a relatively few species. Among European owls some populations of Scops Owl migrate regularly to tropical Africa, while

Owlet-frogmouth

the northern populations of the Striated Scops Owl Otus brucei migrate to the Indus Valley and the Bombay region. Within eastern Asia the Oriental Scops Owl Otus sunia as well as the Oriental Hawk Owl Ninox scutulata migrate between temperate and tropical regions. The two most migratory species in Eurasia are some northern populations of the Long-eared and Short-eared Owls which are partially migrant also in North America. In several species (e.g. Snowy, Hawk and Great Grey Owls), nomadic winter movements or even irruptions occur more or less cyclically, triggered by fluctuations of rodent populations (see IRRUPTION).

Tengmalm's Owl Aegolius funereus has evolved a strategy of partial migration, adult males being resident and females and young being migratory. The periodical food scarcity favours the migration of females and young, and the urgency of guarding the nest-holes of good quality favours residence by the adult males. Food. It has been fairly easy to analyse in detail what owls are eating at different seasons, because the smaller prey are generally swallowed whole, indigestible matter such as fur, feathers, bone, and chitin being regurgitated some hours later in the form of large PELLETS. Owls feed exclusively on animals. Small mammals like rodents and shrews predominate as food items for the majority of owls. Some species feed on birds, reptiles, amphibians, fish, crabs, earthworms and insects. Hunting methods vary according to the prey. A few species hunt actively on the wing, taking moths and other small creatures in flight. Semiaquatic fish-eating owls catch fish in their talons from the surface of rivers, or hunt crabs on shores and river shallows. But most owl species quarter the ground in silent flight, or scan it from a convenient perch, waiting and intently listening for ground-living insects and small mammals. Food is mainly consumed in the fresh-caught state; carrion is only occasionally eaten. Behaviour. Most owls seem to be highly territorial, but some nomadic species, such as the Great Grey Owl and the Short-eared Owl, sometimes form loose colonies. Highly territorial owls (e.g. Eagle and Tawny Owls) are very aggressive towards other birds-of-prey, especially during the breeding season; birds of prey and smaller owls form often as much as 3-5% of the total food of the Eagle Owl. Owls are generally monogamous, nesting in individual pairs, which are apparently permanent. But some males are known to be polygynous: at least, bigamous males of Tawny, Eagle, Snowy, Short-eared and Tengmalm's Owls have been discovered. Owls usually hide away by day in holes, or in dark places in thick foliage, taking advantage mainly of their protective plumage. At least 80 species out of 134 hunt by night; others are known to be active at dusk or in full daylight. In northern latitudes the Snowy Owl and the Hawk Owl hunt during the light nights of the Arctic summer and in winter during the short hours of daylight. Some species seem to enjoy sun-bathing (Little Owl, Burrowing Owl). Voice. Several species of owls sing, some very musically. In temperate regions it is the owls which in late winter or early spring fill the night with music, and in the tropics owls are just part of a formidable chorus of animal songs and calls. Throughout the world they have an extraordinary repertoire of shrieks, hoots and caterwaulings, in a range of frequencies which carry far on the night air. These announce their presence and the existence of occupied territories. Calls are completely diagnostic of species, and owls are as likely to recognize other individuals by voice as by sight during their travels in the dark. Individual Tawny Owls can be identified from sonagrams of their hooting. Breeding. The weather and the food available influence the start of breeding activities and many species appear to make an assessment of rodent abundance; during good vole years they lay earlier and larger clutches than in poor ones. Late snowfalls may cause even advanced broods to be abandoned, while an abundant food supply and high temperatures can encourage reproduction by Barn and Short-eared Owls even in winter. With minor exceptions, owls make hardly any nests themselves; instead, they use other birds' nests--such as the abandoned nest of a raptor or corvid-and holes in trees or rocks and a great variety of other places, including human habitations. Eagle Owls sometimes dig their nest cavities into uninhabited anthills. Owls of taiga and tundra nest on

open ground or in low vegetation; they make a shallow scrape and even add some lining material to their nests (e.g. Snowy and Short-eared Owls). Desert species tend to live underground, taking over abandoned rodent burrows to escape the heat of the sun. Owls' eggs are chalky-white

421

and roundish, the number varying from 1-14. Clutch-size is dependent on the food supply available, the differences from one season to the other being most notable in species which feed on rodents subjected to cyclic population fluctuations. Hence, in years of abundance, the Snowy Owl may have clutches of 10-14 eggs, and in years of food scarcity it may have clutches of 2-4, or not breed at all. Owls lay their eggs several days apart, and incubation starts with the first egg laid, resulting in marked differences in the size of the young in the nest. In good years all the young may survive, whereas in bad years the oldest progeny compete with their siblings for scarce food, and the clutch produces one well-fed fledgling instead of 3 or 4 starved weaklings. Such flexibility maximizes success in good years, while minimizing the risk of total failure in bad years. Usually only the female incubates, while the male forages and brings food to the female; both sexes care for the young. The incubation period is long, being 32-34 days in the Barn Owl, 26-28 in the Long-eared Owl, and 34-36 in the Eagle Owl. The young are nidicolous after hatching, with ears and eyes closed and body lacking independent means of temperature regulation. After the natal down, the young acquire the so-called mesoptile feathers, which are followed by true feathers appearing on the same feather papillae (see PLUMAGE). Young owls become capable of breeding at about the age of one year; i.e. in the first spring after the year of birth. Owls have the reputation of reaching a great age, but records of their longevity are still inadequate. The life expectation of ringed Barn Owls in Switzerland has been found to be surprisingly short, being on average 16 months; only a few individual birds are known to have reached the age of 9 years. But in captivity one Tawny Owl has lived for 22 years and 2 Eagle Owls for 53 and 68 years respectively. See photo VISION. (K.H.V.) H.M. Burton, I.A. (ed.) 1973. Owls of the World. London. Clark, R.J., Smith, D.G. & Kelso, L.H. 1978. Working Bibliography of Owls of the World. Washington. Lundberg, A. 1979. Residency, migration and a compromise: adaptations to nest-site scarcity and food specialization in three Fennoscandian owl species. Oecologia 41: 273-281. Mikkola, H. 1976. Owls killing and killed by other owls and raptors in Europe. Brit. Birds 69: 14~154. Mikkola, H. 1981. Der Bartkauz. Die Neue Brehm Bucherei 538: 1-124. Mikkola, H. 1983. Owls of Europe. Calton. Southern, H.N. 1970. The natural control of a population of Tawny Owls. J. Zoo!' (London) 162: 197-285. Sparks, J. & Soper, T. 1970. Owls, their Natural and Unnatural History. Newton Abbot. Watson, A. 1957. The behaviour, breeding, and food ecology of the Snowy Owl Nyctea scandiaca. Ibis 99: 419-462.

OWLET: term for a nestling

OWL.

Owlet-frogmouth Aegotheles cristatus. (C.E.T.K.).

OWLET-FROGMOUTH: substantive name of the species of Aegothelidae (Caprimulgiformes, suborder Caprimulgi): in the plural, general term, alternatively 'owlet-nightjars' , for the family. Systematics and distribution. The group is related to the frogmouths (Podargidae) and consists of a single genus of small arboreal night jars (in

the ordinal sense) almost restricted to the Papuo-Australian area. One species has penetrated to the Moluccas and another is found in New Caledonia. New Guinea is inhabited by 5 species, of which Aegotheles cristata occurs widely in Australia. Extensive fossil remains of a closely

422

Oxpecker

allied form have been found in the Pleistocene to Recent in New Zealand, described as Megaegotheles nooaezealandiae by Scarlett (1968). Structurally, Aegotheles resembles Podargus but with several differences. The features in which it resembles Podargus, but which are not shared with true nightjars, include the desmognathous palate and the bronchial syrinx; the sternum has two foramina on each side instead of being double-notched. However, it possesses the two carotids normal in the order and an oil gland, and it lacks the powder-down tufts found in Podargus. It is unique in the order in not having caeca. Characteristics. The body length is 20.5-24 em. Plumage characters of mottled brown are similar to those of the frogmouths and true night jars (Caprimulgidae). The frogmouth-like bill is shorter and weaker than in Podargus or Batrachostomus, and it is largely obscured by the forehead feathering. Stiff and partly erectile filoplumes occur on the forehead and lores, with a few softer recurved filoplumes on the chin. The bird sits with an upright, owl-like stance, but it does not adopt the rigid 'broken branch' stance, when alarmed, which is characteristic of Podargus. Generally, it is a more active bird than the comparatively lethargic Podargus. Habitat. Aegotheles lives in forested and semi-open country, and has the same arboreal habits as Podargus. Food. The feeding habits appear to be intermediate between those of the frogmouths and the true nightjars. Aerial hawking for flying insects has been described, but most hunting is done from the ground, the bird sometimes rising to take flying insects; most of the stomach contents analysed suggest that the bird feeds predominantly on terrestrial prey. Rich and Scarlett (1977) infer that the fossil New Zealand M egaegotheles, which tended to gigantism and 'may have been well on its way to becoming another of New Zealand's flightless birds', was a terrestrial insectivore. Voice. The calls include a loud hissing note and a repeated churring call. Breeding. Nesting takes place in hollow trees or occasionally in tunnels in banks. No actual nest may be constructed, or the eggs may be laid on a mat of dry leaves or mammal fur. The colour of the shell is white, as in Podargus, and the clutch is 3 or 4. The fledgling is covered with dense white down. The birds are readily flushed from their roosting or nesting hollows by tapping likely limbs or tree trunks. D.L.S. Fleay, D. 1968. Nightwatchmen of Bush and Plain. Brisbane. Rich, P.V. & Scarlett, R.}. 1977. Another look at Megaegotheles, a large OwletNight jar from New Zealand. Emu 77: 1-8. Scarlett, R.}. 1968. An Owlet-Nightjar from New Zealand. Notornis 15: 254-266. Schodde, R. & Mason, 1.}. 1980. Nocturnal Birds of Australia. Melbourne.

OXPECKER: substantive name of the 2 species constituting the subfamily Buphaginae of the Sturnidae (Passeriformes, suborder Oscines) (see STARLING); in the plural, general term for the subfamily. They are also called 'tickbirds'. The 2 species are similar (starling-like but with short legs) in size (18-19cm long), and are very much alike with dull brown plumage; the sexes are similar, and the bill colouring is fully developed only in adults. Characteristics, habitat and distribution. The Yellow-billed Oxpecker Buphagus africanus which has the terminal half of its broad bill red and the rump paler than the back occurs from west Africa through to western Ethiopia, east Africa and south to southern Africa. It became extinct in South Africa before 1914. The slightly smaller Red-billed Oxpecker B. erythrorhynchus, which has the whole narrow bill red and the back and rump concolorous, has a more restricted geographical range, from Eritrea and the south-eastern Sudan to South Africa and across to northern Namibia. It is an eastern species, its western limit being approximately 30 except in the south of its range. In broad terms, therefore, B. africanus occupies the region west of the Rift Valley system, crossing it only in the area immediately to the north of Mount Kenya and in western Tanzania; it is absent from areas of dense forest, as is B. erythrorhynchus, though penetrating the open parts of the Congo. Both species are typical inhabitants of the African savanna. Oxpeckers are notable for their special association with indigenous African ungulates and also domestic livestock (Artiodactyla and Perissodactyla). The birds are wholly dependent on their mammalian associates. Although the geographical ranges of the two species overlap in parts, their distribution and density are often patchy in accordance with their mammalian associates. In areas of sympatry the Yellow-billed Oxpecker associates more commonly with naked or sparsely furred mammals (e.g. 0E

Yellow-billed Oxpecker Buphagus africanus. CD.A.T.).

the African Buffalo Syncerus cafter) than with mammals with moderately dense fur, including cattle, to which the Red-billed Oxpecker is then restricted. Both species, however, associate with a wide variety of mammals, including rhinoceros, giraffe, warthog, zebra and various antelopes, and both species prefer less densely furred mammals. The association is influenced by the behaviour of the mammals as well as that of the birds. Most ungulates are remarkably indifferent to the birds clambering over their bodies. However, waterbuck, reedbuck, hartebeest, tsesseby and steenbuck, for example, are intolerant of oxpeckers. Despite their naked skins, elephants, which are not ungulates, are not used by oxpeckers, apparently because elephants are intolerant of them. Populations. In the last few decades the distribution and numbers of oxpeckers have been greatly reduced, with the extension of regular dipping of cattle to control ticks. Successful reintroduction into a game reserve in Zimbabwe has been accomplished. Food. Oxpeckers obtain nearly all their food from the skins of their mammalian associates. Despite the differences in bill morphology, both species seem to use the same techniques for foraging. Ticks, chiefly members of the genera Amblyomma, Boophilus and Rhipicephalus, comprise their main food and flies are a supplement. The birds progress on their hosts by walking and hopping, using their sharp, curved claws; their stiff, rather long tails are employed for bracing support when clinging to vertical surfaces. The birds' beaks are laterally flattened, facilitating a 'scissoring' feeding action in which the bill is opened and closed rapidly while being pushed through the pelage or over the skin of the mammalian host. This is the normal method of foraging. Plucking and pecking are also used in capturing ticks, and in feeding on scurf and open sores. The birds occasionally hawk flying insects, but are not very adept at this. At least in the case of the Red-billed Oxpecker, they feed mainly in the morning and late afternoon, resting in the middle of the day. They drink regularly, the host being used as a platform from which the birds descend to waterholes. Voice. In addition to a variety of harsh starling-like calls, oxpeckers have a distinctive hissing alarm call given when disturbed on a mammal or at the nest. It is believed that they act as sentinels for their mammalian associates, particularly rhinoceroses, but this has yet to be critically evaluated: Behaviour. More than a dozen birds can be found on a single large animal, such as a giraffe, but individual foraging groups generally are smaller. The birds roost communally, at traditional sites in trees, reeds, cliffs, buildings etc., the roosts, at which other species of starlings often also roost communally, comprising one or more individual groups of oxpeckers. The roosts decline in size with the onset of the wet season which is the start of the annual breeding cycle. Breeding. Oxpeckers nest in tree cavities. All searching for nest holes is done from the mammalian hosts. Animal hair, dung, grass and rootlets are used for the nest. Up to 5 birds constitute a co-operative breeding group, and all collect nest material. Copulation occurs on the backs of the mammalian associates or on the ground. Only one female and one male actually breed, in that this pair is responsible for the production of fertile eggs (1-5 per clutch, most often 2 or 3) and their incubation (about 12

Oystercatcher

days). The eggs are pinkish white, with small red-brown, purple and lilac spots. In the daytime, the incubating birds relieve each other approximately every hour; the female incubates at night. All members of the group feed the nestlings which continue to be given food once they have left the nest, at about 30 days if undisturbed, and until they are about 3 months old. Up to 3 broods are raised in a season. Breeding overlaps with moult which is exceptionally long; the primaries are replaced over an II-month period in the Red-billed Oxpecker. W.R.S. and R.K.B. Anwell, R.I.G. 1966. Oxpeckers, and their association with mammals in Zambia. Puku 4: 17-48. Bezuidenhout, ].D. & Stutterheim, C.]. 1980. A critical evaluation of the role played by the Red-billed Oxpecker Buphagus erythrorhynchus in the biological control of ticks. Onderstepoort ]. Vet. Res. 47: 51-75. Buskirk, W.H. 1975. Substrate choices of oxpeckers. Auk 92: 604--606. Grobler, ].H. 1979. The re-introduction of oxpeckers Buphagus africanus and B. erythrorhynchus to the Rhodes Matopos National Park, Rhodesia. BioI. Conserve 15: 151-158. Stutterheim, C.]. 1980. Symbiont selection of Redbilled Oxpecker in the Hluhluwe-Umfolozi Game Reserve Complex. Lammergeyer 30: 21-25. Stutterheim, C.]., Mundy, P.]. & Cook, A.W. 1976. Comparison between the two species of oxpecker. Bokmakierie 28: 12-14.

OXYRUNCIDAE: family of Oscines; SHARPBILL.

PASSERIFORMES,

suborder Deutero-

OXYURINI: see DUCK.

Oystercatcher Haematopus ostralegus. (R.G.).

OYSTERCATCHER: substantive name of all the species of Haematopodidae (Charadriiformes, suborder Charadrii); in the plural, general term for this small cosmopolitan family. Characteristics. Oystercatchers, sometimes called 'sea-pies', are large waders (4~S em long) with either black-and-white or wholly black plumage. The powerful bill is characteristic-being long, stout, laterally compressed, and bright orange-red. It is specially adapted for opening the shells of bivalve molluscs but is also used for probing in mud, sand or turf. The rather thick legs are reddish; and each foot has 3 toes, slightly webbed. The tail is short; the wings are long and pointed. There are some slight seasonal and sexual differences, and the juveniles are more dark brown than black and have less brightly coloured bills and legs. On the ground the birds normally walk but can run swiftly. They can swim well on occasion. The flight is rapid and direct, with rather shallow wing-beats. Oystercatchers are noisy and restless birds, often by night as well as by day, the characteristic call being a loud clear klee-eep, klee-eep.

423

Habitat. Oystercatchers are mainly birds of the seashore, and outside the breeding season they gather in flocks, sometimes of many thousands. Flocks of immature birds persist throughout the year, especially in certain favoured areas, for instance, in the British Isles, the northern coasts of the Irish Sea. It has been shown that the birds (at least of the European species) do not breed until 3 years old. Distribution and populations. The family has no representatives breeding in very high latitudes or in tropical Africa or southern Asia. Otherwise, the distribution includes the coasts of most of both Old and New Worlds, and also certain inland areas to be mentioned below. Populations in higher latitudes tend to be migratory. There is only a single genus, and the numerous forms comprised in it are grouped by different authors in from 3 to 6 or 7 species. The taxonomic position is complicated by the existence of melanistic populations, by some regarded as consisting of black mutants and by others as constituting distinct species. The Oystercatcher Haematopus ostralegus in various subspecific forms, some pied and some black, breeds from Arctic Europe to the coasts of the Aegean, Black, and Caspian Seas; on the Canary Islands and the coasts of temperate South Africa; and in Australasia from New Guinea to Tasmania and New Zealand. Further, the race H. o. longipes breeds mainly about inland waters from Kiev eastwards through southern and eastern Russia and Siberia to the Cis-Altai steppes, and is probably the race found breeding on the tributaries of the R. Euphrates in eastern Turkey, up to 1,900 m. The British race H. o. occidentalis has bred inland in Scotland for centuries and has recently begun to spread along the river valleys in the north of England. The form H. o. unicolor (H. 'jinschi' of some authors) breeds far inland along the courses of the snow rivers of South Island, New Zealand. All these inland breeding birds apparently winter on the coasts. Certain of the New World forms are treated by some as races of H. ostralegus. By others they are assigned to separate species, such as the Black Oystercatcher H. bachmani of western North America and the widely distributed American Oystercatcher H. palliatus, Other species which have been recognized are the Sooty Oystercatcher H. fuliginosus of the coasts of Australia and two which both inhabit the coasts of southern South America and the Falkland Islands; of these last, H. ater is a black form while H. leucopodus is pied but with a black chest and under wing coverts, yellow (not crimson) eyelids, and other peculiarities of plumage. Food. The food consists chiefly of molluscs, crustaceans, annelid worms, and insects, varying with the particular habitat (rocky or sandy shores, estuaries, river gravels, moorland, farmland). With their powerful bills, they can knock limpets off rocks. There is some evidence that birds on inland territories breed more successfully than those on coastal territories, probably because they can gather food for the chicks, which are dependent on their parents, unrestricted by the tides. Behaviour and voice. The species present in Europe has an elaborate 'piping' ceremony in which 3 or more birds run about with 'shoulders hunched' and bills held pointing to the ground, while they utter together a rapid high-pitched trill. This behaviour is probably concerned with the separation of breeding pairs from the flock; both sexes take part and either may initiate it-and, apparently, immature birds do not pipe. As Makkink (1942) says, this ceremony is 'a mechanism which first enables the sexes to arrange themselves into pairs, and subsequently creates opportunities for the formed pairs to take up a position' against their fellows. Although this performance usually takes place on the ground, it sometimes occurs when the birds are in Hight. Breeding. The nest is a mere scrape in the ground, which is often decorated-rather than lined-with white shells, bones, stones, and other objects. The 2-4 eggs (usually 3 in the European species) are yellowish buff, heavily marked with dark brown or black. One clutch is laid and both sexes take part in incubation. The cryptic coloration of the eggs is highly effective, and the old birds avoid betraying the position; DISTRACTION BEHAVIOUR ('injury feigning') occurs, and also 'false brooding' at spots where no eggs lie. Incubation, in the European species, normally lasts for 26 or 27 days. The chicks run as soon as their cryptic down is dry; they are, however, fed by their parents for at least 6 weeks; they take about 5 weeks to fledge. See photo FLOCKING. E.J .M.B. Buxton, E.] .M. 1939. The breeding of the Oystercatcher. Br. Birds 33: 184--193. Buxton, E.] .M. 1961. Inland breeding of the Oystercatcher in Great Britain. Bird Study 8: 194--209. Dare, P.]. 1966. The breeding and wintering populations of the Oystercatcher in

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Oystercatcher

the British Isles. M.A.F.F. Fishery Investigations ser. II vol. XXV, no. 5. Dare, P.]. 1970. The movements of Oystercatchers visiting or breeding in the British Isles. M.A.F.F. Fishery Investigations ser. II, vol. XXV, no. 9. Dircksen, R. 1932. Die Biologie des Austernfischers, der Brandseeschwalbe und der Kiistenseechwalbe nach Beobachtungen und Untersuchungen auf Norderoog. J. Orn. 80: 427-521. Heppleston, P.B. 1972. The comparative breeding ecology of Oystercatchers in inland and coastal habits. J. Anim. Ecol. 41: 23-51. Heppleston, P.B. 1973. The distribution and taxonomy of Oystercatchers. Notornis 20: 102-112.

Huxley, J.S. & Montague, F.A. 1925. Studies on the courtship and sexual life of birds. V. The Oystercatcher (Haemaiopusostralegus L.). Ibis (12 ser.) 1: 868-897. Lind, H. 1965. Parental feeding in the Oystercatcher. Dansk Orn. For. Tidsskrift 59: 1-31. Makkink, G.F. 1942. Contribution to knowledge of the behaviour of the Oystercatcher (Haematopus ostralegus L.). Ardea 31: 23-74. Stresemann, E. 1927. Die schwarzen Austernfischer (Haematopus). (Mutationstudien xxvi). Orn. Mber. 35: 71-77. Webster, J.D. 1941. The breeding of the Black Oystercatcher. Wilson Bull. 53: 141-156.

p

and flushed birds may give a somewhat sharper alarm note. Food. Omnivorous diet includes invertebrates, particularly Orthoptera, molluscs and earthworms, and seeds. They feed by probing soft mud or with scything movements of the bill in shallow water. Behaviour. Being so secretive, few behavioural observations have been made, particularly on the American species. R. benghalensis usually occurs solitarily or in pairs, though after breeding flocks comprising several family groups may form. Males outnumber females and polyandry is the general rule, although in sparse populations, such as those in South Africa, monogamous bonds may form. Breeding is during the rainy season and the females take up territories within which they court several males in succession. They declare their territories and attract males with an advertisement flight not unlike the roding of Woodcock Scolopax rusticola. On the ground, one display is used both to woo males and during territorial disputes with other females. At low intensity the female stands sideways on, the far wing raised or extended, the tail fanned or depressed. At higher intensity she faces her opponent or mate, lowers her breast and extends and pronates both wings, bill pointed downwards and tail fanned. Females may actually fight each other in defence of their mates. Breeding. The nest is a pad of woven plant material concealed in dense vegetation and is built by the male, though the female may be in attendance. The normal clutch is 4 (occasionally 5 or 6) pointed oval eggs, glossy cream or yellow marked with bold black blotches, speckles or lines. After laying the female leaves the male to incubate for c. 20 days and rear the young, and goes to court another mate. Bonds form rapidly, the second clutch often being laid before the first is hatched. The nests of one female usually form a loose group 4-10 m apart, and in Japan 2--4 clutches per female are usual. The males attend the nidifugous young and may use the head-on form of display to frighten off predators, as well as occasionally employing a rudimentary form of distraction display to lure observers from the chicks. In the less well-known N. semicollaris the female incubates the eggs, though polyandry appears also to be normal and the male escorts the young. Single nests may be found, usually during July, though groups of 5 or 6 in an area of a hectare are most usual. The nests are also of woven plant matter, and the 1 or 2 eggs are white, evenly mottled with black, sometimes so densely as to appear wholly black. The call is a plaintive whistle. A.S.R.

PACHYCEPHALIDAE; PACHYCEPHALINAE: family and subfamily of PASSERIFORMES, suborder Oscines; THICKHEAD. PADDLING: see

FEEDING HABITS.

PADDY: alternative name (plural 'paddies') for Chionis spp. (for family see SHEATHBILL). PADDY-BIRD: otherwise the Indian Pond Heron Ardeola grayii (see HERON).

PAINTED SNIPE: substantive name for the 2 species of Rostratulidae (Charadriiformes, suborder Charadrii): the Old World Painted Snipe Rostratula benghalensis (colloquially 'painter') and the American Painted Snipe Nycticryphes semicollaris (called 'sleepyhead' in Argentina). Both superficially resemble snipe Gallinago spp. and, like the [acanidae and Gruidae, have two notches on the posterior edge of the sternum. Characteristics. Both species are unmistakable. Skulking and difficult to flush, they often run with lowered head, stopping to bob the head and neck if alarmed. They seldom fly far, with slow wingbeats and dangling legs, before diving into cover. The plumage is spectacular, particularly in the females which are some 10% larger than the males. R. benghalensis (25 em long) has longer legs, shorter bill and tail and broader wings than snipe. The bill is decurved at the tip, the nostrils lying in deep narrow grooves which extend over half-way along the mandible. The eyes lie towards the front of the skull, and the toes are un-webbed. The female has a chestnut face and black crown divided by a thin, buff stripe; diagnostic white spectacles surround the eyes. A white stripe over the shoulder separates the dark head and neck from the bronzy-green upperparts, whose dark vermiculations are only discernible at close range. The rump and rounded tail are browner, and marked with white spots, and the underparts are white, a black band running across the chest. The male is similarly patterned, though the colours are more subdued and less uniform. The chest, neck and coverts are barred, and the spots more obvious, creating a disruptive effect. The bill colour varies; generally it is pale brown, darker at the tip, becoming greenish towards the base. Juveniles resemble males and the downy nestling is striped. N. semicollaris (21.5 em long) is smaller, with a more curved, terminally flattened bill. It has a slight web between the middle and outer toe, and the tail is wedge shaped. The sexes are similar, being deep chocolate brown above, finely barred with black. The head lacks spectacles, having superciliary stripes in addition to that on the crown. Two buff streaks form a V over the back and the coverts bear conspicuous white spots; the primaries are white on their outer edges. The underparts are white and the bill greenish or pink, tipped with red. Immatures are paler and more variegated. Habitat. Low, swampy areas are preferred, with patches of open water interspersed with dense vegetation, as well as paddy fields and freshly flooded land. Birds may leave cover at dawn and dusk to forage on grassland and ploughed fields. Distribution and movements. R. b. benghalensis inhabits Africa, the Middle East and southern Asia; R. b. australis, Australia; and N. semicollaris southern South America. Both species are generally sedentary, though R. b. benghalensis may make short migrations to follow the rains. Voice. R. benghalensis is usually silent outside the breeding season. The voice of the female is deeper than that of the male due to a longer, convoluted trachea, which, during the breeding season, becomes less firmly held in the fat of the neck. The low mellow vot notes given during her display flight carryover long distances. When displaying on the ground to a male, mellow booo notes are given, reminiscent of the sound produced by blowing across a bottle. When confronting a rival or predator, throaty hissing and growling sounds are given by both sexes,

Ali, Salim & Ripley, S.D. 1969. Handbook of the Birds of India and Pakistan, vol. 2. Bombay. Cairns, J. 1940. Birds of Penang and Province Wellesley. Malay Nature Journal 1: 32-34. Kobayashi, K. 1954. (Observations of the Painted Snipe.) Tori 13: 31-39. Kobayashi, K. 1955. (Observations of the Painted Snipe.) Tori 14: 1-13. Lowe, V.T. 1970. Notes on the behaviour of the Australian Painted Snipe. Australian Bird Watcher 13: 218-220.

Painted Snipe Rostratula benghalensis. (M. W.).

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Pair

Muller, K.A. 1975. Threat display of the Australian Painted Snipe. Emu 75: 28-30. Wood-Mason, J. 1878. The structure and development of the trachea in the Indian Painted Snipe (Rhynchaea capensis). Proc. Zool. Soc. Lond. 18 June 1878: 745-751.

PAIR: collective noun for, inter alia, two birds of opposite sexes, ordinarily used of adults (normally of the same species) believed to be mated together. PAIR FORMATION: establishment of a special relation between two birds of opposite sex. Practically every type of relationship between the sexes occurs among birds. Some species, e.g. 'lek birds', have merely a temporary pair bond, the sexes meeting only for copulation (see LEK). More usually there is a lasting relationship, which may endure for days, weeks, or even years, and which may be monogamous, polygamous, or polyandrous (see MATING SYSTEMS; POLYANDRY). Monogamous relationships are most frequent, and it is with that type that this article is primarily concerned. Such relationships are of course normally heterosexual; although pairing between individuals of the same sex is common in captive birds, it is rare in the wild. Pair formation implies that a number of social responses, potentially elicitable by any member of the species, become more or less limited to one individual; at the same time other responses (e.g. aggressive ones) become inhibited towards the partner. When paired, the mates often tend to keep together for much of the time, and may show a special type of searching behaviour if they lose contact. Pair formation depends on an exchange of signals between potential mates over a period of time. These may be visual (e.g. colours or structures, often exhibited by courtship displays-see DISPLAY), or auditory (e.g. song-see VOCALIZATION). Since hybrids are usually at a selective disadvantage compared to their parental types, it is important that pairing should be intraspecific (see HYBRID). For this reason the signals usually differ markedly between closely related species living in the same area (see ISOLATING MECHANISM). Specific differences in courtship postures are shown in every comparative study, and the relevant plumage patterns usually differ between species more than the displays themselves. Sympatric closely related species also often differ markedly in song (e.g. Willow Warbler Phylloscopus trochilus and Chiffchaff P. collybita). The study of hybrids shows that such interspecific differences are usually polygenic, and are thus likely to be of adaptive value. That this value lies in the prevention of hybridization is suggested by the following types of evidence. 1. Divergence is most marked in those characters important in pair formation. Thus amongst cardueline finches, where there may be an interval of some weeks between pair formation and copulation, the early courtship displays differ between species more than do those immediately preceding copulation (see COPULATION). 2. Divergence is often greatest where hybridization is most likely, for instance in the overlap zone of potentially sympatric species. 3. Species characteristics often tend to disappear on oceanic islands, where no closely related species are present. 4. Divergence is more marked in males than in females. This is in harmony with Dobzhansky's view that since gamete loss is more serious for females than for males, it is primarily female preference that will be selected for; but the fact is also explicable in other ways, such as the maintenance of female uniformity by selection for cryptic coloration. Mayr (1942) has shown that hybrids are more common in genera in which copulation is not preceded by an 'engagement' period (e.g. Paradisaeidae; some Tetraoninae), although hybrids do of course occur in groups that form lasting pair bonds. On the whole, however, hybrids are extraordinarily rare in nature, even among species that hybridize readily in captivity when conspecific mates are not available (see HYBRID). Pair formation has been most studied in territorial song-birds (see TERRITORY). Where territorial establishment precedes pair formation and this occurs some time before copulation (e.g. Robin Erithacus rubecula, Snow Bunting Plectrophenax nivalis, Chaffinch Fringilla coelebs), the female is usually first attracted by the song or appearance of the male. The male normally responds aggressively to all intruders on his territory. If the intruder is a male, he flees or fights back. If it is a female not yet ready to pair, she flees. If, however, it is a female in condition, she usually stays around, often showing a 'submissive' posture, and the male's attacks gradually cease. The male then gradually ceases to be aggressive and begins to show courtship behaviour. The range of

variations on this theme is of course enormous. For instance, the process may take anything from minutes to days; the stimuli to which each sex responds may be primarily structural, behavioural, or both; and the male's aggressiveness may cease almost at once or persist right up to copulation. Where pair formation precedes territorial establishment, it may start with the male's behaving aggressively to other members of the flock, although the process is fundamentally similar. Usually the increasing tendency of the male to behave sexually as the season advances is associated with a reduction in his aggressiveness towards his partner, who may then become dominant. Outside territorial song-birds, the diversity of behaviour is even greater. For instance, in some crows and ducks pair formation seems to involve a social ceremony. In most cases that have been studied in detail (e.g. Laridae), however, there seems to be a similar interplay between tendencies to attack, to flee from, and to behave sexually (or socially) towards the mate. The term sexually is, of course, to be interpreted rather widely, since in the early stages the consummatory situation is proximity to the mate rather than copulation, and the relation between male and female is little different from that between flock companions. It will be clear that the dominance relations during pair formation may be very complex; indeed many species pass through a phase in which the female attacks the male during courtship, but the male attacks her at other times, so that a distinction can be made between sexual and social dominance. Although pair formation is usually associated with changes in dominance, it is very difficult to make useful generalizations about the role that dominance plays (see DOMINANCE (2)). Because of the diversity of the processes of pair formation, it is impossible to classify species into a limited number of types. Lorenz (1935) attempted a classification that depends primarily on whether the displays of the sexes are similar or different, on whether one or both sexes show 'releasers', and on whether males respond initially to other members of the species by aggression or courtship. Although his classification has been criticized by N. Tinbergen, D. Lack, and others, and it is clear that his categories do not represent inclusive groups, they are useful as types. R. A.H. Armstrong, E.A. 1947. Bird Display and Behaviour. London. Hinde, R.A. 1959. Behaviour and speciation in birds and lower vertebrates. BioI. Rev. 34: 85-128. Lack, D. 1939. The behaviour of the Robin. I and II. Proc. Zool. Soc. Lond. A, 109: 169-178. Lack, D. 1940. Pair formation in birds. Condor 42: 269-286. Lorenz, K. 1935. Der Kumpan in der Umwelt des Vogels. J. Orn. 83: 137-213, 289-413 (and, 1937. The companion in the bird's world. Auk 54: 245-273). Mayr, E. 1942. Systematics and the Origin of Species. New York. Tinbergen, N. 1948. Social releasers and the experimental method required for their study. Wilson Bull. 60: 6--52. Tinbergen, N. 1952. Derived activities: their causation, biological significance, origin and emancipation during evolution. Quart. Rev. BioI. 27: 1-32. Tinbergen, N. 1953. Social Behaviour in Animals. London. Tinbergen, N. 1959. Comparative studies of the behaviour of gulls (Laridae): a progress report. Behav. 15: 1-70.

PALAEOGNATHAE: a formerly recognized superorder. PALAEOG N ATHOUS: also 'palaeognathine' (Pycraft)-see

PALATE.

PALAEOMONTANE: belonging to the fauna of the alpine or snow (nival) zones of the high mountains of the Palearctic Region. PALAEONTOLOGY: the study of fossilized remains of animals and plants (see ARCHAEOPTERYX; EARLY EVOLUTION OF BIRDS; FOSSIL BIRDS). PALAEOSPECIES: a species existing at an earlier level of geological time, possibly ancestral to one or more species of the present day but distinct from any of them; the ordinary criteria of a species are purely contemporary. PALAEOTROPICAL: inclusive term used by Sclater for his three southern zoogeographical regions in the Old World, contrasted with the Palearctic Region (and on the other hand with the Neotropical ); more generally, a term implying wide distribution in the tropical parts of the Old World (see DISTRIBUTION, GEOGRAPHICAL). PALAEOXERIC: belong to the fauna of the steppes and deserts of the southern Palearctic Region.

Palate

PALAEO-XEROMONTANE: belonging to the fauna of the arid slopes of the low mountains of the southern Palearctic Region. PALAEOZOOLOGY: the part of palaeontology that is concerned with forms ascribed to the Animal Kingdom. PALATABILITY OF BIRDS AND EGGS: regarded both from the subjective human standpoint and, so far as possible, from that of the observed preferences of other animals. The inverse relation that is commonly found between palatability on the one hand and vulnerability and conspicuous coloration on the other is particularly considered. Palatability of the flesh. It is well known that the flesh of birds differs widely in palatability. Some enjoy a high reputation in this respect, e.g. Quail Coturnix coturnix, Partridge Perdix perdix, Red Grouse Lagopus lagopus scoticus, Golden Plover Pluvialis apricarius, Woodcock Scolopax rusticola, Snipe Gallinago gallinago, Teal Anas crecca, Canvasback Aythya valisineria, Corncrake Crex crex, Bittern Botaurus stellaris, and Skylark Alauda arvensis. Others are unfit for the table, e.g. Kelp Goose Chloephaga hybrida, Smew Mergus albel/us, Shelduck Tadorna tadorna, Oystercatcher Ostralegus haematopus, Egyptian Plover Pluvianus aegyptius, Hoatzin Opisthocomus hoazin, and various horn bills, kingfishers, and drongos. (See also UTILIZATION BY MAN.) Attempts to assess relative palatability more exactly by experiments with meat-eating animals, and by observations of tasting panels, have extended knowledge to include a wide range of species not normally eaten by man, and have shown that among relatively vulnerable species, cryptic coloration, whether in the female alone or in both sexes, is generally associated with edibility, and conspicuous coloration with distastefulness. For example, in a series of experiments in which hornets were used in Egypt as assessors of the acceptability of the flesh of 38 species, the two rated as most acceptable (Wryneck Jynx torquilla and Crested Lark Galerida cristata) are also the two most cryptic in appearance; and those of lowest edibility (White-rumped Black Chat Oenanthe leucopyga, Mourning Chat O. lugens, Hooded Chat O. monacha, Pied Kingfisher C eryle rudis, Masked Shrike Lanius nubicus, and Hoopoe Upupa epops) are all conspicuous and include the only three species in the series examined having exclusively black-and-white coloration. On available evidence other and quite unrelated tasters, such as cat and man, show generally similar preferences and aversions. Nauseousness is a common but not invariable attribute of conspicuous birds, for many highly conspicuous species are nevertheless relatively palatable, e.g. various albatrosses (Diomedeidae), storks, egrets Egretta spp., swans Cygnus spp., cranes, gulls, and macaws and cockatoos (Psittacidae); but such birds have no need of a nauseous deterrent, being otherwise protectedby large size, fighting strength, social habits, or ability to escape. Tests recently carried out by members of a tasting panel in Zambia (Department of Game and Tsetse Control) confirm the above general conclusions. Samples of flesh were assessed on a scale from 9.0 (excellent) to 2.0 (inedible). Of 191 species examined, the 19 rated higher than 7.0 include 15 cryptic species, and in 10 of these the female or both sexes are highly cryptic (Quail Coturnix coturnix, the Kaffir (or African Water) Rail Rallus caerulescens, Corncrake Crex crex, African Crake Crecopsis egregia, Water Dikkop Burhinus vermiculatus, Senegal Bustard Eupodotis senegalensis, Black-bellied Bustard Lissotis melanogaster, Double-banded Sandgrouse Pterocles bicinctus, Yellow-throated Sandgrouse P. gutturalis, and Fiery-necked Nightjar Caprimulgus pectoralis fervidus. In contrast, of 14 species with plumage that is black, white, or a combination of both, only the White-breasted Cormorant Phalacrocorax carbo lugubris (7'0) was rated as palatable, and Little Egret Egretta garzetta (6.3), and Openbill Stork Anastomus lamelligerus (6.0) as moderate. Nine of the remainder are relatively or markedly distasteful, notably Pied Crow Corvus albus (4.9), White-winged Black Tit Parus leuconotus (4.8), Black (or Sooty) Chat Myrmecocichla nigra (4.5), Whiteheaded Black Chat Thamnolaea arnotti (4.5), Pied Kingfisher Ceryle rudis (4.1), Southern Black Tit Parus niger (4.1), and Black Cuckoo Cuculus cafer (3.0). The relation between visibility and distastefulness is also seen within the limits of restricted groups, for example: among 6 crakes examined, the only conspicuous species (Black Crake Limnocorax flavirostra) has the lowest edible rating (5.1); of 6 chats, the 3 most conspicuous are also the 3 most distasteful (all 4.5); the same relationship is found in 5 plovers, of which 2 (Blacksmith Plover Vanellus ('Hoplopterus') armatus, 5.1, and Long-toed Water Plover Vanel/us ('Hemiparra') crassirostris, 4.8) are both relatively conspicuous and distasteful.

427

Colour conflict. The inverse relation between acceptability of the flesh and visibility of the plumage is of special interest in a connection with the concept of 'colour conflict'. It has been shown elsewhere (see COLORATION, ADAPTIVE) that concealing (cryptic) and revealing (phaneric) characters subserve many and diverse functions of adaptive value in the struggle for survival. Yet for optical-psychological reasons the two types of coloration, although both advantageous, are generally antagonistic and tend to be mutually exclusive. The conflicting needs of effacement and of advertisement are reconciled in various ways. (a) Conspicuous characters, in birds of which the coloration is predominantly cryptic, may be revealed at special times by the momentary display of bright ornaments normally hidden (as in deflection displays, social recognition marks exposed only in flight, and the buccal feeding releasers of nidicoles, etc.). (b) Again, in many species, cryptic coloration is confined to the more valuable or vulnerable individuals, e.g. females in sexually dimorphic species where the males are conspicuous, e.g. many Anseriformes, Galliformes, and some territorial Passeriformes; and nidicolous young, where adults of both sexes are conspicuous, e.g. oystercatchers, some plovers (Charadriidae), gulls, and terns. (c) Relatively non-vulnerable species otherwise protected have no need for concealment; for them the road to conspicuousness lies open and has generally been taken by both sexes, e.g. cassowaries, gannets, pelicans, flamingos, some birds-of-prey, cranes, swans Cygnus spp., many gulls, and parrots. Such birds are not protected by distastefulness. (d) In many small and otherwise vulnerable birds the advantages of concealment have over-ridden those of visual advertisement, and cryptic coloration is developed in both sexes, e.g. in partridges Perdix spp., francolins Francolinus spp., quails Coturnix spp., coursers Cursorius spp., thickknees, nightjars, pipits Anthus spp., larks, warblers (Sylviinae). The palatability of such birds tends to render cryptic coloration of paramount importance. (e) Another line of evolution has led in the opposite direction, towards conspicuousness in both sexes, e.g. various plovers (Charadriidae), auks, turacos, Hoopoe Upupa epops, wood-hoopoes, kingfishers, barbets, shrikes, drongos, starlings, chats Oenanthe spp. etc. and tits. But this trend has been possible only for relatively defenceless species when it is associated with the counter-deterrent of repugnant taste. The advertising coloration of such birds is (in part) warning (proaposematic) in function. Palatability of eggs. Experiments with egg-eating mammals of several orders (cat, ferret, mongoose, hedgehog, rat), and observations by members of a tasting panel (Low Temperature Station, Cambridge) afford results parallel in many respects to those considered above. Edibility and coloration are related to various factors that influence the availability of eggs to predators. Thus, eggs laid by larger birds, or in colonies, or in sites difficult of access, are in general more palatable than those laid by smaller birds, or by solitary nesters, or in accessible sites. Among otherwise vulnerable species, many eggs in the higher edibility grades are protected by cryptic coloration or are covered by a close-sitting cryptic parent, e.g. in many ducks, game-birds (Galliformes), bustards, rails, waders (Charadrii), sandgrouse. On the contrary, conspicuousness of the shell is often associated with a repugnant taste. In a series of 212 species examined, the shells of the most ill-flavoured eggs were commonly either immaculate white or white with reddish spots: Red-faced Mousebird Colius indicus (3.5), Green Woodpecker Picus viridis (3.5), Verreaux's Eagle Owl Bubo lacteus (3.3), House Wren Troglodytes aedon (3.2), Wren T. troglodytes (2.7), Speckled Mousebird Colius striatus (2.5), Black Tit Parus leucomelas (2.0). Among eggs of low-grade edibility, the most widespread distasteful property is bitterness, which is highly developed in the flavour-pattern of Columbiformes, Cuculiformes, Strigiformes, Coliiformes, Coraciiformes, Piciformes, and Passeriformes. H.B.C. Cott, H.B. 1946. The edibility of birds. Proc. Zoo!' Soc. Lond. 116: 371-524. Cott, H.B. 1954. The palatability of the eggs of birds. Proc. Zoo!' Soc. Lond. 124: 335-463. Cott, H.B. & Benson, C.W. 1970. The palatability of birds, mainly based on observations of a tasting panel in Zambia. Ostrich Sup. 8: 357-384.

PALATE: the bony palate (Fig. 1) is made up of the same elements as are found in reptiles, except that the ectopterygoid or transpalatine is absent. Anterior are the premaxillae, which have shelf-like palatal processes fused in the midline at the front of the bill. Farther back these processes may be separated from each other by a cleft. There is often a large vacuity between them and the palatal processes of the maxillae, or

428 Palate

B

c

o

Fig. 1. Palate bones, seen from below, in A, Rhea (palaeognathous); B, duck Anas (desmognathous); C. fowl Gallus (schizognathous); D, crow Corvus (aegithognathous). In A the contact between pterygoid and vomer is on the dorsal surface of the palate. (A.d'A. Bellairs). bp, basipterygoid process; eu. opening of Eustachian tubes; f. facet for pterygoid on rostrum; mxp. maxillopalatine; pal. palatine; pbs. parasphenoid and basisphenoid fused; pmx. premaxilla; pt. pterygoid; ros. rostrum of parasphenoid; quo quadrate; vo. vomer.

maxillopalatines, which mayor may not be fused or closely approximated in the midline. The vomers are usually fused into a single bone in the adult. On either side of these, and often separated by a gap on each side, are the palatines; behind these are the pterygoids, articulating posteriorly with the quadrates. The internal nares lie between the palatines, the vomers and the maxillopalatines; but in kiwis Apteryx spp., where the palate is exceptionally complete, the internal nares are bordered by the palatines and vomers only, which approximate in front of the choanal opening. Deeply placed in the midline of the palate is the rostrum of the parasphenoid. Posteriorly this bone widens out and is fused with the lower surface of the basisphenoid. The usually common opening of the Eustachian tubes (Tubae pharyngotympanicae) can be seen at the base of the rostrum. In many birds the pterygoids articulate with the parasphenoid rostrum by means of movable joints. Movements of the quadrates are transmitted through the pterygoids and palatines to the BILL, which is thus raised or lowered (kinesis; see SKULL). Taxonomic significance. Since T.H. Huxley's work (1867), the structure of the bony palate has been used as a basis for classifying birds into major groups. The following types of palate have been distinguished: 1. Palaeognathous, or dromaeognathous, characteristic of 'ratite' birds and tinamous (Fig. lA). Vomers large and imperfectly fused, articulating anteriorly with the premaxillae and the maxillopalatines and posteriorly with the palatines and pterygoids (except for Struthio). Pterygoids in contact with the palatines along an unmovable suture and separating

these from the para sphenoid rostrum. Well-developed basipterygoid processes set well back on parasphenoid. Complex pterygoid-quadrate articulation, involving the orbital process of the quadrate. 2. Neognathous, characteristic of carinate birds. Vomers often small and completely fused, sometimes absent. Palatines and pterygoids usually in contact with parasphenoid rostrum, and articulating with each other at a movable joint. Typical basipterygoid processes usually absent, but often replaced by facets on rostrum farther forwards (Fig. IB). Neognathous palates have been further subdivided as follows: (i) Desmognathous (Fig. IB), as in Anseriformes, Pelecaniformes, Psittaciformes, most Accipitriformes and Falconiformes, Strigiformes, and some other groups. Vomers small and tapering. Maxillopalatines broad and meeting each other or the vomers in the midline. (ii) Schizognathous (Fig. lC), as in Columbiformes, Galliformes, Sphenisciformes, Charadriiformes, and others. Vomers tapering in front. Maxillopalatines not meeting each other or vomers in midline, so that there is an extensive longitudinal cleft in the bony palate. The palate of woodpeckers (Picidae), to which the term saurognathous was applied to cover the (erroneously supposed) condition of paired and separated vomers is not distinguishable from the schizognathous condition (de Beer 1937). (iii) Aegithognathous (Fig. ID), as in Passeriformes and a few other groups such as swifts (Apodidae) and night jars (Caprimulgidae). Maxillopalatines separated, fused vomers truncated and broad in front, and forked behind, embracing the parasphenoid rostrum. Today the taxonomic value of the different bony palate patterns is open to question. The various subdivisions of the neognathous condition partly merge into one another, and while these palatal types may be of value as a guide to the systematics of the smaller groups, they do not provide a reliable basis for major group classification. McDowell (1948) denies that the distinction between the palaeognathous and neognathous types may be upheld any longer. Several authors have pointed out that during embryonic development some neognathous birds show an arrangement similar to the palaeognathous condition, with the pterygoid extending forward so as to articulate with the vomers. Later the front end of the pterygoids becomes detached from the rest as the 'hemipterygoid' and fuses with the palatine. Consequently the criterion of a palatine separating the vomer from the pterygoid, formerly thought to be characteristic of neognaths, is in some cases illusory. The similarity in the embryonic arrangement of some neognathous birds may be interpreted as a recapitulation of an ancestral stage, or the palaeognathous palate in the ratites may be a neotenic structure, comparable to other features thought to be neotenic in these birds (see EARLY EVOLUTION OF BIRDS).

Fossil evidence adds no light to the problem. Archaeopteryx is claimed to be neognathous (schizognathous). The reconstruction of the skull of H esperornis by Gingerich suggests a somewhat similar arrangement of the bony palate as in the palaeognaths, yet the vomer does not articulate with the pterygoid, and there is not the complex pterygoid-quadrate articulation. In contrast with McDowell, Bock (1963) has clearly shown that in palaeognaths there is indeed a common morphological pattern and that

. . . . .- -a

....,.....~

f

Fig. 2. View of the horny palate of Fringilla coelebs (A) and Passerina ciris (B). a. abutment; f. furrow.

Pale arctic Region

the palaeognathous palate can be defined by the criteria mentioned above. He stresses its function in transmitting great forces for rhynchokinetic movements of the bill. Thus, the palaeognathous palate may indeed be of crucial importance for understanding of ratite evolution and relationship. Horny palate. Apart from the bony palate there is a horny palate (Fig. 2) on the inner side of the rhamphotheca which covers the upper mandible. Normally this horny palate is a simple vault, but in several dietary specialists such as birds which remove the husks from the seeds before swallowing them (e.g. the granivorous songbirds and the parrots), the horny palate is highly structured with a characteristic system of furrows and longitudinal or cross tuberosities. The furrows lodge the seeds when they are cut open, the tuberosities serve as an abutment when the seeds are pressed off (Ziswiler 1965). In the granivorous songbirds and the parrots (Hornberger 1980) the structure of the horny palate is species-typical and therefore of considerable taxonomic importance. (A.d'A.B.) V.Z. Bock, W.J. 1963. The cranial evidence for ratite affinities. Proc. XIII Int. Orn. Congr. Ithaca: 39-54. de Beer, G. 1937. Development of the Vertebrate Skull. London. (See p. 445.) Gingerich, P.D. 1973. Skull of Hesperornis and early evolution of birds. Nature 243: 70-73. Hornberger, D.G. & Ziswiler, V. 1972. Funktionell-morphologische Untersuchungen am Schnabel con Papageien. Rev. Suisse Zool. 79: 1038-1048. Hornberger, D.G. 1980. Funktionell-morphologische Untersuchungen zur Radiation der Ernahrungs- und Trinkmethoden der Papageien. Bonner Zool. Monogr. 13. McDowell, S. 1948. The bony palate of birds. Part I. The Palaeognathae. Auk 65: 520-549. Ziswiler, V. 1965. Zur Kenntnis des Samenoffnens und der Struktur des hornernen Gaumens bei kornerfressenden Oscines, J.f. Orn. 106: 1-48.

PALATINE: a paired bone of the

SKULL.

PALEARCTIC REGION: or 'Palaearctis', name of zoogeographical region proposed by Philip L. Sclater (1858) (see DISTRIBUTION, GEOGRAPHICAL), comprising the whole of Europe, Africa north of the Sahara, and arctic, boreal and temperate Asia north of the Himalayas. The concept of a 'Holarctic Region' for all cold and temperate land masses of Eurasia and North America was introduced by Alfred Newton and followed widely, reducing the Palearctic and Nearctic (cold and temperate New World) to the rank of subregions. In spite of this, for the sake of convenience the term Region is still generally used. In zoogeography the stress has shifted from the static concept of a 'region' with fixed boundaries to the dynamic and more realistic state of a 'fauna'. Features and boundaries. The main physical features of the Palearctic Region are a basically circumpolar arctic or tundra Zone, a virtually continuous belt of boreal, mainly coniferous woodland known as the taiga from Norway to eastern Siberia, an almost continuous chain of mountains from the Pyrenees, Alps, Carpathians, Caucasus, Elburz, to the Himalayas, and an almost continuous belt of desert from Morocco to Sinai, Arabia, Iran, Turkmenistan, Uzbekistan, Tibet, and Gobi. These features and their histories during the Pleistocene ice-age have exercised a profound influence on bird-life and its distribution. The boundaries of the Palearctic Region are broadly defined in the west, north and east by the Atlantic, Arctic, and Pacific Oceans, separating it from the Nearctic. But in the south there is no clearly defined boundary with either the Afrotropical or the Oriental Regions. Greenland, although geographically part of North America, is, on the evidence of plants, insects, and birds, biologically part of the Palearctic, probably in consequence of the ice-free condition of the arctic deserts in north-eastern Canada at least during the last glacial period and the amount of sea-ice in the North Atlantic in the post-glacial. Only 5 Nearctic species out of 55 have established themselves in Greenland as regular breeding birds, whilst 3 species have reached Iceland (Great Northern Diver Gasna immer, Harlequin Duck Histrionicus histrionicus, Barrow's Goldeneye Bucephala islandica). The Atlantic has been an efficient barrier to avian dispersal. It is remarkable that no purely Palearctic passerine species has reached North America within the memory of man, save perhaps the Wheatear Oenanthe oenanthe in north-eastern Canada, whilst but a single non-passerine-the Cattle Egret Bubulcus ibis has recently established itself in the New World by crossing the Atlantic. In addition, the Black-headed Gull Larus ridibundus and the Lesser Black-backed Gull L. Juscus are busy estab-

429

lishing a foot-hold in eastern North America (via Iceland). Despite the hundreds of North American birds blown across the Atlantic or assisted by ships every year, not one species has yet established itself in Europe, though the Spotted Sandpiper Actitis macularia and Wilson's Phalarope P halaropus tricolor have recently made an attempt. In southern Europe the Mediterranean has been a less efficient barrier to dispersal than the Sahara. The northern and central Sahara are still predominantly Palearctic; but at both ends we find Palearctic species seeping down (e.g, Spoonbill Platalea leucorodia in the west and east, and Little Owl Athene noctua in the east) and Afrotropical species seeping up-some along the coast of Morocco and spreading east to Tunisia and even to Spain, e.g. the Little Buttonquail or Andalusian Hemipode Tumix sylvatica and the Crested Coot Fulica cristata, and several up the Nile Valley and into Lower Egypt and the Jordan Valley, e.g. the Palestine Sunbird Nectariniaosea. The bird faunas of the Canary Islands, Madeira, and the Azores are definitely Palearctic; so is the majority of the birds of the Cape Verde Islands. Sinai is pure Palearctic. In Arabia many Palearctic forms reach the Yemen, as do a few Oriental forms across southern Arabia. At present, mountainous south-west Arabia is included by most biogeographers in the Afrotropical Region. In south-west Asia there are two remarkable cases of interrupted distribution, both Oriental kingfishers-the Whitebreasted Kingfisher Halcyon smyrnensis reaching westernmost Asia Minor and probably even south-eastern Europe, and the White-collared Kingfisher H. chloris reaching the southern Red Sea (outside the confines of the Palearctic), the latter's nearest relative being 3,200 km distant in India. The avifaunas of the Persian Gulf and Iran are predominantly Palearctic with slight Afrotropical and Oriental elements; but farther east we find a more exact boundary between the Palearctic and the Oriental regions in the mountains of northern Baluchistan, the Afghan-Pakistan frontier, and then east along the higher levels of the Himalayas and into China about Szechuan and Hupeh, where the Yangtsekiang is usually considered a faunal boundary, but where in fact there is a large transition zone. North of the Hwang-ho the fauna is definitely Palearctic, as are those of Korea and Japan. In Kamtschatka we find a close relationship with northern Alaskan birds. The narrow Bering Strait, which was land during each of the glacial periods, hardly acts as an efficient barrier for birds. Several Nearctic species have spread to eastern Siberia, e.g. the Grey-cheeked Thrush Catharus minimus, and some true Palearctic species have spread to Alaska, e.g. the Yellow Wagtail Motacillaflaua, Wheatear and Arctic Warbler Phylloscopus borealis, while the Dotterel Charadrius morinellus has occasionally bred there. Effects of Pleistocene glaciations. A large part of the north-western Palearctic has been subjected to arctic and sub-arctic conditions during the series of at least four alternating Pleistocene glaciations, which terminated some 10,000 years ago after persisting for almost 2,000,000 years. In fact, the present climatic condition of the Holarctic can be described as a post-glacial or even as a recent inter-glacial period. However, only small areas of the Palearctic were actually covered by ice-caps involving the complete extermination of bird-life. These included the whole of north-west Europe south to the British Isles, the Netherlands, the southern shores of the Baltic, central Russia, north-east to the Taimyr Peninsula, but not central and east Asia. (See also GEOLOGICAL FACTORS). There were minor ice-caps in the Atlas, Pyrenees, Alps, Himalayas, and mountains of north-east Asia. But even in glaciated regions small pockets of unglaciated land persisted as they do today in Greenland. Far the greater part of the Palearctic Region was ice-free, though tundra and wind-swept cold deserts reigned in extensive peri-glacial areas. Warmer climates and more luxuriant vegetation prevailed, particularly in the east and south-east. In the western Palearctic all climatic vegetation zones were shifted south by a few thousand kilometres. Notably arboreal and forest birds were forced east, south-east and south, and this phenomenon has its counterpart in the post-glacial general return (expansion) westwards, north-westwards and northwards, continuing even today. During the last 100 years more than 28 Eurasiatic species have extended their range westwards and north-westwards, following the retreat of the Fenno-Scandinavian ice-cap and the surrounding tundra and steppes, the most spectacular extensions being those of the Grey-headed Woodpecker Picus canus, Greenish Warbler Phylloscopus trochiloides, and Scarlet Rosefinch Carpodacus erythrinus.

430

Pale arctic Region

There are 66 species of birds breeding regularly in Britain that do not do so regularly in Ireland; the Magpie Pica pica reached Ireland only in 1676, the Stock Dove Columba oenas as recently as 1877, and the Black-necked Grebe in 1906 (but no longer breeds there). Glaciation was the major influence in transforming many continuous into discontinuous distributions. Today we find the Blue or Azurewinged Magpie Cyanopicus cyanus in south-west Spain and again in China and Japan, the Twite Carduelisflavirostris in north-west Europe and again in the Caucasus and central Asian highlands; the Marsh Tit Parus palustris has two disjunct ranges in Europe and east Asia, the White Stork Ciconia ciconia has three disjunct ranges, in Europe, Turkestan, and east Asia. Also it was almost certainly the effect of glaciation that drove the Magpie Pica pica into Yemen, and some Palearctic species into tropical Africa; they left behind isolated populations when conditions in Eurasia allowed them to spread once more into the northern areas where the bulk of their numbers are now found. Examples are the Chough Pyrrhocorax pyrrhocorax in the Ethiopian highlands and the Bittern Botaurus stellaris in southern Africa. Subdivisions. Bird-life in the Palearctic Region is by no means uniform; there are only 41 species in Korea that also breed in the British Isles; and there is still less uniformity among birds from Scandinavia and the eastern Himalayas. It may therefore be useful to suggest at least 7 zones of bird-life in the Palearctic Region, based on B. Stegmann's concept of faunal elements or faunal types. 1. Arctic Zone, with many circumpolar species, some of them extending south to the alpine levels of the European and Asian mountains, including the Tien Shan, but absent from the Himalayas and the Caucasus. The Ptarmigan Lagopus mutus, Snow Bunting Plectrophenax nivalis and numerous waders and waterfowl are typical of this zone. By its circumpolar nature and extreme climatic conditions the Arctic Zone is sometimes considered an independent Region or Sub-region. The Arctic Zone includes a more arid and colder high arctic and a moister and less extreme cold low arctic zone; characteristic species are Brent Goose Branta bernicla, King Eider Somateria spectabilis, Glaucous Gull Larus hyperboreus (part-arctic), Knot C alidris canutus, Sanderling C alidris alba (high arctic), Steller's Eider Polysticta stelleri, Bewick's Swan Cygnus columbianus bewickii (low arctic). The Arctic may include a sub-arctic zone, which is sometimes considered to have its own, independently derived vegetation and fauna. It is the zone of the low birch forest with fascinating tortured stems; characteristic species are Lesser Whitefronted Goose Anser erythropus, Red-breasted Goose Branta ruficollis, Spotted Redshank Tringa erythropus, Pechora Pipit Anthus gustavi. 2. Siberian Zone, characterized by boreal coniferous forest, known as taiga, occupying a continuous belt from eastern Siberian into Scandinavia, with a gradual reduction of the number of species from east to west. Again there are isolated pockets of a Siberian fauna, including the Capercaillie Tetrao urogallus and the Nutcracker Nucifraga caryocatactes, in the sub-alpine zones of mountain ranges in Asia and Europe, such as the Alps and the Pyrenees. The Hawk Owl Surnia ulula, Siberian Jay Perisoreus infaustus, Redwing Turdus iliacus, and Brambling Fringilla montifringilla are typical species of the Siberian Zone. 3. European Zone of deciduous forests, narrowing to the southern Urals. A few species typical of this zone extend to Scandinavia, southwest Siberia, and recently even as far east as Baikal. Characteristic species are the Green Woodpecker Picus viridis, Robin Erithacus rubecula, Song Thrush Turdus philomelos, and Chaffinch Fringilla coelebs. The oak forests of North Africa and the mixed deciduous forests of the Caucasus and Turkestan contain others, such as the Jay Garrulusglandarius, several species of tit Parus, nuthatch Sitta, treecreeper Certhia, and thrush Turdus. 4. Mediterranean Zone, typified by xerophilous shrubs, steppe and semi-desert, and extending through most of lowland southern Europe, North Africa and south-west Asia to Iran and Afghanistan, with a few species extending north to southern England (Dartford Warbler Sylvia undata), central Europe and the steppes of southern Russia. The Cream-coloured Courser Cursorius cursor, bustards Otis and Chlamydotis, and many species of larks Melanocorypha, Calandrella, and warblers Sylvia are typical of the Mediterranean Zone. 5. Old World Desert or Eremian Zone, including the high Mongolian and low Turkestanian deserts, those of Iran and the Near East, with northern Arabia and Sinai, extending into Asia Minor and the northern half of the Sahara. Typical of this zone are sand partridges Ammoperdix, ground jays Podoces, various species of larks Ammomanes, Alaemon,

Ramphocorys, wheatears Oenanthe, rock nuthatches Sitta, and the Trumpeter Finch Bucanetes githagineus. In the south-west of this zone there are many infiltrations from the Afrotropical Region, such as the Ostrich Struthio camelus in north Arabia and north-west Africa until quite recently, and several species of sandgrouse Pterocles. 6. Tibetan Zone, including the northern slopes of the high Himalayas. With the probable exception of the boreal forest zone there is no other continental area of the size of Tibet with such a distinct fauna. Typical are the Snow Partridge Lerwa lerwa, snowcocks Tetraogallus, Blue Grandala Grandala coelicolor, and various species of rosefinches Carpodacus and snowfinches Montifringilla; only the latter are restricted to the Tibetan highlands, the others include also Sino-Himalayan species, of which there are many. 7. Chinese Zone typified by the mixed broad-leaved forests of east Asia prevailing in southern Manchuria, Korea, Japan, and China and extending in the Himalayas as far as Kashmir and the Pamirs. Both the flora and the fauna of this area have maintained a high degree of diversity dating from pre-glacial times. The bird-life includes numerous forms and species that have died out in other parts of the Palearctic through the influence of the Pleistocene glaciations. Typical of the Chinese Zone are many species of pheasants Ithaginis, Pucrasia, Lophophorus, Crossoptilon, Syrmaticus, Chrysolophus and laughing thrushes Garrulax and Pomatorhinus. Comparison with other regions. In size the Palearctic is roughly one and a half times as large as the Nearctic (c. 34 million km 2 against c. 21). However, computed per million krrr", the numbers of species occurring in these regions are almost alike, viz. c. 30 and 35, respectively. Compared with other continents and regions the numbers are low, as there are 85 species per million km 2 in the Afrotropical Region and up to 135 in South America (R.E. Moreau). These numbers may roughly indicate the relative diversity of ecological niches available, which is more restricted in the less hospitable temperate and cold areas than in the-for birds-more friendly humid tropics. Of non-passerine species c. 443 occur in the Palearctic Region; of these 102 occur also in the Nearctic, 112 in the Afrotropical, and 105 in the Oriental Regions. Of passerine species c. 500 occur in the Palearctic Region; of these 16 occur also in the Nearctic, 30 in the Afrotropical, and 101 in the Oriental Regions. There are 194 genera of non-passerine birds and 135 of passerine birds occurring regularly in the Palearctic Region. In the Nearctic Region these numbers are 180 and Ill, respectively. Characteristic forms. If we omit infiltrations from other regions, the Palearctic is more easily characterized by what it has not than by what it has; this applies particularly to its western half in which the devastating influence of the Pleistocene glaciations has been most severe. If we take the buntings Emberiza, we find 9 species in western Europe and 19 in Eastern Asia. We have 5 flycatchers F icedula and M uscicapa in Europe and 14 in Palearctic Asia. On the other hand, of the 16 species of warblers Sylvia breeding in Europe and south-western Asia, not one occurs east of the Yenesei or in Japan; of the 6 species of Phylloscopus this number is, however, 4. Still, the Palearctic has 71 genera peculiar to it, and of these 27 are non-passerine (e.g. pheasant Phasianus, ruff Philomachus) and 44 passerine (e.g. crested lark Galerida, redstart Phoenicurus, long-tailed tit Aegithalos, wall creeper Tichodroma, chaffinch Fringilla). A few groups require especial mention. Of the kingfishers (Alcedinidae) there are c. 87 species in the world and of parrots and parakeets (Psittacidae) c. 340; of these only 7 and 1, respectively, occur in the Palearctic, and 2 and 2 respectively, in the Nearctic. Among the larks (Alaudidae) only one species (Horned or Shore Lark Eremophilaalpestris) occurs in the Nearctic, 24 in the Palearctic, and 49 in the Afrotropical Region. In the pipits and wagtails (Motacillidae) there are 5 species of wagtail Motacilla in the Palearctic, 3 in the Afrotropical Region, and only one, a geologically recent arrival, Yellow Wagtail M. fiava in the Nearctic. There are 13 species of pipit Anthus in the Palearctic, 11 in the Afrotropical Region, and only 2 regularly in the Nearctic. The accentors (Prunellidae) with 13 species are virtually endemic to the Palearctic Region; none of them occurs in the Nearctic and only one marginally (Yemen, Arabia) in the Afrotropical Region. The Horned Lark and Raven Corvus corax are noteworthy examples of truly Holarctic distributions: both species encompass the globe in its Northern Hemisphere, both extend from the Arctic to the tropics, and both breed from 5,500 m to below sea level. Few birds have become extinct in the Palearctic in recent times.

Paralectotype 431

Notable examples are Pallas' Cormorant Phalaeroeorax perspicillatus, Great Auk Pinguinus impennis, a thrush Cichlopasser terrestris and a grosbeak Chaunoproetus ferreorostris from the Bonin Islands, Japan. (R.M.) K.H.V. Bruun, B. & Singer, A. 1978 (revised edn.). The Hamlyn Guide to Birds of Britain and Europe. London. Cheng Tso Hsin. 1973. A Distribution List of Chinese Birds. Peiping. Cramp, S. et al1977- . Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Palearctic. Oxford. Etchecopar, R.D. & Hue, F. 1978. Les Oiseaux de Chine. Non-passereaux. Papeete. Etchecopar, R.D. & Hue, F. 1983. Les Oiseaux de Chine. Passereaux. Paris. Flint, V.E., Boehme, R.L., Kostin, Y.V. & Kuznetsov;A.A. 1983. A Field Guide to the Birds of the USSR. Princeton. Gallagher, M. & Woodcock, M.W. 1980. The Birds of Oman. London. Glutz von Blotzheim, U.N., Bauer, K.M. & Bezzel, E. 1966- . Handbuch der Vogel Mitteleuropas. Harrison, Colin. 1982. An Atlas of the Birds of the Western Palaearctic, London. Heinzel, H., Fitter, R. & Parslow, J. 1979 (revised edn.). The Birds of Britain and Europe with North Africa and the Middle East. London. Il'ichev, V.D. & Flint, V.E. 1982. Birds of the USSR. Moscow [In Russian]. Massey, j.A. et al1982. A Field Guide to the Birds of japan. Tokyo. Meyer de Schauensee, R. 1984. The Birds of China. Oxford. Peterson, R., Mountfort, G. & Hollom, P.A.D. 1983 (4th edn.). A Field Guide to the Birds of Britain and Europe. London. Vaurie, C. 1959. The Birds of the Palearctic Fauna. Order Passeriformes. London. Vaurie, C. 1965. The Birds of the Palearctic Fauna. Non-Passeriformes. London. Vaurie, C. 1972. Tibet and its Birds. London. Voous, K.H. 1960. Atlas of European Birds. Edinburgh. (Atlas van de Europese Vogels. Amsterdam, 1960.)

PALILA: Loxioides bailleui, one of the

HAWAIIAN HONEYCREEPERS.

PALLIUM: the mantle (see TOPOGRAPHY). PALMAR: pertaining to the ventral surface of the manus, or sometimes

of the whole wing.

PALMATE: having three toes connected by webs (see LEG). PALMCHAT: Dulus dominicus, sole member of the Dulidae (Passeriformes, suborder Oscines), It is confined to Hispaniola, West Indies. Some investigators place it in the same family as the WAXWINGS (Bombycillidae) and their presumed relatives the SILKY FLYCATCHERS (Ptilogonatidae)-others prefer classification as a separate family, principally because of the 'communal' nests but also because of the harsher plumage, which lacks the silky quality and blended coloration of waxwings. The total length is about 18 em. The sexes are alike-greyish-olive (or brownish in worn plumage) above, and longitudinally striped with dark brown on a white base below. The head is darker than the back, the feathers having dark shafts; the rump is dark green. The tail is relatively long, the wings short and rounded, and the tenth primary rather long and thin, when compared with waxwings. Likewise the bill is stronger, more curved and compressed, and the nostril is exposed. The juvenile differs in having the throat and foreneck almost entirely dark brown, with only faintly paler edges, and a buffish rump. The species is locally abundant throughout the island of Hispaniola (comprising Haiti and the Dominican Republic) except in rain-forest and at higher altitudes. On nearby Gonave Island the birds are slightly more local in distribution. New nests are built, or old ones repaired or added to, during the spring months (March-June). These are usually large bulging structures-sometimes 1 m in diameter-of sticks and twigs, woven all about the smooth trunks of Royal Palms Roysumea and the bases of their fronds; when the fronds die, the nests fall. Pines are also used, but to a lesser extent, and nests built in them are smaller-used by one or two pairs. Likening such nests to a block of flats is perhaps more apt than the word 'communal'. Pairs occupy their own compartments, to which they alone have access by passages from the outside. Each nest is lined with fine grass and shredded bark, and here the eggs are laid. Nests with central chambers and passages have been described. About 4 eggs are to be found in a clutch; they are white, heavily spotted and blotched with dark purplish grey or with a ring of this colour at the large end. Berries (perhaps especially those of palms), as well as flowers of Cordia

Dulus dominicus. (M. W.)

and other plants, are known to be staple foods. The birds are sociable and gregarious, even drawing together on the tree-limbs when roosting. No song has been recorded, but rather a noisy chattering in chorus as well as a variety of more or less pleasing notes. (J.C.G. [r.) Greenway, j.C. Jr. 1960. Family Dulidae. In Mayr, E. & Greenway, I.C. Jr. (eds.). Check-list of Birds of the World vol. 9. Cambridge, Mass. Wetmore, A. & Swales, B.H. 1931. The birds of Haiti and the Dominican Republic. U.S. Natl. Mus. Bull. 155: 345-352.

PALMCREEPER: substantive name of Berlepschia rikeri, a South American furnariid strictly associated with Mauriita palms (for family see OVENBIRD (I».

PAMPA (PAMPAS): an environment of prairie type characteristic of southern South America (see PRAIRIE). PAMPRODACTYL: having all 4 toes directed forwards or (the first being movable) capable of being so directed (see LEG).

PANCREAS: an unpaired organ lying within the loop of the duodenum (see ALIMENTARY SYSTEM). In addition to secreting digestive juices into the duodenum, it secretes insulin internally, i.e. into the blood-stream (see ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM; NUTRITION). PANDIONIDAE: family of ACCIPITRIFORMES;

HAWK.

PANIC: in a special sense, a sudden wave of alarm that-often for no

reason apparent to the observer-spreads very quickly through a flock of birds (especially waders) or colony (especially gulls Laridae and terns Sternidae). The birds rise and fly off together, usually returning soon; also called a 'dread'.

PANTROPICAL: of widespread distribution in the tropical parts of the world (see DISTRIBUTION,

GEOGRAPHICAL).

PAPILLA, FEATHER: see FEATHER. PARADIGALLA: substantive name of the 2 species of PARADISE of the genus Paradigalla. PARADISAEIDAE: a family of the

Oscines;

PASSERIFORMES,

BIRDS-OF-

suborder

BIRD-OF-PARADISE.

PARADISE BIRD: see BIRD-OF-PARADISE. PARADISE-CROW: substantive name of Lycocorax pyrrhopterus (see BIRD-OF- PARADISE).

PARADOXORNITHINAE: see TIMALIIDAE;

PARROTBILL.

PARAKEET: substantive name of some smaller species of Psittacinae with long, pointed tails (see PARROT).

PARALECTOTYPE: see TYPE

SPECIMEN.

432

Parallelism

PARALLELISM : evolution in related stocks, producing similarity in ways which are not shown by the common ancestor, but derive from its genetic potential. Parallelism may in practice be difficult to distinguish from CONVERGENCE, which is never a sound basis for classification. PARAMO: term applied to an altitudinal zone in the Andes, just above the limit of trees . PARAPATRIC: occupying different but contiguous geographical areas . PARAPHYLETIC: of a single evolutionary ancestry, but not including all the descendents of the common ancestor (see MONOPHYLETIC ; POLYPHYLETIC) . The term is necessary only in CLADISTICS, in which a monophyletic group is further defined as one which does include all the descendants. PARASEMATIC: see under

SEMATIC.

PARASITE: an organism that lives at the expense, so to speak , of another species and commonly in or upon it , without reciprocal advantage to the host-and indeed often with disadvantage. Birds have many parasites (see ECTOPARASITE; ENDOPARASITE; also DISEASE). No bird is itself wholly parasitic . A few, however, are parasitic in respect of parental care (see BROOD-PARASITISM); others are in a sense parasitic, as distinct from predatory, in their feeding habits (see PIRACY) . True parasitism, in which the advantage is all on one side, is to be distinguished from associations that tend to be either neutral or mutually beneficial; thus, in 'commensalism' two species of organisms share the same food, while 'symbiosis' denotes a more intimate partnership (see NESTING ASSOCIATION ) .

PARASITISM: the exploitation by one organism of the resources of another. As a rule the relationship is between a more highly organized host and a less highly organized parasite; thus birds support many 'lower' parasites (see ECTOPARASITE; ENDOPARASITE ), but are rarely parasites themselve s. There are birds, such as skuas , which pirate the food catches of other birds (see PIRACY ), while some other species such as the Cut -throat Finch Amadina fasciata (Estrildidae) usurp the nearly completed nests of ploceids such as the Masked Weaver Ploceus uelatus, and a facultative parallel exists in the occupation of Black Woodpecker's Dryocopus marlius nest-holes by Jackdaws Corvus monedula, or the burrows in Prairie Dog colonies by the Burrowing Owl Alhene cunicularia. In south-east Asia some ploceids such as the Scaly-breasted Munia Lonchura punctulata , the javan Munia L. leucogastnoides or the Java Sparrow Padda oryzivora regularly breed (sometimes several pairs together) in the side-walls of large raptor nests such as those of the Changeable Hawk-eagle Spizaetus cirrhatus, the Grey-headed Fish-eagle Ichthyophaga ichthyaetus or the White-bellied Sea-eagle Haliaeetus leucogaster, often when these nests contain eggs or young (see NESTING ASSOCIATION). A much more highly developed form of exploitation is found in birds which lay their eggs in the nests of birds of other species, and have evolved special adaptations, morphological and behavioural, promoting the acceptance and survival of their eggs and young in the hosts ' nest (see BROOD-PARASITISM). PARASPHENOID: a paired bone of the PARASYMPATHETIC : see

PARENTAL ANTI-PREDATOR STRATEGIES: see

DISTRAC-

TION BEHAVIOUR; PARENTAL CARE .

PARENTAL CARE: the protection, feeding, and general care of young by one or both of the parents from the time of hatching to independence. For care of eggs see EGG; INCUBATION . The amount of parental care expended by adults depends strongly on the mode of development of the young (see GROWTH ) . At one extreme are the ALTRICIAL species whose young are born naked (or nearly so) and unable to leave the nest. They therefore depend completely on the adults for food, brooding and defence from predators until they develop to independence. At the other extreme are such fully PRECOCIAL species as the megapodes, whose young lead an independent existence from the moment of hatching. Between are a series of intermediate forms of various abilities in respect of locomotion and thermo-regulation, of food finding and acquisition and of predator avoidance. Hatching. Much of the hatching process is performed by the chick itself and the parents rarely assist . However, Eastern Bluebird Sialia sialis females have been seen to speed the hatching process by eating part of the shell and membranes of the pipping egg. Sanderlings Calidris alba, Stone-curlews Burhinus oedicnemus and other waders have also been recorded assisting hatching in this manner. Eggshell removal. The majority of birds remove or eat the eggshell after hatching. Only in large ground-nesting species with large and precocial broods e.g . geese, ducks, game-birds and in some of the terns , are the shells left on the nest which is itself soon abandoned by the family. In large tree-nesting species, e.g. herons , the shells may be dropped over the nest edge . Stouter-billed passerines may eat some or all of the shell but slender-billed species and most of the Charadriiformes carry them away. The young Flamingo Phoenicopterus ruber is fed fragments of its shell by the parent, probably to increase its calcium intake for skeletal growth. Eggshell disposal probably serves primarily as an anti-predator func-

SKULL ; PALATE.

NERVOUS SYSTEM.

PARATHYROID GLAND: see ENDOCRINOLOGY

AND THE REPRODUC-

TIVE SYSTEM.

PARATREPSlS : term for PARATYPE: see

DISTRACTION BEHAVIOUR .

TYPE SPECIMEN .

PARDALOTE: substantive name, alternatively 'diamond-bird' , of Pardalotus spp . (for family see FLOWERPECKER) . PARDALOTINAE : see

FLOWERPECKER .

Bittern Botauru s stel/aris removing eggshell from nest. (P hoto: E ]. Hosk ing).

Parental care

tion. Field experiments show that nests with empty eggshells alongside attract predators e.g . crows, more frequently than do nests withou t shells. Study of the factors eliciting eggshell removal by Black-headed Gulls Larus ridibundus shows that the behaviour is not as simple as it first appears; rather it is under close control of a series of responses to the characteristics of the hatched eggshell which together ensure that the parent neither attempts to remove the shell prematurely whilst the young bird is still hatching or is so wet as to be vulnerable to cannibalism by conspecifics, nor tardily, exposing the nest to unnecessary predation risks. Such predation risks are particularly high for many ground-nesting species with precocial young and in these species eggshell removal tendencies peak around the time of hatching. Predation risks are often lower for species with altricial young, either because the parents sit tightly on the nest (thus concealing the hatched eggshells), as in doves, or because the nest sites are relatively inaccessible, e.g . hirundines. Nevertheless, eggshell removal occurs in such species and the removal tendency increases through the laying cycle. One possibility is that hatched eggshells in such species may otherwise slip over and encase the eggs not yet hatched, thereby reducing hatching success: in one study of Barbary Doves Streptopelia risoria 5 of 24 shells not removed within an hour of hatching interfered with other eggs in this way. Nest sanitation. Disposal of the faeces by the parents, either by removing them or by swallowing them, is largely confined to the Passeriformes and the orders immediately related to them . The large broods of nidicolous young require a warm dry nest in the intere sts of hygiene and insulation and their vulnerability to predators requires distant disposal of excreta. In these species, therefore, the faeces are excreted within tough mucous sacs which can easily be carried away by the parent . Faeces are almost invariably produced only after feeding, the adult waiting for the nestling to lift its tail and produce the sac. The parent may prod the young bird near the vent to stimulate excretion . With very tiny young the sacs are immediately eaten by the adult, perhaps because digestion of ingested food is incomplete at this stage and the adult is tied to the nest by brooding requirements . With older young the sacs are carried away and disposed of. Passerines often wipe the material on to tree branches but some, such as swallows and martins, tend to drop them into water. Few go to the lengths of the female Lyrebird Menura novaehollandia which submerges the faeces in a nearby stream if she can and otherwise digs a hole and buries them . Young gulls and terns move away from the nest to defaecate but some tern species void their faeces around the nest where bird and substrate (e.g. sand dunes) are both white . As the nestlings age, sanitation practices change. Sacs may be deposited on the nest rim or, in a roofed nest , in the entrance hole and are carried away by the parent after a feeding visit. In hirundines and other species with inaccessible nests, the young vent their faeces over the nest edge, leading to mounds of sacs outside or on the ground below. Young Kingfishers Alcedo atthis likewise have considerable competence in ejecting liquid faeces through the entrance of their tunnel nest. Woodpeckers and horn bills may void the faeces on to the floor of the nesting cavity where they are absorbed in the litter, to be periodically cast out by the female or young and the litter renewed . Many of the larger species nesting in inaccessible sites, such as eagles, simply void their faeces in liquid form over the nest edge and do so from an early age. Some other species, notabl y the herons , have a nest of loose construction through which the liquid faeces fall. In hot climates this practice may be adaptive , the moist faeces falling on the twigs evaporating and keeping the nest cool. In broods of well-grown Blue Tits Parus caeruleus the faeces are also left in the nest ; perhaps because the water they contain helps cool the crowded nest. The young of some species are able to move from the nest although fed and cared for by their parents there, and some (e.g. Montagu's Harrier Circus pygargus, Night jar Caprimulgus europaeusi do so to defaecate. Brooding . Most young, altricial or precocial, are unable fully to regulate their body temperatures for some or many days after hatching (see GROWTH) and therefore require warming or brooding by the parents. Precocial young require only intermittent brooding but altricial young require almost constant brooding unt il their own temperature control develops. Figure I shows the typical pattern of brooding time in such species. Brooding frequency declines sooner in large than in small broods, because the large broods can conserve their body heat by huddling together. The brooding rhythm of the adults is not endogenously contro lled but

433

Fan-tailed Warbler Cisticola juncidis removing faecal sac from nest. (P hoto: E.] . H osking).

depends on stimuli from the young . When Pied Flycatchers Ficedula hypoleuca were experimentally replaced by older nestlings, brooding frequency decreased, whilst when the growing young were successively replaced with younger ones brooding was substantially prolonged .

100 -0

~80 o

e

.c QJ

.~

50

i ..

'0

~ 20

.. I I ••

5 10 15 20 Days after hatching

25

Fig. I. Variation in brooding attentiveness of Peregrine Falcon Falco peregrinus in relation to nestling age during typical Jun e-July weather. (Modified from Enderson et al 1972.)

434

Parental care

.-

-',.

. "

'.

,-

("

. ~

Doubled-banded Courser Cursorlus africanus defending egg. (P hoto: G .L . Maclean ).

Pr otection from the weather. Adult bird s normally shelter their young from rain, either by brooding them when small or by standing over them with spread wings when large . Pre cocial young may also seek shelter from their parents during rain . In prolonged rain the adult is unable to leave the young unattended and the chicks may suffer from starvation . In a few species , prin cipally the aerial insectivores e.g. swallows, swifts , the adults may themselves be forced by starvation to leave their young unattended. Such species usually have sheltered nests (roofed , in crevices or tunnels, etc.) and the young are exposed to chilling rather than to wetting. Such young may have considerable tolerance of low temperatures, becoming torpid until the adults return. The European Swift Apus apus can survive a week or more in thi s fashion, from an early age . Young birds have poorer physiological respon ses to overheating than to cooling and are dependent on their parents for shading during exposure to excessive insolation. Some heron s defaecate over their young in extremes of sunlight, the resulting evaporati ve heat losses serving to cool the young . Tropical seabirds, notably tern s, often dip to the sea surface to wet the breast feathers before sitting on the nest, thereby cooling eggs and young (see also BELLY- SOAKING) . Protection from predators . A very few species have young equipped to defend themselves against predators: the oil squirting of Fu lmar s Fulmaru s glacialis and other Procellariforme s, the odour gland s of Hoopoes Upupa epops and the massive talons of young eagles being examples. Most young depend on their parents for warning and protection . Most will crouch and 'freeze' on hearing a parental alarm call. Mobile young may run and hide in the surroundings and gull chicks, for example , have individual refuges in the vicinity of the nest . Occasionally, adults may remove the young from danger by leading or carr ying them to a safer site but their main tactics are to atta ck the predator directly or to attempt to distract it from the nest or young. Dire ct atta ck on the predator is particularly common in colonial nesting species and man y bird s may combine to haras s the int ruder by swooping and screaming at it and even striking it with beak or claws. More solitary species, notably Charadrii , may rely on DI STRACTI ON BEHAVIOUR in which the bird appears to have been injured or otherwise incapacitat ed and flutt ers about near the predat or but always just out of reach, un til it has led the enemy far enough from the young for safety, whereu pon it resume s its normal behav iour. Hole-nesting species are occasionally thr eatened on the nest and may use a 'hiss' display to deter the predator at the nest entrance. The behaviour apparently simulates a hissing snake either by vocal mean s (Wryneck Jynx torquillai or by wing movement s (various tits). Adult s disturbed on the nest may also adopt threatening postures and may att ack the intruder with bill and claws or with regur gitated (and evil-smelling) food or oil secretions (F ulmars; coucals Centropus spp.) During diveattacks, gulls and terns may defaecate on the intruder; and Fieldfares Turdu s pilaris are notab le exponents of thi s method of defenc e, their attacks sometimes leading to the death of the faeces-plastered victim . Parents may also carry the young away from danger. A variety of

Chinstrap Penguin Pygoscelis antarctica colony; Sheathbill C hionis alba eatin g penguin 's egg. (P hoto: N . R ankin)

waterfowl carry their young on their backs when swimming or with their beak s in flight , Woodcock S colopax rusticola carry their young between their legs and bod y whilst in flight , and other species car ry young using their feet (Red-tailed Hawk Buteo jamaicensis, Moorhen Gallinula chloropusy. The American Finfoot H eliornis fuli ca has special pocket s of skin under each wing in which to car ry its young whilst swimming or in flight. Other species can walk away from danger carrying their young in their beak (R allus spp .) or under their wings (African ja cana A ctophilornis africanusi . Feedi ng. Some young receive no pare ntal aid in food finding , the extreme being the megapode chick s which are fully independent from hatching. Amongst the more typical pre ococial species, however , the extent of pare nta l involvement varies substantially. Most du ck and shorebird (Charadrii) young are led to food sources but are left to feed them selves. Mute Swans Cygnus olor, however, will pull up submerged vegetation for their offspring and Quail Cotumix coturnix lead the ir young even to indiv idual food items; they may also make food available by scratching the ground . Yet another group of semi-precocial species proffer food to very young chicks; older chicks of the same species feed at food regurgitated by the parents on to the ground in front of them . Full y altri cial nestling s depend on their parents to deliver food into their open bills but semi-altricial raptor chicks can tear up and consume food brought to the nest after a peri od of fully altr icial feeding by their par ent s. Detail s of feeding behaviour are highly species-specific but a few broad generalizations are possible . Most parent bird s feed their young on the same foods as they eat themselves but reserve the larger pre y items for their young (except when feeding tiny young); they consume the smaller prey th emselves. Pre sumably thi s trend reflects the relative economics of prey size and transport-to-nest costs. For the same reason various large seabirds with remote feeding grounds return to their young with a single large meal , often in con junction with mate relief. Several seabird species feed their young by regurgitation of a thi ck stomach oil and doves and pigeons have evolved a similar ploy in the use of ' pigeon-milk' (see CROP MILK ) . In the se and in other species, regurgitated food conta ins an increasing proportion of solid material as the young grow . Feeding is most frequent in the early part of the day, pre sumabl y because the young are most hungry then after their overn ight fast. But bird s with unu suall y small bro ods have been noted to feed small young especially frequently in the middle and warmer part of the day, pre-

Parental care

Blackbird Turdus merula female feedin g young. (P hOIO: E.] . Hosking). sumably because they can then brood the young during the cooler morning s and evenings. The amount of food brought increases with the size of the brood but rarely proport ionatel y, so young in large brood s are frequently underweight and slower growing . This is apparently due to the inability of the parents to collect food fast enough over long period s: at one Great Tit Porus major nest studied , the parents of the over-large brood progre ssively 'tired' earlier each day as the nesting period progre ssed, collecting less food per unit time in late afterno on despite the greater food needs of their growing young . Young are generall y fed more frequently in cold weather , provided the food is available. This responds to the greater energy needs of the young . For other species cold weather results in reduced food availability and the parents may need to leave their young not only unfed but even un-brooded. In wet weather the general rule is to brood the young rather than to seek food for them. Water supply. Most nestlings obtain their entire water requirements from the moisture content of their foods though , in the case of Bullfinches Pyrrhula pyrrhula and other species feeding their young by regurgitation , the young may well receive additional water in the mucu s binding the food items together. Species breeding in hot areas, however, need large quantities of water for evaporati ve cooling and special behaviours have evolved to communicate these needs to the parents. Young Darters Anhinga melanogaster, for example, seek food by begging behaviours performed with the bill closed but seek water with the same behaviour performed after a feed and with the bill open ; in response to such solicitation the adults fly to nearby water and return to regurgitate water into their offsprings' bills. Most precocial young can travel to water but the Namaqua Sandgrouse Pterocles namaqua breed s in the Kalahari Desert 80 krn or more from water. The adult male possesses specially modified ventral feather s with which to transfer a net 10-20ml water from waterhole to chick over these distances. In this way the chick receives water over its 7 weeks of pre-flight life (see SANDGROUSE) . Care during nest departure. The extent to which the departure of the young from the nest receives parental care varies widely between species, from total absence in European Swifts to the elaborations of the 'water-call' and 'exodus call' of the Guillemot Un a aalge and Wood Du ck A ix sponsa respe ctively. Young Swifts depart from their nest without parental attention, often doing so in the absence of the adult , and this is a

435

Sand Martin Riparia npana feeding young at nest entrance. (P hoto:

B . Hu seby).

common pattern amongst altricial species. Generally, however , fledglings are tended by their paren ts for the first few days of life out side the nest. In many such species nest departure is not synchronous and the parents may seek to encourage tard y young to fledge by withholding food: in Bluebirds S ialia sialis feeding rates are markedly reduced in the last day in the nest and more so when one young has left the nest , though feeding is resumed once the brood has fledged and re-united. In some cases adult s seek to indu ce individual laggards to depart the nest by offering them food item s from just out side it. In other species , however , the male and female divide the brood between them , one adult attending the new fledglings, the other those remaining in the nest. Precocial young feed them selves to a large extent and the parents' major role is to warn and guard against predators once the brood has left the nest site after a short post-hat ching period . In such species there may be a premium on the brood departing together, particularly where the chick feeding grounds are some distance from the nest-site. The adults frequently possess a distin ctive nest exodu s call, soft in terre str ial nesters but loud and well-developed where the chicks mu st jump from the nest , as in the tree-holes of the Wood Duck or the cliff ledges of Guillemots. Following a per iod of about 24 hour s post-hat ching during which she repeatedly utters the exodu s call (thus familiar izing the young with her voice) the female Wood Duck reconnoitres the environs of the nest site and , if clear , summons the young from their cavity. Young Guillemots similarly leave their nest-ledges before developing full flight , descending on the 'lift ' of their secondaries, and are prone to gull predation once away from the ledge . Hence the chick s 'fledge' predominantly at dusk following a session of reciprocal 'water-calling'- a loud clear whistling call-between parent and young , culminating in resumed cont act between them on the sea below, the two swimming away through the dusk to offshore (and more gull-free ) water s by dawn . The descent of the chick may be accompanied by an adult flying down behind it, providing physical obstruc tion to aerial predation. Strength and duration of care. The du ration and int ensity of parental care are believed to repr esent a balance between ( 1) the reproductive potential of the parents on ceasing to tend the current young in favour of future broods and (2) their potential on continuing to invest further in the current attempt (giving the current young a better chance of surviving to reproduce). This has two consequences for the bird s. First, the ir willingne ss to pro vide care should increase through the nest

436 Parental ca re

Great Crested GrebeP odiceps cn status feeding fea ther to young on its back. (P h% : E.] . Hosking).

cycle since it will become increasingly difficult for them to get through a replacement cycle successfully. T hus, incubating eggs should be defended more vigorously than newly-laid eggs and hatc hed young should be defended more intens ely than eggs. Empi rical data testing these ideas are scarce but what are available suppor t the hypothesis. T he second conseq uence of the theory is that fledglings should be cared for by the parent s only whilst the return in repro ductive output by doing so exceeds the return obtained by investing the same care into a fresh breedin g attempt. In general term s this is the case, with species in which the young can qu ickly learn to forage for them selves having short periods of post-fledging care , as in small unspecialized passerines, whilst species with unu sual (or very specialized) feeding techn iques have long periods of post-fledging care. Terns have been found tend ing th eir British-born offspri ng whilst on their African winte ring grounds , thu s providing the young with the time and op portu nity to acquire specialized fish-catching techniques with adequate levels of skill before being left to forage independently. H owever , anoth er consequence of th is inclusive FITNESS theory of parent al care is that a period of conflict between parent and offspring as to the amount of care provided mu st arise, th e offspring seeking more than the parent should optimally provide. Empirical data support th is prediction for a variety of species. In a Bewick's Swan Cygnus columbianus stu dy, for exampl e, the pr oporti on of cygnet movement s going immediatel y unguard ed by the adult s increased from 52% to 87% over the first 4 weeks of cygnet life, even though the cygnets seek proximity to th eir parents for their protect ion d uring aggressive encounte rs. Parental care and clutch-size. Precocial species have, on average, larger clutches than altricial species and this difference is freq uent ly attri but ed to a supposed redu ction in the need for parental care for self-feeding chicks . H owever , parent al care in these species takes the form of guardin g against predators and this has to be attai ned over the foraging area of th e ind epend entl y hunting chicks. When pr ey densities are low the chicks mu st hunt over larger areas than can in practice be adeq uately protected by the adults, thu s limiting productive clutch size. For many arctic waders th e clutc h size is 4, suggesting some general limiting factor of this nature and, in one experiment al test of the idea, artificially increased brood sizes of Semi-palmated Sandpipers Calidris pusilla fledged fewer young th an did the natural broods of 4. Thus the provision of parent al care even in the form of chick guarding can in practice be limiting to clutch size in the same way as can parental care thr ough feeding (see also CLUTC H-SIZE). Creches . Chicks of several species normally spend part of their develop ment period in groups or 'creches' attended by a small num ber of adult bird s which may or may not include the parent s of the chicks present at the time . Th e behaviour was noted early in studies of penguins but also occurs in the 'crested' tern s, pelicans, flamin gos, and several waterfowl species, th ough the detailed features of the behaviour differ even with in these species group s.

Sandwich Tern Sterna sanduicensis feeding fledged juvenile. (P hoto:

D . H osking).

In some high latitude species the huddling together of the chicks into creches und oubtedly serves to conserve heat by redu cing the effective surface-to-volume ratio experienced by the chicks. But in the Eider Somatena mollissima and Shelduck Tadornatadorna the chicks are activelv guarded by th e accompan ying adults who are generally (perhaps always) successful breeder s. On the Ythan Estuary in Scotland marked Eider ducks averaged only 4 days with their brood in a creche before leaving to join adu lts feedin g elsewhere on the estuary. Th ese females have fasted to a substantial extent whilst incubating their clutches but the food they need to replenish their reserves--the edible mussel Mytilus edulis-is concent rated into parts of the estu ary remote from the centres for the invertebrates req uired by th eir young- the amp hipods Corophium spp. , a

Great Black-headed Gull L a TUS ichthy aetus male, female and young. (ph0/ 0: V . Si okhin).

Parrot 437

PARENTAL INVESTMENT: see PARIDAE: a family of the

PARENTAL CARE.

PASSERIfORMES,

PARIETAL: a paired bone of the

suborder Oscines;

TI T.

SKULL.

PAROTIA: substantive name sometimes used for the 4 species of

P arotia , usually known as six-wired BIRDS-Of-PARADISE.

PARRAKEET: see

House Sparrow P asser domesticus male feeding fledged juvenile. (P hoto: J .B. & S. B ottomley). gastropod mollusc Hydrobia sp. and a winkle Littorina sp . Hence the ducklings in the creches can be guarded only by the succession of females bringing their offspring to the brood -rearing areas over a period of time. Similar considerations have different conseq uences for local populations of Eiders on rocky (rather th an estuarine) coasts ; these do not form creches but their young feed on the gammarids and other small cru staceans present in the seaweeds whilst the females take mytilids and littorinids present on the rock surfaces to which the seaweeds are attached. Alternat ively, creching may have originated in normal parental caring at high brood densities. Broods then become mixed, either because both pairs of adult s are fighting in defending th eir broods, which then scatter, or because a chick of one brood wanders closer to a foreign brood than to its own parent s and joins the foreign brood when it is called togeth er by its parent s. Such mixing is most frequ ent when brood s are less than a week old. Yet another explanation may lie with th e adult s resorting to creching to share the costs of guarding young chicks among st several adult s: each adult can then spend a longer time feeding. See photos BELLY SOAKING; CARRYING; DISTRACTION BEHAVIOUR ; HEAT REGULATION. R.] .O'C. Koskimies, J.R. & Lahti, L. 1964. Cold-hardiness of the newly hatched young in relation to ecology and distribution in 10 species of European ducks. Auk 81: 281-307.

Skutch, A.F. 1976. Parent Birds and their Young. Austin. Protection of eggs. As a general rule , breeding bird s do not actively engage a pred ator-and thus put them selves at risk-unless it is relati vely safe for them to do so, or as a last resort (though even then not to the extent of losing life or limb ). Rath er , they leave the eggs or young to the safety of their own camouflage or to th at of the site as mu ch as possible. In waders pr ecaut ionary adaptations th at enhan ce the camouflage of the eggs include siting them against a disruptive background (e.g. among cattle droppings) or concealing them, partl y or completely, with nest debri s; also the adoption of inconspicuous rout ines at the nest and the speedy removal of egg-shells as each chick hatch es. The parents may also nest in loose association with other species that actively dem onstrat e, etc. against pred ators when breeding (see DISTRACTI ON BEHAVIOUR ) . If a predator appears, but does not imm ediately threaten the safety of the eggs or young, the att endant adult may react by flushing sooner or later (the timing being adaptably variable according to circumstances) or by adoptin g a concealing posture; it will depart furti vely if necessary-in some species (such as Kittlitz's Sand-plover Charadrius pecuarius) after first speedily covering the eggs or even newly hat ched chicks--and then remain inconspicuously in the general vicinity or depart entirel y. K .E .L.S. Hall, K.R.L. 1958. Observations on the nesting sites and nesting behaviour of the Kittlitz's Sandplover C haradn us pecuanu s, Ostrich 29: 113--125. Simmons, K.E.L. 1955. The nature of the predator-reactions of waders towards humans; with special reference to the role of the aggressive-, escape -, and brooding drives. Behaviour 8: 130--173. Tinbergen, N . et al 1963. Egg shell removal by the Black-headed Gull LaTUS nd ibundu s L.: a behaviour component of camouflage. Behaviour 19: 74-117.

PARAKEET.

PARROT : substantive name of most species of Psitta cidae , sole family of the order Psittaciformes; in the plural, general term for the family and order. Characteristics. Parrots share a number of character s which define the order: the upper mandible is strongly curved and fits over the shorter lower mandible ; a cere surrounds the base of the upper mandible which articulates with the SKULL; the lingu al and jaw musculature is highly developed and complex ; the tarsometatarsus is short, the zygodactyl foot is covered with granular scales; the feather tracts are sparse among prominent bare areas; the moult of the primaries starts in the centre ; the egg shell is white . There is a wide variation in size from a total length of c. 8.4 cm for the Buff-faced Pygmy Parrot Micropsitta pusio to c. lOOcm for the Hyacinth Macaw A nodorhynchus hyacinthinus. In general , the male is slightly larger than the female; the opposite is tru e for some A gapornis spp. The plumage generally is brightl y coloured, the prominent colour being most frequently green . Some species are less colourful, being mostly brownishgreen , grey, black , or white . Most species are sexually monomorphic; in the dim orph ic species the difference between the sexes varies from extreme, e.g. in E eiectus roratus to minimal, e.g. in the Budgerigar M elopsittacus undulatus. Th e juvenile is similar to the adult plumage, only somewhat duller; a distin ct juvenile plum age is found in the ring-necked parak eets (P sittacula spp .), th e Crimson Rosella P latycercus elegans; the Blue-crowned Lory Vi ni australis and others . Th e wings can be elongated and pointed , as in the Swift Parak eet L athamus discolor, or broad and rounded , as in the A mazona spp . Ta ils may be long and pointed or short and sq uarish. The central tail feathers are decorou sly elongated in the Papu an Lory Charmosyna papou; in the racket-ta iled parrots (P rioniturus spp.) the y extend beyond the tip of the tail as bare shafts terminating in spatules. Stiff shafts pr oject from the tip of the tail feathers in the pygmy parrots (M icropsitta spp .) and Nes tor spp. Th e crown feather s are elongat ed and form movable crests in cockatoos. Some lorikeets (V ini spp .) can ruffle their crown feathers , whereas the elongated crown feathers of the Horned Parakeet Eunymphicus cornutus cannot be moved . Elongated hind neck feather s are found in the Collared Lory Phigys solitarius and Hawk-headed Parrot Deroptius accipitrinus. The head is bare and covered only with bristles in the adults of Pesquet's Parr ot P sittrichas fulg idus and the Vulturine Parr ot Gypop sitta vulturina. Bristles are also found at the base of the bill of nocturnal parrots. Th e bill varies in length . It is very long and narrow in the Ne storinae , most Loriin ae, the hanging parr ots (L oriculus spp .), Pesquet's Parrot , the Long-bill ed Corella Caca tua tenuirostris, th e Red-capped Parrot Purpureicephalus spurius, the Slender-billed Conure E nicognathus leptorhynchus, the Tepui Parrotlet N annopsiuaca pany chlora, and Brot ogeris spp. Short bills are found in the black cockat oos (C alyptorhy nchus spp. ), the pygmy parrots and P oicephalu s spp ., most broad-tailed parrots (Platycercini), Ara spp ., and B olborhynchus spp . The Palm Cockatoo Pr obosciger aterrimus, Great-billed Parr ot Tany gnathus megalorhyn chus and Hyacinth Macaw are known for their dispr oporti onately large bills. The tongue is broad and fleshy. In pollen and nectar feeders, the tongue is elongated and bear s epidermal papill ae at the tip , e.g. in the lories, the Swift Parakeet , and the Philippin e Han ging Parr ot L oriculus philippensis. Most parr ots have a well developed crop and a mu scular gizzard. Both organs are redu ced in pollen-ne ctar and fru it specialists. Habitat. Parrots are found mainly in tropical regions but also in temperate zones. They are especially plentiful in lowland trop ical forests. Some have conq uered mountainous regions, e.g. the Derbyan Parakeet P siuacula derbyana in Tibet , or the Kea Nes tor notabilis. Others inhabit more open country, mostly keeping close to waterholes and water courses in arid regions. A few species live on the sea shore, e.g. the Rock Parakeet Ne ophema petrophila, some subspecies of the Red -fronted Parakeet Cy anoramphus nova ezelandiae. Three species are terrestr ial, the

438

Parrot

Kak~po Stngops h~broptilus, the Australian Ground Parrot Pezoporus uiallicus, and the NIght Parrot Geopsittacus occidentalis.

Distribution. Parrots are found around the world, mainly in the Southern Hemisphere, i.e. Australasia, Pacific Islands, Africa, South and Centr~l ~me~ica, ~nd the Caribbean Islands. The northernmost point of the distribution IS reached by the Slaty-headed Parakeet Psittacula himalayana in Afghanistan, the southernmost point by the Austral Conure Enicognathus ferrugineus in Tierra del Fuego. The easternmost island of the Pacific, Henderson Island, is reached by Stephen's Lory V ini stepheni.

