Harvestmen: The Biology of Opiliones 9780674276833

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HARVESTMEN

HARVESTMEN The Biology of Opiliones Edited by Ricardo Pinto-da-Rocha Glauco Machado and Gonzalo Giribet

Harvard University Press Cambridge, Massachusetts, and London, England 2007

Copyright © 2007 by the President and Fellows of Harvard College All rights reserved Printed in the United States of America Library of Congress Cataloging-in-Publication Data Harvestmen : the biology of Opiliones / edited by Ricardo Pinto-da-Rocha, Glauco Machado, and Gonzalo Giribet. p. cm. Includes bibliographical references and index. ISBN-13: 978-0-674-02343-7 (alk. paper) ISBN-10: 0-674-02343-9 (alk. paper) 1. Opiliones. I. Pinto-da-Rocha, Ricardo. II. Machado, Glauco. III. Giribet, Gonzalo. QL458.5.H37 2006 595.4'3—dc22 2006043622

Contents

Contributors vii Preface ix

1 What Are Harvestmen?

1

Glauco Machado, Ricardo Pinto-da-Rocha, and Gonzalo Giribet

2 Morphology and Functional Anatomy

14

Jeffrey W. Shultz and Ricardo Pinto-da-Rocha

3 Phylogeny and Biogeography

62

Gonzalo Giribet and Adriano B. Kury

4 Taxonomy

88

Ricardo Pinto-da-Rocha and Gonzalo Giribet

5 Paleontology

247

Jason A. Dunlop

6 Cytogenetics

266

Nobuo Tsurusaki

7 Ecology

280

David J. Curtis and Glauco Machado

v

vi

Contents

8 Diet and Foraging

309

Luis E. Acosta and Glauco Machado

9 Natural Enemies

339

James C. Cokendolpher and Plamen G. Mitov

10 Defense Mechanisms

374

Pedro Gnaspini and Marcos R. Hara

11 Social Behavior

400

Glauco Machado and Rogelio Macías-Ordóñez

12 Reproduction

414

Glauco Machado and Rogelio Macías-Ordóñez

13 Development

455

Pedro Gnaspini

14 Ecophysiology

473

Flávio H. Santos

15 Methods and Techniques of Study References 525 Taxonomic Index 575 Subject Index 587

489

Contributors Luis E. Acosta CONICET—Facultad de Ciencias Exactas, Físicas y Naturales Universidad Nacional de Córdoba Av. Vélez Sarsfield 299 5000 Córdoba, Argentina

Gonzalo Giribet Department of Organismic & Evolutionary Biology and Museum of Comparative Zoology Harvard University 16 Divinity Avenue Cambridge, MA 02138, USA

Sarah L. Boyer Department of Organismic & Evolutionary Biology and Museum of Comparative Zoology Harvard University 16 Divinity Avenue Cambridge, MA 02138, USA

Pedro Gnaspini Departamento de Zoologia Instituto de Biociências Universidade de São Paulo, CP 11294 05422-970 São Paulo, SP, Brazil

Thomas S. Briggs Department of Entomology California Academy of Sciences Golden Gate Park San Francisco, CA 94118, USA James C. Cokendolpher Natural Science Research Laboratory Museum of Texas Tech University Lubbock, TX 79409, USA David J. Curtis Department of Biological Sciences University of Paisley Scotland, United Kingdom Jason A. Dunlop Institute für Systematische Zoologie Museum für Naturkunde der Humboldt Universität zu Berlin Invalidenstrasse 43 D-10115 Berlin, Germany

Jürgen Gruber Naturhistorisches Museum in Wien Burgring 7 A-1014 Wien, Austria Marcos R. Hara Departamento de Zoologia Instituto de Biociências Universidade de São Paulo, CP 11294 05422-970 São Paulo, SP, Brazil Adriano B. Kury Departamento de Invertebrados Museu Nacional Universidade do Brasil Quinta da Boa Vista 20940-040 Rio de Janeiro, RJ, Brazil Glauco Machado Museu de História Natural Instituto de Biologia Universidade Estadual de Campinas, CP 6109 13083-970 Campinas, SP, Brazil vii

viii

Contributors

Rogelio Macías-Ordóñez Departamento de Biología Evolutiva Instituto de Ecología A.C., Ap. Postal 63 Xalapa, Veracruz, 91000, Mexico Amanda C. Mendes Departamento de Invertebrados Museu Nacional Universidade do Brasil Quinta da Boa Vista 20940-040 Rio de Janeiro, RJ, Brazil Plamen G. Mitov Department of Zoology and Anthropology Faculty of Biology University of Sofia 8 Dragan Zankov Blvd. 1164 Sofia, Bulgaria Abel Pérez González Departamento de Invertebrados Museu Nacional Universidade do Brasil Quinta da Boa Vista 20940-040 Rio de Janeiro, RJ, Brazil

Peter Schwendinger Muséum d’histoire naturelle 1, route de Malagnou, CH-1211 Genève 6, Switzerland Jeffrey W. Shultz Department of Entomology University of Maryland College Park, MD 20742, USA Christopher K. Taylor Department of Terrestrial Invertebrates Western Australian Museum Locked Bag 49, Welshpool 6986 Western Australia, Australia Ana Lúcia Tourinho INPA—Instituto Nacional de Pesquisas da Amazônia Coordenação de Pesquisas Ecológicas/CPEC-Setor V8 Avenida André Araújo, 2936-Aleixo, CP478 69011-970 Manaus, AM, Brazil Nobuo Tsurusaki Laboratory of Biology Faculty of Regional Sciences Tottori University Tottori, 680-8551, Japan

Ricardo Pinto-da-Rocha Departamento de Zoologia Instituto de Biociências Universidade de São Paulo, CP 11461 05422-970 São Paulo, SP, Brazil

Darrell Ubick Department of Entomology California Academy of Sciences Golden Gate Park San Francisco, CA 94118, USA

Flávio H. Santos Departamento de Zoologia Instituto de Biociências Universidade de São Paulo, CP 11294 05422-970 São Paulo, SP, Brazil

Rodrigo H. Willemart Departamento de Zoologia Instituto de Biociências Universidade de São Paulo, CP 11294 05422-970 São Paulo, SP, Brazil

Preface

T

he idea of writing a book on Opiliones started more than four years ago as a result of the need for a comprehensive volume that encompassed all aspects of harvestman biology, as had been done previously for mites, spiders, scorpions, pseudoscorpions, camel spiders, and whip spiders. Although harvestmen are the third-largest group of arachnids and one of the most common finds of amateur naturalists, little synthetic work on their biology and systematics had been put together. This book serves this purpose, and for this reason it has been compiled by a large body of experts working in 11 countries in the Americas, Asia, Europe, and Australia. This is the first time that a large fraction of the available literature on harvestman biology and systematics—including works written in many different languages—has been put together in a comprehensive volume. In doing so, the authors have relied on studies of the unique attributes of Opiliones biology, as well as on general behavioral and ecological investigations conducted using harvestman species. This book should provide the international audience with a broad taxonomic and ecological framework for understanding Opiliones and comparing them with spiders, scorpions, and other well-studied arachnids. Broad in scope, this volume is aimed at answering relevant questions from a diversity of fields, while at the same time indicating areas in which additional research is needed. It is furthermore intended to provide an in-depth summary of our current understanding of harvestman biology and systematics both for researchers already acquainted with harvestmen and for the uninitiated community. Thus the book should be of great interest to arachnologists, as well as to zoologists, ecologists, and amateur naturalists in general. The chapters were written with an interdisciplinary audience in mind, and they give broad synthetic views within their different specialties; the result, we hope, is that the text is palatable enough to attract the interest of experts and nonexperts alike, including graduate students. The book is composed of 15 chapters written by 25 authors. Although extensive editorial work was needed to accommodate the heterogeneity of styles and to avoid the traditional problems of a book with many contributors, a careful reader may certainly encounter some inconsistencies. Some topics have been touched upon in more than one chapter, although we have attempted to eliminate redundancies as much as possible. Other topics have not been discussed in detail in this volume because of the lack of information available in the harvestman literature or because there are currently no active experts on the subject. However, we are confident that the quality and depth of the information provided in the book will supplant any occasional omission. ix

x

Preface

Compiling such a comprehensive volume was no easy task, and the process took almost four years. During this time we received the help of many people to whom we are greatly indebted. First of all, we thank the contributors to this book, who patiently dealt with our many requests and helped during the editing process. All chapters were peer-reviewed, and thus we extend our acknowledgments and gratitude to all the professionals who carefully revised the chapters of the book. We fully realize that reviewing manuscripts is one of the most altruistic tasks and takes enormous amounts of time and effort. As a small token of our appreciation, the names of all reviewers are listed here (institutions of contributors are given in the section “Contributors”): Luis E. Acosta, Dalton de Souza Amorim (Universidade de São Paulo, Brazil), Murray S. Blum (University of Georgia at Athens, USA), Sarah Boyer, Alan B. Cady (Miami University, USA), Jonathan A. Coddington (National Museum of Natural History and Smithsonian Institution, USA), James C. Cokendolpher, Richard M. Duffield (Howard University, USA), William G. Eberhard (Universidad de Costa Rica and Smithsonian Institution, Costa Rica), Malcolm Edmunds (University of Central Lancashire, United Kingdom), Mark A. Elgar (University of Melbourne, Australia), Marcelo O. Gonzaga (Universidade Estadual de Campinas, Brazil), Phillipe Grandcolas (Muséum National d’Histoire Naturelle, France), Jürgen Gruber, Robert Holmberg (Athabasca University, Canada), Tappey H. Jones (Virginia Military Institute, USA), Adriano B. Kury, John R. B. Lighton (University of Nevada, USA), Rogelio Macías-Ordóñez, Michael McAloon (University of Connecticut, USA), Fernando L. P. Marques (Universidade de São Paulo, Brazil), Jochen Martens (Institut für Zoologie, Mainz, Germany), Adriano S. Melo (Universidade Federal do Rio Grande do Sul, Brazil), Douglass H. Morse (Brown University, USA), Arturo Muñoz-Cuevas (Muséum National d’Histoire Naturelle, France), Tone Novak (Facoltà di Pedagogia, Slovenia), Abel Pérez González, George A. Poinar (Oregon State University, USA), Jerome C. Regier (University of Maryland, USA), Adalberto José dos Santos (Instituto Butantan, Brazil), David S. Saunders (University of Edinburgh, Scotland), Peter Schwendinger, Paul Selden (University of Manchester, United Kingdom), William A. Shear (Hampden-Sydney College, USA), Jeffrey W. Shultz, Douglas W. Tallamy (University of Delaware, USA), Nobuo Tsurusaki, Darrell Ubick, Peter Weygoldt (Albert Ludwigs Universität, Germany), and Vito Zingerle (Natural History Museum South Tyrol, Italy). Finally, we would like to thank Ron Clouse and Jim Hesson, who kindly revised the contents and English grammar of several chapters, Humberto Yamaguti for helping with the edition of the plates, and Ann Downer-Hazell from Harvard University Press for sharing her editing expertise and patiently dealing with our many requests and schedule changes. This book is dedicated to our families and students for their understanding and support. It is also dedicated to three of the greatest modern opilionologists, Christian Juberthie, Jochen Martens, and Maria Rambla, whose indefatigable work served as an inspiration to us.

CHAPTER

1

What Are Harvestmen? Glauco Machado, Ricardo Pinto-da-Rocha, and Gonzalo Giribet

T

he name Opiliones, proposed by the Swedish zoologist Karl J. Sundevall (1833), derives from the Latin word opilio, used by the Roman dramatist Plautus (254– 184 BC) in his comedies and meaning “sheep-master”—one of the various categories of Roman slaves. Virgil’s Eclogues, written in 37 BC, also mentions the word opilio, but alluding to a shepherd. This association is probably related to the elevated body position afforded by the long legs of certain harvestman species, thus resembling ancient European shepherds who used to wander about on stilts in order to better count their flocks. The earliest allusion to the order Opiliones in modern literature probably occurred in The Theater of Insects by Moffett (1634), in which they were called shepherd spiders, a name still used in Great Britain nowadays. The author explained that people called them shepherds because they thought that the fields in which they were abundant constituted good sheep pasture. The most popular common names in England nowadays are harvestmen or harvest spiders, probably because some species are quite abundant in the harvest season. Another hypothesis is that the convulsive movement made by their legs after they have become detached from the owner’s body (a common defensive behavior in some species of the order) resembles that of the harvestman’s scythe. The meaning of many common names in European countries is “reaper” (see Table 1.1), and this also may be related to the harvest period or to the appearance of reaping, as with a scythe, when they walk. Curiously, in some provinces of Spain harvestmen are called pedros in allusion to Saint Peter’s Day (June 29), which falls within the harvest season and is a time when some species are especially abundant in the fields. Apparently the common names used in the Netherlands and South Africa, which mean “hay wagon” (see Table 1.1), also allude to the harvest period. In countries where the opiliofauna is dominated by long-legged species, the common names generally make reference to this characteristic morphological trait. Good examples are daddy longlegs, used in North America and Australia, arañas 1

2

What Are Harvestmen?

Table 1.1 Popular names attributed to Opiliones around the world and their respective meaning in English Name (singular)

Country (language)

Meaning

Afterspinne

Germany (German)

False spider

Agostero

Spain (Spanish)

Flock of sheep that graze on recently harvested fields, or simply harvestman1

Araña patona

Mexico and Spain (Spanish)

Long-legged spider

Aranha-alho

Brazil (Portuguese)

Garlic spider

Aranha-bailarina

Brazil (Portuguese)

Dancing spider

Aranha-bode

Brazil (Portuguese)

Goat spider

Aranha-fedorenta

Brazil (Portuguese)

Stink spider

Bodum

Brazil (Portuguese)

Bad smell

Carter

United States (English)

—

Chichina or chinchina

Argentina (Spanish)

Stink bug

Daddy longlegs

United States and Australia (English)

—

Faucheur or faucheux

France (French)

Reaper

Frade-fedorento

Brazil (Portuguese)

Stinky friar

Frare

Spain (Catalan)

Friar

Gira mundo

Brazil (Portuguese)

Traveler

Grandfather-graybeard

United States (English)

—

Harry-longlegs

United States (English)

—

Harvestman

Great Britain (English)

—

Hooiwa

South Africa (Afrikaans)

Hay wagon

Hooiwagen

Netherlands (Dutch)

Hay wagon

Jangnim kóhmi 2

Korea (Korean)

Blind spider

Kanker

Germany (German)

After the Latin word cancer, which means “crab”

Kaszáspók

Hungary (Hungarian)

Reaper

Kosar

Ukraine (Ukrainian)

Reaper

Kosarz3

Poland (Polish)

Reaper

Kosec

Slovakia (Slovakian)

Reaper

Langbein

Norway (Norwegian)

Long legs

Lockespindel

Sweden (Swedish)

Curled-hair spider

Lukki

Finland (Finnish)

Word used only for Opiliones, with no other meaning

Mang zhu

China (Chinese)

Blind spider

Matija

Slovenia (Slovenian)

Long-legged person

Medelwr

Wales (Welsh)

Reaper

Mejere

Denmark (Danish)

Reaper

What Are Harvestmen?

Name (singular)

Country (language)

3

Meaning

Mekuragumo4

Japan (Japanese)

Blind spider

Müjdeci or mücdeci

Turkey (Turkish)

Person who brings good news

Pauk kosac or just kosac

Bosnia and Herzegovina, Croatia, Serbia and Montenegro, Macedonia, and Slovenia (Slavic languages)

Harvestman spider or just harvestman

Pedro

Spain (Spanish)

In allusion to Saint Peter’s Day, which matches with the harvest period

Pendejo

Costa Rica (Spanish)

Fearful

Pinacates

Mexico and Spain (Spanish)

Name used for a black beetle that lives in damp and shadowed places

Putnik

Serbia and Montenegro (Serbian)

Traveler

Schneckenkanker

Germany (German)

Snail harvestman

Sekácˇ i

Czech Republic (Czech)

Reaper

Senokosec

Russia (Russian)

Reaper

Shepherd spider

Great Britain (English)

—

Suha juzˇina

Slovenia (Slovenian)

Thin, bony, and mostly tall person

Teiliwr

Wales (Welsh)

Tailor

Vevkjerringer

Norway (Norwegian)

Old woman weaver

Weberknecht

Austria and Germany (German)

Weaver’s helper

Zatomushi

Japan (Japanese)

Blind bug

Zimmermann

Switzerland (German)

Carpenter

Names directly derived from the name of the order, such as opilionidi (Italian), opilión (Spanish), or opilião (Portuguese), were not included in the list. 1. The first meaning was extracted from Rambla (1974), and the second is an alternative hypothesis since the word agostero comes from agosto (August), which is a harvest month in Spain. 2. In some places the word kóhmi (spider) may also appear as gumi. 3. This word derives from kosiarz, which means “reaper.” 4. This name is no longer used in Japan because the word mekura has discriminatory connotations to blind people.

patonas, used in Mexico, and suhe juzine and matija, used in Slovenia (Table 1.1). In tropical regions, especially in South America, where the opiliofauna is mainly composed of robust and short-legged species, the common names are usually related to the bad smell released by the scent glands located on the anterior margins of the body, a unique morphological feature of Opiliones. In Argentina they use the words chichina or chinchina, which are also applied to stink bugs of the order Heteroptera (Table 1.1). In Brazil names such as bodum, aranha-bode, aranha-fedorenta, aranhaalho, and frade-fedorento are all related to the strong sour smell secreted by the large gonyleptids (Table 1.1), by far the most common family in the country. Biologists know little about the order Opiliones, even though it constitutes, after the Acari (mites and ticks) and Araneae (spiders), the third-largest group of arachnids. In many countries the general public largely ignores harvestmen as well. Perhaps because most species have secretive habits, live in damp and shadowed areas, are dark colored, and are active mainly at night, their existence passes almost unno-

4

What Are Harvestmen?

ticed by humans, which may explain their virtual absence in mythology, folklore, and history. It is worth noting that Robert Hooke (1665), the inventor of the microscope, mentions in his book Micrographia an old superstition of the county of Essex, England, involving harvestmen. According to the tale, killing harvestmen on purpose would bring bad luck because supposedly these mystical animals would help the farmers harvest the crops with the scythe they were alleged to possess. On the other hand, harvestmen do not have such good fame in the United States and Australia, and there is a persistent urban legend that they are extremely poisonous, although their mouthparts are too tiny to inflict wounds on humans. As you will learn in this book, harvestmen are beautiful arachnids that pose no danger to humans. There are several explanations of the origin of this legend, but the most plausible is the confusion regarding the name “daddy longlegs,” which is also used for spiders of the family Pholcidae in those countries. Since some pholcids regularly prey on other spiders—including the redback spider (Latrodectus hasselti), whose venom can be fatal to humans—it is possible that this fact has originated the rumor that they are the most dangerous spiders in the word. However, because of their tiny fangs, pholcids, like harvestmen, are completely harmless to humans. In terms of general morphology, harvestmen are typical arachnids. They have two basic body regions, a prosoma, which carries all the appendages, and a limbless opisthosoma, which has the spiracles and the genital opening, often covered by an operculum (see Chapter 2). The junction between both body regions is not constricted, giving them the appearance of “waistless” spiders. Because of the superficial resemblance between harvestmen and their most famous cousins of the order Araneae, one of their popular designations in German is Afterspinne, that is, “false spider.” Another common German name, Weberknecht (“weaver’s helper”), is also an allusion to harvestman morphology; the second pair of legs is elongated in most species of the order and functions like an antenna, waving in the air while the animal is walking, thus resembling the arm movements of a weaver’s helper disentangling the threads on a loom. (Another meaning is “tailor’s apprentice” because harvestmen cannot make webs.) It is interesting to note that the use of the word Weber (weaver) has led to the wrong idea that harvestmen, which have no spinning organs, can produce silk. Harvestmen are among the oldest arachnids, and the fossil record demonstrates that the group has remained almost unchanged morphologically over a long period, a phenomenon called stasis (see Chapter 5). Unique characteristics of Opiliones, such as paired tracheae, the penis, the ovipositor, and the openings of the scent glands, are already observed in fossils from the Devonian, proving that the group has lived on land and that males transferred gametes directly to females as early as 400 million years ago. In fact, harvestmen are considered one of the most primitive forms of arachnid, possibly closely related to scorpions, pseudoscorpions, and solifuges; together these four arachnid orders form a clade called Dromopoda. However, the exact phylogenetic position of Opiliones within the class Arachnida remains a contentious issue in systematics (see Chapter 3). The first harvestman species to be described were Phalangium opilio and Trogulus

What Are Harvestmen?

tricarinatus, named by Linnaeus in 1758. Since that time some 6,000 species have been described by more than 110 taxonomists, of whom half described more than 10 species. Nearly 200 harvestman species scattered around the world were described between the 1870s and the first decade of the twentieth century (Figure 1.1a), when Eugène Simon, Tord Tamerlan Theodor Thorell, William Sørensen (Figure 1.2a), and Nathan Banks, among others, introduced more than 700 new species. An intense descriptive period occurred between the 1910s and the 1950s, when the German author Carl Friedrich Roewer (Figure 1.2b) was most active, describing more than one-third of the species in the order Opiliones. He created a new system of classification, and his book Die Weberknechte der Erde, published in 1923, is a landmark, containing the 2,000 harvestman species known until that time and many descriptions of new taxa. Roewer’s age was also a time of other important prolific taxonomists, such as the Brazilian Cândido Firmino de Mello-Leitão (Figure 1.2c) and the South African Reginald Frederick Lawrence (Figure 1.2d). Some years later, between 1940 and 1980, the American couple Marie Louise and Clarence Goodnight (Figure 1.2e), the Brazilian Hélia Eller Monteiro Soares (Figure 1.2f), and the Japanese Seisho Suzuki (Figure 1.2g) were also very productive, describing in all almost 700 species. Nowadays, modern authors are more concerned with reviewing groups than with describing an extensive amount of taxa. Exceptions to this pattern are Jochen Martens (Figure 1.2h) and Manuel González-Sponga (Figure 1.2i), who have been working with the rich faunas of the Himalayas and Venezuela, respectively. The tropical faunas of Africa, Asia, and Central South America probably contain a large unknown diversity yet to be described, mainly in the most diverse families Sclerosomatidae, Gonyleptidae, and Cosmetidae. Minute forms, such as the zalmoxids and Cyphophthalmi, may also provide many new species, so the real richness of the order may exceed 10,000 species. Harvestmen are divided into four suborders that contain 45 recognized families and about 1,500 genera. However, the limits and relationships of most families and genera are imprecise, and new families are expected to be discovered. Chapter 4 presents a brief morphological description of all suprageneric groups, including comments on their distribution, relationships, main references, and keys. Representatives of Cyphophthalmi, the oldest suborder, which includes 6 families and 130 species, are distributed worldwide, inhabiting all continents and islands of continental origin. They are among the smallest and most obscure Opiliones, typically measuring between 1 and 3 mm in body length. The suborder Eupnoi includes 6 families and 1,780 species, and some species of this group are among the bestknown Opiliones. They are widely distributed in both hemispheres, and the great majority of the species are soft bodied and long legged. The members of Dyspnoi present a great diversity of sizes and morphologies, including the largest harvestman species, Trogulus torosus, with a body 22 mm long. This suborder is divided into 7 families containing 290 species, which are mainly found in the Northern Hemisphere. Laniatores is the most diverse suborder, composed of 26 families and 3,748 species distributed mainly in tropical and temperate regions of the Southern Hemisphere. Many representatives can reach large sizes, such as the gonyleptid Mi-

5

6

What Are Harvestmen?

Figure 1.1. (a) Cumulative number of described harvestman species (including only valid names of living species) in each decade from 1758 to 1999. Note that the point of inflexion of the curve is in the 1950s, which coincides with the ending of Roewer’s career. The number of species described per decade is strongly correlated with the number of active taxonomists (R2 = 0.637; F = 40.364; p < 0.001). (b) Cumulative number of articles on harvestman biology published from 1901 to 2000. It includes only articles (not theses or congress abstracts) published in English, French, Italian, German, Japanese, Portuguese, and Spanish. Taxonomical works that present only anecdotal information on natural history were not included in the count. The contribution of researchers from each continent is as follows: North America, 23% of all articles; Central America, 3%; South America, 18%; Europe, 47%; Asia, 1%; Africa, 1%; Oceania, 2%.

What Are Harvestmen?

Figure 1.2. The ten opilionologists who have described the most species. (a) The Danish William Sørensen (1848–1916): 157 valid species described. (b) The German Carl Friedrich Roewer (1881– 1963): 2,260 valid species described. (c) The Brazilian Cândido Firmino Mello-Leitão (1886–1948): 347 valid species described. (d) The South African Reginald Frederick Lawrence (1897–1987): 224 valid species described. (e) The American couple Marie Louise Goodnight (1916–1998) and Clarence J. Goodnight (1914–1988): 313 valid species described. (f) The Estonian, naturalized Brazilian Hélia Eller Monteiro Soares (1923–1999): 169 valid species described. (g) The Japanese Seisho Suzuki (1914–): 201 valid species described. (h) The German Jochen Martens (1941–): 147 valid species described. (i) The Venezuelan Manuel González-Sponga (1929–): 219 valid species described.

7

8

What Are Harvestmen?

tobates triangulus (leg IV can reach 185 mm), and some of them are colorful and/or well armed with spines. Although the four suborders are recognized as monophyletic groups, the relationship among them is still controversial (see Chapter 3). There is no doubt that Cyphophthalmi was the first group to derive, but morphological and molecular studies have recently demonstrated that the Dyspnoi could be grouped either with Eupnoi or Laniatores. Relationships among superfamilies/families are also obscure for most groups, mainly the highly diverse Laniatores. Most harvestmen, especially the tropical forms, have a low dispersal capability and high endemicity, and thus they are good models for biogeographic studies (see Chapter 3). Biogeographic studies with harvestmen have just begun, but they may play an important role in our knowledge of the events that have caused the diversification of biotas on both local and regional scales. At the ordinal level, harvestmen are ubiquitous and can be found in all continents except Antarctica, from the equator up to high latitudes (see Chapter 7). We can find them in a great variety of habitats in all terrestrial ecosystems, including in soil, moss, and leaf litter, under rocks, stones, and debris, on vertical surfaces from tree trunks to stone walls, among grassy clumps, and running over high vegetation. The most diverse harvestman communities, however, are reported for tropical areas, especially rain forests. Although some species are widely distributed and can be found in a wide range of habitats, many harvestman species are much more limited in geographic distribution and habitat use, especially in tropical areas. Some species are restricted to caves, and others occur in very specific microhabitats, such as nests of leaf-cutter ants. The influence of physical factors on the spatial distribution of harvestmen has been poorly studied, but temperature and humidity seem to be the most important determinants of their distribution and habitat use. Despite the capacity of maintaining internal homeostasis, there is strong evidence that many harvestman species are inefficient in avoiding water loss. Some morphological and physiological features of the order, such as a large surface/volume ratio, lack of spiracular control, and low osmotic hemolymph concentration, may partially explain why most species are found in damp and shaded areas (see Chapter 14). Phenological patterns present marked variation among species (or even populations of the same species), and few could be regarded as nonseasonal (see Chapter 7). While most representatives of the suborders Cyphophthalmi and Laniatores are active during the whole year, generally with monthly fluctuations in population size, the occurrence of adult individuals in representatives of the suborders Eupnoi and Dyspnoi is usually restricted to a few months of the year. As seen earlier, many harvestman common names in European countries indeed make reference to the phenology of the most common species, wherein the occurrence of adults and the mating season coincides with the harvest period, that is, spring and summer. In temperate regions some annual species overwinter as nymphs from eggs hatched in the fall, or as eggs laid by adults hatched in the spring. The number of nymphal stages varies among different species, ranging from four to eight, but usually six (see Chapter 13).

What Are Harvestmen?

Most harvestman species have an omnivorous diet that includes small, softskinned arthropods and other invertebrates, as well as carrion, plants, and fungi (see Chapter 8). This broad alimentary spectrum may be considered a unique feature among arachnids, which are generally viewed as exclusive predators of invertebrates (mainly arthropods) and small vertebrates. There are a few species that specialize almost exclusively in terrestrial snails and slugs and thus have the common name Schneckenkanker, which means “snail harvestman” in German. In order to find food, most harvestman species seem to rely on an ambush strategy or, more rarely, on active hunting. Periods of waiting are generally intercalated with periods of slow movement in which the individuals, which are unable to form images and probably can only distinguish light from dark, explore their environment using the tips of their second pair of sensorial legs. This particular feature of harvestman biology inspired their popular name in Japan, zatomushi; zato is an ancient word used to designate the players of the biwa, a traditional Japanese stringed instrument that was generally played by blind people, and mushi means “bug.” Therefore, the name associates the walking behavior of harvestmen, with their long second pair of legs stretching ahead like arms, with a blind person fumbling along his way with a walking stick. Unlike most arachnids, harvestmen do not have a pumping stomach to suck the liquefied tissues of their prey, and they masticate their food by ingesting small particles (see Chapter 2). Therefore, they are exposed to parasites and pathogens that otherwise would be filtered out by the feeding mechanism, as occurs in the other arachnids (see Chapter 9). Gregarines are particularly abundant in harvestmen but are uncommon in other arachnids, such as spiders. Additionally, the omnivorous feeding habits of many harvestmen place them in close proximity to contaminated materials, which may result in contact with pathogens or infective stages of some parasites. These are not the only natural enemies of harvestmen; a compilation of the literature clearly shows that the most diverse group of harvestman predators is that of passerine birds (see Chapter 9). Frogs and toads, insectivorous mammals, and spiders are other important groups of predators. To deal with this diversified range of natural enemies, harvestmen have developed a great variety of defensive strategies (see Chapter 10). Some species, for instance, camouflage themselves with debris glued on by a secretion from the integument, and very frequently they respond to predator attacks by feigning death, a defensive behavior known as thanatosis (after the Greek god of death, Thanatos). If disturbed, many long-legged species rapidly vibrate the body, a defensive behavior known as “bobbing” that probably confuses the identification and exact location of the harvestman’s body. Because of this last defense mechanism, in some places of southeastern Brazil the long-legged harvestman species are called aranhas-bailarinas, and in Costa Rica they are known as pendejos (Table 1.1). As we have seen earlier, many common names attributed to harvestmen around the world are related to the bad smell of their scent glands and to their leg movements after they are shed. These two defensive strategies are so conspicuous that they have even attracted the attention of nonexperts in the group, such as the fa-

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What Are Harvestmen?

mous Spanish painter Salvador Dalí, whose interest in bizarre animals is quite evident in his works. In his 1940 painting Daddy Longlegs of the Evening—Hope! Dalí carefully illustrated two common defense strategies in Opiliones (Figure 1.3). The harvestman, clearly a representative of the suborder Eupnoi, occupies a central position in the painting and has lost one of its legs, a defensive strategy known as autospasy (see Chapter 10). Moreover, the individual is surrounded by a swarm of ants that fail to contact the harvestman’s legs, probably because of the action of scentgland secretions, which are known to be a highly effective repellent against these insects. Although the atmosphere of the painting is bleak, the harvestman is a reference to an old French peasant legend that says that the sighting of a harvestman in

Figure 1.3. The painting Daddy Longlegs of the Evening—Hope! (1940, oil on canvas, 10 × 20 inches) by Salvador Dalí, which is an allusion to World War II. A grieving cupid appears in the lower left of the painting, tormented because the world is violently changing. In the center of the painting is the daddy longlegs, which, according to an old French legend, is a symbol of good luck. Thus, in spite of the bleak atmosphere of the painting, Dalí offers hope. Reproduced from Collection of Salvador Dalí Museum, St. Petersburg, Florida; ©2006 Gala–Salvador Dalí Fundation, Figueres (Artists Rights Society, New York); ©2006 Salvador Dalí Museum Inc.

What Are Harvestmen?

the evening hours is a good omen, a portent of good luck, and a symbol of hope. Interestingly, the harvestman’s common name in Turkish (müjdeci or mücdeci) suggests a similar symbolism, since it means a person who brings good news (Table 1.1). Unlike other arachnid groups, many species of Opiliones seem to be highly tolerant of conspecifics. Several species form dense diurnal aggregations consisting mainly of subadults and adults of both sexes (see Chapter 11). In general, individuals aggregate at protected sites and close to a water source. The number of individuals in these groups ranges from 3 to nearly 200 among the Laniatores, but among the Eupnoi there are records of mass aggregations containing more than 70,000 individuals. One of their common names in the United States, “grandfather-graybeard,” is probably related to these huge aggregations since individuals are facing upward and their long legs are hanging down, resembling a beard or wig. Although gregariousness in harvestmen seems to be primarily induced by environmental factors, this behavior may confer several defensive advantages, including strengthening of defensive signals through the collective release of scent-gland secretions, speeding the response to alarm signals provided by the scent secretion, and decreasing each individual’s chances of being eaten (dilution effect). The great majority of harvestmen reproduce sexually, although some species reproduce asexually by parthenogenesis, and the sex chromosomes have been identified as usually XY-XX (see Chapter 6). As we saw earlier, harvestmen may have been the first group of arthropods to evolve an intromittent organ, this being another unique morphological feature of the order among arachnids. However, the study of mating strategies is probably the aspect of their behavior that has received the least attention. Harvestman fertilization is internal, and the transfer of spermatozoa may occur indirectly through spermatophores (in Cyphophthalmi) or directly by means of long and fully intromittent male genitalia in the other suborders (see Chapter 12). Unlike courtship in other arachnids—a process in which males must first “persuade” the female not to consider them as prey and that may require a careful approach and a long-distance, elaborated, highly stereotyped, and species-specific visual or vibratory set of displays—courtship before intromission is often quick and tactile in harvestmen. In some cases, however, males may offer a glandular secretion of their chelicerae before copulation as a nuptial gift for their mates. Many studies also mention intense courtship during intromission and mate guarding after copulation. Additionally, males of many species defend territories, which are used by females as oviposition sites. Given the amazing complexity of the male genitalia and the enormous diversity of types of sexual dimorphism, sexual selection (be it intraor intersexual) has probably played a major role in the evolution of harvestmen. Females may lay their eggs immediately or months after copulation, and the eggs may take from 20 days to more than five months to hatch (see Chapter 13). The forms of parental care may include the production of large yolky eggs, the preparation of nests, the choice of appropriate oviposition sites, and parental care (see Chapter 12). Although maternal care is widespread among arachnids, harvestmen are the only order in which some species present exclusive paternal care, the rarest form of parental investment among arthropods. Both maternal and paternal care

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have been demonstrated to play a crucial role in egg survival, preventing predation and fungi attack. However, the selective forces leading to the evolution of these two forms of parental assistance seem to be very different. Since the great majority of maternal harvestmen are restricted to a single reproductive event during the breeding season, females can achieve greater reproductive success by remaining close to their hatchlings throughout the caring period. Thus maternal care is likely to have evolved as a result of natural selection. In contrast, male care in harvestmen seems to have evolved as a result of sexual selection. According to recent studies, males that provide paternal care are preferred by females and obtain a greater number of copulations than males that are unable and/or unwilling to provide care. Although harvestmen are a fascinating group of arachnids, the dramatic increase in environmental disturbance around the world—especially in tropical regions—may have driven many species to extinction even before their formal description by taxonomists. Many human activities, including pesticide use, forestry operations, air and soil pollution, fire, and even the introduction of domestic animals, have tremendous impacts on the habitats on which harvestmen are dependent (see Chapter 7). Most harvestman species have restricted distributions and can be particularly endangered if human activities unfavorably alter their habitats. This is the case for most cave dwellers, which may be driven to local or complete extinction if the cavernicolous habitat or the nearby external environment is severely disturbed. In fact, almost all harvestman species formally considered endangered around the world are cave dwellers, although many other species living in other habitats may be equally endangered. However, given the paucity of ecological information for the great majority of harvestman species, it is almost impossible to reliably report on their conservation status. Therefore, the preservation of habitats instead of particular species may be the most effective means to protect the diversity of Opiliones around the world. Given their geographic distribution and species richness, it is surprising that harvestmen have remained largely ignored by the general public and zoologists as well. Their behavior and ecology are just beginning to be understood, and in the last two decades the number of studies published on these subjects has increased considerably, especially in South America (Figure 1.1b). Populations of many species are locally abundant, and individuals are easy to observe. Chapter 15 provides an overview of the methods and techniques used to study harvestman biology both in the field and in the laboratory. There you will learn how to collect specimens for ecological sampling, prepare material for cytogenetic studies, preserve pathogens and parasites of harvestmen, and conduct taxonomical and systematic studies. Moreover, you will discover that representatives of the order may be easily maintained in captivity, where they behave in a similar way to that observed in the field. In conclusion, harvestmen are perfect subjects for ecological, behavioral, and evolutionary studies, and we truly expect the reader—whether an amateur or a professional—to find the book a useful tool for progressing in the understanding of the fascinating biology of harvestmen.

What Are Harvestmen?

ACKNOWLEDGMENTS We are grateful to those who helped with popular harvestman names: Astri Leroy and Adriano B. Kury (Afrikaans), Christian Lexer and Edith Karpinos (German), Gabriela Lysakova (Czech), Gilbert Barrantes (Spanish—Costa Rica), Grace Young Kim (Korean), Joanna Znaniecka (Polish), Laszlo Csiba (Hungarian), Luc Vanhercke (Dutch), Luis E. Acosta (Spanish—Argentina), Luis Inda (Spanish—Spain), Marcela Van Loo (Slovakian), Michael Fay (Welsh), Niklas Wahlberg (Finnish and Swedish), Nobuo Tsurusaki (Japanese), Plamen Mitov (Russian), Shan Luan (Chinese), Søren Toft and Theo Blick (Danish and Norwegian), Tone Novak (Slovenian), Ümit Kebapci (Turkish), Wojciech Starega (German, Polish, and Ukrainian), and Samantha Koehler, who helped us contact most of these people. Ron Clouse kindly revised this chapter. We are deeply indebted to Bruno A. Buzatto for helping assemble the literature for Figure 1.1b, to Joan R. Kropf and Carol Butler for giving us permission to reproduce the painting Daddy Longlegs of the Evening—Hope! and the following colleagues for providing the photos in Figure 1.2: Adriano B. Kury, Ann Bochonowski, Nikolaj Scharff, Nobuo Tsurusaki, Peter Jäger, and Zandile Mbhele.

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Morphology and Functional Anatomy Jeffrey W. Shultz and Ricardo Pinto-da-Rocha

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orphological research on harvestmen and other organisms accelerated in the decades after publication of Charles Darwin’s On the Origin of Species as biologists attempted to reconstruct the tree of life and, in so doing, laid the foundations of modern evolutionary morphology. In fact, several studies from the late nineteenth and early twentieth centuries remain the only original sources for information on some aspects of harvestman biology. Basic conclusions from Purcell’s (1894) study of retinal structure were considered definitive until the electron microscopic studies of the 1970s (especially Schliwa, 1979), and de Graaf ’s (1882) study of the reproductive system, with its beautiful color illustrations, is still unsurpassed in detail. In a seminal treatise Hansen and Sørensen (1904) presented original work on Opiliones and reviewed the anatomical research of the nineteenth century. They set a high standard for the comparative morphology of harvestmen, using thorough but economical descriptions and consciously avoiding the speculative “theorizing” that was then threatening to undermine the scientific legitimacy of comparative biology (Bowler, 1996). Europe remained the principal site for research on harvestman morphology throughout the twentieth century. During the 1920s the German zoologist Alfred Kästner emerged as the leading student of opilionology and arachnology in general (Savory, 1961). He synthesized information on all aspects of harvestman biology (Kästner, 1926, 1935a, 1968) and contributed original work on the mouthparts (1931b), digestive and respiratory systems (1933), coxal organs, nephrocytes, and perineural organs (1934), and midgut diverticula (1935b). Later Moritz (1957, 1959) published important descriptive studies of embryogenesis. In France, Millot’s (1926, 1949) comparative histophysiological research inspired a decades-long se14

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ries of studies on arachnids, including harvestmen. Juberthie’s (1964) treatise contains a wealth of information on harvestman morphology, including development, teratology, eye structure, and neuroendocrine systems. Through much of the second half of the century, Juberthie and colleagues continued to add important insights; contributions by Muñoz-Cuevas (1981) on the structure and evolution of the visual system are particularly notable. Extensive phylogenetic surveys of specific organ systems began to appear in the last decades of the twentieth century, perhaps inspired by innovations in phylogenetic methods. Martens and coworkers (Hoheisel, 1980; Martens, 1980, 1986; Martens et al., 1981) surveyed the ovipositor/penis complex throughout the order, and Dumitrescu (1974–1980) made extensive comparisons of midgut diverticula. Comparative morphological research on Opiliones has declined in recent years, an unfortunate trend that this book may help reverse. Much more is known about the external structure of harvestmen than about internal structure because of the predilection of arthropod systematists for cuticular taxonomic characters. Studies of internal structure have often been undertaken with a different purpose in mind. Here, individual species were subjected to intensive study, with findings extrapolated to all Opiliones or even more inclusive groups (e.g., Schliwa, 1979; Becker & Peters, 1985a,b; Dannhorn & Seitz, 1986, 1987; Breidbach & Wegerhoff, 1993). This exemplar or “model organism” approach is more typical of comparative and experimental physiology than the comparative, descriptive approach of systematists. Interestingly, the exemplar chosen was usually the phalangiid Phalangium opilio (Figure 2.1e), a highly visible, anthrophilic species common in countries with long traditions of academic research. For over a century studies on P. opilio have accumulated in diverse journals in many languages. But it was not until the advent of electronic bibliographic databases that one could take full measure of the volume of this work and conclude that P. opilio is actually one of the better-studied arthropods. It stands to reason that much of what is presented here about the internal anatomy and physiology of harvestmen centers on this one species.

PHYLOGENETIC DIVERSITY OF OPILIONES The order Opiliones encompasses about 6,000 described species, making it the thirdlargest arachnid order after Acari (ca. 48,000 spp.) and Araneae (ca. 39,000 spp.). The order is traditionally regarded as a close relative of mites (e.g., Weygoldt & Paulus, 1979), largely because of superficial similarities, such as compact bodies. Recent work places harvestmen near Scorpiones, Pseudoscorpiones, and Solifugae or as the sister group to Scorpiones alone, a view based primarily on similarities of the appendages and mouthparts (see Chapter 3). The two main lineages within Opiliones are Cyphophthalmi (Figures 2.1a, 2.2a–c), which are generally small, shortlegged, heavily sclerotized inhabitants of soil and caves, and Phalangida, which is much more diverse in species, morphology and ecology and includes the familiar long-legged harvestmen (see details in Chapter 3). The Phalangida are divided into

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Figure 2.1. Harvestman diversity. (a) Cyphophthalmi: Pettalus cf. brevicauda (Pettalidae) (photo: G. Giribet). (b) Dyspnoi: Trogulus tingiformis (Trogulidae) (photo: C. Komposch). (c) Dyspnoi: Ischyropsalis kollari (Ischyropsalididae) (photo: C. Komposch). (d) Eupnoi: Caddo agilis (Caddidae) (photo: J. G. Warfel).(e) Eupnoi: Phalangium opilio (Phalangiidae) (photo: J. Shultz). (f) Laniatores: Roeweria virescens (Gonyleptidae) fluorescing under ultraviolet light (photo: J. Silva). (g) Laniatores: unidentified cosmetid (photo: R. Pinto-da-Rocha). (h) Laniatores: Sphaerobunus fulvigranulatus (Gonyleptidae), ventral, showing the everted penis (photo: R. Pintoda-Rocha).

Morphology and Functional Anatomy

Figure 2.2. Dorsal, ventral, and lateral views of representative harvestmen (photos: R. Pinto-da-Rocha). (a–c) Cyphophthalmi: Metasiro americanus (Neogoveidae). (d–f) Eupnoi: (d,f) Jussara flamengo and (e) J. rosea (Sclerosomatidae). (g–i) Dyspnoi: Nemastoma lugubre (Nemastomatidae). (j–l) Laniatores: (j) Eusarcus sp., (l) Discocyrtoides nigricans and (k) Pseudogyndesoides sp. (both Gonyleptidae).

three main groups: Laniatores, Dyspnoi, and Eupnoi. Laniatores is a very diverse lineage (Figures 2.1f–h, 2.2j–l), typically with large, spiny pedipalps (Figure 2.7c) and paired or branched claws on legs III–IV (Figures 2.7f,g). Laniatores has two principal groups: Insidiatores and Grassatores. Eupnoi encompasses the superfamilies Phalangioidea (Figures 2.1e, 2.2d–f), which includes the “daddy longlegs” familiar to inhabitants of northern temperate regions, and Caddoidea (Figure 2.1d),

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a small group with prominent eyes and spiny pedipalps. Dyspnoi also has two superfamilies, Ischyropsalidoidea (Figure 2.1c) and Troguloidea (Figures 2.1b, 2.2g– i), which are both morphologically diverse inhabitants of the Northern Hemisphere.

EXTERNAL MORPHOLOGY General body plan Harvestmen have two main body regions or tagmata (Figure 2.2), an anterior prosoma (cephalothorax) and posterior opisthosoma (abdomen), with a broad and sometimes poorly defined juncture. This contrasts with spiders and certain other arachnids in which these tagmata are separated by a distinct constriction or waist. The prosoma bears six pairs of appendages, chelicerae, pedipalps, and four pairs of legs (I to IV). The dorsal plate that covers the prosoma, the carapace, generally has a pair of closely spaced eyes on an elevated mound, the ocularium, and laterally placed openings, named ozopores, of defensive glands. The opisthosoma has 10 somites, none with appendages, with the dorsal sclerite of the last forming an anal operculum. The openings to the respiratory tract are located on the second opisthosomal somite just behind the last pair of legs. The genital opening is also located ventrally on the second opisthosomal somite, but is shifted anteriorly relative to the dorsal parts and lies between the last pair of legs. The body is compact and varies in shape more than in most other arachnid groups (Figures 2.1, 2.2).

Integument The cuticle has two main layers, an inner endocuticle and an outer exocuticle. The endocuticle is more pliable and is the principal component of articular “membranes” associated with joints and bases of movable setae. The exocuticle varies considerably, from thin and leathery in many Eupnoi and Dyspnoi to thick and hard in the Cyphophthalmi and Laniatores. The cuticular surface is remarkably diverse in Opiliones (Figures 2.2, 2.3), perhaps more so than in any other arachnid order (Martens, 1978a). Macrosculptural features include apophyses, spines, tubercles, denticles, and all manner of cuticular excrescences, as well as depressions, striae, and sulci. This diversity extends to the microsculptural scale. Murphree (1988) conducted a scanning electron microscope (SEM) survey of the integument in a diverse sample of harvestmen and provided a classification of microsculptural features. In some cases cuticular sculpturing is used in stridulation, that is, the production of substrate- or airborne vibrations by moving one body part across another. Stridulatory structures (e.g., Figure 2.3d) are known to occur on the prolateral surfaces of the basal cheliceral segments (several nemastomatids) and on the middle cheliceral segments, as in several Laniatores (Martens, 1978a; Pinto-da-Rocha & Kury, 2003b). The pedipalpal femur is moved against the denticles of the ocularium

Morphology and Functional Anatomy

Figure 2.3. Integumentary structures. (a–b) Eupnoi: (a) Jussara rosea (Sclerosomatidae), chelicera showing slit sensilla; (b) Leiobunum calcar (Sclerosomatidae), glans penis showing campaniform sensilla. (c–d) Laniatores: (c) Pseudogyndesoides sp. (Gonyleptidae), basitarsus showing tuberculate astragalus and setose calcaneus; (d) Pseudopachylus longipes (Gonyleptidae), chelicera showing stridulatory file. (e) Cyphophthalmi: Metasiro americanus (Neogoveidae), ventral view of anal region. (f) Laniatores: Sodreana sodreana (Gonyleptidae), leg, metatarsus showing smooth astragalus and setose calcaneus. (g) J. rosea, articulation between metatarsus and tarsus. (h–i) Dyspnoi: (h) Nemastoma lugubre (Nemastomatidae), leg III, metatarsus/tarsus, sensilla trichodea (short, recumbent setae) and sensilla chaetica (long, erect setae); (i) N. lugubre, pedipalp, glandular clavate setae. (j) J. rosea, genital operculum showing cuticular features.

in several nemastomatids and against the basal cheliceral segment in Ceratolasma (Ceratolasmatidae) (Martens, 1978a). The integument can also be modified for soil crypsis. Trogulids, dicranolasmatids, nemastomatids (J. Martens, pers. comm.), and several other groups have glands that produce an adhesive secretion that attaches soil and other debris to the body for camouflage (see Chapter 10).

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In some species the integument fluoresces under ultraviolet light (wavelength 350–360 nm; Acosta, 1983), as can white and yellow spots or stripes in other species (Figure 2.1f). However, the intensity of fluorescence is not as great as in scorpions. The function of fluorescence, if any, is unknown.

Setae. Setae are hairlike projections of the cuticle, typically with a basal articulation (Figure 2.3). Macrosetae, or articulating “spines,” are large and tend to be scattered rather than clumped. Microsetae are short, narrow setae and frequently occur in large clusters, as at the tip of the pedipalp or legs. Many Eupnoi and Dyspnoi have setae with fine projections along their shafts. These are called plumose or pinnate setae and occur primarily on the pedipalps. In some groups, especially Dyspnoi, the setal projections are concentrated at the tip, giving the seta a clavate (clublike) appearance (Figure 2.3i). Clavate setae are associated with glands, and the secretions pass through fine ducts within the setal shaft and exit through pores at the setal tip (Wachmann, 1970). The secretion is probably an adhesive used in prey capture (see Chapter 8). Those setae with one or more basal sensory neurons are trichoid sensilla and may be specialized for detecting mechanical displacements or chemicals. Harvestmen have two main types of mechanosensory setae, sensilla trichodea and sensilla chaetica (G. S. Spicer, 1987; Guffey et al., 2000; Willemart & Gnaspini, 2004b), and these occur in other arachnids as well (Foelix, 1985). Sensilla trichodea are differentiated by their sharper tips, lower attachment angle, and greater length (Figure 2.3h). They also lack an articulating membrane, but this may be unique to harvestmen. Sensilla chaetica have blunter tips, steeper attachment angles, and shorter length (Figure 2.3h). Certain sensilla chaetica have characteristics of contact chemoreceptors (i.e., terminal pore, whorled striae), but this function has not been verified by ultrastructural or electrophysiological analyses. In general, these sensilla are concentrated at the terminal segments of the pedipalps and legs. Many arachnids also have trichobothria, which are long sensory setae that attach within a cuplike socket and detect air movements (Reissland & Görner, 1985), but these are absent in harvestmen and certain other arachnids (e.g., Ricinulei and Solifugae). Slit and campaniform sensilla. Harvestmen have two kinds of cuticular strain receptors, slit sensilla (lyrifissures) and campaniform sensilla. Slit sensilla appear as small slits in the cuticle (Figure 2.3a), and their associated sensory neurons respond most intensely to strains acting perpendicular to the long axis of the slit (Barth, 1985). They are found in all arachnids except Palpigradi (Shultz, 1990). They occur singly or in groups and are most numerous on basal segments of legs, pedipalps, and chelicerae, often proximally adjacent to articulations. The slit sensilla of harvestmen differ from those of other arachnids in several respects. First, there are relatively few sensilla per leg. Barth and Stagl (1976) counted 45 slit sensilla on the leg of the phalangiid Amilenus (none distal to the femur), compared with 74 in a scorpion, 128 in a whip scorpion, and 325 in a spider, which were distributed on all or most leg segments. Second, the long axes of slit sensilla tend to be oriented perpendicular to the

Morphology and Functional Anatomy

long axis of the leg in harvestmen, while those of other arachnids tend to be oriented parallel to the leg’s axis. Third, while harvestmen have groups of parallel slit sensilla (Figure 2.3a), they are said to lack true lyriform organs (i.e., groups of closely spaced, < 30 ␮m, slit sensilla), which are especially abundant in spiders. Still, the distinction between groups of slit sensilla and lyriform organs is arbitrary (Barth & Stagl, 1976), and there has been no survey of Opiliones with the 30-␮m criterion in mind. Exact functions of slit sensilla in harvestmen have not been determined, but comparisons with other arachnids suggest that they measure strains associated with self-generated movement (proprioception) and the detection of vibrations or other strains imposed by external sources (exteroception). Campaniform sensilla are circular or oval (Figure 2.3b) and are probably functionally similar to slit sensilla, if not simply modified versions of them. Edgar (1963) examined the number and distribution of slit and campaniform sensilla on all legs distal to the coxa in six species of harvestmen: the caddid Caddo agilis, the phalangiids Opilio parietinus and Phalangium opilio, and three sclerosomatids of the genus Leiobunum. He found sensilla on all leg segments, with concentrations near the plane of appendotomy. The number of sensilla per leg ranged from 9 to 13 in C. agilis to 69 to 75 in P. opilio. The antenniform leg II had no more sensilla than the other legs despite its specialization as a sensory organ. Given these results and the possible homology of slit and campaniform sensilla, a comparative study of cuticular strain sensilla in Opiliones seems warranted.

Dorsal sclerites Harvestmen probably descended from arachnid ancestors in which the dorsal surface was covered by an undivided prosomal carapace and a series of free opisthosomal tergites, a condition retained in many arachnid groups. However, dorsal sclerotization in most harvestmen has changed considerably from the primitive condition. In many Eupnoi and Dyspnoi, the carapace often shows evidence of the underlying prosomal segmentation (Figures 2.1e, 2.2d,f, 2.4d). The tergal elements of somites I–IV form a region called the propeltidium, which is sometimes separated by transverse grooves from the apparent tergite of somite V, the mesopeltidium. The mesopeltidium may, in turn, be separated from the tergite of somite VI, the metapeltidium, by a groove or soft cuticle. In some cases the pro- and mesopeltidia are fused, and only the metapeltidium is differentiated (Figure 2.4d). The pro-, meso-, and metapeltidia also occur in other arachnid groups, notably pseudoscorpions, schizomids, and palpigrades. The dorsal opisthosomal surface of harvestmen has even greater variation, and the more common patterns of sclerotization have been named (Martens, 1978a). A scutum completum is formed by consolidation of the carapace and the first eight opisthosomal tergites, as in Cyphophthalmi (Figures 2.1a, 2.2a,c, 2.4a) and Laniatores of the family Oncopodidae (see Chapter 4). It has been suggested that this is the primitive condition for Opiliones, but this hypothesis is inconsistent with outgroup comparison and with the retention of primitive dorsal longitudinal muscles in

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a

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c

d

Figure 2.4. Patterns of dorsal sclerotization. (a) Scutum completum, fusion of carapace and opisthosomal tergites 1–8. (b) Scutum magnum, fusion of carapace and opisthosomal tergites 1–5. (c) Scutum laminatum, carapace and opisthosomal tergites free. (d) Scutum parvum, carapace free, opisthosomal tergites 1–5 fused. Redrawn from Martens (1978a).

higher Opiliones (Figure 2.9d). In a scutum magnum the carapace and the first five opisthosomal tergites are consolidated, as in most Laniatores (Figures 2.1f–h, 2.2j,l, 2.4b) and many troguloids (Figures 2.2g,i, 2.4b). A scutum laminatum is similar to the condition of other arachnids in that the carapace and all opisthosomal tergites are free; this occurs in some ischyropsalidids of the genus Ischyropsalis (Figure 2.4c) and many sabaconids. In a scutum parvum the first five opisthosomal tergites are fused together and free from the carapace; this occurs in most Ischyropsalididae, Phalangioidea (Figures 2.1e, 2.2f, 2.4d), Sabaconidae, and ortholasmatine Nemastomatidae. Note that this nomenclature is not exhaustive and acknowledges recurring structural patterns; it is not a system for establishing homologies.

Prosoma Dorsal structures. The dorsal surface of the prosoma is covered by a sclerotized carapace formed by consolidation of the tergites of six appendage-bearing somites (Figures 2.2a,d,g,j). As noted earlier, the carapace may be uniform or show differentiation of the posterior two somites. The carapace may have spines, especially on the anterior margin, but its most prominent features are typically the eyes and ozopores. Harvestmen typically have a pair of simple eyes placed on an ocularium (ocular tubercle or eye mound) that is usually placed near the middle of the carapace (Figure 2.2). However, the ocularium can be near to or project over the anterior margin of the carapace, or, in a few cases, the eyes may be separated and positioned more laterally. The ocularium can occupy much of the carapace, as in caddoids (Figure 2.1d). The ocularium is usually dome shaped or globose and may be smooth or with small or large spines. In some Dyspnoi, including trogulids (Figure 2.1b) and dicranolasmatids, the eyes are located on projections that form a hood covering the mouthparts. Eyes are reduced or absent in many cave- or soil-dwelling species, including most Cyphophthalmi (Figures 2.2a,c). The openings to the defensive

Morphology and Functional Anatomy

glands, or ozopores, are located on the lateral portion of the prosoma, either on the carapace or in the supracoxal pleural region, at the level of the coxae of legs I–II. They open on the tip of an elevated cone (ozophore) in Cyphophthalmi (Figures 2.1a, 2.2a,c, 2.10e), but are sessile in most other taxa. Ozopores and defensive behavior are discussed in detail in Chapter 10.

Ventral structures. The ventral prosomal surface comprises the pedal coxae, the feeding apparatus (stomotheca), and the intercoxal sternal region. Coxae. The pedal coxae occupy most of the ventral surface area (Figures 2.2b,e,h,k). The coxae of leg I retain some degree of mobility associated with their role in the feeding apparatus. However, there is a strong trend toward immobilization of the other pedal coxae. The coxae of legs II–IV are immobile in some Cyphophthalmi, in Laniatores, and in some Dyspnoi, especially those that are heavily sclerotized and live in the soil. Other taxa retain coxal mobility in all legs (e.g., Eupnoi). The retention of a primitive configuration of extrinsic leg muscles in Eupnoi (Shultz, 1991, 2000) suggests that coxal mobility has been lost repeatedly in Opiliones and that fused coxae are not primitive for the order. Stomotheca. The term stomotheca has been applied to the preoral apparatus of harvestmen (Thorell, 1882; Hansen & Sørensen, 1904) and sometimes scorpions (Shultz, 2000). It is unique in being formed by extensions from the pedipalps and the first pair of legs. Important comparative studies of the stomotheca have been conducted by Pocock (1902b), Hansen and Sørensen (1904), Kästner (1931b, 1933), Snodgrass (1948), Martens (1978a), and van der Hammen (1985). The stomotheca in harvestmen usually consists of six elements, the epistome (labrum), two pairs of coxapophyses (endites, maxillary lobes), and a labium (Figures 2.5c,d, 2.9a). The epistome is a projection that forms the anterior wall of the stomotheca. Its dorsal surface is sclerotized and divided by a transverse invagination or sulcus (Figure 2.9a). Some workers call the part proximal to the groove the clypeus and the distal part the labrum, but the homologies implied by these are not strictly correct (Shultz, 2000). The ventral epistomal surface is constructed from soft, flexible cuticle and often has a distal lobe. The lateral epistomal walls are fused to the medial surfaces of the pedipalpal coxae, and a transverse muscle attaches to the inner surfaces of the epistomal walls (Figure 2.9a). Contraction of this muscle probably pulls the pedipalpal coxae together, and the transverse sulcus may serve to strengthen the epistome against total compression. The epistomal walls also have muscles that dilate the preoral chamber and pharynx (Figures 2.9a–c). The walls project ventroposteriorly into the prosomal space as epistomal arms, which lie on either side of the pharynx, as in Cyphophthalmi, or encircle the pharynx, as in Phalangida (Figure 2.9b). The latter arrangement apparently allows the dilator muscles to expand the pharyngeal lumen circumferentially for ingestion and passage of solid food, an ability that is otherwise rare among arachnids. Coxapophyses are extensions (apophyses) from the coxae of the pedipalps and first leg pair (Figures 2.5b–d, 2.9a). They are sclerotized basally (there may be one or two basal sclerites in leg I), but terminate in large, soft pads that function as “lips.” In

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Figure 2.5. Ventral structures (photos: R. Pinto-da-Rocha). (a) Cyphophthalmi: Metasiro americanus (Neogoveidae). Note absence of genital operculum and intercoxal sternites. (b) Laniatores: Pseudogyndesoides sp. (Gonyleptidae). (c) Dyspnoi: Nemastoma lugubre (Nemastomatidae). (d) Eupnoi: Jussara rosea (Sclerosomatidae). Abbreviations: ch, chelicera; cp1, cp2, coxapophyses of legs I and II; cpp, coxapophysis of pedipalp; cx1–4, coxa of legs I–IV; ep, epistome; g, gonostome; go, genital operculum; lb, labium; pp, pedipalp; st, sternite.

some taxa the posterior surface of the pedipalpal coxapophysis has a narrow sclerotized canal or gutter, the pseudotrachea, which leads to the pharynx (Kästner, 1933; Snodgrass, 1948). Its function is unknown, but it may conduct water and other fluids into the digestive tract. Salivary glands are present within both pairs of coxapophyses (Dumitrescu, 1975b) and empty into the preoral chamber. The coxae of leg II typically have coxapophyses, as well, but they do not end in padlike structures and are not technically part of the stomotheca. In taxa where these coxapophyses are large and movable (Figures 2.5c, 2.9a), they appear to have an auxiliary function in feeding, but they are reduced (Figure 2.5b) or absent in many groups. Small coxapophyses or similar cuticular lobes may be associated with legs III–IV, as well, but their function is unclear. The posterior wall of the chamber is often formed by a labium (Figures 2.5b–d, 2.9a), a sternite derived from the somite of the first walking leg (Winkler, 1957). It is located behind or between the

Morphology and Functional Anatomy

coxapophyses of leg I. It is a large, flattened plate in many Eupnoi and Dyspnoi, but is small in most Laniatores (Figure 2.5b) and absent in Cyphophthalmi. Intercoxal sternal region. The ventral surface of the prosoma posterior to the stomotheca can be divided into two regions, an anterior intercoxal sternal region and a posterior arculi genitales (Hansen & Sørensen, 1904). The intercoxal sternal region does not appear to be a distinct sclerite or sternite but is merely the space between the coxae that takes on different sizes and varying degrees of sclerotization in different groups. The sternal region is attached to coxae II–III by flexible cuticle in most Eupnoi and ischyropsalidoid Dyspnoi, but is narrow and sclerotized in most Laniatores (Figure 2.5b) and broad and sclerotized in many troguloid Dyspnoi. The coxae meet in the midline and obliterate the sternite in some Cyphophthalmi, but a sternite is present in others (Figure 2.5a). The arculi genitales form the dorsoanterior margin of the pregenital chamber (Figure 2.9a) and probably correspond to the sternite of the first opisthosomal somite. Incorporation of this region as a functional component of the “prosoma” is typical of arachnids. A distinction between the sternal region and arculi genitales is not always apparent.

Opisthosoma The opisthosoma has 10 somites (Hansen & Sørensen, 1904) corresponding to postoral somites VII–XVI. However, the last tergite, or anal operculum, lacks a corresponding sternite and is thus comparable to the “telson” of certain other chelicerates, such as horseshoe crabs, scorpions, and whip scorpions. Shultz (2000) has suggested that the harvestman opisthosoma may comprise nine somites and that the anal operculum is a telson. An opisthosoma with 12 or 13 somites is probably the primitive condition in Arachnida (Shultz, 1990). Variation in the segmental pattern of dorsal sclerotization in the opisthosoma was described earlier (see “Dorsal sclerites”). The anterior ventral surface has undergone significant evolutionary modifications. The gonopore is associated with the second opisthosomal somite in all arachnids, but this region is displaced anteriorly between coxae IV in Opiliones such that it appears to be part of the prosoma (Figures 2.2b,e,h,k, 2.9a). Consequently, the margins of sternites and tergites of a somite do not necessarily occur in the same vertical plane. The sternite of the first opisthosomal somite (arculi genitales) is reduced (Hansen & Sørensen, 1904; Winkler, 1957; Figure 2.9a) and forms the anterior margin of the pregenital chamber, within which the ovipositor or penis is withdrawn (Figures 2.9a, 2.16). The pregenital orifice is open in Cyphophthalmi (Figures 2.2b, 2.5a), but is covered by an anterior extension of the second opisthosomal sternite, the genital operculum, in Phalangida. The genital operculum may be a small, semicircular articulated lid, as in Laniatores (Figures 2.2k, 2.5b), or a broad, oblong plate (Figures 2.2e,h, 2.5c,d). The second opisthosomal somite also bears the paired openings to the respiratory system, the spiracles (or stigmata). Each spiracle is located on the lateral surface of the sternite, either on the ventral surface (Figures 2.2b,k) or hidden within a fold between the sternite and coxa IV. Details of spiracular structure are discussed in the section on the respiratory system.

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The arrangement of tergites and sternites around the anus is also variable and sometimes provides important systematic characters. The configuration of sclerites ranges from a relatively simple metameric series of sclerites, as in Laniatores, to a nearly concentric arrangement of sclerites (corona analis), as exemplified by trogulids. Because of reductions and divisions of the perianal sclerites, it is sometimes difficult to homologize them with tergites and sternites of specific segments (Hansen & Sørensen, 1904).

APPENDAGES Chelicerae Chelicerae are the principal feeding appendages (Figure 2.6). Each chelicera has three segments, with the middle (II) and distal (III) segments forming fixed and movable fingers of a chela or pincer. The inner margins of the chelal fingers are equipped with a row of teeth (Figures 2.6a,b). In Dyspnoi (Figure 2.6a) the teeth tend to be flattened translucent (diaphanous) blades; a gap is formed when the chela is closed that is probably used for grooming the other appendages. Chelicerae are enlarged in some groups of the Eupnoi, Dyspnoi (Figure 2.1c), and Laniatores. Adult males in Troguloidea (e.g., Nemastomatidae and Sabaconidae) and Ischyropsalidoidea often have a prominent cheliceral gland used in courtship (see Chapter 12). Except for the opening and closing of the chela, cheliceral movements are restricted largely to a sagittal (vertical) plane, but small movements in other directions are possible. The basal article has a tight but flexible connection to the anterolateral surface of the epistome, which serves as a pivot point, often indicated by a blunt protuberance. Cheliceral muscles are known completely in the sclerosomatid Leiobunum (Shultz, 2000) and the pettalid Chileogovea (Figures 2.6c,d). The muscular anatomy is very similar in the two taxa and consistent with incomplete descriptions of others (Loman, 1903b; van der Hammen, 1985). There are four intrinsic muscles. The bicondylar hinge joint between the basal and middle segments is operated by a flexor and an extensor (Figure 2.6d), and the joint between the middle and distal articles (chelal joint) is operated by a large opener and smaller closer. There are two main groups of extrinsic cheliceral muscles, levators and depressors, with most originating along the medial surface of the carapace (Figure 2.6c) and inserting on the proximal margin of the basal segment (Figure 2.6d). One long, thin extrinsic muscle (Figures 2.6c,d) originates on the anterior margin of the carapace, enters the chelicera, and inserts on the proximal margin of the middle segment. Its function is unclear. A comparable muscle has been observed elsewhere only in scorpions (Lankester et al., 1885; Vyas, 1974). Despite having only three segments, chelicerae are serially homologous with the other prosomal appendages, and some arachnologists, notably Vachon (1944–1976), have used developmental and teratological evidence to homologize these segments with three corresponding regions in the pedipalps and legs. Harvestmen have thus far

Morphology and Functional Anatomy

Figure 2.6. Chelicerae (photos: R. Pinto-da-Rocha). (a) Dyspnoi: Nemastoma lugubre (Nemastomatidae). (b) Laniatores: Sodreana sodreana (Gonyleptidae). (c–d) Cyphophthalmi: Chileogovea oedipus (Pettalidae). (c) Anterior dorsal view showing attachment sites of muscles; (d) lateral view of right chelicera showing muscles (opener and closer of chela not shown). 1, extensor muscle; 2, flexor muscle; 3–5, depressor muscles; 6–7, levator muscles; 8, long extrinsic muscle. (e–f) Teratologically fused chelicerae and pedipalps of Odiellus gallicus (Eupnoi: Phalangiidae) showing correspondence between joints of the two appendages. See text for details. Redrawn from Juberthie (1964). Abbreviations: cg, region of male cheliceral gland; chelicera: ch1, proximal segment; ch2, middle segment; ch3, distal segment; pedipalp: cx, coxa; fe, femur; pa, patella; ta, tarsus; ti, tibia; tr, trochanter.

provided the most useful teratological evidence. Specifically, cheliceral and pedipalpal rudiments occasionally fuse but maintain a degree of independence that allows the spatial relationships of segments and joints to be compared. Juberthie (1964) described and illustrated several examples from the phalangiid Odiellus gallicus (Figures 2.6e,f) and concluded that the proximal segment of the chelicera is homologous to the coxa + trochanter of the pedipalp, that the middle segment is homologous to the femur through the tarsus, and that the distal article is homologous to the apotele (i.e., the claw and its modifications). These results are consistent with those derived from developmental and teratological evidence from other arachnids (Vachon, 1976).

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Pedipalps The pedipalps are positioned between the chelicerae and leg I and are composed of six segments, namely, coxa, trochanter, femur, patella, tibia, tarsus, and claw (Figures 2.7a–c). Pedipalps often resemble reduced legs in Cyphophthalmi, as well as many Eupnoi and Dyspnoi (Figures 2.7a,b), and are used as tactile organs or for manipulating food, clasping mates, or prey capture (see Chapters 8 and 12). The pedipalps are typically large, spiny, and raptorial in Laniatores and Caddoidea for use in prey capture (Figure 2.7c; Chapter 8). The coxae are movable and bear a large coxapophysis that is integrated into the preoral chamber (Figure 2.9a). The distal segments are modified in various ways in different groups, with specific features described in other chapters. In general, the cuticular surface may be smooth with a few setae and no specialized macrosculpture, or it may have denticles, large spines, or seta-covered apophyses associated with prey capture. The claw is also highly variable, ranging from large and sicklelike (most Laniatores, Figure 2.7c) to absent (e.g., Nemastomatidae and Sabaconidae; Figure 2.7a). Pedipalpal musculature is similar to that of the legs, which are described in the next section. The coxa-trochanter joint has a transverse bicondylar articulation equipped with levator and depressor muscles, and the trochanter-femur joint has a vertical bicondylar articulation with remotor and promotor muscles. The trochanter-femur joint does not have a mechanism of appendotomy, as occurs in the legs of many Eupnoi. The femur-patella and tibia-tarsus joints have dorsal hinge articulations, and both have only flexor muscles. The patella-tibia joint usually has a dorsal monocondylar articulation; it can undergo flexion and weak promotionremotion movements. The claw, if well developed, is operated by a levator and depressor muscle (Shultz, 1989).

Legs The legs have the same articles as the pedipalps, except that the tarsus is divided into a proximal metatarsus (basitarsus) and distal tarsus (telotarsus, distitarsus). The coxae may be freely movable, as in most Eupnoi and many Dyspnoi, or largely fused together and to the ventral surface of the body, as in Cyphophthalmi and Laniatores (see Ventral structures). The extrinsic leg muscles of Leiobunum, the only harvestman in which these muscles have been thoroughly described (Shultz, 2000), show an arrangement typical of other chelicerates with mobile coxae, such as horseshoe crabs, spiders, and whip scorpions (Shultz, 1991), with most legs having five muscles arising from the carapace and at least four arising from the endosternite. The persistence of an apparently primitive arrangement of extrinsic leg muscles in some taxa and morphological differences among fused coxae in Cyphophthalmi and Laniatores suggest that coxal fusion has occurred multiple times within Opiliones. The pedipalps and legs I–II sometimes have muscles that attach to the endosternite and appear to operate the coxapophyses (Figure 2.9a). The coxa-trochanter joint has a transverse bicondylar articulation and can un-

Morphology and Functional Anatomy

a

b

c

Ti

d M

e r

f a

h g

Cl

Figure 2.7. Pedipalps (a–c) and legs (d–h). (a) Dyspnoi: Nemastoma lugubre (Nemastomatidae). (b) Eupnoi: Jurassa flamengo (Sclerosomatidae). (c) Laniatores: Pseudogyndesoides (Gonyleptidae). (d) Cyphophthalmi: Metasiro americanus (Neogoveidae), male, leg IV, distal to patella. (e) Eupnoi: Jussara rosea (Sclerosomatidae), leg IV, tarsus and claw. (f) Laniatores: Styloleptes conspersus (Gonyleptidae), leg IV, tarsus, claws, tarsal process. (g) Laniatores: Acrogonyleptes unus (Gonyleptidae), leg IV, tarsus, claws, tarsal process. (h) Eupnoi: Leiobunum nigripes (Sclerosomatidae), leg I (oblique retrolateral view) showing examples of muscles. Based on Shultz (1989) (photos: R. Pinto-da-Rocha). Muscles: 1, Cx-Tr levator; 2, Cx-Tr depressor; 3, Tr-Fe remotor; 4, Fe-Pa flexor; 5, Fe-Pa extensor and Pa-Ti remotor-extensor; 6, Pa-Ti promotor/flexor; 7, Pa-Ti remotor-extensor; 8, Ti-Mt flexor; 9, Ta-Cl depressor; 10, Ta-Cl levator. Abbreviations: Cl, claw; Cx, coxa; Fe, femur; Mt, metatarsus; Pa, patella; Ti, tibia; Tr, trochanter; Ta, tarsus.

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dergo large levation-depression movements. The joint is operated by large muscles that originate from the walls of the coxa (Figure 2.7h). The trochanter-femur joint tends to have a vertical bicondylar joint and undergoes primarily promotionremotion. The muscles arise in the trochanter. Because of their proximal location and differing rotational axes, movements occurring at the coxa-trochanter and trochanter-femur joints can translate into substantial and diverse motion at the distal end of the leg. The trochanter-femur joint in many Eupnoi is often specialized for appendotomy, which will be described later. The femur-patella joint is the primary “knee” of the harvestman leg (Figure 2.7h) and is capable of undergoing the greatest range of flexion-extension movement. Flexion is brought about largely by a simple pinnate muscle that inserts on the ventral proximal margin of the patella via a tendon that spans almost the full length of the femur (Figure 2.7h). The extensor muscle has been overlooked by many workers, probably because of its unusual arrangement. It arises proximally from a dorsal femoral process and the dorsal articular membrane of the femur-patella joint, passes distally through the patella without attachment, and inserts on the posterior margin of the tibia. The extensor is absent in Cyphophthalmi and has a modified tibial attachment in those Laniatores examined thus far. Similar muscles occur in scorpions and pseudoscorpions (Shultz, 1989). The patella-tibia joint has a nearly vertical bicondylar articulation; the dorsal condyle tends to be offset toward the anterior surface, and the ventral condyle is offset toward the posterior surface. The joint is operated by two pairs of antagonistic muscles, one pair arising in the patella and one pair arising in the femur. The extensor of the femur-patella joint belongs to the latter. The tibia-tarsus joint has a dorsal hinge articulation throughout the order and undergoes flexion and extension. A well-developed flexor muscle occurs in all taxa examined so far, but there is no extensor (Figure 2.7h). The tendon of the claw depressor passes through the joint. Sensenig and Shultz (2003) examined Leiobunum to assess the contribution of hydraulic pressure and cuticular elasticity to joint extension and found that internal fluid pressure played no significant role. This contrasts with spiders, where pressure plays a dominant role (Blickhan & Barth, 1985; Sensenig & Shultz, 2003). However, when the joint in Leiobunum is flexed and released, it extends spontaneously and returns about 80% of the energy used to produce the initial flexion. This springlike property is caused by transarticular sclerites that are probably composed of resilin, a rubberlike protein found in many arthropods (Wainwright et al., 1976). Elastic sclerites occur at the tibia-tarsus joints of Laniatores, scorpions, and solifuges and the patella-tibia joint only of solifuges (Sensenig & Shultz, 2003, 2004). No elastic sclerites have been observed thus far in Cyphophthalmi. The tarsus is highly variable within the order. It is divided into a proximal metatarsus and distal tarsus (Figures 2.7d–h). The metatarsus is undivided, although articulation-like points of flexibility occur in some long-legged phalangioids. In some groups, especially in Laniatores and troguloid Dyspnoi, the metatarsus has two distinct regions, the proximal astragalus and the distal calcaneus (Figures 2.3c,f), but there is no joint between these regions. The tarsus in Phalangida is usually di-

Morphology and Functional Anatomy

vided into from 3 tarsomeres, as in Zalmoxidae and Trogulidae, to over 100 in some phalangioids (Figures 2.7e–h). The tarsus is undivided in most Cyphophthalmi (Figure 2.7d). Phalangida are plantigrade (i.e., they stand on the ventral surface of the tarsus), and Cyphophthalmi are unguligrade (i.e., they stand on the tip of the tarsus and the claw); the latter is the primitive state. Most Laniatores possess a constriction that divides the tarsus into a basitarsus and distitarsus. In general, longlegged climbing species have more tarsal segments than short-legged and soildwelling species (see Chapter 7). In many long-legged phalangioids the multisegmented tarsi are prehensile and can wrap two or three times around twigs and stems (Kästner, 1968). This ability is particularly remarkable given that the tarsus has no intrinsic muscles; only tendons of the claw muscles pass through the tarsus (Guffey et al., 2000; Figure 2.7h). The claw is a leg segment operated via long tendons by muscles that originate in the patella, tibia, and metatarsus (Shultz, 1989). There is a single claw on all legs in Cyphophthalmi (Figure 2.7d), Eupnoi (Figure 2.7e), Dyspnoi, and Insidiatores and legs I–II in Grassatores. There are two claws on legs III–IV in Grassatores, although a clawlike tarsal process may project from the tarsus between the two claws and give the appearance of three claws (Figures 2.7f,g). The claws are usually simple, although they may have a row of teeth on the ventral surface, or lateral pegs. The claws of legs III–IV in Insidiatores have small side branches (Briggs, 1971a), with juveniles having more branches than adults (Hunt & Hickman, 1993). In nymphal stages of Grassatores and some Insidiatores there are two additional structures on the third and fourth leg tarsi, a median tarsal claw, the pseudonychium, and a fleshy projection, the arolium (see also Chapter 13). These structures probably allow adhesion to smooth surfaces during ecdysis; they are absent in adults (Gnaspini et al., 2004). The arolium is absent in immatures of Oncopodidae and Triaenonychidae. In some families of Grassatores the tarsal process arises apically in the last tarsomere, above the claws. It varies from a tubercle with long setae to a pronounced cuticular projection; it has been lost secondarily several times.

Appendotomy. The legs in Eupnoi and many long-legged Dyspnoi have lines of weakness at the very base of the femora (Wasgestian-Schaller, 1967; see also Chapter 10). When this line is broken, the distal part detaches, and the muscles of the trochanter pull the small proximal remainder inward, which closes the wound. Breakage can be caused by a predator, or the harvestman can actively detach a trapped leg by a powerful movement of the coxa-trochanter joint. It appears that leverage provided by a distal restraint is required to achieve appendotomy and that the animal cannot cause a leg to simply fall off (Chapter 10). Legs are not regenerated, even when lost in early instars. Legs of phalangioids can twitch for several minutes after appendotomy, with oxygen being supplied by tibial spiracles (Figures 2.12d,e). Posture and locomotion. Most terrestrial arthropods have a characteristic “hanging stance” (Manton, 1952) in which each supporting leg projects upward from the substratum, bends at one or two “knees,” and then angles downward to at-

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tach to the body, which is suspended just above the substratum (Figure 2.8). This posture is thought to enhance stability in small animals that live on exposed surfaces. The difficulty of displacing an animal from a horizontal substrate by a transverse force (e.g., wind) is proportional to the animal’s body mass and stance width (i.e., the distance between the center of mass and point of support) and inversely proportional to the height of the center of mass (Alexander, 1982). Long-legged harvestmen epitomize this posture; their small bodies are held close to the substratum by long legs that form a very broad base of support. Those harvestmen and other arthropods that live in protected areas (e.g., leaf litter, soil, under stones) show less extreme versions of the hanging stance (see Chapter 7). Despite unusual features in the locomotor mechanism of many harvestmen (i.e., long, thin legs and multisegmented, plantigrade, and sometimes prehensile tarsi), the functional morphology of walking has been little studied. Stepping patterns have been examined quantitatively in a few phalangioids, most notably Oligolophus tridens (Ferdinand, 1982) and Leiobunum vittatum (Sensenig & Shultz, in press). These species, like all Phalangida, typically use leg II as a tactile organ rather than for

a

b

Figure 2.8. Locomotion of Leiobunum vittatum (Eupnoi, Sclerosomatidae). (a) Trajectory of the center of mass in the vertical axis. (b) Trajectory of the center of mass in the transverse axis. The animal is moving at a net speed of about 20 cm/s on a smooth, flat substratum. Leg tips indicated by shaded circles are in contact with the substratum and moving backward, others are lifted and moving forward (“alternating tripod” gait). Scale bars = 1 cm. Modified from Sensenig and Shultz (in press).

Morphology and Functional Anatomy

propulsion and walk with an insectlike alternating tripod gait; that is, Left I, Right III, and Left IV move essentially together as one tripod and Right I, Left III, and Right IV move as the other (Figure 2.8). This gait ensures that the center of mass is positioned within a triangular base of support throughout the step cycle (Ferdinand, 1982; Delcomyn, 1985). Significant cyclical displacements of the body’s center of mass occur in running phalangioids (Sensenig & Shultz, in press). The center of mass in Leiobunum vittatum undergoes large vertical displacements (Figure 2.8a) consistent with those predicted by the spring-loaded inverted-pendulum (SLIP) model of pedestrian locomotion (McMahon, 1985; Full, 1989) in that changes in gravitational potential energy occur in phase with changes in forward kinetic energy. The SLIP model maintains that as the center of mass falls, potential energy is converted into forward kinetic energy and some energy is stored as deformation of elastic skeletomuscular structures, or springs. Elastic recoil then assists muscles in producing forward kinetic energy and an increase in potential energy, and the cycle repeats. Transfer of energy from one part of the step cycle to another is thought to increase overall energetic efficiency of travel. The timing of transverse displacements (Figure 2.8b) is consistent with the lateral leg-spring (LLS) model of passive stabilization (Schmidt et al., 2002). Transverse perturbations to locomotion (e.g., uneven, broken, or slippery substrates, wind, conspecifics, predators) can occur rapidly or in such a complicated manner that active, reflex-based mechanisms do not have time to compensate. LLS predicts that passive compensatory mechanisms are engineered into the skeletomuscular system as an array of transversely aligned springs, which serve to dampen unexpected transverse perturbations and to dissipate their effects over several step cycles through oscillation of the spring system. LLS predicts a cyclical pattern of transverse displacements even in unperturbed animals, such as those observed in running L. vittatum.

MUSCULAR SYSTEM Muscles associated with appendages, genitalia, and the digestive tract are described under those headings. This section focuses on the muscles of the body axis.

Prosomal muscles The principal axial muscles in the prosoma are associated with the endosternite. This is a roughly horizontal sheet of connective tissue that acts as an internal skeleton for the attachment of extrinsic appendicular muscles (Pocock, 1902c; Firstman, 1973). It apparently evolved through consolidation of a primitive ladderlike intersegmental muscle system that is still present in many arthropods (Boudreaux, 1979; Shultz, 2001). Endosternal tissue is similar to cartilage but may contain calcium deposits in certain harvestmen (Kovoor, 1978). The ancestral endosternite of arachnids is thought to have spanned the body from the cheliceral to the first opisthosomal somite and to have had a segmental series of muscles. Each

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somite is thought to have had a pair of dorsal and ventral suspensor muscles that attached to the dorsal and ventral body walls within a somite and a pair of posterior oblique suspensor muscles that attached to the dorsal surface of the posteriorly adjacent somite (Shultz, 2001). The various arachnid orders have lost different combinations of suspensor muscles. The endosternite in Opiliones is essentially U shaped, with the lateral arms projecting anteriorly and embracing the supraesophageal ganglion (Figure 2.9a). The anterior ends of the endosternal arms, or anterior horns, attach to the posterior arms of the epistome. Harvestmen apparently retain the ventral suspensors of each leg-bearing somite (contra Firstman, 1973) and the first opisthosomal somite, which

Figure 2.9. Skeletomuscular anatomy of the body axis. (a) Diagrammatic midsagittal section of Leiobunum (Eupnoi, Sclerosomatidae) with chelicerae and most extrinsic appendicular muscles removed. The central nervous system is depicted as a translucent “ghost” to show approximate placement, as well as the endosternite and several extrinsic muscles associated with the coxapophyses of the stomotheca. Based on Shultz (2000). (b– c). Cross sections through the anterior (b) and posterior (c) parts of the pharynx. Redrawn from Kästner (1933). (d) Lateral view of adult female Leiobunum with “transparent” cuticle showing arrangement of opisthosomal muscles. Based on Shultz (2000). (e) Lateral view of Chileogovea (Cyphophthalmi, Pettalidae) showing pleural muscles. Small posterior longitudinal muscles are not shown. Roman numerals refer to postoral somites. Abbreviations: ag, arculi genitales; cm, circular pharyngeal constrictor muscle; cp1, coxapophysis of leg I; cp2, coxapophysis of leg II; cpp, coxapophysis of the pedipalp; cx, coxa; dg, dorsal groove of pharynx; dlm, dorsal longitudinal muscle; dm, pharyngeal dilator muscle; ds, dorsal endosternal suspensor muscle; ep, epistome; es, esophagus; fe, femur; go, genital operculum; lb, labium; oc, ocularium; on, optic nerve; ov, ovipositor; oz, ozophore; pgc, pregenital chamber; ph, pharynx; pm, pleural muscles; pp, pedipalp; scl, supracheliceral lamella; sl, sulcus; tm, transverse muscle of epistome; tr, trochanter; vlm, ventral longitudinal muscle; vs, ventral endosternal suspensor muscle; vt, ventriculus (midgut).

Morphology and Functional Anatomy

attach to the body wall near or between the coxae (Shultz, 2000). The ventral suspensor of somite VII attaches on or near the posterior margin of the last coxa and is usually much larger than the others (Figure 2.9a). Ventral suspensors may seem to attach to the coxae themselves and have been mistaken for extrinsic leg muscles, especially in harvestmen with fused coxae. However, extrinsic leg muscles can be pulled away from the endosternite cleanly during dissection, while ventral suspensors are fully integrated into the endosternal tissue and cannot be separated without damage to both. The dorsal and posterior oblique suspensors have been greatly reduced in number and size in all Opiliones, and those that remain cannot be reliably assigned to specific somites. Most harvestmen retain two pairs of muscles that probably correspond to the dorsal suspensors of somites VI and VII (Figures 2.9a,d,e), but Leiobunum has two additional pairs. One attaches on the carapace between the extrinsic muscle of the pedipalp and leg I, and the other attaches to the dorsal surface of the second opisthosomal somite (Figure 2.9a).

Opisthosomal muscles The primitive ladderlike intersegmental muscle system from which the endosternite apparently evolved is also thought to have spanned the opisthosoma in ancestral arachnids (Shultz, 2001). However, these muscles have been lost, reduced, or simplified in Opiliones. Those muscles that remain appear to function in regulating the volume and/or internal pressure of the hemocoel. The musculature is best developed in those harvestmen with a poorly sclerotized and distensible opisthosoma (Figure 2.9d). In Leiobunum, for example, there are several pairs of longitudinal muscles spanning the ventral body surface, with each muscle tending to attach to every other sternite and with neighboring muscles inserting on different sternites. There are a few dorsal longitudinal muscles; some connect the opisthosoma to the prosoma, and others operate sclerites associated with the anus. There are also segmentally arranged pleural muscles, each of which arises from the lateral surface of the opisthosoma and radiates to adjacent tergal regions. The musculature of harvestmen with a heavily sclerotized opisthosoma tends to be even simpler, especially in those groups with extensive fusion of tergites and sternites. In Cyphophthalmi, for example, the body surface is constructed from two large, compound sclerites, the dorsal scutum completum and the ventral coxosternal sclerite. Axial movements are restricted to adjusting the vertical distance between the dorsal and ventral sclerites and to movements at the anal region. The musculature in this case is limited to a segmental series of large pleural muscles (Figure 2.9e) and a few small longitudinal muscles near the anus.

DIGESTIVE TRACT Foregut The foregut (stomodeum) develops as an anterior ectodermal invagination, and its lumen is lined with a thin layer of cuticle. The lumen of the foregut has six radiating folds throughout its length: two dorsal, two lateral, and two ventral (Loman,

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1903b; Kästner, 1933; Snodgrass, 1948; Janczyk, 1956; Juberthie, 1983; Figures 2.9b,c, 2.14). The pharynx is an expanded anterior region of the foregut equipped with dilator muscles that arise from the inner surfaces of the epistome and, in some cases, the carapace (Kästner, 1933; Firstman, 1973; Shultz, 2000) and insert along the apices of the longitudinal folds of the pharyngeal wall (Figures 2.9a–c). Constrictor muscles also insert along the longitudinal folds, with their attachments alternating with those of the dilator muscles (Figures 2.9a–c). In phalangioid harvestmen the pharyngeal wall between the dorsal folds has a gutterlike canal (Figure 2.9b) similar to the pseudotracheae (Kästner, 1933). Its function is not known. The pharynx ends where the foregut penetrates the central nervous system (Figures 2.9a, 2.14b), whereupon it is called the esophagus. The esophagus empties into the midgut just posterior to the central nervous system, but details of the foregutmidgut junction vary. A valve formed by circular constrictor muscles has been described in Trogulus (Juberthie, 1983; Figure 2.14b). The presence of valves or valvelike structures has not been determined in other taxa.

Midgut or mesenteron The arthropod midgut is derived embryologically from endoderm and lacks the cuticular lining of the fore- and hindguts. The epithelium is derived from embryonic vitellophage cells, which are initially scattered within the yolk but migrate to the periphery at a later stage in development (Moritz, 1957; D. T. Anderson, 1973; see also Chapter 13). The midgut is the largest organ in harvestmen and performs many vital functions, including enzymatic digestion, nutrient absorption, nutrient and waste storage, and water uptake (Frank, 1937; Phillipson, 1961, 1962a; Becker & Peters, 1985a,b; Lipovsek et al., 2004). The main axis of the midgut is divided into an anterior ventriculus and a posterior postventriculus by a dorsal transverse fold (Figure 2.10f). The lateral walls of the ventriculus have three or four pairs of diverticula (ceca, sometimes referred to collectively as the midgut gland), which are simple or branched lobes that fill much of the hemocoel not occupied by other organs (Figures 2.10e,f, 2.11).

Ventriculus and diverticula. The luminal side of the ventricular and diverticular wall is lined with a single-layer epithelium of columnar cells (200–300 ␮m long by 10–20 ␮m wide), which have a brush border of microvilli projecting into the midgut lumen. Basal stem cells (i.e., undifferentiated cells that replace epithelial cells) occur in other arachnids but have not been observed in harvestmen, so the mechanism of cell replacement is not known. The epithelium is organized into multicellular papillae, with each papilla comprising cells of several types. The hemocoelic surface of the epithelial basement membrane is surrounded by muscle cells, tracheae, and strands of intermediate tissue. Intermediate tissue stores lipids and glycogen, but in much lower amounts than in some other arachnids, such as scorpions (Farley, 1999) and solifuges (Ludwig & Alberti, 1992), where it forms a fat body. In Phalangium opilio the epithelium of the ventriculus and diverticula contains three cell

Morphology and Functional Anatomy

a

b

c

d

e

f

Figure 2.10. Development and structure of the midgut. (a–d) Embryological development of the midgut diverticula from yolk in Phalangium opilio (Eupnoi, Phalangiidae). Redrawn from Moritz (1957). (e–f) Midgut of adult Ischyropsalis manicata (Dyspnoi, Ischyropsalididae): (e) dorsal view; (f) ventral view with ventral wall cut away to show interior, including openings to diverticula. Modified from Dumitrescu (1974a). Roman numerals indicate postoral somites. Abbreviations: cl, cardiac loop of coxal organ; ht, heart; OD1–3, primary opisthosomal diverticula 1–3; PD, primary prosomal diverticulum; PO, prosoma-opisthosoma border; tf, transverse dorsal fold of midgut separating ventriculus (vt) and postventriculus (pvt).

types (resorptive, digestion, and excretion cells), and an additional fourth type (ferment cells) is limited to the diverticula. The cells are typically infected with rickettsialike organisms, a feature also present in other arachnids (Becker & Peters, 1985a,b). The resorptive cells may be unique to harvestmen. They have a thin layer of organelle-free cytoplasm just basal to the microvilli followed by a zone of mitochondria and various vesicles. They have numerous specialized vesicles (1 ␮m diameter) interspersed among the mitochondria and appear to contain material for construction of peritrophic membranes (discussed later). Rough endoplasmic reticulum (ER) and dictyosomes extend throughout the middle to basal portions of the cell. The nucleus is located in the middle to basal region and is somewhat long, is lobed, and often has two nucleoli. Resorptive cells contain lipid droplets (5 ␮m diameter) and glycogen rosettes basally. Mineral spherites (0.6–2 ␮m diameter) are distributed throughout the cell. The role of resorptive cells is unclear, but they probably serve to store nutrients used in digestive metabolism (Frank, 1937; Becker & Peters, 1985b). Digestion cells are involved in pinocytotic uptake of material from the midgut lumen. The apical regions are densely populated with vesicles and lysosomes. A large type of vesicle (up to 10 ␮m diameter) is located in the apical region. Ventricular digestion cells also contain a paracrystalline structure of unknown function. Mitochondria and cisternae of rough ER are distributed among these vesicles. Mineral

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Morphology and Functional Anatomy

spherites are distributed throughout the cytoplasm. Digestion cells of the diverticula are larger than those of the ventriculus (ca. 300 ␮m long rather than ca. 200 ␮m) and contain lipid droplets and glycogen basally (Becker & Peters, 1985a,b). Excretion cells lack a well-developed microvillar border, and all organelles are located around a large central vacuole (up to 50 ␮m diameter). The cytoplasm has numerous mineral spherites. Excretion involves ejection of either the vacuole and portions of the cell contents or the entire cell (Phillipson, 1961; Becker & Peters, 1985a,b). The ferment cells, which are probably equivalent to the “secretory” cells of other arachnids, are present only in the diverticula and apparently secrete digestive enzymes into the lumen. The cell has numerous vesicles (ca. 4 ␮m diameter) with mature vesicles positioned apically. The cell has extensive rough ER and mitochondria. Lipid droplets are present, but not glycogen (Becker & Peters, 1985a). It is likely that two or more cell types represent different functional or maturational stages of a single class of epithelial cells; the excretory cells are mature digestion cells.

Mineral spherites. Small concentrically structured, membrane-bound mineral spherites (granules, concretions) are common in the digestive organs of many arthropods (Hopkin, 1989; Köhler, 2002), including horseshoe crabs (Fahrenbach, 1999) and most arachnids. Spherites vary in composition and seem to have several functions, including sequestering heavy metals and mineral storage. As noted in the previous section, intracellular spherites are abundant in the ventricular and diverticular cells of harvestmen. Lipovsek et al. (2002) have shown that spherites in Gyas (Sclerosomatidae) have an organic matrix of glycoproteins and proteoglycans and that other components change throughout the life cycle. Spherites in overwintering juveniles contain high concentrations of calcium and phosphorus and some silicon, but much of the calcium and phosphorus are used during molting in the following spring and summer. Silicon persists throughout life, but at gradually decreasing Figure 2.11. Dorsal views of midgut diverticula from representative harvestmen. Redrawn from Kästner (1934) and Dumitrescu (1974–1980). (a) Cyphophthalmi: Cyphophthalmus duricorius (Sironidae). (b) Laniatores: Sclerobunus nondimorphicus (Triaenonychidae, Northern Hemisphere). (c) Laniatores: Paranuncia ingens (Triaenonychidae, Southern Hemisphere). (d) Laniatores: Discocyrtus invalidus (Gonyleptidae). (e) Eupnoi: Mitopus morio (Phalangiidae). (f) Eupnoi: Astrobunus laevipes (Sclerosomatidae). (g) Eupnoi: Spinicrus nigricans (Monoscutidae). (h) Eupnoi: Tasmanopilio fuscus (Caddidae). (i) Dyspnoi: Ischyropsalis manicata (Ischyropsalididae). (j) Dyspnoi: Ceratolasma tricantha (Ceratolasmatidae). (k) Dyspnoi: Sabacon pygmaeus (Sabaconidae). (l) Dyspnoi: Hesperonemastoma modestum (Ceratolasmatidae). (m) Dyspnoi: Paranemastoma kochi (Nemastomatidae). (n) Dyspnoi: Dicranolasma scabrum (Dicranolasmatidae). (o) Dyspnoi: Trogulus nepaeformis (Trogulidae). (p) Dyspnoi: Trogulus gypseus (Trogulidae). Abbreviations: D1, first primary diverticulum of Laniatores; OD1–OD3, primary opisthosomal diverticula 1–3; PD, primary prosomal diverticulum; pl, ramus prominens lateralis; pm, ramus prominens medialis; ra, ramus anterior; rc, ramus centralis; rca, ramus coxalis anterior; rcp, ramus coxalis posterior; rex, ramus exterior; rl, ramus regrediens lateralis; rla, ramus lateralis; rlong, ramus longitudinalis; rltr, ramus laterotransversalis; rm, ramus regrediens medialis; rmn, ramus medianus; robex, ramus obliquus externus; robint, ramus obliquus internus; rp, ramus posterior; rprml, ramus prominens medialis; rseg, rami segmentales; rtr, ramus transversalis. Scale bars = 1 mm.

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levels. Spherites tend to disintegrate during the adult stage, with the organic matrix being eliminated in waste vacuoles.

Postventriculus. This region (Figure 2.10f) compacts solid digestive waste and absorbs water, but its structure has been well studied only in P. opilio (Becker & Peters, 1985b). Its cells are shorter (up to 100 ␮m) and narrower (up to 80 ␮m) than those of the ventriculus and diverticula; they lack mineral spherites, lipid droplets, glycogen, and rickettsia-like parasites. The postventricular epithelium is composed of two cell types, secretion cells and transport cells. Secretion cells are apparently specialized for construction of peritrophic membranes. They contain two kinds of vesicles, a smaller (ca. 300 nm) type that contains chitin or chitin precursors and a larger (up to 1 ␮m) type that may contain protein. Secretion cells also have cristate mitochondria, an extensive Golgi apparatus, and numerous, widely distributed multivesicular bodies. The transport cells are specialized for removing water from the postventricular lumen and transporting it basally. The terminal microvilli are very long (ca. 6 ␮m), which enhances absorptive surface area, and the cytoplasm contains large cristate mitochondria. Vesicles similar to those of the secretion cells may occur apically, but they are not abundant. Transport cells have an extensive basal labyrinth that may extend up to 40 ␮m into the cell. Peritrophic membranes. Many arthropods secrete a thin, acellular envelope of chitin and protein, the peritrophic membrane (PM), around the contents of the midgut lumen. The once-conventional notion that PMs serve exclusively to protect the midgut epithelium from mechanical injury (reviewed by Peters, 1992) led to a widespread assumption that the largely fluid-feeding arachnids lacked PMs. These oversimplifications were perpetuated long after the discovery of PMs in arachnids (van der Borght, 1966) and in many fluid-feeding insects. Other functions of PMs have been determined primarily from studies of insects and ticks and include lumen compartmentalization, selective permeability, and defense against pathogenic organisms (Terra, 2001). PMs are known from spiders (van der Borght, 1966), mites (Alberti & Coons, 1999), and harvestmen (Peters, 1967; Becker & Peters, 1985b). Within harvestmen, formation and structure of PMs have been examined in only a few phalangioids (Peters, 1967; Becker & Peters, 1985b). Despite the narrow taxonomic sample, results from these studies probably apply to most harvestmen, as similar materials and processes occur in many arthropod groups. It is possible that the gut trace preserved in the Devonian harvestman Eophalangium (Dunlop et al., 2004) represents a chitinous PM. Becker & Peters (1985b) conducted an electron-microscopic study of the midgut in P. opilio and observed two kinds of PM, a thick PM (0.3–0.5 ␮m) composed of a regular pattern of microfibrils and electron-lucent gaps (150–200 ␩m in diameter) and a thin PM (0.1–0.3 ␮m) composed of an irregular array of microfibrils. Thick PM is apparently deposited by ventricular cells between microvilli, with the organized structure of gaps and microfibrils corresponding to the pattern of microvilli and spaces between microvilli, respectively. In contrast, the thin PM seems to poly-

Morphology and Functional Anatomy

merize at the tips of the microvilli, and the pattern of microfibrils is effectively random. The ventriculus produces both thick and thin PMs in a period from two to four hours after a meal. Up to four thick PM layers envelop the ventricular contents. The postventriculus produces only thin PM, and production is apparently continuous rather than being coupled with ingestion or other digestive events. The fecal envelope is composed of several thin PM layers and is up to 24 ␮m thick. PM layers may be compacted within the posterior ventriculus over time, as the deeper layers within the envelope are closer together than more superficial layers. No research has been conducted on specific functions of PMs in harvestmen.

