The Migration Ecology of Birds [2 ed.] 0128237511, 9780128237519

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The Migration Ecology of Birds

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The Migration Ecology of Birds Second Edition

Ian Newton

Academic Press is an imprint of Elsevier 125 London Wall, London EC2Y 5AS, United Kingdom 525 B Street, Suite 1650, San Diego, CA 92101, United States 50 Hampshire Street, 5th Floor, Cambridge, MA 02139, United States Copyright © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www. elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein). Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. ISBN: 978-0-12-823751-9 For Information on all Academic Press publications visit our website at https://www.elsevier.com/books-and-journals

Publisher: Nikki Levy Acquisitions Editor: Simonetta Harrison Editorial Project Manager: Hilary Carr Production Project Manager: Selvaraj Raviraj Cover Designer: Miles Hitchen Illustrations by Keith Brockie Typeset by MPS Limited, Chennai, India

Contents Preface to the first edition Preface to the second edition

1.

2.

xiii xv

Introduction

1

Types of bird movements Constraints of breeding Adaptations for migration The diversity of migration Difficult journeys Sedentary populations Hibernation Summary References

2 3 4 5 5 7 7 7 8

Methodology for migration studies Observations of birds on migration Radar studies Distribution studies Ringing Tracking devices Very High-Frequency radio-transmitters Satellite transmitters The mobile phone network Geolocation (Global Location Sensing or GLS logging) Passive Integrated Transponders tags Other sensors Effects of tags Storage of data Future developments Isotopes and other internal markers Research on captive birds Wind tunnels Breeding programmes Mathematical models Concluding remarks Summary References

Part 1 The migratory process 3.

9 9 10 12 13 15 15 16 17 17 19 19 19 19 20 20 21 22 22 22 23 23 24

4.

Migratory flight

29

Body weight, speed and flight mode Wing shape Power requirements in relation to body weight Effects of migratory fattening Ascending Descending Effects of wind conditions Cutting the costs of flight Consequences of flapping and soaring flight The high performance of some migrating waders The role of body size in bird migration Migration by walking or swimming Social factors Rest and sleep Concluding remarks Summary References

29 31 31 32 33 34 34 35 36

Weather and migration

51

Importance of wind Correction for drift Detection of drift Recent developments Low level flight Soaring species Global wind patterns and migration routes Altitude of migration Changes in conditions with altitude Consequences of high-altitude flight Diurnal and nocturnal flight Reverse migration Detours Summary References

53 54 56 56 57 57 57 58 61 61 63 65 65 67 68

41 41 42 42 44 46 47 47

v

vi

5.

6.

Contents

Fuelling migration

73

Energy needs and body composition Costs and benefits of body reserves Water balance and thermoregulation Migration strategies Alternative strategies Mechanisms of fuel deposition Increased feeding rates and feeding times Change of diet Changes in gut structure and digestive capacity Digestive limitations Reducing expenditure Relative contributions Daily rates of weight gain Changes in body composition Body reserves for survival and breeding Concluding remarks Summary Appendix 5.1: Calculation of flight ranges References

74 77 77 78 78 81 82 82 84 84 84 84 85 85 88 90 90 91 92

Amazing journeys

97

Ocean-crossings by landbirds Desert crossings Trans-Saharan flights Physiological constraints Asian deserts and mountains North American deserts High mountains Ice fields Other remarkable migrations Concluding remarks Summary References

7.

Raptors and other soaring birds Major routes The trans-American flyway The Western European West African flyway The Eurasian East African flyway The East Asian Continental flyway The East Asian Oceanic flyway Some general points Loop migrations Use of thermals and other updrafts Water crossings Extension of migration as a consequence of soaring Timing and food supplies Multiple wintering areas Social factors Numbers entering Africa

97 102 104 105 107 109 109 111 112 112 112 113

117 118 120 120 121 122 122 122 123 123 128 129 130 131 131 132

Numbers entering Central and South America Feeding and energy reserves Summary References

8.

Seabird movements The marine environment Winds and seabird movements Migration patterns Direct migrations from breeding areas to lower latitudes Direct trans-equatorial migrations Figure-8 trans-equatorial migrations Dispersive migrations Migrations to higher latitudes in winter Migrations to east or west Circumpolar migrations Migratory stopovers Long-distance foraging trips The pre-laying exodus Foraging flights during incubation and chick care Fattening of chicks Pre-breeding years Navigational achievements Conclusions Summary References

9.

Speed and duration of migratory journeys Theoretical basis Getting around the problems Measures of migration speed Migration speeds from individual ring recoveries Average migration speeds from population-based ring recoveries Migration speeds from tracked birds Seabird migrations Proportion of migration spent in flight Penguins Migration and geographical range Concluding remarks Summary References

10. Finding the way: senses, displacements and social influences Sensory systems Orientation and navigation Displacement experiments

132 132 133 134

139 139 141 142 142 142 143 144 145 145 146 147 147 148 148 149 150 151 151 152 152

155 156 158 159 159 160 163 173 174 176 176 177 177 178

185 185 187 187

Contents

Other evidence for inherited directional preferences Return of displaced adults to breeding sites Return of displaced birds to wintering sites Further comments on displacement experiments Uncertainties over juveniles Convergence of migration routes Social influences Re-establishment of migration routes Summary References

11. Finding the way: orientation and navigation

189 190 191 193 193 194 195 197 197 198

201

Visual landmarks The sun and polarized light Evidence that birds use the sun as a compass The sun and navigation Evidence that birds use polarized light as a compass The stars The stars and navigation Integrated use of celestial cues The magnetic field Evidence for use of the magnetic field Magnetic navigation Pelagic seabirds Response to specific areas (location cues) Magnetic cues and vagrancy Odours Infrasound and pressure changes Cue conflicts Conclusions on cue-conflicts and recalibration Problems at high latitudes Problems at low latitudes Rhumblines and great circles Dispersive migration Concluding remarks Genetically encoded spatial information Summary References

202 202 202 204 204 205 206 206 206 208 209 211 211 212 213 215 215 216 216 217 217 218 218 220 220 221

Part 2 The timing and control of migration 12. Annual cycles Variations in annual cycles Split migrations Other movements

229 230 232 234

Geographical and other variations within species Relationship between moult and migration Breeding seasons split by migration Sex and age differences Exceptions to general patterns Concluding comments on annual cycles Non-annual cycles Domino effects, catch-ups and delays Internal time keeping Importance of daylength Endogenous rhythms in migrants Geographical variation in photoperiodic responses Equatorial birds Flexible cycles Summary References

13. Migratory control mechanisms Obligate and facultative migration Role of dominance in facultative migrants Migration timing, distances and directions Time-distance programmes Directional preferences Integration of time distance and direction programmes Role of experience Migratory fattening and restlessness Diurnal patterns Autumn migration Split migrations Relationship between breeding, moult and autumn migration Spring migration Spread and consistency in spring departure dates within populations Different populations of a species wintering in the same area Return migration from variable wintering areas Relationship between the internal rhythm and prevailing daylength Relationship between spring arrival, breeding and autumn departure Deferred return to breeding areas Concluding remarks Summary References

vii

234 234 235 235 235 236 236 237 239 241 242 243 243 244 245 246

251 251 253 254 254 255 255 256 257 257 258 259 259 262 263 265 265 267 267 268 268 269 270

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Contents

14. Stopover ecology Breaking the journey Important re-fuelling areas Resuming the journey Change in the diurnal cycle Weather and other factors influencing departure Other findings Age and sex effects Conclusions Summary References

277 278 279 282 286 286 286 287 287 288 289

Part 3 Large-scale movement patterns 15. Seasonal reoccupation of breeding and wintering areas Latitudinal trend in the timing of spring Species differences in spring migration dates Recolonisation patterns Patterns within species Duration of residence Annual variations in spring migration dates Evidence on migration timing from the field Reoccupation of local breeding areas Settlement on territories Components of early migration Withdrawal from breeding areas Competition for winter habitat Winter movements Concluding remarks Summary References

16. Geographical patterns in migration Latitudinal trends Migration and diet Causes of latitudinal trend Distributional shifts Trends within species Altitudinal shifts Ecological niches Comparisons between hemispheres Populations in both hemispheres Relationship between breeding and wintering areas Patterns in distribution

295 296 297 299 301 301 302 302 305 307 309 309 311 311 312 312 312

317 318 321 323 323 323 323 325 325 326 327 327

Comparison of sizes of breeding and wintering areas Migration within the southern continents Africa South America Australasia Concluding remarks Summary References

329 331 331 332 333 334 335 335

17. Variations on a migratory theme

337

Moult migrations Moult migration as originally defined Altitudinal moult migrations Moult at staging sites on autumn migration Movements within the breeding season Movements within the non-breeding season Facultative movements in relation to food supply Facultative movements in relation to weather Overview Opposite-direction migrations Nomadism Desert wetlands Irruptive movements away from deserts Concluding remarks Summary References

18. Sex and age differences in migration Arrival in breeding areas How does one sex achieve an earlier arrival than the other? Age differences in arrival dates Departure from breeding areas Age differences in departure from breeding areas Migratory distance, body size and dominance Age-related differences in migration distances Competition and migration distances Migration and deferred breeding Over-summering in ‘wintering’ areas Other differences between age groups Concluding remarks Summary References

337 338 341 341 342 343 345 346 346 347 347 349 351 351 352 352

355 356 358 359 359 361 363 365 365 367 368 370 371 372 373

19. Dispersal and site fidelity

379

Benefits and costs of site fidelity Natal dispersal

380 381

Contents

Seabirds and other colonial species Sex differences in natal dispersal Competition and natal dispersal Breeding dispersal Dispersal within a breeding season Long-distance natal and breeding dispersal Nonbreeding dispersal Multiple wintering sites Pelagic seabirds Sex-related differences Age-related differences Comparison of breeding and non-breeding site fidelity Fidelity to stopover sites Fidelity to migration routes Post-fledging dispersal Dispersive migration Site attachment Attachment of young birds to natal sites Attachment of young birds to wintering sites Summary References

20. Irruptive migrants: boreal seedeaters Seed crops Irruptive seed-eaters and fruit-eaters Twice-yearly migrants Breeding densities Breeding dispersal Autumn emigration Migration timing Migration directions Winter densities Changes in wintering areas: evidence from ringing Breeding in migration and wintering areas Once-yearly migrants Crossbills Annual cycle Irruptions Change of breeding localities Other Eurasian crossbills North American crossbills Nutcrackers Overview of seed-eaters Coping with boom-and-bust

382 383 384 384 387 388 389 392 392 393 393 393 394 395 395 397 397 397 399 399 400

Regularity in irruptions Directional preferences Other seed-eaters Concluding remarks Summary References

21. Irruptive migrants: owls, hawks and ducks Rodents and rodent-eaters Breeding dispersal Locating areas with abundant food Geographical variation in movement patterns within species Irruptive migrations Changes in wintering areas Nesting outside the regular range Rodents and reproduction Hares and hare-eaters Ducks and ephemeral wetlands Breeding distributions Winter distributions Eurasian ducks Concluding remarks Summary References

ix

429 429 430 430 431 432

437 437 439 445 445 446 446 447 447 447 448 449 450 450 451 452 452

407 408 409 412 412 412 414 417 417 417 418 421 421 421 422 423 425 426 426 427 428 428

Part 4 Evolution of movement patterns 22. Evolution and inheritance of migratory behaviour Adaptations for migration Adaptive timing Partial migration The genetic control of migration: experimental evidence Migratory inclination Timing and distance Migratory directions Morphological features Natural variability A natural change in the migration of Eurasian Blackcaps Heritability and other studies The genes involved Concluding remarks Summary References

459 460 463 463 465 466 467 468 469 469 469 471 471 472 474 474

x

Contents

23. Recent changes in bird migrations Migratory to sedentary Sedentary to migratory Shortening of migrations Lengthening of migrations Changes in migratory directions Changes in migration timing Spring dates Autumn dates Times spent in breeding and wintering areas Ecological mismatches Other climate-driven changes Other rapid changes in behaviour Genetic and facultative responses Genetic responses Facultative responses Summary References

24. Glacial legacies in bird migrations Indirect routes to distant wintering areas Further comments on the legacy of glacial changes Abrupt changes in migration routes Migratory divides Evolution of barrier crossing Topographic influences Loop migrations Migration development towards higher or lower latitudes Evidence from DNA studies Colonization of wintering from breeding areas Development of migration patterns Concluding remarks Summary References

25. Distribution patterns and connectivity Longitudinal patterns Parallel or fan patterns Latitudinal patterns Evolution of alloheimy Nonbreeding distributions among seabirds Connectivity Relationship to population limitation Relationship to genetic divergence Time and energy considerations Summary References

479 483 483 483 484 485 485 486 489 490 490 492 492 493 493 494 495 495

501 501 506 508 508 510 512 513 514 515 516 517 518 519 519

523 523 528 528 531 532 533 535 535 536 539 539

Part 5 Migration systems and population limitation 26. The Palearctic-Afrotropical migration system The birds involved Social systems The African Wintering areas Seasonal changes Wetlands Bird movements within Africa Recent tracking studies Relationships between Eurasian migrants and native African species Habitats Mobility Sahel food supplies Fluctuations and declines in migrant numbers Population fluctuations Population declines Climate and habitat changes in Africa Hunting and predation Natural predation Events in breeding areas Summary References

27. The Nearctic Neotropical migration system The birds and their wintering areas The neotropical wintering areas Migrant social systems Bird movements within the Neotropics Population declines in migrants Causes of declines operating in breeding areas Forest loss and fragmentation Predation Parasitism by cowbirds Food supplies Causes of declines operating in non-breeding areas Factors operating on migration routes Concluding remarks Summary References

547 547 550 550 551 554 554 556 557 558 559 559 559 559 561 564 565 566 566 566 567

573 573 574 575 576 576 579 580 580 581 583 584 585 586 587 587

Contents

28. The East Asian Australasian and other migration systems The EAA migration system The birds Population declines Shorebirds in Australasia Declines in Shorebirds the Yellow Sea problem Other migration systems The Central Asian (Trans-Himalayan) system The Central Pacific migration system Concluding remarks Summary References

29. Population limitation breeding and wintering areas Some general principles Effects of habitat gain or loss on migrants The buffer effect and density dependence Examples of species affected by events in breeding or wintering areas Climatic factors acting in both breeding and wintering areas From winter-limited to summer-limited Convergent and divergent patterns Carry-over effects Other aspects of population limitation in migrants Range size and population limitation Connectivity and population limitation Range segregation and sex ratios Climate change and phenological mismatch Human hunting Pathogens and diseases Concluding remarks Summary References

30. Population limitation migration routes Conceptual models Food limitation at stopover sites Migrant numbers in relation to food supplies

593 594 595 596 596 598 600 600 603 604 604 605

609 610 610 611 612 619 619 620 620 623 623 623 624 624 625 625 626 626 627

633 633 635 635

Depletion of food supplies Food supplies and fattening rates Social interactions, feeding and fuelling rates Poor condition and mortality at stopover sites Influence of weather Influence of predation, disturbance and parasitism Body condition and subsequent performance Effects of stopover events on populations Change of stopover sites Concluding remarks Residual body reserves Winter or spring limitation? Interactions between populations Conservation issues Summary References

31. Mortality on migration Mortality on route Age differences Mortality and migration distance Mass mortality events Weather and in-flight mortality Unseasonable cold before departure from breeding areas Unseasonable cold soon after arrival in breeding areas Conclusions on weather-induced mortality events Human-induced losses Human hunting Illuminated structures Wind turbines Power lines Oil and gas platforms Artificial light General comments Concluding remarks Summary References Glossary Index

xi

635 636 636 637 637 638 641 643 644 645 645 645 646 646 646 647

653 655 658 659 660 660 664 665 666 666 666 666 667 668 668 669 669 669 670 671 677 685

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Preface to the first edition From ancient days the migration of birds has excited the wonder of thoughtful observers. J. A. Thompson (1913)

The phenomenon of bird migration has long fascinated its human observers, who have been continually impressed by the sheer scale and regularity of the movements. It has repeatedly prompted familiar questions about birds, such as where do they go or come from, how do they know where and when to travel and how do they find their way? For more than a century now, bird movements have been subjected to scientific study, and by increasingly sophisticated methodology. In the past 25 years, hardly a year has gone by without the publication of a new book or symposium volume dealing with some aspect of bird migration, and each year dozens of papers have appeared in the scientific journals. In this book, I hope to provide an up-to-date synthesis of much of this information, taking account of both older and newer findings. However, the emphasis throughout is on ecological aspects: on the different types of bird movements, how they relate to food supplies and other external conditions and how they might have evolved. It is mainly in the weight of attention devoted to ecological aspects which have received scant attention in previous reviews that this book differs from earlier ones. It is also in these aspects that, with my own background, I feel most at home with the subject matter. After a brief introduction and survey of methodology, the book is divided into five main sections. The first deals with the journeys themselves: with the constraints and limitations of bird flight, the influence of weather, fuelling needs, migration strategies, travel speeds, the problems of navigation and vagrancy. The second section is concerned with the annual cycles of birds, with how migration relates to breeding and moult, and with the physiological control of these various processes. The third section describes geographical patterns in bird movements across the globe, and the various types of bird movements, such as dispersal, irruption and nomadism, emphasizing the ecological factors that underpin them. The fourth section is concerned with the evolution of migration and other movement patterns of birds, with the role of glacial history in influencing current movement patterns, and with recent changes in migration related to climate change and other human influence. The fifth section discusses how the population ecology of migratory birds differs from that of sedentary ones, and the influence of migration events on the population levels of migratory birds. In particular, it considers the extent to which migratory bird numbers are limited by conditions in breeding, migration or wintering areas. This section is followed by a glossary, references and index. Although the book is intended mainly for research students, I have tried to write simply, in the hope that the text will appeal to anyone with an interest in this fascinating subject, including the many bird-watchers and -ringers who have contributed so much over the years to its development. To keep the book within bounds, I could not mention all recent work on bird migration and have sought to cite examples, rather than every study. Nevertheless, the reference list (up to and including 2006) relates to more than 2500 scientific papers and more than 50 books. It is inevitable in a book of this type that some topics recur in different chapters, as they are relevant to more than one aspect of the subject, but I have tried to reduce this repetition to a minimum and cross-refer between chapters. Nevertheless, each chapter is intended as a stand-alone read. So much of the book is concerned with geography that, while I have tried to provide some helpful maps in the text, some parts would be better read with an atlas, or preferably a globe, close at hand. For permission to reproduce diagrams and other material from scientific journals, I thank the various publishers, authors, ornithological societies and individuals involved, and for providing electronic copies of particular diagrams, I thank John Croxall, Thord Fransson, Mark Fuller, Sidney Gauthreaux, Yossi Leshem and Richard Phillips. I owe a great deal to many colleagues in the field who have discussed various aspects of the subject with me over the years and to several friends for helpful comments on particular chapters, namely Bill Bourne (Chapter 4), Bill Clarke (Chapter 7), Alistair Dawson (Chapters 11 and 12), Barbara Helm (Chapters 11, 12, 20 and the Glossary),

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Preface to the first edition

Lukas Jenni (Chapters 5 and 6), Peter Jones (Chapters 22, 24 and 25), Mick Marquiss (Chapters 15 and 18) and Tim Sparks (Chapter 21). Other colleagues, in their capacity as referees, commented helpfully on certain papers which preceded the book. I owe a particular debt to David Jenkins, who read the whole book in draft (some parts more than once), and offered many constructive suggestions for improvement. Finally, my wife, Halina, for supporting me through the writing process and commented helpfully on the penultimate draft. Ian Newton

Preface to the second edition The amount of research published on bird migration has expanded greatly since the first edition of this book was published in 2008, much of it driven by developments in tracking technology. Owing to constraints on space, I could only include new material in this second edition by deleting a similar amount from the first edition. I have done this mainly by condensing much of the earlier text, and by deleting or reducing some of the Tables and Figures. I have also deleted the chapter on Vagrancy given in the first edition, incorporating parts of it elsewhere in this second edition. As far as I know, the deleted material was not ‘incorrect’ in any way, so hopefully the first edition will retain some value despite the appearance of this successor volume. The first edition is referred to here as ‘Newton 2008’. All the chapters in this second edition have been altered in some respects from the original and all have had new material incorporated. Three new chapters have been added, namely on Seabird movements, Stopover ecology and The East Asian–Australasian and other migration systems, respectively, while the greatly expanded material on bird navigation has been presented as two chapters instead of one. In addition to changes made to some of the original Figures and Tables, 27 new Figures and 14 new Tables have been added. Despite the deletion of many older references, the current list cites more than 3000 scientific papers and books, nearly one-third of which were published since the first edition went to press in 2006. Scientific names of birds are given in each chapter at the first mention only, but also in tables, maps and diagrams. I am indebted to all the colleagues who commented helpfully on chapters in the original volume, and in the present volume also to Keith Bildstein and Alan Hinde (Chapter 7), Mike Harris and Sarah Wanless (Chapter 8), Barbara Helm ˚ ke Lindstro¨m (Chapter 14), Christian Rutz (Chapters 2, 3, 24 and 25), Tim Sparks (Chapters 10, 11, 13 and 14), A (Chapter 23), Iain Tayler (Chapter 28) and Leo Zwarts (Chapter 26). My heartfelt thanks also go to Leo Zwartz for stepping in at a late stage and drawing many of the new maps and diagrams, and helping in other ways. Mirembe Newton also helped in the checking of references. As with the first edition, David Jenkins commented helpfully on the whole book in draft. Finally, I am again indebted to my wife, Halina, for her support through the writing process and for casting a critical eye over the penultimate draft.

Ian Newton

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Chapter 1

Introduction

Common Cranes (Grus grus) on migration That strange and mysterious phenomenon in the life of birds, their migratory journeys, repeated at fixed intervals, and with unerring exactness, has for thousands of years called forth the astonishment and admiration of mankind. Heinrich Ga¨tke, 1895.

The most obvious feature of birds is that they can fly. Many travel quickly and economically over long distances up to thousands of kilometres if necessary crossing seas, deserts and mountain ranges. They also have great navigational skills and are able to remember and locate distant places previously visited. Birds can thereby occupy widely separated places at different times of year, returning annually to the same localities, and adopting an itinerant lifestyle of a kind closed to less mobile creatures. Although migration occurs in other animal groups, including insects, fish, turtles and mammals, in none is it so widely and well developed as in birds. Their collective travel routes span almost the entire globe, and consequently their distributions are continually changing. Movements are most marked in spring and autumn but can occur every month in one region or another, raising questions about the underlying ecological factors that do not arise with more sedentary organisms. A major advantage of flight is its speed. Flight requires more energy per unit time than walking, running or swimming but, because of the greater distance covered, it is the cheapest mode of transport overall. One type of flight, by soaring-gliding, is cheaper still but is practiced mainly by larger species such as albatrosses, which can travel the oceans on little more energy than sitting still (Chapter 3). Nevertheless, while most birds migrate by flying, penguins and some other seabirds migrate by swimming and some landbirds by walking for part or all of their journeys. Most birds are of a size that enables them to become airborne. They have lightweight skeletons and plumage and wing shapes that ensure efficient flight. Their wings are powered by massive breast muscles, the pectoralis and supracoracoideus, which are responsible for downward and upward strokes, respectively. The two pectoralis muscles, one on The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00031-2 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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The Migration Ecology of Birds

each side of the breast, are by far the largest muscles in the body of flying birds, forming more than one-third of the total body mass of some species. These muscles are well supplied with blood vessels and consist of fast-contracting fibres (red fibres), which in many species can beat the wings continuously for days on end. In some species of swifts, the adults remain continuously on the wing for the whole 9 months between breeding seasons, whereas the juveniles remain on the wing all the time between leaving their natal nests and making nests of their own 2 or 3 years later. Compared with other animals, birds are not only homoeothermic (warm-blooded) but also have exceptionally efficient respiratory, cardiovascular and metabolic systems. Together, these systems ensure that the specialized wing muscles are kept well supplied with oxygen and energy-rich fuel and that waste products are swiftly removed, preventing the muscle pain and fatigue familiar to human athletes. The breathing mechanism of birds also results in much more efficient gas exchange than in mammals. A bird’s lungs connect by an array of tubes to a system of thin-walled air sacs. The lungs themselves do not inflate and deflate but receive a continuous supply of air flowing from the air sacs through the lungs to the outside. This system, with its unidirectional flow of air, increases the efficiency of oxygen extraction, and the specialized haemoglobin of birds has an unusually high oxygen affinity. Birds have the same senses as we do (sight, hearing, smell, taste and touch), although some of these senses are more acute or better developed than ours. They also have at least one additional sense that we lack, namely an ability to detect and read the earth’s magnetic field, a sense especially important in navigating over long distances (Chapter 10). With these various traits, birds are pre-adapted for the development of long-range movement patterns, enabling some species of birds to perform some of the most remarkable journeys in the animal world.

TYPES OF BIRD MOVEMENTS The terms ‘resident’ and ‘sedentary’ are usually applied to birds that occupy the same areas year-round and to populations that make no obvious large-scale movements that result in seasonal changes in distribution. For convenience in this book, I shall divide bird movements into six main types: G

G

G

G

First, there are the everyday movements centred on the place of residence, which occur in all birds, whether classed as resident or migratory. Typically, they include the flights from nesting or roosting places to feeding sites, or from one feeding site to another, and can occur in any direction. In most landbirds these movements are short and localized, extending over distances of metres or kilometres. But in other species (notably pelagic birds) regular foraging movements can extend over hundreds (sometimes thousands) of kilometres from the nesting colony. Second, there are dispersal movements. In both sedentary and migratory bird species, after becoming independent of their parents, the young usually disperse away from their natal sites. At the population level, dispersal movements seem to occur randomly in any direction and over distances that can be measured, according to species, in metres, kilometres or tens of kilometres, although in a few species (notably pelagic birds), such distances can be much greater (Chapter 19). Post-fledging dispersal of this type is not known to involve a return journey (see below), but in any case most surviving young subsequently settle to breed at some distance from their hatch sites (called natal dispersal). In addition, some adults may change their nesting locations from year to year (breeding dispersal), or their non-breeding locations from year to year (here called non-breeding or wintering dispersal). Third, there is migration, in which individuals make regular return movements, at about the same times each year, usually in specific directions and often to specific destinations. Compared with dispersal movements, migration usually involves a longer journey over tens, hundreds or thousands of kilometres and in much more restricted and fixed directions. Most birds spend the non-breeding period at lower latitudes than their breeding period. Such migration occurs primarily in association with seasonal changes in food availability, resulting from the alternation of warm and cold seasons at high latitudes, or of wet and dry seasons in the tropics. Overall, directional migration causes a massive movement of birds twice each year between regular breeding and wintering ranges, and a general shift of populations from higher to lower latitudes for the non-breeding season. Fourth, there is another category of migration, which I have called dispersive migration, in which post-breeding movements can occur in any direction from the breeding site (like dispersal), but still involve a return journey (like other migration). Although these movements occur seasonally between breeding and non-breeding areas, they do not necessarily involve any change in the latitudinal distribution of the population or any change in its centre of gravity. Such movements are evident in some landbird species usually regarded as ‘resident’ and include altitudinal movements in which montane birds shift in various directions from higher to lower ground for the non-breeding season (Chapter 17). In addition, many seabirds can disperse long distances in various directions from their nesting colonies to over-winter in distant sea areas rich in food, returning to the colonies the following spring.

Introduction Chapter | 1

G

G

3

Fifth, there are irruptions (or invasion migrations), in which the proportions of birds that leave the breeding range, and the distances they travel, vary greatly from year to year (the directions are roughly the same but often more individually variable than in regular migration). Such movements are usually towards lower latitudes and occur in association with annual, as well as with seasonal, fluctuations in food supplies. In consequence, populations may concentrate in different parts of their non-breeding ranges in different years. Irruptions are found commonly among boreal seedeaters which depend on fluctuating tree-seed crops, and in some northern predators which depend on fluctuating rodent populations (Chapters 20 and 21). Sixth, there is nomadism, in which birds move from one area to another, residing for a time wherever conditions are temporarily suitable, and breeding if possible. The areas successively occupied may lie in various directions from one another. No one area is necessarily used every year, and some areas may be used only at intervals of several years, but for months or years at a time, whenever conditions permit. This kind of movement occurs among some rodent-eating owls and raptors of tundra, boreal and arid regions, and among many birds that live in desert regions, where infrequent and sporadic rainfall leads to local changes in habitats and food supplies (Chapter 17). Because these changes are unpredictable from year to year, individual birds do not necessarily return to areas they have used previously and may breed in widely separated areas in different years.

These are the main types of movements, but others also have been recognized. At the time when young birds disperse away from their natal territories, the adults of some species may also move away from nesting areas to better feeding areas (eg, many waders move from inland to seacoasts at this time). Some authors have treated these movements as a separate category (Noskov & Rymkevich, 2008). They lead to a redistribution of birds after breeding but normally occur within the breeding range. It is a time when many species moult and prepare for their subsequent migrations (Chapter 19). Some birds, mainly waterfowl, become flightless at this time, as they replace all the large wing feathers simultaneously. Many travel beforehand on a ‘moult migration’ to special places which offer for the duration abundant food and relative security from predation (Chapter 17). There are also so-called ‘escape (or fugitive) movements when birds have suddenly to abandon their homes because of some unpredicted physical event that removes habitat or food, such as fire, flood or heavy snow, the latter giving rise to ‘hard weather movements’ from which birds return as conditions improve (Chapter 17). Finally, for various reasons, birds occasionally turn up at places well outside their normal range. Such vagrancy is for some birdwatchers the most exciting type of bird movement, as provides rarities to add to cherished life lists. These different main types of bird movements intergrade, and all have variants, but in any bird population, one or two kinds usually prevail. Almost all bird species show post-fledging and other dispersal movements in addition to any other types of movement they might show, and some species show both nomadic and irruptive movements (Chapters 20, 21). Through migration, irruption and nomadism, birds exploit the resources of mainly different regions at different times. The birds thereby achieve greater survival and reproductive success (and hence greater numbers) than if they remained permanently in the same place and adopted a sedentary (resident) lifestyle. The main variables in these different types of bird movements include (1) the directions or spread of directions; (2) the distances or spread of distances; (3) the calendar dates or spread of dates; and (4) whether or not they involve a return journey. They also differ in whether they occur in direct response to prevailing conditions, or in anticipation of conditions that can be expected to occur in the coming weeks. Anticipatory movements lead birds to leave breeding areas before their survival there would be compromised and to arrive back as conditions again predictably become suitable for breeding. These are all aspects of large-scale bird movements which can be independently influenced by natural selection (Chapter 22), giving overall the great diversity of movement patterns found among birds, related to the different conditions and circumstances in which they live. This book is concerned with all these types of bird movements, but the emphasis is on the seasonal return movements of migration and irruption, which are by far the most spectacular and extreme. Migration itself varies greatly between species, as well as between populations, sex and age groups, in terms of distances travelled, routes taken, timing of journeys and behaviour on route. But it is often useful to distinguish between ‘short-distance’ migrants that make mostly overland journeys within continents and ‘long-distance’ migrants that make longer journeys between continents, often involving substantial sea crossings. Similarly, in terms of timing, some birds can complete their migrations in less than a day each way, while others may take more than 3 months each way and may therefore be on the move for more than half of each year most of the time they are not breeding.

Constraints of breeding In theory, some birds might benefit from remaining on the move at all times of the year, for they could then take advantage of rich food supplies wherever and whenever they occurred. It is mainly the needs of breeding that tie birds to

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fixed localities for part of each year because individuals need to remain at their nests or visit their nests frequently to feed their young. However, in some species, notably some seabirds, one parent can be away for long periods (often days, sometimes weeks at a time), whereas the other remains at the nest. This enables parents to collect food up to hundreds or even thousands of kilometres away from their nesting places, changing their foraging areas from time to time (Chapter 8). As their chick grows, it becomes able to survive on its own for long periods, enabling both parents to be away foraging at the same time. Some of the foraging flights of breeding albatrosses can cover thousands of kilometres (Chapter 8), distances far greater than the total annual migrations of many landbirds. In many bird species, individuals do not breed until they are two or more years old. The immature, non-breeders of such species are not tied to particular localities in the same way as breeders and are free to feed away from nesting areas throughout the year. In the breeding season, it is not unusual in these species for immatures to concentrate in different places from the breeding adults or to move around more, and in some such species the young remain in ‘winter quarters’ year-round, returning to nesting areas only when they are approaching breeding age. This holds for many kinds of seabirds, shorebirds, large raptors and others (Chapter 18).

ADAPTATIONS FOR MIGRATION There is no reason to suppose that migratory birds possess adaptations that non-migrants lack, but migrants have certain features better developed than do non-migrants, because of differences in the balance of selection pressures that act upon them. One of the most crucial adaptations concerns navigation specifically, how birds find their way over long distances. Not only can adult birds migrate back and forth between regular breeding and wintering areas but young birds migrating alone also can find their own way to the usual wintering areas for their species, and back to their natal areas the following spring. In finding their way, research has confirmed that birds use at least two main types of reference systems, based on geomagnetic and celestial cues (sun, stars and skylight polarization patterns) respectively. Birds may also remember routes from year to year and follow them visually and seem also able to follow consistent gradients in odours over the earth’s surface in migrating at least to familiar places. These various external cues are of course of little value to a migratory bird unless it ‘knows’ beforehand either by inheritance or experience where it needs to go. The mechanisms of bird orientation and navigation are discussed in Chapters 10 and 11. The timing of bird migration is equally remarkable. Many long-distance bird migrants arrive at their nesting or wintering places every year at around the same date. This implies the existence in birds of precise timing mechanisms that respond to external stimuli by triggering migration at about the same dates each year and maintaining it for long enough for the birds to cover the distances required. Such mechanisms ensure that individuals arrive in their nesting areas as conditions become suitable for breeding and leave before conditions deteriorate and affect survival. The relatively small variations in timing that occur from year to year are mainly associated with variations in prevailing weather or food (Chapter 15). A third adaptation that facilitates seasonal migration is the ability of birds at appropriate times of year to accumulate large body reserves (mostly fat) to fuel the flights (Chapter 5). Some small birds that cross large areas of sea or desert in which they cannot feed are able to double their usual weight beforehand through fuel deposition, and some species also reduce the mass of other body organs not directly concerned with migration, thus reducing the overall energy needs of the journey. The seasonal changes in body composition that occur in migratory birds are some of the most extreme in the animal world. Birds are also unusual in the speed and efficiency with which they can convert the fatty acids in fuel reserves to the energy needed to power their wings. Most migration consists of periods of flight when fuel is burned, interspersed by ‘stopovers’ when birds replenish their body reserves to enable them to continue their journeys (Chapter 14). The migratory lifestyle also requires that periods of movement are integrated with other events in the annual cycle, especially breeding or moult. In most bird species, these events normally occur at different times of the year. Because the breeding cycle requires that birds remain within restricted localities, it is obvious that individuals cannot breed and migrate at the same time. And because feather replacement can temporarily reduce flight efficiency, it is also not surprising that moult and migration are separated as much as possible. Studies of the annual cycles of birds, and the physiological control of migration within these cycles, are discussed in Chapters 12 and 13. An interesting aspect of bird migration concerns the extent to which individuals are inherently programmed to do the right things at the right times of year. It is not just a case of breeding and moulting at appropriate times which is important in all birds. Without innate programming, a migrant would have little sense of when to migrate, in which direction to fly or for how long. Nor would it know when on its journey to do specific things, such as change direction

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or accumulate extra body reserves in preparation for a long sea crossing. All these aspects require an endogenous schedule which promotes particular physiology and behaviour at appropriate seasons or stages in a journey. This inherent aspect of bird movements adds an additional fascination to study of the controlling mechanisms (Chapters 12 and 13). Yet despite being partly under genetic control, migration patterns among birds show some flexibility and facility for rapid change (Chapter 23). Many bird families contain both migratory and non-migratory populations, indicating little phylogenetic constraint on the development of migratory behaviour. Within species, changes in migratory patterns are presumed to have occurred repeatedly through the Pleistocene glacial cycles and, more strikingly, even in recent decades, as particular populations have become more sedentary, or shortened their migrations, in apparent response to climate warming (Chapter 23). Further understanding of the evolution of migration systems can be inferred from present distribution and movement patterns, as well as from cross-breeding experiments, palaeo-historical and molecular evidence (Chapters 24 and 25). To accommodate a long-distance migratory lifestyle, participants must be able to live in two or more different parts of the world, often on different continents. They must often occupy somewhat different habitats and climatic regimes and deal with different foods, competitors, predators and pathogens, as they occupy distinct niches in their summer and winter homes. Such split lives have consequences that a sedentary lifestyle does not. Unlike resident birds, whose numbers depend on conditions in the single area where they happen to live, the numbers of migrants can be influenced by conditions spread over one or two continents, wherever they breed, stop on migration and spend the winter. Ever at the mercy of human activities, migrants live in multiple jeopardy. It is perhaps not surprising, therefore, that over recent decades of increasing human impact, more migrants than residents have shown marked population declines. Such trends are apparent in both Eurasia and North America, and the factors that limit the population sizes of migrants are discussed in Chapters 26 28.

THE DIVERSITY OF MIGRATION Migration occurs to some degree in most bird species that live in seasonal environments, varying from arctic tundras to tropical savannahs and grasslands. It is in strongly seasonal environments that food supplies vary most markedly through the year, fluctuating between abundance and scarcity in each 12-month period, as driven by seasonal cycles in temperature at higher latitudes or rainfall at lower latitudes. Birds generally time their migrations to be in their breeding areas when food is abundant and absent when it is scarce. Only in the relatively stable conditions of tropical lowland rainforest, where food supplies remain fairly constant year-round, do most of the bird species that breed there remain year-round. Nonetheless, even these forest areas receive a seasonal influx of wintering migrants from higher latitudes. Worldwide, in response to seasonal changes in food supplies, more than 50 billion birds are thought to migrate every year on return journeys between different areas (Berthold, 1993). More than a fourth of all bird species are thought to participate in these movements, but this is probably an underestimate because many species have not been studied in sufficient detail to detect migration if it were to occur, especially in some tropical regions. Almost all migratory landbirds travel to milder climes for the non-breeding period, moving broadly on a northsouth axis. However, many populations also have an easterly or westerly component in their movements, especially those that breed in the central parts of the northern landmasses and move to the warmer edges for winter. A few bird species move almost directly east west. Extreme examples include the Common Pochards (Aythya ferina) which breed in Russia and move up to 4000 km in autumn to winter in Western Europe, in the process crossing up to 80 degrees of longitude (Wernham et al., 2002). Many species in southern Africa breed in the wettest season in the arid west in summer and migrate to the east to winter in the wettest season there. In these regions, it is largely rainfall that influences food supplies. Small numbers of birds, for special reasons, migrate in the opposite direction to most other species, breeding in winter and travelling to higher (rather than lower latitudes) for their non-breeding period (Chapter 16). Juvenile Bald Eagles (Haliaeetus leucocephalus) in southern North America provide an example.

Difficult journeys Bird migrations may thus vary from a few tens to many thousands of kilometres, but it is the long and difficult journeys that best reveal the capabilities of avian migrants. Among landbirds, spectacularly long journeys are made by those species that fly regularly between northern Eurasia and southern Africa or Australasia, or between northern North America and southern South America or Australasia (Figure 1.1). The major advantage of migrating so far between the northern and southern hemispheres derives from the reversal of seasons. The species involved pass both breeding and

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The Migration Ecology of Birds

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FIGURE 1.1 Some long-distance migrations of birds. 1. Alaskan population of Pacific Golden-Plover (Pluvialis fulva); 2. Arctic Tern (Sterna paradisaea); 3. Swainson’s Hawk (Buteo swainsoni); 4. Snow Goose (Anser caerulescens); 5. Many North American breeding species that cross the Gulf of Mexico; 6. Ruff (Calidris pugnax); 7. Many European breeding species that cross the Mediterranean Sea and Sahara Desert; 8. Wheatear (Oenanthe oenanthe); 9. Amur Falcon (Falco amurensis); 10. Arctic Warbler (Phylloscopus borealis); 11. Short-tailed Shearwater (Puffinus tenuirostris). Partly after Berthold (1993).

non-breeding seasons in summer conditions when food is plentiful, although no such birds are known to breed regularly at both ends of their migration route (Chapter 12). Many landbirds that migrate overland have abundant places to stop and feed. They can therefore migrate, rest and feed almost everyday, accomplishing their journeys by a series of short flights. Other birds cross large hostile areas, where they cannot stop and feed. They have to accumulate larger body reserves and make long flights between widely spaced stopping places (Chapter 5). For example, shorebirds typically complete long journeys in 2 4 long stages, refuelling before each stage, and often travelling 1000 5000 km between suitable estuaries, even when mainly following coastlines. The flights themselves comprise long periods of muscular work without food or water, often at great heights over inhospitable terrain, and the rare refuelling sites are crucial to successful journeys (Chapter 14). Landbirds that migrate over oceans provide some of the most extreme examples of endurance flight and precise navigation. They travel without opportunity to feed, drink or rest, over vast stretches of open water devoid of helpful landmarks. They cannot stop, as birds do overland, if the weather turns against them. Yet millions of landbirds regularly cross the Mediterranean Sea and the Gulf of Mexico at their widest points (about 1200 km), and smaller numbers regularly cross longer stretches, such as the western Atlantic between northeastern North America and northeastern South America (2400 3700 km), or the northern Pacific between Alaska and Hawaii and other central Pacific Islands (5000 km). However, the most impressive of all overwater migrations by a landbird is undertaken by Bar-tailed Godwits (Limosa lapponica) from Alaska, which in autumn accomplish an astonishing 175-hour non-stop 10,400 km flight to New Zealand (Chapter 6). Many seabirds perform exceptionally long migrations, but these are perhaps less demanding than the transoceanic flights of landbirds. This is partly because most seabirds are larger and more robust than the majority of landbirds, partly because they travel largely by gliding flight and can make greater use of winds which are generally stronger over most sea than land areas, but also because many species can rest on the sea surface or feed on route. In moving between the Arctic and Antarctic regions, Arctic Terns (Sterna paradisaea) perform the longest known migrations of any bird, entailing round trips of more than 60,000 km each year (Chapter 8).

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Some Antarctic seabirds, mainly various albatrosses, perform circumpolar migrations, riding the winds eastward around the world in the Southern Ocean. Satellite-based tracking results from albatrosses have revealed the extraordinary distances travelled in short time periods. For example, a Northern Royal Albatross (Diomedia sanfordi) flew up to 1800 km in 24 hours, and a Grey-headed Albatross (Thalassarche chrysostoma) circled the globe, covering 22,000 km in just 46 days (Croxall et al., 2005).

SEDENTARY POPULATIONS At the opposite end of the spectrum from migratory populations are sedentary (or resident) ones. A sedentary bird population can be defined as one whose distribution and centre of gravity remain more or less the same year-round, and from year to year. Individuals of sedentary populations typically show no directional bias in their movements at any time of year (unless imposed by local topography) and generally move over much shorter distances than migrants. In Britain, as elsewhere, large numbers of many resident bird species have been ringed as chicks and adults, and the subsequent recoveries of birds found dead and reported by members of the public sometimes years later have given some idea of their overall movement patterns. Typically, most birds of non-migratory species were found near where they were ringed, in all directions, but with progressively fewer at increasing distances. In many resident songbirds, the median distance moved between ringing and recovery was less than 1 km, but some individuals had reached more than 20 km. All these birds are likely to have made their longest movements in the immediate post-fledging period, as they became free of parental care.

HIBERNATION While many birds alleviate seasonal food shortages by migrating elsewhere, many other animals cope with seasonally difficult periods by hibernating for up to several months at a time. They survive at much reduced metabolic rate on body reserves and emerge when conditions improve. At one time, the disappearance of most birds from high latitudes for the winter was attributed to hibernation rather than migration. In fact, at least one species of bird does hibernate in winter. This was discovered in 1946 when a Common Poorwill (Phalaenoptilus nuttallii) (a sort of nightjar) was found in a torpid state in a rock crevice in a California desert (Jaeger, 1949). The bird was inert, its respiration and heart rate were barely detectable, and its body temperature was 18 C 20 C, about half the usual level for birds. The individual was ringed, and in subsequent winters it was found hibernating again in the same crevice. Since then other Poorwills have been found in similar sites in the same condition, and their physiology has been studied in laboratories. Other kinds of birds can also become torpid but remain so only overnight (hummingbirds) or for at most a few days at a time (swifts and colies). Evidently, long-term hibernation is at best extremely rare among birds, most avoiding difficult seasons by migration instead.

SUMMARY The large-scale movements of birds can conveniently be divided into dispersal, dispersive migration, migration, irruption and nomadism, although these different types of movements intergrade with one another, and the same populations may show more than one type. This book is concerned with all these types of movements, but chiefly with migration, defined as a seasonal return movement in fixed directions between separate breeding and wintering ranges. Migration occurs to some degree in most species of birds that live in seasonal environments, where food supplies change from abundant to scarce during the course of each year. It leads to massive twice-yearly changes in the distributions of birds over the earth’s surface. Birds in general are pre-adapted for migration by their powers of flight, and their associated adaptations, such as their lightweight skeletons and plumage, their efficient respiratory, circulation and metabolic systems, and their acute senses, including an ability to read the earth’s magnetic field. Navigation on migration is also achieved by reference to celestial cues (sun, stars, polarization patterns), and in some species also olfactory cues. In most birds, the main events of breeding, moult and migration occur in non-overlapping sequence throughout the year and are controlled largely by internal timing mechanisms. Some migratory birds travel relatively short distances of a few tens of kilometres between their breeding and wintering areas, but others travel hundreds or thousands of kilometres, sometimes crossing long stretches of sea or another inhospitable habitat, where they cannot rest or feed. They accumulate large body reserves in preparation for the journey. Such birds show impressive navigational skills which enable individuals to return to the same breeding and wintering

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sites year after year. Migration occurs broadly on a north south axis, but many species have a strong east west component in their journeys. Because migrants live in more than one area, they encounter a bigger range of food organisms, competitors, predators and pathogens than sedentary populations. Their numbers can be limited by conditions encountered in breeding, migration or wintering areas, adding additional threats to their lives. Individuals in sedentary populations mostly move over short distances of at most a few tens of kilometres and show no directional preferences, so that the population occupies essentially the same range year-round. Only one bird species (the Common Poorwill) is known to hibernate through the unfavourable season.

REFERENCES Berthold, P. (1993). Bird migration. A general survey. Oxford, Oxford University Press. Croxall, J. P., Silk, J. R. D., Phillips, R. A., Afanasyev, V. & Briggs, D. R. (2005). Global circumnavigations: tracking year-round ranges of nonbreeding albatrosses. Science 307: 249 50. Ga¨tke, H. (1895). Heligoland as an ornithological observatory. The result of fifty years experience. Edinburgh, David Douglas.

Jaeger, E. C. (1949). Further observations on the hibernation of the Poorwill. Condor 51: 105 9. Noskov, G. A. & Rymkevich, T. A. (2008). The migratory activity in the annual cycle of birds and its forms. Zool. Zh. 87: 446 57. Wernham, C. V., Toms, M. P., Marchant, J. H., Clark, J. A., Siriwardena, G. M. & Baillie, S. R. (2002). The migration atlas: movements of the birds of Britain and Ireland. London, T. & A. D. Poyser.

Chapter 2

Methodology for migration studies

Ringing a Curlew Sandpiper (Calidris ferruginea). The study of living birds by the banding method, whereby great numbers of individuals are marked with numbered aluminum leg rings, has come to be recognised as a most accurate means of ornithological research. Frederick C. Lincoln, 1935.

An early indication that birds could travel long distances was provided by a White Stork (Ciconia ciconia) which was seen in Germany in 1822 flying around with a spear stuck through its body. When the bird was shot it was found that the spear could be attributed to a region of West Africa. This provided the first firm indication from Europe of a long-distance movement by an individual bird, and since then other storks have been recovered in similar circumstances. In more recent times, bird migrations have been studied by observations (made directly or with radar), by widespread surveys of bird distributions at different seasons, by use of ring recoveries, or in recent years by the use of tracking devices fixed to individual birds which can then be followed on their journeys. Studies of captive birds have provided further information. In this chapter, different study techniques are described, highlighting their pros and cons.

OBSERVATIONS OF BIRDS ON MIGRATION As is obvious to any ornithologist, at particular localities, some bird species appear only in the breeding season, and others in the non-breeding season or at times when they pass through on migration. Watching birds on migration is a favourite pastime for thousands of bird watchers, and in many countries, the concentration points (such as coastal promontories, offshore islands and mountain passes) are now well known. Hawk Mountain in Pennsylvania, which is famous as a viewing site for raptor migration, attracts about 20,000 raptors each autumn, but more than 100,000 human observers. The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00002-6 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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For most bird species, counts of individuals seen on the ground or flying over represent only a small proportion of those passing through. Most migrating birds fly too high to be seen, and in any case many species migrate at night. Migrants come to ground mainly to rest or refuel, or after they have been drifted off course by side winds or forced down by headwinds, mist or rain. Hence, visual counts of migrants cannot usually reflect the true volume of migration or the weather conditions that most favour it (Kerlinger, 1989). On the other hand, any birds seen can usually be identified to species by their appearance or calls. Only for some raptors and other soaring birds, which fly by day lower than most other birds, can ground counts reflect the actual numbers passing. Similar problems hold for most seabirds even though they generally fly low over the waves. Watching migrating seabirds is often done from headlands and counts are highest when strong winds blow the birds close to shore. Normally migrants would be too far out to be counted in this way. Also, some seabird species forage at long distances from their nests, so it is at times impossible to distinguish migration from feeding flights in species in which migration and breeding dates overlap. As for nocturnal migration, low-flying birds can be seen against the lit surface of the moon (moon-watching). This method can only be used near full moon in clear skies and covers only a tiny part of the night sky. But by adventurous calculations involving the moon’s bearing and elevation, counts of birds crossing the face of the moon can be transformed into estimates of the numbers passing over, their direction of movement and even their height and speed (Nisbet, 1959). Using a telescope with 40 3 magnification, an estimated 50% of the birds flying at 1.5 km from the observer were detected, reducing to zero at 3.5 km, based on comparison with radar and infrared observations (Liechti et al., 1995). Other nocturnal observers have used a strong spotlight directed skywards to count the birds passing through the beam. The best device for this purpose is a ceilometer, normally used at airports for measuring cloud height. In warm weather, the lower part of the beam often fills with insects, but birds can be seen flying through the upper part, although the beam typically extends only to a few hundred metres. The light might also attract birds to the beam, biasing results on the numbers passing. In addition, night vision devices and thermal infrared imaging cameras (detecting body heat) can be used to detect birds flying above. By pointing a thermal imaging device of 1.45 degrees opening angle to the sky, migrating birds can be detected from 300 up to 3000 m (Zehnder et al., 2001). Infrared sensors work best at night under clear skies, so are not good for assessing weather effects on migration. Other evidence of nocturnal migration can be obtained by listening for the calls of birds as they pass invisibly overhead. The unaided human ear cannot pick up the normal flight calls of birds beyond about 400 m, but the use of a parabolic reflector and amplifier can extend the range up to 3000 m or more. Some species call more often or more loudly than others, or more in mist than clear skies, so the numbers of calls heard are only broadly related to the number of birds aloft (Farnsworth et al., 2004). Nevertheless, the opportunity that listening affords for identifying species makes it a useful accessory to other methods. Automated audio-recording devices are now available, along with software trained to identify particular species (van Doren et al., 2023). An early indication of the numbers and species of birds migrating at night was provided by lethal collisions of lowflying birds attracted to lighthouses and other illuminated structures (Chapter 31; Ga¨tke, 1895; Clarke, 1912). Extraordinary numbers have sometimes been recorded, such as the 50,000 birds of 53 species killed on one night at one site in Georgia (Johnston & Haines, 1957). Some species, such as Common Snipe (Gallingo gallingo), Water Rail (Rallus aquaticus) and Common Grasshopper Warbler (Locustella naevia) in Europe, seem notoriously prone to such accidents. Mortality occurs mainly on overcast or foggy nights, and the resulting corpses have provided information on the migration seasons, body weights and condition of the species involved.

RADAR STUDIES The use of radar to measure bird migration began in the 1950s. A radar emits short pulses of radio waves and their echoes from targets, whether birds, bats, large insects or airplanes. Because radio waves travel through the atmosphere at close to the constant speed of light, the distance between the radar and the target can be calculated from the time lapse between pulse emission and echo reception. The use of radar revolutionized the study of bird migration because it made observations almost independent of flight altitudes and weather, totally independent of light conditions, and hence fully comparable by day and night. It has taught us much about unseen migration and the influence of weather on bird movements (Chapter 4). It has provided reliable information on the seasonal and diurnal timing of migration, and on the speeds, directions and altitudes of flight (for reviews, see Bruderer, 1997a,b). Radar also swiftly disposed of the idea that migration occurred only in spring and autumn. Birds of one species or another could be seen migrating somewhere on Earth at almost any time of year. However, care is needed in some regions to separate birds from large insects, and

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to estimate reliably the number of bird echoes in the radar beam (for discussion of procedures, see Schmaljohann et al., 2008). Birds can be followed by radar over distances long enough to reveal their reactions to different atmospheric conditions. The numbers of echoes on most radar screens cannot be precisely related to the numbers of birds flying over (because several birds flying close together may appear as a single echo), but the echoes provide relative measures of abundance whether by day or night. Depending on the design, radar can be used to study bird migration over a wide range of spatial scales, and different types of radar are suited to addressing different questions. The most obvious disadvantage of radar is the cost of the equipment and of the trained personnel to maintain and operate it. However, ornithologists have often gained access to radar that exists for other purposes, such as monitoring aircraft or weather patterns. These radars are usually available only at a limited number of fixed installations. The main operational drawback is that birds cannot normally be identified to species, only to broad categories separated by body size, flight speed or wing-beat patterns. The radar echoes often show rhythmic fluctuations that can be used to estimate wing-beat frequency. This procedure enables waders and waterfowl (continuous wing-beats) to be distinguished from passerines (wing-beats broken by pauses), with perhaps two size classes for each group. However, birds flying close to the ground below the radar horizon are usually missed, while some other low-flying birds may be blurred by backscatter from ground objects. Surveillance radars, like those used for traffic control at airports, have a fan-beam of wide vertical angle (10 30 degrees) and narrow horizontal angle (up to 2 degrees). By rotating the radar antenna, a wide swathe of sky can be scanned for echoes with a high horizontal resolution, but no altitude resolution. Spanning an area of more than 100 km across, surveillance radars are good for studies of migration intensity, speed and general direction. On some modern radars, small songbirds can be detected beyond 100 km, and larger birds to more than 500 km, providing they are flying high enough (Bruderer, 1999). With most radars, the displays can be easily recorded on film for subsequent playback and analysis. A useful way of recording the slow-moving echoes of birds is with time-lapse photography, the radar screen with a clock beside it being photographed with a cine camera every 1 2 minutes. Projected at normal speed, a whole night’s migration can then be viewed in a few minutes. Modern radars can provide raw and processed data in different formats, including digital video. Machine learning can now be applied to identify objects more reliably and automate the processing of data. The combination of records from many different surveillance radars at different locations has been used to provide a broad picture of bird migration on particular dates over large regions, including much of North America (Figure 2.1). The US National Weather Service maintains a network of long-range weather surveillance Doppler radars (WSR-88D), collectively known as NEXRAD (for ‘next-generation Radar’). In Europe, a similar system operates under the European Weather Radar Network. These networks provide continuous and nearly complete spatial coverage over most of a continent, and can provide an unprecedented means of observing birds and other flying animals on both local and larger scales (for North America see Gauthreaux et al., 2003; Felix et al., 2008; Ruth et al., 2008; Buler & Dawson, 2014; Dokter et al., 2018; for Europe see Dokter et al., 2011; Nilsson et al., 2019). NEXRAD radars enable the density of birds aloft to be estimated, along with their general speed and direction. They can reveal how migrants respond to weather, artificial lights at night and physical obstacles such as large lakes and mountain ranges, and how closely bird movement patterns are associated with habitats or patterns of land use. They can identify important flyways, stopover and roost sites or locations of likely bird-aircraft collisions. They can also reveal seasonal and annual variations and long-term trends in the intensity of bird migration. Moreover, a comprehensive dataset of nearly every radar sweep, taken every 6 10 minutes, for every NEXRAD site dating back to the mid1990s is archived and available, opening the door to further research. Nevertheless, these weather radars do not provide effective coverage for all areas, and records up to about 20 km from the radar may be unusable in some places due to ground clutter caused by tall buildings. These radars are also not well suited for detecting low-flying birds and are poor at resolving flight altitudes. Smaller surveillance radars, operating over shorter distances, are used mainly at airports, military bases and local television stations, but the data they generate are not usually available to biologists. In contrast to surveillance radars, ‘pencil-beam tracking radars originally designed to lock onto and follow targets such as aircraft or missiles can provide information on the flightpaths of individual birds, recording altitude, speed and direction, and allowing their flight trajectories to be plotted in three dimensions (Bruderer et al., 1995). Alternatively, the beam can be used in a conical scanning mode to provide information on the spatial distribution of migrants (although calculations of bird numbers from conical scanning present problems). Wind profiles can be obtained by using radar to track ascending weather balloons carrying aluminium foil for maximum reflectance. Wind conditions are assessed from the speed and direction of the balloons as they climb through different altitude zones. The headings and airspeeds of migrating birds can then be calculated by comparing the bird data against the wind data.

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Altitude Zone 196–2530 Meters Birds km-3 0–25 26–50 51–75 76–100 101–125 126–150 >150

200

0

200

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FIGURE 2.1 Map depicting bird migration over the United States within the altitude zone 108 1724 m on the nights of 4 9 May 2000. Arrows reflect the positions of weather surveillance radars and show the directions and volumes of migration overhead. Map provided by S. Gauthreau. For further details see Gauthreaux et al. (2003).

Another radar technique involves a vertically projected beam designed to quantify the amount of migration taking place and the heights at which the birds are flying. This gives similar results to those obtained using a ceilometer, except that the radar detects birds through clouds and at all heights. Not all radars exist as fixed installations. Mobile units originally designed for use on ships can also be placed on vehicles, enabling bird migration to be studied anywhere that can be reached by road. The most comprehensive picture of migration can be obtained by a combination of surveillance radar and visual observations by ground-based observers in the same area. In their studies of the migration of soaring birds in Israel, Leshem & Yom-Tov (1996) also used a motorized glider to accompany flocks of large soaring birds over part of their journeys. They could thus record in detail the ups and downs of the birds’ flight, as they climbed in each thermal and glided, losing height, to the next. Further understanding could come from the extension of radar studies to other continents and from analyses of existing long-term data archived from weather radars. The latter could indicate how the timing, routes and volume of migration may have changed over recent decades.

DISTRIBUTION STUDIES For many years, museum collections provided useful information on bird distributions abroad. The aim of skin collectors, operating mainly in the 19th century, was to preserve samples of all the species occurring in different areas. The labels on these specimens still provide information on the tropical wintering areas of many migrants which have yielded few ring recoveries or other records. Among European breeding birds, for example, until recently the winter distribution of the Common Cuckoo (Cuculus canorus) in Africa was still better known from museum skins than from ring recoveries or tracking results.

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Over much of the world, more information is becoming available on the breeding and non-breeding distributions of birds through the collective efforts of birdwatchers. For some regions, these distributions have been depicted at a relatively fine scale in recent ‘atlas’ projects. However, in most tropical regions, where many high-latitude breeding species spend the non-breeding season, bird distributions are still poorly mapped, despite greater travel by birdwatchers. Systems now exist for observers in any part of the world to record their sightings online, adding to a growing pool of information on bird distributions (notably the eBird system run by the Cornell Laboratory of Ornithology in the USA). Such data show where particular species occur at different times of year; revealing breeding and non-breeding ranges, and seasonal progress along migration routes (Sullivan et al., 2014; La Sorte et al., 2016). Animated maps based on such records show the actual routes used by particular species and the speed of progress along them.

RINGING Around the end of the 19th century, research on bird migration experienced a major breakthrough with the start of scientific bird ringing (or banding), which soon became the mainstay of migration studies worldwide. Bird ringing began with the efforts of a schoolmaster, Hans Christian C. Mortensen, in Denmark in 1899, but it quickly spread to other places in Europe, North America and elsewhere. A ring is a light but tough metal band which can be placed loosely around the leg of a nestling or adult bird, with different sizes for different species. The British scheme currently uses rings of 20 sizes, with internal diameters of 2 26 mm. Each ring carries a unique engraved number, identifying the individual bird, and an address to which a recovery can be reported. Each bird can thus be identified unequivocally, and its whereabouts are known at least twice in its life at the time of ringing and recovery. In general, birds ringed as nestlings are of most value because their precise natal locality is known, whereas birds ringed as adults may be of less certain provenance. Depending on when and where they were caught, they may have been local breeders, winter visitors or passage migrants. Some recoveries of ringed birds are provided by other ringers who trap the birds alive and release them again, while other recoveries are provided by hunters or by other members of the public who may report birds found dead or injured. The recovery rates of ringed birds are generally low. In many small species, less than 0.1% of ringed individuals are ever reported again, but in larger species, especially those that are hunted, the proportion can rise above 20%. Of course, for ringers operating repeatedly in the same place, local recapture rates can be much higher, but such local records reveal little about bird movements. In general, therefore, getting useful information about migration in this way depends on ringing very large numbers of individual birds, from which varying proportions may be subsequently reported from elsewhere. Another problem is that recovery rates can vary greatly along migration routes, according largely to the density and interests of the local human population. For example, nearly 300,000 House Martins (Delichon urbica) have been ringed in Britain, but less than 1200 (0.4%) have been recovered. More than 90% of these reports were from within Britain and Ireland, and they gave no indication of migration routes. Only one came from Nigeria, within the presumed wintering range (Wernham et al., 2002). Determining the migration routes and wintering areas of seabirds by use of ringing presents a particular problem, as most relevant recoveries come from birds caught in fishing gear or washed up dead on beaches. These recoveries are obviously biased to areas where people are likely to find them, and dead birds may have drifted in currents taking them far beyond their place of death. In 1903, following the pioneering work of Heinrich Ga¨tke on Heligoland Island (Box 2.1), the first modern-style bird observatory and ringing station was established at Rossitten (now Rybachi) on the Courland Spit in the southern Baltic, a site where migrant birds become concentrated. Subsequently, many other bird observatories were established at other sites in Europe and North America and most are still in operation. Together, they provide a network of wellplaced sites, where migrants can be observed and, more importantly, trapped and ringed in large numbers. During the early 20th century, many countries came to run their own ringing schemes, in most of which ringing was carried out largely by amateurs operating in their home areas, but also making ringing expeditions to more remote places. Nowadays in Europe, the various national ringing schemes are linked by EURING, which coordinates techniques and the electronic handling of data, unifies standards and formats, and stimulates projects and analyses on a pan-European basis. All ringers are trained, tested and licensed before they can operate alone. Many techniques have been used to trap birds, some being developed from ancient methods used to catch birds for food. One important development was a giant funnel trap, big enough to enclose groups of bushes, known as the Heligoland trap, after the place where it was first constructed. At the end of the funnel is a glass-fronted catching box into which birds are driven (Figure 2.2). The numbers of birds ringed increased further in the 1950s with the development of other efficient trapping methods, including mist nets and cannon nets, which increased the range of species that

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could be caught in large numbers. Mist nets are essentially walls of fine, almost invisible netting, each up to 20 m long and up to 2 m high. Each net is erected on poles, and where possible is set against a background of trees and shrubs to prevent the net showing against the sky. Any small bird that hits the net slides into a pocket of net formed by one of 3 or 4 shelf strings, which are threaded horizontally at different levels through the length of the net. In some places, such nets have been hoisted into forest canopies using pulley systems. A different method was developed for catching waders, waterfowl or others that gather in large concentrations on the ground. A cannon- or rocket-propelled net is placed furled on the ground near where birds assemble (a roost or baited feeding area). The several rockets, or projectiles from cannons, are then fired simultaneously, pulling the large net rapidly over the unsuspecting birds (Figure 2.3). A smaller variant of this method is called a ‘whoosh net’ where the net is held under tension, and then triggered, powered by strong elasticated bungee cords (in lieu of explosives).

BOX 2.1 Heligoland Bird Observatory. The first bird observatory, of very different style from those of today, was established on the island of Heligoland (German Helgoland) in the southeastern North Sea, about 60 km west of Denmark and about 80 km north of the German town of Wilhelmshaven. The observatory became famous mainly through the work of Heinrich Ga¨tke, who spent more than 50 years on the island, observing and shooting birds. The skins were sold to museums and private collectors, providing income to Ga¨tke and his local collaborators. In the process, Ga¨tke amassed a great deal of information on the timing and volume of bird migration, and on the occurrence of vagrants on the island. The business of skin collecting meant that particular emphasis was paid to rarities, as in much of modern bird-watching. His famous book, Heligoland as a Bird Observatory, was translated into English and published in 1895. Until the spring of that year, he had recorded 398 different bird species on the island. The book is full of fascinating information, and most of his ideas and interpretations have stood the test of time, although in the absence of proper measuring devices, he greatly overestimated the speed and altitude of bird migration. The bird observatory still thrives on Heligoland, and like other modern observatories, it has become a centre for ringing and scientific study. It is the original home of the so-called Heligoland trap, a large horizontally placed wire-netting funnel, big enough to enclose many bushes, and through which birds can be driven and caught at the end (Figure 2.2). An account of the birds of Heligoland and the work of the modern observatory can be found in J. Dierschke (2022).

FIGURE 2.2 Drawing of a Heligoland bird trap, a large funnel through which birds can be driven and caught in a glass-fronted box at the end.

FIGURE 2.3 Cannon-netting of Eurasian Oystercatchers (Haematopus ostralegus).

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By the end of the 20th century, using a variety of trapping methods, more than 200 million birds had been individually ringed worldwide, giving hundreds of thousands of recoveries, revealing the movement patterns of different populations. Over the years, several ‘atlases’ of bird movements, based on ringing data, have been published (eg Zink & Bairlein, 1995; Wernham et al., 2002; Bakken et al., 2003). Ringing activities tend to be concentrated in particular regions, where opportunities and interest levels are high. Although many of the ringed birds then move on, the subsequent recoveries are probably biased, as mentioned above, towards areas with high-density, interested human populations. Care is therefore needed in the interpretation of ring recoveries, although they can still be useful in defining the flyways and wintering areas of particular breeding populations, the annual and seasonal timing of movements, and any sex and age differences in movements that might occur within species (Chapter 18). Some of the most geographically complete information on migration relates to North American waterfowl. It results from a planned, geographically dispersed ringing effort over many years, and subsequent recoveries provided from all parts of the continent by millions of hunters. Overall, ring recoveries are still a major source of information on bird movements. Taken together, they have revealed a network of bird migration routes that encompass all habitable parts of the globe, and that are travelled annually by millions of migrating birds. It has sometimes been possible to set up coordinated collaborative projects in a wide range of localities along a migration flyway, in which many observers collect data on the same species in a standardized way. The EURING projects on Barn Swallow (Hirundo rustica) and other European African songbird migrants provide examples (EURING website). One drawback of ringing is that the ring can normally be re-read only if the bird is in the hand, alive or dead. Not surprisingly, therefore, researchers have developed methods that enable the re-sighting of marked birds without the need to trap them. Marking has been achieved in different ways depending partly on the species and includes colour rings on the legs, large rings bearing numbers or letters that can be read through a telescope, coloured or numbered neck collars or wing tags. Such marking schemes have greatly increased the rate of information gain for some species, especially waterfowl and waders, and have often yielded multiple records of the same individuals at different places. They have given more accurate information than ring recoveries on the speeds of migration and the duration of stopovers. The information yield from such schemes is, of course, greatly increased if observers along potential migration routes are alerted to look out for tagged birds. For example, in the Black-tailed Godwit (Limosa limosa) in Britain, only 2.5% of ringed birds were ever recovered, but following the introduction of a colour-marking programme and additional observer input, more than 80% of marked birds were later reported, many at several different places on the migration route. In the same way, the use of colour leg-flagging greatly increased our knowledge of shorebird migration in Eastern Asia Australasia and in North South America, providing information on the timing and speed of migration, and of the locations of important stopover sites (Minton, 2003). Birds trapped for ringing can be sexed and aged, enabling differences in timing and other aspects of migration between sex and age groups to be identified. Individuals in the hand can also be measured and weighed, providing information on weight gain and fat deposition in different species, which can then be related to the types of journeys undertaken. Laboratory studies of carcasses have revealed that substantial changes in body composition accompany migration, not simply the gain and loss of fat (Chapter 5). Rates of weight gain are mainly recorded from individuals trapped more than once during their fattening period. Results can then be compared between individuals, between stopover sites and between different dates. From birds in the hand, samples of feathers or blood can also be taken for use in genetic, stable isotope or chemical analyses, and various instruments can now assess the internal body structure of trapped birds without the need to kill them, yielding information on the ratio of fat to muscle, for example (McWilliams & Whitman, 2013).

TRACKING DEVICES In recent decades, four main methods have been developed which allow the day-to-day tracking of individual birds on migration.

Very High-Frequency radio-transmitters Radios attached to birds transmit at Very High Frequency (VHF), and receivers can be carried by hand or fixed to a mast or building, vehicle or airplane. Early studies used airplanes to follow individual birds on migration, but because of international boundaries and other constraints, birds could seldom be followed along their whole migration routes (Cochran et al., 1967; Hunt et al., 1992; Kuyt, 1992). Nowadays, networks of purpose-built automated receiving stations, set up across wide areas can detect tagged birds as they pass by, as in parts of North and South America, Europe and Australia. Started in 2012, the Motus tracking system in eastern North America now has several hundred well-spaced receiving stations each of which can

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pick up signals up to 20 km away. Each station can detect many tagged birds simultaneously as they pass by, storing the data in a central depository for use by anyone involved (Taylor et al., 2017). The ultra-light modus nano-tags (0.13 g) emit a uniquely coded radio signal, allowing tagged birds to be identified individually. Receivers can be hosted by any individual or organization, and all the time the numbers of participants and receiver coverage are expanding. These automated systems are providing information on stopovers as well as on migratory movements.

Satellite transmitters From the late 1980s, it became possible to detect radio signals using satellites circling the Earth. In one of the earliest satellite-based tracking studies, six male Wandering Albatrosses (Diomedea exulans) had 180 g transmitters attached to them at their nests on the Croze´t Isles, midway between South Africa and Antarctica (Jouventin & Weimerskirch, 1990). Four of the six birds were followed for about a month as they wandered around the Southern Ocean looking for food. One flew a total of 15,200 km during 33 days. The satellite located it 385 times, and its maximum flight velocity between location points was 81 km/h. On one day this bird covered a total of 936 km. The other birds flew lesser but still impressive distances, although on foraging trips rather than migration. With further development and reduction in tag sizes, use of satellites now enables birds of various species to be tracked over their whole migrations, anywhere on Earth, thus providing new information on migration routes and wintering areas, migration speeds and durations, and the locations and durations of stopovers. The tags called Platform Transmitter Terminals (PTTs) are mounted on the bird’s back and held in place by a harness designed to cause minimum inconvenience to the wearer (see later). Initial tags were relatively heavy (100 200 g), largely because of the battery needed to power them, so could be attached only to large birds such as albatrosses, swans, geese and eagles. But over the years progressively smaller devices were developed, now down to 5 g, enabling their use on ever smaller birds, the aim throughout being to keep each tag to less than 3% 5% of the weight of the wearer (Kenward, 2001). Initially, all the tags were powered by an on-board battery, which formed most of the weight of the tag and limited its useful life to a matter of months. Various measures, such as intermittent transmission (say once every day or few days, called ‘duty cycling’), were used to lengthen battery life, but few battery-operated PTTs lasted longer than a year. However, from around 1995 tags with solar panels came into use, enabling the use of smaller batteries which could be continually recharged by the sun. In theory, such tags could last for the life of the wearer, and many have now worked for long enough to record successive migrations of the same individuals (Sergio et al., 2014; Meyburg 2021). A major challenge is that these solar panels can get covered by feathers, and that a few days without sun can lead to complete battery discharge, which can destroy the device. But now tags are available which monitor battery levels and shut them down temporarily, as required. Signals from the tags are detected by satellites which continuously circle the Earth over the poles, in the Argos system. This is a French-American system originally intended to detect signals from objects such as buoys and fishing vessels, but which is now used largely for research on moving animals. As a satellite passes overhead, it records the ‘Doppler shift’, detecting the signal at a slightly different pitch as it passes towards and away from the tag, much as the sound of a fast train passing through a station changes as it moves towards and then away from you. From these signals, a position for the tag can be calculated, with an accuracy that depends largely on how directly the satellite passes overhead. The signals from a PTT are recorded, transmitted to a receiving station in France and used to estimate the tag’s position. The information can then be forwarded to the researcher. Location errors can range up to hundreds of kilometres, but the researcher is told the level of reliability of each reading, which depends largely on the angle of the satellite pass and the quality of signals. Errors are generally greater from birds that spend much of their time underwater or in dense tree canopies. However, spatial errors are usually small on the scale of a long-distance migration; they are more than offset by the benefits of global coverage, the near real-time provision of data, and the lack of need to recapture the bird to recover the data (as is necessary with some other tracking devices). A major disadvantage is the cost of the PTT (currently about $1000 3000) and the fees for data processing (about $1000 $4000, depending on the amount of data), up to a total of $7000 per bird. The accuracy of location estimates improved greatly from 2007 when the earlier-developed Global Positioning System (GPS), also based on satellites, came into general use, providing the navigation systems used in smartphones and vehicles. This system receives from the satellites location estimates accurate to within a few metres, regardless of conditions. GPS was developed by the US military, but other systems developed in Russia (GLONASS), China (BeiDou) and Europe (Galileo) are broadly similar. The accuracy of locations enables precise assessments of a bird’s home range at different seasons, as well as the exact path of its migration. Used in conjunction with high-power satellite images or aerial photographs of the ground (as in Google Earth), a bird can be placed accurately within a landscape situated thousands of kilometres from the observer seated at home in front of a PC.

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GPS receivers can be used in conjunction with Argos PTTs, and upload the data via the Argos satellite system. Or they can be used independently, yielding their archived data through ground-based receivers or tag-recovery, for which the bird must be re-caught, enabling the stored data to be downloaded to a computer. Introduced around 2016, these archival GPS tags require much less battery power than PTTs, and can be small enough for use on small land birds. Current GPS tags as small as one gram can record about one location per day and up to 100 precise locations in total, enough to record a migration path, but again the bird needs to be re-caught to recover the data. The mass production and miniaturization of GPS technology has brought the costs down and enabled larger samples of birds to be tracked.

The mobile phone network GPS transmitters based on the Global System for Mobile Communication (GSM/GPS) became available from about 2012. These tags accumulate data on locations at pre-set intervals and periodically transmit them to the researcher through the mobile phone network. This system can handle more data per unit time than an Argos PTT, so ultimately it is more costeffective per location transmitted. The high spatial and temporal resolution of data collected by GSM/GPS transmitters allows in-depth analyses of the flight behaviour of individual birds across complete migrations, recording every time the bird changes speed, height or direction data which, in turn, can be related to prevailing atmospheric conditions. Whereas a satellite transmitter can power a signal over a few thousand kilometres, a cellular device generally transmits only up to about 50 km. The power requirements (and weight) of cellular-based tracking devices can therefore be reduced substantially. However, the performance of this ground-based system is limited by the number and distribution of receivers, which are absent over many areas, including the sea. In addition, users of cellular tracking technologies may encounter difficulties when their birds cross international borders or move among different cellular networks. However, some of these tags now allow ground-based communication with researchers using handheld mobile or fixed nodes, enabling data to be downloaded and tag settings to be reprogrammed.

Geolocation (Global Location Sensing or GLS logging) These devices, typically attached to the back or leg of the bird, dispense with the need for signal transmission, and instead store the information within the device for later retrieval (like some GPS loggers). For many species, the chances of re-catching the same individual are minuscule, but for others, a high percentage of surviving individuals return to the same breeding locations year after year, so that tag recovery is feasible. Needing only a very small battery, such geolocators are smaller and lighter than satellite tags. They can provide the same information as satellite tags on movements and stopovers, but with much less accuracy. The simplest light-level geolocators, wrapped in a single package, comprise a battery, memory chip, clock and light sensor, designed to record ambient light levels at pre-set intervals of one or more minutes. Early models from the 1990s weighed more than 40 g, so were again used mainly on large birds such as penguins (Wilson et al., 1995), but they became smaller over the years, and are now available down to 0.3 g and able to record day-length every 15 minutes, for use on small passerines (8 g or larger). From the recorded timing of sunrise and sunset, location data from anywhere on Earth can be calculated from the length of the day (or night) to indicate latitude, and the time of solar noon to indicate longitude (a change by one hour in the timing of noon relative to Greenwich Mean Time corresponds to a positional shift of 15 degrees of longitude). Several computer programmes are now available to calculate locations from geolocator data (for review see Lisovski et al., 2020). The main advantages of light-level geolocators include their smallness, cheapness and ability to provide one download data from a year or more. Owing to their relative simplicity, they can be produced for less than $100 each. Disadvantages include the lack of reliable latitudinal information around the dates of the equinoxes (approximately 20 March and 22 September) when day lengths are the same 12 hours worldwide, and the reduced precision of locations measured under cloud or other shading. An additional drawback is that, so far, information retrieval has depended on the bird’s survival and return to the capture site, and the researcher’s success at re-trapping it. The precision of geolocation estimates using light loggers depends how accurately the times of sunrise and sunset can be measured. These events are usually identified as the times when light intensity passes a specific threshold. So anything that affects ambient light levels, such as shading from clouds, plumage or vegetation, can lead to errors in location estimates. In early studies, light-level geolocators deployed on marine birds were found to be accurate to around 200 km of latitude (north-south) and around 50 km of longitude (Welch & Eveson, 1999; Phillips et al., 2004a,b). However, marine species experience less shading than most terrestrial birds. For Wood Thrushes (Hylocichla mustelina) in Central American forests, ground-truthing in the field revealed latitudinal errors in location averaging 365 km and longitudinal errors averaging 66 km (McKinnon et al., 2013). Other studies have attached geolocators and GPS tags to the same

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birds and compared the results. On the reasonable assumption that GPS tags gave accurate location estimates, errors in geolocator estimates were up to several hundred km. They became greater closer to the equator, and (as expected) close to the equinoxes, but more surprisingly, errors also varied between species, between geolocator models and between two programmes used to convert geolocator data to locations (Halpin et al., 2021). Nevertheless, despite the errors, geolocators could be regarded as providing reasonable estimates of the migration routes and wintering areas of long-distance migrants (Figure 2.4).

FIGURE 2.4 Migrations of 12 Manx Shearwaters (Puffinus puffinus) nesting on Skomer Island, Wales, based on birds tracked using leg-mounted light-level geolocation loggers. These devices carry light sensors and record information which can be used to estimate the locations of each bird at intervals from prevailing light-dark cycles. The apparent appearance of these pelagic birds overland is attributable to imprecision in some of the location estimates given by this method. Nevertheless, the locations indicate a direct journey from Skomer past West Africa across the southern Atlantic to eastern South America, where the Patagonia Shelf provides a rich wintering area previously known from ring recoveries. The birds then migrate northward up the western Atlantic, and cross to Britain in the northern hemisphere, completing a figure-8 journey. This different return route was revealed by geolocators but not previously known from ring recoveries, and nor was the existence of regular stopover sites, at which some birds remained for up to a fortnight. Modified from Guilford et al. (2009).

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Passive Integrated Transponders tags Other devices are used to record bird presence at predetermined places rather than to track bird movements. Such PIT tags (Passive Integrated Transponders) are about the size of a grain of rice, which can be implanted in a bird’s body or attached to a ring. Each PIT has a unique code which can be read automatically at subsequent dates by a batterypowered receiver placed near the nest or other regularly visited site. This method has been used to record the return dates of individual Common Terns (Sterna hirundo) to their nesting colony (Dittman & Becker, 2003), for example, and to identify individual Peregrines (Falco peregrinus) at nest sites in different years, thus providing information on survival and site-fidelity in a non-migratory population (Smith et al., 2015).

Other sensors In addition to position locators, various other sensors can now be attached to birds, either separately or part of a single unit. They include heartbeat monitors, temperature sensors, pressure (altitude) sensors, depth sensors for diving birds, accelerometers, video and audio loggers and others. Tri-axial accelerometers reveal much about a bird’s flight and other activities, its reactions to winds and other influences, as well as its energy consumption. These various devices add weight, but they can provide unique information on aspects of flight, energy use, feeding and ambient conditions throughout a journey.

Effects of tags Important questions about all types of tags (including wing-tags) concern the extent to which they affect the behaviour, breeding or survival of the wearer. For tracking devices, these questions have now been addressed on the basis of more than 450 measures of impacts across 214 published studies (Bodey et al., 2018). Small but significant negative effects of tagging were apparent on survival, reproduction and parental care. Features of the bird, such as flying style, migration distance and relative tag mass, were significant in producing these effects, as was attachment type and position on the body. That said, many of the studies revealed no measurable effects. Overall, more effects were noted on smaller birds than on large ones, on aerial foragers than on other birds, and on birds in which tags were at the heavy end of the acceptable range for the species concerned (Bridge et al., 2013; Costantini & Møller, 2013; Brlik et al., 2019). In the early days, effects often resulted from the harnesses or other methods used to attach the tag rather than the tag itself, and on small birds more effects were noted from geolocators on legbands rather than backpacks. Many transmitting devices were designed to detach from the bird after a set period, when their useful life was over. As a result of early findings, designs of harnesses and tags improved over the years, so that mishaps now seem rare, and overall impacts have probably been reduced. This is important not only for welfare reasons but also for the reliability of the information gained. Recent studies using up-to-date equipment designs found no obvious impacts of any kind (see Ku¨rten et al., 2019 for Common Tern; Van Wijk et al., 2016 for Hoopoe (Upupa epops)). Nevertheless, researchers using these methods are continually working to minimize impacts and maximize conservation benefits. For further studies of tag effects on birds, check Kenward (2001), Barbraud & Weimerskirch (2012), Weiser et al. (2016) and Green et al. (2019).

Storage of data Some of the tracking technologies described above are able to collect many thousands of locations for each individual, making data analysis a particular challenge. New online data-storage facilities offer tools not only for the management of tracking data but also for archiving and sharing. These services help to make the most of data that are often costly and difficult to obtain and can link or amalgamate different studies to produce further insights. The foremost online archive for tracking data is Movebank hosted by the Max Planck Institute of Animal Behavior in Germany. This is a free global repository for data from individually tracked animals (not just birds) that allows users to maintain sole control of their data or share them with named collaborators or with the wider research community (Kranstauber et al., 2011). This resource offers basic mapping and visualization, as well as data on global weather and land cover, enabling their use in the analysis of bird movements. Data depositories offering further facilities are likely to appear in future.

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The Migration Ecology of Birds

Future developments From September 2020, researchers have also been able to track birds and other animals using the International Space Station, via an ambitious project called the International Cooperation for Animal Research Using Space (ICARUS). The technical requirements for this system include relatively low orbit altitudes of the station (ideally about 320 km, as opposed to the 850-km orbit of the Argos system) and specialized antennae tuned to receive weak signals from the ground and transmit them back to users via Movebank. Because the receiving station is nearer the Earth, the ICARUS trackers do not have to create such strong radio signals as are needed for Argos satellites and can therefore be smaller. The transmitter tags are solar-powered and only activate when the Space Station passes over them on its 16 circuits of Earth per day, thus greatly preserving battery power. The ICARUS project currently implements 5 g radio transmitters that include a GPS receiver, but has plans to use devices weighing less than 1 g in the future, extending studies to much smaller birds. ICARUS could soon provide further insights into bird movements and, for the first time, should give a detailed resolution of movements without the bias toward surviving individuals. We may eventually determine the fate of birds that do not make it back to their original tagging sites, including irruptive species which show little or no sitefidelity. This system may transform the field of animal tracking.

ISOTOPES AND OTHER INTERNAL MARKERS Analyses of stable isotopes in bird tissues can provide information on the broad provenance of trapped migrants. Isotopes are atoms of the same element with different numbers of neutrons, and therefore unique atomic masses. Unlike radioactive isotopes, stable isotopes persist for long periods of time. The stable isotope ratio of an element is expressed, in delta (δ) notation, as the ratio of the rarer, heavier form to that of the commoner, lighter form. Stable isotope ratios of several abundant elements, including hydrogen (H), carbon (C), nitrogen (N) and others vary consistently either across broad geographical regions or between bird habitats and food types (Hobson, 1999). For example, in North America, the ratio of hydrogen to its isotope deuterium (δD) in precipitation varies across the continent, from deuterium-enriched in the southeast to deuterium-depleted in the northwest. These patterns are transferred from plants to animals. Birds absorb isotopes from their food and deposit them in body tissues, giving isotope signatures which reflect either the region where the food was eaten or the habitat and type of food. Birds that move between regions or food webs can retain information of previous feeding locations for periods that depend on the turnover rates of particular isotopes in their body tissues. Keratinous tissues, such as feathers or claws, become metabolically inert when their growth ceases, and maintain an isotopic signature reflecting the food eaten at the time and place of their formation. Other tissues are metabolically active, and retain their signatures for periods ranging from a few days (in the case of liver or blood plasma) to several weeks (in the case of muscle or whole blood), to the lifetime of the individual in the case of bone collagen (Hobson, 2003). Isotope ratios also change as the chemicals concerned pass from prey to predator, upwards through food webs, because of differential loss through excretion and respiration, but these changes are known and can be allowed for in analyses. In practical terms, by catching a bird once only and pulling a single feather, analysing its stable isotope signature by mass spectrometry, and comparing this with known geographical patterns in isotope ratios, it is possible to identify (in very broad terms) where the bird grew its feathers. Even without a baseline reference, one can tell whether different breeding populations have their own distinct wintering areas or whether wintering populations have their own distinct breeding areas. It is thus not necessary to re-capture birds, and the method is equally applicable to museum specimens. Different populations of birds replace their feathers at different times of year. In birds that moult in summer, feathers plucked in wintering areas can reveal the regions where those birds bred (eg Chamberlain et al., 1996; Kelly et al., 2002; Rubenstein et al., 2002). Similarly, for birds that moult in winter, feathers plucked in breeding areas can reveal the regions where those birds wintered (eg Chamberlain et al., 2000). Isotope analyses have shown that different birds sampled in a particular breeding area had wintered in different areas from one another (Møller & Hobson, 2004), and that birds sampled in particular wintering areas had bred in different areas from one another (Hobson & Wassenaar, 2001). They have also revealed the breeding areas of irruptive migrants caught in winter (Newton et al., 2006). Although useful in identifying the regional origins of migrants, and filling gaps in other information, isotope analyses cannot provide anything near the geographical resolution that is possible with other approaches, such as ringing or GPS-tracking. Nevertheless, the method of isotope analysis provides better-than-nothing information for species with low recovery rates in the regions concerned, especially where analysis of several elements rather than one can give greater discrimination.

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Isotope analyses of soft tissues have been used to address other questions, such as (1) whether eggs were formed from food eaten in the immediate breeding area or from food imported to the breeding areas as body reserves accumulated in migration or wintering areas (Chapter 5; Hobson et al., 2000; Klaassen et al., 2001); (2) whether birds breeding in one region had accumulated body reserves on the same or different stopover sites (Hobson, 2003); and (3) whether particular individuals examined in a breeding area had spent the winter in good or poor habitat (knowledge which can then be related to migration and breeding performance; Marra et al., 1998). Turning to other internal markers, analyses of trace elements in feathers have also been used to indicate the broad geographical origins of birds. The proportions of different elements in feathers vary from region to region, according to geological substrate, and these patterns are again passed up the food chain (Hobson, 2005). Sand Martins (Riparia riparia) breeding in different parts of Europe differed markedly in the elemental composition of their tail feathers, indicating that the birds from different breeding areas had moulted in different parts of Africa (which is where the tail feathers are grown). Moreover, tail feathers from the same individuals in different years were similar in elemental composition, implying that individuals were consistent in their African moulting areas from year to year (Sze´p et al., 2003). Other studies of this type have involved Peregrine Falcons (Parrish et al., 1983) and various species of geese (Hanson & Jones, 1976). For years DNA analyses were little used in migration studies (Wink, 2006). This is partly because different geographical populations of some bird species differ insufficiently in DNA to enable their reliable separation at the level of analysis possible, but also because DNA methods were for many years expensive and time-consuming. But as methods have developed and costs declined, genetic profiling has played an increased role in migration studies, notably in the genetic control of migration (Chapter 22) and of the development through post-glacial times of current migration patterns (Chapter 24). The doors are now open for rapid expansion in further DNA research as it relates to migration.

RESEARCH ON CAPTIVE BIRDS Laboratory research on bird migration began in the mid-1920s and rapidly gained ground. Hundreds of experiments on migratory physiology, orientation and other aspects have now revealed most of the relevant physiological processes and controlling mechanisms, at least in broad terms (Chapters 12 and 13). An important discovery was that at appropriate times of year, migratory birds in captivity developed migratory restlessness (Zugunruhe in German), in which they hop and flutter around their cages. This activity can be registered automatically by use of electronic trips under perches (Chapter 13). Migratory restlessness in captive birds occurs either by day (in diurnal migrants) or at night (in nocturnal ones), and has been regarded as the laboratory equivalent of migration itself (see Box 13.1). Such behaviour appears chiefly in birds from migratory populations and much less so, or not at all, in birds from sedentary populations. The number of days on which migratory restlessness is shown has been found to correlate with the natural duration of migration (and hence distance travelled) in the population concerned. Migratory restlessness therefore provides a useful proxy for comparing the migration seasons of captive birds from different populations, and of testing the influence of various factors on migration timing (Chapter 22). In particular, the influence of daylength on migration timing has been examined by manipulating the artificial daylengths (photoperiods) to which captive birds are exposed, and then recording their condition and behaviour. Metabolic rates, food consumption, fat deposition, body weights and migratory activity can all be studied at the same time. Another discovery was that captive birds also developed strong directional preferences at migration times. Such preferences could be measured in individuals using circular ‘orientation cages’, which typically have solid sides and wire tops affording a view of the sky. In one early type, the cage was shaped like the top half of a funnel up to 40 cm in diameter, with an inkpad at the bottom, sloping sides lined with blotting paper and wire mesh across the top. As a bird hops, the ink on its feet leaves a trace on the blotting paper up the sloping sides which provides an index of both the direction and intensity of migration (Emlen & Emlen, 1966). In a later type, automatic registration was achieved in circular cages equipped with radially arranged perches fitted with micro-switches to record directional activity, which can then be passed to some central recording unit (eg Wiltschko, 1968). And more recently, a video camera placed above the cage enabled individual take-off attempts to be recorded separately from other movements, giving more precision and less scatter in recorded directions (Bianco et al., 2016). The simplest of all such cages was designed specifically for use in the field on birds trapped on migration (Busse, 1995; Figure 2.5). Another benefit of studying migratory orientation in caged birds is that the external information received by the bird can be manipulated. For example, the perceived position of the Sun can be altered by the use of mirrors, star patterns can be modified in a planetarium, or the geomagnetic field can be altered using large magnetic coils (Wiltschko & Wiltschko, 1995). These procedures facilitate study of the external cues that might be used by birds to determine their migratory direction (Chapter 11). In these and other studies of captive birds, procedures such as automated image analysis and machine-learned algorithms can now speed up and improve the analysis of data.

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The Migration Ecology of Birds

FIGURE 2.5 Orientation equipment for measuring directional preferences of birds in field conditions: protective non-transparent wall around, and test cage within. The cage is shaped like a round cake. It is made of two circles of wire, connected by eight vertical wires. The top is covered with wire netting through which the test bird can see the sky. The sidewall is covered by transparent foil (kitchen wrap or cling film) on which pecks and scratches are made by the bird in its attempts to escape the cage. The cage is placed in the centre of a circular fence of uniformly coloured solid plastic that prevents the bird from seeing any landmarks other than the sky. After a standard time (say 10 minutes) in the cage, the bird is removed, as is the transparent foil, and the pecks and scratches are counted in each sector of the foil. A new piece of foil is then attached in preparation for the next bird. With two cages available, up to six birds can be tested each hour by a single observer. From Busse (1995).

Wind tunnels Specially developed wind tunnels have revealed much about the mechanics and energy needs of bird flight (Pennycuick et al., 1997). A wind tunnel creates a smooth (laminar) airflow in a test section where birds are trained to fly. The artificial wind speed can be adjusted so that, when the bird flies against the wind, it maintains a constant position. Wind tunnels have been used to test flight mechanical theory (Chapter 3), to measure the metabolic costs of flight and to study flight style using high-speed video cameras. To yield meaningful results, especially on energy consumption, birds must be trained in the wind tunnel beforehand, so that they ‘feel at home’ there, and fly steadily, maintaining a constant position against the wind for long periods.

Breeding programmes The large-scale breeding of captive birds has revealed much about the genetic control and inheritance of different aspects of migratory behaviour, including timing, duration or directional preference (Berthold, 1996). The most convincing results have come from cross-breeding individuals of the same species but drawn from populations with different migratory behaviour (Chapter 22). In general, the resulting offspring showed migratory behaviour that was intermediate in timing, direction and duration between their two parents. Also, by breeding only from the most migratory individuals in a population, migratory behaviour could be enhanced over several generations, and similarly by breeding from the least migratory individuals, populations became increasingly non-migratory. These experiments, conducted mainly on Eurasian Blackcaps (Sylvia atricapilla), confirmed that all major aspects of migratory behaviour can be genetically controlled, and can therefore be altered by selection (Chapter 22).

MATHEMATICAL MODELS Mathematical modelling has helped in formulating questions to be answered by further research. So-called optimization analysis has proved to be a powerful approach in the study of adaptation, and it has been increasingly used to test hypotheses about bird migration (Alerstam & Lindstro¨m, 1990; Alerstam & Hedenstro¨m, 1998; Alerstam, 2011). Models are used to predict behavioural and other patterns that ‘should’ be observed if individuals follow one strategy or another, and the predictions are compared to field observations or experimental findings to see how well they fit, and hence to infer the likely strategy adopted by the bird. The theory of bird flight yields quite specific predictions on the speed and altitude of flight and how they are expected to vary with wind conditions or fuel loads, all of which have been tested with field data. Other aspects examined include patterns of fuel deposition, flights and stopovers, routes and detours, daily and seasonal timing, wind selectivity and wind drift, predation risk, and annual moult and migration schedules (Alerstam & Hedenstro¨m, 1998; Alerstam, 2011). The combination of modelling and field observation thus provides a potentially powerful method for studying migratory adaptations. But such models depend heavily on the assumptions on which they are based. Early assumptions may

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later prove to be unrealistic or based on inadequate knowledge. Such models are nonetheless important in directing research, through defining more precise questions and the types of data needed to address them. Like any other ideas, formal models (often couched in mathematical terms) must be continually tested against experiments and field observations. Progress is often most rapid when predictions are not supported by new data, suggesting that seemingly plausible ideas are probably wrong. In addition, optimality does not necessarily require that all individuals in a population behave in the same way. It requires only that individuals make decisions that raise their own fitness, including making the best of a bad job. Different individuals may therefore pursue different tactics, depending on their own physical condition at the time, and on the prevailing environment as it affects them. Factors that influence individual variation in behaviour are increasingly being incorporated into optimality modelling. In this book, I shall not dwell on the mathematical details of various models (which are often complex and ever subject to revision) but shall instead focus on the understanding that has emerged from their use.

CONCLUDING REMARKS Observation and bird ringing were the main methods used to study bird migration used through much of the 20th century, and bird ringing also facilitated large-scale displacement experiments designed to study the homing and navigational skills of birds. Throughout the latter half of the 20th century, newer and increasingly more sophisticated methodologies were progressively added, gradually spreading migration research to an increasing range of species, and enabling previously intractable questions to be addressed. Most of these methodologies, including radar and tracking technology, were developed for very different purposes, but soon proved their value in studies of bird migration. Throughout this period, no method has been abandoned, and the old methods of observation and ringing are still contributing to the growth in understanding. Migration research has also depended heavily on the contributions of ‘citizen scientists’, whose participation has greatly increased the numbers of active field-workers and the geographical spread of studies. Tracking devices have proved especially useful on species otherwise hard to study, such as landbirds that winter in the tropics or make long trans-oceanic flights, and pelagic seabirds that spend most of their lives at sea. It is now possible to learn the location of a tagged bird to within a few metres, and for a seabird whether it is flying or swimming, whether it is on or below the surface and the depth of its dive. Tracking studies have also led to the discovery of previously unknown migration routes and wintering areas. Who would have guessed, for example, that Red-necked Phalaropes (Phalaropus lobatus) nesting on the Shetland Islands off northern Scotland would travel to winter on the Pacific Ocean between Ecuador and the Galapagos Islands (Smith et al., 2018). When locations are combined with remotely-sensed land cover data, they can also be used to examine habitat use in remote regions (Fraser et al., 2012a,b; Trierweiler et al., 2013). Tracking devices have further revealed the extent to which routes, timing and travel speeds vary between individuals, and the locations of stopover areas used on migration. Modern satellite tags also allow the reliable recording of when and where deaths occur during migration. Each tracking system has its pros and cons in terms of tag weight, power requirements and cost. Through increasing bird body weight, current options include light-level geolocators (down to ,0.3 g), GPS data loggers (1.0 g, able to store 100 locations), satellite PTT Doppler systems (5 g), satellite GPS 1 Argos tags (22 g) and cellular GPS tags (27 g) (Bridge et al., 2011). Only in recent years have small passerines been trackable using such devices. For the migration researcher, an ideal tracking system should be lightweight; it should measure three-dimensional locations (that is, include altitude), transmit data remotely and measure biological parameters of the individual and of the environment through which it passes (Bouten et al., 2013). Each bird tracked should need to be caught no more than once, and the attached equipment should have no detectable impact on the wearer, detaching when no longer necessary. Over the past three decades, we have come progressively closer to these ideals, at least for bigger birds. Looking to the future, further breakthroughs are likely now that tracking devices have been miniaturized to such an extent that they can be safely used on smaller birds, now that devices are available for measuring aspects of the physiological condition of individual birds throughout their journeys, and now that migration studies are spreading to parts of the world where they were previously unknown.

SUMMARY Bird movements have been studied by observations (made directly or with radar), by bird counts at particular localities in different seasons, by wide-scale distribution surveys, by use of ring recoveries to discover routes, and in recent years by the use of tracking devices to follow individual birds day-by-day on their journeys.

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The Migration Ecology of Birds

Most bird migration occurs at heights too great to be seen only with binoculars, and many species travel by night, so counts of migrating birds seen from the ground represent a small and variable proportion of those passing overhead. For most species, visual counts cannot, therefore, reveal the true volume of migration, or the weather conditions that favour it. At night, birds can be seen through binoculars or a telescope as they cross the lit surface of the moon, or through a powerful upwards-directed light beam. Nocturnal migrants can also be detected using night-vision equipment or can be heard passing overhead, aided by use of a parabolic reflector and amplifier. The best measures of the volume of bird migration come from surveillance radars which can be used day or night in all weathers, but cannot give precise identification of species. Ringing is the main means by which the migration routes and wintering areas of breeding birds have been studied in the past, together with any age or sex differences within populations. Ringing identifies individuals unequivocally, but tends to be concentrated in regions with high human interest, as do recoveries. Live birds in the hand can also be measured and weighed, providing information on weight gain and fat deposition; they can also provide samples for various kinds of analyses, and be tested in orientation cages for directional preferences. Colour rings and other conspicuous tags enable individual birds to be identified at a distance without their being recaptured or killed. Through modern technology, individual birds can now be fitted with miniature tracking devices and followed on their migrations, wherever on earth they go, providing information on travel routes and wintering areas, timing and duration of journeys, and locations and durations of stopovers. Four main tracking systems are in current use: VHF radio transmitters for detection by ground-based receivers, PTTs for detection by Argos satellites, transmitters for detection by the mobile phone system (GSM/GPS), and geolocation loggers in which location data are stored in the device for later retrieval. Each method has its own pros and cons with respect to cost, weight, accuracy and longevity of tags. Light-level geolocators can now be used on birds of all sizes, down to small passerines, but give poor positional accuracy, which varies geographically and is affected by cloud cover and other factors. Further miniaturization of GPS tags will facilitate their use on a growing range of species. Analyses of isotope or trace element signatures in bird feathers or other tissues have provided additional insights, linking birds from particular breeding regions with particular wintering regions, or vice versa. Laboratory work has revealed relevant physiological processes and controlling mechanisms, and wind tunnels have been used to study various aspects of bird flight, including energy consumption. Studies of migratory restlessness and migratory orientation on captive birds have provided details of migratory timing and directional preferences in particular populations. Such studies are being increasingly extended to free-living birds.

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Lisovski, S., Bauer, S., Briedis, M., Davidson, S. C. Dhanjal-Adams, K. L. et al. (2020). Light-level geolocator analyses: a user’s guide. J. Anim. Ecol. 89: 221 363. Marra, P. P., Hobson, K. A. & Holmes, R. T. (1998). Linking winter and summer events in a migratory bird by using stable-carbon isotopes. Science 282: 1884 6. McKinnon, E. A., Stanley, C. Q., Fraser, K. C., MacPherson, M. M. Gasbourn, G. et al. (2013). Estimating geolocator accuracy for a migratory songbird using live ground-truthing in tropical forest. Anim. Migr. 1: 31 8. McWilliams, S. R. & Whitman, M. (2013). Non-destructive techniques to assess body composition of birds: a review and validation study. J. Ornithol. 154: 597 618. Meyburg, B.-U. (2021). Lesser Spotted Eagle Clanga pomarina. Pp. 76 87 in Migration strategies of birds of prey in Western Palearctic (eds M. Panuccio, U. Mellone, & A. Agostini). Boca Raton, FL, CRC Press. Minton, C. (2003). The importance of long-term monitoring of reproduction rates in waders. Wader Study Group Bull 199: 178 82. Møller, A. P. & Hobson, K. A. (2004). Heterogeneity in stable isotope profiles predicts coexistence of populations of Barn Swallows Hirundo rustica differing in morphology and reproductive performance. Proc. R. Soc. Lond. B 271: 1355 62. Newton, I., Hobson, K. A., Fox, A. D. & Marquiss, M. (2006). An investigation into the provenance of Northern Bullfinches Pyrrhula p. pyrrhula found in winter in Scotland and Denmark. J. Avian Biol. 37: 431 5. Nilsson, C., Dokter, A. M., Verlinden, L., Shamoun-Baranes, J. Schmid, B. et al. (2019). Revealing patterns of nocturnal migration using the European weather radar network. Ecography 42: 876 86. Nisbet, I. C. T. (1959). Calculation of flight directions of birds observed crossing the face of the moon. Wilson Bull 71: 237 43. Parrish, J. R., Rogers, D. T. & Ward, F. P. (1983). Identification of natal locales of Peregrine Falcons (Falco peregrinus) by trace-element analysis of feathers. Auk 100: 560 7. Pennycuick, C. J., Alerstam, T. & Hedenstro¨m, A. (1997). A new lowturbulence wind tunnel for flight experiments at Lund University, Sweden. J. Exp. Biol 200: 1441 9. Phillips, R. A., Silk, J. R. D., Croxall, J. P., Afanasyev, V. & Briggs, D. R. (2004a). Accuracy of geolocation estimates for flying seabirds. Mar. Ecol. Prog. Ser. 266: 265 72. Phillips, R. A., Silk, J. R. D., Phalan, B., Catry, P. & Croxall, J. P. (2004b). Seasonal sexual segregation in two Thalassarche albatross species: competitive exclusion, reproductive role specialization or foraging niche divergence. Proc. R. Soc Lond. B 271: 1283 91. Rubenstein, D. R., Chamberlain, C. P., Holmes, R. T., Ayres, M. R. Waldbauer, J. R. et al. (2002). Linking breeding and wintering ranges of a migratory songbird using stable isotopes. Science 295: 1062 5. Ruth, J. M., Buler, J. J., Diehl, R. H. & Sojda, R. S. (2008). Management and research applications of long-range surveillance radar data for birds, bats, and flying insects. USGS Science for a changing world. Fact Sheet, 2008 3095. Available from https:// doi.org/10.3133/fs20083095. Schmaljohann, H., Liechti, F., Bachler, E., Steuri, T. & Bruderer, B. (2008). Quantification of bird migration by radar a detection probabliity problem. Ibis 150: 342 55.

Sergio, F., Tanferna, A., De Stephanis, R., Jime´nez, L. L. Blas, J. et al. (2014). Individual improvements and selective mortality shape lifelong migratory performance. Nature 515: 410 13. Smith, G., Murillo-Garcia, O. E., Hostetlar, J. A., Mearns, R. Rollie, C. et al. (2015). Demography of population recovery: survival and fidelity of Peregrine Falcons at various stages of population recovery. Oecologia 178: 391 401. Smith, M., Bolton, M., Okill, J. D., Harris, P. Petrie, G. et al. (2018). Further evidence of transatlantic migration routes and Pacific wintering grounds of Red-necked Phalaropes breeding in Shetland. Br. Birds 111: 428 37. Sullivan, B. L., Aycrigg, J. L., Barry, J. H., Bonney, R. E. Bruns, N. et al. (2014). The eBird enterprise: an integrated approach to development and application of citizen science. Biol. Conserv. 169: 31 40. Sze´p, T., Møller, A. P., Vallner, J., Kovacs, B. & Norman, D. (2003). Use of trace elements in feathers of Sand Martins Riparia riparia for identifying moulting areas. J. Avian Biol. 34: 307 20. Taylor, P. D., Crewe, T. L., Mackenzie, S. A., Lepage, D. Aubry, Y. et al. (2017). The Motus Wildlife Tracking System: a collaborative research network to enhance the understanding of wildlife movement. Avian Conserv. Ecol. 18 (1): 8. Trierweiler, C., Mullie, W. C., Drent, R. H., Exo, K.-M. Komdeur, J. et al. (2013). A Palaearctic migratory raptor species tracks shifting prey availability within its wintering range in the Sahel. J. Anim. Ecol. 82: 107 20. van Doren, B. M., Lostanlen, V., Cramer, A., Salamon, J. Dokter, A. et al. (2023). Automated acoustic monitoring captures timing and intensity of bird migration. J. Appl. Ecol 60: 433 44. van Wijk, R. E., Bauer, S. & Schaub, M. (2016). Repeatability of individual migration routes, wintering sites and timing in a longdistance migrant bird. Ecol. Evol. 6: 8679 85. Weiser, E. L., Lanctot, R. B., Brown, S. C., Alves, J. A. Battley, P. F. et al. (2016). Effects of geolocators on hatching success, return rates, breeding movements, and change in body mass in 16 species of Arctic-breeding shorebirds. Movement Ecol 4: 12. Welch, D. W. & Eveson, J. P. (1999). An assessment of light-based geoposition estimates from archival tags. Can. J. Fish. Aquat. Sci. 56: 1317 27. Wernham, C. V., Toms, M. P., Marchant, J. H., Clark, J. A., Siriwardena, G. M. & Baillie, S. R. (2002). The migration atlas: movements of the birds of Britain and Ireland. London, T. & A. D. Poyser. Wilson, R. P., Scolaro, J. A., Peters, G., Laurenti, S. Kierspel, M. et al. (1995). Foraging areas of Magellanic Pengins Spheniscus magellanicus breeding at San Lorenzo, Argentina, during the incubation period. Mar. Ecol. Prog. Ser. 129: 1 6. Wiltschko, W. (1968). Uber den Einfluss statischer Magnetfelder auf die Zugorientierung der Rotkehlchen (Erithacus rubecula). Z. Tierpsychol 25: 537 58. Wiltschko, R. & Wiltschko, W. (1995). Magnetic orientation in animals. Berlin, Springer-Verlag. Wink, M. (2006). Use of DNA markers to study bird migration. J. Ornithol. 147: 234 44. ˚ kesson, S., Liechti, F. & Bruderer, B. (2001). Nocturnal Zehnder, S., A autumn bird migration at Falsterbo, South Sweden. J. Avian Biol. 32: 239 48. Zink, G. & Bairlein, F. (1995). Der Zug Europa¨ischer Singvo¨gel. Wiesbaden, AULA-Verlag.

Part 1

The migratory process

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Chapter 3

Migratory flight

King Eiders Somateria spectabilis on migration I was perfectly amazed to behold the air filled and the sun obscured by millions of pigeons, not hovering about, but darting onwards in a straight line with arrowy flight, in vast mass a mile or more in breadth, and stretching before and behind as far as the eye could reach. Major King, Ontario, late 19th century, writing of the migration of the Passenger Pigeon.

No one can fail to be impressed by the migrations of birds. Some journeys extend over distances of more than 10,000 km, and involve the crossing of seas and other inhospitable areas. Such migrations require extraordinary navigational skills, massive body reserves to fuel the flights, and sustained nonstop effort sometimes for days on end. Migration differs from ordinary day-to-day flight not only in the much greater length of journeys, but also in the greater altitudes at which it usually occurs. So once underway, birds are usually exposed to a cooler and thinner atmosphere, with reduced buoyancy and oxygen levels. Moreover, areas of suitable habitat, where a migrant can rest and feed safely to replace depleted body reserves, may be limited. Astonishingly, some species, such as grebes, rails and gallinules, may have hardly flown for months before they set off on migration, having moved around mainly by walking or swimming. Yet at the appropriate time, and having accumulated the necessary body reserves, they suddenly ascend into the night sky and fly for hundreds of kilometres nonstop. In Barnacle Geese Branta leucopsis, attached heartbeat loggers revealed that in the weeks before autumn departure the birds flew for no more than a few minutes per day. Yet on migration, they flew nonstop for up to 13 hours at a time, with only occasional breaks in the 2500 3000 km journeys (Butler et al., 2000). Evidently, the amount of practice needed by such birds is minimal, compared with that needed by a human athlete to perform for much shorter periods. Nevertheless, the lengths and types of journeys that birds can undertake are greatly influenced by the body size, wing shape, flight power and other features of the birds themselves. This chapter is concerned with these issues, together with the role of social interactions, rest and sleep on migratory journeys.

BODY WEIGHT, SPEED AND FLIGHT MODE The importance of flight speed to migration is obvious: for a faster bird can cover a greater distance per unit time airborne. The flight speeds of birds have often been measured using a car or airplane travelling alongside, or by using radar to track the movements of individuals (Bruderer & Boldt, 2001). Measures taken from a vehicle or airplane cannot The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00021-X © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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be corrected for wind effects, and are often of doubtful accuracy. Radar measures can be obtained specifically for birds on migration and can be corrected to allow for wind effects, but they do not always provide a reliable identification of species. In addition to measured values, theoretical flight speeds can be calculated from aerodynamic principles on the basis of body mass, wingspan and wing area (Pennycuick, 1969, 2009). These various sources of information all indicate that, while individual birds can vary their flight speeds according to circumstance, larger birds generally fly faster than smaller ones, with body shape and wing shape having additional influence. Flight is clearly not a uniform activity. Many species can vary their speed and wing-beat frequency according to prevailing conditions and intent, and some can switch between different types of flight, such as flapping and gliding. In consequence, some species can change their flight speeds in still air by more than threefold (Bruderer & Boldt, 2001), with wind effects adding further variation. And as birds change their speed and type of flight, their power requirements change accordingly. Within species, the relationship between power requirement and flight speed in flapping flight is not linear, but U-shaped (Figure 3.1). There is a particular speed at which the power required for flight is minimal (Vmp), and flying either slower or faster than Vmp is more costly (Pennycuick, 1969, 1975). This may explain why birds on migration do not usually fly at the maximum speed of which they are capable: full speed is too expensive. Birds are likely to fly either at the “minimal power speed” (Vmp), which gives minimal rate of fuel use and hence maximum time airborne, or at the somewhat faster “maximum range speed” (Vmr), which gives the longest distance on a given amount of fuel. These two speeds span the most economical range of flight speeds for converting fuel into distance. On migration, birds are likely to fly faster than Vmr only in special circumstances, such as when countering a headwind or falcon attack, or in attempting to reach land as soon as possible (Vmt, flight on minimum time or “full speed”). Using various methods, the U-shaped power-speed relationship has been demonstrated in a range of different birds, but the exact shape and depth of the U varies between species (Tobalske et al., 2003; Askew & Ellerby, 2007; Alerstam, 2011). On any form of U, very slow and very fast speeds inevitably require more power (energy per unit time). Comparing species, the theoretical Vmr, roughly doubles for every 100-fold increase in body mass up to around 15 20 kg, the approximate weight limit for flying birds. This generalization is based on theoretical values, however, and

Power required to fly

A Ph

B

Pm

Vmp

Vmr Air speed (Va)

FIGURE 3.1 The energy costs of level flight within species in still air are expressed by the U-shaped power curve. At very low or very fast speeds, the energy required for flight is greater than at intermediate speeds. At low flight speeds costs are high because the wings are held at a high angle relative to the air flow which increases the drag (called “induced drag”). At high flight speeds, costs are high because of raised friction between the bird’s body and the surrounding air, which also increases drag (called parasitic drag). Vmp is the speed that requires minimum power, which minimizes energy cost per unit time; Vmr is the speed that gives the maximum range, which minimizes the energy costs per unit distance covered. It is found by drawing a tangent from the zero point to the power curve, and could be adopted by birds maximizing the distance flown in a migratory flight with a certain amount of fuel; Pm is the minimum power requirement for flight; and Ph is the power required for true hovering flight with zero speed in still air. Lines A and B indicate two species with different maximum power available for flight. Modified from Pennycuick (1969) and Kerlinger (1989). The power requirement on the y axis can be expressed in either of two ways. A mechanical power curve shows the rate at which the flight muscles must do mechanical work in steady level flight as a function of air speed, while a chemical power curve shows the rate at which chemical fuel energy is consumed. The mechanical power can be calculated directly from the mechanics of flight, and the chemical power is then calculated from the mechanical power (Pennycuick 2009). Hovering, in which a bird can remain suspended in one place in still air, is so energetically expensive (except for hummingbirds) that even small birds use it for only brief periods. Raptors such as kestrels do not hover, although they can fly very slowly (4 6 m per second, Videler et al. 1983). Instead of flying at zero air speed, they fly at zero ground speed, while maintaining a positive air speed. In effect, they face into the wind, and fly forward at the same speed that the wind would otherwise blow them backwards. At very slow air speeds, kestrels flap continuously, whereas at faster speeds (in stronger wind) they incorporate bouts of gliding, in which they appear to hang on the wind.

Migratory flight Chapter | 3

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species of similar weight would be expected to vary in their actual flight speeds, according to body and wing shape and other features of the birds themselves (Alerstam et al., 2007). Hummingbirds, pigeons, ducks and auks fly faster than expected from their body weights, while terns, harriers and owls fly slower. In addition, as air density declines with increasing altitude, under the same power input the flight speeds of birds would be expected to rise with altitude, owing to the reduced drag. The relationship between the actual flight speeds of migrating birds and their mean body weights is shown in Figure 3.2, based on radar studies collated by Bruderer & Boldt (2001). These measured flight speeds give broad agreement with Vmr values predicted from body weight. However, the actual slope of the relationship found in studies of this type varies somewhat according to the species included, as variations in wing shape and other features exert their influence (Rayner, 1988; Bruderer & Boldt, 2001). In general, though, small birds fly slightly faster than expected on theoretical grounds, while large birds fly somewhat slower (Welham, 1994; Alerstam et al., 2007), and birds from the same phylogenetic group, which tend to have similar body and wing shapes, tend to fly at similar characteristic speeds (Figure 3.3).

Wing shape Wing design varies greatly between different kinds of birds long-and-thin or short-and-broad according to the various selection pressures that act upon it (Rayner, 1985). Wing size is usually described in terms of wing-loading (body weight divided by wing area), while wing shape is described by aspect-ratio (wing span squared divided by wing area), which varies from about 5 in grouse to more than 20 in albatrosses. Both measures depend on wing area, which is taken as the area of both wings, including the body between them, projected on a flat surface. Both minimum power speed (Vmp) and maximum range speed (Vmr) increase with body weight and wing-loading, because higher speeds become necessary to generate enough lift to support body weight. Also, both speeds decrease slightly as aspect-ratio rises because longer wings are more aerodynamically efficient. Those birds that fly slowly or hover while foraging, such as terns and harriers, typically have long, high aspect-ratio wings, which reduces Vmp and Vmr, and also the power needed to fly at those speeds and the maximum speed possible. In contrast, divers, ducks, geese and auks have relatively short, high-aspect-ratio wings, which allow high speeds without unduly high power. Many small passerines have short, rounded wings of large area and low aspect ratio. Their low wing-loading permits a large increase in weight (through fuel deposition) prior to migration without flight becoming impossible. More extreme wing designs, as in swifts or hummingbirds, are associated with specialized lifestyles, and may limit flight flexibility in other respects.

Power requirements in relation to body weight Using standard aerodynamic models, theoretical relationships between power requirement and flight speed have been calculated for birds over a wide range of body weights. The power (P) required for flight at Vmr increases with body weight (W) roughly according to the relationship P 5 W1.17 (Pennycuick, 1975). However, because larger birds have lower metabolic rates (in the proportion Mass0.75), flight at Vmr is disproportionately more costly for larger birds (up to the weight of obligatory flightlessness). In other words, the chemical power required to fly at Vmr (or Vmp) is greater in relation to basal metabolic rate (BMR) in larger than in smaller birds, accepting other influences such as wing-shape. (Note: Basal metabolic rate is the rate of energy consumption by an inactive bird, not requiring extra energy for growth, food-digestion or thermoregulation.) The actual relationship between metabolic power needed for flight and body mass has been calculated for a number of birds flown in wind tunnels, as shown in Figure 3.4 (Hedenstro¨m, 2010). FIGURE 3.2 Relationship between flight speed (m/s) and body mass in birds that fly primarily by flapping flight. Flight speed measured from visually identified individuals in level flight, followed on migration with highprecision tracking radar. Body weights were taken as likely averages for each species. Flight speeds were corrected to allow for wind effects (according to radio-tracked wind-measuring balloons) and altitude (with birds flying faster in thinner air), all measures being corrected to expected still-air sealevel equivalents. Speed 5 5.1 1 2.97 x body mass, r2 5 0.415, P , 0.001, N 5 77. Data from Bruderer & Boldt (2001).

22.5

Flight speed

20.0 17.5 15.0 12.5 10.0 7.5 5.0 10

100 1000 Body mass (g)

10000

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The Migration Ecology of Birds

FIGURE 3.3 Bird flight speeds (Ue; m/s) plotted in relation to body mass (kg) and wing loading (N/m2) for 138 species of six main monophyletic groups, all of which travel by flapping flight. Speeds are corrected for flight altitudes to sea-level air densities. The lines show the scaling relationships Ue 5 15.93 x (mass) 0.13 and Ue 5 4.3 x (wing loading) 0.31 as calculated by reduced major axis regression for all species. All axes are in logarithmic scale. Inserts show means ( 6 standard deviations) for the six main phylogenetic groups in relation to these scaling lines. Species of the same group tend to fly at similar speeds, and phylogenetic group is an important factor accounting for variation in flight speed (Ue). From Alerstam et al. (2007).

FIGURE 3.4 Relationship between flight metabolic power consumption at cruising speed and body mass for 21 well-studied bird species from different taxonomic families in which flight metabolic rate was measured in laboratory conditions (mainly in wind tunnels). Power consumption in flight is the fuel consumption measured as energy per unit of time (Watts). The relationship between power (y-axis) and body mass (x-axis) in this sample of birds was y 5 53.650.74, r2 5 0.94. Modified from Hedenstro¨m (2010).

1000

Power (W)

100

10 R2 = 0.96 P < 0.001 1 0.001

0.01

0.1 Body mass (kg)

1

10

Effects of migratory fattening One consequence of this body-weight power relationship is that small birds have more power available to them than do large birds, relative to that required to fly (Pennycuick, 1969). This in turn means that, in relative terms, smaller species can carry more extra fuel for migration (Hedenstro¨m, 1993). Larger birds become progressively more restricted in

Migratory flight Chapter | 3

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the proportion of extra weight they can carry which, despite their greater speed, reduces their potential nonstop flight range. The proportionate weight of fuel that can be carried by a bird at maximum range speed (Vmr) has been estimated to decrease linearly with increasing body size, down to none at about 6 kg of fat-free weight. Bigger birds carrying fuel reserves would have to fly at speeds less than Vmr. For example, the observed flight speed of migrating swans is around 64 72 km per hour, which is substantially lower than their Vmr (Klaassen et al., 2004). In contrast, species with a fatfree body mass less than 750 g can theoretically double their weight through fuel deposition and still have sufficient power to fly at Vmr. From the foregoing, the accumulation of fuel reserves by individual birds must automatically increase their Vmr and Vmp, which vary in direct proportion to the square root of body mass (Pennycuick, 1969). Hence, the maximum fuel load in long-distance migrants provides the necessary energy, but it also obliges the birds to fly at higher speed if they are to achieve maximum range. This effect is not trivial. A bird doubling its lean body mass through fuel deposition (as some do) should theoretically increase its Vmr at the start of the flight by about 1.4 times. However, to achieve this, power output must be increased about 2.8 times at the start of the flight, according to calculations by Pennycuick (1969). Muscle growth is one way in which increased power output could be achieved, but there are clearly limits to this. During a long flight in which mass declines through fuel consumption, theoretical Vmr and Vmp also decline, so the bird would be expected progressively to reduce its cruising speed (and power output) if it is to achieve the maximum range possible. Reduction of flight speed during migration has been confirmed in radio-tracked Brent Geese Branta bernicla (Green & Alerstam, 2000). However, maximum range could be achieved only if birds flew at an appropriate Vmr throughout the flight. They are unlikely to manage this with a heavy fuel load, because this would require exceptionally hard work, and excessive demands on the heart and lungs early in the flight. We might expect, though, that birds would fly at Vmr for as much of the flight as possible, reducing their speed as body weight declined. In addition, all theoretical flight speeds (including Vmp and Vmr) are expected to increase with increasing altitude, owing to reduced air density. A bird the size of a thrush has been calculated to have a Vmp of 35.3 km per hour at sea level, which would increase to 45.4 km per hour at 5000 m (although it is not known for certain that thrushes ever do fly at such high altitude). Actually the bird must fly faster at higher altitude if it is to fly at all. It has to generate the same forces as before to support its weight and propel itself forward, but because the air is thinner at higher altitude, the bird is forced to fly faster to compensate. Adjustments could include higher frequency or amplitude of wingbeats, both of which could raise the heart rate and metabolic cost of flight (Bishop et al., 2015). Other studies have measured an increase in the airspeed of migrating birds with increasing flight altitude (and decreasing air density) and also an increase in wingbeat frequency with decreasing air density (Schmaljohann & Liechti, 2009). Because the power needed to fly declines during long flights, as a result of weight loss due to fuel consumption, one might expect either that muscle mass would decline during a long flight or that reduced power output would be expressed as reduced wing flapping. Several studies have confirmed a reduction in muscle mass during flight (Chapter 5), and others have shown decreasing metabolic rate during flight (reflecting declining power output). For example, Barnacle Geese were tracked between Svalbard and Scotland in autumn using satellite transmitters and dataloggers recording heartbeat as an index of metabolic rate (Butler et al., 1998). During the 2500 km journey, heartbeats declined by 29% from 315 to 225 per minute, reflecting a decline in estimated metabolic rate from 104 to 74 W, and paralleling a loss in mean body mass from 2.30 kg at the start of migration to 1.83 kg at the end. Reduction in energy consumption during flight has also been documented in the Northern Bald Ibis Geronticus eremite (Figure 3.5).

Ascending Migration often involves birds ascending to high altitudes. In birds tracked from take-off by radar, climb rate declined with increasing body weight, from more than 2 m per second in a 50-g Dunlin Calidris alpina to 0.32 m per second in a 10-kg Mute Swan Cygnus olor (Hedenstro¨m & Alerstam, 1992). This constraint of reduced climb rate in large birds could be important as they ascend to reach their flying altitude or to cross mountain ranges. Climb rates of Bar-headed Geese Anser indicus and Ruddy Shelducks Tadorna ferruginea crossing the Himalayas have been recorded at 0.6 and 0.74 m per second respectively, well within the predicted range (Chapter 6). The high cost of climbing in large birds that use flapping flight, and the high rates of heart beat required, may be one reason why swans usually fly at relatively low altitudes, even though winds may often be more favourable higher up. For Bewick’s Swans Cygnus columbianus bewickii tracked on migration mainly overland, mean flight altitude was only 165 m (maximum 759 m, Klaassen et al., 2004) and for Whooper Swans Cygnus cygnus migrating over water, mean flight altitude was 228 m (range 68 387 m, although one individual reached 1,856 m, Pennycuick et al., 1999).

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The Migration Ecology of Birds

FIGURE 3.5 Energy expenditure during migratory flight of Northern Bald Ibis Geronticus eremite which travels by continuous flapping. A. Mean ( 6 SD) energy expenditure (kJ/ h) during rest and during flight. B. Relationship between flight energy expenditure EE (kJ/h) and flight duration. From Bairlein et al., 2015.

These altitudes are low compared with those attained by smaller birds, which are typically above 1500 m (Chapter 4). Moreover, after taking off over land, Whooper Swans did not usually exceed 500 m altitude until they had flown for more than 50 km, indicating an extremely slow mean rate of climb (Pennycuick et al., 1999). Probably, their power production in level cruising flight near the start of migration, with heavy fuel reserves, was close to the maximum possible.

Descending For obvious reasons, with help from gravity, the descent of birds at the end of a migratory journey can occur much more rapidly and cheaply than the climb. Birds do not always lose height steadily, but instead some drop almost vertically from high altitude into habitat below, as described long ago on Heligoland Island by Ga¨tke (1895). Similarly, on Cyprus small nocturnal migrants were seen to “drop like stones from the sky at first light and immediately dive into cover” (Bourne, 1959); while on the Louisiana coast in spring, migrant passerines were seen to dive nearly vertically down from more than one kilometre, producing “a whizzing sound as they pulled out of the dive just above the trees” (Gauthreaux, 1972). Such “fallout” also occurs in other circumstances, such as when migrating birds are confronted by a sudden headwind or downpour, and literally drop from the sky to seek refuge. Thousands of birds seem to come from nowhere, ladening trees and bushes or carpeting the ground, presenting an amazing spectacle to any onlooker. One well-known fallout site comprises five hectares of trees at the small town of High Island, on the open coastal plain of Texas, which every spring attracts hundreds of birders keen to witness the spectacle, as birds arrive from their transgulf flight. Geese have a particular form of flight, called “whiffling,” through which they lose height rapidly when over their destination, and this behaviour is seen daily as geese return to their winter night-roosts.

Effects of wind conditions For any flying bird, wind conditions have a big effect on travel speed, and hence on flight times and associated energy expenditure. Wind can be imagined as a large body of air moving at some specific speed (Vw) in a particular direction. The bird is embedded in this moving air, and flies at a speed relative to the air: its air speed (Va). The bird’s speed and direction with respect to the ground represent the net result of its own direction and still-air flight speed and the prevailing direction and speed of the wind. If the wind blows in the same direction as the bird is heading (tailwind), the bird’s theoretical ground speed is Va 1 Vw, whereas if the wind is in the opposite direction (headwind), the bird’s theoretical ground speed is Va Vw. If the wind blows at some angle to the bird’s intended path, the bird could be blown off-course (Figure 3.6). Or alternatively, the bird could allow for this side-wind by adjusting its heading in such a way that the net effect of bird direction and wind direction compensate for one another and thereby keep the bird on track with respect to the ground (Chapter 4). Headwinds of a given speed have much more effect on the flight range of slow-flying (5small) birds than of fast-flying (5large) ones. Against a headwind of 10 m per second (36 km per hour), small

Migratory flight Chapter | 3

FIGURE 3.6 Diagram showing relationships between heading (H, the direction the bird faces), the wind direction (W), and the track (T, direction the bird travels on a journey from A to B). The track vector (T) is the sum of the heading (H) and wind (W) vectors. The angle (α) between track and heading depicts the amount of drift with constant heading, while the angle (β) shows the wind direction in relation to the track direction.

α T

35

H

β

Power required to fly

W

0

0 VW

Vmr(W) Vmr(O) Bird air speed

0 Bird ground speed

FIGURE 3.7 Flight speed in relation to power requirement in different wind conditions. The “power curve” is U-shaped, so that the maximum range on a given fuel reserve will come near the bottom of the power curve (Figure 3.1). It will not come at the very bottom because the slight increase in power needed to fly faster is compensated by the extra length of journey achieved. The best possible speed for cruising is given by the longest tangent from the power curve which passes through the origin (Vm(0)) in still air. The graph shows the situation in still air. However, with a wind blowing, the graph would need to be altered to take into account the real distance over the ground achieved by the bird. This can be done by shifting the origin of the graph to the left if the bird is being helped by a tailwind (Vw) and to the right if the bird is being hindered by a headwind. The resulting tangents, giving the best speed for the maximum range, show that the bird should fly slower with a tailwind (Vmr(W)) and faster against a headwind, compared to the maximum range speed in still air (Vmr(0)). In practice, the amount by which the best speed is varied turns out to be much less than the wind speed encountered. The effect of headwinds and tailwinds will be much greater on slower-flying than faster-flying species which in general have high Vmr. From Pennycuick (1972).

passerines would make no significant progress, while larger migrants could make some progress, but have their still-air flight range reduced to less than half. The important point is that, because large birds fly faster, they can migrate in more adverse wind conditions than small ones, but at a cost in energy terms. Because birds are slowed by headwinds, their ability to complete a journey depends on the amount of fuel they are carrying. Loss of flight range caused by a headwind cannot be prevented, but it can be reduced by flying somewhat faster than Vmr if sufficient power is available. Small birds are better off than large ones in this respect, on account of their greater power margin, which gives greater endurance. This is of special importance for landbirds blown out to sea, when they may be better off slowing down to Vmp to conserve energy and thereby remain airborne as long as possible on the chance of reaching land. In fact, the best strategy for a bird attempting to achieve maximum range would be to fly slower with a tailwind and faster against a headwind (Figure 3.7). Such adjustments have been shown to occur (Liechti, 2006; Alerstam & Gudmundsson, 1999a,b; Hedenstro¨m et al., 2005). For example, the ground speed of night migrants tracked by radar increased with a tailwind, but less than expected (3 4 knots for a 10-knot increase in tailwind) (Bellrose, 1967). In this case, the birds were exploiting wind assistance, but not to the maximum extent possible at Vmr. They were instead minimizing energy expenditure, and at the same time making a gain in flight range of 30% 40% (see also Chapter 4).

Cutting the costs of flight In their migratory flights, birds are often found to perform better than predicted by simple aerodynamic models. This is mainly because birds have various ways of reducing the costs of flight. Their bodies are much more flexible than those

36

The Migration Ecology of Birds

of airplanes, around which aerodynamic theory was developed. Birds can also change the shape of their wings and tail, altering their body outline and lift-to-drag ratio to suit the circumstances; and some can also switch between powered flapping flight and still-wing gliding. In addition, many small birds do not flap continuously during migration but adopt a slightly undulating flight, rising while flapping and dipping on closed or half-closed wings to reduce the drag. Combined with residual lift, bounding flight gives greater distance for a given fuel cost, and allows many small birds to fly faster than they otherwise could (Bruderer & Boldt, 2001). It is also physiologically advantageous, as it gives brief rest times between bouts of flapping (Rayner, 1985). Bounding flight is shown by many passerines, woodpeckers and small owls, among others, and the dipping part of the flight becomes relatively longer the larger the bird. Energy savings of 10% 15% have been estimated. Another way in which some large birds cut their fuel costs is by flying in line or V-formation. This is usual among geese, swans, gulls, cranes, ibises, pelicans, cormorants and others. Each individual flies behind and to the side of the one in front, benefiting from its slipstream, gaining lift and reduced drag (Rayner, 1979). A study of Northern Ibises revealed exactly how this is achieved (Portugal et al., 2014). As a moving bird flaps, it pushes air downward beneath its wings, but as the air squeezes around the outside of the wings, it creates an updraft at the wingtips. A bird flying behind positions its own wingtip in the updraft from the bird in front, and also times its wing beats perfectly to gain the greatest lift from the bird ahead. The individual at the apex of a formation has no such advantage, and frequently changes position, pulling out and joining the line further back. Estimates of energy savings for individual birds flying in V-formation lie in the range of 12% 20%, compared with birds flying alone (Alerstam, 1990; Cutts & Speakman, 1994; Weimerskirch et al., 2001; Maeng et al., 2013). Other birds migrate in flocks of other shapes, but again may save on energy costs. Probably for this reason, Red Knots Calidris canutus and Dunlins followed by radar flew about 5 km per hour faster in flocks than solitarily (Alerstam, 1990). A further means by which some large birds reduce their fuel costs is by passive soaring and gliding on outstretched wings, making use of natural updrafts to climb and remain aloft, and thereby saving energy. Natural updrafts are mainly produced by thermals columns of rising air caused by uneven heating of the ground or by horizontal winds being deflected upwards by slopes and cliffs (“orographic lift,” Chapter 7). Cranes usually fly in V-formation by flapping flight, but may switch to soaring-gliding where conditions permit. The flight mode adopted by different bird species is influenced by their wing-loading; that is, their weight relative to wing area. The heavier the bird, the more difficulty it has in creating lift for flapping flight by muscle power alone, and the relatively greater is the energy saving from switching from flapping to soaring. This may be one reason why soaring-gliding flight is seen mainly in large birds, such as eagles and pelicans (Pennycuick, 1975), and it is perhaps surprising that some other large species, such as geese and swans, migrate entirely by flapping (except in unusual circumstances, Klaassen et al., 2004). However, these large waterfowl migrate mainly in regions where thermals are weak at migration times, and their flock formations provide other ways of reducing energy costs. Even small birds, such as warblers, could save energy by soaring if they had the right wing structure, but they would then travel only very slowly (less than half their flapping speed). Beeeaters may be the smallest birds that regularly travel by a combination of soaring and flapping flight. Moreover, the thermal convection that allows soaring is usually available for only part of each day, and by restricting the daily migration time for soaring flight, assuming time is important, the body size favouring soaring shifts even more towards larger sizes (Hedenstro¨m, 1993). Nevertheless, rising air currents could benefit all birds, not just soaring species, and may be of special value to species that travel long distances over hot deserts. It is not, of course, necessary for an air current to be strictly vertical to permit soaring, so long as the vertical component exceeds the bird’s own rate of sink. From measures of energy consumption in flying birds, the costs of flapping and soaring flight can be compared. These costs are usually expressed in relation to basal metabolic rate (BMR). Flapping flight typically leads to a sevenfold increase in metabolic rate above basal level (BMR) in a resting bird (Norberg, 1996), but as mentioned above, the muscular power required for flapping flight increases steeply with body mass. In comparison, the energetic cost of soaring and gliding is expected to be low (theoretically about 1.56 x BMR, Norberg, 1996), and varies little with body mass, giving a roughly 4 fivefold difference between these two flight modes. Actual measurements suggest considerable variation between species, not least because the costs of flapping flight rise with body size, as mentioned previously. Among the species listed in Table 3.1, the measured costs of flapping flight ranged from about 5 to 25 x BMR, compared with 1.3 to 2.2 x BMR for soaring gliding flight. The average values for the flapping and soaring species in Table 3.1 were 9.3 x BMR and 1.7 x BMR respectively, a roughly similar difference to that estimated by Norberg (1996).

CONSEQUENCES OF FLAPPING AND SOARING FLIGHT In steady flapping flight, a bird must generate the forces which support its weight against gravity, and which provide the forward thrust necessary to overcome friction with the air. The power for both the lift and forward thrust is supplied

Migratory flight Chapter | 3

37

TABLE 3.1 Relative energy costs of flight, expressed as energy consumed during flight/energy consumed at rest (xBMR, basal metabolic rate)a. Body mass (g)

Methodb

xBMR

Source

Black-necked Grebe Podiceps nigricollis

389

ML

25.2

Jehl et al. (2003)

Greater White-fronted Goose Anser albifrons

2600

HR

5.0

Ely et al. (1999)

Barnacle Goose Branta leucopsis

1700

HR

4.8

Butler et al. (2000)

Species Powered flight

d

Great Cormorant Phalacrocorax carbo

2750

Various

6.0

Gre´millet & Wilson (1999)

Northern Bald Ibis Geronticus eremite

1200

DWL

7.7

Bairlein et al. (2015)

Common Kestrel Falco tinnunculus

213

DWL

16.2

Massman & Klaassen (1987)

Bar-tailed Godwit Limosa lapponica

282

ML

8.0

Piersma & Jukema (1990)

Laughing Gull Leucophaeus atricilla

322

WT

11.9

Tucker (1972)

Ring-billed Gull Larus delawarensis

427

WT

7.5

Berger et al. (1970)

Herring Gull Larus argentatus

950

HR

4.8

Kanwisher et al. (1978)

Sooty Tern Sterna fuscata

187

DWL

4.8

Flint & Nagy (1984)

Domestic Pigeon Columba livia

384

DWL

8.0

LeFevre (1964)

Domestic Pigeon Columba livia

435

HR

6.0

Butler et al. (1977)

Thick-billed Murre Uria lomvia

900

ML

12.5

Croll et al. (1991)

White-necked Raven Corvus cryptoleucus

480

WT

14.0

Hudson & Bernstein (1983)

Swainson’s Thrush Catharus ustulatus

30

DLW

5.2

Wikelski et al. (2003)

Herring Gull Larus argentatus

950

WT

1.5 2.2

Baudinette & Schmidt-Nielsen (1974)

Wandering Albatross Diomedia exulans

7000

HR

1.3

Weimerskirch et al. (2000)

Black-brown Albatross Thalassarche melanophrys

3200

HR

2.0

Bevan et al. (1995)

Griffon Vulture Gyps fulvus

7500

HR

1.4

Duriez et al. (2014)

55

HR

2.0

Sapir et al. (2010)

Soaring-gliding flight

c

Bee-eater Merops apiaster

BMR 5 metabolic rate of a bird of that species at rest in a post-absorptive state. DWR- doubly labelled water technique, HR—Heart rate, a proxy for energy expenditure, ML - mass loss, appropriate proportions of fat and protein, WT— wind tunnel. Some of the measures were from birds in wind tunnels or other short flights on which energy consumption is often higher per unit time, on average, than on long migratory flights. This is partly because the proportion of the flight involving energy-demanding take-off and climbing is greater on short flights than long ones. c A mixture of soaring-gliding and flapping flight. d Calculated from figures given in Table 3 of Gre´millet & Wilson, 1999 for resting and flying.Other estimates of the costs of flapping flight are summarized by Norberg (1996) and Hedenstro¨m (2008), but not in terms of BMR. a

b

by the breast muscles, while directional control is provided mainly by the tail. Given sufficient fuel reserves, some birds that migrate by continuous flapping flight (such as waterfowl and waders) can travel for hours or days on end. They can cross water or other hostile terrain, and can fly by night as well as by day. In moving between their breeding and wintering places, therefore, such birds often travel directly, taking the shortest routes (except in unfavourable conditions). As populations, they migrate mostly on a broad front, but concentrate to some extent through mountain passes or along coasts or other “leading-lines” that deviate little from their main direction. Because flapping flight is expensive, however, such species must normally lay down substantial body reserves, especially for travelling over large areas of sea or other inhospitable substrate where they cannot feed. Sustained flapping also produces heat, which may enable birds to fly at high latitudes and altitudes without having to burn extra fuel to keep warm. In hot conditions, however, heat production can result in the need for evaporative cooling (panting), which increases water loss and dehydration

38

The Migration Ecology of Birds

risk. Birds can lessen the risk of over-heating by flying high where the air is cooler, and also by flying at night when the air is cooler still. The situation differs somewhat in birds that migrate mainly by soaring gliding flight, notably the broad-winged raptors, storks and pelicans, which gain most of the energy they need for flight from the ambient atmosphere. Typically, these birds circle upwards in a thermal, then glide with loss of height to the next thermal and rise again; they repeat this process again and again along the migration route, and over long distances in ideal conditions they seldom need to flap their wings (Figure 3.8; Chapter 7). Because the lift comes largely from rising air currents and the forward motion partly from gravity, this still-wing flight mode requires much less internally generated energy than continuous flapping (typically 0.3 2.2 x BMR versus around 5 25 x BMR, Table 3.1). Many soaring species use a mix of gliding and powered flight, but seek to maximize the contribution from gliding. The extreme soaring species thus depend for their migrations mainly on a source of energy external to their own bodies, and unlike flapping birds, soaring species can continually correct for the effects of cross-winds without wasting energy. Soaring gliding flight has other consequences. Because soaring birds travel mostly on still, outwardly stretched wings, they produce less heat than species that continuously flap their wings. In cold climates this could increase the energy needs for heating the body, but in hot climates it reduces the likelihood of over-heating, and the resulting water needs for cooling. Moreover, because of their dependence on updrafts, soaring land-bird species must migrate mainly over land, favouring routes where appropriate conditions develop. They are also constrained to travel by day when the sun heats the land surface, creating rising air currents. Their migration typically reaches its peak, and moves most rapidly, in the middle part of each day when thermal activity is greatest (Chapter 7). It is then that soaring birds travelling through lowland achieve the greatest heights, and can make the longest and fastest glides across country (Spaar, 1997; Spaar & Bruderer, 1996). Soaring landbirds also tend to concentrate along narrow land bridges (such as Panama), or at narrow sea crossings (such as Gibraltar), and thereby avoid spending long periods over water where thermal soaring is less often feasible (Chapter 7). They therefore usually take long roundabout routes between breeding and wintering areas in order to make as much of the journey as possible over land, and minimize the distance travelled by expensive flapping flight. Despite the greater distances, their total energy consumption is thereby greatly reduced, compared with same-sized species that travel by flapping flight. Soaring species produce spectacular concentrations, as birds from large parts of a breeding or wintering range funnel through well-known bottlenecks, including those just mentioned. Moreover, because their travel routes are determined by geography and topography, they tend to take the same traditional narrow-front “corridor” routes year after year (Chapter 7). Whereas in flapping flight a bird replenishes its energy reserves by feeding to accumulate fuel during stopovers, in soaring gliding flight, a bird replenishes its “potential energy” by climbing in thermals or other updrafts. It rapidly loses this potential energy as it glides across country, gradually losing height. The faster the rate of climb in updrafts, the less the time lost in regaining height, and the higher the average cross-country speed. The rate of climb that can be achieved depends mainly on the strength of the updrafts, with smaller birds having a minor advantage in most conditions. An average rate of climb of 0.5 m per second would represent weak soaring conditions, 2 3 m per second would be typical of good conditions, while 5 m per second is not unusual in individual thermals, but would seldom be sustained as an average. FIGURE 3.8 Soaring gliding bird migration, indicating soaring within thermals, gaining height, and gliding between thermals, losing height. Thermals are often topped with cumulus clouds.

Migratory flight Chapter | 3

39

Body weight has interesting effects on overland soaring gliding migration (Pennycuick, 1975). Compared with small soaring species, large ones (with greater wing-loading) have to start later in the day, when thermals are strong enough to lift them; they also tend to rise more slowly, mainly because their turning radius is greater, so they spend more time near the edges of thermals where air currents are weaker than in the centre. But having reached the top of a thermal, they then glide more rapidly across country than smaller species, their greater weight adding speed along a given gliding angle. They nevertheless have some control over gliding speed, and may slow down if necessary (Horvitz et al., 2014). The starting height and glide angle determine the distance that a bird can glide before it needs to climb again. The overall cross-country speed of soaring gliding birds therefore depends partly on their body weight (or more strictly wing-loading), partly on aerodynamic design, and partly on the strength and height of thermals. In general, smaller species rise faster within thermals, but travel more slowly between them than larger species, and being able to make use of weaker thermals, small species can travel for longer each day. Studies support theoretical predictions that soaring flight gives higher migration speeds than flapping flight in bigger species (Hedenstro¨m, 1993; Hedenstro¨m & Alerstam, 1998). This is largely because soaring species consume less energy (relative to body mass), so have to spend less time replenishing their body reserves during the journey. Soaring landbirds migrating on the strength of updrafts produced by winds striking mountain slopes are less constrained than those using thermals because they can migrate for longer each day. Some of the best known concentration points for soaring raptors are in mountain areas, such as the well-known “Hawk Mountain” in Pennsylvania (Chapter 7). Devices attached to the world’s heaviest soaring bird, the Andean Condor Vultur gryphus, measured the frequency of wing-flaps, and hence the extent to which these birds could operate without resorting to powered flight (Williams et al., 2020). In more than 216 hours on the wing, these condors sustained soaring across a wide range of wind and thermal conditions, and flapped their wings for only 1% of the time, mainly associated with take-offs. This gave condors one of the lowest travel costs yet recorded among vertebrates. One bird flew for more than five hours over a distance of 172 km without flapping. This helps to explain how some extinct birds with twice the wingspan of condors could have flown. But soaring gliding flight is not confined to landbirds. Many seabirds make use of up-currents formed as wind is deflected upwards off waves. If a bird turns into this wind, it gains height; it then turns to glide roughly at right angles to the wind direction and therefore parallel to the waves, before turning into the wind to regain height and repeat the process. A bird could also make use of discontinuities in wind flow near the sea surface, as it flies behind a wave crest and then emerges for a time into the unobstructed wind. At this moment, the bird tilts its body so that the temporary gust strikes its underside, providing lift, enabling further onward gliding flight (Pennycuick, 2002). Some seabirds, notably albatrosses and shearwaters, also use “dynamic soaring,” which depends on wind being slowed by friction with the sea surface, an effect which is lessened by height up to about 15 m. The bird first climbs into the wind, then makes a high leeward turn, gaining distance by gliding with the wind whilst losing height. After making a low turn in the trough of a wave, it starts the cycle again (Richardson, 2011; Sachs et al., 2012; Kempton et al., 2022). The track is necessarily zig-zag, which means that albatrosses and similar birds travel much further than on straight line distances. Over most ocean areas, soaring seabirds are normally constrained to fly low over the sea surface, much lower than soaring landbirds dependent on thermals. Strong winds and low energy demand allow soaring seabirds to perform some of the most impressive avian journeys, not only on migration, but also in the breeding season when their prolonged foraging trips may extend over thousands of kilometres (Chapter 8). Thermals are not totally lacking over open sea areas. Over tropical seas, in regions affected by trade-winds, the warm surface water heats the cool wind, leading to thermal formation day and night. Frigatebirds can soar effectively in these weak thermals because they have exceptionally light wing-loading (the lowest of all birds) yet high aspectratio. When away from their nests, Magnificent Frigatebirds Fregata magnificens equipped with satellite transmitters and altimeters remained continuously on the wing (Weimerskirch et al., 2003). Like soaring birds over land, they travelled in a series of climbs and descents, soaring on thermals to heights up to 2500 m and gliding down in the direction of travel. From the heights achieved, they were assumed to spot their prey on the sea surface. Their climb rates in these weak thermals were very slow, averaging only 0.4 m per second, and they travelled forwards extremely slowly, only about 10 km per hour. Their reliance on weak thermals may explain why these birds are restricted to trade-wind zones, where thermal soaring is possible throughout the year. This tracking study also supported an earlier supposition that frigate-birds are unable to settle and take off from the water surface. Soaring flight performance can be analyzed in a similar way to flapping flight, using the relationship between the rate of sink and forward gliding speed to predict the optimal speeds under different conditions (Pennycuick, 1975, 1989). The graph of sinking speed (Vz) against forward speed (Va) is called the “glide polar” (Figure 3.9). It can be

40

The Migration Ecology of Birds

(a)

(b) Air speed (Va)

Vth

Vbg Climbing speed

Vms

0

Forward speed

Vcc

Vopt

Sinking speed

Sink speed (Vz)

Vzm

Vmin

FIGURE 3.9 (a) The glide polar of a gliding bird or sailplane, showing minimum sink speed (Vzm), minimum air speed (Vmin), air speed at best glide ratio (distance covered/loss of height, Vbg), and air speed at minimum sink (Vms). All values are with respect to the air through which the bird flies, and not to the ground. The glide ratio (angle) at any point on the aerodynamic performance curve is equal to a ratio of Va to Vz. The best glide ratio on the glide polar (the maximum ratio of Va to Vz) is determined by drawing a tangent to the curve from the origin. (b) Cross-country speed in thermal soaring. Vth is the achieved rate of climb in thermals and is plotted upward from zero on the same axis as the sinking speed. The optimum speed Vopt at which to glide between thermals is found by drawing a tangent to the polar from Vth. The tangent cuts the speed axis at the average cross-country speed Vcc. The cross-country speed corresponding to some inter-thermal speed other than Vopt can be found by the same construction, but will be less than Vcc. From Pennycuick (1975).

viewed as a type of power curve, in which the power is equal to the sinking speed multiplied by the bird’s body weight. This power comes from the bird’s potential energy (from its height) rather than from the flight muscles. During the glide the bird may close its wings to some extent, thereby reducing drag and increasing speed. In general, a bird sinks faster while travelling at higher air speeds, but the form of the relationship differs between species. As field measurements showed, in each species the maximum glide-ratio (distance covered/height lost) is obtained at a particular air speed, which again differs between species. The maximum glide-ratio of various raptors is around 9 to 15:1, and for albatrosses around 23:1, while the equivalent ratio for sailplanes is typically around 38:1. In other words, from a given starting altitude, sailplanes can reach in a single glide around twice the distance of that achieved by the best gliding birds. This is one of the few instances where, in terms of efficiency, a man-made machine out-performs a bird, although the bird has much greater flexibility in its flight behaviour. Like birds that migrate by flapping flight, soaring species can reduce energy costs by various means. In particular, hawks can adjust their wing and tail shapes to provide more or less surface area. This allows them to exploit a wider range of air speeds and glide ratios than would be possible if these features were constant, and reduce the drag during glides (Kerlinger, 1989). Holding the wings in the level outstretched position would normally consume energy, but some soaring species have anatomical adaptations that allow them to “lock” their wings in place, freeing them from using muscle power for this purpose, and thereby saving fuel. As well as a shoulder lock to hold the wing outstretched, albatrosses and others have a special tendon sheet associated with the pectoralis muscle to prevent the wings from being raised above the horizontal (Meyers & Stakebake, 2005). Albatross flight muscles are also smaller relative to body size than those of flapping birds, especially the supra-coracoideus which is used to raise the wing during an upstroke. With less muscle mass to keep airborne, the gliding albatross saves further energy. In addition, other soaring species typically have part of the pectoralis muscle adapted as a tonic muscle, able to hold the wings out at minimum energy cost (Pennycuick, 1975). Birds that do not soar do not have this divided pectoralis muscle. To summarize this section, migrating birds that travel by flapping flight can normally (1) use prior fat stores to migrate long distances without feeding and, if necessary, without resting; (2) migrate day or night; (3) use direct and short routes; (4) cross large areas of inhospitable substrate without stopping; (5) migrate on a broad front rather than on a well-defined, narrow route; and (6) travel at high altitudes. In contrast, land-bird migrants that travel mainly by soaring and gliding have greatly reduced fuel needs, but over low ground normally (1) migrate only in the warmest part of the day and not at night; (2) avoid large water bodies, and often take roundabout routes with appropriate wind and thermal conditions, thereby increasing the total distance covered; (3) migrate along well-defined and relatively constant

Migratory flight Chapter | 3

41

routes, some of which are taken year after year by most of the population from large areas; and (4) are usually limited in flight altitude above ground by the height reached by thermals (seldom more than 1.5 km at noon overland). Soaring seabirds depend for lift on the action of wind against waves, and usually fly much lower than soaring landbirds. In their dynamic soaring they depend on the gradient in wind speed which is slowest at the level of the waves and increases with rising elevation. They can migrate day and night, wherever wind blows, but albatrosses and other large species are restricted to regions where strong winds occur year-round. Soaring gliding seabirds migrate along particular routes (“wind highways”) that lengthen their journeys, but save on energy costs. Because soaring migrants require less internal energy per distance covered, they could in theory migrate with smaller fat reserves than flapping migrants, and this is supported by what little information is available on the fat levels of soaring landbirds (Chapter 7).

The high performance of some migrating waders Some of the measured rates of energy production during flapping flight are surprisingly high (Table 3.1), with several species reaching production rates more than ten times greater than those measured at rest (as represented by BMR). Most of the flights recorded were short, many in experimental situations such as wind tunnels, where energy inputs may have been high because they included energy involved in start-up and (in wild birds) climbing to cruising height. In birds making long migrations, these activities would have formed a smaller proportion of the total flight. Nevertheless, several shorebird species relying on stored fuel have been found to fly for 6 9 days nonstop at mean rates of energy use 9 10 times higher than BMR (Piersma, 2011). This is another exceptional performance by vertebrate standards. Furthermore, from comparison of pre-flight and post-flight body masses, and calculation of the energy gained from the fat and other tissue metabolized, it emerged that these shorebirds were flying for much longer than previous studies would suggest was possible on the energy expended (Piersma et al., 2022). Different species of long-distance shorebirds lost about 0.41% 0.52% of body weight per hour of flight, compared with losses of 0.56% 1.0% per hour in passerines and other shorebirds making shorter flights, and 2.0% in Ruby-throated Hummingbirds Archilochus colubris crossing the Gulf of Mexico (Hedenstro¨m, 2010). There was no reason to suspect these shorebirds were making use of soaring gliding flight which is unrecorded from shorebirds, so over long-distances these birds may have had some additional advantage in flight efficiency which remains as yet unknown. Nevertheless, estimates of potential flight durations much closer to those recorded were estimated from aerodynamic theory (Pennycuick, 2009), which calculated mechanical power output from physical principles based on body mass, wing design, characteristics of the flight environment, and various assumed parameters (Piersma et al., 2022). The implication was that the physical characteristics of shorebirds themselves, and the way they flew, greatly reduced the rates at which they used their fuel reserves compared with other birds (although probably at the cost of some other ability).

THE ROLE OF BODY SIZE IN BIRD MIGRATION It will be evident by now that body size (and the associated features of metabolic rate, power requirement and flight speed) have a major influence on the flight modes and migration capabilities of birds, with increasing body size bringing increasing restrictions. The power available for flight declines rapidly with increase in body size, and many large birds may have insufficient muscle power or aerobic capacity to fly at Vmr, so are constrained to fly at some slower speed, such as Vmp. Among birds that migrate by flapping flight, the load-carrying capacity decreases with increasing body mass, including the fuel load (Hedenstro¨m & Alerstam, 1992). This constraint in load-carrying is expected to limit the distance that can be flown nonstop by large flapping birds over terrain in which feeding is impossible, although large birds compensate for this to some extent by relatively long wings and by flying more slowly than Vmr (Rayner, 1988). The range a bird can attain on a given fuel load is of special significance in migrants. Large birds are not the best performers in this respect, because they are limited in the fuel they can carry, but nor are small birds, which fly too slowly. Rather some medium-sized birds, notably some shorebirds, can undertake the longest nonstop flights, because they can carry large fuel loads and at the same time fly fast. Both passerines and shorebirds can sustain flapping flight for up to a hundred hours (or more), but because shorebirds fly faster, they can cover greater distances in this time (Chapter 6). These same features may also enable shorebirds to perform better under adverse winds than slower species. The longest apparent nonstop flights recorded for swans reached around 1700 km, for passerines around 3000 km, and for shorebirds around 5000 8000 km, apart from the remarkable 11,000 km flight of Bar-tailed Godwits Limosa lapponica from Alaska to New Zealand (Chapter 6). The longest overall migrations (including stopovers) for swans reached around 3000 km, for geese around 5000 km, and for passerines and waders 12,000 km or more, the latter

42

The Migration Ecology of Birds

covering the distance between the northern parts of the northern continents and the southern parts of the southern ones. Because soaring birds do not need to spend long periods refuelling, they can make longer overall migrations within the same time limits as flapping species of similar body weight. Some Common (Steppe) Buzzards Buteo b. vulpinus migrating between northern Russia and South Africa make journeys of 12,000 km or more, as do Swainson’s Hawks Buteo swainsoni travelling between North and South America. Equally remarkable, the Ruby-throated Hummingbird Archilochus colubris weighs only about 4.8 g, yet regularly crosses the Gulf of Mexico (1100 km) in a nonstop flight of about 18 hours, requiring an estimated 3.2 million wing-beats (Nachtigall, 1993). The range of body sizes found among flying birds spans four orders of magnitude, from the smallest hummingbirds of about 1.5 g to the largest flying species of around 15 kg, such as bustards, pelicans, swans, condors, vultures and albatrosses. Large flying birds become increasingly likely to adopt less strenuous flight modes, such as gliding or formation flying, until at some undefined weight, flight becomes impossible. Flightless birds can be much heavier than flying species, reaching 35 kg in penguins and 150 kg in Ostriches Struthio camelus, while some extinct flightless birds probably reached 400 kg.

MIGRATION BY WALKING OR SWIMMING While most birds migrate by flight, some migrate by walking or swimming. These include not only flightless birds, but also some birds which are able to fly, but in some circumstances opt to walk or swim instead, for at least part of their journey. For example, a pedestrian migration of American Coots Fulica americana occurred in the Warner Valley of Oregon during May 1929 (Prill, 1931). At least 10,000 individuals were seen walking northward over a period of four days. They did not swim or fly (unless alarmed), but followed the shore, 6 25 abreast. They may have been engaged in a moult migration, and some may not have flown because their flight feathers were loosened or already shed. In western North America, the Dusky Grouse Dendragapus obscurus and Mountain Quail Oreortyx pictus perform altitudinal migrations, moving several hundred metres up and down mountainsides between breeding and nonbreeding areas, primarily on foot, despite being able to fly (Cade & Hoffman, 1993; Gutie´rrez & Delehanty, 2020). In flightless landbirds, such as ratites, all movement is inevitably by walking or running. Emus Dromaius novaehollandiae in central Australia have been found to cover hundreds of kilometres at times of drought, with a mean speed of 13.5 km per day (Marchant & Higgins, 1990). Having lost the power of flight, penguins perform regular migrations by swimming, some of more than 1000 km. They are well streamlined and, using their flippers to “fly under water,” penguins can travel at relatively high speeds, larger species faster than smaller ones. Large King Penguins Aptenodytes patagonicus were filmed swimming in an aquarium at 3.4 m per second (more than 12 km per hour). Although penguins can float and swim at the surface, they apparently undertake long sea journeys mainly under water, where the drag on the body is less than on the surface, but they have to come up frequently for air. As they approach the surface, the drag on the body increases, and it has been suggested that leaping clear of the water (porpoising) is energetically less costly than surfacing, and is supposedly undertaken to maintain speed while breathing. Some other seabirds that are normally able to fly, such as auks, may migrate entirely or partly by swimming, remaining in suitable habitat throughout. Young auks have been found to travel by paddling at 40 km per day (Gaston, 1983). The extinct flightless Great Auk Pinquinus impennis, which nested at high latitudes, was a long-distance swimming migrant, wintering in the western Atlantic as far south as Florida and in the east Atlantic south to the Mediterranean, probably involving journeys exceeding 1500 km (Brown, 1985).

SOCIAL FACTORS Many birds migrate in flocks. Individuals take off together and probably many remain together for the flight, but not necessarily for the next stage of the journey. Frequent calling, especially at night or in mist, may help to maintain flock cohesion and direction. It may also induce grounded birds in appropriate condition to join the passing stream (Box 3.1). In caged Bobolinks Dolichonyx oryzivoru, nocturnal call notes, recorded and played back, increased the nocturnal restlessness of birds in migratory condition (Hamilton, 1962). As sound production requires energy at a time when energy use is paramount, we can assume that vocalizations are important in migration, enabling ongoing contact between individuals, whether in obvious flocks or more spaced out. Flocking or other contact during migration may improve navigation through the collective efforts of individuals (Chapter 11); it may also facilitate the search for resources such as food supplies or supportive wind conditions, and give more effective detection and evasion of predators (Flack et al., 2022). In all these respects, naı¨ve juveniles may benefit more from social contact than experienced adults.

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BOX 3.1 Social influences and migration waves among Common Chaffinches. At the Courland Spit on the Baltic coast, Common Chaffinches Fringilla coelebs were collected at different stages of a migratory wave and their carcasses were examined to determine the fat content and amount of food in the gut. These findings were then related to the volume of migration, and a remarkable and consistent pattern emerged. Throughout the migration season, wave after wave of migrants passed through the area. On the first day of each wave only very fat birds flew: they began their movement around sunrise, without feeding beforehand, and continued for about 4 hours. There was then a pause of 1 3 hours, after which the movement was resumed and continued for two hours in the evening. On the second day, the volume of migration reached a peak; again the movement began at sunrise and at first only fat birds flew. As the day progressed, however, the migrating flocks contained increasing numbers of lean birds which, unlike the fat ones, usually had fresh food in their stomachs. This implied that lean birds began their flight later in the day than fat ones and after feeding. During the day the lean birds stopped to feed again: at the same time they attracted down some fat birds, although on this day the latter did not normally feed. By the afternoon, all the lean birds had stopped to feed, and in the evening fat birds were the only ones left flying. On the last day of the wave the migration did not begin at sunrise but only after the birds had fed. Fewer birds participated; they flew with frequent stops and at lower altitude. On this day, almost all the flying birds contained little fat, some feeding occurred throughout the day, and no minor peak in movement occurred in the evening. Some flocks flew in the reverse direction. Each migratory wave usually lasted three days, but varied from one to seven. After it was over, the pause usually lasted three days, but varied from one to eight, depending partly on the weather. During each migratory wave, birds were estimated to cover up to 500 km, in which time individuals expended 2 3 g of fat. Together with stopping time, this amounted to about 500 km per six days, which was consistent with the migratory progress of Chaffinches recorded from ring recoveries (Chapter 9). No sex or age differences were noted among the birds caught on different days of a wave. In their explanation of this pattern, Dolnik & Blyumental (1967) attached great importance to the apparent pull that flying birds had on others which at that time were physiologically less ready to migrate. Since the first birds to fly were the very fat ones, it was presumably the presence of many fat birds, which started to fly under a common stimulus (such as favourable weather) that began each wave. Once started, however, the stream of flying birds stimulated others to join, and the larger the overhead stream the greater the pull. The expenditure of fat by the fat birds, and the frequent stops by lean ones, explained the picture observed in succeeding days of the wave. When most of the fat birds had depleted their reserves, their stopping pulled others down and the wave was brought to a standstill. Movement was resumed after the birds had built up their reserves again, which presumably depended partly on feeding conditions (Chapter 14), and inclement weather could further delay departure. This type of pattern may partly account for the greatly varying fat levels found in migrants caught together on migration at the same place (Chapter 14). The frequency with which the migratory waves appeared thus depended primarily on the time needed for spent birds to replace their fat, modified by variations in the weather which also affected the urge to fly. It was the stimulus of movement by the fat birds on others less fat that caused a large part of the population to move together and produce the wave-like pattern. Although birds moved at various stages of fatness, the amount of fat carried by a bird affected the timing and duration of its flights; and in general the fattest birds made the fastest progress. Nevertheless, this study highlighted the apparent influence of social factors on the migratory process. The birds in this study were making a diurnal overland journey (along the coast) in a region where short-term variations in weather were less extreme than further west in Europe. Possibly in some other regions, the more variable weather has so much influence on migration as to obscure any underlying pattern in the behaviour and physiology of the birds themselves. This work does, however, help to explain why movement does not occur on all days when conditions are apparently ideal, and why it sometimes occurs on days when the weather is less good. The value to the birds in this behaviour probably lies in the advantages of travelling together, including predator avoidance and judgment pooling, as described in the text (see also Chapter 14). From Dolnik & Blyumental, (1967).

Another advantage of migrating in flocks is the energy saving resulting from specific flight formations, such as the V-formation discussed above. Some usually-solitary raptor species are also seen in flocks on migration. While this may result largely from the sharing of narrow migration corridors, individuals clearly benefit from the behaviour of others in moving between thermals (Chapter 7). In effect, each bird watches and follows others along the migration route (for White Storks Ciconia ciconia see Flack et al., 2018), and birds passing in large flocks seem to travel more efficiently, with fewer wing flaps, than those passing in smaller flocks or alone (for Broad-winged Hawk Buteo platypterus see Careau et al., 2006). As is evident to any bird-watcher, typical flock sizes, densities and flight formations differ markedly between species. Among passerines, species that travel in level flight, such as Common Starlings Sturnus vulgaris, usually migrate in dense flocks, whereas in species which migrate by undulating flight, such as finches, individuals keep relatively further apart. Most birds seem to migrate in single species flocks, but some also travel in flocks with related species of similar flight speed.

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Various thrush species sometimes travel together, and so do various tits. Passerines migrating at night usually travel singly or in loose aggregations, with individuals maintaining contact by calls. Similar wing-beat patterns suggested they were the same or similar species. In most species, flocks seldom exceed a few tens of individuals, but in some species occasionally hundreds (Gatter, 2000). Moreover, at times of peak migration, flocks in many species follow in such quick succession that they almost run into one another. This is true even of large species, such as geese and swans, which sometimes appear as an almost continuous parade of flocks of 10 100 individuals. Despite the differences between species, the causal factors behind specific flock sizes and formations are poorly understood, apart from the points mentioned above. The benefits of migrating in flocks may explain why many birds do not start migration from their nesting places which may be scattered over a wide area, but first assemble at particular staging sites, often used year after year, and from which birds depart over a period of days or weeks. This behaviour is especially obvious in shorebirds and waterfowl, but occurs in many others, including cranes, gulls, terns and shearwaters. Through social interactions, including vocal activity, individuals of flocking species seem to communicate their readiness to migrate, and thereby synchronize their departures (for special call used by Eurasian Spoonbills Platalea leocorodia before departure see Lagarde & Piersma, 2021). Some species display pre-flight intention movements, and intense calling, with repeated take-offs and landings, before finally setting off. Among shorebirds, some of these preliminary flights occur in highly structured formations, as do the departures themselves (Piersma et al., 1990). Other normally solitary birds seemingly make special efforts to travel with others. For example, Eurasian Bitterns Botaurus stellaris have been seen to rise from reed beds around dusk and circle around for a while, calling until they are joined by others, and then departing as a group (Puglisi & Baldaccini, 2000). This behaviour has also been seen in American Coots Fulica americana (Hamilton, 1962), and rather surprisingly, in various owls. For example, among migrating Barn Owls Tyto alba, vocalizing individuals at dusk were subsequently joined by others to form loose flocks which then headed out over water (Russell et al., 1991). It is presumably the advantages of migrating with other individuals that encourage such behavior. Some large bird species, such as swans, geese and cranes, travel in pairs or families within the flocks, and some terns and auks also travel with their young (Chapter 10). Other waterfowl, including many species of ducks, form pairs in winter quarters, and the male then accompanies the female back to her breeding area (Chapter 19). Among Eurasian Oystercatchers (Haematopus ostralegus) in Iceland, whether or not an individual migrates follows paternal but not maternal behaviour. Fathers look after their young for longer than mothers do, and evidently have more influence on their behaviour (Me´ndez et al., 2021). Somewhat unexpectedly, some European Bee-eaters Merops apiaster remained in the same groups of unrelated individuals throughout their 14,000 km migration. Groups that separated during migration reformed after 5000 km apart, and while in the nonbreeding areas, groups repeatedly broke up and re-formed. About half the birds studied stayed together throughout the annual cycle (Dhanjal-Adams et al., 2018). Long-tailed Tits Aegithalos caudatus have been found to migrate in groups of related individuals (Chetverikova et al., 2017), and some other migrant passerines occurred in pairs, either on autumn and spring stopover sites or in winter: that is, male female combinations were much more frequent than expected by chance, and the partners behaved as mated pairs (for examples see Greenberg & Gradwohl, 1980). The Bearded Reedling Panurus biarmicus has provided many instances of birds apparently migrating as pairs (Wernham et al., 2002); but whether such liaisons persist into the breeding season or have reproductive consequences is unknown. Despite such examples, we can assume that reproductive pairing before arrival on breeding areas is not common among birds, because in most species that have been studied, the two sexes behave independently when away from their breeding areas, and males arrive, on average, at least several days before females (Chapter 18). Only in relatively few species, including some waterfowl and cranes, do birds arrive already paired. Evidently, in many bird species, individuals do not behave independently of one another on migration, but can be influenced to varying degrees by other individuals. In field conditions, the role of social influence, and its relationship with body condition, has been studied in Common Chaffinches Fringilla coelebs (Box 3.1), and in various other species social influence has been found sufficient to override inherent migratory and directional tendencies (Chapter 10). Experiments have indicated that the social environment can also help to terminate migration under appropriate conditions (Robart et al., 2022). On the other hand, individuals of some species, such as the Common Cuckoo Cuculus canorus, seem always to migrate alone, although the possibility of occasional vocal contact cannot be excluded.

REST AND SLEEP Bird species vary greatly in the distances they can fly without needing rest. Near one extreme, certain gallinaceous birds fly less than 1 km before having to land (Palmer, 1962). Near the other extreme, various swifts outside the breeding season normally remain continuously on the wing day and night, as confirmed by tracking studies of Common Swifts Apus

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˚ kesson et al., 2012; Liechti et al., 2013; apus, Pallid Swifts Apus pallidus and Alpine Swifts Tachymarptis melba (A Hedenstro¨m et al., 2019). Only when these swifts reach breeding age, usually at 2 3 years old, do they occupy nest sites for a few months each year so that daily stationary spells are then imposed upon them. Otherwise, all vital physiological processes, including sleep, apparently occur during flight. Aside from Swifts, one of the pressing questions relating to long nonstop flights by other birds concerns the matter of sleep. Early studies showed that captive songbirds in a migratory state were able to function appropriately despite sleeping only one-third as much as usual (Rattenborg et al., 2004), often having a rest period in the afternoon before departure (Berthold, 1996). Another breakthrough came with the discovery that birds can rest one brain hemisphere at a time, and thus retain awareness and aerodynamic control while “half-sleeping” in flight (Rattenborg et al., 2016). As in mammals, birds exhibit two types of sleep, slow-wave sleep (SWS) and rapid eye-movement (REM) sleep. Whereas SWS can occur in one or both brain hemispheres at a time, REM sleep only occurs in both simultaneously. Each eye is connected to the opposite brain hemisphere. During uni-hemispheric SWS, the eye connected to the awake hemisphere remains open, a state that may allow birds to visually navigate during sleep in flight. Bi-hemispheric SWS may also be possible during flight when constant visual monitoring of the environment is unnecessary. Nevertheless, the reduction in muscle tone that usually accompanies REM sleep makes it unlikely, according to Rattenborg (2006), that birds enter this state in flight. After a long flight, periods of undisturbed recovery sleep may be essential for maintaining normal brain function during wakefulness, and after landing, birds may need to recover the components of sleep they have missed while flying. The recent miniaturization of electroencephalogram (EEG) recording devices makes it possible to measure brain activity during flight. EEG recordings of Great Frigatebirds Fregata minor breeding in Galapagos and flying over the ocean for up to 10 days at a time revealed that they indulged in very short periods of SWS sleep, totalling 42 minutes in each 24 hour period, mostly at night. Remarkably, three-quarters of this sleep involved only one brain hemisphere at a time, and the rest involved both hemispheres at the same time, through all of which the bird remained airborne (Rattenborg et al., 2016). In comparison, when on land, Frigatebirds slept for a daily total of 12 hours, and for half this time rested both hemispheres simultaneously. The important findings were that: (1) these frigatebirds proved able sleep on the wing, but for far less time per day than was normal on land, (2) for much of the time they were asleep on the wing they rested only one hemisphere at a time, and (4) only SWS sleep was recorded from birds on the wing. This is clearly an area where further research is needed, especially for landbirds making multi-day flights overwater. If it turns out that many birds sleep while airborne, the question becomes whether, once on land, they need to recover from deficits of any aspect of sleep incurred during flight. In many birds landing from a long flight, the need for sleep may take precedence over most other activities, as recorded for various shorebirds and waterfowl (Schwilch et al., 2002). Observations describe these birds falling asleep within minutes after arrival, and sleeping for several hours before starting to feed; or passerines after arrival from long over-water flights resting under coastal bushes for much or all of the following day before moving on, apparently without feeding (Schwilch et al., 2002). When crossing desert, many Eurasian-African migrants migrate at night and rest by day, and using bird-born accelerometers, Red-backed Shrikes Lanius collurio were found to spend most of their time sleeping during days between long nocturnal flights (Ba¨ckman et al., 2017). Many other nocturnal migrants have been found to sleep for several hours in the afternoon before they resume their journeys overnight (Cochran & Wikelski, 2005). Heart rate then drops considerably relative to foraging or flying states (Cochran & Wikelski, 2005); and key metabolites differ from those of birds in “feeding” or “flying” states (Jenni & Jenni-Eiermann, 1992). Some aspects of physiological recovery can occur through rest (breaks in periods of exertion), rather than sleep. Almost continuous recording of birds on migration may be needed to pick up brief periods of rest, and few studies of this type have yet been done. However, some Barnacle Geese tracked on migration had their heart rates monitored continuously during the journey. These rates were faster when the birds were flying than at other times. Records suggested that birds settled about every 11 hours (maximum 13 hours) during the journey, even though this often entailed the birds resting on the sea (Butler et al., 2000). Other tracked Barnacle Geese stopped on their 500 km crossing between Iceland and north-east Greenland (Doyle et al., 2022). On six occasions, these geese stopped on the open sea for up to 6 hours, and on five occasions on sea ice for up to 12 hours. Two birds made multiple stops, with one individual taking approximately 100 hours to complete the 500 km crossing. Similarly, some Brent Geese travelling between the Netherlands and the Taimyr Peninsula of Siberia were found to stop about every 6.5 7 hours, on average, which gave flight lengths of 450 500 km. However, some nonstop flights by these birds lasted 14 19 hours, and covered up to 1300 km. It is not always possible to tell whether birds are stopping on the sea for reasons of tiredness or bad weather. However, Whooper Swans migrating from Britain and Ireland to Iceland settled on sea only during periods of low

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visibility or darkness (Pennycuick et al., 1999), and Pink-footed Geese Anser brachyrhynchus making the 650 km seacrossing between North Norway and Svalbard rested on the sea during adverse winds (Geisler et al., 2022). Such stops were recorded nearly four times as often in spring as in autumn, and their effects were not trivial: they led to 23% longer routes, 60% longer durations, 93% longer air distances and 45% higher ratios of air-to-ground distances in spring than in autumn. So for these Pink-footed Geese, breaks caused by wind conditions had a major influence on the time and energy spent on migration, and, despite being able to rest on water, the Barents Sea provided a bigger obstacle to migration in spring than in autumn. In addition, Brent Geese and Greenland White-fronted Geese rested on the Greenland Ice Cap at least during the upward part of the journey, at elevations up to of 2.5 km above sea level (Gudmundsson et al., 1995; Fox et al., 2003). Shorebirds may also settle on the sea from time to time, at least under adverse flying conditions (Piersma et al., 2002). Of course, most landbirds could not rest on water and, despite the many records of birds resting on ships and offshore structures, and possibly also mats of flotsam, most are assumed to fly even their longest over-water journeys nonstop. Nevertheless, the possibility that the need for sleep or rest may help to shape the migratory behaviour of birds, and influence the routes they take, warrants further study (Chapter 14). Some birds may need to rest because they become over-heated rather than tired. Many long-distance bird migrants seem to be able to spend energy at an exceptionally high rate and shed the large amounts of heat produced while flying, all without dehydrating. This holds in many trans-Saharan migrants (Chapter 6). Numerous studies have shown that flying birds lose surplus heat mainly by convection, followed by radiation and evaporation through panting. Nevertheless, some birds seem to over-heat rather easily: for example, Common Eiders Somateria mollissima which in one study preferred to migrate by short flights separated by frequent rests (Guillemette et al., 2016). Tracked Eiders spent less than 15% of each day on the wing, travelling on a stop-go strategy, with migratory flights short (average 16 min) and frequent (average 14 flights per day). This was put down to hyperthermia, for although these birds live in cold regions, they have short pointed wings and heavy wing-loading, rapid wingbeats and fast flight, entailing rapid metabolism. Although not altogether preventing longer flights, the risk of over-heating may be ever-present in Eiders, and also in some other birds with high wing loading and fast wing-beats, such as some gallinaceous birds.

CONCLUDING REMARKS The theoretical background to flight, as outlined above, was developed long ago primarily for still-winged aircraft. Predictions developed from this theory have stimulated studies on most aspects of bird flight, and in most respects these predictions fit birds fairly well. Where birds diverge from predictions, they usually turn out to be more efficient, outperforming airplanes in various respects. This is largely due to the lightness, mobility and flexibility of birds, their ability to flap the wings, alter the sizes and shapes of the wings, and move or fan the tail to meet the needs of the time. This contrasts with the rigidity of fixed-winged aircraft. Moreover, by travelling in specific formations, undulating their flight or combining their efforts in other ways, many birds can make further savings on energy use. Much of this chapter was concerned with the ways in which bird features (such as body weight, wing shape, flight mode and fuel load) interact with one another, and with environmental features (such as wind conditions) to influence migratory capability. Such interactions probably account for some of the big differences in migratory performance (speeds, routes, altitudes and distances) that occur between species, and also within species, according to their current fuel loads and ambient conditions. Theory based on aerodynamic principles is increasingly supported by field data. For example, it provides an aerodynamic rationale for the observation that long-range small bird migrants accumulate relatively greater fuel loads for migration than large birds that also travel by flapping flight, and for why many large bird species migrate by soaring gliding flight, rather than by flapping. Large waterfowl, which travel entirely by flapping flight, are of special interest because of the limited power available to them, and their weight-related restrictions on fuel reserves. Social interactions seem important in the migrations of some birds, synchronizing timing, and probably leading to better energy saving, collective decision making, and predation defense. Resting and sleeping by migrating birds requires more study, with the expectation of big differences between different types of birds. Because many birds have the same requirements on migration, avoiding or minimizing water crossings, ice-sheets, mountain ranges or other barriers, the routes of different species tend to converge, and some geographical locations tend to serve as staging areas for many different species. The result is that migration does not run evenly across the globe but, under the influence of topographic, atmospheric and seasonal conditions, migrants tend to concentrate into well-developed streams. This is especially true of soaring landbirds which each year take the same routes which provide good lift and the shortest possible water-crossings (Chapter 7).

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SUMMARY In birds that fly by flapping flight (as opposed to soaring gliding), the energy need is greater at slow and fast speeds than at intermediate speeds. Most migrating birds are likely to fly at intermediate speeds, somewhere between the "minimal power speed" (Vmp), which gives minimal rate of fuel use and hence maximum time airborne, or at the somewhat faster “maximum range speed” (Vmr), which gives the longest distance on a given amount of fuel. These two speeds span the most economical range of flight speeds for converting fuel into distance. Wind conditions have further influence on the ground speeds attained. Body size sets constraints on migration. With increasing body mass, flight costs increase, as does flight efficiency (energy cost per unit weight) and flight speed, but the amount of fuel (relative to body weight) that can be carried declines, reducing the maximum possible nonstop flight range. Wing design has additional influence on flight speed and efficiency. With favourable winds, swans (some of the heaviest of flying birds) can make nonstop flights covering up to 1700 km and small geese up to 5000 km. Passerines can make nonstop flights of 80 100 hours, enabling them to cover distances of 1500 3000 km, and the faster shorebirds can make nonstop flights of 6 9 days, covering distances up to 8000 km, with one extreme flight exceeding 10,000 km. Most bird species migrate by flapping flight, but some large species migrate mainly by soaring and gliding. This latter method requires much less energy per unit time than flapping flight but, being dependent largely on thermals or other updrafts, soaring land-bird species often have to take roundabout routes avoiding long water crossings. They can also travel only by day, while many other (flapping) birds can travel at night. The energy costs of powered (flapping) flight are around 5 25 times greater than basal metabolic rate, and of soaring-gliding flight about 1.3 2.2 times greater. While these energy needs depend on speed in flapping flight, they are independent of speed in soaring gliding flight, for which the necessary energy comes mainly from the ambient atmosphere. Many seabirds also migrate by soaring-gliding or by a mixture of gliding and flapping, making use of updrafts created by wind against waves. In general, they travel at much lower elevations than do landbirds. Species that migrate by walking or swimming travel more slowly and generally shorter distances than species that migrate by flight, but migrations exceeding 1000 km have been recorded from some penguin species. Some bird species migrate singly and others in flocks, the structure of which varies consistently between different types of birds. The flight times and behaviour of birds are influenced by conspecifics, leading to waves in the passage of birds, characteristic flock sizes and formations. The familiar V-formation of many migrating birds enables individuals to save energy, gaining from the updraft created by the bird ahead. Other flock formations and flight modes may serve a similar function. While fuel and water could clearly limit the length of nonstop flights by birds, most species may need to rest or sleep well before they reach the limit set by fuel reserves. Birds require less sleep during migration than at other times, and can apparently sleep by resting one brain hemisphere at a time.

REFERENCES Alerstam, T. (1990). Bird migration. Cambridge, University Press. Alerstam, T. (2011). Optimal migration revisited. J. Ornithol. 152 (suppl. 1): S5 23. Alerstam, T. & Gudmundsson, G. A. (1999a). Bird orientation at high latitudes: flight routes between Siberia and North America across the Arctic Ocean. Proc. R. Soc. Lond. B 266: 2499 505. Alerstam, T. & Gudmundsson, G. A. (1999b). Migration patterns of tundra birds: tracking radar observations along the Northeast Passage. Arctic 52: 346 71. Alerstam, T., Rose´n, M., Ba¨ckman, J., Ericson, P. G. P. & Hellgren, O. (2007). Flight speeds among bird species: allometric and phylogenetic effects. PLoS Biol 5 (8): e197. ˚ kesson, S., Klaassen, R., Holmgren, J., Fox, J. W. & Hedenstro¨m, A. A (2012). Migration routes and strategies in a highly aerial migrant, the Common Swift Apus apus revealed by light-level geolocators. PLOS ONE 7: e41195.

Askew, G. & Ellerby, D. (2007). The mechanical power requirements for avian flight. Biol. Lett. 3: 0182. Ba¨ckman, J., Andersson, A., Alerstam, T., Pedersen, L. Sjo¨berg, S. et al. (2017). Activity and migratory flights of individual free-flying songbirds throughout the annual cycle: method and first case study. J. Avian Biol. 48: 309 19. Bairlein, F., Fritz, J., Scope, A., Schwendenwein, I. Stanclova, G. et al. (2015). Energy expenditure and metabolic changes of free-flying migrating Northern Bald Ibis. PloS One 10 (9): e0134433. Baudinette, R. V. & Schmidt-Nielsen, K. (1974). Energy-cost of gliding flight in Herring Gulls. Nature 248: 83 4. Bellrose, F. C. (1967). Radar in orientation research. Proc Int. Orn. Congr. 14: 281 309. Berger, M., Hart, J. S. & Roy, O. Z. (1970). Respiration, oxygen consumption, and heart rate in some birds during rest and flight. Z. Vergl. Physiol. 66: 201 14. Berthold, P. (1996). Control of bird migration. London, Chapman & Hall.

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Migratory flight Chapter | 3

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Chapter 4

Weather and migration

White Pelicans Pelecanus onocrotalus soaring in an updraft They [birds] are usually able to choose a period of mild and favouring winds. North winds [in autumn] either lateral or from the rear are favourable, and they wait for them with the same sagacity that sailors exhibit when at sea. Frederick II of Hohenstaufen, 1244 1248; from an English translation of 1943.

Assessing the effects of weather on bird migration is not straightforward. This is partly because migration depends primarily on the intrinsic migratory state of the birds themselves, and only secondarily on weather. This is evident from several types of observations, familiar to any birder (Lack, 1960). First, weather conditions which in spring or autumn would be associated with migration have no such effect at other times. Second, after a hold-up due to bad weather in the migration season, the return of favourable weather may result in unusually heavy passage. Third, after a long hold-up, or late in the migration season, birds may take off in conditions that, at other times, would stimulate little or no movement. Fourth, at any one place, individuals do not usually all set off together, but over periods of days or weeks. Such variations are attributable to variations in the internal states of the birds and the dates they are prepared for the journey. The underlying controlling factor is thus the internal state of the individual, which interacts with weather and other external conditions to influence departure times. The numbers of birds migrating on particular days may thus depend not just on the prevailing weather, but on the weather over preceding days, the date in the season, and the number of birds ready to leave at the time. The association between weather and the volume of migration on particular days is therefore variable. In addition, because species differ in body size and flight mode, they are affected by adverse weather to different extents, and some species can migrate in conditions that would ground others (Lack, 1960, Alerstam, 1978a; Elkins, 2005). All these considerations complicate any assessment of weather effects on migration. Furthermore, different aspects of weather tend to be associated with one another, with some occurring under cyclonic and others under anticyclonic conditions (Lack, 1960, Richardson, 1978, 1990). Even with the help of multivariate statistics, it is often hard to tell which aspects were causal and which coincidental. Almost certainly, migrants do not react to the general weather situation as such, but to one or more components, notably wind and rain. Nevertheless, for the human observer, synoptic weather maps of fronts and pressure systems give a good indication of how much migration to expect at different places on particular days (Box 4.1). The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00006-3 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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BOX 4.1 Weather effects: the bigger picture. In high latitude regions the likelihood of strong bird migration on particular days within the migration seasons can be predicted largely from synoptic weather maps, showing fronts and pressure systems over wide areas. The atmosphere at such latitudes is organized into high and low pressure systems which move approximately eastward. In the northern hemisphere, winds blow clockwise around highs and counter-clockwise around lows. Fronts separate air masses in these systems: warm fronts occur where advancing warm air is replacing cold air, usually east or southeast of an approaching low; and cold fronts occur where cold air is replacing warmer air, usually south or southwest of a low. Precipitation and thick cloud occur most commonly near lows and fronts. Given the importance of wind direction and clear skies, migration timing can be related to these large-scale atmospheric features, even if birds sense only their local manifestations. In the northern temperate region, peak southward migration tends to occur with cool northerly tailwinds as a “low” moves away to the east, or a “high” approaches from the west, or both. Conversely, peak northward migration tends to occur with warm southerly tailwinds, as a “high” moves away to the east, or a “low” approaches from the west, or both. At both seasons, much migration also occurs with light winds near the centre of a high (Richardson, 1990). When birds are concentrated by coasts, ridges or valleys, the numbers passing a given point may be quite different from what the above weather patterns would suggest. Also, the association between synoptic weather patterns and migration volume is likely to decline as birds get increasingly far from their departure points. In the southern hemisphere, different (but related) trends are expected, because winds there blow in the opposite directions around lows and highs. Based mainly on Richardson (1990).

Another potential problem relates to the use of visual observations to assess weather effects. Ground-based observers miss any birds flying too high to be seen by day, and provide little or no information on nocturnal migration. Radar has revealed that most migration of birds that fly by flapping flight occurs above visual range. In fact, the proportion of birds flying within sight, and the proportion that come to ground, tend to be greatest in conditions that are unfavourable for flight (Lack, 1960). Migrants tend to fly low in opposing rather than following winds, and to settle whenever they encounter strong opposing winds, mist or rain, or reach coastlines or islands. The observer equipped only with binoculars might conclude that these were the very conditions that favoured migration, a once commonly held view but the opposite to reality. Birds also tend to fly low along coasts in these conditions, reluctant to strike out over water. It is therefore important to distinguish the influence of weather in promoting migration from its influence in making migration conspicuous (Lack, 1960; Alerstam, 1978a). The use of radar greatly clarified the situation, because it enabled migrants to be detected at almost all heights (missing only those below the radar horizon), day and night, and in all weathers. From radar-based studies, consensus soon emerged that, within the appropriate seasons, migration is favoured by fine anticyclonic conditions with helpful tailwinds, and also by rising temperatures in spring and by falling temperatures in autumn. In effect, at both seasons the birds migrate mainly under clear skies with following or light winds. Clear skies assist navigation, especially at night, by making celestial cues more visible, while following winds reduce the time and energy spent on the journey, and the risk of being blown off course. In contrast, birds seldom take off to migrate in strong opposing winds, dense cloud, mist and rain. Interestingly, weather conditions associated with heavy migration in free-living birds are often also associated with strong migratory restlessness in captive birds, evidently reacting to the same conditions (Gwinner et al., 1992). These conclusions on weather effects were drawn from a large number of short-term studies (mainly by radar) in various parts of the world (Richardson, 1990). However, an almost complete picture of autumn migration was recorded near Nuremberg in Germany by use of a conically scanning pencil-beam radar (Erni et al., 2002). At this site, bird migration increased in volume from early August, reached high levels in September to mid-October and then declined. Allowing for this seasonal trend, about two-thirds of the variation in daily volume of migration was explained by wind and rain, although correlations also emerged with associated weather factors, such as temperature, pressure and cloud cover. Migration was more closely correlated with the duration of rain than with the overall amount per night. After short heavy showers, birds resumed migration, whereas on nights with continuous drizzle, few birds flew. Similar patterns emerged in other studies, including some based on Doppler weather radars in both Europe and North America (La Sorte et al., 2015; Shamoun-Baranes et al., 2017b; Van Doren & Horton, 2018). The importance of temperature to migration remains uncertain. In spring, warmth occurs in association with other conditions favourable to flight, as does cold in autumn. But temperature may have direct effects through influencing the energy balance of the birds themselves, and more importantly through influencing their food intake, because all

Weather and migration Chapter | 4

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vegetative growth, insect activity, and ice melt are temperature-dependent. It is therefore not surprising that the migratory schedules of birds vary somewhat from year-to-year, according to prevailing temperatures, and that unseasonal cold and snow can bring spring migration to a standstill (Chapter 15). Observations of birds about to depart are consistent with the findings from radar studies. Take-off occurs most often on nights with good visibility, bright stars, no overcast or rain, and with light or following winds, these conditions being more influential in long-distance than in short-distance migrants (Cochran & Kjos, 1985; Bolshakov & Bulyuk, 1999). In some species, individuals usually take off singly without preliminary activity. Songbirds leaving from trees and bushes at dusk were seen at first to flutter uncertainly upwards, in ones and twos or small parties, and then, climbing all the time, proceed in the direction of travel, rapidly disappearing into the gloom (Hebrard, 1971). In other species, such as shorebirds, departures can be noisy and impressive affairs, as flock after flock takes off and heads into the distance, calling and climbing till out of sight (Piersma et al., 1990). Occasionally birds at migration times fly up and around for a while before returning to the ground (for Northern Wheatear Oenanthe oenanthe see Schmaljohann et al., 2011). This behaviour is regarded as exploratory, enabling migrants to evaluate conditions aloft before they decide to continue or wait for conditions to change. Departure directions of birds leaving stopover sites do not always reflect their subsequent travel directions. Through use of an automated radio-telemetry system and a tracking radar at Falsterbo in Sweden, the track directions of birds in level flight at high altitudes were more concentrated than the directions of departing and climbing birds, implying that birds can take off in any suitable direction and then adjust their travel direction once aloft (Sjo¨berg & Nilsson, 2015). This view was supported in a subsample of radio-tracked birds that showed a wide scatter of bearings at take-off, but later passed on the same bearings over an offshore radio-receiving station 50 km southeast of Falsterbo. Flight directions seemed to be more affected by winds in climbing than in level flights, which might be explained by birds starting to compensate for wind drift only after they had reached their cruising altitude. In another study, Eurasian Curlews Numenius arquata bearing tracking devices took off into headwinds, but then climbed to altitudes higher than normal where winds were more favourable (Schwemmer et al., 2021). Because they meet different conditions during their journeys, birds usually travel more quickly through some regions than others. For example, many soaring birds migrate more rapidly through warmer than colder regions because of the greater development of thermals in warmer regions. They thus travel more slowly through Europe than through Africa, and make especially rapid progress through the Sahara Desert where soaring conditions are good on almost every day but feeding is not possible (see Shamoun-Baranes et al., 2003 for White Stork Ciconia ciconia, Klaassen et al., 2008 for Osprey Pandion haliaetus, Chevallier et al., 2010 for Black Stork Ciconia nigra). However good the weather at take-off, migrants can encounter poor conditions on route. If they meet low cloud and unfavourable wind, birds may be forced low and, if over the land, they can settle and wait for better conditions. Over the sea, as radar has revealed, landbird migrants that encounter rain, if not at too great a distance, may turn around and fly back to land. But if they enter cloud or mist banks they often become disorientated, milling in all directions and gradually drifting downwind, or actively flying downwind which gives them a good chance of reaching clearer weather (Lack, 1960; Bourne, 1981). If cloud persists, migrants over the sea are sometimes attracted in large numbers to lighted ships or oilrigs (Bourne, 1979, 1983). Although heavy overcast appears inimical for migration, some birds seem to maintain more or less straight courses with complete cloud cover. Below the cloud they can see the ground, and above it the sun or stars. They can also travel by using the earth’s magnetic field to navigate (Chapter 10), a facility probably unaffected by weather. Once on route, the best course of action for a bird may depend on prevailing circumstances, and particularly whether the bird is fat or lean, and over favourable or unfavourable terrain.

IMPORTANCE OF WIND In general, wind speeds are stronger at mid-day than at night or early morning, and increase from the ground, where friction slows the wind, up to several thousand metres. In addition, the air mass in which birds migrate is continually changing in speed and direction, and birds must continually adjust their flight if they are to migrate to a predetermined destination in the most energy-efficient way. That birds respond to wind is shown by the frequent observations that: (1) they depart chiefly in favourable (following) winds; (2) they often select flight altitudes where winds are favourable, changing altitude during the flight if necessary; (3) they compensate for wind drift, at least to some extent, and (4) if winds are unfavourable for several days, migration can be substantially delayed. The long-standing observational evidence that birds mostly set off with following winds has been confirmed for ˚ kesson & individual tracked birds which migrated mainly on days with wind assistance (for passerines see A Hedenstro¨m, 2000, for waterfowl see Green et al., 2002; Klaassen et al., 2004, for waders see Gill et al., 2014a,b). The reluctance of birds to fly against headwinds is clearly adaptive, but can sometimes result in long delays. For example,

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in 1994 when winds were favourable, four radio-tagged Barnacle Geese Branta leucopsis took 5 15 days to migrate between Svalbard and Scotland; but in 1995 when winds were unfavourable for much of the time, radio-tagged birds took 9 36 days, with five individuals arriving 10 days (three birds) and 24 days (two birds) later than the majority (Butler et al., 2003). Moreover, despite the advantage of tailwind assistance, some birds migrate without it (e.g., Thorup et al., 2006a,b; Alerstam, 2011). Birds may well behave differently between regions with different wind regimes, and vary their behaviour according to whether they need to avoid further delay, whether they carry big or small fuel reserves, and whether over land or water. As shown by radar studies, birds often fly slower than usual with a tailwind, and faster than usual against a headwind, apparently conserving energy when conditions allow and expending more when necessary (Chapter 3; Bellrose, 1967; Liechti, 2006; Alerstam & Gudmundsson, 1999a,b; Hedenstro¨m et al., 2005). But where tailwinds exceed the birds own flight speed, they also bring risks, especially over inhospitable terrain, and if their body reserves run out or conditions deteriorate, birds cannot easily return.

Correction for drift If the wind deviates to some extent from a bird’s intended track, the bird can correct for this by adjusting its heading so as to remain on course with respect to the ground (Figure 4.1). Birds do not then fly in the direction they are heading, but at some angle to it, which is closer to the intended track. The greater the crosswind component for a given flight speed, the greater this compensating angle must be (aircraft pilots refer to the angle between heading and track as the drift angle, alpha). This angle can be reduced by flying faster. The point at which a bird is no longer able to compensate for lateral drift is thus a function of wind speed and direction, as well as the maximum flight speed that the bird itself can maintain (called the threshold for drift, Evans, 1966). The three main levels of response to crosswinds include: (1) uncorrected drift so that, under crosswinds, the bird gets further off course with increasing distance (called full lateral drift); (2) the bird compensates for crosswinds but only partly (called partial drift); (3) the bird fully compensates for crosswinds and remains on course throughout its journey, with no drift (Figure 4.1). All three types of response are commonly seen among migrating birds, all incur energy costs, and any amount of drift also involves travelling a longer distance. As a fourth response, a bird over suitable habitat might simply come to ground in a crosswind and wait for conditions to improve. Powered flight 2. Full drift

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FIGURE 4.1 Effects of side-winds (W) on the migratory tracks (T) of birds, depending on adjustments of heading (H), leading to full drift (no compensation, 2, 6), partial drift (partial compensation, 4, 8) and no drift (full compensation, 3, 7). Heading and track are the same when there is no sidewind (1, 5). Upper diagrams relate to powered flight, and the equivalent lower diagrams to soaring flight. If a bird is to continue soaring in a thermal, it will inevitably be transported passively over the ground in whichever direction the thermal is being blown (laterally in the diagrams). The bird may compensate for this during the next gliding phase of the flight. Modified from Kerlinger (1989).

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Over long journeys, birds could cope with crosswinds in other ways (Alerstam, 1979). For example, they might allow themselves to be drifted at high altitudes and then correct for this by overcompensating at low altitudes, as they approach the end of their flight. By flying high at the start they gain the advantage of faster winds at those altitudes, even though their direction is not ideal, and make the correction later in the flight under weaker winds that prevail at lower altitudes (Figure 4.2). Alternatively, if winds shift direction predictably along a migration route, as is common at latitudes 25 35 N, birds could allow themselves to be drifted in one direction at the start of a flight and in the opposite direction towards the end a strategy called “adaptive drift.” This seems to occur on some trans-oceanic flights, for example those in which birds fly from northeastern North America over the Atlantic to Caribbean Islands or South America, on journeys of 3000 4000 km (Williams & Williams, 1990). In autumn, birds depart under south-southeast winds, and once over water, continue flying with the wind in this direction. When they encounter the trade winds near 25 N, their tracks are then drifted to the south and south-southwest as they pass over the Caribbean, allowing the birds to reach South America without adjusting their heading. By not compensating fully for wind drift on the first part of their journey, the birds achieve a faster and more energy-efficient migration to latitudes where wind direction changes, bringing them to their wintering areas in an energy-efficient manner. They are able to follow the pattern in Figure 4.2, making no obvious compensation because crosswinds change predictably from one direction to another along the route. During spring migration, the winds are in the same directions as in autumn, yet the birds must fly in the opposite direction. They therefore make their northward journey to the west overland where winds are weaker and risks are less, but their journey is thereby lengthened. Their entire two-way migration follows a clockwise loop. Similar loop migrations in other parts of the world may also help birds to reap the benefits of favourable winds or minimize the effects of adverse ones (Chapter 25). Radar observations have been used to explore not only the extent to which migrating birds can compensate for drift by crosswinds, but also how much the prevailing circumstances affect the response. Patterns of compensation, full lateral drift, partial drift and downwind drift have all been recorded, depending on wind strength, visibility, day or night, over land or sea, cloud cover, and the stage in the journey. One radar study implied that, as birds spent ever more time over water, the less likely they were to compensate for wind drift (Horton et al., 2016). Perhaps by this late stage in the journey, the birds were tired or short of fuel. Recent studies of drift by crosswinds involved the use of Doppler weather radars (model WSR-88D), which can show the body orientations of birds in flight as well as their direction of travel. These radars can thus reveal how much birds are attempting to compensate for drift and how successful they have been (Van Doren et al., 2016). Radar studies have also confirmed another way in which birds that have been drifted off course overnight attempt to get back on route before continuing their journey. On the Atlantic coast of North America, after nights of drift, mass departures of birds the next morning occurred in directions that would get them back on route (Van Doren et al., 2016). Such birds flew relatively low, benefiting from winds being slowed by friction with the ground. Another example of birds changing their behaviour with respect to wind during the course of migration emerged in Eleonora’s Falcons Falco eleonorae travelling from the Canary Islands across Africa to winter in Madagascar. These birds tended to drift through areas of opposing winds and over ecological barriers, while compensating through areas of weak or supportive winds and over hospitable terrain (Vansteelant et al., 2021). FIGURE 4.2 Optimal use of a crosswind by a migrant. The bird is drifted by the wind during the initial stage of migration and later overcompensates to reach its goal. By invoking different altitude use and varying prevailing winds, variations of this model can be used to test predictions on real birds in the field (see text). From Alerstam (1979).

Starting point

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The Migration Ecology of Birds

Detection of drift How do birds on the wing “know” they are being drifted off course? The most obvious way is by reference to some stable feature, such as the ground below. Use of ground features may explain why compensation seems less frequent in nocturnal than in diurnal migrants, and in birds that are flying high or in fog than in those that are flying low or in clear conditions (Richardson, 1990). For example, during autumn migration, Song Thrushes Turdus philomelos were recorded at night flying along a coastal spit which coincided with their migration direction (Sinelschikova et al., 2020). Under normal visibility, the degree of compensation depended on the velocity of side-winds and on the altitude of flight. On average, at heights below 300 m above ground, the thrushes were able to compensate completely for moderate winds; between 300 and 600 m above ground they compensated partially; but above 600 m they drifted completely. So these birds showed different reactions to the same crosswind depending on their altitude of flight and its apparent effect on their ability to measure drift. But transoceanic migrants have no benefit from obvious landmarks, so how well do they remain on course? At takeoff, such birds are clearly sensitive to local wind conditions, but once over featureless ocean some may fly non-stop for more than 100 hours. Yet despite strong crosswinds and lack of landmarks, juvenile Ospreys Pandion haliaetus maintained remarkably straight tracks day and night for 1,500 2,000 km over the West Atlantic, implying very precise navigation (Horton et al., 2014). The same held for Hudsonian Godwits Limosa haemastica travelling for six days over the Pacific Ocean from Chile to the Gulf of Mexico, on route to their breeding areas in Alaska (Linscott et al., 2022). Despite the fluctuating winds, the birds remained on track, or continually brought themselves back on track, throughout their journey, again implying ongoing precision in navigation. Whether migrating birds compensate for crosswinds may depend not only on their ability to do so, but also on their remaining body reserves. In some circumstances, it may be more economical for landbirds over water to drift downwind than to use scarce fuel reserves to fight against an adverse wind in order to remain on course. These considerations help to explain the great variations observed in bird behaviour with respect to wind, with birds drifting when they can afford to, and compensating when they must (Horton et al., 2016). Clear advantages accrue to migrating birds which take account of geography and wind. In conditions prevailing in central Europe in autumn, a bird migrating only on nights with favourable wind can, on average, increase its flight speed by 30% compared with an individual that disregards wind (Liechti & Bruderer, 1998). Selecting the most profitable flight altitude may result in an additional 40% gain in flight speed. In other words, by responding appropriately to wind conditions, a bird can greatly increase its flight speed and greatly reduce its energy use during a journey through this region. The time needed for re-fuelling decreases accordingly, or the safety margins provided by the body reserves are extended. The bird is also at less risk of being blown far off course. Clearly, there are great benefits to a migrant in responding appropriately to wind, and the huge day-to-day fluctuations in the volume of bird migration seen at particular sites reflect the continual adjustment of bird behaviour to prevailing weather (Alerstam, 1981). Some long non-stop flights may be accomplished only with the aid of a following wind. This was the conclusion of several studies in which the known energy reserves of migrants were compared with their estimated needs on migration (for passerines see Izhaki & Maitav, 1998; for shorebirds see Stoddard et al., 1983; Piersma & Jukema, 1990; Marks & Redmond, 1994; Butler et al., 1997). In other species, wind assistance was found necessary for birds to achieve their migrations in the time observed (Butler et al., 1997), and in yet other species, arrival dates were related to the proportion of days with following winds during the normal migration period (for Bewick’s Swans Cygnus columbianus see Rees, 1982, for Lesser Snow Geese Anser caerulescens see Ball, 1983, for Barnacle Geese see Butler et al., 2003, for American Yellow Warblers Setophaga aestiva see Drake et al., 2014). Prevailing west-east winds in temperate latitudes present a major challenge for most migrants, especially where they could be blown out to sea. One consequence of overland drift is that it often results in concentrations of birds along coastlines. Unless adapted to long water crossings, migrating landbirds are likely to pay the extra energy cost of battling against wind drift when moving along coastlines, specifically to avoid being blown over water when they need to return to land to refuel (Horton et al., 2016). This may be one reason behind the concentrating effect of coastlines, comprising birds that were prepared to accept drift overland but not overwater.

RECENT DEVELOPMENTS In recent years, new technology has enabled the flight behaviour and energetics of birds to be examined in more detail than previously. This stems largely through use of high resolution GPS trackers and additional miniaturized sensors such altimeters, accelerometers and heart-rate recorders (for examples see Paiva et al., 2010; Bishop et al., 2015;

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Shamoun-Baranes et al., 2016, 2017a,b; Sherub et al., 2016; Vansteelant et al., 2015, 2017). Such devices have revealed that birds react rapidly in some cases almost minute by minute to changes in atmospheric conditions so as to achieve more energy-efficient flight. A bird may make almost instant changes to its airspeed, heading or flight mode, and over a longer period to its cruising altitude and course. Some species make what seem to be occasional exploratory climbs or descents to find a better altitude at which to migrate (Norevik et al., 2021). It is through these various responses that adults travel more efficiently, and often more rapidly, than juveniles migrating in similar conditions, implying that these energy-saving tactics are learnt (Chapter 18). The use of operational weather-radar networks has enabled researchers to study bird migration in relation to weather over much larger areas than previously (Shamoun-Baranes et al., 2014; La Sorte et al., 2015; Horton et al., 2016). By using 23 years of spring observations to identify associations between atmospheric conditions and the intensity of bird migration, Van Doren & Horton (2018) developed a migration forecast system operating over wide areas. Their models explained up to 81% of variation in migration intensity across the United States at altitudes up to 3000 metres, and could predict migration events 1 7 days in advance (62% 76% of variation explained). Use of these forecasts could help to reduce collisions of birds with airplanes, buildings and wind turbines; and inform a variety of other bird monitoring programmes. Numbers of migrants across the United States probably exceeded 500 million individuals per night during peak spring passage, offering considerable scope for collisions with the growing numbers of wind turbines and other structures.

LOW LEVEL FLIGHT Although most of our understanding of weather effects on migration is based on radar studies, direct observations show that some low-level flight (below the radar horizon) occurs under headwinds and other conditions that discourage higher level flight. In these conditions, many small birds migrate by “bush-hopping” or “tree-hopping,” in which they flit from bush to bush or from tree to tree, feeding as they go, but travelling continually in the same direction. Warblers, which normally migrate at night, sometimes pass in daytime through extensive bushy or reedy areas in this way, as do tits and other canopy-feeding passerines as they travel through wooded terrain. Many small birds also fly low for short distances in the gaps between showers. Such low-flying birds take more account than high-flying birds of topographical features, being more deflected by hills and water bodies, and in strong winds they often take shelter provided by ground contours or forest edges. In these ways, small birds can maintain some progress on days when they might not otherwise travel. By their combination of flying and feeding (on a fly-andforage strategy), these small passerines resemble swifts and hirundines that pick off insects as they go. But as headwinds increase, fewer and fewer birds take part in these low movements, as species after species drops out and continues migration later.

SOARING SPECIES With respect to wind, soaring birds provide partial exceptions to the patterns outlined above. Up-drafts strongly reduce the energy cost of migration for soaring birds, which often fly in side-winds or light opposing winds if updrafts are present. Thermals develop in calm or light wind conditions, but not in strong winds, which suppresses the migration of soaring birds in some regions, regardless of wind direction. Soaring birds also show no particular tendency to migrate on cold days in autumn, as do many other birds, probably because thermals develop best on warm days (Alerstam, 1978a; Kerlinger, 1989). In mountain areas, however, soaring birds are also helped by crosswinds which strike slopes and are deflected upwards, providing the lift they need (Chapters 3, 7). In such areas, raptors and other birds achieve flight altitudes much higher above sea level than when using thermals over lower ground. In the Himalayas, cranes and raptors have been recorded at more than 6.5 km a.s.l. (Chapter 6).

GLOBAL WIND PATTERNS AND MIGRATION ROUTES Air and water currents vary across the globe in fairly consistent patterns from year to year, creating optimal flyways along which migrants can gain maximum benefit (or minimum cost) on their seasonal journeys (Kranstauber et al., 2015). Global wind patterns could thus have an important selective influence on the evolution of migration routes. They could explain why birds do not always take the shortest route, but may make substantial detours, taking longer but safer or energetically cheaper routes. This is most obvious in soaring landbirds which take routes that minimize water crossings. It is also evident in birds that perform loop migrations, taking different routes on their outward and return

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journeys, allowing them to benefit from tailwinds or avoid headwinds. Loop migrations are common among species that cross ecological barriers, such as deserts, high mountain ranges or oceans (Chapter 24; for Sahara Desert see Erni et al., 2005; Schmaljohann et al., 2009; for Western Atlantic see La Sorte & Fink 2017; for Pacific Ocean see Gill et al., 2009, 2014a,b: and South China Sea see Nourani et al., 2016). Using 21 years of global wind data, Kranstauber et al. (2015) calculated the optimal route (in terms of energy costs) for various landbirds migrating between northern and tropical regions, and compared these routes with the shortest possible (great circle) routes. Because of wind conditions, these optimal routes produced a reduction in median travel times of 26.5% over the shortest routes. The authors suggested that, even if birds were incapable of predicting wind conditions at the time, the optimal route could have evolved over the generations by natural selection. In September many optimal routes between the Americas lay far out over the Atlantic Ocean, whereas in April the optimal routes lay closer to the continent, which matches the loop migrations of many species. Similarly, the routes between Africa and Europe are more eastwards in September than in April, which again matches the routes taken by many birds. The implication is that non-direct routes could have been shaped by consistent wind patterns under the action of natural selection. Within North America, two prominent wind patterns seem to dominate broad-scale migration (La Sorte et al., 2018). The first is the prevailing westerlies that are most marked at mid latitudes. Migrants that encounter these crosswinds during spring migration seem to adjust their headings sufficiently to avoid serious drift (Horton et al., 2018). But in autumn, they seem to time their departures to coincide with lulls in the westerlies that occur after the passage of frontal systems. The second major circulation feature in North America is the low-level jet stream that generates southerly winds through the centre of the continent across the Great Plains. Millions of migrants funnel through the central migratory flyway each spring taking advantage of this shallow northward conveyer belt of air which flows at altitudes of 600 1600 m and reaches speeds up to 133 km per h (Wainwright et al., 2016). Nocturnal migrants select altitudes during spring migration where these tailwinds are strongest, but in autumn they select lower or sometimes higher altitudes where these winds (then opposed to the migratory direction) are weakest (Wainwright et al., 2016). Wind conditions also have big effects on seabirds migrating over oceans (Shaffer et al., 2006; Gonza´lez-Solı´s et al., 2007; Adams & Flora, 2010; Weimerskirch et al., 2015a,b). In both the Atlantic and Pacific, trans-equatorial migrants, including shearwaters, follow general flyways that resemble figure-8 patterns (Shaffer et al., 2006; Gonza´lez-Solı´s et al., 2007). These birds evidently travel in the direction of the prevailing winds, which circulate clockwise in the Northern Hemisphere and counter-clockwise in the Southern Hemisphere (Chapter 8). In following these “wind highways,” birds can seldom take the shortest routes between breeding and wintering areas. For three species of Atlantic shearwaters these low cost routes were 26% 52% longer than the shortest distance routes (Gonza´lez-Solı´s et al., 2009). For such seabirds, the main barriers to migration are areas of strong headwinds and areas of calm, such as the doldrums, or areas of nutrient-poor waters offering little or no food. Pelagic birds tend to avoid these areas by circumnavigating them, or at least delay their journeys until conditions improve. For the three shearwaters, one potential barrier was the near-surface westerlies off central Africa, which temporarily hindered their trans-equatorial movements. Once these westerlies shifted or slackened, the birds crossed this area to their winter quarters. The Wandering Albatross Diomedea exulans and other species also avoid headwinds by circling the globe during their non-breeding period, so as to stay continuously within the zone of westerly winds (Weimerskirch et al., 2012). The implication from recent tracking studies is that the large scale migrations of soaring-gliding seabirds over the oceans are largely driven by wind patterns, shaped not only by land barriers but also by meteorological barriers (Chapter 8).