Movements. Most parrots are more or less sedentary, except for daily local movements between roosting and feeding places. Nomadic behaviour. is especially co~mon among inhabitants of arid regions, e.g. the Budgengar and Cockatiel Nymphicus hollandicus. A few cases of seasonal migratory behaviour are known, e.g. the Swift Parakeet and the Orangebellied Parakeet Neophema chrysogaster. Food. The diet of parrots is mainly vegetarian and includes seeds nuts, berries, fruit, tubers, roots, nectar, pollen, insects, and lichens. Specializations on either food have often been evolved several times independently. However, all parrots (except Pesquet's Parrot) eat some seeds (or nuts) which they always husk before swallowing. Food is often held in the foot when feeding. B.ehaviour. Mo.st parrots are gregarious. Many species live in pairs dunng th~ breeding se~son. The social behaviour of parrots is very complex WIthplay behaviour, courtship and ritualized fighting. Mating is for life, and the pair bond is maintained (except in cockatoos) by mutual preening and partner feeding. The Kea is polygamous. Voice. Parrot calls are mostly screeching, loud, metallic, and unmelodic. High-pitched whistles are characteristic for the Loriinae. Many species emit chattering vocalizations. Some parrots have a soft almost melodic voice, e.g. the Purple-bellied Parrot Triclaria mala~hitacea, Bourke's Parakeet Neopsephotus bourkii. Vocal mimicry has been observed only in captivity. Breeding. Nesting generally takes place in hollow trees without litter material. Loriculus and Agapornis spp. build a nest within tree holes. The Monk Parakeet Myiopsitta monachus builds huge colonial twig nests in trees. The Rock Parakeet and the Patagonian Conure Cyanoliseus patagonus nest in cliffs. The Australian Ground Parrot nests in tufts of grass. Some species nest in termite nests, e.g. the Golden-shouldered Parrot Psephotus chrysopterygius, the Red-faced Lovebird Agapornis pullaria, and the pygmy parrots. Depending on the species, 2-5 eggs are laid on alternate days, incubation, usually (except in cockatoos) by the female only, starting with the second egg. The chicks hatch after 16-32 days. The hatchlings are blind, naked or have sparse down. They are fed and brooded by the female during the first 5-10 days; later the male assists in th.e care .of the young '. After leaving the nest, the young usually remain WIth their parents until the next breeding season. From early times parrots have been valued as pets because of their playfulness and mimicry of the human voice. In recent years, the lucrative pet trade has become, together with habitat destruction, a major threat to the survival of many species. Systematics. Relationships of the Psittaciformes to other orders are u?clear and hypothetical; most likely is a common ancestry with the pigeons, The first fossil parrot is known from the lower Miocene in France. The family comprises about 82 genera and 332 species. Eight subfamilies can be recognized. Nestorinae. The single genus Nestor is endemic to New Zealand and adjacent islands. The 2 species are large, stocky birds. The Kea inhabits sub-alpine regions, whereas the Kaka N. meridionalis inhabits forests. Strigopinae. The single species Stngops habroptilus is endemic to New Zealand. This heaviest parrot of all is flightless and nocturnal. The males display lek-behaviour (see LEK). The recent rediscovery of a small pOl?ula~ion on Stewart Island may save the Kakapo from imminent extmction. Psittrichadinae. The single species Psittrichas fulgidus is endemic to New Guinea and inhabits high elevations. Its diet consists of fruit. It is the only parrot not known to eat seeds or nuts. It drinks with a suction-pump action of the tongue. Cacatuinae. The cockatoos are found in Australia New Guinea and the islands adjacent to the Philippines. They are 'large birds w'ith a movable c.rest, ~ shor~ and high bill, and a narrow, stubby tongue. The plum~ge IS white, pink, grey, or black, with various red or yellow markings. They are specialized seed and nut eaters and drink by scooping

Rosy-faced Lovebird Agapornis roseicollis. (K.]. W.).

up water with their lower mandibles. The Cockatiel is much smaller than the rest of the group and has evolved in convergence to the broad-tailed parrots. Micropsittinae. The pygmy parrots are endemic to New Guinea and the a~jac~nt islands. These smallest of the parrots live in dense forests, climbing along the tree trunks. The bill resembles that of the cockatoos. The tarsometatarsus and the claws are long. Their food consists of lichens and, probably, insects. Loriinae. The lories are found on the Pacific Islands, Australia New Guinea and adjacent islands. They are medium-sized to small birds with extremely colourfull?lumage. They are pollen and nectar specialists, but eat also seeds and Insects, and drink by dipping their brush-tipped tongue into the liquid. Psittacinae. This group comprises 58 of the 82 parrot genera. It can be divided into 4 well-defined tribes, although the exact systematic position of some particular genera is not yet clear. The subfamily includes species of widely varying sizes, colours, appearances and feeding specializations. The group is characterized by a broad fleshy tongue with a spoon-shaped tip and by a drinking mechanism in which the tongue ladles water and swallows it by pushing the tongue against the palate. (1) Platycercini. The broad-tailed parrots are restricted to Australia, New Zealand, New Caledonia, and Fiji. The group consists mostly of seed-eaters, but includes also the pollen feeding Swift Parakeet and the frugivorous shining parrots (Prosopeia spp.) All species have long tails. (2) Psittaculini. This group has the most extensive distribution, from Australia to Africa. Size varies from the small Agapornis spp. to the large Eclectus sp. The appearance varies from stocky parrots with short tails to slim parakeets with extremely long tails. Most species have a coral-red bill. (3) Psittacini. This African group consists of only 2 genera. The Grey Parrot Psittacus erithacus is more frugivorous than the seed and nut specialist Poicephalus spp. to which the Senegal Parrot belongs. (4) Arini. This group is endemic to South America and comprises all Neotropical parrots (141 species of all 332 parrot species). Loriculinae. Previously thought to be closely related to the Agapornis spp., the hanging parrots form a distinct group with the single genus Loriculus. They are small, green birds with a brilliantly red rump. Most species are highly specialized fruit, pollen, and nectar feeders. They drink with a suction-pump action of the tongue. They often roost and rest during the day hanging upside down, hence their name. See photo NEST SITE SELECTION. D.G.H. Dilger, W.C. 1960. The comparative ethology of the African parrot genus Agapomis. Z. Tierpsychol. 17: 649-683. Forshaw.T.M. 1978. Parrots of the World (2nd ed.), Melbourne. Ho~berger, D.G. 1980. Funktionell-morphologische Untersuchungen zur Radianon der Ernahrungs-> und Trinkmethoden der Papageien (Psittaci). Bonn. Zool. Monogr., No. 13. Low, R. 1980. Parrots-Their Care and Breeding. Dorset. Smith, G.A. 1975. Systematics of parrots. Ibis 117: 18-68. Ulrich, S., Ziswiler, V. & Bregulla, H. 1972. Biologie und Ethologie des

Parthenogenesis

Schmalbindenloris, Trichoglossus haematodus massena Bonaparte. Zoo!' Garten N.F., Leipzig 42: 51-94.

PARROTBILL (1): substantive name of most of the species of the subfamily Paradoxornithinae of the Timaliidae (Passeriformes, suborder Oscines); in the plural, a general term for the subfamily (sometimes called Suthoras or Crow-Tits). Certain aspects of the biology of this subfamily, including features of behaviour and moult, have prompted consideration that familial rank might be justified. Characteristics. Parrotbills are small to medium-sized birds, ranging in total length from about 12-28 em. Although somewhat like the tits (Paridae) in general appearance, they are with two exceptions distinguished from other Oscine birds by the peculiarly formed (usually yellowish) bill, which is shorter than the head, very much compressed, and with strikingly convex outlines. The culmen is curved strongly for its entire length, the gonys ascends sharply, and the cutting edges of both mandibles are more or less distinctly sinuous. The nostrils are completely covered in bristles, and the legs and feet are robust, with strong toes and claws. The plumage is very soft and loose. Although numerous generic names have been proposed for the parrotbills on the basis of bill-shape, only 3, Paradoxornis, Panurus and Conostoma are currently accepted, the last 2 being monotypic. The Bearded Reedling or Bearded Tit Panurus biarmicus differs from the typical species in a number of particulars, e.g. in having a more normally shaped bill, in the sexes differing in plumage (with the juveniles resembling the female), and in laying larger clutches. The Great Parrotbill Conostoma oemodium, is much the largest of the subfamily, and has a bill intermediate in shape, though larger, between Panurus and Paradoxornis. The sexes in Paradoxornis and Conostoma are alike in plumage, the coloration ranging from the almost uniform greys and browns of the larger species to complex patterns featuring orange-buff, pinkishbrowns, and black and white. In most species the wings are short and rounded, but the tail is generally long and graduated. One species, the Three-toed Parrotbill Paradoxornis paradoxus, is remarkable among passerine birds in only having three toes, the outer one being a clawless stump attached to the middle toe. Habitat. Parrotbills are birds of dwarf bamboo, rhododendron, and the lower levels of either deciduous or evergreen forest, while many of the smaller species prefer tall grass and reeds. The Bearded Reedling and one Chinese species are confined to reedbeds. Distribution, populations and movements. The 19 species are essentially Sino-Himalayan birds, although several range widely in the Palearctic, and no less than 12 species extend into the mainland countries of south-east Asia, though not entering Malaysia. Amongst the typical parrotbills, the Vinous-throated P. webbianus is perhaps one of the most widely distributed, ranging in 7 races from Manchuria and Korea to Hainan and Burma. The Black-throated P. nipalensis, with 12 subspecies, ranges from Nepal to Taiwan and southwards into the Indo-

439

Chinese countries. On the other hand, one of the most restricted species is P. heudei, a very distinctive intermediate-sized form, which only occurs in the reedbeds bordering an 80 km reach of the Yangtze river in the Chinese province of Kiangsu. The rather aberrant Bearded Reedling, is wholly Palearctic, and ranges in areas of reedbeds from England eastward into Manchuria. Most species are resident, though there is some seasonal and altitudinal movement in the Himalayas, and the western populations at least of the Bearded Reedling have, in the last 30 years, developed a new dynamism characterized by now annual eruptive dispersal and the colonizing of new sites. Food. Insects are commonly taken, as well as vegetable matter such as shoots, buds, berries and seeds, the strong and unusually shaped bill of many species also being well adapted for stripping bamboo stems. Behaviour. All species are gregarious, and forage through tall grass or bamboo in small or large parties, keeping in touch with a continual twittering or cheeping. They fly reluctantly and rather feebly, but are quite agile and somewhat reminiscent of tits Paridae when foraging. Voice. Some of the larger species are quite noisy, with both harsh chattering notes and more musical calls, and at least 2, including the Bearded Reedling, have rather metallic ringing notes. Most species have a variety of cheeping or chittering notes, and another is described by Stuart Baker as 'like ... the plaintive bleating of a kid in distress.' Breeding. The breeding habits of some species and subspecies remain undescribed; much is still to be learnt of the lives of some of the uncommon parrotbills of remote areas. Those whose nidification has been studied build compact cup-shaped nests of grass and strips of bamboo, often thickly lined with finer grasses and sometimes bound with cobwebs. The nest is placed in reeds or grass or among bamboo stems within 2 m or so of the ground. The eggs number 2-4, and may be unspotted blue, or white to creamy or fulvous with speckling and blotching of reddish, greenish-grey or purplish. Both sexes of the Bearded Reedling incubate the clutch of 5-7 eggs for 12-13 days; and the young, fed by both parents, may leave the nest in 9-12 days. Two broods are usual. (H.G.D.) M.W. Ali, Salim & Ripley, S.D. 1971. Handbook of the Birds of India and Pakistan, vol. 6. Bombay. Baker, E.C.S. 1922. The Fauna of British India, 2nd edn. Birds, vol. 1. Deignan, H.G. 1964. Subfamily Panurinae. In Mayr, E. & Paynter, R.A.Jr. (eds.). Check-list of Birds of the World, vol. 10. King, B., Woodcock, M.W. & Dickinson, E.C. 1975. A Field Guide to the Birds of South-East Asia. London. Sharrock, }.T.R. 1976. The Atlas of Breeding Birds of Britain and Ireland. Berkhamsted.

PARROTBILL (2): term sometimes applied, in the plural, to the Psittirostriinae (for family see HAWAIIAN HONEYCREEPER). PARROT-FINCH: substantive name of Erythrura spp. (see ESTRILDID FINCH).

PARROTLET: substantive name of the Neotropical Forpus spp. (Psittacinae, Arini) (see PARROT). PARSON-BIRD: alternative name for the Tui Prosthemadura novaeseelandiae (see HONEYEATER) and in Trinidad for the tanager Tachyphonus rufus. PARTHENOGENESIS: production of a new individual from an egg not fertilized by a male gamete; from Greek parthenos meaning virgin and genesis meaning birth. In application parthenogenesis may be regarded as

Great Parrotbill Conostoma oemodium. (C.B. T.K.).

any mitotic activity in unfertilized eggs, or more conservatively, the development of a macroscopically detectable blastoderm. Parthenogenesis may result in at least two cytological forms. Generative parthenogenesis occurs in animal groups in which chromosomes of the egg are reduced (through meiosis). Individuals that are produced are thus haploid. Automictic parthenogenesis occurs in animal groups in which chromosomes are initially reduced but diploidy is ultimately restored. The hypothesized mechanism for this restoration is suppression or re-entry of the second polar body during the second phase of meiosis. Parthenogenesis appears to be relatively widespread in the animal kingdom. Using a definition of any mitotic activity in unfertilized eggs, parthenogenesis is probably very common. However production of viable offspring is much less common. Of all known cases 90% occur among invertebrate species.

440

Partial migrant

Among birds mitosis may be initiated in the unfertilized egg but organization of the blastoderm generally fails. Naturally occurring parthenogenesis is usually abortive. The only documented cases of production of offspring by parthenogenesis are from domestic varieties of the chicken Gallus gallus and the Turkey Meleagris gallopauo. Automictic parthenogenetic development has been observed in 1% of the unfertilized eggs of standard and cross breeds of chickens; the frequency among various strains of domestic turkeys averages approximately 10%. Selective breeding programmes have increased the frequency of parthenogenesis indicating a genetic basis for the phenomenon. The presence of viruses appears to increase the frequency of parthenogenesis. Fowl Pox, Rous Sarcoma and Newcastle DISEASE have all been shown to play an active role in parthenogenesis in turkeys. Vaccinations using live virus have proven more effective than the killed form. Vaccination/selection programmes have resulted in frequencies of parthenogenetic development approaching 50%. In most cases development is aborted and production of viable individuals is rare. Those that have hatched have been male and of those surviving to maturity only 20% have produced viable sperm. Parthenogenesis resulting in viable offspring in the wild has not been documented in birds. It is suspected in wild Turkeys because of its unusually high level in captivity. However, laboratory experience has shown that the parthenogenetically produced turkeys suffer from malposition in the egg and are generally less vigorous during pipping and hatching than normal young. In addition to poor hatchability, the birds show difficulties with locomotion and feeding during the early post-hatch phases. The probability of successful parthenogenetic production of offspring in the wild appears to be exceedingly low. W.F.P. Beatty, R.A. 1967. Parthenogenesis in vertebrates. In Metz, C.B. & Mulroy, A. (eds.). Fertilization: Comparative Morphology, Biochemistry and Immunology, vol. 1. New York. Olsen, M.W. 1975. Avian Parthenogenesis. US Department of Agriculture ARSNE 65.

PARTIAL MIGRANT: term applied to species of which, in a given breeding area, some individuals are migratory while others are not, e.g. Song Thrush Turdus philomelos in Britain. (see MIGRATION). PAR TRIDGE: substantive name of species of Phasianidae in several genera (Perdix, Ammoperdix, Alectoris, etc.); also the tree partridges Arborophila spp. etc, the Snow Partridge Leruia lenoa, and the bamboo partridges Bambusicola spp. etc. (see under PHEASANT). PARULA: substantive name of the 2 species of Parula (see

WARBLER

(2)).

PARULIDAE: a family of the

PASSERIFORMES,

suborder Oscines;

WARBLER (2).

PARVORDER: a taxonomic category which is a subdivision of an order, ranked between infraorder and superfamily. Used by McKenna (1975), Sibley and Ahlquist (in press). Seealso DNA AND PROTEINS ASSOURCES OF TAXONOMIC DATA.

McKenna, M.C. 1975. Toward a phylogenetic classification of the Mammalia. Pp. 21-46. In Luckett, W.P. & Szalay, F.S. (eds.). Phylogeny of the Primates. New York. Sibley, C.G. & Ahlquist, J.E. In press. The phylogeny and classification of the passerine birds, based on comparisons of the genetic material, DNA. Proc. XVIII Int. Orn. Congr. Ilyichev, V.D. (ed.). Moscow.

PASSAGE MIGRANT: term, alternatively 'transient', applied to birds from the viewpoint of an observer in an area that they pass through on migration without remaining throughout either the summer or the winter; 'bird of passage' is sometimes used as an equivalent but is applied poetically to any migrant (see MIGRATION). For 'passage hawk' see FALCONRY.

PASSERES: used both as an ordinal name synonymous with 'Passeriformes' and (less commonly) as a subordinal name synonymous with 'Oscines' (see below). It was the name used by Linnaeus for his sixth order of birds. PASSERIDAE: family of (1).

PASSERIFORMES,

suborder Oscines,

SPARROW

PASSERIFORMES: an order compnsmg 2 suborders (1) the 'Deutero-Oscines' (with 12 families; name introduced by Voous, Ibis 119 (1977): 224); treated by Feduccia as an order of its own, Tyranniformes, with an independent origin from Coraciiform ancestors, and (2) the 'Oscines' (with 70 families) (see TABLE OF CLASSIFICATION). The families of 'Deutero-Oscines' are often referred to collectively as the 'Suboscine Passeriformes', but the name 'Suboscines' more precisely denotes the Australian Atrichornithidae and Menuridae which have syringeal differences in comparison to the remaining Oscines. The name 'Clamatores' is used alternatively for the Tyranni (but earlier had a wider connotation). The order can also be divided in accordance with the number and arrangement of the syringeal muscles (see SYRINX). In the terminology most lately used, the Tyranni or Clamatores (with which the Eurylaimi agree in the particular respect, although otherwise peculiar), are called 'Mesomyodi', and are subdivided into 'Tracheophonae' (= superfamily Furnarioidea) and 'Haploophonae' (= Tyrannoidea); the Menurae and the Oscines together constitute the 'Acromyodi'. There have been other varian ts of this scheme. The Passeriformes, as an order, are often referred to as the 'perching birds', and the Oscines as the 'song-birds', and from the point of view of European ornithology these two common names are in practice synonymous, the Oscines being the only suborder represented in the Palearctic Region. General characters. Perching and singing are functions reflected in the structure of members of the order. The foot is characteristic. There are always 4 toes, joined at the same level; the hallux is directed backwards and is not reversible. This form of foot is well adapted to perching by the method of gripping a slender branch, twig, reed, grass-stem or wire (see LEG). The toes are never webbed, even in the very few forms that have acquired aquatic habits (Cinclidae, and Cinclodes spp. in the Furnariidae). The syrinx is tracheal in a few (Tracheophonae-see above); otherwise it is in the common tracheo-bronchial position, but with various arrangements of its muscles as already mentioned. The quality of song varies greatly, even among the Oscines, but the order certainly includes the best musicians-and the most accomplished vocal mimics (see VOCALIZATION; and MIMICRY, VOCAL). Among other morphological characters the wing is eutaxic and has either 9 or 10 distinct primaries. The tail most usually has 12 rectrices. The spermatozoa have a distinctive form, not found in other birds. The form of bill shows various adaptations to the kind of food (see BILL). In body size, the members of the order range from very small to the moderate dimensions attained in the larger crows (Corvidae) and the lyrebirds (Menuridae). In feathering they range from inconspicuous drab hues and lack of adornment to brilliant colours and ornamental plumes. Mode of life. The Passeriformes are land birds. Some particularly frequent the vicinity of fresh water, and a very few find their food in it; some live near, or visit, the seashore; but to them all the open sea figures only as a dangerous area to be crossed on migration. Many of them, especially insectivorous species breeding in high latitudes, are migratory in the highest degree; others perform shorter journeys, while others again are sedentary. Widely varying habitats are exploited, including desert, montane areas, man-made environments, roosting and nesting in buildings and making use of 'unnatural' food. Breeding habits show a wide range of difference in nest sites, nests, eggs and so on. The young are nidicolous, being hatched blind, naked, and helpless. In general, parental care-by both sexes-is well developed; a few species, however, are parasitic in this respect (see BROOD-PARASITISM).

Distribution. The order is cosmopolitan, unrepresented only in polar latitudes and on the most forbidding islands. Indeed, its members predominate in the avifaunas of all but a few highly specialized types of environment. Some families of the Oscines are almost cosmopolitan, or are widespread in either the Old World or the New. Familial taxonomy of the Oscines. This is a subject of the greatest difficulty and much speculation. The general resemblance is so high, and the effect of convergence on adaptive characters so great, that trustworthy evidence of relationships between groups is hard to find. As E. Mayr has pointed out, with the exception of the Alaudidae (absence of ossified pessulus in the syrinx) and the Hirundinidae (closed bronchial rings) none of the families can be defined unequivocally by anatomical characters-there is always a hint that these may be functional and not phyletic. Many of the families are nevertheless reasonably distinctive-or at

Pecten

least appear to be so-and their validity as taxa has not been seriously challenged. Others are very unsatisfactory, and their boundaries are obscured by the existence of aberrant forms that may be included or excluded as a matter of opinion. Thus thrushes, warblers, flycatchers, and babblers have been considered by some authors to be so distinct as clearly to warrant the status of separate families, Turdidae, Sylviidae, Muscicapidae, Timaliidae, respectively. Many of the authors working on groups from the Old World Tropics, have treated them as subfamilies or tribes of the family Muscicapidae with all too numerous species and phenetic forms. Another classic area of special doubt includes the Fringillidae, Emberizidae, Thraupidae and other so-called nineprimaried (as opposed to the ordinary ten-primaried) Oscines. There are, in addition, instances which it is merely a matter of opinion, on degrees of difference, whether a few apparently nearly related groups should be treated as separate families or as subfamilies of one; such points are of minor importance. Where it is difficult even to delimit many of the families, it is still more difficult to arrange them all in larger groups. Generally, the song-birds (again excluding the larks and swallows) are divided into 3 major assemblages; (1) Old World insect-eaters and relatives; (2) New World insect-eaters and finches; and (3) crows (Corvidae), birds-of-paradise (Paradisaeidae), and associated families. The remaining more peculiar and isolated families, as well as the Old World nectar-eaters, are then placed rather irregularly within this broad framework (see Mayr and Greenway 1956). Whether or not any groups of families be expressly designated, it is necessary for practical purposes to arrange the families of the suborder in some sequence. Customarily, such a sequence purports to lead from the most primitive to the most specialized, or (chiefly in the past) vice versa. The same lack of real evidence, however, makes this equally in vain; the essential facts are just not known, and may perhaps never be ascertainable. In any event, even were it possible to construct an adequate concept of phyletic relationships, this could not be expressed in a linear sequence such as, for instance, the arrangement of any check-list or other systematic work requires. The most that a sequence can do is to keep together, here and there, a few families that are probably closely related; but it equally brings into juxtaposition other families between which no such near relationship can be supposed to exist. Current views tend to favour a sequence that is traditional, and thus in some ways convenient. There may be reason for believing that the sequence is to some slight extent a 'natural' one, and that it at least serves to keep a few probably related families together-especially those that might perhaps equally well be brought under a single head as subfamilies, and are indeed so treated by some authors. It should nevertheless be recognized and made abundantly clear that, apart from recent progress in biochemical and DNA research, the device is for the most part merely a convention. Thus, a conventional sequence of Passerine families was agreed upon by a committee appointed by the XI International Ornithological Congress (Basel 1954) and published by Mayr and Greenway (1956). This sequence has been followed by the editors and authors of the late James L. Peters' Check-list of Birds of the World. It follows the sequence (1), (2), (3) mentioned above and accepts the view that crows, as well as the whole corvid assemblage (group 3) are the most advanced and highly developed songbirds, a supposition which appears more or less based on the crows' intellectual capacities rather than on anatomical or fossil evidence and therefore has not failed to evoke refutation (Amadon 1957, Delacour and Vaurie 1957, Wetmore 1957, Mayr 1958, Storer 1959, 1971, Sibley 1970). Wetmore (1930, 1951, 1960) and most other Americans basically follow the sequence (3), (1), (2), whereas European authors, following Ernst Hartert's monumental work (1903-38) always have been more inclined to (3), (2), (1). As Storer's (1971) sequence, following (1), (3), (2), is thought to gain widest acceptance, it has been followed here with a few amendments as to the places of Motacillidae and Laniidae, in accordance with Voous (1977). It combines the views that the nine-primaried assemblage of New World insect-eaters, tanagers, finches, sparrows, cardinals and icterids are the most recently developed and diversified large group of birds. The evolution of the seed-crunching and seed-shelling fringilline and emberizine groups is thought to have been a geologically rather recent event, follow-

ing the rapid and equally recent evolution of monocotyledonous plants. Sturnids, ploceids and allies are most advanced among the other groups of songbirds. The nectar-feeding birds form highly advanced groups of their own.

441

Among other authors, Sibley particularly (1976, 1983) has added a new aspect to the systematic arrangement of songbirds by expressing the view that many of the characteristic Australian songbirds have no direct relatives in the other continents, but instead represent ecologically diverse groups comparable to those found in the diversity of Australian marsupials. Similarities between many Australian birds and groups or families occurring in other continents therefore are to be considered as having resulted from parallel or convergent evolution. In addition to the main groups (1), (2), and (3), a fourth group of Old Australian Endemics (e.g. Maluridae, Acanthizidae, Neosittidae) has to be accepted. A secondary radiation of Australian crow-like Endemics (e.g. Callaeidae, Grallinidae, Cracticidae, Paradisaeidae) adds a further dimension to the basic group (3). Numerous details of this theory remain obscure, but the theory in itself is fascinating and illuminating. K.H. V. Amadon, D. 1957. Remarks on the classification of the perching birds. Proc. Zool. Soc. Calcutta, Mookerjee Mem. Vol.: 259-268. Delacour, J. & Vaurie, C. 1957. A classification of the Oscines (Aves). Los Angeles County Mus. Contrib. Sci. no. 16: 1-6. Mayr, E. 1958. The sequence of the songbird families. Condor 60: 194-195. Mayr, E & Greenway, J,C. 1956. Sequence of passerine families (Aves). Breviora Mus. Compo Zool. 58: 1-11. Sibley, C.G. 1976. Protein evidence of the origin of certain Australian birds. Proc. XVI Int. Orn. Congr. Canberra (1974): 66-70. Sibley, C.G. & Ahlquist, J.E. 1983. Phylogeny and classification of birds based on the data of DNA-DNA hybridization. In Johnston, R.F. (ed.), Current Ornithology 1: 245-292. See also references under CLASSIFICATION.

PASSERINE: appertaining to the order Passeriformes; commonly

used substantively for species belonging to that order, members of all others being collectively called 'non-passerines' (see PASSERIFORMES). The form of the word would also admit of its being applied in a restricted sense with reference to the subfamily Passerinae, but to obviate confusion this is better avoided.

PASTOR: substantive name of the Rosy Pastor (or Rose-coloured Starling) Sturnus roseus (see STARLING). PATAGIAL TAG: see PATAGIUM: see

MARKING.

METAPATAGIUM; PROPATAGIUM; WING.

PATELLA: the 'knee-cap', not present in all birds (see LEG;

SKELETON,

POST-CRANIAL.

PATRISTIC: term sometimes applied in taxonomy to resemblances

between forms due to common ancestry, as distinct from resemblances due to convergent adaptation (see CONVERGENCE).

PAURAQUE: substantive name of Nyctidromus and Siphonorhis spp.

(for family see

NIGHTJAR).

PEACOCK: see below. PEAFOWL: substantive name of Pavo spp. and also of Afropavo congensis (and there are also 'peacock pheasants' Polyplectron spp. )-see 'Peacock' and 'peahen' are special names for male and female, but the former may also be used irrespective of sex.

PHEASANT.

PEALEA PHENOMENON: the occurrence of 'spotting or streaking as variations from the normal plumage pattern' in some species of storm-petrels (Hydrobatidae). Specimens showing this and at one time ascribed to a supposed form 'Pealea lineata' were later found to belong to 3 otherwise well known species. Murphy, R.C. & Snyder, J.P. 1952. The 'Pealea' phenomenon and other notes on storm petrels. Amer. Mus. Novit. no. 1596: 1-16.

PECKING: see

BEHAVIOUR, DEVELOPMENT OF.

PECK-ORDER: see

DOMINANCE (2).

PECTEN: a structure on the retina of the avian eye (see VISION).

442

Pectinate

PECTINATE: provided with a serrated (comb-like) edge, as on the inner aspect of the claw on the middle toe of some species and on the sides of the toes in certain Tetraoninae (see under LEG). PECTORAL: pertaining to the breast (see TOPOGRAPHY); for pectoral girdle see SKELETON, POST-CRANIAL. PEDIONOMIDAE: see under

GRUIFORMES; PLAINS-WANDERER.

PEDIUNKER: name for the Grey Petrel Procellaria cinerea, see PETREL.

PEEP: see SANDPIPER. PEEWIT: see PEWIT;

PLOVER (1).

PELAGIC HABITAT: see OCEANIC BIRDS. PELECANI; PELECANIDAE: suborder and family of

PELECANI-

White Pelican Pelecanus onocrotalus. C].B.).

FORMES; PELICAN.

PELECANIFORMES: an order, alternatively 'Steganopodes', comprising 3 suborders: Phaethontes, Pelecani, Fregatae; 6 families: Phaethontidae (TROPICBIRD), Sulidae (GANNET), Phalacrocoracidae (CORMORANT), Anhingidae (DARTER), Pelecanidae (PELICAN), Fregatidae (FRIGATEBIRD).

The order is one of mainly fish-eating birds of substantial size, characterized by having all 4 toes connected by a web (totipalmate), the hallux being turned forward and connected with the second digit. Except in the families first and last named above, the 8th and 9th of the 17-20 cervical vertebrae are so shaped that they articulate at an angle with those in front and behind. PELECANOIDIDAE: family of

PROCELLARIIFORMES; PETREL.

PELICAN: substantive name of all species of Pelecanus of the family Pelecanidae (Pelecaniformes, suborder Pelecani). Pelecanus includes 7 species, divided into 3 groups: (1) Great White Pelican Pelecanus onocrotalus, Dalmatian Pelican P. cnspus, Australian Pelican P. conspicillatus, and American White Pelican P. erythrorhynchos, all large, feed in groups, nest in dense colonies on ground, and never roost in trees; (2) Grey or Spotted-billed Pelican P. philippensis and Pink-backed Pelican P. rufescens, both smaller, usually feed singly, normally nest in trees in loosely packed colonies, and perch at roost in trees; and (3) Brown Pelican P. occidentalis which dives for its food. Sometimes P. crispus is included with P. philippensis but differences in nesting, feeding behaviour and morphology make this invalid. Characteristics. Pelicans are large (140-180 em) aquatic birds with a heavy body, long neck, large head and long, straight bill. The upper mandible is flat with a medium ridge, hooked at tip; the lower is loosely articulated and flexible with a suspended, extensible gular pouch. The wings are long and broad; the tail, short and rounded. Except for the Brown Pelican, the plumage is mainly white with areas of grey, brown and black. The face, throat and orbital area are bare. At courtship the American White Pelican develops a horn-like growth on the bill; the Great White Pelican has a swollen forehead, yellow in the male, orange-red in the female. All species develop startling secondary sex characters in the colours of the head, face and pouch. The sexes are similar, the male usually being larger. Habitat. All inhabit inland fresh and brackish lakes and coastal waters except Brown Pelicans which are restricted to coastal marine habitats. Distribution. Pelicans are pantropical and subtropical. In the New World, the Brown Pelican occurs along the Pacific coast from Washington to Chile and Galapagos and along the Atlantic from North Carolina to the Gulf of Mexico and Caribbean to Guiana. The American White Pelican is found from northern Alberta and Manitoba south to coastal Mexico and Guatemala east to Florida. In the Old World, Great White Pelicans range from Africa and south-east Europe to south-east China and the Malay Peninsula. The Dalmatian Pelican occurs from south-east Europe to Mongolia and northern China south to Iran and northern India. The Pink-backed Pelican occurs in Africa (south of about 20 Madagascar and south-west Arabia. The Grey Pelican inhabits India, southern China, and the Philippines south to the Malay Peninsula and Indonesia. The Australian Pelican occurs throughout Australia in suit0N),

able habitats, and in Tasmania and New Guinea. Populations. Colony size varies from a few individuals to many thousand pairs. Generally pelicans have declined markedly in range and numbers due to pesticides, drainage, and sensitivity to disturbance. Movements. Pelicans fly in V-formation, in lines or single file, often travelling one behind the other with the leader beating wings or gliding, the rest doing likewise. Pelicans also circle high in thermals and soar for considerable distances. Certain pelican populations undergo post-breeding dispersal, with some travelling long distances. Food. The diet is fish and sometimes crustaceans. Most species are surface-feeders, catching fish with the pouch. When the bird puts its bill into the water, the lower mandible expands into a broad scoop. The pelican traps the fish in the pouch under water, raises its head to drain water from the pouch, then swallows the fish whole. Sometimes pelicans transport fish in a partially digested state. The Pink-backed and Grey Pelicans usually swim singly or in small groups and, upon sighting prey, dart out their head and neck to catch fish. The larger species often use a herding technique when groups of 5 to several hundred swim forward, often in V-formation with the open end directed forward towards the beach or shallow water. As the group moves along, several partly raise their wings and simultaneously plunge their heads into the water. Each successful bird raises its bill upward and swallows fish. The Brown Pelican dives to catch fish under water. Behaviour. Pelicans are gregarious all year in groups of a few to several thousand individuals. Their non-breeding behaviour, as typified by the Brown Pelican, includes wing- and body-shake; tail-wag following landing in water or sitting on nest; bill-toss after preening; wing-flap for balance, comfort movement, or reaction to disturbance; wing-and-Iegstretching; glottis-exposure and bill-throw for stretching gular pouch and tissues of throat and upper breast; scratching head, neck, and pouch; bill-plunge to moisten gular pouch and to drink; head-rub to maintain head and neck feathers; preening; bathing; walking; swimming; gular flutter and spreading wings in response to temperature changes; and sleeping. Pelicans appear to arrive at the nesting area unmated. In tree-nesting species the male occupies a potential nest site where he sways the head and bill through a figure-8 (head swaying); arches neck away from body and points bill downward (bowing); turns head from side to side (head turning); raises bill toward horizontal position, stretches gular pouch taut, spreads wings and sometimes opens bill (upright); and throws bill over back, thrashes wings and claps mandibles (bill-clapping, Pinkbacked Pelican). The female initially selects the male, and also performs the above displays. No obvious behaviour precedes copulation. In ground-nesting species the displays are similar; in addition, males and females may swim, walk or fly in groups or walk along shore with head held high, sometimes with wings partly spread (strutting walk); males may gather in groups where they raise bills skyward (upright or head-up), make 'mooing' sounds, then thrust bills toward centre of group (bowing). The female selects the nest site. Voice. Pelicans are usually silent except at breeding colonies. There some produce only an expulsion of air from the lungs during bowing and upright displays, while others produce moo, ha-oogh and deep grunts. Young make screaming and wailing sounds when soliciting food.

Pellet

Breeding. Pelicans are colonial breeders , nesting in trees or on ground free of mammalian predators. Tree nests are large structures of dry sticks, sometimes 30 m above ground. Ground nests are small depressions, sometimes with sticks, leaves, reeds and pebbles . The male collects the nest material, the female builds the nest . In the tropics the nesting season may extend over several months, with some colonies peaking in rains, others in dry season. Usually 2-3 eggs are laid; they are large and elongated with a chalky coating . Incubation lasts 30-37 days, begins with the first egg, and is shared by both parents . The newly hatched young are pink and naked, turn black or grey within 4-14 days, and thereafter develop a coat of white, grey or blackish down. After about 3 weeks, the young of ground-nesting species collect in creches (pods). The young are cared for and fed by both parents . Small young are fed on partially regurgitated food; from about one week on, the young bird puts its head into the parent's pouch and feeds itself. Young pelicans take 70-80 days to reach the flying stage. E. K .U. See photo FLIGHT. Brown, L.H . & Urban , E .K . 1969. The breeding biology of the Great White Pelican Pelecanus onocrotalus roseus at Lake Shala, Ethiopia. Ibis Ill: 199-237. Burke, V.E . & Brown, L.H. 1970. Observations on the breeding of the Pink backed Pelican Pelecanus rufescens. Ibis 1I2: 499-512 . Knopf, F .L. 1979. Spatial and temporal aspects of colonial nesting of White Pelicans. Condor 81: 353-363. Lamba, B.S. 1963. Nidification of some common Indian birds, no. 7. The Spottedbilled or Grey Pelican (Pelecanus philippensis Gmelin). Pavo I: 1l0-1I9. Schaller, G.B. 1964. Breeding behavior of the White Pelican at Yellowstone Lake , Wyoming. Condor 66: 3-23 . Schreiber, R.W. 1977. Maintenance behavior and communication in the Brown Pelican. Ornithol. Monogr. 22. Schreiber, R.W. 1979. Reproductive performance of the Eastern Brown Pelican, Pelecanus occidentalis. Contrib. Sci. Nat . Hist . Mus . Los Angeles County , 317: 1-43. Vestiens, W.J .M . 1977. Breeding behaviour and ecology of the Australian Pelican, Pelecanus conspicillatus, in New South Wales. Aust. Wild . Res. 4: 37-58.

PELLET: a compact mass composed of those undigested portions of a bird's food that have been retained in the stomach by a mechanical barrier for a period before being regurgitated and ejected through the mouth, rather than evacuated as faeces; sometimes described as 'castings' . They vary considerably from species to species with respect to size, colour, shape, and the proportion of prey fragments that can be identified, but they form an important research tool for ornithologists when examining an individual bird's feeding tastes and variations in diet with season, year, region and habitat. The physiology and mechanics of pellet formation have been examined using radio-active tags but there is scope for further studies . Pellets are composed of materials of relatively low nutritional value, while those produced by starved birds in captive conditions show a greater degree of digestion than is normal in the wild. Pellet ejection may be immediate and apparently 'effortless' or may take as long as an hour with apparent 'nausea' . The process often consists of several upward stretches of the head and neck-convulsive movements-followed by a lowering and, especially in passerines, shaking of the head, with the pellet expelled up to I m or more. Pellets are most commonly associated with birds of prey (and notably owls) because their ability to digest bone is poor while the skeletal record in their pellets is good so that the diet may be accurately quantified. Pellet production has been widely observed in birds, covering some 330 species and more than 60 families (International Bird Pellet Study Group) including unlikely groups such as jays (Corvidae), flycatchers (Muscicapidae) and honeyeaters (Meliphagidae). Pellet ejection has also been recorded in certain mammals, reptiles and amphibians . Most pellets produced by large birds comprise a central core of hard materials such as bones, beaks, claws, scales, teeth and chitin, enveloped by softer substances like fur, feathers and, less often, vegetable matter . Lengthy hard food fragments such as bird beaks, legs, and mammal long-bones tend to be aligned with the longitudinal axis, the majority of pellets being elongate and oval in shape, fewer rounded or segmented. The contents of pellets are naturally determined first by the spectrum of food eaten; second, by the digestive ability of the species concerned. Owls usually swallow food items entire and their pellets contain the great majority of all bony elements and good evidence of most invertebrates eaten. Diurnal raptors are not so helpful to the analyst-they tear flesh and bone, digest much bone, frequently only partially consume a prey item, so that the pellet record is incomplete . Herons (Ardeidae) regurgi-

443

tate fur castings with little or no bony evidence of fish, amphibian or mammalian foods. The pellets of other birds may be dominated by single items such as corn husks (Rook Corvus frugilegus), wax (Honey Buzzard Pernis apivorus), fish bones (Kingfisher Alcedo auhis) , sand (Dipper Cinclus cinclus), chitinous insect hard-parts (Spotted Flycatcher Muscicapa striata), crustacean and mollusc fragments (some wadersScolopacidae). Pellets often also contain the unexpected. Scavenging gulls (Laridae) are notorious for the range of bizarre binding materials like cellophane, paper, plastic and rubber incorporated. Pellets can be important sources for the recovery of bird rings, especially those cast by regular small-bird feeders like Kestrel Falco tinnunculus, Short -eared Owl Asio flammeus, and Long-eared Owl A. otus. Other predators like the Barn Owl Tyto alba are very effective aerial 'samplers' of small mammal populat ions, indicating the presence of scarce or rare species and allowing large quantities of mammal bones to be collected far quicker than by normal trapping techniques. The ease with which pellets can be collected varies greatly from species to species. For most passerines one needs to witness the characteristic 'retching' behaviour before searching . Regular visits to the loafing sites of homogeneous groups like gulls and waders can prove productive. Regular roosting sites and occupied nests are otherwise the best sources of material , the last resort being an examination of the stomach contents of dead birds . Fresh pellets are usually damp and soft in texture with a surface mucous layer. This hardens quickly to produce a glossy varnished appearance (Barn Owl). Moisture may comprise 60% of the total initial pellet weight which is rapidly lost by evaporation . The rate at which pellets decompose depends on the species of bird, season, location and the micro-fauna and flora. Barn Owl pellets regurgitated in the protected environs of a dry barn may remain intact for many months, sometimes even years, while Tawny Owl Strix aluco pellets cast in damp woodland vegetation may be rain-leached or ice-shattered in a few days. Pellets composed of vegetable matter such as husks and seeds or fragments of insects, crustacea, or molluscs, are prone to an early breakdown . The most important decomposers of fur and feather castings are certain tineid moths, trogid beetles, mites and saprophytic fungi. The insects especially feed in their larval form on the fur and feather matrix, and pellets may soon crumble into small piles of bones which are easily scattered or buried . A productive exercise is to scrape away earth at traditional nesting places or beneath pellet 'ejection posts' to reveal an historical layer of buried bones . 'Fossilized' pellets have been found during archaeological excavations and helped throw light on the past distribution of small mammals . Pellets can be dissected in a dry or wet state , though most analysts prefer first to soak the material in a shallow tray of warm water before

Marsh Sandpiper Tringa stagnatilis ] .F . Reynolds).

bringing up a pellet. (P hoto:

444

Pellorneini

separating the contents with needles or forceps. A pocket lens or low-power microscope is necessary to identify the prey fragments with the aid of a reference key. For large quantities of pellets a centrifuge may profitably be used to separate the hard and soft elements. Pellets are best preserved dry and entire by an early spray with a strong insecticide followed by several coats of a quick-drying polyurethane. The dissected contents may be stored in glass files or mounted on stiff cardboard. Pellets are excellent ecological tools for the educationalist wishing to demonstrate the principles of food preferences, food chains, and energetics. D.E.G. Chitty, D.H. 1938. A laboratory study of pellet formation in the Short-eared OwL Proc. Zool, Soc. 108: 267-287. Glue, D.E. 1970. Avian predator pellet analysis and the mammalogist. Mammal Review I (3): 53-62. 377-378. Hanson, D.E. 1967. A type collection of bird pellets. Brit. Birds 60 Raptor Philips, J.R. & Dindal, D.L. 1979. Decomposition of rapt or Research 13 (4): 102-111. Southern, H.N. 1954. Tawny Owls and their prey. Ibis 96: 384-410. Yalden, D.W. 1977. The identification of remains in owl pellets. Mammal Society-occasional publication. Reading.

PELLORNEINI: see BABBLER. PELVIC GIRDLE: see SKELETON,

POST-CRANIAL.

PEN: special term for a female SWAN. PENDULINE TIT: substantive name of Remis pendulinus (Passeriformes, suborder Oscines); in the plural general term for the family Remizidae, formerly included in the Paridae (see TIT). There are 10 species in 4 genera. Characteristics. The penduline tits are active birds from 8-14cm long. They share many characteristics with the true tits, but have finer, more pointed bills and are even more acrobatic, being able to climb upside down along the underside of branches. The plumage of Remis is basically pale buff, chestnut and black, and shows considerable variation within populations and between races. The kapok tits Anthoscopus are mostly brown and yellow, and the Verdin Auriparusflasnceps is yellow and grey with a rusty patch on the carpal area. Habitat. Most species are found in open, scrubby areas where they are resident throughout the year, although some are nomadic outside the breeding season. Distribution and systematics. Remis (monotypic) is discontinuously distributed across the Palearctic from the Atlantic to the Pacific; the kapok tits (Anthoscopus, 7 species) are found in dry bush habitats over most of Africa south of the Sahara. In North America the Verdin is restricted to the semi-deserts of the south-western United States and northern Mexico. The Fire-capped Tit Cephalopyrus flammiceps is found in the evergreen forests of the Himalaya. Although structurally very similar to the other Remizidae and using the same highly developed acrobatic foraging and food-handling techniques (Lohrl 1967), its main affinities may lie with the true tits. Food. All species mainly feed on invertebrate prey taken from the outer twigs and branches of trees and bushes, supplemented with seeds and fruit. Behaviour. Most species are generally found in flocks, but the Verdins are solitary outside the breeding season, and it has been suggested that they may have closer links with the Bananaquit Coereba fiaveola than with the Remizidae (Taylor 1970). Voice. Songs are generally poorly developed but the species which flock have sharp, monosyllabic contact calls. Breeding. The 2 widely distributed Old World genera, Remiz and Anthoscopus, build similar, pendulous domed nests of vegetable down and breed as groups rather than distinct pairs. Remiz nests are suspended from twigs and generally about 5 m above water. Nest-building is started by the male weaving a foundation loop of grasses and roots on which the felted nest is built over a period of weeks. The main material used is pappus from willow Salix, poplar Populus, reed-mace Typha or willowherb Epilobium. The 5-10 white eggs, incubated by the female, hatch after about 12 days and the young fledge 16--18 days later. Anthoscopus nests have a prominent false entrance and dummy chamber with the real entrance capable of being closed by the birds. Vegetable down is generally the main nesting material but animal hair may also be used. The clutch consists of 3-6 white eggs, a few less than Remis, and the

Penduline Tit Remis pendulinus. (D. W.).

hatching and fledging periods are a little longer. In both genera the breeding groups may roost together in the nest, and may have cooperative breeding. The Verdin does not have helpers at the nest, and only one of the 3 races uses vegetable down; the other 2 weave their nests from thorny twigs. All Verdins start nest-building from a platform lodged in the outer part of a bush and not from a hanging loop of pliable material. From 3-6 blue-green speckled eggs are laid and the young fledge some 3 weeks after hatching. The Fire-capped Tit lays a clutch of 3 or 4 pale blue-green eggs in a lined hole in a tree. C.J.M. Lohrl, H. 1967. Zur verwandtschaftlichen Stellung von Cephalopyrus flammiceps auf Grund des Verhaltens. Bonn Zool. Beitr. 18: 127-138. W.K. 1970. Some taxonomic comments on the genus Auriparus. Auk 87:

PENG DIN: substantive name of all species of Spheniscidae, sole family of the order Sphenisciformes. Penguins are flightless sea birds of the Southern Hemisphere highly adapted for marine life. They range in weight and stature from birds of about 1kg and 40 em body length to 30kg and 115em. Characteristics. Despite their variation in size, and with breeding habitats ranging from the bare lava shores of equatorial islands through cool temperate forests, sub-Antarctic tussock grassland and beaches to Antarctic sea ice, penguins are remarkably similar in structure and plumage. They are all chiefly blue-grey or blue-black above and mainly white below; specific distinguishing marks are chiefly on the head and upper breast, visible while swimming on the surface. The main chick plumages are grey or brown uniformly or with one of these colours dorsally and white ventrally. Juvenile plumage is usually very similar to, but distinguishable from, that of adults. Most species are slightly sexually dimorphic; penguins of the genus Eudyptes notably so. They lack defined feather tracts (unlike most birds; see PTERYLOSIS) and short specialized feathers closely cover the body surface. Their bodies are highly streamlined, the wings reduced to strong, narrow, stiff flippers, with which they swim rapidly. The feet and tarsi are short, the legs set well back on the body, being used, with the tail, as rudders. On land penguins frequently rest on the short tarsometatarsus (heel) with the stout rectrices forming a prop. The short legs induce a waddling gait but on ice penguins can move rapidly by tobogganning. Penguins have comparatively solid bones and they generally weigh only a little less than the water they displace, reducing the energy required to dive. The duration and depth of dives varies greatly but the Emperor Penguin Aptenodytes forsteri can submerge for 18min and reach at least 265m, while even small species may stay down for 6 min and reach nearly 100m; typical values, however, are very much less than these. Swimming speeds probably range from 2-3 knots up to perhaps 15-20 knots in

Penguin

short bursts. Swimming often involves porpoising, whereby the bird breaks the surface with its momentum carrying it through the air for a metre or so before re-entering the water. This may facilitate breathing while travelling fast and may also confuse potential predators. The basic physical adaptations of penguins are thus concerned with swimming efficiently and also with thermal insulation. In addition to the dense waterproof feather coat, there is a well-defined fat layer and a highly developed vascular counter-current heat exchange system in the flippers and legs. All these are best developed in species of high latitude but are found even in temperate and tropical penguins which live in regions of cool water currents. When on land, however, these adaptations may lead to problems of overheating. It is significant that the species of warmer latitudes have relatively larger flippers and areas of bare facial skin as adaptations to dissipate excess heat. In addition they live in burrows to reduce direct insolation. The fossil record of penguins begins in the late Eocene (45 million years BP) and about 32 species are currently recognized. Most were between 50 em and 1m tall (much as living species) but 2 or 3 species were probably about 150-160cm tall and may have weighed 135kg. Their distribution was similar to that of living species, with most specimens coming from (in order of importance) New Zealand, Patagonia, Antarctic Peninsula, South Australia and South Africa. The fossil record provides no direct indication of the origins of penguins (though they presumably passed through a stage combining flight and underwater swimming like the auks of the northern hemisphere which are their nearest ecological equivalent) but one firm line of evidence suggests a very distant relationship to the Procellariiformes. The 16--18 living species (depending on whether the Royal Penguin Eudyptes(chrysolophus) schlegeli and the White-flippered Penguin Eudyptufa(minor) albosignata are regarded as full species or not) are divided into 6 genera. Most species are currently found between 45°S and 600S, with the greatest species diversity in the New Zealand area and the Falkland Islands; the main numerical concentrations, however, are around the coasts of Antarctica and on the sub-Antarctic islands. The biology and adaptations of 4 of the 6 genera are reviewed later; only the general patterns are summarized below. Distribution. The genus Aptenodytes comprises the 2 largest penguins, Emperor A. forsteri and King A. patagonicus; they are completely allopatric, the former breeding on the sea ice around the Antarctic Continent, the latter breeding at most sub-Antarctic and cold temperate

Chinstrap Penguin Pygoscelis antarctica. (B.P.).

445

islands. The 3 species of the genus Pygoscelis include 2 circumpolar ones, Adelie P. adeliae around the Antarctic Continent and Gentoo P. papua at the sub-Antarctic islands. These 2 species overlap in the Antarctic Peninsula area where the third species, Chinstrap P. antarctica, occurs in considerable numbers, principally between the centres of abundance of the other 2. The Yellow-eyed Penguin Megadyptes antipodes is ecologically similar to the Gentoo and essentially replaces it at the New Zealand subAntarctic islands (not Macquarie Island where Gentoo occurs) and South Island mainland. Of the crested penguins, 3, the Fiordland Eudyptes pachyrhynchus, Snares Crested E. robustus and Erect-crested E. sclateri, have allopatric breeding ranges and are confined to the same area as Megadyptes but the other 2 species, the Macaroni E. chrysolophus and Rockhopper E. chrysocome, have wide circumpolar distributions occurring together at several sub-Antarctic islands. The 4 species of the genus Spheniscus span the greatest longitudinal range with the Galapagos S. mendicuZus at the Equator, the Humboldt S. humboldti from equatorial Peru to central Chile (entirely within the cool Peruvian current), and the Magellanic S. magellanicus in southern South America and its off-lying islands, including the Falklands. The only African penguin, the Jackass S. demersus, is confined to the coast of South and South-west Africa, influenced by the cooler waters of the Benguela and Agulhas currents. The genus Eudyptula, ecologically similar to Spheniscus, has a single species, the Little Blue E. minor, the smallest of the family, throughout New Zealand and much of the south coast of Australia and a closely related species or subspecies, the White-flippered E. albosignata, on the east coast of New Zealand's South Island. Movements. Winter distributions and movements are imprecisely known. The tropical and warm temperate species are sedentary. Most eudyptid species and southern populations of Gentoo and Magellanic Penguins disperse widely (and generally northwards) in winter but northern populations are chiefly resident. Antarctic species move at least to the pack ice edge in winter. Juveniles disperse widely after fledging and there are many records far from breeding sites. Food. Crustaceans, fish and squid are the main prey of penguins. Fish are important in the diet of inshore feeding species, e.g. Spheniscus species, Little Blue and Gentoo Penguins and also of the deeper diving King and Emperor Penguins. Squid perhaps predominate in the food of the King Penguin and seem fairly frequently taken by Emperor and Rockhopper Penguins and some spheniscids. Euphausiid crustaceans (krill) are the principal prey of perhaps all pygoscelid and most eudyptid species and are certainly taken by all Antarctic penguins. When feeding chicks, individuals of most species are at sea exclusively or mainly during daylight hours but by diving they could follow any diel migration of their prey. The Little Blue Penguin is anomalous in not normally feeding its chicks until well after nightfall. As the smallest species it presumably has the shallowest diving capacity and may therefore be more dependent on crepuscular feeding, when a greater proportion of prey are near the surface. It may also be avoiding diurnal predators. Penguins may be assisted in prey detection by echolocation, using sonar based on cavitation clicks produced by their swimming movement. Behaviour. Most penguins are highly social, both on land and at sea, and often breed in vast colonies, only defending the small area around the nest. Although all species have complex courtship and mate recognition behaviour, social behaviours are perhaps most developed in the densely colonial pygoscelid and eudyptid penguins. Of the latter, those species that breed in dense vegetation show less intraspecific interaction, presumably because, like Megadyptes also, their nests are farther apart. Despite living in burrows, spheniscid penguins, which usually breed in dense colonies, have fairly elaborate visual and vocal displays; Eudyptula, in which burrows are usually well dispersed, less so. Emperor Penguins, because of the physiological need to huddle when incubating, lack fixed territories and only defend their immediate living space (when not huddling). Individual recognition, whether of mates or offspring, is based mostly on calls but in burrowing species, and in others where chicks stay close to the breeding site after the brooding period ceases, nest site location is an important, if not a vital preliminary. Breeding. Emperor Penguins breed in winter. King Penguin chicks overwinter at the breeding colony, but are rarely fed during this period and grow mainly during the previous and subsequent summers. Otherwise Antarctic and most sub-Antarctic and cold temperate penguins

446

Penguin

breed in spring and summer and their timing is highly synchronized within and between colonies. The Gentoo Penguin is least well synchronized and at Marion Island it lays in winter (June); this may reduce competition for food with the large number of eudyptid penguins there. The more temperate eudyptid species have a longer breeding season and its timing is more variable. In Spheniscus (except S. magellanicus) there are usually two main peaks of breeding but laying occurs in all months of the year. This is also true of most Eudyptula populations and in South Australia some pairs are able to raise broods successfully twice a year. Penguins usually mate with the partners of previous years: in a colony of Yellow-eyed Penguins 610/0 of pairings lasted 2 to 6 years, 12% 7 to 13 years and the overall divorce rate was 14% per annum; in a study of the Little Blue Penguin one pairing lasted 11 years and the divorce rate was 18% per annum. In a major Adelie Penguin study, however, no pairing lasted 6 years and the divorce rate was over 500/0. Royal Penguins breed first when at least 5 years old; Emperor, King, Gentoo and Adelie Penguins when at least 3 (2) or 4 (d') and Little Blue, Yellow-eyed and Jackass Penguins when at least 2 years old. Only Aptenodytes penguins lay a single egg, the remainder normally laying 2 eggs, occasionally one (inexperienced birds where this is known) or 3. In the Yellow-eyed Penguin (and probably generally) age affected fertility so that hatching success in the study colony was 320/0, 92% and 77% of eggs incubated by birds of age 2, 6 and 14--19 respectively. In eudyptids the first egg of the clutch is very much smaller than the second; only in Rockhopper and Fiordland Penguins do both eggs hatch and only one chick is ever reared. In other penguins hatching is also staggered and this can promote brood reduction, particularly in warmer water species, but even so 2 chicks are not infrequently reared. All penguins have the capacity for storing substantial fat reserves (e.g, before the moult fast) but only the Emperor, King, Adelle and eudyptid penguins undertake long fasts in the courtship, incubation and brooding periods. During fasts lasting 110-115 days for male Emperor Penguins and 35 days for Adelie and eudyptid penguins up to 450/0 of initial body weight may be lost. By contrast Gentoo, Yellow-eyed, Little Blue and spheniscid penguins usually change incubation daily although in some species the female may incubate for more of each day. After the brooding period ceases the frequency with which chicks are fed increases. Intervals between meals are about 3 days for King and Emperor Penguin, about one day for Adelie and most eudyptids but in Gentoo, Eudyptula and Spheniscus both parents bring food each day. The rate of chick growth probably reflects the size of meals and the frequency with which they are delivered. This is presumably determined by food distribution and availability and it has also been suggested that intra-specific competition for food may affect both breeding success and the age (or level of experience) at which first breeding attempts are made. Reduction of interspecific competition between penguins is thought to be achieved by differences in prey type, foraging range and timing of breeding season. Chicks grow rapidly (though initially rather slowly in the Emperor Penguin), particularly in Antarctic species and the Macaroni Penguin among sub-Antarctic species. After 2 to 3 weeks (6 weeks in Aptenodytes) the chicks of species breeding in open areas form large aggregations (Adelie, Gentoo, Aptenodytes) or small ones involving a few chicks from adjacent nests.(Chinstrap, Jackass, Eudyptes spp.). Moult. In most species, once chicks are independent, the parents fatten quickly for a moult fast of 2-6 weeks depending on species. The daily energy cost of moult is about twice that of incubation. Jackass and Galapagos Penguins show a less well defined moult period; moult occurs at any time between breeding attempts. In other species immature birds usually complete moult before breeding birds start and at least in eudyptid penguins the timing of moult becomes later with age until the first breeding attempt is made. Populations. Compared with other seabirds, annual survival of adult penguins is relatively low, being at least 69% for Adelle, 86% for Royal, 870/0 for Yellow-eyed and 86% for Little Blue Penguin, but 95% for Emperor Penguin. Longevity may well be inversely related to breeding success (including juvenile survival) which is high in most Antarctic species except Emperor Penguin, where only 19% of fledglings survive their first year of life. Some penguin populations in the Antarctic Peninsula area have increased substantially in numbers, e.g. Chins trap Penguin has increased fivefold in 30 years at some established sites, while Adelie Penguin has doubled in the same period. This is attributed to greater availability of krill due to the drastic reduction in stocks of Antarctic krill-eating whales. In contrast Jackass and Humboldt Pen-

guins have decreased markedly, chiefly because of human activities like egg and guano collection and commercial fishing. Yellow-eyed Penguins and some Adelle Penguin populations have declined due to increased human interference. J.P.C.

Aptenodytes. This genus comprises the 2 largest living penguins. The Emperor Penguin stands well over 1m tall and weighs 20-40 kg; the King Penguin nearly 1m tall but weights only 10-20 kg. Their plumage is very similar, blue-grey above, white (King) or yellowish (Emperor) below with conspicuous golden or bright yellow auricular patches and orange or violet-blue mandibular plates. Both species have a circumpolar distribution. The Emperor Penguin has the most southerly distribution of any penguin (all colonies being south of 65°S), and as it breeds in winter, faces some of the most extreme climatic conditions for breeding of any bird. The low mean winter temperature (-10 to -20°C), high winds (mean 40kmh- 1 but reaching 150-200 km h -1 at some colonies) and blown spindrift snow combine to produce an environment where heat loss can be critical. There are about 26 known colonies, mainly on the coasts of Enderby, Wilkes and Victoria Land; all but two are on fast sea-ice and most are backed by an ice-cliff providing shelter from wind. They range in size from Coulman Island with c. 25,000 pairs to the Dion Islands with only 500; the world breeding population is estimated at 200,000 pairs. In contrast King Penguins lay in summer (but take a year to raise a chick) on flat or gently sloping ground at sub-Antarctic islands. The world breeding population is about one million pairs with the largest concentrations at the Indian Ocean sub-Antarctic islands (Prince Edward Islands, Crozet Islands) but they breed as far south as South Georgia and the recently re-colonized Heard Island. Data on pelagic movements and distribution outside the breeding season are lacking. Emperor Penguins seem rarely to move outside the Antarctic Circle but stray birds (mainly immature) have reached Tierra del Fuego, Falkland Islands, southern New Zealand and many subAntarctic islands. King Penguins ringed at Iles Crozet have been retrapped at Macquarie and Marion Islands. Both species have been recorded as eating squid, fish and crustaceans, but it is probable that squid and fish form the bulk of Emperor Penguin diet in the breeding season and of King Penguins at least in autumn and spring. Both Aptenodytes species raise large chicks which become independent by the Antarctic mid-summer when food resources are at their most abundant. They have tackled this problem in quite different ways; the King Penguin by taking over a year for a successful breeding attempt and the Emperor Penguin by breeding in the cold, dark Antarctic winter. The latter is possible only with a remarkable conjunction of physiological and behavioural adaptations. An Emperor Penguin's body size and shape combine to provide a relatively low surface to volume ratio (important for reducing heat loss) and in addition its appendages (flipper, bill) are 25% smaller in proportion than in any other penguin. Heat loss is further reduced by extreme proliferation of the vascular counter-current heat -exchange system and excellent insulation is afforded by the very long double-layered, high density feathers which even extend to cover the tibio-tarsi, All these combine to establish a lower ambient critical temperature (below which metabolic rate must be increased to maintain body temperature at a constant level) of -10°C with wind speed of up to 18km h -I. Even though the size of the Emperor Penguin permits it to store proportionately large fat reserves, these would be insufficient to cope with the demands of long fasts in prevailing winter conditions. However a 25-50% reduction in individual heat loss is achieved by adults and chicks huddling in large groups (up to 5,000 birds at IOper m-) and reducing activity to a minimum. This behavioural adaptation is fundamental in permitting Emperor Penguins to breed during the Antarctic winter. Such social behaviour during breeding is unique among the otherwise highly territorial males of the family and is feasible only because of their ability to move with the egg on their feet and cover it (and the young chick) with the pouch-like fold of abdominal skin. Although King Penguins incubate in a similar fashion, they breed with constant inter-individual distance and also lack such extreme physiological specializations, presumably because temperature and wind chill effects rarely exceed their lower critical temperature of - 5°C. Chicks, however, frequently form dense huddles in winter. In the Emperor Penguin, in addition to sex-specific differences, there

Penguin

is a very clear individual variation in calls which, in a species lacking any fixed nest site or territory, is the basis for mate and parent-offspring recognition. In the King Penguin, which has a relatively fixed incubation site, although sex-specific differences are retained, individual variation of calls is much less marked. For Emperor Penguins the breeding season commences with courtship and copulation in March-April, following 2 months at sea laying down substantial fat reserves. Females leave after laying in mid May, having lost 25% of body weight in the 6 week fast while ashore. Only males incubate (for 62-64 days) and also feed the chick for a few days (on an oesophageal secretion comprising 60% protein and 28% lipid) if the return of the female is delayed. During their 110--115 day fast males lose up to 45% of their initial body weight. The female broods the chick for 40 days and thereafter both parents rear the chick through the winter, the chicks themselves forming tight huddles. While losses at the egg stage are fairly consistent (4-16%) between years, chick losses are more variable (usually 4--30% but exceptionally up to 90%) and reflect the variation in winter conditions. Chicks depart in December at only 60% of adult body weight, the lowest figure for any penguin, presumably because the adults need the remaining time to moult and return to breeding condition by the end of the summer. Only 190/0 of fledglings survive their first year of life. However, Emperor Penguins may breed first at 3 years of age (although many do not do so until age 6) and mean annual survival from age 2 is 95%. Life expectancy from fledging is about 20 years. King Penguins start laying in late November and continue until mid April although there are pronounced peaks at the beginning and towards the end of this period. Eggs hatch in 55 days and incubation duties are shared by the parents in 5-day shifts after an initial 14-day shift by the male. Early breeders raise their chick to 80% of adult weight by June and feed it sporadically (fasts of 2 months or so with a weight loss of about 40%) until September when regular feeding resumes until the chicks depart in November-December. The adults then moult and usually lay again in February-March. This time much smaller chicks overwinter (and many die) and finally fledge in January-February. Parents with this timetable cannot breed again until the following summer. After a breeding failure, however, many (but probably not all) birds postpone moult until the following September-October when it thus immediately precedes the next breeding attempt. This variety of breeding and moulting schedules ensures that in any colony at most times there are adults, eggs and chicks at many stages of moult, incubation and growth. The above account applies principally to South Georgia; at lIes Crozet it appears that most adults when successful breed only biennially. J.P. Pygoscelis. A genus, of 3 species, with a circumpolar distribution in the Antarctic and sub-Antarctic. The species are c. 50--60 cm long and weigh between 4 and 8 kg. The Adelie Penguin breeds at numerous sites on Antarctica's coast and associated islands. Colonies range in size from less than 100 to at least 500,000 pairs and it is perhaps the most abundant of any penguin species. With the Emperor Penguin, it is the most southerly breeding penguin. The Chinstrap Penguin occurs in the northern Antarctic, principally in the region of the Scotia Sea and Antarctic Peninsula north of 65°S. The Gentoo Penguin has the most northerly distribution of the three. It breeds at a few Antarctic sites but mostly on sub-Antarctic islands near the Antarctic Convergence, for instance Crozet, Kerguelen, Marion, Prince Edward, South Georgia and Macquarie Islands. It is particularly abundant in the Falkland Islands. Knowledge of the pelagic ecology of these species is virtually confined to the summer breeding period. In winter most populations of Adelie and Chinstrap Penguins must move north near to the limit of pack ice; their subsequent dispersion is unknown. The northern populations of the Gentoo, however, are relatively sedentary. At all seasons the Gentoo Penguin is notably less pelagic than the others and the higher incidence of fish in its diet probably reflects this. Although some Adelie Penguin populations take many larval fish, euphausiids (particularly Euphausia crystallorophias around the periphery of the Antarctic continent and E. superba elsewhere) seem the most important prey for all 3 species and differences in foraging range and possibily size of prey eaten seem significant aspects of interspecific differences in feeding ecology. More is known of the social behaviour of Adelle Penguins but most of their displays have somewhat similar counterparts in the other 2 species. Generally Chinstraps seem more aggressive and Gentoos more timid. In the Adelie Penguin breeding displays are most prevalent among young

447

birds or older non-breeders; after egg laying breeders display rather little. The displays are affected by two important factors. First, these penguins are highly gregarious at sea and when breeding on land they maintain an almost inviolate individual distance and vigorously defend the space within pecking range of their nest. Second, partners associate for relatively few days in a breeding season shortened by the constraints of rigorous climate and high latitudes. There is thus a particular need for straightforward yet accurate communication. Within these constraints the repertoire of basic messages common to all higher vertebrates is present, with the possible exception of play. Individual birds vary greatly in aggression and this may relate partly to age. Some of the younger non-breeders who are physiologically mature enough to breed fail to do so until their social behaviour matures as well. The breeding biology and behaviour of Adelie Penguins has been studied intensively. That of the other 2 pygoscelids is less well known but is probably rather similar, allowing for their more northern distributions and less intensive environmental constraints. Nesting is limited to snowand ice-free areas and, because these are relatively rare in the Antarctic, there is much overlap in the type of terrain that the 3 species choose. Adelies seem to be the most selective, tending to build nests on exposed ridge tops. This may reflect the need in higher latitudes to avoid areas where drifting snow would cover nests or where melt water could inundate them. Chinstraps often prefer slopes, whereas Gentoos more often choose flatter areas closer to the beach, particularly at sub-Antarctic islands where drifting snow may be less of a problem. Adelie Penguins arrive at their colonies a few weeks earlier in the spring than their relatives: September and early October in the Scotia Sea region, but late October in the Ross Sea which is much farther south. Males on average arrive a few days earlier than females. Unusually extensive pack-ice delays the arrival even of Adelies, since they walk over the ice much less rapidly than they swim. Adelie Penguins fast throughout the territory establishment, courtship and egg-laying periods, thus reducing the number of times they have to walk between colonies and accessible feeding areas. Males remain for an additional 2 weeks to incubate eggs while females replenish their fat reserves by feeding at sea. Females incubate for about 10 days, then males for 5 or more days, and, at about the time the female next returns (about 35 days after the first egg was laid) the eggs hatch. With Chinstrap Penguins, which begin to nest after the pack-ice has become more broken up and has diminished in extent, the periods of fasting are shorter, and thus nest-reliefs more frequent, Gentoo Penguins have a daily changeover. The normal clutch for all 3 species consists of 2 eggs. A third egg will be laid only if the first is lost before the second is laid. Full incubation does not begin with the first egg; thus, although 2--4 days occur between laying of the eggs, the chicks hatch about 1-2 days apart. If the pack-ice is more persistent than usual the returns of feeding Adelle Penguins are delayed, resulting in increased numbers of nest desertions as the fat reserves of incubating birds run low. This happens most often when the male is due for relief by the female at the end of his 5-week fast. The accelerating rate by which the ice disappears means that, even on the Antarctic Continent by early summer and the time eggs hatch, feeding trips take only 3 to 4 days and a week later are reduced to one to 2 days. The more frequent nest reliefs also correspond to the period of most rapid growth in the chicks. For the first 3 or 4 weeks one parent continually broods the chicks, but chick requirements become too great for one parent to sustain and both must forage simultaneously. Chicks then group together in creches as a means to reduce predation from skuas Catharacta spp. At 7-8 weeks of age the chicks leave the colony of their own accord and go to sea. In most seasons each breeding pair averages less than one chick fledged. The fledging period is only slightly longer in the Chinstrap Penguin but is at least 12 weeks in the Gentoo Penguin whose actively swimming chicks are often still fed by their parents. Age, and to some extent breeding experience, affect the breeding biology of Adelie Penguins. Very few one-year-olds visit the colony. Many 2-year-olds do so for a few days during the period of chick hatching, but most birds make their first visit as 3 and 4-year-olds and a few not until 5 years. With increasing age, up to about 7 including both breeders and non-breeders, birds arrive earlier in the season, make more visits and stay longer. Some females can first breed at 3 years of age, males at 4, but most females and males first breed at 4-5 and 5-6 years respectively. Most females have bred at least once by 5, but males have not all bred until 8. A year of previous breeding experience increases a

448

Penguin

bird's chances of breeding successfully. Birds that delay their first breeding to later years are often inept, breeding unsuccessfully or failing to breed more often than not. Most breeders are 5-10 years of age. Breeding is hazardous and only a few birds live as long as 18 years; the oldest birds even so tend to be those that first bred at a late age and to be non-breeders in several seasons thereafter. The high mortality among breeders (in which leopard seal Hydrurga leptonyx predation may be important) is apparently offset by high breeding success due to reliable and abundant food sources. D.G.A. Eudyptes, A genus of medium sized (weight 2.6--6kg), heavy-billed penguins differing from other members of the family in being highly sexually dimorphic, in having prominent yellow or orange crests on their heads, and in laying clutches of 2 eggs of very dissimilar size from which only a single chick is reared. There are 5 species (6 if the Royal Penguin E. schlegeli is considered a full species rather than a sub-species of the Macaroni E. chrysolophus) falling into 2 distinct groups: the large Royal and Macaroni Penguins (sometimes classified in the genus Catarrhactes) which have loose dull orange crests arising from the centre of the forehead and 14 rectrices, and the rest which are smaller, with more compact and lustrous yellow crests arising from superciliary stripes on either side of the head, and 16 rectrices. All 5 species occur in the Australasian region and 3 are confined to New Zealand seas. The other 2 species, Rockhopper and Macaroni/ Royal have a circumpolar breeding distribution at sub-Antarctic islands although the Rockhopper Penguin occurs further north (to Tristan cia Cunha) and the Macaroni further south (to the South Shetland Islands). Most species nest colonially in the open either on the coast or inland up to about 300 m. The exception is the Fiordland Penguin, which nests in dense, wet forest north of the Subtropical Convergence on the west coast of the South Island of New Zealand. In this forest environment it experiences considerably less extreme temperature and exposure compared with nesting in the open. The more widespread species are very numerous and one world estimate for the Rockhopper Penguin was 4 3/ 4 million pairs. Some 2 million Royal Penguins nest at Macquarie Island and about 5 million pairs of Macaroni Penguins breed at South Georgia. Least abundant is the Snares Crested Penguin, estimated to have not more than about 50,000 birds at its sale breeding place on the Snares Island, south of New Zealand. After moulting the non-breeding season is spent at sea. Some birds wander far, e.g. an Erect-crested Penguin from New Zealand to the Falkland Islands and a Rockhopper of the northern race to the Chatham Islands, New Zealand. All species probably eat krill and Euphausia superba forms 80% by weight of the diet of Macaroni Penguins at South Georgia. It is possible that the difference in bill size of males and females may result in prey of different sizes being taken. Fish and squid make up the remainder of the diet and are of greater importance to the Rockhopper Penguin. In most species the chick is fed daily, on average, indicating that that the parents are able to forage extensively in continental shelf and slope waters. All species are highly colonial on land and social at sea, only the Fiordland Penguin nesting in a rather dispersed pattern, but this is probably a consequence of the use of a forest habitat and there is nonetheless much vocal interaction among nearby nesting pairs. Crested penguins show a marked philopatry: young birds returning as yearlings usually to that part of the colony where they were born and breeding birds return to the same nest and partner during successive years, although some divorce does occur. A complex system of displays and vocalizations is used, including nearly 20 distinct displays. Breeding takes place in the southern summer except for the Fiordland Penguin which lays in late winter. Maturity is delayed and each successive age group comes ashore earlier and stays longer. Few Royal Penguins less than 6 years old attempt to breed, success appearing to depend upon the parents' age and weight on arrival, and few birds less than 10 years old regularly rear young successfully. The breeding cycles all involve long fasts at the nests before laying (male arriving before female), followed by 10-15 day incubation stints when the on-duty bird again fasts. In all but the Fiordland Penguin the female incubates first, having been ashore for less time than the male. Hatching occurs after 31-37 days and with all the species the male then remains to guard the chick, not feeding it, but fasting for 2-3 weeks. The female alone brings food to the chick during this guard stage. The chick then enters a small

creche and the male leaves for the sea. Thereafter the chick is fed by both sexes, but still mainly by the female, for a total of about 60-75 days depending on species. The parents then depart to sea for between 14 days (Macaroni) and 70 days (Snares Crested), laying down fat reserves nearly equivalent to their original body weight, before a moult fast at the breeding colony lasting c. 25 days. All birds then go to sea, some having reached their minimum weight during the season. Unique to this genus is the laying of first a small and then a large egg. For example, the second eggs of the Rockhopper, Snares Crested and Macaroni Penguins are 46%, 29% and 71% larger respectively than the first eggs of those species. Both eggs are viable but only one chick is reared. In contrast, the difference in egg size is only 17% with the Fiordland Penguin and in this species twins are often reared for a few days. Thereafter, as with the other species, the smaller chick dies; usually, but not always, the chick hatched from the smaller egg. Such a system may exist to cope with the high egg loss consequent on the considerable amount of fighting between neighbours, which in turn results from sexual selection favouring aggressive males. That the eggs are of different sizes ensures that if both hatch-as quite often occurs in the less concentrated colonies of the Fiordland Penguin (where fighting is correspondingly reduced) only one chick survives for long. If the eggs were of similar sizes then many similar sized twins might survive to the guard stage only for both to die when their food needs exceeded their parents' abilities to supply it. J. W. Spheniscus. A genus of 4 medium sized (c. 3 kg weight) species of essentially low latitudes: the Galapagos Penguin breeding on two islands of this archipelago at the Equator, the Humboldt Penguin in Peru and Chile from 6 to 34°S, the Magellanic Penguin breeding north to 32°30'S in western and 48°S in eastern South America and the Jackass Penguin breeding from southern Africa (35°S) north to 16°30'S on the west coast and 26°S on the east coast. They are basically sedentary species but southern populations of the Magellanic Penguin migrate northwards after breeding. This account is taken mainly from recent studies of the Jackass Penguin and the Galapagos Penguin. All Spheniscus species breed in burrows dug with the feet in sand or under rocks and bushes but densely packed surface colonies of Jackass Penguins also occur. They are inshore feeders, restricted to continental shelf areas and their diet is mainly fish, often anchovy Engraulis sp. and pilchards Sardinops sp., though squid are also taken, at least by Jackass Penguins. At sea, Jackass Penguins forage in small groups and dive synchronously, often after a head-bobbing signal. Diving depths or actual foraging techniques are unknown but deep dives are unlikely since they feed mainly on surface-shoaling fish. Two species, the Jackass and the Humboldt, occur in high productive upwelling systems that support large fishing industries. Populations of these 2 species have decreased alarmingly, initially due to egg removal and guano collection, subsequently due to competition for food; the fishing industries of the west coasts of South America and South Africa both 'prey' on the same species of fish as do the penguins. The survival of these 2 species is inextricably linked to the presence of the anchovy and pilchard and therefore to a compromise between exploitation and conservation. The breeding displays of the Jackass Penguin resemble those of other non-Aptenodytes penguins. Adaptation for hole-nesting appears to have resulted in particularly loud raucous vocalizations. Spheniscus penguins engage in 'ecstatic displays' and 'mutual ecstatic displays' as do most penguin species. 'Beak-slapping', an aggressive display, occurs in Jackass and Galapagos Penguins and may be restricted to the genus; during 'beak-slapping' 2 birds (often mates) face each other and shake their heads rapidly so that the beaks slap together. The Magellanic Penguin, with the most southerly distribution, has the most restricted breeding season and moult follows chick fledging. By contrast Jackass Penguins may breed in all months but 2 peaks a year are usually noticeable, the first following the annual summer moult. Galapagos Penguins may breed and moult twice a year (but sometimes not at all); again breeding follows moulting, an unusual pattern in birds. Clutch size is one or (usually) 2 and 2 young may be reared. There is little difference in size between first and second laid eggs. Asynchronous laying and hatching leads to brood reduction by starvation of the younger sibling if the food supply is inadequate. Being inshore feeders, Spheniscus penguins have no breeding fast; changeover at the nest is usually daily; prolonged incubation bouts of 0S

Pessulus

several days normally result in desertion. Jackass Penguin chicks may be fed several times a day, typically in the late afternoon or evening. When older, they are often left alone during the day and may form small creches (usually not more than 5 chicks), and are then fed daily by both parents. The chick-rearing period in the Jackass Penguin varies by as much as 40 days. The younger chick often stays at the nest for as long as 2 weeks after its elder sibling has left. During this period it is able to 'catch up' and even exceed its sibling's weight. Breeding success in Jackass Penguins varies with nest habitat and has been reduced historically by removal of the GUANO 'cap' in which birds once burrowed; surface nests are less successful, due mainly to enhanced predation. A similar trend has apparently occurred in the Humboldt Penguin. The Galapagos and probably the Humboldt Penguin's breeding season and success is related to the occurrence of warm water influxes (El Nino) and a decrease in upwelling. Similar changes in the degree of upwelling may affect the Jackass Penguin in parts of its range. Jackass Penguins fledge at approximately 2/3 the weight of adults and undergo a juvenile dispersal to warmer waters, returning to moult into adult plumage at about one year of age-though this varies by many months. Breeding does not take place in the first year of adulthood, and not always in the second. See photos COLONIALITY; CRECHE; EGG; MOULT; PARENTAL CARE. J.C.

Ainley, D.G., LeResche, R.E. & Sladen, W.J.L. 1983. Breeding Biology of the Adelie Penguin. Los Angeles. Boersma, P.D. 1977. An ecological and behavioural study of the Galapagos Penguin. Living Bird 15: 43-93. Carrick, R. 1972. Population ecology of the Australian Black-backed Magpie, Royal Penguin and Silver Gull. In Population Ecology of Migratory Birds: A Symposium. US Department of the Interior Wildlife Research Report No.2: 41-99. Cooper, J. 1980. Breeding biology of the Jackass Penguin with special reference to its conservation. Proc. 4th Pan. Afr. Orn. Congr.: 227-231. Croxall, J.P. & Prince, P.A. 1980. Food of Gentoo Penguins Pygoscelis papua and Macaroni Penguins Eudyptes chrysolophus at South Georgia. Ibis 122: 245-253. Jouventin, P. 1982. Visual and vocal signals in penguins, their evolution and adaptive characters. J. Compo Ethol., Suppl, 24: 149pp. Jouventin, P. & Le Maho, Y. In press. The Emperor Penguin. Yale. Lishman, G.S. In press. The food and feeding ecology of Adelie and Chinstrap Penguins at Signy Island, South Orkney Islands. J. Zool., London. Reilly, P.N. & Cullen, J.M. 1981. The Little Penguin Eudyptula minor in Victoria, II: breeding. Emu 81: 1-20. Richdale, L.E. 1957. A Population Study of Penguins. Oxford. Stonehouse, B. 1967. The general biology and thermal balances of penguins. In Cragg, J.B. (ed.) Advances in Ecological Research 4: 131-196. Stonehouse, B. (ed.). 1975. The Biology of Penguins. London.

PENIS: male copulatory organ, present in a few kinds of birds (see ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM).

PENNA: alternatively 'pennaceous feather', one in which the barbs form a coherent vane (see FEATHER; and compare PLUMA).

449

Rufous-browed Pepper-shrike Cyclarhis gujanensis. (P.J.K.B.).

The nest is a semi-pendent hammock slung, like that of a vireo, from a fork of a tree or tall bush. The eggs, 2 or 3 in number, are pale cream or pinkish, spotted and blotched with brown. The part played by male and female in incubation is uncertain, but both sexes feed the young. D.W.S.(l)

PERCHING: loosely, the act of standing (sometimes sitting) on some more or less elevated object, especially one providing only exiguous space; more particularly, doing this while gripping the perch with the feet. The Passeriformes are sometimes referred to as the 'perching birds' because their toes, and the flexor tendons actuating these, are notably adapted to gripping a small branch or similar object, e.g. taut wire (see LEG). Many other birds, however, are well able to perch, although lacking the particular specialization of foot structure. Others again can only stand on an object flatfooted, as they do on the ground, and have therefore limited powers of perching; some, of course, make no use of any kind of narrow perch, if indeed they stand in elevated positions at all. A few birds, e.g. night jars, commonly perch along the axis of a branch instead of transversely. Distinct from perching is clinging to the roughnesses of a vertical or overhanging surface; to this action some birds are particularly adapted, e.g. swifts--which are unable to perch in the ordinary sense-woodpeckers and nuthatches among others. The hanging parrots or 'bat parrots' Loriculus spp. have the habit of hanging head downwards, by their feet, from branches. See photo overleaf. PERCHING BIRDS: see PASSERIFORMES. PERDIZ: name used in Latin America for Rynchotus spp. (see

TINA-

MOU).

PEPPER-SHRIKE: substantive name of the 2 species of the subfamily Cyclarhinae of the Vireonidae (Passeriformes, suborder Oscines); in the plural, general term for the subfamily. This is a Neotropical group usually placed among (as here) or close to the vireos. Pepper-shrikes are heavily built birds, 15-18 ern long, with large heads and powerful bills strongly hooked at the tip. The wings are short and the flight is weak; the plumage is loose in texture. The better-known species, the Rufousbrowed Pepper-shrike Cyclarhis gujanensis, has a wide range from southern Mexico south to Uruguay; the other, C. nigrirostris, is confined to Colombia and Ecuador. The Rufous-browed Pepper-shrike is greenish above, with a redbrown steak through the eye, grey crown, 'and yellow breast. It is a bird of open woodland, cultivation, and second growth; it lives in pairs and is sedentary. The food consists mainly of insects and other invertebrates, which the birds search for among the foliage of the middle levels and tops of trees. Pepper-shrikes hold down large prey with the foot and pull it to pieces with the bill, which is also well adapted for tearing open cocoons adhering to leaves and bark. The commonest call is a melodious but monotonous phrase of set pattern, like that of an Old World oriole (Oriolidae); this is uttered repeatedly from leafy cover where the bird itself is often difficult to see. The alarm calls are loud and extremely harsh.

PEREGRINE: Falco peregnnus (see FALCON). PERICARDIUM: see HEART. PERIODICALS, ORNITHOLOGICAL: see under PERIODICITY: see PHOTOPERIODISM;

ORNITHOLOGY.

RHYTHMS AND TIME MEASURE-

MENT.

PERIOSTEUM: see SKELETON,

POST-CRANIAL.

PERIOTIC: a paired bone of the

SKULL.

PERITONEUM: membranous lining of the abdominal cavity and reflected over the outer surfaces of organs lying therein. PERNINAE: see HAWK.

PERVIOUS: as applied to nostrils, see PESSULUS: see SYRINX.

NARIS.

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Pesticide

Sandwich Terns Sterna sandv icensis perching on log. (P hoto: J.B. & S . Bouomley). See

PESTICIDE: a chemical agent used by man to control living organisms which are inimical or believed to be inimical to his interests. The term covers herbicides, fungicides, insecticides, rodenticides , chemosterilants and growth retardants . The term is sometimes used in a more restricted sense as a synonym for insecticide . Most pesticides are synthetic organic substances, but some are inorganic or naturally occurring organic ones. See TOXIC CHEMICALS. PESTS, BIRDS AS : wherever man has established settlements he has found that some of his resources are shared by birds . With most bird species this is acceptable but a few conflict with man' s interests . The result of this conflict is some kind of damage, where the term 'damage' infers a direct loss, ultimately in terms of money, or causes expenditure to counteract the problem . In some instances, however, this definition cannot be strictly applied. A farmer who sees his fields apparently devastated is not prepared to wait until harvest time to see whether his yield is in fact reduced . In other words , if a farmer thinks that birds are causing damage, he will take steps to prevent it whether or not a real loss is incurred. Even where damage does occur, it is often very difficult to estimate the financial losses. The equation is rendered even more difficult by the capacity of some of the pest species to confer potential benefit by their consumption of insect pests. Estimates of damage that are available for some species in some situations indicate that losses can be considerable (Jackson and Jackson 1977) and in developing countrie s severe damage may result in loss of human life. Damage to crops is usually local, however, and although individual farmer s can lose a high proportion of their yields, expressed in national terms birds generally consume only a small proportion of total production. Kinds of damage. Bird problems fall in several areas: agriculture (including horticulture and fisheries), forestry, urban and aviation are those which attract most attention. Damage to agricultural crops occurs mainly at sowing/germination and at ripening, the seeds being the target food; but the foliage is also grazed by some birds, notably pigeons and sometimes by larks, pheasants and geese. The seeds of cultivated crops such as maize, barley, wheat, sorghum , millet and rice are eaten by a wide variety of birds , especially certain sparrows, weavers, starlings , parakeets and New World blackbirds (Icteridae) . Damage to sown and germinating seeds is, owing to the compensatory capabilities of the plants , generally less serious than damage to ripening crops. Following recent changes in animal husbandry, where cereal grains are fed to cattle in the open, post-harvest losses due to starlings and New World blackbirds have become serious in some countries . These bird s, together with some crows, can also be responsible for losses of pelleted animal foods where these are presen ted in the open .

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Many fruiting plants have evolved dispersal mechanisms involving birds and mammals, and cultivated fruit s inevitably suffer the attentions of starlings, thrushes, finches, parrots and many others. The decline of the cherry industry in some areas of Europe is blamed partly on predation by Starlings Stumus vulgaris . Olives in North Africa and grapes in Europe , North America, parts of Africa and elsewhere also suffer severe bird damage, and a wide variety of other fruits is attacked . Fruit blossoms may also be eaten (though some species that attack flowers may be important pollinators e.g. sunbirds Nectariniidae ), and Bullfinches Pyrrhula pyrrhula can cause extensive damage by eating the buds of certain cultivars of apples , pears, plums and blackcurrants. Claims that seabirds can compete with commercial marine fisheries seem to be unfounded , declines being attributed largely to the industry itself. At fish farms, bird predation is of great concern to the owner since financial losses can be high. Herons, gulls, Ospreys Pandion haliaetus and others take fish while Mute Swans Cygnus olor have been blamed for taking fish eggs. Damage in forestry is due mainly to large concentrations of birds such as European Starlings and American Red-winged Blackbirds Agelaius phoeniceus roosting in young plantations. The weight of birds can break off branches, possibly leading to subsequent mis-shapen growth of the trees, and trees may even be killed by the large deposits of guano. While birds are generally welcome around human habitation s, some cultures regard them , or at least some species, as harbingers of ill omen. In some places the breeding and roosting of birds in or on buildings can necessitate expensive cleaning or repair or can cause public health problems. The guano stains beneath House Martin Delichon urbica nests constitute a relatively minor problem but the nesting of some species can cause structural damage. The construction of bulky nests in roof spaces by various starlings and by Jackdaws Corvus monedula can lead to subsequent dangers of damp , while in aircraft hangars nest material and faecal droppings can result in expensive and dangerous problems when they fall into the air intakes of jet engines; occasionally, nests are even built inside aircraft. Woodpeckers have been recorded drilling holes in wooden roofs, telegraph poles and even, in Israel, irrigation pipes. Where thatching is a common roofing material, nest-building in the thatch by birds such as sparrows (P asser) and Indian Mynahs Acridotheres tristis can destroy insulative and water-proofing properties of the roof. Recent inland foraging of various gulls is being accompanied by their breeding on buildings, leading to problems of fouling and unacceptable noise, especially in early morning. Roosting by gulls on buildings has also resulted in damage to roof materials, especially where expanded polystyrene insulation is used. Fouling by roosting Starlings and Feral Pigeons Columba livia in cities results in degradation of masonry, dangerously slippery roads and pavements , and possible dangers of disease. In North

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America, the main problem associated with roosts of icterids and starlings near conurbations lies in the guano providing a growth medium for Histoplasma capsulatum, the causative agent of endemic histoplasmosis in humans. Some pigeon populations have a high incidence of avian tuberculosis Mycobacterium avium and the roosting of gulls on reservoirs increases their potential to transmit salmonellae to man. Psittacosis (a form of ornithosis) can be contracted as a result of close contact with birds, especially parrots and their allies. Wild birds are sometimes claimed to act as vectors of diseases of domestic stock e.g. foot and mouth disease and transmissible gastroenteritis of pigs, but conclusive evidence of the involvement of birds is often lacking. Collisions between birds and aircraft-'bird strikes'-range from relatively minor to catastrophic. Slight structural damage can be expensive to repair but the ingestion of birds by jet engines, leading to engine failure, can result in loss of the aeroplane, sometimes with loss of life. Most bird strikes occur near airfields when aircraft fly low, in the airspace most frequently occupied by birds; it is at take-off and landing that sudden loss of power can be most serious. The species most frequently involved are those, like certain gulls, corvids, plovers (Charadriidae) and starlings, that inhabit open grassy areas. Damage prevention. The two basic approaches are to reduce the population of bird pests by killing them or to make the resource being damaged, or from which damage occurs, less attractive to the birds. Attempts to reduce populations form the basic philosophy of damage reduction of many farmers. Most bird pests are, however, extremely numerous and successful. They have a high annual mortality and population turnover and their 'natural' mortality must be exceeded to achieve effective population reduction. Traditional methods of killing, e.g. by shooting or trapping, fail to achieve the desired level of mortality and even agents of mass destruction using poisons, flame-throwers, explosives (see QUELEA CONTROL; Tahon 1980), stupefying chemicals or surfactants (feather wetting agents-Lefebvre and Seubert 1970) have not reduced general population levels. Mass destruction can provide sufficient reduction to permit alleviation of local damage in some instances (e.g. Quelea and European Starling). In the United States, urban roosting icterids and starlings are killed rather than dispersed to prevent the establishment of new roosts whose guano deposits might act as foci of infection of histoplasmosis. In the western world the growing protectionist lobby is forcing a more critical approach to mass killing of birds and to the techniques that may be employed, and damage prevention measures that do not involve killing will inevitably play a greater role in future. One approach to damage is to let it continue and offer compensation to the farmer. This is done in Canada where the damaging birds are wildfowl, themselves a valuable sporting resource (Boyd 1980). There are obvious difficulties in deciding the level of compensation and who should meet the cost. Another approach, involving similar financial problems, is to provide alternative attractive food for the bird pests, on the farm or in refuges (Owen 1980). More commonly used approaches involve rendering the place where damage occurs less attractive. This can be done in several ways but most techniques rely on the presence of an alternative resource to which the birds may be driven. This is especially true of attempts to drive birds away from vulnerable areas (see SCARING and REPELLENTS, CHEMICAL) rather than of physical modifications to the crop or habitat. The ultimate form of physical modification is to exclude birds totally from a vulnerable resource. Cages to exclude birds are commonly used over fruit in domestic gardens but this form of protection is less frequently adopted in commercial horticulture. Disposable plastic netting is now draped over large areas of vineyards in Europe, while more permanent forms of netting are sometimes used over cherry orchards in Britain and New Zealand: the development of dwarf forms of cherry tree will make this form of bird protection easier in the future. A similar approach has been applied where cattle are fed indoors: a mixture of plastic and wire netting and strips of heavy duty PVC is used to cover entrances to buildings through which birds might otherwise have access (Feare and Swannack 1978). Less complete protection can be afforded by other forms of habitat modification. Good and Johnson (1976) were able to manipulate the positions occupied by Brown-headed Cowbirds Molothrus ater in their roosts by thinning the roosting trees, and Brough and Bridgman (1980) showed that the bird populations of airfields could be reduced by allowing the grass to grow tall. A degree of crop protection may also be

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achieved by growing cultivars that are less susceptible to attack by birds in areas where damage is anticipated. For example, Bullfinches eat certain cultivars of fruit buds in preference to others and some cereal crops have long-awned cultivars that possess some resistance to bird attack (see QUELEA CONTROL). The mechanism of the Bullfinch's selection is not known but, as with scaring devices and chemical repellents, the efficiency of these 'bird resistant' forms is likely to diminish when acceptable alternative foods are absent. C.].F. Boyd, H. 1980. Waterfowl crop damage prevention and compensation programmes in the Canadian Prairie Provinces. In Wright, E.N., Inglis, I.R. & Feare, C.]. (eds.). Bird Problems in Agriculture. Croydon, British Crop Protection Council. Brough, T. & Bridgman, C.J. 1980. An evaluation of long grass as a bird deterrent on British airfields. ]. Appl. Ecol. 17: 243-253. Feare, C.]. & Swannack, K.P. 1978. Starling damage and its prevention at an open-fronted calf yard. Anim. Prod. 26: 259-265. Good, H.B. & Johnson, D.M. 1976. Experimental tree trimming to control an urban winter blackbird roost. Proc. Bird Control Seminar 7: 54-56. Jackson, W.B. & Jackson, S.S. 1977. Estimates of bird depredations to agricultural crops and stored products. EPPO Publication, Ser. B, No. 84: 33-43. Lefebvre, P.W. & Seubert, ].L. 1970. Surfactants as blackbird stressing agents. Proc. Vertebrate Pest Conf. 4: 15&-161. Owen, M. 1980. The role of refuges in wildfowl management. In Wright, E.N., Inglis, I.R. & Feare, C.J. (eds.). Bird Problems in Agriculture. Croydon. Tahon, j. 1980. Attempts to control starlings at roosts using explosives. In Wright, E.N., Inglis, I.R. & Feare, C.J. (eds.). Bird Problems in Agriculture. Croydon.

PE TREL: whole or part of the substantive name of many species in 3 of

the 4 families of the order Procellariiformes (Tubinares); in the plural a general term together with 'tubenoses' for the order. It comprises the families Diomedeidae (albatrosses), Procellariidae (fulmars and shearwaters), Hydrobatidae (storm-petrels) and Pelecanoididae (divingpetrels); in the past some authors have treated the Hydrobatidae as a subfamily of the Procellariidae, but they differ in their serum proteins among other characters. The order forms a group of totally marine species which share a number of distinctive characteristics. Characteristics. The Procellariiformes are distinguished by deeplygrooved, markedly hooked bills. Their long tubular nostrils are associated with a marked development of the olfactory part of the brain. They all have a distinctive musky smell, and it appears that the whole order is adapted to locate either their feeding-area, food, each other or their breeding-places by smell. Most or all species collect and store in their stomachs large quantities of oil from the energy-rich food-stores laid down by marine organisms. This oil is used as food for their young, and is also spat out as a defence against predators. They are very helpless on land, most species being clumsy and walking only with difficulty. The larger ones bite viciously. The tubenoses appear to be a very ancient group, perhaps of southern origin, although several modern genera are already present in northern deposits dating at least as far back as the Miocene. They appear to be most closely related to another southern order, the penguins (Sphenisciformes), the petrels having developed as aerial seabirds while the penguins developed as aquatic ones. The two between them show the most advanced adaptation for a marine environment now found among birds. There are some 23 genera and 80 to 100 species distributed throughout the oceans; one family, the Pelecanoididae, and about half the genera and species are still restricted to the Southern Hemisphere with progressively fewer species in the North Pacific, North Atlantic, Indian Ocean and Mediterranean. Tubenoses all have very similar life histories adapted to the relatively stable, secure, uniform marine environment with its exposure to the weather. They have a long period of immaturity, a long breeding cycle and low reproductive rate adapted for slow formation of the egg and growth of the embryo and chick while the parents travel widely in search of food. They have a long expectation of life in an environment relatively free from predators. They show more variation in other characters adapted for the exploitation of different aspects of the marine environment, notably either from the air or by diving under water, and for the avoidance of interspecific reactions, including size, structure, markings, patterns of distribution and migrations, and timing of breeding seasons and moult. The albatrosses (7~140 em in length) are among the largest and the storm-petrels (12-25 em in length) the smallest seabirds. Within several of the larger groups closely related species of different sizes, habits and appearance are found in the same area. In some cases, such as the alba-

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trosses, prions Pachyptila and gadfly petrels Pterodroma and Bulweria, they are all very similar in structure; in others, such as the fulmars, shearwaters and storm-petrels they show a marked variation in structure adapted for different types of flight or methods of feeding. Many species show a simple counter-shaded colour pattern, dark above and light below, sometimes with contrasting markings on the head, wing-coverts, tail-coverts or flight-feathers; but pale, mottled, or uniformly dark variations are common even among closely related forms. Many species are markedly polymorphic and most show traces of polymorphism. The species nesting in high latitudes tend to be white all over, or grey or pale brown above and white below, with yellow, pink, green or blue and black bare parts; those breeding in warmer climates tend to be brown or black above with less or no white below and red and black or entirely black bare parts. Some groups of closely related species or races show great geographical variation in conformity with this trend. The peripheral markings often provide interspecific recognition characters, including the brightly coloured bills and complex wing-markings of the larger species which display by day, and the white faces of many gadfly-petrels and some shearwaters, and the white rumps of many storm-petrels, which display by night. Closely related species which occur at the same breeding places often show contrasting markings or occur in different colour phases, and races of the same species may show differences in appearance which can be related to the occurrence of species with which they might come into conflict. In general, representative species tend to be smaller, but races of species larger, in lower latitudes, but there is much variation, which can often also be related to the local competitive situation. Some well-defined larger superspecies may have closely related smaller 'shadow species' breeding in the same area at another season, as in the case of the Manx and Little Shearwater Puffinus puffinus and P. assimilis and the Hawaiian and Bonin Petrels Pterodroma phaeopygia and P. hypoleuca and their allies. Marked variation in appearance with age and sex is only found in the largest species, the albatrosses and giant petrels, in which the young birds tend to be dark while male Wandering Albatrosses Diomedea exulans become whiter than the females. Young birds may also show more marked pale feather-edges above in some other species, including the small Hydrobatidae, and at first have soft, undeveloped bills. Their appearance contrasts markedly with that of the senile individuals which are not uncommon in these long-lived species, with more rugged bills, scaly legs, worn or missing claws, and dishevelled plumage. Males tend to be larger than females in most groups, but may be smaller in the Hydrobatidae; marked variation in the amount of sexual dimorphism may occur even among races of the same species. Dwarf individuals sometimes occur, possibly birds which were fed inadequately as chicks; one such runt examined had aspergillosis. Habitat. All species are totally marine, feeding alone or in groups dispersed over the open ocean according to the distribution of their food, more birds and larger flocks occurring in the areas of upwelling and marine turbulence associated with plankton production along the lee shores of the continents and around the convergences between water masses at sea. Distribution and movements. Most species appear to be more or less closely restricted to distinct circumpolar zones of surface water at sea. Some are comparatively sedentary or disperse throughout the habitat outside the breeding season, and others perform more or less complex migrations between good feeding areas in different zones in the same or opposite hemispheres. Some populations appear to perform circular movements, either around the world in the circumpolar belts of winds in the higher latitudes of the Southern Hemisphere, or around the anticyclones stationary in the middle latitudes of other oceans, so that they are assisted by following winds throughout their migrations. These travellers may often be largely young birds, while the adults make more direct movements. The movements of closely related species often appear to have a complementary pattern, so that their distribution forms a mozaic, as for example in the large shearwaters and gadfly petrels. In general, the species occurring in high latitudes of either hemisphere usually appear either to be sedentary or to move into lower latitudes in the winter. The species occurring in middle latitudes may either be sedentary, or move into the tropics or the comparable latitudes of the opposite hemisphere in the winter; and the tropics are occupied either by residents, or by wintering populations of birds breeding in the higher latitudes of both hemispheres and which replace each other at different seasons. Most species breed in the highest latitudes of their range in the

local summer, but some in the lowest latitudes in the winter, possibly either because there are no suitable breeding places in higher latitudes, or because there are too many competitors there, or because they originated in the other hemisphere. Where a number of similar species feed or breed in the same area they are thus often found to avoid competition for food or conflicts at the nest-sites by occurring at different seasons. Populations. The welfare of many species has been affected in recent centuries by human activity. Some have been reduced by past exploitation for food, feathers, or fish bait, but few are known to be killed directly by man now except where their chicks are harvested on a limited scale in Australasia and at Tristan da Cunha, and where they are lost accidentally in fish-nets in northern seas. Many populations have also been seriously reduced by the loss of habitat and predation due to imported mammals such as rats, cats, rabbits, goats, hogs, and mongooses at island breeding sites. A number of species including the Short-tailed Albatross Diomedea albatrus, 2 shearwaters, and 5 gadfly petrels were 'lost' for long periods of years and found to be reduced to small vulnerable populations when they were rediscovered. So far only one species is definitely thought to have been exterminated, the Guadelupe Storm-petrel Oceanodroma macrodactyla, which was lost in the early decades of the 20th century from an island off Lower California invaded by cats. On the other hand, many species including albatrosses, large shearwaters, and the Northern Fulmar Fulmarus glacialis, which is spreading all round the temperate North Atlantic, have profited greatly by feeding on the offal discarded by fishing boats. Food. The natural food of tubenoses consists of the larger zooplankton, cephalopods, fish and sometimes other birds. Many species now follow ships for refuse or food turned up in the wake, and some avoid them. The different groups specialize in catching different foods under different conditions at different distances from the shore, so there is a considerable series of representative forms exploiting different zones of surface water in different oceans. Behaviour. All species normally keep well away from land when not engaged in breeding activities, but may come inshore when the visibility deteriorates and sometimes appear inland in large 'wrecks' after gales. Usually there appears to be some underlying factor such as the failure of the food supply or disease, since they can ride out most bad weather. Birds normally come ashore only to breed, though the more sedentary species may visit the breeding stations at intervals for much of the year. Adults start to re-establish their territories and renovate their nest sites weeks or months before laying. They then usually depart again for a 'honeymoon' lasting days or weeks during which time they appear to feed separately before the female returns to lay and the male to take the first spell of incubation. Voice. There are complex vocal displays at the breeding sites, the larger species also rattling their bills, behaviour carried out both in the air overhead and at the nest. Repertoires include a variety of wailing, moaning, screaming, cackling and squalling noises, often with a weird effect at night so that the birds have been mistaken for evil spirits. At sea they are usually shy, quiet and undemonstrative except when fighting over food. Breeding. Nesting is usually social, sometimes in vast, dense colonies running into hundreds of thousands of pairs, though others are more widely scattered. Most nest on oceanic and offshore islands, but some species may use mainland cliffs and headlands, mountain tops and deserts, and even buildings, if they are undisturbed. The smaller species usually nest in a chamber at the end of a long burrow which they dig for themselves, but sometimes in holes among rocks or concealed in vegetation, and usually come ashore by night, apparently to avoid aerial predators which appear to be their worst natural enemies. The larger species visit more open nests by day. Large nests are built on the ground by the southern albatrosses and poorer ones by the giant petrels, possibly because they are normally compelled to nest in waterlogged situations. Other species may collect any material which is within reach around the nest. They normally lay one comparatively large white egg with a coarse shell and sometimes fine reddish spots, but never well developed markings. The female has a distended cloaca for weeks afterwards (the only indication of her sex for many species). Two eggs have been recorded, probably often the work of 2 females or replacement after an egg is lost, but this appears to be very rare. The incubation period is long, nearly 6 weeks in the smallest storm-petrels, 2 months or more in the larger species, and the chick is hatched blind, but covered in long, thick down. While incubating the egg

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and brooding the chick, the parents relieve each other at intervals of days. The chick is soon left alone and only visited to be fed at equally long intervals. Both parents feed the chick by regurgitation with a mixture of half digested food and oil which is derived from it, and if well fed the chick soon becomes very fat. The frequency of feeding is liable to vary greatly with the weather and possibly the experience of the parents, and sometimes individual chicks or even whole colonies may starve. The successful chicks eventually become much heavier than their parents, though the weight falls again as the feathers grow, and at fledging they usually weigh much the same as the adults. It has been suggested that the parents eventually abandon the chick before it fledges, but in some species at least it may be fed irregularly until it leaves, and some parents may even continue to return to the nest afterwards. Some weakly and backward young, possibly the offspring of dead or incompetent (immature or senile) birds, may certainly be abandoned in the nest, especially in migratory species, but may do well if they are then given supplementary feeds. The fledging period is very long, some 2 months in the storm-petrels, 3-5 in the medium sized species, 9-12 in the largest albatrosses. The young sit quietly in the nest at first, but start to move about and exercise themselves by flapping their wings as the time to leave approaches. Most chicks eventually appear to fly directly from the nest, especially if it is situated inland. They are liable to make abortive flights and land in unsuitable places or come to village lights at night at first, and weakly young may swim out to sea if they can reach the water. Strong young fly well on fledging and probably never see the nest or their parents again; some transequatorial migrants immediately set out on long migrations, which must include a further period of starvation as they cross the tropics, and wrecks are particularly liable to occur at this time. Ringed birds have been recovered in the opposite hemisphere within days of the probable date of fledging. Young birds fend for themselves on leaving the nest and spend their early years at sea, sometimes congregating in 'nurseries' where there is a good food supply. Later, they start to return to land for increasing periods in the breeding season, and also leave to start the annual moult early. During this time they often appear to wander and prospect new sites, though most eventually return to their natal colony. They then spend more years displaying and excavating nests before they start to breed, which the smallest storm-petrels may attempt at 2-3 years, but the largest albatrosses not until they are 5-10 years old, with poor success at first. Once they have started to breed, most species attempt it annually, though within the tropics some species may return at shorter intervals, while the largest albatrosses require 2 years for a successful cycle. Some southern storm-petrels have only one coat of nestling down, but most have two. The juvenile plumage usually appears to be moulted at sea when the birds are about a year old, often in the 'nurseries'. Some of the larger species start a slow body-moult during the breeding season, Snow Petrels Pagodroma nivea completing it, but most species delay the moult of the flight-feathers until they have finished breeding for the year. The migrants may then complete it rapidly in some good feeding area in their winter quarters, though the more sedentary species are slower and start to return to the breeding places before it is finished. The power of flight may be impaired for a time when the moult is rapid, notably in some of the large shearwaters, and may be lost entirely by some of the diving petrels which moult the flight feathers simultaneously. Albatrosses. The family Diomedeidae includes the 14 largest species (length 70-140cm) in the order, with a vast WING SPAN (2-3m), long, hooked bills with separate nostrils, short legs on which they can stand well and run to take off, and short, round tails in the 11 members of the genus Diomedea, but long, pointed tails in the 2 sooty albatrosses of the genus Phoebetria. They achieve continual effortless gliding flight by making use of the updraughts above the waves and the slopes of their breeding islands, and tend to settle on the water when the wind drops. They appear to feed mainly on large cephalopods caught or found disabled at the sea surface, perhaps largely at night, but they can also dive, and take fish and other marine animals. The sooty albatrosses in particular also catch birds, while the other species are among the seabirds which appear to profit most from scavenging around fishing-boats. Albatrosses nest colonially in the open on remote islands, and one of the largest species, the Royal Albatross Diomedea epomophora, colonized Taiaroa Head on the east coast of the South Island of New Zealand when it was protected with a fence. They all have spectacular displays at the nest in which they stand with the wings opened and tail fanned while

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Black-browed Albatross Diomedea melanophris. (B.P.).

the head is stretched out and thrown up and the tip of the bill buried in the plumage of the back between the scapulars, to the accompaniment of gurgling and braying sounds. The members of the genus Phoebetria which tend to nest on cliffs also carry out aerial displays in pairs accompanied by screams. Two of the great albatrosses, the Wandering Diomedea exulans and the Royal, have more complex social displays in which the males (which arrive first at the breeding colony) gather around a female with their vast wings spread, rattling their bills. It seems likely that there was once a community of primitive albatrosses in the circumpolar Tethys Ocean of the Northern Hemisphere during the Tertiary, since fossil remains of an early form, the English Albatross Diomedea anglica, have been found on both sides of the North Atlantic, which is now only visited by stray individuals of the southern species; while the northern species are now confined to the North Pacific. It seems possible that the Galapagos Albatross Diomedea irrorata, which occurs over the cold Peruvian Current within the tropics, is the most primitive surviving form, since it has a simple grey coloration with a paler head and bill and builds no nest. Three rather similar species with contrasting markings breed together at the central North Pacific archipelagoes, the Black-footed Albatross D. nigripes, which is dark brown with a paler face and base to the tail when adult, the Laysan Albatross D. immutabilis, which has a white body with a dark eyebrow, upperwing, back and tip to the tail, and the Short-tailed Albatross D. albatrus, now reduced to a population of a few score birds nesting on islands south of Japan; it is dark when young but becomes white with dark wing-tips when adult. The fact that the northern albatrosses nest in the local winter suggests that the group was originally of southern origin, and they show their greatest development in the Southern Ocean, where there are now 3 distinct groups of species each of which has plumage comparable to one of the northern species, with the addition of distinctive head and wing markings, although they do not appear to be particularly closely related to the northern forms, and differ from them in building nests. The simplest situation and basic pattern of variation is found in the genus Phoebetna, which includes 2 small, dark, agile, long-tailed species with dark plumage and a distinctive incomplete white eye-ring, the Sooty Albatross P. fusca with a dark brown body and yellow stripe on the lower mandible in the subtropical South Atlantic and Indian Ocean, and the Light-Mantled (Sooty) Albatross P. palpebrata, with a paler body and blue stripe on the bill, further south and in the South Pacific. The 3 great albatrosses are much larger than the other species, with an exceptionally long breeding-cycle, so that eggs laid in one summer give rise to chicks which are fed through the winter to fledge a year later. The Royal Albatross is largely white with dark upperwings and breeds in the New Zealand area, dispersing around the world to South America.