Comparative morphology of the diverticular complex. Two systems have been used to organize the considerable diversity of the diverticular complex (Figure 2.11), one in which lobes are numbered in a roughly anterior-to-posterior sequence (A. Müller, 1924; Kästner, 1926, 1933; Moritz, 1957), an approach that proved impractical as more taxa were studied, and a second based mainly on the pattern of diverticular branching (Loman, 1903b; Kästner, 1934; Holm, 1947; Janczyk, 1956; Dumitrescu, 1974a,b, 1975a,b,c, 1976, 1980). The latter system was developed to a great extent by Kästner (1934), who recognized three pairs of primary diverticula (diverticula I–III) arising directly from the ventriculus in an anterior-to-posterior sequence. He was aware that some taxa have an additional lobe (ramus posterior) between diverticula I and II, but he considered it a posterior branch of diverticulum I that had secondarily gained its own connection to the ventricular lumen. He supported his “escaped diverticulum” hypothesis by noting that the epithelium separating diverticulum I and ramus posterior was of the diverticular type rather than the ventricular type that typically separates primary diverticula. However, Kästner’s system proved to be inconsistent with results from ontogenetic studies. During a stage of rapid organogenesis, harvestman embryos develop a series of lateral mesodermal septa that constrict the yolk to form a series of segmentally arranged dorsolateral lobes, the primordial diverticula (Figures 2.10a–d). Phalangiids have four pairs of primordial diverticula that correspond to the prosoma and the first three opisthosomal somites (Holm, 1947; Moritz, 1957; Juberthie, 1964). The second diverticulum (the ramus posterior of Kästner) later merges with the first in some species (e.g., P. opilio), perhaps because of subsequent reduction in the length of the first opisthosomal somite (Moritz, 1957). Diverticular ontogeny in the gonyleptid Pachylus quinamavidensis is similar (Muñoz-Cuevas, 1971b), but the details of embryological events within the prosoma and at the prosoma-opisthosoma boundary are not yet clear. Dumitrescu (1974–1980) surveyed the diverticular complex in harvestmen and modified Kästner’s system to accommodate embryology. He adopted a system of three primary diverticula for Laniatores (DI–DIII) and four for Eupnoi, Dyspnoi, and Cyphophthalmi (DI–IV). The system is somewhat confusing, because DII and DIII in Laniatores are clearly homologous with DIII and DIV in Eupnoi and Dyspnoi; they are the diverticula of the second and third opisthosomal somites in both groups and share important similarities in their structure, development, and orientation with

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respect to the heart and cardiac loop of the coxal organ. The homology of DI in Laniatores is problematic; it may be the diverticulum of the first opisthosomal somite alone or in combination with a prosomal diverticulum. Here we offer a slightly modified terminology that better reflects current understanding of diverticular homology. In Cyphophthalmi, Eupnoi, and Dyspnoi, DI of the Dumitrescu system is renamed the prosomal diverticulum (PD) and the remaining three are opisthosomal diverticula 1–3 (OD1–OD3). The first diverticulum in Laniatores is diverticulum 1 (D1) and the remaining are opisthosomal diverticula 2 and 3 (OD2, OD3) (Figures 2.10, 2.11). Distinct prosomal diverticula occur in other arachnid groups, so presence of a differentiated PD is probably plesiomorphic for Opiliones. The internal complexity of PD varies among harvestman species, with increasing complexity being roughly correlated with increasing body size. The posterior, perhaps metapeltidial, portion of PD often has a medial ramus centralis and an elongate ventrolateral ramus coxalis posterior. The anterior portion of PD may have an anterior lobe (ramus anterior) that projects into the base of the chelicera and a variably developed lateral lobe (ramus coxalis anterior). In its most complicated state each ramus coxalis anterior has three secondary branches corresponding to the coxae of legs I–III. D1 of Laniatores is usually unbranched, but there are exceptions (Figure 2.11c). OD1, or ramus posterior, is a simple, unbranched dorsal lobe. As noted earlier, it sometimes has a common ventricular connection with PD. OP2 has a single lobe in Cyphophthalmi (Figure 2.11a), but the other harvestmen have two lobes, a medial ramus transversalis and a lateral ramus longitudinalis. These lobes usually share an opening to the ventriculus but can have separate openings, as in Mitopus morio (Phillipson, 1961). OD3 has two branches that project posteriorly, a medial ramus medianus and a lateral ramus lateralis, an arrangement that is highly conserved throughout Opiliones. Ramus lateralis may have segmentally arranged branches (rami segmentales) in larger phalangioids and ischyropsalidoids (Figures 2.11e,f,i,j). A third main branch of OD3 (ramus exterior) occurs in Grassatores and certain Insidiatores, including Synthetonychiidae and Triaenonychidae of the Southern Hemisphere (Figures 2.11c,d).

Phylogenetic value of midgut diverticula. The most useful phylogenetic characters have a low propensity for homoplasy (i.e., evolution of similar structures independently in different lineages) and are independent from other characters, and sizedependent effects on midgut function may predispose the diverticular complex to homoplasy and thereby limit its phylogenetic utility. Assuming isometric scaling (i.e., no change in shape with change in size), for any given increase in length L, surface area will increase in proportion to L2 and volume will increase in proportion to L3. As body size increases (all other things being equal), a body volume will eventually be reached at which the demand for nutrients exceeds what the midgut surface area can supply. At this point, one would expect a change in midgut shape with increasing body size to increase the relative amount of diverticular epithelium available for nutrient absorption and storage. The potential for scale-dependent homoplasy seems especially likely

Morphology and Functional Anatomy

in Eupnoi and Dyspnoi, where the prosomal diverticula enlarge through “filling in” of intermuscular niches. Specifically, ramus anterior, ramus coxalis anterior, and ramus coxalis posterior tend to enter the bases of prosomal appendages. A similar process occurs in the opisthosoma, where ramus lateralis develops a series of rami segmentales. This phenomenon may explain similarities between larger phalangioids and ischyropsalidoids (Figures 2.11e,f,i,j). Homoplasy is also expected at the other end of the size spectrum, as small harvestmen from different lineages should tend to have simple, unbranched diverticula (Figures 2.11b,l). Despite the potential pitfalls of diverticular characters for phylogenetic analysis, there appear to be synapomorphic similarities among groups of harvestmen. The presence of only three pairs of opisthosomal diverticula and branching of the third into ramus lateralis and ramus medianus (Figures 2.11a–p) appear to be synapomorphic features of Opiliones. The branching of OD2 to form ramus transversalis and ramus longitudinalis may be synapomorphic for Phalangida (Figures 2.11b–p), and the loss of PD or its consolidation with OP1 may unite Laniatores (Figures 2.11b–d). The presence of an extra branch (ramus exterior) in OP3 may unite Grassatores with the Insidiatores of the Southern Hemisphere (Figures 2.11c,d), thereby implying that the group Insidiatores is paraphyletic (see also Chapter 3). PD in caddoids has an extra branch (ramus prominens medialis; Figure 2.11h) that occupies the space created by the enlarged ocularium characteristic of this group (Figure 2.1d), so these two characters probably do not provide independent support for monophyly of Caddoidea. Trogulids (Figure 2.1b) appear to have a novel allometric relationship between body size and diverticular surface area. They increase relative midgut surface area by enhancing diverticular length rather than diverticular branching, with the largest species packing diverticula in convoluted folds (Dumitrescu, 1974b; Figures 2.11o,p). Hansen and Sørensen (1904) noted that these tightly packed diverticula resemble the gyri of a mammalian brain.

Hindgut or proctodeum The hindgut is a short tube linking the postventriculus and anus (Kästner, 1933). It develops as an ectodermal invagination, and its walls are lined with a thin chitinous intima. Several extrinsic muscles arise from adjacent tergites and sternites and probably dilate the hindgut; dorsal and ventral longitudinal muscles of the posterior body wall probably shorten the hindgut. Simultaneous contraction of these muscle groups likely pushes the fecal mass through the anus (Kästner, 1933; Janczyk, 1956; Shultz, 2000), with anal closure apparently caused by elasticity of the perianal cuticle.

RESPIRATORY SYSTEM Harvestmen respire through an extensive tracheal system (Figure 2.12c) that opens to the atmosphere through a pair of spiracles (Figures 2.12a,b) located on the second opisthosomal somite posterior to the coxae of the last pair of legs (Figures

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1

Mt

Figure 2.12. Respiratory system. (a) Cyphophthalmi: Metasiro americanus (Neogoveidae), spiracle. (b) Laniatores: Pseudogyndesoides sp. (Gonyleptidae), spiracle. (c) Eupnoi: Phalangium opilio (Phalangiidae), schematic dorsal view of main tracheal branches. Based on drawings and descriptions in Kästner (1933). (d) Eupnoi: Opilio parietinus (Phalangiidae), retrolateral view of the tracheal system in the legs showing tibial spiracles. Redrawn from Wasgestian-Schaller (1967). (e) Eupnoi: Cosmobunus granarius (Phalangiidae), details of proximal tibial spiracle. Redrawn from Wasgestian-Schaller (1967). Abbreviations (Latinized names from Kästner, 1933): a, ramus ascendens; ao, ramus aortis; at, atrial thorns; c, ramus cheliceralis; ca, ramus cheliceralis accessorius; Ch, chelicera; Cx1–4, coxae of legs I–IV; ds, distal tibial spiracle; f, fimbrae; Fe, femur; g, ramus genitalis; gl, ramus ganglionaris; ip, ramus intestinalis posterior; la, ramus lateralis; m, ramus medialis; Mt, metatarsus; oc, ramus oculorum; Pa, patella; pa, ramus prosomae anterior; pa1–4, ramus pedis anterior of legs I–IV; pc, ramus pericardiacus; pl, ramus pedipalpis; pla, ramus pedipalpis accessorius; po, ramus posterior; Pp, pedipalp; pp, ramus prosomae posterior; pp1–4, ramus pedis posterior of legs I–IV; ps, proximal tibial spiracle; s, ramus superior; T, tracheal trunk; t, taenidia; Ti, tibia; vn, ramus ventralis; vr, ramus verticalis.

Morphology and Functional Anatomy

2.2b,k). The tracheae are similar to those of insects. The luminal surface has a thin, cuticular lining strengthened by spiral thickenings (taenidia) (Figure 2.12e); the hypodermis, which produces and maintains the tracheal cuticle, lies on the hemocoelic surface. In contrast to insects, harvestmen have a nonmetameric pattern of branching, and tracheae usually end in the hemolymph near organs and tissues rather than within them, although shallow penetration occurs in the muscles of active species (Höfer et al., 2000). Harvestmen are unusual among tracheate arthropods in having hemocyanin (Markl et al., 1986), an oxygen-binding respiratory pigment typically found in the hemolymph of arachnids with book lungs. Pending further investigation, the respiratory system of harvestmen might be classified as a tracheal lung (Höfer et al., 2000). The spiracles take a variety of forms in different groups of harvestmen (Figures 2.12a,b). They may be exposed or hidden, and the opening can have a variety of shapes. The opening is typically guarded by spines or cuticular projections that form a grill or lattice, which can be very ornate. These probably act as filters, excluding particles, parasites, and water from the tracheal system. In contrast, the spiracles of sclerosomatids are open or weakly guarded, and the spiracular atrium is actively dilated and constricted by muscles attached to an internal cuticular lever, or entapophysis (Sˇ ilhavy, 1970; Hunt, 1990b; Hunt & Cokendolpher, 1991). Thus the higher phalangioids appear to have replaced a passive filter with an active one. The pattern of tracheal branching (Figure 2.12c) appears to be fairly constant throughout the order (Kästner, 1933; Höfer et al., 2000), although this inference is based on a small taxon sample. A single main trunk projects upward and forward from each spiracle and passes into the prosoma, where it narrows gradually before ending in the ipsilateral chelicera. Along its path the trunk sends off lateral branches to the appendages. Each leg receives two branches from the trunk in Laniatores, Phalangioidea, and Troguloidea, but only one in Cyphophthalmi (Jancyzk, 1956). The chelicera and pedipalp each receive one branch from the trunk, but an additional trachea enters each appendage through an alternate route. Two large branches, rami prosomae anterior and posterior, sprout from the trunk (Figure 2.12c: pa, pp). The anterior branch serves the chelicera, eye, and anterior aorta; the posterior supplies the pedipalp, central nervous system (CNS), and accessory reproductive glands. Significantly, the posterior branches from each side meet at the midline and form a single transverse trachea in Phalangioidea and Troguloidea, but not in Cyphophthalmi (Jancyzk, 1956). The gonad and genitalia receive branches from the ramus genitalis and ramus ventralis, with the latter also serving the ventral body surface. The digestive tract is supplied by three main branches, ramus ascendens, ramus intestinalis anterior (which also sends a branch to the heart), and ramus intestinalis posterior (Kästner, 1933).

Accessory tibial spiracles Phalangioids are unique in having small accessory spiracles on the tibiae of the pedipalps and legs. Phalangiid and sclerosomatid harvestmen have two small spiracles on the tibia of each walking leg, one proximal and one distal (Figures 2.12d,e).

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The accessory tracheae are guarded by marginal fimbrae and thornlike projections from the walls of the spiracle atrium (Figure 2.12e). The proximal spiracle is connected to a large trachea that supplies the leg proximal to the midtibial region; the distal spiracle attaches to a smaller trachea that serves more distal regions (Hansen, 1893; Loman, 1896; Wasgestian-Schaller, 1967). In adults these spiracles clearly augment the oxygen available to distal leg segments, which are most prone to low oxygen and high carbon dioxide concentrations. The distal spiracle is especially important. The distal parts of the leg assume a distorted posture several weeks after the distal spiracle is sealed, but legs with a sealed proximal spiracle appear unaffected (Wasgestian-Schaller, 1967). Tibial spiracles are the only source of oxygen in legs that twitch after appendotomy. Normal detached legs from adult Opilio twitch for about 23 minutes, but twitch for only about 40 seconds when the tibial spiracles are sealed. In those species examined thus far, tibial spiracles are absent in the first instar but appear in the second. Interestingly, twitching in normal detached legs from instars I–VI is usually very brief, about 2.5 seconds on average, and instars V and VI twitch for about 82 seconds. The average duration of twitching increases when the detached legs of juveniles are placed in an oxygen-rich atmosphere, indicating that the small diameters of the juvenile spiracles greatly limit the rate at which oxygen can be delivered to active muscles (Wasgestian-Schaller, 1967).

CIRCULATORY SYSTEM Harvestmen, like most other exclusively tracheate arachnids, lack the extensive arterial branching and well-defined venous sinuses typical of arachnids with book lungs (scorpions, whip scorpions, whip spiders, most spiders), and vessels are limited largely to a dorsal tubular heart with anterior and posterior aortae (Figures 2.10d,e, 2.14b). The heart is a short tube occupying the middorsal space between the midgut diverticula of the first three opisthosomal somites. An anterior aorta follows the dorsal surface of the midgut anteriorly to the esophagus and empties into a perineural sinus that surrounds the central nervous system and major nerves (Firstman, 1973; Figure 2.14b). The posterior aorta passes rearward along the median dorsal surface of the midgut to which it is attached (Dannhorn & Seitz, 1986). The heart has two pairs of ostia in all harvestmen examined thus far, and their position corresponds roughly to the intersegmental boundaries between opisthosomal somites 1 and 2 and somites 2 and 3 (Moritz, 1957). As in other chelicerates, the heart is innervated by a cardiac ganglion that runs along its middorsal surface. A loop of the coxal organ runs longitudinally along the lateral surface of the heart in Phalangida (Figures 2.10e, 2.13f), a feature discussed in the section on coxal organs. A discrete pericardium has not been described. Heart ultrastructure has been examined in detail in only a few phalangioids. The heart of Mitopus was examined by light microscopy (Økland et al., 1983), and the hearts of Leiobunum, Mitopus, and Rilaena by electron microscopy (Dannhorn & Seitz, 1986). Most of the information provided here is based on the latter study. The

Morphology and Functional Anatomy

heart wall has two cell layers, an internal myocardium and an external epicardium. It lacks an endocardium. In cross section the myocardium is composed of two thin muscle cells that join dorsally and ventrally via intercalated discs. Myocardial cell nuclei occur laterally within a longitudinal ridge. Most myofibrils are oriented circularly and act to constrict the heart during systole. A few longitudinal myofibrils occur at the cell periphery. The epicardium is a single layer of cells enclosing the myocardium and may function as an elastic skeleton. The epicardial cells contain many longitudinally oriented microtubules (ca. 224 per ␮m2) that may serve to dilate the lumen by elastic recoil during diastole. Epicardial and myocardial cells attach at junctions formed by microtubule-associated hemidesmosomes on the epicardial side and cytoplasmic plaques on the myocardial side, an arrangement similar to that found at the junctions of cuticular tendons and skeletal muscle elsewhere in the body. Cytoplasmic plaques anchor myofibrils via actin filaments. The epicardium also receives strands of connective tissue, which suspend the heart from the dorsal cuticle. The heart has two valves. The anterior valve is a dorsal epicardial flap that extends into the anterior aorta. It apparently acts passively to prevent backflow of hemolymph; it lacks contractile elements and innervation. The posterior valve may be controlled actively. It is a vertical slit formed by specialized myocardial cells with vertically oriented myofibrils. The valve is innervated by branches from the cardiac ganglion.

Hemocytes Arthropod hemolymph contains cells that have been classified into the following morphological types: prohemocytes, plasmatocytes, granulocytes, spherulocytes, adipohemocytes, oenocytes, and coagulocytes (J. C. Jones, 1962). This taxonomy is based on insects but appears to apply to many other arthropods. Not all arthropods have all cell types, and a few additional types are known. Dannhorn and Seitz (1987) examined hemocytes in three phalangioid harvestmen (Leiobunum, Mitopus, and Opilio) and found five of the traditionally recognized cell types and no unique type. Prohemocytes are small, ovate cells (ca. 5 ␮m diameter) that represent a small fraction of the hemocyte population. They are relatively unspecialized morphologically and probably represent stem cells of plasmatocytes. Plasmatocytes are larger versions (ca. 11 ␮m diameter) of prohemocytes that use amoeboid movement and specialize in pinocytosis and phagocytosis. They are known to ingest bacteria and dead cells. Granulocytes are about the same size as plasmatocytes and also use amoeboid movement. They appear to develop from plasmatocytes, but phagocytosis has not been observed. Organelles are better developed in granulocytes than in the previously mentioned hemocytes, and mature cells have numerous vesicles containing granules of unknown composition. They may act as storage cells. Spherulocytes are the largest hemocytes in harvestmen (ca. 15 ␮m by ca. 9 ␮m) and contain many membrane-bound spherules (1.5–2.0 ␮m diameter). Spherule size is essentially constant, but their composition changes over time. Spherulocytes are apparently nonmotile. Their function and developmental origin are unknown, but they appear not

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to develop further into another hemocyte type. Coagulocytes appear to be derived from granulocytes. They release granules and disintegrate when transferred to an untreated microscope slide, but not on a clean slide. Other hemocytes seem unaffected by slide treatment. Dannhorn and Seitz (1987) suggested that cellular disintegration is stimulated by bacterial endotoxins in a process analogous that observed in Limulus, where granulocytes release granules in response to endotoxins and other foreign substances. There is as yet no evidence that coagulocytes in harvestmen actually participate in hemolymph coagulation.

Possible hemocytopoietic organs Possible sites of hemocyte production have been identified in only two groups of arachnids, specifically, the lymphoid and supraneural organs of scorpions and the heart wall of spiders (Franz, 1904; Seitz, 1972). Lymphoid organs of scorpions occur in the anterior opisthosoma but penetrate the diaphragm and connect to the coxal organ; supraneural organs occur on the surface of the first two opisthosomal ganglia and their connectives and/or the closely associated supraneural artery. Cells of both organs resemble hemocytes and sequester material injected into the hemolymph (Farley, 1984, 1999). Harvestmen apparently lack structures comparable to the lymphoid organs, but perineural organs similar to the supraneural organs of scorpions are present and surround several opisthosomal nerves. The cells of the perineural organs resemble hemocytes and ingest particles and dyes injected into the hemolymph (Kästner, 1935b). Apparent perineural organs (often called “abdominal ganglia” in the older literature) are known from all major harvestman groups (Loman, 1903b; Kästner, 1935b; Janczyk, 1956). Dannhorn and Seitz (1986) found no evidence of hemocyte production in the heart of Leiobunum.

SPECIAL CELL TYPES: NEPHROCYTES AND OENOCYTES Nephrocytes Nephrocytes are cells of arthropods and onychophorans that recycle macromolecules extracted from the hemolymph by pinocytosis. They are not excretory in the strict sense. The alternative term “athrocyte” has been proposed to avoid the misconception that the cells have a kidneylike function (Locke & Wrightnour Russell, 1998), but the term is not widely used. Each nephrocyte is surrounded by a basal lamina or basement membrane, a characteristic feature of these cells that may be selectively permeable to macromolecules. An extracellular labyrinth or channel system is formed by deep, narrow folds (pedicels) of the plasma membrane and perforated diaphragms that span the closely spaced gaps between folds. It is unclear whether the perforated diaphragms act as filters, valves, or both. Labyrinth walls formed by plasma membrane are specialized for pinocytosis. The cytoplasm contains vesicles that differ in size and content; some are lysosomes. Some nephrocytes are suspended in the hemocoel by strands of collagen or collagen-like material attached

Morphology and Functional Anatomy

to muscles, nerves, and tracheae. They tend to be concentrated on and around the heart, and it is likely that heart movements deform these cells via their connective strands and thereby move hemolymph into and through the labyrinth (Crossley, 1984; Locke & Wrightnour Russell, 1998). Zanger et al. (1991) examined nephrocytes in Leiobunum and distinguished three types, mainly on the basis of their location. Pericardial nephrocytes are located on or near the heart and probably correspond to the “phagocytes” noted by Kästner (1935b) in Phalangium and Opilio. Anterior nephrocytes occur near the ventral surface of the pharynx and adjacent subesophageal ganglion and have been documented in phalangioids (Kästner, 1935b; Zanger et al., 1991) and Cyphophthalmi (Janczyk, 1956). The third class of nephrocytes is distributed throughout the body, attached to muscles, tracheae, nerves, and other structures (Zanger et al., 1991). Nephrocytes in certain insects may produce lysozyme, a protein that breaks down bacterial cell walls and is secreted into the hemolymph upon bacterial invasion or, in some cases, even minor penetration of the exoskeleton. Zanger (1995) examined anterior and pericardial nephrocytes in Leiobunum and found lysozymecontaining vesicles within one to three hours of bacterial challenge, but it was unclear whether nephrocytes were importing lysozyme that had been produced elsewhere or were producing it and exporting it to the hemolymph. The absence of lysozyme in vesicles associated with the nephrocyte’s Golgi apparatus suggests that the protein is produced elsewhere.

Oenocytes Oenocytes are ectodermally derived cells of arthropods characterized by extensive smooth endoplasmic reticulum and numerous mitochondria. The oenocytes of insects produce hydrocarbons for use in the epicuticle and as pheromones and ecdysone (Romer, 1991). Phalangioid harvestmen (i.e., Phalangium, Opilio, and Leiobunum) were the first arachnids in which oenocytes were recognized (Romer & Gnatzy, 1981). They are located in the epidermis of the pedal femora. The cells are large (up to 130 ␮m) and polyploid; the cytoplasm contains smooth ER, mitochondria, guanine crystals, glycogen deposits, and elongate vacuoles (up to 1 ␮m wide and 17 ␮m long) that presumably contain a crystalline material. Romer and Gnatzy (1981) showed that harvestman oenocytes produce ␣- and ␤-ecdysone and thereby identified the first site of ecdysone production in an arachnid. Their assays also revealed ecdysone production in the epidermis of the opisthosomal tergites, although they did not determine whether oenocytes were involved. It is noteworthy that oenocytes in insects are typically concentrated in the epidermis of abdominal tergites and sternites.

COXAL ORGANS Coxal organs (coxal glands) regulate concentrations of ions and water in the hemolymph. These structures, or their serial homologs, occur in many arthropod

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groups and are widely considered homologous, at least in part, with the metanephridia of other invertebrates (Buxton, 1913, 1917; K. U. Clarke, 1979). Each of the two coxal organs in adult harvestmen consists of five parts: sacculus, collecting tubule, labyrinth, bladder, and secretory duct (Figure 2.13). The sacculus is a roughly spherical sac drained by a collecting tubule (Kästner, 1935b). The sacculus probably contains cells (podocytes) specialized for ultrafiltration, as these occur in coxal organs of betterstudied arachnids. The collecting tubule connects, in turn, to a convoluted tubular labyrinth that empties into a large, thin-walled bladder. The bladder opens to the external environment through a cuticle-lined secretory duct. The duct is opened by a small muscle that attaches to the lateral surface of the endosternite and passes through the sacculus before attaching to the duct (Kästner, 1935a; Moritz, 1959). The coxal organs of adult Phalangida are unique in having a labyrinth with a cardiac loop (Loman, 1903b; Kästner, 1926, 1935a,b; Figures 2.10e, 2.13f). The cardiac loop extends posteriorly from the collecting duct into the opisthosoma and extends dorsally along the lateral walls of the midgut diverticula. As the loop approaches the dorsal midline, it meets the heart, turns anteriorly, and passes along the lateral surface of the heart and anterior aorta before reversing course and following the same route back to the prosoma (Figure 2.10e). The function of the cardiac loop is unclear, but it likely increases the area over which coxal-organ fluid and hemolymph can exchange ions and water.

a b

e

c f d Figure 2.13. Diagrammatic left lateral views of developing coxal organ in Phalangium opilio (Eupnoi, Phalangiidae). See text for explanation. (a–e) Based on figures and descriptions in Moritz (1959); (f) based on Kästner (1935b). Abbreviations: 1–4, coxae of legs I–IV; b, bladder; cd', cd", embryonic and adult collecting ducts; cl, cardiac loop; cod, coelomoduct; cor, coxal organ rudiments; lb, labyrinth; s', s", embryonic and adult sacculi; sd', sd", embryonic and adult secretory ducts.

Morphology and Functional Anatomy

Coxal fluid in adult harvestmen exits via openings near the posterior margin of coxa III. The openings occur in the heavily sclerotized sternal region medial to coxa III in Cyphophthalmi and Laniatores (van der Hammen, 1985) and in the flexible cuticle between pedal coxae III and IV in Eupnoi and Dyspnoi. There is evidence that some Grassatores have an additional opening. Hansen and Sørensen (1904) noted that one of them (Sørensen, 1879) traced the coxal organ in gonyleptids to an opening at the lateral margin of the carapace just posterior to the ozopore, an observation confirmed by Loman (1903b) but then largely overlooked by subsequent workers. This opening may correspond to the secretory duct of the embryonic coxal organ of phalangioids (described later) and is probably equivalent to the “posterior opening of the ozopore” surveyed by Hara and Gnaspini (2003). Clearly, the location, origin, function, and phylogenetic distribution of coxal secretory ducts in Laniatores require further study. In considering other possible nonosmoregulatory roles for coxal organs, it is interesting that many arachnids appear to use coxal fluid as saliva. Van der Hammen (1989) noted channels or gutters connecting coxal-organ openings to the preoral chamber in several arachnid groups (e.g., Amblypygi, Ricinulei, Acari, and Araneae) and inferred a salivary role for coxal fluid. Coxal organs open directly into the preoral region in Solifugae (Buxton, 1913) and may serve as salivary glands (Alberti, 1979). Unfortunately, few direct observations of coxal-fluid “salivation” have been reported, but the information available is noteworthy. While feeding, the mygalomorph spider Porrhothele (Hexathelidae) secretes coxal fluid at a rate of about 75 ␮L per hour (in hydrated animals) from ducts opening at the bases of legs I and III. The fluid travels anteriorly in a narrow channel between the coxae and sternum to the preoral chamber (Butt & Taylor, 1986, 1991, 1995). The position of coxal openings in some harvestmen seems compatible with coxal-fluid salivation, but observations of feeding harvestmen are needed to test this possibility.

Development of coxal organs Information available on coxal-organ development is derived primarily from one study of Phalangium opilio (Moritz, 1959; Figure 2.13). Coxal organs develop from mesodermal rudiments located at the posterior wall of embryonic legs I and III (Figures 2.13a–f). Similar rudiments occur on all postcheliceral appendages, but the pedipalpal rudiments disappear rapidly, followed by those of legs II and IV. The rudiment at leg I develops as a proximally opened tube (coelomoduct) that projects into the body (Figure 2.13a). The middle portion of the tube then forms a posterior loop that extends to leg IV (Figure 2.13b), and then develops into components of the embryonic coxal organ (Figure 2.13c). The proximal end expands to form a funnel-like and then spherical sacculus with a tubular extension, the collecting duct, and the distal end establishes an external opening and forms a secretory duct. The distal span of the posterior loop enlarges to form a bladder, and the proximal span elongates and loops to form the labyrinth. The embryonic coxal organ persists into the postembryonic period, but the sacculus, collecting duct, and secretory duct are even-

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tually lost and replaced by corresponding structures derived from mesodermal rudiments of leg III to form the adult coxal organ (Figures 2.13d–f). In constructing the adult organ, the rudiment of leg III generates a tubular “stalk” and proximal “presacculus” (Figure 2.13c). The structure grows inward and encounters the embryonic coxal organ. The presacculus contacts the proximal end of the labyrinth, and the stalk contacts the posterior end of the bladder (Figure 2.13d). The transition from embryonic to adult coxal organ occurs during postembryonic development from the following events: (1) the stalk establishes an external opening at the base of leg III and forms the adult secretory duct; (2) the presacculus fuses to the distal end of the labyrinth, which, in turn, detaches from the bladder; (3) the proximal end of the stalk fuses with the bladder and detaches from the presacculus; (4) the proximal end of the labyrinth establishes a connection with the bladder and loses its connection to the embryonic sacculus; (5) the embryonic sacculus degenerates, and the embryonic secretory duct closes (Figure 2.13e). Subsequent development includes enlargement of the definitive sacculus and bladder and formation of the cardiac loop (Figure 2.13f).

NERVOUS SYSTEM The central nervous system (CNS) of harvestmen consists of a large consolidated neural mass, with the paired appendicular nerves being the only gross morphological evidence of its original segmented architecture. The esophagus passes through the neural mass and divides it into supra- and subesophageal components (Figures 2.9a, 2.14b). The supraesophageal ganglion, or syncerebrum, has two main parts, the protocerebrum and the cheliceral ganglion (deutocerebrum). The protocerebrum is an embryologically preoral structure associated with the eyes, but the cheliceral ganglion originates postorally and takes a preoral position in early development. Until recently, the supraesophageal ganglion of all extant arthropods was thought to include three components (protocerebrum, deutocerebrum, and tritocerebrum), with the deutocerebrum and tritocerebrum representing ganglia of the first and second “antennae,” respectively. The presence of only two units in the supraesophageal ganglion of chelicerates was traditionally attributed to loss of the first antennae and deutocerebrum (Babu, 1985; Weygoldt, 1985), and the chelicerae and cheliceral ganglion were homologized with the second antennae and tritocerebrum. However, developmental genetic research on spiders (Damen et al., 1998) and mites (Telford & Thomas, 1998) revealed that the chelicerae and cheliceral ganglion are homologous to the first antennae and deutocerebrum of other arthropods and that no segmental components are missing in the chelicerate CNS. Rather, the tritocerebrum of chelicerates retains its postoral position in the subesophageal ganglion and may never have been part of the supraesophageal ganglion (see also Mittmann & Scholtz, 2003). The protocerebrum (Figure 2.14a) receives the optic nerves and is mainly involved in the reception and processing of visual information. Its histological struc-

Morphology and Functional Anatomy

abnc lnc plnc on on

aa

a

b

lan

suban

ol1 rn es ol2 suban

opco of1 af2

af1 surco succo

lan

pgp

an

cg

ch1

mg

eg

onc

rg

pn

mv en

pgp

vn

sbnt

pnc

iban

opn ps p1nc

lat mat mdf

es

irco of2 of3

p2nc

p3nc

p4nc

opnc

Figure 2.14. Architecture of the central nervous system. (a) Eupnoi: Rilaena triangularis (Phalangiidae), schematic transverse section of the protocerebrum, showing principal neuropils and tracts. Redrawn from Breidbach and Wegerhoff (1993). (b) Dyspnoi: Trogulus nepaeformis (Trogulidae), schematic sagittal view of the central nervous system, highlighting the neurosecretory system. Redrawn from Juberthie (1983). Abbreviations: aa, anterior aorta; abnc, aboral neurosecretory cells; af1, af2, ascending fascicles 1–2; an, accessory nerve; cg, cheliceral ganglion; ch1, first optic chiasma; eg, esophageal ganglion; en, esophageal nerve; es, esophagus; iban, inferior bilateral associative neuropil; irco, inferior rostral commissure; lan, lateral associative neuropil (= corpus peduncula, mushroom body); lat, lateral ascending tract; lnc, lateral neurosecretory cells; mat, median ascending tract; mdf, median descending tract; mg, midgut; mv, muscular valve; of1–of3, optic fasicles 1–3; ol1, ol2, optic lobes 1–2; on, optic nerve; onc, oral neurosecretory cells; opco, optic commissure; opn, opisthosomal nerve; opnc, opisthosomal neurosecretory cells; p1nc–p4nc, neurosecretory cells of pedal somites I–IV; pgp, paraganglionic plate; plnc, posterolateral neurosecretory cells; pn, pharyngeal nerve; pnc, neurosecretory cells of the palpal somite; ps, perineural sinus; rg, rostral ganglion; rn, rostral nerve; sbnt, subesophageal neurosecretory tract; suban, superior bilateral associative neuropil (central body); succo, superior caudal commissure; surco, superior rostral commissure; vn, ventral paraganglionic nerve.

ture has been studied most intensively in the phalangioid Rilaena triangularis by Breidbach and Wegerhoff (1993), and their findings are generally concordant with those from earlier studies of Phalangium opilio (Holmgren, 1916; Hanström, 1923) and the gonyleptid Acrographinotus (Holmgren, 1916). There are four main groups of neuropils, or synaptic centers, namely, the optic lobes, the superior bilateral associative neuropil (sban) or “central body,” the lateral associative bodies (lan) (corpora pedunculata, “mushroom bodies”), and the inferior bilateral associative neuropil (iban). There are two pairs of optic lobes; the first (distal) lobe receives axons from the optic nerve and sends projections to the second lobe via the first optic chiasma. Descending projections emerge from the second optic lobes and are distributed to ipsilateral neuropils via several pathways, to contralateral neuropils via the second optic chiasma, and to the subesophageal ganglion through the circumesophageal connectives. The lans are connected in one way or another to most of the other protocerebral neuropils and appear to be the primary site of neural integration. The

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sban receives ascending projections from the lans and contains three histologically different strata of unknown significance. The iban has a close association with the lans, including unusual fan-shaped fascicles. The basic architecture of the protocerebrum is similar to that of spiders (Breidbach & Wegerhoff, 1993). The cheliceral ganglion (deutocerebrum; Figure 2.14b: cg) sends and receives information to the chelicerae through a pair of well-developed cheliceral nerves. It is also associated with the rostral ganglion, which is positioned anteriorly just dorsal to the esophagus. It is a component of the sympathetic or stomatogastric nervous system that occurs in most arthropods. The rostral ganglion sends rostral nerves anteriorly along the pharynx and a pair of esophageal nerves posteriorly along the esophagus (Figure 2.14b). The esophageal nerves terminate in the esophageal ganglia, which contain several neuroendocrine cells that apparently control muscle activity of the midgut. The subesophageal ganglion of harvestmen (Figure 2.14b) encompasses all segmental ganglia posterior to the cheliceral somite, although there is often no gross morphological or even histological evidence in adults of the original opisthosomal ganglia. The nerves of the pedipalp and walking legs emerge from the subesophageal ganglion, as well as several opisthosomal nerves. As noted earlier, the so-called abdominal ganglia associated with the opisthosomal nerves are not actually part of the nervous system and may be hemocytopoeitic organs. The internal structure of the subesophageal ganglion was studied most thoroughly by Breidbach and Wegerhoff (1993) in Rilaena. The ganglia of the pedipalps and legs fuse to form a single large neuropil traversed by 10 pairs of longitudinal tracts. These tracts connect posteriorly to a circular opisthosomal tract and pass anteriorly into the supraesophageal ganglion through the circumesophageal connectives. The longitudinal tracts are connected to one another via a complex network of transverse tracts that repeats for each appendage. The two sides of the animal are connected by five commissures. The basic configuration of tracts in Rilaena is similar to that of the spider Cupiennius (Ctenidae). In contrast to the CNS, little work has been conducted on the peripheral nervous system. However, P. opilio was one of the first arachnids in which evidence of efferent regulation of sensory neurons via peripheral synapses was described (Foelix, 1975), but subsequent studies of the system have focused on other arachnids. Other work has concentrated on the neural mechanism that causes twitching of detached legs in phalangioids. Miller (1977) showed that spontaneous movements of the femurpatella and tibia-basitarsus joints are caused by pacemaker neurons in the femur that become active with any change that eliminates communication between the CNS and the pacemaker cells (e.g., appendotomy, amputation, damage to proximal nerves, damage to CNS, and hypoxia). Miller also found that the two leg joints involved are controlled by independent pacemakers and that there is no coordination between the two. The cycle frequency appears to be generated entirely within each pacemaker; there is no evidence of sensory feedback influencing the motor pattern.

Neurosecretion and neurohemal organs The neurohemal organs form part of the endocrine system of arthropods and other invertebrates. They produce, transport, or store neurosecretions (hormones)

Morphology and Functional Anatomy

that are released into the hemolymph or, in some cases, directly to target organs to regulate molting, maturation, vitellogenesis, and other physiological and developmental processes (Gupta, 1983). Pulmonate arachnids have an arterial system that penetrates the supra- and subesophageal ganglia and can have several neurohemal organs associated with different arteries, both inside and outside the central nervous system. In contrast, harvestmen, like other tracheate arachnids, replaced the cerebral arterial system with an arterial envelope that encloses the neural mass and major nerves within a perineural arterial sinus (Firstman, 1973; Figure 2.14b). The neurohemal organs of tracheate arachnids usually take the form of paraganglionic plates (PGPs), which are specialized glial cells located just beneath the neurolemma of the posterior circumesophageal region of the supra- and subesophageal ganglia. The PGPs receive hormones via tracts formed by axons of neurosecretory cells located at the periphery of the supra- and subesophageal ganglia (Gabe, 1954, 1955; Herlant-Meewis & Naisse, 1957; Naisse, 1959; Juberthie, 1964, 1965, 1983; Streble, 1966; Juberthie & Juberthie-Jupeau, 1974). The supraesophageal neurosecretory (NS) system comprises four paired groups of NS cells, the oral, aboral, lateral, and posterolateral NS cell groups (Figure 2.14b). The relative placement is fairly constant throughout the order, although cell number varies within a cell group. Hormones generated in the perikarya of the oral and aboral NS cells are exported via separate axon tracts that merge in the ventral region of the supraesophageal ganglion and then extend posteriorly to the PGP. The tracts associated with the lateral and posterolateral NS cells are not known, possibly because the diagnostic products are conducted rapidly and thus rarely observed “in transit” within histological sections. The subesophageal NS system consists of a metameric series of NS cells associated with the pedipalpal, pedal, and opisthosomal ganglia. A paired subesophageal NS tract is formed by axons from these cells. It travels anterodorsally and joins the supraesophageal tract en route to the PGP, where the NS products accumulate in axon terminals. There are several types of axon terminals situated near the proximal surface of the glial cells of the PGP that can be differentiated by the contents, size, and shape of their vesicles and, to some extent, by the manner in which material is secreted (Juberthie, 1983). The PGPs also receive axons of unknown function. In Trogulus, for example, there is a pair of accessory nerves in the supraesophageal region and a ventral paraganglionic nerve in the subesophageal region.

EYES Extant arachnids have two kinds of eyes, the lateral and median ocelli, which differ in their evolution, development, and morphology (Paulus, 1979). Lateral ocelli evolved through modification of compound eyes and develop embryologically from invaginated thickenings of the embryological epidermis. Lateral ocelli may have a tapetum, a proximal layer that reflects unabsorbed light back through the retina to enhance the efficiency of photon capture. Median ocelli are also widespread in arthropods. Their development is more complicated. In Opiliones and other arach-

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nids a transverse fold of ectoderm grows over the anterior part of the embryonic head to form parts of the supraesophageal ganglion, as well as three ectodermal layers that develop into different parts of the median eye (Moritz, 1957; D. T. Anderson, 1973; Muñoz-Cuevas, 1981). The distal layer forms the lentigen or lenssecreting cells and vitreous body, the middle layer forms the retina, and the proximal layer forms the subretinal membrane. Ancestral arachnids probably had both kinds of eyes, but absence of one or both is common in extant groups. Median ocelli are present in most Phalangida but are sometimes reduced or lost in cave- or soil-dwelling forms; lateral ocelli are absent. Several Cyphophthalmi have small photoreceptors near the base of the ozophore, but it is unclear whether these are vestiges of median or lateral ocelli. Stylocellus (Stylocellidae), for example, has one small cuticular lens and tapetum of undetermined construction located anterior to each ozophore (Hansen & Sørensen, 1904; Shear, 1993c). On the basis of their lateral position and presence of a tapetum, Shear (1993c) suggested that eyes in Stylocellus are true lateral ocelli (see also Mello-Leitão, 1944; Giribet et al., 2002). However, Jancyzk (1956) described a possible photoreceptor on the ozophore of Cyphophthalmus duricorius and indicated that its tracheal supply is homologous with that of median eyes in other harvestmen. Specifically, in both C. duricorius and phalangiids a major tracheal branch (ramus prosomae anterior) projects vertically from the main trunk and eventually splits to supply the anterior aorta and eyes (Kästner, 1933; Jancyzk, 1956; Figure 2.12c: ao, oc). On the basis of the tracheal evidence, the fact that median ocelli occur laterally in certain other harvestmen, such as biantids (Juberthie, 1964), and the presence of tapeta in median eyes of Pycnogonida (Giribet et al., 2002), a case can be made that photoreceptors in Cyphophthalmi are vestiges of laterally displaced median ocelli. It should be noted, however, that Juberthie (1961a, 1964) could not corroborate Jancyzk’s observations from his study of Siro rubens (Sironidae). A firm conclusion on the phylogenetic distribution and homology of photoreceptors in Cyphophthalmi will probably require new comparative anatomical or developmental research.

Eye structure The structure of well-developed median ocelli of several harvestman species has been studied in detail by Purcell (1894), Juberthie (1964), Curtis (1969, 1970), Muñoz-Cuevas (1981), and Schliwa (1979). Here the lens is a subspherical, transparent thickening of the cuticle secreted and subtended by a single layer of columnar lentigen cells derived from the epidermis (Figure 2.15a). This layer is called the vitreous body and, together with the lens, forms the dioptric apparatus (Muñoz-Cuevas, 1978). The vitreous body is separated from the underlying retina by a thin, acellular preretinal membrane. The retina is formed by retinula cells that send axons to the supraesophageal ganglion through the optic nerve. Sheath or glial cells are concentrated toward the base of the retina but send processes distally between the retinula cells. A layer of pigment cells surrounds the eye and prevents extraneous light from entering the retina through the translucent cuticle. The description of the retina provided here is based primarily on the electron-

Morphology and Functional Anatomy

Figure 2.15. Eye structure. (a–d) Schematic sections through eyes showing anatomical differences associated with ocular reduction. (a) Eupnoi: Odiellus gallicus (Phalangiidae), well-developed eye. (b) Dyspnoi: Ischyropsalis luteipes (Ischyropsalididae). (c) I. helwigii mulleneri. (d) I. strandi. All redrawn from Juberthie (1964). (e) Diagrammatic depiction of a retinula. Horizontal lines 1–3 indicate levels of cross sections depicted to the right. Based on descriptions and illustrations in Schliwa (1979). Abbreviations: ac, arhabdomeric cell; ctcl, cuticle; d, dendrite of arhabdomeric cell; dr, distal (“open”) rhabdom; drc, distal retinula cell; hdm, hypodermis; on, optic nerve; pgc, pigment cells; pr, proximal (“closed”) rhabdom; prc, proximal retinula cell; prm, preretinal membrane; rt, retina; rtla, retinula; vb, vitreous body. Scale bar applies to a–d.

microscopic studies of Opilio canestrinii conducted by Schliwa (1979). The basic functional unit of the arthropod retina is the rhabdom (Figure 2.15e: dr, pr), an organized array of microvilli that project into an extracellular space formed by one cell or multiple cells. A rhabdom is considered closed when its constituent cells (Figure 2.15e: pr) surround the extracellular space and separate it from other rhabdoms. In an open rhabdom, microvilli form an interconnected network among many cells (Figure 2.15e: dr). In general, closed rhabdoms are associated with greater visual acuity and require higher light levels to function optimally; open rhabdoms increase light detection at the expense of visual acuity. A section through the eye of a typical phalangiid (e.g., Opilio and Phalangium) reveals both kinds of rhabdoms. A layer comprising open rhabdoms is located distally, just below the preretinal membrane (Figure 2.15e). The closed rhabdoms occupy a much thicker layer proximal to the open rhabdoms (Figures 2.15a,e). The closed rhabdoms are elongated in the proximodistal axis parallel to rays of incoming light. In cross section the closed rhabdom has three radiating branches, with each branch formed primarily by one cell (Figure 2.15e). Radiating branches are typical of closed rhabdoms, but harvestmen may

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be unique in having each branch formed by one rather than two cells. The deepest portions of the retina contain somata of photoreceptive cells, interneurons (arhabdomeric cells), and sheath or glial cells, as well as axons that form the optic nerve. The photoreceptive cells are arranged in units called retinulae. Each retinula (Figure 2.15e) typically has four photosensitive rhabdomeric cells, each with extensive Golgi, rough ER, mitochondria, and screening-pigment granules (Johnson & Gordon, 1990). The three proximal rhabdomeric retinula cells form the closed rhabdom, but they taper distally, and only a small portion of each may participate in forming the open rhabdom. The typical distal rhabdomeric retinula cell sends three branches between or peripheral to the proximal cells. The branches may make a minor contribution to the closed rhabdom but expand distally and function primarily in forming the open rhabdom. The retinula also contains an arhabdomeric nonphotosensitive central cell (Figure 2.15e: ac). This cell sends a dendritic process distally into the closed rhabdom; the dendrite stops before reaching the open rhabdom (Schliwa, 1979). Lateral processes extend from the dendrite and intermingle with the microvilli of the proximal retinula cells. It is likely that the arhabdomeric cell acts as an interneuron that integrates information from the sensory cells or regulates their sensitivity. Similar cells are known only in the median and lateral eyes of scorpions and horseshoe crabs (Fleissner & Fleissner, 1999). Earlier workers apparently mistook the arhabdomeric cell as the central part of the proximal rhabdomeric cell (Purcell, 1894; Curtis, 1969, 1970) and thus erroneously reconstructed a basal cell with one central and three peripheral distal branches.

Structural variation The size and structural complexity of median ocelli vary considerably among harvestmen and are roughly correlated with the amount of light available within the habitat of a species. The eyes described in the previous section are typical of species that inhabit areas with direct or substantial indirect sunlight (Figure 2.15a). However, many harvestmen live in areas of reduced light (dense vegetation, leaf litter, soil, caves) and show concomitant changes in their visual systems. Several studies have focused on interspecific differences within Ischyropsalis and have documented structural changes associated with evolutionary regression of the visual system (Juberthie, 1964; Juberthie & Muñoz-Cuevas, 1973; Muñoz-Cuevas, 1981; Figures 2.15b–d). Specifically, simplification of eyes is associated with reductions in the convexity of the inner lens surface, number of retinulae, length of closed rhabdoms, depth and differentiation of the vitreous body, number of lentigen cells, and amount of screening pigment. In most cases it appears that evolutionary reduction of eyes is caused by paedomorphosis, or early termination of eye development; adults have eyes resembling those of the embryonic or juvenile stages of ancestors. The cave-dwelling I. strandi is exceptional in that early nymphal stages have small but complete eyes, and adults of some populations lose their eyes partially (Figure 2.15d) or entirely through a degenerative process.

Morphology and Functional Anatomy

REPRODUCTIVE SYSTEM The basic architecture of the reproductive tract is similar in male and female harvestmen (Kästner, 1935a; Figure 2.16). The gonad (testis, ovary) is U shaped with a mesodermal gonoduct (sperm duct, oviduct) emerging from each side. The gonoducts fuse and continue distally as a single duct, or uterus internus (vas deferens, uterus), which eventually becomes an ectodermal, cuticle-lined duct, or uterus externus (propulsive organ and ejaculatory duct, vagina), that travels through an eversible organ (penis, ovipositor). When inverted (Figure 2.16), the organ is housed within a pregenital chamber with flexible cuticular walls. The posterior end of the eversible organ attaches to the posterior end of the chamber. The walls of the pregenital chamber have muscles that attach to it laterally and to the genital sternite, and these appear to expand the pregenital lumen and initiate eversion, which is most likely completed by hemolymph pressure. A pair of retractor muscles originates at a posterior tergite and attaches to the proximal end of the eversible organ. There are often accessory glands associated with the walls of the pregenital chamber. Most re-

Figure 2.16. Diagrammatic ventral view of the reproductive system of both male and female harvestmen. The upper figure shows the eversible organ inverted; the lower shows the eversible organ everted. Male/female: gonad = testis/ovary; gonoduct = sperm duct/oviduct; uterus internus = vas deferens/uterus; uterus externus = propulsive organ and ejaculatory duct/vagina; eversible organ = penis (spermatopositor)/ovipositor. Based on de Graaf (1882a) and Kästner (1935a).

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search on the reproductive system has focused on the structure of the penis and ovipositor and has been inspired primarily by the search for characters of taxonomic or phylogenetic significance.

Penis The male eversible organ is usually called a penis, but van der Hammen (1985) noted that the corresponding structure in some Cyphophthalmi seemed too short to act as an intromittent organ, and he introduced the term spermatopositor (see also Chapter 12). The penis in Cyphophthalmi is usually short, with a ring of long setalike projections and several internal muscles (Martens, 1986). The penis in Phalangida has two main parts, a long shaft and a shorter terminal glans (Martens, 1986). The glans is a highly variable and sometimes complicated structure often equipped with spines, setae, and projections of various kinds; some are highly asymmetrical (see Chapter 4). In muscular penes the glans is moved relative to the shaft by one or two muscles that originate from the shaft and insert on a cuticular tendon that ends at the base of the glans. The shaft is typically sclerotized to prevent the longitudinal collapse of the shaft during muscle contraction. This type of penis occurs throughout Eupnoi, Dyspnoi, and in Insidiatores. Grassatores have hydraulic penes; the intrinsic muscles are absent, and the glans is apparently operated by internal hemolymph pressure. The shafts of hydraulic penes are often weakly sclerotized. It is important to note that the terms “muscular” and “hydraulic” refer to the operation of the glans only and not to the entire penis, as eversion and inversion are apparently achieved in all harvestmen by a combination of muscular and hydraulic mechanisms. Seminal products are apparently pushed through the long ejaculatory duct of phalangids through the action of a muscular propulsive organ located just proximal to the base of the penis. The propulsive organ is absent in Cyphophthalmi (Kästner, 1935a).

Ovipositor In Cyphophthalmi and most Eupnoi the ovipositor has a long shaft composed of segmentlike cuticular rings (Figure 2.9a) connected by segmentally arranged muscles. The ovipositor terminates in a furca formed by a bilateral pair of processes derived from divided cuticular rings, with the genital opening positioned basally between them. The furca represents one divided segment in Cyphophthalmi, but two or three in Eupnoi. Each process typically has a laterally placed, subterminal sense organ. Paired seminal receptacles occur just inside the genital opening. They are diverticula of the vagina, often sclerotized, and sometimes associated with glands (de Graaf, 1882a; Martens et al., 1981). Absence of seminal receptacles may indicate that the species is parthenogenetic. It is likely that the elongate, segmented ovipositor is primitive for Opiliones and that segmentation has been lost in several groups (Shultz, 1998). The ovipositors of most acropsopilionine caddids are very short and have only a few segments, but their architecture is basically similar to that of other Eupnoi. The ovipositor in Laniatores is unsegmented and terminates in four lobes. The vagina is X shaped in cross

Morphology and Functional Anatomy

section. Segmentation has also been lost in Dyspnoi, although segmental musculature has been retained in some Troguloidea, and the genital opening is formed by a pair of valves.

ACKNOWLEDGMENTS We are in debt to Juergen Gruber, who supplied Dyspnoi specimens, to Lara Maria Guimarâes for SEM images, and to Jochen Martens and Gonzalo Giribet for suggestions on an earlier version of this chapter. Jeffrey W. Shultz was supported by the Maryland Agricultural Experiment Station.

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3

Phylogeny and Biogeography Gonzalo Giribet and Adriano B. Kury

O

piliones are, together with Acari and Araneae, the most diverse group of arachnids, and they also present a great deal of body-plan disparity (see Chapters 1 and 2). Crown-group Opiliones were already around during the Devonian (see Chapter 5), which corroborates the idea of them being an old group of arachnids that has had time to evolve the enormous disparity observed in the extant harvestman fauna and to colonize all continents and major islands at all latitudes (see Chapter 7). The object of this chapter is to compile phylogenetic and biogeographic evidence to discuss the evolutionary relationships of Opiliones and to propose a working phylogenetic hypothesis.

PHYLOGENETIC STUDIES OF THE ORDER OPILIONES AND ITS RELATIONSHIPS TO THE OTHER ARACHNIDA In order to understand the evolution and origin of the order Opiliones, its phylogenetic placement within the arachnid tree of life needs to be considered. However, the phylogenetic position of Opiliones has remained one of the most contentious issues in arachnid systematics and requires extensive discussion. Fortunately, progress has been made in recent times, in part because of the use of sound phylogenetic methodologies applied to the analysis of morphological data (Shultz, 1990; Wheeler & Hayashi, 1998; Giribet et al., 2002), the careful study of new character systems, including skeletomuscular anatomy (Shultz, 2000), and the incorporation of molecular evidence into the toolkit of arachnid systematists (Wheeler & Hayashi, 1998; Giribet et al., 1999, 2002; Shultz & Regier, 2001). 62

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The issue of Opiliones monophyly and its components Before revising the phylogenetic placement of Opiliones, the issue of Opiliones monophyly needs to be addressed. Since the early recognition of Opiliones, only the discovery of Ricinulei and Cyphophthalmi has challenged the monophyly of the group. Hansen and Sørensen (1904) defined the order and largely established the modern systematics of the group as we recognize it today. Before Hansen and Sørensen, Latreille (1796, 1806) established the family Phalangida for the genera Galeodes (Solifugae), Phalangium (Eupnoi), Trogulus (Dyspnoi), and Siro (Cyphophthalmi). Sundevall (1833) excluded the genus Siro from his order Opiliones and placed it together with his family Galeodides, in his order Solpugae, together with his families Phrynides (Phrynus and Thelyphonus), Scorpionides, and Obisides—an artificial clade containing members of the current orders Opiliones, Solifugae, Amblypygi, Uropygi, Scorpiones, and Pseudoscorpiones. Koch (1839) included all the harvestman families in his order Solpugae, which also comprised the family Galeodides, following Latreille. Later he excluded the family Sironidae from this order (Koch, 1850). Thorell (1876) recognized three main harvestman lineages (“sections”): Palpatores (including Cyphophthalmi), Laniatores, and the new group Ricinulei. Afterward he presented a new division of the order Opiliones into four suborders: Palpatores, Laniatores, Anepignathi (= Cyphophthalmi), and Ricinulei (Thorell, 1892). Karsch (1892) removed the family Cryptostemmatoidae from Opiliones, and Hansen and Sørensen (1904) recognized it as an arachnid order, adopting for it the name Ricinulei, proposed by Thorell for his suborder of Opiliones. After this early period the order Opiliones was considered monophyletic and, to include what we currently recognize as its members, was generally arranged in three suborders: Cyphophthalmi, Laniatores, and Palpatores, the latter with the two tribes Dyspnoi and Eupnoi (e.g., Roewer, 1923). Only one historical note defied its monophyly. On the basis of phenetic criteria, Theodore Savory proposed that Cyphophthalmi be erected as a new arachnid order in a hilarious article reporting the results of an arachnological opinion poll, where the question of erecting the new order was asked. The results of this poll are not less amusing because of the sample size and responsiveness of the voting pool; two did not reply, two were uncertain “but favorably advised progress,” three were in disagreement, and four were strongly in favor (Savory, 1977). We were not told if the ones who disagreed were strongly against it or not. Unfortunately, democracy is no optimality criterion in systematics. The proposal was also justified phylogenetically: “Thus we come to look upon the Cyphophthalmi as the representatives of the ancestral group, from which have evolved the other orders of their subclass, namely the ‘Phalangida’ and the Ricinulei, both of which have passed beyond the stage of using a spermatophore” (Savory, 1977). No other researcher, to our knowledge, has followed such a proposal, and all phylogenetic analyses of harvestmen have corroborated the monophyly of Cyphophthalmi + Phalangida, even when including Ricinulei (e.g., Giribet, 1997; Giribet et al., 1999, 2002; Shultz & Regier, 2001). For a detailed explanation of the morphological characters found in the order, see Chapter 2.

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The sister taxon of Opiliones Although the monophyly of the order Opiliones is well accepted and corroborated by phylogenetic methodology, its sister-group relationships remain more contentious because of the number of phylogenetic trees that have been proposed for arachnids (see a summary of hypotheses in Wheeler & Hayashi, 1998). One of the most influential modern articles on chelicerate phylogenetics, the study of Weygoldt and Paulus (1979), proposed a sister-group relationship of Opiliones to a clade containing Acari and Ricinulei (Figure 3.1A). This system has been endorsed in some textbooks (Ax, 2000), but van der Hammen (1985), in the third part of his “Comparative Studies in Chelicerata” series, proposed the clade Myliosomata, grouping Opiliones, Xiphosura, and Scorpiones on the basis of their coxosternal feeding mode and the presence of a myliosoma. (A myliosoma is a more or less cone-shaped subdivision of the body with a complicated structure [van der Hammen, 1985: 26].) However, in the same article he also suggested an alternative relationship to Tetrapulmonata based on the development of the coxal glands and on the position of the spiracles (van der Hammen, 1985). A slight variation of that tree was published a year later (van der Hammen, 1986; Figure 3.1B). The current thinking until then was that the order Opiliones was related to Acari, as summarized by Shear (1982): “opilionids are evidently closest to some groups of mites.” The first numerical cladistic analysis of chelicerate relationships was the elegant study of Shultz (1990), who proposed a clade containing Opiliones, Scorpiones, Pseudoscorpiones, and Solifugae, which he named Dromopoda (see also Shultz, 1989). The specific position of Opiliones within Dromopoda was as a sister group to the clade Novogenuata (Scorpiones, Pseudoscorpiones, and Solifugae), also proposed by Shultz (1990; Figure 3.1C). The same result was obtained by Wheeler and Hayashi (1998) in the first total-evidence analysis of chelicerate relationships using morphological and molecular data. Some characters supporting this node are the extensor muscles and special articulations at the femoropatellar and patellotibial joints (Shultz, 1989, 1990), the transverse furrows of the prosomal carapace, a reduced intercoxal sternal region, the prosomal endosternite composed of two segmental elements, and perhaps the presence of a stomotheca later lost in Haplocnemata (Shultz, 1990). Another morphological analysis by Giribet et al. (2002) agreed with the monophyly of Dromopoda only when fossils were not taken into consideration, but the addition of relevant fossils such as Eurypterida, palaeophonid scorpions, Proscorpius, or Trigonotarbida resulted in an unresolved pattern that contained three alternative topologies: Dromopoda, Opiliones + Haplocnemata, or Opiliones + nonscorpion arachnids (Giribet et al., 2002). Clearly the addition of the fossils—especially the eurypterids and the putatively marine Paleozoic scorpions—has an effect of pulling scorpions down the tree. The combination of those morphological data with molecular sequence data of the nuclear rRNA genes shows the monophyly of Dromopoda, but the internal resolution of Dromopoda is affected by the inclusion of the fossil taxa. The combined analysis without fossils shows Dromopoda sensu Shultz (1990), but the analysis with fossils shows a sister-group relationship of Opiliones to Haplocnemata (Figure 3.1D).

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Figure 3.1. Hypothesis of relationships of Opiliones to other chelicerate groups as viewed by (A) Weygoldt and Paulus (1979), (B) van der Hammen (1986), (C) Shultz (1990), and (D) Giribet et al. (2002).

As the data (morphological and molecular) stand today, it seems that there is fairly good support for a Dromopoda clade that is also stable under model variation (see Giribet et al., 2002). However, the internal resolution of Dromopoda seems to change with the addition of fossil taxa, a possibility that had not been explored in Shultz (1990) or in Wheeler and Hayashi (1998). Furthermore, an explicit relationship of Opiliones and Scorpiones has been suggested on the basis of skeletomuscular anatomy (Shultz, 2000).

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THE GROUPS OF OPILIONES AND THEIR INTERRELATIONSHIPS An early attempt to produce a phylogenetic tree for the families of Opiliones was presented by Mello-Leitão (1944) on the basis of a few characters used in a hierarchical order (Figure 3.2). For Mello-Leitão there was a sister-group relationship between Cyphophthalmi and Palpatores, resembling the Cyphopalpatores hypothesis that Martens would propose decades later. Mello-Leitão considered Sironidae to be a sister group to a monophyletic group of extant Palpatores, but neither Eupnoi nor Dyspnoi were monophyletic in his scheme. Mello-Leitão also failed to recognize the dichotomy between Insidiatores and Grassatores, but it is interesting to note that he placed Oncopodidae in a rather basal position, as Silhavy (1961) would do decades later. Since the publication of Hansen and Sørensen’s (1904) monograph, the order

Figure 3.2. Evolutionary cactus of the Opiliones proposed by Mello-Leitão (1944).

Phylogeny and Biogeography

Figure 3.3. Alternative hypotheses for the evolution of Opiliones as envisioned by different authors. (A) Cyphopalpatores hypothesis of Martens (1976). (B) Classical hypothesis with Palpatores monophyletic, as in Hansen and Sørensen (1904) or Shultz (1998). (C) Dyspnolaniatores hypothesis of Giribet et al. (1999, 2002).

Opiliones has been recognized to contain three suborders: Cyphophthalmi, Palpatores, and Laniatores. They furthermore divided the Palpatores into two tribes, Eupnoi (containing the current Phalangioidea and Caddoidea) and Dyspnoi (containing the current Ischyropsalidoidea and Troguloidea). While this system has been mostly in use until modern times (Shear, 1982), Silhavy (1961) proposed to give Eupnoi and Dyspnoi a subordinal rank and proposed two new suborders for Laniatores, Gonyleptomorphi and Oncopodomorphi. Shear (1975a) explicitly rejected this system in order to preserve stability, especially in the case of Eupnoi and Dyspnoi. However, this system of classification was challenged by the prominent German arachnologist Jochen Martens, who proposed a radically new hypothesis of harvestman evolution based on the analysis of the genitalia (Martens, 1980). His Cyphopalpatores system (Martens, 1980, 1986; Martens et al., 1981) placed Cyphophthalmi within Palpatores, specifically as a sister group to Ischyropsalidoidea + Eupnoi, rendering Dyspnoi and Palpatores paraphyletic (Figure 3.3A). Since the Cyphopalpatores concept was proposed, it has been adopted in several arachnological studies and textbooks (e.g., Cokendolpher & Lee, 1993; Westheide & Rieger, 1996). Phylogenetic testing of the Cyphopalpatores system using modern cladistic techniques of both morphological and molecular data rejects Martens’s idea and places Cyphophthalmi as the sister group of the remaining harvestmen, the Phalangida (Giribet, 1997; Shultz, 1998; Giribet et al., 1999, 2002; Giribet & Wheeler, 1999; Shultz & Regier, 2001). All these studies found evidence for the monophyly of Phalangida, as well as for each one of the major lineages of Phalangida: Eupnoi, Dyspnoi, and Laniatores. However, disagreement emerged with regard to the status of Palpatores, which appear monophyletic in the studies of Shultz (1998; Shultz & Regier, 2001; Figure 3.3B), but Dyspnoi appeared as the sister group to Laniatores in the studies of Giribet (1997; Giribet et al., 1999, 2002; Giribet & Wheeler, 1999; Figure 3.3C). The new name Dyspnolaniatores was pro-

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posed on the basis of the stability of that clade to parameter variations in phylogenetic analyses (Giribet et al., 2002). A debate between both parties has been going on in recent literature, with critiques in both directions. However, both studies render very similar topologies for most lineages at all levels. The study of Shultz and Regier (2001) supports Palpatores on the basis of analysis of elongation factor-1␣ and RNA polymerase II, as well as the combination of these genes with the ribosomal RNA sequence data of Giribet et al. (1999). The analysis of Giribet et al. (2002) supports Dyspnolaniatores on the basis of the ribosomal and morphological data and includes a larger taxon sampling both within and outside Opiliones. This study furthermore attempts to look at stability, finding that the Palpatores hypothesis is marginally supported. In order not to confound the reader, we decided to follow the well-corroborated evidence—the monophyly of Cyphophthalmi, Phalangida, Eupnoi, Dyspnoi, and Laniatores—and will present sections on the relationships of the four major harvestman clades. Whether Palpatores or Dyspnolaniatores is accepted should not matter in the following sections.

Cyphophthalmi Cyphophthalmi is clearly a monophyletic group comprising six recognized families of small to medium-sized Opiliones thought to retain several plesiomorphies of the order Opiliones, although they may be highly autapomorphic for other characters. The group was clearly defined by Hansen and Sørensen (1904), who presented its first monograph, which is still the most important study of Cyphophthalmi anatomy. They identified two main lineages, which they called subfamilies Sironini [sic] and Stylocellini [sic]. They differ in having a movable coxa I and fused coxae II, III, and IV in Stylocellini, or free coxae I and II in Sironini, among other features. That classification remained in place until the seminal cladistic analyses of Shear (1980, 1993b), who proposed a new system consisting of two infraorders, Temperophthalmi and Tropicophthalmi, which correspond mainly to the Sironinae and Stylocellinae of Hansen and Sørensen. Temperophthalmi currently includes the single superfamily Sironoidea with three families, Troglosironidae, Sironidae, and Pettalidae. Tropicophthalmi is comprised of the superfamilies Stylocelloidea and Ogoveoidea, the first with the family Stylocellidae, and the second with the families Ogoveidae and Neogoveidae. While the main characteristic used by Hansen and Sørensen and subsequent workers for separating the two main lineages is highly conserved, taxa with exceptional articulation of the coxae II have been described: the sironid genera Paramiopsalis and Iberosiro have the second coxae of the legs fused to the third, as in the members of the Tropicophthalmi. Furthermore, “Neogovea” mexasca has a free second coxa, unlike the members of Neogoveidae, but this species now seems to be unrelated to Neogoveidae (Giribet & Boyer, 2002). Although a recent cladistic morphological analysis of most Cyphophthalmi genera (Giribet & Boyer, 2002) agrees with Shear’s (1980) phylogeny in the monophyly of Pettalidae and of Stylocellidae, no support was found for the monophyly of Sironidae, Neogoveidae, or Ogoveidae sensu Shear (1980). Furthermore, the division

Phylogeny and Biogeography

between Tropicophthalmi and Temperophthalmi does not seem to be supported by either morphological or molecular data. The analysis from Giribet and Boyer (2002) is unresolved in many aspects and, like that of Shear (1980), lacks a proper criterion for defining the root position within Cyphophthalmi. In that respect a molecular analysis of 18S rRNA and 28S rRNA sequence data, using other harvestmen as outgroups, suggests two alternative rooting positions for Cyphophthalmi: (a) between Stylocellidae and the remainder families or (b) between Pettalidae and the remainder families. The latter option is favored in recent unpublished analyses that include a much larger diversity of Cyphophthalmi sequences. A major disagreement between the hypotheses of Shear (1993b) and Giribet and Boyer (2002) is the phylogenetic position of Troglosironidae. Shear (1993b) postulated that Troglosiro is the sister group to a clade formed by Sironidae + Pettalidae, hence assigning to it a familial status. However, since the discovery of the first Troglosiro species (Juberthie, 1979), it has been noticed that the opisthosomal sternal region of the male bears glandular pore openings, as in the Neotropical genus Huitaca and in the African genus Ogovea. These structures were not seen as homologous according to their different position in the opisthosomal sternites (Shear, 1979a). More recently, other types of glandular openings have been observed in the opisthosomal sternal areas of the males in several species of American and African Neogoveidae (Giribet & Boyer, 2002; Giribet & Prieto, 2003; Sharma & Giribet, 2005). The presence of opisthosomal sternal glands in the males of members of Troglosironidae, Ogoveidae, and Neogoveidae may reflect apomorphy. Although this remains to be tested morphologically, DNA sequence data suggest that Neogoveidae and Troglosironidae form a monophyletic group. Given the current uncertainty about the position of the root in the Cyphophthalmi tree, it is not possible to discuss evolution of most characters in the group. However, at least two more character systems deserve special attention, although their polarity is essential to understand the evolution within the group. One character is the presence of eyes in most members of Stylocellidae and in several pettalid species from Sri Lanka, Chile, and Australia. The second character is the evolution of the anal pore glands in Sironidae, Pettalidae, and Stylocellidae. Most Cyphophthalmi are blind, although many members of the family Stylocellidae bear a pair of eye lenses in lateral position, frontal to the ozophores. Likewise, members of the pettalid genera Pettalus and Chileogovea and some undescribed Australian pettalids bear eyes incorporated into the base of the ozophore (Juberthie, 1989; Sharma & Giribet, 2006). The identity of these eyes is still disputed. Some authors think that they are homologous to the median eyes of other harvestmen, median eyes that migrated to the edges of the dorsal scutum. However, the eyes of stylocellids appear almost completely transparent with a reflective tapetum, which led Shear (1993c) to postulate that the stylocellid eyes are homologous to the lateral eyes of other arachnids (see Sharma & Giribet, 2006). However, no ultrastructural study of the Cyphophthalmi eyes has been completed. Irrespective of their final status, the eyes of Cyphophthalmi seem to be a plesiomorphic condition lost in several lineages of the group.

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Anal gland pores in opisthosomal tergites VIII and IX have been widely described for male members of Sironidae and Pettalidae (Juberthie, 1962, 1967; Shear, 1980; Giribet & Boyer, 2002; de Bivort & Giribet, 2004) but have not been recorded for the families Neogoveidae, Ogoveidae, or Troglosironidae. The finding of a similar gland pore in Fangensis leclerci from Thailand (Rambla, 1994) led her to classify this species in the family Sironidae. Examination of other Fangensis species led to the inclusion of the genus within the family Stylocellidae (Giribet, 2002; Giribet & Boyer, 2002). Anal gland pores have since been discovered in other stylocellids of the genera Fangensis and Stylocellus, including the species type of the family, S. sumatranus (Schwendinger et al., 2004; Schwendinger & Giribet, 2005). Interestingly, the Cyphophthalmi families that lack anal gland pores have other special glandular openings in the anterior opisthosomal sternal area, and these glands are now thought to be probable homologues of the gland opening in the anal region in pettalids, sironids, and stylocellids (Sharma & Giribet, 2005). Therefore, it may seem reasonable to think that the primitive Cyphophthalmi had eyes and a male with either anal or opisthosomal sternal gland pores and an adenostyle. With the exception of the ozophores, no other homologous glandular systems can be found in the other harvestman lineages. With respect to the genitalia, Cyphophthalmi are supposed to have plesiomorphic conditions for many of the characters, with a muscular spermatopositor and a long segmented ovipositor with sensory structures at the tip. However, the lack of similar structures outside Opiliones does not allow testing this hypothesis further. The presence of spermatophores in some species of Sironidae and Stylocellidae (Karaman, 2005; Schwendinger & Giribet, 2005) may require detailed comparison with other arachnid spermatophores.

Phalangida Variations of the name Phalangida have been commonly used as synonyms to Opiliones, especially in the North American literature since the late nineteenth century (e.g., Banks, 1900; Bristowe, 1949; Edgar, 1990). However, recently the term Phalangida has been applied to the clade formed by Eupnoi, Dyspnoi, and Laniatores, and we use it as such here.

Palpatores Given that the higher taxon Palpatores has been used in numerous studies of harvestman taxonomy and systematics—irrespective of whether it is monophyletic (Hansen & Sørensen, 1904; Roewer, 1923; Shultz, 1998), paraphyletic to the inclusion of Cyphophthalmi (Martens, 1980, 1986; Martens et al., 1981), or paraphyletic to the inclusion of Laniatores (Giribet et al., 1999, 2002)—we are forced to discuss it. Although most of the discussion of its subgroups—Eupnoi and Dyspnoi— can be achieved independently, some of the early work, especially that before Hansen and Sørensen (1904), did not differentiate among these two groups and requires the use of the name “Palpatores.”

Phylogeny and Biogeography

One of the earliest attempts to provide a phylogenetic classification for Palpatores was given by Pocock (1902b). He used the name Plagiostethi (= Palpatores), which was divided into Apagosterni and Eupagosterni, and this classification was followed by other authors (e.g., Roewer, 1910). Apagosterni included the current Phalangioidea and Ischyropsalididae (Phalangiidae and Ischyropsalidae of Pocock); and Eupagosterni included the families of the current Troguloidea (Nemastomidae, Dicranolasmidae [sic], and Trogulidae of Pocock). Nonetheless, most authors of the late nineteenth and early twentieth centuries used taxonomic systems that reflected an understanding of the two palpatorean lineages (Sørensen, 1873; Thorell, 1876, 1877; Hansen & Sørensen, 1904; Roewer, 1923), about which Pocock (1902b: 504) stated that “these conceptions are unquestionably erroneous.” Other authors preferred not to define suprafamilial taxa within Palpatores and used the four recognized families (Phalangiidae, Ischyropsalididae, Nemastomatidae, and Trogulidae, with variable spellings) without specifying their relationships (e.g., Simon, 1879a). Shear (1975a) proposed classifying Palpatores into three superfamilies, Troguloidea (Trogulidae, Nemastomatidae, Ischyropsalididae, Sabaconidae), Phalangioidea (Phalangiidae, Neopilionidae, Leiobunidae, Sclerosomatidae), and Caddoidea (Caddidae). His Troguloidea corresponds to Dyspnoi, while the other two superfamilies comprise the current Eupnoi. Since the widely used classification of Hansen and Sørensen (1904), the only influential articles that have questioned the monophyly of Dyspnoi are the studies of Martens and collaborators proposing the Cyphopalpatores hypothesis. But no phylogenetic testing has ever rendered Cyphopalpatores, and all studies have recognized the two main palpatorean lineages, Eupnoi and Dyspnoi. In fact, these two categories have been used in several taxonomic studies (e.g., Starega, 1976a).

Eupnoi Eupnoi constitutes a clear monophyletic group containing the best-known harvestmen from the Northern Hemisphere, the members of the families Phalangiidae and Sclerosomatidae. Knowledge of the European Eupnoi species is exemplary, and most species were already included in the seminal monograph of Martens (1978b). Currently Eupnoi includes the two superfamilies Phalangioidea and Caddoidea (Shear, 1982). The monophyly of a selected group of members of Phalangioidea has been shown in current phylogenetic analyses (Giribet et al., 1999, 2002; Shultz & Regier, 2001), but the monophyly of Caddoidea reminds yet to be tested phylogenetically. Caddoidea includes the single family Caddidae with two subfamilies, Caddinae and Acropsopilioninae (Shear, 1975a). Phalangioidea is a much larger group, with five families recognized: Phalangiidae, Sclerosomatidae, Neopilionidae, Monoscutidae, and Protolophidae, as well as a few species of uncertain affinities (Cokendolpher & Lee, 1993). Although the monophyly of Phalangioidea has been assumed, only the families Phalangiidae and Sclerosomatidae and a genus of uncertain position, Dalquestia, have been analyzed phylogenetically (Giribet et al., 1999, 2002; Shultz & Regier, 2001). Taxonomic delimitation of the families and

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subfamilies within Phalangioidea remains uncertain in many cases, and no attempt to study the phylogeny of the entire superfamily has been made, despite the fact that this group contains the most typical forms of Opiliones. Hunt and Cokendolpher (1991) presented a cladistic analysis of Phalangioidea restricted to Southern Hemisphere nonentapophysate species. Unfortunately, their results are difficult to interpret in a strict parsimony sense because preferred trees (and not the consensus of the shortest trees) were presented, rooting was done with a hypothetical ancestor, and several hypotheses were proposed after the analysis. Certainly Eupnoi is in urgent need of further systematic study.

Dyspnolaniatores The taxon Dyspnolaniatores was formalized by Giribet et al. (2002) on the basis of phylogenetic evidence presented in this and previous studies combining morphological and molecular evidence (Giribet, 1997; Giribet et al., 1999; Giribet & Wheeler, 1999). The group is comprised of Dyspnoi and its sister group, Laniatores. As mentioned earlier, this was questioned by another phylogenetic analysis based on a different set of molecular characters (Shultz & Regier, 2001), although the analysis from Shultz and Regier is more restricted in terms of taxon sampling and did not include outgroup taxa outside the Opiliones. Both studies show alternative resolutions, and conflict among the loci employed cannot be ruled out, as shown in an analysis of centipede relationships (Giribet & Edgecombe, 2006). Overall, the ribosomal genes are more congruent with morphology than elongation factor-1␣ or RNA polymerase II, as shown in the resolution within the superfamily Ischyropsalidoidea (Shultz & Regier, 2001). Dyspnolaniatores can be diagnosed by the lack of a jointed ovipositor.

Dyspnoi Among the groups of Opiliones, Dyspnoi is perhaps the one that has received the most phylogenetic attention, from both morphological and molecular points of view. The group is restricted to the Northern Hemisphere, and its fauna has been worked extensively (Suzuki, 1965, 1974; Shear, 1975b, 1986; Martens, 1978b; Shear & Gruber, 1983). Dyspnoi is clearly monophyletic, despite Martens’s polyphyletic proposal (Martens, 1980, 1986; Martens et al., 1981). Both morphological cladistic analyses and molecular studies (see previous references) have corroborated the monophyly of the group and clearly show that it is divided into two major lineages— Troguloidea and Ischyropsalidoidea (Martens, 1976)—each receiving the rank of superfamily. Relationships within Ischyropsalidoidea have been investigated in detail (Shear, 1986; Shultz & Regier, 2001; Giribet et al., 2002). It is comprised of three families: Ischyropsalididae, Ceratolasmatidae, and Sabaconidae. From the characters used by Shear (1986) to diagnose the superfamily (presence of metapeltidial sensory cones, loss of segmentation in the ovipositor, reduced or absent pedipalpal claws, and the presence of cheliceral glands in males), none are considered autapomorphic; they

Phylogeny and Biogeography

are Dyspnoi characters, or they may be plesiomorphic or convergent with other Opiliones (see a discussion in Giribet et al., 2002). Disagreement exists over the status of Ceratolasmatidae and Sabaconidae, since molecular analyses tend to place the ceratolasmatid Hesperonemastoma with the sabaconid Taracus. Given the necessity of including members of the genera Crosbycus and Acuclavella in the molecular studies, taxonomic amendments should await more careful studies within the superfamily. The second superfamily of Dyspnoi, Troguloidea, includes the families Trogulidae, Nemastomatidae, Dicranolasmatidae, and Nipponopsalididae, distributed in the Northern Hemisphere. The phylogeny of the nemastomatid subfamily Ortholasmatinae has been investigated by Shear and Gruber (1983). The monophyly of Troguloidea has also been corroborated by morphological and molecular studies (Shultz & Regier, 2001; Giribet et al., 2002) that mostly agree on the following scheme: (Nipponopsalididae (Nemastomatidae (Dicranolasmatidae + Trogulidae))) (Shultz, 1998; Giribet et al., 2002). This group is supported by a similar type of sternum (Hansen & Sørensen, 1904) and by genitalic characters: two muscles in the penis, aciniform vaginal glands in the ovipositor, and outer circular muscles in the ovipositor (Martens et al., 1981; Martens, 1986). Given the evidence for the monophyly of Dyspnoi and the well-delimited number of families and genera, we expect that a more comprehensive phylogenetic study of Dyspnoi will be obtained in the near future. One item remains, though, which is the presence of certain characters, thought to be typical of Troguloidea, in some Caddoidea: metapeltidial sensory cones (Shultz, 1998) and plumose pedipalpal setae with distal clusters of microtrichia (Shear, 1986; Shultz, 1998). The latter character has also been observed in juveniles of different species of Eupnoi (Hunt & Cokendolpher, 1991).

Laniatores Thorell (1876) coined the names Palpatores (Latin palpator, a stroker; a flatterer) and Laniatores (Latin lbniator, butcher) as the first division of Opiliones. While Eupnoi and Dyspnoi were known for a long time and some species were included in the Linnaean classification (Linnaeus, 1758), the first laniatorean was not described until 1818 (Gonyleptes horridus), from Brazil. More Laniatores, especially from Brazil, started to be revealed through the work of Perty (1833). Hope (1837) described a Brazilian Mitobatinae (Gonyleptidae) as an example of an intermediate between Palpatores and Laniatores. What we now call Travunioidea took many years to be discovered. European species were at first put in Scotolemon (Phalangodidae), as was the South African Phalangium rugosum. Simon’s classification of Laniatores (Simon, 1879b) recognized three families, namely, Phalangodidae, Cosmetidae, and Gonyleptidae. Phalangodidae included future members of almost every family. It is noteworthy that Cosmetidae and Gonyleptidae are now deemed to be very closely related families, so Simon’s system detached a specialized group, making a large paraphyletic Phalangodidae. Loman (1902) first recognized the morphological gap between Travunioidea

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(then all in a single family Triaenonychidae) and the other Laniatores and proposed a new suborder for this family—Insidiatores (Latin insidiator, a soldier lying in ambush, one who lies in wait, a lurker)—but this change was mostly not incorporated by subsequent authors. Loman’s concept did not extend to Travuniidae, whose few species known were then placed within Phalangodidae. The nominal family would still take 30 years to be discovered. Pocock (1902a) divided Simon’s Mecostethi into Insidiatores (including his Triaenonychidae, Triaenobunidae, and Adaeidae) and Laniatores, a classification system followed by Roewer (1910). In the beginning of the twentieth century, all previous work was obscured by the unwavering labor of Roewer (see Chapter 1). This indefatigable German author established the base of most future harvestman systematics by using an artificial system based on a few “rank-worthy characters.” Roewer (1923) recognized six families with 32 subfamilies in Laniatores, without grouping any of these families in larger units. Other authors (e.g., Mello-Leitão, 1932, 1938, 1949) expanded some taxa, but did not propose suprafamilial groups in Laniatores. Kratochvíl (1958a) proposed two superfamilies based on claw structure: Oncopodoidea (with six families) and Travunoidea [sic] (with three families). The incorrect derivation of the superfamily name was corrected by Shear (1977) to Travunioidea. Shortly after Kratochvíl’s scheme, a new one was proposed by Silhavy (1961), who split Laniatores into two suborders: Gonyleptomorphi (containing the superfamilies Gonyleptoidea and Travunioidea) and Oncopodomorphi. Both systems recognized three basic groups: (1) the small group Oncopodoidea from Southeast Asia, (2) the families with elaborately branched single claws in the hind legs and muscular penises (Travunioidea, from northern and southern [mostly temperate] latitudes), and (3) the large tropical Gonyleptoidea, with double claws in the hind legs and hydraulic penises lacking musculature. The fundamental difference between the two systems was the internal relationship of these groups: (Travunioidea (Oncopodoidea + Gonyleptoidea)) (Kratochvíl, 1958a) or (Oncopodoidea (Travunioidea + Gonyleptoidea)) (Silhavy, 1961). Martens (1980) published the first comprehensive phylogenetic analysis of Opiliones, dividing Laniatores into three superfamilies, following Kratochvíl’s (1958a) scheme. However, Martens did not use numerical cladistics and relied on an evolutionary scenario to polarize his characters. He also extrapolated character states for some taxa (notably Travunioidea) on the basis of preconceived ideas of phylogeny. As usual at that time, terminals for the cladistic analysis were based on groundplans instead of species. More recently (Martens, 1988; Starega, 1989, 1992; Kury, 1992a,b), certain familial diagnoses were questioned. Kury (1992a, 1993a, 1994a,b, 1997a,b) proposed phylogenetic hypotheses for some families of Gonyleptoidea, but there is no proposed phylogeny for the entire Laniatores. The monophyly of Travunioidea and Triaenonychidae was rejected by Dumitrescu (1975a, 1976) on the basis of detailed examination of the intestinal diverticula (see Chapter 2). The tripartition of the diverticulum tertium into a ramus medianus, ramus lateralis, and ramus exterior stands as a

Phylogeny and Biogeography

putative synapomorphy of Gonyleptoidea (Cosmetidae + Phalangodidae + Assamiidae + Gonyleptidae + Stygnidae) plus Synthetonychia and the southern Triaenonychidae (Adaeulum + Larifuga + Tasmanonyx + Paranuncia + Nuncia). This contrasts with the plesiomorphic bipartite condition of most Travunioidea, namely, Travuniidae (Peltonychia + Speleonychia), Northern Hemisphere Triaenonychidae—for which Dumitrescu coined the name Sclerobuninae (Sclerobunus + Zuma)—Paranonychus, and Pentanychus. The quadripartite condition of the diverticulum primum is a putative apomorphy for the Southern Hemisphere Triaenonychidae. The character used to distinguish families in Travunioidea—the claw structure—varies within a single genus (Hunt & Hickman, 1993). Maury (1988) also acknowledged a set of characters that make difficult the placement of a cave-dwelling Argentinean relict, Picunchenops spelaeus, which ended up in Triaenonychidae. According to the phylogeny proposed by Martens (1980), Oncopodoidea and Gonyleptoidea constitute a monophyletic group, defined mainly by the hydraulic penis lacking musculature (Martens, 1976). Kury informally called this group Grassatores (from Latin grassator, a disorderly person, one who goes rioting about, especially at night, whether for fun and enjoyment or for robbery), a name used by Giribet et al. (2002) and formalized in the catalogue of the New World Laniatores (Kury, 2003). The three superfamilies of Martens (1980)—Travunioidea, Oncopodoidea, and Gonyleptoidea—were recovered in two recent combined molecular and morphological analyses (Giribet et al., 1999, 2002), although taxonomic coverage for Laniatores was restricted to a few species. Molecular-only-based analyses failed to recover monophyly of Triaenonychidae, the only family of travunioids sampled so far (Shultz & Regier, 2001; Giribet et al., 2002). Kury (1993a) pursued the issue of the basic division within Laniatores and has shown further evidence for a diphyletic Travunioidea, refuting Martens’s dichotomy of Oncopodoidea versus Gonyleptoidea (Kury, 2002). Other preliminary conclusions indicate that the widely accepted Travunioidea (= infraorder Insidiatores) does not form a clade (nor do Triaenonychidae sensu lato). “Travunioidea” can be arranged in two clades, here called superfamilies Travunioidea and Triaenonychoidea. The Northern Hemisphere Triaenonychidae (except for the remarkable Fumontana) group with Travuniidae. All Southern Hemisphere Triaenonychidae plus the New Zealand Synthetonychiidae form a clade. Pentanychidae could well form the sister group to all other Laniatores because of the plesiomorphic retention of all opisthosomal sclerites, as in Cyphophthalmi, Eupnoi, and Dyspnoi, but this remains to be tested. So far, molecular analyses relying on nuclear ribosomal genes support monophyly of Gonyleptidae + Cosmetidae + Stygnopsidae + Phalangodidae and do not support Phalangodoidea (= Phalangodidae + Oncopodidae) (Giribet et al., 1999, 2002). Molecular analyses relying on nuclear protein-coding genes support monophyly of Gonyleptidae + paraphyletic Phalangodidae (Shultz & Regier, 2001), but this study did not include Oncopodidae. With such a limited familial sampling, conclusions based on molecular sequences should await further data.

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Martens et al. (1981) provided a nice overview of the structure of ovipositors in representative harvestman species. Many of the phylogenetic conclusions on larger groups are based on those observations. However, their sampling for Travunioidea did not include any Southern Hemisphere species. The derived state of their character “loss of longitudinal inner musculature of ovipositor” supporting the monophyly of Travunioidea (Martens et al., 1981) is based on a state that occurs in three species only (Holoscotolemon unicolor and Theromaster brunnea, both Cladonychiidae, and Peltonychia clavigera, Travuniidae). These species surely form a monophyletic group, but the character state in Triaenonychidae sensu lato remains unknown. The cladistic analysis of Giribet et al. (2002) defended the monophyly of Travunioidea, coding this state in species where the character is unknown, two Southern Hemisphere and one North American Triaenonychidae (Equitius, Triaenobunus, and Zuma). Another problem is the number of apical lobes. This character was extrapolated for all Travunioidea, but it was known for three species of two families in Martens et al. (1981). Descriptions and illustrations of the Pentanychidae Sclerobunus and Paranonychinae (Briggs, 1971a,b) confirm the apomorphic number of four lobes. However, in Picunchenops it is explicitly said to be bilobed, the plesiomorphic state (Maury, 1988), and in all Southern Hemisphere Triaenonychidae (Kauri, 1961) and Fumontana (J. C. Cokendolpher, pers. comm.) it is also bilobed. Forster (1954) did not make any reference to the ovipositor in Synthetonychiidae. Detailed study of the descriptions and illustrations of ovipositors in Martens et al. (1981) reveals a misinterpretation of Martens’s character 23, which supports all nononcopodid Laniatores with penises lacking musculature (his “Gonyleptoidea”). The concentration of glands for oviposition is considered apomorphic, while the presence of diffuse glands in Oncopodidae (Martens et al., 1981) is considered plesiomorphic. Outgroup comparison illustrates that the condition found in Phalangodidae, Gonyleptidae, and other families is similar to the condition found in species of Dyspnoi and Travunioidea and therefore probably plesiomorphic, while the condition in Oncopodidae is apomorphic. These characters are unknown for the vast majority of Laniatores. On the basis of Kury (1992a, 1993a, 1997a,b, 2002, and unpublished analyses), the phylogeny of Laniatores can be reconstructed with a first split between Travunioidea and Triaenonychoidea + Grassatores, the latter group including Zalmoxoidea, Samooidea, Phalangodoidea, Epedanoidea, and Gonyleptoidea. In this scheme Travunioidea includes the Northern Temperate Insidiatores (Travuniidae, Cladonychiidae, Triaenonychidae, Pentanychidae); Triaenonychoidea includes the Southern Temperate Insidiatores (Triaenonychidae, Adaeini, Triaenobunini, Synthetonychiidae) + Fumontana; the other superfamilies are Zalmoxoidea (Icaleptidae, Guasiniidae, Zalmoxidae + Fissiphalliidae), Samooidea (Samoidae + Podoctidae + Biantidae + Kimulidae + Stygnommatidae), Phalangodoidea (Phalangodidae + “Pyramidopidae”? + Oncopodidae?), Epedanoidea (Epedaninae + Acrobuninae + Sarasinicinae), and Gonyleptoidea (Assamiidae + Stygnopsidae + Agoristenidae + Manaosbiidae + Cranaidae + Stygnidae + Cosmetidae + Gonyleptidae) (Figure 3.4).

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Figure 3.4. Summary tree of harvestman relationships with monophyly of Phalangida and paraphyly of Palpatores, as in Giribet et al. (2002), and with Laniatores reflecting the hypotheses of Kury (1992b, 1993a, 1997a,b, and unpub. data). Cyphophthalmi are shown mostly unresolved because of the conflictive hypotheses of Shear (1980), Giribet and Boyer (2002), and Giribet (unpub. data).

Phylogenetic conclusions Elucidating the evolutionary history of the order Opiliones is an exciting research topic that has been explored in depth during the last two decades with the application of cladistic methodology, including parsimony analyses of morphology and molecular data. The number of phylogenetic analyses of Opiliones has grown steadily during this period, and we expect it to keep growing in the coming years. Areas that will need special attention are the relationships within Phalangioidea, relationships among the laniatorean families, and internal analyses of many families whose monophyly has been questioned (e.g., Sironidae, Ceratolasmatidae, Sabaconidae, Triaenonychidae). Having a sound phylogenetic hypothesis that includes representatives of most harvestman genera seems an achievable goal for the next decade or so. A summary phylogenetic account of Opiliones, as we currently recognize it, is provided in Figure 3.4.

THE GROUPS OF OPILIONES AND THEIR BIOGEOGRAPHY Opiliones are rather unusual among arthropods in having limited dispersal ability, as a consequence of their low vagility (with the exception of some temperate Eupnoi). This limitation in colonizing new environments causes present-day distribu-

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tions to reflect historical changes in addition to ecological constraints. Opiliones are therefore a prime candidate group for biogeographic studies. Early workers on systematics had a rather casual approach to biogeography. This is especially true in reference to Carl F. Roewer, who erected taxonomic groups with disjunct distributions that make no sense phylogenetically—the most blatant example being the subfamily Tricommatinae (Roewer, 1935a), based on species from Europe, South America, and Malaysia. Current views place the species of Tricommatinae in at least three different families. Mello-Leitão took biogeography into consideration, but his taxonomic inaccuracy resulted in errors such as the southern Brazilian “podoctid” that happened to be a triaenonychid (Soares & Soares, 1979). Despite the high endemicity of most Opiliones, Goodnight and Goodnight (1951, 1983) failed to recognize the diversity of the current Stygnommatidae and treated them as a single widespread species. Few studies explicitly summarized or discussed species distributions. Loman (1900) presented a clear overview of the global distribution of all harvestman families. Mello-Leitão (1936) proposed a scenario to explain present-day distribution of Gonyleptidae (then including also Cranaidae and Manaosbiidae) and hypothesized a center of origin in the Colombian highlands. Forster (1954) provided detailed distributions of New Zealand Cyphophthalmi and Laniatores. Kratochvíl (1958a) provided distribution maps for the European Cyphophthalmi and relictual Laniatores. Lawrence (1959) discussed relationships among the Madagascan fauna. Kauri (1961) mapped the distribution of the South African species and explained their relationships. Suzuki (1967, 1972b, 1977a) assessed the Japanese biogeography. Silhavy (1979) provided worldwide records for samoids. Starega (1984) offered a scenario to explain the dispersal of Phalangiinae in Africa and later (Starega, 1989) retook Kauri’s discussion on the relationships of the South African fauna. Ringuelet (1959) offered an organization of the zoogeographic areas in Argentina, later refined by Acosta (2002a). For Cyphophthalmi, several authors have provided the distributional ranges for the families and genera (e.g., Juberthie, 1970b; Shear, 1980; Giribet, 2000). The first biogeographic analysis in Opiliones presented a Brooks parsimony analysis of the Brazilian Atlantic forest using the distributions and phylogeny of Mitobatinae (Kury, 1991). Pinto-da-Rocha (2002) presented an analysis for Caelopyginae, Silva (2002) studied the biogeography of Goniosomatinae, and Pinto-daRocha et al. (2005) analyzed the records of occurrence of 84 species of Laniatores and Eupnoi in 11 areas of the Atlantic rain forest of Brazil.

Zoogeographic realms In order to discuss the zoogeographic relationships of the different harvestman taxa, we employ the traditional zoogeographic realms: Afrotropical, Australian, Indo-Malayan, Nearctic, Neotropical, Palearctic, and Oceanian. Four areas that show overlap between major zoogeographic realms are China, Indonesia, Japan, and Mexico, and they require particular discussion. For example, regarding the har-

Phylogeny and Biogeography

vestman fauna, the Japanese islands show a progressive predominance of IndoMalayan versus Holarctic elements toward the south (Suzuki, 1967). Likewise, the Mexican states present more Neotropical-related fauna toward the south (Kury & Cokendolpher, 2000). A few current biogeographic terms are defined here:

• • • • •

Amphipacific (= Amphiberingian, northern transpacific disjunctions): North America and Japan/eastern Asia Temperate Gondwana: Southern South America, southern Africa/Madagascar, India/Sri Lanka, Australia, New Zealand, and New Caledonia Amphinotic (= Austral): Temperate Gondwana without southern Africa/Madagascar Tropical Gondwana: Neotropics, central Africa Wallacea and Sundaland: The continental and insular components of the Malayan Peninsula, including Sumatra, Borneo, Java, and Sulawesi

Cyphophthalmi Cyphophthalmi have championed biogeographic explanations in harvestmen. Its members are found in all continents and major islands of continental origin, with the exception of Antarctica, where they are supposed to have become extinct (Figure 3.5). They have not been able to disperse to any oceanic islands, and instances of recent dispersal between separate landmasses have not been demonstrated. Each of the six recognized families has a well-characterized biogeographic distribution (Figure 3.5): Sironidae has a Laurasian distribution; Neogoveidae is restricted to cir-

Figure 3.5. Geographic distribution of Cyphophthalmi: Neogoveidae (triangles), Ogoveidae (crossed circles), Pettalidae (squares), Sironidae (circles), Stylocellidae (half-colored circles), and Troglosironidae (star).

79

80

Phylogeny and Biogeography

cumequatorial South America, Florida, and western Africa; Ogoveidae is restricted to the Gulf of Guinea in West Africa; Pettalidae has a typical temperate Gondwanan distribution; Troglosironidae is restricted to New Caledonia and is clearly unrelated to Pettalidae; Stylocellidae is found in Southeast Asia, including northern Thailand, Wallacea, Sundaland, and western New Guinea. Phylogenetic analysis of Cyphophthalmi relationships suggests a sister-group relationship of Pettalidae to the remaining families (G. Giribet, unpub. data). Relationships within Sironidae (Boyer et al., 2005) and Pettalidae (Giribet, 2003; Boyer & Giribet, unpub. data) have been explored in detail, and both global and local biogeographic patterns help understand current distributions of species. Within Neogoveidae, both the American and the African species form reciprocally monophyletic groups. Clearly, Cyphophthalmi species show a great potential for becoming a model for biogeographic studies.