ALTITUDE OF MIGRATION The airspace is a much more complex three-dimensional “habitat” than appears from the ground, comprising an ever changing maze of jets, boundaries and eddies, invisible to the eye, but inevitably felt by any bird migrating through it. It consists of a number of layers, each differing in speed and direction, and prone to shift unpredictably, creating a turbulent environment in which to travel. The lower levels constitute the boundary layer, where the air-mass is heavily influenced by the underlying topography. It is within this layer typically up to 3 km above ground—that most bird migration occurs. Birds may continually adjust their cruising height in response to changing conditions, perhaps moving up and down in search of tailwinds, and trying to escape pockets of turbulence or clouds. Study of the altitude at which birds migrate has practical relevance in conservation (because birds can kill themselves against masts and other tall structures) and in aircraft safety (because birds can get caught in engines and bring down planes). Over low land, to judge from radar studies, most migration takes place within 1.5 km of the ground, with decreasing numbers of birds at higher altitudes up to 3 km or more (Bruderer, 1999; La Sorte et al., 2018). However, growing evidence from radar and other tracking studies shows that some birds fly regularly at altitudes of 3 6 km,

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including some small passerines (Liechti et al., 2018; Schmaljohann et al., 2009; Sjo¨berg et al., 2018, 2021). When birds need to cross high mountains or find favourable airstreams, they may fly higher still, occasionally reaching more than 7 km a.s.l. (Chapter 6, Figure 4.3). Radar studies in both Europe and North America have also found that migration generally occurs at higher mean elevation in spring than in autumn and by day than by night, but with wide variation from night to night and place to place, again depending on wind conditions at the time (see Gauthreaux, 1991 for the Louisiana coast, Figure 4.4). Apart from the needs to find favourable winds or to cross mountains, flights at several kilometres high are likely to occur mainly on long non-stop journeys. So much energy is consumed in climbing to high altitudes that this might not be worthwhile on short flights. Migrants from northeastern North America ascended during their autumn flight over the western Atlantic reaching 4 6 km over Antigua in the Caribbean, and later dropping abruptly as they approached South America (Figure 4.3; Williams et al., 1977). But radar has also revealed that birds crossing smaller stretches of water, such as the North Sea or the Great Lakes, lose height during the night, often flying within 100 m above the water, but rising again at dawn (the so-called dawn ascent, Bourne, 1980; Diehl et al., 2003). On the radar screen, overwater echoes disappear late in the night, as birds descend below the radar horizon, and reappear towards dawn, an

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FIGURE 4.3 Altitudinal distribution of migrants as registered by radar studies in: (a) Lowlands of central Europe, spring (Bruderer, 1971); (b) South Sweden, spring, mainly waterfowl and shorebirds (Green, 2004); (c) Antigua, Caribbean, autumn (Williams et al., 1977).

FIGURE 4.4 Correlation between the altitude of densest nocturnal bird migration and the altitude of most favourable wind, as measured by radar in the southeastern United States. The most favourable wind was defined as a wind blowing toward the north-northeast in spring or south-southwest in autumn and occurring at the lowest possible altitude. Regression relationship: y 5 58.6 1 0.987(x), r 5 0.96, t 5 22.9, P ,0.01, N 5 38. Re-drawn from Gauthreaux (1991).

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The Migration Ecology of Birds

appropriate distance along the route. One view is that birds descend during the night in order to find a place to settle. If they find themselves still over water, they ascend at dawn probably to gain a better view and to avoid predation by gulls, which become active around daybreak (Bourne, 1980). If the migrants can then see land, they may change direction and head towards it. According to radar and other tracking studies, some birds also change altitude frequently and rapidly in mid-flight. Fitted with multi-sensor data loggers, Great Snipes Gallinago media travelling from Europe to Africa repeatedly changed altitudes around dawn and dusk between average cruising heights of around 2 km above sea level at night and 4 km by day (Figure 4.5; Lindstro¨m et al., 2021). Regardless of the terrain below, most of these snipes regularly flew at 6 km, and one reached 8.7 km, almost as high as Mount Everest. Their average height was somewhat lower in spring than in autumn, unlike other trans-Saharan migrants (Chapter 6). A similar study of Black-tailed Godwits Limosa limosa migrating in spring between West Africa and Europe showed that birds flew above 5 km on 21% of all flights, and reached maximum altitudes of nearly 6 km above sea level (Senner et al., 2018). At these extremely high altitudes, the birds gained greater wind support and avoided the high air temperatures of lower altitudes, but experienced much thinner air, with a partial pressure of oxygen less than half of that at sea level. The most-studied regular high-flier among birds is the Bar-headed Goose Anser indicus which in crossing the Himalayas has been recorded at around 9 km above sea level (Chapter 6). Soaring birds over level ground are limited in flight altitude by the height reached by thermals, which is greatest around noon and seldom exceeds 1.5 km above ground. During migration, soaring birds are continually rising and falling as they climb in successive thermals and lose height between them, perhaps more than 60 times per 8-hour soaring period (Figure 7.4; Leshem & Yom-Tov, 1996; Spaar & Bruderer, 1996). Unlike many other birds, therefore, they cannot maintain constant altitude over long distances. Soaring birds in mountain areas, where they depend on updrafts, achieve much higher altitudes, and Himalayan Vultures Gyps himalayensis have been recorded soaring on migration to heights greater than 6.5 km above sea level (Sherub et al., 2016). In contrast, soaring seabirds, such as albatrosses, seldom reach more than 15 m above the waves, but this results from the ways in which they use updrafts (Chapter 3). So not all birds are high-fliers.

FIGURE 4.5 Flight altitude of Great Snipes Gallinago media migrating from northern Europe to tropical Africa, showing the regular change in altitude at dawn and dusk. Flight altitudes (m a.s.l.) during autumn (a), within Africa from one wintering area to another (b), and during spring (c), in relation to time of day. The solid dark line and gray shading show the average flight altitude with 95% confidence intervals. Approximate times of day (yellow) and night (grey) are shown for the average date and longitude of migration in each season. Thin grey lines denote individual tracks. For estimating sunrise (03:43) and sunset (18:21) for the autumn flights, an average estimated starting point for all flights of 700 km south of the breeding grounds (56.8 N, 15.0 E) was assumed, and an average date of 23 August. For the spring flights, the estimated sunrise (04:48) and sunset (16:55) times were based on an average starting point for all flights at 0.00 N, 17.00 E, on April 17. For the flights within Africa the estimated sunrise (05:17) and sunset (17:22) were based on an average starting point for all flights at 10.00 N, 8.00 E, on 25 September. From Lindstro¨m et al. (2021).

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Changes in conditions with altitude As they ascend from ground level, migrating birds face progressively changing conditions. Wind speed increases, while air density, oxygen availability and temperature decrease. Once birds break through the cloud layer, they can escape from mist, rain and snow. As stressed above, wind has a major influence on the heights above ground at which birds fly, but wind can frequently alter in direction and strength, affecting the choice of cruising height. This is demonstrated by the trade winds, which give way higher up to the anti-trades blowing in the opposite direction. This situation allows birds to find following winds in both autumn and spring, providing they fly at an appropriate height. In southern Israel, for example, the wind shear associated with the shift from trade to anti-trade winds fluctuates roughly around 1.5 km above sea level. Correspondingly, birds studied by radar flew mainly below this level in autumn, and mainly above it in spring, when some reached heights of almost 9 km a. s. l. In the low-level jet streams of this region, birds also achieved ground speeds of up to 180 km per hour (Liechti & Schaller, 1999). Waders leaving the West African coast for Europe in spring must climb rapidly to altitudes greater than 3 km. It is only at such high altitudes that tailwinds keep the flight costs within reasonable bounds, thereby enabling the birds to complete their 4300-km non-stop flight to the Dutch Wadden Sea coast (Piersma, 1990). Similarly, radio-tagged thrushes tracked on migration in North America ascended as much as 3 km each evening until they found suitable winds (Cochran & Kjos, 1985). With weak winds, they flew lower and accepted some lateral drift. If winds at altitudes above 75 m had adverse head or side components, the birds returned to the ground and did not migrate. In most regions, where little altitudinal choice in wind direction is available, birds can only wait for favourable conditions or change their route between autumn and spring. Apart from wind, the main weather factor influencing the altitude of migration is the cloud base. Most birds fly below the clouds where they can see the ground. The height of the cloud base therefore limits the vertical spread of migration, and if the cloud descends, it compresses the stream downwards, so the average flight altitude decreases, and may become visible. In some situations, however, birds fly above the clouds, presumably relying entirely on celestial or magnetic cues for navigation, with no visual reference to the ground below.

Consequences of high-altitude flight Air densities and associated oxygen levels decline by just over 10% for each 1000 m rise in altitude, which roughly translates to a 27% decline at 3 km, a 41% decline at 5 km and a 65% decline at 10 km, with minor temporal and regional variations. The decline in air density means that, in theoretical still air, birds have to work harder to keep aloft at high altitude, but meet less resistance to forward flight. The maximum range speed increases by an estimated 5% for each 1000 m rise in altitude (Alerstam, 1990), but so does the power required to fly at this speed, which in turn entails a corresponding increase in energy and oxygen consumption. Although there may be no gain in overall range, birds still benefit from flying high, because their increased cruising speed shortens the flight time. In addition, stronger winds and reduced turbulence at high altitudes may reduce the energy costs and flight times even further. Other advantages of high-altitude flight include: (1) a wider view of the ground (which may help birds to stay on course, maintain a straighter track and detect areas of suitable habitat), (2) avoidance of obstacles and deflection by mountains, (3) reduced chance of predation (because birds get above the zone where falcons and other aerial predators normally hunt), and (4) cooler temperatures in hot desert regions, thus reducing the risk of dehydration. At the very highest altitudes at which birds fly, there is also much less diurnal variation in temperature, humidity and other conditions. One cost of highaltitude flight is the climb involved, which is a major effort for heavy species such as geese and swans, but the energy consumed is partly compensated towards the end of the flight, as the birds gain distance while losing height (Chapter 3). Air temperature falls by about 7 C for every 1000 m rise above sea level (or 2  C for every 1000 feet). Over much of the temperate zone, a typical night temperature at ground level in autumn might be 5 C, so that at 1 km altitude, a bird experiences an ambient temperature of about 2 C, while at 3 km it experiences 16 C and at 5 km about 30 C. To this must be added a chill-factor from wind. To some extent, the heat generated by wing-flapping could compensate for the heat loss caused by low air temperature, but at the high altitudes at which birds sometimes fly, the need to keep warm could impose an additional energy drain. In contrast, over hot deserts the heat generated by flight could lead to overheating which the bird could counter by flying higher, by flying at night or by evaporating water through panting (Chapter 3). In hot environments, therefore, high-altitude flight at lower temperatures could greatly reduce the dehydration risk, at least up to the point where the air becomes so thin that water loss is raised through increased respiratory panting (Chapter 6). By flying at night, migrants

62

The Migration Ecology of Birds

experience for any given altitude at least the same temperature reduction as occurs between sea level and 1000 m during daytime (7 C). The heat produced by working flight muscles is not trivial: only about one-fifth of the energy they generate is mechanical, powering flight, while the remainder is heat, the surplus of which must be dissipated by respiration (panting) or by convection. The lower the ambient temperature, the more heat can be lost by convection, and the less water is required for cooling. In one early experiment, a budgerigar flying in a wind tunnel at an air temperature of 18 C 20 C dissipated by evaporation only about 15% of the waste heat generated in the flight muscles, whereas at 36 C 37 C some 47% of the heat was dissipated in this way, entailing much greater water loss (Tucker, 1969). Probably most of the remaining heat at both temperatures was lost by convection from the thinly feathered undersurface of the wings. Air humidity also tends to decline with increase in altitude, especially above the cloud layer. The extreme cold at high altitudes could also increase water loss from a migrant, for cold air is relatively dry when it is inhaled, but saturated when it is exhaled. In addition, if oxygen extraction by the lungs is to remain unchanged at high altitudes, the ventilated volume of air must increase (Carmi et al., 1992). This need has been calculated to increase from sea level to 5 km altitude by as much as 175% per unit distance flown and by 254% per unit time flown in a swan (although swans are unlikely to normally reach this altitude, Klaassen et al., 2004). For this reason, too, migration at very high altitudes brings, not further reduction in dehydration risk as in hot deserts, but increased dehydration risk. Costs and benefits of flight at different altitudes thus vary with circumstances, as well as between species and the physiological constraints under which they operate. Taking these external factors into consideration, along with the variations in body mass, shape and flight mode between species, it is not surprising that different types of birds seem to fly at different altitudes: sea-ducks just above the waves, songbirds mostly up to 1.5 km, and shorebirds often at more than 3 km. Even on the same night, geese migrating over southern Sweden flew at 100 800 m, while shorebirds over the same site flew at up to 3.7 km above sea level (Green, 2004). At Falsterbo, diurnal migrants often appear stratified, with Common Wood Pigeons Columba palumbus and Stock Doves C. oenas occupying the highest band, corvids further down, and then Common Starlings Sturnus vulgaris and finches lower still, and tits just above the trees. The main advantages of low flying (by flapping flight) are that: (1) little energy is expended on climbing, and (2) the ground below is more clearly visible. The main disadvantages are the greater risks from predation and, in hot regions, from overheating and dehydration. Species that migrate by day often fly fairly low (within visual range), and react to the presence of topographical features, such as mountains or coastlines. They may form into streams, as they fly along shorelines or river valleys, or become funneled through mountain passes. But species that migrate by night at high altitude often seem from their radar tracks to be little influenced by the topography below. These high-fliers usually fly on a broad front and often cross mountains and coastlines without deviation. In conclusion, the altitude of migratory flight is related to prevailing atmospheric dynamics, especially wind speed and direction, but also to cloud thickness and height, topography and other factors, as well as the size, wing-shape, flight mode and flight distance of the birds themselves.

DIURNAL AND NOCTURNAL FLIGHT Some bird species migrate mainly by day and others mainly by night. Nocturnal species such as owls and nightjars, or optional diurnal nocturnal species such as waders, might be expected to migrate under cover of darkness. What is interesting is that many normally diurnal species also travel at night. To judge from their eye structure, diurnal birds may have no better vision at night than do humans, but this would still enable them to fly safely through the open skies, seeing star patterns and landscape features that might help them find their way. Apart from soaring landbirds, which depend on daytime thermals, it is not immediately obvious why particular species migrate at one time rather than another. Among passerines: crows, finches, pipits, larks, wagtails, tits, hirundines and others migrate primarily by day, while warblers, flycatchers, thrushes, chats and others migrate primarily by night (Table 4.1). Among non-passerines: pigeons, raptors, cranes, herons and egrets migrate primarily by day; while cuckoos, shorebirds, rails and grebes migrate mainly by night. Comparing different families, there is no obvious and consistent connection between migration times and habitat, diet or other ecology of the species concerned. However, among closely related families, some striking differences occur, as in the passerines just mentioned, and also among waders, in which plovers (Charadriidae) migrate more by day than sandpipers (Scolopacidae). Terns are more likely to migrate at night than are gulls, and several long-distance tern species have been seen setting off in late evening. Among tyrant flycatchers, kingbirds, phoebes and Scissor-tailed Flycatchers Tyrannus forficatus migrate by day and most others at night.

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TABLE 4.1 Diurnal and nocturnal migrants among Holarctic birds. Mainly diurnal

Divers, pelicans, gannets and cormorants, raptors, storks, ibises, spoonbills, flamingos, cranes, pratincoles, grouse, skuas, alcids, pigeons and doves, bee-eaters, woodpeckers, hummingbirds, swallows and martins, jays and crows, kingbirds, phoebes, shrikes, chickadees and titmice, accentors, larks, horned larks, bluebirds, pipits and wagtails, starlings, waxwings, sparrows, New World blackbirds, grackles, cowbirds and meadowlarks, cardueline finches, fringilline finches.

Mainly nocturnal

Grebes, sea-ducks, bitterns, herons, quail, rails and coots, bustards, waders, stone curlews, cuckoos, owls, nightjars, rollers, kingfishers, wryneck, hoopoe, most tyrant flycatchers, vireos, nuthatches and creepers, wrens, thrashers, bluebirds, kinglets (goldcrests), gnatcatchers, Old World flycatchers, chats and thrushes, catbirds, thrashers, warblers, tanagers, towees, New World sparrows, cardinals, dickcissels, New World orioles, tanagers, Old World buntings, longspurs and snow buntings

Both diurnal and nocturnal

Albatrosses and petrels (Procellariiformes), swans and geese (Anseridae), ducks, gulls and terns, shorebirds, swifts.

Short-distance migrants

25

75 50 25 0

N Da M A Du

Percentage

Percentage

Percentage

75 50 0

Goldcrest

Black Redstart

100 75 50 25 0

N Da M S Du

Mistle Thrush

100 75 50 25 0

N Da M A Du

100 Percentage

Chiffchaff 100

Percentage

Yellow-hammer 100

75 50 25 0

N Da M A Du

N Da M A Du

Long-distance migrants

50 25 0

N Da M A Du

Percentage

Percentage

Percentage

75

75 50 25 0

Common Redstart

Firecrest 100

N Da M A Du

75 50 25 0

Song Thrush

100

N Da M A Du

100 Percentage

Willow Warbler 100

Percentage

Ortolan Bunting 100

75 50 25 0

N Da M A Du

75 50 25 0

N Da M A Du

FIGURE 4.6 Diurnal variation in the number of migrants seen (or caught in mist nets) when crossing the Col de Bretolet in the Swiss Alps. N 5 night, Da 5 dawn, one hour on each side of sunrise; M 5 morning, dawn to noon; A 5 afternoon, noon to dusk; Du 5 dusk, one hour on each side of sunset. From Dorka (1966).

Although most species within a family seem consistent in their migratory behaviour, occasional telling exceptions occur, with the tendency to nocturnal migration increasing with migration distance (Dorka, 1966). For example, most species of Emberiza buntings in Europe migrate by day over short distances, but the Ortolan Bunting E. hortulana migrates by night over long distances to reach wintering areas in Africa south of the Sahara. Most pipits migrate by day, but the long-distance Tawny Pipit Anthus campestris, which winters in Africa, migrates mainly by night (Briedis et al., 2020), while the Tree Pipit A. trivialis, which also winters in Africa, migrates mainly by day in northern Europe, but further south moves increasingly to nocturnal migration. Similarly, most pigeons migrate by day over short distances within Europe, but the European Turtle Dove Streptopelia turtur migrates mainly by night over long distances to Africa. In addition, Willow Warblers Phylloscopus trochilus are more nocturnal than Common Chiffchaffs P. collybita, and Common Redstarts Phoenicurus phoenicurus more than Black Redstarts P. ochrurus (Figure 4.6). In both these species pairs, the first mentioned species migrates much further than the second. The division between day and night migrants is most obvious from take-off times, with diurnal migrants leaving in the morning and nocturnal ones in the evening. However, whether day or night, landbirds of both groups must continue flying if they find themselves over water, as must waders and waterfowl over dry land. This explains the appearance of typical day migrants, such as Eurasian Skylarks Alauda arvensis, at lighthouses at night, or of typical night migrants, such as chats and warblers, arriving on the coast around mid-day in bright sunshine. Someone watching thrushes and warblers fly ashore from the Gulf of Mexico in spring might understandably class these birds as diurnal migrants, when in fact they set off after sunset one evening, and took more than one night to complete their non-stop flight. Barn Swallows Hirundo rustica are viewed as typical daytime migrants, feeding on the wing as they go and spending their

64

The Migration Ecology of Birds

nights in large roosts; but they may occasionally turn up at watch points at night, and when crossing the Sahara, they commonly set off and travel in the cool of the night (Chapter 6; Schmaljohann et al., 2007). Moreover, beyond the Arctic Circle, all bird movements for a period in summer inevitably occur in daylight. Thus, whether a species is perceived as a day-migrant or a night-migrant depends partly on the locality, whether the species is seen near the start or end of its journey, and whether there are other reasons for flying at a particular time. It is not impossible that birds could become increasingly nocturnal in migratory behaviour along a gradient from facultative short-distance migrants to obligate long-distance migrants, producing differences between closely related species and also between different populations of the same species. This is another aspect of migration that warrants more study. The main supposed advantages of nocturnal migration are that: (1) more time is left for feeding by day, the only time that most birds can feed, so the entire journey can be accomplished more quickly than by diurnal migration; (2) temperatures are lower at night than in the day which could help to prevent over-heating and dehydration in warm regions; (3) humidity is usually higher at night and early morning, which could further reduce dehydration risk; (4) energy demands are lower, because it costs less to fly in cooler denser night air than in warmer daytime air; (5) wind speeds are generally lower at night, thus reducing the effects of headwinds or crosswinds, and vertical turbulence is less, further reducing the energy costs of flight; (6) the use of stars for navigating is possible; and (7) the likelihood of predation during flight is much reduced. The main threat to flying migrants is from falcons or eagles during the day (plus gulls over water), but a wide range of other raptors take migrants at stopovers. Owls do not normally fly high enough to encounter migrants and in any case seldom catch prey on the wing. The reduced turbulence at night must greatly lessen the energy costs of flight, especially in small birds (Kerlinger & Moore, 1989). Even diurnal migrants concentrate their flight into the first and last few hours of the daylight period, when turbulence is much less than in the warmer middle part of the day. Among small birds, only swallows and swifts, which are adapted to fly throughout the day regardless of turbulence, seem to migrate at similar intensity throughout the daily light period. Among larger birds, soaring species migrate mainly through the middle part of the day, a period when thermals are best developed and progress is most rapid (Chapter 7). The various advantages of night-flying are so obvious that it is hard to imagine why some birds migrate primarily by day (apart from those dependent on thermals). Excluding the soaring species, diurnal migrants mostly travel short distances overall, and restrict their flight to brief favourable periods. In flying by day, they also gain a clear view of the terrain below which may help in recognizing familiar landmarks and staying on course, in finding areas of favourable habitat or already-established feeding flocks. Some diurnal migrants, such as hirundines, migrate on a fly-and-forage strategy, picking up food items as they travel. During passage across regions with poor refuelling prospects, the optimal strategy may be to fly non-stop day and night if conditions permit (Alerstam, 2009). As found from radar studies, diurnal migration usually starts up to an hour before sunrise (when colour vision returns), builds to a peak in the two hours after sunrise and then declines from late morning to early afternoon, but occasionally with a slight resurgence in the late afternoon (Dorka, 1966; Bruderer, 1999). The times when diurnal migrants are resting and feeding is usually when air turbulence is greatest, imposing extra costs on flight. Hummingbirds with their specialized flight are unusual in migrating largely during the mid-day period, leaving time for feeding in the morning and evening, but those that cross the Gulf of Mexico fly at night. These tiny birds are more constrained than most in obtaining enough energy per day, and in responding to the diurnal pattern of nectar production on which they depend. Nocturnal migrants mostly set off around dusk in the hour after sunset. Dusk is the time when colour vision goes, but when birds have maximum opportunity to integrate diurnal and nocturnal navigational clues (Chapter 11). Overland migrants studied by radar reach peak densities and altitudes 1 2 hours later, well before midnight. Typically, the volume of migration remains high during the first half of the night, then declines from around 2 a.m. to mid-morning, as increasing numbers of birds settle. As found by radar, the behaviour of nocturnal migrants can change during the night, seemingly as their motivation wanes. Directional preferences are much stronger during the early part of a flight, around dusk, than towards its end during the following morning (Bruderer, 2001). Night migrants tracked in a coastal area became less likely to strike out over the sea and more likely to veer along the coastline as the night progressed; they also flew at lower altitudes and lower speeds, and increasing proportions flew in reverse directions. All these changes may have been responses to diminishing body reserves, or shifting compromises between straight flight and risk avoidance, depending on prevailing conditions (Bruderer & Liechti, 1998). The frequent finding that flight tracks are less variable over the sea than over land may be explained if only the most highly motivated straight-flying birds continue out to sea, while others settle, fly along the coast or turn back inland.

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65

In general, waterfowl seem more variable in their take-off times than most other birds, starting at any time of day or night, but mostly around sunset. Night-migrating shorebirds mostly set off in the 2 3 hours before sunset, depending to some extent on the state of the tide.

REVERSE MIGRATION Migratory flights in directions opposite to those expected occur commonly in both spring and autumn. They have been explained as responses to adverse weather (with birds turning back when conditions ahead are bad), as orientation errors, or as attempts to correct previous orientation errors or wind drift or over-shooting, with birds back-tracking to a point on route (for example see Pennycuick et al., 1996). When reverse movements occur at coasts, they have also been interpreted as attempts by birds with small fuel reserves to feed inland and increase their reserves before setting out over water (Alerstam, 1978b). By moving inland, the argument goes, the birds avoid the high competition, depleted food supplies or predation risk caused by the build-up of birds near the coast. Inland, birds can accumulate body reserves more rapidly and safely. To judge from recoveries of 20 passerine species ringed in southern Sweden in autumn, reverse movements varied between 9 and 65 km, and species with small fat reserves were more likely to per˚ kesson et al., 1996). Moreover, among Common form reverse movements than were species with larger reserves (A Chaffinches Fringilla coelebs and Bramblings F. montifringilla in the same area, the peak in reverse movements occurred about 3.5 hours after early morning departures in the normal direction; and the average weights of reverse migrants and of birds lingering at the coast were lower than those of birds of the same species that proceeded in the normal direction (Lindstro¨m & Alerstam, 1986). In a later autumn study at the same site of mainly nocturnal migrants, birds flying in the migratory direction were more likely to be fat and adult, while those making reverse movements were more likely to be lean and juvenile (Nilsson & Sjo¨berg, 2016). Reverse migration was also more common under overcast skies and winds with north and east components. No effect was found of temperature, visibility, predation risk (as indicated by Eurasian Sparrowhawk Accipiter nisus numbers), or the total number of birds ringed at the site on the day of departure (taken as a measure of potential competition). Reverse migration was characterized by slower flight speeds (airspeed) and occurred at higher altitudes and later in the night than forward migration. These reverse movements are distinct from those described above which occur after nights of drift and take the birds in a direction (usually east or west) that would get them back on their preferred route. In spring, if birds encounter snow or other bad weather on route or after arrival in breeding areas, they may retreat for some distance in the direction of their wintering areas, providing that body reserves permit (e.g., Ga¨tke, 1895; Sva¨rdson, 1953). Many thousands of birds can be involved in such movements. The birds can advance again with the next warm front, and at times of alternating mild and cold periods, back-and-forth shuttle movements sometimes ensue until birds can eventually settle in their nesting areas. The same occurs among birds that breed on high mountains, which having settled on their breeding areas in spring, move down-slope during spells of bad weather and back again when conditions improve. In northern Europe, the Northern Lapwing Vanellus vanellus is one of the earliest species to return each spring, and is well known for reverse migration. The first individuals to arrive on the coast of Finland in spring often turn back on the same day if they encounter cold and snow. One spring, more than 10,000 individuals per day were counted moving southwest across one 10-km stretch of coast (Vepsa¨la¨inen, 1968). In autumn, when birds generally move towards warmer climes and better feeding conditions, adverse weather is likely to play a smaller role, with journeys less disrupted. Although reverse movements often occur on the same days as normal movements, they are often at different altitude, with birds selecting wind conditions appropriate to their flight direction. They differ from those directed movements which also occur in the mornings but serve to get drifted birds back on course, as discussed above.

DETOURS As will be clear by now, migratory birds do not always travel on the shortest routes between breeding and wintering areas, but for one reason or another take longer or roundabout routes. Suggested explanations include: (1) the difficulty in maintaining straight routes; (2) the geometry of travelling on a globe (constant geographical courses are detours on a sphere), (3) the need for following winds; (4) the need for updrafts or thermals; (5) the advantage of avoiding mountains, watercrossings or other obstacles; and (6) the need to stay within suitable habitat and to use profitable stopover sites that lie off

66

The Migration Ecology of Birds

the most direct route. Tracking studies have shown how much further than the shortest route some species travelled on migration (Table 4.2). Figures varied greatly between studies, but many birds travelled more than half as far again as the shortest route, and in species in which different age-groups were followed, juveniles deviated more than adults from the shortest route. For example, among Golden Eagles Aquila chrysaetos migrating through eastern North America, adults migrated distances 27% longer than the shortest route, sub-adults 52% longer and juveniles 67% longer (Miller et al., 2016a). These age differences presumably reflect the effects of learning. In addition to these examples, sea-ducks often migrate long distances around coastlines rather than taking overland short-cuts between breeding and moulting or wintering areas. For example, most Common Eiders Somateria mollissima breeding on islands far up the St. Lawrence River in eastern Canada flew a coastal route of 2250 km to reach a point on the coast of Maine scarcely 640 km distant from their nesting islands, an overland shortcut taken by only a minority of individuals (Reed, 1975). Because many birds have the same requirements on migration, avoiding or minimizing water crossings, ice-sheets, mountain ranges or other barriers, the routes of different species tend to converge, and the same geographical locations serve as staging areas for many different species. The result is that migration does not run evenly across the globe but, under the influence of topographic, atmospheric and seasonal conditions, migrants tend to concentrate into welldeveloped streams. This is especially true of soaring species which each year take the same routes which provide good lift and the shortest possible water-crossings (Chapter 7).

TABLE 4.2 Distance (km) travelled in relation to shortest possible distance in various species tracked from start to finish on migration. Each figure is an average, based on samples of at least five tracked birds. Ratios below show actual route/shortest route, calculated where necessary from a “straightness index” given in some studies as shortest route/actual route. A 5 adult, J 5 juvenile, SA 5 sub-adult. Most of the species listed below have to cross or circumvent the Gulf of Mexico or the Mediterranean Sea followed by the Sahara Desert. Autumn

Spring

Source

Actual route

Shortest route

Ratio

Actual route

Shortest route

Ratio

Golden-winged Warbler Vermivora chrysoptera, A

4144

3552

1.17

4575

3552

1.29

Kramer et al. (2017) (M)a

Golden-winged Warbler Vermivora chrysoptera, A

4710

3172

1.48

5228

3172

1.65

Kramer et al. (2017) (T)a

Golden-winged Warbler Vermivora chrysoptera, A

6748

3742

1.80

7212

3742

1.93

Kramer et al. (2017) (P)a

Pacific Swift Apus pacificus, A

9015

6660

1.30

10121

7440

1.36

Ktitorov et al. (2022)

Barn Swallow Hirundo rustica

10423

7179

1.45

11288

7179

1.57

Hobson et al. (2015) (NB)a

European Nightjar Caprimulgus europaeus, A

7932

7776

1.02

8039

7776

1.03

Norevik et al. (2017)

Barn Swallow Hirundo rustica, A

4805

3674

1.31

4528

3674

1.23

Hobson et al. (2015) (WS)a

Barn Swallow Hirundo rustica, A

10483

8481

1.23

10663

8946

1.19

Briedis et al. (2018a,b,c)

European Roller Coracias garrulus, A

9407

6672

1.41

Rodrı´guez-Ruı´z et al. (2014) (NS)a

European Roller Coracias garrulus, A

8667

7046

1.23

Rodrı´guez-Ruı´z et al. (2014) (SS)a

Eurasian Whimbrel Numenius phaeopus, A

11848

9952

1.19

11609

9952

1.17

Kuang et al. (2020)

Eurasian Whimbrel Numenius phaeopus, A

11848

9952

1.19

11609

9952

1.17

Kuang et al. (2020)

Eurasian Spoonbill Platalea leucorodia, A

1990

1552

1.28

1897

1593

1.28

Xi et al. (2021) (WM)a (Continued )

Weather and migration Chapter | 4

67

TABLE 4.2 (Continued) Autumn

Spring

Source

Actual route

Shortest route

Ratio

Actual route

Shortest route

Ratio

Peregrine Falco peregrinus, A

5492

4987

1.10

5702

4987

1.14

Sokolov et al. (2018)

Eleonora’s Falcon Falco eleonorae, A

7139

5749

1.24

7245

5845

1.24

Hadjikyriakou et al. (2020)

Snail Kite Rostrhamus sociabilis, A

3170

2670

1.19

3417

2723

1.25

Jahn et al. (2021)

Egyptian Vulture N. percnopterus, A

4843

3265

1.48

5304

3460

1.53

Buechley et al. (2018)

Egyptian Vulture N. percnopterus, J

5803

3298

1.76

6966

3274

2.13

Buechley et al. (2018)

Egyptian Vulture N. percnopterus, A

3256

2745

1.19

3580

2866

1.25

Lo´pez-Lo´pez et al. (2014)

Osprey Pandion haliaetus, A

6991

5994

1.17

6175

5650

1.09

Va¨li & Sellis (2015)

Osprey Pandion haliaetus, A

6026

5149

1.17

Babushkin et al. (2019)

Osprey Pandion haliaetus, A

6336

5612

1.13

Monti et al. (2018)

Osprey Pandion haliaetus, J

6022

4534

1.33

Monti et al. (2018)

Golden Eagle Aquila chrysaetos, A

2156

1698

1.27

2221

1915

1.16

Miller et al. (2016a,b)

Golden Eagle A. chrysaetos, SA

3300

2171

1.52

2695

1967

1.37

Miller et al. (2016a,b)

Golden Eagle A. chrysaetos, J

2189

1311

1.67

3504

2384

1.47

Miller et al. (2016a,b)

Osprey Pandion haliaetus, A

6557

5169

1.17

Anderwald et al. (2021)

Osprey Pandion haliaetus, J

5359

4341

1.23

Anderwald et al. (2021)

Key: M 5 Minnesota, NB 5 New Brunswick, NS 5 northern Spain, P 5 Pennsylvania, SS 5 southwest Spain, WM 5 West Mongolia only, WS 5 Washington State.

a

SUMMARY The numbers of diurnal migrants seen on the move or on the ground by day constitute a variable proportion of the total participants. This is because most migration occurs at night or too high by day to be seen through binoculars. Radar is therefore the best method for studying the day-to-day volume of migration, and its relationship with weather. As found mainly by radar studies: (1) the intensity of migration is influenced positively by clear skies and following winds, and negatively by mist, rain and opposing winds; (2) to some extent most migrants adjust their flight altitudes to seek the most favourable winds; (3) birds can compensate for weak lateral winds and remain on course, but they may drift increasingly off course with stronger crosswinds or at high flight altitudes, and more by night than by day; (4) birds that migrate by flapping flight usually travel on a broad front, although low-flying migrants may be temporarily deflected by topographical features into apparent streams; and (5) among nocturnal migrants adjustments to coastlines increase during the night, as landbirds become more reluctant to strike out over water. Drifted birds can re-orientate after skies clear and wind becomes more favourable. Raptors and other landbirds that migrate mainly by soaring flight provide exceptions to some of these generalizations, because of their dependence on thermals and other updrafts. Wind is among the most important environmental factors shaping bird migration patterns, as birds can benefit from tailwinds, suffer from headwinds, and must deal with the displacement caused by crosswinds. Their reaction to crosswinds can vary according to wind speed, flight mode, migratory season, experience, and length and stage of journey. Global wind patterns which are consistent from year to year influence large-scale bird migration patterns over land and sea, and often result in birds taking round-about routes (rather than shorter direct routes) between their breeding and wintering areas. Birds thereby reach their target areas more cheaply and sometimes more rapidly than if they had taken the shortest, more energy-demanding or risk-prone routes. Winds seem to shape some of the loop migrations widespread among long-distance migrants.

68

The Migration Ecology of Birds

Within their normal limits, birds seem to fly at altitudes that offer the best wind conditions for their progress, although some large species apparently for energetic or physiological reasons seem restricted to relatively low altitudes (,1 km). With increasing height above ground, travel speeds increase and predation risks decline, but the atmosphere thins and temperature plummets. The height of bird migration varies with geographical location, topographical situation, weather, day or night, type of flight (flapping or gliding), and species. Some species have been recorded at heights of several kilometres above sea level, and some around 8 9 km. Some types of birds migrate primarily by day and others primarily by night. In general, all species in particular bird families (if they migrate at all) behave the same way in this respect, but some closely related families behave differently from one another, and within some genera, most nocturnal flight occurs among species that make the longest journeys. By migrating at night, birds can avoid predators and loss of feeding time by day, and travel in less turbulent (less energy demanding) conditions. Mainly in order to avoid difficult areas or weather, most birds that have been tracked on migration flew considerably further than the shortest route.

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Tucker, V. A. (1969). Respiratory exchange and evaporative water loss in the flying Budgerigar. J. Exp. Biol. 48: 67 87. Thorup, K., Fuller, M., Alerstam, T., Ha˚ke, M., Kjelle´n, N. & Strandberg, R. (2006a). Do migratory flight paths of raptors follow constant geographical or geomagnetic courses? Anim. Behav. 72: 875 80. Thorup, K., Ortvad, T. E. & Rabøl, J. (2006b). Do Nearctic Northern Wheatears (Oenanthe oenanthe leucorhoa) migrate nonstop to Africa? Condor 108: 446 51. ¨ . & Sellis, U. (2015). Migration patterns of the Osprey Pandion Va¨li, U haliaetus on the Eastern European East African flyway. Ostrich 87: 1 6. Van Doren, B. M., Horton, K. G., Stepanian, P. M., Mizrahi, D. S. & Farnsworth, A. (2016). Wind drift explains the reoriented morning flights of songbirds. Behav. Ecol. 27: 1122 31. Van Doren, B. M. & Horton, K. G. (2018). A continental system for forecasting bird migration. Science 361: 1115 18. Vansteelant, W. M. G., Kekkonen, J. & Byholm, P. (2017). Wind conditions and geography shape the first outbound migration of juvenile Honey Buzzards and their distribution across sub-Saharan Africa. Proc. R. Soc. B 284: 1855. Vansteelant, W. M. G., Gangoso, L., Bouten, W., Viana, D. S. & Figuerola, J. (2021). Adaptive drift and barrier-avoidance by a flyforage migrant along a climate-driven flyway. Movement Ecol 9: 37. Vansteelant, W. M. G., Bouten, W., Klaassen, R. H. G., Koks, B. J. Schlaich, A. E. et al. (2015). Regional and seasonal flight speeds of soaring migrants and the role of weather conditions at hourly and daily scales. Avian Biol 46: 25 39. Vepsa¨la¨inen, K. (1968). The effect of the cold spring 1966 upon the Lapwing Vanellus vanellus in Finland. Ornis Fenn 45: 33 47. Wainwright, C. E., Stepanian, P. M. & Horton, K. G. (2016). The role of the US Great Plains low-level jet in nocturnal migrant behavior. Int. J. Biometeorol. 60: 1531. Weimerskirch, H., Louzao, M., de Grissac, S. & DeLord, K. (2012). Changes in wind pattern alter albatross distribution and life-history traits. Science 335: 211 14. Weimerskirch, H., Delord, K., Guitteaud, A., Phillips, R. A. & Pinet, P. (2015a). Extreme variation in migration strategies between and within Wandering Albatross populations during their sabbatical year, and their fitness consequences. Sci. Rep. 5: 8853. Weimerskirch, H., Tarroux, A., Chastel, O., DeLord, K. & Cherel, Y. (2015b). Population-specific wintering distributions of adult South Polar Skuas over three oceans. Mar. Ecol. Prog. Ser. 538: 229 37. Williams, T. C. & Williams, J. M. (1990). The orientation of transoceanic migrants. Pp. 7 21 in Bird migration. Physiology and ecophysiology in Bird migration. Physiology and ecophysiology (ed. E. Gwinner). Berlin, Springer-Verlag. Williams, T. C., Williams, J. M., Ireland, L. C. & Teal, J. M. (1977). Bird migration over the western North Atlantic Ocean. Am. Birds 31: 251 67. Xi, J., Deng, X., Zhao, G., Batbayar, N. Damba, I. et al. (2021). Migration routes, behaviour and protection status of Eurasian Spoonbills (Platalea leucorodia) wintering in China. Avian Research 12: 70.

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Chapter 5

Fuelling migration

Garden Warbler (Sylvia borin) fattening on elder berries All creatures are fatter in migrating. Aristotle, writing 2300 years ago.

For migration, many birds put on extra body fat and other reserves for use as fuel during the journey. Typically, they divide their migration into periods of flight, during which reserves are depleted, and stopovers, when reserves are replenished by feeding. Species that travel over favourable terrain tend to migrate in short flights, each lasting up to several hours, broken by periods of rest and foraging, when they can replace the relatively small amounts of fuel used on each stage. In contrast, birds that migrate over large inhospitable areas have to sustain much longer fasts of up to several days, which are preceded by days or weeks of feeding to accumulate the larger body reserves required. Whether short or long flights, however, energy is lost much more rapidly during flight than it can be replenished by feeding. The alternating activities of fuelling and flight have different demands. During fuelling, the bird should be an efficient eating machine, with a large digestive system, able to process larger-than-normal quantities of food for rapid conversion to stored energy. But during flight, it must be an efficient exercise machine, with large muscles, well-functioning lungs, heart and circulatory system. It should carry enough energy-rich fuel for the journey, but a minimum of other body structures that merely add unwanted weight. Some long-distance migrants can greatly alter their internal body structure over a matter of days, as they switch from fuelling to flight mode and back again. All muscles and body organs are energetically costly to maintain, so an ability to change their relative sizes rapidly, according to the needs of the time, forms an important adaptation, not just for migration but also for other events in the annual cycle. Such ‘phenotypic flexibility’ enables disparate activities to be performed more efficiently than would be possible on fixed metabolic and body structures (Piersma & Lindstro¨m, 1997). In addition to fuel deposition, preparation for migration in many birds involves enlargement of the breast muscles, heart and blood vessels, and shrinkage of other organs less important in migratory flight (Piersma et al., 1999). It also involves the activation of enzyme systems for the storage and mobilization of fat, increase in the erythrocyte (haematocrit) content of the blood to enhance oxygen transport (Thapliyal et al., 1982; Jenni-Eiermann & Jenni, 1991) and modifications of behaviour to permit nocturnal flights in some otherwise diurnal species (Chapter 4). This chapter is concerned with the types and amounts of fuel accumulated by birds, with the process of fuelling and changes in body composition, and with how these features vary with the types of journeys undertaken. The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00016-6 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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ENERGY NEEDS AND BODY COMPOSITION Fat provides much more energy per unit weight than any other potential storable fuel. The use of 1 g of fat will yield around 9.2 kcal (or 38 kJ) of energy compared with only about 1.3 kcal (5.3 kJ) from 1 g of protein or 1 kcal (4.0 kJ) from 1 g of carbohydrate (Table 5.1). So weight for weight, fat contains 7 9 times more energy than alternative fuels, and thus provides the maximum energy storage for minimum weight gain. Fat is an even more efficient fuel than highoctane vehicle fuel, and its oxidation yields an equal weight of water, thus contributing to another of the bird’s needs during long-distance flights. Fat not only can be stored without water or protein but also can be metabolized efficiently with less loss of heat and no effect on body glucose. The main drawback of fat is that its metabolism requires the breakdown of small amounts of protein to provide enzymes for the chemical processes involved (the citric acid cycle). In addition, while most tissues in the body can oxidize fatty acids to release energy, some tissues rely instead on carbohydrate or ketone bodies (a reduced form of fatty acids) for energy. Such tissues include the brain and nervous system, red and white blood cells and the kidney medulla. Fat is laid down as adipose tissue (called fat bodies) in various parts of the bird’s body, especially under the skin, and in well-defined deposits within the wishbone (tracheal pit) and around the gut. At least 15 distinct fat depots have been described in passerines (King & Farner, 1965). Just before departure, the subcutaneous fat layer in some long-distance passerine migrants can be so extensive that most of the body appears to be clad in a thick layer of pale-yellow fat. This fat is relatively soft, even at body temperature; and in the hand the bird appears strangely spongy. The precise composition of the fat varies to some extent with the diet of the bird, and with the part of the body where it is stored; but in those species studied (mostly passerines), it consists largely of unsaturated fatty acids, especially oleic, linoleic and palmitic acids, mostly stored in the form of triglycerides (McWilliams et al., 2004; Pierce & McWilliams, 2005). This consistency across species is surprising given the diverse feeding habits of the species involved, suggesting that birds may be selective in their diets and in the fatty acids they lay down as fuel. Captive birds have shown dietary preferences for unsaturated over saturated acids, and for short-chain over long-chain compounds (McWilliams et al., 2004). The pectoral muscles of birds may form more than a third of total body mass and consist predominantly of fast oxidative-glycolyic fibres, which are able to beat the wings continuously at high frequencies for hours or days on end. The flight muscles of many birds are adapted to use fatty acids for energy. They are highly vascularized, with greater capillary-to-fibre ratio than other muscles except the heart (Butler & Woakes, 1990), and are well supplied with mitochondria and aerobic enzymes for the oxidation of fatty acids (Ramenofsky, 1990). In fact, the smallest fibres and greatest capillary densities are found in the flight muscles of birds which migrate the longest distances (Lundgren & Kiessling, 1988). Fatty acids are transported from adipose tissue to flight muscles by the bloodstream, bound either to albumin or to lipoproteins. During long flights, power is produced almost entirely from aerobic metabolism, the respiratory and cardiovascular systems supplying the necessary fuels and oxygen, and also removing the various metabolic end products (eg carbon dioxide and heat). An idea of the amount of fuel deposited by migratory birds can be gained from their body weights (comparing individuals at different stages of fattening; Figure 5.1), and from their ‘fat scores’ based on the yellowish fat that can be seen through the skin of a live bird when the feathers are blown aside. Most such studies record the fat in the furculum

TABLE 5.1 Energy and water yield of the three main fuel types in birds. Lipids in adipose tissue

Protein in skeletal muscle or digestive organs

Glycogen

Energy density (kJ/g) in dry mass

39.6

17.8

17.5

Energy density (kJ/g) in wet mass

37.6

5.3

3.5 4.4

Water content (%)

5

70

75 80

Metabolic water production (g water/g dry matter)

1.05

0.39

0.56

Total water production (g water/g wet tissue)

1.10

0.82

0.89 0.91

Water produced (g water/kJ expended from wet mass)

0.03

0.16

0.21 0.25

Note: 1 kilojoule (kJ) is equivalent to 0.239 kilocalories, and a kilocalorie is popularly called a ‘calorie’ in human dieting. Source: Modified from Jenni & Jenni-Eiermann (1998).

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Body mass (g)

FIGURE 5.1 Body mass changes, reflecting pre-migratory fuel deposition, in male White-crowned Sparrows (Zonotrichia leucophrys gambelii) caught repeatedly in autumn in California. The maximum rate recorded was from a bird which went from 26.5 to 30.4 g in 22.5 h, a 14.7% increase. From Morton (2002).

Adult males Juvenile males

34

75

32 30 28 26 24 22 20 10

20 September

30

10

20 October

30

(wishbone), which appears as a V-shaped hollow at the base of the neck on the underside. Such scores are useful but do not bear a linear relationship to the total fat in the bird’s body; and nor are they comparable across species. But they can be recorded without harm from live birds and can be used for comparisons within species. More detailed studies of fuel deposition have involved analyses of bird carcasses to find the relative proportions of fat, water and lean dry material (the latter comprising mainly body protein, feathers and skeleton) (Table 5.2). Such studies have shown how the body composition of particular species changes over the course of migration, and how these changes vary between species, according to the types of journeys undertaken. Some studies have also examined the composition of different components of the body separately, such as the various muscles and digestive organs (see later).1 Resident bird species, or migrants outside the migration seasons, typically contain fuel (mostly fat) amounting to 3% 5% of their lean body mass. Some migrants apparently travel with reserves no greater than this. However, most regular passerine migrants depart with fuel loads amounting to 10% 30% of their lean body mass, and those making especially long flights accumulate fuel loads between 40% and 70% of their lean mass, approaching 100% in a few species (Fry et al., 1970; Moreau & Dolp, 1970; Alerstam & Lindstro¨m, 1990). Similarly, some shorebirds attain very large fuel loads, as high as 50% 90% of lean body mass, but with a maximum of around 100% in those embarking on the longest non-stop flights. They may thus double their body mass before departure and then lose up to half their body mass during flights over the next few days. Pre-migratory weight increase involves the deposition of body protein as well as fat, so fuel should be regarded as a combination of the two. In the most extreme species, protein contents increase prior to migration by less than twofold, whereas fat contents may increase in parallel but by more than 10-fold. Sandhill Cranes (Antigone canadensis) at migration times add protein and fat in the approximate ratio of 1:10 (Krapu et al., 1985), but some other migratory birds lay down approximately equal weights of protein and fat in the ratio of 1:1 (see later). This variation may result partly from the diets of different species, but in some species also from their needs at different seasons. For example, the 40 50-g mass gain by 200-g European Golden Plovers (Pluvialis apricaria) during autumn stopovers consists almost entirely of fat, but a similar mass gain in spring consists mainly of muscle protein. This seasonal difference may occur because Golden Plovers face energy deficits in autumn and winter when they eat mainly protein-rich earthworms, but protein deficits in spring after arrival in arctic breeding areas when they eat mainly berries left over from the previous year but must soon produce eggs (Piersma & Jukema, 2002). Populations that are obliged to make long non-stop flights are presumably under greatest pressure to maximize their dependence on fat, rather than carbohydrate or protein. Particular bird species can vary across their breeding range in the amount of fuel accumulated, according to the journeys made. For example, three races of Quelea quelea, inhabiting eastern, western and southern Africa respectively; each migrates at the start of the wet season but accumulates different amounts of fat and protein according to the distances travelled (Ward & Jones, 1977). Similarly, among Barn Swallows (Hirundo rustica), the pre-migratory fuel stores accumulated in autumn at different localities in the Mediterranean region match the distances to be covered across sea and desert (Rubolini et al., 2002). Among the Northern Wheatears (Oenanthe oenanthe) that pause in spring

1. The following terms are commonly used by researchers studying migratory fattening: live weight (of the living bird), fresh weight (of a carcass preserved without evaporative water loss, and therefore equivalent to live weight), dry weight (fresh weight minus the water component of the body), lean (or fat-free) weight (fresh weight minus the entire fat component of the body), lean dry weight (fresh weight minus the lipid and water components), and fat (lipid) weight (of the lipid component). In this field of study, the terms fat and lipid are usually used interchangeably (as here), as are the terms weight and mass, and body stores and body reserves.

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on Heligoland Island, birds of the nominate race, which breed over much of Europe, mostly stop and feed for up to a day before moving on, whereas birds of the larger Greenland race usually stay for 10 17 days, building up larger reserves for their long oversea flights (Delingat & Dierschke, 2000). At least 5% 10% of the total energy released during a migratory flight must come from protein to satisfy requirements in the breakdown of fat (Jenni & Jenni-Eiermann, 1998). Hence, the amount of protein metabolised depends partly on the amount of fat metabolised. The protein is obtained not only from the flight muscles but also from other organs, including the gut, body and leg muscles (Piersma & Gill, 1998). However, because the fat fraction contributes so much of the total energy needs, its metabolism has much more influence than protein on the overall flight range. Although protein breakdown is essential for fat metabolism, there are at least two reasons why birds should minimize its use as fuel. First, as mentioned above, wet protein holds only about one-seventh as much energy as the same weight of fat (Table 5.1; Jenni & Jenni-Eiermann, 1999), so per unit weight it is a much less efficient fuel. Second, the metabolism of protein is more complex and inefficient than the breakdown of fat and carbohydrate and also results in toxic by-products. If protein is deposited as a major fuel, therefore, there must presumably be some other reason. Among other things, it supplies important precursors and intermediaries for other physiological processes (McWilliams et al., 2004), but particularly in spring it contributes to egg formation in some species (see later). Its breakdown releases 0.8 g of water per gram of wet protein compared with 0.9 g of water per gram of wet carbohydrate and 1.1 g of water per gram of fat (Table 5.1). Carbohydrate is present as glycogen in the liver and muscle tissue but occurs in such small quantities at migration times that it is of little importance as an energy source. The highest glycogen values reported from birds are about 3.0% of liver mass and about 0.5% of total body mass (Marsh, 1983; Blem, 1990). As they begin to prepare for migration, some small passerines change their metabolism from mainly carbohydrate-based to mainly fat-based (Dolnik & Blyumental, 1967; JenniEiermann & Jenni, 1996). The liver then declines in weight through the reduction in glycogen reserves and shows less diurnal fluctuation. It becomes increasingly involved in lipogenesis, with lipids obtained directly from food or synthesized in the liver itself. They are then transported as lipoproteins in the bloodstream to the adipose tissue. The lipid is hydrolyzed and stored ‘dry’. This is in contrast to carbohydrate and protein, the storage of each gram of which requires 2 5 g of extra water (Table 5.1; Blem, 1990). This is a substantial weight burden, but because some of the water is released during their metabolism, it may help to counter dehydration on long journeys. So while prior to migration, glycogen is a major source of stored energy, fat becomes by far the main source as departure approaches. Because very little fuel can be stored within the working muscles, their metabolic needs are met chiefly by continuous input of fuel materials via the blood system. Of the three fuel types, carbohydrate (glycogen) is the most readily mobilized. Based on evidence from pigeons, the different types of fuel are not used in similar ratio throughout a flight. Carbohydrates are mainly used at the start for the initial take-off and climb, while fatty acids reach their steady-state contribution after 1 2 hours of flight, and amino acids from tissue protein after 4 5 hours (Nachtigall, 1990; JenniEiermann & Jenni, 2003). In birds with a fat content of more than 25%, only about 5% of the energy is derived from protein, but this proportion increases during a journey as fuel is consumed. Once the fat content falls below 5%, about 20% of flight energy derives from protein. This trend has been observed within species, as well as in comparisons between species (Jenni & Jenni-Eiermann, 1998). Eventually, as the fat reserves dwindle, metabolism switches even more to protein, and starvation sets in (Schwilch et al., 2002). Breakdown of adipose tissue has little adverse side effect besides reducing energy stores and, to a small extent, body protein. But the use of too much protein could result in some functional or structural loss, because protein is stored as an integral component of body tissues. A reduction in the digestive organs (consisting mainly of muscle protein) could result in reduced ability to process food so that refuelling rate is low during the first days of stopover (Biebach, 1998; Piersma, 1998). The complete loss of glycogen stores would render sudden fast flights during stopover impossible, making the bird vulnerable to predator attack or unable to chase mobile prey. To cope with emergencies, the migrant would therefore benefit from conserving some glycogen, or from reconstituting some soon after landing (Jenni-Eiermann & Jenni, 2001, 2003). The notion that species use different ratios of fat and protein during migration is supported by findings from blood analyses of birds caught on migration. At several sites, fruit-eating and nectar-eating songbirds have tended to have higher levels of triglycerides (indicating fat metabolism), while insectivores had higher levels of uric acid (indicating protein metabolism) (Jenni et al., 2000; Gannes, 2001; Jenni-Eiermann & Jenni, 2003). Unanswered questions concern the extent to which migratory birds, with extremely rapid energy deposition, can influence the composition of their stores irrespective of food composition, and how much the composition of stores is controlled by metabolic or nutritional constraints. The composition of migratory fat varies to some extent with diet, but

Fuelling migration Chapter | 5

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some fatty acids can apparently be synthesized, or absorbed and stored selectively (Egeler et al., 2003). Another important question is how birds ‘know’ they have accumulated sufficient body reserve for a migratory flight. They can clearly assess their own body condition, as can mammals, but the mechanism is unknown.

Costs and benefits of body reserves As the body reserves of a bird increase, so does its flight and migration speed and its potential flight range, but not in direct proportion. This is mainly because the extra fuel itself requires energy to synthesize, maintain and transport, so as body reserves increase, so do the flight costs per unit distance travelled (Pennycuick, 1989; Lindstro¨m & Alerstam, 1992; Witter & Cuthill, 1993). These costs are usually measured in terms of basal metabolic rate (BMR, the rate of energy consumption by an inactive bird in a stable state, Chapter 3). The metabolic costs of transporting migratory fuel thus rise and fall in line with body weight. For example, in a captive Thrush Nightingale (Luscinia luscinia), BMR increased in almost direct proportion to body mass. Over 48 hours, BMR increased by 22.7%, in parallel with an increase in body mass of 24.3% (Lindstro¨m et al., 1999). Likewise, some Great Knots (Calidris tenuirostris) on their 5400 km non-stop flight from Australia to China in spring lost about 40% of body weight during the 4-day journey. BMRs measured in birds just before and just after their flight were found to have fallen by an average of 42% in association with the reduction in body mass (Battley et al., 2001a). Clearly, BMR varies considerably within individuals, in association with the rapid changes in their body mass (for other figures for Barnacle Geese (Branta leucopsis) and a Northern Bald Ibis (Geronticus eremite) see Chapter 3) In addition to its maintenance and transport costs, extra fuel makes a small bird less agile and more vulnerable to predation. This is another reason for a bird not to accumulate larger body reserves than necessary. Even the slight weight increase shown by small birds during the course of a normal day greatly reduces their lift-off speed and agility, and birds accumulating migratory fat suffer much greater impediment (Witter et al., 1994; Metcalfe & Ure 1995; Lee et al., 1996; Kullberg et al., 1996, 2000; Lind et al., 1999). For example, when captive Eurasian Blackcaps (Sylvia atricapilla) were exposed to simulated predator attacks, individuals carrying a fuel load equivalent to 60% of lean body mass (the maximum recorded in this species) were calculated to suffer reduction of 32% in angle of ascent and 17% in velocity compared with lean Blackcaps (Kullberg et al., 1996). This degree of difference could put fat birds at substantially greater risk (Lind et al., 1999; Burns & Ydenberg, 2002). These considerations should favour a migration strategy of short flights, frequent fuelling and low fuel loads wherever possible, with the alternative of long flights, infrequent fuelling and heavy fuel loads resorted to only when necessary, when birds are crossing inhospitable areas or in a hurry (time minimizing).

Water balance and thermoregulation Birds migrating long distances over sea or desert cannot drink on their journeys. This could give rise to dehydration, especially in hot conditions, where the birds must pant to remain cool. By panting, birds lose heat through the evaporation of water from the damp inside surfaces of the mouth and nostrils. Because fat is stored anhydrously, body water as a fraction of body weight declines as fat is deposited. For this reason, water content is best expressed in relation to lean dry mass. The ratio between the two is highly variable, but in healthy passerines is usually in the range 2:1 2.4:1. In a study of Eurasian Reed Warblers (Acrocephalus scirpaceus), Fogden (1972) took water levels lower than 2:1 as indicating dehydration and found that 11 out of 80 individuals caught on spring migration in Uganda had water contents below this level. He also calculated that of 409 birds of 11 species obtained on the Egyptian coast after crossing the Mediterranean Sea in autumn (and analysed by Moreau & Dolp, 1970), 78% had water indices lower than 2:1, while as many as 12% had ratios lower than 1.4:1. On the same basis, reduced water levels were also apparent among migrants that had crossed the Gulf of Mexico in spring (Odum, 1960). While these findings would seem to indicate severe dehydration after long flights, Fogden (1972) suggested that in some conditions migrants reduce their water levels before departure. This would enable them to reduce total body weight and cover greater distance on their body fat. This view was reiterated by Johnson et al. (1989) on the basis of the pre-migratory changes in body composition found among Pacific Golden Plovers (Pluvialis fulva) on the Hawaiian Islands, preparing for their flight to Alaska. The question whether low water levels reflect dehydration or adaptation to long flights remains open, but birds with such low water levels would surely have little leeway to counter any overheating by panting (Chapter 6). The body temperatures of birds measured during active flight are generally greater than 41 C, up to 4 C higher than normal (Gessaman, 1990). This may improve muscle efficiency and increase maximum power output (Butler & Woakes, 1990). But during normal sustained flight, birds must dissipate more than eight times as much heat as during rest in order not to become overheated. Overheating is a potential problem for migrants during continuous flights at

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The Migration Ecology of Birds

high ambient temperatures, as occur by day over deserts (Chapter 6). Flying birds lose some heat through convection and radiation, especially through their underwings and unfeathered legs and feet, but the amount of heat that can be lost in this way is limited by simple physical processes. So at higher ambient temperatures, evaporative mechanisms (mainly through panting) play an increasing role. The resulting risk of dehydration can be offset either by metabolic water production (from fat and protein metabolism), by ascent to altitudes where the air is cool enough to keep evaporative heat loss at the required level, or by flight at night when temperatures are lower than during the day (up to about 10 C). The bird might also switch to other energy sources: per unit energy released, protein yields about five times as much water as fat, and glycogen at least seven times as much (Table 5.1).

MIGRATION STRATEGIES Some birds may benefit from migrating as quickly as possible (the ‘time minimization model’ of Alerstam & Lindstro¨m, 1990). This gives migrants the longest possible time on their breeding, wintering or moulting sites, but requires large fuel stores to permit long non-stop flights. Other birds may have food available throughout the migration route so that they can stop and feed almost anywhere. Because heavy fuel loads mean greater transport costs, as mentioned above, one way to save energy is to keep fuel loads small and fly only short distances at a time, refuelling as necessary (the ‘energy minimisation’ model). Moreover, because any extra weight also reduces flight performance (notably climb rate and agility), minimizing fuel loads can also reduce predation risks (the ‘predation minimization’ model). The second and third options can be combined as the ‘load-minimizing’ strategy. The particular migration mode adopted by any population might be a compromise between any of these different options, depending partly on the route taken, on the distribution of potential stopover sites, the speed of refuelling possible at different sites, and on the abundance of aerial predators. Because many birds migrate faster in spring than in autumn in an apparent attempt to reach their breeding areas quickly (Chapter 9), they may travel as time minimizers in spring and as energy (or load) minimizers in autumn (for Golden Eagle (Aquila chrysaetos) see Miller et al., 2016a,b). They might also adopt different strategies in different parts of their journeys, according to the terrain to be crossed, making longer non-stop flights over seas or deserts (for Lesser Black-backed Gull Larus fuscus see Bustnes et al., 2013). However, any ideal strategy that a bird might adopt is likely often to be compromised by external conditions, such as adverse weather, poor food supplies or predation threats, all of which could influence behaviour at the time (Chapter 14). We can think of stopover sites as ‘stepping stones’ in a migratory journey, with the intervening flights taking different forms, which Piersma (1987a,b) termed hop, skip and jump, depending partly on the distances involved. For a load (or energy) minimizer, the best strategy would be to use a large proportion of potential refuelling sites along a migratory route (hopping). But a time minimizer would do better to put on a large fuel load at a high-quality stopover site to by-pass poor-quality sites (skipping). It could then migrate more quickly. A landbird that has to cross a large stretch of ocean can only adopt a ‘jump’ strategy, flying a long distance without feeding. Some shorebird species make non-stop flights of 5000 10,000 km, mostly overwater, and travel between northern hemisphere breeding areas and southern hemisphere wintering areas in 2 3 ‘jumps’ (Chapter 6). Studies of the numbers and durations of stopovers, rates of weight gain, departure weights and flight lengths can indicate the strategy pursued, as can migration speed and distance (see later, Chapter 14). A positive relationship between fuel deposition rate and departure fuel load would be expected in time minimizers, but not in energy minimizers (Figure 5.2; Lindstro¨m & Alerstam, 1992).

Alternative strategies Most studies of migratory fuelling in birds have been concerned with fuel deposition before departure, and its replenishment at stopover sites. But some species intent on carrying as little stored energy as possible might pick up food on the way, and at least two ‘fly-and-forage’ strategies can be distinguished. In one type, birds on the wing may pick food items from the air as they travel, swifts and hirundines being obvious examples. In the other, birds may fly low, continually searching for food and coming down when a prey item is spotted, but all the time continuing along their migration route. Over the whole journey, periods of straight fast flight may be interspersed with periods of slower searching flight, but again remaining on route. This strategy has been noted in various seabirds and raptors (from Cory’s Shearwater (Calonectris borealis) see Dias et al., 2012, for Snowy Owl (Bubo scandiaca), see Ame´lineau et al., 2021). Some other birds appear to depart at normal weight without extra fuel deposition, lose weight during the flight, and make it up after arrival in a stopping area an extreme load-minimizing strategy. Without special reserves, small birds could not survive much more than a day without food, but they could travel in this way on short flights lasting a few hours, followed by feeding. However, large birds, such as swans, geese and eagles, can normally survive for many days

Fuelling migration Chapter | 5

FIGURE 5.2 Relationship between departure fuel load and fuel deposition rate among Eurasian Reed Warblers (Acrocephalus scirpaceus) (open symbols) and Sedge Warblers (Acrocephalus schoenobaenus) (filled symbols) in food supplementation experiments during autumn migration in England (based on Bayly, 2007). Fuel loads and rates are expressed in relation to the birds’ lean body mass. The birds are long-distance migrants with winter quarters in West Africa. Both species showed a distinct positive correlation between departure fuel load and deposition rate, supporting the general importance of time minimization. Based on data from Bayly (2007), modified from Alerstam (2011).

1.4 1.2 Departure fuel load

79

1.0 0.8 0.6 0.4 0.2 0.0 0.00

0.05

0.10 0.15 Fuel deposition rate

0.20

without food, so in theory they could travel for longer periods without prior fuel deposition. This is especially so for soaring birds, which expend little more energy on migration than on normal daily life. Most soaring species that have been studied accumulate relatively small amounts of fuel for overland flight (for raptors see Chapter 7), and no premigratory fattening is apparent in White Storks (Ciconia ciconia) at either season, despite migrations of up to 10,000 km (Berthold et al., 2001). These birds feed as they go, mainly in the mornings and evenings, and travel in the middle part of the day, when the thermals that permit soaring gliding flight are best developed. But they face large stretches of the journey, notably through deserts, when they could not expect to feed for several days. Analyses of the weights of six species of trans-Saharan migrants caught at 34 trapping stations located in widely scattered parts of Europe and North Africa revealed four types of fattening patterns on the southward autumn journey (Schaub & Jenni, 2000): 1. Birds accumulate large fuel stores well before they reach the northern edge of the desert and then fly to sub-Saharan Africa without refuelling. This pattern is shown by western populations of Sedge Warblers (Acrocephalus schoenobaenus) and Pied Flycatchers (Ficedula hypoleuca), and possibly also by some individuals of other species. 2. Birds accumulate more fuel at each stopover than is needed to fly to the next, leading to a progressive increase in body mass southwards through Europe toward the desert. This strategy is shown by Garden Warblers (S. borin) and more eastern populations of Pied Flycatchers. 3. Birds migrate in short stages and accumulate only enough fuel at each stopover site to fly to the next, with especially large amounts just before the desert crossing. This strategy depends on finding good feeding sites in the southern Mediterranean region and is adopted by Eurasian Reed Warblers and possibly also by Common Whitethroats (Curruca communis). 4. The same strategy as (3), except that birds put on only moderate reserves before the desert crossing, relying instead on finding food at desert scrub patches or oases or on catching migrant insects. Various hirundines and Spotted Flycatchers (Muscicapa striata) seem to adopt this strategy, and the same may be true for shrikes which can kill and eat their fellow migrants. However, Barn Swallows (Hirunda rustica) that migrate from Italy across the Mediterranean and Sahara accumulate up to 40% fat before the journey, which is much more than those that take the shorter sea crossing at Gibraltar (Rubolini et al., 2002). Similar patterns occur in spring (Curry-Lindahl, 1963; Ward, 1963; Fry et al., 1972). Most northward-bound passerine species fatten well to the south of the Sahara, and undertake a flight much longer than the desert crossing itself, while others proceed in stages to the southern edge of the desert and fatten there. In West Africa, Garden Warblers are among those that fatten far south of the desert, in the Guinea Zone (Ottosson et al., 2005), while Sand Martins (Riparia riparia) and others fatten further north around Lake Chad in the Sahel Zone (Fry et al., 1972). In East Africa, Sedge Warblers and Great Reed Warblers (Acrocephalus arundinaceus) fatten well south of the Sahara (in Kenya Uganda) and fly 2500 km direct to the Middle East; but most other passerine species probably fatten in Somalia much nearer the desert (Pearson, 1990). Birds cross the Sahara in less than a week but can take 3 or more weeks on travelling through Europe. In North America, Helms & Smythe (1969) recognized similar broad categories with respect to fuel reserves and migration itineraries:

80

The Migration Ecology of Birds

1. Intra-continental migrants vary from (a) those that depart on autumn migration with scant fuel reserves, move relatively slowly, and may (eg, Dark-eyed Junco (Junco hyemalis), Savannah Sparrow (Passercualus sandwichensis)) or may not (eg, American Tree Sparrow (Spizelloides arborea)) add reserves as migration progresses, to (b) those that accrue moderate reserves immediately before departure and migrate fairly rapidly (eg, White-throated Sparrow (Zonotrichia albicollis) in some areas). 2. Inter-continental migrants that behave like intra-continental migrants on the first part of their journey through favourable habitat but accrue much larger reserves in the southern States as they approach the sea crossing (eg, Scarlet Tanager (Piranga olivacea) and Bobolink (Dolichonyx oryzivorus)). The importance of food on route is evident in comparisons between related species. For example, Sedge Warblers travelling from Britain to Africa in autumn attain higher rates of fat deposition close to their breeding areas than further south in the Mediterranean region. Their main prey (reed aphids) reach peak abundance in Britain and northern France at migration time but have already passed their peak in southern Europe by the time the warblers arrive. This may be why Sedge Warblers typically deposit very large fat loads in southern England and northern France, from which areas they could then migrate without feeding to their wintering areas south of the Sahara, on journeys exceeding 3000 km (Gladwin, 1963; Bibby & Green, 1981). In contrast, Eurasian Reed Warblers using the same habitat and route eat a wider variety of insects and can fatten at a bigger range of sites until later in the season. Ring recoveries show that they usually migrate through Europe in shorter stages, stopping at various localities on their southward journeys, and accumulating large body reserves only in North Africa, just before the desert crossing, as described above. In making sea-crossings, such as the Mediterranean and Gulf of Mexico, the length of journey varies greatly according to where birds make the crossing, and variations in their fat contents reflect this variation in departure points (Schaub & Jenni, 2000; Cano et al., 2020). In addition, while some species accumulate little more fat than is needed to reach the other side, others have enough fat to travel well into their target continent. For example, among 16 species studied in northern Colombia in spring, individuals of Gray-cheeked Thrush (Catharus minimus), Yellow-billed Cuckoo (Chrysococcyx megarhynchus), American Yellow Warbler (Setophaga aestiva) and Northern Waterthrush (Parkesia noveboracensis) carried enough fat to take them more than 2500 km (Cano et al., 2020). The remaining species were capable of over-water flights to the Yucatan Peninsula or Cuba ( . 1800 km) or shorter flights to middle Central America ( . 1000 km) and probably required one or more additional stopovers to reach their breeding ranges in North America. These differences may result from regional variations in the foraging opportunities open to the different species. At particular sites, birds sometimes stay longer, fatten more rapidly and to higher levels in autumn than in spring (Dolnik & Blyumental, 1967; Morris et al., 1994), and in other species in spring than in autumn (King et al., 1963, 1965; Butler et al., 1987). For example, some waders migrating between eastern Canada and South America accumulate more body fat in autumn when they make a single long flight over the sea to northern South America, than in spring when they migrate by a series of shorter coastal flights, broken by feeding stops (McNeil & Cadieux, 1972). Similarly, birds pausing at an oasis in the Sinai desert of northern Egypt tended to stay there longer and accumulate more body fuel in autumn before crossing the Sahara, than in spring just after the crossing (Table 5.2). The fattening strategy at each season is evidently adapted to the route taken at each season and the numbers and spacing of further potential fuelling sites. These different patterns must presumably be pre-programmed (Bayly, 2007). TABLE 5.2 Mean estimated stopover periods of various passerines at an oasis in the Sinai desert. The average stopover period in most species was longer in autumn before crossing the Sahara than in spring after crossing it. Autumn

Spring

Species present only in autumn Willow Warbler (Phylloscopus trochilus)

10.8 6 3.9

Western Orphean Warbler (Curruca hortensis)

5.6 6 0.6

Red-backed Shrike (Lanius collurio)

3.7 6 0.5

Common Whitethroat (Curruca communis)

6.6 6 2.3

Yellow Wagtail (Motacilla flava)

4.5 6 1.1

Bluethroat (Luscinia svecica)

13.6 6 7.6 (Continued )

Fuelling migration Chapter | 5

81

TABLE 5.2 (Continued) Autumn Common Reed Warbler (Acrocephalus scirpaceus)

3.0 6 0.4

Whinchat (Saxicola rubetra)

2.3 6 0.5

European Pied Flycatcher (Ficedula hypoleuca)

3.1 6 1.1

Spring

Species more numerous in autumn than spring Lesser Whitethroat (Curruca curruca)a

5.0 6 0.5

1.9 6 0.6

Common Chiffchaff (Phylloscopus collybita)

8.1 6 3.4

2.4 6 0.2

Spotted Flycatcher (Muscicapa striata)

3.5 6 0.7

3.2 6 0.7

Tree Pipit (Anthus trivialis)a

3.6 6 0.2

2.2 6 0.3

Eurasian Blackcap (Sylvia atricapilla)

6.7 6 1.8

3.8 6 0.8

Common Redstart (Phoenicurus phoenicurus)

2.8 6 0.6

3.3 6 0.3

1.7 6 0.7

1.5 6 0.2

Species more numerous in spring than autumn

Garden Warbler (Sylvia borin) 2

Notes: This site was so small (a small garden (0.02 km ) at St Catherine’s Monastery surrounded by barren desert) that individual birds could be easily caught on arrival, and the length of stay of a sizeable proportion of birds could be estimated reliably to within narrow limits. It was situated 300 km from the desert’s northern edge and about 2000 km north of the southern edge of the Sahara. In general, the longest stopovers were shown by birds on long migrations for which the stopover site was far from the point of initiation, while the shortest were in species for which the stopover site was close to the point of initiation in autumn. a Difference between autumn and spring, P , .001. Source: From Lave´e et al. (1991).

So within species, breeding populations taking different routes may pursue different strategies, presumably developed according to conditions on route, and the same populations may adopt different strategies at the two seasons. Age differences also occur in some species. For example, among Savi’s Warblers (Locustella luscinioides) in Portugal, juveniles start migrating a month before adults. They leave with low-fat reserves, enough for about 150 km of non-stop flight. The adults depart with much larger reserves, enough for up to 2750 km of non-stop flight, potentially enabling them to reach wintering areas south of the Sahara (Neto et al., 2008). The early-departing juveniles could therefore be classed as energy minimizers and the later-departing adults as time minimizers. In some species, moreover, juveniles may take markedly different routes from adults, entailing different fattening regimes. In the Sharp-tailed Sandpiper (Calidris acuminate), most adults migrate directly from eastern Asia to Australia along a coastal route, stopping periodically to refuel, while juveniles first take a long eastward detour, accrue large fat stores in southwestern Alaska, and then take a trans-Pacific flight to Australia (Chapter 18; Handel & Gill, 2010).

MECHANISMS OF FUEL DEPOSITION Three types of limitation could influence the fuelling rates of birds. One is the amount of food that can be consumed per 24 hours. This rate is affected mainly by such factors as day length, food availability, the feeding efficiency of the bird itself and the constraints on feeding imposed by competitors and predators (Chapters 14, 30). The bird might increase its intake rate in various ways, such as feeding more rapidly or for longer than usual each day, or by selecting the most calorific and easily digestible items. Some waterfowl and shorebirds can feed both by day and by night and can thus achieve higher rates of food throughput than other birds, with correspondingly higher rates of fuel deposition (Zwarts et al., 1990; Kvist & Lindstro¨m, 2003). The second type of limitation is imposed by digestive efficiency which, regardless of intake rate, limits the amount of food that can be processed per unit time (Diamond et al., 1986; Klaassen et al., 1997). Again, birds might maximise throughput in various ways, such as ensuring that food is always present in the crop, ready for passage down the gut as soon as space becomes available, or increasing the throughput rate to digest food less thoroughly but in greater quantity than usual, or by modifying gut structure to hold more food and digest it more rapidly. The third potential constraint comes from crop capacity. Many birds, especially herbivorous species, normally fill the crop before going to roost and digest that food during the night. If crop capacity is small relative to night length,

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The Migration Ecology of Birds

FIGURE 5.3 Changes in food intake and body mass in a captive Whitecrowned Sparrow (Zonotrichia leucophrys) during the spring migration period. After King (1961).

34

Body mass (g)

32 30 28 26 24

Food intake (kJ per day)

120 110 100 90 80 70 4

8 12 16 20 24 28 32 36 40 44 48 Day of experiment

then crop capacity could be said to limit daily intake. To my knowledge, the extent to which crop capacity can be increased at migration seasons has not been studied, although stomach size is known to change during the migration seasons of some birds (see below).

Increased feeding rates and feeding times Hyperphagia (eating more than needed to maintain a stable body weight) occurs in captive passerine migrants, which at appropriate seasons suddenly begin to eat around 25% 30% more per day than usual, promoting mean weight gains of up to 10% per day (Figure 5.3). In some species, higher rates of weight gain have occasionally been recorded, as much as 40% per day in Garden Warblers (Bairlein, 1990). Before spring migration, White-crowned Sparrows (Zonotrichia leucophrys) showed two peaks in foraging, one in the morning and the other before sunset, as observed in both wild and captive birds (Morton, 1967; Ramenofsky et al., 2003). Toward migration time this pattern changed, as birds began to feed throughout the daylight hours, gaining in body mass and fat content. Once migration activity started, some birds ceased feeding in the late afternoon, enabling them to empty their guts and reduce excess weight before the flight, which would normally begin after dark. Shorebirds in West Africa increased their foraging periods from 6 10 hours per day in winter to 12 hours per day during spring fuelling. This change involved more feeding at night, but the total time spent foraging was still limited by the tidal regime (Zwarts et al., 1990). Some birds may achieve hyperphagia at the expense of vigilance, spending less time scanning for predators, as noted in Ruddy Turnstones (Arenaria interpres) (Metcalfe & Furness, 1984). Juveniles in the same area that were not fattening for migration maintained the same high scanning rate. The most obvious way in which a diurnal bird could conserve feeding time is to migrate at night. While this may not increase feeding time over what is usually available, it at least prevents potential feeding time being reduced by flight time. Given this advantage, together with reduced predation risk, the question becomes why any birds migrate by day, apart from overland soaring species dependent on thermals (Chapter 4).

Change of diet Another way in which birds can increase their calorie intake is to concentrate on easily digestible, energy-rich food items. In both the Old and New Worlds, many passerines eat fruit at the time of migratory fattening. They include not

Fuelling migration Chapter | 5

83

only regular fruit-eaters, such as Sylvia warblers, but also others not normally considered frugivores, such as the Pied Flycatcher, Spotted Flycatcher and Yellow Wagtail (Motacilla flava) (Herna´ndez, 2009). The flycatchers in northwest Spain favoured the fruits of Dogwood (Cornus sanguinea) which are relatively rich in lipids. North American Tree Swallows (Tachycineta bicolor) are fond of the lipid-rich fruits of Northern Bayberry Myrica pensylvanica, and each fall flocks of thousands feed on them at many sites along the eastern North American seaboard, sometimes swooping past and plucking the fruits on the wing. In Europe, normally insectivorous House Martins (Delichon urbica) have been seen eating Elderberries (Sambucus nigra) at the time of autumn migration (Brookes, 2008). In many such species, the fruit passes rapidly through the gut, enabling large quantities to be processed in a short time. This change of diet at migration times does not result simply because fruit is more available than insects in late summer, because captive birds, given a choice of insects or fruit, also select fruit then. In the Mediterranean region, at the time of autumn migration, frugivorous warblers increased in body mass about twice as rapidly as purely insectivorous ones, even though the fruit-eaters had to eat more than their own body mass in fruit per day (Ferns, 1975; Thomas, 1979; Izhaki & Safriel, 1989). Likewise, pre-migratory weight gain in European Robins (Erithacus rubecula) showed a close relationship to fruit consumption and was greatest from fruits relatively rich in lipids (Herrera, 1981). Nevertheless, most birds take some insects at the same time as fruit, presumably to supply their protein needs, and captive Garden Warblers, Red-eyed Vireos (Vireo olivaceus), Hermit Thrushes (Catharus guttatus) and others gained weight more swiftly from a mixed diet than from fruit or insects alone (Bairlein, 1998; Parrish, 2000; Long & Stouffer, 2003). In North America, birds eating low-calorie fruits needed to eat more than four times their body mass per day (Smith et al., 2007). For obvious reasons, most fruit-eating occurs in autumn, but many passerines also select fruit before spring migration if it happens to be available. Some of the passerine species that spend the northern winter south of the Sahara eat many fruits in spring, especially those of Salvadora persica, on which they can also fatten more rapidly than on insects (Fry et al., 1970; Stoate & Moreby, 1995). Most fruits contain high proportions of carbohydrate and unsaturated fatty acids that can be easily metabolised to produce body fat. Unsaturated fatty acids in fruit proved ideal for migratory fat formation in captive birds, while other individuals fed on diets containing only saturated fatty acids fattened more slowly (Bairlein & Simons, 1995). In contrast, fruits are generally low in protein (most types 1% 7% of dry mass), with a few exceptions such as Olive (Oleo europaea) (8%) and Elder (Sambucus nigra) (12% 18%), both of which are favoured by birds (Jenni-Eiermann & Jenni, 2003). In Mediterranean regions, where many warblers fatten in autumn before crossing the Sahara, fruits tend to be richer in lipids than those in the temperate zone. And in tropical regions, fruits tend to be even richer in lipids, enabling some bird species to subsist on fruit alone for much of the year, some even raising their young on fruit (Snow & Snow, 1988). Captive birds provided simultaneously with two diets identical in energy content but differing in lipid content, showed clear preferences for lipid-rich foods (Borowitz, 1988; Bairlein, 1990), confirming observations on wild birds (Borowitz, 1988; Snow & Snow, 1988; Smith et al., 2007). In contrast, American Robins (Turdus migratorius) preferred sugar-rich to lipid-rich fruits and absorbed sugars more efficiently, although assimilation of lipids increased from summer to autumn (Lepczyk et al., 2000). Another advantage of fruit is that it can be obtained more easily than insects, being concentrated, predictable, immobile and conspicuous. Its low fibre content also makes fruit quick and easy to digest, and its high water content reduces the need to drink. However, some fruits contain tannins or other toxic compounds which birds have to deal with in various ways. Many passerines that remain insectivorous during migration prefer insects that are rich in fats (eg, caterpillars) or carbohydrates (eg, aphids) and can at times show fattening rates as high as those of fruit-eaters (for high rates of fuelling in Sedge Warblers eating aphids see Bibby & Green, 1981). Other warblers on spring migration prefer nectar over insects, presumably for the same reason. The Yellow-faced Honeyeater (Caligavis chrysops) in eastern Australia was found to increase the ratio of nectar to insects in its diet during both autumn and spring migrations (Munro, 2003). On Ventotene Island off Italy, four migrating warblers (Garden Warbler, Subalpine Warbler (Curruca cantillans), Common Whitethroat and Blackcap) foraged regularly in spring on two commonly flowering species, namely Mediterranean Cabbage (Brassica fruticulosa) and Giant Fennel (Ferula communis), while other migrants visited flowers only occasionally or not at all (Schwilch et al., 2001). Nectar was the main food of these warblers, rather than pollen or insects on the flowers, and in food choice experiments the birds preferred nectar over mealworms. Nectar has some of the same features as fruit, being abundant and conspicuous, wet, rich in sugar and easily absorbed. Most diet studies of migrants refer to small insectivorous frugivorous passerines. It is unknown to what extent other birds change their diets at migration times, but fruit-eating then is known in such unlikely candidates as shorebirds, gulls and cranes (Glutz von Blotzheim et al., 1975, 1977). Pink-footed Geese (Anser brachyrhychus) turned from grass to newly sown grain at migration time, more than doubling their daily energy intake (Madsen, 1985), while Canada

84

The Migration Ecology of Birds

Geese (Branta canadensis) changed from a diet of corn to a mixture of corn and meadow grass in spring, the grain providing carbohydrate (which can be converted to fat) and the grass protein (McLandress & Raveling, 1981). Many species of ducks turn from plant leaves and seeds to invertebrates at the time of spring migration, perhaps to acquire more protein in preparation for egg-laying (Arzel et al., 2006). Raptors that eat migrant birds presumably have diets richer in lipids at migration times, when the fat contents of their prey are greater than usual.

Changes in gut structure and digestive capacity At migration times, some birds increase the size of the digestive tract or adjust its structure to better deal with particular types of food. Such changes usually occur over a few days and have been noted in several species from songbirds to geese (McLandress & Raveling, 1983; Jordano, 1987; Bairlein, 1996; McWilliams & Karasov, 2005; Piersma, 2007). Studies on captive Blackcaps confirmed that the rate of energy assimilation under freely available food was proportional to the size of the intestinal tract and liver (Karasov & Pinshow, 2000). However, it is uncertain whether such gut changes anticipate increased food intake or occur in response to it. The latter seems most likely, but in any case such massive gut changes are presumably not without costs (Karasov, 1996; Hume & Biebach, 1996; Piersma et al., 1999). For one thing, they increase overall body mass, affecting agility and vulnerability to predation.

Digestive limitations Rates of energy intake in birds are often measured in relation to BMR. At normal activity, birds consume energy at a rate equivalent to around 2 3 BMR per day, but early studies undertaken mainly outside migration seasons suggested an upper limit to the daily metabolizable energy intake (DMEmax) of birds at around 4 5 3 BMR, imposed by digestive physiology and theoretically equivalent to a maximum rate of 2200 kJ per kg0.72 of body weight (Kirkwood, 1983). At migration times, however, owing to the steps birds take to improve their food-processing capacity, they can accumulate fuel at even higher rates. Twelve out of 22 species examined at migration times had rates of energy intake exceeding the above theoretical limit (Lindstro¨m & Kvist, 1995). Studies of captive birds in a migratory state, notably shorebirds, showed that, given sufficient food, individuals could fatten at much higher rates than normal up to 6 3 BMR, but reaching up to 10 3 BMR in shorebirds given access to food round the clock (Kvist & Lindstro¨m, 2003). While wild birds would not normally have free access to food all day and night, these findings show what some migratory birds can achieve under near-optimum conditions.

Reducing expenditure As well as increasing energy intake during migratory fuelling, birds can also lessen expenditure by reducing locomotory activity. The switch from insects to berries, for example, may lead to reduction in the energy spent on foraging movements. Birds may also lower their metabolic rates and body temperatures when sleeping at night, as a means of conserving energy, and migrant hummingbirds usually become torpid at night, even when very fat for migration (Carpenter & Hixon, 1988). Barnacle Geese show a progressive reduction in mean daily abdominal temperature (down to 4.4 C below usual), which begins just before the birds embark on their migration and continues, on average, for about three weeks (Butler et al., 2003).

Relative contributions The contributions of several of these mechanisms to migratory fattening have been studied in particular species (Bairlein, 1985; Bairlein & Simons, 1995). For example, the Garden Warbler at migration time eats up to 40% more per day (in terms of convertible energy), and switches from a mainly insect to a mainly fruit diet (often Elder (Sambucus niger) at northern latitudes and figs (Ficus) at Mediterranean latitudes). Increase in digestive and assimilation efficiency accounts for another 20% increase in energy intake during pre-migratory fattening (Bairlein, 1985c, 1991a). This increased efficiency is associated with increases in gut weight and in the rate of synthesis of fatty acids in the liver. In contrast, no such change in digestive efficiency was found in seed-eaters, such as the White-crowned Sparrow (Z. leucophrys) and Bobolink, the extra calories for fuel deposition being obtained entirely by longer feeding periods (King, 1961, 1972; Gifford & Odum, 1965). All these various ways of raising energy intake have costs which affect the bird adversely in other ways, so they normally occur only at migration seasons or at other times of high demand. They are apparently under endogenous control and normally appear only at appropriate times of year, as revealed in captive birds (Berthold, 1996).

Fuelling migration Chapter | 5

Populations

FDRmax

100

10 Passerines Waders Non-passerines

1

0.001

0.01

1

10

Individuals

100

FDRmax

0.1

85

FIGURE 5.4 Maximum fuel deposition rates (FDR, expressed as % lean body mass per day) for populations (upper) and individuals (lower) of free-living migratory birds of different body weights. Data are based on changes in body mass over time (minimum 2 days), either in individuals or in populations. Only the highest value for a species is included. Maximum FDRs were negatively correlated with body mass, both for individuals and for populations. No significant differences in mass-specific daily FDRs were found between passerines, waders and other non-passerines. Combining all species, the relationship between maximum recorded daily fuel deposition and body mass (BM) for populations is 1.16 BM20.35 (r2 5 0.66, P , .001, 95% confidence interval (CI) of slope 0.27 to 0.42) and for individuals 2.17 BM20.34 (r 5 0.54, P , .001, 95% CI of slope 0.23 to 0.44). From Lindstro¨m (2003), in which the original references may be found.

Passerines Waders Non-passerines

10

1

0.001

0.01

0.1 1 Body mass (kg)

10

DAILY RATES OF WEIGHT GAIN The repeated trapping of migrants in the days before they leave on migration has provided information on their individual rates of weight gain (eg, Figure 5.1), from which average and maximum rates for different populations have been calculated (Alerstam & Lindstro¨m, 1990; Lindstro¨m, 2003). Expressed as the daily (24-hour) gain in mass relative to lean body mass, average rates of pre-migratory weight gain (mostly fat), as measured in 58 populations, ranged from less than 1% to more than 7% (maximum 13%). Exceptionally high rates were recorded on particular days, but not sustained over a longer period. In captive passerines, weight gain was often greater on the second than on the first day of fattening, a difference attributed to growth of the digestive tract to facilitate more efficient food processing (Alerstam & Lindstro¨m, 1990; Hume & Biebach, 1996; Klaassen et al., 1997). Comparing species, mean rates of weight gain decline proportionately with increasing body size so that large species generally accumulate reserves more slowly than small ones and depart with relatively smaller reserves (Figure 5.4). The smallest birds have daily weight increases that, in relation to their lean weights, are five or more times greater than those of large birds. This is because the maximum limit to the daily metabolizable energy intake is proportional to BMR (which declines with body mass), rather than to body mass itself (Lindstro¨m, 1991). In field studies of various bird species, maximum rates of daily fuel deposition were rarely above 10% of lean body mass in the smallest birds studied (3 g hummingbirds) and rarely above 2% in the largest (3 kg geese). The three main groups of birds examined (passerines, shorebirds and other non-passerines) showed no significant differences in mass-specific rates of daily fuel deposition (Lindstro¨m, 2003). Combining all species, the relationship between daily fuel deposition and body mass (M) for populations was 1.16 M20.35 (r2 5 0.66, P , .001), and for individuals 2.17 M20.34 (r2 5 0.54, P , .001). The slopes of these relationships were not significantly different from the maximum rate of fat deposition predicted on theoretical grounds as around M20.27, where M is lean body mass (Lindstro¨m, 1991, 2003).

CHANGES IN BODY COMPOSITION In addition to the storage and depletion of fat that occurs over the migration period, the muscles and internal organs can undergo considerable changes in size (Piersma, 1998; Battley et al., 2001b). Such changes occur even in short-distance migrants making frequent stops, but as expected, they are much greater in birds making long uninterrupted flights. They serve to adapt the bird for the journey, providing necessary fuel but also reducing unnecessary weight. As a trans-Saharan migrant, the Garden Warbler can increase its body mass from 18 g in summer or winter to a maximum of about 37 g shortly before setting out over the desert in autumn or spring (Bairlein, 2003). This doubling in

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The Migration Ecology of Birds

15.0

2.5

12.5 Mass (g)

Mass (g)

2.0 1.5 1.0

7.5

0.5 0.0

10.0

B A Heart

B A Lungs

B A Stomach

B A B A B A B A Liver Intestines Kidneys Leg muscles

5.0

B A Pectoral muscles

B A Remainder of carcass

FIGURE 5.5 Comparison of the mass of different organs (lean dry mass) (95% confidence interval) of Garden Warblers (Sylvia borin) before (Ethiopia) and after (Egypt) crossing the Sahara Desert. From Biebach & Bauchinger (2003).

body mass is due largely to fat deposition, but also to increase in protein and water content. In autumn in northwest Africa, preparation takes 10 14 days, with mean rates of weight gain of 0.7 1.0 g per day, and maximum rates of 1.5 g per day (10% of lean body mass), depending on the food available. By comparing Garden Warblers caught in autumn in Turkey (just before a southward Mediterranean Saharan flight) with others caught in spring in Sinai (just after a northward Saharan flight), Biebach (1998) concluded that about 70% of the loss in body mass during migration comprised fat, and the rest protein and associated water. The protein came partly from the breast and leg muscles which were reduced by 19%, but mostly from the digestive tract which was reduced by 39% (Biebach, 1998). Overall, 2.2 g protein and 5.1 g fat were used on this trans-Saharan flight, in an approximate ratio of 1:2.3. Assuming a flight of 2200 km and a mean weight loss of 7.3 g, this gave a mean weight loss of 3.3 g per 1000 km flown, which was not very different from the 3.6 g per 1000 km calculated for this species at sites elsewhere by Bairlein (1991b). After the trans-Saharan flight, it took 1 2 days before gut function and metabolic intake returned to pre-flight level, and 2 3 days for the digestive tract to recover its size (Biebach, 1998). This was consistent with the general finding that, after arrival at a stopover site, long-distance migrants often do not gain weight for 1 3 days and may even lose weight in this period (mean weight loss in 11 passerine species 5 4.4%, range 0% 13%, Alerstam & Lindstro¨m, 1990). In another study of Garden Warblers migrating north over the Sahara in spring, Biebach & Bauchinger (2003) estimated a generally lower rate of weight loss of 1.8 g per 1000 km, but obtained more detailed information on the loss from particular organs (Figure 5.5). The most pronounced weight reduction took place in the liver (57%) and gastrointestinal tract (50%), followed by the flight muscles (26%), leg muscles (14%) and heart (24%). How much these changes occurred immediately before take-off and how much during the flight could not be determined, but Garden Warblers were estimated to thereby save around one-fifth of the energy needed for the same flight made without organ reduction. Protein catabolism made up about 34% of the overall saving, reduced maintenance costs 22% and reduced flight costs 43%. Estimated savings were roughly the same whether birds flew continuously or intermittently (flying at night and resting by day). The reduction in energy costs has presumably been a major driving force in the evolution of organ flexibility in these birds, extending the maximum flight range possible. A similar ranking of organ reductions to the Garden Warbler occurred in three other trans-Saharan migrants, namely the European Pied Flycatcher, Willow Warbler and Barn Swallow (Schwilch et al., 2002). Massive changes in body composition also occur in some shorebirds, which make long non-stop flights over oceans or another inhospitable substrate. Not only are these birds able rapidly to store and metabolize large amounts of fat but they also undergo many other physiological changes, affecting skeletal muscles and internal organs (Piersma & Lindstro¨m, 1997; Battley et al., 2000). Extreme changes were found in Bar-tailed Godwits (Limosa lapponica baueri) collected in Alaska just after take-off on a presumed trans-Pacific flight of around 10,400 km to New Zealand. These godwits had some of the highest fat contents recorded in birds, amounting to 55% of total body mass. They also had relatively large breast muscles and heart (exercise organs), but very small gizzard, liver, kidneys and gut (digestive organs). Upon departure in autumn, these birds apparently dispensed with parts of their metabolic machinery that were not directly necessary during flight, presumably converting them to other tissue. They re-built them upon arrival at the migratory destination so that they could again feed at greater efficiency (Piersma & Gill, 1998). This temporarily reduced digestive function may have been more than compensated by savings on transport costs. Attaining as much as 55% of fat in total body mass has other consequences. Not only must all of the bird’s structure and systems be contained in 45% of the body mass at take-off, but consuming this huge proportion of fat makes heavy

Fuelling migration Chapter | 5

FIGURE 5.6 Comparison of different components of body mass in different samples of Great Knots (Calidris tenuirostris) caught just before and just after a 5420 km flight between northwest Australia and Chongming Island near Shanghai in China. From Battley et al. (2001a,b).

250 200 Mass (g)

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150 100 50 0

B A Total body mass

B A Pectoral muscles mass

B A Total fat mass

inroads into the remaining protein during flight. According to Pennycuick & Battley (2003), the average journey to New Zealand (10,400 km) would entail flying continuously for a week, but the fuel load was sufficient to reach the South Pole (16 000 km), or alternatively to provide a reserve for adverse winds and navigation errors. A second group of godwits from the same population, obtained in spring before departure from New Zealand, would have run out of fat before reaching Alaska, but they could have reached the Yellow Sea area, where these birds stage on their northbound journey. The higher flight-range estimate for the autumn birds from Alaska was not due mainly to their higher fat mass (only 5% higher) but to the higher proportion of fat in the total body mass, which they had achieved in autumn by reducing the mass of other organs before departure. The ‘fat fraction’ is more important than the fat mass in influencing flight range (Pennycuick & Battley, 2003). Turning to another shorebird, samples of Great Knots (C. tenuirostris) were collected before and after a 5420 km flight from northwest Australia to Chongming Island near Shanghai in China (believed to be flown non-stop), again to assess the amount of fat consumed and of protein withdrawn from flight muscles and other organs. This journey took 4 days (Pennycuick & Battley, 2003). These birds showed a big reduction in fat content (but not to zero), and loss of lean tissue mass, with statistically significant reductions in six organs (pectoral muscle, skin, salt glands, intestine, liver and kidney), and non-significant reductions in several others (Figure 5.6). The reductions in functional components between the start and end of the flight were reflected in a lowering of BMR by 42%, one of the fastest rates of BMR change recorded in birds. Only the brain and lungs had not changed over this journey (Battley et al., 2000). Other Great Knots caught in northwest Australia were flown to the Netherlands and kept without food until their body mass had declined to the level found in arriving birds on Chongming Island. Organ reductions were broadly similar but, compared with the fasted birds, those that had migrated had conserved more protein (Battley et al., 2001a,b). Another well-documented example of seasonal change in body composition concerns the Black-necked Grebe (Podiceps nigricollis) in North America, which remains flightless for much of the year, but also undertakes long migrations and massive associated changes in body composition (Box 5.1). It is clear from these various examples that a bird refuelling for long-distance migration is not like a plane landing, refuelling and taking off again. Unlike the plane, the bodies of long-distance migrant birds have to be partly reconstructed at each major stopover and modified again before take-off. We can envisage that the sizes of organs carried at take-off by different populations represent evolutionary compromises between their functions during the pre-departure, flight and post-arrival phases of migration (Piersma, 1998). In all populations, other tissue is invariably deposited along with fat, but in proportions that vary greatly between species, and between different populations of the same species, according to the journeys they make. Before take-off, the pre-departure enlargement of exercise organs and shrinkage of nutritional organs makes sense on long flights where weight reduction is paramount. In other species, the digestive tract is apparently reduced during the flight itself, rather than beforehand, contributing to the fuel and water needs of the migrant on its journey. Prior reductions in nutritional organs appear most pronounced in populations about to overfly oceans that offer few or no opportunities for emergency landings, let alone feeding. Muscle growth and shrinkage may serve more than one function. As explained above, muscle breakdown is necessary for efficient fat metabolism, providing intermediates for the citric acid cycle. It may also provide metabolites such as glucose for proper functioning of the nervous system, and uric acid which is an antioxidant that can de-toxify the free radicals produced when tissues consume oxygen (Dohn, 1986; Klaassen, 1996). At the same time, as muscles

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BOX 5.1 Migration-related changes in the body composition of the Black-necked Grebe (Podiceps nigricollis) through the year. From Jehl, 1997; Jehl et al., 2003. The Black-necked Grebe in North America undergoes remarkable changes in body composition during the course of each year. Incapable of flight for months at a time, this species has the longest non-flying period of any northern hemisphere bird, totalling 9 10 months over the course of a year. In practical terms, the bird flies only to migrate and spends the rest of its life on water, undergoing several cycles per year of expansion and contraction of particular body parts. Yet its existence depends on its ability to fly as much as 6000 km each year to reach high-yield seasonal food supplies that are exploitable by very few other species. After breeding mainly on prairie wetlands, the species migrates to assemble in huge numbers on a small number of hypersaline lakes, notably the Great Salt Lake in Utah and Mono Lake in California, each of which can hold more than a million grebes in autumn. The birds feed on the huge numbers of brine shrimps (Artemia) and alkali flies (Ephydra) available at this time. The grebes arrive mainly in September (but from mid-July to early November), moult their feathers and remain until food supplies have dwindled (usually late November December). They then migrate to wintering areas in the Gulf of California. They begin the return journey from January, travelling via the Salton Sea (in south California) where they remain for at least two months, again becoming flightless, and then in late March April they continue to the Great Salt Lake, and thence to the prairies in April June. When these grebes leave their prairie nesting ponds in late summer they weigh about 420 450 g, but on arrival on the moulting sites after 2 3 nights of flight, they weigh as little as 250 g. Their moult leaves them flightless for 35 days, but they gradually increase in body mass to reach more than 600 g by mid-October. During this period they have accumulated massive fat stores, and their body organs have undergone large changes, involving increases in the size of the digestive organs and leg muscles, and a reduction of 50% or more in breast muscle, to below the size needed for flight. However, at the end of this autumn staging period, when the flight feathers have been replaced, the body changes are reversed. In the 2 3 weeks before leaving southward, the birds lose as much as one-third of their fat reserves, and reduce the size of nutritional organs by up to 75% while building their pectoral muscles and heart (Jehl, 1997). These huge changes in body structure result in a net one-third loss of body mass to 420 450 g. In this way, the grebes optimize flight efficiency by reducing weight and wing loading, and increasing flight range. No other bird species is known to reach migratory condition by losing so much mass before departure (but for nestlings of some species, see Chapter 8). Most of the remaining fat reserves are used during the flight to wintering areas. Juveniles undergo similar but less extreme changes. Additional cycles that involve less marked fattening are repeated in these grebes at breeding and wintering areas and in some individuals also at spring staging areas so that body weight and composition are in continual flux. The extreme reductions in leg muscle mass that occur before every migration reduce flight costs. If the bird maintained the body structure best suited for swimming and feeding, it would need far greater energy reserves for its long-distance migrations. This continual modification of behaviour and body structure as the bird shifts between swimming and flight modes, sedentary and migratory phases, with minimal waste of resources, may have helped the Black-necked Grebe to become the most abundant grebe on earth.

provide the power needed for migratory flights, their shrinkage during a flight may be an adaptation to the reducing weight (and hence reducing power needs) of the bird during its journey (Pennycuick, 1975). In captive Red Knots (Calidris canutus) flown in wind tunmnels, pectoral muscle size rapidly tracked body mass changes that occurred during periods of flight, fasting and fuelling (Lindstro¨m et al., 2000). So on sustained long flights loss of protein is unavoidable, but it may also be strategically convenient (Jenni & Jenni-Eiermann, 1998; Battley et al., 2000). Because protein catabolism results in a higher metabolic water yield per unit energy than lipid, it is of additional value on long, non-stop flights (Table 5.1; Klaassen, 1996). Net water availability during continuous flight could therefore be altered by changes in the relative proportions of the different fuel types used. In Bar-tailed Godwits and other shorebirds on spring migration, fat and protein are deposited in almost equal amounts (fresh mass basis), but because of its greater energy content, fat provides about 90% of the energy required for the flight. The same ratio (roughly half and half) may apply to a much wider taxonomic array of birds, including Common Chaffinch (Fringilla coelebs) and Garden Warbler, as well as various waders. This is far removed from an earlier assumption that all weight increase in migrant birds was due to fat. In some shorebirds, about two-thirds of the increase in flight muscle mass resulted from increases in myofibril mass, and about one-quarter from additional mitochondrial mass, while sarcoplasm increased very little (Evans & Davidson, 1990).

Body reserves for survival and breeding In most species that have been studied, individuals were found to arrive in breeding or wintering areas with some residual body reserves (eg, Sandberg, 1996; Fransson & Jakobsson, 1998; Farmer & Wiens, 1999; Widmer & Biebach, 2001; Morrison, 2006; Krapu et al., 2006). For example, American Redstarts (Setophaga ruticilla) arrived in Michigan breeding areas with enough body fat for at least another 1000 km of further flight, while Bar-tailed Godwits from

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Alaska arrived in New Zealand with enough fat for another 5000 6000 km of flight (Pennycuick & Battley, 2003). However, remaining fuel levels varied greatly between individuals and from year to year in the same population. Considering the energy cost of transporting such reserves, the question arises why birds carry so much more than they apparently need? Extra reserves might act as insurance against food shortage, bad weather or off-course drift on route; they might enable migrants to fly faster than the maximum range speed on flights where they are likely to encounter unfavourable weather; or they may help in ensuring survival after arrival in new areas, especially in spring when local food supplies are still scarce. In spring, they might also enable newly arrived males to concentrate on fighting and territory acquisition, or females to build the reproductive tract and produce eggs earlier than otherwise possible (Chapter 30). In some long-distance migrants, they may also contribute to rebuilding the digestive tract and other organs reduced for the journey (for Red Knot see Ve´zina et al., 2012). Or they may serve more than one of these various functions. It is at high latitudes where the potential breeding season is short that the advantage of body reserves may be greatest, especially if they enable birds to start nesting earlier than they otherwise could. This applies particularly to large species, which generally have long breeding cycles and are therefore most pushed for time. In some waterfowl, reserves accumulated before arrival, and especially at the last stopover site, help the female to form eggs and survive through incubation, when little food is eaten (Newton, 1977; Ebbinge, 1985). Arctic-nesting geese often arrive before vegetation has begun to grow in their breeding areas, and when little food is available. They are described as ‘capital breeders’, because they reproduce largely on the strength of existing body reserves. They contrast with ‘income breeders’ which reproduce on the strength of food eaten at the time. In different goose populations, weight gains of 25% 53% have been recorded before the birds set off on spring migration or from staging sites on route (McLandress & Raveling, 1981). This is a lot for birds of this size. Females accumulate more weight than males, in association with the needs of egg production and incubation. At least some species of high arctic geese, such as the Lesser Snow Goose (Anser c. caerulescens), Ross’s Goose (Anser rossii) and Brent Goose (Branta bernicla), can start egg-laying 2 5 days after arriving in breeding areas, before plant growth has begun, and seem to rely entirely on body reserves. Others feed and regain some weight after arrival but still depend partly on body reserves accumulated further south (Bromley & Jarvis, 1993). In Lesser Snow Geese, the relationship between body reserves and reproductive output was studied from females shot at various stages of breeding in the Northwest Territories of Canada (Ankney & MacInnes, 1978). The potential clutch size of pre-laying females was determined by counting the number of large vascularized follicles in the ovary, and females with larger body reserves had, on average, larger potential clutches. Yet other females collected after laying clutches of different sizes had residual reserves of similar size to one another. The authors concluded that clutch sizes of these geese were determined by the levels of prior nutrient reserves. Breeding females used most of their remaining fat and protein reserves during incubation (85% and 24% respectively). Late in incubation when females had depleted their body reserves, some left their nests to feed, while others were found dead on their nests from starvation. Hence, to reproduce successfully in this area, female Lesser Snow Geese had to accumulate beforehand enough reserves to support the last stage of migration, egg production and maintenance during the 4 weeks of incubation. Only after hatch were they able to feed intensively again and build up body condition for the return migration to wintering areas. Similar findings have emerged in other geese (Chapter 29). Some duck species also depend for reproduction at least partly on body reserves accumulated in wintering or migration areas, as found for example in the Mallard (Anas platyrhynchos), Northern Pintail (Anas acuta) and Northern Shoveler (Spatula clypeata) (Krapu, 1981; Devries et al., 2008; Esler & Grand, 1994; MacCluskie & Sedinger, 2000). However, other ducks accumulate most of the necessary nutrient after arrival in breeding areas, as found for the Greater Scaup (Aythya marila) (Gorman et al., 2008) and Harlequin Duck (Histrionicus histrionicus) (Bond et al., 2007). Sandhill Cranes nesting in arctic North America likewise accumulated substantial body reserves at spring stopover sites, increasing in body weight by about one-third before travelling to breeding areas (Krapu et al., 1985). By the time they arrived, about half the reserve still remained. The main difference from waterfowl was the lack of any obvious difference in reserves between the sexes and the relatively small proportion allocated to egg production. But in cranes, the clutch weighs less than one-tenth of total body mass compared with 20% 40% in geese. Stable isotope analysis has provided another way of telling whether eggs are produced from food eaten in breeding areas or from food eaten in migration and wintering areas. The method depends on the facts that foods eaten in different regions or habitats have different isotope ratios and that these differences are reflected for a time in the body tissues and eggs of the consumer (Chapter 2). Such analyses confirmed that Lesser Snow Geese on Akimiski Island were largely capital breeders, with reserves accumulated mainly south of breeding areas (Klaassen, 2003). In contrast, Greater Snow Geese (Anser caerulescens atlanticus) nesting on Bylot Island in Canada seemed to obtain most of the protein and fat needed for egg production after arrival in the breeding area (Gauthier et al., 2003). Based on isotope analyses over 3 years, body reserves contributed, on average, about 33% of lipid-free yolk nutrients, 27% of albumen and 20% of yolk lipid. However, late-laying females apparently invested proportionally more endogenous reserves in

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their eggs than did early layers. Among different populations of arctic-nesting geese, therefore, considerable variation may exist in the extent that birds rely on residual body stores for reproduction. Unlike geese and those ducks that feed on plant material, shorebirds depend largely on animal matter. Invertebrate food items from tundra and estuarine habitats have distinctly different carbon and nitrogen isotope ratios. In several wader species nesting in arctic Canada and Greenland, carbon isotope analyses showed that egg protein was formed from terrestrial rather than marine foods, and hence was influenced by food eaten after arrival in tundra breeding areas (Klaassen et al., 2001). On the other hand, in another study, eggs in the earliest clutches of Red Knots and Turnstones in the northeastern Canadian Arctic were rich in those isotopes of carbon and nitrogen expected if some residual marine nutrients had been used in their production (Morrison & Hobson, 2004). This occurred even though Calidris sandpipers typically produce clutches equal to 80% 120% of female body mass. Capital and income breeding evidently represent opposite ends of a continuum of variation found among birds. Species and populations may vary in the contribution that body reserves make to reproduction, as may individuals within the same population. Populations also vary in where on the migration route between wintering and breeding areas they acquire the reserves for breeding. Larger species, in which clutch weight forms a small proportion of total body weight, are much more likely to rely heavily on body stores for egg formation than are small species in which the clutch weighs as much or more than the female herself. Thus the body reserves that small passerines and shorebirds carry to the breeding areas can provide at most only a minor contribution to the total protein and fat needed for egg formation, but they may help with initial survival and reproductive activities, enabling earlier egg-laying than otherwise possible (Chapter 30). These various studies highlight the phenotypic flexibility of birds: their ability to change their body composition rapidly, according to the varying extents to which they depend on previously accumulated body reserves for breeding, and the varying stages of the journey at which such reserves are accumulated. It is remarkable that some birds can lay down body reserves for both migration and breeding at the same time and that they transport reserves hundreds, or even thousands, of kilometres from wintering to breeding places. They do this to produce young early enough to exploit the seasonal peak of food at high latitudes and have their young ready to migrate before winter sets in. It is also remarkable that birds can shift protein from one body organ to another, as the muscles and digestive organs change their relative sizes before and after flights. Although less research has been done on the condition of birds when they arrive in wintering areas, studies indicate that residual body reserves are usual there too and can influence subsequent survival (Chapter 29). Body reserves could be advantageous at any stage of migration, cushioning the bird against adverse weather or other unexpected mishaps. But in many species, it is after arrival in breeding areas that residual body reserves are most useful. While clearly supporting the breeding of arctic-nesting geese and others, for smaller birds, residual body reserves could (1) increase survival chances after arrival in breeding areas if weather conditions deteriorate; (2) allow more time to be spent on other activities important to reproduction, such as territorial defence; (3) relieve food demands in the early stages of breeding, allowing an earlier start; and (4) allow females to forage selectively for nutrients important to reproduction, such as calcium, while living mainly off their fat (Sandberg & Moore, 1996). These potential benefits are not mutually exclusive but must presumably be set against the costs of longer stopovers needed to accumulate the extra reserves, the energy to transport them, and any associated predation risks incurred.

CONCLUDING REMARKS One of the most striking features of birds is their ability to fuel high-intensity endurance exercise with fatty acids that are stored in adipose tissue and delivered continuously to the working muscles by the circulatory system. This facility makes birds exceptional among vertebrates (McWilliams et al., 2004). Yet studies have increasingly revealed other amazing ways in which migratory birds have overcome physiological constraints in energy storage and migratory flight. For fuelling, these include various ways of temporarily increasing calorie intake rates, including the extension of feeding times (sometimes into nighttime), night-time migration to leave the day for feeding, the switching of metabolic emphasis from carbohydrate to fat, change of diet and increase in the size and effectiveness of the digestive tract. For flight, they include reduction in the size of digestive organs immediately before or during the flight, and breakdown of protein to supply metabolites needed for the utilization of fat and other purposes. These are all measures that the bird can take for short periods only, as they also have costs, and conflict with other activities or with requirements at other stages of the annual cycle. But what astonishing creatures birds are.

SUMMARY Migration normally requires body reserves (mostly fat) accumulated at appropriate times of year. Depending mainly on the terrain to be crossed, birds migrate on a small fuel reserve/short flight system or on a large fuel reserve/long flight

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system, the latter being necessary in landbirds travelling overseas or other inhospitable areas where they cannot refuel. Birds may vary their migration mode at different stages of their journey, depending on feeding opportunities in different parts of the route. The more fuel a bird carries, the more energy the bird uses in transporting it, which increases the energy cost per unit distance flown. Extra fuel also reduces the bird’s agility in evading attacks by predators. These considerations should favour a migration strategy of short flights, frequent fuelling and low fuel loads wherever possible, with the alternative of long flights, infrequent fuelling and heavy fuel loads only when necessary. The predominant fuel is fat which has five main advantages: (1) it provides the highest concentration of metabolic energy per unit weight; (2) it can be stored dry without accompanying water or protein; (3) it can be metabolised (by the citric acid cycle) more efficiently than protein or carbohydrate; (4) it can be oxidized efficiently and completely by most body tissues, including the all-important flight muscles; (5) muscle fibres relying on fatty acids can work for long periods without tiring. However, carbohydrate and protein are also used as fuel on migratory flights, and metabolism of fat is accompanied by metabolism of protein, which yields intermediates for the citric acid cycle and other important metabolites. The ratio of fat to protein accumulated at migration times varies greatly between species, between populations of the same species and between outward and return journeys. In small passerine migrants, the composition of the diet seems to influence to some extent the composition of the fuel stores laid down. These stores in turn influence the relative composition of the fuel types used during migration and (via their energy density) the flight range. The composition of body stores, notably the ratio of fat to protein, may also vary according to the nature of the journey and the terrain to be crossed, and the subsequent needs of the bird, whether for breeding or survival. Fuel deposition results in rates of daily weight gain up to about 10% (occasionally 13% or more) of lean body mass, with slower rates in larger species, and great variation among individuals. Among passerines and shorebirds, shortdistance migrants usually increase in weight by 10% 30% before departure, and long-distance migrants by 70% 100%, with some species effectively doubling their body mass. Some species may accumulate no obvious reserves for migration but travel for only parts of each day, losing weight but replenishing it on a day-to-day basis. Rapid weight gain for migration mainly results from increased food consumption (feeding time), but in some species also from dietary change and improved digestive efficiency (involving increase in the size of the digestive tract). Rates of weight gain may be environmentally or metabolically limited. Some migrants increase muscle and heart mass before departure and reduce the size of other internal organs (digestive tract and liver). On arrival, the digestive organs are rebuilt before food assimilation at the normal rate can occur again. These changes in body composition are much more marked in species making long-distance non-stop flights lasting several days than in short-distance migrants that can feed and drink every day during their journeys. Many species typically arrive on spring breeding areas with a surplus of body reserves, including both protein and fat. In some species, notably arctic-nesting geese, the reserve is used for both egg production and incubation, at a time when little food is available locally. Body reserves imported to breeding areas may thus have been accumulated on wintering and migration areas at lower latitudes. For these reasons, the various seasonal changes in the body mass and composition of migratory birds are often rapid and substantial. Nevertheless, populations vary in their level of dependence on internal body reserves for breeding.

APPENDIX 5.1

CALCULATION OF FLIGHT RANGES

Much interest has centred on estimating the non-stop flight ranges of birds from their weights or fuel contents on departure. Such estimates require information, not only on the departure weight (or fuel content) of the birds concerned but also on the rate at which weight is lost (or fuel is used) during a journey. This rate has sometimes been estimated by comparing the weights (or body composition) of samples of birds obtained at different points on a journey. Weights taken just before and just after a non-stop flight over a sea or desert give the most reliable estimates of flight costs, for only then can one be sure that the birds had not fed and replenished their body reserves on route (Nisbet, 1963; Fry et al., 1972; Biebach, 1998; Biebach & Bauchinger, 2003). These studies provide estimates of weight loss (or fuel use) per unit time or per unit distance covered. However, they are usually based on mean values from samples of different birds and not on measurements from the same individuals, and they are valid only for the particular wind and other conditions prevailing at the time. Nevertheless, to estimate roughly how far a bird of known weight could fly, these rates of weight loss could be used, together with knowledge (or assumptions) of the lowest weight a migrating bird could reach and still remain active (usually taken as the fat-free weight). If the rates of weight loss are measured per unit time, additional information is needed on the flight speed of the bird to convert hours flown to distance covered. Most published estimates of flight range using this procedure are based on the assumption that the total weight loss during flight is due entirely to catabolism of fat. Where part of the weight loss is due to protein, as seems usual in

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migratory birds, this can greatly reduce the estimate of energy expended, and thus the estimated flight costs. The 24-g Garden Warblers (S. borin) mentioned earlier lost about 7.3 g body weight on a 2200 km trans-Saharan flight, about 3.3 g per 1000 km flown, which involved fat and protein in the ratio 2.3:1 (Biebach, 1998). At the other extreme of body size, Barnacle Geese (B. leucopsis) migrating 1000 km from Svalbard to Scotland weighed an average of 2.30 kg at the start of migration (including 432 g of fat) and 1.82 kg at the end, although some may have fed on route. The amounts of fat and tissue protein required during the 60 hours of flying were estimated at 415 and 126 g respectively, a ratio of 3.3:1, so with no major hold-ups, at least some of the geese could have flown the whole route without feeding (Butler et al., 2003). Other findings on weight loss during migration have been expressed on the basis of loss per unit time for example the 7.4 g per hour weight loss of Black-necked Grebes (P. nigricollis), which was equivalent to less than 2% of total body mass per hour (Jehl et al., 2003). A second way of estimating flight range involves knowledge of the departure weight of the bird, from which its flight cost (rate of fuel use) can be calculated from standard equations depicting the relationship between body weight and BMR (Lasiewski & Dawson, 1967). BMR is higher for passerines than for non-passerines, so different equations are used for the two groups. Flight cost is taken as some multiple of BMR (usually 12 3 BMR). Modifications to the original model of Raveling & Lefebvre (1967) allow for weight loss during flight resulting from fuel consumption (Summers & Waltner, 1979), use actual measurements rather than estimates of flight costs (Davidson, 1984) and allow for variations in the shape of the birds themselves (notably wing-length) (Castro & Myers, 1989). The advantage of this latter correction is that it does not assume that the cost of flight is a consistent multiple of BMR but varies in a way that depends on the aerodynamics of the bird, therefore diverging from the classic 0.7 exponent of metabolic costs versus body mass. It acknowledges that two birds of the same mass can have very different flight costs depending on their aerodynamic design (Castro & Myers, 1989). Only the latter model predicted decreasing costs of flight with decreasing body mass, as also expected on theoretical grounds. This method is thus readily applicable to birds of a wide weight range, providing that information is available on body mass, fuel load and flight speed. The current preferred model for estimating the flight range of migratory birds is that of Pennycuick (1989), again derived mainly from aerodynamic theory, but with later modifications (latest model also available as a software package, Pennycuick, 2009). This sophisticated model can be applied to birds of any size providing that appropriate measures are available for the species concerned. It is by far the best model yet devised, enabling the researcher to test the effects of altering any of the key variables involved. Further refinements to models are likely to occur in the future, as additional information becomes available. All these indirect methods of estimating flight range make no allowance for the wind conditions in which particular birds migrate, for any effects of flight formations, or for other external variables that influence energy consumption. Flight range estimates could therefore be in considerable error. Nevertheless, particular models have useful comparative value for closely related species of similar shape and flight mode (Gudmundsson et al., 1991). Such models also provide a useful check on our understanding: if estimates of flight ranges do not match what migrants on independent evidence are known to achieve, then our knowledge is probably deficient in some way.

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Parrish, J. D. (2000). Behavioral, energetic and conservation implications of foraging plasticity during migration. Stud. Avian Biol. 20: 52 70. Pearson, D. J. (1990). Palearctic passerine migrants in Kenya and Uganda: temporal and spatial patterns of their movements. Pp. 44 59 in Bird migration. Physiology and ecophysiology in Bird migration. Physiology and ecophysiology (ed. E. Gwinner). Berlin, Springer-Verlag. Pennycuick, C. J. (1975). Mechanics of flight. Pp. 1 75 in Avian biology, Vol. 5 (eds D. S. Farner, & J. R. King). London, Academic Press. Pennycuick, C. J. (1989). Bird flight performance: a practical calculation manual. Oxford, Oxford University Press. Pennycuick, C. J. (2009). Modelling the flying bird. London, Academic Press. Pennycuick, C. J. & Battley, P. F. (2003). Burning the engine: a timemarching computation of fat and protein consumption in a 5420 km nonstop flight by Great Knots Calidris tenuirostris. Oikos 103: 323 32. Pierce, B. J. & McWilliams, S. R. (2005). Seasonal changes in composition of lipid stores in migratory birds: causes and consequences. Condor 107: 269 79. Piersma, T. (1987a). Hop, skip or jump? Constraints in migration of arctic waders by feeding, fattening and flight speed. Limosa 60: 185 94. Piersma, T. (1987b). Population turnover in groups of wing moulting waterbirds: the use of a natural marker in Great crested Grebes. Wildfowl 38: 37 45. Piersma, T. (1998). Phenotypic flexibility during migration: optimisation of organ size contingent on the risks and rewards of fueling and flight? J. Avian Biol. 29: 511 20. Piersma, T. (2007). Using the power of comparison to explain habitat use and migration strategies of shorebirds worldwide. J. Ornithol. 148: S45 59. Piersma, T. & Gill, R. E. (1998). Guts don’t fly: small digestive organs in obese Bar-tailed Godwits. Auk 115: 196 203. Piersma, T. & Jukema, J. (2002). Contrast in adaptive mass gains: Eurasian Golden Plovers store fat before midwinter and protein before prebreeding flight. Proc. R. Soc. Lond. B 269: 1101 5. Piersma, T. & Lindstro¨m, A. (1997). Rapid reversible changes in organ size as a component of adaptive behaviour. Trends Ecol. Evol. 12: 134 8. Piersma, T., Gudmundsson, G. A. & Lilliendahl, K. (1999). Rapid changes in size of different functional organ and muscle groups during refuelling in a long-distance migrating shorebird. Physiol. Biochem. Zool. 72: 405 16. Ramenofsky, M. (1990). Fat storage and fat metabolism in relation to migration. Pp. 214 31 in Bird migration: physiology and ecophysiology in Bird migration: physiology and ecophysiology (ed. E. Gwinner). Berlin, Springer-Verlag. Ramenofsky, M., Agatsuma, R., Barga, M., Cameron, R. Harm, J., et al. (2003). Migratory behaviour: new insights from captive studies. Pp. 97 111 in Avian migration (eds P. Berthold, E. Gwinner, & E. Sonnenschein). Berlin, Springer-Verlag. Raveling, D. G. & LeFebvre, E. A. (1967). Energy metabolism and theoretical flight range of birds. Bird-Banding 38: 97 113. Rubolini, D., Pastor, A. G., Pilastro, A. & Spina, F. (2002). Ecological barriers shaping fuel stores in Barn Swallows Hirundo rustica

following the central and western Mediterranean flyways. J. Avian Biol. 33: 15 22. Sandberg, R. (1996). Fat reserves of migrating passerines at arrival on the breeding grounds in Swedish Lapland. Ibis 138: 514 24. Sandberg, R. & Moore, F. R. (1996). Fat stores and arrival on the breeding grounds: reproductive consequences for passerine migrants. Oikos 77: 577 81. Schaub, M. & Jenni, L. (2000). Body mass of six long-distance migrant passerine species along the autumn migration route. J. Ornithol. 141: 441 60. Schwilch, R., Grattarola, A., Spina, F. & Jenni, L. (2002). Protein loss during long distance migratory flights in passerine birds: adaptation or constraint. J. Exp. Biol. 205: 587 695. Schwilch, R., Mantovani, R., Spina, F. & Jenni, L. (2001). Nectar consumption of warblers after long-distance flights during spring migration. Ibis 143: 24 32. Smith, S. S., McPherson, K. H., Backer, J. M., Pierce, B. J., Podlesak, D. W. & McWilliams, S. R. (2007). Fruit quality and consumption by songbirds during autumn migration. Wilson J. Orn. 119: 419 28. Snow, B. & Snow, D. (1988). Birds and berries. Calton, T. & A. D. Poyser. Stoate, C. & Moreby, S. J. (1995). Premigratory diet of trans-Saharan migrant passerines in the western Sahel. Bird Study 42: 101 6. Summers, R. W. & Waltner, M. (1979). Seasonal variations in the mass of waders in southern Africa, with special reference to migration. Ostrich 50: 21 37. Thapliyal, J. P., Pati, A. K., Singh, V. K. & Lal, P. (1982). Thyroid, gonad and photoperiod in the hemopoesis of the migratory Redheaded Bunting, Emberiza bruniceps. Gen. Comp. Endocrinol. 46: 327 32. Thomas, D. K. (1979). Figs as a food source of migrating Garden Warblers in southern Portugal. Bird Study 26: 187 91. Ve´zina, F., Williams, T. D., Piersma, T. & Morrison, R. I. G. (2012). Phenotypic compromises in a long-distance migrant along the transition from migration to reproduction in the High Arctic. Funct. Ecol. 26: 500 12. Ward, P. (1963). Lipid levels in birds preparing to cross the Sahara. Ibis 105: 109 11. Ward, P. & Jones, P. J. (1977). Pre-migratory fattening in three races of the Red-billed Quelea Quelea quelea (Aves: Ploceidae), an intratropical migrant. J. Zool. Lond. 181: 43 56. Widmer, M. & Biebach, H. (2001). Changes in body condition from spring migration to reproduction in the Garden Warbler Sylvia borin: a comparison of a lowland and a mountain population. Ardea 89: 57 68. Witter, M. S. & Cuthill, I. C. (1993). The ecological costs of avian fat storage. Philos. Trans. R. Soc. London, Ser. B. 340: 73 92. Witter, M. S., Cuthill, I. C. & Bonser, R. (1994). Experimental investigations of mass-dependent predation risk in the European Starling Sturnus vulgaris. Anim. Behav. 48: 201 22. Zwarts, L., Blomert, A. M. & Hupkes, R. (1990). Increase of feeding time in waders preparing for spring migration from the Banc D’Arguin, Mauritania. Ardea 78: 237 56.

Chapter 6

Amazing journeys

Bar-tailed Godwits (Limosa lapponica), noted for the longest oversea flights performed by any landbird. Lofty mountain ranges and wide belts of desert are traversed, and lesser or vaster expanses of sea are crossed. William Eagle Clark, 1912

Some birds make what seem to us astounding journeys over oceans, deserts, mountain peaks or other hostile terrain. This chapter focuses on some of these difficult journeys and the various adaptations that enable birds to complete them successfully. Most flying birds can migrate over small areas of hostile habitat that they can cross in a few hours. The difficulties come mainly on longer journeys which require more than 24 hours of non-stop flight or entail physiologically harsh conditions, such as temperature and humidity extremes, or greatly reduced oxygen levels. The fact that some birds can make such arduous journeys does not imply that all could do so. Much depends on features of the bird itself, such as its size and physiology, and also on the habitat to which it is adapted. Oceans are inhospitable for landbirds, continents for pelagic seabirds, open country for forest birds, forests for open country birds and barren deserts for almost all birds.

OCEAN-CROSSINGS BY LANDBIRDS Landbirds that migrate over oceans provide some of the most extreme examples of endurance flight and precise navigation when they travel, without the opportunity to feed, drink or rest, over vast areas of open sea (Figures 6.1 and 6.2). While some landbirds on over-water flights take whatever opportunities for rest are available, stopping on ships, oil rigs and other installations, or even on mats of flotsam, these individuals probably represent an exhausted minority, and almost certainly most landbirds make water crossings non-stop, as implied by radar and tracking studies. On long sea-crossings, weather is paramount, and in coastal areas birds sometimes wait for days for the right conditions with clear skies and good tailwinds. Birds also need enough body fuel not only for the journey but also for any emergencies that might arise on route. Favourable weather at take-off may not hold throughout a journey of up to several thousand kilometres lasting up to several days. The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00033-6 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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FIGURE 6.1 Some major sea-crossings undertaken by landbirds. Some journeys are made only in one direction, while the return is made over a more overland route. Modified from Williams & Williams (1990).

FIGURE 6.2 Round-trip migrations of Bar-tailed Godwits of the Limosa lapponica baueri subspecies which breeds in Alaska and winters in New Zealand. The outward journey is non-stop and covers more than 10,000 km. The return journey follows a different route and involves a long stopover in the Yellow Sea region, separating two non-stop flights of more than 10,000 and more than 6000 km respectively. Modified from Gill et al. (2009) and Battley et al. (2012).

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On long over-water flights, birds have no ground features to help keep them on course but must rely entirely on celestial or magnetic cues. If they encounter mist or rain, they often become disoriented and mill around for hours or drift far off course, as radar observations show. On sea-crossings, natural selection acts harshly against any kind of mistake or mishap, and abundant evidence points to occasional heavy mortality of migrating landbirds over water (Chapter 31). One way round these problems is to fly high enough to avoid mist and rain, and on long over-water flights birds have often been detected by radar at heights exceeding 5 km, but such high-altitude flights can bring other problems (see later). Despite the apparent difficulties, all the major seas and oceans of the world are crossed regularly by landbirds (Figure 6.1, Table 6.1). Each year, millions of birds of a wide range of species cross on a broad front of the Mediterranean Sea in the Old World or the Gulf of Mexico in the New World (Moreau, 1961; Gauthreaux, 1999). At their widest points, both these crossings involve flights of more than 1000 km. Frequent storms make the trans-Gulf crossing hazardous, especially in the autumn hurricane season. Smaller numbers of other birds also cross all major

TABLE 6.1 Some long over-water journeys of migratory landbirds. Flight durations are calculated assuming still air, and for flight speeds of 30 35 km per hour (typical of small songbirds) and of 60 70 km per hour (typical of small shorebirds). In practice, most overseas migration occurs with the benefit of a tailwind, which reduces the flight times Journey

Species

Distance (km)

Flight duration (h) at 30 35 km per hour

60 70 km per hour

Siberia to Australia, across the Pacific

Bar-tailed Godwit (Limosa lapponica menzieri) Great Knot (Calidris tenuirostris)

8000

114 133

Alaska to Hawaii and other American Pacific Islandsa

Pacific Golden Plover (Pluvialis fulva) Bristlethighed Curlew (Numenius tahitiensis) and other shorebirds

4500 8300

71 83

India to East Africa, across the Indian Ocean

Amur Falcon (Falco amurensis)

3000

43 50

Greenland to southwest Europe, across the Atlantic

Northern Wheatear (Oenanthe oenanthe)

2000 3000

China to Australia across the Pacificb

Red Knot (Calidris canutus) and other waders

4500

Northeast North America to South America across the Atlanticc

Various waders, some passerines (including 13 parulid warblers)

2400 3600

69 120

34 60

North America to South America, across the Gulf of Mexico

Many and various species

Up to 1300

37 43

19 22

Europe to Africa, across the Mediterranean

Many and various species

Up to 1600

44 53

23 27

Iceland to Britain, across the Atlantic

Various species

800

21 23

11 13

a

57 100 64 75

Include Lesser Sand Plover (Charadrius mongolus), Eurasian Whimbrel (Numenius phaeopus), Pacific Golden Plover (Pluvialis fulva), Bar-tailed Godwit (Limosa lapponica), Lesser Yellowlegs (Tringa flavipes), Wandering Tattler (Heteroscelus incanus), Grey-tailed Tattler (Heteroscelus brevipes), Long-billed Dowitcher (Limnodromus scolopaceus), Ruddy Turnstone (Arenaria interpres), Sanderling (Calidris alba), Least Sandpiper (Calidris minutilla) and ducks such as Northern Pintail (Anas acuta) and Northern Shoveller (Spatula clypeata), although the bulk of their populations winter elsewhere. For the Bar-tailed Godwits that migrate from Alaska or Siberia to New Zealand, see text; for further details see Chapter 28. b Also Far Eastern Curlew (Numenius madagascariensis), Eurasian Whimbrel (Numenius phaeopus), Great Knot (Calidris tenuirostris), Bar-tailed Godwit (Limosa lapponica menzbieri) and others, either on their southward or northward journeys. c At least eight shorebird species: White-rumped Sandpiper (Calidris fuscicollis), Least Sandpiper (Calidris minutilla), Lesser Yellowlegs (Tringa flavipes), Hudsonian Godwit (Limosa haemastica), Red Knot (Calidris canutus), Short-billed Dowitcher (Limnodromus griseus), Semipalmated Sandpiper (Calidris pusilla) (McNeil & Cadieux, 1972). At least 13 parulid warblers, notably Blackpoll Warbler (Setophaga striata) (Nisbet et al., 1963). Other warbler species make this Atlantic flight occasionally, for at least two dozen species turn up frequently in autumn in Bermuda which lies 900 km east of the North America coast (Scholander, 1955; Wingate, 1973). Some waders, notably Eurasian Whimbrel (Numenius phaeopus), fly as much as 5500 km on this trans-Atlantic journey, taking more than 6 days (146 h averaging 38 km per h, Watts et al., 2021).

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inland waters, such as Caspian and Baikal in the Old World and the Great Lakes in the New World. Crossing these waters by direct flight saves considerable energy over the alternative of flying around them. Smaller numbers of landbird species also make long flights over parts of the Atlantic, Pacific and Indian Oceans. However, only in the North Atlantic do birds regularly cross from one side to the other. At least nine species which breed in Eastern Canada or Western Greenland migrate to winter in Europe or Africa. They include two geese (Brent Goose (Branta bernicla hrota) and Greater White-fronted Goose (Anser albifrons flavirostris)), one passerine (Northern Wheatear (Oenanthe oenanthe leucorhoa)), and six shorebirds: Red Knot (Calidris canutus islandica), Sanderling (Calidris alba), Dunlin (Calidris alpine arctica), Purple Sandpiper (Calidris maritima), Ruddy Turnstone (Arenaria interpres interpres) and Common Ringed Plover (Charadrius hiaticula psammodromus) (Le´andri-Breton et al., 2019). For the Northern Wheatear, this autumn journey constitutes the longest sea-crossing known from any songbird. Wheatears breeding in Northeast Canada and Greenland cross the Atlantic to Western Europe and probably also to West Africa, involving wind-assisted oversea flights of up to 4200 km towards their wintering areas in the western Sahel zone of Africa (Thorup et al., 2006a,b; Delingat et al., 2008; Bairlein et al., 2012). Their return journey runs to the north of the autumn one, with more stops, as birds move north through Britain and Iceland, and then on to Greenland and northeast Canada. Similar patterns, with birds travelling on a more northerly track via Iceland in spring than in autumn, have also been noted in Nearctic Ringed Plovers (Le´andre-Breton et al., 2019) and Purple Sandpipers (Summers et al., 2014), and all these species also cross the Greenland ice cap north of 65 N, at least in spring (see later). By changing routes between seasons, these birds can take advantage of the prevailing anti-clockwise winds associated with the Icelandic low-pressure system. Many species breeding in Iceland spend the winter in the British Isles, a sea crossing of more than 800 km, and others pass through the British Isles on route to West Africa. Eurasian Whimbrels (Numenius phaeopus) make a direct flight of 3900 5500 km from Iceland to West Africa in autumn, but in spring some return directly, while others make a stop in Ireland (Alves et al., 2016). Many species travel from eastern North America, across the Atlantic direct to South America. Judging by their appearance on Bermuda, which lies 900 km east of the North American coast, more than 80 species make this journey each autumn, and others occasionally (Wingate, 1973). Ships have reported that most birds appear within 600 km from the coast, but others appear at more than 2000 km out at sea, mainly warblers and shorebirds (McClintock et al., 1978). Small birds flying from Nova Scotia over the Atlantic face a non-stop 2500 km flight to the West Indies (Greater Antilles), or 3700 km to South America. They include the small Blackpoll Warbler (Setophaga striata, with a fat-free weight of about 11 g, which can double its body weight with fuel reserves before departure (Nisbet et al., 1963). Five individuals tracked on migration travelled for up to 3 days (62 hours) non-stop over 2270 2770 km to reach the West Indies (Greater Antilles), where they re-fuelled before moving on to South America (DeLuca et al., 2015). Some shorebirds that breed on the northern tundras also set off from staging areas in Newfoundland and Nova Scotia and strike out over the Atlantic to South America. They make the longer journey of up to 3700 km, but can fly twice as fast as Blackpoll Warblers (60 70 km per hour vs 30 35 km per hour), so accomplish the flight in around half the time (McClintock et al., 1978). They include the American Golden Plover (Pluvialis dominica), Hudsonian Godwit (Limosa haemastica) and White-rumped Sandpiper (Calidris fuscicollis). Shorebirds and passerines on this journey have been found by radar to reach heights of 4 6 km (Williams et al., 1977), taking advantage of the northwest winds that follow a front. Flight speeds of passerines measured by radar implied flight times of 18 hours to Bermuda, 64 70 hours to the Caribbean and 80 90 hours to South America (Williams et al., 1978). Waders could presumably cover these distances in half the time. This over-water ‘shortcut’ saves more than 1000 km on the more roundabout overland coastal route. In the spring, however, when winds are against them, these same species return by the overland route, northward through eastern North America. Other long sea-crossings by North American birds are undertaken by shorebirds and waterfowl that migrate from Alaska over the eastern Pacific to make landfall at various sites between southern Canada (2500 km) and Baja California (up to 5000 km), depending on species. Again, some species make this flight only in autumn when winds are favourable and return in spring by the longer landward route. Other long over-water journeys are flown by shorebirds and ducks that migrate between Alaska and Hawaii ( . 4000 km) or between Alaska and South Pacific Islands without stopping in Hawaii (6000 9000 km) (Thompson, 1973; Johnson et al., 1989, 1997; Williams & Williams, 1990, 1999; Marks & Redmond, 1994). These journeys are remarkable not only for the distances involved but also for the great navigational precision required to find such tiny wintering areas in the vastness of the Pacific. Participants include the Bristle-thighed Curlew (Numenius tahitiensis), which is the only species that breeds on a continent and winters entirely on Pacific Islands. It occurs as two populations, breeding in north and south Alaska and wintering in the east-central and west-central Pacific Islands respectively. Flights of satellite-tracked birds took 4.5 and 8.5 days to cover 4400 and 8300 km required (Gill et al., 2008).

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Most impressively, the Bar-tailed Godwits (race Limosa lapponica baueri) which breed in Alaska accomplish each autumn an astonishing trans-Pacific flight to New Zealand (Figure 6.2). Satellite-tracked birds flew the whole 7008 11,680 km without stopping in 6 9 days (Gill et al., 2009; Battley et al., 2012). One female flew the 11,680 km in just 8.1 days (1442 km per day). This flight requires enormous fat reserves, and despite considerable shrinkage of other body organs, the birds depart at twice their normal weights (Chapter 5). One advantage of this oversea flight is the saving in distance, for if the birds migrated round the coasts of eastern Asia (which they visit in spring), they would have to travel about 16,000 km one way, a journey about 60% longer than the direct trans-Pacific route. The single flight may also be safer, avoiding exposure to predators, parasites and pathogens, as well as being accomplished in a much shorter period of 6 9 days in favourable winds (Gill et al., 2009). It also saves the birds from having to reconstruct their digestive system en route, which would be necessary if they were to refuel, adding further cost and time to the journey. Some 150,000 L. l. baueri godwits make this journey every year, yet only trivial numbers are ever sighted on Pacific Islands where they might be expected to stop in emergencies. On return passage, when the wind is less favourable, these godwits follow a more circuitous route, travelling first to the Yellow Sea between China and Korea, an overwater distance of about 10,000 km, which satellite-tagged birds also covered in about 7 days (one individual took 9.5 days). The birds re-fuelled there for about 6 weeks, before continuing another 6800 km to the coast of Alaska, near their breeding areas (Gill et al., 2009). This makes the overall spring journey longer in time and distance than the autumn one. It may be favoured by wind conditions, but in addition re-fuelling in the Yellow Sea may give the birds surplus reserves to help with breeding (Chapter 5). Birds that leave New Zealand in spring have fat reserves not much smaller than those that leave Alaska in autumn but have shrunk their internal organs to a lesser extent (Pennycuick & Battley, 2003). A single bird for which the entire migration was tracked, travelled 29,280 km there and back, the longest loop migration yet recorded (Battley et al., 2012). Apart from the length of the journey, the navigational precision required on a trip of this type is breathtaking. From the autumn departure point in Alaska, the target area of New Zealand is so small in the vastness of the South Pacific that it gives little scope for off-route deviations. The days the birds selected for departure gave the greatest possible wind assistance not only at the time but over the whole of both journeys, although to obtain this assistance the birds would have to have continually changed altitude and flown mainly above 3000 m (Conklin & Battley, 2011; Gill et al., 2014a,b). And maintaining an estimated metabolic rate of 8 10 times the basal rate (Pennycuick, 1998; Gill et al., 2005, 2009) for 6 9 days represents a metabolic feat previously unrecorded in any animal and presumably involves an amazing degree of sleep deprivation. Other godwits perform long sea-crossings elsewhere in the world, but none as long as the L. l. baueri birds. One might think that the costs of migration would be high in these long-distance birds, travelling near the extremes of endurance and physiological capability. But they all show high annual survival rates no different from waders making shorter journeys, with little or no evidence of elevated mortality during migration (Conklin et al., 2017). Little is known of landbird migrations over the Indian Ocean, but one of the most notable involves the Amur Falcons (Falco amurensis) which breed in eastern Asia and winter in southern Africa. In both autumn and spring, their migration involves a sea crossing of 2400 3100 km between India and East Africa, the longest over-water flight known from any raptor (Chapter 7; Meyburg et al., 2017a,b). Various other birds, including cuckoos, bee-eaters and nightjars (notably the Jacobin Cuckoo (Clamator jacobinus) and the Blue-cheeked Bee-eater (Merops persicus)) make the same oversea journey. All these species eat dragonflies, large numbers of which also migrate between India and East Africa at the same seasons and could potentially provide an overwater food source (Anderson, 2009). Further south, the Broad-billed Roller (Coracias glaucurus) migrates between Madagascar and the Congo, involving a water crossing of 500 1000 km. Long over-water migrations are also undertaken by three species which breed in New Zealand, namely the Doublebanded Plover (Charadrius bicinctus) which crosses 2000 km of sea to Australia, the small Shining Bronze-cuckoo (Chrysococcyx lucidus) which crosses 2500 km of sea to the Bismarck and Solomon Islands, and the much larger Pacific Long-tailed Cuckoo (Eudynamys taitensis), which crosses 2700 km or more to various small islands in the east and central Pacific. The longest of all bird migrations, however, are performed by seabirds, notably by the Arctic Tern (Sterna paradisaea), in which most individuals migrate each year between Arctic and Antarctic waters. In the process, these terns experience more daylight per year than any other birds, as they shuttle between the continuous daylight of northern and southern summers. No meaningful distance can be given for this migration because individuals remain on the move for most of their non-breeding season, travelling at least part way round the Antarctic continent. But as an extreme example, one tracked Arctic Tern breeding in the White Sea area travelled an estimated 103,600 km between successive breeding seasons (Volkov et al., 2017). Other seabirds that move long distances include the Sooty Shearwaters (Ardenna grisea) which travel from New Zealand more than 64,000 km around the Pacific in their non-breeding period (Chapter 8).

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Not all seabirds can cross oceans. The plumage of cormorants and shags is poorly waterproofed, which restricts the overwater journeys they can make. Also, not all seabirds stick to the sea on their migrations, as some species, such as Parasitic Jaeger (Stercorarius paradisea), make long journeys over land. We know this because they occasionally appear on large lakes (eg, the Great Lakes in North America), and dead ones are occasionally picked up far inland. However, little is known of these overland migrations, as the birds evidently fly high, well beyond the range of human vision. Tracking studies are needed to reveal more of their journeys.

DESERT CROSSINGS Overall, one-third of the earth’s land area is classed as desert (Figure 6.3). The term covers a range of arid landscapes, from the sparsely vegetated regions of western North America to totally barren rock and sand typical of much of the Sahara. Providing there is some vegetation, specialist bird species can survive and breed in such arid habitats, but most birds cannot find sufficient food or water, or remain active at such high temperatures. Most deserts are at their best in spring, after winter rains have promoted plant growth and flowering. They are much less used in autumn when plants have withered under the desiccating heat of summer. The problems of desert flights include the long distances without food or water, low humidity, and searing daytime temperatures which could lead to overheating and dehydration. Birds can avoid the extremes of heat by migrating at night or at high altitudes, or by sheltering in the shade by day. The main sources of water in deserts are rivers flowing in from wetter regions, which provide green bands of riparian vegetation in otherwise parched landscapes, and the scattered oases which form wherever groundwater breaks the surface. The green of these features stands out from a long distance against the brown of the surrounding desert and can provide habitat, food and water for various birds. However, oases and their associated vegetation typically cover very small areas, of up to a few hectares, and are usually few and far between. Although at migration times they can seem packed with birds, they are likely to be visited by only a tiny proportion of those passing over. Moreover, oases are normally used for refuelling only by those species adapted to the habitats they provide. The largest and most severe desert in the world sits right across the path of migrants travelling between western Eurasia and the Afrotropics. The Sahara stretches over 5000 km from the Atlantic coast in the west to the Saudi Arabian

FIGURE 6.3 The main desert areas of the world.

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peninsula in the east, extends 1500 1800 km from north to south and covers 9.2 million km2, about the same size as the United States including Alaska. Much of its huge area is totally bereft of vegetation, lacking even the sparsest of desert scrub. This desert varies greatly in severity in different longitudes. The Atlantic coastal strip in the west provides a continuum of scrubby vegetation running north to south, extending in places up to 200 km inland. In the east, the Nile Valley provides a narrow green corridor for migrants, the only route that is abundantly supplied with both food and water. Over the rest of the desert, vegetation is mostly sparse to non-existent, apart from the few isolated oases, mere pinpricks in the vastness of the desert. Yet despite its inhospitability, this desert is crossed and re-crossed at all longitudes by an estimated 3.1 billion birds of 186 species every year, a total that was much larger in the recent past (Chapter 26). Birds that follow the Nile Valley in the east, with its border of swamps and cultivated land, or the Atlantic coast in the west with its broad belt of sparse desert scrub, could in theory migrate with short flights and frequent refuelling stops, as they could find food at various points on route. The concentrations of migrants are greater at the west and east ends of the desert than in the middle section, at least in autumn, as revealed by radar, but concentrations seem unexceptional in the Nile Valley itself, apart from waterbirds (Moreau, 1961; Biebach, 1990; Bruderer & Liechti, 1999). The option of flight from oasis to oasis is possible only along a row of mountains and oases that stretches southeast from Morocco. Elsewhere, oases are too few and far between to provide effective stepping stones. Most species apparently migrate on a broad front over the most hostile parts of the desert, but the same species may behave differently in spring and autumn, or at different points in the crossing (see below). The greater density of migrants at the west and east ends of the desert in autumn may be as much a consequence of the funneling effect of land areas to the north as of the desert conditions themselves. Most of the west European migrants cross the Mediterranean at its narrowest, around Gibraltar, from which they reach the western edge of the desert, while the east European and Asian migrants cross the desert in its eastern sector or traverse Arabia instead. These various factors combine to make crossing the Sahara one of the most arduous overland journeys undertaken by migrating birds. For some, it also follows (in autumn) or precedes (in spring) a crossing of the Mediterranean Sea at its widest points. In the west and east parts of the North African coastal region green habitat extends hundreds of kilometres to the south, but in the central part little vegetated habitat is available between the sea and the desert, offering only limited opportunities for refuelling. This central coastal strip over most of its length is typically less than 20 km from north to south, consisting of sparse perennial scrub, with the addition in spring of ephemeral herbage dependent on winter rain. Beyond this to the south lies a barren desert. In some bird species, at least some individuals cross both the Mediterranean Sea and Sahara Desert in a single nonstop flight, while others break their journey for refuelling in North Africa (Moreau, 1961; Bairlein, 1992; Biebach, 1998). The Mediterranean Sea is as little as 15 km from north to south at its narrowest point at Gibraltar and as much as 1600 km from north to south at its widest point further east. The Sahara desert varies from 1500 1800 km from north to south at different points along its west-east extent, so the sea-plus-desert crossing requires flights of up to 3400 km, depending on the route taken. These distances refer to north south crossings, and any birds traversing the desert diagonally could face even longer flights. Large birds flying non-stop north south at 80 km per hour (say) in still air would require up to 43 hours for the combined sea-and-desert journey, and around 19 23 hours for the desert alone, while small birds flying non-stop at half this speed would require twice as long (up to about 86 hours). The most numerous species to make this journey is the Willow Warbler (Phylloscopus trochilus), which is also one of the smallest (fat-free weight about 7 g) and slowest fliers (still-air speed on migration 34 km per hour). This species would take up to 100 hours for the sea-and-desert journey in still air, and 44 53 hours for the desert alone. In all such species, however, these times could be substantially shortened with the help of tailwinds, or lengthened by headwinds or stops, or by crossing the desert diagonally. Conditions for trans-Saharan migration differ greatly between the seasons. When the migrants move south in autumn, the region north of the desert is at its seasonal driest, but the Sahel zone immediately to the south is near the end of its wet season. Vegetation is green, flood pools are common and insects are plentiful. In spring when migrants move north, the opposite prevails, as the Sahel is reaching the end of its dry season when conditions for fuelling are far from ideal. But conditions north of the desert are at their best in spring, following winter rains. This seasonal difference in conditions may explain why many more migrants are seen in North Africa and around Mediterranean coasts in spring than in autumn, even though their overall population levels are lower in spring. The implications are that many more birds make a combined Mediterranean Saharan crossing without feeding in autumn than in spring and that many more stop to refuel in North Africa in spring than in autumn. In autumn, when migrants are heading south, the trade winds provide tailwind support from ground level up to somewhere above 1000 m, whereas in spring when the same winds blow, birds must fly above this level to reach the anti-trade winds blowing in the opposite direction, if they are to gain support on their northward journey. Radar and tracking studies

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have confirmed that birds do indeed fly higher over the Sahara in spring than in autumn, thus gaining favourable winds in both seasons (Schmaljohann et al., 2009; Liechti et al., 2018; Jigue´t et al., 2019a,b). Otherwise, the only way to reduce the effect of headwinds in spring would be to fly low, say within 500 m of the ground where winds are slowed by friction. Most species cross the Sahara by accumulating the necessary body reserves beforehand (Chapter 5). Passerines increase their body weight by more than 50%, and some by around 100%, effectively doubling their weights before departure (Chapter 5; Fry et al., 1970; Jenni & Jenni-Eiermann, 1998; Ottosson et al., 2005). While some species, such as Eurasian Reed Warbler and Common Whitethroat, accumulate most of the fuel reserve necessary for the journey close to the desert, others, such as Wood Warbler (Phylloscopus sibilatrix) and Pied Flycatcher (Ficedula hypoleuca), accumulate most of up to several hundred kilometres north of the desert in autumn or several hundred kilometres to the south of it in spring (Chapter 5). This may make fuelling easier for these species but increases the distance they must fly without substantial further fuelling. As shown by tracking studies, Pied Flycatchers fatten mainly in northern Iberia in autumn and may then migrate without feeding until they reach the south of the Sahara (Bell et al., 2022). Sedge Warblers (Acrocephalus schoenobaenus) are even more extreme, accumulating sufficient body reserves as far north as Britain to get them to the south of the Sahara (Gladwin, 1963). This does not mean that these birds fly non-stop, however, only that they do not need to feed on route. Similarly, in spring, species such as the Common Redstart (Phoenicurus phoenicurus) living just south of the desert in the Sahel Zone, fatten there before migration, while some Eurasian Blackcaps (Sylvia atricapilla), Garden Warblers (Sylvia Borin), Whitethroats (Curruca communis) and others fatten well south of the Sahara, in the more mesic Guinea zone (Hjort et al., 1996; Ottosson et al., 2005). In effect, the Saharan crossing is much longer for forest-dwelling species, such as Pied Flycatcher and Wood Warbler, than for open-country or shrub-dwelling species which can find foraging areas at the northern and southern edges of the desert.

Trans-Saharan flights From autumn radar studies at sites in the Egyptian Sahara, Biebach et al. (2000) concluded that about 20% of all migrants detected were involved in non-stop migration and 80% in intermittent migration, with stopovers at the coast (70%) or in the desert (10%). Another radar study on the opposite side of the Sahara in Mauritania also showed the prevalence of intermittent migration, with birds migrating at night and resting by day (Schmaljohann et al., 2007). Birds tracked by satellite or geolocators have confirmed that some birds do indeed cross the Mediterranean Sea and Sahara Desert in a single flight and that some fly even further. Excluding swifts which spend most of their lives on the wing (Chapter 3), the longest non-stop flights so far recorded for trans-Saharan migrants involved some Great Snipes (Gallinago media) which flew directly from their breeding areas in northern Sweden to their wintering areas in subSaharan Africa (Lindstro¨m et al., 2015). Their autumn flights averaged 5500 km and lasted 64 hours, giving average ground speeds of around 90 km per hour, the fastest yet recorded from waders. These birds arrived in the Sahel zone before the rains ended and stayed for about 3 weeks before moving on to the lower Congo River region where they spent the next 7 months. In spring the birds made Sahara-Mediterranean flights at similar speed as in autumn, but the remaining northward migration through Eastern Europe was notably slower, with refuelling stops. Other long non-stop flights were made by Bar-tailed Godwits and Black-tailed Godwits (Limosa limosa) travelling directly from West Africa to the Dutch Waddensea, distances of about 5000 km (Drent & Piersma, 1990; Hooijmeijer et al., 2013), and by Black-tailed Godwits and others travelling around 3000 km between West Africa and Portugal (Loonstra et al., 2019). Non-stop flights over sea and desert are probably also typical of fast-flying ducks, but they remain as yet unconfirmed by tracking studies. Among smaller birds, apparent non-stop flights over sea and desert have been confirmed in some small forest-dwelling passerines, such as the Wood Warbler and Ficedula flycatchers as mentioned above, and smaller numbers of some other species (Box 6.1; Adamik et al., 2016; Jigue´t et al., 2019a,b). However, as first revealed by radar and ground observations, and later supported by tracking studies, most small passerines break their desert journeys in the daytime, but without feeding. They descend to spend the day sheltering motionless near oases, or in the open desert in the shade of rocks, continuing their journey in the cool of night (Bairlein, 1987, 1988, 1992; Biebach, 1990, 1992, 1998; Biebach et al., 1986; Bruderer, 1994; Salewski et al., 2010). Some of them land at dawn, but depending on conditions, others continue for several hours into the day before descending (Jigue´t et al., 2019a,b). In this way, they can cross the desert in a few nocturnal flights, while gaining rest or sleep by day. Examples include many individual Garden Warblers, Lesser Whitethroats (Curruca curruca) and Willow Warblers. The majority of migrants trapped at such rest sites showed high body mass and fat loading, with sufficient reserves for onward flight, so they had not been grounded through lack of fuel. But in resting by day and flying by night, they travelled in cooler and less turbulent air and may thus have reduced their energy costs and dehydration risks, despite adding at least 1 or 2 nights to their journey time (giving 2 4 nights for the total desert crossing). Yet other

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BOX 6.1 Findings from tracking studies of small birds crossing the Sahara Desert. Geolocators employed on 130 individuals of 10 migratory songbird species crossing the Sahara Desert revealed a range of different strategies, with most species making daytime stops (Jigue´t et al., 2019a,b). The Wood Warbler (P. sibilatrix) was the only species in which all three individuals studied made a non-stop flight across the desert in both autumn and spring, in all cases lasting over 2 nights and 2 days. At the other extreme, all 11 Eurasian Reed Warblers (Acrocephalus scirpaceous) and all 18 Common Nightingales (Luscinia megarhynchos) (except one in autumn) stopped in the desert in both seasons, while five Mediterranean Flycatchers (Muscicapa tyrrhenica) all stopped in the desert in autumn. Fifteen Willow Warblers (P. trochilus) revealed the most diverse patterns in autumn, with four individuals performing only nocturnal flights, seven prolonging nocturnal flights into the morning, and four performing non-stop flights over a complete day. These three patterns also occurred among samples of 20 Whinchats (Saxicola rubetra), 22 Spotted Flycatchers (M. striata), 9 Tree Pipits (Anthus trivialis) and the Common Nightingales already mentioned. Overall, diurnal stopover in the desert emerged as a common strategy in autumn, while in spring most species prolonged some nocturnal flights into the day. Non-stop flights over the desert also occurred more frequently in spring than in autumn, and more frequently in tree-foliage gleaners than in others. Temperature sensors suggested that these songbirds crossed the desert with flight bouts at various altitudes according to species and season, ranging from low above the ground in autumn to more than 2000 m in spring. Tracked individuals changed flight altitudes repeatedly during a flight bout, perhaps indicating a continuing search for more favourable winds. Another study involved four Pied Flycatchers (Ficedula hypoleuca), 13 Collared Flycatchers (Ficedula albicollis), 12 Eurasian Reed Warblers (Acrocephalus scirpaceus) and five Aquatic Warblers (Acrocephalus paludicola) (Adamik et al., 2016). Most of these birds made non-stop flights lasting 1 3 days (65% of 29 autumn flights, and 91% of 23 spring journeys). Among Pied Flycatchers from Britain, 45 of 50 Sahara crossings were non-stop, whether in autumn or spring (Bell et al., 2022). Regular daytime stops during migration were also recorded in 13 Great Reed Warblers (A. arundinaceus) and 5 Hoopoes (Upupa epops) flying over the Sahara (Liechti et al., 2018). These birds flew chiefly at night, but sometimes extended their flight into the day. Both species flew at higher mean altitudes in spring than in autumn, and frequently ascended to altitudes above 3000 m and the warblers occasionally to above 6000 m. The duration of journeys recorded from several other species suggested that short rests (presumably in daytime) were usual in tracked Red-backed Shrikes (Lanius collurio), Common Cuckoos (Cuculus canorus) and European Nightjars (Caprimulgus europaeus) (Tøttrup et al., 2011; Willemoes et al., 2014; Norevik et al., 2017). Common Swifts (Apus apus) made some longer pauses, suggesting that they may have found swarms of insects over desert oases (A˚kesson et al., 2016), and one tagged Nightjar made 3 several-day stops in the northern Sahara in spring, perhaps also refuelling on insects (Jacobsen et al., 2017). Overall, these findings confirmed a diversity of strategies among small birds crossing the Sahara, with variations between and also within species, according to season and prevailing conditions.

individuals of these same species stopped at oases where they fed and drank, usually remaining for 2 4 days, but occasionally for up to 3 weeks at a time, if they needed to rebuild body reserves. Other birds seen at oases may have stopped there to rest during the daytime, but without needing to feed (Salewski et al., 2010). Strictly diurnal migrants, such as broad-winged raptors dependent on daytime thermals, stop every night (as shown by satellite tracking of several species, Chapter 7) but would normally obtain no food then. However, some tracked raptors, notably Ospreys (Pandion haliaetus) and falcons which depend less on thermals, have also occasionally been recorded flying over the desert at night. Surprisingly, some species accumulate no more than moderate fat reserves and would need to feed on route to cross the desert successfully. In the Western Sahara, they include the Spotted Flycatcher (Muscicapa striata) and various species of dry scrub habitats, such as the Olivaceous Warbler (Iduna opaca) and Subalpine Warbler (Curruca cantillans). This west side of the desert may offer a mixture of scrub patches and oases close enough to allow stepping-stone journeys (Jenni-Eiermann et al., 2011; Hama et al., 2013). Clearly, a diversity of migration strategies exists for desert crossing, varying from non-stop flights to nocturnal flights with daytime rests, daytime flights with nocturnal rests, and occasional stops of a few days (some involving refuelling at oases or scrub patches). The frequencies of different strategies differ between seasons and also vary between and within species, according to location and conditions at the time. In general, in the absence of feeding stops, most birds seem to take 2 5 days to cross the Sahara, depending on their flight speed, route and number of rest stops.

Physiological constraints The main assumed value of daytime stops is to conserve water because, by remaining inactive in the shade, the bird can minimize internal heat production. Only about one-fifth of the energy expended by the muscle is converted to

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mechanical power and the rest to heat. To avoid overheating, the bird must pant, which leads to water loss and eventually to dehydration (Chapter 4). In the absence of drinking water, this risk can be offset by metabolic water production (as occurs automatically as a bird burns fuel for flight) or, as mentioned above, by flying at high altitudes where the air is cooler, or at night when temperatures are lower than during the day. For flying birds, metabolic water derived from the catabolism of body fat, carbohydrate or protein has been judged as sufficient to offset the danger of overheating in ambient temperatures up to around 10 C (Biebach, 1990; Nachtigall, 1990). Up to this temperature, small birds should therefore have no additional water loss, even on long flights. But above 10 C, further evaporative cooling would be needed, bringing a risk of dehydration. In the Sahara in autumn, if one assumes (from records) an air temperature at ground level of 30 C by day and 8 C by night, and a decline of 7 C with each 1000 m rise in elevation, an air temperature lower than 10 C would be found by day at more than 3000 m above ground, and by night at more than 1000 m above ground. In spring, when the ground would typically be cooler than in autumn, an air temperature of 10 C would be found at an altitude greater than 1750 m by day and 500 m by night. Any deviation from the 10 C estimate would of course alter the altitude estimates. At very high altitudes, birds would find cooler temperatures but also reduced humidity which could raise water loss, with the thinner air leading to increased ventilation, and hence to further loss in respiratory water (Carmi et al., 1992; Carmi & Pinshow, 1995; Klaassen, 1995; Klaassen et al., 1999; Guillemette et al., 2016). Overall, the best option for a small bird may be to fly at night at moderate altitude (say 500 2000 m) and rest in the shade by day. By flying at night, birds also avoid strong daytime turbulence and thus conserve energy. It may be the cooler temperatures in spring that allow small birds to cross the desert more rapidly then than in autumn. Radar measurements of the height distributions of migrants over southern Israel in autumn and spring, combined with simultaneous altitudinal recordings of winds, enabled the relative importance of wind conditions, energy and water constraints on flight range to be assessed (Liechti et al., 2000). Predictions were made of the optimal flight altitude, in the conditions prevailing, if birds took account only of tailwinds, only of energy conservation, or of both energy and water conservation, in achieving maximum flight range. These predicted flight altitudes were then compared with the actual height distributions recorded in the field. The authors concluded that wind profiles, and therefore energy rather than water limitation, governed the altitudinal distribution of these nocturnal migrants. However, this conclusion, drawn from birds spread over a wide range of altitudes, does not exclude the possibility that individuals may adjust their altitude to whatever was most limiting for them at the time, including water if they were becoming dehydrated. Regarding fuel type, calculations for Willow Warblers and Eurasian Golden Orioles (Oriolus oriolus) revealed that, under most flying conditions, if the birds used fat alone as fuel, water could impose the main limitation to their total flight range, but if they used 70% fat and 30% muscle (which is two-thirds water), then energy rather than water could become the main constraint (Klaassen & Biebach, 2000). The bird would then gain 26% less energy than from fat alone, but correspondingly more water. This situation is probably closer to reality. Studies of body composition provide further insight. The proportion of water within a bird’s body decreases with increase in fat content, because fat is stored anhydrously (Chapter 5). However, the fat-free component of a bird’s body usually contains around 67% water, which can reduce to around 55% before the bird expires from dehydration (Haas & Beck, 1979). For Willow Warblers, Biebach (1990) calculated reduction in body water over one night from 67.5% to 62.9%, and over 2 rest days further reduction to 57.9%, which is still above the lethal value. Moreover, the water contents of birds caught in the Sahara Desert were in general around 67% 69% of fat-free weight (equivalent to a water: lean dry mass ratio of around 2:1), which is within the usual range of healthy birds (Chapter 5). In addition, the levels of Na1 ions and urea in the bloodstream, measured as further indicators of the state of hydration, were normal in most birds, and high only in lean ones (Biebach, 1990, 1991; Bairlein & Totzke, 1992). Furthermore, Willow Warblers and other small passerines found dying in the Libyan Desert showed normal water levels but had run out of fat, so in these birds, fuel rather than water seemed to have been limiting (Biebach, 1991). So most of the evidence cited for lack of water stress in migrant birds derives from the absence or scarcity of birds found with lowered water contents, even near the end of a long migration (Biebach, 1990, 1991; Gorney & Yom-Tov, 1994; Landys et al., 2000). This is not true of all samples, however, 78% of 409 birds caught on the Egyptian coast in autumn, after crossing the Mediterranean Sea, had water:lean dry mass ratios lower than 2:1, including 12% with ratios less than 1.4:1 (Fogden, 1972, Chapter 5). The latter were close to the level at which death would be expected. To some extent, as emphasized above, birds could best offset increasing water loss by catabolizing body protein (rather than fat) to yield water. The finding of migrants in the Sahara Desert with high fat but low protein reserves might reflect the effects of dehydration. Migrants clearly show behaviour that could be construed as anti-dehydration, such as shade-seeking, remaining immobile during the hottest part of the day, and drinking heavily on arrival at sites where water was available (Biebach, 1990; Klaassen, 2004).

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In conclusion, these findings suggest that crossing the Sahara even by non-stop flight is practicable with a balanced water budget if the bird flies with a tailwind at an appropriate altitude. This is difficult during the day in autumn because of the need for tailwinds which occur mainly below 1000 m, where temperatures are high. This may be why many birds fly by night and rest by day, as it allows them to remain inactive in shade and not generate extra body heat and thus conserve water. To judge from tracking studies, daytime rests are more frequent in autumn than in the cooler conditions of spring, and extensions of nocturnal flights into the morning are also more frequent in spring (Box 6.1), these differences contributing to overall faster journeys in spring. Nevertheless, evidence from the body composition of birds obtained on the Mediterranean Saharan crossing suggests that, while fuel energy could be limiting in some, water could be limiting in others (Chapter 5). Throughout its breadth, the Sahara would have offered better conditions a few thousand years ago than it does today, offering much more scrub cover, and more drinking sites. Conditions are continually worsening as the desert expands north and south under human influence. The annual rate of desertification in the Sahel has been calculated at about 0.5%, which corresponds to an area of at least 60,000 km2 added each year. In these times of climate change, other areas on the migration route are also becoming drier, including parts of Spain and North Africa and the Sahel zone to the south. Such trends are likely to continue into the future.

Asian deserts and mountains Migrants travelling between eastern Asia and the Afrotropics face a difficult and even longer journey than those migrating between Europe and the Afrotropics. They include eastern populations of the Willow Warbler, Sedge Warbler, Garden Warbler, Common Redstart and Northern Wheatear, among others. These birds have overall journeys 1.5 2.0 times longer than their European equivalents. They have to cross a difficult succession of hostile areas, including the deserts and semi-deserts of western Central Asia, the almost treeless areas of the Iranian highlands, and the deserts of Arabia. Some also have to cross the world’s highest ground in western Asia, including the Tien Shan, Pamiro-Altai and the Himalayas. For forest passerines, inhospitable areas in Central Asia alone span 2000 3000 km, and for eastern Siberian and Alaskan populations of some species total journeys may exceed 14,000 km each way. The migrations of Northern Wheatears tracked from Alaska across Asia to East Africa reached nearly 15,000 km (Schmaljohann et al., 2012). These mainly overland journeys, skirting north of the Himalayas, were the longest yet recorded from any songbird, the same species which over the North Atlantic performs the longest sea crossing known from a songbird (see above). Migration in the Asian deserts and mountains was studied years ago by a large-scale programme of observation and trapping at more than 20 different sites scattered between the Caspian Sea in the west and the Hindu Kush, Pamir and Tien Shan Mountains in the east (Figure 6.4; Dolnik, 1990). These sites together spanned the region from 37 48 N and 53 78 E. This region hosts a crossroads of migration routes to two main wintering areas so that two main axes of migration ran northwest southeast for Siberian birds wintering in southern Asia, mainly India, and northeast southwest for Siberian birds wintering in the Afrotropics. Hence, many of the birds that cross the Asian deserts also cross the eastern Sahara or Arabian Peninsula on the same migration, for which greater fat levels are needed. Of birds captured, 25 species (75.6% of all captures) winter in Africa, and 23 species (9.5% of captures) in Asia, mostly in India, while 8 species (14.9% of captures) winter in either Africa or India. The deserts of Central Asia present a much less arduous journey than the Sahara, because they support more rivers and lakes and generally more vegetation, especially in spring after winter precipitation. An average of 1.5 billion birds (85% passerines) are estimated to cross these deserts on a broad front each autumn and about 0.75 billion each spring, flying mainly at night (Dolnik, 1990). The oases, desert lakes and rivers do not provide adequate foraging sites for all these birds and, because of the intense competition at such places, the rate of fat deposition there is low about the same as in the open desert. Nonetheless, in general, the basic strategy used by passerines migrating across this arid region centres more on effective refuelling during daily stopovers than on maximal fuel storage before starting the journey. The birds thus maintain a moderate rate of travel across the desert, limited by the opportunities for refuelling, but with no net fat loss over the journey. Many birds of forest and other habitats have little option but to feed in unfamiliar arid habitats with little vegetation. On average, a passerine migrant foraging in the Asian deserts accumulates during one day enough fat to support an estimated 1.4 hours of migratory flight in spring and 0.6 hour in autumn (Dolnik, 1990). At both seasons, the average fatness of small passerine migrants initiating nocturnal flight in Asian deserts was 20% of fat-free mass, and in those trapped just at the end of their nocturnal flights it was around 10%, a loss expected over at least 4 hours of nocturnal flight. In the Asian deserts, as in the Sahara, birds found by day in shady places that offered little food tended to have high fat levels, whereas those found at potential foraging sites near water tended to have low fat levels (Dolnik, 1990). Evidently, lean birds were more specific in their choice of resting sites than fat ones.

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FIGURE 6.4 Density (length of arrow) and main direction (azimuth of arrow) of nocturnal bird migration above moon-watch sites indicated by the origins of the arrows. The numbers beneath the maps show the total number of migrants (in millions) that passed in each season through the fronts delimited by the brackets. Large water bodies are indicated by blue shading, the largest being the eastern part of the Caspian Sea at the left and the Aral Sea at longitude 60 E. Mountain ranges are stippled; the Elburz range is at the lower left; the Hindu Kush, the Pamirs and the Tien Shan respectively are eastward from about 65 E. In autumn, birds mostly crossed the mountain ranges (then at their best), avoiding the dry deserts to the west; but in spring they mostly crossed the deserts (then at their most lush) and avoided the mountains (then snow-covered). Redrawn from Dolnik (1990).

The numbers of birds seen and caught in the western deserts were much higher in spring than in autumn, about 2.6 times higher according to data obtained by ‘moon-watching’ (Chapter 2). This was partly because birds took mainly different routes at the two seasons, but also because many birds stopped in spring but flew over in autumn (Bolshakov, 2003). In spring, practically all nocturnal passerine migrants avoided crossing the highlands of Central Asia, which at that time were still snow-covered, and took the desert route instead, whereas in autumn, mountain crossing was much commoner, especially among species wintering in India (Figure 6.4). In addition, captures at stopovers and long-distance recoveries of ringed birds suggested that, in autumn, most transit passerines from the forest zone of central and eastern Siberia made a detour round the north and northwest edges of the deserts. By heading westward towards Europe, before veering southward to Africa, they migrated through more hospitable areas but lengthened the journey by another 2000 km, bringing the total to 8000 10,000 km. It seemed, therefore, that, in spring when the deserts were at their most propitious, many migrants crossed them, feeding on route, but in autumn birds largely avoided the deserts by migrating over the mountains to the east, or by heading westward for 2000 km or more, before veering south towards Africa. By taking somewhat different routes in autumn and spring, the birds made the best of prevailing conditions at both seasons.

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The Arabian Peninsula offers an alternative route from the Sahara into the more habitable parts of Africa. Not only is this desert less wide than the Sahara, but the hills and mountains around its borders are vegetated. It supports a number of oases and generally has more plant life than the Sahara, because it receives more rain. Not surprisingly, therefore, the Arabian Peninsula is crossed not only by the migrants from Asia heading to Africa but also by many birds from central and Eastern Europe. For the European birds, the route through Arabia is used more in spring than in autumn, with many birds performing a loop migration travelling south in Africa and north through Arabia. This route has been confirmed in Red-backed Shrikes (Lanius collurio) and Thrush Nightingales (Luscinia luscinia) by tracking studies (Tøttrup et al., 2011, 2012), but observations and ring recoveries show that Lesser Grey Shrikes (Lanius minor), Great Reed Warblers (Acrocephalus arundinaceus), Sedge Warblers, Willow Warblers, Garden Warblers and Spotted Flycatchers also take this route (Pearson, 1990; Pearson & Lack, 1992).

North American deserts The western North American deserts are easier to cross than the Eurasian African ones, because they are generally smaller, better vegetated, and better endowed with oases and riparian vegetation where birds can feed. Some of the desert towns, with their well-watered gardens, also offer good feeding for some kinds of birds, but many former rivers are now dry for most of the year, through excess water abstraction. Nevertheless, some oases attract many passing migrants, and hotspots for bird-watching can be found scattered through all the main desert areas. In southern California, such hotspots include the Fortynine Springs Oasis in Joshua National Park and the Big Morongo Canyon Preserve (several hectares of riparian cottonwoods) in Morongo Valley, each attracting more than 100 regular passage species at migration times. Again, however, it is likely that most migrating birds fly over without stopping. One of the most interesting birds to cross the western American deserts each year is the Black-necked Grebe (Podiceps nigricollis), as it travels from the Great Salt Lake in Utah to the Gulf of California (Jehl et al., 2003). These aquatic birds develop flight seasonally, especially for migration, losing body weight but building pectoral muscles for the journey (Chapter 5). The shape of these birds, adapted for foot-propelled diving, is not ideal for flight, and the energetic costs are the highest recorded for any bird species, at around 25 3 BMR. The birds take off from water, after a long, footpattering taxi. They fly at night and have to cross more than 1000 km of mainly desert in non-stop flight, potential stopping places being almost non-existent. To judge from radar studies, the flight is direct and fast, taking about 17 hours, and ideally completed within a single night. By storing massive body reserves on the Great Salt Lake in autumn, grebes can postpone their migration beyond the date in autumn when their local food supplies collapse, waiting until nights are longer and thereby benefiting from longer and safer flying time. The grebes thus migrate to their wintering areas later than any other North American bird species and on body reserves accumulated weeks previously (Chapter 5). Black-necked Grebes also seem unusually accident-prone, and departure often falls short of ideal. The birds assemble in large dense flocks, and on appropriate nights, tens of thousands take-off simultaneously, shortly after sunset. This early departure makes the best use of the available dark period, but the numbers involved produce mid-air collisions. On some nights hundreds crash into one another, and some die within moments of taking off (Jehl et al., 2003). If the birds encounter rain or headwinds within an hour or so after take-off, they can return to the staging lakes, as confirmed by radar. But they then suffer further depletion of body reserves until conditions again become suitable, and at that time spent reserves cannot be replenished locally. In some years, conditions turn against these grebes later in their journey, when thousands can drift off course or crash-land in desert snow storms (Chapter 31). The return journey is less hazardous, as conditions are better and birds can stop and feed on route at the Salton Sea, which in spring offers abundant food.

HIGH MOUNTAINS Many migratory birds regularly cross high mountain ranges. The upper valleys may be snow-covered and frozen in spring, when they offer little or nothing for passing migrants, but in autumn many birds can stop and feed in whatever vegetation is available there. The main problems are the costs of climbing to high altitudes (greatest in large birds), and the low temperatures, thin air and low oxygen levels encountered on the highest ranges (Chapter 4). The highest mountains in the world, the Himalayas, sit right across a major north south bird migration route, as do most of the European ranges, such as the Pyrenees, Alps and Carpathians. Depending on their primary direction, birds may cross such mountains or fly around them. Radar studies suggest that many birds cross mountain ranges in non-stop flights, but visual observations confirm that others are funneled through valleys and passes, where they may stop and feed, especially in autumn when the ground is snow-free. For example, at the high pass of Col de Bretolet in the Swiss Alps (1923 m asl), about 75 species have been found regularly to rest and feed, and others occasionally.

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Many species migrate regularly each year over the Himalayas, reaching more than 5 km above sea level. At least one species crosses the highest parts, namely the Bar-headed Goose (Anser indicus), which nests on high-altitude lakes on the Tibetan Plateau and elsewhere, and winters in the lowlands of India. The New Zealand climber, George Lowe, who took part in the first successful ascent of Mount Everest in 1953, reported geese flying over the top. The peak is about 8839 m so the geese could have been flying at around 9 km asl. At this elevation, temperatures sink below 50 C, and oxygen pressures to below one-third of those at sea level. Assuming this observation was valid, it remains the greatest altitude at which any migrating bird has yet been seen. More recently, 38 Bar-headed Geese tracked by satellite typically travelled mainly through the valleys of the eastern Himalayas, hugging the mountains, but avoiding the summits (Hawkes et al., 2011, 2013). They repeatedly gained and lost height, climbing to altitudes greater than 7000 m for parts of their journey, but spending much of their time below 4000 m on a roller-coaster flight found to conserve energy (Bishop et al., 2015). To judge from heart rate, flight costs increased rapidly as air density declined, making it energetically advantageous to track the underlying terrain rather than maintaining highaltitude flight over the whole journey. Their median flying height was only 188 m above the ground. By hugging the contours, the geese could not only save energy but also use the full any available updrafts, reduce their exposure to adverse winds and gain greater safety through improved ground visibility and increased landing opportunities. The atmospheric challenges encountered at the very highest altitudes, coupled with the need for near-maximal physical performance in such conditions, probably explain why these geese rarely flew close to their altitude ceiling, typically remaining below 6000 m. Their chosen route was 112 km longer than the shortest route, but they could complete the Himalayan crossing within a day (around eight hours), even though their ground speeds suggested that they rarely profited from tailwinds. They flew mainly at night and in the early mornings when the air was cooler and denser. Some began their spring migration near sea level and reached altitudes exceeding 7000 m in a few hours, climbing at rates up to 0.6 m per second (equivalent to 2160 m per hour). The Bar-headed Goose is physiologically adapted to high-altitude flight, having bigger lungs for its size than other birds, a large heart which beats unusually rapidly, an improved oxygen supply to muscles and heart through a dense capillary network and haemoglobin that carries more oxygen (Butler, 2010; Hawkes et al., 2011). The blood shows no increase in haematocrit (packed cell volume) or haemoglobin concentration when exposed to simulated high altitude and therefore avoids any increase in viscosity which could impair circulation (Black & Tenney, 1980). Tests have shown that Bar-headed Geese can remain conscious and stand erect in hypobaric chambers under simulated high altitudes of slightly over 12 km (Black & Tenney, 1980). They can thus achieve feats of high-altitude performance that are matched by very few, if any, other animals, and can do so without needing time to acclimatize. It used to be thought that Bar-headed Geese were the only birds which regularly crossed the higher parts of the Himalayas and that most birds took lower routes or avoided these mountains altogether. But as the years have passed and tracking devices have come into use, many species have been found to pass through parts of the Himalayas that entail climbs to more than 6500 m. Such species include the Ruddy Shelduck (Tadorna ferruginia) and other waterfowl, Demoiselle Crane (Grus virgo), Peregrine Falcon (Falco peregrinus), Black Kite (Milvus migrans) and other soaring raptors, and almost certainly many small songbirds. In the Himalayas, Ruddy Shelducks have been found to reach altitudes of up to 6800 m and to climb at rates up to 0.74 m per second (Parr et al., 2017), while Black Kites have been found to accomplish most of their journeys above 3500 m, rising occasionally to above 6500 m (Kumar et al., 2020). In general, in the absence of long feeding stops, most birds seem to take 1 5 days to cross the Himalayas, depending on their flight speed, route and number of rest stops. Weighing around 8 kg with a wingspan of nearly 2.5 m, Himalayan Vultures (Gyps himalayensis) are among the largest of soaring bird species yet migrate annually over the Himalayas. As they climb from 50 to 6500 m by thermalling, they adjust to the halving of air density by increasing their soaring circles by 12.5% for every 1000 m rise in altitude (about 55% overall), and their airspeeds by about 30% overall (Sherub et al., 2016). Other soaring species would be expected to make similar adjustments to minimize their extra power output. In addition to the altitude problem in mountains, strong headwinds are often funneled through the valleys. One wellknown migration route in Nepal includes the Kali Gandaki Valley, which provides a useful corridor through the Himalayas, with passes reaching up to 6.5 km. This route is used each autumn by up to 50,000 Demoiselle Cranes, flocks of which start their daily migration as soon as thermals develop in the mornings, soaring to heights that enable them to cross the passes. However, time is against them, for by mid-morning strong headwinds develop, against which the cranes can make only slow progress. They also experience attacks from Golden Eagles (Aquila chrysaetos), spaced every few kilometres along the valley. Compared to other cranes, Demoiselles have one of the most difficult migrations, as they pass without respite through desert and high mountains which offer very few feeding or safe roosting sites. As revealed by satellite tracking, they accomplish their migration relatively quickly, crossing both desert and mountains within a week (Kanai et al., 2000). However, during their return journey from northwest India, they do not cross the

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Himalayas but fly around their western end, lengthening their journey by 24% (Galtbalt et al., 2022). If the cranes took the mountain route in spring, they would encounter treacherous conditions. High-flying birds must be equipped with mechanisms that prevent altitude sickness (hypoxia) caused by oxygen deficiency in thin air. All flying birds may have this facility to some extent (Novoa et al., 1991), but species living or migrating at high altitudes need additional development of traits which maintain oxygen delivery to the brain, gas exchange efficiency in the lung, cardiovascular and muscular performance, and oxygen diffusion to peripheral tissues (Berthold, 1996; Scott, 2011). Some birds have at least two types of haemoglobin, differing in their capacity to carry and release oxygen. One type acts as ‘normal haemoglobin’ for low altitudes, and the other as ‘high elevation haemoglobin’, which reaches the greatest concentration in the blood of species which fly at especially high altitudes (Heibl & Braunitzer, 1988). In general among birds, lung ventilation is especially effective because of the air sacs, which allow continual flow of air through the lungs, but the lungs themselves also tend to be larger in high-altitude birds. Such birds also tend to have larger wings than their lowland relatives, reducing the metabolic costs of staying aloft in thin air (Scott, 2011). The altitudes reached by many flying birds, without needing time to acclimatize, greatly exceed the limits of most mammals. Without acclimatization, a person is in trouble at more than 4 km above sea level, but with training can reach 5 km without becoming breathless. However, birds in general have an inherently higher tolerance to altitude sickness than mammals. Even a House Sparrow (Passer domesticus) was able to maintain flight at 6.1 km, while the same reduced oxygen level rendered a mouse comatose (Tucker, 1968). But not all birds have such flexibility in their flight altitudes and, whatever the advantages of high-altitude flight, many large species seem constrained to migrate at low elevations, probably for physiological or energy-based reasons (Chapter 3). Further insight has come from studies around the Alps in Europe. Most short-distance migrants, flying northeast southwest in autumn, tend to circumvent these mountains. However, longer-distance migrants on route to Africa fly more directly north south, at higher altitude, and mostly cross the Alps (Bruderer, 1999). Both groups fly lower in headwinds, smaller species being more affected than larger ones, and hence being more often deflected by mountains from their most direct route. Migrants captured in high alpine passes often had more fat and longer wings than conspecifics caught in nearby lowlands, implying that the two groups came from different populations, one breeding further north than the other, as supported by ring recoveries (Bruderer & Jenni, 1990). Any tendency of birds to cross the Alps thus seemed to vary with the distances travelled, flight capabilities and physiological state of the migrants, and with local weather at the time. These findings may well apply to other mountain areas at similar latitude. In the New World, however, most of the mountain ranges, particularly the Rockies and the Andes, run approximately north south, so do not need to be crossed or circumvented by most lower-ground migrants travelling north south. In conclusion, altitude is less of a problem for migrating birds than previously thought, even for species normally associated with lowlands. High-altitude flight is facilitated by efficient respiration, oxygen extraction and circulatory systems, and these adaptations are further developed in regular high flyers, such as Bar-headed Geese.

ICE FIELDS Some birds on their migrations also cross substantial stretches of sea ice. For example, many shorebirds that fly between northern Siberia and northern North America on route to wintering areas in South America have to cross 1800 3000 km of the Arctic Ocean which is almost totally ice-covered, even in autumn (Alerstam & Gudmundsson, 1999). The main participants include Pectoral Sandpipers (Calidris melanotos) and Red Phalaropes (Phalaropus fulicarius). Nevertheless, such flights would seem to offer less of a challenge than over-water flights of similar length, because the birds can at least stop and rest in emergencies. Many Arctic and Antarctic seabirds cross more than 100 km of sea ice to reach their breeding areas in spring, including some penguin species which have to walk. A bigger challenge is presented by the Greenland ice cap, which is up to 1000 km across and reaches more than 3 km above sea level at its highest points. It is crossed regularly by shorebirds and waterfowl on their migrations between breeding areas in northeast Canada or west Greenland and their wintering areas in Europe or Africa. Participants include Brent Geese and White-fronted Geese, which have been shown by tracking studies to stop periodically on the way up the ice cap (Gudmundsson et al., 1995; Fox et al., 2003), and to judge from visual observations also Ruddy Turnstones, Red Knots, Common Ringed Plovers, Purple Sandpipers and Northern Wheatears, at least in spring. Many of these birds cross north of 65 N, where the ice cap rises to its greatest height. Most other birds that breed in western Greenland migrate to North America via the Davis Strait rather than to Europe. This flight involves a sea crossing of around 1000 km. Seabirds regularly cross areas of sea ice to reach their nesting areas, but there is also a spring record of a GPStagged Ivory Gull (Pagophila eburnea) crossing the Greenland ice cap north of 70 N, covering 1345 km in 29 hours on route to its nesting place. The track was markedly direct, and although the bird made several stops on the ice, it reached altitudes of more than 3 km over west Greenland and more than 4 km in east Greenland (Frederiksen et al., 2020).

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OTHER REMARKABLE MIGRATIONS Some birds achieve remarkable migrations, not so much because of the terrain to be crossed, but for what they achieve for their size. Hummingbirds provide striking examples. At least one species, the Ruby-throated Hummingbird (Archilocus colubris), weighs only 3 3.5 g, but after nearly doubling body mass, these birds can fly up to 1100 km across the Gulf of Mexico, a journey of 2 days calculated to involve about 3.2 million wingbeats (Nachtigall, 1993). Another species, the 3 4 g Rufous Hummingbird (Selasphorus rufus) migrates overland from Mexico to breed as far north as 60 N in Alaska, further north than any other hummingbird. Its journey of up to 3000 km seems short compared to some of those mentioned above, but in terms of body lengths, it is allegedly the longest migration of any bird (Healy & Calder, 2020).

CONCLUDING REMARKS The various migrations described in this chapter indicate what some birds can achieve on their annual travels. The journeys involved push some birds to the limits of their endurance: long non-stop flights without normal sleep, rest, food or water. Most involve high fuel deposition beforehand, and special adaptations for high-altitude flight, extreme heat or cold, dehydration, low air densities and oxygen levels conditions in which few animals could survive. The fact that some birds can achieve these high endurance feats without prior training or acclimatization is all the more remarkable. Depending on their journeys, birds need fuel and water in different proportions, and on non-stop flights when they can neither feed nor drink, birds can address these different needs physiologically or behaviourally. They may adjust the ratios of stored and metabolized fat, protein and carbohydrate so that body reserves yield different ratios of energy and water. Alternatively, birds might adjust the times of day (day or night), or the altitudes at which they fly, both of which influence rates of heat and water loss. Birds can also reduce their energy needs by selecting times or altitudes with favourable winds (Chapter 4). Birds often use behavioural means to overcome difficulties, involving for example, choice of wind conditions, flight altitudes and flight times, as well as stopover times and durations, and whether to feed or rest during stopovers. Some types of behaviour are appropriate in some conditions but not in others. For example, the metabolism of body fuel for flight releases heat, which helps to maintain body temperature in cold conditions (high latitudes and altitudes), but could lead to overheating (and hence water loss) in warm conditions (low latitudes and altitudes). Hence, to maintain a favourable energy and water balance, a bird must continually adjust its flight times, flight altitudes and other behaviour according to prevailing conditions. In these various ways, a bird can not only survive but can maximize the time and distance it can fly on a given fuel load.

SUMMARY Landbirds migrating over the sea must often make long non-stop flights without rest, food or water. Many birds fly non-stop for periods exceeding 60 hours. Such flights take passerines over distances up to 3000 km, and shorebirds over 4000 6000 km. The longest non-stop flight known from any landbird species involves one population of Bar-tailed Godwits L. l. baueri, which travels for more than 150 hours non-stop in autumn, covering more than 10,000 km over the Pacific Ocean from Alaska to New Zealand. Many other shorebirds make journeys of up to 6000 km over water, and hundreds of other species cross shorter stretches of up to 1500 km, including those that regularly migrate over the Mediterranean or the Gulf of Mexico. The most arduous desert journeys are undertaken by the many species that cross the most barren parts of the Sahara Desert each spring and autumn, where no food or water are taken on route. Some species cross the Mediterranean Sea and Sahara Desert together in a single non-stop flight; others break their journey to refuel in North Africa; while yet others migrate only at night, and stop in the desert during the day, resting or sleeping in shady places, again without feeding or drinking. Soaring species migrate by day and rest at night. Individuals of the same species may show more than one of these strategies. Only small proportions of birds stop at oases, but more migrate down the west and east sides of the Sahara, where conditions are better than in the central sector. Analyses of the body composition of migrants caught or found dead on the ground suggest that some may be limited on their desert crossing by energy needs, and a much smaller number by water needs. While some birds migrate around mountain ranges, others cross even the highest ranges, including the Himalayas. The main problems are the climb to high altitudes (especially for large birds), and the extreme cold, low air densities and oxygen levels found there. In spring, mountains are also often snow-covered, affording little or no opportunity for birds to feed. Flights at more than 7 km above sea level have been recorded from Bar-headed Geese and other species

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that cross the Himalayas. The geese have special adaptations enabling them to extract and utilize efficiently the reduced oxygen levels at high altitudes, but many other birds can readily fly above 6 km, whatever the terrain below them. Extreme migrations often involve extreme adaptations of high fuel deposition, water conservation and respiratory physiology, as well as behavioural adjustments in flight times, flight altitudes, stopover frequency and duration, and resting or feeding behaviour.

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Johnson, O. W., Morton, M. L., Bruner, P. L. & Johnson, P. M. (1989). Fat cyclicity, predicted migratory flight ranges, and features of wintering behaviour in Pacific Golden Plovers. Condor 91: 156 77. Johnson, O. W., Warnock, N., Bishop, M. A., Bennett, A. J., Johnson, P. M. & Kienholz, R. J. (1997). Migration by radio-tagged Pacific Golden Plovers from Hawaii to Alaska, and their subsequent survival. Auk 114: 4521 4. Kanai, Y., Minton, J., Nagendran, M., Ueta, M. Aurysana, B. et al. (2000). Migration of Demoiselle Cranes in Asia based on satellite tracking and fieldwork. Global Environ. Res. 2: 143 53. Klaassen, M. (1995). Water and energy limitations on flight range. Auk 112: 260 2. Klaassen, M. (2004). May dehydration risk govern long-distance migratory behaviour? J. Avian Biol. 35: 4 6. Klaassen, M. & Biebach, H. (2000). Flight altitude of trans-Sahara migrants in autumn: a comparison of radar observations with predictions from meteorological conditions and water and energy balance models. J. Avian Biol. 31: 47 55. Kumar, N., Gupta, U., Jhala, Y. V., Qureshi, Q., Gosler, A. & Sergio, F. (2020). GPS-telemetry unveils the regular high-elevation crossing of the Himalayas by a migratory raptor: implications for definition of a ‘central Asian flyway’. Sci. Rep. 10: 15988. Landys, M. M., Piersma, T., Visser, G. H., Jukema, J. & Wijker, A. (2000). Water balance during real and simulated long-distance migratory flight in the Bar-tailed Godwit. Condor 102: 645 52. Le´andri-Breton, D.-J., Lamarre, J.-F. & Beˆty, J. (2019). Seasonal variation in migration strategies used to cross ecological barriers in a Nearctic migrant wintering in Africa. J. Avian Biol., 50. Available from https://doi.org/10.1111/jav.02101. Liechti, F., Klaassen, M. & Bruderer, B. (2000). Predicting migratory flight altitudes by physiological migration models. Auk 117: 205 14. Liechti, F., Bauer, S., Dhanjal-Adams, K. L., Emmenegger, T., Zehtindijiev, P. & Hahn, S. (2018). Miniaturized multi-sensor loggers provide new insights into year-round flight behaviour of small trans-Saharan avian migrants. Movement Ecol 6: 19. ˚ ., Alerstam, T., Bahlenberg, P., Ekblom, R. Fox, J. W. Lindstro¨m, A et al. (2015). The migration of the Great Snipe Gallinago media: intriguing variations on a grand theme. J. Avian Biol. 47: 321 34. Loonstra, A. H. J., Verhoeven, M. A., Senner, N. R., Both, C. & Piersma, T. (2019). Adverse wind conditions during northward Sahara crossings increase the in-flight mortality of Black-tailed Godwits. Ecol. Lett. 22: 2060 6. Marks, J. S. & Redmond, R. L. (1994). Migration of Bristle-thighed Curlews on Laysan Island: timing, behaviour and estimated flight range. Condor 96: 316 30. McClintock, C. P., Williams, T. C. & Teal, J. M. (1978). Autumnal bird migration observed from ships in the western North Atlantic Ocean. Wilson Bull. 49: 262 77. McNeil, R. & Cadieux, F. (1972). Fat content and flight range capabilities of some adult spring and fall migrant North American shorebirds in relation to migration routes on the Atlantic coast. Can. Field Nat. 99: 589 605. Meyburg, B. U., Bergmanis, U., Langgemach, T., Graszinski, K. Hinz, A. et al. (2017a). Orientation of native versus translocated juvenile Lesser Spotted Eagles (Clanga pomarina) on the first autumn migration. J. Exp. Biol. 220: 2766 76. Meyburg, B.-U., Howey, P., Meyburg, C. & Pretorius, R. (2017b). Yearround satellite tracking of Amur Falcon (Falco amurensis) reveals the

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Chapter 7

Raptors and other soaring birds

Honey Buzzards (Pernis apivorus) thermal-soaring on migration. ‘if they had continued for a fortnight in the same strength as on that day, we could surely have said that they were in greater number than all the men living on the earth. . . . they are seen to pass in this way as thick as ants, and so to continue for many days.’ Pierre Belon, French traveller-naturalist, writing in 1555 of the migration of Black Kites Milvus migrans on the Black Sea coast.

Some landbird species have large wings relative to their body weight, enabling them to obtain lift from rising air currents. They include broad-winged raptors, pelicans, storks and anhingas, and to some extent cranes, herons and beeeaters. Such species depend more on energy-saving soaring gliding flight (as opposed to energy-demanding flapping flight) than do most other birds (Kerlinger, 1989; Hedenstro¨m, 1993). They migrate primarily by day when thermals are best developed, and over much of the world they avoid long water crossings (Chapter 3). They usually travel low enough to be seen with the naked eye, and in certain places, as determined by geography and topography, they form into predictable migration streams. At these places, they can be studied and counted by ground-based observers equipped only with binoculars in ways that other, higher-flying or night-flying birds cannot. The seasonal timing of their migrations can be assessed accurately and their day-to-day passage can be related to regional or local weather and other conditions. The publication of bespoke field guides depicting soaring birds from below has enabled the different species to be identified more accurately than previously and sometimes also the different sex and age groups. Some aspects of soaring bird migration result from the mode of travel itself, but other aspects apply to migration in general. No sharp division separates species that travel by soaring gliding flight from those that travel by continued flapping. Different species form a continuum of variation between the two extremes, depending on their body mass and wing shape, and in all soaring species the ratio of flapping to gliding varies with air conditions at the time. Among raptors, vultures and eagles are mostly dependent on soaring gliding, followed in descending order by Buteo hawks, honey-buzzards, Milvus kites, accipters and then by harriers and ospreys. Falcons are more active fliers, less dependent on updrafts but making use of them when available. This order of listing broadly follows the order of wing-loading, from lowest to highest, and the variation in wing shape from long and broad, with slotted primary feathers, to long, narrow and pointed, with little or no slotting (high aspect ratio). It also reflects the dependence of these various species on The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00005-1 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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updrafts, and hence the extent to which they form into concentrated migration streams and avoid long sea-crossings. Raptors which travel mainly by flapping flight also tend to migrate singly or in small groups, and occasionally fly at night, rather than in the big concentrations seen by day in obligate soaring species. For parts of their migrations, most soaring species travel on a broad front, but for other parts, they form into concentrated streams. Such streams typically occur at places with short sea-crossings or along landscape features that favour soaring gliding flight, such as mountain ridges, narrow valleys and coastal plains, but also on the east or west sides of large water bodies, as birds hug the shoreline rather than cross the water. Well-known observation points for watching soaring migrants include Hawk Mountain in Pennsylvania, Cape May Point in New Jersey, Corpus Christi in Texas, Veracruz on the Gulf coast of Mexico, Panama in Central America, Falsterbo in Sweden, Gibraltar and the Bosphorus at either end of the Mediterranean Sea, Batumi on the Black Sea coast of Georgia, the Northern Valleys and Eilat mountains in Israel, Suez in Egypt, Chumphon in Thailand and Kenting on the southern tip of Taiwan (Figure 7.1). At these sites, as at many others around the world, large numbers of raptors and other soaring species pass in spring or autumn, with total numbers typically varying between tens of thousands and hundreds of thousands, even millions, depending on the site (Tables 7.1 and 7.2). At many such places, several well-spaced watch points need to be manned simultaneously to gain a realistic idea of the number of birds passing. At sites in Israel, the volume of the migration as assessed each day by ground observers was found to be correlated with the volume of migration measured on the same days by radar (in autumn, r2 5 0.66, P , .001). So at least at these sites, the ground observers were obtaining a reasonable measure of the changes in migration from day to day (Leshem & Yom-Tov, 1996a). Networks of such sites also have been used to monitor trends in continental populations as they pass through migration (Farmer et al., 2010).

MAJOR ROUTES Because they depend on topography, soaring birds generally take the same routes each year, but many take somewhat different routes in autumn and spring, depending on wind and other conditions. Thus the passage at Hawk Mountain in Pennsylvania is marked in autumn but barely noticeable in spring (18,000 vs 1000 birds), while at Eilat in Israel, the passage is much bigger in spring than in autumn (1.2 million vs 26,000 birds). At many watch sites, daily counts have been made through the migration seasons over several to many years, and observers at many well-watched sites publish their data online, updated each year as fresh counts become available.

FIGURE 7.1 Major flyways used by soaring birds. 1. Trans-American Flyway; 2. Western European West African Flyway; 3. Eurasian East African Flyway; 4. East Asian Continental Flyway; 5. East Asian Oceanic Flyway. Note that no major flyways for northern hemisphere raptors extend into New Guinea and Australia. Watch sites mentioned in the text: B, Bosphorus; BM, Bab el Mandeb; BP, Belen Pass; E, Eilat; F, Falsterbo; G, Gibraltar; H, Hawk Mountain; K, Kenting; M, Messina Strait; P, Panama; S, Suez; T, Corpus Cristi; Texas; V, Veracruz, Mexico. Modified from Zalles & Bildstein (2000).

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TABLE 7.1 Examples of annual counts of raptors and other soaring birds at two major migration watch-sites, Veracruz on the east coast of Mexico (autumn) and Eilat at the top of the Red Sea in Israel (spring). Veracruz, Texas (August November 2002): Turkey Vulture (Cathartes aura) 2,677,355; Golden Eagle (Aquila chrysaetos) 3; Mississippi Kite (Ictinia mississippiensis) 306,274; Swallow-tailed Kite (Elanoides forficatus) 272, Black-shouldered Kite (Elanus axillaris) 2; Snail Kite (Rostrhamus sociabilis) 5; Hook-billed Kite (Chondrohierax uncinatus) 165; Plumbeous Kite (Ictinia plumbea) 2; Northern Harrier (Circus cyaneus) 269; Sharp-shinned Hawk (Accipiter striatus) 3152, Cooper’s Hawk (Accipiter cooperii) 2030; Northern Goshawk (Accipiter gentilis) 1; Red-shouldered Hawk (Buteo lineatus) 7: Broad-winged Hawk (Buteo platypterus) 2,386,232, Grey Hawk (Asturina nitida) 326; Red-tailed Hawk (Buteo jamaicensis) 146; Swainson’s Hawk (Buteo swainsoni) 1,009,648: Ferruginous Hawk (Buteo regalis) 2; Common Black Hawk (Buteogallus anthracinus) 7; Harris’s Hawk (Parabutoe unicinctus) 4; Zone-tailed Hawk (Buteo albonatus) 142; Short-tailed Hawk (Buteo brachyurus) 3; Osprey (Pandion haliaetus) 2694; Crested Caracara (Caracara plancus) 2; American Kestrel (Falco sparverius) 4097; Merlin (Falco columbarius) 117; Peregrine Falcon (Falco peregrinus) 714; Roadside Hawk (Buteo magnirostris) 1; Unidentified raptor 177,347. Total raptors 6,571,019. From HMANA website at http://www.hawkcount.org. Eilat, Israel (February16 May 23 1985): European Honey Buzzard (Pernis apivorus) 851,598; Black Kite (Milvus migrans) 28,320; Egyptian Vulture (Nephron percnopterus) 541, Griffon Vulture (Gyps fulvus) 17; Short-toed Snake Eagle (Circaetus gallicus) 345; Western Marsh Harrier (Circus aeruginosus) 242; Pallid Harrier (Circus macrourus) 41; Montagu’s Harrier (Circus pygargus) 17; unidentified (Circus) 37; Northern Goshawk (Accipiter gentilis) 3; Eurasian Sparrowhawk (Accipiter nisus) 138; Levant Sparrowhawk (Accipiter brevipes) 905a; unidentified (Accipiter) 143; Common (Steppe) Buzzard (Buteo b. vulpinus) 225,460; Long-legged Buzzard (Buteo rufinus) 105; unidentified (Buteo/Pernis) 6460; Lesser Spotted Eagle (Clanga pomarina) 74; Spotted Eagle (Clanga clanga) 5; Steppe Eagle (Aquila nipalensis) 75, 053; Imperial Eagle (Aquila heliaca) 61; Unidentified (Aquila) 1111; Booted Eagle (Hieraaetus pennatus) 140; Bonelli’s Eagle (Hieraetus faciatus) 6; Osprey (Pandion haliaetus) 49; Lesser Kestrel (Falco naumanni) 13; European Kestrel (Falco tinnunculus) 37; Eurasian Hobby (Falco subbuteo) 20; Eleonora’s Falcon (Falco eleonorae) 16: Lanner Falcon Falco biarmicus 7; Peregrine (Falco peregrinus) 4; unidentified falcon species 46. Unidentified raptors 2138. Total raptors 1,193,229. a

The total for Levant Sparrowhawk was exceptionally low in 1985, and in 1987 the total for this species was 49,836.

From Shirihai & Christie, 1992.

TABLE 7.2 Some sample counts of raptors at selected watch sites. North and Central America Hawk Mountain (A, 2011), total 22,904, 20 species, including 13,323 Broad-winged Hawk, 4447 Sharp-shinned Hawk, 1697 Red-tailed Hawk (Hawk Mountain website) Cape May, A, average from 1976 2020, total 46,894, 19 species, including 23,012 Sharp-shinned Hawk, 7862 American Kestrel, 2735 Osprey, 1827 Broad-winged Hawk, 1782 Red-tailed Hawk (HawkCount website). Golden Gate, California (A, average from 2003 14), total 26,209, 19 species, including Red-tailed Hawk 8947, Turkey Vulture 8434, Sharp-shinned Hawk 3945, Cooper’s Hawk 2435 (Wikipedia website for Golden Gate Raptor Observatory). Keys, Florida (A, average from 1995 2005), total 13,981, 13 species, including 3737 Broad-winged Hawk, 2971 Sharp-shinned Hawk, 2596 American Kestrel, 1826 Peregrine, 1154 Osprey (Smith et al., 2008). Smith Point, Texas (A, average from 1995 2005), total 51,275, 16 species, including 38,643 Broad-winged Hawk, 4320 Mississippi Kite, 2913 Sharpshinned Hawk, 1529 Turkey Vulture, 1334 American Kestrel (Smith et al., 2008). Corpus Christi, Texas (A, average from 1995 2005), total 639,551, 17 species, including 549,785 Broad-winged Hawk, 40,229 Turkey Vulture, 13,007 Mississippi Kite (Smith et al., 2008). Veracruz, Mexico (A, average from 1995 2005), total 5,260,871, 17 species, including 1,988,826 Turkey Vulture, 155,651 Mississippi Kite, 1,919,949 Broad-winged Hawk, 915,104 Swainson’s Hawk (Smith et al., 2008). Tehuantepec Isthmus, Mexico (A, maximum from 2007 14), total .2 million, numerous species, including 2,103,992 Turkey Vulture, 905,579 Swainson’s Hawk, 34,683 Broad-winged Hawk (Cabrera-Cruz et al., 2017). Talamanca, Costa Rica (A, 2001), total 3 million, 17 species, including 1,367,200 Turkey Vulture, 1,018,666 Broad-winged Hawk, 374,188 Swainson’s Hawk, 207,915 Mississippi Kite (Porras-Pen˜aranda et al., 2004). Talamanca, Costa Rica (S, 2010), total 613,849, 16 species, including 385,699 Turkey Vulture, 116,544 Broad-winged Hawk, 55,496 Swainson’s Hawk, 40,535 Mississippi Kite (Tejeda-Tellez, 2014). Panama, from coast to coast (A, 2004), total .3,125,486 million, 13 species, including 1,111,878 Turkey Vulture, 934,323 Broad-winged Hawk, 724,578 Swainson’s Hawk, 2510 Mississippi Kite, 801 Peregrine (Batista et al., 2005). Europe Falsterbo, A, 2020, total 58,344, 22 species, including 32,114 Eurasian Sparrowhawk, 14,316 Common Buzzard, 4654 Red Kite, 3898 European Honey Buzzard, 1362 Common Kestrel, 1003 Western Marsh Harrier (Falsterbo website). Gibraltar Strait, A, mean counts for 2009 12, total 354,000, 28 species, including 225,000 Black Kite, 59,000 European Honey Buzzard, 33,800 Booted Eagle, 20,000 Short-toed Eagle, 8800 Griffon Vulture (Fundacio´n Migres website). Bosphorus, Turkey, A, 2008, incomplete count (September 22 October 10 only), total 141,844, 25 species, including 74,055 Common (Steppe) Buzzard, ˝ ¨ p et al., 2014). 58,327 Lesser Spotted Eagle, 4242 Short-toed Eagle (Fulo

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TABLE 7.2 (Continued) Messina, Sicily, S, 2011, total 43,000, 40 species, 35,736 European Honey Buzzard, 3414 Western Marsh Harrier, . 1000 Black Kite, 1000 Kestrel, 866 Montagu’s Harrier (Harris, 2013). Bourgas Bay (via Pontica), Bulgaria, A, 1990, the year with the highest annual count during 1979 2003, total 65,605, 34 species, including 31,746 Common (Steppe) Buzzard, 25,786 Lesser Spotted Eagle, 3519 European Honey Buzzard (Michev et al., 2011). Batumi, Georgia (maximum count during A), 2008 19, .1.5 million, 37 species, including 666,364 European Honey Buzzard, 541,226 Common (Steppe) Buzzard, 240,743 Black Kite, 10,808 Montagu’s Harrier, 9509, Lesser Spotted Eagle (Hoekstra et al., 2020). Middle East Northern Valleys, Israel (A, 1997, mean from 1990 99), total 691,761, 30 species, including 322,727 European Honey Buzzard, 68,744 Lesser Spotted Eagle, 45,353 Levant Sparrowhawk, 3224 Short-toed Eagle, 3231 Red-footed Falcon (Shirihai et al., 2000). Eilat, Israel (S, mean of 8 years during 1977 97), total 1.2 million, .40 species, including 466,000 Common (Steppe) Buzzard, 852,000 Honey Buzzard, 36,690 Black Kite, 50,000 Levant Sparrowhawk (Shirihai et al., 2000). Bab el Mandeb, Yemen (1987A), total 246,478, 23 species, including 98,339 Common (Steppe) Buzzards, 76,586 Steppe Eagles, 1202 Short-toed Eagles (Welch & Welch, 1988). Suez, Egypt (S, 1982), total 132,242, 22 species, including 80,887 Common (Steppe) Buzzard, 15,778 Steppe Eagle, 10,000 Lesser Spotted Eagle (Wimpfheimer et al., 1983). Eastern Asia Chumphon, Thailand (A, 2016), total 791,229, 22 species, including 136,683 Crested Honey Buzzard, 177,169 Black Baza, 410,721 Chinese Sparrowhawk, 28,254 Japanese Sparrowhawk, 20,773 Grey-faced Buzzard (Limparungpatthanakij et al., 2019). Kenting, Taiwan (A, 2015), total 94,324, 12 species, including 34,535 Grey-faced Buzzard, 59,290 Chinese Sparrowhawk, 8263 Crested Honey Buzzard, 110 Japanese Sparrowhawk (L. Severinghaus, pers. comm). Kenting, Taiwan (S, 2015), total 40,035, 9 species, including 17,141 Grey-faced Buzzard, 22,625 Chinese Sparrowhawk (L. Severinghaus, pers. comm.) Sangihi, (A, 2008), total 230,000, including 225 Chinese Sparrowhawk, and small numbers of Osprey, harrier species, Japanese Sparrowhawk, Grey-faced Buzzard and Peregrine Falcon (Germi et al., 2009). A

autumn, S

spring. At each site, species listed in order of abundance, see text for scientific names.

Worldwide, migration corridors coalesce into major flyways, at least two of which extend to the southern parts of the southern continents, as described below (Figure 7.1; Zalles & Bildstein, 2000). All tend to converge on narrow land bridges or on short sea-crossings, where the migration streams may be less than a few tens of kilometres across.

The trans-American flyway Each autumn, more than six million raptors travel along one or other part of this 10,000 km overland system of corridors that stretches from boreal Canada to central Argentina (Figure 7.1). At least 32 species migrate along the flyway’s central land corridor that connects North and South America, reaching its narrowest point at Panama. This part of the route carries almost the entire world population of Broad-winged Hawks (Buteo platypterus) (up to 1.8 million), Swainson’s Hawks (Buteo swainsoni) (1.5 million) and Mississippi Kites (Ictinia mississipiensis) (700,000), and also big numbers of Turkey Vultures (Cathartes aura) (2.7 million) and many others (Tables 7.1 and 7.2). The largest numbers of birds (with maximum recorded totals) are seen near Corpus Christi, Texas (more than a million birds in autumn), Veracruz (Mexico, more than six million birds in autumn) and Panama City (more than three million birds in autumn). In South America, routes are not well studied, but satellite tracks suggest that, while Swainson’s Hawks continue on an almost direct southerly route (Kochert et al., 2011), Turkey Vultures head east-south-east towards the eastern grasslands (Dodge et al., 2014). Non-raptors using the central part of the route include American White Pelicans (Pelecanus erythrorhynchos), Wood Storks (Mycteria americana) and Anhingas (A. anhinga), along with many species of non-soaring birds. Although most raptors from North America take the land-route via Central America to reach South America, many Ospreys (Pandion haliaetus), Peregrine Falcons (Falco peregrinus) and others leave North America via the Florida peninsula and then Cuba and on to South America.

The Western European West African flyway Each autumn, at least 354,000 raptors and 160,000 storks travel along one or other part of the 5000 km overland system of corridors that stretches from northern Europe to West Africa, via the short (14 km) sea-crossing at the Strait of

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Gibraltar (Figure 7.1). At least 28 species use this flyway, which for most of its length is dominated by Black Kites (Milvus migrans) (225,000) and European Honey Buzzards (Pernis apivorus) (59,000), along with the 160,000 storks (counts by Fundacio´n Migres). The biggest concentrations of birds are seen in both autumn and spring at the Gibraltar Strait (Table 7.2), where counts have been made mainly on the Rock of Gibraltar or around Tarifa in southern Spain.