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The populations of the Wandering Albatross which breed alongside it are largely dark, like the young Short-tailed Albatross, and never become very white, but the old birds of .the populations breeding elsewhere throughout the Southern Ocean become whiter when adult, some of the southern males becoming as white as Royal Albatrosses. A third dark species D. amsterdamensis has recently also been found breeding in very small numbers on Amsterdam Island in the southern Indian Ocean. The height of complexity is found with a group of medium-sized species with dark brows, backs and tails similar to those of the Laysan Albatross known as 'mollymawks' from the old sailor's name for fulmars. The most familiar species is the Black-browed Albatross Diomedea melanophris, which has a simple black and white plumage pattern and yellow bill when adult. It behaves like the Wandering Albatross, breeding abundantly throughout the subantarctic zone and migrating north in the winter, when it sometimes reaches the northern hemisphere, including Britain, and may become marooned there. In contrast to this, 3 highly-distinct races of Shy Albatross Diomedea cauta retain as adults the more or less grey head and bill found in young mollymawks, and behave like the Royal Albatross, breeding around New Zealand and Tasmania and migrating east and west. Finally, 3 allies of the last group, having grey heads and black bills with distinctive yellow stripes, behave like the sooty albatrosses, breeding on oceanic islands in the subtropical South Atlantic and Indian Ocean (Yellow-nosed Albatross Diomedea chlororhynchos), subtropical South Pacific (Buller's Albatross D. bulleri) and the subantarctic zone of the Southern Ocean (Grey-headed Albatross D. chrysostoma) and disperse throughout these zones of surface water. Fulmarine petrels and shearwaters. The family Procellariidae includes the main body of medium- to large-sized petrels (30-70 em) totalling some 12 genera and over 50 species. They may be divided into 2 subfamilies, the Fulmarinae, largely aerial species with skulls strengthened by fusion of the lacrhymal bone to facilitate seizure of their food from above the surface (except in the small primitive northern genus Bulweria) and the Procellariinae, more aquatic species with longer bills rendered mobile by retention of a separate lacrhymal bone used for seizing fish under water. The Fulmarinae can be subdivided into 3 further specialized groups, the fulmars, prions, and gadfly petrels. The fulmars include 5 highly distinct species or super species of different sizes with a heavy build, short tails and a gliding and flapping flight characteristic of high latitudes. Three monotypic genera are restricted to the Southern Hemisphere, where there are also sibling species of giant petrel Macronectes in the subantarctic and subtropical zones of surface water, while there are closely-related species of Fulmarus in both the Northern and Southern Hemispheres. The Southern Giant Petrel M acronectes giganteus and Northern Fulmar Fulmarus glacialis are polymorphic and may be either dark or pale, the Cape Pigeon Daption capensis and Antarctic Petrel Thalassoica antarctica are chequered brown and white, the pale phase of the Northern Fulmar and its southern representative Fulmarus glacialoides are grey and white, and the Snow Petrel Pagodroma nivea of the antarctic ice is pure white, and remarkable for the possession of 2 races of very different size. All species have broad bills with distensile gular pouches, and all except the Southern Fulmar have some sort of filtering plates or lamellae in the bill. Most probably they once fed mainly on plankton, though the giant petrels at least have always been scavengers and predators; but they have taken readily to feeding behind fishing-boats. They nest in the open or in shallow niches, visiting the nest by day, and have developed oil-spitting as an effective defence. The prions Pachyptila spp. are a group of some 12 very closely-related species and subspecies of small petrel adapted to feed directly upon the smaller organisms in the surface water by straining it through lamellae fringing the bill. They are all very similar in size and appearance, blue-grey above and white below with darker ear-coverts, 'W' markings on the back, and tips to the tail-feathers, and an erratic, mobile, skimming flight; they differ mainly in the size of the bill and its lamellae. The different forms appear to replace each other ecologically in different zones of surface water, feeding in large flocks along the marine convergences at sea and breeding underground on the subantarctic islands in dense warrens which they visit by night. The Blue Petrel Halobaena caerulea is a superficially similar species with a smooth narrow bill and white tips to the tail feathers which appears somewhat intermediate in its structure and behaviour between this group and the next one. The gadfly petrels Bulweria and Pterodroma spp. are a group of some 24 rather similar medium-sized petrels with long wings and short, stout,

heavily-grooved and markedly-hooked black bills; they live far from land in the centre of the oceans. The smaller species, including the primitive northern genus Bulweria, are lightly-built, with fairly long wedge-shaped tails, and a graceful mobile, soaring flight, while the larger members of the genus Pterodroma are sturdy, with shorter rounded tails and a forceful flight in great arcs, between which they may tower in the air. They vary greatly in their coloration and many are polymorphic, but in general they tend to be grey or brown above and may have either white faces and underparts or be equally dark below, though in all plumages they tend to show characteristic wing markings. Comparatively little is known about their biology, but some have a remarkable twisted gut apparently adapted to absorb the oil from cephalopods caught largely at night. They have very long breeding cycles. Some of the larger species visit nests in the open by day on remote southern islands, but most nest in burrows which they visit by night, often in forested mountain slopes far inland. Young birds tend to wander great distances, and, in the Pacific, some appear to carry out transequatorial migrations.

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Great Shearwater Puffinus gravis. (B.P.).

The shearwaters are another large group of some 15 species distributed throughout the oceans, though they tend to be commoner near land. They have longer, more slender bills with smaller hooks, and may also be either dark above and light below or uniformly dark, and some are polymorphic. They may be divided into 2 groups with different flight and feeding habits. Some, including the White-chinned Petrel Procellaria aequinoctialis, Cory's Shearwater Calonectris diomedea and their allies, and the Wedge-tailed and Grey-backed Shearwaters Puffinus pacificus and P. bulleri, are adapted for an aerial way of life, fishing on the wing in the centre of the ocean, which is associated with the development of long wings, tails and legs. Others such as the Grey Petrel Procellaria cinerea, Manx Shearwater Puffinus puffinus, and the remaining members of the genus Puffinus, are adapted for a more aquatic existence diving on fish-shoals offshore. This is associated with the development of shorter wings, tails and legs with flattened tarsi. One species, the Christmas Island Shearwater Puffinus nativitatis, nests more or less in the open on islands in the central Pacific, but they often breed in large, dense colonies of burrows, which they visit by night, near the coasts of offshore islands, though they may also use hills inland. Many species have long and complex migrations between well defined feeding areas in the same or opposite hemispheres. Storm-petrels. The family Hydrobatidae includes 8 genera and over 20 species of small petrel (12-25 em) adapted to catch small marine animals at the water surface. They are all more or less dark above with paler wing coverts, and often white rumps, and vary in colour below. They all breed more or less socially in crevices and burrows, usually on islands, though they may use mainland cliffs or travel inland to nest in deserts. Many carry out considerable migrations, the species from opposite hemispheres replacing each other at different seasons as winter

Petrel

455

alcids behave like the diving-petrels in breeding socially overlooking the sea in holes which they visit by night and where they lay white eggs. The South American group of diving-petrels possess a pointed arch to the lower jaw and comparatively raised, rounded nostrils. They include the largest species, the Peruvian Diving-petrel or Potoyunco Pelecanoides gamotii, which feeds in the cold Humboldt Current and nests on the adjacent guano islands. Further south it is replaced by the medium-sized Magellanic Diving-petrel P. magellani in the channels between the mainland and offshore islands and in the Falklands, and by the Small Georgian Diving-petrel P. georgicus in the subantarctic islands, including South Georgia, Marion and Prince Edward Islands, the Crozets and Kerguelen, and probably Macquarie and other islands south of New Zealand, where there is a colony in the Foveaux Strait. It feeds upon krill Euphausia superba and breeds late in the summer in holes in the sandy upper parts of islands. The New Zealand group is distinguished by the possession of a rounded arch to the lower jaw and flattened, elongated nostrils, and tend to nest early around the vegetated lower slopes of islands and feed upon copepods. They include an uncertain number of forms, notably the medium-sized Common Diving-petrel P. urinatrix, breeding around the Bass Strait in south-east Australia and the main islands of New Zealand,

Wilson's Storm-petrel Oceanites oceanicus. (B.P.).

visitors to the tropics. They may be divided into 2 subfamilies characteristic of different hemispheres, with a wide overlap in range in the intervening area. The Oceanitinae include some 7 more or less highly differentiated forms characterized by the possession of short, rounded wings, nearly square tails, long tarsi and short toes. They are adapted for a distinct mode of progression, walking or hopping along the surface of the water between the waves, picking organisms from the surface as they go. They occur in 2 colour-phases, dark or white below, all species being polymorphic to some degree. Most are restricted to the Southern Hemisphere, but the White-throated Storm-petrel Nesofregetta fuliginosa (= N. albigularis) is resident in the tropical Pacific, the White-faced Storm-petrel Pelagodroma marina has colonized the North Atlantic, and Wilson's Storm-petrel Oceanites oceanicus is a transequatorial migrant which breeds in the antarctic and winters in the northern oceans. The northern Hydrobatinae include some dozen closely-related species which may be derived from Wilson's Storm-petrel, since they also normally occur in the dark phase but may have white rumps. They show a progressive development of a very different type of flight adapted for calmer northern seas, swooping over the surface like terns, which renders them more vulnerable to wrecks. An early stage of development is shown by the British Storm-petrel Hydrobates pelagicus which breeds around the west coast of Europe and winters off South Africa. It reaches its climax in the Pacific, where a minute wedge-tailed species, the Least Storm-petrel Oceanodroma microsoma, occurs off California and a swarm of fork-tailed species of the genus Oceanodroma of different sizes and colours frequent the areas of upwelling there and off Japan and Peru, some migrating to winter in the tropics. Diving-petrels. The family Pelecanoididae contains one genus Pelecanoides which includes 4 or 5 small aquatic petrels (16-25 em) belonging to 2 superspecies which may have originated in South America and Australasia, though they have now developed an overlapping distribution in the Southern Ocean. They are known on Tristan da Cunha as 'flying pinamins' or penguins, and are also remarkable for their similarity to the smaller northern auks, especially the Dovekie or Little Auk AIle alle, which replaces them in the North Atlantic. They are only easily distinguished by their possession of the characteristic tubular nostrils of the Procellariiformes. The resemblance provides an outstanding example of evolutionary convergence in a similar environment, because not only are the 2 groups extremely similar in size, appearance and proportions, both being black above and white below with short bills, wings and tails; they both have a similar whirring rather than gliding flights and dive straight from the air into the water where they use their wings in pursuit of small marine organisms which they collect in gular pouches. Some

Common Diving-petrel Pelecanoides urinatrix. (B.P.).

and a number of very similar small populations breeding at the same sites in the subantarctic islands as the Georgian Diving-petrel and also Tristan da Cunha, Gough Island, the Falklands and probably around southern South America, where it occurs alongside the Magellanic Diving-petrel as well. It seems possible that there may be some overlap in the distribution of the large and small forms of Common Diving-petrel, notably in the Chatham Islands, in which case the small form would rank as a distinct species P. berard. See also ANTARCTIC; OCEANIC BIRDS. See photos AGE; DISPLAY; FEEDING W.R.P.B. HABITS; FLIGHT; NOCTURNAL HABITS. Alexander, W. B. et al 1965. The families and genera of petrels and their names. Ibis 107: 401-405. Bang, B.G. 1966. The olfactory apparatus of tubenosed birds (Procellariiformes). Acta Anat. 65: 395-415. Clarke, A. & Prince, P.A. 1976. The origin of stomach oil in marine birds: analyses of the stomach oil from six species of subantarctic procellariiform birds. J. expo mar. BioI. Ecol. 23: 15-30. Fisher, J. & Lockley, R.M. 1954. Sea-Birds. London. Fleming, C.A. 1941. The phylogeny of the prions. Emu 41: 135-152. jocianin, C. & Mougin, J. 1982. Petrels. In (2nd ed.) Peters' Check-list of Birds of the World, Vol. 1. Cambridge, Mass. Kuroda, N. 1954. On the classification and phylogeny of the Tubinares, particularly the shearwaters (Puffinus). Tokyo. Lockley, R.M. 1942. Shearwaters. London.

456

Pewee

Loomis, L.M. 1918. A review of the albatrosses, petrels and diving-petrels. Proc. Calif. Acad. Sci. (4) 2: 1-187. Murphy, R.C. 1936. Oceanic Birds of South America. 2 vols. New York. Roberts, B.B. 1940. The life cycle of Wilson's Petrel Oceanues oceanicus (Kuhl). Brit. Graham Land Exped. 1934-37 Sci. Rep. 1: 141-194. Swennen, C. 1974. Some observations of the effects of the ejection of stomach-oil by the Fulmar Fulmarusglacialis on other birds. Ardea 62: 111-117. Voous, K.H. 1949. Themorphological, anatomical and distributional relationship of the Arctic and Antarctic Fulmars. Ardea 37: 113-122.

PEWEE: substantive name (in some cases 'wood-pewee') of Contopus ('Myiochanes') spp. (see FLYCATCHER (2)). PEWIT: common alternative name (from the call, and variously spelt) in Britain for the Lapwing Vanellus vanellus (see PLOVER (1)); formerly used also for the Black-headed Gull Larus ridibundus. PEZOPHAPIDAE: family of extinct birds. See under COLUMBIFORMES; SOLITAIRE (now in Pezophapidae, previously 'Raphidae', see DODO).

pH: a symbol followed by a value that is a logarithmic expression of the hydrogen ion concentration of a solution, and thus an index of its reaction. The pH of a neutral solution is 7; above 7 alkalinity increases, below 7 acidity increases.

Red-necked Phalarope Phalaropus lobatus. (A.H.).

PHALAR0 PE: substantive name (coined by Brisson in 1760) of the 3 species of Phalaropodinae (Charadriiformes, family Scolopacidae). They are small, swimming 'sandpipers', breeding in northern latitudes, with dense breast plumage which provides a raft of air on which they float lightly. There are short webs between the bases of the front toes and all 4 toes are expanded and fringed with contiguous convex scales; the tarsus is laterally compressed. Two of the species become seabirds during the 9 non-breeding months; and it is characteristic of all 3 that the sexual roles are reversed, the female being larger and in nuptial plumage more brightly coloured than the male. They are assigned to a distinct subfamily because of their aquatic adaptations, and all 3 have mutually diverged so much that they are placed in separate genera by New World taxonomists. They are Wilson's Phalarope Phalaropus tricolor, the Grey (or Red) Phalarope P. fulicarius, and the Red-necked (or Northern) Phalarope P. lobatus; the alternative English names are those in use in the Americas--the 'Grey' being descriptive of most autumn migrants and the 'Red' of the breeding plumage. Characteristics. Wilson's is slightly the largest (length 23em); it has very long legs and a long needle-like bill, and its toes are evenly fringed, whereas those of the other two are lobed, with a waist at each joint. The Grey (length 20 em) is apparently the most numerous; it has a short bill,

most colourful of the Charadrii; the male plumages are more subdued, and cryptic when the bird sits on the nest. They are unremarkable vocalists, often repeating single soft high notes, tik and peep (also heard at sea); the Grey has additional disyllabic and twittering calls. Distribution and habitat. The Grey and Red-necked are circumpolar breeders, the former mainly in the arctic biome, the latter in the sub-arctic or boreal, but there is some overlap. The Grey is more confined to coastal habitats and often breeds on inshore islands, but both frequent shallow freshwater ponds and lakes; a minority of Red-necks breed far inland. The Red-necked is a rare and rather insecure breeder at several sites on the mainland and islands of Scotland, and until 1971 it bred in western Ireland. The Grey in the British Isles is a sporadic, chieflyautumn, migrant along western coasts, and more rarely elsewhere. In contrast, Wilson's Phalarope is a temperate-zone breeder confined to the interior of North America, from Alberta (probably to 600N) to California (37°N) and east to Ontario. It enjoys a warm summer but many of the ponds and marshes it frequents dry up. It is a bird of inland shores and waters at all seasons, wintering in South America. Movements. The females remain at the breeding colonies only a few weeks, those of the hot-summer species Wilson's being least, and those of the high-arctic Grey most, in a hurry to be off; in all species the majority have left before the peak date of hatching arrives. After the chicks have emerged, the males accompany and brood them; but, only 3-4 weeks after the females have left, the males also aggregate and depart, some of them allegedly deserting small young. Each exodus of adults must relieve the pressure on the food supply, to the benefit of those that stay behind. Finally, after another similar interval, the young themselves are ready to start their long migration. The adults of all species begin their moult before or soon after they leave their breeding places. Most Greys complete it at sea before going south on migration. They are rarely found in the interior of either Asia or North America, and reach their traditional ocean winter resorts near or beyond the equator virtually undetected en route, no doubt largely by sea. An exception is the 4,000 km fringe of the north-west Atlantic, where large numbers are found in autumn feeding and moulting, from Baffin Bay to Nova Scotia, up to 300 km offshore; south of that they disappear. Some may possibly fly non-stop from arctic Siberia to resorts in the Arabian Sea (> 5,000km). The Red-necked, on the contrary, is a conspicuous overland migrant in Asia, funnelling southward in autumn across the steppes, visiting wellknown feeding places, and finally crossing the plateau of Afghanistan/

delicate (length 18em), has the most broadly lobed toes and a bill as fine but not as long as that of Wilson's; in spite of its former American name it is a less northern breeder than the Grey. The Grey and Red-necked in all plumages have dark rumps and show a white wing-bar in flight, whereas the rump of Wilson's is white and there is no wing-bar. All have decorative nuptial plumages, acquired late in spring and, in most individuals, lost before autumn. The various combinations of bay or maroon with white, black, light grey and buff put the females among the

routes in spring (Dementiev et al 1969). In Canada, a less massive overland migration is restricted to the prairies and British Columbia. Red-necks also migrate by sea-routes. Being very light birds, both species are subject to occasional 'wrecks' when caught by gales on migration at sea. At sea both species frequent regions where the mingling of watermasses, or strong offshore winds, lead to turbulence and the appearance of streaks and slicks on the surface, with concentrations of plankton

PHAENICOPHAEINAE: see CUCKOO. PHAETHONTES; PHAETHONTIDAE: suborder and family of PELECANIFORMES; TROPICBIRD.

PHAINOPEPLA: generic name used as common name of P. nitens (see SILKY FLYCATCHER).

PHAINOPTILA: generic name often used as common name of P. melanoxantha (see SILKY FLYCATCHER). PHALACROCORACIDAE: see under

PELECANIFORMES; CORMOR-

ANT.

PHALANX: a bony element (plural 'phalanges') of a digit (see

LEG;

SKELETON, POST-CRANIAL; WING).

unusually broad for a wader. The Red-necked is the smallest and most

West Pakistan and Iran to reach the Indian Ocean. It returns by the same

Pheasant

immediately beneath them (Brown 1979; also OCEANIC BIRDS). The 2 species often keep apart, though by no means wholly. The winter resorts in which the Greys predominate are in the enriched waters off Cape Verde and Angola (Africa), and off Chile (20--400S); the Red-necks are most numerous off the Arabian Peninsula and south of Baluchistan, and over a wide region extending south roughly from Japan to New Guinea, and also off Peru (0--200S) and Argentina. Wilson's Phalaropes migrate overland and southward along the Andes to winter chiefly east of the Cordillera, between the mountains and the Atlantic coast, and especially on the pampas of Argentina. Vagrants have been appearing not infrequently in Britain since they were first detected in 1954, chiefly at migration times. Food. Although in summer phalaropes feed partly ashore, most food is taken at the water surface when they are swimming or wading, and consists largely of insects and small crustacea. All 3 species share the habit of spinning round and round on the water, supposedly to stir up or activate their prey; no doubt the movement is facilitated by having legs amidships, rather than far back like most swimming birds. Sometimes they up-end like ducks, but submerging seems difficult. In the nonbreeding season the Grey and Red-necked live at sea in the tropics or further south, feeding on plankton. Behaviour. All are sociable breeders, usually dispersed in small diffuse groups centred on particular feeding areas or prairie sloughs. In some districts the habitats are extensive, and in suitable parts of south-west Baffin Island and coastal eastern Siberia the Grey Phalarope may be among the commonest birds, reaching 30--200pairs per km 2 (Kistchinski 1975). Apart from defending the actual nest or mate, the females are non-territorial; they make solitary advertising flights over the colony, and there are also aerial chases, usually with one or several females chasing a male. But Schamel and Tracy (1977) also saw mixed chases and chases of a female by males of the Grey Phalarope, which suggests that the roles change when the males have an unmated surplus. Courtship swimming occurs, and copulation with the female swimming on the water can occur in all species; it apparently always does with the Red-necked, and in most instances with Wilson's, whereas the female Grey is normally on her feet either in shallow water or on land. Incidentally the Red-necked and Grey are so tame as to be easily studied at close range. Breeding. Single pair-bonds are the norm. The nest is a scrape with a varying amount of lining. The clutch is 4 eggs, less often 3. Nests are commonly well separated though clumping has been recorded in all species. Incubation (18-24 days) is by the male who alone has broodpatches; their development depends on the typically female hormone prolactin, more of which is secreted by male than female phalaropes. Likewise the female's bright plumage is conditioned by testosterone, normally a male hormone. Depending in part on sex-ratios, single females may frequent the immediate nest-area for much of their mate's incubation period, or they may flock with other females remaining in the neighbourhood (indicating a short-lived pair-bond), or the flocks they join may quit the district. It was long assumed that phalaropes would turn out to be polyandrous, but this has only recently been confirmed, for the Red-necked in Finland and Sweden (Hilden and Vuolanto 1972; Raner 1972), and for the Grey at Barrow, Alaska (Schamel and Tracy 1977). Breeding conditions in the Arctic are notoriously variable, and it appears now that only some females are 'diandrous', and only when there is an excess of males. Graul et al (1977) postulate that reversed sex-roles have evolved in various nidifugous birds which breed in ecosystems where feeding is usually so sparse (and the season so short) as to prevent the female from meeting the cost of incubating the eggs as well as producing them; but, if the male can take over the hatching unaided, the population can still remain viable. Once that has been achieved, it will benefit all concerned still more if, in a spring when feeding is better than usual, a female can attract two batchelors in quick succession and lay each of them a set of eggs, so as to give both enough time to rear their families. V.C.W.-E. See photo COPULATION. Brown, R.G.B. 1979. Seabirds of the Senegal upwelling and adjacent waters. Ibis 121: 283-292. Dementiev, G.P. & Gladkov, N.A. (eds.) 1969. Birds of the Soviet Union, vol. 3. (Translated from the Russian). Jerusalem. Graul, W.D., Derrickson, S.R. & Mock, D.W. 1977. The evolution of avian polyandry. Amer . Naturalist 111: 812-816. Hilden, O. & Vuolanto, S. 1972. Breeding biology of the Red-necked Phalarope

457

(Phalaropus lobatus L.). Ornis Fennica 49: 57-85. Hohn, E.O. 1967. Observations on the breeding behavior of Wilson's Phalarope (Steganopus tricolor) in central Alberta. Auk 84: 220-244. Hohn, E.O. 1971. Observations on the breeding behaviour of Grey and Red-necked Phalaropes. Ibis 113: 335-348. Hohn, E.O. & Mussell, D.J. 1980. Northern Phalarope in Alberta. Canadian Field-Naturalist 94: 189-190. Kistchinski, A.A. 1975. Breeding biology and behaviour of the Grey Phalarope Phalaropus fulicarius in east Siberia. Ibis 117: 285-301. Murphy, R.C. 1936. Oceanic Birds of South America. 2 vols. New York. Raner, L. 1972. Forekommer polyandri hos smallnabad simsnapa tPhalaropus lobatus) och svartsnappa (Tringa erythropus)? Fauna och Flora 67: 135-138. Ridley, M.W. 1980. The breeding behaviour and feeding ecology of Grey Phalaropes Phalaropus fulicarius in Svalbard. Ibis 122: 210-226. Schamel, D. & Tracy, D. 1977. Polyandry, replacement clutches and site tenacity in the Red Phalarope (Phalaropusfulicarius) at Barrow, Alaska. Bird-Banding 48: 314--324.

PHALAROPODINAE: see

PHALAROPE.

PHANERIC: term applied to coloration or other characters that are the opposite of cryptic in that their purpose is to be conspicuous (see COLORATION, ADAPTIVE).

PHARYNX: the cavity of the throat, behind the buccal cavity and leading to the oesophagus and trachea respectively (adjective 'pharyngeal'). PHASE: equivalent of

MORPH

PHASIANIDAE: see under

(see also

POLYMORPHISM).

GALLIFORMES; PHEASANT.

PHEASANT: substantive name of many species of Phasianidae (Galliformes, suborder Galli); used without qualification in Britain for Phasianus colchicus; in the plural serves as a general term for the family. In the pheasants, called by that name, the males have bright colours or elaborate markings; the duller species, mostly a great deal smaller and with shorter tails, are given such names as 'partridges', 'quail', 'francolin', and 'snowcocks', but are not differentiated by any important characteristics, there being in fact a gradual transition between them. American quail are placed in a separate subfamily or tribe, the Odontophorinae, as distinct from the Phasianinae of the Old World. Characteristics. The family is one of terrestrial birds which as a rule feed and nest on the ground, but in the majority of cases roost on trees at night. They are heavy birds; their wings are short and rounded, curved and fitting closely to the body, making them capable of a powerful, fast flight, but-except in some migratory quails--one that cannot be sustained for long (see FLIGHT). The legs are strong, with 4 toes (the hallux inserted somewhat higher than the others) armed with heavy claws, and adapted to scratching; the tarsus often shows a spur, or even 2 or more. The bill is short and thick, the upper mandible overhanging the lower. The tail varies from short to very long, the longest tail feathers being

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Pheasant

Grey Partridge Perdix perdix. (D. W.).

those of Reeves's Pheasant Syrmaticusreevesi and Crested Argus Rheinartia ocellata which reach over I! m in length. The plumage is ample and soft; the sexes are alike in some species, different in others. Most pheasants are easily kept in captivity and are well known as ornamental birds. The most useful domestic bird, the common fowl, derives from a pheasant, the Red ]unglefowl Gallus gallus. Other species such as peafowl Pavo have been kept in complete or semi-captivity for centuries; but they have not yet changed in size or characteristics, although mutations have occurred, such as the 'Black-shouldered Peafowl', 'Melanistic Pheasant', and the 'Yellow Golden Pheasant'. A few of the more spectacular pheasants have figured prominently in myths and legends. This is particularly true of the peafowl which are sacred birds in much of India and appear in Buddhist, Hindu and various pagan mythologies including that of the ancient Greeks. The Buddha is sometimes depicted riding on a displaying peacock, and early Christians used the peacock as a symbol of immortality. A peacock competes with the Crested Argus for identification as the model for the Chinese Phoenix, the Fung-whang, while the Golden Pheasant Chrysolophus pictus has been suggested as the original of the Phoenix itself (see FABULOUS BIRDS). Concrete examples of such myths are to be found in the famous peacock throne of the Moghul and later the Persian emperors, in the heraldic use of peacocks in medieval Europe, or in the use of peacock feathers to denote rank among Chinese mandarins (the long tail feathers of Reeves's Pheasant, worn on the cap, are used to this day in Chinese opera to signify military characters.) For convenience the pheasants are divided into 4 main groups: American quail (18-36 em), These comprise 36 species in 10 genera, of small rotund birds, distinguished from the Old World members of the family in having a stronger bill, the tip and edges of which are sharp and more or less serrated, and by other important anatomical features. Otherwise they resemble the partridges of the Old World and have similar habits. They are, as a rule, brightly and elaborately marked with brown, buff, yellow, reddish, grey, black and white. The tail varies from short to moderately long. The tarsi carry no spurs. The head is often crested and in most species the sexes are different. Old World quail (14-20cm). This group includes 10 species usually placed in 3 genera; they are very small and rounded, and appear tailless with weak bill and legs. The sexes are dissimilar in most species, the males heavily, and in some cases, colourfully marked with blue, brown, black and white. Partridges (16-72 em), The partridges (84 species in about 17 genera) are a large and diverse group of Old World birds with larger bills, stronger legs and longer tails than the preceding groups. The group

includes bush quail, francolins, spurfowl, snowcocks and pheasantgrouse as well as grey-, red-Iegged-, sand-, snow-, stone-, tree-, wood-, and bamboo-partridges. In most species the sexes are similar and cryptically patterned. In a few forest species, notably the Roulro~.d Rollulus roulroul, the male is brightly coloured and crested. They vary In size from the quail-sized bush quail Perdicula to the Himalayan Snowcock Tetraogallus himalayensis which may weigh up to 3 kg. Pheasants (40-235 em). The pheasants proper comprise 48 species in 16 genera, of large but generally more slender birds, often with long, pointed tails and giving lateral displays. In all but one genus, the eared pheasants Crossoptilon, the sexes are different, the males being boldly and sometimes iridescently patterned with blues, reds, greens, and whites, and often adorned with elaborate structures used in display. The group includes [unglefowl Gallus, Peafowl Pavo, and several species well known from captivity such as Golden Pheasants and Silver Pheasants Lophura nycthemera, as well as the 'true' or 'game' pheasants Phasianus. Distribution and habitat. The family in general is distributed throughout the world with the exception of a number of oceanic islands and the polar regions. Most members are natives of the Old World, and apart from artificial introductions, the family is represented in the New World only by the American quails. These are found in the temperate and warm parts of North, Central and South America, from the northern United States (one reaches southern Ontario in Canada) to Peru, Bolivia, Paraguay, and southern Brazil. They are particularly numerous and diverse in the southern United States, Mexico, and Central America. Some live in forests, others on woody or bushy plains and deserts, and a number are found on cultivated land, for example the Bobwhite Colinus virginianus. Some are adapted to life at a high altitude, although they never transcend the limit of the trees. The Old World quail are widely distributed in all the continents of the Old World from Australia to Europe and Africa. There are separate species on Madagascar and New Guinea, but the New Zealand species is now extinct. Quail are typically birds of open country, preferring grassy plains but adapting to cultivated land as well. At least some species roost in tight circles, heads pointing outwards. Partridges are found from Europe to Indonesia, their distribution centred on southern Asia with many species in India, Burma, and Malaysia. Francolins are found mostly in Africa, with only one other (monospecific) genus, the Stone Partridge Ptilopachus present south of the Sahara. Although most partridges live in grassland, scrub and farmland, they inhabit a wide variety of habitats from desert and alpine meadows to dense tropical rainforest. Pheasants are almost entirely confined to Asia. The startling exception to this is the Congo Peacock Afropavo congensis which is restricted to the rainforests of central Africa, where it was only discovered in 1936. Several species have been successfully introduced in other parts of the world, notably Phasianus colchicus which is now established in Europe, North America and New Zealand. Most pheasants inhabit forests, either in the mountains of central Asia and China, or in the tropical rain forests of south-east Asia. A few species are adapted to forest edge (e.g. Gallus), open woodland (e.g. Syrmaticus spp., Pavo), or scrub (e.g. Chrysolophus, Crossoptilon). Ithaginis, Lophophorus and Catreus inhabit scrub, woodland and open grassland on steep, rocky hillsides, and P hasianus prefers patches of dense cover such as tamarisk, scrub or reedbeds, near cultivation, in steppe or in desert. Populations. Pheasants, partridges and quail are of great importance to man as game-birds, providing sport and food. Wild populations are hunted and in Europe and America are sometimes protected and managed. Pheasants (Phasianus) and sometimes partridges (Alectoris and Perdix) are raised in captivity and released to supplement wild populations in some areas. Most species are fairly numerous, but hunting pressure and habitat destruction have already exterminated 2 species (Ophrysia the Indian Mountain Quail, and Cotumix novaezealandiae the New Zealand Quail) and have seriously threatened the survival of at least 16 other species. Most of these are pheasants from tropical and montane forests. However, a number of the endangered species can be bred in captivity and in certain cases (for example the Cheer Catreuswallichii) captive-bred stock has been reintroduced to the wild. There are rumours, too, of rediscovery of the Indian Mountain Quail. Movements. Most pheasants are sedentary in habits and often show strong local attachments. Some mountain species migrate up and down hill at different seasons, and Bulwer's Wattled Pheasant Lophura bulweri

Pheasant 459

is said to be nomadic in search of fruiting trees, but only a few quails of the genus Coturnix are truly migratory. C. coturnix migrates from Europe and central Asia to Africa and India, an astonishing feat for such heavy, round-winged little birds, and Harlequin Quail C. delegorguei of Africa periodically invade suitable areas in large numbers, deserting them again after breeding. Food. The family is mainly vegetarian, but the amount of animal protein taken varies from none to a large proportion of the diet. Pheasants are catholic feeders and rarely specializeon one type or species of food. Important foods include seeds, shoots, berries, roots, bulbs, and insects. Those living in grassland or scrub eat mainly seeds and shoots, while in woodland berries may be more important. In tropical forests, fallen fruit and invertebrates such as grubs and termites are the main items of diet, while at high altitudes in particular, some species (notably eared Crossoptilon, Cheer Catreus, and monal Lophophorus pheasants) are adapted to unearthing bulbs, roots and worms with their feet or bill (Lophophorus uses only its bill and is capable of excavating holes up to 30em in depth in search of bulbs). Peafowl are known to eat lizards and snakes. Desert-dwelling partridges may depend on grasshoppers and locusts, but most partridges and quail are vegetarian as adults. However, the chicks of almost all species in the family are raised on insects and other invertebrates (an exception being snowcock young, which feed on legumes). The current decline of Grey Partridges Perdix perdix in Britain is attributed largely to the increased use of pesticides which kill chick food. Behaviour. A variety of patterns of social organization is found in the family, depending largely on habitat. Most of the American quail and the partridges, living in scrub and open country, are highly gregarious, found for much of the year in 'coveys' comprising one or more family parties. Typically these number between 4 and 10 but in some species living in very bare habitats, such as Callipepela, Colinus, Ammoperdix, Tetraogallus, Lenoa, and Francoiinus spp., such groups may amalgamate to form flocks of 20-40 birds. Most partridges and American quail are monogamous, pairs being formed and maintained all year round; in spring these pairs leave the coveys and remain dispersed during breeding, but they do not defend territories. Some partridges do not gather in coveys, but remain in pairs all year, the broods fragmenting on reaching maturity. These are generally birds such as Rollulus and Melanoperdix that live in dense tropical forests. Except on migration most Old World quail are solitary. Some, however, live, like partridges, in coveys. On the breeding grounds, the males occupy territories which they defend against other males, and in which they sing to attract females who then nest within the territory; they are sometimes polygynous. On migration, they may travel in coveys or larger temporary flocks. Among the pheasants, social patterns are varied and often poorly understood. Those that live in open scrub or open woodland are found in coveys like those of partridges, and are monogamous. Eared iCrossoptiion) and blood pheasants (Ithaginis) often gather in larger flocks of up to at least 20. Coveys break up into pairs in the breeding season. Species living in dense scrub or around the edges of forest are often found in single sex groups or are organized into harems with one male defending each group of females, and surplus males remaining in bachelor groups (for example iunglefowl), Alternatively, the males may defend territories in which live one or more females (for example true pheasants Phasianus and long-tailed pheasants Syrmaticus). Peacocks Pavo defend small aggregated territories resembling leks. Most species,are polygynous, and the males take no part in rearing the young. Species that live in dense forest tend to be more solitary and secretive. Some live in pairs (for example tragopans and the Congo Peacock Afropavo) but others are solitary, and the sexes meet only briefly during the mating season, when males attract females to special display grounds or seek them out (for example argus and peacock pheasants Polyplectron). In some gallopheasants Lophura, the sexes live separately for most of the year, each bird in its own home range, but may gather in flocks at other times. Display and voice. In the quail and partridges, displays are relatively simple affairs; courting males strut around the females with body feathers erected, wings lowered, and tail spread. Patches of colour on the

advertisement by unmated males. Forest species give whistles or hoots the most elaborate forms being the loud, hooting choruses of the tree quails Dendrortyx and the piping, nocturnal song of the singing quails Dactylottyx, Old World quail are more silent except in the breeding season when males give their distinctive song to advertise their territories an~ attract females (the song is a series of high-pitched whistles, quit quit quit repeated many times). Partridges are talkative birds with loud alarm calls, and they are fond of choruses at dawn and dusk. They make a variety of sounds: low, grating creaks (Perdix, Ammoperdix); harsh, staccato sounds, as suggested by the name 'chukar' (Alectoris); cackles (Galloperdix); sharp, high-pitched creaks and twitters (Francolinus Perdicula, Bambusicola), and low, melodious whistles (Tetraogallus)~ Forest partridges give shrill, piping whistles, and some species are fond of duetting, for example Rhizothera longirostris the Long-billed Partridge, and Caloperdix oculea the Ferruginous Wood Partridge. In pheasants, displays are elaborate, colourful and varied. The males of most species display laterally, that is by presenting one flank of their body to the female, with the body feathers and wing lowered on that side, raised on the other, and the tail spread vertically either, in species with flat tails such as tragopans, Koklass Pucrasia and true pheasants, by opening the tail and tilting it on one side, or, in species with compressed arched tails such as gallopheasants, by opening the tail vertically. Such displays exaggerate the size of the performer and reach their most extreme form in the Crested Argus in which the enormous tail feathers (the largest feathers in the world, 15em wide and reaching over 1.5 m in length) are spread, like a sail, in front of the female. Lateral displays are also used in, for example, Phasumus to intimidate other males. Some species do not display laterally or have in addition, different methods. Eared pheasants have simple partridge-like displays, and in long-tailed pheasants Syrmaticus the males strut in front of the females with the feathers of the neck and head erected to give a swollen appearance. Peacock pheasants have both lateral and frontal displays. Monals Lophophorus also display in flight. But the most spectacular displays of all are the great frontal shows of some of the larger, flat-tailed species. In these the tail is erected over the back and spread like a fan, while the wings are lowered or spread and the head is retracted between the shoulders. The effect is to show off the colours of the back (e.g. Lophophorus), wings, tail or tail coverts: in peacocks the latter are enormous and beautifully patterned with metallic ocellae. In the Great Argus Argusianus argus, the secondary feathers are very long and broad and in display they are spread over the back, with the head hidden behind them, so that the bird looks like a huge painted fan. As well as lateral and frontal displays, many pheasants use so-called 'tid-bitting' ceremonies to call their mates to proffered items of food, over which they then display. Displays are often enhanced by the use of special structures, notably bare patches of skin on the face which can be enlarged or flushed at moments of sexual or aggressive excitement. These are normally red, sometimes, in forest species, blue. The commonest forms are the red wattles or facial 'roses' of the true, eared and gallopheasants. In junglefowl, a 'comb' is also present on the crown of the head, and in Bulwer's Wattled Pheasant, the blue facial wattles can be extended beyond the head in front and behind, which, together with the enormous white tail gives this species a bizarre and spectacular display. Tragopans have erectile, bare horns on the head and lappet below the face which can be greatly expanded in display to form a large, blue or yellow bib, patterned with orange, which resembles a brightly coloured piece of silk. Other species possess crests or ruffs used in display. The long, double crest of the Koklass Pucrasia macrolopha can be raised vertically and out from the head, as can the short 'ears' of true pheasants, while in Chrysolophus (Golden and Lady Amherst's Pheasants) the lateral display is enhanced by a beautiful yellow or white ruff, boldly marked with black, which can be spread from the nape to the bill, completely hiding one side of the face. Some pheasants, particularly gallopheasants Lophura, long-tailed pheasants and tragopans, whirr their wings in advertisement displays to announce territory ownership or attract females. Others have loud advertisement calls which may be harsh and grating (Chrysolophus), raucous and deep (Phasianus and Pucrasia), high-pitched and whistling

the crest may be raised and spread. Such display precedes pairing and is not generally repeated before copulation. American quail are on the whole noisy birds; those that live in open country have harsh, repetitive, staccato voices used in alarm calls, choruses at dawn and dusk, or for

wail (Tragopan, Pavo, Argus, Rheinartia). The crowing call of the junglefowl is the well known sound of the domestic cockerel. Apart from crowing calls, some pheasants are talkative and noisy, particularly those that are gregarious like I thaginis, Catreus, Gallus and Crossoptilon, and

face or flank may be exaggerated by the adoption of special postures or

(Ithaginis, Lophophorus, Lophura, Polyplectron), or a plaintive, musical

460

Pheasant, Crow-

make continual clucking or crooning sounds. Others are very silent or like Syrmaticus have weak, quiet voices. Male true pheasants have a raucous, repetitive alarm call, the well known cock cock cock . . . . Breeding. The nest is very simple, usually placed on the ground, perhaps protected by a rock or bush, or situated at the foot of a tree; it may be lined with grass or leaves but not with feathers. In the Crimson-headed Wood Partridge H aematortyx sanguiniceps the nest may be raised on a tussock to avoid flooding, and wood quail Odontophorus of South America are reported to build domed nests; tragopans are unique in building bulky nests in trees. The eggs are plain (white, buff, olive green) or spotted. Clutch size is highly variable: argus and peacock pheasants lay only 2 eggs and most tropical species of all groups lay 3-5 eggs in a clutch. But open country birds lay larger clutches, typically about 8-12; some species lay even more and the Grey Partridge lays probably the largest clutch of all birds, at least 20 eggs in many cases. Clutch size is complicated in Phasianus by egg-dumping habits (several birds may lay in one nest) and in Alectons by 'double-clutching' where the male sometimes incubates a second clutch. There is normally only one clutch in a season, but nest predation is often heavy and birds may re-Iay several times. In most cases the males take no part in incubation, although in monogamous species they may help to rear the young. In at least 2 species, the Golden Pheasant and the Great Argus, the female incubates continuously without ever leaving the nest, even to feed or drink, and without moving for much of the time. The chicks of all species are born fully covered with down and they leave the nest soon after hatching; some have well-developed wing feathers and are soon able to fly and to roost up at night with the mother. Most species mature in their first year, but in a few large pheasants maturation of males in particular is deferred for one or more years and in certain cases (peacocks and argus pheasants) full adult male plumage is not attained for 3-5 years. Such species are often long lived, and one Great Argus survived for more than 30 years in captivity. See photo AGGRESSION. J.T.D. and M.W.R. Allen, D.L. 1956. Pheasants in North America. Washington D.C. Baker, E.C.S. 1930. Game-birds of India, Burma and Ceylon. Bombay. Beebe, W. 1918-1922. A Monograph of the Pheasants, 4 vols. London. Beebe, W. 1926. Pheasants, their Lives and Homes. New York. Delacour, J. 1977. The Pheasants of the World (2nd edn.). Surrey. Hall, B.P. 1963. The francolins, a study in speciation. Bull. Brit. Mus. (Nat. Hist.), Zoo!' 10: 105-204. Howman, K.C.R. 1979. Pheasants, their Breeding, Care and Management. Horncastle. Johnsgard, P.A. 1973. Grouse and Quail of North America. Lincoln, Neb. Potts, G.R. 1980. The effects of modern agriculture, nest predation and game management on the population ecology of partridges (Perdix perdix and Alectoris rufa). Advances in Ecological Research 11: 1-79. Toschi, A. 1959. La Quaglia; Vita-Allevamento--Caccia. Bologna. World Pheasant Association 1980. Proc. 1st Int. Pheasant Symposium, Katmandhu, Dec. 1979.

PHEASANT, CROW-: see

CROW-PHEASANT;

and for family see

CUCKOO.

PHENETIC: term applied in taxonomy to a grouping or arrangement based on observable resemblances that mayor may not also be evidence of phyletic relationship. PHENOLOGY: literally the study of visible appearances, and thus used in respect of seasonally recurring events in animate nature, such as-in the ornithological field-first arrival of a migratory species, first laying of a species, last singing of a species, and the relation of these with meteorological data. PHENOTYPE: the group in which an individual falls by reason of its appearance, which is the result of interaction between external factors and the GENOTYPE; see also GENETICS. PHILEPITTIDAE: see under Oscines; ASITY.

PASSERIFORMES,

suborder Deutero-

PHILOPATRY: fidelity to home area-a term introduced as the English equivalent of ORTSTREUE (see DISPERSAL). PHILYDORINAE: see

OVENBIRD (1).

PHOEBE: substantive name of Sayornis spp. (see

FLYCATCHER (2)).

PHOENICOPTERIDAE: see under

PHOENICOPTERIFORMES;

FLA-

MINGO.

PHOENICOPTERIFORMES: an order, comprising the sole Recent family Phoenicopteridae (see FLAMINGO). In Wetmore's system treated as a suborder Phoenicopteri of the order Ciconiiformes, but other authors consider them more closely related to the Anseriformes, and, more recently, to the Charadriiformes, suborder Charadrii, next to the Recurvirostridae. PHOENICULIDAE: family of PHOENIX: see

CORACIIFORMES; WOOD-HOOPOE.

FABULOUS BIRDS.

PHORESY: transport of one species of organism by another that is not parasitic upon it; the term is applied particularly to insects, e.g. Mallophaga carried by louse-flies on a bird (see ECTOPARASITE). PHORORHACI: see under

FOSSIL BIRDS.

PHOTOGRAPHY: as applied to birds-a comparatively young aspect of ornithology. Although its pioneers were active in the 1890s, it was in fact only during the first decade of the present century, and especially after the First World War, that its impact became important and its practice widespread, until today the camera may be regarded, in varying degrees and with different purposes, as a tool of ornithologists. At one extreme, its object may be purely scientific; at the other, merely recreational-a field sport as it were, with the bird taking second place to the artistic effectiveness of the result. Whilst it is for its scientific value as an aid to ornithology that the camera appeals to the serious student, it is of wide importance in more general directions. Fundamentally, the ornithologist is a collector, as are all naturalists. The museums and private collections are the foundation stone of the science. But as these grew more and more complete, interest turned to the living bird, and with the advent of conservation, as we know it today, aimless collecting fell into disrepute. Here it was that the camera came into its timely own, for with it the instincts of the collector could be satisfied without the need to take life. Again, if today the public is much more 'bird-minded' than even 20 years ago, photography, more than scientific awareness, is one of the main causes. Ornithology, once the hobby of the few, was the interest of those to whom leisure and opportunity gave access. Today it is shared, with vastly differing degrees of seriousness, by all the many who subscribe to societies and clubs that serve birds and their observers (see BIRD- WATCHING).

Illustration. In this minor revolution of our age the bird photographer has played a decisive part. Without illustration it was of little avail to write about, or appeal for, an unknown bird with some strange name. The photograph has added reality and substance to the written word; and the ease with which it can be reproduced has made it available to the public press. Its rise has been at the expense of, or at least has coincided with the decline of, the coloured Plate, and none would for a moment fail to regret that fact. The age, however, of the stately coloured Plate was the age of patronage, and with its passing the photograph filled a vital gap. Moreover, the skill of the painter was confined to the gifted few; the ability to take a photograph, albeit with different degrees of perfection, was open to all capable of mastering its fundamental technique. Thus those who visit distant places are able, either by illustrated books or lectures, to convey visually to the layman their experiences, the countryside, and its birds. This has been the case especially with the moving film, and the influence of bird photography on the public has reached a new peak with its adoption by television. In short, photography in all its guises-monochrome, colour, and cinematography-has gained for birds a very wide audience, not necessarily knowledgeable, but sympathetic and interested; and it is largely from this pool that has sprung modern

'ornithomania' and the general acceptance of the concept of conservation. Scientific applications. In the scientific field, the camera stands supreme in recording bird behaviour, e.g. displays and the like. However vivid the written word, it can never compete with the visual record, with the possibility of frame-by-frame analysis. Electronic flash has enabled the student of avian aerodynamics to see in detail wing positions too fast for the human eye to register. Its ability to stop all movement has assisted in the exact identification of insect food brought by birds to their young.

Piedtail

Photography can also give valuable aid in the enumeration of birds, e.g. sea birds breeding densely on a cliff-face, or flocks of birds such as Anatidae in the open photographed from the air (see CENSUS). Mention may also be made of the photography of radar screens showing birds flying overhead (see RADAR). In systematic work, monochrome or colour photographs of a series of skins are often useful to illustrate an author's point. Trends. Heralded at its advent with acclaim, bird photography has with its increasing popularity come under the fire of criticism. Today pictures of outstanding merit and technical excellence have become the rule, so that the serious ornithologist tends to be scornful of the man who uses a camera but, too often, in his eyes, fails to make any biological contribution along with the photograph. Moreover, photography at the nest, which has for long been the chief focusing point, does entail disturbance. The fact that correct technique and due care of approach can minimize this danger was satisfactory so long as bird photographers were few in number and therefore of little importance. But today many have adopted the pursuit as a field sport, and with numbers the element of possible disturbance becomes of more significance, particularly in the case of rare birds which by their very rarity present a challenge to the photographer. To counter this danger recent legislation has made it an offence deliberately to disturb birds at the nest, and permission for any such photography in Britain has now to be obtained from the Nature Conservancy Council. Consequently there has been a marked reaction from bird-at-the-nest portraits to bird-in-habitat-waders on the tideline, carrion-eaters at bait, birds in flight-in short to illustrate activities rather than to make portraits. Equipment. Until the 1960s most serious bird photography was undertaken with large camera, large lens, and large film or plate and with its going went the infinite beauty of the delicate tones in monochrome and the superb detail of plumage. Such equipment was not easy to use, was cumbersome and heavy and limited in its use. But with the advent of the 35 mm camera bird photography was revolutionized. Small and lightweight bodies, high definition lenses with a great variety of focal lengths ideal for either nest or wait-and-see photography; electronic flash now coupled with the metering system on the camera giving accurate exposures whether used as the main lighting source or as a fill-in to soften harsh shadows; high resolution films in colour and in black and white, with faster speeds making it possible to take photographs that would have been impossible before. Who knows what the future holds in store with the continued rapid advance in photographic technology? One thing is certain: that the computer and video-tape will replace many of the methods used today and these developments will give bird photography new life, new purpose and new areas to conquer. G.K.Y. and E.}.H. Historical

Guggisberg, C.A.W. 1977. Early Wildlife Photographers. London. Kearton, R. 1911. With Nature and a Camera. London. Lodge, R.B. 1908. Bird Hunting Through Wild Europe. London. Pike, O. 1931. Nature Photography. London. Modern Freeman, M. 1984. The Wildlife & Nature Photographer's Field Guide. Beckenham. Gilpin, A. 1978. Nature Photography. Wakefield. Hosking, E. & Gooders, }. 1973. Wildlife Photography. London. Izzi, G. & Mezzatesta, F. 1981. The Complete Manual of Nature Photography. London. Richards, M. 1980. Focal Guide to Bird Photography. London. Warham, J. 1983. The Technique of Bird Photography. (4th edn.). London.

PHOTOPERIODISM: the use of the daily light/dark cycle as a source of predictive information, chiefly in the regulation of seasonal changes in physiological conditions and behaviour. At a given latitude, predictable changes in daylength allow its use by birds and other animals as a proximate factor controlling annual cycles of, for example, breeding, moult and migration in many non-equatorial species. Some species respond directly to increases in photoperiod, beginning the development of, for example, reproductive condition when daylength reaches a threshold value, so that it may be completed in time for the production of young at an opportune season (see BREEDING SEASON). In other species, the seasonal changes in photoperiod may serve also, or only, as a

synchronizer for circannual rhythms (see RHYTHMS AND TIME MEASURE(See also ENERGETICS; MIGRATION; MOULT). Most photoperiodic species become insensitive at a certain time of year to photoperiods which normally would stimulate reproductive development. This phenomenon

MENT).

461

is described as photorefractoriness and its adaptive value is to prevent breeding at seasons when it is disadvantageous. The complex endocrine events associated with photostimulation are reviewed in Murton and Westwood (1977). Baker, l.R. 1938. The evolution of breeding seasons. In de Beer, G.R. (ed.). Evolution. London. Murton, R.K. & Westwood, N.}. 1977. Avian Breeding Cycles. Oxford.

PHYLETIC: used in the same sense as 'phylogenetic' (see

PHYLO-

GENY).

PHYLOGENETIC TAXONOMY: see

TAXONOMY.

PHYLOGENY: sometimes written 'phylogenesis', the evolutionary history of a taxon-contrasted with 'ontogeny', the development of an individual within its own life-span; both 'phylogenetic' and 'phyletic' are used as adjectives. (See TAXONOMY). PHYLU M: a taxonomic category higher than class (see ANIMAL

KING-

DOM).

PHYSIOLOGY: the science of bodily function. The use of chemical and physical methods for this study involves the disciplines of biochemistry and biophysics; or the subject may be divided, according to the particular function studied, into such specialities as neurology and endocrinology. The physiology of birds is dealt with in this work under the names of the various systems of the body, and under other special heads, e.g. HEAT REGULATION; METABOLISM; NUTRITION. PHYTOTOMIDAE: see under

PASSERIFORMES,

infraorder Tyranni;

PLANTCUTTER.

PIAPIAC: Ptilostomus afer (see CROW

(1)).

PICAE: the second order of Linnaeus. PI CARIAE: formerly used as the name of an order, placed next to the Passeres, which included a motley assemblage of groups now placed in the Piciformes, Apodiformes, Caprimulgiformes, Coraciiformes, and Cuculiformes (and by Stresemann in a still greater number of orders), and originally also the birds now placed in the Psittaciformes. PICATHARTINI: see

BABBLER.

PICI; PICIDAE: see below. PICIFORMES: an order, alternatively 'Pici', comprising 2 suborders, Galbulae, Pici; 6 families: Galbulidae (JACAMAR), Bucconidae (PUFFBIRD), Capitonidae (BARBET), Indicatoridae (HONEYGUIDE), Ramphastidae (TOUCAN), Picidae (WOODPECKER). The Galbulae are here divided into 2 superfamilies comprising 5 families; but some authors prefer to place all but the first 2 families in the suborder Pici. The Picidae are divisible into 3 subfamilies-Picinae (typical woodpeckers), Picumninae (piculets), and Jynginae (wrynecks). The relationship of the families is indicated by certain anatomical characters common to all. These include a zygodactyl foot, with a distinctive arrangement of the flexor tendons; also, except in the Galbulidae, absence of down plumage at any age in most species. A specialized form of bill is characteristic of each family. Other characters shared by all of them include those of the bony palate, the rather weak structure of the plate of the breast bone and the general appearance of arboreal birds, reminiscent of early arboreal Passerines, to which they may be actually related. Their wide ecological radiation suggests long periods of development and hence the antiquity of all the families in this order. PICULET: substantive name of Picumninae spp. (see PICUMNINAE: see PIE: see

WOODPECKER).

WOODPECKER.

MAGPIE; TREE-PIE

(for family see

CROW(I)).

PIEDTAIL: substantive name of Phlogophilus spp. (for family see HUMMINGBIRD).

462 Pigeon

PIGEON: substantive name, with 'dove' as a frequent alternative, of

the species of Columbidae (Columbiformes): in the plural general term for the family. In popular speech in England 'dove' is used for the smaller and 'pigeon' for the larger forms, but this usage has not been followed by ornithologists; thus, the Stock Dove Columba oenas is a typical pigeon in every way. Characteristics and distribution. Pigeons vary in size from the Diamond Dove Geopeliacuneata no bigger than a Skylark Alauda aroensis to the crowned pigeons Goura spp., which are nearly as large as hen Turkeys Meleagris gallopaoo (c. 17-90 cm). They have soft, dense plumage with feathers that detach easily, and plump, compact bodies with rather small heads. The wings are usually medium sized but may be rather short and rounded or rather long. The tail may be square ended, rounded or pointed and of variable length. The bill is usually rather small, hard at the tip but soft at the base and with a naked cere over the nostrils. The legs are usually short but are longer in some of the terrestrial species. In most species the female is slightly duller than the male; in some the sexes are alike, but in others the male differs strikingly in colour from the female. The family has been divided into numerous genera, 43 are recognized here; 12 of these are monotypic. The subfamily Columbinae includes not only all the more typical pigeons and doves but also the various superficially partridge-like forms such as the quail doves Geotrygon spp. of Central and South America, the Pheasant Pigeon Otidiphapsnobilis of New Guinea, the many rather small South American doves, and the Australian bronzewings (see later). Most members of this subfamily are primarily seed-eaters; they differ much in colour, but are mostly clad in soft shades of brown, grey or vinous in various combinations. Often they have iridescent, white, or black areas on the neck, wings, or tail that are exhibited in display or when the bird takes wing. The subfamily Treroninae consists of a probably bi-phyletic and possible polyphyletic assemblage of arboreal fruit -eating species. Among them are the green pigeons Treron spp. of the Afrotropical and Oriental regions. These are primarily soft green in colour, often with beautiful yellow, orange or mauve markings and brilliantly coloured eyes and ceres. Unlike other fruit pigeons they have hard, muscular gizzards, and digest the seed of the wild figs on which they largely feed. The often brilliantly coloured fruit doves of the genus Ptilinopus and the larger imperial pigeons Ducula spp. differ from each other in size and in the more diverse colours found in the smaller species; they are widespread in the Indo-Malayan and Pacific areas, a few species reaching India proper and Australia. The New Zealand Pigeon Hemiphaga novaeseelandiae and the very distinct Top- knot Pigeon Lopholaimus antarcticus of eastern Australia are probably related to them, as the blue fruit pigeons Alectroenas spp. of the islands of the Indian Ocean almost certainly are. All these forms have a broad gut and void intact the (often large) seeds of the fruits which they swallow whole. The subfamily Gourinae consists of 3 closely related crowned pigeons Goura spp. of New Guinea. They have large, laterally flattened crests of lacy-looking disconnected or spatulate-tipped feathers. The subfamily Didunculinae comprises only one species, the Toothbilled Pigeon Didunculus strigirostris of Samoa. Only a few of the more noteworthy of the 255 species of pigeons can be mentioned individually here. The Rock Pigeon or Rock Dove Columba livia, a native of Europe, western Asia, India and north Africa, is the ancestor of the many breeds of domestic pigeons and of their feral descendants now common in towns (and often also in the country) throughout most of the world (see DOMESTICATION; HOMING PIGEON). The wild form is bluish grey with two black wing bars and an iridescent neck. It roosts and breeds in caves and on sheltered cliff ledges and feeds on the ground, usually in open areas. The long-tailed Passenger Pigeon Ectopistes migratorius of eastern North America was remarkable for its extreme gregariousness, nesting and migrating in enormous flocks. Unfortunately this made it very vulnerable to human predation and it was exterminated in the wild by 1894 after a long period of relentless exploitation by man (see EXTINCT BIRDS). A closely related but smaller and less brightly coloured species, the Mourning Dove Zenaida macroura, is still common, ranging from Alaska to Panama. The African Collared Dove Streptopelia roseogrisea is the ancestor of the domesticated Barbary Dove or Blonde Ringdove and its white variety the so-called 'Java Dove'. A related Asian species, the Collared Dove Streptopelia decaocto, has recently spread across Europe in a remarkable

Victoria Crowned Pigeon Goura victoria. (D.A.T.).

manner; the first one to be seen in Britain was in 1952; now it is a common and characteristic bird of lowland villages, suburbs, farmsteads and some towns, throughout Britain. The little Masked or Namaqua Dove Oena capensis of Africa and Madagascar frequents open country and is of nomadic habits. It has a very long, graduated tail and shows marked sexual dichromatism, the male having a black face and breast bordered with pale grey, while these areas are light drab in the female. Another strongly dichromatic species, with a most unusual type of sexual difference, the Flame Dove or Orange Dove Ptilinopus victor of Fiji is unique in colour: the male is vivid orange with an olive-yellow head, and the female dark green but with her head the same colour as her mate's. The Australian bronzewing pigeons of the genera Phaps, Geophaps, Ocyphaps and Petrophassa are good examples of adaptive radiation. Although they have diverged greatly in the course of their speciation and adaptation to different biotopes, their colour patterns and behaviour still show their close phylogenetic affinities. They include the only 2 genera, Ocyphaps and Geophaps (subgenus Lophophaps), which have long, pointed crests. Habitat. Pigeons, of different species, inhabit many types of country, from rocky uplands and scrub-grown semi-desert to tropical forest. Most species are at least partly arboreal but a few are terrestrial or cliffdwelling. The family is almost cosmopolitan, being absent only from the Arctic, sub-Arctic, Antarctic and sub-Antarctic areas and some oceanic islands. Feral populations of Columba Livia now exist in some places where no wild species lives or is thought formerly to have done so. Food. Seeds, fruits, berries, flowers and young leaves are the main foods of pigeons but many species also take small snails and/or other invertebrate animals. Some, perhaps most or all, also take such mineral substances as salt-impregnated earth and crushed shell. Most pigeons have strong, muscular gizzards and long, narrow intestines, but in some of the fruit-eating species, the stomach is designed for rubbing off the pulp or pericarp of fruits rather than grinding seeds and the gut is short and wide. These latter birds digest only the pulp of the fruits they eat, voiding the stones intact. Pigeons drink by immersing the bill and sucking, a habit shared with some estrildid finches but one which many species that do not habitually practise it, can and do use when necessary. Behaviour. Most pigeons are strong flyers and some are migratory or nomadic. Some species, however, spend much of their time on the ground and make use of their wings only in an emergency or to fly up to perch on a branch or rock. Most of the species whose behaviour is known are to some extent gregarious when not breeding, some gathering into large flocks. Some species often or usually breed colonially; and in others large numbers of individuals may congregate at good feeding places even in the breeding season. An old writer on domestic pigeons noted that 'These birds have many pretty and whimsical gestures when that they are salacious'. It would be

Piracy

difficult to make a more succinct and yet appreciative statement. Suffice to say that courtship displays are often similar to, though seldom identical with, those used in threat and that, as in other birds, they exhibit bright or striking parts of the plumage or soft parts to best advantage. Pigeons pair at least for the duration of a nesting cycle, in most known cases for an entire breeding season and sometimes for life. In many species the male drives his mate away from potential sexual rivals during the period that she is sexually receptive. The copulation ceremonial may be comparatively short and simple as in the doves of the genus Streptopelia or surprisingly involved and 'complicated' as in some of the Australian forms such as the Diamond Dove Geopelia cuneata. Voice. Typically pigeons utter cooing, crooning or booming calls and inflate their necks when so-doing. Some utter whistling, screaming, harsh or cackling cries in lieu of or additionally to cooing. Some usually or often punctuate their display flights with loud wing-clapping. Rather similar, but less deliberate-seeming, more rattling or clattering wing claps may be made (by some species, including the Rock Pigeon and its feral descendants) when the bird suddenly takes wing in alarm or when it intends to fly fast for some distance, for example to a feeding site some miles away. Breeding. All species whose behaviour is known build a shallow, usually slight but often strongly interwoven nest of twigs, wiry stems, thin roots or similar materials; species that nest on the ground, on ledges or in holes may sometimes dispense with nesting material although more usually they build some sort of nest. One or (in a majority of species) 2 white or (less often) buffish, unmarked eggs are laid. From these hatch helpless nestlings clad sparsely in coarse down which is usually yellow or buff in colour. The young insert their soft bills into their parents' mouths and are fed by regurgitation. They grow rapidly as a rule; some of the smaller species can fly before they are 2 weeks old. Some of the larger species, such as the New Zealand Pigeon, take longer than most and the Nicobar Pigeon Caloenas nicobarica is said to grow astonishingly slowly, not fledging until 3 months old (Nicolai 1969). The female usually does most or all of the building, the male bringing her materials. Both sexes share in incubation (from 14-18 days) and care of the young. Both produce 'pigeon's milk', a nutritious curd-like substance formed by the proliferation and sloughing off of the cells of the lining epithelium of the crop (see CROP MILK); for the first few days this constitutes the sole food of the young. The fledged young are fed by both parents, or by their father only, until at least some days after they are strong on the wing. D.G. Creme, F.H.J. 1975. Breeding, feeding and status of the Torres Strait Pigeon at Low Isles, north-eastern Queensland. Emu 75: 189-198. Goodwin, D. 1967. Pigeons and Doves of the World. London (3rd edn 1983). Nicolai, J. 1969. Tauben. Haltung-Zucht-Arten. Stuttgart. Whitman, e.o. 1919. The Behaviour of Pigeons. VoL 3 of the posthumous works of e.o. Whitman. Washington.

PIGEON, CAPE: sailors' name for the Pintado Petrel Daption capense (see PETREL). PIGEON, HOMING: see HOMING PIGEON MILK: see CROP PIGMENT: see COLOUR;

PIGEON.

MILK.

EGG; PLUMAGE.

PIGMENTS, VISUAL: see VISION. PIHA: substantive name of Lipaugus spp. (for family see COTINGA). PILEATED: crested or capped, referring to the shape of the crownfeathers. PILOT-BIRD: Pycnoptilusfloccosus (for family see WREN

(2».

PINEAL BODY: see NERVOUS SYSTEM (Fore-brain). PINFEATHER: a growing feather still in its sheath. PINION: poetical word for a wing; sometimes applied to the part of the wing comprising the primary feathers, or even to a single one of these.

463

PINIONING: rendering a captive bird permanently incapable of flight by cutting one wing at the carpal joint and so removing the basis from which the primary feathers grow (compare CLIPPING). This procedure makes it possible to keep waterfowl and reasonably large ground-birds in the open; it is the lopsidedness, more than the reduction in wing area, that is effective. PINKFOOT: colloquial short name (plural 'pinkfeet') for the Pinkfooted Goose Anser fabalis brachyrhynchus (see under DUCK). PINTAIL: substantive name of certain Anas spp.; used without qualification for A. acuta (see DUCK). PIOPIO: native name for Tumagra capensis, also known as the New Zealand Thrush, a bird of uncertain affinities but usually placed in the Turnagridae (see THRUSH, NEW ZEALAND). PIPIT: substantive name of species of Anthus and related genera (see under WAGTAIL). PIPPED: see HATCHING. PIPRIDAE: see under

PASSERIFORMES,

suborder Deutero-Oscines;

MANAKIN.

PIQUERO: alternative name for Sula nebouxii (see GANNET). PIRACY: term describing a range of inter- and intraspecific foodstealing activities (also called clepto- or kleptoparasitism). Food items procured by one individual (the 'host') are forcibly stolen by another (the 'pirate' or kleptoparasite). What distinguishes piracy from the many other types of feeding interaction is the fact that the host is usually harassed, often violently and for long periods, into giving up items of food. The pirate may snatch food from the host's grasp or the host may drop an item on being chased. Frequently, however, the host is harried into regurgitating food which has already been swallowed. Severalpirates may harass one host individual at a time and may steal food from each other once it has been secured. 'Piracy' of nest material also occurs, but this article is only concerned with food-stealing. The distribution of piracy among birds. Piracy occurs in many animal groups but it is particularly widespread among birds. Its distribution across the various orders, however, is far from random. Only one duck, the American Wigeon Anas americana, is a regular pirate although ducks are frequently found in mixed species flocks and are themselves hosts for a number of pirate species. Piracy has never been recorded among the seed and fruit-eating Galliformes, Columbiformes and Psittaciformes and is sporadic among passerines even though these constitute the vast majority of bird species. On the other hand piracy is extensive among the Accipitriformes, Falconiformes and Charadriiformes (particularly the families Stercorariidae and Laridae). These 3 orders together contain 600/0 of recorded pirate species but only 70/0 of the known bird species of the world. The frequency of piracy within an order is therefore not simply a reflection of the number of species it contains but appears instead to depend on particular ecological conditions which make piracy profitable. Species of some orders encounter these conditions more often than those of others and the pirate individuals are favoured by natural selection. Conditions favouring piracy. Regular association of one type or another is an obvious prerequisite for the development of piracy. When raptors pursue prey the latter may drop or regurgitate food to avoid capture. Raptor species may then begin to harass rather than capture 'prey' to obtain already immobilized food. Turkey Vultures Cathartes aura, for example, which commonly prey on young Great Blue Heron Ardea herodias chicks, sometimes attack older nestlings. As part of their (successful) defence mechanism, older chicks regurgitate food which the vultures then feed to their own offspring. Various raptor species have also been recorded snatching food from one another including one observation of a triple piracy where a Sparrowhawk Accipiternisuswas robbed by a Merlin Falco columbarius, the Merlin by a Honey Buzzard Pemis apioorus and the Honey Buzzard by a Peregrine Falcon Falco peregrinus.

Piracy is commonest in mixed species colonies of seabirds. In tern colonies, adults steal both from each other and from feeding chicks, and gulls nesting in the colony steal from the terns and from conspecifics. In colonies of Puffins Fratercula arctica and Black Guillemots Cepphus grylle,

464

Piscivorous

Arctic Skua S tercoran us parasiticus parasitizi ng Lesser Black-backed Gull Larus fuscus . (P hoto: P . Muns/ ennan ).

Jackdaws Corvus monedula, gulls and even terns operate as grou nd-based pirate s while skuas tS tercorarius spp. ) and some gulls attack the auks as they retu rn with food to their burrows. Other associations in which piracy is common are single and mixed species feeding flocks (e.g. Black-headed Gulls L aTUS ridibundus ro bbing Lapwings V anellus uanellus of eart hworms), and associations based on scavenging and predator mobbing responses. The mobb ing response app ears to be the origin of Magpies P ica pica stealing from Golden Eagles A quila chrysaetos and of crows stealing from harriers, falcons and kit es. Pirates are most likely to attac k when food carr ied by the host is large, visible, of high qual ity or is scarce and when the host is unlikely to escape. Many species which show piracy are dietary opport unists. In th ese cases piracy is one of many feedi ng strategi es which may be empl oyed at different times. For exampl e the omnivorous House Spar row Passer domesticus has been recorded stealing imm obilized katydid s (Orthoptera) from female digger wasps (S phex spp. ). Several gull and egret species are similarly opport unistic pirates. Some species, however, obtain a large pr oporti on of their food through pir acy. T he frigatebirds (F regata spp .), skuas and jaegers (S tercorarius sp p .) arc probabl y the best kn own ' profess ional' pirates. Specializations for piracy in frigate birds include a vestigial urop ygial gland which greatly redu ces the amount of oil in the feathers and the largest wingspan : body-weight ratio of any bird species. These features enhance acrobatic flight but they also mean the bird s can no longer enter th e water from which most of their food originates. (R. M.) C.J .B. (I ) Brockm ann , H .] . & Barn ard , C.] . 1979. Klept oparasitism in bird s. Anim . Behav. 27: 487-514. Kiillande r, H. 1977. Piracy by Black-headed Gulls on La pwings. Bird Study 24: 186- 194. Meinertz hagen, R. 1959. Pirates and Pred ators. London .

PISCIVOROUS : fish eating. PISHING : sque aking (see H UMAN IMITATION OF BIRD SOUNDS). PITOHUI: substantive name of the 7 species of Aust ralasian pachyceph aline flycatchers of the genus P itohui (see THICKHEAD). PITTA : substantive name of the species of Pittidae (Passeriformes, subo rder Deutero-Oscines, infraorder Pittae); in the plural, general term for the family. The pittas compr ise a rath er uniform family of 29 species, usually placed in the single genu s P itta. They arc mostly confined to the Old World tropi cs, with their cent re of diversity in Sout h-cast Asia where 22 species are found . In 1876 the pittas were placed with th e New World Deutero-Oscines

on the basis of syringeal morph ology, bu t it is a simple type of syrinx and now considered to be unreliable as an indicator of relationships. However , the result of recent anato mical and biochemical stu dies is that the pittas occupy an isolated and highly enigmatic position nearest to the New World Deut ero-Oscines, Fu rth er to th is, the latest volume of Pete rs' 'Check-list of birds of the world' (1979) chose to include the Pittidae in the suborder In certae Se dis. The wing has 10 primaries, the outer most long, and 12 rectrices. The tarsus has a long anterior and a posterior plate. Characteristics. Pittas' size range is 15- 28 em ; weights vary between 42 and 2l 8g. Fift een male Fairy Pittas P itta nympha collected on Taiwan in May had a range of 67.5-1 55 g and a mean of 109g. They are stocky, long-legged , short -tailed bird s and in the field some species might be confused with ground thrushes, the group with which they were originally placed . T hey have also been called 'ant-thrushes' or 'jewelthrushes' . The plumage of man y pitta s is highly colourful. Much of the bright coloration, however , is on the underparts, while the more protectively patterned upperparts effectively conceal them in the dim light of the tropical forest floor. Nin e species are sexually dimorphic, 4 with brightly coloured males and dr ab females. Ju venile birds are more brownish and mottled or spo tte d. Habitat. Moist evergreen or decidu ou s forests, bamboo groves, mangroves, dense secondary scru b and wooded ravines in more open areas; up to 2,500 m . Distribution. Widespread in the Oriental Region as resident s and/or migrants, extending nor th to Japan (one species), east to Austral ia (3) and the Solomon Island s (one) and also tropical Africa (one). Populations. Man y forms are considered rare, but thi s is partl y du e to their retiring hab its; pitt as may be locally common. Movements. Generally sedentary , wit h local or seasonal dispersal, also altit udinal. Eight form s are migratory, including the Ind ian Pitta P. brachyura from the Himalayan region to sout hern Ind ia and Sri Lanka, the Fai ry Pitta from Japan to Born eo and the African Pitta P. angolensis in east and centr al Africa . Some long dista nce vagrancy has been recorded, e.g . the Blue-winged Pitta P. moluccensis has reached NW Australia . Pit tas are nocturnal migrant s and their attraction to lights has provided many records. A study of migrating bird s at F raser's Hill, West Malaysia, revealed the following per iods for the 2 regular migran ts, the Blue-winged Pitta and the Hooded Pitta P. sordida: 25 September22 December and 7 April-9 May. Food. Insects, spiders , worms and part icularl y snails; small shrimps, crabs, lizard s or snakes may also be taken . Other food has seldom been record ed , e.g. the Garn et Pitt a P . granatina on Borne o taking large seeds and Schn eider's Pitta P . schneideri of Sum atra taking vegetabl e matt er . A captive Hooded Pitta studied for one month ate approximately its own

Plains-wanderer

weight in food each day. Behaviour. Normally all pittas live singly or in pairs, but larger groups may occur during migration. Pittas spend most of their time foraging on the ground where they hop about, often flicking and bobbing their tails. If disturbed, they will hop away or fly a short distance, keeping near the ground; in some commoner species this reveals a conspicuous white wing patch. When foraging, pittas flick the leaves and other vegetation over with their strong bills and may sometimes use slight wing flicking movements to flush small prey ahead of them. A stone or log is used as an anvil to break snail shells. An ability attributed to pittas of locating prey by smell is supported by a study of their olfactory system, with the largest olfactory ratio among the Passeriformes. This is exemplified by the captive Hooded Pitta mentioned above that actively sought worms by digging the entire bill into the soft earth provided. Pittas are shy and retiring birds and often only located by calls, an imitation of which will usually bring them into view; outside of the breeding period they may be more silent. When calling, pittas have been observed up to 10m above the ground and short looping flights may be performed from a perch. At night pittas usually roost in trees. An aggressive display observed in a few species involves crouching with fluffed out feathers, wings spread and bill pointed upwards. The distinctive Eared Pitta P. phayrei has long plumes at the side of the nape that may have a special function, as all species have erectile crown feathers, elevated when excited. Voice. A short series of variably pitched whistles, often dissyllabic, is characteristic; also trilling, rolling sounds. Calls may be heard during the day from some species but most often at dawn and dusk, before rainstorms, and on moonlit nights, when some neighbouring birds may call against each other or in chorus. Breeding. The breeding season is variable. In distinctly seasonal areas, pittas are summer breeders, especially the migratory species. Otherwise, as in South-east Asia, they breed in all but the wettest months. The nest may be found up to 8 m above the ground, but usually under 3 m or even on the ground. Sites include stumps, amongst root buttresses of large trees, against banks or fallen trees, in tangled clumps of vegetation or rock clefts. The nest is an untidy globular or elliptical structure of twigs and rootlets often decorated with moss, lined with finer materials and with a low side-entrance. A doormat of animal dung outside the nest is made by the Australian Noisy Pitta P. versicolor. Average dimensions for some nests of the Blue-winged Pitta were: external diameter 20 em, internal 16cm, depth 7.5 em, and entrance 10cm wide. When disturbed, the bird may cover the entrance with a small, leafy twig. So far as is known, both sexes share in nest building, incubation and the care and feeding of the young. The clutch size is 2-7 eggs, but usually 3-5; they vary from a broad blunt oval to a spheroidal shape, some with a large amount of gloss, and are white or buffish with reddish or purplish

465

spots or speckles and fine grey or lilac undermarkings. Fifty eggs of the Indian Pitta measured 23.3-28.2 x 20.0-22.4 mm, with a mean of 24.7 x 21.2mm; average egg weight from a clutch of the Blue-winged Pitta was 5.2 g. The incubation period for a captive Hooded Pitta was 17 days. This was for the first breeding in captivity by J. Delacour (1934). Pittas are difficult to keep and have seldom been bred, partly due to their pugnacious nature. The young hatchlings are fleshy or purplish coloured, sometimes with tufts of natal down on the upperparts. M.D.B. Benson, C.W. & Stuart Irwin, M.P. 1964. The migrations of the pitta of eastern Africa (Pitta angolensis longipennis Reichenow). N. Rhodesian Journ. 5: 465-475. Delacour, J. 1934. Breeding the Hooded Pitta (Pitta cucullatay. Avic. Mag. (4) 12: 222-226. Garrod, A.H. 1876. On some anatomical characters which bear upon the major divisions of the Passerine birds. Part I. Proc. Zool. Soc. Lond. 1876: 506-519. Harrisson, T. 1964. Food capacity of a Green-breasted Pitta P. sordida. Sarawak Mus. journ. 11: 611-615. King, B.F., Woodcock, M.W. & Dickinson, E.C. 1975. A Field Guide to the Birds of South-east Asia. London. McClure, H.E. 1974. Migration and survival of the birds of Asia. Bangkok: ASRCT. Peters, J.L. 1979. Check-list of Birds of the World, vol. 8 (Traylor, M.A. Jr, ed.). Cambridge, Mass.

PITTA, ANT-: see ANTPITTA; PITTIDAE: family of

ANTBIRD.

PASSERIFORMES;

suborder Deutero-Oscines;

PITTA.

PITUITARY GLAND: see ENDOCRINOLOGY

AND THE REPRODUCTIVE

SYSTEM; NERVOUS SYSTEM.

PITYRIASIDIDAE: a family of

PASSERIFORMES,

suborder Oscines;

BRISTLEHEAD.

PLAINRUNNER: substantive name of Coryphistera alaudina and Clibanornis dendrocolaptoides (see OVENBIRD (1)). PLAINS·WANDERER: alternatively 'Collared Hemipode', Pedionomus torquatus, sole member of the Pedionomidae (Gruiformes, suborder Turnices). Pedionomus is placed apart from the buttonquails (Turnicidae) on account of the persistent hind toe, the pyriform instead of oval eggs, and the persistence of paired carotid arteries: but many consider separation as a subfamily (Pedionominae) sufficient. Characteristics. The Plains-wanderer is a small bird (male c. 10em, female c. 12 em), Although superficially like a buttonquail Turnix sp., the Plains-wanderer typically does not exhibit the crouching posture but stands erect like a bustard (Otididae); an interesting photograph published by Purnell (1915) shows clearly the bird's habit of standing 'elevated on its toes' so as to achieve a wide view of the surroundings. The bill is slender and of medium length. The wings are short and rounded, the tail is very short, and the whole body is compact. The plumage shows a cryptic pattern of reddish-brown, buff, and black, paler below; there is a 'collar' of black spots on a white ground. Sexual dimorphism is marked, the female having a chestnut-coloured breast. They are usually loth to fly, preferring to run or 'freeze', and have on occasions been caught by hand. They have a whirring flight like that of a buttonquail. Habitat. Plains-wanderers inhabit open grasslands and plains of south-eastern Australia, where they keep to open areas and avoid the scrubby sections and stubble that are favoured by most buttonquail species. Distribution. The breeding range is from Duaringa, Queenland, in the north, to western New South Wales, Lake Frome (one or two records) and south-eastern South Australia. Most recent records are from Victoria. D'Ombrain (1926) has reviewed certain aspects of the scanty knowledge of the habits of the species, speculating about the reason for its rarity in modern times. Recent records in South Australia, Victoria and New South Wales are widely dispersed but uncommon. Alteration of habitat due to sheep, rabbits, and fires, and the introduction of the fox

Noisy Pitta Pitta versicolor. (N.W.C.).

and feral cat, have undoubtedly contributed to the numerical reduction of the species. Food. Such stomach analyses as have been carried out disclose the presence of insects, seeds, vegetable matter, and sand.

466

Plaintain-eater

Plains-wanderer Pedionomus torquatus. (C.].F.C.).

Breeding. The breeding season is described as being from September to January. The nest is a slight depression in the ground, and 4 eggs make up the clutch; they are pale yellowish or greenish, spotted with grey and olive. The male incubates the eggs and raises the young. (A.K.) H.J.F. Crome, F.H.J. & Rushton, D.K. 1975. Development of plumage in the plainswanderer. Emu 75: 181-184. D'Ombrain,E.A. 1926. The vanishing Plains-wanderer Pedumomus torquatus. Emu 26: 59-63 (map). Purnell, H.A. 1915. The Plains-wanderer in captivity. Emu 15: 141-143 (photograph).

PLAINTAIN-EATER: substantive name (unfortunately misleading) of some species of Musophagidae (see TURACO). PLANTAR: pertaining to the posterior surface of the tarsus (equivalent to the sole).

PLANTCUTTER: substantive name for 3 species of Phytotomidae

(Passeriformes, infraorder Tyranni); in the plural, general term for the family. Phytotoma is a single, polytypic and purely neotropical genus, its 3 species being very alike. Characteristics. Planteutters are heavily built finch-like birds about the size of an European Hawfinch Coccothraustes coccothraustes (1819.5 em), having short wings, rather long tails and with crown feathers pileated to form a slight crest. The plumage on the upper parts is plumbeous and/or brown, in the male streaked more heavily with black. The throat, breast and underparts of the female are light buff and dull ochre with dark streaks; these colours being replaced in the male by bright rufous and chestnut. The males of all species present a conspicuous white wing-bar. Tails in Phytotoma rutila and P. raimondi are blackish with white tips; in the case of P. rara they are black-tipped with chestnut coloured inner webs. Immatures tend to look like females. Legs are short and feet large in comparison; the bill is stout, short, conical and finely serrated in both mandibles. Eyes are bright amber or yellow in both sexes. Habitat and distribution. Plantcutters are typical of bushy and low woodland, preferring rather open country; also well adapted to cultivated fields and orchards where they may cause damage. They are found from about 3,000 m in Andean valleys down to the coast. They have enlarged their range and, locally, their numbers due to increasing cultivation. But intensive pesticide spraying on parts of this artificial habitat may eradicate a whole population. The genus is mainly distributed in western and southern South America. The smallest species, Phytotoma raimondi, the Peruvian Plantcutter (total length c. 18 em) is confined to the coastal fringe of northern Peru between Tumbes and Lima. The Chilean Plante utter Phytotoma rara, the largest representative (19.5 em), has been observed in Chile

from Atacama to Magallanes and along the Andean foothills of Argentina from Neuquen to northern Chubut. The Red-breasted Plantcutter Phytotoma rutila (19 em) is distributed in SE Bolivia, Paraguay, Uruguay and Argentina south to Rio Negro. Movements. Plantcutters are generally sedentary in lowlands, but high-level and southern populations migrate respectively down and/or north during autumn and winter seasons. Food. The genus is entirely vegetarian. The bill is admirably adapted for plucking buds, shoots, tender leaves and different fruits. The birds, being provided with such an instrument of destruction, are considered one of the worst enemies to fruit and horticultural plantations. Behaviour and voice. Plantcutters are commonly observed in pairs and, at the end of the breeding season, family groups are typical. Small flocks of 6 to 12 individuals may be observed flying or foraging together in loose association. They tend to be territorial during the breeding season, males making their presence known by an oft-repeated rasping metallic wheeze. When approached they fly off with an undulating rather sluggish flight to perch on top of another nearby shrub and utter again their unmusical rattle. Breeding. Nesting starts in October and continues into January for Andean populations. The nest is loosely made, flat, untidy and built almost entirely with root fibres. It measures about 10-12 em in diameter and is usually placed in the fork of horizontal branches near the top of low trees or shrubs. Clutch-size 2-4 eggs; these are greenish-blue, sparsely dotted with dark markings which have a tendency to zone at the broad end. (J.D.G.) R.P.S.

PLASMA: see

BLOOD.

PLATALEINAE: see SPOONBILL. PLA Y: an activity performed by a wide variety of bird species; although probably less common in birds than in mammals (Kilham 1974; Ficken 1977). Playful behaviour in young animals may be important in the development of social behaviour and social relationships and may also be useful in the development and/or 'polishing' (or practising and learning) of specific motor skills (but see BEHAVIOUR, DEVELOPMENT OF.) Also, play may result in increased flexibility of behaviour (Ficken 1977). Some birds, as do many mammals (Bekoff and Byers 1981), even use play invitation signals to solicit play from other individuals. Play behaviour in birds may take on a number of different forms including mock-fighting, sexual behaviour and courtship, reciprocal chasing and fleeing, and the performance:of rapid motor sequences such as 'nose-diving' at other birds or performing somersaults in water, and may involve playing with food objects or even making snowballs (Kilham 1974; Keller 1975; Ficken 1977). Social play is probably less common than object play.

Chilean Plantcutter Phytotoma rara. (C.E.T.K.).

Plover

Young raptors have been observed to make hunting movements towards inedible objects and Red-bellied Woodpeckers Centurus carolinus will try to put miscellaneous objects such as bent nails in crevices otherwise used to store food (Kilham 1974). Young Christmas Island Frigatebirds Fregata minor minor will swoop at, pick up, and then drop, leaves and other objects floating on the surface of the sea. Vocal play also may occur. Subsong shows some close similarities with characteristics of nonvocal mammalian play (Ficken 1977). Play by adults is more difficult to understand than is play by young (as is the case in many mammals). Rooks Corvus frugilegus will commonly indulge in tumbling acrobatics; Ravens C. corax have been described as carrying up twigs or pieces of heather, which they drop and then catch again in the air. Various aquatic birds, e.g. Eider Somateria mollissima and Black Guillemot Cepphusgrylle, have been seen to disport themselves in swift currents in a way that suggests that the birds are 'having fun'. Similarly, Adelie Penguins Pygoscelis adeliae have been described as riding in vociferous parties on small iceflows in a tide race, only to swim back to the starting point and begin once again. That play may indeed be enjoyable has been suggested for mammals as well (Bekoff 1976). Adults (and probably young) seem to play most when they are undisturbed and when other more pressing needs (such as food, shelter, warmth) have been satisfied. As in mammals, play rarely occurs when individuals are disturbed or stressed. In many cases it is very difficult to separate playful from non-playful activities, regardless of how amusing the behaviours appear to the human eye. More quantitative data are needed regarding avian play and it would be useful if a list of play criteria could be developed. One should not expect a priori that avian play will necessarily be very similar to mammalian play. Avian play should be studied as an entity in itself before detailed comparisons are made with mammalian play, especially concerning its structure (what animals do when they play), function(s), adaptive significance, development, and evolution. M.B. Bekoff, M. 1976. Animal play: problems and perspectives. Perspectives in Ethology 2: 165-168. Bekoff, M. & Byers, J.A. 1981. A critical reanalysis of the ontogeny and phylogeny of mammalian social and locomotor play: an ethological hornet's nest. In Immelmann, K., Barlow, G., Main, M. & Petrinovich, L. (eds.). Issues in Behavioural Development: the Bielefeld Conference. Cambridge. Ficken, M.S. 1977. Avian play. Auk 94: 573-582. Keller, R. 1975. Das Spielverhalten der Keas (Nestor notabilis Gould) des Zurcher Zoos. Zeitschrift fur Tierpsychologie 38: 393-408. Kilham, L. 1974. Play in hairy, downy, and other woodpeckers. Wilson Bull. 86: 35-42.

PLAYBACK: refers to the broadcasting of recorded songs or calls, usually in the field. Since portable recording equipment became available in the 1950s, this technique has been employed increasingly for research on bird sounds, for censusing, viewing, photographing and capturing birds, and as a control method where birds are regarded as pests. It is suitable for use with any kind of bird which uses any sort of sound for communication. Although birds often respond to poor recordings, playback of good quality and adequate volume is important for most applications. Portable equipment is usually sufficient. Although there is little evidence that playback is harmful, it should be used with restraint. Birds are protected by their tendency to lose interest in repeated sound . signals. Alone or with visual models, playback enables researchers to use experimental methods to investigate the meaning of sound signals by observing responses of listeners. The investigator can vary the location, time of day, stage of the breeding cycle, type of listener to be studied and the individual whose signal is to be broadcast. Various studies have shown that birds can distinguish between sounds of their own and other species and may recognize sounds of mates, parents, offspring and individual territorial neighbours. In certain cases responses between species have been demonstrated. By playing altered or artificial sounds, it is possible to determine which features are sufficient to elicit a particular response. Thus, the acoustic basis of species and individual recognition has been investigated. For most purposes, brief playback experiments are more meaningful than prolonged exposure of birds to an unresponsive sound source.

Playback is especially valuable in the study of territorial behaviour. For example, territory-holders have been removed and recordings played in their territories to investigate the role of song as a 'keep out' signal. Birds that advertise by song usually respond aggressively if recorded

467

songs are played within their territories. By moving the loudspeaker, their defended boundaries can be mapped. Where territories are contiguous, mapping by playback provides an accurate census of the breeding population. However, if members of a species are few and far between, a bird may follow a loudspeaker far beyond the area it normally occupies. Playback is useful for locating rare, inaccessible or nocturnal species. Song or distress calls can be played near traps or mist nets to capture particular individuals. This is useful in studies of breeding birds. Since playback may attract birds which are otherwise difficult to approach,it facilitates close observation, sound recording and photography. It is most effective early in the breeding season (often prior to mating) and when the recording is of the bird's own voice or that of an unfamiliar member of the same population. If the response wanes it may be restored temporarily by changing songs or locations. As a control method, alarm or distress calls have been broadcast to disperse undesirable roosts, reduce bird hazards at airports, and to protect crops. The effectiveness of such measures may diminish with prolonged use. J.B.F. Blackburn, F. 1974. The uses of play-back tape. In Turner Ettlinger, D.M. (ed.). Natural History Photography. New York. Falls, j.a 1978. Bird song and territorial behaviour. In Krames, L., Pliner, P. & Alloway, T. (eds.). Aggression, Dominance and Individual Spacing. New York. Falls, j.B. 1981. Mapping territories with playback: an accurate census method for songbirds. In Ralph, C.j. & Scott, J.M. (eds.). Estimating the numbers of terrestrial birds. Studies in Avian Biology, 6. Falls, j.B, 1982. Individual recognition by sounds in birds. In Kroodsman, D.E. & Miller, E.H. (eds.). Acoustic Communication in Birds, vol. 2. New York. Murton, R.K. 1971. Man and Birds. London.

PLENARY POWERS:

of the

International Commission,

see

NOMENCLATURE.

PLOCEIDAE: a family of the also SPARROW (1)).

PASSERIFORMES,

suborder Oscines;

WEAVER;

PLOCEPASSERINAE: see SPARROW-WEAVER

AND SCALY-WEAVER.

PLOVER (1): substantive name of the majority of species of the Charadriidae (Charadriiformes, suborder Charadrii); in the plural, general term for the family. The other substantive name widely used in the group is 'lapwing', but not all the species that are generically lapwings are in practice so called. A few members of the family have particular names, and one of these, 'dotterel', is sometimes used also as a substantive name of other species of Charadriidae, especially in Australia and New Zealand. Characteristics. Plovers are birds of from small to medium size (15-40 em long), compactly built and thick-necked, with large eyes. They run swiftly and fly strongly. The bill is usually straight, fairly stout, and of only moderate length compared to the size of the head-not showing numerous specialized forms such as are found in the Scolopacidae (see SANDPIPER). The wings are long, the tail is short to medium, the legs are of various lengths, and with or without a vestigial hallux. The plumage differs from that commonly found in the Scolopacidae in that it shows bold colour patterns (in brown, olive, grey, black, and white), but it is nevertheless cryptic owing to the disruptive effect. Common features are a white band on or behind the nape, a dark thoracic band or area, and a dark terminal or subterminal band on the tail. The downy chicks of most species have the white band on the nape, and also a dark cap. A few species show pronounced seasonal change; the sexes are alike or nearly so, and the juvenile plumage is also not strikingly different. Bock (1958) recognized about 50 species of plovers, with a few others doubtfully belonging to the group. They can be broadly divided into the lapwings, recognized by Bock as a single genus Vanellus comprising 24 species; and the true plovers, 5 genera comprising 26 species. This classification amalgamated many genera recognized hitherto, the majority of them monotypic. The earlier classification had been based on characters of doubtful validity-notably the shape of the skull, which is in fact particularly affected by the size of the nasal glands, this in turn depending on adaptation to a fresh-water or saline environment. The classification adopted here recognizes some subdivision of the lapwings at

a generic level. Of additional forms sometimes included in the Charadriidae, Phegornis is retained here on the basis of relationship with the dotterels Eudromias spp. (see Storer in Burton 1974); and the Australian Dotterel Peltohyas

468

Plover

australis, sometimes included with the coursers, is treated as a plover on

the basis of the review by Maclean (1976); but the turnstones (Arenariinae) are firmly placed in the Scolopacidae (see SANDPIPER) (Jehl 1968, Burton 1974); and the MAGELLANIC PLOVER Pluvianellus socialis has been removed from the Charadriidae and placed in a monotypic family Pluvianellidae by J.R. Iehl. The plover family is cosmopolitan in its distribution, but whereas the Scolopacidae are predominantly native to the Northern Hemisphere, the Charadriidae are to a large extent tropical. Lapwings. Although the general appearance of the several species of Vanellus is diverse, the tail is always white basally and usually has a broad black band distally, while the wing always has black primaries and usually a broad white stripe. Characters frequent among the lapwings, but not found in other plovers, are a crest, facial wattles, and wing-spurs; the last correlate with the aggressive nature of the birds, and in species which have no actual spur on the carpal joint a bony knob is present beneath the skin. Africa has the largest number of species. North America has no lapwings, apart from the occasional occurrence of vagrant individuals or flocks of the European Vanellus vanellus; South America has 3 species, probably descended from birds crossing directly from Africa. New Zealand had none, even as regular visitors, until its successful invasion by an Australian form (V. miles novaehollandiae). The English name was originally given to the Lapwing Vanellus vanellus and refers to the rather slow wing-beat. It is a crested species native to middle Palearctic latitudes. The Sociable Plover Chettusia ('Vanellus') gregarius has a circumscribed inland breeding range on both sides of the Ural mountains. The handsome Spur-winged Plover Hoplopterus ('Vanellus') spinosus is found in south-eastern Europe, the Middle East, Egypt and tropical Africa (mostly north of the Equator); in eastern Africa its range is largely allopatric with that of the Blacksmith Plover V. armatus, which replaces it to the south, though the 2 species are patchily sympatric in Kenya where they have both been recorded nesting around the same water hole. Africa seems to have been the centre from which the lapwings have radiated, as judged by present-day distributions and specializations. Separation in eastern Africa by altitude is found between V. lugubris and V. melanopterus and by habitat between V. tectus (in arid thorn scrub) and V. coronatus (on grassland). The former is also a more northerly species, but the ranges are sympatric in Kenya, though with a fair degree of ecological separation. Amongst further habitat specializations may be cited the jacana-like habits of V. crassirostris, which makes a floating nest, and the exploitation of rivers with extensive sandbanks by V. albiceps and other plovers during the dry season. Of the smaller number of species in the Oriental Region, the Redwattled Lapwing V. indicus and the Yellow-wattled Lapwing V. malabaricus are well-known birds in India, where the latter often nests on flat roofed houses. The River Lapwing V. duvaucelii, ranging from India to S. China, is often considered conspecific with the Spur-winged Plover Hoplopterus ('V.') spinosus. Australia holds the Banded Plover V. ('Zonifer') tricolor and 2 subspecies of the Masked Plover V. miles. Golden Plovers. The 4 species of Pluvialis are exceptional in their plumage pattern; the white band on the nape is not present even in the downy chick, and the colour of the back is 'spangled' instead of uniform. These 'spangles', pale feather edgings, often wear off during the winter months. The under parts are largely black in the breeding season in the 3 northern species. They are relatively larger birds than the sand plovers (see below). The Golden Plover P. apricaria (northern and southern races) breeds in northern Europe and the extreme north-west of Asia, reaching the Mediterranean countries and northern India on migration; the southern race is present throughout the year in Britain. The closely related Lesser or American Golden Plover P. dominica (Atlantic and Pacific races) is native to high latitudes in North America and Siberia east of R. Yenesei. Its migrations extend as far as Australia, Argentina and East Africa (e.g. Ethiopia and Somalia). The Grey Plover Pluvialis ('Squatarola') squatarola-called Black-bellied Plover in America-has a Holarctic breeding distribution at very high latitudes; and migrations extending as far as Chile, Cape Province, and Australia. The so-called New Zealand Dotterel P. obscurus has reddish-brown underparts in the breeding season; it is restricted to New Zealand, and one may suppose it to be descended from migrant ancestors of the northern species remaining in the south to breed. Sand plovers. This is sometimes used as a convenient general term for the species here regarded as constituting the genus Charadrius, often

termed 'dotterels' in Australia. They are mostly rather small plovers, but some are of medium size. In general the plumage is brown or grey above and white below except for some expression of a pattern of darker markings that is characteristic of the genus-a dark band across the breast, a black forehead, and a black line from bill to eye. Bock recognized 24 species and divided them into (a) a typical group; (b) sand plovers in the narrow sense; (c) mountain or plains plovers; (d) a number of aberrant forms. The genus is cosmopolitan in its distribution. Of group (a), the familiar Ringed Plover Charadrius hiaticula of Europe also breeds in Greenland and arctic Canada, where it has been known to interbreed with the Semipalmated Plover C. semipalmatus of North America; they are often considered to be conspecific. The Kentish Plover C. alexandrinus of Europe (Snowy Plover of North America) is a small and pale species with only an interrupted breast-band. It is practically cosmopolitan, in different subspecific forms, the most colourful being the Red-capped Dotterel of Australia. The Killdeer C. oociferus, which is larger than those just mentioned, has two breast-bands; it is a bird of inland pastures and breeds from Canada to Peru. Another species with 2 black bands (leaving 3 white areas) is the Three-banded Plover C. tricollaris of Africa South of the Sahara, including Madagascar. The Double-banded Dotterels C. bicinctus, which breed in New Zealand, and some of which then visit Australia, have an upper black band and a lower chestnut one. Typical of group (b) is the Great Sand-plover (or Large Sand Dotterel) C. leschenaultii which has no black on the chest, but a broad band of rufous in the male only; it is a notable migrant, breeding in Central Asia and reaching South Africa and Australia. Amongst group (c), the Mountain Plover C. ('Eupodia') montanus inhabits semi-arid plains in the southern area of the Rocky Mountains, and is notable for its flexible mating system (see later), a supposed adaptation to unpredictable food supplies which vary in quantity from year to year. The Caspian Plover C. asiaticus, which may be conspecific with the larger Oriental Plover C. veredus, breeds in the eastern Palearctic and reaches South Africa and Australia on migration. It seems closely related to the Winter Plover C. modestus of South America. Other genera. In similar habitats to the montane plovers are found the Dotterel Eudromias morinellus, a native chiefly of northern Europe and western Siberia, migrating to the Mediterranean and south-western Asia, and the congeneric E. ruficollis of South America. Also found in South America is Mitchell's Plover Phegornis muchellii, a bird of the edges of mountain torrents, where it feeds on animal prey picked from aquatic plants. The Wrybill Plover Anarhynchus frontalis of New Zealand, breeding in the South Island and migrating to the North Island, is unique among birds in having a laterally deflected bill, the distal quarter being turned to the right; with this it probes for insects under stones on beaches. Habitat. Lapwings are found in a wide variety of habitats during the breeding season, from areas of human habitation (V. malabaricus in India, V. miles novaehollandiae in Australia), through farmland, both arable and grazed pasture (V. vanellus in Europe), sparsely vegetated ground (V. tricolor in Australia), thorn scrub (V. tectus in E. Africa) to sandbanks in major African rivers during the dry season. The 3 species of golden plovers that breed in the northern hemisphere do so in sparsely vegetated mountainous areas or on the arctic tundra. Of the sand plovers, some breed on sandy or pebbly seashores, often nesting only a short distance above the tide-line (C. hiaticula in Europe, C. alexandrinus) , whereas others of the same species may nest inland on shingle beds in rivers or beside lakes, as well as on stony tundra (C. hiaticula in Greenland). C. pallidus breeds around soda-lakes in East and SW Africa. Other species frequent open ground, often far from water, whilst breeding: either lowland fields (C. vociferus) or dry prairies at higher altitudes (C. montanus). Movements. Those species breeding at high latitudes are migratory, some of them performing journeys of up to 10,000 km. Immature birds of the larger species may stay south of the arctic breeding grounds for 1 or 2 years. The migrations of the golden plovers, particularly P. dominica, involve long sea-crossings e.g. from Alaska to Hawaii, and consequently require the storage of large quantities of fat before departure and an accurate navigation system which can be used over the open ocean. In temperate latitudes, many species migrate towards the Equator in autumn but few cross it. Some populations of some species are partial migrants, e.g. the British population of C. hiaticula, and the New Zealand C. bicinctus. In tropical regions, most species move only short

Pluma 469

distances, though this may involve a change of habitat e.g. from riverine sandbanks to nearby ricefields in Nigeria when the large rivers come into flood. European species that feed inland on damp pastures or ploughed land in the non-breeding season, e.g. V. vanellus, move west or south during severe weather in winter or during very dry summer weather, when their foods become unavailable. Food. Plovers forage in a characteristic way, by repeated runs of a few metres at a time, interrupted by pauses spent in an upright or 'headlowered' attitude. A peck at the ground often follows a pause, with a change from the upright to the 'head-lowered' attitude sometimes intervening. Successive runs may involve changes in direction of more than 90°, presumably because birds have detected prey to the side of, or behind, them. Although it has been claimed that plovers hunt by auditory cues (and have been shown to be able to do so in the laboratory), it is unlikely that these are of major importance in field conditions, where sight is used almost exclusively (Pienkowski 1983). Plovers can detect prey when these are active on the surface of the substratum, and they may use foot-trembling to make prey move. They do not search by probing, as do many sandpipers. Their food is mainly animal. On coasts and estuaries, it comprises the larger intertidal polychaetes, small crustacea and small bivalves and gastropods, swallowed whole. Terrestrial plovers take many annelids, dipteran larvae and carabid beetles. Many species feed at night, some probably obtaining a greater proportion of their daily food intake then than by day, as a result of the greater variety and size of invertebrates that become active at the surface of the substratum by night. When feeding, plovers space out much more than sandpipers, and often feed away from the water's edge, even in intertidal areas. In this way, they are able to reduce physical disturbance to the substratum, which might otherwise make prey unavailable. (When disturbed, many prey either become immobile or move to depths beyond the range of a plover's bill.) Some individuals of some species, e.g. P. squatarola, defend feeding territories during the non-breeding season, partly to reduce disturbance to prey, partly to conserve food resources and sometimes to ensure sheltered sites in which to feed during gales (Townshend et al 1984). Behaviour. Many plovers are also territorial during the breeding season, though some species, e.g. V. vanellus in Europe and V. tricolor in Australia, form what have been termed 'loose colonies', in which nests are well spaced, but some co-operation occurs between adjacent pairs in mobbing potential predators. (These loose colonies appear to be determined only in part by suitability of habitat.) Outside the breeding season, plovers tend to be gregarious inland in Europe (e.g. flocks of thousands of P. apricaria and V. vanellus) though never in such large numbers on coastal sites, nor inland in Africa. On the coast, birds that have been feeding while well-dispersed over many sq km of mudflats usually come together to roost, often with sandpipers. Display and voice. Territorial plovers display on the ground at the boundaries of their territories and in the air above them, particularly at the beginning of the breeding season. When in flight, with slow butterfly-like wing-beats, they often 'sing' with melodious long trills. Call-notes, which are usually short whistles or shrill cries, are often reserved for flights to and from roost and feeding areas, and are not always given when birds are disturbed. Other displays connected with nesting include injury-feigning to distract predators from the vicinity of nests (e.g. by shore-nesting plovers such as C. hiaticula), and attacks, by jumping with spread wings, in the faces of large herbivores approaching nesting areas, as shown by African vanellids. V. vanellus in Europe will mob and dive-bomb corvids alighting near their nests. Breeding. Plovers employ a variety of mating systems--monogamy (as in C. hiaticula, although the mate may be changed from one year to the next); polyandry, associated with sex reversal in dotterels, in which the female is brightly coloured and the male incubates; polygyny; and polygamy involving mate-changing by both sexes, as found in C. montanus. Many monogamous species attempt to raise only one brood per year, but this may involve many layings, since predation of the ground nests is heavy. Most breeding habitats are open, either bare or thinly vegetated, and the nests are mere scrapes with little or no lining. Several Charadrius spp. partly cover their eggs with sand when leaving them, a habit most fully developed in the African C. pecuarius which, in a few seconds, completely covers its eggs by stereotyped kicking movements. Tropical plovers may also damp the eggs and substrate with water brought in their belly feathers (see BELLY-SOAKING). Two to 5 eggs are

Golden Plover Pluvialis apricaria. (A.H.).

laid; in many temperate species very consistently 4, in African Charadrius spp. equally consistently 2. They are buff, brown or grey, heavily marked with black, and well camouflaged. In monogamous species, both parents usually incubate and share care of the brood after hatching. First breeding may occur at one-year-old in smaller species, but often not until 2 or 3 in larger species. The chicks are downy and nidifugous, and losses to predators occur chiefly during the first 10 days after hatching, which takes place after 3-4 weeks incubation. Fledging takes from 3 weeks in the smaller to 5 or 6 weeks in the larger species. Annual survival of adults in high, especially of larger species e.g. 80-900/0 for P. squatarola. See photos BELLY-SOAKING; COLORATION, ADAPTIVE; ENERGETICS. P.R.E. Bock, W.]. 1958. A generic review of the plovers (Charadriinae, Aves). Bull. Mus. Compo Zoo., Harvard 118: 27-97. Burton, P.J.K. 1974. Feeding and the Feeding Apparatus in Waders. London. Graul, W.D. 1974. Adaptive aspects of the Mountain Plover social system. Living Bird 12: 69-94. Iehl, J .R., Jr. 1968. Relationships in the Charadrii (shorebirds): a taxonomic study based on color patterns of the downy young. Mem. San Diego Soc. Nat. Hist. 3: 1-54. Maclean, G. 1976. A field study of the Australian Dotterel. Emu 76: 207-215. Pienkowski, M. W. 1981. Differences in habitat requirements and distribution patterns of plovers and sandpipers as investigated by studies of feeding behaviour. Verh. orne Ges. Bayern 23: 105-124. Pienkowski, M.W. 1983. Changes in the foraging pattern of plovers in relation to environmental factors. Anim. Behav. 31: 244-264. Prater, A.J., Marchant, J.H. & Vuorinen, J. 1977. Guide to the Identification and Ageing of Holarctic Waders. Tring. Townshend, D.J., Dugan, P.J. & Pienkowski, M.W. 1984. In Evans, P.R., Goss-Custard, J.D. & Hale, W.G. (eds.). Coastal Waders and Wildfowl in Winter. Cambridge.