Eupnoi Caddids are typically found in temperate zones of both hemispheres—with Amphipacific and temperate Gondwanan distributions (Shear, 1975a)—with the remarkable exception of a record from Venezuela (González-Sponga, 1992b). Apart from Japan, the single record from the Palearctic region is from Baltic amber. Acropsopilio has a large disjunct distribution: northeastern USA, southeastern Canada, Mexico, southern South America (Argentina, Brazil, and Chile), northern South America (Venezuela), Japan (the same species found in the USA and Canada), New Zealand, and Australia. Caddo shows a disjunct Amphipacific distribution: northeastern USA, southeastern Canada, and Japan. Austropsopilio and Tasmanopilio show an Amphinotic distribution: Australia/Tasmania/southern South America (Argentina, Brazil, and Chile). Caddella is found in South Africa, while Hesperopilio is restricted to western Australia. Although these patterns are suggestive of several wellexplained distribution patterns, no phylogenetic analysis has been attempted in the group. The members of the family Neopilionidae are typically distributed across temperate Gondwana, in Chile, Argentina, southern Brazil, South Africa, and Australia. Protolophids are restricted to the western USA. The Metopilio group occurs in the western USA, reaching as far south as Costa Rica. Sclerosomatidae include several subfamilies, from which Gagrellinae are distributed in Indo-Malaya and the Neotropics but absent elsewhere. Gyinae occur at high elevations in the Caucasus, Alps, and Nepal. Leiobuninae are distributed throughout the Palearctic region, as well as in the Nearctic, with a peak of diversity in Mexico, Guatemala, and Costa Rica. Sclerosomatinae are restricted to the Palearctic region. Phalangiidae also include several subfamilies. Phalangiinae are most diverse in the Mediterranean region, having radiated to coastal Africa (Starega 1984), where many endemic genera are recognized. The few Nearctic Phalangiinae are all introduced. Opilioninae are mainly Palearctic, with a few representatives in continental

Phylogeny and Biogeography

Southeast Asia. Oligolophinae are Holarctic, with their peak of diversity in central and western Europe. Finally, Platybuninae occur in central and southeastern Europe, the Balkans, Anatolia, and the Caucasus, with an odd record from Sumatra. There are records of introduced Nelima in Australia and New Zealand (Gruber & Hunt, 1973).

Dyspnoi Dyspnoi are restricted to the Northern Hemisphere, often with restricted distribution patterns. Nemastomatidae have a disjunct Holarctic distribution, with its peak of diversity in the western Palearctic (from the Iberian Peninsula and the Atlas to the Caucasus), reaching as far as Thailand (Schwendinger & Gruber, 1992). Ortholasmatinae have a few species in the eastern Palearctic (Japan) and the Nearctic (western USA). Dicranolasmatidae are recorded from Spain to the Caucasus, Iraq, and Turkey. Nipponopsalididae are restricted to the eastern Palearctic (Japan and Korea). Trogulidae are found in the western Palearctic, with their peak of diversity in the eastern and central Mediterranean region. Ischyropsalididae are found in the western Palearctic, from central Europe to the Iberian Peninsula. Sabaconidae are Holarctic, found from the Iberian Peninsula to Japan and the USA. Finally, Ceratolasmatidae are Nearctic, restricted to the USA.

Laniatores The Northern Temperate Insidiatores probably form a monophyletic group, Travunioidea. They are endemic to the Holarctic realm and occur in both coasts of the USA, Japan, Korea, and Europe, but are absent from central Asia (Briggs, 1969, 1971a, b; Martens, 1978a). Cladonychiidae have a disjunct relictual Holarctic distribution in Europe (Holoscotolemon) and both coasts of the continental USA. Travuniidae have a disjunct and relictual distribution in southern Europe, Japan, Korea, and the western USA. Pentanychidae/Paranonychinae are endemic to the northwestern USA. Sclerobuninae are endemic to the western USA. A group of Southern Temperate Insidiatores (Triaenonychidae and Synthetonychiidae) and the eastern North American Fumontana form the Triaenonychoidea. They occur in the classical Austral realm along the former temperate Gondwana. Although a few genera are reported to occur in more than one continent (Lawrence, 1931; Forster, 1954; Kauri, 1961; Maury & Roig Alsina, 1985), phylogenetic testing of the genera has not been attempted. Grassatores constitute the largest group of Laniatores. Phalangodidae are Nearctic and western Palearctic, especially circum-Mediterranean. Oncopodidae and Epedanidae are found in the Indo-Malayan province, the latter also occurring in China, Nepal, and Japan. Gonyleptoidea occur in tropical Gondwana, Wallacea, and Sundaland, with an interesting area relationship (Kury, 1997c): Assamiidae—the putative sister group to the rest—occur in tropical Asia and central Africa, while the others are endemic to the Neotropics. Of these, Stygnopsidae—which are the possible sister group to other gonyleptoid families—are restricted to Mexico, Belize, and

81

82

Phylogeny and Biogeography

Guatemala. The remaining families are distributed from Costa Rica to subAntarctic Chile and Argentina. An exception is Cosmetidae, which reaches the southern USA. “Samooidea” is an informal group that includes a number of families of small Laniatores that inhabit leaf litter, including Podoctidae, Biantidae, Escadabiidae, Samoidae, Kimulidae, and Stygnommatidae. They occur in tropical Gondwana, Wallacea, and Sundaland, plus Madagascar and India. “Zalmoxoidea” is another pantropical group. The nominal family occurs in tropical Asia, tropical Africa, and the Neotropics, while the other families (Fissiphalliidae, Guasiniidae, and Icaleptidae) are endemic to South America. Some zalmoxoid species are additionally found in Australia and New Caledonia.

Areas and their harvestman taxa The interesting biogeographic patterns shown by the different harvestman families have been summarized in Table 3.1. Here we provide a description of the taxa that occur in each area. Afrotropical

•

• • •

Madagascar: The dominant group is Triaenonychidae, although Biantidae are also diverse, including the typical genera (e.g., Metabiantes) and strange forms such as Hovanoceros. Cyphophthalmi are represented by two species, one pettalid and one of uncertain familial affinity. Seychelles: This region is poorer than Madagascar. It shows a strong presence of Podoctidae, with some Biantidae and Zalmoxidae. Alleged Samoidae (Benoitinus, Mitraceras) do not belong with typical Samoidae. South Africa: Triaenonychidae is the dominant group, followed by Biantidae. Cyphophthalmi of the family Pettalidae are also quite diverse. Assamiidae are poorly represented in this area. Central Africa: Phalangiinae, Assamiidae, and Podoctidae are well represented. Within Cyphophthalmi, Ogoveidae is endemic to the Gulf of Guinea. Neogoveidae is well represented in West Africa. Marwe coarctata is a Cyphophthalmi species of uncertain affinity from Kenya.

Neotropical/Andean (definitions of areas follow Morrone, 2001)

• • • • •

Caribbean: This region is rich in numerous families of Laniatores (Table 3.1). Within Eupnoi, Gagrellinae are well represented. Amazonian: This region presents numerous laniatorean families, including some endemic families, a few Eupnoi, and a large diversity of Cyphophthalmi of the family Neogoveidae. Chacoan: Neogoveidae, Gonyleptidae Metasarcinae, Stygnidae, and Cosmetidae. Paraná: Predominance of Gonyleptidae and Gagrellinae. Andean: Mostly Cranaidae and also Agoristenidae Leiosteninae, Stygnidae, Stygnommatidae, Gagrellinae, and Neogoveidae.

Phylogeny and Biogeography

Nearctic Cosmetidae and Leiobuninae penetrate southeastern and southwestern USA, probably dispersing from the Neotropical regions. Members of both families include large Opiliones. Leiobuninae are recorded to be good dispersers. The same distribution is found for Stygnomma spinifera (presently in Stygnommatidae, but probably Samoidae) from southern Florida and a doubtful record from Ohio.

• •

Mexico: Abundant Nearctic and Neotropical fauna merge in this area, with presence of Stygnopsidae, Zalmoxidae, Gagrellinae, and “Neogovea” mexasca, a Cyphophthalmi of uncertain familial affinity. USA: Numerous groups are found along both coasts of the USA (Table 3.1), while others have more restricted distributions. Ortholasmatinae, Sclerobuninae, Travuniidae, and Pentanychidae/Paranonychinae are restricted to the western USA coast. Caddidae is restricted to the eastern USA. A member of Neogoveidae are restricted to the southeastern USA coast.

Palearctic The Palearctic region has been well studied. Three main regions are considered, and their familial composition is shown in Table 3.1.

• • •

Europe: From the 10 families found in the area, two are endemic, Ischyropsalididae and Dicranolasmatidae. Central Asia: This region is poor in Opiliones diversity, and only members of two Eupnoi families and one Dyspnoi family have been recorded. Japan/Korea: This is an especially rich area that includes, among many other families, the endemic Nipponopsalididae.

Indo-Malayan This area is divided into several regions with independent geological origins, making difficult the distinction of ancestral vicariant patterns from more recent ones explained by dispersal.

• •

Indian subcontinent: Biantidae, Assamiidae, Gagrellinae, and Podoctidae are abundant. Pettalidae are common in Sri Lanka, and Stylocellidae (or close relatives) have been reported from the Arunachal Pradesh province of India, near Myanmar. Southeast Asia: Although divided into a continental and an insular zone, this biogeographic region is homogeneous and includes the endemic families Oncopodidae and Stylocellidae. Biantidae are probably not in the region, despite two doubtful records.

Australian/Oceania

•

Australian continent: Triaenonychidae and Pettalidae are the dominant groups, but several other temperate Gondwanan families occur. A few strange Gras-

83

Biantidae

X

X

X X

X X

X

Dicranolasmatidae

Nemastomatinae

X

X

X

X

X

X

Phalangiidae

X

X

X

X

X

X

X

X

X

X

X

X

X

X

Sclerosomatidae X

X

X

X

X

X

X

Sironidae

Samoidae

Zalmoxidae

X

X

X

Podoctidae

X

X

Assamiidae X

X X

X

X

X

X

X

X

X

X

X

X

X

Epedanidae

X

X

X

X

X

Oncopodidae

Monoscutidae

Gagrellinae

X

X

X X

Neopilionidae

Acropsopilioninae

X

X

X

X X

X

X

X

X

X

X

Triaenonychoidea

Stylocellidae

Wallacea/Sundaland

Palearctic

X

X

X

X

X

X

X

X

X

X

X

X

X

X

IND MAD SEY SAF CHI NZE NCA AUS PAP MEL MIC POL PHI THA CAS EUR NAF JAP WUS EUS

Troglosironidae

Pettalidae

Taxa

Temperate Gondwana

Table 3.1 Summary of distribution of Opiliones in the geographic units of the world

X

X

X

X

X

MEX

Mexican

X

X

X

X

X

X

X

X

X

?

X

X

X

SAM CAR CAF

Tropical Gondwana

X

X

Nipponopsalididae

Temperate Gondwana: IND = India/Sri Lanka/Nepal; MAD = Madagascar; SEY = Seychelles; SAF = South Africa; CHI = Chile/Argentina; NZE = New Zealand; NCA = New Caledonia (Melanesia); AUS = Australia/Tasmania. Wallacea/Sundaland: PAP = Papua New Guinea; MEL = Melanesia (except New Caledonia); MIC = Micronesia; POL = Polynesia; PHI = Malay Peninsula/Indonesia/Philippines; THA = continental southeastern Asia (Thailand, Vietnam). Palearctic: CAS = central Asia; EUR = Europe; NAF = northern Africa; JAP = Japan; WUS = western USA; EUS = eastern USA. Mexican: MEX = Mexico-Guatemala. Tropical Gondwana: SAM = circumequatorial South America; CAR = Caribbean (insular); CAF = central Africa.

X

X X

X

Neogoveidae

X

Lacurbsinae

X

Zalmoxoidea

X X

Ogoveidae

X

Escadabiidae

X

X

Kimulidae

X X

X

Stygnommatidae

Gonyleptoidea

X

X

X

X

X

X

X

X

X

X

X

Stygnopsidae

Ceratolasmatidae

X

X

X

X

X

X

Ortholasmatinae

X

X

X

Caddinae

X

Phalangodidae

Sabaconidae

Travunioidea

X X

Ischyropsalididae X

X

Trogulidae

86

Phylogeny and Biogeography

• • • •

satores, which may be Phalangodidae, and some Zalmoxidae and Samoidae are found. Podoctidae are restricted to a single species. Tasmania: Triaenonychidae are the dominant group, but there are Monoscutidae and Acropsopilioninae. Pettalidae are surprisingly absent from Tasmania. New Zealand: Triaenonychidae and Pettalidae predominate. Acropsopilioninae, Monoscutidae, and one species of Assamiidae also occur. Synthetonychiidae are endemic to New Zealand. New Caledonia: Includes the endemic family Troglosironidae, several Podoctidae, Zalmoxidae, and a few Triaenonychidae. Pacific Islands: Their opiliofauna is typically impoverished because of the low dispersal ability of Opiliones. Samoidae are the dominant group. Melanesia presents the most diverse fauna, with a number of Podoctidae and Zalmoxidae.

Opiliofaunal relationships It appears that the pattern of Laurasia versus Gondwana was replicated several times during the evolutionary history of Opiliones. The widespread purely Holarctic (= Laurasian) taxa include Sironidae, Sclerosomatidae, Sabaconidae, and Travunioidea (the possible sister group to all other Laniatores). Holarctic taxa with more restricted distributions include most Dyspnoi families, Caddinae, and Phalangodidae. Phalangiidae are a typical Laurasian component with dispersal ability; hence their presence in Africa and the Seychelles may be explained by dispersal from the Mediterranean, as postulated by Starega (1984). Evidence for the monophyly of Gondwanan taxa is weak. Within Gondwanan Cyphophthalmi, Pettalidae does not form a clade with Neogoveidae, and it seems that Gondwana is a paraphyletic area from which the Cyphophthalmi diversity originated. In other groups the phylogenetic evidence is so precarious that we prefer to leave the topic open to future discussion. However, it is clear that very few groups encompass the totality of the Gondwanan landmasses. Well-characterized temperate Gondwanan groups are Pettalidae, Triaenonychoidea, and Neopilionidae. The pertinence of India, Seychelles, and Madagascar to the temperate Gondwanan opiliofauna is not unambiguously supported. Although the presence of Triaenonychidae supports unity of Madagascar with the typical temperate Gondwana, Biantinae are present in India, Nepal, Madagascar, Seychelles, South Africa, and central Africa, and there are a few records from Indonesia. Assamiidae (absent from Madagascar and the Seychelles) suggest a relationship of India to central Africa. The monophyly of tropical Gondwana is weakly supported, but again it should be noted that cladistic hypotheses are still needed for most groups, and Cyphophthalmi analyses clearly support monophyly of Neogoveidae, with representatives in both Africa and South America (including Florida, which originated from a Gondwanan fragment). Gonyleptoidea would be another candidate for this support, but Assamiidae are present in India and Australia.

Phylogeny and Biogeography

Biogeographic conclusions Opiliones are excellent candidates for biogeographic studies because of their limited distribution ranges and low dispersal abilities, as shown especially in Cyphophthalmi, Dyspnoi, and many Laniatores. Endemicity of Opiliones is found to be near 97.5% in the Brazilian Atlantic rain forest, whose fauna is predominantly composed of gonyleptids (Pinto-da-Rocha et al., 2005). The fact that some members of a few families are prominent dispersers (e.g., Leiobuninae) should not preclude researchers from continuing to analyze harvestman biogeographic data. However, before meaningful progress can be made in this area, quantitative and qualitative progress needs to be made in the phylogenetic relationships among families and other lower ranks. To date, major progress has been made in solving the relationships among the four suborders of Opiliones. Substantial progress has also been made within Cyphophthalmi and the relationships among their major lineages (e.g., Giribet & Boyer, 2002; Giribet, 2003; de Bivort & Giribet, 2004; Boyer et al., 2005). Although the temperate Gondwanan family Pettalidae seems to be the sister group to all other Cyphophthalmi, relationships among the remainder groups are still poorly understood. Another interesting pattern, assuming monophyly of Dyspnolaniatores, is that Cyphophthalmi and Eupnoi are distributed globally, while Dyspnoi species are restricted to the former Laurasia, and Laniatores are mostly found in the Southern Hemisphere. This pattern may indicate that the separation between Dyspnoi and Laniatores followed the split of Pangea. Clearly, more work needs to be done before harvestman distributional data can be placed into a global biogeographic context for inferring patterns using congruence as an optimality criterion. We anticipate major progress in this neglected area of harvestman research in forthcoming years as the phylogenetic relationships among the harvestman families are elucidated.

ACKNOWLEDGMENTS We thank Ron Clouse, Ricardo Pinto-da-Rocha, Glauco Machado, and two reviewers for their comments and suggestions that greatly improved this chapter. Part of this material is based upon work supported by the National Science Foundation under Grant No. 0236871 to Gonzalo Giribet.

87

CHAPTER

4

Taxonomy Ricardo Pinto-da-Rocha and Gonzalo Giribet

T

he order Opiliones comprises four lineages that have been recognized since the earliest monograph of the group (Hansen & Sørensen, 1904). The evolutionary implications of these four groups, namely, Cyphophthalmi, Eupnoi, Dyspnoi, and Laniatores, as well as the alternative phylogenetic relationships postulated among them, are discussed in Chapter 3. Their anatomy is carefully discussed in Chapter 2. Some peculiarities of taxonomic description are presented in the section “Methods for taxonomic study” in Chapter 15. In this chapter we provide a taxonomic introduction to all 45 extant harvestman families currently recognized, grouped into four suborders. The sections were contributed by specialists in each family in order to provide the reader with the most upto-date knowledge on each group. This cannot be done without incorporating certain biases, both in taxonomic ideas and terminology, but we have attempted to minimize such biases as much as possible. In the first section the 6 families of Cyphophthalmi are discussed. In the second, the 6 Eupnoi families are dealt with. In the third section, in referring to the 7 families of Dyspnoi, Ceratolasmatidae are discussed in three items of generic status because of the disparity in body plans that almost certainly reflects the nonmonophyly of the group. Finally, a monumental section is presented for the 26 families of Laniatores. Each section includes a historical account of the suborder and a key for the identification of all families within the group. Whenever multiple characters can be chosen for recognizing groups, we have focused on those that are easily observable without the need for sophisticated techniques, having the amateur opilionologist in mind. In some cases the families can only be recognized through the use of genitalic characters, whereupon these were used. The key is followed by the systematic description of the families, arranged alphabetically. All families are clearly described and profusely illustrated, with each section including a brief summary of their distribution, relationships to other families, and references to their natural history and 88

Taxonomy

main taxonomic studies. For the most diverse families, keys for the subfamilies have also been provided. With both the descriptive information provided and the additional references, the reader should be able to acquire important knowledge on the family or group of interest. The main references on systematics and natural history are listed at the end of each family; although they are not exhaustive, they attempt to provide the most informative literature for each group. Detailed literature on natural history is given in Chapters 7–14. However, this chapter is by no means a field guide of harvestmen. Monographic studies and local faunas should be sought elsewhere. In order to guide the reader through the sections of this extensive chapter, we provide hereby a basic key to suborders, as well as a synopsis of the richness of genera and species for each group of Opiliones (see Table 4.1). Superfamilies were not included because they are well understood in Eupnoi and Dyspnoi, but not in Cyphophthalmi or Laniatores (see Chapter 3). Key to the suborders of Opiliones 1. Ozopores located at the tip of a conelike structure or ozophore (Figure 4.1a). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cyphophthalmi . Ozopores located on the surface of the prosoma, without ozophores. . . . . . . . . . . 2 2. Claws of legs I–II (single) differ from those of legs III–IV (double, Figures 4.24m, or single and branched, Figures 4.41e–g, 4.42b–g) . . . . . . . . . . . . . . . . Laniatores . Single and similar claws on legs I–IV. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 3. Cheliceral teeth with small regular teeth (“diaphanous teeth,” Figures 2.6a, 4.12e, 4.19d) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Dyspnoi . Without diaphanous cheliceral teeth, with extremely long and thin legs. . . Eupnoi Table 4.1 Synopsis of richness of extant described harvestmen taxa Suborder/Family

Subfamily

Genera

Species

CYPHOPHTHALMI Neogoveidae Shear, 1980

5

13

Ogoveidae Shear, 1980

1

3

Pettalidae Shear, 1980

10

45

Sironidae Simon, 1879

8

27

Stylocellidae Hansen & Sørensen, 1904

4

31

Troglosironidae Shear, 1993

1

7

Incertae sedis

3

3

Acropsopilioninae Roewer, 1923

4

13

Caddinae Banks, 1892

2

9

EUPNOI Caddidae Banks, 1892

(Continued)

89

Table 4.1 Continued Suborder/Family Monoscutidae Forster, 1948

Neopilionidae Lawrence, 1931

Phalangiidae Latreille, 1802

Subfamily

Species

Megalopsalidinae Forster, 1949

3

32

Monoscutinae Forster, 1948

2

2

Ballarrinae Hunt & Cokendolpher, 1991

5

10

Enantiobuninae Mello-Leitão, 1931

2

4

Neopilioninae Lawrence, 1931

1

1

Oligolophinae Banks, 1893

8

51

Opilioninae Koch, 1839 Phalangiinae Latreille, 1802 Platybuninae Stare ˛ ga, 1976 Protolophidae Banks, 1893 Sclerosomatidae Simon, 1879

Genera

Gagrellinae Thorell, 1889 ˇ Gyinae Silhavy ´, 1946 Leiobuninae Banks, 1893

5

108

25

202

9

47

1

8

117

1,004

8

41

14

192

Sclerosomatinae Simon, 1879

4

46

Dicranopalpus group

3

17

Ceratolasmatidae Shear, 1986

4

16

Dicranolasmatidae Simon, 1879

1

17

Ischyropsalididae Simon, 1879

1

35

Incertae sedis DYSPNOI

Nemastomatidae Simon, 1872

Nemastomatinae Simon, 1872

14

147

Ortholasmatinae Shear & Gruber, 1983

2

10

Incertae sedis

6

10

Nipponopsalididae Martens, 1976

1

3

Sabaconidae Dresco, 1970

2

45

Trogulidae Sundevall, 1833

7

44

ˇ Agoristeninae Silhavy ´, 1973

12

15

ˇ Leiosteninae Silhavy ´, 1973

10

54

3

4

248

435

14

96

LANIATORES ˇ Agoristenidae Silhavy ´, 1973

Zamorinae Kury, 1997 Assamiidae Sørensen, 1884 Biantidae Thorell, 1889

Biantinae Thorell, 1889 Lacurbsinae Lawrence, 1959

5

9

Stenostygninae Roewer, 1913

9

17

Zairebiantinae Kauri, 1985

1

1

5

16

116

681

10

29

Cladonychiidae Hadˇzi, 1935 Cosmetidae C. L. Koch, 1839

Cosmetinae C. L. Koch, 1839 Discosomaticinae Roewer, 1923

Suborder/Family Cranaidae Roewer, 1913

Subfamily Cranainae Roewer, 1913 Heterocranainae Roewer, 1913 Prostygninae Roewer, 1913 Stygnicranainae Roewer, 1913

Epedanidae Sørensen, in L. Koch, 1886 Escadabiidae Kury & Pérez, 2003 Fissiphaliidae Martens, 1988 Gonyleptidae Sundevall, 1833

Genera

Species

57

121

1

2

15

17

2

3

73

188

4

6

1

4

Ampycinae Kury, 2003

2

3

Bourguyiinae Mello-Leitão, 1923

8

15

Caelopyginae Sørensen, 1884

9

29

Cobaniinae Kury, 1994

1

2

Goniosomatinae Mello-Leitão, 1935

5

46

Gonyassamiinae Soares & Soares, 1988

2

3

38

142

Hernandariinae Sørensen, 1884

4

12

Heteropachylinae Kury, 1994

8

11

Gonyleptinae Sundevall, 1833

Metasarcinae Kury, 1994

13

25

Mitobatinae Simon, 1879

1

45

129

400

1

1

10

17

4

5

29

51

2

3

Pachylinae Sørensen, 1884 ˇ Pachylospeleinae Silhavy ´, 1974 Progonyleptoidellinae Soares & Soares, 1985 Sodreaninae Soares & Soares, 1985 Tricommatinae Roewer, 1912 Guasiniidae González-Sponga, 1997 Icaleptidae Kury & Pérez G., 2002

2

2

27

47

Kimulidae Pérez González, Kury, & Alonso-Zarazaga, new name

9

30

Oncopodidae Thorell, 1876

5

57

Pentanychidae Briggs, 1971

2

6

Phalangodidae Simon, 1879

20

103

Podoctidae Roewer, 1912

58

120

10

23

8

24

Manaosbiidae Roewer, 1943

Samoidae Sørensen, in L. Koch, 1886 Stygnidae Simon, 1879

Heterostygninae Roewer, 1913 Nomoclastinae Roewer, 1943 Stygninae Simon, 1879 Incertae sedis

1

2

17

49

1

1

Stygnommatidae Roewer, 1923

2

30

Stygnopsidae Sørensen, 1932

8

35 (Continued)

92

Taxonomy

Table 4.1 Continued Suborder/Family

Subfamily

Genera

Species

Synthetonychiidae Forster, 1954

1

14

Travuniidae Absolon & Kratochvíl, 1932

8

22

Kaolinonychinae Suzuki, 1975

2

3

Nippononychinae Suzuki, 1975

3

8

Paranonychinae Briggs, 1971

3

12

Sclerobuninae Dumitrescu, 1976

3

10

Triaenonychidae Sørensen, in L. Koch, 1886

Soerensenellinae Forster, 1954

2

10

108

435

Zalmoxidae Sørensen, in L. Koch, 1886

67

196

Incertae sedis

59

81

Triaenonychinae Sørensen, in L. Koch 1886

CYPHOPHTHALMI Historical systematic synopsis Gonzalo Giribet The first Cyphophthalmi described, “Ciron” from France (Latreille, 1796), did not explicitly refer to a particular species. Eight years later “Ciron” was named “ciron rougeâtre” (or its Latin version Siro rubens) (Latreille, 1804), the nominal species of the harvestmen suborder Cyphophthalmi. It was another 64 years before Joseph (1868a,b) described the second species of Sironidae, Cyphophthalmus duricorius, which gave the name to the suborder. Hansen and Sørensen (1904) excused Joseph for overlooking Latreille’s Siro because it was “a forgotten genus which at that time was not mentioned by anyone in connection with Opiliones” and synonymized it with Siro, where it remained until Boyer et al. (2005) resurrected the genus that gave its name to the suborder. The third described sironid was Simon’s (1872b) Cyphophthalmus corsicus from Corsica, a species later transferred to the genus Parasiro in Hansen and Sørensen’s (1904) monograph. By then, Siro and Parasiro were considered members of the subfamily Sironini [sic], related to the pettalid genera Pettalus and Purcellia. Hansen and Sørensen (1904) also proposed the subfamily Stylocellini [sic] to include the genera Stylocellus, Ogovea, and Miopsalis. The subfamily was raised to family status to include only the genus Stylocellus by Shear (1979b) and was later rediagnosed by the same author (Shear, 1980); this was followed by most subsequent investigators. Giribet (2002) provided an updated description of the family that recognized the genus Miopsalis and transferred the genus Fangensis from Sironidae to Stylocellidae.

Taxonomy

The first American species, Siro acaroides, was described by Ewing (1923), who gave it the new generic name Holosiro, later synonymized with Siro (Newell, 1947). Siro kamiakensis was originally described as Neosiro (Newell, 1943), synonymized by Shear (1980). Metasiro has been considered a member of Sironidae (Shear, 1980), although currently it is considered to be a member of Neogoveidae. Floridogovea was proposed by Hoffman (1963) as a junior synonym of Metasiro. Asia is home to the problematic monotypic genera Suzukielus (from Japan), Fangensis (from Thailand), and the previously mentioned members of the family Stylocellidae plus the Sri Lankan Pettalus. Suzukielus has been considered a member of Sironidae (Shear, 1980), but recent work indicates possible affinities with Pettalidae (Giribet, 2002). Rambla (1994) described Fangensis as a sironid, but phylogenetic analysis has unequivocally removed this genus from this family (Giribet, 2002; Giribet & Boyer, 2002; Schwendinger & Giribet, 2005). The affinities of another monotypic genus, from a cave in Kenya, Marwe, remain uncertain (Shear, 1985; Giribet & Boyer, 2002). Neogoveidae is a large family of Cyphophthalmi, distributed in the tropical regions of Africa and South America. Hansen (1921) described Paragovia sironoides from Bioko (Equatorial Guinea), which he considered to belong to Stylocellini [sic] together with Ogovea and Stylocellus. Davis (1937) later described Neogovea kartabo from Guyana (as Siro kartabo), and a series of species followed from both equatorial West Africa (Juberthie, 1969; Legg, 1990) and tropical South America (Hinton, 1938; Rosas Costa, 1950; Martens, 1969b; Shear, 1977, 1979a; Goodnight & Goodnight, 1980). The family Neogoveidae was proposed by Shear (1980) to include the genera Neogovea (and its junior synonyms Sirula and Brasilogovea), Metagovea, and Paragovia, plus the species “?Gen. enigmaticus” described by Martens (1969b). Shear (1980) also erected the family Ogoveidae to include two genera of Cyphophthalmi with conspicuous exocrine glands opening on the second opisthosomal sternite of males, Ogovea (replacement name given to Ogovia, Hansen & Sørensen, 1904) and Huitaca. Ogovea was known from Bioko (Equatorial Guinea) and Gabon, and Huitaca from Colombia (Hansen & Sørensen, 1904; Hansen, 1921; Juberthie, 1969; Shear, 1979a; Giribet & Prieto, 2003). The discovery of another Cyphophthalmi genus from New Caledonia with exocrine glands in the sternal areas raised skepticism about the relationship of Ogovea to Huitaca (Juberthie, 1979). At the time of Shear’s proposal, only two species of Ogovea and one species of Huitaca were known, and male specimens were available only for one Ogovea species. The discovery of sternal glands in virtually all species of Neogoveidae for which males are known clearly shows that this character may well be apomorphic for a clade containing the families Ogoveidae, Neogoveidae, and Troglosironidae. Given the clear similarity of all somatic characters of Huitaca with the members of the genus Neogovea, Giribet and Prieto (2003) transferred Huitaca into Neogoveidae. The family Ogoveidae is hence monotypic, as defined by Giribet and Prieto (2003), and contains three described species. The diagnosis of Neogoveidae provided by Shear (1980) is hence problematic because of the morphological differences between the three genera, and especially be-

93

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Taxonomy

cause of the inclusion of the Mexican species Neogovea mexasca, which is an exception to most neogoveid characters (Shear, 1977; Giribet & Boyer, 2002), and the exclusion of Huitaca. Huitaca shares with Neogovea the cheliceral type and the claws of the second pair of legs with a row of teeth, not present in the African Ogoveidae. This latter character is shared by all the members of the genera Neogovea, Metagovea, Metasiro, and Paragovia, as well as the troglosironid Troglosiro. The genus Paragovia may need revision, given the radically different external morphology and penial structure in its three species. Pettalidae is the most diverse Cyphophthalmi family, containing more than onethird of the described species of the suborder. The first species, Cyphophthalmus cimiciformis, was described on the basis of a single male from Sri Lanka (P. PickardCambridge, 1875). Later the genus Pettalus, which gives the name to the family, was erected for this species (Thorell, 1876a). Hansen and Sørensen (1904) revised the two species of Pettalus and described the new genus Purcellia from South Africa, classifying these two genera together with the sironid genera Siro and Parasiro into the subfamily Sironini [sic]. Since then numerous species have been described around the territories that formed temperate Gondwanaland during the Jurassic. Shear (1980) erected the family Pettalidae to include eight genera of Cyphophthalmi with dual cheliceral dentition, anal glands, and modified anal regions, among other features. Since then two more genera have been described for Madagascar (Shear & Gruber, 1996) and one from Western Australia (Giribet, 2003). The monophyly of Pettalidae is well corroborated (Giribet & Boyer, 2002). The last family to be named was Troglosironidae. Juberthie (1979) described Troglosiro aelleni from a cave in New Caledonia and erected a generic name for it. Despite the name and its habitat, the species does not present troglomorphic characters. Shear (1993b) described five new species of Troglosiro and proposed the family name to include the six known species of the genus at that time (more species are known now: Sharma & Giribet, 2005). The family category was justified on the basis of a cladistic analysis that rendered Troglosiro as the sister group to Sironidae + Pettalidae (Shear, 1993b), although more recent phylogenetic analyses support a relationship of Troglosironidae and Neogoveidae (Giribet & Boyer, 2002). Key to the families of Cyphophthalmi 1. Claw of leg II with a row of teeth (Figure 4.1h), comb shaped; with (Figures 4.1f, 4.6d) or without opisthosomal sternal gland pores. . . . . . . . . . . . . . . . . . . . . . . . . . 2 . Claw of leg II without a row of teeth; always without opisthosomal sternal gland pores. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 2. Gonostome of males subhexagonal (Figure 4.1d). . . . . . . . . . . . . . . . Neogoveidae . Gonostome of males semicircular (Figure 4.6c) or trapezoidal. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Troglosironidae 3. Adenostyle fringed (Figure 4.5h), second cheliceral segment ornamented (Figure 4.5e) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Stylocellidae Adenostyle not fringed, second cheliceral segment not ornamented . . . . . . . . . . . . . 4

Taxonomy

4. Spiracles shaped as an open circle (Figure 4.3g); cheliceral fingers with dual dentition (Figure 4.3h) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pettalidae . Spiracles circular; single cheliceral dentition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 5. With saddlelike opisthosomal sternal apophysis and associated gland pores (Figure 4.2c); with Hansen’s organ in cuticle (Figure 2.2e). . . . . . . . . . Ogoveidae . Without saddlelike opisthosomal sternal apophysis and associated gland pores; without Hansen’s organ in cuticle. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sironidae

Neogoveidae Shear, 1980 Gonzalo Giribet Etymology: Neogovea, from Greek, new Ogovea. Characterization: • Size: Small to large Cyphophthalmi, 1.05–4.5 mm long. • Dorsum: Body usually oval shaped. Eyes absent. Ozophores of type 2 (facing laterally) (Figure 4.1a). Dorsal scutum heavily granulated. Transverse prosomal and opisthosomal sulci distinct; middorsal longitudinal opisthosomal sulcus absent or inconspicuous. • Venter: Coxae I free; II fused to III. Spiracles circular in most species (Figure 4.1e), but in the shape of an open circle in N. microphaga and in undescribed species from Trinidad and Venezuela. Exocrine glands present on second opisthosomal sternite of males; very conspicuous in Huitaca (Figure 4.1f), where the gland forms a pore field, but also present in Metagovea and Paragovia. Opisthosomal sternal glands not observed in Neogovea or Metasiro. Corona analis complete, showing fusion of opisthosomal sternites 8–9 and tergite IX (Figure 4.1b); not so in Metasiro (Figure 4.1c). Males lacking anal glands or modifications of the anal region (Figure 4.1b); with anal glands in Metasiro (Figure 4.1c). • Chelicerae: Two main shapes, one short and robust, exemplified by Metagovea, and another long and attenuate, as in Neogovea and Huitaca, where the second segment tapers and the movable finger is extremely small (Figure 4.1g); Paragovia presents both types of chelicerae. Basal segment with dorsal crest and a single ventral process; second segment smooth, not ornamented; cheliceral teeth all large and irregular. • Pedipalps: Without distinct modifications; without a ventral process in the trochanter. • Legs: Tarsus of leg I generally with a distinct solea, a modified ventral region with a higher concentration of sensory setae. Ornamentation of legs always present in the metatarsi; in some species of Neogovea and in P. sironoides the tarsus is almost completely granulated. Claw II with a row of ventral teeth (Figure 4.1h); III–IV often with small lateral pegs. Male tarsus IV undivided; adenostyle lamelliform, fimbriate, or digitiform (Figure 4.1i); position of

95

96

Taxonomy

a

b

c

d

e

f

g

h

i

Figure 4.1. Neogoveidae. (a) Female of an undescribed species from Venezuela. Anal region of male: (b) Metagovea philipi; (c) Metasiro americanus. (d) Ventral thoracic complex of male M. philipi. (e) Spiracle of Huitaca ventralis. (f) Opisthosomal sternal exocrine gland organ of male H. ventralis. (g) Chelicera of H. ventralis. (h) Claw of leg II of H. ventralis. (i) Adenostyle of Paragovia sironoides.

adenostyle variable, near the base of the tarsus in Metagovea, Metasiro, Huitaca, and Paragovia, but in a more distal position in Neogovea and P. sironoides. • Genitalia: Spermatopositor very variable even within genera (e.g., Paragovia [see Legg, 1990]), and in general it has a large number of microtrichia, including three groups of dorsal microtrichia in Neogovea and Metagovea (Shear, 1980), or an elongated spermatopositor in Paragovia sironoides. Neogovea has a hypertrophied ventral plate. • Sexual dimorphism: Adenostyle in male tarsus IV. Presence of exocrine glands in the second opisthosomal sternite of males in the genera Huitaca, Metagovea, and Paragovia and anal glands in males of Metasiro. The sternal opisthosomal region of most Neogovea specimens is not preserved, and this character needs reexamination.

Taxonomy

Distribution: The members of the family are restricted to a fringe between 10° north of the equator and 5° south, with the sole exception of the North American Metasiro. Paragovia is found in the Gulf of Guinea area and Sierra Leone, in Africa. Metagovea is restricted to the tropical forests of the Andes, while the other South American genera are found around the Amazonas basin and in the Orinoco basin. Relationships: The cladistic morphological analysis of Giribet and Boyer (2002) did not obtain monophyly of Neogoveidae. However, that study had missing data for several genital characters within Neogoveidae. Two main genital morphologies seem to occur in South America: the Metagovea type and the Neogovea-Huitaca type with the attenuated chelicerae. However, more detailed genital character studies should yield a better understanding of this group, which is known to have very diverse spermatopositor morphologies (Shear, 1977, 1979a; Legg, 1990). Recent molecular studies suggest monophyly of the American neogoveids that form the sister group of the African neogoveids from the Gulf of Guinea, and these form a clade with the North American Metasiro americanus (G. Giribet & S. Boyer, unpublished results). Main references: • Systematics: Rosas Costa (1950), Shear (1977), Legg (1990). • Natural history: Pabs-Garnon (1977).

Ogoveidae Shear, 1980 Gonzalo Giribet Etymology: Ogovia refers to the river Ogooué (spelled Ogové in Hansen & Sørensen, 1904), where the type species was found. Ogovea is a replacement name given to Ogovia by Roewer (1923). Characterization: • Size: Medium to large Cyphophthalmi, 3–5 mm long. • Dorsum: Body usually oval shaped (Figure 4.2a). Eyes absent. Ozophores of type 2 (lateral). Dorsal scutum heavily granulated and divided longitudinally by a conspicuous median furrow. Hansen’s organ (Figure 4.2e), a coticular structure of possible secretory function, present in the body surface of legs, coxae, and opisthosomal sternal region in both males and females. The cuticle of the body and appendages is completely covered with different types of sensory hairs and sensory structures (Figures 4.2e,f). • Venter: Coxae I free; II fused to III. Spiracles of circular shape (Figure 4.2d). Exocrine glands present on second opisthosomal sternite of males, associated with a large apophysis (Figure 4.2c). Corona analis complete, showing fusion of sternites 8 and 9 and tergite IX (Figure 4.2b). Males lacking anal glands or modifications of the anal region. • Chelicerae: Robust; basal segment with a dorsal crest and with a single ventral process; distal segments smooth, not ornamented; cheliceral teeth uniform and nodular.

97

98

Taxonomy

a

d

b

c

e

f

Figure 4.2. Ogoveidae. Male of Ogovea cameroonensis: (a) holotype, ventral view; (b) anal region; (c) sternal opisthosomal apophysis; (d) spiracle; (e) cuticular region of tarsus IV showing Hansen’s organ (H) and different types of sensory hairs; (f) adenostyle.

• Pedipalps: Extremely modified, with long trochanter and short femur that folds around the chelicera. • Legs: Tarsus I with a distinct solea; II almost entirely ornamented; claw of leg II smooth. Male tarsus IV not divided; adenostyle short, triangular, thornlike (Figure 4.2f), placed toward the middle of the tarsus, without accessory tarsal structures. • Genitalia: Spermatopositor with numerous apical microtrichia; numerous ventral microtrichia in a compact group; dorsal microtrichia displaced to two groups; with a membranous structure around the gonopore. • Sexual dimorphism: Adenostyle in male tarsus IV. Presence of exocrine glands in the second opisthosomal sternite of males, associated with the large apophysis (Figures 4.2a,c; male not known for O. grossa). Distribution: Tropical rain forests of equatorial West Africa, along the Gulf of Guinea area in Bioko (Equatorial Guinea), Cameroon, and Gabon (Hansen & Sørensen, 1904; Hansen, 1921; Juberthie, 1969; Giribet & Prieto, 2003). Relationships: The group was revised by Shear (1980) in his cladistic analysis of the suborder Cyphophthalmi. He erected the new family Ogoveidae to include the genera Ogovea and Huitaca. The family was proposed to constitute the superfamily Ogoveoidea together with Neogoveidae, and part of the infraorder Tropicophthalmi together with Stylocellidae. The parsimony analysis of morphological data performed by Giribet and Boyer (2002) shows monophyly of Ogovea, but it rejects monophyly of Ogoveidae sensu Shear (1980) or monophyly of Tropicophthalmi (see also de Bivort & Giribet, 2004).

Taxonomy

Main references: • Systematics: Shear (1980), Giribet & Prieto (2003).

Pettalidae Shear, 1980 Gonzalo Giribet and Sarah L. Boyer Etymology: Pettalus is a name from Greek mythology that appears in Ovid’s The Metamorphoses. Characterization: • Size: Medium to large Cyphophthalmi, 2–5 mm long. • Dorsum: Body usually oval shaped (Figure 4.3). Eyes absent in Parapurcellia, but present with or without a lens in all other genera. Ozophores of type 3 (facing upwards) or facing 45° (Figure 4.3a); of type 2 in Parapurcellia. Prosoma and opisthosoma not clearly differentiated, forming a scutum completum. Dorsal margin generally granulated, with lines lacking granulation delimiting the opisthosomal tergites. Middorsal longitudinal sulcus of opisthosoma absent or inconspicuous. Terminal tergites VIII and IX may become divided in males, and sometimes tergite VII is also divided. Tergites may bear scopulae or concentrations of setae (Figures 4.3d,e). • Venter: Thoracic complex of males with the coxae IV meeting ventrally in the midline for a long distance, with a small gonostome (except Speleosiro) (Figures 4.3b,c). Second coxae free. Spiracles small, in the form of an open circle (Figure 4.3g). Sternal opisthosomal glands absent, but the sternites 6–8 of Karripurcellia become clearly convex in the males and slightly convex in the females. Opisthosomal sternites 8–9 and tergite IX free (Figures 4.3d–f); different degress of fusion exist in Pettalus. Relative position of sternite 9 and tergite IX of “pettalid type” (Figure 4.3f); most females (the males may have modified anal regions) have tergite IX covering laterally sternite 9 and clearly meeting sternite 8. • Chelicerae: May be protruding with a dorsal crest clearly visible from above. Dorsal crest in the basal cheliceral segment; ventral process present or absent. Most chelicerae of robust type, attenuate in some species of Pettalus. Distal segments of chelicerae not ornamented. Dentition of the mobile finger of two types (Figure 4.3h) in most species, except some species from South Africa and New Zealand. A special type of chelicerae with a conspicuous longitudinal apodeme in the second segment is known in Parapurcellia and in several species from New Zealand and Queensland (Boyer & Giribet, 2003). • Pedipalps: With (Figure 4.3i) or without a ventral process in trochanter. • Legs: Ornamentation of metatarsi I–II variable; tarsi I–II smooth or ornamented in dorsobasal part. Claws without a row of ventral teeth or lateral pegs. • Genitalia: Spermatopositor quite uniform, studied for a few species of the genera Pettalus (Sharma & Giribet, 2006), Purcellia (Hansen & Sørensen,

99

100

Taxonomy

a

b

c

d

e

f

g

h

j

i

k

Figure 4.3. Pettalidae. (a) Pettalus lampetides, holotype male, dorsal. Sternal prosomal region of male: (b) P. lampetides; (c) Karripurcellia peckorum. Anal region of male: (d) P. lampetides; (e) Neopurcellia salmoni; (f) Chileogovea oedipus. (g) N. salmoni, spiracle. (h) K. peckorum, cheliceral dentition. (i) Rakaia macra, pedipalpal trochanter. (j) R. macra, undivided tarsus IV of male. (k) N. salmoni, divided tarsus IV of male.

1904), Chileogovea (Juberthie & Muñoz-Cuevas, 1970; Shear, 1993a), Speleosiro (Juberthie, 1971), Austropurcellia (Juberthie, 1988), Rakaia (Juberthie, 1989; Boyer & Giribet, 2003), and Karripurcellia (Giribet, 2003). Spermatopositor short, generally with one pair of movable fingers around the gonopore; with a single series of dorsal microtrichia forming a V, one row of ventral microtrichia, and long apical microtrichia. Ovipositor long, multiseg-

Taxonomy

mented, with two apical lobes, each with a long subterminal seta in a small socket and with a sensitive process. • Sexual dimorphism: Evident in the anal region, which becomes strongly modified in the males of several species (Figures 4.3a,d–f). Anal plates may present ridges (Figure 4.3f) or grooves, or become divided (Figures 4.3a,d), and may present concentrations of setae in the anterior or in the posterior part. Opisthosomal tergite IX divided or entire, with an opisthosomal exocrine anal gland (Figure 4.3f); tergite VIII may become bilobed and present scopulae. Modifications may extend to tergite VII or to the sternal opisthosomal region. Tarsus IV with adenostyle (Figures 4.3j,k) and bipartite in males of several species (Figure 4.3k), including all the South African ones (Purcellia, Speleosiro, and Parapurcellia) and those of some species in Australia and New Zealand. This unique character is also found in the sironid genus Suzukielus and in some American species of the genus Siro. Distribution: Pettalids are found in the Southern Hemisphere (except for the Sri Lankan species), distributed throughout the former temperate Gondwana. The group reaches a peak of diversity in New Zealand with 29 nominal species and subspecies belonging to the genera Rakaia and Neopurcellia. Sri Lanka, with 3 described species of Pettalus, Australia, with 9 described species in the genera Austropurcellia, Karripurcellia, Neopurcellia, and Rakaia, and South Africa, with 8 described species in the genera Parapurcellia, Purcellia, and Speleosiro, are known to have several undescribed species. The genus Chileogovea, widely distributed in Chile, may also have some undescribed species. The monotypic genera Manangotria and Ankaratra are found in Madagascar. Relationships: Hansen and Sørensen (1904) included the genera Pettalus and Purcellia in the subfamily Sironini [sic]. The group was revised by Shear (1980) in his cladistic analysis of the suborder Cyphophthalmi, where he erected Pettalidae. The family was proposed to constitute part of the superfamily Sironoidea together with Sironidae, and part of the infraorder Temperophthalmi. The parsimony analysis of Giribet and Boyer (2002) showed monophyly of Pettalidae, although it was ambiguous about the exact position of the family, suggesting that it could either be a sister group to the remaining Cyphophthalmi or could be related to Sironidae or even to the Japanese genus Suzukielus. Current molecular work (unpublished results by S. Boyer & G. Giribet) suggests that the genera Rakaia and Neopurcellia are not monophyletic, and they are currently under revision. All the species inhabiting Queensland (currently classified in the three genera Rakaia, Neopurcellia, and Austropurcellia) form a monophyletic group. Main references: • Systematics: Lawrence (1933, 1939, 1963), Forster (1948b, 1952), Shear (1980, 1993a), Giribet (2003).

101

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Taxonomy

Sironidae Simon, 1879 Gonzalo Giribet Etymology: Siro, a Latin form of the French name “Ciron.” Characterization: • Size: Small Cyphophthalmi, 1–2.5 mm long. • Dorsum: Body usually oval shaped. Eyes absent. Ozophores of type 1 (facing laterally, on carapace margin) or 2 (facing laterally above edge of carapace). Prosoma and opisthosoma not clearly differentiated, forming a scutum completum. Dorsal region granulated, with lines lacking ornamentation delimiting the opisthosomal segments. Middorsal longitudinal sulcus of opisthosoma absent or inconspicuous. Tergite VIII of males may be shallowly excavated or present a small median knob (in the American species); tergite VIII of females may protrude extensively in some European species. Tergite IX of males entire; divided in Suzukielus. Male anal glands present in tergites VIII or IX (Figures 4.4a–c) or absent. • Venter: Coxa II free; fused to III in Paramiopsalis. Spiracles small and circular (Figure 4.4g) or in the form of an open circle. Sternal opisthosomal glands absent. Sternites 8–9 and tergite IX all free (Suzukielus [Figure 4.4c], Parasiro minor), sternites fused (Parasiro [Figure 4.4d], Paramiopsalis [Figure 4.4e]), or all fused forming a complete corona analis (Siro [Figures 4.4a,b], Odontosiro). Anal plate of males with (Figures 4.4a,c,e) or without (Figures 4.4b,d) longitudinal carina and may present other modifications such as areas deprived of granulation (Figure 4.4b). • Chelicerae: Robust, with a single type of large regular teeth. Second cheliceral segment smooth (ornamented at the base in Odontosiro). With or without dorsal crest and ventral process. • Pedipalps: With or without a ventral process in trochanter. • Legs: Leg I without a distinct solea. Ornamentation of metatarsi I–II variable, from both being smooth to both being ornamented. Claw of leg II without a row of ventral teeth. Claws of some species with lateral pegs. Adenostyle not at the base of the tarsus; lamelliform (Figure 4.4h) or plumose in Paramiopsalis (Figure 4.4i). • Genitalia: Spermatopositor quite uniform, short, generally with one pair of movable fingers around the gonopore; with a single series of dorsal microtrichia forming a V, one row of ventral microtrichia, and long apical microtrichia (Juberthie, 1970b; Shear, 1980). Ovipositor of Parasiro lacks distal sensitive process; sensitive process of the other genera shows some variation. Number of ovipositor segments variable: 5 in Odontosiro, 8–9 in Parasiro, and more than 20 in other genera. • Color: Yellow, orange, red, or blackish. • Sexual dimorphism: Evident in the terminal tergites or anal region of several species with different modifications of the anal plate and anal gland pores (Fig-

Taxonomy

a

b

c

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e

f

h

i

g

Figure 4.4. Sironidae. Anal region of male: (a) Siro rubens; (b) Cyphophthalmus duricorius; (c) Suzukielus sauteri; (d) Parasiro coiffaiti; (e) Paramiopsalis ramulosus. (f) C. duricorius, sternal prosomal region of male. (g) Parasiro minor, spiracle. Adenostyle: (h) C. duricorius; (i) P. ramulosus.

ures 4.4a–c,e). Tarsus IV bipartite in Suzukielus and Siro kamiakensis, or strongly modified in S. sonoma. Distribution: Sironids follow a typical Laurasian distribution, with most species found in temperate Europe and on the west coast of North America, between 34° and 50°N. The genus Suzukielus is the only member of the family known from Japan. Two other species that have been somehow related to Sironidae in one way or another, Neogovea mexasca and Marwe coarctata, live below 35°N, and their affinities need to be studied in more detail. Relationships: Sironidae includes 27 described species, some with up to 5 named subspecies (Giribet, 2000), and currently includes the genera Cyphophthalmus,

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Odontosiro, Paramiopsalis, Parasiro, Siro, Suzukielus, and Tranteeva. Metasiro americanus is here considered a member of Neogoveidae. The relationships of Sironidae have been examined using morphological and molecular data (Giribet & Boyer, 2002; de Bivort & Giribet, 2004; Boyer et al., 2005). In the morphological cladistic analysis by de Bivort and Giribet (2004), the genera Siro, Paramiopsalis, Iberosiro, and Marwe formed a monophyletic group, with Parasiro and Odontosiro forming an independent lineage, and Suzukielus forming the sister group to Pettalidae. The former genus Siro has been recently divided into a mostly Balkan clade of Cyphophthalmus and a western European–North American clade of Siro (Boyer et al., 2005). Main references: • Systematics: Juberthie (1960b, 1964, 1965), de Bivort & Giribet (2004). • Natural history: Juberthie (1958, 1961b, 1962, 1967, 1970a,b), Shear (1980), Karaman (2005).

Stylocellidae Hansen & Sørensen, 1904 Gonzalo Giribet Etymology: Stylocellus, from Greek stxlos, column, pillar, pen, and Latin ocellus, eye. The name may refer to the elongated shape of the animal when compared with sironids, and to the presence of eyes. Characterization: • Size: Small to large Cyphophthalmi, 1–7 mm long. • Dorsum: Body usually oval shaped with a more or less subtriangular anterior end, the base of the triangle formed by the conical ozophores. Eyes present in Stylocellus, absent in Fangensis and Miopsalis. Eye lens located anterior to ozophores (Figure 4.5a,b). Type 2 (facing laterally) ozophores (Figure 4.5a). Tergites of prosoma and opisthosoma fused, forming a scutum completum. Dorsal scutum generally ornamented with granules, with lines lacking granules delimiting opisthosomal tergites. • Venter: Coxa I free; II fused to III. Spiracles large, C shaped (Figure 4.5d). Sternites 8–9 and tergite IX free (Figure 4.5c). Anal plate without modifications in most species, with smooth longitudinal carina in males of Fangensis and some species of Stylocellus (Figure 4.5c). Anal gland pore opening in tergite VIII of males of Fangensis and some species of Stylocellus (Figure 4.5c), including S. sumatranus. The opisthosomal sternal region of several undescribed species from Thailand may present characteristic depressions. • Chelicerae: Different cheliceral morphologies present; some species have short and strong chelicerae, others large ones with delicate distal segment. Second segment more or less extensively ornamented with granules, almost over its entire length in some species of Fangensis (Figure 4.5e) and some putatively related species of Stylocellus. Basal segment with a dorsal and a ventral process,

Taxonomy

Figure 4.5. Stylocellidae. (a) Stylocellus globosus, lateral view of the anterior body end. (b) Stylocellus ramblae, detail of the eye (e) and ozophore; anterior is left. (c) S. globosus, anal region of male. (d) S. ramblae, C-shaped spiracle. (e) Fangensis cavernarus, left chelicera of male with ornamented second article, retrolateral view. (f) F. cavernarus, tarsus IV of male with Rambla’s organ, retrolateral view. (g) Fangensis leclerci, Rambla’s organ. (h) F. cavernarus, adenostyle. (i) F. cavernarus, total spermatopositor, ventral. (j) F. cavernarus, total spermatopositor, dorsal. Figures i and j from Schwendiger and Giribet (2004).

in some species additionally with an anteroventral process (processus inferior exterior sensu Hansen & Sørensen, 1904; second ventral process sensu Giribet & Boyer, 2002) (Figure 4.5e). • Pedipalps: Without distinct modifications; without ventral process on trochanter. • Legs: Claws without ventral teeth or lateral pegs. Tarsi almost completely ornamented with granules. Tarsus IV of male undivided, with a modified structure (Rambla’s organ), associated with the adenostyle in Fangensis (Figures 4.5f,g).

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Taxonomy

• Genitalia: Spermatopositor (Figures 4.5i,j) with three rows of microtrichia: apical microtrichia long, ventral microtrichia (often three) in transverse row, dorsal microtrichia in two groups with bases fused or not. Ventral side of spermatopositor ornamented with small denticles along distal and distolateral margins. Ovipositor long, multisegmented, with two apical lobes, each with a long subterminal seta in a small socket and with a sensitive process. • Color: Varying from different shades of orange to red, maroon, brown, or black. • Sexual dimorphism: In most species restricted to shape of genital region and presence of adenostyle on male tarsus IV (Figure 4.5h). Males of Fangensis and a few species of Stylocellus additionally with anal plate modifications and anal gland pore in tergite VIII (Figure 4.5c); males of Fangensis with Rambla’s organ (Figures 4.5f,g). Distribution: Stylocellids are known from tropical areas of Southeast Asia, including Thailand, Malaysia and Singapore, and from most large islands of the Indo-Malay Archipelago, that is, Sumatra, Borneo, Java, Sulawesi, and the Philippine island of Palawan (Hansen & Sørensen, 1904; Shear, 1979b, 1993c; Giribet, 2000, 2002). Numerous undescribed species are known from these countries and islands, as well as from New Guinea and the Riau and Lingga archipelagos. The Cyphophthalmi specimens reported by Bastawade (1992) from India (Aruna¯chal Pradesh) are closely related to known Stylocellidae but do not share some of the diagnostic characters of the family. Relationships: Since the initial systematic placement by Hansen and Sørensen (1904) stylocellids have been associated with the members of Ogoveidae and Neogoveidae, first forming part of the subfamily Stylocellinae and later considered to constitute the infraorder Tropicophthalmi. Recent cladistic analyses of morphological and molecular data do not support this relationship (Giribet & Boyer, 2002). Although the monophyly of the genus Fangensis seems to be fairly well supported (Schwendinger & Giribet, 2005), it is not clear whether the genera Stylocellus and Miopsalis are monophyletic. At least two very different cheliceral morphologies exist in the group, and also a few Stylocellus species have modified anal plates and anal pores that may indicate a close relationship between them and the genus Fangensis (Schwendinger et al., 2004). Main references: • Systematics: Hansen & Sørensen (1904), Shear (1993c), Giribet (2002), Schwendinger & Giribet (2005) • Natural history: Rambla (1991, 1994), Shear (1993c), Schwendinger et al. (2004), Schwendinger & Giribet (2005).

Troglosironidae Shear, 1993 Gonzalo Giribet Etymology: From Troglosiro; Greek troglos, cave, and Siro, the first genus of the suborder described.

Taxonomy

Characterization: • Size: Cyphophthalmi of small size, 1.7–2.53 mm long. • Dorsum: Eyes absent. Ozophores of type 2 (facing laterally). Dorsal opisthosomal tergites not divided longitudinally by a median furrow. • Venter: Coxa II free, not fused to coxae I or III–IV. Spiracles circular (Figure 4.6e). Opisthosomal sternal area of males with two to four median exocrine gland pores (Figures 4.6a,d); sternites with one or two depressions, sometimes deeply depressed. Opisthosomal sternites 8–9 and tergite IX completely fused, forming a corona analis (Figure 4.6b).

b

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Figure 4.6. Troglosironidae. (a–d) Male of Troglosiro longifossa: (a) ventral view of holotype male; (b) anal region; (c) sternal prosomal region; (d) detail of the opisthosomal sternal depression and gland pores. (e) Spiracle of T. juberthiei. (f) Left chelicera of male T. longifossa. (g) Detail of claw of leg II in T. juberthiei. (h) Adenostyle of T. juberthiei.

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Taxonomy

• Chelicerae: Robust (Figure 4.6f), with basal segment with or without a dorsal crest. Distal segments of chelicerae mostly smooth, sometimes with scalelike ornamentation in the second segment. Mobile digit of chelicerae with a single type of dentition; teeth regular or irregular. • Pedipalps: Without distinct modifications or a ventral process in trochanter. • Legs: Tarsal claws I, III, and IV smooth; II with a row of teeth (Figure 4.6g). Tarsus IV of males entire. Adenostyle short, lamelliform (Figure 4.6h), near the tarsal base. • Genitalia: Spermatopositor with four apical microtrichia fused in pairs and their bases much thickened; movable fingers enlarged; middle pair of dorsal microtrichia sometimes reduced or absent; with dentate/fimbriate lateral margins. Ovipositor long, multisegmented, with two apical lobes, each with a long terminal seta, a short subterminal seta, and a bi- or trifurcated sensitive process. • Color: Dark, brownish to black. Troglosiro raveni has a distinctive color pattern of black and brown, a rare characteristic among Cyphophthalmi. • Sexual dimorphism: Besides the adenostyle and the gonostome area, the presence of the opisthosomal sternal gland pores, often accompanied by profound depressions of the sternal region, is the only sexual character. No modifications in the male anal plate (Figure 4.6b). Male anal glands absent. Distribution: The genus Troglosiro is restricted to New Caledonia in the Coral Sea (South Pacific). Several species have been collected in localities around the island (Sharma & Giribet, 2005), including six undescribed species. Relationships: Juberthie (1979) suggested a relationship of Troglosiro to the sironid genus Siro, although he noticed some affinities to the pettalid genus Parapurcellia. Uncertainty about the position of the genus Troglosiro followed (Shear, 1980, 1985; Juberthie, 1989), until Shear (1993b) proposed a sister-group relationship of Troglosiro to Sironidae + Pettalidae, justifying its familial rank. This result was not corroborated by a morphological cladistic analysis of most Cyphophthalmi genera (Giribet and Boyer, 2002), although the analysis by de Bivort and Giribet (2004) suggests that Troglosiro falls within a Sironidae + Pettalidae clade. The first molecular data presented for Cyphophthalmi (Giribet & Boyer, 2002) indicated a relationship of Troglosiro to Neogoveidae, which shares the presence of sternal opisthosomal gland openings and the toothed claw of leg II. Main references: • Systematics: Shear (1993b), Sharma & Giribet (2005).

EUPNOI Historical systematic synopsis James C. Cokendolpher, Nobuo Tsurusaki, Ana Lúcia Tourinho, Christopher K. Taylor, Jürgen Gruber, and Ricardo Pinto-da-Rocha

Taxonomy

The harvestmen of the suborder Eupnoi are the most familiar Opiliones, not only because they are abundant and diversified almost worldwide but also because they are common in Europe and the USA. They were the first Opiliones to be recorded on paper, being illustrated by Aldrovandus in 1603. Despite the number of species, the group is somewhat homogeneous. Currently only six families are recognized, and the suprageneric relationships among them deserve more attention than they have received. The first harvestman (Phalangium opilio) described with binomial nomenclature by Linnaeus (1758) is now a member of Eupnoi. Linnaeus listed Phalangium under the class Insecta, order Aptera. As other genera and species were described, the names of the classes, orders, and families changed back and forth. Some authors included whip spiders, solifuges, and mites with harvestmen. Latreille (1802a) included all harvestmen and a solifuge in the order Acera, family Phalangites. Latreille (1829) later moved the harvestmen to the order Trachéennes, family Holetra, tribe Phalangiens. Even later, Sundevall (1833) recognized the then-known five genera in three families (Gonoleptides, Phalangides, Trogulides) of his new order Opiliones. Unfortunately, he placed the genus Caeculus (a mite) in Opiliones (Trogulides), while the genus Siro (Opiliones) was placed in the order Acari. Hansen and Sørensen (1904) described the tribe Eupnoi under the suborder Palpatores. Roewer revised all Phalangioidea in his “Revision der Opiliones Plagiostethi” (Roewer, 1910, 1912c) and presented summary redescriptions of all known Eupnoi in Roewer (1923). The classification of Opiliones used by Roewer (1923) was as follows: Suborder Cyphophthalmi Suborder Laniatores Suborder Palpatores Tribe Dyspnoi Acropsopilionidae (not including Caddinae) and other families Tribe Eupnoi Phalangiidae Liobuninae Gagrellinae Leptobuninae Oligolophinae (including Caddinae) Phalangiinae Sclerosomatinae Crawford (1992) presented a new classification and a catalogue of all genera and type species of the superfamily Phalangioidea. He also established the synonym of Argyrasterinae Nakatsudi, 1942—previously synonymized with Leiobuninae by Suzuki (1971)—with Gagrellinae. A synopsis of his classification is as follows: Superfamily Phalangioidea Neopilionidae

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Ballarrinae Enantiobuninae Neopilioninae Monoscutidae Monoscutinae Megalopsalidinae Sclerosomatidae Gyinae Gagrellinae (= Argyrasterinae) Leiobuninae Sclerosomatinae Phalangiidae Phalangiinae (= Leptobuninae, Odontobuninae) Oligolophinae Opilioninae Platybuninae Protolophinae Family incertae sedis Caddids were first recorded by Banks (1892), who described a small harvestman with a prominent ocularium and large eyes occupying most of the propeltidium (Caddo agilis) in Phalangiidae. In 1893 he established for it the tribe Caddini. Silvestri (1905) described Acropsopilio chilensis but did not assign it to a family, noting that it showed characters of both Eupnoi and Dyspnoi. Roewer (1912c, 1923) placed Caddo in the subfamily Oligolophinae (Phalangiidae), a rather heterogeneous group as conceived by him. Roewer (1923) established Acropsopilionidae for Silvestri’s species only on the basis of the original description and placed it in Dyspnoi on the basis of the character “palp tarsus shorter than tibia,” disregarding contradictory evidence. When he later studied Silvestri’s type, he united Caddo and Acropsopilionidae in the subfamily Caddinae in Phalangiidae (Roewer, 1957b). Kauri (1961) and Ringuelet (1962) criticized this move; the latter regarded the similarities as convergent and adhered to placement in two families/superfamilies, while the former suggested a possible union within Acropsopilionidae. In the 1970s the “unified” group became accepted as a family (Cekalovic, 1974: as Acropsopilionidae, presumably following Kauri, 1961; Gruber, 1975, and Shear, 1975a: as Caddidae). Gruber (1975) discussed some systematic problems, such as the position of Caddidae in relation to Dyspnoi and Eupnoi. In the same year Shear (1975a) reviewed the family Caddidae and established for it the superfamily Caddoidea, containing Caddinae and Acropsopilioninae. The second superfamily, Phalangioidea, includes the families Monoscutidae, Neopilionidae, Phalangiidae, Protolophidae, and Sclerosomatidae. Monoscutidae has previously been referred to as Megalopsalididae. However, Crawford (1992) pointed out that the subfamily Monoscutinae had priority over Megalopsalidinae.

Taxonomy

Megalopsalidinae (Megalopsalinae [sic], including Monoscutum) was included by Silhavy (1970) in his extended Neopilionidae. Martens (1976) raised it to family level and corrected the name to Megalopsalididae. Hunt (1990b), Hunt and Cokendolpher (1991), and Taylor (2004) recognized both Monoscutinae and Megalopsalidinae. The monophyly of Monoscutidae is based on a single character, the presence of paired lateral bristle groups on the penis at the shaft/glans articulation (Hunt & Cokendolpher, 1991). Monoscutidae contains two very distinctive subfamilies, Monoscutinae and Megalopsalidinae. Currently, Monoscutinae contains only two monotypic genera, Monoscutum and Acihasta, as well as undescribed species of an uncertain genus from New South Wales, Australia (Hunt, 1990b; Hunt & Cokendolpher, 1991). Megalopsalidinae contains three genera (a checklist appears in Taylor, 2004): Megalopsalis (13 spp.), Pantopsalis (11 spp.), and Spinicrus (8 spp.). Neopilionidae was originally described by Lawrence (1931) in Phalangiidae to include the monotypic genus Neopilio from South Africa. The subfamily was primarily based upon the reduced or absent pedipalpal claw and equal-sized teeth on the chelicerae. South American members were added when Mello-Leitão, (1933b) synonymized Enantiobuninae (Mello-Leitão, 1931, June) with the Neopilioninae (Lawrence, 1931, April). Roewer (1957b) retained the placement in Phalangiidae. Ringuelet (1959) synonymized the South American genera Thrasychirus with Enantiobunus and transferred them to the Leiobuninae (Phalangiidae). Kauri (1961) added the monotypic genus Vibone from South Africa and raised Neopilioninae to family status. Silhavy (1970) recognized three subfamilies within the Neopilionidae: Neopilioninae, Megalopsalidinae, and Enantiobuninae. Shear (1982) and Hunt and Cokendolpher (1991) redescribed the family, with Megalopsalidinae excluded. Hunt and Cokendolpher (1991) also added the first Australian members and described another subfamily (Ballarrinae), primarily on the basis of differences in the pedipalps (setation and reflexed junction of patella and tibia). Although Hunt and Cokendolpher (1991) suggested raising Enantiobuninae to full family status, this has still not been formally done. Phalangiidae is the longest- and best-known group of harvestmen for people living in temperate to subarctic regions of Eurasia (especially Europe) and North America. They have a soft or leathery body (rarely heavily sclerotized, as in Scleropilio) and relatively long legs. The dorsum of the body lacks large tubercles, cones, or long spines (such as those often found in members of Asian Gagrellinae, or Sclerosomatinae) but has sparse short spines. Pedipalps and legs are also often spiny, and legs are generally angulate in cross section in proximal segments (from femora to tibiae). The spiny habitus, leg coxae without marginal rows of denticles, smooth, nonpectinated tarsal claw of the pedipalp, and nonalate penis with a welldelimited glans dorsally bent at an acute angle in resting position and a distinct, more or less movable stylus serve to identify this family, though there are a few exceptions. All the external characters traditionally used to delimit species and genera of Phalangiidae (e.g., armature of dorsal integument of body or appendages) are often highly variable between populations of the same species, or sometimes even within a

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single population of a species. Because of this difficulty, taxonomy of this family has been rather chaotic. The situation has been much improved recently by extensive revisions emphasizing penial morphology made mainly by Martens (for European and Himalayan species), Starega (for Europe, Asia, and Africa), and Cokendolpher (for America), though many genera and species still await further revision. Subfamilial classification of Phalangiidae has not yet been settled because no character can clearly define each subfamily so far proposed. Most widely accepted is a dichotomy of the family into the subfamilies Oligolophinae and Phalangiinae sensu lato, mainly by the presence or absence of a ventral spur on the chelicera (Martens, 1978b). However, the two character states are found in two congeneric species (Paroligolophus agrestis and P. meadii) whose close relationship is well supported by all the other characters (Martens, 1978b), and in some cases it is exemplified as sexual dimorphism or as intraspecific variation (e.g., Metaplatybunus hypanicus, Liopilio yukon). Starega (1973) synonymized Dentizacheinae Silhavy, 1961 with Phalangiinae. Starega (1976a,b) split Phalangiinae s. lat. further into three subfamilies (Phalangiinae sensu stricto, Platybuninae, and Opilioninae), and this system has been followed by some researchers. The monophyly of each of these subfamilies has not yet been tested (it is highly probable that at least Phalangiinae s. str. is not monophyletic), and there are many species that do not conform well to the keys. Protolophidae, endemic to western North America, was originally described as a tribe (Protolophini) of the family Phalangiidae by Banks (1893). Later, Roewer (1911) transferred the type and only genus (Protolophus) to the subfamily Leptobunini (Roewer, 1923, corrected the ending to Leptobuninae), where it remained until the subfamily was dismantled by Cokendolpher (1985b). He suggested raising the group to subfamily status and emended the ending to Protolophinae within the family Gagrellidae. Edgar (1990) listed the genus in the Sclerosomatidae, and Crawford (1992) retained the group at the subfamily level within an unspecified family, but remarked that the group may be justified as a family. Cokendolpher and Lee (1993) raised the group to family status and recognized only the single monogeneric subfamily Protolophinae. Sclerosomatidae was traditionally included in the family Phalangiidae (Loman, 1903b, 1906), but modern classifications (Crawford, 1992; Cokendolpher & Lee, 1993; Giribet et al., 2002) recognize it as a separate family, albeit unclearly delimited. Sclerosomatidae is the largest family in the order Opiliones, with more than 1,300 species distributed in the New and Old Worlds. The family is currently composed of Sclerosomatinae, Gagrellinae, Gyinae (= Gyantinae), Leiobuninae, and the Metopilio genus group of Cokendolpher (1984b) (Crawford, 1992). The more appropriate rank status of these entities is a subject still under discussion. The first four are assigned status of either family or subfamily depending on the author, while the Metopilio assemblage may be an unnamed family or subfamily (Cokendolpher, 1984b). Because of its genital morphology, the assemblage has been listed within Sclerosomatidae by Crawford (1992), later followed by Cokendolpher and Lee (1993). Starega (1976a,b) proposed raising Gagrellinae, Gyinae, and Sclerosomatinae to family status, with Leiobuninae in-

Taxonomy

cluded in Gagrellidae. Martens (1978b, 1982, 1987) refused Starega’s proposal and also included the genera Dicranopalpus and Amilenus in Gyinae. Crawford (1992) disagreed with these inclusions and transferred the genera to what he called the Dicranopalpus group, an assemblage of seven genera considered by him as a family incertae sedis. Crawford also suggested that Leiobuninae and Gagrellinae should be separated for zoogeographic reasons and by the harder opisthosomal scutum present in Gagrellinae. The boundaries among the four accepted subfamilies are obscure, and the inclusion of the Metopilio group as part of Sclerosomatidae has been followed only by Cokendolpher and Sissom (2000). The distinctions between Gagrellinae and Leiobuninae are not clear, and there is morphological continuity at the supraspecific level. The characters supporting the taxa are poorly defined. For the most part, the formerly raised groups of species are artificial and lack phylogenetic meaning. A modern catalogue of the whole group is needed since the only available one is outdated and only covers Neotropical Gagrellinae (Roewer, 1953). Overall, this suborder of common harvestmen needs major phylogenetic studies. Key to Eupnoi families (subfamilies) 1. Eyes enormous and ocularium occupies most of the prosoma (Figures 4.7a,b); legs II shorter than legs IV. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Caddidae....2 . Eyes and ocularium normal; legs II longer than legs IV. . . . . . . . . . . . . . . . . . . . . . . 3 2. Cheliceral segment I with ventral spur; pedipalpal tarsus longer than tibia (Figure 4.7b). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Caddidae (Caddinae) . Cheliceral segment I without ventral spur; pedipalpal tibia longer than tarsus (Figure 4.7a) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Caddidae (Acropsopilioninae) 3. Spiracle of opisthosoma covered by grate of spines (Figure 4.9d) (Distribution: temperate regions of Southern Hemisphere) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 . Spiracle of opisthosoma with entapophysis and no grill. . . . . . . . . . . . . . . . . . . . . . 8 4. Penis with paired lateral bristle groups at articulation of glans and shaft (Figure 4.8d); Australia and New Zealand . . . . . . . . . . . . . . . . . . . . . . . Monoscutidae....5 . Penis without paired lateral bristle groups, at most a pair of spines, at articulation of glans and shaft . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Neopilionidae....6 5. Body rounded; only carapace sclerotized; opisthosoma smooth. Legs relatively long. Chelicerae sexually dimorphic; those of male enormously enlarged (Figure 4.8g). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Monoscutidae (Megalopsalidinae) . Body dorsoventrally flattened, heavily sclerotized; dorsum ornamented. Legs short (femur I less than body width). Sexual dimorphism absent (Figure 4.8c). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Monoscutidae (Monoscutinae) 6. Pedipalpal patella very long (patella about twice as long as tibia); tibia reflexed on the patella so that dorsal angle is less than 180° (Figure 4.9b); Australia, Chile . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Neopilionidae (Ballarrinae)

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. Pedipalpal patella shorter (patella less than 15% longer than tibia); tibia not reflexed upward on patella (Figure 4.9e). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 7. Pedipalpal patella and tibia with dense pile of setae; patella slightly longer than tibia; pedipalpal claw reduced and smooth (Figure 4.9e,f); South Africa. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Neopilionidae (Neopilioninae) . Pedipalps without dense pile of setae; patella much shorter than tibia; claw large and toothed (Figure 4.9c); Chile, Argentina, Brazil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Neopilionidae (Enantiobuninae) 8. Male pedipalp almost always greatly thickened (Figure 4.8h); tarsus shorter than tibia; western North America . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Protolophidae . Pedipalpal tarsus longer than tibia. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 9. Pedipalpal claw smooth. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Phalangiidae...10 . Pedipalpal claw toothed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sclerosomatidae...13 10. Basal segment of chelicera with ventral spur (Figure 4.10f); chelicerae not strikingly different between the sexes . . . . . . . . . . . . Phalangiidae (Oligolophinae) . Basal segment of chelicera without ventral spur; chelicerae sometimes differ between the sexes (Figure 4.10h) . . . . Phalangiidae (Phalangiinae sensu lato) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11 11. Pedipalpal femur (often also remaining segments) thorned ventrally (Figure 4.10j); chelicerae of both sexes similar; penis rodlike, with slightly widened base . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Phalangiidae (Platybuninae) . Pedipalp lacks ventral thorns; male chelicera tends to be modified (Figure 4.10h) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 12. Pedipalpal patella and tibia of adults without distomesal apophyses; chelicerae of both sexes basically the same in structure, though often enormously expanded in male; leg I of male enormously swollen in some species; shaft of penis dorsoventrally flattened (Figure 4.10k) . . . . . . . . . Phalangiidae (Opilioninae) . Pedipalpal patella and tibia with distomesal apophyses; male chelicera tends to be modified in morphology (especially in the distal segment); femur of male pedipalp usually with ventral rows of denticles; shaft of penis generally more rounded. . . . . . . . . . . . . . . . . . . . . . Phalangiidae (Phalangiinae sensu stricto) 13. Coxae II showing distally blunt lobes . . . . . . . . . . . . Sclerosomatidae (Gyinae) . Coxae II not as above . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14 14. Leg femora with noduli (at least one on femur II, Figure 4.11p); dorsum sclerotized . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sclerosomatidae (Gagrellinae) . Leg femora usually without noduli. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15 15. Dorsum heavily sclerotized, often with spines or humps (Figure 4.11c); penis tapering toward tip (Figure 4.11l) . . . . . . . Sclerosomatidae (Sclerosomatinae) . Dorsum less sclerotized, usually smooth; penis not tapering, often with alate part). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sclerosomatidae (Leiobuninae)

Taxonomy

Caddidae Banks, 1893 Ricardo Pinto-da-Rocha and Jürgen Gruber Etymology: Caddo, from North American Caddo, indigenous culture, people, and language. Characterization: • Size: Body length mostly between 1 and 3 mm. • Dorsum (Figures 4.7a–c): Integument largely coriaceous, never heavily sclerotized (some Austropsopilio/Tasmanopilio with small sclerite plates on anterior area of opisthosomal dorsum). Ocularium huge and broad, occupying most of propeltidium and protruding over its anterior rim, sometimes hiding the chelicerae (Acropsopilio), or narrower and inclined forward (some Austropsopilio); deeply depressed medially; smooth, with two anterior tubercles (Austropsopilio), or with two rows of large tubercles (Hesperopilio); eyes large. Prosomal dorsum as broad as long; thoracic segments mostly well marked (in Caddo spp. with two small “metapeltidial cones”). Opisthosomal dorsum and free tergites smooth and unarmed in most species, with setigerous tubercles in Austropsopilio, with paired setae or tubercles in Hesperopilio. Dorsum with three to five anterior segments fused (or perhaps more?) in a sort of scutum, the remaining ones free. • Venter: Genital operculum small in Caddo (Figure 4.7g), resembling the state in some Dyspnoi; large, blunt in acropsopilionines (Figure 4.7f), more similar to condition in phalangioids (Eupnoi). Sternum free. Labium very small in acropsopilionines, larger in Caddo. Coxapophyses of pedipalps with apical tooth (Figure 4.7f, Acropsopilio, Caddella). Coxapophyses of leg I: basal fixed portion longer in Caddo, distal movable (setate) sclerites shorter in transverse axis in Caddo, longer and aligned transversely in acropsopilionines; of leg II immovable. Coxae III–IV with larger lobes in Austropsopilio. Spiracles visible, described in detail only in some species: small, (half) rounded in Acropsopilio chilensis, elongate in A. venezuelensis and Austropsopilio; narrow, slitlike in Caddo, bordered by a smooth “operculum” and enlarged granules; or “kidney shaped” and covered by “grille” in Caddella (Kauri, 1961). Shear (2004) reported “closed” spiracles and absence of tracheae in Acropsopilio chomulae. • Chelicerae: Segment I with (Caddinae) or without (Acropsopilioninae) ventral spur; chela fingers with small or coarser darkened teeth, no narrow diaphanous ones. • Pedipalps (Figures 4.7a,b,d,e): Rather massive and armed with spines in some species. Femur mostly with one to four ventral strong apophyses, each bearing one or several setae, sometimes similar ones on patella and tibia (e.g., Austropsopilio); tibia and tarsus with ventral setae or totally covered by setae. Glandular setae may be present on femur to tarsus; microtrichia are lacking. Claw movable by muscles in Caddo, present (movable?) in Caddella, Hesperopilio, and Austropsopilio males; weak and without muscles in Acropsopilio, lacking totally

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e

k Figure 4.7. Caddidae. (a) Habitus lateral of Acropsopilio neozealandiae; (b) habitus lateral of female Caddo agilis; (c) habitus dorsal of Austropsopilio sudamericanus; (d) prolateral of pedipalp of male C. agilis; (e) prolateral of distal segments of pedipalp of female Austropsopilio sudamericanus; (f) ventral of anterior part of Acropsopilio boopis; (g) same for C. agilis; (h) penis of Caddella capensis; (i) penis of C. agilis, ventral; (j) ovipositor of C. agilis; (k) ovipositor of Tasmanopilio fuscus. Scale bars: c–e = 0.5 mm; g, i = 0.5 mm; j–k = 0.2 mm. Figures a–b, h from Shear (1975a); d, g, i–k from Gruber (1975); c, e from Shultz and Cekalovic (2003); f from Suzuki (1976c).

Taxonomy

•

•

•

•

in Austropsopilio females, which possess a swollen “brushlike” tarsus with glandular setae (Figure 4.7e). Legs: Short in most species, longer and slender in Caddo and Caddella; legs IV are longest in several species, not so in, for example, Hesperopilio. No accessory spiracles on tibiae. Metatarsi (pseudo)articulated, tarsi with low to moderate number of tarsomeres (e.g., 6 to 9 in small Acropsopilio spp., up to 15 to 27 in the larger Caddella spp.). Claws single, smooth. Genitalia: Ovipositor (Figures 4.7j,k): corpus short with at most 3 (most Acropsopilioninae) or longer with 7–12 (Caddinae, Hesperopilio) annuli, furca twosegmented, distal portion long, bearing paired apical sensory organs: a short cone with several immovable branches in Caddinae (see Martens et al., 1981) and Hesperopilio, a long forked seta in most Acropsopilio spp., a four- or fivepronged one in A. boopis and Austropsopilio; sensilla lacking in Caddella. In Tasmanopilio fuscus shaft is soft skinned without sclerotized rings, vagina externa with complex sclerotized armature. Receptacula seminis reduced in some species, probably in connection with parthenogenesis; well developed in Caddella (Kauri, 1961: in base of ovipositor, “Dyspnoi-like”). Caddo agilis has “normally” developed receptacula according to Martens et al. (1981); C. pepperella none (Shear, 1975a). Penis (known in only a few species): in Caddo (Figure 4.7i) rather phalangiid-like, shaft with one muscle, symmetrical glans with straight stylus and a dorsal spine; in Hesperopilio somewhat similar, with glans “sinuous, tapering, with membranous part at base”; in other acropsopilionines penis more or less asymmetrical; glans portion may be long, bifurcate apically, and showing torsion (Caddella, see Figure 4.7h; Austropsopilio / Tasmanopilio), with thin flattened apex (some Acropsopilio), with strong setae (two to nine) on middle region of penis (presumably basal part of glans) of Acropsopilio. Color: Body and legs from yellowish to dark brown; silvery bands and specks and brown parts are common. Prosoma silvery to brown. Ocularium and pedipalp white to brown. Sexual dimorphism: Unknown in Acropsopilio (González-Sponga, 1992a; Capocasale, 2004). Male chelicerae in two Caddella species bear apophyses on first and second segments; C. africana shows difference in chela shape (Kauri, 1961; Starega, 1988). Pedipalp of Caddo agilis longer and more massive in the male than in the female; femur with one ventral blunt tubercle in males and three long setiferous tubercles and distomesal setose lobe in females; male tibia and tarsus ventrally with many short pegs; glandular setae less well developed in male (Figure 4.7d). Males of Austropsopilio with claw, females without; there the swollen tarsus is “brushlike” with glandular setae (Figure 4.7e). Pedipalpal patella of Hesperopilio mainae with large setose lobe in males, lacking in females; tibia small without glandular setae in males, subglobose and heavily setose in females; tarsus with curved claw in male, reduced with small claw in female.

Distribution: Caddids show a wide but discontinuous distribution (Suzuki et al., 1977): Acropsopilio (Japan; North America: eastern USA to southeastern Canada,

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southern Mexico; South America: Venezuela, southern Brazil, Chile, Argentina, Bolivia, Uruguay; eastern Australia, New Zealand); Austropsopilio (eastern Australia and Tasmania; Chile; Shultz & Cekalovic, 2003); Tasmanopilio (Tasmania); Hesperopilio (western Australia, Chile); Caddella (southern South Africa, Kauri, 1961; Stare˛ga, 1988); Caddo (eastern North America: USA, southern Canada; Japan, Kuril Islands). Disjunction patterns involve ones of presumably Neogene age in South America (Maury et al., 1996) and the Holarctic region (eastern North America– Japan: Shultz & Regier, 2004), as well as early/pre-Tertiary ones (South-America– Australia) or even older Gondwanan ones (Africa-Australia). Relationships: A group of controversial position between Eupnoi and Dyspnoi since Silvestri (1905)—a possibly relictual basal group or “connecting link,” as mentioned by several authors. Generally, Caddo looks more “phalangiid-like” (e.g., pedipalps, genitalia), acropsopilionines more “dyspnoan” (pedipalp proportions), but the aspect of the genital operculum shows Caddo more “dyspnoan” than the more “phalangiidlike” acropsopilionines in this respect. Female genitalia approach a “dyspnoan” condition (e.g., Austropsopilio) from a “phalangiid-like” one in Caddo, but even in the former case the apical furca segment is “long” and sclerotized with paired apical sensilla. This character and the dentition of the chelicerae preclude inclusion in Dyspnoi. The monophyly of the family still needs to be proved because of the presence of considerable differences in pedipalpal (especially the tarsus) and genital morphology; doubts have been expressed, for example, by Dumitrescu (1980) and Martens (1986). Hesperopilio may have an intermediate position in genital morphology (Shear, 1996), which at present speaks against a division into two families. Generally, recent morphology-based phylogenetic analyses show Caddidae/Caddoidea as a sister group of Phalangiidae/Phalangioidea (Martens et al., 1981; Martens, 1986; Shultz, 1998; Giribet et al., 1999, 2002), as do later sequence-based analyses (Shultz & Regier, 2001; Giribet et al., 1999, 2002). However, only one terminal was employed (Caddo agilis), so the monophyly of the superfamily was not tested. Main references: • Systematics: Shear (1975a, 1996), Suzuki (1976c). • Natural history: Gruber (1975), Shear (1975a, 1996), Suzuki (1976c), Suzuki et al. (1977), Suzuki & Tsurusaki (1983), González-Sponga (1992a), Tsurusaki (2003), Capocasale (2004).

Monoscutidae Forster, 1948 James C. Cokendolpher and Christopher K. Taylor Etymology: Monoscutum, from Greek monos and Latin scutum, single shield. Refers to the fused dorsal aspect of the body of members of the Monoscutinae. Characterization: • Size: Total body length ranges from 2 to 3 mm for the Monoscutinae to 3 to 10 mm in the Megalopsalidinae.

Taxonomy

• Dorsum (Figures 4.8a,g): Ozopores visible from above. Monoscutinae: body dorsoventrally flattened; heavily sclerotized, dorsum ornamented. All tergites fused except for division between prosoma and opisthosoma. Megalopsalidinae: body rounded, leathery except sclerotized carapace, dorsum of opisthosoma smooth. Carapace: Monoscutinae, sclerotized; Megalopsalidinae: sclerotized, denticulate or smooth, with final posterior tergite of prosoma free in male, smooth and less sclerotized in female.

a

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i g Figure 4.8. Monoscutidae and Protolophidae. (a–g) Monoscutidae: (a) dorsal view of male Monoscutum titirangiense (Monoscutinae) from New Zealand; (b) anterior and (c) lateral view of male chelicera; (d) penis; (e) ovipositor of Acihasta salebrosa (Monoscutinae) from New Zealand; (f) seminal receptacles; note that the middle pair of receptacles is reduced in size. (g) Dorsal view of male of Megalopsalis sp. (Megalopsalidinae) from New Zealand. (h–i) Protolophidae, pedipalp: (h) “normal,” male; (i) female of Protolophus singularis from USA.

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• Venter: Opisthosomal sternites fused, but separated by faint transverse grooves in Monoscutinae. Sternites free in Megalopsalidinae. Venter of opisthosoma and coxae smooth. Spiracles with or without chitinous grate; without entapophysis. • Chelicerae (Figures 4.8b,c,g): Monoscutinae: not enlarged and smooth except for forwardly directed ventral spur on base of first segment. Megalopsalidinae: enormously enlarged in male, both segments heavily denticulate; chelicerae of female not enlarged, denticles present or absent dorsally on first segment. • Pedipalps: Monoscutinae: with prominent apophysis on patella; patella and tibia subequal in length (tibia only slightly longer). Megalopsalidinae: apophysis present or absent on patella. Claw pectinate in Monoscutinae, Spinicrus, and Australian Megalopsalis, smooth in Pantopsalis and Megalopsalis grimmetti. • Legs: Legs round in cross section. Femora of male at least partially denticulate, of females and other leg segments of both sexes usually smooth except for dorsal distally projecting spines at distal end of patella (Megalopsalidinae). • Genitalia (Figures 4.8d–f): Penis with two pairs of bristle groups associated with the shaft-glans articulation; stylus twisted. Ovipositor with threesegmented furca and single slit sensillum on each side of the second pair of furcal segments. Seminal receptacles either one pair (Australian taxa) or two pairs (one pair much smaller) (New Zealand taxa—Megalopsalis species have two pairs of seminal receptacles). • Color: Most species are drab in appearance, being shades of browns to black. Some Megalopsalis are jet black—the male of M. inconstans is especially striking, being jet black with bright orange patches on the carapace. Acihasta salebrosa is tan and brown with numerous opalescent white and gold specks over the dorsum. • Sexual dimorphism: Absent in Monoscutinae. All Megalopsalidinae are sexually dimorphic, and some Pantopsalis species also have male polymorphisms (“normal” and “broad-chelicerate”). Females have small, smooth chelicerae, not as long as the body and usually not rising above the prosoma. In contrast, the males have enormous, strongly denticulate chelicerae, at least twice as long as the body and often longer (Forster, 1949, 1964; Forster & Forster, 2003). Males and females may also differ in degree of sclerotization and in overall color pattern. Denticulation, if it occurs, is mostly restricted to the males. In some species of Pantopsalis, two forms of male have been identified. In the most common form, the chelicerae are longer and more slender than in the other (Taylor, 2004). Males have also been found that resemble females in coloration and degree of sclerotization of the body, though chelicerae remain enlarged. Distribution: Throughout Australia and New Zealand, including Tasmania and the subantarctic islands of New Zealand (Auckland, Snares, Campbell Islands). Relationships: The families of Phalangioidea fall into two groups based on spiracle microstructure: the mainly Northern Hemisphere taxa (Phalangiidae and Sclerosomatidae) with the spiracle accompanied by an entapophysis, and the Southern Hemisphere taxa (Neopilionidae and Monoscutidae) with the spiracles covered by a grate of

Taxonomy

spines in most species. Silhavy (1970) placed the Southern Hemisphere taxa in a single family (Neopilionidae) on the basis of spiracular structure; however, it is debatable whether the grate is homologous in all species (Hunt, 1990b; Hunt & Cokendolpher, 1991), and as a spiracular grate is also found in taxa outside the Phalangioidea (Hunt & Cokendolpher, 1991), it is probably plesiomorphic for the superfamily. The entapophyseate taxa probably represent a monophyletic group of uncertain affinities within the paraphyletic Southern Hemisphere taxa (Hunt & Cokendolpher, 1991). Main references: • Systematics: Forster (1948a, 1949), Silhavy (1970), Martens (1976), Hunt (1990b), Hunt & Cokendolpher (1991), Crawford (1992), Taylor (2004). • Natural history: Meyer-Rochow & Liddle (1988), Hunt (1991).

Neopilionidae Lawrence, 1931 James C. Cokendolpher Etymology: Neopilio, from Greek neo, “new,” and opilio, a genus of harvestman. Characterization: • Size: Ranges in body length from the minute Americovibone lanfrancoae (0.86 mm) to over 4 mm in the Enantiobuninae. • Dorsum (Figure 4.9a): Body small to medium, soft. Integument usually thin, smooth, at the most with minute spines. Last two to four opisthosomal tergites faintly defined by grooves; sternites may or may not be clearly defined. Ocularium low, rounded, canaliculated, unarmed or with minute spines. Ozophores visible from above. • Venter: Coxae unarmed ventrally except for small setae; endites of coxae II more or less perpendicular to long axis of body. Lateral opisthosomal sclerites absent. Opisthosomal spiracle oval, covered by a chitinous grate, visible or concealed beneath coxae IV, lacking an entapophysis (Figure 4.9d). Corona analis absent or vestigial. • Chelicerae: Small (Neopilioninae/Ballarrinae), medium to large (Enantiobuninae); first segment with or without a ventral spur; fingers with continuous row of teeth of subuniform size in most species. • Pedipalps (Figures 4.9b,c,e,f): Both patella and tarsus longer than tibia, patella often longer than tarsus (Neopilioninae and Ballarrinae); patella shorter than tibia and tarsus in Enantiobuninae; femur through tarsus with plumose setae (Neopilioninae and Ballarrinae), absent in the Enantiobuninae; patella and tibia with (Neopilioninae) or without dense pile of setae; tarsal claw lacking or minute with no ventral teeth (Figure 4.9e), or minute with ventral tooth (Neopilioninae and Ballarrinae), or large and pectinate (Enantiobuninae, Figure 4.9c). • Legs: Long and slender in Neopilioninae and Ballarrinae, shorter and thicker in the Enantiobuninae (Figure 4.9a); round in cross section; pseudoarticula-

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a

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Figure 4.9. Neopilionidae. (a) Dorsal view of female Thrasychirus dentichelis (Enantiobuninae) from Chile; (b) lateral view of male pedipalpus of Plesioballarra crinis (Ballarrinae) from Australia (photo: Glenn S. Hunt); (c) tip of pedipalpal tarsus of Thrasychirus modestus (Enantiobuninae) from Chile; (d) abdominal spiracle of Thrasychirus sp. (Enantiobuninae) from Chile. (e–f) Lateral view of female pedipalp (e) and reduced tarsal claw (f) of Neopilio australis (Neopilioninae) from South Africa. (g– j) Penes: (g) Ballarra alpina (Ballarrinae) from Australia; (h) Americovibone lanfrancoae (Ballarrinae) from Chile; (i) Neopilio australis (Neopilioninae) from South Africa; (j) Thrasychirus sp. from Chile (Enantiobuninae). (k–l) Ovipositors: (k) Ballarra longipalpus (Ballarrinae) from Australia; (l) Neopilio australis (Neopilioninae) from South Africa. Figures g–k from Hunt and Cokendolpher (1991).

Taxonomy

tions often present in all metatarsi, femur II, and tibia II; tarsi each with a simple claw that might have small teeth on each side. Leg tibiae with accessory spiracles, often inconspicuous. • Genitalia (Figures 4.9g–l): Penis with one muscle; glans in more or less same axis as shaft; tufts of bristles lacking at glans/shaft junction, but shaft may have left ventrolateral barbed process or pairs of spines. Ovipositor segmented; furca usually long and slender, three-segmented, and with sensory lobes (not in Enantiobuninae); with one to many slit sensilla per second segment; two (Figure 4.9k) or four (Figure 4.9l) seminal receptacles. • Color: Most species are drab in appearance, being from shades of browns to black; but some of the few known species of Opiliones with blue pigment occur in the Enantiobuninae from southern Chile. • Sexual dimorphism: Usually slight. In the Neopilioninae the male pedipalps are thinner than in females. Males of several Ballarrinae and Enantiobuninae have larger chelicerae than females; this is especially noticeable in the Enantiobuninae genus Thrasychiroides and some species of Thrasychirus. Distribution: Neopilioninae are from the Western Cape Province in South Africa; Ballarrinae are from the Western Cape Province in South Africa, southwestern and southeastern Australia (southern Queensland and New South Wales to northern Victoria and Western Australia), and southern Chile (Magallanes); Enantiobuninae are from central and southern Chile, western and southern Argentina, and Rio Grande do Sul to Rio de Janeiro highlands, Brazil. Relationships: See “Relationships” of Monoscutidae. Main references: • Systematics: Lawrence (1931), Mello-Leitão (1931), Ringuelet (1959), Kauri (1961), Hunt & Cokendolpher (1991), Crawford (1992). • Natural history: Cokendolpher & Lanfranco (1985), Hunt & Cokendolpher (1991).

Phalangiidae Latreille, 1802 Nobuo Tsurusaki Etymology: Phalangium, from Greek phalangion, meaning harvestman or longlegged spider (sometimes referring also to a kind of formidable-looking arachnid such as solifuges), or phalangos, meaning finger segment or joint. Characterization: • Size: Body length ranging from 2.2 to 12 mm, with most species around 5 mm. Leg II 10–55 mm long. • Dorsum (Figures 4.10a–c,e): Entire body generally soft and leathery, rarely sclerotized (e.g., Scleropilio). Ocularium relatively high and usually covered dorsally with several tubercles, except for some Opilioninae, such as Egaenus.

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Figure 4.10. Phalangiidae. (a–e) Dorsal and ventral (d) views of habitus, male; (a) Odiellus tienmushanensis (Oligolophinae); (b) Phalangium opilio (Phalangiinae, sensu stricto); (c–d) Acanthomegabunus sibiricus (Platybuninae); (e) Himalphalangium spinulatus (Opilioninae). (f) Chelicera of Oligolophinae (note presence of a ventral spur on basal segment, arrowed). (g) Chelicera and pedipalp (above) of male Phalangium opilio (note absence of a ventral spur). (h–i) Mesal view of chelicerae (h) and pedipalp (i) of male (above) and female (below) of Homolophus arcticus (Opilioninae). (j) Mesal view of pedipalp of male (above) and female (below) of Acanthomegabunus sibiricus. (k–l) Dorsal and lateral views of penis: (k) Homolophus arcticus; (l) Scleropilio insolens (Opilioninae). (m) Ovipositor of Acanthomegabunus sibiricus. Figures a, e–g after Tsurusaki and Song (2000); b, Tsurusaki, original figure; c–d, j, Tsurusaki et al. (2000b); h– i, k, Tsurusaki (1987); l–m, Tsurusaki et al. (2000a).