The Eurasian East African flyway More than 1.5 million raptors travel along this 10,000 km system of largely overland corridors that extends from northeastern Europe and western Siberia through the Middle East into southern Africa (Figure 7.1, Table 7.1). At least 35 species use this flyway which for much of its course follows the Great Rift Valley, and which includes several narrow water crossings. Two main known routes converge on Africa. In the western route, birds pass in autumn, east or west of the Black Sea, over the Bosphorus or Dardanelles and on to cross Jordan and Israel, and then Sinai, entering Africa at the northern end of the Red Sea at Suez (Figure 7.2). In the eastern Caspian Arabia route, birds pass either side of the Caspian Sea, move on south through Arabia and cross into Africa via the Bab el Mandeb Strait at the southern end of the Red Sea. Four raptor species make up the bulk of the flight through the Middle East, namely the European Honey Buzzard (P. apivorus) (up to 852,000), Common (Steppe) Buzzard (Buteo buteo vulpinus) (466,000), Lesser Spotted Eagle (Clanga pomarina) (142,000) and Steppe Eagle (Aquila nipalensis) (75,000), along with White Storks (Ciconia ciconia) (530,000), Black Storks (Ciconia nigra) (17,000) and Great White Pelicans (Pelecanus onocrotalus) (70,000). Major concentrations of birds are seen at several sites in Israel, and at the various water crossings mentioned above, and on the east and west sides of the Black Sea. At most sites, numbers differ greatly between autumn and spring. FIGURE 7.2 Main migration routes for soaring birds through the Middle East, autumn and spring (left), and through Israel alone (right). 1. The western route over the western slopes of Israel’s central mountain spine. 2. The eastern route mainly along the Jordan (Rift) Valley, continuing south during most of the day but crossing to join the western route during part of the day. 3. The Eilat mountain route crosses southern Israel in the region of the Eilat Mountains, running northeast southwest through Jordan and Sinai (from Leshem & Bahat, 1999). The birds using these routes cross to and from Africa via the Gulf of Suez, mostly at its northern or southern ends. Further east, another flyway runs across the Arabian Peninsula, crossing to Africa at the narrow Bab el Mandeb Straits at the southern end of the Red Sea (the so-called Caspian Arabian route). By these various routes, the birds use the shortest water crossings and avoid the wider parts of the Red Sea. The actual positions of the migration streams shift east or west to some extent during the course of each day, from one day to the next, and from the early to the later part of each season, as wind and other conditions change. In autumn, birds enter northern Israel on a single narrow route, with 87% of all soaring birds encountered within a 20 km wide strip, some 11 31 km from the Mediterranean coast. Radar images show long lines of soaring migrants progressing south-southwest parallel to the coast, moving inland with the sea breeze during the course of the day (Leshem & Yom-Tov, 1998).

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The East Asian Continental flyway More than a million raptors travel along one or other part of this 9000 km mostly overland system of corridors that stretches from eastern Siberia to southeast Asia and the Indonesian archipelago, and which includes sea-crossings of 10 60 km at the Straits of Malacca, Sunda, Bali and Lombok (Figure 7.1). Strangely, no migratory raptor species is known to reach Australia in numbers, the flyway being curtailed further north than those in Africa and South America (Chapter 28). At least 33 raptor species migrate along portions of this flyway through eastern Asia, with the bulk of the flight dominated by Crested (Oriental) Honey Buzzards (Pernis ptilorhynchus), Grey-faced Buzzards (Butastur indicus), Chinese Sparrowhawks (Accipiter soloensis) and Japanese Sparrowhawks (Accipiter gularis). In addition, Common (Japanese) Buzzards (Buteo b. japonicus) use the northern half of the flyway, and Black Bazas (Aviceda leuphotes) the southern half. Major concentrations of birds are seen in autumn at Chumphon in Thailand ( . 791,000), at Taiping ( . 64,000) and the Selangor Plain ( . 121,000) in Peninsular Malaysia, and at the Straits of Malacca, including Singapore, suggesting that most of them winter on Indonesian Islands (DeCandido et al., 2004). More than 90,000 individuals of several species have been counted crossing from Bali to Lombok, presumably wintering on the islands to the east (Germi & Waluyo, 2006).

The East Asian Oceanic flyway More than 250,000 raptors travel along this 7000 km largely over-water flyway that stretches from coastal eastern Siberia and Kamchatka to Japan, the Philippines and into eastern Indonesia (Figure 7.1, Table 7.2). At least 26 species migrate along the main part of this flyway, which extends from southern Japan through the Ryukyu Islands and Taiwan to the Philippines and Indonesia. The bulk of the flight is dominated by Grey-faced Buzzards (20,000 at Kenting on the southern tip of Taiwan) and by Chinese Sparrowhawks (up to 201,000), the latter seen in flocks of up to thousands of individuals. Sea-crossings up to 680 km, as recorded in Crested Honey Buzzards (Pernis ptilorhychus) (Nourani et al., 2016), may restrict the variety of species that use this flyway, but some of the over-water crossings fall within the tropical trade-wind zone, so some raptors can take advantage of the weak over-water thermals that develop there. Many of them fly south by island hopping, benefitting from following winds, but travel northward in spring along the mainland route, when the oversea winds would act against them.

Some general points Some species use only certain parts of the major flyways, while other species use other parts, depending on the locations of their breeding and wintering areas. Along each flyway, however, the numbers of birds seen in autumn tend to increase southwards towards the tropics, as more and more individuals join the migration, outnumbering those that stop. Numbers reach a peak in the northern tropics and, as the streams continue southwards, numbers then gradually decline, as birds progressively leave the major flyways to settle in their wintering areas. Nevertheless, substantial numbers of birds continue to the southern parts of all the major flyways. In spring, the reverse geographical trend in numbers occurs as the birds return northwards. Observation sites in temperate latitudes tend to produce seasonal counts up to tens of thousands of individuals, whereas those at lower latitudes can produce hundreds of thousands or millions, with the record coming from Veracruz in eastern Mexico (about 22 N) where more than 6.6 million raptors and other soaring birds were counted in autumn 2001 (website http:// www.hawkcount.org; for earlier counts, see Ruelas Inunza et al., 2000). Other major flyways may remain to be discovered. In particular, only minor routes have yet been described around or through the Himalayas, yet India forms an important wintering area for raptors and other soaring birds. Similarly, Lake Baikal in Siberia is the largest body of freshwater in the world, yet to my knowledge only minor concentration points (,10,000 birds) on its edges have been described. Moreover, little is known of the routes taken by raptors through South America or Africa, although the satellite-tracking of individuals suggests a continuation of narrow corridor routes in some species (see Fuller et al., 1998 for Swainson’s Hawks in South America (see Figure 9.6, Box 9.3); also Meyburg et al., 1995a,b for Lesser Spotted Eagles, Berthold et al., 2002, 2004 for White Storks in Africa). In addition to the major flyways, many minor ones can be discerned, such as the Strait of Messina between Italy and Sicily which is crossed by thousands of raptors in autumn and spring on the route between Europe and North Africa (Corso, 2001; Panuccio et al., 2021). After leaving Sicily, these birds face at least 150 km of open sea before reaching the nearest part of Africa (Tunisia). The numbers of birds counted at established watch sites vary greatly from day to day in the migration seasons and from year to year. Even in common species, counts may vary by more than twofold from one year to the next. Much of this variation may be due to variations in observer effort and weather, which influence the volume, altitude and exact

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route of migration on particular days. Lateral displacement of the migration stream by only a few kilometres can mean that most birds are missed by observers based at a fixed site. Compared with such effects, actual year-to-year variation in population sizes is probably small, but such counts have nevertheless proved useful in revealing long-term trends in populations. As the birds are usually drawn from a wide area, any long-term trends they show are likely to be widespread, over-riding purely local changes. The counts from Hawk Mountain in Pennsylvania and Cape May in New Jersey, and Falsterbo in Sweden, all of which span several decades, have been used to assess long-term population trends (Kjelle´n & Roos, 2000; Farmer et al., 2007), as have the shorter runs of counts from other sites elsewhere (for Israel, see Shirihai et al., 2000; for North America, see Hoffman & Smith, 2003; Bildstein et al., 2008; Smith et al., 2008). The numbers of raptors counted at many concentration sites in the past 70 years were probably much smaller than the numbers present several hundred years ago, especially in Europe, before their populations were so greatly reduced by human activities. Because of their different flight modes and wing shapes, falcons form a minority of birds seen at concentration points, as they travel more on a broad front, crossing water bodies as they come to them, and flying at night if need be. The same applies to a smaller extent to Ospreys and harriers. By migrating day and night, some raptors have travelled remarkable non-stop distances, with tracked Peregrines covering up to 1072 km within a 24 hour period in autumn and up to 1205 km in spring as they travelled across the Eurasian landmass (Sokolov et al., 2018). Tracked Amur Falcons (Falco amurensis) flew non-stop for 2500 3100 km in a 53 65 hour period from Somalia across the Arabian Sea to India, and one individual flew from East Africa over the sea and then India, not stopping until it reached Burma, on a 5-day flight of 5912 km (Meyburg et al., 2017b). This small falcon migrates for a total of 14,500 km between its breeding and wintering areas, which is one of the longest migrations recorded from raptors.

Loop migrations The various ‘loop migrations’ of raptors which take mainly different routes on their outward and return journeys are known from counts on different flyways, from ring recoveries and from the satellite-tracking of tagged birds. They may be shaped by wind conditions, and the need to minimize the risk of serious off-course drift or over-water mortality, or by seasonal differences in the distribution of food-supplies. At least two loop migrations are known through northern Africa, shown by various species of raptors and other birds. In one clockwise loop, many raptors take more westerly course across the Sahara in spring than in autumn, as found by tracking studies on many species, including Eurasian Hobby (Meyburg et al., 2011), Montagu’s Harrier (Circus pygargus) (Limin˜ana et al., 2012b), Western Marsh Harrier (Circus aeruginosus) (Klaassen et al., 2010; Vansteelant et al., 2020), Lesser Kestrel (Falco naumanni) (Limin˜ana et al., 2012a), Booted Eagle (Hieraeatus pennatus) (Mellone et al., 2013) and Egyptian Vulture (Neophron percnopterus) (Lo´pez-Lo´pez et al., 2014). This loop has been attributed to the westerly drift of migrants in spring, resulting from the prevailing easterly winds across the Sahara. The other involves a clockwise loop around the Red Sea, as some raptors travel southward through Arabia, passing down the east side of the Red Sea and crossing to Africa at Bab el Mandeb, and northward up the west side of the Red Sea to cross from Africa at the Gulf of Suez (for Steppe Eagle, see Meyburg et al., 2003). This route has again been attributed to easterly winds which make crossing at Bab el Mandeb easy in autumn but risky in spring, accounting for the much higher counts at Bab el Mandeb in autumn and at Suez and Eilat in spring. The majority of Black Kites, Common (Steppe) Buzzards and Steppe Eagles follow this loop. One of the most striking loop migrations, evident over almost the entire route from eastern Europe and western Asia to southern Africa, is shown by the Red-footed Falcon (Falco vespertinus), in which both wind conditions and food supplies may play a role (Figure 7.3; Katzner et al., 2021). The westerly spring route accounts for the frequent appearance of this species in Western Europe at this time of year, outside the breeding range. Similarly, in North America, many Peregrines migrate southward down the east coast, crossing the Caribbean Islands to South America. But on their return in spring, most Peregrines travel north through the centre of the continent, again like many other species (Figure 9.5; Fuller et al., 1998). In eastern Asia, many types of raptors make long sea-crossings on their southward journeys, benefiting from overwater tailwinds, but migrate more to the west on their return when they follow a landward route up the east side of the continent. In this way, they avoid overwater headwinds and make an overall clockwise route, as first described in Crested Honey Buzzards (Higuchi et al., 2005; Nourani et al., 2016).

USE OF THERMALS AND OTHER UPDRAFTS Birds that travel overland by soaring gliding flight mostly gain lift from rising air (Chapter 3). On many days, updrafts are formed when the wind striking a slope or cliff is deflected upwards (orographic lift). Long mountain ridges thus

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FIGURE 7.3 An extreme example of loop migration: schematic representation of the routes followed during autumn (solid lines) and spring (dashed lines) by Red-footed Falcons (Falco vespertinus). On northbound migration, the birds spend 2 6 weeks refuelling in West Africa, before crossing the Sahara and Mediterranean. Modified from Katzner et al. (2021).

provide excellent flyways for soaring migrants in those (relatively rare) places where the ridge lies roughly northsouth, in a direction appropriate for migration. One such site is the Kittatinny Ridge in eastern North America, which provides a long unbroken source of lift on which hawks can glide with hardly a flap for up to 300 km, beginning in New York State and continuing past Hawk Mountain in Pennsylvania (Kerlinger, 1989). The ridge deflects the prevailing west north autumn winds upwards, at rates often exceeding 3 4 m/s, and sometimes to heights exceeding 300 400 m above ground. The hawks are mostly moving northwest southeast when they encounter the ridge running at right angles to their path. For a time, they ride the up-currents generated by the ridge, even though this activity takes them off their main direction. It gets them to lower latitudes, but eventually they must leave the ridge to continue their journey towards the southeast. Other long ridges used by migrating raptors occur in the Rockies of western North America, the Andes in South America, and in various mountains in the Middle East, including the Rift Valley which extends southwards into Africa. Mountain ranges that run mainly east west, including the Himalayas, offer through routes for migrating soaring birds which, in crossing ridges, generally concentrate over the lowest passes. At least 45 raptor species have been seen migrating through the Himalayas, using several routes running roughly north south, but few species occur in large numbers (Juhant & Bildstein, 2017). Total numbers reach hundreds of thousands and, in addition to Black Kites, Steppe Eagles and other soaring species, they include Peregrines and other falcons (De Roder, 1989; Dixon et al., 2017). Given the winds typical of mountain areas, birds making use of orographic lift can migrate later in the year, on more days and for longer each day than those in flatter terrain dependent on warm-weather thermals. In general, individual birds switch from one form of lift to another, according to the terrain below them, but by using orographic lift, they can travel in conditions when no thermals could develop. In a study of Golden Eagles (Aquila chrysaetos) on spring migration, ridge soaring occurred more frequently in mornings and evenings, earlier in the migration season, and when crosswinds and tailwinds were greatest (Katzner et al., 2015). While soaring birds depend largely on the terrain below them, different species may choose routes offering the most thermal lift or most orographic lift, depending on the type to which they are best adapted (for comparison between Golden Eagle and Turkey Vulture, see Bohrer et al., 2012). With knowledge of the needs of migrant raptors, topographic maps can be examined for likely looking sites, parts of the world still being unexplored in this respect. Thermals are localized columns of rising air created mainly through the uneven heating of the ground by the sun (Chapter 3). These columns rise hundreds of metres, until they have cooled to the temperature of the surrounding air, where they often produce a cumulus cloud, marking their position. They usually begin in the morning once the ground has heated sufficiently but gather strength during the day. They ascend gradually faster and higher, often reaching more than 1000 m at noon, and then wane in the evening as the ground cools. They typically rise at 1 4 m/s (Kerlinger, 1989).

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FIGURE 7.4 The relationships between wing load and average height band in thermals for four species of soaring migrants. Average climbing time in thermals (not shown) increased with increase in body weight. From Leshem & Yom-Tov (1996b).

Birds progress on migration by circling in one thermal to gain height, and then gliding with loss of height to the next thermal where they rise again, repeating the process along the route (see Figure 3.5). This enables birds to travel across the country at around 30 50 km/h, depending on the rate and extent of rise within thermals and the distance covered between thermals (in turn dependent on the ‘glide coefficient’, which is the ratio between the horizontal distance covered by the bird and its altitude loss over that distance). Small species with light wing-loading ascend more rapidly so spend less time in each thermal, but in travelling between thermals they glide less rapidly than large species and so lose more height per unit distance. They can therefore glide less far before having to climb again (Chapter 3; Figure 7.4, Table 7.3). Nevertheless, small species can get underway earlier in the morning and continue later into the evening than large species with heavier wing loading that are restricted to a shorter period each day when thermals are strongest. The flight times of the smaller species migrating through Israel typically extend over 8 10 hours each day (beginning around 9 a.m.) and the larger ones over 6 7 hours (beginning around 10 a.m.). However, all species tend to make more rapid progress in the middle part of the day, when climbs are fastest and highest, and glides are longest (Figure 7.5). Particular species can travel across the country twice as fast around noon than in the morning or evening. When a bird glides, it may partly fold its wings which reduces drag and thereby increases speed; but the reduced wing and tail area also provides less lift, so the bird sinks more rapidly. On occasions, birds may make ‘powered glides’ in which they flap sporadically during inter-thermal gliding. This has the effect of increasing flight speed and enabling birds to attain greater daily distances on migration than by normal soaring gliding flight, but at a greater energy cost. In Steppe Eagles studied by observation and radar in Israel, cross-country speed was related to the climb rate in thermal circling (Spaar, 1997). Over the whole diurnal cycle, the mean climb rate in thermals was 1.9 m/s, but rates up to 5.0 m/s were reached around noon. Mean gliding air speed between thermals was 56 km/h which, allowing for climb times, gave a mean cross-country speed of 45 km/h. The upper limit of migration was about 1600 m above ground but was mostly below 1000 m (Spaar & Bruderer, 1996). Smaller European Honey Buzzards and Common (Steppe) Buzzards achieved lower cross-country speeds, at 37 and 35 km/h. However, in a 12-hour day, Steppe Eagles soared for only 6 hours and covered 270 km, whereas the two smaller species migrated for 10 hours and covered 360 km. Hence, although larger birds can travel faster and further between thermals, they do not necessarily cover more distance per day (Spaar & Bruderer, 1996). On one favourable occasion, White Storks over Israel were able to climb to 1550 m and then glide for 36 km before needing to climb again. Their average flight speed was 57 km/h, about 47% faster than average. Comparisons between the various species of soaring raptors in Israel revealed that (1) the average climbing rate in thermal circling was independent of body size, at 1.5 2.1 m/s, although smaller species had a smaller turning radius, so in theory could benefit more from the faster currents in the centre of the thermal column; (2) during inter-thermal gliding, air speed was positively related to body mass, and gliding angle negatively related to body mass heavier species glided faster, and at shallower angles, losing less height per unit distance; (3) overall cross-country speed relative to the air was positively related to the species body mass, the larger species travelling faster but for fewer hours each day (Figure 7.6, Table 7.3; Spaar, 1997). The better gliding performance of larger raptors fits theoretical predictions about gliding flight (Chapter 3). The same principles apply to sailplanes, and to increase gliding speed, pilots often add water as ballast. The faster a bird glides, the more lift it gains from the airflow below its wings, over and above any obtained from rising air currents. In even hotter conditions, much greater climbs can be achieved by soaring birds. As recorded from a GSM GPS transmitter, on March 21, 2014 an adult male Lesser Spotted Eagle started migration in Ethiopia three hours after sunrise (Meyburg, 2021). Within 12 minutes the eagle reached 2359 m in altitude (climbing speed 3.3 m/s). Between 12.37 and 15.00 hour, the eagle flew five times at altitudes greater than 4000 m, in one case 4220 m above sea level or

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TABLE 7.3 Timing of passage of migrants through Israel, spring and autumn. Only species with the largest totals at each season are shown. Species

Autumn migration

Spring migration

Mid-point between spring and autumn dates

Mean date

90% pass between (days)

Total duration (days)

Mean date

90% pass between (days)

Total duration (days)

Honey Buzzard (Pernis apivorus)

7 Sep

30 Aug 14 Sep (16)

60

5 May

2 12 May (11)

36

6 July

Levant Sparrowhawk (Accipiter brevipes)

20 Sep

14 26 Sep (13)

47

24 Apr

18 26 Apr (9)

71

7 July

Lesser Spotted Eagle (Clanga pomarina)

29 Sep

21 Sep 5 Oct (15)

57 10 Mar

23 Feb 27 Mar (33)

73

Steppe Eagle (Aquila nipalensis)

13 Oct 1 Nov (19)

Honey Buzzard (Pernis apivorus)

7 Sep

30 Aug 14 Sep (16)

60

5 May

2 12 May (11)

36

6 July

Levant Sparrowhawk (Accipiter brevipes)

20 Sep

14 26 Sep (13)

47

24 Apr

18 26 Apr (9)

71

7 July

Lesser Spotted Eagle (Clanga pomarina)

29 Sep

21 Sep 5 Oct (15)

57 10 Mar

23 Feb 27 Mar (33)

73

Steppe Eagle (Aquila nipalensis)

13 Oct 1 Nov (19)

Short-toed Snake Eagle (Circaetus gallicus)

23 Sep

15 Sep 9 Oct (25)

52

Egyptian Vulture (Neophron percnopterus)

19 Sep

6 29 Sep (24)

50

1 Apr

8 Mar 3 May (57)

101

25 June

Western Marsh Harrier (Circus aeruginosus)

23 Sep

7 Sep 6 Oct (30)

57

11 Apr

10 Mar 10 May (62)

100

2 July

Booted Eagle (Hieraaetus pennatus)

22 Sep

8 Sep 1 Oct (24)

56

10 Apr

25 Mar 2 May (39)

87

2 July

Black Kite (Milvus migrans)

14 Sep

31 Aug 4 Oct (35)

53

30 Mar

21 Mar 10 Apr (21)

91

21 Jun

Red-footed Falcon (Falco vespertinus)

2 Oct

25 Sep 13 Oct (19)

49 3 Apr

22 Mar 15 Apr (25)

91

2 Apr

14 Mar 25 Apr (43)

82

Common (Steppe) Buzzard (Buteo buteo vulpinus) White Stork (Ciconia ciconia)

29 Aug

16 Aug 12 Sep (28)

92

Great White Pelican (Pelecanus onocrotalus)

14 Oct

18 Sep 7 Nov (51)

126

From Leshem & Yom-Tov (1996a).

14 Jun

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FIGURE 7.5 Route and altitude in relation to ground level for a flock of Great White Pelicans (Pelecanus onocrotalus) followed by glider through Israel on October 12, 1987. Each dot represents a point where the first birds started to climb or descend in a thermal. Time of day and average velocity are given along the bottom, and the route from take-off to landing that day is shown in the map on the right. From Leshem & Yom-Tov (1996b).

FIGURE 7.6 Gliding speed (left) and cross-country speed (right) relative to the air in soaring gliding flight in raptors of different body mass. BE, Booted Eagle (Hieraaetus pennatus); BK, Black Kite (Milvus migrans); EV, Egyptian Vulture (Neophron percnopterus); GV, Griffon Vulture; HB, European Honey-buzzard (Pernis apivorus); LS, Levant Sparrowhawk (Accipiter brevipes); LSE, Lesser Spotted Eagle (Aquila pomarina); MPH, Montagu’s/Pallid Harrier (Circus pygargus); MH, Marsh Harrier (Circus aeruginosus); SB, Steppe Buzzard (Buteo buteo vulpinus); SE, Steppe Eagle (Aquila nipalensis); SF, Small falcon (ca. 220 g), StE, Short-toed Eagle (Circaetus gallicus). Cross-country speed 5 2.67 3 log body mass 1 1.37; 95% confidence interval of the slope: 1.38 11.23; r11 5 0.63, P , .05. Note that with a following wind, all speeds would be higher. From Spaar (1997).

3202 m above ground. After that, the bird continued migrating until an hour after sunset. On March 29 2014, also in Ethiopia, another bird (a female) attained an altitude of 4771 m above sea level, some 2710 m above ground. In some topographic situations, given appropriate wind and temperatures, updrafts called lee waves are sometimes formed on the downwind sides of mountains. Lee waves reach much greater altitudes than thermals, and sometimes

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extend for several kilometres, even over a water surface. Because of their restricted distribution, they are unlikely to be of widespread importance in soaring bird migration, but they could be used in some situations, as when crossing the Strait of Gibraltar (Evans & Lathbury, 1973; Bildstein et al., 2009) or moving through Panama (Smith, 1985). Migrants using lee waves would normally be too high to be seen from the ground. While most soaring bird migration occurs by day, some species have been seen flying over the sea or other hostile substrate at night. European Honey Buzzards have been recorded by radar migrating over Malta at night (Elkins, 2005) and have appeared on dark nights in autumn at the lighthouse on Heligoland Island off Germany (Ga¨tke, 1895). In addition, Levant Sparrowhawks have been found to enter tree roosts at night in Israel after descending from a daytime flight over desert (Yosef, 2003). Other raptor species that have been recorded flying at night over sea or desert include the Hen Harrier (Circus cyaneus), Osprey, Lesser Kestrel, Hobby and Peregrine, and other over-water migrants, such as Chinese Sparrowhawk, Grey-faced Buzzard, Eleonora’s Falcon and Amur Falcon (F. amurensis) (DeCandido et al., 2006; Limin˜ana et al., 2012a; Lo´pez-Lo´pez et al., 2010; Mellone et al., 2013; Meyburg et al., 2017b). Weather affects soaring landbirds in some of the same ways as other birds. Wind strength and direction influence the number of soaring birds that migrate on particular days, their travel routes, flight altitudes and speeds. Low dense cloud and rain suppress migration altogether. To provide ideal migration conditions, however, different wind directions and temperatures are needed at different sites, depending on local topography, and on the importance of thermals as opposed to updrafts from slopes. Compared to other birds, soaring species depend more on the interaction between wind and topography than on wind alone. In addition, thermals cannot form in strong winds which, in the absence of other updrafts, bring soaring bird migration to a halt, however favourable the wind direction. Hence, on some days that are ideal for most migrating birds, soaring species may be grounded. Observers quickly learn the weather conditions associated with the day-to-day passage through particular migration sites. In general, counts are higher when local conditions are favourable in terms of winds and temperatures, and when birds have been held up for several days previously by poor weather (rain, adverse winds) (see Miller et al., 2016a,b for Gibraltar). At Hawk Mountain, for example the passage is usually large on days after cold fronts have passed through the region. Nevertheless, different species favoured somewhat different conditions for migration and showed different degrees of delay (Allen et al., 1996). Because weather conditions change during a season, migration timing can influence routes and speeds, sometimes causing striking differences between age groups. For example in Europe juvenile Honey Buzzards take markedly different routes to adults, as described below; and in eastern North America, juvenile Golden Eagles travel faster than adults, mainly because they depart later in stronger winds and travel more downwind (Rus et al., 2017).

Water crossings Large water bodies present obstacles for migrating soaring birds mainly because of the absence of adequate thermals. Outside the tropics, regular crossings made by obligate soaring species rarely exceed 20 km (Bildstein, 2006; Agostini et al., 2015). Soaring birds are often held up at such crossing points for days on end, waiting for favourable winds (Bildstein et al., 2009; Vansteelant et al., 2014; Miller et al., 2016a,b; Panuccio et al., 2016). To attempt such a crossing, birds typically soar as high as possible, before departing on a long glide overwater. In ideal weather, Black Kites needed 20 30 minutes to cross the 14 km Strait of Gibraltar, with speeds of 36 50 km/h, starting at 600 1200 m asl and arriving on the opposite coast at an altitude of 20 100 m asl (Santos et al., 2020). Adverse winds lengthened their overwater flights: headwinds by slowing progress and making it impossible for birds to reach the other side on a glide so causing them to flap for longer, and side winds by blowing the birds from short to longer crossing points. Some Black Kites attempted a crossing, only to abort it and turn back, and juveniles made more ‘mistakes’ than adults, more often ending up close to the waves. Exhausted raptors have been seen to fall in the water and drown, especially large species (Partida, 2007; Zu-Aretz & Leshem, 1983), and other overwater losses have been documented by tracking studies (Klaassen et al., 2014; Oppel et al., 2015; Meyburg, 2021). Griffon Vultures (Gyps fulvus) struggle to cross the Strait of Gibraltar in spring, and sometimes land on the beach exhausted, while on one day with strong side-winds eleven immatures were washed up dead (Partida, 2007). Other instances of mortality involved Egyptian Vultures and Lesser Spotted Eagles when juveniles, lacking the guidance of experienced adults, attempted to cross the Mediterranean at places too wide for them (Oppel et al., 2015; Meyburg, 2021). But whatever the species, crucial factors promoting a successful crossing include the length of crossing, starting altitude and wind conditions. Raptors less dependent on updrafts make much longer sea-crossings. These include mainly falcons, but also some other species (eg Pandion, Pernis and Butastur), although they seem dependent on good tailwind support (Meyer et al., 2000; Agostini et al., 2002; Nourani et al., 2016). The record is held by Amur Falcons which, as mentioned above, each year cross the Arabian Sea between India and East Africa on overwater flights of 2540 3100 km. In satellite-tagged

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birds, the autumn crossing occurred in late November, helped at that late date by the prevailing monsoon winds. On the spring journey, the birds took a similar over-sea route, again helped by monsoon winds, rather than an overland route far to the north as previously assumed (Meyburg et al., 2017b). These birds may have exploited as overwater food the concentrations of dragonflies which cross the western Indian Ocean twice each year on similar migrations between India and Africa (Anderson, 2009). One Amur Falcon flew over the sea from East Africa and then India, not stopping until it reached Myanmar on a flight of 5912 km taking 5 days. Other long over-water flights recorded by satellite tracking involved one of 1558 km taking 44 hours by an Osprey migrating south over the west Atlantic, and another by a Saker Falcon (Falco cherrug) which flew 1100 km from Albania across Italy and the Mediterranean to Libya in less than 24 hours (Horton et al., 2014; Prommer & Bagyura, 2021). Among Ospreys, five juveniles which were equipped with GPS-Accelerometer Magnetometer loggers proved able to find and use thermal uplift while crossing the Mediterranean, on average 7.5 times per 100 km, and could reach altitudes of 900 m above the sea surface (Duriez et al., 2018). Their climb rate was 1.6 times slower than overland, and they kept flapping most of the time while circling in the thermals, indicating that the updraft was weak. The frequency of thermal soaring was correlated with differences between sea surface and air temperatures, with thermals produced when surface waters were warmer than the overlying air. Examination of the migrations of five raptor species tracked on oversea journeys in various parts of the world revealed that their sea-crossings were invariably associated with favourable winds and with uplift created by warmer sea and cooler air (Nourani et al., 2021). The routes chosen also offered the greatest long-term certainty in wind conditions. In Europe, while adult European Honey Buzzards from Sweden mainly cross to Africa at Gibraltar, juveniles from the same breeding areas fly directly south and cross wider parts of the Mediterranean, on overwater flights exceeding 600 km. However, they migrate later in autumn than the adults, when over-sea tail-winds are stronger and uplift more available (Ha˚ke et al., 2003; Nourani et al., 2020). The juveniles also have slightly different wing shapes which may help their over-water crossing. Also, because the adults have left by then, the young have no experienced birds to guide them over the safer but more circuitous route over Gibraltar. Despite their longer routes, Swedish adults completed their journey to Africa in only 42 days, on average, compared with 64 days in juveniles. Further east, some adult Honey Buzzards also cross the Mediterranean at its widest parts in autumn and especially in spring, as do Western Marsh Harriers on a beeline route between their breeding and wintering areas (Agostini et al., 2017). In East Asia, overwater flights of up to 680 km made by Crested Honey Buzzards tracked across the East China Sea from Japan were again helped by strong tailwinds and suitable thermals (Nourani et al., 2016). In tropical areas, in the trade-wind zones, the sea in the morning is warmer than the land and air and often generates thermals which are used by raptors. This holds, for example for the Asian raptors that migrate by island-hopping down the eastern seaboard (Flyway 5 above). Raptors using this flyway travel between island groups, flying over the open sea for distances up to 350 km. This migration may be seen at Kenting, at the southern end of Taiwan, where the main participants are Grey-faced Buzzards and Chinese Sparrowhawks, with many other species in smaller numbers. Heading for Taiwan from the south, Chinese Sparrowhawks have been detected over the sea by radar, occurring in long straggling flocks averaging 3.1 km long, travelling at an average of 51 km/h (Sun et al., 2010). In this flyway, the choice of routes seems influenced mainly by the locations of islands and the presence of favourable tailwinds (Nourani et al., 2018). Even small islands, seemingly off the main route, can attract large numbers of passing raptors: for example more than 230,000 were counted in autumn 2007 on Sangihe Island between Mindanao (Philippines) and Sulawesi (Indonesia), almost all Chinese Sparrowhawks (Germi et al., 2009). This migration was unusual in that, in both autumn and spring, the birds had to fly against headwinds, keeping low enough for their flight speed to exceed the countering wind speed.

Extension of migration as a consequence of soaring In travelling between two points, soaring migrants typically cover much longer distances than flapping birds. Extension of the route comes from (1) distance added as a result of circumventing large water bodies and using longer overland routes; (2) distance added due to circling and climbing in thermals, as well as moving between them, which is not necessarily along the shortest and straightest route. These various distances were calculated for four species in Israel using data collected by following birds with a motorized glider (Leshem & Yom-Tov, 1996b). The four species were the Great White Pelican, White Stork, Lesser Spotted Eagle and European Honey Buzzard. Between the centres of their breeding and wintering ranges, these four species had extended their migration distances by 48% 91% compared with straight-line distances. The increased distance caused by circumventing sea areas was estimated at 22% 34% in different species, while the increase resulting from the use of thermals accounted for an additional 23% 57%. Presumably,

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the energy saved by the use of soaring gliding flight more than compensated for the energy consumed from the extra distances flown, and the avoidance of long sea-crossings may have improved survival. Other measures of route lengthening caused by deviations from straight routes varied from 16% to 113% among different soaring raptors tracked on migration, compared with 9% 24% in Ospreys and falcons less dependent on soaring flight (Table 4.2). But all these measures included only horizontal deviations and not vertical ones. Avoidance of long water crossings results in some curious detours, as exemplified by Short-toed (Snake) Eagles (Circaetus gallicus) nesting in central Italy (Agostini et al., 2002; Mellone et al., 2011). Instead of migrating south in autumn, and making the oversea flight from Sicily to North Africa, these birds start by migrating northwest up the Italian peninsula, then move westward and southwestward around the Mediterranean to cross the 14 km of sea at Gibraltar, adding 1300 km to the most direct route. This gives a forceful demonstration, in this species, of the amount of extra travel undertaken to avoid a long and presumably risky sea-crossing. A similar detour is made by Short-toed Eagles nesting in Greece which start their autumn journey by heading north-northeast to take the short sea crossing at the Dardanelles or Bosphorus, rather than the long southward route from southern Greece across the Mediterranean to Libya (Panuccio et al., 2012).

Timing and food supplies Wherever the observation point, the timing and duration of passage varies between species, but within each species both autumn and spring peak dates are remarkably consistent from year to year, as shown for Israel in Table 7.4. For this site, the only exception to this generalization was the Great White Pelican, which showed considerable variation in the peak dates of autumn passage. Comparing the different species of raptors moving through Israel, three general trends emerged: (1) species that eat warm-blooded prey (birds and mammals) generally passed earlier in spring and later in autumn than species that eat coldblooded prey, with the insectivores being last to move north and first to move south (Chapter 15); (2) species that travel in large aggregations (Lesser Spotted Eagle, European Honey Buzzard, Levant Sparrowhawk, Red-footed Falcon) passed within a shorter period each year than other species; (3) species that breed over large areas of Eurasia had the longest passage periods, presumably because birds from different localities had started at different dates and travelled different distances; and (4) whereas for some species the spring passage was of shorter duration than the autumn one (as in many other birds, Chapter 9), in most raptor species the spring passage period was more extended. This trend was most marked in large species whose populations contained a large proportion of immatures, which usually migrated later in spring and over a longer period than adults, spending a much shorter period in the breeding areas (for Common (Steppe) Buzzard, see Gorney & Yom-Tov, 1994; for Lesser Spotted Eagles, see Meyburg et al., 2001). The same held for the White Stork in spring when TABLE 7.4 Average altitude ( 6 SD) and daily progress (velocity 6 SD) of four species of soaring migrants over Israel, together with estimates of the daily flight time and distances travelled. Species

Number

Start height in thermal (m)

End height in thermal (m)

Height band in thermal (m)

Velocity (km/hour)

Mean migration time (h/day)

Mean daily flight distance (km) over Israel

Estimated mean duration of migration (days)a

Great White Pelican (Pelecanus onocrotalus)

467

344 6 175

562 6 186

218

29.2 6 9.1

7.5

249

21

White Stork (Ciconia ciconia)

1059

463 6 209

713 6 221

250

38.7 6 9.6

9.0

348

23

Lesser Spotted Eagle (Clanga pomarina)

78

567 6 201

871 6 184

304

50.9 6 6.7

7.5

381

21

European Honey Buzzard (Pernis apivorus)

215

836 6 211

1123 6 225

287

45.2 6 9.0

10.0

446

23

Measurements made from a motorised glider and light aircraft, as well as by radar. Species listed in decreasing order of body weight. aEstimated time taken to travel between the centre of the breeding range and the centre of the wintering range, assuming that migration occurred on every day over the daily distance shown. These estimates are lower than those uncovered by satellite-tracking of the same species, mainly because migration did not occur on every day.

Source: From Leshem & Yom-Tov (1996a).

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adults began passing over in February, while immatures appeared in April May. Typically, however, whatever the length of the total migration period, the bulk of the birds may pass on a small number of days within it. Food is important to the timing of raptor migration, not so much on the route itself, but in breeding areas (Newton, 1998, Chapter 15). At the end of summer, the first prey animals to disappear with the onset of cold weather at high latitudes are large insects, followed by reptiles, amphibians and also fish which retreat to deeper water. By then, many small birds have begun to migrate, and mammals begin to disappear, some hibernating and others spending increasing periods in sheltered sites where they are unavailable to raptors. During spring, the situation is reversed, with mammals appearing first and large insects last. The Steppe Eagle, which eats chiefly mammals, is the first to migrate north, passing through Israel mainly in early March, while the European Honey Buzzard, which eats mainly bee and wasp larvae, migrates last, in May. The Steppe Eagle spends 6 months in its breeding areas, passing south through Israel mainly in mid-October to mid-November, while the Honey-buzzard spends little over 3 months in its breeding areas, passing through Israel in early September. The eagle also has a longer breeding cycle than the Honey Buzzard, with longer incubation, nestling and post-fledging periods.

Multiple wintering areas Like many other birds, raptors often visit a succession of different areas while on their non-breeding ranges. Among the Eurasian species that winter in Africa, such mobile species, as confirmed by tracking studies, include the Lesser Kestrel (Catry et al., 2011a,b), Montagu’s Harrier (Trierweiler et al., 2013; Schlaich et al., 2016; Limin˜ana et al., 2012b), Marsh Harrier (Strandberg et al., 2008), Lesser Spotted Eagle (Meyburg et al., 1995a,b) and Black Kite (Meyburg & Meyburg, 2009). Individuals of these species have been found to use 2 4 different areas while in Africa, starting in the Sahel zone and often moving further south to moister regions at later dates, as the Sahel dries. Individuals may use the same succession of areas in different years. In contrast, species that remained in one area throughout their stay in Africa included the Osprey (Ha˚ke et al., 2001), European Honey-buzzard (Ha˚ke et al., 2003; Vansteelant et al., 2017) and Booted Eagle (Mellone et al., 2013). Adults of these species migrated directly to their wintering territories in the moister habitats south of the Sahel, while the juveniles often wandered around for a period, presumably until they found a suitable area to which they then returned in later years. In South America, Swainson’s Hawks are perhaps the most mobile of wintering raptors, moving around on grasslands and concentrating in areas of abundant grasshoppers (Kochert et al., 2011), while coastal Peregrines and forest-dwelling Broad-winged Hawks remain on the same territories throughout their stay and return there in subsequent years (McGrady et al., 2002; McCabe et al., 2020).

Social factors One presumed advantage of soaring birds migrating in such concentrations is that it makes finding thermals easier, for most can simply head towards the soaring birds ahead thereby saving time and energy. Observations made by radar and by use of a glider in Israel revealed that, on peak migration days, the lines formed by flocks extended up to 200 km, so that most individuals had before them a continuous route marked out by their predecessors (Leshem & Bahat, 1999). This held for various raptors and storks, all migrating together and using the same thermals. It is difficult with raptors to tell whether the birds migrate in flocks simply because they share the same narrow migration route, and the same updrafts within it, or whether they are attracted to one another for additional reasons. Not surprisingly, the biggest flocks are seen in abundant species which migrate within a short time period, such as the European Honeybuzzard, Steppe Buzzard, Black Kite and Levant Sparrowhawk in the Old World, or the Broad-winged Hawk and Swainson’s Hawk in the New World. Once they leave a thermal, the birds seem to behave more as individuals and head off for the next thermal, whose position is marked by the presence of other circling birds. In this sense, the birds clearly benefit from travelling on the same days as others and from watching one another (for White Storks, see Flack et al., 2018). When making water crossings, birds in larger flocks show reduced flapping rates, possibly because they are more likely than smaller flocks or singles to find an optimal route (Bildstein, 2006; Careau et al., 2006). It is mainly the rarer species, such as Short-toed Eagles and Egyptian Vultures which also depend on thermals that travel as singles or small groups. Where flocks contain birds of mixed ages, the younger birds could learn the most efficient routes from older individuals, and there are examples of juveniles travelling alone taking inappropriate routes and perishing on long sea crossings, while those travelling with adults showed much lower mortality (for Egyptian Vulture, see Oppel et al., 2015; for Lesser Spotted Eagle, see Meyburg et al., 2017a). The benefit of social learning is particularly evident in Short-toed Eagles breeding in Italy and Greece, as mentioned previously, in which the juveniles accompany adults along extremely detoured pathways avoiding long crossings of the Mediterranean (Panuccio et al., 2012). They provide some of the best global examples of how water barriers and social learning can shape the migratory pathways of soaring birds.

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Numbers entering Africa Adding the maximum counts from Gibraltar, Messina (Italy), Israel (or Suez) and Bab el Mandeb (on the southern end of the Arabian Peninsula) for certain soaring species, as given in Tables 7.1 and 7.2, gives minimal rounded estimates of the numbers entering Africa from Eurasia as follows: Short-toed (Snake) Eagle 30,000, Black Kite (spring count) 224,000, Lesser Spotted Eagle 142,000, Steppe Eagle 75,000 (spring count), Booted Eagle 36,000, Levant Sparrowhawk 60,000 and Steppe Buzzard (spring count) 466,000. These species alone total 1,033,000 birds, with White Stork at 422,000, Black Stork (C. nigra) at 20,000 and Great White Pelican at 70,000. Only for these species were the migration seasons reasonably well covered at each site, and no other major routes are known. In addition, European Honey-buzzards alone probably total more than one million, because maximum counts at three major sites sum to 933,000, and exclude the many juveniles that cross the Mediterranean Sea on a broader front. Meaningful counts of falcons and harriers, which migrate by flapping, or by a mixture of flapping and gliding, cannot be made, as they migrate more on a broad front, and can cross the Mediterranean Sea anywhere. Hence, their total numbers are as yet unknown. Nevertheless, the total number of raptors and other soaring birds entering Africa from Eurasia each year could exceed three million.

Numbers entering Central and South America In Panama, along the path of migration, corridors of rising air produce long clouds, and for much of the time raptors fly through the cloud base, taking advantage of the ‘thermal cloud streets’ that enable them to glide for tens of kilometres at a time. They also use the updrafts created by winds hitting the central mountain spine. Counts at Panama are inevitably underestimated, partly because the birds are often hidden by cloud, and also because they often fly higher than visual range. Some fly over the central mountains at 4 6 km above sea level, while others may overfly the midafternoon storms at even higher altitudes (Smith, 1985). Some three million raptors have been counted as they pass northward in spring through Panama (Batista et al., 2005). This figure was probably an under-estimate, because it was only half the total counted in autumn further back along the route at Veracruz. And on November 2, 2014, 2,105,060 raptors, mostly Turkey Vultures and Swainson’s Hawks, passed over Ancon Hill in Panama, the assumed single-day world record for any site (Tweet from Smithsonian Tropical Research Institute). The Veracruz totals, made up of counts at two sites (Cardel and Chichcaxtle), represent the largest migration stream of soaring birds yet seen anywhere in the world. The overall autumn total in 2002 amounted to nearly 6.6 million raptors, including nearly 2.7 million Turkey Vultures, 2.4 million Broad-winged Hawks and 1.1 million Swainson’s Hawks (the latter species exceeding 1.2 million in 2003 and 2005). Up to 25 other raptor species have been seen at this site (Table 7.1), and several other soaring species, including more than 28,000 American White Pelicans. In addition, however, other raptors are known to migrate down the western side of the Americas at similar latitude to Veracruz, and further east, yet others also migrate down the Florida peninsula across the Caribbean Islands to South America. No good estimates are available for these other routes, but the Ospreys counted on passage through southeast Cuba (La Gran Pedra) in autumn would represent about 90% of the known eastern North American population. It seems that the total raptor migration between North and Central South America could well exceed seven million birds, which makes the known Eurasian African total of three million seem small. It may reflect the fact that the western Eurasian raptor population has been more markedly depleted by human action than the North American one.

Feeding and energy reserves The energy cost of soaring-gliding flight has been calculated at around 1.5 2.0 3 BMR (basal metabolic rate), a cost spent mainly in maintaining the wings in gliding position. In contrast, energy consumption during flapping flight has been calculated at 5 25 3 BMR, depending on species and circumstances (Chapter 3). So per unit time, soaring birds could be using only about 8% 30% of the energy consumed in flapping flight, making soaring gliding by far the least energy-demanding mode of travel (Chapter 3). A specific estimate for European Honey Buzzard was within this range of values, at about 17% (Meyer et al., 2000). In extreme cases, exemplified by Gyps vultures, the cost of soaring once the birds are airborne is little more than the cost of sitting still, as judged by the heart rate (Duriez et al., 2014). One would expect, therefore, that soaring birds would need much less migratory fuel than other same-size birds making similar overland journeys or that they would travel further on a given amount. Most of the information available on the feeding and fattening patterns of migrating raptors comes from incidental observations. Many raptors (notably accipiters, harriers and falcons) feed frequently while on the route, having been

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seen to catch prey, or to migrate with swollen crops, or to enter baited traps. Their fat contents are normally low. Insectivorous species have also been watched feeding at concentrations of insects, for example Plumbeous Kites (Ictinia plubea) eating migrating dragonflies (Smith, 1980). In contrast, some other species clearly accumulate substantial fuel reserves for migration, as their body weights can increase by 25% 30% or more before departure. This was recorded in European Honey-buzzards and Ospreys leaving from Europe in autumn, in Broad-winged Hawks leaving Panama and in Steppe Buzzards leaving South Africa in spring (Smith et al., 1986; Gorney & Yom-Tov, 1994). It may be assumed that these species cover at least large parts of their migrations without feeding. Some of them, such as European Honey-buzzards, seem to make no attempt to feed while on migration or migrate along narrow routes in such huge numbers that they would have little chance of obtaining a meal. They travel long distances through deserts or other habitats where little food would be available. In the past, migrating Honey-buzzards were appreciated for their high-fat contents, and at several sites (including Falsterbo) were harvested and salted to serve as winter food. Interestingly, however, about 5% of migrating Crested Honey-buzzards seen in Thailand in autumn had a full crop, with some carrying pieces of bee-comb (DeCandido et al., 2015). But in contrast to European birds, these oriental ones were in the tropics, where bees and wasps may have been more readily available at migration time than in temperate Europe. Lack of feeding by some species is also shown by the absence of droppings or pellets at their night roosts (Smith et al., 1986). Bald Eagles (Haliaetus leucocephalus) have been visibly tracked on migration for up to 15 days and were not seen to feed, and captive eagles commonly fast for more than 2 weeks with no apparent harm (Harmata, 2002). Recent satellite tracking of various soaring species has shown many examples of long, uninterrupted travel periods, sometimes over the whole journey (Berthold et al., 1992; Meyburg et al., 1995a; Kjelle´n et al., 1997; Ha˚ke et al., 2003; Mellone et al., 2015). Black Kites seem not to feed regularly on migration, but they occasionally pause, feed and drink at rubbish dumps. It is not unusual to find starving raptors on migration: for example at least 23 out of 122 Broad-winged Hawks caught at roost sites in Panama (Smith et al., 1986), or occasional Nothern Goshawks (Accipiter gentilis) in irruption years (Mueller et al., 1977). Raptors thus seem to fall into two categories. One contains species which accumulate little or no extra body fat and regularly hunt during migration, either on route or at stopover sites. Accipiters, falcons and harriers belong to this category and also tend to migrate singly or in small groups, which presumably facilitates hunting. Species regularly hunting birds on migration, such as the Peregrine and Eurasian Sparrow Hawk, seem to synchronize their journeys with those of their prey, feeding as necessary on a ‘fly-and-forage’ strategy (Bildstein, 2006). The second category contains longdistance soaring species which accumulate substantial fat stores before migration and perform the whole journey on these stores or have only infrequent stops to replenish them. They include the Broad-winged and Swainson’s Hawks in North America, and the European Honey-buzzard and Steppe Buzzard in Europe, all of which travel in such large concentrations that it would be almost impossible for them to feed on route. They nevertheless stop to drink periodically. But the implication is that they last several weeks without feeding, at least while they are in major migration streams. The Osprey also accumulates large fat stores before migration, but on long journeys, it may stop to feed at suitable lakes, perhaps 1 3 times during a journey through Europe (Strandberg & Alerstam, 2007). Like other birds, many raptor species are likely to show different feeding and fattening strategies in different parts of their range, according to whether their local populations migrate short or long distances (for Osprey, see Monti et al., 2014). Turning to non-raptorial species, White Storks seem to feed every morning when passing through suitable areas, and Great White Pelicans feed and fatten wherever fish are available in abundance. Some other species accumulate substantial reserves. Sandhill Cranes (Grus Canadensis) increased in body mass by about 34% (males) and 30% (females) at major staging sites in spring before continuing to their northern breeding areas (Krapu et al., 1985). Carcass analyses revealed that most of this weight increase was due to fat deposition. Other species of cranes also pause for several days or more at stopover sites to refuel, as shown by tracking studies (see Kanai et al., 2002 for Siberian Crane).

SUMMARY Because soaring birds migrate entirely (or almost entirely) by day, often at heights low enough for observers to identify them from the ground, and because they pass certain points in concentrated streams, some aspects of their migrations have been studied in detail. Precise migration seasons, day-to-day movements in relation to weather, variations in timing and routes between age-groups are all aspects of migration for which more precise detail has been obtained for soaring birds than for most other migrants. On migration, soaring raptors, storks and pelicans depend mainly on updrafts where crosswinds are deflected upwards from cliffs or slopes or on thermals where columns of rising air provide lift, enabling the birds to glide to the next thermal losing height, and then rise again. Such species typically make as much of their journey as possible

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overland, making detours to avoid or minimize water crossings. On a world scale, several major flyways for soaring birds have been identified, along which enormous numbers pass each year: one converges through Panama, a second across the Straits of Gibraltar, a third along the Great Rift Valley in the Middle East, a fourth through Southeast Asia and western Indonesia and a fifth through the islands of eastern Asia to the Philippines and eastern Indonesia. The latter is unusual in the extent of water-crossing, as the birds travel by island-hopping, with individual over-water flights up to 350 km or more. Particularly large numbers of raptors have been counted at Eilat in Israel (. 1.2 million in spring), at Veracruz in Mexico ( . 6 million in autumn) and at Panama (3 million in spring). At particular watch sites, different species pass in the same sequence each year, in both autumn and spring, and mean passage dates are remarkably consistent from year to year. In general, species that pass northward earliest in spring pass southward latest in autumn. In some species, the autumn passage is spread over a longer period than the spring passage, and in others the reverse. Spring passage tends to be the longest in large species in which the nonbreeding immatures migrate towards breeding areas much later than adults. Otherwise, the timing and duration of passage depend on the extent of the breeding range (longer passage with wider latitudinal spread) and diet (bird-eating and mammal-eating species spending longer on breeding areas than reptile-eaters and insect-eaters). Some species take slightly or markedly different routes in autumn and spring, depending largely on wind conditions. Many raptor species are known to feed on migration, especially bird-eating falcons and accipiters which migrate at the same time as their prey, and insectivores some of which also encounter food on route. Eagles and buteos that migrate long distances feed more episodically and probably make large parts of their journeys without eating. At least some raptors are known to accumulate migratory fat (with up to 30% increase in body weight in Steppe Buzzards). Because of their dependence on topography, the wind and other conditions that favour heavy passage differ to some extent from one site to another. However, low cloud and rain are largely inimical to migration by soaring birds, as in other birds.

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Chapter 8

Seabird movements

Wandering albatross (Diomedia exulans), one of the largest and most wide-ranging of all migratory birds. ‘Not all those who wander are lost . . .’ John R. R. Tolkien (1954).

Only in the last few decades have modern tracking devices provided information on the movements of pelagic seabirds, which are difficult to study reliably by using leg rings. Geolocators are ideal for use on these species because individuals usually return annually to the same nest sites, where they can be re-trapped to retrieve the data. Other devices, usually attached to the bird’s leg, can provide extra information: for example immersion devices record whether a bird is on or out of water, and for species that dive for food, depth devices can separate feeding attempts from rests on the surface. This technology has greatly advanced our understanding of both the migrations and foraging behaviour of pelagic birds, especially procellariforms (albatrosses, petrels and shearwaters) whose migrations were until recently among the least known. The distributions of seabirds in the breeding season are governed by nest sites, mainly on sea cliffs or on islands lacking mammal predators. Their distributions at sea are governed mainly by the marine zones to which they are adapted, and the locations of rich feeding areas within those zones (Figure 8.1). Like landbirds, some seabirds may spend the whole winter in one main area, while others visit several different areas in succession. A small number (such as albatrosses) may keep travelling for the whole period between breeding seasons, with breaks for rest and feeding. Most pelagic species travel by night as well as by day, and some evidently feed at night, taking advantage of the nocturnal upwards movement of plankton and its predators to nearer the surface.

THE MARINE ENVIRONMENT In contrast to land areas, marine areas are interconnected, with continuous round-the-world ocean lying both north and south of the main continents as well as between them. Nine main seawater zones are recognized (Figure 8.1), running around the globe and differing in water temperature and density, salt, nutrient and oxygen contents. About 81% of all The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00007-5 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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FIGURE 8.1 Biogeographical seawater zones. Areas of exceptionally high productivity are shaded black, areas of lower but still above average productivity are shaded dark blue. E marks the Evlanov Seamount and basin. Modified from Newton, 2003, based on various sources. 1. The arctic zone embraces the teeming seabirds of northern Canada, Greenland and Eurasia. The Arctic Ocean is shallow, with large continental shelves, and for much of the year ice-covered. Seabirds are present mainly in summer, mainly various auks, although openings in the ice allow some species to remain in winter, notably the Ivory Gull (Pagophila eburnea). 2. The sub-arctic zone is also rich in seabirds, with various auks the most numerous, feeding largely on the abundant capelin, clupeoids and sand eels. 3. The northern temperate (boreal) zone is shallow in many regions, which facilitates wind-generated mixing. Many seabirds in this zone concentrate to feed at the shelf break or at mid-shelf tidal fronts. The water is cold (3 4 C), wind-swept and rich, supporting large fisheries and seabird populations. 4. The northern subtropical zone is less rich and holds fewer breeding seabirds than more northern zones. 5. The tropical zone extends between the seasonally moving limits of the 23 C isotherms, north and south of the equator, rising to 29 C near the equator. Of generally low productivity, in vast areas of the tropics the dominant seabirds are boobies, terns, frigate birds, tropicbirds and tropical procellariiforms, and their main foods include squid and flying fish. 6. The southern subtropical zone contains some cold-water areas within it, notably the Humboldt and Benguela Currents, which support locally endemic species and others found in colder higher-latitude regions. The warmer areas share some species with the tropics. 7. The southern temperate zone supports large numbers of seabirds, especially procellariiforms, feeding mainly on various fishes. 8. The sub-antarctic zone also supports very large numbers of seabirds, especially procellariiforms and penguins, feeding mainly on various fishes and squids. 9. The Antarctic zone is richer in phytoplankton than any comparable area. Under the intense and almost continuous sunlight of the austral summer, productivity is enormous. In places, crustacea such as krill average 30,000 individuals per cubic metre of surface water, reddening the sea over many square kilometres. As in the neighbouring zone, procellariiforms and penguins are the most diverse and abundant species, feeding largely on various fishes and crustaceans.

seabird species breed in 1 2 of these nine zones, another 17% extend to three or four zones, and fewer than 2% extend to more than four zones (Newton, 2003). Although broadly latitudinal in distribution, seawater zones are disrupted to some extent by surface currents which are in turn influenced by winds. Within the marine zones themselves, the locations of major seabird feeding areas depend largely on features that lead to locally increased productivity, such as upwellings, sea mounts, fronts and eddies. At upwellings, nutrients are drawn up from the sea bed to near the surface and then dispersed by horizontal flow. These nutrients support planktonic growth and then other seabird prey such as crustaceans and fish, creating important foraging areas for seabirds and sea mammals. Another important feature of the marine environment is that colder waters usually contain more nutrients and oxygen than warmer waters, and therefore support more life. Cold waters also slow the movements of fish, presumably making them easier for fast-swimming birds to catch than in warm waters. Apart from pack-ice zones discussed below, it is therefore much less important for seabirds to move to lower latitudes for the winter than it is for landbirds, and

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indeed many sea-dwelling birds may move further from land to pass their non-breeding period in places at similar or even higher latitude than their nesting colonies (examples below). The main disadvantages of wintering at high latitudes are the shorter daylengths (for diurnal feeders), the lower temperatures which raise energy costs, and the more frequent storms that can disrupt feeding. In contrast to many land habitats, therefore, productivity in the sea is lowest in tropical and subtropical regions (but with local exceptions), and highest at high latitudes and around continental shelves (including some at low latitudes), especially where rivers provide additional nutrient input. The most productive of large seawater regions is the Southern Ocean, followed by the North Pacific and then the North Atlantic. The areas of lowest productivity are the centres of the Pacific, Atlantic and Indian Oceans. These regional variations in productivity are reflected in similar variations in seabird abundance. During the non-breeding period, many pelagic seabirds travel thousands of kilometres to upwelling regions and frontal zones where prey is most predictable. Some species make similar long journeys even in the breeding season (see below). Water currents flowing towards the equator along the steep margins of continents produce major upwellings, creating areas of high productivity along certain westward-facing coastlines (Figure 8.1). These areas include the Humboldt Current which flows up the coast of western South America and then veers westward in a long cold-water tongue to envelop the Galapagos Islands which lie on the equator 900 km out to sea. A similar Benguela Current runs up the west side of South Africa and is known to fishermen mainly for its abundance of anchovies (Engraulis encrasicolus) and sardines (Sardinops sagax). Correspondingly, in the northern hemisphere, the California current flows southward off western North America and the Canary current off northwest Africa, but others occur off other western coasts that have narrow continental shelves. On some of these coasts, the upwelling occurs year-round, while in others it is seasonal, depending on winds. In addition to the main upwelling areas shown in Figure 8.1, other short-term or weaker upwellings occur locally in many other areas, especially near the edges of continental shelves and around islands and sea mounts. Other productive areas are linked to ocean fronts and eddies, which are important to a range of marine predators, notably in the Southern Ocean where the Subtropical Convergence and the Polar Front offer rich pickings for seabirds. These nutrient-rich areas can be detected not only from the abundance of fish and seabirds they hold but also from satellite images which measure such features as chlorophyll-a concentration and its seasonal changes. Chlorophyll levels reflect the density of phytoplankton, the base of all food chains on which the crustaceans, squids and fishes eaten by birds ultimately depend. Together, these nutrient-rich areas form less than 5% of the total ocean area. They all have productivities up to 10 times greater than the rest of the ocean and collectively support millions of seabirds and other marine predators. Birds use these productive areas not only in the breeding and non-breeding seasons but also as places to refuel on their migrations. Refuelling is known from tracking studies, as tagged birds remain in these places for several days or weeks at a time, while immersion or depth devices record the intensity of their feeding behaviour. For unlike landbirds, seabirds cannot be easily caught and weighed while refuelling. Pack ice covers large parts of the Arctic and Antarctic zones, expanding in winter and retreating in summer. In winter it shuts off the food supply for seabirds over wide areas, apart from open-water polynyas (areas of persistent open water among sea ice) where some specialists can remain to feed.

WINDS AND SEABIRD MOVEMENTS Those seabirds living at high latitudes, especially in the southern hemisphere, have to cope with some of the strongest and most persistent winds on Earth. But many pelagic birds are adapted to winds and make use of them for flight. They live with wind, cannot function effectively without it, and some of their most striking migration patterns are clearly adjusted to benefit from prevailing winds (Chapter 4). For most pelagic species, which travel by wind-assisted dynamic soaring flight, migration is much cheaper than for landbirds that depend on flapping flight. Wandering Albatrosses (Diomedea exulans) achieve high flight speeds on fixed wings using little more energy than when sitting still (Bevan et al., 1995; Weimerskirch et al., 2000). It is this ability, helped by winds, which enable these marine soaring birds to spend most of their lives on the wing, travelling huge distances with relative ease, and sometimes achieving speeds of more than 1000 km/day (Klomp & Schultz, 2000; Shaffer et al., 2006). In taking advantage of prevailing winds, some species perform long circuitous flights, adding hundreds or thousands of kilometres to their journeys over what they might achieve on more direct routes but at greater energy cost (Chapter 4; Gonza´lez-Solı´s et al., 2009). They generally travel in tailwinds or crosswinds, avoiding headwinds as much as possible (Paiva et al., 2010). In contrast to procellariform birds which travel by soaring-gliding flight, pelagic auks fly by flapping flight. They therefore expend much more

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energy on movements than procellariforms, generally spending more time on the water and travelling relatively short distances at a time, sometimes by swimming. Global wind patterns are partly caused by the Coriolis Effect which results from the earth’s rotation and causes a generally clockwise wind circulation in the North Atlantic and North Pacific, and an anti-clockwise flow in the South Atlantic and South Pacific. Around the equator, sandwiched between the two trade wind zones, lies the doldrums, a zone of relatively still air in which sailing ships of the past often became delayed for weeks on end, unable to move out. As shown by tracking studies, these wind patterns have a huge influence on both the foraging flights and migrations of pelagic birds. Some species that migrate between hemispheres follow a figure-8 course as they take advantage of the clockwise circulation in the northern hemisphere and the anti-clockwise circulation in the southern (examples below). Nevertheless, these wind patterns are disrupted by the passage of weather systems, so birds can usually find periods of calmer, stronger or contrary winds that they can exploit as necessary.

MIGRATION PATTERNS Almost all migratory landbirds move to lower latitudes for the winter, but some move long distances to spend their non-breeding period at similar latitudes in the opposite hemisphere (Chapter 16). However, in the vast majority of sea areas which remain ice-free in winter, migration of pelagic seabirds is generally more dispersive in nature. Movements can be in any direction towards rich feeding areas, avoiding large land areas, but often crossing from one side of an ocean to another. Some seabirds even spread to higher latitudes for their non-breeding season, and many move east or west from their nesting colonies, becoming more widely distributed but remaining with the same or neighbouring marine zones. Many seabirds make long movements within their non-breeding period, and some seem to be on the move for most of the time between breeding seasons. Nevertheless, tracking studies suggest that seabird migrations fall into fairly distinct categories, as follows.

Direct migrations from breeding areas to lower latitudes Although north south latitudinal shifts between the seasons occur in most landbird migrants, they are relatively less common in seabirds, predominating in (1) polar species which move in autumn to avoid the expanding sea ice and (2) coastal and inshore-feeding species which in year-round ice-free water still move to milder lower latitudes. Among polar species, Ivory Gulls (Pagophila eburnea) and Ross’s Gulls (Rhodostethia rosea) move southward, keeping ahead of the ice as it forms, but not necessarily by the most direct route (Gilg et al., 2010; Spencer et al., 2014; Matfrei et al., 2015). Similar movements to lower latitudes also occur in arctic-nesting Little Auks (Alle alle), Northern Fulmars (Fulmarus glacialis) and Glaucous Gulls (Larus hyperboreus), which extend south for the winter into sub-arctic and boreal waters. Most coastal species that breed and winter at ice-free latitudes migrate fairly directly southward down the east or west sides of the continents after breeding. Such inshore movements are shown by various gulls, terns and Northern Gannets (Morus bassanus), some species among which reach the northern tropics or beyond. The extinct and flightless Great Auk (Pinguinus impennis) seems also to have been a latitudinal migrant, swimming southward from its North Atlantic colonies as far as Madeira in the east Atlantic and Bermuda and Florida in the west. In the southern hemisphere, northward movements to lower latitudes occur among Cape Petrels (Daption capense) and Southern Fulmars (Fulmarus glacialoides) which breed around Antarctica and islands in the sub-Antarctic zone and move north, escaping winter ice, and reaching areas of productive water, such as the Humboldt Current off South America and Benguela Currents off South Africa. Latitudinal shifts also occur in various penguins, such as the Magellanic Penguin (Spheniscus magellanicus) which migrates northwards by swimming up the coast of South America for up to 1500 km (Pu¨tz et al., 2007).

Direct trans-equatorial migrations As in landbirds, some seabirds which make long journeys between hemispheres occupy roughly similar latitudes in both. Some travel fairly directly but may also cross from one side of an ocean to another. Spectacular examples include Arctic Terns (Sterna paradisaea) which have the longest known migrations of any birds, breeding around the Arctic and wintering around the Antarctic (Salomonsen, 1967). The tracking of individuals from various parts of the breeding range has provided detailed information on their routes, refuelling and wintering areas (Box 8.1).

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BOX 8.1 Arctic Tern migrations. Arctic Terns (Sterna paradisaea) have long been known from ring recoveries to perform the longest migrations of any birds, as individuals travel from their nesting areas around the Arctic to wintering areas around the Antarctic, in the austral summer. Tracking of individuals from various parts of the breeding range has now provided detailed information on their routes, refuelling and wintering areas. Birds from colonies in Greenland and Svalbard took one of two routes, separating in the North Atlantic to follow the coasts of either Africa (the eastern route) or South America (the western route). Birds on the western route continued southward to the Weddell Sea area of Antarctica, while some of those on the eastern route swung eastward into the Indian Ocean for some distance before turning and heading on a more southerly route towards the Weddell Sea. However, all the birds tracked from colonies in northern Russia (White Sea area), Sweden and the Netherlands took the eastern Atlantic route, and after rounding the tip of Africa travelled further eastward through the Indian Ocean to the south of Australia, and then headed southward to near Antarctica. These birds thus made longer migrations to a more easterly area than the Greenland-Svalbard birds, but they also then travelled westward to the Weddell Sea before heading north into the eastern Atlantic on their return northward migration (Fijn et al., 2013; Volkov et al., 2017; Alerstam et al., 2019). Major refuelling occurred in the North Atlantic (including in the Evlanov Basin see text), where in autumn some birds paused for 3 5 weeks. Birds that used the eastern route also paused in the Benguela Current region off Southwest Africa, while those that continued eastward also paused in the south-central Indian Ocean. The major foraging areas in the Atlantic were used on both outward and return journeys, but generally for longer on the former. In the eastern Pacific, Arctic Terns from Alaska followed the western coasts of the Americas, pausing to re-fuel in the California Current off North America and at the north and south ends of the Humboldt Current off South America (McKnight et al., 2013). These birds flew on south to join the North Atlantic birds in the Weddell Sea (Egevang et al., 2010; Fijn et al., 2013; McKnight et al., 2013; Volkov et al., 2017). Tracked birds seemed to navigate between stopover sites of high productivity, with migration corridors passing over less productive areas (McKnight et al., 2013). Tracking devices confirmed that Arctic Terns were exclusively diurnal foragers, spending their nights flying or standing out of the water, possibly on flotsam. Furthermore, with their pole-to-pole migration, Arctic Terns from High Arctic colonies such as Svalbard experienced approximately 80% of all annual daylight possible (the most by any animal), maximizing opportunities for their diurnal foraging. However, with such long journeys, they probably faced strict time constraints throughout the migration, timing stopovers to match local marine productivity while simultaneously aiming to arrive in the wintering areas with sufficient time remaining to complete the annual moult (60 days) before returning north. Arctic Terns can live for 30 years, so the total distance travelled by some birds in a lifetime could exceed 2.7 million km, equivalent to more than three return journeys to the moon. One bird breeding in the White Sea area flew 103,600 km in the non-breeding season (Volkov et al., 2017), the longest distance recorded in one non-breeding period from any Arctic Tern (and probably from any bird), raising the possibility of a lifetime equivalent of four return trips to the moon. Only certain albatrosses have been recorded covering longer distances between breeding seasons, but over longer periods (see text).

Other seabirds migrate between hemispheres but over shorter distances than Arctic Terns. They include Long-tailed Skuas (Stercorarius longicaudus) tracked as they migrated from the arctic tundra of Greenland and Svalbard south through the Atlantic to winter mainly in the Benguela Current or beyond (Gilg et al., 2013; Seyer et al., 2021).

Figure-8 trans-equatorial migrations Other birds that migrate between high latitudes in opposite hemispheres travel along figure-8 routes, taking advantage of the clockwise winds in the northern hemisphere and the anti-clockwise winds in the southern hemisphere. One example is the Manx Shearwater (Puffinus puffinus) which breeds around the British Isles and reaches its wintering area off Argentina on a figure-8 route, giving a round-trip distance of more than 25,000 km (Figure 2.4; Guilford et al., 2009). Tracked birds crossed the Atlantic in the southern hemisphere on the autumn journey, and in the northern hemisphere on the spring journey, and spent regular stopovers of a week or two in productive waters where they rested and fed (as indicated by immersion loggers and depth recorders; Freeman et al., 2013). Another bird with figure-8 migrations is the Sooty Shearwater (Puffinus griseus) which nests on islands in the Southern Ocean and extends into the North Pacific or North Atlantic in its non-breeding period. Some 19 tagged individuals from two New Zealand colonies flew across the Pacific Ocean in a figure-8 pattern that lasted an average of 198 days on a round trip averaging around 64,000 km (Shaffer et al., 2006). Each individual stopped for a period in one of three discrete regions of high productivity, off Japan, Alaska or California respectively, before returning to New Zealand across the central Pacific (Figure 8.2). Similar figure-8 journeys were flown by Sooty Shearwaters breeding on

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FIGURE 8.2 The figure-8 migrations of Sooty Shearwaters (Ardenna grisea) in the Pacific and Atlantic Oceans from breeding colonies on the Falklands and New Zealand respectively. Blue shading embraces the migration routes followed by different individuals. The Pacific route follows the movement of birds to one of four main feeding areas identified (cross-hatched). Compiled from the tracking results of Shaffer et al., 2006 and Hedd et al. (2012).

the Falkland Islands and spending the austral winter in the North Atlantic (Figure 8.2; Hedd et al., 2012). They were also shown by Short-tailed Shearwaters (Ardenna tenuirostris) nesting on islands off Tasmania and wintering in the North Pacific (Carey et al., 2014), and by South Polar Skuas (Stercorarius maccormicki) wintering in the Northern Atlantic and the Northern Pacific (Kopp et al., 2011). One potential obstacle to these long-distance migrations is the equator, where winds are usually lacking and food scarce. Yet tracked birds passed rapidly over the equator without stopping for any length of time, presumably by selecting the occasional days with suitable conditions. Lack of winds may account for the near-absence of albatrosses in most equatorial regions.

Dispersive migrations In many seabird species, individuals from the same colonies may move in various directions after breeding, as shown, for example by ring recoveries and tracking studies of Atlantic Puffins (Fratercula arctica), Common Murres (Guillemots) (Uria aalge), Shags (Gulosus aristotelis) and Black-legged Kittiwakes (Rissa tridactyla) from British colonies (Balmer et al., 2013; Ame´lineau et al., 2021). Although the birds from particular colonies might show a predominance of certain directions imposed by coastlines, at the wider population level, migration can be described as dispersive, with individuals migrating in almost any direction, as appropriate. Tracking studies of these species also revealed substantial movements during winter, often involving marked changes in direction. They also showed that individuals may follow the same routes to their own specific foraging areas from year to year (Ame´lineau et al., 2021). The dispersive movements of Atlantic Puffins have been studied from several colonies. Birds breeding on Skomer Island (off Wales) moved west and northwest from the colony, some reaching as far as Greenland, while others moved southwards towards France and Biscay (Guilford et al., 2011; Fayet et al., 2016). In autumn, all then moved northwards or northwestwards into the North Atlantic. Later in the winter, they travelled southwards, some as far as the Mediterranean, before returning (from a variety of directions) to the colony in spring. For most of the winter, these birds were at higher latitudes than their nesting colony. Atlantic Puffins from Skellig Michael off southwest Ireland also headed northwest, and by September some had reached the seas off Newfoundland and Labrador, where they stayed for 2 6 weeks, before commencing their eastward return journey, which often took them into the Greenland Straight and Icelandic waters, where they spent the rest of the winter along with Skomer birds before returning to their nesting colony (Jessopp et al., 2013). Overall, Irish birds travelled further east than Skomer birds. In contrast, Puffins from the Isle of May in southeast Scotland headed north to

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winter off northwest Scotland and in the North Sea, while some then veered west in the eastern North Atlantic (Harris et al., 2010). So birds from different colonies around the British Isles, only a few hundred kilometre apart on overland distances, headed in various directions after breeding, and ended up in largely different wintering areas, reached by taking different routes. Again, individuals took similar routes in different years. As also shown by ringing and tracking studies, Northern Fulmars from both North America and Europe also mingle in the North Atlantic in winter, occurring anywhere from the latitude of southern Britain north to the ice. Nevertheless, birds from high arctic Canada seemed to concentrate in late winter in the Labrador Sea (Mallory et al., 2008), and the European birds east of the Mid-Atlantic Ridge (Wernham et al., 2002). For the most northerly breeding birds, these areas lie in lower latitudes than their nesting areas, while for the most southerly nesting birds they lie in higher latitudes. So birds from different nesting colonies again approached their wintering areas from a wide range of directions. Some of the pelagic species that have been studied by tracking (Fulmars, Black-legged Kittiwakes, Common Murres, Thick-billed Murres (Uria lomvia), Little Auks, Atlantic Puffin,) had on average 3 4 migration phases and 2 3 distinct stationary phases during their non-breeding period (Ame´lineau et al., 2021). They all fed during their movement phases as well as during their ‘sedentary’ phases. In none of these species are the birds from different colonies likely to be genetically distinct from one another, because birds hatched in one colony may breed in another, ensuring continual gene flow between them (Chapter 19). These birds seem not, then, to be migrating on narrow inherited migration directions, as many landbirds do (Chapter 10). Their migration direction depends on the location of the colony with respect to the wintering area.

Migrations to higher latitudes in winter Some other seabirds from temperate regions winter partly at higher latitudes than their nesting areas. This applied to Pigeon Guillemots (Cepphus columba) breeding on the Farallon Islands off California which migrated entirely northward after breeding to winter off British Columbia and southeast Alaska, returning southward in spring (Johns & Warzybok, 2022). It also applied to some of the Atlantic Puffins, Common Guillemots, Black-legged Kittiwakes and Northern Fulmars mentioned above, which winter in the North Atlantic, and to Balearic Shearwaters (Puffinus mauretanicus) which, having bred on Mediterranean Islands, travelled westward into the Atlantic, and then northward to productive waters off Portugal and Britany (Guilford et al., 2012). In the Southern Hemisphere, Common Diving Petrels (Pelecanoides urinatrix) from two New Zealand colonies moved after breeding some 3000 5000 km southeast to highly productive waters along the Antarctic Polar Front, a shift to higher latitudes where they spent around 3 months before returning on a longer more meandering route to their colonies (Rayner et al., 2017). In shorter movements, Fiordland Penguins (Eudyptes pachyrhynchus) from New Zealand travelled 1500 2000 km after breeding to beyond the Sub-Antarctic Front, a southwest movement to higher latitudes (Thiebot et al., 2020). Other species, such as the Brown Pelican (Pelecanus occidentalis) off western North America and the Bonin Petrel (Pterodroma hypoleuca) of northern Pacific Islands, also migrate to higher latitudes after breeding, but these species nest in winter, so their movements coincide with those of other birds migrating north in spring, in their case to breed.

Migrations to east or west Some seabirds move directly east or west on their journeys, remaining throughout at similar latitude within the same marine zone. Such migrations occur in both hemispheres, but seem especially prevalent in the Southern Ocean, beyond the latitude at which continental land areas get in the way. For example several species that nest on or near New Zealand, such as Cook’s Petrel (Pterodroma cookii), Chatham Petrel (Pterodroma axillaris) and Westland Petrel (Procellaria westlandica), all make long eastward post-breeding migrations (Rayner et al., 2011; Rayner et al., 2012; Landers et al., 2011). Slender-billed Prions (Pachyptila belcheri) have two major breeding colonies at similar latitude more than 8000 km apart, on the Falkland Islands in the south-western Atlantic (60 W) and in the Kerguelen Archipelago in the Indian Ocean (70 E). After breeding, the Falkland birds travelled eastward and the Kerguelen birds westward, ending up in an overlapping non-breeding area about mid-way between the two colonies, at the Antarctic Polar Front in the Southern Ocean (Figure 8.3; Quillfeldt et al., 2015). In addition, Macaroni Penguins (Eudyptes chrysolophus) nesting on the Kerguelen Islands migrated eastward after breeding, spending about 6 months at sea, mostly within the same latitudinal belt (47 49 S) around the Antarctic Polar Front (Bost et al., 2009). Other seabirds nesting on islands in the Indian Ocean provide other examples of east west migrations.

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In the northern hemisphere, the Ancient Murrelet (Synthliboramphus antiquus) makes a mainly east west transoceanic migration after breeding off western Canada, but with a northward diversion (Gaston et al., 2017). It winters in northern Asian waters, and its round trip of 8000 km represents the longest known migration of any auk, almost all on a predominantly east west axis (Gaston et al., 2017). East west movements could occur in some seabirds because most of the boundaries between land and sea (the edges of the main land masses) run roughly north south, so to reach the open sea, pelagic species would need to have an east or west component in their migrations. However, many of the species known to show direct east west movements nest on oceanic islands, from which movements could theoretically occur in any direction. The most striking examples include albatrosses and other species nesting on islands in the Southern Ocean (Birdlife International, 2004). A common feature of east west movements, whether starting on continents or islands, is that they keep birds within the same or adjacent seawater zones, presumably those to which they are best adapted and in which they can obtain their food year-round.

Circumpolar migrations Some species of albatrosses undertake round-the-world journeys, mainly in their non-breeding years separating successive nesting attempts (Figure 8.4). On these journeys, birds keep going in the same direction, while remaining in the same latitudinal belt and the same or adjacent marine zones. The Grey-headed Albatross (Thalassarche chrysostoma)

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FIGURE 8.3 Migration of Skender-billed Prions (Pachyptila belcheri) from the Falkland and Kerguelen Islands, showing east west migration patterns to a shared wintering area (cross-hatched). Compiled from the tracking studies of Quillfeldt et al. (2015). FIGURE 8.4 Circumpolar migration and main foraging areas of a Greyheaded Albatross (Thalassarche chrystostoma) in the 18 months between successive breeding attempts on South Georgia. Modified from Croxall et al. (2005).

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nests on islands in the Southern Ocean between 45 and 55 S. Twelve birds tagged on South Georgia completed at least one circumpolar trip, while three of them undertook two such trips during their non-breeding period, all the time travelling eastward, propelled by the westerlies that blew strongly at those latitudes (Croxall et al., 2005). The fastest recorded round-the-world trip took 46 days and included spells averaging 950 km per day. The shortest possible route would have been 22,000 km but the bird flew a much more sinuous route. But not all Grey-headed Albatrosses from South Georgia made round-the-world journeys: some remained in the southwest Atlantic throughout, while others headed east to spend the southern winter in the southwest Indian Ocean. These three types of behaviour occurred among birds breeding on the same island. Circumpolar migrations have also been recorded from Wandering Albatrosses nesting on the Kerguelen Islands which, during their non-breeding years, circumnavigated Antarctica two or three times, covering more than 120,000 km in a single non-breeding period (Weimerskirch et al., 2015). Other circumpolar migrations have been recorded from Northern Royal Albatrosses (Diomedea sandfordi), which nest on New Zealand and the Chatham Islands, and on their eastward journeys remained within latitudes 30 45 S (Nicholls et al., 1994; Birdlife International, 2004). Similar round-the-world journeys at equivalent latitudes in the northern hemisphere are of course precluded in any pelagic bird by the land masses.

MIGRATORY STOPOVERS In general, long journeys by seabirds, especially when they begin immediately after breeding, appear not to be preceded by a period of fattening. However, lengthy stopovers were evident in the early stages of the migrations of some longdistance seabirds travelling for part of their route over waters poor in food. Arctic Terns and Manx Shearwaters provide examples, and different species may use different areas depending on their route. Although information on rates of weight gain at stopovers is lacking for seabirds, these pauses in migration seem equivalent to the stopovers of landbirds used for refuelling. Some stopover sites revealed by the behaviour of tracked birds on the open sea were so unexpected that some researchers initially doubted their role as refuelling sites. Apart from refuelling, pelagic birds are apt to stop migrating under strong headwinds often associated with passing weather systems. But some recorded stops clearly outlived the longevity of weather systems and were in any case repeated at roughly the same places in different years of varying weather. The distance of some such stopover sites from land and their partially mobile nature may well have allowed them to go largely unrecognized in the past. For diving species, depth devices have now confirmed that tracked birds were not simply resting on the water or sitting out bad weather but were actively feeding (for Manx Shearwater, see Guilford et al., 2009). One major discovery from tracking studies is a feeding area in the central North Atlantic known as the Evlanov Seamount and Basin, lying around 50 N between Newfoundland and France on the mid-Atlantic Ridge (Figure 8.1). This is an extensive area of marine biodiversity which has emerged as an important foraging area for at least 27 seabird species. More than five million birds are thought to use the area at peak times, including more than two million Little Auks, more than one million Black-legged Kittiwakes and nearly one million Atlantic Puffins (OSPAR undated, Davies et al., 2021). While some seabirds, including Manx Shearwater and Arctic Tern, use the area for stopovers on migration, other species use it as a wintering area (Egevang et al., 2010; Catry et al., 2011a,b; Gilg et al., 2013; Kopp et al., 2011; Seyer et al., 2021). Like many other nutrient-rich areas used by seabirds, the Evlanov Basin is not small, as it covers an area of around 106,000 km2, about 80% as big as England. While many migrating seabirds linger in areas of rich food supplies, others rely on picking up food on route. For example Westland Petrels nesting on the South Island of New Zealand migrated eastward to wintering areas off Chile and Argentina (Landers et al., 2011). This 7000 km journey averaged only 6 days, and the return in April (against the wind) 10 days. During their two journeys, these birds spent a mere 10% and 17% of their time on the water, with no evidence of lengthy stopovers. They must either have completed the journey without feeding or picked up food on the wing or during their brief stops. Similarly, migrating Cory’s Shearwaters (Calonectris borealis) in the Atlantic adopted a ‘fly-and-forage’ strategy (Dias et al., 2012). In flying by dynamic soaring, these shearwaters attained high overall migration speeds and were able to travel thousands of kilometres without making refuelling stops and, apparently, without noticeable pre-migratory fattening, at least in spring.

LONG-DISTANCE FORAGING TRIPS An important difference between most pelagic birds and most landbirds concerns the distances travelled from the nest for food. Most landbirds, when breeding, obtain most of their food from within restricted territories or travel at most a

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few kilometres from the nest (some vultures and others excepted). But some pelagic seabirds regularly travel hundreds or thousands of kilometres from the nest, distances in some species as long as their migrations. To put these distances in context, take a small insectivorous passerine which might obtain all its food in the breeding season within about 50 m of its nest, but then fly on a migratory journey in some species extending over more than 5000 km. In such a species, the migratory distance is 100,000 times (or five orders of magnitude) longer than the maximum likely foraging distance. Migration is clearly a totally different undertaking for such birds than it is for many pelagic seabirds, some of which can fly more than 5000 km on individual foraging trips from the nesting colony (see below). Long-distance foraging is necessary in some seabirds because suitable nesting places may lie far from good feeding areas. In addition, the nesting places sometimes hold enormous concentrations of birds which, to gain enough food, must range over huge sea areas. Typically, in the seabirds that feed at long distances, one parent forages away for periods of days or weeks at a time, while the other stays at the nest until the chick is large enough to be left alone.

The pre-laying exodus Procellariiform birds usually return to their nesting sites early in the season, re-establish ownership and pair bonds, and then leave on a ‘pre-laying exodus’ to accumulate elsewhere the body reserves necessary for egg production by the females and the first major incubation stint by the males. Body reserves that the birds may have on first arrival at the colony have largely gone before the time of egg-laying, making it necessary for both sexes to accumulate fresh reserves, often obtained at hundreds or thousands of kilometres from the nesting colonies. At that time of year, it may in many places be more efficient to fly long distances to rich feeding areas than to attempt to accumulate reserves nearby. White-chinned Petrels (Procellaria aequinoctialis) nesting on South Georgia flew more than 2000 km northwest to the Patagonian Shelf off central Argentina, which is also a major wintering area for the same birds (Phillips et al., 2006a,b). In many species, males and females depart at about the same time, leading to a mass exodus from the colony which virtually empties in the run-up to laying as noted, for example in the Short-tailed Shearwater in Australia (Brooke, 2018). In some species, males and females may head to different sea areas, even though both are absent from the colony for a similar period. Murphy’s Petrels (Pterodroma ultima) on Henderson Island in the South Pacific had a pre-laying exodus lasting about 6 weeks. Birds headed southwest, but males travelled a greater average maximum distance from the colony (3800 km) than females (2900 km) (Brooke, 2018). Elsewhere in the Pacific, Chatham Petrels showed a similar difference, the males travelling, on average, around 3700 km and the females around 2300 km (Rayner et al., 2012). It is not clear why, in these and other Pterodroma petrels, males should travel further than females. In other species, such as the Streaked Shearwater (Calonectris leucomelas), both sexes may travel long distances, but females stay away longer than males (Yamamoto et al., 2011). In yet other species, long journeys are made mainly by the females, while the males stay nearer the nest site which they may continue to visit at night. Among Manx Shearwaters nesting on Skomer Island males tended to remain within 300 km of the colony, a distance compatible with their return to land on most nights, while the females went further, some reaching more than 1000 km from the colony (Perrins & Brooke, 1976; Guilford et al., 2009). Time away from the nest in the pre-lay period thus varies up to several weeks, depending on the species, sex and distances involved. Nevertheless, it is amazing that birds may return from spring migration, remain a few weeks in their nesting places, and then migrate in some cases back to wintering areas, before returning to lay an egg and proceed with a nesting attempt. Although widely known among procellariforms, long pre-laying movements also occur in some other pelagic seabirds, including the Brown Skua (Stercorarius antarcticus), Black-legged Kittiwake and Sooty Tern (Onychoprion fuscatus) (Phillips et al., 2007; Bogdanova et al., 2011; Jaeger et al., 2017). In each case, such movements may occur chiefly among individuals nesting in areas remote from rich feeding grounds. The point in returning earlier to the nest site is presumably to re-establish ownership in what is often a highly competitive situation.

Foraging flights during incubation and chick care In procellariform birds, once the single egg has been laid, males take the first incubation stint, lasting days or weeks depending on species, while females go to feed. Thereafter, the partners take turns to tend the egg or chick while the other forages. Once the chick is well grown, both sexes can be away foraging at the same time. Many other seabirds also show this pattern, the period away depending on how close to the colony food is obtained, leading to foraging absences of up to a few hours in some gulls to weeks in some large albatrosses and penguins. At the extreme, some pelagic species forage at enormous distances, ranging over wide areas of sea, and spending 1 3 weeks over each trip, before returning with replenished body reserves and food for the chick. However, they tend to make longer journeys

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during the incubation and late chick stages than in the hatching and early chick stages, when the young need guarding and brooding and more frequent meals. For example early in incubation, Wandering Albatrosses nesting on the Crozet Islands flew an average of 5991 km during each foraging trip, ranging as far as 2602 km from the colony, but towards the end of incubation and in the early nestling periods, distances were reduced to mostly less than 400 km from the colony. When the young were large enough to be left, both adults flew further afield, reaching 1534 km from the colony and covering an average of 6091 km on each foraging trip, during an average absence of 11.6 days (Weimerskirch et al., 1993). Other procellariform species have shown similar seasonal trends in flight distances, feeding nearer the colony in the late incubation and early nesting periods (Phillips et al., 2004a,b; Phalan et al., 2007). Many long-distance foragers fly to feed at latitudes higher than the nesting colony, probably because food is more abundant there. This holds for many species which nest on islands in the Southern Ocean and fly south to Antarctic waters to obtain at least part of their food. It is not only flying seabirds that forage far from their colonies but also some penguins, which must walk or swim, giving them some of the longest absences during incubation. In Emperor Penguins (Aptenodytes forsteri) nesting in winter on the Antarctic sea ice, the males are responsible for the 64-day incubation period, huddling tightly together in temperatures down to -40 C. During this time, after laying their eggs, the females go to sea, and must often walk more than 100 km (maximum recorded 296 km; Ancel et al., 1992) to reach open water provided by polynyas. If they nested nearer to the ice edge and potential feeding areas, the ice would melt in spring before the young were ready to leave (Ancel et al., 1992; Williams, 1995). In another study, tracked females took 8 days to reach open water, walking and tobogganing for 80 km over the ice. They then spent 50 60 days foraging at sea within 100 km of the colony (though roosting in huddles on the ice at night), and another 4 days to return across the shrinking ice sheet to the colony (Kirkwood & Robertson, 1997). The females then took over chick care for 3 4 weeks, while the males left to feed. Later in the breeding cycle, most foraging is probably done at less than 500 km from the colony, but in light pack ice some birds travelled as far as 900 km from the colony. This penguin is extreme in these respects. Among other penguins in the pre-laying and incubation periods, inshore feeding species, such as the Yellow-eyed (Megadyptes antipodes) and Gentoo Penguins (Pygoscelis papua), usually fast ashore for periods of less than 3 days at a time, which implies a more limited feeding range. In contrast, long-distance foragers, such as Ade´lie (Pygoscelis adeliae) and King Penguins (Aptenodytes patagonicus), regularly remain ashore without feeding for 25 40 days at a time (Croxall & Davis, 1999). King Penguins feeding chicks on the Crozet Islands were recorded swimming over 1600 km to foraging areas at 8 higher latitude in winter on the margin of the pack ice, giving round trips exceeding 4000 km (Bost et al., 2004). These figures provide some idea of the distances reached from the colonies, but birds seldom took direct outward routes, and the total travel distances of some foraging birds were much greater than expected from straight-line distances. Another notable finding evident in many species was that, during the breeding season, long foraging trips were mostly to higher latitudes. In the northern hemisphere, Laysan Albatrosses (Phoebastria immuntablis) nesting on Hawaii flew more than 2000 km as far north as the Aleutian Islands and Gulf of Alaska (Ferna´ndez et al., 2001), while in the southern hemisphere, Short-tailed Shearwaters nesting off southern Australia flew more than 3000 km to forage in Antarctic waters, many making round trips exceeding 10,000 km. One bird in the chick-rearing period took 32 days over a foraging trip of 15,220 km (Klomp & Schultz, 2000; Einoder et al., 2011). Such long flights from the nest have no parallel among nesting landbirds, but distances of more than 100 km have occasionally been recorded from some colonial Gyps vultures, Apus swifts and others.

FATTENING OF CHICKS In most bird species, fattening for the first migration does not begin until after the young are fully grown and able to feed themselves efficiently (Chapter 5). But in some species, the young fatten while in the nest, on food provided by their parents, and migrate independently a few days after fledging. They include many seabirds, notably various procellariforms, in which the nestlings reach peak weights much in excess of the adults. Thereafter, they receive little or no additional food from their parents and lose weight until they leave the nest. The young continue to grow their feathers but are still extremely fat at the time of their first flight. Although this fattening in seabird nestlings has long been recognized, it has usually been regarded as an insurance against difficult times until the bird learns to feed itself. However, in many such species, the young set off a few days after fledging on long journeys for which fuel reserves are almost certainly needed. At their peak, young Manx Shearwaters weigh around 20% more than the adults and are extremely fat, from which point they are fed at a much reduced rate. After about 10 more days, the young leave for the sea and thereafter have no

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further contact with their parents (Harris, 1966). Some 36 hours after leaving Skokholm Island off Wales, some ringed young were recovered several hundred kilometres to the south, in the Bay of Biscay. Within 6 weeks, many others were recovered in the seas off Brazil, more than 9000 km across the Atlantic (Perrins et al., 1973). Such flights almost certainly required substantial fuel reserves, for they left little time for feeding by such inexperienced birds. The young would gain obvious advantage in being able to fly directly to the wintering area without having to spend time in a perhaps fruitless search for food on the way. Judging from the estimated fat content of the young and the likely energy costs of their migration, ‘it seems just possible that fat birds could make the 9000 to 10,000 km flight on their reserves’ (Perrins et al., 1973). Like petrels, young Northern Gannets become obese before fledging, reaching around 30% heavier than adults and carrying around 1 kg of fat. The young leave the nest before their flight feathers are fully grown but can glide down to the sea, soon reaching distances of 3 5 km from the colony (Wanless & Okill, 1994). Once on the water, they seem unable to take off again, at least for several days, by which time they have lost further weight and their flight feathers are better grown. They swim long distances in this period, and once they become airborne they can travel even longer distances. Only at some later stage do they begin to hunt for themselves using the aerial diving technique characteristic of the species. Six young Gannets that were caught on the sea in the flightless period were recovered 10 16 days later at distances of 394 2483 km (Wanless & Okill, 1994). They had mean travel rates of 15.1 155.2 km/day, similar to those of many landbirds on migration (Chapter 9). Again, the birds were unlikely to have covered the longer of these distances without fuel reserves.

PRE-BREEDING YEARS Seabirds tend to live a long time and have prolonged periods of immaturity. None breed at less than 2 years old, and some albatrosses do not breed until they are 10 or older (Brooke, 2018). Their populations therefore often contain large numbers of immatures, sometimes comprising more than half the total population of full-grown birds (Klomp & Furness, 1992). The fact that nesting adults must be based in fixed colonies for part of each year restricts their distributions then, compared with immatures which can be much more widely or differently distributed. This segregation of age groups, with the young often foraging in poorer waters, could result from the pressure of competition from experienced adults. Species such as gulls and cormorants base themselves on land during their pre-breeding years, but procellariforms and others can spend several years at sea without ever coming to land. As they mature, they begin to visit nesting colonies and eventually settle on one as the future nesting place. Visits to multiple colonies by pre-breeding birds have long been known from ringing. Because the pre-breeding period of seabirds lasts for several years, this is longer than current tracking devices can operate, stay attached and store information. However, several researchers have managed to attach devices to immature seabirds from the stage when they first set foot in a nesting colony. Some immature Northern Gannets on Grassholm Island off south Wales were caught and fitted with satellite tags (Votier et al., 2011). In general, these immatures spent more time away from the colony and ranged over wider areas than did breeding adults which were also tagged. The average out-and-back journey of an adult was 370 km, whereas immatures travelled three times that distance and varied considerably in their tracks. Some visited other Gannet colonies up to hundreds of kilometres away, but the 25 tracked adults visited only their own colony. Cory’s Shearwaters tagged on Selvagem Grande Island off Morocco provided further information on the behaviour of birds aged 4 9 years (Campioni et al., 2020). Migratory timings and destinations changed progressively through the different age groups. Birds gradually advanced their spring departure dates from non-breeding areas and reduced their travel times, which resulted in a sequential arrival at the colony of the various age groups, and a progressive shortening of their periods in nonbreeding areas. Immatures also changed gradually from a more exploratory to a more conservative way of exploiting resources, reducing both their year-round spatial distribution and the total distance travelled, becoming more consistent in their year-toyear behaviour as adults. All immatures migrated across the equator, compared with only 17% of adults, most of which remained in the North Atlantic year-round. Lastly, during the breeding season, immatures were widely dispersed through the North Atlantic, while breeding adults were concentrated nearer to colonies. In this species, therefore, refinement of migratory behaviour and year-round distribution changed progressively according to age and experience. Among Manx Shearwaters based on Skomer Island, immatures and adults fed in mainly different areas from one another and also showed different foraging efficiencies (Fayet et al., 2015). Immatures made shorter trips than adults, both in terms of duration and distance from the colony (over 200 km for adults and an average of 135 km for immatures). The two age groups also took different directions, with the immatures concentrating south of Skomer and the adults further west in more productive waters. The pattern of GPS fixes was used to calculate how long on each trip a bird was feeding, and by re-catching the bird when it returned to land, its rate of weight gain could be calculated. This rate was significantly less for immatures, confirming they were less efficient foragers, even when feeding away from

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adults. These and other studies of immature seabirds pointed to the pre-breeding years being a time of exploration and learning, particularly the skills of finding food-rich areas and food collection, a process of improvement which probably continues well beyond the age of first breeding.

NAVIGATIONAL ACHIEVEMENTS Pelagic seabirds travel over vast stretches of open sea, yet they can return unerringly to their tiny nesting islands after long migrations or after long-distance foraging trips. Young birds can even return to their nesting islands after several years at sea when they finally reach breeding age, some 3 10 years later, depending on species. In tracking studies, adult Wandering Albatrosses left their nesting islands on foraging flights that took them over distances of several thousand kilometres (Weimerskirch et al., 1993, 1994). After wandering in all directions for several days, individuals invariably returned on a straight line to their breeding island too far away to be visible (Weimerskirch et al., 1993). Penguins are similarly efficient oceanic navigators, even though they remain on and below the water surface while at sea. The King Penguins that travelled up to 1500 km from their nesting places over total journey lengths up to 4000 km also returned on a straight-line course to the colony (Jouventin et al., 1994). Similarly, Emperor Penguins walked in a straight line over featureless sea ice for distances sometimes exceeding 100 km between open water and their nesting areas (Ancel et al., 1992). The fact that all these tracked birds, after wandering widely in various directions, took a straight course home implies that at any one time, they knew exactly where they were with respect to where they needed to go next (usually their nesting colony). Of course, the same efficiency of return from foraging trips might apply to any nesting bird, but the scale of movement is much greater in pelagic seabirds, and over most of the route rules out any possibility of relying on familiar landscape features (for further discussion of seabird navigation, see Chapters 9 and 10).

CONCLUSIONS Ring recoveries can give misleading information in the migrations and foraging areas of seabirds. This is because dead birds can be transported long distances in fishing nets or water currents, and in theory could be washed up on beaches well outside the normal range of their species. Nowadays, with the advent of reliable tracking devices, not only can transoceanic flights be tracked with startling accuracy but it is also possible to tell, within metres, the location of a seabird at any one time, whether it is flying or swimming, at the surface or underwater, or how deep it is diving. It is also possible to monitor a bird’s heart rate and thereby gain an idea of the relative energy costs of different activities. During their pre-breeding years, pelagic seabirds typically wander widely. They may remain in their non-breeding range for the whole of the first year or beyond, or at least for longer periods each year than breeders, exploring many different areas, and then migrating to breeding areas in later years, using mainly different foraging areas from breeders. In some species, individuals initially explore several nesting colonies before they eventually settle to breed. In some species, males and females also forage in mainly different areas from one another, at least for parts of the annual cycle. One of the most striking findings of recent years is that many seabirds migrate to higher latitudes for their nonbreeding period or directly east west or west east, rather than almost universally to lower latitudes, as in landbirds. This could be largely attributed to cold waters being generally more productive than warm ones and to some of the richest marine areas being at high latitudes, yet remaining open in winter. Another striking finding is that some pelagic birds travel huge distances not only on their migrations but also on their foraging flights from nesting colonies. Many different procellariform birds regularly forage at distances of exceeding 2000 km from their nesting colonies in the pre-laying, incubation or late nestling stages, with round-trip distances of more than 15,000 km recorded. Distances out from colonies are similar to those travelled by some of these same species on migration, and much greater than those covered by the majority of landbirds on migration. Some foodcollecting trips are equivalent to flights across the North Atlantic or from Europe to Africa, taking days or weeks to complete. Adults returning from such flights come laden with food for the chick and may also have restored their own the body reserves lost over preceding periods at the nest. Birds can presumably achieve such flights only because they have strong winds constantly available, and complete mastery over their use, making their flights much quicker and cheaper than possible over land. Both adults and young can also withstand long periods of food privation. Tracking studies have further highlighted the extent to which seabirds make use of areas of high productivity as stopover, breeding or wintering areas. Most of the nutrient-rich areas used by seabirds lie beside continents or other land areas and have long been known as productive fisheries. But others lie far from land, forming under the influence of sea-bed contours, and were previously unknown at least to seabird biologists. Each pelagic species may use many such areas during the course of its annual wanderings. The same areas may be used by many different species at the

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same time, including some from far-away nesting places, although birds from northern and southern hemisphere colonies are present in abundance at mainly different seasons. Individual migratory pelagic birds seem familiar with several areas of high productivity which they presumably discover during their early years of wandering. The assumption that many pelagic seabirds do not accumulate migratory fat has not been properly tested because it needs the hands-on study of birds at sea. It is probably erroneous, for the young of procellariforms, gannets and possibly other species accumulate what could be regarded as migratory fat while in the nest, and set off on migration soon after leaving the nest. In addition, the adults of many species remain at stopover areas long enough to accumulate substantial body reserves.

SUMMARY The movements of seabirds are ultimately dependent on the high productivity of specific sea areas, some of which lie at high latitudes. Winds play a major role in the migrations of some pelagic birds which, because of their still-wing flight mode, can travel long distances rapidly at little cost. The patterns of seabird movements from breeding to non-breeding areas include (1) direct movements to lower latitudes within hemispheres, as in most landbirds; (2) direct movements between hemispheres, as in some landbirds; (3) figure-8 movements between hemispheres in some pelagic species; (4) dispersive movements in various directions from nesting colonies; (5) movements to higher latitudes, in contrast to most landbirds; (6) east west movements within the same oceanic zones; and (7) circumpolar migrations in the southern hemisphere. The wider spread of migratory directions shown by dispersive seabirds stems from (1) birds from different colonies taking different (sometimes opposing) directions, partly according to the distribution of land areas; (2) birds from the same colony taking markedly different directions from one another. Frequent movements also occur during the course of a winter, often involving marked changes of directions. All these features can be seen in Atlantic Puffins and other pelagic species wintering in the North Atlantic. Pelagic seabirds also differ from landbirds in their greater reliance on winds as an efficient means of long-distance travel. This behaviour more often takes seabirds on more round-about routes than landbirds including, in some species, long figure-8 migrations between hemispheres. The still-wing flight modes in strong winds enable procellariform birds to cover long distances on very little energy. Learning seems to be important in the honing of migration behaviour in pelagic seabirds, as shown by changes that occur during the lifetimes of individuals. This process is facilitated by the longevity of most seabirds, and the use of the pre-breeding years as a period of exploration, with immature individuals ranging over much wider areas than shown by adults of their species or by most landbirds that have been studied. Some procellariform seabirds also make long foraging flights from their nesting colonies, covering hundreds or thousands of kilometres. The young of such species are able to survive long fasts between feeds. Through food provided by their parents, such young also accumulate large reserves of body fat before setting off on their first migration, immediately after leaving their nests. The use of tracking devices on pelagic seabirds has also helped to identify major foraging areas far from land, some of which were previously unknown to ornithologists.

REFERENCES Alerstam, T., Ba¨ckman, J., Gronroos, J., Olofsson, P. & Strandberg, R. (2019). Hypotheses and tracking results about the longest migration: the case of the Arctic Tern. Ecol. Evol. 9 (17): 9511 31. Ame´lineau, F., Merkel, B., Tarroux, A., Descamps, S. Anker-Nilssen, T. et al. (2021). Comparative study of migration patterns of six pelagic seabird species. Mar. Ecol. Prog. Ser. 676: 127 44. Ancel, A., Kooyman, G. L., Ponganis, P. J., Gendner, J. P. Lignon, J. et al. (1992). Foraging behavior of Emperor Penguins as a resource detector in winter and summer. Nature 360: 336 9. Balmer, D. E., Gillings, S., Caffrey, B. J., Swann, R. L., Downie, I. S. & Fuller, R. J. (2013). Bird atlas 2007-11: the breeding and wintering birds of Britain and Ireland. Thetford, BTO Books. Bevan, R. M., Butler, P. J., Woakes, A. J. & Prince, P. A. (1995). The energy expenditure of free-ranging Black-browed Albatrosses. Phil. Trans. R. Soc. B 350: 119 31.

BirdLife International. (2004). Tracking ocean wanderers: the global distribution of albatrosses and petrels. Results from the Global Procellariiform Tracking Workshop, 1 5 September, 2003, Gordon’s Bay, South Africa. Cambridge, BirdLife International. Bogdanova, M. I., Daunt, F., Newell, M., Phillips, R. A. Harris, M. P. et al. (2011). Seasonal interactions in the Black-legged Kittiwake, Rissa tridactyla: links between breeding performance and winter distribution. Proc. R. Soc. B 278: 2412 18. Bost, C. A., Charrassin, J. B., Clerquin, Y., Ropert-Coudert, Y. & Le Mayo, Y. (2004). Exploitation of distant marginal ice zones by King Penguins during winter. Mar. Ecol. Prog. Ser. 283: 293 7. Bost, C. A., Thiebot, J. B., Pinaud, D., Cherel, Y. & Trathan, P. N. (2009). Where do penguins go during the inter-breeding period? Using geolocation to track the winter dispersion of the Macaroni Penguin. Biol. Lett 5: 473 6.

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Brooke, M. (2018). Far from land. Princeton, University Press. Campioni, L., Dias, M. P. & Granadeiro, J. P. (2020). An ontogenetic perspective on migratory strategy of a long-lived pelagic seabird: timings and destinations change progressively during maturation. J. Anim. Ecol. 89: 29 43. Carey, M. J., Phillips, R. A., Silk, J. R. D. & Shaffer, S. A. (2014). Trans-equatorial migration of Short-tailed Shearwaters revealed by geolocators. Emu 114: 352 9. Catry, P., Dias, M. P., Catry, T., Afanasyev, V. Fox, J. W. et al. (2011a). Individual variation in migratory movements and winter behaviour of Iberian Lesser Kestrels Falco naumanni revealed by geolocators. Ibis 153: 154 64. Catry, P., Dias, M. P., Phillips, R. A. & Granadeiro, J. P. (2011b). Different means to the same end: long-distance migrant seabirds from two colonies differ in behaviour, despite common wintering grounds. PLOS ONE 6: e26079. Croxall, J. P. & Davis, L. S. (1999). Penguins: paradoxes and patterns. Marine Ornithol 27: 1 12. Croxall, J. P., Silk, J. R. D., Phillips, R. A., Afanasyev, V. & Briggs, D. R. (2005). Global circumnavigations: tracking year-round ranges of nonbreeding albatrosses. Science 307: 249 50. Davies, T. E., Carneiro, A. P. B., Tarzia, M., Wakefield, E. Hennicke, J. C. et al. (2021). Multispecies tracking reveals a major seabird hot spot in the North Atlantic. Conserv. Lett 14, e12824. Dias, M. P., Granadeiro, J. P. & Catry, P. (2012). Do seabirds differ from other migrants in their travel arrangements? On route strategies of Cory’s Shearwater during its trans-equatorial journey. PLOS ONE 7 (11): e49376. Egevang, C., Stenhouse, I. J., Phillips, R. A., Petersen, A., Fox, J. W. & Silk, J. R. D. (2010). Tracking of Arctic terns Sterna paradisaea reveals longest animal migration. Proc. Natl Acad. Sci. U S A 107: 2078 81. Einoder, L. D., Page, B., Goldsworthy, S. D., De Little, S. C. & Bradshaw, C. J. A. (2011). Exploitation of distant Antarctic waters and close neritic waters by Short-tailed Shearwaters breeding in South Australia. Austral. Ecol. 36: 461 75. Fayet, A. L., Freeman, R., Shoji, A., Padget, O., Perrins, C. M. & Guilford, T. (2015). Lower foraging efficiency in immatures drives spatial segregation with breeding adults in a long-lived seabird. Anim. Behav. 110: 79 89. Fayet, A. L., Freeman, R., Shoji, A., Boyle, D. Kirk, H. L. et al. (2016). Drivers and fitness consequences of dispersive migration in a pelagic seabird. Behav. Ecol. 27: 1061 72. Ferna´ndez, P., Anderson, D. J., Sievert, P. & Huyvaert, K. P. (2001). Foraging destinations of three low-latitude albatross species. J. Zool. 254: 391 404. Fijn, R. C., Hiemstra, D., Phillips, R. A. & van der Winden, J. (2013). Arctic Terns Sterna paradisaea from the Netherlands migrate record distances across three oceans to Wilkes Land, east Antarctica. Ardea 101: 3 12. Freeman, R., Dean, D., Kirk, H., Leonard, K. Phillips, R. A. et al. (2013). Predictive ethinformatics reveals the complex migratory behavior of a pelagic seabird, the Manx Shearwater. J. R. Soc Interface 10: 20130279. Gaston, A. J., Hashimoto, Y. & Wilson, L. (2017). Post-breeding movements of ancient murrelet Synthliboramphus antiquus family groups, subsequent migration of adults and implications for management. PLOS ONE 12 (2): e0171726. Gilg, O., Moe, B., Hanssen, S. A., Schmidt, M. N. Sittler, B. et al. (2013). Trans-equatorial migration routes, staging sites, and

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wintering areas of a high-arctic avian predator: the Long-tailed Skua (Stercoraruius longicaudus). PLOS ONE 8: e64614. Gilg, O., Stro¨m, H., Aebischer, A. & Gavrilo, M. V. (2010). Postbreeding movements of northeast Atlantic Ivory Gull Pagophila eburnea populations. J. Avian Biol. 41: 532 42. ´ . M., Fox, J. W., Afanasyev, V., Gonza´lez-Solı´s, J., Felicı´simo, A Kolbeinsson, Y. & Mun˜oz, J. (2009). Influence of sea surface winds on shearwater migration detours. Mar. Ecol. Prog. Ser. 391: 221 30. Guilford, T. C., Meade, J., Willis, J., Phillips, R. A. Boyle, D. et al. (2009). Migration and stopover in a small pelagic seabird, the Manx Shearwater Puffinus puffinus: insights from machine learning. Proc. R. Soc. B 276: 1215 23. Guilford, T., Freeman, R., Boyle, D., Dean, B., Kirk, H. Phillips, R. et al. (2011). A dispersive migration in the Atlantic Puffin and its implications for migratory navigation. PLOS ONE 6: e21336. Guilford, T., Wynn, R., McMinn, M., Rodriguez, A. Fayet, A. et al. (2012). Geolocators reveal migration and pre-breeding behaviour of the critically endangered Balearcic Shearwater Puffinus mauretanicus. PLOS ONE 7: e33753. Harris, M. P. (1966). Breeding biology of the Manx Shearwater Puffinus puffinus. Ibis 108: 17 33. Harris, M. P., Daunt, F., Newell, M., Phillips, R. A. & Wanless, S. (2010). Wintering areas of adult Atlantic Puffins Fratercula arctica from a North Sea colony as revealed by geolocation technology. Mar. Biol. 157: 827 36. Hedd, A., Montevecchi, W. A., Otley, H., Phillips, R. A. & Fifield, D. A. (2012). Trans-equatorial migration and habitat use by Sooty Shearwaters Puffinus griseus from the South Atlantic during the nonbreeding season. Mar. Ecol. Prog. Ser. 449: 277 90. Jaeger, A., Feare, C. J., Summers, R. W., Lebarbenchon, C., Larose, C. S. & Le Corre, M. (2017). Geolocation reveals year-round at-sea distribution and activity of a superabundant tropical seabird, the Sooty Tern Onychoprion fuscatus. Front. Mar. Sci.. Available from https://doi.org/10.3389/fmars.2017.00394. Jessopp, M. J., Cronin, M., Doyle, T. K., Wilson, M. McQuattersGollop, A. et al. (2013). Transatlantic migration by post-breeding Puffins: a strategy to exploit a temporarily abundant food resource? Marine Biol 160: 2755 62. Johns, M. E. & Warzybok, P. (2022). Northward migration, moulting locations, and winter residency of California breeding Pigeon Guillemots Cepphus columba. Mar. Ecol. Prog. Ser. 701: 133 43. Jouventin, P., Capdeville, D., Cuenot-Chaillet, F. & Boiteau, C. (1994). Exploitation of pelagic resources by a non-flying seabird: satellite tracking of the King Penguin througholut the breeding cycle. Mar. Prog. Ser. 106: 11 19. Kirkwood, R. & Robertson, G. (1997). The foraging behavior of female Emperor Penguins in winter. Ecol. Monogr. 67: 155 76. Klomp, N. I. & Furness, R. W. (1992). The dispersal and philopatry of Great Skuas from Foula, Shetland. Ringing Migration 13: 73 82. Klomp, N. I. & Schultz, M. A. (2000). Short-tailed shearwaters breeding in Australia forage in Antarctic waters. Mar. Ecol. Prog. Ser. 194: 307 10. Kopp, M., Peter, H.-U., Mustafa, O., Lisovski, S. Ritz, M. S. et al. (2011). South Polar Skuas from a single breeding population overwinter in different oceans though show similar migration patterns. Mar. Ecol. Prog. Ser. 435: 263 7. Landers, T. J., Rayner, M. J., Phillips, R. A. & Hauber, M. E. (2011). Dynamics of seasonal movements by a trans-Pacific migrant, the Westland Petrel Procellaria westlandica. Condor 113: 71 9.

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Mallory, M. L., Akearok, J. A., Edwards, D. B., O’Donovan, K. & Gilbert, C. D. (2008). Autumn migration and wintering of Northern Fulmars (Fulmarus glacialis) from the Canadian high Arctic. Polar Biol 31: 745 50. Matfrei, M., Davis, S. E. & Mallory, M. L. (2015). Confirmation of a wintering ground of Ross’s Gull Rhodostethia rosea in the northern Labrador Sea. Ibis 152: 642 7. McKnight, A., Allyn, A. J., Duffy, D. C. & Irons, D. B. (2013). ‘Stepping stone’ pattern in Pacific Arctic Tern migration reveals the importance of upwelling areas. Mar. Ecol. Prog. Ser. 491: 253 64. Newton, I. (2003). The Speciation and biogeography of birds. London, Academic Press. Nicholls, D. G., Murray, M. D. & Robertson, C. J. R. (1994). Oceanic flights of the Northern Royal Albatross Diomedea epomophora sanfordi using satellite telemetry. Corella 18: 50 2. Paiva, V. H., Guilford, T., Meade, J., Geraldes, P., Ramos, J. A. & Garthe, S. (2010). Flight dynamics of Cory’s shearwater foraging in a coastal environment. Zoology 113: 47 56. Perrins, C. M. & Brooke, M. d L. (1976). Manx Shearwaters in the Bay of Biscay. Bird Study 23: 295 300. Perrins, C. M., Harris, M. P. & Britton, C. K. (1973). Survival of Manx Shearwaters Puffinus puffinus. Ibis 115: 535 48. Phalan, B., Phillips, R. A., Silk, J. R. D., Afanasyev, V. Fukuda, A. et al. (2007). Foraging behavior of four albatross species by night and day. Mar. Ecol. Prog. Ser 340: 271 86. Phillips, R. A., Catry, R., Silk, J. R. D., Bearhop, S. McGill, R. et al. (2007). Movements, winter distribution and activity patterns of Falkland and Brown Skuas: insights from loggers and isotopes. Mar. Ecol. Prog. Ser. 345: 2281 91. Phillips, L., Powell, A. N. & Rexstad, E. A. (2006a). Large scale movements and habitat characteristics of King Eiders throughout the non-breeding period. Condor 108: 887 900. Phillips, R. A., Silk, J. R. D., Croxall, J. P. & Afanasyev, V. (2006b). Year-round distribution of White-chinned Petrels from South Georgia: relationships with oceanography and fisheries. Biol. Conserv. 129: 336 47. Phillips, R. A., Silk, J. R. D., Croxall, J. P., Afanasyev, V. & Briggs, D. R. (2004a). Accuracy of geolocation estimates for flying seabirds. Mar. Ecol. Prog. Ser. 266: 265 72. Phillips, R. A., Silk, J. R. D., Phalan, B., Catry, P. & Croxall, J. P. (2004b). Seasonal sexual segregation in two Thalassarche albatross species: competitive exclusion, reproductive role specialization or foraging niche divergence. Proc. R. Soc Lond. B 271: 1283 91. Pu¨tz, K., Schiavini, A., Rey, A. R. & Luthi, B. H. (2007). Winter migration of Magellanic penguins (Spheniscus magellanicus) from the southernmost distributional range. Marine Biol 152: 1227 35. Quillfeldt, P., Cherel, Y., Masello, J. F., Delord, K. McGill, R. A. R. et al. (2015). Half a world apart? Overlaps in nonbreeding distributions of Atlantic and Indian Ocean Thin-billed Prions. PLOS ONE 10: e0125007. Rayner, M. J., Taylor, G. A., Gaskin, C. P. & Dunphy, B. J. (2017). Seasonal activity and unpredicted polar front migration of northern New Zealand Common Diving Petrels (Pelecanopides urinatrix). Emu 117: 290 8. Rayner, M. J., Hauber, M. E., Steeves, T. E., Lawrence, H. A. Thompson, D. R. et al. (2011). Contemporary and historical separation of transequatorial migration between genetically distinct seabird populations. Nature Comm 2: 332.

Rayner, M. J., Taylor, G. A., Gummer, H. D., Phillips, R. A. Sagar, P. et al. (2012). The breeding cycle, year-round distribution and activity patterns of the endangered Chatham Petrel (Pterodroma axillaris). Emu 112: 107 16. Salomonsen, F. (1967). Migratory movements of the Arctic Tern (Sterna paradisaea) Pontoppidan in the southern Ocean. Biol. Medd. Dan. Vid. Selsk 24: 1 42. Seyer, Y., Gauthier, G., Beˆty, J., Therrien, J.-F. & Lecomte, N. (2021). Seasonal variations in migration strategy of a long-distance Arcticbreeding seabird. Mar. Ecol. Prog. Ser. 677: 1 16. Shaffer, S. A., Tremblay, Y., Weimerskirch, H., Scott, D. Thompson, D. R. et al. (2006). Migratory Shearwaters integrate oceanic resources across the Pacific Ocean in an endless summer. Proc. Natl. Acad. Sci. U.S.A. 103: 12799 802. Spencer, N. C., Gilchrist, H. G. & Mallory, M. L. (2014). Annual movement patterns of endangered Ivory Gulls: the importance of sea ice. PLOS ONE 9 (12): e115231. Thiebot, J.-B., Bost, C.-A., Poupart, T. A., Filippi, D. & Waugh, S. M. (2020). Extensive use of the high seas by vulnerable Fiordland Penguins across non-breeding stages. J. Ornithol. 161: 1033 43. Volkov, A. E., Loonen, M. J. J. E., Volkova, E. V. & Denisov, D. A. (2017). New data for Arctic Terns (Sterna paradisea) migration from White Sea (Onega Peninsula). Ornithologia 41: 58 68. Votier, S. C., Grecian, W. J., Patrick, S. & Newton, J. (2011). Intercolony movements, at-sea behavior and foraging in an immature seabird: results from GPS-PPT tracking, radio-tracking and stable isotope analysis. Marine Biol 158: 355 62. Walls, S. S. & Kenward, R. E. (2020). The common buzzard. London, T. & A. D. Poyser. Wanless, S. & Okill, J. D. (1994). Body measurements and flight performance of adult and juvenile Gannets Morus bassanus. Ringing Migration 15: 101 3. Weimerskirch, H., Doncaster, C. P. & Cuenot-Chaillet, F. (1994). Pelagic seabirds and the marine environment: foraging patterns of Wandering Albatrosses in relation to prey availability and distribution. Proc. R. Soc. Lond. B 255: 91 7. Weimerskirch, H., Guionnet, T., Martin, J., Shaffer, S. A. & Costa, D. P. (2000). Fast and fuel efficient? Optimal use of wind by flying albatrosses. Proc. R. Soc. Lond. B 267: 1869 74. Weimerskirch, H., Delord, K., Guitteaud, A., Phillips, R. A. & Pinet, P. (2015). Extreme variation in migration strategies between and within Wandering Albatross populations during their sabbatical year, and their fitness consequences. Sci. Rep. 5: 8853. Weimerskirch, H., Salamolard, M., Sarrazin, F. & Jouventin, P. (1993). Foraging strategy of Wandering Albatrosses through the breeding season: a study using satellite telemetry. Auk 110: 325 42. Wernham, C. V., Toms, M. P., Marchant, J. H., Clark, J. A., Siriwardena, G. M. & Baillie, S. R. (2002). The migration atlas: movements of the birds of Britain and Ireland. London, T. & A. D. Poyser. Williams, T. D. (1995). The penguins. Oxford, University Press. Yamamoto, T., Taklahashi, A., Oka, N., Katsumata, N., Sato, K. & Trathan, P. N. (2011). Foraging areas of Streaked Shearwaters in relation to seasonal changes in the marine environment of Northwestern Pacific: inter-colony and sex-related differences. Mar. Ecol. Prog. Ser. 424: 191 204.

Chapter 9

Speed and duration of migratory journeys

White Storks (Ciconia ciconia) thermal soaring on migration. There must come a point at which the new facts that have been collected are felt to be both too raw and too numerous, and it is at this point that the need for coordinating principles begins to be felt. Charles Elton (1927).

The periods that different birds spend on migration depend partly on features of the birds themselves, but largely on the distances covered and conditions on the route. At one extreme, some birds can complete their journeys in less than a day: for example a radio-tagged Bald Eagle (Haliaeetus leucocephalus) which flew 435 km between its wintering site in Michigan and its nesting place in Ontario (Grubb et al., 1994). At the other extreme, some landbirds take more than 3 months to reach their distant winter quarters, and a similar period to return, so they spend more than half of each year on migration. Long journey times are also shown by some pelagic birds, which have a fixed base only during the breeding season and are effectively on the move for the rest of the year. In many birds, the rate of travel is limited by external conditions, notably the rate at which food can be obtained to fuel the flights, and also the prevailing weather, which could speed or slow the journeys (Chapter 4). Initial information on the speed of migration came from birds ringed and recovered on passage. Such recoveries carried the risk of error because it was seldom known precisely when a ringed bird left one place or arrived in another. The temptation was therefore to use only the fastest records, as an indication of maximum possible migration speeds. Not only did such records then come from extreme individuals but most also covered only a part of a migratory journey. More representative data came from calculating the mean geographical positions of ring recoveries obtained from a defined breeding population at successive dates through a journey. Thus if recoveries of birds already on migration were centred in mid-October at latitude 30 N, say, and those in mid-November due south at latitude 20 N, then an average of 1 month would have been spent on covering the distance spanned by 10 of latitude (1110 km). Similar estimates were made from the dates that particular populations passed through different watch sites or trapping stations along a route. The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00011-7 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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The most reliable data on migration speeds in recent decades have come from individuals tagged with devices that enable them to be tracked over their whole journey. With daily records of location, flight periods can often be separated from stopover periods (but in practice short breaks of a few hours are easily missed). However, such studies usually involve only small numbers of individuals and carry the assumption that migratory behaviour is unaffected by the device (Chapter 2).

THEORETICAL BASIS In addition to empirical studies, attempts have been made to estimate theoretical migration speeds of particular species from knowledge of their likely flight speeds and rates of fuel deposition and use, for migration involves both flying and fuelling periods (Boxes 9.1 and 9.2, Figure 9.1; Alerstam & Lindstro¨m, 1990; Hedenstro¨m & Alerstam, 1998; BOX 9.1 Calculation of theoretical migration speed. From Hedenstro¨m & Alerstam (1998). The speed of migration (Vmigr) is determined by the rate at which fuel is accumulated (Pdep), the flight speed (V) between consecutive stopover sites (which depends on wind conditions and flight mode, etc.), and the flight power (Pflight), the rate at which energy is consumed), according to the following general relationship: V migr 5

V P dep P dep 1 P flight

This equation relates to still-air migration speed, and wind conditions could greatly influence the actual speed. A graphical illustration of this equation is given in Figure 9.1. For soaring flight, the above equation can be used, but replacing the flapping flight speed (V) with the cross-country soaring gliding speed (Vcc). Power consumption in gliding flight is generally assumed to be a constant multiple of the basal metabolic rate (BMR), and consequently migration speed will be directly proportional to the cross-country performance (Vmig ~ Vcc) in soaring migration. The cross-country speed in typical thermal soaring is given as: V cc 5

VVc Vc 2 Vz

where V is the gliding speed between thermals, Vz is the sink speed (negative downwards) and Vc is the climb rate in thermals (Pennycuick, 1972, 1975, 1989).

BOX 9.2 Calculation of theoretical energy and time costs of migration. From Alerstam et al. (2003) Energy costs Generally, if migration is subdivided into periods of movement, interspersed with periods of stopover, the total energy consumption during migration can be written as: ! PD x 11 E5 (9.1) V P dep where P is the power of locomotion (rate of energy consumption), D is the migration distance, V is the flight speed, Pdep is the rate of energy deposition at stopovers and x is the field metabolic rate at stopovers. Eq. (9.1) can be used to compare the total investment in migration among, for example birds of different size and using different modes of flight. The ratio x:Pdep determines the ratio between energy consumed during stopovers and cost of flight, which in a typical passerine bird may be about 2:1 or larger. From Eq. (9.1), it is also evident that minimizing the ratio P:V, a measure closely related to cost of transport, will minimize the energy cost of migration. Time costs Generally, the time required for migration can be written as: ! D P 11 T migr 5 (9.2) V P dep where P, Pdep and V are defined as for Eq. (9.1). The relationship between stopover and transportation time is P/Pdep, which was estimated to be about 7:1 or larger for small birds (Hedenstro¨m & Alerstam, 1998). Given limited time available for migration, Eq. (9.2) indicates that there is a maximum return distance (Dmax) that a bird can achieve. The time needed for migration is reduced by low locomotion cost (P) and high travel speed (V) and fuelling rate (Pdep). Hence, adaptations favouring low energy cost of transport, high rates of fuel deposition, and optimal scheduling of life history events are expected in long-distance migrants.

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FIGURE 9.1 Graphical depiction of how to calculate the theoretical overall migration speed (Vmigr) on the basis of the power required for flight (Pflight), rate of energy deposition at stopovers (Pdep) and flight speed (V). Migration speed is found where a straight line connecting the point on the downward-extended ordinate indicating Pdep to the point in the powerspeed plane (V, Pflight) intersects the speed axis. The migration speed can be calculated according to the equation in Box 9.1. From Hedenstro¨m & Alerstam (1998).

Flight power

Pflight

Speed Pdep

Vmigr

V

Rate of energy deposition

Alerstam, 2003). Flight speeds can be obtained from radar or tracking measurements (ideally corrected to their still-air values; Bruderer & Boldt, 2001; Alerstam et al., 2007) or from theoretical estimates (Pennycuick, 1969, 1975). Rates of fuel deposition can be measured through repeated weighing of individual birds before migration or at stopover sites. Such measurements are usually taken over periods of days, so include sleeping and other non-feeding times. Rates of fuel use during flight can be measured only with difficulty if birds can be weighed at departure and arrival over a known route. Such rates are more easily obtained as theoretical estimates, based on body mass and other features of the bird (see Appendix 5.1). Rates of fuel (energy) gain and loss are best expressed in some common currency, such as multiples of BMR (basal metabolic rate, the rate of energy use by a resting, inactive bird; Chapter 5). On such a basis, for a small bird with an energy deposition rate of 1 3 BMR per day (above the 2 3 BRM required for normal daily activity), and travelling by flapping flight, the predicted average migration speed is about 200 km/day (Hedenstro¨m & Alerstam, 1998). This includes both flight and fuelling periods. At the higher energy deposition rate of 2.5 3 BMR per day, the predicted speed rises to 300 400 km/day. In larger birds, theoretical migration speeds are lower, at 70 100 km/day for a daily energy deposition rate of 1 3 BMR, and at 150 200 km/day for an energy deposition rate of 2.5 3 BMR. On theoretical grounds, large birds would be expected to migrate more slowly than small ones. This is because large birds require longer to acquire the fuel necessary to fly the same distance and also because large birds cannot carry such heavy fuel loads relative to their body weights (Lindstro¨m, 1991; Hedenstro¨m & Alerstam, 1998). However, large birds also fly faster than smaller ones and can therefore partly compensate for their lower fuelling rates and lower maximum fuel loads. The theoretical maximum speed of migration (including flights and stopovers) was estimated by Lindstro¨m (1990) as proportional to M20.14, where M is body mass. However, migration speed depends not only on bird body mass but also on wing and body morphology. For this reason, the Arctic Tern (Sterna paradisea), with its long and slender wings, is expected to match or even surpass the migration speed of the Willow Warbler (Phylloscopus trochilus) with its relatively broader and shorter wings, in spite of the fact that the tern weighs more than 10 times as much as the warbler (Figure 9.2). Moreover, soaring flight by some large birds can give more rapid overall progress than flapping flight because of its smaller energy needs, and consequent savings on re-fuelling times. With all these considerations, there is no simple answer to the question whether large birds would be expected to migrate slower or faster than small ones. More information than body weight alone is needed to predict the likely migration speed of a particular species. Even allowing for body mass and flight mode, theoretical calculations are likely to provide only very approximate estimates of maximum possible migration speeds, but they point to the enormous influence that feeding rates could have. Within any wild bird population, rates of fuel deposition are highly variable (Chapter 5), and the weather has an additional influence, speeding or slowing a journey (Chapter 4). In spring, the timing of snow melt, or the appearance of specific food supplies, can greatly influence migratory progress. Nevertheless, most of the higher migration speeds recorded in field conditions are similar to the speeds that have been calculated theoretically from knowledge of flight speed, fuel deposition during stopovers and fuel use during flight (Hedenstro¨m & Alerstam, 1998).

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FIGURE 9.2 Expected overall speed of migration by flapping flight in relation to fuel deposition rate Pdep for some selected species on the basis of flight mechanical calculations (still-air conditions). As a reference level of basal metabolic rate (BMR) in birds of different body weight, the allometric equation according to Lasiewski & Dawson (1967) was used. In most cases, fuel deposition rates (Pdep) of migrating birds are limited to levels up to 2 3 BMR, but some greatly exceed this rate (see text). From Alerstam (2003).

From the same type of information, one can also calculate the expected proportion of total migration time spent on fuel intake and deposition (as opposed to flight). Migration speed as a fraction of flight speed is given by the ratio of energy deposition rate to the sum of this rate and the rate of energy consumption for flight (called the ‘flight power’; Box 9.1). For example, for a bird with an energy deposition rate corresponding to 1 3 BMR per hour and an energy consumption rate for flight corresponding to about 7 3 BMR per hour, the bird would require 7 hours of feeding to accumulate the fuel needed for each hour of flight. This ratio is in fact typical of that found from ring recoveries for many species of small passerines, in which the energy requirements of flight are relatively small (Hedenstro¨m & Alerstam, 1998). For birds as large as swans, flight-to-fuelling ratios higher than 1:20 are needed (see later). In the calculation of daily fuelling rates from weight data, allowance is automatically made for sleeping and other activities during fuelling periods. Ideally, however, birds need to be studied over several weeks to provide a reasonable estimate of their flight-to-stopover ratios and in those species that accumulate large fuel reserves before their initial departure, this fuelling period should be included in the estimate of overall migration time. When measured over short periods of up to a few days, or from the point of departure, migration speed can easily be overestimated (and migration time underestimated) because, at this point, the bird has usually already stored some energy for the flight. In contrast to birds that migrate by flapping flight, soaring gliding birds would be expected to spend less time on accumulating body reserves, because much of the energy for their flight is derived from air currents. Power consumption in gliding flight is generally assumed to be a constant multiple of BMR and is unrelated to flight speed. Consequently, the migration speed of soaring gliding species should be directly proportional to their cross-country speed. Because cross-country speed increases with body mass (Chapter 3), migration speed in soaring species might also be expected to increase with body mass, the opposite to the situation in birds that migrate by flapping flight (Hedenstro¨m & Alerstam, 1998). However, overall migration speed is also influenced by the period each day that birds can migrate, and in overland areas where soaring depends on thermals, this period is usually longer for smaller (lightweight) species which can make use of weaker thermals than larger ones (Chapter 3). So in soaring species dependent on thermals, potential air-time may be more limiting than body reserves for overall migration speed.

Getting around the problems From the foregoing, we can conclude that the main factors affecting migration speed in birds are the time taken to accumulate the necessary body reserves, and to a much lesser extent, the flight speed. Both are greatly influenced by environmental conditions. Birds may raise their fuelling rates by seeking areas with the most abundant food supplies, feeding intensively and by dropping their guard against predators to free more time for feeding (Chapter 14; Loria & Moore, 1990; Wang & Moore, 2005). Birds may also reduce stopover time by adopting a ‘fly-and-forage strategy’, common among hirundines and raptors, where foraging is combined with movement in the migratory direction. Even if travel speed is thereby reduced, this could be more than compensated by the reduced need for stopover periods for re-fuelling (Strandberg & Alerstam, 2007; Alerstam, 2011; Dias et al., 2012). Some such species, such as Common Swift (Apus apus), can thereby achieve speeds much greater than similar-sized birds that need regular stopovers

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˚ kesson et al., 2012). Nocturnal migrants can achieve particularly high migration speeds by flying at night and forag(A ing by day, so long as the costs of finding new daily foraging sites and of sleep deprivation are manageable (Alerstam, 2011). In time-selected migration, there will also be strong selection for efficient and intensive foraging, since the total speed of migration is almost directly proportional to the fuel deposition rate (Houston, 2000). The flight speed of the bird is affected primarily by wind conditions (Chapter 4). A migrant can raise its ground speed by departing on days with more beneficial winds and by choosing appropriate flight altitudes. Pronounced selection of conditions with following winds is not necessarily a characteristic of time-selected (rapid) migration, however, because of the potentially large time costs of waiting for such winds to occur. The highest degree of wind selectivity would in fact be expected among energy-selected migrants that attempt to minimize transport costs. Such migrants are predicted to be tolerant of long waiting periods and to postpone departure until they can obtain maximal wind assistance that will lead to minimal flight costs. Birds can also be selective of wind conditions in evolutionary terms by using routes most likely to provide favourable tailwinds. In some situations, this selectivity can lead to loop migration, where spring and autumn routes differ substantially. In some birds, migration speed seems of minor importance, as individuals travel in more leisurely manner, pausing for long periods wherever they encounter plentiful food supplies. The advantage is that they do not pass rapidly through areas of abundant food, when supplies are unpredictable further along the route. They tend to show much more variation in migration speeds than other birds, and in some years may not reach the limits of their wintering range. Various irruptive seed-eaters and vole-eaters provide examples (Chapters 20, 21), as do some species of gulls which tend to follow coastlines than more direct routes and stop to feed every day (for Lesser Black-backed Gulls (Larus fuscus), see Klaassen et al., 2012; for Herring Gull (Larus argentatus), see Anderson et al., 2020). These species could be regarded as extreme energy (load) minimizers.

MEASURES OF MIGRATION SPEED Migration speeds from individual ring recoveries Migration speeds have been calculated for various species (mainly passerines and shorebirds) that were ringed on autumn passage in Sweden and Finland and recovered up to 50 days later at various points on their (mainly overland) migration routes (Hilde´n & Saurola, 1982; Ellegren, 1993, further analysed by Alerstam & Lindstro¨m, 1990; Alerstam, 2003). From these and other records (Figure 9.3), the following generalizations emerged:

Migration speed (km per day)

1. For birds studied over at least 10 days, average migration speeds in the range 21 263 km/day were found for different species. In general, shorebirds migrated more rapidly (median 79 km/day, N 5 13 species) than passerines (medians 27 75 km/day in different groups, see below; Alerstam & Lindstro¨m, 1990). This difference may occur because shorebirds fly faster than passerines, are more selective of favourable winds and migrate at higher altitudes where winds are stronger. In moving between successive staging areas, shorebirds typically fly 500 1000 km in 1 2 days, interrupted by several-day stops, whereas passerines typically migrate overland almost every day at a more even speed, with shorter flights and shorter stops. Including fuelling periods, maximum speeds up to 200 300 km/day were recorded in passerines, and up to 400 1000 km/day in shorebirds. These maximum speeds were consistent with theoretical expectations. 2. Among passerines, average migration speeds varied with autumn starting dates, as early departing species travelled more rapidly than late-departing ones (Figure 9.3). Thus speeds were considerably higher for long-distance species with tropical winter quarters that left early (median speed 75 km/day, n 5 13) than for short-distance temperate zone migrants that left later (median speed 53 km/day, n 5 19), or for irruptive and partial migrants that left latest of all (median 27 km/day, n 5 11). This trend could result from seasonal declines in food supplies or daylengths, leading to reduced rates of fuel Tropical winter quarters Temperate winter quarters Partial/irruptive migrants

120 100 80 60 40 20 0 Aug

Sep

Oct

Nov

FIGURE 9.3 Migration speeds recorded for passerines ringed in Finland in relation to the seasonal timing of migration as recorded at Ottenby in Sweden. The regression line highlights the reduction of migration speed with advance in mean departure date and the differences between different categories of migrants. From Alerstam & Lindstro¨m (1990), based on data in Hilde´n & Saurola (1982).

160

3.

4.

5.

6.

7.

8.

The Migration Ecology of Birds

deposition from late summer into autumn (Alerstam & Lindstro¨m, 1990; Ellegren, 1993; Kvist & Lindstro¨m, 2000). In addition, fast travel may be more important for early, long-distance species bound for the tropics than for later, shortdistance species migrating only within Europe (Alerstam & Lindstro¨m, 1990). Not only do the earlier migrants have further to go, but they probably gain from crossing the Sahara in August September, before the dry season takes hold in the Sahel zone to the south. In association with the above relationships, migration speeds were correlated with the length of journey (Figure 9.3). Juvenile passerines travelling 1000 km on migration covered about 80 km/da, on average, whereas those travelling 5000 6000 km covered about 140 km/day (Alerstam, 2003). Long-distance migrants seem to migrate in longer steps and are more selective of good weather conditions. They are generally nocturnal flyers, leaving the daytime for foraging (although shorebirds can feed day or night given suitable tidal conditions). Among passerines, nocturnal migrants made faster progress, on average, than diurnal migrants (72 km/day vs 53 km/day; N 5 17 and 6 species). In addition, migration flight lengths were longer in nocturnal (177 km) than in diurnal migrants (111 km), even though nocturnal migrants did not always use the entire night for flying (Cochran et al., 1967; Ellegren, 1993). Despite their faster autumn migration speeds, Eurasian Afrotropical migrants, with mean migration distances of 6000 10,000 km, still travelled for much longer periods (median 88 days, n 5 13) than regular temperate zone migrants travelling shorter distances (median 42 days, n 5 10, distances 1700 3000 km), or than partial migrants (median 32 days, n 5 11, distances 200 300 km). Some extremely rapid migrations were recorded in some long-distance passerine migrants. For example, a Willow Warbler travelled 8000 km from Finland to Congo within 56 days, a mean speed of 145 km/day (Hilde´n & Saurola, 1982), while another Willow Warbler travelled from Finland to South Africa in 47 days, a mean speed of 218 km/ day (Hedenstro¨m & Pettersson, 1987). A Marsh Warbler (Acrocephalus paludicola) travelled 1400 km within Africa in 5 days, an average of 280 km/day (Cramp, 1992); and three Barn Swallows (Hirundo rustica) travelled average distances of 250, 350 and 433 km/day over journeys of 8500, 12,000 and 3000 km, respectively (Turner, 2006). However, all these records refer to exceptional individuals, the majority of their species progressing more slowly. The decline in migration speed with advance in departure date did not apply within species. On the contrary, late migrants tended to progress more rapidly than early ones of the same species, at least in the initial part of the autumn journey (for various passerines, see Ellegren, 1993; for juvenile Eurasian Reed Warbler (Acrocephalus scirpaceous) and Sedge Warbler (A. schoenobaenus), see Bensch & Nielsen, 1999; for Goldcrest (Regulus regulus), see Bojarinova et al., 2008). This trend would allow birds that were delayed in their departure from breeding areas to ‘catch up’ during migration (Fransson, 1995). Eurasian Blue Tits (Cyanistes caeruleus) migrating in autumn along the southern Baltic coast travelled an average of about 28 km/day during 15 24 September, increasing significantly to about 38 km/day during 15 24 October (Nowakowski & Chru´sciel, 2004). In some species, adults travelled faster than juveniles. For example adult Dunlins (Calidris alpine) took an average of 4.5 days to travel 660 km, while juveniles took 13 days over the same journey (Hilde´n & Saurola, 1982). A similar age-related difference held in various Sylvia warblers migrating in autumn from northern Europe (Fransson, 1995). By the time they start migrating, juvenile birds appear ‘full-grown’, and in this respect are physically almost as well equipped for migration as older birds.

Average migration speeds from population-based ring recoveries Average estimates are more useful than those obtained from individual flights, because they derive from many individuals and not just a few, possibly extreme ones. Ringing data indicate that Barn Swallows complete the 10,000 km journey between northern Europe and southern Africa at an average speed of at least 150 km/day, as against individual ring recoveries which indicate exceptional speeds up to 340 km/day (Alerstam & Lindstro¨m, 1990). Other average estimates relate to Spotted Flycatchers (Muscicapa striata) between southern Africa and Fennoscandia (spring) at 140 km/day (Fransson, 1986) and to Willow Warblers between Fennoscandia and Africa (autumn) at 85 km/day, both over distances exceeding 10,000 km (Hedenstro¨m & Pettersson, 1987). Birds do not necessarily maintain the same rate of progress over their whole migration. To judge from ring recoveries, some species speed up during the course of their autumn journey, while others slow down. For Willow Warblers travelling from northern Europe to Africa, mean speeds were estimated at 41 km/day over distances of 400 1000 km (N 5 37), 54 km/day over distances of 1000 2000 km (N 5 30), 59 km/day over distances of 2000 3000 km (N 5 40) and 85 km/day over distances greater than 3000 km (N 5 22) (Hedenstro¨m & Pettersson, 1987). Similarly, for birds recovered in the first three weeks after ringing in autumn, mean migration speeds increased with distance in Bluethroats

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(Luscinia svecica), Sedge Warblers, Eurasian Reed Warblers and Lesser Whitethroats (Curruca curruca) from Sweden, and in Garden Warblers (S. borin) and Eurasian Blackcaps (S. atricapilla) from Britain (Ellegren, 1990, 1993; Fransson, 1995; Bensch & Nielsen, 1999). Migration speed increased more rapidly through the journey in long-distance migrants wintering in Africa than in short-distance migrants wintering within Europe (Alerstam, 2003). The reasons are unknown, but weather-induced delays may be fewer and food supplies greater as birds reach lower latitudes. On the other hand, other Sylvia warblers ringed in northern Europe and Britain seemed to slow down during their autumn passage through Europe. Speeds exceeding 100 km/day were recorded mainly in the first 10 days after ringing, and after about 20 days from ringing, average speeds had dropped markedly (Fransson, 1995). Much depends on the nature of the migration, whether by long flights and long stopovers, or short flights and short stopovers. Whatever the migration mode, however, speeds calculated over the early parts of a journey (which often provide most ring recoveries) may not be typical of the whole route, for birds may already have accumulated some migratory fuel when they were caught and ringed. In addition, for obvious reasons, journeys over seas or deserts are almost always undertaken more rapidly than equivalent journeys through more favourable terrain (see later). In a process so dependent on food and weather, migration would also be expected to vary greatly in speed from year to year over the same route. Annual variations have been little studied by ringing, but over the period 1963 98, a fourfold variation in average migration speeds was recorded among Eurasian Blue Tits travelling between various bird-ringing stations along the southern Baltic coast (Nowakowski & Chru´sciel, 2004). In the slowest year, the birds averaged less than 10 km/ day, compared with 38 km/day in the fastest year. In most years, the average speed was in the range 25 35 km/day, making the Blue Tit relatively slow among European passerines. This may be associated with its habit of migrating in short flights just above the tree-tops. The annual variations in speed paralleled those in the Great Tit (Parus major) which, however, migrated generally faster. Interestingly, Coal Tits (Periparus ater) studied in the same way migrated twice as fast in invasion years (40 80 km/day) as in other years (30 40 km/day), possibly because the migratory drive was stronger in invasion years, a difference also noted in Eurasian Siskins (Spinus spinus) (Payevsky, 1971). Most of the estimates of migration speed obtained from ring recoveries refer to autumn, when juveniles predominate, and the few records from spring suggest that faster progress is made then, at least by passerines and shorebirds. Thus Barn Swallows from Britain take an average of 10 weeks to reach South Africa in autumn, travelling at 150 km/ day, and 5 6 weeks to return in spring, travelling at 300 km/day (Mead, 1970). In contrast, Pied Flycatchers (Ficedula hypoleuca) travelled between northern Europe and tropical Africa at average speeds of 120 170 km/day in autumn but only at 100 km/day in spring (Lundberg & Alatalo, 1992). For many diurnal birds, fuelling rates may be influenced not only by the food supplies available on route but also by prevailing daylengths which influence the maximum daily feeding times, and hence the maximum possible migration speed (Kvist & Lindstro¨m, 2000). In many bird species, spring migration occurs closer to the summer solstice than autumn migration, and hence over longer days (Chapter 15; Bauchinger & Klaassen, 2005). The migratory speeds of three species of Sylvia warblers were, on average, 47% faster in spring than in autumn, calculated from ring recoveries of adult birds migrating between the Mediterranean and northern Europe. In parallel, the amount of daylight over the same migratory distance was 26% longer in spring than in autumn, calculated by comparing daylength at the mid-point (52 N) of the migratory journey, and of the spring and autumn migration periods (15 May and 18 September, respectively). If daylength has an influence (through its effect on fuelling), migration speed should also change during the course of a journey, as the bird moves through latitudes with different daylengths. To some extent, the same would be expected in soaring birds which are limited each day by the period when thermals occur (both daylength and temperature dependent). Further information on the difference between autumn and spring migration speeds is given later, incorporating the findings from tracking studies. Ring recoveries have provided further evidence that not all birds are under pressure to migrate as fast as they can. Comparisons between different populations of some species indicate that other factors are involved and that the time available for migration may also have an influence. For example, Common Kestrels (Falco tinnunculus) from northern Sweden travel twice as far as those from the south, but in the same time (Wallin et al., 1987). This difference held even though the entire journey of the short-distance birds lay within the route of the long-distance ones. In spring, the two populations migrated at the same speed, so the northern birds took longer to reach their breeding areas. Similarly, White Storks (Ciconia ciconia) from central Europe using the southwest route through Iberia take about 3 months to reach their winter quarters in West Africa. Those taking the southeast route through the Middle East to East Africa, also take about 3 months to cover twice the distance (Figure 9.4, Bairlein, 2001). Analysing ringing data for four species of Sylvia warblers, Fransson (1995) discovered that British birds travel through Europe at slower average speeds (39 56 km/day) than Scandinavian birds (80 116 km/day). He attributed this to the fact that British birds have shorter total migration distance (and hence may be under less pressure) and a slightly different migration schedule from Scandinavian ones (Table 9.1). These various findings suggest that some populations

162

The Migration Ecology of Birds

7 8 7

9

10

8 6

9

6 5 10 5

4

11

4

3 2 1

12

3 11

12

1 2 N

FIGURE 9.4 Course of first-year migration in White Storks (Ciconia ciconia) from southwestern Germany (westerly route) and northwestern Germany (easterly route), showing the migratory divide. Dots show the average monthly location of ringed birds. The lines join the dots of successive months but do not necessarily reflect the exact routes followed. First-year storks are on the move for much of the year, and most do not reach the breeding areas until it is too late to nest that year. Modifed from Bairlein (2001).

TABLE 9.1 Speed of migration (km per day) of five Sylvia species from northern Europe and Great Britain, estimated according to differences in median trapping dates and median dates of recoveries in the Mediterranean area. From Fransson (1995). Species

Great Britain Autumn

Northern Europe Spring

Barred Warbler (Curruca nisoria)

Autumn

Spring

92

Lesser Whitethroat (Curruca curruca)

56

97

80

98

Common Whitethroat (Curruca communis)

47

186

85

129

Garden Warbler (Sylvia borin)

39

232

116

163

Eurasian Blackcap (Sylvia atricapilla)

52

162

85

162

Source: From Fransson (1995).

Speed and duration of migratory journeys Chapter | 9

163

are not under pressure to migrate in autumn at the maximum speed of which they are capable. Perhaps at this time of year they have a certain period in which to migrate, according mainly to other events in the annual cycle, and can adjust their travelling speed accordingly. The benefits of migrating slowly are that birds can take advantage of rich feeding areas they encounter on route, yet do not need to accumulate the massive fuel reserves required by long flights, thereby lessening the associated predation risks (Chapter 5). They fall in the category of ‘energy minimizers’ (or ‘load minimizers’).

Migration speeds from tracked birds Tracking studies, which have grown so much in recent years, still cover a much narrower range of species than ringing studies, mainly long-distance migrants. Samples for each species also tend to be small, but providing tracking devices do not affect the migration speeds of the wearers, they give more reliable estimates of individual migration speeds than other methods, together with more information on stopovers and weather effects (Table 9.2). They have also provided much more valuable information than bird ringing regarding the movements of pelagic birds. Early studies involved following radio-tagged migrating birds by airplane, a procedure which gave information on behaviour as well as speed. For example seven individual Peregrines (Falco peregrinus) were followed on migration TABLE 9.2 Speed and duration of migratory journeys of various birds, as recorded in tracked individuals. Only species with samples of five or more individuals are included. Each figure is a mean rounded value based on the number of journeys tracked (N). km 5 distance migrated, Days 5 days taken over journey (including breaks), km/day 5 speed of migration calculated from previous two values. Species, migration route

Autumn

Spring

Source

N

km

Days

km/day

N

km

Days

km/day

Common Linnet (Linaria cannabina), within Europe

6

1662

62

27

5

1625

42

39

Ro¨seler et al. (2017)

Ortolan Bunting (Emberiza hortulana), Europe Africa

6

6020

56

108

6

6080

40

152

Selstam et al. (2015)

Snow Bunting (Plectrophenax nivalis), within N. America

12

2600

35

74

8

2147

22

98

McKinnon et al. (2016)

Semi-collared Flycatcher (Ficedula semitorquata), Europe Africa

11

5775

84

69

11

5432

49

111

Briedis et al. (2016b)

Eastern Kingbird (Tyrannus tyrannus), N S. America

8

6437

53

121

8

5220

22

237

Jahn et al., (2013)

Pallid Swift (Apus pallidus), Sweden Africa

21

4340

10

434

17

4706

11

428

Norevik et al. (2018)

European Nightjar (Caprimulgus europaeus), Sweden Africa

12

7931

69

115

12

8039

82

98

Norevik et al. (2017)

Band-tailed Pigeon (Patagioenas fasciata), within N. America

35

740

45

16

35

740

19

39

Casazza et al. (2015)

Eleonora’s Falcon (F. eleonorae), Cyprus-Madagascar

12

7139

25

286

5

7245

19

381

Hadjikyriakou et al. (2020)

Western Marsh Harrier (Circus aeruginosus), Sweden Africa

17

4504

50

90

2

5096

34

150

Strandberg et al. (2008)

Bar-tailed Godwit (Limosa lapponica), Alaska New Zealand

7

10,153

8

1269

8

17,560

57

308

Battley et al. (2012)

White-fronted Goose (Anser albifrons), Netherlands Russia

49

3300

42

79

53

3900

83

47

Ko¨lzsch et al. (2016)

Sooty Shearwater (Ardenna grisea), Falklands N. Atlantic

21

15,696

21

747

21

14,197

21

676

Hedd et al. (2012)

Westland Petrel (Procellaria westlandica) New Zealand

8

7237

6

1206

8

7237

10

724

Landers et al. (2011)

For other species see Table 9.3.

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The Migration Ecology of Birds

across the United States. In each 24-hour period, these birds typically spent 17 hours on a perch, 6 hours in migratory flight, and about 1 hour in hunting. In especially favourable conditions, migration increased to 9 h/day, and when held up by weather, perching increased to 23 h/day. On average, these falcons migrated on 6 days out of 7, generally from mid-morning to late afternoon, when they covered an average of 192 km (W. Cochran, records compiled by White et al., 2002). In another early study, 15 radio-marked adult Bald Eagles were tracked from a vehicle for an average distance of 2019 km in spring (Harmata, 2002). These birds appeared not to feed during the journey and did not migrate on days of overcast or high wind. All their flights occurred at some time within a 9-hour period each day (10.30 17.30 hours), covering an average of 180 km (range 33 435 km), at an average travel speed of 50 km/h (range 20 144 km/h). The birds flew at altitudes of 30 4572 m above ground, but mostly at 1500 3050 m, so for most of the time they were beyond the range of human vision. For two birds in which duration was determined accurately, migration lasted 15 days. Many more studies have involved tagged birds tracked from satellites, in which records of locations came at longer intervals, and without the behavioural details. In one of the earliest, Meyburg et al. (1998a,b) monitored a Short-toed Snake Eagle (Circaetus gallicus) every night on its autumn journey between France and Niger in West Africa, thus recording every roost location and daily travel distance. These distances varied from 17 to 467 km (mean 234 km), and the whole 4685 km journey took 20 days, giving a mean speed of 234 km/day (Figure 9.5). The later development of geolocators and their subsequent miniaturization facilitated the tracking of smaller birds. Details from such studies have given information previously unattainable, again enabling aspects to be examined in more detail than from ringing.

29/7–25/9/1996 25–26/9

28–29/9 29–30/9 30/9–1/10

1–2/10 2–3/10 3–4/10

4–5/10

5–6/10

6–7/10

7–8/10

8–9/10

9–10/10 11–12/10 13–14/10

FIGURE 9.5 Migration of a satellite-tracked radio-tagged Short-toed Snake Eagle (Circaetus gallicus) from France to Niger, showing the daily distances flown and the nightly stopping places. From Meyburg et al. (1998).

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Variations between species. Migration speeds recorded from different species of passerines, raptors and waders are shown in Figures 9.5 9.7. In all three groups, speeds up to 300 km were recorded, and raptors which travelled mainly by soaring flight were not obviously slower than passerines which travelled by flapping flight. Waders travelled generally faster than both groups and all the mean speeds greater than 600 km/day involved long non-stop flights, mostly over water. Whether from satellite tags or geolocators, tracking results largely supported the findings from ring recoveries, in that short-distance diurnal migrants generally travelled more slowly (less than 100 km/day) than long-distance (mainly nocturnal) species (mostly in the range 100 300 km/day); in many species spring journeys were faster than autumn ones, and within species individuals departing late in the season migrated faster than earlier departing birds. Some of the fastest migration speeds were again recorded from waders, especially those making long flights over water or other hostile terrain, with several studies recording mean speeds of more than 1000 km/day on both outward and return journeys (Gill et al., 2009; Johnson et al., 2015; Lindstro¨m et al., 2019). Fast speeds were also shown by some pelagic

(a)

(b)

FIGURE 9.6 Migration routes of (a) Peregrine Falcons (Falco peregrinus) and (b) Swainson’s Hawks (Buteo swainsoni) from North American breeding areas, as shown by the tracks of satellite-tracked tagged adults. From Fuller et al. (1998).

20

Passerines

25

Raptors

12

Waders

10

20 Frequency (n)

15 8 15 10

Spring

6

Autumn

10 4 5 5

0 0

100 200 300 Migration speed (km/d)

2

0 0

100 200 300 400 Migration speed (km/d)

0 0

100 200 300 >600 Migration speed (km/d)

FIGURE 9.7 Migration speeds recorded in various species of passerines (34), raptors (37) and waders (19), based on mean values from tracking studies referenced elsewhere in this book.

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The Migration Ecology of Birds

seabirds, as several species of albatrosses and shearwaters reached speeds of more than 1000 km/day, at least over parts of their journeys. Compared to other small birds, swifts which spend all their time on the wing achieved relatively high migration speeds, with Pallid Swifts (Apus pallidus) averaging more than 400 km/day in both outward and return journeys (Norevik et al., 2018). Soaring raptors maintained relatively high speeds on migration, many averaging 50 250 km/day, including stopovers, and some more than 350 km/day (Figures 9.6 9.8). The species in Box 9.3 illustrate some of the longest journeys found among raptors: the Swainson’s Hawk (Buteo swainsoni) which migrates by soaring gliding flight and makes the entire journey overland and the Peregrine which migrates by a combination of soaring and flapping flight and can include substantial water crossings in its journeys. Among waterfowl, swans and geese were among the slowest of migrants when travelling overland, with mean speeds of mainly less than 150 km/day, even over distances of 5000 6000 km. This was mainly because of the time taken in such large birds on stopover, accumulating the necessary body reserves. Nevertheless, some geese achieved much higher speeds on long sea-crossings, for which the necessary body reserves were accumulated beforehand (see later.) Passerines

Migration in spring (days)

100

Raptors

100

80

80

80

60

60

60

40

40

40

20

20

20

0

0 0

20 40 60 80 100 Migration in autumn (days)

Waders

100

0 0

20 40 60 80 100 Migration in autumn (days)

0

20 40 60 80 100 Migration in autumn (days)

FIGURE 9.8 Relationship between the durations of the autumn and spring migrations of different passerine (32), raptor (20) and wader (15) populations, based on the mean values from different tracking studies referenced elsewhere in this book. The line on each graph shows the relationship expected if the two migrations were of equal duration. Overall, spring migration was faster in most of the passerines and some waders, but no great difference was apparent in any of the raptors, travelling mainly by soaring flight.

BOX 9.3 Migrations of Peregrine Falcons (Falco peregrinus) and Swainson’s Hawks (Buteo swainsoni) from North America. From Fuller et al. (1998). 1. Peregrine Falcon. Sixty-one adult female Peregrines were tracked on migration between nest sites in northern North America or Greenland and wintering sites in southern North America, Central and South America (Figure 9.6). Breeding sites spanned about 35 of latitude and wintering sites about 80 of latitude (from 40 N in the mid-Atlantic United States coast to 40 S in central Argentina). On average, on their southward journey these birds covered 8624 km and on their northward journey 8247 km (taking different routes at the two seasons). Their southward journey took an average of 50 days at around 172 km/ day, and their northward journey took an average of 42 days at around 198 km/day. In general, these birds migrated on a broad front, but in autumn tended to concentrate along coastal routes, and many crossed the Gulf of Mexico or Caribbean. In spring they took more inland routes, on the western side of the Gulf, from which they headed towards various northern destinations. Birds migrating north through a single locality (Padre Island on the Texas coast) diverged for destinations ranging from Alaska to west Greenland. These findings confirmed those obtained over a longer period from ringing that many individual Peregrines which migrate southward down the east coast of North America in autumn migrate northward up the Gulf Coast in spring, performing a ‘loop migration’ like many shorebirds. 2. Swainson’s Hawk. In contrast to Peregrines, Swainson’s Hawks migrate by soaring flight and converge on a relatively narrow route from North to South America through Panama, thus avoiding sea-crossings and showing no great divergence of routes between spring and autumn (Figure 9.6). Of 34 birds tracked from various localities in the breeding range in western North America, all wintered in a relatively small area in South America lying at 30 40 S and 61 64 W. On average, these birds travelled 13,504 km on their southward journey, at 188 km/day, and 11,952 km on their northward journey, at 150 km/day. On southward migration, the birds became concentrated on the Gulf Coast of Central Mexico and remained in a relatively narrow stream through Panama and down the eastern flanks of the Andes.

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Migration speed and body size. At face value, neither ringing nor tracking studies could confirm the theoretical prediction that smaller species should migrate more rapidly than larger ones. Existing tracking studies made it difficult to test reliably for any such relationship. Not only did the same species show markedly different migration speeds on different journeys, but even on the same journey individual adults varied by up to 12-fold in the time taken (see below). Moreover, data on overall migration speeds excluded the initial fattening period which could have extended to several weeks in some large species. Even in spring, when birds are assumed to migrate as rapidly as possible to reach their breeding areas, the migration speeds of passerines appeared generally no faster than those of larger species (including raptors and storks which travel by soaring flight). For many species, it appears that spring speeds were largely influenced by the spread of warmth to higher latitudes (as reflected, for example, in the northward movement of particular isotherms, ice melt or the greening of vegetation, Chapter 15). On this view, species would have moved to progressively higher latitudes as conditions allowed, with no obvious differences between small and large species, whatever their theoretical capabilities. Variations within species. Confirming findings from ringing, within species, individuals from different parts of the breeding range often migrated at different speeds, according to the journeys they made, with long-distance birds usually (but not always) travelling faster (Table 9.3). On average, Northern Wheatears (Oenanthe oenanthe) migrated at nearly twice the speed over the 14,400 km from Alaska to Africa as over the 4040 km from Europe to Africa: averaging 160 km versus 84 km/day in autumn and 265 versus 117 km/day in spring (Bairlein et al., 2012; Schmaljohann et al., 2012). Other Northern Wheatears migrating over the sea from Canada to Europe had to migrate non-stop, with one bird covering the 3400 km from Baffin Island to Ireland in less than 4 days, at 850 km/day (Bairlein et al., 2012). Similar details for different populations of other species are given in Table 9.3. Much depends on re-fuelling stops, and among Ospreys (Pandion haliaetus) breeding in northern and southern Europe, the former travelled five times further but, because of re-fuelling stops, achieved less than half the average migration speed (km per day) of the southern, shortdistance birds which could cover their whole journey without stopping (Monti et al., 2018). Again confirming results from ringing, among birds from the same area, late-departing individuals migrated more rapidly than earlier ones, mainly by reducing the time spent on stopovers. This enabled late-departing individuals to catch up to some extent with earlier ones, reducing the spread of overall arrival dates in wintering or breeding areas (for Wood Thrushes (Hylocichla mustelina) in autumn, see Stutchbury et al., 2011; for Barn Swallows in autumn, see Imlay, 2021; for Red-backed Shrikes (Lanius collurio) in spring, see Pedersen et al., 2016; for Red Kites (Milvus milvus) in autumn, see Maciorowski et al., 2019). Ospreys normally migrate by day, but late-migrating individuals sometimes migrated at night as well (Mackrill, 2017), while late-departing Golden Eagles (Aquila chrysaetos) made up time by flying more direct (but probably more energy-demanding) routes (Miller et al., 2016a,b). Species also migrated more rapidly when crossing barriers or other hostile terrain than over more benign habitat. This was obviously the case for landbirds which migrated over long stretches of water where they could not stop, as in the Northern Wheatears mentioned above. It was also apparent in most trans-Saharan migrants which travelled more rapidly over the desert (where they could rest but not feed) than over the more favourable habitat to the north or south. Examples include the Booted Eagle (Hieraaetus pennatus) (Mellone et al., 2015), Western Marsh Harrier (Circus aeruginosus) (Strandberg et al., 2008), Eurasian Hobby (Falco subbuteo) (Strandberg et al., 2009), European Roller (Coracias garrulus) (Rodrı´guez-Ruiz et al., 2014) and many smaller birds. Faster travel was also seen in species crossing high mountains such as the Himalayas, as exemplified by Peregrines and others (Dixon et al., 2017). Variations among individuals. Tracking studies have also revealed great variations in migration speeds among adults from the same population making essentially the same journey. Some individuals took 2 3 times longer than others or occasionally up to 12 times as long (see below). Much of this variation was associated with the weather encountered on route, because birds departing at different dates encountered different conditions. But additional variation may have resulted from the varying abilities of the birds themselves for example in foraging skills, which could influence their fuelling rates and hence their migration speeds. To take some examples, among Bewick’s Swans (Cygnus columbianus bewickii) migrating between northern Russia and the Netherlands, individuals varied between 8 and 78 days in the time taken to complete their autumn journey. This implied average speeds of 44 400 km/day, a ninefold variation depending on the amount of stopover, which in turn depended largely on weather. In addition, pairs with young took longer over the journey than adults alone, stopping more frequently and arriving later in the wintering areas, probably because juveniles were less able than adults to cover such long distances non-stop (Beekman et al., 2002). Even greater variation was recorded among Barnacle Geese (Branta leucopsis) migrating largely over water from Svalbard via Bear Island to Scotland in autumn over a total distance of 2500 3000 km. Some birds completed this journey in as little as 2 3 days, averaging more than 1000 km/day, during which their stops were of such short duration that they gave little chance to replenish reserves (Butler et al., 1998).

TABLE 9.3 Speed and duration of migratory journeys of various birds, as recorded in tracked individuals. Only species tracked on more than one route, with samples of five or more individuals, are included. Each figure is a rounded mean value based on the number of journeys tracked (N). Km 5 distance migrated, Days 5 days taken over journey (including breaks), km/day 5 speed of migration calculated from previous two values. For scientific names, see text. Species, migration route

Mass

Autumn

Spring

Source

N

km

Days

km/day

N

km

Days

km/days

Common Swift, Sweden Africa

45

6

9769

69

142

6

9208

29

318

˚ kesson et al. (2016) A

Common Swift, Netherlands Africa

45

16

8914

45

198

16

8852

30

295

Klaassen et al. (2014a,b)

Northern Wheatear, Germany Africa

28

5

4040

48

84

5

4218

36

117

Schmaljohann et al. (2012)

Northern Wheatear Alaska Africa

28

3

14,600

91

160

3

14,600

55

265

Bairlein et al. (2012)

Golden-winged Warbler, Minnesota

10

12

4144

59

70

12

4575

36

127

Kramer et al. (2017)

Golden-winged Warbler, Tennessee

10

7

4710

75

63

7

4710

38

124

Kramer et al. (2017)

Golden-winged Warbler. Pennsylvania

10

2

6748

104

65

2

7212

46

157

Kramer et al. (2017)

Great Reed Warbler, Sweden Africa

33

6

6286

41

153

6

7083

32

221

Lemke et al. (2013)

Great Reed Warbler, Turkey E. Africa

33

5

3646

29

126

Great Reed Warbler, Spain

33

3

3078

35

88

3

3526

29

122

Horns et al. (2016) * Koleˇcek et al. (2016)

Great Reed Warbler, Sweden

33

9

5767

39

148

9

5953

22

271

Koleˇcek et al. (2016)

Great Reed Warbler, Czech Republic

33

8

4732

35

135

8

4927

19

259

Koleˇcek et al. (2016)

Great Reed Warbler, Bulgaria

33

4

3433

13

264

4

4476

29

154

Koleˇcek et al. (2016)

Great Reed Warbler, Turkey

33

4

3510

10

351

4

5123

26

197

Koleˇcek et al. (2016)

Barn Swallow, Washington S. America

20

8

4805

57

84

5

4528

24

189

Hobson et al. (2015)

Barn Swallow, New Brunswick

20

10

10,423

70

149

5

1288

46

245

Hobson et al. (2015)

Peregrine, N. S. America

950

61

8624

50

172

61

8247

42

196

Fuller et al. (1998)

Peregrine, Mexico North America

950

6

5059

40

126

13

5059

30

169

McGrady et al. (2002)

Peregrine, Yamal- southern Eurasia

950

17

5288

27

196

13

5337

26

205

Sokolov et al. (2018)

Peregrine, N. Siberia mainly India

950

10

6330

32

198

10

6330

29

218

Dixon et al. (2017)

Montagu’s Harrier, Mid Eur Africa

350

25

4827

31

156

17

306

35

152

Trierweiler et al. (2014)

Montagu’s Harrier, Spain W. Africa

350

9

2566

16

160

5

2930

27

109

Limin˜ani et al. (2012)

Egyptian Vulture, Spain- West Africa

1890

25

3256

13

250

23

3580

19

188

Lo´pez-Lo´pez et al. (2014)

Egyptian Vulture, Balkans Africa

1890

25

4843

23

211

13

5304

25

212

Buechley et al. (2018)

Osprey, Sweden Africa

1550

13

6742

45

150

Osprey, Britain W. Africa

1550

34

6776

22

308

Kjelle´n et al. (2001) 27

6561

27

243

Mackrill (2017)

Osprey, East coast US

1550

35

5134

31

166

Martell et al. (2001)

Osprey, Midwest US

1550

30

5872

26

226

Martell et al. (2001)

Osprey, West coast US

1550

2

3824

13

294

Martell et al. (2001)

Osprey, Florida S. America

1550

7

4105

25

164

Martell et al. (2004)

Osprey, Within Florida

1550

3

145

1

145

Martell et al. (2001)

Osprey, Sweden Africa

1550

15

6336

9

107

Monti et al. (2018)

Osprey, Corsica Africa

1550

10

1492

4

373

Monti et al. (2018)

Osprey, Estonia Africa

1550

10

5676

21

270

Osprey, Russia Africa

1550

4

6026

41

147

Babushkin et al. (2019)

Osprey, Poland Africa

1550

4

6557

32

205

Anderwald et al. (2021)

Osprey, East coast US

1550

35

5134

31

166

Martell et al. (2001)

8

6539

38

172

Va¨li & Sellis (2015)

Lesser Black-backed Gull, Holland

830

14

2036

83

25

13

1965

23

85

Klaassen et al. (2012)

Lesser Black-backed Gull, Norway

830

7

6940

18

386

6

7082

42

169

Bustnes et al. (2013)

Eur. Whimbrel, Siberia Australia

360

8

11,848

90

132

7

11,609

41

283

Kuang et al. (2020)

Eur. Whimbrel, Iceland W. Africa

360

30

6074

59

103

26

6458

66

98

Carneiro et al. (2019).

Eur. Whimbrel, Mackenzie S. America

360

21

11,332

64

177

16

11,518

55

209

Watts et al. (2021)

Eur. Whimbrel, Hudson Bay S. America

360

9

8989

68

132

9

8581

47

183

Watts et al. (2021)

Long-billed Curlew, Oregon California

610

9

1038

3

346

7

1036

3

345

Page et al. (2014)

Long-billed Curlew, Nevada California

610

5

1058

5

212

4

1046

3

349

Page et al. (2014)

Long-billed Curlew, Montana Mexico

610

14

2707

68

40

13

2551

29

88

Page et al. (2014)

Ringed Plover S. Sweden SW. Europe

68

12

2396

21

114

11

2258

23

98

Hedh et al. (2021)

Ringed Plover, N. Sweden W. Africa

68

32

6660

54

123

24

6503

54

120

Hedh et al. (2021)

Common Tern, Germany W. Africa

127

138

5281

12

440

105

5463

22

248

Ku¨rten et al. (2022)

Common Tern, North South America

120

32

7553

88

86

19

7640

32

39

Bracey et al. (2018)

Arctic Tern, Greenland Southern Ocean

a

a

100

11

34,600

80 93

330

11

24,270

0 41

520

Egevang et al. (2010)

Arctic Tern, Svalbard Southern Ocean

100

16

22,900

78

294

16

24,800

54

435

Hroma´dkova´ et al. (2020)

Arctic Tern, Sweden Southern Ocean

100

10

25,840

115

277

10

17,170

44

367

Alerstam et al. (2019)

Arctic Tern, Netherlands Southern Ocean

100

7

29,700

110

420

7

26,000

34

610

Fijn et al. (2013).

Arctic Tern, White Sea Southern Ocean

100

7

44,993

104

432

7

29,098

61

488

Volkov et al. (2017)

a

Refers to two routes, down the eastern and western sides of the Atlantic.

170

The Migration Ecology of Birds

At the other extreme, four birds held up on route by unfavourable winds took 9 36 days over the journey, giving mean migration speeds of 306 76 km/day. Overall journey time thus varied at least 12-fold between individuals. Possibly most Barnacle Geese left Svalbard with enough fuel to complete the journey to Scotland if they could do it within 2 3 days. But if they were held up by weather, their reserves would have become depleted, requiring additional feeding. Soaring species showed similar high variation. Among Ospreys breeding in Sweden and wintering in West Africa, the total length of journey varied between 5813 and 7268 km (longest journey 1.25 times longer than the shortest), but this journey took between 14 and 55 days to complete (greatest value 3.9 times longer than shortest) in a sample of 13 individuals (Kjelle´n et al., 2001). Mean speeds varied between 108 and 431 km/day. Among European Honey Buzzards (Pernis apivorus) over a similar route, the journey varied between 6299 and 7091 km (longest journey 1.13 times longer than the shortest) and took between 34 and 70 days to complete (greatest value 2.06 times longer than the shortest) in a sample of nine individuals (Ha˚ke et al., 2003). Mean speeds varied between 93 and 209 km/day. Common Cranes (Grus grus) migrate by a mixture of soaring and flapping flight. Sixteen individuals migrating from Germany to Spain took 3 28 days (mean of 17 days) over the journey, a ninefold variation over the same route (Alonso et al., 2008). Eight Houbara Bustards (Chlamydotis undulata), which migrate by flapping flight, took 13 73 days over their autumn journeys from breeding areas in Kazakhstan a sixfold variation in the time taken (Combreau et al., 1999). In general, within regional populations, those adults that spent the longest periods on migration spent the shortest periods in their wintering areas, while no effect was apparent on the amount of time spent in breeding areas. However, the main message from all these studies was the huge variation between individuals in the timing and duration of similar journeys, much of it imposed by weather. Migration speed and length of journey. The finding from ringing that long-distance migrants travel more rapidly than short-distance migrants seems also to hold in tracking results, although few short-distance migrants have been studied by tracking. Nevertheless, an assessment of passerine studies (involving 17 populations and 161 individuals in spring and 21 populations and 241 individuals in autumn) confirmed positive relationships between journey length and speed (Schmaljohann, 2019). An increase in the total migration distance of 100 km was associated with an average increase in the overall speed of migration of 3 km/day for short migration distances (up to 1300 km) and 2 km/day for longer ones (up to 10,000 km). This trend was thus in line with earlier studies from ringing (Ellegren, 1993; Fransson, 1995), but contrary to a study on a smaller number of geolocator studies which revealed no such relationship (McKinnon et al., 2013). A relationship between length of journey and migration speed was also apparent among some species of non-passerines (eg Eurasian Woodcock (Scolopax rusticola), Tedeschi et al., 2020), but not others. Difference between autumn and spring migration. Nilsson et al. (2013) examined information from 75 studies in which individual birds were tracked on both their autumn and spring journeys. For each bird they assessed, wherever possible, its airspeed, ground speed, daily travel speed, stopover duration and total speed and duration of the journey. Among these measures, only airspeed (a bird’s flight speed relative to the surrounding air) was under the total control of the bird itself, with increasing airspeed costing additional energy. All other measures (including ground speed) were influenced partly by environmental conditions by food supply, wind and other weather. Most of the birds studied, from several taxonomic families, showed higher speeds and shorter migration durations in spring than in autumn, confirming earlier findings from ringing. These seasonal differences arose mainly from longer and more frequent stopovers in autumn, and only slightly from seasonal differences in flight speeds. Evidently, the rates of foraging and fuel deposition, which influence stopovers, were more important than flight speed in accounting for the seasonal difference in overall migratory performance. Still, the seasonal differences in airspeed suggested that the birds themselves attempted to travel faster in spring than in autumn. Similarly, in a different study involving a tracking-radar, nocturnal passerine migrants flew at consistently higher airspeeds in spring than in autumn, with spring speeds exceeding autumn speeds by an average of 16%, after correcting for wind conditions (Karlsson et al., 2010). Time thus seemed more important in spring than in autumn, a finding also evident in many of the species shown in Figures 9.7 and 9.8. Further studies on a wider range of species have confirmed that spring journeys occur more rapidly than autumn ones in many more species than the other way round (Schmaljohann, 2018). Of 401 individual return bird tracks examined, 69% showed a faster migration in spring, compared with 31% in autumn. In raptors, waders, gulls, near-passerines and passerines, more than half of all individuals migrated faster in spring, whereas the opposite pattern emerged in waterfowl, storks and a few other groups represented by small samples (Table 9.4). The tendency for faster migration in spring is also evident in the data for passerines in Figure 9.7, less so for waders and barely apparent in raptors. In both groups, different populations of the same species sometimes showed different trends, depending on the journeys undertaken.

Speed and duration of migratory journeys Chapter | 9

171

The apparent urgency of spring migration in many birds has been attributed to competition for nesting habitat, as the earliest arrivals get the best places and breed more productively (a pattern frequently observed in field studies, Newton, 1998; Kokko, 1999). Interestingly, however, juvenile Golden Eagles which were too young to hold a nesting territory still travelled more rapidly in spring than in autumn, possibly because of better-soaring conditions in spring (McIntyre et al., 2008; Box 9.4). Instances where birds migrate more slowly in spring than in autumn seem to occur in particular circumstances. Some of the species concerned take longer routes on their return journeys (the spring journey is about 70% longer in the Bar-tailed Godwits (Limosa lapponica) that migrate between Alaska and New Zealand); some face more headwinds in spring (for various transTABLE 9.4 Number of species which migrate faster in autumn than in spring and in spring than in autumn. Data from tracking publications cited in this book. Faster in autumn

Faster in spring

Songbirds

4

27

Near-passerines

2

7

Raptors

7

14

Waterfowl

4

0

Storks

1

3

Cranes

0

1

Waders

7

10

Gulls and terns

3

9

Procellariiforms

3

3

Overall

31

74

BOX 9.4 Details from a tracking study of migrating Golden Eagles (Aquila chrysaetos) in western North America. From McIntyre et al. (2008). Juvenile Golden Eagles from nets in Denali National Park in Alaska migrated southeast to wintering areas in Canada and the United States. Over 2 years, 28 juveniles set off on dates between 15 September and 5 October, travelled distances varying between 818 and 4815 km and arrived in their chosen wintering areas (from the south Yukon to southern New Mexico) 31 86 days later, between 30 October and 28 December. The huge variation in these dates and distances is striking. On average, males travelled further than females. As the eagles travelled further from their breeding areas, their routes diverged increasingly from one another, so their latitudinal/longitudinal spread increased. Nevertheless, their migration tracks were only 9% longer, on average, than if the birds had flown on straight lines to their wintering places. Stopovers varied from 3 to 19 days and were in general longer for birds that made only a single stop during their journey than in those that made multiple stops. Peak movements occurred primarily around mid-day, in the best soaring conditions, speeds ranged from 16 to 73 km/h, and long-term tracking speeds reached the equivalent of 472 km/day. All individuals survived their first autumn migration, but only 14 (50%) survived their first winter. Survival was better among birds that wintered further south. No individuals wintering above 55 N latitude survived the winter, and those wintered more than 49 N were less likely to survive than those wintering further south (X2 5 8.11, df 5 1, P 5 .04). Twelve individuals completed spring migration, starting between 27 March and 8 May and arriving in their summer quarters between 10 May and 13 June, travelling northwest over 24 54 days and distances of 2032 4491 km. Overall, individuals travelled 6% further along their spring migration routes than if they had flown on straight lines to their summer areas. Spring stopovers ranged from 3 6 days, with most individuals making only one or two stops. Peak speeds reached 330 km/day. These juveniles spent their first summer in Alaska or Northern Yukon, usually more than 250 km from their natal areas. During summer, most individuals wandered more than 200 km from the terminus of their spring migration and visited different places for varying amounts of time. Many summered north of their natal sites, some more than 1000 km further north. Interestingly, none of the 28 birds that started autumn migration and 12 that started spring migration died during their journeys. Mean values for these birds were as follows: during the autumn migration, a duration of 60 days, a distance covered 2692 km, and an average speed 45 km/day; during the spring migration, a duration of 42 days, distance covered 3214 km, and an average speed 77 km/day. So although these juveniles were not of breeding age, or competing for nesting territories, they still travelled faster on spring than on autumn migration, possibly due to better-soaring conditions in spring.

172

The Migration Ecology of Birds

Saharan migrants, see Norevik et al., 2017; Panuccio et al., 2021); others stop on route to build up body reserves for breeding (for arctic-nesting waterfowl, see Chapter 5); and others must wait for the appearance of food supplies, as birds are constrained to follow particular isotherms, ice melt patterns or ‘green waves’ on their northward journeys to breeding areas (for Barnacle Geese, see van der Graaf et al., 2006; Ko¨lzsch et al., 2016; for Bewick’s Swan, see Nuijten et al., 2014; Chapter 15). All northern waterfowl may be constrained by ice melt or food supplies in spring in a way that they are not in autumn (for Common Eider (Somateria mollissima) see Mosbech et al., 2006, for geese see Drent et al., 2007). Yet other species, dependent on sporadic food sources, may travel slowly in spring because they are searching for an area with abundant food, such as the rodent peaks sought by Black Harriers (Circus maurus) in southern Africa (Garcia-Heras et al., 2019), by Pallid Harriers (Circus macrourus) on the Eurasian Steppes (Terraube et al., 2012), or by Snowy Owls (Bubo scandiaca) on the arctic tundra (Fuller et al., 2003; Therrien et al., 2015). These owls sometimes continue spring migration through the early summer, apparently in attempts to find a food supply sufficient for reproduction (Chapter 21). The effect of wind on migration is strikingly evident in Common Terns (Sterna hirundo) which in the east Atlantic, where coastal winds blow northsouth, migrate more slowly in spring than in autumn, but in the west Atlantic where coastal winds blow south-north, these terns migrate faster in spring (Becker et al., 2016). So despite any advantage, there might be in ‘time-minimizing’, these various examples provide further evidence for the often over-riding role of environmental conditions in limiting the rate of progress on spring migration. During this season, birds are generally migrating towards worse conditions which will improve later, whereas in autumn they are migrating towards better conditions which may worsen later. Sex and age differences. Among most types of birds, tracked males and females of mated pairs travelled separately and sometimes used wintering areas hundreds or thousands of kilometres apart from one another (for Sabine’s Gull (Xema sabini), see Davis et al., 2016; for Great Spotted Eagle (Clanga clanga), see Meyburg et al., 1998a,b; Figure 9.9). Mates re-united on FIGURE 9.9 Migration routes of a mated pair of Greater Spotted Eagles (Clanga clanga) from a nest site in Germany to wintering sites in Africa. Note that the two mates spent the non-breeding period in widely separated areas. From Meyburg et al. (1998a,b).

Speed and duration of migratory journeys Chapter | 9

173

their return to breeding sites. Exceptions were provided by swans, geese and cranes in which parents and their young migrated together as families to a common wintering area, and back in spring. In other birds in which males and females travel independently, and set off at different average dates, any differences in subsequent migration speed between them could be related to different timing within the season when weather and other conditions may differ. Age differences are another matter. In most species, juvenile birds often move independently from adults and rely on their own inherited behaviour to reach suitable wintering areas. Ringing results have indicated that young birds often migrated more slowly than adults, and the same is true of most of the tracking studies that included adults and young from the same population. Experienced adults tended to be more selective of good weather, oriented more effectively and more often compensated for wind drift; they also spent less time on stopover (possibly because they fed more efficiently) and consequently travelled more quickly than younger, inexperienced birds (Chapter 18; for various raptors, see Thorup et al., 2003a,b; Sergio et al., 2014; Miller et al., 2016a,b; Garcı´a-Macı´a et al., 2021; for Whooping Crane (Grus americana), see Mueller et al., 2013; for White Stork, see Rotics et al., 2016). On average, among Ospreys travelling from Britain to Africa, 34 adults completed their migrations in 21.3 days and 10 juveniles in 37.7 days; the adults had fewer stopovers and flew more directly (Mackrill, 2017). Adults also showed less variation in journey times than juveniles, taking 11 48 days (fourfold variation) over their migration, compared with 8 90 days (11-fold variation) among the juveniles which were more often blown off course. In contrast, juvenile Golden Eagles in eastern North America achieved higher flight speeds than adults, largely because they travelled later than adults when conditions were more favourable, with more tailwinds in autumn and more thermals in spring (Rus et al., 2017). The usual difference between the flight speeds of adults and juveniles was thereby reversed. Even among White Storks in which young and old travel in the same flocks, juveniles tended to lag behind and take longer over the journey than adults (Rotics et al., 2016). The juveniles used winds less efficiently and expended an estimated 14% more energy on migration as a result of their increased use of flapping flight. They took longer over rests and re-fuelling at stopovers. They did not therefore remain in the same flock throughout their journey but fell back in the migration stream as the days progressed. On the other hand, no such differences in migration speed occurred among swans and geese in which the two age groups stayed together as families, the adults holding back with their young when necessary, and migrating more slowly than adults without young, as mentioned above (Beekman et al., 2002).

Seabird migrations The use of tracking devices provided the first reliable information on the migrations of pelagic seabirds, especially for those that travel by soaring gliding flight. Among such species, albatrosses achieved average speeds between 220 and 950 km/day over distances of 3000 25,000 km (Jouventin & Weimerskirch, 1990; Prince et al., 1992; Weimerskirch et al., 1993; Croxall et al., 2005). Based on average rather than occasional speeds, albatrosses that travel by gliding flight are evidently among the fastest of all long-distance travellers. Turning to some smaller soaring gliding seabirds, Sooty Shearwaters (Puffinus griseus) on their figure-eight migrations travelled an average of 64,037 km in 198 days, giving a mean speed of 323 km/day (Shaffer et al., 2006). On parts of the journey, speeds rose to an average of 910 km/day, approaching the highest recorded from albatrosses. Even faster travel was recorded from a Manx Shearwater (Puffinus puffinus) which covered the 7750 km between nesting and wintering area (Wales to Argentina) in 6.5 days, averaging 1193 km/day (Guilford et al., 2009). High travel speeds in many pelagic species can be explained by their wind-assisted still-wing flight mode which is much less energetically demanding than flapping flight and allows birds to travel much longer distances without the need to rest or re-fuel. Moreover, unlike the thermal soaring of some landbird migrants, which at best can proceed for little more than 8h/day, dynamic soaring at sea can be maintained day and night. Flying near the sea surface, it is presumably easier for pelagic seabirds to spot and pick up food on the way, enabling them to fly thousands of kilometres without making major stops (as in the 13,000 km or more recorded in Cory’s Shearwaters (Calonectris borealis), Dias et al., 2012). Among seabirds that travel by flapping flight, Arctic Terns typically cover 250 520 km/day, and Sabine’s Gulls (Xema sabina) over part of their journey reached more than 800 km/day (Stenhouse et al., 2013), and some Black Terns (Chlidonias niger) up to 1245 km/day (van der Winden et al., 2014). Lesser Black-backed Gulls (Larus fuscus) migrating short distances within Europe covered only 44 km/day in autumn, compared with 386 km in a more northern population migrating to sub-Saharan Africa (Table 9.3). Paralleling the situation in most landbirds, almost all seabird species tracked on migration took longer over their outward autumn journeys than over their return spring journeys to breeding areas, on which they made fewer or shorter stopovers. Extreme examples include the Ivory Gulls (Pagophila eburnea) from northeast Canada which travelled a median of 74 days during their autumn migration but only 18 days (24%) during spring (Spencer et al., 2014).

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However, not all tracked species showed this seasonal difference, especially if facing headwinds on the return trip. For example Common Diving Petrels (Pelecanoides urinactrix) from New Zealand covered their outward journey to the Antarctic Polar Front in about 8 days but took around 34 days over their return in spring (Rayner et al., 2017). Longtailed Skuas (Stercorarius longicaudus) also took longer over their spring journey (90 vs 62 days), in their case because of extra feeding on route, assumed to build the body reserves needed for breeding, and thus paralleling the arcticnesting waterfowl mentioned above (Seyer et al., 2021). Comparison with landbirds. High speeds in pelagic seabirds were recorded from individuals travelling almost nonstop, with no prolonged re-fuelling periods to break their journeys. They are therefore more appropriately compared with non-stop flights by tracked landbirds, which give some even faster speeds. For example Bar-tailed Godwits completed the 10,260 km non-stop oversea journey from Alaska to New Zealand in 7.3 days, giving an average speed of 1416 km/day, faster than recorded for any seabird, but achievable as a non-stop flight only with enormous predeposited fuel reserves and a mostly following wind (Gill et al., 2009). Other record speeds from landkhsbirds in nonstop (mainly oversea) migration include 1355 km/day from Great Knots (Calidris tenuirostris) (Battley et al., 2001a,b), 1344 1992 km/day from Brent Geese (Branta bernicla) (Dau, 1992), 1392 km/day from Canada Geese (Branta canadensis) (Gill et al., 1997), 1182 km/day from Amur Falcons (Falco amurensis) (Meyburg et al., 2017) and 1280 km/day from Tree Swallows (Tachycineta bicolor) crossing the Gulf of Mexico (Bradley et al., 2014). However, the current long-distance speed record is held by Great Snipes (Gallinago media), in which some individuals travelled an average of 5849 km between northern Sweden and Africa in 68 hours, giving an average speed of 2089 km per 24-hour day (Lindstro¨m et al., 2021). These various landbirds appeared not to make stops of any kind during their migrations, but the possibility that the geese may have rested for brief periods on the sea cannot be excluded. In any case the travel speeds of all these landbirds exceeded by a broad margin those of albatrosses and shearwaters mentioned above.

PROPORTION OF MIGRATION SPENT IN FLIGHT Knowledge of the duration of migration, obtained from ring recoveries or tracking devices, together with knowledge of the usual flight speed, enable us to calculate how much of the total journey time different species spend on the wing (Table 9.5). For example Common Chaffinches (Fringilla coelebs) usually leave northern Finland in the first half of September and reach their wintering areas in France and Iberia around mid-October, the complete journey taking 5 weeks. The birds thus cover 3000 km at an average of 86 km/day. As they could cover 86 km in 3 hours, and the whole distance (if they could fly non-stop) in 105 hours, they must have spent up to 88% of their total 5-week journey stationary, giving a ratio of flight-to-stopover of about 1:7. This agrees with the theoretical estimate given earlier for birds of this size. Because the energy requirement per hour of flight is generally greater in large birds, and their re-fuelling rates are lower, they take longer to accumulate the fuel necessary for a standard journey than do small birds. Taking an extreme example, five Bewick’s Swans tracked on their autumn migration between Siberia and the Baltic region travelled 2023 km in 34 days, on average (Beekman et al., 2002). With a mean flight speed of 64 km/h, an estimated 32 hours was spent on the wing, giving a flight-to-stopover ratio of 1:25. In spring, the equivalent figures from two birds were also 1:25. These estimates excluded the initial fattening period, but they broadly agree with theoretical predictions, and give some idea of the small proportion of the overall journey time spent by large birds in flapping flight when migrating overland. We should not be misled by the fact that some swans can cross 1000 km of sea in less than two days (see later), because this makes no allowance for the period of prior fuel deposition. In practice, of course, birds often stay longer at stopovers than is needed solely to accumulate fuel (Chapter 14), and in addition, their energy costs in flight are greatly influenced by wind conditions. Estimates of flight-to-stopover ratios are given for some other species on largely overland flights in Table 9.5. They generally support the notion that, among birds that travel by flapping flight, small species spend a greater proportion of the total journey time in flight than larger species. The smallest ratios of around 1:1 1:2 were recorded from two species of swifts which habitually feed on the wing so could get much of their food on migration, while the largest ratios of 1:13 1:31 were from large waterfowl which travel by strenuous flapping flight. Considerable variation was apparent within species, with mean values of 1:4 1:7 from different studies of Peregrines, and of 1:3 1:7 from different studies of Ospreys (Newton, 2008), and 1.3 1.9 for different studies of Northern Wheatears (Table 9.5). These estimates ignore long sea-crossings by geese and swans mentioned above, because the intensive prior fuelling periods were not recorded. For the same reason, all the estimates given in Table 9.5 should be regarded as minimal values. The situation in soaring birds is different. In almost all the species for which relevant data are available, the flightto-stopover ratios in adult birds varied between 1:3 and 1:7, reflecting the much reduced time spent on stopovers

Speed and duration of migratory journeys Chapter | 9

175

TABLE 9.5 Proportion of spring migration spent in flight. Ratio flight:stopover periods represent minimum possible re-fuelling periods because they do not allow for fuel deposition before the start of migration. Figures are mean values from samples of at least five individuals for birds making mainly overland journeys. Species

Distance (km)

Time (days)

Flight speed (km-h)

Time in flight (days)

Ratio flight to stopover

Source

Tawny Pipit (Anthus campestris)

4470

46

30.0

6.2

1:6

Briedis et al. (2016a)

Semi-collared Flycatcher (Ficedula semitorquatus)

5432

49

34.2

6.6

1:6

Briedis et al. (2016b)

Northern Wheatear (Oenanthe oenanthe)

4218

36

47.1

3.7

1:9

Schmaljohann et al. (2012)

Northern Wheatear (O. oenanthe)

14,600

55

47.1

12.9

1:3

Bairlein et al. (2012)

Red-backed Shrike (Lanius cullurio)

11,862

63

46.4

10.7

1:5

Tøttrup et al. (2012)

Snow Bunting (Plectrophenax nivalis)

2147

22

37

2.4

1:8

McKinnon et al. (2016)

Western Kingbird (Tyrannus verticalis)

2378

11

34

2.9

1:3

Jahn et al., (2013)

Great Reed Warbler (Acrocephalus arundinaceus)

7083

32

25.6

11.5

1:2

Lemke et al. (2013)

Barn Swallow (Hirundo rustica)

10,423

69.5

40.7

10.7

1:5

Hobson et al. (2015)

Barn Swallow (H. rustica)

10,663

31

40.7

10.9

1:2

Briedis et al. (2018a,b,c)

Common Cuckoo (Cuculus canorus)

9136

101

37.4

3.8

1:9

Willemoes et al. (2014)

European Nightjar (Caprimulgus europaeus)

8039

82

32

10.5

1:7

Norevik et al. (2017)

Common Swift (Apus apus)

9208

29

38.2

10.0

1:2

A˚kesson et al. (2016)

Pallid Swift (Apus pallidus)

4706

11

37.8

4.8

1:1

Norevik et al. (2018)

Whooper Swan (Cygnus Cygnus)

2940

53.4

63.0

1.94

1:26

Kanai et al. (1997)

Bewick’s Swan (Cygnus columbianus bewickii)

1871

32

64.0

1.22

1:24

Beekman et al. (2002)

Brent Goose (Branta bernicla)

5004

42

59

3.53

1:13

Green et al. (2002)

Barnacle Goose (Branta leucopsis)

2964

40

63

1.97

1:19

de Boer et al. (2014)

Greater White-fronted Goose (Anser albifrons)

3900

83

64

2.54

1:31

Ko¨lzsch et al. (2016)

Barrows Goldeneye (Bucephala islandica)

986

18.6

50

0.82

1:22

Robert et al. (2002)

Lesser Black-backed Gull (Larus fuscus)

7082

42

52

5.7

1:8

Bustnes et al. (2013)

Dunlin (Calidris alpina),

6016

39

58

4.32

1:8

Pakanen et al. (2018)

Common Ringed Plover (Charadrius hiaticula)

6503

54

58

4.7

1:10

Hedh et al. (2021)

Passerines

Near-passerines

Large non-passerines

(Continued )

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The Migration Ecology of Birds

TABLE 9.5 (Continued) Species

Distance (km)

Time (days)

Flight speed (km-h)

Time in flight (days)

Ratio flight to stopover

Source

White Stork (Ciconia ciconia)

1105

69

33

14.1

1:4

Berthold et al. (2004)

Egyptian Vulture (Neophron percnopterus)

5304

25

38

5.84

1:3

Buechley et al. (2018)

Montagu’s Harrier (Circus pygargus)

5306

35

38

5.85

1:5

Trierweiler et al. (2014)

Western Marsh Harrier (Circus aeruginosus)

5096

34

44

4.87

1:6

Strandberg et al. (2008)

Red Kite (Milvus milvus)

1913

13.8

45

1.77

1:7

Pfeiffer & Meyburg (2009)

5872

26

45

5.4

1:4

Martell et al. (2001)

8247

42

44

7.8

1.4

Fuller et al. (1998)

Soaring birds

Osprey (Pandion haliaetus)a Peregrine (Falco peregrinus)

a

Notes: Flight speeds for most species from Bruderer & Boldt, 2001, Alerstam et al., 2007, for Brent Goose from Green & Alerstam, 2000. . a Partly flapping and partly soaring/gliding.

(Table 9.5). These values are generally much lower than equivalent figures from similar-sized birds that migrate by flapping flight, and some are lower even than those from small passerines. They re-affirm the great advantage of soaring flight for large birds: namely, soaring needs much less feeding time, so gives faster overall migration speeds. All the values quoted in Table 9.5 were from adult birds; the non-breeding immatures of some species, under less pressure to return on time to breeding areas, often showed more leisured spring journeys.

PENGUINS Because penguins migrate entirely by swimming, their migration speeds are not comparable with those of other birds. Ten Magellanic Penguins (Spheniscus magellanicus) tracked northward up the coast of Argentina had average travelling speeds of 1.1 1.9 km/h, higher initially and slower later in the journey when the birds encountered better feeding areas (Pu¨tz et al., 2000). Higher mean speeds were recorded for Ade´lie Penguins (Pygoscelis adeliae) on migration, at 1.8 3.4 km/h (Davis et al., 1996). These mean rates translate to average daily distances of 26 46 and 43 82 km in the two species, which are not dissimilar to the average daily distances recorded for many short-distance passerine migrants (including stopovers). Other travelling speeds have been reported for various penguins in the breeding season when they were feeding chicks, with measures of 3 4 km/h for Southern Rockhopper Penguins (Eudyptes chrysocome) (Pu¨tz et al., 2003), 7 km/h for Magellanic Penguins (Boersma et al., 2009), and 7 10 km/h for the larger King Penguins (Aptenodytes patagonicus) (Pu¨tz et al., 1998). These are greater than the speeds achieved on migration.

MIGRATION AND GEOGRAPHICAL RANGE The durations of a breeding cycle (from egg-laying to the independence of young) and of moult increase with body size in birds, leaving less time to complete a return migration within an annual cycle. This may constrain the length of a total migratory journey that can be undertaken by large bird species, and hence their geographical ranges. Among large waterfowl, radio-tracked Bewick’s Swans spent about 33% of the year on migration, while storks and cranes gave figures up to 59% of each year in different populations, and raptors up to 42% of each year in different populations (Newton, 2008). As expected, the migration period depended on the journey, with species making the longest migrations taking the longest periods. It would be hard to imagine some large species being able to perform even longer migrations without compromising reproduction or moult (Hedenstro¨m & Alerstam, 1998). The problem is perhaps especially acute in some species of geese and swans which seem unable to begin migratory fattening until vegetation growth begins in spring, providing the necessary increase in food supply. Such species also make some of the slowest journeys (including feeding periods), and it is perhaps not surprising that no arctic-nesting goose or swan species migrates further

Speed and duration of migratory journeys Chapter | 9

177

than about 6000 km, while journeys twice this length are performed by many smaller birds, and also by large soaring species, such as Steppe Eagles (Aquila nipalensis) and Lesser Spotted Eagles (Clanga pomarina) which require less fuelling time. But in large species especially, any constraint on migration distance could limit the geographical range.

CONCLUDING REMARKS Calculations of maximum possible theoretical migration speeds are informative, even though not all birds necessarily attempt to migrate as quickly as possible. Instead of being ‘time minimizers’, they may be ‘load minimizers’, migrating in short stages requiring no great fuel deposition, thus reducing their overall energy need and predation risk (Alerstam & Lindstro¨m, 1990; Chapter 5). In addition, few birds can feed at the maximum possible rate recorded for their species, because inexperience, poor food supplies, high predation risk or competition may limit the daily intakes of most individuals, and hence rates of fuel deposition. Birds may also at times be delayed by adverse weather long beyond the date at which they become ready to depart. All these types of constraints tend to slow the overall migration and raise the variability within populations. In addition, at least in autumn, some species may gain no advantage in passing rapidly through areas of abundant food, if they cannot be sure of finding plentiful supplies further along the migration route. They would be better to stay and feed while ever the food lasts. The autumn journeys of irruptive seed-eaters, for example vary greatly in timing from year to year, according to the seed crops encountered, and in most years, travel speeds are by no means close to the maximum possible (recall the slow rates of progress shown by irruptive species in Figure 9.3). For these various reasons, therefore, we can expect that most birds do not normally migrate at the theoretical speeds of which they are capable. It is perhaps in ideal conditions in spring, when birds are heading for their breeding areas that they are most likely to approach their maximum speeds, but even then most birds cannot migrate long ahead of the appearance of suitable food supplies. The fact that many species follow particular isotherms, snow melt patterns or ‘green waves’ towards their breeding areas emphasizes the constraining effects of food supply on the progress of spring migration (Chapter 15). Except where stated otherwise, all the measures of migration speeds given in this chapter exclude the initial fuelling period before birds set off on their journeys. Although this period forms part of the migration, it can be determined only by a separate study. To judge from recorded rates of weight gain, small passerines take from 1 day to 3 weeks to accumulate the required body reserves, while long-distance shorebirds and waterfowl can take several weeks, depending on the length of the subsequent flight.

SUMMARY Depending on the distance travelled, a one-way migratory journey can last from several hours up to several months. Some species that migrate long distances between northern and southern hemispheres spend around half of each year on migration. Most migration time is spent on accumulating body reserves to fuel the flights. Among passerines, species that migrate at night tend to make faster progress than diurnal migrants, long-distance migrants make faster progress than short-distance migrants of similar size, and species that leave their breeding areas early in the migration season migrate more rapidly than later migrants (including partial and irruptive migrants), and birds that leave their wintering areas early in the migration season migrate more slowly than those that leave later. The shortening daylengths as autumn progresses may account for the fact that migrants bound for the tropics migrate early in the season (5long feeding days) and thereby achieve relatively fast migration speeds, while short-distance migrants migrating late in the season (5shorter feeding days) travel more slowly. Large species have relatively higher flight costs than small ones and take longer to accumulate the necessary body reserves. The ratio of flight to stationary time during the migration periods of small passerines is typically around 1:7, matching theoretical predictions, and in larger species that travel by flapping flight the recorded ratios are around 1:1 to 1:3. Among soaring species, recorded ratios vary between 1:3 and 1:7. However, these ratios can vary greatly between populations and between individuals in the same population, apparently depending largely on prevailing weather and fuel deposition rates. Individuals from the same breeding area have been found to vary up to several-fold (in extreme cases up to 12-fold) in the time they take to complete the same journey. Nevertheless, maximum observed migration speeds in different species are fairly close to their maximum theoretical estimates. Although they need to spend less time feeding, small passerines do not always achieve higher migration speeds than larger species that also travel by flapping flight: typically 50 200 km/day in small songbirds versus 50 250 km/day in larger species. Among large birds, species that travel by soaring gliding flight achieve faster average speeds than

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The Migration Ecology of Birds

similar-sized species that travel by flapping flight, mainly because soaring species do not need to accumulate and maintain such large fuel reserves. Some pelagic seabirds that use soaring gliding flight travel even faster, with mean speeds of around 1000 km/day recorded from some albatrosses and shearwaters. Such high speeds are also achieved by some waders and waterfowl making long oversea flights. In favourable winds with sufficient body reserves, geese have been found to fly 5000 km over water within 60 hours, giving mean speeds of nearly 2000 km per 24-hour day, or around 80 km/h. Some waders travelling long distances over water have been recorded at average speeds exceeding 1300 km/day, and the record is held by Great Snipes travelling from northern Europe more than 5000 to central Africa that reached more than 2000 km/day. All these species fly by flapping flight and achieve greater speed than the fastest albatrosses and other pelagic birds which travel by soaring gliding flight. Environmental conditions, notably food availability at stopover sites, more often limit the rate of progress on spring migration than on autumn migration, and many species follow patterns of ice melt or vegetation growth in moving to higher latitudes in spring. In some species that travel by flapping flight, fuelling times associated with large body size may make it impossible to breed, moult and migrate long distances within 1 year, and could thereby limit their migration distances (and hence their geographical ranges).

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Selstam, G., Sondell, J. & Olsson, P. (2015). Wintering area and migration routes for Ortolan Buntings Emberiza hortulana from Sweden determined with light-geologgers. Ornis Svecica 25: 3 14. Sergio, F., Tanferna, A., De Stephanis, R., Jime´nez, L. L. Blas, J. et al. (2014). Individual improvements and selective mortality shape lifelong migratory performance. Nature 515: 410 13. Seyer, Y., Gauthier, G., Beˆty, J., Therrien, J.-F. & Lecomte, N. (2021). Seasonal variations in migration strategy of a long-distance Arcticbreeding seabird. Mar. Ecol. Prog. Ser. 677: 1 16. Shaffer, S. A., Tremblay, Y., Weimerskirch, H., Scott, D. Thompson, D. R. et al. (2006). Migratory Shearwaters integrate oceanic resources across the Pacific Ocean in an endless summer. Proc. Natl. Acad. Sci. U.S.A. 103: 12799 802. Sokolov, V., Sokolov, A. & Dixon, A. (2018). Migratory movements of Peregrine Falcons Falco peregrinus, breeding on the Yamal Peninsula, Russia. Ornis Hungarica 26: 222 31. Spencer, N. C., Gilchrist, H. G. & Mallory, M. L. (2014). Annual movement patterns of endangered Ivory Gulls: the importance of sea ice. PLOS ONE 9 (12): e115231. Stenhouse, I. J., Egevang, C. & Phillips, R. A. (2013). Trans-equatorial migration, staging sites and wintering area of Sabine’s Gulls Larus sabini in the Atlantic Ocean. Ibis 154: 42 51. Strandberg, R. & Alerstam, T. (2007). The strategy of fly-and-forage migration, illustrated for the Osprey (Pandion haliaetus). Behav. Ecol. Sociobiol. 61: 1865 75. Strandberg, R., Klaassen, R. H. G., Ha˚ke, M., Olofsson, P., Thorup, K. & Alerstam, T. (2008). Complex timing of Marsh Harrier Circus aeruginosus migration due to pre- and post-migratory movements. Ardea 96: 159 71. Strandberg, R., Klaassen, R. H. G., Olofsson, P. & Alerstam, T. (2009). Daily travel schedules of adult Eurasian Hobbies Falco subbuteo variability in flight hours and migration speed along the route. Ardea 97: 287 95. Stutchbury, B. J. M., Gow, E. A., Done, T., MacPherson, M., Fox, J. W. & Afanasyev, V. (2011). Effects of post-breeding moult and energetic condition on timing of songbird migration into the tropics. Proc. R. Soc. Lond. B 278: 131 7. Tedeschi, A., Sorrent, M., Bottazzo, M., Spagnesi, M. Telletxea, I. et al. (2020). Inter-individual variation and consistency of migratory behaviour in the Eurasian Woodcock. Curr. Zool. 66: 155 63. Terraube, J., Arroyo, B. E., Bragin, A., Bragin, E. & Mougeot, F. (2012). Ecological factors influencing the breeding distribution and success of a nomadic, specialist predator. Biodivers. Conserv. 21: 1835 52. Therrien, J.-F., Pinaud, D., Gauthier, G., Lecompte, N., Bildstein, K. L. & Beˆty, J. (2015). Is pre-breeding prospecting behavior affected by snow cover in the irruptive Snowy Owl? A test using state-space modelling and environmental data annotated via movebank. Movement Ecol. 3 (2015): 1. Thorup, K., Alerstam, T., Ha˚ke, M. & Kjelle´n, N. B. (2003a). Bird orientation: compensation for wind drift in migrating raptors is age dependent. Proc. R. Soc. Lond. B 270: S8 11. Thorup, K., Alerstam, T., Ha˚ke, M. & Kjelle´n, N. (2003b). Can vector summation describe the orientation system of juvenile Ospreys and Honey Buzzards? An analysis of ring recoveries and satellite tracking. Oikos 103: 350 9. Tøttrup, A. P., Klaassen, R. H. G., Kristensen, M. W., Strandberg, R. Vardanis, Y. et al. (2012). Drought in Africa caused delayed arrival of European songbirds. Science 338: 1307.

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Chapter 10

Finding the way: senses, displacements and social influences

Blackpoll Warbler, famed for its long over-sea migration ‘on their journeys, the migrants not only travel vast distances overland, but also cross pathless seas and oceans. The question is how do they find their way? How are they guided? Here we are face to face with one of the greatest mysteries to be found in the animal kingdom.’ William Eagle Clarke, 1912.

Many birds are capable of migrating, year after year, from their customary nesting sites to exactly the same winter quarters, sometimes using the same refuelling sites on successive journeys. Young birds migrating alone can find their way unaided by experienced adults to the usual wintering areas for their population, and back to their natal areas the following spring. Yet for some species breeding and wintering areas may lie half a world apart on different continents. Some pelagic seabirds cover enormous distances during their foraging flights, as well as during their migrations, over what appears to us as featureless ocean, yet they can return repeatedly on a straight course to the tiny islands where they breed. How do birds achieve these remarkable feats of navigation over such huge distances? To migrate effectively, birds need a sense of where they are and need to be, a sense of direction, an ability to navigate from one place to another, and a sense of time, both seasonal and diurnal. In short, they need the equivalents of a compass, map, clock and calendar, together with a good memory, all packed into a brain that in some birds is smaller than a pea. It is not just a question of finding the way, for birds must also know where on their journeys to change direction or to accumulate extra body reserves in preparation for a long flight. The fact that birds can respond appropriately at specific places on their route further implies that they possess some geographical positioning sense an ability to detect and react in an appropriate manner to conditions at particular locations. Over time, ornithologists have managed to unravel some of these mysteries but others remain unresolved. This chapter concentrates on the sensory equipment that allows birds to perform such impressive journeys, some of the experiments that indicate what birds are capable of in terms of navigation, and the ways that individuals interact on their journeys. The various methods of navigation are discussed in Chapter 11.

The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00026-9 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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SENSORY SYSTEMS Birds have the same senses as we do (sight, hearing, smell, taste and touch), plus at least one additional sense that we lack, namely an ability to detect and read the earth’s magnetic field (reviews: Birkhead, 2012; Martin, 2020). All these senses, except taste and touch, are apparently used in navigation (Chapter 11). Vision. Relative to skull size, the eyes of birds are generally much bigger than ours and provide greater acuity. Some birds can detect small objects at 4 5 times the distance that we can. In addition, many birds can perceive ultraviolet and plane-polarised light facilities beyond our own. However, in terms of their light-gathering power, the eyes of most diurnal birds are probably much the same as ours, enabling these species to fly in the dark through the open airspace and to see the stars above and the landscape below (Martin, 2020). Collisions with obstacles such as radio towers or wind turbines occur mainly on dark misty nights when vision is restricted. The eyes of owls and other nocturnal birds have exceptional light-gathering power but such species form only a small minority of all birds. Reading most navigational cues depends on the eyes which are therefore as crucial to migration as to normal life. Olfaction. The old idea that most birds have only a poor or moderate sense of smell may need revision. In some species, notably procellariiform seabirds (albatrosses, petrels and shearwaters), this sense is well developed, supported by massive olfactory bulbs in the brain (Bang & Cobb, 1968; Wenzel, 1991). These birds use olfaction to detect food, and any fish offal dropped on the sea surface will attract them from wide distances (as in the process of ‘chumming’ used by birdwatchers to attract birds at sea). As well as food-finding, olfaction may be one of the means by which procellariform birds locate their nesting colonies, even individual nesting burrows, often on remote islands (Bonadonna et al., 2003), and there is increasing evidence for the use of olfaction in seabird navigation (Chapter 11). Among landbirds, much research concerns homing pigeons which are capable of navigating home in a familiar area using their sense of smell (Chapter 11). On a local basis, they could learn the surrounding odour patterns and use them in the same way they might learn landscape features to find their way by sight. Hearing and pressure senses. Birds also have a generally well-developed auditory sense, allowing individual migrants to detect the calls of other migrating birds at night. They can also detect infrasound, the low-frequency noises (down to 0.05 Hz) which we cannot hear but that can travel over hundreds of kilometres (Kreithen & Quine, 1979; Hagstrum, 2001). These sounds are mostly made by physical processes, such as wind against mountain ridges or waves against shorelines or large waterfalls. From studies of pigeon hearing, it has been deduced that, through infrasound, these birds could detect Niagara Falls from more than 400 km away (Bedard, 2021). Such sounds could give strong directional clues to birds able to detect them, but it is unknown how much birds use them in navigation or hazard avoidance (Keeton, 1980; Wallraff, 2003). Birds also seem able to detect changes in barometric pressure (Hein et al., 2011) and to perceive wind direction and speed during flight, probably by reference to the ground below. These abilities enable birds to sense impending weather systems, select optimal flight altitudes and sometimes correct for wind drift when on migration (Chapter 4). Magneto-reception. The fact that birds and many other animals can detect and respond to the earth’s magnetic field is hard for us to understand because we have no magnetic sense ourselves, and neither birds nor we have obvious external organs by which to detect it. But unlike light, smells and sound, magnetic sensations can pass through body tissues. Theoretically, this means that an organism could detect magnetic fields via chemical reactions or other means, almost anywhere within its body. Two main mechanisms of magneto-reception have been proposed in birds. One involves iron-rich particles, such as magnetite, a specific form of permanently magnetic iron oxide. Magnetic-iron compounds are found in many organisms, and in birds are located in the beak region, in tissues that surround the olfactory nerve and bulbs, as well as in bristles that project into the nasal cavity (Beason & Nichols, 1984; Falkenberg et al., 2010; Wiltschko & Wiltschko, 2019). The structure they comprise could function in orientation by measuring magnetic intensity and perhaps also the alignment of force lines as a component of a navigational map (Wiltschko & Wiltschko, 2007, 2019). This information is transmitted to the brain through the ophthalmic branch of the trigeminal nerve. The second proposed mechanism is based in the eyes. It involves a magnetically-sensitive chemical reaction entailing electron transfer between donor and acceptor molecules a ‘radical pair’ mechanism involving directiondependent reactions in specialized photo-pigments in the retina (Ritz et al., 2000, 2004). This system can apparently operate only under short-wavelength light (the ultraviolet-blue-green end of the spectrum). From the eyes, information on the direction of the magnetic field is thought to be transmitted via the ophthalmic branch of the trigeminal nerve to a specific forebrain region (cluster N, active in night-time vision), where it is decoded to yield compass information (Mouritsen et al., 2005). The roundness of the eye allows force lines of any alignment to be detected, and hence could theoretically indicate both the present location and direction towards a goal (Ritz et al., 2004). Cryptochrome is a likely receptor molecule because it is the only known animal protein in which the absorption of photons leads to the formation of radical pairs (Ritz et al., 2000; Mouritsen, 2018).