PLOVER (2): used as substantive name of certain species not included in the Charadriidae-Egyptian Plover Pluvianus aegyptius (see COURSER); Norfolk Plover (or Stone-curlew) Burhinus oedicnemus and Stone Plover Esacus magnirostris (see THICKKNEE); Upland Plover (or Bartram's Sandpiper) Bartramia longicauda (see SANDPIPER); Crab-plover Dromas ardeola (see CRAB-PLOVER); and, not even in the Charadriiformes, Quail-plover Ortyxelos meiffrenii (see BUTTONQUAIL). PLOVERCREST: Stephanoxis lalandi (for family see HUMMINGBIRD). PLOVER, MAGELLANIC: see MAGELLANIC

PLOVER.

PLOVER, QUAIL-: see BUTTONQUAIL. PLOVER, SAND: see

SAND-PLOVER;

for family see

PLOVER (1).

PL U MA: alternatively 'plumage feather', one in which the barbs are free instead of forming a coherent vane (see FEATHER; PLUMAGE; and compare PENNA).

470 Plumage

PL UMAG E: also called 'ptilosis', the aggregate of which the feather is the unit, and the outstanding character distinguishing the Class Aves from all others (see FEATHER). While the general nature of plumage is constant for all birds, differences in 'its characteristics are found between one species and another, and to a minor extent between populations of a species (whether sharply separable into races or not); and certain broad differences are common to particular taxonomic groups of species. Further, there are differences related to age, sex and season. There is also individual variation, strongly marked in some species; and occasional abnormalities occur (see PLUMAGE, ABNORMAL). The plumage of the individual bird is periodically renewed (see MOULT). Functions. The plumage constitutes a mechanical and thermal protective covering for the body. Parts of it are essential components of the organs of flight-the wings, and to a lesser extent the tail (see FLIGHT). In addition, the plumage helps to streamline the body, reducing friction during movement on the ground, in the air, and-in the aquatic environment of many species--on or below the surface of the water. For all these it combines high efficiency with minimal weight. It exerts its influence on the energy economy of the body (see HEAT REGULATION) partly through the insulation provided by the air trapped among the feathers and partly by its coloration. During incubation the plumage has a special role in that the feathers and associated brood patches of bare skin are important in maintaining the eggs at optimum temperature (see INCUBATION).

Other functions of the plumage are: to make aquatic birds waterproof (but the feathers of cormorants (Phalacrocoracidae) soak water, which has the function of reducing buoyancy), to carry water (see BELLYSOAKING; SANDGROUSE), to facilitate the catching of insects in flight and as tactile organs (bristles), to collect acoustic energy and direct it into the ear (the ear coverts of owls (Strigiformes) and to facilitate the escape from a predator by the sudden shedding of part of it, in analogy with a lizard shedding part of its tail ('fright moult'). The plumage is also the most important element in the external appearance of the bird. As such, the differences which it shows playa great part in determining recognition of other members of the same species. In some, also, the plumage is mainly responsible for a cryptic, mimetic, or aggressive appearance of the bird (see COLORATION, ADAPTIVE). In very many it includes the principal manifestations of the secondary sexual characters and parts of the plumage are often specially adapted for use in DISPLAY. Apart from providing visual stimuli, feathers-sometimes specially modified-playa part in the production of auditory signals (see MECHANICAL SOUNDS). In all these relations to behaviour the plumage is important for the perpetuation of the species. Terminology. A bird which attains maturity has, in succession, a number of plumages. The plumages of a temperate zone bird, which has a breeding plumage differing from that outside the breeding season, the latter being identical at 11/ 2 years old with that at 21/ 2 years old, can be named in one of the following two ways: (Dwight 1900) Natal Juvenile Ist non-nuptial 1st nuptial Adult non-nuptial Adult nuptial

(Humphrey and Parkes 1959) Natal Juvenal 1st basic 1st alternate Definitive basic Definitive alternate

If the plumage is the same during and outside the breeding season it is termed annual or basic. If there are three plumages per cycle the third may be termed supplemental. Plumages may also be defined with respect to the age of the bird, the season of the year or the brightness of the feathers. In most cases, especially in technical studies of plumage succession and moult, the terminology of Humphrey and Parkes probably is to be preferred (see MOULT for further explanation), but it was criticized by E. Stresemann. Humphrey and Parkes also defined the plumage in a new way, namely as a single generation of feathers that is brought about by a moult. The aggregate of feathers of a bird at a given time is then termed the feather coat, which may consist of one or several 'plumages' (= feather generations); e.g. a 4 month old domestic hen has three 'plumages'. There is, however, a very long tradition for using plumage either in a general way to describe the feather coat or the appearance of a given bird at a given time, and this is adhered to here. Natal plumage. The plumage of the chick on hatching is downy. But

in many species, e.g, pigeons (Columbiformes), parrots (Psittaciformes) and passerines, this is sparse, providing virtually no covering, and in some, e.g. kingfishers (Alcedinidae) and woodpeckers (Picidae), it is entirely absent; in others e.g. ducks (Anatidae) and waders (Charadriiformes), it is thick, soft and beautiful-and in these instances often of cryptic coloration. In some species, e.g. cormorants, the nestling is naked at hatching, but later develops down. A few groups of birds, e.g. penguins (Spheniscidae) and owls, produce a second set of down or semiplumes. The two successive sets may be termed protoptile and mesoptile, respectively. In the megapodes (Megapodiidae) the natal plumage consists of contour-like feathers, not down (Becker), and the young are able to fly almost at once. Juvenile plumage. This is the first plumage in which contour feathers are present. Usually the growing juvenile feather bears the preceding natal down on its tip, but soon the down falls off. It was formerly held that the natal down and the juvenile feather comprised only one feather generation, the natal down being merely the downy tip of the juvenile feather. This view has been abandoned. Juvenile feathers are simpler in structure than corresponding adult ones (fewer barbs per unit length, fewer barbules with hooklets, etc. (Gohringer 1951). Where sexual dimorphism occurs, the juvenile plumage of both sexes usually resembles quite closely the plumage of the adult female. There are exceptions to this rule, for in the Koel Eudynamus scolopacea and the Somali Chestnut-wing Starling Onycognathus blythii the juvenile birds of both sexes resemble the male. In some species, e.g. the Gannet Sula bassana, where the adults show no broad differences between the sexes, the juvenile plumage differs totally from that of the adult. In others, the juvenile plumage resembles that of the adults, but is nevertheless distinguishable, e.g. in the Kingfisher Alcedoatthis, where the young have similar colouring but lack the brilliance of the adults. Yet another pattern, in which the young have a distinctive dress, is exemplified by the Great Spotted Woodpecker Dendrocopos major; juvenile birds of both sexes have the top of the head red but, after moulting from the juvenile plumage, they acquire the distinctive sexual dimorphism of the parents, i.e. the black crown in both and the red nuchal band that distinguishes the male. This may be an instance of ontogeny repeating phylogeny, indicating that an ancestral form had at one time the red crown both in adults and in the young, and that the present sexual dimorphism represents a later specialization. Spotting and longitudinal striation is often more marked and cryptic in juvenile than in adult (definitive) plumages. The cryptic effect can be related to die juveniles' lack of environmental experience and consequently greater vulnerability to predators. In a few species, e.g. the Red-backed Shrike Lanius collurio, two similarly coloured juvenile plumages follow each other. Plumage change with age. In many species (passerines in particular) the plumage that follows the juvenile plumage is so similar to that of the adult bird in the same season, that close inspection is necessary to disclose a difference (e.g. in European Robin Erithacus rubecula some rectrices tend to be more pointed and some wing-coverts tend to have larger bright spots in first year birds). In a few instances, e.g. the Shore (or Horned) Lark Eremophila alpestris, there may be no observable distinction at all, so that the definitive basic plumage is assumed direct from the juvenile plumage. In other species, e.g. the male European Blackbird Turdus merula, this second plumage is clearly intermediate between those of the juvenile and adult birds. Often flight and tail feathers belonging to the juvenile feather generation are retained for the succeeding plunrrage. In small birds, in general, the plumage does not change appreciably with age after the bird is about 11/ 2 years old. In male Pied Flycatcher F icedula hypoleuca, however, the brown or black plumage colour continues to intensify up to an age of perhaps 5 years (Winkel et al 1970). Also many larger species e.g. geese Anser, show only minor plumage changes after their first year to year and a half. In some species the plumage succession may extend over a span of years. Examples are provided by albatrosses (Diomedeidae), gannets, large birds of prey and the larger gull Larus species, but also by some passerine birds, such as the males of some species of birds-of-paradise (Paradisaeidae) with their elaborate display plumages. In the Twelvewired Bird-of-Paradise S eleucidis melanoleuca the period may be as long as 7 years (at least in captivity).

Plumage

The attainment of the final plumage roughly coincides with the age at which breeding starts, but the correlation is not always close. In the European Sea Eagle Haliaeetus albicilla breeding starts when the birds are about 4 years old, by which age the dark brown juvenile plumage has changed through gradually lighter plumages into the light grey-brown plumage of the adult; the tail also has changed from brown to predominantly white, but it may be several more years before it becomes pure white. In captivity the Bald Eagle Haliaeetus leucocephalus may take 10 years to reach the definitive plumage. The plumages intervening between the juvenile plumage and the adult or definitive plumage are most precisely termed first, second (etc.) basic/ non-nuptial and alternate/ nuptial. Collectively the less accurate term 'immature plumage' may be used; for the later stages also 'sub-adult plumage'. Seasonal plumage changes. In species with a seasonal change of plumage, the plumage worn outside the breeding season is the nonnuptial or basic, while the plumage worn during the breeding season is the nuptial or alternate. The non-nuptial or basic plumage is usually duller than the nuptial or alternate plumage, and the term 'basic' stems from considering the dullness primitive (Humphrey and Parkes). To give an example, the basic plumage in many waders is characterized by white under parts as opposed to black or red in the alternate plumage. Striking nuptial plumages and accessories are assumed by both sexes in the grebes (Podicipedidae), the divers (Gaviidae) and the herons (Ardeidae}--the plumes of the head, mantle and other regions of the last-named forming most impressive additions to the breeding dress. SEXUAL DIMORPHISM is very common and usually more marked in the alternate i.e. breeding plumage, than in the basic plumage. Where a dull basic/ non-nuptial plumage is worn for only a short period, as in ducks and some sunbirds (Nectariniidae), it is sometimes referred to as eclipse plumage (see MOULT); but it is not certain that this plumage corresponds to the basic/non-nuptial plumage of other birds. Some sunbirds have a bright plumage the whole year. If this corresponds to the annual/basic plumage of other birds, the eclipse plumage of some sunbirds must be regarded as a specialized interpolated plumage serving a protective function (E. Stresemann). In some species, e.g. the Sharp-tailed Sparrow Ammospiza caudacuta, there are two nearly identical plumages per year. This may be related to abrasion caused by the species' habit of foraging in wet vegetation. The length of the period during which each plumage is worn varies with the species; in the Dunlin Calidris alpina the basic plumage is present for 7-8 months (September-April) while in the Mallard Anas platyrhynchos it is worn for only 2-3 months. Other terms for the basic/ non-nuptial/eclipse plumage are off-season, non-breeding and winter plumage, though in northern temperate dabbling ducks the 'winter' plumage is actually worn during the later summer months. The alternate or nuptial plumage is also termed breeding, nesting or summer plumage. Some species have more than two plumages annually. In the adult male Long-tailed Duck Clangula hyemalis four plumages are recognized: transitional autumn, winter, transitional summer and full non-breeding. It is assumed that the first two correspond to the nuptial plumage of other ducks, the latter two to the non-nuptial plumage, but some tracts bear three feather generations in a year. The major moults are not continuous, but interrupted or halted for several weeks, so that annual plumages are produced. In ptarmigans Lagopus as well as in the male Ruff Philomachus pugnax three annual plumages are present. In the Ruff the third plumage is related to display, while in the Long-tailed Duck and ptarmigans the plumage succession probably favours camouflage in changing habitats. Component units. Outwardly, most birds appear to be uniformly covered with contour feathers. In most species, however, the feathers, other than down, grow only from definite tracts (pterylae) of skin (see PTERYLOSIS).

The total number of feathers usually runs into thousands (see but the plumage weight usually equals only 5-7% of the body weight. More than 95% of the plumage volume consists of air. The plumage comprises feathers of several different types (for details of development and structure see FEATHER): 1. Contour feathers. Except for the natal plumage, these constitute the most important element of the ordinarily visible plumage. They include FEATHERS, NUMBER OF),

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the primary and secondary remiges of the wings and the rectrices of the tail, the coverts that-above and below-cover the bases of the remiges and rectrices and also cover the ear orifices, and feathers on other parts of the body (see TAIL; TOPOGRAPHY; WING). 2. DO'Wn. Except in the natal plumage, down rarely contributes to the appearance of the plumage, being hidden from view as a separate layer beneath the contour feathers, where it forms an undercoat in many species. Sometimes down is partly visible, as at the neck in vultures, where the contour feathers have become suppressed as an adaptation to the method of feeding. Some groups of birds entirely lack down in the adult plumage, e.g. ratites, pigeons, and coraciiform birds except kingfishers. In such cases the downy portion of the contour feathers fulfils the corresponding function; but contour feathers with downy portions are present as well as down in many species. 3. Semiplumes. These, like adult down, are hidden from view by the contour feathers. They are often abundant in the abdominal region. 4. Filoplumes. Although these are normally associated with and concealed by the contour feathers they may be visible in some species, e.g. Chaffinch Fringilla coelebs, at the nape. They are seen very strikingly on the nape and back of the Hairy-backed Bulbul Hypsipetes criniger. The white feathers found on the heads, necks and thigh patches of some cormorants are presumably also filoplumes. 5. Bristles. In a few species bristles are found on the toes, but otherwise bristles are confined to the neck and to the head, most frequently at the base of the bill (rictal bristles), the lores, the eye, the malar and the gular regions. Those above the base of the bill and on the lores are sometimes known as 'vibrissae'. Bristles specialized as eyelashes and other bristles in the eye region may serve to keep foreign particles out of the eye. Most groups of birds possess bristles, but some groups, e.g. tubenoses (Procellariiformes) and flamingos (Phoenicopteridae), seem to lack them (Stettenheim 1974). 6. Powder feathers. Where these are densely packed in patches, they may be recognized outwardly in the plumage, e.g. on the Kagu Rhynochetos jubatus and herons (Ardeidae). In other species, e.g, some pigeons and parrots, they are dispersed among the contour feathers and so hidden from view. Powder feathers are widespread among birds, but many groups lack them, including nearly all passerine families. Their function is not well understood; the powder may contribute to making the plumage waterproof or to changing the plumage's colour, so that it becomes more bluish grey. Adaptive differences. Some degree of specialized adaptation can be recognized in practically all the feathering of a bird. Most important of all is the modification of wing feathers to serve the vital function of flight, to which they are most perfectly suited. Minor examples are the beautifully graded and shaped feathers of the facial disc and 'ears' of many owls and the curious rosette of feathers surrounding the uropygial gland (see OIL GLAND).

During the course of evolution, notable differences of plumage quality have become established between different taxonomic groups. Contrast, for example, the scale-like feathers of penguins-a character already discernible in embryonic life-and the soft, abundant feathering of owls, in which flight as near silent as possible is essential to the birds' mode of predation. Take again the water-resistant property of the feathering of the Anatidae and other aquatic birds, which is primarily a structural adaptation: the barbules bear many relatively long outgrowths (E. Rutschke), which, together with the barbules themselves, break up the interface between the surrounding water and the air in the plumage into numerous minute areas. Due to its surface tension, the water is not able to displace the air present in these minute areas and a stable waterair interface is produced. Probably the main function of uropygial gland secretion as a water-repellent is to impregnate the feather substance of the barbules and their outgrowths so that they retain their flexibility and do not break or become disordered. Plumage variation. Individual birds of a given population normally differ from each other slightly with respect to plumage characteristics. Corresponding feathers may vary between individuals in length, shape, pattern of pigmentation and colour, and in at least two Accipiter hawks there is evidence that these features are constant over the years, so that they can be used for the recognition of individual birds (Opdam and Muskens 1976). In addition to this normal, continuous variation there are more striking types of variation. A given plumage of a species may show several colour

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phases (see POLYMORPHISM) or individuals may show abnormalities (see PLUMAGE, ABNORMAL).

A further type of variation appears to have phylogenetic significanceas an atavistic manifestation. The study of the subject received a great stimulus from the classical experiments of Darwin in back-breeding fancy varieties of domestic pigeon to the similitude of the original stock, the Rock Dove Columba Livia. Another example is provided by the occurrence, in the Britsh race of the Robin Erithacus rubecula melophilus, of a variant in which the breast pattern approximates closely to that found in the Japanese Robin Luscinia akahige. A recurring character in the gulls of the genus Larus, namely an oblong white patch in the region of the carpal joint, has been noted in individuals of Heermann's Gull L. heermanni, the Herring Gull L. argentatus and the British race of the Lesser Black-backed Gull L. fuscus graellsii, indicating the extremely close affinity of these three forms. A white neck ring, which is a constant character in the drake Mallard, and which can occur also in the duck of that species, occurs on occasions in the Gadwall A. strepera both in immature and adult drakes, in the Shoveler A. clypeata, in the WigeonA. penelope, in the Yellow-billedTeal A. flavirostris and in the European race of the Teal A. crecca crecca, although in the last two it is at best vestigial and incomplete; it also occurs in some Pintail A. acuta drakes in eclipse plumage. In all the above examples interspecific hybridization is not involved. Where this has been the case, more striking instances have occurred (see also HYBRID). An example is provided by the progeny of a drake European Teal and a duck Shoveler A. clypeata in which appeared the striking facial bridling that is the most characteristic feature of the drake Baikal Teal A. formosa when in adult nuptial plumage. A summary of plumage variants in the Anatidae is given by Harrison and Harrison (1963). Associated behaviour. Some species make use of their own or other down and feathers as nesting material. The habit of plucking their own breast down to use as a nest lining is well developed among ducks. In the bowerbirds (Ptilonorhynchidae) any available bright feathers are among the objects used for decorative purposes in the surroundings of the bower (see BOWERBIRD). There is also the physiological value of ingested feathers. Among birds of prey feathers are taken in the course of ingesting avian prey and facilitate pellet formation (see PELLET). In grebes the feathers are apparently plucked from the bird's own body surface, but subserve the same purpose. Preening, ANTING, DUSTING, SUNNING and flirting with smoke and fire form part of the behaviour of a bird towards its own plumage (see COMFORT BEHAVIOUR). ALLOPREENING is a social response in some species, while mutual preening by a pair occurs in the normal relations between the sexes. An apparent perversion is the feather picking indulged in by domestic fowls and by game-birds (Galliformes) in captivity. (J.M.H.) J.D. Dwight, J. Sr. 1900. The sequence of plumages and moults of the passerine birds of New York. Ann. N.Y. Acad. Sci. XIII: 73-360. Gohringer, R. 1951. Vergleichende Untersuchungen tiber das Iuvenil- und Adultkleid bei der Amsel (Turdus merula L.) und beim Star iStumus vulgarisL.). Revue suisse zool. 58: 279-358. Harrison, J.M. & J.G. 1963. A Gadwall with a white neck ring and a review of plumage variants in wild-fowl, Bull. Brit. Orn. Cl. 83: 100-108. Humphrey, P.S. & Parkes, K.C. 1959. An approach to the study of molts and plumages. Auk 76: 1-31. Lucas, A.M. & Stertenheirn, P. 1972. Avian anatomy. Integument. Agriculture Handbook 362. Washington, D.C. Opdam, P. & Mtiskens, G. 1976. Use of shed feathers in populations studies of Accipiter hawks (Aves, Accipitriformes, Accipitridae). Beaufortia 24: 55-62. Stettenheim, P. 1974. The bristles of birds. Living Bird 12: 201-234. Winkel, W., Richter, D. & Berndt, R. 1970. Uber Beziehungen zwischen Farbryp und Lebensalter mannlicher Trauerschnspper (Ficedula hypoleuca). Vogelwelt 91: 161-170.

PLUMAGE, ABNORMAL: plumage abnormalities may be due to changes in the amount and distribution of the pigments normally present, chemical changes in the pigments producing abnormal colours, changes in feather patterning, or changes in the structure of feathers. Such abnormalities are in many cases extremes of tendencies apparent in the individual variation of a species. They are, of course, to be distinguished from normal differences in colour and pattern resulting from geographical variation or POLYMORPHISM.

Abnormal pigmentation. This is the most frequently occurring type of plumage abnormality, at times affecting most of the commoner pigments, the melanins--black or grey Eumelanin, brown or buff Phaeomelanin and chestnut-red Erythromelanin-and the red and yellow lipochrome pigments. Atypical pigmentation. The more extreme variations of this type are sometimes grouped under the term 'heterochroism'. Occasional individuals of a wide range of species, from penguins to passerines, show a marked reduction or loss, or a considerable increase, in the pigments normally present. Although often referred to as chance mutations, in the form in which they occur they are remarkably consistent, genetically controlled and usually recessive, and can predictably be produced by subsequent controlled breeding. Under natural conditions individuals showing such variations are usually at a disadvantage and short-lived, mainly because their greater conspicuousness makes them more liable to predation. In addition, reduced pigmentation weakens the feather structure, causing accelerated abrasion and wear, particularly of flight feathers, and this may affect mobility. Loss of pigmentation also affects the retina of the eye and can lead to impaired sight in bright light. There is evidence in some species of a failure to recognize abnormally-coloured individuals as potential partners in pair-formation. In captive Greenfinches Carduelis chloris, nestlings with variant plumage are at a disadvantage compared with normal youngsters in the same brood and often fail to survive until fledging. Of variations resulting from an increase in the pigment present, the best-known is probably 'melanism' in which the amount of black and/or brown melanin present increases, and may spread to parts of the plumage which normally lack melanin, masking other colours where these are present. The bird usually appears entirely black or dark brown or a mixture of both. Apparent melanism is sometimes due to a staining of feathers by industrial wastes, soot or oil. The term 'erythrism' is sometimes used for cases in which chestnut-red replaces other melanins. 'Flavism', an excess of yellow pigment spreading into parts of the plumage where it does not normally occur, is rare in the wild, but is apparent in some domesticated strains of the Canary Serinuscanaria and Budgerigar Melopsiuacus undulatus. Partial loss of pigment, affecting all the colours present and reducing them in intensity, is rare. It is called 'dilution' by bird breeders and 'leucism' in scientific writings, although the latter term is also used at times for various forms of schizochroic loss (see below) of single pigments which make the plumage appear paler. The complete loss of feather pigment is more common. This may occur as true 'albinism' in which pigment is absent throughout the body, a condition resulting in red eyes and pale pink legs and bill. In other cases, genetically different from true albinism, pigment is absent from the plumage but the normal body colours are retained. In species in which some or all of the plumage is normally white, the normal condition can often be distinguished from these white variants by the presence of small amounts of greyish pigmentation in the downy bases of the white feathers. Partial whiteness, usually in the form of one or more asymmetrical patches of plumage, is more frequent than total whiteness. It is controlled by recessive genes which appear to carry the capacity for partial loss of plumage pigmentation, but not to control its location on the body, resulting in individual differences also apparent if the variation is passed on to offspring. However, within any group of related species, partial whiteness is likely to occur more consistently on some areas of plumage than on others. The amount of white may increase in area on an individual with successive moults, but it appears not to have been established whether this is an aspect of ageing due to a hereditary factor or the result of some increasing physiological disorder. Schizochroism. The other major source of colour abnormality is a phenomenon sometimes called 'schizochroism'. In this a pigment normally present in the plumage is absent, or several pigments may be missing. This changes coloration or affects patterns by leaving white areas on feathers where the missing pigments would normally be present, unless another pigment also occurs on this part of the feather and now appears alone. The predominant colour of many bird plumages is a dull brown formed by a mixture of both brown and black melanin. In the noneumelanic form of schizochroic plumage abnormality only the black colour is lacking, and the bird appears a pale buffish-brown, with white markings where black alone was present. If other pigments are normally present they will be unaffected. In captive birds this condition is usually

Plumage, abnormal

described as 'buff', 'fawn' or 'cinnamon'. It is controlled by a sex-linked gene and is usually found only in females in the wild. The non-phaeomelanic variation is less frequently seen. It usually appears mainly ash-grey, and is sometimes referred to as a 'silver' variety. It is under different genetic control from the last, being apparently autosomal, and birds showing it are as likely to be male as female. In both types of loss the feathers, with reduced quantities of melanin, are subject to more rapid abrasion than are normal feathers, and also bleach rapidly. By the time that they are due to be moulted, the normally-exposed portions of feathers may have lost their melanin, and the bird may appear white unless closely examined. The chestnut-red melanin, when present, seems little affected in such variant plumages. The loss of both black and brown with retention of chestnut-red is known in the Zebra Finch Poephila guuata, and has been recorded once in the Waxwing Bombycilla garrulus. Loss of chestnut-red with retention of other melanins seems unknown in wild birds but occurs in the 'penguin' strain of the domesticated Zebra Finch. Schizochroic variants in which all melanins are lacking from the plumage appear albino or white-feathered except where red and yellow pigments are also present, the latter persisting as coloured areas on otherwise white plumage. Such variations are known in the finches (Fringillidae), waxbills (Estrildidae), and weavers (Ploceidae); while loss of black in normally green parrots such as the Budgerigar and the Ring-necked Parakeet Psittacula krameri produces yellow individuals in which normally dark markings are white. In some cases loss of melanin revealsa more extensive distribution of red or yellow, which is normally masked by other pigments. The converse of the last variation produces individuals having the normal melanin pigments, with white areas where red or yellow would occur, and modification of areas of mixed pigmentation. In parrots this produces blue forms, lacking the yellow pigment which would make them appear green, and with the black melanin modified to blue by Tyndall scattering (see COLOUR). Other examples lacking red and yellow pigments are known in the finches and in the Yellow Wagtail Motacilla flava. Once the general pigment distribution in the plumage of any species is known, it is usually possible to predict what potential plumage abnormalities there might be, and their likely appearance; but unexpected abnormalities sometimes occur. The distinctive patterns which are characteristic of the display plumages of males of many species appear to be to some extent under independent genetic control and not necessarily responsive to changes in the pigmentation of the remainder of the plumage. This is particularly true of the patterns on head and breast; thus in what would otherwise be recognized as non-eumelanic variants of the House Sparrow Passer domesticus and Painted Quail Coturnix chinensis, these parts of the plumage retain much of the black patterning. Pigment replacement. Rarely, one colour is replaced by another. An abnormal change to chestnut-red melanin occurs in individuals of some wader species (Charadriiformes), particularly in the Woodcock S colopax rusticola and Common Snipe Gallinago gallinago. It is also found in gamebirds (Phasianidae), as in the rufous or 'montana' variant of the Grey Partridge Perdix perdix. The abnormal replacement of red by orange has occurred in individuals of the Red-eared Waxbill Estrilda troglodytes and Senegal Firefinch Lagonosticta senegala, in the latter proving to be a recessive inherited character. Gynandromorphs. A striking abnormal variation in pigment distribution results from a possible chromosomal accident which produces an individual that is visually half-male and half-female, possessing both an ovary and testis. In sexually dimorphic species the two sides show the different plumage colours and patterns of the two sexes (and differences in other characters such as wattles, if present), joining abruptly along the mid-line. This phenomenon has been recorded in a number of passerine species, and in the Pheasant Phasianus colchicus, Flicker Colaptes auratus and Budgerigar. In species with marked sexual size dimorphism, this abnormality may produce an individual with dissimilar legs and wings and with distortion of the bill and other medial features. Pigment deficiency. Plumage abnormalities sometimes very similar to those of genetic origin, already mentioned, may be the results of deficiencies or excesses in diet. They occasionallyoccur in wild birds but are more often seen in captive individuals. Some may be distinguished from genetic variants in that they are temporary and may be partially or wholly corrected in later life. Others are permanent and may be the outward evidence of pathological disorders. The former are sometimes

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evident in hand-reared birds which show a lack or excess of normal pigment in the plumage, corrected when the individual has greater opportunity to select its own food and moults into adult plumage. Inadequacy of diet is likely to be cumulative in its effects, and during feather growth is sometimes apparent as a gradual reduction in pigmentation, producing feathers that are increasingly whitish towards the bases. The white bases to remiges occurring on some individual wild Carrion Crows Corvus corone and Rooks C. frugilegus have been ascribed to diet deficiencies but may be of genetic origin. An initially deficient but gradually rectified diet may produce pale-tipped feathers. Brief or intermittent periods of starvation may produce one or more narrow transverse bands across feathers, indicating the extent of growth during the period of deficiency. Such inadequacies of diet will not affectfeathers once they are fully grown. On a nestling where all feathers are growing simultaneously, pale transverse bands may occur in similar positions on most feathers, creating a plumage pattern similar to some of genetic origin. Such barred patterns have been described for young crows Corvus spp. White transverse bands of this type have been experimentally induced by hormone injections during moult. Abnormal white feathers may appear when injury to individual feather follicles or to areas of skin results in follicles continuing to produce feathers but unable to produce melanin. An abnormality of unknown origin in the African Grey Parrot Psiuacus erithacus results in the replacement of normal grey body feathers by red ones lacking melanin and similar to those normally present in the tail. Unsatisfactory diet in captive birds may produce melanism which is in some instances irreversible. In captive finches this has been attributed to an excess of oily seeds, particularly hemp seed. It may result in wholly black plumage but in the early stages the melanin is sometimes irregularly distributed, affecting only some feathers and producing an asymmetrical spotted appearance. Excess of red-pigmented material in the diet may affect the appearance of the plumage. Prior to the production of Red Factor canaries in which red and orange colour is genetic in origin, powdered red peppers were fed to give an orange tint to yellow canaries. Orange-tinted plumage in wild birds has been recorded for a Yellow Wagtail feeding around a red palm-oil effluent, and in Greenfinches feeding on yew berries. Diet deficiency, particularly a lack of carotene, may result in a reversible reduction or loss of red and yellow pigments in feathers. Birds showing a complete loss of these colours may resemble some schizochroic variant forms. This most frequently occurs as an abnormality of captive birds. Blue-grey and white plumage may replace green and yellow, and a bronzy tint occur instead of red. The red colour of captive flamingos (Phoenicopteridae) is largely lost if the diet lacks a substitute for the crustaceans from which this is normally derived. A similar effect may occur in some species due to loss of fugitive pigment from plumage after a period of exposure to light, without any deficiency of diet. A pink tint on freshly-moulted white plumage of some gulls (Laridae) and ducks (Anatidae) is soon lost; and in some tropical bee-eaters (Meropidae) and kingfishers (Alcedinidae) the green feathers of the plumage fade to a light blue through loss of yellow pigment by the time that they are moulted. In the Hunting Cissa Cissa chinensis the normally bright green plumage rapidly becomes light blue in captive birds and also in stored museum skins. Pattern variations. The patterns created by variations in melanin distribution on feathers are a distinctive plumage character of many species, and within populations marked variation in visible pattern is unusual. From a study of the pigment patterns on feathers it seems probable that the patterns apparent on the plumages of many species have undergone a series of progressive changes in the past to evolve that which is now present, and that a uniform colouring may mask earlier patterns. The occurrence on feathers of markings differing from simple transverse bars, such as those induced by experimental hormone injection in some game birds and domestic fowl, may therefore be due to the revelation, when complete pigmentation is inhibited, of earlier evolved patterns. Similarly, earlier patterns on areas of plumage may have been lost, but the genetic potential for their production may remain. This would appear to be the underlying cause for the appearance on some hybrid birds of patterns not apparent in either parent but present on closely-related species. The bimaculate face patterns of some Anas duck hybrids may be an example of this. Variant individuals showing elements of pattern or colour characteristic of other subspecies or related species occur sporadi..

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cally in a wide range of taxa, and these variations may be of similar origin. In some instances a recurrent variation is not a character of any extant species, as in the case of the white carpal patch which has been noted on individuals of several different species of gulls. In normal plumage the appearance is controlled not only by direct genetic factors but also by the relative levels of hormones which determine the occurrence of sexually dimorphic plumages and the seasonal breeding and non-breeding plumages. Any imbalance of the endocrine system is likely to have a noticeable effect on plumage, and in some instances this has been studied in experimentally created conditions, as well as in individuals showing changes which are of pathological origin. In some gamebirds such as the Pheasant and the domestic fowl a reduction in the level of the female hormone may result in females assuming male plumage. This may also occur through the atrophy of ovaries from age or disease. It may not necessarily imply a loss of all female functions since exceptionally individuals have laid eggs when in male plumage. This can occur in other species and there is a record of a male-plumaged Common Redstart Phoenicurus phoenicurus laying eggs in the wild. Female birds have only a single ovary on the left side of the abdominal cavity and if this is removed a mixed gland (ovotestis) develops in a similar site on the right hand side. In game birds the plumage assumed by the castrated female is of a male type and becomes increasingly male with successive moults. Conversely, in castrated Pheasants the male assumes a plumage resembling that of the female. In some breeds of domestic fowl most of the males are hen-feathered. Paradoxically, if such birds are castrated, a more typical male plumage is produced. The hen-feathered condition is controlled by the testes but appears to be hypersensitive to such female hormones as are normally present in the sexually active male. In the House Sparrow, the male of which retains the sexually dimorphic plumage throughout the year although it is partially concealed by dull feather edges in winter, the sexual plumage is under genetic control, but a character affected by hormone levels and lost through castration is the black bill colour of the male breeding dress. Feather structure abnormalities. Abnormalities of feather structure occur infrequently and in wild birds are usually lethal. Like pigment abnormalities, they may be the result of disease or temporary food deficiencies, or may be genetically determined and can be maintained by controlled breeding in captive birds. The more rapid abrasion and loss of portions of plumage deficient in melanin has been mentioned above. Structural abnormalities may have a similar effect. An abnormal weakness of structure resulting in rapid wear of the distal part of the feather vane with retention of a tapering rachial zone, to give a 'needle-tailed' effect to the rectrices, has occurred on both rectrices and remiges of individuals of the Guillemot Uria aalgeand Black Guillemot Cepphus grylle. A complete breakdown of the structure of these feathers, resulting in flightlessness, has been recorded for the Eurasian Jay Garrulus glandarius and Shelduck Tadoma tadoma. Abnormally loose and fluffy plumage may be produced by failure of the interlocking barbule structure, or absence of the necessary barbicels. If the abnormality affects the remiges and rectrice s, such a variation is usually lethal in the wild. In captivity hereditary strains of a similar type have been selected to produce the 'silky' form of the domestic fowl, domestic pigeon Columba Livia and Barbary Dove Streptopelia roseogrisea. A similar breakdown of feather structure associated with reduced pigmentation, possibly resulting from disease and producing plumage with a 'hairy' appearance, has been noted in the Eurasian Jay and the Moorhen Gallinula chloropus. A structural defect resulting in a twisting of the rachis of contour feathers to produce a frizzled effect occurs at times in captive finches, and hereditary strains have been established. Hereditary strains with a complete absence of all feathers have been produced in the domestic fowl and domestic pigeon but have failed to survive for long. Although most of these structural abnormalities are rare, one type of defect is of more frequent occurrence. If a bird undergoes one or more days of inadequate diet when feathers are growing, the deficiency may result in a narrow transverse zone or line of weakness across the vane of the feather. (As already mentioned, pigmentation may also be affected.) This transverse line of defective structure is usually referred to as a 'hunger trace' or 'hunger fault'. Feathers with such faults are liable to break off after a time along the line of weakness, and if this occurs on a number of flight feathers it may make flight difficult or impossible. It was

particularly a matter of concern to man in the early practice of falconry.

C·l·O.H.

Harrison, C.j.O. 1963. Grey and Fawn variant plumages. Bird Study 10: 219-233. Harrison, C.}.O. 1963. Non-melanic, carotenistic and allied variant plumages in birds. Bull. Br, Orn. Club 83: 90-96. Harrison, C.}.O. 1963. Mottled plumage in the genus Corvus, its causation and relationship to fundamental barring. Bull. Br, Orn, Club 83: 41-50. Harrison, C.}.0. 1963. The post-ocular green stripe as a plumage character of the Anatidae. Bull. Br. Om. Club 83: 15-20. Harrison, C.}.0. 1965. The chestnut-red melanin in schizochroic plumage. Ibis 107: 106-108. Harrison, C.j.O. & Washington, D. 1969. Abnormal reddish plumage due to 'colour feeding' in wild greenfinches. Bird Study 16: 111-114. Sage, B.L. 1962. Albinism and melanism in birds. Br. Birds 55: 201-225.

PLUMAGE MIMICRY: see MIMICRY. PLUMAGE VARIATION: see

PLUMAGE.

PLUMBEOUS: lead coloured. PL U ME: a feather, usually long and showy, developed for the purposes of display. PLUMELETEER: substantive name of Chalybura spp. (for family see HUMMINGBIRD).

PLUMULA: a down feather (see PLUMAGE). Natal or nestling down plumage, when present, is called 'neossoptile'. PLUNGING: see

SWIMMING AND DIVING.

PLUSHCROWN: substantive name of Metopothrix aurantiacus, a South American furnariid (for family see

OVENBIRD (1)).

PLUVIANELLIDAE: see under CHARADRIIFORMES;

PLOVER, MAGEL-

LANIC.

PNEUMATIZATION OF BONE: a term denoting the air-holding

properties of the skeleton or parts of the skeleton. Aerated bones are characteristic of the class Aves, but also occur in the skull of crocodiles and, according to Bellairs and Jenkin (1960), were very probably features of the fossil pterodactyls. Since very light and hollow bones are also found in dinosaurs, it is not inconceivable that the origin of pneumatization is to be sought in the early archosaurs, from which all these groups stem (see EARLY EVOLUTION OF BIRDS). Pneumatized bones are hollow, the hollow parts communicating with the air-sac system. Air is supplied to the cranial bones via the air-sacs of the nasal and tympanic cavities, and to the postcranial skeleton via the air-sacs of the respiratory apparatus proper (see RESPIRATORY SYSTEM). Skull pneumatization. The extent of pneumatization can easily be examined in the skull-roof. Unpneumatized parts (so-called windows) appear featureless and more or less translucent. They consist of a single layer of bone. Pneumatized parts of the skull-roof appear speckled in passerines and have a labyrinthine conformation in non-passerines. They consist of bilaminate bone, the two layers sandwiching the spongiosa, bony tissue rendered cancellous by action of bone-excavating cells. The extent of pneumatization can vary markedly both between and within different orders, families and species. No universally applicable rule can be formulated about this. Skulls which are for the most part weakly or not at all pneumatized are seen in e.g. kiwis (Apterygiformes), divers (Gaviiformes), herons (Ardeidae) and auks (Alcidae). Quite varied development of pneumatization occurs e.g. among wildfowl (Anseriformes), raptors (Accipitriformes, Falconiformes), gulls (Laridae) and woodpeckers (Picidae). Predominantly strongly or even fully pneumatized skulls are possessed by e.g, ostriches, rheas and cassowaries (Struthioniformes), pigeons and doves (Columbiformes), parrots (Psittaciformes) and nightjars (Caprimulgidae). The only two orders in which all members pneumatize completely are the owls (Strigiformes) andapart from a very few exceptions--the passerines (Passeriformes). Numerous examples of the amount of pneumatization of the skull-roof in various groups of birds are given in papers by Harrison (1957), Verheyen (1953) and Winkler (1979). In young birds the available studies show a different process of

Poetry, birds in

development of pneumatization in non-passerines and passerines. This phenomenon is closely correlated with differences in brain-development: in non-passerines the brain grows evenly to its adult volume and in most species the pneumatization-process terminates with attainment of the ultimate body-size. In the few non-passerines in which pneumatization continues beyond this point, additional bone is laid down on the outer surface of the skull, as Stork (1972) has established for pigeons. Pneumatization on the inner surface would cause pressure on the brain. But in young passerines the brain goes through an overweight phase, after which it shrinks to the adult volume. For this reason the skull in this group remains unpneumatized until maximum brain-volume is attained. The pneumatization process only sets in when the brain begins to contract to its adult volume. This point approximately coincides with the fledging of the passerine nestling. In contrast to non-passerines, pneumatization takes place against the internal skull-surface. Its function here is to fill out the gap between the unpneumatized skull-roof and upper brain-surface left by the shrinkage-process of the brain. Pneumatization of skull-roof and ageing. In passerines the state of pneumatization of the skull-roof has long been used in establishing age. Since Baird (1963) first demonstrated how the state of pneumatization can be examined through the skin even in live birds, this method of ageing has become important in bird ringing. As nearly all passerines are fully pneumatized when adult (exceptions are noted in Winkler), all incompletely pneumatized birds can be recorded as immatures. However fully pneumatized individuals may only be definitely termed adult during the part of the year in which no juveniles with completed pneumatization can be expected. The dates from which fully pneumatized juveniles can occur have been given by Wood (1969) for certain North American passerines and by Winkler for European species. Depending on species the pneumatization process takes 2 to 8 months, beginning in the occipital region and finishing over the forehead. Among European species pneumatization takes least time in the Willow Warbler Phylloscopus trochilus (2 months) and longest in the Yellowhammer Emberiza citrinella (over 8 months). Occasionally the latter fails to achieve complete pneumatization. In general the stage of pneumatization in non-passerines cannot be employed as an ageing criterion. Pneumatization of postcranial skeleton. This has been far less well studied than that of the skull-roof and again is far more extensively developed in some species than in others. Diving birds like penguins (Spheniscidae), divers Gavia spp. and cormorants Phalacrocorax spp. are more poorly pneumatized than large flying birds like albatrosses (Diomedeidae) and eagles Aquila spp. A number of examples are contained in Bellairs and Jenkin and in Stresemann (1934). Generally the skeleton of large species in a related group appears to be more highly pneumatized than that of smaller species. As demonstrated both by Bellairs and Jenkin, and Stresemann, pneumatization of the postcranial skeleton begins with the penetration of developing bone by fine air-sac diverticula. The air-sac diverticula follow the resorption of the bone marrow and expand through the interior of the bone until they occupy its entire cavity. Function of pneumatization. It is obvious that pneumatization primarily serves to save weight and so enhance flying ability. In addition, a pneumatized bone proves to be structurally more stress-resistant than an unpneumatized one. However, the great differences in extent of pneumatization between different orders of birds remain unexplained. Adaptations to specialized modes of life certainly play an important role here. Thus Harrison comments on the fact that almost all deep-diving birds are but very poorly pneumatized. They thereby minimize the natural tendency to buoyancy during diving. Stork ascribes a function of brain-insulation to the pneumatization of the skull. Winkler considers the significance of skull-pneumatization to lie in, among other things, its balancing out the two functions of the skull-roof, namely on the one hand to enclose securely the brain and on the other to provide insertions for musculature and sockets for the large eyes. Since pneumatization has above all a functional character, its extent cannot be employed as a taxonomic criterion. R.W. Baird, J. 1963. On ageing birds by skull ossification. The Ring 37: 253-255. Bellairs, A. d'A. & Jenkin, C.R. 1960. The skeleton of birds. In Marshall, A.J. (ed.), Biology and Comparative Physiology of Birds, vol. I. New York. Harrison, J.G. 1957. A review of skull pneumatization in birds. Bull. Br. Orne Cl. 77: 70-77. Stork, H.-J. 1972. Zur Entwicklung pneumatischer Raume im Neurocranium der

475

Vogel. Z. Morph. Tiere 73: 81-94. Stresemann, E. 1934. Pneumatizitat des Rumpf- und Extremitatenskeletts. In Kukenthal, W. (ed.). Handbuch der Zoologie. Aves. Berlin und Leipzig. (See pp.79-80). Verheyen, R. 1953. Contribution a l'etude de la structure pneumatique du crane chez les oiseaux. Bull. Inst. R. Sci. Nat. Belgique 29: 1-24. Winkler, R. 1979. Zur Pneumatisation des Schadeldachs der Vogel. Orne Beob. 76: 49-118. Wood, M. 1969. A bird-bander's guide to determination of age and sex of selected species. Pennsylvania State University.

POCHARD: substantive name of some Aythya spp. and of Netta spp.; used without qualification in Britain for A. ferina; in the plural, general term for the tribe Aythyini (see

PODARGIDAE: see under

DUCK).

CAPRIMULGIFORMES; FROGMOUTH.

PODICIPEDIFORMES: an order, comprising only the cosmopolitan family Podicipedidae (see GREBE). The ordinal name, which on the basis of a different view of the etymology of the type genus Podiceps was for a short time called Podicipitiformes, is derived from the family name Podicipedidae, which in its turn was validated in Opinion 981 of the Bulletin of the International Commission on Zoological Nomenclature 29 (1) 1972: 152. Before 1956 the name of the order used by the American Ornithologists' Union was Colymbiformes, for which see COLYMBIDAE.

PODICIPITIFORMES: obsolete term, see

PODICIPEDIFORMES.

PODOTHECA: the horny covering of the unfeathered parts of the legs

and feet (see

LEG).

POETRY, BIRDS IN: for birds, as for man, the dominant senses are

those of sight and hearing; the world of their experience seems, therefore, more comprehensible than one perceived mainly through scent or touch. Their form is often elegant and their colours attractive; the songs of some have long pleased man; their power of flight is enviable. Some build their nests not only in gardens and orchards but even in man's farm buildings and houses, so that these are familiar to man as no other wild animals are. Their domestic behaviour-the nests they build, the care they give to their young-are, again, not remote from human experience. And yet they are rendered mysterious and a cause of curiosity by their migrations. All in all, birds are a natural source of myth and of poetry; but the amount of actual observation of their lives which is available to a poet is necessarily limited. Perhaps the earliest folk-song of Europe to survive was that sung by Rhodian boys to welcome the Swallow, but 7 or 8 centuries earlier a Minoan artist on Santorini had painted a Spring fresco of Swallows, with a pair rising beak to beak against a background of rocks and lilies. Hesiod, Simonides, Aristophanes and other Greek poets associated the return of the Swallow with spring, for even three and a half millennia ago it nested about man's buildings and so made itself more noticeable than other summer migrants. ('Swallow' for the poets often included the House Martin and the Red-rumped Swallow, both of which nest on buildings. The poets are always 'lumpers' not 'splitters'.') But the Swallow's twitter, which has pleased many an English poet-Sir John Davies even preferred it to the Nightingale-seemed to the Greeks no more than a barbarous gabble. The Cuckoo's call-for Shakespeare, with his love of puns, a 'word of fear unpleasing to a married ear'-was a sign of spring to Hesiod, and Aristophanes recognized in it a warning to be off to work in the fields. The spring arrival of these birds was noted, but they were not, like storks and cranes, observable while on migration. Homer compared the clamour of the Trojan host to the noise of migrating cranes, and Hesiod and Aristophanes took the sound in autumn to be a sign that it was time to plough and to sow; Euripides seems to have been more impressed by the spectacle of the long-necked birds in flight 'passing beneath the Pleiads and Orion in the night', probably the first mention of moon-watching. And the winter quarters of cranes were not, like those of Swallows, beyond the limits of the known world.

The song of the Nightingale has evoked the charmed response of poets from Homer to our own time, and from Persia to Britain. Some of them-Aristophanes, Nashe, Lyly, Barnfield-have even attempted to transcribe its song into human syllables. Dafydd ap Gwilym addressed a

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Poetry, birds in

poem to the Nightingale in the Birch Grove (was this in Wales?) and Milton saluted the bird 'that on yon bloomy spray Warblest at eve when all the woods are still',

in the earliest of his sonnets, and often referred to it elsewhere. His friend Marvell, whose poetry gives precise descriptions of birds, observed that 'Low Shrubs she sits in, and adorns With Musick high the squatted Thorns.'

And Izaak Walton, their elder contemporary, shows that he had chosen to listen to the song: 'He that at midnight, when the very labourer sleeps securely, should hear, as I have very often, the clear airs, the sweet descants, the natural rising and falling, the doubling and redoubling of her voice, might well be lifted above earth, and say, "Lord, what music hast thou provided for the Saints in Heaven, when thou affordest bad men such music on Earth!" Collins noted Sophocles's 'peculiar fondness for the song' which he heard at Colonus, and Peacock also referred to this. Keats, hearing the song at Hampstead, was prompted to write perhaps the best known of all poems in its praise, and Robert Bridges wrote a sensitive lyric on the song. Throughout the bird's range the poets have celebrated its song: in English and Welsh, in German and Italian, in Greek and Persian; no other bird has been so universally admired. Much of the poetry about the Nightingale derives from the primitive and savage myth of Tereus, Procne and Philomela (the Hoopoe, Nightingale and Swallow), on which Sophocles wrote a tragedy, of which only a fragment remains. Ovid retells the myth in Metamorphoses VI (the source of later versions) but with Philomela now the Nightingale not, as in Greek sources, the Swallow. For the poets the Nightingale was feminine, and she sang her sad song 'leaning her breast against a thorn.' But these things are the effects of myth, not of observation. Another myth, of Aedon who murdered her child Itylus in error and prayed to be changed into a Nightingale, was known to Homer: in the Odyssey Philomel 'in bow'ry shades unseen To vernal airs attunes her varied strains, And Itylus sounds warbling o'er the plains.'

Swinburne's poem is the best known version of this story in English. Probably more English poets knew the myths than had ever listened to the song, and one cannot help questioning whether the bird whose song Cowper heard on New Year's Day, 1792, was, as he supposed, a Nightingale. No other song-bird has attracted so much myth as the Nightingale, and poetry about Song Thrush, Blackbird and Skylark owes rather more to personal observation. Robert Browning, in Home Thoughts from Abroad, recalled the song of the Chaffinch and of 'the wise thrush; he sings each song twice over Lest you should think he never could recapture The first fine careless rapture.'

The same characteristic repetition was noted by Tennyson and, 250 years earlier, by William Browne of Tavistock. John Clare, a most observant countryman who mentions many birds, heard 'a merry thrush Sing songs of rapture,'

and he watched her skilful modelling of her nest, where Marvell noted with pleasure how he might 'through the Hazles thick espy The hatching Throstles shining Eye.'

Spenser, in The Faerie Queene, singles out the refreshing quality of the song when Calepine, released from captivity, and now regaining strength, 'Upon a day he cast abrode to wend, To take the ayre, and heare the thrushes song.'

And the song made a similar appeal to Hardy, when 'every spirit upon earth seemed fervourless as I', 'At once a voice arose among The bleak twigs overhead In a full-hearted evensong Of joy illimited; An aged thrush, frail, gaunt, and small, In blast-beruffled plume, Had chosen thus to fling his soul Upon the growing gloom.'

Michael Drayton, who has some claim to be the best ornithologist among English poets, said 'Of all birds, only the blackbird whistleth',

and with 'the blackbird whistles from the thorny brake' Thomson recognized the same quality. Theocritus, 2,000 years before, had remarked the clarity of its notes, and poets in the Greek Anthology leave no doubt of their preference for its song to that of the thrush-in Greece, no doubt, the Mistle Thrush. The 'early, cheerful, mounting lark' both by its conspicuous songflight and by the quality of its song makes a strong contrast with the Nightingale singing its plaintive song at night in 'verdurous glooms and winding mossy ways', and it has delighted many English poets. Wordsworth drew the contrast in a poem addressed To a Skylark: 'Leave to the nightingale her shady wood; A privacy of glorious light is thine; Whence thou dost pour upon the world a flood Of harmony, with instinct more divine; Type of the wise who soar, but never roam; True to the kindred points of Heaven and Home!'

When Romeo must leave Juliet she says: 'It was the nightingale, and not the lark, That pierced the fearful hollow of thine ear; Nightly she sings on yond pomegranate-tree: Believe me, love, it was the nightingale.'

But Romeo is not convinced: 'It was the lark, the herald of the morn, No nightingale: look, love, what envious streaks Do lace the severing clouds in yonder east: Night's candles are burnt out, and jocund day Stands tiptoe on the misty mountain tops.'

Gray, like Wordsworth, notes song-flight and song: 'the skylark warbles high His trembling thrilling ecstasy; And, lessening from the dazzled sight, Melts into air and liquid light.'

Meredith attempted to describe the song: 'He drops the silver chain of sound, Of many links without a break, In chirrup, whistle, slur and shake ... A press of hurried notes that run So fleet they scarce are more than one.'

In the finest of all the poems inspired by the Skylark, which Shelley heard 'while wandering among the lanes' near Leghorn, he devised a stanza to represent its continuous, trilling melody: 'Sound of vernal showers On the twinkling grass, Rain-awakened flowers, All that ever was Joyous, and clear, and fresh, thy music doth surpass.'

Shelley heard his Skylark 'on a beautiful summer evening', but most of the poets associate the song with break of day. This is especially the time for song, before the busy human world has filled the air with discordant sounds, and the dawn chorus must have delighted many when getting up with the lark was the normal custom. The best description of this is Michael Drayton's in Poly-albion, where he writes of the birds of his native Warwickshire greeting the dawn in the Forest of Arden-where else, indeed, should a friend and neighbour of Shakespeare choose?-and he names many birds which 'with their deere open throats Unto the joyfull Morne so straine their warbling notes That Hills and Valleys ring, and even the ecchoing Ayre Seemes all compos'd of sounds.'

Among these he names the Woodlark, which Gerard Manley Hopkins made the subject of an unfinished poem, where he transcribes the song: 'Teevo cheevo cheevio chee: o where, what can that be? Weedio-weedio: there again! So tiny a trickle of song-strain.'

William Browne has a description of 'a musical concert of birds' no doubt in his native Devon: 'The lofty treble sung the little wren; Robin the mean, that best of all loves men; The nightingale the tenor, and the thrush The counter-tenor sweetly in a bush ... The crow was willing they should be beholding For his deep voice, but being hoarse with scolding, He thus lends aid; upon an oak doth climb And nodding with his head, so keepeth time.'

Poetry, birds in

Poets of the greatest age of English music, in the 16th and 17th centuries, were especially responsive to the song of birds. Henry Vaughan, different from other poets as always, thought of a bird waking from sleep: 'Hither thou com'st: the busie wind all night Blew through thy lodging, where thy own warm wing Thy pillow was. Many a sullen storm (For which course man seems much the fitter born,) Rain'd on thy bed And harmless head. And now as fresh and chearful as the light Thy little heart in early hymns doth sing.'

John Clare may rival Skelton and Drayton for the number of birds whom he mentions, among them some which seldom enter poetry, such as the Snipe, Yellowhammer, Blue Tit, Sand Martin, Corncrake and Firetail (Redstart) which, apprehensive when a hedger stops a gap near her nest in a hollow tree, 'Of everything that stirs she dreameth wrong And pipes her "tweet tut" fears the whole day long.'

And, when his mind had broken, he could still delight in the birds he knew: 'Little trotty wagtail he went in the rain, And twittering, tottering sideways he ne'er got straight again. He stooped to get a worm, and looked up to get a fly, And then he flew away ere his feathers they were dry.'

But it is not the province of the poet to contribute detailed knowledge of the lives and habits of individual species and it is often pointless to try to make precise identifications. One of the strangest legends about the song of birds is of the swan-song-the song which the swan was said to sing only as a prelude to its own death. Certainly the Greeks, among whom the legend arose, would not have differentiated between Mute and Whooper Swans, both of which occur in the north, but it is tempting to suppose that the species which gave rise to the legend was the Whooper. Alcaeus said that swans transported Apollo to the land of the Hyperboreans, to the uttermost north, and Aristophanes said that the birds 'clattered their wings together in praise of Apollo, and through an aery cloud came their cry.' Perhaps someone noticed the musical cry of Whoopers before they left in the spring and, not seeing them again, devised the legend of the swan-song. The unrelated myth of Zeus taking the shape of a swan to woo Leda, who laid the egg (or two eggs) from which hatched Helen of Troy and the Heavenly Twins, was first told by Euripides and has attracted many painters and poets since his time, including W.B. Yeats who wrote a fine sonnet-his only sonnet-on the theme. But that story cannot reward ornithological research. The Wild Swans at Coole shows Yeats watching unmythical birds at a favourite place of his, and yet imagining them to have that timelessness which Keats imagined for his Nightingale. Birds' lack of individual characteristics seems to deprive them of those personal qualities whose passing is the source of so much human grief. Swans are large and conspicuous not small and retiring like so many song-birds, but these man has long kept in cages and aviaries, where the poets have praised or lamented them. Catullus' address to and elegy on Lesbia's sparrow are probably the most famous of these, but by no means the earliest. The Greek Anthology includes a number of epitaphs on tame partridges-Alcibiades kept a pet Quail-or on song-birds, some of which had been killed by cats, and Catullus knew Simias' epitaph on a partridge. Some have doubted whether Lesbia's pet was a humble sparrow, but it chirruped (pipiabat) and sparrows are still kept as pets in Italy, as in England in the 16th century. Skelton wrote a long poem, and his best, when Jane Scrope's pet sparrow was killed by the nunnery cat, and though he was more interested in Jane than in her pet there is no reason to doubt that it was a sparrow: indeed the lecherous disposition of sparrows was something that Skelton could exploit. Sidney pretended to be jealous of Stella's pet sparrow which, like Jane Scrope's and George Gascoigne's and like himself, was called Philip. Skelton, who names 75 birds in his poem-far more than Shakespeare in all his works-followed the medieval tradition of birds attending a requiem mass, as does Shakespeare in The Phoenix and Turtle; but this tradition derived ultimately from Ovid who, in his elegy on a parrot (Amores 11.6) summoned the birds to its funeral. 'Psittacus, Eois imitatrix ales ab Indis, occidit: exsequias ite frequenter, aves; ite, piae volucres, et plangitepectora pinnis et rigido teneras ungue notate genas.'

477

Later Statius also wrote a lament for a dead parrot. They were fashionable pets in Imperial Rome. If the poets' sympathies are usually with the owners of the pet birds there are, nevertheless, some whose imagination is touched by the bird's imprisonment in a cage. Everyone knows Blake's 'A robin redbreast in a cage Puts all Heaven in a rage,'

but the exaggerated violence of expression is far less acceptable than Chaucer's gentle understanding: 'Tak any brid, and put it in a cage, And do al thyn entente and thy corage To fostre it tendrely with mete and drinke, Of aile deyntees that thou canst bithinke, And keep it al-so clenly as thou may; Al-though his cage of gold be never so gay, Yet hath this brid, by twenty thousand fold, Lever in a forest, that is rude and cold, Gon ete wormes and swich wrecchednesse. For ever this brid wol doon his bisinesse To escape out of his cage, if he may; His libertee this brid desireth ay.'

Thomas Hardy, seeing a caged bird whose eyes had been put out, and hearing it singing, made a subtle contrast with man by adapting St Paul's words on charity: 'Who hath charity? This bird. Who suffereth long and is kind, Is not provoked, though blind And alive ensepulchred? Who hopeth, endureth all things? Who thinketh no evil, but sings? Who is divine? This bird.'

Cowper, who wrote an elegy On theDeath of Mrs Throckmorton's Bulfinch (which was killed by a rat) wrote a better poem On a Goldfinch starved to death in his cage: 'Time was when I was free as air, The thistle's downy seed my fare, My drink the morning dew; I perch'd at will on ev'ry spray, My form genteel, my plumage gay, My strains for ever new.'

But man's cruelty and neglect brought this happy liberty to an end. A more unusual epitaph, for this is on a wild bird, is Samuel Rogers' On a Robin-Redbreast, which was 'inscribed on an urn in the flower-garden at Hafod.' 'Tread lightly here, for here, 'tis said, When piping winds are hushed around, A small note wakes from underground, Where now his tiny bones are laid. No more in lone and leafless groves, With ruffled wing and faded breast, His friendless, homeless spirit roves; -Gone to the world where birds are blest! Where never cat glides o'er the green, Or school-boy's giant form is seen; But Love, and Joy, and smiling Spring Inspire their little souls to sing!'

Poems about Robins are innumerable, for it is familiar in most English gardens where its confiding nature and attractive song, which is repeated in autumn when most other birds are silent, endears it to man. The nursery rhyme, Who killed cock robin? has been known to generations of children, probably from the 15th century on; and the strange legend that the robin 'fynding the dead body of a Man or Woman, wyll cover the face of the same with Mosse', was attached to the story of the Babes in the Wood, and so again made known in the nursery. Both the ballad and the legend date from the late 16th century, if not earlier. Only a bird as well known to man as the Redbreast could have acquired a nickname, which indeed has now become its usual name, just as 'Jackdaw' has supplanted the older 'daw'. The rascally repute of this bird has also been established by the Ingoldsby Legend of The Jackdaw of Rheims, one of the most amusing poems about a bird. By contrast with such anthropomorphic accounts of birds Marvell has a vivid description of the Hewel (Green Woodpecker) who 'walks still upright from the Root, Meas'ring the Timber with his Foot; And all the way, to keep it clean, Doth from the Bark the Wood-moths glean.'

478 Poetry, birds in

Clearly he had enjoyed watching a wild woodpecker about its daily life. Emigrants from Britain to the New World were seldom poets, but Alexander Wilson, the Scottish pedlar poet author of the American Ornithology (1808-14), wrote of American birds which had not previously been celebrated in verse: the Ruby-throated Hummingbird which 'Sips with inserted tube the honeyed blooms, And chirps his gratitude as round he roams.'

And he notes the iridescence of the plumage, where 'Each rapid movement gives a different dye.'

He has poems descriptive of other American birds, among them the Blue Jay and the tyrant flycatcher or Kingbird. This then was persecuted and Wilson sought to dispel prejudice by presenting the reader with a short poetical description of its life-history. Edna Millay's Bobolink is more about herself than the bird, and Robert Frost's charming poem On a Bird Singing in its Sleep does not identify the species. Poe's Raven has the traditional, sinister qualities but is as mythical as Coleridge's albatross. Men have kept birds not only as pets, for the beauty of their plumage and the charm of their song, and for food, but also for sport, especially the noble sport of FALCONRY which provided imagery for medieval poets and for Shakespeare. In 2 Henry VI there is reference to flying at the brook, and Michael Drayton, again, provides the best poetic account of this sport in the Norfolk section of Poly-Olbion, where the quarry is wildfowl. Drayton clearly had first-hand knowledge of the sport through Sir Thomas Monson and Sir Henry Goodere, both of whom he knew well, and both of whom were noted falconers. The later and less aristocratic sport of shooting has also been noted by the poets, perhaps best of all by Pope in Windsor-Forest, though the prey here would not all be at risk from modern sportsmen: 'With slaught'ring Guns th' unweary'd Fowler roves, When Frosts have whiten'd all the naked Groves; Where Doves in Flocks the leafless Trees o'ershade, And lonely Woodcocks haunt the watry Glade. He lifts the Tube, and levels with his Eye; Strait a short Thunder breaks the frozen Sky. Oft, as in Airy Rings they skim the Heath, The clam'rous Lapwings feel the Leaden Death: Oft as the mounting Larks their Notes prepare, They fall, and leave their little Lives in Air.'

Thomson's humanitarian sentiment deflected him from describing the sport: 'These are not subjects for the peaceful muse, Nor will she stain with such her spotless songThen most delighted when she social sees The whole mix'd animal creation round Alive and happy.'

The ancient Japanese custom of fishing with trained cormorants has been celebrated in tankas and it may be that the training of cormorants demands similar patience and skill to the training of falcons. Hopkins' poem The Windhover is a masterpiece on a falcon (Kestrel) but has no reference to the sport; there are few poems about birds of prey outside the context of falconry, though Alexander Wilson has one on the Osprey. Even eagles have not found much favour with the poets, apart from their legendary ability to gaze at the sun and their identification in Greek myth with Zeus as was fitting for the 'feathered king'. Tennyson's six lines, which recall the legend, surpass all others: 'He clasps the crag with crooked hands; Close to the sun in lonely lands, Ringed with the azure world, he stands. The wrinkled sea beneath him crawls; He watches from his mountain walls, And like a thunderbolt he falls.'

Seabirds are as remote from man as eagles, and the most famous of them in poetry, the Ancient Mariner's albatross, is a symbol rather than a bird-a bird which Coleridge had never seen. As we might expect, it is poets from the highland zone of Britain who have written of seabirds: Dafydd ap Gwilym has an elegant cywydd to a snow-white gull on the margin of the sea, and in the Anglo-Saxon Seafarer there is mention of the clamour of Gannets and the crying of 'sea-mews'. But the finest description is James Thomson's in Autumn: Or, where the Northern Ocean in vast whirls Boils round the naked melancholy isles Of farthest Thule, and th' Atlantic surge Pours in among the stormy Hebrides,

Who can recount what transmigrations there Are annual made? what nations come and go? And how the living clouds on clouds arise, Infinite wings! till all the plume-dark air And rude resounding shore are one wild cry?

Thomson's birds are immersed in activities which have nothing to do with man. In Norway, too, Ibsen has some well-observed poems about seabirds. With these one might place Shakespeare's well-known lines about a Dabchick, which he had clearly observed, though, as usual, he requires it only for a simile for human behaviour: 'Like a dive-dapper peering through a wave, Who, being looked on, ducks as quickly in.'

The nocturnal owls, remote from man in another way, have, by their stealthy flight and eerie cries, always seemed sinister, and this has perhaps been enhanced by their facial discs and frontal gaze, 'the staring owl' of Shakespeare, which has some human suggestion. The 13th century poem of The Owl and the Nightingale, in which the two birds debate the matter of what benefits they confer on man nevertheless has some natural charm of observation though the two birds are very anthropomorphic. Aristophanes' comedy The Birds, first produced at Athens in 414 BC, remains the most comprehensive and in many ways most remarkable of all European tributes to birds. It exhibits man's world seen through the eyes of birds, and, inevitably, seen as comic, an ornithomorphic view of man, so to say. It includes 'scraps of birdlore culled from every quarter-from history, poetry, legend, fable, proverb, and personal observation,' from all the varied responses of man to the fascination of birds. It could only have been written by a man who enjoyed looking at and listening to birds, and perhaps better than any other piece sums up what European poets for nearly 3,000 years have been writing about birds. E.J.M.B. Chapin, C. 1937. The Bird-Lovers' Book of Verse. London. Douglas, N. 1928. Birds and Beasts of the Greek Anthology. London. Geikie, A. 1916. The Birds of Shakespeare. Glasgow. Harting, J.E. 1871. The Ornithology of Shakespeare. London. Henn, T.R. 1972. The Living Image. London. (Especially for Falconry) Hilditch, G. 1954. In Praise of Birds. London. Lack, D. 1950. Robin Redbreast. Oxford. Lockley, R.M. 1958. The Bird Lover's Bedside Book. London. Massingham, H.J. 1922. Poems about Birds. London. Munsterberg, P. 1980. The Penguin Book of Bird Poetry. London. Paton, N. 1894. The Birds and the Bards. Pollard, J. 1977. Birds in Greek Life and Myth. London. Priestley, M. 1937. A Book of Birds. London. Robinson, P. 1883. The Poets' Birds. London. Thompson, D' A. W. 1936. A Glossary of Greek Birds. London.

POIKILOTHERMAL: 'cold-blooded', opposite of (see HEAT REGULATION).

HOMOIOTHERMAL

POINTED·TAIL: substantive name of Berlepschia rikeri (see

OVEN..

BIRD (1)).

POISONING: see TOXIC

CHEMICALS.

POISONING, LEAD: see DISEASE; and under

GRIT.

POLIOPTILINAE: see GNATCATCHER. POLLINATORS: agents-avian in this context-in the pollination of plants. Birds may be predators on plants or they may be used by plants as agents of pollen flow or SEED DISPERSAL. In the latter cases, the plants have adaptations for attracting birds and often for restricting less efficient visitors. There has evidently been a long history of co-evolution between birds and plants, in the course of which mutual adaptations have been acquired. In typical bird-pollinated flowers the corolla tube is long and generally narrow, the ovary is inferior, and the nectar, which is produced mostly during the day when the flower is open, is stored at the base of the corolla. The colour is very often (but by no means always) red. Bird-flowers usually do not produce a scent or have nectar guides that might facilitate insect visits. Within bird-flowers there are even more

Polyandry

refined specializations that limit the .range of bird species that can visit each flower efficiently. Birds of a wide variety of families (hummingbirds, honeyeaters, sunbirds, orioles (Icteridae), tanagers, finches, estrildid finches, flowerpeekers etc.) visit flowers and, at least sometimes, remove nectar. Not all of these visitors effect successful pollination. Some birds (e.g. estrildids and finches) remove and mandibulate the flower to force nectar out; others, such as some honeycreepers (Thraupidae), may probe into the nectar chamber through the corolla wall, contacting neither the stigma nor stamens. These nectar thieves have probably been important selective agents for the evolution of thick corollas and inferior ovaries. Birds adapted for feeding on flower nectar often have relatively long bills, and extensible tongues with fringed bifurcated tips. The tongue of sunbirds and hummingbirds has a longitudinal trough in which nectar moves by capillary action. In neither group is the trough sufficiently enclosed to permit a 'soda straw' sucking action. Other, less specialized nectar feeders among birds have fringe-tipped tongues (e.g. the 'brushtongued' parrots), but generally lack the bifurcated tip. Legitimate visitors to flowers probe through the distal corolla opening to reach the nectar chamber at the base of the corolla, at the same time either depositing or removing pollen. The position of stamens and stigma differs in different bird-flowers, and this may help to ensure that the pollen removed by a bird is transferred to another flower of the same species. The pollen of bird-flowers is generally sticky and may coat the bird's surfaces. There is very little evidence that birds regularly eat pollen (though this may be an important source of amino acids for some insects and bats) or are searching for insects in the flowers that they probe (despite categorical statements in the earlier literature). They visit the flowers only for the nectar, which in the case of specialized nectarivores provides their main energy source. The composition of floral nectar includes (in addition to water) sugars, usually composed primarily of sucrose, glucose and fructose; small amounts of polysaccharides; and small quantities of other substances (see below). Nectar in bird-pollinated flowers varies at least from 10% to about 50% sugar concentration by weight, the majority being in the range 15-25%. Insect-pollinated flowers tend to have somewhat higher concentrations of sugar, and also nectar that varies widely in concentration through time as a result of evaporation from the more open flowers. The other substances contained in nectar include amino acids, proteins and lipids. While some of these are of some nutritional potential for birds the concentrations tend to be lower in bird-pollinated than insectpollinated flowers. The few hummingbirds that have been tested in the laboratory either reject or show no preference for sugar solutions containing amino acids at approximately natural concentrations. It seems to be the general rule that nectarivorous birds derive most non-energetic nutrients from insects captured away from the flowers. Most hummingbird-pollinated plants do not have perches that provide direct access to the flowers. Hummingbirds must usually hover while feeding, although where possible they will use an available perch, such as an adjacent leaf. Most other nectar specialists visit plants with convenient perches. Large nectar feeders such as orioles and parrots are facultative visitors although some tropical trees may use orioles as their principal pollinators. Nectarivorous birds may increase the benefit from foraging by preferentially visiting flowers that have accumulated the largest amounts of nectar. Sunbirds, Hawaiian honeycreepers (Drepanididae) and hummingbirds have been shown to organize their visits so as to make the nectar reward per flower more than could be expected from random foraging. This probably involves some memory of locations in a foraging area. Long-term memory has been recorded in hummingbirds that, for example, return to the location of a feeder after a migratory absence. Foraging patterns by nectarivores influence gene flow among the plants at which they feed. Non-random foraging (see above) will tend to equalize the visitation rate to each potential pollen donor and recipient. Behavioural interactions among the pollinators will also influence geneflow between plants. Thus a territorial bird, defending a concentrated group of flowers, will generally carry pollen only over short distances, while a bird that feeds on flowers that are too sparse to be suitable to defend as a feeding territory will carry pollen over longer distances. The effect on the plants will depend on the degree of local adaptation. For at least one insect-pollinated plant, Delphinium nelsoni, there is evidence that pollen flow over relatively short distances increases individual

479

reproduction. Shorter or longer distances of pollen movement may disrupt local adaptations and lower reproductive success through reduced seed set or reduced viability of offspring. Colour, especially red, is often assumed to play an important role in attracting bird visitors to flowers. However, hummingbirds will visit flowers (and feeders) displaying colours from near ultraviolet to red, provided that they obtain nectar rewards. The importance of red may lie in the contrast with green foliage as well as in the ability of birds to discriminate red wave lengths. Some insects, at least, are less capable or incapable of red discrimination, so that colour may function to restrict insect visitors to hummingbird-flowers. See photo FEEDING HABITS. L.L.W.

POLYANDRY: general term for mating systems in which individual females regularly mate with two or more males in the course of a breeding season. Polyandrous mating systems are confined to a few groups of non-passerine nidifugous birds, in nearly all of which each nest is tended by a single parent-in most cases the male only, in a few cases by the male and female at separate nests. It is often combined with a reversal of the usual sex roles in courtship, the female being larger and more brightly coloured than the male and playing the dominant role. In contrast to POLYGYNY, which is characteristic of seed-, fruit- and nectar-eating birds, polyandrous species mostly eat animal food. The main feature of typical polyandrous breeding systems is that the male takes charge of the eggs laid by his mate, thus freeing her to lay another clutch for another male. Hence polyandry is normally successive (or serial). Simultaneous polyandry is known in two species of hawks, one species of jacana, the Tasmanian Waterhen Tribonyx mortierii, and the Noisy Miner Manorina melanocephala, a honeyeater with a highly developed group breeding system. The reasons for the original reversal of the sex roles in families in which polyandry is the rule are not known. When the contributions of the two sexes to the care of the nest and young are unequal, the female will normally be expected to take the greater part, as her investment in the reproductive effort is the greater (see MATING SYSTEM). Whatever the original causal factors in the various groups in which it occurs, polyandry is clearly adaptive in making possible an increase in the reproductive output, especially when conditions suitable for breeding are shortlived. In principle it can easily be derived from a monogamous breeding system in which the female lays 2 clutches of eggs, the first of which her mate incubates while she takes charge of the second. The following treatment is systematic, and includes all groups of birds in which polyandry has been reliably reported. Ratites. The Australian Cassowary Casuarius casuarius practises successive polyandry. Pairs are formed, but after laying the female leaves the clutch to the male and may mate with one or more further males. (The nesting behaviour of the Emu Dromaius novaehollandiae is similar, but females apparently do not normally pair with a second male.) In the Greater Rhea Rhea americana successive polyandry is combined with harem polygyny. The male collects a harem of females, all of whom lay in his nest. He then takes sole charge of the nest and eggs and the females move on and mate with another male. Mating systems vary geographically in the Ostrich Struthio camelus; in the East African race at least (S. c. massaicus), females mate promiscuously with several males. Tinamous. The breeding systems are varied in this family, but in all species that have been studied in detail the male takes charge of the nest and its contents. Some species are monogamous; in others there is successive polyandry, and in at least 3 species successive polyandry is combined with harem polygyny (see POLYGYNY). Hawks. The Galapagos Hawk Buteo galapagoensis practises what has been called 'co-operative polyandry' (Faaborg et alI980). One to 4 males mate with a single female, and all males help in the care of the eggs and young. Polyandrous groups apparently breed more successfully than monogamous pairs. Less complete evidence indicates that the breeding system of Harris's Hawk Parabuteo unicinctus of desert areas of North America is similar. In these cases polyandry seems to be an adaptive response to breeding in habitats where food resources are poor or unpredictable. Partridges. In the Red-legged Partridge Alectoris rufa in captivity, after pair formation the female lays a clutch of eggs which her mate incubates and then a second clutch which she herself incubates. In the wild, however, there is evidence that females may lay clutches for successive males.

480

Polyboroidinae

Buttonquail. Successive polyandry appears to be the rule. There is some evidence for it also in the related Plains-wanderer Pedionomus torquatus (sole member of the Pedionomidae), and in one of the 3 species of mesites (Mesitornithidae), another related family. Possibly therefore the system evolved early in the evolutionary history of this section of the Gruiformes. Rails. The Tasmanian Waterhen lives in groups, each female associating with one to 3 males. All of them mate with her and help to raise her young. Jacanas. Successive polyandry is the rule in the Indian species Hydrophasianus chirurgus, and probably in Metopidius indicus. The Neotropical species J acana spinosa has a system of simultaneous polyandry. Each female has from one to 4 males which hold sub-territories within her own territory. Females are generally larger than males in all species; in Jacana spinosa the difference is extreme, females weighing 75% more than males. Painted snipe. Successive polyandry is the rule, at least in the Old World species Rostratula benghalensis. The female is larger and more brightly coloured than the male. Sandpipers, plovers and phalaropes. Most sandpipers and plovers seem to be normally monogamous, but successive polyandry occurs in a number of northern and montane species. The initial stage in the evolution of polyandry in this group is probably shown by Temminck's Stint Calidris temminckii, a species which seems normally to be monogamous: the female lays 2 successive clutches, the first of which is incubated by the male and the second by the female. A similar system probably occurs in the Little Stint C. minuta, Sanderling C. alba, and Mountain Plover Charadrius montanus. In the Spotted Sandpiper Actitis macularia polyandry is more advanced, females laying a succession of up to 4 clutches for different males, the last of which they help in incubating. In the Dotterel Eudromias morinellus the system seems to be essentially the same, but females are not recorded as laying more than 2 successive clutches. In the phalaropes the mating system has long been controversial. Polyandry (successive) was assumed, and recent research has confirmed it for the Red-necked Phalarope Phalaropus lobatus and Grey Phalarope P. fulicarius (see PHALAROPE). Honeyeaters. The Noisy Miner of eastern Australia has a highly developed communal breeding system (Dow 1978). Females may mate with several males of the group to which they belong, and as many as 14 different males have been seen feeding the young in one nest. Though the system qualifies as polyandrous, it is rather one of promiscuity modified by the dominance relations obtaining among the males, the dominant male of a group achieving most of the copulations. D.W.S. (1) Bruning, R. F. 1975. Social structure and reproductive behavior in the Greater Rhea. Living Bird 13: 251-294. Dow, D.D. 1978. Reproductive behavior of the Noisy Miner, a communally breeding honeyeater. Living Bird 16: 163-186. Faaborg, J., de Vries, T., Patterson, C.B. & Griffin, C.R. 1980. Preliminary observations on the occurrence and evolution of polyandry in the Galapagos Hawk (Buteo galapagoensis). Auk 97: 581-590. Goodwin, D. 1953. Observations on voice and behaviour of the Red-legged Partridge Alectoris rufa. Ibis 95: 581-614. jenni, D.A. & Collier, G. 1972. Polyandry in the American jacana (Jacana spinosa). Auk 89: 743-765. Lancaster, D.A. 1964. Life history of the Boucard Tinamou in British Honduras. Part II: breeding biology. Condor 66: 253-276. Ridpath, M.G. 1964. The Tasmanian Native Hen. Aust. Nat. Hist. 14: 34&-350. (See also references under MATING SYSTEM.)

POL YBOROIDINAE: see POLYGAMY: see MATING

HAWK.

SYSTEM.

POLYGYNY: general term for mating systems in which individual males regularly mate with two or more females in the course of a breeding season; thus excluding the cases of occasional bigamy recorded in many normally monogamous species. For general considerations of the part played by the two sexes in the care of eggs and young, see under MATING SYSTEM.

A clear-cut classification of the many forms of polygyny is hardly possible, partly because of their variety and variability and partly because of inadequate knowledge of the biology of many of the species concerned. A distinction is usually made between (1) harem polygyny, in which a male maintains simultaneous pair-bonds with two or more females,

(2) successive (or serial) polygyny, in which a male pairs with two or more females in succession, and (3) promiscuity (often associated with LEK displays), in which the male mates with as many females as offer themselves to him, and no pair-bonds are maintained. 'Promiscuity'is, however, not a very suitable term, as females of such species are by no means promiscuous but highly selective in their choice of mates, though males may be relatively undiscriminating. The term 'polybrachygamy' (many brief matings) has been proposed by Selander (1972). In some ratites and tinamous harem polygyny is combined with POLYANDRY. A distinction may also be made between 'resource-based' polygyny, in which the male makes some resource, over which he has control, available to the females with which he mates, and polygyny that is not based on any resource, in which the male contributes nothing but his genetic material to the reproductive effort of the females with which he mates. This distinction is biologically important, but in particular cases it is not always possible to decide, on the evidence available, whether a system is resource-based or not. A further difficulty arises, in some cases, in attempting to distinguish polygyny from promiscuity in species which have not received detailed study with marked individuals. One of the main preconditions for the evolution of polygyny is that the female should be able to tend the eggs and young single-handed, or with only a small amount of assistance from her mate. This condition is met in several of the groups of birds in which polygyny occurs (e.g. game-birds, waders, hummingbirds), but it applies less obviously to polygynous species in passerine families in which monogamy is the rule. In these cases it seems that polygyny results from certain features of the habitat and associated food resources. It is found especially in species that exploit highly productive but structurally simple habitats, in which food is concentrated in a narrow spatial range (e.g. some marsh birds), or habitats that offer widespread feeding areas but restricted nest-sites (e.g. some colonial tree-nesters). In such conditions some males may be able to control territories in which two or more females may be able to breed successfully, while less successful males may obtain suboptimal or unsuitable territories, or none at all. A further factor favouring polygyny may be a domed or hole nest, which reduces the energetic costs of incubation and feeding the young and so may make it easier for the female alone to tend the nest (e.g. wrens, dippers). Since the functional classification is difficult, for the reasons given above, the following treatment is systematic, and includes all groups of birds in which polygyny has been reliably reported. Lek species are mentioned but not dealt with in detail; for a fuller treatment see under LEK.

Ratites. In the Greater Rhea Rhea americana the male collects a harem of up to 15 females, all of whom lay in his nest. He then takes sole charge of the eggs and young while the females move on and lay for another male (harem polygyny combined with successive polyandry). In the Ostrich Struthio camelus mating systems differ in different populations. Males of the southern race (S. c. australis) collect a harem of females who all lay in one nest, but the dominant female helps the male in incubation and all the females help in care of the young. In the E. African race (S. c. massaicus) several females lay in one nest but a harem is not formed; only one female, the 'major' female, remains associated with the male and his nest. (In the Emu Dromaius novaehollandiae monogamy seems to be the rule.) Tinamous. In at least 3 species (Nothocercus bonapartei, Nothoprocta cinerascens and Crypturellus boucardi) the breeding system is essentially the same as in the Greater Rhea: the male collects a harem of several females, which lay in his nest and then move on to another male. Other tinamous are monogamous or serially polyandrous; in all of them the male takes charge of the nest and its contents. Bittern. Males of the Bittern Botaurus stellaris (and possibly other Botaurus spp.) may have several females nesting within their territories. Presumably this is a case of harem polygyny, but it needs further study. Nothing comparable has been recorded in other members of the Ardeidae. Ducks. In contrast to the great majority of the species, the tropical ducks of the closely related genera Cairina and Sarkidiornis (Muscovy and Comb Ducks) are reported to be promiscuous, each drake copulating with several females. The Musk Duck Biziura lobata of Australia is also promiscuous. The evidence comes mainly from birds in captivity, and more detailed observations on wild birds are needed. Harem polygyny may be involved. Harriers. Polygyny is regular in the Hen Harrier Circus cyaneus,

Polymorphism

Montagu's Harrier C. pygargus, and probably Marsh Harrier C. aeruginosus. In the Hen Harrier as many as 7 females have been recorded breeding in an area occupied by a single male. Game-birds. Several species of grouse (Tetraoninae) and the Great Argus Argusianus argus and Crested Argus Rheinartia ocellata (Phasianidae) have lek displays. In the Common Pheasant Phasianuscolchicus, and probably many other pheasants with pronounced sexual dimorphism, the system is one of harem polygyny; the male contributes to the reproductive success of his mates by feeding them in the period before egg-laying, and they may benefit by nesting within his defended territory. Mating systems in the Phasianidae need further study, ranging as they do from monogamy (e.g. partridges) to lek systems; almost certainly there is wide variation in the development of polygyny, linked with the extent of the male's contribution to the reproductive effort of his mates. The Turkey Meleagris gallopauo (Meleagridae) has a system of harem polygyny in which the male apparently contributes nothing except genetic material. Bustards. In the Great Bustard Otis tarda males display in leks and are either promiscuous or perhaps form temporary bonds with particular females; in either case they are polygynous. The Little Bustard Tetrax tetrax has been reported to be polygynous and monogamous; the Houbara Chlamydotis undulata is said to be monogamous. Mating systems in this family need much more study. Waders. Several species that breed at high latitudes in the north are polygynous. In 4 species, the Ruff Philomachus pugnax, Great Snipe Gallinago media, Buff-breasted Sandpiper Tryngites subruficollis, and Pectoral Sandpiper Calidrismelanotos the males are promiscuous, the first 3 of these displaying in leks or 'exploded leks' (see under LEK) to which the females come for mating. Harem polygyny is found in 2 species (Curlew Sandpiper Calidris ferruginea and White-rumped Sandpiper C. fuscicollis) and possibly a third (Sharp-tailed Sandpiper C. acuminata). The Eurasian Woodcock Scolopax rusticola, a woodland breeder, practises successive polygyny (see RODING). Hummingbirds. Polygyny is probably general throughout the family; there is no convincing evidence for monogamy in any species. In the great majority of the species the males contribute nothing except genetic material to the reproductive effort of the females with which they mate. Lek displays occur in several species; in many others males display solitarily. In a few hummingbirds, however, resource-based mating systems occur. In the Anna Hummingbird Calypte anna and the Fierythroated Hummingbird Panterpe insignis males are territorial over flower clumps rich in nectar, and allow access to these food sources to females with which they have mated, and possibly also to their young. Males of the Hairy Hermit Glaucis hirsuta hold territories along stretches of forest stream, within which up to 3 females may nest. In this case it seems that competition for specialized stream-side nest-sites is so strong that the help of the male is needed for effective defence of the nest against conspecifics. Honeyguides. A resource-based mating system of a special kind is found in the Orange-rumped Honeyguide Indicator xanthonotus of the Himalayan foothills. Males defend the huge combs of the bee Apis dorsata, and feed on the wax. Females mate only with comb-holding males, and they and later their young are allowed access to the comb of the male with which they have mated. Casual observations suggest that some African honeyguides may have similar mating systems. Lyrebird. Polygyny is apparently regular in the Superb Lyrebird Menura novaehollandiae of south-eastern Australia. It is not certain whether females form any sort of pair bond with the males with which they mate, but it is known that they may visit more than one displaying male before mating. Cotingas and manakins. Many members of these 2 families are polygynous. The males display either in leks or solitarily, mating with the females that they attract to their display areas. Frugivory seems to be the main predisposing factor in the evolution of polygyny in this group. Thus in the related family Tyrannidae, most of whose members are insectivorous, monogamy is the general rule, but one of the more markedly frugivorous species, Pipromorpha oleaginea, has a lek system analogous to but less highly developed than the lek systems of cotingas and manakins. Dippers. Polygyny appears to be regular in the American Dipper Cinclus mexicanus, and may be expected to occur in other species.

Wrens. Four northern species are regularly polygynous, but so far as known no tropical species are. In the European Wren Troglodytes troglodytes, polygyny is most prevalent in the habitats that are richest in food, and the same is probably true of the Marsh Wren Cistothorus

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palustris of North America. It seems that in this family polygyny is likely to develop when the food supply is rich enough for the female to be able to feed the young effectively single-handed; the male can then increase his reproductive output by acquiring more than one female and reducing the assistance that he gives to each of them. Old World flycatchers. In the Pied Flycatcher Ficedula hypoleuca and Collared Flycatcher F. collaris a proportion of the males are bigamous. The adaptive basis of polygyny is probably essentially the same as in the wrens. Old World warblers. Polygyny is regular in Cetti's Warbler Cettia cetti and the Great Reed Warbler Acrocephalus arundinaceus. In the former, the largest males tend to acquire most females. In the latter, males that occupy territories that are especially rich in food tend most often to be polygynous, and the adaptive basis seems to be the same as in the wrens. Penduline tits. In the Eurasian species, Remiz pendulinus, males build a succession of nests, attracting a female to each one in turn. This system seems to be essentially similar to that of the weaver-birds dealt with below. Buntings. In the Dickcissel Spiza americana a proportion of the males are bigamous. The Corn Bunting Miliaria calandra has also been claimed to be polygynous, but the evidence is conflicting. American orioles etc (Icteridae), Two groups of species in this family, all colonial breeders, are regularly polygynous, the marsh-living blackbirds (Agelaius, Euphagus, Xanthocephalus, and probably other genera) and the tropical tree-nesting caciques (Ostinops, Cacicus, and related genera). In the former group, the main predisposing conditions seem to be that food is generally very plentiful in the best habitats and that a proportion of the males can occupy the best areas and exclude the other males (cf. the Marsh Wren, above, in which similar conditions obtain). The latter group of species are mainly frugivorous, and nestcolonies are in traditional (presumably safe) trees away from feeding areas. Males are much larger than females and take no part in nesting. Successful males may mate with several different females; whether they are promiscuous, as is usually thought, or dominate a part of the colony and mate with the females in that part, needs further investigation. Weavers. Successive polygyny occurs in 3 colonially nesting genera, Ploceus, Bubalornis and Euplectes. Males build a succession of nests, displaying at each newly completed nest to attract a female and then building another as soon as the previous one is occupied. There is an evident correlation between polygyny and diet in this family; thus the polygynous species are all seed-eaters, while the insectivorous species are monogamous. Australian magpies (Cracticidae). In Gymnorhina tibicen, a group breeder, a male may mate with one to several females in his group. Mating and other relationships within this and other group-breeding species are dealt with more fully under CO-OPERATIVE BREEDING. Birds-of-paradise and bowerbirds. Polygyny is the rule in most members of these 2 families. Males display either solitarily or in leks and take no part in the nesting duties. As in the cotingas and manakins, a mainly frugivorous diet seems to be an important predisposing condition for the evolution of polygyny. D. W. S. (1) Balfour, E. & Cadbury, C.]. 1979. Polygyny, spacing and sex ratio among Hen Harriers Circus cyaneus in Orkney, Scotland. Ornis Scand. 10: 133-141. Bibby, C.]. 1982. Polygyny and breeding ecology of the Cetti's Warbler Cettia cetti. Ibis 124: 288-301. Cronin, E.W. & Sherman, P.W. 1976. A resource-based mating system: the Orange-rumped Honeyguide. Living Bird 15: 5-32. Lill, A. 1979. An assessment of male parental investment and pair bonding in the polygamous Superb Lyrebird. Auk 96: 489-498. Price, F.E. & Bock, C.E. 1973. Polygyny in the Dipper. Condor 75: 457-459. Selander, R.K. 1972. Sexual selection and dimorphism in birds. In Campbell, B. (ed.). Sexual selection and the descent of man: 18~230. London. Siegfried, W.R. 1979. Social behavior of the African Comb Duck. Living Bird 17: 85-104. Verner, ]. 1964. Evolution of polygamy in the long-billed marsh wren. Evolution 18: 252-261. Wolf, L.L. & Stiles, F.G. 1970. Evolution of pair cooperation in a tropical hummingbird. Evolution 24: 759-773. (See also references under LEK and MATING SYSTEM.)

POLYMORPHISM: term that was defined by Ford (1945) as the coexistence in one interbreeding population of two (dimorphism) or more distinct and genetically determined forms, the least abundant of which is present in numbers too great to be due solely to recurrent mutation. The

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frequency of the rarer form has been variously defined as 1-5% by subsequent authors. The commonest use of the term for ornithologists occurs in relation to distinct plumage colour variants (strictly polychromatism) which have a genetic basis and which are not merely sexual, seasonal or developmental plumage variations. Examples would be the dark and light colour morphs of the Arctic Skua Stercoranus parasiticus or the red and grey morphs of the Screech Owl Otus asio. In recent years, however, polymorphism has been investigated in birds and other organisms at the molecular level using electrophoresis and other techniques to detect discontinuous genetic variation in enzyme systems. The essence of Ford's definition is that the morphs must firstly be phenotypically distinguishable with discontinuities in the phenotype, since polymorphism must not be used to include continuous or quasidiscontinuous variation. These discontinuities, however, need not be obvious to the eye, since enzyme polymorphism requires considerable biochemical manipulation for its detection. Secondly, the phenotypic variants must be genetically distinct and there should be some understanding of the genetic basis of the polymorphism. Minimally it should be demonstrated that there is allelic segregation at at least one gene locus. The difference between discontinuous and continuous genetic variation, while easy to understand conceptually, is often difficult to distinguish in practice. Huxley (1955) considered clutch-size differences in birds to be an example of polymorphism, insofar as clutch-size is a meristic character and a clutch of 2 is phenotypically different from one of 3 eggs. However, as shown by Perrins and Jones (1974), the underlying genetic basis for clutch size variation is presumably polygenic, similar to most continuous phenotypic variation, with no clear correlation of particular genotypes with particular clutch sizes. CLUTCHSIZE variation is clearly quasi-discontinuous variation. Investigations into polymorphism in birds have fallen into 3 major categories: genetic, evolutionary and taxonomic. Genetic studies have been carried out in an attempt to elucidate the genetic basis for the phenotypic discontinuities of polymorphism, but on relatively few species. Genetic differences between red and grey morphs of the Screech Owl have been ascribed to a single pair of alleles with red dominant to grey. Red-footed Boobies Sula sula on the Galapagos Islands have been classified into 3 morphs: Brown, Intermediate and White. In this case two codominant alleles at one locus was the simplest genetic explanation for the polymorphism, the intermediate plumage birds being heterozygous. A similar explanation could account for the polymorphism in Arctic Skuas. Lemmetyinen et al (1974) postulated 2 independently assorting pairs of alleles at each of 2 loci to account for the polymorphism in Arctic tern Sterna paradisaea chicks. Thorneycroft (1966) showed a chromosomal basis for the plumage polymorphism in the White-throated Sparrow Zonotrichia albicollis and other chromosomal polymorphisms have been detected in species showing no detectable phenotypic variation. The genetic tools available to the ornithologist studying polymorphism in a wild population of birds are limited. Since controlled crosses are usually not possible, it is necessary to use data from samples collected in the field where sample size often limits reliability of interpretation. Unless long term studies are carried out with marked birds, it is possible to use family data only if the polymorphism is visible in adult and young birds. Interpretation is also difficult if the genes controlling polymorphism do not obey the HARDY-WEINBERG equilibrium. If, for example, mating between the morphs is not random, it becomes difficult to predict the distribution of the morphs in the offspring of different types of matings. A genetic analysis of families of the dimorphic Lesser Snow Goose Anser caerulescens which did not rely on Hardy-Weinberg equilibrium, led to the postulation of a 2-allele, single gene explanation for the difference between the blue and white morphs of the snow goose, with the allele for blue coloration incompletely dominant over the allele for white. Evolutionary studies in polymorphism have been concerned mainly with the question of natural selection. R.A. Fisher stressed that the presence of a stable polymorphism implies a selective balance between the morphs, with one genotype favoured in some circumstances, another genotype favoured in others. Various explanations have been put forward to explain the maintenance of polymorphism. These include: (a) heterozygote advantage (heterosis) where organisms carrying both alleles (heterozygotes) in a 2-allele polymorphism have a higher reproductive fitness than the homozygotes; (b) negative assortative mating, i.e. the tendency of one morph to choose the other morph as a mate; (c)

frequency dependent selection, where the fitness of a morph varies with its frequency in the population, such that a morph has higher fitness than its alternate when rare and vice versa; and (d) balance of advantages due to temporal or spatial heterogeneity in the environment. Huxley, following Dobzhansky's work with Drosophila, believed that heterozygote advantage was the primary explanation for the maintenance of polymorphism in birds; this has not been shown in the avian literature. Negative assortative mating is the rule in the White-throated Sparrow with tan morphs usually mating with white morphs. It has also been documented in some populations of Arctic Skuas, but is not necessarily the mechanism whereby the polymorphism is maintained. Dark birds could be favoured where early breeding is advantageous, whereas light birds are favoured where late breeding is preferable. Neither of these explanations has been effectively demonstrated. Apostatic selection is selection for variation for its own sake and is thought to be maintained by FREQUENCY DEPENDENT SELECTION, in that a given phenotype is favoured in direct proportion to its rarity through frequency dependent predator pressure. No avian prey species has been demonstrated to be polymorphic due to apostatic selection, but the hypothesis has been extended to include parasitic birds such as cuckoos and predators such as hawks and skuas. It has been argued that the hosts of parasitic cuckoos would be less likely to recognize and respond to a rare morph, which would be to the advantage of that morpho Paulson (1973) has hypothesized that the rarer morphs of a predator would be less familiar to a potential prey individual and thus have a greater chance for successful capture. This advantage should lead to balanced polymorphism and could explain the high frequency of polymorphism in hawks and skuas. In contrast to the classic studies in Lepidoptera where selective differences between the morphs have been amply demonstrated, there are far fewer avian examples. The reasons for this are simple. Fitness differences between morphs would be very small or non-existent and to detect fitness differences over a range of temporal or spatial environments would require extremely large sample sizes. Thus, although Lemmetyinen et al (1974) postulated that grey morphs of the Arctic tern were favoured in areas dominated by grey rocks and brown morphs where the rocks were reddish or the soil sandy, they could detect no differences in reproductive fitness between the morphs in either environment. A notable example is the Lesser Snow Goose. An early study showed the blue morph increasing in frequency at the expense of the white morpho This was accounted for by higher nest predation and hunter pressure on the white phase birds. However, a later study of a different population and with a sample of several thousand birds over 10 years found no differences in reproductive fitness between the 2 morphs. All other measures of reproductive fitness at different stages of the life cycle also showed no differences. An interesting case where disruptive selection pressure has been suggested to account for the dimorphism is the European Cuckoo Cuculus canorus where Voipio (1953) suggested mimicry of 2 common European raptors , the Kestrel Falco tinnunculus and the Sparrowhawk Accipiter nisus, the red morph resembling the former, the grey morph the latter. Similarity to the models, it was postulated, enables the Cuckoo to intimidate the host species. Evolutionary studies have also centred around the question of assortative mating and mate choice. Many species of birds choose mates randomly with respect to morpho There is no evidence of assortative mating in Red-footed Boobies, Screech Owls, some populations of Arctic Skuas, New Zealand Fantails Rhipidura fuliginosa, and Ferruginous Hawks Buteo regalis. In White-throated Sparrows there is strong negative assortative mating. In some populations of Arctic Skuas, and Western Grebes Aechmophorus occidentalis, there is positive assortative mating. In Snow Geese there are elements of both positive and negative assortative mating. Only in Snow Geese has it been shown that the assortative mating is a consequence of mate choice based on morph appearance (Cooke 1978). In this species, a bird from a monomorphic family will generally choose a mate of the same morph as that of its family. By manipulation it has been shown that the choice of a mate is a function of learned experience during the pre-pairing period of the bird's life. This is important because it shows that a learned response can influence the genetic structure of a population, and thus the degree of mixed matings within the population. Kalmus and Maynard-Smith (1966) showed that in theory such a mechanism could lead to speciation of former morphs

Potoo

but only if 1000/0 efficient. In Snow Geese, only 85% of the birds from monomorphic families choose a mate of that family colour. Two other notable examples of evolutionary studies of polymorphic birds are of interest. The Ruff Philomachus pugnax is a polygamous shorebird with males showing a considerable variety of breeding plumage morphs, The darker morphs have greater success at acquiring territories and attracting mates than the white morphs. The genetics of plumage colour in this species are obscure and the reasons for the maintenance of the white morphs are puzzling. A possible genetically based behavioural polymorphism in the Common Eider Somateria mollissima is described by Milne and Robertson (1965). The population consists of migratory and non-migratory birds, the 2 groups having different gene frequencies at a number of gene loci where enzyme polymorphism occurs. Enzyme polymorphisms have been much studied in the hope of discovering more about the genetic structure of bird populations, both inter- and intra-specifically. Enzyme polymorphism as detected by electrophoresis is less frequent among birds than amongst most other taxa studied. Reasons for this are unclear. The third area of interest in polymorphism is taxonomic and systematic. It has been pointed out that visible polymorphism in birds is restricted to relatively few families-Procellariidae, Ardeidae, Accipitridae, Falconidae, Stercorariidae and Cuculidae. Elsewhere it is scattered among one or two species within a family, e.g. Phalacrocoracidae, Anatidae, Phasianidae, Haematopodidae, Scolopacidae, Alcidae, Strigidae, Corvidae, Turdidae, Muscicapidae, Laniidae, Thraupidae and Estrildidae. A well known observation related to polymorphism is the phenomenon of 'ratio-clines', where the proportion of the morphs differs in different parts of the range. A classical example is the Guillemot Uria aalge, where the frequency of the bridled morph increased with latitude from below 0.5% to over 50%. Attempts to relate this and other ratio-clines to differing environment conditions along the clines have seldom been successful. The selective pressures affecting the relative fitness of the morphs are obviously complex and gene flow along the clines must be taken into account. In addition, genetic drift and historical factors playa role. The Lesser Snow Geese which winter on the Gulf Coast of USA consist predominantly of blue morphs at the eastern end of the distribution and white morphs at the west. There is some historical evidence that the 2 morphs were formerly allopatric with blue morphs wintering in the Mississippi delta and the white morphs in Texas. The mixing of the morphs may be recent as a result of historical modification by man of traditional feeding areas by such policies as burning of marshes, and the cline may reflect a stage in the equilibrium of the morphs. Rockwell and Cooke (1977) showed that localized changes in the ratios of the morphs in time and space could be explained largely by gene flow between populations. Why the original difference occurred in the wintering distribution of the morphs is not answered. In the early development of ideas on speciation, major mutations such as those found in polymorphic species were thought to be the origin of new species. Mayr (1970) has summarized the reasons why speciation is now thought to be mainly due to selection acting on genes affecting continuously variable characters differentially in different isolated subpopulations of an originally inter-breeding population. While this is clearly true and generally accepted, there are some interesting species groups where polymorphism may have represented a stage of their evolutionary history. In many taxa there are dark species, light species and polymorphic species consisting of both light and dark morphs (Buteo, Anser(Chen),Phalacrocorax, Haematopus, Ardeidae, Falco,Sula). In Sula for instance, most species are white but the Brown Booby Sula leucogaster is brown and the Red-footed Booby is dimorphic. Most Anser geese have a grey plumage, but the Ross Goose Anser rossii is white and the Lesser Snow Goose dimorphic. Perhaps the Brown Booby and Ross Goose have had a dimorphic period in their evolutionary past. In fact the Ross Goose is polymorphic in its gosling stage. Often polymorphism has not been recognized taxonomically as such. For example, the Brown Jay Cyanocorax morio and the Sooty-capped Bush Tanager Chlorosphingus pileatus, both of which are dimorphic, were formerly each separated into 2 species. Presumably there are many examples of polymorphism as yet undiscovered, particularly in the tropics and in cases where there is a strong ratio-cline. If there is strong positive assortative mating among the morphs, this will appear similar to the hybridization between closely related species. Only a careful genetic analysis will elucidate the true taxonomic status. F.C.

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Cooke, F. 1978. Early learning and its effect on population structure. Studies of a wild population of snow geese. Z. Tierpsychol. 46: 344-358. Ford, E.B. 1945. Polymorphism. BioI. Rev. 20: 73-88. Huxley, I.S. 1955. Morphism in birds. Acta XI Int. Orn, Congr., Basel 1950: 309-328. Kalmus, M. & Maynard-Smith, S. 1966. Some evolutionary consequences of pegmatypic mating systems (imprinting). Amer. Nat. 100 (916): 619-635. Lemmetyinen, R., Portin, P. & Vuolanto, S. 1974. Polymorphism in relation to the substrate in chicks of Sterna paradisaea. Ann. Zool. Fenn. 11: 265-270. Mayr, E. 1970. Populations, Species and Evolution. Cambridge, Mass. Milne, H. & Robertson, F.W. 1965. Polymorphism in egg albumen protein and behaviour in the eider duck. Nature (London) 205: 367-369. Nelson, I.B. 1969. The breeding behaviour of the Red-footed Booby, Sula sula. Ibis Ill: 357-385. Paulson, n.R. 1973. Predator polymorphism and apostatic selection. Evol. 27: 269-277. Perrins, C.M. & Jones, P.I. 1974. The inheritance of clutch size in the Great Tit (Parus major L.). Condor 76: 225-229. Rockwell, R.F. & Cooke, F. 1977. Gene flow and local adaptation in a colonially nesting dimorphic bird: the Lesser Snow Goose. Amer. Nat. 111: 91-97. Thorneycroft, H.B. 1966. Chromosomal polymorphism in the White-throated Sparrow, Zonotrichia albicollis (Gmelin). Science 154: 1571-1572. Voipio, P. 1953. The hepaticus variety and the juvenile plumage types of the cuckoo. Ornis Fennica 30: 97-117.

POLYPHYLETIC: of more than one evolutionary ancestry; applied to an assemblage of species, and contrasted with MONOPHYLETIC. POLYTOPIC: found in different places-applied to a form that has widely separated populations. POL YTYPIC: term applied to a taxon that has more than one unit in the immediately subordinate category, e.g. a genus comprising 2 or more species, or a species divisible into subspecies-contrasted with MONOTYPIC.

POMATORHININI: see BABBLER. POORWILL: substantive name of Phalaenoptilus nuttallii and Nyctiphrynus spp. (see NIGHTJAR; also WHIP-POOR-WILL). POPULATION DYNAMICS: see AGE;

ECOLOGY.

POPULATION INDEX: a measure of population level related to a base figure, usually 100 (see CENSUS). PORPHYRIN PIGMENTS: see COLOUR. PORTAL: term applied, especially, to a system of veins draining the abdominal portion of the alimentary tract and associated organs to the liver, but also to some other systems similarly leading into glandular organs (see VASCULAR SYSTEM). POSTURAL FACILITATION: see FACILITATION, POSTURE: see

POSTURAL.