Taxonomy

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•

Anterior rim of prosoma often medially with a group of tubercles (often called a “trident” when the group consists of three conspicuous tubercles). Ozopores situated near the bases of legs I, visible from above. Venter (Figure 4.10d): Leg coxae without marginal rows of denticles, smooth and with only sparse setae. Genital operculum and opisthosomal sternites also with only sparse setae. Lateral opisthosomal sclerites absent. The spiracles are not covered with a chitinous grate (a discriminating feature from Neopilionidae and Monoscutidae, some of which show resemblance in external appearance to this family). Chelicerae: Proximal cheliceral segment with (Oligolophinae, Figure 4.10f, arrowed) or without (Phalangiinae sensu lato, Figure 4.10h) a ventral spur. In some species the male chelicerae are conspicuously enlarged in size (e.g., Zacheus, Egaenus, Homolophus), with elongated processes generally on the second segment (e.g., Phalangium, Figure 4.10g, arrowed), or extremely elongated (some species of the African genus Rhampsinitus). Pedipalps (Figures 4.10i–j): Claw smooth but rarely slightly toothed (e.g., African genus Odontobunus, North American genus Leptobunus, or European species Rilaena balcanica). Legs: Cylindrical but often pentagonal or hexagonal in cross section, with rows of spines or setae on the edges. Femora without nodules. Tibiae with two accessory spiracles, one near the proximal and one near the apical end. Genitalia: Penial glans (in resting position) bent dorsally at an acute angle at the base (Figures 4.10k,l); this clearly delimits the movable, articulated glans from the penial shaft. Stylus also well delimited and movable. Shaft lacks lateral wings. Ovipositor (Figure 4.10m) long and segmented with a bifurcated tip. Color: Body usually light brown to dark brown or gray, sometimes with greenish tones or with white areas, some species more colorful with reddish to pink areas; venter often lighter colored, distinctly white (e.g., in Phalangium opilio). On dorsum there is often a medial marking referred to as the “saddle” that usually extends from the preocular area of the prosoma to opisthosomal tergite V (sometimes to tergites VII–VIII) and sometimes with a lighter median band. Sexual dimorphism: Generally the “saddle” is more conspicuous in males than in females (with exceptions, e.g., Opilio, where the female has the more distinctly marked dorsum). In many species (especially in species other than Platybuninae), the pedipalpal tarsus bears a row (or a belt) of denticles ventromedially in males but not in females. Male chelicerae are often modified in different ways in Phalangiinae sensu stricto, or inflated in Opilioninae. Leg I is also often swollen in males of Opilioninae.

Distribution: Eurasia (excluding southern and southeastern Asia), Africa (North to South Africa), and North America. Some synanthropic species (Phalangium opilio, Opilio parietinus) can also be found in Australia and New Zealand as introduced (Gruber & Hunt, 1973). Among the harvestmen of Phalangioidea (so-called long-

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legged harvestmen), this family seems to be most adapted to arid environments and is even found in semiarid lands with sparse vegetation such as the Middle East, central Asia, and Mongolia. The most northern member of Opiliones is the phalangiid Mitopus morio, which occurs well past the Arctic Circle as far north as 73° (D. Walker, 1860). Among the four subfamilies, Platybuninae seems to be limited mostly to the western half of Eurasia and is most diverse in the southern part of Europe and the westernmost part of Asia. Opilioninae occupies the whole temperate region of Eurasia, with a large number of species in Europe. In Siberia (excluding the Maritime Province), Mongolia, and the northern half of China, including Beijing, Phalangiidae is the only family of Phalangioidea encountered. Relationships: Delimitation of Phalangiidae has been a moot issue for decades. In his influential work Martens (1978b) defined Phalangiidae broadly to include Leiobuninae, Gyinae, Sclerosomatinae, and Gagrellinae, because Gyinae shows a condition intermediate between Phalangiidae sensu stricto and LeiobuninaeGagrellinae-Sclerosomatinae by having pedipalps with a nonpectinate claw. However, recent researchers, especially those from countries outside the distributional range of Gyinae, tend to prefer a narrower definition of Phalangiidae (e.g., Shear, 1982; Hillyard & Sankey, 1989; Crawford, 1992), which has been followed here. Other than Gyinae, the North American “Metopilio assemblage” (which includes Dalquestia, Diguetinus, Eurybunus, Globipes, and Metopilio and is now provisionally treated under Sclerosomatidae; Gruber, 1969a; Cokendolpher, 1984b, Cokendolpher & Lee, 1993) also shows a resemblance to this family in appearance. Removal of the assemblage from Phalangiidae on the basis of the striking difference in penial morphology (harvestmen of this assemblage have an alated penis with a glans jointed straight to the shaft) was supported by a recent molecular phylogeny of Opiliones (Giribet et al., 2002), where Dalquestia occupies a sister position to “Phalangiidae + Sclerosomatidae.” The genus Lanthanopilio from Costa Rica, which was first described under Phalangiinae (Cokendolpher & Cokendolpher, 1984) but was provisionally transferred to the Dicranopalpus group (family incertae sedis) by Crawford (1992), may be placed near the “Metopilio assemblage.” An external appearance similar to that of Phalangiidae is also found in some species of Neopilionidae (e.g., South American Enantiobuninae; see Cokendolpher & Lanfranco, 1985). These facts suggest that some of the diagnostic characters of Phalangiidae such as soft or leathery body with a typical “saddle” marking are plesiomorphic, though the possibility of convergence cannot be excluded. Main references: • Systematics: Martens (1973, 1978b), Starega (1976a,b, 1984, 2003), Cokendolpher (1981b, 1985b), Hillyard & Sankey (1989), Edgar (1990), Crawford (1992), Tsurusaki & Song (2000), Tsurusaki et al. (2000b). • Natural history: Phillipson (1959), Spoek (1963), Edgar (1971), Slagsvold (1976), Tsurusaki (2003).

Taxonomy

Protolophidae Banks, 1893 James C. Cokendolpher Etymology: Protolophus, presumably from Greek proto, first, and Greek lophus, crest or tuft. It is uncertain what Banks meant by his name. It could refer to the crest of spines on the ocularium or the crest or tuft of small spines on the small preocular hump. Characterization: • Size: Body length (excluding chelicerae) 4–6 mm (males), 6–8 mm (females). • Dorsum: Ozopores facing anterolaterally, but visible from above. First five areas fused, each generally bearing a median pair of humps. • Carapace: Sclerotized. Preocular area without trident. Large hump present, sometimes reduced. • Venter: Opisthosomal sternites free. Coxae often with lateral rows of teeth; maxillary lobes of the second coxae straight. Spiracles with entapophysis and no grill. • Chelicerae: Without apophysis or large tubercles; first segment ventrally with spur. • Pedipalps (Figures 4.8h,i): Female pedipalps slender with large apophysis on distal end of patella and sometimes smaller apophysis on end of tibia. Male pedipalps almost always greatly thickened and rarely with an apophysis; tarsus generally shorter than tibia and narrowing throughout its length; tibia with small ridge and often an adjoining depression ventrally in males; tarsus with rows of tubercles ventrally. Tarsal claw small, smooth, and generally untoothed. • Legs: Legs relatively short (femur II generally shorter than body length); round in cross section; all femora and tibiae without pseudoarticulations or nodules. • Genitalia: Penis with a relatively straight shaft, without a noticeable junction between glans and truncus; not inclined or otherwise demarcated except by the presence of very minute setae on the glans surface. Ovipositor with threesegmented furca with one slit sensillum per side on the second segment; two seminal receptacles. • Color: Body and legs light tan to black, sometimes mottled or irregularly banded. One species with white lines on the dorsum. • Sexual dimorphism (Figures 4.8h,i): Present in all species. Females have smaller, smooth chelicerae and thin pedipalpal segments with a long apophysis on the patellae and shorter apophysis on the distal end of the tibiae. In contrast, the males have large chelicerae and greatly thickened pedipalps, generally without apophysis. The male pedipalpal tarsus also has rows of strong tubercles. Male dimorphism also occurs, but it is unknown if it is present in all species: a larger, more robust type and a smaller, effeminate type. This type of dimorphism is rare in harvestmen. The differences in the pedipalps are striking, with normal males often having femora twice as thick as those of effeminate males of the same population.

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Distribution: Western USA (Oregon, California, Utah, Arizona, New Mexico, and one dubious record from Texas) and northern Mexico (Baja California). Relationships: The families of Phalangioidea fall into two groups based on spiracle microstructure: the primarily Northern Hemisphere taxa (Protolophidae, Phalangiidae, and Sclerosomatidae) with an entapophysis in the spiracle and the Southern Hemisphere taxa with the spiracles being covered by a grate of spines in most species and lacking an entapophysis. The structures of the pedipalps and penes separate Protolophidae from all other entapophysate families. The simple straight penis and humps/tubercle pairs on the opisthosoma are most similar to those of the members of Sclerosomatinae (Sclerosomatidae). Main references: • Systematics: Banks (1893), Cokendolpher (1985b), Edgar (1990), Crawford (1992), Cokendolpher & Lee (1993). • Natural history: Cokendolpher et al. (1993).

Sclerosomatidae Simon, 1879 Ana Lúcia Tourinho Etymology: Sclerosoma, from Greek sklêros, hard, and sôma, body. Characterization: • Size: From very small and delicate, around 2 mm (body size), such as some Neotropical species of Gagrellinae, to larger, sometimes reaching 10 mm or more, such as Oriental species. • Dorsum: Body oval and usually inflated, flattened in Sclerosomatinae (Figure 11f). Ocularium armed or unarmed with small or/and big granules, apophysis, or spines (Figures 4.11e,f). Carapace includes prosomatic tergites of segments I–V; tergites are fused, but sometimes a partial groove can be detected between tergites IV–V and posterior to the ocularium. Pair of free lateral sclerites beside tergite V (posterior margin of the first piece of the prosomatic scute) is present. Second prosomatic tergite (tergite VI) distinct from carapace. Opisthosomatic tergites (nine tergites of somites VII to XV): first five are fused into a single plate—the dorsal opisthosomal scute, Scutum parvum (Figure 4.11n). Neotropical Gagrellinae, such as Holmbergiana, Parageaya, and Pectenobunus, Asian Gagrellinae, and some Leiobuninae species often have one or more spines or protuberances on the dorsal scute (Figure 4.11g); the Dalquestia (Metopilio group) has seven rows of tubercles (Figure 4.11o). Next two tergites are free; tergites XIV and XV are fused. • Venter: Corona analis usually present, absent in some New World genera of Gagrellinae and in Nepalese Sclerosomatinae. Opisthosomatic sternites (10 sternites of somites VII to XVI). Sternite VII forms an arch fragmented around the genital operculum (originates from the sternites IX to XIV [XIII and XIV

Taxonomy

a

h

b

i

j

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l

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m

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Figure 4.11. Sclerosomatidae. (a–e, n–o) Habitus dorsal: (a) Amilenus aurantiacus (Dicranopalpus group); (b) Gyas titanus (Gyinae); (c) Homalenotus quadridentatus (Sclerosomatinae); (d) Leiobunum oharai (Leiobuninae); (e) Prionostemma farinosum (Gagrellinae); (n) Jussara luteovariata (Gagrellinae); (o) Dalquestia formosa (Metopilio group). (f–g) Lateral: (f) Pygobunus okadai (Sclerosomatinae); (g) Leiobunum japonicum tawanum (Leiobuninae). (h–m) Penis: (h) Gyas annulatus (Gyinae); (i) Amilenus aurantiacus (Dicranopalpus group); (j) Leiobunum tohokuense (Leiobuninae); (k) Dalquestia formosa (Metopilio group); (l) Homalenotus quadridentatus (Sclerosomatinae); (m) Abaetetuba citrina (Gagrellinae). (p) Geaya sp., pseudoarticular nodule of the leg (Gagrellinae).

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• •

•

•

•

•

fused]), includes free lateral pieces—arculi genitales I (anterior pairs of paired free sternites) and II (posterior pair)—and corresponds to the free lateral pieces of sternites X and XI (Hansen & Sørensen, 1904; see also Tourinho & Kury, 2001, for further information on morphology). Chelicerae: Reinforced in Leiobuninae; ventral apophysis of basal segment blunt and inclined distally in (European) Sclerosomatinae. Pedipalps: Slender and elongate; shorter in some soil-dwelling species such as Pseudastrobunus and Granulosoma (Sclerosomatinae) and Systenocentrus japonicus or Paraumbogrella pumilio (Gagrellinae). Tarsus with a short ventrodistal comb of specialized bristles (Sclerosomatinae and Gagrellinae). Claw pectinate. Legs: Generally round in cross section; femora with pseudoarticular nodules in most of the Gagrellinae (also found in some Leiobuninae) (Figure 4.11p). Coxae II showing distal blunt lobes (Gyinae). Coxae often with marginal rows of denticles or humps. Claws smooth. Genitalia: Penis with four regions: shaft (truncus), alate portion with developed winglets (Figure 4.11m), vestigial or completely absent (Figures 4.11h–l) in Sclerosomatinae and in a few species of Oriental Gagrellinae such as Melanopa grandis, reduced in Metopilio group species (Figure 4.11k) and some Neotropical Gagrellinae such as Jussara flamengo (see Tourinho-Davis & Kury, 2003); the left and right winglets are more or less fused to each other along the median line. Lateral border of shaft with pores, slits, and depressions. The beginning of the glans is evidenced by the superior margin of the winglets (Figure 4.11m). The surface of the glans has many pores that delimit the end of the glans area and the beginning of the stylus. Stylus surface is smooth without pores. Color: Variable. The species have all kinds of colors, from light to dark, and metallic-colored patches, stripes, or spots that vary in size and color on dorsal and ventral surfaces are also present. Sexual dimorphism: Present by the different color pattern and/or design. Spots and stripes can be different in male and female, males are generally smaller than females, and the body sclerites (especially the free sclerites) usually are tightly arranged in the males and more separated in the females, therefore much more sharply marked. Adult males bear a ventromesal row (or rows) of denticles on their pedipalpal tarsus. The presence of at least one more nodule in the femora of females is also a secondary dimorphism in Neotropical Gagrellinae species.

Distribution: New World: South America, including the Antilles (Gagrellinae and Leiobuninae); Central and North America (Gagrellinae, Leiobuninae, and Metopilio group); and Old World: Europe, Africa, and Asia (represented by the four subfamilies, Gagrellinae occurring only in Asia). Relationships: Statements on the phylogenetic relationships of the subfamilies included in Sclerosomatidae without a systematic review are purposeless. There is morphological continuity between Asian Gagrellinae/Leiobuninae, Sclerosomatinae/Gagrellinae, and Gyinae/Leiobuninae, as shown by Martens (1973, 1982). It seems that Dicranopalpus and Amilenus do not share a set of similarities with the

Taxonomy

other species included in Gyinae; in these species the penis has the same morphological pattern present in other gagrellines and leiobunines. If their inclusion in Gyinae is considered as suggested by Martens, then Gyinae may be paraphyletic. The presence of nodules on the leg femora separates Gagrellinae species from those of the other three subfamilies, although some species have several nodules on the leg femora. Some leiobunines show nodules in the femora, and even the character “softer dorsal scutum” used to diagnose leiobunines can be found in some species assigned to Gagrellinae, such as Gagrellopsis nodulifera and the Leiobuninae species of the genera Pseudogagrella, and Pseudomelanopa (N. Tsurusaki, pers. comm.). Giribet et al. (2002) used four species of two representatives of Sclerosomatidae (Leiobuninae and Sclerosomatinae) in a cladistic analysis of Opiliones, combining both morphological features and molecular data. The results agreed with Crawford’s classification, with Sclerosomatinae placed within Leiobuninae, therefore rejecting the monophyly of Leiobuninae, and rejected the idea that the Metopilio group (represented by Dalquestia formosa) is part of Sclerosomatidae. It seems that several species of Gagrellinae are misplaced in Leiobuninae, or Gagrellinae and Leiobuninae should be settled together, as Starega (1976a) stated. The clade is still problematic, and the addition of more genera, including species of Gagrellinae, is in need of future analyses. Main references: • Systematics: Roewer (1910, 1923, 1953), Martens (1973, 1978b, 1987), Cokendolpher (1980, 1982, 1984b), Crawford (1992), Tourinho & Kury (2001), Tourinho-Davis (2003), Tourinho-Davis & Kury (2003), TourinhoDavis (2004a,b). • Natural history: Edgar (1971), Cokendolpher (1984b), Tsurusaki (1986, 2003), Coddington et al. (1990), MacKay et al. (1992); Cokendolpher et al. (1993).

DYSPNOI Historical systematic synopsis Jürgen Gruber Dyspnoi was already recognized as a clade of Palpatores (corresponding to the tribe Trogulini [sic] Sørensen, 1873, and the family Nemastomoidae Thorell, 1876, respectively, see below), by Hansen and Sørensen (1904) to include three families, namely, Ischyropsalidoidae [sic] (containing the genera Ischyropsalis, Taracus, Tomicomerus, Sabacon, Parasabacon, and Phlegmacera), Nemastomatoidae [sic], and Troguloidae [sic] containing the subfamilies trogulini [sic] and Dicranolasmatini [sic]. The group, now accepted as monophyletic (see Chapter 3) (dissenting opinions, maintaining in effect a closer relationship of Ischyropsalidoidea to Phalangioidea, were published by Pocock [1902b] and Martens [1980]), includes a modest number of species from the Northern Hemisphere classifed into the two superfamilies Troguloidea and Ischyropsalidoidea.

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Troguloidea, despite the lack of apparent somatic characters supporting it, is well defined through genitalic characters (Martens, 1976) and recovered in modern phylogenetic analyses of morphology and/or molecules (see Chapter 3). Trogulidae species are short-legged, soil-dwelling, and soil-encrusted Dyspnoi distributed in the western Palearctic. Latreille (1802a) established Trogulus for species earlier placed in Phalangium and Acarus. Sundevall (1833) established the family Trogulides [sic], which then also contained the mite Caeculus. Simon (1872b) first used the family name in the form Trogulidae, but he also included the genus Cyphophthalmus in this family. Sørensen (1873) recognized a tribe Trogulini (in the family Opilionides), which included Trogulus and his new genera Anelasma, Dicranolasma, and Amopaum, together with Ischyropsalis and Nemastoma. Thorell (1876b) placed in his family Nemastomoidae [sic] the subfamilies Nemastomini [sic] (Ischyropsalis, Nemastoma, Dicranolasma) and Trogulini [sic] (Trogulus and Anelasma). Simon (1879c) founded the classification followed by the majority of subsequent authors, with the family Trogulidae and subfamilies Dicranolasmatinae and Trogulinae, the latter comprising Trogulus, Anelasmocephalus (nomen nov. for Anelasma), and the newly established genera Calathocratus and Metopoctea, the latter synonymized with Trogulus by Dahl (1903). Pocock (1902b) placed Dicranolasma in a separate family. Roewer published a few papers concerning Trogulidae specifically, disregarding the subfamily classification; later he (Roewer, 1940) added three new genera: Trogulocratus, Platybessobius, and Kofiniotis. Silhavy (1967a) added Anarthrotarsus. Roewer (1923, 1950) and other authors included the North American forms described by Banks (1894) and subsequent workers, placing them in Trogulidae on the basis of superficial similarities. These discordant elements were later transferred to other families (Gruber, 1969b; Martens, 1976, 1978b; Shear & Gruber, 1983), and Dicranolasmatinae was again elevated to family rank (Gruber, 1974). The family as now understood (e.g., Martens, 1976, 1978b) appears homogeneous, comprising two groups of genera that differ in body form, hood form, surface sculpture, tarsal formula, and midgut anatomy (Dumitrescu, 1974b). The family Nemastomidae [sic] was established by Simon (1872b) for the genera Nemastoma and Ischyropsalis. This extended use persisted in Thorell (1876b) (subfamily Nemastomini, including also Dicranolasma). Simon (1879c) restricted the family to the genus Nemastoma, which he divided into two groups according to relative leg length. The family diagnosis used by subsequent authors was formulated by Hansen and Sørensen (1904). Roewer (1914a) followed Hansen and Sørensen in his diagnosis of the family, adding the new genus Crosbycus, and divided the genus into eight species groups (Roewer, 1919). He then presented a revision of the family (Roewer, 1951), beginning the dismemberment of the large genus Nemastoma into a new Nemastoma (with eight species groups), Mitostoma (with four species groups), and Acromitostoma and Crosbycus. Roewer used only a few characters to diagnose his genera, often creating artificial groups. Kratochvíl (1958b), ignoring penis morphology, proposed a reorganization of the family, dividing the group into smaller taxa and naming the subfamilies Nemastomatinae, Mitostomatinae, and Giljarovi-

Taxonomy

inae, comprising nine genera. Silhavy (1966b) explicitly stressed the use of penis morphology in generic taxonomy and found only partial correspondence with Kratochvíl’s groups, which were subsequently dismissed (Gruber, 1976). Gruber and Martens (1968) clarified the question of the type species of Nemastoma. The North American representatives of Nemastomatidae were removed from the family, with the suggestion that they belonged to (or were close to) Ischyropsalididae (Gruber, 1970). On the other hand, the North American (and eastern Asian) Ortholasma and Dendrolasma were shown to have nemastomatid affinities and were placed in the new subfamily Ortholasmatinae (Shear & Gruber, 1983). Kratochvíl’s genera were revised by Starega (1976b), Gruber (1976, 1979), and Martens (1978b), among others. Current understanding of nemastomatid genera remains unsettled; some of Roewer’s and Kratochvíl’s names have been validated by the use of additional characters taken especially from penis morphology, notably by Martens (1978b), but a family clarification is still needed. Some authors therefore have preferred the use of the old name Nemastoma (sensu lato) for species that cannot be placed more precisely (e.g., Prieto, 2004). Dicranolasmatidae is a monogeneric family containing forms of trogulid-like facies distributed in the western Holarctic, mainly the Mediterranean region. Simon (1879c) established the subfamily Dicranolasmatinae within Trogulidae. Pocock (1902b) elevated the group to family rank as Dicranolasmidae [sic], while Hansen and Sørensen (1904) retained the subfamily status as Dicranolasmatini. Subsequently the subfamily distinction was mostly neglected until the mid-1970’s, when the family was revalidated (Dumitrescu, 1974b, 1975a; Gruber, 1974; Martens, 1976, 1978b). The first species of Nipponopsalididae was described from Japan by Sato and Suzuki (1939; see also Suzuki, 1940) as Ischyropsalis abei. Two species from Hokkaido and Korea were subsequently described (Suzuki, 1958, 1966a), and Martens and Suzuki (1966) established the genus Nipponopsalis for these species in Ischyropsalididae. Martens (1976), mainly on the basis of characters of the male genitalia, erected the family Nipponopsalididae. Ischyropsalidoidea is also a monophyletic group (see Chapter 3) and includes the monotypic family Ischyropsalididae and two families of uncertain monophyly, Sabaconidae (with the genera Sabacon and Taracus) and Ceratolasmatidae (with the genera Ceratolasma, Acuclavella, Hesperonemastoma, and Crosbycus). The phylogeny of the group was studied in detail by Shear (1986), who proposed a classification based on a nonnumerical cladistic analysis with the following structure: ((Sabacon, Taracus) (Ischyropsalis ((Acuclavella, Ceratolasma) (Crosbycus, Hesperonemastoma))). Shear includes in the family Ceratolasmatidae the genera Acuclavella, Ceratolasma, Crosbycus, and Hesperonemastoma. However, monophyly of Sabaconidae and especially of Ceratolasmatidae has been challenged in recent molecular analyses (see Chapter 3) that found Taracus to be a sister group to Hesperonemastoma (Giribet et al., 2002). The family Ischyropsalididae sensu Shear (1986) is a monogeneric family confined to Europe, mainly the southwestern region. The first species was described by

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Panzer (1794) as Phalangium hellwigii, but Koch (1839) established the genus Ischyropsalis for it and his new species I. kollari. Subsequently the most important contributions came from Simon (1872b and later publications), who described several species from France and the Iberian Peninsula and (1879c) established the family Ischyropsalidae [sic], comprising also the genera Sabacon and Taracus. However, Simon (1872a) seems also to have originated confusion in the use of the name I. hellwigii (based upon specimens misidentified by Koch), further aggravated in the publications of Roewer, until it was finally cleared up by Martens (1969a). Hansen and Sørensen (1904) reviewed the family on the basis of original material and gave it the delimitation that was followed in the next six decades, commenting on the striking heterogeneity of this family, but advising against splitting it. Roewer (1914a, 1923, 1950) used the concepts of the latter as a foundation for his work and described several new species. Further contributions to the knowledge of morphology and systematics of Ischyropsalis were published by Hadzi (1928, 1942, 1954). Martens (1969a) published a comprehensive revision of the genus Ischyropsalis that answered many questions that had been vexing researchers for years (see also Martens, 1978b). Dresco (1966, 1970) revised mainly western European species, corrected some of Simon’s mistakes, and transferred Sabacon to the new family Sabaconidae. In Shear’s (1986) analysis of Ischyropsalidoidea, he restricts Ischyropsalididae to the genus Ischyropsalis. The family Ceratolasmatidae was established by Shear (1986) to accommodate genera that had been transferred from other families to Ischyropsalidoidea or were newly described. This group was based mainly on characters of body sclerotization, scutum sculpture, and leg surface microsculpture. Monophyly of Ceratolasmatidae is, however, questionable (Giribet et al., 2002; Shultz & Regier, 2001), and it is composed of three possibly monophyletic groups: Ceratolasma + Acuclavella, Hesperonemastoma, and Crosbycus. This scheme is followed here. Ceratolasma tricantha was first placed in Trogulidae and later transferred to Ischyropsalididae (Gruber, 1969b, 1978). The related genus Acuclavella, with four known species, was described by Shear (1986). The first Hesperonemastoma species described was Nemastoma troglodytes (renamed N. packardi by Roewer [1914a] on grounds of homonymy). Gruber (1970) presented evidence that these species did not belong to Nemastomatidae, but show closer relationships to Ischyropsalididae (especially Taracus and Sabacon), and erected the new genus for them. A placement in Ischyropsalididae was doubted by Dumitrescu (1975a, 1980), who suggested a separate family for the genus on the basis of his anatomical studies. Shear (1986) finally established the family Ceratolasmatidae, containing a rather diverse assemblage of genera, among them Hesperonemastoma. The first Crosbycus species to be described was Nemastoma dasycnemum from eastern North America, with some reservations as to its generic position (Crosby, 1911). Roewer (1914a) created the genus Crosbycus for this species, based on the free opisthosomal scutum. This led several European authors, including Roewer (e.g., 1951) himself, to describe as “Crosbycus” juvenile or immature specimens of Old World nemastomatids—as cleared up by Gruber and Martens (1968) and

Taxonomy

Rambla (1968). C. dasycnemus remains the only valid species of the genus. Gruber (1970) excluded Crosbycus definitively from Nemastomatidae, without precise familial placement (“in Ischyropsalididae?”). A possible monotypic family Crosbycidae was suggested by Martens (1976, 1978b). Shear (1986) presented a redescription and a review of our knowledge on this species. Suzuki and Kunita (1972) recorded the first Crosbycus in Japan, and Tsurusaki and Song (1993) in China. The disparity between these three groups does not allow a common characterization, and because of this they will be presented separately in this chapter. The family Sabaconidae, which before was placed in the family Ischyropsalididae, was established by Dresco (1970) as monogeneric for the genus Sabacon, mainly on the basis of the unique external features. Simon (1879a) described Sabacon paradoxus from France in Ischyropsalididae. In the same year Koch (1879) described another species from Siberia, Nemastoma crassipalpis. Further species were reported from North America by Packard (1884) and Weed (1893a), and Pavesi (1899) described the genus Tomicomerus. Hansen and Sørensen (1904) created the genus Parasabacon for Koch’s Siberian species, which, like Phlegmacera, was synonymized with Sabacon by Roewer (1914a), who also synonymized all North American Sabacon species within S. crassipalpis. Dresco’s family at first met with reservations for various reasons (Martens, 1972b; Suzuki, 1974; Shear, 1975b; Gruber, 1978), until Martens (1976) accepted the family and rediagnosed it as a monogeneric taxon, mainly on the basis of penis morphology (Martens, 1978b, 1983). Shear (1986) synonymized Tomicomerus with Sabacon (relationships of the poorly known Tomicomerus were already discussed in Shear [1975b]; it appears somewhat intermediate between Sabacon and Taracus) and included Taracus in an extended family. Hansen and Sørensen (1904) rediagnosed the genus in Ischyropsalididae, followed by Roewer (1914a, 1923, 1950). Shear (1986) presented a new diagnosis for the genus. Biogeographically, Dyspnoi constitutes one of the most conserved higher groups of Opiliones, with most families finding restricted distributions (see Chapter 3), always along temperate regions, with the exception of some ortholasmatines entering the tropics on high mountains in Mexico (Shear & Gruber, 1983) and northern Thailand (Schwendinger & Gruber, 1992). Troguloidea was also found in tropical latitudes during the Cretaceous (Giribet & Dunlop, 2005). Key to the main groups of Dyspnoi Gonzalo Giribet 1. Fused meso-metapeltidium with one or more sensory cones. . . . . . . . . . . . . . . . . . 2 . Without metapeltidial sensory cones. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 2. One metapeltidial sensory cone. . . . . . . . . . . . . . . . . . . . . . . Sabaconidae: Taracus . More than one metapeltidial sensory cone . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 3. Two metapeltidial sensory cones. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 . More than two metapeltidial sensory cones . . . . . . . . . . . . . . . . Ischyropsalididae

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4. Pedipalpal tarsus reflexed on the mesal surface of the tibia (Figures 4.18c,d). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sabaconidae: Sabacon . Pedipalpal tarsus not reflexed on the mesal surface of the tibia. . . . . . . . . . . . . . . . 5 5. With a unique frontal process of ocularium and carapace (Figures 4.12a,b), which hide the short chelicerae and pedipalps . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ceratolasmatidae: Ceratolasma . Without frontal process of ocularium; with erect, acute spine in ocularium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ceratolasmatidae: Acuclavella 6. Elongated chelicerae, longer than body length (Figures 4.17a–d). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nipponopsalididae . Chelicerae much shorter than body length. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 7. Soil crypsis by glandular adhesion of soil particles (in adults). . . . . . . . . . . . . . . . . 8 . Without soil crypsis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 8. Eyes in the middle of hood projections (Figure 4.14a). . . . . . Dicranolasmatidae . Eyes at hood base or on ocularium (Figures 4.19a,b) . . . . . . . . . . . . . . . Trogulidae 9. Pedipalpal tibia and tarsus with plumose setae . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 . Pedipalpal tibia and tarsus without plumose setae, but often with clavate glandular setae (Figures 4.16g,h). . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nemastomatidae 10. Pedipalp extremely thin and elongate (Figure 4.13h). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ceratolasmatidae: Crosbycus . Pedipalp not as thin. . . . . . . . . . . . . . . Ceratolasmatidae: Hesperonemastoma

Ceratolasmatidae Shear, 1986 Jürgen Gruber Ceratolasma + Acuclavella group Etymology: Ceratolasma, from cerato-, horn shaped, from Greek kéras, horn, referring to the processes of ocularium and carapace; the second part of the name derives from names of similar forms such as Ortholasma or Dendrolasma. Characterization: • Size: Harvestmen of medium size, about 4–6 mm body length, with moderately short legs. • Dorsum: Moderately flattened (Ceratolasma males) or distinctly arched (Acuclavella). Well sclerotized or somewhat leathery, sculptured with coarse granules or warts. Prosoma with meso- and metapeltidium demarcated by furrows, the latter with paired paramedian cones. Ocularium on anterior border, with

Taxonomy

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erect or prone median process, in the latter case forming part of a “hood” together with lateral carapace processes, covering chelicerae and pedipalps. Ozopores not visible from above. Opisthosoma with scutum parvum, its areas bearing paired tubercles or cones (Figures 4.12a,b). Venter: Corona analis normally developed. Opisthosomal sternites free, spiracles hidden in furrow behind coxa IV. Genital operculum demarcated by (partly obscured) basal suture. Coxae more or less immovable. Coxapophyses: coxa I with movable (distal) lobe, II with small lobe with seta, III–IV with tiny lobes. Prosomal sternal area with free transverse sternum placed between coxae III. Labium large, well sclerotized (Figure 4.12c). Chelicerae: Normal size; chela dentition with narrow transparent teeth and coarser teeth distally. Basal segment with dorsal glandular area in males and in Ceratolasma tricantha with dorsolateral stridulation field (Figures 4.12d,e). Pedipalps: Short and moderately stout, femur in Ceratolasma tricantha forming part of a stridulatory apparatus. Distal segments of even diameter, without narrowed bases. Hair cover: setae and microtrichia, the latter on tarsus, tibia, and patella; no evident glandular setae, at least in adults. Tarsus with tiny pegshaped claw rudiment (Figure 4.12f). Legs: Moderately short; segments cylindrical. Surface sculpture of femora with small scalelike and partly lobed denticles, subtending short blunt setae, and longer setae in rows; patellae and tibiae similar, microtrichia from apical part of tibiae distad. Tarsi moderately multiarticulate. Genitalia: Penis (Figures 4.12g–h): shaft more or less evenly narrowing apicad, containing one pinnate muscle with short tendon; glans with ventral tongue-shaped plate, with short spinelike setae, stylus in prolongation of glans. Ovipositor (Figure 4.12i) short, unsegmented, and soft; two apical lobes with a few setae around base of lobes, a few setae apically. Color: Acuclavella with sclerotized parts black; Ceratolasma shows a striking pattern with brown and white parts. Sexual dimorphism: Dorsum more arched in females, dorsal sculpture more pronounced in males; chelicerae of males with gland organ in basal segment (Figure 4.12d).

Distribution: Western North America: northern California, Oregon (Ceratolasma, one species), Washington, Idaho (Acuclavella, four species). Relationships: Close to Ischyropsalis according to Gruber (1969b, 1978), Martens (1969a, 1978b), and Dumitrescu (1975a, 1980), on the basis of characters of pedipalps, coxapophyses, prosomal sternal region and labium, ovipositor, and midgut anatomy. Placed in a separate family together with Hesperonemastoma and Crosbycus by Shear (1986), mainly on the basis of sculpture characters. Recent cladistic analyses (Shultz & Regier, 2001; Giribet et al., 2002) support the first alternative.

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Figure 4.12. Ceratolasmatidae. Ceratolasma tricantha, from Gruber (1978): (a) male, habitus dorsal; (b) male, habitus lateral; (c) female, prosomal sternal region and coxapophyses, ventral; (d) male, right chelicera, prolateral; (e) male, right chelicera, chela in frontal; (f) male, right pedipalp, prolateral; (g) penis, ventral; (h) penis, apical part, ventral; (i) ovipositor. Scale bars: figures a–b = 0.4 mm; c, g = 1 mm; d–f, i = 0.5 mm; h = 0.25 mm.

Taxonomy

Main references: • Systematics: Gruber (1978), Shear (1986). • Natural history: Gruber (1978), Shear (1986). Hesperonemastoma group Etymology: Hesperonemastoma, from Greek hespera, west, alluding to the occurrence in the New World, plus name of original genus. Characterization: • Size: body length about 1–2 mm. • Dorsum: “Nemastoma”-like appearance; body surface generally well sclerotized, granulated. Dorsum with scutum magnum, ocularium on anterior border (eyes reduced in troglobites); ozopores not visible from above. Dorsal scutum with varied relief and macrosculpture elements—segmentally ordered low humps in some species, or rows of anvil-shaped tubercles and pairs of pointed spines in others. • Venter: Corona analis typically developed; opisthosomal sternites free, genital operculum comparatively large, delimited by membranous furrow. Prosomal sternal region sclerotized and fused to pedal coxae II–III (Shultz, 1998). Coxae not movable; no regular marginal tubercle rows. Coxapophysis of coxa I with fixed basal lamella and movable distal sclerite; coxa II with small lobe (Shultz, 1998). Labium small. • Chelicerae: comparatively long, of normal shape; chela fingers with (about 20) diaphanous narrow teeth and a subapical coarse dark tooth. Males may have glandular organs in second segment (Figure 4.13c). • Pedipalps: moderately long to elongated, slender. Femur without distinct basal bend, tibiae and tarsi with narrowed bases (“stalked”), slightly inflated (visibly so in stouter pedipalps). Tarsal claw rudimentary, peg shaped. Hair cover of pedipalps: characteristic “plumose” glandular setae, denser especially on tibia and tarsus. Microtrichia only in low number ventroapically on tarsus (Figures 4.13d,e). • Legs: Moderately long; surface of proximal segments (trochanter to patella) with granulation or scales and setae; distal segments with microtrichia cover and setae. Tarsomeres around 10. • Genitalia: Penis (Figure 4.13a): shaft stout, straight or slightly curved ventrad, with two-lobed basis, containing one pinnate muscle with (mostly) short tendon inserting ventrally on base of glans. Shaft cuticle on dorsal side with longitudinal “folds.” Glans broadly conical, with stout spinelike setae. Stylus well differentiated, straight or bent. Ovipositor (Figure 4.13b): short, unsegmented, soft cuticle with fine denticulation; two apical lobes, few setae around distal cleft. Vaginal glands with common duct. • Color: Inconspicuous, generally only brown or black. • Internal anatomy: Dumitrescu (1975a, 1980) found in H. modestum a peculiar arrangement of midgut diverticles: only three pairs, as in Laniatores.

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a

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i h f Figure 4.13. Ceratolasmatidae. Hesperonemastoma spp., from Gruber (1970): (a) H. pallidimaculosum, penis in dorsolateral view; (b) H. modestum, ovipositor; (c) H. pallidimaculosum, male, right chelicera, prolateral; (d) H. modestum, male from USA, right pedipalp, prolateral; (e) H. pallidimaculosum, right pedipalp tarsus, retrolateral. (f–i) Crosbycus dasycnemus (drawings by J. Gruber): (f) penis, ventral (from Japan); (g) ovipositor, with vaginal glands outlined (from Japan); (h) female, right pedipalp, prolateral (from North America); (i) pedipalp tarsus, prolateral (same specimen).

Taxonomy

• Sexual dimorphism: males may show morphological peculiarities and glandular organs on chelicerae (glandular tissue, swellings or dorsal “horns” on second segment) and pedipalps (granulation, glandular tissue, and other features, especially on femora) (Figures 4.13c,d). Distribution: Restricted to North America: an eastern range in the Appalachian region, a western one (or two) in the Rocky Mountain and West Coast regions (Shear, 1986). Relationships: The placement in Ischyropsalidoidea is supported by genital morphology, especially ovipositor structure, and other characters, but the precise relations in this group are still unsettled. Gruber (1970) placed Hesperonemastoma in the already heterogeneous family Ischyropsalididae, leading to a modified family characterization still more diverse than the traditional one. A grouping together with Sabacon, Tomicomerus, and Taracus was suggested in Gruber (1978). Dumitrescu (1975a, 1980) proposed a separate family for the genus. Shear (1986) placed the genus in his heterogeneous family Ceratolasmatidae. Recent molecular and morphology-based cladistic analyses (Shultz & Regier, 2001; Giribet et al., 2002) did not resolve Hesperonemastoma and Ceratolasma as sister groups, but showed closer relations of the former to Taracus. Main references: • Systematics: Gruber (1970), Dumitrescu (1975a, 1980), Martens et al. (1981), Shear (1986). • Natural history: Murphree (1987). Crosbycus group Etymology: Crosbycus, named after Cyrus R. Crosby, American entomologist and arachnologist. Characterization: • Size: Crosbycus dasycnemus is a tiny harvestman—with less than 1 mm body length, one of the smallest—of gracile shape, but with well-sclerotized integument and peculiar surface sculpture, especially of the legs. • Dorsum: Carapace with ocularium on anterior border; ozopores visible on lateral border; metapeltidium “incorporated in carapace,” divided by membrane fold from opisthosomal scutum, which shows evidence of progressive sclerotization in adult stage: primary sclerites (on united areas I–III, distinct areas IV and V) are soldered by secondary sclerotization of membrane parts into a scutum parvum; the primary tergites and the secondarily sclerotized parts remain clearly distinguishable by their sculpture, the former with coarser denticles interspersed among granulation (see Shear, 1986: Figure 38). • Venter: Corona analis with reduced sternal part. Genital operculum large and broad, with distinct basal suture. Sternum and labium not sclerotized.

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Coxapophyses: coxa I with movable sclerite with setae; II with small immovable lobe with two setae; II–IV with proximal parts (“endites” of Shear, 1986: Figure 39) set off from distal portions, the latter with coarser denticles as on body. Chelicerae: Normal shape; chela dentition with about 10 or 11 transparent and 1 dark tooth on each finger. Pedipalps: Long and very thin, sparsely set with “plumose” glandular setae; tarsal claw lacking totally (Figures 4.13h,i). Legs: Moderately long, thin, with peculiar surface sculpture: femora, also patellae and tibiae, with dense cover of setae, spikes, and nonarticulated curly hairs (trichomes); the bent ends of the latter produce a “secondary surface” that gives the segment a spindle-shaped outline; distal segments with setae and microtrichia. Tarsi thin, with few tarsomeres. Genitalia: Ovipositor short, unsegmented, and unsclerotized, two distal lobes with few setae, two massive vaginal glands with common ducts, no receptacula seminis (Figure 4.13g). Penis (Figure 4.13f) relatively large, of simple form with one intrinsic muscle and several thicker setae on symmetrical glans. Color: sclerotized parts black or brown, membranes whitish. Sexual dimorphism: The few known males are smaller than the females; genital operculum longer, with slightly triangular shape of anterior border in males (in females broadly rounded). Otherwise not notably distinct—chelicerae (and pedipalps) of males show no (“epigamic”) glandular organs.

Relationships: Crosbycus can be placed in the Ischyropsalidoidea on the basis of several characters (e.g., genital morphology, especially of ovipositor; glandular hairs of pedipalps). Several interesting anatomical traits are still unknown (midgut anatomy, finer internal structures of ovipositor). Molecular data are also lacking. It has been placed alongside Hesperonemastoma (by Shear, 1986), with which it shows certain superficial similarities. Peculiar characters such as the morphology of dorsum and coxae, sculpture of legs, and thin pedipalps with total reduction of claw place the genus in an isolated position; establishment of a separate family, as suggested by some authors, will have to wait for a proper phylogenetic analysis. Distribution: Eastern North America to Eastern Asia. Main references: • Systematics: Crosby (1911), Shear (1986). • Natural history: Shear (1986).

Dicranolasmatidae Simon, 1879 Jürgen Gruber Etymology: Dicranolasma, from Greek dikranos, two-headed, two-pronged, and elasma, a (metal) plate (referring to the “hood”).

Taxonomy

Characterization: • Size: Body length between 3 and 6.4 mm. • General: Sclerotized parts of integument tough-leathery to hard, set with elongated papillae bearing terminal setae, and small globular papillae; encrusted with soil articles, except apical parts of leg metatarsi (calcanei) and tarsi, chelicerae, pedipalps, and other mouthparts, and small areas of body surface. • Dorsum: Body moderately flattened dorsally, anterior end with large headlike “hood” consisting of two curved processes, the eyes in the middle of their length (Figure 4.14a). Laminae suprachelicerales typically developed, hidden under hood. Ozopores hidden. Dorsum covered by scutum magnum; opisthosoma broader than prosoma, especially in females. Free tergite VI visible from above. • Venter: Corona analis complete; opisthosomal sternites free and entire; genital operculum maximally twice as broad as long, with basal suture also in males. Prosomal sternal area fused to coxae. Leg coxae immovably fused, without rows of marginal tubercles. • Chelicerae: About half the body length, hidden under hood in adults; chela with narrow diaphanous teeth. • Pedipalps (Figure 4.14b, c): Short and weak in adults, about half the body length, hidden under hood, with simple setae, without claw. • Legs: Legs short (from about body length, leg I in some species, up to three times body length); femora to tibiae I and III–IV incrassate, thinner and cylindrical in leg II; metatarsi thin, with short calcanei, metatarsus IV long; tarsi thin, with few tarsomeres (mostly around 5 to 6; 3 to 18 on leg II). • Genitalia: Penis (Figure 4.14e) long (about half the body length); shaft moderately stout, mostly tapering evenly distad, without basal “bulb,” containing two muscles with short tendons. Glans slightly asymmetrical, with short spinelike setae, short stylus of variable shape. Ovipositor (Figure 4.14d) short, corpus unsegmented, surface set with setae on low sockets, furca with two segments; receptacula seminis: on each side one, two, or three, in one species multiple sacs. • Color: Sclerotized parts brown to black, body surface largely covered by adhering soil particles. • Sexual dimorphism: Other than in measurements and proportions, differences are shown in shape of genital operculum (narrower and longer in males) and in tarsomere number on legs I–II in most species (higher in males); in most species there are glands in “apophyses” on the basal segment of the male chelicerae, in one species group also glandular areas on the male pedipalp. • Immature forms: Deviate significantly from adults: different integument structure with simpler sculpture, often lesser incrustation; hood develops gradually; the relatively longer and stronger pedipalp (Figure 4.14c) with spines on proximal segments and glandular clavate setae on distal segments are carried outside the still-undeveloped hood.

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Figure 4.14. Dicranolasmatidae. (a) Dicranolasma hirtum, male, dorsal (integument sculpture partially simplified); (b) D. pauper, adult male, right pedipalp, prolateral; (c) D. hirtum, subadult, right pedipalp, prolateral (setation of tibia and tarsus omitted); (d) D. cristatum, ovipositor (receptacula seminis indicated); (e) D. cristatum, penis, dorsal (cuticular surface structure partially indicated in distal part). Scale bars: a = 2 mm; b–e = 0.5 mm.

Distribution: Western Palearctic, mainly Mediterranean region northward to the southern Alps, Carpathians, eastward to the Caucasus and Iraq, the Levant, and southward to western North Africa. Relationships: Dicranolasmatidae is closely related to Trogulidae and Nemastomatidae. Relationships were interpreted differently according to the characters envi-

Taxonomy

sioned: near—or part of—Trogulidae (Koch, 1867; Simon, 1879c; Hansen & Sørensen, 1904; Roewer, 1923; and most authors following him), or closer to Nemastomatidae (Thorell, 1876b; as an independent family closer to Nemastomatidae: Pocock, 1902b; Gruber, 1974; Dumitrescu, 1975a; Martens, 1978b; Shear & Gruber, 1983; Kury, 2002). The first arrangement is mainly based on integument sculpture, including “soil crypsis,” leg metatarsi with calcanei, paired hood (i.e., “facies characters”), and penis shape with long muscles (the latter a plesiomorphic character); the second is based on “general body architecture” with free opisthosomal sternites, shape of genital operculum, midgut structure, and pedipalp characters (shape of femur, “nipplelike” claw rudiment, and clavate hairs, at least in juveniles). The characters common to Dicranolasma and nemastomatids are mostly symplesiomorphies; some allegedly synapomorphic characters proving monophyly of Nemastomatidae + Dicranolasmatidae (Martens, 1978b: clavate hairs of pedipalps; Shear & Gruber, 1983: penis muscles with long tendons) are either symplesiomorphies (clavate hairs also in the outgroup Nipponopsalididae) or erroneous (tendons are short in Dicranolasma). One recent phylogenetic analysis based on morphological and molecular data (Giribet et al., 2002) clearly supports Trogulus as sister to Dicranolasma. Shultz and Regier (2001), however, state that relationships within Troguloidea were ambiguous in one of their analyses. Main references: • Systematics: Martens (1978b), Gruber (1998). • Natural history: Weiss (1975), Gruber (1993, 1996).

Ischyropsalididae Simon, 1879 Jürgen Gruber Etymology: Ischyropsalis, from Greek ischyros (strong) and psalis (shears), in reference to the large chelicerae (C. L. Koch, 1839). Characterization: • Size: Body length between 3.8 and 8.5 mm. • General: Rather large harvestmen with strongly elongated chelicerae and moderately long legs (Figure 4.15a), with tendency to reduction of body sclerotization; body integument (sclerites) variously granulated, sometimes tuberculated (Ischyropsalis nodifera), never strongly sculptured or habitually encrusted with soil. • Dorsum: Carapace with median infolded extension between chelicerae, emarginated above chelicera insertions; no distinct laminae suprachelicerales; lateral sclerotized margin (pièces épimériennes of Simon) separated from main part of carapace by a membrane and continuous with the latter only on the anterior end, bearing the dorsally visible ozopores. Carapace more or less strongly domed by origin of cheliceral muscles behind eye tubercle, with U-shaped furrow behind. Ocularium somewhat removed from anterior border (Figure 4.15b), broad and deeply furrowed to nearly bipartite (sometimes reduced in

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Figure 4.15. Ischyropsalididae. (a) Ischyropsalis luteipes, from Simon (1879a); (b) I. manicata, prosoma in lateral, modified from Martens (1969a); (c) I. hadzii, male, dorsum (flattened), modified from Hadˇzi (1942); (d) I. ravasinii, male, right chelicera, prolateral; (e) I. ravasinii, male, right pedipalp, prolateral (in outline); (f) I. manicata, penis, lateral; (g) I. hellwigii, penis, ventral; (h) glans penis, ventral (stylus not shown); (i) ovipositor, dorsal. Scale bars: d–e; eq 4 mm; f–g, i = 1 mm; h = 0.3 mm.

troglobites). Posterior rim of prosoma set off by furrow, bearing two to (mostly) multiple cones. Dorsum of opisthosoma with scutum parvum (comprising areas I–V) or with dissolution stages (scutum intermedium or laminatum), especially in females and troglobites (Figures 4.15a,c). • Venter: Corona analis somewhat reduced, sternal part lacking. Sternites free, spiracles visible, genital operculum rather small, with basal suture in males and females. Prosomal sternal region with free sternum and large labium. Leg coxae without marginal tubercle rows, more or less united in mechanical unit.

Taxonomy

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Coxapophysis I with two sclerites; II with small conical lobes; III–IV with very small immovable lobes. Chelicerae: Longer than body (about one and a half to nearly two times the body length), robust to gracile according to species, generally armed with tubercles and spines; second segment more or less spindle shaped with basal “stalk,” fingers of chela with coarse dark teeth near base and slender transparent teeth in subdistal part (Figures 4.15a,d). Pedipalps: Elongated, but slender, distal segments not with narrowed bases, surface with setae and microtrichia, without glandular hairs; claw reduced to straight peg (Figure 4.15e). Legs: Moderately long, slender; femora without larger sculpture elements, only with setae and microtrichia. Genitalia: Penis: shaft straight, moderately stout, slightly widened basally, one intrinsic muscle in about basal half of shaft, with rather long tendon inserting ventrally on glans base; glans symmetrical, its dorsal face continuous with shaft sclerotization, distinct from ventral plate, numerous (short or long) setae in dorsal and ventral groups, stylus thin, bent against glans (Figures 4.15f–h). Ovipositor short and broad, unsegmented, rims of apical opening with dense seam of fine curved trichomes, an apical group of setae on each side of opening, dorsal surface with a larger number of setae in apical part, only a few ventrally; receptacula seminis tube shaped, multiple (mostly about 4 to 5, up to 10, on each side) (Figure 4.15i). Color: Plain and sclerotized parts black or brown, membranes pale or with blackish violet pigmentation. Sexual dimorphism: Males with more extensive sclerotization (e.g., scutum parvum versus scutum laminatum in female), body of females less sclerotized than that of males. Basal segment of male chelicerae often with distal glandular organs, swellings, and hair fields (poorly developed in I. kollari and related forms, seemingly reduced in some troglobites). Chelicerae of males in some species slender, with reduced sculpture (spines or tubercles). Patellae of male pedipalps with small laterodistal apophyses in some species.

Distribution: Restricted to Europe: northern part of Iberian Peninsula (northern Portugal to Cantabrian Mountains), Pyrenees, the Massif Central in France, the Alpine Chain to Slovenia, central Europe (mainly the mountainous regions) east of the Rhine (reaching the Netherlands and northwestern Germany in the north, central Poland in the east), the Carpathian Mountains, Dinaric Mountains to Bosnia and Herzegovina (see Novak et al., 1985, for discussion of spurious records in this region, still found in Rambla & Juberthie, 1994), and the Apennine Peninsula to Calabria, with a doubtful record from Sardinia (Chemini, 1995). Relationships: Ischyropsalis and the monotypic family based on it belong in the relatively loosely circumscribed superfamily Ischyropsalidoidea. The cladistic analysis of Shear (1986) showed Ischyropsalis as a sister group to Ceratolasmatidae, but characters suggested by Martens (1969a, 1978b) and Gruber (1978) as supporting

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a closer relationship between Ischyropsalis and Ceratolasma (alone) were in part interpreted as plesiomorphies (e.g., form of sternum and endites, simple penis); but other supporting characters, such as structure of pedipalps (where independent loss of plumose setae occurred twice in the hypothesis) and ovipositor, or midgut anatomy (Dumitrescu, 1975a, 1980), were disregarded. In the combined morphological and molecular analysis of Giribet et al. (2002) and in the molecular analysis of Shultz and Regier (2001) Ischyropsalis is sister to Ceratolasma, but not to Hesperonemastoma. So the earlier hypothesis that Ceratolasma and Acuclavella from western North America are the closest relations of Ischyropsalis is still tenable. Taracus with its likewise elongated chelicerae and similar chelae dentition is not closely related. Main references: • Systematics: Dresco (1966), Martens (1969a, 1978b), Martens et al. (1981), Prieto (1990a,b), Luque (1991). • Natural history: Juberthie (1961a, 1965, 1974), Martens (1969a,c, 1975a,b, 1978b).

Nemastomatidae Simon, 1872 Jürgen Gruber Etymology: Nemastoma, from Greek nema (thread) and stoma (mouth), in allusion to the thin pedipalps. Characterization: • Size: Body length between 1.2 and 5.6 mm. • Dorsum: Flattened to strongly arched. With scutum magnum (Figures 4.16a–c) or scutum parvum with tendency to fusion (Ortholasmatinae, Figure 4.16d). In some species a scutum compositum develops by secondary sclerotization of membranes posterior and lateral of the primary scutum (in the adult stage) to include also at least one of the free tergites. Ocularium near anterior border of scutum, in some forms with processes, elaborated into a hood (Ortholasmatinae, Figure 4.16d) or divided into two columns; reduced in troglobites. Three laminae suprachelicerales generally well developed and delimited from carapace. Ozopores not freely visible. Scutum finely or coarsely granulated, variously sculptured or armed with macrosculptural elements—nearly flat, with low segmental humps on areas (Figure 4.16c), with cone-shaped tubercles (Figure 4.16a), with low or high pegs or spines, in some groups with rows or a network of connected anvil-shaped tubercles (Figures 4.16b,d). • Venter: Corona analis well developed, as are free sternites; anterior sternite narrowed to base of genital operculum. Genital operculum with well-developed basal suture in females, without it in males. Spiracles not visible. Prosomal sternal area fused with coxae. Leg coxae well delimited but immovable, with marginal rows of tubercles, often anvil shaped (Figure 4.16c).

Taxonomy

a

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Figure 4.16. Nemastomatidae. Nemastomatinae, males, habitus: (a) Paranemastoma superbum, dorsal; (b) Mitostoma gracile, dorsal (body length about 1.5 mm); (c) Nemastoma bidentatum sparsum, lateral. (d): Ortholasmatinae: Dendrolasma mirabile, male, habitus dorsal (body length about 2.9 mm); (e) Ortholasma rugosum, right chelicera of male, prolateral view; (f) same for Giljarovia turcica. (g–h): Right pedipalps of males, prolateral view: (g) O. rugosum; (h) G. turcica, showing stridulatory area. Penes: (i) Mitostoma gracile; (j) Nemastoma triste; (k) “Pyza” taurica; (l) Paranemastoma superbum, glans penis, ventral; (m) Dendrolasma mirabile; (n) D. mirabile, ovipositor. Scale bars: e–h, k, m–n = 0.5 mm. Sources: a–c, i–j, l, from Martens (in press); d–e, g, i, m, n, from Shear and Gruber (1983); f, h from Gruber (1976); k from Gruber (1979).

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• Chelicerae: Normal proportions, often sexually dimorphic; dentition of chela with narrow, diaphanous teeth (Figures 4.16e,f). • Pedipalps: Length and girth variable, from short and stout ones to strongly elongate and gracile ones (Figures 4.16a,b). Femora with “basal bend.” Tibiae and tarsi with narrowed bases and somewhat inflated, less markedly so in elongated, thin pedipalp. Tarsal claw absent, but with “nipplelike” rudiment. With clavate glandular setae especially on distal segments, sometimes reduced in adults (Figures 4.16g,h). • Legs: Generally moderately short to long, segments of various shapes—femora to tibiae may be incrassate or thin, distal segments generally thin. Femora often with pseudoarticulations. Surface of proximal segments with various microsculptural elements; metatarsi without calcanei. Tarsi moderately pluriarticulated. • Genitalia: Penis (Figures 4.16i–m) long, shaft with incrassate bulb-shaped base (its walls often cleaved medially) containing the two intrinsic penis muscles, their tendons therefore long. Shaft varying in shape from stout with extended bulbous base (Figure 4.16i) to slender and straight with relatively shorter basal portion (Figure 4.16k) or extremely slender and elongate with basal bulb sharply set off and bent against main portion of shaft (Figure 4.16j). The shaft may bear lateral wings below the glans in certain groups (Figure 4.16k). Glans variously shaped—symmetrical (Figure 4.16k) or more or less asymmetrical (Figure 4.16l), with mostly short stylus (exceptions especially in Ortholasmatinae, Figure 4.16m) and variable setation. Ovipositor unsegmented, truncus soft skinned, short to very short, with nonglandular setae, apical portion (furca) with two weakly delimited segments, sometimes slightly sclerotized (Figure 4.16n). • Color: Mostly pale brown to black, sometimes patterning with paler or darker parts; a common and striking pattern in several genera consists of silvery white (nacreous) or golden spots on a generally black dorsum (Figure 4.16a). • Sexual dimorphism: Apart from size and proportions, males may show a more prominent dorsal armature with cones or spines, and generally a different shape of genital operculum (longer and narrower, without basal suture). Male chelicerae in most species with glandular organs opening on the basal segment, often associated with dorsal apophyses; toothlike apophyses sometimes also on second segment (Mitostoma, ortholasmatines). Pedipalps of males may bear distal apophyses on patellae; glandular areas on femur, tibia, and especially patella may occur in ortholasmatines. Key to subfamilies 1. Ocularium with median process extending anteriorly and forming a hood together with lateral carapace processes (Figure 4.16d). . . . . . . . Ortholasmatinae 2. Ocularium without median process extending anteriorly or forming a hood (Figures 4.16a–c; a median erect spine or a bipartite ocularium may occur). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nemastomatinae

Taxonomy

Distribution: The family shows a disjunct Holarctic distribution: Nemastomatinae are a western Palearctic group, occurring in nearly all of Europe, in the north to Scandinavia and Iceland, in the east to the Urals and the Caucasus; in North Africa in the northern part of the Atlas region; in southwestern Asia from Anatolia and the Levant to Caucasia and northern Iran, with outliers in the Pamirs, the Tien Shan, and the northwestern Himalayas (J. Martens, pers. comm.). Most species are restricted to rather small areas in the mountains of the southern part of the whole area; only a few species extend to the far north and northeast. One western European species has been introduced into eastern North America. Ortholasmatinae is an Amphipacific group—western North America (Mexico, California, Oregon, Washington, British Columbia) and eastern Asia (southern Japan and northern Thailand). Relationships: Nemastomatidae represent the largest and most diverse group of troguloids. Interfamilial relationships in this superfamily are still somewhat controversial (see discussion under Dicranolasmatidae). Nemastomatidae and Dicranolasmatidae show several (but mainly probably symplesiomorphic) similarities (Ortholasmatinae show convergent similarity to the latter); some allegedly synapomorphic characters proving monophyly of Nemastomatidae + Dicranolasmatidae (Martens, 1978b: clavate hairs of pedipalps; Shear & Gruber, 1983: penis muscles with long tendons) are either symplesiomorphies (also in Nipponopsalididae) or erroneous (short tendons in Dicranolasma). A recent phylogenetic analysis (Giribet et al., 2002) supported monophyly of Nemastomatidae as a sister to Dicranolasma and Trogulus. Main references: • Systematics: Gruber & Martens (1968), Gruber (1976, 1979), Martens (1978b), Rambla (1980a, 1983), Shear & Gruber (1983), Starega (1986), Schwendinger & Gruber (1992), Prieto (2004). • Natural history: Immel (1954), Juberthie (1964), Starega (1986), Thaler & Knoflach (2001).

Nipponopsalididae Martens, 1976 Jürgen Gruber Etymology: Nipponopsalis, combination of Nippon (Japan) with the ending of Ischyropsalis. Characterization: • Size: Body length between 2.3 and 4.1 mm. • Dorsum: Integument generally poorly sclerotized, with limits of sclerites sometimes indistinct. Carapace domed with large low ocularium, eyes rather large, no laminae suprachelicerales (pièces épimériennes), anterior border with median infolding and slight emarginations above chelicerae; ozopores very small, visible on carapace border. Mesopeltidium fused to carapace, metapeltidium free. Opisthosoma with scutum parvum in males (with some tendency to

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Figure 4.17. Nipponopsalididae. (a) Dorsal of Nipponopsalis abei, male; (b) same, female; (c) dorsal of N. yezoensis, male; (d) dorsal of N. coreana, male. (e–f) Penis of N. abei: (e) lateral view, (f) ventral view. (g) N. abei, ovipositor. Sources: a–b, Suzuki (1940); c, Suzuki (1958); d, Suzuki (1966a); e–g, Suzuki (1986).

thinning or dissolution) and scutum laminatum to dissectum in females. Free tergites VI–VII visible from above (Figures 4.17a–d). • Venter: Corona analis incomplete; lateral parts of tergite IX and anal operculum large. Opisthosomal sternites free, poorly or not sclerotized; genital operculum also soft with indistinct basal delimitation; spiracles hidden in furrow behind coxae IV. Prosomal sternal area fused to coxae. Labium small. Coxae poorly sclerotized, rounded, without marginal rows of tubercles. • Chelicerae: Elongated (longer than body) and strong, well sclerotized and with species-characteristic and partly sexually dimorphic sculpture (Figures

Taxonomy

•

•

•

•

•

4.17a–d); chela fingers with narrow diaphanous teeth in middle and coarser dark teeth in distal portion. Pedipalps: Slender and very long (much longer than body) (Figure 4.17c), with sparse simple setae in adults (in juveniles with clavate setae on tibia and tarsus); tarsus without claw. Legs: Long, gracile, femora with pseudoarticulations; femora (in N. abei) with setae, dispersed small dark denticles and dense granulation, distal segments with setae, microtrichia beginning on apex of tibia. Genitalia: Penis (Figures 4.17e,f); sheath with sclerotized stiffening rods, long, about three-quarters of body length; shaft moderately slender, generally tapering uniformly from base, containing two long muscles with short tendons; glans three-branched with lateral plates set with setae shielding the median part with opening of seminal duct. Ovipositor (Figure 4.17g) with unsclerotized, unsegmented corpus, covered with bristles on low sockets, denser toward apex; furca bisegmented, its thin sclerites with longer setae. Receptacula seminis: two small oval sacs in the distal part of the corpus. Color: Generally inconspicuous; sclerotized parts brown to black, darker in chelicerae; membranous parts partially with hypodermal pigment; also body with paler spots, legs with white rings. Sexual dimorphism: Females larger than males. Males generally with scutum parvum, females with scutum laminatum/dissectum (Figures 4.17a,b). Chelicera in males somewhat stouter, with different armature, for example, in N. abei (apophyses interlock; Figures 4.17a,b); no secretory organs in males (in the case of N. coreana, Figure 4.17d, still doubtful). Pedipalps in males of N. yezoensis with thickened, spindle-shaped tibia and tarsus possibly containing glandular tissue (Figure 4.17c).

Distribution: Limited to eastern Asia: Japanese islands from Hokkaido (N. yezoensis) and the main islands (N. abei) southward to Ryukyu Islands (N. abei longipes); also on Kuril Islands (N. yezoensis) and Korean Peninsula (N. coreana). A supposed occurrence in the far east of Russia (Tchemeris, 2000) was based on a misidentification. Relationships: The placement of Nipponopsalididae within the superfamily Troguloidea is supported by genital morphology, presence of pedipalpal clavate setae in juveniles, and sternal conformation. The position of the ozopores and the lack of distinct laminae suprachelicerales deviate from the usual conditions in this superfamily. Two recent phylogenetic analyses (Shultz & Regier, 2001; Giribet et al., 2002) resolved Nipponopsalis as the sister group to the other troguloids. The overall similarity to Ischyropsalis is a case of convergence. Main references: • Systematics: Martens & Suzuki (1966). • Natural history: Miyosi (1942).

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Sabaconidae Dresco, 1970 Jürgen Gruber Etymology: Sabacon derives from the name of an Egyptian king (Gruber, 2003). Characterization: Primarily based upon Sabacon, with additions on Taracus in parentheses. • Size: Body length in Sabacon between 1.2 and 5.4 mm (between 2 and 5.5 mm in Taracus, the lower value perhaps based on nymphs). • General: Integument of body mostly poorly sclerotized; body sclerites with “diffuse” limits, if present at all on opisthosoma (similar or even less sclerotized in Taracus). • Dorsun (Figures 4.18a,b): Carapace often poorly delimited laterally. Ocularium near anterior border, the latter with median notch leading to sclerite extending to epistome, no distinct laminae suprachelicerales; ozopores visible. Metapeltidium free, often poorly or not sclerotized, with median pair of sensory cones. Opisthosomal dorsum with scutum parvum, laminatum, or dissectum or with total lack of continuous sclerotization. (Taracus, Figure 4.18k: Ocularium set far back from frontal margin, unfurrowed; carapace with median elevation, origins of cheliceral muscles on either side of ocularium; one median cone behind eye tubercle. Opisthosomal dorsum poorly sclerotized, maximal development a scutum laminatum.) • Venter: Sternites and genital operculum poorly sclerotized; prosomal sternal region scarcely sclerotic at all, seemingly variable between species, with or without elevated setae groups. Coxapophyses in Sabacon lacking on coxa II (small lobes present in Tomicomerus). (Taracus: Sternum reduced to two small plates with single setae; coxa II with small lobe.) • Chelicerae (Figures 4.18e,f): Relatively small, sexually dimorphic; chela with characteristic dentition of narrow transparent teeth. (Taracus: Chelicerae strongly elongated, as in Ischyropsalis, but segments of more cylindrical shape, second segment not stalked; chela dentition with coarse teeth in basal third, Figure 4.18k.) • Pedipalps (Figures 4.18c,d): Highly characteristic—often somewhat longer than body, relatively stout; tibia and tarsus more or less strongly inflated, stalked, with dense brushlike cover of glandular (plumose) setae, tarsus folded back against medial side of tibia, fitting into a hairless area; a very small claw rudiment is present in some species. Microtrichia occur in some species on pedipalp patella. (Taracus: Pedipalps strongly elongated, rather slender; tibia and tarsus cylindrical, with dense “bottlebrush” setation of glandular hairs, tarsus bent under tibia, Figure 4.18k.) • Legs: Moderately long, variable, femora in some species with pseudoarticulations, surface smooth or with low sculpture, and setae. • Genitalia: Penis of Sabacon (Figures 4.18g,i): Characteristic and highly derived (Martens, 1983); shaft more or less slender and flattened dorsoventrally, basal

Taxonomy

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Figure 4.18. Sabaconidae. (a–d): Sabacon paradoxus: (a) male, habitus dorsal; (b) female, habitus dorsal; (c) male, right pedipalp, prolateral; (d) female, right pedipalp, prolateral. (e–h) S. crassipalpis: (e) male, right chelicera, prolateral; (f) female, right chelicera, prolateral; (g) penis, dorsal; (h) ovipositor. (i) S. dentipalpis, ovipositor. (j) S. imamurai, apical part of penis, lateral. (k–m) Taracus birsteini: (k) male habitus, lateral; (l) glans penis; (m) ovipositor. Scale bars: a–d = 2 mm; e–g = 0.5 mm; i = 1 mm; j = 0.2 mm; k = 5 mm. Sources: a–e, Martens (1983); f–i, Martens (1989); j, Suzuki (1974); k–m, Tchemeris (2000).

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portion sharply bent dorsad against main portion, with walls reduced to lateral fork, the one muscle concentrated here, with long tendon. Glans with variously developed setation, stylus rather long, of variable form. Ovipositor (Figures 4.18h,i) unsegmented, soft skinned, only the distal “lips” at most very slightly sclerotized, with longer setae; shape of ovipositor conspicuously variable in the genus, from “stumpy” types, hardly longer than broad, their corpus without or with few setae, to “elongate” types with dense setation over surface of corpus. For internal anatomy, see Martens et al. (1981). (Taracus: Penis, Figure 4.18l: straight, shaft rather stout, muscle in shaft, not concentrated basally, glans conical with numerous short setae; ovipositor: see Figure 4.18m.) • Color: Various tones of brown in sclerotized parts, otherwise blackish purplish pigmentation, ventral side often paler. • Sexual dimorphism: Body sclerotization, especially opisthosomal scutum, is generally better developed in males, which possess a scutum parvum in some species; pedipalps (Figures 4.18c,d) are more slender in males; the patella bears medioventral teeth distally in several species. Chelicerae (Figures 4.18e,f): basal segment with gland organs in males, often on more or less conspicuous apophyses; sometimes the second segment is also modified. (Taracus: Males without glandular organs in chelicerae; pedipalp patella with teeth.) Distribution: Disjunctly Holarctic: southwestern Europe (northern Iberian Peninsula and Pyrenees, southern France including parts of Massif Central, southwestern Alps and northern Apennines in Italy), with an isolated occurrence in southern Wales; Asia: Himalayan region (Nepal, Sikkim, Bhutan), central Asia and Siberia, eastern Asia (China [Liaoning, Sichuan, also Shaanxi and Gansu, Martens, pers. comm.], Korean Peninsula, Japanese islands to southern Kuril Islands); North America: western USA from California northward, British Columbia to southern Alaska; eastern (and central) USA to southern Canada. (Taracus: Western North America and eastern Siberia; Shear, 1986.) Relationships: Sabaconidae is clearly monophyletic (autapomorphies in penis and pedipalp structure). Tomicomerus (synonymized with Sabacon by Shear, 1986) differs in details (penis, coxapophyses). The placement of Taracus is questionable (it differs especially in “more plesiomorphic” penis, median mesopeltidial sensory cone, less specialized pedipalps, and strongly elongated chelicerae). Hesperonemastoma may be closely related, with a similar pedipalp setation, but differs in scutum development and in its unique midgut anatomy. Recent cladistic analyses (Shultz & Regier, 2001; Giribet et al., 2002) refute “Sabaconidae” as conceived by Shear (1986). Main references: • Systematics: Martens (1972b, 1978b, 1983, 1989), Suzuki (1974), Shear (1975b, 1986), Juberthie et al. (1981a,b).

Taxonomy

• Natural history: Juberthie (1965); Martens (1972b, 1983); Lopez et al. (1978); Tsurusaki (2003).

Trogulidae Sundevall, 1833 Jürgen Gruber Etymology: Trogulus, somewhat obscure; Latreille (1804) said under “Trogule: trogulus”: “Par ce mot on a désigné un coqueluchon” (a monk’s hood), a somewhat enigmatic statement. Perrier (1929) derives the name from Greek trogein, gnawing, in allusion to the rough, “gnawed-upon” appearance. Characterization: • Size: Body length between 2 and 22 mm. • General: Cuticle well sclerotized, tough-leathery, with papillate-glandular sculpture and soil incrustation, only small parts of body surface, leg tarsi and calcanei, and mouthparts excepted. • Dorsum: Body more (Trogulus, Figure 4.19a) or less (Anelasmocephalus: “drop shaped”) flattened; body shape characteristically elongate-oval, with long and broader opisthosomal part and narrower prosoma (Figures 4.19a,b). Dorsum with scutum magnum, segment boundaries sometimes visible, especially between prosoma and opisthosoma; free tergite VI forms posterior end. Ocularium on anterior border. Paired processes more (e.g., Trogulus) or less (e.g., Anelasmocephalus) elongated, form together with long papillae, which in part bear terminal setae (“spines”), a small hood, which hides chelicerae and pedipalps from dorsal view (Figures 4.19a,b). Laminae suprachelicerales hidden under hood; ozopores not freely visible from above. • Venter (Figure 4.19c): Corona analis well developed. Opisthosoma with ventral scutum, sternites fused but still well delimited, divided by median suture; a pleural furrow between dorsal and ventral scuta allows distension of opisthosoma. Genital operculum short and broad, delimited by basal suture. Spiracles not freely visible. Prosomal sternal area fused with coxae. Leg coxae fused, immovable, without distinct marginal tubercle rows; coxa I distinctly curved anteriad, forming lateral borders of the “camerostome” containing the anterior appendages (Figure 4.19c). • Chelicerae: Short (less than half of body length) and comparatively slender, hidden under hood; chela with narrow diaphanous teeth (Figure 4.19d). • Pedipalps: Very short (less than one-fourth of body length) and weak, but compact, distal segments not with narrowed bases, of limited mobility; with few setae, no glandular setae; claw lacking totally (Figure 4.19e). • Legs: Short (from less than body length, e.g., leg I, to about one and a half body lengths, leg II, according to species) and stout, segments with exception of a short distal portion of metatarsus (calcaneus) and tarsus (covered with microtrichia) bearing papillae like body surface, soil-encrusted. Tarsomere number low, from one to six.

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Figure 4.19. Trogulidae. (a) Anelasmocephalus cambridgei, habitus dorsal (without incrustations) (drawing by H. Bürgis); (b) Trogulus tricarinatus, anterior part of body, dorsal without incrustations (from Komposch, 2000b). (c) A. cambridgei, body in ventral view (drawing by H. Bürgis); (d) Calathocratus beieri, male, right chelicera in prolateral view; (e) C. beieri, male, left pedipalp in prolateral view; (f) C. beieri, penis, dorsal; (g) apical part, ventral; (h) C. beieri, ovipositor. Figures d–h from Gruber (1968). Scale bars: a–c = 1 mm; d–f = 0.5 mm; g–h = 0.1 mm.

Taxonomy

• Genitalia: Penis (Figures 4.19f,g) relatively short (about one-fourth to onethird of body length, maximally less than half), shaft stout, in general evenly narrowing from base, containing two muscles with short tendons. Glans simple, more or less asymmetrical, slightly movable; stylus not clearly distinct from glans. Ovipositor (Figure 4.19h) moderately short, corpus unsegmented, covered with setae elevated on conical protuberances containing gland sacs, furca with two segments. • Color: Sclerotized parts brown to blackish, surface covered by soil incrustation. Overall coloration therefore influenced by substrate type. • Sexual dimorphism: Only minor differences in dimensions. No pheromone glands on male chelicerae or pedipalps (Figures 4.19d,e). • Juvenile stages: Differ much from adults: cuticle less sclerotized with paler coloration, lacking characteristic adult sculpture elements; the hood develops gradually; it does not totally hide the pedipalps at first, which are still visible on the outside. Distribution: Western Palearctic (Europe without northern and eastern regions, Mediterranean area with western North Africa and the Levant, in Southwest Asia to the Caucasus and northern Iran); Trogulus tricarinatus introduced in eastern North America. Relationships: Though very different in external appearance from other phalangids, Trogulidae were placed, together with Dicranolasmatidae, Nipponopsalididae, and Nemastomatidae, in the superfamily Troguloidea, mainly on account of genital morphology and sternal structure (Martens, 1976). The relation to Dicranolasmatidae is somewhat controversial but supported in some molecular analyses (Giribet et al., 2002). Main references: • Systematics: Martens (1978b), Martens & Chemini (1988). • Natural history: Pabst (1953), Martens (1978b).

LANIATORES Historical systematic synopsis Adriano B. Kury Major changes in the systematics of Laniatores have been proposed by a great number of authors, writing in a diverse set of languages, including Latin, German, English, Portuguese, Spanish, and Italian, over a span of 170 years. Most family names were created in the nineteenth century, while a surge of activity can be detected at the end of the twentieth. The arrangement of families in larger groups is not yet stable.

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In the late, eighteenth century, when the systematic study of Opiliones was mostly restricted to European researchers, the single genus Phalangium was recognized, being enough for the immediate post-Linnean scheme. Latreille (1802a) recognized the family Phalangides, which was in essence identical to the order Opiliones of today, but which was later equated only to the family Phalangiidae (Crawford, 1992). Kirby (1818) was the first to recognize the group Laniatores, erecting the new genus Gonyleptes, based on Brazilian material. Sundevall (1833) organized the five known genera and recognized three of the four current suborders of Opiliones in the following classification, which included an unjustified emendation for the genus name Gonyleptes: Ordo Opiliones Fam. 1. Gonoleptides new [= Laniatores]: genera Gonoleptes and Mitobates new. Fam. 2. Phalangides [= Eupnoi]: genus Phalangium. Fam. 3. Trogulides new [= Dyspnoi]: genera Trogulus and Caeculus. Perty (1833), who focused on the Brazilian fauna, discovered many new Laniatores, erected six new genera, and offered a systematic arrangement with two divisions in which Cosmetidae were surprisingly grouped together with his concept of Phalangium, which corresponds to the present-day Eupnoi + Dyspnoi. Perty’s classification was as follows: Familia Trachearia Phalangida—Divisio Phalangiorum Divisio Ima. 1. Gonyleptes 2. Ostracidium new 3. Goniosoma new 4. Stygnus new 5. Eusarcus new Divisio IIda. 6. Cosmetus new 7. Discosoma new 8. Phalangium Hope (1837) described a new genus “intermediate between Gonyleptes and Phalangium.” The genus in question was later discovered to be a synonym of Mitobates, a gonyleptid with very long legs, rectangular body, and armature of femora/tibiae absent. Thorell (1876) proposed a major classification, organizing the order Opiliones into two suborders, which merged Cyphophthalmi with Palpatores. Laniatores were divided into two families, one including the European and American genera and the other the Australasian ones.

Taxonomy

Ordo Opiliones Sectio I. Palpatores new Fam. Phalangioidae Fam. Nemastomoidae Subfam. Nemastomatini Subfam. Trogulini Fam. Cyphophthalmoidae Sectio II. Laniatores new Fam. Gonyleptoidae Fam. Cosmetoidae That same year Thorell (1876) reported the first Southeast Asian Laniatores for both of his families and created Oncopodidae as a subfamily of Cosmetidae. His classification of the Laniatores was as follows: Sectio Laniatores Fam. Gonyleptoidae Fam. Cosmetoidae [Fam. Cosmetinae] Fam. Oncopodinae new Simon (1879b) erected some new genera of Laniatores (for which he coined the term Mecostethi), mainly from South America. Important changes are the restriction of Cosmetidae to its present sense, explicitly excluding Oncopus, which was transferred to the newly created Phalangodidae, already in the sense later used by Roewer and followers. Another important change was the organization of Gonyleptidae into subfamilies. The planned part of his work including Coelopyginae/Caelopyginae never saw the light, and the name appeared only casually lost amid the text, making all subsequent authors (including Kury, 2003) assign this subfamily to Sørensen. His classification follows: Sub-Ordo Opiliones Mecostethi new 1. Familia—Phalangodidae new 2. Familia—Cosmetidae 3. Familia—Gonyleptidae 1. Sub-familia—Stygninae new 2. Sub-familia—Mitobatinae new 3. Sub-familia—Coelopyginae new 4. Sub-familia—Gonyleptinae Karsch (1880) described the genus Adaeum (a triaenonychid) from South Africa and considered it to be an intermediate between the families Cosmetidae and Gonyleptidae.

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Sørensen (1884) presented results of the study of diverse material, mainly from South America. He created several new families that were later mostly downgraded to subfamilies of Gonyleptidae. His classification of the Laniatores is as follows: Subordo II: Laniatores I. Phalangodidae II. Cosmetoidae III. Assamioidae new IV. Hernandaroidae new V. Gonyleptoidae VI. Coelopygoidae “new” (in parallel with Simon) VII. Pachyloidae new Following this classification, Sørensen (1886), in a book chapter dealing with Australasian fauna, presented important modifications by establishing new genera and as many as five of the currently accepted families. Interestingly, he recognized the affinity between his Dampetroidae from Australia and his own Assamioidae (described two years earlier) from India but failed to translate this into a classification. His classification (which was quickly adopted by Thorell) is as follows: Ordo Opiliones Subordo I. Palpatores Phalangioidae Subordo II. Laniatores Triaenonychoidae new Phalangodidae Zalmoxioidae new Epedanoidae new Samoidae new Dampetroidae new Gonyleptoidae Thorell (1889) created the family Biantoidae and later elevated Oncopodidae to family rank (Thorell, 1891). This change appeared in some of his works published in the 1890s and was promptly adopted by subsequent authors. Loman (1900, 1902) created the new suborder Insidiatores to include only Triaenonychidae. Epedanidae still included many unrelated genera today placed in various families. The classification he presented is as follows: Opiliones Sub-ordo Laniatores Fam. Oncopodidae Fam. Cosmetidae

Taxonomy

Fam. Gonyleptidae Fam. Assamiidae Fam. Epedanidae Fam. Biantidae Sub-ordo Insidiatores new Fam. Triaenonychidae Sub-ordo Palpatores Fam. Phalangiidae Subfam. Phalangiini Subfam. Gagrellini Pocock (1902b) criticized the Insidiatores of Loman, not in concept, but rather in degree, stating that there should be a group including Insidiatores + Laniatores. Within the same spirit of symmetry, he split the young family Triaenonychidae into three different ones, so that Insidiatores would have more than one family, namely, Adaeidae, Triaenobunidae, and Triaenonychidae. Pocock (1902a) created the superfluous family name Hinzuanidae to replace Biantidae on the basis of the fact that the generic name Hinzuanius predated Biantes by five years. The International Commission on Zoological Nomenclature (ICZN) (1999) states that any generic name may be chosen as the type of a family, not necessarily the oldest. Loman (1903a), in view of the criticism of Insidiatores by Pocock, hastened to explain his views in more detail. His system recognized Dyspnoi (a mix of current members of Eupnoi and Dyspnoi) and was the first to claim a position for Oncopodidae within the group known today as Grassatores (the same hypothesis defended by Martens, 1980). His classification follows: Suborder I. Palpatores Suborder II. Laniatores a. Sterrhonoti new (fam. Oncopodidae) b. Camptonoti new (fam. Gonyleptidae, Epedanidae, Assamiidae) Suborder III. Insidiatores Suborder IV. (?) Cyphophthalmi (= Anepignathi of Thorell) Roewer (1912b) promoted many changes in Assamiidae and Phalangodidae, such as creating many subfamilies, uniting the Australian Dampetridae with the African/Indian Assamiidae, and merging Zalmoxidae into Phalangodidae. He later summarized the taxonomy of the order Opiliones in a large volume (Roewer, 1923), complemented by a long series of addenda until the 1950s. His classification was immensely influential and persisted for many decades in spite of its numerous flaws. Many of the families of the former authors were downgraded to subfamilies: 1. Suborder Cyphophthalmi 2. Suborder Laniatores

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Taxonomy

1. Family Oncopodidae 2. Family Phalangodidae 1. Subfam. Samoinae 2. Subfam. Phalangodinae 3. Subfam. Tricommatinae 4. Subfam. Biantinae 5. Subfam. Stygnommatinae new 6. Subfam. Ibaloniinae 7. Subfam. Podoctinae 8. Subfam. Erecananinae 9. Subfam. Acrobuninae 10. Subfam. Sarasinicinae 11. Subfam. Epedaninae 12. Subfam. Dibuninae 3. Family Assamiidae 1. Subfam. Trionyxellinae 2. Subfam. Dampetrinae 3. Subfam. Assamiinae 4. Family Cosmetidae 1. Subfam. Cosmetinae 2. Subfam. Discosomaticinae 5. Family Gonyleptidae 1. Subfam. Pachylinae 2. Subfam. Prostygninae 3. Subfam. Phareinae 4. Subfam. Stenostygninae 5. Subfam. Gonyleptinae 6. Subfam. Mitobatinae 7. Subfam. Caelopyginae 8. Subfam. Cranainae 9. Subfam. Heterocranainae 10. Subfam. Stygnocranainae [sic] 11. Subfam. Stygninae 12. Subfam. Heterostygninae 13. Subfam. Hernandariinae 6. Family Triaenonychidae 1. Subfam. Triaenonychinae 2. Subfam. Adaeinae

Taxonomy

3. Subfam. Triaenobuninae 3. Suborder Palpatores 1. Tribe Dyspnoi 2. Tribe Eupnoi Sørensen, in an assembly of unpublished notes, published only posthumously by Henriksen sixteen years after his death (Sørensen, 1932), proceeded with the trend to create many smaller families, strongly contrasting with the then-widespread system by Roewer, which treated most of them as subfamilies. Henriksen tried hard to align Sørensen’s system with Roewer’s, even inserting the new families in Roewer’s classification. The Sørensen/Henriksen scheme is as follows: Opiliones Laniatores Superfamilia Gonyleptoidea Familia Hernandariidae Familia Gonyleptidae Familia Stygnidae Superfamilia Phalangodoidea Familia Acrobunidae Familia Dibunidae Familia Epedanidae Familia Erecananidae Familia Ibaloniidae Familia Minuidae new Familia Phalangodidae Familia Podoctidae Familia Samoidae Familia Saracinicidae [sic] Familia Stygnommatidae Familia Stygnopsidae new Familia Tricommatidae Not arranged in superfamilies Familia Assamiidae Familia Cosmetidae Familia Oncopodidae Familia Triaenonychidae Absolon and Kratochvíl (1932a,b,c) created the family Travuniidae, of interest mostly to speleologists. Hadzi (1935) created Cladonychiinae as a new subfamily of Triaenonychidae, which passed unnoticed until being resurrected by Cokendolpher (1985b). Mello-Leitão (1933a, 1938) reviewed Sørensen’s (1932) Phalangodoidea

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Taxonomy

(= Roewer’s Phalangodidae), adding important changes and breaking the large Phalangodidae into three separate families: Biantidae, Podoctidae, and Phalangodidae. He merged Sørensen’s Minuidae and Stygnopsidae into Phalangodidae and created the new subfamilies Isaeinae and Minuidinae within Phalangodidae. Mello-Leitão’s classification is as follows: Laniatores Assamiidae Biantidae new Biantinae Stygnommatinae Dibuninae Cosmetidae Gonyleptidae Oncopodidae Phalangodidae Acrobuninae Epedaninae Isaeinae new Minuidinae new Minuinae Phalangodinae Sarasinicinae Stygnopsinae Tricommatinae Podoctidae new Erecananinae Ibaloniinae Podoctinae Stygnidae Triaenonychidae Roewer (1943) provided a synoptic table for the classification of Gonyleptidae, contributing a few new subfamilies and summarizing all his and Mello-Leitão’s contributions to that family in the 1920s and 1930s. Mello-Leitão (1949), in his last article, provided a new general arrangement of Laniatores and explained at length his criteria of diagnosis. Phalangodidae was kept exactly as in his 1938 article. He recognized Travuniidae, absent from virtually all 1940s literature, separated Assamiidae with tarsal processes in a new family, Trionyxellidae, elevated the rank of Stygnommatinae (then in Biantidae) to family, and described a new subfamily of Gonyleptidae (Dasypoleptinae). In a review of Laniatores from New Zealand, Forster

Taxonomy

(1954) described many new genera and created a very influential system for Triaenonychidae, separating the egg-guarding species from the non-egg-guarding as two subfamilies and downgrading Pocock’s families to tribes. He also created the new family Synthetonychiidae, which he regarded as closely related to Triaenonychidae. Kratochvíl (1958a), on the basis of posterior tarsal claw structure, proposed two superfamilies of Laniatores, Oncopodoidea and Travunoidea [sic], retrieving the system of Loman (1902) and Pocock (1902b) defended years later by Martens. He ignored the subdivisions proposed by Mello-Leitão (1938, 1949) and created the new family Paralolidae and another subfamily of Phalangodidae, Lolinae. Lawrence (1959), while dealing with Biantidae from Madagascar, created Lacurbsinae, a name buried amid the text and forgotten by most subsequent authors. Silhavy (1961), contradicting Kratochvíl (1958a), placed Oncopodidae in the suborder Oncopodomorphi as the sister group to all other Laniatores (= Gonyleptomorphi), which remained unchanged. Later Silhavy (1973), on the basis of material from the Antillean region and Trinidad, described Agoristenidae and Caribbiantinae (in Biantidae) and recognized the classification of Mello-Leitão (1938, 1949). Silhavy (1974) recognized Stygnopsidae after some dubious inclusions and exclusions of its genera in Phalangodinae or Phalangodidae Stygnopsinae (e.g., Goodnight & Goodnight, 1944, 1946). Travunioidea were more intensely investigated in the 1970s; Briggs (1969) created the family Erebomastridae and later (Briggs, 1971a,b) reviewed most North American species of Triaenonychidae and proposed a new subfamily. Suzuki (1975b, 1976e) followed Briggs and also proposed two new subfamilies of Japanese/Korean Triaenonychidae. Both Briggs (1974a) and Suzuki (1976d) devised a phylogenetic scheme based on the number of lateral prongs of the tarsal claws of adults and juveniles. Dumitrescu (1976), on the basis of his studies of the midgut diverticules, proposed a subfamily of Triaenonychidae ignored by all other authors. Martens’s (1980) nonnumerical cladistic analysis combined the LomanKratochvíl concept of Insidiatores versus Laniatores sensu stricto with the Sterrhonoti versus Camptonoti of Loman (1903a). Soares and Soares (1984) revalidated Hernandariinae and later (1985) described Progonyleptoidellinae and Sodreaninae, all considered subfamilies of Gonyleptidae. Kauri (1985) focused on the Laniatores of central Africa and placed Dibuninae and Stygnommatinae among Biantidae, together with his new subfamily Zairebiantinae. South America provided some new families of small, soil-dwelling Laniatores, all described within the last 20 years. Martens (1988) created Fissiphalliidae on the basis of Colombian material. González-Sponga (1997) erected Guasiniidae from Venezuela. Kury and Pérez G. (2002) described Icaleptidae on the basis of material from Ecuador and Colombia. The 1990s and the twenty-first century saw many rearrangements in the established groups, partly due to the use of numerical cladistic analyses. Kury (1992a) removed Tricommatinae from Phalangodidae, an arrangement unquestioned for 80 years, and upgraded it to family level. Kury (1994a,b) studied the basal branches of

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Taxonomy

Gonyleptidae, described Cobaniinae, Metasarcinae, and Heteropachylinae within Gonyleptidae, and transferred Cranainae, Heterocranainae, Prostygninae, and Stygnicranainae to Cranaidae. Pinto-da-Rocha (1995a) proposed the identity of Silhavy’s Caribbiantinae with Roewer’s Stenostygninae. Kury (1997a) removed Manaosbiinae from Gonyleptidae, created the family Manaosbiidae, and transferred to it 26 genera that were previously in Gonyleptidae or Cranaidae. In a cladistic analysis of Agoristenidae, Kury (1997b) described Zamorinae and synonymized Angelinae with Leiosteninae. Pinto-da-Rocha (2002) synonymized Dasypoleptinae with Caelopyginae. Kury (2002) offered evidence that the non-Grassatores Laniatores are a diphyletic group, but this has not yet been organized and properly documented for publication. Kury (2003) published an annotated catalogue of the New World Laniatores, which contained the characterization of the new family Escadabiidae and Ampycinae, a new subfamily of Gonyleptidae. In this catalogue there is also a table with a classification of Laniatores as viewed by the author based on either published or unpublished data. Changes to the system include a definition of the family Epedanidae containing four subfamilies formerly in Phalangodidae and a formalization of Grassatores—recovering the concept of Loman (1903a) of Insidiatores versus Laniatores sensu stricto. Key to the families of Laniatores Ricardo Pinto-da-Rocha 1. Ocularium separated into two parts (Figure 4.22c) or absent (Figure 4.42a). . . . 2 . Ocularium unique or with eminence between eyes. . . . . . . . . . . . . . . . . . . . . . . . . . 9 2. Ocularium and eyes absent (except most troglobites) . . . . . . . . . . . . . . . . . . . . . . . . 3 . Ocularium and eyes present (Figure 4.22c) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 3. Pedipalps without ventral setae on sockets or both much shorter than pedipalp length (Figure 4.28g); claws III–IV single or very branched on a stem (Figures 4.41e–g). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 . Pedipalps with ventral setae on large sockets (both longer than pedipalpal tarsus length, Figure 4.42i); two single claws on legs III–IV. . . . . . . . . . . . . . Travuniidae 4. Claws III–IV single. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Guasiniidae . Claws III–IV branched (Figures 4.41e–g). . . . . . . . . . . . . . . . . Synthetonychiidae 5. Male basichelicerite elongated, segment II with spines or conspicuous tubercles (Figure 4.39b); body outline pyriform to hourglass in dorsal view (Figure 4.36b). ......................................................................6 . Male basichelicerite not elongated, segment II smooth or granulated; body outline rectangular-subrectangular in dorsal view (Figure 4.38d) . . . . . . . . . . . . . . . . . . . 7 6. Dorsal surface covered with low tubercles; leg I small-tuberculate; pedipalp with moderate setae with low sockets on tibia-tarsus; without spine between eyes (Figures 4.39a,b). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Stygnommatidae

Taxonomy

. Dorsal surface with conspicuous tubercles and spines; leg I with tubercles longer than segment width; pedipalp with huge setae and sockets on trochanter-tarsus; most species with a spine with large base between eyes (Figures 4.36a–c). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Podoctidae 7. Tarsal process (legs III–IV) present in most species; penis with well-defined ventral plate (Figures 4.38g–i) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Stygnidae . Tarsal process (legs III–IV) absent; penis without well-defined ventral plate, blunt apically . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 8. Pedipalps thin, without setae (Figures 4.22d–f), or with a few setae on pedipalpal femur-patella; never with dorsal tubercles on patella-tarsus . . . . . . . . . Biantidae . Pedipalps robust, with numerous setae or tubercles on femur-patella; with dorsal tubercles on patella-tarsus (Figures 4.26a,b) . . . . . . . . . . . . . . . . . . . . Epedanidae 9. Tergites I–VIII fused (scutum completum, Figures 4.33a,b); tarsi I–IV with one to three tarsomeres . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Oncopodidae . Tergites VI–VIII free; tarsi I–IV with four or more tarsomeres (sometimes only tarsus I with three tarsomeres). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 10. Two single unbranched claws on tarsi III–IV. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11 . Diverse complex claws on tarsi III–IV (Figures 4.34f, 4.44l–p) . . . . . . . . . . . . . 28 11. Tarsal process present (Figures 2.7f,g). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 . Tarsal process absent. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15 12. Ocularium strongly depressed between eyes, without or with small tubercles (Figures 4.24g, 4.32c); body brown . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13 . Ocularium not depressed between eyes, unarmed, with small tubercles to large spines; body color varies from light color to black. . . . . . . . . . . . . . . . . . . . . . . . . 14 13. Pedipalps spatulate (Figure 4.24o); male basitarsus I not spindled. Cosmetidae . Pedipalps cylindrical; male basitarsus I spindled (Figure 4.32b). Manaosbiidae 14. Pedipalps densely covered with dorsal tubercles (Figures 4.25d). . . . Cranaidae . Pedipalps without dorsal tubercles or just some scattered. . . . . . . Gonyleptidae 15. Pedipalpal femur with a ventral row of tubercles (Figures 4.21c,d), close to each other, sometimes equal sized, tubercles shorter than femur height . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Assamiidae . Pedipalpal femur without a ventral row of tubercles close to each other; tubercles, when present, usually on ventrobasal portion, scattered and low. . . . . . . 16 16. Dorsal scutum with lateral margins almost parallel or with a slight constriction on sulcus I (Figure 4.20a). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17 . Dorsal scutum with lateral margins with a marked constriction on sulcus I; opisthosoma much wider than prosoma . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18 17. Femur–tibia I usually filiform (Figure 4.20e); pedipalp may have setae longer than tarsus length (Figure 4.20f); cheliceral segment II never has tubercles, fingers with weak teeth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Agoristenidae

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Taxonomy

. Femur–tibia I width similar to legs II–IV; pedipalp with setae shorter than tarsus length; cheliceral segment II with tubercles, fingers with strong teeth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Epedanidae 18. Pedipalpal femur compressed (Figure 4.23b); tarsal claws III–IV fused basally in a narrow stem (Figure 4.23f). . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cladonychiidae . Pedipalpal femur not compressed or slightly compressed; tarsal claws III–IV separated. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19 19. Setae of pedipalpal tibia-tarsus longer than pedipalpal tarsus length (Figures 4.35a,b) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Phalangodidae . Setae of pedipalpal tibia-tarsus shorter than pedipalpal tarsus length. . . . . . . 19 20. Coxa IV inserted ventrally (Figures 4.31a,d) . . . . . . . . . . . . . . . . . . . . Icaleptidae . Coxa IV inserted laterally. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21 21. Prosoma much shorter (width and length) than rest of dorsal scutum (Figure 4.31i) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22 . Prosoma a little shorter (width and length) than opisthosoma . . . . . . . . . . . . . 25 22. Dorsal scutum sulci never V shaped; penis without pergula and rutrum. . . . . 23 . Dorsal scutum sulci V shaped in most species (Figures 4.45b,c); penis with pergula and rutrum (Figures 4.45h,i) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24 23. Distitarsi I three-segmented . . . . . . . . . . . . . . . Gonyleptidae (Tricommatinae) . Distitarsi I two-segmented. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Kimulidae 24. Penis with a long stragulum, with arrow-shaped apex, protecting a long, straight, and slender stylus (Figure 4.45i) . . . . . . . . . . . . . . . . . . . Fissiphalliidae . Penis with a short stragulum, with arrow-shaped apex, stylus short (Figure 4.45h) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Zalmoxidae 25. Scopulae present on tarsi III–IV (Figure 4.37e); metatarsus III of male swollen (Figure 4.37d) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Samoidae . Scopulae absent on tarsi III–IV; metatarsus III not swollen . . . . . . . . . . . . . . . . 26 26. Male tibia I or II and male femur IV incrassated or tibia I saddle shaped/warty (Figures 4.27b,e) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Escadabiidae . Male tibiae and femur IV not incrassated; tibia I not saddle shaped/warty. . . . 27 27. Area I divided by median groove (Figures 4.29a–i); coxa II with maxillar lobes; male chelicera usually not swollen . . . . . . . . . . . . . . . . . . . . . . . . . . Gonyleptidae . Area I undivided (Figure 4.40a); coxa II without maxillar lobes (Figure 4.40b); male chelicera swollen. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Stygnopsidae 28. Ocularium rounded, close to anterior border of carapace; body usually densely covered with granules/tubercles, can harbor spines (Figures 4.43b,c, 4.44h) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Triaenonychidae . Ocularium in median position on the carapace, twice as wide as long; body smooth or with a few small granulates, never with spines . . . . . . . . . . . . . . . . . 29

Taxonomy

29. Claws III–IV multibranched (on a 90° stem), placed on a stem (Figure 4.42b); tarsus II with five to six segments. . . . . . . . . . . . . . . . . . . . . . . . . . . . . Travuniidae . Claws III–IV with five branches (never on a 90° stem, Figures 4.34f,g); tarsi II with 13 to 15 segments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pentanychidae

ˇilhavy´, 1973 Agoristenidae S Ricardo Pinto-da-Rocha and Adriano B. Kury Etymology: Agoristenus, presumably from Greek agora (gathering) and stenos (few); related to rarity of the family at time of discovery. Characterization: • Size: body length around 2–5 mm. • Dorsum: Body trapezoidal attenuate (Zamorinae, Figure 4.20c), rectangular (Leiosteninae, Figure 4.20a) to oval (Agoristeninae, Figure 4.20e). Ocularium close to anterior border, very high with a pair of spines (Zamorinae, Figure 4.20c) or low with median depression (saddle shaped, Figure 4.20a) and usually smooth and unarmed (Agoristeninae, Leiosteninae, Figure 20a). Four areas on dorsal scutum, often effaced; I–IV and posterior margin with small tubercles; I divided; III–IV, posterior margin, and free tergites with or without a pair of spines. • Venter: Coxae with transverse rows of granules, growing larger anteriorly. Coxae I–III parallel to each other, IV a little more developed, but not hypertelic. Spiracles usually exposed. • Chelicerae: Similar in both sexes (Agoristeninae) or with enlarged segment II on males (Zamorinae and almost all Leiosteninae); segment I smooth or with small tubercles on dorsal. • Pedipalps: Short, thick with short setae (Agoristeninae, Zamorinae, Figure 4.20c) or slender with very long setae (Leiosteninae, Figure 4.20f). • Legs: Usually straight; I filiform and very short (Agoristeninae, Leiosteninae), II–IV normal or very long (Leiosteninae), I–IV short and densely granulate (Zamorinae, Figure 4.20c); IV with large tubercles in some males (Agoristeninae) or minute-tuberculate. Coxa IV anterior (near grooves II–III). Tarsal formula: 4–9(3):7–28(3–6):5–8:5–10. Tarsal process absent (except males of Lichirtes); claws smooth and subparallel. • Genitalia (Figures 4.20g–i): Truncus with an apical ventral plate short, unarmed, and divided; with strong setae bent to proximal side, uniramous (Zamorinae), bifid, or trifid (Agoristeninae, Leiosteninae). Stylus usually with dorsal soft longitudinal crest or keel. • Color: Varies from yellowish to dark brown; may show yellow stripes or white or green patches. Legs and tubercles may be darker. • Sexual dimorphism: Shown by cheliceral hand (segment II) swollen in males, tubercles on trochanter to tibia (mainly on leg IV) of males, and enlarged male astragalus IV.