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Evidence suggests that birds use radical pair processes in the eyes to gain directional information (the magnetic compass), while the magnetite-based mechanism is implicated in the detection of magnetic intensity and could be used mainly as a positioning (map or signpost) sense (reviews: Wiltschko & Wiltschko, 2007, 2019; Mouritsen & Ritz, 2005). Together, the two mechanisms provide different components of a navigational system that could in theory enable birds to find their way for long distances over land or sea. A third possible means of magneto-reception has been mooted, involving the vestibular system of the inner ear (mainly concerned with balance), and potentially based on an electromagnetic induction mechanism (Kobylkov et al., 2020). But further research is needed to check on this potential mechanism and for its possible involvement in navigation. While birds can undoubtedly detect and respond to the earth’s magnetic field and use it for navigation, we are still far from understanding how they do it.

ORIENTATION AND NAVIGATION In discussing route finding, it helps to separate orientation (determining a compass bearing, the appropriate direction) from navigation (maintaining a course from a starting point to a specific goal). The initial setting of a compass course can be done with information from the starting point alone, whereas navigation to a pre-determined goal requires both directional and other information on the route. To navigate a route, animals are expected to need the equivalents of a compass and a bi-coordinate map, both provided by environmental cues. Our own bi-coordinate maps use latitude and longitude, but birds must presumably use some equivalent natural gradients, which vary in two or more different directions. Some early studies of the migratory capabilities of birds involved trapping large numbers on autumn migration, transporting and releasing them in a distant location, and using the resulting ring recoveries to find where they went (Figure 10.1a). Such experiments revealed that naive young birds behaved differently from experienced adults. Young birds on their first autumn migration did not correct for their displacement and failed to reach their expected wintering areas. Instead, they continued on their usual migratory heading for about the same distance they would normally have travelled from the capture site. The inference was that inexperienced birds migrated on the basis of information expressed as a direction and distance from the starting point, distance being controlled by the duration of migratory activity (Chapter 22). The information could be equivalent to an instruction like: ‘travel for 6 weeks towards the southwest’, or, in cases of non-straight routes: ‘travel for 6 weeks toward the southwest and then for 5 weeks toward the south-southeast’ (Wiltschko & Wiltschko, 2003). This system is known variously as clock-and-compass, bearing-anddistance or vector migration. In contrast to young birds, experienced adults which had presumably travelled the route before made the necessary corrections after displacement, changing direction and reaching their former wintering areas. Homing to a known site is more complicated than the ability to head only in a particular compass direction because it involves true navigation, involving a map sense an ability to head towards a specific point on the earth’s surface from some distant location. It is generally assumed that, to build a useable mental map, birds initially gather information within their home area, learn predictable spatial gradients of environmental cues within it and then extrapolate from those gradients to unfamiliar areas beyond the familiar range the ‘gradient hypothesis’. The inherent instructions from clock-and-compass systems obviously vary between species, according to their particular breeding and wintering areas, and also within species for birds from different parts of the breeding range. One clear example is provided by ‘migratory divides’ in Europe, where many birds nesting in the western half of Europe migrate southwest to enter Africa around the west end of the Mediterranean, whereas birds of the same species in the eastern half of Europe migrate southeast to enter Africa via the mainly land-based route around the eastern Mediterranean. In this way, many birds avoid crossing the Mediterranean at its widest parts. Experiments have confirmed that birds on the west and east sides of Europe inherit different directional preferences and time programmes in line with their natural migration patterns (Chapter 22).

DISPLACEMENT EXPERIMENTS The biggest displacement experiments undertaken involved Common Starlings (Sturnus vulgaris) which migrate westsouthwest in autumn through the Netherlands to winter in northern France and southern Britain. Over a period of years, Perdeck (1958, 1967) caught and ringed more than 19,000 Starlings during their autumn journey. He released about 7500 on site to act as controls and transported 11,500 others by air 500 km south-southeast from the capture site for release in Switzerland (Figure 10.1b). The subsequent ring recoveries from translocated juveniles were on a line west-

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FIGURE 10.1 (a) Displacement experiment, showing the difference in response to displacement between adult birds (which homed to a familiar wintering area) and juvenile birds which flew in an appropriate direction, but without correcting for displacement off course. (b) Difference in recovery patterns of adult and juvenile Common Starlings (Sturnus vulgaris) displaced from their migration route through the Netherlands about 500 km south-southeast to release sites in Switzerland. Filled circles show recoveries of juveniles and open circles of adults during the ensuing autumn winter. Both panels based on Perdeck (1958), with this version modified from Newton (2008) and Piersma et al. (2020).

southwest of the release site and extended for a similar distance as usual, bringing them into southern France and northern Iberia. This indicated that the translocated juveniles had kept some pre-determined directional preference and normal migration distance but had not corrected for their displacement. They therefore migrated parallel to the normal route and wintered south of the regular wintering area for their population. The adults, in contrast, which had already experienced the normal wintering area, corrected for their displacement, and after release headed northwest towards their normal wintering areas with which they were familiar. They had evidently ‘realised’ they were off course at the release site and took a different direction from usual to correct this. The age-related (or experience-related) difference in behaviour occurred whether the birds were released in separate juvenile and adult groups or in mixed-age groups. Recoveries from subsequent years showed that, while juveniles tended to return to the new wintering areas reached after their displacement, both age groups continued to return to their original natal/breeding areas with which they were familiar. The conclusions were that (1) autumn-migrating adult Common

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Starlings used goal navigation (homing) to reach their known wintering areas, whereas the juveniles used onedirectional orientation, moving on a fixed bearing for a fixed distance; and (2) juveniles were able to fix both their personal breeding and wintering areas in their first year and migrate between these areas in subsequent years by goal navigation, a process dependent on learning. In another experiment, Starlings were transported in the migration season from the Netherlands to Barcelona in eastern Spain (Perdeck, 1967), an area much favoured by wintering Starlings. Despite being transported to a suitable wintering area, the displaced youngsters moved on west for several hundred kilometres across the width of Spain. The implications were again that the length and direction of the migratory journey were controlled by internal influence and that migration continued in the normal direction from the release site while ever the drive to migrate persisted. These experiments formed important milestones in the study of bird navigation. Many similar experiments on other species, also based on ringing, gave similar results, with juveniles and adults differing in behaviour (review: Newton, 2008). In a more recent experiment with longer-distance migrants, White-crowned Sparrows (Zonotrichia leucophrys) were transported across North America from west side to east side, where they were released and their initial departure paths determined by radio-tracking. As in the above experiments, the juveniles continued in their normal migratory direction heading southward, whereas the adults changed course, now heading west-southwest towards their traditional wintering area, apparently attempting to compensate for their transcontinental displacement of 3700 km (Thorup et al., 2007). These sparrows thus behaved like Starlings, even though their migrations were longer and they travelled individually rather than in flocks. With birds caught on migration, such as Perdeck’s Starlings, it could be argued that, rather than the directions being innate, they were learned on the earlier part of the journey, before the birds were caught and ringed (Piersma et al., 2020). However, this was not true for other studies in which the birds were ringed in their breeding areas before migration began or were raised and tested singly in captivity, using orientation cages (Chapter 22). Despite the lack of opportunity to learn from older birds, these juveniles still showed directional preferences typical for their population. However, one alternative explanation remains open for all the field experiments, namely that juveniles had the ability to correct for their displacement but were not motivated to do so. They had never visited the wintering area before so had no attachment to particular parts of it. None of them were displaced so far that they would end up outside the wintering range of their species. Additional evidence for pre-determined directional preferences came from other early field experiments, in which young birds of various species were held in their natal areas until all other individuals of their species had left. After their release, the young birds were found from subsequent sightings and ring recoveries to have migrated in the direction normal for their population, despite the assumed lack of more experienced birds to guide them (for White Storks (Ciconia ciconia), see Schu¨z, 1949; for Blue-winged Teal (Spatula discors), see Bellrose, 1958). In yet other experiments young birds were released outside their normal breeding range and found from ring recoveries to migrate in a direction more or less expected for their population (for White Storks, see Schu¨z, 1938; Bloesch, 1956, 1960; for Herring Gull (Larus argentatus), see Drost, 1955; for Blue-winged Teal, see Vaught, 1964). However, no firm conclusions could be drawn from the directions taken, because they would be expected to be generally southward in both natal and release areas. But at least these experiments showed that young birds were not dependent on adults to stimulate and indicate the general direction of their migration. Moreover, the fact that juveniles of all these species, whether caught on breeding or migration areas, travelled after displacement approximately the same distance as they normally would, was attributed to the involvement of an internal clock, a long-term time-keeping mechanism (or ‘endogenous rhythm’) which ended migratory behaviour after an appropriate period (Chapter 12). Although this idea came from observations of wild birds, additional evidence came from measuring the period of migratory restlessness in captive birds from different populations (Berthold, 1996). Birds from populations that naturally migrated the longest distances showed the longest periods of migratory restlessness (Chapter 22). All this information collectively was held to support the notion of ‘clock-and-compass’ or ‘vector’ migration, in which young birds had an inherent tendency to migrate in a particular direction for a pre-determined period, behaviour which could get them to a wintering area appropriate for their population.

Other evidence for inherited directional preferences Inheritance of migratory directions is further supported by those species in which juveniles migrate to wintering areas independently of adults. The Common Cuckoo (Cuculus canorus) provides a striking example because the last young leave the breeding areas up to a month after the last adults, yet they still find their way to their African wintering areas (for tracking study, see Vega et al., 2016). These young Cuckoos also seem to migrate independently of one another and also independently of their various foster species, which in any case winter in a range of different areas. The same

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is true for some other cuckoos in which the juveniles leave breeding areas later than adults, including the Pacific Longtailed Cuckoo (Eudynamis taitensis) which breeds only in New Zealand and winters on a wide arc of small Pacific Islands, extending over 11,000 km from Palau in the west to Pitcairn in the east (Gill & Hauber, 2012). Given this distribution, finding the wintering areas would seem to require even greater navigational precision than shown by the Common Cuckoo of Eurasia.

Return of displaced adults to breeding sites Further evidence for a map sense (bi-coordinate navigation) in birds came from experiments in which breeding adults were taken from their nests, marked and released elsewhere. Frequent nest checks could then reveal whether and when the marked owners returned. Experiments on more than 50 species, from songbirds to seabirds, showed some remarkably high rates of return over distances varying from a few kilometres to more than 5000 km, depending on species ˚ kesson, 2003). Some non-migratory species, such as the Eurasian Tree Sparrow (Matthews, 1968; Wiltschko, 1992; A (Passer montanus), returned only in small numbers and only over short distances of up to 10 km, perhaps using their knowledge of the local terrain (Creutz, 1949). Other species returned after transportation over hundreds or thousands of kilometres, sometimes from areas they could never have visited on their normal migrations, so they must have used other more sophisticated means than prior knowledge (Matthews, 1968). Returns over the longest distances were reported from pelagic seabirds. For example in the Layson Albatross (Diomedia immutabilis), 14 of 18 displaced adults returned to their nests on Midway Island in the central Pacific within 30 days, after having been transported between 2116 and 6629 km to six locations lying in different directions from the breeding colony (Kenyon & Rice, 1958; Figure 10.2). These birds showed an extraordinary ability to return quickly over long distances, suggesting that they did not spend much time searching and soon headed homeward. The fastest bird covered 5148 km in 10 days after release, giving a mean speed of 515 km/day. Similarly, a Manx Shearwater (Puffinus puffinus) displaced from Wales to eastern North America managed the return distance of 4800 km in only 12 days, an average of 400 km/day (Matthews, 1968), and two Leach’s Storm Petrels (Hydrobates leucorhous) released off the coast of southern England returned to their nests in New Brunswick in 14 days, averaging 217 miles/day (Billings, 1968). Satellite tracking of displaced birds has given further insight into how birds react to experimental displacements. For example just before their normal departure time in late summer, some adult Common Cuckoos were displaced from their breeding areas in Denmark 2500 km southwest to Spain, well off their normal migration route which ran due south-southeast from Denmark (Willemoes et al., 2015). Six birds that gave meaningful results all headed towards the migration route normally taken by Cuckoos breeding in Denmark and by the non-displaced control birds in the experiment (Figure 10.3). All displaced birds flew towards staging areas normally used by this population during autumn migration, but different individuals travelled to different staging areas and joined their normal migration route at widely FIGURE 10.2 Homing of Laysan Albatrosses (Diomedia immutabilis) breeding at Midway Atoll and displaced to different sites around the Pacific Ocean. Eighteen albatrosses were transported to six different sites between 2116 and 6629 km away, and 14 of them returned to the breeding island within 30 days. From Kenyon & Rice (1958).

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FIGURE 10.3 Tracking of displaced Common Cuckoos (Cuculus canorus) in time and space. (a) post-breeding routes of six adult Cuckoos whose migration was successfully monitored (red tracks) after being displaced from Denmark to Spain (arrow) compared with the migrations of eight adults non-displaced Cuckoos from Denmark and southern Sweden (green tracks: autumn vs spring routes indicated as solid vs dotted lines respectively). Stars indicate final wintering destination and shaded areas indicate population-specific autumn staging areas considered as possible navigation targets. (b) Initial movements of 11 adult Cuckoos within the 15 days following displacement including endpoint directions and mean direction (black dots and solid black line in circle diagram) compared to direction towards origin (red dotted line), first and second staging areas (blue and green triangles) of control birds and first post-breeding departure direction (grey triangle) of control birds. (c) Timing of autumn migration of displaced birds (red lines) compared to control birds (green lines). From Willemoes et al., 2015, re-printed under a Creative Commons Licence.

separated points. Two-headed for known staging areas in Europe, one northeast and the other southeast, before turning southward on the normal route to central Africa. The other four displaced adults headed from Spain across the Sahara in a south or southeast direction towards their usual staging or wintering areas but stopping off in unfamiliar areas on the way. Apparently, these Cuckoos possessed a map sense extending far beyond their population-specific flyway and made their own decisions on how to reach their normal wintering areas.

Return of displaced birds to wintering sites Most experiments involved birds displaced in the breeding season from their nesting places to which they presumably had a strong incentive to return. Other experiments involved the displacement of birds from their normal wintering sites, some from one side of North America to another (Figure 10.4). They showed that birds caught as adults were more likely to

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return in the same or a later winter than birds caught as juveniles and that the return of juveniles depended on how long they had spent at the site before they were caught and moved (Bellrose, 1958; Ralph & Mewaldt, 1975, 1976). In another study, 30 adult and 69 juvenile Sanderlings (Calidris alba) were transplanted from Bodega Bay in California 200 km south (Myers et al., 1988). Overall, 60% of adults but only 4% of juveniles later returned and re-settled in Bodega Bay, either in the same or a subsequent winter (Table 10.1). The age difference was strongest among birds moved in autumn (from which no juveniles returned) but was non-existent among birds moved in winter. By that time the juveniles had apparently been in Bodega Bay long enough to have become attached to the site, and they returned in the same proportion as adults which were familiar with the site from previous winters. Broadly similar results came from earlier displacement experiments involving wintering ducks (McIlhenny, 1934, 1940; Bellrose, 1958).

FIGURE 10.4 Long-distance displacements of Golden-crowned Sparrows (Zonotrichia atricapilla) and White-crowned Sparrows (Zonotrichia leucophrys) from a wintering site at San Jose´ in California to Baton Rouge (Louisiana) and Laurel (Maryland). Shaded area depicts the breeding range of the populations under study. Of 411 birds displaced by aircraft 2900 km east-southeast to Baton Rouge, 26 were re-caught the following winter at their initial capture site in San Jose´. In the next winter, of 660 birds transported to Laurel, 15 were re-caught at their initial capture site in the following winter. Of special interest were six of 22 birds displaced to Laurel after they had already returned from Baton Rouge. All birds are presumed to have returned to the breeding range in the interim, and one was caught on spring migration at an intermediate location; adults returned in greater proportion than juveniles. The rate of return next year by young sparrows to the capture site varied according to the date of displacement. Those displaced before mid-January were less likely to return, possibly because site attachment had not occurred before then. After Mewaldt, 1964; Ralph & Mewaldt, 1975, 1976.

TABLE 10.1 Effects of age and season on the proportions of Sanderlings (Calidris alba) that returned to a wintering site (Bodega Bay) in the same or subsequent winters after being transplanted to another wintering site 200 km to the south. Returned and settled in Bodega Bay after transportation

Did not return to Bodega Bay after transportation

Autumn (October November) Adults

13

5

Juveniles

0

45

Winter (January) Adults

4

Juveniles

3

8 21

Difference between age groups in autumn: χ 5 40.9, P , .001; in winter χ 5 2.2, P , .13. Source: From Myers et al. (1988). 2

2

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Further comments on displacement experiments Overall, it seems that motivated birds can return to any site that they have previously visited, providing the flight lies within their capabilities. However, individuals of migratory species usually return successfully from longer displacement distances, in greater proportions and at higher speeds than non-migratory birds (Matthews, 1968; Wiltschko, ˚ kesson, 2003). Species thus seem to vary in their homing abilities, according to their normal movement behav1992; A iour. The same holds for comparisons between migratory and sedentary populations of the same species, such as Whitecrowned Sparrow (Mewaldt, 1964) or Herring Gull (Matthews, 1968). Experiments with completely sedentary species, such as House Sparrows (Passer domesticus), gave no returns from further than about 12 km. In most homing experiments, the proportions of individuals that returned declined with increasing distance of displacement, and allowing for distance, adults returned in greater proportions than juveniles. But whether migratory or non-migratory, young or old, many birds clearly have a map sense, which they can use at any time of year. The same holds for many other animals subjected to displacement experiments. Birds returning from short distances may use local landmarks as a guide, but those returning over long distances through unknown terrain must use some other means.

UNCERTAINTIES OVER JUVENILES Despite the early displacement experiments, the question remained whether juvenile birds have any sort of inherent location sense and could correct for displacement if motivated to do so. Evidence suggests that at least some species do, including the Common Cuckoos mentioned above. In a further experiment during southward migration, translocated juvenile and adult Common Cuckoos were moved 1800 km to the east from Rybachi on the southern Baltic coast for release in Kazakhstan, and their subsequent journeys were tracked by satellite (Thorup et al., 2020). After displacement, both juveniles and adults travelled individually towards the route of non-displaced control birds to the west. Individuals varied greatly in the tracks taken, and corrections for displacement only became apparent after the birds had travelled more than 500 km. Nevertheless, these findings demonstrated the potential for young Cuckoos to return to their population-specific migration route after displacement, a response typical of experienced adults. This implied the possession of an innate positioning system which allowed first-time migrating Cuckoos to locate their wintering grounds. A similar facility has also been found in some first-time migrants among marine fish, turtles and cetaceans. Other evidence comes from displacement experiments that have tested the directional preference of birds of various species in orientation cages. Some young birds showed no change in directional preference after displacement and thus, like the earlier experiments above, supported the clock-and-compass model (Hamilton, 1962; Mouritsen & Larsen, 1998). Other young birds in similar experiments appeared to change their preferred direction to correct for displacement (real or virtual), taking a direction that would lead them to some place on their normal migration route (Rabøl, 1970, ˚ kesson et al., 2005; Thorup & Rabøl, 2001, 2007; Thorup et al., 2011). Both juveniles and adults were involved 1994; A ˚ kesson et al., 2005). in some long-distance displacements, and both corrected appropriately (notably A Birds that inherit only a specific direction would be expected to show some variation around the mean, and a progressive divergence with increasing distance travelled, producing a fan-like pattern. Ringing and tracking studies show that such a pattern is indeed shown by some species (Chapter 25). But in other species, individuals often fly roughly parallel to one another on the same narrow track (as in Linnet (Linaria cannabina), Newton, 1972; or Common Cuckoo (Cuculus canorus), Willemoes et al., 2014). This would be expected if birds were heading for a restricted area, signalled by specific conditions of some kind. Furthermore, all migrating birds are liable to be drifted off course by cross-winds so would be expected to have evolved some mechanism to correct for this drift. In theory, birds migrating overland might maintain a straight course by reference to landmarks below them, but the same could not hold for birds migrating over open seas, above clouds or flying on dark nights. A striking example of drift correction was shown by satellite-tracked juvenile Ospreys (Pandion haliaetus) migrating over the Atlantic southward towards Caribbean Islands. Despite strong crosswinds and lack of landmarks, these birds maintained day and night remarkably straight tracks for 1500 2000 km over the open ocean (Horton et al., 2014). This implies a very precise navigational system which was more than just directional and could operate in the absence of obvious landmarks. This might be expected in adult birds homing to a known area, but in this case involved youngsters on their first migration that could not have operated on clock-and-compass alone. Instead of ‘clock-and-compass’, the authors suggested the term ‘clock-and-chord’. Nevertheless, not all birds resist crosswinds and occasionally some turn up as vagrants in areas way off route. But even for these, evidence is accumulating that some individuals attempt to correct for their displacement and get back on course. When naturally drifted migrants (including juveniles) were caught and tested in orientation cages or tracked

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TABLE 10.2 Recoveries of vagrant birds ringed in Britain that suggest re-orientation towards the regular range. Species

Usual breeding and wintering range

Subsequent recovery of vagrant

Ring-necked Duck (Aythya collaris)

Breeds across Canada and the northern USA and winters in southern States and Central America

An adult male ringed at Slimbridge, Gloucestershire, March 1, 1977, was shot at Isertoq, southeast Greenland, in May of the same year, suggesting that it was heading northwest to the regular breeding range

Booted Warbler (Hippolais caligata)

Breeds central Palaearctic, and winters in India; nearest population to Britain breeds in Russia

A juvenile ringed at Spurn, Yorkshire, on 16 September 1993 was re-caught at Wetheren, Belgium, on 5 October of the same year, suggesting that it had re-orientated eastwards

Penduline Tit (Remiz pendulinus)

Resident in middle and southern latitudes of continental Europe; nearest population to Britain breeds in Denmark

An adult female ringed at Icklesham, Sussex, in October 1988 was recaught at Kuismaren, Sweden, in May 1989, suggesting that it had re-oriented towards the usual breeding range

Rustic Bunting (Emberiza rustica)

Breeds from Sweden across northern Eurasia and winters in Southeast Asia; nearest population to Britain breeds at 60 N in Sweden

A female ringed and present on Fair Isle during June 12 19, 1963 was recovered in Greece four months later, suggesting that it had re-oriented eastwards

Red-breasted Flycatcher (Ficedula parva)

Breeds from eastern Europe across Eurasia, and winters in India and Southeast Asia

An adult male ringed on Shetland on September 6, 1997 was trapped again in Norway 13 days later, suggesting that it had re-oriented eastwards

Barred Warbler (Curruca nisoria)

Breeds from central Europe east to western Siberia and winters in East Africa

A bird ringed in September 1978 on Fair Isle was recovered in February 1979 in Yugoslavia indicating that it had re-orientated eastward. Similarly, another ringed in Sweden on August 26, 1976 was recovered in Syria on September 16, 1976

Source: From Wernham et al. (2002).

using radio-transmitters (Able, 1977; Evans, 1968; Moore, 1990; Thorup et al., 2011), or when they were subjected to simulated displacement in a planetarium (Rabøl, 1992), they corrected for their displacement or virtual displacement and headed towards their normal route. Furthermore, some juvenile birds caught and ringed as vagrants way off course were later reported from a locality nearer to their normal route, implying that they too were attempting to correct for their displacement (examples in Table 10.2 from among British ring recoveries). So to summarize, the difference between adults and juveniles found in early displacement experiments was not borne out in some subsequent ones, especially those involving long east west displacements. Could it be that, in field experiments, the distance, direction or manner of displacement influenced the way the juveniles responded or could they simply not have been motivated sufficiently in some experiments to correct for their displacement, having never visited the areas previously? Or could it simply be that species vary in their ability to correct for displacements, just as they vary in other aspects of migratory behaviour? The most impressive directional corrections were shown by juvenile and adult long-distance migrants that were displaced predominantly east west, and over distances of 1000 km or more (Kishkinev et al., 2015; Loonstra et al., 2019; Thorup et al., 2020). Birds may have to be at least several hundred kilometres off route before they could detect (or would react to) their displacement. Nevertheless, the implication from these various findings is profound, namely that the juveniles of at least some long-distance species have an innate sense of where they need to be in the non-breeding season, even though they have no previous experience in the area concerned. They can home to an area which has not yet become home, an aspect of navigation to which we will return in Chapter 11.

CONVERGENCE OF MIGRATION ROUTES Acceptance that juveniles, as well as adults, possess some form of map sense and can seek out through some inherent mechanism particular localities (signposts) on their migration routes is consistent with other types of bird behaviour which are hard to explain on a clock-and-compass system alone. This applies particularly to populations which converge to particular pinch-points on their migrations and then diverge again, so that on a map, their migration routes have the form of an egg-timer. Examples include populations which concentrate from wide areas to use a narrow sea-

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crossing (eg Gibraltar), a narrow land bridge (eg Panama) or a localised re-fuelling area on route (Fransson et al., 2005), or head to a small island on a trans-oceanic flight. If Bar-tailed Godwits flying from Alaska to New Zealand diverged only 1 from a straight route, they could miss their destination. Surely they must have some way of finding New Zealand other than by attempting to follow a pre-determined starting direction. These same birds, in response to prevailing wind conditions, take a much more circuitous route back to Alaska, yet throughout the birds behave as though they know their position with respect to their ultimate target area. The same difficulty holds for other birds which migrate to a small island (or archipelago) in a large ocean. Other examples of route constriction have emerged from satellite tracking of birds on migration. For example, adult and juvenile Eleonora’s Falcons (Falco eleonorae) migrating from a wide span of Mediterranean islands to Madagascar through West Africa showed unexpectedly concentrated tracks in the last part of their migration as they precisely reached the west coast of the Mozambique channel to cross at the narrowest part (Figure 25.6; Gschweng et al., 2008; Mellone, 2021); while in a similar targeted movement, adult Eurasian Hobbies (Falco subbuteo) migrating from Sweden concentrated to cross the West African rainforest at its narrowest part, fanning out again on the other side (Strandberg et al., 2009). With rainforest forming a possible ecological barrier, many migrants may cross the equator either at 15 E, like the Hobbies, or at 30 40 E, east of the rainforest where large-scale migration is well documented. To a greater or lesser extent, all these species provide examples of fan-shaped migration patterns in which birds concentrate from a wide span of migration routes to a narrow span as they reach specific points in their journeys. Once they are through these bottlenecks, their tracks may diverge again. Such patterns lead to the view that juveniles (as well as adults) can combine clock-and-compass programmes with some external cues associated with species-specific or population-specific areas situated along the migratory route (signposts) to increase the precision of their journeys. By this means, they might keep one course until they reached signpost A and then change direction to signpost B, and so on until reaching their species-specific wintering area as the final signpost. Such signposts imply in birds an innate response to specific conditions associated with signpost areas, detectable from a distance. This leads to the idea of an inbuilt navigational system serving the same purpose as a global positioning system (GPS), an idea developed further in Chapter 11.

SOCIAL INFLUENCES Many of the experiments discussed above involved single individuals which had to find their own way home. But in normal migration, most birds travel in flocks or loose groups, thus allowing for the emergence of either experienced leaders or collective decision-making, perhaps leading to optimal ‘mean directions’ (Biro et al., 2006). In support of this view, as migrating Eurasian Skylarks (Alauda arvensis) passed overhead, the directional scatter was found to decrease as group size increased (Rabøl & Noer, 1973). The same held in an experiment in which randomly assembled groups of 3 6 homing pigeons showed a reduction in both directional scatter and homing times compared with single birds (Tamm, 1980). In another telling experiment, two groups of pigeons were experimentally manipulated to have different orientation preferences. When single individuals from each group were released together, their track was intermediate between the paths that the birds would have taken if they had been released individually (Burt de Perera & Guilford, 1999). In some species, therefore, individuals are clearly influenced in their migratory directions by their travelling companions. In many bird species, young migrate from their natal areas at the same times as experienced adults, and in some species, notably cranes, swans and geese, the young also travel in family parties with their parents, as known from ringing (called guiding). In one study, all members of a family of Greater White-fronted Geese (Anser albifrons) were tracked throughout their migration, revealing that one or other parent always led the V formation, guiding the young over the entire route (Ko¨lzsch et al., 2020). In some other species, such as Caspian Tern (Hydroprogne caspia), the young travel to wintering areas with their father, separate in wintering areas, but remain faithful to the route in future years (Byholm et al., 2022). So in these species, young birds could learn migration routes from older ones, with appropriate knowledge passed down the generations by cultural transmission. This is a major advantage in species which need to use consistent but restricted migration routes or have only localised re-fuelling places along their flyways (eg swans, geese and cranes). Without the benefit of socially acquired knowledge, many young birds could find themselves in unsuitable places for migration or foraging and suffer the consequences. But adherence to traditional sites does not, of course, prevent birds from changing their routes and foraging places if the need arises. The young chicks of some auk species (guillemots, Razorbill (Alca torda), Synthilborhamphus murrelets) accompany their parents for their first few weeks of life on route to their wintering areas, but it is uncertain whether they stay together for the whole journey, let alone learn the route.

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Young individuals of some other species are clearly influenced in migratory behaviour by the example of other unrelated individuals. This is especially evident in soaring birds which typically migrate along narrow routes centred on short sea crossings or narrow land bridges (Chapter 7). For instance, 754 young White Storks were transported from the Baltic region (where storks normally migrate southeast) and released at migration time in western Germany (from where storks normally migrate southwest) (Schu¨z, 1950). The resulting ring recoveries from the released birds showed a strong tendency towards the southwest, approximating the direction taken by the local storks, rather than the southeast direction prevalent in the homeland of the released birds. It was assumed that the released storks were influenced in their direction by the local ones migrating at the same time. In another experiment, radio-tagged juvenile White Storks were displaced far to the east outside the breeding range of the species and released within their normal migration season (Chernetsov et al., 2004). In the absence of any local storks, these released birds showed a wide spread of directions (SW-WSW), rather than the expected narrow SSE heading normally shown by their population. The authors suggested that naive juvenile White Storks (and maybe other soaring migrants) rely on social interactions when selecting their autumn migratory route to a much greater extent than previously supposed and to a greater extent than passerine long-distance migrants tested in orientation cages. In other words, in addition to inherent directional preferences, specific migration routes are partly learned from more experienced birds, an opportunity denied to these experimental birds. Evidence of juveniles learning narrower and safer migration routes from experienced adults has also emerged from studies of soaring raptors, such as Egyptian Vulture (Neophron percnopterus) and Lesser Spotted Eagle (Clanga pomarina) (Oppel et al., 2015; Meyburg et al., 2017a,b). In the latter, over a 12-year period, 85 juveniles were reared in captivity for release into the declining German population, including 50 birds that were translocated from Latvia 940 km to the east (Meyburg et al., 2017a,b). In 2009, 12 translocated juveniles, as well as 8 native juveniles and 9 native adults, were satellite-tracked on route to Africa. Native juveniles departed around the same time as the local adults, and most of these juveniles and all the adults used the eastern flyway around the Mediterranean. In contrast, translocated juveniles departed on average 6 days before local eagles so had no local guidance. Five travelled directly southward and died in the central Mediterranean region. Consequently, fewer translocated juveniles (4/12) than native juveniles (7/8) reached Africa. The conclusion was that juvenile eagles had a much better chance of learning the all-important southeastern flyway if they left at an appropriate date to connect with experienced elders on migration. It was not clear why translocated juveniles departed so early. In all soaring birds, migrating by day, individuals may also learn from other soaring species not only their own. On migration days, mixed species form long streams of migrants readily visible along traditional routes. For individuals within these streams, the locations of the all-important thermals and other updrafts are shown by the birds ahead. As another example of social influence on migration routes, some Black-tailed Godwits (Limosa limosa) from the Dutch breeding population were released 1000 km to the east in Poland, where they migrated along with Polish birds, using the same routes and stopover sites (Loonstra et al., 2019). Their siblings, back in the Netherlands, used instead the routes and stopovers traditional to the Dutch population. It seemed that birds from each area learned their routes by travelling with the local birds, although in this species birds from both populations headed broadly southwest. Migration has even been induced in non-migratory stock by the example of other migratory individuals of the same species. Eggs obtained from English non-migratory Mallards (Anas platyrhynchos) were hatched in Finland and the Baltic region (Valikangas, 1933; Pu¨tzig, 1938). The resulting 116 young were allowed freedom with the local migratory Mallard. They gave 19 recoveries up to 2300 km away, all within the normal winter range of the host population. In contrast, other translocated English young released in autumn, after departure of the local ducks, remained near the release points during winter. Once again, innate behaviour was apparently over-ridden by social influence. Related species use the same staging areas as one another, and occasionally individuals get caught up in flocks of other species and end up in wintering areas other than their own. This phenomenon has long been known in geese, in which occasional species are seen as rare vagrants among flocks of regular species (eg Snow Geese (Anser caerulescens) in Western Europe among Pink-footed Geese (Anser brachyrhynchus), or Red-breasted Geese (Branta ruficollis) in Western Europe among Greater White-fronted Geese, or Barnacle Geese (Branta leucopsis) in North America among Canada Geese). But one of the most striking examples is the appearance of Hudsonian Godwits (Limosa haemastica) among Bar-tailed Godwits (Limosa lapponica) in New Zealand. This case is the more remarkable because this migration involves the longest known sea-crossings performed by any landbirds, originating in Alaska. All these examples indicate the influence of social behaviour on migration timing and routes. Self-learning also seems important, at least in some long-lived species which refine their migration routes and timing as they gain experience (Chapter 18). The biggest changes occur between the first and second year of life, but in some species improvements have been noted up to the 7th year (Sergio et al., 2014). Some of the recorded changes

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differ from those seen in most other species, and at first seem counter-intuitive. For example in several species, from Common Cuckoos to Honey Buzzards (Pernis apivorus) and Streaked Shearwaters (Calonectris leucomelas), the juveniles took straighter more direct routes than adults to their wintering areas (Vega et al., 2016; Ha˚ke et al., 2003; Yoda et al., 2017). This was consistent with the juveniles on their first journey, travelling without adult guidance, following a clock-and-compass system. In contrast, adults from the same breeding area took longer and more circuitous but safer routes, which could be interpreted as modifications resulting from learning, either from personal experience or from other individuals. Modification of migration routes through exploration and refinement could be especially important in long-lived species which can undertake similar journeys many times during their lives (Guilford et al., 2011; see also Chapter 18).

Re-establishment of migration routes The knowledge that young geese, swans and cranes appear to find their specific wintering localities by accompanying their parents has been used to re-establish populations and migration routes in regions from which former populations had been eliminated (Ellis et al., 2003). Captive-bred young were taught to follow ultralight or microlight aircraft (in the same way that they would naturally follow their parents), and then at the appropriate date, they were led on a long ‘migration’ to an appropriate wintering area. For example, young Whooping Cranes (Grus americana) released on former breeding areas in central Wisconsin were taught to fly behind an ultralight plane. The plane was then used to guide these young from their release area 1800 km south to former wintering grounds in Florida that had not been used for many years. The cranes were over-wintered successfully there. In spring, they returned unaided to their surrogate natal area, and in autumn, they migrated again to their new wintering site. Apparently, one journey was enough to fix a migration route for these young birds. Further releases were made subsequently, and by 2018 the new Wisconsin population contained 102 individuals, including many nesting pairs. Eight years of data from cranes migrating individually or in groups without ultralight escort yielded evidence of long-term social learning from older individuals (Mueller et al., 2013). This learning gradually reduced deviations from a straight-line path, yielding over 7 years a 38% shortening in the flight path, changing a sinuous to more direct but still safe route. In another experiment, Sandhill Cranes (Grus canadensis) did not necessarily fly the exact route in spring that they had used on their first autumn training flight. In general, the birds used the most direct route in spring rather than repeat the circuitous autumn path necessitated by motorised craft needing to refuel and avoid obstacles (Ellis et al., 2003). This implied that particular landscape details were not of primary importance in the directed migration of these birds. It also implied that the birds knew the direction of home from their present position. From 15 similar experiments conducted during 1990 2001, which also included Canada Geese and Trumpeter Swans (Cygnus buccinator), most of the birds reached a new wintering area chosen for them and returned on their own to their starting area next spring (Sladen et al., 2002; Ellis et al., 2003). Once again, these birds probably had an innate migratory direction, like other birds that have been studied, but social factors influenced the actual route and stopover sites used on migration, and in some species, even whether migration occurred (for social influences on other aspects of migration behaviour see Chapter 3).

SUMMARY Birds have the same senses as we do, but their vision is generally more acute than ours and extends into the ultraviolet range, their hearing extends to infrasound, and they also have a magnetic sense that we lack. The prevailing idea is that magnetite-based receptors near the beak detect the intensity and possibly other aspects of the magnetic field which help in navigation, while a radical pair mechanism based in the eyes could detect the alignment of the force lines, which helps in compass orientation. The navigational abilities of birds have often been studied by displacement experiments through which birds are caught from the wild and transported far from their current location and then followed to assess their ability to return to a familiar area. Such experiments have been done with birds caught at their nests, on their migration routes or in their wintering areas. Migratory birds are far better at returning to familiar areas than are resident species, as judged by the distances from which they can return, the proportions of displaced individuals that return and their speed of return. Some pelagic birds displaced from their nests soon returned to those nests from distances of thousands of kilometres. Inexperienced juvenile birds apparently have an innate ability to fly on a pre-determined compass course for an appropriate time to reach wintering areas appropriate to their population; they may change direction at different stages of their migration and can reverse directions for their return in spring. They apparently have an inherent seasonal directional preference and an internal calendar clock to switch migratory behaviour on and off at appropriate seasons. Experienced birds also know the positions of areas previously visited, and can return to them in successive years. In addition to a simple ‘clock-and-compass’

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system, therefore, experienced birds must also have a ‘map sense’ which enables them to find familiar places again, often by direct flight. Adult birds, and the juveniles of at least some species, can also correct for displacements off the migration route (as by wind or experiment) and can get back on course if motivated to do so. True navigation, involving a positioning (map) sense, is assumed to require sensitivity to at least two gradients of environmental features running in different directions to create a bi-coordinate (or multi-coordinate) grid-based map, from which birds could determine their geographical position and homeward direction, even from places new to them. Bi-coordinate navigation could provide continual positional feedback, enabling birds to correct for drift or directional mistakes. Increasing evidence implies that both juvenile and adult birds have some kind of innate positioning system that guides them to specific target areas (signposts) which lie on migration routes or in wintering areas. In some bird species, young migrate singly and later in the year than adults so could not readily learn specific migration routes from more experienced individuals. However, in species that migrate in flocks, social interactions with experienced conspecifics seem to play an important role in establishing the route of migration. This is most evident in swans, geese and cranes which travel as families, with the young able to learn from their parents. In some flocking species, experiments have shown that social influences can sometimes over-ride inherent migratory and directional tendencies.

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Creutz, G. (1949). Untersuchungen zur Brutbiologie des Feldsperlings (Passer m. montanus L.). Zool. Jahrb. 78: 133 72. Drost, R. (1955). Wo verbleiben im Binnenland frei aufgezogne Nordsee-Silbermo¨wen. Vogelwarte 18: 85 93. Ellis, D. H., Sladen, W. J. L., Lishman, W. A., Clegg, K. R. Duff, J. W. et al. (2003). Motorised migrations: The future or mere fantasy? Bioscience 53: 260 4. Evans, P. R. (1968). Reorientation of passerine night migrants after displacement by the wind. Br. Birds 61: 281 303. Falkenberg, G., Fleissner, G. Schuchardt, K. et al. (2010). Avian magnetoreception: elaborate iron mineral containing dendrites in the upper beak seem to be a common feature of birds. PLOS ONE 5: e9231. Fransson, T., Jakobsson, S. & Kullberg, C. (2005). Non-random distribution of ring recoveries from trans-Saharan migrants indicates species-specific stopover areas. J. Avian Biol. 36: 6 11. Gill, B. J. & Hauber, M. E. (2012). Piecing together the epic transoceanic migration of the Long-tailed Cuckoo (Eudynamys taitensis): an analysis of museum and sighting records. Emu 112: 326 32. Gschweng, M., Kalko, E. K. V., Querner, U., Fiedler, W. & Berthold, P. (2008). All across Africa: highly individual migration routes of Eleonora’s Falcon. Proc. R. Soc. B 275: 2887 96. Guilford, T., Freeman, R., Boyle, D., Dean, B., Kirk, H. Phillips, R. et al. (2011). A dispersive migration in the Atlantic Puffin and its implications for migratory navigation. PLOS ONE 6: e21336. Hagstrum, J. T. (2001). Infrasound and the avian navigational map. J. Exp. Biol. 203: 1103 11. Ha˚ke, M., Kjelle´n, N. & Alerstam, T. (2003). Age-dependent migration strategy in Honey Buzzards Pernis apivorus tracked by satellite. Oikos 103: 385 96. Hamilton, W. J. (1962). Bobolink migratory pathways and their experimental analysis under night skies. Auk 79: 208 33. Hein, C. M., Zapka, M. & Mouritsen, H. (2011). Weather significantly influences the migratory behaviour of night-migratory songbirds tested indoors in orientation cages. J. Ornithol. 152: 27 35. Horton, T. W., Bierregaard, R. O., Zawar-Reza, P., Holdaway, R. N. & Sagar, P. (2014). Juvenile Osprey navigation during trans-oceanic migration. PLOS ONE 9: e114457.

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Myers, J. P., Schick, C. T. & Castro, G. (1988). Structure in Sanderling (Calidris alba) populations: the magnitude of intra- and inter-year dispersal during the nonbreeding season. Proc. Int. Ornithol. Congr. 19: 604 15. Newton, I. (1972). Finches. London, Collins. Newton, I. (2008). The Migration Ecology of Birds (1st ed.). London, Academic Press. Oppel, S., Dobrev, V., Arkumarev, V., Saravia, V. Bounas, A. et al. (2015). High juvenile mortality during migration in a declining population of a long-distance migratory raptor. Ibis 157: 545 57. Perdeck, A. C. (1958). Two types of orientation in migrating Starlings, Sturnus vulgaris L., and Chaffinches, Fringilla coelebs L., as revealed by displacement experiments. Ardea 46: 1 37. Perdeck, A. C. (1967). Orientation of Starlings after displacement to Spain. Ardea 55: 93 104. Piersma, T., Loonstra, A. H. J., Verhoeven, M. A. & Oudman, T. (2020). Rethinking classic Starling displacement experiments: evidence for innate or for learned migratory directions? J. Avian Biol. 2020: e2337. ¨ ber das Zug verhalten umgesiedelter englischer Pu¨tzig, P. (1938). U Stockenten. Vogelzug 9: 139 45. Rabøl, J. (1992). Star-navigation in night-migrating passerines. Dansk Orn. Foren Tidskkr 86: 177 81. Rabøl, J. (1994). Compensatory orientation in Pied Flycatchers, Ficedula hypoleuca, following a geographical displacement. Dansk Orn. Foren Tidskkr. 88: 171 82. Rabøl, J. & Noer, H. (1973). Spring migration of the Skylark (Alauda arvensis) in Denmark. Vogelwarte 27: 50 65. Ralph, C. J. & Mewaldt, L. (1975). Timing of site fixation upon the wintering grounds in sparrows. Auk 92: 698 705. Ralph, C. J. & Mewaldt, L. R. (1976). Homing success in wintering sparrows. Auk 93: 1 14. Ritz, T., Adem, S. & Schulten, K. (2000). A model for photoreceptorbased magnetoreception in birds. Biophysical J. 78: 707 18. Ritz, T., Thalau, P., Philips, J. B., Wiltschko, R. & Wiltschko, W. (2004). Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429: 177 80. Schu¨z, E. (1938). Auflassung ostpreussischer Jungsto¨rche in England 1936. Vogelzug 9: 65 70. Schu¨z, E. (1949). Die Spat-Auflassung ostpreussischer Jungsto¨rche in WestDeutschland durch die Vogelwarte Rossitten 1933. Vogelwarte 15: 63 78. Schu¨z, E. (1950). Fru¨h-Auflassung ostpreussischer Jungstorche in WestDeutschland durch die Vogelwarte Rossitten 1933 36. Bonner Zool. Beitr. 1: 239 53. Sergio, F., Tanferna, A., De Stephanis, R., Jime´nez, L. L. Blas, J. et al. (2014). Individual improvements and selective mortality shape lifelong migratory performance. Nature 515: 410 13. Sladen, W. J. L., Lishman, W., Ellis, D. H., Shire, G. & Rininger, D. L. (2002). Teaching migration routes to Canada Geese and Trumpeter Swans using ultralight aircraft,1990 2001. Waterbirds 25 (Spec. Publ. 1): 132 7. Strandberg, R., Klaassen, R. H. G., Ha˚ke, M., Olofsson, P. & Alerstam, T. (2009). Converging migration routes of Eurasian Hobbies Falco subbuteo crossing the African equatorial rain forest. Proc. R. Soc. B 276: 727 33. Tamm, S. (1980). Bird orientation single Homing Pigeons compared with small flocks. Behav. Ecol. Sociobiol. 7: 319 22. Thorup, K. & Rabøl, J. (2001). The orientation system and migration pattern of long-distance migrants: conflict between model predictions and observed patterns. J. Avian Biol. 32: 111 19.

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Thorup, K. & Rabøl, J. (2007). Compensatory behaviour after displacement in migratory birds a meta-analysis of cage experiments. Behav. Ecol. Sociobiol. 65: 825 41. Thorup, K., Ortvad, T. E., Rabøl, J., Holland, R. A. Tøttrup, A. P. et al. (2011). Juvenile songbirds compensate for displacement to oceanic islands during autumn migration. PLOS ONE 6 (3): e17903. Thorup, K., Vega, M. L., Snell, K. R. S., Lubkovskaia, R. Willemoes, M. et al. (2020). Flying on their own wings: young and adult Cuckoos respond similarly to long-distance displacement during migration. Sci. Rep. 10: 7698. Valikangas, I. (1933). Finnische Zugvo¨gel aus englischer Vo¨geleiern. Vogelzug 4: 159 66. Vaught, R. W. (1964). Results of transplanting flightless young Bluewinged Teal. J. Wildl. Manage. 28: 208 12. Vega, M. L., Willemoes, M., Thomson, R. L., Tolvanen, J. Rutila, J. et al. (2016). First-time migration in juvenile Common Cuckoos documented by satellite tracking. PLOS ONE 11: e0168940. Wallraff, H. G. (2003). Zur olfakorischen Navigation der Vo¨gel. J. Ornithol. 144: 1 31. Wenzel, B. M. (1991). Olfactory abilities of birds. Proc. Int. Orn. Congr. 20: 1820 9.

Wernham, C. V., Toms, M. P., Marchant, J. H., Clark, J. A., Siriwardena, G. M. & Baillie, S. R. (2002). The migration atlas: movements of the birds of Britain and Ireland. London, T. & A. D. Poyser. Willemoes, M., Blas, J., Wikelski, M. & Thorup, K. (2015). Flexible navigation response in Common Cuckoos Cuculus canorus displaced experimentally during migration. Sci. Rep. 5: 16402. Willemoes, M., Strandberg, R., Klaassen, R. H. G., Tøttrup, A. P. Vardanis, Y. et al. (2014). Narrow-front loop migration in a population of the Common Cuckoo Cuculus canorus, as revealed by satellite telemetry. PLOS ONE 9 (1): e83515. Wiltschko, R. (1992). Das Verhalten verfrachteter Vo¨gel. Vogelwarte 36: 249 310. Wiltschko, R. & Wiltschko, W. (2003). Mechanisms of orientation and navigation in migratory birds. Pp. 433 56 in Avian migration (eds P. Berthold, E. Gwinner, & E. Sonnenschein). Berlin, Springer-Verlag. Wiltschko, R. & Wiltschko, W. (2007). Magnetoreception in birds: two receptors for two different tasks. J. Ornithol. 148: S61 76. Wiltschko, R. & Wiltschko, W. (2019). Magnetoreception in birds. J. R. Soc. Interface 16, 20190295. Yoda, K., Yamamoto, T., Suzuki, H., Matsumoto, S., Mu¨ller, M. & Yamamoto, M. (2017). Compass orientation drives naı¨ve pelagic birds to cross mountain ranges. Curr. Biol. 27: R1152 3.

Chapter 11

Finding the way: orientation and navigation

Common Starlings (Sturnus vulgaris) migrating at night ‘Nature does not accommodate itself to the comprehensions of man’. Galileo.

When considering bird movements, as stressed in the previous chapter, it helps to separate ‘orientation’ from ‘navigation’. Orientation is concerned with establishing from the current location the direction for migration, whereas navigation is concerned with finding and maintaining an appropriate course between fixed localities. True navigators can find any places they have previously visited; they can correct for displacements occurring at any point in a journey, and they can find their way home (to breeding or wintering areas) from previously unknown places to which they have been experimentally displaced (Chapter 10). They act as though they know their position at any time and possess a map to get anywhere they need to go. Mental maps indicating position could most readily be based on two or more environmental gradients varying in different directions over the earth’s surface, forming a virtual grid analogous to latitude and longitude (a ‘bi-coordinate’ map). By learning the gradients within a familiar area, the argument goes, the bird could extrapolate those gradients well beyond its familiar area and thus take an appropriate direction to a target area, whether known or not. For orientation or navigation, birds are now known to use several types of environmental cues, some of which function locally and others over wider areas. Birds clearly respond to landmarks with which they are familiar, especially in their home areas, and on a wider scale they can gain information from the sun, skylight polarization and the stars, and ˚ kesson, 2003; Wiltschko & Wiltschko, 2003, 2009, 2015, magnetic field lines and odour gradients (for reviews see A 2019). The use of these various cues has been studied in detail, but a prior requirement for migration is that the bird should ‘know’ beforehand either by experience or inheritance what direction it should take on migration. An experienced bird is normally homing to a known goal, but a naive juvenile on its first migration does not have a specific known goal, only an inherent directional preference and time programme, and perhaps also an indication of an appropriate target area (Chapter 10). Effective use of any of these environmental cues, over short or long distances, requires a period of learning, and often frequent revision as the bird proceeds on its journeys. In other words, the use of all these environmental cues is based on a combination of innate and learned components. These various migration cues are discussed in the sections below, but it is evident that birds do not rely on any one of these aids alone but can transfer from one type to another, as appropriate at the time. They can also calibrate different cues against one another to ensure accuracy and consistency in directional information. The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00017-8 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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VISUAL LANDMARKS Visual landmarks clearly play a crucial role in the movements of a bird around its home area, and presumably also as it approaches another suitable habitat after a migratory flight. During its journey, a bird may also react to bigger landscape features, such as coastlines or mountain ranges. Depending on learning and memory, response to local landmarks probably also explains how some migratory birds, once they reach their general target area, find the same breeding or winter territories from year to year. Modern tracking devices have made it possible to follow the precise routes that birds follow and examine the use they make of various landmarks. For example different homing pigeons released repeatedly from the same locality near Oxford developed personal routes to the home loft. These routes were by no means the straightest possible but appeared to connect a series of landmarks or landscape features, such as main roads, leading roughly in the right direction (Biro et al., 2004). Although a big step from local movements, some birds may in theory memorize landscape features along their migration routes and, after their first journey, use them to navigate on subsequent journeys. This would seem most possible in species that migrate short distances or travel along linear landscape features such as mountain ranges, coastlines or river systems. Species such as geese and cranes could fit this category, and they have the additional advantage that their aquatic habitats are visible from aloft day and night. They also travel in flocks, so individuals could benefit from collective memory. Many other birds tracked on migration in successive years clearly do not migrate by use of familiar landmarks because over much of their journeys they follow somewhat different routes each year (eg Vardanis et al., 2016), or fly at high altitude at night, so could not distinguish the detail below. Another way in which birds including juveniles with no previous experience of a route could make use of landscape features is in maintaining a constant direction, lining up a number of landscape features, one after another in the same direction, and flying directly from one to another, adding further features as they move along the route (a form of piloting). Such a system could also help to prevent birds from being blown off route by crosswinds, at least over land where suitable features are obvious, and could provide continuity between night and day. But in whatever way landmarks may be used, they do not define the position of the bird in space relative to the goal on a map, but rather provide a route to the goal. It would be hard to know whether any birds make their entire overland migrations on the strength of landscape features alone, either memorized or chosen from a constant directional course. But they clearly have other options.

THE SUN AND POLARIZED LIGHT From its position in the sky, the sun can provide information on season, latitude and direction, but only if account is taken of seasonal and diurnal changes in its position. During the course of each day, as is obvious, the sun follows an arc in the sky, travelling clockwise from east to west, and reaching its highest point at noon, indicating due south in the northern hemisphere and due north in the southern hemisphere. In addition, the noon height of the sun varies with season (in any one place, by definition highest in mid-summer and lowest in mid-winter) and with latitude (directly overhead at noon on the equator at the two equinoxes, lower at noon with increasing latitude). Unlike ourselves, birds can also distinguish polarized light. This is light consisting of waves of electric field vectors vibrating only in a single plane, as opposed to unpolarized light whose waves vibrate in more than one plane. Unpolarized light can be transformed into polarized light either artificially by passing light through particular materials that let through only single-plane light waves or naturally when light strikes a surface from a low angle. The most intense polarized light from the sun is produced near dawn and dusk when the sun is low with respect to the horizon, and it is at these times when birds seem to use polarized light as a compass system (Muheim et al., 2006b).

Evidence that birds use the sun as a compass This story begins with some ground-breaking experiments by Kramer (1951, 1952, 1957). Under a sunny sky, Common Starlings (Sturnus vulgaris) were kept in circular wire cages during the migration period oriented in the same direction as free-living Starlings. They varied the angle they took to the sun according to the time of day. If the sky became overcast, obscuring the sun, their directional preference disappeared. When their view of the sun’s direction was changed using mirrors, the birds oriented at the same angle to the apparent sun as they would to the real sun at that time of day (Kramer, 1951; Figure 11.1). These experiments confirmed that Starlings could use the sun as a compass, but only with the aid of a time-keeping mechanism, allowing for time of day and adjusting their directional preference accordingly.

Finding the way: orientation and navigation Chapter | 11

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FIGURE 11.1 Orientation of spontaneous diurnal migratory activity in a caged Common Starling (Sturnus vulgaris) under various conditions of sun exposure. The bird was tested in a pavilion with six windows during the spring migration season. (a) Behaviour under clear skies. (b) Behaviour under total overcast, when the sun was not visible. (c) Behaviour when the image of the sun was deflected 90 counter-clockwise by means of mirrors. (d) Behaviour when the sun was deflected 90 clockwise by means of mirrors. Each dot represents 10 s of fluttering activity. Dotted lines show incidence of light from the sky, Arrows denote mean direction of activity. Redrawn from Kramer (1951).

By this procedure, birds were able gradually to correct for the daily movement of the sun across the sky. Given a simulated stationary sun, a caged migrant orientated at different angles according to time of day, also confirming the effect of an internal clock. This double system became known as the time-compensated sun compass. The use of a sun compass has now been confirmed experimentally in more than 10 wild bird species, including penguins walking over ice fields (Emlen & Penney, 1964). It may be commonly used by diurnal migrants (Schmidt-Koenig et al., 1991). At least one typical night migrant, the European Robin (Erythacus rubecula), could also use the sun compass when tested in the daytime (Helbig, 1991). However, simply seeing the sun provides a naive bird with little useful information. The bird must live at a site for some time and learn the way in which the sun moves across the sky to use it as an effective directional aid. If birds from the northern hemisphere are transported to the southern hemisphere, they initially orientate themselves incorrectly, interpreting the sun as if they were in the northern hemisphere (indicating south rather than north) (Schmidt-Koenig et al., 1991). However, they quickly make the necessary change. Presumably, regular trans-equatorial migrants must also be able to make this adjustment twice each year when they cross the equator, and one possible mechanism is explained below. Common Starlings and homing pigeons are able to use the sun compass anywhere on the globe: both under polar conditions when the sun does not set, and under equatorial conditions when it reaches its zenith. Because the arc traced by the sun in the sky varies with season and geographical position, birds need to read the sun separately in each area they visit. If they can adjust for time of day on the basis of their experience in the previous few days, their response should be appropriate for the latitude and time of year. Birds could use the sun compass not only to set their direction but also to detect changes in their heading during flight (Guilford & Taylor, 2014). Little is known about the use of the sun and other celestial cues by seabirds. However, in one experiment, use was made of the burrow-nesting habit of the Manx Shearwater (Puffinus puffinus) which stays underground for many days

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at a time, with the only source of external light coming from the burrow entrance. In the experiment, rubber mats were placed over shearwater nest entrances, imbedded with an array of LEDs controlled by timers. The internal clocks of the incubating adults could thus be shifted by several hours before the birds were taken far out to sea and their homeward journeys tracked using GPS trackers (Padget et al., 2018). The birds’ trajectories back towards the colony were significantly twisted in the predicted directions (anti-clockwise for slow-shifted birds and clockwise for fast-shifted birds). Although the effect was small, it implied that these shearwaters were using a time-compensated sun compass to judge direction, like the captive Starlings studied by Kramer (1951). As with any natural compass system, the sun compass has its limitations. One is that it is only available for part of each 24-hour period, as it cannot be used at night or under dense cloud. In addition, when heading south in autumn or north in spring, birds would have to constantly adjust their compensation mechanisms to the changes in latitude, and when heading east or west they would need continual readjustment of their internal clocks to the changes in longitude (time-shifts). Birds may well use the sun compass in areas where they are resident for a time, re-establishing it afresh after each journey, but whether it is of major importance during migration remains an open question.

The sun and navigation For a bird to use the sun for navigation, and not just for compass orientation, it must be able to determine its position on earth from the sun at any time that the sun is visible. This would in turn involve the bird measuring some equivalent of latitude and longitude. The sun could be used for this purpose if the bird could measure the arc of the sun that is the angle made by the path through which the sun is moving in relation to the horizon (Matthews, 1968). Each day in the Northern Hemisphere, the highest point reached by the sun lies due south, thus indicating direction, and occurs at noon, thus indicating time. In its home area, a bird is familiar with the sun’s pattern of movement. Placed in different surroundings, the bird could theoretically project the curve of the sun’s movement after watching only a small segment of its course. By judging the height of the sun’s arc at noon and comparing it with the comparable measure from its home area, the bird could in theory obtain a measure of its latitudinal shift. However, we have no inkling that a bird does this. Longitude cannot be measured independently of time, because changes in both result from the regular rotation of the earth. But longitude can be ascertained, for example from the time when the sun reaches its highest position in the sky (local noon) in relation to time in the starting area, as revealed by an internal clock. To detect change in their longitudinal position, the birds would therefore in effect need two internal clocks: one accurately fixed on home-time and another that quickly adapts to local time, the difference between the two giving the ‘time-shift’. This indicates how the sun might be used for navigation, but the only relevant experiment known to me revealed no evidence for a doubleclock mechanism in birds that could detect east west displacements (Kishkinev et al., 2010). As yet, then, despite its use as a compass, we have no good evidence that the sun is used for navigation. Other cue systems are more likely to be used for this purpose.

Evidence that birds use polarized light as a compass The ability of birds to detect polarization patterns has been shown in many experiments, and various species of normally nocturnal migrants responded to manipulations of polarized skylight, as seen at sunset (Able, 1993). Usually, the birds were tested individually outdoors in otherwise normal conditions in cages covered by sheet polarizing material (Able, 1989; Moore, 1982; Moore & Phillips, 1988; Phillips & Moore, 1992; Helbig & Wiltschko, 1989; Munro & Wiltschko, 1993). In each case, the birds changed orientation as predicted by alterations in the alignment of the polarizing sheets. However, the visual stimulus created by this procedure is quite unnatural, and birds sometimes oriented differently under artificial polarized light from the way they did under naturally polarized skylight (Helbig & Wiltschko, 1989). Nevertheless, the experimental birds were responding to polarized light as an orientation cue, rather than to other sunset features. Moreover, when the natural polarization pattern was eliminated by depolarizers placed on top of orien˚ kesson & tation cages, songbirds became disoriented in some (Helbig, 1990, 1991), but not all experiments (A Ba¨ckman, 1999). The main benefit of polarized light at dawn or dusk is that it can give a clear meridian for use as a directional cue and can thus be used to calibrate other types of compass cues. The skylight polarization pattern is also apparent when the sun is not visible, providing that part of the sky remains clear of cloud. Under totally overcast skies, birds in orientation cages showed scattered orientation, suggesting they could not orientate under these conditions (Moore, 1987; ˚ kesson et al., 2001). It is probably mainly its use in calibrating other compass systems that polarized light is important A to migrating birds (see below), although it is still not understood exactly how birds make use of this cue in direction

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setting (for discussion, see Sjo¨berg & Muheim, 2016). A potentially significant discovery was that the magnetic compass in captive Zebra Finches (Taeniopygia guttata) was operational only when overhead polarized light was aligned parallel but not perpendicular to the magnetic field. This finding implied a direct interaction between polarized light and the light-dependent magnetic compass (discussed below), but again further work is needed to interpret this finding (Muheim et al., 2016).

THE STARS In both hemispheres, the stars rise in the east and set in the west but in the northern hemisphere they revolve anticlockwise around the north celestial pole (the polar star), while in the southern hemisphere they revolve anti-clockwise around the south celestial pole (which has no specific star). Based on experiments in the northern hemisphere, providing enough of the night sky is visible, nocturnal migrants can use the stars as a compass. When tested in orientation cages, migrants oriented correctly on clear starry nights but often became inactive or disoriented under overcast skies (Thorup & Rabøl, 2007). Birds also became confused if star patterns were varied experimentally in a planetarium (Sauer & Sauer, 1955, 1960; Wagner & Sauer, 1957; Hamilton, 1962; Emlen, 1967a,b). Since the outdoor experiments were performed on moonless nights, and all planetarium tests were conducted without showing the planets, the stars themselves were implicated as the crucial cues. When Indigo Buntings (Passerina cyanea) were tested under a natural starry sky during autumn migration, they preferred southerly directions. They maintained this southerly preference under an artificial star pattern imitating the natural sky in a planetarium. But when the artificial star pattern was changed by 180 degrees, the birds changed their directional preference to the north. Under a static night sky, they showed no obvious migratory restlessness. In young birds, effective use of a star compass involved learning during a short sensitive period before the onset of the first migratory journey. In the northern hemisphere, the stars rotate around the Pole Star during the course of each night, and birds evidently learned the centre of rotation of the night sky and used this as the cue to north. Captive Indigo Buntings lacking early experience of the night sky failed to orientate correctly in a planetarium (Emlen, 1967b, 1970, 1975). As with the sun compass, the ability and tendency to acquire this knowledge appeared to be innate, and recent experiments suggest that hand-reared Pied Flycatchers (Ficedula hypoleuca) denied the opportunity to see the stars in autumn might nevertheless learn to use the stars as a compass in spring (Zolotareva et al., 2021). Some birds can develop this ability under unnatural star patterns, as shown for example by the selective blocking out of constellations in the artificial sky. The key factor was the rotation of the night sky about the Pole Star, and even an extremely simplified and reduced star pattern would suffice for orientation, so long as it rotated about a single conspicuous star. Thus nestling Indigo Buntings raised under an artificial sky with the star Betelgeuse (in the constellation Orion) as the point of rotation treated Betelgeuse in the same way as the Pole Star when subsequently tested. For captive birds, any pattern of small light dots can successfully substitute for the natural stars so long as the birds can observe the pattern rotating with one revolution per day. A simple artificial ‘sky’ with just 16 light dots was enough to show that, for European Robins and Garden Warblers (Sylvia borin), rotation alone was the crucial factor (Wiltschko & Wiltschko, 1976; Wiltschko et al., 1975a, 1987). Birds apparently do not inherit detailed knowledge about the star pattern but are equipped with an inherent tendency to look for the centre of rotation and interpret this as ‘polewards’. Whatever the compass system, migratory birds need to change direction between spring and autumn. When captive Indigo Buntings were kept on different photoperiod regimes so that some were in spring condition and others in autumn condition, both groups could then be tested together under the same planetarium sky. The birds in spring migration condition headed northward, while those in autumn condition headed southward (Emlen, 1969). The direction of headings was apparently not dictated by the stellar sky, but the stars did represent a reliable compass for birds whose internal state told them to migrate north or south. The use of a star compass has now been demonstrated experimentally in at least six different bird species, all of which seemed to use the centre of celestial rotation as their reference. More than seven clear nights seemed to be needed for birds to work out the star compass (Emlen, 1975; Wiltschko et al., 1987; Michalik et al., 2014). They then learned the geometrical star patterns and thereafter no longer needed to observe celestial rotation (Emlen, 1975; Wiltschko et al., 1987; Mouritsen & Larsen, 2001). The use of a stellar compass was further supported by outdoor experiments in which birds at night that were denied access to other meaningful (magnetic) information nevertheless headed in their migratory direction using the stars alone (eg Bingman, 1984; Mouritsen, 1998). Moreover, in most studies orientation deteriorated or disappeared entirely under heavily overcast skies, further suggesting a reliance upon celestial information (Thorup & Rabøl, 2007). However, some birds continued to orient under overcast and could be assumed to be using other (probably magnetic) cues (see below).

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The stars and navigation If the birds use the rotating star pattern only to define the position of the poles, and hence as a compass, then no correction for time of day is necessary. They may, however, gain further information from star patterns. As birds proceed on their journeys lasting up to several weeks, star patterns that were once visible disappear below the horizon behind them, while others appear above the horizon in front, another indication that birds are unlikely to rely throughout on particular star patterns. However, for purposes of navigation, the centre of rotation above the horizon gets gradually lower with decreasing latitude, and could thus provide a bird with a measure of changing latitude. The measurement of longitude from star patterns could again be done only by measurement of the degree of time shift (Foster et al., 2018). But as mentioned above, this would require the use of two internal clocks, for which experiments have provided no support (Kishkinev et al., 2010). As yet, it seems that, although the stars are used as a compass, they are not used by birds for establishing their global position or any more complicated navigation. Alternative cues must be used instead.

Integrated use of celestial cues Nocturnal migrants often set off around dusk, when celestial cues related to the sun (eg sunset position, horizon glow, and skylight polarization pattern) are clearly visible, and when at the same time the star pattern is gradually emerging. Birds could therefore make use of all these celestial cues within a relatively short period. Radar observations reveal that migratory birds keep flying in the same direction through the transition from day to night or night to day (eg Myres, 1964). This implies that birds can switch from the sun to stars for navigation or use some totally different system, such as the magnetic compass, as discussed below. In addition, some arctic species which migrate by night at lower latitudes necessarily migrate in daylight at high latitudes in summer when the sun never sets. Bright moonlight can make ground-based features more visible but can apparently hinder the use of star patterns and produce the same disturbing effects as cloud (Wagner & Sauer, 1957). The moon itself is not known to play any obvious role in bird orientation, other than by affecting light values.

THE MAGNETIC FIELD ˚ kesson et al., 2014; Wiltschko & Another major system of bird orientation makes use of the earth’s magnetic field (A Wiltschko, 2019; Muheim et al., 2014). To understand how this field might be used, imagine the globe as a hugely powerful magnet, whose north magnetic pole is situated fairly close to the geographic North Pole, and whose south magnetic pole is similarly close to the geographic South Pole. Running through the atmosphere between the two magnetic poles are invisible (to us) longitudinal lines of magnetic force, which circle the globe rather like the segments of an orange (Figure 11.2). The field lines leave the earth vertically at the southern pole, then curve round the earth and re-enter its surface vertically at the northern pole. The magnetic vectors thus point upwards in the southern and downwards in the northern hemisphere but lie parallel to the earth’s surface at the magnetic equator. Their inclination (dip angle from the horizontal) thus varies from 90 degrees at the poles to 0 degrees at the equator. Hence, for any creature that can measure the inclination of the force lines, the earth’s magnetic field can indicate latitude and direction (toward the equator or pole) within each hemisphere. The strength (intensity) of the magnetic field also varies predictably over the earth’s surface, being generally strongest near the poles and weakest near the equator. Both inclination and intensity could therefore give measures of latitude to any animal with an appropriate magnetic sense, but in most regions on earth these parameters vary in sufficiently different directions that they could also help with bi-coordinate navigation (Figure 11.3; Bostro¨m et al., 2012a). However, a better measure of longitude could be given by magnetic declination, the angle between geographic and magnetic poles, which varies mainly along an east west axis. The magnetic North Pole is currently situated at about 78 N, 103 W in northernmost Canada (Queen Elizabeth Islands), and the magnetic South Pole is at 64 S, 138 E (just off Antarctica between Ade´lie Land and Wilkes Land). So not only do the magnetic poles not coincide with the geographic poles, the magnetic equator does not precisely overlie the geographic equator. From measures of intensity, inclination and declination most locations on earth have their own unique combination of parameter values and could provide site-specific knowledge to any animal able to read them. Experiments have now shown that many birds can read magnetic inclination and intensity, and at least one species behaved in an experiment as though it could also read magnetic declination (Kishkinev et al., 2015). So two or three of these magnetic parameters together could provide a map system for use in navigation as well as orientation. Unlike celestial cues, the magnetic field can give consistent information both day and night in all weathers, and unlike the sun compass, it needs no correction for time of day. No wonder, then, that various kinds of migratory animals appear to make use of it, including not only birds but also reptiles and amphibians, butterflies and other insects (Mouritsen, 2018).

FIGURE 11.2 Diagram depicting force lines in the earth’s magnetic field.

Intensity

Inclination

Declination

FIGURE 11.3 The earth’s magnetic field. Upper left. Contours of magnetic intensity shown in steps of 5000 nT. Upper right. Contours of magnetic inclination shown in steps of 20 degrees. Light grey lines positive (down) values, blue lines negative (upward) values. Thick line 0 degrees, horizontal force line. Lower left. Contours of magnetic declination shown in steps of 10 degrees. Grey lines positive values, blue lines negative values. Thick lines 0 degrees. Modified from World Magnetic Map developed by NOAA/NCEI and CIRES, December 2019.

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Despite its advantages, however, the magnetic field does not provide a perfect system of positioning everywhere. In areas with geomagnetic anomalies where magnetic parameters can be distorted, and in areas close to the geomagnetic poles where the field lines are vertical, a bi-coordinate map might be difficult or impossible to use. Also, at particular localities, geomagnetic parameters change through time, undergoing a diurnal cycle resulting from electromagnetic radiation from the sun, as well as other variations caused by occasional magnetic storms, also stemming from events on the sun. Moreover, the positions of the two magnetic poles change slightly over the centuries with respect to true geographical north and south. And over a much longer geological timescale, the polarity of the magnetic field has switched several times, with north and south reversing, so polarity has not formed a consistent source of reference. These features seem not to present major problems for birds, however, partly because birds have additional sources of positioning information, as described above, and partly because learning is involved in the use of any navigation system, enabling birds to adjust to changes in any system through time.

Evidence for use of the magnetic field So what is the evidence that birds do indeed make use of the earth’s magnetic field during migration? It had long been known that nocturnal migrants can at times orientate correctly even under completely overcast skies (as shown by radar), as can caged birds unable to see the sky. However, caged birds lost this ability when isolated from both the sky and the earth’s magnetic field behind metal-reinforced walls. Moreover, when the magnetic field experienced by caged European Robins was rotated using a powerful electromagnetic coil so that, for example, magnetic north was shifted to the east while the field’s total intensity and inclination, as well as other potential directional cues, were kept unchanged, the birds altered their orientation accordingly (Wiltschko & Merkel, 1966; Wiltschko, 1968). This crucial early experiment confirmed that birds could respond appropriately to the earth’s magnetic field, despite also using celestial cues for orientation. It was the first demonstration of the use of the magnetic field by any animal. It was later shown that the magnetic compass of birds involves the measurement of inclination (Wiltschko & Wiltschko, 1972), thus indicating to a bird the latitude and in a limited way direction (poleward or equatorward). Lacking an ability to distinguish one pole from another, when crossing the equator birds must switch their migratory programme from ‘fly equator-wards’ (towards decreasing angles of inclination) to ‘fly pole-wards’ (towards increasing angles of inclination) to be able to continue on their intended route. Experimental evidence from Garden Warblers implied that exposure to the horizontal magnetic field simulating the situation at the magnetic equator triggered the change in migratory programme (Wiltschko & Wiltschko, 1992). A similar mechanism was confirmed in the North American Bobolink (Dolichonyx oryzivorus) (Beason, 1992), which also responds to a horizontal magnetic field by shifting its orientation relative to the angle of inclination. The test birds also seemed to make use of celestial cues to help keep on course, with star patterns providing an independent guide to direction. All trans-equatorial migrants using a magnetic compass to orientate face this problem on both their outward and return journeys. The fact that birds rely largely on inclination, ignoring the polarity of the magnetic field, means that they would not have been affected by reversals of polarity occurring in the distant past. It also means that birds which colonised one hemisphere from another had a pre-existing navigation system (poleward or equatorward) that would work in either hemisphere (eg see Chapter 23). These various findings have been replicated in other bird species tested in similar ways (Wiltschko & Wiltschko, 1995, 1999; Gudmundsson & Sandberg, 2000; Schwarze et al., 2016). Some passerines were hand-raised without any view of the sky and, when tested during autumn migration, they headed in their population-specific migratory direction with the magnetic field as the most likely cue (Wiltschko & Wiltschko, 2003). These birds were tested in temperate latitudes, and other birds tested at higher latitudes, where the angle of magnetic inclination was steeper, needed to have observed celestial rotation (to fix north) in order subsequently to adopt the correct heading in relation to magnetic cues ˚ kesson et al., 2001). alone (Weindler et al., 1996; A Another interesting property of the magnetic compass in birds is that, at any one time, it operates only within a narrow functional range around the strength of the ambient magnetic field. Fields with markedly lower or higher intensity cause disorientation, at least for a time. European Robins accustomed to the normal magnetic field in Frankfurt (0.46 gauss) could spontaneously orient within the range 0.38 0.57 gauss, but initially gave random bearings in fields lower or higher than this. However, if the birds were kept in the altered field for a few days, they could then orient correctly in fields as low as 0.16 gauss or as high as 0.81 gauss (Wiltschko, 1978). They needed time to adjust to changed intensities. A similar sensitivity to altered field strengths was also found in Common Whitethroats (Curruca communis) and Garden Warblers (Wiltschko & Merkel, 1971; Wiltschko, 1974), and even in domestic chickens (Wiltschko et al., 2007). The birds’ ability to adapt to a range of field strengths would permit them to adjust to the range of magnetic intensities they would encounter at different latitudes during migration.

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Another significant feature of the avian magnetic compass is that it is light-dependent, which is consistent with the eyes being a major receptor (Chapter 10). In total darkness created in laboratory conditions, experimental birds can no longer orient in their migratory direction (Stapput et al., 2008). But this level of complete darkness can seldom occur in nature. For nocturnal migrants, even very low light levels seem sufficient for magnetic compass orientation. In laboratory tests, birds were well oriented in the light levels which occur more than 45 minutes after sunset. Clear nights provide sufficient light even without the moon, and migrants may avoid migrating in really dark conditions created by heavy overcast and rain. If they migrate at all on such nights, they may fly above the cloud layer, as shown by radar studies (Myres, 1964). A further finding is that birds require short-wavelength light, ultraviolet-blue-green, for good orientation, and under yellow and red light alone experimental birds become disoriented (Wiltschko & Wiltschko, 2007; Mouritsen et al., 2004). Further evidence that birds use the magnetic field stems from the fact that they respond to magnetic anomalies which upset their journeys. Experiments in an area of strong anomaly (R. Wiltschko et al., 2009; Schiffner et al., 2011) clearly showed that birds can sense magnetic intensity, but also confirmed that they can navigate without magnetic cues, having other means to find their way (as above). More information is needed on the extent to which birds can measure and use magnetic declination, which is the most obvious way (apart from time shifts) that they might assess longitude. In one key experiment, Eurasian Reed Warblers (Acrocephalus scirpaceus) responded appropriately to an alteration in declination alone (Chernetsov et al., 2017), but this result could not be replicated in Robins or Garden Warblers (Chernetsov et al., 2020). In a subsequent experiment, the orientation of Eurasian Reed Warblers was tested by exposing them in cages to geomagnetic cues of unfamiliar magnitude normally encountered only beyond their natural distribution (Kishkinev et al., 2021). These birds demonstrated re-orientation towards their migratory corridor as if they had been translocated to the corresponding location, but only when all naturally occurring magnetic cues (including declination) were presented, not when declination alone was changed. These birds apparently assessed declination along with inclination and intensity and also showed that they could navigate using geomagnetic cues extrapolated beyond their previous experience. Further research is required on the response of birds to magnetic declination, but similar responses have been reported in sea turtles (Putman et al., 2011). Overall, the use of a magnetic compass has now been demonstrated experimentally in at least 24 bird species from different continents, including diurnal and nocturnal migrants travelling over short or long distances, and also in resident species (Holland, 2014). The number of experiments and species is so high because for many years some scientists remained sceptical, finding it hard to believe that birds should possess such an impressive sensory quality that we lack, and use it in the way they apparently do. Given what we now know, the use of a magnetic compass may well be widespread (if not universal) among birds, even though it may be more commonly used by some species than by others. An interesting observation was that, when small songbirds were placed singly in orientation cages in which they could not see the sky, they showed repeated head-turning behaviour, first to one side then the other. This behaviour, recorded from above, was interpreted as an attempt by the bird to assess the direction of the magnetic force lines. Head turning began before each bout of migratory restlessness (Mouritsen et al., 2004).

Magnetic navigation So what is the evidence that birds can use magnetic information not only for orientation but also for navigation to a known goal or for correction following displacement? Magnetite particles around the beak region may provide one receptor system (Chapter 10). Caged passerine migrants treated with a magnetic pulse (0.5 T) strong enough to alter the magnetization of single-domain magnetite showed a marked deviation from their migratory direction (Wiltschko et al., 1994; Wiltschko et al., 1998a,b). Apparently, the pulse did not inactivate any potential receptor but caused it to provide the birds with false information. However, the response to the pulse was restricted to experienced migrants that navigate towards an already familiar goal, whereas young birds flying on innate compass courses on their first migration were not affected by this treatment (Munro et al., 1997). This suggested that the pulse affected a receptor that provides birds with a magnetic component of the ‘navigational map’. It changed the course to be pursued, while the magnetic inclination compass (based in the eyes) remained unaffected (Munro et al., 1997; Wiltschko et al., 2006). The effects of the pulse were short-lived, however, as the deflection lasted only 2 3 days after which the birds underwent a phase of disorientation. After 10 days they were again able to head in their migratory direction (Wiltschko et al., 1994). These observations on caged migrants were paralleled in free-living birds that were caught at a stopover site, treated with a pulse, released and radio-tracked to record their departure directions (Holland & Helm, 2013). Here, too, young birds on their first migration proved unaffected; adult birds that departed within ten days of treatment were random in their directions, while those that departed after ten days took their normal migratory direction. Overall, these experiments demonstrated the use of the magnetic sense in navigation, as opposed to compass orientation alone. The latter

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apparently depends on the second magnetic receptor (in the eyes) which is immune to pulse treatment. This was probably why juveniles, relying on compass orientation alone, were unaffected by pulse treatment. Studies in which migrants were displaced, either in reality or virtually by simulating in a cage the magnetic conditions of a distant region, also implicated the use of a magnetic sense in navigation. Nocturnally migrating Eurasian Reed Warblers caught on spring migration at Rybachy in the eastern Baltic showed a NE orientation (towards their nesting areas) when tested locally in orientation cages. But when these birds were moved about 1000 km eastward to the Moscow region (and outside their breeding range), tests showed an NW orientation (Chernetsov et al., 2008). This new direction would lead them to their normal breeding areas. Evidently, the warblers were able to detect their longitudinal displacement and correct for it by changing their heading to their breeding areas, implying the use of bicoordinate navigation, including the assessment of longitude. This experiment did not reveal which navigation system was used by the displaced birds, so in another experiment, Eurasian Reed Warblers caught on spring migration at Rybachy were again tested in orientation cages and were found to head northeast (Kishkinev et al., 2015, 2021). But when these birds were experimentally exposed at Rybachy to the magnetic conditions (of intensity, inclination and declination) found 1000 km further east near Moscow, they changed their heading to northwest (Figure 11.4). This occurred even though the birds were displaced virtually rather than in reality and were exposed naturally at the time to all the other navigation cues available at Rybachy. The implication was that magnetic information alone was sufficient to cause a change in migration direction after a large simulated longitudinal shift in position. A further experiment showed that birds did not make this directional change if the ophthalmic branch of their trigeminal nerve was cut, preventing magnetic information travelling from the beak region to the brain. This result provided further evidence that the birds were using magnetic cues to measure a longitudinal shift (Kishkinev et al., 2013; Pakhomov et al., 2018). Unlike celestial cues, this method would not involve the use of time shift. The various experiments described above, and many others, leave no doubt that many birds are able to navigate using the earth’s magnetic field.

FIGURE 11.4 Results of the virtual magnetic displacement study on Eurasian Reed Warblers (Acrocephalus scirpaceus). Centre: a map of the capture site (Rybachy, Kaliningrad region), the site of virtual displacement (Zvenigorod, Moscow region) and the breeding range of Eurasian Reed Warblers in the region (shaded middle grey). The solid arrow on the map shows the virtual displacement direction and distance. The broken arrow at the capture site shows the mean migratory direction of Eurasian Reed Warblers passing through Rybachy, and the broken arrows at the virtual displacement site show the two working hypotheses: (1) no compensation, or (2) compensation towards the breeding destinations (solid line oval). The circular diagrams show the orientation of Eurasian Reed Warblers tested at the capture site during spring migration 2004 07 (a) and 2012 13 (c) and the same birds’ orientation after a physical (b) or virtual (d) 1000 km eastward displacement. The data in circular diagrams (a) and (b) are from Kishkinev et al. (2013). Each dot at the circle periphery indicates the mean orientation of one individual bird; arrows show mean group vectors; the dashed circles indicate the radius of the group mean vector needed for 5% and 1% levels of significance according to the Rayleigh test of uniformity; solid lines flanking mean group vectors give 95% confidence intervals for the group mean directions. From Kishkinev et al., 2015, reproduced on a Creative Commons Licence.

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Pelagic seabirds In such a featureless environment as the open ocean, one might expect that pelagic seabirds would use magnetic information to navigate. But whether they do or not, evidence implies that they do not necessarily need it and can return to a known site on alternative cues. Cory’s Shearwaters (Calonectris borealis) carrying magnets on both wings and head (to disrupt perception of the earth’s magnetic field) were released 160 and 900 km from their breeding colony (Massa et al., 1991). They homed with the same success as control birds released without magnets. The same held for nine Wandering Albatrosses (Diomedia exulans) which had magnets fixed to their heads, along with back-transmitters to reveal their movements (Bonadonna et al., 2005). On their normal foraging flights over several thousand kilometres, these birds showed no impairment in their ability to return to specific nest sites compared with control birds equipped only with transmitters. The two groups showed no differences in trip duration or length or in directness of the homeward flight, implying that these birds did not require magnetic cues to navigate back to their nesting colonies. The same held for Waved Albatrosses (Phoebastria irrorata) on their foraging flights between the Galapagos Islands and the Peruvian coastline (Mouritsen et al., 2003), for nesting White-chinned Petrels (Procellaria aequinoctialis) caught and displaced 300 360 km (Benhamou et al., 2003), and also for Cory’s Shearwaters displaced about 800 km (Gagliardo et al., 2013). In these and other experiments, geomagnetic information did not seem crucial, presumably because alternative cues were available (see below). However, such experiments are based on the assumption that magnets attached to the birds do indeed prevent them from reading the earth’s magnetic field, which may not necessarily be true, considering that birds can ‘tune in’ to particular levels of intensity (gauss values, Wiltschko, 1978). At least one study did imply the use of magnetic information by a pelagic seabird. Ring recoveries obtained over the last 80 years were used to investigate whether magnetic inclination might be used as a navigational aid by Manx Shearwaters returning from the southern hemisphere to their natal areas in the northern hemisphere, usually 3 years after fledging (Wynn et al., 2020). For any one location, the angle of magnetic inclination changes slightly from year to year, drifting either north or south by about 1.34 degrees (nearly 150 km) but retaining the same average position in the long term. In this study, most birds joined their natal colony, and only birds recruited to other colonies were examined to see whether their colony change correlated with latitudinal change in the Earth’s magnetic field in the years between fledging and recruitment. Remarkably, findings were consistent with this proposition. In years when the angle of inclination of the natal colony had shifted north, the average latitude of recruitment was to the north, and when the angle of inclination had shifted south, so had the average latitude of recruitment. As these findings fulfilled their prior predictions on the magnitude and direction of latitudinal shift, the authors suggested that (1) natal magnetic inclination had been learned prior to fledging; and (2) it was used to provide latitudinal information when making the first return trip from the wintering grounds. The birds must presumably have used some other cue to arrive at the correct longitude of their natal site. The adults, returning each year to their former nest sites, were evidently less influenced by the year-toyear variations in magnetic cues. In the section above on the use of the star compass, it was explained how birds kept artificially under spring or autumn daylengths would show southward or northward directional preferences, as appropriate. There is also evidence that a magnetic response may influence the direction taken at migration time. One study used Bobolinks, transequatorial migrants from the New World. When the magnetic inclination angle was experimentally switched from northern to southern positions in a planetarium with seasonally appropriate, but stationary, star patterns, Bobolinks captured in late summer changed orientation from southward to northward after 1 5 days under the new magnetic regime. It was suggested, therefore, that these birds may use the earth’s magnetic field as the primary cue for orientation (Beason, 1989). Similar findings emerged in a southern hemisphere diurnally migrating species, the Yellow-faced Honeyeater Lichenostomus chrysops of Australia (Munro & Wiltschko, 1993). In outdoor tests in spring, captive birds preferred southerly (poleward) directions when tested in the local geomagnetic field. But under a magnetic field with a reversed vertical component (that is, with inclination pointing down rather than upwards) the birds reversed their directional tendencies and oriented northward (equatorward). These results again implied the use of the magnetic field for direction finding through assessment of magnetic inclination.

Response to specific areas (location cues) There is another way in which the earth’s magnetic field seems to be involved in bird migration. Many landbirds that cross deserts or oceans accumulate the necessary fuel reserves just before embarking on the crossing, which may occur part way through their journeys. Others change direction at particular points in their journeys. They evidently ‘know’ that they have reached an appropriate place to accumulate large body reserves or change direction, even though they

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may never have made the journey before. One possible mechanism involves an inherent time response: after a given period from the start of migration, the bird changes its behaviour. Another possible mechanism involves response to the specific conditions found at particular sites. Experiments using an artificial magnetic field implied that some birds use magnetic information to indicate regions where they must accumulate large fat reserves before crossing a barrier, change direction, or stop migrating. For example young hand-reared Pied Flycatchers from central Europe showed a distinct change in compass heading when exposed in captivity to values of the magnetic field normally encountered in southern Europe, where the normal migratory route shifts from southwest to south. But the altered magnetic field was followed by the shift in orientation only when applied at the appropriate time during the migratory period (Beck & Wiltschko, 1988). In Pied Flycatchers, therefore, the magnetic conditions of the location where the change is to occur and the time programme seemingly interact to produce an appropriate innate response at an appropriate location. These specific magnetic conditions acted as a signpost and initiated the next leg of the journey. In other experiments, some juvenile Thrush Nightingales (Luscinia luscinia) were caught in autumn in Sweden and exposed to the geomagnetic conditions (intensity and inclination) normally experienced in northern Egypt. They quickly accumulated high-fat levels appropriate for their subsequent desert crossing (Fransson et al., 2001; Kullberg et al., 2003; Henshaw et al., 2008). This happened whether they were exposed to a step change in magnetic field (as when they were switched suddenly from Swedish to Egyptian conditions) or to a gradually changing field, as they would normally experience on migration. Both groups contrasted with control birds, exposed throughout to the geomagnetic conditions of southern Sweden, which accumulated much smaller fuel loads more slowly. However, birds trapped late in the onset period of autumn migration accumulated a high fuel load irrespective of magnetic treatment. It seemed that the relative importance of endogenous and environmental factors in the fattening of individual birds was affected by date, as well as by location (see also Chapter 12). These experiments suggested that fuelling decisions encoded in the endogenous migration programme depended on external (and local) geomagnetic information. Later studies on other migratory species gave similar results (for European Robin, see Kullberg et al., 2007; for Northern Wheatear (Oenanthe oenanthe), see Bostro¨m et al., 2010, 2012b). All these experiments involved juveniles, implying that the response to particular locations (a sort of map sense) was innate, not dependent on previous experience, and was elicited when the bird encountered specific magnetic conditions. Further experiments implied the use of magnetic information in re-finding areas previously experienced. For example adult Silvereyes (Zosterops lateralis) used magnetic conditions to signal when they had arrived in their wintering areas, previously experienced (Fischer et al., 2003). Adults were tested near the mid-point of their south north migration in southeast Australia. Birds exposed in captivity to artificially generated magnetic field values of inclination and intensity normally experienced near the start of their migration orientated north-northeast as appropriate. In contrast, birds exposed to magnetic field values that they would experience near the end of their migration ceased to show any significant directional preference; in this respect, they acted as though they had arrived in wintering areas. In contrast, no effects of changing the artificial magnetic field were noted on inexperienced young birds caught prior to their first migration, another indication for this species that juveniles migrate on a different system from experienced adults. These experiments gave results in line with the findings reported above of Manx Shearwaters apparently returning to their natal areas for the first time using magnetic cues. In summary, experiments have implied that birds use the magnetic field to trigger particular responses. The specific magnetic conditions found in particular areas on migration routes have been found to trigger extra fuel deposition (ahead of a long flight), a directional change, or an end to a migratory journey. If young birds in the wild are responding in the way that experimental findings suggest, they are not just using a clock-and-compass system on their first migration but are also benefiting from an inborn response to the magnetic signals of specific regions.

Magnetic cues and vagrancy Further evidence for the use of a magnetic sense comes from the fact that migrating birds can respond to natural fluctuations in the earth’s magnetic field, especially during nocturnal solar storms when the natural force lines can become temporarily distorted (Moore, 1977; Bianco et al., 2019). Among data from two million captures of 152 landbird species in North America over 60 years, a strong association emerged between natural disruptions to the Earth’s magnetic field and the levels of avian vagrancy recorded during autumn migration (Tonelli et al., 2023). In addition, increased solar activity, which disrupts the avian magnetoreceptor, generally counteracted this effect, possibly by disabling the ability of birds to use the magnetic field to orient, and forcing them to use different cues. These findings further signify the importance of the magnetic field to migrating birds, and also link its temporary distortion to avian vagrancy.

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ODOURS As humans, we are poorly equipped to appreciate any odour gradients that might occur in the outside world, but even with our impoverished senses, we can detect aromatic differences (due largely to changing vegetation) as we travel, for example from the Mediterranean through temperate to boreal regions. To many scientists, it seemed unlikely that suitable atmospheric odours could have a sufficiently stable distribution to provide reliable spatial information, adequate for navigation. However, a study in Germany revealed that various volatile organic compounds were indeed distributed on fairly stable gradients in the atmosphere (Wallraff & Andreae, 2000). These gradients were sufficiently constant to allow odour-based navigation, although odours may change with season, as well as with geographical location. Stable ratios, rather than absolute concentrations, of at least three different compounds were reckoned as sufficient to provide enough information for displaced pigeons to return home over short distances. Such odour gradients could theoretically also allow long-distance navigation well beyond a few hundred kilometres. There is now no doubt that some bird species use olfaction (smell) in navigation. Until 50 years ago, the olfactory sense was considered insignificant in most birds, and olfactory cues had never seriously been considered as possible sources of information for position-finding. The ability of homing pigeons to find their home loft in a local area on the basis of odours was first discovered by Papi et al. (1971, 1973) working in northern Italy. Unmanipulated pigeons released at varying distances up to 61 km from the home loft quickly returned, whereas ‘anosmic’ birds (whose olfactory nerve had been severed or rendered insensitive) released at the same time usually failed to return. In one experiment, only 4 out of 19 anosmic birds returned to their home loft, compared with 38 out of 40 control birds. These and other findings led to the notion that pigeons at the home loft learn the local odours carried by the winds from different directions and can use the local odour-scape as a compass. Unsurprisingly, this idea met with scepticism. Opponents doubted that pigeons would have this ability and also questioned the existence of environmental odours sufficiently stable in distribution to enable navigation. In addition, experiments in different regions gave some different results, which at the least implied that pigeons relied less on odours in some regions than in others. In a later experiment replicated 10 times, pigeons were transported in airtight containers ventilated by air purified by charcoal filters to a ‘false release’ site more than 25 km away, where they were allowed to breathe the local air for a few hours (Benvenuti & Wallraff, 1985). Then the birds were transported in pure air to a new site located in the opposite direction with respect to home. Here they were subjected to nasal anaesthesia and released. At the false release site, these birds had experienced the local odours, while at the true release site they were immune to the local odours. The birds then oriented towards what would be the home direction from the false release site, while the control birds exposed to the local air at the true release site oriented towards home. Each set of experiments was repeated so that the false release site in one trial became the true release site in the next, and vice versa, strengthening the conclusion that pigeons make use of local odours in their homing behaviour. Pigeons also use visual landmarks in a familiar area to find their way home, and for convincing evidence of the role of olfaction, the possibility of visual evidence had to be eliminated. This was done in an experiment exploiting the ability of pigeons to show homeward orientation in a cage at a release site. The orientation before take-off from a circular arena was recorded for both anosmic and intact pigeons displaced to familiar sites (Gagliardo, 2013). The birds were tested twice from each of three sites, but in one test the birds could view the surroundings, while in the other the arena was surrounded by a screen to prevent this. The intact pigeons displayed homeward orientation in both visual conditions, but the anosmic birds headed homeward only when they could see the landscape. This was interpreted as showing that pigeons can orientate correctly using either visual or olfactory cues. Forty years of experiments conducted in different countries by different people have demonstrated that pigeons deprived of their sense of smell and released at unfamiliar locations are, in most cases, randomly scattered or oriented in a direction different from home and are invariably impaired in their ability to find home (Wallraff, 2005; Gagliardo, 2013). It is not known which odours are important to birds, but pigeons proved able to incorporate artificial odours in their olfactory map if exposed to air currents blowing artificial odours from specific directions (Papi et al., 1974; Ioale` et al., 1990). They learned to recognise these odours and associate them with a particular place. Considering all the evidence accumulated over the years, visual familiarity with the release site area turned out to be the only alternative source of information allowing navigation in olfactory-deprived pigeons. They seemed not to have used magnetic information, even though other experiments show they can detect it. Turning to wild birds, much reduced homing ability was detected in anosmic Common Swifts (Apus apus) displaced 47 66 km from their nesting colony in Italy (Fiaschi et al., 1974), and in anosmic Common Starlings displaced more than 60 km from their nesting colony in Bavaria (Wallraff et al., 1995). Evidence for the role of olfaction in longdistance migration also emerged from a study on Lesser Black-backed Gulls (Larus fuscus) displaced 1080 km

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westward from the normal migration route. Displaced gulls did not correct for their displacement when the olfactory nerve was cut, whereas displaced intact gulls were corrected for their displacement and headed towards their normal wintering area (Wikelski et al., 2015). Procellariform birds have a particularly well-developed olfactory sense (Chapter 10) so seemed especially likely to use odours in navigation. These birds have long been known to find food in the ocean by smell and similarly to find their burrow or mate in the colony at night (Benvenuti et al., 1993; Bonadonna et al., 2003; Dell’Ariccia & Bonadonna, 2013; Nevitt, 2008). But the question remained whether these birds use olfaction to guide their long-distance flights, rather than magnetic or other cues. One experiment involved the displacement by boat of Cory’s Shearwaters from their nests in the Azores Islands for release in the open ocean about 800 km away (Gagliardo et al., 2013). Powerful magnets were attached to the heads of one group of birds to disrupt inputs from the earth’s magnetic field, while a second group was rendered anosmic by coating their nasal mucosae with zinc sulphate (which deadens the surface cells until a new layer forms a few weeks later). Satellite-tracking devices were used to assess the birds’ performance, for comparison with a third, control group of unmanipulated birds. Most control birds headed homewards soon after their release and were back on their nests within a few days. Magnetically disrupted birds showed a similar pattern, in line with experiments reported above. But anosmic birds were poorly oriented and roamed widely over the eastern Atlantic, showing very poor homing. The implication was that a sense of smell was crucial to getting these birds home swiftly, but a magnetic sense was not. While ranging close to their colonies, shearwaters probably learn the geographical distribution of different odours, their ratios or gradients and are able to use this information in a map-like way to extrapolate their position beyond familiar areas. This is no different from the assumptions made concerning the use of celestial or magnetic cues. Knowledge of the odour-scape can presumably accrue bit by bit as birds progressively extend the area with which they are familiar. This does not mean that seabirds do not use other (visual) cues where they are available. In the Mediterranean Sea, where coasts and islands abound, experiments involved Scopoli’s Shearwaters (Calonectris diomedia), which were taken from an island off Italy and released 500 km away off Barcelona, out of sight of land (Pollonara et al., 2015). Magnetically disrupted birds homed rapidly or fairly rapidly, as did controls, but anosmic birds again took much longer. Tracking revealed that anosmic birds made greater use of familiar coastlines which were more readily available in the Mediterranean than in the open ocean where earlier experiments were made. It seemed that shearwaters could map their ranges on a large scale, using learned landscape features when in sight of land, but they became more dependent on olfactory or other cues over the open ocean. In another experiment, the free-ranging foraging trips of incubating Scopoli’s Shearwaters were GPS-tracked over the Mediterranean (Padget et al., 2017). Again, individuals were either made anosmic with zinc sulphate solution, magnetically impaired by attachment of a strong magnet or used as controls. Birds from all three treatments embarked on foraging trips had indistinguishable at-sea schedules of behaviour and returned to the colony having gained mass. However, in the pelagic return stage of their foraging trips, anosmic birds were not oriented towards the colony although coastal navigation was unaffected. These results imply that seabirds use an olfactory map to guide them across seascapes but can also use landscape features close to shore. Trials with albatrosses, mentioned above, revealed that birds could return to their home colonies from far away with their magnetic system disrupted. Olfaction remained an alternative mechanism they may have used. It is now accepted that odour gradients exist over oceans in the same way as other odour gradients exist over land (Nevitt, 2008). At large spatial scales (thousands of square kilometres), an olfactory landscape superimposed upon the ocean surface reflects oceanographic or bathymetric features where phytoplankton accumulate and an area-restricted search for prey is likely to be successful. At smaller spatial scales (tens to hundreds of square kilometres), birds could use both odours and visual cues to pinpoint prey directly. It is still uncertain to what extent the birds have to learn the odour-scape, in addition to having inherent tendencies to seek out particular odours. Priority questions for future research include: how widespread is olfactory navigation among birds; does oceanic navigation performed by seabirds depend critically on olfactory cues; are such cues only used for homing to the nest and finding food or are they also a key component of navigation during migration; and do birds exploit any convenient atmospheric signal, or rely on specific types of chemicals? While some bird species seem to use olfaction as a preference, others clearly do not. For example Eurasian Reed Warblers rendered anosmic, together with untreated controls, were moved between the same capture and displacement sites (Rybachy and the Moscow region) where earlier tests were performed (Pakhomov et al., 2018; Kishkinev et al., 2020). Following release, birds were tracked for the first few kilometres using an array of automated radio-tracking towers. Both anosmic and intact warblers showed an anticlockwise re-orientation towards the northwest, implying that neither group used olfaction to re-orientate, and supporting the earlier conclusion on the role of magnetic cues. So at least in this nocturnal songbird migrant, the olfactory system was not crucial for determining geographic position.

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INFRASOUND AND PRESSURE CHANGES Infrasound derives mainly from physical processes, such as wind against mountain ridges or waves on shorelines, and can travel over hundreds of kilometres (Chapter 10). Given their stability, such sounds could give strong directional clues to birds able to detect them. They could in theory provide infrasound maps which birds could learn to use in navigation. There is no proof that birds do use infrasound in this way, but the possibility has often been raised (Hagstrum, 2001). For example Gschweng et al. (2008) tracked some Eleonora’s Falcons (Falco eleonorae) from their breeding islands in the Mediterranean to their wintering areas in Madagascar. They suggested that young Eleonora’s Falcons could have used infrasound over part of the route, particularly to find the shortest crossing from Africa to Madagascar (about 200 km which some birds flew at night). One tracked juvenile which landed near the central coast of Mozambique moved slowly north along the coastline for three days until it located the shortest crossing. Birds and other animals also react to temporary disturbances, such as avalanches, volcanoes, sunamis and distant storms, all of which produce infrasound. Sonic booms from aircraft can also disrupt the performance of homing pigeons (Hagstrum, 2001). Sometimes birds also behave in a way which suggests that they can predict impending weather, for example by postponing migration when a storm is brewing. An example of storm avoidance was provided by some Golden-winged Warblers (Vermivora chrysoptera) in the south-eastern United States (Streby et al., 2015). In April 2014 five males arrived back on their breeding areas in Tennessee. Soon afterwards, a tornado approached, causing massive damage across the region. At least 24 hours before the storm’s arrival at their breeding area, these warblers left, embarking on a 1500 km clockwise circuit towards Georgia and Florida. After a 5-day absence and the passage of the storm, the warblers returned to their territories in Tennessee. What alerted the birds to the approach of the storm was unknown, but changes in infrasound were suggested, probably pre-empting any change in air pressure. Nevertheless, birds may be able to detect impending storms by monitoring barometric pressure, changes in which may help birds in moving from areas of high to low pressure or vice versa. Using either infrasound or this related pressure sense in arid lands, birds could move towards distant areas where rain is falling, and where habitats will soon become suitable. Such behaviour has been recorded among birds in desert areas of Australia and elsewhere but has so far defied explanation (Chapter 17). Such a pressure sense could also assist migrants in maintaining their flight altitude, and homing pigeons have proved able to detect barometric pressure changes equivalent to those occurring over 10 m altitude or less (Keeton, 1980).

CUE CONFLICTS The various compass cues discussed above vary in their availability and reliability according to geographical location, season, weather and time of day. Birds would therefore be expected to use different cues in different situations, to give precedence to certain cues over others where they give conflicting messages and to re-calibrate their different compasses frequently against the most reliable ones. Research has aimed to find which of these various cues are used for preference in different circumstances and which (if any) provide the ultimate reference for calibration purposes (for reviews see Emlen, 1975; Able, 1993; Wiltschko et al., 1997; Muheim et al., 2006a,b; Newton, 2008; Sjo¨berg & Muheim, 2016). Most cue-conflict experiments involved presenting a caged bird with two (or more) orientation cues at once, manipulating one of them while leaving others unchanged, and then monitoring the response of the bird (Able, 1993; Muheim et al., 2006a,b). A typical experiment might involve placing an orientation cage surrounded by an electric coil outdoors under a clear night sky. The bird in the cage would then have access to two known orientation cues, the stars and the magnetic field. The coil could be used to shift the direction of magnetic north as perceived by the bird so that magnetic compass directions differ from star-based ones. If, as compared to control birds tested in an unaltered magnetic field, the experimental birds changed direction in line with the magnetic field shift, one would conclude that in this situation magnetic information took precedence over stellar information. Just such an experiment was conducted on three species of Sylvia warblers and European Robins captured on migration (Wiltschko & Wiltschko, 1975a,b). When the directions of stellar and magnetic north were at variance, the birds seemed to orient preferentially with respect to magnetic cues. The warblers changed direction during the first test in the conflict situation, but the Robins took several nights of cue conflict before they changed (a finding later replicated on the same species elsewhere; Bingman, 1987). Many cue-conflict experiments have been done over the years. While most involved the use of orientation cages, others used free-flying birds tracked in the wild. For example Catharus thrushes were caught on migration in North America and exposed to an experimentally deflected magnetic field during twilight, and then released and radio-tracked

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on their subsequent night flights (Cochran et al., 2004; Cochran & Wikelski, 2005). Their tracks indicated that the thrushes relied on their (mis-calibrated) magnetic compass for the nocturnal flight, apparently ignoring stellar cues. The experimental birds changed to normal orientation again on succeeding nights, apparently having recalibrated their magnetic compass (correctly) back to north, presumably on celestial cues. However, in a similar experiment, free-living Song Thrushes (Turdus philomelos) did not recalibrate their magnetic compass from solar twilight cues but rather showed a simple domination of either a magnetic or stellar compass (Chernetsov et al., 2011). Other birds, tested in orientation cages and apparently migrating on a magnetic compass, made no change in directional preference when exposed to conflicting sunset (polarization) cues (Wiltschko et al., 2008; Schmaljohann et al., 2013). So ˚ kesson et al., 2015). Some natural variataken as a whole, experiments have given variable and often contradictory results (A tion in response to different cues would be expected, depending especially on time of day and location, and different birds may have different hierarchies of orientation cues. But aspects of the experiments also proved relevant. Among birds tested in orientation cages, only birds which were exposed to the full sky with a view of the horizon showed directional change under a cue-conflict, the birds apparently using sunset/polarized light cues to recalibrate their magnetic compass (Bingman, 1983; Prinz & Wiltschko, 1992; Able & Able, 1995; Weindler & Liepa, 1999; Cochran et al., 2004). No such re-calibration occurred in birds tested in funnels or cages which prevented them from seeing the horizon (and hence the sunset). Most of these studies revealed a dominance of magnetic cues over celestial ‘sunset’ cues (Muheim et al., 2006a,b, 2007, 2009). Nevertheless, as mentioned above, free-flying birds which could see the horizon also varied in their response to cue-conflict experiments, some showing dominance of celestial over magnetic cues and others the reverse.

Conclusions on cue-conflicts and recalibration So what conclusions can be drawn on cue conflicts? Individual birds can apparently use information from several compass mechanisms, with emphasis on whatever cues are most reliable in the conditions prevailing. They may switch from one type of cue to another during the course of a journey and may continually calibrate one against another, depending on location, weather and light values (Wiltschko et al., 1998a,b; Muheim et al., 2003). With one type of cue calibrated against another, magnetic and celestial compass mechanisms are not strictly independent of one another but could be viewed as different components of an integrated system of direction finding. The resultant recalibration process ends the conflict so that all directional information is in harmony again, and birds can derive their direction of flight from any available cue (Wiltschko & Wiltschko, 2015). But whatever their sensory capacities, birds may be better able to fix their position and future direction when stationary on the ground than when in migratory flight (Lack, 1960), and major changes in direction generally follow major stopovers, as shown by tracking studies. As mentioned above, birds apparently need a few days to learn the movement patterns of the sun or stars or local magnetic conditions in a new place to be able to fix their position or re-assess their future direction precisely.

Problems at high latitudes Migration routes in the Arctic and Antarctic are of special interest. It is near the poles where the longitude lines are closest together so that migrants become exposed to the most rapid time-shifts, and where birds are faced with difficulties in using any sort of recognisable compass. The use of a sun compass brings problems of time compensation during rapid longitudinal (east west) displacement, but is still usable. Use of a star compass is not possible in the polar summer because, under continuous daylight, stars are not visible for up to several months, and during this light period, there is also no dawn or dusk, when skylight polarization patterns are most apparent. In addition, a magnetic compass is unreliable in a wide region around the north and south magnetic poles owing to the rapid changes in declination of the geomagnetic field in those regions, as well as the very steep angles of inclination. The temporal variations in the geomagnetic field during magnetic storms are also particularly large around the poles. At high latitudes, therefore, complications surround the use of both celestial and magnetic compasses. Orientation ˚ kesson et al., experiments at high latitudes confirmed that birds made use of celestial cues (Ottosson et al., 1990; A 2001), but also that they could detect magnetic information, despite the high angle of inclination (Muheim et al., 2003). White-crowned Sparrows (Zonotrichia leucophrys) under simulated overcast could select a magnetic compass course ˚ kesson et al., 2001). This finding implied a very where the inclination angle was less than 3 degrees from the vertical (A accurate receptor in a species that does not normally live at such high latitudes. Nevertheless, the combined experience of both the night sky and the geomagnetic field seemed crucial for songbirds at high latitudes to find the appropriate direction to a specific wintering area (Weindler et al., 1996). Once a bird has established geographic north and south with respect to the local geomagnetic field, magnetic cues could come to assume a greater role in navigation.

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Problems at low latitudes On the equator, days are the same length (12 hours) year-round, and the sun is overhead at mid-day, reducing its value as an indicator of north or south. Birds migrating from the north have the sun in front of them as they head south, and as they cross the equator they have to adjust to having the sun behind them. For stellar orientation, an unobstructed view of the centre of the rotating night sky is no longer available near the equator, as this centre has sunk to appear closer to or below the horizon. However, new star patterns become available in this region, and follow a simpler path across the sky, rising in the east, and then again disappearing below the horizon in the west. Stellar orientation based on experience from high latitude breeding areas can therefore be expected to be challenging in equatorial regions, but we can assume that birds on migration have the capacity to learn new star patterns for orientation as they become visible near the equator (Emlen, 1967, 1970). Another problem, already mentioned, is that the magnetic force lines run horizontally in equatorial regions, making it potentially difficult for migrants using an inclination compass to distinguish north from south. This raises the question how far they have to ˚ kesson, 1993). In laboratory conditions, birds can distintravel to obtain magnetic cues that distinguish north from south (A guish inclination angles in equatorial regions as low as 5 degrees from the horizontal (Schwarze et al., 2016), which would be reached about 560 km from the equator on either side.

RHUMBLINES AND GREAT CIRCLES A further question concerns the type of route that birds take on their journeys, considering that they are travelling over the surface of a large sphere. The most straight-forward procedure would be to set off in an appropriate direction and maintain the same heading throughout the journey on a rhumbline (loxodrome) route. This type of journey has simple navigational needs, and if it ran directly north south, it would also be the shortest route between two points and would not involve a time shift. However, if the journey had an easterly or westerly component, crossing lines of longitude as most routes do, a constant heading would still be the simplest but not the shortest route. A great circle (or orthodrome) route covers the shortest distance between two longitudinally separated points on a sphere, but it requires continual change in direction during the journey (Figure 11.5). Great Circle routes are thus more demanding than rhumbline routes in their navigational needs. Among the known mechanisms, only a sun compass with no compensation for changes in local time would lead birds along a track similar to a great circle route across longitudes. Such a track is apparently flown by shorebirds travelling across longitudes in the high Arctic (Alerstam, 2011; Kok et al., 2020). However, another way in which birds Queen Elizabeth Islands

1A

Taimyr

2A

1B 2B Iceland

Wadden Sea FIGURE 11.5 Great circle (orthodrome) and rhumbline (loxodrome) routes between points of departure and destination for migratory flights by certain high arctic shorebirds and Brent Geese (Branta bernicla), drawn on a Mercator map projection. Between Iceland and the Queen Elizabeth Islands, great circle (1A) distance and courses are 2535 km and 328 degrees/265 degrees (initial/final course). Rhumbline (1B) distance and course are 2665 km and 300 degrees throughout. Between the Wadden Sea and Taimyr Peninsula, great circle (2A) distance and courses are 4234 km and 23 degrees /110 degrees (initial/final course). Rhumbline (2B) distance and course are 4634 km and 59 degrees throughout. Spring flight routes by the high arctic migrants are in agreement with rhumbline but not with great circle routes. Modified from Alerstam (1990). Further notes: Projecting the rounded surface of the earth onto a flat, two-dimensional map causes inevitable distortions which are important to bear in mind when charting and analysing migration routes, or when plotting the geographical ranges of birds. The familiar Mercator projection (a cylindrical projection), as used above, is useful because it represents routes with constant geographical courses (rhumblines or loxodromes) as straight lines. This type of projection has been traditionally used for nautical charts. However, because the longitude lines are drawn parallel to one another rather than converging towards the poles, the scale varies with latitude on this projection, so that polar distances and areas are exaggerated in comparison with equatorial ones.

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might achieve an approximate great circle route, but using rhumbline navigation, would be to divide the journey into stages, with one or more appropriately positioned stop-sites, flying straight from one to another, but making a directional change at each one. Such dog-leg routes are common among migrating birds, often taken to avoid long water crossings or high mountains, or make use of refuelling sites that are somewhat off course. The journey is thus divided into successive stages with different main orientations. Most of the migrants that travel in autumn from Western Europe to Africa migrate southwest into southern Iberia and then, benefiting from the short sea-crossing, take a more southerly course into Africa. Without this change in direction, they would end up over the Atlantic Ocean. Overall, straight rhumbline routes based on constant compass headings appear more likely for many bird populations, especially those migrating only short distances, and are consistent with the routes frequently recorded within Europe or North America by ringing and tracking studies. They also fit the experimental evidence (based mainly on songbirds) of a genetically fixed directional preference that steers inexperienced juveniles towards their wintering areas (although they may change directions at specific points in their journeys). From the tracks taken by individual birds on migration, several studies have attempted to work out, not only whether they followed rhumblines or great circles but also which navigation system they are likely to have used, whether celes˚ kesson & Bianco, 2017; Thorup et al., 2006; Sokolovskis et al., 2018). In general, such studies retial or magnetic (A affirm that many long-distance migrants probably used different compass systems in different regions, different seasons, different weathers or times of day. This may largely explain why tests of orientation mechanisms sometimes gave different results in different experiments on the same species (Mouritsen, 2018). In addition, while birds may use celestial or magnetic cues over most of a long-distance flight, they are clearly dependent on visual landmarks near the end of their journey when homing into their destination, and seeking roosting or nesting places (Mouritsen, 2018).

DISPERSIVE MIGRATION Research on the inheritance of migration has mostly concerned species in which individuals show the same narrow migration direction, which either is controlled genetically or is partly learned by following more experienced individuals. It is as yet unknown whether similar control mechanisms apply to dispersive migrants, in which birds from a single population can move away in various directions after breeding to separate wintering areas (Guilford et al., 2011). In many seabird species, for example individuals seem to scatter after breeding in random directions from the colony (spanning 360 degrees unless constrained in certain directions by land areas, Chapter 8). Could individuals, programmed to migrate, select random directions in their first year and then stick to the same routes in subsequent years or could they choose different directions in different years, with little or no consistency between years? Among seabirds, both patterns have been described from tracking studies. Individuals of some species stuck to the same routes and wintering areas from year to year (for Atlantic Puffin (Fratercula arctica), see Fayet et al., 2016; for Northern Gannets (Morus bassanus), see Fifield et al., 2014), while individuals of other species showed high variability in routes and wintering areas from one year to the next (for Cory’s Shearwater, see Dias et al., 2013). Whether these different types of behaviour are species-specific or result from conditions at the time remains to be seen. In general, however, dispersive migrants seem to differ from other migrants only in the much wider range of directions taken, while other aspects of migration seem similar to those of other birds (Chapter 19).

CONCLUDING REMARKS Pulling together findings from both this and the previous chapter, the known navigational tools available to migrating birds include (1) celestial compasses based on the sun, skylight polarization and stars; (2) a magnetic compass based on components of the earth’s magnetic field; (3) an olfactory map based on consistent odour gradients, (4) an internal clock, recording diurnal (circadian) and longer-term changes; (5) an inherited mean migratory direction and time programme, which together ensure that the bird flies in an appropriate direction for an appropriate time; and (6) a map sense used for reaching previously experienced places. The last also implies a good spatial memory. In addition to these various route-finding mechanisms, birds seem also to possess a ‘location response’, through which they use magnetic or other conditions in specific target areas to signal a change in behaviour leading to greater fat deposition, a change in direction or a halt to migration. This innate mechanism may operate in conjunction with an internal clock and applies in both adults and juveniles. Several lines of evidence imply that birds can locate such specific locations (signposts) from a distance for example by following the gradients in the magnetic field and are not merely reacting to them once they are there. In theory, such a location sense could provide an alternative means to the clock-and-compass system through which juveniles could find a wintering area appropriate to their population.

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Equipped with these navigational aids, a bird could use at least five different route-finding strategies: 1. In guiding or ‘follow-the-leader’, some birds in migratory condition might complete their migration by following other individuals which know the way, thereby learning the route, as in the waterfowl and cranes discussed in Chapter 10. Any birds using this method would benefit from a back-up mechanism (eg clock-and-compass) in case they were left to travel on their own. They would also need to be selective in the birds they follow, either through timing or recognition or they might otherwise follow the wrong birds to the wrong wintering area (as happens occasionally). Birds that travel in flocks, or at least in contact with other individuals, can also reach collective decisions on where to head at any point in the journey (Chapter 10). 2. In piloting, a migration route can be retraced by using a sequence of learned landmarks (as shown in homing pigeons; Biro et al., 2004; Meade et al., 2006). This method would require birds to build a landmark-based map during a previous journey which could then be retraced during subsequent journeys. Such landmarks could be visual, magnetic or olfactory, and in theory also auditory. This is not a method for inexperienced migrants but could help birds return to known areas. Both experienced and inexperienced migrants could also use a succession of landmarks, selected at the time, to steer a straight course, minimizing the effects of drift. 3. In clock-and-compass (vector) navigation, birds aim to head in a constant migratory direction (which may change one or more times during a journey) for an innately determined amount of time controlled by the internal clock (Chapter 10). By this mechanism, birds could reach previously unknown but appropriate wintering areas. Theoretically, birds of all ages could use this orientation strategy which has been demonstrated experimentally in young passerines and others. With this facility alone, however, birds are unable to determine their position and may therefore be unable to correct for serious drift, directional mistakes, over-flight, or experimental displacement. 4. Travelling between signposts. It is difficult to explain how a simple clock-and-compass programme can lead inexperienced birds from a wide breeding area to converge on a small area, such as narrow sea-crossing or a localised refuelling area on route, unless they can aim for specific target areas (signposts) using innately coded external cues. In this way, birds might keep one course until they reach signpost A, and then maybe change direction to reach signpost B, and so on until their reach their species-specific wintering area, as the final signpost. The response of birds to the specific magnetic conditions in particular areas is the most tested mechanism. 5. In bi-coordinate navigation, birds can sense at least two global coordinates forming a reliable grid through which they can determine their geographical position and homeward direction, even outside areas previously experienced. Bi-coordinate navigation could provide continual positional feedback, enabling birds to correct for drift or directional mistakes. Theoretically, birds of all ages may have this facility, but experimental evidence from several species suggests that it is used primarily by experienced birds returning to a known area. It also seems that birds have emergency strategies for when things go wrong for example when landbirds are caught over the sea in bad weather, they might reverse direction and retrace the route or, if the wind is too strong to fly back, they may continue on the same heading or downwind until land appears. Migrants commonly experience wind drift during flight, and often compensate for this displacement at the time or during a later flight, showing that some course recording and correction is at work, whether or not they ‘know’ the coordinates of their migratory goal (Thorup & Rabøl, 2001). The fact that juvenile (as well as adult) birds can correct for drift may seem at odds with some of the displacement experiments discussed in Chapter 10, in which adults corrected for displacement and headed towards their former wintering areas, whereas juveniles continued on their usual direction and made no correction. However, displaced juveniles have never experienced a wintering area so may have no motivation to correct for displacement, even if they could. Also, drifted juveniles experience the drift and can see their surroundings, whereas artificially displaced birds travel in a vehicle or airplane and are unable to see the outside world. The method of lining up successive landscape features and flying from one to another is one obvious way of maintaining a consistent course in a crosswind, but this is little help over the sea where some birds can nevertheless maintain straight tracks in variable wind conditions (Horton et al., 2014). One of the most striking features of research on bird navigation is the diversity of results obtained, with contradictory findings coming from the same species in different experiments. Much of this divergence of findings can now be attributed to (1) birds using several different means of orientation, according to circumstances at the time; (2) such features as location, time of day, and prevailing weather, all influencing the way a bird reacts in a particular experiment; (3) the exact experimental protocol which can also have big effects on bird behaviour, as illustrated by results from cue-conflict experiments which depend on whether or not the bird can see the horizon in the test situation. These issues only emerge gradually, as researchers struggle to explain their differing findings.

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Other, as yet unappreciated, environmental cues could provide goal-orienting birds with some sort of map information. Suggested possibilities include some sort of inertial navigation system (which measures movements without reference to external cues), different components of the magnetic field, sun and stars, and use of the Coriolis force. These proposed mechanisms have so far found no support, and some would require levels of sensory perception well beyond those known in birds (Berthold, 1993).

Genetically encoded spatial information The apparent existence in birds of an inherent location response, though which individuals seek out and respond to specific localities (signposts), is a step beyond the ‘clock-and-compass’ concept, and could account for some previously unexplained findings: (1) the ability of many pelagic seabirds and others to return swiftly to their nesting colonies when artificially displaced for long distances into areas they are unlikely to have ever visited; (2) the ability of naive young birds on migration, as well as experienced adults, to correct for displacement to areas they could not have visited previously (for juvenile Common Cuckoos (Cuculus canorus), see Thorup et al., 2020); (3) the ability of juvenile birds (and adults) departing from a wide mainland area to reach small, isolated islands in large oceans, or to converge on narrow routes, as at short sea-crossings, before spreading out again (as shown by many soaring species (Chapter 7), Marsh Warblers (Acrocephalus palustris), Eleonora’s Falcons and others (Thorup & Rabøl, 2001; Gschweng et al., 2008)); (4) the ability of some birds to follow migration routes that deviate markedly from the most direct, sometimes with substantial detours differing between autumn and spring; (5) the ability of some birds, despite being buffeted by winds, to maintain remarkably straight and narrow routes on migration, even over an apparently featureless ocean (Horton et al., 2014); (6) many seabirds and other transoceanic migrants (eg Bar-tailed Godwits (Limosa lapponica)) clearly make adaptive use of winds, taking circuitous (longer and non-direct) routes to their wintering or breeding areas, yet seeming aware of their locations throughout; (7) seabirds nesting on opposite sides of an island such as Britain, although from the same gene pool, may start their migrations in opposite directions yet end up in the same general wintering area, as in Atlantic Puffins and others, adults and juveniles (Chapter 8). Individuals act as though they have personal GPS devices (Thorup & Holland, 2009). Birds are not unique in these respects, for innate navigational responses have been demonstrated in the juveniles of many marine animals (including turtles, eels and salmon), all of which apparently navigate to specific target areas using the earth’s magnetic field (Putman et al., 2011, 2014; Naisbett-Jones et al., 2017). Although we do not understand how such geographical goal areas could be genetically encoded, or whether they always involve magnetic parameters, we have to accept that such positioning systems exist in at least some birds and other animals.

SUMMARY Migratory birds have a number of orientation and navigation mechanisms available to them. As cues to compass directions, they can use celestial information (from the sun, skylight polarization and stars) or magnetic information (inclination and intensity of force lines, and possibly also declination). The sun compass must be adjusted to allow for time of day, so an important component of this mechanism is the bird’s internal time sense. Almost certainly, birds also use known landmarks to recognise previous travel routes and home areas, and perhaps also to help maintain a straight course or detect drift. Some birds also use odour gradients to find their way either locally or (in the case of some seabirds) over longer distances. Effective use of all known compasses employed by migratory birds must be learned and can be modified by experience, if necessary cross-checking them at points along a route. Birds seem to use whichever navigation mechanism is appropriate in prevailing conditions and may change during the course of a journey. The availability and reliability of different environmental compasses varies between regions, seasons and local conditions, so that for instance the sun compass cannot be used at night or if the sky is totally overcast, the star compass cannot be used during the day, or during high-latitude summers with round-the-clock daylight, and a magnetic compass based on the angle of inclination is unusable around the geomagnetic poles and the geomagnetic equator. Use of these compasses also requires (1) a time-compensating system for the sun compass, (2) an ability to relate star patterns to the celestial rotation for the star compass, and (3) sensory receptors capable of detecting the plane of polarized light and the alignment of the geomagnetic field. To avoid errors in orientation when switching between compasses, each of these systems must be calibrated with respect to a common reference system. For many birds, the primary calibration reference appears to be derived from celestial cues, including polarization patterns present at sunset and possibly also at sunrise. The pattern of stellar rotation may also be used to indicate geographical north in calibrating magnetic cues.

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Turning to navigation, detectable non-parallel gradients of two or more different map components would enable a bird to determine its current location and its direction to a target area. Such a map requires an animal to learn the alignment and, possibly, steepness of two or more environmental gradients within its familiar area, and to extrapolate these gradient(s) beyond. Then, by comparing the value of such a map component at an unfamiliar site with that of the home area the bird could interpret its position along a gradient in relation to home. Given experience, birds could determine latitude (or shifts in latitude) at any time, either through the height above the horizon of the sun at noon, the height of the centre of star rotation above the horizon or from magnetic parameters, all of which birds can apparently sense. In using celestial cues, long east west migrations present greater navigational problems than north south flights because they involve time shifts, as the birds pass through successive time zones, a problem greatest at the highest latitudes, where the longitude lines are closest together, requiring more rapid adjustment. Although in theory, birds might measure time shift (through use of a ‘double clock’), there is yet no evidence that they can do so, and nor is there any global celestial cue through which birds are definitely known to detect their longitudinal position. However, experiments have demonstrated the ability of birds to detect longitudinal displacements using magnetic cues, and more studies are needed to assess the use of magnetic declination by birds. The extent to which birds travel on rhumbline routes (on a constant direction throughout the journey) or on great circle routes (requiring continual changes of direction during the journey) is unresolved. Several lines of evidence imply that birds possess a location sense, enabling them to head towards specific localities, even juveniles on their first migrations. Such localities may be staging areas on migration where extra fattening or directional changes are needed or wintering areas where migration terminates.

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Finding the way: orientation and navigation Chapter | 11

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Part 2

The timing and control of migration

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Chapter 12

Annual cycles

Ringed plover (Charadrius hiaticula) incubating For everything there is a season, and a time for every purpose. Ecclesiastes 3: 1.

Migration has to fit around other major events in the annual cycle of birds, namely breeding and moult. Depending on the species, these three activities vary in their timing and duration, in the sequence in which they occur, and in the extent to which they overlap with one another (Newton, 2011). Most bird species have only one breeding period each year, during which they raise one or more broods, but some (mainly tropical) species have two separate breeding periods. Many species also have only one moulting period per year, but some have two or more; and most species migrate twice each year (to and from their breeding areas), while others move three or more times or only once per year (from one breeding area to another). How these variations are controlled in relation to external conditions is of special interest in migrants because these birds are exposed in each calendar year to conditions in more than one part of the world. In the annual cycles of birds, all three processes of breeding, moult and migration require extra food beyond that needed for daily maintenance, so is it ideal to separate these processes as much as possible. Breeding normally occurs when food for feeding young is most readily available, while moult and migration are fitted around breeding. Only by breeding successfully can individuals pass on their genes to future generations and populations can be maintained. Moults are necessary because over time feathers wear and degrade, reducing their aerodynamic and insulative functions. Extra food is needed partly for feather synthesis and partly to compensate for greater heat loss and reduced flight efficiency during the replacement period, the extra energy coming partly from a reduction in other activity at that time (Jenni & Winkler 2020b). Impairment of flying ability also raises the risk of predation. Similarly, migration serves to enhance the survival and reproductive prospects of the bird but also requires extra food to fuel the flights. Migration also involves risks from extreme weather, predation and other factors. In matters of timing, whether of breeding, moult or migration, it is helpful to distinguish between ultimate and proximate causal factors (Lack, 1954). Ultimate factors include those aspects of environment, such as seasonal fluctuations of food supply which influence the timing of various events through their effects on the survival and reproductive success of individuals. They thereby influence the optimal period for the bird to undertake particular activities, and through the action of natural selection, favour individuals that have annual cycles arranged in the most effective manner. Proximate factors are those such as daylength which birds can use as reliable cues to begin preparing for breeding, moult and migration at appropriate dates each year. The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00024-5 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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VARIATIONS IN ANNUAL CYCLES Most parts of the world are seasonal in terms of daylength, warmth or precipitation, and hence also in terms of biological productivity. At high latitudes, the favourable season is relatively short, lasting only about one-fourth of each year. Nutritionally, the most demanding event in the annual calendar of birds is reproduction, which as mentioned above, normally overlaps the season of most abundant food. Other events fit around this. Migration is timed so that birds are present on their breeding areas for long enough to rear young, taking advantage of the favourable season, but are absent for the unfavourable season when their survival there would be precarious and reproduction impossible. To breed successfully, birds must remain in a fixed locality, at least until their young are well-grown and mobile, which prevents their migrating then. Likewise, moulting birds have missing and part-grown flight feathers, which could hamper migration (Hedenstro¨m, 2004). For these reasons, migration is normally confined to particular parts of the annual cycle, and in most species is separated from breeding and moult (exceptions below). In species that do not breed until they are 2 or more years of age, immatures have more freedom than adults in the times they moult and migrate, and often do so at somewhat different times of year. Eight common sequences of annual cycle events among migratory birds reveal the various ways in which birds arrange their annual schedules (Figure 12.1). Comparing species, moult is much more variable in timing than breeding and migration, but moult still tends to occur at annual or other regular intervals. In general, residents and short-distance migrants moult in summer after breeding (residents more slowly, sequence 1), while long-distance migrants moult either in late summer in the breeding area (as in sequence 1), in autumn at a migratory staging area (sequence 2) or in winter quarters (sequence 3), depending on the population (Newton, 2008, 2009; Kiat et al., 2018; Jenni & Winkler, 2020a,b). In many other migratory species, the moult is split, occurring partly in one area and partly in another, separated by migration. It can be split between breeding and wintering areas (sequence 4), between breeding and staging areas (sequence 5), or between staging and wintering areas (sequence 6). Moult normally stops during migration so that the bird can fly with a full set of flight feathers, some old and others new. The bird resumes the second part of moult wherever it left off the first part (with few exceptions). In the last two of these patterns (sequences 5 and 6), a split moult is associated with a split migration, each part of migration involving separate periods of fat deposition. In other (mostly large) species, split moults are associated with breeding (as moult stops temporarily during chick feeding), or with periods of winter food shortage. But the story does not end here, for while most migratory species have a single moult, in some cases split into two bouts, other species have two separate moults, replacing the same feathers twice each year. One moult occurs either before or after autumn migration (the post-nuptial or pre-basic moult), and the other before or during spring migration (the pre-nuptial or pre-alternate moult) (sequences 7 and 8). In most twice-yearly moulting species, the autumn moult is complete and the spring moult is partial, involving the body feathers only (and sometimes a few tertial, secondary or tail feathers). However, in a small proportion of species that moult twice each year, such as the Wood Warbler (Phylloscopus sibilatrix), the autumn moult is partial and the spring moult complete, while in other species, such as the Willow Warbler (Phylloscopus trochilus) and Bobolink (Dolichonyx oryzivorus), both moults are complete, involving the replacement of both wing and body feathers. In some species with two moults per year, both plumages look the same, but in other species the males or both sexes don a special breeding plumage, more brightly coloured than the drab winter garb. Spring moults of body feathers into breeding plumage occur in many species of passerines, shorebirds and others, and usually overlap with spring migration. In many species of ducks, the pre-nuptial moult (mainly body feathers) follows a few weeks after the post-nuptial moult (complete), beginning in the sequence body wing body. In consequence, drakes are in dull ‘eclipse’ plumage for only 3 months, and in bright breeding plumage for the rest of the year (Cramp & Simmons, 1977; Bluhm, 1988). In association with this, many species of ducks form pairs while in winter quarters, whereas most other birds pair up in breeding areas. The above generalizations apply to small or medium-sized birds in which the moult occurs as a distinct event in the annual cycle, typically lasting 2 3 months (Table 12.1). In many such species, breeding, moult and migration each occupy short periods that can all be fitted within a year without overlap, and often with a quiescent period as well (Figure 12.1). During the latter, birds may not be breeding, moulting or migrating, but they may be recovering in body condition or building up immunity or some other non-obvious process. However, in some large birds, such as vultures and albatrosses, breeding and moult may take so long that they cannot both be fitted within a calendar year without overlapping and in some such species, moult may also overlap with migration, especially body moult which does not reduce flight efficiency (Stresemann & Stresemann, 1966).

Annual cycles Chapter | 12

Breeding

Breeding

Moult

Pre-breeding migration

1 Post-breeding migration

Pre-breeding migration

Post-breeding migration, phase 1

2 Moult

Quiescence Post-breeding migration, phase 2

Quiescence

Breeding

Breeding

Pre-breeding migration

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Post-breeding migration

Moult, phase 1 Pre-breeding migration

3

4 Post-breeding migration

Moult

Quiescence

Quiescence

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Moult, phase 2

Breeding Post-breeding migration, phase 1

Moult, phase 1 Pre-breeding migration and moult

5

Post-breeding migration, phase 1 Moult, phase 2

Quiescence

Pre-breeding migration and moult

Moult, phase 1

6

Post-breeding migration, phase 2

Quiescence

Moult, phase 2

Post-breeding migration, phase 2

Breeding

Breeding

Pre-breeding migration

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7

Pre-nuptial moult

8 Post-breeding migration

Quiescence

Post-breeding migration

Pre-breeding migration

Pre-nuptial moult

Post-nuptial moult Quiescence

FIGURE 12.1 Some variations in the annual cycles of birds. The quiescent period is when the bird is not breeding, moulting or migrating. (Continued)

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In some of the largest flying birds, such as vultures, condors and albatrosses, each moult cycle lasts more than a year but again may be arrested during difficult periods, such as chick-rearing. Otherwise, such birds appear to moult more or less continuously and may have two or more moult waves in the primary and secondary flight feathers at once (so-called serial moult, Stresemann & Stresemann, 1966). In contrast, some large aquatic birds, such as waterfowl and grebes, circumvent the problem of slow feather growth in a different way, by moulting all their flight feathers simultaneously and becoming temporarily flightless. The whole feather series is then replaced within the time taken to grow the longest primary (about 4 weeks in ducks, 6 weeks in geese). The extreme is shown by penguins which replace all their feathers wing and body simultaneously, while resting and fasting on land for the whole period. For a time, the old feathers remain attached to the new ones growing below, so that insulation is maintained throughout. Among birds as a whole, the main events of breeding, moult and migration vary greatly in the time they take. The breeding cycle can last from about 5 weeks in some small passerines to more than a year in large albatrosses (giving more than the 12-fold variation between species), a complete moult takes from about a month in some small passerines to 2 4 years in some large eagles and albatrosses (say, up to 48-fold variation), while in migrants, journey times can vary from less than 2 days per year to around 220 days (111-fold variation; Newton, 2008). The bigger figures for migration come from some pelagic seabirds, some of which seem to remain on the move for most of the time between successive breeding attempts.

Split migrations

L

Split migrations are especially common in shorebirds and passerines, some of which moult over several weeks at a staging site on route to winter quarters. Shorebird examples include some populations of Dunlin (Calidris alpina) and Purple Sandpiper (Calidris maritima). Passerine examples include the Lazuli Bunting (Passerina amoena) and Bullock’s Oriole (Icterus bullocki) of western North America, the Great Reed Warbler (Acrocephalus arundinacous) and Thrush-Nightingale (Luscinia luscinia) of Europe-Africa, and the Chestnut Bunting (Emberiza rutila) and Yellow-breasted Bunting (Emberiza aureola) of eastern Asia (Young, 1991; Stresemann & Stresemann, 1966; Jenni & Winkler, 2020a,b). Split migrations are also common in waterfowl, many of which first migrate to special sites where they moult, becoming flightless as they replace their large wing feathers, and only after completing wing moult moving on to wintering areas (Chapter 17). Songbirds which moult on staging sites in autumn tend to replace their feathers more rapidly than do other populations of the same or similar species which moult in their breeding or wintering areas. This may be because the chosen staging areas usually offer at that time exceptionally abundant food supplies. Western North American songbirds which migrate to moult in the late summer Mexican monsoon region have some of the fastest rates of feather growth recorded in Nearctic songbirds (de la Hera et al., 2012). In passerines and shorebirds, moult during the non-breeding season usually takes longer than the post-breeding moult in summer, which could be due to difficulties in getting enough food or, alternatively, to relaxed time constraints in completing the moult in non-breeding areas. Sequence 1. Examples: Common Chaffinch (Fringilla coelebs), Common Redpoll (Acanthis flammea), Thrush-Nightingale (Luscinia luscinia), Fieldfare (Turdus pilaris), Jack Snipe (Lymnocryptes minimus). Sequence 2. Examples: Lazuli Bunting (Passerina amoena), Great Reed Warbler (Acrocephalus arundinaceus), River Warbler (Locustella fluviatilis), Northern Lapwing (Vanellus vanellus), Green Sandpiper (Tringa ochropus), various ducks. Sequence 3: Examples: Common Rosefinch (Carpodacus erythrinus), Wood Warbler (Phylloscopus sibilatrix), Least Flycatcher (Empidonax minimus), Orchard Oriole (Icterus spurius), Barn Swallow (Hirundo rustica), Common Swift (Apus apus), Eurasian Whimbrel (Numenius phaeopus), and some shearwaters, terns and skuas that breed and winter in opposite hemispheres. Sequence 4: Examples: Yellow-bellied Flycatcher (Empidonax flaviventris), Barred Warbler (Curruca nisoria), Purple Martin (Progne subis), Alpine Swift (Apus melba), Scops Owl (Otus scops), Bee-eater (Merops apiaster), Red-necked Nightjar (Caprimulgus ruficollis), European Turtle Dove (Streptopelia turtur), Osprey (Pandion haliaetus), European Honey Buzzard (Pernis apivorus), Collared Pratincole (Glareola pratincola), Marsh Sandpiper (Tringa stagnatilis). Sequence 5: Examples: Kentish Plover (Charadrius alexandrinus), Spotted Redshank (Tringa erythropus), some individuals of Curlew Sandpiper (Calidris ferruginea), Red-necked Stint (Calidris ruficollis) and Solitary Sandpiper (Tringa solitaria). Sequence 6: Examples: Wilson’s Phalarope (Phalaropus tricolor), Spotted Sandpiper (Actitis macularia) and other populations of shorebirds. Sequence 7: Examples with two complete moults per year: Willow Warbler (P\hylloscopus trochilus), Bobolink (Dolichonyx oryzivorus), Sharp-tailed Sparrow (Ammospiza caudacuta); examples with one complete and one partial moult per year: Rose-breasted Grosbeak (Pheucticus ludovicianus), Melodious Warbler (Hippolais polyglotta). Sequence 8. Examples: Lanceolated Warbler (Locustella lanceolata) and some other Locustella warblers, Great Knot (Calidris tenuirostris), Curlew Sandpiper (Calidris ferruginea), Western Sandpiper (Calidris mauri). Details from Stresemann & Stresemann, 1966; Newton, 2009; Remisiewicz, 2011; Jenni & Winkler, 2020a,b).

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TABLE 12.1 Moult schedules of various warblers, shorebirds and raptors in relation to migration. Old World Warblers Moult in the breeding area before autumn migration

Dartford Warbler (Curruca undata), Subalpine Warbler (Curruca cantillans), Common Chiffchaff (Phylloscopus collybita)

Moult in the wintering area after autumn migration

Greenish Warbler (Phylloscopus trochiloides), Arctic Warbler (Phylloscopus borealis), Wood Warbler (Phylloscopus sibilatrix). Icterine Warbler (Hippolais icterina), Sedge Warbler (Acrocephalus schoenobaenus)

Moult in a staging area (or first wintering area) during a break in autumn migration. Split moult, partly in the breeding area before migration and partly in the wintering area after migration

Common Whitethroat (Curruca communis), Common Reed Warbler (Acrocephalus scirpaceus), Great Reed Warbler (Acrocephalus arundaceus), Grasshopper Warbler (Locustella naevia), Orphean Warbler Curruca hortensis

Two moults, the post-nuptial moult in the breeding area after breeding, and the prenuptial moult in the wintering area

Willow Warbler (Phylloscopus trochilis)

Two moults, post-nuptial and pre-nuptial, both mainly or entirely in the wintering area

Melodious Warbler (Hippolais polyglotta), Lanceolated Warbler (Locustella lanceolata) and some other Locustella species

Shorebirdsa Moult in the breeding area before autumn migration

Killdeer (Charadrius vociferous), Jack Snipe (Lymnocryptes minimus), some populations of Purple Sandpiper (Calidris maritima) and Dunlin (Calidris alpina)

Moult in the temperate wintering area after autumn migration

Some populations of European Golden Plover (Pluvialis apricaria) and Red Knot (Calidris canutus)

Moult in the tropical wintering area after autumn migration

Lesser Sand Plover (Charadrius mongolus), Great Knot (Calidris tenuirostris), Sanderling (Calidris alba), Curlew Sandpiper (Calidris ferruginea), Little Stint (Calidris minuta), Western Sandpiper (Calidris maura), Wood Sandpiper (Tringa glareola)

Moult in a staging area (or first wintering area) during a break in autumn migration

Green Sandpiper (Tringa ochropus), Northern Lapwing (Vanellus vanellus), some populations of Semipalmated Sandpiper (Calidris pusilla) and Dunlin (Calidris alpina), Wilson’s Phalarope (Phalaropus tricolor)

Split moult, partly in or near the breeding area and partly in the wintering area

Collared Pratincole (Glareola pratincola), Lesser Golden Plover (Pluvialis dominica), Black-tailed Godwit (Limosa limosa), Marsh Sandpiper (Tringa stagnatilis), Ruff (Calidris pugnax)

Split moult, partly in or near the breeding area and partly at a staging area on autumn migration

Kentish Plover (Charadrius alexandrinus), Spotted Redshank (Tringa erythropus), some Red-necked Stints (Calidris ruficollis), some Ruff (Philomachus pugnax) and some Snipe (Gallinago gallinago)

Split moult, partly on a staging area during autumn migration and partly in the wintering area after migration

Wilson’s Phalarope (Phalaropus tricolor), Spotted Sandpiper (Actitis macularia), some populations of Knot (Calidris canuta) and Dunlin (Calidris alpina)

Raptors Moult in the breeding area before autumn migration

Eurasian Sparrowhawk (Accipiter nisus), Common Kestrel (Falco tinnunculus), White-tailed Kite (Elanus leucurus), Sharp-shinned Hawk (Accipiter striatus), Common Black Hawk (Buteogallus anthracinus), Red-shouldered Hawk (Buteo lineatus), and other short-distance migrants

Split moult partly in the breeding area before autumn migration, and partly in the wintering area after migration

Eurasian Hobby (Falco subbuteo), European Honey Buzzard (Pernis apivorus), Mississippi Kite (Ictinia mississippiensis), Swainson’s Hawk (Buteo swainsoni), Osprey (Pandion haliaetus), Swallow-tailed Kite (Elanoides forficatus), and other long-distance migrants.

a In addition to a complete post-nuptial moult, almost all shorebirds have a partial pre-nuptial body moult, which starts in winter quarters, and in some species continues into spring migration. Source: From Cramp (1992), Cramp & Simmons (1983), Jenni & Winkler (2020a,b), Kjelle´n (1994).

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Other movements In addition to the main events in the annual cycle, some species perform other movements. In particular, many birds show a period of dispersal in late summer, after the young have become independent but before they migrate (postfledging dispersal in juveniles, and post-breeding dispersal in adults, Chapter 19). This dispersal is apparent in resident and migratory species, but especially in juveniles that fledge early in the season so have more time before they moult or migrate. Some authors have recognized this period of movement as a distinct event in the annual cycle (Noskov & Rymkevich, 2008), and migratory restlessness at this time has been recorded (Van Doren et al., 2017). It is mainly a period of re-distribution after breeding, leading individuals to find and concentrate in areas of abundant food, occurring in any direction but requiring no obvious preparation such as fat deposition. There are also so-called ‘escape movements’, when individuals suddenly leave an area when confronted by an unexpected loss of habitat or food supplies, as might be caused by flooding, freezing or prolonged drought. So-called ‘hard weather movements’ are in this category when birds may leave in response to sudden snowfall (Chapter 17).

Geographical and other variations within species Although the diversity of annual schedules is shown most strikingly in comparisons between species, variation also occurs between different geographical populations of the same species (Noskov et al., 1999; Newton, 2008; Jenni & Winkler, 2020b). In particular, with increasing latitude, the migrations of many species lengthen and take up more of the year, while the periods devoted to breeding and moult decline in association with the decreasing length of the favourable season. Some small species which raise 2 3 broods per year at lower latitudes might have time for only one brood at high latitudes, where they may also moult more rapidly. In the White-crowned Sparrow (Zonotrichia leucophrys), for example moult lasts about 83 days in California, reducing to about 47 days in Washington State; that is shortening by 2.6 days per degree of latitude over a latitudinal span of 14 degrees (Mewaldt & King, 1978). The extent of overlap between breeding and moult also increases with latitude (and altitude), further compressing the two processes into a shorter period, and both processes become more synchronized between individuals. Furthermore, in some species, populations breeding at lower latitudes moult in breeding areas, whereas those breeding at higher latitudes may postpone their moult for winter quarters. For example, European Barn Swallows (Hirundo rustica) in the southernmost breeding populations, which are resident or short-distance migrants, moult during June August after breeding; whereas those in the northernmost populations begin moulting in September October after they have migrated to distant wintering areas. At intermediate latitudes, varying proportions of individuals show a split moult, starting in breeding areas, arresting during migration, and resuming in winter quarters (Cramp, 1988). Other geographical variants in the timing and duration of moult occur in shorebird species, mainly in association with the latitudes of breeding and wintering and the resulting seasonal cycle of food availability (Cramp & Simmons, 1983; Serra, 2000; Underhill, 2003; Remisiewicz, 2011). After migration to Britain, Red Knots (Calidris canutus) and Ruddy Turnstones (Arenaria interpres) begin moulting their primaries at the end of July and take about 77 and 94 days, respectively to replace their primaries. But other populations of these species which migrate much further to the coasts of South Africa do not begin their moult until they reach there in September October, with the ensuing primary moult taking 95 days in Red Knots and 119 days in Ruddy Turnstones (Summers et al., 1989, 2010; Underhill, 2003). An important feature of moult is that it can be arrested in a way that a successful breeding attempt cannot. Within species, the position of the split can vary between populations, again according to regional variations in the seasonal cycle of food availability (Mead & Watmough, 1976; Swann & Baillie, 1979). In terms of control, it is as though the demands of breeding (and to some extent migration) can over-ride those of moult and slow or stop it when necessary (Wingfield & Farner, 1979; Hahn et al., 1992).

Relationship between moult and migration Whatever the annual sequence, moult is scheduled in most small and medium-sized bird species in such a way that no migrant has to fly with large gaps in its wings (Stresemann & Stresemann, 1966; Payne, 1972). The extent to which moult is completed before autumn departure may depend directly on the time available between the end of breeding and the start of migration (Berthold & Querner, 1982). While most passerines migrate only with fully grown flight feathers, late moulting individuals which are presumably under pressure to leave before conditions deteriorate start autumn migration before completing their moult (for Common Whitethroat (Sylvia communis), see Hall & Fransson, 2001; for Rose-breasted Grosbeak (Pheucticus ludovicianus), see Cannell et al., 1983). Among many bird species, the

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juveniles replace only their body plumage, and not their flight and tail feathers, before autumn migration. Again, juveniles often start migration before their body moult has finished, especially those moulting late in the season (for examples see Ginn & Melville, 1983).

Breeding seasons split by migration Unlike moult and migration, a breeding cycle from egg-laying to fledging cannot be split between two separated periods. However, some species with short breeding cycles are able to raise successive broods in widely separated areas in the same year, migrating between the different breeding areas. Examples include the Common Quail (Coturnix coturnis) in the grasslands and cereal fields North Africa and Europe, the Common Redpoll (Acanthis flammea) and Siskin (Spinus spinus) in the forests of northern Europe, the Red-billed Quelea (Quelea quelea) in African grasslands, and several species in western North America (Chapter 17; Rohwer et al., 2009). Split breeding seasons allow species that could raise only one brood per year in a given locality to become multi-brooded, provided they can raise young to independence within a relatively short period. Their intervening migrations are substantial, covering up to several hundred kilometres (Chapter 17).

Sex and age differences Comparing different species, breeding seems invariably to occur during the season of greatest food supplies, and the other events at less good times. But what happens to other events when breeding is omitted or curtailed: do they move into the period normally filled by breeding? The answer seems to be yes, as shown in the following examples. In species in which one sex alone raises the young, the other is free to get on with the rest of its life. In ducks, for example after eggs are laid, the females are responsible for incubation and chick care, while the males move on to moulting areas and eventually to wintering areas up to several weeks ahead of females. Similarly, in many shorebird species, the young are raised by one parent, leaving the other to proceed with migration and moult. In the Ruff (Calidris pugnax), females raise the young, allowing males to moult and migrate earlier. But in the Spotted Redshank (Tringa erythropus) and others, males raise the young, allowing females to migrate and moult earlier. In yet other species, such as Black-tailed Godwit (Limosa limosa) and Northern Lapwing (Vanellus vanellus), both sexes raise the young and both migrate and moult at about the same time. The repetition of these various patterns in different bird families re-emphasizes the link between parental care and the timing of migration and moult. Breeding delays these other processes. Similarly, in those species in which individuals do not breed until they are two or more years of age, the moult is brought forward into the period occupied by older birds by breeding. Examples occur among shorebirds, seabirds, herons or raptors. After the first migration to wintering areas, these birds usually do not return to breeding areas in their first summer, but stay there year-round; or if they do migrate they travel later than adults and return earlier, fitting both migrations within the optimal season, while older individuals of their species are breeding (Chapter 18). Non-breeding shorebirds also moult up to several weeks earlier and take longer than breeding adults. For example while adult Red Knots after breeding took about 71 days to moult on the Wadden Sea wintering area, immatures and non-breeders which over-summered in the area started moult 4 weeks earlier and spread it over 87 90 days (Dietz et al., 2013). These various patterns indicate that, without the constraints of breeding, immature individuals migrate and moult earlier in summer than older birds of their species which are still breeding at the time, postponing their moult and migration until later in the year. Other age-related differences are harder to explain. In some western North American songbirds, juveniles moult in breeding areas before migration, while adults postpone their moult until they reach staging or wintering areas (Rohwer & Manning, 1990; Butler et al., 2002). Some Common Starlings (Sturnus vulgaris) in northern Europe show the opposite pattern, as adults remain to moult in their breeding areas while juveniles migrate to moult at a staging area (Chapter 17).

Exceptions to general patterns Species which feed on the wing, such as terns and hirundines, commonly replace their flight feathers while on migration, at least where food is abundant (for Black Tern (Chlidonias niger), see Van der Winden, 2002). In some tern species, adults also feed their recently fledged young while on migration, giving overlap between these different activities. Some hirundines moult their feathers while breeding or while migrating through favourable terrain, but not when they

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have a long flight over sea or desert (Elkins & Etheridge, 1977; Cramp, 1988; Jenni & Winkler, 2020a). For example Northern Rough-winged Swallows (Stelgidopteryx serripennis) in eastern North America moult, while migrating south over land, but pause for about 2 months on the north side of the Gulf of Mexico, crossing when they have finished wing moult (Yuri & Rohwer, 1997). In addition, some auk species swim to their wintering areas; the young set off before they can fly, accompanied and fed by a parent on route. This behaviour facilitates overlap between breeding and migration but is possible only because the young develop their insulating body plumage and can swim from an early age, migrating through continuously suitable habitats. Because the adults stay with their young for several weeks and can escape their main predators (large gulls) by diving, they also moult on migration, shedding and replacing all their flight feathers simultaneously. Some species of auks, such as the Common Murre (or Guillemot) (Uria aalge), thus engage in breeding activity, moult and migration at the same time. Other exceptions to the main patterns can be found in the ornithological literature, while others are likely to emerge in the future.

Concluding comments on annual cycles The main message to emerge from studies of the annual cycles of birds concerns the variability between species in the sequence of different events through the year, their timing, duration and extent of overlap. This flexibility is manifest mostly by differences between species, but also between geographical populations of the same species, between sexes, and between immatures and breeding adults. The fact that moult and migration can be split into two periods, while some other process occurs in the interim, adds to the variation. In the simplest pattern, found in resident birds, the annual cycle consists of only two components, breeding and moult, while in others a quiescent period is added too. In the more complex annual cycles of migrants, up to seven different components occur in succession throughout the year (Figure 12.1, types 5 and 6). Inevitably, however, increase in the number of components in the annual cycle brings reduced flexibility in the timing of any one component (Wingfield, 2008). In general, large bird species take longer to breed and moult than small ones and show greater overlap between these activities. The timing of migration cannot have evolved independently of breeding and moult, only in association. Conflicting pressures operate in the timing of any event (Table 12.2), giving different optimal solutions in different circumstances, but with breeding generally talking precedence at the season of greatest food availability. In addition to the patterns described above, considerable variation in timing occurs within populations, an aspect discussed in the next chapter.

NON-ANNUAL CYCLES In some large birds, such as the Wandering Albatross (Diomedia exulans), pairs take more than 1 year to raise a chick to independence (Warham, 1990). These birds therefore breed every second year but at about the same time of year, so the annual environmental cycle still imposes its pattern. Moult overlaps with breeding and also lasts more than a year, but proceeds more rapidly in the gaps between breeding attempts. Four other albatross species are known to breed every second year, at least in parts of their range (Warham, 1990). In all these species, the colonies are occupied every year but the occupants change from one year to the next. Other birds living in non-seasonal tropical environments where conditions are nearly uniform throughout the year have cycles that last less than a year. They include seabirds whose populations breed every 6 months such as Greater Crested Terns (Sterna bergii) on Aldabra Atoll and White Terns (Gygis alba) on Christmas Island (Pacific), every 7 8 months such as White-tailed Tropicbirds (Phaethon lepturus) on Ascension Island and Aldabra Atoll, and Bridled Terns (Onychoprion anaethetus) on Aldabra Atoll, and every 9 10 months such as Sooty Terns (Oochoprion fuscata) on Ascension Island, Christmas Shearwaters (Puffinus nativitatis) on the Pitcairn Islands, and Audubon’s Shearwaters (Puffinus lherminieri) and Swallow-tailed Gulls (Creagrus furcatus) on the Galapagos Islands (references in Reynolds et al., 2014). The intervals between breeding attempts depend largely on the duration of the breeding cycle in different species, and away from the equator most of them breed at annual intervals. Breeding-moult cycles lasting less than a year also occur in some land-bird species in equatorial South America where, in a semi-arid area with erratic rainfall at 3 30’N, 8 out of 10 species bred year-round, but with the cycles of different individuals out of phase with one another (Miller, 1954). In the Rufous-collared Sparrow (Zonotrichia capensis), individuals took 6 months to complete a cycle of breeding and moult and again moved from one cycle to the next in swift succession (Miller, 1959). This species thereby accomplished two full cycles within each calendar year, but again at any one time different birds were at different stages. Outside equatorial regions, this same species has a single breeding period each year, which shortens with increasing latitude, as in other birds. Breeding moult cycles shorter than 1 year have been described in other species elsewhere (Newton, 2008), and other examples may emerge as more studies are done in equatorial regions.

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TABLE 12.2 Likely selection pressures and trade-offs influencing the timing of various events in the annual cycles of birds. Advantage

Disadvantage

Arrive early in breeding area

Obtain good nesting territory, an earlier start to breeding and more time for a repeat nest. Early chicks get a better start

Increased risk of adverse weather after arrival, loss of body condition or starvation

Arrive late in breeding area

Decreased risk of adverse weather, and hence loss of body condition and starvation after arrival

Relegation to poor territory, late start to breeding, and shorter breeding season.

Breed as soon as possible after arrival

Often better able to exploit the peak food supply. Fit in additional (or repeat) breeding attempts

Increased risk of adverse weather during first nesting attempt, with higher costs to parents, especially laying females

Curtail period of parental care

May allow adults time for further breeding attempt or earlier moult or migration

May jeopardise survival of young

Finish breeding early in favourable season

Moult at optimal time, with good quality feathers

Fewer nesting attempts within season, or shorter period of parental care

Finish breeding late in favourable season.

More nesting attempts within season, or longer period of parental care.

Moult overlapped with other activities or compressed to less suitable time, producing poorquality feathers

Moult in breeding area

Take advantage of summer food supply. Migrate with new feathers

May occupy time that could be used for extended parental care, or for raising an extra brood, or delay departure from breeding areas

Moult in wintering area

Allows longer breeding season in summering area; more time available for moult than in breeding areas, so requires less extra food per day

Adults must migrate with old worn feathers. Food may be scarcer than in summer, and winter movements could be hampered

Overlap between breeding and moult

Saves time in the favourable season

Increases the daily food needs, and could reduce fitness and feather quality of parents and young

Depart earlier in autumn

Avoid unseasonably cold weather; reach stopover sites before food depleted, and obtain best territories in winter quarters

Fail to make maximum use of the potential breeding moulting season

Depart later in autumn

Make maximum use of potential breeding- moulting season

Risk of cold weather and reduced food supplies, which may prevent departure or cause starvation. May be relegated to poor territory in winter quarters

Migrate in short flights with minimal fat deposition

Saves time spent on fattening before starting migration, reduces predation risk, and saves fuel transportation costs

Lengthens journey time. Suitable refuelling places may be far apart

Migrate in long flights with high fat deposition

Shortens journey time, and allows crossing of longdistance unfavourable areas

Long periods of fattening, with high predation risk, bringing high fuel transportation costs

DOMINO EFFECTS, CATCH-UPS AND DELAYS In any bird population, individuals which are late to arrive on their breeding areas are likely to breed later than others, and then to moult and migrate to wintering areas later, in a ‘domino effect’ (Piersma, 1987a,b). But birds cannot get progressively later year after year (or progressively earlier) without getting out of step with environmental conditions. They need to catch-up at some point and re-set their clocks. In theory, opportunities for catch-up could come at any stage in the annual cycle, but there are two stages when delayed individuals can most readily gain time. Firstly, birds that fail in their breeding can moult and migrate earlier than they otherwise would, catching up on any delay and getting ahead of birds that nest successfully. Secondly, any birds that, for whatever reason, arrive late in their wintering areas could catch up over winter, avoiding any delay in their departure dates in spring. This is perhaps most likely in species which experience a quiescent period in winter

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when for some weeks no moult or migration intervenes to cause further delay. As evidence of catch-up during this period, in many birds, the start of spring migration is spread over a much shorter period each year than is the start of autumn migration, itself influenced by the highly variable dates that birds in the same population finish breeding. This variation is reduced over winter so that all birds can start their spring migration at dates undistorted by earlier delays. The difference in spread between autumn and spring migration dates has long been evident from observations, and more recently also from tracking studies. As an extreme example, in one year 29 Hudsonian Godwits (Limosa haemastica), migrating from Alaska to Chile, arrived in their wintering sites over a period of 59 days but left in spring in as few as 7 days. One bird arrived in Chile 32 days after the average date, but in spring departed 2 days before the average date. Other studies revealed catch-ups during autumn or spring migration, as late birds spent less time on stopovers than earlier ones (Box 12.1). In a few species, however, no over-winter catch-up occurred, and individuals which migrated late from breeding areas also migrated late from wintering areas (for European Nightjar (Caprimulgus eurpaeus), see Norevik et al., 2017; for Red-eyed Vireo (Vireo olivaceous), see Callo et al., 2013). Possibly in these species, individuals were running on different annual schedules, some earlier than others. Another possibility is that, as both these species moult in winter quarters, this process may have been delayed by a late arrival, and in turn delayed the spring departure. The following findings have commonly been found in species studied by tracking individuals over months or more: (1) most of the variability in timing between individuals arose during the breeding season, as birds stopped breeding at different stages, according to whether they succeeded or failed, giving carry-overs to successive events in the annual cycle; (2) variation in timing then decreased in successive events through the year from post-breeding migration (most variable) in one year to the start of breeding in the next year (least variable); (3) the main reduction in variability was achieved by catch-ups over winter, but some also during autumn and spring migrations, mainly through reductions in the numbers and durations of stopovers (Box 12.1). Nevertheless, among tagged birds of many species, individuals that departed earliest on migration also arrived earliest, a trend that held in both autumn and spring, implying that in these species catch-ups were only partial (Figure 12.2; for Wood Thrush, see Stanley et al., 2012, for Bar-tailed Godwit, see

BOX 12.1 Examples of catch-ups during the annual cycles of birds from the same populations. Catch-ups over the period spent in the non-breeding area Evidence consists mainly of the greater spread in arrival dates in wintering areas compared with the spread in departure dates from wintering areas. Examples include Egyptian Vulture (Neophron percnopterus) (31 vs 11 days, N 5 6; Lo´pez-Lo´pez et al., 2014); Hudsonian Godwit (Limosa haemastica) (59 vs 7 days, N 5 29; Senner et al., 2014); Bar-tailed Godwit (Limosa lapponica) (55 vs 30 days, N 5 101,146; Conklin & Battley, 2012); Eurasian Whimbrel (Numenius phaeopus) (28 vs 14 days, N 5 56; Carneiro et al., 2019), Great Snipe (Gallinago media) (55 vs 25 days, N 5 19; Lindstro¨m et al., 2015); Common Sandpiper (Actitis hypoleucos) (20 vs 17 days, N 5 10; Summers et al., 2019), Peregrine (Falco peregrinus) (25 vs 18 days, N 5 20, 14; Sokolov et al., 2018). Exceptions to the above include the small proportion of species which moult just before their spring migration, and in which a late or slow moult can delay departure (for Mallard (Anas platyrhynchos), see Dugger, 1997; for Barn Swallow (Hirundo rustica), see Van den Brink et al., 2000). Other exceptions are species in which individuals from the same breeding area can winter over a wide span of latitude, and individuals with the furthest to travel on their return journey set off much earlier than others. Both these situations tend to increase the spread in spring departure dates in birds from the same breeding population. Catch-ups during the autumn migration period Evidence consists of the greater spread in departure dates of birds from breeding areas than the spread in their arrival dates in their wintering areas. This difference arises from later-departing individuals migrating faster, with fewer or shorter stopovers, than earlier-departing birds. Examples include Wood Thrush (Hylocichla mustelina) (Stutchbury et al., 2011; Stanley et al., 2012); Hoopoe (Upupa epops) (van Wijk et al., 2017, Barn Swallow (Hirundo rustica) (Imlay et al., 2021); Red Kite (Milvus milvus) (Maciorowski et al., 2019). Catch-ups during the spring migration period Evidence consists of the greater spread in departure dates of birds from wintering areas than the spread in their arrival dates in their breeding areas. This difference arises from later-departing individuals migrating faster, with fewer or shorter stopovers, or more direct (but riskier) routes than earlier-departing birds. Examples include Peregrine (Falco peregrinus) (Sokolov et al., 2018); Dunlin (Calidris alpina) (Warnock et al., 2004); Red-backed Shrike (Lanius cullurio) (Pedersen et al., 2016); Pied Flycatcher (Ficedula hypoleuca) (Ouwehand & Both, 2017); Wood Thrush (Hylocichla mustelina) (McKinnon et al., 2015); Barn Swallow (Hirundo rustica) (Pancerasa et al., 2022).

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FIGURE 12.2 Relationship between the departure dates of Wood Thrushes (Hylocichla mustelina) from Central American wintering areas and their arrival dates in Pennsylvanian breeding areas. In general, birds that were early to leave their wintering sites were also early to arrive in their breeding areas, the whole journey averaging 21 days. Based on 56 migration tracks of 45 different individuals. Modified from Stanley et al. (2012).

Breeding arrival date (Days from 1 Jan)

160 Male

150

239

Female

140

130

120

110 70

80 90 100 110 120 Spring departure date (Days from 1 Jan)

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Conklin et al., 2010; for Great Reed Warbler (Acrocephalus arundinaceus), see Lemke et al., 2013; for Western Kingbird (Tyrannus verticalis) see Jahn et al., 2013). Another way of reducing delays is to skip or overlap particular processes that are normally separated. Birds that arrive too late on their breeding areas may abandon nesting altogether that year (as in geese, Newton, 1977). Birds that breed late may start to moult while they are still feeding young (as in Eurasian Bullfinch (Pyrrhula pyrrhula) and European Greenfinch (Chloris chloris) Newton, 1966; Newton & Rothery, 2005), or birds that moult late may start migrating before they finish feather growth (as in Common Whitethroat (Curruca communis); Hall & Fransson, 2001). Similarly, Common Swifts (Apus apus) normally moult in their winter quarters, but when held up in Finnish breeding areas by bad weather they started moulting at the usual time in October when they would normally be in Africa (Kolunen & Peiponen, 1991). This implies the influence of an underlying intrinsic rhythm (discussed below), which allows some delay but limits each event to an appropriate season (its ‘time window’). It is clearly not necessary for a bird to complete one event in the annual cycle before it can start the next: birds that fail part way through a breeding cycle may then move on to moult and migration, albeit somewhat earlier than usual. Nevertheless, lateness or overlapping of events that are normally separated can have adverse consequences; for example overlap between breeding and moult can result in low-quality feathers, which are light in weight and often show ‘fault bars’ at which they can later break. This can result in reduced insulation and flight efficiency, with potential effects on survival and reproductive success. In the Slaty Brushfinch (Atlapetes schistaceus) in Andean forests, individuals overlapping breeding and moult produced lighter and shorter wing feathers than individuals that were moulting but not breeding. Moreover, individuals overlapping breeding and moult showed reduced flight speed during escape flights, implying greater vulnerability to predation (Echeverry-Galvis & Hau, 2013). The relationships between successive events in the annual cycle are explored further in Chapter 13.

INTERNAL TIME KEEPING While the main environmental (ultimate) factor controlling the annual cycles of birds is the seasonality of the environment, the main intrinsic (proximate) factor is an endogenous rhythm (internal clock) within the bird. This selfsustaining rhythm tends to ensure that the major processes of migration, breeding and moult occur in the correct sequence each year, and at roughly the right times. Such self-sustaining rhythms are presumed to have evolved over time to ensure that the different events are synchronized to seasonal changes in the bird’s environment. Migrations are frequently anticipatory in nature. Birds set off towards their breeding areas in expectation of conditions that will develop there later in the year, enabling them to raise young. They time egg-laying so that their young hatch when food suitable for feeding them is sufficiently available. The same birds leave their breeding areas before conditions deteriorate so much that they could no longer survive there, in advance of a worsening of conditions. To act by anticipation, many species rely largely on their endogenous clock, coupled with environmental information (eg daylengths), to trig˚ kesson & Helm, 2020). ger preparation for some predictable future event at an appropriate time (A Evidence for an internal rhythm has come largely from studies on captive birds kept for up to several years under rather specific constant daylengths (Gwinner, 1968, 1971, 1972, 1981, 1986; Berthold, 1984b; Berthold & Terrill, 1991;

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Helm, 2006; Helm et al., 2005, 2013; Karagicheva et al., 2016). Such birds have no clue from the outside world as to what the date might be. Yet they usually moult and reach breeding and migratory condition in the correct sequence, and at roughly appropriate intervals, with corresponding changes in body weights, gonad sizes and hormone levels. Such findings imply the existence of some underlying internal controlling system. However, in conditions of constant daylength, the cycles do not stick strictly to a year but tend to drift, getting either shorter or longer over time, hence the term ‘circannual’ cycles (from circa 5 about, annus 5 year), which typically last 9 14 months. In the real world, the natural cycle of daylength serves to keep this internal rhythm to an appropriate annual periodicity. The existence of internal circannual rhythms, underlying the natural yearly cycles, and persisting for at least two cycles, has now been shown experimentally in more than 20 different bird species, including resident and migratory, temperate and tropical, passerines and non-passerines, as well as in other animals and plants (Newton, 2008). Such intrinsic cycles evidently underlie the control of seasonal activities in a great variety of organisms. Among birds, Garden Warblers (Sylvia borin) and Eurasian Blackcaps (Sylvia atricapillus) kept under constant photoperiodic conditions (10 light:14 dark) have shown up to 10 successive moult cycles in eight calendar years, suggesting that, in these species, a circannual rhythm keeps running throughout the entire lifetime, requiring no obvious environmental stimulus. In such experiments, different birds housed in the same room got out of phase with one another, providing further evidence that the rhythms are endogenously controlled and can be expressed in the absence of environmental cues. Also, the fact that such cycles are shown by birds that have been hand-reared and kept under constant conditions from hatching further implies that they are innate and do not arise from early experience (Gwinner, 1981, 1996; Berthold, 1984b). The neural control centre of such cycles is unknown, but it almost certainly differs from that of the better-researched circadian (diurnal) rhythm, control of which lies within the medial basal hypothalamus (Ball & Balthazart, 2003). Under artificial constant daylengths, circannual cycles may be reflected in gonad condition alone, in moult alone, in migratory condition alone, or in any combination of these measures. The cycles can thus be viewed as consisting of separate but integrated components involving different activities (Wingfield, 2005). Which of these components are expressed in captive birds depends largely on the constant photoperiod to which the birds are exposed, and perhaps also on the time of year (5internal physiological state of the birds) when the experiment starts. In Common Starlings (Sturnus vulgaris), for example the range of constant photoperiods under which gonad size and moult are expressed is narrow, at about 11.5 12.5 hours (Schwab, 1971; Gwinner, 1996). Outside this range, no proper gonadal cycles occur (Dawson, 2007). It seems that photoperiods act as ‘permissive’ factors, setting limits to the expression of the different components of circannual rhythms; each component may occur only if the experimental photoperiod is close to the range of natural daylengths to which the bird is normally exposed for that component. In many species, long light periods tend to suppress gonad growth altogether, even when maintained for several years (Sansum & King, 1976; Wingfield & Silverin, 2002), but they seldom suppress moult and fattening. On specific experimental photoperiods, different activities can thus be eliminated from the annual cycle, separated or overlapped with other activities. Such findings are relatively rare and restricted to particular photoperiods, but they again suggest that the different components of the annual cycle are to some extent independent of one another and that the chosen photo-regime can affect the phase relations among them (King, 1972). In a study of Red Knots (Calidris canutus) kept under constant 12L:12D, pre-breeding components of the annual cycle (pre-migratory weight gain and adoption of breeding plumage) kept roughly to a periodicity of 1 year, while post-breeding components (including wing moult) got gradually later, giving cycles greater than 1 year (Karagicheva et al., 2016). Under natural conditions, as mentioned above, the different components of the annual cycle are normally kept in phase with one another by external influences, notably the natural daylength cycle. Spontaneous endogenous rhythms are most apparent in long-distance migrants, which are normally exposed to varying photoperiodic regimes on migration, and in which the need for some form of endogenous control is greatest (as appreciated long ago by Rowan, 1926). They are also apparent in some resident species of equatorial regions, where daylengths are constant year-round. For example, equatorial African Stonechats (Saxicola torquata axillaris) kept caged in constant 11.8L:11.2D conditions in Germany went through up to 12 reproductive-moult cycles in a 10-year period (Gwinner, 1996). However, in temperate zone residents and short-distance migrants caged in constant conditions, the cycles tend to continue for less long and are more variable among individuals. They seldom proceed for more than 1 year, and the different events tend to become increasingly out of phase with one another, as found in some populations of Eurasian Blackcaps (Sylvia atricapilla) (Berthold et al., 1972) and in European (as opposed to African) Stonechats (Saxicola torquata) (Gwinner, 1996). It is also clear that different species or geographical populations react differently to the same constant daylength regime, presumably reflecting their adaptations to different daylength regimes in natural conditions. For example birds from three different races of Stonechats from Kazakstan, Western Europe and tropical Africa kept on identical

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constant photoperiod conditions, showed different endogenous cycles, appropriate to their different home areas. The races differed chiefly in the time afforded to different activities, notably their ‘reproductive windows’, but also their moult timing and pre-migratory preparations (Helm et al., 2005). Similarly, seasonal changes in body mass and nocturnal restlessness were compared between Northern Wheatears (Oenanthe oenanthe) from three populations, breeding in Iceland, Norway and Morocco, respectively, and all kept under the same constant photoperiod during their first year of life (Maggini & Bairlein, 2010). Birds from the three populations differed in the timing and intensity of nocturnal restlessness during autumn in line with the distance they would normally travel, and the Icelandic birds also showed a greater increase in body mass, in line with their long initial sea crossing. The evolution of regional responses of this type clearly depends on ‘site fidelity’, behaviour in which individuals and their offspring remain in, or return to, the same general areas to breed each year (Chapter 19). Only then can populations evolve specific regionally appropriate responses.

Importance of daylength Under natural conditions, as indicated above, the endogenous cycles of many birds are kept to time by seasonal daylength changes, and in experimental conditions particular events can be advanced or delayed by appropriate use of an electric light (Farner & Follett, 1966; Lofts & Murton, 1968; Wolfson, 1970; Dawson et al., 2001). For example if migratory birds of some species are exposed in late winter to photoperiods longer than natural days, their sex organs begin to grow earlier than usual, and they show migratory and reproductive behaviour prematurely (Rowan, 1925, 1926; Wolfson, 1970; Lofts et al., 1963; Ramenofsky et al., 2012). The importance of daylength as a time-keeper (Zeitgeber) derives from its reliability. At any given location, its seasonal changes are consistent from year to year, making it the most obvious environmental feature that, at most latitudes, gives a reliable cue to date. The synchronization of the internal annual cycle to photoperiod has been shown most convincingly in experiments in which birds were exposed to seasonal photoperiodic cycles with periods deviating from 12 months (eg 6-month cycles). As a rule, the birds’ biological rhythms then conformed to the altered photoperiodic regime (Gwinner, 1986, 1990). For example when the normal annual cycle of daylength was compressed to 6 months without altering its amplitude, Garden Warblers (Sylvia borin) went through four instead of two moult periods within one calendar year, two instead of one gonad cycle, and four instead of two periods of migratory restlessness (Berthold, 1996). The same occurred in Sardinian Warblers (Curruca melanocephalus), in which the usual single annual moult occurred twice within one calendar year (6 months apart). It also occurred in Stonechats (Saxicola torquata), which underwent two gonad and moult cycles in one calendar year (Gwinner & Helm, 2003). More remarkably, Dark-eyed Juncos (Junco hyemalis), which were exposed to four periods of short (9-hour) days and five periods of long (20-hour) days in 1 year, showed in this time five periods of gonadal activity, five of fat deposition and two of moult (Wolfson, 1954). By compressing the normal annual photoperiodic cycle into 2 months, Common Starlings (Sturnus vulgaris) showed up to six gonadal cycles in one calendar year, but on this extreme regime the testes did not fluctuate over the full range and moult was disturbed and incomplete (Gwinner, 1996). A second line of evidence for the role of the daylength as a time-keeper involves birds from the northern hemisphere which were introduced into the southern hemisphere. Such birds normally adjusted to the local daylength regime within a year or so of their release. Their annual cycles remained essentially unaltered, except that they were 6 months out of phase with those in their original home (Aschoff, 1955). This finding has been duplicated in many phase-shifting experiments on various captive birds (Gwinner, 1986). It has also been studied in Barn Swallows (Hirundo rustica) from North America which around 1980 began to breed within their traditional wintering range in southern South America (Winkler et al., 2017). Apart from the 6-month inversion of their annual cycles, these birds did not migrate as far as their ancestors but shortened their journey to winter in northern South America (as shown by the use of geolocators). By 2015, much the same had happened in American Cliff Swallows (Petrochelidon pyrrhonota) which began to nest in their former wintering area in Argentina, again also changing appropriately the timing of other events in their annual cycles (Areta et al., 2021). Something similar presumably happened in several north Eurasian species which began naturally to breed in their traditional wintering areas in southern Africa and are now well established there (Newton, 2003; Randall, 2013; Helm & Muheim, 2021). While daylength in specific localities changes in a consistent manner from year to year, the weather, food supplies or other conditions at particular dates vary considerably. It is therefore advantageous for wild birds to be able to respond, not only to daylength but also to other secondary factors, and modify their activities to suit conditions at the time. Plant growth and invertebrate activity begin much later in cold springs than in warm ones, and any bird that did not respond appropriately to this variation could be seriously disadvantaged. Secondary environmental factors may thus

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fine-tune the timing of various events to prevailing conditions: for example enabling the bird to arrive on its breeding area and start nesting at what is an ecologically suitable time that year (Lack, 1954; Wingfield et al., 1993). In general, the effect of daylength (interacting with an endogenous rhythm) could be said to initiate the preparatory processes that precede each event. Then, as development proceeds, other modifying factors, such as food supply, mate behaviour and nest-site availability, come to play a greater role (for examples of food effects, see Newton, 1998; for mate and social influences, see Lewis & Orcutt, 1971; for nest sites, see Village, 1990). Daylength has another useful property that is almost certainly used by birds, namely that its annual cycle varies in a consistent manner with latitude. This provides a means by which migrants from the same population could identify their latitudinal position with respect to breeding or wintering areas, enabling them to time their migrations in an appropriate manner from different latitudes within the breeding or wintering range. More generally, daylength provides a basis for selection to encode the seasonal behaviour of populations to latitudinal conditions, a facility particularly evident in migratory populations (Chapter 13). Daylength is not the perfect time keeper worldwide. On the equator, it is constant at 12 hours year-round. And in the high arctic, daylight continues over several weeks each summer. Events which begin during this period of constant light, such as post-nuptial moult, are assumed to begin under the control of the endogenous rhythm (Noskov et al., 1999). However, all the birds breeding in the high arctic experience periods of night-time darkness during the rest of the year, either within the arctic or at lower latitudes in their migration and wintering areas. These patterns could help to keep their endogenous cycles on appropriate annual schedules.

Endogenous rhythms in migrants Migratory birds that breed at high latitudes and winter in regions close to and beyond the equator face two particular problems in the control of their annual cycles. First, birds that winter near the equator can spend half of each year under constant daylengths. Hence, in contrast to other species, such birds cannot rely on changes in daylength for timing those seasonal activities that occur in their wintering areas, notably spring fattening, pre-nuptial moult and departure for breeding areas. Second, unlike birds that remain in the same hemisphere year-round, long-distance migrants that cross the equator are exposed to relatively long days in both summer and ‘winter’ (5austral summer). They breed during the long days of the boreal summer, but not in the long days of the austral summer, even though conditions in their austral ‘wintering’ areas may be similar to those that stimulate reproduction in their northern breeding areas. These facts raise questions in such long-distance migrants on what prevents reproduction in wintering areas yet stimulates pre-nuptial moult, migratory fattening and departure at appropriate dates. Again, the evidence suggests the intervention of an endogenous time-keeper, causing the bird to react to particular conditions in different ways, or not at all, at different stages of its circannual cycle. This time-dependence can be shown systematically by plotting the response of a bird to a particular stimulus over the whole of an annual cycle. Typically, a response may come only in one or two parts of the ˚ kesson & Helm, 2020). cycle (A In resident birds of higher latitudes, present in the same locality year-round, control of the annual cycle by an endogenous rhythm, kept to time by daylength changes, would seem relatively straightforward, because at any one locality, daylength varies in a consistent fashion from year to year, providing a reliable indication of date. In fact, in this situation, an endogenous circannual rhythm might seem unnecessary. In long-distance migrants, however, the situation is more complicated because, within the space of a few days, birds can pass rapidly from one daylength regime to another. One way to cope with such problems is to restrict the period of response to daylength to only part of the year, using that period for ‘clock-setting’, and then allowing the internal rhythm to run for a period, regardless of external daylength. The proven existence of a ‘refractory period’, when birds do not respond by gonad growth to otherwise stimulatory daylengths, is consistent with such a mechanism, as is the finding that long-distance migrants (exposed to the most rapid and complex changes in daylengths) rely more heavily on a self-sustaining internal rhythm than do short-distance migrants and residents (Gwinner, 1972). The critical photoperiod for the ending of photo-refractoriness, which prevents the gonads of migrants from developing in the austral summer, is related to the photoperiodic conditions of the ‘wintering’ areas (Gwinner & Helm, 2003). Not surprisingly, endogenous factors seem to have more influence on the timing of various events in species that migrate to the tropics and beyond than in species that migrate short distances within the northern continents (Gwinner, 1972; Hagan et al., 1991). Thus long-distance migratory Willow Warblers (Phylloscopus trochilus) displayed in experimental conditions a firm endogenous control over migratory restlessness, with changes in body weight and moult persisting for more than 2 years in a constant 12-hour photoperiod (L12:D12). In contrast, the closely related but shortdistance migratory Common Chiffchaffs (Phylloscopus collybita), which winter in temperate and Mediterranean zones,

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lost any endogenous control of these activities within a year, so that body weight became almost constant, and migratory restlessness and moult became irregular or ceased (Gwinner, 1971, 1972). Kept under natural daylengths, Willow Warblers moulted earlier and more rapidly than Common Chiffchaffs; they prepared for migration earlier and showed more fattening and restlessness. Most of these differences persisted when birds were kept under constant daylengths, indicating some degree of endogenous control. The same was found for different races of African Stonechats (Saxicola torquata) kept in the same, constant conditions (Helm et al., 2009). Endogenous control mechanisms have presumably been fine-tuned under the action of natural selection on ancestral generations. As evidence for genetic influence on annual cycles, first-generation hybrids kept under natural daylengths have shown patterns of migratory timing and fat deposition that are intermediate between those of their parents (for waterfowl, see Murton & Westwood, 1977; for Sylvia warblers, see Berthold, 1984a, 1990, 1996; Pulido & Berthold, 2003; for Phoenicurus redstarts, see Berthold, 1990; for Stonechats (Saxicola torquata), see Helm et al., 2009). Other evidence of genetic influence comes from heritability studies based on parent offspring comparisons (for breeding dates, see van Noordwijk et al., 1981; for moult, see Larsson, 1996; for migration dates, see Møller, 2001; Pulido et al., 2001; Pulido & Berthold, 2003, Chapter 22). Yet further evidence comes from the changes that have occurred in wild birds in response to particular selection pressures (for laying dates of Great Tit (Parus major), see Visser et al., 1998; for spring migration dates of American Cliff Swallow, see Brown & Brown, 2000).

Geographical variation in photoperiodic responses With increasing latitude, the annual warm season becomes progressively shorter, starting later and ending earlier, while the cold season becomes longer. Correspondingly, most migratory bird species arrive later in spring, often breed over a shorter period, and leave earlier in autumn at higher latitudes than at lower ones (Chapter 15). Yet in the northern hemisphere, birds from the north of the range do not start breeding when they pass through the southern parts, at a time when individuals that breed in those areas have already started nesting. Nor do southern birds continue migrating northwards with others of their species once they have reached their own particular breeding areas. The implication is that birds nesting at different latitudes have different inherent responses to daylengths, thereby adjusting their annual activity cycles to the latitude at which they breed. This view is amply confirmed by experiments involving the manipulation of photoperiods (for Dark-eyed Junco (Junco hyemalis oreganus), see Wolfson, 1942; Singh et al., 2021; for rosy-finches Leucosticte, see King & Wales, 1965; for Common Chaffinch (Fringilla coelebs), see Dolnik, 1963; for Willow Warbler (Phylloscopus trochilus), see Gwinner, 1972; for waterfowl, see Murton & Westwood, 1977; for Ficedula flycatchers, see Gwinner, 1990; for Great Tit (Parus major), see Silverin et al., 1993; for African Stonechat (Saxicola torquata), see Helm et al., 2009). In general, populations breeding at higher latitudes require longer daylengths before gonad maturation occurs; but their gonads may then remain active for a shorter period than in birds that breed at lower latitudes. Birds could adjust their response to different latitudes, under the action of natural selection, in at least three different ways. First, they could alter their rate of response to the same daylength stimulus. Second, they could alter the length of a latent (refractory) period, before a response became possible. Third, they could alter their photosensitive threshold, so that they needed a shorter or longer daylength (or different number of days with daylength above a minimum value) to trigger a response (Wolfson, 1959; Marshall, 1960; Murton & Westwood, 1977). Which of these mechanisms birds use as they extend their breeding ranges into lower or higher latitudes is still uncertain. In addition, different species or populations living together in the same area show differences in photosensitivity that correspond to differences in the timing of events in their respective annual cycles (for different species of pigeons, see Lofts et al., 1967; for passerines, see Singh et al., 2021).

Equatorial birds Birds that live year-round near the equator experience more or less constant daylengths throughout their lives. Some live in relatively aseasonal habitats, such as rainforest, whereas others live in open country, where seasonal rainfall causes seasonal fluctuations in food supplies. In these latter species, the regular wet dry seasons and associated food changes may act as external time-keepers. Nevertheless, some equatorial and desert birds show endogenous circannual cycles when kept in constant conditions in captivity (Gwinner & Helm, 2003) and can also respond to photoperiodic changes (Lofts, 1964; Gwinner & Scheuerlein, 1999; Bentley et al., 2000). In Panama at 9 N, the Spotted Antbird (Hylophylax naevoides) experiences daylengths that vary only between 12 and 13 hours, from December to June. Yet in experimental conditions, individuals responded by song to an increase in photoperiod of only 17 minutes, and by gonad growth to an increase of 28 minutes (Hau et al., 1998).

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Daytime light intensity, rather than duration, could act as a time-keeper for some equatorial birds. It changes greatly with cloud cover and hence reflects the cycle of dry and wet seasons in relation to which many tropical birds breed. The experimental exposure of African Stonechats (Saxicola torquata) to a constant 12.25-hour photoperiod, but with cyclic changes in daytime light intensity, caused their gonadal and moult rhythms to become synchronized with the cycles of light intensity (Gwinner & Helm, 2003). Control birds exposed to the same photoperiod, but to a constant high light intensity, were not synchronized and showed variable responses. These results suggest a role for daytime light intensity as a circannual timing mechanism and also provide a possible explanation for the strong responsiveness of African Stonechats to photoperiodic change: light intensity and daylength may act synergistically on one and the same mechanism. However, a later study concluded that African Stonechats (Saxicola torquata axillaris) could probably respond to the slight changes in timing of sunrise and sunset that occur on the equator, despite the constant year-round daylength (Goymann et al., 2012). Sunrise and sunset times also emerged as a likely cue stimulating the twice-yearly egg-laying in Stripe-breasted Tits (Meliniparus fasciiventer) in equatorial Uganda (Shaw, 2017).

FLEXIBLE CYCLES Most birds breed regularly at the same times each year, but others breed at varying times depending on food supplies, with knock-on effects on the timing of moult and movements. Given sufficient food, at least three patterns have been recorded. The first involves a substantial extension of the normal breeding season, as found in Galapagos finches and others (Gibbs & Grant, 1987). The second involves a main breeding season in spring and an additional one in autumn, separated by moult, gonad regression and re-growth, as noted in the Tricolored Blackbird (Agelaius tricolor), Pinyon Jay (Gymnorhinus cyanocephalus) and others (Payne, 1969; Ligon, 1971). The third involves breeding in different months in different years, whenever food is sufficiently plentiful, often depending on irregular rainfall which promotes the growth of fresh vegetation and invertebrate activity on which bird breeding depends (Chapter 17). The same species may breed in different months in different years, sometimes at more than annual intervals and sometimes less, depending on when it rains. The timing of moult seems to be more regular, but when rain falls, moult is arrested and breeding starts. In the central Australian desert, for example rain is unpredictable, and at particular localities can fall at widely different dates each year. Some desert birds apparently remain ready to breed for much of the year, but nest only when stimulated by fresh rainfall or the resulting surge in green vegetation or food supplies (eg Serventy, 1971; Zann et al., 1995; Leitner et al., 2003; Voigt et al., 2007). They include not only landbirds, such as the Zebra Finch which can breed for more than 10 consecutive months if conditions remain suitable (Zann et al., 1995), but also various waterbirds which move rapidly into areas where rain has fallen. They breed in the resulting shallow lakes and move on again when the lakes dry out (Frith, 1967; Chapter 17). Such birds have a long ‘reproductive window’, but nest only at times within this period when conditions are suitable. In contrast to breeding, moult in these desert birds occurs on a more fixed schedule, but if rain falls unexpectedly, moult may or may not be suspended as breeding begins (for Galapagos Finches, see Snow, 1966; for Budgerigar (Melopsittacus undulatus), see Wyndham, 1982; for Zebra Finch, see Zann et al., 1995). In birds that breed in response to rainfall, it is uncertain what actually triggers breeding an increase in food supplies or the sudden appearance of green vegetation, as shown by experiments (Marshall & Disney, 1957; Voigt et al., 2011). A similar opportunist strategy is seen in Red (Common) Crossbills (Loxia curvirostra) in boreal regions. These birds depend on conifers, but the seeds of different species become available at different times of year. Seed abundance also varies greatly from year to year, so crossbills face both temporal and spatial unpredictability in food sources (Chapter 20). They can breed over much of the year, but most nesting occurs sometime between September and May, depending on local seed supplies (Newton, 1972; Berthold & Gwinner, 1978; Benkman, 1987). Correspondingly, the testes of male Red Crossbills can be active over a long period from late autumn to the following summer (Berthold & Gwinner, 1978). This allows the birds to breed in late summer or autumn, soon after they have found new areas of ripening cones, or in the winter and following spring. Juveniles may be fertile only a few weeks or months after fledging and can start breeding while still in juvenile plumage (Berthold & Gwinner, 1978; Hahn et al., 1997). Yet despite this variable breeding season, and associated movement patterns, the single annual moult occurs consistently in July September, sometimes overlapping with breeding, at least at the population level (Newton, 1972; Hahn, 1998). Experiments have shown that Red Crossbills and some other opportunist breeders can respond to photoperiod (Hahn, 1998), even tropical ones which under natural conditions experience little or no daylength variation (for Red-billed Quelea (Quelea quelea), see Lofts, 1964).

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To judge from these various findings, both regular (seasonal) and opportunistic (aseasonal) breeders depend partly on an endogenous rhythm, and both can respond to photoperiod in captivity. However, opportunist breeders have longer ‘reproductive windows’ and respond more strongly to prevailing ecological cues (notably food supplies) to fine-tune the timing of their nesting and movements (Wingfield, 1980; Hahn et al., 1997). Some opportunist breeders can delay or arrest moult or movement to breed if food happens to be plentiful at the time when moult and movement would normally occur. Many northern birds also show great flexibility in the timing and extent of their movements, which vary from year to year in relation to food availability (so-called irruptive migrants, Chapters 20, 21).

SUMMARY Depending largely on the environments in which they live, bird populations show great variation in the timing and sequence of the major events in their annual cycles. In most species, for nutritional and other reasons, migration, breeding and moult occur at different times of year, but in the same sequence every year. In some species, wing moult overlaps extensively with breeding, but in general, neither process overlaps with migration, although exceptions occur. In many migratory species, the autumn (post-breeding) migration and moult are split into two or more stages, with each stage of moult occurring in a different area. Some species can even breed in more than one area during the course of a year, migrating up to several hundred kilometres between areas. Such variations are apparent not only between species but also between different populations of the same species, depending on the locations of their breeding and wintering areas and the intervening distances. In terms of positioning within the annual cycle, breeding normally takes precedence, occurring at the best time of year, but when breeding is curtailed or omitted, post-breeding moult and migration move forward by up to several weeks into the period otherwise taken by breeding. Of all major processes, moult is most variable between species and populations in its positioning within the annual cycle. The main ultimate factor governing the annual cycles of birds is apparently the seasonality of the environments in which they live and the associated changes in food supplies. The main proximate controlling factor is an endogenous rhythm within the bird, which is kept to time by seasonal changes in daylengths. This self-sustaining rhythm is revealed in captive birds kept for years on constant photoperiods. Such birds may depart from the usual annual periodicity, but typically show repeated periods of gonad activity, moult or migratory restlessness and fattening, depending on the photoperiod under which they are kept. In general, under artificially constant conditions, endogenous cycles continue for longer in tropical species and in long-distance migrants than in temperate zone residents or short-distance migrants. Species that breed and winter in opposite hemispheres, and experience long days in both summer and ‘winter’, apparently rely on this internal rhythm to suppress reproduction in winter quarters. Those that winter there or in equatorial latitudes (where daylengths are constant year-round) probably rely largely on the internal rhythm to prevent homeward migration until an appropriate date in spring. At particular latitudes (away from the equator), daylength alters in a consistent manner from year to year and therefore gives a reliable indication of date. Evidence that birds respond to daylengths (through adjustment of the internal rhythm) comes from several findings. First, gonad growth, moult or migratory activity can be advanced or delayed by experimental exposure to longer or shorter photoperiods. Second, birds can be made to undertake more than one ‘annual’ cycle in a calendar year by alternating periods of exposure to long and short photoperiods. And third, birds adjust their annual cycles when transported to the opposite hemisphere, becoming about 6 months out of phase with conspecifics in the original home area (a finding replicated in photoperiod experiments on captive birds). Birds also respond to secondary stimuli, such as temperature, food supply or social conditions, to fine-tune the timing of various events to conditions at the time, and can delay or delete particular processes as the need arises. Different populations have different inherent cycles, and respond differently to the same daylength regime so that their annual cycles are adjusted to their particular needs. Captive-bred hybrids behave intermediately between their two parents, implying genetic control of the endogenous timing and response mechanisms. Similarly, within species, birds breeding or wintering at different latitudes respond to the prevailing daylength regime in such a way as to reach breeding, moulting or migratory condition at times appropriate to the latitudes concerned. The combination of an endogenous rhythm as a template for seasonal activity, together with daylength as a synchronizer, provides many birds with a basis for seasonal timing that operates well under variable seasonal conditions and movement patterns. This dual system gives reliability, precision and flexibility, enabling preparation for each event in good time, and promoting the slowing or speeding of each process as conditions dictate.

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Noskov, G. A. & Rymkevich, T. A. (2008). The migratory activity in the annual cycle of birds and its forms. Zool. Zh. 87: 446 57. Noskov, G. A., Rymkevich, T. A. & Iovchenko, N. P. (1999). Intraspecific variation of moult: adaptive significance and ways of realisation. Proc. Int. Ornithol. Congr. 22: 544 63. Ouwehand, J. & Both, C. (2017). African departure rather than migration speed determines variation in spring arrival in Pied Flycatchers. J. Anim. Ecol. 86: 88 97. Pancerasa, M., Ambrosini, R., Pomano, A., Rubolini, D., Winkler, D. W. & Casagrandi, R. (2022). Across the deserts and sea: inter-individual variation in migration routes of south-central European Barn Swallows (Hirundo rustica). Movement Ecol 10: 51. Payne, R. B. (1969). Breeding seasons and reproductive physiology of Tricolored Blackbirds and Red-winged Blackbirds. Univ. Calif. Publ. Zool. 90: 1 115. Payne, R. B. (1972). Mechanisms and control of molt. Pp. 103 55 in Avian biology (eds D. S. Farner, J. R. King, & K. C. Parkes). New York, Academic Press. Pedersen, L., Fraser, K. C., Kyser, T. K. & Tøttrup, A. P. (2016). Combining direct and indirect tracking techniques to assess the impact of sub-Saharan conditions on cross-continental songbird migration. J. Ornith. 157: 1037 47. Piersma, T. (1987a). Hop, skip or jump? Constraints in migration of arctic waders by feeding, fattening and flight speed. Limosa 60: 185 94. Piersma, T. (1987b). Population turnover in groups of wing moulting waterbirds: the use of a natural marker in Great crested Grebes. Wildfowl 38: 37 45. Pulido, F. & Berthold, P. (2003). Quantitative genetic analyses of migratory behaviour. Pp. 53 77 in Avian migration (eds P. Berthold, E. Gwinner, & E. Sonnenschein). Berlin, Springer-Verlag. Pulido, F., Berthold, P., Mohr, G. & Querner, U. (2001). Heritability of the timing of autumn migration in a natural bird population. Proc. R. Soc. Lond. B 268: 953 9. Ramenofsky, M., Cornelius, J. M. & Helm, B. (2012). Physiological and behavioural responses of migrants to environmental cues. J. Ornithol. 153: 181 91. Randall, R. M. (2013). House Martins make a home. African Birdlife 1: 58 9. Remisiewicz, M. (2011). The flexibility of primary moult in relation to migration in Palaearctic waders an overview. Wader Study Group Bull 118: 163 74. Reynolds, S. J., Martin, G. R., Dawson, A., Wearn, C. P. & Hughes, B. J. (2014). The sub-annual breeding cycle of a tropical seabird. PLOS ONE 9: e93582. Rohwer, S., Hobson, K. A. & Rohwer, V. G. (2009). Migratory double breeding in Neotropical migrant birds. Proc. Natl. Acad. Sci. U.S.A. 106: 119050 5. Rohwer, S. & Manning, J. (1990). Differences in timing and number of moults for Baltimore and Bullock’s Orioles: implications to hybrid fitness and theories of delayed plumage maturation. Condor 92: 125 40. Rowan, W. (1925). Relation of light to bird migration and development of changes. Nature 115: 494 5. Rowan, W. (1926). On photoperiodism, reproductive periodicity, and the annual migrations of birds and certain fishes. Proc. Boston Soc. Nat. Hist. 38: 147 89.

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Sansum, E. L. & King, J. R. (1976). Long-term effects of constant photoperiods on testicular cycles of White-crowned Sparrows (Zonotrichia leucophrys gambelii). Physiol. Zool. 49: 407 16. Schwab, R. G. (1971). Circannual testicular periodicity in the European Starling in the absence of photoperiodic change. In M. Menaker). Washington, DC, National Academy of Sciences. Senner, N. R., Hochachka, W. M., Fox, J. M. & Afanasyev, V. (2014). An exception to the rule: carry-over effects do not accumulate in a long-distance migratory bird. PLOS ONE 9: e86588. Serra, L. (2000). How do Palaearctic Grey Plovers adapt primary moult to time constraints? An overview across four continents. Wader Study Group Bull 93: 11 12. Serventy, D. L. (1971). The biology of desert birds. In D. S. Farner, & J. R. King). Avian biology (Vol. 1, pp. 287 339). London, Academic Press 287 339. Shaw, P. (2017). Rainfall, leafing phenology and sunrise time as potential Zeitgeber for the bimodal, dry season laying pattern of an African rain forest tit (Parus fasciiventer). J. Ornithol. 158: 263 75. Silverin, B., Massa, R. & Stokkan, K. A. (1993). Photoperiodic adaptation to breeding at different latitudes in Great Tits. Gen. Comp. Endocrinol. 90: 14 22. Singh, D., Reed, S. M., Kimmitt, A. A., Alford, K. A. Stricker, C. A. et al. (2021). Breeding at higher latitude is associated with higher photoperiodic threshold and delayed reproductive development in a songbird. Hormones Behav 128: 1044907. Snow, D. W. (1966). Moult and the breeding cycle in Darwin’s Finches. J. Ornithol. 107: 283 91. Sokolov, V., Sokolov, A. & Dixon, A. (2018). Migratory movements of Peregrine Falcons Falco peregrinus, breeding on the Yamal Peninsula, Russia. Ornis Hungarica 26: 222 31. Stanley, C. Q., MacPherson, M., Fraser, K. C., McKinnon, E. A. & Stutchbury, B. J. M. (2012). Repeat tracking of individual songbirds reveals consistent migration timing but flexibility in route. PLOS ONE 7: e40688. Stresemann, E. & Stresemann, V. (1966). Die Mauser der Vogel. J. Ornithol. 107: 3 448. Stutchbury, B. J. M., Gow, E. A., Done, T., MacPherson, M., Fox, J. W. & Afanasyev, V. (2011). Effects of post-breeding moult and energetic condition on timing of songbird migration into the tropics. Proc. R. Soc. Lond. B 278: 131 7. Summers, R. W., de Raad, A. L., Bates, B., Etheridge, B. & Elkins, N. (2019). Migration timing, staging areas and non-breeding localities of Scottish breeding Common Sandpipers Actitis hypoleucos. J. Avian Biol. 50: 1 11. Summers, R. W., Underhill, L. G., Waltner, M. & Swan, R. L. (2010). Differences in biometrics and moult of non-breeding Red Knots Calidris canutus in southern Africa and Scotland reflect contrasting climatic conditions. Ibis 152: 127 35. Swann, R. S. & Baillie, S. R. (1979). The suspension of moult by transSaharan migrants in Creˆte. Bird Study 26: 55 8. Underhill, L. G. (2003). Within ten feathers: primary moult strategies of migratory waders (Charadrii). Pp. 187 97 in Avian Migration (eds P. Berthold, E. Gwinner, & E. Sonnenscheion). Berlin, Springer Verlag. Van den Brink, B., Bijsma, R. G. & van der Have, T. M. (2000). European Swallows Hirundo rustica in Botswana during three non-

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Wolfson, A. (1959). Ecologic and physiologic factors in the regulation of spring migration and reproductive cycles in birds. Pp. 38 70 in Comparative endocrinology in Comparative endocrinology (ed. A. Gorbman, et al. (Eds.),). New York, Wiley. Wolfson, A. (1970). Light and darkness and circadian rhythms in the regulation of annual reproductive cycles in birds. Pp. 93 119 in Photore´gulation de la Reproduction chez les Oiseaux et les Mammife´res (eds J. Benoit, & I. Assenmacher). Paris, Colloques Intern CNRS No. 172.

Wyndham, E. (1982). Movements and breeding seasons of the Budgerigar. Emu 82: 276 82. Young, B. E. (1991). Annual moult and interruption of the fall migration for moulting in Lazuli Buntings. Condor 93: 236 50. Yuri, T. & Rohwer, S. (1997). Molt and migration in the Northern Rough-winged Swallow. Auk 114: 249 62. Zann, R. A., Morton, S. R., Jones, K. R. & Burley, N. T. (1995). The timing of breeding by Zebra Finches in relation to rainfall in central Australia. Emu 95: 208 22.

Chapter 13

Migratory control mechanisms

White-crowned Sparrow (Zonotrichia leucophrys), commonly used in experimental work on migration. Yea, the stork in the heavens knoweth her appointed time; and the Turtle (Dove), and the Crane, and the Swallow observe the time of their coming. Jeremiah (viii.7).

This chapter is concerned with the control of migration with the factors that stimulate migration at appropriate times of year and influence the directions and distances travelled. It is concerned with the external factors to which birds respond, such as daylength and food supply, and also with the internal regulating mechanisms. It thus attempts to integrate the findings from both field and laboratory studies and develops some aspects of migration mentioned in Chapter 12. The behavioural changes in a bird about to migrate involve an urge to depart given suitable weather and a tendency to fly long distances in one particular direction rather than any others. In addition, many normally diurnal birds also become active and migrate at night. The symptoms of this ‘migratory state’ are easily noticed in captive birds, which in appropriate seasons develop ‘migratory restlessness’ (or ‘Zugunruhe’), when they hop and flutter round their cages and show long periods of wing-whirring (fluttering the wings rapidly while perched, Box 13.1). Some species, such as the White-crowned Sparrow (Zonotrichia leucophrys), also spend long periods pointing the bill skywards and fluttering upwards, which in a net-topped cage provides a broad view of the night sky (Ramenofsky et al., 2003). Because most birds cannot feed while flying, the chief physiological change necessary for migration involves the accumulation of fat and other body reserves to sustain the bird and fuel its flight (Chapter 5). The symptoms of this state include increases in the food intake and weight of the bird, and the deposition of body fat (Chapter 5). Once adequate fat has accumulated, migration usually follows, but adverse weather might delay departure (Chapter 14).

OBLIGATE AND FACULTATIVE MIGRATION At the outset, it is useful to distinguish between obligate migration (formerly called instinct or calendar migration) and facultative migration (formerly called weather migration). In obligate migration, all main aspects are viewed as under firm internal (genetic) control, mediated by daylength changes, which gives great annual consistency in the timing, directions and distances of movements (Chapter 22). For the most part, each individual behaves in the same way year after year, migrating at similar dates and often for similar distances. Typically, obligate migrants leave their breeding areas well before food-supplies collapse. Their behaviour can be regarded as anticipatory, in that they leave before conditions become impossible for them. They tend to migrate long distances, often to the tropics or beyond, and frequently travel by night. The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00015-4 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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BOX 13.1 Migratory restlessness When caged birds reach a migratory state, they usually show periods of wing-whirring, together with increased perch-hopping, body turning and other activities. Cages are too small to allow flight and while birds that are caged straight from the wild flutter around and try to escape, they eventually adjust to cage-life, and show wing-whirring instead a cage-adapted behaviour, viewed as “migration in a sitting position” (Berthold, 1996). Migratory restlessness (or Zugunruhe) has now been recorded in caged birds from more than 100 different species. It can be quantified from the alteration of the normal pattern of diurnal locomotor activity, especially from peaks in activity at species-specific times of day or night. The behaviour can be recorded automatically in various ways. By subtracting activity patterns obtained in non-migratory periods from those recorded during migratory periods, migratory restlessness can be quantified, basing the comparison on day-time or night-time activity, as appropriate. The notion that this behaviour in caged birds is equivalent to migration in wild birds is supported by four types of observation. First, it is typically most extreme in birds from migratory populations and is much less developed in birds from nonmigratory ones. Second, in more than 25 species and populations studied in detail, migratory restlessness is broadly related to the specific migratory seasons of the population concerned. Third, at least in some species, the duration of the autumn period of migratory restlessness corresponds to the length of the autumn migratory journey (Figure 13.2). Fourth, in nocturnal migrants, the behaviour occurs at night and in diurnal migrants in the daytime. Typically, the intensity of nocturnal migratory activity is higher on moonlit than on overcast nights. Recent studies have further validated the link between Zugunruhe in cages and migration in the wild (Eikenaar et al., 2014; Mukhin et al., 2018). For example, Northern Wheatears (Oenanthe oenanthe) were caught from the wild and kept overnight, testing them for restlessness and then in the morning releasing them with a radio-tag. Individuals showing very little migratory restlessness remained on a stopover for longer than one night, whereas most individuals showing more restlessness departed sooner. These findings further validated the use of migratory restlessness as a proxy for the motivation to migrate (Eikenaar et al., 2014) Nevertheless, the link between Zugunruhe and migration in the wild is not always so clear-cut, and not all nocturnal activity can be viewed as migratory restlessness. Resident populations of otherwise migratory species can sometimes show apparent Zugunruhe; some birds occasionally show nocturnal restlessness outside the normal migration seasons; and the correlation between duration of restlessness and migratory distance has not always held. However, such discrepancies can usually be explained on other grounds, and it seems safe to conclude that Zugunruhe is strongly related to migration, although not consistently so.

In contrast, facultative migration is viewed more as a direct response to prevailing conditions, especially food supplies which vary from year to year. The same individual may migrate in some years but not others (Chapter 22). Within a population, the proportions of individuals that leave the breeding range, the dates they leave and the distances they travel can vary greatly from year to year, as can the rate of progress on migration, all depending on conditions at the time (Sva¨rdson, 1957; Terrill, 1990; Moore et al., 2003; Newton, 2012). In consequence, facultative migrants may be seen on migration at almost any date in the non-breeding season (at least into January in the northern hemisphere), and their winter distributions can vary greatly from year to year (Chapters 20, 21). Nevertheless, other aspects must presumably be under firmer genetic control, notably the directional preferences and the tendency to return at appropriate dates in spring. Compared with obligate migrants, facultative migrants tend to migrate shorter distances, although many exceptions occur. The two types of migrants thus have different distribution patterns in mid-winter. Whereas obligate migrants are concentrated in a distinct wintering area, usually far from the breeding area, facultative migrants are typically found over the whole migration route from breeding to wintering areas, usually tailing off with increasing distance, but with marked annual variations (Newton, 2012). The distinction between obligate and facultative migrants is useful because it reflects the degree to which individual behaviour is sensitive to prevailing external conditions and hence varies from year to year. However, obligate and facultative migrants are best regarded, not as distinct categories, but as opposite ends of a continuum, with predominantly internal control (5rigidity) at one end and predominantly external control (5flexibility) at the other. Another reason for not drawing a sharp distinction between the two categories is that many birds seem to change from obligate to facultative mode during the course of their journeys, as the endogenous drive to migrate wanes with time and distance, and the stimulus to continue becomes more dependent on local conditions (Helms, 1963; Terrill & Ohmart, 1984; Gwinner et al., 1985; Terrill, 1990). Theoretically, the initial obligate phase of any journey might take the migrant across regions where the probability of overwinter survival is practically zero: where any individuals that attempted to winter in the past were eliminated by natural selection. As migration continues to more benign areas and

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survival probability rises, the bird switches to a facultative mode, in which it benefits by responding to local conditions, for example, by stopping where food is abundant. The obligate phase would therefore be expected to be undertaken much more rapidly, on average, than the facultative phase, which involves longer and more variable stops. Such a twophase migration, with obligate and facultative stages, would also ensure that, in any particular year, the bird migrated no further than necessary. In some species, only the tail end of the migration may be facultative, in others the entire journey. Most irruptive migrants, such as redpolls and siskins, are near the latter end of the spectrum. Further support for the idea that migration is often two-phase comes from studies of captive birds. In White-throated Sparrows (Zonotrichia albicollis), Helms (1963) identified two subdivisions of migratory behaviour in both autumn and spring. The first phase (which he called the ‘motivational subdivision’) was characterized by intense and continuous night-time activity, while the second phase (the ‘adaptational subdivision’) was less intense, with numerous interruptions and greater variability. Helms (1963) aligned these two phases with the behaviour of free-living birds during spring migration, as they switched from an intense, highly directed phase to a more casual ‘wandering phase,’ in which they searched for suitable habitat and took advantage of local opportunities. In addition, observations of the directional preferences of caged migrants revealed an increasing variance in headings towards the end of the migratory period (Wiltschko & Wiltschko, 2003).

Role of dominance in facultative migrants Because birds compete for food, and vary in dominance or feeding efficiency, some individuals could survive in conditions where others would die unless they moved on. In facultative migrants, the subordinate sex and age groups typically migrate in greater proportions, at earlier dates, or extend further from the breeding areas, than the dominants (Chapter 18). In many facultative migrants, adult females are more migratory than adult males, juveniles more than adults, and late-hatched young more than early-hatched ones (Chapter 18; Gauthreaux, 1978; Lundberg, 1985; Smith & Nilsson, 1987; Chapman et al., 2011). Such differences have led to the notion that competition (or its effect on body condition) is involved as a proximate mechanism stimulating migration in those individuals least able to survive in local conditions. But because dominant individuals are also often larger than others, they may be able to better survive winter cold and fasting (Ketterson & Nolan, 1976). For these dominant individuals, one advantage of staying over winter is assumed to be acquisition of the best nesting territories in early spring before the migrants return (Schwabl, 1983; Kokko et al., 2006). The sequence of behavioural events stimulating migration in facultative migrants could thus be hypothesized as social status - competition - failure to obtain a winter territory or sufficient food - difficulty in maintaining body condition - departure. On this mechanism, the overall proportion of birds stimulated to migrate would depend on feeding conditions that year, with more birds from the dominant age groups departing in poor food years than in good ones. That the effects of food supply could be mediated by social dominance was shown in captive Dark-eyed Juncos (Junco hyemalis), in which subordinate individuals were most likely to put on fat and show migratory restlessness (Figure 13.1; Terrill, 1987). It may seem surprising that losers can put on fat, but they seem to do so through changes in physiology and behaviour, feeding for much longer each day than usual at the expense of other activities. SINGLE FOOD SOURCE

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1 DOM SUB 23 pairs LOW FOOD

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FIGURE 13.1 Effect of social environment, food availability and distribution on migratory restlessness of Dark-eyed Juncos (Junco hyemalis). Low food: 8 g of food per day for each twosome; high food: 14 g of food per day for each twosome. Single source: food placed in a single container in the centre of each pair’s cage; double source: food divided between two containers. SUB, subordinate partners of twosomes; DOM, dominant partners. From Terrill (1990).

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MIGRATION TIMING, DISTANCES AND DIRECTIONS Under natural daylengths, caged birds from obligate migratory populations develop fat reserves and migratory restlessness at appropriate dates in autumn and spring, at about the same times as their wild counterparts. Evidently, the same factors that stimulate departure in wild birds trigger restlessness in captive ones kept on natural daylengths (Gwinner, 1972; Berthold, 1996). The role of daylength in promoting these processes (in association with an endogenous rhythm) is shown by findings discussed in detail later, namely that (1) captive birds experimentally exposed to photoperiods longer than natural days in spring develop migratory condition earlier than their wild counterparts; and (2) birds exposed to photoperiods shorter than natural days in late summer or autumn also develop migratory condition earlier than their wild counterparts. In addition, wild birds tend to leave under falling temperatures in autumn and under rising temperatures in spring (Lack, 1960; Dierschke, 2006; Sjo¨berg et al., 2015; Woodworth et al., 2015; Chapter 4), but the actual departure dates are also influenced by other aspects of weather (Chapter 14).

Time-distance programmes In general, the further apart breeding and wintering areas are the greater the duration and intensity of migratory restlessness shown by caged birds. Different Sylvia warblers migrate average distances varying from a few hundred to nearly 6000 km, and in captivity they show corresponding average periods of restlessness varying from less than twenty to more than 1000 hours (Figure 13.2). The Marsh Warbler Acrocephalus palustris, which breaks its autumn journey between Europe and southern Africa for up to several weeks in equatorial Africa, shows in captivity a prolonged and two-phase pattern of autumn restlessness; but in spring when it returns in a shorter single period, it shows in captivity a shorter single period of restlessness (Berthold & Leisler, 1980; Berthold, 1993). In addition, the amount of fat accumulated by captive birds at migration times is related to the types of journeys they make in the wild. Birds that migrate by long flights, as from Europe to sub-Saharan Africa, typically accumulate more fat in captivity than do birds that migrate short distances within Europe (Chapter 22; Berthold, 1973, 1984). This contrast is evident in comparisons between related species, such as Willow Warbler (Phylloscopus trochilus) and Common Chiffchaff (Phylloscopus collybita) (Gwinner, 1972), and between different populations of the same species which migrate different distances, as in the Blackcap (Sylvia atricapilla) (Figure 20.2; Berthold & Querner, 1981). Even more remarkably, sex differences in the timing and duration of migratory restlessness emerged in captive birds of several species tested in spring (males earliest in White-throated Sparrow, Dark-eyed Junco, Eurasian Blackcap (S. atricapilla), Pied Flycatcher (Ficedula hypoleuca) and Common Redstart (Phoenicurus phoenicurus), Helms, 1963; Ketterson & Nolan, 1983; Terrill & Berthold, 1989; Coppack & Pulido, 2009), and in Dark-eyed Juncos also tested in autumn (females earliest, Holberton, 1993). These sex differences in migration timing held even though males and females were exposed to identical photoperiods and ad-lib food. They were taken as indicating inherent differences in circannual rhythmicity or photoperiodic responsiveness between the sexes, presumably evolved through different selection pressures. They do not exclude the possibility that, in the wild, sex differences could also be influenced by other factors, such as winter habitat and access to food (Marra et al., 1998). Taken together, these various findings indicate that the timing and duration of migratory behaviour are adaptive, and partly under endogenous control as ‘time-distance programmes’. Genetic influence is supported by various findings, notably by hybridization experiments in which hybrids between species showed behaviour intermediate between that of their parents (Chapter 22). FIGURE 13.2 Relationship between the usual distance migrated and the number of hours that captive juveniles showed migratory restlessness, shown for different populations of Sylvia warblers. The longer the journey undertaken by wild birds, the more hours of migratory restlessness were shown by captive birds from the same population. From Berthold (1973).