COMFORT BEHAVIOUR; SIZE; SLEEP.

POTOO: substantive name of the species of Nyctibiidae (Caprimulgiformes, suborder Caprimulgi); in the plural, general term (alternatively 'tree-nighthawk') for the family. 'Potoo' is the creole name for one of the species; it was apparently used for the first time in ornithology by Gosse in Birds of Jamaica (1847). Characteristics. Potoos are 23-50 em in length, rather long-winged and long-tailed birds, with soft cryptic coloration of grey, white, buffish-brown and almost black. The sexes are alike. The downy nestlings are white with narrow dark shafts (Nyctibius griseus) or white barred all over with brown (N. grandis). The bill is small and terminally decurved with a projecting 'tooth' on the maxillary tomium. There is a huge mouth of which the inside is flesh coloured. The legs are very short. The eyes are very large; N. griseus has a bright yellow iris, N. grandis a dark brown one, but both species reflect bright orange at night. Their flight is silent. Habitat. N. griseus and N. grandis inhabit open woodland and also cultivated land, e.g. coffee and citrus plantations. Distribution. The family is confined to tropical Middle and South America. The family consists of a single genus, with 5 species. The Great

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Potoo

Common Potoo Nyctibius griseus. (C.E. T.K.).

Potoo Nyctibius grandis is much the largest (weights from Surinam: 5 males 450--624, mean 533 g; 7 females 504-604, mean 557g). It has been recorded locally in Central America (records from Guatemala, Nicaragua and Panama) and is widespread in South America, south to Peru and Brazil. The best known species, the Common Potoo N. griseus, is considerably smaller (weights from Surinam: 4 males 146-167, mean 156g; 2 females 149, 155g). It has the widest distribution, occurring from southern Mexico east through Central America and throughout South America south to Argentina, and also on the islands of Jamaica, Hispaniola, Gonave, Trinidad and Tobago. The 3 other species are rare and their ranges are probably not fully known. The Long-tailed Potoo N. aethereus is rufous and has a long, markedly graduated tail with the central feathers pointed. It is recorded from Guyana, southern Venezuela, western Colombia, eastern Peru, Paraguay and Brazil. The White-winged Potoo N. leucopterus is distinguishable by its white, black-tipped inner wing-coverts, forming a broad white band on the wing. It is recorded from Venezuela, northern Colombia and the coastal region of Brazil in Bahia. The Rufous Potoo N. bracteatus is the smallest, and is most rufous with the tail feathers barred black and tipped with white. It is recorded from Guyana, Colombia east of the Andes, eastern Ecuador and eastern Peru. Food. The recorded food of N. griseus consists of insects of several orders (Hemiptera, Orthoptera, Coleoptera, Isoptera, Lepidoptera), that of N. grandis of various Coleoptera. Behaviour. Potoos are strictly nocturnal, solitary and arboreal, spending the day sitting in an upright attitude on a branch of a tree or the top of a stump (cf. FROGMOUTH). Head scratching is done indirectly (over the wing). The roost is often used for a long time at a stretch. The birds become active in the evening, especially on bright moonlight nights, catching flying insects. This they do in flight from an elevated perch after the fashion of flycatchers (Muscicapidae), returning with their prey to the observation point. Voice. N. griseus has a strophe of plaintive, very melodious notes in an exactly descending scale. N. grandis has a rich vocabulary, including a guttural Oorroorooo, also a barking wow in which the head is thrown back with the bill pointed upwards. Breeding. The single egg is laid in a small depression on a tree stump or branch, sometimes quite near the ground, but occasionally at a great height. The bird incubates by sitting in an upright position on the egg. When it feels unobserved and is at ease, it incubates with the head withdrawn and the bill pointed forwards, the plumage fluffed and relaxed; on becoming alarmed, the whole bird stiffens and lengthens slowly upwards, the bill pointing straight up and partly open, the eye partly opened into a slit. It can be closely approached and even handled, but then the bird threatens by opening its large eyes, fluffing out its plumage and spreading its tail, snapping its bill and opening wide its huge mouth. The eggs of this species are oval and white without much gloss and are

sparsely marked with small lilac and brown spots. Eggs from Trinidad measure 41.5 x 32.0mm, from Surinam 35.9 x 26.1 mm and from Brazil 36.2 x 29mm. The only known egg of N. grandis, from Brazil, was similar and measured 52.1 x 38.3 mm. Eggs of N. griseus have been found in Costa Rica in December, in Colombia in January, in Trinidad in March, April, July and August, in Surinam in April, and in Brazil in November and December. An egg of N. grandis was found in Brazil in July, and a nestling in Surinam in June. A probable egg of N. aethereus was found in Paraguay in December. Skutch (1970) studied the nesting habits of N. griseus in Costa Rica. He found that both parents incubated, covering the egg continuously except for an interval not exceeding 15min at daybreak and a longer interval of 45-95 min at the beginning of the night. The long nocturnal session and the even longer diurnal session appeared to be continuous and by different parents. They apparently never turned or even touched the egg in its precarious position. The incubation period was at least 33 days. The newly hatched nestling rested from the first facing the supporting branch just as the parents did when incubating and brooding. During the first 2 weeks a parent brooded the nestling, but ceased nocturnal brooding when it was 19 days old and diurnal brooding when it was 25 days old, after which it was always alone. When 10 days old it was fed 15 times by both parents on a moonlight night between nightfall and dawn, and when 35 days old it was fed 10 meals. When being fed, the nestling uttered a hoarse buzz. At the age of 26 days it was first seen to rest on a branch above the nest; at 35 days it was well feathered. Its first short flight was seen when it was 47 days old, and on its 51st day it finally flew from the tree and was not seen again. From the laying of the egg to its departure at least 84 days elapsed. F.H. Borrero, H.A. 1970. A photographic study of the Potoo in Colombia. Living Bird 9: 257-263. Haverschmidt, F. 1968. Birds of Surinam. Edinburgh. Skutch, A.F. 1970. Life history of the Common Potoo. Living Bird 9: 265-280.

POTOYUNCO: a name for Pelecanoides garnotii (see PETREL). POULT: a domestic chicken; sometimes applied to other species. POULTRY: collective term for birds of domesticated species (as distinct from 'game') used for the table (see DOMESTICATION). POWDER DOWN: feathers which produce a fine powder (see FEATHER; PLUMAGE).

PRAIRIE CHICKEN: substantive name of Tympanuchus spp. (see GROUSE).

PRATINCOLE: substantive name of the species of the subfamily Glareolinae (Charadriiformes, suborder Charadrii, family Glareolidae); in the plural, a general term for the subfamily. Pratincoles, like the closely related coursers (subfamily Cursoriinae; see COURSER), are an entirely Old World group found throughout Africa, southern Europe, Asia and Australasia. Only 2 genera are currently recognized: Glareola with 7 species (pratincola, nordmanni, maldivarum, ocularis, nuchalis, cinerea and lactea) and Stiltia with one species (isabella). Australian Pratincole Stiltia isabella is structurally and behaviourally intermediate between the coursers and the pratincoles and, although it shows greater affinity with the pratincoles, it provides a clear evolutionary link between the 2 subfamilies. Characteristics. Like most coursers, Glareola has a pectinated middle toe, but Stiltia does not. Members of the genus Glareola are characteristically short-legged and have short tails; Stiltia is long-legged, has a square tail and a dark belly-band, giving it the appearance of a courser. All the pratincoles have long wings (especially so in Stiltia), a black-and-white tail and rump pattern, plain brown or grey dorsal plumage, little or no sexual dimorphism, a black bill with a bright red or orange base, and a fairly well developed hind toe which is somewhat raised above ground level. Their front toes are much longer than those of the coursers. The long wings are an adaptation to catching flying insects on the wing, although pratincoles also feed on the ground. They measure 18-30 em and weigh 80--100 g. The Collared or Red-winged, Black-winged and Oriental Pratincoles (Glareola pratincola, G. nordmanni and G. mnldivarum) have a narrow black collar bordering the yellowish throat; they are obviously closely related to each other and may be merely races of one species.

Predation

Habitat. All the Glareola species live near water, usually in the form of large rivers, but sometimes marshes or flooded rice paddies. Stiltia is less water-dependent and inhabits open semidesert or dry grasslands, although water is often available in the form of rivers, lakes or temporarily flooded hollows. Distribution and movements. The Collared Pratincole has breeding populations from South Africa north to Europe and east to north-western India; all are migratory, but their movements have yet to be mapped out in detail. The Black-winged Pratincole breeds from south-eastern Europe to western Asia and migrates to Africa when not breeding. The Oriental Pratincole is an eastern Asian breeder, some populations of which migrate southward as far as Australia and rarely to New Zealand. The Madagascar Pratincole G. ocularis breeds on Madagascar and migrates in the non-breeding season (from about April to September) to East Africa. The White-collared Pratincole G. nuchalis of tropical Africa, the Grey Pratincole G. cinerea of West Africa and the Little Pratincole G. lactea of India and southeastern Asia are all resident. They have less deeply forked tails, lack a black collar and are sometimes put in a separate genus, Galachrysia. The Australian Pratincole breeds in northern and central Australia (rarely as far south as Adelaide) and migrates in the southern winter northwards, part of the population remaining in northern Australia and the rest crossing the sea to Indonesia. Food. All pratincoles feed entirely on insects caught on the wing or on the ground. The Australian Pratincole probably feeds mostly on the ground, chasing its prey with a swift run ending in a sudden turn with a wing outstretched, apparently to stop the prey from escaping further. Behaviour. The pratincoles are all highly gregarious at all times, even when breeding. During migration they occur in flocks of several hundred birds. Like coursers, they are especially active in the evening when the flocks zig-zag to and fro with high-pitched calling. Flocks may wheel high in the air, and the riverine species often skim the surface of the water while feeding. Voice. Pratincoles are particularly vocal in flight, although they also have contact calls given on the ground. The notes are high-pitched trilling or twittering in the genus Glareola and beautiful piping whistles in Stiltia. Alarm calls are somewhat harsher in tone. When inactive, pratincoles are mostly silent, often settling in a more or less close pack, all facing in the same direction and remaining motionless and inconspicuous. Breeding. The Glareola species breed colonially near large rivers or marshes, sometimes on rocks in the middle of a river. Their nest is a mere scrape in the ground or a hollow on a rock. The eggs number 1-4 per clutch depending on the species (usually 2-3) and are well camouflaged with their bold irregular dark markings on a light yellowish background. Eggs of the Red-winged Pratincole in southern Africa are very dark-an adaptation to the birds' habit of often nesting on areas of burnt grassland. Their downy young are similarly blackish in colour. The Australian Pratincole also nests in loose colonies, but on open stony semidesert in inland Australia. Like other pratincoles it nests near water, usually temporary pans flooded by recent rain, sometimes up to

485

2 km away. It makes no nest, laying its clutch of 2 eggs on a bare patch of soil among stones or gravel. The eggs resemble stones in colour and texture. The downy plumage of the chicks is pale buff with almost no markings, to match the light coloured clay substrate of the normal breeding habitat. In all pratincoles both sexes incubate almost equally, with a nest-relief occurring every 1-2 hours. In very hot weather (when air temperatures exceed 35°C) the changeovers may be more frequent than this. Incubation is said to take 17-18 days in the Collared Pratincole and 21 days in the Australian Pratincole. The young leave the nest as soon as they are dry, and are led to the shelter of a shady shrub from which they emerge only to be fed by a parent arriving with an insect in its bill. The chicks obtain all their water from their food; like the adults they have a functional salt gland (see EXCRETION, EXTRARENAL) which removes excess sodium chloride and conserves water. The adults drink frequently. In very hot weather at least one species, the Little Pratincole, soaks its belly feathers at the nearest water and flies back to its nest to cool its eggs at each nest-relief which occurs about every half hour (see BELL-SOAKING). Courtship in the pratincoles consists of elegant displays usually involving the wings and head-down body postures. Injury-feigning distraction displays are well developed in all species when they have eggs or young. G.L.M. Maclean, G.L. 1976. A field study of the Australian Pratincole. Emu 76: 171-182. Sterbetz, I. 1974. Die Brachschwalbe. Wittenberg.

PRE-ADAPTATION: see under

ADAPTATION.

PRECOCIAL: active immediately after hatching (see PRECOCIOUS FLIGHT: see

YOUNG BIRD).

FLIGHT, PRECOCIOUS.

PREDATION: the killing of members of one species by members of another species for food (see also FEEDING HABITS); the term is almost entirely confined to discussion of the effects of activities of predators upon the population of the prey species (see also ECOLOGY). A predation study demands a means of ascertaining the numbers in which a species is present in a given area, and the numbers killed within that locality by a known predator. The population may be measured directly or by a sampling method such as the LINCOLN INDEX; the second parameter demands that some visible and measurable traces of the slaughter remain: feathers, bones, skulls, elytra or wings of insects or even rifled dwelling places, as in the cases of the larvae of beetles of the genus Pissodes or of the moth Ernarmonia conicolana, whereof the ravaged and uninvaded wintering chambers can be distinguished. In Holland, remnants at nests and plucking places were used to show that about half the deaths of all House Sparrows Passerdomesticus in the area were due to the talons of Sparrowhawks Accipiter nisus. During a vole plague on the Scottish Border, pellets and stores at nesting sites showed that Short-eared Owls Asio flammeus were making inroads on the rodent population of not more than 0.05% per diem, and that the owls were, in fact, not in any way checking the plague. During an outbreak of Archips fumiferana in the spruce forests of Ontario, S.C. Kendeigh calculated that, at most, bird predation destroyed 50/ 0 of the larvae. There is one classic case of the effects of bird predation being immediately visible: during an outbreak of defoliating insects in Prussia in 1905, the woods of the Baron von Berlepsch, where the nesting of birds had been encouraged, were said to stand out 'among the surrounding woods like a green oasis' (see NEST SITES, MAN-MADE). The incidence of bird predation may vary greatly from year to year in one locality, or within a single season between places very close together. In an area of rural Suffolk, England, 49 samples of marked Helix asperse were released between the years 1956 and 1978. Of 1,009 snails released, 164 were recovered at the anvils of Song Thrushes Turdus philomelos, giving a minimal predation rate of 16%. In the 3 consecutive years 1956 to 1958 predation rates were 44%, 13% and 28%, while in 1963 (after a very severe winter) thrush predation was nil. At 2 sites within 200 m of one another predation rates in 1959 were 44% and 80/0. The effects of predation are not always adverse to the population level of the victim species. It has been demonstrated mathematically that if the

7

Collared or Red-winged Pratincole Glareola pratincola. (C.E.T.K.).

principal cause of death in a species be the attacks of a pathogenic organism, and that if a predator tends to take weakly or sick specimens, the final result of the predation will be to increase the population of the prey species.

486

Preen gland

The effects of predation are not, of course, limited to alterations in the population levels of the prey species. Predation pressure is the effective agent in the evolution of cryptic adaptations of form and behaviour, as has been so clearly demonstrated in the relationship between Song Thrushes and the polymorphic snail Cepea nemoralis. See photo PARENTAL CARE. P.H.T.H. Gibb, J.A. 1958. Predation by tits and squirrels on the eucosmid moth Enarmonia conicolana (Hey.). J. Anim. Ecol. 27: 375-396. Nicholson, A.]. 1936. The balance of animal populations. J. Anim. Ecol. 2: 131-178. Rudebeck, G. 1950-1. The choice of prey and modes of hunting of predatory birds with special reference to their selection effect. Oikos 2: 65-88; 3: 200-231. Sheppard, P.M. 1951. Fluctuations in the selective value of certain phenotypes in the polymorphic land snail Cepea nemoralis (L.). Heredity 5: 125-134. Tinbergen, L. 1946. Der Sperwer al Roofijand van Zangvogels. Ardea 34: 1-213.

see COMFORT BEHAVIOUR; FLIGHTLESSNESS.

BEHAVIOUR.

PROCRYPTIC: see under CRYPTIC. PROEPISEMATIC: see under EPISEMATIC. PROGESTERONE: see ENDOCRINOLOGY AND THE REPRODUCTIVE

SYSTEM.

PROKINESIS: the form of upper jaw mobility seen in the majority of birds (including all with holorhinal nostrils), in which rotation takes place about a region of flexible bone (zone elastica craniofacialis) at the junction of upper jaw and neurocranium. See SKULL.

PROLACTIN: see CROP, MILK; ENDOCRINOLOGY AND THE REPRO-

PREEN GLAND: see COMFORT BEHAVIOUR. PREENING:

Hydrobatidae (Petrel), Pelecanoididae (Diving Petrel). For general characteristics of the family see PETREL.

DUCTIVE SYSTEM. See

photos

COMFORT

PREFRONTAL: a paired bone of the SKULL. PREMAXILLA: the main bone, on each side, of the upper jaw (see SKULL).

PROMEROPIDAE: a family of PASSERIFORMES, suborder Oscines;

SUGARBIRD.

PROOTIC: a paired bone of the SKULL. PROPATAGIUM: a membranous fold of skin along the anterior margin of the wing from shoulder to carpal joint (see MUSCULATURE; WING).

PREMIGRATORY RESTLESSNESS: marked behavioural changes in nocturnal migrants, particularly small passerines, which develop an additional activity rhythm during the hours of darkness, when they normally roost (see MIGRATION).

PROPRIOCEPTIVE: the senses involved when what is perceived is internal (sometimes termed 'interoceptive').

PRICKED: see WINGED.

PROTECTION: see CONSERVATION.

PRICKLETAIL: Siptornisstriaticollis, a South American furnariid (for family see OVENBIRD (1».

PRIMARY: or 'primary feather' , anyone of the flight feathers borne on the manus (carpometacarpus and digital phalanges)-contrasted with the 'secondaries', borne on the forearm (see PLUMAGE; WING). The primaries are best numbered from the carpal joint outwards, but as the opposite practice is followed by some authors it is always desirable to say which is being used (cf. Ashmole et alI961). In most non-passerine species there are-not counting a remicle, if present (see REMICLE)-10 primaries in normal individuals, but in grebes, except the flightless Rollandia micropterum, storks and flamingos, there are 11. In passerine birds, there are basically 10 primaries, but the 10th (outermost) is reduced to various extents in the different families, being vestigial in many and absent in the so-called nine-primaried Oscines (see PASSERIFORMES). (Stresemann 1963). See also MOULT; WING FORMULA. Ashmole, N.P., Dorward, D.F. & Stonehouse, B. 1961. Numbering of primaries. Ibis 103a: 297-298. Stresemann, E. 1963. Variations in the number of primaries. Condor 65: 449-459.

PRIMARY COVERTS: see TOPOGRAPHY. PRIMITIVE: retaining characters (known or, often, presumed) of an ancestral form. Alternatively, and in general preferably, the term may be applied to characters that are similar to those of an ancestral form.

PRINIA: generic name commonly used as English substantive name of Prinia spp., alternatively 'long-tail' (see WARBLER (1) (Grass warblers». PRION: substantive name of Pachyptila spp. (see PETREL). PRIONOPIDAE: a family of PASSERIFORMES suborder Oscines;

HELMET-SHRIKE.

PRIORITY, LAW OF: see NOMENCLATURE.

PROTEIN METABOLISM: see ENERGETICS; METABOLISM; NUTRI-

TION.

PROTOPTILE: term applied to the first of two nestling down plumages, in cases where there is such a sequence, the second then being called 'mesoptile' (see PLUMAGE). PROTOZOA: see ENDOPARASITE. PROVENTRICULUS: see ALIMENTARY SYSTEM; also, for stomach

oil, under PETREL.

PROXIMAL: nearest to the centre of the body or to the point of attachment (e.g. of a limb); opposite of DISTAL. PROXIMATE: applied to factors, in a system of causation, that immediately precede the effect; contrasted with ULTIMATE. PRUNELLIDAE: a family of the PASSERIFORMES, suborder Oscines;

ACCENTOR.

PSEUDAPOSEMATIC: see under APOSEMATIC. PSEUDEPISEMATIC: see under EPISEMATIC. PSEUDOCHELIDONINAE: see SWALLOW. PSEUDONESTOR: alternative substantive name for the Maui Parrotbill Pseudonestor xanthophrys, one of the HAWAIIAN HONEYCREEPERS. PSEUDOSCHIZORHINAL: see NARIS. PSEUDOSUCHIA: see under FOSSIL BIRDS. PSILOPAEDIC: with little or no down when hatched (see YOUNG

PROAPOSEMATIC: see under APOSEMATIC.

BIRD).

PROCELLARIIDAE: see below.

PSITTACIDAE: see PSITTACIFORMES; PARROT.

PROCELLARIIFORMES: an order, alternatively 'Tubinares', comprising 4 families: Diomedeidae (Albatross), Procellariidae (Shearwater),

(see PARROT).

PSITTACIFORMES: an order comprising only the family Psittacidae

Pterylosis

PSITTACOSIS: a virus disease, on occasion communicable to man, originally described as affecting parrots (Psittacidae) and allied birds but now known to affect widely different species (e.g. the Fulmar Fulmarus glacialis), as the result of infection by an identical or closely related virus, and therefore sometimes called 'ornithosis' (see DISEASE). PSITTIROSTRINAE: see PSITTRICHADINAE: see PSOPHIIDAE: see under

HAWAIIAN HONEYCREEPER. PARROT.

GRUIFORMES; TRUMPETER.

PTARMIGAN: substantive name of Lagopus spp. other than L. I. scoticus and sometimes L. lagopus; used without qualification in Britain for L. mutus, elsewhere known as the Rock Ptarmigan; in the plural (sometimes unchanged), serves as a general term for the genus (see GROUSE).

PTEROCLETES; PTEROCLIDIDAE: see below. PTEROCLIDIFORMES: an order, comprising the sole family Pteroclididae (see SANDGROUSE). In Wetmore's system treated as a suborder Pterocletes of the order Columbiformes, but other authors consider them more closely related to the Charadriiformes, particularly the COURSERS Glareolidae. PTERODACTYL: see

WINGS, COMPARATIVE ANATOMY OF.

PTERYGOID: a paired bone of the

SKULL

(see

PALATE).

PTERYLA: (plural pterylae): an area of skin bearing contour feathers; a tract of contour feathers arranged in rows (see PTERYLOSIS). PTERYLOGRAPHY: the study of feather tracts (see PTERYLOSIS). PTERYLOSIS: the arrangement of contour feathers into orderly groupings (pterylae or feather tracts) on the skin; pterylae may also contain filoplumes, down, and/or powderdown among the contour feathers. The intervening spaces (apteria) are completely devoid of contour feathers, but may contain semiplumes, down, powderdown, or no feathers at all. Except in a few species that have visible areas of bare skin (e.g. naked-headed vultures), the skin of birds appears to be fully and evenly covered by feathers. In reality, most birds have their feathers growing from relatively limited tracts. Land species usually have narrow pterylae, Pt. capitalis

'--

Pt. cruralis Pt. ventralis

Pt. caudalis Fig. 1. A generalized passerine, showing the 8 major pterylae (feather tracts). (Redrawn by J. William Hardy from Ames, Heimerdinger & Warter 1968).

487

on about half of the skin area; the remainder of the body has essentially bare skin, overlain by the feathers that fan out from adjoining pterylae and cover the apteria. Waterbirds tend to have wider pterylae, and narrow apteria filled with down. Only in adult ratites, penguins Spheniscidae, and screamers Anhimidae are the contour feathers distributed uniformly over the body, but still arranged in discernible patterns (rows) and with at least a few small apteria in such areas as the ventral midline, the axillary region, or the head and neck; well-developed embryos of these birds show clearly defined pterylae and apteria. Pterylosis, therefore, is a basic feature of all birds----and is as uniquely avian as feathers themselves. Use as a taxonomic character. The study of pterylosis (pterylography) has considerable potential for systematics studies. Although it is still in its infancy from the standpoint of the number of taxa studied, many different tract patterns are found to be indicative of relationships. The system seems to be evolutionarily conservative, and thus is most useful at the higher levels of classification (usually familial or above.) The only class-wide study of pterylography was made by its founder, C.L. Nitzsch (1867), in the early 19th century. His broad sampling of Aves, however, was just a beginning; since then morphologists have concentrated on describing the pterylae of additional species, studying them in finer detail, and applying their findings to systematics studies. The most significant differences of pterylae seem to lie in the number of feathers present and the internal patterns (arrangement of follicles into rows) in the major body tracts (spinal and ventral), and in the wings and tail. Nomenclature. Most birds are feathered by discrete, easily visible, groupings of contour feathers. Whether each discernible patch is called a 'tract', or whether several related components should be classified together as a 'tract', is arguable. Following Nitzsch's concept of a bird's body being covered by a few large tracts, the 8 major pterylae may be termed: 1. Pteryla capitalis: the capital tract, that covers all surfaces of the head, often in many discrete subunits. 2. Ptetyla spinalis: the spinal or dorsal tract, that extends, continuously or divided, narrow or broad, from the nape of the neck to the base of the tail and covers the dorsal neck, back, and rump. In passerines this tract typically is an uninterrupted band of feathering, narrow on the neck, broadly expanded over the back, and narrowing again on the rump. 3. Ptetyla ventralis: the usually complex ventral tract, that covers the under surface from the neck to the cloaca. In passerines this takes the form of a substantial band of feathering on each side of the body from the upper breast to the flanks, then branching to a thin band that extends down either side of the abdomen to end at the cloaca. A broad median apterium, the site of the brood patch in many species, is enclosed by the 2 forks of this tract. 4. Pteryla humeralis: the humeral, scapular, or scapulohumeral tract, that covers the base of the wings and shoulders; commonly it is a relatively simple rectangular patch of feathers. 5. Pteryla alaris: the wing feathers (remiges) and their associated coverts. 6. Pteryla femoralis: the femoral tract, that covers the base of the legs, also usually with a simple rectangular grouping. 7. Pteryla cruralis: the often sparse crural tract, that covers the legs. 8. Pteryla caudalis: the tail (rectrices) and its coverts, and adjacent feathering of the uropygial gland and cloaca. The tracts associated with appendages (humeral, alar, femoral, crural) are paired; the others are centred on the long axis of the body and have essentially perfect bilateral symmetry. In different species, genera, or families, the tracts may be well developed or merged, or subdivided to various degrees, leading to refinements of their terminologies. The apteria, being present only in the absence of, or between, pterylae, customarily are named by their location on the body or their relationship to adjacent pterylae. Function. The adaptive significance of having feathers grouped into pterylae, with apteria in between, has never been satisfactorily explained. The answer probably involves many factors: the reduction of total feather weight; the reduced physiological drain by growing fewer feathers; the increased mobility of the limbs by having apteria under moving joints; and better thermoregulation through controlled heat exchange from bare skin. (See also FEATHER; FEATHERS NUMBER OF; M.H.C. PLUMAGE.) Clench, M.H. 1970. Variability in body pterylosis, with special reference to the genus Passer. Auk 87: 650-691.

488

Ptilogonatidae

Lucas, A.M. & Stettenheim, P.R. 1972. Avian Anatomy-Integument. Agriculture Handbook 362, part 1. Washington, D.C. Morlion, M.L. & Vanparijs, P. 1979. The pterylosis of five European corvids. Gerfaut 69: 357-378. Nitzsch, C.L. 1867. Pterylography. London.

PTILOGONATIDAE: a family of PASSERIFORMES, suborder Oscines; SILKY-FLYCATCHER.

PTILOGONYS: generic name often used as substantive name of Ptilogonys spp. (see SILKY-FLYCATCHER). PTILONORHYNCHIDAE: a family of the Oscines (see

PASSERIFORMES,

suborder

BOWERBIRD).

PTILOPAEDIC: clad in down when hatched (see

YOUNG BIRD).

PTILOPODY: the condition of having feathers on the tarsus and toes. PTILOSIS: synonym of

PLUMAGE.

PUAIOHI: Phaeornis palmeri of the Hawaiian Islands (for subfamily see THRUSH).

PUBIS: a paired bone (plural 'pubes') of the pelvic girdle, partly fused with the other elements (see SKELETON, POST-CRANIAL). PUFF-BACK: substantive name of Dryoscopus spp. (see SHRIKE). There are also 'puff-back flycatchers' Batis spp. (for family see FLYCATCHER (1)).

PUFFBIRD: substantive name of some species of Bucconidae (Piciformes, suborder Galbulae); in the plural, general term for the family. This consists of 10 genera and 33 species of small or medium-sized arboreal birds (14-29 em long) confined to continental tropical America. Characteristics, distribution and behaviour. The puflbirds are closely related to the jacamars (Galbulidae). Their large heads, abundant, lax, often dull-coloured plumage, and short tails make them appear stout and 'puffy', whence their name. The bill, of short or medium length, often notably stout, is decurved or hooked at the tip. The feet are zygodactylous, with two toes directed backward. The family is best represented in the Amazon Valley and Colombia, and is largely confined to warm lowlands. Its ancestors appear to have been much more widely distributed, and may have been the dominant small perching birds during the Eocene in North America, where at least 5 genera of the fossil family Primobucconidae have been found in deposits of this age in Wyoming. One of the largest and most widespread extant members of the Bucconidae is the handsome, 25 em long White-necked Puflbird Notharchusmacrorhynchus, which ranges from southern Mexico to north-eastern Argentina. Both sexes are largely black on the dorsal surface. The forehead, nuchal collar, sides of the head, and under parts are white, with a broad black band across the breast. The thick, tapering bill is black. Slightly smaller is the White-whiskered Puflbird, or Softwing, Malacopula panamensis, which is found from southern Mexico to western Ecuador. The male is largely chestnut-brown and cinnamon, with the posterior under parts pale buff or whitish. Both above and below the female is more olive and greyish. Both sexes are liberally spotted and streaked with tawny and buff on the upper parts and streaked with brown and dusky on the breast and sides. Both sexes wear the long, slender, slightly curved, white malar tufts which are indicated by their name. Their large eyes are dull red. Both the White-necked Puflbird and the White-whiskered Puffbird are found singly or in pairs, or sometimes in family groups of 3 or 4, but never in flocks. They rest motionless for long periods on a more or less exposed lookout perch at no great height, apparently lethargic but actually keeping a sharp watch for suitable food. By means of a

surprisingly sudden dart, they snatch a caterpillar, winged insect, spider, or small lizard from a neighbouring bough, or sometimes they drop down to seize it amid low herbage. Then they carry it back to a perch and devour it at leisure. A very different type of pufIbird is the Swallow-wing Chelidoptera tenebrosa, widespread in tropical South America. This is a stout, largeheaded bird about 15 em in length. When folded, its long wings reach almost to the end of its short tail. Both sexes are largely blackish, with a

White-whiskered Pufibird Malacoptila panamensis. (C.B. T.K.).

patch of white on the lower back and rump. The abdomen is rufouschestnut, which pales to white on the under tail coverts. The voyager along the Amazon and its great tributaries often sees these graceful birds perching in pairs on the topmost naked twigs of tall riverside trees, whence they make long, spectacular darts to snatch insects (including many winged ants) from the air, much in the fashion of some of the bigger American flycatchers (Tyrannidae). Because of their very plain attire, the 4 species of the genus Monasa are called 'nunbirds'. The Black-fronted Nunbird M. nigrifrons of the Amazon valley is about 29 em long. In both sexes, the upper plumage, wings, and tail are dull black and the ventral surface is dark grey. The bill, which tapers from a broad base to a sharp point, is bright orange-whence the name 'pico de lacre' ('sealingwax bill') sometimes applied to birds of this genus. More gregarious than other puftbirds, nunbirds travel in small flocks, and at least one species breeds cooperatively. The 6 small species of the genus N onnula are known as 'nunlets'. Both sexes of the 14-cm-Iong Grey-cheeked Nunlet N. frontalis are plain brown above and ochraceous or tawny below. This species is found in the lowlands of Colombia and eastern Panama, and little is known of its habits. Voice. Puflbirds show the same contrasts in voice as in plumage. The loudest utterance of the White-whiskered Puflbird is a high, thin whistle or 'peep'. The Swallow-wing has a weak, appealing whistle. The sociable nunbirds have a surprising range of utterances from soft, musical murmurs to far-carrying shouts. From 3 to 10 White-fronted Nunbirds Monasa morphoeus, often perching in a rowan a high, horizontal branch or liana, join their almost soprano voices in a chorus that rings through the rain forest for 15-20 min. While calling, pufIbirds often twitch their tails from side to side. Breeding. The breeding habits of pufIbirds are poorly known, but two main types of nests have been discovered: cavities which they carve in the hard, black, arboreal nests of termites, and burrows in the ground. Less frequent sites include hollow trees, holes made by woodpeckers, burrows made by small mammals, and oven-shaped nests of clay built by the Pale-legged Hornero Furnariusleucopus. Both sexes of the Black-breasted Puflbird Notharchus pectoralis take turns at digging with their bills into the side of a large, roughly globular termitary. Their narrow, horizontal tunnel expands at its inner end into a neatly rounded chamber, on the hard floor of which the eggs rest. Burrows of the White-whiskered Puflbird have been found in the gently or at times steeply sloping, leaf-strewn ground in rain forest. From a round opening, the tunnel descends with a slight inclination for about 50 em. At the lower end it widens into a chamber, which is lined on the bottom and sides with brown dead leaves. Around the opening of the burrow, which is flush with the ground, the birds arrange twigs, petioles, and the like to form a low collar, through which they enter and leave, and which makes the aperture less conspicuous. This feature is far more strongly developed in the Black Nunbird Monasa atra of northern South America, which above the entrance to its descending burrow in level ground raises a large pile of coarse dead sticks; the birds reach their burrow through a rounded tunnel that runs along the surface of the

Pytilia

ground beneath the heap of sticks. Probably the chamber at the inner end is lined with dead leaves, like that of the White-fronted Nunbird, which, however, arranges only a low collar around the mouth of its 100-125 em long burrow. The Swallow-wing, however, places no sticks or other material around the entrance to its burrow, which may be in a bank or in level ground. Like the tunnels of other puflbirds, those of the Swallowwing are downwardly inclined and straight, but they are longer than those of other species, up to 200 em in length. The eggs rest on a slight lining of dry grass. Puflbirds lay 2 or 3, rarely 4, white, glossy eggs that resemble the eggs of woodpeckers. These are incubated by both parents, at least in the Black-breasted and the White-whiskered Puflbird. The latter incubates according to a simple but unusual schedule; the male sits continuously from early afternoon to the following dawn, then the female takes one long session of 5-8 h. The eggs are unattended for a half hour or more between these sessions. Black-breasted Pufibirds take shorter sessions, entering and leaving the nest a number of times in a day. The incubation period is unknown. Newly hatched puflbirds are blind and perfectly naked, without natal down. The prominent callous pads on their heels are smooth, as in jacamars and motmots. The male White-whiskered Puflbird does all the brooding and his duller mate nearly all the feeding, an arrangement that may have some slight protective value. When only a day or two old, the blind nestlings move up the tunnel to take food from their mother at the burrow's mouth. This consists of large, badly mangled insects, with an occasionalspider or small lizard, carried in the parent's bill, one item at a time. Waste is not removed from the burrow. After the father ceases to brood them by night, the nestlings, now with open eyes and becoming feathered, at nightfall somehow raise up the fragmented leaves from the bottom of the chamber to form a screen between themselves and the entrance tunnel. They leave the burrow at the age of 20-21 days, when they are well feathered and have 'whiskers' like their parents. Blind, naked nestlings of the White-fronted Nunbird toddle up to the mouth of their longer burrow to receive food from the 3 or 4 adults-parents plus helpers-who often attend them. After emerging at the age of about 30 days, juvenile nunbirds rise high into the trees. Soon they take their food in a spectacular manner, flying up from a distance to snatch it from an attendant's bill as they shoot past. This provides practice for nunbirds' habitual mode of foraging. A.F.S. Burton, P.J .K. 1976. Feeding behaviour of the Paradise jacamar and the Swallowwing. Living Bird 15: 223-238. Haverschmidt, F. 1950. Notes on the Swallow-wing, Chelidoptera tenebrosa, in Surinam. Condor 52: 74-77. Sclater, P.L. 1882. A Monograph of the Jacamars and Puff-birds, or the Families Galbulidae and Bucconidae. London. Skutch, A.F. 1948. Life history notes on puff-birds. Wilson Bull 60: 81-97. Skutch, A.F. 1958. Life history of the White-whiskered Soft-wing Malacoptila panamensis. Ibis 100: 209-231. Skutch, A.F. 1972. Studies of Tropical American Birds. White-fronted Nunbird. (Publ. Nuttall Ornith. Club no. 10) Cambridge, Mass.

489

PUFFIN: substantive name of Fratercula spp. (see AUK); used without qualification, in Britain, for the sole Atlantic species, F. arctica. See photo FLIGHT. PUFFINOSIS: name given to a disease of the Manx Shearwater Puffinus puffinus, probably allied to psittacosis and sometimes causing heavy mortality among the young birds (see PSITTACOSIS). PUFFLEG: substantive name of Eriocnemis spp. (for family see HUMMINGBIRD).

PUKEKO: native name for the Purple Gallinule Porphyrio melanotus of New Zealand, considered by some to be a race of P. porphyria (for family see RAIL). PULLET: an immature female domestic fowl (which may lay infertile eggs). PULLUS: a nestling or chick prior to fledging. Most frequently used of ringed birds and of museum specimens, as an age-class term. PULMONARY ARCH: see VASCULAR SYSTEM. PUPIL: the opening in the iris of the eye (see VISION). PURPLETUFT: substantive name of the 3 species of lodopleura, a genus of small, somewhat swallow-like COTINGAS, the males of which have an erectile patch of bright violet feathers on either flank. PYCNONOTIDAE: a family of the PASSERIFORMES, suborder Oscines; BULBUL.

PYGOPODES: formerly used as the name of an order which embraced the present Gaviiformes and Podicipediformes and originally also the Alcae. PYGOSTYLE: the fused caudal portion of the vertebral column (see SKELETON , POST-CRANIAL).

PYLORIC ORIFICE: the exit of the gizzard into the duodenum (see ALIMENTARY SYSTEM).

PYRRHULOXIA: Cardinalis sinuatus (formerly Pyrrhuloxia sinuatus) (see CARDINAL-GROSBEAK). PYRRHULOXIINAE: see CARDINAL-GROSBEAK. PYTILIA: substantive name of the 3 species of Pytilia, an African genus of waxbills (see ESTRIDID FINCH).

become even larger as the dry season progresses and food becomes increasingly patchily distributed. Irrigated crops ripening then are especially vulnerable. 3. To crops maturing in areas of early rainfall by Queleas on their 'early-rains' migration (see ITINERANT BREEDING). Early control methods in all these situations centred around a strategy of permanent reduction of the Quelea population to a level where they would no longer be of economic importance. However, despite increasingly desperate attempts to eradicate the birds, using flame-throwers to destroy their nests, explosives placed in the roosts, and finally by aerial spraying of roosts and colonies with highly toxic organophosphorus contact poisons like parathion (in a single year an estimated 183 million Queleas were destroyed in South Africa alone), no long-term reduction of the population occurred. The long-distance migrations regularly undertaken by Queleas simply meant that other individuals invaded every year from outside the controlled area. Destruction of birds on this scale does, however, result in a local population reduction, perhaps for long enough for a crop to be harvested without loss. Similarly, the destruction of nests removes the very real threat of damage to nearby fields by newly fledged young (though if the nesting bushes are simply chopped down the adults frequently continue feeding the young even at ground level). Such a strategy of 'immediate crop protection', which ignores birds not actually causing damage, is now carried out by aerial spraying from a helicopter or fixed-wing aircraft of fenthion, a more safely handled organophosphorus poison. The method is very hazardous, involving low-level flying often in the dark, may kill other species and poison livestock, and pollutes the environment (though fenthion degrades quickly). The chemical is applied at rates of 20251/ha- 1 of 20% active ingredient (4-5 kg/ha- 1) and often more. Lower dosages may inhibit the birds' feeding so that they die later of starvation but this is not attempted routinely. Spraying is expensive, requires highly-skilled personnel and cannot be used over water or near villages and is often not worthwhile on small numbers of birds. In such situations traditional methods of bird scaring are often resorted to, such as banging gongs and throwing sticks. However, the net effect of this is to scare the birds from field to field, spreading the damage more evenly over all the plots (though a farmer unable to employ as many scarers as his neighbour is penalized), rather than reduce the overall damage. The point is that damage often occurs when the Queleas have no readily available alternative food source and birds that would otherwise starve are nearly impossible to keep off the crops. Likewise distasteful chemical repellents applied directly to the crop (e.g. methiocarb) may be effective enough when the neighbouring farmer cannot afford to use them, for the birds simply descend on his crop instead. However, their widespread use forces the starving birds to eat the contaminated grain. For the same reason acoustic scarers may be ineffective and the growing of 'bird-proof' varieties of cereal, e.g., 'goose-necked' sorghum or long-awned wheat, may only reduce crop losses where Queleas have an alternative choice of food, or can move elsewhere. Dissuasive methods may only work where damage is caused by birds already on migration; certainly large-scale killing has no long-term benefit in such a situation for the dead birds are immediately replaced by new arrivals. The timing of Quelea migrations may be used to advantage in some regions, where the harvest may be gathered while the birds are elsewhere. In northern Botswana early crops (either early-planted or quick-maturing) may be harvested before Queleas returning on their 'breeding migration' produce young in local colonies. In Cameroun and Chad rice is grown in an area not normally inhabited by Queleas though they pass through on migration. There damage can be reduced if the vulnerable period of growth, when the grain is at the 'milky' or 'doughy' stage, can be timed to occur before the birds pass through on their southward 'early rains' migration. Normally, however, this dovetailing of the agricultural calendar with the Queleas' seasonal migration pattern cannot easily be done. In the near future Quelea control will continue to rely on large-scale destruction of birds, though it is to be hoped with a minimum of environmental pollution. See photo COLONIALITY. P. J.J.

QUADRAT: a square of ground of any size used for sampling (see CENSUS).

QUADRATE: a paired bone of the

SKULL.

QUADRATOJUGAL: a paired bone of the

SKULL.

QUAIL: substantive name of species in two distinct groups of Phasianidae, the American quails of the subfamily Odontophorinae and the Old World quails Coturnix spp. etc. (the so-called 'bush-quails' of India are in fact dwarf partridges)--see PHEASANT. The arrival of migratory parties, still a familiar event in Mediterranean countries, is described in the Book of Numbers, 11, 31: 'And there went forth a wind from the Lord, and brought quails from the sea, and let them fall by the camp, as it were a day's journey on this side, and as it were a day's journey on the other side, round about the camp, and as it were two cubits high upon the face of the earth.' QUAIL, BUSTARD- or BUTTON-: see BUTTONQUAIL. QUAIL-DOVE: substantive name of Geotrygon spp. (see

PIGEON).

QUAIL-FINCH: Ortygospiza atricollis (for family see

ESTRILDID

FINCH).

QUAIL- THRUSH: alternatively 'ground-thrush', substantive name of Cinclosoma spp. (see RAIL-BABBLER). QUELEA: substantive name of the 4 species of Quelea, a genus of African weaverbirds one of which, the Red-billed Quelea Q. quelea, periodically becomes a serious agricultural pest (see QUELEA CONTROL; WEAVER).

QUELEA CONTROL: action taken against the Red-billed Quelea

Quelea quelea (see WEAVER) to reduce the damage that this notorious pest

causes to small-grain cereal crops in Africa. The majority of small grain cereals in Africa, such as millet, sorghum and increasingly rice and wheat, are grown in the savanna regions. The savannas include extensive tracts of annual grasslands that produce vast quantities of seed, supporting very high densities of granivorous birds. Of these, Queleas are easily the most numerous, feeding in flocks numbering tens of thousands and whose roosts and breeding colonies frequently contain millions of individuals. Because of the similarity of their natural food of wild grass seeds to the grains of cultivated grasses grown by man, Queleas can cause extensive damage to cereal crops, though usually only when their preferred wild food is not readily available. Crop damage caused by this huge number of birds can be devastating, particularly to subsistence farmers who may regularly lose 30-50% of their crop and occasionally the whole crop. In many African countries either the national government or international agencies accept responsibility for trying to alleviate crop losses by maintaining Quelea control units. The effectiveness of the methods they use has been greatly improved by research into Quelea ecology and patterns of crop damage. Quelea damage occurs at 3 main periods of the year: 1. From the middle to end of the rains as rain-fed cereals are ripening. Damage is usually caused by hordes of young birds newly fledged from

local breeding colonies. Whereas adult Queleas may migrate elsewhere to rear another brood (see ITINERANT BREEDING) the young do not move far in the first few weeks of independence and often use the old colony as a roost so that any fields within foraging distance (10-15 km) will be subject to continuing depredations unless harvested. 2. In the dry season to irrigated crops. This time of year is one of increasing food shortage as the stock of dry grass seeds produced during the previous rains is gradually depleted. Quelea roosts and feeding flocks

Elliott, C.C.H. 1979. The harvest time method as a means of avoiding Quelea damage to irrigated rice in Chad/Cameroun. J. Appl. Ecol. 16: 23-35. Ward, P. 1979. Rational strategies for the control of queleas and other migrant bird pests in Africa. Phil. Trans. R. Soc. Lond. B287: 289-300.

490

Quintocubitalism

QUEO: Rhodinocichla rosea (for family see TANAGER). QUETZAL: Pharomachrus mocinno, often called Resplendent Quetzal and sometimes Resplendent Trogon (see TROGON); also the substantive name of other Pharomachrus spp.

491

QUILL: the calamus of a feather, or the calamus and rachis together; more loosely used for the feather itself, especially a remex or rectrix (see FEATHER).

QUINTOCUBITALISM: or 'eutaxis' (see

WING).

R

maximum range is proportional to the fourth power root of echoing area. As a consequence, radar can detect small targets, like birds, bats and insects, at surprisingly long distances--maximum range of a target 1/10,000 the echoing area of another, is VIO the maximum range of the larger target. Echo information from radars with horizontally rotating beams normally are displayed on a plan position indicator (PPI), and with vertically nodding beams on a range height indicator (RHI). Two principal types of radars have been used as tools in ornithology-fan-beam surveillance and pencil-beam search/tracking radars. The former is most suitable for obtaining a broad view of bird movements over large volumes of air space, while the latter provides height data, and, when operated in a tracking mode, gives detailed and continuous information for individual birds or bird flocks about flight speed, height and direction. Doppler radar has also been used for recording bird flight speeds. The radar echoing area of a bird depends on the ratio of the size of the bird to the radar wavelength. When this ratio is high, optical scattering from the bird of radio waves occurs, and the echoing area is effectively that of a sphere of water equal to the mass of the bird, or about half the silhouette area of an equally-sized metal sphere. This applies to most bird species when registered by X-band (wavelength 3 em) radars. For ratios smaller than one, Rayleigh-type scattering of the radar waves occurs, and the echoing area becomes disproportionately small. As a consequence, L-band (wavelength about 25 ern) radars are poor for detection of small birds. For bird sizes similar to the radar wavelength, echoing areas fluctuate, due to interference scattering, and may be as high as four times that of the water sphere or as small as one-quarter of the water sphere. These fluctuations occur when an S-band (wavelength 10em) radar is used to detect small and medium-sized birds. The echoing area of a bird is not constant but varies greatly with direction from which the bird is observed. Detailed analysis of modulations in the reflected radar signal, signature analysis, reveals the wing-beat pattern of flying birds, in terms of flapping frequency, duration of flapping and non-flapping periods. Characteristic echo signatures can be used for species identification. The first extensive radar studies of bird migration, in the years just before and after 1960, were carried out by Ernst Sutter in Switzerland, David Lack in Great Britain, and William H. Drury, J.A. Keith and Ian C.T. Nisbet in the United States. Lack mapped migration across the North Sea at all times of the year, and initiated analysis of many of the behavioural and ecological problems in bird migration pursued in later radar studies. Extensive radar investigations of bird migration have since been carried out in further areas in and around Great Britain, e.g., Shetland, the Hebrides and the English Channel, in many regions of the United States, Canada and the West Indies, in Scandinavia, and in Switzerland, where migration over both the lowlands and the Alps has been studied by surveillance as well as tracking radars. Marine radars

RACE: used synonymously with SUBSPECIES. The term 'race' is preferred by some, as indicating the geographical basis of subspecific differentiation and perhaps suggesting a more flexible concept. On the other hand, 'subspecies'· is the official term in the International Code of Zoological Nomenclature (1984)-see NOMENCLATURE. RACHIS: sometimes 'rhachis', the distal portion of the shaft of a feather, bearing the vane (see FEATHER). RACING PIGEON: see HOMING

PIGEON.

RACKET; RACQUET: a terminal broadening of the vane of a feather, characteristic of (especially) certain of the rectrices in some species; the subterminal portion of the rachis of such a feather may be devoid of barbs or carry a relatively narrow vane. RACKETTAIL: substantive name of Discosura longicauda and Ocreatus underwoodii (for family see HUMMINGBIRD); and of Tanysiptera spp. (see KINGFISHER). RAD AR: makes possible the detection and mapping of simultaneous bird movements over wide areas, and of bird movements that cannot be detected visually-at night, at high altitudes, within and above clouds. Since its start in the late 1950s, radar ornithology has developed into several different branches and has greatly expanded knowledge of the timing and course of bird MIGRATION. The principles of 'RADAR' (RAdio Detection And Ranging) involve transmission of pulses, usually 0.1-5 f.LS long, of radio waves, normally ~25 em wavelength, and reception of the reflected signal. Radio waves propagate with the speed of light, and the range to the target can be determined from the time taken for the echo to return. The azimuth and, for radars with a vertically narrow beam, elevation of the radar antenna give the direction to the target. The resolving power of the radar is dependent on pulse duration and beam width, while maximum detection range is determined by transmitting power, receiver sensitivity, gain of aerial and echoing area of the target. The inverse square spreading rule applies to both outgoing and reflected radio waves, with the result that

B

~n t::o&

Nova Scotia

ATLANTIC OCEAN

Puerto Rico

J.~.

Antigua

'\: --Barbados / 'oo~

Tobago

SOUTH AMERICA

(B) Long-distance autumn migration across the western North Atlantic Ocean (Williams & Williams, 1978, in ref. 4, below).

Fig. 1. Examples of migratory routes mapped in radar studies. (A) Spring migration of the Baltic Sea Eider Somateria mollissima population. (From Alerstam, Bauer & Roos 1974. Ibis 116).

492

Radar

493

A 2000

15 0 0

E (f)

tll

1000

1:

0>

'Qi J:

500 ground leve l

a

a

5

10

ATLANTIC OCEAN

15 20 Distance (km)

25

Fig. 2. Examples of radar tracksof migrating bird flocksor individuals. (A) Height versus horizontal flight distancein a flock of Cranes Grus grus on soaring migration in south Sweden. (From Pennycuick, Alerstam & Larrson 1979. Ornis Scand. 10). have been used for monitoring bird migration across the Mediterranean Sea and the western North Atlantic Ocean. So far radar has only been used in one tropical country (Ghana) and not yet in the Southern Hemisphere. Main ornithological research issues analysed in radar studies are the following: (1) Mapping of geographica l patterns of bird migration or bird roosting movements. High-power surveillance L-band radars permit effective mapping of routes of migrat ing birds up to 100-200 km from the radar station . Echo-type and speed can be used for distinguishing a few broad categories of birds. More detailed identification is not usually possible, except for a few distinctive behaviour patterns (e.g. , Starling Stumus vulgaris roosts, aerial roosting Swifts Apus apus) and diurnal bird movements if radar recording is combined with simultaneous field observations from a network of sites, or from an aircraft . Under such premises, radar studies may provide a detailed picture of the migratory pattern of a single species, as exemplified in Figure IA for the spring migration of the Baltic Sea Eider Somateria mollissima population. Widening the perspective from the short-distance Eider migration to routes about 10 times as long, Figure IB demonstrates a migratory pathway across the western North Atlantic Ocean, documented by observations from radars at places indicated in the figure, and from radars on board ships. This pathway is regularly used by passerines and shorebirds on autumn migration, flying non-stop for 60-100 hours over the open ocean, with median heights at Puerto Ricol Antigua often as high as 4,000-5 ,000m, top heights close to 7,000m. (2) Population monitoring. Combined radar and field observations, providing data on numbers of echoes from migrating bird flocks and mean flock sizes, respectively , can be used for estimating population sizes. By way of example, the Baltic Sea Eider population is estimated in this way at 750,000 birds, an estimate later confirmed by aircraft censuses of breeding birds in the countries concerned. (3) Migratory intensity in relation to weather . Radar has provided extensive evidence that following winds and absence of precipitation are key factors associated with dense broad-front migration. Radar investigations of points (1), (2) and (3) are often embodied in bird hazard to aircraft studies . (4) Flight strategies of birds. Detailed tracking radar data on , e.g., flight speed, altitude and wing-beat pattern are used for testing theories about mechanics and aerodynamics of bird flight, including gliding and soaring theory. Figure 2A shows, as an example, a minute-by-minute radar record of height versus distance along the migratory direction of a flock of Cranes Grus grus. The Cranes use soaring migration, gaining height by circling in thermals and gliding between thermals toward s their goal. Radar studies demonstrate that migrat ing birds select altitudes with favourable winds . The majority of migrants regularly fly below 1,000 m, while maximum heights have been noted from 6,000 to above 8,000 m . (5) Orientation of migrating birds. Radar observations show that in

30

35

40 '---' 5 km

(B) Flight paths of White-throated Sparrows Zonotnchia albicollis released alofton clear spring nights. (From Emlen & Demong 1978, in ref. 4, below).

Fig. 3. Waves and arcsof echo which are caused by departures of birdson migration from known roosts have been recorded, both by day and by night. Fig. 3 is a plan-position photograph takenat 06.39 on 5 March 1958, within one minute of sunrise. Arcs of echo are spreading from three separate pointson thedisplayat the same time. In eachcase the sector of arc recorded is that moving eastward from its source, a standard direction of migration at this season. The most clearly-defined arcs are those to the northeast of the radar. Twoare strongly evident, separated by a distance of 8 km, and a fainter third 6 km fartherahead. In all, 7 waves of echospread out from this point, the first leaving the roost at 06. 20, 20 minutes before sunrise, and the last at 06.46, 6 minutes after sunrise. (P hoto: W . G.

Harper)

some instances migrants compensate completely for wind drift over land and coastal areas, in other instances they are dr ifted to some degree by wind, and over the open sea they fail to compensate completely for wind drift. Explanations of these results are as yet only speculative. Experiments with small migrants, carried aloft in a box beneath a balloon, released and tracked by radar, demonstrate that the birds are welloriented in clear nights and when horizon glow from the setting sun is visible, but not so in overcast nights. Radar tracks of individual White-throated Sparrows Zonotrichia albicollis, experimentally released

494 Radiale

under clear spring nights, with the birds most often flying off in their normal migratory direction, are shown in Figure 2B. T.A. Eastwood, E. 1967. Radar Ornithology. London. Richardson, W.]. 1979. Radar techniques for wildlife studies. Nat. Wildl. Fed. Sci. Tech., Ser. 3: 171-179. Schaefer, G.W. 1968. Bird recognition by radar. A study in quantitative radar ornithology. In Murton, R.K. & Wright, E.N. (eds.). The Problems of Birds as Pests. London. Schmidt-Koenig, K. & Keeton, W.T. (eds.). 1978. Animal Migration, Navigation, and Homing. Berlin.

RADIALE: one of the proximal carpal bones (see

+1.5vdc

7turns

5-25pf

SKELETON, POST-

CRANIAL; WING).

RADIATION (1): in the evolutionary sense, divergence of forms of common ancestry, with increasing dissimilarity as a result of differences in adaptation-the antithesis of convergence (see ADAPTATION; CONVERGENCE; see also EVOLUTION; NATURAL SELECTION; SPECIATION).

XTAl

11----

RADIATION (2): in the distributional sense, geographical spread of a species or group of related species from the area in which the particular species or the ancestral species of the group (e.g. family) was originally evolved as a separate entity (see DISTRIBUTION, GEOGRAPHICAL; RANGE CHANGES; see also SPECIATION). RADIATION (3): in the physical sense, with only incidental application in ornithology, emission of ionizing rays-to which birds or other organisms may become exposed. RADIO TELEMETRY: see RADIO TRACKING AND BIOTELEMETRY. RADIO TRACKING AND BIOTELEMETRY: the remote monitoring of an animal's location by wireless is called radio tracking and remote monitoring of its physiology (e.g. heart rate) is termed biotelemetry. Radio telemetry involves a battery powered transmitter which emits low-powered signals via a transmitting antenna. These signals are received by another, directionally sensitive antenna which connects to a receiver. Ideally, the directional properties of the receiving antenna allow bearings to be taken on the animal's position from two places and the point at which these bearings intersect marks the animal's location. Biotelemetry and radio tracking should not be undertaken lightly; they are expensive, time-consuming and often, frustrating; but can lead to answers to biological questions which are otherwise unobtainable (e.g., location of sleep sites used by elusive nocturnal birds). Described here are practical aspects of selecting, building and using telemetry equipment. The history of radio telemetry effectively began in the early 1960s. Early circuits were simple, robust, adaptable to both loop and whip antennae and could be packaged to fit most birds and mammals. A similar circuit (Fig. 1) was developed to capitalize on the more useful features of these circuits. Using this transmitter design, the writer has successfully tracked many species of birds. If a resistive device is incorporated in the circuit at R T (150-400 K) physiological and environmental parameters can be measured by pulse interval modulation. For instance, a 200-K thermistor (at 25°C) may be substituted to measure linear temperatures between 31° and 45°C, accurate to O.l°C. This temperature transmitter has been used to measure 24 h egg and body temperatures of incubating gulls (Larus argentatus and L. fuscus). Other environmental parameters such as light level (R T = photoresistor), presence of moisture, and pressure (if a strain gauge is substituted for R T ) can also be measured. If the circuit of Fig. 1 is built with subminiature components, it weighs as little as 1.0 g and operates for 7-10 days using a 0.3 g mercury hearing aid battery. This transmitter has been field-tested on birds as small as Great Tits Parus major weighing approximately 20 g and effective tracking ranges are up to 100m in thick forest and 500 m line of sight. Powerful multistage transmitters are required for long-range tracking (3-10km). By pulsing the transmitter 2 or 3 times every few seconds, individual animals can be recognized, much as the alphabet and numbers are recognized through Morse Code transmission. Pulse interval modulation allows activity and mortality sensing. An easily built two-stage activity-sensitive radio-tracking transmitter is shown in Fig. 2. The values given result in a pulse rate of 60 min"! when

2000pf

Fig. 1. A miniature, crystal controlled transmitter.

the mercury switch is shorted. Opening the contacts of the mercury switch results in a doubling of the rate. Changes in pulse rate caused by opening and closing the switch allow movement to be detected. The sensitivity of the device to particular movements usually depends on where the transmitter is fitted to the animal and hence how it moves relative to the plane of animal movement. Unambiguous distinction can be made between inactive resting, sporadic and continuous activity. Batteries. A compromise between battery weight, increased transmitter life and range limits the use of many transmitters. Battery failures either through self-deterioration or penetration by moisture have been the commonest causes of transmitter failure (followed by poor-quality transmitter crystals). Recently, advances have been made using solar cells, where benefits were obviously only to studies of diurnal birds unless rechargeable batteries were incorporated into the solar transmitter. Encapsulation and attachment. Transmitter components should be encapsulated in light-weight, durable and waterproof materials. Components should be coated in beeswax which increases waterproofing and facilitates the removal and replacement of batteries. As a general rule, the total package (transmitter, battery, antenna, harness and encapsulation), should weigh less than 3-5% of the animal's body weight. Radio harnesses for birds include chest packs attached by a loop antenna that circles the bird's body, backpacks attached by harness loops under the wings with a whip antenna trailing down the bird's back and tail-mounted either on imped or natural feathers (see Amlaner and Macdonald 1980, for review). Swanson and Keuchle (1976) mounted a transmitter above a duck's bill using a nasal pin. Their transmitter included a switch so positioned that it changed the pulse rate depending on whether the duck's head was up, or down as when feeding. Welfare. It is imperative for both humanitarian and scientific reasons that the transmitter does not hamper or damage the animal in any way. Boag (1972) found that Red Grouse Lagopus lagopus scoticus wearing transmitters fed less than those without. Sargeant, Swanson and Doty (1973) suggested that fitting a radio pack to a Blue-winged Teal Anas discors contributed to its being preyed on by Mink Mustela vison (see Siegfried et alI977). Comparisons can be made between observations on the same animal before and after radio tagging, but some effects may be very subtle, e.g., on long-term reproductive potential. Kenward (1977) found no difference in weight loss or dispersion tendency of Goshawks Accipiter gentilis wearing transmitters from those wearing leg rings and noted that the hourly rate of bringing prey to the nest was the same for a Sparrowhawk Accipiter nisus before and after being fitted with a transmitter. Amlaner, Sibly and McCleery (1970) conducted a detailed study of the survival and hatching success of Herring Gulls carrying

Rail

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RADIUS: a bone of the forelimb (see SKELETON, POST-CRANIAL; also a barbule in the vane of a feather (see FEATHER).

495

WING);

RAFT: a closely-packed flock of birds on water.

I

I

RAIL: substantive name of many species of Rallidae (Gruiformes, suborder Grues); in the plural, general term for the "family. The rails constitute a homogeneous and cosmopolitan family. Characteristics. Rails are small- to medium-sized birds (20--65 em + long) with the body laterally compressed, with moderate to long legs and toes, short rounded wings of 10 or 11, rarely 8 or 9 primaries, and a short and soft tail usually of 12 rectrices (rarely as few as 6 feathers, sometimes Mercury almost non-existent). The bill varies from long and curved to short and Reed 2000pf conical. The plumage is of loose texture and the flight feathers are switch moulted simultaneously. The sexes often differ in size, the males being larger, but rarely differ in coloration. The plumage varies from nearly black or greenish-blue (but even deep purple) to olive-brown, buffish, or chestnut, sometimes with dark streaks and with white bars or spots. Habitat. Although some forms prefer dry plains, Rails are mainly Fig. 2. A two stage transmitter for use in long range radio tracking studies. It includes a mercury switch whose movement enables the animal's activity ground-dwelling water and swamp birds (see SWIMMING AND DIVING), to be monitored through changes in 'bleep' rate. well adapted to living in dense vegetation. Distribution. Rails are found in all continents north to the Arctic dummy transmitters weighing between 10--50 g and found that wearing Circle and south to the islands of the sub-Antarctic Convergence. Some heavier transmitters decreased survival of the offspring. 129 species are or were known, contained in 18 genera. Five genera are Basic radio tracking. Tester (1971) suggested three categories of error monotypic. The typical genus includes the Water Rail Rallus aquaticus, all of which could act together to frustrate the tracker's ability accurately the only member of this genus with a Palearctic distribution; it is to locate his quarry: error inherent in the receiving equipment and its distinguished by a long red bill. It occurs from Great Britain and Iceland, operation, error resulting from the animal moving while bearings are discontinuously, to eastern Asia; migrants often fall victims to striking being taken, errors resulting from anomalies such as reflection and against lighthouses and powerlines. North American representatives are refraction of the signal creating false bearings. the larger Clapper Rail R. longirostris and King Rail R. elegans, inhabiting Although not commonly stressed in the literature, the radio tracker's salt and freshwater marshes. The smaller and warmly brown-tinged subjective 'feel' for the radio landscape of his study area is widely Virginia Rail R.limicola is found in marshes of the Western Hemisphere. acknowledged as an important facet of accurate radio tracking. The Widely spread over the southern part of Africa is the Cape Rail R. following suggestions help to minimize the risks of both movement and caerulescens, very similar to the Water Rail but with uniform dark brown topographical error. Take consecutive bearings with as little delay as upper parts. In south-eastern Asia, from southern China and India to the possible. For direction finding it is easier to detect the difference between Philippines and Sulawesi, the Blue-breasted Banded Rail R. striatus is signal and silence (i.e., null) than between signal and louder signal. found; in India this species, with its rufous crown and hind neck and its Know the individual features of the landscape well, and how they affect dark brown upperparts barred with white, is one of the most familiar radio signals. If errors are suspected, take several alternative bearings; at water birds. Rather similar, but smaller and with the back black-streaked least three are necessary to detect movement errors. When radio tracking olive-brown, is the Slate-breasted or Lewin's Water Rail R. pectoralis, from a car it is helpful to continue listening to the signal while travelling occurring in Australia, Flores, and the mountains of New Guinea. In the between reception sites so that fluctuations in signal strength along the same area and distributed also over the lesser Sunda Islands, Sulawesi, route can be noted in the context of the landscape. Bearings and the and the Philippines, is the beautiful Banded Rail R. philippensis, derived radio locations should be ranked in terms of their accuracy, characterized by a rufous pectoral band and a grey eye-stripe. More depending on both the width of the null points and the variation of restricted in distribution is the Barred Rail R. torquatus, inhabiting the successive bearings that do not intersect at the same spot. Philippines, Sulawesi, and New Guinea. The head is blackish with a Conclusion. Radio tracking is an invaluable addition to the biologist's broad white line under the eye. Of the 13 other species included in this skills and fieldcraft, and has contributed to diverse studies (reviewed by genus, there are 3 in South America and 1 in Madagascar, while the other Macdonald 1978). Just as this technique has revolutionized studies of 6 are or were inhabitants of small islands; of these last, one species still elusive species during the past decade or so, now people look to the survives on Guam, but the others, known from Tahiti, Wake Island, and possibility of transmitting and receiving additional information, through the Chatham Islands, are extinct. biotelemetry, as the next methodological advance (Amlaner 1978; Of the 2 known species of island woodrails the one formerly occurring on New Caledonia, Rallus lafresnayanus, is extremely rare, but a tiny Amlaner and Macdonald 1980). C.J .A. population (18 birds in 1972) of the other, R. sylvestris, is still found on Amlaner, C.J., Jr. 1978. Biotelemetry from free ranging animals. In Stonehouse, B. Lord Howe Island; these forms are more forest than swamp birds. (ed.). Animal Marking: Recognition Marking of Animals in Research. London. Another peculiar form is the still common Inaccessible Island Rail Amlaner, C.J., Jr. & Macdonald, D.W. (eds.). 1980. A Handbook on Biotelemetry Atlantisia rogersi, a very small, flightless, dark rail with degenerate and Radio Tracking. Oxford. Amlaner, C.J., Ir., Sibly, R. & McCleery, R. 1978. Effects of transmitter weight hairlike plumage; it lives in the tussock grass which covers the island. on breeding success in herring gulls. Biot. Pat. Montn. 5: 15~163. Representatives of the banded crakes Rallina spp. are distributed from Boag, D.A. 1972. Effect of radio-packages on behaviour of captive red grouse. J. India to northern Australia. All have warm rufous heads and breasts, the Wildl. Mngmt. 36: 511-518. abdomen more or less clearly banded black and white; they are shy and Kenward, R.E. 1977. Predation on released pheasants (Phasianus colchicus) by retiring birds, living in marshes or along streams in dense undergrowth. goshawks (Accipiter gentilis) in central Sweden. Viltrevy 10: 79-112. Of the woodrails Aramides spp. of Middle and South America, eastern Macdonald, D.W. 1978. Radio tracking: some applications and limitations. In Indonesia and northern Australia 11 subspecies are known. They are Stonehouse, B. (ed.). Animal Marking: Recognition Marking of Animals in large rails with stout bills, generally olive-brown upperparts, grey breast, Research. London. Sargeant, A.B., Swanson, G.A. & Doty, H.A. 1973. Selective predation by mink, and black hind parts;' when flushed they take wing reluctantly. The Mustela vison, on waterfowl. Am. MidI. Nat. 89: 208-214. wekas Gallirallus are restricted to New Zealand. They occur from sea Siegfried, W.R., Frost, P.G.H., Ball, I.J. & McKinney, D.F. 1977. Effects of level to well up in the mountains in different habitats. They are brownish radio-packages on African black ducks. S. Afr. J. Wildl. Res. 7: 37-40. in colour and the wings are rudimentary. Not unlike in general appearSwanson, G.A. & Keuchle, V.B. 1976. A telemetry technique for monitoring water ance, but with a more conical bill and red legs, is the Nkulengu Rail fowl activity. J. Wildl. Mngmt. 40: 187-189. Himantornis haematopus, living in the forests of West and Central Africa. Tester, J.R. 1971. Interpretation of ecological and behavioral data on wild animals Here also occurs the Grey-throated Rail Canirallus oculeus, with chestnut obtained by telemetry with special reference to errors and uncertainties. Int. neck and breast, olive upper parts and white spots on the almost black Proc. Symp. Biotelemetry S. 57 CSER, Pretoria: 385-408.

[:

496 Rail

Sora Rail Porzana carolina. (C.J.F.C.).

wing feathers. The Corncrake or Landrail Crex crex is distributed over most of Europe and well into central Asia; its favourite habitat is grassland. In winter it migrates into Africa and may erupt occasionally into other southern latitudes. One of the larger genera is Porzana, with a world-wide distribution and comprising some 21 species, one extinct (palmeri). Of these the Spotted Crake P. porzana, the Little Crake P. parua, and Baillon's Crake P. pusilla, are European birds which also range over part of middle Asia. Baillon's Crake has a peculiar discontinuous distribution, being also known from the southern part of Africa and from Australia and New Zealand. A widespread North American species is the Sora P. carolina, in winter reaching northern South America and accidentally occurring in Great Britain. Ranging from the Philippines to Australia, New Zealand, and many Pacific islands is the Spotless Crake P. tabuensis, a dark leaden-grey species with dark brown upper parts. Other species occur in South and Central America (3), in eastern and south-eastern Asia (3), in Australia and Oceania (2), and in Madagascar (1). In some species there is a slight difference in plumage between the sexes. In Africa the Black Rail Porzana flavirostra, with a yellow bill, is one of the commonest species. Restricted to America are 11 species of Laterallus; of these the only one known in North America is the American Black Rail L. jamaicensis, a small bird with white spots and streaks on the upper parts, frequenting grassy inland swamps and brackish coastal marshes. Diminutive in size are the pygmy rails Cotumicops spp. (here taken to include Sarothura); the 13 species occur from Africa to the Western Hemisphere and Japan. They show a well-marked sexual dimorphism, and are exceedingly secretive in habits. Six species of Amauromis are distributed from India to the Solomon Islands; except for the White-breasted Waterhen A. phoenicurus, they are dull grey and olive-brown. The large Watercock Gallicrex cinerea has a reddish frontal shield projecting backwards in a horn; it is found over a wide area from southern to eastern Asia, and migrants reach the Greater Sunda Islands. The Moorhen or Waterhen or in America Common Gallinule Gallinula chloropus is distributed over much of the world, being found in all continents except Australia and having colonized many oceanic islands. In Australia, New Guinea, and eastern Indonesia it is replaced by the closely related Dusky Moorhen G. tenebrosa. In Africa occurs the small Lesser Moorhen G. angulata. The moorhen of Tristan da Cunha, Gallinula ('Porphyriomis') nesiotis nesiotis, was hardly able to fly and is now extinct; but another subspecies, G. n. comeri, is still not uncommon on Gough Island. The widespread (American) Purple Gallinule Porphyrula martinica has relatives in Africa and South America; alieni and flavirostris. A large species is the (Old World) Purple Gallinule or Swamphen Porphyria porphyrio, with a discontinuous distribution from southern Europe through southern Asia to Australia, New Zealand, and islands in the Pacific, and also occurring in Africa and Madagascar. It is azure or greenish-blue below, brown or almost black above, and has a stout and conical bill; all populations are now generally considered as belonging to 3 species, including the flightless Takahe Porphyrio ('Notornis') mantelli from New Zealand, thought to have become extinct but rediscovered in recent years in some inaccessible valleys in the mountains on South

Island. The Coot Fulica atra has lobed toes and a white frontal shield and is found over the greater part of Europe, Asia, and Australia, as is the American representative F. americana over the greater part of the Americas. Of the remaining 7 species, one is African and all others are Central and South American in distribution. Of these the Giant Coot F. gigantea and the Horned Coot F. comuta breed in the high mountain lakes of the Andes; the latter species has the remarkable habit of using stones for building its nest. Food. The diet is varied-mainly animal, but some species prefer vegetable food. The robbing of eggs and young of other birds is known. Behaviour. Rails walk with bobbing heads and flirting tails possibly correlated with acuity of vision, as in other walking birds such as pigeons. Some of them are good flyers, covering long distances during migration; but in others, living on oceanic islands, the power of flight has been reduced, and in these cases the introduction of rats or other predators can at once endanger the existence of the species. The majority of the species have secretive habits and many are nocturnal, so that our knowledge of the life of many forms is still scanty. Voice. At dusk and during the night rails may make themselves conspicuous by their specific loud calls and harsh repetitive squeals or monotonous notes like knocking pebbles together. Breeding. Nests are well concealed; the clutch-size ranges from 1-14 eggs, sometimes due to more than one female laying in situ. The ground colour varies from near white to ochreous or brownish buff, often with reddish, greyish-brown, or black specks, spots, or blotches. The eggs may be incubated by both sexes for from 2 1/ 2 to nearly 4 weeks. The nestlings are covered with black or dark brown down; they leave the nest soon after hatching and are cared for by both parents, sometimes also by young of an earlier brood. They become independent in up to 8 weeks. See photo INCUBATION. S.D.R. Fitter, R. 1973. Takahe Rescue Plan. Oryx 12: 180-181. Olson, S.L. 1973. A Classification of the Rallidae. Wilson Bull. 85: 381-416. Ripley, S.D. 1977. Rails of the World. A Monograph of the Family Rallidae. Boston. Steinbacher, G. 1939. Zur Brutbiologie des grunfussigen Teichhuhns (Gallinula chloropus L.). J. Orn. 87: 115-135.

RAIL-BABBLER: substantive name of some species of the subfamily

Orthonychinae (Cinclosomatinae) of the family Timaliidae (Passeriformes, suborder Oscines); in the plural, general term for the subfamily. Within it are placed provisionally a small number of insectivorous species which all occur, except one, in the Australian-Papuan region and are all essentially terrestrial in their habits. They have thickset bodies and short bills, generally with small heads and thin necks. Their legs are fairly long, their tails broad and their plumage soft and fluffy. There are many uncertainties about their taxonomic relationship; they do not seem to be closely related to one another, and they may even belong to entirely different groups. These uncertainties are reflected in current Australian field-guides. Thus the logrunners or chowchillas (Orthonyx, 2 species), the quail-thrushes (Cinclosoma, 5 species) and the whipbirds and wedgebills (Psophodes, 4 species, although wedgebills were formerly in Sphenostoma) are either placed in a family of their own (Orthonychidae) or else, as here, absorbed into the babblers (Timaliidae); so are the scrub-robins (Drymodes, 2 species) which in the field-guides are placed in the thrushes (Turdidae). Also in this grouping are here included the genera E upetes (4 species), Melampitta (2 species) and the monotypic genera Androphobus and Ifrita. The provisional nature of the classification adopted here for these groups must be stressed. Recent evidence from DNA hybridization indicates that these and other Australian passerine birds of uncertain affinities are all the result of evolutionary radiation of ancestral Australian endemic stocks, and that the resemblance of some of them to babblers, thrushes and other passerine groups is attributable to convergence (Sibley and Ahlquist 1982). Characteristics. The logrunners have robust legs and feet and a specialized tail in which the shafts of the feathers are modified at the tip into stiff spines, used to help prop up the birds while they feed. The sexes in both species may be distinguished through the colour of the throat, white in the male and chestnut in the female. The Northern Logrunner Orthonyx spaldingi (length c. 25 em) is much larger and is more cleanly marked black and white than the Southern Logrunner O. temminckii

Ramphastidae

(length c. 18em) which is mottled br~wn ~bo~e. The 2 Melampiua species are black all over and also differ m SIZe (~8 em and. 29 em respectively). They are active birds which cock their short ~ails and nervously flutter their wings as they move through the vegeta~on. T?e whipbirds and wedgebills (length 2~27 em) are noted for their erectile crests. They are, in general, dull drab birds in which the sexes are the same, although the whipbirds do have a prominent white patch or streak on the throat. The quail-thrushes (length 2~30 em) are distinctively and boldly marked, particularly the males which are larger than the females. Males have two patterns of black and white on the underparts and these are used to determine the limits of the various species. The colour of the upperparts is variable in species living in dry habitats and matches the colours of the local soils. The white tips of the dark tail feathers are conspicuous in flight, which occurs in short bursts, is low and fast, and terminates with the bird running at the flying speed. The young of all species are spotted. The sexes are alike in the scrub-robins (length 19--20 em). One notable distinction between the 2 species is the colour of the mantle; this is grey in the Southern Scrub-robin Drymodes brunneopygia and reddish-brown in the. Northern Scrub-robin D. superciliaris. They habitually cock their tails at about 45°, and raise and lower them, and flick their wings nervously whilst moving through the undergrowth. In marked contrast to the rest of the group, the Eupetes species (length 20-30 em) are brightly coloured blue, chestnut, or reddish, have rather long necks and their young are unspotted. The Green-backed Babbler Androphobus viridis is unique in having a dark olive-green mantle and so is the Blue-capped Babbler Ifrita kO'Waldi in having a shiny blue crown with a black patch in the centre. Habitats, distribution and movements. The logrunners are mainly confined to rain-forests along the eastern coastal belt of Australia, but the Southern Logrunner surprisingly turns up again in New Guinea. The 4 species of Australian quail-thrushes are found on stony ground, particularly on ridges where there is plenty of cover, and live in open forests. The Ajax Quail-Thrush Cinclosoma ajax is found throughout the lowlands of south-east and south New Guinea but only locally in the west. Whipbirds and wedgebills are confined to Australia. Three are dry country species whilst the Eastern Whip bird Psophodes olivaceus is found in dense thicket in or near the wet forests along the east coast. The 2 scrub-robins also occupy quite different habitats, the Northern Scrubrobin in forests in New Guinea and north-eastern Australia and the Southern Scrub-robin in dry country outside the forests in a number of localities in southern Australia. All the Eupetes species are forest birds; 3 are found in New Guinea and the other, the Malaysian Rail-babbler E. macrocercus, occurs on the Malaysian Peninsula, Sumatra, Borneo and the Natuna islands. The remaining genera, Melampiua, Ifrua and Androphobus are found in mountain forests in New Guinea, the majority are rare and Androphobus is only found on the Snow and Weyland Mountains. Food. Insects of one kind or other are the main diet of the majority of the rail-babblers but fruit has been found in the stomachs of some Melampitta and Eupetes species. The logrunners clear leaves from the soil by rapid scratching, throwing debris aside, and use both feet to excavate for food. The distinctive bare patches that remain on the forest floor give the birds' presence away. The Blue-capped Babbler is unique in the group, feeding at all levels of the forest, often reaching the tree-tops as it searches the moss-covered trees in a treecreeper-like manner. Behaviour. Little or no information is available for the majority in this grouping. The logrunners, whipbirds and wedgebills and quail-thrushes move in pairs or small parties, but are sometimes solitary. The quailthrushes are particularly shy and secretive, and freeze when disturbed or burst up from cover like quails. Voice. Quail-thrushes and logrunners announce their presence by their loud, penetrating contact calls, especially at dawn and dusk. The quail-thrushes also have territorial songs and use song posts that may be as high as 6'm. The Northern Logrunner is an accomplished mimic and is said to drown the song of other birds with its oft-repeated choui chouxhilla, The remarkable whipcrack call of the Eastern Whipbird is an antiphonal duet. The other whipbird and 2 wedgebills also duet but not the Chiming Wedgebill Psophodes occidentalis. The song patterns of scrub-robins have similarities to those of the quail-thrushes. Breeding. Most members of the group nest near or on the ground. Logrunners build globular nests made from sticks, ferns, fibrous leaves,

497

mosses, etc., and these may be placed on a bank, against a stone .or log. Whip birds and wedgebills use similar materials but the nes! IS cupshaped and placed 1-2 m high in bracken, sh!ub. or sapling .. T~e quail-thrushes and some, possibly all, Eupetes species line a depreSSIon In the ground with grass, leaves and rootlets, often sheltered. by an overhanging rock. In contrast, the Green-backed Babbler places ItS nest as high as 4 m above the ground. .. . Known clutch-sizes are 2-3 (whipbirds and quail-thrushes), 1-2 (Eupetes and logrunners) and one egg (Blue-capped Babbler). Th~ eggs vary from white to pinkish buff, blue-white or blue-g.reen and ar~, In the majority of species, marked with brown, black, reddish or purplish-grey spots or blotches. Pure white eggs are laid by logrunners and the Blue-capped Babbler. Incubation and fledging periods appear to be unknown. H.J.de S.D. and L.G.G. Frith, C.B. 1971. Some undescribed nests and eggs of New Guinea Birds. Bull. Br. Orn. Club 91: 46-49. Sibley, C.G. & Ahlquist, J .E. 1982. The relationships of ~e. Au.stralo--Papuan scrub-robins Drymodes as indicated by DNA-DNA hybridization. Emu 82: 101-105. Sibley, C.G. & Ahlquist, J.E. In press. The phylogeny and classification of the passerine birds, based on comparisons of the genetic material, DNA. Proc. XVIII Int. Orn. Congr.

RAIL, BENSCH'S: misnomer for the Monias Monias benschi (see MESITE).

RAIN BATHING: see COMFORT

BEHAVIOUR.

RAIN-BIRD: name variously applied in different parts of the world (usually because the birds, when particularly noisy, are supposed to predict rain), e.g., to the Green Woodpecker Picus viridis in Britain (see WOODPECKER), the Grey Currawong Strepera versicolor in Australia (see CURRAWONG), the White-browed Coucal Centropus superciliosus in parts of Africa and other members of the Cuculidae in the New World and Australia (see CUCKOO), and Peale's Petrel Pterodroma inexpectata in New Zealand (see PETREL); also 'rain-goose' to the Red-throated Diver Gavia stellata in Orkney (see DIVER), and 'rain-quail' (because abundant in some parts in the rainy season) to Coturnix coromandelica in India (see under PHEASANT).

RAINBOW-BIRD: Australian name, alternatively Rainbow Bee-eater, of Merops omatus (see BEE-EATER). RAIN-FOREST: a tropical environment characteristic of areas where there are both high temperatures and heavy rainfall, the latter spread throughout the year; seasonal heavy rains (monsoon) produce a different result. In most parts of the world the true rain-forest has little undergrowth and consists mainly of trees rising unbranched for 30-50 m and then spreading to form part of a 'canopy' that is continuous for great distances, broken only---except temporarily for accidental reasons-by vertical rock faces and the courses of large streams. The avifauna is richer in species than that of any other habitat. During the second half of the 20th century the rain-forests of the world began to suffer massive destruction with the prospect that only vestiges would be left by the end of the century. Campaigns to 'save the rain-forest' have figured largely in the programmes of the World Wildlife Fund and other conservation organizations. RAIN-POSTURE: special anti-rain attitude adopted by birds of many families (both passerine and non-passerine), especially those frequenting open habitats and tropical areas subject to seasonal downpours, typically while perching with little or no shelter in heavy rain; the near-vertical stance with head retracted and feathers tightly sleeked against the contours of the body helps to drain the water off and minimize its wetting effects. RALLIDAE: see under

GRUIFORMES; RAIL.

RAMI, MANDIBULAR: (plural of 'ramus'), the two halves of the lower mandible, separated by soft tissue near the base but uniting distally in the gonys (see BILL).

RAMPHASTIDAE: see under

PICIFORMES; TOUCAN.

498 Ramus

RAMUS: a barb of a feather (see FEATHER); also in the sense shown

under

RAMI, MANDIBULAR.

RANGE CHANGES: the enlargement or contraction of, in particular,

the breeding area of a species. It is clear from the fossil record that fundamental changes in bird distribution patterns have followed major planetary climatic cycles: hence in the warm Tertiary Period (20-40 million years ago) such tropical families as the turacos (Musophagidae), barbets (Capitonidae) and trogons (Trogonidae) extended into what is now Europe; while at the other extreme large parts of Eurasia must have had very impoverished avifaunas at the height of each Pleistocene glaciation. Recent changes have been less profound, but a good many have been detected in the short period (about 300 years) that ornithologists have been documenting bird distributions (see DISTRIBUTION, GEOGRAPHICAL).

Range expansions. The common occurrence of range expansion (geographical radiation) in the past can be inferred from the present extensive distributions of many species, on the presumption that each of these has spread from a more limited area in which speciation took place; the point has all the more validity when a species has begun to fragment into morphologically distinguishable populations (becoming SUBSPECIES), showing that some factor or factors have interrupted the even gene flow that kept the original population homogeneous. Past geographical radiation has led to such anomalies as the Old World larks (Alaudidae) having a Nearctic representative (Eremophila alpestris), and the New World family of wrens (Troglodytidae) sharing one species (T. troglodytes) with Eurasia. Such theoretical considerations apart, range expansion has visibly occurred, in various species and to a substantial extent, within the period of detailed ornithological recording. Within the historical period gradual range expansions have been more common than abrupt ones, even after excluding cases where expansion has been a consequence of recovery from an earlier catastrophic decline. Doubtless a variety of reasons have caused this gradual spread. Thus the northward expansions shown by a variety of temperate zone species in northern Europe (including Iceland) in the 1920s and 1930swere clearly correlated with simultaneous climatic amelioration, and few of these gains were lost when this phase ended in the 1940s/1950s (with a subsequent lowering of mean spring temperatures in northern Europe). Since 1950there has been an increased tendency for boreal species to nest further south in Scandinavia and especially in Scotland. Two (perhaps interacting) mechanisms have been suggested: the evolution of blocking anticyclones over Scandinavia in spring which induce some migrants to settle and breed further south than normal, and the adoption of new breeding areas following the acquisition of wintering grounds closer to the area to be colonized (exemplified in Scotland by Shore Lark Eremophila alpestris and Lapland Bunting Calcarius lapponicus). The range expansion of a species over a continental area may (on occasion) be quite rapid, and a particularly remarkable instance has been the spread of the Collared Dove Streptopelia decaocto from the Balkans to the Atlantic within 30 years. In this case, and in those of the marked northward spread in western Europe of Cetti's Warbler Cettia ceui and Serin Serinus serinus, it is tempting to postulate genetic changes that conferred wider habitat and/or climatic tolerances. No range expansion can succeed unless the new territory invaded provides suitable conditions, whether through environmental improvements within the area, or through the colonizing species adapting to new conditions-as when the typically alpine Dotterel Eudromias morinellus nests below sea level in Dutch polders, and the cliff-nesting Kittiwake Rissa tridactyla breeds on sand dunes (regularly in Denmark). Another important circumstance leading to range expansion is that of long-distance migrants breeding in their wintering areas; it may be relevant that most such cases involve species having delayed maturity, and therefore not infrequently oversummering within their respective winter ranges. An analysis of elements in the Afrotropical avifauna of European origin showed a continuum from long-established and welldifferentiated taxa, through established breeders little or not at all morphologically distinguishable from European populations, to northern migrants nesting only irregularly in Africa. (In contrast, there have been only a few, marginal, cases of Afrotropical species extending into North Africa or southern Europe.) This phenomenon of 'migration suspension' can also be inferred to have occurred in the New World, where a number of migratory species have given rise to resident insular races in the Caribbean, on Galapagos, and elsewhere.

An abrupt range expansion occurs when a species colonizes an island (more rarely a continent) where it does not normally occur even as a migrant; and there are few, even oceanic, islands which do not have their own endemic land-birds as consequences of invasions in the past. Perhaps because the number of ecological niches on islands is restricted, and liable to be filled through speciation by the ancestral colonizer, there are few modern examples of successful abrupt range expansion. One conspicuous exception concerns the invasion-type movements across the Tasman Sea from Australia, whereby New Zealand has gained breeding populations of Silvereye Zosterops lateralis (since 1856), Grey Teal Anas gibberifrons (probably since the late 19th century), Spur-winged Plover Vanellus miles (since about 1932), White-faced Heron Ardea novaehollandiae (since 1941), Royal Spoonbill Platalea regia (since 1950, still rare), Coot Fulica atra (since 1954), Black-fronted Dotterel Charadrius melanops and Welcome Swallow Hirundo neoxena (both from 1958). Moreover, during the 1970s there were New Zealand breeding records for Masked Wood Swallow Artamus personatus (1972 only), and for Australian Dabchick Tachybaptus novaehollandiae and Hoary-headed Grebe Podiceps poliocephalus (both of which seem to be in process of establishing themselves). There are also now frequent records of the Cattle Egret Bubulcusibis and even reports of breeding. Cases elsewhere include two high-latitude colonizations: of Greenland by the Fieldfare Turdus pilaris (in 1937, following an invasion during a period of climatic amelioration), and of South Georgia by the Speckled Teal Anasflavirostris (population discovered in 1971). Certain irregular irruptions, especially those occurring in spring, may lead to breeding in new areas, although not usually to permanent establishment therein (see IRRUPTION). On the other hand, some overseas invasions--possibly accidental in origin-may result in successful colonization simply because suitable conditions were already present in the new area, inaccessible until the ocean barrier was passed. Moreover, artificially introduced species may be able to spread rapidly for the same reason, especially if the newcomer happens to be more versatile than potential native competitors; such secondary range expansion has been seen with the Starling Stumus vulgaris in America, and in a variety of European passerines liberated in man-modified habitats in Australia and New Zealand. Among natural but accidental colonizations, the classic example is the spectacular spread by the Cattle Egret Bubulcusibis in the New World, where since about 1930 it has extended its range explosively both northwards and southwards; it is presumed that the colonizers reached South America from Africa via St Helena and St Paul's Rocks, where there have been recent sightings to show that transatlantic vagrancy by the species is continuing. In the opposite direction it spread via New Guinea to Western Australia, with frequent sightings in the 1950s. The first record from New Zealand was in 1963. The circumstances of range expansion among sea birds are obviously somewhat different, in that their often wide non-breeding ranges may include many potential new breeding sites. It seems likely that, in these birds, range expansion stems from population pressure within established colonies; in the cases of gulls, at least, new food sources from man's waste products and new safe roosts on artificial reservoirs appear to have been important factors. The expansion potential of seabirds is demonstrated in Britain and Ireland by the remarkable spread of the Fulmar Fulmarus glacialis (confined to St Kilda until 1878) and Kittiwake, by the establishment of new Gannet Sula bassana colonies, and by the adoption of nest sites on roof tops and other buildings in towns and cities by several species of gull. Despite a variety of Nearctic vagrants reaching Europe annually, there has been only one known instance of nesting-of Spotted Sandpiper Actitis macularia in Scotland-excluding two instances of Black Duck Anas rubnpes hybridizing with Mallard A. platyrhynchos in England. Range contractions. With the exception of populations endemic to small islands, for which unchecked decline will result in extinction (see EXTINCT BIRDS), declines most often manifest themselves in reduced densities that are not necessarily reflected (at least initially) in contractions of gross distributions. Where declines and contractions of range occur, the ultimate factors may be natural (often climatic) or unnatural (usually through human impact). In either category, species with restricted habitat requirements are the most vulnerable. Climatic amelioration in North Atlantic regions in the 1920sand 1930s enabled various temperate species to expand northwards (see above), but also resulted in contractions for some arctic species at the southern periphery of their range; instances include Brunnich's Guillemot Uria

Recognition

lomvia and Little Auk Alle alle in Iceland, and Ivory Gull Pagophila eburnea in Svalbard. When this warming phase ended by the 1950s, expansion by temperate birds slowed down and some early gains were lost, for example by Starlings in northern Fenno-Scandia. In Britain, modern contractions by certain insectivorous summer migrants, such as WryneckJynx torquilla and Red-backed Shrike Lanius collurio, may have been exacerbated by change towards cooler and wetter spring weather. At the other climatic extreme, increased aridity has resulted in an enlargement of southern deserts to the detriment of some resident species: Ostriches Struthio camelus formerly occurred much further north in Africa (also in the Middle East); while reduced Sahelian rainfall has also affected the survival of various European-breeding trans-Saharan migrants crossing or wintering in this zone. Short-term, traumatic weather factors (such as an unusually severe winter) generally have only a temporary effect, but can be serious in island situations: it may have been a hurricane which exterminated the remnant population of Grand Cayman Thrush Turdusravidus. Special cases include contraction following hybridization with a more successful (dominant) congener-Mexican Duck Anas (platyrhynchos) diazi and Black Duck with Mallard in North America----or through BROOD-PARASITISM affecting breeding success in a small population-as in Kirtland's Warbler Dendroica kirtlandii in Michigan; such instances are generally preceded by declines through (especially) habitat loss, leaving small populations more vulnerable to other pressures. The more worrying cases of range contraction observed this century are those attributed, directly or indirectly, to man's interventions. By far the more important factor has been habitat loss, especially through wetland drainage and deforestation, and it has affected tropical and temperate species alike. Changed agricultural practices have also made their impact in various ways. Thus more intensive land use has caused contractions affecting bustards (Otididae) and Demoiselle Cranes Anthropoides virgo on the steppes of the USSR and Prairie Chickens Tympanuchus cupido on the North American equivalent; changed hay-cropping regimes (following mechanization) have reduced the European population of Corncrakes Crex crex; pesticide usage has hit raptors especially; while greater care of livestock has been one cause for declines of vultures in southern Europe. When habitat loss is coupled with overhunting, the total impact is serious; classic cases include Eskimo Curlew Numenius borealis, Wild Turkey Meleagris gallopavo, the extinct Passenger Pigeon Ectopistes migratorius and various Asian cranes (Gruidae). Trapping for AVICULTURE is thought to have contributed to reductions among certain Australian parakeets (Psittacidae) and Asian pheasants (Phasianidae). Restricted populations have also proved vulnerable to the impact of alien species, especially mammals, introduced by man, whether through habitat destruction, e.g., by pigs and goats, or through direct predation on ground-nesting birds. Introduced disease has been suggested as a factor in a Hawaiian study, though it has not been established that this R.W.H. applies to larger land masses. Buckley, F.G. & Buckley, P.A. 1980. Habitat selection and marine birds. In Burger, J. et al (eds.). Behavior of Marine Animals, vol. 4. New York. Leek, C.F. 1980. Establishment of new population centers with changes in migration patterns. J. Field. Om. 51: 168-173. Murray, A.D. 1979. Colonization of Scotland by northern birds, 1820--1977. Scott. Birds 10: 158-174. Snow, D.W. 1978. Relationships between the European and African avifaunas. Bird Study 25: 134--148. Williamson, K. 1976. Recent climatic influences on the status and distribution of some British birds. Weather 31: 362-384.

RANK: see BIOSTATISTICS. RAPHIDAE: see under

COLUMBIFORMES; DODO.

RAPTOR: term used in much the same senses as

BIRD-OF-PREY.

RATIO-CLINE: a geographically continuous change in the ratio in which different morphs are present within a species that is dimorphic or polymorphic in appearance or behaviour (see POLYMORPHISM). RATITAE: see below.

RATITE: having a flat, raft-like sternum, i.e., without a keel; the converse of 'carinate' (see SKELETON, POST-CRANIAL). The structure is especially characteristic of the orders of flightless running birds, mainly

499

of large size, formerly grouped together as the 'Ratitae' and still loosely referred to collectively as the 'ratites' (see EARLY EVOLUTION OF BIRDS). A more or less ratite condition of the sternum is also found in some flightless species in other orders (see FLIGHTLESSNESS). A family based on the fossil genus Eleutherornis is referred to the Struthioniformes, and one based on Dromornis to the Casuariiformes (see FOSSIL BIRDS). Further, the Tinamiformes (Tinamidae) of the Neotropical Region, although flying and carinate, are considered to be closely related to the 'ratites' (see TINAMOU). The living or geologically recent ratites are all comprised in the order STRUTHIONIFORMES.

RAVEN: substantive name of some large species of Corvidae; used without qualification, in Britain, for Corvus corax (see CROW (1)). RAYADITO: substantive name of the 2 species of Aphrastura, a South American furnariid genus (for family see OVENBIRD (1)). RAZORBILL: Alca torda (see AUK). RECENT BIRDS: those forms that either exist at the present day or at least survived into geologically recent times. RECESSIVE: see GENETICS. RECOGNITION: a term that was originally applied to human behaviour but requires a new definition when applied to animal behaviour. The prefix 're' implies a learning process which allows the subject to identify an object as something that it has met before, and to distinguish it from other things. It has nevertheless been shown (R.A. Hinde) that a Canary Serinuscanaria will 'recognize' nest material as something to build a nest with (its behaviour shows that it identifies it and distinguishes it from other objects) when it has never before seen such material. Similarly, we speak of 'sex recognition', 'species recognition', and so on, when responses are confined to certain classes of objects, irrespective of the way in which this specificity of the response developed-whether it is 'innate' or has to be acquired. 'Recognition' is therefore usually taken to mean identification and distinction of an object or a class of objects among the multitude of external things that an animal is likely to encounter. It is not an absolute achievement; the range of objects identified and grouped together may vary from very wide (sex recognition) to very narrow (individual recognition); it never is so wide that it comprises all things; it probably never is so narrow as to be just one unique thing---even the best human observer may find it difficult to distinguish between identical twins. The width of the range is adapted in such a way as to make 'errors' in the natural situation sufficiently rare to avoid frequent miscarriages. 'Recognition', therefore, is an expression referring to what could be called the 'degree of specific releasability' of a response, and it has to be studied by an analysis of the stimulus situation evoking the response. This response is not (as often in human beings) a verbal one, but it has to be a recognizable movement. In this sense, birds can be said to recognize a very great number of things. The range is usually wide in responses to food; a Song Thrush Turdus philomelos recognizes red berries as a class (and perhaps distinguishes between several kinds), and also snails and earthworms. The range is extremely narrow in all cases of individual recognition. There is a graded series between these two extremes. Recognition is often achieved in a series of steps, viz., when the response is really a chain of separate reactions, each elicited by different stimuli provided by the same object. Thus the first response of a female Red-necked Phalarope Phalaropus lobatus to a prospective mate is often misdirected; she may approach birds of several other species (Purple Sandpiper Calidris maritima; Lapland Bunting Calcarius lapponicus; Ringed Plover C haradrius hiaticula). After this initial approach, however, the next response is shown only to Red-necked Phalaropes, while the other birds are ignored. Yet this second response is still the same to males and females and only the third step shows sex recognition, for it is then that females are chased and males are accepted. This seems to be a very general method of achieving specificity of response in spite of the relatively unspecific nature of each stimulus situation (see SIGN STIMULUS).

In many examples recognition is not dependent on previous conditioning; the female Canary's recognition of nest material has

500 Recognition, individual

already been mentioned; similarly, a young Herring Gull Larus argeniatus responds 'innately' to the adults' alarm calls. But song-birds refusing to eat wasps or their mimics have had to learn to recognize them as obnoxious, and a goose Anser sp. learns to recognize its fellow geese, first as representatives of a species, and later as individuals (see LEARNING; BEHAVIOUR, DEVELOPMENT OF). In symbiotic relationships in the widest sense (including intra-specific as well as inter-specific relationships), recognition has been enhanced by specializations both on the sensory side (responsiveness to special stimuli) and on the effector side (by the development of unambiguous releasers (see RELEASER)); a striking example of the latter is the specificity of song, and of signals that keep a flock of birds together. Highly specific releaser-response relationships seem to have been developed in connection with reproductive isolation between sympatric species (see SPECIATION; also ISOLATING MECHANISM; COLORAN.T. TION, ADAPTIVE). RECOGNITI0 N, INDIVID U AL: the ability of individual birds to recognize particular familiar individuals of the same species. To show that one bird recognizes another it is necessary to demonstrate that it behaves differently towards the familiar individual than towards other conspecifics, and that the response is not solely due to recognition of a particular site or context. Individual recognition of offspring by parents has been demonstrated in many species of colonial seabirds, including penguins (Adelle Pygoscelis adeliae, Yellow-eyed Megadyptes antipodes and King Penguin Aptenodytes patagonicus), terns (Arctic Sterna paradisaea), gulls (Blackheaded Larus ridibundus and Herring Gull L. argentatus) and Guillemots (Uria aalge), where parents bring food to their own chick in the midst of the colony even if it has strayed away from the nest site. Correspondingly, offspring of some seabirds, including guillemots, several species of gulls, and Wandering Albatross Diomedea exulans are able to recognize their parents and run towards them but not towards other adults that land nearby. In most species, recognition develops gradually during the early growth of the offspring (although auditory recognition may develop before hatching) resulting in the offspring becoming 'imprinted' on their parents. It is usually before adequate recognition has developed, when the chicks are very young, that in some species, parents may adopt strange chicks. Recognition may continue after the young have fledged in cases where parental care continues. Species where individual recognition of offspring by parents has not been established during the nestling period include Black-browed Diomedea melanophrys and Grey-headed Albatross D. chrysostoma, Gannet Sula bassana, Kittiwake Rissa tridactyla, and Puffin Fratercula arctica; and many passerines, for example Robins Erithacus rubecula and Pied Flycatchers Ficedula hypoleuca. This could be due to the small chance that the young will stray from the nest site or that the parents will mistakenly feed strange chicks. Mutual recognition between monogamous partners has been documented in a wide variety of species including Gannets, Bewick's Swans Cygnus columbianus beunckii, Herring Gulls, Flickers Colaptes auratus, Jackdaws Corvus monedula and American Goldfinches Spinus tristis, where individuals begin greeting displays when their partner appears at a distance. In some species recognition is observed even when partners have been separated for several months. Recognition by territory owners of neighbouring territory holders occurs in several passerine species where individuals show a stronger aggressive response to strangers than to neighbours. Evidence that birds recognize unrelated flock members is less abundant, although experiments showing an increased aggressive response of domestic hens to strangers introduced into a small stable flock indicate recognition. How individuals recognize each other is not always clear. In experiments showing recognition of neighbouring territory holders, individual birds were distinguishing differences in the songs (not the positions) of their neighbours from others. In particular, pitch and detailed phrase morphology have been found to be important in individual recognition in some species. However, among songbirds, it is not yet clear whether individual recognition can occur in species with large song repertoires. Auditory cues are also used by offspring guillemots, ducks (Wood Duck Aix sponsa), and domestic chicks even before hatching, and by partners of pairs in American Goldfinches. Recognition by visual cues has seldom been demonstrated directly. But Guillemots Uria aalge, whose eggs show great variation, and Ostriches Struthio camelus are able to recognize their own eggs (see AUK; OSTRICH).

Observations of birds recognizing their parents, mates and other flock members at a distance, in the absence of audible vocalizations, have been described for Gannets, Pintails Anas acuta, Herring Gulls, and Marsh Tits Parus palustris. Whether in these cases the birds are distinguishing particular physical characteristics or idiosyncratic behaviour is not clear. At closer range, experimental evidence suggests that the precise cues involved are mainly on the head: artificial changes in appearance of the head, neck and comb in chickens were most successful in preventing recognition by flockmates. In wild Bewick's Swans, individuals sometimes peck their mates when the latter are feeding with their heads below the water, but when the mate brings its head up a greeting immediately occurs, often with no audible vocalization. Despite the scarcity of evidence, the use of visual cues in individual recognition seems likely to be widespread in view of the exceptional visual acuity of birds and the extent to which they communicate visually. D.K.S. Beer, e.G. 1970. Individual recognition by voice in the social behaviour of birds. In Lehrman, D.S., Hinde, R.A. & Shaw, E. (eds.). Advances in the Study of Behaviour, vol. 3: 27-74. Brooks, R.J. & Falls, J.B. 1975. Individual recognition by song in White-throated Sparrows. II Features of song used in individual recognition. Can. J. Zoo1. 53: 1749-1761. GOOI, A.M. & Ortman, L.L. 1953. Visual patterns in the recognition of individuals among chickens. Condor 55: 287-298. Krebs, J.R. 1977. The significance of song repertoires: the Beau Geste hypothesis. Anim. Behav. 25: 475-478. Nelson, J.B. 1966. The behaviour of the young Gannet. Br. Birds 59: 393-419. Thorpe, W.H. 1968. Perceptual bases for group organization in social vertebrates, especially birds. Nature 220: 124-128. Tickell, W.L.N. & Pinder, R. 1972. Chick recognition by albatrosses. Ibis 114: 543-548. Tinbergen, N. 1953. The Herring Gull's World. London.

RECORDING: ultra-quiet song (see BEHAVIOUR, DEVELOPMENT OF (Subsong)); also, of course, the human activities of mechanically registering and reproducing bird or other sounds, and, more generally, the keeping of regular notes and observations. RECOVERY: see MARKING. RECTRIX (RECTRICES): a main tail feather (see TAIL). RECTUM: the large intestine (see ALIMENTARY SYSTEM). RECURVED-BILL: Megaxenops pamaguae; sometimes applied also to X enops spp. (see OVENBIRD (1)). RECURVIROSTRIDAE: see under CHARADRIIFORMES. The family comprises the avocets and stilts (see under AVOCET). REDBILL: name in South Africa for Anas erythrorhyncha, otherwise Red-billed Pintail (see DUCK). REDBREAST: alternative name of the Robin Erithacus rubecula (see THRUSH).

REDHEAD: Aythya americana (see DUCK). REDIRECTION: the direction of a behaviour response at other than the normal object. As a rule, animal behaviour is directed at certain parts of, or objects in, the environment-food-pecking is directed at food, attack is directed at a rival, and so on-and this is made possible by steering (as distinct from merely releasing or inhibiting) mechanisms; but in certain circumstances a response is directed at an object other than that normally drawing the response. Such responses to abnormal objects can be classed in two categories. On the one hand, when an animal is very hungry it may peck at inedible or inadequate objects not normally aimed at; a sexually deprived animal may copulate with substitute partners sometimes very unlike the normal partner; and a broody bird may sit on objects very dissimilar to eggs. These responses have in common that they are directed at a substitute object in the absence of the adequate object, and that the adequate object is preferred as soon as it is present. On the other hand, when a man scolds his subordinate after he has himself been rebuked by his superior, or kicks a chair in anger although the fellow human who aroused his anger is there, we speak of a redirected

Releaser

attack; and such redirected attacks are common in birds. They occur when an individual is provoked to attack another individual, but cannot do so because it is either afraid of its attacker or is inhibited in some other way, for instance by personal 'love' for its sex partner. A redirected attack may be aimed at a third bird happening to be near, or it may be as extreme as table-banging by an angry human; thus a male Herring Gull Larus argematus regularly pecks violently into the ground when facing a rival near the territory's boundary. It seems likely that such redirected attacks have also contributed to the 'raw material' from which signal movements have evolved (see DISPLACEMENT ACTIVITY; RELEASER). They are often followed by displacement activities, and can probably determine which particular displacement activity will be shown by providing stimuli that facilitate one particular movement. N .T .

REDPOLL: substantive name of 2 Carduelis spp.; used without qualification, in Britain, for C. flammea (see FINCH). See photo NEST

REFUGE: see CONSERVATION. REGENT-BIRD: Regent Bowerbird Sericulus chrysocephalus (see BOWERBIRD).

REGION, ZOOGEOGRAPHICAL: or faunal region, see DISTRIBUTION, GEOGRAPHICAL.

REGULIDAE: a family recognized by some authors, but here merged in the subfamily Sylviinae of the Muscicapidae (see WARBLER (1)). REGURGITATION: ejection of partially digested food from the gizzard, as food for young; ejection of PELLETS; ejection of stomach oil by young birds, e.g., Fulmar Fulmarus glacialis, under threat from an intruder (see ODOUR). See photo PARENTAL CARE.

BUILDING.

REINFORCEMENT: see LEARNING.

REDSHANK: substantive name of Tringa totanus, for which it is used in Britain without qualification, and one congener (see SANDPIPER). See photo COPULATION.

REJUNGENT SPECIES: see RING-SPECIES.