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Figure 4.20. Agoristenidae. Leiosteninae, Trinella bubonica: (a) habitus dorsal; (b) lateral. Zamorinae, Zamora vulcana: (c) habitus dorsal; (g) penis, dorsal. Agoristeninae, Leptostygnus leptochirus: (d) habitus lateral; (e) dorsal. Leiosteninae, Trinella matintaperera: (f) pedipalpus; (h) penis, dorsal; (i) lateral. Scale bars: a–f = 1 mm; g–i = 0.1 mm. Sources: a–b, González-Sponga (1997); c, g, Kury (1997b); d–e, Kury (1993b); f, h–i, Pinto-da-Rocha (1996c).

Taxonomy

Key to subfamilies 1. Leg I short and thick, ocularium enlarged (Figure 4.20c). . . . . . . . . . . Zamorinae . Leg I elongated and filiform, ocularium low, strongly depressed medially (Figure 4.20a). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 2. Male chelicera swollen; pedipalp with long setae on ventral femur and tibia-tarsus (Figure 4.20f) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Leiosteninae . Chelicera similar in both sexes; pedipalp with short setae on ventral femur and tibia-tarsus (Figure 4.20d). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Agoristeninae Distribution: Agoristeninae is endemic to the Greater Antilles. Leiosteninae and Zamorinae were recorded from northern South American countries (Peru, Colombia, Venezuela, Guyana, Surinam, French Guiana, and Brazil). Relationships: Leiosteninae and Agoristeninae are sister groups, and Zamorinae is the basal clade (Kury, 1997b). Agoristenidae is the sister group of all Gonyleptoidea except Stygnopsidae (Kury, 1997c). Main references: • Systematics: Silhavy (1973), González-Sponga (1987), Kury (1993b, 1997b). • Natural history: González-Sponga (1987), Pinto-da-Rocha (1996c).

Assamiidae Sørensen, 1884 Adriano B. Kury Etymology: Assamia, from Assam, the province in India where Assamia westermanni has been collected. Characterization: • Size: Medium-sized to large Laniatores, body length 2–8 mm. Legs I–IV very variable, 4–25/8–70/5–30/7–40 mm long. • Dorsum: Dorsal scutum (Figures 4.21a,b,e) outline much wider at opisthosoma, often with a major constriction at area IV. Mesotergum usually clearly divided into areas by grooves, which may be partially effaced. Armature of areas and tergites highly variable, perhaps either completely smooth and unarmed or armed with spiniform apophyses. In some species the scutum is densely covered with granules and tubercles. Ocularium always present, usually low and with weak armature, sometimes elevated, forming a frontal cone (Figure 4.21e), with eyes much reduced or absent (Irumuinae). • Venter: Coxae apically with large lobes. Spiracles often concealed by stout tubercles (Figure 4.21b). • Chelicerae: Cheliceral hands usually not swollen, and basichelicerite rarely with ornamentation of tubercles, but when present may be extremely dense

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(as in Scabrobunus from India, Figure 4.21i). Exceptionally, chelicerae can be extremely long only in males (as in Eubaeorix from Myanmar, Figure 4.21h) or swollen in males (as in Bolama, Figure 4.21g, and Mermerus). Pedipalps: Very homogeneous with ventral row of setiferous tubercles on the compressed femur and ventromesal and ventroectal (distal one largest) spines in patella-tibia-tarsus (Figures 4.21c,d). Tibia and tarsus do not form a subchela. When the animal is alive, the pedipalps rest on the chelicerae. Legs: Usually long, straight, and unarmed, often entirely smooth. Apical part of coxae ventrally and dorsally often with large lobes and projections (Figures 4.21e,f). Femur to tibia IV may be crooked and/or inflate. Distitarsus I two- or three-jointed; II typically three- or four-jointed. Color: Background usually reddish brown to yellow, with black mottling and reticulation. Some species have white drawings on dorsal scutum. Genitalia: Known for only a few species. Shape of ventral plate and distal part of truncus extremely variable (Figures 4.21d,e). Glans is mounted on a sac whose distal part is eversible, being often spiny, exposing the stylus (Figures 4.21j,k). Sexual dimorphism: Weakly developed, sometimes present in male chelicerae or leg IV.

Subfamilies: The numerous Roewerian subfamilies are unsupported, and some were already synonymized by Starega (1992). There are at least five great groups of Assamiidae: (1) the dampetrines from Australia and Papua New Guinea, (2) the typical Indian/Nepalese Assamiinae, (3) the Sri Lankan/Indian pseudonychiate genera known as Trionyxellinae, (4) the central African Erecinae, and (5) the small, blind, cave- on soil-dwelling Irumuinae. Boundaries of these groups do not coincide with the subfamilies as currently recognized. A key to the subfamilies cannot be provided at this time because of the uncertainty of the subfamilial designations. Distribution: Assamiids are endemic to the Old World. There are several Erecinaelike groups in many countries of central Africa, reaching South Africa, where they are rare and confined to the northeastern portions. Assamids are completely absent from Madagascar, Europe, the Pacific islands, and the Americas. Dampetrinae diver-

Figure 4.21. Assamiidae. (a–d) Pashokia yamadai, male from Nepal: (a) Habitus dorsal, showing the powerful frontal prongs in the carapace; (b) habitus ventral; (c) right pedipalpus, ectal, showing the typical compressed femur with a ventral row of small setiferous tubercles; (d) left pedipalpus (female), mesal. (e–f) Typhlobunus troglodytes, male from Kenya: (e) habitus dorsal; (f) ventral. (g) Bolama spinosa, male from Guinea-Bissau, habitus lateral, showing cheliceral hand inflated and rows of high spines on scutal areas and free tergites. (h) Eubaeorix gravelyi, male from Myanmar, habitus lateral, showing the immensely developed chelicerae. (i) Scabrobunus filipes, male from India, habitus dorsal, showing densely clustered tubercles at coxa IV and chelicerae. (j–k) Schematic penis structure in lateral view showing the eversible spiny funnel (Stacheltrichter); (j) unexpanded; (k) expanded. (l) Typhlobunus sp, male (Tanzania), penis, distal part, dorsolateral. (m) Nilgirius scaber, male (India), penis, distal part, lateral. Scale bars: l–m = 60 ␮m. Sources: a–d, Suzuki (1970); e–f, Roewer (1923); h Roewer (1927); j–k, Martens (1977). Photos: D. Ubick.

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sified in Australia, Papua New Guinea, and to a lesser degree in Indonesia. Apart from India, there are many species of Assamiinae-like groups in the Indian subcontinent (Bangladesh, Bhutan, Nepal, Sri Lanka). A few species have been recorded also in Southeast Asia, in Myanmar and Malaysia. Relationships: Assamiidae was included by Kury (1993a) in a cladistic analysis of what is now known as Grassatores, and was identified as the sister group of the American Gonyleptoidea. The spiny funnel of the penis has very similar counterparts in Mexican Stygnopsidae, and the outline of the dorsal scutum is typical of Gonyleptoidea (Kury, 1997c). However, more data are needed to test this hypothesis. Main references: • Systematics: Sørensen (1884, 1886), Roewer (1912b, 1935b, 1940), Martens (1977, 1986), Starega (1992). • Natural history: Roewer (1935b), Martens (1977, 1993b), Hillyard (1981), Kauri (1989).

Biantidae Thorell, 1889 Adriano B. Kury and Abel Pérez González Etymology: Biantes, son of Parthenopaeus, was one of the Epigoni who marched against Thebes in Greek mythology. Characterization: • Size: Body 1.5–5.5 mm long. Legs I–IV: 3–12/4.3–23/3–16/4.5–25 mm long. • Dorsum: Dorsal scutum trapezoid in Biantinae, in Stenostygninae almost rectangular (Figure 4.22i); in Lacurbsinae it has convergent posterior margins (Figures 4.22c,k). Frontal border of the carapace straight with small cheliceral sockets. Common ocularium absent; the placement of the eyes is far backward in the carapace for Biantinae and Stenostygninae, more or less in the middle in Lacurbsinae (Figure 4.22k), and in Zairebiantes the eyes are placed close together near the front (Figure 4.22b). Typically with small frontal hump. Sulcus I marked, mesotergal areas typically unarmed in Biantinae (except in a few species, e.g. Fageibiantes bispina, Hovabiantes spp., Biantes parvulus, and B. albimanus from the Seychelles); in many species of Antillean stenostygnids, Lacurbsinae and the areas and free tergites can be armed with a powerful spiniform apophysis. • Venter: Without remarkable features; tracheal spiracles not concealed by bridges, but may be hidden under the fold separating coxa IV from the spiracular area. • Chelicerae: With well-marked bulla, hypertelic in males of Stenostygninae. • Pedipalps: Enlarged, subchelate tibia-tarsus armed with large setiferous tubercles, patella ventrally with or without a mesoventral setiferous tubercle, thin and almost unarmed femur, commonly with only one ventrobasal small setif-

Taxonomy

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erous tubercle. Zairebiantinae (Figure 4.22d) with pedipalps armed in all segments. Legs: Commonly without relevant armature (Figure 4.22a) except in some species with strong spiniform apophysis in femur IV of males, such as Hovabiantes spp. (Biantinae), and in Lacurbsinae with a leg IV enlarged with incrassate tibia showing strong spiniform ventral apophysis (Figure 4.22c). Without tarsal process and scopula except in Stenostygninae. Metatarsus III spindled only in Stenostygninae. Genitalia: Typically (as in Nepalese Biantinae, Figure 4.22n) can be distinguished by having a fully retractable capsula interna. The follis is reduced, modified in a pair of soft titillators that almost invert its position when the capsula interna is everted (see Figure 4.22n). Capsula interna formed by a pair of rigid and tubular conductors, stylus simple (without parastylar collar). Truncus without a welldefined ventral plate as in Gonyleptoidea, cylindrical, blunt apically (some species with lamina ventralis developed, e.g., most of the Malagasy Biantinae). In some species the pars distalis is laterally widened. Pars distalis ventrally with small acute setae and subapical Schwellkörper, division between pars distalis and pars basalis not evident. Stenostygninae have a pair of well-developed rigid titillators that cover the entire capsula interna and do not invert its position when the capsula interna is exposed; they also have small less developed conductors. Stenostygnus pusio has a flattened pars distalis apically divided with small titillators. Color: Many species have a uniform mahogany background; many are yellow with brownish or blackish mottling. Sexual dimorphism: Zairebiantinae and Biantinae commonly without remarkable sexual dimorphism. Exceptions in Biantinae: Some species of Hovabiantes from Madagascar have heavy armature in the femur to tibia IV of the males (Lawrence, 1959); South African species of Metabiantes may have dimorphism in metatarsus II, which is serrated in males, or in trochanter II, which is immensely swollen in males (Lawrence, 1937a). There is a notable sexual dimorphism in size and pattern of the genital operculum in Nepalese Biantinae (Martens, 1978a). Lacurbsinae have a zalmoxiform leg (Figure 4.22c). Stenostygninae have a hypertelic chelicera (except in Stenostygnus) and enlarged metatarsus III. The hypertelic condition of the chelicera could be present and absent in males of the same species; for that reason this character needs to be carefully taken when sexing individuals. Key to the subfamilies

1. Opisthosomal scutum much wider in the middle, with acuminate apophyses in the lateral areas. Tibia and metatarsus IV heavily armed and/or swollen in males (Figure 4.22c) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Lacurbsinae . Opisthosomal scutum never wider in the middle, without armature in the lateral areas (Figure 4.22b,i,j). Tibia and metatarsus IV slender and cylindrical in both sexes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

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Taxonomy

2. Eyes close together and placed in the anteromedian region of the carapace (Figure 4.22b). Pedipalpal femur tapering distally and armed with strong setiferous tubercles. Tarsi III–IV without scopula . . . . . . . . . . . . . . . . . . . . . . . . . . . Zairebiantinae . Eyes widely separated and placed in the lateroposterior region of carapace. Pedipalpal femur not tapering and unarmed. Tarsi III–IV with dense scopula (Figure 4.22h). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 3. Opisthosomal scutum subrectangular. Chelicerae of male mostly inflated. Titillators rigid and completely covering the capsula interna (Figure 4.22l). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Stenostygninae . Opisthosomal scutum smoothly growing wider posteriorly. Chelicerae of male never inflated. Titillators soft and folding to outside revealing the capsula interna (Figure 4.22n) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Biantinae Distribution: The peak of diversity of typical Biantidae is in the Indian subcontinent—with many species described from Nepal—Madagascar, and nearer Indian Ocean islands, and they barely penetrate in Southeast Asia. Many genera occur in Africa, while Stenostygninae are poorly represented in the northern part of South America, but peak in the Greater Antilles. Relationships: Biantidae is included in Samooidea, which appears to have undergone a major radiation in the Neotropics, resulting in the diverse and closely related families Kimulidae, Escadabiidae, Stygnommatidae, and Samoidae and other species of uncertain affinities. Main references: • Systematics: Roewer (1923), Martens (1978a). • Natural history: Martens (1978a), González-Sponga (1992b).

Cladonychiidae Hadˇzi, 1935 Thomas S. Briggs and Darrell Ubick Etymology: Cladonychium, from Greek, branched claw. Figure 4.22. Biantidae. (a) Lacurbs sp. (Cameroon), male, habitus lateral. (b) Zairebiantes microphthalmus (Zaire), male, habitus lateral (from Kauri, 1985). (c) Lacurbs spinosa (Cameroon), male, habitus dorsal (from Roewer, 1923). (d) Z. microphthalmus (Zaire), pedipalpus, lateral (from Kauri, 1985). (e) Biantes sherpa (Nepal), pedipalpus, lateral (from Martens, 1978a). (f) Galibrotus carlotanus (Cuba), pedipalpus, lateral (from Avram, 1977). (g) Caribbiantes sp. (Cuba), male, metatarsus III, ventral. (h) Caribbiantes sp. (Cuba), male, last segment of tarsus III showing scopula, ventral. (i) G. carlotanus (Sˇilhavy´, 1973) from Cuba, male, habitus dorsal (from Avram, 1977). (j) Biantes sp. (India), male, habitus dorsal. (k) Lacurbs sp. (Cameroon), male, habitus dorsal. (l) Caribbiantes sp. (Cuba), male, distal part of penis, dorsolateral. (m) Z. microphthalmus (Zaire), distal part of penis, dorsolateral (from Kauri, 1985). (n) Biantes sherpa (Nepal), distal part of penis expanded, lateral and dorsal (from Martens, 1978a). Photos: a and k by A. B. Kury; g–h, j, and l by A. Pérez González. Abbreviations: Co = conductors, Ti = Titillators.

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Characterization: • Size: Body length 1.7–4.0 mm. • Dorsum (Figures 4.23a,d): Eyes, when present, situated on median tubercle. Areas undivided. • Venter: Without a free ninth tergite, lateral sclerites absent. Sternum with broadened posterior portion between fourth coxae. Endites of second coxae extend forward, ectal and, in some genera, anterior to labial processes. • Chelicerae: Vary as a generic character; basal segment smooth or with one to three small spines on dorsum. • Pedipalps (Figures 4.23b,c): Robust, femur and tibia spinose, tarsus with more than four prominent spines. • Legs: Distitarsi II with three or more tarsomeres. Tarsal formula: 4–9(2–3):8– 20:4–8:4–8. Claws III–IV bifurcate with two branches fused to narrow stem (Figures 4.23e,f); juveniles have four to six branches and an apical arolium on stem. The length of stem and angle of branches vary among genera. • Genitalia (Figures 4.23g–j): Truncus with muscles in base (Holoscotolemon) or from base to apex (Nearctic genera). Distal attachment of muscles is to chord or tendon that articulates the apical glans and has a basal extension of at least half the length of the truncus. Glans simple, typically with two to three pairs of setae, with dorsal and ventral plates joined around stylus, laterally compressed in some genera (Cryptomaster, Erebomaster). Ovipositor with four apical lobes and long to short apical setae. • Color: Typically reddish brown to dark brown, but pale yellow in troglobitic species. • Sexual dimorphism: Males of Theromaster have elongate tubercles and swollen movable finger of chelicera; pedipalp with spur at base of apical claw, ectoventral spines fused at base of tarsus, and a dense row of reduced ventral spines on femur. Males of Cryptomaster and Speleomaster have the ventral surface of tibia II with distal swelling or tubercle bearing enlarged setae in males. Some males of Holoscotolemon have pronounced spination on the pedipalpal tarsus. Distribution: Holoscotolemon is Palearctic, ranging from France east to Romania and Serbia and Montenegro, with most species occurring in northern Italy. The remaining genera are Nearctic (USA). Cryptomaster and Speleomaster are western, found in Oregon and Idaho, respectively. Erebomaster and Theromaster are eastern, occupying the region from Arkansas and Indiana to Virginia and Alabama. A new genus, Proholoscotolemon, has recently been described from Baltic amber (Ubick & Dunlop, 2005). Relationships: The monophyly of Cladonychiidaeis supported by the uniquely bifurcate claws III–IV that develop from an aroliate juvenile claw. Also, all genera have a relatively simple glans morphology, which was regarded as derived within Travunioidea (Martens, 1986). Both Martens (1986) and Hunt and Hickman (1993) regarded Cladonychiidae as most closely related to Travuniidae, not only on the basis of simplified glans structure but also because of reduced musculature of the penis. However, as both Nearctic cladonychiids and southern European travuniids have a

Taxonomy

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Figure 4.23. Cladonychiidae. (a–b, e–f) Holoscotolemon unicolor; (c–d, g–j) Erebomaster acanthina. (a, d) Habitus dorsal. (b–c) Lateral. (e–f) Hind claws, lateral and dorsal. (g–h) Ovipositor, lateral and ventral views; (i–j) penis, ventral and lateral views. Photos: D. Ubick. Figures a–d from Briggs (1969, 1974a). Scale bar next to a applies to images a–f (a–b = 1 mm, c–d = 0.5 mm, e–f = 200 ␮m). Scale bar next to i applies to images g–j (= 30 ␮m).

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fully musculated truncus in the penis, it appears that muscle reduction was independently derived. A relationship with Pentanychidae was suggested by Briggs (1971b), not only on the basis of glans simplification, but also because of similarity in claw structure. For example, claws III–IV of Pentanychus have two apical branches enlarged to where further reduction of the basal ones would result in a cladonychiid claw. This reasoning suggests that the eastern Nearctic cladonychiids, which have small, vestigial branches on their claws, may be basalmost in the family. Main references: • Systematics: Hadzi (1935), Briggs (1969), Cokendolpher (1985a), Martens (1978b), Tedeschi & Sciaky (1994), Ubick & Dunlop (2005). • Natural history: Juberthie (1964)

Cosmetidae Koch, 1839 Adriano B. Kury and Ricardo Pinto-da-Rocha Etymology: Cosmetus, from Greek kosmetós, ornate. Characterization: • Size: Body length 3–12 mm long, leg IV 4–54 mm long. • Dorsum (Figures 4.24b–d,g,j,k): Dorsal scutum widest at area II or III. Ocularium is very low, saddle shaped, placed on middle of prosoma; each ocular globe bears a crest of small pointed tubercles or is smooth. Ozopores slitlike, one opening partially covered by tubercle of coxa II. Scutal areas are often indistinct; sometimes the sulci can be distinguished by color pattern or absence of tubercles; scutum and tergites are typically weakly armed (sometimes area III or IV or free tergites with strong spines or tubercles or fused spines, Figures 4.24j,n); anal operculum sometimes with stout apophyses; scutum normally covered with minute granules. Body can be extremely elongate. Coxa IV usually entirely visible or more rarely partially visible on dorsal view. • Ventral (Figure 4.24h): Coxa I possesses ventrally a notch for the locking of pedipalpal trochanter, forming a channel flanked by apophyses that may show large variation in the diverse genera (C. P. Ferreira, pers. comm.). • Chelicerae: Rear margin of basichelicerite has plenty of teeth and spines or is smooth. • Pedipalps (Figures 4.24a,o): Coxa very short, trochanter much longer than wide, clavate; femur is strongly compressed laterally with serrate ventral margin sometimes also on dorsal. Tibia is spoon shaped, mesally concave, expanded ectally, and very weakly armed with ventral setae in all extensions or on distal half; tarsus is shorter than tibia with two rows of thin or thick ventral setae, claw slightly curved. The pedipalps cover the frontal part of the chelicerae, mainly the tibia, as a scutum. In nymphs the pedipalp is longer than in adults (especially the patella and tarsus), slender, and cylindrical (Juberthie, 1972, Goodnight & Goodnight, 1976).

Taxonomy

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Figure 4.24. Cosmetidae. (a–b) Ambatoiella vigilans male from Ecuador, habitus: (a) lateral; (b) dorsal. (c) Platycynorta clavifemur, male from Peru (from Roewer, 1957a). (d) Ferkeria vestita male from Bolivia (from Roewer, 1947). (e–f) Paecilaema pectinigerum, from Honduras, femur IV; (e) prolateral; (f) retrolateral (from Roewer, 1923). (g–h) Cynortula oblongata, from Ecuador, habitus: (g) dorsal; (h) ventral (from Roewer, 1927). (i) Eucynortula metatarsalis from Mexico, metatarsus IV (from Roewer, 1923). (j) Vonones octotuberculatus from French Guyana (from Roewer, 1923). (k) Metagryne albireticulata from Peru (from Roewer, 1952). (l–m) Cosmetus peruvicus from Peru (from Avram & Soares, 1983): (l) tarsus I; (m) tarsus III, showing pectinate claws; (n) habitus lateral. (o) Paecilaema sp. from Brazil, femur to tarsus of pedipalp, ventral. (p–q) Metavononoides sp. from Brazil, distal part of penis: (p) dorsal; (q) lateral. Scale bars: a–b = 1 mm.

• Legs (Figures 4.24a,e,f,i): Short and thick with (e.g., Flirtea) or without tubercles or smooth, long, and thin. Males of species from the Northern Hemisphere tend to have more powerful leg IV (mainly femur, but also tibia and patella, Figures 4.24e,f) than southern ones. Male coxa IV with small process on apex. Distitarsus I with three to four tarsomeres, II with three to five. Tarsi III–IV

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densely covered by short setae; claws III–IV parallel, smooth or pectinate (Figures 4.24l,m). • Genitalia (Figures 4.24p,q). Penis is standard gonyleptoid and very conservative, with rectangular ventral plate, puffed sac-glans, and well-developed thumblike dorsal process. Distal margin of ventral plate straight to concave. Dorsal group of setae is always present; ventral group of setae is lacking in several genera. Stylus is bent in the apex with a barbed crest of serrate projections in almost all species, sometimes is slender and cylindrical. A ventral process is present in some Venezuelan genera. Most knowledge on cosmetid genitalia is from Venezuelan (González-Sponga, 1992b), Cuban (Silhavy, 1966a) and Brazilian (Soares, 1974) species. Cokendolpher and Jones (1991) described the male genital system. • Color: Pattern of dorsal scutum, free tergites, and legs from reddish to blackish brown, with variable shapes of whitish, yellowish, or even greenish patches. These patches are made of wax over the exocuticle, produced by glands probably on the cuticle, and can be removed with scalpels or forceps. Metatarsus sometimes with darker ring patches. Rhaucus vulneratus (from Colombia) possesses blood-red stripes. • Sexual dimorphism: It may be present in the chelicerae swollen in males, or in femur and tibia IV thickened and with rows of similar spines in males. Some genera possess a male basitarsus I thickened. Females have genital operculum wider than in males. The males of the Brazilian species Roquettea singularis possess two pairs of immense protuberances on the scutum with unknown function. Subfamilies: Two subfamilies are currently recognized: Cosmetinae with smooth claws on tarsi III–IV, and Discosomaticinae with pectinate claws on tarsi III–IV. Ringuelet (1959) rejected this subdivision on the basis of the absence of characters other than armature of claws and the great external similarity of genera with and without pectinate claws. Cosmetinae is diagnosed by a symplesiomorphic state, and there is no indication whether pectinate claws arose only once, characterizing Discosomaticinae as a clade. Distribution: Cosmetidae is endemic to the New World. The peak of its diversity is in northern South America, Central America, and Mexico, where one-third to onehalf of harvestman species are represented by this single family. They are numerous in the Amazonian and Andean realms and also in the Caribbean. They also reach southward as far as Argentina and southern Brazil (Metalibitia). A few species inhabit the Brazilian Atlantic forest, mostly belonging to Metavononoides. A few species now in Vonones reach far northward into the USA, where they occur in many of the southern states. The majority of species seem to have restricted distributions. In a survey along the Venezuelan coast, only one species (Anduzeia punctata) occurred in three states (González-Sponga, 1992b), the other species being much more restricted. Cosmetids occur from sea level to altitudes as high as 4,150 m in Oligovonones brunneus (González-Sponga, 1992b).

Taxonomy

Relationships: Cosmetidae doubtless belongs to Gonyleptoidea, where it shows a superficial resemblance to Assamiidae. It was hypothesized by Kury (1992a) to be closest to Gonyleptidae, and this placement has not been refuted up to now. The extraordinary similarity of basal gonyleptids such as Metasarcinae (Kury, 1994a) and supposedly basal cosmetids such as Meterginus reinforces this hypothesis of relationship, mainly based on the saddle-shaped ocularium and penis structures. Main references: • Systematics: Roewer (1912a, 1923), Mello-Leitão (1932), Goodnight & Goodnight (1953a, 1976), González-Sponga (1992b), Kury (1994a, 2003). • Natural history: Parthasarathy & Goodnight (1958), Juberthie (1972), Goodnight & Goodnight (1976), Juberthie & Manier (1977), Cokendolpher & Jones (1991), Pinto-da-Rocha (1995b), Sabino & Gnaspini (1999).

Cranaidae Roewer, 1913 Ricardo Pinto-da-Rocha and Adriano B. Kury Etymology: Cranaus, from the Greek anthroponym Cranaus, the successor of Cecrops as king of Attica. Characterization: • Size: Body length 6–16 mm, leg IV 21–95 mm long. • Dorsum (Figures 4.25a,b,e,f,k): Widest at area II or groove III. Ocularium placed in the middle of the prosoma; rounded and high, with or without (some Prostygninae) median depression, small-tuberculate or with two high spines. Ozopores slitlike, one opening partially covered by a tubercle of coxa II. Area I divided (sometimes area II “invades” area I in the middle, as in Stygnicranainae and most Cranainae genera), normally with one tubercle on each side (most cranaines), and more elevated (Cranainae, except Puna); area II tuberculate; III with two spines upward or backward, rarely two round tubercles (Allocranaus). Tergite I normally small-tuberculate, with two spines (some Santinezia); II small-tuberculate, with two tubercles or one (Tripilatus); III normally with two spines, one large (Licornus and Thaumatocranaus) or smalltuberculate. • Venter: Coxa IV small-tuberculate or with two tubercles or spines close to the spiracular area in males (cranaines: Phareicranaus, Spinivunus and Santinezia, Figures 4.25a–e). Posterior margin of spiracular area with large unpaired apophyses in males of some cranaines (e.g., Alausius, Ventrifurca, Figures 4.25a,c). • Chelicerae: Segment I with few tubercles or densely tuberculate. • Pedipalps (Figure 4.25d,f): Short and heavy or elongate and thin (Stygnicranainae); pedipalp dorsally coarsely tuberculate from trochanter to tibia (except Cutervolus, Peladoius, Stygnicranainae). Femur small-tuberculate, with a row of dorsal tubercles (as in most Prostygninae), or with a dorsoapical stout

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Taxonomy

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tubercle (as in Phareicranaus and Santinezia). Setal sockets of tibia longer than setae; tarsus with two ventral rows of short and wide setae (Stygnicranainae). Legs (Figures 4.25b,k): With a few tubercles or spines (except prostygnines Cutervolus, Prostygnus and Yania). Coxa IV tuberculate, with a short and straight external apophysis. Femur IV straight or slightly S curved. Tarsal process strong, claws smooth or pectinate (Heterocranainae). Genitalia (Figures 4.25g–j): Stylus long and slender, straight with apex slightly swollen, ventral process of glans absent, dorsal process of glans rarely present. Ventral plate oblique in relation to the axis of the truncus, usually rectangular and robust, sometimes guitar shaped, apical border with V cleft or straight, rarely thin (Cutervolus); with distal group of one to six setae on each side and one to five median, no basal setae (except Cutervolus). Color: Normally brown to black greenish, legs sometimes lighter to yellowish. Some with white stripes on the lateral border (Acanthocranaus, Tryferus), on the scutal areas (Digalistes, Prostygnus), or on the median region, or with white circles on mesotergum and tergites (some Phareicranaus and Santinezia). White tubercles on lateral margin and areas (Cranaus, Neocranaus, some Phareicranaus). Sexual dimorphism: Carapace may be much larger in males of Prostygninae (Figure 4.25k) and Heterocranainae, reducing the size of area I and with a greater development of ocularium. Male chelicerae may be enlarged. Femur of pedipalps in males may be laterally flattened and with a dorsal (also ventral) spiny keel, while it is cylindrical and less spiny in females. Coxa IV of male may bear a pair of stout ventral apophyses near the spiracles in a few genera of Cranainae such as Santinezia. Armature of leg IV more conspicuous on males. Key to subfamilies

1. Carapace with strong sexual dimorphism (Figure 4.25k), better developed in male, squeezing space of area I. Area II not invading area I. Armature of mesotergum usually weak or absent, at most consisting of a pair of low spines in area III. Ocularium usually highly convex (Figures 4.25f,k). Area I unarmed. Femur IV never with distal prolateral spines. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 Figure 4.25. Cranaidae. (a) Ventrivomer ancyrophorus from Ecuador, male habitus in lateral view, showing the apophyses both of stigmatic area and of coxa IV (arrows). (b–c) Ventrisudis mira from Colombia, male habitus in dorsal and ventral views, showing the columnar apophysis of the stigmatic area and the straight femur IV with scattered spines. (d) Spinicranaus diabolicus from Ecuador, male pedipalp in mesal view, showing the dorsoapical apophysis and the coarse granulation of the patella and tibia (arrows). (e) Santinezia hermosa from Peru, male habitus in lateral view, showing the high and sharp spine on the ocularium and the mesotergal area III (arrows). (f) Yania metatarsalis from Ecuador, male habitus in lateral view, showing the strong dorsal and ventral spiny carinae of pedipalpal femur (arrow). (g–h) Tryferos elegans (male) from Ecuador, distal part of penis in dorsal and lateral views, showing the oblique ventral plate and the basal folds of the glans (arrows). (i–j) Prostygnus vestitus (male) from Venezuela, distal part of penis in lateral and dorsal views, showing the clearly marked dorsal process of glans (arrow) and the nonoblique ventral plate. (k) Yania sp. (Ecuador), male habitus in dorsal view, showing the greatly developed carapace squeezing the area I (arrow). Scale bars: e–f = 1 mm; g–j = 0.1 mm. Sources: a, d, Roewer (1923); b–c, Roewer (1963); e, Pinto-da-Rocha and Kury (2003b); f, Kury (1994b). Photo: A. Kury.

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. Carapace without sexual dimorphism, not affecting space of area I. Area II invading area I until touching the scutal groove (Figure 4.25b). Armature of mesotergum mostly present as very high and sharp spine. Ocularium mostly low and depressed in the middle. Area I usually with a pair of short spines. Femur IV with a few distal prolateral spines. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 2. Tarsal claws III–IV pectinate; rich ornamentation of scutum, mainly with contrasting white granules; all femora substraight and smooth elongate; scutal area III always with a pair of short spines . . . . . . . . . . . . . . . . . . . . . . Heterocranainae . Tarsal claws III–IV smooth; scutum remarkably smooth; femur IV short and sigmoid with tubercles all along (Figure 4.25k); scutal area III mostly unarmed, paired spines present only in a few species . . . . . . . . . . . . . . . . . . . . . Prostygninae 3. All pedipalpal segments, specially femur and patella, slender and much elongate, tibia/tarsus forming subchela. . . . . . . . . . . . . . . . . . . . . . . . . . . . . Stygnicranainae . Pedipalpal segments short (Figures 4.25d,e), tibia and tarsus not forming subchela . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cranainae Distribution: Mainly northern South America (except for two species in Panama and Costa Rica). Most of the diversity in the family (Colombia and Ecuador) seems to be related to the cloud forest, from 500 to 3,500 m high, where it merges with subparamo vegetation. Perhaps cranaids show a high endemicity related to small mountain areas, as do gonyleptids. Some species were recorded from páramos between 4,000 and 5,000 m where the soil is sandy and covered with low shrubs and grass, and others from the Amazonian rain-forest lowlands (Peru and Brazil) and upland rain forest (Venezuela and Colombia) where the vegetation is exuberant. Cranaids were also recorded from Peru, Bolivia, Brazil, Venezuela, and the Guyanas. Relationships: Kury (1994b) transferred Cranainae, Heterocranainae, Prostygninae, and Stygnicranainae from Gonyleptidae to Cranaidae and proposed it as the sister group to Cosmetidae + Gonyleptidae. He also proposed a close relationship between Cranainae and Stygnicranainae on the basis of the large and divergent spines on the ocularium and area II projecting into area I. Main references: • Systematics: Roewer (1923, 1932, 1943, 1963), Caporiacco (1951), Pintoda-Rocha & Kury (2003a). • Natural history: Pinto-da-Rocha & Kury (2003a), Machado & Warfel (2006).

Epedanidae Sørensen, 1886 Adriano B. Kury Etymology: Epedanus, from Greek êpedanós (weak, feeble).

Taxonomy

Characterization: • Size: Body of adults 2–5 mm long, 1.52–3 mm wide. Legs variable, adult legs I–IV: 5–15, 8–28, 5–20, 6–26 mm long. • Dorsum (Figures 4.26a,b): Opisthosomal scutum with sides straight, only a little wider than prosomatic carapace, posterior border substraight. Common ocularium may be absent (Dibuninae); when present, it is narrow, low, without depression, usually with strong median spine, seldom unarmed. In many species the scutal areas I–II are fused, a unique feature among Laniatores. Scutal areas with varied armature, usually unarmed or with a pair of acute high spines. Free tergites typically smooth and unarmed. • Venter: Sternum straight, widening and bifurcating a bit near genital operculum. Spiracles clearly visible. • Chelicerae (Figures 4.26c–o): Heavy with strong teeth in both fingers. Hand much swollen in male. • Pedipalp (Figures 4.26a,b,o): Coxa very long. Femur usually very elongate, may bear ventral rows of spines and sometimes dorsal tuberculation. Patella may be very long, widening abruptly distally. Tibia and tarsus with powerful ventroectal and ventrodistal spines. Claw extremely long, at least equal to tarsal length and applied against it. • Legs: Long and thin, especially tibia and tarsi I–II filiform. Coxa IV barely visible under scutum; femur I without ventral row of spines; IV unarmed, straight; tarsi III–IV with a pair of claws smooth or pectinate and with or without thick scopulae. Distitarsus I two- or three-segmented, II two- to foursegmented. Tarsal claws are extremely diverse: they may be angulated, possess a large basal lobe, or bear secondary mesal processes. • Genitalia (Figures 4.26p–q): Ventral plate of penis not sharply defined, with distal border concave or entire, setae arranged in a circle around the capsula interna; follis well developed, partially sunken into truncus. Structures of capsula interna more or less fused to each other. • Color: Most species are light brown with sparse black mottling. A few possess white patches on the scutum. • Sexual dimorphism: Cheliceral hand in males bulky and swollen, fingers thickened and strongly curved with varied processes. Pedipalps in males much more heavily spined. Key to subfamilies 1. Common ocularium lacking; eyes sessile, far removed from each other (Figure 4.26b). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Dibuninae . Eyes placed laterally at the base of a well-marked common ocularium (Figure 4.26a) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 2. Tarsi III–IV with dense scopula . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acrobuninae . Tarsi III–IV without scopula . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

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Taxonomy

3. Distitarsus I with three tarsomeres . . . . . . . . . . . . . . . . . . . . . . . . . . . Sarasinicinae . Distitarsus I with two tarsomeres . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Epedaninae Distribution: Epedanidae is endemic to Asia. Dibuninae is one of the dominant components of the opiliofauna of the Philippines. The other three subfamilies are more abundant in Indonesia, Thailand, and Malaysia. They also occur in Myanmar (Burma) and highlands of Nepal. There are a few records from Japan, southern China, and Vietnam. Relationships: Epedanidae was identified as the sister group of Gonyleptoidea in a cladistic analysis of Grassatores (Kury, 1993a). The loose structure of the glans and follis seems to support this view. Internal relationships of the four subfamilies have not been investigated. Main references: • Systematics: Roewer (1938), Suzuki (1969), Kury (1993a, 2003). • Natural History: Miyosi (1941).

Escadabiidae Kury and Pérez in Kury, 2003 Adriano B. Kury and Abel Pérez González Etymology: Escadabius, from type locality Escada, Pernambuco, Brazil, and Greek bios (living). Characterization: • Size: Dorsal scutum 2.5–3.5 mm long. • Dorsum (Figure 4.27a): Dorsal scutum campaniform, with sides straight, hourglass shaped in a few species. Ocularium small, with a few granules and sometimes a median spine. Mesotergum divided into four areas by straight transverse grooves, without relevant armature, area I longer than the others. • Venter: Sternites may be smooth and unarmed or with huge lateral projections (in Escadabius and Jim, Figure 4.27c). • Chelicerae (Figure 4.27a): Weak and not sexually dimorphic. Basichelicerite short, with well-marked bulla. • Pedipalps (Figures 4.27a,c): More or less as long as dorsal scutum. Without special modifications. Femur with two to three ventral setiferous tubercles, patella

Figure 4.26. Epedanidae. (a) Pasohnus bispinosus from Malaysia, male, habitus lateral (from Suzuki, 1976c). (b) Dibunus albitarsus from Philippines, male, habitus, lateral view, and detail of pedipalpus, mesal view (from Roewer, 1927). (c–n) Left chelicerae, frontal view, sample of diversity in the family (all from Roewer, 1938). (o) Takaoia sp. from Malaysia, pedipalpus and chelicerae, lateral. (p) Takaoia sp. from Malaysia, distal part of penis, dorsolateral. (q) Dibunus sp. from Philippines, distal part of penis, dorsolateral. Photos: o–p by D. Ubick, q by A. Kury.

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Figure 4.27. Escadabiidae. (a) Baculigerus sp. (Ceará), male habitus, dorsal view. (b) B. littoris (Bahia), male tibia II, lateral, showing modification. (c) Escadabius ventricalcaratus (Pernambuco), male coxa IV, stigmatic area and free sternites showing multiple falciform apophyses. (d) B. sp. (Ceará), coxa IV showing strong granulation and bifid apophysis (circle). (e) E. ventricalcaratus (Pernambuco), male habitus, lateral view. (f–h) B. sp. (Ceará), distal part of penis, views dorsoapical, ventral, and lateral, respectively. Photos: A. Kury.

Taxonomy

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with one mesal setiferous tubercle. Tibia and tarsus each with a row of a few ventromesal and ventroectal setiferous tubercles. Legs: All legs short and granulous. Coxa IV of male coarsely granulate, with dorsoapical apophysis made up of two subequal branches (Figure 4.27d). Its lateral border is parallel to the main axis of the body. Femora I–III straight, IV curved subbasally, strongly incrassate in males of Escadabius (Figure 4.27e). Tibiae I–II (Figure 4.27b) with differentiated porose distal area that may develop into a deep notch and/or a huge apophysis. Genitalia: Penis (Figures 4.27f–h) like that of the other “Samooidea”; it possesses a pair of rigid conductors and a reversible capsula interna. Ventral plate (Figure 4.27g) not defined, as in Gonyleptoidea. Pars distalis well separated from pars basalis by a constriction (absent in the Escadabius), with a ventral lamina apicalis that may be armed with small lateral spines. Pars distalis with a ventral keel-shaped protuberance (Figure 4.27h). Pair of well-developed rigid conductors that do not sink deeply into the glans socket (Figure 4.27f,h); conductors are vestigial in Escadabius. Stylus is very large and apically surrounded by a well-developed hornlike parastylar collar (Figure 4.27f). Color: Background light to dark brown, with more or less intense yellow mottling; legs may be ringed. The preserved specimens of Escadabius are yellowish. Body and appendages are pale yellow in the troglobite species. Sexual dimorphism: Male and female are remarkably uniform in chelicerae, pedipalps, armature, and legs, except for the tibiae I and II, which only in males bear a bulky distal region, distinguished by different color and granulation, that may develop into a notch and may extend forming a strong process. In a few species (e.g., genus Escadabius), the free sternites of males bear greatly developed spiniform apophyses, while those of females are unarmed.

Distribution: Neotropics, Brazilian endemism. Originally the family was restricted to the coastal margin of the Brazilian states of Pernambuco and Bahia, but with all unpublished records (including Spaeloleptes new familial assignment) the distribution should be expanded to the coast of Ceará State and caves in the dry central part of the state of Minas Gerais, where the cavernicolous escadabiids could represent an example of relictual distribution. Relationships: Some genera were included in the matrix of Laniatores of Kury (1993a), grouped with Kimulidae (Samooidea). A possible sister-group relationship of both families is based on the presence of an incrassate femur IV in males and penial characters: clear division between pars distalis and pars basalis, ventral keel in pars distalis, and the presence of an apparently homologous small parastylar collar. Two species groups can be recognized in Escadabiidae: (1) The Escadabius species group is characterized by the dorsal scutum clearly campaniform and strongly convex, femur IV strongly incrassate, and sternites with large lateral falciform projections in males; penis without setae and conductors very small; pars distalis not separated from pars ventralis by a groove; lamina apicalis of pars distalis weakly developed. (2) The other group includes the remaining genera. They are characterized

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by more variable habitus body shape from hourglass to campanifom, sternites poorly armed or unarmed, and femur IV not enlarged in males, but with tibia I or II (or both) modified in a warty or saddle-shaped mound. The penis has small setae and conductors well developed; pars distalis separated from pars ventralis by a groove; lamina apicalis of pars distalis well developed. Recifesius pernambucanus is included in the second group because of the clear division of pars distalis and pars basalis. Main references: • Systematics: Roewer (1949), Soares (1978, 1979).

Fissiphalliidae Martens, 1988 Ricardo Pinto-da-Rocha Etymology: Fissiphallius, from Latin fissus (split) and Greek phallos (penis). Characterization: • Size: Dorsal scutum 2.0–3.3 mm. Leg IV 3.1–8.6 mm. • Dorsum: Body trapezoidal, mesotergum higher than prosoma. Ocularium close to anterior border, narrow with two tubercles or one large spine. Four areas on dorsal scutum; I–IV and posterior margin smooth or with small tubercles; I undivided; grooves I–IV “V” shaped (Figure 4.28a) or straight (Figure 4.28b). Free tergites with one long tubercule or small-tuberculate. Anal opercle tuberculate, or with one or three larger tubercles. • Venter: Genital opercle larger or shorter than spiracular area. • Legs: Legs straight, short, tuberculate; IV with larger tubercles in some males. Coxa IV anterior (near grooves II–IV), small-tuberculate or with pointed tubercles. Femur and tibia with some larger tubercles apicad, never longer than segment width. Tarsal formula: 3–4(2):5–7(3):5:5. Claws smooth and subparallel. Tarsal process and scopulae absent. • Chelicerae: Similar in both sexes; bulla well defined, smooth or smalltuberculate. • Pedipalps: Short, thick, femur with two basal long and one subapical mesal setae, patella with one mesal seta, tibia and tarsus with ectal-mesal setae. • Genitalia (Figure 4.28c): Truncus with a long rutrum and a dorsal plate called a stragulum opposite each other; both protect the long, straight, and slender stylus. An inflatable vesicle is on the base of the stylus and allows it to overcome the length of the rutrum to reach the feminine pore. Ventral plate with two to three pairs of setae on venter of distal half, pergula on median region with two to four pairs of setae. • Color: Varies from yellowish to pale brownish with or without brown stripes or dots on dorsal scutum and free tergites. • Sexual dimorphism: Males show larger tubercles on trochanter to tibia (mainly on leg IV), free tergites, and anal opercle. Females have body and legs smaller than males. Male of F. martensi has a swollen area on venter of tibia II, perhaps a glandular region.

Taxonomy

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Figure 4.28. Fissiphaliidae and Guasiniidae. (a–c) Fissiphaliidae: (a) habitus of Fissiphallius sturmi; (b) habitus of F. martensi; (c) penis of F. martensi. (d–i) Guasiinidae: (d) habitus dorsal of Guasinia delgadoi; (e, i) penis; (f) mesal view of chelicera of G. persephone; (g) pedipalp; (h) habitus lateral. Scale bars: b = 1 mm; c = 0.05 mm; f–g = 0.5 mm; h = 500 ␮m; i = 20 ␮m. Sources: a, Martens (1988); b–c, Pinto-da-Rocha (2004); d, González-Sponga (1997); e–g, i, Pinto-da-Rocha and Kury (2003b).

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Distribution: Recorded from the highlands (3,250–3,700 m) of Bogotá (Colombia) and lowlands of central and eastern Amazon rain forest. Relationships: Kury and Pérez G. (2002) stated that Fissiphalliidae could form a monophyletic group with Zalmoxidae, or it could be a group within Zalmoxidae, on the basis of the tagmosis of the ventral plate divided by a setose median pergula and the presence of a stragulum (= capsula externa). These families are related to Guasiniidae and Icaleptidae (Pinto-da-Rocha & Kury, 2003b) by the presence of a stragulum. Main references: • Systematics: Martens (1988), Pinto-da-Rocha (2004). • Natural history: Martens (1988).

Gonyleptidae Sundevall, 1833 Adriano B. Kury and Ricardo Pinto-da-Rocha Etymology: Gonyleptes, from Greek gony, joint, knee, and leptos, thin, fine, delicate. Characterization: Gonyleptidae is one of the most diversified families of Opiliones, not only in number of species but also in morphological disparity and coloration patterns; the variation is large in most structures. • Size: Small (Tricommatinae) to large (Gonyleptinae, Pachylinae, and Goniosomatinae); body length from 0.6 (male of Berlesecaptus convexus, Tricommatinae) to 17 mm (male of Sadocus ingens, Pachylinae); leg IV length from 2 (Berlesecaptus convexus) to 185 mm (male of Mitobates triangulus, Mitobatinae). • Dorsum: Carapace much narrower than opisthosomal scutum in most species (Figures 4.29a,c–g) except some Tricommatinae, the caelopygine Thereza (Figure 4.29b), the Metasarcinae, and the mitobatines Mitobates, Mitobatula, and Ruschia, which present a subrectangular body; Ampheres shows almost triangular body shape; some genera of Tricommatinae have ovoid outline (Figure 4.29i). Frontal hump present except in Ampycinae; with tubercles short or long (Hernandariinae). Dorsal scutum normally longer than wide except in Cobaniinae (Figure 4.29g) and some Pachylinae such as Discocyrtus and Sadocus. With one or two ozopores on each side, sensorial pegs present in Goniosomatinae, Bourguyiinae, and some Pachylinae. Body depressed in Bourguyiinae, convex in most other gonyleptids. Common ocularium always present, normally on middle of carapace, sometimes near the anterior margin of scutum, normally convex, except in Bourguyiinae and some genera of Tricommatinae and Metasarcinae, in which it is flattened; armature ranges from absent, with one or two tubercles, to one or two straight apophyses (apex acuminate or blunt), a few species with curved spine directed frontward or straight inclined frontward. The armature of scutal areas and free tergites is

Taxonomy

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Figure 4.29. Gonyleptidae. Dorsal habitus of males: (a) Mitobatinae, Promitobates ornatus; (b) Caelopyginae, Thereza speciosa; (c) Goniosomatinae, Acutisoma unicolor; (d) Gonyleptinae, Neosadocus sp.; (e) Sodreaninae, Gertia hatschbachi; (f) Pachylinae, Discocyrtus sp.; (g) Cobaniinae, Cobania picea; (h) Hernandariinae, Piassagera brieni; (i) Tricommatinae, Rezendezius lanei. Photos: R. Pinto-da-Rocha.

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•

extremely variable, from smooth to armed with one or more tubercles or spiniform processes; the sculpture of the body is finely granular in most species. Area III often armed. Lateral margin of Gonyleptinae normally with a row of large and blunt protuberances. Three or four areas on dorsal scutum; sulci well marked; area I divided by median groove except in Tricommatinae; IV rarely divided. Posterior margin (“area V”) may be armed with one or a pair of tubercles. Free tergites with long tubercles on the lateral angles in most Heteropachylinae and some females of Goniosomatinae; tergites II–III with median tubercle always present in Bourguyiinae and females of some Gonyleptinae (Sphaerobunus), and I–II or III conspicuously armed with apophyses in several Pachylinae. Venter: Posterior margin of spiracular area deeply concave in most Progonyleptoidellinae, Gonyleptinae, and Pachylinae. Free sternite I (= sternite IV) may be projected in complex lobes matching the apophyses of coxa IV of males in Tricommatinae. Chelicerae: Similar in size in both sexes and small in relation to the body size except in Metasarcinae, where the male possesses segment II hypertelic; bulla of segment I (basichelicerite) often with low dorsal or marginal tubercles. Fingers with teeth of variable sizes. Pedipalps: Femur longer than dorsal scutum in Sodreaninae (Figure 4.29e), cylindrical in Sodreaninae, Caelopyginae, and Progonyleptoidellinae, laterally compressed in others; with row of thick ventral setae on Metasarcinae, Ampycinae, and Goniosomatinae. Some genera of Tricommatinae with stridulatory rack basally on the inner surface. Patella long in Sodreaninae; with mesal setae in Goniosomatinae and Metasarcinae. Tarsus ventrally straight in most groups, convex in Caelopyginae, Progonyleptoidellinae, Hernandariinae, and Sodreaninae; with short and long ventral setae on tibia and tarsus; also with two median ventral rows of short and thick setae in mentioned groups, but thin setae in Gonyleptinae, Goniosomatinae, and some Pachylinae; claw long and curved, almost same length as tarsus. Legs: Coxa IV dorsally visible in entire extension (Figure 4.29d) except in Metasarcinae, Heteropachylinae, and Progonyleptoidellinae; with dorsoapical apophysis short to robust, single or bifid, much more developed on males, normally directed laterad, sometimes backward; sometimes also with internal apophyses. Trochanter, femur, and tibia IV armed with tubercles/apophyses in males of most groups in countless shapes and arrays, except Mitobatinae (Figure 4.29a), Bourguyiinae, and some Tricommatinae (Figure 4.29i); femur IV with dorsobasal apophysis in Heteropachylinae, Pachylospeleinae, Gonyleptinae, and some Pachylinae. Male femur IV ranging from straight (much elongated in Mitobatinae) to sigmoid or sinuous. Apex of femur and tibia sometimes slightly incrassate in males. Tarsal process either absent (most Tricommatinae), reduced to long setae on a well-developed socket, or well developed as claws. Scopulae on legs III–IV present in most groups except some Pachylinae and Mitobatinae. Claws smooth in most members of the family,

Taxonomy

pectinate in tree-dwelling taxa such as Caelopyginae, Heteromitobates discolor (Goniosomatinae), and Parampheres (Gonyleptinae). Tarsal formula: from low in Tricommatinae (3:3:4:4), with cylindrical tarsomeres, to high in Progonyleptoidellinae (7:17:15:20), with globular tarsomeres. Male basitarsus normal to inflated (presumably with associated gland). • Genitalia (Figures 4.30a–i): Penis with ventral plate well defined, rectangular or pyriform with basal lobes more or less developed in most subfamilies (extremely developed in Gonyleptinae-like subfamilies; see Figures 4.30e,i), basal lobes lacking in Heteropachylinae, Goniosomatinae (Figure 4.30a, ventral plate rectangular), Cobaniinae (Figure 4.30g, ventral plate trapezoid), and Ampycinae (Figure 4.30b, ventral plate ovoid). In Metasarcinae ventral plate provided with a pair of spiny laterobasal sacs. In Tricommatinae ventral plate with regionalization in a swollen basal part and a distal lamina parva (Figure 4.30f). Lateral margin of ventral plate with two groups of setae, extremely variable in size and shape. Distal margin of ventral plate entire or with a wellmarked parabolic, U-shaped or V-shaped cleft (Figures 4.30e,i); in some cases the cleft is very deep, dividing the plate into two valves (Figure 4.30b, Ampycinae). Apical setae may be straight or helicoidal, sometimes very elongate (e.g., in some Bourguyiinae, Figure 4.30d). Glans columnar, more or less elongate, rarely with thumblike dorsal process (Figure 4.30g), much more frequently with ventral process, which may be digitiform or flabelliform or adopt a variety of shapes in Pachylinae. Ventral and dorsal processes only occur together in the Bourguyiinae and Parabalta (Pachylinae). Stylus usually elongate and straight, but in many species it is short and thick, bent in the apex, with a varied covering of granules and small apophyses. • Color: Extremely variable, from brownish (most Pachylinae, Metasarcinae, Tricommatinae) to black (most Gonyleptinae, Ampycinae, Cobaniinae, Hernandariinae) in most species, but some groups (Bourguyiinae, Caelopyginae, Progonyleptoidellinae, and Sodreaninae) with very colorful patterns (yellowish, orange, greenish), some of them with lighter or darker patches or spots on the integument; apparently the yellowish or whitish patches are waxy and are deposited over the integument. Most Goniosomatinae and many Pachylinae possess lighter color over sulci I–IV; some waxy patches are visible only in living or dried preserved specimens; arthrodial membranes of coxae and trochanters are sometimes pink to purple colored. • Sexual dimorphism: Coxa IV of males is much wider and strongly developed, clearly visible under the scutum in dorsal view, while that of females is much smaller and often hidden under the scutum borders. In general, males have more and higher tubercles and/or apophyses on leg IV; sometimes the leg is thicker and more curved than in females. In pachyline-like species males can bear tubercles or apophyses (currently of diagnostic value) that are smaller or even lacking in females; sometimes the situation is just the opposite. Males of Bourguyiinae, some Tricommatinae (such as Pseudopachylus and Camarana), and especially Mitobatinae have a very elongate straight femur and tibia IV.

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Figure 4.30. Gonyleptidae. Distal part of penis: (a) Goniosomatinae, Acutisoma ensifer; (b) Ampycinae, Ampycus telifer; (c) Heteropachylinae, Pseudopucrolia mutica; (d) Bourguyiinae, Bogdana ingenua; (e) Progonyleptoidellinae, Cadeadoius niger; (f) Tricommatinae, Pseudopachylus longipes; (g) Cobaniinae, Cobania picea; (h) Pachylinae, Discocyrtus testudineus; (i) Sodreaninae, Zortalia inscripta. Photos: a, M. B. da Silva; b–i, R. Pinto-da-Rocha.

Taxonomy

Iporangaia has an unusual dimorphism on metatarsus IV, which has the calcaneus swollen. Many Pachylinae have basitarsus I thickened in males. Metasarcinae males possess an enlarged chelicera. In most species of Progonyleptoidellinae the spines of the mesotergum are present as low rounded tubercles in males and high pointed spiniform processes in females. Key to subfamilies 1. Pedipalpal femur with row of strong spines on ventral surface; pedipalpal patella usually with mesal subdistal spine . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 . Pedipalpal femur without row of strong spines on ventral surface; pedipalpal patella unarmed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 2. Area II invading area I up to scutal groove; ocularium without median depression (Figure 4.29c) (Southern and southeastern Brazil). . . . . . . . . . . Goniosomatinae . Area II not invading area I (groove II does not touch groove I); ocularium with median depression (Peru, Bolivia, and Argentina) . . . . . . . . . . . . . . Metasarcinae 3. Pedipalpus at least twice as long as body, femur very long and slender; often scutal grooves underlined in white (Figure 4.29e) (southern and southeastern Brazil). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sodreaninae . Pedipalpus shorter or nearly as long as body, femur more or less robust; scutal grooves not underlined in white . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 4. Tarsi III–IV with high count (usually above 12) of globular tarsomeres; pedipalpal tarsus long with ventral surface convex, provided with double row of setae; distitarsus II with 4–6 tarsomeres . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 . Tarsi III–IV with low count (below 10, usually 6–7) of cylindrical tarsomeres; pedipalpal tarsus short, with ventral surface flattened without double row of setae; distitarsus II with 3 tarsomeres (rarely 4–5) . . . . . . . . . . . . . . . . . . . . . . . . . . 6 5. Tarsal claws III–IV pectinated; coxa IV of males appearing under scutum in dorsal view (Brazilian Atlantic forest) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Caelopyginae . Tarsal claws III–IV smooth; coxa IV of males hidden under scutum in dorsal view (Brazilian Atlantic forest). . . . . . . . . . . . . . . . . . . . . . . . . . . Progonyleptoidellinae 6. At least one free tergite of male fused to opisthosomal scutum or all tergites fused among them (Brazilian Atlantic forest, north of Espírito Santo) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Heteropachylinae . No tergite fused, all of them actually free in both sexes . . . . . . . . . . . . . . . . . . . . . . 7 7. Ocularium as a high cone on the anterior margin of carapace with a hook at the apex. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 . Ocularium as an ovoid variedly armed with spines and apophyses, but never with hook . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 8. Coxa IV of male clearly surpassing scutum. . . . . . . . . . . . . . . . . Pachylinae (part) . Coxa IV of male hidden under scutum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

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9. Frontal margin of carapace unarmed; femur IV of male dimorphically elongate. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Tricommatinae (part, e.g., Pseudopachylus) . Frontal margin of carapace with strong apophyses below paracheliceral projections; femur IV without dimorphism, short in both sexes (southeastern Brazil). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Gonyassamiinae 10. Scutal area I often undivided; tarsus III–IV without tarsal process; distitarsus I two- or three-segmented. . . . . . . . . . . . . . . . . . . . . . . . . . . . Tricommatinae (part) . Scutal area I almost always divided into left and right halves; tarsus III–IV with tarsal process; distitarsus I three- (rarely four-) segmented. . . . . . . . . . . . . . . . . 11 11. Femur IV dimorphically elongate, much longer in male, with armature very weak or absent in both sexes (Figure 4.29a) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 . Femur IV with other manifestations of sexual dimorphism, usually more curved and/or with more spines on male . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14 12. Ocularium with paired armature; area III usually with a pair of spines or tubercles; femur IV entirely straight and unarmed (Figure 4.29a), posterior ozopore absent or much smaller than anterior ozopore (Brazilian Atlantic forest). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Mitobatinae . Ocularium unarmed or with paired armature; area III unarmed; femur IV with weak distal armature, posterior ozopore present, of the same size as anterior ozopores. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13 13. Coxa IV with apical outer apophysis bifurcate with subequal branches; ocularium low and wide, unarmed or with a median hemispheric tubercle; base of femur IV always unarmed; distitarsus II three-segmented (Brazilian Atlantic forest) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Bourguyiinae . Coxa IV with apical outer apophysis bifurcate with very unequal branches; ocularium high, narrow, unarmed; base of femur IV with rows of tubercles; distitarsus II four- or five-segmented (São Paulo) . . . . . . . . . . . . . . Pachylospeleinae 14. Frontal hump of carapace armed with two spines or acute tubercles . . . . . . . . 15 . Frontal hump of carapace unarmed. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16 15. Pedipalpal tarsus flattened ventrally; ocularium never with geminated armature (eastern Brazil, Argentina) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Gonyleptinae . Pedipalpal tarsus biconvex; ocularium with two tubercles united apically (Southern Brazil, Argentina, Paraguay) . . . . . . . . . . . . . . . . . . . Hernandariinae 16. Coxa IV strongly projected laterally, making the body much wider than long; integument glossy black (Figure 4.29g) (Southeastern Brazilian highlands). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cobaniinae . Coxa IV moderately projected, body at most slightly wider than long, integument dark yellow to dark brown (rarely black), leatherlike. . . . . . . . . . . . . . . . . 17 17. Body covered with protuberances; coxa IV with powerful uniramous apophysis in male; trochanter IV with weak tubercles; ocularium armed with two cones

Taxonomy

oblique frontward or unarmed, never with unpaired armature; free tergites (at least the third) with strong median spine (Amazonia) . . . . . . . . . . . . Ampycinae . Body smooth or with setiferous tubercles; coxa IV with apophysis recurved (Figure 4.29f) and mostly bifid in male, often pointed posteriorly; trochanter IV often with powerful recurved apophyses; ocularium with unpaired armature (sometimes in hook) or two erect spines; free tergites with variable armature, commonly weak . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pachylinae Distribution: Recorded from southern South America (including Falkland Islands) to Costa Rica, with one isolated record from Guatemala. The highest diversity is found in southern Chile, Brazilian coastal forests, and the Andes up to Peru. They are rare in Amazonia and the Andes of Ecuador and Colombia. Seven subfamilies are endemic to the Brazilian coast: Caelopyginae, Sodreaninae, Goniosomatinae, Pachylospeleinae, Gonyassamiinae, Progonyleptoidellinae, and Bourguyiinae. The majority of the diversity of the Hernandariinae and Tricommatinae also occurs in this environment. The degree of endemism is highly dependent on the terrain; species of gonyleptids associated with mountain ranges show a marked trend to occupy restricted areas, whereas species from flatter areas possess much wider distributions. Gonyleptids are rare and little diversified in xeric vegetation formations in Pantanal, Cerrado, and Caatinga. In the Chaco the environment varies, and gonyleptids thrive in the humid parts. However, central Argentina (semiarid vegetation of mountains of Córdoba and humid vegetation of Yungas in the northwest) and the temperate forests—called Bosque Valdiviano—of Chile harbor an impressive number of endemic species. Metasarcinae is exclusive to the Andean and sub-Andean realms (see Acosta, 2002b). Relationships: Gonyleptidae is the sister group to Cosmetidae, and both are related to Stygnidae and Cranaidae (Kury, 1992b). The family seems to be monophyletic on the basis of several characters, including the presence of a frontal hump on the carapace, a well-developed coxa IV, dorsal process of glans lost and ventral process present, two pairs of ozopores, chelicera not dimorphic, and opisthosomal scutum much wider than prosomal scutum. However, not all of these characters are present in all members of the family. The relationships among gonyleptid subfamilies are poorly understood, although most of the subfamilies seem to be monophyletic, perhaps with the exception of the two most diverse subfamilies, Pachylinae and Gonyleptinae. Main references: • Systematics: Roewer (1923), Mello-Leitão (1932), Ringuelet (1959), Pintoda-Rocha (2002), Kury (2003), Pinto-da-Rocha et al. (2005). • Natural history: Muñoz-Cuevas (1971a), Matthiesen (1983), Acosta et al. (1993, 1995), Gnaspini (1995, 1996), Machado & Oliveira (1998, 2002), Elpino-Campos et al. (2001), Machado & Raimundo (2001), Machado (2002), Pérez G. & Kury (2002), Mestre & Pinto-da-Rocha (2004), Pereira et al. (2004).

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Guasiniidae González-Sponga, 1997 Ricardo Pinto-da-Rocha Etymology: Guasinia, from Guasina, an island in the delta of the Orinoco River, Venezuela. Characterization: • Size: Body length about 1.4 mm. • Dorsum (Figures 4.28d,h): Body slightly constricted at groove I, densely covered by tubercles. Ocularium close to anterior border and with no vestige of eyes. Grooves II–V parallel and unarmed. Free tergites unarmed. • Venter: Spiracles close to coxae IV and distant from posterior margin. • Legs: Trochanter clublike (Figure 4.28h). Tarsal formula: 3–4(2–3):4–12(2– 4):5:5–6. Claws smooth and subparallel. Tarsal process absent. • Chelicerae: Similar in both sexes; segment I smooth or with small dorsal tubercles. Stridulatory organ on Guasinia persephone (Figure 4.28f). • Pedipalps (Figure 4.28g): Short and thick; femur depressed with ventral and prolatero-subapical tubercles; tibia and tarsus as long as the femur, with setae reduced, without socket and similar to hair. • Genitalia (Figures 4.28e,i): Ventral plate modified as apical portion of truncus separated from the shaft by a constriction. Lateral margins of ventral plate twist around the main axis of the truncus and are fused to each other, resulting in a funnel-shaped calyx. There are two groups of setae in the ventral plate, the basal group with large foliaceous-spatulate setae, the distal group with small cylindrical acuminate setae. Distal portion of truncus proximal to ventral plate depressed, forming a cavity where glans structures are inserted. Capsula externa well developed as a membranous sac projected into two paired lobes (titillators). Capsula interna absent, stylus free. • Color: Yellowish; some appendages may be depigmented. • Sexual dimorphism: Without a pattern in the described species, shown by larger tubercles on trochanter to tibia IV of males, or segmented male metatarsus II or smaller number of tubercles. Distribution: Venezuela (states of Bolivar and Delta del Amacuro) and Brazil (state of Amazonas). Relationships: The presence of a well-developed capsula externa of the penis arising from a distal depression of the truncus and projecting into two titillators instead of being a solid plate articulated with the truncus relates Guasiniidae to Biantidae, Kimulidae, and Stygnommatidae, which form the superfamily Biantoidea sensu Kury and Pérez G. (Pinto-da-Rocha & Kury, 2003b). The penis differs from that of the other biantoids in lacking the tubular conductors flanking the stylus. The short pedipalpal claw, tarsus twice as long as tibia, and tarsus with reduced ventral setae are autapomorphies of the family.

Taxonomy

Main references: • Systematics: González-Sponga (1997), Pinto-da-Rocha & Kury (2003b). • Natural history: Pinto-da-Rocha & Kury (2003b).

Icaleptidae Kury and Pérez G., 2002 Adriano B. Kury and Abel Pérez González Etymology: Icaleptes, from Ica, a Chibchan people who inhabited the slopes of Sierra Nevada de Santa Marta, and leptes, a truncation of the generic name Gonyleptes, the first laniatorean to be described. Characterization: • Size: Dorsal scutum 3.0–3.3 mm long. Femora I–IV 0.6–0.8 / 0.8–1.1 / 0.6– 0.8 / 0.8–1.6 mm. • Dorsum: Ocularium well developed (Figure 4.31b), large, unarmed; frontal border of ocularium arises directly from frontal margin of carapace, forming a straight profile like a wall (Figures 4.31a,c), perpendicular to the main axis of the body. Frontal hump of carapace absent. Scutum unarmed, free tergites and sternites unarmed or with transverse row of small tubercles (Figure 4.31d). Mesotergal areas unarmed, either well marked or not defined. • Venter: Free sternites I–V each with a transverse row of minute setiferous tubercles or with a median cluster of small granules forming a stripe. Anal operculum smooth. • Chelicerae: Weakly developed, basichelicerite short with well-marked bulla, hand small. No sexual dimorphism. • Pedipalps (Figures 4.31a,c): Segments short and stout with short and delicate setiferous tubercles. • Legs: Trochanter IV of male with inner distal or subdistal apophysis. Femur IV of male with row of prolateral spines (Figures 4.31a,c). Tarsal formula: 3– 4(2):6–7(3):5:6. Coxa IV with ventral inner spiniform apophysis surmounting the spiracles. • Genitalia (Figures 4.31e–h): Ventral plate not divided into regions. Stragulum (see Zalmoxidae) short, wide, with well-developed lateral lobes, articulated to the truncus like a jackknife. Capsula interna simple, with small parastylar collar formed by two lobes (unknown in Zalmopsylla). Lamina ventralis not covering the stragulum laterally, armed with three pairs of powerful spatulate setae and longitudinal ventrodistal rows of small acuminate setae. • Color: Dark yellow background with varied darker mottling. • Sexual dimorphism: Strong dimorphic leg IV, male coxa IV ventrally inserted, which causes leg IV to be positioned under the body, as in a flea (Figures 4.31a,c,d), laterally inserted in females as in most Laniatores. Distribution: Hitherto only recorded from Ecuador (Cotopaxi) and northern Colombia (Sierra Nevada de Santa Marta), but likely to occur also in Venezuela.

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c

a

d b

e

f

g

h

i

j

k

l

Figure 4.31. Icaleptidae and Kimulidae. (a–h) Icaleptidae. (a) Icaleptes malkini, male (Colombia), Habitus lateral. (b) I. malkini, male (Colombia), ocularium, frontal. (c) Zalmopsylla platnicki, male (Ecuador), habitus, lateral. (d) Z. platnicki, male (Ecuador), free tergites and sternites, posterior view. (e–g) Z. platnicki, male (Ecuador), distal part of penis, dorsal, lateral, and ventral views. (h) I. malkini, male (Colombia), distal part of penis, dorsal view. (i–l) Kimulidae. (i) Minuella dimorpha male (from Venezuela), habitus dorsal (from González-Sponga, 1987). (J) Minuella sp. (from Venezuela), penis, distal part, laterodorsal. (k) Kimula elongata (from Puerto Rico), penis, distal part. (l) Metakimula sp. (from Cuba), penis, distal part. Scale bars: a–d = 1 mm; g–h = 0.1 mm. Figures: Kury & Pérez G. (2002). Photos: A. Pérez González. Abbreviations: as = acuminate setae; pl = parastylar lobes; ss = spatulate setae; St = stragulum.

Taxonomy

Relationships: González-Sponga (1987) described some “phalangodids” under the genus Phalangodinella, currently in Zalmoxidae (Kury, 2003), that show some degree of rotation of the insertion of leg IV and a large ocular tubercle. A more detailed study of their phylogeny will tell if the “flea leg” is synapomorphic for Icaleptidae and could lead to a broader concept of the family. The phylogenetic relationships of Icaleptidae have never been explored. The family forms part of Zalmoxoidea, characterized by the stragulum, which may be formed by the fused conductors articulated to the truncus like a jackknife. Kury and Pérez G. (2002) considered Icaleptidae to be closely related to Zalmoxidae and Fissiphalliidae. Guasiniidae was also considered to be related to Zalmoxoidea (Pinto-da-Rocha & Kury, 2003b). The penis of Guasiniidae shows affinities with that of Icaleptidae, possessing a wide stragulum, three pairs of powerful spatulate setae, and small acuminate setae distally in the lamina ventralis; the distal calyx seems to be synapomorphic for Guasiniidae. This hypothesis needs to be tested in the future. Main references: • Systematics: Kury & Pérez G. (2002).

Kimulidae Pérez González, Kury, and Alonso-Zarazaga, new name Abel Pérez González and Adriano B. Kury Nomenclatural note: Minuidae, as based on an invalid generic name, is also invalid and, as such, needs a replacement (M. Alonso-Zarazaga, pers. comm., 2003). The following nomenclatural acts are therefore recommended: Minuella Roewer, 1949 which is the oldest junior synonym available for Minua, takes precedence, forcing restoration of all species combined under Minua. Kimulidae Pérez Gonzalez, Kury & Alonso-Zarazaga nomen nov. is established to replace Minuidae. The type genus is Kimula Goodnight & Goodnight, 1942. Minuidinae Mello-Leitão, 1933 would be a family-group name available for replacing Minuidae, but according to our research, Minuides Sørensen, 1932—the type genus of Minuidinae—should be included in Zalmoxidae. Etymology: Unknown. Characterization: • Body: Dorsal scutum bell shaped (Figure 4.31i), with laterals of carapace convex. Opisthosomal scutum widest at groove II and slightly constricted at area III or IV (Tegipiolus without any constriction). Opisthosomal scutum outline in lateral view high, but somewhat flattened, not rounded convex. Ocularium prominent, granular, armed with a medial spiniform apophysis erect or curved or sinuous or inclined anteriorly. In Tegipiolus the basis of the ocular tubercle is very broad and thick. Mesotergum with four areas, area I longer than the others. In the species of Metakimula the sulcus II is effaced on the sides or even entirely lacking. Mesotergal areas typically densely granular but un-

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armed; in a few species area I possesses a pair or a transverse row of pointed tubercles. Lateral margin of scutum may have enlarged spiniform tubercles, larger at area II. Free tergites with pointed corners or unpaired median apophyses. Free sternites may bear varied armature, rows of spines or unpaired spines. Chelicerae: With well-marked bulla and without remarkable armature. Pedipalps: Setiferous tubercles never strongly developed. Femur convex dorsally with ventral and dorsal scattered setiferous tubercles, group of two basal setiferous tubercles with the basalmost tubercle always much reduced and always with mesal subdistal setiferous tubercle. Patella with one mesal subdistal setiferous tubercle. Tibia a little elongate, usually longer than tarsus, marginated with lateroectal and lateromesal rows of two to seven setiferous tubercles. Tarsus with lateroectal and lateromesal rows of three to four setiferous tubercles. Legs: III–IV without tarsal process and scopula. Male coxa IV well developed, visible under scutum in dorsal view, roughly armed with heavy granules or acute tubercles; trochanter IV has a characteristic ventral spine, and the femur is very incrassate, with a ventral row of strong spiniform apophyses; tibia and metatarsus are roughly tuberculate, and at their apices they have very enlarged and globose ventral tubercles. Tarsal formula: 4(2):6– 13(2):5:5–6 (except in Fudeci, 3:5:5:5). Genitalia: Truncus cylindrical without a well-defined ventral plate, as in Gonyleptoidea. Pars distalis well differentiated from the pars basalis by one sulcus (Figures 4.31j–l) or the border between both, easily recognizable by the upper limit of the pars basalis striate area. Pars distalis laterally armed with three or four strong spatulate spines (Figures 4.31j–l), in some species lanceolate (e.g., Kimula, Metakimula) (Figures 4.31k,l), in others rounded (e.g., Kimula cokendolpheri, Tegipiolus pachypus) and ventrally with four small acute setae. The pars distalis has a very peculiar form, apparently synapomorphic for the family, with the lamina ventralis surrounding the capsula interna (conductors + stylus). The apical extremes of the lamina ventralis are enlarged, fingerlike, touching one another dorsally, the apical region of the pars distalis commonly with two folds that can be ventrally entire or divided (Figure 4.31h). With two rigid conductors that could be lamelar (as in Kimula and Metakimula) (Figures 4.31k,l) or greatly developed and enlarged (as in Tegipiolus). In Kimula spp. and Metakimula the stylus has a small subapical sheet that could be interpreted as a parastylar collar (Figures 4.31k,l). The genitalia of the species of Minuella and Fudeci curvifemur are rudimentarily illustrated (González-Sponga, 1987); this fact is a considerable limitation for a detailed interpretation of the genitalic features, but the drawings are sufficient for identifying the family genitalic ground plan. Color: Typical of soil- and litter-dwelling harvestmen. Body brown; the chelicerae, pedipalps, legs, and prosoma bear yellowish patches and in some aspects appear reticulated. Troglobite species show a uniform light brownish orange.

Taxonomy

• Sexual dimorphism. Male leg IV: Trochanter and/or femur IV may be incrassate or strongly curved, tibia and metatarsus IV enlarged and roughly tuberculate. Free sternites with lateral apophyses. Female smaller. In females of Kimula cokendolpheri the trochanter IV has a ventrodistal spine rather than the blunt tubercle of the male and the free sternites lack the median apophysis. Males of Kimula and Metakimula show some morphs with heavily swollen femur IV, while other morphs possess only rows of spines. Distribution: Kimulidae has a disjunct distribution. The core of the species occurs in Venezuela, Colombia, and the West Indies. An isolated species Tegipiolus pachypus new familial assignment was found in northeastern Brazil, representing a group morphologically (as well as geographically) isolated. Relationships: Kimulidae seems to be closely related to Escadabiidae, a family from Brazil, both belonging to the Samooidea group of families. Main references: • Systematics: Sørensen (1932), Mello-Leitão (1933a, 1938), Goodnight & Goodnight (1942c, 1943), González-Sponga (1987). • Natural history: González-Sponga (1987), Pérez González & de Armas (2000).

Manaosbiidae Roewer, 1943 Adriano B. Kury Etymology: Manaosbia, from type locality Manaos (Manaus), Amazonas, Brazil, called Greek bios (living). Characterization: • Size: Body length 3.5–10 mm, leg IV 12–49 mm long. • Dorsum (Figures 4.32a,f,g,h): Opisthosomal scutum with sides convex, only a little wider than prosomatic carapace, posterior border substraight. Ocularium narrow, low, without depression, with a pair of weak small spines. Ozopore like Figure 4.32d. Scutal area I armed with a pair of small spines; III with a pair of stouter spines. Free tergites II–III often with a pair of small spines. • Chelicerae: Weakly developed in both sexes, with bulla variably armed. • Pedipalps (Figures 4.32a,f): Smooth, without strong armature; femur cylindrical, neither flattened nor keeled. • Legs (Figure 4.32b): Coxa IV barely visible under scutum, dorsally covered with pointed tubercles and armed with a spiniform apical apophysis; trochanters I–III may bear ectal spines; femur IV unarmed, straight or a little crooked; only proximal tarsomeres of basitarsus I swollen spindlelike in male; tarsi III–IV with a pair of smooth claws (pectinate in Syncranaus cribum), occasionally sparse scopulae.

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Figure 4.32. Manaosbiidae. (a) Saramacia schematic (redrawn from Kury, 1997a). (b) Manaosbia, tarsus of leg I (from Kury & Pinto-da-Rocha, 2002); (c) habitus lateral; (d) ozopore region; (e) penis, dorsal and lateral views. (f–g) Zygopachylus, displacement of fluid from scent gland along taenidium, lateral and dorsal views (from Cokendolpher, 1987b). (h) Saramacia sp. from Brazil. Photos: b–d, A. B. Kury; e, h, R. Pinto-da-Rocha.

Taxonomy

• Genitalia (Figure 4.32e): Ventral plate of penis rectangular and elongate, with distal border concave or entire, basal setae stout, slightly bent, median two pairs of setae of ventral plate dorsally located, distal setae strongly curved but not helicoidal; stylus straight, usually bent in apex; glans long and columnar, without dorsal or ventral processes. • Color: Most species are uniformly dark brown with black mottling (Figure 4.32h). Appendages in general are much lighter, attaining yellow hues and often bearing dark rings. A few species possess large white tubercles on laterals of mesotergum. • Sexual dimorphism: Basitarsus I of male with basal two joints swollen spindlelike (Figure 4.32b), sometimes fused in a single piece. Distribution: Manaosbiidae has been recorded from Panama, the Lesser Antilles, Venezuela (plus Trinidad), the Guyanas, Colombia, Ecuador, northern and central Brazil, and Peru. The southern limit seems to be the Brazilian state of Mato Grosso do Sul. Habitats include lowland Amazonian rain forest up to submontane Andean forests, dry forests in Central America, and riparian forests in Brazil. Relationships: On the basis of evidence from the genital structure, Manaosbiidae is a member of the superfamily Gonyleptoidea (Kury, 1993a), but its relationship to the other families is unclear. Main references: • Systematics: Roewer (1913, 1915a, 1943), Kury (1997a, 2003). • Natural history: Rodríguez & Guerrero (1976), Mora (1990, 1991).

Oncopodidae Thorell, 1876 Peter Schwendinger Etymology: Oncopus, from Greek onkos (mass, growth, swelling, tumor) and podos (leg). Thorell (1876a) translated onkos into the Latin tumidus, which means “swollen” or “inflated” and refers either to the stout legs of the type genus or, more likely, to its ovoid, uniarticulate tarsi. Characterization: • Size: 2.3 mm (male of G. asli) to 10.7 mm (male of Oncopus truncatus). • Dorsum (Figures 4.33a,b): Somewhat pear shaped, with prosomal region narrower than opisthosomal region. Carapace and opisthosomal tergites I–VIII fused into a single plate (scutum completum) with a quite smooth surface and few or no projections. Ocularium low or a more or less elevated, rounded or pointed tubercle. Paired conical or unpaired lobelike projections from posterior margin of carapace region and from anterior margin of first opisthosomal area forming a more or less distinct “bridge” (oncopodid synapomorphy; Figure 4.33c). Dorsal scutal areas of opisthosoma distinctly bulged and smooth (Palaeoncopus) or low and carrying pairs of rounded paramedian tu-

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Figure 4.33. Oncopodidae. (a) Habitus of Gnomulus baharu, male (from Schwendinger & Martens, 1999). (b) Habitus of Oncopus truncatus, female (from Schwendinger, 1992). (c) Carapaceopisthosoma bridge of G. rostratus, dorsolateral view. (d) Penis of G. sumatranus, lateral view (from Schwendinger & Martens, 1999). (e) Apex of penis of Palaeoncopus gunung, dorsal view (from Martens & Schwendinger, 1998); (f) same of Biantoncopus fuscus, glans expanded, lateral view (from Martens & Schwendinger, 1998); (g) same of G. sumatranus, dorsal view (from Schwendinger & Martens, 1999); (h) same of O. feae, dorsal view (from Schwendinger & Martens, 2004). (i) Penis of Caenoncopus cuspidatus, dorsolateral view (from Martens & Schwendinger, 1998).

Taxonomy

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bercles, the last ones projecting beyond posterior scutal margin in several Oncopus spp. Venter: First leg coxae free, others fused. Anteroproximal processes usually present on ventral side of coxae III and IV and often a posteroproximal one on coxa III; most Oncopus spp. additionally with scalelike anteroproximal apophysis on coxa II. Sternum very narrow, lanceolate. Genital operculum triangular to semicircular, in two Oncopus spp. with small anterior tubercle. Spiracles mostly hidden under posterior processes of coxa IV. All opisthosomal sternites fused to ventral scutum. Small, unmodified anal plate formed by tergite IX. Chelicerae: Weak to robust (particularly in some Oncopus males). Basal segment with or without retroventral process; dorsal tubercle or boss more or less extensive (largest in male of G. imadatei). Second segment with ventrodistal process in Oncopus and in ?Martensiellus sp., several Oncopus spp. also with ventroproximal process on third segment. Pedipalps: Ventral processes on trochanter and femur; few Oncopus spp. with pro- and retroventral processes on patella and tibia, respectively. Claw relatively short compared with other Laniatores, movable only to a limited extent. Legs (Figures 4.33a,b): Relatively short and stout; legs II and IV longer than legs I and III. Few tarsomeres; tarsal formula: 1:1:1:1 (Oncopus), 1:1:2:2 (C. cuspidatus, Martensiellus), 1:1:3:3 (Palaeoncopus, other Caenoncopus), 2:2:2:2 (few Gnomulus), 2:2:3:3 (Biantoncopus, most Gnomulus). Pore organ present on all undivided tarsi, that is, all leg tarsi in Oncopus and tarsi of anterior legs in Palaeoncopus, Caenoncopus, and Martensiellus. Anterior legs with single claw; posterior ones with double claw. No spines, but a few setae (most on tarsi). Paired lobelike processes (their tips touching each other) on pro- and retrolateral distal margin of coxae and femora, only pro- and retroventral processes distally on tibiae. A pair of dorsal tubercles on each coxa II, in some Gnomulus spp. an unpaired dorsal tubercle on each coxa IV. Some Oncopus spp. with dorsoproximal tubercle on femur II and ventroproximal one on femur IV. Genitalia: Penes highly species specific and displaying a great variety of forms. Truncus penis without musculature, dorsoventrally depressed (Caenoncopus; Figure 4.33i) or tubelike (all others; Figure 4.33d), with subapical lateral setae (Figures 4.33d–i), Oncopus additionally with apical setae (Figure 4.33h). Glans penis operated by hemolymph pressure; directed upward (distad) at rest (Martensiellus, Palaeoncopus, Biantoncopus; Figures 4.33e,f) or downward (proximad) (all others; Figures 4.33g–i); expandable in Martensiellus tenuipalpus and in Biantoncopus (Figure 4.33f). Glans usually composed of a membranous socket carrying a pair of lateral sclerites connected by a median plate (oncopodid synapomorphy); stylus and a pair of membranous tubes (reduced in Palaeoncopus; Figure 4.33e) embedded between lateral sclerites and median plate (Figures 4.33f–h). Glans in Caenoncopus modified to an asymmetrical hypertrophied stylus lacking other elements (Figure 4.33i). Ovipositors not distinctive, very short, unsegmented, circular in cross section (in very small species) or laterally compressed (in most species; oncopodid synapomorphy), distally with two broadly truncate lobes, each one carrying a row of short setae. Internal structure typical for Laniatores,

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with cross-shaped vagina, ring fold, and eight peripheral receptacles in O. truncatus (sub O. acanthochelis). • Color: Usually amber, with dark brown reticulation in carapace region and with dark brown margin and transversal bands in opisthosoma region of dorsal scutum. Dark transversal bands also on ventral scutum. A few undescribed Gnomulus spp. with conspicuous orange ground color. Juveniles gray brown in ground color. • Sexual dimorphism: Males differ from females in larger, more elevated carapace region and stronger chelicerae (most Oncopus, few Gnomulus); more extensive dorsal tubercle or boss on basal segment of chelicerae and larger ventral processes on pedipalpal trochanter and femur (many Gnomulus); stronger proventral process on pedipalpal patella (few Oncopus); stronger metatarsus III (G. crassipes); wider genital operculum (few Gnomulus); denser pubescence (presumably composed of glandular setae) on ventral scutal areas (some Gnomulus); more elevated, bulged, and pallid ventral areas (some Gnomulus), or areas keeled, with white enclosures (some Oncopus). External sexual dimorphism in other genera less pronounced (Caenoncopus) or absent (Palaeoncopus, Biantoncopus). Distribution: Known from the Himalayan region and from eastern and southeastern Asia, that is, the area between Nepal, southwestern China (Sichuan Province), northern Vietnam, the Philippines, Waigeo Island off the northwestern tip of New Guinea, Java, and northern Thailand. Relationships: Oncopodids belong to the “hemolymph-pressure Laniatores” (= Grassatores sensu Kury, 2003), which have lost the musculature of their penis. According to most recent authors (Martens, 1980; Shear, 1982; Shultz, 1998; Giribet et al., 2002; Schwendinger & Martens, 2002a), Oncopodidae is a sister to the remaining families within this group. Main references: • Systematics: Roewer (1923); Martens (1976, 1980, 1986), Martens et al. (1981), Schwendinger (1992, 2006), Martens & Schwendinger (1998); Schwendinger & Martens (1999, 2002a,b, 2004, 2006).

Pentanychidae Briggs, 1971 Thomas S. Briggs and Darrell Ubick Etymology: Pentanychus, from Greek, refers to the five branches on claws III–IV of adults. Characterization: • Size: Body length 1.9–2.8 mm. • Dorsum (Figures 4.34b,c): Scutum trapezoidal; anteriorly with low ocularium bearing lateral eyes; posteriorly with five transverse rows of tubercles repre-

Taxonomy

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Figure 4.34. Pentanychidae. (a) Abdomen, ventrolateral, showing lateral sclerites (LS) and the free ninth tergite (T9). (b–c) Pentanychus hamatus, female: (b) lateral; (c) dorsal. (d–e) P. bilobatus, pedipalpal femur, lateral: (d) male; (e) female. (f–h) P. spp., hind claws: (f–g) P. flavescens, adult, dorsal and lateral; (h) P. hamatus, juvenile, dorsal view showing arolium. (i–j) P. flavescens, female, ovipositor: (i) ventral; (j) lateral. (k–m) Pentanychus hamatus, penis: (k–l) ventral (k) and lateroapical (l) views, showing labial process; (m) dorsoapical view. Abbreviations: L, Labial process; O, stylar opening; P, parastylar lobes; S, stylus. Figures from Briggs (1971b). Photos: D. Ubick. Scale bar for a–c = 1 mm.

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senting fused tergites. Free tergites VI–VIII with transverse row of tubercles. Tergite IX separated from anal operculum (Figure 4.34a). Venter: Sternum elongate pentagonal, posteriorly setose. Genital operculum oval. Opisthosoma with basal sternite broad, bearing exposed round spiracles; middle sternites narrow; distal sternite broad. Lateral opisthosomal margin with three pairs of sclerites (Figure 4.34a). Chelicerae: Distal segment with setose tubercles along dorsal surface. Pedipalps: Segments stout; femur with dorsal row of setose tubercles and ventral with five megaspines (Figures 4.34d,e), patella tuberculate, tibia with three ectal and four mesal megaspines, tarsus with four ectal and four mesal megaspines and apical claw. Legs: Distitarsus II with about six tarsomeres. Tarsal formula: 5–6(2–3): 13– 15:4:4. Claws III–IV with two pairs of branches on uniform central prong (Figures 4.34f,g). Juvenile claws III–IV with six branches and distal arolium (Figure 4.34h). Genitalia (Figures 4.34i–m): Male penis with basal sac of papillate texture and cylindrical truncus fully lined with muscles. Glans sagittate, simple, ventrally with a pair of stout setae. Stylus short, with apical opening and a pair of lateral lobes that may represent a bifurcate dorsal lobe. Female with ovipositor having broad, elongate lateral lobes, each bearing acute apical seta and about two elongate subapical setae. Dorsal apical lobe reduced and ventral apical lobe narrow. Color: Yellow to orange integument. Most species have various degrees of black pigmentation on scutum and tergites. Sexual dimorphism: The male of Pentanychus has a greatly enlarged pedipalpal femur bearing a stout ventral process (apparently homologous with the female middle megaspine) and an enlarged labial process, often with a complex arrangement of hooks and lobes (Figures 4.34d,e). The male of Isolachus is unknown.

Distribution: Pacific Northwest of the USA, from middle Washington to southwestern Oregon. Relationships: Briggs (1971b) placed Pentanychidae in a clade with Triaenonychidae and Cladonychiidae(as Erebomastridae), all of which have claws III–IV with five or fewer branches, and more distantly related to those families with a multibranching peltonychium, which at that time included only Travuniidae and Synthetonychiidae. Pentanychids were considered the basalmost members of “apeltonychia” on the basis of a number of proposed plesiomorphies: claws III–IV of adults with a relatively high number of branches, claws III–IV of juveniles with an arolium, tergite IX separated from the anal operculum, and lateral sclerites present on the opisthosoma. Subsequently, Suzuki (1972c, 1975a,b, 1976b) described a remarkable fauna of triaenonychids from East Asia. Some of these, for example Yuria, resemble pentanychids in having lateral sclerites and a free ninth tergite. Others, such as Kainonychus, have similar claw branching to that of pentanychids (such as the Nearctic Paranonychus). Most interesting is the fact that the majority of these species have

Taxonomy

multibranched tarsi III–IV, even including the peltonychium state. Given that juveniles have more highly branched claws, a higher number in adults has been interpreted as plesiomorphic (Briggs, 1971b; Suzuki, 1975b) relative to the typically trifurcate state in Triaenonychidae. Thus the claw morphology of pentanychids, and also the East Asian triaenonychids, places them relatively basal to typical triaenonychids. Additional triaenonychids with high variation in claw branching were later discovered in the Australian fauna and even within a single genus, Lomanella (Hunt & Hickman, 1993). These authors questioned the usefulness of the claw character in defining travunioid families. They further argued that Pentanychidae was not based on synapomorphies. However, this may not necessarily be true if the apparently unique sexually dimorphic structures in Pentanychus turn out to be present in males of Isolachus. This point was previously made by Martens (1986), who concluded that, on the basis of the morphology of the male genitalia, pentanychids could not be separated from triaenonychids. In his analysis of triaenonychid glans types, he argued that the most primitive form is also the most complex, having three lobes in addition to the stylus. In Pentanychus the glans is rather simplified. The ventral plate is absent, apparently fused to the stylus, and probably represented by a pair of stout setae. The dorsal plate appears to be reduced to two small, apical, parastylar lobes. Thus, if pentanychids are included in triaenonychids on the basis of the glans structure, and in contrast to their somatic morphology, they would be in a relatively derived clade, perhaps near the Japanese Kainonychus or the North American Paranonychus. On the other hand, similarly simple glandes occur also in travuniids and cladonychiids. These two families have dramatically different claws III–IV: travuniids with peltonychia and cladonychiids with two-branched claws. At least the Nearctic travuniids have a free ninth tergite, which Briggs (1971b) considered primitive (but was interpreted as derived by Rambla, 1980b). The claw type of cladonychiids, however, could certainly be derived from that of Pentanychus, which has the two apical branches much larger than the others. Clearly, more detailed study is needed to determine the probable relatives of Pentanychidae, as well as the future of its family status. Main references: • Systematics: Briggs (1971b).

Phalangodidae Simon, 1879 Darrell Ubick Etymology: Phlangodes, from Greek phalanx, genitive phalangos, a line of soldiers in formation (Jaeger, 1959), probably referring to the rows of pedipalpal spines. Characterization: • Size: Total body length from 0.8 to 3.0 mm. • Dorsum (Figure 4.35c): Body oval, with scutum and three free tergites (reported as fused in Paralola). Scutum with transverse groove and constriction separating prosoma from opisthosoma; ocularium central, at or near anterior

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margin, and bearing two eyes; both eyes and ocularium may be reduced in cavernicolous species; few to several pairs of anterior tubercles present at anteriolateral scutum margins; opisthosomal portion of scutum divided into five areas with transverse rows of tubercles. Venter: Sternum and genital operculum enclosed by leg coxae; opisthosoma with six sternites and anal operculum. Chelicerae: Not enlarged; basal segment sometimes with ectobasal swelling, dorsal surfaces often tuberculate. Pedipalps (Figures 4.35a,b): Armed with megaspines: trochanter with 0–2 ventral; femur with 3–4 ventrobasal and 1–2 mesodistal; patella with 1 ectal and 1–3 mesal; tibia with 2 ectal and 2–3 mesal; tarsus with 2 ectal and 2 mesal. Tarsus with stout apical claw. Legs: Range in length from short to relatively long, with a leg II/scutum length ratio from 2 to 8. Tarsal formula: commonly 3:5:5:5, but reduced in some species to 3:3:4:4 and as high as 5:8:6:8 in others. Tarsi III–IV with two smooth claws, lacking tarsal process (pseudonychium). Genitalia: Penis (Figure 4.35e–g) without muscles; truncus with thin ventral plate entire, notched, or bifurcate, usually ventral in position, rarely lateral or swollen, armed with setae, sometimes also with rigid apical spine; glans of variable complexity, expands by telescoping or unfolding from truncus, consists of stylus and two or more accessory lobes. Ovipositor (Figure 4.35h,i) with cuticle smooth, microspined, or imbricate; apex divided into two or four lobes, with five to seven pairs of apical setae, sometimes with an additional one to three pairs of subapical setae, occasionally with a pair of apical teeth. Color: Typically yellowish to orange brown, rarely with maculations, depigmented in troglobites. Sexual dimorphism: There is considerable intrageneric variation in the form and degree of dimorphisms. Within Texella, species range from having only one up to four dimorphisms (Figure 4.35a). The function of some of these structures seems apparent, such as the male clasping process (spur) at the base of leg IV (Sitalcina, Texella, Scotolemon) and the prong on the pedipalpal tarsus for opening the female genital operculum (Calicina). For others, it remains obscure. The following list is incomplete because males of several

Figure 4.35. Phalangodidae. (a–b) Right lateral view: (a) Texella spinoperca, male with extruded penis showing prominent sexually dimorphic structures, a spur on trochanter IV (x) and a postopercular process (y); (b) Texella mulaiki, male with extruded penis lacking prominent dimorphic structures but with strongly troglomorphic features, the absence of eyes, a reduction of the ocularium, and the elongation of palpal segments and megaspines. (c) Microcina homi, showing areolate sculpturing on scutum. (d) Anterior right lateral part of scutum, Calicina serpentinea, a savanna-dwelling species with absence of eyes and few small anterior tubercles. (e– g) Penis morphology: (e) Calicina digita, lateral, glans partially expanded; (f–g) Penis, bifurcate ventral plates in dorsolateral (f) and dorsal (g) views: (f) Texella reyesi, showing thin lateral prongs and enlarged glans; (g) Bishopella laciniosa, showing expanded lateral prongs and reduced glans. (h–i) Ovipositor: (h) Texella reyesi, showing hyperexpanded ovipositor with four apical lobes; (i) Sitalcina californica, showing hooked apical setae and imbricate ovipositor cuticle. Photos: D. Ubick.