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Directional preferences Birds taking different directions in the wild show the same directional differences when tested in captivity. Some migrants in spring retrace their path of the previous autumn, but loop migrants take markedly different routes at the two seasons (Chapter 24). When tested for directional preferences in orientation cages, hand-reared Garden Warblers (Sylvia borin) kept in constant (12L:12D) conditions changed their mean heading from southwest to southeast part way through their autumn migration period. This corresponded with a change they would normally make part way through their journey between central Europe and Africa (Gwinner & Wiltschko, 1978, 1980). They made no such change in spring, when they return by a more direct northerly route. The whole pattern was in line with the loop migration routes between Europe and Africa revealed by ring recoveries. Other spontaneous shifts in directional preferences were also recorded during the migration seasons of captive Eurasian Blackcaps (Helbig et al., 1989), Pied Flycatchers (Beck & Wiltschko, 1988) and Yellow-faced Honeyeaters (Lichenostomus chrysops) (Munro & Wiltschko, 1993), all of which perform loop migrations in the wild. The most obvious difference between seasons, namely the direction of travel, is apparently controlled by daylength changes and their effects on the bird, increasing daylengths in spring causing the bird to head north and decreasing daylengths in autumn south. By appropriate manipulation of photoperiods, Emlen (1969) brought two groups of captive Indigo Buntings (Passerina cyanea) into spring and autumn migratory condition at the same time as one another. He then tested the directional preferences of both groups under identical planetarium skies. Birds in autumn condition oriented southward, and those in spring condition northward. In some earlier experiments, Dark-eyed Juncos and American Crows (Corvus brachyrhynchos), which had been exposed to long photoperiods in mid-winter, moved northward when released. However, castrates of these species migrated southeast after release, as did control birds that had not been photo-stimulated (Rowan, 1925, 1932). This finding suggested that the effects of daylength could be mediated by the differing levels of gonadal hormones present in autumn and spring. A later study showed that the orientation of captive White-throated Sparrows could be reversed by altering the temporal pattern of administration of the hormones prolactin and corticosterone. Birds injected with prolactin 4 hours after they had been injected with corticosterone oriented southward, whereas birds given prolactin 12 hours after corticosterone oriented northward (Martin & Meier, 1973). It seemed that the state of the gonads (and associated hormones), themselves dependent on the daylength regime, could influence migratory direction to springappropriate or autumn-appropriate, as the case may be.

Integration of time distance and direction programmes The combination of inherent time distance programmes and directional preferences provides a plausible explanation of how juvenile birds, migrating on their own, can reach wintering areas unknown to them but specific to their population. After an appropriate time, caged birds from both European and North American breeding areas lost their autumn restlessness and fat reserves, even though they had moved no further than their cages allowed. Moreover, when captive juveniles were experimentally transported to their species-specific wintering areas, or even beyond their normal wintering range, the migratory activity they showed in cages persisted as long as that of individuals kept in the breeding area (for experiments on young Garden Warblers, Lesser Whitethroats (Curruca curruca) and Pied Flycatchers, see Gwinner, 1971; Rabøl, 1993). These birds also showed appropriate directional preferences. Similarly, juvenile Common Starlings (Sturnus vulgaris) and other species that were trapped on migration, flown by airplane and released immediately in the usual wintering areas for their population, or at some other locality off the normal route, resumed migration. Ring recoveries revealed that these transported birds moved in the same direction and covered about the same additional distance that they would have travelled had they not been displaced (Chapter 10; Perdeck, 1964, 1967). These experiments again suggested control of timing and direction in juvenile birds by an innate endogenous programme, rather than by location. In a different type of experiment, juvenile Blue-winged Teal (Spatula discors) were caught in autumn, held in captivity for some days and released at the same place. Many then migrated in the same direction but over shorter distances than normal (Bellrose, 1958). This would also be expected if they were migrating to a time programme. While all these findings suggest that non-breeding destinations are broadly set by inherent time distance and directional programming, this does not mean that birds are unable to move on if they encounter unsuitable conditions, or if they are homing to a specific site experienced in a previous year. Nor does it mean that all migratory species behave in this way, irruptive and other facultative migrants being more flexible in timing and distance (Chapter 20).

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Role of experience On current thinking, then, the urge to migrate in autumn and spring, at least in obligate migrants, is genetically controlled, accompanied by changes in physiology and behaviour, and kept on schedule by daylength changes (Gwinner, 1972, 1986; Berthold, 1996; Chapter 12). This inherent system controls both fattening and migratory restlessness, as well as the general direction and time-course of migration. These ideas were based mainly on experimental work involving naı¨ve juvenile birds which had no previous knowledge of the wintering range of their population. The situation differs somewhat in experienced birds migrating to a known site, as first shown in the experiments with Common Starlings and others described in Chapter 10. Whereas juveniles made no correction for their displacement in autumn, and continued in the usual direction but parallel to their usual route, adult birds displaced off their normal route in autumn changed direction and headed to their previous wintering areas. However, on return migration to their breeding areas, both juveniles and adults proved able to return to the region of their birth or previous breeding (Chapter 10; Perdeck, 1958). Prior experience of an area enabled both juveniles and adults to compensate for their displacement and find their way back. Early findings on the role of experience were extended by work on Dark-eyed Juncos, in which adults usually return to the same breeding and wintering sites in successive years. Adults caught in July on their breeding areas and transported to a locality within the wintering range showed the usual autumn restlessness and fattening, perhaps because they were not released on their specific wintering areas of previous years (Ketterson & Nolan, 1986). On the other hand, birds caught in winter and held at the capture site over summer showed no migratory restlessness and fattening during the next autumn. This held for birds kept on local “wintering area” photoperiods, and for birds kept on wintering areas but exposed to longer photoperiods typical of their breeding areas. The locations of these captive birds on their previous wintering areas apparently suppressed their autumn migratory behaviour. But both groups showed migratory behaviour in spring. A further experiment involved a similar procedure, except that adult Juncos that had been held captive over summer in their wintering areas were released there in September, the normal time of autumn migration. Of 129 birds released, 47 were subsequently re-sighted in the release area, often within the same home range where they had been caught in the previous winter. Evidently, these birds, which were already in wintering sites known to them, did not migrate that autumn. However, they apparently did migrate in the following spring (as none were found in wintering areas), and in the next autumn when some re-appeared on their winter ranges (Ketterson & Nolan, 1986). The holding of Juncos on a previous (known) wintering site was apparently sufficient to suppress the usual autumn migration. It was uncertain what happened to the birds that were not re-sighted, but if they had dispersed only a short distance from the release sites, they would not have been found. Overall, these experiments provided further indication that the endogenous template of migration could be altered by experience. Adults and juveniles behaved differently, as the former had experience of a wintering area and the latter not. However, both groups had experience of former breeding (or natal) areas and could return there after displacement or after being held captive. Dark-eyed Juncos that were kept captive in wintering areas for up to two months beyond the normal spring departure date disappeared (presumably migrated) upon release, even though their gonads were by then in full breeding condition (Wolfson, 1942, 1945). Likewise, among various warblers and finches that were caught in spring and held captive at a locality on route, migratory restlessness and appropriate directional preferences continued for up to several weeks longer than normal (Merkel, 1956; Shumakov et al., 2001). Bramblings (Fringilla montifringilla) caught on spring migration, but south of their breeding range, also showed northeast directional preferences until late August, long after their spring migration would normally have finished. These various findings could be interpreted as continuing attempts by these birds to reach their breeding areas, again indicating the importance of locality in suppressing the migratory behaviour of experienced birds returning in spring to a familiar area. It may account for the fact that some other birds caught from the wild and tested in captivity continued spring restlessness well into summer, or autumn restlessness well into winter, much beyond the normal migration seasons. They could have been birds held far away from their previously experienced breeding or wintering sites. That spring migration can be suppressed by recognition of a familiar area was shown in an experiment with Indigo Buntings (Sniegowski et al., 1988). Males were caught on their nesting territories, held over winter and released there in spring at a date when migration was just beginning in conspecifics wintering far to the south. Controls were transported and released 1000 km to the south. Seven out of 20 buntings released in spring on their nesting territories remained, while eight out of 20 released to the south returned to their nesting localities. The remaining birds in each group were unaccounted for. Nevertheless, these results indicated that when migrants were exposed before spring migration to their previous nesting place, they stayed there and did not migrate.

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TABLE 13.1 Results of some trap and retention experiments (see text). Experiment

Result

Interpretation

Species

Source

Held over first winter in breeding area

Did not subsequently migrate

Fixation to former wintering area greater than motivation to migrate in autumn

White Stork (Ciconia ciconia)

Fiedler (2003)

Held in wintering area over summer and then released

Did not migrate but stayed in wintering area until spring

Fixation to former wintering area greater than motivation to migrate in autumn

Dark-eyed Junco (Junco hyemalis), Dunnock (Prunella modularis)

Ketterson & Nolan (1986)

Held in breeding area over winter and then released

Did not migrate but stayed in breeding area until autumn

Fixation to former breeding area greater than motivation to migrate in spring

Indigo Bunting (Passerina cyanea)

Sniegowski et al. (1988), Ketterson & Nolan (1990)

Held on spring migration route

Showed prolonged migratory restlessness

Failure to reach breeding area resulted in migratory restlessness beyond the normal period

Dark-eyed Junco (Junco hyemalis), Chaffinch (Fringilla coelebs), Brambling (Fringilla montifringilla)

Merkel (1956), Shumakov et al. (2001)

Held on spring migration route and released about two months late

Left site, presumably on migration

Failure to reach breeding area resulted in prolongation of migratory behaviour

Dark-eyed Junco (Junco hyemalis), Brambling (Fringilla montifringilla)

Wolfson (1942, 1945), Shumakov et al. (2001)

During reintroduction projects at various localities in Western Europe, White Storks (Ciconia Ciconia) were reared and kept in aviaries for at least one winter, which prevented them from migrating as they normally would. After they had been released, they remained in the same areas year-round, breeding and wintering there and supported by supplementary food in winter. However, their free-living offspring migrated as normal for their population, yielding ring recoveries along the usual southwestern migration route (Fiedler, 2003). These findings provided further indication that experience based on learning and memory can modify the inherent migratory behaviour of individuals. The findings from these different types of experiments, summarized in Table 13.1, imply that the endogenous mechanisms controlling the timing and occurrence of migration, as evident especially in naı¨ve juveniles, could be over-ridden by the experience and site-attachment shown in older birds.

Migratory fattening and restlessness The role of feeding conditions in affecting fattening rates, body condition and departure dates has been established in the field for a range of species from Sedge Warbler (Acrocephalus schoenobaenus) (Bibby & Green, 1981) to Greylag Goose (Anser anser) (van Eerden et al., 1991). In field experiments, birds fed supplementary food fattened more rapidly and left earlier than other individuals which had access only to natural food (Fransson, 1998; Da¨nhardt & Lindstro¨m, 2001; Schmaljohann & Dierschke, 2005). In general, individuals that fattened most rapidly left first, whether in autumn or spring, or from starting or stopover sites (Chapter 14). Poor feeding conditions contributed to the variation in departure dates between individuals and delayed the progress of whole populations in some years (Chapter 30).

Diurnal patterns Another facet of migration that seems to be inherently programmed is the diurnal pattern of activity. It is not simply that, in captivity, diurnally migrating species show migratory restlessness by day, and nocturnally migrating ones by night. The hour-to-hour patterns of restlessness seen in captive birds, whether day or night, match fairly precisely the hour-to-hour patterns of migration seen in the wild (for White-throated Sparrow, see McMillan et al., 1970, for Common Reed Bunting (Emberiza schoeniclus), see Berthold, 1978). As further evidence for endogenous influence, Common Redstarts caught on migration through Europe were held captive for three days under constant dim light and permanent food (Coppack et al., 2008). Despite the absence of

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external stimuli, these birds showed clear bimodal activity patterns, with intense nocturnal activity alternating with diurnal foraging and resting periods. The onset of their migratory activity coincided with the time of local sunset and within individuals was consistent on consecutive nights, another indication that these night-migrating birds were influenced by autonomous circadian cycles, albeit previously entrained by the diurnal light cycle. The fact that many normally diurnal birds migrate at night implies that they switch seasonally from almost exclusively day-time activity to round-the-clock activity, with flight mainly at night. Nocturnal activity is strikingly evident on radar screens at migration times, and in captive birds by their patterns of migratory restlessness. Throughout the year, diurnal migrants in captivity show a peak of (feeding) activity in the morning and a smaller one in late afternoon, but at migration times, these peaks are much more marked (e.g. Munro, 2003). In addition, nocturnal migrants in captivity tend to become inactive in the afternoons before nights of migratory activity. They cease feeding about two hours before dusk, which in the wild would give time for the gut to empty before take-off (Ramenofsky et al., 2003). They go to roost in the normal way and become active some time later.

AUTUMN MIGRATION Migrants normally leave their breeding areas when conditions deteriorate, but not sufficiently to reduce their survival chances. In association with the earlier onset of winter at high latitudes, many multi-brooded species, which can vary the length of their breeding seasons, generally withdraw from high-latitude parts of their breeding range first, and from lower-latitude parts later. But single-brooded species, whose breeding cycle is of fixed length, both start and end their breeding later at higher latitudes, so also tend to migrate later from higher latitudes. The assumption is that, in order to prepare for autumn migration, populations have evolved responses to different daylength regimes, appropriate to the latitude at which they breed. From any one area, departure dates also differ widely between species, depending largely on their type of food and when it becomes scarce (Chapter 15). As elsewhere in this book, I use the term autumn migration for the post-breeding exodus towards wintering areas, even though in some species this migration occurs in the latter half of summer. In obligate migrants, in which all individuals leave the breeding area each autumn, the dates of migration at the population level are in general fairly consistent from year to year. This is apparent not only in the dates that birds leave their breeding areas but also in the dates they pass particular places on their migration routes and arrive in wintering areas. For example, among raptors migrating through Israel, the timing and duration of passage varied greatly between species, but within species the autumn passage dates were remarkably similar between years (as were spring dates). Over nine years, the confidence intervals of the mean autumn dates ranged between 1.5 and 3.4 days (vs 2.1 5.5 days for spring dates), depending on species (Leshem & Yom-Tov, 1996). Obligate migrants usually set off on migration soon after finishing breeding or after moult if they moult in breeding areas, so at the population level, departure dates are roughly similar from year to year. However, this is not always true of facultative migrants which, if conditions are favourable, may linger longer in breeding or stopover areas, leaving only when food supplies dwindle or are shut off by snow and ice. Mean autumn migration dates may therefore vary greatly from year to year, depending on local food supplies, as may rates of travel. This situation is exemplified by most short-distance migrants, but especially by irruptive seed-eaters (Chapter 20), and by waterfowl and others affected by frost (e.g. Hario et al., 1993). For example, Eurasian Siskins (Spinus spinus) passed through Falsterbo Bird Observatory in Sweden in largest numbers, and at the earliest dates, in years when birch seeds (the main autumn food) were scarce, with peak passage varying by up to several weeks between years (Sva¨rdson, 1957; Chapter 20). Likewise, the date on which the last Whooper Swans (Cygnus cygnus) left Lake Chuna on the Kola Peninsula each year during 1931 1999 varied between about 20 September and 9 November, depending on when the lake froze over (Gilyazov & Sparks, 2002). Such facultative migrants evidently depart chiefly when deteriorating conditions encourage them to leave. Together with variable conditions on migration routes, this facultative response gives wide variation in the dates that birds arrive in their various wintering areas, the more distant of which may be reached only in occasional years. Various species in captivity have started or increased their migratory restlessness in autumn, in response to a lowering of temperature or a restriction of food-supply (reviews Farner, 1955; Helms, 1963). For some captive Whitethroated Sparrows in autumn, Berchtold et al. (2017) manipulated temperatures between 4 C, 14 C and 24 C and monitored their behaviour. At warm temperature (24 C), none of the birds showed migratory restlessness. However, the probability of showing restlessness and its intensity increased at cooler (14 C and 4 C) temperatures. These findings implied that temperature could influence whether birds stay or leave, and that their response to temperature was additional to their response to daylength or other cues.

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Split migrations Although autumn migration in some species can be considered as a single event, consisting of alternating periods of flight and fattening, other species break their autumn journeys for periods of several weeks, much longer than is needed for re-fuelling (Chapter 12). Some species moult during this break in migration. Long breaks are shown by many Eurasian migrants to Africa, which remain in the northern tropics for several weeks, and only later move on to the southern tropics (Chapter 26). In this way, they get the best from both regions, remaining in the northern tropics until conditions deteriorate and arriving in the southern tropics at the optimal time, after fresh rains have promoted vegetation growth. In captivity, as mentioned already, such species showed two separated peaks of migratory restlessness (Berthold, 1993). Equivalent behaviour is shown by some species that migrate between North and South America (Terrill & Ohmart, 1984; McKinnon & Love, 2018). Interrupted migrations are also evident in various irruptive and other facultative migrants which may break their journeys to exploit food supplies they encounter on route, not necessarily in the same places in different years (Sva¨rdson, 1957; Newton, 1972, 2008; Chapter 20). Probably most species that migrate within the northern continents move further from their breeding areas during the course of the winter, as weather worsens and food-supplies decline. The first part of their migration may be obligate and the latter part facultative. One consequence of such split migration is that the outward journey (including the breaks) takes more than 3 months in some species, whereas the return journey in spring is unbroken and can take less than 1 month.

Relationship between breeding, moult and autumn migration In species that moult in their breeding areas, individuals that finish breeding late also moult and migrate later (e.g. Mitchell et al., 2012; van Wijk et al., 2017). However, they may begin moult earlier with respect to a nesting cycle, well before their young have fledged, and may also moult more rapidly than earlier birds (for Dunlin (Calidris alpina), see Johnson & Minton, 1980, for White-crowned Sparrow, see Morton & Morton, 1990, Morton, 2002, for European Goldfinch (Carduelis carduelis), see Newton & Rothery, 2009). By these means, individuals breeding until late in the season reduce the delay in their migration. In some passerines, the delay in moult caused by late breeding is greater in females than in males, producing differences in departure dates between the sexes, including members of the same pair (Ginn & Melville, 1983, for Cetti’s Warbler (Cettia cetti), see Bibby & Thomas, 1984, for Willow Warbler, see Norman, 1990). Similar things happen in the juveniles. In multi-brooded populations, young are produced over periods of several weeks. Compared to early-hatched young, later ones start to moult at a later date but at an earlier age, and may also replace their feathers more rapidly or less completely (for Common Chaffinch (Fringilla coelebs), see Dolnik & Gavrilov, 1980; for various warblers, see Berthold, 1988, for White-crowned Sparrow, see Morton, 2002, for Stonechat (Saxicola torquata), see Helm, 2003, for European Greenfinch (Chloris chloris), see Newton & Rothery, 2005). Among Great Tits (Parus major) in northern Europe, first brood young start moulting in July, and second brood young in midAugust, the mean age at the start of moult decreasing over this period from 56 to 42 days, and the mean duration of moult from 67 to 59 days (Bojarinova et al., 1999). Because of these differences, the late-hatched young also migrates at an earlier age than early-hatched ones, with a mean difference of four weeks between their departure dates (Bojarinova et al., 2002). These differences between early and late birds again tend to lessen the delay in the migrations of late birds. In addition, while early young normally prepare for migration after completing moult, late birds may begin to fatten well before the end of moult (for Garden Warbler and Eurasian Blackcap, see Berthold, 1975). Among Mountain White-crowned Sparrows, Z. l. oriantha in California, autumn fattening usually took 8 9 days, as found by the repeated weighing of individuals (Morton, 2002). In a few early individuals, moult had been finished for up to two weeks before fattening began, but in some late birds, fattening began up to two weeks before moult ended. The time-saving resulting from quicker development of late young can be substantial. For example, among European Stonechats kept in captivity on natural daylengths, the mean age of moult onset declined from about 105 days to 59 days, the mean moult duration from 65 to 50 days and the mean age of onset of migratory restlessness from 180 to 120 days among young hatched from mid-April to early-August (Figure 13.3). This 16-week hatching period was thus reduced to eight weeks in the onset of migratory fattening. Similarly, in German Blackcaps, the earliest young leave the nest in late May and the latest in August. Their hatching dates are spread over about 72 days, but owing to accelerated development (especially of moult), the late young develop migratory activity only 18 days later than the early ones. Late young are ready to migrate in September, but without accelerated development they could not depart until mid-November, a dangerously late date (Berthold, 1988). One consequence of the

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FIGURE 13.3 The relationship between hatching date and age of onset of moult (top), moult duration (middle) and age of onset of migratory restlessness (bottom) in captive European Stonechats (Saxicola torquate) kept on natural daylengths. Later hatching individuals start moult and migratory fattening at a later date, but at an earlier age than early-hatched ones and also moult more rapidly. Modified from Helm et al. (2005).

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relationship between hatching date and development rate is that, in years of late breeding, an entire population can moult, on average, later (but juveniles at an earlier age) and more rapidly than usual in preparation for migration (for Lapland Longspur (Calcarius lapponica), see Fox et al., 1987). Conversely, if birds fail in their breeding, they usually start moulting or migrating earlier than usual, and in poor breeding years, many individuals can begin their post-breeding migrations a week or more ahead of normal, whether passerines, shorebirds or waterfowl (Maisonneuve & Be´dard, 1992; Blomqvest et al., 2002). In experimental conditions, various passerine migrants started post-juvenile moult and autumn migratory activity at a younger age if held under short photoperiods (Gwinner, 1972; Jenni & Winkler, 2020; Berthold, 1996; Noskov et al., 1999; Coppack et al., 2001; Gwinner & Helm, 2003). They also moulted and fattened more rapidly, or showed more overlap between moulting and fattening (for Bobolink (Dolichonyx oryzivorus), see Gifford & Odum, 1965, for Whitecrowned Sparrow, see Moore et al., 1982, for Bluethroat (Luscinia svecica), see Lindstro¨m et al., 1994, for Lesser Whitethroat, see Hall & Fransson, 2001, for Eurasian Siskin, see Newton & Dawson, 2011). These findings indicated that the shortening days of autumn accelerated the development of late-hatched young in the wild. In all these species, the ending of moult probably does not itself promote the start of fattening because the two events do not invariably coincide, and as fattening rates increase with reducing daylength (5advancing date), this can be regarded as another time-saving adaptation in late birds. In various species, late individuals may also accumulate greater fat reserves than early ones before they leave their breeding areas or stopover sites. Increased fattening rates or greater fat reserves in late season have been recorded in many species, including Bluethroat (Ellegren, 1991), Common Whitethroat (Curruca communis) and Lesser Whitethroat (Ellegren & Fransson, 1992), Eurasian Blackcap (Izhaki & Maitav, 1998a,b), Eurasian Reed Warbler (Acrocephalus scirpaceus) (Balanc¸a & Schaub, 2005), Goldcrest (Regulus regulus) (Bojarinova et al., 2008) and Temminck’s Stint (Calidris temminckii) (Hedenstro¨m, 2004). Similarly, in several passerine species studied at Ottenby in Sweden, body mass and fat level were found to increase during the course of the several˚ kesson et al., 1995; Fransson, 1998; Da¨nhardt & Lindstro¨m, 2001). Evidence week autumn migration season (A from ring recoveries and tracking studies revealed that birds which migrated late in the season also travelled more rapidly than earlier ones from the same population, as again described in a wide range of species from ringing and tracking studies (Chapter 12). Speed of migration may therefore be another aspect of the annual cycle that responds to date, more rapid migration late in the season being achieved by faster and greater re-fuelling rates, and shorter stopovers. The influence of daylength on migration speed was shown experimentally in Long-tailed Tits (Aegithalos caudatus) caught on migration and taken into captivity (Bojarinova & Babushkina, 2015). Some individuals were kept on natural photoperiods while others were switched to shorter photoperiods. At the beginning of the experiment, locomotory activity was the same in both groups. But three weeks later, individuals exposed to shorter days (simulating a delay in migration) showed significantly higher levels of activity. The implications were that Long-tailed Tits were photosensitive in October with respect to their migratory behaviour, and under natural conditions they would speed up their migration under shorter days. In conclusion, response to daylength not only influences the timing of autumn migration: in late-breeding adults, and in juveniles hatched late in the season, it can speed up the moult and increase the overlap between breeding and moult (adults only), or between moult and fat deposition. It can also increase the rate and extent of fat deposition and increase the speed of migration. These various responses all serve to reduce the delay in migration caused by late breeding. The acceleration of development under short daylengths, known as the ‘calendar effect’ (Berthold, 1993), is of functional significance in allowing late birds to leave breeding areas before conditions worsen sufficiently to threaten survival (Berthold et al., 1970; Berthold, 1988). In species which depart immediately after breeding, findings with respect to moult do not hold, because moult is postponed until after arrival in a staging area or winter quarters. There are, however, costs to more rapid development late in the season. Feathers grown during a period of rapid moult are sometimes of poorer quality, which could reduce a bird’s chance of survival (Dawson et al., 2000). The greater fat levels accumulated by late migrants may also make them more vulnerable to predation. Hence, the greater acceleration and overlap of different processes in late birds probably involves a trade-off. It saves time but only at the cost of additional daily energy needs and reduced feather quality. While studied mainly in passerines, links between breeding, moult and autumn migration timing are also apparent in other species, including waterfowl, in all of which late birds show at least partial catch-ups (MacInnes, 1966; Maisonneuve & Be´dard, 1992; Black & Rees, 1984). Nevertheless, late breeding still leads to late migration, because ‘catch-ups’ in this period are not complete.

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SPRING MIGRATION Birds normally leave their wintering areas so as to reach their nesting areas in time to breed at the most favourable season. Many migrants winter so far from their breeding areas that they could not judge conditions there from their position in wintering areas. They can only leave these areas at a time that natural selection has decreed is appropriate, using an internal timer, perhaps coupled with local conditions, as a cue. Their behaviour is again ‘anticipatory’. Among species wintering in the temperate zone, the main known environmental stimulus for spring migration (superimposed on an endogenous rhythm) is increasing daylength which promotes extra feeding, fattening and migratory restlessness at appropriate dates for the population concerned (Rowan, 1926; Farner & Follett, 1966; Lofts & Murton. 1968; Wolfson, 1970; Dawson et al., 2001; Ramenofsky et al., 2012). In species that moult in spring, this is also initiated by increasing daylengths, as is gonad growth, each process occurring in appropriate overlapping sequence through the season. As in autumn, migratory birds can also respond to daylengths encountered on their journey. Captive Stonechats at spring migration time were exposed to two different photoperiodic regimes, one typically experienced during migration through the temperate region (fast change) and the other typical of lower latitudes (slow change). These differences were small and short-term, but they had immediate and longer-term effects on the birds (Helm & Gwinner, 2006). Slow-change migrants (mimicking African conditions) continued migratory activity longer than fast-change migrants (mimicking European conditions). The slow-change birds also delayed the growth and subsequent regression of their testes, moulted and developed autumn migratory activity later in the year. These longer-term effects were appropriate if the slow-change birds had started spring migration at more southern latitudes than fast-change birds, in Africa as opposed to Europe. In many species, gonad growth and sperm formation begin before the birds leave their wintering areas and continue during migration, while in others they begin during migration (for Eurasian migrants, see Rowan & Batrawi, 1939, Lofts, 1962, Bauchinger et al., 2007; for North American migrants, see Blanchard, 1941, Wolfson, 1942). Some species have been seen to copulate while on migration, and females have been found with sperm in their reproductive tracts (Quay, 1989; Moore & McDonald, 1993). This seems to be usual in geese, for example, which remain in pairs yearround, and in some populations, copulation and egg-formation begin even before the birds have left their winter quarters (McLandress & Raveling, 1983). Egg formation in these geese takes around 12 days, and laying can occur within a few days after arrival in nesting areas. In yet other species, most gonad growth occurs after the birds have arrived in breeding areas, and copulation is seen only after the establishment of a territory and subsequent pair formation. Much depends on the interval between arrival and egg-laying, which can span days or weeks, depending on the species and the ecological circumstances in which it lives. In general, it is in late-arriving species (relative to the latitude) that gonad development is most advanced on arrival, and in which the interval between arrival and egg-laying is shortest (Berthold, 1996). The relationship between spring migration and the development of breeding condition thus varies between populations, in line with the conditions experienced. In species that undergo a spring ‘pre-nuptial’ body moult into breeding plumage, this process also starts in winter quarters and proceeds through migration. However, its timing varies greatly between individuals seen together in the same wintering and staging areas. Among shorebirds at spring stopover sites, some individuals may be in predominantly winter plumage, while others at the same sites at the same time are in predominantly breeding plumage, with every intermediate. Much may depend on the latitude at which different individuals are headed to breed, with those nesting at the lowest latitudes (and hence arriving earliest) showing the most advanced moults. Nutritional conditions may also influence the timing and duration of this moult, accounting for some of the variations within populations. In support of this view, some free-living Swamp Sparrows (Melospiza georgiana) provided with extra food began their pre-nuptial moult earlier than usual (Danner et al., 2014). In preparing for spring migration, the effects of daylength may be modified by both temperatures and food supplies. For example, captive White-crowned Sparrows exposed to air temperatures increasing from 5 C to 26 C advanced the time of migratory restlessness compared with control birds held at constant low temperature (Lewis & Farner, 1973). And in a later experiment, gonad development was accelerated in birds on long days exposed to 20 C and 30 C (Wingfield et al., 2003). However, it is hard to tell whether temperature acted directly on these birds, or through its effect on their energy needs and the food available for reproductive development. The food available at stopovers can influence not only fuelling rates, but also gonad growth, as shown experimentally in Garden Warblers (Bauchinger et al., 2009). Among captives subjected to simulated stopovers, food was limited to one group and fed ad lib to another. The two groups showed no significant difference in body mass, but the well-fed birds showed greater testis growth, higher levels of testosterone in blood plasma and more behaviour typical of territorial and sexual contexts.

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As migrating birds approach their breeding areas, environmental cues become more reliable predictors of conditions at their destinations. Factors (such as daylength) that give fairly rigid timing in the earlier parts of the journey are likely to become less important during the course of migration, and other cues, such as temperature, habitat condition and food supply become more important, leading birds to more precisely time their arrival in breeding areas to match the local conditions.

Spread and consistency in spring departure dates within populations Migrants tend to leave particular wintering areas over a limited period of days or weeks, but in roughly the same period each year, some species or populations before others (e.g. King & Mewaldt, 1981). This holds in both obligate and facultative migrants. The year-to-year consistency in migratory timing within species is evident not just from field observations, but also from studies on captive passerines. In White-crowned Sparrows, for example, the standard error was 1.0 day for the mean date of onset of pre-migratory fattening during eight different springs in males kept outdoors in winter quarters (King & Farner, 1965; King, 1972). Among wild birds, however, subject to differing conditions, the situation is more variable, with poor feeding conditions slowing the rate of fattening and delaying departure (Chapters 14, 30). Nevertheless, departures are usually spread over a shorter period in spring than in autumn (Chapter 12), and individual year-to-year consistency in migration dates is greater in spring than in autumn (Box 13.2). In autumn, as explained above, wide variation in the departure dates from particular breeding areas results from wide variation in the dates that individuals finish breeding and are able to proceed on to moult or migration. In spring, for most species, there is no such prior activity that can delay departure, although in some, a late or slow moult might lead to delay (for Mallard (Anas platyrhynchos), see Dugger, 1997, for Barn Swallow (Hirundo rustica), see Van den Brink et al., 2000). Nevertheless, effects of weather and other variables on spring migration may be felt in wintering areas and at almost any point on route (Chapter 15). Some bird populations have shown considerable year-to-year variation in the progress of spring migration. For example, the mean passage dates (5capture dates) of male Eurasian Blackcaps through Israel over seven springs varied between 6 April and 3 May, and in late years the spread in passage dates was also less, as was the difference in mean dates between the sexes (Izhaki & Maitav, 1998a). In general, as found in many localities, species that migrate earliest in spring show more spread in their passage or arrival dates, and bigger variation in mean passage or arrival dates between years than species that migrate latest in spring (e.g. Francis & Cooke, 1986; Hagan et al., 1991). The growth in tracking studies has provided measures of the consistency (or otherwise) in the migration dates of the same individuals in different years. In some species, individuals may vary by no more than a few days in their departure or arrival dates from one year to the next, although in the population as a whole, these dates may be spread over several weeks (e.g. Battley, 2006). Such individual consistency could be due to inherent differences in migration timing between individuals, or to other differences between them, such as quality of winter territories or abilities to feed and fatten. Measures of year-to-year consistency in various aspects of migration are nowadays quantified as ‘repeatability values’ (Box 13.2, Figure 13.4). A widespread finding has been that, in spring, individual adults migrate at fairly consistent dates from year to year, with birds arriving early in one year arriving early the next year (Chapter 15). In long-distance migrants, a spread in departure dates from wintering areas does not necessarily result in a similar spread in arrival dates on breeding areas. Birds encounter different conditions on their journeys, and early birds are more likely to be delayed by poor weather or food supply, enabling later ones to catch up with them. In Red Knots (Calidris canutus), which migrate in spring from Tierra del Fuego to arctic Canada, departures from successive stopover sites become progressively more concentrated, so that from Delaware Bay, the last staging site before the breeding areas, almost the entire population leaves within a 3-day period, usually 28 30 May (Baker et al., 2004). In this species, then, the spread in departure dates from wintering areas is reduced along the migration route, so that most birds arrive in breeding areas within the same few-day period. It is as though migration schedules get tighter and more compressed as birds get nearer to their breeding areas, as noted also in other waders (Farmer & Wiens, 1999; Battley et al., 2004). Evidently, a ‘calendar effect’ may operate in spring, as well as in autumn, affecting the timing and extent of fattening, and the duration of stopovers, altogether speeding up the migration of late birds. To give some spring examples, the fattening rates of Red Knots in Delaware Bay increased by two or three times between mid-May and late May (Atkinson et al., 2007), while in semi-palmated Sandpipers (Calidris pusilla) passing through South Carolina, stopover durations decreased, and fat levels increased, as spring progressed (Lyons & Haig, 1995). Similarly, in Sedge Warblers studied on spring stopover in southern Israel, late birds gained weight faster and to a greater extent than earlier birds (Yosef & Chernetsov, 2004), and White-throated Sparrows departing from their Florida wintering areas late in the

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BOX 13.2 Repeatability of individual migration dates. Researchers had often noticed that, in particular breeding populations, certain birds always return earlier in the arrival sequence than others. The degree of consistency in the arrival or departure dates of individuals in different years is often quantified by use of repeatability (r) estimates. Originally developed for use in genetic studies, r values describe the degree of variation within individuals in relation to the degree of variation between individuals. Values of r less than 0.2 are regarded as reflecting slight repeatability (consistency in year-to-year dates), r between 0.2 and 0.4 low repeatability, r between 0.4 and 0.7 moderate repeatability, and r of 0.7 and higher as high repeatability. A review involving adult breeders of 47 species examined the timing of four key stages of the annual migration cycle (dates of departure from wintering area, arrival at breeding areas, departure from breeding area, and arrival at wintering area) (Franklin et al., 2022). The range of values obtained for these species was unexpectedly wide, ranging between 0 in some species to more than 0.9 in others in all four measures. Overall, the individual repeatability of all these timings across the 47 species averaged 0.414 (95% confidence interval: 0.3 0.5), confirming that consistent individual differences in migratory timings are common among birds. The date of departure from the wintering area was more repeatable than the dates of arrival or departure from the breeding areas. This was consistent with the findings that variable conditions encountered on migratory journeys can disrupt the degree of consistency in arrival times, and that the variable end to breeding activities has a major influence on departure dates from breeding areas (see text). Greater consistency in departure dates from wintering areas presumably arises in most birds through relative lack of any preceding or prevailing events likely to interfere with these departures. In the same analysis, no significant differences in repeatability values were found between land birds (18 species), waterbirds (14 species) or seabirds (15 species), or between the sexes. Nor were significant differences found between measurement methods (satellite-based or geolocation), numbers of individuals studied or numbers of measurements per individual. For some species, repeatability values have also been calculated for the actual routes taken by migrants in different years and the sites occupied in breeding and wintering ranges (Lo´pez-Lo´pez et al., 2014; Vardanis et al., 2016; Watson & Keren, 2020). Some species followed essentially the same route in different years (high repeatability) and others rather different routes (low repeatability) to their breeding or wintering localities. Some striking feats of memory became evident in some satellitetracked birds which took the same routes in successive years, even to the extent of repeating apparent mistakes. For example, a Lesser Spotted Eagle (Clanga pomarina) in successive autumns took the same diversion off its route and back again, which added an apparently unnecessary 500 km and 2 3 days to its migration (Meyburg et al., 2002). This bird seemed to have remembered and repeated the same unnecessary detour from one year to the next. Repeatability values as calculated above have their limitations. In particular, because each r value is a comparative measure of the degree of intra-individual variation in relation to the degree of inter-individual variation, each value is affected by the other (Conklin et al., 2013; Dingemanse et al., 2022). With a given amount of intra-individual variation, the r value would rise with increase in the amount of inter-individual variation. In addition, many existing r values are based on small samples studied over a small period of years; some are based on calendar dates of arrival and others on standardized dates in relation to an annual mean; some combine sex or age groups, while others separate them. Some based on birds tagged in wintering areas include birds nesting at different localities, or even at different latitudes, which could influence the degree of inter-individual variation in arrival and departure dates. It is not surprising, then, that estimates of repeatability values have varied widely between different populations of the same species, and within the same population at different times (four estimates of r values for the arrival dates of Black-tailed Godwits (Limosa limosa) in their breeding places ranged between 0.18 and 0.51, Gunnarsson et al., 2006; Gill et al., 2014a,b; Lourenc¸o et al., 2011). For studies of individual consistency in timing, therefore, it may often be more telling to revert to the old method and calculate for each individual within a given area the actual dates of departure or arrival in different years, or their individual dates in relation to the annual population means, leaving aside the amount of spread between individuals which is influenced by different factors.

150

Year 2 (Day from 1 Jan)

120 330

140 110

310

130 100

290

120 Male Female

270 270

310 290 330 Year 1 (Days from 1 Jan)

90

90

110 100 110 120 Year 1 (Days from 1 Jan)

110

120 130 140 150 Year 1 (Days from 1 Jan)

FIGURE 13.4 Correlation between the timing of particular events in consecutive years in Wood Thrushes (Hylocichla mustelina) nesting in Pennsylvania and wintering in Central America. Lines show 1:1 relationships. Modified from Stanley et al. (2012).

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migration season accumulated more fat than those that left earlier (Johnston, 1966). All these changes would have served to accelerate the migration of ‘late’ birds within populations, but whether through an inherent response to daylength (time of year) or a response to increased food supply in late spring remains uncertain.

Different populations of a species wintering in the same area Different species wintering in the same area, and hence subject to the same daylengths and other conditions, may start their migrations at different dates, weeks or sometimes months apart, depending on the distance they have to travel and the dates their breeding areas become fit for occupation (for shorebirds, see Piersma et al., 1990). Such differences are also found in different races (or populations) of the same species wintering in the same area, as shown for Whitecrowned Sparrows in California (Blanchard, 1941) and Yellow Wagtails (Motacilla flava) in tropical Africa (CurryLindahl, 1958, 1963). Although exposed to the same winter conditions, the members of the various races differ in the dates at which their gonads develop, and at which they accumulate fat and depart for breeding areas (Blanchard, 1941; Curry-Lindahl, 1963; Fry et al., 1972). Such differences were confirmed experimentally in two races of Dark-eyed Juncos, which showed different threshold responses to the same regime of increasing photoperiods (Singh et al., 2021). In general, in these northern hemisphere species, races that breed furthest south are first to leave, and those that breed furthest north are last. Thus, in the Yellow Wagtail, the earliest to leave their shared wintering areas in spring is the southern race M. f. feldegg, then M. f. lutea, followed by M. f. flava and M. f. flavissima, and finally M. f. thunbergi. These various races arrive in their breeding areas in the sequence that they leave, spanning the period March June, from south to north. Inherent differences in endogenous rhythms could explain such population differences, as could inherent differences in the threshold daylengths required to trigger departure. Either mechanism could account for how birds of different races can leave their shared wintering area in appropriate sequence and reach their respective breeding areas (at different latitudes) at appropriate dates. However, the Yellow Wagtails are the more remarkable because several races winter together on the equator, where daylength is constant year-round. In these birds, endogenous control seems essential, with different races responding differently, according to where they breed, and setting their ‘internal clocks’ before they reach the equator, so as to leave at appropriate dates some months later. Another example of differential population departure dates was provided by Curlews (Numenius arquata) wintering in the Dutch Wadden Sea which were tracked on spring migration (Schwemmer et al., 2021). Individuals that were first to leave this area stopped in breeding localities at 58 N, while those that were last to leave continued for another 10o further north, departing and arriving three weeks later. Birds using intermediate breeding areas were intermediate in% their migration dates. However, such trends are not universal, for in Eurasian Woodcocks (Scolopax rusticola) wintering in Italy, the opposite held, and birds with the furthest to go left first (Tedeschi et al., 2020). Endogenous influence on migration timing is supported by the observation that the onset of spring migratory restlessness in caged warblers in Europe coincides with the spring departure of conspecifics from their equatorial wintering grounds (e.g. Gwinner, 1968). Captive migrants spontaneously resume spring migratory activity after a winter rest, even when kept under constant daylengths. Moreover, different species or different races of the same species kept under identical captive conditions reach breeding, moulting or migratory condition at different dates appropriate to the latitude at which they breed (for Phylloscopus warblers, see Gwinner, 1972). It seems that the seasonal timing of winter events in equatorial or trans-equatorial migrants is mainly accomplished by the involvement of an endogenous timing mechanism, as discussed in Chapter 12, but gonad growth is also activated under constant or shortening daylengths, as expected in equatorial or austral conditions (Hamner & Stocking, 1970; Bluhm et al., 1991). Among populations wintering in the temperate zone, endogenous control would seem less important after the winter solstice than in equatorial regions, because in the same area in the temperate zone, different wintering populations could respond to different threshold daylengths, so that they left in an appropriate sequence. However, an endogenous influence, or an ability to separate increasing from decreasing days, would still be necessary in the temperate zone to prevent such birds from returning northward under the same daylengths in autumn that stimulate northward migration in spring.

Return migration from variable wintering areas In many bird species, the migrants from particular breeding areas can winter over a wide span of latitude and daylength regimes. For example, Eurasian Siskins breeding in the northern boreal forest of Western Europe may winter anywhere between mid-Sweden and Morocco, a latitudinal span of about 30 degrees, and the same individuals may winter at widely separated places in different years (Newton, 1972). The general pattern in such species is that return migration begins earliest from the most distant (southern) parts of the wintering range, and latest from the most northern parts.

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This sequential withdrawal from lower to higher latitudes can be spread over many weeks. For example, in the Redbreasted Nuthatch (Sitta canadensis) in North America, the last birds withdrew from the southern parts of the wintering range, in northern Florida (30 N), as early as 21 February, from North Carolina (35 N) by 24 March, from West Virginia (38 N) by 28 April, and from Pennsylvania (41 N) by 15 May (Harrap & Quinn, 1996). Progressive withdrawal in spring from a latitudinal span of 11 degrees was thus spread over a period of about 12 weeks, or 7.6 days later per degree northward. In wintering White-crowned Sparrows in western North America, the date of onset of premigratory fattening also varied linearly with latitude, averaging 3.3 days later for each degree of latitude northward. By implication, withdrawal was spread over seven weeks from the 14 degrees of latitude involved (Figure 13.5, Table 13.2; King & Mewaldt, 1981). In experiments on Pied Flycatchers, captive males exposed to winter daylengths typical of southern Europe began pre-nuptial moult, migratory activity and gonadal maturation about one month earlier than control birds held under the normal African photoperiods (Coppack & Both, 2002; Coppack et al., 2003). Because spring daylengths are longer in southern Europe than in tropical Africa, these flycatchers presumably perceived the date as being later than it actually was, so they prepared earlier than usual for migration. In addition, captive Garden Warblers kept in winter in photoperiodic conditions found at latitude 20 S (i.e. longer but decreasing daylengths) initiated gonad growth and migratory activity significantly earlier than conspecifics held under a shorter and more constant equatorial photoperiod (Gwinner, 1987). Such a built-in response to photoperiod not only regulates the normal date of migration, but could enable birds to react appropriately to location changes between winters. Overall, evidence from both field and laboratory indicates that, within populations, the timing of spring fattening and departure are latitude-specific and, at any one wintering latitude, fairly consistent between years. Whatever the endogenous influence, therefore, individuals must react appropriately to whichever daylength regime they find themselves under at the time. In some long-distance migrants, part of the population winters north of the equator and another part south of the equator. Even the same individuals may winter north or south of the equator in different years. Among some radio-tagged White

FIGURE 13.5 The median dates (1/ 2 5 days) of onset of spring premigratory fattening in White-crowned Sparrows (Zonotrichia leucophrys gambelii) wintering at different latitudes in western North America. Regression analysis indicates a delay of 3.3 days, on average, for every additional degree N of latitude. From King and Mewaldt (1981).

TABLE 13.2 Pre-migratory fattening in White-crowned Sparrows (Zonotrichia leucophrys) wintering at different latitudes in relation to aspects of photoperiod. Although birds fattened at widely different dates at different latitudes and had experienced different total amounts of daylight since the winter solstice, the mean daylength between the solstice and start of fattening was about the same in birds from all latitudes. Mean wintering latitude ( N)

Days of start of premigratory fatteninga

Cumulative daylight hours from winter solsticea

Mean daylength (hours) from winter solstice to the start of migratory fatteninga

32.3

68

707

10.39

34.2

74

766

10.35

37.4

84

866

10.31

46.5

115

1200

10.43

a From 21 December (winter solstice), only one possible date which birds might use as an anchor point. From King and Mewaldt (1981).

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Storks, one individual wintered at various localities between 10 N and 30 S over four different years, each time returning successfully at an appropriate date to its nesting site in central Europe (Berthold et al., 2002). One female, tracked on return migration in six different years, set off, on average, around 24 February in four years when she was at 29 34 S, but about 18 days later, on average on 14 March, when she was at 3 S 4 N. She took an average of 75 days over the 11,000 km longer journey, arriving on 24 April 28 May in different years, and an average of 57 days over the 7000 km journey, arriving on 25 April 25 May in different years. There was no significant difference in arrival dates, according to length of journey (Berthold et al., 2004). Similar patterns were noted in Black-tailed Godwits (Limosa limosa) breeding in the Netherlands, some of which wintered in West Africa and others in Iberia. The West African birds started migration earlier than the Iberian ones, so that both arrived in breeding areas at about the same date (Kentie et al., 2017). While daylength response may reduce the delay in dates of arrival in breeding areas among birds wintering furthest away, it may not eliminate it altogether. Among eight radio-tagged Willow Ptarmigan (Lagopus lagopus), autumn migration distances and spring arrival dates were correlated, the furthest migrating individuals arriving back latest in spring (Gruys, 1993). Similar positive correlations between migration distance and spring arrival and egg-laying dates were found in tracked Savannah Sparrows (Passerculus sandwichensis) breeding in eastern Canada (Woodworth et al., 2016), in Pied Avocets (Recurvirostra avosetta) breeding in Germany (Ho¨tker, 2002) and various other species elsewhere (Chapter 31). So it seems that while many species have adjusted to variable wintering areas, making an appropriately earlier start from more distant locations, others have not, and individuals migrating longer distances suffer the penalty of later arrival, namely poorer breeding (Chapter 15). Possibly competition for wintering areas nearest the colony forces some birds to winter further way, or alternatively, some species may not have fully adjusted to a changed distribution.

Relationship between the internal rhythm and prevailing daylength All northern migrants wintering north of the equator set off on their spring journey in conditions of increasing daylengths, whereas those wintering south of the equator set off under decreasing daylengths. Flexibility in wintering areas within species again implies the importance of an internal clock in influencing the timing of spring departure, for outside the breeding season individuals may be exposed to markedly different daylength regimes from year to year. If these birds use some aspect of daylength to calibrate their internal clocks, they must do so in their breeding areas, at a latitude which they occupy consistently from year to year. Because birds can measure daylength, the longest day (at the summer solstice) could provide a useful baseline against which any internal clock could be re-set, but so far as I am aware, this possibility has not been tested. Despite the use of an internal clock as the primary timer, birds must presumably also respond to prevailing daylengths in order to adjust the timing and speed of migration to their particular wintering latitude, as explained above.

RELATIONSHIP BETWEEN SPRING ARRIVAL, BREEDING AND AUTUMN DEPARTURE In long-distance migrants that raise only a single brood each year and then leave for wintering areas, the timing of arrival in breeding areas can influence the timing of all subsequent events up to post-breeding departure (Chapter 12). This is because the breeding cycle, consisting of egg-laying, incubation and chick growth, is of fairly constant duration, both from bird to bird and from year to year. Thus in springs, when birds arrive early in their breeding areas, they can usually breed earlier and depart earlier in late summer, the whole sequence of events being affected by spring weather (Nisbet, 1957; Sokolov & Payevsky, 1998; Sokolov et al., 1999). Moreover, in years of widespread breeding failure in arctic-nesting shorebirds and others, the post-breeding migration occurs much earlier than usual, as mentioned above. Consider some specific examples. The Common Swift (Apus apus) migrates soon after breeding, postponing moult for winter quarters. Each pair leaves Britain within a few days after raising its brood. In this species, the date of departure is clearly determined primarily by the completion of breeding, which is in turn influenced by the date in May when breeding starts (Lack, 1956). Since the latter is influenced by temperature, the mean date of departure of Swifts in August depends on the weather in the preceding May. More recently, year-to-year correlations between spring arrival or laying dates and autumn departure dates have been noted in northern Europe in the Bluethroat (Luscinia svecica), Willow Warbler, Arctic Warbler P. borealis, Pied Flycatcher and Little Bunting (Emberiza pusilla), among others (Ellegren, 1990; Sokolov et al., 1999). Again, the implication is that in such single-brooded obligate migrants, autumn departure dates depend not so much on environmental conditions at the time, but on the completion of previous events in the annual cycle, whether the end of breeding or

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moult in adults or the end of growth or moult in juveniles, as the case may be. In line with this, the timing of peak autumn migration in different years at Rybachi on the Baltic coast was related to the preceding April temperature in 15 species examined, emerging as statistically significant in five such species (Sokolov et al., 1999). In none of these species was the timing of autumn migration related to local temperature at the time. Such close coupling between the timings of spring and autumn migration would not be expected in birds that can raise more than one brood each year, nor in some facultative migrants in which individuals may linger in breeding areas well beyond the end of moult in autumn when food is plentiful.

DEFERRED RETURN TO BREEDING AREAS In some long-lived bird species, individual migrants leave their natal areas in their first autumn and do not return in the next spring, but only in a later one, when they are two or more years old (up to four years in Bristle-thighed Curlews (Numenius tahitiensis), Marks & Redmond, 1996). These young birds either remain in their ‘wintering’ areas yearround over one or more years, or they may return only part-way towards the breeding areas or they may visit the breeding areas for only a small part of the breeding season, migrating later in spring and earlier in autumn than older birds. They perform both migrations in less hurry than the breeding adults, and at more favourable times. Such patterns are shown by various raptors, seabirds, shorebirds and others in which individuals do not breed until they are several years old (Chapter 18). Most of the first-year shorebirds that stay in ‘wintering areas’ show no sign of pre-migratory fat deposition or spring moult into breeding plumage, but remain light in weight and in well-worn winter plumage until the next post-breeding’ moult in late summer into new winter plumage. In other individuals, “pre-breeding” moult and fattening are much delayed, sometimes into July, too late for the birds to breed that year (McNeil et al., 1994). Lack of both weight gain and “pre-breeding” moult was apparent among juvenile Curlew Sandpipers (Calidris ferruginea) in South Africa, among Turnstones (Arenaria interpres) in Scotland, and among Western Sandpipers (Calidris mauri) in Panama, while adults wintering in the same places began moult, accumulated body fat and left in spring in the usual manner (Elliott et al., 1976; Metcalfe & Furness, 1984; O’Hara et al., 2002). Although the birds that stay year-round in “wintering areas” may skip the “pre-breeding” moult into summer plumage, they undergo the late summer “post-breeding” moult up to several weeks earlier than do adults returning from breeding areas. Turnstones over-summering in England moulted seven weeks earlier than adults returning from their arctic nesting grounds (Branson et al., 1979), and Western Sandpipers over-summering in Panama moulted 3 4 weeks earlier than returning adults (O’Hara et al., 2002). They provide examples of birds moulting at a more favourable time of year when not constrained by breeding to a less favourable time later in the year. Interestingly, while juvenile Western Sandpipers wintering in Panama remained there through their first summer, other juveniles wintering in Mexico, nearer their breeding areas, returned to the breeding range in their first spring (Lank & Nebel, 2006). The failure of immatures to migrate, or their tendency to return later and travel shorter distances than adults, might result from inability to obtain enough food and accumulate fat at the same rate as more experienced adults (Chapter 18). Alternatively, it might result from an inherent, endogenous response that matures with age, leading birds of some species not to return to nesting areas in their earlier years or to visit nesting areas only to prospect for suitable sites but not to breed. Resolving these questions must await more research, but whatever the answer, endogenous factors are presumably involved in initiating moult and movements at appropriate dates, at least in birds that winter in equatorial or opposite-hemisphere regions. A proximate factor of possible importance is the reproductive state of the individual at the time of spring migration. This migration may be triggered only when the bird achieves reproductive capability, with high levels of gonadal hormones, at two or more years of age (similar to the attainment of hormone-dependent breeding plumage in some species). In first-year gulls and others, the testes develop only partially in the first year of life, and not until late in the breeding season (for review, see Lofts & Murton, 1968). After their first nesting attempt, most individuals of species showing deferred maturity evidently return to breeding areas every year, or miss only occasional years, as judged by the annual recurrence of marked individuals at their usual nest sites (Chapter 19).

CONCLUDING REMARKS In several respects, migration differs markedly between the two seasons. In autumn, birds leave their breeding areas under decreasing daylengths as conditions are deteriorating. In moving toward lower latitudes, they generally meet more clement conditions (except where they have to cross a large area of sea or desert). In spring, by contrast, most

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birds leave their same-hemisphere wintering areas under increasing daylengths, when conditions are improving or at least benign. In moving towards higher latitudes, they generally encounter progressively worsening conditions; and are often held up by bad weather. Environmental conditions, and the appearance of food supplies at particular latitudes, may have much more influence on the progress of migration in spring than in autumn (Chapter 15). The birds themselves are also in different physiological states at the two seasons. In autumn, the migrants travel with regressed gonads, and in spring with growing gonads, which leads to seasonal differences in hormonal states, which may in turn influence aspects of the migration, including direction (see above). In some species, patterns of fat deposition, routes taken, flight lengths and speeds of travel also differ in a consistent manner between the two seasons. For reasons of physiology, experience and external conditions, therefore, the spring journey differs from the autumn one. Even captive birds behave differently at the two seasons: for example, caged White-crowned Sparrows show more intense nocturnal restlessness in spring, but over a shorter period of days than in autumn (Ramenofsky et al., 2003). At least some of the differences in migratory behaviour and fattening patterns observed in many species between autumn and spring are evidently under endogenous influence and presumably have an adaptive basis. Study of the proximate control of bird migration has revealed the crucial role of increasing daylengths in spring and to a lesser degree of decreasing daylengths in autumn in triggering preparation for migration. Changing daylengths also influence the rate of fattening and other events, leading to a general speeding up of processes later in a migration season. Although this may have costs, the benefit in autumn is in minimizing delay in the departure of late birds from breeding areas, as conditions deteriorate. In spring, the benefit is in minimizing delay in the return of late birds to their breeding areas, a delay often reducing breeding success (Chapter 15). While the primary control is by daylength (operating on an underlying endogenous rhythm), secondary factors are also involved, notably food supplies which influence the rate at which fat can be deposited, and previous events in the annual cycle which, if running late, can delay the onset of fattening and migration. A late moult in summer (in turn caused by late breeding) can delay departure from breeding areas, while (in fewer species) a late or slow moult in winter can delay departure from wintering areas. If birds had greater freedom in migratory timing, they would presumably avoid the hurricane seasons, which span the main autumn migration period in several parts of the world. Weather does, however, influence the actual dates of flights within the migration seasons (Chapter 4), and possibly also the routes taken, which often differ between autumn and spring, in line with seasonal differences in prevailing winds or feeding conditions (Chapter 24). In addition, the immature non-breeders in some species have greater freedom in migratory timing than breeding adults and tend to migrate later in spring and earlier in autumn, when conditions are better. By implication, it is mainly the need to breed at the best time of year that constrains migration to occur at somewhat less favourable times. Because individuals in the same population migrate at widely different dates within a season, they inevitably encounter different conditions on route. Changing wind conditions, for example, may cause individuals from the same area to take different routes, to spend different times over their journeys, experience different fuel needs and sometimes end up in widely separated wintering areas (Chapter 25). This variation can in turn influence their over-winter survival and subsequent breeding performance, an aspect developed in later chapters.

SUMMARY In obligate migration, all main aspects are viewed as under firm internal (genetic) control, mediated by daylength changes, giving a high degree of consistency in timing, directions and distances of movements from year to year. For the most part, each individual behaves in the same way year after year (except for immatures in species with deferred breeding). In contrast, facultative migration is viewed more as a direct response to prevailing conditions, especially food supplies. Within a population, the proportions of individuals that leave the breeding range, the dates they leave and the distances they travel, can vary greatly from year to year, as can the rate of progress on migration, all depending on conditions at the time. The same individual may migrate in some years but not in others. In general, obligate migration occurs in populations whose food supplies in breeding areas are predictably absent in winter, whereas facultative migration occurs in populations whose food supplies in breeding areas vary greatly from one winter to another, according to weather or other variables. Obligate and facultative modes can be regarded as opposite ends of a continuum, with predominantly internal control at one end and predominantly external control at the other. In addition, many migrants may change from obligate to facultative mode during the course of their journeys. An endogenous programme influences the time course (and hence distance) of autumn migration among obligate migrants. Evidence for endogenous control has come from findings that (1) the timing and duration of migratory restlessness in captive birds resembles the temporal pattern of migration in free-living birds; (2) populations which migrate over different distances show corresponding differences in the amount and duration of migratory activity in cages (and

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hybrids show intermediate patterns); and (3) experimental interruption of migration or migratory restlessness is not subsequently compensated for. These findings apply primarily to juveniles on their first journey and do not necessarily hold in experienced adults returning to a known area. In many species, departure dates from breeding areas on autumn migration are spread over periods of up to several weeks, because they are influenced by variations in the dates that individuals finish breeding and (in some species) moulting. Adult passerines breeding until late in the season also start moulting later, but earlier with respect to the stage of a nesting cycle, and replace their feathers more rapidly than earlier birds, thus minimizing the delay in autumn departure. Similarly, young produced late in the season moult at an earlier age, and more rapidly than earlier hatched young, again reducing the delay in their migration. Late birds also begin fattening before the end of moult and may migrate more rapidly. As confirmed experimentally, this acceleration in development in late birds is triggered by the shortening daylengths of late summer and autumn. Preparation for spring migration appears to be influenced primarily by daylengths in association with an endogenous rhythm, the latter being particularly important in populations wintering in equatorial and opposite hemisphere regions. The spread in departure dates between individuals wintering in the same area may be attributable partly to inherent differences between them, but also in some species to variations in completion of winter moult, and in their feeding and fattening rates. Adverse weather can cause further delays. In some single-brooded populations, the dates of arrival or egg-laying in spring influence the dates of autumn departure because, with a breeding cycle of roughly constant length, early arrival (or egg-laying) allows early departure. Post-breeding departure dates in such populations thus depend more on preceding spring weather than on current autumn weather. This does not necessarily hold in multi-brooded populations in which finishing dates bear no consistent relationship with starting dates. In some bird species with deferred maturity, individuals remain in wintering areas and do not return to breeding areas until they are two or more years old; other individuals may return part-way towards breeding areas, or may visit breeding areas only for a short time each year, leaving wintering areas later and returning earlier than breeding adults. Mechanisms that control the occurrence and timing of migration in such species during the early years of life await study.

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Chapter 14

Stopover ecology

Pallas’ Warbler (Phylloscopus proregulus), a rarity in Western Europe, is most often seen on stopover When weather turns unfavourable, birds settle on the coast which is deluged with thousands of migrant birds, which pile up in such immense pyramiding concentrations that every bush and tree in some areas is sometimes crowded with birds. George H. Lowery, 1951.

For most birds, stopovers make up most of the time spent on migration and account for almost all the variation in the duration of migration found within populations. Birds may break their journeys for various reasons and for varying periods; they may or may not feed at the time, and they may lose or gain body reserves. Birds normally spend stopovers in habitats similar to those they occupy at other times. Key questions concerning stopovers are why birds break their flights when they do and why they set off again when they do. Both decisions could be influenced by external factors such as prevailing weather, local habitat and food supply, and by internal factors such as the physiological condition of the bird at the time. External factors are relatively easy to assess, but internal ones are less so. Miniaturized bio-logging devices are beginning to provide information from birds in flight, and perhaps one day we may have data on the state of a bird day by day through its journey on such features as time in flight, level of tiredness1, sleep patterns, metabolic rate, heart rate, body temperature and so on. But for the time being, most relevant information comes from birds trapped on stopovers which can be weighed, tested and monitored until they leave. For several reasons, birds would be expected to vary in their response to external factors. They may differ in the risks they are prepared to take, depending on species and terrain to be crossed. For example large waterfowl with their waterproof plumage, which are able to settle on the sea in emergencies, might be less deterred by poor weather for oversea flights than, say, small songbirds. Secondly, small short-lived species with high reproductive rates (r-selected) might react to particular conditions differently from large, long-lived species with low reproductive rates (K-selected). For short-lived species, getting to the breeding area on time may be more important than for long-lived species likely to have many more breeding opportunities ahead of them (Schmaljohann et al., 2022). On this basis, r-selected species might be more prone to accept risks to breed at the next opportunity, whereas K-selected species might act to delay migration and miss a breeding opportunity to lessen their mortality risk. So in risk-taking, most birds would be expected to fit somewhere on a continuum between these extremes. Age may also play a role, if only because, on average, older birds are likely to have less life ahead of them than younger ones, which may therefore be expected to show more risk1. In ourselves the term ‘tiredness’ usually refers to the need for sleep and recovery from physical or mental exertion. Whether birds feel tired in the same way as we do is an open question, but birds can clearly endure much longer periods of unbroken exercise and sleeplessness than any mammal can as many birds can stay on the wing for several days at a time. The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00022-1 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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averse behaviour perhaps breaking their flights to rest and re-fuel more often than older birds, or requiring better weather conditions in which to migrate. Thirdly, a distinction has been drawn between birds that act to migrate as quickly as possible (time minimizers) and those that act to migrate as cheaply as possible (energy minimizers) (Alerstam & Lindstro¨m, 1990; Chapter 5). For all these reasons, we can expect that conditions leading to stopping and re-starting on migratory journeys will not be the same for all species, for all individuals within a species, or for different points in their journeys. Different flight modes, notably flapping or soaring, also require somewhat different weather conditions, the latter particularly thermals or other updrafts. Taking all these considerations into account may well account for some of the varying results obtained in studies of stopover behaviour, as discussed below.

BREAKING THE JOURNEY In theory, a flying bird might come to land because of the time of day (getting dark in the case of diurnal migrants, getting light in the case of nocturnal migrants), the appearance of a barrier (such as a water crossing) or traditional refuelling area, or a deterioration in weather (wind or rain). All such external factors may encourage a bird to break its journey, as may internal factors such as depletion of fuel reserves, and the need for rest, food or drink or re-assessment of position, if this is easier when stationary than on the wing (Chapter 11). Any of these factors could bring a migrating bird to ground, and their alleviation could enable the bird to set off again and continue its journey. While some stopovers may therefore be ‘planned’ ahead of time, as when waterfowl and waders migrate between traditional re-fuelling areas, other stopovers may be facultative (taken in some circumstances but not others), and yet others are enforced by unfavourable weather. Observations and tracking studies suggest that many birds break their journeys without feeding, stopping overnight (diurnal migrants) or in daytime (nocturnal migrants). Some of these stops last no more than a few hours. Other stops involve feeding to replenish body reserves and can vary in duration depending on the reserves required (with longer stops and bigger reserves needed before crossing a barrier such as sea or desert). In any case, departure normally depends on suitable weather, with delays caused, for example by rain or strong headwinds. One obvious function of some stopovers is to sit out bad weather, and for soaring species, this can mean any conditions which inhibit the development of thermals, whether cold, wind or rain (see Mallon et al., 2021 for Turkey Vultures (Cathartes aura)). One little-studied aspect of stopover is the assumed need for rest (Chapter 3). The fact that birds often sleep soon after arrival (as seen frequently in waders and waterfowl) suggests that the need for rest is important (Schwilch et al., 2002b; Battley et al., 2001a; Aborn & Moore, 2004; Ba¨ckman et al., 2017). Other types of physiological restoration could also occur at stopovers, including recovery from muscle damage, from oxidative damage (resulting mainly from fat metabolism and reduced anti-oxidant activity) and from reduced immune function sometimes incurred during long flights (Guglielmo et al., 2001; Owen & Moore, 2008; Skrip et al., 2015; Eikenaar et al., 2020). But whether these types of damage are sufficient to cause birds to break their journeys or are simply repaired when birds stop for other reasons is as yet unknown. Another possible factor that could cause migrating birds to land is the need to drink, for although birds produce metabolic water during long flights, this may be insufficient to meet their needs (Chapter 6). Also, because birds sometimes fly at altitudes that may be cold enough to cause hypothermia, or through hot environments sufficient to cause hyperthermia, some stopovers may serve to restore normal body temperature, or at least to prevent it from straying dangerously low or high (Chapter 3). Birds on brief rest stops behave differently from those intent on re-fuelling (Moore, 2018). Typically, resting birds are less specific in their habitat choice than feeding birds, and individuals of normally territorial species make no attempt to establish a territory. They are in flight mode rather than in feeding mode, and it may be more energyefficient to move on while reserves last than to reconstruct digestive machinery and start to feed again before this becomes necessary. When birds do remain to feed, they may eat much less than usual and put on weight more slowly on the first day or two than subsequently, supposedly because of the time taken to re-build the digestive system to work at full capacity (Chapter 5; Klaassen & Biebach, 1994). If flight muscles are overly reduced in mass (as seen in occasional individuals), this reduction in flight capacity can hinder escape from predators, as shown for nutrient-depleted Dunlins (Calidris alpina) subjected to attacks by falcons (Bijlsma, 1990), and for lean Northern Wheatears (Oenanthe oenanthe) which fell prey to Sparrowhawks (Accipiter nisus) more often than heavier ones (Dierschke, 2003). These lean birds may have been feeding hard to recover condition but at the expense of vigilance. At some places, birds pause for extended periods of up to 2 3 months, much longer than they need to re-fuel, which is normally achieved rapidly near the end of their stay. The birds apparently make no attempt to re-fuel until conditions dictate that they should move on. Big numbers of birds may assemble at regular ‘staging areas’ every year; some species may moult there, and in some instances, such stops are followed by a change in migratory direction. Such

Stopover ecology Chapter | 14

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stationary periods are now recognized in many species. In some they have been regarded merely as long stopovers on migration and in others as being the first of two or more successive wintering areas, depending mainly on their location on the overall migration route. These long stops have been known in Palearctic-Afrotropical migrants for more than 50 years (Moreau, 1972; Jones, 1985) and have more recently come to light in some Nearctic-Neotropical species. They occur mainly in autumn, but in some species also in spring (eg see Chapters 26 28). It seems, then, that some migratory stops involve little more than rest or sleep for less than a day with no significant re-fuelling; others involve stopovers of several days for re-fuelling, while yet others last up to several weeks and involve more than re-fuelling. These different categories of stopover are sometimes hard to separate because in practice birds show a continuum in stopover durations and weight loss or gain. Different types of migration strategies, and their associated stopovers, are encapsulated in the notion of ‘hop, skip and jump’ systems, discussed in Chapter 5 (Piersma, 1987a,b). Be aware that many authors, in their calculation of stopover periods using data from tracking devices, have included only days when the bird did not migrate. This clearly greatly underestimates time on the ground, as the bird may fly for only part of each day. Nocturnal migrants, in particular, could in theory fly and feed hard every 24 hour period through their journeys, if local conditions were suitable.

IMPORTANT RE-FUELLING AREAS Previous lack of distinction between these different types of stopover led to the perceptions that most migratory landbirds use numerous re-fuelling sites during any one journey, that birds can stop almost anywhere with appropriate habitat, and that at the population level migration occurs as a continuous stream. This may hold true for some species, especially short-distance diurnal migrants travelling through favourable terrain and feeding on route. But recent tracking studies on a range of long-distance migrants have shown that individuals often make long stopovers at just one to four key staging areas along their overland routes, at each of which they accumulate large energy reserves (Bayly et al., 2017). The same sites are used year after year by large numbers of birds and seem important in the migrations and persistence of the populations concerned. This type of migration, with few regular stopover sites, is well-known in some shorebirds, geese and cranes, and in Europe and North America, many such re-fuelling sites are now protected as nature reserves. For smaller birds of forest and other widespread habitats, hints at the existence of such locations within Europe have come from ring recoveries (see below), and from tracking studies, with birds making long flights between small numbers of key places. In tropical regions, these places are only now being identified, and virtually none are protected. They can vary from relatively small sites of less than 100 km2 to larger regions of 100,000 km2 or more. Ring recoveries have revealed variations in the migration strategies of Eurasian-Afrotropical migrants, along with some major staging areas (Wernham et al., 2002). Some species ringed in Britain, such as Eurasian Reed Warbler (Acrocephalus scirpaceus), Common Whitethroat (Sylvia communis) and Sand Martin (Riparia riparia), have provided recoveries widely scattered through southern France and Iberia, implying that these species stop almost anywhere in these parts of their journeys towards Africa. In other species, however, the recoveries are heavily concentrated in specific regions, with few or none elsewhere: Pied Flycatchers (Ficedula hypoleuca) and Tree Pipits (Anthus trivialis) in western Iberia, Lesser Whitethroats (Curruca curruca) in the Alps region of northern Italy, and Wood Warblers (Phylloscopus sibilatrix) in peninsular Italy. These latter patterns suggest that these species migrate in a single long flight from their breeding areas to specific regions in the southern half of Europe, and from there they may travel without other long pauses to sub-Saharan Africa. Their journey could thus be completed in two long ‘jumps’, separated by a single long stopover for replenishment of body reserves. This view is generally supported by other data from Britain, such as the pre-departure body weights of birds, or their appearance or lack of appearance at coastal bird observatories. Some of the same species have different re-fuelling areas on the return journey, and individuals are seen (and rings recovered) in much greater numbers in North Africa in spring than in autumn (Chapter 6). Similar patterns have been described from trans-Saharan migrants breeding in Fenno-Scandia, as illustrated in Figure 14.1 (Fransson et al., 2005). From these breeding areas, Thrush Nightingales (Luscinia luscinia) and Common Whitethroats were recovered almost entirely on the Egyptian coast during autumn migration, whereas Barred Warblers (Curruca nisoria), Eurasian Blackcaps (S. atricapilla) and Lesser Whitethroats were recovered mainly in a region embracing Israel, Lebanon, and parts of Jordan, Syria and Turkey. Willow Warblers (Phylloscopus trochilus) were recovered in both regions. Trapping activities take place through all these regions, and the different recovery patterns again imply that different species have different major re-fuelling regions on route to winter quarters. Localized fuelling has long been known in species with restricted habitat areas, such as some waterfowl and shorebirds, but is more surprising in small birds that seem to have lots of suitable habitat distributed along their migration routes. Perhaps again, at migration times only parts of this habitat may provide food abundant enough for fuel deposition. However, these

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The Migration Ecology of Birds

FIGURE 14.1 Recoveries of birds ringed in northern Europe that were found in the eastern Mediterranean region. Lines connect the ringing and recovery sites for each individual. Left. Thrush Nightingale (Luscinia luscinia). Right. Eurasian Blackcap (Sylvia atricapilla). These are two of seven passerine species which migrate from northern Europe around the eastern Mediterranean in autumn for which there are sufficient ring recoveries for analysis. From Fransson et al. (2005).

staging areas are large, covering thousands of square kilometres, and birds from different parts of the breeding range may use different regions for stopover, as shown, for example by Lesser Whitethroats from Britain (stopping in northern Italy) and those from northern Europe (stopping in the Middle East). The existence of these major re-fuelling areas does not of course prevent the birds from breaking their journeys at other sites if tiredness, hunger or weather intervene. The examples from ring recoveries discussed above are largely restricted to Europe because ringed birds tend not to be reported from most of Africa. However, data from tracked birds have shown the importance of particular localities for re-fuelling there (Figure 14.2). Examples include the Red-backed Shrikes (Lanius collurio) which, in migrating between southern Scandinavia and southern Africa, used two major staging areas in southeast Europe and northeast Africa on the outward journey, and two on the return journey in eastern Africa and southeast Europe respectively (Tøttrup et al., 2012). Similarly, Common Cuckoos (Cuculus canorus) tracked from breeding sites in southern Scandinavia used three main staging areas on both outward and return migrations to Central Africa, but different areas for the two journeys (Figure 14.2; Willemoes et al., 2014). For spring migration, tracking studies have shown that some species stage in the woodland zone of West Africa, apparently fuelling there before travelling north across the Sahara

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Common Cuckoo

Red-backed Shrike

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Thrush Nightingale

FIGURE 14.2 Maps showing major staging and wintering areas in the migrations of three species from Scandinavia to sub-Saharan Africa, as determined by tracking studies. Modified from Thorup et al. (2017).

˚ kesson et al., 2012; Jacobsen et al., 2017; for Common Cuckoo, see Willemoes (for Common Swift (Apus apus), see A et al., 2014; Hewson et al., 2016). Eurasian Nightjars (Caprimulgus europeus) use the same zone further east in central Africa (Norevik et al., 2019a), and even further east, the Horn of Africa may serve the same purpose for several species. This woodland zone is where rain falls earliest after the preceding dry season, as the rain belts move from south to north of the equator (Chapter 26). Similarly in the New World, studies on several tracked species have revealed some major re-fuelling sites. For example, Veeries (Catharus fuscescens) made multi-day stopovers in three main regions, the south-eastern United States, northern Colombia and the northern Amazon, when on route from Delaware to the southern Amazon basin (Heckscher et al., 2011). In a different study, Veeries at the Colombian site accumulated sufficient fuel in an average stopover of nine days to fly 2200 km, enough to reach their Amazonian wintering areas (Bayly et al., 2012). Bobolinks (Dolichonyx oryzivorus) used fewer regions still, with many birds making one long stopover in the Llanos (grasslands) of Venezuela and Colombia, while travelling between North American breeding areas and South American wintering areas (Renfrew et al., 2013). Tree Swallows (Tachycineta bicolor) from widely separated breeding areas also shared a long autumn stopover in Louisiana before moving on to their wintering areas (Laughlin et al., 2013). Further west, the funnel-shaped geography of Central America concentrates millions of migrating raptors at several points in the Colombian Darie´n and Panama, Costa Rica and southeast Mexico. Again, it is important to distinguish between restroost stops lasting less than 24 hours and multi-day re-fuelling stops, and growing numbers of studies show individual birds making long stops in just a few strategic areas. As shown by tracking studies, several species migrating from North to South America make prolonged stopovers in the Sierra Nevada de Santa Marta (Colombia) and the Yucatan Peninsula (Bayly et al., 2017). The Sierras form a high and isolated mountain range, offering a wide range of habitats near the coast in northern Columbia, which comprise ideal fuelling areas for birds about to cross the sea in spring to North America. Grey-cheeked Thrushes (Catharus minimus) pausing at this site for around two weeks in spring were found to accumulate enough body reserve to fly more than 3000 km, in some individuals far enough to reach their breeding areas in eastern Canada (Go´mez et al., 2017). Other evidence for specific re-fuelling areas comes from Wood Thrushes (Hylocichla mustelina) and Red-eyed Vireos (Vireo olivaceus) which enter North America in spring through a narrow span of longitude in Louisiana, the same region as used by Tree Swallows in autumn (Stutchbury et al., 2009; Stanley et al., 2012; Callo et al., 2013). Some re-fuelling areas are used in both spring and autumn, and others at only one of these seasons. One-season use arises because migration occurs on different routes at the two seasons (as in loop migrants), or because some sites offer suitable feeding conditions at one season but not at the other. For example Bewick’s Swans (Cygnus columbianus bewickii) use the White Sea as a stopover site in spring but not in autumn (through poor re-fuelling rates then; Beekman et al., 2002), and over the years Barnacle Geese (Branta leucopsis) have reduced their use of Baltic stopover sites on spring migration (in parallel with declining fuelling rates and increasing predation risk there; Jonker et al., 2010). Seabirds migrating entirely over the sea would seem to have plenty of opportunities to pick up food on route. But this is not always the case. Many species breeding at high latitudes migrate over the equator, and tropical seas are

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The Migration Ecology of Birds

BOX 14.1 Mixed foraging strategy shown by Cory’s Shearwaters (Calonectris borealis) on migration. From Dias et al. (2012). Many migrating seabirds linger in areas of rich food supplies, but others rely on picking up food on the way. Cory’s Shearwaters tracked on migration did both, but mainly adopted a ‘fly-and-forage’ strategy, similar to that seen in some raptors and hirundines. Through the use of dynamic soaring, these shearwaters attained high overall migration speeds and were able to travel thousands of kilometres without making major stops. They spent around 50% of their time flying, but seldom for more than four hours at a time, migrating more by day than by night, but longer during times of full moon. But in more than 100 migration tracks recorded over a 4-year period, stopovers in nutrient-rich areas were recorded on about 60% of outward journeys, but in no return journeys to breeding areas. By picking up food while on migration, Cory’s Shearwaters proved able to fly distances of 13,000 km or more without major breaks. They modified their daily schedules when crossing nutrient-poor waters, and travelled more slowly on the post-breeding journey (average 429 km/day) than on the pre-breeding journey (average 644 km/day), with a final sprint to the nesting colony. On autumn migration, about 10% of tracked shearwaters detoured more than 5000 km from the main migratory pathway to spend 15 31 days in the nutrient-rich Evlanov area around the northern mid-Atlantic Ridge where they presumably built up body reserves. Clearly, individuals varied in both their migration routes and fuelling strategies.

notoriously poor in food. In any case, foods such as fish tend to be concentrated in particular localities, which are few and far between (Chapter 8). Evidence is accumulating that, like some landbirds, some seabirds re-fuel at traditional staging areas before continuing migration. After breeding in Western Europe, Black Terns (Chlidonias niger) assemble at one major feeding area, the IJsselmeer on the Dutch coast. Here they increase in body mass by 25% 30% within 2 3 weeks, enough for them to fly non-stop over 3600 km to West Africa. The birds ascend in the evening to high altitudes ( . 500 m) and fly by night. Although Black Terns are seen at localities on route, no important stopover site is known between the IJsselmeer and West Africa (Van der Winden, 2002). In Namibia, a similar increase in body mass of these terns was noticed just before spring migration. Other terns may also make long flights between regular rich feeding areas, rather than hunting as they travel. Recent tracking studies have revealed the locations of many major refuelling areas used by pelagic seabirds, often associated with up-currents which ensure an abundance of food (Chapter 8). Other seabirds travel on mixed strategies, picking up some food on route, and also stopping for long periods in known rich feeding areas (Box 14.1). Some stopover sites are used by many species, some of which come together at no other time of year. Ecological segregation, based on the usual factors of body size, bill structure and dietary choice, is likely to reduce competition between species for resources at stopover sites, as is temporal occurrence, as different species and populations may pass through at different times, consistent from year to year. How much this temporal segregation results from the need to avoid competition, as opposed to other considerations such as differences in breeding time, is an open question.

RESUMING THE JOURNEY Much research has centred on the question of what encourages birds to stay longer at a particular stopover site or what stimulates them to move on, accepting that some aspects of behaviour may vary with the type of bird (and especially its body size), and between ‘energy minimizers’ and ‘time minimizers’. In general, energy minimizers would be expected to accumulate small reserves and make short flights between frequent fuelling stops. Time minimizers would be expected to adopt the same strategy in conditions of abundant stopping places offering rapid fuelling rates, but to accumulate large fuel reserves and make long flights where stopping places offering rapid fuelling rates were few and far between, as described in Chapter 5 (Alerstam & Lindstro¨m, 1990). The same species may show different behaviour in spring and autumn, or at different stages of the same journey, according to the terrain to be crossed. But once on the ground, the first problem for a re-fuelling migrant is to find habitat rich enough in food to make this possible. Many freshly arrived nocturnal migrants can be seen moving around at dawn. Their short movements have been interpreted as attempts to find good feeding sites, as have some short-distance night-time flights (Lindstro¨m & Alerstam, 1986; Moore, 2018). Freshly arrived migrants are sometimes in poor condition, with low-fat reserves (Chapter 30, Bairlein, 1985a,b; Biebach, 1985; Salewski & Schaub, 2007), but they usually replenish their reserves during stopover (Alerstam & Lindstro¨m, 1990), and the size of the reserves or their rate of accumulation typically affects when they leave a stopover site. Many studies have measured weight gain (mostly fuel deposition), migratory restlessness and directional preferences of captive birds as they approach migration time, while other studies have examined the weight and directional preference of wild birds trapped on stopover sites and tested at night in orientation cages. In general, once birds that had arrived lean

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had accumulated expected levels of migratory fat, they showed both increased migratory restlessness and expected directional preferences (Berthold, 1996, 2001; Yong & Moore, 1993; Sandberg et al., 1998, 2002; Schmaljohann et al., 2011). Expected levels of migratory fat depended on species and stage of journey, as some species started migration with high levels of fat, while others started with lower levels but increased them on successive stopovers as they reached a sea or desert barrier (Chapter 5; Odum et al., 1961; Schaub & Jenni, 2000). For birds about to cross such barriers, only high-fat reserves were found to trigger departure in the appropriate direction (Berthold, 1996; Piersma & Gill, 1998; Schaub & Jenni, 2000; Battley et al., 2000; Schaub et al., 2008, Chapter 5). In addition, birds that were migrating relatively late in the season often accumulated fat to greater levels and migrated more rapidly than earlier birds (Ellegren, 1993; Lindstro¨m et al., 1994; Fransson, 1998; Schaub & Jenni, 2000; Paxton & Moore, 2017; Chapter 12). The importance of food availability at stopover sites is shown by the following types of findings, drawn from a range of different studies: 1. Freshly arrived birds were more likely to stay at sites where food was plentiful and move on rapidly from sites where food was scarce (Bibby & Green, 1981; Spina & Bezzi, 1990; Ottich & Dierschke, 2003). 2. Re-fuelling rates (as judged by weight gains) were found to vary from place to place and time to time, according to prevailing food supplies (Box 14.2, Figure 14.3; Bibby et al., 1976; Bibby & Green, 1981; Cherry, 1982; Piersma, 1987a,b; Prop & Deerenburg, 1991; Bayly et al., 2019). 3. Mean stopover durations varied with food supplies, as birds put on weight more slowly where food was scarce than where food was abundant (Figure 14.3; Piersma, 1987a,b; Russell et al., 1994; Bayly et al., 2019). 4. Birds that arrived at particular sites with low body reserves stayed longer than those that arrived with larger reserves (Dolnik & Blyumental, 1967; Cherry, 1982; Bairlein, 1985a; Biebach, 1985; Biebach et al., 1986; Moore & Kerlinger, 1987; Dunn et al., 1988; Serie & Sharp, 1989; Loria & Moore, 1990; Ellegren, 1991; van Eerden et al., 1991; Kuenzi et al., 1991; Morris et al., 1996; Yong & Moore, 1997; Cohen et al., 2014). 5. Lean birds of some species, apparently desperate for food, fed more rapidly, using a wider range of techniques and feeding places, than birds with residual fat stores (Loria & Moore, 1990). They thus restored their energy levels sooner than otherwise possible (Wang & Moore, 2005). 6. Birds in some places could not accumulate body fuel for spring migration until local food availability increased in some way (for Eurasian Whimbrel (Numenius phaeopus), see Zwarts, 1990).

BOX 14.2 Foraging and migration of European Nightjars (Caprimulgus europeus). From Norevik et al. (2019a). European Nightjars are long-distance migrants which forage on the wing at night but only in conditions light enough for them to see their prey (flying insects). Their foraging is therefore greatly affected by the phase of the moon. Birds tracked on migration between Europe and Africa were found to double their daily foraging activity during moonlit nights, apparently taking advantage of light-dependent fuelling opportunities. This resulted in clear cyclicity in the intensity of migratory movements, and at times all the 39 tracked birds migrated simultaneously following periods of full moon. In this species, therefore, cyclic influences from the moon acted as an important regulator of the migratory progress of individuals and synchronized them to give marked pulses of migration, driven by cyclicity in foraging opportunities another demonstration of the role of food supplies in influencing migratory progress.

FIGURE 14.3 Relationship between food supply (aphids) at a stopover site: (left) tendency to stay; and (right) rate of migratory weight gain in Sedge Warblers (Acrocephalus schoenobaenas). From Bibby & Green (1981).

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7. Fuel deposition rates declined in rain or other conditions expected to reduce feeding rates (Farmer & Wiens, 1999; Schaub & Jenni, 2001; Davis et al., 2005; Krapu et al., 2006). 8. The provision of supplementary food to wild migrants led to increased rates of weight gain compared with unfed birds (for Bluethroat (Luscinia svecica), see Lindstro¨m & Alerstam, 1992; for Common Whitethroat, see Fransson, 1998; for European Robin (Erithacus rubecula), see Da¨nhardt & Lindstro¨m, 2001; for Garden Warbler (Sylvia borin), see Bauchinger, 2002; for Eurasian Reed Warbler (Acrocephalus scirpaceus), see Bayly, 2006). Some of the highest fuelling rates recorded involved birds receiving additional food. 9. Rates of fuel deposition most commonly reported in field studies (1% 3% of lean mass per day) were much lower than the maximum rates ( . 7% of lean mass per day) recorded from individuals in the same population. This finding implied that most individuals fed at rates too low to fuel at the maximum possible rate (Lindstro¨m, 2003). For 1 3 days after arrival at a re-fuelling site, migrants often did not gain weight and sometimes even lost weight. This was most obvious in migrants arriving after a long flight and may have been due to their need to re-build the digestive tract to work more effectively, as mentioned above (Chapter 6). Moreover, at some study sites, fattening rates were reduced by competitors feeding on the same food supplies (Hansson & Pettersson, 1989; Moore & Yong, 1991; Dierschke, 2006), or by disturbance from predators or human hunters, which sometimes caused birds to leave a site earlier than expected. For example in a study in central Finland over several years, the numbers of Mallards (Anas platyrhynchos) and other ducks fell by more than 90% just after the start of the hunting season. Most birds left the area completely and any remaining birds were concentrated in protected areas (Va¨a¨na¨nen, 2001). Similarly, mass departures of Greylag Geese (Anas anser) from Norway occurred in the first few days of hunting and were ascribed to the disturbance involved (Follestad, 1994). Probably most of these birds would have soon left anyway, but hunting was sufficient to trigger their departure prematurely. Moreover, geese subjected to human hunting at spring stopover sites accumulated lower body reserves and subsequently showed lower breeding success than undisturbed birds (Chapter 30). Instances are also known of shorebirds reducing their use of re-fuelling areas subject to increasing human activity (such as Plymouth Beach in Massachusetts, Pfister et al., 1992), and of Western Sandpipers (Calidris mauri) in British Columbia reducing their stopover durations and fuel loads over a period of years as Peregrine Falcons (Falco peregrinus) increased in numbers there (Ydenberg et al., 2004). In the same area, Western Sandpipers avoided places of experimentally increased predation risk (Pomeroy et al., 2006), and in southern Sweden finches preferred areas where their fuelling rates were lower but attacks from predators less frequent (Lindstro¨m, 1991), while more widely in the Baltic region Barnacle Geese Branta leucopsis reduced their use of stopover sites as the numbers of predatory White-tailed Eagles Haliaetus albicilla increased (Jonker et al., 2010). Findings such as these raise the likelihood that increased predator presence could change the behaviour of migrants on route, with birds staying longer and accumulating more body reserves where the risks of predation were low, and staying for short periods and accumulating only small reserves where these risks were high, providing that appropriate stopping places were available elsewhere on the route. The opposite situation was observed in Denmark where the creation of reserves in which hunting was banned led to marked delay in onward migration and to big increases in the numbers of birds present at one time, both hunted and non-hunted species (Chapter 30; Madsen, 1995). Some species were present for up to several months longer than previously, and increases of up to 20-fold were recorded in individual species. While birds can readily adjust their behaviour in response to the presence of predators, they are unlikely to be able to detect and react to pathogens and parasites in the same way. By the time a bird feels the effect of a pathogen or parasite, it is too late. Assuming that the chance of a bird encountering a pathogen increases with the number of localities visited, the best way a bird might lessen this risk is to reduce the number of stops on route, in other words, adopt a high fuel load/long flight strategy. So while predation risk is deemed to favour an energy-minimizing strategy with frequent stops, disease risk should favour a time-minimizing strategy with few or no stops on route. Obviously, if a bird is sick, it is unlikely to leave on migration. In this context, an interesting result emerged from a study of Red Knots (Calidris canutus) that were flown non-stop for six days in a wind tunnel to mimic migration (Hasselquist et al., 2007). The long flights had no detectable effects on immune responses or corticosterone levels. So flight performance per se may not have been particularly stressful or immunosuppressive in these Knots. However, some individuals refused to fly for extended periods. Before flights started, these non-flyers had significantly lower antibody responses against a test pathogen (tetanus) than the birds that carried out the full flight program. This suggested that only birds in good physical condition may be willing to take on heavy exercise. Similarly, in several species caught on stopover, immune function was low on arrival but improved as body reserves increased over the following days (Owen & Moore, 2008; Eikenaar et al., 2020). In other words, immune capability seemed related to body condition and could be lost and regained during the course of a journey.

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FIGURE 14.4 The relationship in Northern Wheatears (Oenanthe oenanthe) caught on Heligoland Island between the change in fuel load from capture to the third morning in captivity and the change in migratory restlessness from the first to the third night after capture (n 5 42). Migratory restlessness was expressed as the number of 15-minute periods in a night during which a bird showed at least five activity counts. Modified from Eikenaar & Schla¨fke (2013).

40 Change in migratory restlessness

285

30 20 10 0 R² = 0.22 P = 0.002

-10 -20 -0.3

-0.1 0.1 Change in fuel load

0.3

The finding from wild birds trapped on stopover that individuals with large fuel reserves showed more intense migratory restlessness than those with low reserves was as expected (Figure 14.4; Bulyuk & Mukhin, 1999; Fusani et al., 2009; Fusani et al., 2011; Eikenaar & Schla¨fke, 2013; Lupi et al., 2019). In other studies, birds were trapped and weighed, provided with supplementary food, and then equipped with radio transmitters or other devices to record their departure under natural conditions (Schmaljohann & Dierschke, 2005; Smith & McWilliams, 2014). Birds with the greatest fuel reserves soon left the area, while light-weight birds remained longer to fatten further (Bibby & Green, 1981; Cherry, 1982; Bairlein, 1985a, Loria & Moore, 1990; Sandberg & Moore, 1996a,b; Fusani et al., 2009; Goymann et al., 2010; Eikenaar & Schla¨fke, 2013; Smith & McWilliams, 2014; Cohen et al., 2014; Deppe et al., 2015; Woodworth et al., 2015; Schmaljohann & Klinner, 2020). In one experiment, Red-eyed Vireos were trapped as they were about to cross the Gulf of Mexico in autumn. Each was weighed and tested for directional preference. It was then fitted with a small light stick, released on its own 1 2 hours after sunset, and followed with binoculars until lost from view (Sandberg & Moore, 1996b). Before their release, significantly more fat vireos (81%) than lean ones (61%) showed migratory activity in cage tests. After release, all the fat birds flew out of sight in the migration direction. Some 38% of the lean birds stayed at their current location, and most of the others took a direction diametrically opposed to the migration direction. Similar results on the relationship between fat levels, inclination to migrate and directional preferences were obtained through release experiments using European Robins and Pied Flycatchers (Sandberg et al., 1991), Swainson’s Thrushes (Catharus ustulatus) (Sandberg et al., 2002), and Northern Wheatears (Schmaljohann et al., 2011), and in cage tests on Common Chaffinches (Fringilla coelebs) (Ba¨ckman et al., 1997) and Snow Buntings (Plectrophenax nivalis) (Sandberg et al., 1998). In general, the greater the level of stored fat, the more likely was the bird to show in the field or in test cages an appropriate preferred direction. Many lean birds preferred the opposite direction but temporarily reversed migration is not uncommon in the wild when birds encounter a sea coast or another barrier. They may be trying to find more ˚ kesson et al., 1996). profitable feeding areas away from the crowded coast (Chapter 4; A All these various findings confirm that the fat levels of a bird on migration influence both its tendency to depart on each leg of the journey and the strength of its directional preference. However, most of the above studies were conducted at localities where the birds were about to cross the open sea. The behavioural difference between lean and fat birds seemed less marked in birds migrating overland where feeding sites were frequent, and body condition had much less influence on stopover durations and departures. In several species faced with a flight through favourable terrain, departing individuals showed a wide range of fat levels, suggesting no specific level at which departure was triggered (Tsvey et al., 2007; Schaub et al., 2008). Such birds might then simply vary the length of their flights, according to their available fuel levels. Interestingly, Red-eyed Vireos showed both types of response at different seasons. When about to cross the Gulf of Mexico in autumn, only fat birds departed and showed appropriate directional preferences, as mentioned above, but in spring when birds had just crossed the Gulf and faced an overland journey, they left with variable and generally much lower fat levels, and regardless of fat levels they showed appropriate directional preferences (Sandberg & Moore, 1996b). In some situations, birds departing from a coastal site may have the choice of striking out overwater or moving further along the coast. Both options may get the bird nearer its destination, but the coastal route may prolong the journey. A bird’s choice may then be influenced by its body reserves or prevailing weather (Ru¨ppel et al., 2023).

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Change in the diurnal cycle The diurnal cycle of nocturnal migrants also changes as they accumulate migratory fat. Four songbird species were caught on stopover at an oasis in Algeria and kept in cages fitted with activity recorders (Bairlein, 1985a, 1992). Generally, lean birds were active only during daylight, feeding as normal. In contrast, fat birds remained inactive by day without feeding but became active at night when they would normally have migrated. Birds with moderate fat reserves fed during the day and were also active at night. Nocturnal migratory activity was thus clearly associated with fat levels. Birds vary in the time of night when they depart, which could influence the distance they could travel before dawn, and hence their overall migration speed (Mu¨ller et al., 2016, 2018). In various studies, under favourable weather, individuals with high-fat levels departed early in the night, often within the first hour after sunset. Long-distance migrants tended to depart before short-distance ones, and all birds departed earlier after sunset in spring (when nights were shorter) than in autumn (Sjo¨berg et al., 2017). In contrast, birds migrating with little fuel and under unfavourable wind showed great variation in their nocturnal departure times. Some of these birds may not have been setting off on migration, but on some more local movement, perhaps to find a better feeding area (see later). Weather changes during the night could also modify any intrinsic patterns.

Weather and other factors influencing departure Given appropriate fuel levels, weather conditions also influenced departures, as expected (Chapter 3). In many studies, birds were found to leave under falling temperatures in autumn and rising temperatures in spring (Dierschke, 2006; Sjo¨berg et al., 2015; Woodworth et al., 2015; Chapter 4). At both seasons, clear skies and following winds encouraged birds to leave, while clouds and headwinds often delayed them. However, some sites rarely offered optimal conditions, so birds then left in conditions that elsewhere would delay them. In addition, from the same sites, some birds were left under ‘worse’ conditions than others, apparently according to their intended journeys (Da¨nhardt & Lindstro¨m, 2001; Packmor et al., 2020). For example among two races of Northern Wheatears on Heligoland Island, birds of the race (O. o. leucorhoa) facing a long over-sea journey to Greenland departed only under optimal conditions, while birds of the race (O. o. oenanthe), heading northward through Europe left under a wider range of (mostly less favourable) conditions (Dierschke & Delingat, 2001). Many species have been recorded flying against headwinds, even in terrain where they could come to land (Chmura et al., 2020). In addition, among species that migrated in flocks, some individuals were apparently influenced in their departure times and routes by others (Chapter 3). Examples were commonest in waterfowl and cranes where young migrate with their parents, but have been described in other species too (Chapter 3; Dolnik & Blyumental, 1967; Flack et al., 2018).

Other findings Another interesting finding, derived mainly from tracking studies and already mentioned, was that not all birds that left a stopover site departed on migration. Some made shorter flights in directions different from the expected, with some moving back along the route. Studies showed these birds to be light in weight, so they could have been ˚ kesson et al., 1996; seeking better feeding areas before continuing their journeys (Lindstro¨m & Alerstam, 1986; A Sandberg & Moore, 1996a,b; Mills et al., 2011; Smolinsky et al., 2013; Stach et al., 2015). In the past, such birds could have been counted as departing on migration, underestimating their times spent on stopover, and in some cases, also underestimating their fuel load at departure. One tracking study showed that some of these shortdistance birds left at night so could easily be assumed to be continuing migration, although in this study they landed again within 30 km (Taylor et al., 2011). In effect, nearby places visited in quick succession comprise a single stopover, albeit embracing a larger-than-usual area. Some other differences between studies could be interpreted in terms of energy or time minimization. For it was not just the absolute levels of fat which influenced a bird’s behaviour but also the rate of accumulation (as expected on theoretical grounds, Alerstam & Lindstro¨m, 1990). The greater the rate of fuelling, the more likely a bird to stay to accumulate more fat and the greater its fuel load at departure, a good strategy for a ‘time minimizer’ (Bibby et al., 1976; Schaub et al., 2008; Schmaljohann & Eikenaar, 2017). These findings led to the notion that birds which could not fuel at the desired rate moved on quickly to search for other feeding sites; if they encountered sites with enough food, they re-fuelled at whatever rate was possible there, spending as long as necessary to accumulate the required reserves (Schaub et al., 2008; Schmaljohann & Dierschke, 2005; Schmaljohann & Eikenaar, 2017; Klinner et al., 2020). Hence,

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both light and heavy birds could leave specific stopover sites light birds to search for other feeding sites and heavy ones to continue migration. The finding that birds unable to accumulate body reserves move on rapidly agrees with laboratory findings, in which migratory restlessness of captives increased when food supply was reduced and body mass declined, decreased when abundant food was provided, but increased again when fat levels reached a threshold (Biebach, 1985; Gwinner et al., 1988). It also agrees with field studies showing that birds losing mass are likely to move on rapidly (Rappole & Warner, 1976; Kuenzi et al., 1991). What is less certain is the role of endogenous factors in influencing the time spent on major staging sites. The fact that birds stay at some sites, or at particular latitudes, much longer than they need to fatten, suggests the involvement of endogenous or photoperiodic influences. In addition, there are also circumstances in spring when birds may ‘get ahead of themselves’, if they arrive early at a staging site, and need to wait until conditions at the next site (including breeding areas) should have reached a condition suitable for occupation. This seems to apply particularly to the last major stopover before breeding areas, as is especially obvious in shorebirds and waterfowl. In this way, staging sites may also serve as waiting areas, enabling birds to adjust their migration schedules to meet optimal timing of arrival at their next destination (Peng et al., 2015).

Age and sex effects In many species, adults trapped at stopover sites put on weight more rapidly achieved greater body reserves, and stayed for shorter periods than first-year birds; and within age groups, males put on weight more rapidly, achieved greater body reserves, and stayed for shorter periods than females (for age differences see Serie & Sharp, 1989; Ellegren, 1991; Gorney & Yom-Tov, 1994; for sex differences see Morris et al., 1994; Otahal, 1995). These differences may have arisen because young birds were at a competitive disadvantage in the presence of older ones, and females in the presence of males. Juveniles may also have foraged less efficiently than adults, resulting in generally slower fuel accumulation and migratory progress, with longer or more frequent stopovers (for Gray Catbird (Dumetella carolinensis) see Heise & Moore, 2003, for Dunlin see Ro¨sner, 1990, for cranes and raptors see Ueta & Higuchi, 2002). In some species in which females are bigger than males, the sex-related difference in fuelling rates may be reversed, as females at particular sites had generally shorter stopovers (Figuerola & Bertolero, 1998; Butler et al., 1987). Such age and sex differences in feeding rates could influence the travel speeds, departure and arrival dates, and survival chances of individuals during migration. It is hard to tell how much they result from competition acting here and now at stopover sites, or from genetically-controlled age-linked and sex-linked differences in migration strategies that could have evolved as a result of competition and other differential selection pressures in the past. Sex differences in migratory timing were apparent in birds kept in identical conditions and fed ad lib in captivity, so were taken as genetically-controlled (Chapter 18; Coppack & Pulido, 2009). However, age and sex differences are not apparent in all species, or at all stopover sites (Morris et al., 1996; Maitav & Izhaki, 1994). Occasionally, juveniles are found to be heavier than adults on average (Butler et al., 1987; Alerstam & Lindstro¨m, 1990; Woodrey, 2000), possibly because juveniles migrate at a more favourable time of year (earlier in autumn or later in spring), so may have the advantage of a better food supply than adults.

CONCLUSIONS Given that birds have to break their migratory journeys to rest and feed or to avoid adverse weather, many factors influence how long they stay at a site, how much body reserve they accumulate, and when they move on. The fattening patterns of birds do not entirely conform to the simple model: arrive lean, fatten rapidly to a threshold, and then depart as soon as weather permits. Apart from appropriate body reserves and their rates of accumulation, the following external factors have been found to influence a bird’s likelihood to continue on migration from a stopover site: (1) geographical location on the migration route, and whether a short or long flight is next required; (2) the date in the season and level of urgency in moving on; (3) temperature trend, with birds more likely to leave under decreasing temperatures in autumn and rising temperatures in spring; (4) food availability and other site-specific factors, with birds more likely to depart quickly if fattening is difficult and to stay longer if fattening is easy; (5) recovery from ‘tiredness’ and other physiological consequences of endurance flight; (6) weather especially winds, cloud and precipitation; (7) presence of competitors and predators which can reduce feeding and fuelling rates, while predators also raise the risk of death; (8) social influences through which individuals may be encouraged by other birds to migrate earlier than they otherwise would or take somewhat different routes (Chapters 3,10). Internal factors, such as re-fuelling and restorative processes,

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are not necessarily additive in their effects on departure dates, as they can occur simultaneously, or while waiting for a weather change. Birds sometimes pause for longer than usual at the last major stopover on spring migration, as they wait for improving conditions to open their nesting areas. One of the striking findings from research at stopover sites is the extent to which similar studies, at different dates and places, have given strikingly different results. For example, within a population, birds with large fuel reserves would be expected to show a greater departure probability than those with smaller reserves. Many studies have confirmed this expectation, but others have shown no relationship between fuel stores and departure probability. Similarly, birds would be expected to depart in conditions with following winds, as this would minimize the time and energy needed for a journey. Again many studies have shown exactly this, but others have not, with some birds even leaving under strong headwinds, despite the greater costs and risks involved. The important point is that stopovers could have several different functions, and different migrants may stop when they do or resume migration when they do for different reasons. Moreover, the behaviour of any migrant depends on context, as each adjusts its behaviour to the combination of pressures that affect it at that time. Only in this way can we account for the different findings; for example, that some birds leave in conditions that would ground others, or that late in the season when birds could be pushed for time, they leave in poorer weather or poorer body condition than those that left earlier. Despite these many influences, there is nevertheless a minimum total number of hours that a bird must normally spend on stopover to gain the fuel necessary for its migratory journey (including the initial fuelling period). The faster the re-fuelling rate, the shorter the time the bird needs to spend on total stopover, and in theory, the shorter its overall migration time (Lindstro¨m et al., 2019). Through its influence on fuelling rate, food supply thus becomes the major external factor limiting migration speed, even though other factors, such as weather, may add to the time spent on fuelling, and slow the overall migration further. Different stopover sites offer different feeding conditions and predation risks, and may therefore differ in the proportion of the total fuel need that they provide. With the influence of feeding rate and other factors, total time spent on stopover is not normally a variable that birds can change at will (except perhaps in ambiguous cases where stopover provides more than re-fuelling and could be regarded as the first spell in a wintering area). The ultimate reasons why migrants may interrupt a migratory flight are to minimize either (1) an immediate fitness cost, which is the risk of mortality or physical injury or (2) a delayed fitness cost, which could include reduced reproductive success or lower survival probability at a later date, as carry-over effects. For instance, if a migrant takes shelter instead of flying through a thunderstorm, it has a better chance of surviving, giving an immediate fitness benefit. Alternatively, a bird that leaves a stopover under favourable weather but before accumulating ideal fuel reserves may be subsequently unable to breed, suffering a later fitness cost. But because we cannot normally measure the fitness consequences of particular behaviour, these ideas provide little more than aids to thought. The closest proxies to fitness measures are encapsulated in the optimization models of Alerstam & Lindstro¨m, 1990, updated by Alerstam, 2011 (Chapter 5).

SUMMARY For most birds, stopovers make up most of the time spent on migration, and account for almost all the variation in the duration of migration found within populations. The main reasons that birds break their journeys are to replenish their body reserves so that they can continue on migration, to rest or to sit out periods of unfavourable weather. Some birds may also come to ground to recover from dehydration, chilling or overheating. Birds accumulate body reserves appropriate to the journeys they have to undertake, with large reserves needed for long non-stop flights overseas or another terrain where feeding is not possible. The rate at which birds can accumulate body reserves varies with local food supplies, the local density of competitors feeding on the same resource, and the levels of disturbance caused by predators. Sometimes birds unable to gain weight, or harassed by potential predators, move to other feeding sites, even back-tracking along the migration route. Intense predation and disturbance, as caused by human hunting, sometimes lead birds to move further along their migration route earlier than they otherwise would, shortening their stopovers and, by implication, reducing their departure fuel loads. When tested for directional preferences, birds with appropriate body reserves are more likely to show appropriate preferred migration directions than are birds with smaller body reserves, inadequate for further migration. Several factors could lead a bird to break its journey, and similarly several factors (besides re-fuelling) could influence its resumption.

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Part 3

Large-scale movement patterns

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Chapter 15

Seasonal reoccupation of breeding and wintering areas

Canada Geese (Branta canadensis) on route to northern breeding areas. Every bird student has noted the feverish impatience with which certain species push northwards in spring, sometimes advancing so rapidly upon the heels of winter as to perish in great numbers when overtaken by late storms. Lincoln (1935a,b).

As winter ends, days lengthen and temperatures rise, migratory birds begin to move towards their breeding areas. One species after another spreads in wave-like manner towards higher latitudes, progressively re-settling areas vacated since the previous year. Birds establish territories and acquire mates in preparation for breeding. After young have been raised, they withdraw again, usually to lower latitudes where they spend the non-breeding period. These large-scale distributional changes enable birds to exploit the surge in fresh food supplies produced each spring and summer at high latitudes while avoiding the shortages of winter. Seasonal changes in the food supplies of birds are driven by seasonal changes in daylength and weather mainly by temperature at higher latitudes and by rainfall at lower latitudes. Seasonal changes ultimately influence how much of each year migrants can remain in their breeding areas without reducing their survival prospects. With increasing latitude, spring begins later and autumn begins earlier, shortening the growing season for plants, the activity season for insects, and the potential breeding season for birds. Away from the equator, the annual temperature cycle typically lags about 1 month behind the daylength cycle. In the northern hemisphere, while the longest day falls on 21 June, the warmest day in any particular locality falls, on average, around 21 July. Similarly, while the shortest day occurs on 21 December, the coldest day falls, on average, around 21 January (Preston, 1966). The peak dates of spring and autumn migration for various bird species at different localities in North America are shown in Figure 15.1. At each locality, the mid-date between spring and autumn migration dates averages around 17 July, the warmest time of year. The migrations of most bird species seem to hinge around the annual temperature cycle rather than around the daylength cycle. For it is the temperature cycle that, at high latitudes, has most influence on vegetation growth and bird food supplies. Within any one breeding area, the timings of spring arrival and autumn departure differ between species according to when their particular food supplies reappear in spring and collapse in autumn. In general, regardless of latitude, those species that arrive relatively early in their breeding areas depart relatively late, but exceptions occur (Figure 15.2). The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00012-9 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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FIGURE 15.1 Peaks dates of migration for (a) 18 species that pass each spring and autumn through Alaska at 64 50’N, (b) 18 species that pass each spring and autumn through Minnesota at 44 55’N, and (c) 33 species that pass each spring and autumn through Pennsylvania at 40 40’N, together with their bisectrix dates (midway between median dates of spring and autumn passage). Migration dates shown in black, bisectrix dates in grey. Note the vastly greater spread in migration dates than in bisectrix dates, and the greater spread in autumn than in spring dates. From: (a) Preston (1966), (b Winker et al. (1992), (c) Benson & Winker (2001).

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Moreover, the peak migration dates for different species at particular localities are spread over a shorter period in spring than in autumn (Figure 15.1), and within most species, spring arrival occurs over a shorter period than autumn departure (Chapter 14).

LATITUDINAL TREND IN THE TIMING OF SPRING The temperature of 10 C is often taken to indicate the start of spring conditions, suitable for rapid plant growth and insect activity. The spread of the 10 C isotherm from south to north through Europe is shown in Figure 15.3, based on the average figures over many years. This particular isotherm takes more than 3 months to spread north-eastwards through the whole continent, beginning in the southwest in February March and not reaching the northernmost areas until July. It also takes almost as long to spread from the lowest to the highest parts of mountain areas, such as the Alps. It gives a good indication of the timing of spring conditions, suitable for bird breeding, in different parts of the continent. Owing to continuing climate warming, the contour lines are gradually shifting northward, but the basic pattern of progressive north-eastward spread remains unaltered. The problem of using particular temperature values, like this, as a signal of spring’s arrival is that they take no account of previous temperatures and daylengths which may also have influenced plant and insect development. The alternative is therefore to use some biological measure of the timing of spring, and for this purpose, the dates of first apple flowering are often used. This measure takes more than 2 months to progress from the southwest to the northern limits of the apple in southern Scandinavia. But whatever measures are taken, they indicate that conditions become suitable for bird breeding in the northernmost parts of Europe at least 3 months later than in the south. The spread is even greater in North America which covers a greater span of latitude than Europe.

Seasonal reoccupation of breeding and wintering areas Chapter | 15

FIGURE 15.2 Relationship between median spring and autumn migration dates for various species in (a) Alaska (64 50’N, N 5 18); (b) Minnesota (44 55’N, N 5 18); and (c) Pennsylvania (40 40’N, N 5 33). In general, species that arrived early tended also to depart late, and vice versa. Regression relationships: Alaska, b 5 1.09, r 5 0.69, P , .002; Minnesota, b 5 0.61, r 5 0.43, P , .01; Pennsylvania, b 5 0.97, r 5 0.78, P , .001. Details from Preston (1966), Winker et al. (1992), Benson & Winker (2001).

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In recent decades, other measures of vegetation growth have been used in studies of bird movements. One is the socalled ‘normalized difference vegetation index’ (NDVI) which from satellites measures the intensity of greenness on the earth below (Box 15.1). This index has been used to follow the spread of spring vegetation growth in northern latitudes, and also the waves of vegetation growth that follow rain belts in Africa and other dry regions. Vegetation greening is important to all herbivorous animals, including birds and also the plant-feeding insects which serve as food for other birds. Greening in each locality is caused by the sudden growth of ground vegetation or leafing of deciduous trees. In its early growth stages, new plant tissue is rich in nutrients, notably easily digestible protein. As time progresses, and new plant tissue ages, its nutrient content and digestibility decline. So-called green waves also affect lakes and seas, as warming promotes phytoplankton blooms at successive latitudes, followed by zooplankton blooms which provide food for higher predators, including fish, and influence the timing of seabird breeding.

Species differences in spring migration dates The rates at which most bird species spread poleward in spring seem to be associated with the dates that their particular foods become available at successive latitudes. Migrating birds need food not only for daily maintenance but also to fuel successive stages of their journeys (Chapter 5). There would be no advantage in migrating birds getting ahead of their food supplies for they would then lose body reserves and might even have to turn back (as sometimes happens, Chapter 4). For each species, therefore, the timing of spring arrival at particular latitudes generally coincides with the re-appearance of appropriate food supplies, enabling their survival.

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FIGURE 15.3 The advance of spring, as shown by the dates that the rising 10 C isotherm reaches different parts of Europe. From T. H. Sparks, unpublished.

Because some types of food become available before others, different species arrive at particular localities in a fairly consistent sequence from year to year. Species which depend on spring thaw to release their food supplies (e.g., some waterfowl and waders) are some of the first to arrive, followed by those that depend on aerial insects (e.g., midges), and in turn by those that depend on larval insects from later-developing leaves (e.g., some warblers). Nectar-feeders are

Seasonal reoccupation of breeding and wintering areas Chapter | 15

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BOX 15.1 The NDVI as a measure of landscape greenness. The NDVI (normalized difference vegetation index) is a measure of the amount of greenness in a landscape, as assessed remotely from satellites. It ranges from 21 to 11. Negative values of NDVI (values approaching 21) correspond to water, and values close to zero (20.1 to 0.1) generally correspond to areas of barren rock, sand or snow. Low positive values are associated with grassland and scrub (approximately 0.2 0.4), and high values (approaching 1) with temperate and tropical forests. Importantly, this index changes as vegetation grows in response to rainfall or warmth and declines as vegetation dies in response to drought or cold, as at the onset of winter. NDVI values have provided good resolution over wide areas against which ecological responses to rainfall or temperature can be examined. Both these weather variables can have direct and indirect effects on plant productivity, plant tissue quality for phytophagous insects and other herbivores, and insect abundance, all of which may determine food availability for migratory birds. The term ‘Surplus NVDI’ is defined as the difference between NVDI values at the time of interest and either the annual average value or the annual minimum value, as stated.

even later, because they depend on the opening of flowers; and the spring migration of the Ruby-throated Hummingbird (Archilochus colubris) through much of North America is closely synchronized in successive localities with the peak flowering of Jewelweed (Impatiens biflora), a major source of spring nectar (Bertin, 1982).

RECOLONISATION PATTERNS In the first half of the 20th century, attention was given by observer networks to recording the northward advance of various bird species in spring (Figure 15.4). In general, earlier migrants took longer over the journey and spread north at a slower rate per day. Five African European migrants, namely the Barn Swallow (Hirundo rustica), Willow Warbler (Phylloscopus trochilus), Common Redstart (Phoenicurus phoenicurus), Wood Warbler (Phylloscopus sibilatrix) and Red-backed Shrike (Lanius collurio), arrived in southern Europe on progressively later dates averaging 13 February, 5 March, 15 March, 1 April and 1 April, respectively. They spread north through western Europe at average speeds of about 40, 46, 66, 70 and 88 km/day, respectively, and took 109, 88, 61, 45 and 45 days to get from the southern to the northern parts of their breeding ranges (Southern 1938a,b, 1939, 1940, 1941). Their northward progression generally kept step with particular isotherms (different isotherms for different species), but like the isotherms, their migrations tended to accelerate with distance northwards. Of these species, the Barn Swallow bred over the widest latitudinal range, and its period of spread over this range (109 days) roughly fitted expectations from the different indices of the northward advance of spring conditions, mentioned above. More recent studies in other parts of Europe have shown similar trends, with the species arriving latest in southern Europe making the fastest progress northward for six species travelling through Britain, see Huin & Sparks (2000); for seven species travelling from Italy to Sweden, see Jonze´n et al. (2006). Remember that these rates of spread refer to the dates that birds first appeared in successive localities and not to the movement speeds of individuals which can be faster, as revealed by ringing and tracking studies (Chapter 9). The relationship with particular isothermal lines, different lines in different species, presumably arises because temperature gives a good indication of the date at which each area becomes suitable for particular species to settle. The fact that the migratory advance is slower in colder springs is further indication of the importance of the development of a food supply. It does not necessarily mean that the species migrate in direct response to temperature, but rather in accordance with the development of their particular food supplies which temperature affects. In recent years, tracking studies have also enabled the progress of migration to be examined in individual birds. For 23 species of passerines and non-passerines that were tracked migrating between Africa and Europe, the time of arrival at breeding sites was c.1.5 days later for each degree northwards reflecting the later spring green-up at higher latitudes. The whole pattern was also 6 7 days later along the eastern flyway (through the east end of the Mediterranean) than along the western flyway (through the west end), reflecting the cooler conditions and later green-up at more eastern longitudes (Briedis et al., 2020). Similar trends have been found in North America (Lincoln, 1935a). Some species, such as Canada Goose (Branta canadensis), push north ‘on the heels of winter’ and keep step with the 35 F (3 C) isotherm, as advancing warmth melts the ice on lakes and rivers and creates bare ground for feeding (Lincoln, 1935a). In other species, such as Blackpoll Warbler (Seophaga striata), the northward movement occurs much later in spring and much more rapidly, often with increasing rapidity towards the northernmost breeding areas (Figure 15.4). Mean rates of advance in different North American species varied from about 30 km/day in the earliest species to 300 km/day in the latest, towards the ends of their journeys. This again parallels the rate of spring warming which gets progressively more rapid with advancing date and increasing latitude.

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(a)

(b)

(c)

(d)

FIGURE 15.4 The northward advance of various migratory bird species in spring. (a) Common Redstart (Phoenicurus phoenicurus) through Europe (Southern, 1939); (b) Barn Swallow (Hirundo rustica) through Europe (from Southern, 1938a,b); (c) Cliff Swallow (Hirundo pyrrhonota) through Central America into North America (Lincoln, 1935a); and (d) Blackpoll Warbler (Setophaga striata) through the Caribbean Region into North America (Lincoln, 1935a).

In recent years, the northward progression of summer migrants has been studied by more modern methods, involving mass participation through social media, to record the occurrence of bird species on continental scales on a daily basis. The most highly developed system so far is the ebird scheme in North America, established in 2002 by the Cornell Laboratory of Ornithology. One study, based on these data, enabled the spring recolonization and autumn decolonization of eastern and western parts of the continent to be examined over the years 2009 15, for various terrestrial bird species (La Sorte & Fink, 2017). The findings largely re-affirmed the patterns shown by earlier studies but

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provided more data for a much bigger range of species, with the potential to examine annual variation. It also showed that recolonization proceeded more rapidly on the eastern than on the western side of the continent. Further study of ebird data gave broad support for the role of vegetation greening in spring in a wide array of species (La Sorte & Graham, 2020).

Patterns within species With increasing latitude, as the annual warm season becomes shorter, many species spend progressively shorter periods in breeding areas, arriving later in spring and leaving earlier in autumn. The first individuals to arrive at successive localities in the breeding range are normally those that nest there, these settlers being followed by others heading for even higher latitudes. By the time that birds arrive at the highest latitude breeding areas, perhaps in late May or June, other individuals of their species at lower latitudes may already have young. In response to this low-to-high-latitude settling pattern, different races are seen to move through particular localities in sequence according to the latitude at which they breed. For example among American Yellow Warblers (Setophaga aestiva) migrating north through Arizona, the first birds to arrive in March and early April belong to the local breeding race (Setophaga aestiva sonorana). Races breeding further north do not arrive until late April, and the Alaskan race (Setophaga aestiva rubiginosa) does not until May June (Phillips, 1951). Similar differences occur among populations of White-crowned Sparrows (Zonotrichia leucophrys) (Blanchard, 1941), Yellow Wagtails (Motacilla flava) (CurryLindahl, 1963; Moreau, 1972), Eurasian Blackcaps (Sylvia atricapilla) (Klein et al., 1973), Pied Flycatchers (Ficedula hypoleuca) (Both & te Marvelde, 2007; Figure 15.5), European Golden Plovers (Pluvialis dominica) (Lamarre et al., 2021) and many others studied on passage, all arriving first in areas where breeding first becomes possible. Such temporal differences extend back along the migration route, and where several populations winter in the same region, those that nest at lower latitudes depart first, and those that nest at the highest latitudes last (Chapter 13). The temporal segregation of populations passing northward may have the additional effect of reducing competition between individuals from different populations, as they pass through the same areas at different times. If one watches passage migration at low latitude localities, species are found to differ not just in their mean passage dates but also in the spread of their passage dates, with some species taking much longer to move through than others. Typically, species with short passage periods are those that breed over a narrow span of latitude (with relatively small breeding ranges), whereas those with long passage periods breed over a wider span of latitude, giving a wider range of dates at which different localities become fit for occupation (for shorebirds, see Nisbet, 1957; for raptors see, Leshem & Yom-Tov, 1996).

Duration of residence Because of the shortness of the favourable season at high latitudes, populations that breed there remain for relatively short periods. This can be illustrated by the migration records from the Alaska Bird Observatory situated at 64 50’N, where the average frost-free period each year spans only 105 days (Benson & Winker, 2001). The six species of passerines that migrate there from within North America were present on their breeding areas for little more than this an average of 120 days or 33% of the year. The 12 species of passerines that migrate there from Central or South America were present for an average of only 91 days, or less than 25% of the year. These various estimates were based on the FIGURE 15.5 Median passage dates in spring through North Africa of Pied Flycatchers (Ficedula hypoleuca) breeding at different latitudes in Europe, based on information from ring recoveries. Populations passed through North Africa in order of their breeding latitude, south to north. From Both & te Marvelde (2007).

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TABLE 15.1 The number of days spent by five migratory species on their breeding areas at different latitudes in North America, calculated from the median dates of spring and autumn migration. Species

Alaska 

Minnesota

64 50’N

44 45’N

Grey-cheeked Thrush (Catharus minimus)

98

124

Swainson’s Thrush (Catharus ustulatus)

95

116

Northern Waterthrush (Seiurus noveboracensis)

86

113

Wilson’s Warbler (Wilsonia pusilla)

98

105

Blackpoll Warbler (Setophaga striata)

94

121

In addition to the above records, estimates were given for the Alder Flycatcher (Empidonax alnorum) of 48 days in Alaska and 73 days in S. Ontario at 40 42’N, and for the American Yellow Warbler (Setophaga aestiva) of 84 days in Alaska and 104 days in S. Manitoba at 50 1’N. Source: From Winker et al. (1992), Benson & Winker (2001).

intervals between the median spring and autumn migration dates, as assessed from the numbers of birds caught each day at the bird observatory. Comparable estimates of residence periods for the same species at lower latitudes were longer than in Alaska (Table 15.1). In Minnesota, at 44 55’N, 18 long-distance migrants remained for up to 105 days or less (compared to 91 in Alaska). Among five species that bred in both areas, the Minnesota birds stayed, on average, 22 days longer in their breeding areas than their Alaskan equivalents. The shortest periods in Minnesota of 95 days or less were shown by the Yellow-bellied Flycatcher (Empidonax flaviventris) and Least Flycatcher (Empidonax minimus), both of which left immediately after breeding (Winker et al., 1992). This pattern of longer residence in lower latitude areas is widespread in birds, but not universal (see later).

Annual variations in spring migration dates Movement from wintering areas is thought to be triggered by an endogenous rhythm, with departure dates modified by prevailing local conditions (Chapter 13). However, most information on annual variation in migration timing is based, not so much on departure dates from wintering areas, but on passage dates through particular localities or on arrival dates in breeding areas. Weather information is also now available from whole migration routes from wintering to breeding areas, and in recent decades satellites have provided daily images of the state of the vegetation across the world. So we can now examine how conditions in wintering and migration areas influence the start and progress of spring migration, as in the ebird data mentioned above. Weather is involved through affecting the growth of vegetation and potential food supplies, or more immediately by creating wind and other conditions that favour flight in an appropriate direction. In the tropics and subtropics of Africa and South America, studies of many species have shown that annual variations in the start and progress of migration are influenced positively by rainfall and associated vegetation growth, and negatively by drought and lack of plant growth. In other words, the birds migrate earlier and faster in wet conditions when vegetation is greener and insect prey are presumably more plentiful. Further north, in much of Europe and North America, local temperatures are paramount, with many birds travelling more rapidly and arriving in breeding areas earlier in warm springs than in cold ones. Warmth in the northern continents not only encourages plant growth and insect development but also brings favourable winds from the south which speed birds on their northward journeys, often enabling them to migrate and arrive in good physical condition for breeding (Gonza´lez-Prieto & Hobson, 2013). In practice, however, long-distance migrants can sometimes be speeded on their journeys by favourable conditions in the early part of their routes only to be slowed by unfavourable weather later in their journeys through higher latitudes.

Evidence on migration timing from the field Because of variable conditions on route, we would not necessarily expect a good correlation between departure dates from wintering areas and arrival dates in breeding areas, especially in species which take many days over the journey. Nevertheless, various trans-Saharan migrants have arrived earlier at passage (P) or breeding sites (B) in Europe in springs following good (5wet) conditions in their African wintering areas and later in springs following poor (5dry)

Arrivals of Barn Swallow (days)

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FIGURE 15.6 Effect of the Sahel rainfall on Barn Swallow (Hirundo rustica) arrival dates in Spain in the following spring, over 57 years. Annual arrival of Barn Swallows is the annual average of residuals of first arrival dates, calculated from a model allowing for spatial variability. Based on data in Gordo & Sanz (2006), Gordo (2007).

8 6 4 2 0 -2 -4 n=6

16

-100

-50 0 50 Sahel rainfall index

17

13

5

-6 100

conditions when most foods were inevitably scarcer (Figure 15.6; for Barn Swallow, see Saino et al., 2004b (B); for five species, see Gordo et al., 2005 (B); for three species, see Gordo & Sanz, 2008 (B); for Pied Flycatcher, see Both, 2010 (P); for Common Redstart, see Finch et al., 2014). Recent experiments on Pied Flycatchers were especially telling (Ouwehand et al., 2023). In an area of the Ivory Coast in West Africa, some individuals were provided with extra food on their winter territories, while others were left only with their natural arthropod foods. The fed birds fattened more rapidly and left earlier on migration than the unfed birds. The study covered 2 years, in one of which rain came much earlier than in the other. Overall departures were earlier in the wetter year when arthropod numbers peaked earlier. Similar findings emerged for Common Cuckoos which left a major staging area in West Africa earlier in years when rain fell earlier, promoting an earlier burst in insect food supplies (Davies et al., 2023). The dates that birds left this area had a major effect on the dates they arrived on their British breeding areas, although conditions on route also had some influence. Nevertheless, other studies which have recorded no tendency for earlier migration in years with better conditions in wintering areas, at least with migration dates recorded at points on route (P) or arrival in breeding areas (B). They suggested later migration in years with good conditions in African wintering areas than in years with poor conditions [for 15 passerine species, see Robson & Barriocanal, 2011 (P); for five passerine species, see Tøttrup et al., 2008 (P); for Barn Swallow, see Balbontin et al., 2009 (B)]. However, being based on passage and arrival dates, we cannot exclude an over-riding influence of conditions on route. The apparent role of poor food supplies in delaying migration through Africa was striking in some studies. Redbacked Shrikes and Thrush Nightingales (Luscinia luscinia), which winter in eastern Africa, arrived on their European breeding areas unusually late in 2011, when they had been held up in the Horn of Africa at a time of severe drought (Tøttrup et al., 2012). In this year, tracked individuals of both species stayed there for an average of 18 and 29 days, respectively, compared with 9 and 21 days in wetter years. Shortage of food in the drought year could have slowed their rates of fattening, delaying the rest of their journeys through to breeding areas. As an example of more direct weather effects, the late arrival of White Storks (Ciconia ciconia) in central Europe, which migrate by soaring flight, has been linked with the stronger headwinds and poorer thermal conditions associated with cold springs (Rotics et al., 2018). Similar relationships between weather and migration timing have also been documented in some Neotropical migrants. Among Kirtland’s Warbler (Setophaga kirtlandii), years with dry conditions in wintering areas on the Bahamas (implying poor food supplies) were associated with late arrival in Michigan breeding areas, followed with poorer subsequent breeding success (Rockwell et al., 2012). Also, among American Redstarts (Setophaga ruticilla), wet conditions and abundant food in tropical Jamaican wintering areas were associated with good body condition, early departure and early arrival in North American breeding areas (Studds & Marra, 2007, 2011; McKellar et al., 2012). The influence of food supplies on departure and migration dates is also shown by the findings that, in particular years, birds wintering in food-rich habitats reach migratory conditions and travel earlier than those in poorer habitats, a trend evident in both Old and New World species for American Redstart (Setophaga ruticilla), see Studds & Marra, 2007; for Black-throated Blue Warbler (Setophaga caerulescens), see Bearhop et al. (2004); for Northern Waterthrush (Partesia noveboracensis), see Smith et al. (2010); for Black-tailed Godwit (Limosa limosa), see Gunnarsson et al. (2006); for Montagu’s Harrier (Circus pygargus), see Schlaich et al. (2016). Birds from good wintering habitats also tended to arrive earlier in breeding areas and breed more productively than those from poor winter habitats. Moreover, among American Redstarts in Jamaica, experimental reduction of winter food supplies in good habitat, through the use of insecticide, reduced the body condition and delayed the departure of American Redstarts (Cooper et al., 2015). All

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Mean arrival date

these findings are in line with studies from stopover sites confirming the influence of food supplies on the fuelling rates of individual migrants (Chapter 14). But as in the Old World, the opposite situation was also recorded in the New World. In South America, tracked Swainson’s Thrushes wintering in native forest (the most food-rich habitat) departed later than birds wintering in coffee plantations, but the later (forest) birds were then able to migrate more rapidly and suffer no delay in their arrival in North American breeding areas (Gonza´lez et al., 2020). Habitat conditions can influence bird numbers seen on the ground, and in many areas, birds break their journeys in greater numbers, or for longer periods, in years when food is abundant there than in other years (for a difference between wet and dry years in the West Indies, see Faaborg et al., 1984). Once birds which have wintered in the tropics reach the northern continents, they come under the same weather conditions that influence the short-distance migrants that winter within these continents. Here, the message is more consistent between studies: birds depart earlier and make faster progress in warm springs than in cold ones (Figure 15.7; Cooke et al., 1995; Huin & Sparks, 1998; Ahola et al., 2004). At particular localities, temperatures in early spring show more annual variation than temperatures in late spring, and accordingly, early-arriving species typically show significantly more year-to-year variation in arrival dates than do late-arriving ones (Gilyazov & Sparks, 2002; Tryjanowski et al., 2002; Figure 15.8). Disruptions in the normal arrival sequence occur in years when warm and cold periods alternate through the spring, and in some years a spell of bad weather on the migration route can produce a twin-peaked arrival pattern (for Sand Martin (Riparia riparia), see Elkins, 2005). In the northern continents, then, the advance of species from lower toward higher latitudes each spring is linked with warming conditions and the ecological changes they set in train. This pattern is well shown by geese whose northward advance is closely linked to both ice melt and plant phenology. The birds arrive at successive latitudes just as plant growth begins (usually above 3 C) and follow a ‘green wave’ northwards, taking advantage of the spring flush of growth on forage plants at successive staging sites (van der Graaf et al., 2006; Si et al., 2015; van Wijk et al., 2012; FIGURE 15.7 Arrival dates of Barn Swallows (Hirundo rustica) in Britain in different years in relation to mean February March temperatures. From Sparks et al. (1999).

9 April

1 April

24 March 0

1

2

3

4

5

6

7

8

February–March mean temperature

(b) 16

16

14

14

Standard deviation in mean arrival date

Standard deviation in mean arrival date

(a)

12 10 8 6 4 2

12 10 8 6 4 2

0

0 50

70

90 110 130 Mean arrival date

150

50

70

90 110 130 Mean arrival date

150

FIGURE 15.8 Annual variations (as reflected in standard deviations, SD) in the first arrival dates of migratory species in relation to their mean first arrival dates over many years. (a) An area in western Poland, 1913 96 (Tryjanowski et al., 2002); (b) an area in northern Russia, 1931 99 (Gilyazov & Sparks, 2002). In both areas, earlier arriving species had more variable first arrival dates. They were mainly short-distance migrants that wintered within Europe, while the later arriving species were mainly long-distance migrants wintering in Africa south of the Sahara. Regression equations: western Poland, SD 5 19.6 0.103x, where x is the mean first arrival date, r 5 0.65, P , .01; northern Russia, SD 5 11.7 0.0724x, r 5 0.80, P , .001.

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Ko¨lzsch et al., 2016). However, before reaching their nesting areas, the migrating geese may overtake the green wave, arriving on nesting areas ahead of it and lay and incubate their eggs on the strength of body reserves (Chapter 5). In most years, their eggs hatch as the green wave reaches the breeding areas, and the goslings then have rich vegetation on which to feed and grow. Many species of other waterbirds follow the ice melt northward in spring and arrive on their breeding areas part way through the melt when there is sufficient open water and snow-free land for them to feed. Among Bewick’s Swans (Cygnus columbianus bewickii) tracked from the Netherlands to the Russian Arctic, spring migration proceeded slowly as in each staging area the birds waited for the advancing thaw. The autumn journey was faster, because then the swans travelled well ahead of the ice, avoiding the risk of getting frozen in (Nuijten et al., 2014). As another example, the advance of Snowy Owls (Bubo scandiaca) and Rough-legged Buzzards (Buteo lagopus) over the arctic tundra in spring followed the snow-melt line northward, gradually exposing the ground vegetation which held their rodent prey (Curk et al., 2020). The Peregrine (Falco peregrinus) followed at a later stage of snow-melt when almost all the ground was clear and suitable avian prey were arriving. In some other species, an effect of local food supply on arrival dates has been detected over and above any effect of temperature. For example Bramblings (Fringilla montifringilla) arrive on their northern breeding areas earlier in years of good spruce crops than in other years (Mikkonen, 1981). As the cones open, the seeds provide an early food supply, enabling the birds to survive earlier than usual in their breeding areas until their main summer foods (caterpillars) become available in nearby birch woods. In one area over a number of years, the size of the spruce crop, together with air temperature and snow cover, explained 89% of the annual variation in Brambling arrival dates. Among shorebirds migrating northward through the prairies of North America, fattening rates were dependent on preceding precipitation and the state of local wetlands (Krapu et al., 2006). Female Pectoral Sandpipers (Calidris melanotos) stopping to refuel at Missouri wetlands gained larger fat loads in wet years than in dry years (Farmer & Wiens, 1999), and Least Sandpipers (Calidris minutilla) and Western Sandpipers (Calidris mauri) in western Texas accumulated 7% 9% more fat in a wet than in a dry year (Davis et al., 2005). Fattening is clearly dependent on food supplies, and the greater the fat reserves of birds, the quicker their remaining journey could be. It is seldom certain to what extent early arrival in particular years is due to earlier departure of a species from wintering areas or to faster progress on route but, because the same weather patterns influence large parts of the migration route, migrants come under the influence of warmer or colder (or wetter or dryer) conditions long before they reach their breeding areas. Among short-distance migrants wintering within Europe, birds may leave their wintering areas earlier in warm than in cold years, as found, for example in 17 species wintering in Spain (Sokolov, 2006). In the warm years, these birds also arrived earlier in their breeding areas (for Song Thrush (Turdus philomelos), see also Redlisiak et al., 2021). Similar findings were held in North America where birds were found to leave wintering areas earlier in warm springs (Zaifman et al., 2017) and made more rapid progress on route (Marra et al., 2005). Several other studies noted relationships between arrival dates in breeding areas and temperatures or other conditions back along the migration route, including the wintering areas (Hu¨ppop & Winkel, 2006; Sokolov, 2006; Halkka et al., 2011). For nine species of short-distance migrants passing through Heligoland Island off Germany during 1960 2014, weather variables in wintering and stopover areas explained 58% 77% of the year-to-year variation in spring passage dates (apart from Common Chaffinch (Fringilla coelebs) at 38%), while for six long-distance trans-Saharan migrants the equivalent figures were 72% 86% (Haest et al., 2018, 2020). Increased spring temperatures contributed strongly to the net advance in spring migration dates observed over the 55-year period but improved wind conditions, especially over the Maghreb and Mediterranean, made an even bigger contribution. Within species, the conditions encountered during travelling are likely to differ between populations depending on the timings and routes of their journeys (for Pied Flycatcher, see Both et al., 2006). Whatever the mechanisms, the implications of these various studies are that arrival dates in breeding areas depend on conditions in both wintering and migration areas and that departures from winter quarters, or stopover sites on route, can be delayed by poor feeding conditions, which may in turn slow fattening rates and migration speeds. In some species, delayed arrival has also been associated with reduced numbers (implying reduced survival) and subsequently with reduced breeding success (Briedis et al., 2017; Mondain-Monval et al., 2020).

REOCCUPATION OF LOCAL BREEDING AREAS In spring, individual birds seem to be under pressure to return to breeding areas early, to gain precedence in competition for territories or nest sites, and to gain time, increasing their chance of raising young. But there are limits to earliness because, unless they carry huge body reserves (like geese), birds cannot survive in breeding areas until food becomes

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sufficiently plentiful there. Typically, among the early-arriving species, individuals first concentrate in particular places where food is available moving only later to their nesting places as conditions permit. For example, hirundines often first appear in spring over wetlands, where midges first become abundant, and only later spread to their nesting sites, which may be scattered through the surrounding landscape. Montane species often appear first in valleys, moving up as the higher ground becomes snow-free and habitable. Later-arriving species seem to settle directly on their territories, especially those returning to territories of the previous year. Nocturnal migrants, absent in the evening, are often found on their territories at dawn when they start singing and chasing intruders (e.g., Nolan, 1978). They seem to switch instantly from migration to reproductive mode. An extreme example is provided by a male Wood Warbler which was caught on spring migration and ringed on the Isle of Man off western Britain on 8 May. The following morning, less than 24 hours after ringing, the same bird had established a territory 205 km further north, and by that evening it had attracted a mate and started nest-building (Morton, 1986). In many species, reoccupation of local breeding areas each spring follows the pattern depicted in Figure 15.9. In the population as a whole, arrival may be spread over some weeks, but most individuals arrive around the middle of this period unless disrupted by poor weather. In most species, males tend to arrive before females, and older individuals in better body condition commonly arrive and pair up before younger or poorer condition ones (Francis & Cooke, 1986; Hill, 1988; Møller, 1994a,b; Lundberg & Alatalo, 1992; Vergara et al., 2007). This may be because older, bettercondition birds depart earlier from their wintering areas, as noted, for example in the Great Reed Warbler (Acrocephalus arundinaceus) (Nisbet & Medway, 1972) and American Redstart (Marra et al., 1998). Alternatively, it may be because they spend the winter nearer to their breeding areas (as in many species, Ketterson & Nolan, 1983), or migrate faster (also in many species, Hilde´n & Saurola, 1982; Ueta & Higuchi, 2002, Chapter 9). Whatever the mechanism, birds in good condition generally reach the breeding areas before others and can presumably also better survive the costs associated with early arrival, including a poorer food supply which improves with time (Møller, 1994a,b; Kokko, 1999). In many species, it is not unusual for members of the same pair, despite often wintering far apart, to arrive on their nesting territories on about the same day, or at least on much closer dates than expected by chance (for Black-tailed Godwit, see Gunnarsson et al., 2004; for White Stork, see Tryjanowski et al., 2004). This synchrony could be a consequence of their individual migration schedules that happened to coincide and allow them to pair together in the first place, remaining faithful in subsequent years. In many species that have been studied, males are surplus to females, and it is the latest arriving males that usually end up without a mate. How might competition for territories and mates influence the arrival patterns of migrants? In mathematical models of this situation, increasing the number of competitors for territories can generate cascading pressure for early arrival, which advances arrival dates even further ahead of optimal breeding dates. If the habitat is saturated, so that latecomers risk not obtaining any territory, or if the worst territories are of much lower quality than the rest, competition may lead to most breeders arriving within a short interval, followed by a much later non-breeding contingent (as seen in some raptors and others). The penalties for later arrival are not necessarily greatest for the earliest arriving birds, but for those that have the most to lose if they drop a few places in the arrival sequence (Kokko, 1999). The fact that some populations seem to arrive on breeding areas up to several weeks before they start nesting has been attributed to competition for territories, which provides strong selection pressure for early arrival. However, as emphasized above, birds can only respond to that pressure if the breeding areas offer sufficient food at that time. An extreme example is provided by Snow Buntings (Plectrophenax nivalis) in arctic Greenland, where males arrive in early FIGURE 15.9 The pattern of arrival by Prairie Warblers (Setophaga discolour) in a breeding area at Bloomington, Indiana. The diagram is based on the combined data from 1958 to 1965 but corrected for annual variation in arrival periods by counting the first day of arrival each year as Day 1. In different years, the first arrival date varied between 11 and 22 April for males, and between 21 and 28 April for females. The mean interval separating the first male and female in each year was 5.1 days (extremes 1 and 9 days). As may be seen, males in general arrived before females. Modified from Nolan (1978).

Cumulative percentage arrived

100 Males 80 Females 60 40 20 0 0

5

10 15 20 Day from first arrival

25

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April, 6 8 weeks before nesting and 2 4 weeks ahead of females. During this lengthy pre-nesting period, males commonly experience severe storms and temperatures down to 30 C, and considerable mortality can occur. Yet year after year, the males continue to arrive at this early date, to compete for territories in the limited high-quality nesting habitat (Meltofte, 1975). The importance of an early return is also evident in some colonial cliff-nesting seabirds, in which pairs compete for limited space on cliff ledges. Apparently to secure their sites, birds return weeks or months before egg-laying, and in some species, return dates became progressively earlier as populations grew and competition intensified. Northern Fulmars (Fulmarus glacialis) are now present on their nest sites almost year-round in Britain, mates taking turns to guard the site, foraging between times. Eggs are laid in May. Similarly, over most of their breeding range, Common Murres (Guillemots) (Uria aalge) return to their breeding colonies in late winter or early spring, some 2 months before the first eggs are laid. Return dates to cliff colonies on the Shetland Isles, off Scotland, became earlier by 25 weeks from March to October during a 10 12 year period. This change coincided with a period of continued population growth and was attributed to intensified competition for nest sites (Harris et al., 2006). Autumn returns persisted for about 10 years, after which return dates gradually reverted to late winter, as the population declined. Over the whole period, the correlation between mean annual return date and population size was highly significant (r 5 0.695, P , .001, n 5 29 years). This link between arrival dates and potential competition levels did not rule out an influence of food supply, which, through a period of change, could itself facilitate earlier arrival or over-wintering and at the same time promote population growth. The basic problem inherent in the timing of spring migration is that individuals arriving early in breeding areas stand to benefit from greater production of young that year, but they may die if conditions at the time of arrival are bad. Birds that nest at high latitudes often risk facing an untimely cold snap or snowfall that cuts off their food supply. The earlier in spring they arrive, the more likely this is to happen, killing or weakening a large proportion of the earlyarriving individuals (Chapters 22 and 31). On the other hand, within the limits of the possible season, the earlier that birds begin to nest, the greater the number of young they are likely to produce. Not only do first arrivals tend to acquire better territories, nest sites or mates than later arrivals, but they also lay earlier in the season and often produce more young, as demonstrated in many species (Table 15.2). In some of these species, the latest birds to arrive failed to get either territory or mate. The Barn Swallow illustrates the conflicting pressures on migration timing, as it benefits greatly from an early start to breeding, but the costs of early arrival are evident in cold seasons by mortality among early-arriving males (Møller, 1994a,b, 2001). In these inclement seasons, birds suffer from snowstorms, when their increased energy demand is coupled with an absence of insect prey. Catastrophic losses early in the season can exert a measurable selection pressure on migration dates if losses hit early-arriving individuals more severely than others, as evident among migrant Cliff Swallows (Hirundo pyrrhonata) in Nebraska (Chapter 22; Brown & Brown, 2000). Arrival date has an inherited component in both these swallow species, leading in cold springs to selection for later arrival. If early arrival confers the competitive advantage of prior occupancy but increases the risk of mortality, arrival date can be viewed as a trade-off between opposing pressures, but sometimes the ‘best’ males may be able to survive when others could not (Drent et al., 2003).

Settlement on territories In any area, it is commonly found after detailed study that territories vary in quality: that is, in the fitness benefits they confer on their occupants. The quality of nesting habitat is assessed from measurements of cover, disturbance, local food supplies or proximity to good feeding areas (whichever is most relevant in the population concerned), or more directly from the feeding rates, survival or reproductive rates of previous occupants. On the basis of such assessments, places classed as best are generally occupied first each spring. As these places become occupied, later arrivals are relegated to poorer places. For example Pied Flycatchers arriving in central Sweden in spring settled in deciduous areas in preference to coniferous (Figure 15.10). In deciduous areas, food supply increased earlier in spring, the birds settled at greater density, laid earlier and raised larger broods than in the conifers. Also, the males (but not the females) that occupied deciduous areas were larger than those in coniferous areas, presumably because the bigger individuals were better able to secure places in the best habitat (Lundberg et al., 1981). Patterns of spring settlement, with the best areas occupied first, have been described in many other bird species, including Northern Wheatear (Oenanthe oenanthe) (Currie et al., 2000), Painted Bunting (Passerina ciris) (Lanyon & Thompson, 1986), Great Reed Warbler (Bensch & Hasselquist, 1991), Savi’s Warbler (Locustella luscinioides) (Aebischer et al., 1996), Black-tailed Godwit (Gunnarsson et al., 2005) and Black Kite (Milvus migrans) (Sergio et al., 2007).

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TABLE 15.2 Relationship in various bird species between spring arrival date in breeding areas and subsequent breeding performance. In general, an early arrival relative to other individuals resulted in better performance. K 5 effect between arrival date and breeding measure observed. Species

Mate acquisition

Territory quality

Laying date

Clutch size

Young per nest

Sources

Northern Wheatear (Oenanthe oenanthe)

K

K

K

K

K

Currie et al. (2000)

Black Redstart (Phoenicurus ochruros)

K

American Redstart (Setophaga ruticilla)

K

Landmann & Kollinsky (1995) K

K

American Redstart (Setophaga ruticilla)

K

K

K

Kirtland’s Warbler (Setophaga kirtlandii)

K

K

K

Great Reed Warbler (Acrocephalus arundinaceus)

K K

K

Savi’s Warbler (Locustella luscinioides)

Smith & Moore (2005) Ka

Rockwell et al. (2012)

K

K

Bensch & Hasselquist (1991)

K

K

Aebischer et al. (1996)

K

Takaki et al. (2001)

K

Lundberg & Alatalo (1992)

K

Møller (1994a,b), Saino et al. (2004a,b)

K

Gunnarsson et al. (2005)

K

Ho¨tker (2002)

K

Sergio et al. (2007)

Styan’s Grasshopper Warbler (Locustella pleskei) European Pied Flycatcher (Ficedula hypoleuca)

K

Barn Swallow (Hirundo rustica)

K

K

K

Black-tailed Godwit (Limosa limosa)

Lozano et al. (1996), Norris et al. (2004)

Pied Avocet (Recurvirostra avosetta) Black Kite (Milvus migrans)

K

Barnacle Goose (Branta leucopsis)

K

K

White Stork (Ciconia ciconia)

K

K

Dalhaug et al. (1996) K

Tryjanowski et al. (2004), Vergara et al. (2007)

a

Young per year, as some birds had two broods.

Cumulative percentage

100

FIGURE 15.10 Settling and egg-laying dates of Pied Flycatchers (Ficedula hypoleuca) in broad-leaved and coniferous forests in central Sweden. In the preferred broad-leaved areas, food supply increased earlier in spring, the birds settled earlier and at greater density, and annual breeding success (in terms of young per female) was higher than in coniferous areas. Modified from Lundberg et al. (1981).

Broad-leaved Coniferous

50

Clutches started

Territories occupied

0 4

6

8

10

12

14

16 18 May

20

22

24

26

28

30

1

3 June

5

7

9

Seasonal reoccupation of breeding and wintering areas Chapter | 15

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In some species, the same sequence of territory settlement was held year after year in the same area, even though the occupants changed, and even though some early settlers were displaced by later-returning former owners. In not all species do individuals establish a nesting territory as soon as they arrive in breeding areas. Instead, they feed in flocks for some days or weeks before they eventually take up a nest site (e.g., Pied Avocets (Recurvirostra avosetta), Ho¨tker, 2002). Acquisition of the best nesting places in such species cannot therefore be due directly to early arrival, but birds that arrive earliest may also be the ones most able to compete for nesting places.

Components of early migration Early arrival in breeding areas could be due to earlier departure from wintering areas, faster migration on route, or a combination of the two. Several studies have shown that the departure dates of individuals from wintering areas are the strongest predictors of their arrival dates in breeding areas, with factors acting on route in most years contributing relatively little to variation in arrival dates (Stanley et al., 2012; Tøttrup et al., 2011; Callo et al., 2013; Jahn et al., 2013). Based on tracking studies, Schmaljohann (2019) calculated that, in general, starting migration one day later would result in arrival timing delayed by 0.4 0.8 days. Similarly, increasing the total migration distance by 1000 km would result in 2 days of delay in arrival time in spring and 5 days of delay in autumn (assuming no delay due to unusual weather). The generality with which the start date of migration is correlated with arrival timing within species suggests that departure date is the key factor regulating arrival timing and is therefore an aspect on which natural selection could act strongly.

WITHDRAWAL FROM BREEDING AREAS Regional variation in the onset of winter conditions can again be tracked by following particular isotherms as they move from higher to lower latitudes, bringing colder conditions southwards across the northern continents (Figure 15.11). In autumn, the 10 C isotherm takes nearly 3 months to spread southward through Europe. Although studied in less detail than spring arrival, the autumn withdrawal of migratory birds from the northern continents occurs, as expected, from the top down, as northern populations generally leave before southern ones (for exceptions see below). Moreover, the whole process of withdrawal occurs more slowly in autumn than the process of recolonization in spring, a least in North America (La Sorte & Fink, 2017). As mentioned earlier, species tend to leave particular localities in autumn in reverse order to that in which they arrived in spring: that is, the latest to arrive are first to go (Figure 15.2). This sequence is again broadly linked with the decline in their respective food supplies, associated with falling temperatures and plant senescence or shut-down (La Sorte et al., 2014). The earliest species to leave particular localities also show less year-to-year variation in their departure dates than do the last to leave (Gilyazov & Sparks, 2002). Many short-distance migrants which migrate within the northern continents seem to follow the frost wave (0 C) southwards, as freezing conditions shut off their food supply, as lakes ice over, soil surfaces harden and plants stop growing and tree leaves fall. Through programmes such as ebird, sufficient data are now available to plot the withdrawal of different species from much of a continent and see how closely the process keeps step with moving isotherms. In different species, the whole process of withdrawal can again take several weeks, or up to 3 months in species such as the Barn Swallow which breed over a wide span of latitude. Low-latitude populations may still be on their breeding areas when individuals from higher latitudes pass through on route to winter quarters (for Yellow Wagtail in Europe, see Curry-Lindahl, 1963; for Wilson’s Warbler (Wilsonia pusilla) in North America, see Kelly et al., 2002). A different widespread trend is evident in some single-brooded species, which spend about the same amount of time on their nesting areas at all breeding latitudes, but can both arrive and depart earlier from southern than from more northern parts of the breeding range. For example migratory Ospreys (Pandion haliaetus) nesting in Florida arrive at their nest sites about 1 month earlier than those in New York and New Jersey and also depart for their wintering areas about 1 month earlier (Martell et al., 2001, 2004). It is as though the annual cycle of high-latitude breeders is simply shifted later relative to that of lower-latitude breeders. Birds from all latitudes in the breeding range seem to leave soon after raising their single brood and are not ‘driven out’ by declining food availability in the way that some other species (mostly short-distance multi-brooded migrants) may be. A similar delaying of the whole annual cycle with increasing breeding latitude has been described in the Semi-collared Flycatcher (Ficedula semitorquata), Tree Swallow (Tachycineta bicolour) and Purple Martin (Progne subis) and is presumably general in widespread bird species that raise only a single brood per year (Briedis et al., 2016; Gow et al., 2019; Neufeld et al., 2021). It seems, then, that in the northern continents autumn migrations fall into two main categories: one where northern populations start first and overtake southern ones on route, and the other, involving mainly single-brooded species, where southern populations migrate south before northern ones.

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The Migration Ecology of Birds

FIGURE 15.11 The advance of autumn, as shown by the dates of return of the falling 10 C isotherm to various parts of Europe. From T. Sparks, unpublished.

Patterns of autumn departure also differ between obligate (complete) migrants, in which all individuals leave every year, and facultative (partial) migrants in which the proportions of individuals that leave, and their dates of departure, vary with local conditions at the time (Chapter 13). In obligate (often long-distance) migrants, individuals seem to leave their breeding areas as soon as they can after breeding or after breeding and moulting, as the case may be. In many

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such species, departure occurs before vegetation senescence and the collapse of local food supplies (Briedis et al., 2020). Unlike the situation in spring when food is scarce but increasing, in late summer food is plentiful but often declining and the weather is still mild. So if the birds have finished breeding and have no reason to wait longer, it is advantageous to migrate while conditions are still good, and before food supplies on migration routes have become depleted. They might also establish themselves in wintering areas at an early date, perhaps getting places in the best habitat. This holds especially in species which hold territories in winter quarters and is probably the main selective pressure for rapid departure and progress on the autumn journey. Hence, while spring arrival usually coincides fairly precisely with the re-appearance of new food supplies, autumn departure of some obligate migrants may precede the autumn collapse of food supplies by up to several weeks (Schneider & Harrington, 1981). Facultative migrants show less year-to-year consistency and urgency in autumn departure dates, and many individuals seem to remain on breeding areas as long as conditions allow, leaving up to several weeks later in some years than in others, and sometimes long after the end of moult (Chapter 14). This holds for seed-eating finches, which, in years of good tree-seed crops, stay all winter or leave much later than in years of poor crops (Chapter 20). They can stay after snowfall, providing that seeds remain on the trees, whereas other finch species, which pick seeds from low herbaceous plants or the ground, may be ‘driven out’ by the first heavy snowfall. Likewise, many northern waterbirds leave as their wetland habitats begin to freeze over, which occurs much earlier in some years than in others. Because shallow waters freeze before deep ones, shallow-water dabbling ducks usually leave before deep-water diving ducks. In these facultative migrants, access to local food supplies seems to have a major influence on the dates of departure and rates of southward migration, with birds lingering on route while food lasts, and travelling much less far in some years than in others.

Competition for winter habitat In species that compete for territories or feeding areas in winter, studies have shown an advantage of arriving early relative to other individuals. For example wintering American Kestrels (Falco sparverius) arriving in Florida from the north occupied habitats in decreasing order of their quality in terms of food supply. Early-arriving birds (mostly females and juveniles) acquired most of the good places, while later arrivals took the less good places (Smallwood, 1988). Hence, as in breeding areas, the best places were occupied first, and by the earliest birds. But it is not only territorial species that benefit from early arrival in wintering areas. On an estuary in southern England, Eurasian Oystercatchers (Haematopus ostralegus) accumulated first on the two most preferred mussel beds where feeding rates were highest (Goss-Custard et al., 1982, 1984). But as more birds arrived and interactions increased, birds progressively occupied the less favoured mussel beds. Later-arriving adults displaced immatures already present on the favoured beds. Moreover, as mussel stocks declined on the favoured beds, more birds left, but in reverse order of their dominance rank, to feed on less preferred beds or in other habitats. In this species, therefore, the effects of arrival date were modified by dominance relations among age groups, but within age groups the benefits of early arrival relative to other individuals were still apparent. Another example of first arrivals taking the best habitats, and thereby having greater chance of surviving the non-breeding season, is the Ruddy Turnstone (Arenaria interpres) (Wernham et al., 2002), while evidence for the best habitat being occupied first during a period of population increase is available for the Black-tailed Godwit (Gill et al., 2001).

Winter movements While in some bird species individuals migrate to winter in a single locality each year, others change localities one or more times during the winter, usually moving progressively further from their breeding areas. Within the northern continents, these movements are most marked in irruptive species whose food supplies fluctuate from year to year, causing the birds to travel in several steps and varying distances from year to year (Chapters 20, 21). Within-season movements are also common in tropical wintering areas, again occurring in response to diminishing food supplies, with migrants staying in particular areas only as long as conditions permit (Chapter 26; Moreau, 1972; Jones, 1995). Because in any one area, decline in food supply depends partly on the number of birds exploiting it, competition is probably involved in triggering onward movements of at least part of the population (for Purple Martin, see Stutchbury et al., 2016). In both Africa and South America, some migrants remain within the northern tropics throughout the northern winter, occupying two or more areas during their stay, while others move on to the southern tropics, exploiting both hemispheres habitats at the same seasonal stage of development but 6 months apart (for further discussion, see Chapters 26, 27).

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The Migration Ecology of Birds

In general, for northern hemisphere birds, in the same way that breeding areas empty in autumn from the top down (north to south), wintering areas empty in spring from the bottom up (south to north). Individual species begin migrating first from the most southern parts of their winter range, and progressively later from more northern parts, with the whole withdrawal spread over several weeks (e.g., see Chapter 13). For birds that breed in the southern hemisphere, the same patterns hold, but with the directions reversed: south to north in autumn and north to south in spring, in both cases towards lower latitudes in autumn and higher latitudes in spring.

CONCLUDING REMARKS The benefits of early arrival in breeding and wintering areas could lead to the whole breeding cycle becoming earlier and earlier, if it were not constrained in some way. The brake on this process occurs in spring, when birds cannot occupy breeding areas and start nesting until conditions become suitable. In addition, multi-brooded species gain from remaining in breeding areas as late as possible if they could raise another brood, even though this may delay to some extent their departure to wintering areas. Again the birds face a trade-off between the advantages of extra reproduction and the disadvantages of a late migration, when food is likely to be scarce, and when the better habitat in wintering areas is likely to be already occupied. The benefits of early arrival in wintering areas are perhaps greatest in populations in which individuals occupy the same areas throughout a winter. Yet many migratory bird species periodically move within a winter or occupy different areas in different winters. Perhaps in these circumstances, early arrival could carry little advantage.

SUMMARY Migratory bird species in Europe and North America have been found to spread northward in spring at average rates of 30 300 km/day, in step with improving conditions, as reflected in the northward advance of particular isotherms, bringing warmer weather and vegetation growth. In general, early-migrating species progress more slowly than later ones. Barn Swallows, which breed over a wide span of latitude, take more than 3 months each year to re-colonize all parts of their breeding range. The rate at which the northern continents are colonized each spring, from low to high latitudes, is often much slower than the migration speeds of individual birds, as birds must often wait for snow melt or other conditions to improve. Overall, the northern continents are occupied by migrants each spring from south to north, associated with the northward progression of spring conditions. Many birds benefit from arriving relatively early in their breeding areas, as they are then able to obtain better territories and mates than later arriving birds, and often show better breeding success. However, if they arrive too early, they risk food shortage, and may sometimes die from late cold snaps. These conflicting selection pressures are likely to influence the average spring migration (and arrival) dates of different species. Nevertheless, species migrate at different dates, depending partly on when their particular foods become sufficiently available, and in general they travel earlier in warm springs than in cold ones. The arrival dates of many species in particular localities are spread over a shorter period than their autumn departure dates. Some species spend only 2 3 months each year on their high-latitude breeding areas. Most migratory birds vacate their breeding areas on the northern continents in autumn from north to south, in reverse order to that in which they re-colonized in spring. However, in some other species, notably single-brooded obligate migrants, southern-nesting populations (having completed their breeding earlier) move out first. There are thus two main patterns in autumn withdrawal: in one the northern breeders depart first, and in the other the southern ones. Overall, the northern continents are drained of migrant birds in autumn from north to south, and wintering areas from south to north in spring, with the opposite patterns in the southern hemisphere.

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Krapu, G. L., Eldridge, J. L., Gratto-Trevor, C. L. & Buhl, D. A. (2006). Fat dynamics of arctic-nesting sandpipers during spring in mid-continental North America. Auk 123: 323 34. La Sorte, F. A. & Fink, D. (2017). Migration distance, ecological barriers and en-route variation in the migratory behavior of terrestrial bird populations. Glob. Ecol. Biogeog. 226: 216 27. La Sorte, F. A. & Graham, C. (2020). Phenological synchronization of seasonal bird migration with vegetation greenness across dietary guilds. J. Anim. Ecol. 90: 343 55. La Sorte, F. A., Fink, D., Hochachka, W. M., DeLong, J. P. & Kelling, S. (2014). Spring phenology of ecological productivity contributes to the use of looped migration-strategies by birds. Proc. R. Soc. B: Biol. Sci. 281: 20140984. Lamarre, J.-F., Gauthier, G., Lanctot, R. B., Saalfeld, S. T. Love, O. P. et al. (2021). Timing of breeding site availability across the North American Arctic partly determines spring migration schedule in a long-distance Neotropical migrant. Front. Ecol. Evol., 9. Available from https://doi.org/10.3389/fevo.2021.710007. Landmann, A. & Kollinsky, C. (1995). Age and plumage related territory differences in male Black Redstarts Phoenicurus ochropus the (non)-adaptive significance of delayed plumage maturation. Ethol. Ecol. Evol. 7: 147 67. Lanyon, S. M. & Thompson, C. F. (1986). Site fidelity and habitat quality as determinants of settlement pattern in male Painted Buntings. Condor 88: 206 10. Leshem, Y. & Yom-Tov, Y. (1996a). The magnitude and timing of migration by soaring raptors, pelicans and storks over Israel. Ibis 138: 188 203. Lincoln, F.C. (1935a). The migration of North American birds. U.S. Dept. Agric., Washington D.C. Circular No. 363: 1 72. Lincoln, F.C. (1935b). The waterfowl flyways of North America. U.S. Dept. Agric., Washington D.C. Circular No. 342: 1 12. Lozano, G. A., Perrault, S. & Lemon, R. E. (1996). Age, arrival date and reproductive success of male American Redstarts Setophaga ruticilla. J. Avian Biol 27: 164 70. Lundberg, A., Alatalo, R. V., Carlson, A. & Ulfstrand, S. (1981). Biometry, habitat distribution and breeding success in the Pied Flycatcher Ficedula hypoleuca. Ornis Scand 12: 68 79. Lundberg, A. & Alatalo, R. (1992). The Pied Flycatcher. London, Poyser. Marra, P. P., Hobson, K. A. & Holmes, R. T. (1998). Linking winter and summer events in a migratory bird by using stable-carbon isotopes. Science 282: 1884 6. Marra, P. P., Francis, C. M., Mulvihill, R. S. & Moore, F. R. (2005). The influence of climate on the time and rate of spring bird migration. Oecologia 142: 307 15. Martell, M. S., Henny, C. J., Nye, P. E. & Solensk, M. J. (2001). Fall migration routes, and wintering sites of North American Ospreys as determined by satellite telemetry. Condor 103: 715 24. Martell, M. S., McMillian, M. A., Solersby, M. J. & Mealey, B. K. (2004). Partial migration and wintering use of Florida by Ospreys. J. Raptor Res. 38: 55 61. McKellar, A. E., Marra, P., Hannon, S., Studds, C. E. & Ratcliffe, L. (2012). Winter rainfall predicts phenology in widely separated populations of a migrant songbird. Oecologia 172: 595 605. Meltofte, H. (1975). Ornithological observations in northeast Greenland between 76 00’ and 78 00’ N. Lat., 1969-71. Meddr. Grønland 191: 9. Mikkonen, A. (1981). Factors influencing spring arrival of the Brambling Fringilla montifringilla in northern Finland. Ornis Fenn 58: 78 82.

Seasonal reoccupation of breeding and wintering areas Chapter | 15

Møller, A. P. (1994a). Phenotype-dependent arrival time and its consequences in a migratory bird. Behav. Ecol. Sociobiol. 35: 115 22. Møller, A. P. (1994b). Sexual selection and the Barn Swallow. Oxford, University Press. Møller, A. P. (2001). Heritability of arrival date in a migratory bird. Proc. R. Soc. Lond. 268: 203 6. Mondain-Monval, T. O., Briggs, K., Wilson, J. & Sharp, S. P. (2020). Climatic conditions duiring migration affect population size and arrival dates in an Afro-Palearctic migrant. Ibis 162: 572 80. Moreau, R. E. (1972). The Palaearctic-African bird migration system. London, Academic Press. Morton, R. (1986). Rapid territory establishment by a Wood Warbler. Ringing Migration 7: 56. Neufeld, L. R., Muthukumarana, S., Fischer, J. D., Ray, J. D., Siegrist, J. & Fraser, K. C. (2021). Breeding latitude is associated with the timing of nesting and migration around the annual calendar among Purple Martin (Progne subis) populations. J. Ornithol. 162: 1009 24. Nisbet, I. C. T. (1957). Wader migration at Cambridge sewage farm. Bird Study 4: 131 48. Nisbet, I. C. T. & Medway, L. (1972). Dispersion, population ecology and migration of Eastern Great Reed Warblers Acrocephalus orientalis wintering in Malaysia. Ibis 114: 451 94. Nolan, V. (1978). The ecology and behaviour of the Prairie Warbler (Dendroica discolor). Ornithol. Monogr. 26: 1 595. Norris, D. R., Marra, P. P., Kyser, T. K., Sherry, T. W. & Ratcliffe, L. M. (2004). Tropical winter habitat limits reproductive success on the temperate breeding grounds in a migratory bird. Proc. R. Soc. Lond. B 271: 59 64. Nuijten, R. J. M., Ko¨lzsch, A., van Gils, J. A., Hoye, B. J. Oosterbeek, K. et al. (2014). The exception to the rule: retreating ice front makes Bewick’s swans Cygnus columbianus bewickii migrate slower in spring than in autumn. J. Avian Biol. 45: 113 22. Ouwehand, A., Asso, A. A., Johnston, B., Bot, S. Bil, W. et al. (2023). Experimental food supplementation at African wintering sites allows for earlier and faster fuelling and increases flexibility in spring migration departure in Pied Flycatchers. Ardea, 111. Phillips, A. R. (1951). Complexities of migration: a review. Wilson Bull 63: 129 36. Preston, F. W. (1966). The mathematical representation of migration. Ecology 47: 375 92. Redlisiak, M., Remisiewicz, M. & Mazur, A. (2021). Sex-specific differences in spring migration timing of Song Thrush Turdus philomelos at the Baltic coast in relation to temperatures on the wintering grounds. Eur. J. Zool. 88: 191 203. Robson, D. & Barriocanal, C. (2011). Ecological conditions in wintering and passage areas as determinants of timing of spring migration in trans-Saharan migratory birds. J. Appl. Ecol. 80: 320 31. Rockwell, S. M., Bocetti, C. I., Marra, P. P. & Amenazada, M. (2012). Carry-over effects of winter climate on spring arrival date and reproductive success in an endangered migratory bird, Kirtland’s Warbler (Setophaga kirtlandii). Auk 129: 744 52. Rotics, S., Kaatz, M., Turjeman, S., Zurell, D. Wikelski, M. et al. (2018). Early arrival at breeding grounds: causes, costs and a tradeoff with overwintering latitude. J. Anim. Ecol. 87: 1627 38. Saino, N., Sze´p, T., Ambrosini, R., Romano, M. & Møller, A. P. (2004a). Ecological conditions during winter affect sexual selection and breeding in a migratory bird. Proc. R. Soc. Lond. B 271: 681 6.

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Chapter 16

Geographical patterns in migration

Northern Lapwings (Vanellus vanellus) on migration The migratory habit enables a species to enjoy the summers of northern latitudes while avoiding the severity of the winters. Lincoln (1935a,b)

Migration is the most spectacular of bird movements. It can be defined as a large-scale return journey which occurs each year between breeding and wintering (or non-breeding) areas. Involving seasonal shifts of millions of individuals, it produces a massive twice-yearly re-distribution of birds over the earth’s surface. High-latitude regions receive birds mainly in the breeding season, while lower-latitude regions support wintering birds from higher latitudes, as well as year-round residents. Migration thus increases the number of species that occur in particular regions, even though some are present for only part of the year. Throughout the world, migration is most apparent wherever the contrast between summer and winter (or wet season and dry season) conditions is most marked. It allows individual birds to exploit different areas at different times of the year, whether to benefit from seasonal flushes of food or to avoid seasonal shortages. In fact, some birds occupy habitats over winter that they could not use for breeding and then occupy breeding areas that would not support them in winter. This applies to all arctic-nesting shorebirds which spend the winter on coastal mudflats where, due to tidal flooding, they cannot nest, and then migrate north to breed on the arctic tundra which is frozen and snow-covered for the rest of the year. Thus some bird species exist only by exploiting widely separated and different habitats at different seasons. Although most marked at high latitudes, migration also occurs in the tropics, especially in the savannahs and grasslands exposed to regular wet and dry seasons. In the northern tropics, many species move south for the non-breeding season, some crossing the equator, while in the other half of the year, many species of the Southern Hemisphere move north. In contrast, birds confined to lowland equatorial rainforest are probably the least migratory, especially the small insectivores of the understorey where conditions remain relatively stable year-round. This year-round consistency in the The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00014-2 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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rainforest environment removes the need for extensive movements, and many individuals may remain within the same few hectares throughout their adult lives. In the same forests, however, some nectar-eaters and fruit-eaters move within small latitudinal or altitudinal bands in response to flowering and fruiting patterns, while other birds from higher latitudes move in for their ‘winter’ (Levey & Stiles, 1992). Most migratory bird species thus form parts of different communities at different seasons, and may interact with different species in their breeding and non-breeding homes. They may be exposed to different climatic and different dietary regimes and different predators and parasites in the two areas. Overall, more than one-fourth of the world’s 10,000 or so bird species are likely to perform migratory movements in at least part of their range, causing a general shift in the centre of gravity of populations towards the north for the boreal summer and towards the south for the austral summer.

LATITUDINAL TRENDS Worldwide, the number of breeding landbird species found per unit area generally decreases progressively from equatorial to polar regions (but is also generally low in barren deserts and mountaintops). At the same time, the proportions of species that are migratory increase from equatorial to polar regions, as the contrast between summer and winter conditions widens (Newton & Dale, 1996a,b). Migration thus tends to steepen the latitudinal gradient in species numbers between summer and winter. Progressing northward up the western seaboard of Europe, for example the proportion of breeding bird species which move out totally to winter further south increases from 29% of species at 30 N (North Africa) to 83% of species at 80 N (Svalbard), a mean increase of 1.3% of breeding species for every degree of latitude (Figure 16.1). The relationship between proportion of summer visitors and latitude holds, it has been suggested, because at high latitudes the numbers of resident birds are kept low by winter severity. The flush of food in summer is greater than the small number of resident bird species can exploit, leaving a surplus available for summer migrants. The latter therefore increase in proportion with latitude, as the severity of the winters increases, and the numbers of year-round resident species decline. At lower latitudes, a high proportion of breeding species can remain year-round, leaving fewer openings for summer visitors (Herrera, 1978; Morse, 1989). A similar relationship between migration and latitude holds in the largely different avifauna of eastern North America, where the proportion of migrants among breeding species also increases with distance northwards from 12% at 25 N to 87% at 80 N, a mean increase of 1.4% per degree of latitude (Figure 16.2). The difference between the two regions (Figure 16.3a) reflects the climatic shift between east and west sides of the Atlantic: over most of the latitudinal range, at any given latitude winters are colder in eastern North America than in Western Europe. Correspondingly, at any given latitude, a greater proportion (an average of about 17% more) of breeding species leaves eastern North America for the winter than leaves Western Europe. The slopes of the two linear regression lines calculated from the data in Figure 16.3a do not differ significantly, but the intercepts do (F1,19 5 27.5, P , .001), reflecting this climatic difference. On both continents, this northward trend in migration is easily understood in terms of winter conditions. In Europe, mean January temperatures exceed 10 C only in southern Spain and North Africa; they lie within the range 0 C 5 C in much of Western Europe but fall below freezing and as low as 15 C in most of Fennoscandia and to 20 C in Novaya Zemlya in the far north. Midwinter daylengths are around 11 hours at 35 N in southern Europe but decrease to zero at the Arctic Circle. The season of plant growth lasts 6 9 months at 35 50 N but shrinks to less than 3 months in Svalbard, a mean decline in growing season of about 1 month for every 11 of latitude. In continental Western Europe, most fresh waters north of 55 N freeze in winter, although they mostly remain open in Britain and Ireland. Much of the Baltic and Barents Seas also ice over during the course of the winter, closing these areas to seabirds. In North America, similar latitudinal trends occur but are more marked because the continent spans a wider range of latitudes than Europe. The few species that remain to winter in the far north include the Common Raven (Corvus corax), Rock Ptarmigan (Lagopus muta), Gyrfalcon (Falco rusticolus) and Snowy Owl (Nyctea scandiaca) among landbirds, and the Northern Fulmar (Fulmarus glacialis), Ivory Gull (Pagophila eburnea) and Glaucous Gull (Larus hyperboreus) among seabirds. The most northerly seabirds depend on the open water provided by polynyas, and some of the gulls also scavenge the remains of seals killed by Polar Bears (Ursus maritimus). Some individuals of these species may move south to some extent for the weeks of complete darkness. Similar relationships between migration and latitude have been shown among the birds of particular habitats (Herrera, 1978), and among the birds of particular families, such as flycatchers in South America (Chesser, 1998). They presumably hold worldwide in both hemispheres. Such relationships were studied mainly during the latter half of the

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FIGURE 16.1 Map of Western Europe showing the proportions of breeding bird species at different latitudes which migrate south for the winter. From Newton & Dale (1996a).

20th century, for which the temperatures quoted above were averages. Although the situation is now changing through climate warming, resulting in corresponding changes in bird ranges (Chapter 23), the latitudinal trends persist. In some recent winters, open waters have become available where once they froze every year, and on the seas, the freeze line has shifted northwards. The decline in proportion of migrants with decreasing latitude, established above for Europe and North America, continues southwards towards the equator. By 8 latitude in Panama, only five (0.6%) out of 807 breeding species are wholly summer migrants (Ridgely & Gwynne, 1989). These five species are all insectivores which move further south for the austral wet season, namely Swallow-tailed Kite (Elanoides forficatus), Plumbeous Kite (Ictinia plumbea), Common Nighthawk (Chordeiles minor), Piratic Flycatcher (Legatus leucophaius), and Yellow-green Vireo (Vireo flavoviridis).

FIGURE 16.2 Map of eastern North America showing the proportions of breeding species at different latitudes which migrate south for the winter. From Newton & Dale (1996b).

(a)

South for winter

% species migrating south in autumn

100 90 80 70 60 50 40 30 20 10 0

Eastern North America Western Europe

25 30 35 40 45 50 55 60 65 70 75 80 Latitude qN (b)

North for summer

% species migrating south in autumn

100 90 80 70 60 50 40 30 20 10 0

Eastern North America Western Europe

25 30 35 40 45 50 55 60 65 70 75 80 Latitude qN

FIGURE 16.3 Proportions of breeding bird species (y-axis) at different latitudes (x-axis) in Western Europe and eastern North America which migrate south for the winter (a) or north for the summer (b). For southward migration, on regression analysis for Western Europe: y 5 41.49 1.03 1 0.02x2, r2 5 0.97, for eastern North America: y 5 75.05 1 4.33x 0.3x2, r2 5 0.98. For northward migration, on regression analysis for Western Europe: y 5 55.65 0.66x, r2 5 0.81; for eastern North America, y 5 123.72 3.22x 1 0.03x2, r2 5 0.87. For one of these relationships, a quadratic equation gave a significantly better fit than a linear one. From Newton & Dale (1996b).

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The converse of these relationships for Western Europe and eastern North America is shown in Figure 16.3b as the proportions of the birds wintering at different latitudes that move north for the summer. As expected, this proportion is greatest in the south: in Western Europe affecting 36% of species wintering at 35 N, and declining northward to 8% of species wintering at 70 N (mostly seabirds) and none at 80 N. In eastern North America, the equivalent figures are 52% at 25 N decreasing to none at 70 N. Again the slopes of the regression lines do not differ between continents but the intercepts do (F1,16 5 9.9, P , .01). Throughout the latitudinal range, the proportion of wintering species that leaves northward for the summer averages around 10% greater in eastern North America than in Western Europe, again reflecting the climatic difference between the regions. The precise regression relationship varies somewhat between birds of different habitats. In addition, 23% of all species breeding in Western Europe, and 24% of those in eastern North America, leave these areas completely in autumn for the tropics or beyond, returning in spring (Newton & Dale, 1996b). The proportions of all bird species at particular latitudes that are migratory are correlated not only with latitude but also with various climatic factors that vary with latitude, such as the temperatures of the hottest or coldest months or the temperature difference between the hottest and coldest months (Newton & Dale, 1996a). These various measures are of course interrelated, but what really matters is the degree of climatic difference between summer and winter. It is this difference that for many birds governs the difference in food supply between summer and winter at particular latitudes, and hence the difference in environmental carrying capacity between the two seasons. The seasonal difference in carrying capacity may also vary from west to east, according to changes in climate (as between west and east sides of the Atlantic). From west to east across Europe, summer climates become warmer and drier, and winter climates become colder. In consequence, progressing eastward through Europe into Asia, increasing proportions of the local breeding species become migratory. This is especially obvious in comparing populations of coastal areas that live under mild oceanic climates with those at similar latitudes further inland that live under more extreme continental climates. For example, Common Starlings (Sturnus vulgaris) live year-round on the Shetland Islands at 60 N, while at the same latitude in Russia (and for 10 15 south of it) Starlings are wholly migratory. At any given latitude, islands tend to have a lower percentage of migrants than comparable mainland localities, presumably because the surrounding seas buffer islands against the extremes of climatic fluctuation. At some mid-latitude areas, similar numbers of species may be present in summer and winter, but species composition changes somewhat between seasons, because some species from lower latitudes are present only in summer and other species from higher latitudes only in winter (Newton & Dale, 1996a,b). Seasonal changes in bird communities in particular regions are tied to seasonal changes in the types of food available. This emphasizes the point that migrants often exploit seasonal abundances in both their breeding and non-breeding areas. It is a strategy that, for obvious reasons, is much more developed in birds than in most other animals, some kinds of which hibernate through the cold season. Although seasonality in the movements of birds is evident worldwide, in warmer regions, rainfall becomes more important than temperature. In tropical regions, away from the equator, overall rainfall declines and becomes increasingly irregular and localized. In addition to their north south movements, many bird species that winter in the dry tropics tend to concentrate wherever rain has fallen, and food is most available at the time, varying in distribution from year to year.

MIGRATION AND DIET Superimposed on the overall latitudinal trend is another related to diet. Broadly speaking, those species that are resident year-round in a particular region exploit foods that are available there all year, whereas those that leave after breeding exploit foods that disappear or become scarce then. In the northern coniferous forests, for example residents include mainly species that feed directly from trees, on wood-dwelling or bark-dwelling arthropods (woodpeckers, tits, treecreepers), fruits and seeds (some corvids, finches, tits), buds or other dormant vegetation (grouse), or that eat mammals and other birds (some corvids, raptors and owls). In contrast, species that depart for the winter include those which eat active leaf-dwelling or aerial insects (warblers, hirundines) or which eat foods that become inaccessible under snow or ice (ground-feeding finches and thrushes, some raptors, waterfowl and waders). Towards the equator, as winters become less severe, the range of bird dietary types that stay for the winter increases, as a wider range of food types remains available year-round. To illustrate in more detail the link between migration and seasonal changes in food availability, consider two examples. First, Most European songbirds feed either on (1) insects or other invertebrates, (2) seeds and fruits, or (3) a mixture of both categories (Newton, 1995a). Of these food types, seeds and fruits are much more available in winter at high latitudes than are insects. Within each of the three groups, the proportion of migrants increases with latitude, following the general trend in birds as a whole (Figure 16.4). But at each latitude from about 35 N, a larger proportion of insect-eaters than of seed-eaters leaves, while species with mixed insect seed diets are intermediate. Furthermore, the

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80 70 60

60

Insect diet Mixed diet Seed diet

Mean migration distance (latitudinal shift)

Percentage of species migrating

insect-eaters generally move longer distances, many wintering in the tropics and some south of the equator (Figure 16.4). The result is that insect-eaters are concentrated at more southern latitudes for their non-breeding season than seed-eaters. The same holds for New World migrants, in which most small insectivorous warblers winter in Central America (30 N 10 S, with fewer further south) and most seed-eaters further north (mostly 40 15 N) (Keast, 1995). Among these general relationships, specific exceptions occur, such as the seed-eating European Turtle Dove (Streptopelia turtur) which winters in Africa. As a second example, consider the various European raptors which also differ in the extent to which their foods remain available at high latitudes in winter (Newton, 1998b). Species can be divided according to whether they feed primarily on warm-blooded prey (birds and mammals which remain active and available in winter at high latitudes) or on cold-blooded prey (reptiles, amphibians and insects, which become inactive and unavailable in winter). Within each raptor group, the proportion of migratory species again increases with latitude, but at any one latitude, a larger proportion of the species that eat cold-blooded prey than of those that eat warm-blooded prey leaves for the winter, while species with mixed diets are intermediate (Table 16.1). The cold-blooded feeders also migrate furthest. The reasons for this difference are fairly obvious, in that species which eat cold-blooded prey and breed at high latitudes must winter in the tropics or Southern Hemisphere temperate areas if they are to have access to the same types of prey year-round. Of the 22 species of European raptors that eat mainly warm-blooded prey, most winter entirely within Europe and only one species (Booted Eagle (Hieraaetus pennatus)) winters largely in Africa (Table 16.1). Of the nine species that eat mainly cold-blooded prey, some winter partly in Europe and partly in Africa, but most winter entirely in Africa. Moreover, all six insectivorous species winter south of the Sahara, four of them entirely (and two largely) south of the equator, where the seasons are reversed. So most insectivorous species live in almost perpetual summer, in conditions in which they have easy access to their insect food supply year-round. Again, the 12 species with mixed diets show intermediate patterns. These findings again underline the link between migration and seasonal changes in specific food sources (Newton, 1979).

50 40 30 20 10 0 30

35

40

45 50 55 Latitude qN

60

65

70

Insect diet

50 Mixed diet

40 30

Seed diet

20 10 0 30

35

50 55 60 65 40 45 Central latitude of breeding range qN

70

FIGURE 16.4 Migration in relation to diet in European songbirds. Left. Proportion of species breeding at different latitudes which migrate south for the winter. Right. Distances moved by migrants as measured by the difference between the central latitudes of the breeding and wintering ranges. Lines calculated by regression analyses. From Newton (1995b).

TABLE 16.1 Wintering areas of European raptors in relation to diet. Figures show numbers of species in each category. Wintering area

Main prey types Warm-blooded

Mixed

Cold-blooded

North of Sahara

16

0

0

North and south of Sahara

5

8

2

South of Sahara

1

4

7

Significance of variation between categories (examined by Monte-Carlo randomisation test): χ 4 5 35.9, P , .001. Of 22 species that eat mainly warm-blooded prey, only one species (Booted Eagle (Hieraaetus pennatus)) winters almost entirely in Africa. In contrast, seven of nine species that eat mainly cold-blooded prey winter entirely in Africa. They include six insectivores, four of which winter entirely (and two largely) south of the equator, where the seasons are reversed. The 12 species with mixed diets show intermediate patterns. Source: From Newton (1998a). 2

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That movements are related to diet is also apparent in tropical regions, even though many such movements are relatively short. In tropical forests, nectar-eaters and fruit-eaters move around more than other species, probably because flowers and fruit are much more seasonal and patchy in occurrence than are the insects and other small creatures eaten by other birds (Morton, 1980; Levey & Stiles, 1992). Because flowers and fruit are generally more abundant in the canopy and forest edge, it is these parts of forest environments that show the greatest seasonal variation in their bird populations, the understorey species maintaining the most sedentary lifestyles year-round (see above). Species of open habitats, such as savannah and grassland, tend to fluctuate strongly through the year because such habitats tend to be more seasonal than forest, notably in rainfall, which affects the food supplies of most species.

Causes of latitudinal trend The trends discussed above provide strong circumstantial evidence for the overriding role of seasonal changes in food supplies (as influenced by seasonal changes in daylength and weather) as the main driver of migration patterns in birds. Further evidence along these lines is presented below. But this does not rule out a contributing role for other factors, such as competition, predation or parasitism. All these pressures may decline with increasing latitude because of the general latitudinal decline in the total numbers of animal species, whether these animals act as competitors, predators or parasites. At one time or another, all these factors have been proposed as contributing to the evolution of migration, or at least as favouring breeding at higher latitudes.

DISTRIBUTIONAL SHIFTS As implied already, the overall effect of bird migration is to alter the latitudinal distribution of birds between summer and winter so that species numbers in the Northern Hemisphere are at their greatest in the northern summer and in the Southern Hemisphere in the austral summer (northern winter). Take the west European migrants as an example. Some species move relatively short distances within Europe, but others move longer distances to Africa or southern Asia. But the net result, each autumn and spring, is a huge latitudinal shift in avifaunal distribution (Figure 16.5). In summer, the whole European assemblage of breeding landbirds is (by definition) concentrated north of 25 N, but in winter the same assemblage extends southwards as far as the southern tip of Africa (35 S). Forty-eight species of European birds reach the southern Cape of South Africa (Harrison et al., 1997), and some seabirds extend into the seas beyond. Many arctic-nesting species pass the northern winter largely in the Southern Hemisphere, including some populations of many shorebird species, three skuas Stercorarius, Arctic Tern (Sterna paradisaea) and other terns, Sabine’s Gull (Xema sabini) and others. They gain the advantage of summer conditions year-round.

Trends within species The above analyses (Figures 16.1 16.5) were based on the presence or absence of species at particular latitudes in the northern winter. They were therefore based only on complete migrants, while for purposes of analysis partial migrants (in which only a proportion of individuals leave for the winter) were counted as year-round residents. However, in many such species that breed over wide areas, a greater proportion of individuals migrate from higher than from lower latitudes. Thus some such species in the Northern Hemisphere are completely migratory in the north of their breeding range and completely sedentary in the south, while in intervening areas some individuals leave while others stay (partial migration). European examples include the Eurasian Blackbird (Turdus merula) and Peregrine Falcon (Falco peregrinus), and North American examples include the American Robin (Turdus migratorius) and Red-tailed Hawk (Buteo jamaicensis). In general, therefore, the extent to which any population migrates for the winter broadly corresponds to the degree of seasonal reduction in food supplies. Taking account of partial as well as complete migrants, the latitudinal trends discussed above would be even more marked.

ALTITUDINAL SHIFTS By moving a few hundred metres down a mountain slope, birds can achieve as much climatic benefit as by moving several hundred kilometres to lower latitudes, but without the extra winter daylength. Mirroring the latitudinal trend, with rising altitude increasing proportions of breeding species move out for the winter, but these altitudinal movements can be in any directions that reach lower ground. They occur on all major mountain ranges and can involve a large proportion of local montane species. Worldwide, at least 1238 bird species have been identified as altitudinal migrants, about

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FIGURE 16.5 Latitudinal shift between summer and winter distributions of bird species that breed in Europe. Includes wintering areas in Europe, Asia and Africa. From Newton (1995b).

10% of all bird species, but with huge regional variation (Barc¸ante et al., 2017). In the Himalayas, at least 65% of all species are thought to perform altitudinal migrations (Boyle, 2017). The height of the mountain range has some influence, but seasonal altitudinal movements occur even on relatively low mountains, such as the Great Dividing Range in southeast Australia, where several montane species appear in lowland towns and farms in winter (see later). Owing to such movements, the valleys and foothills of montane regions often hold a far greater variety of birds in winter than comparable areas of similar habitat in flatter terrain. Mountains provide opportunities for individual birds to exploit the different timings of vegetation growth, flowering, fruiting and insect emergence that occur within short distances at different elevations on the same slopes. At some times of year, montane species can also move downslope in response to spells of bad weather, moving back when weather improves. Some montane species appear to be obligate migrants, the entire population leaving for the non-breeding season, but most appear to be partial or facultative migrants moving over relatively short distances, varying from year to year. The main drivers of altitudinal migration as for latitudinal migration seem to be weather and food supplies. At high latitudes, mountains are often subject to strong winds and heavy snowfall, and at lower latitudes to torrential rainfall. On some tropical mountains, rain can pour down for several days at a time, and the total annual rainfall can often exceed 8 10 m. Most birds cannot feed effectively in heavy rain, resulting in their downslope movements for the nonbreeding period, and short-term down and up movements at other times of year (Boyle et al., 2010). Moreover, while most birds move to high elevations to breed, some species breed on lower ground and then move upslope for the non-breeding season, exploiting feeding opportunities that become available on higher ground in winter. Examples include the Dusky Grouse (Dendragapus obscurus) in western North America (Cade & Hoffman, 1993) and the Nene Goose (Branta sandvicensis) on Hawaii (Hess et al., 2012).

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All the above examples involved birds that changed altitude within the same general region, but in addition, some longerdistance migrants occupy habitats at different altitude zones in their widely separated breeding and wintering areas. For example the Golden-cheeked Warbler (Setophaga chrysoparia) breeds at elevations less than 600 m in Texas but winters in Central American highlands at elevations averaging greater than 1600 m (Rappole, 2013). The term altitudinal migrant has not usually been applied to such long-distance migrants whose summer and winter homes happen also to lie at different elevations.

ECOLOGICAL NICHES By remaining in the same general area year-round, non-migrants experience the full force of seasonal changes in local climate and food supplies. But migrants, in moving mainly to places with milder climate, can reduce the degree of seasonal fluctuation in the conditions to which they are exposed. In the extreme, some of those species which move to the opposite hemisphere in the non-breeding season can find similar conditions year-round: they live in almost perpetual summer, the Arctic Tern (Sterna paradisaea) being a striking example. Nevertheless, more than 80% of 355 bird species migrating through Eurasian African flyways showed little or no overlap between their breeding and non-breeding climatic niches (Ponti et al., 2020). In general, the difference in climatic niche between breeding and non-breeding areas increased with increasing migration distance, as might have been expected (see also Dufour et al., 2020). Climate aside, to judge from written accounts, most species seem to have similar ecology in their breeding and wintering areas. They occupy habitats of similar structure and take similar types of foods in similar ways. The actual plant species that comprise the habitat, or the plant or animal species that comprise the diet, may differ between breeding and wintering areas, but superficially they look much the same, whether in tree-less habitats or forests. However, some bird species seem to occupy a wider structural range of habitats in the non-breeding season, while others make marked switches in habitat types between seasons. They may move, say, from inland wetland to open ocean, open tundra to seashore, or forest to scrub, or they make switches in the types of foods eaten, such as animal to plant material (insects to seeds). Extreme examples include the sandpipers that switch from tundra to seashore and from insects to worms and molluscs or the skuas that switch from tundra to ocean and from lemmings to fish, or the sea ducks that switch from freshwater lakes to open sea and from soft-bodied insects to hard-shelled molluscs. The term; niche-tracker’ is used for species which occupy areas of similar climate or habitat yearround, and ‘niche switcher’ for those that occupy areas of markedly different climate or habitat in breeding and non-breeding seasons. Particular species can be niche trackers in terms of climate and niche switchers in terms of habitat, or vice versa. Hypotheses regarding the evolution of migration would generally predict ‘niche-following’ as primitive, and ‘niche-switching’ as derived, and thus as representing a step in the evolution of these species, and not just in their migration patterns.

COMPARISONS BETWEEN HEMISPHERES Migration of landbirds from their breeding areas is a much more obvious phenomenon in the northern than in the Southern Hemisphere. This is partly because habitable land covers three times the area in the Northern Hemisphere than in the Southern Hemisphere, and the difference is most marked at high latitudes (we can ignore Antarctica because it holds no landbirds, only seabirds) (Figure 16.6). In North America, Greenland and Eurasia, some landbird habitat extends north of 80 N, but in the Southern Hemisphere, South America reaches only to 55 S, Africa to 35 S, Australia to 43 S and New Zealand to 47 S. The net result is that latitudes 30 80 N hold 15 times more land than do latitudes 30 80 S, and it is at these latitudes that winters are coldest, and migration is most developed (for discussion of area effects in South America, see Chesser, 1994; and in Australia, see Chan, 2001). The greater latitudinal spread of land in the Northern Hemisphere results in generally longer journeys than are undertaken by Southern Hemisphere breeders, which are closer to the equator year-round. These factors are likely to explain the reduced prevalence of migration in the Southern Hemisphere and the relative proximity of breeding and non-breeding ranges typical of many Southern Hemisphere migrants (Chesser, 1994; Jahn et al., 2004; Dingle, 2008; Somveille et al., 2013). Another factor is temperature, which has a steeper downward gradient north of the equator than south of it. For example in the New World the mean midwinter (January) temperature at the Tropic of Cancer is about 13 C, while the mean midwinter temperature (July) at the Tropic of Capricorn is 16 C, a 3 C difference. Yet at 50 N in North America, the mean midwinter temperature is 15 C, while at 50 S in South America, it is 0 C, a 15 C difference. Similar hemisphere differences are apparent in much of the Old World too. This temperature differential may result from the wider sea area in the Southern Hemisphere, buffering seasonal temperature extremes. It may explain why greater proportions of species leave from temperate latitudes in the Northern Hemisphere than in the Southern Hemisphere. For example, about 29% of species leave completely for the winter from Morocco, but only 6% of species

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The Migration Ecology of Birds

(a)

(b)

FIGURE 16.6 The greater land areas in the northern than in the Southern Hemisphere, shown by land area (a) and habitats (b). The habitats refer to vegetation zones before human impact, only parts of which still remain. From Rosenzweig (1992).

leave from equivalent latitudes around the Cape in South Africa (Newton & Dale, 1996a,b; Harrison et al., 1997). It is presumably largely for both these land-related and temperature-related reasons that landbird migration is much more marked in the northern than in the Southern Hemisphere (see also Dingle, 2008; Somveille et al., 2013). While many landbird species that breed in the Northern Hemisphere migrate south of the tropics, no landbird species that breeds in the Southern Hemisphere moves north of the tropics. This difference in long-distance migration might also result from the difference in available land areas between the two hemispheres. Birds migrating south from the northern continents encounter progressively smaller habitable land areas, which could force some individuals to extend far to the south. In general, the numbers of migrants from the northern continents decline with increasing distance southwards into the southern continents, as more and more species settle for the winter. In contrast, birds migrating northward from the southern parts of the southern continents encounter widening land areas, so may need to move less far north before they find sufficient wintering habitat. In Africa, no breeding landbird species migrates north of the Sahara, in South America none (apart from stragglers) reach as far north as Mexico, and in Australasia none migrate north of New Guinea. It is not that birds which breed in the Southern Hemisphere do not move around, but rather that most migration is short-distance and partial (involving only part of a population), altitudinal (and also short-distance) or nomadic (as birds concentrate locally in line with sporadic rainfall patterns). Relatively few species make regular longdistance moves. It remains to be discovered to what extent the two sets of migrants, from northern and southern regions, occupy the same niches in the tropics but at different times of the year. Pelagic seabirds provide a telling contrast with landbirds in the extent of seasonal migration. The reduced land areas in the Southern Hemisphere mean that the sea areas are correspondingly more extensive than in the Northern Hemisphere. Linked with these greater sea areas and large numbers of scattered island breeding sites, pelagic seabirds are much more numerous in the Southern Hemisphere than in the northern, both species and individuals. Correspondingly, a greater proportion of southern than Northern Hemisphere breeding seabird species make long migrations. Five (11%) of 47 species that breed north of the tropics extend to south of the tropics in the northern winter, whereas 14 (23%) of 61 species that breed south of the tropics extend to north of the tropics in the austral winter (calculated from maps in Harrison, 1983). The implication is again that the sheer numbers of birds, in relation to the habitat available, influence the distances moved and area occupied outside the breeding season.

Populations in both hemispheres Very few migratory bird species have separate breeding populations north and south of the tropics. Examples include the Little Tern (Sterna albifrons) and Whiskered Tern (Chlidonias hybridus) in Asia Australia, the Black Stork (Ciconia nigra) and Booted Eagle in Europe Africa, and the Turkey Vulture (Cathartes aura) and Black Vulture (Coragyps atratus) in North South America. In all these species, the northern birds winter in the south when the southern birds are breeding, but among the terns, the southern birds also winter in the north when the northern birds are breeding. It is as though there is a single population of terns occupying the same range but with part of the population breeding at one end of the migratory terminal and another part at the other end. In each area, terns from each population can be distinguished according to whether they are in breeding or non-breeding plumage.

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RELATIONSHIP BETWEEN BREEDING AND WINTERING AREAS Patterns in distribution In most bird species, breeding and wintering ranges are coincident or overlapping, while smaller numbers show a latitudinal gap between the two, differing in extent between species (Figures 16.7 and 16.8, Table 16.2). In both Old and 1. Resident year-round throughout the entire latitudinal span of the range.

FIGURE 16.7 Main migration patterns found in Northern Hemisphere birds, based on the degree of separation between breeding and wintering ranges. See also Table 16.2.

2. Present in summer only in the northern part of the range, and year-round in the southern part.

3. Present year-round only in the northern part of the range, and in winter only in the southern part.

4. Present in summer only in the northern part of the range, year-round at intermediate latitudes, and in winter only in the southern part.

5. Summer range immediately to the north of the winter range, with little or no overlap.

6. Summer range separated from winter range by a latitudinal gap in which the species occurs only on passage.

FIGURE 16.8 Frequency distribution of latitudinal gaps between breeding and wintering ranges, calculated for west Palaearctic breeding birds. C, coincident; O, overlapping; A, adjacent.

200

Number of species

175 150 125 100 75 50 25 0 C

0 A 5 10 15 20 25 30 35 40 45 50 55 Degree gap between breeding and wintering ranges

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The Migration Ecology of Birds

TABLE 16.2 Migration patterns of birds in the Northern Hemisphere, arranged roughly in order of decreasing segregation of breeding and wintering ranges. Total no. in each categorya 1. Present year-round throughout their whole latitudinal range

Old World examples: Black Grouse (Tetrao tetrix), Eurasian Green Woodpecker (Picus viridis), Black-billed Magpie (Pica pica), House Sparrow (Passer domesticus)

195

New World examples: Ruffed Grouse (Banasa umbellus), Northern Bobwhite (Colinus virginianus), Common Raven (Corvus corax), Carolina Wren (Thryothorus ludovicianus)

64

Old World examples: Common Wood-pigeon (Columba palumbus), Eurasian Skylark (Alauda arvensis), European Serin (Serinus serinus), European Robin (Erithacus rubecula)

22

New World examples: Red-tailed Hawk (Buteo jamaicensis), Common Moorhen (Gallinula chloropus), Blue Jay (Cyanocitta cristata), Common Grackle (Quiscalus quiscula)

47

Old World examples: Eurasian Blackbird (Turdus merula), Siberian Tit (Parus cinctus), Willow Tit (Parus montanus), Pine Grosbeak (Pinicola enucleator)

21

New World examples: Evening Grosbeak (Hesperiphona vespertina), House Finch (Carpodacus mexicanus)

23

4. Present only during the summer breeding season in the north of their range, year-round at intermediate latitudes, and only during winter in the south

Old World examples: Eurasian Woodcock (Scolopax rusticola), Rook (Corvus frugilegus), Redwing (Turdus iliacus), Common Starling (Sturnus vulgaris)

111

New World examples: Canada Goose (Branta canadensis), Short-eared Owl (Asio flammeus), Cooper’s Hawk (Accipiter cooperii), Song Sparrow (Melospiza melodia)

52

5. Summer breeding range immediately to the north of the wintering range

Old World examples: Ruddy Turnstone (Arenaria interpres), Great-spotted Cuckoo (Clamator glandarius), Bluethroat (Luscinia svecica), Ring Ouzel (Turdus torquatus)

22

New World examples: Red-breasted Merganser (Mergus serrator), House Wren (Troglodytes aedon), Yellowthroated Warbler (Setophaga dominica), Vesper Sparrow (Pooecetes gramineus)

34

Old World examples: Arctic Tern (Sterna paradisaea), Eurasian Dotterel (Charadrius morinellus), Sanderling (Calidris alba), Red-footed Falcon (Falco vespertinus), Lesser Grey Shrike (Lanius minor), Icterine Warbler (Hippolais icterina)

117

New World examples: Whistling Swan (Cygnus c. columbianus), Brent Goose (Branta bernicla), Swainson’s Hawk (Buteo swainsoni), Long-tailed Jaeger (Stercorarius longicaudus), Iceland Gull (Larus glaucoides), Baird’s Sandpiper (Calidris bairdii), Bristle-thighed Curlew (Numenius tahitiensis), Snow Bunting (Plectrophenax nivalis)

144

2. Present only during the summer breeding season in the north of their range, year-round in the south

3. Present year-round in the north of the range, only during winter in the south

6. Summer breeding range separated geographically from the wintering range by a gap in which the species occurs only on passage. Some of these species cross large stretches of inhospitable sea or desert in which they cannot feed during migration

a The proportions in the six categories differ significantly between western Europe-Africa and eastern North America-South America (χ25 5 85.7, P , .001), reflecting mainly the smaller proportions of class 1 species, and the greater proportions of classes 5 and 6 species, in North America. The three species of Southern Hemisphere seabirds that spend the northern summer (austral winter) off Europe, and the eight that spend the northern summer off eastern North America, are excluded from analysis.

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New Worlds, the greatest separation of breeding and wintering ranges is found, as expected, in species that breed only at high latitudes in one hemisphere and winter only at high latitudes in the opposite hemisphere. Among landbirds, the Swainson’s Hawk (Buteo swainsoni) is one of the most extreme examples, as it breeds between 25 and 65 N in North America and winters between 24 and 40 S in South America, giving a 49 latitudinal gap between breeding and wintering ranges (apart from small numbers that winter in parts of the southern USA). Among seabirds, the Arctic Tern is the most extreme example, breeding between about 50 and 80 N and wintering between about 40 and 70 S, giving a 90 latitudinal gap between breeding and wintering ranges.

Comparison of sizes of breeding and wintering areas Whether overlapping or separate, those migratory species that have the largest breeding ranges also tend to have the largest wintering ranges, and vice versa (Newton, 1995a). This point is illustrated in Figure 16.9 for 57 species of landbirds that breed entirely within Eurasia and winter entirely within Africa so that their breeding and wintering ranges are completely separated. As another reflection of the same phenomenon, European landbirds and freshwater birds which breed over the widest span of latitude also winter, and vice versa (Figure 16.10). These correlations may have their basis in the ecology of the species themselves, in that those species that have the widest climatic and habitat tolerances may be able to spread over the largest areas, summer and winter. Alternatively, the correlations may depend on the abundance of the species concerned, in that those that have the largest populations (for whatever reason) spread over the largest areas, summer and winter (Newton, 1995a). These two explanations are not mutually exclusive, and in practice are difficult to separate. The correlations between sizes (or latitudinal spans) of breeding and wintering areas hold only as general tendencies, however, and some species do not fit the overall patterns. Moreover, because of the geographical scale involved, (a) 10 9 8 7 6 5 4 3 2 1 0

FIGURE 16.9 (a, b) Sizes of breeding and wintering ranges of 57 landbird species which breed entirely in Eurasia and winter entirely in Africa. (c) Relationship between sizes of breeding and wintering ranges of the same 57 species. Warblers are shown separately as open circles. From Newton (1995a).

Number of species

Breeding range

2

4

6

8

10 12 14 16 18

20

22

24 26 28 30 32 34

8

10 12 14 16 18

20

22

24 26 28 30 32 34

Number of species

(b) 10 9 8 7 6 5 4 3 2 1 0

Wintering range

4

2

6

Range (km2

1 000 000)

(c) Wintering range (km2 106)

22 18 14 10 6 2 0

2

4

6

8

10

12

14 16 18 20

22 24 26 28 30 32 34

Breeding range (km2 106)

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FIGURE 16.10 Relationship between the latitudinal spans of breeding and wintering ranges of west Palaearctic breeding birds. Some species winter entirely in the west Palaearctic and others partly or entirely in Africa. Excludes seabirds. Spots show mean values, and lines show one standard error and one standard deviation on either side of the mean. The lack of relationship in coastal birds can be attributed to the fact that in winter they switch from an areal distribution in inland areas to a linear distribution along coastlines, often with a very wide latitudinal spread. From Newton & Dale (1997).

measures of range size can only be crude and take no account of areas within the range that lack suitable habitat. They also take no account of the fact that the bulk of the population may occupy only part of the winter range at one time, either shifting south during the course of the northern winter or occurring at any one time only in those parts where rainfall or other factors have created suitable conditions (Chapter 17). Despite the general correlation between the sizes of breeding and wintering areas, in about 69% of Eurasian African migrants the breeding range is noticeably larger than the wintering range. This percentage is significantly greater than the expected 50% (chi2 5 4.0, P , .05). The most extreme example is the Lesser Grey Shrike (Lanius minor), whose breeding range in Eurasia covers an area at least seven times greater than its known wintering range in southwest Africa, which is centred on the Kalahari basin. In contrast, in only 31% of species is the wintering range larger than the breeding range. The most extreme examples include the Olive-tree Warbler (Hippolais olivetorum) and Subalpine Warbler (Curruca cantillans) whose known wintering ranges cover more than twice the area of their respective breeding ranges. However, these low-density species are little known in Africa, and their effective wintering ranges may have been overestimated by the inclusion of records of vagrants or occurrences in occasional years only. For the 57 Eurasian Afrotropical landbird migrants as a whole, however, wintering ranges are, on average, about one-third smaller than breeding ranges, and in some species only parts of the wintering range may be occupied at any one time (Figure 16.9). These findings imply that most species live at greater densities in their African wintering areas than in their Eurasian breeding areas, but whether this reflects differences in available land area, or in the per unit area capacities of the two regions to support the birds at the times they are present remains unknown. It may be that individual birds need more space in Eurasia when they are feeding young than in Africa when they have only themselves to feed. Moreau (1972) estimated that, owing to warmer weather, the individual daily energy needs of passerines in Africa were about 60% of their breeding season needs. Whatever the reason for the differences between sizes of breeding and wintering ranges, a similar phenomenon occurs in the New World, where migrants from large parts of North America concentrate each winter in a relatively small area in the northern neotropics. Here the impacts of geography and land areas on range sizes are shown even more clearly than in the Eurasian African species. Eighty-four out of 89

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neotropical songbird migrants breeding in eastern North America have wintering ranges averaging half the size of their breeding ranges; in only five species are the wintering ranges larger (Mills, 2006). Nevertheless, the sizes of breeding and wintering ranges of different species are broadly correlated. Among wetland birds (waterfowl and waders) that winter in inland areas, the sizes of breeding and wintering ranges are also correlated, but in contrast to landbirds, wintering ranges are generally larger and cover a greater latitudinal span (Figure 16.10). This may be because, as wetlands become scarcer southwards (from tundra to savannah), freshwater birds have to spread over greater areas than landbirds in winter to find enough suitable habitat. Freshwater birds may also make longer movements within a winter than most landbirds, in response to rainfall patterns (Newton & Dale, 1997). It is hard to get an appropriate measure of the availability of shallow (and often temporary) wetlands in Africa, compared to Eurasia. The total annual renewable water resource, calculated as the ‘average annual flow of rivers and groundwater generated from endogenous precipitation’, was given by the World Resources Institute (1994) as 4184 km3 for Africa, compared with 17219 km3 for Eurasia. This translates to 0.14 km3 per km2 of land area in Africa and 0.32 km3 per km2 of land area in Eurasia, more than a twofold difference between these land masses. Moreover, greater evaporation in Africa would greatly increase this difference in terms of surface water, and the big variations in rainfall, both from year to year and from place to place, would further contribute to the sporadic nature of much wetland habitat in Africa. Most shorebird species switch from an expansive distribution on the tundra in summer to a linear distribution on coastlines in winter (Newton & Dale, 1997). They therefore breed only in a narrow span of latitude, mostly between 70 and 80 N, but in winter extend southwards over 116 of latitude between about 60 N and 56 S, reaching the southern tip of Africa (35 S), Australasia (47 S) or South America (56 S). Some species, such as Ruddy Turnstone (Arenaria interpres), can be found in winter on many a rocky coast within this wide latitudinal span, while others, such as Red Knot (Calidris canutus), may be restricted to the relatively few extensive mudflats offering suitable conditions. Because of the seasonal switch in habitat, it is difficult to compare the sizes of their breeding and non-breeding ranges but, as a group, shorebirds show no relationship between the latitudinal extents of breeding and non-breeding ranges (Figure 16.10). Overall, then, the correlation between summer and winter range sizes is most obvious in non-coastal landbirds.

MIGRATION WITHIN THE SOUTHERN CONTINENTS Excluding Antarctica, the Southern Hemisphere contains only about one-third of the land area of the Northern Hemisphere and little of this extends into temperate regions. So most parts of the southern continents escape cold winters, yet span a wide enough range of latitude to accommodate the native bird species year-round. Apart from the seasonal influx of birds from the northern continents, therefore, the southern continents have self-contained migration systems (Dingle, 2008). On all the southern continents, the north south migrations of the local breeding birds (austral migrants) more or less coincide with the north south movements of the inter-continental migrants from the Northern Hemisphere, because the movements of both groups are driven by the same seasonal changes in climate and food supplies. However, away from the equatorial rainforests, bird movements are linked not so much to temperature as to the corresponding wet dry seasons, and the predictability or otherwise of rainfall. The migrations of many species are relatively short-distance and partial, so are often hard to detect without special study. Nevertheless, some species cross the equator on seasonal journeys exceeding 2000 km. Differences in the ecological circumstances prevailing between the three southern continents impose some broad-scale differences in their bird migration patterns.

Africa Rainfall and vegetation zones in Africa mirror one another on both sides of the equator, progressing from rainforest in the wettest equatorial regions, through deciduous woodland to increasingly dry savannahs and grasslands, and then desert (Chapter 26). In consequence, many birds can find equivalent habitat on both sides of the equator, and because the wet seasons are reversed between north and south sides, they can, by migrating between the northern and southern tropics, benefit from the wet seasons in both. Some species breed in the northern tropics and spend their non-breeding season in the southern tropics. Others breed in the southern tropics and spend their non-breeding season in the northern tropics. Yet others have separate breeding populations both north and south of the equator, each crossing to the other side on migration (Figure 16.11).

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FIGURE 16.11 Diagrammatic representation of the main migration patterns within Africa, and between Africa and Europe. Examples include partial migrants. - breeding to wintering area. 1. Within the northern tropics, breeding in the northern wet season: Examples: Grasshopper Buzzard Eagle (Butastur rufipennis), White-throated Bee-eater (Merops albicollis), African Collared Dove (Streptopelia roseogrisea), Red-shouldered Cuckooshrike (Campephaga phoenicea). 2. Within the southern tropical temperate zone, breeding in the southern wet season: Examples: Fiscal Flycatcher (Melaenornis silens), Greater Striped Swallow (Hirundo cucullata), Black Cuckooshrike (Campephaga flava), Square-tailed Nightjar (Caprimulgus fossii). 3. Within both the northern and the southern tropics, migrating nearer to the equator for the dry season: Examples: Spotted Ground Thrush (Zoothera guttata), African Striped Cuckoo (Oxylophus levaillantia), Woodland Kingfisher (Halcyon senegalensis). 4. Transequatorial migration, breeding in the northern wet season: Examples: Abdim’s Stork (Ciconia abdimii), Lesser Crested tern (Sterna bengalensis), Plain Nightjar (Caprimulgus inornatus), Dusky Lark (Pinarocorys nigricans). 5. Transequatorial migration, breeding in the southern wet season: Examples: Openbill Stork (African Openbill) (Anastomus lamelligerus), Standard-winged Nightjar (Caprimulgus longipennis), Pennant-winged Nightjar (Macrodipteryx. vexillarius). 6. Transequatorial migration with two populations, one breeding in the northern wet season and the other in the southern wet season: Examples: Black Kite (Milvus migrans), Wahlberg’s Eagle (Aquila wahlbergi), Jacobin Cuckoo (Oxylophus jacobinus). 7. Eurasian-northern tropics, breeding in the Eurasian warm season: Examples: Melodious Warbler (Hippolais polyglotta), European Pied Flycatcher (Ficedula hypoleuca), Woodchat Shrike (Lanius senator), European Turtle Dove (Streptopelia turtur). 8. Eurasian-southern tropics, breeding in the Eurasian warm season: Examples: Icterine Warbler (Hippolais icterina), Barn Swallow (Hirundo rustica), Common Swift (Apus apus), Red-footed Falcon (Falco vespertinus).