REDSTART (I): substantive name of Phoenicurus spp.; used without qualification, in Britain, for P. phoenicurus (see THRUSH). REDSTART (2): substantive name, in North America, of species of Setophaga and Myioborus (see WARBLER (2)). REDTHROAT: Sericornis brunneus (see WARBLER,

AUSTRALIAN).

RED TIDE: the bloom of a single-celled organism in the sea, its large numbers often imparting a rusty-red coloration. In temperate waters the organism is usually Gonyaulax tamarensis, which, when at high densities, produces an extremely powerful nerve poison to which birds and mammals are very sensitive. Frequent red tides are recorded from the west coast of North America. The first major outbreak in Europe this century occurred in 1968, killing 80% of the breeding shags Phalacrocorax aristotelis on the Farne Islands (NE England) in a few days, and many other species being affected. Since then, blooms have been recorded from Norway to Spain. Red tides in tropical waters are caused by a different organism which does not produce a toxin but which de-oxygenates the water, killing large numbers of fish, but few seaJ.C.C. birds. REDUCTION-DIVISION: meiosis (see CELL;

GENETICS).

REDWING: Turdusiliacus(see THRUSH); in North America sometimes applied to the Redwinged Blackbird Agelaiusphoeniceus (see ORIOLE (2)); in Africa applied to Francolinus levaillantii(see PHEASANT). REED-FINCH: substantive name of Donacospiza albifrons, a South American finch (for family see BUNTING). REED-HAUNTER: substantive name of Limnornis curvirostris and Limnoctites rectirostris (for family see OVENBIRD (1)). REEDHEN: substantive name sometimes applied to gallinules of the genus Porphyrula (for family see RAIL). REEDLING: alternative name for the Bearded Tit Panurus biarmicus (see under PARROTBILL). REELING: see CHURRING. REEVE: see RUFF. REFLEX: 'an innate relatively simple and stereotyped response involving the central nervous system and occurring very shortly after the stimulus which evokes it; it specifically involves a part only of the organism, though the whole may be affected, and is usually a response to localized sensory stimuli' (Thorpe 1951)-see FIXED ACTION PATTERN; also LEARNING. REFRACTORY PERIOD: see penultimate paragraph of OLOGY AND THE REPRODUCTIVE SYSTEM.

ENDOCRIN-

SOl

RELEASER: term originally given a precise and unambiguous definition by Lorenz in 1935 but since applied in two very different senses. In the original sense, a releaser is not a stimulus, but a type of effector device (in the widest sense-s-either a structure, or a movement, or a scent, or a call) with a very specificfunction, namely that of providing stimuli which release (or inhibit) a response or a set of responses in another animal of the same species. The concept became necessary when it was pointed out that there are structures, movements, sounds, and so on which can be shown to provide such stimuli, for which no other function can be found, and which are obviously well suited to the broadcasting of stimuli. Thus, the red colour of the breast feathers of a Robin Eruhacus rubecula, the brightly coloured wing specula of ducks (Anatidae), the red patch on the lower mandible of a Herring Gull Larus argentatus, the nest-showing ceremonies of various male birds (Wren Troglodytes troglodytes; Kestrel Falco tinnunculus; Black-headed Gull Larus ridibundus; Redstart Phoenicurus phoenicurus; Pied Flycatcher Ficedula hypoleuca), the head-tossing movements of female gulls (Larinae), the song of male song-birds, alarm calls, and many more, all provide stimuli releasing or directing more or less specificresponses in fellow members of the species, and are therefore called releasers. The 'rodent-run' and other distraction displays of waders (Charadrii) and other birds lure predators away from the brood (see DISTRACTION BEHAVIOUR); these activities, like the hissing of the Great Tit Porus majorand Wryneck]ynx torquilla, aposematic coloration, and the luring flight of honeyguides (Indicatoridae), subserve interspecific communication; the term releaser can of course be applied to them as well. While the word is not important, provided that it is used consistently, the distinction between the two concepts (releaser and stimulus) is essential. The difference between the concept of releaser and that of sign stimulus, to which the word 'releaser' is often applied, is to be found in the adaptedness of the releaser as a signalling device (see SIGN STIMULUS). A pike Esox lucius, snapping at a piece of shiny metal dragged through the water, is responding to a sign stimulus normally provided by its prey. Yet the silvery shine of, for example, a roach has certainly not developed as a means to enable the roach to be captured by a pike; if anything, the pike has helped to exert selection pressure against such conspicuousness. The red spot on the bill of the Herring Gull, on the contrary, must have been favoured by selection pressure, since it helps in eliciting the chick's begging, which in turn stimulates its parent to feed it; and song, by attracting females, facilitates pair formation and as such is favoured by selection. The argument is particularly convincing in those cases where releasers have developed in spite of the dangers to which they expose their bearers in other contexts, especially when they make them more vulnerable to attack by predators. Thus the term 'releaser' is intended to characterize a category of effector by its exclusive or main function, just as the term 'wing' is used to name any organ which provides lift and propulsion in flight, even although a wing may also be used as, for instance, a weapon in fighting. Many releasers, such as alarm calls, have been shown literally to release a response. Others, such as the head-flaggingin gulls and other 'appeasement gestures', stop a response (see DISPLAY); others again, such as the song of male song-birds, release and also direct the movements of other birds (in this case, repulsion of males and attraction of females). For this

502 Relict

reason, the term 'signalling device' is perhaps preferable. The latter example also shows that one feature may have more than one function. The second function need not be that of signalling, and its demands may even conflict with those of the releaser function; the most obvious examples of such conflicting demands are procryptic birds that have at the same time conspicuously coloured structures; such species have reached a compromize by concealing the bright colours so long as they are not actually needed. Comparative studies sometimes enable one to make a guess at the origin of releasers, and it is probable that they are secondary specializations of organs and movements primarily adapted to other functions, selection pressure having favoured simplicity, conspicuousness, and unambiguity; and this seems in accord with the known properties of the sensory functions through which they exert their effect (see SIGN STIMULUS). Evolution being a slow and gradual process involving a very large number of extremely small steps, it is evident that the distinction between organs which are obvious, highly specialized releasers (such as the wings of a male Argus Pheasant Argusianus argus) and those that are not yet, or no longer, or not exclusively releasers cannot be sharp. This is of course true of every category of organ. The function of an alleged releaser is often suggested by observations but can be experimentally tested in experiments with dummies. N.T. Lorenz, K. 1935. Der Kumpan in der Umwelt des Vogels. J. Orn. 83: 137-213, 289-413.

RELICT (or RELIC): term applied to isolated (sometimes discontinuous) populations that appear to represent a former much wider distribution. REMEX: a main flight feather; the remiges are classed as primary and secondary (see PLUMAGE; PRIMARY; WING). REMICLE: term properly restricted to a small feather found on the wing in some species, attached to the second phalanx of digit II. Most authors have considered it to be a vestigial primary remex, but Stresemann believes it to have been a covert to the terminal claw possessed by ancestral forms (see under PRIMARY). REMIGES: plural of

REMEX.

REMIZIDAE: family of PASSERIFORMES suborder Oscines;

PENDULINE

TIT.

RENAL FUNCTION: see EXCRETION,

EXTRARENAL.

REPELLENTS, CHEMICAL: man has probably tried to protect his crops with chemical repellents of some kind ever since he first tilled the soil. Concoctions of plants which, at least to humans, have pungent odours or an unpleasant taste feature in countless 'cottage' remedies for the prevention of bird damage and this folklore extends to the use of foul-smelling animal oils, faeces and urine, all of which may be used as ingredients in traditional repellent formulations. It is understandable that people should use such materials in an attempt to repel animals; we find them unpleasant, therefore other species having similar sensory systems will also find them unpleasant. This reasoning finds support in the fact that some animal species themselves employ chemical repellents in defence; skunks (Mephitis) are legendary in this respect but there are many less well-known examples including some birds. For example, Fulmars Fulmarus glacialis defend the nest site by squirting intruders with a foul-smelling liquid regurgitated from their crops and Eiders Somateria mollissima cover their eggs with faeces before leaving the nest unattended. However, these mechanisms have probably evolved for use against predatory mammals, rather than birds, and confirmation of the practical value of chemical repellents against birds is hard to find. Since any repellent effect is first dependent on the bird perceiving the stimulus, it is pertinent to consider what we know about the chemical senses of birds. By far the most important of these are the senses of SMELL (olfaction) and TASTE (gustation) and, although normally regarded as separate functions, they are so closely related as to be, at times, indistinguishable. Consider a bird approaching a potential food source. The olfactory system will be the first of the chemical senses to receive stimulation; the question is 'Do birds have a functional sense of smell?' This has been a subject of controversy ever since Darwin and Audubon

addressed themselves to the problem and is not fully resolved yet. On present evidence it seems fair to conclude that the olfactory mechanism is functional in most birds but only a few species exhibit odour-related behaviour in connection with food. If most birds disregard olfactory cues then in practice it will prove impossible to manipulate their behaviour via this channel of communication. Clearly this would not be true for those few species that do seek food by smell, e.g., the Kiwis Apteryx and honeyguides Indicator; their food-finding would be vulnerable to disruption by the introduction of false or masking odours. But these species are not pests and, unless future research reveals otherwise, we should regard the birds that eat our crops as unresponsive to odours. Hence the development of olfactory repellents seems unlikely. If odours will not repel birds then perhaps flavours can be used to better effect. Nobody seriously doubts that birds can taste but nevertheless the role of gustation in food selection remains obscure. As in mammals, the sensory receptors for the perception of flavours are the 'taste buds', consisting of clusters of cells lying in cavities in the epithelium of the tongue, but whereas mammals typically have many thousands of taste buds few birds have more than a hundred. It is tempting to conclude that birds are correspondingly less sensitive to flavours than mammals but this is not necessarily so; for instance it has been shown (Duncan 1963) that pigeons can discriminate between substances that are tasteless to man. It is logical to assume that an animal possessing a functional sense of taste will utilize that sense in the selection of food, yet there is little evidence that birds do so. Englemann (1940) concluded that hens select grains on the basis of shape, and to a lesser extent colour; taste played little or no part. Much of the experimental work done since then, often in connection with the search for chemical repellents, points to the conclusion that taste per se is not very important to birds and suggests that a substance is unlikely to qualify as a bird repellent simply because it has an unpleasant flavour. However, taste stimuli rarely occur in isolation; certainly the ingestion of food represents a complex sensory experience, involving visceral, tactile, olfactory and thermal information in addition to that concerned with flavour. In consequence, behaviour that gives every appearance of being tasteorientated may be controlled by other factors. Some authorities refer to a specific 'chemical sense' in birds and regard the many unspecialized nerve endings as receptor organs. If such a sense exists, it remains ill-defined and there is little to indicate how it functions. It is certainly true that in some cases chemical stimulation may result in pain, or other disturbing sensations, and animals quickly learn to avoid situations that give rise to such unpleasant experiences. This is known as 'conditioned aversion' and typically follows sub-lethal poisoning by a toxic food. The phenomenon often occurs in connection with poison baiting for rodent control when the condition is known as 'bait shyness' . In those circumstances it is a highly undesirable response, because it reduces the consumption of bait and hence the kill, but it is exactly the response we endeavour to achieve with repellents. Some chemicals, e.g., lithium chloride and certain carbamate compounds, seem to possess properties conducive to the establishment of aversive associations of this type and which can result in a dramatic avoidance of further contact with the chemical. One such compound, methiocarb, is now widely used in the USA and elsewhere as a bird repellent (Rogers 1980). Despite being highly poisonous few, if any, casualties occur because birds are repelled before they have time to ingest a lethal dose. Nevertheless, there are obvious risks associated with the use of such chemicals and it is open to question whether very toxic substances qualify to be called 'repellents'. Chemical defence mechanisms evolved by insects against bird predators usually involve cardiac glycosides which have a specific action on the vertebrate heart. They also have side-effects, one of which is to stimulate vomiting, and since the emetic dose is about half the lethal dose this functions as a safety factor and normally prevents retention of a lethal dose. Brower (1969) has pointed out that in such a mechanism there are 3 levels at which repellency can occur; basic gastronomic rejection, brought about by the effect of the poison, and subsequently rejection by recognition of flavour or appearance as a conditioned response. It has been suggested that such aversive conditioning could be applied to predator-prey problems involving large raptors (Brett et alI976). These experiments are a stimulating advance in repellent research although confirmation of success in practical application is still awaited. Another mechanism of repellency is that of behaviour-modifying chemicals. There is no evidence for the existence in birds of any mechanism analogous to that of pheromones in insects, but chemicals

Respiratory system

have been used to modify behaviour in a different way. Birds display great panic following the ingestion of the compound, 2,4-animopyridine, possibly because they suffer pain and partial paralysis. Affected birds tend to utter distress calls and fly in spirals; conspecifics hearing the calls, and observing the strange behaviour, usually flee. Thus, for gregarious species, large flocks may be scared away by the aberrant behaviour induced in a few individuals. A bait containing 1% or 2% of treated particles is used and in this way sufficient can be laid to prove attractive whilst ensuring that relatively few birds are affected. It is sometimes argued that such a method is a useful conservation tool, since it avoids mass destruction, but many people consider the technique to be inhumane and its use is prohibited in many countries, including Britain. Yet another approach to repellency is to consider feeding mechanisms and exploration of this is just beginning. It is obvious that any particular species of animal accepts as food only a narrow spectrum of potentially nutritious items. In other words, they are selective and this implies the existence of a mechanism of discrimination which results in acceptance or rejection. If these mechanisms can be elucidated they may mark a significant step toward the discovery of really effective repellents. E.N.W. Brett, L.P., Hawkins, W.G. & Carein, J. 1976. Prey-Lithium aversions III: Buteo

hawks. Behavioral Biology 17: 87-98. Brower, L.P. 1969. Ecological chemistry. Scientific American 220(2): 22-29. Duncan, C.]. 1963. The response of the feral pigeon when offered the active ingredients of commercial repellents in solution. Annals of Applied Biology 51: 127-134. Englemann, C. 1940. Versuche tiber die Beliebtheit einiger Getreidearten beim Huhn. Zeitschrift fur vergleichende Physiologie 27: 525-544. Rogers, ].G. 1980. Conditioned taste aversion: its role in bird damage control. In Wright, E.N., Inglis, I.R. & Feare, C.]. (eds.). Bird Problems in Agriculture. British Crop Protection Council Symposia Series Monograph 23.

REPRODUCTIVE ISOLATION: a situation in which intrinsic factors wholly or largely prevent interbreeding between closely related species, or populations of a species (see ECOLOGICAL ISOLATION; ISOLATING MECHANISM; SPECIATION). It is to be distinguished from geographical or ecological isolation, where extrinsic circumstances prevent contact between populations that might otherwise be fully capable of interbreeding. REPRODUCTIVE RATE: see CLUTCH-SIZE (Reproductive rates and other reproductive tactics); ECOLOGY. REPRODUCTIVE SYSTEM: see ENDOCRINOLOGY

AND THE REPRO-

DUCTIVE SYSTEM.

REPTILIAN ANCESTRY: see EARLY EVOLUTION

OF BIRDS.

RESERVE, NATURE: see CONSERVATION. RESIDENT: remaining throughout the year in the area under reference, the term being applied to a species, subspecies, population, or individual bird as the context requires; in another usage the term means breeding in the area, a distinction being then drawn between 'permanent resident' and 'summer resident' (='summer visitor')--see MIGRATION. RESONANCE: setting up vibrations that increase the volume of a sound (see SYRINX; also MECHANICAL SOUNDS). RESPIRATORY SYSTEM: in general, this system in birds is differentiated into the rigid lungs for gas exchange and into the air sacs, which act as bellows for their ventilation. This differentiation is based on the subdivision of the avian body cavity by septa (Duncker 1979). The unique avian respiratory system is characterized by the highest gas exchange capacity in vertebrates, and in its development it is necessarily based on the incubation in an egg. Each of the two symmetrical lungs fills one of the cavities which are situated in the dorsal portion of the rigid thoracic cage. Each pleural cavity (Fig. 1) is lined medially by the vertebral column and its ventral processes, dorso-laterally by the flat transverse vertebral processes and by the ribs and their musculature. Dorsally, the ribs arch through the pleural cavity, making deep incisions into the lung. Ventrally, the pleural cavity is lined by the horizontal septum, which originates from the

503

Fig. 1. Drawing of a preparation of a Mallard duck Anas platyrhynchos, left side from lateral. Thoracic and abdominal wall musculature has been removed and the lung is extirpated out of the pleural cavity. Horizontal septum (h) with Mm. costoseptales (h'), oblique septum (0). Cervical (A), clavicular (B), cranial (C) and caudal CD) thoracic, and abdominal (E) air sacs. (From Duncker 1971).

ventral margin of the vertebral column or its ventral processes, and is inserted, descending slightly ventrally, on to the ribs. At this lateral margin the horizontal septum contains the costoseptal muscles, which dilate during inspiration and contract during expiration (Fedde et al 1964). The actions of these muscles compensate for the slight volume changes of the pleural cavity, which are minimal due to their dorsal position in the rigid rib cage. Thus, the avian lung maintains a constant volume during the respiratory cycle, in contrast to reptilian and mammalian lungs which are inflated and deflated by the respiratory movements. The volume changes of the respiratory movements act only on the air sacs, which ventilate the rigid bronchial system of the lung. The air sacs are situated in the subpulmonal cavity (Duncker 1979) beneath the lung and its horizontal septum. The symmetrical subpulmonal cavities are cranially united and together with the air sacs fill the thorax cranial to the heart, often protruding into the lower neck. Lateral and caudal to the heart, the subpulmonal cavity with the air sacs occupies the space on each side between the body wall and the intestines, separated medially from the intestines by the oblique septum. This septum originates from the vertebral column and cranially from the lateral pericardial wall; it is inserted ventrally near the lateral margin of the sternum. The subpulmonal cavity extends further caudally than the lung; and varies in extent among the different avian families. Only the most caudal air sac invades the peritoneal cavity and spreads dorsally around the intestines (Fig. 1). The air sacs are thin-walled and in addition to filling the subpulmonal cavity and the dorsal peritoneal cavity, protrude in the form of diverticula between different organs: between the kidneys and the synsacrum, around the articulations of the bones of the trunk and the neck including the shoulder and hip joint; they also invade the bones of the trunk, the vertebral column and the proximal bones of the wing and leg. Additionally, they invade the vertebral canal between the vertebral bodies and the dura mater in the thoracic and lower neck region. This pneumatization is found in the majority of birds, independent of their body size, but varying in extent; it is generally reduced or lacking only in some birds which swim under water. It has no function in connection with respiration. Upper air ways. The air enters through the external nares at the upper bill into the nasal cavities. The location, form and direction of the external nares are highly variable, e.g. near the tip of the bill in kiwis, at the base of the bill in most species. The air passes through the nasal cavities and/or the oral cavity, which function in warming and humidifying the air, and in olfactory control. This passage over the mucosal surfaces is important, especially in small species, as an aid to effective heat and water balance by re-utilization of the expired air (SchmidtNielsen et al 1970). The slit-like opening of the glottis at the base of the tongue, which is controlled by muscles, regulates the in- and out -flow of air. There are no vocal chords as in mammals; the sound production in birds is restricted to the SYRINX. The glottis opens into the larynx, which leads into the trachea. The avian trachea is, in contrast to mammals, totally surrounded by tracheal rings, which ossify in many species. Externally, the trachea is accompanied over its length by the tracheal muscles. The lower trachea enters the cranial thoracic aperture, where it is surrounded by the clavicular air sac, which incorporates also the bifurcation of the trachea. In some birds, especially in penguins, the trachea is double-tubed, starting more or less distant from the larynx. Starting at the bifurcation, the two extra pulmonary primary bronchi run

504 Respiratory system

bronchus (Fig. 3). This system makes up the paleopulmo (Duncker 1971), which is present in all birds. Between the posterior primary bronchus and the air sac ostia of the caudal air sacs an additional connection is formed via a parabronchial network (Fig. 5), the neopulmo (Duncker 1971). The neopulmo is absent in penguins and emus; it is found in all other birds and is most highly developed in galliform and song birds. The paJeopulmo. The 4 medioventrobronchi (Figs. 2, 3, 4) originate dorsomedially from the entering primary bronchus, one directly behind the other. The first bends cranially, the others medially: they dilate and ramify, spreading over and occupying the ventral surface of the lung directly above the horizontal septum. The first medioventrobronchus, with its numerous branches lying side by side, occupies the cranial third of the ventral lung surface and terminates cranially, bending on to the dorsolateral lung surface, medially on to the lower medial surface. The second medioventrobronchus continues, with its branches, along the ventral covering of the lung surface, followed by the third medioventrobronchus which reaches the mediocaudal edge of the lung. The terminal branches of both medioventrobronchi curve onto the lower medial surface. The fourth medioventrobronchus joins the third on its lateral side, in most species with only a few branches or none at all. Only the lateral part of the ventral lung surface caudal to the lung hilus is not occupied by medioventrobronchial branches, but rather by paleopulmonic parabronchi. A branch of the first medioventrobronchus penetrates the horizontal septum cranial to the lung and opens into the cervical air sac. The third medioventrobronchus, directly after its origin, gives off a short, wide stem, which bifurcates through the horizontal septum directly medial to the lung hilus and opens into the clavicular and into the cranial thoracic air sacs. The region lateral to the hilus contains the lateral ostia into the clavicular and cranial thoracic air sacs. This region is supplied by a large lateral branch of both the first and second medioventrobronchus and in many species also by a lateral branch of the fourth medioventrobronchus (Fig. 3). However, in most species these ostia are not directly connected to the medioventrobronchus branches, but via the parabronchial net. Fig. 2. Schematic cross section of the trunk of a White Stork Ciconia ciconia, view from cranial on to the caudal part of the trunk, out of which only the primary bronchus (2) projects. The lung with medioventrobronchi (3), mediodorsobronchi (4), lateroventrobronchi (5) and parabronchi (6) above the horizontal septum; beneath it, between body wall and oblique septum, the air sacs (D, E). Between both oblique septa space for the intestines. (From Duncker 1971).

toward the lung hilus. They are surrounded by C-shaped bronchial cartilages, which also protect the first short part of the intrapulmonary primary bronchus. Then the cartilages disappear completely; the further primary bronchus and all other bronchi of the avian lung are free of cartilage. The respiratory epithelium of the trachea and primary bronchi contain glands consisting of goblet cells, varying in number depending on the species and on the size of the bird. Goblet cells are responsible for the final humidification of the air (Menuam and Richards 1975). Lungs. The lungs (Fig. 4) are not lobed and adhere to the walls of the pleural cavities. They are fixed and rigid in form and are constant in volume during all respiratory phases. The primary bronchus enters the lung hilus through the horizontal septum at the ventral lung surface together with the pulmonary vessels. The primary bronchus gives off immediately on its dorso-medial side the first set of secondary bronchi (the 4 medioventrobronchi) (Fig. 2), which spread over the ventral lung surface. The primary bronchus continues on its course to the dorsolateral lung surface, at or near which it bends caudally. It then runs in a dorsally curved course to the caudal lung margin, giving off the second set of secondary bronchi (the 7 to 10 mediodorsobronchi) which spread out at the laterodorsal surface of the lung. Opposite the mediodorsobronchi, the 4 or 5 lateroventrobronchi originate, spreading out between the primary bronchus and the horizontal septum. At the caudal lung margin the primary bronchus terminates in the abdominal air sac. From the internal surfaces of these 3 sets of secondary bronchi the parabronchi originate (Figs. 2, 3). The parabronchi of the medioventrobronchi anastomose with those of the mediodorso- and lateroventrobronchi in the planum anastomoticum, situated medially in the lung. The cranial air sacs are connected to the medioventrobronchi, the caudal air sacs to the first lateroventrobronchus and to the terminal primary

Fig. 3. Semi-schematic drawing of the lung and air sacs of the Stork. Trachea 0), primary bronchus (2), medioventrobronchi (3), mediodorsobronchi (4), lateroventrobronchi (5), parabronchi (6). Connections of the cranial air sac group indicated by black arrows: cervical (A) to the first medioventrobronchus, clavicular (B) and cranial thoracic (C) air sacs to the third medioventrobronchus and to the lateral ostia. Connections of the caudal air sac group are indicated by white arrows: caudal thoracic (D) and abdominal (E) air sacs to the lateroventrobronchus and caudal primary bronchus. (From Duncker 1972).

The 7 to 10 mediodorsobronchi (Figs. 2, 3, 4) originate dorsally from the primary bronchus, starting at that point where it bends caudally. The first 3 or 4 mediodorsobronchi originate directly one behind the other, their openings being separated from each other by only a thin membrane, whereas the distances between the openings of the succeeding mediodorsobronchi increase. All mediodorsobronchial openings are directed caudally, and the first 3 or 4 one above the other (Fig. 4). After their

Respiratory system

9

Fig. 4. Drawing of the left lung of a Mute Swan Cygnus olor, from lateral. The lateral part of the lung has been removed to (1) expose primary bronchus (2), medioventro- (3), mediodorso- (4), lateroventrobronchi (S) andparabronchi (6).Ostiaintothe caudal thoracic (D') andabdominal (E') air sacs. The surface of the lung between the secondary bronchi is covered by thin-walled air bubbles (9). (From Duncker 1972). initial cranial course, the mediodorsobronchi bend dorsomedially, except for the first and the last, which bend mediocaudally. They spread over the dorsolateral surface of the lung, directly beneath the thoracic wall. The first mediodorsobronchus ramifies into a large number of branches and supplies a broad area at the cranial lung surface, including the ventral part of the lung surface lateral to the lung hilus. The remaining mediodorsobronchi have a decreasing number of branches, and the last one, none at all. They supply areas of decreasing extent, which lie exclusively dorsal to the primary bronchus. In most species the neighbouring branches join each other directly, covering the entire dorsolateral surface. Their terminal branches end at a greater distance from the cranial margin of the lung, but mediodorsally they curve onto the medial surface. The mediodorsobronchi do not have any air sac connections. The 2 to 5 lateroventrobronchi (Figs . 2, 3, 4) originate from the primary bronchus opposite the middle mediodorsobronchi. Their openings are directed caudally similarly to those of the mediodorsobronchi, and after their initial cranial course they bend ventrally and caudally. The first lateroventrobronchus is usually large, has no branches, and does not give off parabronchi into the paleopulrno. It connects to the caudal thoracic air sac via a funnel-shaped opening, penetrating the horizontal septum near the lateral lung margin between the lung hilus and the caudal lung margin. The next one to 4 smaller lateroventrobronchi regularly do not have ramifications. They occupy the space between the primary bronchus and the horizontal septum, giving off parabronchi medially. The lateroventrobronchi mark the lateral border of the paleopulmo, lying at the lateral lung surface in birds that lack a neopulmo . The parabronchi of the paleopulmo (Figs. 2, 3) originate (I) from the entire internal surfaces of the medioventrobronchi and their terminal branches, and (2) from the entire internal surfaces of the mediodorso- and lateroventrobronchi and their terminal branches. Directly after their origin, they are interconnected with the neighbouring parabronchi by short ramifications. In most species they then run without further ramifications straight toward the medial planum anastomoticum. There, each parabronchus is connected with 2 or 3 parabronchi of the opposite side. Thus, the medioventrobronchi on one side are connected to the mediodorso- and lateroventrobronchi on the other side. The first and second medioventrobronchi and their lateral branches receive parabronchi from the first and second mediodorsobronchi and their lateral branches. The third and fourth medioventrobronchi receive parabronchi from all the succeeding mediodorsobronchi, the fourth medioventrobronchus also from the small lateroventrobronchi. These latter parabronchi lie directly at the ventral lung surface upon the horizontal septum, lateral to the fourth medioventrobronchus. The neopulmo. Only in a few groups, such as penguins and emus , does the paleopulmo make up the entire lung . In cormorants and storks , there is a small additional network of parabronchi, the neopulmo (Fig. S). It connects the caudal primary bronchus with the ostia of the caudal air sacs. The neopulmo becomes larger in more highly developed birds such as ducks , gulls and pigeons, and it achieves its highest development in plovers and sandpipers and in galJiform birds (Fig . 5). The neopulmo never exceeds 20% of the total lung volume. The neopulmonal parabronchi possess the same species-specific structure as those of the

505

paleopulmo, but they are richly interconnected over their entire length, lacking long unramified sections. The neopulmonal parabronchi (Fig. 5) originate from the lateral side of the primary bronchus, starting cranially at the origin of the first mediodorsobronchus, and also from the lateral sides of the large and the succeeding smaller lateroventrobronchi. In species with a more highly developed neopulrno, parabronchi originate also from the initial pans of the mediodorsobronchi and run toward the ostia of the caudal thoracic and the abdominal air sacs, entering the ostia laterally, often forming a separate funnel-shaped opening or a collecting saccobronchus . In a larger neopulmo, multiple layers of interconnected parabronchi occupy the lateral pan of the lung and displace the primary bronchus, together with the origins of the mediodorso- and latero-ventrobronchi, medially into the lung. In a large neopulmo, an increasing number of neopulmonal parabronchi connect with the abdominal air sac, whereas in the primary bronchus the diameter terminally decreases. Thus, in galJiform and song birds the primary bronchus is functionally substituted by the neopulmonal network, its entrance into the abdominal air sac being reduced

Fig. S. Semi-schematic drawing of the paleopulmo and neopulmo. (a) King

Penguin Aptenodytes patagonicu s, without a neopulrno, (b) Mallard Anas platyrhynchos with a medium-sized neopulmo, (c) Domestic Fowl Gallus domesticus with a highly developed neopulmo. Trachea (1), primary bron-

chus (2), medioventro- (3), mediodorso- (4), lateroventrobronchi (S), neopulmonal parabronchi (7), saccobronchi (8), cervical (A), clavicular (B), cranial (C) and caudal thoracic (D), abdominal(E) air sacs withtheirostia. (From Duncker 1971).

506 Respiratory system

diameter (5 f.Lm-14 um, species-specific) similar to blood capillaries. The air capillaries intrude between the numerous blood capillaries and fuse around them to form a sponge-like three-dimensional net (Fig. 8). The blood capillaries, originating from interparabronchial arterioles, run slightly curved, but mostly without interconnections, from outside the parabronchi toward its lumen. Here, beneath the atria, they collect into small venules which bring the blood back into the interparabronchial venules. This intermingled meshwork of blood and air capillaries makes up the large surface at which the gas exchange between blood and air takes place (Fig. 9). The basic structure of the parabronchus varies only to an astonishingly limited degree in different bird species, even with extreme differences in body size, taxonomic position and flying ability. The diameter of parabronchi varies from maximally 2 mm in ostriches, swans and turkeys to minimally 0.5 nun in some small song-birds and hummingbirds. In the latter and other advanced flyers, the atrial zone may be reduced or lacking, whereas the basic parabronchial form is found in poor flyers. The anatomical constancy is due to the fact that exchange of gas in the air capillaries takes place only by diffusion, so that a thickness in these capillaries of more than 0.5 nun is ineffective. Based on certain physical laws stating that the surface tension of the wet phase of the air capillary boundary against air strongly increases with the reduction of the diameter of the air-conducting structure, the volume constancy of the lung and the

b Fig. 6. Diagram of the paleopulmo and its air sac connections, (a) inspiratory phase, (b) expiratory phase. The black arrows indicate the direction of air flow during the respiratory phases; the white arrows express the air sac dilatation or compression. Trachea (1), primary bronchus (2), medioventro- (3), mediodorso- (4), lateroventrobronchi (5) and para bronchi (6). Cervical (A), clavicular (B), cranial (C), caudal thoracic (D), and abdominal (E) air sacs. (From Duncker 1974).

to a diameter smaller than a parabronchus. However, the large lateroventrobronchus, connecting with the caudal thoracic air sac, is never reduced in its diameter. Its ostium is laterally enlarged by the development of the neopulmonal ostium, or it is displaced toward the medial ventral lung surface, and a separate neopulmonal ostium occupies the lateral lung margin. A large neopulmo also expands into the lung region lateral to the hilus, replacing the lateral branch of the first mediodorsobronchus. Thus, the neopulmo receives direct connections to the lateral ostia of the clavicular and cranial thoracic air sacs. The parabronchus (Fig. 8) is the functional unit of the avian lung, being unique among vertebrates. It consists of a long hollow tube, through the lumen of which the air flows. The parabronchial lumen is surrounded by a zone of hollow chambers, the atria, through which the air diffuses into the surrounding broad mantle of exchange tissue. The exchange tissue is made up of a blood-capillaryI air-capillary meshwork, which is supplied by arterioles and venules running in the interparabronchial septa between the neighbouring parabronchi. The parabronchial lumen is surrounded by circular bundles of smooth muscle cells, which are interconnected by oblique strands, or by a more hexagonal arrangement of these bundles, varying in different species. Between the bundles, openings from the lumen into the atria are separated by thin membranes (Fig. 8), which carry only a few capillaries to supply the muscles. Around the muscle bundles and in these membranes a loose network of elastic fibres is found, whereas in the mantle of exchange tissue there are no elastic fibres. Thereby, the diameter of the parabronchiallumen can be changed by the interaction of smooth muscle bundles and elastic fibres without altering the volume of the exchange tissue. From the outside of each atrium a few infundibula invade the parabronchial mantle, giving rise to a great number of air capillaries. These are air-filled tubes lined by a very thin epithelium and in their

Fig. 7. Scheme of the vascular system of paleopulmonal parabronchi. The inspired air (white arrows) flows through a mediodorsobronchus (above) into the parabronchi, where the gas exchange takes place. The end expiratory air leaves the parabronchi (below) via a medioventrobronchus (densely stippled arrows). The venous blood flows through the pulmonary artery (dark) to all levels of the parabronchus, the arterial blood mixed from all parabronchial levels leaves the lung through the pulmonary vein (light). (From Duncker 1974).

Respiratory system

507

Fig. 9. Three-dimensional drawing of the wall of a parabronchus. At the left, atria are seen, separated by thin septa, from which a few infundibula originate. At the right, one infundibulum in longitudinal section is shown, giving origin to numerous air capillaries which cross-link and interlace, making up a three-dimensional meshwork around the blood capillaries. (From Duncker 1974).

Fig. 8. Drawing of a parabronchus. On the left side: the atria with departing infundibula, which give off the air capillaries, making up a three-dimensional meshwork around the blood capillaries. On the right side: in the interparabronchial septa, arterioles (dense stippling) give off blood capillaries, which run toward the lumen where theycollect to venules (light stippling); the latter penetrate the parabronchial mantle into the interparabronchial veins. The septa of the atria and their smooth muscle bundles are supplied by a loose capillary network. (From Duncker 1974). rigid structure of the parabronchial mantle were a necessary precondition for the evolution of small tiny gas exchange structures, which have simultaneously allowed an enormous increase in the exchange surfaces. The vascular system. The pulmonary artery enters the lung hilus cranial to the primary bronchus. It ramifies between medioventro- and mediodorsobronchi among the parabronchi so that its branches reach all pans of the parabronchi by the shortest distances (Fig. 7). A long parabronchus, connecting the medioventro- to the mediodorsobronchi, is equally supplied over its entire length with arterioles . The numerous venules of a parabronchus are collected into branches of the pulmonary vein, which run in the neighbourhood of the branches of the pulmonary artery. The pulmonary vein leaves the lung hilus caudal to the primary bronchus . The parabronchi of the neopulmo receive their vascular supply from caudal branches of the pulmonary artery and vein; a large neopulmo receives a separate, lateral branch of both vessels (see also VASCULAR SYSTEM) .

Air sacs. Air sacs are large, extremely thin-walled extensions of bronchi, which expand beyond their penetration of the horizontal septum beneath the lung, filling the subpulmonal cavity or the dorsal peritoneal cavity. Their poor vascularization by the systemic circulation excludes panicipation in gas exchange and determines their function as bellows for ventilation. In the basic arrangement, a total of 9 air sacs exist, which can be separated into two functional groups : (I) the cranial air sacs, including the paired cervical, the unpaired clavicular and the paired cranial thoracic sacs (Figs. I, 3, 5), are all connected to the medioventrobronchi; (2) the caudal group of air sacs consists of the paired caudal thoracic and the

paired abdominal air sacs(Figs . 1,2,3,5). The latter are directly connected to the primary bronchus, which terminates in the abdominal air sac ostium . The caudal thoracic sac is connected to the large Iateroventrobronchus, and thus it is also connected to the caudal primary bronchus . The cranial group of air sacs occupies the space in the subpulmonal cavity in front of and lateral to the pericardium. The caudal thoracic air sac occupies the caudal pan of the subpulmonal cavity, whereas the abdominal sac invades the dorsal peritoneal cavity. An abdominal air sac located in the peritoneal cavity is lacking only in kiwis. Their air sac, in which the primary bronchus terminates, lies in the subpulmonal cavity as the most caudal one. The paired cervical air sac (Fig . 3) is connected by a branch to the first medioventrobronchus which penetrates the horizontal septum cranial to the lung hilus. The air sac extends cranially into the lower neck region, below the ventral neck musculature, adjacent and dorsal to the oesophagus. Lateral to the oesophagus the cervical air sac joins the dorsal part of the clavicular sac to form a separating membrane. By reduction of this membrane the cervical sac can fuse with the clavicular sac, as in turkeys or hummingbirds. The cervical air sac gives off pneumatic diverticula into the adjacent vertebral bodies, and a larger diverticulum between the rib cage and the cranial part of the scapula and the shoulder joint. The clavicular air sac (Fig. 3), unpaired due to the early fusion of embryonic paired sacs during development, is connected to both lungs by a short stern of the third medioventrobronchus, medial to the lung hilus, and via the ostium at the lung margin lateral to the hilus . It fills the most cranial part of the thoracic cavity in front of the pericardium and beneath the lung and bulges through the cranial thoracic apenure under the skin and muscles cranial to the thorax . The clavicular air sac expands laterally to the pericardium where it joins the cranial thoracic air sac to form a separating membrane. In a large number of families the clavicular air sac extends ventrally and caudally between the pericardium and the sternum, most often as a narrow diverticulum up to the middle of the sternum. However, in hummingbirds and song-birds the clavicular air sac extends up to the caudal margin of the sternum. In contrast to all other air sacs, the clavicular sac surrounds several structures, which run through the cranial thoracic apenure: the oesophagus, the trachea with syrinx and extrapulmonary primary bronchi, the tracheal muscles, the subclavian artery and parts of the brachial plexus . The carotid artery, the jugular vein, the accompanying endocrine glands, and the vagus nerve run in the membrane separating the clavicular and cervical air sacs. In addition to numerous diverticula for the pneumatization of the adjacent bones, the clavicular air sac gives off large diverticula between the scapula and the rib cage, and also into the axilla and around the shoulder joint. The paired cranial thoracic air sac (Fig. 3) is connected to the third medioventrobronchus medial to the lung hilus and to the ostium at the lung margin lateral to the hilus, very similar to the clavicular sac. This air sac is bordered dorsally by the horizontal septum and medially by the pericardia1 wall and the oblique septum, and laterally by the thoracic wall. Caudally, the air sac is separated from the caudal thoracic air sac by a membrane, which originates out of the joined walls of both air sacs. The cranial air sac in the majority of birds is smaller than the caudal thoracic sac, but in pigeons and galliform birds it is larger. An extreme situation

508 Respiratory system

arises in turkeys, in which the caudal thoracic air sac is lacking and the cranial thoracic air sac occupies the entire caudal subpulmonal cavity. In hummingbirds and song-birds the cranial thoracic air sac retains the original position, but is fused with the clavicular sac. In these species the cranial group of air sacs is represented by only one sac, which possesses all the ostia of the fused 5 sacs. The adjacent bones are supplied with pneumatic diverticula from this air sac, whether fused or not. The paired caudal thoracic air sac (Figs. 2,3, 5) is bordered dorsally by the caudal part of the horizontal septum, which contains the ostium of the lateroventrobronchus. Into this ostium the parabronchi of the neopulmo or its saccobronchus open laterally. Medially, the caudal thoracic sac is bordered by the oblique septum, laterally by the thoracic wall. The caudal extension of this air sac varies largely in different families and thereby also its volume. The caudal thoracic air sac is large in most birds, but relatively small in pigeons and galliform birds. In the turkey, the connections of the missing caudal thoracic air sac to the lateroventrobronchus and to the neopulmo are incorporated into the ostium of the abdominal air sac. The abdominal air sac (Figs. 2, 3, 5) is connected to the caudal primary bronchus, which at the caudal lung margin penetrates the united, dorsal, perpendicular portion of the horizontal and oblique septa and opens into the funnel-shaped air sac ostium. The abdominal air sac is the only one (with the exception of the kiwi) which is not situated in the subpulmonal cavity, but spreads out in the dorsal peritoneal cavity lateral to the dorsal mesentery. The air sac wall adheres to the dorsal body wall over a varying wide oval area, so that the cranial parts of the kidney and the testes are covered, but not the left ovary. From the margins of this area of adhesion the very thin walls of the abdominal air sac hang freely movable into the peritoneal cavity. The dimensions of the air sac walls are limited in penguins, ostriches and rheas, but in most other birds are so wide that the thin walls are regularly folded up between intestinal loops. Air sac diverticula protrude from the dorsal area of adhesion between kidney and synsacrum, into the synsacrum and the femur, and around the hip joint. The ostia of the air sacs and their connecting bronchi are to some extent structurally different. The ostia into the cranial air sacs are rigidly extended into the horizontal septum; the connecting medioventrobronchi are not able to vary their. diameter. The ostia into the caudal thoracic and abdominal air sacs are also rigidly extended into the horizontal septum or in the septum at the caudal lung margin. However, the connecting lateroventrobronchus and the terminal primary bronchus possess a well-developed circular musculature. In contrast to the medioventrobronchi, which are poor in musculature and rigidly stretched, these connecting bronchi can vary their diameter, and thus they may contribute to the regulation of air flow into and out of these air sacs. The ventilation of the lung is caused by the volume changes produced by the respiratory movements, which act only on the air sacs. The measured pressure changes are the same in all air sacs. During inspiration, fresh air flows directly through the primary bronchus and the large lateroventrobronchus into the caudal air sacs (Fig. 6a). In contrast, the cranial air sacs receive an inflow of air only via the richly interconnected medioventrobronchi. Thus, a pressure gradient to the mediodorsobronchi is developed, causing the air to flow from the primary bronchus through the mediodorsobronchi via the parabronchi and through the medioventrobronchi into the cranial air sacs. They therefore receive only expiratory air. During expiration, the air from the caudal air sacs is forced into the openings of the mediodorsobronchi, which are situated one above the other (Fig. 6b). This air flows through the parabronchi and through the medioventrobronchi, where it is joined by air from the cranial air sacs, leaving the lung through the primary bronchus. Thus, the air flows unidirectionally during inspiration and expiration through the paleopulmonal parabronchi (Scheid 1979, 1982) which is a consequence of the arrangement of the secondary bronchi and the orientation of their origins and their air sac connections. In contrast to this unidirectional ventilation of the paleopulmo, the neopulrnonal parabronchi are ventilated in directions altering with the respiratory phase, due to the fact that this parabronchial net lies in the direct connection between the primary bronchus and the caudal air sacs. The gas exchange in the long parabronchi, whether ventilated unidirectionally or otherwise, is physiologically unique and much more efficient than in mammalian alveoli. The venous blood perfuses equally all capillaries over the entire length of the parabronchus (Fig. 7). In the proximal portion of the parabronchus the blood exchanges with fresh air,

whereas in the more distal parts it exchanges with increasingly deoxygenated air, up to the terminal part of the parabronchus where the venous blood comes into equilibrium with the fully exchanged (end-expiratory) air. The gas content of the blood, varying in composition at the various parabronchial levels, has a lower CO 2 partial pressure than the endexpiratory air, and under hypoxic conditions, e.g. during flight at high altitudes (Scheid 1979, 1982), also has a higher O 2 partial pressure than the expired air. This so-called cross-current exchange system is responsible for the high physiological efficiency of the avian lung. Contrary to earlier belief, the movements of birds due to flight are totally independent of respiratory movements, and they do not even support respiration. The two activities are anatomically independent of each other. The large flight muscles originate solely from the broad sternum, the coracoid, the clavicula and their membranes, but not from the rib cage (the respiratory apparatus), from which the movements of the flight apparatus are isolated by loose connective tissue and air sac diverticula. The respiratory movements are produced only by the muscles of the ribs and their uncinate processes, which give them a more effective leverage, and by the muscles of the abdominal wall (Duncker 1971). The separation of flight and respiratory movements has been proven by recording wing beats and breaths, which are found in different relationships to one another, varying from 3: 2 to 5: 1 in most species investigated. Only in the crow Corvus and the pigeon a 1: 1 synchrony occurs (Berger and Hart 1974), which was the reason for the statement that flight and respiratory movements were coupled. Ontogenetic development. Because of its structural peculiarities the avian lung/air sac system requires special developmental conditions. At the beginning of the second half of the incubation period, the lung fuses with the walls of the pleural cavity. Only the air sacs, which develop at the same time, can be inflated in the embryo. A few days before the end of the incubation period, the lung is fully developed together with all secondary bronchi and parabronchi. At this time air capillaries sprout from the atria into the parabronchial wall between the developing blood capillaries. The parabronchi and their developing air capillaries are full of pulmonary fluid. One to three days before hatching, the embryo ingests the amniotic fluid and the rest of the albumen, and breaks the membrane to the air space inside the egg. At this time regular respiratory movements start, and the embryo breathes air, thereby starting ventilation of the lungs and air sacs, and also of the parabronchi. During this time the gas exchange of the embryo is carried out by the chorio-allantoic membrane, but after ventilation has started the pulmonary fluid gets resorbed from the developing air capillaries. Thus, the gas exchange is increasingly taken over by the growing blood--capillary/ air-capillary network, until at the end of this process, the embryo hatches. The air capillaries cannot be inflated because of their high surface tension and the rigid construction of the lung; moreover, they cannot suddenly be emptied of pulmonary fluid at the moment of birth. Therefore, birds require one to three days before hatching for their lungs to develop full functional status, during which time an overlap of the gas exchange process by the chorio-allantoic membrane and the air ventilation of the lungs occurs; this is only possible in a hard-shelled egg. Thus, the phylogenetic development of viviparity, which would have a number of biological benefits also for birds, was denied avian species by the structural peculiarities of their respiratory system (Duncker 1971, 1978) (see also DEVELOPMENT, EMBRYONIC). H.-R.D. Berger, M. & Hart, J.S. 1974. Physiology and energetics of flight. In Farner, D.S. & King, J.R. (eds.), Avian Biology, vol. 4. New York. Duncker, H.-R. 1971. The lung air sac system of birds. Ergebn. Anat. Entwickl.Gesch. 45, 6: 1-171. Duncker, H.-R. 1972. Structure of avian lungs. Respir. Physiol. 14: 44-63. Duncker, H.-R. 1974. Structure of the avian respiratory tract. Respir. Physiol. 22: 1-19. Duncker, H.-R. 1978. Development of the avian respiratory and circulatory systems. In Piiper, J. (ed.). Respiratory Function in Bird, Adult and Embryonic. Berlin. Duncker, H.-R. 1979. Coelomic cavities. In King, A.S. & McLelland, J. (eds.), Form and Function in Birds, vol. 1. London. Fedde, M.R., Burger, R.E. & Kitchell, R.L. 1964. Anatomic and electromyographic studies of the costopulmonary muscles in the cock. Poultry Sci. 43: 1177-1184. Menuam, B. & Richards, S.A. 1975. Observations on the sites of respiratory evaporation in fowl during thermal panting. Respir. Physiol. 25: 39-52. Scheid, P. 1979. Mechanism of gas exchange in bird lungs. Rev. Physiol. Biochem. Pharmacol. 86: 137-186. Scheid, P. 1982. Respiration and control of breathing. In Farner, D.S. & King,

Rhea

509

j.R, (eds.). Avian Biology, vol. 6. New York. Schmidt-Nielsen, K., Hainsworth, F.R. & Murrish, D.E. 1970. Counter-current heat exchange in the respiratory passages-Effect on water and heat balance. Respir. Physiol. 9: 263-276.

RESTLESSNESS, PRE-MIGRATORY: see PRE-MIGRATORY RESTLESSNESS.

RETICULATE: term applied to a podotheca consisting of small scales, the divisions between which form a fine network (see LEG). RETINA: part of the eye (see VISION). RETRAP: see MARKING;

TRAPPING.

REVERSE MIGRATION: a phenomenon in which birds fly in a direction opposite to that which they would be expected to take during a particular migration (see WEATHER AND BIRDS (Reverse migration)). RHABDORNITHIDAE: family Oscines; CREEPER, PHILIPPINE.

of

PASSERIFORMES,

suborder

RHACHIS: see RACHIS. RHAMPHOTHECA: the horny covering of the bill, the upper and lower parts of it being sometimes separately designated rhinotheca and gnathotheca (see BILL). Greater Rhea Rhea americana. (M.Y.)

RHEA: substantive name of the 2 species of Rheidae (Struthioniformes, suborder Rheae); in the plural, general term for the family. The group is restricted to the campo region of South America, where the birds are called 'Ema' or 'Nhandu' (Nandu). They are large running ratites, showing a general resemblance to the Ostrich Struthio camelus of Africa. The Ostrich, Cassowaries Casuarius, Emu Dromaius novaehollandiae and rheas are considered to be of monophyletic origin. Characteristics. The Greater Rhea (or Common Nandu) Rhea americana, to which the following account refers, stands about 1.5 m high and weighs 2~25 kg or more. The normal coloration is not conspicuous, but white individuals are not uncommon. The sexes are similar, but the males are slightly taller. Each foot has 3 well-formed toes, and the birds are fine runners. When alarmed they run with their necks stretched almost horizontally, and they can double at right angles to their course. At the same time they lift one of their wings, with a sail-like or ballooning effect. When there is enough cover they crouch down to conceal themselves. Although the wings are bigger in proportion than those of other ratites, they are useless for flying; they cover the upper part of the rump like a cloak when they are at rest. Unlike those of the Ostrich, the feathers have little commercial value; they are used in South America as dusters. Rectrices are absent. Rheas love to bathe and they are able to swim. Habitat. Generally the species prefers country with taller vegetation to pure grasslands, with the breeding territory near a swamp or river if possible. Distribution. Rhea americana is found from north-eastern Brazil to central Argentina. The other species, in a closely related genus, is Darwin's Rhea Pterocnemia pennata, occurring from Patagonia to the high plateaux of the Andes in southern Peru. It is somewhat smaller; the plumage shows white spots on a brownish background. Food. Rheas feed on tender leaves, roots, seeds, and the like, also eating many insects, especially grasshoppers, and small vertebrates. Behaviour and voice. The birds live in flocks; except in the breeding periods these groups consist of 2~30 individuals, at times considerably more. Occasionally they mix with herds of the Bush Deer Dorcelaphus bezoarticus, both species keeping a sharp look-out. In regions where they are not hunted they also mix with grazing cattle. Old male birds are solitary. At the beginning of the breeding period the older males chase away the young ones and fight with their rivals by twisting their necks together, biting, and kicking. The male displays in front of 3--8 females: he runs to and fro, stands in front of them, pulls his neck in, jerks his wings and then spreads them away from his body so that the feathers flutter in the breeze. He frequently lets out a kind of low roar which sounds more like the voice of some wild beast than of a bird. At the same time he stretches his neck straight upwards, the inflated oesophagus serving as a sounding

board. The Rhea also produces other sounds; the syrinx is better developed than in the Ostrich. Breeding. At a dry spot protected by bushes, the victorious male prepares a shallow hollow in the ground by ripping away the grass with his bill; frequently he uses an already existing depression and often works at a number of spots. Finally, he lines the hollow with some dry vegetable matter. Some of the nests are surrounded by an open zone partly prepared by the birds themselves biting off the grass; this zone occasionally serves to protect the nest against campo fires. The male then leads the females to the nest, showing his strikingly light-coloured rump. Frequently they have already started laying, dropping their eggs in various spots; but now they concentrate on the definite nest. It may happen that 6 females, one after another, each lay an egg in the nest and then leave together. Even females that belong to a different flock will join in and, consequently, the clutch may increase rapidly. Each female lays an egg every 2 or 3 days up to a total of 11-18. Otherwise they do not bother with the nest. After there are a certain number of eggs in the nest the male begins to incubate. From then on he defends the nest by stretching out his neck and moving it in a snake-like fashion accompanied by hissing and snapping. Females who want to lay more eggs in the nest must behave submissively to reduce the male's aggression before they are allowed to do so. More eggs are also laid in the vicinity; the male rolls into the nest, with his bill, those eggs nearest it. Depending on circumstances, the clutch is complete with from 13 to 2~30 eggs; but clutches with more than twice that number of eggs have been found (e.g. 80). The number of eggs which go to waste is even larger. The measurements of the eggs vary considerably, the average is about 132 x 90 rom; the weight of an egg is about 600 g. Newly laid eggs of Rhea americana are golden yellow, but this quickly fades to an off-white colour. The eggs of Pterocnemia pennata are green. After an incubation of 35-40 days by the male alone, the young hatch, one shortly after the other. They are grey with dark stripes. The young soon leave the nest, led by the male. They keep contact with each other by long-drawn plaintive whistles. Even so they get lost at times, especially when they lag too far behind after cowering low at the sign of danger. The strays will join another flock, if possible, and this results in considerable age variations within flocks. The development of the young is rapid; after 5 months they are already as big as the adult birds. Sexual maturity, however, is not reached for 2 years. H.S. Brunning, D.F. 1974. Social structure and reproductive behavior in the Greater Rhea. Living Bird 13: 251-294. Darwin, C. 1845. The Voyage of H.M.S. 'Beagle' (abbreviated title). London. Faust, R. & Faust, I. 1962. Beobachtungen iiber die Brutbiologie der Ratiten. I. Rhea americana. Zool. Garten 26: 163-175.

510

Rheae; Rheidae

~~:.. _... '", .....

Hudson, W.H. 1920. Birds of La Plata Vol. 2. London. Krieg, H. 1940. Als Zoologe in Steppen und Waldern Patagoniens. Miinchen.

RHEAE; RHEIDAE: suborder and family of

5

STRUTHIONIFORMES;

RHEA.

10

RHINOCRYPTIDAE: family of Oscines;

PASSERIFORMES,

suborder Deutero-

TAPACULO.

15

RHINOTHECA: term sometimes applied to the part of the rhamphotheca covering the upper jaw (see

BILL).

RHIPIDURIDAE: a family of

PASSERIFORMES,

-.. V) suborder Oscines;

FANTAIL.

~

§.

20 25

(J)

RHOMBOID SINUS: a structure in the avian spinal cord (see

E

~

30

NERVOUS SYSTEM).

RHYNCHOKINESIS: a form of upper jaw mobility seen in some

birds with schizorhinal nostrils, in which the flexible region has shifted rostrally, and bending occurs instead at various points along the length of the upper jaw (zonae elasticae maxillares) (see SKULL (Cranial kinesis)).

RHYNOCHETI; RHYNOCHETIDAE: see under

3S 1,0

I,S GRUIFORMES;

KAGU.

50

RHYTHMS AND TIME MEASUREMENT: processes which

recur at regular intervals in organisms or groups of organisms are commonly referred to as rhythms or periodicities. Four groups of biological periodicities constitute a special category in that their periods match natural environmental periodicities: tidal, daily, lunar and annual rhythms with periods of 12.4h, 24.0h, 29.5 days and 365 days, respectively. The 4 corresponding kinds of biological rhythms represent special adaptations which have evolved in many organisms to cope with the conspicuous temporal changes in the environment associated with the tides, the succession of day and night, the phases of the moon, and the cycle of the seasons. Since these environmental periodicities are highly stable and predictable, organisms have been able to evolve innate endogenous temporal programmes in physiology and behaviour, with the result that particular biological activities are performed at specific appropriate phases of the environmental cycles. In that respect biological rhythms often serve as clocks, i.e. time measuring systems that both couple temporal programmes of performance with environmental cycles and guarantee the appropriate sequence in the successive events of the programme. In birds, as in most other organisms, all physiological and behavioural processes are organized on the basis of a daily periodicity. Similarly, annual rhythms are common, at least in birds inhabiting the temperate and higher latitudes with their pronounced seasons. Overt tidal and lunar rhythms, on the other hand, are less widespread in birds, but in some species they serve a significant function; for some seabirds and waders that feed in the intertidal zone, a tidal rhythm is superimposed on the daily pattern of foraging activity. Lunar rhythms related to the variations in nocturnal light-intensity are sometimes found in the time of onset and end of activity in crepuscular birds such as the foraging flight of Nightjars Caprimulgus europaeus, the LEKS of Black Grouse Tetrao tetrix, and in the duration of nocturnal restlessness in migratory passerines. The breeding cycles of the Sooty Tern Sterna fuscata on Ascension Island and of 2 passerines on Borneo closely approximate 10 lunar cycles, suggesting that reproduction in these birds is somehow controlled by the phase of the moon. But, whereas endogenous tidal and lunar rhythms have been investigated in other organisms, nothing is known about the properties of such rhythms in birds. The following account is therefore restricted to daily and annual rhythms. Dally rhythms General features. Although daily rhythms in biological activities closely match the daily environmental cycles to which they are adapted, they are not usually caused by them. This is indicated by the persistence of daily biological rhythms in experimental conditions devoid of daily variations. The daily rhythm of perch-hopping in the Chaffinch Fringilla coelebs continues for many cycles even when the bird is maintained in continuous light and at constant temperature. During the first 12 days of the experiment shown in Fig. 1, the bird was exposed to a 24-h light-dark

Time (hours)

Fig. 1. Circadian rhythm in perch-hopping activity of a Chaffinch Fringilla coelebs. Each day's record is displayed below the record of the previous day. Black bars indicate intense activity. The bird was kept from day 1 through 12 (top box) in conditions of bright light from 2000h to 0800h (light area in the box) and dim light from 0800h (shaded area outside the box) each day. From day 13 onwards it was kept in continuous dim light until day 37 (bottom box) when it was exposed once again to alternating bright and dim light on a 24h light cycle. Note the persistence of the rhythm under constant conditions with a circadian period shorter than 24 h, and its entrainment by the light-dark cycle.

cycle, but when the light was kept on continuously, the times of onset of successive bouts of activity shifted progressively forward relative to local time, indicating a 'free-running' rhythm of activity and rest with a period shorter than 24 h. Such a deviation of the period from 24 h-usually not exceeding about ± 200/0 of 24 h-is characteristic of daily biological rhythms in constant conditions. This observation excludes the possibility that uncontrolled daily environmental cues might cause the rhythmicity in the animal and thus justifies the designation of these periodicities as 'circadian rhythms' (from circa = about and dies = day). Whereas circadian rhythms have a period slightly different from 24 h under constant conditions, their period is exactly 24 h under natural conditions. There must, therefore, be daily rhythmic factors in the animal's normal environment which are capable of synchronizing circadian rhythms with the natural day. Such environmental cycles capable of synchronizing (entraining) biological rhythms are called Zeitgebers. For birds, as for essentially all other organisms, the most important Zeitgeber of circadian rhythms is the 24-h rhythm in light-intensity, i.e. the alternation between day and night. In Fig. 1 the free-running activity rhythm of the Chaffinch in constant darkness is 'caught' by the lightdark cycle; the bird's natural free-running period is altered to the period of the Zeitgeber. Other Zeitgebers of avian circadian rhythms are 24-h temperature cycles of an amplitude greater than 30°C, and acoustical signals consisting of regular daily alternations between noise and silence. However, the effectiveness of these supplementary Zeitgebers is small compared with that of light-dark cycles. Since circadian rhythms persist without damping for many cycles in constant conditions they behave like self-sustaining oscillators in the technical sense. Therefore, the terminology of general oscillator theory is often used for describing them. They are innate: circadian locomotor activity rhythms develop even in chicks raised from the egg in constant darkness. Their period length T is relatively unaffected by environmental influences. It is particularly significant for the use of these rhythms as

Rhythms and time measurement

clocks that T shows little variation over a wide range of temperatures. This holds true for all sorts of organisms, including cold-blooded. A change in temperature of 10°C usually changes T predictably, but by less than 5%. For birds, an increase in environmental temperature usually leads to a slight shortening of T. Apart from temperature, light intensity has slight but consistent effects on T. In diurnal birds T usually shortens as light-intensity increases, whereas in nocturnal birds the reverse may be true, at least under high light intensities. In addition, physiological factors (e.g. reproductive state) may affect T. Within a single organism different biological functions are often controlled by different discrete circadian clocks. When, under constant environmental conditions, circadian rhythms are no longer synchronized, those of, e.g. body temperature and locomotor activity, may free-run with different TS. Even a single function may be under the control of more than one circadian oscillator. Thus, locomotor activity of birds kept in continuous dim light may, under certain conditions, 'split' into two components, the morning and evening peaks of activity, which separate and free-run with different periods. Under normal conditions of synchronization, however, the various circadian rhythms usually assume rather rigid phase-relationships to each other, ensuring that each circadian function occurs at the right phase of the environmental cycle and in the proper sequence relative to the other functions. Whereas a Zeitgeber of circadian rhythms is by definition capable of changing T so that it matches its own period T, the range of possible T-values to which circadian rhythms can entrain is limited: it extends from about 18h to about 30 h. Between these limits, the range of T-values within which entrainment occurs depends on the nature of the Zeitgeber cycles, its amplitude, and the natural period T« of the animal's circadian rhythm. As the Zeitgeber period increases or the natural period of the circadian rhythm decreases, the phase of the biological rhythm shifts forward relative to the phase of the Zeitgeber rhythm. The phase relationship (t/J) between the two rhythms is given by t/J --- T/ Tn' as predicted if entrained circadian rhythms were, to behave like selfsustaining oscillators under the influence of an external periodic driving force. Many aspects of circadian rhythms of animals under different Zeitgeber conditions are consistent with this relationship. For instance, it has been found that the circadian locomotor activity rhythm in many diurnal birds is relatively more phase-advanced in summer than in winter; the size of this seasonal difference increases with increasing latitude. Such changes are to be expected if the animal responds to the average light intensity it experiences in the course of a day, since this is higher in summer than in winter (and the extent of this seasonal difference is greater at higher latitudes). Since Tn of a diurnal bird shortens with increasing light-intensity but T does not change, one should expect higher t/J values in the synchronized state in summer. Hence, some of the systematic seasonal and latitudinal changes in t/J can be interpreted as a consequence of the seasonal and latitudinal changes in day length. It must be emphasized, however, that other variables such as the duration of twilight affect the activity pattern as well. Synchronization, in principle, is possible only if there is a periodically changing sensitivity of the circadian rhythm to stimuli from the Zeitgeber. This phenomenon has been explored in detail for the sensitivity of circadian rhythms to light. Light pulses and transitions from light to darkness or from darkness to light cause phase shifts of the circadian rhythm which are dependent in direction and amplitude on the phase of the rhythm hit by the light signal. This relationship is represented in so-called phase-response curves. On the assumption that light-pulses mimic the dark/light/dark transitions occurring during a natural day, phase-response curves can be used to predict the behaviour of circadian rhythms under various Zeitgeber conditions. This model of entrainment has proved successful in explaining the behaviour of avian circadian rhythms in, for instance, the Japanese Quail Coturnix japonica and the House Sparrow Passer domesticus. For these, the limits of the range of entrainment and the dependence of t/J on T or on photoperiod can be quantitatively derived from phase-response curves. Localization of circadian pacemakers. Although it is clear that in higher vertebrates there is a multitude of circadian rhythms occurring at various levels from the organ down to the cell, there is now equally good evidence that this circadian system is integrated by central circadian pacemakers. In at least some passerine birds such a pacemaker seems to be localized in the pineal gland. If House Sparrows held in constant darkness are pinealectomized, their free-running rhythms of locomotor activity and body temperature are almost instantaneously abolished. Rhythmicity is

511

restored, however, when the pineal of another sparrow is transplanted into the anterior chamber of an eye. The emerging rhythm has the phase of the rhythm of the donor bird. These results strongly suggest that the pineal is a circadian pacemaker, driving or integrating overt circadian rhythms, and that the information about circadian time is chemically transmitted to the subordinate system. Presumably melatonin, a hormone produced by the pineal, is the essential substance. In birds, as in other vertebrates, melatonin concentration shows a conspicuous daily rhythmicity with high values during the dark (inactive) and low values during the light (active) phase of each day. The synthesis of melatonin is controlled by the activity of the enzyme N-Acetyl-transferase which exhibits a strong daily (circadian) rhythm, persisting for at least two cycles in chickens kept in continuous darkness, and even in isolated chicken pineals cultured in vitro. Chronic melatonin treatment affects the free-running circadian activity rhythms in both sparrows and European Starlings Sturnus vulgaris. The highly disorganized circadian activity rhythms of pinealectomized Starlings kept in continuous dim light can be synchronized by daily injections of melatonin. All these facts, taken together, suggest that the pineal is the seat of a self-sustaining circadian oscillator, which controls overt circadian rhythms by its rhythmic output of melatonin. Whereas pinealectomy results in arhythmic activity in the House Sparrow, the White-crowned Sparrow Zonotrichia leucophrys and the White-throated Sparrow Z. albicollis, pinealectomy of European Starlings leads to impairment and instability but not complete abolition of the circadian rhythm of locomotor activity. In Japanese Quail and the chicken Gallusgallus, in contrast, pinealectomy has no profound effect on circadian activity rhythms. These interspecific differences may reflect differences in the degree of self-sustainment, not of the circadian oscillator in the pineal itself, but of a subordinate oscillatory system which is affected by the pineal output. If this subordinate system is comprised of a population of circadian oscillators, the different effects of pinealectomy in the different species might be due to differences in the mutual coupling among these oscillators. In the gallinaceous birds, coupling may be strong, so that even in the absence of the pineal driver a normal circadian rhythm persists, whereas in sparrows coupling may be weak, so that the rhythm deteriorates in the absence of the pineal pacemaker, with the Starling intermediate. Even in pinealectomized sparrows a residual rhythmicity can be observed, as their locomotor activity rhythms can still be synchronized by light as for normal birds: it takes the rhythm about a week to disappear if such birds are subsequently transferred to constant darkness. This observation can be interpreted in terms of an internal uncoupling of circadian suboscillators controlling locomotor activity. Another important part of the circadian system controlling locomotor activity is localized in the suprachiasmatic nuclei (SCN), in the anterior hypothalamus. In sparrows; their ablation has effects similar to pinealectomy. However, it is not clear yet how the pineal and the SCN interact, and how both of them eventually control the overt circadian functions. Photoreceptors for the entrainment by light. In birds, the eyes are not the most important photoreceptors involved in the perception of the lightsynchronizing circadian rhythms. Blinded House Sparrows can still entrain to 24-h light-dark cycles. However, the eyes are normally also involved, because after sparrows are blinded they require a greater minimum light intensity for synchronization to a 24-h light-dark cycle. The extraocular photoreceptors are located in the brain. This has been shown in experiments in which the entrainment response of normal sparrows to low-amplitude light-dark cycles was abolished by opaque material, placed on top of the bird's skull, which greatly reduces the light intensity reaching the brain. Conversely, the entrainment threshold can be lowered by plucking feathers from the head, thereby drastically increasing the light-intensity penetrating the skull. So far, the photoreceptors in the brain have not been identified. Adaptivefunctions of circadian rhythms. The selective forces, which have led to the evolution of endogenous circadian rhythms in all eukaryotic organisms, are still obscure. It is possible that their primary function early in evolutionary time was the maintenance of internal temporal order among various metabolic functions. This, indeed, may still be a major function of some modern circadian systems. However, it is clear that many organisms now utilize circadian rhythms for a variety of other purposes as well. Many physiological and behavioural functions follow endogenous daily programmes that match periodically recurring and therefore predictable environmental demands. For instance, feeding

512 Rhythms and time measurement

activity of many diurnal birds shows a bimodal pattern, with morning and evening peaks. The evening peak may be adaptive in that it enables a bird to store a surplus of energy for the coming night, whereas the morning peak may be a mechanism to make up for the deficiencies built up during the previous night of starvation. However, this daily pattern does not depend on the availability of or demand for food, since it persists in constant conditions with a circadian period, even if food is available ad libitum. One of the possible advantages of such preprogramming is that the complex biochemical and behavioural events related to food uptake and digestion can be temporally organized relative to each other, early enough that the organism is ready for feeding at the appropriate times of day. Anticipation of future demands is also a major function of both physiological and behavioural circadian rhythms. For example, body temperature begins to increase long before the daily onset of activity, so that the animal's metabolic state is already elevated when it becomes active. In diurnal birds that migrate at night, both normal day-time activity and nocturnal migratory unrest are under circadian control. The alternation between these two types of activity is accompanied by circadian changes in preferred light intensities in a gradient. European Robins Erithacus rubecula select high intensities during their daytime activities (such as feeding) but low intensities during their nocturnal activities (such as migratory calling). Obviously the naturally occurring variations in light intensity have become incorporated as an 'expectation' in the endogenous circadian organization of these birds. Circadian programmes are often highly flexible and subject to modification by individual experiences. In a sense, the circadian system provides a '24-h continuous loop tape recorder' on which the experiences of an individual animal at particular times of a day are stored. This ability is illustrated by the phenomenon of Zeitgedachtnis or time memory, first described for the honey bee but later also demonstrated for birds. Under experimental conditions bees can be trained to search for food at particular places at particular times of day; even if no longer rewarded, this temporal and spatial pattern persists for some days before it eventually becomes extinguished. Presumably, many of the daily habits that can be observed in free-living animals result from a similar circadian programming of learned behavioural functions based on some form of time memory. Circadian rhythms also provide the basis for special adaptations. One of these is 'time-compensated sun-compass orientation', first discovered in birds and bees by G. Kramer and K. von Frisch respectively. Birds tending to fly in a particular direction during migratory unrest, or searching for food in a direction to which they had been trained, compensate for the sun's apparent movement by continuously changing their orientation angle relative to the sun in such a way that a constant compass direction is maintained. That a circadian clock is involved can be demonstrated by experiments in which birds are exposed to artificial light-dark-cycles shifted relative to the natural day; this procedure resets the animals' circadian rhythms within several days. If then tested under the sun again, they select the compass direction predicted by the hypothesis that the birds relate the sun's position to subjective circadian time. This can be shown even more convincingly in experiments in which the circadian clock of birds is allowed to free-run under constant conditions, and by testing birds under an artificial stationary sun: each bird behaves as though the sun was moving and changes its orientation angle relative to it in the expected counter-clockwise direction (see NAVIGATION).

Many seasonal events are controlled by the annual variations in photoperiod, the light fraction of the 24-h day. The stimulatory effect of long photoperiods on the development of avian reproductive systems has been extensively investigated. If temperate-zone birds are exposed in winter to a long photoperiod simulating spring or summer conditions, the pituitary begins to secrete gonadotrophins which in turn initiate gonadal recrudescence. Neither the duration of light time nor the duration of dark time is important; the release of this response depends only on the phase of the animal's circadian rhythm which is exposed to light. If birds are exposed to a short non-stimulatory light period, followed by an extended (more than 24 h) dark period, which is then interrupted by another short light period (given at different times in different experimental groups of birds), their responses are usually a function of the circadian phase hit by the second light period, as shown in Fig. 2. Light periods with maximal effects and those with minimal effects on release of luteinizing hormone from the pituitary of White-crowned Sparrows are spaced approximately 24 h apart; the pattern of response is a circadian

o

24

Time (hours)

48

after last

72

real

dawn

96

Fig. 2. The effect of an 8 h light period given at various intervals after beginning of darkness on plasma luteinizing hormone concentration in White-crowned Sparrows Zonotrichia leucophrys. The whiteand blackbars at the top illustrate the various treatments. (White= period of light, black= period of darkness). Birds were previously maintained on 8h of light per day and a pre-experimental bloodsample wastaken for all birds earlyin the last 8h light period. The post-experimental sample wastaken 7-16h after the end of the test photoperiod. The ordinateshows the change in hormone concentration between these two samples that resulted from a particular treatment. (From Follett et al 1974). rhythm itself. These results are consistent with the hypothesis proposed in 1936 by E. Bunning, according to which organisms are equipped with a circadian rhythm in photosensitivity which measures day-length by determining whether or not light falls on a particular photo-inductive phase of that rhythm. Details of this circadian time-measuring process are still unknown but there is now compelling evidence that a circadian rhythmicity is involved somehow, not only in mediating the gonadal growth response to long days, but also in other seasonal activities such as migratory behaviour, moult and gonadal recrudescence (see ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM; MIGRATION; MOULT).

Annual rhythms

General features. Like daily rhythms some annual biological periodi-

cities are endogenously pre-programmed as circannual rhythms. Figure 3 demonstrates that annual variations in testicular width persisted in European Starlings maintained for 3 1/ 2 years under constant photoperiodic conditions. Periods of increased testicular size alternated regularly with periods of moult. The interval between successive corresponding events deviated from one year, indicating that these rhythms are not driven by uncontrolled annual environmental cues. Circannual rhythms persisting for at least two cycles, with periods deviating from 12 months, have been demonstrated for at least 15 avian species. Functions shown to be under circannual control are gonadal activity, migratory disposition, moult, feeding and body weight. In Garden Warblers Sylvia borin and Blackcaps S. atricapilla up to 9 successive circannual moult cycles have been measured under constant photoperiodic conditions, suggesting that in these species a circannual clock keeps running throughout the entire lifetime. In some species, however, circannual rhythms tend to damp out with time; and yet others show no annual rhythmicity at all if kept under seasonally constant conditions. This suggests that circannual rhythms are not as ubiquitous

Ringdove

513

N

as circadian rhythms, and represent special mechanisms that have evolved in only a few species, for special purposes. Circannual rhythms behave in many respects like circadian rhythms. There is evidence that they are innate. Their period in constant conditions seems to be relatively insensitive to environmental variables such as the actual duration of the constant photoperiod. And some results suggest that different functions may be controlled by different circannual clocks. Like circadian rhythms, they can be synchronized by cyclic variations in environmental conditions. In birds, the annual cycle in photoperiod constitutes such a circannual Zeitgeber; the period of the circannual rhythm can be altered by compressing the period of the normal annual change in photoperiod into less than 12 months. Using this technique in the European Starling, up to 8 cycles in testicular size and moult can be squeezed into one calendar year, indicating that the range of entrainment of these circannual rhythms is large compared to that of circadian rhythms. Adaptive functions of circannual rhythms. Since circannual rhythms, in contrast to circadian rhythms, appear to be restricted to certain species, it appears likely that they have evolved independently several times to serve specific biological functions. In migratory birds, one such function may be the timing of seasonal events at those times of year when reliable seasonal timing cues are not available. Circannual rhythms appear to be most strongly involved in the control of migratory disposition and moult in equatorial migrants that live for about 6 months each year in a tropical environment where seasonal environmental changes are absent or highly variable. However, they also occur in some short-distance migrants and even in entirely resident species such as the Crested Tit Parus cristatus. In migrants, timing of seasonal activities is not the only function of circannual rhythms. Nocturnal migratory restlessness of caged first-year warblers shows a seasonal pattern similar to the changes in average migratory speed of free-living conspecifics during their actual migration. Moreover, when warblers of various species, which normally migrate over different distances, are maintained in cages, corresponding differences are found in the duration and amount of migratory restlessness. These differences are related to the distance normally covered by the birds on their actual migration: the longer the distance between breeding grounds and winter quarters, the greater the intensity of autumnal migratory restlessness observed in the caged birds. These results suggest that the time course and distance normally covered by these warblers during their first autumn migration may be controlled, atleast in part, by a circannual programme determining the seasonal time course and total intensity of migratory unrest and, hence, that a circannual clock may be part of these birds' navigational system. Even the directional component of migration appears to be affected by Starling

August / September n=51

E

E

N

5 April /June n=120

E

W

October I December n=75

Fig. 4. Spontaneous seasonal changes of directional preferences in Garden Warblers Sylvia borin during nocturnal migratory restlessness. Garden Warblers were kept throughout the experiment under a constant 12: 12 hour light-dark cycle and tested repeatedly in circular orientation cages. The birds had no view of the sky but were exposed to the natural earth's magnetic field. The three circular diagrams summarize the results obtained in August and September (upper left), in October through December (lower left) and in April through June (right diagram) of the following year. The data are plotted on a relative scale such that the radius equals the greatest amount of activity in anyone 15° sector. The large arrows at the periphery of the diagrams show the direction of the mean vector calculated for each test series. Numbers in the diagrams refer to the number of tests. The map in the centre shows schematically the changes in migratory direction known to occur in Garden Warblers in the wild in the course of the year (After Gwinner & Wiltschko 1978, 1980).

a circannual rhythm. If Garden Warblers are maintained under a constant 12-h-photoperiod and tested repeatedly in orientation cages for directional tendencies of their nocturnal migratory unrest, they show changes in their directional preferences corresponding to the changes in migratory direction of free-living conspecifics (Fig. 4). This suggests that the shifts in migratory direction occurring in these birds along their way to and from their winter quarters may not be controlled primarily by exogenous cues but rather be the result of spontaneous circannual changes in the birds' internal physiological state. E.G.

o

Aschoff, J. (ed.). 1981. Handbook of Behavioral Neurobiology, vol. 5. New York. Gwinner, E. 1975. Circadian and Circannual rhythms in birds. In Farner, D.S. & King, J.R. (eds.). Avian Biology, vol. 5. New York. Menaker, M. (ed.). 1971. Biochronometry. Washington, D.C. Pengelley, E.T. (ed.). 1974. Circannual Clocks. New York. Saunders, D.S. 1977. An Introduction to Biological Rhythms. Glasgow.

~ o ~ RICE BIRD: alternative name for the Bobolink Dolichonyx oryzivorus ~

2

(see ORIOLE

(2».

RICHMONDENINAE: see EMBERIZIDAE;

CARDINAL-GROSBEAK.

RICTAL: pertaining to the gape; often applied to bristles in that area. RIDING: young on parents' backs, see CARRYING. A

J

A

0

D

F

Time of year (months) Fig. 3. Left: Variations in testicular width (curves) and occurrence of moult (black bars) of 6 European Starlings Sturnus vulgaris kept for 43 months under an 11: 11 (upper three) or a 12: 12 (lower three) hour light-dark cycle. Right: Symbols connected by lines indicate dates at which the same birds began to moult in the successive years of the experiment. Note the persistence of the rhythms under these seasonally constant conditions and the deviation of the period of the rhythms from year to year. (After Gwinner 1981).

RIFLE-BIRD: substantive name of species of Ptiloris (see

BIRD-OF-

PARADISE).

RIFLEMAN: Acanthisuta chloris (see under WREN

(3).

RINGDOVE (or RINGED DOVE): name (also 'Ring-dove', 'Ring Dove') applied to the so-called Streptopelia 'risoria', a domesticated variety of one of the subspecies of S. decaocto; liable to confusion with 'Ring Dove' (etc.) used as an alternative name for the Wood-pigeon Columba palumbus (see PIGEON).

514 Ringing

RINGING: see MARKING. RINGNECK: substantive name sometimes used for the 2 Australian parrots of the genus Bamardius; not to be confused with Ringneck(ed) Parakeet , sometimes used for Rose-ringed Parakeet Psittacula krameri (see PARROT) . RING OUZEL: Turdus torquatus, a western Palearctic mainly montane distribution.

THRU SH

of

RING-SPECIES: term (for which R. Meinertzhagen has alternatively suggested 'rejungent species') expressing the concept that a species may differentiate into a graded series of geographical forms and that extreme members of the series may later come into direct contact, through range expansion, and then prove to be so different from each other as to behave as separate species; this occurs in that fraction of the total range in which both forms are found, whereas elsewhere (the long way round the ring, so to speak) they remain connected by intermediate forms. In such a case, when the extreme forms are recognized as separate species, the allocation of intermediates as subspecies of one or the other becomes somewhat arbitrary. Examples are to be found in Parus major/minor, Lanius schach/ tephronotus, Pycnonotus barbatus]tricolor/ capensis, Acrocephalus arundinaceus/ stentoreus, Apus apus]pallidus, Merops superciliosus/ philippinus and Larus argentatuslfuscus. See also ISOLATING MECHANISM; SPECIATION ; SPECIES; SUBSPECIES.

RITUALIZATION: the evolutionary process responsible for the origin of displays and for the changes which occur in these to make them more effective in evoking the appropriate behaviour in the partner (see DISPLAY) . For example, displacement preening movements have been incorporated into the male courtship display of ducks (see DISPLACEMENT ACTIVITY) : in some species they have been reduced so that they can no longer make any contribution to feather care, and instead simply draw attention to features such as the 'sail' of the Mandarin drake Aix galericulata . The formal pointing movement , made more conspicuous by this enlarged feather ('morphological enhancement ' of the display) serves purely to influence the behaviour of others. Ritualization also plays a role in the evolution of inter-specific signals, such as the 'broken wing' display of certain waders, which serves to draw predators away from the nest or chicks (see DISTRACTION BEHAVIOUR) . This article concentrates on the ritualization of visual displays; similar principles apply to the evolution of auditory signals. Explanation of this process requires description of the various types of change which are found to occur during the evolution of displays, and the analysis of the reasons for them and of the mechanisms involved. The functional analysis of the changes involves two distinct problems. Where a display modifies the behaviour of a member of a different species (as in anti-predator displays) so that the interests of the partners in the interaction are opposed, the evolutionary changes must make the display better able to tap a pre-existing responsiveness in the partner. For instance, the eyespot displays of certain moths tap an avoidance response in small birds which must be of benefit to these birds in interactions with predators . Here, selection must fit the display to a feature-detecting mechanism which is maintained by independent selective forces. In contrast, when displays operate within a species, or between species that compete for resources, it is not always obvious what selective forces determine the pattern of responsiveness of the reacting individuals . One possibility is illustrated by aggressive displays. These operate in some instances to allow opponents to assess their chances of success in combat with the rival, and in this case the reactor should respond to cues which provide reliable information about the rival's fighting ability. The selection acting on the display, enhancing the apparent potential of the displaying animal, will be opposed by selection on the reactor , making it unresponsive to bluff. An alternative possibility is illustrated by parentoffspring interactions where the interests of parent and offspring are in harmony. Here , the responsiveness of the reactor to signals may be constrained by general features of its perceptual system, and the fact that signals must be detected against a particular background . Within these general constraints, any appropriate changes in the responsiveness alone, or the signal alone, or changes in both together (providing they were compatible) might benefit the partners. In this situation we have no idea what factors determine which change, or combination of changes, will occur.

Black -headed Heron A rdea melanocephala greet ing display at nest , (P hoto:

J . Taylor). The types of change that have occurred in displays over the course of evolution are well known as a result of 'comparative ethology'. Comparison of the behaviour of many species from a family or smaller taxonomic group allows us to infer the origin of many of the components of their displays, and the way in which they have evolved. For example, in the Estrildid finches, males of many species carry a grass-stem in their bill during courtship. This originated as an element of nest-building behaviour, and in the Red-browed Finch Aegintha temporalis the stem is carried throughout courtship and copulation , and may subsequentl y be built into the nest. In other species, which drop it before copulation, it becomes symbolic rather than functional behaviour , and in the Crimson Finch Neochmia phaeton it is entirel y symbolic in nature , since the type of stem chosen for the courtsh ip dance is different from the material chosen for nest building. Among the other groups which have received particularly intensive comparative study are the gulls, gannets and boobies, weavers, ducks, finches and buntings. Comparative work has shown that displays arise from a variety of sources: intention movements of locomotion, attack or escape and nest building; displacement activities such as preening or feeding; and autonomic responses such as feather raising. Ritualization has produced changes in the speed of performance of motor patterns, the omission or differential exaggeration of components or other changes in their detailed co-ordination , and the development of rhythmic repetition of elements. Displays may also evolve a 'typical inten sity' rather than vary in intensity with the underl ying motivation . Associated with these changes may be the development of morphological structures which emphasize the displays. Since the changes are all of the sort which make the display conspicuous to the human observer, it seems likely that they increase its conspicuousness to the reactor , but there is little direct information on this point. Hailman 's (1977) demonstration, that the winter plumage colours of bay and sea ducks (Aythyinae) fit the particular requirements for signals visible against the background of the water surface, shows what can be done for the static colour-badges which enhance displays,

Roa

but there is no equivalent work on the properties required for conspicuousness in the actions themselves. Often, ritualization increases the appearance of formality in an action (leading ultimately to such elaborate behaviour as the courtship dance of the Great Crested Grebe Podiceps cristatus). In some cases (for example, the 'strut display' of the Sage Grouse Centrocercus urophasianus) the display has become highly stereotyped, but not all displays are as stereotyped as was once believed. Detailed film analysis of a few displays has revealed unsuspected variation in the presence or intensity of elements, so that earlier descriptions of these as unitary displays involved oversimplification: this fine variation was related to the stimulus situation and the motivation of the displaying animal. While the displays in question came from the lower vertebrates, analogous examples in birds may include the 'song spread' display of the Carib Grackle Quiscalus lugubris (in which independent variation of beak and wing elevation is related to the sex of the partner), and also the 'upright facing away' display of the Laughing Gull Larus atricilla (in which two forms of the display, differing in whether the brown hood is hidden from the partner, are used differentially in sexual and aggressive contexts) . Use of film and videotape should make possible a more thorough analysis of ritualized displays than was possible with the eye alone, but the underlying problem is one of pattern-recognition, and cannot be solved by simple measurement . However, it is clear that the appearance of formality in many ritualized displays need not be synonymous with their stereotyp y. A more dramatic change which has sometimes occurred as a result of ritualization is the transfer of signal function from one structure to another. The Greater Bowerbird Chlamydera nuchalis presents a conspicuous patch on the back of its head to the female as it manipulates the objects in its bower, and the objects themselves play little part in its display. But in the Fawn-breasted Bowerbird C. cerviniventris, the head-patch has been lost (although the movements for its presentation remain) and presentation to the female of the objects in the bower plays a much more important role in the display. With the transfer of display function to the bower, this species has been able to respond to predation pressure by losing the conspicuous male plumage, so that male and female are alike. This example illustrates the point that even when used for communication within a species, ritualization must involve response to several selection pressures : predation pressure will limit the evolution of conspicuous displays and unwieldy ornaments; selection for interspecific divergence may occur where closely-related species occupy the same habitat and, within the species, there may be selection for contrast between two displays (for example, aggressive and appeasement displays are often antitheses of one another). The habitat will influence the types of action available as a starting point for ritualization (for example, the importance of bathing and cleaning movements in duck displays can be understood in the context of their aquatic display), and constraints arising from existing displays will also influence the direction of future evolution. For example, the symbolic carriage of nest material in estrildid courtship displays is a modification of earlier displays in which the material was functional.

Black-headed Gulls Larus ridibundus greeting display. (P hoto: H . Schouten ).

515

Blue-footed Booby Sula nebouxii greeting display. (P hoto: F . Polking ).

It has been argued that the further evolution of a display is also constrained by its underlying motivation : for example, that selection will act by changing the strength of aggressive or fearful tendencies underlying a threat or courtship display rather than modify the display as a unit . (T his interpretation is based on the 'conflict hypothesis' of display; see AMBIVALENCE. ) But we know much less about the evolutionary changes in the motivation of displays than about changes in their form, and the possibility that phylogeny constrains displays in this way should not lead to the neglect of current selective forces which might be responsible for the constraints . The conflict hypothesis makes sense of the phylogeny of many displays, but it is not yet certain that, in its present form, it provides the best interpretation of their causation; and the possibility that during the course of evolution the elements of displays have become divorced from their original motivation (the process of 'emancipation') must also be considered . There is little direct evidence on these points, and statements about the motivational changes underlying ritualization must still be considered tentative. P.G .C. Barlow, G.W. 1977. Modal action patterns. In Sebeok, T.A. (00.). How Animals Communicate. Bloomington. Beer, C.G. 1975. Multiple functions and gull displays. In Baerends, G.P., Beer, C.G. & Manning, A. (OOs.). Function and Evolution in Behaviour. Oxford. Blest, A.D. 1%3. The concept ofritualisation.lnThorpe, W.H. & Zangwill, O.L. (eds.). Current Problems in Animal Behaviour. Cambridge. Dawkins, R. & Krebs,I.R. 1978. Animal signals: information or manipulation? In Krebs, I .R. & Davies, N.B. (OOs.). Behavioural Ecology. Oxford. Haihnan, I.P. 1977. Optical Signals. Bloomington. Huxley, J.S. 'I al. 1966. A discussion on ritualisation of behaviour in animals and man. Phil. Trans. Roy. Soc. Lond., B, 251: 249-524 . ROA: former Maori name for a bird that may have been Apteryx haasti,

516 Roadrunner

as some authorities have concluded, or possibly a late surviving species of Dinornithiformes (see MOA).

ROADRUNNER: substantive name of Geococcyx spp. (see CUCKOO). ROATELO: in the plural ('roatelos'), alternative general term for the Mesitornithidae (see MESITE). ROBIN: commonest name in Britain today for Erithacus rubecula, the more formal alternative 'Red-breast' having become an almost pedantic usage. From this original source, the name has been transplanted to other parts of the English-speaking world and attached to local species actually or supposedly resembling the prototype, in being red-breasted or in other ways. Thus, in North America it is applied to the familiar Turdus migratonus, a larger but also red-breasted bird; and the Indian Robin Saxicoloides fulicata is a chat with chestnut underparts. It has also been used by ornithologists in fabricating English names for foreign species of Turdinae, either as a simple substantive name or in compounds such as 'magpie-robin', 'scrub-robin', 'bush-robin', and 'robin-chat' (see under THRUSH; also CHAT; SCRUB-ROBIN). Outside the Turdinae, 'robin' is the substantive name used in the Australasian Region for various Muscicapinae, some of them with red breasts, e.g. Petroica spp. in Australia and New Zealand; and in Australia for certain Pachycephalinae, e.g. Eopsaltria spp. (see THICKHEAD). And it is an avicultural name ('Pekin Robin') for Leiothrix lutea (see BABBLER). Further, 'robin' is misapplied in some quite unrelated groups, e.g. as a popular misnomer for the Jamaican Tody Todus todus, a small, dumpy, red-breasted bird (see TODY). See photos BILL ABNORMALITIES; COMFORT BEHAVIOUR; VOCALIZATION. ROC: see FABULOUS BIRDS. ROCKET NET: see

TRAPPING.

ROCKFOWL: substantive name of Picathartes spp. (see BABBLER). ROCKJUMPER: substantive name of Sphenoeacus pycnopygius, a warbler confined to arid rocky areas in south-western Africa (for family see WARBLER (1». RODENT RUN: see

DISTRACTION BEHAVIOUR.

RODING: the territorial or patrolling flight of male birds (from the Anglo-Saxon 'rode', meaning to raid). The term is usually applied only to the characteristic twilight display flights performed by male Eurasian Woodcock Scolopax rusticola during the period February-July (in Britain). When roding, woodcock fly above the woodland canopy with a distinctive, deliberate wing action, uttering every few seconds a series of croaks followed immediately by a far-carrying squeak. Research with radio-tagged birds suggests that roding woodcock are not defending exclusive territories but are searching for females with which to mate. Males are successively polygynous and differ significantly in their success at locating and mating with females, but unlike other waders with polygynous mating behaviour, they do not defend either an exclusive or specific area to which females are attracted and in which mating and/or nesting takes place. Instead the male displays solitarily over an extensive area (sometimes more than IOOha in extent) until called down by a receptive female. Then, probably to ensure that he alone copulates with her, he remains with the female constantly, close to the nest site, until the eggs are laid, before resuming display flights. G.J .M.H. ROLLER: substantive name of the 11 species of the family Coraciidae (Coraciiformes, suborder Coracii); see also GROUND-ROLLER and CUCKooROLLER. Rollers comprise 2 genera of Old World, essentially paleotropical, insectivores; species of Coracias are sit-and-wait predators searching from tree perches for large arthropods on the ground, and species of Eurystomus hawk insects in flight and are markedly crepuscular. Characteristics. The head is large, the neck short, the legs rather short and syndactylous feet small but robust. In Coracias the beak is crowlike-strong, arched and hook-tipped, and in Eurystomus (the broadbilled rollers) it is short and wide. Flight is strong and the wings quite

Lilac-breasted Roller Coracias caudata, (N.A.).

large. The tail is narrow and of medium length, and several species have elongated outer rectrices. Rollers are handsome birds with strong but muted colours, mainly dark blue and azure, with olive, chestnut and pink in Coracias and lilac and cinnamon in Eurystomus. The sexes are alike and juveniles resemble adults. Rollers get their name from their impressive courtship flight, a fast, shallow dive from considerable elevation with a rolling or fast rocking motion, accompanied by loud raucous calls. Whether they actually somersault as has been claimed needs confirmation. Most are aggressive and readily fly at people and raptors, using the same rolling action. All are arboreal, and when Coracias species land on the ground in pursuit of their prey they may use a clumsy hop. Systematics and distribution. Relationships among the coraciiform families remain controversial. There is good evidence that rollers have close affinity with the ground-roller (Brachypteraciidae) and less close affinity with the cuckoo-roller (Leptosomatidae) (both of Madagascar). Studies of anatomy, behaviour, ectoparasites, pterylosis and egg proteins suggest some affinity of rollers with bee-eaters and, decreasingly, with motmots, kingfishers and todies, hoopoes and hornbills. Within the Coraciidae relationships are easier to discern (Fry 1978). Coracias comprises 8 species and systematically they fall into two groups and an isolated species. The first group are 3 large (length 33-38 em, excluding long tail-streamers), olive-backed, full-tailed rollers: C. benghalensis of southern Asia, and C. naetna of African savannas and C. temminckii of Sulawesi, both of which seem to be derivatives of C. benghalensis. The second group are 4 lightly-built species (length range c. 28-30 em) with brown backs and narrow tails: C. garrulus of the western Palearctic, its allospecies C. abyssinica of the northern tropical woodlands of Africa, the east and southern African C. caudate whose range borders with C. abyssinica along the Rift Valley, and C. spatulata, which is restricted to mopane and Brachystegia woodlands of southcentral Africa and is broadly sympatric with C. caudata. All 3 African birds in this group have long outer tail feathers, racqueted in C. spatulate. The isolated roller is C. cyanogaster, a small azure and dark blue bird of the I soberlinia woodlands north of the African equatorial rainforests, with whitish hood, black back, and short tail streamers. In the genus Eurystomus (length 27-30 em) there are 3 species, and they resemble Coracias rollers in their raucous voices, rolling display flights, aggressiveness, and also somewhat in plumage. They hawk insects from elevated perches and have a strong, buoyant flight on rather long wings-feeding at dusk they resemble hawks or nightjars. Beaks are short, strong and very wide, and the tail is narrow and short, without streamers. E. glaucurus is widespread in sub-Saharan Africa and in Madagascar, a migratory woodland bird having rich brown plumage, violaceous below, with purple primaries and light blue in the tail. E. gularis of the African rainforest zone is very similar, and both have bright yellow beaks. E. orientalis is larger, dusky blue with scarlet beak and legs, and is distributed in 11 races from New South Wales to Nepal and

Roosting

through China north to SooN on the lower Amur R.; a white patch showing conspicuously in flight gives it the name Dollar-bird. Distribution, habitat and movements. The habitat is varied tropical woodlands and all types of open country from thornveld in South Africa to parks, cultivated fields and suburban gardens in the tropics, grassy hillsides with scattered trees, plains, scrubland and forests in Europe, Asia and Australia. Rollers breed from about 600 N in the west Palearctic and SooN in the east, south to about 300S in Africa and 35°Sin Australia, being absent only from desert regions and from central and north-west Europe. Most species are migratory, and move by day. From Europe and south-west Asia C. garrulus migrates to winter, exclusively, in open country from tropical Africa to the Cape. Madagascan E. glaucurus winter in south-east Africa. High-latitude populations of E. orientalis migrate towards the Equator and the species winters in India, south-east Asiaand Indonesia between the Tropic of Cancer and Java and New Guinea. Food. Coracias: large arthropods taken on the ground-mainly beetles (930/0) in Asia, and grasshoppers and crickets (270/0) and ants and termites (40%) in Mrica; also mantises, bugs, cockroaches, centipedes and scorpions. Rarely slugs, frogs, small lizards and birds; also grapes, figs and other small fruits. EuryslomUS: insects taken in flight, mainly beetles in Asia and ants and termites (80-950/0) in Africa. Occasionallythey take prey from trees or the ground-s-molluscs, centipedes, spiders, small frogs and fruits (Thiollay 1971). Behaviour and voice. In monogamous pairs for most of year and family parties after breeding; but C. naeoia is reportedly more gregarious. Somerollers form small looseflocksduring migration; Eurystomus also congregates to feed at a hatch of flying termites. Otherwise, rollers are strongly territorial when breeding, and probably also on their wintering grounds. The voice is a harsh, guttural aaa-aaaaa, repeated in a frenzied staccato during courtship flights. Birds call periodically several times an hour, perched or flying, often in response to each other. Intense calls are accompanied by a lively bowing. Breeding. Rollers nest in holes in trees and bamboos, in hollow stumps, old walls, cliffsand mud-banks; feathers or a few chips of rotting wood may be added as nest-lining. Eggs are glossy white, subspherical; 4 is the commonest clutch at both low and high latitudes. Both sexes incubate and feed the young. The incubation period is 17-19 days (data for 3 species only); the nestling period is not known but is not less than C.R.F. 20 days. Cracraft, J. 1971. The relationships and evolution of the rollers: families Coraciidae, Brachypteraciidae, and Leptosomatidae. Auk 88: 723-752. Fry, C.H. (In press). Rollers. In Fry,C.H., Keith, S.K. & Urban, E.K. (eds). The Birds of Africa, voL III. London. Thiollay, J.-M. 1971. Les guepiers et rolliers d'une zone de contact savane-foret en Cote d'Ivoire. L'Oiseau et R.F.O., 41: 148-162.

ROLLER CANARY: see CAGE BIRD. ROOK: Corvusfrugilegus (see CROW

(1)).

ROOKERY: primarily a nesting colony of Rooks Corous frugilegus; but applied to colonies of some other birds, including penguins (Spheniscidae). ROOKOOING: the production of a bubbling sound by the male Black Grouse Tetrao tetrix at the LEK. ROOSTING: derived from an old German word meaning 'a sleeping house for fowls', the term has often been used synonymously with SLEEPING, but while roosting birds usually sleep, at other times they simply rest. Roosting also includes the act of going to or taking up a roost, i.e. travelling, gathering and establishment of site. Roosting has also been confused with 'loafing' (Amlaner and Ball 1983), a term stemming from a German word for tramp or vagabond, and meaning 'to spend time idly'. In contrast to loafing, the main purpose of roosting is for sleep. Loafing also includes activities involved in COMFORT BEHAVIOUR and digestion. Although loafing flocks almost inevitably include sleeping birds, they do not always form for sleeping, and hence are not always roosting flocks. Birds may loaf at any time of day or night, singly or communally, between periods of any sort of activity, notably feeding. As in roosting, birds may use habitual loafing sites, and resort to them from some distance. Some categories of birds, e.g. immatures, non-breeders and off-duty breeders, may loaf at times

517

when other birds are occupied with parental duties (see CLUB). The off-duty bird may also loaf at the nest-site, while its mate may loaf whilst sitting on the nest itself. In general, the use of the term loafing should be encouraged wherever quiescent behaviour does not have a strictly roosting function (N.J. Ball). Several recent papers discuss the functions of communal roosts, and observations on particular species are scattered throughout the literature; for reviews see Ydenberg and Priss (1981), Amlaner and Ball (1983). Roosting habits of Western Palearctic species are summarized in Cramp and Simmons (1977 et seq.). Most recent papers dealing especially with roosting refer to timing, thermal benefits and shelter, censusing, and pest control. Times of roosting. The times of day when birds roost are adapted to their other activities, especiallyfeeding. Unless sick, birds generally roost only when there is nothing more important to do, such as feeding or defending a territory, or when temporary (weather) conditions preclude their normal activity. Most species accordingly roost at night, although night feeding species roost during the day. Waders (Charadrii) and wildfowl feeding in the inter-tidal zones may, depending on the state of the tide, roost either during the day or at night, as they feed largely by touch and can find food in the dark. Other species are known to feed nocturnally, for example, swans (on submerged vegetation), some diving ducks (e.g. Pochard Aythya ferina) and Sooty Terns Sterna fuscata. Tits (Parus spp.), have been observed feeding by the light of street lamps. Birds roost for a shorter time in summer than in winter, but even in the continuous daylight of high latitude summers they spend periods asleep, some species sleeping sporadically throughout the 24 hours, but others at a particular time, usually around midnight (see SLEEP). Precise timing. As times of sunrise and sunset change throughout the year, so do the times at which birds roost. Some authors claim a characteristic light intensity for awakening ('Weckhelligkeit') for each species but this term does not seem very useful for, although there may be thresholds below which activity normally ceases, prolonged studies show that these threshold intensities change gradually with the season. Moreover, experiments in which birds were kept under constant conditions showed that they retain a sleeping rhythm similar to their natural one, at least for a few days. Seasonal changes in timing of roosting are most obvious at high latitudes, e.g. northern Scandinavia, where in the middle of winter passerines awaken and retire at far lower light intensities than in summer. This is presumably due to the amount of time they require to find sufficient food relative to day length, as food reserves of many passerines may only just exceed their requirements for a single night in extreme conditions (extreme conditions may also pertain during long tropical nights). For example, in temperate latitudes Murton et al (1963) have shown that Woodpigeons Columba palumbus need to spend 95% of available winter daylight feeding. Superimposed on these general seasonal changes are day to day variations, due in part to weather, particularly if this affects light intensity. Several brief studies have referred to this aspect, but none of them adequately. The researchers have tended to concentrate on the effects of minor factors, such as temperature, even though the influence of major factors, such as light intensity, are as yet little understood. Moreover, they often overlook the fact that cloudy days are, on average, both darker and warmer than clear days. Unpublished evidence suggests that birds use both their knowledge of the time of-day at which it generally 'gets dark' (from their 'internal clock', see RHYTHMS AND TIME MEASUREMENT) and the prevailing light intensity to predict when it will 'get dark' on a particular day, and therefore by what time they need to be at the roost. It is then reasonable to suppose that other factors would determine their response to this prediction, so that individuals which had, early on, found sufficient food would be likely to play safe, and arrive earlier at their roost than those that were still hungry. Similarly, it is known that birds flying long distances to a roost will leave their feeding ground earlier on darker days and on days when they must fly into the wind. Dawn chorus. A number of papers refer to dawn awakening, particularly the relative times at which different species start to sing in the (spring) dawn chorus. The times, and light intensities, for these onsets of song also vary seasonally and daily. In a series of experiments Kacelnik (1979) has investigated the reasons for the dawn chorus and its timing in the Great Tit Parus major. He considers the dawn chorus to be a special case of a 'trade-off' between the competing demands of feeding and territorial defence. Thus the dawn chorus of Great Tits occurs at a time of

518 Roosting

Long-tailed Tits Aegithalos caudatus in winter roost in December, southern Primorskiy, USSR. (Photo: Y. Shibnev). day when low light intensity and low temperature (affecting prey mobility) reduce feeding efficiency, while territorial intrusions are at their peak and vocal defence of territory, by song, is more effective due to enhanced sound transmission (poor visibility militates against visual display). Kacelnik concludes that no single factor hypothesis can explain the timing of the dawn chorus . Roost site. Birds have two basic requirements of a roost site, namely, protection from predators and shelter from the elements. Holes are presumably both safe and warm. City centres are warmer than surrounding land (I. 4°C warmer , and drier , in London ), while street lights may permit birds to find roosting perches later (if they can see adequately by street lighting), or even serve as warm roost sites themselves, while the better lighting should aid detection of predators . Wildfowl and many seabirds tend to roost on islands, on the water or in open sites where predators can approach them less readily. Many ground-feeding birds roost either in the open or perch on low branches, out of the reach of foxes Vulpes spp. and other predators. Many species roost as solitary individuals. The nest site may be an important roost both prior to, as well as during, nesting (incubating birds are often asleep). In communal roosts the alarm calls of the more alert individuals may often function to warn their companions of danger , as with quails Cotumix spp. which roost in grouped circles, each individual facing outwards . The fine stru cture of roosts, for group or communal roosting species, may be important, as birds at the centre of a line or group are presumably less vulnerable to predation. Swifts Apus apus may pass the night on the wing, although they also use more conventional sites, such as the nest. Shelter is needed to help the bird maintain its body temperature, as it must burn food reserves during the night which it cannot replenish until morning. Small birds, with a large surface to volume ratio, lose heat more rapidly, and particularly in cold climates. Those that roost in holes have the advantage that the heat they lose warms the air around them, but even roosting under cover, such as in a conifer wood, can appreciably reduce heat loss by radiation . Several species of grouse tunnel out roosts under snow. More important, however, is shelter from rain and wind, which reduce the insulative benefits of fluffing up the feathers and thereby lead to more rapid chilling. Swingland (1977) has shown that communally roosting Rooks CQI'VUS frugilegus apparentl y compete for sheltered sites: the more dominant older birds force younger individuals, which also have lower food reserves, from the higher , more sheltered sites to lower, more exposed ones; those lower sites may also incur greater risk from predators. Yom-Tov (1979) has shown that birds low

down in a communal roost may have the water-repellent properties of their feathers seriously impaired by droppings from those roosting above them . Small waders may roost among larger species, using them as 'windbreaks' . In extreme cold weather some species may huddle closely together, e.g . Long-tailed Tits Aeguhalos caudatus, treecreepers, wrens, swifts, Australian wood-swallows (Artamidae), Emperor Penguins Aptenodytesforsteri, Bobwhite Quails Colinus virginianus and many others . Hummingbirds may also roost in enclosed spaces, but have a remarkable ability, rare among birds, of becoming nocturnall y torpid , their body temperature dropping to as low as 4°C. Reducing the temperature difference between their body and the environment also reduces their energy loss, thus helping them to survive long cool nights and live in areas they could not otherwise inhabit (see TORPIDITY ) . Communal roosting. Many territorial species roost within their territory boundary during the summer, and some during winter too. Outside the breeding season birds that feed in flocks generally roost communally, e.g. Rooks, Starlings Stumus vulgaris, finches, hirundines (Hirundinidae), pigeons and many waders. Some relatively unsociable feeders may also congregate to roost, e.g. the Pied or White Wagtail Motacilla alba. Terns form communal roosts just prior to the breeding season, where courtship and copulation may take place. Large mixed roosts of several species are not uncommon , e.g. Starlings, Common Grackles Quiscalus quiscula, Brown-headed Cowbirds Molothrus ater and Red-winged Blackbirds Agelaius phoeniceus in North America. Waders for example, roosting communally on a tide-island in an estuary , may simply resort to the safest site available from their dispersed feeding areas. In other instances, however, the reasons for communal roosting are much less obvious. Starlings, for example, often roost near their feeding sites in autumn, but desert these in winter in favour of larger roosts that may be 50krn or more away. These sites may be used year after year. It is difficult to assess the numbers of birds using them, but some Starling roosts contain several hundreds of thousands , while the Quelea Quelea quelea, a serious pest of grain crops in large parts of Africa, collects at night into roosts of millions (see QUELEA CONTROL) . Many species that roost communally perform spectacular aerobatic displays around the roost, and often have conspicuous staging posts ('pre-roost gatherings') where groups congregate before a mass entry into the roost. Such displays may act as visual markers, locating the present roost site for birds unfamiliar with it; this could be particularly useful if unpredictable disturbance, e.g. predators, should alter the precise location of a roost from one day to the next. Similarly, there are typical sequences of

Rynchopidae

behaviour for dawn emergence, and the mass dawn exits of Starlings, at 3- or 4-minute intervals, even produce spectacular patterns of radially dispersing 'rings' on RADAR screens. The larger communal roosts may contain so many birds that vegetation is damaged, even destroyed, either by physical damage or by the toxic effects of accumulated droppings; in exceptional circumstances this may cause serious local problems to man , e.g . in city centres, or to forestry and agriculture. It seems unlikely that predator avoidance is responsible for the enormous total numbers in the larger roosts, and there has been much speculation as to their likely function. An attractive hypothesis, proposed by Ward and Zahavi (1973), suggests that these roosts serve as 'INFORMATION CENTRES' as to where to find food locally. They point out that communal roosts are normally composed of species whose food is patchily distributed, locally super-abundant and ephemeral, so there is accordingly no advantage to be gained from trying to 'defend' such a food source, nor in 'keeping its location quiet' . Conversely , birds not knowing of such food sources would gain from following others to feeding sites. In these circumstances (patches of super-abundant, ephemeral food) all individuals could benefit from the pooled information. Cheating (trying to keep a patch quiet, but still knowing about those of others) would be difficult and, if the patches are ephemeral, risky. Accordingly, a system of mutual benefit might persist due to advantages accruing to individuals. (For Posture see SLEEP. ) P.I.B. See photo COMFORT BEHAVIOUR .