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genera are either not known or have not been adequately described (Proscotolemon, Lola, Paralola, Haasus). Male modifications: enlarged ocularium (Microcina); increased number of anterior tubercles on scutum (Texella); elongated anal operculum (Ausobskya); enlarged sternal prongs (Phalangodes, Bishopella, Crosbyella); enlarged genital operculum (Ptychosoma, Texella); reduced genital operculum (Scotolemon); postopercular process (Texella); elongated pedipalpal segments (Ausobskya); swollen pedipalpal femur (Banksula); increased number of megaspines on pedipalpal femur (Sitalcina); increased tuberculation on pedipalpal femur (Banksula); reduced megaspines on pedipalpal tibia and patella (Banksula); dorsal spur on pedipalpal tarsus (Calicina); enlarged megaspines on pedipalpal tarsus (Calicina); dorsoapical process (Drüsenorgan, Martens, 1972a) on tarsus II (Ausobskya); increased tuberculation on trochanter IV (Sitalcina); enlarged process (spur) on trochanter IV (Scotolemon, Sitalcina, Texella); trochanter-femur clasper on leg IV (Scotolemon, Sitalcina). Female modification: apical teeth or tubercles on genital operculum (Texella). Distribution: Phalangodidae is best represented in the western Nearctic, which has over two-thirds of the more than 100 described species. The greatest endemism is in California, home to four endemic genera (Calicina, Microcina, Sitalcina, and Banksula) with about 50 species. Texella, with 28 described species, occurs from California to Texas. The eastern Nearctic, which has not been recently studied, has only 11 species distributed among Phalangodes, Bishopella, Crosbyella, Tolus, Undulus, and Wespus. Numerous undescribed species are presently known from just the western Nearctic. Provisionally included in Phalangodidae is the Mexican genus Guerrobunus with its three species. The relatively depauperate Palearctic fauna is known from three disjunct regions. The Canary Islands and Japan each have a monotypic genus, Maiorerus and Proscotolemon, respectively. The richer Mediterranean fauna has some 18 species in Ptychosoma, Scotolemon, Lola, Paralola, Ausobskya, and Haasus. The disparity between the species richness of the Nearctic and Palearctic is noteworthy. Given the many more decades of collecting in the latter region, and especially in Europe, at least some of the difference would appear to be real. It is not clear, however, if the absence of species from the Mediterranean to Japan represents a genuine gap or an artifact of inadequate sampling. Relationships: Monophyly of Phalangodidae is currently based largely on the number and arrangement of pedipalpal megaspines. This pattern is generally fairly uniform except for some genera, such as Guerrobunus (see Vázquez & Cokendolpher, 1997), which may need to be excluded from the family. Most of the genera also share a general conformity in the genital morphology, with some exceptions. The most widely deviating morphologies are in males of Haasus and perhaps of Ptychosoma and females of Proscotolemon. Our knowledge of the intrafamilial relationships remains fragmentary pending further revisionary studies of several taxa. Generic limits need to be stabilized for all the eastern Nearctic genera, which were originally defined on usually unreliable somatic characters, and the Mediterranean Scotolemon, Ptychosoma, and Ausobskya, where several species seem to be misallocated. Other genera,

Taxonomy

such as Lola, Paralola, and Proscotolemon, will remain enigmatic until males are described. Despite these limitations, two hypotheses of relationship have been proposed. The first is that the fundamental division in the family is based on the form of penis expansion. A glans that telescopes out of the truncus, considered plesiomorphic, occurs in Calicina (Figure 4.35e) and Ptychosoma, whereas a glans that unfolds from the truncus (Figures 4.35g) occurs in all other genera for which males have been described (Ubick & Briggs, 1989). The second suggests a close relationship between the genera with deeply bifurcate ventral plates, namely, Banksula, Texella (Figure 4.35f), and Phalangodes, and the nominal genera of the eastern Nearctic (Figure 4.35g). Although this clade is strictly Nearctic, a possible Palearctic counterpart may be found in the species of Ausobskya and Scotolemon with apically notched ventral plates. Although the relationship of Phalangodidae to other Grassatores is currently unresolved and a sister group has not been identified, it appears that the family occupies a relatively basal branch on that tree. Phalangodids are somatically plesiomorphic, having a well-defined ocularium and lacking pedipalpal and tarsal modifications present in gonyleptoids and others, as well as genitalically. The penis, at least in its basal members, has a ventral plate that is a thin extension of the truncus, apically entire, and having only simple setae. In the basal genus, Calicina, the glans telescopes from the truncus rather than unfolds from it. This condition also occurs in Assamiidae and Biantidae (Martens, 1986). Especially striking is the resemblance between Calicina and some East Asian genera, such as Bupares, Buparellus, and Parabeloniscus (Suzuki, 1973), currently placed in Epedanidae. If, as is expected, this type of penis turns out to be primitive in Grassatores, then the similarities are plesiomorphies, suggesting a paraphyletic relationship between these taxa. Main references: • Systematics: Crosby & Bishop (1924), Roewer (1935a), Kratochvíl (1937, 1958a), Goodnight & Goodnight (1942a, 1945), Kraus (1961), Briggs (1968, 1974b), Brignoli (1968), Martens (1972a, 1978b), Rambla (1972, 1973, 1977, 1993), Suzuki (1973), Silhavy (1976), Starega (1976b), Briggs & Ubick (1981, 1989), Martens & Lingnau (1985), van der Hammen (1985), Ubick & Briggs (1989, 1992, 2002, 2004), Thaler (1996), Vázquez & Cokendolpher (1997). • Natural History: Silhavy (1976), Ubick & Briggs (1989), Thaler (1996).

Podoctidae Roewer, 1912 Adriano B. Kury Etymology: Podoctis, from Greek pous, podos (foot) and oktis (spine), referring to the ventral row of long spines in femur I. Characterization: • Size: Medium-sized Laniatores, body length 2.5 to 5 mm. Legs I–IV extremely variable, 3–10/10–30/7–21/9–28 mm long.

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• Dorsum: Dorsal scutum (Figures 4.36a–c) outline can be ovoid or subtrapezoidal, in general without strong constrictions, and the carapace is not much smaller than the opisthosomal scutum. Mesotergum usually clearly divided into areas by grooves; the areas may be connected by tubercular bridges. No areas fused. Armature of areas and tergites highly variable, perhaps either completely smooth and unarmed or armed with strong spines, which bear subapical setae. In some species the scutum is profusely covered with warts, wrinkles, granules, and tubercles. Common ocularium (or interocular mound) not always present; it may be very high and densely granulous. Sometimes eyes are wide apart in separate individual mounds, always linked to the frontal part of the carapace by tubercular bridges (which may be a synapomorphy for the family). • Venter: Coxae I–IV more or less radiating from sternum, coxa IV not greatly enlarged in oblique position. Coxae connected by clearly marked tubercle bridges, densely tuberculate tubercles growing larger anteriorly. No dimorphism reported for genital operculum. Stigmatic area V-shaped. Stigmata may be concealed by tubercles. • Chelicerae: Hands usually not swollen. • Pedipalps: With ventral row of spines in femur and ventromesal and ventroectal spines in patella-tibia-tarsus. Tibia and tarsus do not form a subchela. • Legs: Legs usually long and straight, often covered with rows of pointed tubercles, especially leg I, which in most species has powerful ventral and dorsal rows of setiferous spines in both sexes (Figure 4.36k). Distitarsus I one- or twojointed; II one- to four-jointed. • Genitalia: Penis is unique (Figure 4.36l); the dorsal plate is deeply cleft, and there is an inflatable sac that inflates and exposes the stylus, flanked by two powerful prongs (Figures 4.36m–o). • Color: Background color usually brown to yellow, some species are deep green; legs may be ringed in black and yellow; scutal spines may be black, sharply contrasting with background. • Sexual dimorphism: Shown in basichelicerite, which is very long and armed in males (Figures 4.36d–f). The pedipalp in males may be thickened at the base with a cluster of divergent spines (Figures 4.36i,j) or extremely elongate (Figures 4.36g,h), while the female pedipalp is short. Also shown in ocularium, which in male can be wider or much more elaborate in ornamentation and leaned back against the scutum (Figures 4.36b,c). Distribution: The peak diversity of the family is in Southeast Asia, especially in New Guinea. It also occurs in Melanesia, Micronesia, Japan, India, Sri Lanka, Madagascar, Seychelles, Mauritius, and central Africa. A single species is known from Australia. One species, Ibantila cubana, is reported from the New World (Silhavy, 1969a), introduced in a botanical garden in Cuba (A. Pérez González, pers. comm.). Brasiloctis bucki, the Brazilian “Podoctidae” of Mello-Leitão (1938), was later transfered to Triaenonychidae (see Soares & Soares, 1979).

Taxonomy

223

Figure 4.36. Podoctidae. (a–c) Lomanius longipalpus mindanaoensis from the Philippines: (a) Habitus, male, lateral; (b) female, dorsal; (c) male, dorsal. (d–f) Hoplodino hoogstraali from the Philippines: (d) Female chelicera, ectal; (e) male chelicera, mesal; (f) ectal. (g–h) L. longipalpus mindanaoensis from the Philippines: (g) left pedipalpus of male, ectal; (h) left pedipalp of female, ectal. (i– j) Hoplodino hoogstraali from the Philippines: (i) left pedipalp of male, mesal; (j) left pedipalpus of female, ectal. (k) Lomanius longipalpus mindanaoensis from the Philippines, left leg I of male, lateral. (l) Heteropodoctis quinquespinosus from Papua New Guinea, distal part of penis, dorsal. From: Suzuki (1977b). Scale bar l = 150 ␮m. Photo: D. Ubick. (m–o) unspecified podoctid, schematic view of penis: (m) unexpanded, lateral; (n) unexpanded, dorsal; (o) expanded, lateral (from Martens, 1986).

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Relationships: Largely unknown. The family belongs to Grassatores, and it is possible that it is related to Samooidea, although there is no obvious relationship with any family. Main references: • Systematics: Roewer (1912b, 1923, 1949), Suzuki (1964a,b, 1969, 1977b), Rambla (1984), Starega (1992). • Natural History: Roewer (1929a), Suzuki (1977b), Martens (1993b).

Samoidae Sørensen, 1886 Abel Pérez González and Adriano B. Kury Etymology: Samoa, from the Pacific island Samoa. Characterization: • Size: Small to medium-sized harvestmen; body length: 1.9–5.5 mm. • Dorsum: Body as an asymmetrical hourglass, anterior half much shorter, posterior half rounded, laterally convex appearance (Figures 4.37a,b). Ocularium low and wide present in Samoa, Badessa, Feretrius, and Zalmoxista australis new familial assignment, in Kalominua narrower and taller, in Akdalima and Reventula wide and ending in an acute spine, in Arganotus developed, elliptical, convex, and projected as a low cone bearing an apical spine, and in Pellobunus a very low cone. Body low (almost smooth) or densely covered with low rounded granules (Figures 4.37a,b). Mesotergum with four areas poorly defined, unarmed (Figures 4.37a,b) (except in Reventula amabilis). Free tergites unarmed. • Venter: Some taxa possess ventrally a pair of medial apophyses in coxa IV. • Chelicerae: Basichelicerite very long, smooth, unarmed, and enlarged without a conspicuous bulla (Figure 4.37c). Hand massive, with fingers short and strongly toothed, smooth, granulate or with a few short spinelike tubercles. • Pedipalps (Figure 4.37f). Not enlarged. Coxa well developed, femur commonly large, very convex dorsally, with two low ventrobasal setiferous tubercles and one mesal subdistal setiferous tubercle. In some species (such as Akdalima jamaicana, Orsa daphne) the femur mesodistal and the patella have peculiar cuticular apophyses. Tibia commonly with three ectal and two mesal low setiferous tubercles where the basis of the two mesal ones could be modified or enlarged (e.g., Samoa variabilis, Reventula amabilis). Tarsus with lateroectal and lateromesal rows of two to three setiferous tubercles. In some species the femur dorsal has a row of granules, and the patella-tibia dorsally is heavily granulous (e.g., Reventula amabilis). • Legs: III–IV without tarsal process. Scopula (Figure 4.37e) commonly present but highly variable from well developed in Samoa to almost imperceptible (or absent?) in Kalominua. Claws smooth. Tarsal formula: 4(2):6–9(3):4–5:5–6. • Genitalia (Figures 4.37g,h): Truncus cylindrical, without a well-defined ventral plate as in Gonyleptoidea, ending in one calyx. Pars distalis not differenti-

Taxonomy

Figure 4.37. Samoidae. (a) Akdalima sp., male, habitus dorsolateral. (b) Akdalima sp., male, habitus dorsal. (c) Pellobunus insularis, chelicera, mesal. (d) Pellobunus sp., metatarsus III, ventral. (e) Reventula sp., tarsus III showing the scopula, lateral. (f) Pellobunus sp., right pedipalp, mesal. (g) Arganotus sp., distal part of penis, dorsolateral. (h) Pellobunus sp., distal part of penis, ventrolateral. All photos by A. B. Kury. Abbreviations: Ag, astragalus; Bu, bulla; Ca, calcaneus; Ci, capsula interna; Cx, calyx; Fs, foliar spines; Map, medial acute process; Pd, pars distalis; Sas, short acuminate spines; Sc, scopula.

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ated from pars basalis by any remarkable groove or constriction. In Kalominua spp. the pars distalis is compressed dorsoventrally, and the calyx is reduced. Internally or lateroapically the calyx may possess paired spines and a medial acute process (as in Samoa variabilis). Pars distalis ventral and laterally armed with strong spatulate (foliar) spines. In some taxa there is a group of four ventroapical short acuminate spines (Figure 4.37h) (as in Akdalima, Pellobunus, Reventula). The capsula interna is eversible and formed by a pair of conductors completely fused with the stylus, forming a single structure. The follis is not modified and not observed externally. Soares and Avram (1981) provided the only informative published drawing from a Kalominua when they described Crosbyella inermichela, adopted here as Kalominua penis type. • Color: Dull light brown to yellow or green yellow background with darker mottling, sometimes dark brown. • Sexual dimorphism: Metatarsus of leg III is swollen spindlelike (receptor or secretor?) in males (Figure 4.37d). The basichelicerite and the pedipalps are bigger in males, and the females do not have the ventral medial apophysis in coxa IV. Distribution: Typical Samoidae occur in Polynesia, Melanesia, Australia, Mexico, the West Indies, and Venezuela. In all these forms the external morphology and genitalia are remarkably similar. The family has been cited also from continental Africa, Madagascar, Seychelles, and Indonesia, but most of these records are doubtful or clearly not Samoidae. The Seychellan “Samoidae” (Benoitinus, Mitraceras) belong to Samooidea, but for now it is impossible to assign them to any family, and their genitalia do not match those of typical Samoidae from Polynesia and Central America. Relationships: Samoidae appears to be related to the rest of “Samooidea” by the presence of a penis with one capsula interna eversible formed by a pair of conductors and a stylus. The scopula relates samoids to Biantidae; the penial calyx to Neoscotolemon spp.; the modified metatarsus III to Stenostygninae and Neoscotolemon spp. Only a revisionary project including Zalmoxoidea and Samooidea could give us more solid elements to understand the relationships of these two closely related groups. Main references: • Systematics: Sørensen (1886), Roewer (1923), Silhavy (1977, 1979), Starega (1992), Kury (2003). • Natural history: González-Sponga (1987).

Stygnidae Simon, 1879 Ricardo Pinto da Rocha Etymology: Stygnus, from Greek stygnós, devil, diabolic being.

Taxonomy

Characterization: • Size: dorsal scutum 0.9–5.7 mm ; leg IV 2.6–48.7 mm long. • Dorsum (Figures 4.38a–e): Body usually rectangular. Ocularium separated into two pieces in the middle of the prosoma or close to groove I. Area I normally divided. Areas I and IV and posterior margin with small tubercles, I with two large spines on Yapacana; III with two large spines (fused in one species of Eutimesius), rarely with tubercles or unarmed. Free tergites unarmed or armed with a pair of tubercles (Sickesia and several Stygnus). • Venter: Usually small-tuberculate; males of Nomoclastes possess a huge curved spur on coxa IV (Figure 4.38a). • Chelicerae: Similar in both sexes or with enlarged segment II in males; segment I smooth or with small tubercles on dorsal. • Pedipalps: Short and thick to slender and elongate (Figure 4.38f). Very enlarged in Protimesius and Pickeliana (Stygninae). • Legs: Distitarsi I–II normally three-segmented. Tarsi cylindrical (Stygninae, Heterostygninae) or depressed (Nomoclastinae). Tarsal formula: 4–9:6–26:6– 11:6–13. Claws smooth and subparallel or pectinate and opposite each other (Heterostygninae). Tarsal process thick or reduced to a long hair in some small Stygninae. • Genitalia: Truncus of penis with an apical ventral plate thick (Nomoclastinae, Stygninae; Figures 4.38g,i) or slender (Heterostygninae, Figure 4.38i). Distal margin of ventral plate straight, slightly concave, or with U-shaped cleft. Setae on lateral of ventral plate or rarely absent, reduced in size (Heterostygninae) or enlarged (Stygninae, Nomoclastinae). • Color: Varies from light brown to reddish; some species of Heterostygninae present white patches, stripes, or spots on dorsal scutum. • Sexual dimorphism: Shown by large cheliceral segment II on males; larger tubercles on trochanter, femur, and tibia (mainly on leg IV) of males (Heterostygninae and Stygninae); and large spur on ventral male coxa (Nomoclastinae). Key to subfamilies 1. Eyes close to each other in the middle of the prosoma (Figures 4.38a,c); apex of distitarsi III–IV bilobate; pedipalpal femur and patella short and thick . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nomoclastinae . Eyes separate and close to groove I (Figures 4.38d,e); apex of distitarsi III–IV straight; pedipalpal femur and patella long and thin (Figure 4.38f). . . . . . . . . . . . 2 2. Claws III–IV opposite, pectinate; distitarsi III–IV depressed. . . . Heterostygninae . Claws III–IV parallel or subparallel, smooth; distitarsi III–IV cylindrical. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Stygninae

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Figure 4.38. Stygnidae. (a) Habitus: lateral view of Nomoclastes quasimodo (Nomoclastinae); (b) Protimesius laevis (Stygninae). (c–e) Habitus dorsal: (c) Nomoclastes taedifer (Nomoclastinae); (d) Stygnoplus clavotibialis (Heterostygninae); (e) Stygnus luteus (Stygninae). (f) Stygnus luteus, pedipalp, lateral. (g–i) Penis: (g) Nomoclastes quasimodo; (h) Innoxius magnus (Heterostygninae); (i) Stygnus pectinipes (Stygninae). Scale bars: a–f = 1 mm; g–i = 0.1 mm. Figures after Pinto-da-Rocha (1997).

Taxonomy

Distribution: From the Lesser Antilles (Heterostygninae) to northern and central South America (Nomoclastinae endemic to central Colombia and Stygninae from north of the Tropic of Capricorn). The Amazonian rain forest hosts the highest diversity. Distribution patterns are poorly known since half the species are known only from the type material. Relationships: Stygnidae are Gonyleptoidea (sensu Martens, 1986), placed in the group of families with a tarsal process (Cranaidae, Manaosbiidae, Cosmetidae, and Gonyleptidae), and the group is the sister of Cosmetidae and Gonyleptidae by the presence of the dorsal process on the penis glans and by the short and thick stylus (Kury, 1992a). The monophyly of Stygnidae is supported by the ocularium separated into two pieces, a trochanter IV with one large dorsal tubercle, scopula with long and spatulate hairs, and distal tarsomere of distitarsi III–IV short, wide, and slightly depressed (Pinto-da-Rocha, 1997). Main references: • Natural history: Friebe & Adis (1983), Pinto-da-Rocha (1997). • Systematics: Roewer (1923), Pinto-da-Rocha (1997).

Stygnommatidae Roewer, 1923 Abel Pérez González Etymology: Stygnomma, from preexisting genus Stygnus and Greek omma, eye (“the one who has eyes like Stygnus.” i.e., separated). Characterization: The monophyly of Stygnommatidae needs to be studied in depth; however, we already possess some elements of the artificiality of the current concept. For this reason the characterization offered here is restricted to Stygnommatidae sensu stricto, that is, to the species more closely related to Stygnomma fuhrmanni that share the same morphological and genital ground plan. The rest of the species that do not share these characters should be segregated from this family. • Size: Medium-sized to large Laniatores; body length from 3 to 6 mm (up to 12 mm with chelicera). • Dorsum: Body hourglass shaped, with the carapace roughly as long as the mesotergal shield (Figure 4.39b). Common ocularium lacking, eyes widely separated, located directly on the carapace in a position more or less halfway between the anterior border and the scutal groove (Figure 4.39b). Some species with a small spiniform apophysis between the eyes. Frontal hump absent (Figure 4.39a). Cheliceral sockets big and well marked (Figure 4.39b). Ozopores only visible laterally. Furrows of the mesotergal areas vestigial; areas recognizable only by the coloration or a longitudinal row of small granules. Areas without outstanding armor, except for an undescribed species from Trinidad and Tobago that presents a small medial protruded tubercle in area III. Free tergites unarmed, with a longitudinal row of granules.

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a b

e

c

d f

g

h

i

Figure 4.39. Stygnommatidae. (a–b) Stygnomma sp.: (a) female, lateral, showing the tipical pedipalpus; (b) male habitus, dorsal. (c–h) Penis of Stygnomma sp.: (c–d) from Venezuela; (c) pars distalis, dorsal; (d) schematic of lateral penis; (e) from Colombia; (f) from Colombia, pars distalis, lateroapical; (g) from Costa Rica, pars distalis ventral, with calyx; (h) from Ecuador, pars distalis inflate. (i) Metatarsus III showing the division astragalus/calcaneus and the slightly incrassate calcaneus. Scale bar: d = 1 mm. Abbreviations: Ag, astragalus; As, acute setae; Ca, calcaneus; Co, conductors; Cx, calyx; Fo, follis; Fs, foliar setae; Pb, pars basalis; Pd, pars distalis.

Taxonomy

• Venter: Without remarkable features; tracheal spiracles not concealed. • Chelicerae (Figures 4.39a,b): Hypertelic in both sexes; basichelicerite lengthened, without conspicuous bulla, and it can be armed with a strong spiniform apophysis. • Pedipalps: (Figure 4.39a): Strong, enlarged, armed in all segments, and with the tarsus highly reduced respective to tibia. Coxae lengthened, strongly developed, and heavily armed with spiniform apophyses (strongest in the dorsum); trochanter ventrally with three setiferous tubercles and dorsally with two. Femur enlarged with a ventral row of spiniform apophyses and two ectal and two mesal setiferous tubercles of short setae, some species with dorsal armature. Tibia enlarged, armed with ventral spiniform apophyses and setiferous tubercles; most species show medially a pair of characteristic setiferous tubercles with pedestal enlarged and rounded. Tarsus reduced, armed with setiferous tubercles of long setae. • Legs: Relatively short (usually for a body length around 5 mm, legs I–IV measure 12:17:12:15 mm) without relevant armature; metatarsi divided into astragalus/calcaneus (Figure 4.39i), without tarsal process and scopula. Tarsal formula: 6–8:9–14:6:6–7. • Genitalia: Truncus cylindrical, in some species with globous pars distalis, without a well-defined ventral plate as in Gonyleptoidea (Figure 4.39d). Pars distalis with foliar or pointed setae (Figures 4.39c,e–h). Apex of the pars distalis whole (Figure 4.39c) or divided (Figure 4.39f), convex or concave, some ending up to form a calyx (Figure 4.39g). Follis exposed (Figures 4.39e,f), internally upholstered with digitiform projections that grant it a grooved appearance to the clinical microscope (Figures 4.39c,h). Capsula interna eversible with two rigid conductors (Figure 4.39e), which can be tubular or laminar (Figure 4.39c) and in some species can present apophyses and/or projections. • Color: Typical of litter-dwelling species; can vary from a very dark brown, almost black, to a light orange brown in the troglobitic species. Some species show lighter coloration coincident with the mesotergal areas. An interesting variegate arborescent coloration has been observed in the mesotergal scutum that stretches from groove I to the posterior margin. • Sexual dimorphism: Weak. Males with slight widening of the calcaneus of the metatarsus III and accentuation of the armature of the pedipalps, fundamentally in the dorsal coxa and ventral femur. Some males can present accentuated cheliceral hypertely. Distribution: Neotropical: Mexico, Belize, Costa Rica, Panama, Cuba, Jamaica, U.S. Virgin Islands, Puerto Rico, Trinidad and Tobago, Colombia, Venezuela, Ecuador, Peru (new record), and Brazil. Nearctic: USA (southern Florida; the reference from Ohio is a misidentification), Mexico (Tamaulipas). Indomalay: Indonesia, Malaysia. The stygnommatids sensu stricto are exclusively Neotropical, from Costa Rica, Panama, Colombia, Venezuela, Ecuador, Peru, and the Brazilian Amazonia, with a species from Trinidad and Tobago.

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Relationships: Stygnommatidae belongs to Samooidea; it is closest to Samoidae, Biantidae, and Podoctidae, characterized by the penial internal capsule completely eversible with two separate or fused conductors. The position inside this group is little understood. Main references: • Systematics: Roewer (1923), Goodnight & Goodnight (1951), GonzálezSponga (1987), Kury & Cokendolpher (2000), Kury (2003). • Natural history: Goodnight & Goodnight (1951), González-Sponga (1987).

Stygnopsidae Sørensen, 1932 Amanda C. Mendes and Adriano B. Kury Etymology: Stygnopsis, from preexisting genus Stygnus and Greek opsis (aspect, appearance). Characterization: • Size: From medium to large sized; body length 2.5 (Karos) to 7 mm (Hoplobunus). • Dorsum (Figures 4.40a,c–f): Outline of dorsal scutum subrectangular, constricted at scutal groove; in Karos carapace much narrower, giving the body a pyriform shape. Lateral margin of scutum projected to the sides, forming a pair of lobes in Karos, Paramitraceras, and Sbordonia. Mesotergum clearly divided into four areas; sometimes third and fourth fused entirely or partially; none of them divided by a longitudinal groove. All scutal areas unarmed except area III, armed with a pair of paramedian spines in Stygnopsis, and area IV with an unpaired backward-directed spine in Karos. Free tergites all unarmed. Granulation varied; dense cover in Karos, Paramitraceras, and Sbordonia. Common ocularium always present as a high cone, situated more or less near the anterior margin of the carapace, armed with an unpaired spine, sometimes reduced or missing (blind species). In Karos the ocularium is low, more removed from the anterior margin of the carapace, armed with two pointed tubercles. • Venter (Figure 4.40b): Maxillary lobe of coxa II lacking. Spiracles clearly visible. Spiracular area well detached from coxa IV. Spiracular area T shaped except in Paramitraceras, where it is very short, almost like a sternum of Bothriuridae. Coxae I–IV densely granulous, granules growing stouter from IV to I, especially in Hoplobunus and Stygnopsis, where granulation of coxa I is heavy. • Chelicerae: Basichelicerite very long (almost as long as the carapace, Figure 4.40a), granulous, and without developed bulla in Hoplobunus and Stygnopsis; short in Karos (Figure 4.40c). In Paramitraceras and Sbordonia the bulla is very stout and spiny. Cheliceral hand not swollen in Karos, moderately swollen in Paramitraceras, Stygnopsis, and Hoplobunus, and immensely swollen in Sbordonia.

Taxonomy

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Figure 4.40. Stygnopsidae. (a–b) Hoplobunus boneti, male habitus (Mexico): (a) dorsal; (b) ventral. (c) Karos rugosus: male habitus, dorsal (from original description). (d) Stygnopsis valida, female dorsal (Mexico) (photo: A. B. Kury). (e) Hoplobunus queretarius, lateral of male (Mexico, from original description). (f) Sbordonia sp.n., male dorsum (Honduras). (g–h) Hoplobunus boneti, distal part of penis, dorsal and lateral (Mexico). (i) Paramitraceras granulatus (Mexico): male, distal part of penis, dorsal. (j–k) Stygnopsis valida (Mexico), male, distal part of penis: (j) dorsal; (k) laterodorsal (photos: D. Ubick). (l) Karos sp., male, glans, lateral (photo: A. L. Tourinho). Scale bars: a, c, f = 1 mm; g–i = 0.1 mm.

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• Pedipalps: Segments short, elongate (especially patella and tibia) in Stygnopsis and Hoplobunus (Figures 4.40d,e). Tibia and tarsus always armed with mesoventral and lateroventral spines. Femur with dorsal and ventral row of tubercles, much larger in Sbordonia. In Karos granules are densely clustered, not forming rows. Tarsus and tibia laterally projected as a keel in Paramitraceras and Sbordonia. • Legs: Very long or short. Tarsal formula: 4–7:10–17:6–8:7–10. Tarsus with smooth double claws, without scopulae or pseudonychium. Trochanter III moderately to strongly inflated. • Genitalia (Figures 4.40g–l): Ventral plate of penis not well defined: setiferous region not greatly flattened; it starts cylindrical as the rest of the truncus and grows thinner apically, where it may be divided into two revolving lobes. Setae are typically long, but may be very short, as in Stygnopsis. Ventral and ventrolateral setae are numerous and not arranged in rows. There is a pair of setae flanking the follis. Dorsal part of setiferous region of truncus is excavated, bearing the follis, which is well developed, multifolded, and covered with numerous small spines in the apical region. The follis appears to be partially eversible to expose the stylus, which is inserted in it. • Color: Dark brown to black, appendages much lighter. Many troglomorphic species are pale light brown. • Sexual dimorphism: The armature of the fourth leg in females is reduced in comparison with that of males, and their chelicerae, although enlarged, are smaller than those of the males. Distribution: Stygnopsidae is mostly Mexican, with records from the southern USA (Hoplobunus), Guatemala, El Salvador, and Belize (Paramitraceras). This places them in the region intermediate between the Nearctic and Neotropical realms, although their affinities are clearly Neotropical (Kury, 1997c). The record of Paramitraceras from Colombia (Flórez & Sanchez, 1995) is mistaken (see Kury, 2003). As in other Laniatores, most species have narrow distributions. Relationships: Kury (1993a) proposed a sister-group relationship to Epedanidae, although later (1997c; Kury & Cokendolpher, 2000) he considered that Epedanidae could be the sister group to a broader Gonyleptoidea including also Assamiidae and that Stygnopsidae would be the sister group to the rest of Gonyleptoidea. Main references: • Systematics: Roewer (1923), Sørensen (1932), Goodnight & Goodnight (1942b, 1944, 1953b), Silhavy (1974, 1977), Kury (2003). • Natural history: Silhavy (1974, 1977).

Taxonomy

Synthetonychiidae Forster, 1954 Adriano B. Kury Etymology: Synthetonychia, from Greek synthetos (compounded, composite) and onychion, diminutive of onyx (claw). Characterization: • Size: Dorsal scutum between 1.0 and 1.7 mm long. Legs I–IV 2.2–3.6/3.1– 5.2/2.6–4.3/3.2–5.4 mm long. • Dorsum: Dorsal scutum pyriform in dorsal view (Figure 4.41a), hemispherical in lateral view (Figure 4.41b), with eyes far away from the frontal border. Grooves separating the areas absent. Ocularium lacking, but the eyes are placed close together. • Chelicerae: Not swollen; basichelicerite very short, without noticeable bulla. Hand with a few minute tubercles. • Pedipalps (Figures 4.41c,d): Without keels, processes, or spines, only a few scattered minute setae. In some species trochanter of male has stout ventral and dorsal processes. Pedipalpal tibia of male slender and tarsus still more slender and elongate. Pedipalp of male with a dorsoapical process in tibia and a ventral subapical stout spine in tarsus. • Legs: Smooth and unarmed. Tarsal claws III–IV bear a complex structure (Figures 4.41e–g), called “synthetonychium” and comparable with the peltonychium of the Travuniidae. Median prong is large and flattened. There are numerous strongly developed lateral prongs and usually a small accessory tooth. Tarsal formula: 3:5:4:4. • Genitalia: Penis (Figures 4.41h–j): with muscle extending entire length of truncus. Dorsolateral plates reduced to two lobes pointing dorsally. Ventral plate typically tongue shaped, strongly concave ventrally, with two pairs of setae. Stylus very long, with two parastyli (when present) fused along threefourths of its length. • Color: Body background yellowish brown to reddish brown, sometimes shaded in black. Chelicerae and pedipalps with dense black reticle. Legs may have darker and lighter rings. • Sexual dimorphism: Shown in pedipalps and shape of the genital operculum. Distribution: Endemic to New Zealand. Relationships: Forster (1954), when describing the family, stated, “I consider this family to be most closely related to the Triaenonychidae.” Martens (1986) also defended this point of view and went a bit further, stating (my translation): “Regarding their male genital morphology, they are very close to Triaenonychidae. Perhaps this family is a side branch of the New Zealand Triaenonychidae, with which they share the degree of reduction of armature of glans. The familial status, granted mainly by the aberrant habitus, is probably not sustained.” Briggs (1971b, Figure 1) included Synthetonychiidae in his phylogenetic tree of Travunioidea, making it arise straight

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g Figure 4.41. Synthetonychiidae. (a) Synthetonychia minuta (New Zealand), habitus without appendages, dorsal. (b) Undetermined (New Zealand), habitus, lateral view. (c–d) S. cornua (New Zealand): (c) male pedipalp, ectal view; (d) female pedipalp, ectal view; (e– g) Synthetonychia spp. (New Zealand), examples of of tarsi IV different synthetonychia: (e) S. glacialis; (f) S. oparara; (g) S. acuta. (h–j) Undetermined from New Zealand, penis: (h) Dorsal, (i) ventral, (j) lateral views. a, c–g modified from Forster (1954); b, h–j from Martens (1986).

Taxonomy

from the “hypothetical ancestral travunoid” in the same way as Travuniidae and a clade composed of all other taxa. Suzuki (1975b) kept this arrangement, changing only internal relations in Triaenonychidae. Hunt and Hickman (1993) called the synthetonychiid claw a peltonychium, implying that it is homologous with the travuniid claw. According to a preliminary analysis (Kury, 2002), Synthetonychiidae form a clade with the Southern Temperate Triaenonychidae. This implies an independent acquisition of such a complex structure as the peltonychium or, in other words, that the synthetonychium is not homologous with the peltonychium. Main references: • Systematics: Forster (1954), Martens (1986). • Natural history: Forster (1954).

Travuniidae Absolon and Kratochvíl, 1932 Adriano B. Kury Etymology: Travunia is the Latin name of the city of Trebinje, Bosnia and Herzegovina. Characterization: • Size: Small Laniatores, 1–3 mm. • Dorsum (Figure 4.42a): Body convex, mostly rounded posteriorly, only slightly constricted in anterior third. Frontal border of carapace unarmed. Segments of body ill marked by incomplete grooves, mostly lacking. All areas, tergites, and sternites unarmed. Ocularium, when present, low, granular, far from the frontal border of the carapace. Eyes may be reduced and depigmented. Ninth tergite and lateral free sclerites (Figure 4.42p) present in non-European genera. • Venter: Sternum wedge shaped (Figure 4.42h). • Chelicerae: Basichelicerite slender, with only scarce dorsal ornamentation of tubercles. Cheliceral hands never swollen. • Pedipalps: Pedipalps robust and strongly spined, femur dorsally convex, with ventral row of setiferous tubercles and mesal subapical setiferous tubercle (Figure 4.42i). • Legs: Tibia and tarsus with powerful mesal and ectal setiferous tubercles. Setae inserted subdistally in sockets. Legs I–IV slender and unarmed. Claws III–IV with peltonychium (complex claw formed by central shield and many pairs of lateral branches, sometimes asymmetrical) attached to a stem at distal part of tarsus (Figures 4.42b–g). Tarsal formula: 3–6(2–3):5–6(3–4):4:4; only Travunia has such high counts as 6(3) in leg I; other genera have 3–5(2). • Genitalia: Penis (Figures 4.42j–n) with musculature often reduced to basal portion of truncus (Figures 4.42j–l). Glans with sclerites fused including the stylus. Ovipositor unsegmented, four-lobed, with only scattered setae (Figure 4.42o).

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a

b

c

d Figure 4.42. Travuniidae. (a) Travunia anophthalma, dorsal scutum (redrawn from Absolon & Kratochvíl, 1932c). (b) Peltonychial claw of leg IV in lateral view from Travunia anophthalma distitarsus and claw (redrawn from Absolon & Kratochvíl, 1932c). (c–g) Examples of adult peltonychial claw in dorsal view: (c) leg III, Abasola borisi; (d) leg IV, Abasola borisi; (e) Dinaria vjetrenicae; (f) Travunia anophthalma; (g) Yuria pulchra. Redrawn from several sources (Absolon & Kratochvíl, 1932; Roewer, 1935a; Hadˇzi, 1973; Suzuki, 1975a). (h) Abasola troglodytes, sternum, coxae and stigmatic area, ventral view (redrawn from Roewer, 1935a). (i) Peltonychia leprieuri, right pedipalp, mesal (from Martens, 1978b). (j–n) Penis: (j) Dinaria vjetrenicae, distal part, ventral; (k–n) Peltonychia postumicola, dorsal, lateral, distal dorsal and distal lateral (from Martens, 1976, 1978b, 1986, and Suzuki, 1975a, respectively). (o) Peltonychia clavigera, ovipositor (from Martens, 1978b). (p) Yuria pulchra, view of free abdominal sclerites (from Suzuki, 1975a).

e

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• Color: Color in general uniform dark yellow to pale yellow; troglobites are depigmented. • Sexual dimorphism: No secondary sexual dimorphism. Distribution: Europe, Japan, and USA. The records for Slovenia are erroneous (Novak & Gruber, 2000).

Taxonomy

Relationships: Branched claws are present in most Triaenonychidae, but the peltonychium as a unique complex claw would be a potential synapomorphy for the genera of Travuniidae. However, similar structures develop in many apparently unrelated Travunioidea such as Synthetonychiidae (Forster, 1954), some Australian Triaenonychidae of the genus Lomanella (Hunt & Hickman, 1993), and the Argentinean troglobite triaenonychid Picunchenops (Maury, 1988). The monophyly of Travuniidae is not corroborated by any unique structure, but even so the presence of the peltonychium could be a synapomorphy (convergent in other Travunioidea). Travuniidae is most closely related to Cladonychiidae because the musculature of the penis is restricted to the base and the complex of the glans is short, with all median and dorsal components fused in a single structure. It is possible that Travuniidae is paraphyletic with respect to Cladonychiidae because some of its genera (at least Peltonychia) appear closer to this family in genital morphology. The replacement of the peltonychium for a cladonychium could be a synapomorphy for Cladonychiidae in a scenario of a paraphyletic Travuniidae. The presence of additional opisthosomal sclerites in the genera Yuria and Speleonychia is a retention of a plesiomorphic state, shared with Pentanychidae. This would add support to a paraphyletic Travunioidea, but would need an extra ad hoc hypothesis of independent loss of those sclerites in other Travuniidae plus Cladonychiidae and in all other Laniatores. Main references: • Systematics: Absolon & Kratochvíl (1932a,b), Hadzi (1935), Roewer (1935a), Suzuki (1975a), Martens (1980). • Natural history: Suzuki (1975a), Marcellino (1982).

Triaenonychidae Sørensen, 1886 Adriano B. Kury Etymology: Triaenonyx, from Greek triaina (trident, three-pronged fish spear) and onyx (claw). Characterization: • Size: Medium-sized Laniatores; body length typically 3 to 5 mm, although some South African Triaenonychinae can be much smaller (down to 1 mm), and on the other side some Adaeinae are much larger (up to 10 mm). Legs I– IV almost always short, 4–7/6–12/4–8/6–10 mm long. • Dorsum (Figures 4.43a–c): Dorsal scutum width increasing backward without major constriction. Mesotergum seldom clearly divided into areas by grooves; usually areas are marked by arrangement of tubercle rows. No areas fused. Armature of areas and tergites usually weak, formed by small paired acuminate spiniform tubercles. Ocularium usually present, mostly very narrow and high with unpaired armature (Figure 4.43o). Ocularium lacking sometimes, and eyes are sessile, placed close together. Eyes elevated, much higher than the level of the carapace (Figure 4.44h). Anterior margin of cara-

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a

d

e b Figure 4.43. Triaenonychidae. (a) Holonuncia katoomba from Australia, habitus lateral (from Hunt, 1992); (b–c) South African Adaeinae, schematic granulation of Adaeulum (b) and Larifuga (c) (from Lawrence, 1933). (d–e) Araucanobunus juberthiei from Chile, coxae, sternum, and genital opercle of male and female (from Maury, 1993). (f– h) Typification of outlines of sternum of the three tribes of Triaenonychinae: (f) Triaenonychini; (g) Adaeini; (h) Triaenobunini (redrawn from Forster, 1954). (i–m) Further elaboration on the sternum outline of genera of South African Adaeini: (i) Montadaeum; (j) Larifuga; (k) Paradaeum; (l) Adaeulum; (m) Cryptadaeum (redrawn from Lawrence, 1931). (n) Undetermined Triaenobuninae from Chile showing complex ornamentation of tubercles of dorsal scutum; (o) detail of carapace tubercle (photos: A. B. Kury). Scale bar: a = 1 mm.

c i

j

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g f

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pace with rows of spines (Figures 4.43b,c, 4.44n). Ozopores hidden by a padshaped apophysis of coxa II. • Venter: Coxae (Figures 4.43d,e) more or less parallel, coxa IV not greatly enlarged. Spiracles sometimes concealed by tubercles. Shape of sternum extremely variable (Figures 4.43f–m). • Chelicerae: Hands usually not swollen and basichelicerite rarely with dorsal ornamentation of tubercles, but mesal pointed tubercles are common (Figure 4.44e).

Taxonomy

c

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d

f g a

b

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j l

i

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k

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Figure 4.44. Triaenonychidae. (a–b) Araucanobunus juberthiei from Chile, penis, ventral and lateral (from Maury, 1993). (c–d) Ceratomontia mendocina from Argentina, penis, lateral and ventral (from Maury & Roig Alsina, 1985). (e–g) Graemontia natalensis from South Africa: (e) chelicera, mesal; (f) pedipalpal femur, mesal; (g) leg I, mesal (from Lawrence, 1937a). (h) Ankaratrix illota from Madagascar, ocularium, lateral (from Lawrence, 1959). (i) Pristobunus henopoeus from New Zealand, habitus dorsal (from Forster, 1954). (j) Undetermined, from Madagascar, ozopore arrowed (photo: A. B. Kury). (k) Holonuncia cavernicola from Australia, metatarsal notch (from Hunt, 1992); (l–p) Lomanella spp. posterior claws (from Hunt & Hickman, 1993). (q) Undetermined from Madagascar, typical three-pronged claw (photo: A. B. Kury).

• Pedipalps: Large, much stronger than legs, not crossed in the region of the trochanter. Armed with ventromesal and ventroectal spines in patella-tibiatarsus (Figure 4.43a). Femur variedly armed with apophyses and spines, ventrally in many genera with strip of fine beadlike granules. Tibia and tarsus do not form a subchela. • Legs: Usually short, substraight, and armed only with tubercle rows. Large, elaborate apophyses never present. Coxa I ventrally with strong frontal apophyses. Femur I in many species armed with ventral and/or dorsal rows of

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setiferous spiniform processes (Figure 4.44g). Metatarsus I may be notched in males and provided with strong setae. Tarsi I–II with a single claw, III–IV with a multifurcate (usually trifurcate) claw (Figure 4.44q). Tarsal formula: 2–3(1– 2):2–20 (usually 2–4):3–4:3–4. • Genitalia (Figures 4.44a–d): Truncus penis filled with a single muscle. Glans very complex, with a full complement of noneversible sclerites, including a dorsal plate, dorsolateral plates, and a ventral plate. These are rarely found together in the same species. Sometimes the stylus is extremely elongate, and plates and spines may be fused with it. • Color: Background usually yellowish, orange, or dark brown, with black mottling and reticulation. No white markings on dorsal scutum. • Sexual dimorphism: Manifested typically in pedipalps, which in males are stronger and incrassate. In a few species chelicerae of males have supplementary spatulate mesal apophyses. Leg I tarsomeres in females may be slightly lower. In many species males possess a notch in metatarsus I. Also in some species the ocularium of males is more developed than that of females. The genital operculum may be elongate in males and wider in females. Male dimorphism (poeciloandry) reported by Forster (1954), Hunt (1985), and Maury and Roig Alsina (1985), where some males have secondary dimorphic features only weakly developed, though genitalia are normal.

Key to subfamilies 1. Tarsal claws III–IV in adults with two to three pairs of accessory lateral branches. ......................................................................2 . Tarsal claws III–IV in adults with one pair of accessory lateral branches . . . . . . . 4 2. Tarsal claws III–IV in juveniles with three pairs of accessory lateral branches. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Paranonychinae . Tarsal claws III–IV in juveniles with four to five pairs of accessory lateral branches. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 3. Tarsal claws III–IV in juveniles with four pairs of accessory lateral branches. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Kaolinonychinae . Tarsal claws III–IV in juveniles with five pairs of accessory lateral branches . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nippononychinae 4. Side branches of claws III–IV in adults much shorter than median prong . . . . . . 5 . Side branches of claws III–IV in adults equal in length to or larger than median prong . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sørenseniellinae 5. Diverticulum tertium of midgut with three diverticula. . . . Triaenonychinae (6) . Diverticulum tertium of midgut with two diverticula . . . . . . . . . . Sclerobuninae 6. Sternum slender, with a spear-shaped anterior expansion and lateral expansions posteriorly. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . undetermined tribe

Taxonomy

. Sternum subtriangular or wedge shaped, without anterior and posterior expansions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Adaeini 7. Width of posterior expansion much less than length of sternum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Triaenonychini . Width of posterior expansion equal to or greater than the length of the sternum. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Triaenobunini Distribution: USA, Canada, Aleutian Islands (Umnak and Atka), Japan, Korea, Tasmania, continental Australia, New Zealand, subantarctic islands Crozet, Auckland, and Campbell, Madagascar, Chile, Argentina, and southern Brazil. Some triaenonychid genera are distributed across the Austral continents; the possibly nontriaenonychids of the Boreal temperate region also cross continents (Paranonychinae; see Shear, 1986). Relationships: In Chapter 3 it is suggested to split Triaenonychidae, as traditionally conceived, into at least two different families. The Boreal genera should be grouped with Travuniidae, while the Austral genera represent Triaenonychidae sensu stricto and may include the strange Synthetonychiidae (Kury, 2002). Main references: • Systematics: Pocock (1902b), Roewer (1915b, 1931), Hickman (1958), Briggs (1971a), Suzuki (1975b, 1976e). • Natural History: Lawrence (1938), Hunt (1972), Maury (1988).

Zalmoxidae Sørensen, 1886 Adriano B. Kury and Abel Pérez González Etymology: Zalmoxis is the name of a Thracian Dacian god. Characterization: • Size: Small Laniatores. • Dorsum and venter: Dorsal scutum campaniform, tending to pyriform (see Figures 4.45a–c,g). Ocularium well developed, unarmed or with small tubercles, far removed from frontal margin of carapace (Figures 4.45a–c,g). Frontal hump of carapace absent. Scutal area I usually longer than the others. Mesotergal grooves often V shaped. Scutal areas unarmed or with transverse rows of hair-tipped tubercles (Traiania) and armed with paramedian spines; free tergites and sternites unarmed or with transverse row of pointed tubercles (or median spiniform apophyses, as in Stygnoleptes analis). • Chelicerae (Figure 4.45e): Weakly developed, basichelicerite short, with wellmarked bulla, hand commonly small. • Pedipalps (Figure 4.45f): Segments short and stout, never elongate. Femur with two ventrobasal setiferous tubercles and a mesal subdistal setiferous tubercle. Patella with mesal subdistal spine. Tibia and tarsus with mesal ventral and ectal

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Figure 4.45. Zalmoxidae. (a) Protodiasia saltensis from Argentina, male, habitus dorsal (from Ringuelet, 1959). (b) Ethobunus cubensis from Cuba, male, habitus dorsal (from Sˇilhavy´, 1979). (c–d) Zalmoxis lavacaverna from Australia, male, habitus, dorsal/lateral views (from Hunt, 1993). (e–f) Cersa kratochvili from Cuba, chelicera/pedipalp, lateral views (from Sˇilhavy´, 1979). (g) Sphoeroforma familiaris from Venezuela, male, habitus dorsal (from González-Sponga, 1987). (h–j) Zalmoxidae, Fissiphalliidae, Icaleptidae, respectively, schematic view of movement of penis (from Kury & Pérez G., 2002). (k) Minuides milleri from Cuba, distal part of penis, lateral (from Sˇilhavy´, 1978). (l–m) Gjellerupia sp. from Papua New Guinea, distal part of penis, ventrolateral and dorsolateral (photos: P. Fong). Abbreviations: Pe, pergula; Ru, rutrum; St, stragulum; Sy, stylus; Tr, truncus; VP, ventral plate.

ventral rows of two to four setiferous tubercles. Some species with tibia incrassate in males and lanceolate setae, as in genus Absonus from Venezuela. • Legs: Usually rather short, densely covered with minute granules. Leg IV with different manifestations of sexual dimorphism in all podomeres but coxa and tarsus. Coxa IV without dorsoapical spine. Tarsal formula: 3(2):6–8(3):5–6:6. Tarsal process present in a few species from Venezuela. • Genitalia (Figures 4.45h,k–m): Capsula externa visible, well developed and modified into a stragulum (new name, from Latin stragulum, a spread, covering, bedspread), articulated to the truncus like a jackknife. Morphology of

Taxonomy

the capsula interna unknown in most species, in some of them simple without two laminar conductors. Lamina ventralis divided into two tagmata: (1) the distal rutrum (from Latin ru¯trum, a spade, shovel), which is hammer shaped or spade shaped, usually bearing two pairs of paramedian setae, and (2) the basal pergula (from Latin pergula, a projection or shed in front of a house, used as a booth, stall, shop), which is a girdle bearing two to four pairs of erect setae, which may be very elongate (e.g., in Minuides and Sphoeroforma both new familial assignment). The stylus is exposed by the bascule movement of the stragulum (Figures 4.45h–j). • Color: From dark brown to dark yellow background with varied darker mottling to pale yellowish in small edaphic species. • Sexual dimorphism: Some species such as Soledadiella macrochelae and Phalangoduna granosa show hypertelic sexually dimorphic chelicera. Leg IV with stronger spines in male femur IV. Femur IV may be variedly curved and with different parts thickened in males. Patella IV in a few species clavate with stout spines in male. Tibia IV of male incrassate distally with two ventral parallel rows of spines. Metatarsus IV occasionally sinuous in male. Leg IV elongate in males (Pachylicus, some Ethobunus), pedipalpal tibia swollen, basitarsus III swollen, femur III incrassate, with porose (glandular?) area as in Minuides. Silhavy (1978) described a new type of stridulatory apparatus for a new Cuban species of Minuides; nevertheless, we have had the opportunity to study Silhavy’s type and see that the “stridulatory apparatus” was in fact the porous area that appears also in the ocularium of the species. These porous regions are found in diverse Zalmoxoid/Samooid species (such as the Baculigerus group in Escadabiidae and Costabrimma spp). Distribution: Disjunct distribution. Many species in Neotropics, from Costa Rica to Brazil. Southern limit is uncertain; on the Atlantic coast it appears to be northern Rio de Janeiro State. In Australasia, from Papua New Guinea to Pacific islands and Australia. Afrotropical: Seychelles and Mauritius, but the species from Madagascar do not belong here. Not recorded from mainland Africa. In Indo-Malaya mostly in the Philippines and Indonesia. Relationships: Zalmoxidae are surely closely related to Fissiphalliidae and Icaleptidae (Figures 4.45i,j) because of the presence of a stragulum. Fissiphalliidae clearly show the modification of the ventral plate into a pergula and a rutrum, the main synapomorphic character of Zalmoxidae. The decision to keep Fissiphalliidae as a family was adopted because of the peculiar form of the enlarged fingerlike stragulum, which is only an autapomorphy at that level. The recognition of higher-level synapomorphies uniting Fissiphalliidae with Zalmoxidae, but no currently recognized synapomorphy for Zalmoxidae, only potentially threatens the unity of this family. In order to detect monophyletic groups inside Zalmoxidae, it is necessary to evaluate the importance of details of pergula + rutrum such as their shape and position, as well as the form of the stragulum. If exclusive derived character states for Zalmoxidae are not found, the adequate decision would be to merge

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Fissiphalliidae into Zalmoxidae. Meanwhile, hundreds of obscure species with tiny, complex, and hard-to-interpret male genitalia are waiting for study, one of the hardest challenges to opilionologists. Main references: • Systematics: Sørensen (1886), Roewer (1912b, 1923), González-Sponga (1987), Starega (1989), Kury & Cokendolpher (2000), Kury (2003). • Natural history: González-Sponga (1987).

ACKNOWLEDGMENTS The authors thank the anonymous reviewers and authors for useful comments and suggestions on other families’ sections. The following people and institutions provided funding or resources or helped authors improve their sections: Leon Baert; Renner Baptista; H. Bürgis; CAPES; Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq); Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP); Fundação Universitária José Bonifácio (FJUB); Alessandro Giupponi; Randall Gutiérrez; Marcos Hara; Glenn S. Hunt; Peter Jäger; Laura Leibensperger; Christian Komposch; Jochen Martens; Juan Mata; Mt Albert Landcare Research (Auckland); National Science Foundation, USA (NSF); Norman Platnick; Maria Rambla; Seito Suzuki; Osvaldo Villareal; Carlos Víquez; Humberto Yamaguti; the Zoological Society of Japan. Abel Pérez González was recipient of an Ernst Mayr Travel Grant from the Museum of Comparative Zoology.

CHAPTER

5

Paleontology Jason A. Dunlop

D

espite the diversity of living Opiliones, relatively few fossil harvestmen have been described. The principal reason for their rarity in the fossil record is that, like other arachnids, harvestmen lack a mineralized exoskeleton. This means that they can only become preserved under special environmental conditions, and it forces us to reconstruct the history of the group over geological time on the basis of only a small number of “windows” of exceptional preservation. Harvestmen are terrestrial animals; thus in many cases preservation was only possible in circumstances where they fell into, or were washed into, a body of water with high rates of sedimentation that buried the animal quickly. Alternatively, a harvestman had to blunder into sticky tree resin that trapped the animal and eventually solidified and turned into amber. The most important fossil sites for harvestmen are detailed in this chapter. It should be added that there are some arachnid fossils that were not originally recognized as harvestmen, but that nevertheless belong to Opiliones (Table 5.1). Conversely, other fossils have at some stage been interpreted as harvestmen (e.g., Phalangites), but careful restudy has shown that they belong to other animal groups (Table 5.2). Another important point to note is that a substantial number of fossil harvestmen in the literature remain only partially described. For example, an Australian Mesozoic specimen has only been tentatively assigned to a higher taxon, and there are various reports of undescribed amber and Florissant shale material that clearly merit further study. The last comprehensive summary of fossil Opiliones was Petrunkevitch’s (1955) contribution to the Treatise on Invertebrate Paleontology. A number of new taxa and/or fossil occurrences have been documented since that time, and other useful reviews or summaries include Starega (1976a, 2002), Cokendolpher and Cokendolpher (1982), Cokendolpher (1987a), Selden (1993a,b), Selden and Dunlop (1998), and Giribet and Dunlop (2005). 247

Eupnoi (?) Eotrogulidae Nemastomoididae Nemastomoididae Eupnoi (?) Dyspnoi (?) Eupnoi (?)

Eotrogulus fayoli

Nemastomoides elaveris

Nemastomoides longipes

Kustarachne tenuipes

Echinopustulus samuelnelsoni

Unnamed example

Dyspnoi

Halitherses grimaldii

Trogulidae Samoidae (?) Kimulidae Samoidae Caddidae Gyinae

Trogulus longipes

Philacarus hispaniolensis

Kimula sp.

Hummelinckiolus silhavyi

Caddo dentipalpis

Dicranopalpus ramiger [= Opilio corniger] [= Dicranopalpus palmnickensis]

CENOZOIC

Eupnoi (?)

Unnamed example

MESOZOIC

Eupnoi

Brigantibunum listoni

Affinities

Eophalangium sheari

PALEOZOIC

Taxa

Eocene

Eocene

Eocene

Eocene

Eocene

Eocene

Upper Carboniferous

Lower Carboniferous

Upper Carboniferous

Upper Carboniferous

Upper Carboniferous

Upper Carboniferous

Upper Carboniferous

Upper Carboniferous

Lower Carboniferous

Lower Devonian

Age

suprageneric rank to which each fossil has been assigned is also indicated.

Baltic amber

Baltic amber

Dominican amber

Dominican amber

Dominican amber

Geiseltal, Germany

Myanmar amber

Koonwarra, Australia

Montceau-les-Mines, France

Western Missouri, USA

Mazon Creek, USA

Mazon Creek, USA

Commentry, France

Commentry, France

East Kirkton, Scotland

Rhynie, Scotland

Locality

MB.A.

MB.A.

PAC

PAC

PAC

GM

AMNH

Unknown

MHNM

YPM

USNM

YPM

MNHM*

MNHM

GLAHM

PBM

Repository

Koch & Berendt, 1854; Menge, 1854;1 Roewer, 19392

Koch & Berendt, 18541

Cokendolpher & Poinar, 1998

Cokendolpher & Poinar, 1992

Cokendolpher & Poinar, 1992

H. Haupt, 1956

Giribet & Dunlop, 2005

Jell & Duncan, 1986

Dunlop, 1996b

Dunlop, 2004a

Scudder, 1891; Petrunkevitch, 1913

Petrunkevitch, 1913

Thevenin, 1901

Thevenin, 1901

Dunlop & Anderson, 2005

Dunlop et al., 2004

Main references

Table 5.1 Summary of the known fossil harvestmen in the literature, arranged stratigraphically from oldest to youngest. The family or lowest

Sclerosomatidae Sironidae Leiobuninae Leiobuninae Samoidae Phalangiidae

Unnamed example

Siro platypedibus

Amauropilio atavus

Amauropilio lacoei

Pellobunus proavus

Phalangium sp.

Quaternary

Miocene

Oligocene

Oligocene

Eocene (?)

Eocene (?)

Eocene

Oligocene

Eocene

Eocene

Eocene

Eocene

Near Rome, Italy

Dominican amber

Florissant, USA

Florissant, USA

Bitterfeld amber

Bitterfeld amber

Baltic amber

Florissant, USA

Baltic amber

Baltic amber

Baltic amber

Baltic amber

Baltic amber

Baltic amber

Baltic amber

Unknown

USNM

USNM

AMNH

MB.A.

AMRD

MB.A.

MCZ

Gdansk, ´ Poland*

MB.A.

MB.A.

MB.A.

Gdansk, ´ Poland*

Gdansk, ´ Poland*

MB.A.*

Mastororill, 1965

Cokendolpher, 1987a

Petrunkevitch, 1922

Cockerell, 1907

Dunlop & Giribet, 2003

Barthel & Hetzer, 1982

Koch & Berendt, 1854; Ubick & Dunlop, 2005

Petrunkevitch, 1922

Menge, 1854; Roewer, 1939

Koch & Berendt, 1854

Koch & Berendt, 1854; Roewer, 1939

Koch & Berendt, 1854

Menge, 1854; Roewer, 1939

Menge, 1854

Koch & Berendt, 1854

Abbreviations of the repositories are as follows: American Museum of Natural History, New York (AMNH); Amber Museum, Ribnitz-Darmgarten, Germany (AMRD); Hunterian Museum, Glasgow (GLAHM); Geiseltalmuseum of the Martin-Luther-Universität Halle-Wittenberg, Germany (GM); Palaeontology Department, Museum für Naturkunde, Berlin (MB.A.); Museum of Comparative Zoology, Harvard University (MCZ); Museum d’Histoire Naturelle de Marseille (MHNM); Muséum National d’Histoire Naturelle, Paris (MNHN); Poincar Amber Collection (PAC); Paleobotany Section, Münster University, Germany (PBM); Smithsonian Institution, United States National Museum, Washington (USNM); Peabody Museum of Natural History, Yale University (YPM). An asterisk indicates that the type could not be traced and may be lost. 1. The types of both Koch and Berendt (1854) and Menge (1854) were reported as lost by Petrunkevitch (1958), at least with respect to the spiders. In fact, Koch and Berendt’s harvestman types are in the MB.A., and all of them except Opilio ovalis have been confirmed in this collection (Dunlop, 2006), where they have oxidized slightly and, with some exceptions, have become rather dark, opaque, and difficult to photograph. Menge’s material was originally held in the Westpreussische Provinzialmuseum, Danzig ´ Poland). After World War II the Gdansk ´ material seems to have become split up, but traces of it can be found in the Muzeum Ziemi in Warsaw and the Naturkunde (= Gdansk, Museum of Leipzig, Germany (Kosmowska-Ceranowicz, 2001). 2. Roewer’s types were part of the private collection of, Dr. Bachofen-Echt. His types of Sabacon bachofeni have been confirmed as being in the Naturwissenschaftliche Sammlung des Bayerischen Staates, Munich. Although Keilbach (1982) cites this same repository for Roewer’s other harvestman types, they could not be traced in Munich recently, or in the other known repository of Bachofen-Echt’s material in the Paleontological Institute of the University of Vienna.

Phalangioidea

Sabaconidae

Sabacon claviger

Cladonychiidae

Nemastomatidae

Nemastoma incertum

Petrunkevitchiana oculata

Nemastomatidae

Mitosoma denticulatum

Proholoscotolemon nemastomoides

Nemastomatidae

Histricostoma (?) tuberculatum

Eocene

Eocene

Phalangiidae (?) Sclerosomatidae

Cheiromachus coriaceus

Eocene

Phalangiidae (?)

Leiobunum longipes [= Leiobunum inclusum]

Opilio ovalis

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Table 5.2 Fossils erroneously or dubiously assigned to Opiliones Taxa

Real identity

Age

Locality

Main reference

Dinopilio gigas

Spider (?)

Upper Carboniferous

Rakonitz, Czech Rep.

Fritsch, 1904

Nemastomoides depressus

Phalangiotarbid

Upper Carboniferous

Mazon Creek, USA

Petrunkevitch, 1913

Rhabdotarachnoides simoni

Plant material (?)

Lower Permian

Rotliegend, Germany

H. Haupt, 1957

Hasseltides primigenius

Crinoid

Lower Jurassic

Solnhofen, Germany

Weyenbergh, 1869

Phalangites priscus

Crustacean

Lower Jurassic

Solnhofen, Germany

Münster, 1836

Unnamed example

Mite or tick (?)

Upper Cretaceous

NW France

Schlüter, 1978

Unnamed example

Crustacean or pycnogonid (?)

Upper Cretaceous

Sahel-Alma, Lebanon

Roger, 1946

Phalangopus subtilis

Spider

Eocene

Baltic amber

Menge, 1854

Amphitrogulus sternalis

Spider (?)

Oligocene

Aix-en-Provence, France

Gourret, 1886

Phalangillum hirsutum

Spider (?)

Oligocene

Aix-en-Provence, France

Gourret, 1886

Oligoopilionus aquaticus

Uncertain

Oligocene

Piatra Neamt, Romania

Ciobanu, 1977

This list does not include early monographs on fossil arachnids (reviewed by Pocock, 1911) in which the extinct arachnid orders Trigonotarbida (= Anthracomartida) and Phalangiotarbida (sometimes called Architarbida) were assumed by some authors to be subgroups within Opiliones.

HARVESTMAN ORIGINS The origins of harvestmen, like those of most arachnid orders, are uncertain, and even their sister group remains an unresolved and contentious issue (see Chapter 3). Relationships aside, it seems likely that most of the arachnid orders were established in a recognizable form by the Devonian period and, barring some debate about scorpions, that they were probably fully terrestrial at this time (Shear & Kukalová-Peck, 1990). Recent discoveries show unequivocally that harvestmen are at least 400 million years old and that by this stage they were fully terrestrial, air-breathing animals. Given that this oldest known example (Dunlop et al., 2003, 2004) is astonishingly modern looking, it seems reasonable to predict that harvestmen existed in the Silurian or maybe even earlier. The oldest known harvestman appears to show most autapomorphies of living Opiliones (discussed later). Unfortunately this means that there is no fossil stem lineage showing how and when the ancestors of modern harvestmen acquired the characteristic features of the group. We can only speculate about what pre-Devonian harvestmen or their forebears might have looked like, and whether the common ancestor of the group was an aquatic or terrestrial animal.

Paleozoic harvestmen Rhynie. The Rhynie chert, Scotland, is one of the most important localities for understanding the early evolution of terrestrial plants and arthropods. The fossils’ significance is their great age, around 400 million years (Early Devonian: Pragian),

Paleontology

coupled with their extraordinary, three-dimensional preservation in a hard, translucent matrix. All ectodermal structures have been preserved, including some internal features. The Rhynie chert has been interpreted as a Devonian hot-spring environment with pools or lakes surrounded by low vegetation and a community of terrestrial arthropods. Harvestmen are rare here compared with more abundant specimens of mites and the extinct, spiderlike trigonotarbid arachnids. The Rhynie chert represents deposition on the marshy margins of a hot spring that was periodically inundated by overbank flooding. From this water a sinter deposit precipitated out, silicifying the cuticles of the organisms and resulting in their exquisite and detailed preservation. Rice et al. (2002) provided a summary of the geological setting at Rhynie and listed additional background literature. The Rhynie fossils of the harvestman Eophalangium sheari comprise two principal specimens (Dunlop et al., 2003): a series of lateral sections beginning near the midline (Figures 5.1a–b) and a ventral view in which the actual sternites of the opisthosoma are mostly missing to show the inside of the body (Figure 5.1c). The lateral sections show the mouthparts, a median eye tubercle, and a divided carapace joining broadly onto a squat, compact opisthosoma. The most significant feature is an elongate, annulate ovipositor that sits in a cuticular sheath, bears fine setae, and identifies the specimen as female. Unfortunately the distal tip of the structure is not preserved. Because this relatively large (ca. 10 mm long) Rhynie fossil has median eyes, it is clearly not a Cyphophthalmi; thus its annulated ovipositor strongly implies that it can be referred to Eupnoi. Turning this specimen over to examine it in a more lateral plane reveals an extensive tracheal system. This is the oldest record of actual tracheal tubes for any arthropod (some slightly older millipede fossils preserve spiracles) and proves that the Rhynie harvestmen were living on land as early as the Devonian period. Again, the similarities with living phalangioid harvestmen (see Höfer et al., 2000) are remarkable, and the same basic morphology is preserved in this 400-million-year-old fossil. The largest branch, or stem trachea, enters the prosoma, while a series of diverging secondary tracheae serves the opisthosoma and can even be traced around the gut. The second specimen (Figure 5.1c) is smaller and male. It preserves both trachea and a penis with a slightly swollen, setose tip resting near the gonopore. Under high magnification there is a suggestion of two pairs of penis muscles. Extant Eupnoi have only one muscle, meaning either that the male is not conspecific with the female or (if conspecific) that there were grades of Paleozoic harvestmen expressing different character combinations from living clades. The second specimen also preserves the long, slender legs typical of many common extant harvestmen and further reinforces the idea that these fossils differ little in gross morphology from certain living species. Of the characteristic autapomorphies of Opiliones (e.g., penis and one pair of trachea), only ozopores have yet to be found. The presence of a penis and an ovipositor in these fossils strongly suggests that the typical copulation behavior and subsequent egg laying in the substrate seen in modern harvestmen (see Chapter 12) had evolved as early as the Devonian.

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Figure 5.1. The oldest known harvestman, Eophalangium sheari from the Rhynie chert, Scotland (photos: H. Hass). (a) Female in lateral section showing ovipositor. (b) Reverse side of same specimen showing gut and trachea. (c) Male opisthosoma in ventral section showing styliform penis and opisthosoma surrounded by long, slender legs. Scale bars = 1 mm.

East Kirkton. A single specimen of another long-legged and remarkably modernlooking harvestman (Figure 5.2a) was briefly described by Wood et al. (1985) from the East Kirkton locality near Edinburgh, Scotland. This material is nearly 340 million years old (Lower Carboniferous: Viséan). The site has been interpreted as a lake and lakeside environment at which volcanic activity and hot springs created an unusual water chemistry enabling the preservation of the plants and animals (Rolfe et

Paleontology

253

Figure 5.2. Carboniferous harvestmen. (a) Brigantibunum listoni from East Kirkton, Scotland (photo: L. Anderson). (b) Eotrogulus fayoli from Commentry, France (reproduced from Thevenin 1901). (c–d) Part and counterpart of Nemastomoides longipes from Mazon Creek, USA (photos: C. Neumann). (e) Kustarachne tenuipes from Mazon Creek, USA (photo: F. Marsh). (f) Echinopustulus samuelnelsoni from western Missouri, USA. Scale bars = 5 mm.

al., 1994). Abundant scorpions and eurypterids are known from this locality, but other arachnids (apart from the harvestman) are curiously absent. The fossil is compressed more or less on its side onto a slab of limestone. It does not preserve anything like the same amount of detail as the Rhynie fossils, although under low-angle lighting there are hints of what may be an extended annulate ovipositor lying across the body. Selden (1993b) commented on the difficulty in assigning this specimen to

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any particular group within Opiliones. Nevertheless, it is remarkably modern looking and on first glance could easily pass for a fossil of a living genus like Phalangium or Leiobunum. Given that older Eupnoi-like examples are known from Rhynie, the East Kirkton fossil was tentatively referred to this clade by Dunlop and Anderson (2005), who named it Brigantibunum listoni.

Coal Measures. The Upper Carboniferous Coal Measures of Europe and North America preserve a rich fauna of terrestrial arthropods. Most of the larger-bodied extant arachnid orders (Araneae, Amblypygi, Uropygi, Opiliones, Scorpiones, Solifugae, Ricinulei) have been recorded from the Coal Measures, and even tiny soil fauna elements such as mites have been recovered by macerating sediments of this age. The Coal Measures are widely interpreted as having been warm, swampy, forest environments from a time about 300 million years ago when Europe and North America formed part of a single continent. Widespread economic exploitation of coal sites, combined with a passion for fossil collecting in the late nineteenth and early twentieth centuries, has ensured that many specimens of plants, arthropods, and even vertebrates exist in museum collections. These Coal Measures fossils are not preserved in the coal itself, but rather in shales or concretions in the intervening rock layers between coal seams. There is an important difference between these two types of preservation. Shale fossils (e.g., at Commentry) have been flattened onto the rock matrix, while concretion fossils (e.g., at Mazon Creek) are preserved within a hard, ironstone nodule and often retain more of their three-dimensional structure. Early workers on Carboniferous arachnids, of whom Fritsch (1904) is a good example, often assigned some unusual fossils to Opiliones—fossils that are now recognized as belonging to the extinct arachnid orders Trigonotarbida and Phalangiotarbida. Some of these fossils were given names that made them sound like harvestmen, such as the trigonotarbids Anthracosiro and Stenotrogulus (and its synonym Cyclotrogulus) or the phalangiotarbid Opiliotarbus. Nevertheless, none of these forms actually belongs to Opiliones. Interestingly, fossil trigonotarbids in the family Eophrynidae were heavily armed with spines and tubercles and look remarkably similar to some living harvestmen of the suborder Laniatores (Loman, 1900). This resemblance must, however, be interpreted as the convergent evolution of defensive adaptations. There is convincing evidence, such as fossilized book lungs, for grouping trigonotarbids with spiders, whip spiders, and whip scorpions (Dunlop, 1996a). Plesiosiro madeleyi from the Coal Measures of the English Midlands is another fossil with a name derived from a harvestman, in this case the Cyphophthalmi Siro. However, in its original description this species was assigned to an extinct, monotypic order named Haptopoda. Plesiosiro madeleyi does somewhat resemble both Cyphophthalmi and Trogulidae, and Shear and Kukalová-Peck (1990) commented that it may belong in Opiliones. The revision of Dunlop (1999) could not identify any unequivocal harvestman autapomorphies in P. madeleyi and maintained Haptopoda as a distinct order. Dinopilio gigas was described as a harvestman from the Coal Measures of the Czech Republic. It looks more like a spider than a harvestman (Pocock, 1911) and was transferred by Petrunkevitch (1953) to an extinct spider family, Pyri-

Paleontology

taraneidae. The validity of this family and the status of D. gigas are being revised (P. Selden, pers. comm.). Although not strictly from the Coal Measures, Rhabdotarachnoides simoni is a fossil 30 mm long from the Lower Permian of the Rotliegend in Germany. H. Haupt (1957) tentatively referred it to Opiliones, comparing it with Nemastomatidae. This specimen cannot even be confidently identified as an arthropod and appears to be simply a fortuitously shaped plant fragment (Rößler et al., 2003; Table 5.2).

Genuine Carboniferous harvestmen. Two unequivocal Carboniferous fossil harvestmen were described by Thevenin (1901) from the Coal Measures of Commentry in northern France: Eotrogulus fayoli (Figure 5.2b) and Nemastomoides elaveris. As their generic names suggest, both Commentry fossils were considered to be similar to the living genera Trogulus and Nemastoma, respectively. It should be added that Eotrogulus was at one stage erroneously thought to be a trigonotarbid (Fritsch, 1904; Petrunkevitch, 1913). Petrunkevitch (1913) described two new fossil harvestmen from Mazon Creek, Illinois, USA, one of the most famous Coal Measures localities. Alexander Petrunkevitch published a number of monographs on fossil arachnids, but his interpretations must be treated with caution (Selden, 1993b) since his descriptions and illustrations were often poor. His two Mazon Creek harvestmen were originally placed in Protopilio, but later he synonymized the genus Protopilio with the older Nemastomoides (Petrunkevitch, 1953). Nemastomoides longipes is a genuine, long-legged harvestman (Figures 5.2c,d) with an oval body expressing segmentation, mostly toward the posterior end of the opisthosoma. What is interesting about this specimen is that it seems to show a rather Cyphophthalmi-like condition (see comments in Petrunkevitch, 1949) in which the genital operculum does not extend fully over the genital opening, as in the Phalangida. Perhaps there was a grade of Paleozoic non-Cyphophthalmi harvestmen in which the modern condition of the genital operculum had not yet fully evolved. The other Mazon Creek species, N. depressus, is actually a poorly preserved example of the extinct arachnid order Phalangiotarbida (Beall, 1997; Table 5.2). Petrunkevitch (1955) erected two new families to accommodate the Carboniferous harvestmen. However, the diagnoses of both families included characters that should not be part of the ground plan of Opiliones (cf. Shultz, 2000). The extinct Eotrogulidae were supposed to have free coxae, whereas the coxae are fused and immovable in all other harvestmen. Nemastomoididae were supposed to have a clearly defined oval sternum between the leg coxae, whereas the harvestman sternum is widely accepted as being highly reduced. The validity of both these fossil families is thus questionable. From published illustrations, E. fayoli looks like a genuine trogulid (Figure 5.2b), whereas in my opinion the two valid Nemastomoides species resemble Eupnoi more than Dyspnoi. A new Carboniferous harvestman from a Coal Measures nodule from western Missouri, with poorly expressed segmentation, a dorsal ornament of fine tubercles, and four prominent spines on its back, was described as Echinopustulus samuelnelsoni (Dunlop, 2004a; Figure 5.2f). Except for the spines, it looks somewhat like a trogulid

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and has been tentatively assigned to the Dyspnoi. Dunlop (1996b) figured an undescribed Carboniferous harvestman of uncertain affinities from the Stephanian of Montceau-les-Mines in France. This fossil is known only from the coxosternal region plus a single, relatively long leg. A number of curious fossils from the Coal Measures of England described as Nephila-like araneomorph spiders in the genus Archaeometa may also be harvestmen (P. Selden, pers. comm.). In these strange, long-bodied specimens leg II appears to be longest, a characteristic feature of most harvestmen. The status of these fossils is currently being revised. Unequivocal harvestmen have not been recorded from the Permian.

Kustarachnida. Kustarachne tenuipes from the Coal Measures of Mazon Creek was originally described as a phalangiotarbid. Two further species were added by Melander (1903) and one by Petrunkevitch (1913), although one of Melander’s species was subsequently recognized as a fossil Ricinulei. Petrunkevitch (1913, 1949, 1955) interpreted Kustarachne (Figure 5.2e) as the sole genus of a new, extinct, arachnid order that he named Kustarachnida. This order was characterized by a unique combination of characters, including a carapace with a single pair of eyes, a camarostome (i.e., fused pedipalpal coxae), chelate pedipalps, a pedicel, a small pygidium at the end of the opisthosoma, and long, slender legs. On the basis of this supposed camarostome, Petrunkevitch regarded kustarachnids as closely related to Uropygi (see review in Dunlop, 1996a, 2004b). Beall (1986, 1997) suggested that many of Petrunkevitch’s diagnostic characters for Kustarachnida were simply misinterpretations of the fossils and that the combination of a compact body, a single pair of eyes, and long, slender legs implied that these fossils were misidentified harvestmen. Other authors (Selden, 1993a,b; Dunlop 1996a,b) accepted Beall’s proposal. Restudy of the type of K. tenuipes has confirmed these interpretations (Dunlop, 2004b). The reported chelate pedipalps, pedicel, and pygidium are not present in the fossil, and Kustarachnida should be treated as a synonym of Opiliones. Petrunkevitch also seriously misinterpreted the carapace of K. tenuipes, failing to recognize that it is divided into a propeltidium + mesopeltidium and a metapeltidium. In fact, K. tenuipes superficially looks like a modern Eupnoi, at least in dorsal view (Figure 5.2e), where the anterior opisthosomal tergites are indistinct, but become better defined posteriorly. The other two Kustarachne species, K. extincta and K. conica, are poorly diagnosed, appear not to be particularly well preserved, and may simply be synonyms of K. tenuipes (thus they were not included in Table 5.1).

Mesozoic harvestmen The arachnid fossil record is very sparse throughout the whole Mesozoic period (Selden, 1993b). In spite of some recent discoveries of new terrestrial arthropodbearing localities, we still know more about the Paleozoic arachnids than the Mesozoic ones. From what little data are available, the Mesozoic arachnids generally appear to represent a fairly modern-looking fauna. The extinct orders (Haptopoda, Phalangio-

Paleontology

tarbida, and Trigonotarbida) are no longer found, and many Mesozoic arachnids can be assigned to, or at least closely resemble, living families. Unfortunately there are hardly any unequivocal Mesozoic harvestmen with which to test this hypothesis of a fundamental faunal shift between the Paleozoic and the Mesozoic. There are no reports of harvestmen from the Triassic. Hasseltides primigenius from the famous Jurassic Solnhofen limestone in Germany was originally thought to be a fossil spider (Weyenbergh, 1869). It was subsequently reinterpreted as a harvestman (van Hasselt in Weyenbergh, 1874), but was eventually shown to be a crinoid (van Regteren Altena in Petrunkevitch, 1955). A more common, long-legged Solnhofen fossil, Phalangites priscus, described by Münster (1836), has, at one time or another, been interpreted as either a pycnogonid (sea spider), a spider, or a harvestman. Detailed study has confirmed earlier suspicions that these fossils (and similar genera) are the molted exoskeletons of larval phyllosome crustaceans (Polz, 1975). Of the remaining Mesozoic harvestmen, Roger (1946) figured material from the Upper Cretaceous of Sahel-Alma, Lebanon, which Cokendolpher and Cokendolpher (1982) suggested might be a “Palpatores.” A close reading of Roger’s article reveals that this fossil actually comes from limestone and not, for example, from Cretaceous Lebanese amber. Sahel-Alma is a fully marine environment that makes these fossils’ assignment to Opiliones extremely unlikely. Roger suggested that they might have become washed in, but his alternative suggestions of affinities with crustaceans or pycnogonids seem intuitively rather more likely (Table 5.2). Schlüter (1978) identified a putative harvestman from fossil amberlike resins from the Upper Cretaceous (Cenomanian) of the Paris and Aquitaine basins in northwestern France. The original drawing is poor and seems to show a smooth dorsal body surface and a distinctly demarcated anterior region resembling the capitulum of a tick, even down to the tiny, paddle-shaped pedipalps. Its assignment to Opiliones is not accepted here (Table 5.2). Surprisingly, there has so far been no report of harvestmen from the Lower Cretaceous Crato Formation of Brazil, an important locality that has otherwise yielded a rich Mesozoic arachnid fauna including spiders, scorpions, solifuges, whip scorpions, whip spiders, and mites. An unnamed (and more genuine-looking) long-legged harvestman was described by Jell and Duncan (1986) from the Lower Cretaceous of Koonwarra, Victoria, Australia. Although it resembles a typical Eupnoi, Selden (1993b) commented on the difficulty in assigning it to a taxon. Reexamination of this Cretaceous harvestman would be welcome. Recently a Dyspnoi harvestman, Halitherses grimaldii (Figure 5.3b), has been found in Myanmar (Burmese) amber (Giribet & Dunlop, 2005). This first Mesozoic amber harvestman is a long-legged species with a pustulate body, large eyes, and highly setose chelicerae. It may be related to ortholasmatine nemastomatids. Myanmar amber also yields spiders, mites, scorpions, and pseudoscorpions (Grimaldi et al., 2002), many of which are as yet undescribed.

Cenozoic harvestmen Baltic amber. Amber is one of the most famous and most beautiful forms of preservation (Figures 5.3a–e). Amber is fossilized tree resin, and fossils contained in

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Figure 5.3. Mesozoic and Tertiary harvestmen. (a) Siro platypedibus from Bitterfeld amber, Germany (photo: G. Giribet). (b) Halitherses grimaldii from Myanmar (Burmese) amber (photo: G. Giribet). (c) Caddo dentipalpis from Bitterfeld amber. (d) Histricostoma (?) tuberculatum, from Baltic amber. (e) Hummelinckiolus silhavyi, a Laniatores from Dominican amber. (f) Petrunkevitchiana oculata from Florissant, Colorado, USA (drawing reproduced from Petrunkevitch 1922). All specimens ca. 1–3 mm in body length.

Paleontology

it are usually referred to as inclusions. Good general accounts of amber preservation and the diversity of the fauna can be found in Schlee (1990), Poinar (1992), and A. Ross (1998). Amber harvestmen have not been studied with quite the same intensity as spiders (Wunderlich, 2004), but nonetheless the most diverse assemblage (10 species) of fossil harvestmen are those described from Baltic amber (Table 5.1). These ambers (also called “Prussian amber” by Scudder, 1891) have been recovered widely across the Baltic region and are of considerable commercial value. A consequence of this is the risk of fakes, either through copals (subfossil resins only a few thousand years old) being sold as amber or through inclusions being placed into genuine ambers to increase their value. So far this does not seem to have affected the harvestman record, and there are established methods to test whether amber is genuine or not (A. Ross, 1998). Amber is notoriously difficult to date accurately, but the Baltic amber is generally regarded as being Eocene in age, about 38–54 million years. Valuable overviews of the general Baltic amber fauna can be found in Larsson (1978) and Weitschat and Wichard (2002). The first record of a “Phalangium” in Baltic amber was by Schlotheim (1820), and the first named species appears to be Phalangium succineum by Presl (1822). This name was listed by Scudder (1891), but not by subsequent authors, and the original Latin description may not even refer to a harvestman (Dunlop, 2006). Illustrations are lacking, and the status of this name is unclear. Berendt (in Gravenhorst, 1835) mentioned six “Opilio” specimens in Baltic amber, and the three main systematic authors are Koch and Berendt (1854), Menge (1854), and Roewer (1939). Note that Berendt (1845) also listed their forthcoming names (as nomina nuda) in a preliminary report on his monograph. It is also worth mentioning that Berendt (1830) assigned some Baltic amber inclusions to Phalangium cancroides (a pseudoscorpion, now belonging to the genus Chelifer) and to the common extant harvestman Phalangium opilio (see also Scudder, 1891). This sole report of a living harvestman species in amber has not been confirmed by later work and is not included here in Table 5.1. Larsson (1978) noted that isolated (and unidentifiable) harvestman legs, probably Eupnoi, are sometimes found in Baltic amber. He suggested that these were deliberately autotomized by animals trying to escape the sticky resin. Larsson further noted that the best-preserved examples tended to be the nemastomatids, but that many were known from juveniles, which might imply seasonality in resin production, with predominantly young individuals being caught after their hatching period. The Baltic amber also includes a beautiful example of Caddo figured by Kupryjanowicz (2001) together with juvenile examples of other species. Additionally, there are some undescribed examples of the suborder Laniatores (Poinar & Cokendolpher, unpub. data), which is quite rare in the fossil record (Table 5.1).

Baltic amber systematics. The described Baltic amber harvestmen were listed by Scudder (1891), Starega (1976a, 2002), Keilbach (1982), and Dunlop (2006). On the basis of Starega and Ubick and Dunlop (2005), the Baltic harvestmen can currently be referred to Phalangiidae (two species), Sclerosomatidae (two species), Caddidae (one species), Nemastomatidae (three species), Sabaconidae (one species),

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and Cladonychiidae (one species). Keilbach erroneously referred the laniatorean Proholoscotolemon nemastomoides to the Eupnoi family Phalangiidae. He also included Phalangopus subtilis as a harvestman, but this genus and species is listed by Petrunkevitch (1955) as Araneae incertae sedis and by Scudder (1891) and Bonnet (1958) under Syctodidae (Table 5.2). Some taxa have been transferred since their original description. For example, Bishop and Crosby (1924) correctly referred the large-eyed Platybunus dentipalpis (Koch & Berendt, 1854) to the extant genus Caddo (Figure 5.3c). There are, however, a number of discrepancies in the generic placements between Petrunkevitch (1955) and Keilbach (1982). The latter appears not to have accepted Petrunkevitch’s amendments, even though, for example, the transfer of Opilio ramiger to Dicranopalpus is wholly justified on the basis of the predominant pedipalpal apophysis. Furthermore, two of Menge’s species are listed, without comment, as nomina nuda by Keilbach. It is also worth noting that the fossil Leiobunum longipes is the senior homonym of an extant species (see details in Cokendolpher, 1984a). Menge (1854) only formally described one fossil Leiobunum species, yet in the introduction to this work he lists a species (without description) as Leiobunum saparum. This is presumably a lapsus, with two names (longipes and saparum) being accidentally proposed for a single specimen. Starega’s (1976a) transfer of Nemastoma tuberculatum (Figure 5.3d) to Histricostoma appears valid on the basis of the presence of characteristic spines on the opisthosoma. Starega (1976a) also referred Gonyleptes nemastomoides to the extant southern European Laniatores genus Scotolemon—recently transferred to a new cladonychiid genus, Proholoscotolemon, by Ubick and Dunlop (2005)—and Starega (2002) revised the entire Baltic amber fauna on the basis of new Polish material, proposing a number of new synonyms and generic placements, all of which have been incorporated here into Table 5.1. In this revision all the species of Roewer (who conspicuously failed to cite the earlier studies) were regarded as junior synonyms of either Koch and Berendt’s or Menge’s taxa, and further synonyms among both these latter authors’ species were also recognized. The main conclusion to be drawn from Baltic amber is that, apart from the possible phalangiid Cheiromachus coriaceus—a nomen dubium according to Dunlop (2006)—all but one of the unequivocal Baltic amber harvestmen can currently be placed in extant genera (Table 5.1).

Dominican amber. The second major amber deposit is Dominican amber that is collected from two regions of the Dominican Republic on Hispaniola, usually referred to as the “northern” and “eastern” areas. Compared with some 180 years of research on Baltic amber, the significance of the inclusions in Dominican amber has only been recognized relatively recently, and the first record of harvestmen was by Schlee and Glöckner (1978). The dating of Dominican amber is also imprecise, but in their account of the geological setting Iturralde-Vinent and MacPhee (1996) proposed that all the inclusion-bearing amber was derived from a single sedimentary basin, which could be constrained to an early to mid-Miocene age of around 15–20 million years. This would be younger than Baltic amber, and this date has been ac-

Paleontology

cepted by, for example, Penney (1999) for the amber spiders. However, Cokendolpher and Poinar (1992, 1998), cited an older, Upper Eocene age (ca. 30–45 million years) for the Dominican amber harvestmen they described from the El Mamey Formation, deriving this date from Cepek (in Schlee, 1990). This would make their harvestmen equivalent in age to the Baltic amber fauna. It is beyond the scope of this work to assess the relative merits of these dating schemes. Dominican amber may be anywhere between 15 million and 45 million years old (G. Poinar, pers. comm.), and for convenience taxa are listed in Table 5.1 according to the age under which they were originally described. Only four Dominican amber harvestmen have been formally named. Significantly, all of them are “phalangodid” Laniatores (Cokendolpher, 1987a; Cokendolpher & Poinar, 1992, 1998) and have been referred to Samoidae (Table 5.1). Additionally, a Kimula species is now Kimulidae (see Chapter 4). All the Dominican amber fossils (Figure 5.3e) can be placed in extant genera that are still distributed in the Caribbean region today. Cokendolpher and Poinar (1992, 1998) commented on the fact that although four fossil “phalangodids” have been recorded from Hispaniola, only a single living species is known. In a similar vein, Penney (1999) has argued for spiders that the Dominican amber record can predict the occurrence of extant taxa in the otherwise poorly known Recent Hispaniolan fauna. This probably applies to harvestmen too. Cokendolpher (1987a) also mentioned the presence of additional (undescribed) Dominican amber Laniatores in the Staatliches Museum für Naturkunde in Stuttgart, Germany.

Bitterfeld and other ambers. A less well-known amber is the Bitterfeld (or Saxon) amber found in eastern Germany. Earlier accounts date this as Miocene (ca. 22 million years), although the insect and spider faunas show strong similarities to Baltic amber and lead some authors (e.g., Röschmann, 1997; Wunderlich, 2004) to the conclusion that this is an older (perhaps 40 million years) amber, reworked into younger sediments. Dunlop and Giribet (2003) discuss this further, and the Bitterfeld and Baltic ambers are sometimes treated together as “Samlandic amber.” Material from Bitterfeld includes a single, undescribed Bitterfeld phalangiid identified and figured by Moritz (in Barthel & Hetzer, 1982), which was further listed in Schumann and Wendt (1989), plus other undescribed material. Significantly, this Bitterfeld material includes the first fossil record of Cyphophthalmi, Siro platypedibus, a complete and modern-looking example (Figure 5.3a) with rather laterally compressed legs, perhaps indicative of fossorial behavior. Work in progress on other Bitterfeld inclusions in Berlin suggests the presence of some new species, plus other taxa such as Caddo dentipalpis (Figure 5.3c) and Histricostoma tuberculatum, previously recorded from Baltic amber. As with the insects and spiders, this tends to support an older date for the Bitterfeld inclusions (Figure 5.4). Other late Mesozoic and Tertiary ambers are known to bear inclusions (e.g., Mexican, Lebanese, Romanian, New Jersey, Spanish, Russian). So far they have not yielded any described harvestmen (Keilbach, 1982; Schlee, 1990), but it is possible that undiscovered material exists either in museum or private collections.

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Figure 5.4. The distribution over time of the four major harvestman clades, showing the approximate ages of the main fossil localities detailed in the text. Cladogram after Giribet et al. (2002). Note the long ghost ranges for Cyphophthalmi and Laniatores, predicting that older fossils of these groups have yet to be discovered.

Florissant. One of the most important nonamber sites for Cenozoic arachnids is the Florissant Formation in Colorado, USA. This significant locality has yielded plants, mammals, insects, and also a rich fauna of spiders (e.g., Petrunkevitch, 1922), plus a small number of harvestmen. This mid-Oligocene site is interpreted as a lake deposit surrounded by forests from about 35 million years ago (see Gregory, 1994, for details of the flora, geological setting, and further background literature). Intermittent volcanic activity is thought to have created dust clouds that buried the plants and animals and preserved them in the lake sediments. Thus Florissant is a more “typical” example of fossilization, with the specimens compressed in shales. Florissant preservation is not as good as in amber, although it does include remarkable details of spines and setae. The first harvestman described from Florissant was Leptobunus atavus, a fossil placed in an extant genus by Cockerell (1907). Petrunkevitch (1922) overlooked Cockerell’s article, but added two more species, again in an extant genus: Phalangium oculatum (Figure 5.3f) and P. lacoei. Subsequently, Mello-Leitão (1936) created two new (extinct) genera for Petrunkevitch’s species, namely, Petrunkevitchiana and Amauropilio, respectively. He also accidentally introduced the combination Amauropilio lawei (for lacoei), a lapsus according to Cokendolpher and Cokendolpher (1982). All three species were recognized as valid (Table 5.1), although Cokendolpher and Cokendolpher (1982) noted that most of the diagnostic characters of Petrunkevitchiana were based on erroneous features in the original description (see also Starega, 1976a). Petrunkevitchiana oculata was regarded as an incertae sedis member of the Phalangioidea of uncertain familial affinities, while the remaining two species were both referred to Amauropilio. This fossil genus was placed in the subfamily Leiobun-

Paleontology

inae and compared in particular with species of the extant genus Homolophus, with which it shares the characters of relatively short legs and smooth pedipalpal claws. Note that Homolophus has since been referred to Togwoteeus (see Holmberg & Cokendolpher, 1997). Additional undescribed harvestmen from Florissant are present in the Museum of Comparative Zoology at Harvard University (R. Cutts, pers. comm.).

Other Cenozoic records. Other Tertiary shale deposits that preserve spiders are known, such as the “Braunkohle” of Rott in Germany and the Green River locality in the USA. Harvestmen have yet to be reported from these localities, but might be predicted because intensively studied sites such as Florissant have yielded both spider and harvestman material. Harvestmen have been reported from some Tertiary nonamber sites. Trogulus longipes was described by H. Haupt (1956) from the Eocene “Braunkohl” of Geiseltal in eastern Germany. This locality has been interpreted as a subtropical environment 50 million years old preserving both swamp and forest habitats, and the harvestman was found among a rich insect fauna. Haupt’s figures of two of the three specimens show disarticulated arthropods whose overall size and ovoid shape is consistent with them being trogulids. No unequivocally diagnostic features of Trogulidae are apparent, although the (rather poor) figures imply an opisthosoma with about four large, medially divided tergites, a morphology vaguely similar to living Trogulus species. Therefore, T. longipes is tentatively retained here within Opiliones (Table 5.1). Gourret (1886) described two harvestmen from the Oligocene of Aix-enProvence in France, which Petrunkevitch (1955) regarded as inadequately described spiders. On the basis of Gourret’s plates, the “phalangiid” Phalangillum hirsutum does look more like a spider, while the “trogulid” Amphitrogulus sternalis is more enigmatic, less obviously a spider, and reexamination of the material would be welcome. Oligoopilionus aquaticus was described by Ciobanu (1977) as a phalangiid from the Oligocene of Piatra Neam’t in eastern Romania. However, Crawford (1992) doubted whether this poorly preserved fossil was even an arachnid and noted that, as its species name implies, it was discovered among an assemblage of offshore marine mollusks and fish—a surprising place to find a harvestman. Therefore, in the light of Crawford’s criticisms, O. aquaticus is not accepted here as a genuine harvestman (Table 5.2). Finally, Mastororill (1965) recorded a Phalangium spicies from Quaternary sediments near Rome in Italy. Many Quaternary deposits, which date up to about 1.6 million years ago, are known to yield these so-called subfossil arthropods. These are mostly insects with resistant cuticles (beetles being especially common), but mites and the hard parts of spiders have occasionally been recovered too. It would not be surprising to find additional harvestmen among such material.

CONCLUDING REMARKS Compared with other arachnids, the Early Devonian harvestman (400 million years) is one of the oldest known arachnids that represents a crown-group taxon,

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that is, is assignable to a living clade (Eupnoi). Mites possibly date back to the midOrdovician (ca. 470 million years) and unequivocally to the Early Devonian, stemgroup scorpions to the mid-Silurian (430 million years), and stem-group spiders to the mid-Devonian (380 million years). Pseudoscorpions are also known from the mid-Devonian. The extinct trigonotarbids are known from the late Silurian (414 million years) and the phalangiotarbids from the Early Devonian (400 million years). Except for the tiny and weakly sclerotized palpigrades and schizomids, the remaining arachnid orders are all first recorded as fossils from the Carboniferous, nearly 300 million years ago (Selden, 1993a,b). The fossil record of the harvestmen is too fragmentary to tell us much about their origins and evolution. There is nothing like the hypothetical “Eophalangia” proposed by Silhavy (1961), which acts as a common ancestor to the known harvestman groups or as a missing link resolving relationships within Opiliones or between Opiliones and other arachnid orders. The fossil record does, however, date the earliest occurrence of various taxa within Opiliones. Of the major harvestman suborders, Eupnoi goes back potentially to the Devonian, Dyspnoi to the Carboniferous, and Laniatores and Cyphophthalmi to somewhere between the Eocene and Miocene (Figure 5.4). In fact, if the basic harvestman phylogeny of (Cyphophthalmi (Eupnoi (Dyspnoi + Laniatores))) is correct (see Chapter 3), then we can predict that the Cyphophthalmi lineage must also be at least around 400 million years old and the Laniatores lineage at least around 300 million years old, the minimum possible ages for the divergence of these clades. Put another way, Cyphophthalmi and Laniatores express extraordinarily long “ghost ranges” of around 360–380 million and 260– 280 million years, respectively. The extreme rarity of the Cyphophthalmi from the fossil record remains a puzzle, but is probably due to their small size and cryptic, soil-living habits, which restrict their likelihood of fossilization. The comparative rarity of fossil Laniatores is rather curious, given that the living ones are diverse and can be quite large and heavily sclerotized. Perhaps their rarity in the fossil record is a consequence of their predominantly Gondwanan distribution. With the exception of the Brazilian Crato Formation, this biogeographic area covering the Southern Hemisphere has so far yielded comparatively few fossil sites with rich arachnid faunas. Most arachnid-rich Paleozoic localities are found in Europe and North America, and they all yield fossils of predominantly Eupnoi or troguloid harvestmen. Fossil Laniatores are only found with any sort of regularity in the Cenozoic, New World Dominican amber. A fossil Laniatores related to the extant southern European Holoscotolemon implies that the genus was once more widely distributed than today and would support the idea of a relatively warm paleoclimate for the Baltic amber-producing forest. Similarly, the Baltic Dicranopalpus and Histricostoma species appear to occur further north than any of the present-day examples—although Dicranopalpus is currently migrating northwards in Europe at quite a rapid pace—while it is interesting to note that Caddo occurs in Baltic amber, but is wholly absent from the recent European fauna (Starega, 2002). The most remarkable feature of the harvestman fossil record is the modernity of

Paleontology

almost all the specimens discovered thus far (Figures 5.1–3). Like the most familiar harvestmen in modern Northern Hemisphere ecosystems, the majority of the fossil harvestmen are of the “daddy-longlegs” type (Eupnoi) with a small, compact body and long, slender legs. Even the very oldest forms look like this (Wood et al., 1985). With the exception of the two Florissant genera (one of which is based on a poorly informative specimen) and two Baltic amber genera, all fully identified Cenozoic harvestmen can be referred to living genera. Paleontologists refer to this phenomenon in which there is little or no morphological change over long periods of time as stasis. Harvestmen seem to be a particularly good example of stasis, but the reasons why they have managed to survive apparently unaffected by a changing environment, mass extinctions, and the rise of other major plant and terrestrial animal groups (from winged insects to early tetrapods to mammals and birds) remain unclear. Most Paleozoic harvestmen at least superficially resemble modern, long-legged Eupnoi, and, on the basis of the annulate ovipositor, the Rhynie examples can probably be assigned to this clade. This implies that harvestmen are an ancient group that radiated before the Devonian and, at least in the Eupnoi line, have remained fundamentally unchanged ever since.

ACKNOWLEDGMENTS I thank Paul Selden (London) and Richard Cutts (Manchester), Lyall Anderson (Edinburgh), Neil Clarke (GLAHM), Hans Kerp and Hagen Hass (Münster), Jürgen Gruber and Norbert Vávra (Vienna), Agnes Rage, André Nel, and Mark Judson (MNHN), Christian Neumann (MB.A.), Tim White (YMP), Dan Levin and Finnegan Marsh (USNM), Andy Ross and Mark Pointer (BMNH), Wojciech Starega (Siedlce), George Poinar Jr. (Oregon), Barbara Kosmowska-Ceranowicz (MZ), Meinolf Hellmund (Halle), Sylvie Pichard (MHNM), Helmut Meyer (NSBS), Dave Grimaldi (AMNH), Gonzalo Giribet (Harvard), Peter Jäger (SMF), and Ronny Rößler (Chemnitz) for providing access to material in their care and/or information about specimens, repositories, and localities during the preparation of this chapter. James Cokendolpher, Dave Penney, Darrell Ubick, Bill Shear, the reviewers, and the editors all kindly provided valuable comments on an earlier version of the manuscript.

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CHAPTER

6

Cytogenetics Nobuo Tsurusaki

S

ince the first account of spermatogenesis in Nemastoma lugubre (Nemastomatidae) by the Russian cytologist Iwan Sokolow (1929), approximately only 30 studies have been published on harvestman chromosomes, including those presenting only fragmentary information. Despite this rather sluggish activity, these chromosomal studies have revealed the usefulness of chromosome information in harvestman systematics, as well as extremely fascinating features of their population cytogenetics, such as polyploidy, sex chromosome systems, B chromosomes, and chromosomal hybrid zones. This chapter presents a brief review of the cytogenetic aspects of Opiliones and their relevance to various fields of evolutionary studies.