More than 500 African breeding species migrate within the continent (Curry-Lindahl, 1981). Those that cross the equator to equivalent habitats on the other side are relatively few in number, and most move entirely within the northern tropics, or entirely within the southern tropical and temperate zones. In each case, the general trend is for species to move towards wetter (lower latitude) areas for the dry season (Figure 16.11; for raptors, see Figure 16.12). In addition, in the mountainous areas of the east and south, many species make seasonal altitudinal movements. For example in Natal in southern Africa, no less than 76 species have been described as altitudinal migrants (Johnson & MacLean, 1994). In Africa, as in Europe, the proportions of species in each region that are migratory are related to the average temperature of the coldest month (Hockey, 2000). In regions where this temperature exceeds 20 C, less than 10% of species are migratory. The likelihood of any one species being migratory again depends on its diet, with frugivores being mainly sedentary and insectivores migratory. This applies particularly to those species that eat aerial insects (swallows, swifts, nightjars), large active insects (halcyonid kingfishers and rollers) or larvae of large flying insects (cuckoos). Over the entire latitudinal range from northern Europe to southern Africa, a strong linear relationship exists between the proportion (P) of birds that are resident and the mean temperature of the coldest month (P 5 1.92 T 1 53.66, r2 5 0.96, df 5 19, P , .001, Hockey, 2000). This extends the relationship discussed above for European birds alone.

South America The mirror-image symmetry of vegetation zones north and south of the equator, which is so marked in Africa, is less prominent in South America, where altitude effects on climate and vegetation are greater. Correspondingly, smaller proportions of South American breeding species are known to undertake transequatorial migrations (although this may be partly due to inadequate information). As in Africa, most movements involve species moving to lower latitude areas for the non-breeding season (Levey & Stiles, 1992; Joseph, 1997; Jahn et al., 2004, 2020). For some species, this can still involve trans-equatorial movements exceeding 2000 km each way. Other species move on a west east axis, notably water birds which breed in the interior and winter on the coast. As expected, many species in the Andes where winters can be harsh, move to lower elevations for the non-breeding season. Most migration takes place within the continent, although some species may reach the Caribbean Islands in winter.

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FIGURE 16.12 Seasonal changes in the distribution of four migratory raptors in West Africa. Dark shading frequent sightings, light shading infrequent sightings. In this region, migratory raptors stay in the southern woodlands during the local dry season, while food is plentiful and hunting conditions are good. When it rains heavily and the grass grows rapidly to 1.3 m high, the migrants move north to the short grass areas, where the rains are later and lighter and produce less growth of vegetation. The birds thus manage to remain in a fairly favourable environment all year and, while in the north, they breed, taking advantage of a short seasonal surplus of food which is not fully utilized by the sparse resident population. Species differ in the extent of their migrations, and in the periods spent at different latitudes, depending on their particular needs, but the general northward passage occurs at the start of the rains in ‘spring’ and the southward passage at the end of the rains in ‘autumn’. From Thiollay (1978).

Estimates of the numbers of intra-continental migrants in South America range from 220 to 237 species, compared with 318 species of inter-continental (Nearctic Neotropical) migrants (Rappole, 1995). The South American figures are almost certainly underestimated, considering the richness of the avifauna and the inadequate state of knowledge. One-third of all known migratory species belong to the Tyrannidae (New World Flycatchers), reflecting the overall preponderance of this family across the continent and their dependence on flying insects (Chesser, 1994; Jahn et al., 2004). In recent years, the use of geolocators on some South American breeding species has revealed other long migrations, with some species using two or more areas in succession during the non-breeding period (Jahn et al., 2020). Even though the equator passes through Brazil, on current information at least 198 (10.3%) of 1919 species breeding there are migratory or partial migratory (Somenzari & Whitney 2018). Further south, at higher latitudes in Tierra del Fuego, about 50% of breeding birds are migratory (Humphrey et al., 1970).

Australasia Migration within the Australo-Papuan region is largely self-contained, as no landbird species breeding there is known to migrate beyond Wallace’s Line in Lombok in southernmost Indonesia (Dingle, 2008). The sparsity of people over most of the region, and limited bird ringing means that information on migration is based mainly on seasonal numerical and distributional changes. On this basis, about 163 Australian landbird species are known to migrate in at least part of

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their range. Conspicuous partial migration occurs in about 44% of 155 non-passerine species and 32% of 317 passerines examined (or about 40% overall, Chan, 2001). Similar findings emerged from bird count data from eastern Australia in which 36% (146/407) of species were detected as making movements (Griffioen & Clarke, 2002). East of the Great Dividing Range, rainfall is generally adequate, and seasonal temperature changes largely influence seasonal productivity. Birds move northward toward the subtropics and tropics for the winter. Some species in the southern parts of their range are completely migratory, but many species are partial migrants occupying much the same geographical range year-round, but showing seasonal south north shifts in numbers, mostly over distances of less than 1000 km. Eastern examples include the Scarlet Myzomela (Myzomela sanguinolenta) and Yellow-faced Honeyeater (Caligavis chrysops) (Clarke et al., 1999; Munro, 2003). Nevertheless, some species perform longer movements. They include the many water birds that migrate from Australia to New Guinea in the non-breeding season, including egrets, ibises, pelicans and ducks. For three species of egrets that come from southeastern Australia, this entails a journey of more than 3000 km (Geering & French, 1998). Forest-dwelling species that move between Australia and New Guinea include the Pied Imperial Pigeon (Ducula bicolor), Metallic Starling (Aplonis metallica), Buff-breasted Paradise Kingfisher (Tanysiptera sylvia) and others (Roshier & Joseph, 2014). In the south, at least five species leave Tasmania completely for the winter, spending their non-breeding season in Australia or beyond, namely the Swift Parrot (Lathamus discolor), Orange-breasted Parrot (Neophema chrysogaster), Pallid Cuckoo (Cacomantis pallidus), Shining Bronze-Cuckoo (Chrysococcyx minutillus) and Satin Flycatcher (Myiagra cyanoleuca) (Chan, 2001; Dingle, 2004). Other eastern species are altitudinal migrants on the Great Dividing Range. They include such conspicuous species as Yellow-tailed Black Cockatoo (Calyptorhynchus funereus), Golden Whistler (Pachycephala pectoralis) and Regent Bowerbird (Sericulus chrysocephalus). Whereas these species move to lower ground for the winter, others, such as the Eastern Spinebill (Acanthorhynchus tenuirostris), move uphill to exploit (Banksia collina) pollen at higher elevations in winter. Except for the monsoonal north and small areas in the southwest and south-centre that have a Mediterranean-like climate, rainfall over most of Australia west of the Dividing Range is sparse and erratic, making it the driest continent overall. Because bird breeding in these circumstances is frequently tied to erratic rainfall, migration can be complex and variable, but many species show an underlying north south pattern (Nix, 1976; Chapter 17). Comparing different parts of Australia, the proportions of birds that are migratory decline with increase in the amount and evenness of the annual rainfall. Where the annual total exceeds 125 cm and is well distributed through the year, 70% 85% of honeyeater species (Meliphagidae) are year-round residents, but in the central desert, where annual rainfall is 20 28 cm and erratic, fewer than 50% are residents, and many seem to perform nomadic movements in response to patchiness in rainfall (Keast, 1968; Chapter 17). New Zealand now holds relatively few native landbird species, and only three of these spend the winter elsewhere. They include the Pacific Long-tailed Cuckoo (Eudynamis taittensis) which winters in a wide arc of islands from New Guinea across the Marshall and Caroline Islands to the Marquesas in the east; the Shining Bronze-Cuckoo (Chrysococcyx lucidus) which migrates to the Bismarcks and Solomons; and the Double-banded Plover (Charadrius bicinctus) which migrates to southeast Australia for the winter. The last two species also breed within Australia. Many of the remaining species in New Zealand migrate within the country.

CONCLUDING REMARKS The overriding role of food supplies in influencing the movement patterns of birds is evident from (1) the link between migration and climatic seasonality, with greater proportions of migrants in increasingly seasonal environments; (2) the relationship in different species between migration and diet; (3) within species, the regional variations in the proportions of individuals that leave for the non-breeding season, with more birds leaving the most seasonal environments; (4) the locations of wintering areas; and (5) the precise seasonal timing of movements, such that birds are absent from breeding areas at a time when their particular foods are scarce there (Chapter 15). Some authors have stressed the role of climate and competition in influencing migration patterns, but both these factors are likely to act primarily through the food supply (see Chapter 25 for effects of competition). Any role that predation and parasitism might play supposedly acts through reduction in the importance of these factors with increasing latitude. Migratory habits are so closely related to diet and to the seasonal fluctuations in the food types involved that it is hard to tell whether any other factors have any influence beyond those that act through food. The main problem is that diet is related to almost all aspects of the morphology, ecology and behaviour of birds, as well as to migration, so any factor could seem to be important to migration through association.

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In species that migrate between the northern and the Southern Hemispheres, the question arises why the same individuals do not breed twice in 1 year, in both summer and winter quarters. One reason in many species is that individuals moult while in winter quarters, a process that takes several weeks or months and could not be undertaken at the same time as breeding (Chapter 12). Another reason is that many migratory species do not remain for long in the same area in winter but periodically move on as food supplies become depleted (Chapters 15, 26). This exploitation of temporary abundances is one way in which migrants in the Southern Hemisphere could avoid competing with the local residents which, breeding at that time, are tied to fixed nesting areas. Neither explanation applies to all migratory species, however, and there are still some that are sedentary while they are in both breeding and wintering areas, and would seem able to breed in both, 6 months apart but do not. A related question is why many birds, having had a winter break, do not breed more than once at different localities on their migration routes. Migrants that travel in spring northward through Europe and North America, and have short breeding cycles, would seem able to breed in the southern parts of these continents, before moving on to breed again further north. They could then raise a greater number of young per year than by exploiting only the short favourable season in the north. The fact that a few species are known to do this (see Chapter 17) makes it even harder to explain why most do not. However, some have breeding cycles too long to fit two in a year, and many others have competing conspecifics nesting at lower latitudes where they can raise two or more broods in a season.

SUMMARY Migration is most pronounced in environments in which food supplies vary greatly through the year, in regions with the greatest difference between warm and cold seasons or between wet and dry seasons. It enables birds to exploit seasonal abundances and avoid seasonal shortages. Broadly speaking, birds move to keep themselves in favourable habitat for as much of the year as possible, allowing for the fact that their requirements may differ between the breeding and nonbreeding seasons. The proportions of breeding species that leave for the winter increase with latitude, as winters become more severe and seasonal changes in food availability more marked. At any particular latitude, migration is also related to diet; only species whose food remains available year-round can stay there in winter. Migrations cause huge seasonal latitudinal and, to some extent, longitudinal changes in the distributions of birds. From low to high latitudes, a progressively greater proportion of breeding species leave for the winter, and few species remain in winter north of the tree line. In mountain regions, many bird species migrate from high to lower ground for the winter, and back again in spring. Most latitudinal migrants occupy larger geographical ranges in the breeding season than in the non-breeding season when populations become more concentrated, but across species, the sizes of breeding and wintering ranges are correlated. The main exceptions include many shorebirds which breed over wide continental areas and switch in the non-breeding season to linear distributions along coastlines. Among landbirds, migration is much more marked in the northern than in the Southern Hemisphere. This is associated mainly with the far greater land areas in the Northern Hemisphere, especially between latitudes 30o and 80 N, % continents where migration is most developed. Many landbirds from the northern continents migrate into the southern for the non-breeding season, but none from the southern continents migrate into the northern continents. In the southern continents, most migration is short-distance and partial, altitudinal or nomadic. Among pelagic birds, in contrast, migration is more marked among Southern Hemisphere species, many of which spend their non-breeding season in the Northern Hemisphere. This is associated with the greater sea areas and more abundant nesting islands in the Southern Hemisphere, which support much greater numbers of seabirds there. Few Northern Hemisphere seabirds migrate beyond the southern tropics, but many southern ones migrate beyond the northern tropics.

REFERENCES Barc¸ante, L., Vale, M. M. & Alves, M. A. S. (2017). Altitudinal migration by birds: a review of the literature and a comprehensive list of species. J. Field. Ornithol. 88: 321 35. Boyle, W. A. (2017). Altitudinal bird migration in North America. Auk 134: 443 65. Boyle, W. A., Norris, D. R. & Gugliemo, C. G. (2010). Storms drive altitudinal migration in a tropical bird. Proc. R. Soc. B 277: 2511 19. Cade, B. S. & Hoffman, R. W. (1993). Differential migration of Blue Grouse in Colorado. Auk 110: 70 7.

Chan, K. (2001). Partial migration of Australian landbirds: a review. Emu 100: 281 92. Chesser, R. T. (1994). Migration in South America: an overview of the austral system. Bird Conserv. Int. 4: 91 107. Chesser, R. T. (1998). Further perspectives on the breeding distribution of migratory birds: South American austral migrant flycatchers. J. Anim. Ecol. 67: 69 77. Clarke, M. F., Griffioen, P. & Loyn, R. H. (1999). Where do all the bush birds go? Wingspan 9: 1 16.

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Curry-Lindahl, K. (1981). Bird migration in Africa. Movements between six continents. London, Academic Press. Dingle, H. (2004). The Australo-Papuan bird migration system: another consequence of Wallace’s Line. Emu 104: 95 108. Dingle, H. (2008). Bird migration in the southern hemispehere: a review comparing continents. Emu 108: 341 59. Dufour, P., Deschamps, S., Chantepie, S., Renaud, J. Gue´guen, M. et al. (2020). Reconstructing the geographic and climatic origins of longdistance bird migrations. J. Biogeog. 47: 155 66. Geering, D. & French, K. (1998). Breeding biology of the Regent Honeyeater Xanthomyza phrygia in the Capertee Valley, New South Wales. Emu 98: 104 16. Griffioen, P. A. & Clarke, M. F. (2002). Large-scale bird-movement patterns evident in eastern Australian atlas data. Emu 102: 97 125. Harrison, J. A., Allan, D. G., Underhill, L. G., Herremans, M. Tree, A. J., et al. (1997). The atlas of Southern African birds. Vol. Vols. 1 & 2. Johnannesburg, Birdlife South Africa. Harrison, P. (1983). Seabirds. An identification guide. Beckenham, Kent, Croom Helm. Herrera, C. M. (1978). Ecological correlates of residence and nonresidence in a Mediterranean passerine bird community. J. Anim. Ecol. 47: 871 90. Hess, S. C., Leopold, C. R., Misajon, K., Hu, D. & Jeffrey, J. J. (2012). Restoration of movement patterns of the Hawaiian Goose. Wilson J. Orn. 124: 478 86. Hockey, P. A. K. (2000). Patterns and correlates of bird migrations in sub-Saharan Africa. Emu 100: 401 17. Humphrey, P.S., Bridge, D. Reynolds, P.W. & Peterson, R.T. (1970). Preliminary Smithsonian manual: birds of Isla Grande (Tierra del Fuego). Smithsonian Institute Press, Washington, D.C., USA, and University of Kansas Museum of Natural History, Lawrence, Kansas, USA. Jahn, A. E., Levey, D. J. & Smith, K. G. (2004). Reflections across hemispheres: a system-wide approach to New World bird migration. Auk 121: 1005 13. Jahn, A. E., Cueto, V. R., Fontana, C. S., Guaraldo, A. C. Levey, D. J. et al. (2020). Bird migration within the Neotropics. Auk 137: 1 23. Johnson, D. N. & MacLean, G. L. (1994). Altitudinal migration in Natal. Ostrich 65: 86 94. Joseph, L. (1997). Towards a broader view of neotropical migrants: consequences of a re-examination of austral migration. Ornitol. Neotropical 8: 31 6. Keast, A. (1968). Seasonal movements in the Australian honeyeaters (Melaphagidae) and their ecological significance. Emu 67: 159 209. Keast, A. (1995). The Nearctic Neotropical bird migration system. Israel J. Zool. 41: 455 76. Levey, D. J. & Stiles, F. G. (1992). Evolutionary precursors of longdistance migration: resource availability and movement patterns in Neotropical landbirds. Am. Nat. 140: 447 76. Lincoln, F.C. (1935a). The migration of North American birds. U.S. Dept. Agric., Washington D.C. Circular No. 363: 1 72. Lincoln, F.C. (1935b). The waterfowl flyways of North America. U.S. Dept. Agric., Washington D.C. Circular No. 342: 1 12. Mills, A. M. (2006). Winter compression of migrants in Central America. J. Avian Biol. 37: 41 51.

Moreau, R. E. (1972). The Palaearctic-African bird migration system. London, Academic Press. Morse, A. H. (1989). American Warblers. Cambridge, MA, Harvard University Press. Morton, E. S. (1980). Adaptations to seasonal changes by migrant landbirds in the Panama Canal Zone. Pp. 437 53 in Migrant birds in the Neotropics (eds A. Keast, & E. S. Morton). Washington, DC, Smithsonian Institution Press. Munro, U. (2003). Life history and ecophysiological adaptations to migration in Australian birds. Pp. 141 54 in Avian migration (eds P. Berthold, E. Gwinner, & E. Sonnenschein). Berlin, SpringerVerlag. Newton, I. (1979). Population ecology of raptors. Berkhamsted, Poyser. Newton, I. (1995a). Relationship between breeding and wintering ranges in Palaearctic-African migrants. Ibis 137: 241 9. Newton, I. (1995b). The contribution of some recent research on birds to ecological understanding. J. Anim. Ecol. 64: 675 96. Newton, I. (1998a). Migration patterns in West Palaearctic Raptors. Pp. 603 12 in Holarctic birds of prey (eds R. D. Chancellor, B.-U. Meyburg, & J. J. Ferrero). Calamonte, ADENEXWWGBP. Newton, I. (1998b). Population limitation in birds. London, Academic Press. Newton, I. & Dale, L. (1996a). Relationship between migration and latitude among west European birds. J. Anim. Ecol. 65: 137 46. Newton, I. & Dale, L. C. (1996b). Bird migration at different latitudes in eastern North America. Auk 113: 626 35. Newton, I. & Dale, L. C. (1997). Effects of seasonal migration on the latitudinal distribution of west Palaearctic bird species. J. Biogeog. 24: 781 9. Nix, H. A. (1976). Environmental control of breeding, post-breeding dispersal and migration of birds in the Australian region. Proc. Int. Ornithol. Congr. 16: 272 305. Ponti, R., Arcones, A., Ferrer, X. & Vieites, D. R. (2020). Seasonal climatic niches diverge in migratory birds. Ibis 162: 318 30. Rappole, J. (1995). The ecology of migrant birds. A Neotropical perspective. Washington, DC, Smithsonian Institution Press. Rappole, J. H. (2013). The avian migrant. The biology of bird migration. New York, Columbia University Press. Ridgely, R. & Gwynne, J. A. (1989). A guide to the birds of Panama with Costa Rica, Nicaragua, and Honduras (2nd ed.). Princeton, NJ, Princeton University Press. Rosenzweig, M. L. (1992). Species diversity gradients: we know more and less than we thought. J. Mammal. 73: 715 30. Roshier, D. & Joseph, L. (2014). Weak migratory interchange by birds between Australia and Asia. Pp. 389 413 in Invasion Biology and ecological theory: insights from a continent in transformation (eds H. H. Prins, H., & I. Gordon). Cambridge, University Press. Somenzari, M. & Whitney, B. M. (2018). An overview of migratory birds in Brazil. Pape´is Avulsos De Zoologia 58, e20185803. Somveille, M., Manica, A., Butchart, S. H. M. & Rodrigues, A. S. L. (2013). Mapping global diversity patterns for migratory birds. PLOS ONE 8: e70907. Thiollay, J.-M. (1978). Les migrations des rapaces ens Afrique occidentale: adaptations ecologiques aux fluctuations saisonie`res de production des ecosystems. La Terre et la Vie 32: 89 133.

Chapter 17

Variations on a migratory theme

Shelduck (Tadorna tadorna) on moult migration Bird migration as a world phenomenon has existed as long as birds have flown . . . it is the specific circumstances that are so fascinating. R. E. Moreau (1972).

Most bird migration consists of an outward and return journey between fixed breeding and wintering areas. Other types of bird movements occur in a more limited number of species. They include (1) so-called ‘moult migration’ in which birds visit particular areas to replace their feathers; (2) long movements within the breeding season; (3) long movements within the non-breeding season, including irruptions and weather movements; and (4) nomadism in which birds move around in various directions and distances, seeking areas where conditions are suitable at the time. These variants can all be related to the particular ecological circumstances faced by the species concerned.

MOULT MIGRATIONS The term ‘moult migration’ was originally used for movement to a site used only for purposes of moult, often at higher latitudes than the breeding area, or at least in a direction different from that of the subsequent autumn migration (Salomonsen, 1968). More recently, the same term has also been used for altitudinal movements that some birds make to reach suitable moulting areas, and also for the first leg of an autumn migration which leads to a staging area where birds moult before continuing on their journey (Leu & Thompson, 2002), or indeed for any journey which is broken by a period of moult (Tonra & Reudink, 2018). This takes the term well beyond its original and most useful meaning, namely a distinct movement that could not be regarded as a pause on a regular migration route (Jenni & Winkler, 2020).

The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00013-0 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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Moult migration as originally defined Each year, some waterfowl travel long distances from their nesting places to assemble in large numbers in specific areas that offer abundant food and safety. The same areas are used for this purpose year after year. Here, birds pass the flightless period, replacing all their large wing feathers simultaneously within the space of a few weeks before moving on to wintering areas. Body moult begins before flight feather moult and continues afterwards. Among geese, moult migrations are undertaken entirely by non-breeders and failed breeders, and their moulting areas nearly always lie at higher latitudes than the nesting places, from a few tens to more than 1000 km away (Figure 17.1). For example Taiga Bean Geese (Anser f. fabalis) nesting in Finland fly more than 1500 km to reach moulting areas in Novaya Zemlya (Piironen et al., 2021). By leaving breeding areas, such birds avoid competing with families which stay there, and by moving to higher latitudes where plant growth begins later than in the breeding areas, the birds gain from more protein-rich food, as well as from longer days. But in consequence, their autumn migrations to wintering areas are then longer than those of successful breeders which have stayed with their young in lower latitude nesting areas and migrated to wintering areas directly from there. Similar moult migrations occur in many duck species but are more variable in direction than those of geese. Most Common Shelducks (Tadorna tadorna) from Europe gather each summer on the vast tidal mudflats of the Grosser Knechtsand in the German Wadden Sea, where they feed on the abundant mud-snail (Hydrobia ulva). The birds converge on this site from all directions, travelling up to several hundred kilometres from their breeding areas, with numbers peaking at more than 200,000 individuals. Yearlings and young adults arrive first, followed by failed breeders, then successful adults, which (unlike geese) leave their well-grown young behind (Patterson, 1982). Smaller concentrations assemble at various other sites within the breeding range. After moult, the birds drift back to their breeding areas over a period of weeks or months or move on to wintering areas. In various other ducks, the males, together with non-breeding or failed females, also perform moult migrations, leaving the successful females to hatch and tend their broods. Once their young are grown, some of the adult females perform a moult migration, being last to arrive in moulting areas, while others remain in their breeding areas and moult their flight feathers there. Freshwater ducks favour large lakes offering abundant food and cover, while sea ducks favour sheltered bays, similarly offering plentiful food. During their flightless stage, safety from predators is paramount. In some duck species, individuals have been found by ringing to travel distances of more than 3000 km from breeding to traditional moulting sites and some of the largest concentrations hold tens of thousands or hundreds of thousands of birds (Veen et al., 2005). In general, sea ducks perform longer journeys than freshwater ducks. Usually, birds fly quickly and directly from breeding to moulting sites, and even sea ducks, which normally stick to the coast, sometimes fly long distances overland to take the shorter routes (Salomonsen, 1968). A particularly big arrival of birds on moult migration was noted at Mud Lake, Idaho, where during one night (5 August) no less than 52,000 dabbling ducks of six species suddenly appeared (Oring, 1964). Some of the more impressive moult migrations of ducks are described in Box 17.1. Ducks take 3 5 weeks to regrow their flight feathers, depending on species, shelducks and geese take 4 6 weeks, and swans about 6 weeks. However, some individuals arrive in moulting areas weeks before starting their wing moult or leave long after finishing it, providing that food remains available. Typically, flocks arrive and leave over a several week period so that sites can be occupied by moulting birds for 2 4 months. For example Barrow’s Goldeneyes (Bucephala islandica) in eastern Canada travel north from their nesting areas around 1000 km to arctic waters, and spend 3 4 months there, longer than they spend in nesting areas, and much longer than the 31-day flightless period resulting from wing-moult (Robert et al., 2002). In those waterfowl whose moulting sites lie north of their breeding areas, the moult migration could be considered a northward extension to the spring migration. But many species take a different direction, sometimes at right angles to their normal migration axis. Moreover, because sites within the breeding range can attract birds from all directions, there is clearly no directional consistency between individuals. In addition, birds can periodically change their moulting sites in response to changes in water depths, or as established sites are destroyed or new ones are created by human action. Given these facts, it seems unlikely that birds from different parts of the breeding range inherit different directional preferences for moult migration, especially considering that individual waterfowl can sometimes breed in widely separated places in different years (Chapter 21). Rather they could learn the locations of favoured moulting sites from other individuals, with this knowledge passed on by tradition. However, not all birds in a particular region participate in a moult migration; some males may remain to moult in their breeding areas, along with the females and young. Nevertheless, many waterfowl show year-to-year constancy in their use of moulting sites, as for example Egyptian Goose (Alopochen aegyptiaca) (Ndlovu et al., 2013), Barrow’s Goldeneye (Savard & Robert, 2013), King Eider

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FIGURE 17.1 Moult migrations of geese. The arrows show the direction and distance from origin to destination. Greylag Goose (Anser anser) (3), Taiga Bean Goose (Anser fabalis) (5 9, 11), Pink-footed Goose (Anser brachyrhynchus) (1), Greater White-fronted Goose (Anser albifrons) (5 9, 11), Canada Goose (Branta canadensis) (2, 13 15) and Brent Goose (Branta bernicla) (4, 9, 10, 12). Modified from Salomonsen (1968).

(Somateria spectabilis) and Steller’s Eider (Polysticta stelleri), regardless of the breeding places used in each year (Knoche et al., 2007; Flint et al., 2000). The fact that different populations of a species may mix together on moulting areas leads to some individuals switching from one breeding population to another (Ko¨lzsch et al., 2019).

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BOX 17.1 Some moult migrations of ducks. King Eiders (Somateria spectabilis) from most of eastern arctic Canada travel to coastal areas in mid-western Greenland to moult. By that time, the participants have spent as little as 3 weeks in their breeding areas, and they travel eastward up to 2500 km, forming a concentration of more than 100,000 birds. After moult, the birds migrate to wintering areas off southwest Greenland where they are joined by the females and young (Salomonsen, 1968). Birds from the western part of the North American breeding range migrate westward to concentrate at various sites around the Bering Sea, staying in their moulting areas for 8 weeks or more before moving to wintering sites (L. Phillips et al., 2006). Long-tailed Ducks (Clangula hyemalis) in eastern Siberia perform an extensive migration across the Arctic Ocean to Wrangel Island, north of the breeding range, where they gather in tens of thousands. Another large concentration occurs near Thule in northwest Greenland, again attracting birds mainly from further south (Salomonsen, 1968). Common Goosanders (Mergus merganser) from much of northwest Europe migrate from their breeding areas to northernmost Norway, forming a scattered concentration of about 35,000 birds (mostly drakes) in various river-mouths, from which they later move southward to their wintering areas. Drakes are virtually absent from breeding areas from June to October (Little & Furness, 1985). Common Scoters (Melanitta nigra) from the northeast migrate each summer to the west coast of Jutland, Denmark, where they reach more than 150,000 individuals. After moulting, some birds remain there, while others move on elsewhere, but not necessarily as soon as moult has finished (Salomonsen, 1968). Common Pochards (Aythya ferina) assemble each summer on various waters in the mid-latitudes of Europe, including the IJsselmeer in the Netherlands (50,000 individuals) and Ismaninger Reservoir in Bavaria (20,000 individuals). Collectively, they far exceed the European population, and contain many birds from further east. Initially, males form nearly 100% of both populations, but as the season wears on, females gradually increase to nearly 50% by late September. Many Tufted Ducks (Aythya fuligula) and other species use the same sites, with similar seasonal changes in sex ratios (Van der Wal & Zomerdijk, 1979). Some 10,000 40,000 Great-crested Grebes have also been counted on the Dutch IJselmeer (Piersma, 1987). Most of these moulting sites were described decades ago, and the numbers of birds using them may have changed markedly since that time.

Other wetland birds also gather in large concentrations to moult, and some make long journeys to get there. This is true for European and American Coots (Fulica atra and Fulica americana) and for various grebes, all of which become flightless for a time. In western North America, most Black-necked (Eared) Grebes (Podiceps nigricollis) from prairie breeding areas migrate to moult on the Great Salt Lake in Utah or on Mono Lake in California, saline waters which together hold more than two million birds in late summer, feeding on the masses of brine shrimps. From there, after moulting, the birds move on to winter on the sea off California (Chapter 5; Storer & Jehl, 1985; Jehl, 1997). In Europe, up to 186,000 Black-necked Grebes have been counted on Burdur Go¨la¨ in Turkey (Hagemeijer & Blair, 1997), and smaller numbers elsewhere. What could be construed as moult migrations have also been reported from divers, flamingos, and some cranes (Jehl, 1990). Because of moult migration, then, many waterbirds occupy at least three main areas each year for breeding, moulting and wintering; and some also make long movements within their wintering range (see later). Some seabirds perform similar migrations, as they moult in specific areas, often at higher latitude than their breeding places, and then migrate to a different area for wintering. An example is the Ancient Murrrelet (Synthliboramphus antiquus) from western Canada, which migrates north through the Bering Strait to the Chutki Sea for moult and then moves back to lower latitudes for winter (Gaston et al., 2017). In the Little Auk (Alle alle), non-breeders leave Greenland colonies in late July or August, in advance of breeding adults, and move northward to moult in rich feeding areas along the edge of the pack ice, although for these birds the actual moulting localities may vary from year to year, according to ice conditions (Jehl, 1990). In all these various waterbirds, then, moult migration differs from typical migration in several respects. First, the flight direction is often different from autumn or spring migration and may vary by up to 360 degrees among birds converging on a single site from different parts of the breeding range. Second, only certain sectors of the population participate; goose pairs with young stay behind, as do some female dabbling and diving ducks with broods. Third, the localized and unusually high population densities found at moulting areas are unique in some species, whereas in breeding and wintering areas the birds scatter over much wider areas. Fourth, all these waterbirds become flightless during moult, as they replace all their flight feathers simultaneously. This does not happen in any of the species in the two other categories below. As in most other migrations, however, individuals follow a rigid schedule, with the timing of moult migration varying only slightly from year to year, according to the timing and success of breeding. Some species travel such long distances that they must presumably accumulate body reserves to fuel the journey, although I know of no published information.

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Altitudinal moult migrations Some montane passerines in western North America have been found to move upslope to moult after breeding (Wiegardt et al., 2017). Although of short distance, such altitudinal moves in a hot region provide a cooler and moister environment, plus the same advantages as movements to higher latitudes, namely vegetation at an earlier stage of development, and hence more nutritious and richer in insects. Participants include the Orange-crowned Warbler (Oreothlypis celata), Townsend’s Warbler (Setophaga townsendi), Hermit Warbler (Setophaga occidentalis), Cassin’s Vireo (Vireo cassinii) and Wilson’s Warbler (Wilsonia pusilla), among others (Tonra & Reudink, 2018, Hedley 2019). After moult is completed, the birds proceed southward to their wintering areas. Other species that move higher to moult include the Rock Ptarmigan (Lagopus muta) and Ring Ouzel (Turdus torquatus) on European mountains (Jenni & Winkler, 2020).

Moult at staging sites on autumn migration Moulting at staging sites on autumn migration is known mainly from passerines and shorebirds and occurs commonly in both the Old and New World species (Chapter 12). Several Eurasian African migrant passerines moult partially or completely on their first major staging site in Africa, south of the Sahara. Following moult, they migrate further south within Africa. Examples include the Eurasian Reed Warbler (Acrocephalus scirpaceous), Great Reed Warbler (Acrocephalus arundinaceous) and others mentioned in Chapter 12. This pattern has probably arisen because it allows birds to extend their breeding season and then postpone moult until after they have reached the northern tropics towards the end of the wet season, when the land is still green and food plentiful (Chapter 26). Similarly, about half of the migrant passerine species breeding in western North America leave their nesting areas after breeding and migrate to the southwestern United States and northwest Mexico (the Mexican Monsoon area). Here they perform a partial or complete moult, then resume migration to their wintering grounds further south (Rohwer et al., 2005; Pyle et al., 2009, 2018). This pattern has probably arisen because much of lowland western North America dries out in late summer, while the summer monsoon in the southwest provides fresh vegetation and insects. In contrast, in eastern North America, which is less affected by summer drought, the same or similar species moult in their breeding areas or close by. Western species undertaking these movements include Bullock’s Oriole (Icterus bullockii), Lazuli Bunting (Passerina amoena) and Western Tanager (Piranga ludoviciana) from breeding areas to the north, and the Painted Bunting (Passerina ciris) from breeding areas to the east. The proportion of the population undertaking these migrations varies between species, age groups and years, depending on conditions in breeding areas, and individuals show little or no fidelity to specific localities (Young, 1991; Pyle et al., 2009). In most of the species concerned, only the adults migrate before moulting, while the juveniles (replacing only their body feathers) remain to moult near their natal areas before migrating. In some species, however, both adults and juveniles postpone moult until they have reached their staging areas. While North American ornithologists speak of a moult in a staging area (presumably because it occurs in North America), European ornithologists refer to a moult in the first of succession wintering areas (when it occurs in Africa). However, in both cases, the moult occupies the same position in the annual cycle, and only birds from parts of the breeding range are involved, while birds from other parts moult in their breeding areas. In northeast Europe, some Common Starlings (Sturnus vulgaris) migrate immediately after breeding before their moult begins or in its early stages. Ring recoveries suggest a first movement of 300 1200 km, followed by a second movement in autumn after moult has finished. The two phases of migration are indistinguishable in direction and altitude of flight, and both include some nocturnal flights (Kosarev, 1999). Juveniles participate mainly in the first period, moulting in their migration areas, and adults mainly in the second period, after moulting in their breeding areas (opposite to the North American species above). The post-breeding migration of the whole Starling population therefore occurs as two well-separated waves (Figure 17.2). The many shorebird species in which adults moult at staging areas on autumn migration include the Green Sandpiper (Tringa ochropus) and Bar-tailed Godwit (Limosa lapponica) in Britain (Wernham et al., 2002). Similarly, after breeding, several hundred thousand adult Wilson’s Phalaropes (Phalaropus tricolor) gather at saline lakes in western North America, where they replace only the first 3 4 primaries along with the tail and nearly all the body plumage. Females arrive by mid-June and males a fortnight later (Jehl, 1996). Individuals remain for up to 6 weeks, doubling their weight before departing on an apparent non-stop flight of 4800 km to South America. Although most shorebirds do not become flightless during moult (except for the Bristle-thighed Curlew (Numenius tahitiensis) on Hawaii), the same factors as in waterfowl are likely to influence their choice of site: low predation risk in an area with abundant food available over a long enough period.

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FIGURE 17.2 Autumn migration of Common Starlings (Sturnus vulgaris) through Ottenby in south Sweden. The first peak consists mainly of juveniles before moult and the second peak mainly of adults after moult. Modified from Sva¨rdson (1953).

Mean number of birds per day

2000

1500

1000

500

0 3

13 23 June

3

13 23 July

2

12 22 August

1 11 21 September

1

11 21 31 October

These various moult migrations can thus be viewed in some species as an extra post-breeding movement in the annual cycle of the species concerned, and in other species as a part of the autumn migration, involving a several-week stop in a favourable area on route to winter quarters.

MOVEMENTS WITHIN THE BREEDING SEASON In some multi-brooded bird species, individuals may nest in more than one locality each year. Typically, they raise one brood in one place, then migrate up to several hundred kilometres, and raise another brood elsewhere. So-called itinerant breeding was first suspected in the Common Quail (Coturnix coturnix) in which females arriving in Italy in June July, apparently to breed, often showed regressing brood patches from an earlier breeding attempt, and were frequently accompanied by young no more than 2 months old. These young must have hatched from clutches begun in March, when breeding would have been possible only in North Africa. Reports of a general exodus of Quail from Tunisia in spring after breeding support this view, and single birds ringed there in May and early June were recovered in Italy and Albania respectively, 2 3 months later (Moreau, 1951; Cramp & Simmons, 1980). Late clutches in northern Europe during August September could result partly from an influx in mid-summer of birds that have previously bred in the Mediterranean region. Apparently, the males leave southern Europe once the females have laid and move on to establish new territories further north, where females join them later. Many females do not reach the most northern areas where males predominate (Aebischer & Potts, 1994). Common Quail can mature and breed at 3 months old so that young produced in the southern parts of the breeding range could breed in the same summer in the more northern parts, along with the adults on their second or third attempt. About half of the large numbers of Quail that bred in France in 1987 were judged to have hatched earlier in the same year (He´mon et al., 1988). Itinerant breeding is also shown by the Red-billed Quelea (Quelea quelea) which feeds on grass seeds on the African savannahs. Throughout the dry season, these birds subsist on seeds picked off the ground, but when the rains break, this seed suddenly germinates, removing the food supply and causing the birds to move on. From germination, it takes about 2 months for fresh grass seed to become available again. Along with insects associated with the growing vegetation, this fresh grass seed provides a food supply on which Queleas can breed. After raising their young, the birds move en masse, stopping again in another area where rain fell about 2 months previously and new grass seed has formed, enabling the birds to breed again (Ward, 1971; Jaeger et al., 1986). In theory, the birds could follow the rains in successive breeding attempts, each time moving hundreds of kilometres, and stopping when the dry season halts further grass growth. In most parts of their range, they could make at least 2 3 nesting attempts in a year, perhaps more in certain regions. Within this framework, the pattern is variable from year to year, depending on regional variations in rainfall and grass seed production. However, conditions suitable for rearing young do not last long in any one place and, despite a breeding cycle of only 5 weeks, Queleas cannot raise two broods in the same place. The adults abandon their young at about 3 weeks old, with enough body fat for their survival, and continue on their breeding migration. They stop when the dry season prevents further grass growth for a time, relying on fallen seeds from the ground. Some other birds in semi-arid regions of the world which breed at a particular stage in the dry wet seasonal cycle may also raise successive broods in places far apart. Multiple breeding along a migration route, following a rain belt, has been suspected in the Eared Dove (Zenaida auriculata) in northeastern Brazil (Bucher, 1982), and substantial shifts

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in colony sites during a single season have been suspected in the White-crowned Pigeon (Patagioenas leucocephala) on Hispaniola (Arendt et al., 1979), in the Tricolored Blackbird (Agelaius tricolor) in California (Hamilton, 1998), and in the Spanish Sparrow (Passer hispaniolensis) in Kazakhstan and elsewhere (Summers-Smith, 1988; Cramp & Perrins, 1994). Itinerant breeding has also been recorded in various species in Australia, such as the Zebra Finch (Taeniopygia guttata) (Zann & Runciman, 1994). Other European birds which can raise successive broods in localities far apart in the same year include some cardueline finches, such as Common Redpoll (Acanthis flammea) and Eurasian Siskin (Spinus spinus) which depend on different types of tree seeds (Chapter 20). Other carduelines have been found to move shorter distances (up to a few tens of kilometres) during a breeding season (Newton, 2000). Also over shorter distances, some Sand Martins (Riparia riparia) changed colonies between successive broods in the same season (Mead, 1979). In North America, on the basis of circumstantial evidence, the Phainopepla (Phainopepla nitens), Sedge Wren (Cistothorus platensis) and Dickcissel (Spiza americana) probably also raise successive broods in the same year in different regions (Walsberg, 1978; Bedell, 1996; Basili et al., 1997). The same holds in some waders such as the Eurasian Dotterel (Charadrius morinellus) in which some ringed males were found to nest first in Scotland and then, after nest failure, to have another attempt in Norway (Wernham et al., 2002). In North America, in the Snowy Plover (Charadrius nivosus), one partner (usually the female) deserts the first brood soon after hatching to re-nest with a new mate, sometimes tens or hundreds of kilometres away, leaving the first brood to be raised by the jilted partner (Stenzel et al., 1994). Unexpectedly, 3 out of 10 Water Rails (Rallus aquaticus) tracked with geolocators from Norway were found to move 129 721 between successive nesting attempts in the same season (Lislevand et al., 2020). Several species which breed first in temperate North America have been found to migrate several hundreds or thousands of kilometres to breed a second time in northwest Mexico (Rohwer et al., 2009). In this region, monsoon rains fall during July September, causing deciduous trees to burst into leaf and flower, encouraging an abundance of insect prey, as well as seeds from grasses and other plants. After breeding in temperate North America, at least five migrants, namely Yellowbilled Cuckoo (Chrysococcyx megarhynchus), Cassin’s Vireo, Yellow-breasted Chat (Icteria virens), Hooded Oriole (Icterus cucullatus) and Orchard Oriole (Icterus spurius), move into this region and breed a second time. Females of these species that were starting to breed often had featherless brood patches, signs that they had nested earlier in the same season. Yet no recently fledged juveniles of these species were present in July, suggesting that the adults had not bred in northwest Mexico earlier in the same summer. Many adults of these five species sampled were clearly breeding when collected in this region, as males had fully enlarged testes and females were laying. In addition, males of all five species were found singing on territories or guarding females, and in two species nests were found. Other species from further north, mentioned earlier, also moved into this area to moult, and later in the year all these species left for wintering areas further south. Itinerant breeding enables species that could raise only one brood per year in a given locality to become multibrooded. Prerequisites are a short breeding cycle with early independence of young. Species with long breeding cycles, involving prolonged parental care, would not be expected to become itinerant breeders in seasonal environments, because they could not raise more than one brood in the time available. The itinerant breeders mentioned above seem to fall into two categories: one involving local movements of up to a few tens of kilometres, and the other longer movements of up to several hundred kilometres between different points on an established migration route. Both types could occur in a wider range of species than recorded, but itinerant breeders are clearly rare or non-existent in the vast majority of well-studied European and North American migratory birds. It might be thought that many species migrating north through Eurasia or North America in spring could raise more broods by stopping at different latitudes on route than by breeding only for a short season in the north, where only one brood can be fitted into the time available. The prior occupation of more southern habitat by other competitive conspecifics may be the main factor preventing this. Moreover, the southern habitat usually remains suitable for further nesting after the first broods fledge, which encourages birds to stay (Chapter 12). This is not true for known itinerant multibrooded species, such as Red-billed Queleas, which settle in areas that have only just become suitable, and hence where there is no established prior population, and which have to move on if they are to breed again in the same season because local conditions soon deteriorate. A remarkable feature of some of these examples is that individuals move so far between successive breeding attempts that the movement can be fairly described as a migration, inserted within a breeding season. Prior fat deposition has been recorded at least in Queleas, the amount varying between three populations, according to the distances they travel (Ward & Jones, 1977).

MOVEMENTS WITHIN THE NON-BREEDING SEASON Whereas many birds migrate only between a single fixed breeding area and a single fixed wintering area, individuals of other species make substantial movements during the course of a non-breeding season, often extending further from their

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breeding areas as the season progresses. In some species, such movements are regular, somewhat analogous to different stages of a single migration, but the birds stay in the same place for up to several weeks between each move (Chapters 14, 26). The separate moves occur at about the same dates each year, and each move may be preceded by fat deposition. Many species that breed in Eurasia and winter in Africa perform such stepwise migrations, pausing for a time in the Sahel zone (where some of them moult, as described above), and then move further south within the northern tropics or beyond the equator to the southern tropics (Jones, 1995; Chapter 26). Movements within the non-breeding season are less wellknown among North American migrants wintering in South America, but the tracking of individuals on migration is providing ever more examples (McKinnon et al., 2013; Chapter 27). In many species, departures from particular areas are often linked with decline in food-supplies, as measured by some surrogate variable, such as NDVI (Chapters 26 and 27). Mainly through tracking studies, individuals of 91 different species in 34 families were found to visit more than one locality during the same winter, mostly some 50 500 km apart (Teitelbaum et al., 2023). Most of these birds had two different wintering areas, but some had more, and the same individuals often behaved differently from year to year, depending on conditions (Berthold et al., 2002). Some species made many more moves, as exemplified by Snow Buntings (Plectrophenax nivalis) in Ontario which moved every few days during December February, over distances of 3 490 km (McKinnon et al., 2019). Other species move between three areas each year that are not on the same direct route. As found by satellite tracking, Prairie Falcons (Falco mexicanus) leave their breeding areas in southwest Idaho between late June and mid-July (Steenhof et al., 2005). They migrate northeast across the continental divide to spend the rest of the summer in Montana, Alberta, Saskatchewan and the Dakotas. They stay there for 1 4 months, and then in October move southwards around 1000 km to the southern Great Plains, mainly in Texas. After 5 months there, they return directly to their breeding areas (Figure 17.3). This three-step cycle of movements enables these falcons to gain access to abundant prey year-round, and individuals used the same three areas in successive years. Their absence from breeding areas at the hottest time of year coincides with the period when their main prey (ground squirrels) is underground and unavailable. But in the cooler areas occupied in late summer, ground squirrels remain active into autumn. In their wintering areas, Prairie Falcons feed largely on migratory birds which overwinter there, especially Horned Larks (Eremophila alpestris). Ferruginous Hawks (Buteo regalis), which also eat ground squirrels, perform similar movements between breeding, post-breeding and wintering areas, with birds from different regions heading in different directions to their particular post-breeding areas (Schueck et al., 1998; Watson & Keren, 2020). Individuals showed strong fidelity to their breeding and wintering localities, but often changed autumn localities from year to year, or changed localities within an autumn, responding perhaps to prevailing prey. Several species of hummingbirds also move through three or more different regions each year. For example Anna’s Hummingbird (Calypte anna) breeds in spring in the coastal shrubland of southern California, summers in the high mountains of California, and winters in the deserts of Arizona and Mexico, thereby ensuring that its need for nectar is met year-round (Stiles, 1973). Some birds seem to be on the move continually between leaving their breeding range one year and returning the next and do not stop for any prolonged period in winter. For example several Gyrfalcons (Falco rusticolus) tagged in FIGURE 17.3 Three-part migration of Prairie Falcons (Falco mexicanus), as revealed by the satellite tracking of radiotagged birds nesting in southern Idaho. B, breeding area; PB, post-breeding area; W, wintering area. After breeding, the birds move northeast to spend the summer in cooler areas at higher latitude or elevation where ground squirrels remain available, and then after 1 4 months, they move southward to winter mainly in northern Texas, returning in spring directly to their breeding areas. Based on Steenhof et al. (2005).

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northwest Greenland had no obvious winter destination and travelled continually during this non-breeding period, at times spending up to 40 consecutive days at sea, presumably resting on icebergs and feeding on seabirds (Burnham & Newton, 2011). During the winter, one juvenile female travelled over 4548 km over an approximately 200-day period, spending over half that time over the ocean between Greenland and Iceland. Some pelagic seabirds provide further examples of almost continual movement through the non-breeding period (Chapter 8).

Facultative movements in relation to food supply In many species, movements in the non-breeding season are optional (facultative). They can take place at almost any time if feeding becomes difficult. In some northern species, the proportions of birds that leave the breeding range, and the distances they travel, vary greatly from year to year (Chapter 20). Most individuals stay in the north in years when food is plentiful there, wintering within, or just south of, their breeding areas, but moving further south in years when food is scarce. Such annual variations are most pronounced in finches and other birds that depend on fluctuating treeseed crops (eg Common Redpolls and Eurasian Siskins), and in raptors and owls that depend on fluctuating (cyclic) rodent species (eg Rough-legged Buzzards (Buteo lagopus) and Snowy Owls (Bubo scandiaca)) (Chapters 20, 21, Figure 17.4). Their so-called ‘invasions’ or ‘irruptions’, in which every few years they appear in large numbers well outside their usual range, follow periodic widespread crop failures (finches) or crashes in rodent-prey populations (raptors). Irruptions therefore occur in response to annual, as well as seasonal, reductions in food supplies. Irruptive migrants provide extreme examples, but year-to-year distributional changes dependent on flexible migration patterns occur in a wide range of birds. Many bird species seem able to migrate (by ‘escape movements’) at any date in the non-breeding season if stimulated to do so by reduced food supplies, and usually they move further along the regular migration route. For example in the Yellow-rumped Warbler (Phylloscopus chloronotus), autumn densities at a number of sites in Arizona and northern Mexico were correlated with local food supplies (Terrill & Ohmart, 1984). Subsequent declines in the abundance of both insects and warblers at particular sites occurred during cold spells. Declines at Arizona sites corresponded with increases at more southerly Mexican sites, suggesting movements, with the magnitude of changes correlated with insect availability. Similar findings have emerged for many other species that migrate within the temperate zone (eg Pulliam & Parker, 1979; Niles et al., 1969), as well as in many that reach the tropics (Chapter 26). Experiments have shown that captive birds can develop migratory restlessness in response to food deprivation in winter, well beyond the normal migration period (Gwinner et al., 1985; Chapter 13). In all such species, further movement in the usual direction of migration may give the birds the best chance of finding food.

(a) Snowy Owl

(b) Common Redpoll

FIGURE 17.4 North American winter ranges of (a) Snowy Owl (Bubo scandiaca) and (b) Common Redpoll (Acanthis flammea) that winter mainly at high latitudes (shaded area), but in years of greatest food shortage extend far to the south (dotted line).

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Facultative movements in relation to weather Facultative movements are also shown by species that obtain their food from water or the ground, and which move out in response to freezing temperatures, snow or drought. Such escape (or weather) movements occur as soon as waters freeze or snow covers the ground, cutting off food supplies. The dates of such movements therefore vary between years, depending on the weather, and in mild winters need not occur at all. Even in the arctic, some waterfowl and gulls remain in autumn to feed in remaining patches of open water until long after most other migrants have left. They are forced out as the last open waters freeze in winter. Hard weather movements are often extremely obvious. Whenever cold weather strikes, thousands of birds can be counted as they stream past particular observation points and as large regions are evacuated within a matter of hours. Counts made at such times in Britain include the 20,000 Eurasian Skylarks (Alauda arvensis) that passed westward over the Axe Estuary in Devon on December 28 1964, or the 8300 counted in 2 hours as they passed south over a site in northeast Scotland on January 24 1976; the 4500 Northern Lapwings (Vanellus vanellus) that passed southwest over Tring in 50 minutes on December 9 1967, and the 10,200 that passed in 2.5 hours over Portsmouth, Hampshire on January 30 1972 (Wernham et al., 2002). Over much of the world, ducks usually travel at night, so are seldom seen on migration, but their weather movements are marked by sudden massive overnight increases in the numbers on particular wetlands, following the onset of hard weather back along the migration route. Many hard weather movers usually return soon after conditions improve again, sometimes less than a week later and over distances up to several hundred kilometres. They thereby avoid competition for food, which is likely to be more intense in the overcrowded hard weather refuges than in the areas previously left. During the winter, some birds can shuttle back and forth along part of their migration route, on average getting further from their breeding areas as winter advances. It seems that some facultative migrants have some sense of where they ought to be that is as near to the breeding areas as conditions allow and can migrate effectively in either direction during the course of a winter. Weather movements were found by radar to occur almost every day and night in November February between Britain and continental Europe (Lack, 1963). The Northern Lapwing and Common Starling were the most frequent participants, but many other species were involved too, including finches, thrushes, larks, plovers, grebes and other waterfowl (Elkins, 1988; Evans & Davidson, 1990; Ridgill & Fox, 1990). Lapwings fleeing from hard winters may reach Spain, where they are known as avefria (birds of the cold). In the rare years when the cold weather extends to the usual hard-weather refuge areas (eg southwest Ireland), enormous mortality may occur among the huge numbers of migrants concentrated there (Clarke, 1912). Needless to say, hard weather movements are much more pronounced in severe winters than in mild ones, and in some regions, they have become less frequent in recent decades as winters have mellowed, and birds have become less abundant for other reasons. Some wetland species perform the equivalent of hard weather movements in summer, often to higher latitudes, in their attempts to escape drought. Such movements have most often been recorded among various herons and ducks (in which they merge with moult migrations). In addition, at least one non-wetland species in Europe performs extensive weather movements in summer. The Common Swift (Apus apus) feeds on small high-flying insects abundant only in fine weather. As found by radar studies, these birds escape cold rainstorms by flying clockwise round the depression and returning behind it (Lack, 1956). In the process, they can travel up to 2000km. It is mainly the non-breeders that participate in these movements, but also some breeders, forming flocks of up to 50,000 birds. Other examples of weather movements are found in mountains after birds have settled on their high altitude nesting areas but are subsequently driven down by late spring snowfalls, as described for example in White-crowned Sparrows (Zonotrichia leucophrys oriantha) nesting on the high Sierras of Califormia (Hahn et al., 2004).

Overview The important point to emerge from these sections is that migration is not always a simple two-season movement between fixed breeding and wintering areas. Some species move between three distinct areas: a breeding area, a late summer or autumn area, and a wintering area. Others move only when necessary, and no further than necessary, wintering much nearer to their breeding areas in some years than in others, thereby saving on the costs of migration. Yet others seem to spend much of their lives on the move, following the same route each year, pausing for a few weeks here and a few weeks there. Their mobile lifestyle enables them to exploit food supplies at different places at different times. It is a lifestyle that birds more than most other animals can adapt to the full. These various examples of movements within the breeding or non-breeding seasons provide further circumstantial evidence for the underlying role of weather and food supplies in governing the movement patterns of birds (although in some cases also modified by other influences such as disturbance and predation, Chapters 14, 30).

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OPPOSITE-DIRECTION MIGRATIONS While in the northern hemisphere, most landbirds migrate southward in autumn and northward in spring, breeding at higher latitudes than their wintering areas, some species show the opposite pattern, breeding in winter or early spring and migrating north to their non-breeding areas. For example among Bald Eagles (Haliaeetus leucocephalus) that nest in southern North America, the young are raised in winter or early spring. They then move northwards for up to 2200 km, spending from May to September in Canada and Alaska, where they feed largely on salmon which fill the rivers at that time (Broley, 1947). The young eagles therefore travel north in spring and south in autumn with the conventional migrants but, unlike them, they have been reared in the south before doing so. Many adult and sub-adult eagles also leave the south in spring, but it is not clear whether they travel as far as the juveniles. This migration was first established from the ringing of nestlings in Florida (Broley, 1947), but more recently it has been confirmed in radiotracked young from Florida (Mojica et al., 2008), California (Hunt et al., 1992) and Arizona (Hunt et al., 2009), and in colour-marked young from Texas (Mabie et al., 1994). This last study also confirmed that some young eagles returned to their natal areas to breed. A second example is shown by Red-tailed Hawks (Buteo jamaicensis) ringed as chicks in southern California (Bloom et al., 2015). Most of these birds were recovered to the north, at distances up to 1462 km from their natal nests. Sixteen hawks from the same area, equipped with satellite transmitters as fledglings, migrated up to 1388 km northward, mainly in May August, and returned mainly in September of the same year. This pattern was repeated annually until the birds acquired a territory and mate, at which point they became resident in southern California. Migration by pre-breeding birds was probably a response to a shortage of a major prey (ground squirrels) during the driest time of year. Ring recoveries suggested a similar pattern across the continent: juveniles and young adults ringed south of 35 N migrated northward, whereas those ringed north of 40 N migrated southward. A third example relates to Long-legged Buzzards (Buteo rufinus) breeding during December-July in Israel (Friedemann et al., 2020). Adults were tracked on their post-breeding migration northwards for more than 1000 km to spend their non-breeding period in Syria, Turkey and Russia, returning southward mainly in September October. Most of these Long-legged Buzzards travelled north and then south at the same time as most other migrants. Again, the movement could be related to a seasonal food shortage in breeding areas. From satellite images, the migration and wintering areas showed consistently more favourable greenness indices (NDVI values) than found in their breeding areas at that time, providing ideal foraging conditions with low vegetation for Long-legged Buzzards. The young of several species of herons, raised in winter in the southern United States, disperse in various directions but mainly northward, again presumably to exploit the presence of fish in shallow water in the northern spring and avoid the effects of drought in more southern areas (Lincoln, 1935). Similar but less marked summer movements have been recorded among herons in Europe, and in the southern hemisphere some heron species in Australia also migrate to higher latitudes after breeding (Maddock, 2000). In addition, the non-breeders of some seabird species, including the Little Auk and several skua species, spread up to several hundred kilometres northward beyond their natal colonies in summer, exploiting the summer flush of food at higher latitudes, and some winter-breeding petrels and shearwaters also move to higher latitudes in their non-breeding period. Northward dispersal to feeding areas before southward migration has also been recorded in Northern Gannets (Sula bassana) nesting in Britain, and may well occur in other species too (Kubetzki et al., 2009).

NOMADISM Even greater flexibility in movement patterns is shown by species that exploit sporadic habitats or food sources. Such species often appear to be truly nomadic, as they show little or no year-to-year consistency in their movement patterns, either in timing, direction or distance. They continually shift from one area to another, residing for a time in whichever part of their range food is plentiful at the time. Their movements might be regarded as a series of sequential dispersals. Of course, many bird species wander locally over distances of a few kilometres in search of food, but so-called nomadic species can travel hundreds of kilometres from one breeding area to another or from one non-breeding area to another. It is partly a matter of scale. However, much of what we know about nomadic movements is based on inference, so far supported only to a small extent by ringing or tracking studies. This is a consequence of the mobility of the birds themselves, and the fact that most of them live in areas largely devoid of people. In general, nomadism is associated with ecosystems in which the underlying productivity and the densities of resident bird species are very low, but in which periodic pulses of high productivity occur, with resources sufficiently abundant to support major influxes of birds from elsewhere. Most nomadic species are specialists, feeding on only a small

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range of food items, which appear occasionally in extreme abundance. Many are seed-eaters, which in deserts mostly specialize on the masses of grass seeds produced after rain has fallen. Others are nectar-feeders which exploit the blossoming of trees which follows rain, or insectivores which tend to specialize on ‘plague’ insects, such as noctuid moth larvae, grasshoppers or locusts. Yet others are predators which feed on the other birds that move in or on the rodents that increase in response to vegetation growth and seeding, while flamingoes move in to exploit the temporary abundance of algae and small invertebrates that develop in alkaline lakes. Nomadism is best developed in desert regions, in places governed by sporadic rainfall, which influences plant growth and invertebrate densities, as well as the availability of surface water for waterfowl. Nomadism seems to occur in response to the variability, rather than the severity, of the desert environment, and in the most unpredictable conditions, both the movements and breeding of birds become increasingly aseasonal. Following rain, landbird densities in particular localities can increase more than a hundred-fold within a few days, and waterbirds that have been absent for years can re-appear in huge numbers on new floodwaters (Dean, 2004). In such environments, the survival of many bird species depends primarily on their mobility. In deserts as elsewhere, nomadic movements are often superimposed on regular north south migrations so that populations are concentrated at different latitudes at different times of year, but always patchily distributed, wherever food occurs. This is obvious in northern regions, as mentioned above, in some seed-eaters which depend on variable tree-seed crops and in some predators which depend on cyclically fluctuating rodents (Chapters 20, 21). It is also obvious in some Australian species, such as the seed-dependent Budgerigar (Melopsittacus undulatus) and Cockatiel (Nymphicus hollandicus), or the blossom-dependent Black Honeyeater (Sugomel nigrum) and Swift Parrot (Lathamus discolor) (Pizzey & Knight, 2007; Stojanovic et al., 2015). On the other hand, no regular latitudinal shifts are apparent in other Australian nomadics, such as the seed-eating Flock Bronzewing (Phas histrionica) and Princess Parrot (Polytelis alexandrae) or the rodent-eating Letter-winged Kite (Elanus scriptus). The latter tends to concentrate at local outbreaks of Long-haired Rats (Rattus villossissimus) which follow the vegetation growth resulting from rain. Overall, at least 93 (13%) of 742 landbirds in Australia move about the interior, either on a combination of regular migration and nomadism or on nomadism alone (Cottee-Jones et al., 2016). In South America, nomadism and aseasonal breeding have been reported in the Temminck’s Seedeater (Sporophila falcirostris) and Buffy-fronted Seedeater (Sporophila frontalis) in relation to the sporadic masting of bamboo (Guadua and Chusquea) species (Areta et al., 2013). Yet other bird species behave to some extent nomadically only in the non-breeding season and return to the same nesting localities each year. Examples from among Eurasian African migrants include the White Stork (Ciconia ciconia), Black Kite (Milvus migrans), Lesser Spotted Eagle (Clanga pomarina), Lesser Kestrel (Falco naumanni), Redfooted Falcon (Falco vespertinus), Amur Falcon (Falco amurensis) and Black-winged Pratincole (Glareola nordimanni). Typically, these species specialize in their non-breeding areas on sporadic food sources, such as locusts and grasshoppers, emerging termites, large nesting colonies of Red-billed Quelea or Wattled Starlings (Creatophora cinerea), or small animals disturbed by grass fires. Some of these prey species are available at the same localities for a short time every year, but others only after rainfall. The importance of food supplies is further shown by the fact that some typical nomadic species become regular breeders in parts of their range where food is more consistently available. Examples include the White-fronted Chat (Epthianura albifrons) in southern Australia (Dean, 2004) and the Red Crossbill (Loxia curvirostra) in Europe (Chapter 20). According to Dean (2004), some 233 arid-land bird species worldwide could be classed as primarily nomadic. They form varying proportions of desert avifaunas in different regions (Figure 17.5). In deserts in the northern hemisphere, regular seasonal migrants tend to outnumber year-round nomadic species, especially in the colder regions (Dean, 2004); but in the warm deserts of the southern hemisphere, nomadic species tend to outnumber regular migrants. This difference between hemispheres is attributed mainly to the greater fluctuation and unpredictability of rainfall in warm southern regions (associated with El Nin˜o La Nin˜a events). In Australia, where conditions are most variable, up to 46% of desert bird species can be classed as nomadic, a greater proportion than in deserts in any other region (Dean, 2004). Nomadic birds of the African and Asian deserts are typified by sandgrouse (Pteroclidae), larks (Alaudidae) and sparrows, weavers and finches (Passeridae). Those of Australian deserts are typified by honeyeaters (Melophagidae), parrots (Psittacidae) and crows (Corvidae), and those of New World deserts by finches (Fringillidae). Overall, nomadism is found in about half the bird families that breed in arid and semi-arid environments. It seems more related to diet than to phylogeny but occurs disproportionately in some families, such as sandgrouse, all of which are nomadic to a greater or lesser extent, as are many larks. Poor conditions over most of the range, coupled with good conditions in other parts, can sometimes produce enormous concentrations of birds. For example in the austral summer of early 2004, an estimated 2.9 million Oriental

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Percentage bird species 0 Cold Northern Desert Turkey (115) Transcaspia (56) Turkestan Desert (148) Kazakhstan (69) Afghanistan (120) Mongolia (107) Gobi Desert (85) Takla Makan Desert (80) Great Basin Desert (101) Cold Southern Desert Patagonia (88) Puna (197) Warm Northern Desert Thar Desert (141) Iranian Desert (116) Arabian Desert (184) Morocco (92) Libya (70) Sahara Desert (124) Chad (219) Eritrea (302) Ethiopia (351) Mali (210) Mauritania (178) Niger (192) Somalian Desert (270) Sudan (324) Sahel (550) Sonoran Desert (187) Chihuahuan Desert (162) Mojave Desert (62) Mexico (159) Warm Southern Desert Namib Desert (48) Karoo (158) Kalahari Desert (140) Madagascar (39) Central Australia (79) South Australia (206) Western Australia (207) Monte Desert (235) Chaco, Argentina (145) Atacama Desert (127) Peruvian Desert (222) Ecuador (Santa Elena) (150)

5

10 15 20 25 30 35 40 45 50

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FIGURE 17.5 Proportions of breeding species in different arid regions that have been classed as nomadic. Total numbers of breeding species in parentheses. Nomadic species reach significantly greater numbers (and proportions) in the warm deserts of the southern hemisphere than in similar deserts in the northern hemisphere χ2 with Yates’ correction 5 12.17, P 5 .005, and also significantly greater numbers (and proportions) in all southern hemisphere arid regions regardless of winter temperatures χ2 with Yates’ correction 5 17.76, P , .001. The deserts of Australia hold the highest proportion of nomadic species (compared with all other southern hemisphere deserts, χ2 with Yates’ correction 5 89.09, P , .001). From Table 2.3 in Dean (2004).

Pratincoles (Glareola maldivarium) gathered along 235 km of coastal grassland in northwest Australia, feeding on the abundant grasshoppers (Sitters et al., 2004). These birds breed widely over Southeast Asia and migrate mainly to Australia for their non-breeding season. In most years, the birds are thinly spread over a wide area. This makes them hard to find, and the total flyway population had been previously estimated at only 75,000 individuals. But the circumstances of early 2004 led to a huge localized concentration, and a greatly revised overall population estimate.

Desert wetlands In the Australian central desert, rainfall is more irregular in amount, timing and distribution than almost anywhere else on earth (Dingle, 2004). Persistent heavy rain can produce widespread flooding, giving rise to large areas of wetland habitat, while subsequent droughts can eliminate these wetlands for years on end (Roshier & Reid, 2002). Many thousands of temporary wetlands can vary in size from a few square metres to thousands of square kilometres. Some such as Lake Eyre are terminal water bodies filled by major drainage systems; others are lakes filled by local drainage or overflow areas from swollen rivers. These floodlands last at most a few months before they dry out. Whenever rain falls, they are re-created to varying extents, but at irregular intervals. In eastern Australia, total wetland varies from almost nothing in extreme drought years to more than 20,000 km2 in the wettest years (Figure 17.6).

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FIGURE 17.6 Temporal variation in the total water area in the major inland drainage basins of eastern Australia, 1986 2001. Modified from Roshier & Reid (2002).

During their short lives, these wetlands can be enormously productive of aquatic invertebrates and sometimes also fish. Most Australian waterfowl are highly mobile, and it is not uncommon, as ring recoveries have shown, for individual ducks to move more than 3000 km from one area to another (Roshier & Reid, 2002). The most extreme examples of nomadism include the Grey Teal (Anas gracilis), Freckled Duck (Stictonetta naevosa) and Pink-eared Duck (Malacorhynchus membranaceus), but many other species are also involved (Frith, 1967). As in deserts elsewhere, stilts and avocets benefit from the flooding of normally dry hollows, feeding on the masses of crustaceans that result. Other waders benefit mainly as the water evaporates, leaving as it withdraws a broad but temporary band of soft mud in which these birds can probe for prey. Both movement and breeding patterns have evolved to take advantage of such temporary bonanzas. Lake Eyre has been called the sump of Australia: a dry salt plain at times of drought, and a rich shallow lake extending over thousands of square kilometres at times of flood, perhaps once every 20 years. When floods begin, thousands of waterbirds appear and begin to breed. One colony of Australian Pelicans (Pelecanus conspicillatus) reached 50,000 pairs, the largest on record. Some birds must have travelled 1500 km to reach this area from the coast. It remains a mystery how such birds find suitable localities within vast desert areas: whether they search at random over appropriate range, relying entirely on visual cues, or whether they respond to climatic and other cues that indicate the most rewarding directions to fly. Older birds might remember specific sites, but this still leaves the question of how they know the time is right, as there is nothing regular about the rains that bring the floods. In theory, birds could find suitable areas by travelling with the wind, which blows towards the low-pressure areas that bring rain. They might also respond to gradients in temperature or air pressure. However, many birds arrive at floodwaters long after the weather that produced the flooding has gone, and in some cases the flooded land lies hundreds of kilometres from where the rain fell (Roshier et al., 2008a,b). So far, only limited numbers of desert nomads have been studied using tracking devices. For some satellite-tagged Grey Teal that made long-distance flights ( . 150 km), conditions at the origin and destination of the flights were examined from satellite images of the ground below (Roshier et al., 2008a,b). Two types of flight were distinguished: 13 out of 32 flights were regarded as targeted because they took the birds to major flooding events up to 1050 km away, while 11 other flights took birds to areas of minor rainfall. The rest were regarded as prospective in nature as the birds were apparently searching for suitable habitat. No birds were found to leave areas of good existing wetland. Typically, many species of the central Australian desert build up in numbers as a result of good breeding in occasional wet years, then move outwards to the more humid peripheral districts in the following dry years (Nix, 1976). Banded Stilts (Cladorhynchus leucocephalus) live for years as non-breeders on scattered briny coastal lagoons. But within days of rain falling inland, they concentrate in tens of thousands on newly formed shallow lakes, feeding on the freshly hatched swarms of brine shrimps Artemia or Paratemia (Robinson & Minton, 1989; Pedler, 2017). They breed while conditions last, making repeated nesting attempts, while the young form huge cre`ches. However, as the water evaporates, the land soon resorts to its normal parched state. The stilts then return to the coast, if necessary leaving the last thousands of eggs and young to die. Years may pass before they can breed again and not necessarily in the same sites. A more recent 6-year study, involving satellite imagery and aerial surveys, confirmed the inferences reported above but also revealed that breeding attempts were more frequent than expected from previous records. Across the area surveyed, nesting episodes were detected seven times more often than reported during the previous 80 years. However, many of these episodes were short-lived, as large nesting colonies that were formed following

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minor floods were mostly abandoned when the water evaporated before the eggs could hatch (Pedler et al., 2018). This would have further reduced the chance of breeding events being recorded. Within days of distant rainfall inland, two tagged Banded Stilts left the coast and flew 1000 2000 km inland to reach flooded salt lakes. On other occasions, twelve tagged birds rapidly moved 357 1298 km away from drying inland sites to the coast (Pedler, 2017).

Irruptive movements away from deserts Normally, desert species are able to remain within their regular range, in the wettest years penetrating deep into the driest areas, but at times of widespread drought, they may move out into neighbouring habitats, as in Australia. The same phenomenon is illustrated by the westward movements of Rose-coloured Starlings (Pastor roseus), Pallas’s Sandgrouse (Syrrhaptes paradoxus) and others from the Central Asian steppes into Western Europe. In their regular range, Rose-coloured Starlings may settle in thousands in suitable localities, breed and then move on. They feed their young mainly on grasshoppers and locusts and seldom occur in abundance in the same localities in successive years. Their irruptions outside the usual range occur in spring and early summer, apparently in years when birds return from winter quarters in the Indian subcontinent to find their food supply has failed over wide areas (Schenk, 1934). Big irruptions into Western Europe occurred in 1853, 1907 09, 1925, 1932 and 1948, but subsequently they became less frequent and extended less far, with only stragglers reaching Western Europe (Cramp & Perrins, 1994). However, a major movement into Europe occurred in summer 2002, with birds reaching as far as Britain and Iceland. In this year, many thousands of pairs bred outside the usual range, with an estimated 14,000 pairs in Romania, 2000 pairs in Bulgaria and 10,000 non-breeding birds in Hungary (Fraser & Rogers, 2004). Nesting at various places in Bulgaria coincided with an outbreak of locusts (Davies & Sharrock, 2000). More recent irruptions in Europe occurred in 2018, 2020 and 2021 (van der Spek, 2022). Ring recoveries are scarce, but of two birds ringed during an invasion in Hungary in spring 1925, one was recovered the next April in a wintering area nearly 5000 km to the east in Pakistan, and the other was recovered 11 years later, in July 1938, in the regular breeding range 3910 km to the east in Uzbekistan (van der Spek, 2022). The irruptions of Pallas’s Sandgrouse, which occurred from the steppes of Turkestan and Kazakhstan into western Europe in the spring summers of 1859, 1863, 1872, 1876, 1888, 1891, 1899 and 1908 (with small numbers in some of the intervening years and subsequently) were attributed to seed shortage (mainly of the chenopod (Agriophyllum globicum)) resulting from prolonged drought. Again, after each of these irruptions there were occasional breeding records, some from as far west as Britain. Irruptions in eastern Asia occurred in different years, indicating that regional factors affected different segments of the population. No substantial emigrations are known to have occurred subsequently, possibly because populations have declined following degradation of nesting habitat.

CONCLUDING REMARKS On a global scale, bird movements are clearly highly variable, compared with the regular there-and-back movements of most migrants. A few species breed in more than one area in the same year, and many occupy a succession of areas during each non-breeding season. Many migrate to special areas for moulting. Not all bird movements are restricted to spring and autumn; not all occur at the same seasons from year to year, and not all long-distance movements occur mainly around a north south axis, or even on a consistent axis. The irregularity of some of these movements implies that they occur as a direct response to habitat and food conditions at the time, and are in no sense ‘anticipatory’ as is much regular seasonal migration. For the most part, movement patterns have been inferred from local numerical changes. In a few species have they been supported by ring recoveries, and in even fewer by the use of modern tracking devices. The sparsity of information is expected in species which live mainly in areas where human population density is extremely low, and whose movements are so variable from year to year. More extensive use of satellite-based tracking should greatly improve our understanding of the nomadic movements of individual birds. In the meantime, many questions remain, notably: how do nomadic species know when and where to go? From how far away can they detect suitable conditions? How far do individuals move? And to what extent are their lifetime movements directional? As mentioned above, many birds classed as nomadic still have a north south component in their movements, in line with latitudinal seasonal trends in temperature and rainfall. Once again we see the different kinds of bird movements grading into one another, whether migration and nomadism or migration and dispersal. In any one population, however, one or two kinds usually prevail.

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The Migration Ecology of Birds

SUMMARY The movement patterns of birds are hugely variable, depending largely on ecological circumstances. Some waterfowl perform ‘moult migrations’ after breeding, when they move in large numbers to traditional sites, offering abundant food and safety. They stay at least long enough to moult their flight feathers, shedding them all at once, and remaining flightless for several weeks until replacement feathers are grown. Moulting sites can lie in any direction from breeding areas, although in many species of geese non-breeders and failed breeders migrate to moult at higher latitudes than their breeding areas, starting their migration to wintering areas soon after completing wing moult. In addition, some passerines and others in mountain areas move to higher elevations to moult, while some shorebirds and passerines moult at staging areas on their post-breeding migration, retaining their powers of flight throughout. Some bird species move within seasons, in summer raising successive broods in different places, or in winter occupying a succession of areas and moving further from their breeding range as the winter progresses. In many birds, winter movements occur in response to food shortages caused either by depletion of snow and ice or in response to frequent disturbance. Irruptive species, dependent on annually varying food supplies, migrate much further in some years than in others, concentrating wherever they encounter sufficient food. Nomadism occurs mainly in some southern hemisphere desert species which live under the influence of sporadic rainfall. Typically, they show little or no annual consistency in the timing and directions of their movements, but each year concentrate to breed wherever food (and in some species water) is available at the time. Some species of boreal and tundra regions are also nomadic in breeding areas to some extent, in association with sporadic tree-seed crops or rodent peaks. Some of these species are also seasonal north south migrants, moving much further in some years than in others, depending on food supplies, and each year concentrating where food is most available. Some Eurasian African migrants, while breeding in the same localities year after year, are to some extent nomadic in their African wintering areas, again concentrating wherever food is plentiful at the time.

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Variations on a migratory theme Chapter | 17

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Lack, D. (1956). Swifts in a tower. London, Methuen. Lack, D. (1963). Migration across the southern North Sea studied by radar. Part 5. Movements in August, winter and spring, and conclusion. Ibis 105: 461 92. Leu, M. & Thompson, C. W. (2002). The potential importance of migratory stopover sites as flight-feather molt staging areas: a review for Neotropical migrants. Biol. Conserv. 106: 45 56. Lincoln, F.C. (1935). The migration of North American birds. U.S. Dept. Agric., Washington D.C. Circular No. 363: 1 72. Little, B. & Furness, R. W. (1985). Long-distance moult migration by British Goosanders Mergus merganser. Ringing Migration 6: 77 98. Lislevand, T., Hahn, S., Rislaa, S. & Briedis, M. (2020). First records of complete annual cycles in Water Rails Rallus aquaticus show evidence of itinerant breeding and a complex migration system. J. Avian Biol. 2020: e02595. Mabie, D. W., Meredino, M. T. & Reid, D. H. (1994). Dispersal of Bald Eagles fledged in Texas. J. Raptor Res. 28: 2113 19. Maddock, M. (2000). Herons in Australasia and Oceania. Pp. 123 49 in Heron conservation (eds J. A. Kushlan, & H. Hafner). London, Academic Press. McKinnon, E. A., Fraser, K. C. & Stutchbury, B. J. M. (2013). New discoveries in landbird migration using geolocators, and a flight plan for the future. Auk 130: 211 22. McKinnon, E., Laplante, M.-P., Love, O. P., Fraser, K. C., MacKenzie, S. & Ve´zina, F. (2019). Tracking landscape-scale movements of Snow Buntings and weather-driven changes in flock composition during the temperate winter. Front. Ecol. Evol. 2019: 00329. Mead, C. J. (1979). Colony fidelity and interchange in the Sand Martin. Bird Study 26: 99 106. Mojica, E. K., Meyers, J. M., Millsap, B. A. & Haley, K. L. (2008). Migration of Florida sub-adult Bald Eagles. Wilson J. Orn. 120: 304 10. Moreau, R. E. (1951). The British status of the Quail and some problems of its biology. Br. Birds 44: 257 75. Moreau, R. E. (1972). The Palaearctic-African bird migration system. London, Academic Press. Newton, I. (2000). Movements of Bullfinches Pyrrhula pyrrhula within the breeding season. Bird Study 47: 372 6. Niles, D. M., Rohwer, S. A. & Robins, R. D. (1969). An observation of midwinter nocturnal tower mortality in Tree Sparrows. BirdBanding 40: 322 3. Nix, H. A. (1976). Environmental control of breeding, post-breeding dispersal and migration of birds in the Australian region. Proc. Int. Ornithol. Congr. 16: 272 305. Ndlovu, M., Cumming, G. S., Hockey, P. A. R., Nkosi, M. D. & Mutumi, G. L. (2013). A study of moult-site fidelity in Egyptian Geese, Alopochen aegyptiaca, in South Africa. African Zool 48: 240 9. Oring, L. W. (1964). Behaviour and ecology of certain ducks during the post-breeding period. J. Wildl. Manage 28: 223 33. Patterson, I. J. (1982). The Shelduck. A study in behavioural ecology. Cambridge, Cambridge University Press. Pedler, R. D. (2017). Banded tilt movement and breeding ecology in arid Australia. Ph.D. Thesis, Deakin University. Pedler, R. D., Ribot, R. F. H. & Bennett, A. T. D. (2018). Long-distance flights and high-risk breeding by nomadic waterbirds on desert salt lakes. Conserv. Biol. 32: 216 28.

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Phillips, L., Powell, A. N. & Rexstad, E. A. (2006). Large scale movements and habitat characteristics of King Eiders throughout the non-breeding period. Condor 108: 887 900. Piersma, T. (1987). Population turnover in groups of wing moulting waterbirds: the use of a natural marker in Great crested Grebes. Wildfowl 38: 37 45. Piironen, A., Paasivaara, A. & Laaksonen, T. (2021). Birds of three worlds: moult migration to high arctic expands a boreal-temperate flyway to a third biome. Movement Ecol 9: 47. Pizzey, G. & Knight, F. (2007). The field guide to the birds of Australia. Sydney, HarperCollins. Pulliam, H. R. & Parker, T. A. (1979). Population regulation of sparrows. Fortschr. Zool. 25: 137 47. Pyle, P., Leitner, W. A., Lozano-Angulo, L., Avilez-Teran, F. Swanson, H. et al. (2009). Temporal, spatial, and annual variation in the occurrence of molt migrant passerines in the Mexican monsoon region. Condor 111: 583 90. Pyle, P., Saracco, J. F. & Desante, D. F. (2018). Evidence of widespread movements from breeding to moulting grounds by North American landbirds. Auk 135: 506 20. Ridgill, S. C. & Fox, A. D. (1990). Cold weather movements of waterfowl in western Europe. Slimbridge, International Waterfowl and Wetlands Research Bureau, IWRB Special Publication 13. Robert, M., Benoit, R. & Savard, J.-P. L. (2002). Relationship among breeding, molting and wintering areas of male Barrow’s Goldeneyes (Bucephala islandica) in eastern North America. Auk 119: 676 84. Robinson, T. & Minton, C. (1989). The enigmatic Banded Stilt. Birds Int 1: 72 85. Rohwer, S., Hobson, K. A. & Rohwer, V. G. (2009). Migratory double breeding in Neotropical migrant birds. Proc. Natl. Acad. Sci. U.S.A. 106: 119050 5. Rohwer, S., Butler, L. K., Froehlich, D. R., Greenberg, R. & Marr, P. P. (2005). Ecology and demography of east west differences in molt scheduling of Neotropical migrant passerines. Pp. 87 105 in Birds two worlds (eds R. Greenberg, & P. P. Marra). Baltimore, MD, Johns Hopkins University Press. Roshier, D. A. & Reid, J. R. W. (2002). Broad scale processes in dynamic landscapes and the paradox of large populations of desert waterbirds. Pp. 148 55 in Avian landscape ecology: pure and applied issues in the landscape ecology of birds (eds. D. Chamberlain & A. Wilson). Proc. 11th IALE (UK) Conference, University of East Anglia. Roshier, D. A., Asmus, M. & Klaassen, M. (2008a). What drives longdistance movements in the nomadic Grey Teal Anas gracilis in Australia? Ibis 150: 474 84. Roshier, D. A., Doerr, V. A. J. & Doerr, E. D. (2008b). Animal movement in dynamic landscapes: interaction between behavioural strategies and resource distributions. Oecologia 156: 465 77. Salomonsen, F. (1968). The moult migration. Wildfowl 19: 5 24. Savard, J.-P. L. & Robert, M. (2013). Relationships among breeding, moulting and wintering areas of adult female Barrow’s Goldeneyes (Bucephala islandica) in Eastern North America. Waterbirds 36: 34 42. Schenk, J. (1934). Die Brutinvasionen des Rosenstares in Ungarn in den Jahren 1932 und 1933. Aquila 38 41: 136 53. Schueck, L., Maechtle, T., Fuller, M., Bates, K., Seegar, W. S. & Ward, J. (1998). Movements of Ferruginous Hawks through western North America. J. Idaho Acad. Sci. 34: 11 12.

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Chapter 18

Sex and age differences in migration

Male and female Chaffinch (Fringilla coelebs) For many years past, I have observed that, towards Christmas, vast flocks of Chaffinches have appeared in the fields. . . . when I came to observe them all narrowly, I was amazed to find that they seemed to me to be almost all hens. Gilbert White (1789).

In many bird populations, sex and age groups differ in aspects of their migrations, notably in the proportions of each sex and age group undertaking migration, the timing of outward and return journeys, and the distances travelled. The latter produce geographical gradients in the sex and age ratios of species in the non-breeding season, with one group predominating nearest to the breeding areas and the others further away. Such differences have been recorded in a wide range of bird species, including passerines, shorebirds, ducks, raptors, herons, seabirds and others. In some species, the differences are great, with little or no overlap between sexes or age groups, but in other species, the differences appear chiefly in mean values, with extensive overlap between groups. Most of the data on differential migration derive from observations and ring recoveries, and in recent decades also from tracking studies. In many species, sex and age groups also differ in body size. In most of these, males are bigger than females, but in raptors, owls, some shorebirds and others, females are bigger than males. These sex differences are usually slight, but in some species (notably some raptors and shorebirds), the differences are substantial, with one sex weighing up to twice as much as the other. In most birds, as judged by weights and wing lengths, juveniles are also slightly smaller than older birds of the same sex. Body size may affect the dominance status of individuals, their ability to withstand cold and food shortage, and various other features that could in turn affect their movement patterns. Sex differences in some aspects of migration have been known for a long time. The Swedish taxonomist Linnaeus in 1758 gave the scientfic name Fringilla coelebs (meaning ’bachelor finch’) to the Common Chaffinch because it was chiefly males which stayed to winter in Sweden where he lived, while females moved to lower latitudes. Nowadays, our knowledge of differential migration is still largely restricted to species in which the sex and age classes can be readily distinguished by colour or size. Few studies have yet examined sex-differentiated migration in sexually monomorphic species, because of the special methods (e.g., DNA analyses) needed to distinguish the sexes The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00003-8 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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(Catry et al., 2004; Remisiewicz & Wennerberg, 2006). So excluding monomorphic species, Cristol et al. (1999) listed 146 bird species in which sex or age differences in some aspect of migration were known or suspected, against 16 for which no evidence had been found (though often on small samples). Sex and age differences in migration are associated with: (1) the different roles of the sexes in breeding, which influence their migration timing; (2) the timing and extent of other events in the annual cycle, notably moult, which again influence migration timing; and (3) body size and dominance in which differences between sex and age groups can often be linked to both migratory timing and distances. These different aspects are explored below, followed by discussion of the movements of immature non-breeders.

ARRIVAL IN BREEDING AREAS Some birds, such as many waterfowl, arrive in spring on their breeding areas already paired. However, in most other bird species pair formation occurs in the breeding areas, with males arriving first on territories (called protandry) to which they then attract females. Some examples are given in Table 18.1, but many others, mainly from Europe and North America, can be found in Francis & Cooke (1986), Morgan & Shirihai (1997), Stewart et al. (2002), Newton (2008), Tøttrup & Thorup (2008) and Briedis et al. (2020). Most are based on birds caught on spring passage through ringing stations, and relatively few on arrivals in breeding areas (Figure 18.1). Several other findings have emerged from such studies. First, the lag between the mean arrival dates of males and females can vary between a few days in most species up to 3 weeks in others; second, the sex difference in mean arrival dates is generally greater in species which arrive early in the season than in those that arrive later (Francis & Cooke, 1986), and related to this, the difference is generally greater in short-distance than in long-distance migrants. Third, in warm springs when the whole migration begins early, sex differences tend to be greater than in cold springs when the whole migration begins later and is more compressed (Francis & Cooke, 1986; McKinnon et al., 2016). Fourth, within species in any one year, differences in the arrival dates of males and females are greater among the first arrivals of each sex than in the last arrivals of each sex (Tøttrup & Thorup, 2008). These statements are generalizations that apply to most but not to all species studied, and some have been found in a much wider range of species than others. Several hypotheses have been proposed to explain the earlier arrival of males (Morbey et al., 2012), of which the three most important are as follows: The cold tolerance hypothesis assumes that early arrival is advantageous and predicts that males arrive earlier in spring because, owing to their larger body size, they are better able than females to withstand the adverse weather that can be encountered on route or at breeding sites early in the season (Ketterson & Nolan, 1976, 1983). This explanation is most plausible for species in which the size difference between the sexes is great, but for most species, this difference is probably too small to have any significant effect, as is the difference in arrival dates. Moreover, some species arrive so late in spring that the weather is generally good by then. This hypothesis is also known as the cold susceptibility or body size hypothesis. The rank advantage hypothesis argues that male male competition for access to prime breeding sites is the main driver of protandry (Kokko, 1999). Nesting territories are often limited in number and variable in quality. So by arriving early, the argument goes, males gain access to the best of the territories available, thus raising their reproductive prospects. This is seen as a male male affair, with females playing no part except as a resource over which males later compete. However, similar competition and pressure for early arrival is likely to apply also to females. In some species, female female competition could be stronger than male male competition, because females compete for a resource namely males on territories that is initially scarcer than the vacant territories contested by males (Kokko et al., 2006). This could give selective pressure for females to arrive early in the migration season, although there would be little point in them arriving before males. In effect, there are both costs and benefits associated with arrival date, and in most species males gain more than females from arriving early (Morbey & Ydenberg, 2001). Much could depend on the sex ratio in the potential breeding population, and in many bird species males seem surplus to females among birds of breeding age (Lack, 1954; Newton, 1998). It is therefore uncertain how widely this rank advantage hypothesis could apply. It is also known as the arrival time or territorial defence hypothesis. In the third mating opportunity hypothesis, earlier arrival of males provides direct benefits in terms of mating success, whether by providing a mate from a limited number available, by providing more than one mate as in conventional polygyny or by providing more opportunities for extra-pair copulations (and subsequent paternity). Field studies have provided abundant evidence that early arriving males do indeed acquire the best territories and mates (judged on past performance), a greater number of mates in polygynous species (Hasselquist, 1998; Reudink et al., 2009), and more often achieve extra-pair paternity (Langefors et al., 1998; Møller et al., 2009) and higher overall reproductive

Sex and age differences in migration Chapter | 18

357

TABLE 18.1 Sex and age differences in the timing and distance of migration in various bird species. Autumn departure (earliest latest)

Distance travelled (nearest furthest)

Spring arrival (earliest latest)

Sources

Common Chaffinch (Fringilla coelebs)

JF, JM, AF, AM

JM, AM, JF, AF

AM, AF, JM, JF

Schifferli (1963), Payevsky (1998)

Brambling (Fringilla montifringilla)

J, A

JM, JF, AM, AF

Snow Bunting (Plectrophenax nivalis)

J, AM, AF

AM, JM, AF, JF

AM, AF, J

Meltofte (1975), Smith et al. (1993), McKinnon et al. (2016)

Dark-eyed Junco (Junco hyemalis)

F, M

JM, AM, JF, AF

AM, JM, AF, JF

Ketterson & Nolan (1983)

White-crowned Sparrow (Zonotrichia leucophrys)

JM, AM

AM, JM, AF, JF

King et al. (1965), Morton (2002)

Blue Tit (Cyanistes caeruleus)

M, F

AM, AF, JM, JF

A, J

Smith & Nilsson (1987)

F, M

F, M

M, F

Cade & Hoffman (1993)

M, F

M, F

Schroeder & Braun (1993)

AM, AF, JM, JF

Wallin et al. (1987), Village (1990), Kjelle´n (1992, 1994)

Passerines

Jenni (2021)

Non-passerines Blue Grouse (Dendrogapus obscurus) Prairie Chicken (Typanuchus cupido) Eurasian Kestrel (Falco tinnunculus)

J, AM, AF

AM, AF, JM, JF

American Kestrel (Falco sparverius)

JF, JM, AF, AM

AM, AF, JM, JF

Osprey (Pandion haliaetus)

AF, AM, J

AM, AF

AM, AF, I

Hoffman et al. (2002), Bai & Schmidt (2012)

Eurasian Sparrowhawk (Accipiter nisus)

JF, JM, AF, AM

AF, AM, J

AM, AF, JF, JM

Saurola (1981), Kjelle´n (1992)

Northern Harrier (Circus hudsonius)

J, AF, AM

F, M

AM, AF, JF, JM

Hamerstro¨m (1969), Mueller et al. (2000)

Western Marsh Harrier (Circus aeruginosus)

J, AF, AM

J, AF, AM

Kjelle´n (1992), Agostini et al. (2021)

European Honey Buzzard (Pernis apivorus)

A, J

AM, AF, J

Kjelle´n (1992), Howes et al. (2020)

Tufted Duck (Aythya fuligula)

AM, AF, J

M, F

M, F

Wernham et al. (2002)

Western Sandpiper (Calidris mauri)

M, F

M, F

M, F

Harrington & Haase (1994), Bishop et al. (2004)

Great Cormorant (Phalacrocorax carbo)

J, A

AM, AF, J

AM, AF, J

Bregnballe et al. (1997)

Scolopi’s Shearwater (Calonectris diomedia)

AM, AF

AM, AF

AM. AF

Mu¨ller et al. (2014)

Black-browed Albatross (Thalassarche melanophrys)

AF, AM

AM, AF

AM, AF

Phillips et al. (2005)

Arnold (1991), Mueller et al. (2000), Hoffman et al. (2002)

For data on other North American species see Benson & Winker (2001) and Carlisle et al. (2005), and for sex-related differences in migration distances of Nearctic species wintering in the tropics see Komar et al. (2005). Migration timing is in some species inferred from passage dates, rather than from departure and arrival dates. M male, F female, A adult, J juvenile less than one year, I immature, older than one year but not of adult breeding age. For many more examples, see Newton (2008).

Cumulative total (%)

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The Migration Ecology of Birds

100 90 80 70 60 50 40 30 20 10 0

Adult male 1st year male Adult female 1st year female

0

10

20 30 40 Day of arrival (standardised)

50

FIGURE 18.1 Spring arrival schedules of Whitecrowned Sparrows (Zonotrichia leucophrys) at Toiga Meadow Pass, California. The records for 4 years are standardized so that the date the first bird was captured each year was called Day 1 of arrival for that year. Older males (N 5 82) arrived on average 5.4 days earlier than first-year males (N 5 62, t 5 4.20, P , .001), and older females (N 5 43) arrived, on average, 5.0 days earlier than first-year females (N 5 51, t 5 2.51, P 5 .014). Overall, however, the arrival dates of different sex and age groups overlapped considerably. From Morton (2002).

output that year than later arriving males (Chapter 15). Other studies revealed that males arrived more in advance of females in those species likely to be subject to strong sexual selection. Thus among migratory songbirds, the number of days separating the average arrival dates of males and females was found to be greater in species showing the greatest degree of (a) sexual colour differences (Rubolini et al., 2004), (b) sexual size differences (Kissner et al., 2003; Briedis et al., 2020), and (c) extra-pair paternity among males (Coppack et al., 2002; Canal et al., 2012). These measures can all be taken as indicators of the strength of sexual selection by female choice. In addition, theoretical models have also highlighted the mating opportunity hypothesis as the most plausible of the various explanations for spring protandry in migratory birds (Kokko et al., 2006). Whatever the evolutionary causes underlying protandry, adults that arrive after their former territory has already been occupied by another individual of the same sex are sometimes able to oust the newcomer, but much depends on how long the new bird has had to establish itself (Newton, 1998). In general, however, birds that arrive late relative to others of their sex have less choice and are relegated to less favoured territories where they produce fewer young (Chapter 15). Some late-comers may fail to acquire a mate or even a territory in habitats that appear fully occupied (Newton, 1998). That the sex difference in arrival time is linked to reproduction is also consistent with other observations. Firstly, while males arrive earlier than females in spring when breeding is about to begin, the two sexes migrate at about the same dates as one another in autumn when breeding has finished for that year (for Bluethroat (Luscinia luscinia), see Ellegren, 1990; for Eurasian Blackcap (Sylvia atricapilla), see Izhaki & Maitav, 1998; for Red-backed Shrike (Lanius collurio), see Pedersen et al., 2019). Secondly, in species in which females rather than males establish territories, the females arrive first (protogyny). In some shorebird species, females are bigger than males and undertake some aspects of breeding that in most bird species fall to males. In these species, the females compete with one another for territories and for the later-arriving males which, after the eggs are laid, take on the remaining parental duties. Examples include the Eurasian Dotterel (Charadrius morinellus), the three phalarope Phalaropus species, and Spotted Sandpiper (Tringa macularia) (Myers, 1981; Oring & Lank, 1982).

How does one sex achieve an earlier arrival than the other? The above hypotheses were concerned with the ultimate (evolutionary) causes of differential spring migration, but a further question is how males (or females) achieve their earlier arrival (the proximate causes). In principle, sexual differences in spring arrival dates could result from one sex showing: (1) an earlier start to migration than the other, (2) shorter travel distances as a result of wintering nearer to breeding areas, (3) a faster migration, or (4) some combination of these aspects (Coppack & Pulido, 2009). All these mechanisms have been documented. Starting dates. In many passerines and shorebirds, in which the sexes winter side by side in the same area, males fatten and leave first (Rogers & Odum, 1966; Nisbet & Medway, 1972; Cramp, 1988; Bishop et al., 2004; Catry et al., 2005). Also, in recent tracking studies males left wintering areas before females. On the basis of more than 350 migration tracks of 14 species of small trans-Saharan migrants, males departed from their African non-breeding sites, on average, about 3 days earlier and reached their European breeding sites about 4 days earlier than females (Briedis et al., 2020). The same has been observed in some larger species, such as White Stork (Ciconia ciconia) (Rotics et al., 2018). When kept in captivity under identical conditions and natural spring photoperiods, males of various species also began migratory activity before females (for Dark-eyed Juncos (Junco hyemalis), see Holberton, 1993; for Blackcap, see Terrill & Berthold, 1989; for Garden Warbler (Sylvia borin), see Widmer, 1999; for Pied Flycatcher (Ficedula hypoleuca) and Common Redstart (Phoenicurus phoenicurus), see Coppack & Pulido, 2009). In all these studies, sexual

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359

differences in the onset of migratory activity were at least as large as the sexual difference in arrival dates observed in the populations from which the captive birds were taken. This suggests that, in these species, sex differences in the onset of migration were caused primarily by different endogenous cycles or photoperiodic sensitivities. Moreover, in captivity male Northern Wheatears (Oenanthe oenanthe) started their spring migratory activity earlier than females not only when they were kept under natural photoperiods but also when they were kept under constant photoperiods. This implied that the sex difference was endogenously controlled, as an inherent attribute (Maggini & Bairlein, 2012). In tracking studies, individual differences in departure dates were usually maintained through the migration so that arrival and departure dates were positively correlated, as in Great Reed Warblers (Acrocephalus arundinaceus) (Lemke et al., 2013), Common Redstarts (Kristensen et al., 2013), Wood Thrushes (Hylocichla mustelina) (Stanley et al., 2012, Figure 12.2) and Red-backed Shrikes (Tøttrup et al., 2012; Pedersen et al., 2019). The shrikes began their migration in South Africa several thousand kilometres from their breeding areas and took several months over the journey, yet maintained the sexual time difference throughout (Pedersen et al., 2019). Despite these hardwired control mechanisms, the timing of migration in spring may be modified by the physical condition of the individual bird, as well as by the conditions encountered on route (Chapters 14, 15; Gordo, 2007; Pulido, 2007). Wintering areas. In many birds of northern regions, males spend the winter closer to their breeding areas, on average, than do females (see below), so even if the two sexes started migration on the same dates, males should be first to arrive. Several studies confirm that birds wintering closer to breeding areas often get back earlier in spring, but in these studies sexes were not distinguished (Liechti et al., 2015; Woodworth et al., 2016; Ho¨tker, 2002; Rotics et al., 2018; Bregnballe et al., 2006). Nevertheless, by wintering closer to breeding areas, male birds could expedite their return to the breeding grounds in three ways. First, the distance between non-breeding and breeding areas is shorter and travelling time is consequently reduced. Secondly, photoperiodic cues experienced by males wintering at higher latitudes could cause an earlier onset of spring migration (Coppack & Pulido, 2009). Thirdly, by remaining nearer to breeding areas, males should experience weather more typical of the breeding area, and thus be able to return there as soon as conditions permit, whereas this is more difficult for females wintering further away (Alerstam & Ho¨gstedt, 1982). Migration speeds. Studies on some protandrous species indicate that males also travel faster on migration than females, mainly through having fewer or shorter stops. In competitive situations, males can feed faster than females and accumulate fuel reserves and complete the journey more rapidly (Lindstro¨m & Alerstam, 1992; Moore et al., 2003; Seewagen et al., 2013, Chapter 13). These differences may result from the greater dominance of males, giving them better access to food supplies, and perhaps widening the sex difference in migration timing as birds travel towards their destinations.

Age differences in arrival dates In addition to the sex difference in arrival dates, young birds nesting for the first time typically arrive on their breeding areas some days later than older and more experienced birds of the same sex. Such age differences have been noted in a wide range of species, from passerines and raptors to shorebirds and seabirds (Table 18.1; Stewart et al., 2002; Newton, 2008). Two proposed explanations are not mutually exclusive. First, because young birds cannot compete effectively with older ones for nesting territories, they are better to arrive later in the season, when most old birds have already settled, thereby saving the energy they would otherwise waste on futile battles. On this basis, later arrival would be under endogenous (genetic) control. Secondly, because of their inexperience and subordinate status with respect to older birds, young adults cannot feed as efficiently before departure from wintering or stopover sites, so are delayed on migration (Chapter 14). On this basis, later arrival is under external influence and results partly from prevailing conditions. In Wood Thrushes migrating north from South America, juveniles not only departed later from tropical wintering sites than adults but also became progressively later as they moved northward. The increasing delay was driven by more frequent short stops by juveniles along the way, particularly as they got closer to breeding sites, perhaps needed to feed and maintain body condition. Juveniles also had smaller wings than adults which may have increased their energy expenditure during migration (McKinnon et al., 2016).

DEPARTURE FROM BREEDING AREAS Most birds set off on autumn migration soon after breeding (in species which suspend or postpone moult for stopover or wintering areas), or after they have finished breeding and moulting (in species that moult in breeding areas). In either case, failed breeders can usually depart on migration earlier than successful breeders which must stay and rear their

360

The Migration Ecology of Birds

young to independence. In some species, the two sexes depart at about the same dates, on average, but in other species the two sexes migrate at markedly different dates, linked with differences in their parental roles. Where only one sex looks after the young, the other migrates at an earlier date. This is seen, for example, in most duck species in which the males play no part in parental care and leave their breeding places up to several weeks before the females and young (Chapter 17; Cramp & Simmons, 1977). The same holds in some shorebird species in which only the females remain with the young until they are full-grown, while the males leave at earlier dates (as in Curlew Sandpiper (Calidris ferruginea) and Ruff (Calidris pugnax)). In other shorebirds, however, the males raise their young to independence, and the females depart earlier (as in Spotted Redshank (Tringa erythropus), Wood Sandpiper (Tringa glareola) and Grey Plover (Pluvialis squatarola)). This latter difference is greatest in phalaropes and others in which females depart after egg-laying, several weeks before males, leaving all incubation and chick care to their partners (Jehl, 1986). In yet other shorebirds, both partners help to the same stage with parental care, and the two sexes migrate at about the same time as in Northern Lapwing (Vanellus vanellus) and Black-tailed Godwit (Limosa limosa). In all these shorebird species, the young tend to leave after the adults, perhaps requiring longer to prepare themselves, but also being free of the need for a complete post-breeding moult. Hence, the general sequence of post-breeding migration in shorebirds begins with failed breeders, followed by the successful breeders of the non-parenting partner, then the parenting partner (or both partners), and finally the young. Departure dates in a population can thus spread over several weeks, as can the subsequent arrival dates in moulting or wintering areas (Cramp & Simmons, 1983). In migratory populations of many small raptor species, such as the Eurasian Sparrowhawk (Accipiter nisus) and Sharp-shinned Hawk (Accipiter striatus), the adults migrate after completing moult. Females start moult around the time of egg-laying, while the males, who provide the food, delay the start of moult until around the time of hatch. This difference enables the females to finish moulting and depart on migration earlier, leaving any remaining parental care to their mate (Kjelle´n, 1992). Larger raptors start moult while they are breeding but then suspend moult while they migrate, females usually leaving before their partners (up to 3 weeks earlier in the Osprey (Pandion haliaetus), Martell et al., 2001). However, in the European Honey Buzzard (Pernis apivorus), in which the sexes share breeding duties equally, partners depart at similar dates. Other bird species which show some degree of uniparental care show similar marked sexual divergence in autumn migration dates. The fact that these patterns are repeated independently in different phylogenetic groups further emphasizes the link between the breeding system and the timing of autumn migration. Passerines and other species in which both sexes help to rear the young to independence show at most minor sex differences in autumn departure dates, amounting to only a few days in mean dates (Mills, 2005; Briedis et al., 2020; Lehikoinen et al., 2017). Nevertheless, in many species, these differences are consistent and statistically significant. Various explanations have been proposed, some drawing on the same ideas as for spring migration: The breeding investment hypothesis. Where males leave breeding areas ahead of females, on average, it has been suggested that females might end breeding in poorer conditions than males and need longer to prepare for migration (Lehikoinen et al., 2017; Briedis et al., 2020). The same could hold for later departing males in species in which males play a bigger role in parental care. This hypothesis should not apply to juveniles. The longer migration hypothesis. Where females migrate a few days before males, on average, this has been viewed as an adaptation to females having to cover longer distances to reach more distant wintering areas, a difference also recorded in young of the year (for Ruby-crowned Kinglet (Corthylio calendula), see Mills, 2005; for Bluethroat, see Ellegren, 1991). The cold tolerance hypothesis. The larger sex should be able to stay longer into autumn because of its lower susceptibility to falling temperatures (Ketterson & Nolan, 1976; Mills, 2005). This is likely to apply, if at all, to short-distance migrants which are the latest species to leave their breeding areas; long-distance migrants normally depart earlier, while conditions are still mild. It should hold for juveniles as well as adults. The rank advantage hypothesis. When applied to the acquisition of winter territories, the idea is that females and juveniles should depart first to gain some priority in territory acquisition (Mills, 2005). At this season, males and females usually occupy different territories, rather than sharing territories, as in the breeding season. Hence, the advantage of early arrival in winter quarters should apply to both sexes, but perhaps more to females. Nevertheless, dominant males arriving later may be able to displace newly established females, and in addition this hypothesis is unlikely to apply to the many species that are non-territorial in winter and forage in flocks. The mating advantage hypothesis. When applied to departure dates, the idea is that males should migrate later after breeding to protect as long as possible their future breeding territory. In some species, this behaviour appeared to help males secure the same territory in the following year (for Black Redstart (Phoenicurus ochropus), see Weggler, 2000; for Dusky Warbler (Phylloscopus fuscatus), see Forstmeier, 2002). In theory, this hypothesis could also apply to juvenile birds which in some species seek temporary territories before they leave on migration, returning to them the

Sex and age differences in migration Chapter | 18

361

following spring to breed (for European Robin (Erythacus rubecula), see Zimin, 2001, 2002; for Black Redstart, see Weggler, 2000). Interestingly, species which showed the greatest degree of spring protandry (males arriving before females on breeding areas) also showed the greatest degree of autumn protogyny (females leaving breeding areas before males), a relationship found, for example among nine passerines migrating through Heligoland Island (Figure 18.2; Coppack & Pulido, 2009). This could be taken as further evidence that territory defence (and consequent reproductive success) is a major factor underlying sex differences in the migration dates of some species. As yet, however, none of these hypotheses can be considered well supported, and all require further assessment. They could all apply to at least to some species: the breeding investment hypothesis at least to those species showing big differences in parental care; the longer migration hypothesis to species in which one sex migrates further than the other; the cold-tolerance hypothesis to short-distance migrants which stay latest in their breeding areas when temperatures are falling; the rank advantage hypothesis to species which establish territories in winter quarters; and the mating advantage hypothesis to those species which establish or re-establish territories after breeding to which they return next year. Some of the sex differences in mean dates are very small, however, in some species only 1 3 days. They may be statistically significant but their biological significance is less certain. Some studies have also revealed sex differences in the timing of autumn migration in juveniles. Among 14 passerine species caught at Bird Observatories in Finland in autumn, adults showed either no difference in migration dates between the sexes (12 species) or protandry with males leaving first (two species). Among juveniles, significant sex differences in juveniles were found in 10 out of 14 species, in all of which females left, on average, 1 7 days before males (Lehikoinen et al., 2017). This was in line with all but the first of the above hypotheses. Furthermore, among short-distance migrants the sex difference in migration timing was significantly connected with the degree of sexual size dimorphism in species, perhaps in line at least with the cold tolerance hypothesis.

Age differences in departure from breeding areas Age differences in autumn migration dates have been recorded in a wide range of bird species, from passerines to raptors and shorebirds and seabirds (Figures 18.3 and 18.4). The link with previous events in the annual cycle is again strongly apparent. Among passerines, the adult juvenile difference seems to depend on whether birds moult in breeding areas before they migrate, or whether they migrate immediately after breeding, with moult either started and then suspended or delayed until after they arrive in wintering areas (Chapter 12). Most species that moult completely before autumn migration are short-distance (usually partial) migrants, while most of those that arrest or delay moult are long30

15

Males earlier

Spring protandry (days)

20

7

10

4

5

9

R S = 0.90, P < 0.01

25

1

3 2

8

6 5 Males later

0 -2

0

2 4 Autumn protogyny (days)

6

8

FIGURE 18.2 Correlation between the extent of protandry during migration in the spring and the extent of protogyny in autumn among nine Palaearctic passerine migrants trapped between 1960 and 2000 at Heligoland, off Germany. Ring recoveries indicate that migrants caught on Heligoland originate from Scandinavian breeding populations. (1) Eurasian Blackcap (Sylvia atricapilla); (2) Common Linnet (Linaria cannabina); (3) Common Whitethroat (Curruca communis); (4) Redstart (Phoenicurus phoenicurus); (5) Ring Ouzel (Turdus torquatus); (6) Common Blackbird (Turdus merula); (7) Goldcrest (Regulus regulus); (8) Common Chaffinch (Fringilla coelebs); and (9) Common Reed Bunting (Emberiza schoeniclus). The degree of protandry is defined as the difference between the median trapping dates of females and males, with positive values signifying earlier passage of males. The degree of protogyny in autumn is defined as the difference between the median trapping dates of males and females, with positive values signifying earlier migration by females. Level of significance based on Spearman’s rank correlation. Modified from Coppack & Pulido (2009).

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The Migration Ecology of Birds

FIGURE 18.3 Migration departure schedules of (a) juvenile and (b) adult Whitecrowned Sparrows (Zonotrichia leucophrys) based on the pooled data for 7 years from Toiga Meadow Pass, California. No sex difference in departure dates was detected, but juveniles left 3.2 days earlier, on average, than males. The range of departure dates was 45 days for juveniles, and 37 days for adults, with most of the variation traceable to inter-year variation in breeding dates. Departure was delayed about 1 day for every 2 days that nesting had been delayed by environmental conditions, such as persisting snow cover earlier in the summer. Over the 7-year period, mean departure date varied by about 14 days in juveniles and 8 days in adults. From Morton (2002).

Percent of departures

(a) 40 Juveniles N = 241 30 20 10 0 5

10

15

20

25

30

5

10

15

20

20

25

30

5

10

15

20

Percent of departures

(b) 40 Adults N = 199

30 20 10 0 5

10

15

Day of departure

distance migrants wintering in the tropics. In short-distance migrants, juveniles migrate earlier than adults, on average, presumably because the juveniles replace only their body feathers, a process which takes less time than the adults take to replace their entire plumage, including flight feathers. But in species that suspend or postpone moult, the adults can leave their nesting areas soon after their young become independent, while the young themselves take another week or more before they are ready to undertake their first migration. This dichotomy seems to hold as a general rule in passerines, with only rare exceptions where both age groups leave at the same mean dates (Benson & Winker, 2001; Carlisle et al., 2005; Newton, 2008; Kiat & Izhaki, 2016). Throughout its range, the Common Cuckoo (Cuculus canorus) provides an extreme example of an age difference, for the adults leave before their last young, reared by other species, have even left the nest, giving a difference in mean departure dates between the two age groups of about 1 month (Wyllie, 1981). Both adults and young moult in winter quarters. An opposite pattern occurs in the Yellow-bellied Flycatcher (Empidonax flaviventris) in North America, in which adults migrate before they moult but juveniles only after completing their partial post-juvenile moult. This results in juveniles showing peak passage dates along the Texas coast nearly a month later than those for adults (Rappole, 2013). Similar departure patterns are seen in raptors (Table 18.1; Figure 18.4). In short-distance migrants that finish moult before migrating, such as the Eurasian Sparrowhawk, juveniles leave the breeding areas earlier than adults. The juveniles do not moult in their first autumn of life but retain their juvenile plumage (acquired in the nest) for another year. But in most long-distance migrants in which adults suspend moult and migrate immediately after breeding, such as the Osprey and Honey Buzzard, most adults tend to leave before juveniles, departing as soon as the young are independent but still gaining the experience necessary to undertake migration. After nesting in the arctic, adult shorebirds usually leave their breeding areas well before the juveniles, and moult at a migratory staging site or in winter quarters. This temporal difference can be increased by the juveniles’ slower progress on migration, resulting from longer and more frequent stopovers, use of poorer sites and less direct migration routes (Saurola, 1981; Evans & Davidson, 1990; Baccetti et al., 1999). In some populations in which only the adults stop and moult at a staging site, the two age groups arrive in wintering areas at about the same date, as observed in Dunlins (Calidris alpina) in southern Europe (Baccetti et al., 1999). Hence, in all these species from different phylogenetic groups, whether adults or juveniles depart first on autumn migration is linked to whether or not they migrate immediately after breeding, and where and when they moult. The pressures are somewhat different in juveniles and adults because, while the juveniles have a shorter moult restricted to body feathers (or in some species no moult), the adults have a longer complete moult, including flight and tail feathers.

Sex and age differences in migration Chapter | 18

Sparrowhawk

(a) 4000 2000

30 Adult Male Female

Adult Juvenile

20 10 0 Numbers seen

0 Numbers seen

Hobby

(b)

6000

363

2000 4000 6000

10 20 30 40

8000 Juvenile Male Female

10 000 12 000

50 60 70

14 000 Jul

Aug

Sep

Oct

Nov

Jul

Aug

Sep

Oct

Nov

FIGURE 18.4 Numbers of (a) Eurasian Sparrowhawks (Accipiter nisus) and (b) Eurasian Hobbies (Falco subbuteo) seen migrating through Falsterbo, Sweden, at different dates in autumn. In the Sparrowhawk, which is a partial migrant, juveniles moved before adults and females before males. Similar patterns were shown by other partial migrants, including Northern Goshawk (Accipiter gentilis) and Red Kite (Milvus milvus). In the Eurasian Hobby, which is a complete long-distance migrant, adults moved before juveniles, but sexes could not be distinguished. Similar patterns were shown by other complete long-distance migrants, including European Honey Buzzard (Pernis apivorus), Montagu’s Harrier (Circus pygargus) and Osprey (Pandion haliaetus). From Kjelle´n (1992).

Another common trend is for young hatched earlier in the season to migrate earlier than those hatched later, but the later young also migrate at a younger age, allowing them to leave before winter sets in. This has been noted in Blackcaps and others in captivity, and in many other species in the wild (Chapter 13). Among Eurasian Spoonbills (Platalea leucorodia) nesting in the Netherlands, young fledged early in the season migrate both earlier and further than late-fledged young (Lok et al., 2011).

MIGRATORY DISTANCE, BODY SIZE AND DOMINANCE In many species, as mentioned already, birds of different sex and age groups migrate different distances from one another, again with some overlap but giving some latitudinal segregation of the sexes and ages in wintering areas. Such patterns have been repeatedly shown from recoveries of birds ringed at the same breeding or staging places (Figure 18.5). In most such species, females migrate further, on average, and winter at lower latitudes than males. This difference is substantial in the Ruffs that migrate through Western Europe, in which most males remain within Europe, whereas most females winter in sub-Saharan Africa, where females (which are smaller) can outnumber males by more than ten to one (Gill et al., 1995). Other studies have examined sex ratios among birds from different wintering localities, either by observation or from trapped samples or museum skins. They include a wide range of species, some of which winter in temperate areas and others in tropical areas (Table 18.1; Komar et al., 2005). These studies have also revealed geographical gradients in winter sex ratios, with a predominance of males nearest the breeding areas and of females furthest away. Such gradients are common in diving ducks (Figure 18.6; Nichols & Haramis, 1980; Alexander, 1983; Carbone & Owen, 1995), but less pronounced in dabbling ducks in which many individuals form pairs in early winter and remain together thereafter (Owen & Dix, 1986; Hepp & Hines, 1991). Among studies reviewed by Cristol et al. (1999), females migrated further than males in at least 77% of 53 species, and young migrated further than adults in at least 38% of 53 species. Individuals migrating further were usually from those sex and age groups whose body size was smaller (71% of 69 size comparisons between population classes), socially subordinate (82% of 44 comparisons), and later to arrive at breeding areas (74% of 58 comparisons). However, as implied by the figures, some species deviated from these patterns; and while in most, the smaller sex migrated further, in some the smaller sex migrated less far. So although certain patterns are widespread among birds, they are not universal. Five main hypotheses attempt to explain sex differences in migration distances and the resulting latitudinal trends in winter sex ratios. The cold tolerance hypothesis assumes that sexual segregation in winter is linked to differential

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The Migration Ecology of Birds

FIGURE 18.5 Mean distances between ringing and recovery sites for adult (N 5 961) and juvenile (N 5 84) Common Starlings (Sturnus vulgaris). The birds were ringed in their breeding areas in eastern North America and recovered in winter (January February) further south. Birds from further north moved longer distances, but juveniles moved further than adults. Modified from Dolbeer (1982).

FIGURE 18.6 Sex ratios among wintering Pochards (Aythya ferina) in relation to latitude in Western Europe. Redrawn from Carbone & Owen (1995).

Males per 100 females

350 300 250 200 150 100 50 0 35

40

45 50 Degree latitude

55

60

susceptibility to cold, with larger-bodied males able to winter further north, closer to breeding areas (Ketterson & Nolan, 1976, 1979; Jenkins & Cristol, 2002). The dominance hypothesis assumes that subordinate females are forced by competition with dominant males to move further from breeding areas (Terrill, 1987; Choudhury & Black, 1991). The rank advantage (arrival time) hypothesis considers differential advantages between males and females in the timing of arrival in breeding areas, with the territorial sex (usually male) benefiting through wintering closer to breeding areas (Ketterson & Nolan, 1979; Stouffer & Dwyer, 2003). The ‘predation risk hypothesis’ proposes that the latitudinal distribution of males and females should vary with weight-dependent predation risks (Nebel & Ydenberg, 2005). Birds escape more easily from avian predators if they are light and agile (Kullberg et al., 2000). In general, birds carry less fat in warmer climates than cold ones, so gain more security by moving closer to the equator (eg Davidson, 1984). In sexually dimorphic species, this advantage is greatest in the heaviest sex which might therefore be expected to winter in warmer latitudes than the lighter sex. Such a pattern is apparent in some wader species. Lastly, the resource partitioning hypothesis predicts that sex differences in feeding habits lead to a spatial separation of males and females, for example in those waders which show sexual dimorphism in beak size, enabling the sexes to probe to different depths. The sub-surface invertebrate prey of some waders may be found at greater average depth with increasing proximity to the equator where ambient temperatures are higher (Mathot et al., 2007). Correspondingly, in the Curlew Sandpiper males are smaller with a shorter beak than females and migrate further into the southern hemisphere (to higher latitudes). Yet again, however, these different explanations of sex differences in migration distances could apply to different species, and several explanations could apply to any one species. All are speculative and mostly untestable. The body size and dominance hypotheses are for obvious reasons hard to separate. Little evidence of sex differences in migration distances was found in the American Woodcock (Scolopax minor), Sanderling (Calidris alba) and Red Phalarope (Phalaropus fulicarius), despite females being larger than males (Myers, 1981; Diefenbach et al., 1990), nor in American Black Ducks (Anas rubripes) in which males are bigger than females (Diefenbach et al., 1988). Nor were such differences found in Eurasian Siskins (Spinus spinus) and Savannah Sparrows (Passerculus sandwichensis) in which the sexes are of similar size (Payevsky 1998; Rising, 1988). On the other hand, among Indigo Buntings (Passerina cyanea) migrating from North to Central America, the usual sequence is reversed, as females

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predominate in the northern part of the wintering range and males in the southern part (Komar et al., 2005). These examples again emphasize that, although some patterns of behaviour are widespread among birds, exceptions are numerous. The sexes of albatrosses often use markedly different regions, both in their immature years and in their later nonbreeding periods. For example among Wandering Albatrosses (Diomedia exulans) nesting on the Crozet Islands, females moved north and northwest to occupy tropical and subtropical waters located southeast of Africa whereas males moved south and southeast and more than double the distance to occupy sub-Antarctic and Antarctic waters lying south ˚ kesson & Weimerskirch, 2014). Similar large differences in non-breeding areas between and southeast of Australia (A the sexes were also noted in Black-browed (Thalassarche melanophrys) and Grey-headed Albatrosses (Thalassarche chrysostoma). These findings did not necessarily imply genetically controlled sex differences in migratory direction, if birds simply head in the direction in which they can most efficiently fly. In all three species, the larger sex with heavier wing-loading foraged in ocean zones with stronger winds (Phillips et al., 2004). The seasonal sex segregation in these birds could therefore be attributed to niche divergence mediated by differences in flight performance. Whatever the reason why the sexes of a species winter in mainly different regions, this segregation could have important consequences. The regions concerned could differ in their ability to support the numbers of birds involved, leading to differential mortality rates and marked inequalities in sex ratio. In addition, by wintering in largely different regions, the two sexes could come under different selection pressures, leading to greater divergence in body size and other features than might occur if they wintered in the same regions. These are further aspects of differential migration that have yet to receive attention from researchers.

Age-related differences in migration distances Any major sex difference in migration distances shown by adults of a species is also apparent among the juveniles, but within sexes the juveniles tend to move further. For example based on ring recoveries, such differential migration by age classes was found in 10 species of British seabirds: Gannet (Morus bassanus), Great Cormorant (Phalacrocorax carbo), European Shag (Gulosus aristotelis), Black-headed Gull (Larus ridibundus), Lesser Black-backed Gull (Larus fuscus), Herring Gull (Larus argentatus), Great Black-backed Gull (Larus marinus), Common Murre (Guillemot) (Uria aalge), Razorbill (Alca torda) and Atlantic Puffin (Fratercula arctica) (Wernham et al., 2002). The magnitude of these age-related differences varied between species, with median distances of 141 and 84 km in immature and adult Blackheaded Gulls, ranging up to 1380 and 639 km in immature and adult Gannets. Similar differences emerged from other studies of seabirds (eg for Great Cormorant, see Bregnballe et al., 1997; for three large gull species, see Kilpi & Saurola, 1984), and in several species of terns the wintering areas of different age groups were almost completely segregated (for Common Terns (Sterna hirundo) in the West Atlantic, see Hays et al., 1997; for Roseate Terns (Sterna dougallii) in the eastern Asian Australasian flyway, see Minton, 2003). Because adults are usually slightly larger than juveniles, the cold tolerance hypothesis has been proposed as an explanation for the age differences in migration distances, but it is by no means certain that the small size difference found between the age groups of most species would have significant effects on heat loss. It is more likely that age differences in migration distances could result from other pressures, such as dominance status or experience, which would allow adults to survive nearer to their breeding areas and cause juveniles to migrate further. The arrival time hypothesis, in the present context, applies only to species which defer breeding until beyond their first year: it proposes that reproductively active (adult) birds benefit from wintering closer to the breeding grounds, as this could facilitate an earlier return and increase breeding output, while this benefit is not relevant in immatures not yet of breeding age. Juveniles do not invariably migrate further than adults. Among Common Chaffinches and Bramblings (Fringilla montifringilla) that were ringed on autumn migration on the southern Baltic coast, adults were recovered at significantly greater distances than juveniles (Payevsky, 1998). The same was true of Fieldfares (Turdus pilaris) in Europe (Milwright, 1994), and of the males of various small seed-eaters in North America, including the Dark-eyed Junco, White-crowned Sparrow (Zonotrichia leucophrys) and American Goldfinch (Spinus tristis) (Ketterson & Nolan, 1982, 1983; King et al., 1965; Morton, 1984; Prescott & Middleton, 1990). In Dark-eyed Juncos, the most abundant classes from highest to lowest latitudes were juvenile males, adult males, juvenile females and adult females (Ketterson & Nolan, 1982, 1983).

Competition and migration distances Competition over food or other resources can have differing effects on the sex and age groups within a population (the dominance hypothesis; Gauthreaux, 1978, 1982b). For example among Eurasian Blue Tits (Cyanistes caeruleus) in a

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breeding area in Sweden, the proportion of migrants increased from adult males (virtually none), through adult females, juvenile males and juvenile females ( . 40%). In addition, more late-hatched juvenile males than early-hatched juvenile males migrated (Smith & Nilsson, 1987). These proportions were correlated with the sizes and dominance relations within the population, with adult males the most dominant and late-hatched juvenile females the least. Such migratory patterns are frequent among passerines, raptors, gulls and other seabirds (Gauthreaux, 1982a; Dolbeer, 1991; Kjelle´n, 1994; Catry et al., 2004; Bregnballe et al., 1997), although the dominance relationships which supposedly produce them are often assumed (as a correlate of body size), rather than measured directly. In partial migrants, the commonest pattern is for juveniles to migrate in greater proportion, to leave earlier and return later, and to winter further from the breeding areas than adults. Moreover, in several species, late-fledged young migrate further than earlier ones and may return later to breeding areas the following spring (Jakober & Stauber, 1983; Bairlein, 2001). The implication that the same individuals may move further in their first than subsequent years has been confirmed in some species by ring recoveries (Newton, 1972; Schwabl, 1983). The role of competition in influencing migration distances was nicely illustrated by Grey Plovers on the Tees Estuary in northeast England (Townshend, 1985). Some newly arrived juveniles established territories there only to be soon displaced by larger juveniles, or after a few weeks by later arriving adults. Two of the displaced juveniles (which had been colour-marked) were subsequently seen on another estuary 900 km to the south. Because migration is costly in terms of energy needs and mortality risks, birds can be expected to minimize the distances moved, and settle in the first suitable site they reach within the wintering range (Greenberg, 1980; Gauthreaux, 1982b; Pienkowski & Evans, 1985). Pressure from other birds may push them further along the route so that subordinate individuals are likely to move furthest. If body size dominance relationships are important in differential migration, species with a greater degree of sexual size dimorphism should show a bigger sex difference in migration distances than species with little sexual size dimorphism. The winter distributions of two highly dimorphic icterid species (the Common Grackle (Quiscalus quiscula) and Red-winged Blackbird (Agelaius phoeniceus)) fit this prediction, whereas the sexes of the monomorphic Common Starling (Sturnus vulgaris) show no difference in winter distributions (as shown by ring recoveries of birds from the same breeding areas; Dolbeer, 1982). However, female Brown-headed Cowbirds (Molothus ater) migrated the same average distance as males, even though they are considerably smaller. In addition, in some raptors in which females are bigger than males, males migrate further. The difference is extreme among Peregrines (Falco peregrinus) that breed in Greenland, where nearly 400 ringed in nesting areas gave 125 winter recoveries in the Americas. All females were found between 28 N and 2 S and all males between 2 S and 26 S. On average, males were found 4000 km further south than females, and their migrations often exceeded 25,000 km annually (Lyngs, 2003). Despite their longer migrations, males arrived back on nesting places no later than females. Other raptors in which males migrate further than females, on average, include the Northern Goshawk (Accipiter gentilis) (Mueller et al., 1977), Hen Harrier (Circus cyaneus) (Wernham et al., 2002), Western Marsh Harrier (Circus aeruginosus) (Panuccio et al., 2013) and Rough-legged Buzzard (Buteo lagopus) (Kjelle´n, 1994). The findings on these raptors are thus consistent with both the dominance and winter cold tolerance hypotheses, but not with the hypothesis that males winter near breeding areas to get back quickly in spring. But in other raptors the opposite occurs, with females in Common Kestrels (Falco tinnunculus), American Kestrels (Falco sparverius), Saker Falcons (Falco cherrug) and Ospreys moving further than males, especially the juveniles (Village, 1990; Kjelle´n, 1994; Arnold, 1991; Prommer et al., 2012; Martell et al., 2001; Bai & Schmidt, 2012). So again any relationship between body size/dominance and migration distance is not clear-cut or consistent, even among closely related species. As well as latitudinal gradients in sex and age ratios, some species show altitudinal gradients. For example among Snow Buntings (Plectrophenax nivalis) wintering in Britain, the proportion of males decreased from mountain to coastal sites (as well as from north to south), both trends reflecting the tendency of males to winter nearest the breeding areas, and for females to occur in climatically milder places (Smith et al., 1993). In Dark-eyed Juncos of the race (Junco hyemalis carolinensis), females moved further downslope than males from their ridge-top nesting areas, a tendency more marked in severe winters than mild ones (Rabenold & Rabenold, 1985). Likewise, among Willow Grouse (Lagopus lagopus) and Rock Ptarmigan (Lagopus muta) on Alaskan mountains, most males remained in winter on the alpine tundra where they breed, while most females moved downslope into the forest zone (Weeden, 1964). These findings were again consistent with the hypothesis that dominance in competition for food or feeding places affects winter distribution patterns. The Blue Grouse (Dendrogapus obscurus) is unusual in that both sexes often move upslope for the winter, vacating fairly open breeding areas for dense forest, where they eat conifer needles (Cade & Hoffman, 1993). However, the males moved furthest, and as in other montane species, they wintered at higher elevations than the females.

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No age-related differences in wintering latitude were apparent from ring recoveries of the Evening Grosbeak (Hesperiphona vespertina) (Prescott, 1991), Cedar Waxwing (Bombicilla cedrorum) (Brugger et al., 1994), Barn Swallow (Hirundo rustica) (Wernham et al., 2002), Osprey (Poole & Agler, 1987), Mallard (Anas platyrhynchos) (Nichols & Hines, 1987), Pacific Black Duck (Anas superciliosa) (Diefenbach et al., 1988) and American Woodcock (Scolopax minor) (Diefenbach et al., 1990). In fact, age-related differences in migration distances and winter distributions do not appear to be nearly as frequent as gender-based differences. Whether this is because age-related differences are smaller, and therefore harder to detect, or because they are genuinely less frequent, remains to be seen. While dominance relationships appear to be general in bird populations, they are likely to result in differential survival and migration chiefly in competitive situations, where resources are limited. In fights over food, dominants usually win over subordinates, and in the same area dominants may survive the winter in greater proportions (Kikkawa, 1980). Among Mallards in much of northern Europe, males predominate in wintering populations, but in areas where birds were artificially fed, the sex ratio was more equal (Nilsson, 1976). Among non-migratory Song Sparrows (Melospiza melodia), the survival rate of subordinates in the presence of dominants was increased when food supplies were experimentally supplemented (Smith et al., 1980). Among European Robins, apparent overwinter survival was greater among individuals that remained near their breeding areas than among those from the same locality that migrated to distant wintering areas (Adriaensen & Dhondt, 1990). The assumptions of the dominance hypothesis thus gain some support from field studies conducted for other reasons.

MIGRATION AND DEFERRED BREEDING In some long-lived birds which do not breed until they are several years old, differences in wintering areas are apparent between age groups, as individuals winter progressively closer to breeding areas as they age, or spend shorter periods in the furthest areas. This pattern is shown for Herring Gulls in Figure 18.7, based on ring returns from breeding colonies around the Great Lakes in North America (Moore, 1976). Similar patterns have been noted in other gulls (Spear, 1988; Marques et al., 2010). The difference between age groups in date of return to breeding areas is greatest in those (mostly large) species that do not breed until they are several years old. In such species, the immatures are under less pressure to return early to the breeding areas in spring, and in some, the young migrate much later than the adults and take longer over the journey. Among various eagle species that pass through Israel each spring, the age groups migrate in order of oldest first to youngest last, but there is considerable overlap between them (Shirihai et al., 2000). The youngest age groups of some eagles and vultures return to breeding areas up to several weeks later than adults, and too late for them to attempt 100

Percent of total recoveries

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Juvenile 1 year old 2 year old Adult

70 60 50 40 30 20 10 0 Nov Dec Jan Feb Mar Apr May Jun Jul

1600 1500 1400 1300 1200 1100 1000 900 800 700 600 500 400 300 200 100 0

Juvenile 1 year old 2 year old Adult

Nov

Dec

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FIGURE 18.7 The seasonal distribution of Herring Gulls (Larus argentatus) breeding on the Great Lakes region of North America. (a) Monthly proportion of rings recoveries from each age class south of the Great Lakes region. (b) Mean monthly distance of ring recoveries from each age class. In November, when the weather was mild, all age classes were recovered near the breeding areas. But as winter progressed, the age classes became increasingly separated, with the youngest birds moving furthest south. Then, as conditions improved again from March, all age classes moved northwards towards the breeding places, where most of the population spent the summer. Nevertheless, some first- and second-year birds remained well south of the nesting areas during the breeding season. Data based on 6949 recoveries of juveniles, 1900 of 1-year-olds, 879 of 2-year-olds, and 2956 of older birds (adults) were obtained during 1929 71 from birds ringed at colonies mainly within 44 46 N. Year classes separated at 31 May each year, the approximate date of peak hatch. From Moore (1976).

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breeding that year. Radio-tracking revealed that immature Lesser Spotted Eagles (Clanga pomarina) and Steppe Eagles (Aquila nipalensis) migrate more slowly and later in spring, and arrive in breeding areas up to 10 weeks later than adults (Meyburg et al., 1995, 2001; Meyburg & Meyburg, 1999). As they make no attempt to nest, the immatures suffer no obvious penalty by arriving late. The same held for Steller’s Sea Eagles (Haliaeetus pelagicus), some juveniles of which migrated shorter distances than adults and spent the summer in areas well south of their natal areas (Ueta et al., 2000; McGrady et al., 2003). Later spring journeys and earlier autumn ones, and over-summering in places south of the breeding areas were also recorded in immature Black Kites (Milvus migrans), compared with breeding adults (Sergio et al., 2017; Ovˇciarikova´ et al., 2020). In three species studied in Japan by satellite tracking, namely Steller’s Eagle, Black-faced Spoonbill (Platalea minor) and White-naped Crane (Antigone vipio), the immatures on spring migration stayed, on average, about twice as long on stopover sites, and took about twice as long over the whole journey as adults. In this study, the two age groups showed no difference in the mean distances between stopover sites or in the overall distance travelled (Ueta & Higuchi, 2002). The longer stopovers of immatures may have reflected a lack of urgency in reaching breeding areas, as well as a lower feeding efficiency and rate of fuel accumulation. Unlike breeding adults, immatures are not tied to nesting sites, so are free to move around in summer and explore larger areas. As an extreme example, among Bearded Vultures (Gypaetus barbatus) in the Annapurna Himalayan range (Nepal), territorial adults showed annual home ranges averaging about 150 km2, whereas immatures wandered over vast ranges averaging nearly 24,000 km2, about 160 times larger (Subedi et al., 2020). Similar, but less extreme, differences between immatures and adults have been noted in several other large raptors, in addition to cranes, seabirds and others.

OVER-SUMMERING IN ‘WINTERING’ AREAS In some long-distance migrants, non-breeding individuals can be seen in ‘winter quarters’ in every month of the year. These are mostly young individuals that do not breed until they are 2 or more years old. They stay in their wintering areas beyond their first winter, returning to the breeding area in a later year (deferred return). In this way, the age groups are separated geographically in the breeding season, thereby reducing competition between them, and the young birds avoid the costs and risks of an unnecessary return journey. Alternatively, the immatures may migrate only part way from their wintering areas, passing the summer at sites on route to the breeding area, sometimes getting nearer year by year, as described above (graded return). Once sexual maturity is attained, these birds make a full return migration and usually settle to breed close to where they were hatched (Chapter 19). From then on, they normally show the usual twice-yearly migrations. Over-summering in ‘winter’ quarters is regular in at least 15 families of birds, being best known among raptors, shorebirds and seabirds. Within these groups, it is most prevalent in the longer-lived species in which individuals do not normally breed until they are several years old. Through ringing and tracking studies, over-summering in ‘wintering areas’ has been confirmed in first-year and some older immatures of various raptors that breed in Europe and winter in Africa. They include the Osprey, Egyptian Vulture (Neophron percnopterus), European Honey Buzzard, Short-toed Snake Eagle (Circaetus gallicus), Black Kite, and some Western Marsh Harriers and some Montagu’s Harriers (Circus pygargus) (Saurola, 1994; Sergio et al., 2017; Howes et al., 2020; Mellone et al., 2011; Ovˇciarikova´ et al., 2020; Panuccio et al. 2021). In most of these species, even occasional adults can be seen in Africa during the northern breeding season (the local wet season). This holds even for small species, such as the Common Kestrel, in which individuals usually return and breed in their first year (Thiollay, 1989). There is also a northward shift within Africa of these ‘summering’ birds, with many more individuals in the Sahel and Sudan zones in the summer wet season than in the winter dry season (tantamount to a part-way return). Similarly, most Black-crowned Night Herons (Nycticorax nycticorax) migrate from Europe to winter in the Sudan Sahel zones of Africa, where a high proportion of immatures remain during their first 2 3 years (Brosselin, 1974). Among seabirds that perform long migrations, the younger age classes often remain in ‘winter quarters’ for the summer or at least in sea areas separate from those used by the breeding adults. As they get older, these non-breeding immatures migrate progressively nearer to breeding areas (as found, e.g., in Fulmars (Fulmarus glacialis) and Northern Gannets, as well as in the Herring Gulls in Figure 18.7). As the years pass, increasing proportions begin to return to nesting colonies during summer, ‘prospecting’ for nest sites, but usually arriving later in spring and departing earlier in summer than breeding adults. For example, at a colony of Common Terns nesting in Germany, fledglings were marked with transponders, allowing their subsequent return to be registered automatically. Most individuals returned to the colony for the first time as 2-year-olds and remained as ‘prospectors’ for a year or more before starting to breed. Prospectors arrived later than breeders (too late to breed), and first-time breeders arrived, on average, 17 days later than experienced breeders

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(laying, on average, 19 days later). The arrival dates of older Common Terns got progressively earlier with increasing age and experience, but on average, males arrived earlier than females (Dittman & Becker, 2003). In the longer-lived Wandering Albatross, the variability was even greater, as recruitment to the breeding population took 2 8 years after first return to the natal colony (Pickering, 1989). In successive seasons, from first return to pairing, the date of arrival became earlier, and the number of days spent ashore and interacting with other individuals increased (Figure 18.8). Birds that paired arrived earlier and spent more time ashore than birds with similar experience which did not pair that year. In the season following pairing, birds returned at the same time as breeders, but most did not produce eggs. They left in mid-season and bred the following year. In this and other seabird species, the successive arrivals of established breeders, new breeders and then prospectors can be spread over periods of weeks or months each year, as can their subsequent departure. Similar patterns of (1) pre-breeding birds over-summering in ‘wintering’ areas, (2) returning part way towards breeding areas, or (3) returning to breeding areas for a shorter time than nesting adults, occur in some shorebirds, mainly in larger species and in those that migrate the longest distances to winter in the southern hemisphere. Among 20 Asian wader species wintering in Australia, the usual age of first northward migration based on ring recoveries was assessed as 1 year in 13 species, 1 2 years in four species, 2 3 years in two species, 3 years in two species, 3 4 years one species, and 4 years in five species (Rogers et al., 2006). The latter included the Far Eastern Curlew (Numenius madagascariensis), Eurasian Whimbrel (Numenius phaeopus), Bar-tailed Godwit (Limosa lapponica), Red Knot (Calidris canutus) and Great Knot (Calidris tenuirostris). However, species inhabiting freshwater or other inland habitats generally returned at a younger age than species restricted to coastal habitats, perhaps because the freshwater species had more potential re-fuelling areas on the route. Variations occur within species, with those birds migrating the longest distances tending not to return to breeding areas in their first year (Summers et al., 1995; Hockey et al., 1998). In the Western Sandpiper (Calidris maura), most juveniles wintering in California and western Mexico moult into breeding plumage gain fat and migrate north in their first spring. In contrast, nearly all juveniles wintering further south in Panama do not moult, gain fat or migrate north, but instead spend their first summer in predominantly winter plumage in their non-breeding areas (Nebel et al., 2002; O’Hara et al., 2005; Tavera et al., 2020). The difference between these sites was assumed to reflect a latitudinal trend within Western Sandpipers, with the birds showing an increasing propensity to over-summer the further from the breeding areas they spent the winter. Over-summering young waders can certainly achieve high survival rates. For example

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FIGURE 18.8 Attendance patterns of Wandering Albatrosses (Diomedia exulans) at a nesting colony in relation to experience, South Georgia Island. Each horizontal bar spans the median arrival to median departure dates of males and females. In successive seasons after first arrival, the date of arrival became earlier (F6,371 5 43.0, P , .001) and the number of days spent ashore increased (F3,371 5 63.3, P , .001). Redrawn from Pickering (1989).

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among Bristle-thighed Curlews (Numenius tahitiensis) that migrate from Alaska to the Hawaiian Islands, the average annual survival of birds after their first arrival in Hawaii exceeded 91% for the first year, 93% for the second year and 97% for the third year, compared with 85% in older migrating adults (Marks & Redmond, 1996). Clearly, the younger age classes suffered no survival penalty from staying in ‘wintering’ areas year-round and may have benefited. Almost certainly, deferred return to breeding areas is in many species an inherent trait, evolved because young birds have little or no chance of breeding successfully and benefit from avoiding the risks of a long return journey to breeding areas. It does not exclude the possibility that some birds are unable to return because, for one reason or another, they cannot accumulate the body reserves needed to make the journey. These explanations are not mutually exclusive, and even under genetic influence, there is clearly great flexibility in the age of first return.

OTHER DIFFERENCES BETWEEN AGE GROUPS Age groups may differ in other aspects of migration. Juveniles often take longer to accumulate migratory fuel than adults, migrate with lower fuel loads, stay longer at stopover sites, and take longer to complete their journeys (Chapters 14, 30). Such differences have been attributed partly to the lower experience and social status of juveniles, compared with adults. When they leave their breeding areas, juveniles also show more spread in departure directions than adults (Chapter 12), and the two age groups sometimes migrate along partly different routes, with juvenile passerines and others more likely to fly round water bodies than to cross them (Crysler et al., 2016), more likely to be drifted off course by crosswinds, and more likely to become concentrated in coastal areas (e.g., Murray, 1966; Ralph, 1971; Woodrey, 2000). In a study by radar, wind drift was less pronounced in spring than in autumn when migrants included a large number of naı¨ve juveniles migrating for the first time (Ba¨ckman & Alerstam, 2003). This further suggests that experience helps birds improve the degree to which they compensate for the effects of crosswinds. When the effects of drift and compensation were removed by considering only situations with low wind speeds, headings during spring tended to become more concentrated than in autumn, suggesting a more accurate orientation of the birds during spring, either because birds improved between seasons or because some poor performing birds, present in autumn, had not survived to spring. Other aspects of migratory performance which differ between juveniles and adults, largely through improvements in the performance of individuals, are described in Box 18.1. BOX 18.1 Age-related improvements in migratory performance. The biggest changes in migratory performance occur between the first and subsequent journeys of individual birds. These changes result from learning from personal experience (Wynn et al., 2020) or from following the example of other (older) individuals (social learning, Mueller et al., 2013). Evidence has come mainly from the tracking on migration of the same individuals in successive years, with examples from cranes (Mueller et al., 2013), pelagic seabirds (Pe´ron & Gre´millet, 2013; Campioni et al., 2020) and raptors (Sergio et al., 2014), and from comparisons between the migration tracks of birds of different age groups (with examples also from passerines). Examples of social learning derive from birds that travel in flocks, including soaring species that come together in the same thermals (Rotics et al., 2016; Panuccio et al., 2012). Improvements to migratory performance recorded in one or more species include: (1) earlier departure from wintering areas and arrival in breeding areas (shown to benefit subsequent breeding success), (2) straighter and less sinuous migration routes with fewer deviations (giving faster, more energy-efficient journeys), (3) reduced susceptibility to adverse weather, (4) taking detours to give longer but safer routes, (5) longer (faster) distances travelled per day, (6) fewer and shorter stopovers (again reducing journey times), (7) better use of tailwinds and less drift under crosswinds, (8) higher climb efficiency, improved soaring/flapping flight ratios and faster migration speeds in soaring species, all leading to (9) shorter, less energydemanding journeys and earlier arrival in good condition in breeding or wintering areas, with less spread in migration dates.1 Such changes occur not just between the first and second years of life, as recorded in a range of species, but can continue over several years of life at least up to the seventh year in Black Kites (Milvus migrans) (Sergio et al., 2014). These trends have been recorded in the same individuals tracked at successive ages, but in Black Kites some additional improvement in the average performance of age groups was due to the selective mortality during their early lives of individuals that made mistakes or performed poorly in others ways (Sergio et al., 2014). In contrast, juvenile Black-tailed Godwits (Limosa limosa) that strayed off the normal route were not more likely to die than those that took the normal route, implying that in these species improvements with age occurred entirely through learning (Verhoeven et al., 2021). Nevertheless, in several species, including Egyptian Vulture (Neophron percnopterus) and Black-tailed Godwit (Limosa limosa), juveniles tracked on their first outward migration suffered greater mortality than on their return migration or than adults on either journey (Oppel et al., 2015; (Continued )

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BOX 18.1 (Continued) Verhoeven et al., 2021). Among Manx Shearwaters (Puffinus puffinus) in the breeding season, adults also had greater feeding efficiency than younger birds, gaining more weight per unit time foraging (Fayet et al., 2015). This is another difference that could affect migration. In long-lived species, then, the development of an efficient migratory strategy is evidently a prolonged, complex and dynamic process, built partly on experience. Learning can evidently begin from an early age, at least in Great Frigatebirds (Fregeta minor), in which the young learned to correct for wind drift during their first few weeks of flight (Wynn et al., 2020). 1. Examples of species showing one or more of these changes include European Nightjar (Caprimulgus europaeus) (juveniles vs adults, Evens et al., 2017), Cory’s Shearwater (Calonectris borealis) (several age groups, Campioni et al., 2020), Scopoli’s Shearwater (Calonectris diomedea) (juveniles vs adults, Pe´ron & Gre´millet, 2013), Streaked Shearwater (Calonectris leucomelas) (juveniles vs adults, Yoda et al., 2017), Wandering Albatross (Diomedia exulans) (juveniles vs adults, Weimerskirch et al., 2006), Great Frigatebird (Fregeta minor) (juveniles vs adults, Wynn et al., 2020), Eleonora’s Falcon (Falco eleonorae) (juveniles vs adults, Mellone et al., 2013), Griffon Vulture (Gyps fulvus) (juveniles vs adults, Harel et al., 2016), Black Kite (Milvus migrans) (improvements up to 7 years, Sergio et al., 2014), Red Kites (Milvus milvus) (immatures vs adults, Garcı´a-Macı´a et al., 2021), Osprey (Pandion haliaetus) and European Honey-buzzard (Pernis apivorus) (juveniles vs adults, Thorup et al., 2003a,b), Egyptian Vulture (Neophron percnoperus) (juveniles, immatures, adults, Oppel et al., 2021), White Stork (Ciconia ciconia) (juveniles vs adults, Rotics et al., 2016), Whooping Crane (Grus americana) (improvements up to 7 years, Mueller et al., 2013), Black-tailed Godwit (Limosa limosa) (juveniles vs adults, Verhoeven et al., 2021), various passerines (juveniles vs adults, Ellegren, 1993), Savannah Sparrow (Passerculus sandwichensis) (juveniles vs adults, Mitchell et al., 2015). For other differences between juvenile and adult behaviour, see Chapter 13; Crysler et al., 2016; A˚kesson et al., 2021.

An extreme difference in migration routes between adults and juveniles occurs in Sharp-tailed Sandpipers (Calidris acuminata) which breed on the east Siberian tundra (Handel & Gill, 2010; Lindstro¨m et al., 2011). Most adults migrate directly to Australia along a coastal route through eastern Asia, stopping periodically to refuel. In contrast, the juveniles first take a long eastward detour, accrue large fat stores in southwestern Alaska, and then take a trans-Pacific flight to Australia. The reason for the difference is unknown, but it may be because conditions favour different routes at different times of year, with juveniles migrating a month later than adults. Staging in Alaska enables the juveniles to rapidly accumulate large fuel reserves with little risk of predation. Among soaring birds, some big differences in the migration routes of adults and juveniles have emerged from tracking studies in which the adults learn to avoid crossing risky barriers and instead take more roundabout but safer routes. In Honey Buzzards, for example juveniles on their first flight from Sweden take a direct route south over the Mediterranean at its widest parts, whereas adults from the same breeding area take a detour to cross the sea at Gibraltar, the shortest possible sea-crossing (Schmid, 2000; Ha˚ke et al., 2003). Similarly, in Streaked Shearwaters (Calonectris leucomelas) migrating from on the north of Honshu Island (Japan), the adults travelled round the island, remaining overwater throughout, while the inexperienced juveniles headed directly south over the island with its mountains (Yoda et al., 2017). In both these species, while the juveniles followed a straight (presumably innate) compass course southward, the experienced adults had learned to take the longer but safer route. The same holds for Ospreys in eastern North America, where the juveniles take a straight route over the western Atlantic, while the adults take the longer route down the coast (Horton et al., 2014).

CONCLUDING REMARKS Overall, sex and age differences in the timing and distances of migration in birds are associated with mating and parental systems, annual cycle features and body size/dominance relationships within populations. All these influences may modify the timing and distance of migration within the constraints imposed by environmental conditions. Where closely related species in the same taxonomic family differ in mating and parental systems, they also show corresponding differences in migration behaviour. The occurrence of similar patterns in unrelated families emphasizes the role of mating and parental systems in influencing migration timing. In both spring and autumn, sex differences in average migration dates vary from a matter of days in some species to weeks in others, depending on the relative roles of the sexes in breeding. Age differences in timing are also frequent, with younger birds generally arriving later in spring than older adults of the same sex, and juveniles leaving in autumn before adults in most species that moult locally, and after adults in most species that migrate before moulting. In many species, females migrate further than males, on average, and juveniles migrate further than adults, giving geographical gradients in sex and age ratios across the wintering range. Exceptions occur to all these general patterns, presumably depending on the ecological circumstances of the species concerned.

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Various hypotheses have been proposed to explain differences in the timing and distances of migration in the different sex and age groups of a population. None of these explanations has yet proved universally applicable across species. Different hypotheses could apply to different species, and in any given species, each aspect of behaviour can be explained by more than one hypothesis. Nevertheless, sex differences in spring migration dates seem generally related to mating opportunities and sexual selection, resulting from male male competition and female choice. In most bird species, adult males are the largest individuals and are therefore socially dominant over females and juveniles. Unless birds arrive in breeding areas already paired, males arrive in breeding areas before females, on average, but many of the same species show no obvious sex differences in autumn migration dates. The relevance of early arrival to mating opportunities is also shown by the earlier arrival of females in species (mainly some waders) in which females are larger than males and take the pre-eminant role in territorial and reproductive behaviour. On the dominance hypothesis, as usually interpreted, dominance acts here and now to influence bird behaviour, depending on conditions at the time. In many partial migrants, dominance relationships supposedly lead subordinates to migrate in the greatest proportion and over greater distances: females further than males and juveniles further than adults. In obligate migrants in which all individuals migrate every year, dominance effects on migration are much less apparent. Travel itself may have costs which increase with the length of journey, thus leading to selection for shorter movements; and if these travel costs are greater in young than older birds, selection could in turn result in young birds performing shorter journeys than older ones (as in Dark-eyed Juncos and some other seed-eaters, see above). With genetic factors (rather than prevailing conditions) having the major influence on migration distances, each sex/age class would be expected to winter each year in whichever regions offered in the long term the best prospects for survival and future reproduction, rather than where they were pushed by local competition. It is unlikely that the optimal wintering area, resulting from the balance of these various selective forces, would coincide exactly for each sex/age class of a species, considering their differences in morphology, behaviour and reproductive roles. Understanding differential migration then becomes an ‘optimality’ problem to be solved separately for each sex and age class. There is clearly scope here for further research. Dominance and other factors could thus influence movements through direct effects on individuals at the time of migration, or through evolution, by providing a consistent selection pressure on one sex to migrate earlier or further, or to occupy a different type of habitat from the other, so that such features become innate and under genetic influence. Hence, differential migration could result from either mechanistic (proximate) or evolutionary (ultimate) causes, or both. One could be a precursor to the other. Research on captive birds has provided evidence for genetic control of sex differences in some aspects of migration behaviour in at least two species, namely the Dark-eyed Junco and Eurasian Blackcap, an aspect developed in Chapter 22.

SUMMARY In many bird species, sex and age differences occur in the proportions of individuals that migrate, in the timing of outward and return movements, and in the distances travelled, leading to geographical gradients in sex and age ratios in the non-breeding season. Among passerines, short-distance partial migrants migrate after moulting in breeding areas. Typically, females migrate in greater proportion, depart earlier, travel further from their nesting areas, and return later than males; and juveniles migrate in greater proportion, depart earlier, and return later than adults. Many species of obligate long-distance migrants leave after breeding and suspend or delay moult until they reach a staging area or winter quarters. Typically, in such species, males leave the breeding area before females, and adults before juveniles. Sex and age differences in migratory timing can be explained partly in terms of dominance and competition within populations, duration and extent of moult, and perhaps also by other (as yet unknown) factors. Sex differences in migration timing, which are found in a wide range of birds, are also linked with the different roles of the sexes in breeding and with the associated position of moult in the annual cycle. Many exceptions to these general patterns are linked with the particular life history characteristics and circumstances of the populations concerned. Thus in species in which only one partner looks after the young, the other leaves breeding areas earlier (males in ducks, males in some shorebirds and females in others). Typically, in these wader species, adults leave breeding areas earlier than young of the year. In most bird species, males arrive in breeding areas, on average, earlier than females, the difference varying between species from a few days to a few weeks. The reverse sequence holds in species in which females rather than males compete for territories and mates. Within each sex, young birds arrive later than older ones, on average. Sex and age differences in migration distances may result from current competition or past conditions and their effects on genetic control mechanisms.

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In migratory species in which individuals do not breed until they are 2 or more years old, the immatures typically spend 1 or more years in their ‘wintering areas’, saving the costs and risks of apparently unnecessary journeys, or they migrate only part way towards the breeding areas. They also migrate later in spring than older birds and depart earlier in autumn, staying in breeding areas only for short periods, their timing getting closer to that of adult breeders with increasing age. Such behaviour is common in large waders, raptors, herons, storks, seabirds and others which do not normally breed in their first year of life.

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Sex and age differences in migration Chapter | 18

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Chapter 19

Dispersal and site fidelity

Ruddy Turnstone (Arenaria interpres) with identifying colour rings There is probably no single aspect of the entire subject of bird migration that challenges our admiration for birds so much as the unerring certainty with which they cover thousands of miles of land and water to come to rest in exactly the same spot where they spent the previous summer or winter. Lincoln (1935)

In many bird species, as revealed by ring recoveries, individuals tend to breed in the same general area where they were raised; and thereafter they often use these same territories or even the same nest sites in successive years. This holds more for one sex than the other but is true of both territorial and colonial species. Moreover, individuals of some species also winter in the same localities in successive years and may also use the same refuelling sites on migration, while some waterfowl use the same moulting sites. Such site fidelity is apparent in both resident and migratory populations, but in migrants it implies the existence of precise navigational skills and homing behaviour, through which individuals seek out, year after year, the same specific places hundreds or thousands of kilometres apart. Birds that occur in the same places in successive years are said to show site fidelity, while those that move from one place to another are said to disperse. Both site fidelity and dispersal are concerned with the distances which separate different places of residence in the same individual. Other terms in frequent use include ‘homing’ the tendency to return to a previously occupied site, wherever it may lie and philopatry which signifies continued residence in the area of birth, or return there in later life. In studies of dispersal and site fidelity, it is useful to distinguish for individuals: (1) natal dispersal, measured by the distances between natal and first breeding sites; (2) breeding dispersal, measured by the distances between the breeding sites of successive years; and (3) non-breeding dispersal, measured by the distances between the wintering sites of successive years. These dispersal distances are of interest because they influence the persistence and dynamics of local populations, the genetic structure of populations, and the potential for colonization and range expansion The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00001-4 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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(Newton, 2003). There is also post-fledging dispersal, a term used for the initial movements of young birds away from their natal sites on becoming independent of parental care, and the fidelity that some species show to migration routes and stopover sites. And then there is dispersive migration in which birds spread out after breeding and return for the next breeding season. This chapter is concerned with all these various aspects of bird behaviour and the environmental factors that influence them. Site fidelity and dispersal have been studied primarily with the help of ringing. Most studies have been made by observers working in defined areas, ringing nestlings or adults in one year and noting where they are found in a later year in the same area. Such records are invariably biased in favour of short-distance moves because, being confined to the study area, they are not balanced by the longer moves of any individuals which settled outside the area and remained undetected. Some study areas are so small compared with the natal dispersal distances of the birds themselves that only a tiny proportion of ringed chicks is found breeding there in later years, the majority of survivors having settled elsewhere. In general, for each species, the larger the study area (up to a point), the greater the proportion of locally raised young are later found breeding within its boundaries (see Sokolov, 1997 for European Pied Flycatcher (Ficedula hypoleuca)). In areas where practically every chick was ringed, any unringed individuals breeding within the area can be taken as immigrants hatched elsewhere. Despite the bias towards short-distance moves, records from particular study areas have established the facts that: (1) in most species males show greater site fidelity than females; and (2) birds generally move further between their natal and first breeding site than between the breeding sites of successive years (Newton, 2008: p. 491 94). Less biased information on dispersal distances comes from recoveries of ringed birds reported by members of the public. Even if all the birds are ringed in a particular locality, the recoveries are not confined to that locality, so can give a less biased picture of dispersal distances. Although the natal sites are known precisely for birds ringed as chicks, the assumption usually has to be made that individuals of reproductive age recovered in the breeding season were in fact nesting, or had the potential to nest, at the localities where they were reported. Collectively, such records reflect the settling patterns of individuals with respect to the ringing site, regardless of their movements in the interim, which remain unknown. In some large, long-lived species, care must also be taken to distinguish immatures, which may occur in areas partly different from the breeding adults of their population (Chapter 18). In recent decades, other unbiased information on site fidelity and dispersal distances has come from the tracking of individuals in successive years. These studies have often confirmed the repeated use of the same breeding, wintering or stopover localities, but samples are usually small.

BENEFITS AND COSTS OF SITE FIDELITY There are obvious benefits to a bird in nesting near where it was raised, and in returning there each year, providing conditions permit. One relates to local knowledge, a benefit that holds in both breeding and wintering areas, and at any sites the bird might stop on migration. Familiarity and prior ownership might also enable a bird to better defend its feeding and breeding sites against competitors. These advantages may enhance a bird’s survival and reproductive prospects. Moreover, through long-term residence over many generations, gene flow is restricted, and populations can become adapted through natural selection to the conditions prevailing in their particular region. The benefits of local experience and local adaptation, acting at the level of the individual, could thus be the main selective forces underlying natal philopatry and site fidelity in birds, wherever conditions permit. Another advantage of site-fidelity stems from the social cohesion it facilitates. Many birds pair with the same partner each year, even though they may live separate lives outside the breeding season. Partners can re-unite if they share a common breeding site (like most birds) or a common breeding and wintering site (like some sea-ducks in which partners separate after egg-laying and re-unite on wintering areas, Robertson & Cooke, 1999). In some species with longterm pair bonds, breeding success improves as pairs remain together, but declines for a time following a change of mate (Black, 1996). For these species then, site-fidelity enables partners which migrate independently to re-find one another on the nesting place and gain the associated reproductive benefits. But whether mate fidelity is a selective force behind the evolution of site fidelity or an incidental consequence of site fidelity remains an open question. Dispersal also has advantages. One is that birds can leave areas where conditions are poor or over-crowded to find somewhere better. Some birds occupy successional habitats which get less suitable over time, while others exploit patchy or ephemeral habitats or food sources, which are available in different places in different years. By moving from one good area to another, as appropriate, individuals may enhance their survival and reproductive prospects. Dispersal could also reduce the chance of closely related individuals pairing together, thereby avoiding inbreeding and its associated reductions in breeding success and offspring viability (Greenwood et al., 1978; Keller et al., 1994). The chances of

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inbreeding are further reduced if, as in many bird species, one sex settles to breed at greater distance from its natal site than the other (Greenwood & Harvey, 1982), or if birds are more likely to disperse if close relatives are present in the same group or vicinity (Pa¨rt, 1996; Wheelwright & Mauck, 1998; Cockburn et al., 2003). Conversely, individuals which mate with genetically very different individuals may produce offspring that are less well adapted to local conditions. Theoretically, an optimal balance between the contrasting risks of inbreeding and outbreeding would allow sufficient genetic mixing without disrupting local adaptations. Dispersal distances influence where this balance is drawn. But whether such genetic considerations have influenced the dispersal patterns of birds or are simply consequences of dispersal patterns resulting from other influences remains unknown. There are clearly benefits and costs to both site fidelity and dispersal, which are influenced by the ecological circumstances in which the bird lives.

NATAL DISPERSAL In many bird species, when the ring recoveries of young birds in a subsequent breeding season are plotted in relation to the hatch site, the numbers of recoveries tend to be greatest in the vicinity of the hatch site and decline progressively with increasing distance. Typically, the recoveries come from all sectors of the compass, indicating no directional preference at the population level. Such patterns, based on ring recoveries, are shown for several species in Figures 19.1 and 19.2. In each species, the density of recoveries declines rapidly in concentric circles out from the natal site. Such settling patterns are found in both migratory and sedentary species. Factors such as landscape structure, habitat and nest-site availability, territory sizes and prior occupancy by other individuals can all influence how close to its natal site an individual can settle and breed. FIGURE 19.1 Locations of Eurasian Sparrowhawks (Accipiter nisus) ringed as chicks and recovered in a later breeding season, shown in relation to natal site (centre). Recoveries came from all sectors of the compass and declined in density with increasing distance from the hatching site. Recoveries came from members of the public and were not obviously biased in favour of short-distance moves. From Newton (1979).

N

W

50 km

E

20 km

Recoveries per 1000 km2

82 km 250

120 km

200

S

150

Total recoveries = 201

100 50 0 0–10

11–20

21–30 31–40 41–50 Distance from hatch-site

51–60

61

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The Migration Ecology of Birds

50

(a) House Martin

Percentage

Percentage

40 30 20 10 0 25

125 175 225 275 Metres

75

25

0

150

250

350

450 550

650

Kilometres

(c) Lesser Kestrel

50

(b) Collared Dove

50

325

Percentage

Percentage

75

75

55 50 45 40 35 30 25 20 15 10 5 0

(d) Blue-footed Booby

% male % female

50

25

FIGURE 19.2 Natal dispersal patterns of several species ringed as chicks and recovered in a later breeding season. All species show a decline in numbers with increasing distance from the natal site, but the form of the relationship differs between species, and distances are greater in some species than in others. (a) Common House Martin (Delichon urbica) (Rheinwald, 1975); (b) Eurasian Collared Dove (Streptopelia decaocto) (Hengeveld, 1993); (c) Lesser Kestrel (Falco naumanni) (Negro et al., 1997); and (d) Blue-footed Booby (Sula nebouxii) within a colony (Osorio-Beristain & Drummond, 1993).

0 10

30

50

70

90 110

Kilometres

30

60

90

120

150

Metres

Such skewed settling patterns have been found in almost all bird species that have been studied, but with some species dispersing over much longer distances than others (Newton, 1979; Paradis et al., 1998; Wernham et al., 2002). In general, larger species tend to breed further from their natal sites than do small ones, as might be expected, but this relationship is rather loose because of the other factors that influence dispersal distances. Within species, the settling pattern may differ somewhat from year to year or from region to region, depending on local circumstances, including the density of the population and the patchiness of habitat in the region concerned (for European Pied Flycatcher, see Sokolov, 1997; for Long-tailed Tit (Aegithalos caudatus), see Russell, 1999; for Eurasian Blue Tit (Cyanistes caeruleus) and Great Tit (Parus major), see Matthysen et al., 2001). Some small forest species are reluctant to cross open land, which can therefore subdivide a population more firmly than would happen in continuous forest (for Marsh Tit (Poecile palustris), see Broughton et al., 2010). The same holds for landbirds nesting on offshore islands (Weatherhead & Forbes, 1994), and for birds requiring special nest sites, such as cliffs, whose dispersal distances are influenced by the locations of such sites. In general, natal dispersal distances also tend to be greater in migratory species than in closely related resident ones, and the same is true for migratory and resident populations of the same species. For example among Common Blackbirds (Turdus merula), natal dispersal distances increased from Denmark through Norway and Sweden to Finland, in line with increasing migratoriness of breeding populations (Main, 2002). In partial migrants, such as the Song Sparrow (Melospiza melodia), migratory individuals showed greater natal dispersal distances than resident ones in the same area (Nice, 1933). This may have been because residents were already settled on territories by the time the migrants returned, causing them to move greater distances.

Seabirds and other colonial species In colonial species, natal dispersal is influenced by the distribution of colonies, but settlement patterns are essentially the same as in other birds, with most individuals breeding in their natal or neighbouring colonies. This holds for colonial landbirds, such as Sand Martin (Riparia riparia) (Mead & Harrison, 1979) and Lesser Kestrel (Falco naumanni) (Negro et al., 1997) and for a wide range of colonial seabirds, including gulls and terns, auks, shags and sulids, petrels and others (Newton, 2008: 485, Barlow et al., 2013). In some seabirds, many individuals settle to breed in the same part of a colony where they were raised. This finding is much more frequent than expected if individuals settled at random within their natal colony. It also occurs in a wide range of species, including penguins (Williams, 1995), albatrosses (Fisher, 1971), shearwaters (Richdale, 1963), auks (Gaston et al., 1994; Halley et al., 1995), skuas (Klomp & Furness, 1992), shags (Aebischer, 1995) and others. In a

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large colony of Blue-footed Boobies (Sula nebouxii) off Mexico the median distance between natal site and subsequent breeding site was less than 30 m (Figure 19.2; Osorio-Beristain & Drummond, 1993), and in a colony of Nazca Boobies (Sula granti) on Galapagos the median dispersal distances of males and females were 26 and 105 m, respectively. As adults, both sexes retained the same sites year after year (Huyvaert & Anderson, 2004). Such findings on the philopatry of seabirds are more remarkable than the bland figures suggest. Take the Shorttailed Shearwater (Puffinus tenuirostris), for example 23 million of which breed annually in burrows and headlands around southeastern Australia, migrating to the northern Pacific for the non-breeding season (Skira, 1991). On one tiny island in Bass Straight, a population of a few hundred birds was studied for more than 50 years. Over 40% of young hatched on this island later returned there, mainly to the same part of the colony where they were hatched, and a constant 45% of the breeding population consisted of locally hatched recruits (Serventy & Curry, 1984). Such precision in the selection of a breeding location is extraordinary, considering the wide-ranging migration, the average 7-year gap between fledging and first breeding, and the fact that less than 1 km from the study site was a much larger island holding several hundred thousand nesting shearwaters. In any colony, then, breeders typically include some individuals raised within the colony and others that have moved in from elsewhere. During the establishment and growth phases of a colony, immigration is high, as expected, so that most of the occupants have been raised elsewhere, whereas during a decline phase the reverse may be true (for seabirds, see Porter & Coulson, 1987; Phillips et al., 1999; He´naux et al., 2007; for geese, see Larsson et al., 1988; Johnson, 1995). Gulls and terns that nest on unstable substrates, such as sandbanks, often have to move their breeding places as sites become washed away or flooded, accessible to mammalian predators, or infested with ticks and lice. Whole colonies can sometimes disband and re-form elsewhere, affecting the dispersal distances of both first-time and established breeders. Among southern African species, entire colony shifts were frequent in Hartlaub’s Gulls (Chroicocephalus hartlaubii), Great Crested Terns (Sterna bergii), Roseate Terns (Sterna dougallii) and Cape Cormorants (Phalacrocorax capensis) (Crawford et al., 1994). Other species in the same region occupied more stable substrates and showed strong colony persistence, as in African Penguins (Spheniscus demersus), Cape Gannets (Morus capensis), Bank Cormorants (Phalacrocorax neglectus), Great Cormorants (Phalacrocorax carbo) and Great White Pelicans (Pelecanus onocrotalus). In some cliff-nesting seabirds, generation after generation has used the same sites for centuries. In many seabird species, individuals are known to visit colonies for 1 or more years before they attempt to breed, supposedly acquiring experience and local knowledge on which to assess the relative merits of potential nesting places (Chapter 18). The number of colonies visited by individuals during this pre-breeding phase seems to vary between species. Among Great Skuas (Stercorarius skua) on Foula (Scotland), virtually all individuals seemed to visit only their natal colony in their pre-breeding years (Furness, 1987; Klomp & Furness, 1992), but in European Storm Petrels (Hydrobates pelagicus) and Atlantic Puffins (Fratercula arctica), individuals regularly visited more than one colony, sometimes hundreds of kilometres apart, before settling to breed (Mainwood, 1976; Harris, 1984).

Sex differences in natal dispersal In some bird species, both sexes show similar dispersal distances, but in many others, one sex moves further than the other, at least as a general tendency. The commonest pattern is for young females to move further between hatch site and breeding site than males, as found in many passerines, owls and raptors, gallinaceous birds, waders and colonial seabirds (Greenwood, 1980; Clarke et al., 1997; Newton, 2008). In all such species, therefore, more males than females in local populations have been raised locally. Most northern waterfowl show sex-biased dispersal, but with males moving furthest, as documented in swans, geese, shelducks, and in various diving and dabbling ducks (Mihelsons et al., 1986; Rohwer & Anderson, 1988; Clarke et al., 1997; Nilsson & Persson, 2001). In many such species, in contrast to most other birds, pairing occurs in wintering areas, and the male then accompanies the female to her natal area. Because birds from different breeding areas may share the same wintering places, the males of some species have settled to breed up to several hundred kilometres from their natal sites (Salomonsen, 1955; Cooke et al., 1995). Moreover, the males of some migratory ducks have a different mate each year, so they may change their breeding sites substantially from one year to the next. They contrast with some sea ducks, geese and swans which normally keep the same mate and breeding place for several-to-many years (Savard, 1985; Anderson et al., 1992). In some sea ducks, as mentioned above, partners separate after egg-laying and re-unite in wintering areas, as seen in marked pairs of Common Eiders (Somateria mollissima), Barrow’s Goldeneyes (Bucephala islandica) and Harlequin Ducks (Histrionicus histrionicus) (Robertson & Cooke, 1999). Other species in which males disperse further than females between natal and breeding sites include some waders that show ‘sex-role reversal’, with the female defending the territory and the male doing the incubation and chick care.

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The Migration Ecology of Birds

Examples include the Spotted Sandpiper (Actitis macularia) and various phalarope Phalaropus species (Oring & Lank, 1982; Colwell et al., 1988). Like the ducks, these species have a social system based on mate defence, but unlike many ducks, they form into pairs in the breeding area. Males also disperse further than females in some lekking species, such as Great Bustard (Otis tarda) (Alonso & Alonso, 1992). In some group-living birds, the young remain with their parents for up to several years before they disperse, mostly over short distances (for Florida Scrub Jay (Aphelocoma coerulescens), see Woolfenden & Fitzpatrick, 1978; for Acorn Woodpecker (Melanerpes formicivorus), see Ko¨enig & Mumme, 1987; for Arabian Babbler (Turdoides squamiceps), see Zahavi, 1989; for Siberian Jay (Perisoreus infaustus), see Ekman et al., 1994). Delayed dispersal has developed, it is supposed, in situations where all suitable habitat is occupied by territorial groups, leaving nowhere for unattached birds to live (for experimental evidence in Seychelles Warbler (Acrocephalus sechellensis), see Komdeur et al., 1995). The adults then gain by allowing their young to remain in the territory, with access to its resources, until an opening becomes available elsewhere. The young pay for their long-term accommodation by helping with territorial defence and (in some but not all species) by feeding subsequent broods. While they forgo reproduction themselves, they may gain some ‘inclusive fitness’ if they help to raise younger siblings. To become breeders, young males sometimes inherit the territory from their father, or take over another territory nearby, but young females almost always move to another territory, as does any breeding female whose son takes over the home territory. The dispersal of young birds from the natal territory is thereby delayed by up to several years, and inbreeding is largely prevented by females moving more often or further than males. In general in such group-living species, however, natal dispersal distances tend to be short.

Competition and natal dispersal Although a tendency to disperse from the natal site seems inherent in birds, competition may influence the distances moved, as implied by four main types of evidence. First, in some studies, the young moved further from their natal sites in years of high than low population density (Greenwood et al., 1979; Nilsson, 1989) or the young moved further in successive years as a local population grew (Wyllie & Newton, 1991; Negro et al., 1997). Second, in other studies the young moved further from their natal sites in years of low food supply when competition is likely to have been high (Saurola, 2002; Byholm et al., 2003). Some such species depended on cyclically fluctuating vole populations, and their natal dispersal distances were longer in years when vole numbers reached their cyclic low. Third, within populations, young fledged late in the season dispersed further, on average, than young fledged earlier (Nilsson, 1989; Village, 1990; Newton & Rothery, 2000). In addition, the provision of supplementary food to non-migratory Song Sparrows greatly reduced emigration from the study area, a supposed effect of reduced competition (Arcese, 1989). And in an experimental study of Great Tits, when 90% of the first brood young had been removed, young from late broods settled much nearer to their natal sites than in other years, another result attributed to reduced competition (Kluijver, 1971). These various findings, which derive from both resident and migratory populations, imply that natal dispersal distances may be density-dependent, and influenced by levels of competition, whether for territories, food or nest or roost sites. The limited size of typical study areas has probably often hampered the detection of density dependence because, as explained above, only short-distance moves are detected there. Among Peregrines (Falco peregrinus) breeding in Britain, no discernible relationship between density and dispersal distance was found in a limited study area, but when region-wide recaptures and recoveries were included in the analyses, a density-dependent relationship emerged, again suggesting that dispersal distances were increased by competition (Morton et al., 2018).

BREEDING DISPERSAL One of the earliest findings to emerge from bird-ringing, as stated above, was that, once individuals had bred in an area, they tended to stay there or return there to breed year after year. Individuals occupied the same territories in successive years or moved to other territories nearby. In many species of seabirds and raptors, individuals often returned to exactly the same nest sites. In some species, the proportions of adults returning to particular study areas each year was so high that, allowing for known mortality rates, few if any individuals could have moved elsewhere (Figure 19.3; Table 19.1). To judge from general ring recoveries, not constrained by size of study area, breeding dispersal shows a similar skewed pattern to natal dispersal, but over shorter distances (e.g., Jackson, 1994; Paradis et al., 1998; Winkler et al., 2004). Typically, within species, mean adult dispersal distances are about one-half as great as natal distances, but in some species only one-sixth as great, with the majority of adults nesting very close to where they bred the previous year (Figure 19.4).

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FIGURE 19.3 Proportions of adults in migratory bird populations that returned to the same breeding sites (upper) or wintering sites (lower) in successive years. Allowing for mortality, the species depicted reveal some of the most extreme examples of site-fidelity in birds, in which all (or almost all) surviving individuals may be inferred to have returned to the same site in successive years. Some of the species shown bred in one continent and wintered in another.

Such patterns of site fidelity are again evident in a wide range of species, including passerines, raptors, game birds, waders, waterfowl and colonial seabirds, both resident and migratory (Newton, 2008). For example in the Common House Martin (Delichon urbica) studied in some German villages, the median dispersal distance between natal and first breeding sites was found to be 75 m, whereas for breeding adults moving between nesting sites of different years, the median distance was 35 m. Some 7% of adults returned to exactly the same nests in successive years (Rheinwald & Gutscher, 1969). More detailed studies have revealed other patterns among established breeders: (1) sex differences in site fidelity, with males in most species more likely than females to stay on the same territory from year to year (Greenwood, 1980; Winkler et al., 2004), possibly related to sex differences in territory acquisition and defence; (2) a tendency for greater site-fidelity in later life (Newton, 1993; Winkler et al., 2004), possibly related to increasing benefits through life of sitefamiliarity; (3) a greater tendency to change territories after a breeding failure than after a success (Newton & Marquiss, 1982; Jime´nez-Franco et al., 2013), possibly related to site quality, (4) a tendency to move to better territories (judged by previous breeding success) through early life (Matthysen, 1990; Hilde´n, 1979), possibly related to increased status and competitive ability; and (5) a strong tendency for a change of territory to be associated with a change of mate (Handel & Gill, 2000; Newton, 2001). Where birds changed territories, females not only moved more often than males but also over longer distances. Sex differences in breeding site fidelity have been noted in more than half the species so far studied, from passerines to raptors, waders and seabirds (for other examples, see Tables 19.1 and 19.2; Newton, 2008: p. 491 94). In some species, they are pronounced. For example in the European Pied Flycatcher, 93% of surviving males returned each year to their previous nesting locality, while only 39% of surviving females did so, the rest moving elsewhere (von Haartman, 1949). In an experimental study, when most of the ringed female flycatchers in 40 ha of woodland were laying or incubating, all nest boxes were removed, including the occupied ones. The males remained in the area and continued singing, but only 1 day after box removal, not a single female could be found (Berndt & Sternberg, 1968). Of the 146 females involved, 37 were found later in the same season nesting in other woods nearby, having moved 1.4 18.3 km, some to areas where they had bred in previous years. This was about the same range of distances as female flycatchers would normally have moved between years.

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The Migration Ecology of Birds

TABLE 19.1 Annual return rates of migrant juvenile and adult birds to specific study areas in successive breeding seasons. Species

Location (size of study area)

Natal area

Breeding area

Unsexed young

Male

Female

N

%

N

%

N

%

Source

House Wren (Troglodytes aedon)

Illinois (128 ha)

6299

2.8

643

38

1468

23

Drilling & Thompson (1988)

Great Reed Warbler (Acrocephalus arundinaceous)

Sweden (200 ha)

477

9

59

54

66

57

Bensch & Hasselquist (1991)

Willow Warbler (Phylloscopus trochilus)

England (47 ha)

232

5

104

28

57

23

Lawn (1982)

Pied Flycatcher (Ficedula hypoleuca)

Russia (50 km2)

1840

9

256

28

327

15

Sokolov (2000b)

Prairie Warbler (Setophaga discolour)

Indiana (50 ha)

272

4

55

60

105

19

Nolan (1978)

American Redstart (Setophaga ruticilla)

New Brunswick ( . 150 ha)

172

5

398

36

119

21

Lemon et al. (1996)

Common Shelduck (Tadorna tadorna)

Scotland (12 km2)

422

19

186

91

183

99

Patterson (1982)

Northern Lapwing (Vanellus vanellus)

England (877 ha)

801

28

171

74

129

70

Thompson et al. (1994)

European Golden Plover (Pluvialis apricaria)

Scotland (100 ha)

100

26

77

78

35

77

Parr (1980)

Temminck’s Stint (Calidris temminckii)

Finland (?)

170

21

112

79

61

70

Hilde´n (1979)

Long-billed Curlew (Numenius americanus)

Idaho (?)

270

4

14

71

29

69

Redmond & Jenni (1982)

Semi-palmated Sandpiper (Calidris pusilla)

Manitoba (200 ha)

802

4

415

61

401

56

Sandercock & GrattoTrevor (1997)

Burrrowing Owl (Speotyto cunicularia)

Manitoba (?)

538

4

87

40

78

24

De Smet (1997)

The data are drawn from studies in which attempts were made to identify all individuals present, separating males and females. Records for different years are pooled. N 5 number marked, % 5 percentage recovered. Note the lower return rates for juveniles returning to their natal areas than for adults returning to their former breeding areas. This is due partly to higher mortality rates of juveniles which allow fewer to return, and partly to their longer dispersal distances, which lead fewer to settle in the study area, compared with returning adults. Among established breeders, in most species return rates were higher for males than for females. For other records see Newton (2008).

FIGURE 19.4 Relationship between the geometric means of the natal and breeding dispersal distances of 31 bird species, based on recoveries from the British ringing scheme. From Paradis et al. (1998).

Breeding dispersal (km)

100

10

1

0.1 0.1

1

10

Natal dispersal (km)

100

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387

TABLE 19.2 Dispersal distances of House Wrens (Troglodytes aedon) in Ohio. Distance away

% Recoveries in later years of birds ringed as Breeding males

Breeding females

Nestlings

(N 5 278)

(N 5 279)

(N 5 181)

In same nest box

31

26

2

Up to 1000 feet (0.3 km)

53

44

13

1000 2000 feet (0.3 0.6 km)

6

11

19

2000 4000 feet (0.6 1.2 km)

7

9

25

4000 7000 feet (1.2 2.1 km)

3

5

19

7000 11,000 feet (2.1 2.5 km)

3

7

2 5 miles (3 7.5 km)

1

4

5 10 miles (7.5 15 km)

.1

9

Over 10 miles ( . 15 km)

2

Source: From Kendeigh (1941).

TABLE 19.3 Within-season nest site-fidelity and mate-fidelity in the Eastern Phoebe (Sayornis phoebe) in Indiana. Males

Females

Same nest site in same territory

127

135

Different nest-site in same territory

22

28

Different nest-site in different territory

1

2

Same mate throughout season

124

115

Different mate after loss of first mate

14

6

Different mate after ‘divorce’

7

3

Site fidelity

Mate fidelity

Note that sample sizes differ between categories. Source: From Beheler et al. (2003).

Dispersal within a breeding season Many birds raise more than one brood per season or attempt a second nest if the first fails. These second attempts normally occur close to first attempts. Some birds may even use the same nest sites for repeat broods, especially some cavity nesters where sites are scarce. In most species, the same partners stay together for successive nests in a season but in some species, some individuals change territories and partners within a season, especially after nest failure, with the female often moving further than the male (e.g., Yellow-breasted Chat (Icteria virens), Thompson & Nolan, 1973; Barn Swallow (Hirundo rustica), Shields, 1984; Eastern Phoebe (Sayornis phoebe), Beheler et al., 2003; Table 19.3). In some species, it is not unusual for individuals to raise successive broods in widely separated localities within the same breeding season (Chapter 17). Examples include some cardueline finches which feed on sporadic food supplies, settling temporarily wherever food is plentiful, and moving elsewhere for the next nesting attempt that year (for Eurasian Bullfinch (Pyrrhula pyrrhula), see Newton, 2000; for Common Redpoll (Acanthis flammea) and Eurasian Siskin (Spinus spinus), see Chapter 20). Other species change location part way through a breeding season in line with changes in habitat structure (including crop growth on farmland). For example Penduline Tits (Remiz pendulinus) in central Europe often raise first and second broods in different patches of riverine and lakeside scrub, as conditions

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The Migration Ecology of Birds

change through the season, with movements generally greater than 0.5 km, and some extending up to 208 km (Franz, 1988). Yet other examples include the few species (e.g., Common Quail (Coturnix coturnix)) which habitually stop and breed at two or more points on a spring migration route (Chapter 17). In some polyandrous shorebirds, such as Eurasian Dotterel (Charadrius morinellus) and Snowy Plover (Charadrius nivosus), the females lay one clutch for the male to incubate and then leave in search of another male to raise a second clutch. In the process, as shown by ringing, the females can travel hundreds of kilometres between nesting attempts (Wernham et al., 2002; Stenzel et al., 1994).

LONG-DISTANCE NATAL AND BREEDING DISPERSAL The year-to-year homing behaviour shown by the species discussed so far is not universal in birds. It may be favoured only where habitats remain fairly stable from year to year, and where returning birds can expect to survive and reproduce. It would not be expected in species that depend on unpredictable habitats or food supplies which are available in different places in different years. This holds, for example in some ground-nesting tundra species affected by variable patterns of spring snow conditions (Tomkovich & Soloviev, 1994; Saalfeld & Lanctot, 2015), in some waders and waterbirds affected by fluctuating water levels (Johnson & Grier, 1988; Robinson & Oring, 1997), in desert species affected by irregular rainfall (Chapter 17), in some boreal finches that exploit sporadic tree-seed crops (Chapter 20), or in some predatory birds that exploit locally abundant rodents (Chapter 21). The local population densities of such species often fluctuate greatly from year to year, in line with fluctuating habitat or food supplies. The speed with which local numbers increase in response to improving conditions has encouraged the view that such species are nomadic, with individuals concentrating in different areas in different years, wherever conditions are good at the time. For some such species, ring recoveries have now confirmed that some individuals do indeed breed at hundreds or thousands of kilometres from their natal sites and in widely separated areas in different years (Chapters 20, 21). The extent and depth of prairie wetlands in North America vary greatly from year to year, according to previous rain and snowfall. Diving duck species, such as the Redhead (Aythya americana), Canvasback (Aythya valisineria) and Lesser Scaup (Aythya affinis), which occupy the deepest and most stable wetlands, show the greatest degree of sitefidelity; while dabbling species, such as the Northern Pintail (Anas acuta) and Blue-winged Teal (Spatula discors), which use the shallowest and most ephemeral wetlands, tend to settle wherever conditions are suitable at the time (Chapter 21; Johnson & Grier, 1988). This opportunist settling behaviour is reflected in long natal and breeding dispersal distances and by low return rates to particular areas, as assessed by ringing (Table 19.4). In years of extreme drought on the prairies, many Northern Pintail and other ducks continue their spring migration northward and settle to breed on the tundra. This means that many Pintails that were raised on the prairies moved much longer distances in drought years to breed further north, as again shown by ring recoveries (Figure 21.7; Smith, 1970). Dabbling ducks, and to a lesser extent some species of freshwater diving ducks, contrast with some sea ducks, which breed in more stable habitats and typically show much higher natal and breeding site fidelity (Dow & Fredga, 1983; Savard & Eadie, 1989; Cooke et al., 2000).

TABLE 19.4 Sex and age differences in the percentage return rates of waterfowl to particular study areas in successive breeding seasons. Natal dispersal Males

Breeding dispersal

Females

Males

Females

N

%

N

%

N

%

N

%

Northern Shoveller (Spatula clypeata)

134

1

116

3

19

11

20

15

Gadwall (Anas strepera)

42

2

28

7

236

9

54

41

American Wigeon (Anas americana)

6

0

3

33

11

9

21

38

Canvasback (Aythya valisineria)

206

1

101

27

52

10

75

76

Lesser Scaup (Aythya affinis)

91

4

76

49

351

9

58

66

Species arranged according to habitat preference, shallow (ephemeral) to deep (permanent) waters. Only studies with both sex and aged groups represented are shown. Source: From Johnson & Grier (1988) in which the original references may be found. For other waterfowl studies, see Rohwer & Anderson (1988).

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Wader species that nest in habitats that normally remain stable from year to year, such as Eurasian Oystercatcher (Haematopus ostralegus), Dunlin (Calidris alpina) and Common Sandpiper (Tringa hypoleucos), show strong philopatry and site fidelity, while species that nest in patchy and ephemeral habitats or are affected by variable patterns of snow-melt, such as Curlew Sandpiper (Calidris ferruginea) and Little Stint (Calidris minuta), show much less natal philopatry and less adult site fidelity (Evans & Pienkowski, 1984; Tomkovich & Soloviev, 1994). Species that show low site fidelity also show low mate fidelity, because pairing occurs annually on or near nesting areas and former partners do not normally move together to the same places. In the American Avocet (Recurvirostra americana), which favours ephemeral wetlands, individuals were found to move up to 325 km between breeding sites in different years (Robinson & Oring, 1997). Many other waterside birds, which require specific conditions for nesting, change their breeding places between years, in association with changes in water levels and vegetation, or the flooding and exposure of sandbanks where they nest. In conclusion, short dispersal distances and high site-fidelity are characteristic of bird populations whose habitats or food supplies stay reasonably stable from year to year, whereas long-distance dispersal and low site fidelity are shown by populations whose habitats or food supplies vary in distribution from year to year. Moving when conditions deteriorate is likely to improve survival and breeding success in the conditions prevailing. Because of the moves, numbers in particular localities fluctuate greatly from year to year, in line with changes in habitat or food conditions. Differences in dispersal patterns between species have led some authors to divide birds into two types: those with limited natal dispersal, and even more limited breeding dispersal (strong site-fidelity) and those with wide-ranging natal and breeding dispersal (little or no site fidelity). In practice, variation between these extremes is continuous, and the same species may lie at different points on the continuum in different parts of its range, depending on the stability of local habitats and food supplies (Chapter 20).

NONBREEDING DISPERSAL Once they have wintered in an area, individuals of many bird species return there with the same consistency as they return to their breeding localities. Studies of winter site fidelity, like breeding site fidelity, have been conducted mainly by researchers working in the same small areas year after year (Table 19.5). So again, while such records are useful in confirming site fidelity, most give little idea of the proportion of surviving birds that disperse elsewhere. However, in some species, the proportion of individuals recorded in the same places from winter to winter was close to the expected annual survival, implying that almost all surviving individuals were site faithful (examples in Figure 19.3). More generally, return to the same wintering localities has been recorded incidentally for a wide range of passerines, raptors, gulls, waders, waterfowl and others, with many examples in the ornithological literature. Other recent examples involved birds that were tracked on migration to the same wintering places in consecutive years, including the Willow Flycatcher (Empidonax traillii) (Paxton et al., 2017), Common Tern (Sterna hirundo) (Ku¨rten et al., 2022), Long-billed Curlew (Numenius americanus) (Page et al., 2014) and various raptors such as Osprey (Pandion haliaetus) (Martell et al., 2001; Va¨li & Sellis, 2015), Grey-faced Buzzard (Butastur indicus) and Crested Honey Buzzard (Pernis ptilorhynchus) (Shiu et al., 2006), Red Kite (Milvus milvus) (Garcı´a-Macı´a et al., 2021), Broad-winged Hawk (Buteo platypterus) (McCabe et al., 2020), Peregrine (Dixon et al., 2017; Sokolov et al., 2018) and Prairie Falcon (Falco mexicanus) (Steenhof et al., 2005). In contrast, Eurasian Hoopoes (Upupa epops) tracked from Europe to Africa did not return to the same wintering areas in successive years (van Wijk et al., 2016). Levels of site fidelity recorded by tracking give an unbiased picture of site fidelity, because all individuals can be followed, regardless of where they go. The fact that birds have greater freedom to move around in the non-breeding than in the breeding season influences measures of site fidelity. Some species base themselves on communal roosts, from which they range out into surrounding areas to feed. Common Starlings (Sturnus vulgaris) and Barn Swallows can range more than 50 km from their winter roosts, so records of individuals tens of kilometres apart in different winters may still represent ‘site fidelity’ in a way that breeding season records at such distances would not (Oatley, 2000). Many shorebirds are faithful to their roost sites in different years, and the median distance moved by ringed Dunlin trapped in different winters (14 km) was well within their daily travel range on large estuaries (Rehfisch et al., 1996). Nevertheless, site fidelity in winter seems to show the same pattern as in the breeding season, with ring recoveries in subsequent winters being centred on the first-recorded site and declining sharply with increasing distance. Such skewed patterns have been documented in many species, but again the distance scale varied greatly between species (Newton, 2008: p. 502). In northeast Scotland, shorebird species were ranked in order of decreasing winter site fidelity (5increasing dispersal) from Purple Sandpiper (Calidris maritima) (most site faithful), through Ruddy Turnstone (Arenaria interpres),

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TABLE 19.5 Annual return rates of migrant birds to specific study areas in successive winters. Species

Location (size of study area)

Unsexed N

%

Source

Whinchat (Saxicola rubetra)

Nigeria (?)

176

54

Blackburn & Cresswell (2015)

Siberian Blue Robin (Luscinia cyane)

Malaysia (15 ha)

156

46

Wells (1990)

Willow Flycatcher (Empidonax traillii)

Costa Rica (?)

55

71

Koronkiewicz et al. (2006)

Great Reed Warbler (Acrocephalus arundinaceus)

Malaysia, area 1 (10 ha)

62

50

Nisbet & Medway (1972)

Great Reed Warbler (Acrocephalus arundinaceus)

Malaysia, area 2 (2 ha)

83

37

Nisbet & Medway (1972)

Marsh Warbler (Acrocephalus palustris)

Zambia (7.6 ha)

17

47

Kelsey (1989)

Melodious Warbler (Hippolais polyglotta)

Ivory Coast (?)

69

6

Salewski et al. (2000)

Greenish Warbler (Phylloscopus trochiloides)

India (200 ha)

25

52

Price (1981)

Willow Warbler (Phylloscopus trochilus)

Ivory Coast (?)

110

0

Salewski et al. (2000)

European Pied Flycatcher (Ficedula hypoleuca)

Ivory Coast (?)

94

23

Salewski et al. (2000)

Prairie Warbler (Setophaga discolour)

Puerto Rico (8 ha)

25

40

Staicer (1992)

Black-throated Blue Warbler (Setophaga caerulescens)

Jamaica (?)

57

46

Holmes & Sherry (1992)

Cape May Warbler (Setophaga tigrina)

Puerto Rico (8 ha)

8

38

Staicer (1992)

Northern Parula (Setophaga americana)

Puerto Rico (8 ha)

65

49

Staicer (1992)

American Redstart (Setophaga ruticilla)

Jamaica (?)

11

51

Holmes & Sherry (1992)

Males

England (one garden)

69

48

Burgess (1982)

Females

England (one garden)

67

19

Burgess (1982)

Adults

California (8 ha)

306

30

Mewaldt (1964)

First-years

California (8 ha)

868

24

Mewaldt (1964)

Golden-crowned Sparrow (Zonotrichia atricapilla)

California (8 ha)

2456

18

Mewaldt (1964)

Blue Tit (Cyanistes caeruleus)

White-crowned Sparrow (Zonotrichia leucophrys)

Eurasian Oystercatcher (Haematopus ostralegus) 5-year-olds

England (?)

734

89

Goss-Custard et al. (1982)

2- to 4-year-olds

England (?)

475

83

Goss-Custard et al. (1982)

71

80

Evans (1981)

Grey Plover (Pluvialis squatarola)

2

England (,100 km )

Pacific Golden Plover (Pluvialis fulva) Territorial (1 2 years) Territorial (older) Non-territorial (1 2 years)

Hawaiian Islands (,10 km2)

34

90

Johnson et al. (2001)

2

78

80

Johnson et al. (2001)

2

16

82

Johnson et al. (2001)

2

Hawaiian Islands (,10 km ) Hawaiian Islands (,10 km )

Non-territorial (older)

Hawaiian Islands (,10 km )

35

67

Johnson et al. (2001)

Eurasian Curlew (Numenius arquata)

England (,100 km2)

119

82

Evans (1981)

Common Redshank (Tringa totanus)

Wales (4 km)

61

86

Burton (2000)

England (306 km )

115

84

Smith et al. (1992)

Adults

Helgoland (150 ha)

117

85

Dierschke (1998)

First-years

Helgoland (150 ha)

30

63

Dierschke (1998)

Green Sandpiper (Tringa ochropus)

2

Purple Sandpiper (Calidris maritima)

(Continued )

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TABLE 19.5 (Continued) Species

Purple Sandpiper (Calidris maritima)

Location (size of study area)

England (13 km) 2

Unsexed

Source

N

%

61

66

Burton & Evans (1997)

Sanderling (Calidris alba)

England (,100 km )

93

91

Evans (1981)

Ruddy Turnstone (Arenaria interpres)

England (13 km)

71

86

Burton & Evans (1997)

Ruddy Turnstone (Arenaria interpres)

Scotland (6 km)

42

95

Metcalfe & Furness (1985)

Males

Northeast England (?)

56

77

Coulson et al. (1984)

Females

Northeast England (?)

55

69

Coulson et al. (1984)

Canada Goose (Branta canadensis)

Minnesota (,100 ha)

271

78

Ravelling (1979)

540

76

Percival (1991)

Great Black-backed Gull (Larus marinus)

Barnacle Goose (Branta leucopsis)

2

Scotland (,10 km ) 2

a

Greater White-fronted Goose (Anser albifrons)

Scotland (,100 km )

531

85

Wilson et al. (1991)

Barnacle Goose (Branta leucopsis)

Netherlands (many areas)

576

90

Ebbinge (1991)

Texas-Louisiana (,100 km )

77

86

Prevett & MacInnes (1980)

Males

British Columbia (?)

82

77

Robertson & Cooke (1999)

Females

British Columbia (?)

66

62

Robertson & Cooke (1999)

Males

Maryland (12.5 km2)

91

26

Limpert (1980)

Females

Maryland (12.5 km2)

37

11

Limpert (1980)

Snow Goose (Anser caerulescens)

2

Harlequin Duck (Histrionicus histrionicus)

Bufflehead (Bucephala albeola)

Other examples for neotropical migrants in Rappole et al. (1983), for waterfowl in Robertson & Cooke (1999). The data are drawn from detailed studies in which attempts were made to identify all individuals present. Records for different years are pooled. N 5 number marked, % 5 percentage known to return the next winter to the same area. Sizes of study areas are given in hectares or as length of coastline. a This is the percentage of re-sightings (not total birds) that were in the same site, so is not comparable to most of the other data presented in which return rates include mortality as well as movement elsewhere.

Curlew (Numenius arquata), Common Ringed Plover (Charadrius hiaticula), Eurasian Oystercatcher, Redshank (Tringa totanus), Dunlin, Bar-tailed Godwit (Limosa lapponica) to Red Knot (Calidris canutus) (least site faithful), the differences being linked with the degree of year-to-year stability in their habitats and food supplies. Red Knots regularly moved from estuary to estuary during the course of a winter, and many visited the same several estuaries every winter. Except for the last three species, more than 94% of recaptured individuals were found in the same section (within 10 km) of a large estuary within and between winters (Rehfisch et al., 2003). In the same study, juvenile Dunlins were found to move longer distances between roosts than adults. Nevertheless, as expected, the degree to which individual shorebirds move from one wintering site to another depends partly on the distances between sites, as exemplified by colour-marked Sanderlings (Calidris alba) occupying sites 3 30 km apart in Portugal (Lourenc¸o et al., 2016). The chance of recording ringed individuals at particular sites increases with their length of stay, and many more individuals could use a site within a winter than are present at one time. Duration of stay is often linked with measured food supplies and social status, so that greater return rates are recorded in good than in poor food years, in adults than in first-year birds (eg 76% vs 48% in Great Cormorant; Ye´sou, 1995), or in territorial than in non-territorial individuals (Table 19.5; Johnson et al., 2001). The potential for observational bias gives uncertainty in how much the recorded variations in return rates between years and localities, or between sex and age groups, are due to differential survival, differential site-fidelity or merely to different durations of stay. All three factors could contribute to some degree to recorded return rates based on ring recoveries, adding to the effect of size of study areas. With tracking studies, these issues normally do not arise, although samples are often small. Studies of small insectivorous/frugivorous passerines (mainly Sylviidae and Parulidae) in the tropics have reported high winter recurrence, suggesting that at least most surviving individuals have returned to the same localities in

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successive years (Nisbet & Medway, 1972; Pearson, 1972; Price, 1981; Kelsey, 1989; Holmes & Sherry, 1992; Salewski et al., 2000; Latta & Faaborg, 2002). On the other hand, studies of similar species (mostly Sylviidae and Turdidae) in the Mediterranean region have generally reported lower return rates, indicating that many birds could have changed winter quarters within or between years (Herrera, 1978; Finlayson, 1980; Cuadrado, 1992, 1995; Catry et al., 2003). As the Mediterranean species depend more heavily on fruit in winter, it would not be surprising if they were less territorial and site faithful than their tropical equivalents which take more insects, and hence have more consistent food supplies. Moreover, some of the studies involved only territorial individuals (e.g., Nisbet & Medway, 1972; Kelsey, 1989), while others involved a mixture of territorial and non-territorial ones (e.g., Constat & Ebert, 1995; Cuadrado, 1995). Non-territorial birds might be expected to show less site fidelity. Swans, geese and sea ducks generally show high return rates to wintering sites, as to breeding sites, while freshwater diving ducks show lower return rates, and dabbling ducks lower still (Robertson & Cooke, 1999). These variations again relate partly to the stability and permanence of the various habitats that these different species occupy, and to changing water levels and ice cover. Wide dispersal between one winter and the next has been well documented from ring recoveries of several duck species, including Common Pochard (Aythya ferina) (see Figure 21.8) and Tufted Duck (Aythya fuligula) (Wernham et al., 2002).

Multiple wintering sites Many birds visit several sites during the course of a winter, generally moving progressively further from their breeding areas, each move seemingly triggered by depletion of local food supplies. Among Eurasian Blackcaps (Sylvia atricapilla) wintering in Spain, individuals returned each year to particular sites but varied their length of stay according to the size of the local fruit crops on which they fed (Cuadrado et al., 1995). The same held for Eurasian Siskins and other species which exploit annually variable seed supplies (Senar et al., 1992). Apparently, many northern birds which eat the seeds or fleshy fruits of trees take broadly the same migration route each year but pass particular latitudes much earlier in some years than in others, reaching the limits of their potential wintering range only in years of widespread crop failure (Chapter 20). The same holds for some ground-feeding seed-eaters whose food may be covered by snow, for some raptors and owls which depend on temporarily and locally high rodent populations, and for some waterfowl whose access to food varies with water levels and ice cover (Chapter 21). Similarly, in tropical regions, many species of migrants from northern continents visit two or more widely separated sites each year, returning to the same sites in different years. Originally suspected from observations, this behaviour has now been confirmed by tracking studies of individual migrants (Chapters 26, 28). Examples include Pallid Swifts (Apus pallidus) and Montagu’s Harriers (Circus pygargus) wintering in Africa (Norevik et al., 2018; Trierweiler et al., 2014) and Eastern Kingbirds (Tyrannus tyrannus) and Veeries (Catharus fuscescens) wintering in South America (Jahn et al., 2013; Heckscher et al., 2011, 2015).

Pelagic seabirds As it occurs in pelagic birds, fidelity to non-breeding areas is on a quite different spatial scale from what is meant by ‘site fidelity’ in landbirds. The wintering areas of pelagic species may be 2 4 orders of magnitude larger than those of landbirds, covering wide areas of upwelling or other productive waters (Chapter 8). On this basis, fidelity to non-breeding areas embracing thousands of square kilometres has been shown in Manx Shearwaters (Puffinus puffinus) (Guilford et al., 2009), Common Murres (Guillemots) (Uria aalge), Thick-billed Murres (Uria lomvia) (McFarlane Tranquilla et al., 2014), Atlantic Puffins (Ame´lineau et al., 2021), Northern Gannets (Morus bassanus) (Fifield et al., 2014), Black-legged Kittiwakes (Rissa tridactyla) (Le´andri-Breton et al., 2021), various albatrosses (Croxall et al., 2005; Phillips et al., 2005) and others. However, substantial shifts in wintering locations between years have been noted in Cory’s Shearwaters (Calonectris borealis) and others (Box 19.1; Dias et al., 2010), but whether such shifts are linked with food-supplies remains unknown. Fidelity to a large sea area may be partly a consequence of the sea presenting a more mobile habitat than land, as areas of specific conditions may shift in position from time to time, according to wind and current patterns. It may also result partly from the use by seabirds of highly mobile fish species which can themselves travel over long distances from day to day. In any case, seabirds clearly present a great contrast between the huge areas they use at sea and the same highly localized nest sites they use from year to year, whether specific cliff ledges, ground sites or burrows. Unlike pelagic species, seabirds that base themselves on land for resting and sleeping return to much more limited areas in successive winters, as exemplified by Great Cormorants and European Shags (Gulosus aristotelis) (Ye´sou, 1995; Grist et al., 2014) and by various gulls and terns (Coulson et al., 1984; Clark et al., 2016; Goodenough & Patton, 2019; Ku¨rten et al., 2022).

Dispersal and site fidelity Chapter | 19

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BOX 19.1 Movements of Cory’s Shearwaters (Calonectris borealis). Among Cory’s Shearwaters (Calonectris borealis), individuals from a single population headed to different destinations and sometimes also shifted between them in successive years (Gonza´lez-Solı´s et al., 2007). From both the Azores and Canary Islands, some individuals spent the non-breeding period off Brazil, and others off South Africa, either in the Benguela Current on the west side or in the Agulhas Current on the east side. Yet other individuals remained north of the equator and wintered in the Canaries Current. These areas were all nutrient-rich, offering abundant food. Of 14 other Cory’s Shearwaters tracked in successive years from a colony on the Salvage Islands, north of the Canaries, nine used the same wintering area in successive years, mostly in the Benguela Current, while the other five switched between years: two from the south to north Atlantic, two from the western to eastern South Atlantic and one from the Benguela to Agulhas Currents (Dias et al., 2010). This switching meant that some individuals spent successive winters in areas 7000 km apart, in different hemispheres. Possibly birds learned of different wintering areas by following other individuals on migration, and one non-breeding bird in two successive winters (at 4 and 5 years old) was found to visit all the different wintering areas of its population, a trip that entailed flying at least 108,000 km (Dias et al., 2010). Changes between such widely separated sites, some lying north and others south of the nesting colonies, represented an extraordinary degree of flexibility, compared with most birds.

Sex-related differences Sex-differences in return rates to particular wintering areas were noted in various species from Blue Tits to Harlequin Ducks, Buffleheads (Bucephala albeola) and Great Black-backed Gulls (Larus marinus) (Table 19.5). However, at least part of this sex difference may have resulted from differential survival rather than differential site fidelity. In contrast, ring recoveries and sightings gave no indication of sex differences in the winter site fidelity of Whinchats (Saxicola rubetra) in Nigeria (Blackburn & Cresswell, 2015) or of American Woodcock (Scolopax minor), Black Ducks (Anas rubripes) or Canvasbacks in eastern North America (Nichols & Haramis, 1980; Diefenbach et al., 1988, 1990). No sex differences in winter site fidelity would be expected in adult geese and swans because they remain in pairs year-round, as exemplified by Whooper Swans (Cygnus cygnus) and Bewick’s Swans (Cygnus columbianus bewickii) (Scott, 1980; Black & Rees, 1984).

Age-related differences In many bird species that migrate to lower latitudes, the adults often move shorter distances than the young (Chapter 18). So in these species, little or no winter site fidelity would be expected between the first and later years of life. Moreover, some long-lived species, in which individuals do not breed until they are several years old, show a progressive change to shorter distance moves or to shorter periods away from the breeding areas, with increasing age (Chapter 18). Such patterns have been noted in ring recoveries from a wide range of birds, including the Herring Gull (Larus argentatus) (Figure 18.7), Grey Heron (Ardea cinerea) (Olssen, 1958), Eurasian Oystercatcher (Goss-Custard et al., 1982) and Common Guillemot (Birkhead, 1974). This means that some individual birds occupy different areas in successive winters as they age, or that they spend progressively less time on their more distant wintering areas as they age. Studies on other species have indicated increasing winter site fidelity with increasing age and social status, greater in males than in females (Table 19.5; for Great Cormorant, see Ye´sou, 1995; for Greenland White-fronted Geese (Anser albifrons flavirostris), see Marchi et al., 2010, for Mallard (Anas platyrhynchos), see Nichols & Hines, 1987; for swans, see Scott, 1980; Black & Rees, 1984), matching the findings from breeding areas (see above). Again, however, it is usually uncertain how much the higher return rates of adult birds, compared to young ones, are due to greater site-fidelity and how much to greater survival. Tracking studies may eventually help to address this question.

COMPARISON OF BREEDING AND NON-BREEDING SITE FIDELITY Species which use the same nest sites from year to year do not necessarily show the same fidelity to wintering places. For example four White Storks (Ciconia ciconia) tracked by satellite over several years used the same nest sites every year but in different areas in Africa from year to year, depending on rainfall and resulting food supplies. One bird wintered in Tanzania in 1 year, further north in Sudan in the second year, but then went as far as South Africa in the third year and Botswana in the fourth. Hence, this one individual wintered in different years in places that extended from the northern tropics to the southern temperate zone (Berthold et al., 2002).

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Other species show the opposite tendency, with less fidelity to their breeding than to their wintering areas. For example in some arctic-nesting shorebirds, such as Curlew Sandpiper and Sanderling, breeding sites may change from year to year according largely to snow-melt patterns, but wintering sites are more consistent and are used by the same individuals year on year (Tomkovich & Soloviev, 1994; Elliott et al., 1976; Lourenc¸o et al., 2016). To set against these patterns, other species show extreme site fidelity in both breeding and wintering areas, while others show little or no site fidelity in either breeding or wintering areas, depending on the degree of predictability in their habitats and food supplies (Chapters 20, 21).

FIDELITY TO STOPOVER SITES Most migrants pause for refuelling up to several times during their journeys (Chapter 14). Some birds have been identified in successive years at the same places which they visit for a few days or weeks at a time. And because some species take different routes on their outward and return migrations, individuals may use different sites at the two seasons. To some extent, the landscape itself and its associated habitat areas are likely to impose some patterns of recurrence, regardless of any inherent tendencies in the birds themselves. Most passerines migrate in a broad front over more or less continuously suitable habitat, offering a wide choice of potential stopping places. In addition, the turnover of birds at stopover sites is high, as individuals normally stay only for short periods, often less than 1 day, so the chances of re-locating particular individuals by trapping are low. Not surprisingly, therefore, most studies in which researchers trapped large numbers of passerine migrants year after year at the same stopping sites found little or no evidence of individual year-to-year site fidelity; others gave small, but highly variable, proportions of retraps, exceeding 10% only in rare cases (Moreau, 1969; Nisbet, 1969; Veiga, 1986; Winker et al., 1991; Winker et al., 1992; Cantos & Telleria, 1994). However, for Eurasian Reed Warblers (Acrocephalus scirpaceus) caught in large numbers at an autumn stopover site in Israel, the return rate was 22% of 123 individuals, which was not very different from the return rate of summer breeders in the same area (27% of 210 individuals) (Merom et al., 2000). Some of the low return rates of passerines were perhaps no greater than expected by chance, if birds had paused at random in suitable habitat encountered on route. Higher rates of recurrence might be expected at habitat patches situated on the edges of seas or deserts that offer the last chance to feed before a crossing or the first chance after a crossing. For other migratory birds, notably waterfowl and shorebirds, suitable feeding areas are often localized and far apart, and it is in such species that the highest recurrence rates have been recorded. Some shorebirds and geese have only one or two main stopover sites on their migration routes, so inevitably almost the entire population may use these sites on each journey. Many ringed or tracked birds of these species have visited the same staging sites year after year (for shorebirds, see Pienkowski, 1976; Evans & Townsend, 1988; Harrington et al., 1988; Pfister et al., 1998; Wernham et al., 2002). The minimum annual return rate of adult Semi-palmated Plovers (Charadrius semipalmatus) to 10 15 ha of beach at Manomet in eastern North America, where the birds stayed for about 3 weeks each autumn, averaged 71% (Smith & Houghton, 1984). This proportion was similar to the likely annual survival rate, implying that most surviving individuals returned. Another large estimate of 65% was obtained for Sanderlings at a staging site in southwest Iceland (Gudmundsson & Lindstro¨m, 1992). Similarly, among Greenland White-fronted Geese staging in two areas of Iceland, and seen in more than one season, 89% were re-sighted within 4 km of the capture site from spring to the following autumn, 88% from autumn to the following spring, 96% from one spring to the next, and 100% from one autumn to the next (Fox et al., 2002). Same-season site fidelity (97%) was thus significantly greater from year to year than different season site fidelity (87%, Fisher’s exact test, n 5 177, P , .05). But the overall rates were again so high as to imply that all (or almost all) surviving birds used the same sites in successive years. Studies in which the same individuals were tracked on migration for more than 1 year have confirmed the repeated use of particular stopover sites, as in the Osprey (Va¨li & Sellis, 2015), various geese and swans, waders such as Eurasian Whimbrel (Numenius phaeopus) (Watts et al., 2021a,b), and various terns and gulls such as the Lesser Black-backed Gull (Larus fuscus) (Baert et al., 2022). High return rates to stopover sites might also be expected in soaring raptors, storks, cranes and pelicans, in which entire populations funnel each spring and autumn through narrow bottlenecks (Chapter 7). Such narrow-front migration is likely to limit the number of stopover sites available, thus raising the probability that individuals use the same places on successive journeys. Many individuals may use these sites for roosting, but not necessarily for feeding. Among birds in general, however, this degree of stopover site fidelity is probably exceptional, and despite following broadly the same route, many migrants may stop at different places in different years, either by choice or by force of circumstance. Summarizing, passerines and others that encounter many possible stopping places on their journeys apparently show less fidelity to specific stopover sites than do some waterfowl and shorebirds for which potential stopping places are

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few and far between. Among many passerines, fidelity to stopover sites is much less marked than fidelity to breeding or wintering sites, but other birds with a limited number of potential stopping places show similar high fidelity to these sites as they do to their breeding and wintering localities.

FIDELITY TO MIGRATION ROUTES The fact that some birds turn up at the same stopover sites in different years implies some constancy in the routes taken, a possibility that has been checked in recent years in individual birds tracked on migration. Caution is needed, however, not only because of potential inaccuracies in location estimates but also because long-distance journeys from different years plotted on a small-scale map can appear almost identical, while on the ground they can be tens or hundreds of kilometres apart. One method used so far is to measure longitude values at particular latitudes on route for successive journeys and use the difference between them as a measure of route consistency. On this basis, individual Ospreys, dependent on specific lakes to provide fish, migrated along highly consistent routes from year to year, while different individuals used markedly different routes and foraging areas from one another. In contrast, Western Marsh Harriers (Circus aeruginosus), which have wider choice of foraging habitats, showed less individual consistency in their routes from year to year, but also less variation in routes between individuals (Vardanis et al., 2016). Other raptors showing high fidelity to migration routes and stopover sites between years, as well as to breeding and wintering places, include Grey-faced Buzzards and Oriental Honey Buzzards satellite tracked in East Asia, the latter taking different routes in spring and autumn (Shiu et al., 2006). Among seabirds, high repeatability in migration routes taken by individuals in different years was recorded in Gull-billed Terns (Gelochelidon nilotica) and Common Terns (Goodenough & Patton, 2019; Ku¨rten et al., 2022), while in other birds, such as Wood Thrushes (Hylocichla mustelina) and Egyptian Vultures (Neophron percnopterus), individuals took different routes in different years, depending on wind conditions (Stanley et al., 2012; Lo´pez-Lo´pez et al., 2014). Nevertheless, some generalizations emerge from published tracking studies. First, the greatest individual constancy in routes is apparent in large waterfowl and other birds which migrate directly between regularly used staging sites, and among raptors which concentrate each year at narrow sea-crossings. Secondly, much greater variation is shown in routes of species that have no such regular staging sites but break their journeys at many different places. Thirdly, individuals tracked in more than one year often showed less variation in routes than did different individuals tracked in the same years: in other words, the variation within individuals was less than the variation between individuals (for Common Swifts (Apus apus), see Wellbrock et al., 2017; for Long-tailed Skuas (Stercorarius longicaudus), see van Bemmelen et al., 2017).