519

Amlaner, C.]. Jr. & Ball, N.]. 1983. A synthesis of sleepin wildbirds. Behaviour 87: 8S-119. Cramp, S. & Simmons, K.E.L. 1977 et seq. The Birds of the Western Palearctic. Oxford. Kacelnik, A. 1979. Studies of foraging behaviour and timebudgeting in Great Tits (P orus major). D.Phii. thesis, Univ. of Oxford. Murton, R.K., Isaacson, A.]. & Westwood, N.]. 1963. The feeding ecology of Woodpigeons. Br. Birds 56: 34S-375. Swingland, l.R. 1977. The social and spatial organisation of winterroosting in the Rook (Corvus[rugilegus). J. Zoo!' Lond. 182: 509-528. Ward, P. & Zahavi, A. 1973. The importance of certain assemblages of birds as 'information centres' for food-finding. Ibis 115: 517-534. Ydenberg, R.C. & Priss, H.H.T .L. 1981. Review on Functions of Roosting. Proceedings of 5th annualconference on functions of roosting. Texel. Yom-Tov, Y. 1979. The disadvantage of low position in colonial roosts: an experiment to test the effects of droppings on plumage quality. Ibis 121: 331-333.

ROSEFINCH: substantive name of most species of Carpodacus, a Holarctic and mainly montane genus of finches (for family see FINCH). ROSELLA: substantive name of the Australian Platycercus spp. (Psittacinae, Platycercini) (see PARROT). ROSTRATULIDAE: see

CHARADRIIFORMES; PAINTED SNIPE .

ROSTRUM: the bill or beak (see

BILL);

adjective , 'rostral'.

ROSY -BILL: Netta peposaca (see

DUCK).

ROULROUL: Rollulus roulroul (see under r-SELECTION: see

PHEASANT).

K-SELECTION .

RUBY: Clytolaema rubricauda (for family see

HUMMINGBIRD).

RUBY-CHEEK: name, alternatively 'Ruby-cheeked Sunbird', of

Anthreptes singalensis (see SUNBIRD) .

RUBYTHROAT: substantive name of some Luscinia spp. (for subfamily see THRUSH ) . RUFF: name of Philomachus pugna x as a species; also a term particularly for the male, the female then being termed 'reeve' (see SANDPIPER) . See photo LEK. RUKH: see

FABULOUS BIRDS.

RULES: statements formulating what appear to be regularities in natural phenomena, e.g. in the correlation of morphological variation with geographical, climatic , or other factors---e .g . ALLEN'S RULE; BERGMANN'S RULE ; GLOGER'S RULE .

RUMP: see

TOPOGRAPHY.

RUNNING: see

LOCOMOTION, TERRESTRIAL; LEG.

RUSH: a fall of birds on migration (see

FALL).

RUSHBIRD: substantive name of Phleocryptes melanops, a South American furnariid (see OVENBIRD ( 1» . Starlings Slumus vulgaris above mass roost. (P hoto: F . Polking).

RYNCHOPIDAE: see under

CHARADRIIFORMES; SKIMMER .

s

than those of savanna habitats. The plumage is close and thick with a dense underdown, even on the apteria (see APTERIUM; PLUMAGE), which insulates the birds against extremes of heat and cold. The central tail feathers of 6 species are elongated and pointed. The wing is aquintocubital (lacks the fifth secondary remex: see PLUMAGE; WING) and has 11 primaries which are long and adapted to strong sustained flights undertaken daily to water. Despite their short legs, sandgrouse walk and run well. Their toes are also short, sometimes partially webbed. The family includes 2 genera, Syrrhaptes (tarsus and toes completely feathered, hind toe absent) and Pterocles (tarsus feathered in front only, toes naked, hind toe rudimentary and raised above ground level). Other generic divisions based on plumage characters or drinking times are generally considered unacceptable except perhaps as subgenera which from time to time have included E remialector, N .amapterocles, Parapterocles, Macleanornis, Nyctiperdix, Dilophilus and Calopterocles. Habitat. Most sandgrouse inhabit arid to semi-arid regions, including the major deserts of Africa and Asia. They prefer areas covered with stones or low shrubby growth. A few species live in rather dry savanna. The Tibetan Sandgrouse Syrrhaptes tibetanus is montane. Distribution. The 14 species of the genus Pterocles occur in Africa, southern Europe and southern Asia, including the Indian subcontinent. P. personatus is confined to Madagascar. The 2 species of Syrrhaptes inhabit the steppes and mountains of central Asia. The main centres of sandgrouse distribution are the Sahara, the Kalahari and the deserts of the Middle East. Movements. Most sandgrouse are resident or locally nomadic, but the most southerly populations of the Namaqua Sandgrouse Pterocles namaqua, the Zambian populations of the Yellow-throated Sandgrouse P. gutturalis and the Indian populations of the Black-bellied Sandgrouse P. orientalis are truly migratory. Pallas's Sandgrouse Syrrhaptes paradoxus of the central Asian steppes has undergone eruptive 'migrations' in certain years as far west as Britain and nearly as far east as Peking (see IRRUPTION). British immigrants remained and bred, although they are unlikely ever to have become established. Food. All sandgrouse feed mainly on small hard seeds picked up from the ground. They may sometimes take small bulbs, green leaves, shoots, berries and even insects (termites and ants) especially during the breeding season. Grit is eaten for grinding food in the gizzard. The largely dry food necessitates daily drinking, particularly in hot weather. Drinking times are regular and species-specific (either in the morning or at dusk). Ten species are morning drinkers, 4 drink at dusk, and 2 are said to drink both morning and evening, but this needs confirmation. A few individuals of both kinds of sandgrouse may drink twice a dayprobably mainly birds that have been incubating in the hot sun during the day, since most evening drinkers of morning-drinking species appear to be females. Sandgrouse drink by taking a draught of water into the mouth by sucking once or twice and then raising the head to swallow (see DRINKING); this process is repeated up to 10 times but takes just a few seconds. When the crop is full the bird flies directly away from the water unless it is a member of a mated pair whose mate is still drinking: then it waits until the two can flyaway together. Behaviour. Although sandgrouse pair off monogamously when breeding, they are all highly gregarious, especially when gathering to drink.

SABREWING: substantive name of Campylopterus (including 'Pampa') spp. (for family see HUMMINGBIRD). SACRUM (adj. SACRAL): the part of the vertebral column between the lumbar and caudal portions (see SKELETON, POST-CRANIAL). SADDLE: term used where the colour of the upper surface of the wings continues across the mantle without a break. See TOPOGRAPHY. SADDLEBACK: Creadion ('Philesturnus') carunculatus (see

WATTLE-

BIRD (2).

SADDLEBILL: sometimes used alone as the name of the Saddle-billed Stork Ephippiorhynchus senegalensis (see STORK). SAGITTAL: in the median longitudinal plane of the body, e.g. a section from head to tail in the mid-line; the 'sagittal suture' is the junction of the parietal bones of the skull. SAGITTARII; SAGITTARIIDAE: see under

ACCIPITRIFORMES;

SECRETARY-BIRD.

SAHEL ZONE: the belt of grassland with trees (savanna) and thorny scrub which lies immediately south of the Sahara, and which is subject to drought. SAKABULA: Euplectesprogne (see WEAVER). SAKER: Falco cherrug (see FALCON). SALIVARY GLANDS: see ALIMENTARY SALPORNITHIDAE: family of

SYSTEM; TONGUE.

PASSERIFORMES,

suborder Oscines;

CREEPER, SPOTTED.

SALTATOR: generic name used as substantive name of Saltator spp. (see CARDINAL-GROSBEAK). SALT GLAND: alternatively 'lateral nasal gland' (see

EXCRETION,

EXTRARENAL; NARIS).

SALTING or SALTMARSH: an area of intertidal mud which has been colonized by salt-adapted plants. SAMPLING: see BIOSTATISTICS. SANCTUARY: see CONSERVATION. SANDERLING: Calidris (formerly Crocethia) alba (see See photo LOCOMOTION, TERRESTRIAL.

SANDPIPER).

Pin-tailed Sandgrouse Pterocles alchata. (C.E. T.K.).

SANDGROUSE: substantive name of the species of Pteroclididae (Pteroclidiformes); in the plural (unchanged), general term for the family. This mainly Afro-Asian group has affinities with the waders (Charadriiformes, suborder Charadrii) and the pigeons (Columbidae), but is best regarded as having separate ordinal rank; resemblance to true grouse (Tetraoninae) is purely superficial. Characteristics. Sandgrouse are terrestrial birds, much like pigeons in size and shape. They vary in length from 25-48 em, including the elongated tail feathers in the larger species; weights range from 170g to 650g; most are between 230 and 300g. They are coloured in soft shades of grey, red, yellow, brown and buff, often marked with white and black. The males of most species have breast bands and all show sexual differences in coloration. Species inhabiting semi-desert tend to be paler 520

Sandpiper

The birds call in flight as they travel to the waterholes, thereby attracting others of the same species (and sometimes other species) along the way, until drinking flocks may number thousands of birds. Sandgrouse may fly up to 80 km to water each day (a round trip of 160km) at a cruising speed of about 70km/h. Depending on the species, the birds may land right at the water's edge (or even in the water), drink quickly and depart at once, or they may assemble some distance from the water and then fly or run down to it once the coast is clear. Both these methods reduce the possibility of attack by predators. Voice. Sandgrouse calls are characteristic whistles or clucks, usually in phrases of two, three or more syllables. These calls are most often heard in flight, but other quieter calls are also heard from birds on the ground. Breeding. Sandgrouse pair off during the breeding season which is largely determined by rainfall and the resulting adequate food supply. The nest is a shallow scrape on the ground, usually out in the open, but sometimes against a stone, shrub or grass tuft. The scrape is sparsely lined with small stones or bits of dry vegetable matter gathered by the parents during incubation. The clutch is almost invariably 3 eggs, rounded at both ends, coloured dull pinkish or greenish and more or less heavily marked with grey, brown and olive. The female incubates by day and the male by night; both sexes have a brood patch. The eggs hatch after 21-31 days. The downy chicks leave the nest as soon as the last to hatch is dry, following the parents to forage for seeds. They are not fed at all by either parent, but are shown food by the parents pecking at suitable items. They are provided with water by a unique mechanism. The male soaks his belly feathers during his daily drink and the chicks take the water from his wet plumage on his return. He adopts an upright 'watering posture' which exposes the wet belly and attracts the chicks from their hiding places under shrubs. Female sandgrouse seldom soak their belly feathers, probably doing so only if the male has been killed by a predator, or perhaps when the brood has reached the age at which the male's water-carrying capacity needs to be augmented by the female. The belly feathers of both sexes are specially adapted to taking up water in a bed of microscopic filaments on the inside surface of the feathers against the body, where evaporation is reduced to a minimum while the birds are in flight. Nevertheless the distance over which enough water can be carried in this way is limited to about 30km. Young sandgrouse are watered thus until after their first moult when they fly to water like the adults. Only Syrrhaptes tibetanus appears not to water its young from its belly feathers, but lets them drink at open water which is freely available in streams resulting from snow-melt in their high mountain habitat; this species also lacks the specialized feather structure. When the chicks are very young, the parents fly to water separately so that the chicks are not left unattended; from the age of about 3 weeks, they are left alone as the parents fly together to drink. The young can fly at the age of 4-S weeks. BELLY-SOAKING behaviour and a similar, though less well developed microscopic feather structure occurs in the closely related waders (Charadriiformes), but waders that transport water in their belly feathers do so only for cooling eggs and chicks, not for providing drinking water. G.L.M. See photo BELLY-SOAKING. Cade, T.j. & Maclean, G.L. 1967. Transport of water by adult sandgrouse to their young. Condor 69: 323-343. Fieldsa, J. 1976. The systematic affinities of sandgrouses (sic), Pteroclididae. Vidensk. Meddr dansk naturh. Foren. 139: 179-243. George, U. 1969. Uber das Tranken der JUDgeD und andere Lebensausserungen des Senegal-Flughuhns, Pterocles senegal/us, in Marokko. j. Orn. 110: 181-191. Joubert, C.S.W. & Maclean, G.L. 1974. The structure of the water-holding feathers of the Namaqua Sandgrouse. Zool. Afr. 8: 141-152. Maclean, G.L. 1968. Field studies on the sandgrouse of the Kalahari Desert. Living Bird 7: 209-235. Maclean, G.L. 1976. Adaptations of sandgrouse for life in arid lands. Proc. XVI Int. Orn. Congr.: 502-516. Thomas, D.H. & Robin, A.P. 1977. Comparative studies of thermoregulatory and osmoregulatory behaviour and physiology of five species of sandgrouse (Aves: Pteroclididae) in Morocco. J. Zool., Lond. 183: 229-249.

521

SAND PIPER: a term often restricted to the members of 2 genera (Tringa and Calidris) of long-billed wading birds (waders = shorebirds) in the family Scolopacidae (Charadriiformes, sub-order Charadrii); more broadly used to include the whole of the family of sandpipers and snipe, many of which are referred to normally by other substantive names which encompass only single species or small groups of species (as outlined below). (For reference to related families see under CHARADRIIFORMES.) Characteristics. Members of the Scolopacidae vary in length from 12-60 em but frequently a large proportion of this is the slender, long and often decurved bill (recurved in a few species). The bill is flexible and can be opened at the tip only (see RHYNCHOKINESIS). It is often assumed that long bills have evolved for probing but this delicate mechanism is also well suited for collecting seeds and berries. Usually sandpipers have long legs, the tibia is partially bare and the toes are long; the hallux is short, and absent in one species (Sanderling Calidris alba). The wings are normally long and pointed, the tail short and the neck long. In summer plumage the upper-parts of most species are a mixture of rich browns and greys and, in some species chestnut reds, the underparts being often well spotted and streaked. In winter these markings are usually lost and the upper parts are also more uniform. It is generally assumed that the plumage is cryptic and this is certainly the case in summer in the nesting habitat. However, at communal roosts flocks of Knot Calidris canutus can be seen for several km from the air, and clearly the plumage draws particular attention to them at this time (Ward and Zahavi 1973). Other species of flocking waders have similar plumage characteristics, though perhaps do not stand out as much as Knot. Habitat. In the breeding season sandpipers are birds of open habitats, moorland and tundra. In the non-breeding season they are mainly gregarious and to be found in coastal areas, particularly in the intertidal regions of estuaries. Distribution. Most sandpipers inhabit the Northern Hemisphere during the breeding season and occur into the high Arctic; the majority breed at high latitudes and several species have a circumpolar distribution. Most are highly migratory and in winter many species occur well into the Southern Hemisphere. Generally speaking, the more northerly breeding populations undertake the longest migrations and the temperate breeders the shortest migrations; these latter often winter within the breeding range whilst the former perform transequatorial migrations. Due to their extensive distribution, it is not surprising that several species show variation in both size (often clinal) and colour (more than one morph). These have probably evolved in some cases through isolation and it is possible that some previously recognized sub-species, e.g. Southern Dunlin Calidris alpina schinzii, British Redshank Tringa totanus britannica, are hybrids derived from previously separated breeding populations. Usually there is a large degree of overlap of populations in winter quarters but some, e.g. Knot, seem to be almost totally separated, Greenland/N. Canada and Siberian populations wintering in western Europe and N. Africa respectively. Food. During winter, invertebrates form the major part of the diet, most food being collected from, or not far below, the surface of the intertidal zone, or from shallow water. Occasionally insects are taken on the wing, and form a high percentage of the diet during the breeding season; at this time berries are also important to some species at higher latitudes. In winter a large part of the food is taken at night. Behaviour. During feeding and roosting sandpipers mainly form single species parties or flocks, but species often intermingle, particularly when leaving the estuary roosts. All species are strong flyers and those which flock often perform complex aerial movements, which, like their winter plumage, are clearly evolved to attract attention. These flights are very spectacular and the precision with which they are performed is remarkable, particularly in tightly packed flocks of Knot. Many species are territorial during the breeding season but others, e.g. Redshank, lack specific territorial boundaries and are semi-colonial. The pair bond is usually monogamous and, at least in some species, for life. It is established in smaller sandpipers in the first or second year of life, and perhaps as late as the third year in some species. Female Redshanks have been recorded incubating a full clutch within 10 months of hatching. Polygamy has been suggested as occasional in some species, e.g, Greenshank Tringa nebularia, but it is difficult to be certain of this. There is often an elaborate courtship display, beginning with a song flight (often later used in distraction display) associated with pair formation; in some species at least there are ground chases and complex pre-copulatory ceremonies. Distraction displays vary from repetition of display flight

522 Sandpiper

(e.g. Oystercatcher Haematopus ostralegus, Redshank) to 'rodent-runs' (Purple Sandpiper Calidris maritima) and injury feigning (Reeve Philomachus pugnax). There is a great variety of call notes, from raucous squeaks to extended songs. Some species, especially snipe, also produce non-vocal sounds (see MECHANICAL SOUNDS).

Breeding. The nest is usually on the ground, often concealed in herbage, though a few species use disused nests of arboreal birds e.g. Fieldfares Turdus pilaris. The scrape, often made during a 'scraping ceremony' by the male in the presence of the female, is lined usually after laying the first egg and more lining is added during incubation. Eggs usually number 4, but in some cases 2 or 3. Most species have pyriform eggs, with dark brown and black markings, on a paler ground; all are cryptically coloured. Incubation normally begins with the last egg and chicks hatch almost simultaneously. Both sexes usually share incubation, though one bird often takes the greater share. Downy young leave the nest within a day of hatching and may make extensive journeys (often 1-2 km) to suitable feeding areas. The chicks crouch when alarmed and may be carried over obstacles by parent birds. The parental role varies with species. In some populations of Sanderling (Arctic Canada but not Greenland) and in Temminck's Stint Calidris temminckii, the female lays 2 clutches and each bird of a pair incubates a clutch; in other species e.g. Pectoral Sandpiper C. melanotus, only the female incubates, while only male phalaropes incubate (see PHALAROPE). Normally both parents tend chicks for at least part of the fledging period but in Pectoral and Curlew Sandpipers C. ferruginea only the female remains; in these cases the bird leaving the brood migrates south first, which may relieve pressure on the food supply. Taxonomic sub-divisions. The taxonomic sub-division of the group is based largely on skeletal structure and external morphology but has been improved by recent work on the colour pattern of downy young and studies of electrophoretic protein patterns. The sub-families recognized are: Tringinae (curlews, godwits and tringine sandpipers); Arenariinae (turnstones); Scolopacinae (woodcock); Capellinae (dowitchers and snipe); Calidriinae ('calidritine' sandpipers, the Eroliinae of some authors); Aphrizinae (Surfbird). Within the Scolopacidae there are 85 species in 27 genera. Curlews, Godwits and Tringine Sandpipers. The curlews are the largest members of the family and are characterized by their long decurved bills. The Eskimo Curlew Numenius borealis is now extremely rare; however, its close relative the Little Curlew N. minutus is not in immediate danger in eastern Siberia where it nests in an interesting association with the Golden Eagle Aquila chrysaetos from which it apparently derives a degree of protection through other predators being excluded from the eagles' territories. The Eurasian Curlew N. arquata is the largest Palearctic species and is replaced in the Nearctic by the Long-billed Curlew N. americanus. The Whimbrel N. phaeopus, which has a circumpolar distribution, occupies a more northerly range and in North America is referred to as the 'Hudsonian Curlew'. The Slender-billed Curlew N. tenuirostris is now quite rare and restricted to a small area of Western Siberia. Curlews make extensive migrations, the Little Curlew, which nests in Siberia, reaching Australia. Like the curlews, the godwits are large waders but they have long, slightly recurved bills. There are 4 species in a single genus Limosa, the Marbled and Hudsonian Godwits (L. fedoa and L. haemastica) being Nearctic forms whilst the Bar-tailed and Black-tailed Godwits (L. lapponica and L. limosa) are Palearctic breeders. The Upland Sandpiper (Bartram's Sandpiper or Upland Plover) Bartramia longicauda is a North American species in a mono typic genus and is possibly more closely related to the curlews and godwits than to the tringine sandpipers. There are 9 species in the genus Tringa, the largest of which are the Greater Yellowlegs T. melanoleuca of North America and the Greenshank T. nebularia of Eurasia, both a little smaller than godwits. The Greenshank occupies a range in Eurasia intermediate between that of the more northerly Spotted Redshank T. erythropus and the more southerly Common Redshank T. totanus, though there is overlap of

ranges in western Europe. In North America the Lesser Yellowlegs T. flavipes replaces the Redshank ecologically. Two species, the Solitary Sandpiper T. solitaria and the Green Sandpiper T. ochropus, nest in trees, in the abandoned nests of other birds, as may the Wood Sandpiper T. glareola. Two species closely related to the genus Tringa are placed in the genus Actitis. These are the Common Sandpiper A. hypoleucos and its North

Common Sandpiper Actitis hypoleucos. (A.H.).

American replacement the Spotted Sandpiper A. macularia; both occur in temperate latitudes. The Terek Sandpiper Xenus cinereus breeds from Finland to eastern Asia; the latter is the only area from which the Spotted Greenshank (Armstrong's Sandpiper) Pseudototanus guttifer has been recorded breeding. The Grey-rumped Sandpiper H eteroscelus brevipes and the Wandering Tattler H. incanus are thought by some authorities to be conspecific but their ranges overlap in Anadyrland (N .E. Siberia), and there are morphological differences of an order justifying their being regarded as specifically distinct. The Willet Catoptrophorus semipalmatus is a large (for tringine sandpipers) species with no obvious relatives; it is an inhabitant of middle North American latitudes. The rare Tuatamu Sandpiper (Peale's Sandpiper) Aechmorhynchus parvirostris is another species with no obvious present day close relatives, though 2 closely related species (one of them possibly conspecific) are now extinct, the White-winged Sandpiper Prosobonia leucoptera of Tahiti and the Sharpbilled Sandpiper Aechmorhynchus cancellatus known only from a single specimen. Like the Tuatamu Sandpiper both these latter species had a limited distribution in Polynesia. Turnstones. From both electrophoretic studies and downy chick patterns it appears that turnstones Arenaria are a tringine off-shoot, rather than relatives of the plovers. There are 2 species, the Ruddy Turnstone A. interpres, which has a circumpolar breeding distribution mainly within the Arctic but south to the Baltic Sea, and the Black Turnstone A. melanocephala which is restricted to Alaska. Turnstones usually occur in small flocks on rocky shores where they often feed in the company of Purple Sandpipers. Flocks seldom exceed 100 birds and they feed mainly on invertebrates found under stones which they push over with their short, blunt bills. The bill is also used for excavation but never for true probing. Turnstones will also feed on carrion and eggs of their own and other species. Turnstones are the most littoral of all waders and only rarely are they found far from the coast. On such occasions they remain on moss and lichen tundra in short vegetation and do not close their toes in walking as do some waders which are adapted to deeper vegetation. Turnstones make extensive migrations and the Ruddy Turnstone can be found wintering in South America, South Africa, Australia and New Zealand. Woodcock. Five species of woodcock are generally recognized, the European Woodcock Scolopax rusticola, 3 oriental species of the same genus, and the American Woodcock Scolopax minor, which is smaller than the European species. All have a relatively long, straight bill and the eyes are set well back on the head. The legs are relatively shorter than in most other waders, the neck is short, the body compact and the head relatively large, the external opening of the ear being below, instead of behind the orbit.

Woodcock are the only group of waders to frequent woodland; woods with damp floors on fertile mull soils with a high earthworm content are preferred. The spring display flight of the European Woodcock is known as RODING. It occurs at dusk and is an owl-like flight, much more frequently seen than the ground display of courtship which leads to coition. This display involves the male strutting round the female with drooping wings and fanned tail, but very little is known of the courtship of woodcock.

Scapus

As in the snipe, normally only the female incubates, in contrast to most waders where the sexes share incubation. The eggs of woodcock tend to be more rounded than other wader species and paler in colour than most sandpipers'. The European Woodcock has been recorded on several occasions carrying the young between the legs, against the belly. Snipe. Like woodcock, snipe have long, straight bills and relatively short legs. They often remain undisturbed until almost trodden on, even when feeding, and then flush in a characteristic zig-zag flight. They are birds of open marsh land throughout the year and seldom occur on the shore. Some species are solitary though others occur in small groups ('wisps'), but seldom in large flocks. Several species produce loud non-vocal sounds ('drumming' or 'bleating') with the outer tail feathers in flight and a similar habit has been recorded in the Little Curlew. Snipe are birds of lower latitudes and generally do not perform extensive migrations. They are found in most temperate regions of the world; members of the genus Gallinago (Capella) of which there are 13 species occur also as visitors to southern Asia and Australia. The Common Snipe G. gallinago is a cosmopolitan species and is known as the Fantail Snipe in India. Like the Jack Snipe Lymnocryptes minimus, the Great Snipe G. media has a more restricted range in the Palearctic and is unique in being, apart from the Ruff Philomachus pugnax, the only wader with a lekking system (LEK) of courtship. Perhaps of particular interest in this group is the sub-antarctic Snipe Coenocorypha aucklandica, races of which occur in subsidiary islands around New Zealand; uniquely in the group, this species nests in burrows excavated by other birds; it appears to fly little and to be largely nocturnal. Recent work has shown that dowitchers are probably more closely related to snipe than to godwits. The Asian Dowitcher Limnodromus semipalmatus is the only Old World species, nesting in Siberia. Most authorities now treat the American dowitchers as 2 species, the Longbilled Dowitcher L. scolopaceus and the Short-billed Dowitcher L. griseus. These nest in the Arctic and sub-arctic and perform long migrations, unlike most snipe. Calidritine sandpipers. These are, perhaps, the true sandpipers and most are placed in the genus Calidris, which contains the smallest waders, the stints. The 23 species are birds of high latitudes with a circumpolar breeding distribution and because of this many perform extensive migrations; out of the breeding season they are birds of the shore and generally highly gregarious. They are known as 'peeps' in North America. Their twittering calls are not as loud as those of tringine sandpipers. The Knot C. canutus is the largest species, 25 cm in length, whereas the Least Sandpiper C. minutilla is only half this size. The most southerly breeder is the Dunlin which nests as far south as south-western England and the southern Baltic. Most calidritine sandpipers have medium sized pointed bills, used for picking and probing. The Spoon-billed Sandpiper C. pygmeus of Northeast Asia is exceptional in having flattened and broadened tips to both mandibles. This species feeds differently from most sandpipers, not running from place to place, but running forward often up to its belly in water, moving its bill in semi-circles in front of it. Its feeding mechanism is not clearly understood. A second exception is the Sanderling, often placed in the monotypic genus Crocethia; it is the only sandpiper lacking a hind toe. Whilst most calidritine sandpipers feed outside the breeding season on sandy and muddy shores, the Purple Sandpiper and Rock Sandpiper C. ptilocnemis feed on rocky shores often in the company of turnstones. The most aberrant member of this group is the Ruff, so named because the male sports an erectile collar of feathers and ear tufts during the breeding season; the female (reeve) lacks these adornments and is much smaller. The male's breeding plumage is associated with communal displays on a 'hill' or LEK, to which females are attracted. The female incubates and tends the young alone and there is no permanent pair bond. In this it is unique in the Scolopacidae. The Ruff breeds right across northern Eurasia and migrates south as far as Ceylon or Cape Province. Surfbird. Some authorities have included the Surfbird Aphriza virgata with the turnstones but recent work has shown that, whereas turnstones have affinities with the tringine sandpipers, the Surfbird has calidritine origins. Like turnstones, the Surfbird lives on rocky shores and its short bill suggests a convergence with the plovers. It breeds in Alaska, in mountainous regions above the tree line. See photos COMFORT BEHAVIOUR; COPULATION; DISTRACTION BEHAVIOUR;

EGG-TOOTH;

FACILITATION,

SOCIAL;

FEEDING

HABITS;

523

HATCHING; LEK; LOCOMOTION, TERRESTRIAL; PELLET; VOCALIZATION.

W.G.H.

Hale, W.G. 1980. Waders, London. Jehl, J .R., Jr. 1968. Relationships of the Charadrii (Shorebirds); a taxonomic study based on color patterns of the downy young. Mem. S. Diego Soc. Nat. Hist. 3: 1-54. Nethersole-Thompson, D. 1951. The Greenshank. London. Nethersole-Thompson, D. & M. 1979. Greenshanks. Berkhamsted. Prater, A.J., Marchant, J.H. & Vuorinen, J. 1977. Guide to the Identification and Ageing of Holarctic Waders. Tring. Seebohm, H. 1887. The Geographical Distribution of the Family Charadriidae. London. Sibley, C.G. & Ahlquist, J.E. 1972. A comparative study of the egg-white proteins of non-Passerine birds. Yale. Ward, P. & Zahavi, A. 1973. The importance of certain assemblages of birds as information centres for food finding. Ibis 115: 517-534.

SAND-PLOVER: substantive name of some species of Charadrius (for family see PLOVER (1)). See photo ENERGETICS. SANITATION, NEST: see PARENTAL

CARE.

SAPPHIRE: substantive name of Chlorestes notatus and many Hylocharis spp. (for family see HUMMINGBIRD). SAPPHIREWING: Pterophanes cyanopterus (for family see HUMMING.. BIRD).

SAPPHIRONIA: substantive name (some authors) of Lepidopyga spp. (for family see HUMMINGBIRD). SAPSUCKER: substantive name of Sphyrapicus spp. (see

WOOD-

PECKER).

SARMATIC: derived from the coastal fauna of the brackish or salt inland 'Sarmatic Sea' of late Tertiary and Pleistocene times, an extension of the eastern Mediterranean. SAUROGNATHOUS: see PALATE. SAUROPSIDA: term embracing reptiles and birds. SAURORNITHES: name formerly used for a sub-class equivalent to the Archaeornithes (see under CLASS). SAVANNA: also written 'savannah', a type of open country found in semi-arid regions or in those with a long dry season; term originally applied in South America but now used widely as a habitat description. For example, in Africa immediately south of the Saharan desert there is a belt of 'thorn-scrub savanna', characterized by a sparse vegetation of spiny bushes and tufted grass; south of that, where there is a substantial rainfall during part of the year, is a belt of 'grass-woodland savanna', park-like country characterized by patches of woodland and isolated trees in a general area of abundant long grass withering in the dry season. SAWBILL: general term for the mergansers Mergus spp. (see DUCK). SAW-WHET: Aegolius acadica, a very small North American

OWL.

SAW-WING: substantive name used in East Africa for rough-winged swallows of the genus Psalidoprocne (see SWALLOW). SCAL Y- WEAVER: name of 2 species of weavers of uncertain systematic position. For family see SPARROW-WEAVER AND SCALY-WEAVER. SCANSORIAL: pertaining to the act of climbing, especially on tree-trunks (see LEG; LOCOMOTION, TERRESTRIAL). SCAPULA: a paired bone ('shoulder blade') of the pectoral girdle (see SKELETON, POST-CRANIAL).

SCAPULARS: (plural) the feathers above the shoulder (see

TOPO-

GRAPHY).

SCAPUS: term sometimes applied to the whole stem of a feather, i.e. calamus and rachis combined (see FEATHER).

524 Scaring

SCARING: a scaring stimulus is one that produces stress within birds so that they will try to avoid it. In this article bird scaring refers to the use of such stimuli to deter birds from areas where they cause damage. There is a great diversity in the sorts of bird damage that can occur, whether to agricultural or horticultural crops, fisheries or property. Traditionally the term bird-scarer has been applied to devices that deter birds without physical contact; such scarers therefore involve visual and/or auditory stimuli. Deterrents using tactile or gustatory stimuli, which clearly require physical contact, have been called 'bird repellents' (see REPELLENTS, CHEMICAL).

Traditional scaring techniques have involved the use of sudden loud sounds and/or bright novel objects which startle birds and cause them to flee (see Frings and Frings 1967). Purely visual devices range from the classic scarecrow to brightly coloured material suspended from poles, tethered balloons and various 'windmill-like' devices with vanes of different colours. A folklore has grown up that some colours, in particular red and orange, are 'naturally' repugnant to birds; there is however, no scientific evidence to support this belief. By far the most common acoustic scarer is the propane gas gun. Gas from a cylinder is periodically released into a firing chamber where it is ignited, the interval between explosions being adjustable. The sound level of these explosions can measure as much as 130 decibels at a distance of 1m from the mouth of the gun. In order to minimize noise nuisance it has been suggested that ultrasonic scarers, emitting sound frequencies above the normal human hearing range, should be used. Unfortunately the upper frequency limits of the bird species so far investigated are very similar to man's. Even in those species that can detect frequencies as high as 25,000 cycles/sec in laboratory tests (e.g. the Bullfinch Pyrrhula pyrrhula), the frequency range over which the birds' hearing is most sensitive is much lower, between 2,000 and 4,000 cycles/ sec. Just as people living next to a main road may slowly adapt to the traffic noise, so birds gradually lose their fear of loud and/or novel scarers. This process is called habituation. To slow the rate of habituation, one should, where possible, use periodic rather than continuous presentation, frequently vary the site and type of scarer, and occasionally reinforce the response by providing a real source of danger, such as shooting at birds around the scarers (for a recent review see Slater 1980). More recently, scarers have been developed that employ natural frightening stimuli encountered by birds. Most avian pests are prey to mammals and other birds at some stage of their life cycle and thus scarers that seek to mimic aspects of encounters with predators will to some degree be reinforced naturally outside the scaring context. The birds' fear response to devices of this kind should therefore persist longer than to scarers that rely upon the startle response produced by novelty, for a bird that does not quickly and repeatedly respond to predators is unlikely to survive. Indeed many species have a genetically inbuilt tendency to respond to various cues associated with the presence of predators. Trained raptors have been used with some success on airfields where birds pose serious dangers to aircraft (BlokpoeI1976). Models of birds of prey suspended from balloons or mounted on poles are generally ineffective, probably because raptor recognition can involve quite complex visual cues, such as plumage details, as well as features based upon flight characteristics. Much more successful have been attempts to deter birds using the calls they emit when they sight a predator (alarm calls) or are actually caught by one (distress calls). Broadcasts of these calls are now commonly used on airfields to clear the runways of birds before aeroplanes land or take off (Busnel and Giban 1965, Blokpoel 1976). Such calls are at present less widely employed in agriculture; perhaps their most common use is in the dispersal of Starling Sturnus vulgaris roosts. Responses to broadcast calls vary between species, some (e.g. Starlings) disperse immediately whilst others (e.g. Rooks Corvus frugilegus) approach and mob the loudspeaker before dispersing. Several species (e.g. Woodpigeon Columba palumbus) seem not to have alarm or distress calls, but apparently use visual means to communicate fear. For example, geese, when disturbed, frequently adopt a pre-flight posture which involves the vertical straightening of the neck and a rapid side-to-side shaking of the head. By using models that mimic this posture, Inglis and Isaacson (1978) successfully deterred skeins of Dark-bellied Brent Geese Branta bernicla bernicla from landing in fields containing the models. Similarly work by Murton and his colleagues (Murton et a11974) suggested that the white wing bars of Woodpigeons were used as a visual alarm signal eliciting flight, and prototype devices

that mimic these characteristics can deter Woodpigeons from landing in their vicinity (see Inglis 1980). The development of devices that employ the pest species' own acoustic and/or visual alarm signals seem to offer the best prospect for the production of an efficient scarer, although this is something that it is very difficult to quantify; firstly because within any given area there will be variation over time in the numbers of birds attempting to feed, and secondly because at any given time, areas will differ in their attractiveness to birds. An obvious general 'rule-of-thumb' is that scarers are most effective at those times of the year when alternative food sources are available nearby. The provision of cheap decoy crops together with the erection of scarers on the more valuable areas is likely, therefore, to be the most satisfactory method of protection. A problem could arise, however, if the decoy crops were provided throughout those periods of the year when starvation has a powerful influence on the population size of the pest, in that more birds may survive to return the following year. I. R.I. Blokpoel, E. 1976. Bird Hazards to Aircraft. Canada. Busnel, R.G. & Giban, J. 1960. Colloque sur la Protection Acoustique des Cultures et Autres Moyens d'Effarouchement des Oiseaux, jouy-en-josas 1958. Paris. Busnel, R.G. & Giban, J. 1965. Le Probleme des Oiseaux sur les Aerodromes. Colloque tenu a Nice les 25, 26 et 27 Novembre 1963. Paris. Frings, H. & Frings, M. 1967. Behavioral manipulation (visual, mechanical and acoustical). In Kilgore, W.W. & Doutt, R.L. (eds.). Pest Control: Biological, Physical and Selected Chemical Methods. New York. Inglis, I.R. 1980. Visual bird scarers: an ethological approach. In Wright, E.N., Inglis, I.R. & Feare, C.J. (eds.). Bird Problems in Agriculture. London. Inglis, I.R. & Isaacson, A.J. 1978. The responses of dark-bellied brent geese to models of geese in various postures. Anim. Behav. 26: 953--958. Murton, R.K., Westwood, N.J. & Isaacson, A.J. 1974. A study of woodpigeon shooting: the exploitation of a natural animal population. J. Appl. Ecol. 11: 61-81. Slater, P.J.B. 1980. Bird behaviour and scaring by sounds. In Wright, E.N., Inglis, I.R. & Feare, C.J. (eds.). Bird Problems in Agriculture. London.

SCA UP: substantive name of some Aythya spp.; used without qualification in Britain for A. marila (see DUCK). SCHIZOGNATHOUS: see PALATE (Neognathous). SCHIZORHINAL: see NARIS. SCIMITAR-BABBLER: see BABBLER. SCIMITAR-BILL: substantive name of Rhinopomastus spp. (see WOOD-HOOPOE).

SCISSOR-BILL: alternative substantive name of species of Rynchopidae (see SKIMMER). SCLEROPHYLL FOREST: evergreen forest in which the dominant tree species have hard leathery leaves normally less than c. 10cm long, resistant to water loss. Very variable in species composition, occurring throughout the world in areas with periodic (usually seasonal) water shortage. SCLEROTIC: see SKULL;

VISION.

SCLERURINAE: see OVENBIRD

(1).

SCOLOPACIDAE: see under CHARADRIIFORMES. The family includes species known as 'woodcock', 'snipe', 'sandpipers', 'curlews', and 'godwits', and by various special names (see under SANDPIPER). SCOPI; SCOPIDAE: suborder and family of CICONIIFORMES;

HAMER-

KOP.

SCOTER: substantive name of Melanitta spp. (see DUCK). SCRAPE: a shallow water-filled hollow excavated to attract water birds. See also NEST SCRAPE. SCRATCHING: for head scratching see COMFORT BEHAVIOUR; for scratching the ground see FEEDING HABITS. See photo COMFORT BEHAVIOUR.

Scrub-bird

525

several days and stay in wet areas until they are old enough to run to safety. Black-necked Screamer adults feed chicks in captivity. M.W.W. Bell, J., Bruning, D. & Winnegar, A. 1970. Black-necked Screamers seen feeding a chick. Auk 87: 80S. DeMay, I.S. 1940. A study of the pterylosis and pneumaticity of the screamer. Condor 42: 112-118. Gill, F.B., Stokes, F.]. & Stokes, C.C. 1974. Observations on the Horned Screamer. Wilson Bull. 86: 43-50. Gizels, K. 1969. Systematic position of the Screamers (Anseriformes, Anhimidae): Data on immunological analysis of protein composition in lenses. So. Zool. Zh. 45: 1202-1206. Haffer, ]. 1969. Notes on the wing and tail molt of the screamers, the sunbittern, and immature guans. Auk 85: 633-638. Rumboll, M.A.E. 1975. Espolones metacarpales del chaia (Chauna torquatai. EI Homero 9: 316. Stonor, C.R. 1939. Notes on the breeding habits of the Common Screamer (Chauna torquata). Ibis 81: 45-49. Weller, M.W. 1967. Notes on some marsh birds of Cape San Antonio, Argentina. Ibis. 109: 391-411.

Crested Screamer Chauna torquata. (C.E. T.K.).

SCREAMER: substantive name of the 3 species of Anhimidae (Anseriformes, suborder Anhimae). Characteristics. Screamers are goose-like birds (length 69-90 cm) with heavy bodies and small heads, but longer, fleshy legs, and semi-palmate feet with the hind toe long and not elevated. The bill is more like that of gallinaceous birds. On the leading edge of wing are 2 spurs 2-5 em long which shed their outer layers periodically. Such shells found imbedded in breasts of other screamers suggest that the spurs are used in aggressive encounters. One species has a long (up to 15cm) cartilaginous horn attached to the crown, but its delicate structure suggests decoration rather than armament. Screamers are unique in lacking uncinate processes on the ribs that provide support for the delicate body cage of other living birds. Unlike other waterfowl, they lack well-defined feather tracts, simultaneous wing moult and copulatory organ. Small air cells between the skin and muscle are more widespread than even in Pelecaniformes and create rumbling or crackling noises on take-off. The sexes differ little in size. They swim well but high on the water and somewhat belaboured; diving has not been recorded. They are strong flyers and at least one species soars regularly. Habitat and distribution. The Crested Screamer Chauna torquata is grey with white and black rings on the neck. It is well known because of its extensive distribution in the pampas of Argentina, Uruguay and southern Brazil and in the subtropics in Bolivia and Paraguay. Crested Screamers are most numerous near marshes where they may graze with livestock. Pairs and flocks roost in shallow water at night. The Blacknecked Screamer Chauna chauaria occurs in a small area in Colombia and Venezuela, and differs from the Crested Screamer in its more extensive black neck, chin and face. The largest of the 3 is the Horned Screamer Anhima cornuta of the tropical savannas of the Guianas, northern Venezuela, Colombia, western Ecuador, Peru, Brazil and Bolivia. Whereas the other 2 screamers are predominantly grey, this species is a glossy greenish-black. Horned Screamers perch in trees regularly, where they probably roost overnight, and like other screamers, feed on grasses and sedges near water. Food. Screamers are herbivores that graze near lakes and marshes or feed on aquatic plants. Insects are thought to be taken by or for young. Behaviour. Information is based mostly on studies of Crested Screamers. Pairs are obvious year-round, but they seek isolation in marshy areas in late winter or early spring where they trumpet (duet) and mutualpreen. Mating occurs on land. Large flocks of non-breeding birds suggest that maturation is delayed for several years. Voice. They are highly vocal birds with piercing trumpet-like alarm calls, also uttered while soaring. Breeding. The nest is constructed of aquatic plants or sticks, usually over water. Both sexes build the nest and probably incubate. Down is rare or lacking in nests. Four to 7 eggs are laid at intervals of 35-40 h, and incubation requires 43-45 days. The young remain in or near the nest for

SCRUB-BIRD: substantive name of the 2 species of the Atrichornithidae (Passeriformes, suborder Oscines); in the plural the general term for the family. Characteristics. The Noisy Scrub-bird Atrichornis clamosus (21 em) and the Rufous Scrub-bird A. rufescens (16cm) are small terrestrial birds with strong pointed bills; long powerful legs; short rounded wings and long graduated tails. The dorsal plumage is brown (more rufous in A. rufescens) with fine black cross bars; the ventral plumage grades from white on the chin to rufous at the vent. Males are larger and also have a black bar across the upper chest which in A. rufescens extends down the flanks. Systematics. Traditionally, this small endemic Australian family has been grouped with the lyrebirds in the suboscine suborder Menurae. This arrangement is based mainly on the facts that both families have only 3 pairs of intrinsic syringeal muscles compared to 4 in other Passeres, and that the lower tracheal rings are not fused into a 'drum'. In addition, certain skeletal features such as the rudimentary clavicles in the scrub-birds and the number of flight and tail feathers in the lyrebirds were used to support this arrangement. Both families are ancient and relict members of the Australian avifauna. Habitat. Both species are primarily birds of wet forest, and occupy the ecotone between forest and swamp or where the canopy is broken. Such areas have a ..dense zone of shrubs and rushes, which provides essential nest sites, nest material and cover. The feeding habitat is on the forest side of this zone where the decreased density of shrubs and rushes allows the development of a litter layer which is the main food source. The only known population of the Noisy Scrub-bird is confined to the narrow gullies and soakage lines on an elevated headland of about 2,000ha. The Rufous Scrub-bird is found in scattered areas of suitable habitat. Distribution. The scrub-birds have an interrupted distribution. A. clamosus is only known from an isolated headland on the south coast of Western Australia, while A. rufescens is found in a small number of isolated montane locations from southern Queensland to northern New South Wales. Though formerly more widespread, the reduced distribution and population of scrub-birds since the mid 1800s has been caused by the destruction of habitat for agricultural pursuits and forestry and by the increased frequency with which their habitat has been burnt. Drought and introduced predators may also have played a minor role. Populations. Because of the dense habitat and their secretive habits no census of scrub-birds is possible, but counts of singing males provide an index of the number of breeding pairs. During the 1960s the number of A. clamosus breeding pairs was of the order of 40-50; since 1970 the number has increased from 45 to 138 in 1983. It is unlikely that there are more than a few hundred breeding pairs of A. rufescens. Food. Both species are generalized insectivores, who may also prey occasionally on small lizards or frogs. Most of their prey is obtained from the litter layer which they poke into or turn over with a sideways flick of the bill. Occasionally they flush insects by a rapid drumming on one foot on the litter, or more rarely by vibrating the erected breast feathers on the litter. Less frequently, they hunt insects at the base of lower levels of the rushes and shrubs that form the understorey of their habitat. Behaviour. Scrub-birds are fast, alert ground-dwelling birds, who

526 Scrub-bird

the wild. For about 7 days after hatching the female broods after each feed, but subsequently only at night. The chick fledges at about 25 days, after which it stays with the female, probably until the start of the next breeding season. Chicks are fed a wide variety of invertebrates and occasionally a small lizard or frog. The female removes the faecal sacs which she deposits in a stream or under a bush. If the egg is lost, the female will build another nest and relay. Little is known of the breeding of A. rufescens, but it is probably similar to A. clamosus except that 2 eggs are laid and the nest is completely lined. Conservation. Following the rediscovery of A. clamosus in 1961, a reserve was established with a resident ranger. Constant policing and the development of a fire-break system have prevented any fires in this area since 1970. The consequent regeneration of habitat has contributed to the increase in population since 1970. In the short term the population appears reasonably secure. In 1975/76 a captive colony of 1 male and 3 females was established and in 1979 the first chick was successfully reared. Knowledge of how to breed the species in captivity should assist in the long term survival of the species. A. rufescens, although rare, is not endangered because all the known localities are within National Parks and are of sufficient number that its long term survival seems as assured. G.T.S.

Noisy Scrub-bird Atrichornis clamosus. (N. w.e.).

rarely fly and then only a few metres. They are seldom seen, and usually only the song of the male indicates their presence. A. clamosus male territories are well dispersed and adjacent males rarely make contact except by song. Their territories range from 5-10 ha, within which the males may spend up to 800/0 of their time in an area of 1-2 ha centred on the best feeding places. Males have a number of roosting sites in trees or taller shrubs away from their feeding area to which they move after sunset and leave before sunrise. Males are generally monogamous, although they may mate with females on adjacent territories who have lost their mates. Polygamy was observed in the captive colony. Females occupy areas with suitable breeding habitat and good feeding on the periphery or away from the males' preferred station. They nest in the same area year after year and only move their site after losing the egg or chick. The little contact between males and females is probably confined to the breeding season. At its beginning, young males may occupy territories in sub-optimal habitat for 1-15 weeks. They do not develop their territorial song until the second, and may not be sexually mature until their third year. Females may breed in their first year and, if they cannot acquire a territory, may nest adjacent to an established pair. What little is known of A. rufescens suggests that it is similar to A. clamosus except that the males only defend their territories during the breeding season. Voice. The male A. clamosus has a loud and far reaching territorial song of 10-20 notes. Individual males may have 4 or 5 song patterns, all of which may be given in the same bout of singing. Males within hearing distance of each other have similar patterns of song. These continually change and the songs of any group may be quite different from year to year. The plasticity of the song pattern is in marked contrast to that of A. rufescens which has a very stereotyped and simple song not varying significantly throughout its range. A. clamosus males have another song, briefer than territorial song, more variable and of lower intensity, and which incorporates modified segments of the song of other species; it is used in interactions with other scrub-birds. In similar situations A. rufescens uses pure mimicry. A. clamosus also has a three-note call and two alarm notes. These alarm notes are the only vocalizations of the females of both species. Breeding. Both species breed during the wet season, winter for A. clamosus and spring/summer for A. rufescens. The male A. clamosus plays no role in nest building, incubation, feeding the chick or nest sanitation. The female builds a domed nest with a side entrance, lining the bottom with decayed rushes or wood which dries hard. Nests are built close to the ground, usually near a stream, and take about 3 weeks to build; the single egg is laid 1-2 weeks after the nest is completed. Incubation takes 36-38 days in the wild, but only 30-33 days in captivity. The difference may be attributed to the increased time needed to feed in

Chisholm, A.H. 1951. The story of the scrub-birds. Emu 51: 285-297. Smith, G.T. 1976. Ecological and behavioural comparisons between Atrichornithidae and Menuridae. Proc. XVI Int. Orn. Congr.: 125-136. Smith, G.T. 1977. The effect of environmental change on six rare birds. Emu 77: 173-179. Smith, G.T. & Forrester, R.I. 1981. The status of the Noisy Scrub-bird Atrichornis clamosus. BioI. Conserv. 19: 239-254. Smith, G.T., Nicholls, C.A., Moore, L.A. & Davis, H. 1983. The results of a breeding program for the Noisy Scrub-bird (Atrichornis clamosus) in captivity. West. Aust. Nat. 15: 151-157. Smith, G.T. & Robinson, F.N. 1976. The Noisy Scrub-bird-an interim report. Emu 76: 37-42.

SCRUB-FOWL: name sometimes applied to Megapodius spp. (see MEGAPODE).

SCRUB-ROBIN: substantive name of Drymodes spp. (see RAILalso used for Erythropygia (or 'Cercotrichas') spp., alternatively 'bush-robins' or (in one case) 'Rufous Warbler' (for families see WARBLER (1); THRUSH).

BABBLER; THRUSH);

SCRUB-WREN: substantive name of Sericornis spp. (see

WARBLER,

AUSTRALIAN).

SCUTELLATE: term applied to a podotheca consisting of rather large and often overlapping scales (see LEG). SCYTHEBILL: substantive name (formerly 'sicklebill') of Campylorhynchus spp. (see WOODCREEPER). SEA EAGLE: see HAWK (True kites and fish eagles). SEARCH IMAGE: a predator can be said to 'adopt a Search Image' when it can be shown that it has learnt to see prey which it at first overlooked. Many of the insects and other animals which are preyed upon by birds are highly camouflaged in that their colour and patterning blend in very closely with their background. Birds have, nevertheless, been shown to be able to 'break' the camouflage when they have had experience of finding a particular type of prey. As an example of this, de Ruiter (1952) found that, when Jays Garrulus glandariusand Chaffinches Fringilla coelebs were first shown the stick-like caterpillars of geometrid moths resting among twigs, they apparently failed to see them. But although the birds took a long time to find their first caterpillar, some birds which had eventually found an insect were then able to pick out the other insects without difficulty. They were thus 'taken in' by the camouflage at first, but were able to detect the difference between sticks and caterpillars after they had sampled the first insects. The birds could then be described as having adopted a Search Image for stick insects. Similar phenomena have been observed in crows, domestic chicks and other birds. It should be pointed out, however, that not everyone uses the term Search Image in the same way. Some people use the term to cover cases where a predator simply develops a taste for a type of food even when it is not camouflaged, and there is no suggestion of a change in how easily the

Secretary-bird

527

predator can see it. (The predator might just be learning, for example, which of several conspicuous foods are best to eat.) These different uses have led to confusion and, in some quarters, a feeling that the term should be dropped altogether. But without it, we would have no name to give the process of a predator learning to see through its prey's camouflage. So, used in this restricted sense, the term Search Image does serve a useful function. It is a graphic way of describing an important behavioural phenomenon. M.D. de Ruiter, L. 1952. Some experiments on the camouflage of stick caterpillars. Behaviour 4: 222-232.

SEASONAL CHANGE: occurring in birds in respect of physiological condition and behaviour, and very often also of external appearance and location (either or both). The cycle of a bird's life is usually an annual one, linked with the recurring seasons-whether these be summer or winter, or wet season and dry (see RHYTHMS AND TIME MEASUREMENT; WEATHER AND BIRDS). The alternation in physiology and habits is, in adults, between reproductive and non-reproductive periods (see BREEDING SEASON). It may involve a greater or lesser degree of geographical displacement (see MIGRATION; and IRRUPTION). The physiological changes include the seasonal replacement of feathers and other integumentary structures (see MOULT). This mayor may not involve marked change in external appearance, as when there is a distinctive breeding plumage in one or both sexes (see PLUMAGE). SEA-SWALLOW: popular name for

Secretary-bird Sagittarius serpentarius. (K.J.W.).

TERN.

SEA-WATCHING: a form of BIRDWATCHING from a single observation point, usually a prominent headland, whence passing birds are counted and identified over a period of hours or days. Sometimes sea-watches are co-ordinated over a number of stations to yield comparative data. The term is not usually applied to watches from on board ship, which have been carried out all over the world, notably by the Royal Naval Birdwatching Society.

Characteristics. A large bird with a wing span of just over 2 m, weighing about 4 kg, and standing over 1m tall, characterized by long legs that are feathered to the inter-tarsal joints, a well-developed basal web which joins the 3 front toes, elongate central tail feathers and a loose crest of spatulate feathers on the nape. The hooked bill, display flights and carnivorous diet suggest affinitieswith large eagles. The long legs and nesting habits are stork-like, but there are also many similarities with the seriemas (Gruiformes) of South America. Bustards and cranes have also been suggested as relatives, but until the species is properly studied and homologous and convergent characters are separated, the true relationships will remain obscure. Habitat and distribution. The Secretary-bird is found in open savanna, grassland and steppe, shunning areas that are heavily wooded or densely vegetated or of broken terrain. It is found in Africa south of the Sahara desert, although fossils are known from France. Populations and movements. No regular movements are known, but in many areas and at certain seasons it is locally nomadic as food supplies fluctuate. Densities of a breeding pair per 45 km 2 (grassland in South

nestlings of ground-nesting birds (e.g. plovers) are also taken. All hunting is done while walking with long, measured strides over the ground, prey being immobilized by kicking with the short, stout toes and their nail-like claws. The reach attained with the long legs and agility obtained by using wing movements allow active prey to be killed, such as birds and mice, or dangerous prey avoided such as venomous snakes. If snakes cannot be subdued on the ground, they are taken aloft and dropped from a height. Small animals burnt in fires may be scavenged. Behaviour. Adults are usually in pairs, holding and residing in a territory as long as conditions permit. Numbers may congregate at water-holes to drink or bathe, or at temporarily abundant food sources such as grassland fires, but often these appear to be non-breeding birds. Territorial advertisement consists of soaring flights made almost daily and during the heat of the day, sometimes with calling, and defence may involve aerial chasing or running and kicking fights on the ground. Voice. The Secretary-bird is mostly silent, but has a variety of deep croaking calls. Loud croaking precedes breeding and is uttered perched or during display flights. A single high pitched croak signifies alarm, a deep croak indicates threat. Small chicks make a loud chucking noise, later croaking and sometimes they throw back their heads as they call. Mewing calls are made at roosts. Breeding. Displays consist of undulating diving flights by either sex, with croaking calls. The nest, which is used year after year, is built of sticks, weeds and grass and forms an extensive platform on top of a tree or bush, often rather low (3-7.s m above ground) and usually in a thorny species. The basin is lined with dry material, mainly grass tufts. Up to 3 white eggs, rather pointed, and small for the size of the bird, are laid at intervals of several days. Incubation proceeds for 45 days, almost entirely by the female, the male delivering food carried in the crop and regurgitated on the nest rim. The chicks hatch in white or grey down, the second down being darker, and the feathers appear on the crest when they are 3 weeks old. The female gives most attention to them at first, although either parent may brood and feed them. Within a month of hatching the female leaves the nestlings for much of the time to help the male search for food. At first a liquid diet, probably of partly digested food, is fed to the chicks, but later whole items are given and latterly the food is left on the nest for the chicks to feed themselves. They leave the nest 65-80 days after hatching, being barely able to fly, and spend about a month in the nest area learning to hunt before moving off to join the

but higher densities in richer environments or lower in more arid areas are likely. Food. Largely rodents, reptiles, large beetles and grasshoppers, but any small animal up to the size of a hare may be eaten if caught. Eggs and

the year, usually in spring or summer, and is probably linked to food availability. The immature bird resembles the adult but has a pale grey eye (which is hazel in the adult) with black barring on the underwing and undertail coverts (both white in the adult). A.C.K.

SECONDARY: or 'secondary feather', anyone of the flight feathers borne on the forearm (ulna), as contrasted with the 'primaries' borne on the manus (see PRIMARY; also PLUMAGE; WING); they are sometimes called 'cubitals'. The secondaries are customarily numbered inwards from the carpal joint. SECONDARY COVERTS: see TOPOGRAPHY. SECONDARY SEXUAL CHARACTERS: see

SEXUAL DIMOR-

PHISM.

SECRETARY-BIRD: Sagittarius serpentarius; sole extant speciesin the Sagittariidae, a family currently placed in the Accipitriformes, suborder Sagittarii,

Africa) to one per 20 km2 (tropical savanna in South Africa) are known,

parents on their foraging expeditions. Breeding may occur at any time of

528 Secretion, internal

Brown, L.H. & Amadon, D. 1968. Eagles, Hawks and Falcons of the World. Feltham. Kemp, A.C. & M.l. 1978. Bucorous and Sagittarius: two modes of terrestrial predation. Proc. Symp. Afr. Predatory Birds. pp. 13-16. van Someren, V.G.L. 1956. Days with birds. Fieldiana: Zoology 38.

SECRETION, INTERNAL: see

ENDOCRINOLOGY AND THE REPRO-

DUCTIVE SYSTEM.

SEDENTARY: commonly used in the special sense of 'non-migratory' (compare RESIDENT). SEED..CRACKER: substantive name of Pyrenestes spp. (see ESTRILDID FINCH).

SEED DISPERSAL: in this context, the dispersal of seeds, and hence of the plants producing them, by birds. Many seed-eating birds act as distributors; they do so, however, more or less accidentally, by failing to digest a proportion of the seeds or by dying with a full crop or stomach. Nevertheless, by such means plants are on occasion dispersed over great distances (Ridley 1930). A primary distinction should be made between such birds, which are essentially seed-predators (although some, such as the parrots and many pigeons, are commonly referred to as frugivores), and the true or 'legitimate' frugivores, which digest the fleshy parts of fruits and void the seeds intact. Avian frugivores of the latter sort are the main distributors of many trees, shrubs and epiphytic plants, and of a smaller number of herbaceous plants. They are especially numerous in tropical forest, and the interaction between them and their food plants has led to mutual adaptations (see COEVOLUTION). There is reason to think that fleshy fruits of the kind eaten by birds evolved early in the history of the flowering plants in equable, tropical conditions; and that other kinds of fruits, such as those dispersed by wind, evolved later, perhaps in association with the climatic deterioration that took place during the Pliocene. The interaction between a frugivorous bird and its food plant is in the nature of a bargain: the bird obtains nourishment from the fleshy part of the fruit, and in exchange disperses the seed or seeds. To understand the details of the bargain, in particular the benefits obtained by each party, it is necessary to know the relative mass of flesh and seed, the number of seeds per fruit, the nutritive content of the flesh, the proportion of the crop harvested by the frugivore, the distances and sites at which the seeds are dropped, and many other things. In spite of much recent research on frugivory in birds, few studies have been thorough enough to give quantitative data on all of the important factors, and generalizations remain tentative. A broad distinction can be drawn between unspecialized and specialized frugivores, and between the kinds of fruit on which they feed. An unspecialized frugivore is one that regularly takes other foods besides fruit, and cannot subsist indefinitely on fruit alone. It is typically an opportunist, taking fruits as and when they become available. In order to attract unspecialized frugivores, it will be advantageous for a plant to have conspicuous fruits and a well-synchronized fruit crop. The fruits are usually borne in profusion, and linked with this, the nutritive content of individual fruits is not very high; they tend to be watery (succulent) and to contain mainly sugars and little fat or protein. Typically they are small, and contain small seeds. Many small trees and shrubs that colonize clearings, edge habitats and other transient areas of secondary vegetation have fruits of this unspecialized sort. As colonizers of temporary open ground, they tend to be in competition with one another, not only for ground space but also for dispersal agents. Thrushes, tanagers in tropical America, and bulbuls in the Old World tropics are typical unspecialized frugivores. It is characteristic especially of the tropics that temporarily superabundant supplies of unspecialized fruit are exploited by birds of many families that are not usually thought of as frugivorous, e.g. woodpeckers and tyrant-flycatchers. Many plant families produce unspecialized fruits, among the most important in the tropics being the Rubiaceae and Melastomataceae, and in North Temperate regions the Rosaceae and Caprifoliaceae. Specialized frugivores are typically larger birds than unspecialized frugivores, and the fruits that they eat are correspondingly large. Plants producing such fruits are mainly trees of primary tropical and subtropical forest. A common type of fruit consists of a single seed surrounded by a dense and nutritious, and often surprisingly thin, layer of flesh. Specialized frugivores process such fruits remarkably quickly, stripping off the flesh and regurgitating the large seed, which represents so much useless

ballast, intact. In another common type of nutritious fruit the seed is partly or entirely covered by an aril, which is an edible outgrowth of the seed itself. A number of fruits of both these types have been analysed and have been found to contain high percentages of fat and protein. Fruits of these kinds are often not very conspicuous, probably because they need to attract only a small number of regular frugivores which are likely to be resident and to know intimately the fruit resources available in their area. They also tend to be available over a longer period than the fruits that are produced in a mass to attract opportunist unspecialized frugivores. Specialized fruit-eating birds belong to fewer families than the unspecialized fruit-eaters, and are mainly tropical. The most important families are the toucans and cotingas in the American tropics, the turacos in Africa, the horn bills in Africa and south-east Asia, the birds-ofparadise in Australasia, and the true fruit-pigeons (Columbidae, genera Ducula, Alectroenas and Ptilinopus only, other pigeons being seedpredators) in south-east Asia and Australasia. Trees producing fruits adapted for specialized frugivores belong to a variety of families, the Palmae, Lauraceae and Burseraceae being of outstanding importance. A limited number of birds in all the main tropical and subtropical areas are specialized feeders on the fruits of mistletoes (Loranthaceae) and the chief dispersers of these plants. Some epiphytic plants may also be dispersed by these birds (bromeliads, aroids, and the epiphytic cactus Rhipsalis). The coevolutionary relationship between bird and plant is close, and there are some special features that set it apart from the typical bird-fruit relationship discussed above. The birds are mostly small (as are the fruits), with short and rather stout bills, and may have highly modified digestive systems. Effective dispersal depends on the seeds being lodged in a crack on a tree branch, and the fruits are adapted for this by having the seed embedded in a sticky coating which resists digestion in a bird's gut. The bird either swallows the fruits whole and passes them very rapidly through the alimentary canal, voiding them with their sticky coating intact so that they adhere to the branch on which they land, or squeezes the fruit in the bill, swallows the skin and pulp, and wipes the seeds off onto the branch on which it is perched. The most important mistletoe-berry eaters are the mistletoe-birds (Dicaeidae) of south-east Asia and Australasia, the small neotropical tanagers of the genera Euphonia and Chlorophonia, and the small African barbets of the genus Pogoniulus. A few species of other families are also more or less specialized eaters of mistletoe berries, for instance the Phainopepla Phainopepla nitens and the small neotropical flycatcher Tyranniscus vilissimus. Among the seed-predators there is one group of birds that have apparently co-evolved with the plants that they exploit and act as their main dispersal agents. They are seed-hoarders or 'scatter-hoarders', birds of temperate or boreal regions that bury large numbers of seeds in late summer and autumn and dig them up and eat them, or feed them to their young, in the following winter and spring. All those that are known are nutcrackers and jays (Corvidae). Storing food for later consumption is a widespread habit in the Corvidae and some other families, especially the tits and nuthatches, and all these birds must occasionallyact as dispersal agents for the plants whose seeds they store, but in most cases there is no evidence that they are the main dispersal agents or that any coevolutionary adaptations are involved. One species at least of pine, however, in the mountains of western North America, Pinus edulis, has co-evolved with Clark's Nutcracker Nucifraga columbiana and perhaps other corvids, producing seeds that are especially suitable for being harvested by the nutcracker. Similarly, the European Jay Garrulus glandarius is the main disperser of oak trees (Quercus spp.), and jays have probably been the main selective agent determining acorn size (Bossema 1979). (See also FOOD STORING.)

Seeds, and other parts of plants, furnished with hooks or barbs are occasionally distributed by birds, but probably are adapted primarily for dispersal by other kinds of animals. Birds may, however, be significant agents of dispersal of plants that they use for nest material. The melastomataceous herb Nepsera aquatica, whose fruiting panicles are used as nest lining by many small neotropical birds, may be mainly distributed in this way. Ridley (1930) gives other examples. No thorough study has, however, been made of the importance of birds as distributors of plants other than by ingesting or storing their seeds. See photo FEEDING HABITS. D. W.S. (1) Bossema, I. 1979. Jays and oaks: an ceo-ethological study of a symbiosis. Behaviour 70: 1-117. McKey, D. 1975. The ecology of coevolving seed dispersal systems. In Gilbert,

Semi-species

L.E. & Raven, P. (eds.). Coevolution of Animals and Plants. Austin. Ridley, H.N. 1930. The Dispersal of Plants throughout the World. Ashford. Snow, D.W. 1971. Evolutionary aspects of fruit-eating by birds. Ibis 113: 194-202. Vander Wall, S.B. & Balda, R. 1977. Coadaptarions of Clark's Nutcracker and the pinon pine for efficient seed harvest and dispersal. Ecol. Monogr. 47: 89-111. Walsberg, G.E. 1975. Digestive adaptations of Phainopepla nuens associated with the eating of mistletoe berries. Condor 77: 169-174.

SEEDEATER: substantive name of species of Sporophila and allied genera in the New World, and of Serinus spp. in southern Africa (for family see FINCH). SEED-FINCH: substantive name of certain small seed-eating species, particularly in the Neotropical genus Oryzoborus, also called 'rice grosbeaks' (for family see FINCH).

SEEDSNIPE: substantive name of the 4 species of Thinocoridae (Charadriiformes, suborder Charadrii, superfamily Thinocoroidea); in the plural (usually unchanged), general term for the family. The name derives from the birds' diet of seeds and other vegetable matter, and their snipe-like flight, including the bzeep take-off call, although they have no near relationship to snipe (Gallinago species, family Scolopacidae) on present evidence. Seedsnipe are undoubtedly charadriiform, but it has not yet been possible to establish which are their closest relatives. Characteristics. Seedsnipe are entirely South American and range in size from that of a quail Cotumix to that of a small partridge Perdix. The genus Thinocorus contains the 2 smaller species, the Least Seedsnipe T. rumicioorus (measuring about 18em and weighing 50-60 g) and the Grey-breasted Seedsnipe T. orbignyianus (measuring about 20em and weighing 110-140 g). The genus Attagis comprises the 2 larger species, the Rufous-bellied Seedsnipe A. gayi (about 30cm long and weighing 300-400g) and the similar-sized White-bellied Seedsnipe A. malouinus. They resemble doves (Columbidae) or sandgrouse (Pteroclididae) with plump bodies, small heads and short legs, but they have relatively long toes; the middle toe is as long as or longer than the tarsometatarsus. The bill is shaped rather like that of a partridge and the nostrils are protected by shield-like coverings. The plumage is cryptically coloured in grey, black, brown, white and rufous. The belly is white in the 2 Thinocorus species and in the White-bellied Seedsnipe, but rufous in the Rufousbellied Seedsnipe. Males of the 2 Thinocorus species have dove-grey breasts bordered ventrally by a black collar. The Least Seedsnipe also has a vertical black line joining a black-bordered white throat to the chest band to give an anchor-shaped effect. The 2 Attagis species have the breast finely marked with black. Sexual dimorphism is well developed in Thinocorus, but almost absent in Attagis. Seedsnipe all have long wings and are excellent fliers. Habitat and distribution. The White-bellied Seedsnipe lives on wind.. swept hilltops above the treeline on Tierra del Fuego and the islands south to Cape Horn; it also extends northward into the southernmost parts of the Andes in Chile and Argentina. The Rufous-bellied Seedsnipe, the largest and most strictly montane member of the family, lives just below the snowline in the puna or paramo zone of the Andes of Ecuador, Peru, Bolivia, Argentina and Chile up to about 5,500m. The Grey..breasted Seedsnipe is also an Andean bird, but of rather lower elevations, especially in the southern parts of its range in Patagonia and Tierra del Fuego where it inhabits open grasslands. The Least Seedsnipe is not montane, occurring in arid country down to sea level, from Ecuador in the north to northern Tierra del Fuego in the south. It is common in Argentine Patagonia. Movements. Southern populations of the Least Seedsnipe migrate northward in winter as far as the province of Buenos Aires; more northerly populations are sedentary or nomadic, especially in the more arid areas. The other species of seedsnipe may merely move to lower elevations in winter, but do not appear to undergo long migrations. Food. Seedsnipe spend most of their time on the ground feeding on seeds and green leaves. The arid..zone Least Seedsnipe feeds on succulent leaves as a source of water. None of the 4 species of seedsnipe appears to drink under natural conditions, although they will do so in captivity. Behaviour. During the breeding season seedsnipe are monogamous and move about in pairs or family groups. In winter when they are not breeding, the birds gather in large ftocks which are migratory or nomadic. They roost at night on the ground, often in groups, making shallow scrapes in which to lie. The males have characteristic territorial

529

flight displays in the breeding season, accompanied by a mellow song which may also be given from a perch on top of a rock or, in the case of the Least Seedsnipe, a bush or tall weed. Territorial males frequently fight vigorously at their territory boundaries. Voice. The songs of seedsnipe are mostly mellow-toned, incorporating hooting notes like pukupukupuku and may be uttered for many minutes at a time without a break. When taking off they give a short bzeep call like that of a snipe. Breeding. Seedsnipe nest on the ground, either in the open or next to a grass tuft or low shrub. They lay 4 eggs in a scrape filled with dry plant material. The eggs are usually creamy to pinkish in ground colour, spotted with shades of brown, grey and mauve. The White-bellied Seedsnipe and some females of southern populations of the Least Seedsnipe lay eggs of a greenish ground colour; this seems to be an adaptation to the greener habitats in the higher..rainfall regions inhabited by these birds. Incubation is by the female only in the Thinocorus species and possibly in the others too. Both Thmocorus species invariably cover their eggs completely with nest material when they leave the nest (whether to feed or when disturbed). The White-bellied Seedsnipe may also do so (although only one nest has ever been recorded), but the Rufous-bellied seems not to line its nest scrape thickly enough to allow of egg-covering. Where it occurs, egg-covering is done rapidly with side.. ways movements of the feet. An incubating female leaves the nest to feed for about an hour in the morning and again in the late afternoon. During the incubation period the male seedsnipe spends much time on a perch near the nest, where he acts as a lookout, giving a warning call and running away with the female as soon as danger is sighted. If disturbed suddenly at the nest, especially if she has not had time to cover the eggs, the female performs an elaborate injury-feigning distraction display as she ftutters away low over the ground. The incubation period of the Least Seedsnipe is about 26 days. The young are led away from the nest by both parents as soon as they are dry, but only the female broods them. From the start they feed by themselves on seeds and green leaves and do not need to be shown food by their parents. Like the adults they do not normally drink water. The young fty at about 7 weeks of age. If disturbed with young, both parents will perform distraction displays, but those of the male are less elaborate, usually consisting only of the 'rodent-run' typical of waders (see DISTRACTION BEHAVIOUR). See photo COLORATION, ADAPTIVE. G.L.M. Humphrey, P.S., Bridge, D., Reynolds, P.W. & Peterson, R.T. 1970. Birds of Isla Grande (Tierra del Fuego). Preliminary Smithsonian Manual. Washington, D.C. Madean,..G.L. 1969. A study of seedsnipe in southern South America. Living Bird 8: 33-80. Sibley, C.G., Corbin, K.W. & Ahlquist, J.E. 1968. The relationships of the seed-snipe (Thinocoridae) as indicated by their egg white proteins and hemoglobins. Bonn. zool. Beitr. 19: 235-248.

SELECTION: see NATURAL SELECTION; and under SPECIATION. SEMATIC: serving as a signal, e.g. of warning or attraction. This adjective is the base of such terms-applied particularly to colorationas 'aposematic' (protective) and 'episematic' (aiding recognition), and of compounds thereof (see under APOSEMATIC; EPISEMATIC); also GAMOSEMATIC. 'Allosematic' (adventitiously derived from association with other organisms-see NESTING ASSOCIATION), and 'parasematic' (deftecting attention from one part of the body to another, e.g. from more to less vulnerable parts). Not all such terms as these have application in ornithology. See, in general, COLORATION, ADAPTIVE. SEMICIRCULAR CANALS: in the ear (see HEARING

AND BALANCE).

SEMIPALMATE: half webbed. SEMIPLUME: a feather type intermediate between contour feather and down (see FEATHER; PLUMAGE). SEMI-PRECOCIAL: newly hatched young which have eyes open, are down covered, stay at the nest until able to walk and are fed by parents (see YOUNG BIRD).

SEMI-SPECIES: a term of convenience for geographically isolated forms, with obviously near relatives elsewhere, that may be either species (members of a superspecies) or subspecies, there being no way of applying the objective test.

530 Senescence

SENESCENCE: see under

AGE.

SENMURV: see FABULOUS BIRDS. SEQUENCE: see ARRANGEMENT. SERAL COMMUNITY: a community of plants and animals associated with a stage of a SERE. For example, in Britain bare ground will develop through the seral stages of grassland, scrub and lowwoodland to deciduous forest. Each stage will have its characteristic seral community of birds. Grassland will support a bird community of Skylarks Alauda arvensis and Meadow Pipits Anthus pratensis, the low scrub stage species such as Dunnock Prunella modularis and Whitethroat Sylvia communis. A more advanced scrub seral stage will contain several warblers and Nightingales Luscinia megarhynchos, and the climax forest, with its components of mature and dead trees, a more varied community including tits Porus, Nuthatches Siua europaea, treecreepers Certhia and woodpeckers. SERE: a series of plant communities leading to climax vegetation. SERICORNIS: substantive name of some Australasian warblers of the genus Sericornis (for family see WARBLER, AUSTRALIAN). SERIEMA: substantive name of the 2 species of Cariamidae (Gruiformes, suborder Cariamae); in the plural, general term for the family. The birds are to be found in the drier areas in south-central South America. The common name is derived from the Tupi word 'cariama', rendered in Latin as Cariama by Marcgrave in his account published in 1648, copied by Willughby in his Ornithologia of 1676, and so given in many subsequent accounts. Seriema, a modification of the original American Indian word used in Brazil, is preferred and is now replacing the other form in current ornithological writings. Numerous fossil species related to the modern Cariamidae have been described from middle Tertiary beds of Argentina, and a closely related fossil family, the Bathornithidae, with 4 species described in the genus Bathornis, was common during Oligocene time in the Great Plains area of North America. Characteristics, habitat and distribution. Seriemas are allied to cranes (Gruidae) and rails (Rallidae), and are placed in the same order. They show resemblance in form to small cranes (lengths 66-86cm) as they have long necks, long slender legs, and elongated muscular bodies. The head is heavily feathered, with a frontal crest, the tail is long, and the wings are rounded. The Crested Seriema Cariama cnstata, which ranges from central and eastern Brazil south through Paraguay to northern Argentina and Uruguay, is the best known, from its wide distribution and from the fact that the young are readily domesticated and are often taken and reared among fowls, where they serve efficientlyas guardians to give warning of predators. The Crested Seriema, which stands about 76em tall, is greyish-brown in colour with fine darker vermiculations throughout; the wings and tail are broadly banded with black and white, and the feathers of the underparts have pale longitudinal streaks. The frontal crest is conspicuous, and the bill and legs are red. It lives in areas of open scrub mixed with grasslands, where it moves about on foot and runs rapidly to escape any enemy. Burmeister's Seriema Chunga burmeisteri, found only in Argentina and the western Chaco of Paraguay, is somewhat smaller, with a much less conspicuous frontal crest. It is greyer in plumage, unstreaked below and with a creamy white belly, and the bill and legs are black. It lives in areas of rather open, thorny woodland, where it ranges the ground like the other species. As they are hunted for game, they are wary, so that except for occasional distant glimpses of birds running swiftly through cover their presence is known mainly through their high-pitched yelping calls. Food. Both species of the family are omnivorous in feeding, and are among those birds that regularly eat smaller snakes of any kind. The common supposition that seriemas have an immunity to the venom of the poisonous species is not true, since it has been found experimentally that birds of both species were killed by injections of attenuated amounts of a crotaline snake poison. Voice. The loud calls of both seriemas often indicate their presence when the birds themselves are not seen. Breeding. The nest of the Crested Seriema, rather compactly made of

Crested Seriema Cariama cristata. (C.J.F.G.).

sticks, is recorded up to 3 m above the ground. The eggs, which regularly number 2, are faintly pink when fresh but fade to dull white, sparingly marked with lines or small blotches of brown that appear dark grey or dull purple where overlaid by deposits of shell. The young, covered with dark down when hatched, remain in the nest under the care of the parents until well grown. The nest of Burmeister's Seriema is located low in trees, and the 2 eggs are similar to those of the other species but with heavier markings. A.W. (D.W.S. (1»).

SERIN: substantive name of most Serinus spp.; used without qualification, in Britain, for S. serinus (see FINCH). SEROLOGICAL CHARACTERS: those expressing differences between species in respect of the chemical nature of the proteins in, particularly, the blood serum-as shown by precipitation reactions and other tests. These proteins (also referred to as 'antigens' or 'serum globulins') represent an important part of the animal constitution and are conservative hereditary traits; they are thus of potential value as supplementary taxonomic criteria; and the same applies to the albumens of egg-white (see DNA AND PROTEINS AS SOURCES OF TAXONOMIC DATA; TAXONOMY).

SERPENT EAGLE: same as eagles). SERTOLI CELLS: see (Reproduction).

HARRIER EAGLE

(and see

HAWK

(Snake

ENDOCRINOLOGY AND THE REPRODUCTIVE

SYSTEM

SERUM: see BLOOD;

SEROLOGICAL CHARACTERS.

SESAMOID: term applied to small, isolated pieces of bone or cartilage formed in tendons or ligaments. SET: in respect of eggs, has the same meaning as CLUTCH (see also EGG). SETOSE: carrying bristle-like feathers. SEVEN SISTERS: name applied collectively to parties of the Jungle Babbler Turdoides striatus in India, from the habit of associating in small bands, often of about 7 birds, at all times of year (see BABBLER). Whistler points out that there is a vernacular (but masculine) equivalent, 'sathbhai', in which the numeral is used in an approximate sense. Related species have similar habits and may sometimes have the term applied to them. SEX, CHANGE OF: see OVOTESTIS. SEX, DETERMINATION OF: see GENETICS. SEXUAL CHARACTERS: those differentiating male and female. Primary sexual characters are the testis and ovary; accessory sexual characters are other parts of the reproductive system (see ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM); secondary sexual characters are

Sexual dimorphism

531

those, apart from the foregoing , in which the sexes differ-in bird s, notab ly in plum age and voice, sometimes also in size (see below). SEXUAL DIMORPHISM: the existence of differences in appearance between male and female members of a species. (For dim orphi sm not related to sex, see POLYMORPHISM. ) Th ere are differences of size, structure, shape, plumage and coloration . Although sexual differences in behaviour (for example, singing by males but not by females) should not strictly be referred to as sexual 'dimorphism', because morphology means the study of physical form , in fact most of the theories of sexual dimorph ism apply both to sexual differences in form and in behaviour. Kinds of sexual dimorphism. Most sexual dim orphism in bird s is of size and shape, and of coloration . There are a few example s of stru ctu ral dimorphi sm . The bill of the extin ct Hu ia H eteralocha acutirostris is one (see WATTLEBIRD ( 2) ) . Th e male's bill was relatively short, straight, and stout; the female's was longer , more slender, and more curved . Sexual differences in size are found in many species. T he Capercaillie Tetrao urogallus is an extreme example , in which the male is more than twice the weight of the female. In the American JacanaJacana spinosa, by contrast, the female is 75% heavier than the male. In most species there is smaller (less than about 10% of body weight ) sexual dimorphism in weight , and males tend to be the heavier sex. Pluma ge dimorphism is the main source of sexual differences of colour, although in some species the bills or th e legs are of different colours. The sexual dimorph ism of the Peafowl Pa vo cristatus is largely due to the greater development in the male of the upp er tail-coverts, to form the beautiful metallic green train with its array of eye-spots. Similarly bizarr e plumage differen ces are found in the bird s-of-paradi se (Paradisaeidae). For instance, in the King of Saxony Bird-of-Paradise Ptendophora alberti, the male has two plume s, one growing out of each side of his head . Th e plumes are about 45 em long, which is twice the length of the rest of the bird . In most sexually dimorphic species the sexes show the same constant sex difference throughout the year . But th is rule is not universal. In the phalaropes, for example , the males and female both moult into a very similar winter plumage, but in the summer they moult into differing plumages, the female being more brightl y coloured. Theories of sexual dimorphism. The general reason for the evolution of sexual dimorphi sm is that natural selection can favour different characters in males and in females. There are three part icular theories, variously invoking sex differenc es in reproduction (' sexual selection' ), in feeding, and in risk of predation . Sexual selection. The theory of SEXUAL SELECTIO N was invented by Charles Darwin, who used it in his book The Descent of Man , and S election in relation 10 Sex (1871) to explain sexual dimorphism in bird s. Sexual dimorphism , he argued , evolves when males (substitu te 'females' in role-reversed species) with certain characteristics mate more than do males with other characteristics. The mating advantage might be due either to success in competition with other males, or because females preferent ially mate with males that possess some part icular characteristic. Preferential mating by females with the most extravagantl y adorned males is the most likely explan ation of the extreme sexual dimorphism such as that found in the Peafowl. Sexual selection is the only known theory which can explain the evolution of deleterious sexually-dimorphic characters, characters that redu ce survival. Th e Peacock would probably survive better without his long train , but the train might still be a net benefit if it conferred a sufficient advant age in mating. Males, then , in these sexually dim orp hic species may have a higher mortality rate than females. There are few observations testing this supposition . In one study of the Great-t ailed Grackle Quiscalus mexicanus the sex ratio among nestlings was found to be I : I. Tw o samples of adult s revealed female biased sex ratios (43% and 29% males in the two samples of939 and 1,349 individuals). Th e male Great-tailed Grackle is more brightly coloured and has a longer tail than the female. The bright colour might attract pred ators, and the long tail was observed to inhibit flight, especially in strong wind . Feeding. Some differences between the sexes may have evolved to reduce competition for food between the male and female of a pair . If the male and female have a different bill size, they may eat different food . Thus when the pair forage they will not compet e for the same food. For example, Selander (1972) studied the feeding habit s of male and female melanerpine woodpe cker s M elanerpes spp., which live on Caribb ean Island s, and in central Amer ica. The species inhabiting the islands of

Stonecha t S axicola torquata male (above) and female (below) showing sexual dimorphism . (P holO: J .B . & S . Bottomley).

H ispaniola and Puerto Rico have bills which are strongly sexually dim orphic . When Selander watched the feeding habits of the two sexes he found differen ces. The male and the female therefore probably take different food. To prove th at sexual dimorphism serves to redu ce competition for food between males and females it is not enough to show that males and females take different food. It mu st also be shown that food is in so short a supply that the pair catch more food than if the y were not dim orphi c. That food is in sufficiently shor t supply in th e melanerpine woodp eckers has not been pr oved , but it is a reasonable assum ption. Predation. Th e colours of birds may act as signals of various kinds to predators. The most important kind in the evolut ion of sexual dim orphism is probably the signal to the predator th at the signalling bird is an 'unprofitable pr ey'. Some kind s of prey are easy to catch , and so 'profitable' to the predator. Other s (' unprofitable') are less easy to catch . The pr eda tor would , if it could distingui sh the easy from the difficult pre y, concentrate on the easy catches . Thus if a bird is a difficult catch it may evolve bright coloration so that the predator , after a few failed attempts, will learn not to try to catch tha t kind of prey. Th e theory is very similar to the evolution of warn ing coloration in which pred ators learn to avoid sickening or distasteful prey by virt ue of its bright colorati on . That predators learn not to eat sickening prey has been proved in experiments. The two sexes may differ in how easy they are for a predator to catch. If one sex is bigger , it may be better able to fight back . If one sex has to sit on the eggs, it will not be able to run away from predators so easily as the other sex which is not tied to the eggs. The sex which sits on the eggs will

532 Sexual selection

then evolve camouflage-it will become cryptically coloured. The other sex will evolve to be conspicuous. The 'predation' theory predicts that the brightly coloured sex will be eaten less than the cryptic sex. This is the exact opposite of the prediction of the 'sexual selection' theory. As was noted above, few facts have been collected on sexual differences in mortality due to predation. Explaining trends in sexual dimorphism. The three theories are not completely exclusive of one another. Sexual dimorphism could be favoured at the same time both by sexual selection and by the reduction of competition for food. In other cases the theories are exclusive: the theories of sexual selection and of predation lead to exactly opposite predictions of the relative mortality of the two sexes. The different theories also explain different kinds of dimorphism. The feeding theory explains sexual dimorphism of the feeding organ such as the bill; the predation theory explains sexual dimorphism of coloration; the sexual selection theory is more versatile: it can in principle explain sexual dimorphism of coloration, or of the size of any parts of the bird. The main force in the evolution of sexual dimorphism would ideally be discovered by testing the three theories on many individual species. In the absence of such detailed studies, some idea of the main forces can be obtained by deriving different predictions from the three theories about which kinds of species should show sexual dimorphism and which should not. In all three theories there is a connection between the mating system and sexual dimorphism; but the connection is not the same in each case. If sexual dimorphism evolves to reduce competition for food between the sexes, sexual dimorphism should be commoner in monogamous than in polygamous species. If, for example, the breeding group is of one male and three females, all the females would compete for the same food, and sexual dimorphism would be ineffective in reducing competition. However, the general trend is the opposite. Sexual dimorphism tends to be greater in polygamous than in monogamous species. If sexual dimorphism does reduce competition for food, therefore, it is probably a secondary consequence. The theory of sexual selection predicts a greater degree of dimorphism in polygamous than in monogamous species because there is greater competition for mates in polygamous species. Species with the most extreme differences between the males in the number of matings should evolve the most extreme dimorphism. This prediction is borne out: the extremely polygamous LEK species tend to be the most dimorphic. Sexual selection also predicts 'reversed' sex dimorphism in role-reversed species such as jacanas and phalaropes. In these species only the males care for the young, so sexual selection is reversed and females compete for males. The predation theory makes similar predictions to the theory of sexual selection. If one sex cares for the young while the other is active, the more active sex will be more brightly coloured. So both theories predict the same patterns of sexual dimorphism in polygynous and polyandrous species. Sexual selection, feeding, and predation are the main (but not the only) factors affecting sexual dimorphism. We do not yet know their relative importance. See photos HEAT REGULATION; LEK. M.R. Baker, R.R. & Parker, G.A. 1979. The evolution of bird coloration. Philosophical Transactions of the Royal Society of London B287: 63-130. Selander, R.K. 1972. Sexual selection and dimorphism in birds. In Campbell, B. (ed.). Sexual Selection and the Descent of Man. London.

SEXUAL SELECTION: a form of natural selection resulting from competition between members of one sex for opportunities to mate with members of the opposite sex. Darwin pointed out that sexual selection could arise either by direct competition for access to members of the opposite sex, e.g. by fighting ('intrasexual selection') or by differences in ability to court members of the opposite sex ('epigamic' or 'intersexual selection'). The distinction is not absolute: males may compete with each other for high quality territories and females may choose to mate with males that possess such territories. Sexual selection often results in the production of characteristics, such as the bizarre plumage and exhausting courtship behaviour of the Ruff Philomachus pugnax, that benefits the individual but is wasteful in terms of the species as a whole. The realization that this is also true of other forms of natural selection has led evolutionists to consider sexual selection as part of natural selection, rather than as a distinct phenomenon (see NATURAL SELECTION). In general, the number of offspring a female produces does not depend on the number of males she mates with but on her capacity to produce eggs. Selection will generally favour females that only allow themselves to

be inseminated by males that are likely to have genetically fit offspring, since those offspring will bear the genetic output of the females. Males, however, can inseminate many females with little physiological effort, so selection generally favours males that inseminate any willing females, even females that are unlikely to produce many offspring. This is why females generally require to be courted whereas males are less discriminating. It is also why sexual selection is most intensive in males. In birds, parental care is important in determining the survival of offspring and a male may increase his reproductive output more by caring for the offspring of one mate than by striving to obtain many mates but not helping to raise his offspring. This is why birds are typically monogamous, in contrast to the majority of animals. In those species where paternal care is less important, polygyny prevails and there is more intensive sexual selection. Many polygynous species show marked SEXUAL DIMORPHISM, with elaborate male plumages and much effort put into competition between males. In species where males, not females, are mainly responsible for parental care, the males are a resource for which females compete, so that sexual selection is more intensive on the females than on the males, leading to 'sex-role reversal' (e.g. PHALAROPE). Though of reduced intensity, sexual selection still occurs in monogamous species. The members of each sex compete to mate with those members of the opposite sex that are likely to produce most surviving offspring, because they are ready to breed at the optimum season, are in possession of high quality territories, and are likely to be good parents. While the processes of intra sexual selection are easy to understand, those involved in epigamic selection are less dear. Such selection arises because females (usually) choose males with certain characters. If some females show a preference for a particular type of male, and the rest of the females show no preference, then the preferred type of male will be selectively favoured, other things being equal. Furthermore, as first noted by R.A. Fisher, the preference itself is selectively advantageous. Males of the preferred type, and thus the females that prefer them, will tend to produce sons of the preferred type; these will be selectively favoured because they are of the preferred type; thus their mothers, females showing the preference, will tend to produce more grandchildren than females that do not show the preference. Thus there is a runaway process in the joint establishment of the preference and the preferred characteristics. The female choice may originate in various ways. Its origin may be 'accidental', a by-product of other selective forces operating on the behavioural repertoire of the female. Alternatively females may choose mates that are likely to be good fathers, either because they are able to care for their offspring well or because they are likely to pass on to their offspring genes that will result in the offspring being genetically fit. Courtship feeding by terns, for example, may be a way in which a male demonstrates his fish-catching abilities, on which his success as a father partly depends, to a potential mate. Sexual selection may be important in the development of breeding barriers between species. Suppose that the hybrids between two populations are less fit than individuals of pure parentage, as may happen when the genetic constitutions of two populations originally of the same species come to diverge markedly. In each population, selection will favour those individuals that choose to mate only with members of their own population. The result will be the evolution of discriminatory behaviour and of species-specific recognition characters (see SPECIATION). J.J.D.G. Halliday, T. 1980. Sexual Strategy. Oxford. O'Donald, P. 1980. Genetic Models of Sexual Selection. Cambridge.

SHAFT: see FEATHER. SHAG: substantive name almost interchangeable with 'cormorant' for

Phalacrocorax spp.; but in the British Isles, each name standing alone, Shag means P. aristotelis and Cormorant means P. carbo (see CORMORANT).

SHAKESPEARE'S BIRDS: see POETRY,

BIRDS IN

(References).

SHAKETAIL: substantive name sometimes used for Cinclodes spp. (see OVENBIRD (1)). SHAMA: substantive name of some Copsychus spp .. (for subfamily see THRUSH).

Shikra

533

SHANK: a popular term for the whole or some part of the leg, lacking definition (see LEG). In such bird names as 'redshank' it clearly refers to the visible part of the leg, and especially to the so-called tarsus (which is in fact the foot, and thus not equivalent to any part of the human leg that would be thus termed). SHAPE AND POSTURE: see SIZE. SHARMING: grunts and squeals of a Water Rail Rallus aquaticus. SHARPBILL: substantive name of Oxyruncus cristatus, sole member of the family Oxyruncidae (Passeriformes, infraorder Tyranni). A Neotropical species with a rather discontinuous distribution in upper tropical and lower subtropical humid forests in Costa Rica, Panama, southeastern Venezuela, Guyana, Surinam, south-eastern Brazil and Paraguay. It is about 16em long with a stout, short-legged, small-headed appearance. The bill tapers from a broad base to a sharply pointed tip. The plumage is olive green above and pale yellow below, profusely spotted with black. A flattened crest with elongated scarlet feathers is present but usually concealed. The sexes are similar in appearance but males have a serrated outermost (lOth) primary of unknown function. Sharpbills are occasionally encountered among canopy-feeding flocks of barbets, honeycreepers and tanagers. Birds watched in the Serra dos Orgaos, Brazil, in December were feeding largely on invertebrates, 'caught with great agility from among the leaves in the very outermost twigs of the canopy. A common technique involved hanging upside down and feeding tit -like with rapid pecks into the bases of leaf-clusters' (Brooke et al 1983), to which the bird's sharp bill is well adapted. Stomach contents and other field observations suggest a diet mainly of berries. Males apparently call from expanded leks of 4 to 6 individuals. The advertisement call varies geographically but is basically a buzzy, highpitched, long-drawn-out whistle, which gradually descends in pitch. The first Sharpbill's nest was found in October 1980 in montane forest some 50km north of Rio de Janeiro. It was situated just below the higher leaves in the canopy of a 30 m tall tree. Only one bird, assumed from its drab plumage to be the female, was ever seen. The nest was a shallow cup made of leguminous petioles and a few dry leaves, coated with mosses, liverworts and spiders' webs, and was saddled, like a hummingbird's nest, on a slender horizontal branch. There were probably 2 eggs, which hatched after between 14 and 24 days' incubation; the fledging period was probably 25-30 days. N .G.S. Brooke, M. de L., Scott, D.A. & Teixeira, D.M. 1983. Some observations made at the first recorded nest of the Sharpbill Oxyruncus cristatus. Ibis 125: 259-261. (Contains useful list of references.) Mees, G. 1974. Additions to the avifauna of Suriname. Zoo!' Mededelingen 48: 55-67. Ridgely, R.S. 1976. A Guide to the Birds of Panama. Princeton. Wetmore, A. 1972. The Birds of the Republic of Panama, Part 3. Smithsonian Institution.

SHARPTAIL: abbreviated name of the Sharp-tailed Grouse Tympanuchus phasianellus (see GROUSE). SHEARTAIL: substantive name of Doricha spp. and Thaumastura cora (for family see HUMMINGBIRD). SHEARWATER: substantive name of certain species of Procellariidae, in the genera Puffinus, Procellaria, etc.; in the plural, a general term for these (see PETREL). The name is sometimes locally misapplied to other sea birds, e.g. Rynchops spp. (see SKIMMER). See photo NOCTURNAL HABITS. SHEATHBILL: substantive name of the 2 species of Chionidae

(Charadriiformes, usually placed in the suborder Charadrii); in the plural, general term for the family. Characteristics. Sheathbills are small white pigeon-like shorebirds 36-42 em long; biochemical indicators suggest slightly closer affinities with Lari than with Charadrii. 'Sheathbill' derives from the horny yellow-green sheath that covers the base of the short, stout bill. In American Sheath bills Chionis alba the bill is yellow and black, in the Lesser Sheathbill Chionis minor (which is slightly smaller) it is almost entirely black. The eyes are pink-rimmed and the cheeks bear wattles and patches which are small in juveniles, bigger in mature birds. The plumage is entirely white with grey underdown. The legs, blue-grey or pink, are short and stout, and the toes

Sheathbill Chionis alba. (B.P.).

have only vestigial webs. Although sheathbills have been seen in flight several hundred km from land and are capable of long migratory flights, they spend much of their time on the ground, trotting busily about the shore in search of food and showing reluctance to fly even when pursued. The wings are small, with sharp carpal spurs that the birds use in fighting. Males are slightly larger and heavier than females. Habitat and distribution. Sheathbills live on or close to the shore of islands in the sub-antarctic sectors of the Atlantic and Indian Oceans, often but not exclusively in association with penguin colonies. Sheathbills (or American Sheathbills) breed on South Georgia, the South Orkney and South Shetland Islands, possibly the South Sandwich Islands, and the Antarctic Peninsula to about 65°S; some winter in Patagonia, the Falkland Islands and Tierra del Fuego, others are resident through the year. Lesser sheathbills breed on Marion, Prince Edward and Heard Islands and lies Crozet and Kerguelen; island races are postulated. Food. Sheathbills feed on shore animals of the intertidal zone; they eat large quantities of Ulva and other algae, perhaps for the animals that live among them, and dig with their bills in crevices between rocks. Stranded plankton, faeces of seals and penguins, carcasses and offal of every kind are taken. On penguin colonies they scavenge for eggs and fallen chicks, darting between the brooding parents to pick up scraps of spilled food; some learn to flutter or peck at parents engaged in feeding their chicks, causing both to spill food. Though constantly in danger from darting beaks, they are usually quick enough to escape without harm. Behaviour. Between breeding seasons they live in small flocks, quarrelling frequently among themselves and feeding communally. They are inquisitive and enterprising in searching for food, quickly learning to associate with men at expedition bases and campsites. Voice. Sheathbills are usually silent; chicks have cheeping alarm and food calls, adults croaking or growling threat calls. Breeding. The nests are built in crevices and under boulders, often on a rocky headland overlooking a penguin colony. Sheathbills continue to feed gregariously but nest in isolation; nests are well hidden and approached indirectly. Two to 4 brown eggs, flecked with grey or black, are laid in December/January; incubation (both parents) takes 29 days. Chicks hatch asynchronously in brown down, changing to grey mesoptile down at 7 days and fledging in 7 to 9 weeks. Most pairs rear one or 2 chicks only. B.S. Burger, A.E. 1979. Breeding biology, moult and survival of Lesser sheathbills Chionis minor at Marion Island. Ardea 67: 1-14. Jones, N.V. 1963. The Sheathbill, Chionis alba (Gmelin), at Signy Island, South Orkney Islands. Bull. British Antarctic Survey 2: 53-71.

SHELDGEESE: general term for some larger species of Tadornini (Anatidae) (see under DUCK). SHELDUCK: substantive name of Tadorna spp.; used without qualification in Britain for T. tadorna, and sometimes written 'sheld-duck' or 'sheldrake' (see DUCK). SHELL-GLAND: or 'uterus', part of the oviduct (see

LAYING;

ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM).

SHIELD, FRONTAL: a hard, featherless plate extending from the base of the upper mandible backwards over the forehead, as in coots Fulica spp. and others (compare CASQUE).

SHIKRA: Accipiter badius (see HAWK).

534 Shoebill

SHOVELER: substantive name of some Anas spp.; used without qualification in Britain for A. clypeata (see DUCK).

family Pityriasididae. Recently the bush-shrikes have been placed in their own family Malaconotidae (see Benson and Benson (1977) for reasons and references) but Voous retains them as a subfamily of Laniidae. Sibley (1970) has emphasized, however, that relationships between shrikes are complicated by the frequency of convergence of the shrikelike bill, and similarities of egg white protein patterns of some bush-shrikes and true shrikes are not sufficient proof of a relationship between them. Of the 68 species of true shrikes and bush-shrikes recognized by Hall and Moreau (1970), the only ones not endemic to the Afrotropical Region are an isolated population of the Black-headed Tchagra Tchagra senegala in North Africa, and 13 species of Lanius which inhabit the Holarctic region, apart from a race of the Black-headed Shrike L. schach found in New Guinea. Six of the 8 Lanius species endemic to Africa are closely related to Eurasian species and a number of superspecies have been proposed (Hall and Moreau 1970, Mayr and Short 1970). Similarly Hall and Moreau have grouped 37 of the other 47 African shrikes into 9 superspecies. Their approach emphasizes the high degree of specialization and subsequent speciation that has occurred in African shrikes, and their groupings and nomenclature are followed here. They retain the genus Rhodophoneus, which Rand (1960) absorbs into Tchagra, and place the members of the genus Telophorus in Malaconotus. In the past these have been separated on the grounds of size but this ignores the remarkable evolutionary parallelism that exist in the 2 genera (White 1962). Systematic characteristics. All shrikes have a sharply hooked bill with a tooth in the upper bill and a corresponding notch in the lower mandible. Their legs and feet are strong and the claws sharp for catching prey. The wing has 10 primaries and the tail 12 rectrices. Malaconotinae. These are a mixed group. In some (Malaconotus) the bill is large and strong, in others (e.g. Tchagra) moderately so, and in others (Dryoscopus) relatively weak. The feathers on the rump are soft and elongated, particularly so in Laniarius and Dryoscopus. Seven genera are recognized: Lanioturdus, Nilaus, and Rhodophoneus (all monotypic), Dtyoscopus (6 species), Tchagra (5 species), Laniarius (15 species) and Malaconotus (16 species). In many species, but not all, the sexes are dimorphic. Their lengths range from medium (14.5-19.5 em) in Dryoscopus to large (18.5-27.0cm) in Malaconotus. Laniinae. These are the most typical of the shrike family. The bill is particularly strong and heavily notched, the external nostrils are oval and partly covered with small hairs, the rictal bristles are well developed, the tarsus scutellated only in front and lamellated behind. Two genera are recognized: Lanius (21 species) and Corvinella (2 species) which is occasionally split into a third genus Urolestes. The majority are sexually dimorphic. In Lanius lengths are in the range 15-31 em and in Corvinella 30-35cm. Field characteristics, habitat and distribution Malaconotinae. Of the 3 species in monotypic genera, the most widely distributed is the Brubru Nilaus afer. It inhabits moist and dry savanna woodlands north and south of the Equator and several races are recognized. Males are black above, females brown, and both are mottled with white and buff; the underparts are white with some chestnut. Four of the 6 puff-backs Dryoscopus spp. are placed in a superspecies. They are similarly patterned black, white and grey above and white below. Differences between males mainly lie in bill size; the females have distinctive colours. Usually they are allopatric but when sympatry occurs the species are always ecologically separated. The Black-backed Puffback Dryoscopus cubla occupies the mainly deciduous woodland in southern Africa and the Puff-back D. gambensis similar habitat in West Africa. The Black-shouldered Puff-back D. senegalensis occurs in secondary forest in Zaire and Nigeria, and Pringle's Puff-back D. pringliiin dry acacia steppe in north-east Africa. In contrast, the other puff-backs are forest birds. The tchagras have rufous wings, brown backs, paler underparts, black

SHRIKE: substantive name (or part of compound name) of most species of Laniidae (Passeriformes, suborder Oscines); in the plural, general term for the family. Formerly considered by Rand (1960) to include 4 subfamilies: Prionopinae, the helmet-shrikes; Malaconotinae, the bush-shrikes; Laniinae, the true shrikes; and the monotypic Pityriasinae containing the Bornean Bristlehead Pityriasis gymnocephala. In this volume Voous, following others, places the helmet-shrikes in their own family Prionopidae and, in addition, places the Bristlehead in its own

mainly brown heads and each may be distinguished from the others by the size of the bill and amount of black on the head; in addition, all 3 are allopatric. The Brown-headed Tchagra Tchagra australis is widespread in savanna woodland throughout Africa; it is replaced by the Threestreaked Bush-shrike T. jamesi in acacia steppe in Somalia and Kenya and by Levaillant's Bush-shrike T. tchagra in the coastal strip from Natal to Cape Town. In contrast, the Black-headed Tchagra T. senegala has a black crown and, although it has a similar distribution to australis, it, in

SHOEBILL: name, alternatively 'Shoe-billed Stork' or 'Whale-headed Stork', of Balaeniceps rex, sole member of the Balaenicipitidae, a family of disputed affinities. It has usually been placed in the order Ciconiiformes, sometimes in the suborder Ardeae, sometimes, as here in the suborder Ciconiae-even in the Ciconiidae (see STORK) instead of in a separate family-and sometimes in a suborder of its own. Wetmore (1960) holds that it has affinities both with Ciconiae and Ardeae, and that the resemblance of the skull to that of Pelecaniformes is due to convergence. More recent behavioural and morphological studies have not altered this assessment (Guillet 1979). Characteristics, habitat and behaviour. The Shoebill is a large bird, standing 120em high or more, with slaty plumage, long dark grey legs with very long toes. The most obvious character is the large head on a not very long neck, with a slight untidy crest on the nape and an enormous bulging bill, particoloured and carrying a hook on the upper mandible. It is a bird of swamps and water margins, often standing on 'islands' of floating vegetation. In such situations it remains motionless, bill on breast, waiting for fish or other aquatic prey to come within reach. The highly modified bill is adapted for catching and extracting prey among dense aquatic vegetation; and it is not used, as has been claimed, for digging lung-fish out of the mud. It is partly nocturnal in its habits and it is considered to be of a rather sluggish disposition; but it can fly strongly-and soar-on its broad wings, with neck drawn in and bill resting on the breast (as in the Pelecanidae). It is not a gregarious bird; and it is rather silent, apart from a laughing note and a stork-like clattering of the bill which is mainly performed during territorial and courtship displays. Distribution. The species has a limited range in eastern tropical Africa, mainly in the southern Sudan, northern Uganda, and some eastern parts of Zaire. The semipermanently flooded White Nile valley and the swampy borders of Uganda lakes are typical habitats. Breeding. The nest is a truncated cone of grass placed on floating vegetation, occasionally on an islet; in this, 2, sometimes only 1 or 3 bluish white chalky eggs are laid. The young are downy and nidicolous. (A.L.T.) A.G. Benson, C.W. 1961. The breeding of the Whaleheaded Stork in Northern Rhodesia. Northern Rhodesia J. 4: 557-560. Buxton, L., Slater, J. & Brown, L.H. 1978. The breeding behaviour of the Shoebill or Whaleheaded Stork Balaeniceps rex in the Bangweulu Swamps, Zambia. E. Afr. Wildl. J. 16: 201-220. Feduccia, A. 1977. The Whalebill is a stork. Nature, vol. 266, No. 5604: 719-720. Guillet, A. 1979. Aspects of the foraging behaviour of the Shoebill. Ostrich, 50: 252-255. Saiff, E.J. 1978. The middle ear of the skull of birds: the Pelecaniformes and Ciconiiformes. Zoo!. J. Linn. Soc. 63: 315-370. Wetmore, A. 1960. A classification for the birds of the world. Smiths. Misc. ColI. 139(11): 1-37.