GENERAL FEATURES Chromosome numbers To date, the chromosome number is known for only 43 species belonging to 11 families, which represent only a small percentage of the total number of harvestman species. This number reaches 80 species when unpublished data are included (Table 6.1). The diploid chromosome number in harvestmen ranges from 10 to 109, which is similar to that of spiders (range: 7–94 in males; > 300 species studied, Suzuki, 1954) and scorpions (range: 14–100; 34 species studied, Shanahan, 1989a,b; Yamazaki et al., 2001) and exceeds that of Pseudoscorpiones (range: 21–54; 20 species studied, Troiano, 1990; Stahlavsky & Kral, 2004) and Acari (range: 1 in haploid males to 35; > 110 species studied, Pijnacker & Ferwerda, 1975; Helle et al., 1984; Helle & Pijnacker, 1985). Amblypygi and Uropygi had just one species studied each, and for both the chromosome number was 25 in the males (Millot & Tuzet, 1934). Chromosome numbers exhibited by each of the four suborders of Opiliones are as follows. 266

Cytogenetics

267

Table 6.1 Number of chromosomes (2n) according to sex surveyed in harvestmen Taxa

Country

Sex

Number

References

CYPHOPHTALMI Sironidae Parasiro coiffaiti

France

MF

30

N. Tsurusaki & J. Martens, unpub. data

Siro rubens

France

M

30

Juberthie, 1956

Japan

F

30

Tsurusaki & Cokendolpher, 1990

Dalquestia formosa

USA

M

22

Tsurusaki & Cokendolpher, 1990

Lacinius ephippiatus

Germany

M

32

N. Tsurusaki & J. Martens, unpub. data

Mitopus ericaeus

England

M

32

Jennings, 1982

Mitopus morio

Russia

M

32

Sokolow, 1930

Mitopus morio

Germany

M

32

N. Tsurusaki & J. Martens, unpub. data

Mitopus morio

England

M

32

Jennings, 1982

EUPNOI Caddidae Caddo agilis Phalangiidae, Oligolophinae

Mitopus morio

Japan

MF

32

Tsurusaki & Cokendolpher, 1990

Odiellus aspersus

Japan

MF

20

Suzuki, 1941; Tsurusaki & Cokendolpher, 1990

Oligolophus hanseni

France

MF

30

N. Tsurusaki & J. Martens, unpub. data

Oligolophus tridens

Russia

M

32

Sokolow, 1930

Oligolophus tridens

Germany

MF

16

N. Tsurusaki & J. Martens, unpub. data

Japan

M

24

Tsurusaki & Cokendolpher, 1990

Opilio canestrinii

Germany

MF

24

N. Tsurusaki & J. Martens, unpub. data

Opilio parietinus

Russia

M

24

Sokolow, 1930

Phalangiidae, Opilioninae Homolophus arcticus

Opilio parietinus

Austria

M

24

N. Tsurusaki & J. Martens, unpub. data

Opilio ruzickai

Austria

MF

24

N. Tsurusaki & J. Martens, unpub. data

Russia

M

32

Sokolow, 1930

Phalangium opilio

Germany

MF

24–26

Phalangium opilio

France

M

24

Phalangiidae, Phalangiinae Phalangium opilio

N. Tsurusaki & J. Martens, unpub. data Juberthie, 1956

Phalangium opilio

France

M

24

N. Tsurusaki & J. Martens, unpub. data

Phalangium opilio

USA

M

32

Tsurusaki & Cokendolpher, 1990 (Continued)

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Cytogenetics

Table 6.1 Continued Taxa

Country

Sex

Number

MF

16

References

Phalangiidae, Platybuninae Lophopilio palpinalis

Germany

N. Tsurusaki & J. Martens, unpub. data

Megabunus diadema

France

M

28

N. Tsurusaki & J. Martens, unpub. data

Rilaena triangularis

Russia

M

36

Sokolow, 1930

USA

M

18/20

Tsurusaki & Cokendolpher, 1990

Japan

MF

14–22

Tomohiro, 1940; Tsurusaki et al., 1991; Gorlov & Tsurusaki, 2000a

Protolophidae Protolophus tuberculatus Sclerosomatidae, Gagrellinae Gagrellopsis nodulifera Gagrellula ferruginea

Japan

M

22

Gagrellula ferruginea

Japan

MF

10–22

Suzuki, 1941 N. Tsurusaki, unpub. data

Melanopa grandis

Japan

MF

20

Tsurusaki & Cokendolpher, 1990

Melanopa unicolor

India

M

18

Sharma & Dutta, 1959

Paraumbogrella pumilio

Japan

MF

10

Tsurusaki, 1982a; Tsurusaki & Cokendolpher, 1990

Psathyropus tenuipes

Japan

MF

18 + 0–18 Bs

Tsurusaki, 1993; Gorlov & Tsurusaki, 2000a,b

Systenocentrus japonicus

Japan

M

10

Suzuki, 1966b

Eumesosoma roeweri

USA

MF

22

Tsurusaki & Cokendolpher, 1990

Leiobunum blackwalli

Germany, Austria

M

20

N. Tsurusaki & J. Martens, unpub. data

Leiobunum crassipalpe

USA

M

22

Parthasarathy & Goodnight, 1958

Sclerosomatidae, Leiobuninae

Leiobunum curvipalpi

Japan

MF

24

Leiobunum globosum

Japan

MF

46–52

Suzuki, 1957; Tsurusaki, 1990 N. Tsurusaki, unpub. data

Leiobunum hiasai

Japan

M

24

Tsurusaki, 1985b

Leiobunum hikocola

Japan

M

18

Tsurusaki, 1985b

Leiobunum japanense

Japan

M

16

Suzuki, 1976b

Leiobunum japonicum

Japan

MF

20

Suzuki, 1941; Tsurusaki & Holmberg, 1986

Leiobunum kohyai

Japan

M

20

Suzuki, 1976a; Tsurusaki, 1985b

Leiobunum limbatum

Austria

MF

22

N. Tsurusaki & J. Martens, unpub. data

Leiobunum manubriatum

Japan

MF

24/46–49

Leiobunum montanum

Japan

MF

18–26

N. Tsurusaki, unpub. data Suzuki, 1976a; Tsurusaki, 1985a

Leiobunum nigripes

USA

M

22

Parthasarathy & Goodnight, 1958

Leiobunum rotundum

Germany, Austria

MF

20

N. Tsurusaki & J. Martens, unpub. data

Leiobunum rupestre

Russia

M

22

Sokolow, 1930

Leiobunum sadoense

Japan

M

18

Tsurusaki, 1985b

Leiobunum tohokuense

Japan

MF

20/22/24

Tsurusaki, 1990

Cytogenetics

Taxa

Country

Sex

Number

Leiobunum ventricosum1

USA

M

22

Nelima genufusca

Japan

MF

18–22

Nelima nigricoxa

Japan

MF

16–22

Nelima paessleri

Canada

M

22

Nelima satoi

Japan

MF

16

Nelima satoi

Japan

MF

14–20

269

References Parthasarathy & Goodnight, 1958 N. Tsurusaki, unpub. data N. Tsurusaki, unpub. data Tsurusaki & Holmberg, 1986 Tsurusaki & Cokendolpher, 1990 N. Tsurusaki, unpub. data

Nelima silvatica

Germany

F

18

N. Tsurusaki & J. Martens, unpub. data

Nelima similis

Japan

M

20

Tsurusaki & Cokendolpher, 1990

Togwoteeus biceps

USA

MF

22

Holmberg & Cokendolpher, 1997

Sclerosomatidae, Sclerosomatinae Astrobunus laevipes

Austria

MF

22

N. Tsurusaki & J. Martens, unpub. data

Homalenotus quadridentatus

France

M

22

N. Tsurusaki & J. Martens, unpub. data

Prosclerosoma hispanicum

France

M

20

N. Tsurusaki & J. Martens, unpub. data

Ischyropsalis luteipes

France

M

16

Juberthie, 1956

Ischyropsalis pyrenaea

France

M

16

Juberthie, 1956

Dicranolasma soerenseni

France

MF

28

N. Tsurusaki & J. Martens, unpub. data

Mitostoma chrysomelas

Austria

M

24

N. Tsurusaki & J. Martens, unpub. data

Nemastoma dentigerum

Germany

MF

16

N. Tsurusaki & J. Martens, unpub. data

Nemastoma lugubre

Russia

M

16

Sokolow, 1929

Japan

M

14

N. Tsurusaki, unpub. data

DYSPNOI Ischyropsalididae

Nemastomatidae

Nipponopsalididae Nipponopsalis abei Sabaconidae Sabacon makinoi

Japan

MF

10–14

Tsurusaki, 1989

Sabacon paradoxus

France

M

16

Juberthie, 1956

Sabacon pygmaeus

Japan

M

14

Suzuki, 1966b

Trogulidae Trogulus closanicus

Austria

MF

26

N. Tsurusaki & J. Martens, unpub. data

Trogulus nepaeformis

France

M

20

Juberthie, 1956

Trogulus sp.

France

M

16

N. Tsurusaki & J. Martens, unpub. data (Continued)

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Table 6.1 Continued Taxa

Country

Sex

Number

References

USA

MF

78

Cokendolpher & Jones, 19911

Japan

M

40

Suzuki, 1966b

Goniosoma spelaeum

Brazil

M

92–109

Oliveira et al., 2000

Gonyleptes curticornis

Brazil

M

61–88

Oliveira et al., 2000

Mischonyx cuspidatus

Brazil

M

64–78

Oliveira et al., 2000

Neosadocus sp.

Brazil

M

68–81

Oliveira et al., 2000

Progonyleptoidellus striatus

Brazil

M

80–96

Oliveira et al., 2000

Pseudopachylus longipes

Brazil

M

65–87

Oliveira et al., 2000

LANIATORES Cosmetidae Vonones sayi Epedanidae Pseudobiantes japonicus Gonyleptidae

F = female; M = male. The symbol “/” indicates that no heterozygotic karyotype has been found between the two chromosome numbers, and “–” indicates that not only homozygotic karyotypes but also heterozygotic karyotypes have been found between the two chromosome numbers. Bs = B chromosomes. 1. Although Parthasarathy & Goodnight (1958) reported 2n = 25 (with XO sex chromosome system), these results are considered dubious.

Cyphophthalmi. Chromosomes have been reported for males of a single species, the sironid Siro rubens (Juberthie, 1956). The chromosome number of this species was 2n = 30, with all chromosomes appearing to be acrocentric. This diploid number is also shared by both males and females of Parasiro coiffaiti (Sironidae) from the Pyrenees (N. Tsurusaki & J. Martens, unpub. data). Eupnoi. This is the group of harvestmen for which information on chromosomes is most abundant (Table 6.1), probably because of higher availability of funding and lab equipment for researchers living in temperate regions of the Northern Hemisphere and the relatively large body size of the animals, which facilitates handling and dissection. Caddo agilis (Caddidae), which is the only species whose chromosome data are available in Caddoidea, has a chromosome number of 2n = 30 (Tsurusaki & Cokendolpher, 1990). Among Phalangioidea, phalangiids show higher chromosome numbers (2n = 16–36) than protolophids (2n = 18–20) and sclerosomatids (2n = 10–26). Among the latter, the number exhibited by the Gagrellinae (2n = 10– 22) seems to be lower compared with the Leiobuninae (2n = 16–26) and Sclerosomatinae (2n = 20–22). Dyspnoi. Chromosome numbers of this group are known for only seven species (Sokolow, 1929; Juberthie, 1956; Suzuki, 1966b; Tsurusaki, 1989), ranging from

Cytogenetics

2n = 10 to 28. The number seems to vary even among species within a single family (Table 6.1).

Laniatores. Only two species have been studied so far. Cokendolpher and Jones (1991) reported 2n = 78 in a North American cosmetid, Vonones sayi, most of which were short meta- or submetacentric chromosomes. No sex chromosomes were detected. In contrast, Suzuki (1966b) reported that the Japanese epedanid Pseudobiantes japonicus has n = 20 chromosomes (hence the diploid number is probably 40), although details of the observation have never been published. These chromosome numbers are among the highest in Opiliones when two tetraploid forms with 2n = ca. 48, found in the Japanese Leiobunum (Sclerosomatidae), are excluded. A precise count of the chromosome number in these species is, therefore, rather difficult, compared with species in the other three suborders. Recently, Oliveira and her colleagues began a chromosomal survey for South American representatives of Laniatores (see Table 6.1). Although none of their results have been formally published, the results are remarkable in two aspects: (1) they include the highest chromosome number (2n = 92–109) reported (from the gonyleptid Goniosoma spelaeum), and (2) extensive intra-and interindividual variation of chromosome numbers (Table 6.1).

Structure of chromosomes Harvestman chromosomes usually have a well-defined centromere, and metaand submetacentric chromosomes are far more frequently encountered in the karyotypes than acro- or subtelocentric ones. The predominance of meta- or submetacentric chromosomes in harvestmen contrasts markedly with the situation in spiders, in which telo- or acrocentric chromosomes are the norm (Suzuki, 1954; Cokendolpher & Brown, 1985; Tugmon et al., 1990; Tsurusaki et al., 1993; Gorlov et al., 1995; Gorlova et al., 1997). It is well known that chromosomes of mites are often holocentric or holokinetic, that is, each of their chromosomes lacks a localized centromere (Wrensch et al., 1994). Holocentric chromosomes are also known in some species belonging to spiders of the families Segestridae and Dysderidae (Benavente & Wettstein, 1980), as well as most species of Scorpiones (Shanahan, 1989a). In their review of holocentric chromosomes and inverted meiosis, Wrensch et al. (1994) suggested that holocentric chromosomes might be present also in Opiliones. This theory should be tested in future studies, especially when chromosomes observed are small and distinct constrictions are not detected.

Sex chromosome system Sex chromosome composition in Opiliones has been identified as usually XY-XX (male heterogametic), and the Y chromosome is always smaller than the X one (Tsurusaki, 1982a, 1985a,b; Tsurusaki & Holmberg, 1986; Tsurusaki & Cokendolpher, 1990). In Opiliones, no species with an XO-XX sex chromosome system has been found, although transition between the XY-XX and the XO-XX systems is considered

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to be somewhat common in various groups of insects, such as Orthoptera and Coleoptera (White, 1973), and the XO system and its derivatives (e.g., XXO and XXXO) are ordinary systems in Acari (Oliver, 1981, 1989) and Araneae (Hackman, 1948; Suzuki, 1954). In more than 300 species of spiders cytologically studied, the exception to the rule is found only in four species of the salticid genus Pellenes (Maddison, 1982). XY systems were found in Pseudoscorpiones (Troiano, 1990, 1997) and Acari (Flechtmann & Flechtmann, 1984; Helle et al., 1984). In contrast, the presence of female heterogamety with ZW (female)–ZZ (male) is suggested in two species of Phalangiidae, Mitopus morio (Tsurusaki & Cokendolpher, 1990) and Odiellus aspersus. The female heterogamety might be shared by other phalangiids since no heteromorphic pair of sex chromosomes has been found in males of six other species of the family so far reported. The ZW-ZZ system has never been reported in any species of Arachnida other than Opiliones. Moreover, mixed occurrence of XY-XX and ZW-ZZ systems in a monophyletic group at the ordinal level or below is rather rare (Bull, 1983), though it has been found even within a single species, such as the fly Musca domestica and the frog Rana rugosa (Miura et al., 1998).

Polyploidy When an organism bears more than two sets of homologous chromosomes, the individual is called a polyploid. Polyploidy is found in two parthenogenetic harvestmen, Leiobunum manubriatum and L. globosum, both of which are found in northern Japan. The two species are presumably facultative parthenogens, and males are found in some southern populations, although their frequencies are usually low (Tsurusaki, 1986). Leiobunum manubriatum consists of diploid males and females with 2n = 2x = 24 and tetraploid females with 2n = 4x = ca. 48 chromosomes (the number fluctuates from 46 to 49 as aneuploidy). In contrast, both males and females of L. globosum are tetraploids with 2n = 4x = ca. 48 chromosomes (the number varies among individuals, with the ranges 49–52 in males and 46–49 in females), and their karyotypes are quite similar to those of tetraploid females of L. manubriatum. Polyploidy is a somewhat common phenomenon in parthenogenetic animals (Suomalainen et al., 1987), but the occurrence of tetraploid males deserves attention, since polyploidy is extremely rare in bisexual animals. Müller (1925) and Ohno (1970) ascribed the rarity of polyploidy in animals to the prevalence of gonochorism and sex determination by heteromorphic sex chromosomes among them. It is remarkable that in both L. manubriatum and L. globosum the heteromorphic pair of chromosomes, which can safely be considered sex chromosomes, have been identified, although they might be dysfunctional.

B chromosomes B or supernumerary chromosomes are extra dispensable chromosomes whose number varies within populations of a single species, or often among cells of a single individual (Jones & Rees, 1982; Camacho, 2004). Why such dispensable chromosomes are maintained in populations is not yet fully understood. Some studies have

Cytogenetics

proposed a selective advantage of individuals with B chromosomes or of certain frequencies of B chromosomes within a population (Robinson & Hewitt, 1976; Plowman & Bougourd, 1994). However, other studies have failed to show such adaptive effects of Bs, and some of them even detected deleterious effects on their carrier and hence suggested their nature as selfish DNA (Hewitt et al., 1987; Werren et al., 1988; Shaw & Hewitt, 1990; R. N. Jones, 1991; Camacho et al., 1997; Muñoz et al., 1998). B chromosomes occur extensively in the sclerosomatid Psathyropus tenuipes, which shows strict coastal distribution in southwestern Japan (Tsurusaki, 1993; Gorlov & Tsurusaki, 2000a,b; Tsurusaki & Shimada, 2004). The Bs are widespread over the whole geographic range of the species, and nearly every individual possesses at least one B, while the mean number of Bs for the population reaches about four. The number of Bs often fluctuates to some extent even among cells from the same individual. The Bs are almost completely heterochromatic, varying considerably in size and morphology (Figure 6.1), and behaving as univalents at meiosis. The number of Bs detected increases northward throughout the Japanese islands, although the local number varies considerably as well. Populations along the Seto Inland Sea are characterized by a lower number of Bs (< 2) than those in other areas (Tsurusaki & Shimada, 2004). It has been revealed that embryos of the species contain fewer number of Bs than adults, suggesting that the number of Bs increases during embryonic and postembryonic development and that adult females of the species tend to lay eggs with fewer numbers of Bs. How and why such seasonal fluctuation and geographic variation of the number of B chromosomes emerge is still unknown.

a 2n = 18

b

2n = 18 + 10 B’s

c 2n = 18 + 19 B’s Figure 6.1. Some representative karyotypes of the Japanese harvestman Psathyropus tenuipes (Sclerosomatidae). (a) Nakajima Island in the Seto Inland Sea. (b) Maruyama, Sapporo, Hokkaido. (c) Campus of Hokkaido University, Sapporo. Chromosomes arranged on the second row in b and c are B chromosomes. Scale bar = 5 ␮m. Extracted from Tsurusaki (1993).

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Cytogenetics

Another intriguing phenomenon is found in B chromosomes of P. tenuipes. Gorlov and Tsurusaki (2000a) found that susceptibility to gregarines, which are protozoan parasites frequently found in the midgut of harvestmen, may differ between individuals with odd and even numbers of Bs in this species. For example, the infection rate by gregarines was lower in individuals with moderate numbers of Bs (4–6) than in those with both extremes (0–2 or 8–12) in B-even individuals, whereas no such trend was detected in B-odd individuals. This phenomenon differs from usual odd-even effects often reported in plants, such as rye and maize (Jones & Rees, 1982), in which some phenotypes vary in a zigzag pattern according to whether the number of Bs retained in an individual is odd or even. Further studies are needed in order to know whether this peculiar mode of odd-even effect in P. tenuipes is the norm in B chromosomes of this species. B chromosomes seem to be common also in other species of harvestmen. The chromosome number of Phalangium opilio (Phalangiidae) shows variation in some European populations (e.g., 2n = 24–26 in a population in Mainz, Germany), suggesting involvement of B chromosomes (N. Tsurusaki & J. Martens, unpub. data). The enormous discrepancy in reported chromosome numbers in P. opilio between populations in western Europe, Russia, and North America (see Table 6.1) may also be caused by the fluctuation of B chromosome numbers. In the distributional ranges of the 2n = 20 karyotype of the sclerosomatid Nelima nigricoxa (Sclerosomatidae) in western Japan, individuals with 2n = 22 have been rarely found always as an intrapopulational polymorphism. The 2n = 22 karyotype seems to be derived from an addition of two large isochromosomes to the normal karyotype with 2n = 20 (N. Tsurusaki, unpub. data).

GEOGRAPHIC DIFFERENTIATION OF KARYOTYPES AND CHROMOSOMAL HYBRID ZONES As previously stated, the number of chromosomes in harvestmen often fluctuates considerably among closely related species. The numerical variation of chromosomes has been found frequently even within a single species when more than one population was surveyed for the species. These include the sabaconid Sabacon makinoi and the sclerosomatids Leiobunum montanum, L. tohokuense, Gagrellula ferruginea, Gagrellopsis nodulifera, Nelima nigricoxa, and N. satoi (references in Table 6.1). Ubiquitous geographic variation in the karyotypes of harvestmen contrasts with that of spiders, whose karyotypes are often invariable even at the familial level and are almost completely invariable within a species; one of the very rare exceptions is the Australian sparassid Delena cancerides (Rowell, 1985; Hancock & Rowell, 1995). This phenomenon is ascribed to the low vagility of Opiliones that promotes inbreeding in small isolated populations, a condition required for the establishment of a population fixed for a newly emergent karyotype. Suzuki (1956, 1959) first recognized the variation in chromosome number in Gagrellula ferruginea and its relatives, as well as in the curvipalpe group of Leiobunum

Cytogenetics

(Suzuki, 1957, 1976a,b). He first tried to use this chromosomal information as the basis for species delimitation of those “taxonomically difficult” species because of enormous geographic differentiation in external morphology, including male genitalia (Suzuki, 1976a,b). However, information accumulated so far suggests that the differences in chromosome number usually do not work as insurmountable barriers to gene flow, and when two races with different chromosome numbers abut emergence of a hybrid zone is the norm, rather than accomplishment of a distributional overlap. A more comprehensively studied example of such chromosomal hybrid zones is the case of the Japanese harvestman Gagrellopsis nodulifera. This species, occurring on Honshu, Shikoku, and Kyushu, is univoltine with adult emergence in spring (May to June). Although the species is extremely conservative in external morphology, the diploid chromosome number of the species varies from 14 to 22 even in a small area from Tottori Prefecture to the northern part of Hyogo Prefecture in the Chugoku Mountains, southwestern Honshu (Tsurusaki et al., 1991; Gorlov & Tsurusaki, 2000c). Each population forms a hybrid zone with neighboring populations with different chromosome numbers where they abut, unless they are isolated by open plains along a river. Of those hybrid zones, the most spectacular example can be found in the Chizu area, which corresponds to the upper basin of the Sendai River in the eastern part of Tottori Prefecture, where two races with 2n = 16 and 2n = 22 meet and hybridize (Tsurusaki et al., 1991). The width of this hybrid zone ranges between 5 and 15 km (Gorlov & Tsurusaki, 2000a; Figure 6.2). Gorlov and Tsurusaki (2000a) investigated frequencies of each karyotype in eight populations along the Ashizu Gorge, which runs across the hybrid zone (Figure 6.2). The authors found that no populations harbor the whole range of karyotypes from 2n = 16 and 22 within this zone, and the mean number of chromosomes per population gradually changed. Variation in the chromosome number was formerly ascribed to Robertsonian rearrangements (Tsurusaki et al., 1991), but detailed analyses of meiosis of karyotypic heterozygotes revealed involvement of tandem fusion/fission, at least to a certain extent. This was due to dicentric chromosomes or chromosomes with unequal chromatids, both of which are expected to emerge in meiosis of karyotypic heterozygotes when tandem fusion/fission was the case. Frequencies of intermediate homozygotes with 2n = 18 and 2n = 20 were much higher, whereas the frequencies of karyotypic heterozygotes (especially di- and triheterozygotes) were lower than those expected from the Hardy-Weinberg theorem. The more trivalents a karyotype retained, the greater its deficiency. Frequencies of nondisjunction at meiosis of heterozygotes (2n = 17, 2n = 19, and 2n = 21) were invariably about 0.1 on average. This frequency is much higher than those (0.03– 0.04) obtained for Nelima nigricoxa in two hybrid zones (2n = 16/17/18 and 2n = 18/19/20) around Mt. Daisen, western Honshu, which resulted from Robertsonian rearrangements (Tsurusaki & Gorlov, unpub. data). It is known that frequencies of nondisjunction usually become higher than the centric fusion/fission, that is, Robertsonian rearrangement, when tandem fusion/fission is involved in the heterozygote (Spirito, 1998). In the hybrid zone, double heterozygotes that bear two trivalents at meiosis are also found, although their frequencies are low. It was found

275

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Cytogenetics

Figure 6.2. Changes in frequencies of individuals of the harvestman Gagrellopsis nodulifera (Sclerosomatidae) with different chromosome numbers through collecting sites along the Ashizu Gorge, upper reach of the Sendai River in eastern Tottori Prefecture, southwestern Honshu, Japan (photo: N. Tsurusaki). The numbers inside the histograms indicate the sample of individuals studied for each locality. Population numbers correspond to those used in Figure 1 of Gorlov and Tsurusaki (2000c).

that frequencies of chromosomes with unequal chromatids or dicentric chromosomes are extremely inflated compared with single heterozygotes with only one trivalent or homozygotes. As the process that forms this hybrid zone, the following scenario can be envisaged. Initially, when two forms with 2n = 16 and 2n = 22 first meet, triple heterozygotes result from the hybridization of the two forms (2n = 19 = 8 + 11). Extremely high frequencies of abnormal meiosis are expected at meiosis of the heterozygote, and production of normal sperm is extremely hampered. However, if some normal

Cytogenetics

gametes are produced in those triple heterozygotes, and those heterozygotes backcross with individuals with one of the parental karyotypes, problems in offspring production are reduced. Then the hybrid zone enlarges its width by repeating hybridization with parental 2n = 16 and 2n = 22 populations at both lateral sides. During the process a cline emerges for the distribution of chromosome number within the hybrid zone. As the width of the hybrid zone increases, secondary hybrid zones in each of which difference in chromosome number is only two gradually emerge by natural selection since decrease of fitness in a simple heterozygote is trivial and relative fitness of intermediate homozygotes with 2n = 18 or 2n = 20 is high. At the final stage, populations fixed for those intermediate homozygotes with 2n = 18 or 2n = 20 and three secondary hybrid zones where difference of chromosome number is only 2 (2n = 16/18, 18/20, 20/22) are formed within an initial hybrid zone. Such outcomes for a hybrid zone formed between two chromosomal races differing by two or more steps in chromosome number were first envisaged in chromosomal hybrid zones in mice, referred to as “staggered hybrid zones” (Searle, 1991, 1993). Situations in the hybrid zone in the Ashizu Gorge correspond to the second stage in the scenario just described. In contrast, populations almost fixed for 2n = 20 are found near the Kuroo Pass on the mountain ridge between Tottori and Okayama, where the hybrid zone is about 15 km wide. In many chromosomal hybrid zones detected so far in harvestmen, the difference in the chromosome number between the two parental populations is two (one step). Those hybrid zones may include the zone that originally initiated from hybridization between two races whose difference in chromosome number was two steps or more, but changed to staggered hybrid zones through natural selection. Natural selection against karyotypic heterozygotes is thus likely to result in degeneration of a single hybrid zone whose chromosomal change is two steps or more into two or more hybrid zones, in each of which the change is just one step, where the difference in diploid chromosome number is two. Does such negative heterosis in heterozygotes promote reproductive isolation between the two chromosomal races? It is very likely that the chromosomal heterozygotes are negatively selected by natural selection because of nondisjunction at their meiosis. However, at least a part of their offspring return to homozygotes unless their gamete production is incompletely hindered. Those homozygotes do not show any abnormalities in the gamete production. Thus it is unlikely that these chromosomal hybrid zones work as barriers to gene flow between the two chromosomal races at both ends of the respective zones.

CHROMOSOME POLYMORPHISM THAT MAY BE RELEVANT TO MALE DIMORPHISM Intrapopulational polymorphism in chromosome number that cannot be categorized as B chromosomes, sex chromosomes, or a chromosomal hybrid zone is known

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Cytogenetics

in Protolophus tuberculatus (Protolophidae). Males of this species are dimorphic (normal and effeminate) in pedipalpal size. Of the two males (one normal and one effeminate) studied, Tsurusaki and Cokendolpher (1990) found that the normal male had 2n = 18, whereas the effeminate male showed 2n = 20. This suggests a possible relevance between the chromosomal polymorphism and the male dimorphism in external morphology of the species. In the salticid spider Maevia inclemens, also with male dimorphism, it was shown that the two male morphs are genetically determined by involvement of accessory chromosomes (Painter, 1914). Further study is needed of the chromosomes of P. tuberculatus.

CONCLUDING REMARKS Although the study of chromosomes in Opiliones is in a nascent state, a survey of the information accumulated thus far suggests that this is a very prolific and promising field. Of the various chromosomal phenomena that can be encountered in cytogenetic harvestmen studies, the most noteworthy would be their enormous variability in chromosome number in space. In the family Sclerosomatidae, geographic variation in chromosome number can be found in as many as seven species in the Tottori Prefecture, Japan. This number corresponds to about twothirds of the total species number of sclerosomatid harvestmen found there. Much remains to be learned about the forces related to their chromosomal diversity. As stated earlier, it is likely that their low vagility upholds a prerequisite for the fixation of a karyotype newly arisen through chromosomal rearrangements. Conversely, there are species whose chromosomes are quite invariable both in number and morphology. This is exemplified by Melanopa grandis, which invariably shows a karyotype with 2n = 20 in more than 20 populations karyotyped over a wide geographical range (Tsurusaki & Cokendolpher, 1990) despite its enormous geographic differentiation in external morphology (Suzuki, 1972a). The source of these differences will need to be addressed in future studies. Another chromosomal feature that is intriguing from a different perspective is the uniqueness of the suborder Laniatores, shown by its dramatically higher number of chromosomes compared with the other groups of harvestmen. The meaning of such differences remains a mystery. However, a long stagnant period in research activity for chromosomes in Laniatores seems to have recently dissolved; hence increased attention to sampling will provide improved insights in systematics and phylogeny of the suborder, as well as Opiliones as a whole.

ACKNOWLEDGMENTS I thank J. C. Cokendolpher and R. Pinto-da-Rocha for their critical reading of the manuscript. Some unpublished data for European species cited in Table 6.1 were ob-

Cytogenetics

tained during my stay at Professor J. Martens’s lab in 1993, with the help of Drs. J. Gruber, F. Damico, and I. Gorlov. Thanks are also due to Dr. N. Takagi, Professor Emeritus of Hokkaido University, who taught me an air-drying technique with lactic acid treatment when I was a postgraduate student. In honor of his ninety-first birthday in 2005, this review is dedicated to Dr. Seisho Suzuki, Professor Emeritus of Hiroshima University, who pioneered harvestman cytotaxonomy.

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CHAPTER

7

Ecology David J. Curtis and Glauco Machado

H

arvestmen are a common component of terrestrial environments and, as we intend to show in this chapter, are often an appropriate subject for ecological studies. They are dense and diverse in many habitats, are easy to detect and collect, and in many countries (especially in temperate regions) are reasonably well known taxonomically. Although a great amount of ecological information about harvestmen exists in the form of quantitative samplings throughout the world, few attempts have been made to understand their general patterns of species occurrence in both time and space. After searching a wide range of synecological literature, we have assembled here most of the information on species occurrences in different habitats and their co-occurrences in communities in order to discuss the emergent trends. In the first two sections of this chapter we consider spatial and temporal patterns of species distributions, stressing the major environmental factors related to harvestman abundance and richness. In the third section we present basic data on harvestman communities, with special reference to species richness and relative abundance, trophic relationships, and resource partitioning. Finally, we discuss the impact of human activity on harvestman populations by providing some examples in which they are negatively or positively affected and mentioning some endangered species.

SPATIAL PATTERNS Distribution and habitat use Harvestmen appear to be ubiquitous, being found in all continents except Antarctica from the equator to high latitudes (81°N and 56°S; Cokendolpher & Lanfranco, 1985). We can find them in a great variety of habitats: in soil, moss, leaf litter, and grassy clumps; under rocks, stones, and debris; on vertical surfaces from tree trunks to stone walls; and running over tall vegetation (Cloudsley-Thompson, 280

Ecology

281

1958). The most diverse harvestman communities are reported for tropical areas (Figure 7.1A), especially humid forests. In fact, 18 of the 20 communities reported to have 20 or more species occur in tropical areas. Perhaps the localities with the richest communities in the world are found in the coastal Atlantic forest of Brazil, where the harvestman fauna commonly exceeds 25 species in a given area (Pintoda-Rocha, 1999; Pinto-da-Rocha et al., 2005). There is a clear decline in species richness toward the poles, and accordingly, in temperate regions it rarely exceeds 12 species in a community (Figure 7.1A). This pattern of distribution has been widely reported for many taxonomic groups, such as insects, arachnids, several vertebrates, and plants, and may be related to ecological and/or phylogenetic factors (review in Wiens & Donoghue, 2004; see also Chapter 3).

A

B

Figure 7.1. (A) Histogram showing the distribution of local richness of harvestman species in tropical and temperate communities. (B) Box-plot (median, quartiles, and maximumminimum values) of the local richness of harvestman species in forested (n = 89 sites) and open habitats (n = 70 sites) around the world (Mann-Whitney, Z(U) = 7.539; p < 0.0001). Sources: Europe: Todd (1949);Williams (1962); Pearson and White (1964); Curtis (1973, 1975, 1978a,b); Davis and Jones (1978); Chemini (1980, 1981); Löser (1980); Bliss et al. (1981); Bliss (1982); Adams (1984); Almquist (1984); Bliss and Tietze (1984); Hippa et al. (1984); Rambla (1985); Schaefer (1986); Decleer and Segers (1989); Blick and Bliss (1991); Owen (1991); Alderweireldt et al. (1993); Gruber (1993); Freudenthaler (1994a,b, 1999); Ru˚ˇzicˇka et al. (1995); Komposch (1996, 1997a,b, 2000a); Docherty and Leather (1997); Komposch and Gruber (1999); Loch (1999); Zingerle (1999); Dennis et al. (2001); Hicks et al. (2003). North America: Edgar (1971); Carter and Brown (1973); Jennings et al. (1984); Corey and Stout (1990); Cokendolpher et al. (1993); Koponen (1994). South America: Cokendolpher and Lanfranco (1985); Capocasale and Gudynas (1993); Gnaspini (1996); Pinto-da-Rocha (1999); Adis (2002); Bragagnolo and Pinto-da-Rocha (2003; unpublished data); Brescovit et al. (2004); Almeida-Neto et al. (2006); L. E. Acosta (unpublished data); A. B. Bonaldo (unpublished data). Japan: Tsurusaki (1999, 2003).

282

Ecology

Although harvestmen appear to be more diverse in mesic environments, they are not uncommon in xeric environments, even deserts (Hunt, 1991; Cokendolpher et al., 1993). The sclerosomatid Trachyrhinus marmoratus, for instance, may be locally very abundant in desert areas of the Chihuahuan Desert in the southern USA (MacKay et al., 1992). However, if we analyze the harvestman richness from different types of habitats, a striking pattern emerges: median richness of harvestmen in forested habitats is 2.8 times higher than in open habitats, including grasslands, rocky landscapes, deserts, gardens, and bogs (Figure 7.1B). Open habitats show marked seasonal variations in abiotic factors, mainly temperature and humidity, which probably restrict the occurrence of many harvestman species (see Chapter 14). Additionally, forested habitats are structurally more complex and probably provide a greater diversity of suitable habitats. Some harvestmen occur in mountain and alpine habitats, being recorded as high as 4,000 m in the Himalayas (Martens, 1984, 1993a) or in the páramos of Colombia (Roewer, 1914b), but species richness seems to decrease with altitude. Empirical data on altitudinal distribution for harvestmen are scarce, but our analysis of harvestman vertical distribution (900–3,300 m) in the Eastern Alps from Komposch and Gruber (1999) revealed a monotonic decrease in species richness along the elevational gradient (R2 = 0.81; F = 46.01; p < 0.001). Moreover, species with higher mean elevations tended to cover broader elevational range sizes, thus inflating the species number at lower elevational bands. Species at higher elevations probably have more tolerance to changes in climatic factors, such as temperature and humidity, because the climate is more variable at mountaintops. This pattern of distribution is known as “Rapoport effect” (Blackburn & Gaston, 1996) and has been described for butterflies (Fleishman et al., 1998) and ants (Sanders et al., 2003). In the future, studies in tropical and small elevational ranges would help the understanding of how harvestman richness changes along gradients where the variability in climatic factors is less accentuated than in temperate regions. Regarding spatial distribution and habitat occupancy of individual species, some harvestman species, especially those of the suborder Eupnoi, can have a wide distribution and can be found in a wide range of habitats (see also Chapter 3). Perhaps the most widespread harvestman species is the phalangiid Mitopus morio, a Palearctic species that occurs in North Africa, Europe, Asia north of the Himalayas, and Canada and presents a broad habitat occupancy, ranging from woodlands to tundra and from sea level to high–altitude montane locations (Slagsvold, 1976; Bliss & Arnold, 1983; Tchemeris et al., 1998; Tchemeris, 2000). As would be expected, this species is not uniformly distributed over its environmental ranges and usually consists of a number of disjunct populations inhabiting distinct habitats. Therefore, some phenotypic differences have been found among populations of M. morio, as described by Jennings (1983). Similar cases of morphological variation were described early on for certain species of Leiobunum (Sclerosomatidae) along a latitudinal gradient in the USA (Weed, 1893b). There is a gradual increase in body size and leg length in individuals of L. vittatum, L. ventricosum, L. politum, and L. aldrichi from the north to at least as far south as latitude 37°N. Additionally, the proportionate increase in the leg length southward seems to be greater than that of the body. According to Weed (1893b), the

Ecology

most important factors determining this increase in size are probably the climatic conditions that, with the decreased seasonality and snow period in the south, presumably result in a more abundant food supply and longer period of growth. Contrary to the examples just cited, many harvestman species, including most Cyphophthalmi and Laniatores, are much more limited in geographic distribution and habitat use (see also Chapter 3). This is especially the case with cave dwellers, or troglobites, which are found among all suborders of Opiliones (Rambla & Juberthie, 1994). The genus Texella (Phalangodidae), for instance, occurs in caves from the southern USA, and most of its representatives are considered to be troglobites (Ubick & Briggs, 1992; Figure 7.2A). Troglophiles are those organisms in which some populations complete their life cycles inside caves, while others do not. The troglophilic “Daguerreia” inermis (Gonyleptidae), for example, occurs in several caves in southeastern Brazil but was also recorded from epigean habitats far from caves (Pinto-daRocha, 1996b; Figure 7.2B). Trogloxenes are those organisms that use caves only part of their lives, such as certain species of the genus Gyas (Sclerosomatidae), which enter caves to hibernate during winter snow in eastern Europe (Novak et al., 2004), and species of the subfamily Goniosomatinae (Gonyleptidae), which use caves for diurnal shelter and during reproduction (Machado, 2002). Cave-dwelling harvestmen may exhibit some adaptations to subterranean habitat that generally are more evident among the troglobites (Figure 7.2A). One of these adaptations is the reduction or even complete loss of the eyes (e.g., Juberthie, 1964). Among some cavernicolous species the ocularium is present, but no eyes are visible externally; among others the eyes are present, but the retina does not have the characteristic black color and seems to be nonfunctional. Other common subterranean features are the increased length of the legs, partial or total absence of tegumentary pigmentation, and weak sclerotization of the cuticle (Goodnight & Goodnight, 1960). Little is known about the physiological adjustments of these cavernicolous animals, but they are probably less tolerant to changing conditions in their environment than related species living outside the caves. Morphological adaptations probably related to habitat use may also be found among noncavernicolous species. Species that live mostly on the vegetation present a greater number of tarsal segments than their relatives that live on the ground. This is the case for some arboricolous gonyleptids belonging to the subfamilies Caelopyginae, Progonyleptoidellinae, and Sodreaninae, which have 8 to 12 segments in the tarsi III and IV (Figure 7.2C). Their closest relatives of the subfamilies Hernandariinae and Gonyleptinae spend most of their lives on the ground and the number of tarsal segments in legs III and IV is always less than 8 (Figure 7.2D). It is possible that a greater number of segments helps harvestmen cling onto vegetation by forming coils at the end of their legs (Guffey et al., 2000; see also Chapter 2). Fine-scale habitat preferences may contribute to the distribution of species between microhabitats, with, for example, different species spending more time in different layers of vegetation (Edgar, 1990). Thus small, short-legged species, such as trogulids and nemastomatids (Figure 7.2E), live in the soil or leaf litter, while larger species, including the oligolophines, are found mainly in the ground-layer vegetation. Longer-legged species occur predominantly higher up on the branches of

283

A

B

D

C

E

F

Figure 7.2. (A) The phalangodid Texella cokendolpheri, a strictly cavernicolous species that presents elongated appendages and marked eye reduction (photo: J. Krejca). (B) The troglophilic “Daguerreia” inermis (photo: R. Pintoda-Rocha). (C) The gonyleptid Iporangaia pustulosa, an arboricolous species that inhabits moist forests in southeastern Brazil and has from 14 to 19 tarsal segments in legs III and IV (photo: B. A. Buzatto). (D) The gonyleptid Neosadocus maximus, a ground-dwelling species, also from southeastern Brazil (photo: G. Machado). Although this species is a close relative of I. pustulosa, it has fewer tarsal segments in legs III and IV (4 to 5), which correspond to the plesiomorphic state and are related to a terricolous habit. (E) The short-legged nemastomatid Dendrolasma parvula, a species that lives in the soil and leaf litter in Japanese forests (photo: N. Tsurasaki). (F) The long-legged Mitopus morio, which is commonly found higher up on the branches of shrubs (photo: J. G. Warfel). Scale bars = 10 mm.

Ecology

shrubs (e.g., Mitopus morio; Figure 7.2F) or on tree trunks and up in the canopy (e.g., Leiobunum rotundum and Phalangium opilio). It is noteworthy, however, that the distribution of different species relative to environmental strata may depend on their foraging activities and may also vary with time of day (Todd, 1949; see also Chapters 8 and 14). Moreover, the relationship between leg length and habitat use seems to apply only for some North American and European species, but not for most tropical Laniatores. Thus, although widely reported in the opilionological literature, this relationship should be viewed with care and deserves rigorous testing, taking into account the phylogeny of the group. Some harvestman species may also occur in very specific microhabitats, as is the case for the gonyleptid Riosegundo birabeni, which lives inside the nests of the leafcutter ant Acromyrmex lobicornis. Maury and Pilati (1996) suggest that ant nests provide a wetter microhabitat that allows this harvestman to colonize arid zones in Argentina. Tank bromeliads are also frequently occupied by harvestmen (e.g., González-Sponga, 1987, 1992b), probably because these plants accumulate water and thus provide a suitable microenvironment that prevents climatic stress. Indeed, some harvestman species are entirely dependent on tank bromeliads for reproduction, such as the gonyleptid Bourguyia albiornata (Machado & Oliveira, 2002; see also Chapter 12). Some triaenonychids, such as Muscicola picta and Algidia viridata, appear to be restricted to moss, and their green coloration probably functions as camouflage (Cloudsley-Thompson, 1958). Another interesting example is the Brazilian escadabiid Baculigerus littoris, which is mainly found in the intertidal zone among debris (Soares, 1979). As our knowledge of the biology of harvestmen increases, many more examples of microhabitat specificity will probably be discovered.

Influence of physical factors The influence of physical factors on the spatial distribution of harvestmen has rarely been studied. Todd (1949) stated that temperature and humidity are the most important determinants of harvestman distribution and habitat use. Unlike scorpions and many spiders, harvestmen are very susceptible to dehydration, and the need for moist habitats is probably a significant ecological factor that limits the occurrence of most species of the order in xeric zones (see Chapter 14). Young nymphs are particularly vulnerable to desiccation and thus spend most of their time in leaf litter, under logs and rocks, and in other moist microhabitats. As they grow, individuals ascend to the vegetation, as was recorded for several species of the families Sclerosomatidae and Phalangiidae (Todd, 1949; Edgar, 1971). The most comprehensive study of the influence of environmental parameters, such as relative humidity and temperature, on harvestman distribution was done by Edgar (1971), who reported laboratory results for four species of Leiobunum consistent with their preferred microhabitats in the field (see Table 14.1). Leiobunum vittatum—cited as one of the most widespread species in the northeastern USA, living in a wide variety of habitats from dense woodland to open bogs—had the highest temperature preference and the lowest relative humidity preference, survived longest in dry air, and lost

285

286

Ecology

the least weight under desiccation. At the other extreme, the corresponding values for L. politum, a species vulnerable to low humidity, are consistent with its life in litter in very moist situations. L. calcar, another species found to be vulnerable to low humidity, often lives in ecotones with openings in the canopy that allow penetration of rain and dew, but avoids sunlight by inhabiting litter. The fourth species, L. aldrichi, had the lowest temperature preference but was intermediate in terms of relative humidity preference, which is consistent with its favored habitat of moist, cool shade under dense woodland canopy where the shrub layer is sparse. The influence of habitat structure on harvestman abundance and distribution remains poorly explored. Working with a harvestman community in woodlands of southeastern England, Adams (1984) found that leaves of different sizes resulted in a litter layer of contrasting characteristics of density and compressibility, which in turn favored the occurrence of different harvestman species. Thus the short-legged Nemastoma bimaculatum (Nemastomatidae) was associated with the dense beech litter, while the long-legged Lacinius ephippiatus (Phalangiidae) was most frequent in chestnut litter, which has larger interleaf spaces. Moreover, on the basis of the general distribution of species in woodlands, Adams (1984) suggested that habitat structure could be an important factor affecting harvestman distributions. Edgar (1971) also showed that different harvestman species are found in different vegetation types in woodlands from Michigan, USA. The results, however, may be attributed to differential preferences of the species to the microclimatic conditions generated by each type of vegetation rather than a specific association between harvestmen and vegetation characteristics. Corey and Stout (1990) showed that the abundance of harvestmen in sandhills in Florida (USA) was not correlated with shrub density, ground cover, or plant litter. In another study Jennings et al. (1984) showed that litter depth had little influence on either mean catches of ground harvestmen or the mean number of harvestman species. Therefore, more studies allied with experimental manipulation of the habitat structure are necessary in order to better understand the causal effects of habitat structure on harvestman distributions. Unlike to scorpions (Polis, 1990), harvestman distributions do not seem to be greatly influenced by edaphic factors. In the case of the Trogulidae, however, there is a clear pattern of occurrence in places where the soils are derived from limestone and are thus rich in calcium carbonates. Since representatives of this family feed exclusively on snails (see Chapter 8)—animals that require calcium carbonate from the soil to build their shells—the distribution of trogulids may actually reflect the distribution of their prey (Hillyard & Sankey, 1989).

TEMPORAL PATTERNS Phenology is concerned with the evident activity of a species over the course of the year and usually focuses on recognizing when adults are active and mobile. A trawl through much of the available literature has provided data for Table 7.1, which lists the phenological patterns for 71 harvestman species in 16 countries.

X

MAY

xX

xX

xX

xX

X

xX

xX

x

xX xX

X

x

xX

xX

X

X

xX

xX

H. quadridentatus

x

x xX

X

xX

X

X

xX

X

xX

xX

X

x

X

xX

x

X

xX

X

X

xX

x

X

xX

X

X

X

X

JUL

Homalenotus quadridentatus

x

x

H. palpale

H. suzukii

xX

xX

H. nepalense

xX

x

Himalphalangium dolpoense xX

x

X

H. nigrolineata

xX

xX

H. instructa

xX

x

X

X X

—

X

—

X

Harmanda kanoi

—

X

G. annulatus

Gyas annulatus

X

X

Globipes sp.

xX

Gagrella varians

xX

X

X

Euzaleptus minutus

X

xX

x

Dalquestia formosa

xX X

x

X

X

X

X

JUN

Centetostoma bacilliferum

Caddo agilis

X

X

X

APR

X

—

X

MAR

A. laevipes

—

X

FEB

X

—

X

JAN

Astrobunus laevipes

Amilenus aurantiacus

EUPNOI

Parogovia pabsgarnoni

CYPHOPHTHALMI

Taxa

environments

xX

X

X

X

x

X

x

xX

X

X

X

xX

xX

xX

x

X

X

X

X

xX

X

X

x

x

X

X

X

xX

xX

X

x

X

x

X

AUG SEP

x

X

x

xX

xX

X

X

xX

X

X

xX

X

OCT

xX

x

X

xX

X

X

—

xX

X

X

xX

X

—

X

NOV

xX

x

x

xX

X

X

—

X

X

X

—

X

DEC

Spain

Spain

Himalayas

Himalayas

Himalayas

Himalayas

Himalayas

Himalayas

Himalayas

Czech Rep.

Austria

New Mexico

Himalayas

Himalayas

Texas

Spain

Japan

Austria

Austria

Austria

Sierra Leone

Locality

woodland

grassland

montane

montane

montane

montane

montane

montane

montane

woodland

montane

montane/ wood

montane

montane

grassland

woodland

woodland

woodland

open

montane

woodland

Environment

(Continued)

Rambla, 1985

Rambla, 1985

Martens, 1993a

Martens, 1993a

Martens, 1993a

Martens, 1993a

Martens, 1993a

Martens, 1993a

Martens, 1993a

Borek, 1958

Komposch, 1997a

Cokendolpher et al., 1993

Martens, 1993a

Martens, 1993a

Cokendolpher & Sissom, 2000

Rambla, 1985

Tsurusaki, 2003

Freudenthaler, 1994b

Komposch, 1996

Komposch, 1997a

Legg & PabsGarnon, 1989

Source

Table 7.1 Seasonal patterns of activity for a range of species in different parts of the world, indicated by “Locality” (states, in the USA), and in different

—

L. blackwalli

L. townsendi

L. rupestre

L. rotundum

L. rotundum

x

x

x

—

—

— x

x

xX

xX

X

x

xX

X

X

X

xX

X

X

X

X

xX

X

X

X

xX

X

X

X

X

X

X

L. rotundum

X

xX

X

xX

X

xX

x

X

X

X

X

X

AUG SEP

X

—

xX

xX

xX

xX

x

x

X

X

xX

X

X

X

JUL

L. rotundum

—

x

x

x

L. rotundum

L. rotundum

x

X

X

x

x

—

—

L. manubriatum

—

—

—

X

L. japonicum

—

—

L. blackwalli

L. globosum

X

Leiobunum blackwalli

L. horridus

X

L. horridus

x

X

X

X

X

X

JUN

L. ephippiatus

x

x

x

x

x

x

L. ephippiatus

X

MAY

L. ephippiatus

X

APR

X

MAR

L. ephippiatus

x

FEB

X

x

JAN

L. ephippiatus

Lacinius ephippiatus

Taxa

Table 7.1 Continued

xX

—

X

X

xX

X

X

X

xX

xX

X

OCT

xX

—

X

—

X

X

—

X

X

X

x

NOV

xX

—

—

—

X

—

—

X

x

DEC

New Mexico

Austria

Wales

England

Austria

Germany

Germany

Spain

Japan

Japan

Japan

Austria

Germany

Spain

Austria

Germany

Wales

Germany

England

Austria

Austria

Scotland

Locality

montane

woodland

montane

grass/wood

woodland

grassland

woodland

woodland

woodland

woodland

woodland

woodland

woodland

woodland

woodland

grassland

montane

woodland

grass/wood

woodland

open

woodland

Environment

Cokendolpher et al., 1993

Freudenthaler, 1994a

Pearson & White, 1964

Phillipson, 1959

Bliss, 1982; Freudenthaler, 1994b

Bachmann & Schaefer, 1983b

Bliss et al., 1981

Rambla, 1985

Tsurusaki, 1986

Tsurusaki, 2003

Tsurusaki, 1986

Bliss, 1982

Bliss et al., 1981

Rambla, 1985

Freudenthaler, 1994b

Bachmann & Schaefer, 1983b

Pearson & White, 1964

Schaefer, 1986

Phillipson, 1959

Freudenthaler, 1994a,b

Komposch, 1996

Curtis, 1978a

Source

x

x

x

xX

M. morio

x —

—

M. morio

—

M. morio

— X

—

M. morio

M. morio

M. morio —

x

—

x

X

—

x

X

X

x

—

M. morio

— X

—

X

M. morio

Mitopus glacialis

Metopilio sp.

x

X

x

X

x

x

X

x

xX

X

xX

X

xX

xX

X

x

xX

X

xX

X

X

X

xX

X

X

X

xX

xX

x

X

x

M. diadema

X

x

X

X

X

x

X

x

X

M. diadema

Megabunus diadema

L. palpinalis

L. palpinalis

X

X

x

L. palpinalis

x

X

x

x

x

x

X

—

L. palpinalis

x

—

x

—

L. palpinalis

Lophopilio palpinalis

Leiobunum sp.

X

X

X

X

xX

X

X

xX

x

X

X

xX

X

X

X

X

X

X

xX

X

X

x

X

X

X

xX

X

X

—

X

X

—

xX

X

—

X

x

X

X

X

X

X

—

—

X

—

x

X

—

X

x

X

X

xX

—

Wales

Norway

England

Wales

Austria

Austria

Germany

Scotland

Austria

New Mexico

England

Wales

Scotland

Wales

England

Scotland

Germany

Germany

Austria

Austria

montane

woodland

grass/wood

montane

montane

woodland

woodland

woodland

montane

montane

woodland

montane

woodland

montane

grass/wood

woodland

woodland

grassland

rocky

montane

(Continued)

Pearson & White, 1964

Solem & Hauge, 1973

Phillipson, 1959

Goodier, 1970

Komposch, 1997a

Freudenthaler, 1994b

Bachmann & Schaefer, 1983b

Curtis, 1978a

Komposch, 1997a

Cokendolpher et al., 1993

Phillipson, 1959

Goodier, 1970

Curtis, 1978a

Pearson & White, 1964

Phillipson, 1959

Curtis, 1978a

Bachmann & Schaefer, 1983b; Schaefer, 1986

Bachmann & Schaefer, 1983b

Freudenthaler, 1999

Komposch, 1997a

—

—

x

X

X

x

X

x

xX

O. tridens

O. tridens

X X

x

x

X

x

O. tridens

X

X

x

O. tridens

O. hanseni

O. hanseni

X X

O. troguloides

O. troguloides

Oligolophus hanseni

x x

O. aspersus

X

x

X

X

X

xX

X

X

X

xX

xX

xX

xX xX

xX

xX

xX

x

xX

x

x

x

Odiellus aspersus

x

x

x

N. suzukii

xX

N. suzukii

xX

xX

X

X

X

xX

X

X

X

X

X

X

X

X

X

X

X

X

X

xX

X

—

xX

xX

xX

X

X

X

AUG SEP

N. semproni

x

xX

xX

X

X

JUL

X

x

x

xX

X

JUN

N. semproni

N. genufusca

X

xX

X

MAY

x

X

x

X

APR

Nelima genufusca

M. chrysomelas

x

—

x

x

—

—

M. chrysomelas

—

M. chrysomelas

—

X

MAR

X

—

M. chrysomelas

X

FEB

M. chrysomelas

X

JAN

Mitostoma chrysomelas

Taxa

Table 7.1 Continued

X

X

X

X

X

X

X

X

X

X

X

—

X

X

X

X

X

—

X

OCT

X

X

X

X

X

X

X

X

X

X

X

X

xX

X

—

X

X

NOV

X

X

X

X

X

X

—

xX

—

—

X

DEC

Germany

Austria

Austria

Scotland

Scotland

England

Spain

Spain

Spain

Japan

Japan

Japan

Japan

Austria

Austria

Wales

Netherlands

Wales

Austria

Austria

Scotland

Locality

woodland

rocky

open

woodland

woodland

grass/wood

woodland

woodland

grassland

woodland

woodland

woodland

woodland

woodland

open

woodland

woodland

montane

grassland

montane

montane

woodland

woodland

Environment

Bachmann & Schaefer, 1983b; Bliss et al., 1981

Freudenthaler, 1999

Komposch, 1996

Curtis, 1978a

Curtis, 1978a

Phillipson, 1959

Rambla, 1985

Rambla, 1985

Rambla, 1985

Tsurusaki, 2003

Tsurusaki, 2003

Tsurusaki, 2003

Tsurusaki, 2003

Freudenthaler, 1994a

Komposch, 1996

Tsurusaki, 2003

Tsurusaki, 2003

Pearson & White, 1964

Meijer, 1972, 1984

Goodier, 1970

Komposch, 1997a

Freudenthaler, 1994a

Curtis, 1978a

Source

X

x

x

xX

X

P. opilio

P. opilio

X

Phalangium opilio X

x

X

x

X

P. agrestis

P. meadii

X

P. agrestis

X

X

X

X

Paroligolophus agrestis

— X

—

Paraumbogrella pumilio

—

X

x

x

X

X

X

P. quadripunctatum

P. quadripunctatum

X

—

P. quadripunctatum

—

X

X

X

X

X

xX

x

x

X

xX

X

X

X

xX

X

x

X

xX

X

X

X

xX

xX

xX

X

xX

X

X

X

X

xX

X

X

X

X

X

xX

X

X

X

—

—

X

X

Paranemastoma bicuspidatum

—

x

X

—

—

X

O. saxatilis

O. ravennae

O. ravennae

—

x

X

X

X

X

X

X

X

X

X

X

Opilio dinaricus

—

—

X

O. tridens

—

X

X

X

—

X

x

O. tridens

O. tridens

O. tridens

O. tridens

X

X

X

X

—

X

X

—

X

X

—

X

X

—

X

X

X

X

X

X

—

—

—

—

—

Austria

Spain

Spain

Scotland

Wales

England

Scotland

Japan

Austria

Austria

Austria

Austria

Scotland

Austria

Germany

Austria

England

Wales

Austria

Austria

Germany

open

woodland

grassland

woodland

montane

grass/wood

woodland

woodland

montane

woodland

rocky

montane

woodland

woodland

woodland

montane

grass/wood

montane

montane

woodland

grassland

(Continued)

Komposch, 1996

Rambla, 1985

Rambla, 1985

Curtis, 1978a

Pearson & White, 1964

Phillipson, 1959

Curtis, 1978a

Tsurusaki, 2003

Komposch, 1997a

Freudenthaler, 1994a,b

Freudenthaler, 1999

Komposch, 1997a

Curtis, 1978a

Bliss, 1982

Bachmann & Schaeffer, 1983b

Komposch, 1997a

Phillipson, 1959

Pearson & White, 1964

Komposch, 1997a

Bliss, 1982; Freudenthaler, 1994a,b

Bachmann & Schaefer, 1983b

— x

X

Platybunus bucephalus

P. bucephalus

Pokhara occidentalis

X

X

x

APR

—

R. triangularis

R. triangularis

x —

R. triangularis

R. triangularis

R. triangularis

—

R. triangularis

R. triangularis

x

R. triangularis

—

x

—

—

x

X —

—

Rilaena triangularis

—

x

—

—

x

—

x

x

—

x

X

x

X

xX

X

x

MAY

xX

xX

xX

x

JUN

X

xX

X

X

x

X

X

X

X

x

—

—

MAR

x

X

x

—

—

FEB

Psathyropus tenuipes

Protolophus singularis

—

JAN

P. opilio

P. opilio

Taxa

Table 7.1 Continued

X

X

xX

X

X

X

X

xX

xX

xX

X

xX

X

JUL

X

x

X

xX

xX

x

xX

xX

X

X

x

X

X

x

x

x

X

AUG SEP

x

x

X

xX

x

OCT

—

x

—

x

—

X

X

x

—

—

NOV

—

x

—

—

x

—

X

x

—

—

DEC

Wales

Norway

England

Austria

Austria

Austria

Germany

Germany

Scotland

Japan

New Mexico

Himalayas

Germany

Austria

Austria

Austria

Locality

montane

woodland

grass/wood

montane

woodland

woodland

grassland

woodland

woodland

woodland

montane

montane

woodland

montane

montane

woodland

Environment

Pearson & White, 1964

Solem & Hauge, 1973

Phillipson, 1959

Komposch, 1997a

Freudenthaler, 1994a

Bliss, 1982; Freudenthaler, 1994a

Bachmann & Schaefer, 1983b; Schaefer, 1986

Bliss et al., 1981

Curtis, 1978a

Tsurusaki, 2003

Cokendolpher et al., 1993

Martens, 1993a

Bachmann & Schaefer, 1983b; Schaefer, 1986

Komposch, 1997a

Komposch, 1997a

Freudenthaler, 1994b

Source

X X X X

Nemastoma bimaculatum

N. bimaculatum

N. bimaculatum

N. bimaculatum

N. lugubre

—

I. kollari

I. hellwigii

Ischyropsalis hellwigii

X

X

X

X

—

X

X

X

X

—

X

—

—

Dicranopalpus gasteinensis

—

xX

Dicranolasma scabrum

X

xX

X

X

X

X

xX

X

X

X

xX

X

X

A. cambridgei

xX

X

X

A. cambridgei

X

X

xX

—

Anelasmocephalus cambridgei

DYSPNOI

xX

X

xX

xX

—

Zaleptiolus implicatus

— x

X

x

Xerogrella dolpensis

T. marmoratus

Trachyrhinus marmoratus

Sclerobunus robustus

X

xX

X

X

X

xX

X

xX

xX

X

X

xX

X

X

X

X

xX

xX

xX

xX

X

X

X

X

X

X

X

X

xX

X

xX

X

x

X

X

X

X

X

X

X

X X

X

X

X

—

—

xX

xX

X

X

X

X

—

xX

X

xX

xX

— X

X

X

xX

xX

X

X

X

x

xX

X

X

X

X

X

X

Austria

Wales

England

Wales

Scotland

Austria

Austria

Austria

Austria

Austria

Germany

Germany

Spain

Himalayas

Himalayas

Texas

New Mexico

New Mexico

rocky

montane

grass/wood

montane

woodland

montane

woodland

rocky

montane

woodland

woodland

grassland

woodland

montane

montane

desert

montane

montane

(Continued)

Freudenthaler, 1999

Pearson & White, 1964

Phillipson, 1959

Goodier, 1970

Curtis, 1978a

Komposch, 1996

Freudenthaler, 1994b

Freudenthaler, 1999

Komposch, 1997a

Gruber, 1993

Bachmann & Schaefer, 1983b

Bachmann & Schaefer, 1983b

Rambla, 1985

Martens, 1993a

Martens, 1993a

MacKay et al., 1992

Cokendolpher et al., 1993

Cokendolpher et al., 1993

T. nepaeformis

T. nepaeformis

T. nepaeformis

—

x

—

S. makinoi

Trogulus nepaeformis

x x

Sabacon imamurai

—

—

N. triste

—

—

—

N. triste —

X

N. triste —

X

X

N. quadripunctatum X

xX

N. lugubre

APR

X

MAR

N. lugubre

FEB x

JAN

N. lugubre

Taxa

Table 7.1 Continued

X

X

x

x

X

X

xX

X

x

MAY

X

X

xX

x

X

X

X

xX

X

JUN

X

X

X

xX

x

X

X

X

xX

X

X

JUL

X

X

X

xX

x

X

X

X

X

X

X

X

xX

xX

X

X

X

X

X

X

X

AUG SEP

X

X

xX

X

—

X

X

X

X

X

OCT

—

X

xX

X

—

X

X

X

X

X

NOV

—

—

—

X

X

DEC

Germany

Germany

Austria

Austria

Japan

Japan

Austria

Austria

Austria

Czech Rep.

Netherlands

Austria

Germany

Locality

woodland

grassland

montane

rocky

woodland

woodland

montane

woodland

rocky

woodland

grassland

woodland

grassland

Environment

Bachmann & Schaefer, 1983b

Bachmann & Schaefer, 1983b

Komposch, 1997a

Freudenthaler, 1999

Tsurusaki, 2003

Tsurusaki, 2003

Komposch, 1997a

Freudenthaler, 1994a, b

Freudenthaler, 1999

Borek, 1958

Meijer, 1972, 1984

Bliss, 1982; Freudenthaler, 1994b

Bachmann & Schaefer, 1983b

Source

xX xX X xX xX xX X X

Acutisoma longipes

Auranus parvus

Discocyrtus sp. 1

Eucynortula lata

Goniosoma spelaeum

Mischonyx cuspidatus

Pachyloidellus goliath

Tricommatinae

X

X

xX

xX

xX

X

xX

xX

X

X

X

xX

xX

x

X

x

xX

X

X

xX

xX

xX

xX

X

xX

xX

X

X

xX

xX

xX

xX

X

xX

xX

X

X

xX

xX

xX

—

X

—

xX

X

X

X

X

X

x

xX

xX

—

X

—

xX

X

X

X

X

xX

xX

xX

—

X

—

xX

X

X

X

xX

xX

xX

—

X

—

xX

X

X

X

X

xX

xX

xX

xX

X

xX

xX

X

X

X

X

X

xX

xX

xX

xX

X

xX

xX

X

—

—

X

X

X

xX

xX

xX

xX

X

xX

xX

X

—

—

—

Brazil

Argentina

Brazil

Brazil

Brazil

Brazil

Brazil

Brazil

Uruguay

Germany

Austria

Austria

Austria

woodland

rocky

woodland

cave

woodland

woodland

woodland

cave

grassland

woodland

montane

woodland

rocky

Mestre & Pinto-daRocha, 2004

Acosta et al., 1995

Mestre & Pintoda-Rocha, 2004

Gnaspini, 1995, 1996

Friebe & Adis, 1983

Mestre & Pintoda-Rocha, 2004

Friebe & Adis, 1983

Machado & Oliveira, 1998

Capocasale & Bruno-Trezza, 1964

Bliss et al., 1981

Komposch, 1997a

Bliss, 1982

Freudenthaler, 1999

Recorded activity in each month is indicated in uppercase for adults and lowercase for nymphs. High levels of activity are marked with boldface, and strong peaks are underlined. The symbol “—” indicates no observations. Not all authors recorded nymphs.

X

Acanthopachylus aculeatus

LANIATORES

—

X

—

T. tricarinatus

—

—

T. tricarinatus

—

X

—

—

T. tricarinatus

—

X

T. tricarinatus

296

Ecology

By considering in how many months adults were recorded, a full range of seasonalities is apparent, from extremely stenochrone (in only 1 month) to completely eurychrone (in all 12 months). Very few species could be regarded as nonseasonal (eurychrone): one Cyphophthalmi, six Eupnoi, one Dyspnoi, and seven Laniatores (Table 7.1). However, it is important to stress that the number of eurychrone species presented in Table 7.1 is clearly underestimated, since the great majority of the Neotropical Laniatores (Mestre & Pinto-da-Rocha, 2004; G. Machado, pers. obs.), as well as most Cyphophthalmi (G. Giribet, pers. comm.) are present throughout the year, but there are few studies on the phenology of these groups. It has long been recognized that different harvestman species have different types of life cycles. Todd (1949), for instance, recognized three main life-history patterns for British harvestmen: (a) species active all year with overlapping generations and varying periods of adult presence, (b) annual species that overwinter as nymphs from eggs that hatch in the autumn, or (c) annual species that hatch in spring and die before winter, through which they survive as eggs. The duration of development can be annual, biennial, or perennial (Martens, 1978b), and the period of mating (generally equivalent to the recording of active adults in collections) can be eurychrone or stenochrone. If it is stenochrone, peak activity may be in the spring, or in summer to autumn, or in the winter. In a more recent study Tsurusaki (2003) provided another classification of harvestman life cycles based on the hibernating stage of 30 species from Japan. According to him, there are species that hibernate as (a) eggs (22 species), (b) juveniles (3 species), (c) adults (3 species), and (d) eggs and juveniles (2 species). The study also stressed the relationship between life cycles and phylogeny, showing that, with few exceptions, the stage of hibernation is rather uniform within a family or genus. There are also variations in life cycles among harvestmen living in tropical and near-subtropical parts of the world. In Sierra Leone all instars of the Cyphophthalmi Parogovia pabsgarnoni (Neogoveidae) occur throughout the year, but show three peaks: one in January (early dry season), one in April–June (early wet season), and one in September–October (late wet season). Legg and Pabs-Garnon (1989) related these peaks to changes in soil and litter decomposition associated with the activities of decomposer organisms. In the wet central Amazonian forest of Brazil, two species of Laniatores, Auranus parvus (Stygnidae) and Eucynortula lata (Cosmetidae), have life cycles adjusted to the annual flooding regime (Friebe & Adis, 1983). Reproduction and early development occur while the forest is flooded (probably on tree trunks), and when the water recedes, development to adulthood proceeds on the forest floor before the harvestmen retreat once more up into the trees. Acosta et al. (1995) provide an additional example with the gonyleptid Pachyloidellus goliath, which occurs in the Pampa de Achala (ca. 2,000 m altitude) in Argentina. At this altitude there are marked seasonal variations, especially in temperature, with a frosty period from March to November; hence the activity of P. goliath is restricted to the warmer part of the year (October–April). The net effect of the different ways in which species are influenced by environ-

Ecology

mental conditions is that their activities are spread over different times of the year. With regard to adult activity, nine out of ten species studied by Phillipson (1959) were stenochrone, overwintering as eggs. The only eurychrone species, with adults being present all through the year, was Nemastoma bimaculatum (Nemastomatidae), which contrasts with Curtis’s (1978a,b) account of N. bimaculatum in western Scotland, where the species was more stenochrone. It is interesting to note that in the Durham populations this species overwinters as both eggs and adults; overwintering eggs are laid from August to early December and hatch from April onward, but overwintering adult females have developing eggs that are laid from May to July before these adults die by August. Phenological patterns may also present marked variation along an altitudinal gradient, as was demonstrated by Martens (1984, 1993a) for some sclerosomatid harvestmen in the Himalayas. Figure 7.3 shows annual life-history diagrams for five species for which there are clear differences in their phenology. At the lowest altitudes Gagrella varians adults are active all through the year and have overlapping generations. Eggs are produced in March and April, and then nymphs can be found from May to September. At a slightly higher altitude a similar pattern emerges, but, as shown by Harmanda instructa, generations overlap in March instead of September, and nymphs persist alongside the adults for most of the year. Then, as we go higher into more extreme conditions, the overlap of generations disappears, and the period of adult activity shortens. In addition, during the harsher parts of the year populations persist as nymphs (Harmanda nigrolineata), nymphs overlapping with adults (Himalphalangium nepalense), or eggs (Himalphalangium dolpoense). It is clear, therefore, that the phenology of a species may vary across its geographic range and also among the habitats it exploits. In order to investigate this subject in more detail, let us come back to Table 7.1 and examine the 26 stenochrone species that occur in at least two different habitats and show variations in their life cycles. Their habitats were classified using four broad categories: (a) open habitats, including grasslands and moors/heaths; (b) woodland habitats, which include deciduous, coniferous, and mixed forests, including scrub; (c) rocky areas and deserts; and (d) montane habitats. Then, to test for any effects of the habitat on the duration of adult phase, for each species the number of months as an adult was compared through a paired t-test between populations in each type of habitat (which controls for any phylogenetic effects). The main result was that woodland populations spend more time as adults than populations of the same species living in grasslands or montane habitats (p < 0.05). We found no difference between woodland and rocky/desert populations, but since only eight species had populations in both of these habitat categories, this could be the result of small sample size. Clearly, in open habitats and at high altitudes there is marked seasonal variation in environmental factors, mainly temperature and humidity; consequently, in those habitats the period of adult activity is significantly shortened, and populations persist as eggs or nymphs most of the year.

297

298

Ecology

Figure 7.3. Phenology of some Himalayan harvestmen. Note the shift from eurychrone adults at lower altitudes—even with overlapping generations (black) and rapid development from eggs—up to the stenochronicity of the highaltitude species, which spend much of the year as resting eggs. The period spent as juveniles also varies between the species. Based on Martens (1984).

HARVESTMAN COMMUNITIES Species richness and relative abundance Ecological communities can be described and compared using simple parameters, such as species composition, species richness, and relative abundance of their representatives. In this section we used data from 88 sites in continental Europe and Britain in order to make some tentative comparisons between harvestman communities using such parameters (see references in Figure 7.4). These data are derived

Ecology

299

A

B

Figure 7.4. (A) Relationship between local richness of harvestmen and dominance (expressed here as the percentage of the most common species in the community) in 54 European communities. (B) Box-plot (median, quartiles, and maximum-minimum values) of the dominance (expressed here as the proportion of the most common species in the community) in forested habitats (n = 31 sites) and open habitats (n = 23 sites), considering only the European communities (MannWhitney, Z(U) = 2.292; p = 0.0219). Sources: References are the same as in Figure 7.1, excluding Pearson and White (1964); Curtis (1973); Davis and Jones (1978); Bliss et al. (1981); Adams (1984); Schaefer (1986); Decleer and Segers (1989); Komposch and Gruber (1999); Zingerle (1999); Dennis et al. (2001).

solely from studies that investigated communities and thus exclude single-species accounts or faunistic lists. The sample comprises a relatively small number of species (53) belonging to the suborders Dyspnoi (19) and Eupnoi (34). In spite of the heterogeneity in sample quality, the data set provides us with an opportunity to find general patterns without the complication of intercontinental variation in species composition. The harvestman richness in the European communities analyzed here ranged from 2 to 19 species. As previously recorded for scorpion communities (Polis, 1990), there is an inherent and artificial bias for species-poor communities to be characterized by one dominant species and for species-rich communities to show more evenness (Figure 7.4A). Dominance tended to be higher in communities of open habitats compared with communities of forested habitats (Figure 7.4B). This pattern is prob-

300

Ecology

ably related to two factors: (a) communities of open habitats have fewer species than communities of forested habitats, and (b) communities of open habitats may be composed of one or a few very resistant species that have physiological adaptations to tolerate the stressful conditions of these habitats and numerically dominate the community. More than 60% of the open-habitat communities were dominated by one of the following species (all belonging to the family Phalangiidae): Phalangium opilio (17.1%), Oligolophus tridens (17.1%), Odiellus troguloides (8.6%), Mitopus morio (8.6%), and Rilaena triangularis (8.6%). For at least one of these dominant species, P. opilio, there is a detailed physiological study showing that the individuals are quite resistant to water loss (Clingenpeel & Edgar, 1966), which may explain why this species inhabits and establishes dense populations in open habitats throughout the world. There has been no previous effort by opilionologists to determine which factors are associated with numerical dominance, but some trends seem to emerge from the dataset on European communities. First, large size is not a requisite for dominance, as has been previously reported for scorpions inhabiting sand habitats (Polis, 1990). Large species, such as Odiellus spinosus and Egaenus convexus, are generally rare, whereas some small species, such as Nemastoma lugubre and O. tridens, may be common. Second, specialist feeders, including trogulids and some representatives of the genus Ischyropsalis, which feed exclusively on snails (see Chapter 8), are rarely among the dominant species. Third, dominance seems to be habitat dependent, since the majority of the species (13 out of 20) dominate either in open or forested habitats, but not both. The seven species that dominate in both habitats—Lophopilio palpinalis, M. morio, Nemastoma bimaculatum, N. lugubre, O. tridens, Paranemastoma quadripunctatum, and R. triangularis—also dominate 75% of all sampled communities. Their most readily apparent common characters are that they have wide geographic distributions and simply occur in a great variety of habitats, from woodlands to cultivated fields, suggesting that these features may also influence numerical dominance. Moreover, dominant species seem to be highly fecund (see Table 12.2), but this trend is not very clear and deserves further attention. The studies on European communities also provide interesting information on the spatial and temporal variation in the relative abundance of individual species. Two extreme cases of spatial variation are O. tridens, which ranged from 0.2% in a wood from Austria (Gruber, 1993) to more than 96.4% in a wood from Germany (Bliss, 1982), and M. morio, which ranged from 0.1% in a garden from England (Owen, 1991) to 82.3% in a Scots pine forest from Scotland (Docherty & Leather, 1997). Why the relative abundance of these species varies so much along their distribution range is an important question to understand the structure of the communities. The answer is probably related to local ecological conditions, including abiotic factors such as temperature and humidity, as well as availability of resources such as prey and oviposition sites. Nearly nothing is known about the role of intra- and interspecific competition on the composition and relative abundance of species in harvestman communities (discussed later). However, 8 of the 10 most common harvestman species in our dataset show a negative correlation between their relative

Ecology

301

Figure 7.5. Long-term changes in the relative abundance of 10 harvestman species in an English garden. Only 3 species (Odiellus spinosus, Opilio saxatilis, and Leiobunum blackwalli) that were present throughout the 10-year period are shown (after Owen, 1991). The remaining 7 species (Oligolophus tridens, Paroligolophus agrestis, Mitopus morio, Phalangium opilio, Opilio parietinus, Leiobunum rotundum, and Nelima gothica) were recorded sparsely during the study and are presented as “Other.”

abundances and the species richness of the communities in which they are found. This result suggests that in communities where the resources are somehow limited, the addition of species promotes interspecific competition, which affects the relative abundance of their representatives, including the numerically dominant species. Regarding temporal variation, one study reports abundance data from exactly the same traps over a full decade. Owen (1991) concisely listed long-term changes in an English garden where there were marked changes in species composition and their relative abundance from year to year. Only three species were present throughout the 10-year period: Odiellus spinosus, Opilio saxatilis, and Leiobunum blackwalli (Figure 7.5). The remaining seven species (Oligolophus tridens, Paroligolophus agrestis, M. morio, P. opilio, Opilio parietinus, L. rotundum, and Nelima gothica) were recorded sparsely during the study, always with low relative abundances. Moreover, the relative abundance of the three most common species presented great variation throughout the study. Odiellus spinosus, for instance, was always the dominant species, but its relative abundance ranged from 47.7% to 89.5%, nearly a twofold difference. The relative abundance of L. blackwalli also presented an enormous variation, ranging from 1.4% to 11.1%. Owen (1991) does not provide an explanation for such annual variation, but the results of this study indicate that both species composition and relative abundance may vary considerably over time. The temporal variation of species abundances certainly deserves more attention because it may help us understand how different species respond to environmental disturbance.

Trophic relationships and resource partition The importance of predators in energy and nutrient cycling is a function of the quantity of prey biomass they capture, which in turn is a function of the predators’

302

Ecology

density, biomass, metabolism, and energy transfer efficiency (Polis, 1993). There is little information on these points for harvestmen, and the data presented here come from the most comprehensive study on the role of Opiliones as predators (Schaefer, 1986). The study was conducted in a beech woody ecosystem in Germany, where Lophopilio palpinalis, Lacinius ephippiatus, Mitopus morio, and Platybunus bucephalus were the dominant species. Soil and litter samples showed that the total harvestmen fauna (nine species) had a mean annual density of 19 individuals/m2 and a mean biomass (as dry weight) of 11 mg/m2. These values were very low compared with other predatory macroarthropods in the leaf litter, such as spiders (135 mg/m2), staphylinid beetles (76 mg/m2), and centipedes (366 mg/m2). Estimates suggest an annual consumption rate by the total harvestman fauna ranging from 0.2 to 1.0 kcal/m2/year. These values represent only a small fraction of the annual production of the leaf-litter arthropod community and only a small portion of the total pressure exerted by predatory arthropods, including spiders, staphylinids, and centipedes (Schaefer, 1986). Comparable results were found in another type of habitat, a deciduous woodland forest in England (Todd, 1949). The number of harvestman species was 17, the density in the ground layer ranged throughout the year from 0 to 50 ind./m2, and the biomass ranged from 0 to 200 mg/m2. Despite the lack of information on the role of harvestmen as predators in Todd’s article, it is possible to estimate the annual amount of prey captured using monthly harvestman densities (see Table 6 in Todd, 1949) and adult daily food consumption (nearly 0.001 g; see Phillipson, 1960a,b, 1963). The conclusion is that all harvestmen living on one hectare of land would have a combined consumption of 65 kg of prey per year. By comparison, a similar estimate was made by Foelix (1996) for spiders, and the result was 47,500 kg of prey in one hectare per year. However, it is important to stress that Foelix’s number is clearly overestimated, since it does not consider seasonal variation in density (of 130 ind./m2, no less), and it assumes a daily rate of prey consumption of 0.1 g/day—100 times more than that estimated for an adult harvestman. Obviously, we need rigorous estimates of the impact of arachnids as predators based on empirical field data, since at present, and except for a study of desert scorpions (Polis, 1993), the available information is based only on hypothetical calculations. Whenever we study species assemblages, we may consider distributions and coexistence mechanisms in at least three ways: (a) temporal activity (phenology) segregation, (b) small-scale spatial segregation, and (c) resource partition. Nonoverlapping phenological patterns may be one of the most important coexistence mechanisms, and temporal succession of harvestman species (such as that shown in Figure 7.6 for Scottish woodland species) is frequently seen. Harvestmen also share their habitats with other cursorial hunters, and these seasonal patterns may extend to other arthropod groups. Indeed, in Scotland, wolf spiders (Lycosidae) tend to have their peak activity in spring or early summer, to be replaced in later months by harvestmen (Stinglhammer, 1987). This can even be extended to include nonarachnid taxa, such as beetles. Löser (1980), for instance, showed temporal separation between nocturnal Carabidae and Opiliones, in which maximal activity occurs before and after midnight, respectively.

Ecology

303

Figure 7.6. Seasonal succession of Scottish harvestmen, shown as the percentage of the annual total derived from two years’ pitfall sampling; all species to the same scale. The total counts for each species are Mitopus morio = 246, Lacinius ephippiatus = 298, Nemastoma bimaculatum = 11,241, Oligolophus hanseni = 160, Paroligolophus agrestis = 443, Oligolophus tridens = 1,123, and Lophopilio palpinalis = 1,339. A sequence of seven species shows successively later peaks in adult activity through the late summer into early winter. Mitopus morio shows a fairly widespread activity period with three peaks, and both O. hanseni and O. agrestis are bimodal. The remaining species show single, sharp peaks in abundance. This temporal sequencing may contribute to the coexistence of these species in their woodland habitat.

Coexistence mechanisms may also operate on a spatial basis, so that species are segregated by different habitat preferences. Adams (1984, 1985), for instance, found highly overlapping diets and no evidence for resource competition in his study of harvestman communities in deciduous woods in England, the main species of which were Anelasmocephalus cambridgei, Nemastoma bimaculatum, Lophopilio palpinalis, Lacinius ephippiatus, M. morio, Leiobunum blackwalli, and L. rotundum. He concluded that habitat structure and density were the critical factors influencing the structure of the harvestman communities. This conclusion, of course, cannot be generalized for other sites throughout the world, and the mechanisms of coexistence of species in harvestman communities remain an open field for future research.

HARVESTMAN CONSERVATION Human impact on harvestmen Harvestman distributions may be influenced by both biotic and abiotic factors, including climatic conditions and habitat structure. Therefore, any human activity that promotes changes in natural habitats may negatively affect some species of the

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group. Human impacts may be very subtle, and even the action of walking over ground vegetation can affect spider and harvestman communities (Curtis et al., 1990). Other human activities, however, have tremendous impact on the habitats on which harvestmen are dependent. Agricultural and infrastructure development projects, for instance, can result in habitat fragmentation, which can endanger harvestmen directly or indirectly. In this section we list some study cases that illustrate how human activities can negatively or positively affect harvestman populations. Many reports concern the impact of fertilizers and pesticides on harvestman populations. In the Czech Republic numbers of the harvestman Phalangium opilio dropped slightly with the use of urea + ammonium nitrate fertilizer for winter wheat crops (which was also associated with a dramatic decrease in invertebrates overall), and they dropped significantly with the application of deltamethrin pesticide on spring barley fields (Pekár, 1997a,b). Additionally, spider and harvestman quantities were also found to be slightly affected by combined fertilizer/insecticide applications on winter wheat (Pekár et al., 1997). The effects of insecticides on harvestmen living in apple orchards were studied in the northwestern USA (Epstein et al., 2000), and the authors found significant decreases in populations of many arthropod groups, including, although usually to a lesser extent, harvestmen. It has been suggested that the long-legged harvestmen stand high enough not to touch the pesticidecovered ground, thus reducing the impact of contact pesticides (Haws, 1995). If this is true, short-legged species should be more severely affected than the long-legged species, but this prediction has not been experimentally tested. Forestry operations obviously can alter the habitat conditions available to harvestmen. In the USA Jennings et al. (1984) found significantly more individuals and species (mainly Leiobunum calcar) in uncut strips and dense spruce-fir woods than in clear-cut strips. Species diversity of spider and harvestman communities in peat bogs varies significantly with heterogeneity in vegetation structure (Curtis & Bignal, 1980), which in turn can be strongly influenced by management practices such as drainage and peat cutting. With drainage or simply the passage of time, peat-bog vegetation may be replaced by woodland (many peat bogs are also planted with coniferous tree species), and consequently the opiliofauna changes. Sometimes the actual species of trees that are planted can have an impact on harvestman populations: rougher bark on tree trunks provides more refuges for harvestmen and their prey and can influence the diversity of spider and harvestman communities (Curtis & Morton, 1974). Less obvious, perhaps, are pollutant effects on forest habitat. Bliss and Tietze (1984) described changes in species composition in harvestman communities in German woodlands affected by air pollution. The authors suggested that these changes could be caused by alterations in microclimate conditions, which in turn were associated with changes in the vegetation. Another study on how pollutants affect harvestmen has been done in an abandoned lead- and zinc-smelting complex in Arnoldstein, Austria, which was in operation for almost five centuries. Rabitsch (1995) analyzed metal accumulation in several arthropod groups, including harvestmen and spiders, and showed that lead, the main pollutant of the region, be-

Ecology

came heavily accumulated in all arachnid species, especially in those sites near the smelting complex. Additionally, sex-specific accumulation occurred mainly in harvestmen, with males usually having to manage higher quantities of this type of stress. Finally, no indication of changes in life cycle parameters was found, but a negative correlation between metal accumulation and body weight was found. It seems obvious, therefore, that soil and vegetation contaminated with metals may negatively affect predatory groups, such as spiders and harvestmen, which accumulate great quantities of pollutants from the lower levels of the trophic chain. Fire also has drastic effects on harvestman populations (e.g., Curry et al., 1985, in Australia; Loch, 1999, in Germany). The most comprehensive study of the effects of fire on arachnids was conducted by Schaefer (1980a,b), who recorded the recolonization of a burned pine forest by several arthropod groups in northern Germany. Regarding the arachnids, only a few harvestmen and spiders survived the fire, but the burned area was rapidly recolonized by individuals originating from surrounding areas, such as woodlands and open habitats. After about two years the burned pine forest was characterized by a number of species and a population density that did not differ from the values in unburned pine forests in the vicinity. However, species composition was markedly different because the immigrating individuals belonged to two different ecological groups: (a) species typically found in the pine forests, such as the harvestman Paroligolophus agrestis (Phalangiidae), and (b) species from open habitats that established dense populations after the fire, such as the spider Pardosa lugubris (Lycosidae). Thus the arachnids in the burned area formed a typical community quite different from the one that inhabited the original pine forest. Harvestmen may also be negatively affected by domestic animals. Free-range domestic birds, such as chickens and geese, resulted in some reduction in harvestman activity in an experimental apple orchard in Michigan, USA (Clark & Gage, 1997), which might be explained as a result of direct predation by chickens and/or habitat disturbance by both bird species. In another study the number of catches of arachnids was compared in three tussocky grassland areas in upland Scotland: with no livestock, with sheep only, and with sheep and cattle (Dennis et al., 2001). For most species of spiders, harvestmen, and pseudoscorpions, the abundance was greater in the ungrazed area. However, for the harvestman Mitopus morio, the most common arachnid species, significantly more individuals were found in the shorter swards of the area managed with sheep only. According to the authors, this pattern of captures may have been an artifact of its behavior of walking over the grass canopy and thus above the pitfall traps used for sampling in the area with no livestock and taller vegetation. But not all human impacts are detrimental to harvestmen. An extreme example of a benign effect is the construction of artificial islands and their subsequent colonization by arachnids, as described by Komposch (1996). Within about three years, five species of Opiliones (Phalangium opilio, Oligolophus tridens, Lacinius ephippiatus, Astrobunus laevipes, and Nelima semproni), as well as 58 spider species, had established populations in these artificial islands. There are several synanthropic species, and the construction of human settlements and buildings can provide homes for populations and communities of harvestmen. For example, Novak et al. (2002) report that of the

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65 Slovenian species, 42 are found in urban centers, particular examples being Phylangium opilio, Nelima semproni, Opilio saxatilis, Leiobunum rotundum, Trogulus nepaeformis, Opilio parietinus, and Nemastoma bidentatum sparsum. The richness of the Slovenian urban opiliofauna may be due to some extent to the relatively small size of these towns and the proximity of primary habitats. Certain species of Cyphophthalmi can thrive in disturbed environments. In Bioko, Equatorial Guinea, the neogoveid Paragovia sironoides could be found in large densities in a cocoa plantation. Other species are abundant in semimanaged botanical gardens in South Africa, Singapore, and Sri Lanka (G. Giribet, pers. comm.). Some synanthropic species may increase their ranges largely in response to human activities, mainly urbanization and agriculture. Phalangium opilio and Opilio parietinus are phalangiids characteristic of disturbed habitats and widely distributed throughout the Holarctic region; today, because of human introduction, they are also common in New Zealand (Hillyard & Sankey, 1989). Other well-reported cases are Opilio canestrinii and O. ruzickai (Phalangiidae), two synanthropic species that are expanding their ranges in Austria (Komposch, 1993), and Leiobunum limbatum, a species that lives on houses and other man-made structures and is expanding its range in Germany (Bliss, 1990). Neotropical examples include the gonyleptids Discocyrtus invalidus, D. oliverioi, and Mischonyx cuspidatus, which are found in both natural and urban environments (Elpino-Campos et al., 2001; Mestre & Pinto-daRocha, 2004; Pereira et al., 2004). These three species have wide geographic distributions in Brazil, contrasting with other closely related species, which are generally confined to some mountains or natural forest patches.

Endangered species As we have shown, many species of Opiliones seem to be currently threatened by human activities that promote habitat degradation, destruction, and fragmentation. Harvestman species that have very restricted distributions can be particularly endangered if human activities unfavorably alter their habitats. This is the case for most troglobitic harvestmen, which may be driven to local or complete extinction if the cavernicolous habitat is disturbed by pollution, development of nearby land, or even noncontrolled visitation to the caves. All troglobitic taxa are considered to be threatened in Brazil, but the only troglobitic harvestmen on the “Red List of Threatened Species” are the gonyleptids Iandumoema uai, Pachylospeleus strinatii, and Giupponia chagasi and the minuid Spaeleoleptes spaeleusa. Another example is the phalangodid Maiorerus randoi in the Canary Islands, which has been found in only one cave and is included in the “National Catalogue of Threatened Species” of the Spanish government (Oromí & Izquierdo, 1994). Similarly, the troglobitic phalangodids Texella cokendolpheri, T. reddelli, and T. reyesi, which are restricted to certain caves in Texas, are listed as endangered species in the USA. In some areas these Texella species are threatened by degradation of their habitats, and in others by the invasion of the fire ant Solenopsis invicta into the caves (Reddell & Cokendolpher, 2001). Opiliones found in very restricted habitats around desert springs or mountain-

Ecology

tops may also be endangered if the habitat is being changed by human activities. This is the case for the phalangodids Calicina minor and several species of the genus Microcina, generally found under serpentine rocks, particularly in association with serpentine grassland or woodland vegetation in central California, USA. All these species are being considered for listing as endangered species but have yet received no governmental protection (J. C. Cokendolpher, pers. comm.). Other examples of vulnerable species include two Argentine gonyleptids: Pachyloidellus fulvigranulatus, which is found only on the top of the highest peak of the Sierras Chicas chain in the province of Córdoba, and Pachyloidellus borellii, which occurs as morphologically distinct populations in rapidly disappearing rain-forest patches in the provinces of Salta and Jujuy. Indeed, given the high rate at which humans are destroying these rainforest patches, it is possible that some geographic variants of P. borellii will disappear in the near future (L. E. Acosta, pers. comm.). Up to now, however, no harvestman species has been recognized as endangered in Argentina, and therefore, P. fulvigranulatus and P. borellii receive no governmental protection. Opiliones, like other secretive animals, can be in danger of extinction without anyone ever noticing. Our knowledge of African harvestmen is close to zero (see Chapter 1), and the same is true for harvestmen of tropical Asia and most of the Amazonia. The process of habitat destruction in these regions has increased significantly in recent decades, and we are certainly losing many species of plants and animals (Sayer & Whitmore, 1991), in some cases even before their formal descriptions by taxonomists. This may be particularly frequent among invertebrates, especially those groups that have historically attracted the attention of few researchers, such as harvestmen. Only recently have certain species—almost exclusively the cave dwellers—been receiving some attention of researchers and conservationists and thus have some kind of governmental protection. Given the paucity of ecological information for the great majority of harvestman species, it is almost impossible to provide any comment about their conservation status. Therefore, preservation of habitats, instead of particular species, may be the more effective means of protection of the diversity of Opiliones around the world.

CONCLUDING REMARKS In the course of this chapter we looked at spatial and temporal patterns in the occurrences of harvestman species in both large and small scales. Thereafter, we discussed how the activities of some species are distributed over the seasons and touched on how this may be influenced by various environmental factors. We also saw how communities may be described and compared in terms of such parameters as species richness and species abundance. While we recognize the markedly different species composition of geographically separated communities, we have evidence for at least two potential mechanisms that contribute to the separation and thus the coexistence of different species of harvestman and other taxa: temporal activity patterns and habitat preferences.

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It is important to emphasize, however, that there are more than 6,000 species of harvestmen worldwide, few of which have been featured in this chapter. The majority of publications record the distribution and taxonomy of single species, with no indication of the coexistence of species in delimited areas. Thus we suffer from a scarcity of information at the community level. At the population level there are no studies that provide data on survivorship, mortality, or any kind of intraspecific interactions that may influence the distribution of individuals in the space. There is much to learn about these fascinating assemblages of species, and because they, as arthropod predators, probably influence the populations of many other species, we have ample reason to expand our knowledge of harvestman ecology. An updated perspective on harvestman ecology was presented here, and we hope that it stimulates young arachnologists to develop a lifelong interest in the subject.

ACKNOWLEDGMENTS We express our thanks to all our colleagues who were kind enough to provide us with information and data. This chapter was greatly improved through comments by A. J. Santos, G. Giribet, G. Q. Romero, M. Almeida-Neto, P. R. Guimarães Jr., R. Pinto-da-Rocha, R. Macías-Ordóñez, and three anonymous reviewers. D. Curtis dedicates this chapter to the late Dr. Ron Pearson, who, as his Ph.D. supervisor years ago, inspired him to set off on this long voyage of discovery, and to his wife Angela for her constant support. G. Machado is supported by a research grant from FAPESP (02/00381-0).

CHAPTER

8

Diet and Foraging Luis E. Acosta and Glauco Machado

H

arvestmen are often defined as omnivorous, which is a quite remarkable feature among arachnids. Collectively, harvestmen are chiefly predators of small, soft-skinned arthropods and other invertebrates. Many species are also opportunistic scavengers, and some regularly ingest vegetal matter. This broad spectrum is seldom shown at species or genus level, and differential food preferences arise when a particular harvestman taxon is considered. Given the ubiquitous distribution and abundance of harvestmen, questions about the composition of their diet, as well as their means of obtaining food and manner of eating, are relevant issues to be tested and studied. The aim of this chapter is to summarize and review current knowledge of diet and foraging habits in Opiliones.

WHAT DO HARVESTMEN EAT? A historical perspective A long controversy has existed over what constitutes the actual diet of harvestmen. Some early authors, such as Menge (1850) and Henking (1888), asserted that harvestmen were unable to eat anything other than dead insects or plants. In contrast, Simon (1879a), O. Pickard-Cambridge (1890b), and Banks (1901) emphasized that harvestmen feed mostly on living insects, and Rühm (1926) reported his observation of a Phalangium eating a living wasp. Although M. E. Walker (1928) was still convinced that harvestmen fed only on fruit juices and other plant matter, authors have increasingly discredited the old beliefs by providing further credible reports of harvestmen as predators (e.g., Jeannel, 1926; Steinböck, 1931; Bishop, 1950; Pabst, 1953; Immel, 1955). While nowadays it is accepted that most harvestman species primarily capture live prey, subtle differences in perspectives persist. Juberthie (1964), Martens (1978b), 309

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and Moritz (1993) consider harvestmen as primarily predacious, while Gnaspini (1996) defined their diet as “largely omnivorous, with preference for animal matter.” It seems that attempts at generalization have been somewhat biased by the taxon most familiar to or best studied by a given investigator. Interestingly, Santos and Gnaspini (2002) pointed out that if observations in nature are considered, Goniosoma spelaeum (Gonyleptidae) is to be classified as a “generalist carnivore with a highly opportunistic diet,” while preferences shown in captivity would best label the species as “generalist omnivore, with preference to carnivory.” All evidence suggests that considerable variation exists among taxa, and hasty generalizations may be misleading. Despite these discussions, careful studies on the feeding habits of harvestmen are scarce. Records of harvestman food items are usually a combined list of field observations on prey intake and all items accepted in captivity. Prey records from nature are few, many are anecdotal, and most studies rely on small sample sizes. For most of the literature, the issue of food has typically been referred to as a part of wider studies on the biology of a given taxon. Additionally, plenty of scattered patchy references to feeding exist, although attempts to comprehensively review all these materials are rare. For cave harvestmen, a list of accompanying species is often provided as presumable prey items, but direct observations are lacking in most cases. Polyphagy, wide distributions, and relatively high abundance of harvestman populations suggest an important role of the group in ecological webs (see Chapter 7). Most contributions, especially the earlier studies, concentrate on European and North American species, chiefly referring to Eupnoi of the families Phalangiidae and Sclerosomatidae (mainly Leiobuninae), and to a lesser extent to some Dyspnoi such as Nemastomatidae and Ischyropsalididae. In recent years an increasing number of studies have focused on Neotropical gonyleptids. Despite this, our knowledge of harvestman diet and feeding habits remains very limited because it is based on relatively few representatives of approximately 10 families out of the more than 40 currently recognized in the order. Obviously, more information on several other families is needed to obtain a reasonably complete picture.

Prey selection Recorded prey items of harvestmen encompass varied insects, arachnids (including other harvestmen), myriapods, isopods, earthworms, leeches, gastropods, and even small vertebrates (Table 8.1). As stated earlier, most authors characterize harvestmen as generalist feeders, emphasizing the large number of food items they can consume. This view has led to the conclusion that harvestman feeding behavior shows little or no trace of discrimination. However, a detailed analysis of the available data strongly suggests that most harvestmen have a preferred set of prey types, including both size classes and taxonomic affiliations. Prey that represent a higher cost than benefit for harvestmen include animals that are beyond the size range of their trophic apparatus (chelicerae and in some cases also the pedipalps), chemically noxious prey, and those arthropods that have the capacity to reverse the direction of the predator-prey interaction (Figure 8.1A).