POST-FLEDGING DISPERSAL Once they become independent of their parents, the young of many species disperse from their natal sites, for a time moving in various directions and progressively further with increasing age (for Pied Flycatcher, see Sokolov, 2000b; for Golden Eagle (Aquila chysaetos), see Soutullo et al., 2006b; for Common Buzzard (Buteo buteo), see Walls & Kenward, 2020). As birds hatched in particular study areas gradually leave, others hatched elsewhere to move in. This moving and mixing happens every year at this time. Yet post-fledging dispersal is the least conspicuous of all bird movements, for it occurs at a time when many birds are at their most silent and often moulting. They accumulate no special body reserves and probably move mostly by short, low flights. They appear in a wider range of places than when nesting, but at the population level no large-scale latitudinal shift is apparent. Evidently, the tendency to disperse is inherent and hence endogenously influenced. After a period of post-fledging dispersal, juveniles of some sedentary species may stay in their dispersal areas thereafter, while juveniles of migratory species depart for winter quarters (for Barn Swallow, see Ormerod, 1991; for Pied Wagtail (Motacilla alba yarrelli), see Dougall, 1992; for Sand Martin (Riparia riparia), see Mead & Harrison, 1979; for Willow Warbler (Phylloscopus trochilus), see Norman & Norman, 1985; for Common Kestrel (Falco tinnunculus), see Village, 1990). The young from early broods have a longer period between fledging and migration than young from later broods and tend to wander over wider areas from the nest. In some species, a sex difference is also apparent, with females dispersing at an earlier age and further from their natal sites than males in the Willow Warbler (Norman, 1994), and males earlier and further than females in the Eurasian Sparrowhawk (Accipiter nisus) (Newton, 1986). On their return next spring, migrants settle near their natal areas in the pattern mentioned earlier, sometimes in the localities to which they dispersed in the post-fledging period. This was shown, for example in European Robins (Erithacus rubecula) studied near Lake Ladoga in Russia (Zimin, 2001). In this area of 7 3 1.5 km, most local young

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were replaced by immigrants during the period of post-fledging dispersal. The immigrants established and stayed on territories until they had completed moult, and then left on migration. Survivors returned the following spring to nest in the study plot, often in the same places where they had moulted the previous autumn. So in its effect on settling patterns, post-fledging dispersal was tantamount to natal dispersal. For a few weeks in late summer, the pattern of ring recoveries in migrants is similar to that of natal dispersal, with no directional bias (except in a few species in the northern hemisphere which have shown a northerly bias in postfledging dispersal; as in Sand Martin (Mead & Harrison, 1979), Lesser Kestrel (Olea, 2001), Northern Gannet (Kubetzki et al., 2009), and certain herons, Chapter 17). Then, as the young age, recoveries come from longer distances and are more directionally orientated, as the initial centrifugal dispersal gives way to long-distance directed migration. The change from random to directed movements is also evident among birds caught from the wild and tested in orientation cages (Shumakov, 2001). In those passerines that moult in their breeding areas, the transition from dispersal to migration occurs around the end of moult, and hence earlier in young from earlier than from later broods (Boddy, 1983; Dougall, 1992). But in some other long-distance migrants, which do not moult in their breeding areas, directional movement begins soon after the young become free of parental care, as shown, for example by the general southwesterly movement of newly independent European Pied Flycatchers, Lesser Whitethroats (Curruca curruca) and others revealed by ringing on the Courish Spit (Sokolov, 2000a). In some species, such as the European Robin and Eurasian Reed Warbler, post-fledging dispersal can occur at night (Rezvyi & Savinich, 2001; Mukhin & Bulyuk, 2001). Dispersing Eurasian Reed Warblers are attracted by nocturnal song playback and can be caught in mist nets placed in reed-beds near the tape recorder, the majority in the last third of the night. That such birds are dispersing rather than migrating is indicated by their age (mostly 39 52 days), state of moult, lack of migratory fat and lack of consistent directional preferences when tested in orientation cages (Bulyuk et al., 2000; Mukhin, 2004). Because Robins and Reed Warblers migrate at night, it is perhaps not surprising that they also disperse then; but one wonders how many other species do so. Nocturnal restlessness has also been recorded in captive juveniles of resident populations of Stonechats (Saxicola torquata) during the period of post-fledging dispersal before moult, giving further indication of endogenous influence (Van Doren et al., 2017). Some larger birds can travel extraordinary distances in their post-fledging movements. For example, satellitetracked juvenile Saker Falcons (Falco cherrug) in eastern Europe often moved more than several hundred km from their nest sites at this stage, and some more than a thousand kilometres. After an extensive period of nomadic travel, birds usually settled in one or more areas for a few weeks before heading southwest on migration (Prommer et al., 2012). In some species, when young are dispersing from their natal areas, adults also move away from their nesting places, perhaps in search of better feeding areas. Many waders depart for the coast after their young have become independent, assembling in flocks, where they may also moult and prepare for migration. Other examples of birds settling in areas away from the nest for a period before migration include Western Marsh Harriers and Montagu’s Harriers, the latter moving to higher altitudes where at that time grasshopper prey are more abundant than on breeding areas (Strandberg et al., 2008; Limin˜ana et al., 2008). In some large non-migratory raptors, post-fledging dispersal is a more prolonged affair which can extend over several years into adult life. Before the young finally leave their natal territories, they may undertake occasional excursions outside the territory, exploring places up to tens of kilometres away, only to return to their natal territory for a further period. Some young leave for good in the first autumn, while others may remain on their natal territories, tolerated and sometimes fed by their parents, until the start of the next breeding season. For several years, the young may then continue to roam over wide areas, spanning thousands of square kilometres, but pausing for days or weeks in particular places, until they eventually settle on a nesting territory. Young which disperse earliest in the season tend to move over longer distances. Temporally settlement often occurs in areas which lack breeding pairs, where immatures can live without interference. Such areas tend to be used year after year by successive cohorts of occupants. Birds eventually settle to breed on a territory which is usually not far from their own natal territory. Through the use of tracking devices on individuals, variants of this pattern have been described in non-migratory Common Buzzards and Red Kites which usually breed for the first time in their second or third year, and in Golden Eagles (Aquila chrysaetos), Spanish Imperial Eagles (Aquila adalberti) and White-tailed Eagles (Haliaetus albicilla), which typically breed for the first time in their fifth or sixth year (Ferrer, 1993; Walls & Kenward, 1998; Evans et al., 1999; Soutullo et al., 2006a,b; Whitfield et al., 2009; Weston et al., 2013; Engler & Krone, 2021). In such species, as in many others, males tend to settle to breed nearer their natal sites than females. Among Spanish Imperial Eagles, dispersal distances declined with advance in hatching date, with later-hatched young moving shorter distances. However, young that were fed ad lib in a reintroduction programme, and were probably in better condition, showed no such relationship (Ferrer & Morandini, 2017).

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DISPERSIVE MIGRATION Ring recoveries resulting from post-fledging dispersal usually decrease with increasing distance from the origin, as in natal dispersal, but they may extend further in some years, regions or habitats than in others, and further in one sex (usually females) than the other. In many resident species, recoveries come from greater average distances in successive months from fledging into winter, and then towards spring they come from localities progressively closer to the origin. The out-and-back movement patterns that are implied are apparent in a wide range of ‘resident’ species in Britain, from passerines to seabirds (Newton, 2008). Outward return movements have been confirmed independently in many species from tracking studies (e.g., Spruce Grouse (Dendragapus canadensis), Herzog & Keppie, 1980; Blue Grouse (Dendragapus obscurus), Cade & Hoffman, 1993; Greater Prairie Chicken (Tympanuchus cupido), Schroeder & Braun, 1993; Red Kite, Evans et al., 1999; Great Bustard, Morales et al., 2000; Common Buzzard, Walls & Kenward, 2020; and various seabirds, Chapter 8). In all these species, individuals moved outward from their natal or nesting areas after the breeding season, spent the winter in various other areas, and then moved back in time for the next breeding season. Individuals may use the same breeding and wintering places each year (for Spruce Grouse, see Herzog & Keppie, 1980). Because this dispersal is a back-and-forth seasonal movement, consistent in timing from year to year, it parallels directional migration. But at the population level it differs in that (1) it is not directional (unless direction is imposed by landscape or coastline); (2) the movements are also relatively short say mostly in the range of a few kilometres or tens of kilometres (at least in passerines and game birds); (3) recoveries drop off rapidly with increasing distance rather than concentrating in a specific distant wintering area; and (4) all or most individuals remain year-round within the breeding range of the species (although some seabirds may disperse far from their colonies to remote feeding areas, see below). The term ‘dispersive migration’ seems appropriate for this type of movement, emphasizing that it is seasonal, in various directions, and involves outward and return stages. While not obviously associated with seasonal changes in food supplies, one function of the movement is presumably to seek out good feeding sites for the winter or to exploit places that are suitable for wintering but not for breeding. It is clearly not related to latitudinal trends in food supplies. In some species, males typically migrate in smaller proportion than females, leave somewhat later and return earlier to their breeding areas next spring. In these respects, the return movements resemble the partial migrations of other birds. They also show sex differences in the distances moved, and in some lekking species in which males play no part in parental care, males travel further on average than females, as in Blue Grouse (Cade & Hoffman, 1993) and Great Bustard (Morales et al., 2000). Significant differences in the distances moved are also apparent between age classes in some species, such as Black Grouse (Tetrao tetrix) (Marjakangas & Kiviniemi, 2005). Dispersive migrations occur on a much grander scale among some seabirds, which move in various directions away from their nesting colonies after breeding, but often remain within the same sea-water zones as those used in the nesting season (Figure 19.5). This has been indicated by ring recoveries from many species, and more convincingly by the use of geolocators attached to birds at their nesting colonies. Examples from colonies around Britain include Atlantic Puffins, Guillemots, European Shags and Black-legged Kittiwakes, although birds from particular colonies might show a predominance of certain directions imposed by coastlines (Wernham et al., 2002; Chapter 8).

SITE ATTACHMENT Attachment of young birds to natal sites The young migratory birds must presumably learn the location of their natal area before they leave it, for only then could they return there after a long migration. This assumption has been confirmed experimentally in various species. When eggs or nestlings were transferred from one area to another, tens or hundreds of kilometres away, the resulting adults were often found breeding near their foster home rather than near their original home. However, the age of the birds at transference emerged as crucial, because attachment to a locality occurred at a specific stage of development: in passerines in the post-fledging period, between leaving the nest and leaving the area (Lo¨hrl, 1959; Berndt & Winkel, 1979; Sokolov et al., 1994). In one experiment, young Collared Flycatchers (Ficedula albicollis) were hand-reared at one site, and released at different ages at another site about 90 km to the south and previously unoccupied by this species (Lo¨hrl, 1959). Individuals released before or early in post-juvenile moult returned next spring to the release site, whereas those released late in moult or after moult did not return there. A short period of freedom during the first fortnight or so after

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FIGURE 19.5 Dispersive migration of two species of seabirds, based mainly on recoveries of birds ringed as nestlings in Britain (Wernham et al., 2002). (a) Common Murre (Uria aalge). (b) Black-legged Kittiwake (Rissa tridactyla).

leaving the nest appeared sufficient to fix the locality on these birds. Further research showed that fixation to a potential breeding locality occurred between 45 and 55 days of age in both Collared Flycatchers and Pied Flycatchers (Berndt & Winkel, 1979). The young of these species are raised in cavities, so would have no opportunity to view the outside world until they left the nest. In another experiment, young Common Chaffinches (Fringilla coelebs) released in a new area at less than 30 days old returned to this new area in a subsequent year, while those older than 40 days returned after migration mainly to their natal place (Sokolov, 1997). Evidently, site imprinting in Chaffinches occurred between ages 30 and 40 days, again mainly in the post-fledging period, before the young dispersed. However, if Chaffinches were hand-reared without sight of the outside world and then released at 50 days of age, some still returned to the release site in a later year. So if birds were denied the chance to learn the site at the usual age, they could do so later. If they learnt at the usual age, subsequent experience did not alter the preference established then. Age at site attachment for various other small passerines lay in the range 30 55 days, depending on species and rate of development (Sokolov, 2000a). Other experiments have involved pelagic seabirds in which individuals range over large areas of the ocean before they return to their natal colonies up to several years later. Owing to the building of a military airbase, 3124 Laysan Albatross (Diomedea immutabilis) fledglings were transferred from Midway Atoll in the Pacific to other colonies up to 400 km away (Fisher, 1971). Most of the survivors returned to Midway Island years later, as they reached breeding age. By the time they were moved, they had already become attached to their natal area and were unaffected by the move. But if young were relocated long before they reached fledging age, some of the transported chicks later returned to the release site rather than to the natal site. The sensitive stage, when site attachment occurred in this open-nesting species, fell in the last fourth of the 24-week nestling period. Even in burrow-nesting Short-tailed Shearwaters, the young developed an attachment to the natal colony long before they could fly (Serventy et al., 1989). Attachment occurred in the nestling period, as revealed by translocation experiments in which eggs and chicks of different ages were moved between colonies on different islands (Serventy et al., 1989). It was thought to occur at night when chicks sat outside their burrows and could see the wider world. After several years at sea, with annual migrations covering 30,000 km, returning birds distinguished their own colony from other colonies only 1 and 3 km away, as mentioned above. The tendency of young birds to breed near where they were raised has contributed to the success of conservation programmes in which bird species have been reintroduced to areas from which they were earlier eliminated. Even where young raised in the release area moved away after becoming independent, most of the survivors returned there to breed, leading to the establishment of a new local population. This has occurred in a wide range of species, including waterfowl, raptors and seabirds (Newton, 1979; Kress & Nettleship, 1988; Cade, 2000). Again the implication was that

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the young became fixated to the locality during their early life. All the above experiments are consistent with the view that birds learn their natal locations visually, but they do not exclude the possibility that they also use other clues, such as some aspect of the local magnetic field, as suggested for Manx Shearwaters (Wynn et al., 2020).

Attachment of young birds to wintering sites The attachment of young migrants to specific wintering localities seems to occur soon after their arrival there. Of 111 wintering Palm Warblers (Setophaga palmarum) that were caught soon after arriving in the Bahamas, 34 were released where they were caught, and the rest were transported and released at sites 10 and 23 km away. The proportion recaught at the capture site was about the same in all three groups, showing that displaced birds had returned there. Moreover, birds translocated at early dates in their stay (28 November 2 December) showed no difference in return rates from birds moved at later dates, suggesting that in this species site fixation had occurred fairly soon after arrival (Stewart & Connor, 1980). Similarly, juvenile and adult Dunlins that had arrived at a wintering site mainly in September October were displaced 133 km from the site at different dates in November December (Baccetti et al., 1999). From the proportions that returned from birds displaced at different dates, the juveniles seemed to have become attached to the site during November, within 1 2 months after arriving there. By December, return rates were the same as those of adults which had known the site from previous years (for similar findings on Sanderling, see Table 10.1).

SUMMARY Dispersal is a movement from one place to another. For individual birds, it can be measured by the distances between natal sites and subsequent breeding sites (natal dispersal), between the breeding sites of different years (breeding dispersal), and between the wintering sites of different years (non-breeding dispersal), regardless of any movements made in the interim. In all these types of dispersal, as well as in post-fledging dispersal, directions appear random (in any direction). Dispersal enables individuals to leave areas of overcrowding or poor food supply to explore and find somewhere better; it also reduces the chance of birds pairing with a close relative. At the population level, dispersal movements influence gene flow and the genetic structure of populations, facilitating or suppressing the development of locally adapted populations and subspecies. Dispersal movements also influence patterns of abundance and distribution across the range, enable depleted local populations to recover, vacated areas to be recolonized or new areas to be occupied, leading to range expansion. In many resident and migratory bird species, individuals tend to settle and breed near where they were raised, and the numbers of dispersed individuals decline with increasing distance from the natal site. However, individuals of large bird species generally move longer distances than those of small species. In addition, individuals of species that depend on ephemeral habitats or food sources tend to disperse further, on average, than do individuals of species with annually consistent habitats and food sources. Within species, dispersal distances also vary with population density and other factors that promote competition and differ according to gender and other features of the individual. In many bird species, on average, females move further between natal and breeding sites than do males, but in waterfowl and some others, males move furthest. In general, adults move over much shorter distances between their breeding attempts of successive years than young of their species move between natal and first breeding sites. Where conditions remain fairly stable from one breeding season to the next, adults of many species use the same nesting territories in successive years, although some individuals move to nearby territories, females more often than males, especially after a breeding failure. Where local conditions fluctuate from year to year, adults can move long distances between nesting sites of successive years. Long natal and breeding dispersal distances (of up to hundreds or thousands of kilometres) are frequent, for example in some seedeaters that depend on sporadic tree-seed crops, in some predatory species that specialize on cyclically fluctuating rodents, in some ducks that depend largely on ephemeral wetlands, and in some arctic-nesting waders influenced by patterns of snow melt. All such species may concentrate in different areas in different years, wherever conditions at the time are good. In wintering areas, some birds return to the same localities from year to year, while others are more mobile, within and between winters. The broad spectrum, from winter residency to almost continual and variable movement, appears to reflect a gradient in consistency of food supplies, ranging from stable and predictable to unstable and unpredictable. In many ‘resident’ bird species, post-fledging dispersal turns into dispersive migration, in that dispersed individuals move back toward their natal site as the breeding season approaches. In such out-and-back movements, directions appear

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random, but as in directional migration, one sex may disperse further than the other and juveniles further than older birds. Dispersive migration thus has some features of dispersal (directions highly variable but generally short distances) and some features of migration (return movement, often differing between the sexes, and repeated year after year). Young birds become fixated on the natal area in the late nestling or post-fledging period, depending on species, and on the wintering area within a few weeks after their first arrival there. Whatever other types of movements are undertaken by birds, dispersal can have both population and genetic consequences.

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Dispersal and site fidelity Chapter | 19

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Chapter 20

Irruptive migrants: boreal seed-eaters

Eurasian Siskins (Carduelis spinus), irruptive migrants from boreal regions In the course of this year, about the fruit season, there appeared, in the orchards chiefly, some remarkable birds which had never before been seen in England, somewhat larger than larks, which ate the kernel of the fruit and nothing else, whereby the trees were fruitless to the loss of many. The beaks of these birds were crossed, so that by this means they opened the fruit as if with pincers or a knife. The first documented record of a Crossbill invasion in England, Matthew Paris, 1251

Most migrations in birds are regular, taking place at the same dates, in the same directions, and for similar distances each year, as individuals move between the same breeding and wintering localities. In irruptive migrations, the proportions of birds leaving the breeding range, and the distances and directions they travel, vary greatly from year to year. While regular migrations are associated with regular and predictable food supplies, irruptions are associated with sporadic food supplies, which vary greatly in abundance and distribution from one year to the next (Newton, 2006a). Typical irruptive migrants are food specialists for at least part of the year, and all can breed or winter in widely separated areas in different years. 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. Typical irruptive migrants of northern regions include (1) boreal finches and others that depend on fluctuating treeseed and fruit crops; (2) owls and others that depend on cyclically fluctuating prey populations; and (3) waterbirds that depend on ephemeral wetlands created by irregular rainfall. The movements of all such species can be understood only in terms of their underlying ecology, which is therefore described in some detail. This chapter is concerned with the seed-eaters and the next chapter with the other groups. Among the specialist seed- and fruit-eaters, most individuals stay in the north in years when food is plentiful there, wintering within or just south of their breeding areas, but moving to lower latitudes in years when food is scarce. Their irruptions, in which they appear in large numbers well outside their usual range, follow periodic widespread crop The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00025-7 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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failures. Irruptive migration thus occurs in response to annual, as well as seasonal, reductions in food supplies. The effect of food shortage is often accentuated because the birds themselves tend to be numerous at such times, as a result of good breeding and survival in previous years when food was plentiful (Lack, 1954; Bernd & Henss, 1967; Ko¨enig & Knops, 2001). It is not, therefore, merely poor food supplies that stimulate large-scale emigration, but poor supplies relative to the number of birds present. Fieldfares (Turdus pilaris) left an area in southern Finland when their main food source (Rowan (Sorbus aucuparia) berries) had been reduced to an average of about two fruits per bunch (Tyrva¨inen, 1975). The date at which this occurred depended on both the initial crop size and the number of consumers. Accordingly, mass emigration in different species has been linked with either ‘food shortage’ or ‘overpopulation’. Most irruptive seed-eaters are hard to study because they breed mainly at high-latitudes where human population densities are low and the chances of obtaining ring recoveries are extremely small. Moreover, because of their irruptive behaviour, many such species are seldom in the same area long enough for prolonged study. For these reasons, an understanding of their movement patterns must be pieced together from information collected over a long period and scattered widely through the ornithological literature, although ring recoveries are slowly adding new information. Only in recent years have tracking tags become small enough to be used on these species, but low site fidelity means that the chance of re-trapping the same individuals to recoup the information from geolocators is minuscule.

SEED CROPS Typically, northern tree-seed crops vary greatly in size from year to year, and in some years fail completely (Figure 20.1). Fruiting depends partly on the natural rhythm of the trees themselves and partly on the weather. Trees of most species require more than 1 year to accumulate the nutrient reserves necessary to produce fruit. For a good crop, the weather must ideally 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 reduced or delayed for another year. In any one area, most of the trees of a species fruit in phase with one another partly because they come under the same weather, and often those of several different species also crop in synchrony. The result is a great profusion of tree fruits in some years and practically none in others. Good crops almost never occur in consecutive years, and nor do poor crops, but each good crop is usually followed by a poor one (Figure 20.1; Ko¨enig & Knops, 1998, 2000). The trees in widely separated areas may be on different fruiting regimes, partly because of regional variations in weather, so good crops in some areas may coincide with poor crops in others. Nevertheless, good crops may occur in many more areas in some years than in others, so the total continental seed production also varies greatly from year to year. An analysis of the fruiting patterns of various boreal conifer species at many localities in North America and Eurasia revealed high synchrony in seed production in localities 500 1000 km apart, depending on tree species. The synchrony declined at greater distances, and by 5000 km no correlation was apparent within particular tree species (Ko¨enig & Knops, 1998). Later studies gave similar conclusions for various Eurasian and North American trees, with asynchrony in cropping emerging at distances greater than 1000 or 2000 km, depending on tree species (LaMontagne et al., 2020; Zamorano et al., 2018). These figures give some idea of the range of distances that must separate the successive breeding and wintering areas of some boreal finches if the same individuals are to have access to good treeseed crops every year. Nevertheless, the seed crops of some tree species fluctuate less than others. Among European trees, Scots Pine (Pinus sylvestris) produces smaller but more consistent crops than Norway Spruce (Picea abies), and Alder (Alnus glutinosa) produces more consistent crops than Birch (Betula pendens) and (Betula pubescens). Also while most conifers produce their seeds in the same year as flowering, Scots Pine takes another year for the cones to form. FIGURE 20.1 The mean number of Norway Spruce (Picea abies) cones per tree each year in southern Sweden, 1909 67. From Hagner (1965) and Go¨tmark (1982).

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409

The timing of ripening and release of seeds is also important to the birds that eat them. Some conifer species release most of their seeds within a short period in autumn, others more slowly over winter, and yet others in spring, or even more gradually over 2 or more years. Prolonged release occurs in some Pine Pinus and Larch Larix species which can thereby provide food for seed-eaters even in non-cropping years. For most finches, the seeds are most available while they remain on the tree; once they fall to the ground they become rapidly removed by other animals or covered by snow. Among European irruptive finches that depend on tree seeds, only the Brambling (Fringilla montifringilla) feeds for preference on the ground, though others do so occasionally; among the North American irruptive species, all seem to prefer the trees.

IRRUPTIVE SEED-EATERS AND FRUIT-EATERS Species known for their irruptive migrations are listed in Table 20.1, along with their main food plants. Some such species eat seeds year round, but different types of seeds at different seasons, as exemplified by redpolls and siskins. Others eat mainly insects in summer and seeds (or fleshy fruits) in winter, as exemplified by the Bohemian Waxwing (Bombycilla garrulus), Brambling (Fringilla montifringilla) and Evening Grosbeak (Hesperiphona vespertina). These last two species tend to concentrate in breeding areas with insect outbreaks: the Brambling in areas with high densities of the moth (Epirrita autumnata), and the Evening Grosbeak and others in areas with Spruce Budworm (Choristoneura fumiferana) (Morris et al., 1958; Enemar et al., 1984; Lindstro¨m et al., 2005). Both species eat tree seeds in winter. Most irruptive seed-eaters make autumn and spring movements, like most other birds, but varying in distance according to the seed-crops encountered (Sva¨rdson, 1957; Newton, 1972; Jenni, 1987). Only when the migrants are exceptionally numerous or their food generally scarce do they reach the furthest parts of their wintering range as an ‘invasion’ (Figure 20.2). However, crossbills and nutcrackers, which eat conifer seeds year-round, apparently make only one major movement each year, from regions where last year’s crops were good to regions where the current year’s crops are good (see later). TABLE 20.1 Established year-to-year correlations between bird abundance and food supply in seed-eating and fruiteating birds. Species

Preferred winter fooda

Summer densities

Winter densities

Autumn emigration

References

Great Spotted Woodpecker (Dendrocopos major (P))

Spruce, Pine and other seeds

K

K

K

Pynno¨nen (1939), Formosov (1960), Eriksson (1971)

Bohemian Waxwing (Bombycilla garrulus (H))

Rowan and other berries

K

Siivonen (1941), Tyrva¨inen (1975), Bock & Lepthien (1976)

Fieldfare (Turdus pilaris (P))

Rowan and other berries

K

Tyrva¨inen (1975)

Coal Tit (Periparus ater (P))b

Spruce seeds, insects

K

Formosov (1965)

Black-capped Chickadee (Parus atricapillus (N))

Conifer seeds, insects

K

Bock & Lepthien (1976)

Great Tit (Parus major (P))

Beech seeds

K

K

Ulfstrand (1962), Perrins (1966), Berndt & Henss (1967)

Blue Tit (Cyanistes caeruleus (P))

Beech seeds

K

K

Ulfstrand (1962), Perrins (1966)

Wood Nuthatch (Sitta europaea (P))

Spruce seeds

K

Berndt & Dancker (1960), Enoksson & Nilsson (1983) (Continued )

410

The Migration Ecology of Birds

TABLE 20.1 (Continued) Species

Preferred winter fooda

Red-breasted Nuthatch (Sitta canadensis (N))

Pine and other conifer seeds

Brambling (Fringilla montifringilla (P))

Beech seeds and caterpillars

K

Eurasian Siskin (Spinus spinus (P))

Birch, Alder and conifer seeds

K

Pine Siskin (Spinus pinus (N))

Conifer, Birch and Alder seeds

Common Redpoll (Acanthis flammea (H))

Birch and Alder seeds

Arctic Redpoll (Acanthis hornemanni)

Summer densities

Winter densities

Autumn emigration

References

K

Bock & Lepthien (1976), Widlechner & Dragula (1984), Davis & Morrison (1987)

K

K

Silvola (1967), Enemar et al. (1984), Nilsson (1984), Lindstro¨m (1987), Lindstro¨m et al. (2005), Hogstad (2000, 2005), Jenni & Neuschulz (1985), Jenni (1987), Eriksson (1970c), Mikkonen (1983)

K

K

Sva¨rdson (1957), Haapanen (1966), Hogstad (1967), Eriksson (1970b), Petty et al. (1995), Fo¨rschler et al. (2006)

K

Bock & Lepthien (1976), Widlechner & Dragula (1984)

K

K

Evans (1966a), Eriksson (1970a), Enemar et al. (1984)

K

K

Bock & Lepthien (1976), Nystro¨m & Nystro¨m (1991)

Eurasian Bullfinch (Pyrrhula pyrrhula (P))

Rowan and other tree seeds and berries

K

K

Sva¨rdson (1957), Fox et al. (2009)

Pine Grosbeak (Pinicola enucleator (H))

Rowan, other tree fruits and buds

K

K

Grenquist (1947), Bock & Lepthien (1976)

Evening Grosbeak (Hesperiphona vespertina (N))

Maple and other treeseeds

K

Parks & Parks (1965), Bock & Lepthien (1976)

Purple Finch (Haemorhous purpureus (N))

Various treeseeds

K

Bock & Lepthien (1976), Ko¨enig & Knops (2001)

Red (Common) Crossbill (Loxia curvirostra (H))

Spruce and other conifer seeds

K

K

K

Reinikainen (1937), Formosov (1960), Newton (1972), Bock & Lepthien (1976), Benkman (1987), Petty et al. (1995), Fo¨rschler et al. (2006)

Two-barred (White-winged) Crossbill (Loxia leucoptera (P))

Larch and other conifer seeds

K

K

K

Newton (1972), Larson & Tombre (1989), Bock & Lepthien (1976)

Parrot Crossbill (Loxia pytyopsittacus (P))

Scots Pine seeds

K

K

K

Newton (1972)

Eurasian Jay (Garrulus glandarius (P))

Oak seeds

K

Cramp & Perrins (1994)

K

(Continued )

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411

TABLE 20.1 (Continued) Species

Preferred winter fooda

Thick-billed Nutcracker (Nucifraga c. macrorhynchos (P))

Hazel and Swiss Stone Pine seeds

Thin-billed Nutcracker (Nucifraga c. caryocatactes (P))

Siberian Stone Pine seeds, Brush Pine seeds

Clark’s Nutcracker (Nucifraga columbiana)

Whitebark Pine and other conifer seeds

Summer densities

Winter densities

K

K

Autumn emigration

References

K

Mattes & Jenni (1984)

K

Formosov (1933), Ananin & Sokolov (2009)

K

Lanner (1996)

H, Holarctic; N, Nearctic; P, Palaearctic. a Scientific names of trees: alder Alnus, Beech (Fagus sylvatica), birch Betula, Hazel (Corylus avellana), larch Larix, maple Acer, oak Quercus, Rowan (Sorbus aucuparia), Scots Pine (Pinus sylvestris), Siberian Stone Pine (Pinus sibirica), spruce Picea, Swiss Stone (Arolla) Pine (Pinus cembra), Brush Pine (P. pumila), Whitebark Pine (Pinus albicaulis), Chihuahua Pine (Pinus chihuahuana). Where several species in the same genus are involved, only the generic name is given. b In this species, mass emigration has been more frequently linked with high numbers (which may cause food shortage) or with high spring temperatures which promote high breeding success (Markovets & Sokolov, 2002).

Many birds

Many birds

Few birds

Few birds

Win

teri

ng

ran g

e

Breeding range

No birds

1

No birds

Many birds

Few birds

2

3

4

FIGURE 20.2 Model of migration system in irruptive finches. The birds leave the breeding range across boreal Europe each autumn on a broad front, travelling southwest, but only until they meet areas with abundant seed crops. The sporadic cropping pattern of trees means that each year birds from some sectors of the breeding range must travel further than others. The next year, the pattern of tree cropping and migration may differ so that birds from particular sectors of the breeding range travel different distances in different years. From Jenni (1987). Scenario 1 good crops throughout the wintering range: all birds accommodated in northern areas, nearest the breeding areas, and crops further south remain unused; survival good. Scenario 2 good crops in the north of the wintering range, but not in the south: all birds accommodated in northern areas; survival good. Scenario 3 good crops in the south of the wintering range but not in the north: birds accommodated in the southern areas; survival moderate. Scenario 4 crop failure throughout the wintering range: birds spread widely, but at low densities; survival poor. On this model, it is in the northern parts of the wintering range that correlations between seed crops and bird densities in different years would be expected to be most marked; further south, good crops can sometimes occur with few birds, or vice versa. Most tree species, such as Birch Betula and Rowan Sorbus aucuparia, retain their seeds into the winter, so the finches that eat them take the seeds directly from the trees, regardless of snow. Other trees, such as Oak Quercus robur and Beech Fagus sylvatica, shed their seeds in autumn so that the birds that eat them must take them from the ground. Such birds are therefore also affected by snowfall, which can render abundant seed crops unavailable. Thus, the movements and winter distributions of the Bramblings Fringilla montifringilla in different years are a function of both Beech crops and snowfall (Jenni & Neuschulz 1985, Jenni 1987).

412

The Migration Ecology of Birds

TWICE-YEARLY MIGRANTS Like most other landbirds, twice-yearly migrants generally move to more southern latitudes in autumn and to more northern ones in spring, but unlike other birds, they may concentrate to breed and winter in different areas in different years, wherever their food is plentiful at the time. Their local numbers thus fluctuate greatly from year to year according to local food supplies, and in winter may range between total absences in years when appropriate tree seeds are lacking, to thousands of birds per square kilometre 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 (Sva¨rdson, 1957; Newton, 1972; Jenni, 1987). In consequence, the distance travelled by the bulk of the migrants varies between years, 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 ‘invasion’ (Figure 20.2). By this strategy, birds travel no further than necessary and do not pass over good feeding areas which might be the only ones available that year. Other species also exploit the same foods as the irruptive species but do not depend so heavily on them, so are less affected by the fluctuations in fruiting. Similarly, some of the species listed in Table 20.1 may be irruptive in some parts of their range but not in others, depending on the breadth of the diet and the level of fluctuation in their total food supply. Populations that have access to a wide range of dietary items are less likely to experience a shortage of all types in the same year. The Eurasian Bullfinch (Pyrrhula pyrrhula), Wood Nuthatch (Sitta europaea) and various titmice Parus spp. are all irruptive in parts of their range and elsewhere are either residents or regular migrants.

Breeding densities Among irruptive seed-eaters, breeding densities in particular localities have long been known to show big year-to-year fluctuations (for references, see Table 20.1). In one study, densities of Common Redpolls (Acanthis flammea) fluctuated about 39-fold over a 20-year period, with the highest densities coinciding with exceptionally good Dwarf Birch (Betula nana) crops, the low bushes and their seed-catkins protected under snow since the previous year (Enemar et al., 1984). Densities of Eurasian Siskins (Spinus spinus) fluctuated 6- to 50-fold in four different areas in parallel with the spruce cone crop (Haapanen, 1966; Hogstad, 1967; Shaw, 1990; Fo¨rschler et al., 2006); and densities of Bramblings fluctuated by 5- to 26-fold in three different areas in parallel with the abundance of moth larvae (E. autumnata) (Silvola, 1967; Lindstro¨m, 1987; Lindstro¨m et al., 2005; Hogstad, 2000, 2005). In all these species, local increases in numbers from one year to the next were often far greater than could be explained by high survival and reproduction from the previous year, so must also have involved immigration (Figures 20.3 and 20.4). Such species contrast with other seed-eaters, whose densities typically vary by less than threefold from year to year.

Breeding dispersal One line of evidence suggesting frequent shifts between breeding localities in different years comes from measured rates of turnover in the occupants of particular study areas. In regular migrants, if the birds occupying a particular study area are trapped and ringed in the breeding season, large proportions of the same individuals are usually found breeding in the same area next year. Most are found on the same territories, and those that change territories usually move over relatively short distances, staying within the general area. Return rates are usually within the range 30% 60% for passerines, and 60% 90% for nonpasserines (Chapter 19). Allowing for expected mortality, such high figures imply that most surviving individuals return to breed in the same limited area year after year. In some regular migrants, the same holds for wintering areas (Chapter 19). FIGURE 20.3 Densities of Common Redpolls (Acanthis flammea) in 9 km2 of birch scrub in Swedish Lapland, 1963 82. Over this period, the fluctuations in numbers were mostly moderate, but with exceptionally large numbers in 1968 and 1971, which could only have resulted from massive immigration. In these 2 years, the birch crop was unusually good, the seeds having remained on the trees from the previous summer when they were formed. In these years, Redpolls overwintered in the area, started breeding earlier than usual, and produced larger clutches, some raising more than one brood. In 1978 few Redpolls occurred in the area, despite good numbers in the preceding and following years. From Enemar et al. (1984).

100

Pairs per km2

75

50 25 0 1962 1965 1968 1971 1974 1977 1980 1983 Year

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413

Spruce crop

(A) 4

45

3

40

1 0

Siskin pairs per km2

1959

1960

1961

1962

1963

50 40 30 20

Siskin pairs per km2

2

35 30 25 20 15 10 5

10 0

0 1959

1960

1961 Year

1962

1963

0

1

2 Spruce crop

3

4

(B) 200

60

Caterpillars Brambling density

Brambling density

Brambling

100

0 1972

50 40 30 20 10 0

1979

1986 Year

1993

2000

0

50

100

150

200

Caterpillar density

FIGURE 20.4 (A) Numbers of breeding Eurasian Siskins (Spinus spinus) in relation to the spruce crop in Finland. Siskins shown in pairs per km2 and cone crops classified into four categories.. For similar patterns for Siskins in other areas see Hogstad, 1967; Shaw, 1990; and Fo¨rschler et al., 2006. (B) Numbers of breeding Bramblings (Fringilla montifringilla) in relation to the abundance of the geometrid moth Autumnal Moth (Epirrita autumnata) caterpillars in northern Norway. Bramblings measured as number of singing males, and Epirrita as the number of caterpillars per 100 net sweeps in birch trees during 1972 98. Similar data were given for other areas by Silvola (1967) and Lindstro¨m (1987). Moth outbreaks occur about every 10 years and last several years at a time. They are synchronized over large areas. (a) From Haapanen (1966); (b) Redrawn from Hogstad (2000).

Among irruptive migrants, in contrast, return rates to the same study area are much lower (Table 20.2). For example among Bramblings trapped in the breeding season in various areas, individuals were seldom or never caught in the same locality in a later year, so each year’s occupants differed from those the year before. In one study, only 7 (0.6%) of 1238 adults were re-trapped in the same area, and none of 1806 juveniles, despite a regular annual trapping programme over many years (Lindstro¨m et al., 2005). Similar findings have come from studies on other irruptive species elsewhere, in which all recorded return rates were very much lower than expected from their annual survival rates (Table 20.2). The implication was that large proportions of individuals changed their nesting locations from year to year. For some irruptive species, small numbers of ring recoveries confirm this. Three Bramblings were found in different breeding seasons at places 280, 420 and 580 km apart; one Eurasian (Northern) Bullfinch (Pyrrhula pyrrhula) at places 424 km apart (natal dispersal), two Common Redpolls at places 280 and 550 km apart, one Lesser Redpoll (Acanthis cabaret) at places 300 km apart (natal dispersal), and one Eurasian Siskin at places 120 km apart. In North America, two Pine Siskins (Spinuss pinus) were found at places 346 and 1138 km apart (Brewer et al., 2000). Of nine recoveries of Evening Grosbeaks in different breeding seasons, two were at the same place, three were within 100 km and four had moved 322 946 km (Brewer et al., 2000). Clearly, long-distance moves from one breeding area to another are not unusual in irruptive finches.

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The Migration Ecology of Birds

TABLE 20.2 Annual return of individual birds to the same area—irruptive migrants. Species

Number ringed

Number (%) re-caught in a later year in the same place

Location (years)

References

Brambling (Fringilla montifringilla)

1238

7

(0.6%)

Sweden (19)

Lindstro¨m et al. (2005)

Eurasian Siskin (Spinus spinus)

391

30

(7.7.%)

Scotland (6)

Shaw (1990)

Pine Siskin (Spinus pinus)

1322

4

(0.3%)

Oklahoma (?)

Baumgartner & Baumgartner (1992)

Common Redpoll (Acanthis flammea)

?

?

(,1.%)

Alaska (?)

Troy (1983)

Cedar Waxwing (Bombycilla cedrorum)

54

2

(3.7%)

Ohio (6)

Putnam (1949)

Evening Grosbeak (Hesperiphona vespertina)

2637

0

(0)

New York (18)

Yunick (1983)

Evening Grosbeak (H. vespertine)

.1700

48

(0.3%)

Pennsylvania (14)

Speirs, in Newton (1972)

Pine Siskin (S. pinus)

3810

0

(0)

New York (18)

Yunick (1983)

Pine Siskin (S. pinus)

4045

0

(0)

New York (2)

Yunick (1997)

Pine Siskin (S. pinus)

1322

4

(0.3%)

Oklahoma (4)

Baumgartner & Baumgartner (1992)

Common Redpoll (Acanthis flammea)

7946

0

(0)

New York (18)

Yunick (1983)

Common Redpoll (A. flammea)

1800

0

(0)

New Hampshire (?)

Troy (1983)

Common Redpoll (A. flammea)

5200

16

(0.3%)

Alaska (?)

Troy (1983)

Common Redpoll (A. flammea)

5998

1

(0.02%)

Belgium (2)

Herremans & Gielen (2020)

Purple Finch (Haemorhous purpureus)

2822

13

(0.5%)

New York (18)

Yunick (1983)

Purple Finch (H. purpureus)

1015

51

(5.0%)

North Carolina (5)

Blake (1967)

Brambling (Fringilla montifringilla)

2330

16

(0.5%)

England (7)

Browne & Mead (2003)

Breeding areas

Wintering areas

Autumn emigration Typically, as mentioned above, the numbers of birds undertaking migration, and the distances involved, vary greatly from year to year. Huge annual variations in the numbers of passing migrants are evident at migration watch sites, such as Falsterbo and Ottenby in Sweden, in which the numbers of some irruptive species can vary from nil in some years to many thousands of individuals in other years (Figures 20.5 and 20.6). For example during 1973 2021, the Eurasian Jay (Garrulus glandarius) count at Falsterbo was nil in 39 years, but good numbers passed in other years, reaching 19,004 in 1994. Over the same period, Bohemian Waxwings varied from nil in 14 years to 22,850 in 2004, and Common Redpolls from nil in 3 years to 44,343 in 2017 (Falsterbo Bird Observatory website). These annual fluctuations were far greater than those recorded in more regular long-distance migrants counts of which typically varied by up to three- to fourfold, occasionally up to 10-fold, between years. Similar differences between irruptive and regular migrants have been recorded at other watch sites (e.g., Dorka, 1966; Gatter, 2000). The extent of autumn emigration from the breeding range has been related to food supplies in almost all irruptive seed-eating and fruit-eating species discussed here, being greatest in years when high densities coincided with poor seed crops (Table 20.1; Figures 20.6 and 20.7a). Moreover, the various species that depend heavily on the same seed or

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415

FIGURE 20.5 Annual fluctuations in the numbers of four irruptive species (all diurnal migrants) counted during August November while migrating over Falsterbo¨ in southern Sweden, 1973 2008. Note different scales. Compiled from data on the Falsterbo¨ website, attributed mainly to G. Roos and N. Kjellen.

b r2 p

b r2 p

b r2 p

FIGURE 20.6 Numbers and timing of Eurasian Siskins (Spinus spinus) migrating through Ottenby each year in relation to the size of the Birch Betula seed crop further north. Drawn from data in Sva¨rdson (1957).

fruit crops as one another tend to irrupt in the same years. They include the Eurasian Blue Tit Cyanistes caeruleus and Great Tit (Parus major) both of which eat Beech (Fagus sylvatica) mast, and the Red (Common) Crossbill (Loxia curvirostra) and Great Spotted Woodpecker (Dendrocopus major) both of which eat spruce seeds. Where different tree species fruit in phase with one another, the number of participating species is increased further. Over much of the boreal region of North America, conifer and other tree crops tend to fluctuate biennially, and in the alternate years with poor crops several species that depend on them migrate to lower latitudes. The migrations of

416

The Migration Ecology of Birds

200

4 150 3 100 2 50

1

500 Autumn catch of Bullfinches

Rowanberry index in Finland (bars)

5

Bullfinch winter index in Finland ( ●)

irruptive species are therefore much more regular in North America than in Europe and much more synchronized between species (Bock & Lepthien, 1976; Kennard, 1976; Larson & Bock, 1986; Ko¨enig & Knops, 2001; Figure 20.8). For much of the 20th century, at least eight species of boreal seed-eaters tended to irrupt together in response to the widespread synchronization of seed-crop fluctuations (namely Common Redpoll, Pine Siskin, Purple Finch (Haemorhous purpureus), Evening Grosbeak, Red-breasted Nuthatch (Sitta canadensis) and Black-capped Chickadee (Poecile atricapillus), as well as the Red Crossbill and Two-barred (White-winged) Crossbill (Loxia leucoptera) discussed later). These species vary in the proportions of conifer and broad-leaved tree seeds in their diets (Table 20.1; Bock & Lepthien, 1976; Kennard, 1976; Ko¨enig & Knops, 2001). Over periods of years, different species of trees in the same area can drift in and out of synchrony with one another, affecting the movements of the birds that specialize on them. During the period 1921 50, the biennial pattern and synchrony between the various North American seedeaters was less marked than before or after this period (Larson & Bock, 1986). In some years, irruptions were evident across North America, but in other years only in western or eastern regions (Ko¨enig & Knops, 2001). In addition, crop failures and irruptions from montane areas south of the boreal region were not well synchronized with those within the boreal region (Bock & Lepthien, 1976).

400

300 200

100 R² = 0.45

0

1977

1981

1989 1985 Autumn season

1993

0

0

10

100 Norwegian Rowanberry index

1000

FIGURE 20.7 Left. Annual Rowanberry (Sorbus aucuparia) abundance indices for North Karelia, Finland (histogram columns) compared with the annual Finnish winter bird count index for Eurasian (Northern) Bullfinch (Pyrrhula pyrrhula) during 1977 95 (linked filled squares); Right. Annual autumn catches of Eurasian Bullfinches at the Christiansø Bird Observatory, Denmark, plotted against the annual Rowanberry (Sorbus aucuparia) indices from Norway (note logarithmic scale), to the north, during 1976 2001 and 2004 (y 5 103.9 ln(x)1 699.2, r2 5 0.45, F1,22 5 18.3, P , .001). Based on data from Fox et al. (2009).

FIGURE 20.8 Year-to-year variation in the winter ranges of three species of seed-eating birds that breed in northern North America. Dots show large wintering populations in local regions. In years of low food supply in the north, all species tend to winter far to the south. From Bock & Lepthien (1976).

Irruptive migrants: boreal seed-eaters Chapter | 20

417

Migration timing In some irruptive migrants, autumn migration begins much earlier than usual in the years of large-scale emigration. For example the peak autumn days for Siskins (Spinus spinus) at Falsterbo during 1949 88 varied from mid-August to mid-November in different years (Roos, 1991), and elsewhere heavy southward movements have been seen as late as December January (Sva¨rdson, 1957). Over a 9-year period, Siskins passed through Ottenby Bird Observatory in largest numbers, and at the earliest dates, in years when the birch crop further north was poor (Figure 18.6; Sva¨rdson, 1957). The tendency for birds to linger longer in the north in years of good tree-seed crops has been noted in many other irruptive seed and fruit-eaters (Berndt & Henss, 1967; Gatter, 2000; Kanerva et al., 2020), as has their tendency to arrive earlier in more southern wintering areas in invasion years. Annual variations in autumn migration dates are clearly much greater in irruptive than in other migrants, which travel at approximately the same dates each year (Chapter 13). Most irruptive seed-eaters begin to take their main winter food in late summer or autumn before their migration begins, so the size of the crop can have a direct influence on departure dates and numbers leaving. Other species start migrating before the winter seed crop is ready and tend to migrate at more consistent dates from year to year. They include the Brambling, Wood Nuthatch and various tits, all of which eat Beech (Fagus sylvatica) mast in winter, but begin to leave before the seeds are ready (Berndt & Dancker, 1960; Eriksson, 1971).

Migration directions In most European bird species, individuals from the western parts of the breeding range tend to use migration routes and wintering areas that lie to the west of birds from the eastern parts, migrating along roughly parallel routes (Chapter 25). However, this tendency is less marked in irruptive than in regular migrants because irruptive migrants typically show a greater east west component in their movements, and also greater directional spread. In addition, irruptive species may end their journey at widely different places on the route each year. Thus in any given year, birds from one part of the breeding range may stay in the north if food permits, while those from another part may extend far to the south (Figure 20.2). The following year, the pattern may differ. It is these behaviours that contribute to individuals turning up in widely separated places in different winters. Most are at different points on the same migration axis, but some may end up in one winter far to the west or east of their location in a previous winter. Even within a winter, the birds may wander in various directions, and end up markedly to the east or west of their initial route (for Bohemian Waxwings, see Cornwallis & Townsend, 1968). The greater directional spread of irruptive, compared to regular migrants, is evident from observations at migration watch sites, and also from subsequent ring recoveries of birds trapped on migration. Typically, the recoveries of irruptive migrants ringed in autumn and recovered in the following months show two or three times the angular spread as those of regular migrants (for example, see Payevsky, 1998). The wide directional spread in irruptive migrants is apparent within years but also stems from birds taking mainly different main directions in different years. From Common Redpolls ringed in Fennoscandia, most ring recoveries in 1965 came from directions east-southeast (mostly in Russia), whereas in 1972 and 1986 they came from directions to the southwest (mostly in western Europe) (Figure 20.9; Zink & Bairlein, 1995; Lensink et al., 1986; Thies, 1991). This difference could be explained if the birds were tracking seed crops, which took them in different directions from their breeding areas in different years. Another feature of irruptive migrants is that they often make long movements within a winter, staying in one area as long as food lasts, and moving further along the migration route when food runs out (for Pine Grosbeak (Pinicola enucleator), see Grenquist, 1947; for Common Redpoll, Bohemian Waxwing and Fieldfare, see Haila et al., 1986). In effect, the birds move progressively further from their breeding areas during a winter, stripping seed and fruit crops as they go. Because most species take their food from the trees, they are little affected by weather, but Bramblings which feed on the ground, may be forced to leave areas of good seed crops when snow renders their food unavailable. Their winter distribution in particular years thus depends on both seed crops and snowfall (Jenni, 1987).

Winter densities Correlations between numbers of birds and size of fruit crops in wintering localities have been documented in several species of irruptive migrants, but mostly in northern parts of the wintering range (Table 20.1; Figure 20.7b). Further south, such correlations would be expected to be weak or non-existent, because the birds reach the more distant localities only in exceptional years. In some years, seed crops are available, but no birds from further north turn up to use them, having settled in good feeding areas already encountered. Conversely, irruptive migrants may turn up in remote areas in some years only to find their favoured foods are lacking (as shown, for example by the large numbers of Eurasian Jays which irrupted into Western Europe in 1983, a year almost devoid of acorns; John & Roskell, 1985).

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The Migration Ecology of Birds

FIGURE 20.9 Winter recoveries of Common Redpolls (Acanthis flammea) ringed in Finland. Circles After Zink & Bairlein (1995).

winter 1965/66, dots

winter 1972/73.

Changes in wintering areas: evidence from ringing Among the irruptive species studied, return to wintering sites in later years was even rarer than return to breeding sites (Table 20.2). Despite some very large numbers ringed (often in gardens), return rates of seed-eaters were mostly nil or less than 1% (but with Purple Finch at 5% in one area). Evidently, extremely few individuals of such species returned to the same localities in subsequent years. They showed little or no winter site fidelity, compared with regular migrants (Chapter 19). Among Eurasian species, most captures of the same individuals in successive winters lay at localities on the same migration axis, as mentioned above (including some more than 3000 km apart), but others included substantial east west displacements. Extreme examples included a Bohemian Waxwing found in Poland one winter and in Siberia in a later winter (6000 km apart), and several Common Redpolls present in western Europe in one winter and in China in another one (8350 km apart) (Table 20.3). Another Common Redpoll was recorded in North America in one winter and Eurasia in a later winter, having been ringed in Michigan and recovered near Okhotsk in Siberia, some 10,200 km to the northwest (Troy, 1983). All these birds are likely to have returned to the breeding range in the interim (though not necessarily to the same locality) and taken a markedly different migration direction in the second year. Further records of this type are shown in Box 20.1 and Table 20.3. North American ringing records also reveal transcontinental movements by boreal finches. Although most species breed across the entire continent in boreal forest, birds breeding in Alaska and other parts of the northwest tend to migrate east-southeast to winter in the eastern States, thereby avoiding the open land of the prairies. Birds from eastern Canada migrate south-southwest to also winter in the eastern States, the same region as the western birds (Brewer et al., 2000). Many of the records of individual Common Redpolls and Pine Siskins found on opposite sides of the continent in different winters (Troy, 1983; Kaufman, 1984) may therefore represent northwestern breeders that remain in the northwest in one year and migrate far along their east-southeast route in another year. However, some individuals have been recovered well south of the boreal forest on different sides of the continent in different winters, suggesting that they had taken different directions from the breeding range in different years. For example a Cedar Waxwing (Bombycilla cedrorum) ringed in California one April was recovered in Alabama 3000 km to the east 2 years later, and a Pine Siskin ringed in Quebec in one winter was recovered 3950 km to the southwest in California in a later winter (for other interesting ringing records from North American species see Table 20.3). Although they are extreme examples, dozens of individuals of various irruptive species have now been recorded at places 500 1500 km apart in different winters. The extent to which irruptive finches wander for food is well shown by the Evening Grosbeak in North America which breeds in conifer forests and moves southeast in autumn. This species feeds mainly on large, hard tree-fruits, but also visits garden feeders, a habit which makes it easy to catch. Over 14 winters, 17,000 individuals were ringed at a

TABLE 20.3 Examples of irruptive species in widely separated localities in different winters (December March).

Bohemian Waxwing (Bombycilla garrulus)

Ringed

Recovered

Distance (km)

Sweden

Siberia

3060

Sweden

Siberia

4070

Poland

Siberia

4500

Ukraine

Siberia

6125

Sweden

Russia

2980

Sweden

Russia

2280

Sweden

Russia

2910

Czechoslovakia

Russia

2282

Czechoslovakia

Kazakhstan

3826

Scotland

Russia

3714

Hungary

Russia

3158

Hungary

Russia

5138

Finland

Russia

4649

Brit. Columbia

N. Dakota

1360

Cedar Waxwing (Bombycilla cedrorum)

California

Alabama

3000

Brambling (Fringilla montifringilla)

Belgium

Turkey

3000

Britain

Greece

2500

Eurasian Siskin (Spinus spinus)

Pine Siskin (Spinus pinus)

Common Redpoll (Acanthis flammea)

Evening Grosbeak (Hesperiphona vespertina)

Eurasian Bullfinch (Pyrrhula pyrrhula)

Spotted Nutcracker (Nucifraga caryocatactes)

Belgium

Lebanon

3000

Sweden

Iran

3000

Ontario

California

3537

Quebec

California

3950

New York

Br. Columbia

3470

Tennessee

Br. Columbia

3780

Pennsylvania

Washington

2800

Sweden

Russia

1800

Sweden

Russia

2571

Czech Repub.

Russia

3024

Hungary

Siberia

3013

Belgium

China

8350a

Alaska

New Brunswick

5200

Quebec

Alaska

4850

New Jersey

Alberta

3250

Saskatchewan

Vermont

2550

New Jersey

Alberta

3250

New Jersey

Manitoba

2100

Alaska

Saskatchewan

2730

Michigan

East Siberia

10,200

Maryland

Alberta

3400

Virginia

Newfoundland

2200

Quebec

Georgia

1750

Finland

Siberia

1981

Finland

Siberia

2398

Finland

Siberia

2350

Czech Repub.

Russia

2282

These recoveries, which are selected as extreme examples from among many, refer mainly to birds that seemed to be on a different migration axis in different winters, being recovered in winter far to the east or west of where they were ringed in a previous winter. Other examples in Box 20.1. a This movement is matched by at least seven others between western Europe and China, but some involve October-November dates: from Norway to eastern China (6079 km), Finland to eastern China (5109 km), Belgium to China (7298 km), eastern China to Sweden (6480 km), eastern China to Norway (6578 km), eastern China to the Netherlands (7444 km), and eastern China to Denmark (6948 km) respectively, all 1 3 years later.

Source: Newton (2008), van der Spek (2022).

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The Migration Ecology of Birds

BOX 20.1 Other examples of individuals of irruptive species found in widely separated areas in different winters (December February). Bramblings (Fringilla montifringilla) ringed in Britain or Belgium in one winter were recovered as far east as Turkey and the Balkans in a later one, and Bramblings ringed in Switzerland in one winter were recovered at various localities from Ireland to Greece and Georgia in a later one (Jenni & Neuschulz, 1985). Similarly, many Bramblings that were ringed in Western Europe (Belgium Germany Switzerland) at 5 15 E in one winter (November February) were retrapped at a similar latitude at 60 70 E in a later winter (Zink & Bairlein, 1995). These various records at similar latitude involved up to 65 degrees of longitudinal displacement between one winter and another. Of 17 long-distance recoveries of Eurasian Bullfinches (Pyrrhula pyrrhula) ringed in Finland in winter, nine were at 550 1000 km and eight at more than 1000 km away in a later winter. Fifteen were between south-southwest (Hungary and Poland) and east (Russia) of the ringing site (including two at 1920 km and 2350 km east in Siberia), one was north-northeast and another north-northwest. Another three ringed in Sweden were found at 475 1491 km, between northeast to southeast in a later winter (Cramp & Perrins, 1994). These records involved longitudinal displacements of up to 45 degrees. Many Eurasian Siskins (Spinus spinus) were ringed in western Europe (Belgium, France or Iberia) in one winter and recovered as far east as Turkey and the Balkans in a later winter, at places up to 2500 km apart; one ringed in Belgium in April was re-caught about 3000 km to the southeast in Lebanon in the next November and another ringed in Sweden in October 1980 was recovered 3000 km to the southeast in Iran in January 1982 (Glutz von Blotzheim, 1997). These records involved longitudinal displacements of up to 35 degrees. Four Pine Siskins (Spinus pinus) in North America were caught at localities 2055 3780 km apart in different winters, involving 15 44 degrees of longitudinal displacement (Brewer et al., 2000). Common Redpolls (Acanthis flammea) provide some of the most extreme examples of individuals found in well-separated areas in different winters. In Eurasia, one bird ringed in Hungary in February 1978 was recovered 3300 km to the east-northeast in Sverdlovsk in west Siberia in March 1979 (Glutz von Blotzheim, 1997). Other striking records involve eight birds which moved between Western Europe and China, with individuals 5109 7444 km apart in different winters (Table 20.3). In North America, 12 Common Redpolls were caught at localities 1345 4836 km apart in different winters, involving 8 43 degrees of longitudinal displacement (Brewer et al., 2000). The most striking was a bird ringed in Michigan in one winter and recovered 10,200 km away in east Siberia in a later winter (Table 20.3). Five Evening Grosbeaks (Hesperiphona vespertina) were caught at localities 925 3402 km apart in different winters, involving 2 42 degrees of longitudinal displacement (Brewer et al., 2000). Many Redwings (Turdus iliacus) were ringed in Europe west of 10 E in one winter, and recovered east of 55 E in a later winter, at places more than 3000 km apart (Zink, 1981). Of Redwings ringed in winter in Britain, dozens have been recovered in subsequent winters as far east as Italy, Greece and Turkey, and some as far east as Israel and Iran, at localities up to 5000 km and up to 50 degrees of longitude apart (Milwright, 2002). Even birds from the same brood have been recovered in widely separated localities in the same winter. Many Fieldfares (Turdus pilaris) were found as far apart as Ireland and Italy, England and Turkey, or as Switzerland and Georgia, in different winters, at localities 2000 3000 km and up to 35 degrees of longitude apart (Zink, 1981; Milwright, in Wernham et al., 2002). Again, birds from the same brood were recovered in widely separated areas in the same winter. The furthest recovery in different winters was a bird ringed in France in December 1961 and recovered in February 1963 some 6027 km away in Osinnike, Russia, a longitudinal displacement of 85 degrees (van der Spek, 2022). Many Bohemian Waxwngs (Bombicilla garrulous) were recorded in Eurasia west of 20 E in one winter and 45 65 E in another, at places more than 2000 km apart (Zink, 1981). These recoveries involved some in which longitudinal displacements exceeded 50 degrees. One ringed in Finnish Lapland in March 2003 was recovered 4649 km away in Irkutsk, Russia in April 2004, one ringed in Sweden in February 1996 was recovered 4231 km away in Novosibirsk, Russia in March 1997, and another ringed in Sweden in March 1996 was recovered 3132 km distant in Tyumen, Russia in February 1997 (van der Spek, 2022). Other Bohemian Waxwings have been found at the same place at intervals of one, two or three years, in successive irruptions. The longest movement yet recorded for the species involved a bird ringed in December 1967 in Hungary and recovered 7883 km to the east in the Amur region of Russia in the following October, a longitudinal shift of 102 degrees (van der Spek, 2022).

site in Pennsylvania. Of these, only 48 (0.003%) were recovered in the same place in subsequent winters, yet 451 others were scattered among 17 American States and four 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 four Provinces (D. H. Speirs, in Newton, 1972). These recoveries show how widely individual grosbeaks range, and how weak is their tendency to return to the same place in later years.

Irruptive migrants: boreal seed-eaters Chapter | 20

421

TABLE 20.4 Number of Common Redpolls (Acanthis flammea) ringed in winter in North America that were recovered in successive years after ringing. Years until recovery 1

2

3

4

5

Northern region

34

26

4

2

1

Southern region

6

28

0

5

2

North of the Canadian border, recoveries declined steadily with time, as expected from mortality. South of the Canadian border, recoveries peaked every second year as expected from the biennial pattern in migration. From Troy (1983).

Common Redpolls in North America showed another interesting pattern, associated with the biennial cropping of their food plants (Table 20.4; Troy, 1983). Most birds were ringed at garden feeders, and in the northern parts of the winter range (north of the Canadian border), recoveries fell off steadily from 1 to 5 years after banding, as expected from mortality. However, in the southern parts (south of the Canadian border), recoveries peaked 2 years after banding, with a minor peak 4 years after, as expected from the biennial migration pattern. Most recoveries were of birds caught at different sites in different winters, some more than 2000 km apart. But some were found at the same sites in successive winters (mainly in the north) or two winters later (mainly in the south). Irruptive species also show greater turnover at particular sites within a winter than do non-irruptive ones (for Brambling, see Browne & Mead, 2003; for Eurasian Siskin, see Senar et al., 1992), and some individuals may be continually on the move through the winter.

Breeding in migration and wintering areas It is not only the autumn distances that vary from year to year in irruptive seed-eaters, but also the following spring distances. The Common Redpoll curtails its migration by up to several hundred kilometres to breed in southern Fennoscandia in some years when the spruce crop there is good. Once the seeds have fallen, the birds move north with their young to their usual birch-scrub breeding areas, where they raise another brood. Such movements have not been proved by ringing but have been inferred from simultaneous changes in the populations of the two regions and, in particular, from the late arrival in these years of birds in the birch areas with their free-flying young. Such events have been documented in at least seven different years (Peiponen, 1967; Hilde´n, 1969; Antikainen et al., 1980; Go¨tmark, 1982). In years with little or no spruce seed, the birds bred only in the birch, raising a single brood. Similarly in Eurasian Siskins, adults and recently fledged juveniles were in several years seen migrating northeast in May July over the Courland Spit in the southern Baltic (Payevsky, 1994). Some of the adults were clearly paired at the time, and many trapped females had a shrunken brood patch, signifying a recent nesting attempt. The first females with brood patches usually appeared at this site towards the end of April. In the years 1984 87, some 23% 91% of adult females trapped in late April July had brood patches, as did 35% 86% of yearling females (total females caught 5 1230). One juvenile caught in June 1959 had been ringed 25 days earlier, 760 km to the southwest, in Germany. While it could not be proved that the adults among these Siskins went on to breed elsewhere in the same year, they clearly had enough time to do so. Some other irruptive species have been recorded breeding well to the south of their usual range in certain years, sometimes in their wintering areas following an invasion. Examples include Brambling, Eurasian Bullfinch, Lesser Redpoll, Common Redpoll, Bohemian Waxwing and Coal Tit (Periparus ater) (Newton, 2008; Fox et al., 2009), in addition to the crossbills and nutcrackers discussed later.

ONCE-YEARLY MIGRANTS Crossbills Perhaps the most famous of irruptive migrants in the northern hemisphere are the crossbills, which feed year-round almost entirely on conifer seeds obtained directly from the cones (Newton, 1972, 2006b). Three main boreal species are recognized, the Red (Common) Crossbill and the Two-barred (White-winged) Crossbill which occur in suitable coniferous habitat across North America and Eurasia, and the Parrot Crossbill (Loxia pytyopsittacus) which occurs in pine forests of northern Europe. These species differ in body and bill size and specialize on different types of

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The Migration Ecology of Birds

BOX 20.2 Different types of Red (Common) Crossbills. In Europe, large-billed races of Red Crossbills (Loxia curvirostra) occur in the southern parts of the range, in the isolated mountain pine forests of (1) southern Spain and the Balearic Islands (Loxia c. balearica), (2) southern Italy, Sicily and Northwest Africa (Loxia c. poliogyna), (3) the southern Balkans, Greece and Cyprus (Loxia c. guillemardi), (4) Corsica (Loxia c. corsicana), (5) the Crimea (Loxia c. mariae) and (6) Scotland (Loxia c. scotica). The first two of these large-billed subspecies (1 and 2) feed mainly on seeds of Aleppo Pine (Pinus halapensis), the next two (3 and 4) mainly on Black Pine (Pinus nigra), the Crimean Crossbill (5) mainly on Black Pine and Scots Pine (Pinus sylvestris), and the Scottish Crossbill (6) mainly on Scots Pine. In addition to these taxonomically recognized types, over the last 30 years, it has emerged that other Common (Red) Crossbills exist in many different forms across their Holarctic range, differing in body size, bill shape and call notes. The calls are distinguishable only to the practiced ear or from sonograms. About 18 types have so far been described in Europe and ten in North America. Although more than one type may occur together in the same invasion area, the different types tend to keep apart, often concentrating on different types of conifers, and, despite occasional cases of mixed pairs (Benkman, 1993), they usually mate with their own kind. Each type apparently depends on at least one key conifer species, defined as one which normally produces cones somewhere in its range every year, holds its seeds at least until late winter, and for one reason or another does not get totally eaten by other seed-eaters (Benkman, 1993). Nevertheless, all crossbill types are able to feed from other conifer species, albeit with lower rates of seed intake (as measured on both wild and captive birds). Several types have been recorded in the same invasion areas, including at least three types simultaneously in Britain and six simultaneously in northern Wisconsin (Summers et al., 2002; Brady et al., 2019). On those parts of the DNA examined, little or no difference could be found between different types of crossbills, and the differences in mtDNA between Common and White-winged Crossbills were also small (Groth, 1991, 1993; Questiau et al., 1999; Piertney et al., 2001). For further details of Common Crossbills see Groth, 1993; Benkman & Young, 2020; Marquiss & Rae, 1994, 2002; Summers et al., 1996, 2002. Two-barred (White-winged) Crossbills (Loxia leucoptera), which have finer bills than most types of Red Crossbill, appear to show less geographical variation, but the North American race (L. l. leucoptera) has a smaller and narrower bill than the Eurasian (Loxia l. bifasciata), and an even larger billed, pine-feeding form of this species (Loxia l. megaphaga) occurs isolated on the island of Hispaniola, where it specializes on the seeds of the West Indian Pine (Pinus occidentalis). Such geographical variations in crossbills imply that, despite their widespread wanderings, they are sufficiently faithful to particular regions to have become adapted to the conifers growing there.

conifers, the Two-barred mainly on soft-coned species, the Red Crossbill mainly on medium-coned species, and the Parrot Crossbill on the very hard thick-scaled cones of Scots Pine (Pinus sylvestris). In addition, Red Crossbills also vary in body and bill size from region to region across their extensive range, in association with the particular conifer species that grow there (Box 20.2). These regional types also vary in call-notes, and during irruptions several call types have been recorded simultaneously in the same invasion areas (Summers et al., 2002; Brady et al., 2019). Where several conifer species occur in the same region, crossbills can switch from one species to another through the season, according to the different patterns of cone ripening and seed fall (Benkman, 1987). Both Red and Twobarred Crossbills can breed in any month of the year, depending on the species of conifers available. However, most breeding occurs in late summer autumn as fresh cones mature or in late winter spring as they open to release their seeds (Newton, 1972; Benkman, 1987; Benkman, 2020).

Annual cycle Over much of Europe, Red Crossbills depend mainly on Norway Spruce (P. abies). Each year, new cones begin to form in May, providing food for Crossbills from about June into the winter, and particularly from January on, when the cones begin to open, making seed extraction easier. By late May, when most cones and seeds have fallen, they are lost to Crossbills, which then switch to alternative foods, and eventually to the new Norway Spruce crop (Marquiss & Rae, 1994, 2002). In most years, Red Crossbills remain within the boreal forest, concentrating each year in areas where spruce cones are plentiful. In particular areas, their breeding numbers tend to fluctuate on roughly 2 4 year cycles, in line with the local cone crops (Figure 20.10; Reinikainen, 1937; Formosov, 1960; Thies, 1996; Fo¨rschler et al., 2006). The birds have one major period of movement within the summer of each year, as they leave areas where the previous year’s spruce crop was good but coming to an end, and concentrate in areas where the current year’s crop is good but forming. Between these times, some birds concentrate temporarily in Scots Pine areas. It is only at this period of transition, in summer, that Red Crossbills in Europe have been found with substantial fat reserves, presumably deposited as

5 4 3 2 1 0 40 30 20

423

40

30 Crossbill pairs

Crossbill pairs

Spruce crop

Irruptive migrants: boreal seed-eaters Chapter | 20

20

10

10 0 1927 28 29 30 31 32 33 34 35 36 1937 Year

0 0

1

2 3 Spruce crop

4

5

FIGURE 20.10 Relationship between the population density of the Red Crossbill (Loxia curvirostra) and the cone crop of Norway Spruce (Picea abies) in Finland (n 5 7, rs 5 0.826, P 5 .028). Crossbills in number of pairs per 120 km transect; spruce crop ranked in five categories. For similar patterns in other areas, see Thies, 1996; Fo¨rschler et al. (2006). From Reinikainen (1937).

‘migratory fat’ (Newton, 1972, 2006b; Marquiss & Rae, 2002). However, lesser movements occur at other times of year in relation to local changes in food availability, as seeds are shed or consumed, or as cones open and close. In a good cone year for Norway Spruce, Crossbills may begin nesting in autumn, within weeks after arriving in a new area, and may continue for as long as the food holds out. A pair may start a second nest while still feeding young from the first, and young birds may begin breeding while they themselves are still in juvenile plumage (Berthold & Gwinner, 1978; Jardine, 1994; Hahn et al., 1997). The main breeding period, however, is in January April, when the cones begin to open, making seeds more readily available. As seeds and cones fall through May, breeding in Norway Spruce areas comes to an end and the birds move on.

Irruptions In some years, apparently when high populations coincide with poor Norway Spruce crops over wide areas, Red Crossbills leave the boreal forest and move south-westward through Europe, appearing in many places that lack suitable conifer habitat. For example between 1880 and 2000, Red Crossbills irrupted in Britain on at least 40 occasions, at intervals of 1 9 years (Newton, 1972, 2006b). Each time, the birds appeared sometime during late May October, but mainly in June July. The fact that trapped migrants differed slightly in bill dimensions from one irruption to another (Davis, 1964; Herremans, 1988; Edelaar & Terpstra, 2004) suggested that not all movements originated from the same region. Most of these irruptions included small numbers of other crossbill species (L. pytyopsittacus or L. leucoptera) (Newton, 1972). Further evidence that not all irruptions originated in the same region came from museum skins collected in Britain, which contained Crossbills from 30 different irruption years between 1866 and 2009, enabling feathers from these skins to be analyzed for their isotope levels (Marquiss et al., 2012). In 17 of these years, feathers from these birds contained relatively high levels of deuterium, suggesting origins somewhere between northern Scandinavia and north-western Russia. In these years, the birds also arrived in Britain early, in June and July. In 10 other irruption years, medium deuterium levels suggested origins further east, in northern Russia east of about 40 E. In three of the 30 years, the deuterium values were lower still, suggesting an origin in Siberia east of the Urals, and these birds arrived in late July, August and September. Hence, in years when migrant Crossbills had lower deuterium values, they tended to arrive later in the migration season, which was consistent with their having travelled further. In the remaining three irruption years, a wide range of deuterium values suggested that birds had come from more than one of these regions. Other work has shown that some irruptions to Britain and elsewhere contain birds of more than one bill-size and call type, and up to three types have occurred in the same area in the same year (Summers et al., 2002), further implying more than one source area. Irruptive movements occur at about the same time of year as normal annual movements but are more directional (towards the southwest) and cover much longer distances (with extremes at more than 5000 km). These differences could be explained by the birds achieving a higher migratory state in irruption years. A similar change occurs in normal migrants as they switch in late summer from random dispersal movements to directional long-distance migration (for Barn Swallow (Hirundo rustica), see Ormerod, 1991; for Willow Warbler (Phylloscopus trochilus), see Norman & Norman, 1985).

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The Migration Ecology of Birds

Once on the move, some Crossbills can reach the extreme southwest of Europe, some 5000 km from their boreal breeding range. Thousands of irrupting Crossbills have been ringed at trapping sites in central Europe, giving hundreds of recoveries (Newton, 1972, 2006b; Payevsky, 1971; Weber, 1972; Schloss, 1984). Almost all recoveries within the current cone year (June May) were to the south and west (mostly southwest) of the ringing site, while many of those in later years were far to the northeast, in the boreal zone of northern Russia, almost all in a region west of the Urals (Figure 20.11; Newton, 2006c). Overall, at least 29 adults caught on migration during different invasions through central Europe were recovered back in the boreal forest to the northeast, 1 3 years later. None was found in northern boreal forest within the same spruce year as it was ringed in central Europe (Newton, 2006c). If the outward movement was stimulated by food shortage, birds would gain no advantage in returning to their area of origin before the next year’s crop was ready. In addition to ring recoveries, observational evidence for eastward or north-eastward return movements in the summers of non-invasion years is available from several localities (Newton, 2006c). The return movement is much less conspicuous than the outward one, perhaps because it involves smaller numbers and occurs in more than 1 year. The main axis of outward migration is clearly northeast southwest, as in most other seed-eaters, but unlike them, Crossbills remained for a year or more before returning.

FIGURE 20.11 Recoveries of Red Crossbills (Loxia curvirostra) ringed at migration time in June October of invasion years in Germany and recovered in the following year (filled circles) and later years (open circles), respectively. All the 83 birds recovered in the following year (to 31 May) were in the invasion areas of western Europe, whereas 22 out of 44 birds recovered in later years were far to the northeast, in the boreal zone of northern Russia (significance of difference in distribution, chi2 5 34.2, P , .001). Only movements more than 50 km are included. These recoveries indicate that some irrupting Crossbills return to their region of origin in a later year. Map compiled from the recoveries listed in Schloss (1984), which include recoveries from the invasions of 1930, 1935, 1953, 1956, 1959, 1962, 1963, 1972, 1977 and 1979, although two-thirds of all recoveries in Russia probably stem from the invasion of 1963. Schloss (1984) lists nine other recoveries in northern Russia of birds ringed in Germany in non-invasion years or outside the migration season, some of which are in Figure 20.11. In addition to the records shown, another Red Crossbill ringed at Falsterbo in Sweden on August 12, 1963 was recovered in a later year at Gayny in northern Russia at 60 18’N, 54 18’E (Roos, 1984), and one ringed in Northamptonshire in England on June 2, 1991 was recovered 1958 km east-northeast on April 14, 1998 in Pskov in northern Russia (58 16’N, 28 54’E) (Clark et al., 2000). For other recoveries of birds ringed in Switzerland, see Newton (1972).

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If irrupting Crossbills had remained in the regular range, they would almost certainly have starved, but by moving out, a proportion survived to return in a later year, and may even have bred in the interim. Hence, the adaptive value of periodic mass emigration is presumably the same as in regular annual migration, namely the avoidance of starvation. Those irrupting birds that find areas of seeding conifers often remain to breed. Mostly they move away after one breeding season, but some irruptions have resulted in the longer-term colonization of new areas (e.g., pine plantations in southern Britain).

Change of breeding localities Ring recoveries also imply that individual Red Crossbills have bred in widely separated areas in different years, taking the main breeding season in Norway Spruce areas as January April inclusive. Movements of Red Crossbills that were ringed in January April 1 year and recovered in the same period in a later year are shown in Figure 20.12. They include 10 recoveries of birds ringed as adults (representing breeding dispersal) and four birds ringed as juveniles and recovered as adults (representing natal dispersal). These various birds were reported up to 4 years after ringing; their successive capture sites were between 28 and 3170 km apart and included eight birds that had moved more than 2000 km. These great distances separating the breeding areas of different years are thoroughly in line with the long irruptive movements of the species. None of these birds was reported as nesting at the time of ringing or recovery, but they were all within the usual breeding season from within the recorded breeding range. Moreover, no records have emerged of individuals in the same spruce locality in successive spruce years, which is consistent with good crops seldom occurring in the same locality 2 years running. This contrasts with the situation in Pyrenean Mountain Pine (Pinus uncinata) forests, where seed crops are relatively stable from year to year, and where Red Crossbills are more sedentary, with many individuals trapped in the

1000 km

FIGURE 20.12 Ringing and recovery sites of Red Crossbills (Loxia curvirostra) that were both ringed and recovered in different breeding seasons (taken as January April in areas of Norway Spruce (Picea abies)). Continuous lines ringed as adults (representing breeding dispersal); dashed lines ringed as juveniles (representing natal dispersal). Compiled mainly from information in Schloss (1984); also from Danish Ringing Report (1931 34), Swedish Ringing Report (1965), Swiss Ring recoveries provided by Dr. L. Jenni, and Russian ring recoveries provided by Dr K. Litvin. Details listed in Newton (2006c).

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The Migration Ecology of Birds

same place in successive years (Senar et al., 1993). These findings from a pine area again imply that the frequent movements in spruce areas are driven by the huge annual fluctuations in regional crop sizes. Similarly, colour-marked Scottish Crossbills (Loxia c. scotica) were re-sighted in the same pine areas in successive years or had moved over distances of at most a few tens of kilometres (Marquiss & Rae, 2002). The same presumably holds in other pine areas in Europe, most of which hold local races of large-billed crossbills (Box 20.2). The return of crossbills after an outward movement is analogous to the ‘homing’ of other migrants, but unlike most other species, crossbills sometimes breed before returning. This means that, if they are to reach their ancestral home, young raised in invasion areas have to make their first migration in a direction opposite to the first migration of their parents and all other individuals raised on the regular range. Several ring recoveries of birds from Germany to northern Russia, and another from south Sweden to northern Russia, are consistent with such a movement. All these birds were hatched in breeding seasons following invasions. Perhaps the juveniles simply travelled with returning adults (as reported by Weber, 1972). An alternative possibility is that the directional preferences of Crossbills differ according to geographical location, with birds leaving northern Russia moving mainly southwest, and those leaving central Europe moving mainly northeast. In one respect, this would be no different from other migrants, which head in one direction from their breeding areas and in the opposite direction from their non-breeding areas. But it differs in that Red Crossbills would need to take different directions at the same time of year, and both times after breeding, rather than at markedly different seasons, as in twice-yearly migrants. To judge from recent east west displacement experiments on other bird species (Chapter 10), this might be expected, but it would be interesting to test at migration time the directional preferences of young Crossbills raised in the two regions, and whether they relate to the local magnetic field.

Other Eurasian crossbills Where the Two-barred Crossbill feeds primarily on larch, it may not suffer such extreme fluctuations in food supply as the spruce-feeding Red Crossbill. This is because larch cones remain on the tree with some of their seeds for 2 3 years, so poor crops can be buffered by carry-over from previous years. This may explain why this species is much less irruptive in western Eurasia than the Red Crossbill, and appears in only very small numbers south of the boreal zone, mostly along with Red Crossbills. Irruptions into Scandinavia occur during cone failures in larch further east in Russia. They tend to occur from late summer, as new cones ripen, but at longer intervals than the 2 4 years recorded in North America (Bock & Lepthien, 1976; Larson & Tombre, 1989). Two-barred Crossbills have come to Britain mainly in the same years as Red Crossbills, though much less frequently (Newton, 1972), with larger numbers than usual recorded in 1889, 1956, 1979, 1985 87, 1990 and 2008 (Cramp & Perrins, 1994; Harrop & Fray, 2009). Adding to a small population in the native pinewoods of northeast Scotland, small numbers of immigrant Parrot Crossbills also appear in Britain, mainly in the same years as Red Crossbills. Relatively large invasions occurred in 1962, 1982, 1990, 2013 and 2017. Unlike the other European crossbills, Parrot Crossbills move mainly in the autumn, in keeping with the different phenology of their food plant, as the seeds in new pine cones are not normally developed much before September. One individual that was ringed as a nestling in Norway was recovered in the breeding season 3 years later 340 km to the east, in Sweden (Norwegian Ringing Report, 1966 67). Like other crossbills, Parrot Crossbills may nest in peripheral invasion areas for a year or two, before disappearing, as recorded occasionally in Denmark, southern Britain and the Netherlands.

North American crossbills North America has a far greater variety of conifer species than Europe, and many seem to crop synchronously over wide areas. It also has a wide range of Red (Common) Crossbills, at least 10 different types having been described, each occurring in mainly different regions from the others and adapted to the conifer species that grow there, particularly those that hold their seeds at times when others do not (Box 20.2). The different crossbill types are distinguished not only by their body and bill sizes but also by their slightly different calls, and are numbered 1 10 (Groth, 1993; Benkman & Young, 2020). At least six call types were found in an invasion across northern Wisconsin in 2017 (Brady et al., 2019). Most arrived in summer autumn, nested from mid-winter through into spring, and departed by midsummer 2018, as cones shed their seeds. Like European conifers, North American species vary in the dates their cones mature, and in the dates the cones fall or shed their seeds. Hence, while the main period of movement in most crossbills occurs in May July, as in Europe, when new crops are forming, there can also be substantial movements in autumn winter, as cones of early shedding species become depleted of seeds. This in turn depends not just on the species of conifer but also on the initial crop

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size and the weather, as cones open more in warmth. Thus big movements can also occur in September November if warmth leads to rapid seed shedding, but in different weather, movements are delayed to varying extents, as seeds are retained for longer. Under optimal conditions, with favoured conifer species producing large cone crops, enough seeds are retained to sustain crossbills through the winter into spring when warmth causes the final seeds to fall and the birds to search for areas where new crops are forming. Depending on conditions, particular populations might thus make 1 3 movements per year (Benkman & Young, 2020). However, the main periods of fat deposition (indicative of major movements) occur in late spring in crossbill types that depend on soft-coned spruces, firs and hemlocks, and in autumn in pine feeding types (Cornelius et al., 2021). Most nesting in North America occurs during two main periods: July September when seed crops are developing and maturing and January April when ample seed remains in the cones from the previous year (Benkman & Young, 2020). Poor crops in the northwest of North America stimulate irruptive flights heading east-southeast in the boreal zone, covering 4000 km or more. In eastern North America, White-winged Crossbills often arrive in areas of Tamarack (Larix laricina) and White Spruce (Picea glauca) in late May July, as the new cones are forming, and breed on the strength of the new crop (Benkman, 1987; Cornelius & Hahn, 2012). When this seed has fallen, usually by November, they switch to Black Spruce (Picea mariana), whose seeds can remain available in the cones until the following summer. But if the Black Spruce crop is poor, White-winged Crossbills then irrupt into regions south of the usual range. This movement occurs in October November, coinciding with seed fall from Tamarack and White Spruce. In the same region, Red Crossbills (with their larger bills) can exploit all the conifers eaten by White-winged Crossbills but can also tackle pines efficiently, so they have a greater range of food-plants available to them. Only if pine cones are scarce do Red Crossbills also emigrate, mostly from November onwards (Benkman, 1987). During autumn, seed availability or consumption rates appear to determine whether crossbills remain in an area or emigrate. For example on seven occasions when seed consumption rates in October November were high ( . 0.4 mg kernel/s), reflecting abundant seed, White-winged Crossbills stayed, whereas on three occasions when seed consumption rates were lower, indicating fewer seeds, they mostly left (Benkman, 1987, 2020). They also departed earlier in autumn when seed was scarcer (Benkman & Young, 2020). Some individual ringed Red Crossbills in North America have been recorded at the same site two years later, but others were recovered more than 2000 km away (Adkisson, 1996). Of particular interest are two birds, recorded in the same months of different years. One bird was recorded in May of 1991 and 1992 at localities 1409 km apart, and another was recorded in August 1990 and 1993 at localities 521 km apart. Without knowledge of local breeding seasons, it is hard to interpret these movements, but they would not be expected in a regular migrant moving annually between fixed breeding and wintering areas.

Nutcrackers Other irruptive seed-eaters include the Spotted Nutcracker (Nucifraga caryocatactes) of Eurasia and the Clark’s Nutcracker (Nucifraga columbiana) of western North America. These species feed primarily on the seeds of various large-seeded pines, which they cache in the ground in late summer to eat during the ensuing winter into the next breeding season. Like crossbills, they make one major annual movement, in July September (as the new cones form), with occasional irruptions outside the usual range. Having settled in appropriate areas, their strategy of living mainly off food stores ideally requires continued residence until the next crop is ready. Like Crossbills, nutcrackers breed early in the year and can rear their young entirely (or almost entirely) on seeds. Their overwinter survival and breeding success vary from year to year in line with the size of seed crops (Lanner, 1996). The Spotted Nutcracker of Eurasia has several subspecies, each occupying a different part of the range and depending on different conifer species. The most widespread type is the slender-billed (Nucifraga c. macrorhynchos), which occurs over most of Siberia and depends on the seeds of the Siberian Stone Pine (Pinus sibirica) and, further east, the Korean Stone Pine (Pinus koraiensis). In north-western Europe, where large-seeded conifers are lacking, the thickbilled (N. c. caryocatactes) lives in mixed deciduous coniferous areas, but depends in winter mainly on Hazel (Corylus avellina) nuts, which it caches in late summer in the same way that other subspecies cache pine seeds. Further south, in the Alps, it also uses the hard-shelled Arolla Pine (Pinus cembra) seeds. All these nutcrackers adjust to annual variation in local cone crops by re-distributing themselves each year within the regular range (mainly in July September) and by exploiting alternative small-seeded conifers when their main food is scarce. However, in years when major food sources are scarce over wide areas, the birds leave their regular range in large numbers and live as best they can off any suitable plant or animal material they can find.

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The Siberian (N. c. macrorhynchos) performs the most spectacular irruptions, reaching in some years as far as Western Europe, on journeys of several thousand kilometres. Thirty-one irruptions into Europe were recorded in the 250 years from 1750, at intervals of 1 33 (mean 8) years (Mayaud, 1947; Cramp & Perrins, 1994). In the 20th century alone, the figures were 13 irruptions, at intervals of 2 16 years (mean 7.7). Only in the largest irruption of 1968, which started as far east as Lake Baikal, did large numbers of birds reach Britain, a journey exceeding 7000 km (Hollyer, 1970), with smaller numbers occurring in at least 5 other years. Again, not all invasions necessarily originated from the same region (Formosov, 1933). In such invasions, surviving birds normally stay until the next year, like crossbills, but in 1968 some nutcrackers that reached Western Europe reversed their migration and returned homeward in the same autumn, but possibly not as far as their region of origin. A partial return eastward movement within weeks of the westward late-summer exodus was recorded at Lake Ladoga in Russia (Noskov et al., 2005). Overall, 16 birds ringed mainly in Fennoscandia (outside the regular range), and chiefly in the invasions of 1968 and 1995, were later recovered some 2016 4797 km to the east (within the breeding range). These recoveries confirmed that, after their irruptions into Western Europe, birds returned successfully to the regular breeding range where they were recovered up to 10 years later (including four from 1968 within four months after ringing; van der Spek, 2022). Like crossbills, some nutcrackers can remain in invasion areas for up to a year, breeding if food supplies permit. Small longer-term populations have been established after invasions in areas where suitable food trees had been planted where none existed before (Lanner, 1996). Following the invasion of 1968, colonies of Slender-billed Nutcrackers (N. c. macrorhynchos) from Siberia became established in Finland and Belgium in areas where Stone Pines (Pinus sibirica) and (P. cembra) had been planted (Cramp & Perrins, 1994); and after the invasion of 1977, similar colonies were established in Sweden (Elmberg & Mo, 1984). Those Thick-billed Nutcrackers (N. c. caryocatactes) that live in northern Europe move shorter distances to the south, while those in the mountains of central Europe move mainly to adjacent lower ground in years of extreme food shortage. Big movements of central and northern European birds do not usually coincide with one another, nor with the bigger movements into Europe of Siberian birds (Mattes & Jenni, 1984). In North America, Clark’s Nutcracker breeds in the western mountains, but not in the northern boreal forest which lacks large-seeded pines. Like the Eurasian species, it depends on different types of conifers in different parts of its range, moving around each summer and autumn (mostly September) to areas where new crops are good (Lanner, 1996; Tomback, 2020). It also moves altitudinally to exploit conifer species growing at different elevations. In years of widespread crop failure that follow good crops, the birds extend mainly to lower ground nearby, in the deserts, plains and coastal areas, but some have been recorded far to the east, more than half-way across the continent (Fisher & Myres, 1980). Invasions into the lowlands of California and other southwestern states occurred in 1898, 1919, 1935, 1950, 1955 and 1961, at intervals of 5 21 years (mean 12.6 years) (Davis & Williams, 1957, 1964). At the northern end of the range, in Alberta, invasions of low ground during 1904 76 occurred in 1919, 1960, 1965, 1972 and 1976; that is in mainly different years from those in the southwestern States (Fisher & Myres, 1980). Like some other irruptive migrants, Clark’s Nutcrackers sometimes breed in invasion areas before withdrawing to their regular range (Tomback, 2020). In North America, other corvids also harvest and store pine seeds, namely the Pinyon Jay (Gymnorhinus cyanocephalus), Steller’s Jay (Cyanocitta stelleri) and Scrub Jay (Aphelocoma californica), but none of these species is so heavily dependent on pine seeds as nutcrackers, and none performs obvious irruptive migrations.

OVERVIEW OF SEED-EATERS Coping with boom-and-bust By changing breeding and wintering areas between years, irruptive seed-eaters lessen the effects of the massive food shortages they would experience if they occupied the same areas every year. Nevertheless, they may still be exposed to hugely fluctuating food supplies, as reflected in their reproductive rates. For example in an area of northern Sweden, Bramblings bred every year over a 19-year period, but in greatly varying numbers, depending on food supply, mainly (E. autumnata) caterpillars (Lindstro¨m et al., 2005). Post-breeding juvenile-to-adult ratios varied more than 10-fold over this period, from 3.54 in good Epirrita years to 0.33 in poor ones. Common Redpolls and Eurasian Siskins can breed for more than twice as long in good spruce years than in other years (giving time for 2 3 broods instead of 1 2) and could thereby double their annual production of young (Peiponen, 1967; Shaw, 1990). In good seed years, both species begin nesting as early as March, when conifer cones open. After these seeds have fallen, the birds raise another one or two broods on the fresh seeds of herbaceous plants which form in May July, depending on area, or (in the case

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of Redpolls on the tundra) on the seeds of Dwarf Birch (Betula nana) left from the previous year. In poor spruce years, only the later broods are reared. Among Red Crossbills, the annual variations may be even greater, for in mixed conifer areas in which different tree species release their seeds in widely different months, individual Crossbills could in theory breed for more than 9 months each year, raising brood after brood (Newton, 1972). But in areas containing only Norway Spruce (P. abies), individuals breed for no more than half this time or, in poor cone years, not at all. The fact that juveniles often predominate among irruptive species caught on migration has been taken as evidence that irruptions follow good breeding seasons (Lack, 1954). Care is needed, however, because in such facultative migrants juveniles often leave the breeding areas in greater proportion and earlier than adults and move greater distances. Nevertheless, when most of the migrants in particular years are adults, this probably reliably indicates a poor breeding season. This situation was recorded, for example among Red Crossbills in 1963, when young formed only 6%, 8%, 31% and 37% of the birds caught at four localities in Western Europe (Newton, 1972). It compares with up to 88% of juveniles recorded in other irruption years. Similarly, study of Spotted Nutcracker skins in museums suggested that the movements of 1864, 1911 and 1968 consisted entirely of adults, and about half the adult females collected in the 1968 irruption had never laid eggs. In contrast, from the irruptions of 1885, 1913 and 1954 only juveniles were collected in Western Europe, while in other irruptions both age-groups were represented (Cramp & Perrins, 1994).

Regularity in irruptions Because the cropping patterns of many northern tree species are more regular than random, they would be expected to impart some regularity to large-scale emigration among seed-eaters. In addition to the biennial pattern shown by several species in North America, a 7-year rhythm emerged in the influxes of Two-barred Crossbills in autumn to Finland during 1960 88 (Larson & Tombre, 1989), a 5 6 year rhythm in the irruptions of Pine Grosbeaks to southeastern Canada during 1889 1936 (Speirs, 1939), and a 4 5 year rhythm in the movements of Eurasian Jays in the Swabian Alps of central Europe during 1954 73 (Gatter, 1974). Such regularity reflects patterns in tree-seed production but may not necessarily persist over longer periods, and in many areas irruptions seem irregular. Irruptions of seed-eaters have been studied chiefly in the reception areas, where the degree of regularity probably varies with distance from the breeding range. While every irruption might reach the nearest areas, only the largest would reach the furthest areas, as illustrated above for nutcrackers and others. Sometimes, invasions come not just in 1 year but in two or more successive years, hence the term ‘echo flights’. However, these might involve birds from different parts of the breeding range, obscuring any regularity there might be in more local breeding populations. For example, most invasions of the Pine Grosbeak into Germany came from the north, and the birds belonged to the European subspecies, but in 1892 a larger subspecies invaded Siberia (Grote, 1937). Similarly, invasions of Redpolls into central Europe in 1985 and 1986 were mainly long-billed ‘holboellii’ types and hence probably came from within the range of the Larch (Larix dahaurica) in Siberia (Two-barred and Red Crossbills also came from this area in 1985). Moreover, different Red Crossbill invasions to Western Europe have involved birds with different bill sizes or isotope levels, as mentioned above, indicating different areas of origin, and in more recent years birds of more than one call-type have appeared in the same invasion areas.

Directional preferences In Western Europe, the usual migration direction of most irruptive species is southwest, a direction in which birds could usually be expected to find suitable habitat and food supplies, especially in montane conifer forests. Birds from further east, however, tend to have a stronger westward component in their movements, which brings them to Western Europe, either within the boreal forest itself or further south into the temperate region. They thereby largely avoid the dry steppe and desert lands of Asia in which their survival chances would presumably be low. Such patterns led Sva¨rdson (1957) to suggest that some boreal birds performed regular pendulum movements, moving first west and then east across the boreal forest of Eurasia. Evidence for east west shifts also comes from ring recoveries of Common Redpolls, some of which showed easterly autumn movements within the boreal zone. Of two ringed in northern Norway in August 1977, one was reported 3091 km due east near Novosibirsk 2 months later on October 20, 1977, and another was reported 2753 km east-southeast near Chaklovo on March 12, 1978. In the 1965 irruption, some birds ringed in Finland and reached the edge of the Altai in central Asia, over distances up to 3573 km. Other recoveries relate to Redpolls ringed in Western Europe in one winter and recovered as far east as China in a later winter (Box 20.1; Table 20.3), but these could relate to birds from a particular breeding area migrating in different directions each year.

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In North America, too, there is a strong west east component in the movements of some irruptive species. Red and White-winged Crossbills, Evening Grosbeaks, Common Redpolls and Pine Siskins from the northwest of the continent tend to move east-southeast in autumn, as mentioned earlier, while Purple Finches move first east-southeast to the Great Lakes region, then veer south towards Texas and Louisiana (Benkman, 1987; Houston & Houston, 1998; Brewer et al., 2000). By these movements, all species avoid the desert and prairie areas of the mid-west and remain largely in forested areas that provide their food. Recent research on tree-seed crops has suggested a basis for east west movements of seed-eaters across the northern continents, as climatic conditions are such as to favour large tree-crops in east or west in different years. In North America, as in Europe, irruptive migrations can follow two directional axes, east west and north south. According to Strong et al. (2015), climatic conditions across the North American boreal region tend to form dipoles, where poor summer conditions (which influence tree-cropping) in one part of the range are typically accompanied by good conditions in the opposite part, be it east versus west or north versus south. They suggest that irruptions work on a push pull system, where movements are driven not only by the ‘push’ of falling local food supply but also by the inherent ‘pull’ to the opposite part of the range where conditions would be expected to be better. Further work is needed on this issue.

Other seed-eaters Although variations in autumn movements are especially marked in species that eat tree-seeds, they are apparent to smaller extent in those that feed from herbaceous plants. In arid regions, the local production of such seeds can vary greatly from year to year, according to rainfall patterns, and in other regions their availability is affected by patterns of agriculture or snowfall. Many seed-eaters concentrate at different points on their migration routes in different years, depending on seed supply (Pulliam & Parker, 1979; Dunning & Brown, 1982), and ringed individuals have occurred at widely separated points on that route in different winters (for European Goldfinch (Carduelis carduelis) and Eurasian Linnet (Acanthis cannabinna), see Newton, 1972; for Dark-eyed Junco (Junco hyemalis), see Ketterson & Nolan, 1982), or have moved further along the route during the course of a winter (Haila et al., 1986; Terrill & Ohmart, 1984). This is less extreme irruptive behaviour, with more directional consistency.

CONCLUDING REMARKS So how do irruptive migrants differ from regular migrants? Most obviously, their numbers at particular localities fluctuate much more from year to year than those of regular migrants, and in most species, these fluctuations have been clearly linked to fluctuations in prevailing food supplies. The fact that these birds can go from absence to abundance in less than a year strongly suggests the role of movements in influencing local densities, giving big changes in distribution across the range from year to year. The movement has been confirmed by ring recoveries, showing that some irruptive seed-eaters can breed or winter in localities hundreds or thousands of kilometres apart in successive years, often on an east west axis. This behaviour is strikingly different from that of regular migrants, which usually return to the same breeding localities year after year, and often also to the same wintering localities, migrating mainly over a north south axis. To judge from the variable extent and timing of their migrations, many irruptive species while genetically equipped to migrate must presumably respond directly to food conditions at the time. Only in this way could they show the level of flexibility in the movement patterns recorded. Food shortage apparently acts not only as the ultimate causal factor to which migration is supposedly adapted but also as the main proximate factor delaying or promoting departure from particular localities (for food manipulation experiments on captive Pine Siskins, see Robart et al., 2019, 2022). The advantage of strong endogenous control of migration, as shown by regular obligate migrants, is that it can permit anticipatory behaviour, allowing birds to prepare for an event such as migration before it becomes essential for survival, and facilitating fat deposition before food becomes scarce. But such a fixed control system is likely to be beneficial only in predictable circumstances, in which food supplies change in a consistent manner, and at about the same dates, from year to year. It is not suited to populations that have to cope with a large degree of spatial and temporal unpredictability in their food supplies. It is these aspects of food supply which probably result in irruptive migrants showing greater variations in autumn timing, directions and distances, selection having imposed less precision on these aspects than in regular migrants. Both regular and irregular systems are adaptive, the one to consistent and predictable foods and the other to inconsistent and unpredictable foods (Table 20.5). Nevertheless, regular (obligate) and irruptive (facultative) migrants are best regarded, not as distinct categories, but as opposite ends of a continuum, with predominantly endogenous control (5rigidity) at one end and predominantly external control (5flexibility) at the other (Chapter 13).

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TABLE 20.5 Comparison between typical regular and typical irruptive migration. Regular (obligate) migrants

Irruptive (facultative) migrants

Habitat food

Predictable

Unpredictable

Breeding areas

Fixed

Variable

Wintering areas

Fixed

Variable

Site fidelity

High

Low

Proportion migrating

Constant

Variable

Timing

Consistent

Variable

Distance

Consistent

Variable

Direction

Consistent

Variable

Migration

Some irruptive migrants vary geographically in their behaviour, being more strongly irruptive in some regions than in others. It is easy to appreciate how such regional variation might evolve within species, as food supplies across the breeding range change from more predictable to less predictable, partly in association with the diversity of food types available, and with the degree of their year-to-year fluctuation. This is little different in principle from the transition from resident to migratory found in many bird species from low to high latitudes. It accounts for why some species, such as the Great Tit and Eurasian Bullfinch, are essentially resident in some parts of their geographical range, irruptive in other parts, and perhaps regular migrants in yet other parts (Cramp & Simmons, 1980; Cramp & Perrins, 1993). Each mode of behaviour is adapted to the nature of the food supply in the region concerned, in accordance with their different food plants.

SUMMARY The seed crops of some northern tree species vary greatly in size from year to year, both in particular regions and over the two northern landmasses. However, seed crops in different regions fluctuate independently of one another, so that good crops in some regions coincide with poor crops in others. Each year, the birds that depend on tree seeds tend to settle at greatest densities in areas with the largest crops and, in line with the variable fruiting patterns, some individuals breed and winter in widely separated areas in different years. In different breeding seasons, as in different winters, ringed individuals of several species have been found at localities hundreds or thousands of kilometres apart. In years of widespread food shortage (or high numbers relative to food supplies), extending over many thousands or millions of square kilometres, large numbers of birds migrate much further than usual, appearing mainly in more southern areas, as an irruptive migration. In North America, over long periods, irruptions of several species occurred about every second year, but in Europe irruptions have been much less regular and less synchronized between species, ultimately dependent on regional differences in tree-cropping. Crossbills depend year-round on conifer seeds. In much of Europe, Red Crossbills make one major movement each year, in summer, between the shedding of one spruce seed crop in certain areas and the formation of the next crop in other areas. In years of widespread crop failure, the movements become more directional, and birds leave the regular range in large numbers, occurring as irrupting flocks well outside their usual range, only to return in a later year. The same holds for Spotted Nutcrackers in the boreal zone of Eurasia, while Clark’s Nutcrackers in North America move from the western mountains to neighbouring lowlands. Compared with regular (obligate) migrants, irruptive (facultative) migrants show much greater year-to-year variations in the proportions of individuals that migrate, and greater individual and year-to-year variations in the autumn timing, directions and distances of movements. The control systems are flexible in irruptive migrants, enabling individuals to respond to feeding conditions at the time. Regular and irruptive migrants probably represent opposite extremes of a continuum of migratory behaviour found among birds, from narrow and consistent at one end to broad and flexible at the other. Both systems are adaptive, the one to conditions in which resource levels are predictable temporally and regionally, and the other to conditions in which resource levels vary unpredictably. Depending on the predictability of its food supply, the same species may behave as a resident or regular migrant in one part of its range, and as an irruptive migrant in another.

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Chapter 21

Irruptive migrants: owls, hawks and ducks

Snowy Owl (Bubo scandiaca), an irruptive migrant from the tundra Its distribution is irregular, it being abundant at one season and almost totally unknown the next. E. W. Nelson (1887), on Snowy Owls

This chapter is concerned with two other groups of irruptive birds, firstly those owls and other predators that specialize on voles and other cyclically fluctuating prey, and secondly those ducks that depend on ephemeral wetlands. Again, the large-scale movements of these species can best be understood in light of their underlying ecology. Ducks are not usually regarded as irruptive migrants but, particularly in arid regions, they show many of the typical features.

RODENTS AND RODENT-EATERS Owls and raptors that depend on cyclically fluctuating prey species often suffer food shortages in years when their prey numbers crash. In some species this leads to massive emigration. Two main prey systems are involved: (1) a 3 5 year cycle of small (microtine) rodents in the northern tundras, boreal forests and temperate grasslands; and (2) an approximately 10-year cycle of Snowshoe Hares (Lepus americanus) in the boreal forests of North America (Elton, 1942; Lack, 1954; Keith, 1963; Stenseth, 1999). The numbers of certain grouse species also fluctuate cyclically, in some regions in parallel with the rodent cycle and in others with the longer hare cycle (Ho¨rnfeldt, 1978; Keith & Rusch, 1988; Newton, 1998). Any predators that specialize on such prey species, as well as more generalist predators that also eat other things, are affected by the fluctuations in these prey. The main microtine rodents that undergo cyclic fluctuations are plant-eating lemmings (Dictrostionyx and Lemmus) on the tundra and voles (Microtus and Clethrionomys) in other open habitats (including forest openings) further south. Populations of these rodents do not reach a peak simultaneously over their whole range, but the cycles may be The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00023-3 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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The Migration Ecology of Birds

synchronized over huge areas embracing thousands of square kilometres, out of phase with those of more distant areas. However, peak populations may occur simultaneously over many more areas in some years than in others, giving a measure of synchrony, for example to lemming cycles over large parts of northern Canada, but with regional exceptions (Chitty, 1950). In addition, vole cycles tend to lengthen northwards from about 3 years between peaks in temperate and southern boreal regions to 4 5 years in northern boreal regions (Figure 21.1). The amplitude of the cycles also increases northwards, from barely discernable in some southern temperate regions to marked fluctuations further north, where peak densities typically exceed the troughs by more than 100-fold (Hanski et al., 1991). On the tundra, the periodicity of lemming cycles is in some places even longer (5 8 years between peaks on Wrangel Island, Menyushina et al., 2012), and the amplitude even greater, with peaks sometimes exceeding troughs by more than 1000-fold (Shelford, 1945). In most places, the increase phase takes up most of the cycle and the crash phase occurs within 1 year. Importantly, the crash phase often occurs during spring and summer, which can cause widespread breeding failure among rodent predators (eg Lockie, 1955; Maher, 1970). Specialist rodent-eating birds include various owls, diurnal raptors and skuas (jaegers). In general, these birds would have to shift their breeding areas by at least several hundred kilometres every one or every few years if individuals were to breed under adequate food conditions every year. Owls and other predators show two main types of response to fluctuations in their rodent prey. One type is shown in resident species, which, while preferring rodents, also eat other things. They can therefore remain on their territories through low rodent years, switching to alternative prey, but their survival and breeding output may be much reduced (Newton, 2002). The Tawny Owl (Strix aluco), Ural Owl (Strix uralensis) and Barn Owl (Tyto alba) are in this category, responding to prey numbers chiefly in terms of the number of young raised (Saurola, 1989; Petty, 1992; Taylor, 1994). This type of response, shown by resident rodent feeders, produces a lag between prey and predator numbers so that high predator breeding densities follow 1 2 years after good food supplies and low densities follow poor supplies. Prey and predator densities go up and down in parallel, but with the predator behind the prey (Newton, 2002). The natal dispersal distances of these species also tend to be longer in poor rodent years (see later). The second type of response is shown by prey-specialist nomadic species, which concentrate to breed in different areas in different years, depending on where their rodent prey are plentiful at the time (Figures 21.2 and 21.3). Typically, individuals might have 1 2 years in the same area in each 3 5 year vole cycle, before moving on when prey decline. Response to change in food supply is almost immediate, and the increases in numbers from one year to the next are often far greater than could be explained by high survival and reproduction from the previous year, so must also involve immigration. The Short-eared Owl (Asio flammeus), Long-eared Owl (Asio otus), Northern Hawk Owl (Surnia ulula), Snowy Owl (Bubo scandiacus), Boreal (Tengmalm’s) Owl (Aegolius funereus) and Great Grey Owl (Strix nebulosa) are in this category, as are the Common Kestrel (Falco tinnunculus), Hen (Northern) Harrier (Circus cyaneus) (hudsonius), Pallid Harrier (Circus macrourus) and Rough-legged Buzzard (Buteo lagopus) in some regions. Their local breeding densities can vary from nil in low rodent years to several tens of pairs per 100 km2 in intermediate (increasing) or high rodent years. In a 47 km2 area of western Finland, for example over an 11-year period, numbers of Short-eared Owls varied FIGURE 21.1 Index of Field Vole (Microtus agrestis) densities in spring, summer and autumn in Kielder Forest, northern England, over 15 years. Note that in most years vole densities increased from spring to summer (the owl breeding season), but in some years they decreased from spring to summer. Modified from Petty (1999).

250

Vole density (with SE bars)

200

150

100

50

0 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99

Irruptive migrants: owls, hawks and ducks Chapter | 21

1981

1982

1983

439

1984

FIGURE 21.2 Annual variations in the breeding distribution of Great Grey Owls (Strix nebulosa) in Finland. Small dots dots nests. Modified from Solonen (1986).

territorial pairs; large

between 0 and 49 pairs, numbers of Long-eared Owls between 0 and 19 pairs, and Common Kestrels between 2 and 46 pairs, all in accordance with spring densities of Microtus and other voles (Figure 21.4; Table 21.1; Korpima¨ki & Norrdahl, 1991). All these predators were summer visitors to the area concerned and settled according to vole densities at the time. Their fluctuations contrast with findings from other owls and raptors that depend on a wider range of prey species and show much more stable breeding densities from year to year (Newton, 1979, 2003). Some species that exploit cyclically fluctuating vole populations move around mainly within the breeding range, settling wherever rodents are sufficiently plentiful, as exemplified by the Boreal Owl and Northern Hawk Owl in forest. In other species, parts of the population migrate to lower latitudes in winter, thereby avoiding the worst effects of snow cover, and return to the breeding range each spring, again settling in areas where voles are numerous at the time. This pattern is exemplified by the Short-eared Owl, Long-eared Owl, Common Kestrel, Northern Harrier and Pallid Harrier over much of their breeding ranges (Hamerstro¨m, 1969; Korpima¨ki & Norrdahl, 1991; others). All these species hunt from the wing, which requires more energy than the sit-and-wait methods of some other rodent-eaters (Sonerud, 1984). This may be why they tend to leave areas with prolonged winter snow. They may redistribute themselves in relation to vole densities at least twice each year, in autumn and spring. Snowfall can affect this pattern because under deep snow voles can become largely unavailable to most northern owl species (the Great Grey Owl is exceptional in being able to penetrate up to 50 cm of snow with a hard crust). In general, however, in their movement patterns, specialist rodenteaters parallel the boreal seed-eaters discussed in Chapter 20. On the northern tundras, some species of skuas also eat microtine rodents. These birds spend most of their lives at sea but return to the tundra to breed. They seem to return to the same breeding areas each year but nest only if rodents are plentiful, remaining as non-breeders in other years. This pattern has been found in Pomarine Skuas (Stercorarius pomarinus) in Alaska (Pitelka et al., 1955; Maher, 1970) and in Long-tailed Skuas (Stercorarius longicaudus) in northern Europe (Andersson, 1976). In the latter, a similar number of pairs returned to the study area each spring, but the percentage that bred varied from 0% to 100%, according to rodent abundance, giving nest densities over 9 years of 0 60 per 100 km2. In years of low rodent numbers, the birds took a range of different foods, including bird eggs, but in years of high rodent numbers, they ate almost nothing else. At 19 localities across the Siberian tundra examined in 1 year, the numbers of nesting Pomarine and Long-tailed Skuas in different areas were correlated with local lemming numbers at the time, as were the local numbers of Snowy Owls and Rough-legged Buzzards, although the latter two tended to avoid each other (Wiklund et al., 1998).

Breeding dispersal As in boreal seed-eaters, evidence for movements among rodent predators comes partly from the high turnover among birds caught each year in the same localities. In all the species listed in Table 21.1 that were studied in this respect, return rates to the same breeding area were extremely low compared to what would be expected from their annual survival rates. Among Common Kestrels, of 146 individual breeders trapped and ringed in a 63 km2 area in

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The Migration Ecology of Birds

FIGURE 21.3 Year-to-year changes in the densities of Snowy Owls (Bubo scandiacus) in different parts of northern Canada, as judged from questionnaire surveys of trappers and other local residents. Each dot marks the centre of an area covered by an individual trapper. Large dots marked increases from previous year; small dots marked decreases from previous year. Changes in owl numbers generally matched those of lemming numbers, and changes were synchronized over much of northern Canada, with a few regional exceptions. From Chitty (1950).

1944–45

1000 km

1945–46

1000 km

1946–47

1000 km

Finland over an 11-year period, only 13% of males and 3% of females were found back in the same area in a later year (Korpima¨ki & Norrdahl, 1991). The implication is that a large proportion of breeders changed their nesting localities from year to year. More direct evidence for wide-scale movements stems from adults that were found in widely separated areas in different breeding seasons. Most information of this type relates to Boreal Owls, which nest readily in boxes and have

Vole abundance Owl breeders

60 45

1500

30

1000

15

500

0

77

78

79

80

81

82

83

84

85

86

87

Hare abundance Owl floaters Owl territory holders

(B) 125

0

2.00 1.75

100

1.50 1.25

75

1.00 50

0.75 0.50

25 0

FIGURE 21.4 Annual fluctuations in the breeding densities of the (A) Short-eared Owl (Asio flammeus) in relation to Microtus vole densities in an area of western Finland, and (B) the Great Horned Owl (Bubo virginianus) in relation to Snowshoe Hare (Lepus americanus) densities in an area of the Yukon, Canada. Modified from Korpima¨ki & Norrdahl (1991), Rohner (1995).

Hare abundance

Number of pairs

2000

Vole abundance

Number of pairs

(A)

0.25 0.00 88

89

90

91

92

93

TABLE 21.1 Established year-to-year correlations between bird breeding density, autumn emigration and food supply in rodent-eating birds. Summer

Autumn emigration

References

Raptors Northern Harrier (Circus cyaneus)

K

Hamerstro¨m (1969), Hagen (1969)

Pallid Harrier (Circus macrourus)

K

Terraube et al. (2012), Limin˜ana et al. (2015)

Rough-legged Buzzard (Buteo lagopus)

K

Common Kestrel (Falco tinnunculus)

K

Cave´ (1968), Hagen (1969), Korpima¨ki & Norrdahl (1991), Village (1990)

Black-shouldered Kite (Elanus axillaris)

K

Malherbe (1963), Mendelsohn (1983)

K

Schu¨z (1945), Hagen (1969), Court et al. (1988), Potapov (1997), Wiklund et al. (1998)

Owls Short-eared Owl (Asio flammeus)

K

K

Village (1987), Korpima¨ki & Norrdahl (1991)

Long-eared Owl (Asio otus)

K

K

Village (1981), Korpima¨ki & Norrdahl (1991)

Great Grey Owl (Strix nebulosa)

K

K

Hilde´n & Helo (1981), Nero et al. (1984), Duncan (1992, 1997), Bull & Duncan (2020)

Snowy Owl (Bubo scandiaca)

K

K

Shelford (1945), Chitty (1950), Newton (2002), Wiklund et al. (1998), Therrien et al. (2014), Robillard et al. (2016), Holt et al. (2020)

Northern Hawk Owl (Surnia ulula)

K

K

Korpima¨ki (1994)

Boreal Owl (Aegolius funereus)

K

K

Korpima¨ki & Norrdahl (1989), Cheveau et al. (2004)

K

Rasmussen et al. (2020)

Saw-whet Owl (Aegolius acadicus)

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The Migration Ecology of Birds

FIGURE 21.5 Ringing and recovery sites of adult Boreal Owls (Aegolius funereus) that were identified in different breeding seasons. Continuous lines females; dashed lines males. Only movements greater than 100 km are shown. From Newton (2003), compiled from information in Lo¨fgren et al. (1986), Korpima¨ki et al. (1987) and Sonerud et al. (1988).

Male Female 500 km

been studied at many localities in Europe (Figure 21.5). In this species, the males in some regions are mainly resident and the females are more dispersive. Both sexes tend to stay in the same localities if vole densities remain high, moving no more than about 5 km between the nest boxes used in successive years. But if vole densities crash, females move much longer distances, with many having shifted 100 600 km between breeding sites in different years (Figure 21.5). In contrast, fewer long movements were recorded from males, with only two at more than 100 km. The greater residency of males was attributed to their need to guard cavity nest sites which are scarce in their conifer nesting habitat, while their smaller size makes them better able than females to catch small birds, and hence to survive through low vole conditions (Lundberg, 1979; Korpima¨ki et al., 1987). When voles become plentiful again, male owls still have their previous nest sites and are again able to attract females which move in to exploit the abundant prey. In the northern boreal zone, however, where small birds are scarce in winter, both sexes tend to vacate areas with low vole numbers. Far fewer records are available for other nomadic owl species, because the chances of recording marked individuals at places far apart are low. However, in a study of Short-eared Owls in south Scotland, 21 breeders were tagged in 1976. Vole numbers then crashed, and only one of the tagged birds remained to breed there in 1977. Two others were reported in spring 1977 in nesting habitat 420 and 500 km to the northwest, and the latter, at least, was proved to breed there (Village, 1987). Of seven breeders tagged in 1977, when vole numbers began to increase, three bred in the area in 1978. Hence, as in Boreal Owl, individuals seemed more likely to remain to breed in successive years when voles were increasing than when they were declining. Recoveries of Northern Hawk Owls and Great Grey Owls ringed as breeding adults include examples of both males and females residing in an area from one nesting season to the next when vole abundance remained high, but leaving when vole numbers declined (Sonerud, 1997; Duncan, 1992). Adult radio-marked Great Grey Owls in Manitoba and

Irruptive migrants: owls, hawks and ducks Chapter | 21

443

Minnesota dispersed an average of 329 km (range, 41 684 km, N 5 27) between breeding sites in response to prey population crashes. Eleven marked birds that did not disperse died (Duncan, 1992, 1997). Some of the birds that moved returned to their original breeding place in a later year and were found breeding there, raising the possibility that they may have shuttled between different regular breeding areas, up to several hundred km apart, in different years. Other ringing-based records of breeding dispersal in woodland owls include two adult Great Grey Owls in northern Europe found at localities 300 and 430 km apart in different breeding seasons (Hilde´n & Solonen, 1987), and three adult Longeared Owls in North America found at localities more than 450 km apart (Marks et al., 1994). More revealing information is available for four adult female Snowy Owls which were radio-tagged while nesting near Point Barrow in Alaska and tracked by satellite over the next 1 2 years (Fuller et al., 2003). These birds mostly stayed in the Arctic but dispersed widely in different directions from Point Barrow, reaching west as far as 147oE and east as far as 116oW, a geographical spread encompassing nearly one-third of the species’ Holarctic breeding range.% Two birds that bred % Barrow in 1999 were present during the next breeding season in northern Siberia (147 E and 157 E, respectively), at Point up to 1928 km east of Point Barrow, and then in the following breeding season, they were on Victoria Island (108 W) and Banks Island (121 W), respectively, having passed eastward through Point Barrow (Table 21.2; Figure 21.6). The two birds that bred at Point Barrow in 2000 were also present on Victoria and Banks Islands in the breeding season of 2001. Successive summering areas of these four birds were thus separated by distances of 628 1928 km (Table 21.2). From the dates they were present, some could have bred successfully, while others were unlikely to have done so. None returned to the same breeding or wintering site used in a previous year, but three passed through Point Barrow again in 2001. In winter these Snowy Owls made long-distance moves at various dates; one bird remained continually on the move, venturing as far south as 59 N, but spending no more than a fortnight at any one place, while another remained for 2.5 months in one place. Only two ventured south of the breeding range, one briefly but the other staying for more than 2 months at 60 N in southern Alaska. Some spent time in winter on sea ice far from land, presumably hunting seabirds. A later tracking study in the Canadian Arctic revealed similar behaviour, with distances between the consecutive nesting places of nine satellite-tracked females averaging 725 km and ranging from 18 to 2224 km (Therrien et al., 2014). This study also revealed extensive ‘prospecting’ movements, as individuals wandered over distances up to 4093 km in the weeks before breeding, apparently searching for areas with abundant lemmings (see below). Among diurnal raptors that specialize on rodents, three Pallid Harriers in Kazakhstan moved an average of 403 km between two successive breeding locations, with a maximum of 834 km (Limin˜ana et al., 2015), and among Black Harriers (Circus maurus) tracked in South Africa, three settled on their former breeding areas and two others at distances 230 and 530 km from their previous breeding area (Garcia-Heras et al., 2019). Regarding natal dispersal, movements exceeding 1000 km have been documented for Short-eared Owls (up to about 4000 km), Long-eared Owls (up to about 2300 km) and Hawk Owls (up to 2700 km), as well as for Rough-legged Buzzards (up to 2700 km) (Saurola 1983, 2002; Saurola, 1997; Cramp & Simmons, 1980; Cramp, 1985). The recorded natal dispersal distances for young owls of various species ringed in Finland indicate much longer median and maximum distances from irruptive than from ‘sedentary’ species (Table 21.3). Among diurnal raptors, Galushin (1974) summarized data from Russian ring recoveries showing that irruptive (mostly vole-eating) species had much longer dispersal distances than non-irruptive ones. The mean natal dispersal distance of the Rough-legged Buzzard was given as 1955 km (but with no mention of sample size). TABLE 21.2 Locations of four adult female Snowy Owls (Bubo scandiaca) in successive breeding seasons. Owl number

Breeding seasons 1999

2000 



2001

54

Alaska 71 N, 156 W

Siberia (70 N, 157 E)

Victoria Islandb (73 N, 108 W)

57

Alaskaa 71 N, 156 W

Siberiac (71 N, 147 E)

Banks Islandc (73 N, 121 W)

80

Alaska 71 N, 156 W

Victoria Islandb (73 N, 115 W)

81

Alaskaa 71 N, 156 W

Banks Islandc (73 N, 122 W)

a

b





a

Great circle distances between places where successful breeding was known or probable were 628 km between Point Barrow and Banks Island (bird 81) 1548 km between Siberia and Banks Island (bird 57) and 1928 km between Point Barrow and Siberia (bird 57). All were radio-tagged at Point Barrow, Alaska in 1999 (numbers 54 and 57) or 2000 (numbers 80 and 81), and tracked by the Argos satellite system. From Fuller et al. (2003). a Known to have bred. b Unlikely to have bred successfully. c Probably bred.

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The Migration Ecology of Birds

FIGURE 21.6 Movements of a radio-tagged female Snowy Owl (Bubo scandiacus) tracked by satellite between the summers of 1999 and 2001. Filled circles show known likely breeding sites in three consecutive years (see Table 21.2), and open circles show other sites where the bird spent more than four weeks at a time. Constructed from information in Fuller et al. (2003).

TABLE 21.3 Average natal dispersal distances (km) of owls ringed as nestlings in Finland and found dead in a subsequent breeding season. Species

Number recovered

Median distances (km)

Maximum distance (km)

Eurasian Eagle Owl (Bubo bubo)

563 (20)

52 (47)

416 (114)

Tawny Owl (Strix aluco)

1126 (1288)

22 (17)

386 (270)

Ural Owl (Strix uralensis)

538 (1036)

28 (22)

339 (205)

Pygmy Owl (Glaucidium passerinum)

10 (131)

8 (15)

183 (288)

Northern Hawk Owl (Surnia ulula)a

2

490

869

Great Grey Owl (Strix nebulosa)

16 (6)

227 (124)

912 (315)

Long-eared Owl (Asio otus)

48

287

1759

Short-eared Owl (Asio flammeus)

16

822

3453

Boreal Owl (Aegolius funereus)

96 (541)

71 (78)

874 (588)

Sedentary species

Nomadic species

Figures in parentheses refer to additional birds recaptured alive at nest sites. a The two birds moved 111 km and 869 km. Source: From Saurola (2002).

Irruptive migrants: owls, hawks and ducks Chapter | 21

445

These various irruptive owls and raptors thus contrast greatly with more sedentary populations, which exploit more stable food supplies. In such species, adults usually remain in their territories year after year, with only small proportions moving to other territories, usually nearby (for Tawny Owl, Ural Owl and Barn Owl, see Saurola, 1989, 2002; Petty, 1992; Taylor, 1994). One consequence of such site fidelity is strong mate fidelity, as partners remain together from year to year. Natal dispersal distances are mostly less than 30 km, with few exceeding 100 km (for Tawny Owl, see Petty, 1992; Saurola, 2002; for Ural Owl, see Saurola, 1987, 2002; for Barn Owl, see Taylor, 1994; also Table 21.3). In resident as well as in nomadic species, movements are generally longer in poor food years than in good ones (Taylor, 1994; Saurola, 2002; Korpima¨ki, 2020). Typically, the numerous young produced in peak prey years move further than young produced in other years, because it is they that experience the crash that follows the peak.

Locating areas with abundant food One of the long-standing questions about species that exploit sporadic food supplies is how they find areas with sufficient food to enable them to breed. Evidence from tracking studies implies that they just search for them, as evident in 12 female Snowy Owls, some followed in more than 1 year. During their pre-breeding movements from mid-March to early June, tracked individuals constantly switched from moving to searching behaviour (Therrien et al., 2015). They passed most rapidly, often in straight-line flight, over areas of deep snow where they were least likely to detect lemmings and searched intensively with zig-zag flights over areas where snow cover was sparse and shallow. On average, individuals began their prospecting movements on 5 April 6 17 (SD) days and continued for 36 6 25 days. During that time, they covered an average of 1251 6 1175 km, often alternating between moving and searching behaviour, and patrolling several distinct searching areas before eventually settling for the summer. The maximum distance between searching areas in a given year averaged 828 km (range 220 2433 km). Settlement date, distance between searching areas, total travelled distance and the duration of prospecting movements were longer in the year when the density of lemmings in the region concerned (Bylot Island) was lowest (Therrien et al., 2014). Likewise, Pallid Harriers returning from migration to breed in Kazakhstan undertook apparent prospecting trips lasting up to 3 weeks and covering up to 3000 km (Limin˜ana et al., 2015); and Black Harriers after arriving within the breeding range in South Africa made prospecting movements covering several hundred kilometres (maximum 1135 km) (Garcia-Heras et al., 2019). Presumably, these birds used both sight and sound to detect their prey.

Geographical variation in movement patterns within species The same species may show regional variation in movement behaviour depending on food supply, and the extent to which alternative prey are available when favoured prey are scarce. Examples of regional variation among diurnal raptors include Common Kestrel and Hen and Northern Harriers, in which the proportion of rodents in the diet differs from region to region. The more varied the diet, the less the chance of all prey types being scarce at the same time, the more stable are their local breeding densities and the greater the site fidelity shown by individuals. Examples among owls include the Boreal Owl, which has been described as a resident generalist predator of small mammals and birds in central Europe, as partially nomadic (with males mainly resident and females moving around) in south and west Finland, and as a highly nomadic microtine specialist in northern Fennoscandia, in areas with pronounced vole cycles and fewer alternative prey (Korpima¨ki, 1986). Great Grey Owls are regarded as highly irruptive in their northern boreal breeding areas but as altitudinal migrants or residents on mountains further south (Bull & Duncan, 2020). Snowy Owls could be regarded as regular migrants to the northern prairies, as they appear there every year, but in markedly varying numbers, while in the east of the continent, they are more strongly irruptive, with much greater annual fluctuations (Kerlinger et al., 1985). The return rates of adults to former nesting areas can vary regionally within species, according to the degree of year-to-year stability in food supply. In comparison with the return rates mentioned above for Kestrels in Finland of 13% males and 3% females, Village (1990) recorded rates of 29% and 18% for males and females in Scotland, and of 43% and 36% in southern England, commenting that the more sedentary nature of the English population was ‘due to the greater stability of the food supply both within and between years’. In a study in the Netherlands, as many as 70% of adult Kestrels remained from year to year when vole numbers were on the increase, and as few as 10% when vole numbers crashed (Cave´, 1968). Similarly, the Long-eared Owl showed greater year-to-year site fidelity in the Netherlands than in Finland (Wijnandts, 1984; Korpima¨ki, 1992), as did the Great Grey Owl in some parts of North America compared with others (Bull & Duncan, 2020), while the Barn Owl has proved highly sedentary in Britain (Taylor, 1994) but more dispersive in parts of continental Europe (with movements up to 2000 km recorded) and in parts of North America (Bairlein, 1985; Marti, 1999).

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The Migration Ecology of Birds

Irruptive migrations Like the irruptive finches, some rodent-eating species respond to periodic crashes in their main food supply by winter emigration, appearing south of their breeding range in much larger numbers than usual. Others show marked annual fluctuations in breeding success, dependent on food supply, and leave in the biggest numbers after good breeding seasons. Both responses relate to food supplies and lead to regular periodicity in their movements. Irruptions of Snowy Owls from the tundra to the boreal and temperate regions of eastern North America have been documented at least since 1880. Throughout the next 120 years, irruptions occurred every 3 5 years, at a mean interval of 3.9 (SE 6 0.13) years (Newton, 2002, 2008). Moreover, in periods when information on lemmings was available from potential breeding areas to the north, mass movements of owls coincided with crashes in lemming numbers (Shelford, 1945; Chitty, 1950); but more recent studies put greater emphasis on lemming-dependent breeding success (Robillard et al., 2016; Santonja et al., 2018). In western North America, irruptions were not well synchronized with those in the east, presumably reflecting asynchrony in lemming cycles between breeding regions. In eastern North America, two other vole-feeders, the Rough-legged Buzzard and Northern Shrike (Lanius borealis), have irrupted at similar 3 5 year intervals, mostly (but not always) in the same years as Snowy Owls (Davis, 1937, 1949; Speirs, 1939; Shelford, 1945; Lack, 1954). Perfect synchrony between the three species would not be expected, because their breeding ranges only partly overlap. In the shrike, the cyclic pattern in invasions was most marked before 1950, after which the fluctuations became more irregular and eventually hardly apparent (Davis & Morrison, 1987). In North America, Northern Hawk Owl irruptions also tend to occur at 3 5 year intervals but in different years in different regions (Duncan & Duncan, 2020). Although modified by snow cover, they seldom extend south of the boreal region. Great Grey Owl irruptions are occasionally recorded south and east of the usual breeding range, with big flights noted in various eastern regions in 1978, 1983, 1991, 1995 and 2004 (Nero et al., 1984; Jones, 2005; Bull & Duncan, 2020). Among Boreal Owls, winter irruptions showed roughly 4-year cycles in Quebec, extending just south of the boreal forest in years when the main prey (Clethrionomys gapperi) was scarce (Cheveau et al., 2004). Winter invasions of Hawk Owls and Great Grey Owls in this region occurred in the same years but were less marked, and of shorter distance than those of Boreal Owls. The Hawk Owl also takes young hares and birds, so may be buffered to some extent against shortages of voles. Saw-whet Owls (Aegolius acadicus) are classed as regular migrants but are significantly more numerous at ringing stations about every fourth year when trapped samples contain much greater proportions of juveniles (Rasmussen et al., 2020). In Europe too, the Great Grey, Long-eared and Short-eared Owls also seem to migrate on regular 3 4 year patterns, again linked with cycles in their prey (Harvey & Riddiford, 1996; Schmidt & Vauk, 1981; Hilde´n & Helo, 1981). As in seed-eaters, movements often begin earlier than usual in irruption years and mortality among the participants is sometimes heavy, as illustrated by the 500 Great Grey Owls found dead in Ontario in 2004 05 (Jones, 2005).

Changes in wintering areas To my knowledge, few ring recoveries from different winters are yet available for any species of irruptive owls, but in recent years tracking studies have provided useful information for Snowy Owls. They have shown that most individuals remain in the arctic year-round, hunting either on the tundra for lemmings or at openings in sea ice for sea ducks (Fuller et al., 2003; Therrien et al., 2011). However, some Snowy Owls move south to winter in the temperate zone in numbers that vary greatly from year to year. The satellite-tagged individuals mentioned above were present in widely separated localities in different winters in the Arctic and often moved long distances within a winter (Fuller et al., 2003). For 21 other female Snowy Owls tracked by satellites, the mean distance between their wintering locations of different years was 389 km (range: 20 2731 km). Excluding the one individual that switched between Arctic and temperate zones, the mean distance became 271 km, and the range was 20 1479 km (Robillard et al., 2018). These distances were lower than breeding dispersal distances mentioned above (mean: 710 km, range: 85 1617 km, n 5 35). South of the breeding range, some Snowy Owls have returned to the same wintering sites in successive years (Holt et al., 2020). Of 419 individuals ringed over 39 years in a 65 km2 area in Minnesota, 43 were present in the area in later years. Of these, 38 returned for the following winter, eight for two consecutive winters, four for three consecutive winters, and one for four consecutive winters. Nine returned in non-consecutive years. Another ringed bird was re-sighted in two winters at a site 1700 km to the northwest. In another winter study over 33 years in Massachusetts, 17 of 452 ringed owls returned in one or more subsequent winters. All these records referred to birds wintering in the temperate zone which offered a much more varied and consistent food supply than is available on the tundra in winter, making site fidelity more feasible.

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Trapping efforts have revealed considerable turnover during the course of a winter in the individuals of irruptive species present at particular sites (for Snowy Owl, see Kerlinger et al., 1985; Smith, 1997; for Great Grey Owl, see Nero et al., 1984). The implication is again that, in the non-breeding period, some individuals move around, perhaps in continual search for good hunting areas. Local abundances of voles can attract high densities of nomadic owls, and in these conditions some species form communal winter roosts, as frequent in Long-eared, Short-eared and Great Grey Owls (Cramp, 1985; Nero et al., 1984). In some years, the migrants may travel long distances without encountering any areas with abundant food, and in such cases their mortality rates are likely to be much higher than usual, as exemplified above (Jones, 2005).

Nesting outside the regular range Various species of owls have also been recorded nesting well outside their regular range in years of abundant food. For example several hundred pairs of Snowy Owls bred on the tundra of Swedish Lapland in 1978, where they had been rare to nonexistent in previous years (Andersson, 1980). Snowy Owls bred in Finnish Lapland in 1974, 1987 and 1988, but before these dates none had been seen for several decades (Saurola, 1997). Similarly, Northern Hawk Owls bred in an area in Norway in the peak years of only four out of seven observed vole cycles (Sonerud, 1997). This lack of response may arise because in many years the entire owl population can be accommodated in certain parts of the range with abundant prey, without needing to search out other parts. In Fennoscandia, the numbers of Snowy and Hawk Owls at any time seem to be influenced not only by the occurrence of a rodent peak but by the arrival of large numbers of immigrants from further east (Sonerud, 1997). In more central parts of the range, the owls may exploit a much greater proportion of the rodent peaks. When voles were plentiful, Hawk Owls also bred temporarily in invasion areas well south of their usual breeding range in North America (Duncan & Duncan, 2020). Among diurnal raptors, numbers of Rough-legged Buzzards, Common Kestrels and Pallid Harriers were also found breeding outside the regular range in localities where voles were plentiful (Galushin, 1974).

Rodents and reproduction Specialist rodent-eaters are known for raising large families (up to eight or more young per brood in some species) in years when prey are plentiful, but few or none in years when prey are scarce, or when prey crash from abundant to scarce during a summer (Cramp, 1985; Newton, 2002). Juveniles formed 85% of 80 Northern Hawk Owls handled on irruption in northern Europe in 1950, 100% of 52 caught in 1976, and 88% of 150 museum skins collected over several years, implying that these irruptions followed good breeding seasons (Cramp, 1985). Among Saw-whet Owls caught on migration in Virginia, juveniles formed 82% in two irruption years, compared with an average of 33% in other years (Whalen & Watts, 2002). The age composition of wintering Snowy Owls was assessed over a 25-year period in both regular (North American Prairies and Great Plains) and irregular (northeastern North America) wintering areas, on the basis of individuals that were trapped or photographed. The proportion of juveniles varied from about 30% to more than 90% per year in regularly used areas, and from nil to more than 70% in irregularly used areas, but in both types of areas the proportion of juveniles increased with overall abundance (Santonja et al., 2018). These findings also implied the importance of breeding success in influencing the size of irruptions. Interestingly, subsequent mortality rates among juveniles increased with the size of the invasion, in a density-dependent manner (McCabe et al., 2021). Nevertheless, some owl invasions apparently followed poor breeding, as only 4 out of 126 Great Grey Owls trapped in Manitoba in 1995 were juveniles (Nero & Copland, 1997), and a big invasion into Ontario in 2005 included virtually no juveniles (Peck & Murphy, 2005). In these situations, mass emigration was apparently not stimulated primarily by good breeding, as proposed for Snowy Owls (Robillard et al., 2016), but by shortage of prey. Combining the two situations, we can again assume that mass emigration occurred when the ratio of birds to food was high.

HARES AND HARE-EATERS Other striking examples of the link between widespread winter emigration and food supply are provided by the Northern Goshawk (Accipiter gentilis) and Great Horned Owl (Bubo virginianus), which eat Snowshoe Hares (Lepus americanus). The fluctuations in Snowshoe Hare numbers across North America have been recorded for more than 200 years, initially from the number of hare pelts provided each year to the fur market, and latterly from detailed field studies (Elton, 1942; Keith, 1963; Krebs et al., 2001). However, unlike the situation in rodents, the hare cycle appears synchronized over much of boreal North America, with populations across the continent peaking in the same years, at roughly 10-year intervals (Keith & Rusch, 1988; Krebs et al., 2001). In particular localities, peak densities can exceed troughs by more than 100-fold (Adamcik et al., 1978).

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Both Northern Goshawks and Great Horned Owls seem to show much greater numerical fluctuation in the northern boreal region, where they depend primarily on Snowshoe Hares than further south where they have a wider range of prey. In the northern range, these birds would gain little by breeding in widely separated localities in different years because of the synchrony in hare fluctuations across the range. Nevertheless, these hare-eaters do perform massive southward irruptions, abandoning their northern breeding areas at least for the winter, and returning there in summer when alternative prey are available. Because Goshawks fly by day and are more readily seen, their invasions have been better documented than those of owls. They occur for 1 3 years at a time, but at about 10-year intervals (Newton, 2008), coinciding with known lows in the Snowshoe Hare cycle (Keith, 1963; Mueller et al., 1977; Keith & Rusch, 1988). It is usual for juveniles to predominate among migrants in most years when relatively few birds leave the breeding range, but for adults to predominate in invasion years, which follow poor breeding seasons. Thus among more than 12,000 Goshawks trapped over a number of years at Cedar Grove in Wisconsin, juveniles formed more than 80% of the total in most years, but less than 50% in the invasion years of 1962 63 and 1972 73 (Mueller et al., 1977). Migrating Great Horned Owls fly by night, and because they move into more southern regions already populated by resident Great Horned Owls, their irruptions have been less well documented. However, all those that I could find recorded coincided with Goshawk invasions, and hence with low hare numbers, again providing indications that food shortage stimulated large-scale emigration in this mainly resident species (Newton, 2008). In a study in the Yukon Territory, emigration rates of radio-marked Great Horned Owls increased over a period of years from 0% to 33% for territory holders (N 5 2 54 in different years) and from 0% to 40% for non-territorial floaters (N 5 2 18 in different years), as hares declined (Rohner, 1996). Over a much longer period, large numbers of Great Horned Owls were ringed in Saskatchewan, also within the range of the Snowshoe Hare. Most winter recoveries came from the southeast, but from greater distances in years with low hare numbers, when some individuals travelled more than 1000 km from their breeding sites (Houston & Francis, 1995; Houston, 1999).

DUCKS AND EPHEMERAL WETLANDS Our understanding of the distributions and movement patterns of the more obvious irruptive migrants has been pieced together over many years mainly from local observations and ring recoveries. For North American waterfowl, however, detailed continent-wide monitoring of breeding and wintering distributions has been undertaken over many years by aerial survey. This has enabled wide-scale distribution patterns to be examined in relation to prevailing wetland conditions, in both breeding and wintering areas. In one analysis, duck numbers counted annually in May over a 27-year period were examined in relation to wetland conditions across a large part of western North America (Johnson & Grier, 1988). Much of this region is arid prairie and subject to large annual fluctuations in precipitation. Wetlands therefore varied greatly in numbers and extent from year to year, with the shallower ones disappearing altogether in dry years. In this scenario, Johnson & Grier (1988) envisaged three possible patterns of spring settlement in this vast region: 1. Homing, with adults returning to breeding areas used in the previous year, and yearlings returning to near their natal areas. This pattern was expected where habitat conditions remained fairly stable from year to year. On this system, the large-scale breeding distribution of particular species would be expected to be fairly consistent over time. 2. Opportunistic settling, in which birds occupy the first suitable sites encountered on their return migration routes, providing that such sites are not already taken by other birds. This pattern was expected where habitat conditions in particular localities were unpredictable from year to year. Such opportunistic settling could minimize migration costs by ensuring that individuals migrate no further than necessary, but it could result in large-scale changes in the distribution of populations from year to year, depending on the distribution of suitable wetlands. It could also result in some long-distance shifts of individuals between their natal and breeding sites, and between their breeding sites in different years. Local abundance levels would be influenced not just by local conditions, but also by conditions elsewhere in the range. 3. Flexible settling, in which birds home to the area used in the previous year, but move on if conditions there are not suitable. This pattern could be viewed as a compromise between the first two (homing and opportunistic settling) and could affect yearlings more than adults. If birds simply maintained the same migration direction when they moved on, this would result in a general onward displacement of breeding birds when conditions in the usual breeding areas were unsuitable (although birds might not breed as well in these more distant areas as in their usual areas). If yearlings that had not bred previously were more willing to move on than were site-faithful adults, yearlings would be mainly responsible for the year-to-year changes in distribution, again expected to be large.

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Breeding distributions Evidence for some level of opportunistic settling emerged for all 10 species of ducks examined, in that their numbers in particular breeding areas fluctuated from year to year in relation to annual pond numbers. The most obvious opportunists, showing the biggest distributional changes from year to year, inhabited shallow and ephemeral wetlands (which dried out during droughts), notably Northern Pintail (Anas acuta), Mallard (Anas platyrhynchos), Blue-winged Teal (Spatula discors) and Northern Shoveler (Spatula clypeata). At the other extreme, showing the biggest distributional stability from year to year, were the diving ducks, such as Redhead (Aythya americana), Canvasback (Aythya valisineria) and Lesser Scaup (Aythya affinis). Their numbers showed generally poorer correlations with local pond numbers than the dabbling species, because they occupied only the deepest (most permanent) ponds and ignored the shallow temporary ones (for levels of year-to-year site fidelity in different species, see Chapter 19: Table 19.4). The distributional patterns that emerged for some species year after year were consistent with breeding habitat being filled as it was encountered on spring migration. Four species spent the winter mainly in the southern States and in spring migrated roughly northward. They included the Gadwall (Anas strepera) and Green-winged Teal (Anas carolinensis) (dabble-feeders), and the Canvasback and Lesser Scaup (dive-feeders). In all these species, the best correlations between bird numbers and pond numbers were found in the southern parts of the breeding range, and the poorest correlations in the northern parts, supposedly reached mainly by birds unable to find accommodation further south. Three other species wintered in large numbers in the southwestern States and in spring migrated mainly north and northeast, namely the American Wigeon (A. americana), Northern Shoveler and Northern Pintail. The numbers of these species showed high correlations with pond numbers in southwestern count areas, but the correlations again decreased northwards. It seemed, therefore, that large segments of the populations of these seven species could have responded to wetland conditions as they encountered them on return from their wintering areas, moving progressively further in the same direction as habitats became filled. Three other species (Mallard, Blue-winged Teal and Redhead) appeared to respond more directly to conditions in the central parts of their breeding ranges, as this was where the year-to-year correlations between population numbers and pond numbers were highest. Hence, the habitat which these three species filled first was not that which lay closest to their wintering areas. Flexible settling, indicated by overflight of the usual breeding areas in dry years, was shown to some extent by all species. It was most marked in dabbling ducks, notably Northern Pintail, Mallard, Gadwall, Blue-winged Teal and Green-winged Teal, but was also evident in the diving Redhead and Canvasback. All these species were displaced to the north and northwest in prairie drought years, occurring then in much greater numbers than usual in boreal and tundra regions. The American Wigeon, by contrast, was displaced to the east and northeast during drought years. These results confirmed earlier findings that, in years of drought on the prairies, more Pintails than usual overflew the prairie breeding areas to settle further north in the boreal forest and tundra of Canada, Alaska and eastern Siberia, a movement confirmed both by counts and ring recoveries (Figure 21.7; Smith, 1970; Henny, 1973). The magnitude of Pintail migration into eastern Asia, for example thus depended on water conditions some 4500 km away. Breeding success was evidently poorer in the north, as shown from the ratio of young to adults shot in the subsequent winter. This ratio was lowest following springs when the greatest proportions of Pintail occurred in northern breeding areas. Some similar findings were evident in Mallard (Pospahala et al., 1974). 2.00

(b) 2.00

1.75

1.75

1.50

1.50

Age ratio in harvest

Ratio north/south populations

(a)

1.25 1.00 0.75 0.50

1.25 1.00 0.75 0.50

0.25

0.25

0.00 1.25 1.50 1.75 2.00 2.25 2.50 2.75 3.00 3.25 3.50

0.00 0.30 0.25 0.50 0.75 1.00 1.25 1.50 1.75 2.00 2.25

Index of prairie pond numbers (millions)

Ratio north/south populations

FIGURE 21.7 Distribution and breeding success of Northern Pintails (Anas acuta) in relation to wetland conditions on the Canadian prairies. (a) Relationship between numbers of ponds and lakes on the prairies in May and the proportion of the total Pintail population found breeding north of the prairies, 1958 68 (r 5 0.91, P , .001) (b) Relationship between the proportion of the total Pintail population in northern areas and overall breeding success (r 5 0.92, P , .001). Modified from Smith (1970).

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In general, these various patterns were supported by ring recoveries, with diving ducks showing strong site fidelity on breeding areas, and dabbling ducks variable but generally much lower site fidelity (Chapter 19: Table 19.4; Johnson & Grier, 1988). The Blue-winged Teal was extreme in various local studies, in that very few adults or young were found to return to the same areas in successive years. The northward displacement of several species in drought years from the prairies to the tundra was also confirmed by ringing; it represented a substantial shift in the breeding sites of adults in successive years and between natal and breeding sites for yearlings.

Winter distributions The winter distributions of North American ducks also vary from year to year, depending on prevailing conditions, and many birds make substantial movements within winters. In general, species move further south in cold winters than in mild ones or further when low rainfall reduces the numbers of wetlands available. This pattern in Mallard was confirmed by winter ring recoveries which were centred further north during winters when December January temperatures were high than when they were low (Nichols et al., 1983). Birds also tended to concentrate in areas that experienced greater autumn winter rainfall, and hence good wetland conditions. Similarly, in the Wood Duck (Aix sponsa), both adults and young migrated further in years of low summer rainfall and the young also migrated further south when autumn temperatures were lower than normal (Hepp & Hines, 1991). Both rainfall and temperature affect the availability of wetland habitat and food, competition for which may well stimulate further migration, with young ducks more affected than older ones.

Eurasian ducks Although best studied in North America, ringing has confirmed similar distributional patterns among ducks in Eurasia. In particular: (1) some species of ducks take up to 4 5 months over their post-breeding migration, with the bulk of the population moving more rapidly or further in some years than in others; (2) individuals may winter in widely separated areas in different years; and (3) spring settling patterns may also vary from year to year. As in North America, all these features have been linked with patterns in water levels, freezing and thawing, all of which influence the distribution of habitat and associated food supplies. Thus in Teal (Anas crecca), spring settling patterns depended on conditions when the birds arrived: ring recoveries were concentrated to the south and west parts of the breeding range in wet, cool years, and to the north and east in dry, warm years (when wetlands were fewer and smaller than usual) (Wernham et al., 2002). Depending on shallow waters, Teal are clearly sensitive to local conditions, whether drought, flood or freeze, which involves them at times either in continual movement or alternatively in residency for weeks on end, all manifest on a continental scale. Teal show low site fidelity in both breeding and wintering areas, and individuals may be found in different winters at localities hundreds or thousands of kilometres (up to 3500 km) apart. The same holds for some diving ducks, with individual Common Pochards (Aythya ferina), Tufted Ducks (Aythya fuligula) and others found up to several hundred kilometres apart in different winters (Figure 21.8; Wernham et al., 2002). In Common Pochard breeding dispersal distances of 200 600 km have also been noted, and in female Tufted Ducks up to 2500 km, but only a small proportion of females made such long moves (Blums et al., 2002). During hard winters many ducks appear in greater numbers than usual in milder southern and western parts of the European continent. Ring recovery distances of several ducks (Eurasian Wigeon (Anas penelope), Teal, Northern Pintail, Common Pochard and Tufted Duck) were greater in cold winters than in mild ones, and greater in cold spells than in equivalent mild periods (Ridgill & Fox, 1990). Other species showed no significant differences. Such hard weather (or ‘escape’) movements were associated with greater mortality than usual, but this may have resulted from greater vulnerability to hunting. A measure of the extent to which some dabbling ducks wander in different years is given by the many individuals of Mallard, Wigeon and Pintail that were ringed in Western Europe and later recovered in the furthest parts of eastern Asia (Spina & Clark, 2006). Such moves are reminiscent of those of boreal finches found at opposite ends of the Eurasian or North American landmasses in different winters (Chapter 20). The numbers of waterfowl wintering near the northern limits of the wintering range depend on ice cover, which normally reaches its greatest extent in February March. Many more birds stay in mild winters, with most open water, than in more severe winters (see Hario et al., 1993 for southwest Finland). This holds for sea ducks as well as for freshwater species. In many regions, recent warmer winters have resulted in waterfowl wintering further north than previously (Lehikoinen & Jaatinen, 2012, Chapter 23). Access to food clearly has a big influence on the winter distributions of ducks, again emphasizing the facultative nature of at least parts of their migrations. As well as ducks, other wetland birds are likely to be influenced by fluctuating wetland conditions, in the southern continents as well as the northern ones, with the most variable conditions in Australia (Chapter 17).

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FIGURE 21.8 Recovery locations of Pochards (Aythya ferina) ringed in Britain in winter and found elsewhere in a later winter, showing that individuals can be found in widely separated areas in different winters. Only movements greater than 20 km are shown. There were 128 movements over 20 km and another 29 under 20 km. Modified from Wernham et al. (2002).

CONCLUDING REMARKS All the species discussed above whether owls, raptors or ducks show similar behaviour in response to the fluctuating and sporadic nature of the resources on which they depend. The rodent-eaters and the ducks tend to concentrate each year in areas of favourable conditions, and migrate variable distances, moving towards milder climes in autumn, often in several stages, separated by weeks of residence. Some such species also migrate variable distances in spring, partly because many individuals settle in different parts of the breeding range each year, depending on conditions encountered on route. This flexible settling behaviour differs strikingly from those species in which individuals occupy fixed breeding and wintering areas from year to year, but it is adaptive for the species concerned, which face unpredictable variations in habitat or feeding conditions from year to year, in either breeding or non-breeding seasons or both. The hare-eating Northern Goshawk and Great Horned Owl show similar features but tend not to change their breeding areas from year to year. This can be attributed to their main prey species fluctuating in synchrony over almost the whole boreal region, giving no clear advantage to breeding dispersal, and thus contrasting with other irruptive species which in any given year can expect to find different conditions in different parts of their breeding range. Irruptive migrations have been associated with either high numbers (following good breeding success) or food shortage. In the Rough-legged Buzzard, in which heavy movements have shown roughly 4-year periodicity, the big years must be dependent on high production of young (associated with good prey supplies), because this species apparently vacates its breeding range totally in winter, regardless of local food supply. A large proportion of young was evident every 3 4 years among Rough-legged Buzzards passing through Falsterbo in Sweden (Kjelle´n, 2019). High population levels (as opposed to crashes in lemming numbers) have also been suggested as underlying major irruptions of Snowy Owls in eastern North America (Robillard et al., 2016). However, some other species, such as Great Grey Owls, Great Horned Owls and Goshawks, have left the breeding range in big numbers following poor breeding years, as indicated by the small proportions of young among the emigrants. Nevertheless, these two situations have the same basic cause, namely a state of imbalance between the birds and their food supply, with large-scale emigration stimulated whenever current numbers greatly exceed the prevailing food supply.

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SUMMARY In northern regions, densities of small rodents normally fluctuate on an approximate 3 5 year cycle, but the peaks occur in different years in different regions. The raptors and owls that depend on cyclic rodents may breed or winter in widely separated areas in different years, wherever prey are plentiful at the time. Some owl species that exploit sporadic rodent supplies move around mainly within the breeding range (e.g., Boreal Owl, Northern Hawk Owl), but in other owl and raptor species, at least part of the population migrates to lower latitudes for the winter, thereby avoiding the worst effects of snow cover. These birds return to the breeding range each spring, settling wherever voles are plentiful at the time (e.g., Short-eared Owl and Long-eared Owls, Common Kestrel, Northern, Hen and Pallid Harriers). In years of widespread food shortage (relative to numbers), some rodent predators leave their breeding range in large numbers, appearing in more southern areas as irruptions. In eastern North America, irruptions of Snowy Owls, which have been well documented since 1880, have occurred every 3 5 years, at a mean interval of 3.9 years. Similar 3- to 5-year periodicity has been noted in the movements of some other rodent-eating owl and raptor species in parts of North America and Europe. In North America, Snowshoe Hares fluctuate greatly in numbers, with roughly 10-year periodicity, more or less synchronized over the whole boreal region. Irruptions of Northern Goshawks and Great Horned Owls, which prey primarily upon Snowshoe Hares, have occurred for 1 3 years at a time, coinciding with known lows in the hare cycle. The movements of ducks are influenced by the fluctuating availability of suitable wetlands and associated food supplies, as influenced particularly by summer drought and winter ice. According to the types of habitat they occupy, species show varying degrees of site fidelity, and in some species, distribution patterns change markedly from year to year. This is especially true of species that occupy shallow, ephemeral waters which disappear altogether in dry years. Many individuals breed or winter in widely separated areas in different years, and migrate further in some years than in others. These species provide further evidence for the importance of prevailing environmental conditions in influencing bird movement patterns.

REFERENCES Adamcik, R. S., Todd, A. W. & Keith, L. B. (1978). Demographic and dietary responses of Great Horned Owls during a Snowshoe Hare cycle. Can. Field Nat. 92: 156 66. Andersson, M. (1976). Population ecology of the long-tailed Skua (Stercorarius longicaudus). J. Anim. Ecol. 45: 537 59. Andersson, M. (1980). Nomadism and site tenacity as alternative reproductive tactics in birds. J. Anim. Ecol. 49: 175 84. Bairlein, F. (1985). Dismigration und Sterblichkeit in Su¨ddeutschland beringter Schleiereulen (Tyto alba). Vogelwarte 33: 81 108. Blums, P., Nichols, J. D., Hines, J. E. & Mednis, A. (2002). Sources of variation in survival and breeding site fidelity in three species of European ducks. J. Anim. Ecol. 71: 438 50. Bull, E. L. & Duncan, J. R. (2020). Great Gray Owl (Strix nebulosa), version 1.0. In S. M. Billerman). . Ithaca, NY, Cornell Lab. of Ornithology. Cave´, A. J. (1968). The breeding of the Kestrel, Falco tinnunculus L., in the reclaimed area Oostelijk Flevoland. Netherlands J. Zool., Lond. 18: 313 407. Cheveau, M., Drapeau, P., Imbreau, L. & Bergeron, Y. (2004). Owl winter irruptions as an indicator of small mammal population cycles in the boreal forest of eastern North America. Oikos 107: 190 8. Chitty, H. (1950). Canadian arctic wildlife enquiry, 1943 49, with a summary of results since 1933. J. Anim. Ecol. 19: 180 93. Court, G. S., Bradley, D. M., Gates, C. C. & Boag, C. C. (1988). The population biology of Peregrine Falcons in the Keewater District of the Northwest Territories, Canada. Pp. 729 39 in Peregrine Falcon populations. Their management and recovery (eds T. J. Cade, J. H. Enderson, G. J. Thelander, & C. M. White). Boise, The Peregrine Fund.

Cramp, S. (1985). Handbook of the birds of Europe, the Middle East and North Africa. Vol. Vol. 4. Oxford, Oxford University Press. Cramp, S. & Simmons, K. E. L. (1980). Handbook of the birds of Europe, the Middle East and North Africa. Vol. Vol. 2. Oxford, Oxford University Press. Davis, D. E. (1937). A cycle in Northern Shrike emigrations. Auk 54: 43 9. Davis, D. E. (1949). Recent emigrations of Northern Shrikes. Auk 66: 293. Davis, D. E. & Morrison, M. L. (1987). Changes in cyclic patterns of abundance in four avian species. Am. Birds 4: 1341 7. Duncan, J. R. (1992). Influence of prey abundance and snow cover on Great Grey Owl breeding dispersal. M.Sc. Thesis, Winnipeg, University of Manitoba. Duncan, J. R. (1997). Great Grey Owls (Strix nebulosa nebulosa) and forest management in North America: a review and recommendations. J. Raptor Res. 31: 160 6. Duncan, J. R. & Duncan, P. A. (2020). Northern Hawk Owl (Surnia ulula), version 1.0. In S. M. Billerman). . Ithaca, NY, Cornell Lab. of Ornithology. Elton, C. S. (1942). Voles, mice and lemmings. Oxford, Oxford University Press. Fuller, M., Holt, D. & Schueck, L. (2003). Snowy Owl movements: variation on a migration theme. Pp. 359 66 in Avian Migration (eds P. Berthold, E. Gwinner, & E. Sonnenschein). Berlin, Springer-Verlag. Galushin, V. M. (1974). Synchronous fluctuations in populations of some raptors and their prey. Ibis 116: 127 34. Garcia-Heras, M.-S., Arroyo, B., Mougeot, F., Bildstein, K., Therrien, J.-F. & Simmons, R. E. (2019). Migratory patterns and settlement areas revealed by remote sensing in an endangered intra-African migrant, the Black Harrier (Circus maurus). PLOS ONE 14 (1): e0210756.

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Hagen, Y. (1969). Norwegian studies on the reproduction of birds of prey and owls in relation to micro-rodent population fluctuations. Fauna 22: 73 126. Hamerstro¨m, F. (1969). A harrier population study. Pp. 367 83 in Peregrine Falcon populations: their biology and decline in Peregrine Falcon populations: their biology and decline (ed. J. J. Hickey). Madison, University of Wisconsin Press. Hanski, I., Hansson, L. & Henttonen, H. (1991). Specialist predators, generalist predators, and the microtine rodent cycle. J. Anim. Ecol. 60: 353 67. Hario, M., Lammi, E., Mikkola, M. & So¨dersved, J. (1993). Annual ˚ land Islands fluctuations in numbers of wintering waterfowl in the A in 1968-92. Suomen Riista 39: 21 32. Harvey, P. V. & Riddiford, N. (1996). An uneven sex ratio of migrant Long-eared Owls. Ringing Migration 11: 132 5. Henny, C. J. (1973). Drought displaced movement of North American Pintails into Siberia. J. Wildl. Manage. 37: 23 9. Hepp, G. R. & Hines, J. E. (1991). Factors affecting winter distribution and migration distance of Wood Ducks from southern breeding populations. Condor 93: 884 91. Hilde´n, O. & Helo, P. (1981). The Great Grey Owl Strix nebulosa a bird of the northern taiga. Ornis Fenn 58: 159 66. Hilde´n, O. & Solonen, T. (1987). Status of the Great Grey Owl in Finland. Pp. 116 20 in Biology and conservation of Northern Forest Owls (eds R. W. Nero, R. J. Clark, R. J. Knapton, & R. H. Hamre). Fort Collins, CO, USDA For. Gen. Tech. Rep. RM-142. Co. Holt, D. W., Larson, M. D., Smith, N., Evans, D. L. & Parmelee, D. F. (2020). Snowy Owl (Bubo scandiacus), version 1.0. In S. M. Billerman). . Ithaca, NY, Cornell Lab. of Ornithology. Ho¨rnfeldt, B. (1978). Synchronous population fluctuations in voles, small game, owls and tularemia in northern Sweden. Oecologia 32: 141 52. Houston, C. S. (1999). Dispersal of Great Horned Owls banded in Saskatchewan and Alberta. J. Field Ornithol. 70: 343 50. Houston, C. S. & Francis, C. M. (1995). Survival of Great Horned Owls in relation to the Snowshoe Hare cycle. Auk 112: 44 59. Johnson, D. H. & Grier, J. W. (1988). Determinants of breeding distributions of ducks. Wildl. Monogr. 100: 1 37. Jones, C. D. (2005). The Ontario Great Grey Owl irruption of 2004 2005: numbers, dates and distribution. Ontario Birds 23: 106 21. Keith, L. B. & Rusch, D. H. (1988). Predation’s role in the cyclic fluctuations of Ruffed Grouse. Proc. Int. Ornithol. Congr. 19: 699 732. Keith, L. B. (1963). Wildlife’s ten-year cycle. Madison, WI, University Wisconsin Press. Kerlinger, P., Lein, M. R. & Sevick, B. J. (1985). Distribution and population fluctuations of wintering Snowy Owls (Nyctea scandiaca) in North America. Ecology 63: 1829 34. Kjelle´n, N. (2019). Migration counts at Falsterbo. Vol. 32/1 2, pp. 27 37). Sweden, Bird Census News27 37. Korpima¨ki, E. (1986). Gradients in population fluctuations of Tengmalm’s owl Aegolius funereus in Europe. Oecologia 69: 195 201. Korpima¨ki, E. (1992). Population dynamics of Fennoscandian owls in relation to wintering conditions and between-year fluctuations of food. Pp. 1 10 in The ecology and conservation of European Owls (eds C. A. Galbraith, I. R. Taylor, & S. Percival). Edinburgh, Joint Nature Conservation Committee.

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Nero, R. W., Copland, H. W. R. & Mezibroski, J. (1984). The Great Grey Owl in Manitoba, 1968 83. Blue Jay 42: 129 90. Newton, I. (1979). Population ecology of raptors. Berkhamsted, Poyser. Newton, I. (1998). Population limitation in birds. London, Academic Press. Newton, I. (2002). Population limitation in Holarctic owls. Pp. 3 29 in Ecology and conservation of owls (eds I. Newton, R. Kavanagh, J. Olson, & I. R. Taylor). Collingwood, VIC, CSIRO Publishing. Newton, I. (2003). The Speciation and biogeography of birds. London, Academic Press. Newton, I. (2008). The Migration Ecology of Birds (1st ed.). London, Academic Press. Nichols, J. D., Reinecke, K. J. & Hines, J. E. (1983). Factors affecting the distribution of Mallards wintering in the Mississippi Alluvial Valley. Auk 100: 932 46. Peck, M. K. & Murphy, G. B. (2005). The Ontario Great Grey Owl irruption of 2004 2005: mortality, sex, moult and age. Ontario Birds 23: 122 37. Petty, S.J. (1992). Ecology of the Tawny Owl Strix aluco in the spruce forests of Northumberland and Argyll. Ph.D. Thesis, Milton Keynes, Open University. Petty, S. J. (1999). Diet of Tawny Owls (Strix aluco) in relation to Field Vole (Microtus agrestis) abundance in a conifer forest in northern England. J. Zool. Lond. 248: 451 65. Pitelka, F. A., Tomich, P. Q. & Treichel, G. W. (1955). Breeding behaviour of jaegers and owls near Barrow, Alaska. Condor 57: 3 18. Pospahala, R. S., Anderson, D. R. & Henny, C. J. (1974). Population ecology of the Mallard. II Breeding habitat conditions, size of breeding populations, and production indices. Washington, DC, U. S. Fish & Wildlife Service, Resource Publication 115. Potapov, E. R. (1997). What determines the population density and reproductive success of Rough-legged Buzzards, Buteo lagopus, in the Siberian tundra? Oikos 78: 362 76. Rasmussen, J. L., Sealy, S. G. & Cannings, R. J. (2020). Northern Sawwhet Owl (Aegolius acadicus). In A. F. Poole). . Ithaca, NY, Cornell Lab. of Ornithology, version 1.0. Ridgill, S. C. & Fox, A. D. (1990). Cold weather movements of waterfowl in western Europe. Slimbridge, International Waterfowl and Wetlands Research Bureau, IWRB Special Publication 13. Robillard, A., Gauthier, G., Therrien, J.-F. & Beˆty, J. (2018). Wintering space use and site fidelity in a nomadic species. J. Avian Biol, 49. Available from https://doi.org/10.1111/jav-10707. Robillard, A., Therrien, J. F., Gauthier, G., Clark, K. M. & Beˆty, J. (2016). Pulsed resources at tundra breeding sites affect winter irruptions at temperate latitudes of a top predator, the Snowy Owl. Oecologia 181: 423 33. Rohner, C. (1995). Great Horned Owls and Snowshoe Hares what causes the time-lag in the numerical response of predators to cyclic prey. Oikos 74: 61 8. Rohner, C. (1996). The numerical response of Great Horned Owls to the Snowshoe Hare cycle: consequences of non-territorial ‘floaters’ on demography. J. Anim. Ecol. 65: 359 70. Santonja, P., Mestre, I., Weidensaul, S., Brinker, D. Huy, S. et al. (2018). Age composition of winter irruptive Snowy Owls in North America. Ibis 161: 211 15. Saurola, P. (1983). Movements of Short-eared Owl (Asio flammeus) and Long-eared Owl (A. otus) according to Finnish ring recoveries. Lintumies 18: 67 71.

Saurola, P. (1987). Mate and nest-site fidelity in Ural and Tawny Owls. Biology and conservation of northern forest owls (eds. R. W. Nero, R. J. Clark, R. J. Knapton & R. H. Hamre). Fort Collins, CO. USDA Forestry Service General Technical Report RM-142. Saurola, P. (1989). Ural Owl. Pp. 327 45. In I. Newton). . London, Academic Press. Saurola, P. (1997). Monitoring Finnish owls 1982 1996: methods and results. Pp. 363 80 in Biology and conservation of owls of the northern hemisphere (eds J. R. Duncan, D. H. Johnson & T. H. Nicholls). Second International Symposium, February 5 9, 1997. Winnipeg, Manitoba, Canada. United States Department of Agriculture. Saurola, P. (2002). Natal dispersal distances of Finnish owls: results from ringing. Pp. 42 55 in Ecology and conservation of owls (eds I. Newton, R. Kavanagh, J. Olsen, & I. Taylor). Collingwood, VIC, CSIRO Publishing. Schu¨z, E. (1945). Der europa¨ischer Rauhfussbuzzard, Buteo l. lagopus (Bru¨nn.), als Invasionsvogel. Jahr. Vereins Vaterlandische Natuurkunde Wu¨rttemburg 97 101: 125 50. Shelford, V. E. (1945). The relation of Snowy Owl migration to the abundance of the Collared Lemming. Auk 62: 592 6. Schmidt, R. C. & Vauk, G. (1981). Zug Ringfunde auf Helgoland durch ziehender Waldohreulen und Sunpfohreulen (Asio otus and A. flammeus). Vogelwelt 102: 180 9. Smith, R. I. (1970). Response of Pintail breeding populations to drought. J. Wildl. Manage. 34: 943 6. Smith, N. (1997). Observations of wintering Snowy Owls (Nyctea scandiaca) at Logan Airport, East Boston, Massachusetts from 1981 1997. Pp. 591 597 in Biology and conservation of owls of the northern hemisphere (eds. J. R. Duncan, D. H. Johnson & T. H. Nicholls). Second International Symposium, February 5 9, 1997. Winnipeg, Manitoba. United States Department of Agriculture. Solonen, T. (1986). Breeding of the Great Grey Owl Strix nebulosa in Finland. Lintumies 21: 11 18. Sonerud, G. (1984). Effect of snow cover on seasonal changes in diet, habitat and regional distribution of raptors that prey on small mammals in boreal zones of Fennoscandia. Holarctic Ecol 9: 33 47. Sonerud, G. (1997). Hawk owls in Fennoscandia: population fluctuations, effects of modern forestry, and recommendations on improving foraging habitats. J. Raptor Res. 31: 167 74. Sonerud, G. A., Solheim, R. & Prestrud, K. (1988). Dispersal of Tengmalm’s owl Aegolius funereus in relation to prey availability and nesting success. Ornis Scand 19: 175 81. Speirs, J. M. (1939). Fluctuations in numbers of birds in the Toronto Region. Auk 56: 411 19. Spina, F. & Clark, J. (2006). EURING: its role in flyway and migration atlases. Pp. 569 73 in Waterbirds around the world (eds G. C. Boere, C. A. Galbraith, & D. A. Stroud). Edinburgh, The Stationery Office. Stenseth, N. C. (1999). Population cycles in voles and lemmings: density dependence and phase dependence in a stochastic world. Oikos 87: 427 61. Taylor, I. (1994). Barn owls. Predator prey relationships and conservation. Cambridge, University Press. Terraube, J., Arroyo, B. E., Bragin, A., Bragin, E. & Mougeot, F. (2012). Ecological factors influencing the breeding distribution and success of a nomadic, specialist predator. Biodivers. Conserv. 21: 1835 52. Therrien, J.-F., Gauthier, G. & Beˆty, J. (2011). An avian terrestrial predator of the Arctic relies on the marine ecosystem during winter. J. Avian Biol. 42: 363 9.

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Therrien, J.-F., Gauthier, G., Pinaud, D. & Beˆty, J. (2014). Irruptive movements and breeding dispersal of Snowy Owls: a specialized predator exploiting a pulsed resource. J. Avian Biol. 45: 536 44. Therrien, J.-F., Pinaud, D., Gauthier, G., Lecompte, N., Bildstein, K. L. & Beˆty, J. (2015). Is pre-breeding prospecting behavior affected by snow cover in the irruptive Snowy Owl? A test using state-space modelling and environmental data annotated via movebank. Movement Ecol. 3 (2015): 1. Village, A. (1981). The diet and breeding of Long-eared Owls in relation to vole numbers. Bird Study 28: 215 24. Village, A. (1987). Numbers, territory size and turnover of Short-eared Owls Asio flammeus in relation to vole abundance. Ornis Scand 18: 198 204.

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Village, A. (1990). The Kestrel. Calton, T. & A. D. Poyser. Wernham, C. V., Toms, M. P., Marchant, J. H., Clark, J. A., Siriwardena, G. M. & Baillie, S. R. (2002). The migration atlas: movements of the birds of Britain and Ireland. London, T. & A. D. Poyser. Whalen, D. M. & Watts, B. D. (2002). Annual migration density and stopover patterns of Northern Saw-whet Owls (Aegolius acadicus). Auk 119: 1154 61. Wijnandts, H. (1984). Ecological energetics of the Long-eared Owl (Asio otus). Ardea 72: 1 92. Wiklund, C. G., Kjelle´n, N. & Isakson, E. (1998). Mechanisms determining the spatial distribution of microtine predators on the Arctic tundra. J. Anim. Ecol. 67: 91 8.

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Part 4

Evolution of movement patterns

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Chapter 22

Evolution and inheritance of migratory behaviour

Eurasian Blackcap (Sylvia atricapilla), used in experiments on the heritability of migratory behaviour Bird migration, in its more highly developed forms, is both too regular in its performance and too provident in its anticipation of events to be conceivable as being created anew each year by the mere pressure of external forces. . . . Migration must, then, be a recurrent manifestation of a mode of behaviour which has become inherent in the nature of various species. A. Landsborough Thomson (1936).

Migration might be expected to occur wherever individuals survive or reproduce more successfully if they move seasonally between different areas than if they remain in the same place year-round (Lack, 1954). The usual reason why breeding areas become unsuitable during part of the year is lack of food. Such shortages occur for many birds because plant growth stops and many kinds of invertebrates die, hibernate or become inaccessible under snow and ice. At high latitudes, daylengths also shorten in winter to such an extent that many diurnal birds would have too little time to get enough food, even if it were available. Hence, the purpose of the autumn exodus from high latitudes is fairly obvious. The reason why birds leave their wintering areas to return in spring is less obvious because many wintering areas seem able to support them during the rest of the year. But if no birds migrated to higher latitudes in spring, these latitudes would remain almost empty of many species, and a large seasonal surplus of food could go largely unexploited. Under these circumstances, any individuals that moved to higher latitudes, with increasing food and longer days, might raise more offspring than if they stayed at lower latitudes and competed with birds resident there. So whereas the advantage of autumn migration can be seen as improved winter survival, dependent on better food supplies in winter quarters, the main advantage of spring migration can be seen as improved breeding success, dependent on better food The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00018-X © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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supplies in summer quarters. Compared to survival, reproduction also has more stringent requirements in terms of specific food needs and predation avoidance. In effect, migration reduces the seasonal fluctuations in food supplies to which a population could otherwise be exposed. Species that breed in one hemisphere and ‘winter’ at an equivalent latitude in the opposite hemisphere, where the seasons are reversed, would seem to profit from the best of both worlds. Further, some habitats offer abundant food to facilitate survival but cannot be used for reproduction, with tidal mudflats used by wintering shorebirds providing an example. Migration thus also enables birds to make use of different and widely separated habitats for survival and reproduction (and sometimes also for moulting, Chapter 17). While seasonal change in food supply is clearly influential for bird migration, this does not rule out effects of other factors, such as reduced predation (Fretwell, 1980; McKinnon et al., 2010), parasitism (Piersma, 1997; Balstad et al., 2021), or competition for food or other resources (Cox, 1968). All these pressures may decline with increasing latitude because of the general latitudinal decline in the total numbers of animal species, whether these animals act as predators, parasites or competitors. At one time or another, they have been proposed as contributing to the evolution of migration, and for predation some evidence is available for a latitudinal decline, at least in one region (McKinnon et al., 2010). Whatever the main selective forces, therefore, the migratory habit ensures over the long term that species in seasonal environments adapt and maintain movement patterns that allow individuals to survive and breed better than if they remained in the same area year-round. The main fitness cost of migration is seen as the increased mortality associated with the journey itself (Chapter 31). Most recorded mortality incidents relate to storms and unseasonable weather, which can kill thousands of birds at a time, sometimes causing widespread reductions in breeding numbers. Other risks include exposure at lower latitudes to a greater range of pathogens, predators and competitors, as mentioned above, all of which could have additional fitness costs. For the migratory habit to persist, therefore, despite the risks involved in long journeys, the net benefits to individuals of moving both ways must outweigh the costs. Conversely, year-round residence presumably persists in populations where the net benefits of staying in one area outweigh the costs of seasonal movement. At the population level, one incidental consequence of migration, it may be assumed, is greater overall numbers. Because the breeding area could not support that number of birds year-round, the overall population is larger as a result of seasonal movement. For many species, the geographical range is also larger because birds can breed in areas where they could not remain year-round, nesting at higher latitudes only by virtue of migration. Species that are entirely migratory, with separate breeding and wintering ranges, exist today only through their seasonal movements. Other animals which are less mobile than birds usually cope with seasonal shortages in other ways, notably by hibernation a metabolic shutdown involving torpor. Hibernation is known only in a single bird species, the North American Poorwill (Phalaenoptilus nuttallii), but shorter periods of torpidity occur in other species (Chapter 1).

ADAPTATIONS FOR MIGRATION Assuming that migration evolved as an adaptation to life in seasonal environments, it may have occurred among birds for a long time, perhaps even in the earliest species. Nevertheless, the ice ages evidently played a major role in its recent development in high-latitude regions. At the height of the last glaciation, much of the northern hemisphere above about 50 N was covered with ice and generally devoid of terrestrial life. Colonization of these areas by plants and animals followed the retreat of the ice which began about 12,000 years ago and continues to this day. This means that some of the longest and most impressive of current bird migrations must have developed within this period, as birds spread gradually from lower to higher latitudes to occupy the newly available habitats. At the start of this process, when birds were confined to lower vegetated latitudes, they may have been residents or shorter-distance migrants. Moreover, the last 2.5 million years have seen more than 20 glacial cycles of varying severity, so bird migration systems could have been in continual flux over this whole period. Many populations are likely to have passed through alternating sedentary and migratory phases, each lasting for many thousands of years. As explained later, the ability to migrate was perhaps ever-present in these populations, becoming suppressed or re-activated according to prevailing conditions and the changing pressures of natural selection (Berthold, 1999; Pulido, 2007). It would be misleading to divide bird species neatly into migratory and sedentary. Both types of behaviour can be found in a single species or even in a single population. In the northern hemisphere, many widely distributed bird species are completely migratory in the north of their breeding range, completely resident in the south, and partially migratory in between, with the proportion of birds leaving any particular breeding locality corresponding to the degree of seasonal reduction in food supplies (Chapter 16). Where populations are entirely migratory or entirely resident, their behaviour is usually considered obligatory, and under firm genetic control, with individuals behaving in the same way

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every year. In contrast, partial migration1 can apparently arise in two different ways. In one way ‘obligatory migratory’ and ‘obligatory resident’ individuals occur intermixed in the same breeding area but again behave consistently from year to year. In the other way, the behaviour of each individual is optional (facultative), enabling it to behave differently in different circumstances, staying in the breeding area in years when conditions are favourable there, and leaving in other years (Chapter 13). Although migration may require adaptations in morphology, physiology and behaviour, it is not hard to see how it might have evolved because intermediate stages still occur. For instance, some bird species do not migrate at all, others travel only short distances, and yet others long distances. The full range of variation can be found among different populations of the same species, or even among individuals from the same population, as mentioned above. Further, the main adaptations needed for long-distance migration, such as seasonal fat reserves, timing mechanisms and orientation skills, are all found in less developed form in non-migratory birds, as well as in other animals. These features are all necessary for effective migration to develop but could have arisen independently of migration, in different contexts. The main feature that sets migration apart from other long-distance movements is that it involves a two-way journey in more or less fixed directions. The ability to perform a return movement is necessary before any migration pattern (as defined above) can evolve. But all birds are able to return repeatedly to their nests, as well as to particular feeding or roosting sites, and the same is true for other animals. In addition, many non-migratory birds move locally away from their nesting areas after each breeding season and return for the next. Even juveniles, after wandering widely in the non-breeding season, normally return to settle near their natal sites to breed, and other non-migratory birds revisit the same wintering sites in successive years (Chapter 19). In resident populations, such movements are fairly short and localized, but they provide a basis from which the longer return movements of migration might evolve, step by step, each extension being beneficial in its own right. The ability of even resident birds to return to their home areas from at least several kilometres away has been shown repeatedly in experiments in which individuals were trapped, transported ˚ kesson, 2003). Many of the displaced birds quickly to a different location and released (Chapter 10; Matthews, 1968; A re-appeared at their capture sites. There is, however, a difference between the needs of short-distance and long-distance moves. In theory, shortdistance moves could be performed entirely on the basis of learned landscape features, as a bird gets to know its local area. But to return from long distances requires something more, an ability to orientate by different globally available signposts, as provided, for example by celestial or magnetic cues. Such an ability is almost certainly inherent to some degree in all birds because it is present in lower animals, including the reptiles from which birds evolved. Similarly, it is not hard to imagine how, given a sense of location, directional preferences could evolve from random dispersal movements. In seasonal environments any birds which move long distances after breeding are more likely to meet favourable conditions in some directions than in others. In time, though natural selection, this should promote the development of an inherent component to directional preferences (mainly southward in the northern hemisphere). It is not just the directions but also the distances, and hence the specific wintering areas, that could be fixed in this way by natural selection, the birds from each population wintering wherever they can reach and survive best, taking account of the mortality costs of getting there and back. Only in populations which on balance have an equal chance of finding food in any direction (like some nomadic ones) is no directional preference likely to become fixed by natural selection. All birds have timing mechanisms which ensure that they breed and moult at appropriate and consistent times of year, and in migrants, such mechanisms also promote movements at appropriate dates. They ensure that birds arrive in their breeding areas each spring in time to take advantage of the favourable season and leave after breeding in late summer or autumn before deteriorating conditions reduce their survival chances. These timing mechanisms are basically endogenous (within the bird) but are entrained by seasonal changes in daylength and modified by other environmental conditions (Chapter 12). Birds travelling long distances over unfavourable terrain often lay down substantial body reserves for the flight. Accumulation of body fat is common in all kinds of animals in preparation for predictable periods of privation. Many birds lay down body reserves in preparation for breeding or in winter in association with severe weather and long nights. In accumulating migratory fat, therefore, birds are merely modifying a pre-existing facility for a different purpose, rather than developing a completely new adaptation. Long-distance migration can often take several weeks, a period which may involve modification of other events in the annual cycle, such as moult (Chapter 12). Most small passerines, resident and migrant, moult in summer after breeding, but some long-distance migrants set off soon after breeding and postpone their moult until after they have 1. The term partial migration is used here for the individual variation in behaviour within a breeding population, not for the variation between different populations of the same species.

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reached their tropical wintering areas. Among the Eurasian warblers, the summer moult seems to be the ancestral pattern, while winter moult has apparently evolved independently 7 10 times within this group (Svensson & Hedenstro¨m, 1999). As these birds colonized northern breeding areas in post-glacial times, thereby lengthening their migrations, summer moult could have given way to winter moult. Other patterns, such as split moults and twiceyearly moults, also seem to have evolved from the ancestral state of summer moult, in adaptation to various migration patterns. Evolutionary transitions from resident to migratory or vice versa, as well as changes in the extent and pattern of migration, apparently occur without phylogenetic constraint: residents, short-distance migrants and longdistance migrants often occur among closely related species, or even among different populations of the same species, occupying different parts of a breeding range. Migration also involves morphological changes as birds become more adapted for long-distance flight. Migratory species usually have longer and more pointed wings, shorter square-ended tails and smaller bodies than closely related residents (Figure 22.1; Leisler & Winkler, 2003). Pointed wings and short tail are most efficient during level flight because they reduce drag, whereas more rounded wings and longer tail give greater maneuverability and more rapid lift at take-off (Kerlinger, 1989; Rayner, 1990). Wing shape is thus a compromise between conflicting demands, the balance being drawn differently in resident and migratory populations. Change is achieved mainly by altering the relative lengths of different feathers, but bone lengths (femur, ulna and carpo-metatarsus) also correlate with migratory distance, as does the size of the sternum and coracoid bones, giving greater surfaces for flight muscle attachment in longdistance migrants (Calmaestra & Moreno, 2000). Correlations between morphology and migration distance are apparent within several groups of birds of widely different body shapes (Winkler & Leisler, 1992; Marchette et al., 1995; Mo¨nkko¨nen, 1995; Lockwood et al., 1998; Leisler & Winkler, 2003). Such differences occur even between sedentary and migratory populations of the same species (Alerstam, 1990; Fiedler, 2005). For example among different populations of Eurasian Blackcaps (Sylvia atricapilla), with increasing migratory distance: (1) wing length, aspect ratio and wing pointedness increase; (2) wing load decreases; (3) slots on the wing tips become relatively shorter; (4) the alula becomes shorter in relation to wing length; and (5) the tail becomes shorter in relation to wing length. These changes are significantly greater than expected from the simple trend of increasing body mass from southern to northern populations (Fiedler, 2005). Moreover, it is not only external features which are modified in migratory birds but also internal ones, including the brain. Migratory birds have a more highly developed hippocampus, and a more effective spatial memory than non-migratory ones, another difference evident in comparisons between resident and migratory populations of the same species (Cristol et al., 2003). For the most part, then, migratory birds do not possess any fundamentally different adaptations from residents, whether orientation mechanisms, physiological, morphological or other features. Migration simply involves the further development or modification of features already present in non-migratory populations. However, one apparent novel feature is the evolution of narrow directional preferences to suitable wintering areas from the situation of no such preferences shown at the population level in dispersal and nomadism. Directional preference away from the breeding area is a heritable migratory trait in its own right, distinct from other traits (Bell, 2000). Each such inherited trait is amenable to the action of natural selection, either independently or in association with other traits. Moreover, all can be modified in an incremental manner, in which each small appropriate change brings fitness benefits. This is a firm basis from which the different movement patterns of birds, and their associated adaptations, can be shaped. FIGURE 22.1 The wing formulae of two Old World wetland warblers clearly fall into two groups rounded wings of the comparatively sedentary (or totally resident) Cetti’s Warbler (Cettia cetti) and pointed wings of the highly migratory Sedge Warbler (Acrocephalus schoenobaenus). Note the relative lengths of the outer flight feathers, which give greater ‘aspect ratios’ in the migrants. Modified from Mead (1983). See also Winkler & Leisler (1992).

Sedge Warbler

Cetti’s Warbler

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If existing bird movements were arranged in order of increasing specialization, the sequence might run: multidirectional one-way dispersal, nomadism, multi-directional return dispersal (including altitudinal movements), facultative return migration over restricted directions, and obligate return migration over restricted directions. Dispersal movements are performed by all bird species, usually by the young after they become independent of parental care, and at the population level they can occur in any direction from the starting point (Chapter 19). Nomadism can be regarded as a form of dispersal performed repeatedly through life and usually over longer distances, as birds apparently move in any direction from one area of temporary suitability to another (Chapter 17). Dispersive migration is also multidirectional but involves a return journey (Chapter 19). True return migrations across latitudes involve movements in restricted directions, whereas facultative movements are stimulated largely by conditions at the time, and hence vary from year to year, obligate movements occur consistently every year, usually between fixed breeding and wintering areas, being more firmly under endogenous control. They are also anticipatory, made in expectation of conditions to come. This may be the sequence in which the most impressive and fixed bird migrations have evolved. Listing the different types of bird movements in this way reinforces the point that migration itself (or any other type of movement) is not a trait in its own right, but an attribute made up of several components, each of which can be independently modified by natural selection to give the variety of movement patterns seen today. These variable traits are all prerequisites for the evolution of effective migration, but their origins are independent of migration. One important goal for comparative studies of migration should therefore be to identify the genes responsible for each component of migration and establish their distribution across different bird families.

ADAPTIVE TIMING Some food shortages are predictable because they occur at about the same time every year, in response to the changing seasons. This enables birds, through evolutionary mechanisms, to anticipate periods of shortage and to depart while they are still able to accumulate fat reserves for the journey. Similarly, birds can leave their wintering areas at a time that allows them to arrive in their breeding areas at an appropriate date in spring when breeding again becomes possible. Most migration is presumed to have evolved in response to these predictable seasonal changes in food supplies. Many migrants react to environmental cues such as daylength in conjunction with an endogenous calendar, in such a way that they can prepare for migration ahead of time (Chapters 12 and 13). On current understanding, this is the situation in obligate migrants in which the whole population leaves the breeding area each autumn in anticipation of a predictable loss of food supplies in the weeks to come. In facultative migrants, however, the proportion of birds that leaves the breeding range varies according to food and other conditions at the time. In such populations, food shortage would then act as both an ultimate and a proximate factor in influencing whether particular individuals migrate; food conditions might also influence the date of departure, the length of journey, and the date at which birds move on from place to place along the route. Such an immediate response allows for the fact that some food shortages are unpredictable in that they occur as a result of unseasonable extreme weather, fruitcrop failures and other irregular events. Because these shortages cannot be reliably anticipated, birds can only respond to conditions at the time, moving out as food gets scarce, and not always with the benefits of prior fat deposition.

PARTIAL MIGRATION Partial migration can be divided into obligate and facultative types (Chapter 13). In obligate partial migration, certain individuals in a population migrate some distance every year regardless of prevailing conditions, while other individuals remain resident. Particular individuals behave in the same way throughout their lives. This situation is presumed to occur where migratory behaviour is genetically controlled, and where there is no overwhelming advantage in staying or migrating. In some years, perhaps, the migrants do best and in others the residents so that in the long term both types persist in the same breeding area (Berthold & Querner, 1982b; Biebach, 1983; Pulido, 2011). Although they interbreed, mating may be assortative to some extent, if resident birds pair up in spring before the migrants arrive (eg see Bearhop et al., 2005). Such a dual strategy is often viewed as the crucial intermediate stage in the transition from full resident to full migrant, or vice versa (see later). In this system, the advantage of each type of behaviour depends partly on what other individuals do. If more and more birds became resident (say), the time would come when the winter food supply would not support them. Competition would then increase, leading to greater mortality in the resident sector, eventually tipping the balance in favour of migration. In this way, changes in the relative advantages of the two types of behaviour could ensure that the ratio of residents to migrants in any one population was kept roughly in line with local conditions (Lundberg, 1987).

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The relative advantages of resident versus migrant may change over the years if environmental conditions change, such as winter temperatures or winter food supplies in breeding areas (see Chapter 23 for examples). They may also differ between areas, and in many partial migrants a greater proportion of individuals migrates from higher than from lower latitudes. Obligate partial migration could thus be viewed as an ‘evolutionarily stable strategy’ because, with the appropriate ratio of migrants and residents in the local breeding population, in the long term the fitness pay-offs for both genotypes are balanced, and in the conditions prevailing no one type can completely replace the other (Berthold, 1984a; Kaitala et al., 1993). One relevant study involved European Shags (Gulosus aristotelis) on the east coast of Scotland (Grist et al., 2017). In this population, resident individuals had higher reproductive rates than migrants. On average, residents hatched their broods 6 days earlier and fledged 0.2 more chicks per year than migrants. Hatch date and breeding success also varied with a pair’s joint migratory strategy and resident resident pairs hatched their broods 12 days earlier than migrant migrant pairs and fledged 0.7 more chicks per year on average. The observed frequencies of migrant migrant and resident resident pairs in the population did not differ from those expected by chance, providing no evidence that mating was assortative with respect to migratory strategy. However, while in seven of the nine study years, the survival of residents and migrants was similar, in two winters with extreme weather events, embracing both breeding and wintering areas, migrants survived significantly better than residents (Acker et al., 2020). So strong reproductive selection against migration in several years contrasted with episodes of strong survival selection against residence in 2 other years, helping to maintain both types of behaviour in the population. Turning now to facultative partial migration, the same individuals may migrate in some years and not in others, depending on conditions at the time. Because birds compete and vary in dominance or feeding efficiency, some individuals are able to survive in conditions where others would perish unless they moved out (Kalela, 1954; Gauthreaux, 1978, 1982). In many partially migrant populations, a higher proportion of juveniles than adults, and of females than males, migrate (Chapter 18). This fits the dominance order in such populations so that when food is scarce, juveniles fare less well than adults and females less well than males. In this situation, facultative partial migration is a ‘conditional response’ to food supply, and the same individual can vary its behaviour according to its own circumstances (Smith & Nilsson, 1987; Schwabl & Silverin, 1990; Chapman et al., 2011; Kokko, 2011; Hegemann et al., 2015). Even if the migrants survive, on average, less well than residents, they survive better than they would have done if they had not migrated. In other words, migration is the optimal strategy for those individuals at the time, a behavior that could be selected from the benefits it brings. This conditional strategy seems much the commonest form of partial migration (Chapman et al., 2011). Take the European Robin (Erithacus rubecula) which is a facultative partial migrant in Belgium (Adriaensen & Dhondt, 1990). In one study, most males that nested in parks and gardens were resident year-round, whereas most males that nested in woodland were migratory, as were all females from both habitats. Resident males survived, on average, about three times better than migratory individuals (50% vs 17%), and even during the extremely cold winter of 1984 85, residents still survived best. In addition, resident males were much more likely than migratory ones to obtain a mate (74% vs 44%). On the basis of both survival and mating success, the expected reproductive success of resident males was 2 4 times greater than that of migratory males. So why did migration persist? In ecological jargon, partial migration was a ‘conditional strategy with unequal pay-offs’: if individuals could find a territory locally in which they had a good chance of surviving the winter, they could stay; if not, they had to migrate, for only then did they stand any chance of surviving the winter. On this basis, socially dominant individuals were more likely to become resident, and subordinate ones to migrate. This could explain why females migrated more than males, why resident and migratory males tended to use different breeding habitats, and why young of early broods were less migratory than those of later broods. So the argument is that each bird responds to conditions at the time in a way that maximizes its own survival chances. And as these conditions include competitive pressure from other individuals, migration becomes densitydependent: the more birds there are relative to resources, the greater the proportion that leaves for the winter. One review of partial migration in birds and other animals compared various fitness measures in residents and migrants from the same populations (Buchan et al., 2020). Twenty-three studies of 18 species provided 129 fitness measures. Of these, 73% showed higher fitness in residency, 22% in migrancy and 5% reported equal fitness in both. Among the bird species examined, all showed higher survival among residents, the benefits increasing with the number of years over which effects were calculated. The importance of residency may have been because these studies were made over a period of climate warming, when the relative advantage of residency in the species concerned was increasing, or because all or most of the studies involved populations in which migration was a conditional rather than obligate strategy (as in the Robins discussed above).

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Although most studies in this review showed that residents survived better than migrants, reproductive rates were not reported, so the two strategies could not be properly compared. However, in a partial migratory population of European Blackbirds (Turdus merula) studied over 7 years in Germany, migrant Blackbirds wintering in southern Europe had 16% higher probability of surviving the winter than residents remaining in Germany (Zun˜iga et al., 2017). A subsequent modelling exercise revealed that residents should have 61% higher breeding success than migrants to outweigh the survival costs of residency. This should have been possible if enough of the residents, present on breeding areas earlier in spring, were able to raise an extra brood. The two types of partial migration, involving an obligate genetic dimorphism in migratory tendency (with some individuals always migrating and others always not) or a facultative migration dependent on individual circumstances, are not necessarily mutually exclusive. They may represent extremes of a continuum, or both could operate to varying degrees in the same population (Lundberg, 1988). In addition, migration might be conceived as a split journey in which the first part was obligatory and under genetic control, and the second part was facultative and more under environmental control (Terrill, 1990). This would account for the fact that, in some migratory species, the whole population departs in autumn, but the distance that most individuals travel varies greatly from year to year depending on the conditions (especially food supplies) encountered on route (Chapter 20). Some researchers have distinguished between ‘breeding partial migration’ when residents and migrants interbreed in the same area as part of the same population (as in the examples above), and ‘non-breeding partial migration’ when residents and migrants co-exist in the non-breeding season and are separated geographically in the breeding season (Kaitala et al., 1993; Kokko & Lundberg, 2001; Gillis et al., 2008; Chapman et al., 2011). But this latter system is not true partial migration as originally conceived, which requires that residents and migrants breed in the same area, and at least occasionally with one another. The second situation is traditionally described as ‘winter sympatry’, and because populations separate in the breeding season, they do not interbreed.

THE GENETIC CONTROL OF MIGRATION: EXPERIMENTAL EVIDENCE For many years, ideas on the role of natural selection in shaping bird migration patterns were based on little more than surmise. One indication of genetic control was the year-to-year consistency in all aspects of the migratory behaviour of particular populations, including the timing, directions and distances travelled. Where young and old birds migrate together, the young could possibly learn from older birds the seasonal timing, migration routes and wintering areas. But in many species, the two age groups migrate independently of one another, sometimes weeks apart, giving little or no opportunity for cultural transmission of information. In experiments on some species, young birds were held in their natal area until all other individuals of their species had left, or transported outside their usual range. The young were then released. They were found from subsequent sightings and ring recoveries to have migrated in the direction normal for their population (Chapter 10). The only plausible explanation was that migratory directions were inherent. Other early evidence revealed a genetic difference between resident and migratory individuals in the same breeding population of Common Eiders (Somateria mollissima) (Milne & Robertson, 1965). The egg albumen proteins showed a genetic polymorphism, in which the ratios between two alleles differed between resident and migratory individuals. Field observations revealed that residents and migrants did not normally interbreed, because individuals of both types paired in winter, so were already assorted according to wintering area when they later met on their common breeding area. From the 1980s, the role of genetic factors in the control of migration has been shown experimentally, mainly by Peter Berthold and his colleagues, who found that Eurasian Blackcaps and other songbirds could be bred on a large scale in aviaries (Berthold & Helbig, 1992; Berthold, 1995, 1999). Different populations of Blackcaps varied from completely migratory to completely sedentary in different parts of the birds’ range. The various migratory populations also differed in their migration dates and the directions and distances travelled. Most of these traits could be measured in captive birds by assessing the timings and amounts of migratory restlessness (or Zugunruhe), a specific behaviour involving fluttering and wing-whirring which appears in caged birds mainly at migration seasons (Box 14.1). Directional preferences of individuals could be assessed by placing them in orientation cages and checking where they most frequently headed. Both restlessness and headings could be recorded automatically, as described in Chapter 2. The main finding was that when birds from different populations were cross-bred, the offspring showed migration features that were intermediate between those of their parents. Moreover, if individuals with particular traits were selected and bred together, these traits became enhanced in future generations. This held for the timing and duration of migratory restlessness and for directional preferences. The overriding implication was that all these aspects of migration were under genetic control and could thus be changed in the wild by natural selection, depending on the survival and reproductive benefits of different behaviours in the conditions prevailing. Crucial experiments are summarized below.

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Migratory inclination Experiments in which individuals showing high levels of migratory restlessness were paired together showed that the trait persisted or increased in the offspring. Similarly, when individuals showing low levels of restlessness were paired together, the trait persisted or decreased in the offspring. These findings confirmed for both Blackcaps and European Robins that the amount of migratory restlessness was to a large extent genetically pre-programmed (Berthold & Querner, 1981; Biebach, 1983). Moreover, cross-breeding of migrant with non-migrant strains (using Blackcaps from south Germany and the Cape Verde Islands) resulted in the partial transmission of migratory activity to 33% of the first-generation offspring, again indicating that the urge to migrate was inherited (Berthold et al., 1990). High or low levels of migratory restlessness (assumed to reflect migratoriness or sedentariness) could be selected for phenotypic uniformity within as few as 3 6 generations. More precisely, after three generations of selection, migratory behaviour was fixed in the migratory line, whereas selection over 5 6 generations was needed to produce an almost exclusively ‘resident’ stock. These experiments thus revealed not only high heritability in migratory behaviour but also how rapidly behaviour could change in response to strong selection pressure. In nature, selection is never likely to be that strong, so substantial changes would be expected to take longer, perhaps decades or more, depending partly on the longevity of the species concerned. In another study, Blackcaps from widely separated populations (southern Finland, southern Germany, southern France and the Canary Islands off North Africa) were hand-raised and tested under identical conditions. The proportion of migrants showing a given level of migratory restlessness among birds from the four areas differed markedly: from 100% of birds from Finland and Germany to 80% of those from southern France, and to only 23% of those from the Canary Islands. The number of nights of migratory restlessness shown by migratory individuals also differed between populations, declining from north to south (Figure 22.2; Berthold & Querner, 1981). Appropriate differences in physiology (moult and fat accumulation) and morphology (wing shape) were also found between the different populations (Berthold & Querner, 1982a). Cross-breeding of individuals from two of these populations (southern Germany and the Canary Islands) gave offspring of intermediate characteristics, again implying that migratory features were under genetic control (Figure 22.2). In a later experiment, a completely migratory population of captive Blackcaps became partially migratory in response to selection for lower migratory activity alone (Pulido & Berthold, 2010). In four generations of artificial selection on migratory activity, not only did the amount of activity decrease but the frequency of non-migrants increased, from zero in the parental and first generation of hybrids to 4.5% 13%, in the second to fourth generations. This result implied that a completely migratory population could evolve residency by selecting for lower amounts of migratory activity without the need to introduce ‘residency genes’ by mutation or gene flow. Among Blackcaps, Stonechats (Saxicola torquata) and Northern Wheatears (Oenanthe oenanthe) from different parts of the breeding range showed different migratory behavior in captivity, according to the journeys they make in the wild (Helm et al., 2005; Van Doren et al., 2017; Maggini & Bairlein, 2010; Bulte & Bairlein, 2013). Moreover, when birds from two populations of the same species showing different migratory behaviour were hybridized in captivity, their offspring showed features intermediate between those of the parent populations. This applied to the

FIGURE 22.2 Patterns of migratory activity (Zugunruhe) of Blackcaps (Sylvia atricapilla). (A) Activity of birds of four different populations. (B) Activity of birds of two of these populations and their hybrids. SFi birds from southern Finland, SG southern Germany, SFr southern France, CI Canary Islands. From Berthold & Querner (1981).

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timing, intensity and duration of spring and autumn migratory restlessness as measured in Stonechats (Helm et al., 2009; Van Doren et al., 2017), and to the levels of autumn fattening as measured in Wheatears (Maggini et al., 2017). This again implied genetic inheritance of these features. Intermediate patterns of behavior were also noted in hybrids between migratory Common Quail (Coturnix c. coturnix) and non-migratory Japanese Quail (Coturnix c. japonica) (Dere´gnaucourt et al., 2005), and in wild hybrids between Lesser Spotted Eagle (Clanga pomarina) and Greater Spotted Eagle (Clanga clanga) (Va¨li et al., 2018). These eagle hybrids were tracked on migration, and while their timing was closest to that of C. pomarina, their migration lengths and winter distributions were closer to those of C. clanga.

Timing and distance In some bird species, the number of nights (or days) that individuals show migratory restlessness correlates with the actual distance travelled by their population (Figure 22.2; Box 13.1). This led to the view that migration was controlled in part by endogenous time programmes, entrained by the seasonal change in daylength (Chapter 12). Again, the timing of migratory activity, whether early or late in the season, or long or short in duration, could be influenced by selective breeding in captivity. The cross-breeding experiments with Blackcaps, mentioned above, confirmed that migratory activity is a population-specific quantitatively inherited characteristic. Restlessness began earlier and continued longer in one parent population than in the other (Berthold & Querner, 1981), while the first-generation hybrids showed intermediate patterns of behaviour (Figure 22.2). In another experiment, Blackcaps from a migratory population (southern Germany) were selected for later onset of migratory activity (Pulido et al., 2001). After only two generations of artificial selection, the mean onset of migratory activity was delayed by more than 1 week. Experiments involving the cross-breeding of different species also proved instructive. In southern Germany, the Common Redstart (Phoenicurus phoenicurus) is a long-distance migrant, travelling up to 7000 km to tropical Africa, whereas the Black Redstart (Phoenicurus ochruros) is a short-distance migrant, travelling about 1000 km to Mediterranean winter quarters. The young of both species hatch at about the same time in May June, but the Common Redstart moults earlier and more rapidly in preparation for its longer journey, beginning in August. In captivity, this is reflected in the early appearance and long duration of nocturnal migratory restlessness. In contrast, the Black Redstart’s period of restlessness is later (October November) and briefer. The Common Redstart also becomes much heavier through fat deposition and retains its fat for much longer than the Black Redstart. The two species were therefore ideal for cross-breeding experiments to elucidate the genetic control of these aspects. In the event, hybrids between the two proved to be intermediate in all respects between their parent species, in the timing and duration of migratory restlessness, the timing of moult and the degree of fat deposition (Berthold, 1999). Yet again, the strong implication was that all these aspects were under genetic control. In addition to the Blackcap and two Redstarts, in at least two other obligate partial migrants, the occurrence of migratory and non-migratory individuals has been shown to be genetically determined, namely the central European populations of the European Robin (Biebach, 1983) and Eurasian Blackbird (Schwabl, 1983). Indications of genetic control have also been found in particular populations of the Song Sparrow (Melospiza melodia) (Nice, 1937, reanalysed by Berthold, 1984b), Silvereye (Zosterops lateralis) (Chan, 1994), Great-crested Grebe (Podiceps cristatus) (Adriaensen et al., 1993) and others. How quickly changes from migrancy to residency could occur in the wild would depend not only on the initial level of genetic variation in the behaviour of the population and on the strength of the selection pressure but also on generation times (or longevities) and on whether matings were selective or random among genotypes. If matings were assortative, with individuals of similar migration habits pairing together, the change to new migration habits in the population could occur more rapidly than if matings were random between genotypes. Measures of migratory restlessness, along with breeding experiments, showed that in Blackcaps, non-migrants, short-distance migrants and long-distance migrants were part of the same continuum of variation in a single trait, as reflected in restlessness. The binary response (migrate or not migrate) was caused by a threshold which divided individuals into those above and below. Thus all birds without measurable migration in the wild had activity levels in captivity at the low end of a continuous distribution, below the limit of expression or detection (Pulido et al., 1996). Similarly, the division between short-distance and long-distance migrants was caused by variation in the numbers of nights on which they showed appropriate behaviour. These findings had profound implications for the evolution of migration because they suggested that ecologically significant transitions between resident or migratory, and between short- and long-distance migration, could come about by selection on a single trait. Of course, other selections would be needed to change the migratory direction and fattening pattern, as discussed later.

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Most probably, then, migratory traits are threshold characters determined by multiple genetic loci. This mode of inheritance, based on quantitative genetics, supersedes the idea of a single locus determination of a genetic dimorphism (migrate or not), because the offspring of given pairs are normally intermediate in their behaviour (Berthold et al., 1990; Berthold 1996). Consistency tests on captive birds showed that individuals with a low level of restlessness did not change to a high level in subsequent years, although some individuals that initially showed a high level subsequently showed a lower level (equivalent to wild birds becoming less migratory in later life) (Berthold, 1993). In the Blackcap and Dark-eyed Junco (Junco hyemalis), migratory behaviour (5high restlessness) was also expressed in a greater proportion of females than males, raising the possibility of sex-linked inheritance (Berthold, 1986; Terrill & Berthold, 1989; Holberton, 1993). In this situation, any sex difference in migratory tendency would result partly from genetic influence but would not exclude additional influence from dominance relationships. These various findings support the view that inborn, temporal patterns of migratory activity serve as time programmes which, together with inherited migration directions, enable inexperienced, first-time migrants to ‘automatically’ cover the distance between their breeding areas and their specific wintering areas. They embody the so-called vector system of migration and help to explain why young birds, with no previous experience of a wintering area, can find their own way to an appropriate locality, without help from experienced adults (Chapter 10). Inherited time programmes thus equip the birds with knowledge of when to migrate and when to stop. This does not exclude the possibility that birds might also respond to the specific conditions in potential wintering areas to terminate their migration (ecological or magnetic conditions, for example Chapter 11).

Migratory directions The finding that captive migrants, during periods of migratory restlessness, flutter in their cages with an appropriate heading, suggested that migratory directions were also under genetic control. This could be easily tested on Blackcaps because in Europe this species shows a migratory divide, with those from the western part of the continent migrating southwest in autumn and those from the eastern part southeast. Moreover, the eastern populations migrate around the eastern edge of the Mediterranean to East Africa, so they must change their course (by about 60 degrees clockwise) from southeast to southsouthwest about halfway through their autumn journey. Western populations migrate southwest and winter mainly in the western Mediterranean region; they therefore have a shorter journey and do not obviously change direction on route. With birds from two localities lying west and east of the migratory divide, hand-raised and tested under identical conditions, this behavioural difference did indeed seem to have a genetic basis (Figure 22.3). In orientation cages, Blackcaps from western Germany kept a constant southwest course throughout the season, as expected from their relatively direct route to the Iberian Peninsula and northwest Africa, whereas those from eastern Austria started with a southeast course in September October, and changed within 10-days to a south-southwest course in November (Helbig et al., 1989). It seemed that young Blackcaps not only inherited from their parents a general starting direction, but a fairly detailed time direction programme appropriate to their dogleg migration route. Moreover, when Blackcaps from both sides of this divide were cross-bred, the first-generation hybrids showed a wider spread of directional preferences than either parent population, but on average directly southward, in an intermediate direction between the two parent groups (Helbig, 1991). These findings thus confirmed the genetic basis of migratory directions and, through crossOctober

November

N

N

E

W

S

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FIGURE 22.3 Orientation directions of Blackcaps (Sylvia atricapilla) from two populations breeding east and west of a migratory divide in Europe, and from hybrids between these two populations. Within the inner circle, triangles indicate the parental population from southwest Germany (filled) and eastern Austria (open), while in the outer circle, dots show first-generation offspring of mixed pairs bred in aviaries. Arrowheads indicate group mean directions. The hybrids took directions intermediate between the two parental forms. Note the seasonal shift in direction shown in November by the southeastward migrating parents and the intermediate orientation of the hybrid offspring. From Helbig (1991, 1996).

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breeding, revealed a phenotypically intermediate mode of inheritance. The implication is that, if birds from southwest and southeast migrating populations interbred where they meet, their offspring would inherit intermediate, and possibly inappropriate, directional preferences. Any selection against the hybrids could help to maintain the directional differences between populations, perhaps leading eventually to taxonomically distinguishable subspecies (Chapter 24). Evidence for an intra-seasonal change in direction, genetically determined and endogenously programmed, was also found in Garden Warblers (Sylvia borin) (Gwinner & Wiltschko, 1978) and Pied Flycatchers (Ficedula hypoleuca) (Beck & Wiltschko, 1988) in Europe, and in Yellow-faced Honeyeaters Laligavis in Australia (Munro & Wiltschko, 1993). In the wild, all these species showed a change in direction part way through their journey, and in captivity, a change in directional preferences. It is not sufficient that birds inherit a directional tendency that allows them to reach winter quarters. They must also be able to reverse this direction in spring to return to their breeding areas. Such reversal in direction has been demonstrated in tests of hand-raised Indigo Buntings (Passerina cyanea), Blackcaps and Garden Warblers (Chapter 11; Emlen, 1969; Helbig et al., 1989; Gwinner & Wiltschko, 1978, 1980). In autumn, Garden Warblers orientated southwest, changing some days later toward south or south-southeast, but in spring they headed towards the north, fitting with the loop migration recorded in wild Garden Warblers (Gwinner & Wiltschko, 1978, 1980). Less direct indications for genetic control of migratory directions in various other species stem from the facts that (1) inexperienced migrants tested in orientation cages showed regular species-specific and population-specific migratory directions; (2) displaced first-time migrants [White Storks (Ciconia ciconia), Schu¨z et al., 1971, Common Starlings (Sturnus vulgaris), Perdeck, 1958] showed migratory directions parallel to those of their parental populations (Chapter 10); (3) partial migrants also migrate regularly in specific directions; (4) many young birds [notably Common Cuckoos (Cuculus canorus) migrate from Eurasia and tropical Africa independently of their parents (Chapters 10 and 18)]; and (5) inexperienced warblers and flycatchers show population-specific seasonal changes in their directional preferences in captivity matching the changing course of migration in wild birds. All these findings indicate that such migrants possess pre-programmed migratory directions or directional sequences, although they may, of course, deviate from their genetically prescribed course in response to local topography, weather and other conditions (Chapter 4).

Morphological features The cross-breeding experiments with exclusively migratory Blackcaps from southern Germany (with long wings and high body weights) and poorly migratory conspecifics from the Canary Islands (with short wings and low body weights) demonstrated the genetic influence on both characteristics. Wing lengths, as well as body weights, were intermediately expressed in the hybrids (Berthold & Querner, 1982a). Similarly, in a later study, hybrids between migratory and nonmigratory Blackcap populations, from Moscow and Madeira, showed intermediate values between parental populations in wing length, wing shape and wing area, while in other variables they resembled either parent population (Fiedler, 2005).

Natural variability Another interesting finding confirmed in captive birds concerns the level of individual variation in migratory restlessness and directions apparent within some populations. Among Blackcaps that breed in the Mediterranean region, some individuals are resident, while others travel mainly short distances up to 1300 km. Correspondingly, migratory restlessness among captive individuals from this region varied by a factor of 100. In contrast, Blackcaps that breed in Germany are wholly migratory, travelling distances from about 700 4500 km to reach winter quarters which extend from southern France to the Ivory Coast (Berthold, 1996). The amount of migratory restlessness displayed by captive individuals from this region varies by a factor of about six (between about 150 and 900 hours) and occurs over generally longer periods than the Mediterranean birds. Individuals from resident populations of other species have also shown low levels of migratory restlessness in spring and autumn, including tropical Stonechats (Helm & Gwinner, 2005). The important point is that not all individuals in the same population are equal in their migratory behaviour and that substantial variation exists on which natural selection can act if necessary. The supposed influence of different levels of migratory activity on the behavior of the birds themselves is shown in the hypothetical ‘threshold’ model in Figure 22.5.

A natural change in the migration of Eurasian Blackcaps A new migration route of central European Blackcaps to winter quarters in Britain and Ireland (as opposed to the western Mediterranean region) was discovered from ring recoveries (Zink, 1962; Berthold, 1995). Prior to 1960, Blackcaps were

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rare during winter in Britain and Ireland, but from the late 1980s thousands of individuals wintered regularly. For nearly 40 years, ringing provided no indication that these birds were raised in Britain or Scandinavia. However, many Blackcaps ringed during the breeding season in Belgium, southern Germany and western Austria were recovered in a west-tonorthwest direction, some of them in Britain and Ireland. These are all areas where southwest migrants also breed. It therefore appeared that, within a period of 30 years, a portion of the southwest migrating population in central Europe had shifted their migration toward the west and northwest and that the majority of British-wintering Blackcaps originated from this region. To see whether this new migration had a genetic basis (as opposed to being due to increased wind drift or other prevailing conditions), some wintering Blackcaps were caught in southwest England, bred in captivity in Germany, and then tested for directional preferences in standard conditions. Both the adults and their offspring showed a west-northwest preference, indicating that the new migration route represented an evolutionary change that had apparently arisen within recent decades (Figure 22.4; Helbig, 1994, 1996). Such a change presumably started from one or more individuals with an unusual directional tendency that found themselves in a new area where they could survive the winter. These pioneers may have been individuals from the extreme end of a range of directional preferences already existing within the central European source population, or mutant individuals with a new directional preference not previously represented. But whatever the origin of the pioneers, it would not have been enough merely for them to have been blown off course, because the new route could not have been inherited by their offspring. It must have been genetically influenced. Once started, the selection pressures that may have favoured wintering of continental Blackcaps in Britain rather than in the Mediterranean region could have included (1) factors acting in the new wintering area, such as progressively milder winters, or improved food supply provided at garden feeders, and at winter fruit bushes planted in recent times; (2) factors related to the location of the new wintering areas, such as a shorter migration distance (by up to 1500 km) and possibly an earlier return to breeding areas; or (3) factors acting in the former Mediterranean wintering areas such as drought-induced declining food supplies and increasing competition. Other ringed Blackcaps from central Europe have been found in autumn further north than Britain but have not established wintering populations, possibly because at these higher latitudes the winters are too cold for them or garden bird feeders too scarce. Captive British wintering Blackcaps show migratory restlessness at a date that would enable them to arrive in their central European breeding areas by 1 April, whereas Mediterranean wintering birds would not arrive until about 17 April. In addition, the mean testis size at the date of arrival was about 25% greater in the first group than in the second. An early return could enable British-wintering Blackcaps to pair preferentially with one another (assortative mating based on differential arrival times), and perhaps raise an extra brood each year, speeding the evolution of the new habit. Field studies revealed that, on average, birds from British wintering areas did indeed arrive in central European breeding areas about 10 days earlier than those from Spanish wintering areas and were 2.5 times more likely to mate with one another than at random (Bearhop et al., 2005; Delmore et al., 2020). The British-wintering birds also settled in the better nesting territories and produced larger clutches and broods. In view of these findings, the British-wintering birds may eventually out-compete and replace the Spanish-wintering ones. It is also surprising that British-breeding Blackcaps have apparently not yet become partially resident, with some individuals remaining all year in their breeding areas. So far, only three recoveries of confirmed British-bred Blackcaps have been obtained in Britain in winter, but this may well mark the start of a new habit. Meanwhile, most British Blackcaps continue to winter in Iberia and North Africa. (A)

(B)

N

W

E

S

(C)

N

W

E

S

N

W

E

S

FIGURE 22.4 Autumn orientation of Blackcaps (Sylvia atricapilla) caught in winter in Britain (A), their captive-bred first-generation offspring (B), and a control group from southwest Germany (C). Each symbol shows the direction of the mean vector of one individual during 15 20 tests. The findings indicate that British wintering Blackcaps have different inherent directional preferences from Blackcaps that breed in the same area of central Europe but winter to the southwest in Iberia. Modified from Helbig (1996).