SHOEMAKER: name applied to the White-chinned Petrel Procellaria aequinoctialis, also called 'Cape Hen' in South Africa (see PETREL). SHOOTING: see under

UTILIZATION BY MAN.

SHORE-BIRD: term used in North America in the same sense as 'wader' is in the British Isles (see WADER). SHORELARK: Eremophila alpestris, the 'Horned Lark' in American usage (see LARK). SHORTWING: substantive name of Brachypteryx spp, (see THRUSH). SHOULDER: see under

MUSCULATURE; SKELETON, POST-CRANIAL;

WING.

and white graduated tails and patterned heads. Three of them have

Shrike

general, prefers a drier habitat. The Blackcap Tchagra T. minuta is restricted to wetter areas than are the other tchagras and is the only one which is sexually dimorphic. The Laniarius species divide into 3 colour groups in each of which the species are largely allopatric. In the crimson group, 3 out of the 4 species with crimson underparts inhabit acacia steppe and sometimes are considered conspecific; the Gonolek L. barbarus in West Africa, the Blackheaded Gonolek L. erythrogaster in central Africa and Burchell's Gonolek L. atrococcineus in southern Africa. The fourth, L. mufumbiri, is smaller, has a distinctive orange tinge to the crimson, and is confined to papyrus swamps in central Africa. In other parts of Africa they are replaced by other members of the group which are coloured differently. The most divergent of the group is the Red-naped Bush-shrike L. ruficeps found in the arid acacia steppe of north-east Africa. The black of the back is mixed with grey and white and it has a prominent white eye-stripe not present in the others. The female is more olive grey on the mantle. In the other species of this group the sexes are alike. The black and white group has 4 species often considered conspecific. The best known is the Bell Shrike or Tropical Boubou L. aethiopicus, which is glossy blue black above and pinkish white below. It inhabits thickets in savanna woodland throughout Africa, both lowland and montane. In southern Africa, coastal Gabon and Angola, and in the forests of Sierra Leone and Guinea, it is replaced by 3 other species of the group. The black group, some of which show sexual dimorphism, range in colour from deep black to dark slate grey. The Sooty Boubou L. leucorhynchus occurs in West African and Zaire lowland forest blocks and, in contrast, the Slate-coloured Boubou L. funebris in acacia steppe in north-east Africa. The distribution of the other 2 species is restricted to separate montane forest blocks some 2,200 km apart. Of the Malaconotus species 10 are grouped into 2 superspecies. Both contain savanna and forest species, those in the lowland forest being polymorphic. The remarkable feature about them is that wherever a savanna or forest form of one superspecies meets a corresponding form of the second superspecies there is almost perfect colour match between them. Thus the savanna dwelling Sulphur-breasted Bush-shrike M. sulfureopectus, with green back, grey head and mainly yellow underparts, is simply a small replica of the much larger savanna species, the Grey-headed Shrike M. blanchoti. Similarly the small Many-coloured Bush-shrike M. multicolor, found in the forests of West Africa and Zaire, is matched in colour by the Fiery-breasted Bush-shrike M. cruentus, a larger forest species in the other superspecies (further details are given in Hall, Moreau and Galbraith 1966). Of the remaining 6 species, 3 are grouped to form a third superspecies. They are all bright green above, their tails are black and breasts red with a black pectoral band. Two are birds of thicket and forest edge, Perrin's Bush-shrike M. viridis in Angola, and the Four-coloured Bush-shrike M. quadricolor in Kenya, Mozambique and South Africa. The other, Doherty's Bush-shrike M. dohertyi, is confined to mountains of eastern Zaire. Laniinae. The true shrikes are birds of open woodland, rarely forest edge. They have the habit of dropping off a perch when alarmed and flying off close to the ground before swooping up to the next perch. When perched they frequently swing their tails from side to side, and up and down. Two of the red-backed group occur in Africa. Emin's Shrike Lanius gubemator inhabits the savannas north of the Equator, and Souza's Shrike L. souzae the brachystegia woodlands south of the Equator. Both are similar but not identical to the Red-backed Shrike L. cristatus (collurio considered a race of L. cristatusi the male of which has a grey head, a black eye streak, and a grey rump. The races of cristatus in Asia are a uniform mouse brown on the upperparts and these have sometimes been treated as a separate species. Other red-backed shrikes replace it in south-east Asia and India and overlap its distribution in eastern Asia. Five black and white shrikes, all with long graduated tails, are found in Africa. All are essentially allopatric, but when sympatry occurs there is ecological segregation between species. The most widely distributed is the Fiscal Shrike L. collaris which occurs throughout Africa in savanna woodland, forest clearings and cultivations. The Great Grey Shrike L.

excubitor, a paler bird than collaris, is only found along the southern edge of the Sahara but is widespread in the Palearctic and is the only shrike found in North America (the Loggerhead Shrike being considered a race); numerous races have been described. Two other African black and

535

Woodchat Shrike Lanius senator. (A.H.).

white shrikes with very long tails, the Grey-backed Fiscal L. excubitorius and the Long-tailed Fiscal L. cabanisi, are noted for their sociability. They are allopatric and occur in wooded savannas of central and east Africa. Two other sociable shrikes in Africa have unusual coloration; the Yellow-billed Shrike Corvinella corvina of west and central Africa is a heavily streaked brown shrike with yellow bill, the Magpie Shrike C. melanoleuca, confined to the southern half of Africa, is black with some white on the flanks and in the tail. The Strong-billed Shrike L. validirostris is of interest as it is confined to the Philippines and found in oak and pine forest between about 1,300 m and 2,600m. Its upperparts are grey, wings and tail brown-black, and underparts grey-white with rufous flanks; a black streak extends from the lores to the ear coverts. Movements. Although there are no ringing data to show that shrikes endemic to Africa migrate within it, there are visual records which suggest that local movements occur in some populations of the Sulphurbreasted Bush-Shrike, and are likely in the Brubru and Magpie Shrike. Africa is the wintering area for all populations of the Lesser Grey Shrike L. minor, Wood chat L. senator and Nubian Shrike L. nubicus, and for some populations of the Red-backed Shrike and the Red-tailed Shrike L. isabellinus (Moreau 1972); their other populations winter in south-east Asia. Of the other Laniinae found outside Africa only 4 migrate southwards after breeding further north; the Chinese Great Grey Shrike L. sphenocercus winters from Korea southwards; the Tiger Shrike L. tigrinus winters in the Malay peninsula, some stragglers reaching the Philippines and Sulawesi; some populations of the Bull-headed Shrike L. bucephalus winter in central Korea and south China; and some populations of the Black-headed Shrike migrate into northern India. Only the most northern populations of the Great Grey Shrike migrate southwards after breeding.

Food Malaconotinae. These are predominantly insectivorous. All tchagras, Rhodophoneus and most, if not all, Laniarius species feed near or on the ground in or under thicket, but in more open areas Rhodophoneus is more arboreal. The Flycatcher-shrike Lanioturdus torquatus feeds both on the ground and in trees. All other members of the subfamily are arboreal feeders, the puff-backs feeding much like warblers. Occasionally the Grey-headed Shrike takes other food items (various vertebrates and bird's eggs), and so do the Southern Boubou L. ferrugineus, the Brownheaded Tchagra and the Black-headed Tchagra (van Someren 1956). Laniinae. These characteristically search the ground for prey from a vantage point, from which they drop to the ground to catch it. Although a great variety of insects are taken, many depend on small vertebrates for an important part of their diet. They may catch insects on the wing,

search for prey on the wing, hovering before pouncing on it, and some

search leaf litter. Most Palearctic species use larders but only 2 shrikes in Africa are known to do so, Mackinnon's Shrike L. mackinnoni and some races of the Fiscal Shrike. None of the shrikes that winter in Africa are known to use larders while there.

536 Shrike

Behaviour Malaconotinae. In general, bush-shrikes are found singly or in pairs but small groups (5 or 6 birds), apparently not family groups, of Brownheaded Tchagras, Grey-headed Shrikes and Fiery-breasted Shrikes have been reported. They breed in pairs and some remain paired throughout the year (observed in Laniarius, Dryoscopus, Tchagra and Malaconotus species) (Kunkel 1974). What little data we have on this group suggest that both sexes build nests, incubate and feed young, and that territories are maintained outside the breeding season by some savanna species. The puff-backs and the Brubru form mixed feeding parties with other species in the non-breeding season. Courtship display in Dryoscopus involves the raising of the rump feathers by the male to produce the puff from which the genus obtains its name; this also occurs in some Laniarius species (details in van Someren 1956). In the tchagras it involves a display flight with duetting, and some wing flapping, although less developed in the Blackcap Tchagra. Little is known of the monotypic genera Lanioturdus and Rhodophoneus. Both are found in parties, particularly the latter which forms noisy display groups on the ground at dusk, the significance of which is not known. Laniinae. The majority of true shrikes breed in pairs, are highly territorial even when on migration, and some are known to hold territories in their winter quarters (Red-backed Shrike, Lesser Grey Shrike and probably the Great Grey Shrike). The migratory species are usually solitary in winter quarters and usually migrate singly, but the Woodchat and some races of the Red-backed Shrike are paired on arrival at their breeding grounds. The Fiscal Shrike may remain paired for several years and Souza's Shrike remains paired outside the breeding season. In several species both sexes help in nest building, incubation and feeding young; in others the male has only been reported feeding young. In contrast, the 2 Corvinella species, the Grey-backed Fiscal and the Long-tailed Fiscal, are all highly social. Although the first 3 breed in groups of 5 or more birds (Grimes 1980), some populations, at least, of the Long-tailed Fiscal breed in pairs with individual territories (van Someren 1956). Nothing is known about the permanency of the pair bond; in the Yellow-billed Shrike a female may remain the breeding female of a group for more than one breeding season and then become the breeding female of a subsequent group. Voice Malaconotinae. The bush-shrikes have a diverse range of calls rather than a recognized song, although the Olive Bush-shrike M. olivaceus is noted for its warbling song. The Brubru, an onomatopoeic name, utters a drawn out brruuu, reminiscent of a pea whistle, which often is answered by the female with a similar note of lower pitch. The calls of Dryoscopus species are variously described as loud, oft repeated or prolonged whistles; the Puff-back has a melodious song and the Black-backed Puff-back is known to duet. The tchagras are noted for their melodious, almost human whistles, given during a display flight, occasionally from a perch, while the female responds antiphonally with a call characteristic of the species. Duet song, usually antiphonal, is characteristic of all the Laniarius species. Each Malaconotus species has loud, distinctive and repetitive calls, that of the Bokmakierie M. zeylonus is onomatopoeic, and duetting is frequent. Laniinae. Although the true shrikes have harsh and discordant contact and alarm calls, the majority of them have notable songs and many are good mimics. Breeding. The nests of the Brubru, puff-backs, tchagras, gonoleks and boubous are inconspicuous but neatly formed shallow cups, either secured to a horizontal branch as in the Brubru, or placed in a fork of a tree from 2-7 m above ground. Occasionally nests of puff-backs are found as high as 18m. Materials used include tendrils, spider webs, lichen, rootlets, grass and bark fibre. In Malaconotus the nests of the majority of species are usually shallow cups of twigs, tendrils and root fibres, lined with finer materials, and placed 3-8 m above ground; some species build as high as 18 m. The nest of Lagden's Bush-shrike M. lagdeni is described as a bulky bowl of dry leaves and bracken. The nests of the Laniinae also vary a great deal. Those constructed at high latitudes have wool, hair and feathers as lining, whereas those at lower latitudes are usually lined only with tendrils and fibres or grass. Nests are built from twigs, tendrils and other materials and usually placed 3-9m high in a tree, although the Red-backed Shrike prefers thickets and brambles.

Shrike eggs have a range of ground colours, variously listed as white, greyish-white, pale-blue grey, blue, greenish blue, and pale pinkish. The eggs are either streaked, speckled or blotched with various shades of brown, purple-brown and chestnut-brown, the markings being concentrated usually at the large end. The clutch size of bush-shrikes is either 2 or 3, not 4 or more. By contrast, a clutch of 4 or more has been recorded in the following African Lanius species: Fiscal Shrike, Somali Shrike L. somalicus, Taita Fiscal L. dorsalis, Grey-backed Fiscal, Long-tailed Fiscal and the 2 Corvinella species; in others for which data are known the clutch is 2 or 3 (Mackinnon's Shrike, Souza's Shrike, Great Grey Shrike). The resident shrikes in India and south-east Asia have clutches between 3 and 6, although it is 2 for the New Guinea race of the Black-headed Shrike. The clutch size of shrikes breeding in higher latitudes is in the range 5-7, but larger clutches are not uncommon. Incubation periods are most frequently in the range 12-14 days, occasionally 15-18 days for some Lanius species. The most frequently reported range for the nestling period is 16-20 days, but 12-15 days are recorded for the Red-backed Shrike and the Lesser Grey Shrike. The breeding seasons of shrikes in Africa, India, and south-east Asia are prolonged and overlap both dry and wet seasons. The migratory shrikes breed during the northern summer, some as early as April but mainly in late May, June and early July. L.G.G. Benson, C.W. & Benson, F.M. 1977. The Birds of Malawi. Limbe. Grimes, L.G. 1980. Observations of group behaviour and breeding biology of the Yellow-billed Shrike Corvinellacorvina. Ibis 122: 166-192. Hall, B.P. & Moreau, R.E. 1970. An Atlas of Speciation in African Passerine Birds. London. Hall, B.P., Moreau, R.E. & Galbraith, I.C.J. 1966. Polymorphism and parallelism in the African bush-shrikes of the genus Malaconotus (including Chlorophoneus). Ibis 108: 161-182. Kunkel, P. 1974. Mating systems of tropical birds: the effects of weakness or absence of external reproduction-timing factors, with special reference to prolonged pair bonds. Z. Tierpsychol. 34: 265-307. Mayr, E. & Short, L.L. 1970. Species Taxa of North American Birds. Cambridge, Mass. Moreau, R.E. 1972. The Palaearctic-African Bird Migration System. London. Rand, A.L. 1960. Family Laniidae. In Mayr, E. & Greenway, J.C. Jr. (eds.). Check-list of Birds of the World, vol. 9: 309-365. Sibley, C.G. 1970. A comparative study of the egg-white proteins of passerine birds. Bulletin 32. Peabody Museum, Yale University. van Someren, V.G.L. 1956. Days with Birds. Fieldiana: Zoology 38. White, C.M.N. 1962. A revised Check-list of African Shrikes, Orioles, Drongos, Starlings, Crows, Waxwings, Cuckoo-shrikes, Bulbuls, Accentors, Thrushes and Babblers. Lusaka.

SHRIKE, ANT-: see ANTSHRIKE;

ANTBIRD.

SHRIKE-BABBLER: substantive name of Pteruthius spp. (see BABBLER).

SHRIKE, BUSH-: see BUSH-SHRIKE; SHRIKE. Also used as substantive name in some genera of Formicariidae (see ANTBIRD). SHRIKE, CATERPILLAR-: see CUCKOO-SHRIKE. SHRIKE, CROW-: name sometimes applied to Strepera spp. See CURRAWONG.

SHRIKE, CUCKOO-: see CUCKOO-SHRIKE. SHRIKE, FLYCATCHER-: see CUCKOO-SHRIKE. SHRIKE, HELMET-: see HELMET-SHRIKE. SHRIKE, PEPPER-: see PEPPER-SHRIKE. SHRIKE, SONG-: name sometimes used for

CRACTICIDAE.

SHRIKE, SWALLOW-: see WOOD-SWALLOW.

SHRIKE-THRUSH: substantive name of Colluricincla spp. (see THICKHEAD) .

SHRIKE-TIT: substantive name, in Australia, of Falcunculus spp. (see THICKHEAD) .

Sign stimulus 537

SHRIKE-TYRANT: substantive name of the species of Agriomis, a genus of South American tyrant-flycatchers (see FLYCATCHER (2)). SHRIKE, VANGA: see VANGA. SHRIKE-VIREO: substantive name of species of the subfamily Vireolaniinae (Passeriformes, suborder Oscines); in the plural, general term for the subfamily. The shrike-vireos are a small group of arboreal song-birds confined to the forested regions of continental tropical America. The 2 genera and 3 species are sometimes placed in a separate family, the Vireolaniidae, but are now often included, as here, in the Vireonidae. The shrike-vireos differ from typical vireos in having a heavier bill, which is hooked at the tip (see VIREO; also PEPPER-SHRIKE). They feed mainly upon caterpillars and mature insects which they glean from the foliage of trees but vary their diet with berries. Like typical vireos and pepper-shrikes, they hold large objects beneath a foot while they tear them apart with the bill. Characteristics, habitat, distribution and behaviour. The Chestnutsided Shrike-Vireo Vireolanius melitophrys-the only member of its genus-is a stout, long-tailed bird about 17cm long. The largest member of the subfamily, it is also the northernmost and the only one of which the sexes, although similar in plumage, are readily distinguished in the field. Its upper plumage in plain olive-green, with the top and back of the head slate-grey, bordered on each side by a yellow superciliary stripe, below which a black band stretches from the lores to the ear coverts. The ventral plumage is white, with black malar streaks and a chestnut band that crosses the breast and continues along the sides and flanks. This little-known bird is found, chiefly in forests of pine, oak, and other broad-leaved trees, from central Mexico to the volcanic highlands of Guatemala and from 1,200 to 3,OOOm. It forages, often in pairs, amid the foliage of trees and shrubs at all heights, where it moves slowly and deliberately, peering from side to side, sometimes hanging inverted to pluck an insect from a leaf. Among its notes are a low, nasal rattle and a peculiar, long-drawn, high-pitched, far-carrying, whistled screech. The two known nests, built by both sexes, were hemispheric cups, attached by their rims to the arms of horizontal forks, in the usual manner of vireos. Situated amid foliage at heights of 7-8 m, they were composed largely of filamentous lichens and vegetable fibres. Eggs, incubation and care of young remain undescribed. The 2 species of Smaragdolanius inhabit heavier, more humid forests at low and middle altitudes. The Green Shrike-Vireo S. pulchellus is about 14em long. Its upper plumage is bright parrot-green with more or less blue on the crown. The throat is yellow, and the remaining under parts light greenish yellow. From south-eastern Mexico to Colombia and north-western Venezuela, this bird lives in the upper levels of the forest, from which it sometimes ventures into neighbouring clearings with scattered trees. Although its loud, clear, tirelessly repeated whistles, grouped in trios or more rarely quadruplets, are often heard, its nest has apparently never been found. Equally unknown are the breeding habits of the Slaty-capped Shrike-Vireo S. leucotis, widespread in tropical South America. Both sexes are olive-green above, mostly bright yellow below, with the head boldly marked with a yellow superciliary band, a black streak through the eye to the hindhead, and below this a white streak. A.F.S. Barlow, J.C. & James, R.D. 1975. Aspects of the biology of the Chestnut-sided Shrike-Vireo. Wilson Bull. 87: 320-334.

SIBIA: substantive name of the species of Heterophasia and Grocias.

BABBLERS

of the genera

SIBLING SPECIES: 2 or more closely related species that are morphologically very similar but are reproductively isolated (i.e. able to inhabit the same area without interbreeding); sometimes called 'cryptic species'. SICK BIRDS, CARE OF: see CARE OF INJURED,

SICK AND ORPHANED

BIRDS.

SICKLEBILL: sole or substantive name used for various species possessing the form of bill suggesting it; these belong to several widely separated families. Thus, it is the name of Falculea palliata (see VANGA) and of Hemignathus procerus (see HAWAIIAN HONEYCREEPER), the latter

alternatively called 'Akialoa'. Again, it is the substantive name of

Drepanornis spp. and Epimachus spp. (see BIRD-OF-PARADISE), and also of Eutoxeres spp. (see HUMMINGBIRD). Further, it has been used (but 'scythebill' is now preferred) as the substantive name of Gampylorhynchus spp. (see WOODCREEPER); and it is sometimes applied, in Australia, to the White Ibis Threskiornis molucca (see IBIS).

SICKLES: term (plural) sometimes applied to elongated central tail feathers, found in certain species. SIEGE: see ASSEMBLY, NOUN

OF.

SIERRA-FINCH: substantive name of the species of Phrygilus, a genus of finches found in the Andes and the temperate southern extremity of South America (for family see FINCH). SIGHT: see VISION. SIGNAL: see DISPLAY;

RELEASER.

SIGNIFICANCE: see BIOSTATISTICS;

STATISTICAL SIGNIFICANCE.

SIGN STIMULUS: term coined by E.S. Russell to indicate those parts of the available environmental information to which an animal responds at any given moment, particularly when these are strikingly limited. One sees the first indications of this restriction to a few stimuli in observations of astonishing errors such as a Herring Gull Larusargentatus chick pecking at a cherry in the way in which it does at its parent's red bill-tip; or waders panicking when another wader descends in a wildly swooping flight, thus showing roughly the same type of movement as a striking Peregrine Falco peregrinus; or aggressive or sexual responses to animals only remotely similar to the adequate objects. Such 'errors' are in curious contrast to other evidence demonstrating the wonderful acuteness of a bird's perceptive abilities, and this apparent paradox has led to experiments in which the potentialities of the sense organs were compared with the actual stimulus situations releasing particular responses. In birds, the majority of papers on this subject deal with visible stimuli. The potentialities of the eyes are studied with as great a variety of methods as possible: by studying conditioned responses of the intact animal, by observing pupillary reactions, by electrophysiological recordings in or behind the retina, and so on. There is now much evidence to show that the visual acuity of birds is high, that they can recognize forms well, and that their discrimination of intensity and colour is of the highest order (see' VISION). Observations on geese (Anser spp.), gulls, crows and other birds have shown that they can distinguish between individuals of their own species much better than even a highly trained human observer. Actual stimulus situations releasing a particular response have been studied by means of tests with dummies. In these, precise imitation of the natural object normally releasing the response (the standard dummy) is offered in alternation with dummies lacking one or more characteristics, and the intensity or frequency of the response to these various dummies is compared. If there is no or little difference of effect between the standard dummy and one of the incomplete dummies, the character lacking in the latter can be of no or little importance as a stimulus; if the difference is striking, this is indicative of a sign stimulus. There are indications that the difference between a sign stimulus and a non-effective aspect of the environment is often one of degree only. In this way it was found, for instance, that the red patch on an adult Herring Gull's lower mandible is effective in releasing the chick's begging response, whereas the yellow of the rest of the bill is no more effective than any other colour, and this is expressed by saying that the red patch provides a sign stimulus. Further tests showed that it acts by its colour as well as by its contrast with the rest of the bill. Similarly, dummy tests with Song Thrush Turdus philomelos nestlings revealed that one of the sign stimuli is provided by the parent's head, which acts through being a protuberance of the outline of the body-above the body and with a certain size in relation to that of the body. Precise investigations of this type, in which the potentialities of the sense organs involved and the actual stimulus situations are systematically explored and compared, are still very much needed, but there seems to be little doubt that many responses are released (and others inhibited) by very simple stimulus situations.

538 Silktail

The fact that not all available information is 'used' or admitted for eliciting the response is posing an interesting physiological problem: where and how is the information refused passage? Lorenz (1935) pointed out that the restriction of a response to very few aspects of the total situation seems to be typical of 'innate' (i.e. non-conditioned) behaviour, and that conditioning usually leads to a fuller use of all details of the situation (unless special manipulations of the experimenter subsequently reduce the numbers of details used). Thus the conditioned responses to individual birds, or fear responses to (often amazingly slight) changes in the usual environment, are strikingly different from responses that occur prior to conditioning. This suggestion has not been followed up experimentally to any extent. Sign stimuli often have to be described in 'configurational' terms, which means that they evoke complicated processes of reception that cannot, at the present stage of analysis, be measured on one linear scale. Thus, many responses can be elicited only by a special type of movement, or by a special shape, or by a certain degree of contrast between two colours. In such cases it has been possible to design 'supernormal' stimuli, exaggerating the quality of the natural object to which the animal responds. For instance, the speckling of eggs can be exaggerated in models until they are preferred to normal eggs. N.T. Lorenz, K. 1935. Der Kumpan in der Umwelt des Vogels. J. Orn. 83: 127-213, 289-413. Russell, E.S. 1943. Perceptual and sensory signs in instinctive behaviour. Proc. Linn. Soc. Lond. 154: 195-216. Tinbergen, N. 1951. The Study of Instinct. Oxford.

SILKTAIL: substantive name for the taxonomically perplexing, monotypic and sexually monomorphic Lamprolia oictoriae (Passeriformes, suborder Oscines) of Vanua Levu (= L. v. kleinschmidti) and Taveuni (= L. u. oictoriae) Islands, Fiji; locally called Satin Flycatcher (Watling 1982). In general appearance it is extremely suggestive of a diminutive bird-of-paradise, to which family it has often been tentatively allied; but it has also been considered possibly part of the thrush-flycatcher-warbler complex Muscicapidae and of the Australasian Malurinae (Harrison and Parker 1965), within the babblers Timaliidae (Cottrell 1967). Olson (1980) reviews the evidence against a paradisaeid relationship, and on the basis of plumage, external morphology and zoogeography suggests a placement in the MONARCH FLYCATCHERS (Monarchidae) closest to the genera Clylorhynchus, Metabolus and Monarcha. Certainly the nest of Lamprolia is unlike those of Paradisaeidae but like those of Monarchidae. The present view of K.H. Voous is to place it close to the genera Eremiornis and Cinclorhamphus of the Sylviidae. Characteristics. A small (13 cm long) fine-billed insectivorous passerine of velvet black plumage with a silky-white rump, upper tail coverts and upper tail, and with iridescent tipped scale-like feathers about the head, neck, throat and breast which may appear blue, green or violet. Juveniles are like adults but duller, less glossy and spangled; the white tail develops clearly in the first juvenile plumage, whereas other decorativeplumage appears only gradually with age. An adult just completing moult, and others in fresh post-moult plumage, have been recorded in mid-July. Habitat and food. The Silktail is a bird of mature forests, found from over 1,000 m to the coast where forest remains, but mostly above 400 m where it actively forages for insects in the lower understorey and on the leaf litter. Behaviour. It is most frequently encountered singly, in pairs, or a pair with fledged young, but groups of up to 6 join mixed feeding flocks. Voice. Adult song is an unimpressive series of slurred trilled whistles, three initial notes slightly descending in pitch, followed by two or three elaborations of the same note; the entire song lasting 5 seconds. Breeding. Breeding takes place throughout the year, with a possible peak in June-September. Two aggressive display postures have been seen but no courtship display is 'recorded. The nest is a deep thickwalled, loosely built cup slung beneath a horizontal twig fork 1-3 m above ground, usually below large leaves. The clutch is only one egg, and observations suggest that only one parent incubates as no change-over was seen at the nests. C.B.F. Cottrell, G.W. 1967. A problem species: Lamprolia uictoriae. Emu 66: 253-266. Harrison, C.J.O. & Parker, S.A. 1965. The behavioural affinitiesof the blue wrens of the genus Malurus. Emu 65: 103-113. Heather, B.D. 1977. The Vanua Levu Silktail (Lamprolia victoriae kleinschmidti): A

preliminary look at its status and habits. Notornis 24: 94-128. Holyoak, D.T. 1979. Notes on the birds of Viti Levu and Taveuni, Fiji. Emu 79: 7-18. Olson, S.L. 1980. Lamprolia as part of a South Pacific radiation of Monarchine flycatchers. Notornis 27: 7-10. Watling, D. 1982. Birds of Fiji, Tonga and Samoa. Wellington.

SILKY-FLYCATCHER: substantive name of certain species of the family Ptilogonatidae (Passeriformes, suborder Oscines); in the plural, general term for the family. The relationship of the 3 genera and 4 species, ranging from south-western United States to western Panama, has long been disputed; often they have been classified as a subfamily of the Bombycillidae; but evidence from egg-white proteins, as well as other features, fails to uphold this treatment. Their closest relatives may be the solitaires Myadestes (family Turdidae). Characteristics, habitat and distribution. Silky-flycatchers range from about 17-23 em in length. They have short, rather broad bills, relatively short wings, and short tarsi. The Phainopepla Phamopepla nuens, which ranges from deserts and arid woodlands of south-western United States to the highlands of Mexico, is a slender, long-tailed, crested bird with silky plumage, shining black with white wing patches on the male, grey on the female. The 2 species of Ptilogonys are also slender, long-tailed, and prominently crested. The males are grey or blue-grey with yellow flanks and crissum, black wings, and black-andwhite tails; the females are similar but more olivaceous. The Grey Silky-flycatcher P. cinereus inhabits pine-oak woodlands in the highlands of Mexico and Guatemala. The Long-tailed Silky-flycatcher P. caudatus, which has elongated central tail feathers, is confined to the high mountains of Costa Rica and western Panama. The Black-and-yellow Silky-flycatcher Phainoptila melanoxantha, with the same range as the Long-tailed, is crestless and more thrushlike in aspect. The male is mostly glossy black, with bright yellow rump, sides, and crissum; the female is more olive. Food, voice and behaviour. Phainopepla and the 2 species of Ptilogonys associate in loose, wandering flocks. They perch on high, exposed treetops, from which they make long, spectacular sallies to catch insects. P hainoptda lives in pairs amid lower, denser montane vegetation and seizes insects on less spectacular darts. All members of this family eat many berries. Ptilogonys and Phainopepla use their voices freely but sing sparingly and not brilliantly. Breeding. The only species that have been carefully studied, the Phainopepla and the Long-tailed Silky-flycatcher, breed in monogamous pairs. Nuptial feeding is frequent. All 4 species build compact open cups in shrubs and trees, often high. Those of the Long-tailed Silky-flycatcher are composed almost wholly of grey beard-lichen Usnea; those of the Black-and-yellow largely of green moss; those of the other 2 species of more varied materials. Building is done chiefly or exclusively by the male Phainopepla, but by both sexes of the Long-tailed Silky-flycatcher. Phainopepla lays 2-3 (rarely 4) eggs; Ptilogonys, 2; and Phainoptila, 2 (1 record). The eggs of all 4 species are grey or greyish white, heavily marked with brown or lilac. Both sexes of Phainopepla incubate, but only the female Ptilogonys. The incubation period of the former is 14-15 days;

Size

539

of the latter, 16-17 days. Nestlings have abundant white down, long in Phainopepla, in short, compact tufts in Ptilogonys. Both sexes feed the young, which remain in the nest for 18-19 days in Phainopepla, 24-25 days in Ptilogonys. A.F.S. Bent, A.C. 1950. Life histories of North American wagtails, shrikes, vireos, and their allies. Bull. U.S. Natl. Mus. 197: i-vii, 1-411. Kiff, L.F. 1979. The nest and eggs of the Black-and-yellow Silky-flycatcher (Phainoptila melanoxantha). Auk 96: 198-199. Rand, A.L. & Rand, R.M. 1943. Breeding notes on the Phainopepla. Auk 60: 333-341. Sibley, C.G. 1973. The relationships of the silky flycatchers. Auk 90: 394-410. Skutch, A.F. 1965. Life history of the Long-tailed Silky-flycatcher, with notes on related species. Auk 82: 375-426.

SILVERBILL: substantive name of some Lonchuraspp. (see ESTRILDID FINCH).

SILVER-BIRD: Empidornis semipartuus (for subfamily see FLYCATCHER (1).

SILVER-EYE: name used for some species of Zosteropidae (see WHITE-EYE).

SIMURG: see FABULOUS BIRDS. SINGING: see VOCALIZATION. SINGLE-BROODED: laying a single clutch during a breeding season, although a replacement may be laid if the first clutch fails. See CLUTCH-SIZE.

SINUATED: term applied to a feather of which one edge appears as if cut away along a wavy line-not abruptly as when the vane is emarginated. SINUS VENOSUS: see HEART. SIRKEER: Taccocua leschenaultii (for family see CUCKOO). SIRYSTES: generic name used as common name of Sirystes sibilator (for family see FLYCATCHER (2)). SISKIN: substantive name of some Carduelis (or 'Spinus') spp.; used without qualification, in Britain, for C. spinus (see FINCH). SITE-ATTACHMENT; see TERRITORY. SITTELLA: alternatively 'treerunner'; in the plural, substantive name for the 3 species of Neosittidae or Daphoenosittidae; (Passeriformes, suborder Oscines). Formerly included in the Sittidae (see NUTHATCH), sittellas differ in leg musculature, bill morphology, plumage, nest type and social structure (Rand 1936; R. Orenstein). They may be most closely related to other Australian Oscine groups such as whistlers and monarch flycatchers (Sibley and Ahlquist 1982). Characteristics, habitat and distribution. The Varied Sittella Daphoenosuta (== N eositta) chrysoptera is a common resident of open Eucalyptus or Acacia woodland in Australia. It resembles a small nuthatch (10-12 cm) with a laterally compressed, upturned bill and a conspicuous white or orange-buff band across the flight feathers. The possibly conspecific Papuan or Mountain Sittella D. papuensis, which lacks the wing-band, is an uncommon New Guinea species of moist mountain forests between 1,075 and 2,450 m. The Black Sittella or Pink-faced Nuthatch D. miranda, locally common in Papuan mountain forests between 2,000 and 3,500 m, is a straight-billed, blackish bird with a rose-red face and white wing-band. Sittellas show limited sexual dimorphism, varying among races. Juveniles have whitish spots. Varied and Papuan Sittellas vary geographically in head colour and, in D. chrysoptera, in bill colour, streaking in the plumage, and wing-band colour. The 5 recognized races of Varied Sittella were long considered separate species, but all except, possibly, 2 hybridize extensively where they meet (Ford 1980). Food. Foraging Varied Sittellas explore branches in a series of rapid, tight spirals, working from their tips towards or on to the trunk, climbing

Varied Sittella Daphoenositta chrysoptera, female and male (below). (N.W.C.).

head downwards or on the undersides of limbs. They pry up bark flakes for invertebrates or, rarely, use twigs to probe deeper crevices (Green 1972). Birds may fly long distances between trees; their flight is undulating. The Papuan species behave similarly, although D. miranda may be less acrobatic (Diamond 1972). Behaviour and voice. Sittellas associate in groups of 3 to 12 or more, males outnumbering females. Members maintain contact with thin, high-pitched calls, louder in flight, and with rapid wing-flicks which expose the wing-band when it is present. The song has a series of 'zitting' notes. Breeding. Daphoenosiua chrysoptera breeds between July and March. All group members build the nest, a cup of spider-webs and cocoons, camouflaged with bark and lichen, placed up to 20 m high in a vertical fork. Normally only one female lays and incubates. There are usually 2 or 3 eggs, pale blue or greyish-white with dark spots and blotches. Incubation takes 12 or 13 days. Young birds remain in the nest for 13 or 14 days, fed by all group members, including juveniles from previous broods (Noske 1980). R.O. Diamond, J.M. 1975. Avifauna of the eastern highlands of New Guinea. Publ, Nuttall Ornith. Club 12: 1-438. Ford, J. 1980. Hybridization between contiguous subspecies of the Varied Sittella in Queensland. Emu 80: 1-12. Green, C. 1972. Use of tool by Orange-winged Sittella. Emu 72: 185-186. Noske, R.A. 1980. Co-operative breeding and plumage variation in the Orangewinged (Varied) Sittella. Corella 4: 45-53. Rand, A.L. 1936. The rediscovery of the nuthatch Daphoenosiua with notes on its affinities. Auk 53: 306-310. Sibley, C.G. & Ahlquist, J.E. 1982. The relationships of the Australo-papuan Sittelas Daphoenosiua as indicated by DNA-DNA hybridisation, Emu 82: 173-176.

SITTIDAE: a family of the

PASSERIFORMES,

suborder Oscines (see

NUTHATCH).

SIVA: substantive name of some Minla spp. (for family see BABBLER). SIZE: discussions of the evolution of birds are usually concerned exclusively with the radiation of different kinds, emphasizing body shape and posture, plumage colour, bill shape and feeding behaviour or taxonomic affinity. However, it is not so much the kind of bird as the size that has the most dramatic effect on the bird's requirements and ecological opportunities.

540 Size

There are several measurements for describing the size of a bird. The most satisfactory of these is body weight or mass, primarily because it overcomes the complex variability of linear measurements due to differences in shapes of birds. However, there are considerable seasonal changes in body mass of migratory birds, and of birds such as penguins (Sphenisciformes) which fast during incubation, as well as weight changes due to egg formation and laying. Clark (1979) has provided an excellent review of these problems and bibliography on bird weights. Range of sizes. The first known bird, Archaeopteryx lithographica, was somewhat lighter than a pigeon; its body mass has been estimated at about 270 g. Apparently from a start in this size-range, there evolved a range in sizes from the Bee Hummingbird Calypte(Mellisuga) helenae to the Giant Moa Dinornis giganteus and the Elephant Bird Aepyornis. The mass of the Bee Hummingbird is variously given as from 1.6 g to less than 3 g, while Amadon (1947) estimated 236 kg for the Giant Moa and 457kg for the Elephant Bird. The largest living bird, the Ostrich Struthio camelus, may weigh 100-136kg as an adult, 67,500 times as much as the smallest. Including the extinct forms, the class Aves has spanned a 228,500-fold range in body mass. The range in sizes of living land mammals is considerably greater (see Table 1), but in the case of elephants or mammoths, the huge mass is supported by four limbs instead of two. If we limit consideration of the largest mammal representatives to bipedal forms the range is 350,000 to 680,000, about the same order of magnitude as birds. The avian extremes, hummingbirds and ratites, differ not only in size, but in form, locomotion, habits, and ecological niches. The smallest birds are able to extract a net energy profit from minute droplets of nectar in flowers, taken during an energy-expensive hovering manoeuvre. Energy-balance considerations have made the hummingbird plan seemingly unsuitable at sizes greater than 21 g. The lower size limit for hummingbirds may be related to problems of overnight survival on body energy reserves or the mechanics of the avian method of oviparous reproduction (see Brown et alI978). At the other extreme, the Ostrich's large body size must have conferred benefits such as an opportunity to exploit a grazing niche or reduced vulnerability to attack. It is more instructive to consider size ranges within some phylogenetic and locomotive subgroupings (Table 1). Within several orders, the range in body mass exceeds 2 orders of magnitude, although there are exceptions to this in the more specialized groups such as penguins, ducks and swifts. There is an upper limit to flying size (see below and FLIGHT), but the range in body mass for fliers is 10 times that for diving birds. Heat loss to the highly conductive water may limit the smallest size practical for diving, but some warm-blooded mammals dive successfully despite very small sizes: the watershrews Sorex palustris or N eomys fodiens have one-fifth the mass of the dipper or water ouzel (Cinclus). An important characteristic of flying birds is the wing-loading, or ratio of body mass to the surface area of the wings which provides lift. Analyses by Hartman (1961), Greenewalt (1962) and others have shown that wing-loading increases with body mass; that is, the surface area of the wings was not increased in proportion to body mass increase as larger birds evolved. At any given body size for comparison, gliding and soaring birds have very light wing-loading. Heavy wing-loading is the rule for diving birds that use the wings to swim underwater. They have been limited in wing size because of the greater resistance to movement in water, which has considerably greater viscosity and density than air. Pennycuick (1969, 1972) derived an equation relating characteristic velocities (such as stalling speed, speeds for minimum power consumption or maximum range) to the square-root of wing-loading. Thus to remain airborne a diving bird with relatively smaller wings must fly at a greater speed than a non-diving bird of similar mass. Allometry. There are no birds weighing more than 13kg, and still capable of horizontal flapping flight, although it is speculated that some large fossil carinates may have been capable of flight. Pennycuick (1969) provided a theoretical basis for the upper limit to body mass for flight. If

a basic body-plan for a bird is scaled up such that its linear dimensions (height, length, width) are each multiplied by a factor of 10, then its volume will be increased to 10 x 10 x 10, or 1,000 times as great. Built of the same materials, the mass to be lifted in flight will be 1,000 times that of the prototype bird. The power required to lift this mass will actually be proportionately greater, about 3,200 times as great as the bird that weighed 1/1,000 as much. The force generated to flap the wings by the pectoralis and supracoracoid muscles is proportional to the cross-section-

at area of these muscles. Thus the power available has increased by a factor of only 10 x 10 while power requirements for sustained flight have

increased by 32 x lOx 10. A disproportionate increase in muscle mass to offset the power requirements would require greater oxygen and energy supply. Thus the heart, lungs, and the digestive tract, kidneys, and liver would have to be increased to meet the metabolic requirements for the larger muscles, making the bird still larger and more difficult to lift. Failure to appreciate the subtleties of scaling has led biologists to a number of erroneous conclusions. It is often stated that birds have faster heart beats and lighter skeletons than do mammals, but compared on an equal-mass basis, this generalization is untrue (Prange et al 1979). It is also untrue that larger birds lose less heat than small birds (Calder 1974). The study of scaling is allometry (alIos = other; rnetryon a measure), first applied to birds in a study of egg size by I.S. Huxley. Contributions of Max Kleiber, Samuel Brody and others have led to a rapidly increasing use of allometric analysis of avian biology. This, in turn, has yielded fundamental understanding of the dimensions of eggs and incubation, the similarity in basal metabolic rates of mammals and birds (except Passeriformes, which are characteristically higher in this regard), the insulative equivalence of feathers and fur, and the longer life spans of birds as compared with mammals. From body mass, we can predict practically any feature of a bird's natural history, its flight speed, territory size, energy requirements and the size of body organs. Note in Fig. 1 that the size-dependent changes are not scaled in the same proportion. Skeletal mass must increase more than heart mass, and the brain mass increases less than either. Allometric analysis is simple, mathematically. The best fit for the relationship of many biological variables (Y) to body size is an exponential or power function of body mass (M):

Y=aMb 10,000

100

~ o

'0

t:.

-

« w 0:: «

100

Ie:

'E

>

z w

10

:::::>

a

w

cr.: LL.

-::

!!! (/) (f)

« :E z « (.!)

0::

0

100(/)

:>.

C

0.1

~

w

::E 10 i= 0.01

Ig

109

100g

I kg

10kg

100kg

BODY MASS

Fig. L A sample of avian life history and body construction features which scale as various exponential functions of body mass (Y = aMb ; see text). Note that the scales (vertical and horizontal) are logarithmic, which results in straight-line plots, the slopes of which are the exponents b. These lines represent mathematical generalizations; values for actual birds vary above and below the line of statistical best-fit. This shows that, in the evolutionary scale-up, the heart size increases in approximately direct proportion to body size increase while the heart beat, wing beat, and breathing frequency (min"! means per minute) are fast in small birds and slow in large birds. The skeletal mass and territory size increase in greater proportion, while the brain increase does not keep pace with body size increase. Size increase has proportionately the same effect on incubation period and lifespan. (By permission of Harvard University Press).

Size 541

Table 1: Size ranges in bird groups compared with mammals. Smallest species

Type of animal

BodyM (g)

All birds

Bee Hummingbird Calypte helenae

2

Ostrich, Struthio camelus *Elephant Bird Aepyornismaximus

All land mammals

Pygmy Shrew M icrosorex hoyi

2

African Elephant Loxodonta africana

Bipedal mammals

Little Pocket Mouse Perognathus longimembris

8

Ratites

Little Spotted Kiwi Apteryx oweni

Penguins

Little Penguin Eudyptula minor

Procellariiformes

Storm Petrel Hydrobates pelagicus

666 1,100 28

Body M (kg)

Largest species

Ratio of largest/smallest

135 457

67,500 228,500

7,000

3,043,478

Gorilla, Gorillagorillat Man Homo sapiens

290 70

35,366 8,537

Ostrich Struthio camelus *Elephant Bird Aepyomis maximus

135 457

203 686

Emperor Penguin Aptenodytesforsteri *Fossil Penguin Pachydyptes

42.5 100i

39 91

12.7

45

Wandering Albatross Diomedeaexulans (wingspan 3.5m)

Pelecaniformes

White-tailed Tropic-Bird Phaethon lepturus

300

Dalamatian Grey Pelican Pelecanuscrispus

13

43

Anseriformes

White Pygmy Goose N euapus auritus

220

Trumpeter Swan Cygnuscygnusbuccinator

12.5

57

Galliformes

Painted Quail Excalfactoria chinensis

40

Wild Turkey M eleagris gallopaoo

13

318

Gruiformes

Lark-quail Ortyxelos meiffrenii

18

Great Bustard Otis tarda

17

933

Trochilidae

Bee Hummingbird Calypte helenae

2

Giant Hummingbird Patagona gigas

0.021

11

Passeriformes

Flycatcher Abrornisalbogularis

5

Raven Corvuscorax

1.7

355

Flying birds

Bee Hummingbird Calypte helenae

2

Trumpeter Swan, Cygnuscygnusbuccinator

12.5

6,250

Diving birds

Dipper Cinclusmexicanus

Emperor Penguin Aptenodytesforsteri *Fossil Penguin Pachydyptes

43

850 2,000

50

* Extinct; body mass estimated. t Knuckle-walker Quadripedal. :I: Olson and Hasegawa (1979, Sci. 206: 688) report that the largest fossil plotopterid (Pelecaniformes) may have been larger than any of the

If b is 1.0, there is a straight-linear proportionality (i.e. doubling of body mass has involved a doubling of Y, such as a doubling of heart or respiratory system size). If b exceeds 1.0 the curve becomes increasingly steep. For example, as bird size increases, the skeleton must be progressively a larger percentage of body mass, and the power requirement for flight grows disproportionately as well. When b is a fraction less than 1.0, a doubling of body mass requires less than twice as much of Y, and the graph of the relationship is shallower. Thus a 100g bird requires less than twice as much (about 1.7 times) food or metabolic heat production as does a 50 g bird. A b value of zero indicates that the variable is independent of size of the bird or egg. For example, body temperatures of resting birds are independent of body mass, although the temperature of a hand-held or struggling bird may rise more rapidly the smaller the bird. Birds' eggs, large and small, all lose about 150/0 of their fresh mass by evaporation during the incubation period. Finally, if b has a negative value, the allometric correlate decreases as the body size increases; the heart of a goose beats more slowly than a hummingbird heart, and the wing beat is also much slower. Plotted on logarithmic scales, these relationships all take the form of straight lines, the exponents becoming slopes of the straight lines, which are fitted by the method of least squares regressions (see BIOSTATISTICS). The plots or equations then provide a basis for comparing birds with mammals in general or for comparing unusual birds with more 'typical' ones (such as the differences in insulation between a ptarmigan Lagopus and a bird of more moderate climate). From allometric analysis we can appreciate the complexities of natural selection for larger or smaller birds, and we can predict approximately the requirements or dimensions of the yet unstudied birds. When consistent patterns emerge from the analysis there is strong suggestion of underlying physical constraints which have had a major influence upon the evolution of birds. With this background, one can begin to analyse the structure, physiology, and life history of birds from a fresh perspective.

Birds and mammals compared. We can then make fair comparison of birds and mammals if they are of the same sizes. From Table 2, it may be observed that the basal rates of energy demand by birds and mammals are indistinguishable, as are their skeletal weights. Compared at 1kg size,

Table 2: A Comparison of Birds and Mammals Based Upon Body Size 1 kg

Effect of sizeincrease (exponents) Bird Mammal 0.72 0.75

Basal metabolic rate (ml 02/hr)

1kg bird 679

mammal 676

Energy cost of travel (kJ/km)a

49

118

0.77

0.60

Speed of travel (km/hr)"

47

6

0.17

0.24

Skeleton mass (g)

65

61

1.07

1.09

Brain masse (g)

7

11

0.51

0.66

Heart mass (g)

9

6

0.94

0.98

161

54

0.91

1.06

Lung mass (g)

13

11

0.95

0.99

Incubation/gestation Cda)

28

70

0.17

0.23

Lifespan (yr), in captivity

28

12

0.19

0.20

Heartbeat/min

156

241

-0.23

-0.25

Breaths/mind

17

54

-0.31

-0.26

Respiratory system volume

a. Compares flying of birds with running of mammals. 1 k] 0.239 kcal or energy in 25mg fat. b. Pennycuick, C.J. (1969) Ibis Ill: 525, theoretical calculation for minimum power requirements for birds; Heglund, N. et al (1974) Science 186: 1112, empirical regression for trot-gallop transition of mammals. c. Note difference in proportionate effects of size upon brain mass. These relationships predict that birds with body mass under 34 g would have larger brains than mammals of the same sizes, while above 34g size mammals have progressively larger brains than do birds. d. Excluding Passeriformes.

542 Size

birds have smaller brains than mammals, but the smaller scaling exponent translates to the fact that very small birds «34 g) have larger brains than mice of the same size. Except for small birds and mammals «34 g) birds have smaller brains. Birds' hearts and respiratory systems are larger, and heart beats and breathing are slower. Time required for incubation of eggs is less than one half of that required for mammalian gestation, but birds' lifespans are more than twice those of mammals of equal size. Birds not only fly faster than mammals can run, but the energy cost for a bird of 1kg or less to fly a km is less than half the cost for the equivalent mammal to run that distance. The difference in exponents means that size has a greater proportionate influence on birds (0.77) than on mammals (0.60). The relative advantage is reduced to 63% of mammalian running cost at the maximum body size for flying birds. From this energy comparison it is obvious why migration is more common in birds than in mammals. Amongst the mammals, long distance migration is limited to the larger terrestrial mammals, to bats and to marine mammals. Having compared these two classes of 'warm-blooded' vertebrates, consider the details of scaling within the class Aves. As noted above, with the evolution of larger birds, the margin between power available and power required for flight decreased until flight was no longer feasible. Similarly the 'dead weight' of the skeleton must increase out of proportion to body size increase. This is slightly offset by the fact that the brain need not increase in linear fashion to coordinate the bird's physiology. Organs basic to life support, such as heart, lungs, respiratory system, gut mass, and blood volume are increased in an approximately direct linear proportion to body mass increases (Calder 1974; 1984). The exponent 0.94 for heat mass as a function of body mass may reflect more than statistical scatter in its departure from strict linearity (1.0). This may be attributed to the fact that the largest birds are not fliers and do not experience as intense demands for oxygen, hence can manage with hearts that are proportionally somewhat smaller than those of smaller birds. Heart rate bears an inverse relationship to heart mass, the smaller heart beating more rapidly. This is seen not only within Class Aves, but in the comparison with Mammalia, noted above. A 1 kg bird has a heart 1.48 times as heavy as that of a 1kg mammal, while the mammal's resting heart rate is 1.55 times as fast as the heart of a 1kg bird. From more limited data, there appears to be no significant difference in ratios of active to resting heart rate between birds (2.6 ± 0.75 s.d.), eutherian mammals (2.13 ± 0.945 s.d.), and marsupial mammals (2.24 ± 0.35 s.d.), nor is there any size-related trend to the variability within these groups. Similarly, breathing rates decrease as respiratory system volume increases with body mass in both birds and mammals. At a comparable 1kg body mass, the breathing rate of the mammal is 3.1 times that of the bird, while the RESPIRATORY SYSTEM of the bird has 3 times the volume of that of the mammal. Body size and environment. Within many species or genera, body size increases with increasing latitude or altitude, increases which are associated inversely with temperature. These empirical trends are established beyond argument, but their interpretation has been controversial (James 1970). The smaller the bird, the greater the ratio of surface area (cc M 2/3) to volume (ccMI). Since heat is produced by the volume or mass of tissues but lost by the surface, the higher surface: volume ratio is taken to indicate a greater liability for heat conservation. While it is true that the metabolic cost per gram is higher in smaller birds, the total heat loss from a large bird is greater than from a small bird. Body size and temperature. The body temperatures at which birds live are size-independent, 40 ± 1.5°C when resting, 43 ± O.5°C when heat-stressed or highly active. The heat production which supports the body temperature (T b) is a by-product of metabolism. The basal (minimal) metabolic rate is proportional to M 3/ 4 • When the environmental temperature (T e) is below a critical lower limit (T Ie) this metabolic rate is insufficient to maintain the body at 40°C, and shivering commences in proportion to the difference (T b - T e) and is inversely related to the amount of insulation contributed by the plumage, a resistance (R) to heat flow. Consideration of the plumages of a goose and a tit tells us that the larger the bird, the thicker its insulation. The thermal insulation R is generally proportional to the square-root of body mass, M 1/2, that is to say it does increase with size, but not as much as body mass or body surface (M2/3). Consequently, the goose produces more heat and loses more heat than does a tit, and a big tit loses more heat than a little tit. A

male Black-capped Chickadee Parusatricapillus in Alaska weighing 11.1g exposed to O°C would lose heat at a rate of 0.66 watts, while at the lower latitude of Ohio, USA, the chickadee weighs 10.0 g and exposed to O°C, loses heat at a rate of 0.63 watts (Calder 1974). How then can the size increase that is correlated with lower environmental temperature be interpreted? The amount of energy reserves a bird can store as fat and in the crop and gut contents is at least a linear function of body mass, that is to say, amount of energy o: M 1.0. The rate of their depletion during a fast imposed by blizzards or ice-storms is proportional to the metabolic rate, rate ccM 3/ 4 • Endurance time equals amount/rate, M I -7 M3/ 4 = M 1/4. This positive fractional exponent says that the larger tit will survive longer. Ecological consequences of size: lifespan. The larger the bird, the longer its lifespan (Mo. 2, Lindstedt and Calder 1976 (see also AGE». The allometry of maximum longevity data from birds indicates that birds survive 61% longer in captivity than in the wild (bird-ringing records). The difference between wild and captive longevities must reflect the effects of disease, predation, and (or) uncertainties of food supplies in natural environments. In captivity, birds have maximum lifespans well over twice those of mammals of the same body size. If fertile lifespan was a similar proportion of total lifespan in both classes, the birds would have a greater opportunity for successful reproduction. Ecological consequences of size: reproduction. The larger the bird, the larger the egg (exMO.77) and the longer the incubation period (cc Mg~~y or M~gi2). Compared on a body mass-equivalent basis, incubation of bird eggs is considerably more expeditious than gestation in mammals, requiring only 41% as much time. This perhaps reflects a natural selection that reduced the period of exposure to predation. Ecological consequences of size: territory. Both territory and home range increase with increasing body size. When food habits were not considered, Schoener (1968) found that both territory (ccM1.09) and home range (cc M 1.16) increased in greater proportion than body mass. Treated separately, territory and home range of birds consuming animal food increased even more disproportionately with body mass increase ( oc M 1.31, M 1.39, respectively), while territories of omnivores and herbivores increased in a less than linear fashion (ccMO. 3S, MO. 70, respectively). Obviously, on a given amount of land of suitable habitat, there will be more small birds with small territories than large birds with large territories. Thus, the larger the bird, the fewer its numbers. This would mean that other things being equal, larger birds would be generally more vulnerable to extinction, and large carnivores would be especially vulnerable. To this effect may be added the previously mentioned correlation of long incubation period with large bird size, which could increase the vulnerability. Certainly many birds listed as extinct, vanishing, or endangered were or are large, absolutely or within their taxa: moas, elephant-birds, Dodo, Arabian Ostrich, Whooping Grus americana and Japanese Cranes G. vipio, the bustards Otididae, Takahe Notornis, California Condor Gymnogyps californianus and Ivory-billed Woodpecker Campephilus principalis. Other considerations. There are sex differences in size (see SEXUAL DIMORPHISM). Full size is attained before fledging of altricial species or by the time of replacement of down by feathers in precocial species (see GROWTH; YOUNG BIRD). The consequences of body size extend to all aspects of avian biology. W.A.C. Amadon, D. 1947. An estimated weight of the largest known bird. Condor 49: 159-164. Brown, J.H., Calder, W.A. & Kodric-Brown, A. 1978. Correlates and consequences of body size in nectar-feeding birds. Amer. Zool. 18: 687-700. Calder, W.A. 1974. The consequences of body size for avian energetics. In Paynter, jr., R.A. (ed.). Avian Energetics. Cambridge, Mass. Calder, W.A. 1984. Size, Function and Life History. Cambridge, Mass. Clark, G.A., Jr. 1979. Body weights of birds: a review. Condor 81: 193-202. Greenewalt, C.H. 1962. Dimensional Relationships for Flying Animals. Washington. Hartman, F.A. 1961. Locomotor Mechanisms of Birds. Washington. james, F.C. 1970. Geographic size variation in birds and its relationship to climate. Ecology 51: 365-390. Lindstedt, S.L. & Calder, W.A. 1976. Body size and longevity in birds. Condor 78: 91-94. Pennycuick, C.J. 1969. The mechanics of bird migration. Ibis Ill: 525-556. Pennycuick, C.J. 1972. Animal Flight. London. Prange, H.D., Anderson, J.F. & Rahn, H. 1979. Scaling of skeletal mass to body mass in birds and mammals. Amer. Nat. 113: 103-122. Rahn, H., Paganelli, C.V. & Ar, A. 1975. Relation of avian egg weight to body weight. Auk 92: 750-765.

Skeleton, post-cranial

543

Schoener, T.W. 1968. Sizes of feeding territories among birds. Ecology 49: 123-141.

SKEIN: see ASSEMBLY,

NOUN OF.

SKELETON, POST-CRANIAL: the internal framework (endoskeleton) of the body which, along with the SKULL protects and supports its soft structures. Together with the muscular system (see MUSCULATURE), it forms an integrated system for exerting force and movement (see LOCOMOTION, TERRESTRIAL; FLIGHT). Nature and development. The skeletal system is composed of bone, cartilage, and ligaments. Bone is a living tissue composed of an inorganic mineral (hydroxyapatite: Ca lO(P04)6(OH)z), laid down in an organic matrix (collagen fibres). Together these substances form fibrils. In lamellar bone the fibrils lie parallel to each other, whereas in woven bone they are tangled more or less at random. The composite structure of bone makes it more rigid than collagenous fibres, more flexible and resistant to fracture than mineral, and more versatile in the kinds of loads it can withstand than either of its components alone. The red marrow found within bones is the primary blood-forming organ in the adult (see BLOOD), and bones may serve as storage areas for calcium and phosphorus. Most bones have a complex organization (Fig. 1). On the outside is a tough fibrous membrane (periosteum). Mature bone is composed of an outer layer of dense, ivory-like, compact bone and an inner network of thin sheets of bone (trabeculae) and intercommunicating spaces (cancelli) which together form spongy bone. The spongy bone often has a hollow central cavity which contains marrow or fat or outgrowths of the air sacs (see PNEUMATIZATION OF BONE; RESPIRATORY SYSTEM). The greater part of the skeleton is first laid down in the embryo (see DEVELOPMENT, EMBRYONIC) as a cartilaginous framework and later converted into bone by the process of ossification. Most bones thus ossify in cartilage and are called cartilage bones. Some, however, ossify directly without going through a cartilaginous stage, and these are known as membrane bones; except for the clavicle, they are confined to the SKULL, where they make up the roof, parts of the side walls, and most of the jaws and palate. In the adult, cartilage is found mainly as articular pads which serve as shock absorbers and to reduce friction between bones. Bones begin to appear early in embryonic development, but many of them are not completely ossified until maturity. The ossification of a cartilage bone, such as a limb bone, begins in the middle of the shaft, the ends remaining cartilaginous for a time. The bone grows longer as the result of the proliferation of cartilage near the ends and, as new cartilage is formed, it is progressively converted into bone. In addition to growing in length, a bone also grows in thickness as new material is deposited beneath the periosteum. As the entire structure increases in size, it is remodelled so that it retains its shape, bone tissue being added in some places and removed in others. A bone and its internal structure will develop normally only under the influences of the surrounding muscles and soft tissue. Two types of ligaments have been reported in birds: collagenous-fibre ligaments, which are highly elastic and noncompliant, and yellow elastic ligaments, which are elastic and relatively compliant. Little is known of the properties and distribution of yellow elastic ligaments; they are known from the avian neck and may be found in the wings of some birds.

P'~.J.-sy

t...} . • af"

"''c

C Fig. 1. A, B. Transverse sections through mid-shaft of femur (A) not pneumatized, and humerus (B) pneumatized, of fowl Gallus. The thickness of the bone wall, and the relative thickness of the compact and spongy bone, varies in different specimens, especially in the femur. (Partly based on data from A. S. King.) (C) Diagram showing structure of synovial joint. ac. articular cartilage; as. air sac; c. cavity of joint; cb. compact bone; 1. ligament of joint capsule; m, marrow; p. periosteum; sb, spongy bone; sy. synovial membrane; t. bone trabecula.

Fig. 2. Two fundamental geometric types of articular surfaces. (a) Ovoid, which may be convex (male) or concave (female). Note that the solid body presents ovoid profiles in two planes at right angles and that the curvatures of the two may be different. (b) Saddle-shaped surfaces, which are concave-convex. In practice both types of surfaces may vary from only slightly to highly curved. Thus ovoid surfaces may be 'almost flat' or 'almost spherical', but the majority show intermediate grades of curvature, and much variation in change of radius from place to place. (Courtesy of Williams & Warwick, 1973, and Longman Group Ltd.)

Most avian ligaments are collagenous-fibred bands between bones; articular ligaments and linkage ligaments are the two main kinds. Articular ligaments bind the bones of the skeleton together; they prevent the articulations from being disrupted under stress and fix the type and extent of movement between two bones at an articulation. Linkage ligaments are known only from the head; they span two or more articulations and limit or couple the movement of the bones they join. The joints between bones differ greatly in their structure and mobility. The arrangement of a typical freely moving joint is shown in Fig. Ic. Contact between the two bones is made by cartilaginous surfaces on their ends. The surfaces have a low coefficient of friction and are lubricated by the viscous synovial fluid. The joint is enclosed in a fibrous capsule, lined by the synovial membrane and usually strengthened with ligaments. Sliding, angular, circumductional, and rotational movements at joints may be combined to produce an almost infinite variety of movements. Two fundamentally different articular surface shapes, ovoid and saddle-shaped (Fig. 2), make these movements possible. Ovoid surfaces are either convex in all directions (male ovoid) or concave in all directions (female ovoid) whereas saddle-shaped surfaces are convex in one plane and concave at right angles. In addition to allowing motion between bones, articulation, along with ligaments and muscles, reduces stress and redistributes forces within the skeleton. Factors influencing form and structure of bones. The shape of bones and joints and their internal structure are adapted to the functions which they have to perform and the strains to which they are subjected in life. The degree to which this is the result of hereditary factors or of use during embryonic or later life has been extensively studied. A femur of relatively normal shape will develop from isolated fragments of limb bud removed from the embryo and grown in a tissue culture, despite the absence of muscles and of the possibility of movement. In cultures of limb-bud material the skeleton will differentiate into the elements of the thigh and leg, and joint rudiments will appear at the appropriate places. On the other hand, the finer details of the normal skeleton do not develop perfectly. The rudimentary joints tend to fuse, although they can be made to develop more normally if the bones are artificially moved. The shape of bones and the amount of bony material present in a skeletal bone depend to a great extent upon the magnitude of the forces acting upon the skeleton. For example, the surface markings of bones reflect the shape of the attached connective tissue structures: depressions (fossae) are produced by fleshy muscular attachments; elongated (crista), pointed (process), or rounded (tuberosity, tubercle, or trochanter) elevations are usually associated with the attachment of tendons. The thickness of the wall of bones and the arrangement of the internal trabeculae are readily modified by changes in stress patterns. Bone apposition by osteoblasts and bone resorption by osteoclasts are in balance under normal conditions. Under greater-than-normal strains bone apposition will predominate; under decreased stresses bone absorption will predominate. Weak but steady compression may cause erosion; a steady tension may cause the appearance of bony processes at muscle attachments, ossification of collagenous tissue, and formation of sesamoid bones; and new articulations may develop when two bones contact one another and continue to rub together. The arrangement of the internal trabeculae has been shown to correspond to the lines of force acting on

544 Skeleton, post-cranial

the bone. When local stresses are applied, trabeculae may undergo a corresponding condensation and reorientation. The evidence thus indicates that the major features of the skeleton's architecture are determined by heredity, but many of the finer details that appear later in the embryo or after hatching depend for their proper development on environmental factors such as movement and mechanical stress. Skeletal structure is also affected by diet and by the action of chemical substances (hormones) secreted into the bloodstream by certain ductless glands such as the pituitary, parathyroids, and sex glands (see ENDOCRINOLOGY AND THE REPRODUCTIVE SYSTEM). Adequate supplies of calcium and of vitamins such as A and D are necessary for normal ossification and growth, and (as in mammals) rickets and other deficiency diseases will occur in their absence. Changes in the composition of the adult skeleton are associated with physiological processes accompanying such activities as moulting and egg laying. In chickens and pigeons, additional bone tissue (medullary bone) is laid down in the marrow spaces of limb bones before the eggs are laid, and this is subsequently reabsorbed and the calcium thus liberated used in the formation of the eggshell. A similar condition may be artifically induced in male or immature female birds by the use of hormones. Evolutionary history. The skeleton of birds most closely resembles that of reptiles, especially that of members of the subclass Archosauria (e.g. dinosaurs, pterosaurs, crocodiles). Birds share the following skeletal characteristics with reptiles: 1. The skull and atlas are articulated by a single occipital condyle. 2. The lower jaw is composed of several elements and is hinged on a movable quadrate bone. 3. The ear has a single ossicle, the columella (or stapes). 4. The ribs have uncinate processes, a characteristic found elsewhere in only a few reptiles. 5. The ankle is formed by an intertarsal joint. 6. The pubic bone slants backward as in some dinosaurs. Until recently it was generally accepted that birds arose from the pseudosuchian thecodontians, a group of primitive archosaurian reptiles. Recent reevaluation of the fossil record strongly indicates that the immediate ancestor of birds was among the small coelurosaurian theropod dinosaurs (see EARLY EVOLUTION OF BIRDS). The Jurassic bird Archaeopteryx possessed a remarkable combination of reptilian and avian features (see ARCHAEOPTERYX). There is great diversity in the form of avian skeletons, which is evident when the skeletons of ratites, penguins, or hummingbirds are compared with those of typical songbirds. Many of our ideas about the relationships of the higher categories of birds are based on characteristics of the skeleton. Most of these ideas were developed at the turn of the century, after which morphological studies generally declined. Recently systematists have shown renewed interest in using skeletons for a variety of taxonomic and evolutionary ecological studies. Skeletons offer a wider variety of measurable characteristics than do skins for those interested in variation among and between populations and a host of qualitative characters for those interested in phylogenetic studies. Unfortunately, few such studies have considered the physiological adaptations of bone mentioned above. Thus, similarities between species which use similar environments, such as grebes (Podicipedidae) and divers (Gaviidae), or flamingos (Phoenicopteridae) and avocets (Recurvirostridae), are as likely to be the result of adaptations as they are to be the result of common ancestry. Current museum skeletal collections are grossly inadequate for the work which needs to be done. Special avian features. Most of the striking features of a bird's skeleton are associated with its two independent and specialized methods of locomotion, flying with the forelimbs and walking with the hind ones. In typical birds, both fore and hind limb girdles are stoutly built, since each has to support the whole weight of the body alone when the bird is, respectively, flying or walking. The shoulder (pectoral) girdle and sternum form a unit that is firmly (although not immovably) attached to the ribs, and the pelvic girdle is rigidly fastened to a long segment of backbone. Birds have forelimbs with highly modified skeletons in which the arm, forearm, and hand all playa part in supporting the wing (see WING, COMPARATIVE ANATOMY OF).

The hindlimb is also specialized. Some of the metatarsals, which actually belong to the foot, are fused and lengthened so that the leg, like those of certain dinosaurs and running mammals, appears to contain an extra segment. The vertebral column, except for the neck region, is comparatively immobile, and many of the vertebrae are fused. As in

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Fig. 3. Neck vertebra of bird: (A) from in front, (C) from behind; (B) shows hind part of vertebra from the side. as. articular surface; pz, poz. pre- and post-zygapophyses.

the skeleton of many birds is lightened by extensive pneumatizauon. Vertebrae and ribs. The vertebral column of birds is usually subdivided into cer~ical (~eck), thoracic (chest), lumbar (loins), sacral (hip), and caudal (tall) regions. The total number of vertebrae varies between about 40 and 60; most of the difference is due to variation in the number of cervical vertebrae. The joint surfaces of most of die unfused vertebrae are heterocoelous (saddle-shaped) (Fig. 3), but in penguins, waders or shorebi~ds (Charadrii), and parrots some of the thoracic vertebrae may have opisthocoelous (hollowed out behind ovoid) joints. The first two cervical vertebrae (atlas and axis) differ in structure from the rest: in the hornbills (Bucerotidae) they are fused into a single bone. Some of the ~ter~saurs,

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Fig. 4. Skeleton of trunk of goose Anser sp. (After Kingsley, Comparative Anatomy of Vertebrates, 1917). ac. acetabulum; c. carpals; co. coracoid; f. femur; fu, furculum: h. humerus; il, ilium; is. ischium; k. sternal keel; me. metacarpals; D. sternal n.0tch; ph. phalanges; pu, pubis; r. ribs; ra, radius; sc. scapula; sr, sternal nbs; st. sternum; ul. ulna; un. uncinate process; II, III, IV, digits. Curved arrow shows direction of pull of pectoralis secundus muscle.

Skeleton, post-cranial

neck vertebrae are highly modified in the darters (Anhingidae), most cormorants (Phalacrocoracidae) and herons (Ardeidae), in which the neck is permanently kinked but can be partly straightened suddenly to capture fish. The rib-bearing thoracic vertebrae have little movement, and some of them may be fused. The ribs articulate with the vertebrae by two heads and are divided into dorsal (vertebral) and ventral (sternal) segments which are jointed together (Fig. 4). The sternal segments are bony, unlike the corresponding costal cartilages of mammals; possibly their ossification, although it also occurs in ratites, is an adaptation to the stresses of flight. Most of the ribs have uncinate processes, each bound by ligaments and muscles to the rib behind, which help to strengthen the chest.

545

brace the wings apart. The clavicles are much reduced in a few flying birds (e.g. some parrots). Reduction or loss of the clavicles is also seen among certain ground-living birds; these include the ratites, in which the two bones do not even approach one another in the midline. In ratites the forelimb as a whole is reduced, especially in the kiwis (Apterygidae) and the giant extinct' moas (Dinornithidae); in the latter the skeleton of the arm and hand seems to have been entirely absent. The head of the humerus is expanded and has crests for muscle attachments. Its outer end articulates with the radius and ulna. The latter is the stouter of the two forearm bones and often bears a row of quill knobs where the secondary flight feathers attach. The relative lengths of the wing segments (arm, forearm, manus) vary widely among birds, the functional significance of which needs more work; they are said to be correlated with the type of flight. Generally, in strongly flying birds (e.g. swifts) the forearm and hand are longer than the humerus; in soaring birds (e.g. albatrosses Diomedeidae) the reverse is true. The carpal bones of the wrist are reduced in the adult to two (radial and ulnar complexes), although others occur in the embryo and later either disappear or fuse with each other or with the metacarpal (to form a carpometacarpus). Only three of the fingers are present; whether these represent the I, II, and III or the II, III, and IV digits of the series is in dispute. (The II, III, and IV convention is used here.) Each digit is represented by a metacarpal and one or more phalanges. Metacarpal II is fused with the base of III, and III and IV are partly fused. The II digit has some power of independent movement and carries the bastard wing (alula). In a few birds one or more of the digits are clawed. The nestling Hoatzin Opisthocomus hoazin uses these for scrambling about after leaving the nest. (See also WING.) Pelvic girdle and hindlimbs. As in other vertebrates, the pelvic girdle

Fig. S. Pelvis and synsacrum of fowl, seen from below. cv. caudal vertebrae; fo, fossa for part of kidney; il, ilium; is. ischium; pp. pectineal process; pu, pubis; py. pygostyle; sy. synsacrum.

A number of posterior thoracic, lumbar, sacral, and anterior caudal vertebrae are fused together to form the synsacrum (Fig. 5). This is ancylosed or at least very firmly attached to the pelvic girdle, so that the weight of the body when borne by the legs is widely distributed along the backbone. Behind the synsacrum are a number of movable tail vertebrae and then a structure composed of several fused elements known as the pygostyle (plough-share bone). This bone carries the tail feathers, and its movements are important to flight. Sternum. The sternum or breastbone has a well-developed keel (carina) in modern flying birds (carinates), to which are attached the strong pectoral muscles. Its posterior end varies in shape, having one or two notches or holes (fenestrae), or one of each, on each side in many species (Fig. 4). In swans (Cygnus spp.) and some cranes (Gruidae) it is hollowed in front to contain folds of the trachea. There is no sternal keel in ratites; the sternum is flat ('raft-like') or slightly bossed. Pectoral girdle and wings. The pectoral girdle (Fig. 4) consists, on each side, of the scapula, coracoid, and clavicle. The scapula is very long and firmly attached to the ribs by muscles and ligaments; the coracoid extends down from the front of the scapula to the sternum. The glenoid cavity, with which the head of the humerus articulates, is situated at the junction between scapula and coracoid. It is shallow, allowing the limb free mobility. Each clavicle articulates with the front of the coracoid and scapula so that a hole, the foramen triosseum, is enclosed between the three bones. The tendon of the supracoracoideus muscle passes through this hole and, curving backwards, is attached to the head of the humerus; this muscle gives the wing power on its upstroke (see FLIGHT). The two clavicles are usually fused in the midline forming the furcula ('wishbone' or 'merry thought'). The angle of the furcula is generally widest in birds with strong flight, the bone acting as a curved strut to

m Fig. 6. Right leg and foot of fowl, seen from in front.

6. fibula; mt.I, first metatarsal; mt. fused metatarsals; ph. phalanges; tao tarsal contribution to tibiotarsus above and tarsometatarsus below shown between the interrupted lines. ti, tibia. I-IV, digits.

546 Skeleton, post-cranial

is formed, on each side, by the ilium, ischium, and pubis, which are partly fused. The pubis has a most unusual orientation, found elsewhere only in some dinosaurs: it lies parallel to and beneath the ischium (Figs 4, 5). Except in the Ostrich Struthiocamelus, the pubic bones do not meet to form a symphysis enclosing the pelvic outlet; this condition may be related to the size and hardness of the bird's egg. The acetabulum, into which the head of the femur fits, lies at the junction of the three pelvic bones and is perforated. Behind it there is usually a large ischiatic foramen. The proximal end of the femur has a prominent process (trochanter) to which muscles are attached. Many species have a kneecap, or patella. The condyles of the femur articulate with the tibia and fibula at the knee. The tibia, the inner of these bones, is much the larger. In most birds the fibula ends as a thin splint about two-thirds of the way down the tibia (Fig. 6), though in a few (e.g. penguins) it may reach the ankle (intertarsal joint). A bird's ankle is constructed very differently from that of a mammal. In most vertebrates a series of small bones, the tarsals, is arranged in two rows between the bones of the leg and those of the foot. In birds, however, some of the tarsals of the proximal row have disappeared while others have fused with the lower end of the tibia. Thus the tibia referred to in the previous paragraph should, strictly speaking, be termed the tibiotarsus. Similarly, some of the bones of the distal tarsal row have become fused with the metatarsus. Consequently, the ankle joint is actually situated between the proximal and distal rows of tarsals, instead of between the proximal tarsals and the leg bones as in man. These observations have been derived mainly from the study of embryos and cannot be verified from adult skeletons. Most birds have 4 toes, each represented by a metatarsal element and a number of phalanges. The fifth toe is normally absent. The metatarsals of the second, third, and fourth toes are very long and fused; some of the tarsals are fused with their proximal ends. The result is a single bone known as the tarsometatarsus; its compound nature is apparent at its distal end, where it divides into three pulley-shaped processes or trochleae, each corresponding with one metatarsal (Fig. 6). In penguins the metatarsals are less closely fused than in other birds; this is no longer regarded as a primitive feature, since it has been shown that the fusion was often more complete in fossil than in living forms. The second, third, and fourth toes each articulate with the appropriate metatarsal pulley and generally point forward. They contain 3, 4, and 5 phalanges, respectively, the distal one being clawed. In many birds there is also another toe, the first (hallux), which is short and points backward. Its metatarsal is small and attached to the back or side of the tarsometatarsus; it contains at most only 2 phalanges. Since it is opposed to the other toes, it may be an important aid in perching. It tends to be reduced in birds that do not perch and may be elevated some distance above the other toes. In ratites (except kiwis) it is absent. The Ostrich is peculiar in having only 2 toes, probably the third and fourth. Special modifications of the feet in various birds are described in LEG. Pneumatization. Some of the bones in birds contain extensions from the nose and middle ear (in the case of the skull bones) or from the air-sacs that originate from the lungs (see RESPIRATORY SYSTEM). During the process of pneumatization, which begins in the late embryo and is not completed until some time after hatching, these extensions grow into the bones. Th~ holes through which they enter may be seen in the dry skeleton; In the humerus, for example, there is a large pneumatic foramen on the inner aspect of the proximal end. The number of bones that become pneumatized varies greatly, but accurate data on the extent of pneumaticity are available for only a few species (see PNEUMATIZATION J.G.S. OF BONE). A general account of the skeleton, with extensive references to the literature is ' given by the first four of the following: Bellairs, ~. d'A. & Jenkin, C.R. 1960. The skeleton of birds. In Marshall, A.J. (ed.). Biology and Comparative Physiology of Birds, vol. 1. New York.

George, J.C. & Berger, A.J. 1966. Avian Myology. New York. Portmann, A. 1950. In Grasse, P.-P. (ed.). Traite de Zoologie, vol. 15. Paris. Stresemann, E. 1927-1934. Aves. In Kukenthal, W. & Krumbach, T. (eds.). Handbuch der Zoologie, vol. 7 pt. 2. Berlin. Baumel, J.J. 1979. Osteologia. In Baumel, J.J. (ed.). Nomina Anatomica Avium. New York. Baumel, J.J. 1979. Arthrologia. In Baumel, J.J. (ed.). Nomina Anatomica Avium. New York.

Bock, W.J. 1974. The avian skeletomuscular system. In Farner, D.S. & King, J.R. (eds.). Avian Biology, vol. 4. New York. Liem, K.F. 1977. Musculoskeletal system. In Kluge, A.G. (ed.). Chordate Structure and Function, 2nd edn. New York. Ostrom, J.H. 1976. Archaeopteryx and the origin of birds. BioI. J. Linn. Soc. 8: 91-182. Storer, R.W. 1971. Adaptive radiation of birds. In Farner, D.S. & King, J.R. (eds.), Avian Biology, vol. 1. New York.

Black Skimmer Rynchopsniger. (B.P.).

SKIMMER: substantive name of the 3 species of the family Rynchopidae (Charadriiformes, suborder Lari); also called shearwater, sea dog, or scissorbill. The Indian Skimmer Rynchops albicollis inhabits India, Pakistan and Burma; R. flavirostris is African; and the Black Skimmer R. niger has several races in eastern North, Central and South America. Characteristics. Skimmers, c. 40cm long, are brownish-black above with white underparts, face and forehead. Their bills are yellow or red with black or yellow tips, and their small, moderately webbed feet are also red. Similar in body weight to a medium-sized tern or small gull, they appear deceptively large because of their relatively long, pointed wings and long, deep, laterally compressed bill. Females resemble males but are markedly smaller, averaging 250 g as opposed to 350 g for males of North American niger. Juveniles differ from adults in having dark bills and feet and the upper parts streaked with brown and buff. Skimmers are unique among birds in that the pupil closes to a narrow, vertical slit in bright light. Anatomical and behavioural studies show affinities with gulls, terns, and skuas, and suggest an early departure of the skimmer line from the ancestral Lari. Habitat. In South America and the Old World skimmers frequent lakes and rivers, breeding on sand bars exposed during the dry season. When rivers run high during the rainy season they move to estuaries and the coast. Perhaps because high river water coincides with the breeding season of North American skimmers, they are exclusively coastal,

~ A 2

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B

Fig. 1. Bill of the Black Skimmer Rynchopsniger. (A). La~eral vie~ of adult. 1 and 2 are planes of sections shown in (B). (B) Oblique sections of upper (1) and lower (2) mandibles. (C). Bill of 87g chick in lateral and ventral views. (R.L. Zusi)

Skua

547

Fig. 2. Black Skimmer Rynchops niger catching fish. Drawn from selected frames of a single motion picture sequence. (R.L. Zusi)

breeding on barrier islands and dredge banks. The more northerly and southerly populations of niger perform north-south migrations. Food. In bill structure and feeding behaviour Rynchops is unique. The lower mandible is laterally flattened like a knife blade and it protrudes well beyond the upper, which itself is narrow and oval in cross section (Fig. 1). A skimmer can raise its upper jaw about 45° above the closed position while depressing the lower jaw. Skimmers catch their prey (fish and shrimps) by flying low over the water with the upper jaw.raised and the lower jaw open and immersed. When the sharp edge of the lower mandible strikes prey the head doubles under the body of the flying bird and the jaws snap shut (Fig. 2). The prey is drawn out of the water while the bird's head faces back or down, and is swallowed in flight or after the bird alights. Motion of the head cushions the shock and enables the shorter upper mandible to reach prey struck beyond its grasp. With the upper jaw raised during skimming, the lower jaw cuts the water unobstructed and the chance of striking prey is increased. The oft repeated statement that fish slide up the inclined edge of the lower mandible is incorrect. Usually skimmers feed in shallow water containing high concentrations of prey. Flying in ones or twos, or sometimes in loose flocks, they cut a straight path apparently without seeing individual prey, but the birds are attracted to surface disturbances caused by swarms of fish. Their essentially tactile method of foraging permits them to feed also at night, which they do even under the darkest conditions. The lower jaw of a foraging bird may strike submerged obstacles or the muddy bottom, and the head then doubles under the body. Breakage and abrasion at the tip of the rapidly growing rhamphotheca of the lower jaw control its length. Fishing rates in the Black Skimmer have been measured under various conditions at one fish per half minute (rarely much faster) to one per 6 minutes of skimming. Sometimes a catch is lost through kleptoparasitism by gulls. Behaviour. When not feeding, skimmers typically preen, bathe, or rest in a dense flock facing into the wind. The Black Skimmer exhibits a variety of displays associated with aggression, pair formation and maintenance, territorial defence, and copulation. These show little correspondence to displays of the blackcapped terns, but resemble those of noddies Anous, gulls, and skuas. Only with the latter do they share a distraction display when the young are threatened. Voice. The voice of niger is a short or protracted arp, arp ... , and of albicollis a nasal kap, kap ... recalling the yapping of young fox hounds; that of the smaller flavirostris is a sharp kik kik ... , or a harsh, tern-like kreeep, Breeding. Skimmers nest in loose colonies, generally on open sand or shell, but niger occasionally nests on seawrack in salt marsh with terns, or even on gravel roofs. Colonies vary in size from only a few birds to many hundreds or several thousands. In mixed colonies Common Terns Sterna hirundo usually outnumber the Black Skimmer and are more aggressive, affording the skimmers protection from predatory gulls. The African Skimmer, however, is known to mob and chase away such predators as Sacred Ibis Threskiornis aethiopicus, herons, monitor lizards, and crocodiles. Mortality of eggs is caused by sudden rain squalls, and some colonies are subject to destruction from storm tides. Skimmers are single-brooded but they will lay again after destruction of eggs during a period of about 2 months in eastern North America. The nest is a hollow maintained by kicking sand back while the bird

success of about 800/0, but 10 of 11 surviving fledglings were the first hatched of the brood, which pecked and chased younger siblings at feeding time. It is stated of flavirostris that the first chick wanders off within a day of hatching and the remaining eggs are abandoned. Parents are known to wet their feet and belly feathers while flying over water before returning to incubate or brood, presumably to promote cooling of the eggs or young; out of the breeding season wetting of these parts probably serves to wash off mud (see BELLY SOAKING). Chicks, difficult to see in their cryptic down, squat and dig into a hollow in the sand, sometimes kicking sand on to their backs. They are offered freshlycaught fish or shrimps carried from the feeding ground crosswise in the adults' bills. The mandibles of chicks are of nearly equal length, permitting them to take food from the adult or from the ground (Fig. 1). Young begin to fly at about 5 weeks and at this time the differentiation in mandible lengths is under way. Fledged young continue to beg from their parents or other adults, but they also engage in skimming. A young bird flying with its parents probably learns quickly the most auspicious places in which to forage. R.L.Z.

variety of brown, black, and lilac spots and blotches. In North America clutches are usually 4 (2-5); in Africa and Asia usually 3 or less (1--4). Both sexes incubate and care for the chicks. Incubation begins with the first egg and lasts about 3 weeks. One study of niger showed a hatching

SKUA: substantive name, especially in British usage, of all members of the Stercorariidae (Charadriiformes, suborder Lari); in the plural, general term for the family. Usage in North America and elsewhere prefers the name 'jaeger' (German word meaning 'hunter') and restricts

squats or incubates. Eggs are creamy white marked with an endless

Erwin, R.M. 1977. Black Skimmer breeding ecology and behavior. Auk 94: 709-717. Erwin, R.M. 1979. Species interactions in a mixed colony of Common Terns (Sterna hirundo) and Black Skimmers (Rynchops niger). Anim. Behav. 27: 1054-1062. Modha, M.L. & Coe, M.J. 1969. Notes on the breeding of the African Skimmer Rynchops flavirostris on Central Island, Lake Rudolf. Ibis Ill: 593-598. Murphy, R.C. 1936. Oceanic Birds of South America, vol. 2, New York. Sears, H.F., Moseley, L.J. & Mueller, H.C. 1976. Behavioral evidence on skimmers' evolutionary relationships. Auk 93: 170-174. Zusi, R. 1962. Structural adaptations of the head and neck in the Black Skimmer, Rynchops nigra L. Pub!. Nuttall Orne Cl. no. 3: 1-101.

SKIN: the protective and containing integument of the body, consisting of an underlying dermis and an overlying epidermis. The dermis is relatively thick and highly organized, being supplied with muscles, blood vessels, and nerves. The thinner and simpler epidermis consists of layers of cells, renewed by proliferation from the basal (Malpighian) layer as the outer layers die and become horny (keratinized). The epidermis of birds is notable for the special external structures to which it gives rise and by which it is almost wholly covered--especially the feathers, but also the horny sheathing of the bill, legs, and feet, with the claws on these last (see FEATHER; BILL; LEG). Correlated with the presence of this covering is the almost complete absence of skin glands; the exceptions are a few small glands within the external auditory meatus and the oil gland on the rump (see OIL GLAND). The skin of birds thus does not perform the function of sweating, which has an important physiological role in mammals, and does not produce a sebaceous secretion for lubrication of its surface or outgrowth; nor can it playa great part in heat transmission (see HEAT REGULATION). The skin is, however, supplied with tactile nerve-endings or 'Herbst's corpuscles' (see TOUCH). Its blood vessels give the skin, at least in some instances, the capacity of exhibiting transient colour changes (flushing), visible on bare patches or even through the horny covering of bill and legs (see HERON; OSTRICH). In some birds there are such appendages as spurs, wattles, combs, lappets, sacs, or pouches (see INTEGUMENTARY STRUCTURES). For care of the body surface generally see under COMFORT BEHAVIOUR. 'Skin' is also the term applied to the usual unmounted study specimen of a bird (see MUSEUM).

548 Skua

Great Skua Stercorarius (Catharacta) skua. (B.P.).

'skua' (from Icelandic word 'skufr') to Catharacta. The family contains 2 genera, Catharacta (not recognized elsewhere in this work) and Stercorarius; the latter has 3 species, all northern: the Arctic Skua (or Parasitic Jaeger) S. parasiticus, the Pomarine Skua (or Pomarine Jaeger) S. pomarinus, and the Long-tailed Skua (or Long-tailed Jaeger) S. longicaudus. Catharacta, formerly considered to be a superspecies with one boreal representative and several forms in the far south, is now divided into 3 species. (1) C. skua comprises 4 allopatric sub-species distinguished by plumage and measurements: C. s. antarcticus (Falkland Skua), C. s. lonnbergi (Brown or Subantarctic Skua), C. s. skua (Great Skua), and C. s. hamiltoni (Tristan Skua). (2) C. maccormicki (South Polar or McCormick's Skua) breeds on the Antarctic continent, overlapping C. s. limnbergi with limited hybridization on the Antarctic peninsula. (3) C. chilensis (Chilean Skua) overlaps with C. s. antarcticus in Patagonia, also with some hybridization. Characteristics. The skuas are sometimes treated as a subfamily of the Laridae. They are similar to gulls in size (lengths 50-58 em) but have dark plumage, and a faster, stiffer wingbeat. They are widely known for their habit of chasing other seabirds in flight until they disgorge food (see PIRACY). Like gulls, they are chiefly associated with the sea, but may breed far inland. In Stercorarius, adult plumage varies between a light phase, with the underparts and collar creamy or almost white and the head conspicuously dark-capped, and a dark phase with the whole plumage almost uniformly dark (see POLYMORPHISM). The dark phase is very rare in S. longicaudus and possibly does not occur in adult plumage; in the other 2 species the proportion of light and dark birds varies from area to area. In Shetland less than one fifth of the Arctic Skuas are light, but further north the proportion is generally higher, up to almost 100°10 in Svalbard and arctic Canada. In Stercorarius the primary shafts and bases are always white, but less prominent than in Catharacta; the 2 central rectrices are much elongated-pointed and fluttering in S. longicaudus but twisted through 90° and appearing clubbed in S. pomarinus. The bill is gull-like, unusually soft in its basal half, where a pair of separate thin plates overlie the nostril area, but hard and rather strongly hooked towards the tip. The feet are gull-like also, but with more strongly curved, sharp claws. Juveniles of all Stercorarius species are barred below. Barring may be retained in immature plumage and is found in a very small proportion of breeding adults. During winter adults may become somewhat barred below, apparently due to partial moult of body feathers. Among Catharacta, only juveniles of C. chilensis show any barred plumage, and this is confined to the back and scapulars. In Catharacta the plumage is generally brown, with conspicuous white wing patches at the base of the primaries. C. maccormicki is dimorphic, with light phase birds increasing

in frequency at higher latitudes. The wings appear a characteristic velvety-black, contrasting with the body colour. C. chilensis adults are decidedly rufous in body colour, have cinnamon under wing coverts and the head has a markedly capped appearance. C. s. lonnbergi is a large, heavy form with a fairly uniform medium brown plumage, C. s. antarctica relatively small with a stubby deep and powerful bill, while C. s. hamiltoni is intermediate in appearance between C. s. lonnbergi and C. s. skua; adults of the latter can be identified by their conspicuously streaked plumage. Habitat. All skuas are marine outside the breeding season, but probably frequent areas less than 50km from coasts, although they remain entirely independent of land. Catharacta breeds socially, although nest dispersion varies greatly between and within species. Colonies are often adjacent to bird cliffs or penguin rookeries, on open ground. The Arctic Skua nests in colonies on moorland in association with seabird communities in Scotland, the Faeroes, Iceland and elsewhere, but also nests in well dispersed territories on arctic tundra. Pomarine and Long-tailed Skuas are exclusively tundra nesters. Distribution. The 3 Stercorarius species are northern circumpolar breeders. Their ranges overlap widely. S. longicaudus generally extends furthest north. The breeding of all 3, but especially S. pomarinus is influenced by local fluctuations in lemming Lemmus abundance. The 3 species exclude each other from their territories. S. pomarinus is highly nomadic and moves to areas of lemming abundance. In years when it breeds, it excludes the 2 smaller species from the area. Catharactaskua is notable for having a bipolar distribution. C. s. skua is confined to the North Atlantic, nesting in Shetland, Orkney, Caithness, Sutherland and the Outer Hebrides, the Faeroes, Iceland, and has recently colonized Bear Island, Svalbard and north Norway. Non-breeders may appear anywhere in the North Atlantic, from Svalbard to Brazil. C. s. hamiltoni nests only on Gough and Tristan, C. s. antarctica nests on the Falkland Islands and adjacent coast of South America, and C. s. lonnbergi nests on part of the Antarctic peninsula, and on subantarctic islands all round the continent. C. maccormicki nests on the Antarctic continent. C. chilensis nests along the west and south coasts of South America south of 35°S,and on the east coast between Puerto Deseado and Puerto Gallegos. Populations. On the edge of its range, in Scotland, numbers of Arctic Skuas have increased a little this century, lately to around 2,400 breeding pairs, but in the Faeroes numbers have declined considerably in recent years. In the Arctic, numbers of the 3 Stercorarius species are unknown, but presumably large. C. s. skua has a total population of 12,000 breeding pairs, half nesting in Britain, with the largest single colony of 3,000 pairs on Foula (Shetland). C. s. hamiltoni numbers less than 6,000 breeding pairs, C. s. antarctica between 3,000-5,000 pairs, C. s. lonnbergi about 20,000 pairs, C. maccormicki about 7,000 pairs and C. chilensis at least 10,000 pairs. In addition, each population contains large numbers of immature birds, perhaps about equal to the number of breeding pairs. Movements. Stercorarius spp. are all long-distance migrants. S. pomarinus has a well-marked winter concentration off the highly productive coast of West Africa between 25° and SON, and non-breeders occur there in summer also. S. parasiticus winters further south, commonly on the continental shelves of southern Africa and Australia, but dark phase birds apparently move less far south than light phase individuals, indicating a leap-frog migration. Fledglings of C. s. skua migrate to south-west Europe in winter, with most ringing recoveries off the coast of Iberia, while some move as far as Brazil, Guyana and the Cape Verde Islands. In summer the immatures move northward again, many 2 to 4 year old immatures visiting high latitudes between Greenland and Svalbard. A high proportion of adults remain in British waters throughout winter. Icelandic birds show similar movements to the British population but with a large number of birds migrating down the west coast of the Atlantic, where very few British Great Skuas are found. Food. S. pomarinus feeds largely on lemmings in summer and by predation on small seabirds (notably phalaropes) in winter, less regularly by fishing or piracy. S. longicaudus lives on lemmings, insects, berries, small birds and eggs in summer and by piracy, chiefly on terns, in winter. In arctic tundra areas S. parasiticus feeds on insects, berries, small birds and eggs and only to a limited extent on rodents. In coastal areas, such as Orkney and Shetland, it subsists largely by piracy on terns, auks and Kittiwakes Rissa tridactyla, similarly in winter. C. s. skua variously splash-dives for surface fish, preys directly on seabirds and terrestrial mammals, robs gulls, auks and Gannets Sula bassana of food and scavenges, e.g. behind fishing boats. Southern Catharacta have a similar

Skull

range of feeding habits; C. s. lonnbergi is particularly associated with penguin rookeries, but C. maccormicki survives largely by catching food for itself at sea. Behaviour. Skuas are normally monogamous and pair for life. In C. s. skua a few exceptional cases have been recorded where a male paired with 2 females which layed in the same nest; in C. s. limnbergi colonies on islands off New Zealand and on Marion Island, such trios have also been found to occur regularly, as have others comprising 2 males and 1 female, although this social system is not found in any of the other Catharacta. Distances between skua nests vary from the extreme spacing on arctic tundra, where nests are often 2 km or more apart and skuas defend at least 1sq km against congenerics (hunting over some 3 sqkm), down to a spacing of nests only 5 m apart, in rare cases within colonies on small islands off north Scotland. On Foula, 306 pairs of Arctic Skuas bred in a colony occupying 1.7 sq km, or approximately the area defended by a single pair breeding on arctic tundra. A partial explanation for the variation lies in the fact that the birds nesting in Shetland do not obtain a significant amount of food within the territory, but feed at sea. There have been detailed studies of the behaviour of each species of skua. Most exhibit the same display patterns, although only the smaller species use a 'distraction display' as well as diving on intruders near the nest. Whether standing, swimming or flying, Catharacta typically display their white wing patches by stretching their wings vertically upwards, back to back, an advertisement posture found in less intense form in the Pomarine Skua, but not found in Arctic or Long-tailed Skuas. Voice. Skuas are very vocal at their breeding places, but are usually silent elsewhere. Stercorarius spp. make high-pitched cat-calls and harsh, deeper notes. Catharacta spp. have a short grunting call and a long display call which is used in mate-greeting and indicating ownership of territory or food items. Breeding. As skuas have only two brood patches, birds with 3 eggs usually fail to hatch any. Clutches of 2 are normal with about 10% laying only 1 egg. Although hatching success of skua clutches is normally high, in Catharacta colonies, where food is short, usually only one chick is fledged by each successful pair; the second-hatched chick, younger by one or 2 days, is often killed by its sibling. S. parasiticus begins to breed (on Fair Isle) at between 3 and 6 years of age (most at 4), but apparently at a younger age in arctic Russia. C. s. skua begins to breed (on Foula) at between 5 and 10 years of age (most at 7 or 8), but a year earlier in the small colony on Fair Isle between Orkney and Shetland. See photos AGGRESSION; PIRACY. R.W.F. Andersson, M. 1973. Behaviour of the Pomarine Skua Stercorarius pomarinus Temm. with comparative remarks on Stercorariinae. Ornis Scand. 4: 1-16. Andersson, M. 1976. Social behaviour and communication in the Great Skua. Behaviour 58: 40-77. Devillers, P. 1978. Distribution and relationships of South American Skuas. Le Gerfaut 68: 374-417. Furness, R. W. 1978. Movements and mortality rates of Great Skuas ringed in Scotland. Bird Study 25: 229-238. Furness, R.W. 1979. Foods of Great Skua Catharacta skua at North Atlantic breeding localities. Ibis 121: 86--92. Maher, W.J. 1974. Ecology of Pomarine, Parasitic and Long-tailed Jaegers in northern Alaska. Pacific Coast Avifauna 37: 1-148. O'Donald, P. 1983. The Arctic Skua: a Study of the Ecology and Evolution of a Seabird. Cambridge. O'Donald, P., Wedd, N.S. & Davis, J.W.F. 1974. Mating preferences and sexual selection in the Arctic Skua. Heredity 33: 1-16. Young, E.C. 1978. Behaviour ecology of liinnbergi skuas in relation to environment on the Chatham Islands, New Zealand. New Zealand Journal of Zoology 5: 401-416.

SKULL: the bony and cartilaginous elements of the head, housing the brain and special sense organs, and providing a rigid framework for the feeding apparatus (jaws and hyoid). The remainder of the bird's skeleton is treated separately (see SKELETON, POSTCRANIAL). General topography and nomenclature of parts are considered first, followed by a review of mechanical properties. The positions of most of the skull bones (the majority paired, occurring on each side) are shown in Fig. 1, and only a few are named in the text. On the whole, they are similar to those of reptiles, although certain reptilian bones such as the postorbital are

absent, and the temporal region is much modified. The skull is light, and often extensively pneumatized (see PNEUMATIZATION OF BONE), with a compact, rounded braincase. It is pierced by various foramina which transmit cranial nerves and blood vessels. Usually, the cranial sutures

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550 Skull

close early in life, so that identification of the various bones in the adult may be difficult. Articulation with the atlas is by a single occipital condyle. Orbits and nares. The orbits are usually very large, and, except in a few forms such as parrots, are not completely ringed by bone. They are separated from each other by a vertical plate known as the interorbital septum or mesethmoid bone; this is generally incomplete, the gaps being filled in life by connective tissue or cartilage. In the kiwis Apteryx, which have (for birds) very small eyes, this septum is absent, and the orbits are separated mainly by the very large nasal cavities; this is a specialized condition associated with the great development of the organs of smell (see SMELL). The external nostrils are set back near the base of the bill, except in the kiwis where they are at its tip. In some birds, e.g. gannets Sula spp., the nostrils become closed by the growth of the surrounding bones (see RESPIRATORY SYSTEM). The nasal cavities, which are lined by mucous membrane, and the cartilaginous nasal capsule that invests them, are situated inside the bones of the bill. Each nasal cavity opens in front at the external nostril and on the palate at the internal nostril; it is separated from that of the opposite side by a cartilaginous septum. Turbinal cartilages project into each nasal cavity from its outer wall, increasing the area of mucous membrane. In some birds, the nasal capsule and septum are poorly ossified. Upper jaw and palate. The skeleton of the upper jaw is formed mainly by the premaxillae, which in life are sheathed by the horny rhamphotheca. The attachment of the upper jaw to the skull is flexible, so that, as in many reptiles, it is able to move relative to the braincase; this property, known as cranial kinesis, is discussed further below. Key elements in kinesis are the quadrates, which articulate with the cranium at the rear of the orbit. Their lower ends in turn articulate with the jugal bars (jugal and quadratojugal), and with the pterygoids, which rostrally articulate with the palatines. Other elements of the palatal complex and their variations are treated separately (see PALATE). Lower jaw. The lower jaw, on each side, is usually made up of 6 bones, the front one being the dentary (generally the largest) and the rear one the articular. The latter may be produced backwards as a retroarticular process, giving increased attachment area and leverage for M. depressor mandibulae. This increases the force of jaw opening-a feature of birds which excavate for food by 'gaping', i.e. inserting the closed jaws into a substrate, then opening them. Articulation with the rest of the skull is between the quadrate and the articular. The two halves of the lower jaw meet in a symphysis of varying length rostrally. In several groups, lateral flexion can occur along the free ramus on either side, permitting the gape to be widened, a mechanism discussed further below. Teeth are unknown in any recent bird, though some workers have claimed to identify rudimentary tooth-germs in bird embryos. Hyoid skeleton. The tongue is supported by a median bone, the entoglossum; this is often partly cartilaginous, and may take the form of paired bones linked by cartilage or ligament, as in many parrots. It articulates with another median element (the basibranchiale) from the caudal end of which arise the paired cornua or hyoid horns, each consisting of a ceratobranchiale anteriorly, articulating with the epibranchiale posteriorly. The horns curve out, then round the posterior end of the mandible to lie near the occipital region of the cranium. In WOODPECKERS, the entoglossum itself is tiny, but the basibranchiale and horns are greatly elongated, giving them the ability to protrude the tongue for great distances; at rest, the horns extend round the top of the skull, in some species even entering a nostril or curving far round the orbit. Ossicles. As in amphibians and reptiles, there is only a single bone, the columella (stapes), for conducting sound vibrations from the eardrum to the inner ear; the form of this ossicle has some value as a taxonomic character (see Feduccia, 1980). The extra 2 mammalian ear ossicles, the incus and malleus, are represented in birds by the quadrate and articular respectively. In some owls, the bony ear region is asymmetrical on the two sides of the head, a condition probably associated with their highly developed ability to locate sound sources. The sclerotic coat of the eye is cartilaginous, and the front of the eyeball is reinforced by a series of usually 16 to 18 small, overlapping bony plates known as scleral ossicles. They assist in the process of visual accommodation (see VISION). In some birds there is also a small horseshoe-shaped bone (os opticus) in the sclera, surrounding the optic

nerve as it enters the back of the eyeball. Sesamoids are present at the quadrate/mandible articulation in many birds, and are exceptionally highly developed in the Kokako Callaeas cinerea of New Zealand. Cranial kinesis. Despite claims that have at times been made that some birds have akinetic upper jaws, it appears that the ability to move the upper jaw relative to the braincase is of universal occurrence throughout the class. For detailed accounts of the mechanism of kinesis, see Bock (1964) and Buhler (1981). Compared with the condition in which only the lower jaw moves, as in mammals, kinesis confers several advantages, viz: (a) Maintenance of the primary axis of orientation. When the jaws are opened, the position of their long axis changes relatively little in position, in contrast to the situation in a mammal, in which it is considerably displaced as the lower jaw moves downward. This property may have great value when fast moving prey has to be captured. (b) In general, cranial kinesis permits a wider gape when the jaws are opened-a feature of special significance in some specialized methods of feeding. (c) Maintaining the mandible in the closed position. Coupling of upper and lower jaws (see below) permits a considerable reduction of the muscular effort needed to hold the jaws closed; if the upper jaw is heavier than the lower, this effort will in fact be nil. (d) Faster closing jaws. (e) A shock absorbing mechanism for all forces acting on the jaws, permitting a lighter skull construction than in mammals. Lightness is also aided by the wider spread of jaw muscle attachments in the kinetic skull, which reduces stress per unit area. Two main types of kinesis are usually recognized. In prokinesis, exhibited by the majority of birds, the whole upper jaw moves about its articulation with the cranium. The articulation is usually formed by a narrow strip of flexible bone though, in large parrots, a set of synovial joints is present instead. Force to raise and lower the upper jaw is provided mainly by muscles attached to the palatines, pterygoids and quadrates (see MUSCULATURE), and is transmitted to the upper jaw via the palatines and jugal bars. In rhynchokinesis, the musculature and palatal complex function in essentially the same way, but the base of the upper jaw is rigid, and bending takes place further forward along the jaw. To make this possible, the upper jaw is separated for much of its length into a median dorsal bar, and paired ventral bars. Backward or forward movement of the ventral bars is permitted either by a flexible nasal bar, or (as in ratites and tinamous) a gap in the nasal bar. Rhynchokinesis occurs in the Gruidae, Charadriiformes, and Trochilidae, and in ratites and tinamous. It reaches its most sophisticated level of development in long-billed sandpipers, such as Snipe Gallinago gallinago or Curlew Numenius arquata (Burton 1974). The bending zone in such species is situated very far forward, enabling the distal region only of the jaws to be opened to grasp subterranean prey while probing. Alternatively, retraction of the upper jaw in highly rhynchokinetic species enables its tip to move backwards relative to the lower, a facility which can be used in shifting food towards the mouth, or in manipulating awkward objects. Lower jaw movements. The simplest and most basic lower jaw movement is depression, in which the whole jaw is rotated downwards about the quadratomandibular articulations. In some birds, notably parrots and finches, these articulations also permit gliding movements, so that the jaw can additionally be moved backwards and forwards. More complicated is the action of lateral spreading, in which the mandibular rami are bowed outwards to enlarge the gap between them. This action is possible only in birds possessing two pairs of flexion zones within the mandibular rami, and is seen in various groups which regularly have to swallow large objects (e.g. many fish-eating birds, gulls and fruit pigeons Ptilinopus) or as an adaptation to special feeding methods (e.g. night jars, pelicans). Spreading of the mandibles is achieved in most cases by the action of part of the pterygoideus muscle, which pulls the medial process of the lower jaw forwards, causing the rear part of the mandibular ramus to swingoutwards. In gulls, this action is also aided by a guiding effect of the quadratomandibular articulation, and in barn owls Tyto is entirely produced by this means, taking place automatically as the lower jaw is depressed. An excellent detailed account of lower jaw structure and mobility is provided by Buhler (1981). Jaw coupling. It is possible for the actions of upper and lower jaws to be coupled, that is to say, mechanically linked so that elevation of the upper jaw cannot occur without depression of the lower. Typically, such coupling is effected by the postorbital ligament, when loaded by muscle

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Bock, W.J. 1964. Kinetics of the avian skull. J. Morph. 114: 1-42. Bock, W.J. & Morioka, H. 1971. Morphology and evolution of the ectethmoidmandibular articulation in the Meliphagidae (Aves). Morph. Jb. 135: 13--50. Buhler, P. 1981. Functional anatomy of the avian jaw apparatus. In King, A.S. & McLelland, J. (eds.). Form and Function in Birds, vol. 2. London. Burton, P.J.K. 1970. Some observations on the Os uncinatum in the Musophagidae. Ostrich Sup. 8: 7-13. Burton, P.J.K. 1974. Feeding and the Feeding Apparatus in Waders. London. Feduccia, A. 1980. The Age of Birds. Cambridge, Mass. Fisher, H.I. 1955. Some aspects of the kinetics in the jaws of birds. Wilson Bull. 67: 175-188. Zweers, G.A. 1974. Structure, movement and myography of the feeding apparatus of the Mallard (Anas platyrhynchos L.). Neth. J. Zool. 24: 323-467.

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