Evolution and inheritance of migratory behaviour Chapter | 22

471

In association with their earlier arrival dates, resulting in partial reproductive isolation, the northwest-migrating Blackcaps have already diverged genetically and phenotypically from southwest-migrating ones (Rolshausen et al., 2009). The former differ in molecular markers (microsatellites), and on average have more rounded wings (associated with their shorter migrations), more pointed beaks (associated with the change in diet from fruit to more seeds and fat) and browner colouration (attributed to colder, damper weather in Britain). These differences are small, but all are statistically significant. So in only half a century, the novel migratory route led to divergence in a variety of traits. This is of special interest because the two migratory groups breed in the same region, and little evidence has previously emerged for sympatric speciation in birds, the possible eventual consequence of continued genetic divergence. However, the divide may prove to be temporary, and in time one migratory genotype may gradually replace the other in their shared breeding range which now ranges from northern Spain through France and Germany across to Poland (Delmore et al., 2020).

Heritability and other studies Further evidence for the genetic control of migratory traits has come from studies of resemblance among genetically related individuals, such as siblings or parents and their offspring (heritability). Close resemblance in any trait between closely related individuals can be assumed to result partly from their shared genes (inheritance), partly from similarity in the environments to which they are exposed, and partly to varying interactions between genetic and environmental factors. In free-living birds in their natural habitats, environmental influences can sometimes be so great as to mask the effects of genetic variation. But in captive birds kept in uniform conditions, environmental variation can be kept to a minimum, enabling the contribution of genetic factors to be more clearly revealed. Of five estimates of the heritability of migratory timing or activity from studies of free-living birds, only one was statistically significant (Pulido & Berthold, 2003). This lack of significance may have been due partly to variation in the environmental conditions to which these individuals were exposed, to low sample sizes, to low precision of measurements taken in the field, or to greater age variation of some wild samples (assuming age effects on traits). In contrast, however, of eight estimates of heritability concerned with migratory timing in captive birds, and five concerned with the intensity of migratory activity, all indicated statistically significant heritability (Pulido & Berthold, 2003). Significant estimates of heritability obtained in different studies were as follows: for the date of onset of autumn migratory activity 0.34 0.67, for the date of cessation of autumn migratory activity 0.16 0.44, for the date of onset of spring migratory activity 0.67, for the date of arrival at the breeding site 0.54, and for the amount/intensity of autumn migratory activity 0.36 0.53 (Pulido & Berthold, 2003). So these estimates, taken under controlled conditions, provided further evidence for genetic influence over the traits examined. Other field studies provided a different type of evidence. American Cliff Swallows (Petrochelidon pyrrhonata) in central North America were exposed in 1996 to a severe cold snap in the middle of the spring arrival period, when insects became inactive, killing many of the newly arrived birds (Brown & Brown, 2000). Other swallows arrived after the event. Observations in later years showed that the cohort hatched after the selection event contained a greater proportion of later-arriving birds than earlier cohorts so the mean arrival date of the whole population was shifted later. Reaction to the cold snap thus seemed to have changed the genetic composition of the population, in favour of laterarriving genotypes. Although in some years early arrival gave better nest success, this advantage was apparently offset by the greater risk of mortality in occasional cold years, the resulting arrival dates being a compromise between these opposing selection pressures (Chapter 13). Likewise, bad weather in central Europe in the autumn of 1974 eliminated many late-departing migrants among hirundine populations, as millions of birds died (Chapter 31). The effects of this selective mortality were apparent for several subsequent years when departures finished earlier in autumn than in the years before this event. This change was most evident in Barn Swallows (Hirundo rustica) but also appeared in Common House Martins (Delichon urbica) and Sand Martins (Riparia riparia) (Gatter, 2000).

THE GENES INVOLVED For decades, research on the evolution of migration in birds was based on studies of live birds, and how their behaviour could be altered by selective breeding in captivity. It was clear from this work that multiple genes were involved in the control of migration, but only recently have attempts been made to identify the genes concerned. Candidate genes influencing particular aspects of migration have now been identified in a few species, such as orientation behaviour in Swainson’s Thrush (Catharus ustulatus) (a region on chromosome 4, Delmore & Liedvogel, 2016) and Willow Warbler (Phyllospcopus trochilus) (regions on chromosomes 1 and 5; Lundberg et al., 2017), and the timing and duration of

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migratory behaviour in several other species, such as Blackpoll Warbler (Setophaga striata) (allele length of Clock and Adcyap1 genes, Ralston et al., 2019). A major advance came with the use of high-throughput sequencing technologies to trace the evolutionary history of migration in the Blackcap. This study was based on the genomes of 110 individuals collected from across the breeding range, spanning the full spectrum of migratory behaviour known in this species (Delmore et al., 2020). It revealed that Blackcap populations began to diverge from one another about 30,000 years ago when they were confined to glacial refuges but that some apparent gene mixing between groups of migrating and resident Blackcaps occurred around 5000 years ago. The propensity to migrate, direction (orientation) and distance of migration all mapped to a small number of genomic regions common to all Blackcaps. But surprisingly, these regions did not overlap with those reported from other species of migratory songbirds, suggesting that there may be multiple ways to generate variation in migration. This was an important finding because it had long been hypothesized that there may be a shared genetic mechanism for migration, not only in birds but also in other animals (Liedvogel et al., 2011; Liedvogel & Lundberg, 2014; Liedvogel & Delmore, 2018). The differences between the different Blackcap populations tended to be in parts of the genome that affect whether a given gene is switched on or off. Through serving as a regulator of the migratory syndrome, such a system could further explain how existing migratory behaviour can change rapidly. The study of the entire genomes of migratory birds promises to bring fresh insight to our understanding of the evolution and control of bird migration. It is not impossible that migration even if basically controlled by a small number of genes can be influenced by a much wider range, and by different genes in different types of birds. These issues remain to be resolved.

CONCLUDING REMARKS Most of this experimental research was concerned with the modification and further development of migratory behaviour, and not with its inception. Most also involved only one species, although most findings were confirmed on others. They imply that, given sufficient underlying genetic variation and strong-enough selection pressure, some wild birds could change their migratory habits within only a few generations in response to environmental change (for more examples see Chapter 23). Moreover, the intermediate behaviour of hybrids implies control of each aspect by several genes, and not just one (for any behaviour controlled by a single gene would be expected to show an on off pattern, with no scope for intermediates). Artificial selection for higher and lower levels of migratory activity among captive Blackcaps resulted in changes in subsequent generations not only in the frequency of individuals showing migratory activity but also in the amount of migratory activity they showed (Pulido & Berthold, 2010). The correlation between these two traits was strong, suggesting that both were controlled by the same genes. Genetically, both incidence and amount were aspects of the one trait. This finding has implications for the evolution of migration: in particular, that obligate migrants and non-migrants could be present in all bird populations, although the frequency of one or other may be very low in populations classed as completely sedentary or completely migratory. On such a system, all bird populations could be considered as partially migratory, differing only in degree of migratory behavior (reflected in captive birds by degree of migratory restlessness). High correlations between migratory traits (date of onset, incidence, and duration of migratory activity) suggest that such traits are expressed as a syndrome: that is different traits do not occur in isolation, but as a suite of connected features. This means that, if selection changes one trait, others will change at the same time. If, for instance, the survival of sedentary individuals increases due to milder winters in the breeding areas, the frequency of non-migrants in the population will rise as a direct response to selection. But at the same time, migratory individuals in that population would be expected gradually to delay their autumn departure from the breeding area and to shorten their migration distance as correlated responses (Pulido & Berthold, 1998, 2003, 2010). This fits the fact that partial migrants often travel only short distances and, compared with obligate migrants, usually leave late and return early to their breeding areas. It also implies that the difference between facultative and obligate migration might be a question of degree, rather than type, involving genetic influence over a moveable threshold (Figure 22.5). Migratory syndromes may also include other features, such as morphology and physiology and could potentially affect traits that extend beyond migration. For example changes in the timing of migration might in turn influence the timing of reproduction in species in which these processes are adjacent in the annual cycle (Liedvogel et al., 2011). Migratory syndromes have so far received limited attention (but see Dingle, 2006), and their existence has been doubted, with little evidence for deeply rooted co-adapted trait complexes (Piersma et al., 2005). But much depends on the numbers and types of characteristics that are lumped together as a potential syndrome. On the basis mainly of the experimental results described above, Berthold (1999) proposed what he called a ‘comprehensive theory’ of migration control. The theory centres on the concept of obligate partial migration, in which individuals vary in their inherent migratory activity. This situation is clearly widespread (and possibly universal) in birds,

Frequency

Evolution and inheritance of migratory behaviour Chapter | 22

Obligate Facultative Obligate residents migrants migrants

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FIGURE 22.5 The threshold model of migration in a population of partial migrants. The bell-shaped curve reflects the hypothetical distribution of different levels of migratory activity in such a bird population. Birds with the lowest levels of activity are non-migratory, those with somewhat higher levels are facultative migrants that migrate only under adverse conditions, while those with even higher levels are obligate migrants that migrate under all conditions. The positions of the thresholds are not fully fixed and can be shifted to either side by environmental factors. Modified from Pulido (2011).

Migratory activity

enabling complete migrancy or complete residency to be achieved or lost, depending on selection. That occasional migrants exist in basically sedentary populations has long been evident, as exemplified in analyses of British ring recoveries (Wernham et al., 2002). No clear-cut difference separated resident and migratory species, but different species showed a continuum of variation in the proportion of individuals that had made long-directed moves. This could account for many familiar aspects of bird movements: for why occasional individuals of normally migratory species (eg Barn Swallow) can be seen in breeding areas in winter, long after other individuals of their species have left; and why, even in the most sedentary of species, occasional ringed individuals are recovered in autumn or winter at long distances, all in a restricted direction to lower latitudes. For example the Stock Dove (Columba oenas) is considered strictly resident in Britain, yet 1% of ring recoveries resulted from long-distance moves. What is clear is that, once obligate partial migration has evolved, the whole range of behaviour from strictly resident to strictly migratory can develop in short-lived birds in much less than a human lifetime. If the propensity for resident or migratory behaviour exists in a population, as research implies, as a gradient rather than as a dichotomy, selection to change from resident to migratory (or vice versa) could begin anywhere on the behavioural gradient. It does not necessarily depend on the prior presence of a few migratory individuals in an otherwise resident population (or vice versa). It also means that an ability to migrate can lie dormant in a population for generations, over a long sedentary period, until activated by changed conditions (Pulido, 2011). This theory of in-built flexibility contrasts with an earlier suggestion that migration might have evolved independently several times in birds by convergent evolution. If this were so, it could be controlled by different mechanisms (including different genes) in different types of birds. Because most of the relevant work so far has involved passerines, this theory of multiple control mechanisms cannot yet be considered invalidated. Moreover, all the known examples of variable or changing migratory behaviour, whether from wild or captive birds, refer to species that live in seasonal environments, where migration is the norm. Whether birds that have spent their entire evolutionary history in the relatively stable environment of lowland tropical rainforest could develop latitudinal migration so rapidly is much less certain and provides an obvious opening for further research. Examples of neotropical families or sub-families which contain no known migratory species include the Pipridae, Dendrocolaptinae, Formicariidae, Rhinocryptidae, Conophagidae and Thamnophilidae. Another gap in our understanding concerns the extent to which differences in migratory features (such as distance and direction) are reflected in the level of overall genetic differentiation between populations. The few existing studies suggest that differences in migratory behaviour between populations occupying contiguous breeding ranges generally do not correlate with strong overall genetic differentiation, as reflected in microsatellite or mitochondrial DNA (for Blackcap, see Helbig, 1994; Pe´rez-Tris et al., 2004; for Willow Warbler, see Bensch et al., 1999; for Prairie Warbler (Setophaga discolor), see Buerckle, 1999; for Great Bustard (Otis tarda), see Pitra et al., 2000). Rather, changes in their migratory behaviour seem to result from selection on relatively few loci (Helbig, 2003). This conclusion agrees with the view that few genes may be involved in the expression of migratory traits, even though they may be ‘switched on’ by other genes (Helbig, 1994, 1996), and that strong correlations exist between these traits (Pulido & Berthold, 2003). It also agrees with the finding that some evolutionary changes in migratory behaviour can happen rapidly (within a few generations), and that such adaptations are population-specific rather than species-specific. This discussion leads to the question of how many different aspects of migratory behaviour (or traits) there might be on which selection could act (see also Chapter 1). We have one apparent gradient in behaviour, as reflected perhaps in Zugunruhe, which determines the timing and distance of migration (from residents to short-distance and long-distance

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migrants). Associated with this is another gradient in patterns and levels of fuel deposition in preparation for different types of journeys. We have a third apparent gradient between mainly endogenous control (regular long-distance migrants) to mainly external control (facultative irruptive migrants). We have a fourth apparent gradient in breadth of directional preference (from no preference to strong and narrow preference towards a particular direction). Fifth, we have an apparent binary response on whether the movement is one-way or return (but even this might be regarded as a graded response from no return, through partial return to full return, Chapter 13). These are all behavioural gradients on which selection could act. The discovery of correlations between different aspects of migration may tempt us to reduce these different aspects of variation to as small a number as possible. But given the enormous diversity of movement patterns found among birds, pooling aspects of behaviour in this way (from correlations in a small number of similar species) brings the risk of masking other kinds of variation. Each additional aspect of modification allows an extra ‘degree of freedom’, and hence finer adjustment of behaviour to environments and species needs. There is also the role of ‘epigenetic effects’ changes in gene expression that can occur through environmental influence without modification in the controlling DNA. Such effects could, for example explain some aspects of facultative migration and differences in behaviour between young and old from the same population. Acknowledgement of all aspects of variation may be necessary to account for the wide range of movement patterns found among bird populations.

SUMMARY Migration is a product of natural selection, leading species in seasonal environments to adopt movement patterns that enable individuals to survive and breed most effectively. Autumn migration gives improved winter survival through providing access to greater food availability in winter quarters. Spring migration gives improved breeding success, through greater seasonal food availability and longer days in summer quarters. The roles (if any) of predation, parasitism and competition in the evolution of migration are less obvious. Migratory birds seem to possess no major adaptations that resident birds lack; they differ only in the degree of development and modification of particular traits, whether concerned with orientation, physiology or morphology. Some bird populations are obligate migrants and others are obligate residents. Yet others are partial migrants in which some individuals stay year-round in their breeding areas while others migrate elsewhere. Partial migration can apparently arise in two ways, either with a mixture of obligate migrants and obligate residents in the same population or with the entire (or part of the) population consisting of facultative migrants in which migration is optional, with individuals varying their behaviour according to conditions at the time. Breeding experiments on captive birds have shown that various aspects of migratory behaviour, such as the intensity, timing and duration of migratory activity, along with directional preferences, are under genetic control and can be altered by selection to give substantial changes within a few generations. Such changes may be facilitated by genetic correlations between some traits so that selection for one trait can alter others at the same time. In particular, the occurrence of migratory behaviour is probably controlled by the same genes that control migration distance, operating via the amount of migratory activity. Directions are evidently controlled independently, and individual variation in directions is less in long-distance than in short-distance migrants. Overall, migratory behaviour seems to be controlled by multiple genes with small effects. Since 1960, a natural change has occurred in the migratory behaviour of Blackcaps. Some central European birds changed their direction of migration and now travel west-northwest to winter in southern Britain (the local British breeding birds continuing to migrate southwest to Iberia). Breeding experiments have confirmed that this new migratory behaviour is inherited. Further evidence for the genetic control of migration has come from studies of the resemblance in behaviour between genetically related individuals (heritability), both in captive and wild birds. Most migratory traits that have been examined show moderate to high heritability. In a few species, genes concerned with certain aspects of migration have been identified, opening an important field for further study.

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Lundberg, P. (1987). Partial bird migration and evolutionary stable strategies. J. Theor. Biol. 125: 351 60. Lundberg, P. (1988). The evolution of partial migration in birds. TREE 3: 172 5. Maggini, I. & Bairlein, F. (2010). Endogenous rhythms of seasonal migratory body mass change and nocturnal restlessness in different populations of Northern Wheatear Oenanthe oenanthe. J. Biol. Rhythms 25: 268 76. Maggini, I., Bulte, M. & Bairlein F. (2017). Endogenous control of fuelling in a migratory songbird. Sci. Nat. 104: 93. Marchette, K., Price, T. & Richman, A. (1995). Correlates of wing morphology with foraging behaviour and migration distance in the genus Phylloscopus. J. Avian Biol. 26: 177 81. Matthews, G. V. T. (1968). Bird Navigation (2nd ed.). Cambridge, Cambridge University Press. McKinnon, L., Smith, P. A., Nol, E., Martin, J. L. Doyle, F. I. et al. (2010). Lower predation risk for migratory birds at high latitudes. Science 327: 326 7. Mead, C. J. (1983). Bird migration. Feltham, Middlesex, Country Life Books. Milne, H. & Robertson, F. W. (1965). Polymorphism in egg albumen protein and behaviour in the Eider Duck. Nature 205: 367 9. Mo¨nkko¨nen, M. (1995). Do migratory birds have more pointed wings? A comparative study. Evol. Ecol. 9: 520 8. Munro, U. & Wiltschko, W. (1993). Magnetic compass orientation in the Yellow-faced Honeyeater, Lichenostomus chrysops, a day migrating bird from Australia. Behav. Ecol. Sociobiol. 32: 141 5. Nice, M. M. (1937). Studies in the life history of the Song Sparrow. Trans. Linn. Soc. New York (4), 1 247. Perdeck, A. C. (1958). Two types of orientation in migrating Starlings, Sturnus vulgaris L., and Chaffinches, Fringilla coelebs L., as revealed by displacement experiments. Ardea 46: 1 37. Pe´rez-Tris, J., Bensch, S., Carbonell, R., Helbig, A. J. & Tellerı´a, J. L. (2004). Historical diversification of migration patterns in a passerine bird. Evolution 58: 1814 32. Piersma, T. (1997). Do global patterns of habitat use and migration strategies co-evolve with relative investments in immunocompetence due to spatial variation in parasite pressure? Oikos 80: 623 31. Piersma, T., Pe´rez-Tris, J., Mouritsen, H., Bauchinger, U. & Bairlein, F. (2005). Is there a ‘migratory syndrome’ common to all migrant birds? Ann. N. Y. Acad. Sci. 1046: 282 93. Pitra, C., Lieckfeldt, D. & Alonso, J. C. (2000). Population subdivision in Europe’s Great Bustard inferred from mitochondrial and nuclear DNA sequence variation. Mol. Ecol. 9: 1165 70. Pulido, F. (2007). The genetics and evolution of avian migration. BioScience 57: 165 74. Pulido, F. (2011). Evolutionary genetics of partial migration the threshold model of migration revisited. Oikos 120: 1776 83. Pulido, F. & Berthold, P. (2003). Quantitative genetic analyses of migratory behaviour. Pp. 53 77 in Avian migration (eds P. Berthold, E. Gwinner, & E. Sonnenschein). Berlin, Springer-Verlag. Pulido, F. & Berthold, P. (2010). Current selection for lower migratory activity will drive the evolution of residency in a migratory bird population. Proc. Natl. Acad. Sci. U.S.A. 197: 7341 6. Pulido, F. & Berthold, P. (1998). The microevolution of migratory behavior in the Blackcap: effects of genetic covariances on evolutionary trajectories. Proc First Meeting Eur. Ornithol. Union. Biol. Cons. Fauna 102: 206 11.

Evolution and inheritance of migratory behaviour Chapter | 22

Pulido, F., Berthold, P., Mohr, G. & Querner, U. (2001). Heritability of the timing of autumn migration in a natural bird population. Proc. R. Soc. Lond. B 268: 953 9. Pulido, F., Berthold, P. & van Noordwijk, A. J. (1996). Frequency of migrants and migratory activity are genetically correlated in a bird population: evolutionary implications. Proc. Natl. Acad. Sci. USA 93: 14642 47. Ralston, J., Lorenc, L., Montes, M., Deluca, W. V. Kirchman, J. J. et al. (2019). Length polymorphisms at two candidate genes explain variation of migratory behaviors in Blackpoll Warblers (Setophaga striata). Ecol. Evol 9: 8840 55. Rayner, J. M. V. (1990). The mechanics of flight and bird migration performance. Pp. 283 99 in Bird migration. Physiology and ecophysiology in Bird migration. Physiology and ecophysiology (ed. E. Gwinner). Berlin, Springer-Verlag. Rolshausen, G., Segelbacher, G., Hobson, K. A. & Schaefer, H. M. (2009). Contemporary evolution of reproductive isolation and phenotypic divergence in sympatry along a migratory divide. Curr. Biol. 19: 2097 101. Schu¨z, E., Berthold, P., Gwinner, E. & Oelke, H. (1971). Grundriss der Vogelzugskunde. Berlin, Paul Parey. Schwabl, H. (1983). Auspra¨gung und Bedeutung des Teilzugverhaltens einer sudwestdeutschen Population der Amsel Turdus merula. J. Ornithol. 124: 101 15. Schwabl, H. & Silverin, B. (1990). Control of partial migration and autumnal behaviour. Pp. 144 55 in Bird migration: physiology and ecophysiology in Bird migration: physiology and ecophysiology (ed. E. Gwinner). Berlin, Springer-Verlag. Skrip, M. M., Bauchinger, U., Goymann, W., Fusani, L. Cardinale, M. et al. (2015). Migrating songbirds on stopover prepare for, and recover from, oxidative challenges posed by long-distance flight. Ecol. Evol. 5: 3198 209.

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Chapter 23

Recent changes in bird migrations

Pied Flycatcher (Ficedula hypoleuca), a species affected adversely in some regions by climate warming The far-reaching works of man in altering the natural conditions of the earth’s surface can so change the environment necessary for the well-being of the birds as to bring about changes in their yearly travels. Lincoln (1935)

We saw in the previous chapter how the migratory habits of birds can be rapidly altered under the influence of selection, continually shaped and re-shaped in response to changing conditions. Change in the migratory behaviour of wild birds has attracted attention in recent years, largely through growing interest in the effects of climate change. With a generally warming climate, one might expect birds to have responded accordingly, with migratory species wintering at higher latitudes than previously, or arriving earlier and departing later from their breeding areas. A further question is whether any observed changes result merely from pre-existing flexibility in behaviour, or from genetic changes produced by natural selection. Many of the changes observed in bird migration need entail no genetic change because, in every aspect, there is flexibility through which individuals can adjust their behaviour to some extent according to prevailing conditions (facultative responses). For example, the same birds might arrive on their breeding areas earlier in warm springs than in cold ones, or they might migrate further in cold winters than in mild ones. Hence, as climate changes from year to year, or over longer periods, birds have considerable scope for adjusting their behaviour to match these changes without the need for any genetic change in the controlling mechanisms. However, under consistent directional selection, genetic changes are not hard to imagine. Consider a partially migratory species in which some individuals have a genetic propensity to migrate and others do not. During a series of severe winters, the migrants survive better than the residents. As a result, the offspring of the migratory genotypes would comprise an ever greater proportion of each succeeding generation, gradually changing the genetic composition and migratory habits of the population. Conversely, during a series of mild winters, the resident genotypes, able to commandeer the best territories and start nesting early, could come rapidly to outbreed and outnumber the migrants. Perhaps the most likely scenario is that, under consistent selection pressure, facultative changes eventually give way to genetic ones. It is also possible that in some areas, climate changes have been too rapid for evolutionary change, so that bird populations are unable to persist under the altered conditions. Only through special study on a case-by-case basis can we tell to what extent any observed changes in migratory behaviour have resulted from changes in the gene pool of the population. For the most part, we can only measure the extent of changes, their correlation with environmental changes and any associated trends in population levels. The following sections illustrate the different types of change observed in bird populations over recent decades, with examples in Table 23.1.

The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00029-4 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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TABLE 23.1 Examples of recorded changes in migration patterns. Excludes changes in timing of migration described in the text. A. Shortening of autumn migration to winter nearer breeding areas Cape Gannet (Morus capensis)

Early ring recoveries of South African ringed birds from West Africa, but no recent recoveries, perhaps because of fisheries discards in the Benguela upwelling region now allow them to stay south, nearer their breeding areas

Oatley (1988)

Various waterfowl

Number of species wintering in Lithuania increased from 17 in the 1940s to 42 in the 1990s, and total numbers increased from several thousands in the 1930s to 150,000 in the 1990s. This was due largely to reduction in migration distance (shown by ringing), with smaller proportions reaching western Europe. It was especially obvious in Mallard (Anas platyrhynchos) and Mute Swan (Cygnus olor)

ˇ zas et al. (2001) Svaˇ

Bewick’s Swan (Cygnus columbianus bewickii)

Over a 50-year period, migration shortened and the wintering area in Europe shifted eastward at about 13 km/year, shortening individual migration distances by 353 km. Over 40 years, the time spent in wintering areas shortened by about 38 days.

Nuijten et al. (2020)

Greylag Goose (Anser anser)

Wintering grounds changed from Spain to the Netherlands, a previous region of stopover.

Nilsson (2006).

Greater White-fronted Goose (Anser albifrons)

Gradual shortening of migration of north European and west Siberian birds to give greater proportions wintering in continental Europe and smaller proportions in Britain

Stroud et al., in Wernham et al. (2002)

Snow Goose (Anser caerulescens)

Historically wintered primarily in Louisiana, Texas and Mexico. Many now winter further north in rice-growing areas of Iowa, Nebraska, Missouri and Arkansas

Cooke et al. (1995)

Canada Goose (Branta canadensis)

Formerly wintered mainly in the southern tier of States, now winters mainly in the middle tier of States

Hestbeck et al. (1991)

Red-crested Pochard (Netta rufina)

Increasing proportion of population wintering in central, as opposed to the southwest, Europe

Keller (2000)

Sharp-shinned Hawk (Accipiter striatus)

Now remaining in northeastern breeding areas in North America, and declining at migration sites further south, associated with increased gardenbird feeding and more northern wintering of prey species

Viverette et al. (1996)

American Kestrel (Falco sparverius)

General shortening of migration routes in western North America between 1960 and 2009; increase in birds wintering in northern States and decrease in southern States

Heath et al. (2012)

Various raptors

During 1977 2008, several raptor species in Europe shortened their migrations and no longer cross the Gibraltar Strait

Onrubia & Telleria (2012)

Great White Egret (Egretta alba)

Increasing proportion wintering in mid-latitudes of western Europe

Marion et al. (2000),

Black-crowned Night Heron (Nycticorax nycticorax)

Increasing proportion wintering in southern Europe and North Africa as opposed to sub-Saharan Africa

Pineau (2000)

Squacco Heron (Ardeola ralloides)

Increasing proportion wintering in southern Europe and North Africa, as opposed to sub-Saharan Africa

Hafner (2000)

Common Crane (Grus grus)

West European population formerly wintered in Spain Morocco, now winters mainly in France Spain and eastern Germany. Following construction of the dam at Lac du Der (Champagne, northern France) cranes started to use this site as a major stopover, and also as a wintering area, thus shortening their migration by about 1500 km each way

Alonso et al. (1994), and others

White Stork (Ciconia ciconia)

Formerly wintered entirely in Africa, thousands are now wintering regularly in the Mediterranean region, notably Spain, Bulgaria and Israel, with shortstopping confirmed by ring recoveries.

Berthold (1996), Fiedler (2003) (Continued )

Recent changes in bird migrations Chapter | 23

481

TABLE 23.1 (Continued) A. Shortening of autumn migration to winter nearer breeding areas Lesser Black-backed Gull (Larus fuscus)

Winters further north in Europe. Was a summer visitor to northern Europe but over last 40 years changed, so that large numbers now stay over winter

Hickling (1984)

Common Chiffchaff (Phylloscopus collybita)

Increasing proportion winter in Britain

Lack (1986)

Great Reed Warbler (Acrocephalus arundinaceus)

Formerly wintered entirely in Africa, south of the Sahara. Some now wintering in Spain

de la Puente et al. (1997)

Bluethroat (Luscinia svecica)

Increasing proportion wintering in Spain as opposed to sub-Saharan Africa

Bermejo & de la Puente (2004)

Yellowhammer (Emberiza citronella)

Increasing proportion winter in Finland

Va¨isa¨nen & Hilde´n (1993)

Eurasian Bullfinch (Pyrrhula pyrrhula)

Increasing proportion winter in Finland

Va¨isa¨nen & Hilde´n (1993)

European Greenfinch (Carduelis chloris)

Increasing proportion winter in Finland and Sweden

Va¨isa¨nen & Hilde´n (1993)

Hooded Crow (Corvus corone cornix)

Much reduced numbers wintering in eastern England now than in the 19th century, attributed to greater proportion of European birds wintering further north and east, confirmed by ringing

O’Donoghue, in Wernham et al. (2002)

B. Shortening of spring migration to breed nearer wintering areas Barnacle Geese (Branta leucopsis)

Breeding population established on Gotland and other sites around the Baltic and in the Netherlands, thus shortening migration to Novya Zemlya by 1300 km, or more. Birds from a different population have also started to breed in Iceland, thus shortening migration to Greenland by more than 500 km

Larsson et al. (1988), Forslund & Larsson (1991)

C. Change in direction to establish a new wintering area Greater White-fronted Goose (A. albifrons)

Change in wintering sites from central Europe to the Netherlands and western Germany associated with a directional change of 15 degrees to give a new route along the Baltic coast

ˇ zas et al. (2001) Svaˇ

Black Stork (Ciconia nigra)

Recolonized west Europe in 1970s 1980s probably from eastern populations. These birds started migrating southwest through Gibraltar, whereas eastern European populations migrate southeast through the Bosphorus

G. Neve, in Sutherland (1998)

White Stork (C. Ciconia)

The descendants of birds that started breeding in South Africa in 1933 have been satellite-tracked northward for about 3000 km in the non-breeding season

Underhill (2001)

Little Egret (Egretta garzetta)

Southern European birds migrate south, often across the Sahara. Many now move northwest to winter in northern France and southern Britain. Most of these birds are now resident in these areas

Marion et al. (2000)

Eurasian Blackcap (Sylvia atricapilla)

Some central European birds switched from migrating southwest to winter in western Mediterranean area to migrating north or northwest to winter in Britain

Helbig (1994)

D. Change from migratory to resident population Great Crested Grebe (Podiceps cristatus)

Increasing proportion in the Netherlands has become resident

Adriaensen et al. (1993)

Mute Swan (Cygnus olor)

From the first record in 1955, up to 2000 birds now winter near their breeding areas in Lithuania

ˇ zas et al. (2001) Svaˇ

Canada Goose (Branta canadensis)

Birds from migratory North American populations introduced to Britain have become resident, apart from newly developed moult migration.

Wernham et al. (2002) (Continued )

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The Migration Ecology of Birds

TABLE 23.1 (Continued) A. Shortening of autumn migration to winter nearer breeding areas Various waterfowl

Northern European populations have become more sedentary in association with reduced winter ice cover

Meller et al. (2016)

Red Kite (Milvus milvus)

Increasing proportion in Scandinavia has become resident

Kjelle´n (1992)

Eurasian Blackbird (Turdus merula)

Formerly wholly or mainly migratory in mid-latitudes of western Europe, now mainly resident

Berthold (1993, 1999), Main (2000)

Common Chiffchaff (P. collybita)

First recorded in 1846, the numbers wintering in Britain have increased greatly since 1940. They include some local birds and some migrants from Europe which may indicate a change in direction

Green, in Wernham et al. (2002)

Great Tit (Parus major)

Once-migratory population in the Finnish city of Oula near the Arctic Circle is now resident, following food provision by householders

Orell & Ojanen (1979)

Blackbird (Turdus merula)

The proportion of residents in the Netherlands breeding population increased from about 70% to 90% over the period 1955 1990.

van Vliet et al., 2009

Common Starling (Sturnus vulgaris)

Central European populations have become partially resident, with increasing numbers staying in towns in winter

Merkel & Merkel (1983), Berthold (1993)

E. Change from resident to migratory population Cattle Egret (Bubulcus ibis)

Migration system has arisen in North America, and within Australia and between Australia and New Zealand (2000 km)

Telfair (2020), Maddock & Geering (1994)

Common Starling (S. vulgaris)

Birds introduced into North America from British resident population have become migratory over much of continent

Kessel (1953), Dolbeer (1982)

House Finch (Carpodacus mexicanus)

Resident population introduced to eastern North America became migratory in less than 30 years, with different migration directions (southsouthwest) from west to east across the breeding range. Females migrate, on average, further than males.

Able & Belthoff (1998)

European Serin (Serinus serinus)

As spread north in Europe, switched from being resident to migratory

Berthold (1999)

F. Establishment of breeding population in former wintering range Leach’s Storm Petrel (Hydrobates leucorhous)

Now breeds on islands off South Africa

Harrison et al. (1997)

Manx Shearwater (Puffinus puffinus)

Now breeds on the west side of Atlantic, in a former migration area

Storey & Lien (1985)

White Stork (C. ciconia)

Started breeding in South Africa about 1933. Now regular. Winters in the tropics of Zaire and Rwanda

Harrison et al. (1997)

European Bee-eater (Merops apiaster)

Thousands now breed in South Africa

Harrison et al. (1997)

Barn Swallow (Hirundo rustica)

From around 1980, it began to breed within the traditional wintering range in southern South America. Now winters in northern South America.

Winkler et al. (2017)

Cliff Swallow (Petrochelidon pyrrhonota)

From 2015, it began to breed within the traditional wintering range in Argentina. Now winters in northern South America.

Areta et al. (2021)

G. Lengthening of autumn migration Great White Pelican (Pelecanus onocrotalus)

Shifted wintering sites following development in the Nile Delta in Egypt to further south

Crivelli et al. (1991)

Red-breasted Goose (Branta ruficollis)

Shifted wintering grounds from Azerbaijan to Romania and Bulgaria following habitat changes

Vangelewe & Stassin (1991)

Common Chaffinch (Fringilla coelebs)

Vast predominance of females in flocks in southern England in the late 18th century changed to more equal ratio in the late 20th century

Wernham et al. (2002)

.

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MIGRATORY TO SEDENTARY Over a wide range of latitudes, many bird populations have become more sedentary over recent decades (Bo¨hning-Gaese & Lemoine, 2004). Prior to 1940, the Lesser Black-backed Gull (Larus fuscus) was almost entirely migratory in Britain, only a few individuals remaining year-round. But nowadays, large numbers of all age groups stay for the winter, feeding mainly on refuse dumps which have increased the winter food supply (Hickling, 1984). Similarly, in the Eurasian Blackbird (Turdus merula), British and mid-European populations became progressively more sedentary during the last century, as winters mellowed (Berthold, 1993; Main, 2000; van Vliet et al., 2009). In both Europe and North America, many seed-eaters are now wintering further north within their breeding range, in association with the provision of suitable food at garden feeders (Table 23.1). Among many other short-distance and medium-distance migrants, increasing numbers of individuals now winter in areas where they once were wholly migratory, these species developing into typical partial migrants. The effect has been to expand the winter avifauna of many high-latitude regions. Among Great Bustards (Otis tarda) in central Spain, some males remained in their breeding areas, while others migrated immediately after mating to cooler areas. Out of 180 radio-tagged males, 35% remained resident, while 65% migrated an average of 90 km (Palacı´n et al., 2016). Mortality was about three times greater among migrants than among sedentary birds, largely due to collision with power lines. Accordingly, the proportion of residents in the population increased from 17% in 1997 to 45% in 2012, and as climate and habitat did not change in the study area over this period, the change to greater residency was regarded as a response entirely to human-induced mortality. Whether it resulted from natural selection or social influence, as suggested by the authors, its effect was to favour sedentary over migratory individuals.

SEDENTARY TO MIGRATORY Examples of change from sedentary to migratory behaviour are less common, and generally accompany an extension of breeding range into higher latitudes. For example, the European Serin (Serinus serinus) was once restricted to the south of Europe where it was resident, but in the early 20th century it spread north, where it became migratory. In more recent years, with milder winters, this migratory population has become partially resident (Berthold, 1999). Likewise, since the 19th century, many bird species have spread north in Fennoscandia, including the Northern Lapwing (Vanellus vanellus), Common Starling (Sturnus vulgaris), Eurasian Blackbird and Dunnock (Prunella modularis). In their newly colonized breeding areas, they are essentially migratory, whereas further south, they are partial migrants or residents (Schu¨z et al., 1971). Common Starlings introduced to North America at the end of the 19th century, supposedly came from resident British stock. They were initially sedentary in the eastern United States, but in connection with range expansion, migrants appeared in different proportions in different regions (Kessel, 1953; Dolbeer, 1982). Similarly, as Cattle Egrets (Bubulcus ibis) spread northward through North America, they remained resident in Florida and other southern parts, but became migratory further north (Maddock & Geering, 1994). During the 19th century, Snowy Egrets (Egretta thula) were eliminated by human persecution from the northern parts of their breeding range in North America, where they were migratory. They survived only in the southern parts where they were resident. But as the remnant resident population has recovered in recent decades, birds have spread northwards, where they have again become migratory in the newly colonized areas (Rappole, 2013). Several other North American species spread northward in the late 19th and early 20th centuries, benefiting from new habitat created incidentally by human activity, and became increasingly migratory in the newly colonized areas (Rappole, 2013).

SHORTENING OF MIGRATIONS So-called ‘short-stopping’ has occurred in many species as food has become more readily available at higher latitudes in winter, either through human activities or climate change. Several populations of Canada Geese (Branta canadensis) in North America responded in this way to agricultural changes or to the creation of refuges where food was provided (e.g., Terborgh, 1989; Hestbeck et al., 1991), as did Greylag Geese (Anser anser) and Common Cranes (Grus grus) in Europe (Alonso et al., 1994; Nilsson, 2006). Other species of waterfowl have also shortened their migrations, apparently in response to warmer winters, as open water has remained available nearer the breeding areas. This is shown by increased numbers wintering in northern and eastern parts of Europe, and declining numbers of the same species wintering in the south and west. Yet other waterfowl have shortened their migrations in apparent response to reduced disturbance and predation, as sanctuaries have been established in areas previously open to hunting (Chapters 14 and 30).

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The Migration Ecology of Birds

Many partially migratory raptors have also shortened their migrations, as judged by the reduced numbers now crossing Gibraltar Strait compared with the more northern Falsterbo (Onrubia & Telleria, 2012). This has occurred despite an overall increase in numbers. Shortened migrations in many other species have been reflected in the changing distributions of ring recoveries. Among 30 species of short-distance or partial migrants ringed in the breeding season in Germany, a tendency towards wintering at higher latitudes than previously was found in 10 species, and at lower latitudes in three species, but again ring recoveries were affected by changes in land use and hunting, as well as in climate (Fiedler et al., 2004). Similarly, between 1932 and 2004, winter recovery distances also decreased among birds ringed during the breeding season in the Netherlands (Visser et al., 2009). Of 24 species examined, 12 showed a significant decline in distances moved. Species from dry open habitats shortened their distance the most, species from wet open habitats the least and woodland species were intermediate. More and more European migrants that formerly wintered entirely in sub-Saharan Africa are now wintering in increasing numbers in the Mediterranean region. Examples include the Yellow Wagtail (Motacilla flava), Common House Martin (Delichon urbica), Osprey (Pandion haliaetus), Lesser Kestrel (Falco naumanni) and White Stork (Ciconia ciconia) (Table 21.1; Berthold, 2001; Onrubia & Telleria, 2012). From the 1990s, increasing numbers of White Storks were found wintering in Spain, with counts of less than 8000 in 1995, increasing to around 55,000 in 2020 (A. Onrubia, in litt.). These birds were almost all adults from Spanish and central European breeding populations, while juveniles from the Spanish population continued to migrate into sub-Saharan Africa (Flack et al., 2016). The suitability of southern Europe as a new wintering area is mainly due to the increased food supply provided by landfill sites. European winterers gain from this new food supply, and also from the reduced risk of a shorter migration and the potential to return earlier to breeding areas than African winterers (Chapter 15). Not surprisingly, those storks that winter in southern Europe now survive substantially better than those that winter in sub-Saharan Africa (Rotics et al., 2017; Be´cares et al., 2019). White Storks do not breed until they are 2 or more years old, and in the past, young birds stayed in Africa through their second summer or migrated only part-way towards their breeding areas (Chapter 15). But in recent years, instead of staying in Africa, increasing numbers have returned to southern Europe to pass their second summer, although without nesting. The mean distance of ring recoveries of second-summer birds from their natal sites in north Germany was 2517 km in 1923 1975, reducing to 720 km in 1978 1996 (Fiedler, 2001). Some Whooper Swans (Cygnus cygnus) and Barnacle Geese (Branta leucopsis) have shortened their migrations in another way, by establishing nesting populations hundreds of kilometres south of their historic breeding range, nearer to wintering areas (Table 21.1). This type of change is more difficult to explain, but may in some cases be due to suitable habitat being created by human activities, or to expansion into former range from which the species were eliminated in the past, or simply to unprecedented population increase leading to an expansion of breeding range into lower latitudes. Such changes involved not only young individuals breeding for the first time but also some older individual birds making a lifetime change in their breeding area.

LENGTHENING OF MIGRATIONS In species that have expanded their breeding areas to higher latitudes but have retained the same wintering areas, some extension of migration routes is inevitable. Eurasian examples include: (1) Black-winged Stilt (Himantopus Himantopus) which is expanding its breeding range northward (France, Ukraine, Russia), but still winters south of 40 N latitude; (2) European Bee-eater (Merops apiaster) which has expanded northwards in almost all central European countries, yet still winters entirely in Africa south of the Sahara; (3) Citrine Wagtail (Motacilla citreola) which is expanding its breeding range from Asia westward into Europe, but still winters in India and Southeast Asia (Fiedler, 2003). Some of these range expansions involve migrations lengthened by up to 1000 km. These types of change must have occurred in many species after each glaciation, when ice receded and plants and animals spread from lower to higher latitudes (Chapter 24). In some other species, greater proportions of ring recoveries are now being obtained from the distant parts of migration routes than formerly, but it is hard to tell whether this is due to altered migration behaviour or to changed recovery chances along the routes (Fiedler et al., 2004). Over recent decades, hunting has declined much more in the northern and mid-latitudes of Europe than further south. This could affect the migratory behaviour of hunted species, or merely the distribution of reported ring recoveries. Wintering Honey Buzzards Pernis apivorus have increased in southern Africa over recent decades, apparently in association with loss of habitat further north in East Africa, implying a lengthening of migration (Howes et al., 2019).

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CHANGES IN MIGRATORY DIRECTIONS In addition to the Eurasian Blackcap (Sylvia atricapilla) described in the previous chapter, changes in the direction of migration, leading to the adoption of new wintering areas, have been recorded in several species (Table 23.1). For example, Little Egrets (Egretta garzetta) breeding in southern France migrated southward, some crossing the Sahara to winter in the Afrotropics. But from the 1970s, increasing numbers began to migrate northwest to winter in northern France, southern Britain and Ireland (Marion et al., 2000). Some later became residents in these areas, and from the 1990s started to breed there. Similarly, Lesser Black-backed Gulls from Europe began increasingly from the 1980s to winter on the coasts of eastern North America, a change which requires a much stronger westerly component in migratory directions. Other possible examples of directional changes, beginning with vagrancy, are mentioned in Chapter 24. A different type of directional change is shown by some Northern Hemisphere species which now breed in the southern hemisphere and have reversed the direction of their autumn and spring journeys, from south to north and north to south. Examples include several species introduced from Europe to New Zealand in the 19th century. Similarly, White Storks are thought to have naturally started to nest in their South African wintering area around 1933, but they now migrate north to spend their non-breeding period in Zaire and Rwanda (Harrison et al., 1997), while the Barn Swallow (Hirundo rustica) and American Cliff Swallow (Petrochelidon pyrrhonota) have established themselves in former wintering areas in Argentina and now migrate to winter in more northern parts of South America (Winkler et al., 2017; Areta et al., 2021). This phenomenon may have been going on for thousands of years, considering the numbers of bird species that have conspecifics, or closely allied forms, breeding in equivalent habitats in the opposite hemisphere (Snow, 1978; Newton, 2003).

CHANGES IN MIGRATION TIMING Studies of long-term trends in the arrival times of birds in their breeding areas are mostly based on dates of first sightings, as it is these dates that are most frequently recorded. In some European localities, such records go back over periods exceeding 300 years (Lehikoinen et al., 2004). The problem with first arrival dates is that many refer to only single individuals, which by definition are not typical of their populations. Also, in species that undergo marked changes in numbers over the study period, first dates tend to be earlier in years of greatest abundance, possibly because of the statistical effect on the chance of observation (Loxton & Sparks, 1999; Sparks, 1999). The median or mean arrival dates of populations in their breeding areas are more representative but have been recorded much less often, and chiefly in recent decades. They depend on detailed studies in particular areas, where the arrival date of each individual (or occupant of each territory) was recorded. Other migration dates come from bird observatories where watching or trapping was maintained throughout the migration seasons each year, enabling median or mean passage dates (and standard deviations) to be calculated (Newton et al., 2010; Van Buskirk, 2012; Miles et al., 2016, 2017). Because departures from particular study areas are hard to record and attract less interest than spring arrivals, most of our data on autumn migration comes from bird observatories. Whereas arrival (or departure) dates refer to birds from a single population breeding at a particular locality, passage dates usually refer to birds from much wider areas, counted at a point on their migrations. Some studies have compared first and median or mean passage dates from the same site over a period of years and found the various dates to be correlated with one another (Hu¨ppop & Hu¨ppop, 2003; Jenni & Ke´ri, 2003; Va¨ha¨talo et al., 2004; Sparks et al., 2005; Rubolini et al., 2007a,b). In addition, in years when first arrivals were early, the total arrival or passage period generally became more prolonged. But whatever the recording process, long-term counts from all these sources reveal similar general long-term trends in migration timing. Under the presumed influence of long-term climate warming, many birds now arrive in their breeding areas earlier in spring and depart later in autumn than in the past, spending from a few days to a few weeks longer per year in their summer quarters. Such changes have become apparent in a wide range of species at many localities across Eurasia and North America (see later). However, not all species have shown such changes. Some of the exceptions may result from observational deficiencies, for they refer to species that have undergone marked changes in status over the period concerned, making it more or less easy to detect the earliest arrivals and latest departures, where these dates were the measures used. Other exceptions are inexplicable and may be due to changes in conditions that are independent of temperature, such as wind patterns or food supplies. A lengthening of passage periods has been detected at bird observatories, where daily counts were made throughout the migration seasons. This trend was first quantified among long-distance migrants at Fair Isle off northern Scotland, in which migration at both seasons became spread over a longer period, with birds arriving not only earlier but also later as the years progressed (Miles et al., 2017). These changes were not due to more birds moving through each year

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The Migration Ecology of Birds

BOX 23.1 Studies of migration timing on Fair Isle, Scotland. Since 1934, Fair Isle off northern Scotland has hosted one of the first and best known bird observatories in the world. Based on daily counts over 60 years (1955 2014), the pattern of migration timing was examined in 13 species of long-distance migrants that passed through but did not breed on the island. In each year and each season, the timing of the full migration period of each species was quantified using ten metrics, namely: the first observation date, the 5th, 10th, 25th, 50th (median), 75th, 90th and 95th percentile dates, the last observation date and the mean date. These ten metrics were selected because they collectively spanned the total migration period and provided a detailed insight into the full migration timing of each species. For each species in each season, the ten metrics of migration timing were not strongly or consistently positively correlated with each other. This meant that, on Fair Isle, no single metric could be used as a reliable proxy for all nine others, or as a proxy for the overall migration period. In spring, the timing of the early migration phase (first date, 5th and 10th percentiles) had become earlier in most (11 out of 13) species, and for some species substantially earlier (up to 18 days over 60 years). Yet, in most species, there was relatively little change in the timing of the core migration phase (25th, 50th and 75th percentile dates and the mean date). Furthermore, the late migration phase (90th and 95th percentiles and last observation date) in most species changed little through the years or in seven species became later by up to 14 days in different species. In autumn, as in spring, in most (11 out of 13) species, the timing of the early migration phase became earlier, and in some species substantially so (up to 24 days in different species). Again, however, in most species, the timing of the core migration phase changed relatively little. In the late migration phase, later migration movements were detected across the 60 years in 11 of the 13 species. Such delays were often sizeable, up to 16 days in different species. Overall, in most species, in both spring and autumn, the early migration phase became earlier, the core migration phase changed little and the late migration phase either changed little or became later producing a ‘fan-shaped’ pattern of migration timing across the 60-year period. Consequently, by the end of the study, most species showed a longer migration period, often substantially so, in both spring and autumn (up to 5 weeks in each season). A minority of species showed little change in migration timing across the 60 years, as found in the Common Redstart (Phoenicurus phoenicurus) and Whinchat (Saxicola rubetra) in spring and Pied Flycatcher (F. hypoleuca) in autumn. Further investigation showed that the expansion of the migration season could not be explained in any species by increasing abundance or by individuals spending longer periods on the island; it could only have been due to genuine changes in migration timing at the population level. The timing of migration in spring and the following autumn, or in autumn and the following spring, were not closely linked. In all species, values of the ten phenology metrics for each spring generally were not strongly correlated with corresponding values for the following autumn, nor were values for each autumn strongly correlated with values for the following spring. In other words, migration timing in consecutive seasons was apparently independent; an early (or late) spring was not consistently followed by an early or late autumn, and the same was true of an early (or late) autumn compared with the following spring. From Miles et al. (2017).

or to their staying longer on the island. They could be explained only by genuine extension in migration seasons, although with a net trend to earlier (for more details see Box 23.1). The same lengthening trend was noted on a much wider scale using spring data for 195 species from 21 European and Canadian bird observatories (Figure 23.1; Lehikoinen et al., 2019). In most species, migration seasons started earlier and became more prolonged with increasing spring temperature. Overall, at these places, spring timings advanced by about one week in 57 years, being generally greater for the beginning and median phases of migration than the end phases. Short-distance migrants advanced the start of their migration periods more than long-distance migrants. Such changes were less noticeable in Canada than in Europe, even when corrected for the rate of temperature change. Further evidence for the lengthening of migration periods was provided for birds passing through a site in Pennsylvania (Van Buskirk et al., 2009).

Spring dates From 983 Eurasian bird populations in which first arrival dates in breeding areas were monitored over periods of years, 59% showed no significant change, 39% became significantly earlier and only 2% became significantly later (Lehikoinen et al., 2004). Both short-distance and long-distance migrants showed the same trends. From 222 populations for which mean passage dates could be calculated over periods of years, 69% showed no change, while 26% became significantly earlier and only 5% became significantly later. The average change of first arrival date over all species and sites was 0.37 days/year, while the equivalent figure for mean passage dates was 0.10 days/year, both

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FIGURE 23.1 The spring migration phenology indicator shows the median migration dates of bird species in European and Canadian bird observatories (temperate and boreal regions) according to LMM (linear mixed model) fit from 1959 to 2015. The year 1959 receives value 0 and annual bars show 95% confidence intervals. From Lehikoinen et al. (2019).

FIGURE 23.2 Mean first arrival dates of Common Chiffchaff (Phylloscopus collybita) and Eurasian Blackcap (Sylvia atricapilla) at eight coastal bird observatories in Britain during 1960 1996. In both species, the response to temperature is in the order of 2 3 days earlier per 1 C rise in mean spring temperature. From Sparks (2000).

Apr 20 Apr 10 Blackcap

Mar 31 Mar 21

Chiffchaff

Mar 11 1960

1970

1980 Year

1990

2000

figures being statistically significant. It is not obvious why the two figures differed, but in general, the mean migration dates were based on larger, more standardized data sets. Despite the long-term trends, migration and arrival dates still fluctuated from year to year in line with local temperatures (Figures 23.2 and 23.3).1 Typically, most birds arrived about 2.5 3.3 days earlier for every 1 C increase in spring temperature (based on 203 regression analyses for different Eurasian bird populations, Lehikoinen et al., 2004). In a similar analysis from sites across Europe over the period 1960 2006, using many of the same data, first arrival dates advanced, on average by 0.37 days/year (as above), while median arrival dates advanced significantly less, at 0.158 days/year; nevertheless, the two dates were correlated (Rubolini et al., 2007a,b). The smaller number of studies available from North America revealed some similar trends (Bradley et al., 1999; Inouye et al., 2000; Butler, 2003; Mills, 2005a; Murphy-Klaassen et al., 2005; Van Buskirk et al., 2009), although in some eastern parts of the continent, longterm change in temperature and migration dates were less marked than in Western Europe. Another major metaanalysis of the timing of spring migration, mainly in Europe and North America, found that, on average, birds have significantly advanced their spring migration time by 0.21 days/year and 1.2 days/ C (Usui et al., 2017). The records involved in this study spanned a period of 265 years (1749 2014), but most were obtained in the last half-century. Despite strong correlations between arrival dates and temperatures in breeding areas, much of the variance in arrival dates remains unaccounted for. However, arrival dates are also influenced by weather further down the migration route or in wintering areas (Sokolov, 2006; Haest et al., 2020), as well as by other aspects of weather such as wind, and by different factors such as food supply (Chapter 15). Poor weather on one part of the route can hold up migration, even though conditions may be favourable further along the route. One example of the effects of conditions on migration routes is provided 1. Most researchers have used annual temperatures from localities on the migration route or breeding area, while some have used the winter spring index of the North Atlantic Oscillation (NAO), a large-scale climate phenomenon influencing weather in this region (e.g., Hu¨ppop & Hu¨ppop, 2003; Va¨ha¨talo et al., 2004; Stervander et al., 2005; Sokolov, 2006; Zalakevicius et al., 2006; Van Buskirk et al., 2009). The NAO index is calculated as a difference in normalized values of atmospheric pressure between the Azores and Iceland for each month. Positive values indicate warmer and wetter winter spring weather (followed by earlier spring migration) in northwest Europe and the opposite weather conditions and later arrival dates than usual in southern Europe (for further details of the NAO see Chapter 29).

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The Migration Ecology of Birds

FIGURE 23.3 (a) Mean first arrival dates of Barn Swallows (Hirundo rustica) averaged for seven bird observatories in Britain, 1970 1997, during which time mean arrival dates advanced by about 1 week in association with gradual spring warming. (b) Relationship between mean first arrival date and the mean temperature for February March in the breeding areas. From Sparks et al. (1999).

Mean arrival date

Apr 8

Apr 1

Mar 25 1970

1975

1980

1985 Year

1990

1995

FIGURE 23.4 Rate of change in first arrival dates (days per year) of 56 bird species in Lithuania (Zuvintas Strict Nature Reserve) in 1966 1995, in relation to their average arrival dates. Regression (day 151 January): change 5 0.0003 3 day2 1 0.071 3 day 4.933, r2 5 55.2%. Negative values indicate earlier arrival. From Lehikoinen et al. (2004), based on Zalakevicius & Zalakeviciute (2001).

by the Hudsonian Godwit (Limosa haemastica) which breeds in two distinct areas in North America (Senner, 2012). Over a 37-year period, spring arrival dates at Beluga River in Alaska became 9 days earlier than in the early 1970s, whereas in Churchill, Manitoba, arrival dates became 10 days later. This difference occurred even though these two populations shared the same wintering grounds and the same migration route for much of the journey. It was associated with a recent divergence in climatic conditions in the last fifth of the journey, after the two populations had separated to take different routes. Not all studies have shown a single sustained long-term trend in migration dates. For example, at the Rybachy Bird Observatory on the Courish Spit in the southeastern Baltic, warm springs in the 1930s and 1940s, and then in the 1960s and 1980s, were associated with significantly earlier migration in many species of passerines, while colder springs during the 1950s and 1970s were associated with later passage (Sokolov et al., 1998). At a reserve in the southern Urals, the arrival dates of 16 studied species had not changed over the years 1971 2005. This was explained primarily by the absence in this region of any long-term trend in spring weather, although arrival dates still varied from year to year, according to local spring temperatures (Sokolov & Gordienko, 2008). Overall, in the spring migration dates of different species over recent decades, several patterns have emerged: G

G

Greater changes have occurred in the spring migration dates of early-migrating than of later-migrating species (Figure 23.4). This was associated with the weather (including temperature) having changed to a greater extent earlier than later in the spring (for passage dates, see Sokolov et al., 1998, for arrival dates at breeding sites, see Slagsvold, 1976; Loxton & Sparks, 1999). Greater changes have occurred in the arrival dates of short-distance than long-distance migrants presumably because short-distance migrants generally arrive earlier in spring (same point as above) and show more flexibility in their migration timings (Tryjanowski et al., 2002; Butler, 2003).

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G

G

G

G G

489

Greater changes have occurred in the arrival dates of small bird species than large ones. This was possibly because the smaller species were more sensitive to annual temperature differences and their effects on food supplies (although their shorter generation times would also have favoured more rapid genetic change than was possible in large, longer-lived species). However, other studies found that larger species showed more advance than smaller ones (Usui et al., 2017), possibly because larger species were better able to withstand lower temperatures. Year-to-year arrival dates of short-distance migrants generally showed a correlation with spring temperatures in the breeding locality, but such correlations were less obvious in long-distance migrants (Tryjanowski et al., 2002). Moreover, where it was explored, weather back along the route often showed a better relationship with arrival dates than did weather at the arrival location itself (e.g., arrival dates of Barn Swallows in Britain were more strongly correlated with weather in France Spain than with weather in Britain, Huin & Sparks, 1998). Spring weather has not changed everywhere in the same way. Correspondingly, the degree of change in bird arrival dates in breeding areas has varied geographically, with arrival dates in most areas getting earlier as springs have warmed, but in some areas getting later as local springs have cooled. In the western Mediterranean region, springs have become cooler than previously, which may have further slowed the return of long-distance migrants from tropical Africa to the mid and higher latitudes of Europe. Advances in arrival dates showed no clear relationship with habitat or diet (Usui et al., 2017). Most species still arrived in particular breeding areas earlier in warm springs than in cool ones.

Four explanations may account for the fact that more short-distance migrants than long-distance migrants now arrive earlier in spring, and in closer correlation to temperatures in breeding areas. First, the stronger endogenous control of migration in long-distance migrants might dampen any reaction to a changing environment (Gwinner, 1986; Berthold, 1996). Short-distance migrants are typically more flexible (facultative) in their response, and more able to alter their behaviour in relation to prevailing conditions (Chapter 13). Second, the closer a species winters to its breeding areas, the more closely correlated are the day-to-day weather changes in the two areas, enabling short-distance migrants to react more rapidly and appropriately. Third, the longer the journey, the more likely are birds to meet adverse weather that holds up migration for a time. Fourth, as mentioned above, over much of Europe and North America weather in early spring, when most short-distance migrants arrive in their breeding areas, has improved more than weather later in spring, when most long-distance migrants arrive. Because in most bird species, males arrive in breeding areas before females (Chapter 15), studies based on first arrival dates concern males only. Nevertheless, studies of various songbird species migrating through bird observatories in spring revealed that both sexes have responded to warmer springs, with males remaining ahead of females by about the same amount as in earlier years (Rainio et al., 2007; Tøttrup & Thorup, 2008). On the other hand, a study of Barn Swallows in Denmark revealed that only males had started to appear earlier, while females arrived at about the same dates they did 30 years previously, giving no advance in egg-laying (Møller, 2004). Earlier arrival in breeding areas in response to warmer weather could be brought about by birds: (1) leaving wintering areas earlier, (2) increasing the speed of spring migration (through reducing numbers or durations of stopovers), (3) wintering closer to the breeding area, or (4) a combination of these various possibilities. Evidence for changes in all these respects has emerged from studies of tracked birds (Chapter 13), and more rapid progress in warm springs than in cold ones has been recorded in many migrants from the dates they pass through successive observation sites in different years. Of more interest, perhaps, is why some species have shown no change in spring migration dates over the years, even though spring temperatures in breeding areas have risen. For example, contrary to other waders nesting in Iceland, the Eurasian Whimbrel (Numenius phaeopus) has not changed its arrival dates in more than 30 years (Carneiro et al., 2019). Tracked individuals were more consistent in their timing of spring than their autumn migration, and the most consistent stage in spring was departure from wintering sites. Stability in migration dates over long periods may result from inflexibility in schedules or life histories.

Autumn dates Changes in autumn migration dates over recent decades have been generally less, and more variable, than changes in spring dates (Gatter, 2000; Bairlein & Winkel, 2001; Fiedler, 2001; Sparks & Mason, 2001; Hu¨ppop & Hu¨ppop, 2005; Jenni & Ke´ri, 2003; Lehikoinen et al., 2004; Mills, 2005; Sokolov, 2006; Van Buskirk et al., 2009; Miles et al., 2016). Two patterns have emerged, involving either earlier or later departures over the years. In some single-brooded populations, especially those that winter in the tropics, earlier arrival is followed by earlier breeding and moult, resulting in birds being ready to depart earlier. In such populations, the timing of successive events through the summer, including

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arrival, egg-laying, hatching, fledging, moult and autumn migration, are all correlated with spring temperatures, and departures show little or no relationship with the prevailing autumn temperatures (Chapter 13). Birds depart as soon as their physiological state permits, but an earlier spring arrival pulls the whole cycle forward to give an earlier autumn departure (Ellegren, 1990; Sokolov et al., 1998; Sokolov, 2000, 2001; Bojarinova et al., 2002). At Rybachy on the southern Baltic coast, the warming of the 1960s and 1980s led to significantly earlier mean dates of spring passage, of breeding and of autumn passage. Conversely, colder springs during the 1970s caused a shift towards later spring passage, later breeding and later autumn passage (Sokolov et al., 1999). These trends occurred in both short-distance and long-distance migrants. But most of the migrants through Rybachy came from northerly breeding areas that gave time for only one brood. Similar relationships were found for single-brooded long-distance migrants passing through the Swiss Alps in autumn (Jenni & Ke´ri, 2003). The long-distance migrants may have benefited in autumn from an earlier crossing of the Sahara, enabling them to reach the Sahel zone to the south well before the wet season ended. In contrast, shorterdistance migrants passing over the Alps and wintering north of the Sahara mostly showed a later autumn passage. These were chiefly passerine species that could raise more than one brood per year, so they could better take advantage of a longer season by remaining longer in their breeding areas. Further south and west in Europe, where individuals can raise two or three broods in the same season, departure dates of passerines have tended to get later as local temperatures rose (Bairlein & Winkel, 2001; Sparks & Mason, 2001), but it is not known whether this was associated with a lengthening of the breeding season. Similar trends were apparent among 78 songbird species passing through a banding station in Pennsylvania in autumn (Van Buskirk et al., 2009). Among short-distance (mostly multi-brooded) migrants wintering within North America, autumn migration became later over a 46-year period (1961 2006), but among long-distance (mostly singlebrooded) migrants wintering in the neotropics, the autumn passage became earlier, in parallel with the earlier spring passage.

TIMES SPENT IN BREEDING AND WINTERING AREAS Given the observed changes in migration timing, many birds might now be expected to spend more days per year in their breeding areas and fewer in their wintering areas than in the past. Such changes have been confirmed for European migrants migrating through Gibraltar and wintering in the Gambia in West Africa (Lawrence et al., 2022). In the species studied, time in Europe increased by 16 days, on average, during a 27-year monitoring period at Gibraltar (12 species, 1991 2018), while their stay in the non-breeding range declined by 63 days, on average, during a 57-year monitoring period in the Gambia (20 species, 1964 2019). These figures, referring to non-equivalent periods, still represent substantial changes to the annual routines of long-distance migrants. Similarly, at higher latitudes in Europe and North America, short-distance migrants among waterfowl and raptors are now spending more than an extra month in their breeding areas (Lehikoinen & Jaatinen, 2012; Van Buskirk, 2012). The later arrival of snow and ice in autumn may largely account for this, the movements of these birds being generally more flexible (facultative) than those of long-distance migrants wintering in the tropics.

ECOLOGICAL MISMATCHES The timing of spring migration is assumed to have evolved so that birds can arrive in their breeding areas early enough to ensure that young are raised when food is most plentiful (Lack, 1954). But climate change may now be affecting this long-established pattern. In many birds, the progress of spring migration is influenced by weather along the migration route, but the development of the food supplies that permit reproduction rests entirely on conditions in breeding areas. Any developing discrepancy between conditions on route and conditions in breeding areas could lessen the synchrony between chick-rearing and food supply. In addition, in the breeding areas themselves, birds may respond more or less rapidly than their food organisms to temperature rise, so that the two get further out of step with one another. With many studies reporting a greater advance of spring migration timing in short-distance than in long-distance migrants (Lehikoinen et al., 2004; Rubolini et al., 2007a,b; Miller-Rushing et al., 2008; Usui et al., 2017), this trend could cause a greater mismatch in the long-distance birds. This is the majority finding, but other studies have found no difference in the degree of advance in migration times between short and long-distance migrants (Hu¨ppop & Hu¨ppop, 2003; Zalakevicius et al., 2006) or even a reverse pattern (Stervander et al., 2005; Jonze´n et al., 2006a). These differences among studies may result from differences in the pattern of climate change between regions or time periods, or from differences in methodology or sampling bias.

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An apparent example of mismatch is provided by Pied Flycatchers (Ficedula hypoleuca) nesting in the Netherlands and elsewhere, where climate change has led to earlier development of the food supply on which breeding depends, but spring migration has not advanced sufficiently to allow flycatchers to make such good use of this food supply as they did in the past (Both & Visser, 2001). Despite advancing egg-laying by as much as 10 days, this was still too late for the food supply, resulting in reduced breeding success. In areas with the biggest mismatch, population levels declined by about 90% over a 20-year period (Both et al., 2006). Other late-arriving woodland species which relied on a narrow food peak for breeding, such as the Wood Warbler (Phylloscopus sibilatrix) and Icterine Warbler (Hippolais icterina), also showed big declines in breeding numbers. However, marshland species which had the advantage of a longer food peak showed at most a slight decline in breeding numbers (Both et al., 2009a). In contrast, residents and short-distance migrants which in both habitats were present earlier in the season showed no decline. In addition, long-distance migrants declined more severely in forests in Western Europe than in northern Europe, where temperatures during spring arrival and breeding had advanced less (Both et al., 2009b). The development of the vegetation and insects on which most birds depend in breeding areas is likely to be influenced by local temperatures and other conditions over the preceding several weeks. With this in mind, Saino et al. (2011) calculated the accumulated winter and spring temperatures (degree days) as a proxy for the timing of spring biological events in breeding areas. From studies on 117 bird species from various parts of Europe over five decades, they found that migrants, and particularly those wintering in sub-Saharan Africa, now arrive at higher accumulated degree days than in the past, and thus become increasingly mismatched to spring phenology. These birds reach breeding areas earlier than in the past, but again not early enough to keep up with the extent of climate warming. Species with the greatest thermal mismatch showed greater population declines. These findings provide additional support to the ideas that some migratory birds are in some areas becoming progressively mismatched with their food supplies and that failure to respond adequately can cause population declines, presumably through reduced reproductive output (Saino et al., 2011). Another large-scale study in North America combined satellite images and citizen science (eBird) data to estimate changes in the interval between spring ‘green-up’ and migratory arrival for 48 breeding passerine species across the continent. Dates of both arrival and green-up changed over time, usually in the same direction (earlier or later). Birds adjusted their arrival dates, but nine of 48 species did not keep pace with rapidly changing green-up, and across all species, the gap between arrival and green-up increased by over half a day per year over the 12 years, 2001 2012. As green-up became earlier in the east, the arrival of eastern breeding species increasingly lagged behind, whereas in the west where green-up typically became later birds arrived increasingly earlier relative to green-up. These findings highlight that the timing of species arrivals and vegetation development have changed at different rates and in different directions. Any change could produce mismatches with adverse effects on bird breeding. Because long-distance migrants could have no clue from their wintering areas of weather conditions on their breeding areas, several thousands of kilometres away, it has been assumed that big mismatches could be rectified in the longer term only by changes in the genetic control mechanism, so as to promote spring migration at an earlier date. Departure dates from wintering areas are apparently triggered primarily by a photoperiodically timed endogenous rhythm, evolved through natural selection, which ensures that birds leave in time to reach their breeding areas at an appropriate date, although adverse conditions locally or on route can also delay migration beyond the optimal date (Chapter 13). Only by further evolution acting on this endogenous control mechanism is the primary trigger date for departure likely to be changed. In this situation, the selection pressure to migrate earlier is applied in the breeding area, but the action to accomplish an earlier arrival occurs weeks earlier in the wintering area, hundreds or thousands of kilometres away (Visser et al., 2004). Changing this control mechanism may be a relatively slow process, perhaps explaining why the year-to-year arrival dates of long-distance migrants are less well correlated with temperatures in breeding areas than are the arrival dates of short-distance migrants, wintering nearer to breeding areas and able to respond to weather facultatively. The need for a genetic change in the control system was suggested as one reason why flycatchers were returning too late to take advantage of the earlier peak in their caterpillar prey. However, it was later found that Pied Flycatchers and other species had indeed advanced their passage through North Africa by 2 weeks between 1980 and 2005, easily enough to cancel the mismatch. The subsequent delay was caused by conditions further north in Spain and France where temperatures during the time of flycatcher passage had not changed over the years in parallel with those in more northern breeding areas (Both, 2010; Jonze´n et al., 2006b). So, although the flycatchers arrived earlier in southern Europe, they were then delayed on the next stage of their journey. The gap between arrival and egg-laying became shorter over the years, but birds were still too late to catch the food peak. Another mismatch was found in American Robins (Turdus migratorius), which breed at high elevation in the Rocky Mountains of Colorado. Their spring arrival dates advanced by 2 weeks over a 20-year period, but at the same time,

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winter snowfall increased and took longer to melt, giving a mismatch between arrival dates and the exposure of bareground feeding areas (Inouye et al., 2000). Mismatches were also shown in seven of eight American warbler species, where wintering and staging areas had not warmed as much as breeding areas, again leading to arrival after the advancing resource peak (Strode, 2003). Different mismatches have been described in some arctic nesting geese which are now arriving in their breeding areas too late for their goslings to catch the most nutritious stage in the growing vegetation on which they feed, with mismatches up to 20 days, affecting gosling growth and reproductive output (Doiron et al., 2015; Ross et al., 2017; Lameris et al., 2017). These examples raise the general point that the photoperiodic responses of many birds may have become less reliable predictors of seasonal change in food supplies as climate has warmed. This is not a new problem, as it is faced by all birds which expand their breeding ranges into different regions, but it may take time for them to adjust genetically to new situations, during which time they could perform less well than usual, sometimes with effects on population levels. The effect of mismatches on population trends is discussed further in Chapter 29.

OTHER CLIMATE-DRIVEN CHANGES Over 40 years on the Crozet Islands in the Southern Ocean, winds have generally strengthened and moved poleward (Weimerskirch et al., 2012). Long-term demographic and foraging records revealed that Wandering Albatrosses (Diomedia exulans) shifted their foraging ranges poleward over this period in conjunction with wind patterns, while their rates of travel and flight speeds increased. Consequently, in the 20 years from 1990, the duration of foraging trips declined and breeding success improved. In addition, the birds increased in body mass by more than 1 kg from their initial weights of about 8 kg in females and 9.5 kg in males. Foraging performance thus emerged as the key link between climate change and population processes.

OTHER RAPID CHANGES IN BEHAVIOUR Some of the changes in distributions and migration timing seen in birds over recent decades have occurred so rapidly that they must have involved many individuals switching from one type of behaviour to another. Such switches have been confirmed by ringed individuals, as in the shortening of the spring migration of Barnacle Geese to establish new colonies 1300 km south of the traditional breeding range (Larsson et al., 1988), or the shifting of migration routes of Ruffs (Calidris pugnax), 1500 km further east from western to eastern Europe (Verkuil et al., 2012; Chapter 30). In addition, in long-lived species, individuals have improved their migratory performance during their lifetimes (Sergio et al., 2014), and in social species, some individuals have altered their migration patterns by learning from others (Mueller et al., 2013; Palacı´n et al., 2011). But neither of these latter changes are necessarily associated with environmental change. Over recent decades Icelandic Black-tailed Godwits (Limosa limosa islandica) changed their migration timing, and expanded their wintering and breeding ranges, but almost all this change was brought about by the pioneering behaviour of juveniles. Older birds continued to do what they had always done, returning year after year to the same breeding and wintering localities, and often also to the same stopover sites on migration. They also tended to travel at about the same dates each year, to within a few days (Figure 23.5). Evidently, individuals of this species established their behaviour in their first year, and stuck mainly to the same patterns for the rest of their lives. Distributional changes thus resulted from generational shifts, as young birds adopted different behaviour from their parents (Gill et al., 2014a,b, 2019). The same held in another population of Black-tailed Godwits Limosa l. limosa in which young birds changed a major stopover site from one area to another 300 km north, while adults continued to use the old site (Verhoeven et al., 2018). It also occurred in Common Cranes in which immatures wintered in the nearest of two wintering areas, contributing more than adults to a shortening of migration routes and northward shift in wintering range (Alonso et al., 2008). In contrast, though, in North American Whooping Cranes (Grus americana) older birds seemed to be the main innovators, as groups containing older, more experienced individuals established new overwintering sites closer to the breeding grounds, leading to a rapid population-level shift in migration patterns. These new sites were in areas where temperatures and food availability from agriculture increased, improving conditions for overwintering (Teitelbaum et al., 2016). Another big change in migration route and breeding area was recently recorded among Pink-footed Geese (Anser brachyrhynchus) which bred on Svalbard and wintered mainly in Denmark (Madsen et al., 2023). With a ten-year period, some of these geese had switched to breeding on Novaya Zemlya, some 1000 km east of Svalbard and involving a 24% longer journey. Novaya Zemlya had apparently become more suitable as a breeding area as a result of climate change. It is not known how the first Pink-feet reached this area, but they may have travelled in flocks of other geese,

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FIGURE 23.5 Dates of spring arrival into Iceland of (a) 54 individually marked Black-tailed Godwits recorded on arrival in 4 8 years, during the period 1999 2012 (filled circles, ordered from earliest to latest) and the rates of change (open circles, days per year) in arrival among these individuals, and (b) 46 individuals hatched in different years (y 5 1496 0.69 3 , r2 5 0.34, P , .001), and subsequently recorded on spring arrival. The findings indicate that individuals occupy a fairly consistent place in the arrival sequence, although varying slightly in arrival dates from year to year. They also show that individuals arrive earlier if they were hatched in later years. From Gill et al. (2014).

notably Taiga Bean Geese (Anser fabalis) which already had a migration route there. Other Pink-feet then travelled with the pioneers, giving within a few years a new population of 3000 4000 pairs, formed by continued immigration and local breeding. These birds have so far maintained the same wintering area in Denmark.

GENETIC AND FACULTATIVE RESPONSES These various observations, along with the breeding experiments discussed in Chapter 22, all serve to confirm that migration is a dynamic process, subject to continual change in response to prevailing conditions. Some aspects, such as an abrupt change in the direction of migration, imply rapid evolutionary change, but other aspects could represent either genetic or facultative responses to changing conditions. In any marked long-term change, both are likely to be involved, the birds responding initially by facultative means, and eventually by genetic change, as natural selection comes increasingly to bear. Facultative responses are relatively limited (though variable in extent between species), and if environmental conditions continue to change in the same direction, such responses become inadequate to deal with the new conditions. Only genetic change may then enable the population to respond appropriately to conditions beyond the previous range.

Genetic responses Although all main aspects of migratory behaviour studied in captive birds have been shown to have heritable components (Chapter 22), genetic change over a period of years is not easy to demonstrate in wild birds. The most convincing way is to test wild birds in standard conditions in captivity, but this requires compliant species and suitable facilities. The assumption is that if individuals taken from the wild in different years or from different regions express behavioural differences when kept under identical conditions, these differences are likely to have a genetic

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basis. This conclusion is strengthened if the trend is maintained in captive-bred offspring from these birds, unaffected by other parental effects or experiences in the wild. Such a test was made on samples of Eurasian Blackcaps randomly collected as nestlings from the same locality and hand-raised each year over a 13-year period (Pulido & Berthold, 2004, 2010). In successive samples of birds, the amount of autumn migratory activity was found to decline towards a later onset and reduced intensity (less activity per night). Similarly, Pied Flycatchers were taken from the wild to examine the timing of various events within their annual cycles. After 21 years of global warming, the experiment was repeated in identical conditions, using birds from the same German study site. The phase of the circannual clock, which controlled spring moult, migration and reproductive timing, had advanced by 9 days. The wild population mirrored these changes, concurrently advancing egg laying by 11 days (Helm et al., 2019). The findings from these experiments on Blackcaps (for autumn migration) and Pied Flycatchers (for spring migration) were precisely as expected if the populations had responded genetically to changing conditions, so at least in these species the changes observed may represent a genetic response resulting from natural selection. In any population the rate of evolutionary change is limited by (1) the amount of genetic variation within the population at the time; (2) the strength and consistency of selection pressure; and (3) the extent to which selection on one trait causes parallel changes in others, which could be beneficial or detrimental. Genetic variance can be reduced in populations that have suffered recent numerical declines in which much of the variance was lost (genetic bottlenecks). Such variance can be increased again by immigration and gene flow from another population, or in the longer term by mutation and other means. However, immigration and gene flow can also have deleterious effects if they break up locally adapted gene complexes and make a local population less well adapted to local conditions. Single selection events, such as spring storms, can cause a rapid genetic change in the arrival dates of populations (Chapter 22), but counter-selection pressures could rapidly reverse the situation, and change arrival dates back to their original state. Selection pressures must act consistently in the same direction over several generations if they are to have any more than temporary effects on the genetic composition of a population. Most selection probably acts to stabilize the gene pools of populations rather than to change them. Moreover, most migratory traits (notably incidence, intensity and timing) are part of a syndrome of co-adapted traits (Pulido & Berthold, 2003), so selection on one trait is likely to have simultaneous effects on the others. If this is disadvantageous in the new conditions, it may take many generations of selection to dissociate the beneficial traits from the detrimental ones before evolutionary change can occur. Evolutionary change may thus be rapid or slow, depending on circumstances.

Facultative responses The most convincing evidence for the existence of facultative responses comes from marked individuals in the wild which behave differently in different years, depending on prevailing conditions. Lots of evidence has emerged that individuals adjust their spring arrival dates to current conditions, or migrate in some autumns or habitats but not in others or migrate at different dates and for different distances in different years (Chapter 13). All these aspects could be under genetic influence, but the range of individual flexibility of behaviour in some populations is very wide (so-called ‘facultative migrants’, Chapter 13). One study confirming both significant heritability and directional selection on spring arrival dates nevertheless concluded that the advance of 6 days in the arrivals over 20 years of Great Reed Warblers (Acrocephalus arundinaceus) resulted from phenotypic plasticity rather than genetic change (Tarka et al., 2015). One consequence of facultative migration is that the proportion of migrants in a population could alter over time without the need for any genetic change. In particular, if the population increased or food declined, resulting competition could cause a greater proportion of birds to leave their breeding areas in autumn. Ring recoveries over the period 1960 1990 showed that an increasing proportion of Greenfinches (Chloris chloris) in southeast England performed seasonal movements. This change coincided with a period of population growth, so competition may also have intensified over this period (Main, 1996). Similarly, the proportions of ring recoveries of Common Linnets (Linaria cannabina) breeding in Britain, which came from the far end of the migration route in Iberia, increased over several decades (Wernham et al., 2002). This change coincided with big reductions in winter food supplies over much of the route (caused by loss of weed seeds through herbicide use), which could have stimulated more birds to migrate longer distances than before. Such changes could have resulted from either facultative or genetic responses to the altered conditions. Overall, both genetic and facultative responses are likely to be involved in modulating migration traits, with birds responding initially by facultative means, and eventually by genetic means, as natural selection comes into play. For this and other reasons, it is hard to separate totally genetic from facultative changes, considering that the limits to

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flexibility may themselves be genetically controlled, as in the comparison between obligate and facultative migrants (Chapter 22). But whatever the basis of the observed changes, it is presumably in these various ways that birds continually adjusted their migration patterns to the massive climate changes of the past, and through which we can expect them to respond in future.

SUMMARY Records indicate that many (but not all) bird species have changed some aspects of their migratory behaviour over recent decades or longer, in response to changed conditions, with (1) earlier arrival in spring, (2) earlier or later departure in autumn, (3) shortening or lengthening of migratory routes, (4) directional changes and (5) changes in ratios of resident to migratory individuals in particular breeding areas, and in the occurrence of wintering birds in regions previously lacking them. Almost all these changes are associated with changes in food availability, or with climatic conditions that are likely to have affected food availability, such as milder winters. Most examples of shifts to increasing migratoriness involve species that have extended their breeding ranges into higher latitude areas where overwintering is not possible or risky. Short-distance migrants, which winter within the northern continents and generally arrive earlier in breeding areas and depart later than long-distance migrants, have advanced their arrival dates and delayed their departure dates more than long-distance migrants. In general, around the globe, temperature rise associated with climate change has been more marked with increasing latitude, making longer-distance migrants more susceptible to mismatches between spring arrivals and optimal food supplies. Such mismatches are some of the least expected but most significant changes resulting from climate warming. They are caused by plants and invertebrates developing more rapidly in spring than previously, and more rapidly than migratory birds can adjust their arrival dates by the required amount. Mismatches may be one reason why long-distance migrants have in general declined more markedly than residents and short-distance migrants in recent decades. Some of the observed changes in migratory behaviour could represent an immediate (facultative) response to prevailing conditions, and others may have resulted from genetic changes caused by natural selection. Despite the difficulties of detecting genetic changes, evidence for a few species has indicated genetic changes in migration timing, and for at least one species in migratory intensity and direction. In practice, most changes in migratory behaviour are likely to start as facultative responses which become genetically entrenched as selection comes to act in a more consistent manner from year to year.

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Chapter 24

Glacial legacies in bird migrations

Northern Wheatear (Oenanthe oenanthe) whose migration routes are thought to reflect post-glacial colonization patterns It is comparatively easy to trace the probable steps in the evolution of the migrations of some species, and some routes have developed so recently that they still plainly show their origin. Fredrick C. Lincoln (1935)

This chapter examines some of the more puzzling migrations of birds to understand how they might have evolved, and why they continue to persist. Some extraordinary journeys can be explained most plausibly in terms of past conditions likely to have influenced their development. The conditions most relevant to current migration patterns relate to the last glaciation which at its southernmost limit ended about 11,700 years ago, and progressively later further north. During this glaciation, most of the northern continents were covered in ice, so current migration patterns in these areas must have evolved since then. Five aspects are considered here: (1) indirect migration routes and seemingly unnecessarily distant wintering areas; (2) migratory divides; (3) long migrations over seas or other hostile areas; (4) loop migrations; and (5) the development of migration, from lower to higher latitudes and from higher to lower latitudes. The main conclusion is that many current migration routes and patterns can be explained in terms of post-glacial conditions.

INDIRECT ROUTES TO DISTANT WINTERING AREAS To minimize travel costs, birds would be expected to take the shortest, most direct routes between their breeding and wintering areas which should ideally be as close as possible. Yet many birds take long roundabout routes between one area and the other or use breeding and wintering areas exceptionally far apart, ignoring other much closer and apparently suitable areas. The challenge is to understand why. Some roundabout routes might be explained on grounds of The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00004-X © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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safety, if the shortest route is more risky (say with adverse winds or sea-crossings), or on grounds of competition avoidance (if closer areas are already occupied by other populations of the same or similar species). However, these explanations seem unable to account for all such migrations, some of which can most plausibly be explained by past events, with populations now migrating along ancient colonization routes. A likely example is provided by the Northern Wheatear (Oenanthe oenanthe), which from Eurasia colonized Greenland and northeast Canada in the west and Alaska in the east, yet continues to migrate to Africa (Figure 24.1). Greenland Canadian birds cross the Atlantic in one of the longest sea-crossings undertaken by a passerine, while the Alaskan birds cross the Bering Sea and travel via Siberia and then the Middle East, covering a distance of around 14,500 km to reach Africa (as confirmed by tracking, Bairlein et al., 2012). If Wheatears from the two ends of the breeding range were to migrate instead to South America or to Southeast Asia, respectively, where no Wheatears currently winter, they could halve their migration distances. Perhaps Africa is the only continent suitable for wintering Wheatears, but a more likely explanation is that the outlying populations have failed to evolve new routes. Suitable new routes would need a big step-change in direction, and any intermediate routes would land them in the south Atlantic or Pacific, respectively, so would immediately be selected against. It is not just Northern Wheatears that behave in this way. Several other species that have apparently colonized Alaska from the east end of Eurasia (eg the Arctic Warbler (Phylloscopus borealis) and Yellow Wagtail (Motacilla flava)) continue to winter in the Old World. The same is true for other species (eg Common Ringed Plover (Charadrius hiaticula) and Red Knot (race (Calidris canutus islandica))) that have apparently colonized Greenland and northeastern Canada from western Eurasia. Conversely, several other species (eg Grey-cheeked Thrush (Catharus minimus) and Pectoral Sandpiper (Calidris melanotos)) that have colonized eastern Siberia from North America continue to winter in the New World (Table 24.1). It is as though the current migration routes of these various species retrace their ancestral routes of spread from likely glacial refuges. As a species expands its breeding range, it simply adds step after step to its already existing migration route. The route we see now could thus be interpreted largely as a consequence of post-glacial colonization history (Thomson, 1926; Cox, 1968). Existing long-distance migration patterns, with most New World species migrating within the New World and most Old World species migrating within the Old World, may make it difficult for species to spread from one landmass to the other (Bo¨hning-Gaese et al., 1998). The few species that do breed and winter on both landmasses are mostly

Breeding range Wintering range

FIGURE 24.1 Migration routes of Northern Wheatears (Oenanthe oenanthe) from different parts of their breeding range (light shading) to their wintering range (dark shading) in Africa.

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TABLE 24.1 Species that breed in both Eurasia and North America, but winter entirely in the Old World or entirely in the New World. Recent colonists from Siberia to Alaska that winter in the Old World

Recent colonists from Alaska to Siberia that winter in the New World

Recent colonists from Europe to Greenland and northeast Canada that winter in the Old World

Northern Wheatear (Oenanthe oenanthe), Bluethroat (Luscinia svecica), Arctic Warbler (Phylloscopus borealis). Yellow Wagtail (Motacilla flava). White Wagtail (Motacilla alba). Red-throated Pipit (Anthus cervinus), Siberian Tit (Parus cinctus), Rustic Bunting (Emberiza rustica), Rufous-necked Stint (Calidris ruficollis), Pacific Golden Plover (Pluvialis fulva)a, Bar-tailed Godwit (Limosa lapponica)

Grey-cheeked Thrush (Catharus minimus), Pectoral Sandpiper (Calidris melanotos), Baird’s Sandpiper (Calidris bairdii), Buffbreasted Sandpiper (Tryngites subruficollis), Long-billed Dowitcher (Limnodromus scolopaceus), Snow Goose (Anser caerulescens), Sandhill Crane (Grus canadensis)

Northern Wheatear (Oenanthe oenanthe), Common Ringed Plover (Charadrius hiaticula), Red Knot (Calidris canutus islandica), Ruddy Turnstone (Arenaria interpres), Brent Goose (Branta bernicla hrota)

a

Small numbers now winter in coastal California, perhaps representing the start of winter range expansion in the New World.

northern species that could cross where the continents are closest together. Several such species now breed right across both North America and Eurasia, and winter in both the New and Old Worlds, respectively. Examples include many northern shorebirds and waterfowl, Peregrine Falcon (Falco peregrinus) and Merlin (Falco columbarius), and several passerines, such as Barn Swallow (Hirundo rustica) and Sand Martin (Riparia riparia). At some time in the past, all these species presumably colonized one northern land mass from the other but managed to evolve new migration routes within the continent most recently colonized. It may be partly a matter of time, with only the most recent colonists still retaining ancestral routes to old wintering areas, but this remains speculative. Seemingly unnecessarily long migrations also occur within the northern land masses themselves. Some bird species breed across the whole of northern Eurasia, for example but winter entirely in Africa or entirely in Southeast Asia (Table 24.2). Birds breeding at the most distant end of Eurasia thus travel across the entire west east span of this land mass, as well as to lower latitudes, to reach their wintering areas at one end. These species have presumably spread to breed across Eurasia from one end to the other, yet have again retained their ancestral wintering grounds. Some species, such as Greenish Warbler (Phylloscopus trochiloides) and Common Rosefinch (Carpodacus erythrinus), spread from Asia into Europe during the 19th 20th centuries but continue to migrate to Southeast Asia. Although they may follow ancestral routes of spread, these routes would presumably not persist unless they served their purpose in present conditions. However, a difficulty in evolving (by gradual change) new routes to totally new wintering areas may be the main reason for their continuing existence. Other migratory species that breed across Eurasia have split wintering grounds, with western populations moving southwest into Africa and eastern populations into Southeast Asia. These species may have survived the glaciations in more than one refuge, one lying near or within Africa and the other near or within Southeast Asia. For example the Great Reed Warbler (Acrocephalus arundinaceus) winters in both regions, so may have had two refugia (or groups of refugia), from which it subsequently spread across the Eurasian landmass (for other examples, see below under Migratory Divides). Alternatively, such species may have survived the last glaciation at one end of the land mass, spread across the whole land mass following ice melt and vegetation growth, and then developed a secondary wintering area at the other end of the landmass. Similar patterns are also evident within Europe. Thus, all Red-backed Shrikes (Lanius collurio) migrating from Europe to Africa cross at the eastern side of the Mediterranean, including those from Spain which start their autumn journey by flying northeast then east before turning south (Tøttrup et al., 2017). Marsh Warblers (Acrocephalus palustris) and Lesser Whitethroats (Curruca curruca) also migrate eastward before turning south into Africa. Why do they not fly directly southwest through Spain into Africa like many other species? Perhaps there is an adaptive explanation for the current roundabout route, but another possibility is that these species survived the last glaciation only in southeast Europe eastern Africa, and in post-glacial times spread first to the eastern then western part of Europe for breeding, with the western birds having so far failed to evolve a new and more direct route through Iberia into Africa. Similarly, other species migrate from southern Italy northward and then westward into Spain before moving southward into Africa, presumably for similar reasons (for Melodious Warbler (Hippolais polyglotta) see Pilastro et al., 1998; for

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TABLE 24.2 Different migration patterns of passerine species that breed across much of Eurasia and winter in the tropics. (1) Western and eastern populations winter entirely in Africa

(2) Western and eastern breeding populations winter entirely in Southeast Asiaa

(3) Western breeding populations winter in Africa and eastern populations in Southeast Asia, with a migratory divide

Common Whitethroat (Curruca communis), Garden Warbler (Sylvia borin), Willow Warbler (Phylloscopus trochilus), Spotted Flycatcher (Muscicapa striata), Common Redstart (Phoenicurus phoenicurus), Northern Wheatear (Oenanthe oenanthe), Rock Thrush (Monticola saxatilis), Ortolan Bunting (Emberiza hortulana)

Common Rosefinch (Carpodacus erythrinus), Lanceolated Warbler (Locustella lanceolata), Arctic Warbler (Phylloscopus borealis), Greenish Warbler (Phylloscopus trochiloides), Red-breasted Flycatcher (Ficedula parva), Taiga Flycatcher (Ficedula albicilla), Pechora Pipit (Anthus gustavi), Siberian Accentor (Prunella montanella), Redflanked Bluetail (Tarsiger cyanurus), Rustic Bunting (Emberiza rustica), Little Bunting (Emberiza pusilla), Yellow-breasted Bunting (Emberiza aureola)

Grasshopper Warbler (Locustella naevia), Great Reed Warbler (Acrocephalus arundinaceus), Lesser Whitethroat (Curruca curruca), Common Chiffchaff (Phylloscopus collybita), Eurasian Golden Oriole (Oriolus oriolus), Sand Martin (Riparia riparia), Barn Swallow (Hirundo rustica), Red-rumped Swallow (Cecropis daurica),

Common House Martin (Delichon urbica), Tawny Pipit (Anthus campestris), Tree Pipit (Anthus trivialis), Red-throated Pipit (Anthus cervinusm), Yellow Wagtail (Motacilla flava), Bluethroat (Luscinia svecica), Black Redstart (Phoenicurus ochruros), Desert Wheatear (Oenanthe deserti), Blue Rock Thrush (Monticola solitarius)

Note: Richard’s Pipit Anthus richardii breeds in the eastern Palaearctic, Africa and Australasia, but migrates in small numbers through Western Europe, presumably on route to Africa. a Including India.

Short-toed Snake Eagle (Circaetus gallicus) see Mellone et al., 2011). This detour adds 1000 km to the potentially shorter route southward from Italy across the sea to Africa. Another curious migration is shown by the Aquatic Warbler (Acrocephalus paludicola) which breeds in Eastern Europe but migrates first west to Western Europe before turning south to Africa (Salewski et al., 2019). This species might have colonized Eastern Europe from the west, then died out as a breeder in the west but retained its original migration route. Many other examples of curious routes to distant wintering areas can be found among Eurasian birds, and some have developed in recent years in association with range expansion (for the Paddyfield Warbler (Acrocephalus agricola) see Zehtindjiev et al., 2010). In North America, too, some species breed across the northern parts of the continent but concentrate to winter at lower latitudes entirely in the west or entirely in the east. About 33 species of the eastern forests are assumed to have spread westward, north of the prairies, in the boreal forests, yet migrate through the east of the continent on route to Neotropical wintering areas. Again, the implication is that, in the genetic control of migratory direction, progressive minor extensions or modifications to an existing route can develop more readily than abrupt big-step changes, taking the bird in a completely different direction. For many years, the view that some migration routes retraced ancestral routes of spread was no more than plausible speculation, but recent DNA analyses have added support. Rather than changing in response to selection pressures, parts of the DNA in organisms are thought to change at fairly constant rates over time, owing to mutations which alter the sequence of individual nucleotides along the length of the molecule. By comparing this sequence in equivalent pieces of DNA (usually mtDNA) in individuals from different parts of the breeding range, it is sometimes possible to work out their routes of spread, even when different populations diverge from one another. For example, Swainson’s Thrush (Catharus ustulatus) is now separated into two genetically distinct populations, one of which occupies the west coast region of North America north into Canada, and the other the northern part of the continent from Alaska to Newfoundland. The two populations meet and interbreed around the British Columbian Alaskan border. Judging from DNA dating, the two populations diverged during the last glaciation, when they were probably confined to separate southwestern and southeastern refuges from which they subsequently spread and met. They now have migration routes that seem to retrace their likely routes of spread from these two refuge areas (Ruegg & Smith, 2002;

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Ruegg et al., 2006). The western coastal population migrates south along the Pacific coast to western Central America and Mexico, whereas the continental northern population migrates southward over the Gulf of Mexico to northern South America (routes confirmed by tracking studies, Delmore et al., 2012). The spring migration of the northern population of this species, northward then westward, mirrors the expansion route of the boreal forest, following the last glacial retreat. Other North American species with similar distributions and indirect migration routes include the Hermit Thrush (Catharus guttatus) and Grey-cheeked Thrush (C. minimus) (Brewer et al., 2000). Western and eastern types of other North American birds also differ in mitochondrial DNA (for the American Yellow Warbler (Setophaga aestiva) see Milot et al., 2000; Boulet & Gibbs, 2006; for Fox Sparrow (Passerella iliaca) see Zink, 1994), suggesting that they diverged in separate western and eastern refuges. Similarly, two populations of Willow Warblers (Phylloscopus trochilus) breed in Sweden, the subspecies trochilus in the south and the subspecies acredula in the north. The two populations differ morphologically, and show different migration routes to different wintering areas, trochilus moving southwest into West Africa and acredula southeast into eastern and southern Africa (Bensch et al., 1999, 2002; Chamberlain et al., 2000). They can also be distinguished by their DNA or by the stable isotope ratios in their feathers, reflecting their different wintering areas where moult occurs (Figure 24.2). Their contact zone, at about 62 N and spanning 350 km, is paralleled in other species that breed in Scandinavia, both birds and other animals. Such examples are explained by the post-glacial colonization of Scandinavia which occurred along two routes, one from the southwest and the other from the east, over the northern end of the Baltic.

G 15N

12 11 10 9 8 7 6

Equator

55 57 59 61 63 65 67 69 Latitude

FIGURE 24.2 Recoveries of Willow Warblers (Phylloscopus trochilus) ringed in Sweden. Those from birds ringed in southern Sweden are shown as filled circles and those from northern Sweden as squares. The breeding distribution shows the approximate location of the hybrid zone between two subspecies (Phylloscopus trochilus acredula) in the north and (P. t. trochilus) in the south, where there is a migratory divide. The diagram shows the 13C signature in birds from southern Sweden, the hybrid zone, and northern Sweden. These data reflect the location of the winter moult in Africa, and hence the differing wintering areas of the two populations. The hybrid zone marks an area where ice during the last glaciation was unusually thick, so land to the north and south cleared much earlier, allowing colonization by plants and animals. When the ice went completely, organisms from the south and north could meet, producing hybrid zones, and in the case of the Willow Warbler, a migratory divide. Based on Chamberlain et al. (2000).

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Pink-footed Geese in the two populations referenced in Figure 25.3 look the same, but differentiated in mtDNA sometime in the last 10,000 years during glacial retreat, as the current Greenland-Iceland population became separated from the current Svalbard one (Ruokonen et al., 2005).

Further comments on the legacy of glacial changes Recent estimates suggest that more than 20 glaciations occurred in the last 2.5 million years, together occupying about 90% of this period (Newton, 2003). In each one, ice sheets spread from the poles to much lower latitudes than today, obliterating vegetation or pushing it southward, along with its animal inhabitants. During the peak of the glaciations, most European bird species (along with most plants and other animals) were confined to one or more of the three southern peninsulas of Iberia, Italy and the Balkans, although the latter two were joined across the top of the Adriatic Sea. Other glacial refuges existed in North Africa and on the Mediterranean Islands, as well as to the east of the Mediterranean. The islands were larger than today, and in some cases joined together, owing to lower sea levels. Each of these major refuge areas would not have provided a single stretch of uniform habitat, but rather a range of different habitats at different latitude and altitude zones, providing a big enough range of habitats overall to allow most European species to survive through the glacial maxima. During each interglacial, the ice retreated, allowing both plants and animals to spread from their glacial refuges to higher latitudes, and in many cases achieve a more continuous distribution. During each period of spread, migration systems would have had to adjust. Many existing migration routes, assumed to follow ancestral routes of spread, are likely to start within, or pass through, breeding areas occupied in glacial times. Depending on species and area, some such refuges may still be used for breeding, wintering or both. As indicated above, some species are thought to have survived the last glaciation in only one refuge area, and others in more than one. This is a plausible hypothesis for why in some species, the whole migration filters through one region, whereas in other species migrations separate (at a “migratory divide”) into different streams towards different regions. In species occupying more than one glacial refuge, the separate populations sometimes differentiated, giving rise to separate species or subspecies, which subsequently spread out from their refuges to form overlap or hybrid zones where they met (for review see Newton, 2003). Many such “suture” zones run roughly north south through central Europe, marking the overlap between taxa such as Common Nightingale (Luscinia megarhynchos) and Thrush Nightingale (L. luscinia), and Carrion Crow (Corvus c. corone) and Hooded Crow (C. c. cornix). The precise position of these suture zones varies from species to species, possibly reflecting differential rates of spread from their separate glacial refuges. Such divides are also apparent in taxonomically undifferentiated populations, such as the White Stork (Ciconia ciconia) and Eurasian Blackcap (Sylvia atricapilla) in Europe, although western and eastern populations of some such species may be separable through DNA analyses. This is the case in the Great Reed Warbler in which northwestern European populations are separable on mtDNA from more eastern ones (those east of Greece-Latvia, Bensch & Hasselquist, 1999). To judge from ring recoveries, 26% of 103 passerine bird species in Europe have migratory divides that are located along longitudinal lines in Central Europe, somewhere between 10 and 20 E (Møller et al., 2011). This is consistent with the assumption of a glacial origin for such divides in the Iberian and Balkan peninsulas followed by re-colonization of higher latitudes. In a review of DNA studies among European birds, evidence for geographical structuring was evident in 14 species. In North America, too, many birds were probably confined to southwestern and southeastern parts of the continent during glacial times, and still have distinct southwestern and southeastern wintering areas. Longitudinal suture zones occur through western North America, marking the overlap zone between such species as Lazuli Bunting (Passerina amoena) and Indigo Bunting (P. cyanea), and Bullock’s Oriole (Icterus g. bullockii) and Baltimore Oriole (I. g. galbula). These and other populations, on either side of these suture zones, whether classed as species or subspecies, apparently retained their ancestral migration routes, following different routes to different winter quarters. Other suture zones in North America occur around the northern Rocky Mountains, where populations spreading up west and east sides are likely to have met. Hybrid zones are apparent between the two forms of Swainson’s Thrushes, discussed above, and between the Audubon Warbler (Setophaga audubioni) and Myrtle Warbler (S. coronata) (Toews et al., 2014). In the Tundra Swan (Cygnus columbianus) which breeds across much of the North American tundra and winters on the west or east coasts, the migratory divide lies far to the west, near Point Hope in Alaska, and the bulk of the population (including that part directly north of the Californian wintering area) winters on the east coast (Figure 24.3). Knowledge of glacial history thus provides a plausible hypothesis of why some species, which now breed across a continental land mass, migrate to one end of that land mass while others migrate to the other end or both ends.

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FIGURE 24.3 Breeding and wintering ranges of the Tundra Swan (Cygnus columbianus) in North America, showing the migratory divide in Alaska. Birds from the southwest of the breeding range in Alaska winter on the western side of the continent, but birds from most of the breeding range winter on the eastern side of the continent.

Breeding range Wintering range

Based on present-day examples, many birds may have crossed the ice sheets during the glacial periods to breed on the restricted vegetated areas that persisted north of the ice. This idea is supported by the patterns of subspeciation seen in waders and other arctic breeding species today, in many of which different subspecies are centred on areas known to have remained ice-free in summer throughout the glacial periods (Ploeger, 1968; Newton, 2003). In this case, birds could have continued to nest at some locations in the far north throughout the Pleistocene glaciations, as well as in the interglacials. During the glaciations, however, they would have needed to cross hundreds or thousands of kilometres of ice between their breeding and wintering areas, longer distances than are covered today by those species that cross the Greenland ice sheet. Molecular dating has also pointed to the role of glacial cycles in leading to the subdivision and divergence of some arctic-nesting birds. For example, Red Knots now breed across the arctic tundra, with six subspecies differing in morphology, breeding areas, migration routes and wintering areas (Figure 25.4). DNA analyses suggest that Red Knots persisted through the last glaciation in Old and New World refugia, and diverged into two main lineages about 34,000 years ago (Conklin et al., 2022). Further subdivisions occurred much later, as the species spread over the new areas of tundra that emerged through glacial retreat, and probably involved at least two instances of secondary contact and interbreeding between birds from the two main lineages. This process of spread, admixture and differentiation produced the six subspecies of today. Similarly, the Dunlin (Calidris alpina) now breeds widely across northern Eurasia and North America, and five main genetic lineages have been recognized, each centred on a different breeding area (Wenink et al., 1993, 1996). All these lineages appear to have differentiated in isolation sometime in the late Pleistiocene and (like the Red Knots) to have maintained their differences as a result of strong philopatry. Further structuring of Dunlin populations occurred during the retreat of the ice sheets during the last 10,000 years. Other mtDNA analyses implied that: (1) some other species survived in a single refuge, from which they spread to their current ranges (for Common Eider (Somateria mollissima) see Tiedemann et al., 2004, for Marsh Warbler see Arbabi et al., 2014, for Boreal Owl (Aegolius funereus) see Koopman et al., 2005); (2). other species differentiated into two refuges (or groups of refuges) Savi’s Warbler (Locustella luscinoides) in Iberia and the Balkans (Neto et al., 2012), Great Reed Warbler somewhere in Western Europe and the Middle East (Hansson et al., 2008), Eurasian Skylarks (Alauda arvensis) in two main refuges (or groups of refuges) at opposite ends of Eurasia (Zink et al., 2008); and (3) Common Rosefinches occurred in three refuge areas, in the Caucasus, central-western Eurasia, and northeastern

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Eurasia respectively (Hung et al., 2012). Research on the evolutionary history of 63 bird species revealed that 59% of taxa showed divergent mtDNT lineages within species and 76% of these separations were dated to the Pleistocene glaciations (Avise & Walker, 1998).

Abrupt changes in migration routes How could a sudden change in migration route evolve? Clearly, if a single-step mutation took birds to a new wintering area where they could survive, this genetic change might be passed to subsequent generations, leading to the establishment of a new wintering area. However, big single-step changes are unlikely, and many that occur could take birds in inappropriate directions or across hostile terrain that they would be ill-equipped to cross. Even if they survived and returned successfully to breeding areas, they would be few in number and would be likely to pair with birds with normal directional preferences, probably resulting in the loss of the new directional trait. Unlikely such a successful step-change seems, it may have happened occasionally, beginning from vagrancy (Newton, 2008). Take, for example, Richard’s Pipit (Anthus richardi) which breeds on Siberian grasslands and normally winters in Southeast Asia (Dufour et al., 2021). Originally regarded as a rare vagrant, this species has appeared with increasing frequency in southwest Europe, and some individuals have returned to the same wintering area in southern France in different years. Studies involving geolocators revealed that these birds migrate an astonishing 6000 km to breed in central Asia, suggesting that a regular migration has now developed (Dufour et al., 2021). Another possible example concerns the Yellow-browed Warbler (Phylloscopus inornatus) which also breeds in Siberia and winters in Southeast Asia (Dufour et al., 2022). Also formerly regarded as a rare vagrant, hundreds of individuals are now recorded annually in Western Europe, including Britain. These warblers may have established new wintering areas, for which Western Europe lies on the route. One Yellow-browed Warbler was caught in January 2018 near Tarifa in Spain and re-caught at the same place in November of the same year, possibly wintering there or passing through in successive years (Tonkin & Gonzalez, 2019). Occasional spring records may reflect a return passage. A significant feature of both these examples is that change of route occurred on the same landmass, so its development would not have involved long over-water flights. Another factor of likely importance is that individuals with a new genetically determined route should be able to pass that route to their offspring. This is most likely to happen if, as shown in Blackcaps, individuals with the new route arrived on breeding areas before others, so paired selectively with one another (Bearhop et al., 2005). As yet, we do not have this information from these Siberian species. Moreover, an alternative explanation remains available, namely that both species have long migrated to Europe as a result of a migratory divide, but in such small numbers that they were long regarded as vagrants instead of regulars.

MIGRATORY DIVIDES Many species that have wide breeding ranges show a “migratory divide,” with the birds on each side taking different directions to different wintering areas. Often (but not always) such divides lead birds to circumvent geographical obstacles such as seas, deserts or mountain ranges. They have been described in many European species that fly to Africa via the shortest sea-crossings at the western and eastern ends of the Mediterranean. Examples include the White Stork, Black Stork (C. nigra), various soaring raptors, and some small warblers, such as the Blackcap, Common Whitethroat (Curruca communis) and Willow Warbler (Figure 24.2). Hence, while one explanation of migratory divides is that they represent the meeting point of populations that spread in post-glacial times from different glacial refuges, another proposes that they evolved more recently to circumvent barriers. The two explanations are not mutually exclusive, for while divides may persist as post-glacial legacies, they may now serve a secondary role in directing birds around unfavourable areas. However, the taxonomic or genetic differentiation shown in many species on either side of the divide implies long-term independent evolution, from a refuge-based origin. In some species, DNA analyses have dated the separation of west and east populations roughly to the last glacial period when these populations were refuge-based or beginning to spread (for Swainson’s Thrush in North America see Ruegg & Smith, 2002; Ruegg et al., 2006; for Blackcap in Europe see Pe´rez-Tris et al., 2004; Delmore et al., 2020). Whatever the origin of migratory divides, an interesting question is how they persist, given that directional preferences are inherited, and the populations on either side can (at least in theory) interbreed where they meet. The persistence of the divide may be due to the fact that migratory directions and distances inherited by hybrids are generally intermediate between those of their parents (Chapter 22). Hybrids arising in the contact zone might then be less viable than the parental forms, contributing to the maintenance of the divide, and the genetic integrity of both populations. In this case, migratory divides might help to continue the speciation process begun in glacial refuges by reducing

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interbreeding between the populations on either side of the divide. Intermediate migration routes and reduced survival of hybrids have been reported on the basis of genetic or geolocator evidence for Hermit Thrush and Swainson’s Thrush in North America (Alvarado et al., 2014; Delmore & Irwin, 2014). This reduced survival of hybrids would be expected to lead eventually, in each species, to reproductive isolation between the two forms, and thus to speciation. Different stages in this process are currently found at migratory divides, with taxa varying from barely differentiated forms showing frequent interbreeding, through recognized subspecies to full species showing little or no interbreeding. Hybrid zones can be relatively narrow. The transition between SW and SE migrating Blackcaps in Europe spans in different places only 10 86 km, presumably again the result of selection against hybrids which prevents the zone from spreading further (Delmore et al., 2020). Typically, hybrids show more variability in routes than the parent forms, and not all take an intermediate route through unfavourable terrain (Helbig, 1991; Delmore & Irwin, 2014). Among Willow Warblers in Sweden, in which one form migrates southwest and the other southeast, hybrids were found to take the route of one parent through a system of genetic dominance, so did not suffer the disadvantage of an intermediate route (Sokolovskis et al., 2022). Similarly, based on the stable isotope values of feathers grown in winter quarters, wild-hatched hybrids between the Pied Flycatcher (Ficedula hypoleuca) and Collared Flycatcher (F. albicollis) in Sweden wintered in the same African areas as Pied but not Collared Flycatchers. The authors argued that this pattern could explain the unexpectedly high annual survival of hybrid flycatchers, greatly reducing the ecological costs of hybridization (Veen et al., 2007). A similar dominant mode of inheritance from one parent was also shown in hybrids between the Great Reed Warbler and Clamorous Reed warbler (Acrocephalus stentoreus) which followed the migratory route of the former (Yohannes et al., 2011). One of the best-documented examples of non-hybridization at the divide concerns the Greenish Warbler, in which populations spreading northwards in post-glacial times around the west and east sides of the Tibetan Plateau met on the north side of the Plateau, in southern Siberia (Irwin et al., 2001). During their isolation, the two forms had not only developed minor genetic differences (recognizable in their mtDNA) but also different songs. Where they meet on the north side, birds from the two populations do not respond to one another’s song, so they do not interbreed significantly. In effect, they behave where they meet as different species, but are linked by a ring of interbreeding populations encircling the south side of the Plateau. The two forms migrate southward down the west and east sides of the Plateau to reach their wintering areas. Of 97 long-distance migrants breeding in Siberia, most (85%) use only one route around the Plateau (42 through Kazakhstan, 40 through eastern China). Of 15 species that use both routes, seven are known to have migratory divides between western and eastern subspecies, and others may do so (Irwin & Irwin, 2005). In four additional cases, migratory divides exist between western and eastern sister species. In the far north of Eurasia and North America, other migratory divides occur, especially among seabirds and waders which, on leaving the tundra, initially fly along the northern coasts before turning south along the Atlantic or Pacific coastlines. In Eurasia, many species show an abrupt migratory divide at about 100 E on the Taimyr Peninsula, with post-breeding movement west of that site being mainly west-southwest and east of that site mainly east-southeast, more or less parallel to the coast (Alerstam & Gudmundsson, 1999). The Taimyr Peninsula lies midway across the Eurasian land mass. Hence, in whatever way this divide evolved, it may persist largely as a result of distance-dependent flight costs, with all populations seeking the shortest route to potential wintering areas. However, not all tundra species show a divide at this point, and some take more southerly routes across the Eurasian landmass to their winter quarters. Any shorebirds migrating from Taimyr to India (say) would have to cross at least 5000 km of land (including the Himalayas) before reaching another marine coastal site. Around the Arctic, many migratory divides exist in the tundra, which coincide for many different species, suggesting colonization mainly from coastlines on the two sides of the continent (Henningsson & Alerstam, 2008). Other migratory divides occur in Greenland, with birds from the west and southern parts of the island wintering in North America, and those from the northeast wintering in Europe (for Snow Buntings (Plectrophenax nivalis) and others see Lyngs, 2003), presumably reflecting the areas from which they first entered Greenland. However, not all known migratory divides are as narrow as that mentioned above for the Blackcap, but can extend across several hundred kilometes, as described in Greylag Geese Anser anser nesting across coastal Finland (Piironen & Laaksonen 2023). The Red-necked Phalarope (Phalaropus lobatus) which breeds across the Arctic and winters on saline waters shows an especially interesting divide. One population breeds around the North Atlantic from Scotland across Iceland and Greenland into North America and flies up to 10,000 km mainly over water to winter in the tropical eastern Pacific Ocean. Another population breeds in northern Europe and Russia and migrates about 6,000 km largely over land to winter mainly on the Arabian Sea (van Bemmelen et al., 2019). These findings imply that Scotland was colonized from the west rather than from the nearer population to the east in northern Europe (Smith et al., 2018).

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FIGURE 24.4 Model depicting the evolution and maintenance of a migratory divide without the necessary involvement of glacial refuge areas. (A) Hypothetical starting scenario, with a continuous breeding range, and two separate wintering areas, each visited by birds from all parts of the breeding range. Migration costs are proportional to lengths of lines depicting routes. (B) Migratory divide resulting from differential survival consequent upon differential migration costs (or from migration costs plus asymmetrical competition favouring use of nearest breeding and wintering sites). In this model, the carrying capacity of the two wintering areas is assumed to be equal. The divide then appears mid-way through the breeding range, so that the populations on each side are of about equal size. (C) Situation resulting from differential survival consequent upon differential migration costs, together with wintering areas of markedly different qualities or carrying capacities. Since the carrying capacities of the two wintering areas are unequal, the migratory divide would be expected to shift from the centre of the breeding range towards whatever side had the wintering area of the smallest capacity. Other modifications to the model could be envisaged by changing the relative distances of the wintering sites from the breeding range, and hence the migration costs. Modified from Lundberg & Alerstam (1986).

Even in the absence of geographical barriers or twin glacial refuges, it is not hard to see how migratory divides may arise (Figure 24.4). Imagine a species with a wide breeding range that has two wintering areas near either end. Imagine now that migration costs increase with length of the journey, in proportion to the lengths of lines in Figure 24.4A. If birds with higher migration costs suffer greater mortality and return in smaller proportion to the breeding range, generation after generation, then segregation of breeding populations with a clear migratory divide will develop (Figure 24.4B). If competition on wintering areas is intense, this could lead to a gap in the breeding range of the species, because individuals migrating the longest distances to fill that gap could be disadvantaged during competition on the wintering range, and continually be eliminated by selection. Breakdown of the divide could occur if conditions in one wintering area were so good that birds from all parts of the breeding range benefited from migrating there. A migratory divide could in theory shift by populations changing their inherited migration direction under the action of natural selection, but a more likely mechanism would be through the spread of the more successful wintering population into the breeding range of the other, gradually replacing it (Figure 24.4C). If there are any divides that develop on the basis of flight costs, with birds from different halves of a wide breeding range migrating to different sides of a landmass, and with selection against hybrids that take intermediate directions, this process alone could initiate genetic divergence, with the two widely separated wintering areas having the same effect as past refuges. In conclusion, the various migratory routes and patterns of distribution described above could represent carry-overs from conditions prevailing long ago. But they would be unlikely to persist if they were markedly disadvantageous in present conditions. Nevertheless, the reason that some birds stick to their present migration routes may stem from the difficulty of making a single large-step change in migratory habits that would otherwise be beneficial: for example, a big change in direction that would greatly reduce the length of the migratory journey. For some of the patterns described above, alternative explanations have been proposed, again involving untested assumptions. However, the idea that glacial conditions and post-glacial colonization patterns could have influenced current migratory patterns is increasingly supported by DNA studies. Growing evidence implies that differences in the migration routes of populations separated by migratory divides promote genetic divergence and ultimately reproductive isolation associated with speciation (Delmore et al., 2015).

EVOLUTION OF BARRIER CROSSING It is easy to envisage how migration might evolve in species that have suitable areas for breeding and wintering adjacent to one another, giving a continuum of habitat between the two. This would then enable a gradual incremental lengthening of the journey. But it is more difficult to understand the origin of those migrations in which the breeding and wintering areas are separated by hundreds or thousands of kilometres.

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One possible way is through the loss of intervening habitat or populations. In many species whose breeding and wintering areas are now contiguous, the birds from the most northerly areas often migrate furthest, overflying the birds in intervening areas (leapfrog migration, see later). But if the intermediate populations for some reason died out, this would leave the outer areas, one for breeding and the other for wintering, with a gap between the two. The intervening population may die out through the gradual loss of intervening habitat so that birds initially migrating in continuous habitat find themselves crossing first short then increasingly longer stretches of unsuitable terrain. The main difficulty is to explain how land-birds could evolve an ability to cross large stretches of sea or desert which usually offer no opportunities for refuelling. If a species were to evolve such a migration today, it would entail not a gradual change in migration strategy but an abrupt change, with markedly greater fat deposition and flight lengths. One obvious possibility is that barriers which are now wide, such as the Sahara Desert, were once narrow, so that migration could have lengthened gradually as the barrier widened. Migrants would then have been able to lengthen their flights bit by bit to match the need. Climate changes, with their effects on vegetation, could thus lead to the splitting of a once-contiguous vegetation type, in the way that the Sahara Desert was once largely scrub-covered but now separates scrub to the north and south, or the boreal forest now separates open tundra from open steppe. This would enable birds to evolve gradually longer migrations as their breeding and wintering areas became progressively further apart. Alternatively, although a barrier may always have been wide, it may once have held more potential stopping places than are present now, perhaps more oases in the desert or more islands in the sea. If such stepping stones disappeared gradually as islands might be covered by rising sea levels this would have resulted in the progressive evolution of longer flights. Some long over-sea migrations are still hard to explain, notably those to Pacific islands (Piersma et al., 2022). Yet the entire population of the Bristle-thighed Curlew (Numenius tahitiensis), which nests in western Alaska, now winters on central Pacific islands, along with large numbers of Pacific Golden Plovers (Pluvialis fulva), Wandering Tattlers (Tringa incana) and other shorebirds. These islands are volcanic, so were never connected to a continental land mass. Still other species, such as the Bar-tailed Godwit (Limosa lapponica), fly from Alaska southward across the Pacific to winter quarters in New Zealand (Chapter 6). Such migration routes offer only a few scattered islands or coral atolls where birds could rest and feed. While in glacial times when sea levels were lower, the numbers and sizes of islands were probably larger than today, the hazards of a long oversea migration must always have been great, posing questions of how it could have evolved. One obvious mechanism involves progressive corner cutting. Imagine a shorebird that once migrated from Alaska across to Siberia and then down the coast of eastern Asia to winter on the coasts of Southeast Asia and Australasia. By cutting across the Pacific initially over short distances in the north, and then over progressively longer distances further south, it could gradually lengthen its oversea flights but progressively shorten its total journey, gradually abandoning previous stepping-stones and eventually resulting in a single non-stop flight. Another hypothetical scenario envisages an already long-distance population migrating mainly overland, breeding, say, in Central Siberia and wintering in South Asia. The population expanded eastward while prolonging its migration, initially via wintering sites on the Philippines, the Indonesian islands and New Guinea, Australia and eventually reaching New Zealand (Hedenstro¨m, 2010). The gradual elongation of overwater flights could also explain how migration to Pacific Islands evolved, if the islands were once stepping stones on a longer journey to Southeast Asia and Australasia, which was then foreshortened. These different hypothetical stages are shown by different species today which make overwater flights of different lengths between the same breeding and wintering areas. The suggested starting situation is still shown by stints and others that migrate from Alaska first west, then southward down the coasts of eastern Asia. Representing an intermediate stage, other species cross the northern Pacific to join the Asian coastline at some point, before proceeding southward along that coastline. At the extreme are the Bar-tailed Godwits mentioned above, which now cross the Pacific non-stop in autumn from Alaska to New Zealand (Chapter 6). Migration over other sea areas, such as the Gulf of Mexico, could have evolved in a similar way, from an initial movement around the western Gulf coast to a gradual lengthening of the overwater flight giving a reduction in the total journey length; so too could the long overwater route between northeastern North America and South America now taken in autumn by some shorebirds and songbirds. This pattern could have started as a mainly coast-hugging eastern North American flight, crossing the Caribbean Islands, and then shifted gradually eastward over the Atlantic, to give a progressively more direct (and hence shorter) overall route, but again requiring a progressively longer, non-stop overwater flight (Figure 24.5). The direct overwater flight not only cuts the distance and saves energy, but probably also reduces the risks of daytime predation from falcons and other predatory birds. All these means of evolving long-distance barrier crossing can be inferred from existing patterns of variation. They would allow gradual development of a long-distance non-stop migration system over seas or deserts, without the need

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FIGURE 24.5 Development of long oversea migrations by progressive corner cutting. By this process, the sea-crossing is gradually lengthened, but the total journey is gradually shortened. Different stages in this process (1 5) are shown today in different species and may be presumed to represent the steps through which the longest overwater journeys developed. Note that the long oversea flights off eastern North America are made mainly in autumn, with most birds taking a longer overland route in spring when winds over the sea are less favourable (Chapter 4).

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for a sudden step-change in one or more aspects of migratory behaviour. This makes it easier to understand how such long and difficult migrations might have evolved. It does not of course prove that they did evolve in this way. Long non-stop flights may have other advantages besides barrier crossing. They could shorten journey times and prevent the need for participants to stop in areas where the risks of predation, disease or food shortage could be great. They could in theory develop over continental land areas where suitable staging areas are abundant but gradually dropped from journeys, as flights are gradually lengthened. Having evolved in relatively favourable conditions, such ready-made long-distance flights could then be shifted longitudinally a bit at a time to cover long distances over adjoining sea areas, if there was an advantage in doing so. Some wader species perform non-stop flights of 5000 10,000 km from North to South America, and one might imagine some of these being shifted progressively westward over the Pacific, leading to the use of Pacific Islands as staging or wintering areas (Piersma et al., 2022). Compared to landbased flights, over-sea flights might shorten distances, offer more favourable winds and reduce the risk of in-flight predation, even though occasional storms can inflict mortality (Chapter 31).

Topographic influences There are conditions when a long roundabout migration is advantageous: an end result in itself, rather than a historical legacy or stage on the way to a more direct route. By taking a detour, birds may avoid crossing an area of unsuitable habitat, even though such a non-stop flight may seem within their capabilities. The detour may offer benefits, such as (1) reduced risk from adverse weather or predators, (2) reduced energy costs, despite the longer journey (if, for example, winds are more favourable), or (3) suitable habitat in which the birds can stop and feed, thereby saving on fuel transportation costs. From examination of a number of common detour routes taken by birds, Alerstam (2001) concluded that the saving on fuel transportation costs was probably a paramount evolutionary driver (also for loop migrations discussed later). In Eurasia, the major obstacles to migration, such as the various mountain ranges, the Asian deserts and the Mediterranean Sea, run west east, at right angles to the mainly north south migration routes. While some birds migrate over these obstacles, others migrate to one side or the other and avoid them. This gives another reason, in addition to the aforementioned glacial legacy hypothesis, for separation of autumn migration directions in Europe and elsewhere between southwest and southeast. An examination of the departure directions of central European passerines revealed that 45 species start their migration in a southwest direction, 10 in a southeast direction, while three species show funnel-shaped migration toward Italy and the central Mediterranean. In addition, 13 species show a spread of

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FIGURE 24.6 Schematic representation of initial departure directions (arrows) of central European passerine species on their way to the Mediterranean, and the number of species concerned. From left to right: southwest migration (45 species), southeast migration (10 species), both directions (13 species), between southwest and southeast 5 funnel migration into the central Mediterranean Region (3 species), clear migratory divide (16 species). From Bairlein (1985).

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FIGURE 24.7 Some well-documented loop migrations in different regions. A. Western North America, shown by various waterfowl, shorebirds and others, notably Brent Geese (Branta bernicla) and Western Sandpiper (Calidris mauri). B. Eastern North America, shown by various passerines, shorebirds and others, notably Blackpoll Warbler (Setophaga striata). C. Western Europe North Africa, shown by various passerines and others, notably Pied Flycatcher (Ficedula hypoleuca). D. Middle East North Africa, shown by various passerines and others, notably Red-backed Shrike (Lanius collurio).

directions between southwest and southeast, and 16 others show a migratory divide that separates migrants moving southwest from those moving southeast (Figure 24.6, Bairlein, 1985). A migratory divide is imposed on many North American birds by the Rocky Mountains which run roughly northsouth down the western side of the continent. Birds breeding to the west of this range migrate southward down the western side of the Americas, while those from the eastern two-thirds of the continent migrate mostly southeast, into the southeastern States, Caribbean Islands and South America. Nevertheless, because most of South America lies east of North America, most intercontinental migration occurs on a northwest southeast axis, at least for part of the route. The most obvious barriers for land-birds are provided by seas, barren deserts, icefields and sometimes mountain ranges any areas in which the species concerned could not feed or drink or would have to expend special efforts to cross. Any area could form a barrier for some species if it does not provide habitat in which individuals could rest and refuel. For example, for birds of open tundra, the boreal forest could represent a huge barrier to easy migration. In general, barriers may have at least three main long-term consequences for bird migration: (1) they may stop onward movement altogether; (2) they may lead to detours, where at one or both migration seasons the barrier is circumvented, thus lessening the risks, and providing opportunities for feeding on route; or (3) they may lead to modification of the fattening regime, ensuring that birds accumulate sufficient fuel to get across the barrier without any on-route feeding.

LOOP MIGRATIONS This term is applied to the many populations that take markedly different routes on their outward and return journeys. Loop migrations are widespread, having been described for passerines, shorebirds, raptors, seabirds and others from many different parts of the world (Figure 24.7). Some European species travel into Africa via Iberia, but return by a more central route mainly through Italy (e.g., Garden Warbler (Sylvia borin), Pied Flycatcher (Ficedula hypoleuca)),

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the whole migration following an anti-clockwise loop (spring migration east of autumn route, Gwinner & Wiltsko, 1980). Further east, Common Cuckoos (Cuculus canorus) that migrate from Europe through the Balkans into Central Africa take a more westerly route back, moving to West Africa, and then up through central Europe to their breeding areas, on a clockwise route (spring migration west of autumn route, Figure 14.2, Willemoes et al., 2014), a pattern also detected in Common Swifts (Apus apus), European Nightjars (Caprimulgus europeus) and Barn Swallows, all from the ˚ kesson et al., 2012; Norevik et al., 2017; Pancerasa et al., 2022). Yet other species travel mid-longitudes of Europe (A south over the eastern Mediterranean, and back further east mainly via Arabia on another anticlockwise loop (e.g., for Red-backed Shrike and Thrush Nightingale see Thorup et al., 2017). As to whether the route is clockwise or anticlockwise seems to depend on the distribution of suitable winds and food supplies at the time of the journey. Among Great Reed-Warblers, for example, some populations migrate clockwise while others mainly those wintering in east Africa migrate anti-clockwise (Koleˇcek et al., 2016). In eastern North America, prevailing winds north of 35 40 N blow from west to east, whereas south of 30 35 N they blow from east to west. Many species in eastern North America make their southward journey to the east of their northward journey, following a clockwise pattern. This is strikingly apparent in those species that fly over the Atlantic between northeastern North America and the Caribbean islands or northeastern South America in autumn but return in spring over the land route further west. Prevailing winds favour their southward autumn journey over the Atlantic, but would be inimical there for their northward return in spring (Chapter 4). Similarly, tracked Tree Swallows (Tachycineta bicolor) migrated directly over the Gulf of Mexico in autumn, choosing days with strong following winds, but in spring when winds were mainly unfavourable, most took the land-based route to the west, a journey three times as long but less risky (Bradley et al., 2014). The role of feeding conditions is shown, for example, in several hummingbird species of western North America which migrate up the Pacific coast in spring, taking advantage of the spring flowers on low ground, and down the Rocky Mountains in autumn when flowers are more plentiful on high ground (Phillips, 1975; Healy & Calder, 2020). On both journeys, the birds arrive in successive localities just as suitable flowers are opening to release their nectar. Another example of loop migration dependent on ground conditions in central Asia involves many different species switching seasonally between low desert routes in spring and high mountain routes in autumn (Figure 6.4). Evidence that both the outward and return routes are under genetic influence comes from the directional preferences shown by birds in captivity. For instance, captive Garden Warblers from central Europe tested in orientation cages in autumn initially showed a southwest heading, but after some days switched to southeast (Chapter 13). This change fits with their migration southwest via Iberia and then southeast into tropical Africa. In spring, by contrast, these captive birds headed directly north throughout, which fits with their normal return through Italy (Gwinner & Wiltschko, 1978, 1980). It seems that selection pressures on the outward journey can act independently of those on the return journey. But this does not exclude the possibility that some individuals could respond facultatively to conditions at the time: for example, going where the wind takes them (Chapter 15).

MIGRATION DEVELOPMENT TOWARDS HIGHER OR LOWER LATITUDES In contemplating the development of migration, two scenarios have been proposed: (1) that the breeding range is the original year-round home of a population, and the wintering range is the secondary home, visited to enhance survival through the most difficult season; or (2) that the present wintering range is the original year-round home, and the breeding range is the secondary home visited to enhance reproductive prospects (Lack, 1954; Cox, 1968; Cox, 1985; Levey & Stiles, 1992; Rappole & Tipton, 1992; Safriel, 1995; Bell, 2000; Rappole & Jones, 2002; Salewski & Bruderer, 2007). In theory, current migration patterns could have evolved from either of these starting points. But most current migration developed as birds spread from low to high latitudes at the end of the last glaciation, so range expansion and migration almost certainly developed hand in hand. This is not a question of the origin of migration, but of how past migratory patterns were modified to produce current ones. A recent example of this process was the northward expansion of the European Serin (Serinus serinus), which is resident in southern Europe, but extended its breeding range northwestward during the 19th 20th centuries, becoming increasingly migratory in the newly colonized areas (Mayr, 1926; Newton, 1972). Other examples include the Cattle Egret (Bubulcus ibis) in North America which became increasingly migratory as it spread north (Telfair, 2020). Such recent colonists show that occupation of higher latitudes can occur over a matter of decades given suitable habitat. Colonization of new breeding areas is achieved by normal dispersal processes, and migration develops secondarily in response to conditions in the newly occupied areas. Most bird populations in seasonal environments are likely to contain a mixture of migratory and non-migratory individuals, or a range of individuals with different thresholds for the

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initiation of migratory behaviour (Chapter 22; Berthold, 1999; Pulido, 2007). This inherent variation within a population provides the raw material on which natural selection can act to produce a predominantly migratory population from a predominantly resident one, or vice versa (Chapter 22). During each glaciation, as explained above, most vegetation in the two northern land masses was compressed into their southern parts by spreading ice. Subsequent re-colonization of northern regions involved a general northward movement of bird breeding ranges in line with the northward advance of suitable vegetation following ice melt. Evidence for this process derives from the expansions of bird-dispersed plants following glacial retreat, the history of which is evident from plant remains preserved in peat. Bird species that were sedentary could have remained so, or become migratory in the more northern of the areas colonized. Species that were migratory during the glaciation (wintering at lower latitudes than their breeding refuges) could have moved both their breeding and wintering areas northward, or they could have retained the same wintering areas, and simply lengthened their migrations as their breeding range spread northward. The latitude at which migration was favoured over residency is likely to have varied between species, depending on their particular food needs, but giving in each species a geographical gradient from wholly resident at the lowest latitudes, through partially migratory to wholly migratory at the highest latitudes (see Rappole & Jones (2002) for some similar proposals in the evolution of tropical-temperate zone migration). Based on climate reconstructions, climatic seasonality was still usual over wide areas at the height of the last glaciation, so bird migration may have been almost as prevalent then as now, albeit concentrated within a narrower span of latitude (Somveille et al., 2020). Some authors have proposed the development of small-scale seasonal dispersal movements (tracking locally available resources) as a precursor to range expansion and the development of migration (e.g., Levey & Stiles, 1992; Rappole, 1995). However, individuals of every studied bird species disperse to some extent, and range expansion would be expected even in the most sedentary of species, with migration developing secondarily as they spread into more seasonal environments (Bell, 2000).

Evidence from DNA studies The idea that migration developed as birds spread north from breeding areas has gained support from DNA analyses. Many species now live in areas that remained favourable during the glaciations, as well as in higher latitude areas that could have been colonized only since glacial retreat. Most that have been studied show more mitochondrial DNA variation in the refugial than in the more recently colonized areas. They are assumed to have colonized from the edge of their refugial ranges, and for this reason show less genetic variation than the source population as a whole. Examples include the Greenfinch (Chloris chloris) in Europe (Merila¨ et al., 1997) and the American Yellow Warbler (Setophago aestiva) and MacGillivray’s Warbler (Geothlypis tolmiei) in Central and North America (Klein & Brown, 1994; Mila´ et al., 2000). Similarly, in the Chipping Sparrow (Spizella passerina), genetic studies suggested that migratory populations in North America descended from sedentary populations in southern Mexico and that migration evolved as a result of a northward population expansion into temperate North America following glacial retreat from 18,000 years ago (Mila´ et al., 2006). Reductions in genetic variance with increasing latitude, assumed to result from post-glacial leading edge spread, have also been described in plants, insects and mammals on both northern continents (Hewitt, 2000). In some species, estimates have been made from mtDNA of both the dates and routes of spread. On this basis, Common Chaffinches (Fringilla coelebs) appear to have spread from North Africa into southern Europe within the last 370,000 years and spread further north through Europe only during the past 15,000 3000 years, behind the retreating ice sheets (Baker, 2002). Only the more northern populations, breeding in the most seasonal environments, have become migratory. For the Eider, study of mitochondrial DNA suggested that (1) the species survived in a single glacial refuge, (2) the current Baltic Sea population is genetically closest to a presumed ancestral population, and (3) postglacial spread progressed stepwise fashion via the North Sea region and Faeroe Islands to Iceland (Tiedemann et al., 2004). Several other widespread species examined from different parts of their deglaciated North American ranges have shown unexpectedly low levels of mitochondrial DNA differentiation, despite, in some species, high levels of phenotypic differentiation (for Red-winged Blackbird (Agelaius phoeniceus) see Ball et al., 1988; for Song Sparrow (Melospiza melodia) see Zink & Dittman, 1993; for Swamp Sparrow (Melospiza georgiana) see Greenberg et al., 1998; for Chipping Sparrow see Mila´ et al., 2006). Yet again, the implications are that large deglaciated areas were colonized by individuals from limited areas and that such species underwent morphological differentiation only after they had spread to their current range in the last 10,000 years or so. This is too short a period to expect much geographical variation in mitochondrial DNA. These species contrast with those mentioned above which are supposed to have spread from two or more different refuges because they show two or more distinct types based on divergence of mtDNA over a longer period. Examples are the Great Reed Warbler and Savi’s Warbler in Europe

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(Bensch & Hasselquist, 1999; Neto et al., 2012), and the Hermit Thrush and American Yellow Warbler in North America (Alvarado et al., 2014; Milot et al., 2000; Boulet & Gibbs, 2006). In the Hermit Thrush, the split was dated nearly a million years ago, in an earlier glacial period, but divergence may have been reinforced at later glaciations when the species was each time pushed back to southwestern and southeastern refuge areas, a pattern also expected in other species (Alvarado et al., 2014). Evidence for genetic isolation between northern migratory and southern resident populations of the same species has emerged for the Prairie Warbler (Setophaga discolor) in North America (Buerckle, 1999). Within the continent, the species is resident year-round only in mangrove habitat around the Florida coastline, while migratory Prairie Warblers breed further north over a large part of the continent. Some of these migrants also winter in Florida, where they could come into contact with the resident population. The two populations are morphologically similar but can be separated genetically, having split from one another probably in the late Pleistocene. This situation suggests how birds spreading northward to breed can become genetically isolated from their southern parent population by migration, even though the two forms overlap in wintering range. The isolation develops presumably because the two forms breed in different regions and at different times of year. This could lead in time to further genetic divergence, first to subspecific and then perhaps to specific levels. Because individuals can then reproduce only if they migrate to breed at the higher latitudes to which they have become adapted, migration can at the same time become genetically (rather than behaviourally) controlled obligate rather than facultative. The two processes leading to genetic divergence and genetic control of migration are likely to occur hand in hand (Jahn et al., 2004). Marked genetic differences were also apparent between southern sedentary and two northern migratory forms of the American Yellow Warbler, the latter having diverged and spread north in post-glacial times (Boulet & Gibbs, 2006). In summary, most current bird migration patterns probably arose in the same way, with dispersing individuals from lower latitudes spreading to higher latitudes, where they could exploit the seasonally abundant resources available for breeding, but returning by migration to lower latitudes for the non-breeding season. This view of migration systems is based on the notion that “migratory genes” persist even within essentially resident populations, allowing species continually to change in migratory habits as well as in distribution, in response to ever-changing conditions. Many highlatitude species could have continually switched from migratory to non-migratory as the glaciers ebbed and flowed, opening and closing potential breeding areas (Zink & Gardner, 2017). These ideas are concerned mainly with the modification of pre-existing movement patterns, and not with the evolution of the species themselves which could in theory have arisen at either low or high latitudes and spread from there, developing resident or migratory behaviour as conditions decreed.

Colonization of wintering from breeding areas The above discussion argues that current migration systems developed as species spread from lower to higher latitudes, becoming more migratory as they reached environments where overwintering was difficult. This situation would have affected all those species that colonized high-latitude areas after the last glaciation and is evident today in species that are still spreading north. We can imagine that the same process in reverse occurred repeatedly through the Pleistocene, when glacial conditions pushed southward. Previous resident populations would then need to become migratory to survive the colder winters, before being prevented altogether from breeding or wintering at higher latitudes by the advancing cold and surviving only at lower latitudes. As we are now in an interglacial period, the existing migration system is likely to have been established as explained above, but there are recent examples of resident species introduced to higher latitudes by human action which then developed migration to lower latitudes secondarily. One example involves the House Finch (Carpodacus mexicanus), introduced from California (where it is sedentary) to the New York area. Over 30 years, as the population expanded, the migratory habit developed, and now a large proportion of the once sedentary population migrates to winter further south, thereby acquiring new wintering areas (Able & Belthoff, 1998). The same happened in the Common Starling (Sturnus vulgaris) after birds from the resident British stock were introduced to the New York area in 1890 91. Within 60 years the species had spread over much of North America, the most northerly breeding birds having become migratory or partially migratory, with only the most southern ones remaining sedentary (Kessel, 1953; Dolbeer, 1982). Similarly, as Cattle Egrets spread north through North America, they remained resident in Florida and other southern parts but became migratory further north (Maddock & Geering, 1994). Providing that genetic instructions for migration persist in populations through both resident and migratory phases in their history, one type can develop from the other whenever distributions or conditions change. There has probably been no time when conditions were not changing somewhere in the range, and even in the height of the glaciations migration was almost certainly prevalent among bird populations in seasonal environments (Somveille et al., 2020; Thorup et al., 2021).

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DEVELOPMENT OF MIGRATION PATTERNS As a species expands from lower to higher latitudes, and birds at the expanding front become increasingly migratory, more and more individuals are likely to concentrate for the winter in the original lower latitude range. Theoretically, the resulting competition for limited resources could lead to one of four scenarios, depending on circumstances: 1. The total numbers wintering in the original range could be limited, preventing any further expansion of breeding range to higher latitudes, so that the amount of wintering habitat limits the extent of the breeding range. 2. If the winter immigrants from high latitudes are competitively superior to the original population when the two come together on their joint wintering area, the original resident population could itself develop migration to areas beyond its current range, being replaced in its breeding area each winter by the immigrants. This scenario depends on the presence of suitable wintering habitat beyond the original range and would give rise to a system of “chain migration” in which breeding populations are seasonally replaced by wintering populations of the same species. In this way, populations from successive latitudes maintain the same south north sequence in wintering areas as they do in breeding areas, but the whole series is displaced towards the equator in winter (for examples see Chapter 25). 3. If the winter immigrants were inferior in competition with the original breeding population, their numbers could be held at a low level (as in point 1 above), or they could develop an even longer migration to winter in previously unoccupied areas beyond the original range. This possibility again depends on suitable wintering habitat being available and would give rise to a system of “leapfrog migration” in which the migrant population winters beyond the area occupied by the resident population. In this way, populations of a species breeding at different latitudes reverse their sequence in winter, with those breeding furthest north wintering furthest south (or vice versa in the southern hemisphere) (for examples see Chapter 25). 4. Alternatively, if the immigrants were competitively superior, they could eliminate the original population completely. The species would then persist as a single population breeding at high latitude and wintering at low latitude, and the original breeding range would be vacant during that part of the year when the wintering population was away on its higher latitude breeding range. One way in which the migrant population could achieve competitive superiority is through the greater fecundity expected at higher latitudes. Even if the two populations then competed on equal terms on their shared wintering range, with no difference between them in average survival rates, the more fecund population (with greater average reproductive rate) would in time outbreed the other, either holding it at much lower level or eliminating it altogether in their shared range (Mills & Weir, 2007). Given these possibilities, the transition from resident to long-distance migrant emerges as a three-stage process, beginning with the origin (maintenance or re-expression) of the migratory habit, followed by the establishment of a fully migratory population, and in some cases ending with disappearance of the ancestral resident population. On the latter process, the general pattern that emerges involves a “rolling forward” of the breeding range of a species as new breeding populations are established at higher latitudes and old ones are lost at the trailing edge. This process could have been greatly facilitated by the development of productive high-latitude habitats in the wake of glacial retreat, but may also continue into periods of climatic stability (Bell, 2000). On this mechanism, improvements for breeding in one part of the range can, through winter competition, lead to retreat or extinction in another part. The implication is that were it not for the seasonal influx of migrants from higher latitudes, the same species might be resident over a wider span of latitudes. The species can winter at lower latitudes, but year-round residency is reduced or prevented there by competition for winter food supplies with conspecifics that breed at higher latitude. This consideration may help to explain why many migratory birds do not breed in their wintering areas even though conditions seem suitable there year-round. Take the Osprey (Pandion haliaetus), for example, which does not breed in the tropics and sub-tropics of South America and Africa, even though the bulk of the northern continental populations winter there, and the immatures from these populations remain there year-round. Ospreys can obviously survive through the year at low latitudes, and one likely reason they do not remain to nest there is that they can achieve greater reproductive output by migrating to nest at higher latitudes, returning for the intervening winters. In such cases, intraspecific competition for resources in low-latitude wintering areas may be a major driving force preventing additional Ospreys from becoming resident there. Shorebirds contain many high-latitude migrants. Global populations of such species may be limited by the availability of coastal food supplies in the non-breeding season (Chapters 29, 30), and as a consequence are entirely accommodated in the breeding season in the high-latitude habitats where they achieve the greatest reproductive output, taking migration losses into account. Many of these high-latitude species could probably breed at lower latitudes and be more widespread at that season if highly productive tundra habitat were not available. On this view, intra-specific competition

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on the wintering grounds could have a major role in influencing the overall population sizes, breeding distributions and migrations of birds (see Henningsson & Alerstam, 2005 for tundra-nesting shorebirds and for further discussion Chapter 25). As an apparent example of the effects of winter food supplies on breeding distributions, many seabird species, once restricted to arctic nesting areas, spread southward during the twentieth century, greatly increasing their numbers (Newton, 2003). These range expansions were in a direction opposite to that expected under global warming but could be explained by birds being originally confined to areas where they could achieve the highest fecundity, and as these areas became filled, spreading southward to establish new breeding colonies during a period of overall population growth. Examples from the Northeast Atlantic include the Northern Fulmar (Fulmarus glacialis), Northern Gannet (Sula bassana), Great Skua (Stercorarius skua), various large gull species and Common Eider. The increase and spread of most of these species have been linked to greatly increased food supplies resulting largely from the development of the fishing industry, and the resulting waste produced from the processing of fish at sea (Furness et al., 1992). Populations breeding over a wide span of latitude share a common wintering area, in which competition was probably reduced as food supplies increased. These various events illustrate how the breeding range of a migrant may be limited by competition for restricted food supplies in winter quarters. If this food supply increases and the overall population grows, birds may compete for nesting sites in the existing range, which may promote an expansion in breeding range, if necessary into lower latitude areas where breeding success may be lower than in the high-latitude range.

CONCLUDING REMARKS Many of the ideas proposed in this chapter, although based on a firm observational foundation, are necessarily speculative, but they help to explain the evolutionary and ecological background of current migration patterns. They show how complex migration patterns might have arisen step by step, each affording fitness benefits in its own right. They cannot be tested directly in the field, particularly those that depend on past changes in the nature and distribution of habitats. The results are therefore more circumstantial than the quantitative or experimental studies that support other aspects of migration research. Yet they help us to understand how some otherwise puzzling aspects of current bird migration systems might have arisen, and if we disregard them merely because they cannot be formally tested, we risk ignoring some of the most important evolutionary aspects of the subject. As human-induced global warming has progressed, many bird species have changed their distributions and migration patterns in recent decades along the same lines as deduced in earlier post-glacial times. Moreover, only 50 years ago, almost all aspects of the evolution and genetic control of bird migration were speculative, and increasingly they were confirmed or modified by experiment or by genetic studies. Already DNA analyses have helped to date and define post-glacial colonization routes, confirming that they match some current migration routes. Perhaps, therefore, in the coming years, other as yet intractable aspects of the subject will yield to scientific ingenuity or new methodology. In the study of bird migration, we are faced with two seemingly contradictory ideas: first that migration is highly labile, and second that it is highly conserved. The rapid growth in northwestward migration in Blackcaps is often used as an example of how easily migration routes can change, and the broad biogeographic patterns discussed in this chapter of how rigid and constrained many of the routes may be. This dichotomy of viewpoint can be resolved by considering what would be needed to change the status quo. Where changes involve small incremental steps, each bringing fitness benefits, they can occur rapidly, but where they involve a big change from one situation to another in which intermediate steps would be lethal, they tend not to occur, leading to long-term stability in migration routes. Most of the observed patterns of alteration in migration routes involve gradual change, in which each incremental step is itself of benefit, or at least has no large fitness cost. Patterns that seem resistant to change are those that, to be viable, would involve a marked step-change in some feature, such as migratory direction or fat deposition, while the intermediate steps could be lethal. The birds may thus be locked into some patterns simply because the step-changes in genetic control needed to break free of them are unlikely to arise by a single mutation. Some extreme journeys of today, involving long sea- or desert-crossings, can most plausibly be explained by gradual development, followed by eventual loss of the intermediate stages. Some of the strangest migration routes are likely to have developed in early post-glacial times, when many species were expanding into high-latitude regions recently freed of ice, but these routes might not persist today if the birds could make the step-changes in genetic control necessary to exploit more efficient options. The persistence of long, roundabout migration routes provide a cautionary reminder against the notion that birds invariably behave optimally (but see Alerstam, 2001). Apparent legacies of the past are clearly evident in the migration routes and divergence patterns of many birds worldwide. Selection cannot act on a clean slate but must start on a pre-existing gene pool, adapted to different (past) conditions.

Glacial legacies in bird migrations Chapter | 24

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SUMMARY Some long and indirect migration routes probably follow ancestral routes of post-glacial range expansion. Species maintain these routes to their full extent, even though, for birds breeding at the end of the colonization route, apparently suitable alternative wintering areas are available much closer. The failure of such birds to switch to new routes may be due to the difficulty of making in one step the huge changes in migratory direction and fattening regime necessary. In effect, the birds are locked into an existing genetically controlled system in which small incremental modifications may be possible, but not the big single step-change necessary to bring a fitness benefit. In those migrations in which breeding and wintering areas are now well separated, possible intermediate stages can be envisaged through which such journeys might have evolved. The same holds for chain and leapfrog migration patterns, both of which could be explained by past events. Similarly, migratory divides may mark the meeting points of two populations that re-colonized northern areas after the last glaciation, with each population spreading from a different refuge and then following on migration its ancestral colonization route. Such patterns are likely to persist only if they serve adequately in present conditions, and many take the birds around migratory barriers. Populations of a species that were judged to be isolated from one another during glacial extremes often have distinct DNA (and sometimes also distinct taxonomic status), as well as separate breeding, migration and wintering areas. Differences in the migration routes of populations separated by migratory divides promote genetic divergence between them and ultimately the reproductive isolation that can lead to speciation. Loop migration, in which birds take different routes in spring and autumn, probably occurs in response to seasonal differences in conditions, notably weather (especially wind) and food supply, which make the outward route more favourable in autumn and the return route more favourable in spring. In many species, migration is likely to have developed hand in hand with range expansion, as birds spread into higher latitude areas where they could breed, but from which it was necessary for them to return to lower latitudes to winter. This was probably the prevailing pattern as birds re-colonized high-latitude areas following each glacial retreat. It can be seen today in some species that are spreading northward within Europe or North America. Similarly, other species, introduced from low to high latitudes by human action, have changed from resident to migratory, utilizing lower latitudes in winter. The same probably happened at the start of each glaciation, when advancing cold changed resident into migratory populations, before eventually obliterating the higher latitude populations altogether. When breeding populations expand and become more migratory as they spread to ever higher latitudes, competition is likely to occur in common wintering areas. This competition could result in (1) a constraint to further growth in numbers and expansion of breeding range; (2) development of chain migration; (3) development of leapfrog migration; or (4) elimination of breeders from the original range. Which process prevails is likely to depend on circumstances, particularly the competitive relationships between breeders from different latitudes and the availability of suitable wintering habitat beyond the original breeding range.

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Telfair, R. C., II (2020). Cattle Egret (Bubulcus ibis). In S. M. Billerman). Ithaca, NY, Cornell Lab. of Ornithology, version 1.0. Thomson, A. L. (1926). Problems of bird migration. London, Houghton Mifflin. Thorup, K., Pedersen, L., da Fonseca, R. R. & Rahbek, C. (2021). Response of an Afro-Palearctic bird migrant to glaciation cycles. Proc. Natl. Acad. Sci. U.S.A. 118, e2023836118. Thorup, K., Tøttrup, A. P., Willemoes, M., Klaassen, R. H. Strandberg, R. et al. (2017). Resource tracking within and across continents in long-distance bird migrants. Sci. Adv. 3: 1 11. Tiedemann, R., Paulus, K. B. Scheer, M. et al. (2004). Mitochondrial DNA and microsatellite variation in the Eider duck (Somateria mollissima) indicate stepwise postglacial colonization of Europe and limited current long-distance dispersal. Mol. Ecol. 13: 1481 94. Toews, D. P. L., Brelsford, A. & Irwin, D. E. (2014). Isotopic variation across the Audubon’s-Myrtle Warbler hybrid zone. J. Evol. Biol. 27: 1179 91. Tonkin, S. & Gonza´lez, J. M. (2019). Ringing recovery of Yellowbrowed Warbler in Andalucia confirms overwintering in successive winters. Br. Birds 112: 686 7. Tøttrup, A. P., Pedersen, L., Onrubia, A., Klaassen, R. H. G. & Thorup, K. (2017). Migration of Red-backed Shrikes from the Iberian Peninsula: optimal or sub-optimal detour? J. Avian Biol. 48: 149 54. van Bemmelen, R. S. A., Kolbeinsson, Y., Ramos, R., Gilg, O. Alves, T. A. et al. (2019). A migratory divide among Red-necked Phalaropes in the Western Palearctic reveals contrasting migration and wintering movement strategies. Front. Ecol. Evol., 7. Available from https://doi.org/10.3389/fevo.2019.00086. Veen, T., Svedin, N., Forsman, J. T., Hjernquist, M. B. Qvarnstro¨m, A. et al. (2007). Does migration of hybrids contribute to post-zygotic isolation in flycatchers? Proc. R. Soc. B 274: 707 12.

Wenink, P. W., Baker, A. J., Ro¨sner, H.-U. & Tilanus, M. G. J. (1993). Hypervariable-control-region sequences reveal global population structuring in a long-distance migrant shorebird, the Dunlin (Calidris alpina). Proc. Natl. Acad. Sci. U.S.A. 90: 94 8. Wenink, P. W., Baker, A. J. & Tilanus, M. G. J. (1996). Global mitochondrial DNA phylogeography of Holarctic breeding Dunlins (Calidris alpina). Evolution 50: 318 30. Willemoes, M., Strandberg, R., Klaassen, R. H. G., Tøttrup, A. P. Vardanis, Y. et al. (2014). Narrow-front loop migration in a population of the Common Cuckoo Cuculus canorus, as revealed by satellite telemetry. PLOS ONE 9 (1): e83515. Yohannes, E., Lee, R. W., Jochimsen, M. C. & Hansson, B. (2011). Stable isotope ratios in winter-grown feathers of Great Reed Warblers Acrocephalus arundaceus, Clamorous Reed Warblers A. stentoreus and their hybrids in a sympatric breeding population in Kazakhstan. Ibis 153: 502 8. ˚ kesson, S. (2010). Autumn orientation Zehtindjiev, P., Ilieva, M. & A behaviour of Paddyfield Warblers, Acrocephalus agricola, from a recently expanded breeding range on the western Black Sea coast. Behav. Process. 85: 167 71. Zink, R. M. (1994). The geography of mitochondrial DNA variation, population structure, hybridisation, and species limits in the Fox Sparrow (Passerella iliaca). Evolution 48: 96 111. Zink, R. M. & Dittman, D. L. (1993). Population structure and gene flow in the Chipping Sparrow (Spizella passerina) and a hypothesis for evolution in the genus Spizella. Wilson Bull 105: 399 413. Zink, R. M. & Gardner, A. S. (2017). Glaciation as a migratory switch. Sci. Adv. 3 (9): e1603133. Zink, R. M., Pavlova, A., Drovetski, S. & Rohwer, S. (2008). Mitochondrial phylogeographies of five widespread Eurasian bird species. J. Ornithol. 149: 399 413.

Chapter 25

Distribution patterns and connectivity

Bar-tailed Godwits (Limosa lapponica), known for long-distance migrations, with few refuelling stops With increasing knowledge as to the winter distribution of species, and more especially subspecies of migratory birds, it becomes possible to determine more precisely the relationship between the summer-quarters and the winter-quarters of particular forms: this is a line of enquiry that is usefully supplemented by records of individual marked birds, and one that may throw interesting light upon the evolutionary origin of migrations. A. Landsborough Thomson (1936).

Migration leads to marked changes in the distribution of birds during the course of each year. Within each species, birds from different parts of the breeding range segregate during the winter in various longitudinal and latitudinal patterns. This raises questions about how these different patterns of winter distribution arise and persist and what effects they might have on the genetic structure and dynamics of populations. Competition is often held to influence the distributions of wintering populations with respect to one another, but other factors such as habitat and migration costs are also involved. An important question concerns the extent to which individuals from the same breeding area migrate to the same nonbreeding area as one another, and vice versa. Years ago, Salomonsen (1955) used the term alloheimy for populations that live in different wintering areas, and synheimy for those that co-exist in the same wintering area. In reality, these categories represent the extremes in a continuum of variation from total separation to total overlap. The degree of year-round separation between breeding populations is nowadays expressed by measures of ‘connectivity’, which reflect the degree to which birds from different parts of the breeding range also occupy different parts of the wintering range (see later).

LONGITUDINAL PATTERNS In many bird species, individuals that breed furthest west in the breeding range tend to winter furthest west in the nonbreeding range, and those that breed furthest east also winter furthest east (Figure 25.1). Allowing for the uneven The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00009-9 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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FIGURE 25.1 Examples of parallel migration among west Palaearctic breeding birds, from ring recoveries. (a) Common Chaffinches (Fringilla coelebs) ringed at the Courland Spit, Russia (filled square, filled dots) and at the Col de Bretolet, Switzerland (open square, open dots). (b) Common House Martins (Delichon urbica) from Europe to Africa. (a) Redrawn from Bairlein (1998). (b) From Hill (1997).

distribution of land masses, this pattern holds in both Old and New Worlds, reflecting the more or less parallel migrations of populations. Such patterns have been revealed by ring recoveries from most groups of birds, and more recently confirmed for some species by tracking studies or on wider spatial scale by stable isotope or DNA analyses (for Dunlin (Calidris alpina), see Wenink et al., 1996; Wennerberg, 2001; for Swainson’s Thrush (Catharus ustulatus), see Ruegg & Smith, 2002; for Wilson’s Warbler (Wilsonia pusilla), see Clegg et al., 2003; Paxton et al., 2007; for Loggerhead Shrike (Lanius ludovicianus), see Chabot et al., 2012; for Common Nightingale (Luscinia megarhynchos), see Hahn et al., 2013; for Wood Thrush (Hylocichla mustelina), see Stanley et al., 2014; for Montagu’s Harrier (Circus pygargus), see Trierweiler et al., 2014). In addition, 23 species of passerines and near-passerines tracked on migration between Europe and Africa showed evidence of parallel migrations, with significant correlations between the longitudes of breeding and wintering areas (Briedis et al., 2020). But despite these broadly parallel migrations, there can still be considerable longitudinal overlap in winter between birds from different breeding areas (see below). Based mainly on findings from waterfowl, Lincoln (1935) proposed that migratory birds in North America followed four main flyways: the Pacific, Central, Mississippi and Atlantic Flyways. This division soon came to form the political basis for waterfowl management and hunting throughout the continent. For the most part, it reflected biological reality, because of the more or less parallel migrations of different populations. The system was further developed by Bellrose (1968) who used radar surveillance and ringing records of waterfowl to describe the presence of migration corridors within the flyways. He defined a corridor as a narrow strip of airspace used by waterfowl as they migrated between their breeding and wintering grounds. In some places, the corridors were little more than 16 km wide, in others more than 200 km, depending on local topography and landscape. Such more-or-less parallel migrations need not necessarily involve competition, as sometimes assumed, for they could be explained by the birds from different segments of the breeding range taking the shortest routes between their breeding and wintering areas. Other factors being equal, any birds that deviate from the parallel pattern and cross the routes of other populations, are likely to lengthen their journeys, and thus have greater migration costs. In practice,

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however, the shapes of the main land masses can greatly distort these potentially parallel migration patterns, ensuring that most do not run directly north-south. The migration corridors of some species are narrow over almost the whole route, as in some cranes, geese and shorebirds that travel between traditional widely spaced stopover and wintering sites. For example, Whooping Cranes (Grus americana) from their small breeding area in northern Canada migrate along a narrow corridor directly to their only wintering site at Aransas on the Texas coast and then back along the same route (Kuyt, 1992, Figure 25.2). In some species of geese, different populations remain separated year-round as they move from different breeding localities, along different flyways to their own traditional wintering areas (Figure 25.3). Similarly, many shorebirds tend to travel along coastlines which provide potential stopping sites, if needed. This situation of narrow separated routes is no different in principle from the parallel but broad-front migration of most widespread species, except that the different breeding or wintering areas are highly localized, well separated and easily recognized. The different populations (or subspecies) of many widespread species also remain separated year-round. An example is the Red Knot (Calidris canutus), which breeds at high arctic latitudes throughout the world and performs long and complex migrations to reach wintering areas that extend from northern temperate to southern temperate regions. The population associated with each breeding area migrates to a discrete wintering area, although some populations may come together for a time on migration (Figure 25.4). For example, the subspecies islandica from Iceland and canutus from Siberia occur together in the Wadden Sea in western Europe, the former wintering there and the latter staging on migration and then moving on to West Africa. Although the migrations of Red Knots and other shorebirds are far from parallel, they still result in birds maintaining the same west-east distributional sequence on both breeding and wintering areas. In contrast to this pattern is fan (or funnel) migration, in which birds from a small part of the breeding range can spread out across a wide part of the wintering range where they can intermix with birds from other parts of the breeding range (Figure 25.5). This also results in birds from a small part of the wintering range spreading out to breed over a wide part of the breeding range. There is no clear dividing line between parallel and fan migration because different species reveal a continuum of variation between these extremes, depending partly on geography. And in populations showing fan migration individuals can still show correlations between the longitudes of their breeding and wintering FIGURE 25.2 Autumn and spring migration corridors of Whooping Cranes (Grus americana), as defined by VHF radiotracking, between their sole breeding area in Canada and their sole wintering area at Aransas, on the Texas coast. The corridor extended for about 4000 km and varied in width between 80 and 300 km. The map is a Mercator projection. Redrawn from Kuyt (1992) and Alerstam (1996).

Y

FIGURE 25.3 Breeding areas, migration routes and wintering areas of three populations of Barnacle Geese (Branta leucopsis) and two populations of Pink-footed Geese (Anser brachyrhynchus). Black shading depicts the separate breeding and wintering areas, grey the migration routes, and white spots the main stopover sites. Based on Madsen et al. (1999).

islandica rogersi

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FIGURE 25.4 Year-round separation of different subspecies of Red Knots (Calidris canutus). These birds breed only on high arctic tundra (65 83 N), different subspecies in different regions, and winter on coastlines between latitudes 58 N and 53 S. Due to their specialized sensory capabilities, Red Knots generally eat hard-shelled prey found by probing into intertidal substrates. Ecologically suitable coastal sites are few and far between, so these birds must routinely undertake flights of several thousands of kilometres. Black breeding areas; grey wintering areas; blue lines approximate migration routes. This example, along with many other shorebirds, geese and others, indicates how populations maintain their distinctive distributions year-round. Modified from Conklin et al. (2022).

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FIGURE 25.5 Fan migration as illustrated by Peregrine Falcons (Falco peregrinus) trapped and attached with satellite tags during winter on the Gulf Coast of Mexico (north of Tampico) and subsequently tracked to breeding areas across the Arctic. Lines connect the winter trapping site with the subsequent breeding sites but do not necessarily depict the routes flown. From McGrady et al. (2002).

localities. Striking examples of fan migration, in which birds from a wide breeding range are funnelled into a small wintering range, are shown by the Lesser Grey Shrike (Lanius minor) and Eleonora’s Falcon (Falco eleonorae) in the Old World or by the Prothonotary Warbler (Protonotaria citrea) in the New World (Figure 25.6; Newton, 1995; Mellone, 2021; Tonra et al., 2019). In addition, many raptors and other soaring species become funnelled during migration through points with narrow land bridges (such as Panama) or short sea-crossings (such as Gibraltar) (Chapter 7). Their various migration routes are shaped like an hourglass, constrained in the middle. This leads to mixing on these migration routes of birds from widely separated parts of the breeding range, as evident from both ringing and tracking studies (Chapter 7). Some striking examples of fan migration have been uncovered in recent years in which individuals from small study areas spanning less than one kilometre across can be found scattered over wide areas spanning thousands of kilometres across, intermixed with individuals from other parts of the breeding range. To give some extreme examples, 15 Willow Warblers (Phylloscopus trochilus) from a 0.5 km area in Denmark were fitted with geolocators and followed to their wintering areas which were spread over more than 3000 km of longitude across the width of Africa, in each area presumably mixing with Willow Warblers from other parts of the breeding range (Lerche-Jørgensen et al., 2017). Similarly, 18 adult male Great Reed Warblers (Acrocephalus arundinaceus) breeding around a single lake in Sweden were spread across more than 3300 km of West Africa during the non-breeding season (Lemke et al., 2013); seven adult Common Redstarts (Phoenicurus phoenicurus) from a 30 ha wood in eastern Denmark were spread across nearly 2000 km in West Africa (Kristensen et al., 2013); and twelve Northern Wheatears (Oenanthe oenanthe) from a study area in Sweden were spread over 2000 km in West Africa (Arlt et al., 2015). An even more extreme fan migration was found in Little Ringed Plovers (Charadrius dubius), 23 individuals of which were tracked from the same small breeding site in southern Sweden to wintering sites extending from West Africa through the Middle East to India, giving a spread of more than 7000 km between extreme western and eastern wintering sites, and large differences in the migration distances of individuals (Hedenstro¨m et al., 2013). In some species, even breeding partners tracked by satellite wintered in areas separated by more than 1000 km, as shown in Ospreys (Pandion haliaetus), Greater Spotted Eagles (Clanga clanga), Sabine’s Gulls (Xema sabini) and others (Chapter 8; Kjelle´n et al., 1997; Meyburg et al., 1998a,b; Stenhouse et al., 2012). Similarly, individuals found at any one wintering site would be expected to derive from a wide range of breeding localities and show fan migration on their return journey (for Peregrines (Falco peregrinus), see Figure 25.5; for Wood Thrushes, see McKinnon et al., 2014a,b). As well as west-east spread, some populations also show wide north-south

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FIGURE 25.6 Fan migration route of Eleonoras Falcons (Falco eleonorae) which breed across the width of the Mediterranean and concentrate to winter mainly in northern Madagascar. Spots mark nesting colonies. Compiled from Mellone (2021).

spread in wintering areas, with different individuals from the same breeding areas spread over up to several thousand km of latitude, as explained below. Other extreme examples of widely spread wintering areas include various irruptive migrants in which birds found in any one breeding area can migrate to widely separated wintering places, and birds wintering on any one area can have come from widely separated breeding places (Chapters 20, 21). For example, Bramblings (Fringilla montifringilla) ringed in winter in Switzerland have been recovered over a wide expanse of boreal breeding range from Scandinavia to central Siberia, an east-west spread of about 2000 km and 50 degrees of longitude (Jenni, 2021). Some of the longitudinal spread in the wintering localities of birds from the same breeding area may be due to variation in their inherited migration directions, and further variation may be due to stochastic factors, such as the effects of sidewinds, especially among juveniles which on their first migration have no precise goal (in the way that adults may be returning to specific territories used in previous years). For example, among European Honey Buzzards (Pernis apivorus), 31 juveniles tracked from places spread over 118 km in southern Finland gradually diverged on migration so that by the time they reached tropical Africa, cumulative wind drift had dispersed them over a longitudinal front extending over 3340 km (Vansteelant et al., 2017). In contrast to juveniles, adults headed to specific areas known from previous years (Chapter 19; Cresswell, 2014). Evidently, the routes and non-breeding sites used by adults resulted partly from the way that wind and other conditions had shaped their first journeys.

Parallel or fan patterns What are the factors that promote fan migration as opposed to parallel migration? One obvious influence is the shapes of the major land masses, which could require compression of routes on one direction and their expansion on return (as in the autumn and spring movements between North and Central America). The second is the spatial distribution of suitable habitat, which could be sufficiently patchy as to preclude the possibility of parallel migration, and require some degree of fan migration. This situation is exemplified by shorebirds which breed across the tundra but concentrate to winter on highly localized coastal mudflats. Third, strictly parallel migrations could be fatal for species which depend on sporadic food supplies, available in some areas one year and in other areas the next, such as the boreal finches which exploit tree-mast crops (Chapter 20), or the Eurasian migrants which winter in the drier parts of Africa where variable rainfall patterns result in changing patterns of food availability from year to year (Chapter 26).

LATITUDINAL PATTERNS The north-south distribution of populations in the non-breeding season is more complicated than their west-east distributions, and in the Northern Hemisphere, three main patterns are found (Figure 25.7). In so-called chain migration,

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FIGURE 25.7 Three common patterns of latitudinal replacements in the migrations of various bird species: (a) chain migration in which populations occur in winter in the same latitudinal sequence as on their breeding areas; (b) leapfrog migration in which populations occur in winter in reverse latitudinal sequence as on their breeding areas; (c) telescopic migration, in which populations from different breeding areas occur together in the same wintering area. Partly from Salomonsen (1955).

(b)

(a)

(c)

populations maintain the same north-south sequence in both breeding and wintering areas, so that birds that breed furthest north in the breeding range also winter furthest north in the wintering range, while birds that breed furthest south also winter furthest south. The more northern (usually larger) birds sometimes replace others as they move south, so that the same areas are occupied year-round, but by one population in summer and another in winter. For example, in the Common Redshank (Tringa tetanus) Icelandic birds move to Scotland and the North Sea area, while the local breeding birds move further south (Cramp & Simmons, 1983). Other examples of chain migration are provided by ring recoveries of the European Goldfinch (Carduelis carduelis), Linnet (Linaria cannabina), White Wagtail (Motacilla alba), Eurasian Sparrowhawk (Accipiter nisus), Tufted Duck (Aythya fuligula) and Common Gull (Larus canus) from different parts of Europe (Salomonsen, 1955; Kilpi & Saurola, 1985; Siriwardena & Wernham, 2002), and of the American Coot (Fulica americana), Sharp-shinned Hawk (Accipiter striatus) and others from different parts of North America (Phillips, 1951; Ryder, 1963; Smith et al., 2003; Stanley et al., 2014). Further examples of chain migration have been established by stable isotope analyses (for American Redstart (Setophaga ruticilla), see Norris et al., 2006) and by tracking studies (for Northern Gannet (Morus basanus), see Fort et al., 2012; for Common Swift (Apus apus), ˚ kesson et al., 2020). see A In the second latitudinal pattern, called leapfrog migration, birds that breed furthest north in the northern hemisphere winter furthest south, reversing their latitudinal sequence between summer and winter (Chapter 24). This pattern is found commonly within various species of passerines, raptors, waders, waterfowl, gulls and other seabirds (Salomonsen, 1955; Moreau, 1972; Kilpi & Saurola, 1985; Boland, 1990; Ramos et al., 2015; Wernham et al., 2002; Hallgrimsson et al., 2012; Panuccio et al., 2021; Nilsson et al., 2022). Well-known examples include the Fox Sparrow (Passerella iliaca), west of the Rockies in North America (Swarth, 1920; Bell, 1997) and the Common Ringed Plover (Charadrius hiaticula) in Europe (Salomonsen, 1955; Figure 25.8). In all these examples, leapfrog patterns were established by ringing, but in recent years, similar patterns have emerged through stable isotope analyses (for Wilson’s Warbler, see Clegg et al., 2003; Paxton et al., 2007; for MacGillivray’s Warbler (Geothlypis tolmiei), see Paxton & van Riper, 2006), and through tracking studies (for Golden Eagle (Aquila chrysaetos) in eastern North America, see Nelson et al., 2015). In the third latitudinal pattern, termed telescopic migration, populations that breed over a wide span of latitude become telescoped in the non-breeding season into a narrower span, so that birds from different breeding latitudes intermix in winter. Populations that are allopatric in summer thus become sympatric (or ‘synheimic’) in winter (although they may still show west-east separation through parallel migrations). In the Palaearctic-Afrotropical migration system, Savi’s Warblers (Locustella luscinioides) occupy a wintering range only one-seventh of the latitudinal span of the breeding range (Moreau, 1972). Similar patterns are also shown by Common Grackles (Quiscalus quiscula) and Common Starlings (Sturnus vulgaris) in eastern North America (Dolbeer, 1982; Figure 25.9), by Rosy Finchesm, Leucosticte atrata, Leucosticte tephrocotis tephrocotis and Leucosticte tephrocotis littoralis in western North America (King & Wales, 1964), by several races of Yellow Wagtails (Motacilla flava) in parts of Africa (Salomonsen, 1955; Curry-Lindahl, 1958; Cramp, 1988), and by various races of some Nearctic Neotropical migrant species in parts of Mexico (Rappole & Warner, 1980). In many other species, in both Old and New Worlds, northern migratory races winter within the range of more southern resident ones. Telescopic migration also applies to migration from wintering to breeding areas, as populations wintering over a wide north-south span of latitudes become concentrated for breeding within a narrower span. Some shorebird species, such as Grey Plover (Pluvialis squatarola) and Sanderling (Calidris alba), occupy coastal sites scattered over much of

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FIGURE 25.8 Leapfrog migration in: (a) Fox Sparrow (Passerella iliaca) and (b) Common Ringed Plover (Charadrius hiaticula). Re-drawn from Swarth (1920) and Salomonsen (1955).

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Common Grackle Starling

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FIGURE 25.9 Mean distance ( 6 SE) from ringing to recovery sites for adult Common Grackles (Quiscalus quiscula) (N 5 855) and Common Starlings (Sturnus vulgaris) (N 5 1116), illustrating telescopic migration in two species ringed on their breeding areas in eastern North America (75 100 longitude), and recovered in winter (January February) further south, in a narrower span of latitude. In both species, birds from more northern breeding areas travelled further, on average, but wintered in the same latitudinal band as birds from more southern breeding areas. Redrawn from Dolbeer (1982).

0 32–33 34–35 36–37 38–39 40–41 42–43 44–45 46–47 Latitude of ringing site

the world in the northern winter, but withdraw to breed within a relatively narrow span of arctic tundra. Similarly, Eurasian Stone-curlews (Burhinus oedicnemus) and Western Marsh Harriers (Circus aeruginosus) wintering over a wide area from southern Britain to sub-Saharan Africa can be found breeding together in southern Britain in summer (Wernham et al., 2002). In chain migration, the distances may be more or less similar among populations, even though these populations migrate between different areas, but in the other two latitudinal patterns, the high-latitude breeding populations migrate

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furthest, with the greatest population differences occurring in leapfrog migrants. It is impossible to say from the data available how common these different patterns of latitudinal segregation are among migrants, or whether they differ in frequency between regions. These questions could most readily be answered, at least for Europe, by comprehensive analyses of existing ring recoveries, which are yet to be done.

EVOLUTION OF ALLOHEIMY Whatever the pattern of geographical segregation among wintering migrants, if such differences are genetically influenced through migratory behaviour, it is not hard to envisage how they might have come about (Figure 25.10). Imagine that populations which breed in separate areas come together on a common wintering area. If the numbers that this wintering area could support were limited (say by food supplies), and individuals of one population were better adapted to that area, they would in time be expected via competition to replace individuals of the other population completely, either eliminating them or leading them to winter elsewhere. This latter situation would occur if individuals started to winter outside the original range and were then favoured by natural selection over those that remained in the original range. The wintering areas of the two populations would then become separated. As a second scenario, imagine that in a joint wintering area, birds from separate breeding populations competed on equal terms for food or some other scarce resource, with the same proportion of each population surviving the winter. If individuals of one population had, on average, a consistently higher reproductive rate than the other, then in time one population would be expected to replace the other completely in their shared wintering area, again either eliminating birds from that population or forcing them to winter elsewhere (Chapter 24). This is a way in which a sedentary population could become migratory, under pressure of competition from individuals of another population increasingly wintering in the same area (Sutherland & Dolman, 1994; Bell, 2000). Likewise, imagine that birds in a given breeding area, where their numbers were limited, divided between two wintering areas. If the birds with a genetic predisposition to go to one wintering area survived consistently better than the birds visiting the other area, the first group would eventually replace the second completely. In these ways, competition could act as a selective force behind a genetic change in migratory habits, leading ultimately to year-round geographical segregation of populations. In these times of environmental change, we can expect that some populations are now in the process of changing their distributions with respect to one another. Whether the development of alloheimy leads to chain or leapfrog patterns could depend on the competitive relationships between individuals from the different populations, as explained in Chapter 24 (Cox, 1968; Holmgren & Lundberg, 1993; Bell, 2000). If individuals in a higher latitude population settling in a wintering area were competitively superior to the individuals of the same species resident there, the immigrants could either eliminate the residents, or force them to become migratory, moving to lower latitudes for the non-breeding season, and thus setting up a system of chain migration (Bell, 2000). If, on the other hand, the northern birds were inferior in competition with the more southern residents, the northern ones would benefit from moving to yet lower latitudes beyond the breeding range, thus becoming leapfrog migrants. Hence, whether one or other system developed over time could depend on the past competitive relationships between individuals from the different populations. This raises the question of how synheimy could persist, with populations from different breeding areas wintering together in the same area and depending on the same foods. One way would be if they were each limited in numbers on A

B

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FIGURE 25.10 Migration of three neighbouring populations (A, B and C) showing (A) synheimy (complete sharing of wintering areas, weak connectivity), (C) alloheimy (complete separation of wintering areas, strong connectivity) and (B) an intermediate situation (partial separation of wintering areas, moderate connectivity). The upper rectangles indicate breeding areas, the lower rectangles indicate wintering areas, and the arrows indicate the scattering of migrants from each breeding area. A gradual change from pattern 1 to 3 could come from selection resulting from competition between individuals from different breeding populations or from selection to reduce migration distances, eventually giving rise to ‘parallel migration’ (see text). Pattern 1 could be maintained or developed in species that utilize sporadic habitats or food supplies, whose distribution within the winter range varies markedly from year to year (as for some irruptive migrants, Chapters 20 and 21). To judge from ring recoveries and tracking studies, the intermediate situation (2) is the most common. From Salomonsen (1955).

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their breeding areas, so that collectively, they did not reach the limit of their shared wintering space and hence did not compete seriously for resources there. Another way would be if they were limited either in breeding or wintering areas by factors other than resources, say by predators or parasites, which held the populations below the level at which serious competition for food occurred. A third way in which synheimy could persist is if the different populations differed in their ecology, reducing any potential competition between them. For example, in many areas, resident populations of some species stay near their breeding places year-round, eating whatever foods are available there, while winter visitors of the same species from elsewhere move around from place to place, exploiting temporary abundances of food such as fruit crops or insect outbreaks (for Eurasian species in Africa, see Chapter 26). In this case, the survival of both residents and migrants in the same area depends on the mobility of the migrants, and their ability to seek out locally abundant food supplies which are often greater than the local residents can consume themselves. Resident and migratory populations may also differ in habitat use, as found among Eurasian Blackcaps (Sylvia atricapilla) and European Robins (Erithacus rubecula) wintering in Spain (Pe´rez-Tris & Tellerı´a, 2002; Tellerı´a & Pe´rez-Tris, 2004). Fourth, synheimy of different breeding populations may also persist in species whose habitats and food supplies are sporadically distributed, changing in the location from year to year. This situation exists for seed-eating boreal finches, vole-eating raptors and owls and many freshwater ducks (Chapters 20 and 21). It leads individuals to move around, within and between winters, and prevents their developing strong winter site-fidelity, which underpins the evolution of alloheimy. Competitive superiority of one wintering population over another could arise in a number of different ways: the individuals in one population may be larger, and hence dominant in aggressive interactions or better able to resist cold; they may gain the benefits of prior occupancy if they are already established when individuals of the second population arrive; or they may differ in morphology and behaviour in a way that enables them to more efficiently exploit local food supplies or avoid predators and parasites. Alternatively, they may, in their particular breeding range, be able to achieve a higher mean reproductive rate, and simply ‘outbreed’ the other population, gradually replacing it in their common wintering range where overall numbers are limited. This latter situation has been explored in a demographic model for a migratory shorebird, the Eurasian Oystercatcher (Haematopus ostralegus), in which different breeding populations shared the same wintering area. Initially, as winter habitat was progressively removed in simulations, all populations decreased in parallel. However, as habitat loss continued, the populations with lower fledgling production began to be affected most (Goss-Custard et al., 1995; for wider application of this model, see Mills & Weir, 2007). These various considerations suggest that intraspecific competition could be a driving force behind geographical segregation patterns among migratory bird populations, at least for latitudinal segregation. For longitudinal segregation, minimization of flight costs could also have a major influence. Various mathematical models have been devised to explore these patterns further. They indicate that such factors as latitudinal gradients in habitat suitability, migration costs and annual time or energy budgets could all add to competition as potential selective forces behind different patterns of geographical segregation, including chain, leapfrog and overlap patterns (Cox, 1968; Greenberg, 1980; Lundberg & Alerstam, 1986; Holmgren & Lundberg, 1993; Bell, 1997, 2000; Mills & Weir, 2007). We have no way of judging which selective forces are likely to have applied in particular cases, although the possible role of energy budgets is discussed below.

NONBREEDING DISTRIBUTIONS AMONG SEABIRDS Seabirds which stay close to shorelines tend to show similar patterns in their winter distributions to landbirds, as shown by the examples mentioned above. However, pelagic species are generally much more mobile and dispersive than are either other seabirds or land-birds; they range over larger areas, and birds from different breeding areas show greater potential for mixing in wintering areas. Moreover, it is only in recent years, following the development of tracking technology, that information on pelagic species has become available, revealing some intriguing patterns. At one extreme, Black-browed Albatrosses (Thalassarche melanophris) from different nesting places showed largely mutually exclusive foraging ranges, each being used by the birds from a particular island group, both in breeding and non-breeding periods (BirdLife International, 2004). Some level of segregation of breeding populations in wintering areas was also found among Great Skuas (Catharacta skua), Atlantic Puffins (Fratercula arctica), Common Murres (Uria aalge) and Thick-billed Murres (Uria lomvia) in the North Atlantic (Magnusdottir et al., 2012; Fayet et al., 2017; Merkel et al., 2021). Nevertheless, birds from more widely separated nesting colonies tended to occur in more widely separated wintering areas. Some pelagic species are, of course, sub-divided in distributions by the continental land masses. Thus many species that breed around the Southern Ocean or Antarctica migrate northward for the winter, becoming segregated by the southern continents into Pacific, Atlantic and Indian Ocean wintering areas. Tracked Sooty Shearwaters (Ardenna grisea) breeding on islands off New Zealand headed to the North Pacific after breeding, while their Falklands

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counterparts headed to the North Atlantic (Figure 8.2; Shaffer et al., 2006; Hedd et al., 2012). Similarly, two distant populations of South Polar Skuas (Stercorarius maccormicki) breeding on the Antarctic continent migrated northward to winter in the tropical Indian Ocean and temperate North Pacific, respectively (Weimerskirch et al., 2015a,b). Interestingly, those skuas from nesting colonies lying due south of the tip of South America split, with some individuals migrating to the North Pacific and others to the North Atlantic, each following the same route in successive years (Kopp et al., 2011). Within each major ocean, widely separated nesting populations of other species mingled to a large extent in a common wintering area, as exemplified by the Black-legged Kittiwake (Rissa tridactyla) in the North Atlantic and the Slender-billed Prion (Pachyptila belcheri) in the Southern Ocean (Frederiksen et al., 2012; Quillfeldt et al., 2015). In one large-scale study, tracking devices were fixed on Black-legged Kittiwakes nesting in a range of colonies on both sides of the North Atlantic, spanning almost the entire breeding range of the species (Frederiksen et al., 2012). Some 236 devices were retrieved and provided data. Using these data, it was estimated that 80% of the 4.5 million adult Kittiwakes in the North Atlantic wintered in the western half, between Newfoundland and the Mid-Atlantic Ridge, mostly over deep-water areas. In other words, birds from a wide breeding range wintered in this same general area. Only some birds nesting in Ireland and western Britain wintered east of this Ridge, nearer to Europe. In general, it seems that wintering seabird populations show a similar range of distributional differences and overlaps as wintering landbirds, but intermixing of birds from different parts of the breeding range in winter quarters seems more common among pelagic species than among inshore species.

CONNECTIVITY From a breeding area perspective, connectivity can be defined as the amount of overlap (and intermixing) in wintering locations that occurs between individuals from geographically separated breeding areas (Webster et al., 2002; Boulet & Norris, 2006). It gives a measure of the extent to which individuals remain associated between seasons and, therefore, of the extent to which they are exposed to the same environmental conditions and selection pressures as one another year-round (Webster et al., 2002). Migratory populations from different breeding areas that are separated year-round through also having discrete migration and wintering areas (such as the geese in Figure 25.3) are said to show strong connectivity (with little or no mixing between birds from different breeding populations). In contrast, birds from different breeding populations that come together and intermix in a shared wintering area are said to show weak connectivity. In this case, individuals from the same breeding area do not all occupy the same wintering area as one another, so they are exposed to different environmental conditions and selection pressures. These examples represent the ends of a range of variation between populations, which differ in the extent to which their winter distributions overlap. In general, parallel migration systems would be expected to produce greater connectivity than fan and telescopic systems which produce more mixing. For ring recoveries to provide information on migratory connectivity, they should ideally be obtained from multiple breeding and wintering localities, enabling the degree of overlap between birds from different breeding areas in their wintering range to be assessed. For many species, hundreds or thousands of useable ring recoveries are available, while for others, none at all, but the main problem is that recovery and reporting chances may vary across the wintering range, giving a biased picture of seasonal distributions. However, birds tracked by geolocators or satellite tags from either breeding or wintering areas do not suffer from this type of geographical bias, because they are not dependent on reporting rates. But so far, relatively few species have been tagged in sufficient numbers over a broad enough geographical scale to give representative results. At their best, ring recoveries and tracking methods can reveal connectivity on a fine scale, with bird locations being obtained with an accuracy to within metres or hundreds of metres for ringing and GPS studies, and within 100 200 km for geolocator studies. Measures of connectivity based on stable isotope analyses of feathers grown at sites of interest (Hobson & Wassenaar, 1997; Marra et al., 1998; Rubenstein et al., 2002), on genetic markers, such as microsatellites and mitochondrial DNA (Wennerberg, 2001), on combinations of these techniques, give broader-scale estimates of potential breeding or wintering areas (Chabot et al., 2012; Clegg et al., 2003). Other researchers have combined the findings from broad-scale and more precise methods to define the potential breeding or wintering areas of particular populations (Boulet et al., 2006; Macdonald et al., 2012; Hobson & Kardynal, 2016; McKinnon & Love, 2018). Some recent large-scale studies have focused on the role of connectivity in influencing demography and population trends across a breeding range. Birds using certain parts of the wintering range, where feeding conditions were good, showed consistently better survival or breeding success than birds using other parts of the wintering range (for Blacktailed Godwit (Limosa limosa), see Alves et al., 2013, for European Shag (Gulosus aristotelis), see Grist et al., 2017, for Atlantic Puffin, see Fayet et al., 2017). Birds wintering in the best areas often arrived in breeding areas and started

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nesting earlier than birds from other areas. Such studies showed that a bird’s wintering locality could influence its subsequent performance, sometimes leading to differences in population trends between areas (Fayet et al., 2017; Merkel et al., 2021). Conversely, thorough mixing in a common wintering area has resulted in birds from different breeding areas showing the same year-to-year fluctuations in survival, and sometimes also in breeding success (for examples from seabirds, see Strøm et al., 2021). Migratory connectivity has two components: ‘population spread’ describes the degree to which individuals from a single breeding area spread out in winter, while ‘inter-population mixing’ describes the degree to which individuals from different breeding areas mix together in winter. Generally speaking, high population spread in wintering areas will promote inter-population mixing (‘weak’ connectivity), while low population spread will reduce mixing (‘strong’ connectivity). However, the relationship between population spread and inter-population mixing is likely also to depend on geography by the relative extents and positions of the breeding and non-breeding ranges. Intermixing is important because it influences the degree to which the populations from different breeding areas are demographically isolated from one another. In populations with strong connectivity, events on particular segments of the wintering range are likely to affect only the particular breeding populations using these areas. However, in populations with weak connectivity, events on particular segments of the wintering range are likely to affect individuals from a much larger part of the breeding range. Whatever their severity, such effects are likely to dilute over a wide part of the breeding range so that they may be barely apparent in any one limited breeding area. There are also practical reasons for assessing the links between populations, notably to facilitate effective conservation measures and to better understand disease transmission. One method of quantifying connectivity involves measuring the distances between the same birds in both their breeding and non-breeding areas and then calculating the correlation coefficient between the values from the two seasons. This tells us whether individuals which are furthest apart in breeding areas are also furthest apart in wintering areas. Based on such distance estimates, Mantel’s correlation coefficient (rM)1 provides useful measures, varying between 21 (no connectivity) to 11 (total connectivity). An early estimate was based on the ringing and recovery sites of Barn Swallows from much of Europe, which gave a very low rM value of ,0.03, indicating very low connectivity. Estimates for other species were based on tracking (mainly geolocator) studies of birds from more restricted areas. Among European species, they gave generally higher estimates of 0.25 for European Nightjars (Caprimulgus europaeus) (Norevik et al., 2019a,b), 0.56 for Montagu’s Harriers (Trierweiler et al., 2014) and 0.58 for Lesser Kestrels (Falco naumanni) (Sara` et al., 2019). All these measures concern connectivity between breeding and wintering areas, but for Montagu’s Harrier, the equivalent value measured from wintering to breeding areas was 0.60 (Trierweiler et al., 2014). Among North American species, rM values based on tracking studies have varied between of 0.07 for Prothonotary Warblers (Tonra et al., 2019) to 0.29 for Common Nighthawks (Chordeiles minor) (Knight et al., 2021), 0.33 for Wood Thrushes (Stanley et al., 2014), and 0.61 and 0.84 for different studies of Ovenbirds (Seiurus aurocapilla) (Cohen et al., 2019; Hallworth & Marra, 2015). Studies on Swainson’s Thrushes in two breeding areas in central California and British Columbia indicated very strong connectivity (rM 5 0.73), with the two populations wintering in different areas from one another (Cormier et al., 2013). Studies of the same species in different locations would be expected to give different measures of connectivity. Purple Martins (Progne subis) have now been tracked using geolocators from nesting colonies across their North American breeding range. Birds of the eastern subspecies (Progne subis subis) showed weak connectivity (little spatial structure) in winter distribution as individuals from colonies across the breeding range were found in the same core wintering region in the northern Amazon basin (Fraser et al., 2012a,b). Birds from a single breeding colony wintered, on average, 900 km apart and overlapped in distribution with birds from other breeding colonies up to 2000 km away. This extensive mixing of breeding populations in a wintering area translates to weak connectivity. However, at the broader subspecies level, Purple Martins show strong connectivity. Tracked individuals from the western North American subspecies (Progne subis arbicola) had a distinct wintering area in southeastern Brazil and showed no overlap with the

1. A Mantel test is one way of testing for spatial autocorrelation, and usually involves measures of distance. For each species inter-population mixing can be quantified as the Mantel correlation coefficient (ranging from 21 to 11) between pairwise distance matrices of the breeding and non-breeding sites of individuals (Ambrosini et al., 2009). This quantifies the extent to which distances between individual breeding sites are maintained in relative terms during the non-breeding season. Strong positive Mantel coefficients (rM) indicate that individuals which breed close together also spend the non-breeding season relatively close together, and vice versa (that is, low inter-population mixing). Cohen et al. (2018) devised an extension of the Mantel’s test which is likely to improve the estimates of connectivity in situations where sampling effort is not proportional to true abundance across the range of the species, and when the strength of migratory connectivity varies across the range.

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wintering range of the eastern subspecies. These results emphasize the importance of spatial scale (as well as phylogenetics) in defining patterns of connectivity. The interest is usually in much smaller parts of the range, where measures can reveal weak or strong connectivity for local populations. Thus, five populations of Collared Flycatchers (Ficedula albicollis) (maximum distance of 100 km between populations) on the Baltic island of Gotland showed consistently different stable isotope values in feathers grown in the African wintering areas (Hjernquist et al., 2009). This implied that these five breeding populations on the same island were also wintering in separate areas (5strong connectivity). Measures of connectivity can also vary with the parts of the annual cycle that are compared: breeding with migration areas, or breeding with wintering areas. Timing is also important, because different populations may occupy the same areas (notably stopover sites) at different dates, so they have no opportunity to interact directly despite using the same area. For measures of connectivity to be most meaningful, studies must be planned for particular species in specific areas with specific aims in mind. Distributional overlap (5weak connectivity) is almost inevitable in populations from a wide breeding area which become concentrated into a narrow wintering area or migration corridor. Examples include the millions of birds which migrate from North American breeding areas through Panama to South American wintering areas. The breeding range of some of these species may stretch over 4000 km from west to east in North America, but in some species, birds from across this wide range may concentrate and pass through a land bridge less than 100 km across. Similar bottleneck sites occur in other parts of the world, leading to concentrations of birds (especially soaring birds) at short-sea crossings. Having passed through a narrow bottleneck, these birds may spread out again as they continue on their journeys but are by now usually mixed with individuals from other parts of the breeding range, as confirmed in some species by ringing and tracking studies. Measures of connectivity calculated as described above can therefore vary along a migration route, and not just between breeding and wintering areas. They may also change as birds move between localities within a winter.

Relationship to population limitation Estimating how much long-distance migrant populations spread out and mix during the non-breeding season is helpful in understanding the effect of external conditions on population dynamics. In a review of published studies, Finch et al. (2017) examined variation in population spread and inter-population mixing in long-distance migrant land-bird populations (712 individuals from 98 populations of 45 species) from studies in the Nearctic-Neotropical and PalaearcticAfrotropical migration systems. They used only studies based on tracking devices (geolocators or satellite tags) and ignored ring recoveries because of the geographical bias in recovery chances. For individuals which moved between several non-breeding sites, only the location of the first site was considered. They restricted analyses to adult birds tagged during the breeding season in the northern hemisphere. Individuals of the same species tagged within 100 km of one another (which in almost all cases meant the same study site) were assigned to the same population, with such ‘populations’ being the principal units of analysis, using the Mantel test as a measure of migratory connectivity. The mean distance between two individuals from the same breeding population (all species combined) during the non-breeding season was 743 km, covering 10 20% of the maximum width of Africa or South America. Individuals from different breeding populations tended to mix during the non-breeding season, although some degree of spatial segregation was apparent in species with relatively large non-breeding ranges. Much of the between-population variation in population spread was predicted by geography, and populations using non-breeding zones with limited land availability (e.g., Central America compared to northern South America) showed lower population spread. Despite some overlap between individuals from different breeding populations in winter, their distributions were non-random, with positive correlations between breeding and non-breeding longitudes, as well as between the distances separating the breeding and non-breeding sites of individuals. The main finding, however, was that strong connectivity was quite rare in widely distributed migratory landbirds (Finch et al., 2017). The conservation implications of weak connectivity are that the loss of any non-breeding site will have a light but widespread effect on many local breeding populations, as described above, rather than a catastrophic effect on any one population, and thus reduce the effect on local breeding populations of local habitat destruction in non-breeding areas. Similarly, the protection of any one non-breeding site will benefit birds from a widespread of breeding sites, but because these birds will form only a small minority of birds in any one breeding locality, the effects will be similarly slight.

Relationship to genetic divergence Levels of connectivity can influence not only local population dynamics, but also, in theory, evolutionary change. This is because connectivity affects the extent to which migrants from the same breeding areas are exposed to the same

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selective pressures. For example, when connectivity is strong, most individuals from one breeding population will migrate to the same non-breeding location and will thus be subject to similar selective pressures as one another in both seasons, potentially leading to pronounced local adaptation. By contrast, when connectivity is weak, individuals from one breeding area migrate to a variety of non-breeding locations, which might vary in the selective pressures they impose. If populations from different parts of the breeding range remain separated from one another for long enough, they can be expected to diverge genetically, as each becomes more closely adapted to the conditions in its particular range. In the absence of immigration of birds from elsewhere, this divergence may become sufficient to warrant the designation of subspecies, and eventually full species status. Many existing subspecies are associated with migratory divides and different non-breeding ranges, illustrating how this process might proceed (Chapter 24). Similarly, if a population becomes increasingly alloheimic through time, and its connections with other populations decline, its chances of genetic divergence are likely to rise. For most bird species, the choice of non-breeding areas is largely irrelevant to the choice of mate because birds form pairs in their breeding areas. But many species of ducks, form pairs in non-breeding areas, sometimes involving individuals from widely separated parts of the breeding range (Chapter 19). This mixing may account for the fact that migratory ducks show almost no morphological variation across the whole of Eurasia or North America. They sit in sharp contrast to most other bird species which, by mating with individuals from their own breeding area, are more likely to develop local adaptations, sometimes recognized in subspecific designations. It is widely accepted that strong (spatial) migratory connectivity can lead to little or no gene flow between populations, thus promoting local adaptations and ultimately, perhaps, speciation (Bensch et al., 1999). But only recently has evidence emerged for birds that temporal segregation can have the same effects. A prominent example is the Eurasian Blackcap, in which there is apparently little or no gene flow between two sub-populations despite them meeting in a common breeding area (Chapter 22). This is mainly explained by differences in the dates of arrival and onset of breeding between these sub-populations which results in assortative mating, restricted gene flow and ultimately phenotypic divergence (Berthold et al., 1992; Bearhop et al., 2005; Rolshausen et al., 2009; Delmore et al., 2020).

TIME AND ENERGY CONSIDERATIONS While the ideas discussed above emphasize the role of competition in influencing the development and maintenance of wintering areas, other models focus on energy and time costs. Imagine that, within a potential wintering range, sites progressively further from the breeding range are more benign, so that day-to-day survival is higher there, but migration costs increase with increasing distance from breeding areas (Greenberg, 1980). The longer the period in each year that birds spend away from their breeding areas, the greater their survival benefits compared to sites closer to the breeding range. Greenberg supposed that natural selection would lead to the non-breeding area being located wherever the benefits of improved survival most exceeded the costs of reduced survival imposed by migration to and from it. If migration costs were the same, regardless of length and date of journey, then longer movements to warmer areas should be favoured, other things being equal. The benefits should be especially great in high-latitude species which generally spend least time on breeding areas and most on wintering areas, and therefore gain the benefits of enhanced survival for the longest period each year. This could provide another explanation for leapfrog migration in which the most northerly breeding populations winter furthest south (but does not eliminate a role for competition). Testing this and similar models requires measurements within species of the energy costs for migrants wintering in different areas, and their fitness consequences. Most relevant studies available to date involve shorebirds. Measurements of energy expenditure (using the doubly labelled water technique) were made on free-living Sanderlings wintering at four different latitudes in New Jersey, Texas, Panama and Peru (Castro et al., 1992). The minimal living cost (observed in Panama) was equivalent to twice the basal (resting) metabolic rate (2BMR), while the peak value (observed in New Jersey) was roughly twice this value (4BMR), mainly reflecting differences in winter temperatures, and hence in thermoregulatory costs, between the two sites. These findings thus confirmed the large savings in body heat maintenance enjoyed by individuals migrating to the tropics. But the energy costs for the birds in reaching these different areas remained unknown. More details were obtained for the Red Knot which breeds in the high arctic but spends its non-breeding season at specific localities spanning a wide range of latitudes, from northern temperate through tropical to southern temperate regions (Figure 25.4). Although many individuals winter at British latitudes, the cold makes this location almost prohibitively expensive for them. During November February, their daily energy costs amount to 4BMR, which is only just achievable in the conditions prevailing, even though the birds adopt all the energy-saving tactics they can muster

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(Piersma et al., 1991). At lower latitudes, the energy costs of keeping warm are much reduced. Largely because of the temperature difference, the maintenance costs of Red Knots in West Africa were about 2.4 BMR, 40% less than in Europe (although the food supplies were also poorer). In fact, in tropical areas, Red Knots and other shorebirds may face the opposite problem to keeping warm namely, that of getting rid of surplus heat which some species achieve by resting on water between bouts of feeding. Interestingly, Red Knots wintering further from their breeding areas do not necessarily incur greater energy costs on migration (Piersma et al., 1991). This was shown in a comparison between two subspecies, one (C. c. canutus) breeding in Siberia and migrating via western Europe (the Wadden Sea) to West Africa (a round trip of 18,800 km), and the other (C. c. islandica) breeding in northeast Canada and Greenland, and migrating via Iceland to winter mainly in eastern England and the Netherlands (round trip of 9600 km) (Table 25.1). Most individuals performed these migrations in two non-stop flights separated by a single stopover. Although canutus knots migrated twice as far as islandica ones, the costs of migration were estimated to be of similar magnitude, because of differences in tailwind availability on route. Both there and back, canutus birds flew parallel to the main weather systems and could always find following winds, sometimes up to 5 km above ground. Such winds could almost double the flight speed of canutus birds, giving them much shorter flight times and reduced travel costs than the shorter-distance islandica birds. On this basis, the canutus birds, by leapfrogging the islandica ones, gained the best wintering area (in terms of energy gain) but at no greater cost in getting there. As a further point, food availability does not necessarily vary in any systematic manner with latitude, and harsher weather at higher latitudes can sometimes be coupled with higher food availability (Castro et al., 1992; Piersma et al., 1993; Mathot et al., 2007). Thus Red Knots have lower fuelling rates at tropical intertidal sites than at either more northern or more southern sites (Piersma, 2007). The energy costs and benefits of occupying different winter locations might then not always be as expected, but in any case could create fitness inequalities which could shape the overall distributions and population trends of the populations concerned Another study involved Icelandic Black-tailed Godwits Limosa limosa islandica wintering on sea coasts in south Ireland, eastern England and Portugal (Alves et al., 2013). For these birds, the energy benefits of the most distant winter location (Portugal) were sufficient to outweigh the greater migration costs. Birds that wintered in west Portugal experienced not only lower thermoregulatory costs but also considerably higher energy intake rates (mainly through greater prey biomass) than conspecifics wintering in south Ireland and eastern England. The thermoregulatory demands in Portugal could be met by foraging for only about 5.1 hours/day on the mudflats. By contrast, in south Ireland, foraging for 9 hours/day (the maximum possible on these tidal mudflats) was insufficient to cover thermoregulation, and TABLE 25.1 Travel distances and approximate annual average energy expenditure on long-distance flights by temperate wintering Red Knots (Calidris canutus) of the subspecies islandica (Ellesmere Island to the Netherlands) and tropically wintering Red Knots of the subspecies canutus (Siberia to West Africa). Cost factors for long-distance flights were calculated from estimated fat losses over the journey. Route

Subspecies islandica

West Africa Wadden Sea (km)

canutus 4600

Wadden Sea Taimyr (km)

4800

Wadden Sea Iceland (km)

2100

Iceland Ellesmere Island (km)

2700

Total one-way (km)

4800

Total return (km)

9600

9400 18,800

Travel cost (kJ/km)

0.7 0.8

0.3 0.5a

Annual flight cost (kJ/year)

6720 7680

5640 9400

Average cost on annual basis (W)

0.22 0.25

0.18 0.30

a

a

Estimated from measures of fat loss on migration of 0.8 kJ/km for southeast England to northern Norway, 0.7 kJ/km for northern Norway to Ellesmere Island, 0.3 kJ/km for West Africa to the Netherlands (Wadden Sea) and 0.5 kJ/km for Wadden Sea to Siberia (Taimyr). Observational evidence shows that these distances are normally covered in a single non-stop flight, the whole one-way journey being made up of two flights with a single stopover. From Piersma et al. (1991).

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additional foraging on nearby grasslands was required. In eastern England, despite godwits increasing their foraging time over winter, their maintenance needs were barely met during some winter months, and suitable grasslands were not available locally to provide other food. Overall, Icelandic godwits wintering in west Portugal enjoyed a more positive energy balance, showed higher survival and arrived in Iceland significantly earlier than godwits wintering in east England, despite undertaking a longer spring migration that required double the energy. Earlier arrival enabled the Portuguese-winterers to occupy better breeding habitat. In this situation, therefore, conditions in different wintering areas produced population-wide fitness inequalities in both nonbreeding and breeding seasons. It left open the question of why some birds continued to winter in eastern England when they would have apparently been better off in Ireland and better still in Portugal. But in godwits, as in some other bird species, much depends on where young birds settle on their first migration, for survivors then tend to remain faithful to that site for the rest of their lives. The authors suggested that lateness in season or poor body condition may have caused some young birds to end their first migration in England (in the north of the wintering range), rather than moving on further south. These studies on shorebirds thus led to two conclusions: (1) for birds taking different routes (like the two races of Red Knots), travel costs are not necessarily greater on the longer migration, because they depend partly on wind conditions; (2) for birds wintering further from their breeding areas on the same route, travel costs may be greater, but maintenance costs in warmer wintering areas may be lower; and (3) food intake rate also plays a major role, and may not vary with latitude in the manner expected. These comparisons were concerned primarily with energy budgets, however, and not with the mortality risks from periods of energy shortage, or from other causes, which may have differed greatly between populations migrating different distances and wintering in different areas. It is not the energy budget as such that matters, but the costs in terms of mortality and reproduction that provide the selection pressures affecting migratory and wintering areas of different populations. And energy costs are of limited importance if food is sufficiently plentiful that birds can easily meet them. Nevertheless, these calculations on the energy costs of migration question the assumptions on which some models of the evolution of migratory behaviour have been based. They do not eliminate the likelihood that, among closely related taxa, differences in winter range evolved partly in response to competition between individuals from different populations. Competition involves the all-important food supplies which underpin both migration and survival. Studies on other birds have given some puzzling results. For example, among Eurasian Spoonbills (Platalea leucorodia) nesting in the Netherlands, short-distance migrants wintering in southern Europe showed higher annual survival than long-distance migrants wintering in West Africa (Lok et al., 2013, 2015). The short-distance birds also laid eggs earlier than long-distance ones and produced chicks of better condition (Lok et al., 2017). Assuming these findings were typical, and given the advantages of short-distance wintering, one wonders why any birds migrated as far as West Africa. One possible explanation, suggested by the authors, was a delay in the evolutionary response to climate change which has made wintering in Europe more profitable than in the past. If this is true, one would expect the proportion of migrants wintering in Europe to increase in years to come, leading to a reduction in average migration distances. Similar research on seabirds revealed that the energetic consequences of different migration strategies balance out. Among Northern Gannets nesting in east Scotland and wintering at varying distances south to West Africa, the longer travel costs in the West African birds were offset by thermoregulatory gains; however, these long-distance birds were latest (by 12 days) to arrive at the nesting colony in spring (Garthe et al., 2012). In another study, based on Svalbard, Thick-billed Murres were found to migrate further than Common Murres, but the overall energy expenditure estimated for the non-breeding season was similar in both species. Evidently, longer-distance migration was again offset by the greater warmth of the wintering area (Fort et al., 2013). Other studies also revealed that seemingly plausible assumptions on the travel and wintering costs of migrants do not necessarily hold. One study examined the annual costs of flight in Lesser Black-backed Gulls (Larus fuscus) from the same colony in the Netherlands but which followed different migration strategies (Shamoun-Baranes et al., 2017a,b). The annual cumulative distances travelled by gulls wintering in West Africa, over 4000 km from the nesting colony, did not differ significantly from the annual cumulative distances travelled by individuals of the same breeding colony wintering only a few hundred kilometres away in Britain. This comparison considered all flight and not just migratory flight, and birds wintering in both areas spent roughly similar times on the wing. For thermoregulation, the short-distance migrants should face relatively high energy expenditure through spending the entire annual cycle in the temperate zone, compared to migrants overwintering in coastal West Africa. However, the short-distance migrants again arrived earlier on the breeding grounds than long-distance migrants and could thereby have gained priority access to prime nesting sites. Some of the species discussed above may be in the process of altering their migratory habits in response to changing conditions. We would not then be dealing with a stable situation. In any case, the value of energy costs in explaining migration patterns is limited, because what matters is the ease with which birds can obtain the food to meet those costs, and their impacts on survival or reproductive success. These are the factors that most influence the strength and direction

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of natural selection. Only in the Black-tailed Godwits and Eurasian Spoonbills among the above studies were fitness differences between wintering areas assessed in terms of survival and subsequent reproduction. The main point to emerge is that expected patterns of energy demand do not always hold. This may be partly because existing measures of energy demand are too crude, but in any case, for a fuller understanding of the costs and benefits of different migration patterns found within species, studies of energy and time budgets must be combined with studies of survival and reproduction. In any case, the energy needs of individuals are not entirely divorced from the spatial distributions of populations. The minimization of competition through the spatial segregation of populations could be an important factor influencing the ease with which individuals could meet their energy needs, whatever their wintering area (for exploration of the roles of energy budgets and competition in the distribution patterns some North American species, see Somveille et al., 2021).

SUMMARY As a result of migration, bird distributions change seasonally. Nevertheless, in many species, some longitudinal segregation of populations in breeding areas is more or less maintained in wintering areas, through migration along parallel routes. Birds that occur furthest west in the breeding range also occur furthest west in the non-breeding range, while those that breed furthest east also winter furthest east. An alternative longitudinal pattern is fan migration in which birds from a large part of the breeding range may funnel into the narrow width of a small wintering range, or birds from a narrow width of the breeding range may spread across a wide span of wintering range, intermingling with birds from other areas. Three main latitudinal patterns are (1) chain migration (northernmost breeding population wintering furthest north and southernmost furthest south), (2) leapfrog migration (northernmost breeding population wintering furthest south), or (3) telescopic migration (birds from a wide latitudinal span of breeding range concentrating in the same narrow latitudinal span of wintering range, or vice versa). Connectivity is concerned with the degree to which populations of a species from different breeding areas overlap and mix in non-breeding areas. At one extreme, specific breeding and wintering populations may be tightly linked, with virtually no seasonal mixing with individuals from other populations (strong connectivity). At the other extreme, birds from a particular breeding area may spread over a larger part of the wintering range, intermingling with birds from other parts of the breeding range (weak connectivity). If connectivity is strong (and hence mixing weak), the effects of events in the wintering area will be limited to the particular local breeding population that winters there, and are likely to be noticeable in that breeding area. But if connectivity is weak, local winter events will have only diffuse effects on breeding populations across a broader area, and will be less noticeable in particular breeding areas. Populations showing strong connectivity over long enough periods are also likely to diverge genetically from other populations of their species, owing to consistent selection pressure in the areas concerned, gradually adapting populations to particular local conditions. Patterns of winter distribution among migratory birds are consistent with the notion that competition has been a major factor in their development. However, non-breeding distributions have been examined, not just in terms of competition theory, but also in terms of energy budgets, including the costs of wintering at different latitudes and the costs of migrating different distances. They suggest that, while in general, the daily energy costs of winter survival decline with decreasing latitude, as expected from the warmer temperatures, the energy costs of migration do not necessarily correlate well with the distance travelled but also depend on the route taken and the prevailing winds. More studies are needed on the energy budgets of migrants wintering in different areas, combined with studies of fitness measures (survival and reproduction). As yet, nothing in the consideration of energy budgets is at odds with the idea of competition as a factor influencing the winter distributions of migratory birds, even though other factors, including the costs of migration, are almost certainly involved.

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Part 5

Migration systems and population limitation

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Chapter 26

The Palearctic-Afrotropical migration system

Sand Martins (Riparia riparia), whose European breeding numbers are strongly affected by conditions in African wintering areas. If there were no warmer lands to the south, the Palaearctic avifauna would be considerably poorer. David Lack, 1954.

Each autumn, after breeding in Eurasia, many millions of birds, from tiny warblers to large eagles, travel to wintering areas in tropical Africa, and back again next spring. This is perhaps the most impressive migration system in the world, not merely because of the huge numbers of participants but also because of the long and formidable journeys involved. Birds from the west of Eurasia cross the Mediterranean Sea and Sahara Desert, while those from further east cross the deserts of southwest Asia and Arabia. Many of these same birds also negotiate high mountain ranges, whether in Europe or Asia (Figure 26.1). Moreover, once in Africa, all these migrants cram into a geographical area less than half the size of their Eurasian breeding grounds, adding to an avifauna already rich in native species (Moreau, 1972). Those that winter north of the equator do so in a season of progressively deteriorating conditions. On their return, most migrants must fatten for the journey in the Sahel zone, just south of the Sahara, at the driest time, when many types of food are near their seasonal low.

THE BIRDS INVOLVED Of the landbirds that breed in the Palaearctic region (comprising most of Eurasia), about 186 species winter wholly or partly in Africa south of the Sahara, excluding seabirds (Table 26.1). Some 169 of these migrants are drawn from the western Palaearctic the region lying immediately to the north of Africa, with a similar number of (mainly the same) species (164) coming from the mid-Palaearctic between 45 E and 90 E (Table 26.1). Only about 24 species are known to come from the eastern Palaearctic, beyond 90 E, and some even from Alaska and the Yukon, although this latter figure may increase in the years ahead, as more tracking studies are undertaken. Some of these birds on their journeys travel as much as 180 westward, covering more than 10,000 15,000 km by the shortest (great circle) routes to reach their winter quarters (nearly as far as from London to Sydney). They include such spectacular travellers as the Amur Falcon (Falco amurensis), Northern Wheatear (Oenanthe oenanthe), Common Cuckoo (Cuculus canorus) and the tiny The Migration Ecology of Birds. DOI: https://doi.org/10.1016/B978-0-12-823751-9.00008-7 © 2024 Elsevier Ltd. All rights reserved, including those for text and data mining, AI training, and similar technologies.

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