Diet and Foraging

311

Table 8.1 Reported food items for harvestmen of the four suborders Taxa

Food items

Source

CYPHOPHTHALMI Sironidae Cyphophthalmus duricorius [Eu]

Pierced dipterans (Calliphora)1 and beef1 1

Juberthie, 1964 1

Parasiro coiffaiti [Eu]

Dead podurid collembolans and ant pupae

Siro rubens [Eu]

Collembolans,1 pierced dipterans (Calliphora),1 and cow meat1

Juberthie, 1964

Keroplatid dipteran larvae (glowworms)

Pugsley, 1984; Meyer-Rochow & Liddle, 2001

Collembolans,2 homopterans,2 psocopterans,2 dipterans,2 myriapods,2 spiders (also2), harvestmen (Nemastoma lugubre), isopods,2 earthworms,2 and gastropods2

Sankey, 1949b; Todd, 1950; Sunderland & Sutton, 1980; Adams, 1984

Joseph, 1868b

EUPNOI Monoscutidae Megalopsalis tumida [NZ]

Phalangiidae, Oligolophinae Lacinius ephippiatus [Eu]

Lacinius horridus [Eu]

Homopterans (aphids)

Mitov, 1988

Mitopus glacialis [Eu]

Glacier collembolans

Steinböck, 1931

Mitopus morio [Eu]

Juveniles: collembolans and heteropteran nymphs. Adults: dipterans (tipulids and muscids; also 2), neuropteran (chrysopid larvae), homopterans (cercopids, aphids; also 2), psocopterans,2 dermapterans, ants, spiders (also 2), other harvestmen (six species), myriapods,2 isopods (also 2), earthworms (also 2), gastropods (also 2), and dead vertebrates

Kästner, 1931a; Bristowe, 1949; Sankey, 1949b; Todd, 1950; Phillipson, 1960b; Sunderland & Sutton, 1980; Adams, 1984; Cannata, 1988; Dixon & McKinlay, 1989

Odiellus spinosus [Eu]

Spiders and a mite

Sankey, 1949b

Oligolophus tridens [Eu]

Collembolans, homopterans (aphids, psyllids, delphacids, jassids), beetles (chrysomelids), lepidopteran larvae, dipterans (phorids and muscids), millipedes, spiders, harvestmen (Mitopus morio), mites, isopods, earthworms (enchytraeids), small snails, plant matter, nuttyseeds, dead vertebrates, and bird droppings

Bristowe, 1949; Sankey, 1949b; Todd, 1950

Paroligolophus agrestis [Eu]

Collembolans, homopterans (aphids), a dipteran larva (stratiomyid), a lepidopteran larva, ants, isopods (also 2), a small gastropod (snail), and bird droppings

Bristowe, 1949; Sankey, 1949b; Sunderland & Sutton, 1980; Dixon & McKinlay, 1989

Homopterans (aphids), diplopods,3 spiders, dead vertebrates, and pollen

Sankey, 1949b; Pfeifer, 1956; Dixon & McKinlay, 1989

Phalangiidae, Opilioninae Opilio parietinus [Eu]

(Continued)

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Table 8.1 Continued Taxa Opilio saxatilis [Eu]

Food items

Source

Homopterans (aphids) and dipterans

Sankey, 1949b; Dixon & McKinlay, 1989

Phalangium opilio [Eu, NA]

Collembolans, heteropterans (mirids), homopterans (aphids and psylloids), orthopterans (acridids), dead (crushed) and live beetles (curculionids, chrysomelids, and carabid larvae), lepidopteran larvae (noctuids), dipterans (calliphorids and culicids), ants, wasps (dead?), chilopods (Geophilomorpha), harvestmen (Oligolophus tridens), spiders, mites (tetranychids), isopods,2 gastropods (live Helix acuta), and dead vertebrates

Rühm, 1926; Kästner, 1925, 1931a, 1935b; Bristowe, 1949; Sankey, 1949b; Todd, 1950; Whiteley, 1961; Katayama & Post, 1974; Sunderland & Sutton, 1980; Mitov, 1988; Dixon & McKinlay, 1989; Drummond et al., 1990

Rilaena triangularis [Eu]

Dipterans, a dead wasp, and isopods2

Immel, 1955; Parisot, 1962; Sunderland & Sutton, 1980

Lophopilio palpinalis [Eu]

Collembolans, homopterans, psocopterans, dipterans, myriapods, spiders, earthworms, gastropods (all2), and juices of the mushroom Cantharellus cibarius3

Sˇilhavy´, 1942; Adams, 1984

Megabunus diadema [Eu]

Dipterans (chironomid)

Bristowe, 1949

Platybunus bucephalus [Eu]

Dipterans and lepidopteran larvae

Kästner, 1931a, 1935b

Platybunus pinetorum [Eu]

A homopteran

Cannata, 1988

Gagrellula ferruginea [As]

A fungus (Mycena sp.)

Uyemura, 1935

Melanopa sp. [As]

A slime fungus (Myxomicetes)

Huzita, 1936

Hadrobunus maculosus [NA]

Earthworms

Halaj & Cady, 2000

Leiobunum aldrichi [NA]

Small lepidopterans (moths), dead ants, spiders, bits of earthworms and gastropods (slugs), lichens,3 and algae3

Bishop, 1949b, 1950; Edgar, 1971

Leiobunum blackwalli [Eu]

Homopterans ( jassids), a small lepidopteran larva, dipterans,2 millipedes, harvestmen (Oligolophus tridens), earthworms (also2), gastropods (also 2), and bird droppings

Bristowe, 1949; Sankey, 1949b; Parisot, 1962; Adams, 1984

Leiobunum calcar [NA]

Earthworms

Halaj & Cady, 2000

Leiobunum limbatum [Eu]

Heteropterans (mirids)

Pfeifer, 1956

Leiobunum nigripes [NA]

Ephemeropterans and earthworms

Phalangiidae, Phalangiinae

Phalangiidae, Platybuninae

Sclerosomatidae, Gagrellinae

Sclerosomatidae, Leiobuninae

3

3

Halaj & Cady, 2000

Leiobunum politum [NA]

Earthworms, lichens, and algae

Edgar, 1971; Halaj & Cady, 2000

Leiobunum rotundum [Eu]

Homopterans (bythoscopids, euscelids, typhlocybids, aphids—also 2), psocopterans,2 dipterans (tipulids, cordilurids, muscids, mycetophilids, culicids; also 2), lepidopterans (eucosmids),

Kästner, 1935b; Bristowe, 1949; Sankey, 1949b; Todd, 1950; Adams, 1984; Dixon & McKinlay,1989

Diet and Foraging

Taxa

Food items

313

Source

wasps (ichneumonids), beetle larvae, spiders (also 2), harvestmen (Oligolophus tridens), myriapods,2 isopods (also 2), earthworms,2 pulmonate gastropods (also 2), and dead vertebrates Leiobunum sp. [NA]

Hickory nuts

Wickham, 1918

Leiobunum ventricosum [NA]

Adult heteropteran (cydnid)

J. C. Cokendolpher, pers. comm.

Leiobunum vittatum [NA]

Dead crushed beetles (carabids), dead flies,1 dead moths,1 earthworms, and red raspberries

Edgar, 1971; Katayama & Post, 1974; Halaj & Cady, 2000

Nelima paessleri [NA]

Dipterans (mycetophilid and tipulid), lepidopterans (moths), and isopods (all 3)

Holmberg et al., 1984

Nelima semproni [Eu]

Gastropods (slugs)

Komposch, 1992

Togwoteeus biceps [NA]

Dead crushed beetles (carabids)

Katayama & Post, 1974

Acarid mite (mentioned as Tyroglyphidae)1

Sankey, 1949b

Drosophila flies and a lepidopteran larva (geometrid)

Gruber, 1993

Ischyropsalis hellwigii hellwigii [Eu]

Gastropods and occasionally dead insects1

Verhoeff, 1900; Martens, 1965, 1978b; J. Gruber, pers. comm.

Ischyropsalis kollari [Eu]

Blattodeans,1 flying dipterans (e.g., Drosophila),1 isopods,1 and gastropods1

Janetschek, 1957; Martens, 1975c, 1978b

Ischyropsalis pyrenaea [Eu]

Cave trichopterans (also 1)

Juberthie, 1964

Histricostoma drenskii [Eu]

Collembolans and homopterans (psylloids)

Mitov, 1988

Nemastoma bimaculatum [Eu]

Collembolans, homopterans, psocopterans, dipterans, myriapods, spiders, isopods, earthworms, and gastropods (all2)

Sunderland & Sutton, 1980; Adams, 1984

Nemastoma lugubre [Eu]

Mites, “putrescent wood, which became gelatinous” [sic]

Rimsky-Korsakow, 1924; Parisot, 1962

Paranemastoma quadripunctatum [Eu]

Collembolans,1 mites,1 and earthworms (enchytraeid)1

Immel, 1954

Paranemastoma radewi [Eu]

Homopterans (aphids), coleopterans, and dipterans (adults and guanophil larvae)

Mitov, 1988

Sclerosomatidae, Sclerosomatinae Homalenotus quadridentatus [Eu] DYSPNOI Dicranolasmatidae Dicranolasma scabrum [Eu]

Ischyropsalididae

Nemastomatidae

(Continued)

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Table 8.1 Continued Taxa

Food items

Source

Trogulidae Anelasmocephalus cambridgei [Eu]

Gastropods,1 occasionally freshly dead insects,1 and live earthworms (enchytraeid)1

Pabst, 1953

Anelasmocephalus hadzii [Eu]

Gastropods,1 occasionally freshly dead spiders1

Komposch, 1992

1

Trogulus nepaeformis [Eu]

Gastropods, occasionally freshly dead insects1 and live earthworms (enchytraeid)1

Pabst, 1953

Trogulus tricarinatus [Eu]

Gastropods,1 a young diplopod,1 occasionally freshly dead insects1 and live earthworms (enchytraeid)1

Pabst, 1953; Sankey, 1949b

Fungi growing on a rotting log inside a cave

Goodnight & Goodnight, 1960

Acutisoma longipes2 [SA]

Leg fragments of an orthopteran, an adult (dead) and a larva (alive) of a lepidopteran (moth), a dipteran (tipulid), a dead ant, a dead wasp, insect remains wrapped in silk, an adult moth wrapped in silk (stolen from a spider), a dead harvestman (Holcobunus sp.), spider egg sacs (theridiosomatid), a dead earthworm, and a dead hirudinean

Sabino & Gnaspini, 1999; Machado et al., 2000; G. Machado, pers. obs.

Goniosoma spelaeum [SA]

Lepidopteran larvae and adults (noctuids), neuropterans (ascalaphids), dipterans (tipulids), and isopods

Gnaspini, 1996; Santos & Gnaspini, 2002

Fruit, insects, and metamorphic tree frogs

Gnaspini, 1996; Machado & Pizo, 2000; Castanho & Pinto-daRocha, 2005; G. Machado, pers. obs.

Homopterans, small adult beetles (scarabaeids), adult and larvae of lepidopterans, winged ants, earthworms (Microscolex dubius), and crustose lichens3

Acosta et al., 1995

Larvae of beetles,3 a dead diplopod, “dead animals” [sic], guano,3 fungi,3 and plant debris3

Pinto-da-Rocha, 1996a

LANIATORES Cladonychiidae Erebomaster flavescens [NA] Gonyleptidae, Goniosomatinae

Gonyleptidae, Gonyleptinae Neosadocus variabilis [SA]

Gonyleptidae, Pachylinae Pachyloidellus goliath [SA]

Gonyleptidae, Pachylospeleinae Pachylospeleus strinatii [SA]

Diet and Foraging

Taxa

Food items

315

Source

Phalangodidae Banksula spp. [NA]

Collembolans1

Briggs & Ubick, 1981 1

Scotolemon spp. [Eu]

Small cave beetles (silphids, also )

Jeannel, 1926; Kästner, 1935b

Texella sp. [NA]

Cave collembolans

J. C. Cokendolpher, pers. comm.

Small cave beetles (silphids, also1)

Jeannel, 1926

Keroplatid dipteran larvae (glowworms)

Pugsley, 1984; Meyer-Rochow & Liddle, 1988, 2001

Travuniidae ?Peltonychia spp. [Eu] Tryaenonichidae Hendea myersi cavernicola [NZ]

The geographic occurrence of each species is indicated in square brackets after the species name: As = Asia, Eu = Europe, NA = North America, NZ = New Zealand, SA = South America. Unless otherwise indicated, mentioned preys were recorded in the field and are deemed to have been taken alive. 1. Remarkable reports in captivity. 2. Items from antisera analyses of gut contents of individuals taken in nature. 3. Food items hypothesized but not yet proven.

Most harvestman prey recorded thus far fits within the category of small, softskinned invertebrates that can be easily seized by pedipalps and/or chelicerae. The integument of the prey needs to be thin enough to be lacerated by the chelicerae. Therefore, insects with a hard exoskeleton, such as most beetles, are generally refused even if they are dead (Edgar, 1971), unless they are crushed (Bishop, 1950; Katayama & Post, 1974). Large prey items are commonly rejected since they may offer risk of injury, and capturing them represents a waste of energy (Figure 8.1A). A similar pattern has been described in scorpions (McCormick & Polis, 1990), solifuges (Punzo, 1998), and spiders (Riechert & Luczak, 1982), in which prey selection is dependent on size and type of exoskeleton. In all these arachnid groups, including harvestmen, morphology of the trophic apparatus is a critical feature that determines whether the prey can be physically immobilized. The generalist and voracious dietary character of most harvestmen led Adams (1984) to consider food a minor critical factor in their ecology. Diet flexibility dependent on local prey abundance has been shown for a couple of polyphagous Leiobunum species (Adams, 1984). The relative availability of different prey types in the local environment is also likely to affect the composition of the diet in species that occupy different habitats. Habitat use is correlated with harvestman morphology (see Chapter 7), so that meaningful diet differences are expected to occur among small litter dwellers (such as nemastomatids), long-legged species that climb vegetation (such as many phalangiids and leiobunines), and robust harvestmen (such as many gonyleptids). Differences were proved regarding the relative importance of certain food items even for individuals of the same species living in different microhabitats. The diet of the phalangiid Mitopus morio, for instance, differs signifi-

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Figure 8.1. (A) Prey offered to adults of the harvestman Mitopus morio in a laboratory experiment (original data from Phillipson, 1960a). White bars represent prey taken and black bars represent prey rejected by the harvestmen. Body length of males ranges from 4.2 to 5.3 mm and that of females from 6.4 to 8.2 mm (Martens, 1978b). (B) Relative contribution of eight prey types in the diet of the harvestman Mitopus morio (Phalangiidae) living on the ground layer and vegetation, as revealed through antisera analyses of gut contents (original data from Adams, 1984). The frequency of the items differs significantly in the two microhabitats (g test = 31.48; d.f. = 8; p = 0.0001). ISO = Isopoda; ARA = Araneae; OLI = Oligochaeta; DIP = Diptera; GAS = Gastropoda; HYM = Hymenoptera; MYR = Myriapoda; PSO = Psocoptera.

Diet and Foraging

cantly between individuals captured on the ground and on vegetation (Adams, 1984; see also Figure 8.1B). Furthermore, diet composition may also vary throughout the life span of a single species since individuals increase in size and because juveniles and adults often differ in the type of microhabitat they occupy (Todd, 1949; Phillipson, 1960b; Edgar, 1971; Hillyard & Sankey, 1989). Examples that combine these two factors can be found in British phalangiids and leiobunines that migrate from the ground layer to the herb layer and from there to the tree trunks as they mature (Todd, 1949).

Gastropod predators Although most harvestmen are generalists, remarkable cases of specialist feeders are known among European harvestmen, namely, Ischyropsalis hellwigi hellwigi (Ischyropsalididae) and members of the family Trogulidae, which feed almost exclusively on terrestrial snails and slugs (Pabst, 1953; Martens, 1965, 1969a; Nyffeler & Symondson, 2001). Malacophagy is widespread among spiders, and about 20 genera in both Araneomorphae and Mygalomorphae have been shown to feed on gastropods (reviewed in Nyffeler & Symondson, 2001; Pollard & Jackson, 2004). Two species of scorpions, Opistophthalmus carinatus (Scorpionidae) and Hadogenes troglodytes (Ischnuridae), also eat pulmonates regularly (McCormick & Polis, 1990). However, no evidence exists of specialized gastropod predators among spiders and scorpions. Verhoeff (1900) was the first author to report malacophagy in a harvestman. A specimen of Ischyropsalis hellwigii that he attempted to rear died without ever accepting dead flies, but a second specimen readily attacked and ate living snails and slugs and survived for at least nine months. I. hellwigii hellwigii, which bears conspicuous powerful chelicerae (Figure 8.2), has been reported to consume pulmonate snails of the families Vitrinidae, Clausiliidae, Helicidae, and Zonitidae, as well as terrestrial arionid and limacid slugs (Verhoeff, 1900; Martens, 1965; Nyffeler & Symondson, 2001). However, it is worth noting that captive individuals were recorded to occasionally accept dipterans (Martens, 1978b) or freshly killed pierced larvae and pupae of Tenebrio molitor (J. Gruber, pers. comm.). Except for a single report of Ischyropsalis kollari eating vitrinid gastropods (Janetschek, 1957), most congeners, including I. luteipes, I. pyrenaea, I. strandi, and I. hellwigii lucantei, seem not to consume pulmonates but to eat various arthropods instead (Juberthie, 1964; Martens, 1969a, 1978b). Despite the belief of Silhavy (1957) that Trogulus nepaeformis only fed on snail mucus, seemingly all members of this family prey on gastropods. Pabst (1953) and Komposch (1992) offered several small-sized gastropods to captive trogulids, either collected among the accompanying fauna or not, and almost all were consumed. Even the earlier developmental stages attacked and ate live gastropods. Trogulids occasionally accepted freshly killed insects or spiders and live enchytreid worms, but gastropods were always preferred if available. The relationship between trogulids and their gastropod prey is so tight that representatives of this harvestman family are scarce in soils poor in calcium carbonate where snails are scarce (Pabst, 1953;

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A

Figure 8.2. (A) Female of the harvestman Ischyropsalis hellwigii hellwigii (Ischyropsalididae) feeding on a slug, Arion sp. (photo: J. Gruber). (B) Broken snail shells, feeding remains left by Ischyropsalis hellwigii hellwigii (photo: J. Martens). Scale bars = 10 mm.

B

see also Chapter 7). Dependence on snails in trogulids extends beyond nourishment since they require empty shells to lay their eggs (see Chapter 12).

Scavengers Harvestmen are generally assumed to be predators that may opportunistically eat dead prey (Figures 8.3A,B). With the exception of some mites, all other arachnids generally reject dead prey, and most records of necrophagy in these groups are

Diet and Foraging

A

B

C

D

E

F

Figure 8.3. (A) The harvestman Leiobunum manubriatum (Sclerosomatidae) feeding on the corpse of an earthworm in Japan (photo: N. Tsurusaki). (B) A female of L. vittatum feeding on a dead centipede in an abandoned quarry in Pennsylvania, USA (Photo: J. G. Warfel). (C) A male of Neosadocus variabilis (Gonyleptidae) feeding on a metamorphic tree frog, probably a Hypsiboas faber (Hylidae), in the Atlantic forest of southeastern Brazil (photo: R. A. Moraes). The predatory behavior was not observed; thus it is not possible to know if the prey was caught alive. (D) Leiobunum sp. feeding on the autotomized tail of the skink Eumeces fasciatus (Scincidae) in Virginia, USA (photo: T. McCormack). (E) Erginulus sp. (Cosmetidae) feeding on fruit remains in Costa Rica (photo: J. G. Warfel). (F) A male of Neosadocus variabilis feeding on a fallen fruit in the Atlantic forest of southeastern Brazil (photo: R. Andrade). Scale bars = 5 mm.

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restricted to captive individuals (Robinson, 1981; McCormick & Polis, 1990; but see Ross, 1981). Determining the relative importance of scavenging versus predation in the diet of a given species would be ecologically meaningful since these two modes of acquiring energy have different impacts on the dynamics of the ecosystem (Halaj & Cady, 2000). However, most observations are of harvestmen already consuming prey; thus it is not always clear whether this involves predation or scavenging (Kästner, 1931a, 1935b; Bristowe, 1949; Nyffeler & Symondson, 2001; Figure 8.3C), although the former scenario is often assumed. When scavenging, harvestmen may consume a wider range of prey items (Hillyard & Sankey, 1989). Morse (2001) reported interesting observations of Phalangium opilio (Phalangiidae) consuming intact carcasses of bees, wasps, and noctuid moths dropped by the crab spider Misumena vatia (Thomisidae) beneath the inflorescences where the spiders hunted. Sankey (1949b) provided unusual records of Oligolophus tridens, Mitopus morio, P. opilio, Opilio parietinus (all Phalangiidae), and Leiobunum rotundum (Sclerosomatidae) feeding on dead vertebrates, including fish, mammal, and bird remains, although none in an advanced state of decay (see also Figure 8.3D). Seemingly, not all species are equally inclined to scavenge. According to Immel (1955), individuals of Rilaena triangularis (Phalangiidae) only accepted dead pierced prey if they had been starved for a prolonged period. Captive Paranemastoma quadripunctatum, Nemastoma bimaculatum (both Nemastomatidae), Lacinius ephippiatus, and M. morio (both Phalangiidae) accepted only freshly killed or immobilized prey, but no carrion (Immel, 1954; Adams, 1984).

Vegetarians and fungivores Arachnids are essentially predatory organisms, but nearly 7,000 species of plant-feeding mites are found worldwide (Baker & Wharton, 1952). Until recently, a debate existed as to the extent to which uptake of vegetal matter was true for harvestmen (Hillyard & Sankey, 1989). However, laboratory records, as well as field observations, indicate that several phalangiids and sclerosomatids and nearly all studied gonyleptids normally eat some kind of plant and/or fungal matter, probably as a diet complement (references in Table 8.1; see also Figure 8.3E for a case among cosmetids). Bristowe (1949) recorded “a pellet of vegetable matter” and “the inside of a nutty seed” as consumed by Oligolophus tridens. There is evidence that the phalangiid Opilio parietinus eats pollen (Pfeifer, 1956), and Edgar (1971) observed one Leiobunum specimen feeding on a ripe raspberry. In captivity, juvenile Lacinius dentiger (Phalangiidae) accepted apples and pears (Mitov, 1988), and the gonyleptid Iporangaia pustulosa ate carrots and lettuce (Hoenen & Gnaspini, 1999). Finally, Halaj and Cady (2000) recorded several leiobunines in a hedgerow of a soybean field ingesting blackberries, nectar, and “other plant items.” A remarkable case involves the tropical gonyleptid Neosadocus variabilis, which was recorded in the field consuming fallen fruit (Gnaspini, 1996). Machado and Pizo (2000) conducted an experiment to investigate frugivory in this species and

Diet and Foraging

determined that N. variabilis exploits several fleshy fruits (Figure 8.3F). These authors detected a tendency for this species to prefer lipid-rich fruits and speculated that lipids obtained in fruits might equal lipid uptake from an arthropod prey. Such switching would allow the species to exploit an abundant resource available yearround in tropical forests (Machado & Pizo, 2000). Less frequently, some harvestmen were reported or supposed to eat fungi (references in Table 8.1). The Japanese sclerosomatids Gagrellula ferruginea and Melanopa sp. were observed to feed on a mushroom and a slime fungus, respectively (Uyemura, 1935; Huzita, 1936). Silhavy (1942) recorded specimens of the phalangiid Lophopilio palpinalis consuming juices of the mushroom Cantharellus. Fungivory is widespread among insects but is rare among arachnids, and mites are the only other major group of arachnids known to consume this kind of material (e.g., Nawar et al., 1993). In contrast to these records, several harvestman species have never been seen accepting food of vegetal or fungal origin; among these are the snail-specialized trogulids and Ischyropsalis. Additionally, neither Nemastoma bimaculatum, Lacinius ephippiatus, and Rilaena triangularis nor the widespread Mitopus morio eat plant matter, as revealed either by observations of captive animals or by examination of fecal pellets (Immel, 1955; Phillipson, 1960a; Adams, 1984).

Cannibalism Intraspecific predation is an important aspect in the biology of arachnids because it may influence population structure, life history, competition for mates and resources, and habitat use (Polis, 1981). Several reports indicate that harvestmen may sometimes kill and eat conspecifics and that cannibalism is somewhat common among phalangiids and leiobunines (see Table 9.3 in Chapter 9). Nonetheless, cannibalism has been observed more frequently to be inflicted upon weaker specimens, early stages of development, and during the molting cycle, when individuals are less mobile or the integument is soft. Gruber (1993) observed juvenile Dicranolasma (Dicranolasmatidae) being cannibalized, and Littlewood and Littlewod (1989) recorded a female Mitopus morio eating a molting conspecific in the field. The cannibalistic habit of targeting juvenile harvestmen markedly decreases as they approach adulthood and their integument hardens (Edgar, 1971). Immel (1954) stressed that cannibalism is somewhat common among early stages of Paranemastoma quadripunctatum, but she never observed this behavior among adults. Though less frequently, large and healthy individuals may also be attacked and eaten by groups of conspecifics: two specimens of Leiobunum aldrichi were observed attacking and eating a third one (Edgar, 1971). Group cannibalism occurs in several arthropods, such as backswimmers, red bugs, social hymenopterans, termites, and lacewing larvae (see Polis, 1981). It is important to stress, however, that among harvestmen such an attack was probably not the result of a coordinated behavior or group foraging, as probably occurs in the above-mentioned arthropods. According to Parisot (1962), male Platybunus bucephalus (Phalangiidae) often

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fight for females during the reproductive season, and the loser is generally eaten by the winner, while unreceptive females may eat unfortunate courting males (see Chapter 12). Unreceptive females of scorpions and spiders commonly eat the courting males, which are generally smaller (Elgar, 1992). In harvestmen, however, this behavior is rare, and sexual cannibalism in P. bucephalus is an exception, probably the result of captive conditions. In contrast, Juberthie (1964) did not observe a single case of cannibalism in adult Sironidae, Phalangodidae, Ischyropsalididae, Nemastomatidae, or Trogulidae. Nonetheless, some evidence exists that adult Ischyropsalis hellwigii may eat conspecifics if they are already dead, and some degree of cannibalism among juveniles is also suspected (J. Gruber, pers. comm.). The gonyleptids Acanthopachylus aculeatus and Goniosoma spelaeum ate only dead conspecifics (Capocasale & Bruno-Trezza, 1964; Santos & Gnaspini, 2002), and the same was reported for New Zealand triaenonychids (Forster, 1954). Cannibalism of eggs has been observed frequently (see Table 9.3 in Chapter 9). Eggs are a developmental stage particularly vulnerable to cannibalism since they are rich in energy and nutrients and are relatively defenseless unless they are hidden or guarded by a parent. Egg cannibalism is widespread, occurring in practically every major group of animals, including gastropods, arachnids, social and nonsocial insects, fish, amphibians, and birds (Elgar & Crespi, 1992). Moreover, cannibalism of eggs is thought to be an important selective pressure in the evolution of parental care in Laniatores (see Chapter 12).

Diet in captivity Many species reared in captivity accepted not only live or pierced prey, but also a surprising variety of plant matter and even commercial food. However, some items have been reported to be taken only if nothing else was available (Edgar, 1971), and others were never accepted. Todd (1949) reared several phalangiids and leiobunines on a mixture of dried egg, flour, and yeast. Klee and Butcher (1968) fed captive Phalangium opilio with dried bacon and corn meal. Edgar (1971) maintained phalangiids using dried and pulverized lean beef, as well as beetles, grasshoppers, and mayflies prepared in the same way. A complex artificial dietary formula containing dehydrated bread, prawns, carrots, and several vitamins was successfully tested on the sclerosomatid Gagrellula saddlana (Anuradha & Parthasarathy, 1977). Observations in captivity may be biased because harvestmen may take food items they normally would not consume in nature (Pabst, 1953). For example, the gonyleptid Goniosoma spelaeum accepted vegetal matter in the laboratory, but it was never seen consuming plants in nature despite many hours of field observations (Santos & Gnaspini, 2002). Pfeifer (1956) stated that the phalangiids he reared, although able to eat vegetable matter, always preferred food of animal origin. Moreover, he observed that if fed with moist bread and vegetables for long periods, harvestmen developed constipation problems, which were easily cured by feeding on animal matter again. Adult Leiobunum manubriatum, L. globosum, and Nelima nigricoxa

Diet and Foraging

(sclerosomatidae) reared in captivity can be maintained healthy over a long period of time by using fish sausage and bread as diet. However, supplementary food items seemed necessary to ensure the maturation of ovaries (N. Tsurusaki, pers. comm.).

Drinking water Water availability is a critical requirement for harvestmen (Kästner, 1926; see Chapter 14). Several authors stressed the importance of providing water to captive individuals; otherwise, they may die in a few hours or days (Bishop, 1950; Cloudsley-Thompson, 1958; see also Chapter 15). This need, however, is clearly not the same for all species, and some authors indicated that harvestmen may drink little (or nothing) if the environment is humid enough to prevent desiccation (Pabst, 1953; Immel, 1954; Hillyard & Sankey, 1989). Harvestmen often have been described drinking water directly with the mouthparts (e.g., Kästner, 1926, 1935b; Pabst, 1953; Savory, 1962; Capocasale & BrunoTrezza, 1964; Acosta et al., 1995). To imbibe water, P. quadripunctatum touches a humid surface or water pool with the densely haired tip of legs and/or pedipalps and brings minute water droplets to the mouth (Immel, 1954). Leiobunum rotundum has been seen scraping grass stalks with its mouthparts, and Mitopus morio grasps the surface of leaves with the chelicerae, supposedly to draw moisture from plant juices (Todd, 1950). Also, the large Goniosoma spelaeum chews plants to obtain water (Santos & Gnaspini, 2002). There is one bizarre report of a harvestman, presumably a phalangiid, drinking milk from a saucer (Heath, 1914).

FINDING FOOD Because of the broad spectrum comprised in the diet of many harvestmen, the process of food detection does not follow a single or strict pattern but includes at least two major components that alternate or combine opportunistically: hunting live prey and gathering immobile food items. To capture living prey, most harvestman species seem to rely on an ambush strategy or, more rarely, on active hunting. In several species periods of waiting are intercalated with periods of slow movement in which the individuals explore their environment using the tips of their forelegs, thus enabling the harvestman to encounter items such as carrion or vegetal matter. The sensory mechanisms involved in each process have also been subjected to debate, as shown later.

Detection of living prey Most observations indicate that harvestmen are relatively stationary while seeking live prey. Except for one record of Mitopus glacialis actively capturing glacier-dwelling collembolans (Steinböck, 1931), most authors describe hunting harvestmen in a sitand-wait position (Phillipson, 1960a; Machado et al., 2000; Santos & Gnaspini,

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2002). Several authors agree that prey is probably primarily detected through mechanical stimuli, as occurs with scorpions (McCormick & Polis, 1990), ground spiders (Foelix, 1996), and solifuges (Punzo, 1998). Harvestmen do not possess trichobothria, but their legs and pedipalps are known to be covered by a great quantity of sensory hairs (see Chapter 2). Some of these hairs, known as sensilla trichodea, are responsible for detecting mechanical stimuli (Guffey et al., 2000; Willemart & Gnaspini, 2004b). Phillipson (1960a), Martens (1975c), and Santos and Gnaspini (2002) consider that physical contact with prey is needed to detect it and initiate capturing movements. This contact may happen when the prey passes near the harvestman and accidentally touches its appendages, especially the tarsus of leg II. Despite the evidence for the need of physical contact with the prey, Kästner (1941) and Immel (1954, 1955) reported that Mitopus morio, Paranemastoma quadripunctatum, and Rilaena triangularis also seem to react to movements of the prey without the need of physical contact, thus suggesting distance mechanoreception. Hunting harvestmen adopt a motionless posture, sometimes for several hours, with extended appendages and legs II straight upward or sideways (Figure 8.4A). This posture is widespread among gonyleptids, such as Acutisoma longipes (Machado et al., 2000), Goniosoma spelaeum (Santos & Gnaspini, 2002), and Pachyloidellus goliath (Acosta et al., 1995). A remarkably similar foraging strategy is employed by whip spiders, which use their first pair of sensorial legs to detect prey and move only a few centimeters throughout the night (Weygoldt, 2000). Individuals of some Goniosomatinae species also show a curious hunting position in which the body hangs between two leaves or stick branches while legs I and II are maintained free and waving around (Figure 8.4B). In this position the body and the legs of the individuals may emulate a spiderweb to increase the chance of intercepting flying insects (Santos & Gnaspini, 2002). Despite Bishop’s (1950) belief that eyes of Leiobunum aldrichi allow this diurnal harvestman to detect movement at distances of several feet, or Parisot’s (1962) supposition that flying Drosophila are caught once they enter the visual field of phalangiids, it is unlikely that harvestman eyes play an important role in prey detection, at least for most studied harvestmen (Kästner, 1926; Pabst, 1953; Immel, 1954). The first experiment on the role of vision in prey detection was conducted with Rilaena triangularis, whose individuals capture “so resolutely a flying fly, that one could think prey is detected visually” (Immel, 1955). However, individuals of this species with eyes covered were as capable of capturing flies as control individuals. Furthermore, specimens of R. triangularis showed no reaction when separated from living flies by transparent glass but readily assumed a hunting posture if a fly touched the glass, suggesting detection of vibrations transmitted through the substrate (Immel, 1955). Although vision seems not to be important in prey detection among most arachnids, exceptions include spiders of the families Deinopidae, Lycosidae, Salticidae, and Thomisidae (Foelix, 1996), as well as some diurnal solifuges (Punzo, 1998). Among harvestmen, generalizations also should be made cautiously, since the large eyes of Caddo agilis (Caddidae), together with its very agile movements,

Diet and Foraging

A

C

B

D

Figure 8.4. (A) Female of Neosadocus variabilis (Gonyleptidae) in a typical sit-and-wait position with legs II extended sideways (photo: B. A. Buzatto). (B) Female of Acutisoma proximum in a curious hunting position, in which the body hangs between two leaves or sticks while legs I and II freely flutter about (photo: M. O. Gonzaga). (C) Lateral view of a female Sodreana sodreana (Gonyleptidae) showing the armature of the pedipalps (photo: R. J. Sawaya). Note the especially elongated femora and patellae that increase the range of movement of the raptorial appendages. Arrow indicates the apical claw. (D) Female of Stygnus sp. (Stygnidae) accomplishing leg threading (photo: G. Machado). Scale bars = 10 mm.

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strongly suggest that they represent specializations for visual prey detection and capture (Tsurusaki, 2003; see also Figure 2.1d in Chapter 2). The only evidence that harvestmen may use vision for hunting comes from the cave dwellers Hendea myersi cavernicola (Triaenonychidae) and Megalopsalis tumida (Monoscutidae), which feed almost exclusively on the glowworm Arachnocampa luminosa (Diptera: Keroplatidae). Despite their cavernicolous habits, both species have well-developed eyes, and behavioral tests in the laboratory simulating the dim blue green light of glowworms demonstrated that both harvestman species detect and approach the source of light (Meyer-Rochow & Liddle, 1988, 2001; see also Chapter 14). Furthermore, it was also experimentally demonstrated that radiation from an ultraviolet source caused both species to turn away. These observations lead to the conclusion that neither Hendea nor Megalopsalis is blind, and that their capacity for distinguishing different sources of light serves an important function. The ability to orient toward the glowworm light certainly enhances their foraging efficiency inside the caves, where food is generally scarce and patchy. Additionally, since both species are troglobites and present reduction in body pigmentation, individuals are also able to recognize and avoid areas of ultraviolet radiation, such as openings in the cave (Meyer-Rochow & Liddle, 1988, 2001).

Chemoreception Harvestmen may also take prey encountered during exploratory walks (Santos & Gnaspini, 2002), and chemoreception is likely to play a central role in this act. Pabst (1953) showed that trogulids can follow trails of mucus left by snails, insofar as the trail is not dried out. These observations support the idea of food detection by chemical stimuli, probably performed by pedipalps and/or legs I–II. The most important chemoreceptors in harvestmen are the sensilla chaetica, located mainly on the distal segments of legs I and II (Guffey et al., 2000; Willemart & Gnaspini, 2004b). Although few studies exist on the morphology and the function of these receptors, chemical cues are probably important in food localization. It was believed that the long pedipalps of nemastomatids, which bear dense apical brushes of hairs, were used by the individuals to follow chemical trails as well, but this hypothesis was not supported by experiments made with Paranemastoma quadripunctatum by Immel (1954). This species possesses a well-developed taste sense (contact chemoreception), probably located on the mouthparts, but olfaction could not be proven (Immel, 1954). In contrast, Santos and Gnaspini (2002) suggested that some kind of airborne chemoreception might be involved in the rapid reaction shown by some harvestmen when food is placed in their terrarium. Observations on captive Pachyloidellus goliath and Discocyrtus prospicuus, reacting within two to three minutes after food (pierced Tenebrio larvae or ham) was provided several centimeters away, support this view (L. E. Acosta, pers. obs.). Similarly, olfaction was implied from observations made by Willemart (2002) on captive Acutisoma discolor (Gonyleptidae) that, in addition, were also able to follow a presumable trail where a food item was dragged.

Diet and Foraging

Chemosensory capabilities, especially olfaction, might be more likely linked to scavenging habits than to predation.

PREY CAPTURE Once aware of the presence of food, the otherwise motionless harvestman may pounce rapidly to capture prey with its appendages (Kästner, 1935b; Immel, 1954, 1955; Pfeifer, 1956; Gruber, 1993). Unlike scorpions and most spiders, harvestmen have no venom glands, so prey must be immobilized and secured with pedipalps, chelicerae, and/or legs, and only then is it eaten, usually while still alive. As stated earlier, size and hardness of the potential prey may signal the harvestman whether to pursue or refuse it (Phillipson, 1960a). Some harvestmen approach live prey slowly, and violent movements displayed by the latter often cause retreat of the predator (Kästner, 1926; Rühm, 1926; Edgar, 1971; Katayama & Post, 1974). Juvenile dicranolasmatids have been reported to capture prey as large as or larger than themselves (Gruber, 1993). Also, delicate long-legged phalangiids and leiobunines are known to subdue relatively large prey compared with their body size (Immel, 1955; Edgar, 1971). Platybunus bucephalus and R. triangularis were reported to kill large lepidopteran or dipteran larvae by subduing the prey with chelicerae and pedipalps for as long as half an hour, until it no longer offered resistance (Kästner, 1931a; Immel, 1955). On three separate occasions a Leiobunum nigripes female was observed killing and consuming an ephemeropteran imago almost two and a half times her size (Halaj & Cady, 2000). Pyrenean cave species of Scotolemon (Phalangodidae) were reported to be particularly ferocious when preying on Speonomus beetles (Jeannel, 1926). Verhoeff (1900) reported that a terrestrial slug twice as long as Ischyropsalis hellwigii could be attacked and consumed in one night.

Diversity of mechanisms and devices Phalangiids, such as Rilaena triangularis and Mitopus morio, as well as some leiobunines, are able to catch dipterans in flight by suddenly moving their walking legs (drawing all legs inward), then passing the fly to the pedipalps, and finally grasping the prey with the chelicerae (Immel, 1955; Pfeifer, 1956; Phillipson, 1960a; Parisot, 1962). Pedipalps, together with legs I, serve to manipulate the prey and secure it if it is still struggling (Stipperger, 1928; Bishop, 1949b, 1950). Most phalangiids and leiobunines have delicate pedipalps, bearing only a small apical claw, but in some (e.g., Platybunus, Megabunus, Lophopilio), these appendages are armed with strong ventral spines, especially on the femur (Martens, 1978b). This armature likely plays a role in restraining a thrashing prey, as suggested by Stipperger (1928) and Steinböck (1931). Femoral spines of the pedipalp of Caddo agilis are similarly suspected to be used in prey capture (N. Tsurusaki, pers. comm.). In Laniatores the main hunting appendages are the remarkably armed pedipalps (Kästner, 1935b; Martens, 1978b), which bear ventrolateral rows of spines on the tibia and tarsus

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and sometimes also on the femur; in addition, the tarsus has a strong apical claw, which provides an efficient subchelate tool (Figure 8.4C). Such armed pedipalps are also found in whip spiders and, as in most Laniatores, they are used as raptorial weapons in prey capture (Weygoldt, 2000). Pedipalps of Dyspnoi are, in contrast, pediform, without any kind of armature or a single apical claw. Among them, the pedipalps of nemastomatids are covered by noticeable sphere-tipped, glandular hairs, denser on the apical portion (Martens, 1978b; see also Figure 2.3i in Chapter 2), whose secretion was deemed to be adhesive and serve in prey capture (Rimsky-Korsakow, 1924; Kästner, 1935b). Direct observations on Paranemastoma quadripunctatum did not support this function: the pedipalpal hairs seem to be no longer functional in adults, which use their chelicerae to grasp prey, securing it with the long pedipalps (Immel, 1954). In Dicranolasmatidae, adhesive hairs of the pedipalps are restricted to nymphal stages (Martens, 1978b). Juvenile Dicranolasma scabrum use these hairs to glue collembolans up to twice their size and then rapidly pass the prey to the chelicerae (Gruber, 1993). In a similar way many solifuges (including adults) use their pedipalps, with adhesive organs, to capture prey and pull it toward the chelicerae (Punzo, 1998). The conspicuous hairs that cover the pedipalpal tibia and tarsus of Sabacon paradoxus (Sabaconidae) histologically proved to be of sensory and glandular nature, and their possible role as adhesive hairs for prey capture was also hypothesized (Juberthie et al., 1981b). Shear (1996) states that sabaconids use the pedipalps as a stick “flypaper” to capture prey, which is then raked off the pedipalps with specialized cheliceral combs. The “sticky mechanism” attributed to several Dyspnoi is probably more effective for or limited to juveniles and smaller species (J. Gruber, pers. comm.). Snail eaters simply grasp their prey with the chelicerae. Ischyropsalis kollari was reported to catch flying Drosophila by using legs I–II and then seizing it with the chelicerae (Martens, 1975c, 1978b). In a similar way Cyphophthalmi species capture their prey, mainly collembolans and proturans, by using their chelicerae (Kästner, 1935b; Juberthie, 1964).

THE FEEDING ACT Food transport Unless food items are too large to be transported, many harvestmen carry them away from the capture site. Phalangiids and leiobunines most commonly move to an elevated site (Henking, 1888; Stipperger, 1928; Bristowe, 1949; Todd, 1949; Parisot, 1962; Edgar, 1971; Halaj & Cady, 2000; Morse, 2001), whereas other harvestmen— trogulids, ischyropsalidids, nemastomatids, dicranolasmatids, and gonyleptids—hide in a sheltered place (Pabst, 1953; Immel, 1954; Capocasale & Bruno-Trezza, 1964; Martens, 1975a; Komposch, 1992; Gruber, 1993; Elpino-Campos et al., 2001). In several gonyleptids studied by Hoenen and Gnaspini (1999), movement away from the food source may be mediated by contact with other individuals, since they stop and

Diet and Foraging

begin to eat when they no longer touch each other. Since food theft in harvestmen was recorded both in the field and in the laboratory, carrying food away might help prevent or attenuate competition with other predators, including conspecifics (Hoenen and Gnaspini, 1999; Halaj & Cady, 2000). Several scorpions also take prey to a shelter or to an elevated site before consumption, and this behavior probably protects the individuals from predation while feeding (McCormick & Polis, 1990). Nonetheless, cases of food sharing have been reported for some harvestmen species when a large piece of food was involved and it was not possible to transport it (discussed later).

Ingestion and assimilation Feeding in harvestmen may last from a few minutes to several hours. By alternate movements, the chelicerae cut off pieces of the cuticle and the inner tissues of the prey (Kästner, 1925; Immel, 1954). The initial bites are usually inflicted on parts where the integument is thinner, such as the opisthosomal intersegmental membranes (Pfeifer, 1956; Whiteley, 1961; Parisot, 1962). A clear fluid originating in the mouth often mixes with the food particles (Kästner, 1935b; Pabst, 1953; Immel, 1954). The soft, movable mouthparts (maxillary lobes of coxae of pedipalps and forelegs) are usually applied directly on the food item, collecting loose particles and fluids and directing them into the foregut; chelicerae also help bring food pieces to the stomotheca (Martens, 1975a,c). Unlike most arachnids, harvestmen swallow small particles, not just extraoral predigested liquids, so that most digestion may be enteric (see Chapter 2). While the animal is eating, sensory legs II are normally raised and slightly moving (Edgar, 1971; Martens, 1975c; Komposch, 1992). After feeding, many species clean their appendages with the mouthparts (Kästner, 1925; Stipperger, 1928; Bishop, 1950; Parisot, 1962; Edgar, 1971; see also Figure 8.4D). Small chitin pieces can be detected in the feces and gut contents of harvestmen (Rühm, 1926; Steinböck, 1931; Bishop, 1950; Pfeifer, 1956; Phillipson, 1960a; Capocasale & Bruno-Trezza, 1964). Dixon and McKinlay (1989) exploited this fact to identify parts of aphids in the enteric contents of harvestmen caught in pitfall traps. An intact Tetranychus mite was found in the midgut of Phalangium opilio (Katayama & Post, 1974). However, many prey items become unrecognizable, especially the softskinned ones, and analyses of gut fluids have been done using antisera to identify ingested prey types (e.g., Ashby, 1974; Sunderland & Sutton, 1980; Adams, 1984). Verhoeff (1900) and Martens (1965, 1975a) provide details of the feeding of the snail eater Ischyropsalis hellwigii hellwigii. After several unsuccessful attempts to grasp the smooth shell surface, the harvestman finally seizes the apertural lip of the shell with one chelicera. The predator normally moves from the site of capture, carrying the snail held under its body. Thereafter the harvestman places the snail on the ground with the shell opening oriented upward and begins to cut off the soft tissues with the other chelicera; small pieces are ingested with the help of the maxillary lobes. As a defense, the snail retracts its body into the inner whorls, but the harvestman then uses its powerful chelicerae to break off pieces of the shell, starting with the aperture margin. The procedure continues until the soft parts are reached

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again and the gastropod’s body is completely consumed (Martens, 1965, 1975a). The remains of the meal may consist of the broken shell, sometimes with mostly the columella remaining (Figure 8.2B). Only snail species with an armed aperture (such as the adult clausiliids) are seemingly able to resist the attack of harvestmen (Martens, 1975a). Although all Ischyropsalis species bear large chelicerae (Martens, 1978b), those of I. hellwigii hellwigii are especially robust, which may account for the remarkable feeding specialization of this species (Martens, 1975a). Trogulids consume the soft parts of their prey without damaging the shell. The chelicerae cut pieces off the snail while still alive, and if the prey is so large that internal tissues cannot be reached with the mouthparts alone, then the harvestman enters the shell through the aperture to consume it (Pabst, 1953). Members of this family are able to eat gastropods larger than themselves, but smaller snails are preferred if available (Pabst, 1953; Komposch, 1992). The snail may eventually react by secreting abundant mucus and foam, which were reported to make individuals of Anelasmocephalus hadzii relinquish the attack (Komposch, 1992). Because of the differences in the feeding strategies, Nyffeler and Symondson (2001) termed trogulids shell intruders, as opposed to I. hellwigii hellwigii, a shell breaker. A comparison between gastropod-specialized harvestmen and carabid beetles reveals an interesting convergent evolution of morphologies (see Nyffeler & Symondson, 2001). Like trogulids, carabids of the genus Cychrus have an elongated flat head and pronotum that enables them to crawl into the snail and pull out the soft bodies. By contrast, carabids of the genus Procerus are heavily built animals with powerful mandibles that enable them to crush large, hard-bodied prey. Like I. hellwigii hellwigii, Procerus beetles are shell breakers. It has been calculated that adult Mitopus morio assimilates 47% of the food consumed, while assimilation of second-instar specimens reaches 74% (Phillipson, 1960b). This difference may result from the less powerful chelicerae of young harvestmen, which are obliged to ingest softer (i.e., more digestible) parts of the prey than adults do (Phillipson, 1960b). Nymphs seem to be remarkably ravenous and die in a few days without food. Adult harvestmen, however, have been reported to resist long periods of starvation. When food is available again, they are able to consume large amounts at one time, producing a noticeable abdominal expansion and a dramatic increase of body weight (Pabst, 1953; Immel, 1954, 1955). This ability to consume a great quantity of food at one time, a highly efficient food-storage organ, and a low metabolic rate may together enable harvestmen to survive long periods of food deprivation, as recorded for scorpions and spiders (Polis, 1990; Foelix, 1996). The digestive system of harvestmen seems to be adapted to cope with certain defensive toxins of their prey. Mitopus morio, for instance, tolerates the defensive alkaloids of the larvae of the chrysomelid leaf beetle Oreina cacaliae (Hartmann et al., 2003). Ingested alkaloids are efficiently detoxified by N-oxidation in the gut and rapidly eliminated with the feces. This is the only example of a nonsequestering arthropod that is able to detoxify alkaloids by N-oxidation. Further studies should be done in order to test if this adaptation is a general taxonomic feature of Opiliones or a specific physiological trait of M. morio.

Diet and Foraging

FORAGING ACTIVITY Daily activity patterns Like the great majority of arachnids, most harvestmen are nocturnal foragers, hiding during the day in moist shelters under rocks or in crevices, moss, or logs (see Chapter 7). The sclerosomatid Leiobunum rotundum spends the daytime climbing on tree trunks and descends to the herb layer at dusk. There it hunts for food on the underside of plants, bringing the prey back to the upper side to consume it (Todd, 1949). In Pampa de Achala (Argentina), Pachyloidellus goliath appears in high densities after dusk (at around 9 p.m. in summer), emerging from under the large stones and from the deep crevices of the granite outcrops where they shelter during the day (Acosta et al., 1995). A detailed ethogram on captive individuals of Discocyrtus oliverioi indicated that foraging activity takes place mostly between 6 p.m. and 2 a.m., and that during the daytime most individuals remain resting inside shelters. However, a number of exceptions exist, especially among the Holarctic phalangiids and leiobunines, which have diurnal activity, including feeding (Pfeifer, 1956; see also Chapter 14). A number of gonyleptids use caves as diurnal shelter but walk to the epigean habitat at night in search of food. The diel cycle of Acutisoma longipes and Goniosoma spelaeum has been studied in detail (Gnaspini, 1996; Machado et al., 2000; see also Chapter 14). Individuals of these two species follow a fixed trail for exiting and reentering the cave. Specimens of G. spelaeum that followed one of these fixed trails always climbed the same tree at night. Field experiments are needed to test if route fidelity in goniosomatines is mediated by chemical cues or if the harvestmen have a spatial memory of the trail. During the day, while individuals are found inside the caves, little feeding activity was recorded for G. spelaeum (Santos & Gnaspini, 2002). In contrast, individuals of A. longipes were observed consuming conspecific eggs, as well as egg sacs of the troglophile spider Plato sp. (Theridiosomatidae). The egg sacs of Plato hang 4–6 cm off the cave walls by means of a single silk thread, but the large goniosomatine harvestmen manage to retrieve them with their armed pedipalps. Adult specimens of G. spelaeum do not leave the cave every night, but early nymphs and ovigerous females forage outside almost daily (Gnaspini, 1996). Quantitative comparisons of the behavioral repertory of males and females in the gonyleptid Mischonyx cuspidatus yielded similar results (Pereira et al., 2004). Females fed at a higher frequency than males despite the fact that exploration activities were not significantly different between the sexes. It is known that the respiratory rate of female harvestmen increases when they are producing and maturing eggs (Phillipson, 1962b, 1963). This physiological change during egg development probably accounts for the higher requirement for food in G. spelaeum, as well as in M. cuspidatus. In species that present maternal care, accumulation of energy is crucial not only for egg production and maturation, but also for maintenance of females during egg guarding, a period in which they are prevented from foraging (see Chapter 12). Studying British phalangiids, Williams (1962) showed that most foraging activities occurred at night. When hungry, however, harvestmen could be found active

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during the day, but only if the relative humidity was high. In order to test the effect of hunger on the activity schedule, the author conducted laboratory trials with individuals of Oligolophus tridens. The results demonstrated that foraging activity of starving individuals started progressively earlier each day when compared with fed individuals. Additionally, diurnal movements were more frequent among the starving individuals. Temperature may also influence foraging activities in harvestmen. Capocasale and Bruno-Trezza (1964), for instance, showed that the appetite of captive individuals of Acanthopachylus aculeatus (Gonyleptidae) seems to be directly related to environmental temperature.

Foraging strategies Concerning the broad classical categories currently recognized for predatory strategies, most harvestman species are ambush predators rather than active hunters (Acosta et al., 1995; Machado et al., 2000; Santos & Gnaspini, 2002). Ambush minimizes energy expenditure and is commonly found among species with a low metabolic rate that can survive long periods of food deprivation. On the contrary, active hunters spend much time searching for a putative prey, which involves a comparatively greater expenditure of energy (Schoener, 1971). Despite their theoretical importance, ambush and active hunting represent endpoints on a continuum of strategies, and pure examples of these two types of foraging strategies are rarely found in arachnids (Riechert & Luczak, 1982). Closer to the “active-hunter” end of the foraging strategies, individuals of Mitopus glacialis were observed actively searching and capturing collembolans (Steinböck, 1931), and Todd (1949) describes Mitopus morio as an active hunter that is frequently seen walking on the herb layer. Also, specialized predators, such as the snail eaters, must search actively for their prey. In these cases the high costs demanded in food location may be counterbalanced since a great percentage of the body of a gastropod is potential food. Therefore, the harvestman can extend the period of prey handling and nutrient extraction (Nyffeler & Symondson, 2001). Species that regularly include fruits in their diets, such as Neosadocus variabilis, also need to actively search for this type of food. As occurs with gastropods, fruits are generally nutrient rich and may represent a satisfying reward for a foraging harvestman. Moreover, in some tropical forests fleshy fruits are produced in great quantities and almost continuously through the year (see Machado & Pizo, 2001), which certainly minimizes the searching time. As mentioned earlier in several harvestman species periods of waiting intercalate with periods of exploratory displacements. Exploration was the most frequent behavioral category accomplished by captive individuals of the gonyleptid Discocyrtus oliverioi, comprising almost 70% of all behavioral acts (Elpino-Campos et al., 2001; Figure 8.5). Analysis of the relative frequency of the three behavioral acts designated within the category of exploration showed that walking about accounted for nearly 28% of the total, while remaining in the same place and sensing the substrate with legs I–II comprised the remaining 72%. Since pierced worms were preferred over live termites, these results are clearly consistent with predominantly scavenging habits, which demand increased searching activities. Cavernicolous

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Figure 8.5. Daily activity pattern of the harvestman Discocyrtus oliverioi (Gonyleptidae) based on three different days of samples and obtained from eight captive individuals. The sun and moon indicate dawn and dusk, respectively. Modified from Elpino-Campos et al. (2001).

species of Goniosomatinae also represent good models of a mixed strategy of foraging. Despite the fact that individuals of Acutisoma longipes and Goniosoma spelaeum are commonly seen motionless on vegetation at night, with extended legs II, for the former species it has been proved that they can walk as far as 70 m away from the cave entrance (Machado et al., 2000). Although individuals of G. spelaeum move a much shorter distance, up to about 5 m from the cave entrance, they can be found in the canopy, as high as 20 m above the ground (Santos & Gnaspini, 2002).

Stealing, robbing, and sharing Several instances of harvestmen attempting to steal prey held by another individual have been reported. The thief individual may flee, bringing its meal to a more secure site, or the two individuals may fight for the food (Bishop, 1949b, 1950; Pabst, 1953; Immel, 1954; Edgar, 1971; Komposch, 1992; Gruber, 1993; ElpinoCampos et al., 2001). Most reports refer to intraspecific interactions, but Willemart (2002) also recorded fights in captivity between individuals of the gonyleptids Acutisoma discolor and Neosadocus variabilis. This author reported several observations in which an individual simply steals food from another (conspecific or not), without reaction of the latter. The fighting individuals “pull and tug” the same piece of food or attack each other with cheliceral bites. The dispute may end with a winner, but occasionally it results either in the item breaking, with each harvestman receiving a piece (Willemart, 2002), or the two or more individuals finally sharing the food

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A

B

Figure 8.6. (A) Three individuals of the harvestman Pachyloidellus goliath (Gonyleptidae) feeding on an earthworm in Pampa de Achala, Argentina. Food sharing is very common in this species, and up to five individuals may be found feeding on the same prey (photo: G. Machado). (B) Three sclerosomatid harvestmen feeding on the corpse of a grasshopper in Kentucky, USA (photo: J. G. Warfel). Scale bars = 10 mm.

(Trogulidae: Pabst, 1953; Nemastomatidae: Immel, 1954; Dicranolasmatidae: Gruber, 1993; Gonyleptidae: Willemart, 2002; see also Figure 8.6). Kästner (1926) mentioned that four or five phalangiids may peacefully concentrate around a large vegetal piece. Food sharing in nature has been reported by Bristowe (1949: two Paroligolophus agrestis sharing bird droppings), Acosta et al. (1995: three male Pachlyloidellus goliath simultaneously feeding on a caterpillar, still alive), and Halaj and Cady (2000: a male and a female Leiobunum nigripes jointly extracting an earth-

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A

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C

D

Figure 8.7. Sequence of the harvestman Acutisoma longipes (Gonyleptidae) stealing a moth from the ctenid spider Enoploctenus cyclothorax (photos: J. Sabino). (A) The harvestman approaches the spider that is holding the prey with the chelicerae. (B) The individual touches the spider with the second pair of sensorial legs. (C) The harvestman suddenly moves toward the spider, which moves backward, retreating from the prey. (D) The harvestman takes the prey while the spider moves away.

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worm from a burrow). These observations contrast with those on most other arachnids in which food sharing is extremely rare (e.g., Weygoldt, 1969; McCormick & Polis, 1990; Uetz & Hieber, 1997). Field observations of a harvestman stealing prey from another predator or attempting to do so are scarce. A female Acutisoma longipes was observed stealing a moth partially wrapped in silk from the ctenid spider Enoploctenus cyclothorax (Sabino & Gnaspini, 1999; Figure 8.7). By rapidly trampling over the startled spider, the harvestman provoked it to release its prey. Then the thief took the moth, and the spider moved away. This action seems likely to be an opportunistic theft, rather than a case of regular kleptoparasitism (Sabino & Gnaspini, 1999). Machado et al. (2000) also found an individual of A. longipes in the field carrying insect remains wrapped in silk, but it is unclear whether it stole the prey or simply took advantage of an abandoned item. Morse (2001) observed an adult Phalangium opilio unsuccessfully trying to grasp a half-consumed bee from the thomisid spider Misumena vatia. Cosmetids of the genera Cosmetus and Metavononoides have been observed taking prey from webs of the pholcid Blechroscelis sp. (Sabino & Gnaspini, 1999).

APPLIED ASPECTS M. E. Walker’s (1928) emphatic statement that phalangiids are of no economic value whatsoever is likely far from being true. Because of their polyphagous habits, broad distributions, and abundance, harvestmen have received increased attention as a potential agent for pest control in agroecosystems. The widespread Phalangium opilio seems to be one of the preferred species for study (Halaj & Cady, 2000; Newton & Yeargan, 2001, and references therein). In New Zealand (where the species was introduced) this harvestman was estimated to be responsible for 31.5% of total arthropod predation on the lepidopteran Pieris rapae in cabbage crops, from the egg to the third-instar stage (Ashby, 1974). This percentage was much higher than that observed for a lycosid spider (2.0%). In contrast to P. opilio, which readily climbs plants in search of prey, the lycosid spider was never observed on plants and showed little climbing ability, suggesting that it feeds only on larvae that fall from the plant; therefore, its importance as a biological control agent is quite small (Ashby, 1974). Harvestmen also ranked among the top predators of lepidopteran larvae in corn agroecosystems, especially at the beginning of the season (Brust et al., 1986). Dixon and McKinlay (1989) detected that six harvestmen species inhabiting potato fields in Scotland (P. opilio, Opilio saxatilis, O. parietinus, Mitopus morio, Paroligolophus agrestis, and Leiobunum rotundum) had aphid remains in their enteric contents. Phalangium opilio was the dominant species in the field, with 54% of the examined specimens having eaten aphids. The same harvestman species was significant in reducing survival of early instars of the Colorado potato beetle, a quite destructive chrysomelid (Drummond et al., 1990). Newton and Yeargan (2001) tested the predatory capabilities of P. opilio on the noctuid lepidopteran Helicoverpa zea in the laboratory and de-

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termined that fourth- and sixth-instar juveniles and adult females attacked both eggs and first-instar larvae of the insect, while second-instar juveniles did not. Although P. opilio alone appears unable to keep populations of any pest under control, it serves as one member of a complex of generalist predators inhabiting crops that, collectively, may be able to keep pest densities low. Working on the lynx spider Oxyopes salticus (Oxyopidae), Young and Lockley (1985) reached a similar conclusion: the species plays a major role in keeping several pest species at low levels, but it cannot control pest outbreaks alone. As occurs with spiders (reviewed in Wise, 1993), field studies with harvestmen as biocontrol agents have not always produced conclusive evidence. A field study performed by Halaj and Cady (2000), for instance, found no evidence to conclude that harvestmen could be important biological control agents in soybean fields. Interestingly, the authors found that earthworms constitute nearly 47% of the total food items of five leiobunine species. This type of predation suggests that harvestmen are important for local food-web dynamics by providing evidence for an upward trophic connection between soil detritivores and grazing subsystem foragers (Halaj & Cady, 2000).

CONCLUDING REMARKS Feeding has always been a primary question regarding the biology of any animal group, and even early publications on harvestman biology contain some reference to this very basic topic. After decades of debate and many attempts at generalization, it seems clear now that meaningful variation exists across different taxa within the order Opiliones. Most studied species proved to be opportunistic generalists whose food habits ranged from preying on small invertebrates to occasionally gathering dead prey and sometimes even vegetal matter. Others appear more specialized, with a much narrower food spectrum. All observations indicate that harvestmen play an important role within food webs. A number of questions remain unsolved, such as the relative importance of scavenging versus predation in natural conditions, that is, the actual ecological role of specific harvestman species. Previous studies have shown that harvestmen can play an important role in food webs of temperate regions, but absolutely nothing is known for tropical environments. The potential of harvestmen as biological control agents was tested for a few species, and most results obtained pointed out that allied with other predatory arthropods, they can produce a significant decrease in pest populations. Likewise, still more needs to be known about the feeding habits of many families not studied thus far. The great variation in habitat use, cheliceral and pedipalpal morphology, and body size and behavior of these nonstudied families suggests that a wider range of prey and trophic interactions remains to be discovered. The issue of food habits in harvestman biology is quite old in the literature, but it continues to offer a wide-open field of opportunities for further research.

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ACKNOWLEDGMENTS This chapter greatly benefited from the criticism and helpful suggestions made by J. Gruber, J. C. Cokendolpher, D. H. Morse, A. B. Cady, and an anonymous reviewer. Special thanks go to J. Warfel, J. Gruber, J. Martens, N. Tusurusaki, R. A. Moraes, T. McCormack, R. Andrade, B. A. Buzatto, M. O. Gonzaga, R. J. Sawaya, and J. Sabino for generously facilitating some of the photographs contained in this chapter. The authors also thank Drs. J. Gruber, J. C. Cokendolpher, J. Martens, B. Schottler, N. Tsurusaki, P. Jäger, W. Lourenço, C. Komposch, P. Gnaspini, R. H. Willemart, and D. Ubick for their valuable help in gathering the highly scattered information and also for kindly sharing unpublished observations. L. E. Acosta is a researcher of CONICET, and G. Machado has a research fellowship from FAPESP (02/0381-00).

CHAPTER

9

Natural Enemies James C. Cokendolpher and Plamen G. Mitov

A

lthough this chapter is titled “Natural Enemies,” it also covers some associations that are neutral or potentially beneficial to Opiliones. Predation, cannibalism, disease-causing pathogens, and many parasites are clearly detrimental to dead or dying Opiliones. It appears that the impact of gregarine parasites and phoretic riders is not life threatening, but they may reduce fitness. Likewise, bacteria, seeds, and spores that are carried by Opiliones (through no special efforts of the transmitted) appear to be neutral except for a reduction in fitness simply by the extra load the animals have to carry or waste energy trying to remove. Only in the cases of some mites, cyanobacteria, algae, and liverworts are mutualistic relationships suggested. In these cases the individuals might receive some assistance from the mites as they apparently groom the host, or the hosts might acquire a camouflage from the green coloring of the chloroplasts. We know little about the associations of Opiliones. Although there are approximately 6,000 described species in the order, there are fewer than 100 reported species of pathogens and parasites, only slightly over 300 species of predators, and only about two dozen phoretic/endozoic/epizoic associations recorded worldwide. Part of the problem is that the simple observation and reporting of such associations are not considered of high scholarly value, and therefore many events go unrecorded. Furthermore, most pathologists and parasitologists cannot identify Opiliones even to order, and harvestmen researchers likewise cannot generally identify predators, parasites, or pathogens except in very general terms. The number of associations is also underreported because of the difficulty in observing these activities. Most harvestmen are nocturnal or cryptic, and therefore their struggle for life goes essentially undetected by humans. The beginning points for the study of harvestman enemies are two classics that came out in the same year (Bristowe, 1949; Sankey, 1949b). Since that time numerous reports have been published, but no updated reviews appeared until the mid1990s (Cokendolpher, 1993; Mitov, 1995). In the following discussions specific de339

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tails will be brief. Lists (Tables 9.1–9.3) are supplied that detail species records and pertinent literature.

PARASITES AND PARASITOIDS Parasitism is a common way of life, since over half the known animals of the planet are parasites (Meeûs & Renaud, 2002). It is no surprise, then, that harvestmen are attacked by numerous species of parasites and parasitoids (Figure 9.1). Few parasitologists are trained as arachnologists, and therefore many hosts are not identified beyond class or order in the literature. Some records of harvestmen are lost in the more general lists as “Arachnida,” whereas some records for long-legged spiders are misidentified as Opiliones (Cokendolpher, 1993). Similarly, arachnologists who discover parasites often do not identify the agent beyond “gregarine” or “nematode.” Generally, the parasite, if retained, is improperly preserved (wrong fixative or stage of development) for further identification (for instructions see Chapter 15). Because of the lack of good taxonomic characters in some groups (e.g., Microsporida and juveniles of Mermithidae), collective groups have been named and are used in Table 9.1. Such groups or genera often include species that probably are not related. This group name is used simply for “taxonomic convenience” and includes species not readily placed in known genera (possibly because a particular life stage is unknown) and species incertae sedis. Although most parasites are not fatal in Opiliones, all the nematode parasites and insect parasitoids will kill the harvestman host. In the few cases of pompilid wasps attacking Opiliones, it is not certain if it was parasitism, predation, or mistaken identity. The wasps were observed attacking harvestmen, but observations of feeding or nest provisioning were not recorded (Evans, 1948). Most adult pompilids feed almost exclusively on nectar sources (Evans, 1953). Only a few species have also been observed feeding on hemolymph from captured spiders, but not harvestmen. Another general characteristic of this group is that all known species feed their larvae exclusively with spiders (Evans, 1953). This suggests that wasps might mistakenly attack harvestmen as a spider and later reject the prey. This still might result in the death of the harvestmen, but such attacks would be very infrequent. The two most commonly reported parasites are the endoparasitic gregarines and the ectoparasitic mites (Table 9.1). Both of these are large, easily observed parasites, and for that reason they are probably more often detected than the smaller endoparasitic species. The frequency of occurrence of both appears to increase with the age and size of the harvestman host. It is not clear why this increase occurs. Perhaps it is related to a longer period of exposure (including the probability of reinfesting oneself) or the higher biomass availability, or both. Like many topics related to harvestman biology, this is an area that needs detailed study. In the case of the gregarines, adult parasites (Figures 9.1A,B) pass gametocytes in the harvestmen’s feces (Figure 9.1C), which dehisce and release many thousands of infective oocysts. The oocysts are ingested by harvestmen and start the cycle over

B

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D

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Figure 9.1. Parasites of Opiliones. (A–C) Undetermined gregarine parasite from the sclerosomatid harvestman Leiobunum nigripes. (A) Ventral view of dissected harvestman showing large trophozoites/sporonts in the abdomen (sternites are removed). (B) Two gametocysts in feces of harvestman. (C) Closeup of trophozoite (photos: J. C. Cokendolpher). (D) Immature mermithid parasite emerging from the abdomen of the phalangiid Phalangium opilio (photo: G. Poinar). (E) The nemastomatid Paranemastoma radewi with transparent, jellylike masses flowing from the mouth and anus; masses active with variety of saprophage nematodes (photo: P. G. Mitov). (F) Corpse of Phalangium opilio (Phalangiidae) that was killed by the nematode Steinernema carpocapsae. Note developing nematodes adjacent to the opened body (photo: G. Poinar). (G) Leiobunum politum (Sclerosomatidae) with immature, parasitic Leptus mite attached to the abdomen (photo: J. C. Cokendolpher). (H) Adult, free-living Leptus mite that feeds upon the sclerosomatid Leiobunum townsendi as an immature (photo: J. C. Cokendolpher).

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Table 9.1 Parasites and parasitoids of Opiliones Parasite/Parasitoid

Opiliones host

Source

PHYLUM MICROSPORA: CLASS MICROSPOREA, ORDER MICROSPORIDA Microsporidium weiseri

Opilio parietinus

Cokendolpher, 1993

Carinostoma ornatum, Dicranolasma scabrum, Equitius doriae, Graecophalangium atticum, Lacinius dentiger, L. ephippiatus, L. horridus, L. insularis, Leiobunum globosum, L. manubriatum, L. nigripes, L. politum, L. rumelicum, Lophopilio palpinalis, Metaplatybunus grandissimus, Mitopus morio, Odiellus lendli, O. pictus, Opilio dinaricus, O. ruzickai, O. saxatilis, Paranemastoma aurigerum ryla, P. radewi, Phalangium opilio, Pyza bosnica, Rilaena balcanica, R. cf. serbica, R. serbica, Trogulus tricarinatus, Zachaeus anatolicus, and Z. crista

Cokendolpher, 1993, pers. obs.; Gruber, 1993; Mitov, 1993, 2000a,b, 2003, 2004, pers. obs.; Mitov & Stoyanov, 2004

Actinocephalus megabuni

Megabunus diadema

Cokendolpher, 1993

Anthorhynchus longispora

Leiobunum rotundum, Mitopus morio, Opilio parietinus, and Platybunus bucephalus

Cokendolpher, 1993

Anthorhynchus sophiae

Lacinius ephippiatus, Leiobunum blackwalli, L. rotundum, Mitopus morio, Oligolophus tridens, Phalangium opilio, and Rilaena triangularis

Cokendolpher, 1993

Arachnocystis arachnoidea

Oppalnia sp.

Cokendolpher, 1993

Contospora opalniae

Oppalnia sp.

Cokendolpher, 1993

Cosmetophilus vonones

Vonones sayi

Cokendolpher, 1993

Doliospora repelini

Leiobunum rotundum, Megabunus diadema, Mitopus morio, Oligolophus tridens, Opilio parietinus, Phalangium opilio, and Platybunus bucephalus

Cokendolpher, 1993

Doliospora troguli

Trogulus tricarinatus

Cokendolpher, 1993

Echinoocysta phalangii

Oppalnia sp.

Cokendolpher, 1993

Sciadiophora sp.

Leuronychus pacificus1

Clopton, 2003

Sciadiophora caudata

Phalangiidae, Mitopus morio, Odiellus spinosus, and Phalangium opilio

Cokendolpher, 1993

Sciadiophora claviformis

Mitopus sp.

Cokendolpher, 1993

Sciadiophora fissidens

Phalangiidae, Lophopilio palpinalis, Phalangium “crassum,” and P. opilio

Cokendolpher, 1993

Sciadiophora gagrellula

Gagrellula saddlana

Cokendolpher, 1993

Sciadiophora geronowitschi

Phalangium opilio

Cokendolpher, 1993

PHYLUM APICOMPLEXA: CLASS SPOROZOASIDA Undetermined gregarine (Figures 9.1A–C)

CLASS SPOROZOASIDA, ORDER EUGREGARINORIDA

Natural Enemies

Parasite/Parasitoid Sciadiophora phalangii

Opiliones host

343

Source

Lacinius dentiger, Leiobunum rotundum, Mitopus morio, Opilio parietinus, Phalangium opilio, Phalangium sp., Platybunus bucephalus, P. pinetorum, and Rilaena triangularis

Cokendolpher, 1993

Phalangium opilio

Cokendolpher, 1993

Brachylecithum sp.

Phalangium opilio

Cokendolpher, 1993

Unidentified larval fluke

Phalangium opilio

Cokendolpher, 1993

Synthetonychiidae and/or Triaenonychidae, Rilaena triangularis, and Siro minutus

Cokendolpher, 1993; Karaman, 1993

Heterorhabditis bacteriophora

Phalangium opilio

Cokendolpher, 1993

“Rhabditid” nematodes

Lacinius horridus, Paranemastoma radewi, and Phalangium opilio

Cokendolpher, 1993; Mitov, 2000b

Steinernema carpocapsae (Figure 9.1F)

Phalangium opilio

Cokendolpher, 1993

Undetermined/Agamomermis (Figure 9.1D)

Phalangiidae, Gonyleptes fragilis, Lacinius dentiger, L. ephippiatus, L. horridus, Leiobunum globosum, L. manubriatum, Lophopilio palpinalis, Mitopus morio, Opilio parietinus, Paecilaemana quadripunctata, Paranemastoma radewi, Phalangium opilio, Protolophus sp., Rilaena balcanica, R. cf. serbica, Thrasychirus sp., Togwoteeus biceps, and Zachaeus crista

Cokendolpher, 1993; Mitov, 2000b; Poinar et al., 2000

Agamomermis phalangii

Phalangium opilio

Cokendolpher, 1993

Agamomermis truncatula

Opilio sp. and Phalangium opilio

Cokendolpher 1993; Poinar et al., 2000

Agamomermis “incerta”

Mitopus morio

Cokendolpher, 1993

PHYLUM PLATYHELMINTHES: CLASS CESTODA, ORDER CYCLOPHYLLIDEA Pseudhymenolepis redonica CLASS TREMATODA, ORDER DIGENEA

PHYLUM NEMATODA Unspecified nematodes

CLASS SECERNENTIA, ORDER RHABDITIDA

CLASS ADENOPHOREA, ORDER MERMITHIDA

(Continued)

344

Natural Enemies

Table 9.1 Continued Parasite/Parasitoid

Opiliones host

Source

PHYLUM ARTHROPODA: CLASS ARACHNIDA, ORDER ACARI Allothrombium chanaanense, A. fuliginosum, and Allothrombium sp.

Opiliones

Raykov & Rimskiy-Korsakov, 1948; Cokendolpher, 1993

Allothrombium neapolitum

Phalangium sp. and Zachaeus crista

Cokendolpher, 1993

Charletonia enghoffi

Bunochelis canariana

Cokendolpher, 1993

Charletonia southcotti

Metagagrella tenuipes

Cokendolpher, 1993

Erythraeidae

Leiobunum blackwalli, L. rotundum, Mitopus morio, Nelima silvatica, Oligolophus hanseni, O. tridens, Opilio parietinus, Paroligolophus agrestis, Phalangium opilio, and Rilaena triangularis

Gabrys, 1991; Cokendolpher, 1993

Leptus beroni

Lophopilio palpinalis, Megabunus diadema, Mitopus morio, Oligolophus hanseni, Opilio canestrinii, O. ruzickai, Opilio sp., Phalangium opilio, and Rilaena triangularis

Fain, 1991; Cokendolpher, 1993; Fain & D’Amico, 1997

Leptus bicristatus, L. jocquei, L. polythrix, and L. puylaerti

Cristina lettowi

Cokendolpher, 1993

Leptus gagrellae

Gagrella sp.

Cokendolpher, 1993

Leptus gyas

Gyas titanus

Fain & D’Amico, 1997

Leptus hidakai

Opilio pentaspinulatus

Cokendolpher, 1993

Leptus ignotus

Opiliones and Phalangium opilio

Haitlinger, 1990; Fain & D’Amico, 1997

Leptus indianensis

Leiobunum aldrichi, L. calcar, L. formosum, L. nigripes, Leiobunum sp., L. speciosum, and L. ventricosum

Cokendolpher, 1993; McAloon & Durden, 2000

Leptus kalaallus

Mitopus morio

Cokendolpher, 1993

Leptus lomani

Sadocus funestus

Cokendolpher, 1993

Leptus nearcticus

Leiobunum aldrichi, L. nigripes, and L. vittatum

Cokendolpher, 1993

Leptus oudemansi

Cynorta sp.

Cokendolpher, 1993

Leptus “phalangii”

Mitopus morio, Oligolophus tridens, and Platybunus bucephalus

Dahl et al., 1935; Stadler & Schenkel, 1940; Pfeifer, 1956; Gabrys, 1991

Leptus phuketicus

Gagrellula niveata and Gagrellula sp.

Southcott, 1994

Leptus stieglmayri

Opiliones

Cokendolpher, 1993

Leptus spp. (Figures 9.1G,H)

Cynorta roeweri, Dicranolasma scabrum, Egaenus convexus, Eumesosoma roeweri, Eumesosoma? sp., Eurybunus sp., Krusa sp., Lacinius ephippiatus, Leiobunum aldrichi, L. aff. depressum, L. flavum, L. montanum montanum, L. nigripes, L. rotundum,

MacKay et al., 1992; Cokendolpher, 1993, pers. obs.; Gruber, 1993; Guffey, 1998; Prieto Trueba & Bauzá Ferré, 1999; Toft, 2004;

Natural Enemies

Parasite/Parasitoid

Opiliones host L. politum, Leiobunum spp., L. townsendi, L. vittatum, Lophopilio palpinalis, Marthana nigerrima, Mitopus morio, Odiellus pictus, Oligolophus tridens, Opilio parietinus, O. ruzickai, Paroligolophus agrestis, Phalangium opilio, Phalangium sp., Platybunus bucephalus, Protolophus singularis, Rilaena triangulares, Togwoteeus biceps, and Trachyrhinus marmoratus

345

Source D. Palmer, pers. obs.

New genus near Leptus

Acanthoprocta pustulata, Eubalta meridionalis, Metagyndes pulchella, Thrasychirus dentichelis, and T. modestus

Cokendolpher, 1993

Trombiculidae

Gagrella alba, G. curvispina, G. formosae, G. sexmaculata, and Metamarthana fusca

Dankittipakul & Sonthichai, 2002

Trombidium hungarium

Egaenus convexus

Cokendolpher, 1993

Trombidium sp.

Nelima sp.

Cokendolpher, 1993

Undetermined mites

Synthetonychiidae and/or Triaenonychidae, Equitius doriae, Gagrellopsis nodulifera, Globipes sp., Goniosoma spp., G. spelaeum, Lacinius dentiger, L. ephippiatus, L. horridus, Leiobunum townsendi, L. ventricosum, Lophopilio palpinalis, Mitopus morio, Nelima paessleri, Odiellus lendli, Opilio dinaricus, O. ruzickai, Pachyloidellus goliath, Paranemastoma aurigerum ryla, P. radewi, Phalangium opilio, Prionostemma panama, Pyza bosnica, Rilaena cf. serbica, Trachyrhinus rectipalpus, Vonones sayi, Zachaeus anatolicus, Z. crista, and Z. hebraicus

Acosta et al., 1993; Cokendolpher, 1993; Gnaspini, 1996; Mitov, 2000b

Ceratopogonidae

Gagrellula ferruginea and Nelima nigricoxa

Cokendolpher, 1993

Cyclorrhapha larvae

Discocyrtus invalidus

Cokendolpher, 1993

Lasiohelea opilionivora

Sclerosomatidae

Lane, 1947

Phoridae

Iporangaia pustulosa

G. Machado, pers. comm.

Phoridae?

Goniosoma spp. and Goniosoma spelaeum

Gnaspini, 1996

Undetermined larvae

Acutisoma longipes

Machado et al., 2000

Anoplius marginatus

Odiellus pictus

Cokendolpher, 1993

Chalcididae

Synthetonychiidae and/or Triaenonychidae

Cokendolpher, 1993

CLASS INSECTA, ORDER DIPTERA

CLASS INSECTA, ORDER HYMENOPTERA

Original source citations not listed here are found in Cokendolpher (1993). 1. This host genus does not occur in the region reported. There is no doubt that it is misidentified.

346

Natural Enemies

again. It is likely that harvestmen reinfect themselves by defecating at or near areas that they frequent for drinking, eating, or resting, although this has not actually been observed. The oocysts are small enough that harvestmen could pick them up when moving through the environment and ingest them during grooming. Likewise, they could be exposed to the oocysts if they stop to inspect feces of other harvestmen. One of us (J. C. Cokendolpher) unsuccessfully attempted to infect some harvestmen by placing active oocysts in the water offered to captive harvestmen. Although some authors (Tsurusaki, 1986; Mitov, 2000b) have recorded the number of gregarines in wild populations over time, the lack of good characters to identify the gregarines reduced the amount of information that could be obtained from these reports. It is not known if these are all members of a single species or changes in numbers of two or more species over time. The lack of good identification characters also keeps us from knowing the extent of distribution of these parasites geographically, as well as their host species. Some of the records in the literature are suspect because not all the life stages of the parasites are known and it is likely that more than one species could be lumped under a single parasite’s name. Most of the harvestman species found on Mt. Vitosha (Bulgaria) were highly parasitized by gregarines in the autumn (Mitov, 2000b). Tsurusaki (1986) found similar infestations in Leiobunum spp. (Sclerosomatidae) in Japan. Some specimens of the phalangiids Rilaena cf. serbica, Lacinius horridus, and Mitopus morio from Mt. Vitosha were parasitized by both gregarines and mermithids. The mermithids were found during April to November, mostly on the open grassy habitats, which are in contact with water. The placement near water probably facilitates the parasitism by the mermithids. Mermithids can emerge from their host into damp situations, where they mature and deposit eggs. The life cycle of mermithids that attack harvestmen is unknown. It is possible that most, if not all, have an indirect life cycle like that recorded in spiders (Poinar & Early, 1990). In this case the infective egg of the mermithid would be ingested by a paratenic host that would later be eaten by a harvestman. The parasite would be ingested along with the paratenic host. In the known case of spiders, the paratenic hosts are caddis flies and mayflies—items that have already been recorded in the diet of harvestmen (see Chapter 8). Mermithids with a direct life cycle enter their hosts via direct penetration of the cuticle. The indirect type of development would bypass cuticle penetration and would allow the parasite access to the host hemocoel. The nematode parasites are split between the mermithids that presumably kill their host upon emerging through the cuticle to molt to maturity (Figure 9.1D) and the rhabditid nematodes (Figure 9.1E) that inject their host with pathogenic bacteria that kill the harvestman. Other rhabditid nematodes are saprophagic and can be seen on harvestman eggs (Mitov, 2000b), as well as on recently deceased individuals (Figure 9.1F). These latter nematodes presumably do not harm the eggs. The literature data concerning other protozoans and helminthes parasitizing harvestmen are very scarce (Table 9.1). Only a single blood-borne microsporidium

Natural Enemies

(Microsporidium weiseri) has been observed (Silhavy, 1960) in Opiliones, and little is known about it. Harvestmen are recorded to be intermediate hosts of a few Platyhelminthes, but in no case are they the primary host of these flukes or tapeworms. Mites known to be parasitic on harvestmen belong to the families Trombiculidae, Thrombidiidae, and Erythraeidae. Only the larval forms are parasitic (Figure 9.1G), whereas the nymphs and adults are predaceous on small insects. Because the larval and postlarval stages of these three families are heteromorphic (do not resemble each other; see Figures 9.1G,H), systematists have long used different scientific names for each (Southcott, 1991). Only after the larval and postlarval stages are associated by rearing can any meaningful classifications be constructed. Erythraeid mites deposit a cone of cementing material at the attachment site that, along with their inserted chelicerae, forms a tight anchorage (Åbro, 1988). The attached larva can then suck hemolymph and tissue fluids over a long period of time. Parasitic mites appear to have a preference for certain regions of the body and legs of harvestmen (McAloon & Durden, 2000; Mitov, 2000b). It is evident that most of the mites are attached to the leg femora, patella and tibiae, ocularium, and dorsal metasoma. The coxae, trochanters, metatarsi, tarsi, chelicerae, and ventral metasoma bear the fewest larvae. None were found on the pedipalps. The latter fact, as well as the sparse coverage of metatarsi and tarsi, may be due to the walking mechanism of harvestmen (Kästner, 1931a), or to the possibility that these parts are easily reached and readily cleaned by the animals themselves. Ultrastructural studies by McAloon and Durden (2000) also suggest that this attachment-site selection could be due to integumentary morphology. Åbro (1988) stated that no violent defense on the part of the harvestman had been recorded. Observation of living harvestmen with mites revealed no rubbing or twitching that would indicate that the mites were causing any distress (J. C. Cokendolpher, pers. obs.). A relatively small number of harvestmen in a population will be parasitized by most of the mites. This frequency distribution was observed by McAloon and Durden (2000) in the USA and by Mitov (2000b) in Bulgaria. Multiple attached mites per harvestman were not uncommon: 709 mites on 500 harvestmen in the USA and 813 mites on 339 harvestmen in Bulgaria. In several cases the load of parasites per harvestman was extraordinary. Ten to 14 mites per Leiobunum formosum were recorded on 9 out of 500 infested harvestmen in the USA study. Among the most heavily affected specimens in Bulgaria were the phalangiids M. morio, with 21 (only on legs), and Zachaeus crista, with the highest number (32) of mite larvae found on a single host specimen (on legs and body). It is uncertain if this results from a potential host being exposed to a large number of host-seeking larvae recently hatched from an egg mass or if a previously parasitized harvestman is physically or behaviorally more susceptible to multiple attacks. Flies of the family Ceratopogonidae are blood feeders. These flies have occasionally been seen feeding on harvestmen. This is an association that is probably overlooked by most observers because of the small size of the flies. Phoridae flies have

347

348

Natural Enemies

been seen attacking Brazilian Opiliones (Gnaspini, 1996; G. Machado, pers. comm.). Members of the family Phoridae are diverse in their feeding habits, but some species are known to be parasitoids. These parasitoids lay an egg on the body of the host, which hatches and develops internally in the host for several instars.

PATHOGENS There are relatively few pathogens known from Opiliones, and most of these are recorded only in one or limited numbers of incidents (Figure 9.2). The majority of records are of pathogenic fungi—in many cases attacking eggs (Goodnight & Goodnight, 1976; Mora, 1987, 1990; Ramires & Giaretta, 1994; Machado & Oliveira, 1998, 2002; Elpino-Campos et al., 2001; Machado, 2002; Figures 9.2C,D). From the class Hyphomycetes, there are records of Hymenostilbe verrucosa infecting phalangiids (Mains, 1950; Leatherdale, 1970), Metarrhizium anisopliae in Megalopsalis tumida (Meyer-Rochow & Liddle, 1988), Nomuraea atypicola in Leiobunum vittatum (Greenstone et al., 1988), and Engyodonthium aranearum infecting several species of Opiliones (Ciccarone & Campadelli, 1998). Gonyleptids and manaosbiids are attacked by pathogenic fungi of the class Pyrenomycetes that may cause the death of the individuals (Möller, 1901; Koval, 1974; Figure 9.2B). Equally lethal is the zygomycete Pandora phalangicida, which attacks individuals of Phalangium opilio (Lagerheim, 1898; Ellis, 1956; Leatherdale, 1958, 1970). One species of fungus, though, Entomophaga batkoi, is known to cause considerable numbers of deaths in European harvestmen. An epizootic (temporary increase in the incidence of infections) was observed during late summer by Balazy (1978). Keller (1987) reported that this species of fungus was rather common from late July to the middle of September and often caused epizootics along the borders of forests and hedges. An infected harvestman will crawl up in the vegetation and die while hanging onto a blade of grass or other plant part (Figure 9.2A). Similar behavior has been noted in some insects, such as flies, grasshoppers, wasps, and caterpillars, which become fixed to an aboveground substrate when infected by other entopathogenic fungi (Keller, 1987). No doubt pathogens are more numerous and widespread. Because most opilionologists do not recognize diseased harvestmen, it is likely that most cases go undetected. Only two species of pathogenic bacteria (Xenorhabdus luminescens and X. nematophilus) have been recorded for harvestmen, both attacking the phalangiid Phalangium opilio (Poinar & Thomas, 1985). Additionally, no rickettsial or viral disease has been diagnosed in harvestmen (Morel, 1978), but this may be more a case of no one looking than an absence. Viral and rickettsial diseases have been shown to occur in as high as 5%–10% of a natural population in nonacarine arachnids studied (Legendre & Morel, 1980; J. Haupt, 2000). Cory et al. (1988) recovered active Panolis nuclear polyhedrosis virus from the feces of harvestmen, but no disease in the harvestman was noted.

Natural Enemies

A

C

B

D

Figure 9.2. Pathogens of Opiliones: (A) Diseased Oligolophus tridens (Phalangiidae) hanging from a grass blade. Harvestmen infected with Entomophaga batkoi fungi clasp the upper parts of plants where they die (modified from Keller, 1987). Scale bar = 5 mm. (B) Corpse of a manaosbiid (?) harvestman from Guyana covered by the pathogenic fungus Torrubiella gonylepticida (photo: J. Spatafora). Scale bar = 5 mm. (C) Corpse of the gonyleptid harvestman Acutisoma discolor covered by an unidentified fungus (photo: G. Machado). Saprophytic and pathogenic fungi are difficult to separate by sight alone. Scale bar = 10 mm. (D) Egg batch of the gonyleptid harvestman Acutisoma proximum attacked by fungi (photo: B. A. Buzatto). Scale bar = 10 mm.

349

350

Natural Enemies

PREDATORS Predation of harvestmen is complex in that the age and reproductive state of both the predator and prey have to be considered. Because of space limitation, we have only indicated this in Tables 9.2 and 9.3 as regards Opiliones: eggs versus freemoving individuals. The age of the harvestman is important primarily because of the size, mobility, and thickness of the cuticle of the harvestman. Some predators are able to successfully predate only upon smaller, softer-bodied harvestmen, whereas others only eat larger, more active prey. With some predators, juvenile harvestmen escape notice entirely, while the adults are easily detected and fed upon. The time and site of activity of the harvestman is also important. Predators that feed primarily by sight (e.g., birds and lizards) take more prey that is larger, diurnal, and more active, whereas predators that feed in the litter or soil (such as insectivorous mammals and some marsupials) often take smaller, less mobile prey that they can smell or hear moving. Other small generalist predators, such as ants, spiders, and assassin bugs (Figure 9.3), will take whatever they can catch and hold. The age of the predator is important because smaller predators can only take small prey. Likewise, the reproductive state of the predator can alter the number of prey taken. Vertebrates have been documented to alter the number of harvestman prey they take during different seasons. Part of this may be due to the increased percentage of harvestman prey available during certain seasons, but in other cases it appears to be related to the reproductive state of the predator or availability of other foods. Examples are some of the birds, which take increased numbers of harvestmen when feeding their young. This is especially true of granivorous birds that lack a food-storage organ, such as a crop. These birds feed large quantities of arthropods (including harvestmen) to the nestlings (MacMillan & Pollock, 1985, and citations therein). Locality also appears to be important, as demonstrated by the toad Bufo marinus (Bufonidae). In its native habitat in Puerto Rico, this species takes an insignificant number of harvestmen (Leonard, 1933), whereas in an introduced population in Queensland, Australia, it feeds almost exclusively on harvestmen (R. J. Raven, pers. comm.). Individual preferences or perhaps opportunity also result in uneven captures of harvestmen within a population of predators. Examination of guts of 67 Cuban tree frogs, Osteopilus septentrionalis (Hylidae), from Tortola, British Virgin Islands, West Indies, revealed that 6 frogs had eaten Metacynortoides obscurus (Cosmetidae): 2 ate a single harvestman, 3 ate 2 harvestmen, and 1 individual ate 9 harvestmen (J. C. Cokendolpher, pers. obs.). These data certainly recommend larger sample sizes when conducting experiments with predators/prey. Some predators will drop a harvestman when exocrine gland chemicals are first emitted (see Chapter 10). This initial response has been recorded in the literature as “none feeding.” However, other studies have revealed in the case of some birds, mammals, and ants that they will repeatedly attack the harvestman until it

Natural Enemies

351

Table 9.2 Vertebrate predators of Opiliones Predator

Opiliones prey

Source

PHYLUM CHORDATA: CLASS OSTEICHTHYES, ORDER CYPRINIFORMES Leuciscus cephalus

Phalangium opilio

Bristowe, 1949

Opiliones, Mitopus morio, and Phalangium opilio

Bristowe, 1949; Thomas, 1962

Bombina bombina

Opiliones

Barusˇ et al., 1992a

Bufo achalensis

Pachyloidellus goliath

Acosta et al., 1995

Bufo asper, B. cognatus, B. compactilis speciosus, B. marinus, B. terrestris americanus, B. viridis, B. woodhousei fowleri, B. woodhousei woodhousei, and Bufo spp.

Opiliones

Leonard, 1933; Smith & Bragg, 1949; Berry, 1970; R. D. Clarke, 1974; Obrtel, 1976; Tomov, 1990; Yiyit et al., 1999; R. J. Raven, pers. comm.

Bufo hemiophrys

Phalangium opilio

Holmberg, 1970

Bufo ictericus (Figure 9.4A)

Acutisoma proximum

B. A. Buzatto, pers. comm.

Hyla cinerea cinerea

Opiliones

Kilby, 1945

Leptodactylus ocellatus

Opiliones (Laniatores)

A. A. Giaretta, pers. comm.

Osteopilus septentrionalis

Metacynortoides obscurus

New data

Pseudacris triseriata maculata

Phalangium opilio

Holmberg, 1970

Rana clamitans

Opiliones

Jenssen & Klimstra, 1966

Rana graeca

Lacinius dentiger, L. horridus, Paranemastoma sp., and Trogulus sp.

Beshkov, 1970

Rana pipiens

Opiliones, Phalangium opilio, and Togwoteeus biceps

Moore & Strickland, 1954; Holmberg, 1970

Rana pipiens sphenocephala

Eumesosoma nigrum, Leiobunum aurugineum, Leiobunum sp., and Vonones sayi

Kilby, 1945

Rana ridibunda and Rana spp.

Opiliones

Hristova, 1962; Obrtel, 1976

Rana sylvatica

Leiobunum calcar, Odiellus pictus, and Phalangium opilio

Holmberg, 1970

Rana temporaria and/or Bufo bufo

Anelasmocephalus cambridgei, Lacinius ephippiatus, Leiobunum blackwalli, L. rotundum, Mitopus morio, Nemastoma chrysomelas, Nemastoma lugubre, Paroligolophus agrestis, Phalangium opilio, and Rilaena triangularis

Bristowe, 1949; Houston, 1973

CLASS OSTEICHTHYES, ORDER SALMONIFORMES Salmo salar and S. trutta

CLASS LISSAMPHIBIA, ORDER ANURA

(Continued)

352

Natural Enemies

Table 9.2 Continued Predator

Opiliones prey

Source

CLASS LISSAMPHIBIA, ORDER CAUDATA Ambystoma tigrinum

Opilio parietinus and Phalangium opilio

Holmberg, 1970

Aneides ferreus

Opiliones

Whitaker et al., 1986; Petranka, 1998

Eurycea longicauda

Opiliones

Anderson & Martino, 1967; Petranka, 1998

Eurycea lucifuga

Opiliones, Bishopella laciniosa, Leiobunum sp., and Phalangodes armata

Hutchison, 1958; Peck, 1974; Peck & Richardson, 1976; Petranka, 1998

Hydromantes italicus gormani

Ischyropsalis apuana and Trogulus coriziformis

Bruno, 1973

Plethodon cinereus, P. cinereus cinereus, P. dunni, P. glutinosus, P. idahoensis, P. jordani, P. oconaluftee, P. vehiculum, and P. wehrlei

Opiliones

Smallwood, 1928; Pope, 1950; Davidson, 1956; Dumas, 1956; Brandon, 1965; Edgar, 1971; Powders & Tietjen, 1974; Hall, 1976; Wilson & Larsen, 1988; Petranka, 1998

Salamandra atra

Platybunus pinetorum and Ischyropsalis hellwigii

Klewen, 1988

Salamandra salamandra

Nemastomatidae and Trogulidae

Beshkov & Tsonchev, 1963

Salamandra s. salamandra

Opilio parietinus

Klewen, 1988

Ablepharus kitaibelii

Opiliones

Barusˇ et al., 1992b

Alopoglossus angulatus

Opiliones

Vitt & Caldwell, 2003

Ameiva ameiva

Opiliones

Vitt & Caldwell, 2003

Basiliscus basiliscus

Opiliones

Barden, 1943

Cnemidophorus sacki and C. tessellatus

Trachyrhinus rectipalpus

Milstead, 1958

Gonatodes hasemani and G. humeralis

Opiliones

Vitt & Caldwell, 2003

Lacerta muralis, Lacerta taurica, and Lacerta sp.

Opiliones

Bristowe, 1949; Angelov et al., 1972a, c

Lacerta muralis muralis

Pyza bosnica

Mitov, 1995

Lacerta viridis

Opiliones and Zachaeus crista

Angelov et al., 1972b; P. G. Mitov, pers. obs.

Lacerta vivipara

Opiliones and Mitopus morio

Darevskiy, 1953; Avery, 1966; Sirbu, 1977; Barusˇ et al., 1992b

Lacerta vivipara vivipara

Phalangiidae, Lacinius horridus, Phalangium opilio, and Rilaena triangularis

Mitov, 1995

Ophisaurus apodus

Opiliones1

Yadgarov, 1974

Prionodactylus eigenmanni

Opiliones

Vitt et al., 1998

Stellio lehmanni

Phalangiidae (?)

Petrochenko, 1992

Teratoscincus scincus

Opiliones

Yadgarov, 1977

CLASS REPTILLIA, ORDER SQUAMATA

Natural Enemies

Predator

Opiliones prey

353

Source

CLASS MAMMALIA, ORDER CARNIVORA Cerdocyon thous

Opiliones (Laniatores)

Facure, 1996

Meles meles

Mitopus morio, Odiellus spinosus, Paroligolophus agrestis, and Phalangium opilio

Sankey, 1949b

Mephites mephites

Phalangium opilio

Holmberg, 1970

Vulpes vulpes

Phalangium opilio

Sankey, 1949b

CLASS MAMMALIA, ORDER CHIROPTERA Myotis bechsteini

Phalangiidae

Wolz, 1992

Myotis emarginatus, M. nattereri, and M. thysanodes

Opiliones

Whitaker et al., 1977; Bauerová, 1986; Bauerová & Cˇerveny´, 1986

CLASS MAMMALIA, ORDER DIDELPHIMORPHIA Didelphis aurita

Opiliones

Cáceres & Monteiro-Filho, 2001

Philander frenata

Opiliones

Santori et al., 1997

Philander opossum (Figure 9.4B)

Acutisoma longipes and Goniosoma spelaeum

Gnaspini-Netto, 1993; Gnaspini, 1996; Pellegatti-Franco & Gnaspini, 1996; Machado et al., 2000

Crocidura suaveolens

Opiliones

Burda & Bauerová, 1985; Bauerová, 1988

Erinaceus europaeus

Leiobunum blackwalli, L. rotundum, Mitopus morio, Odiellus spinosus, Oligolophus tridens, Opilio parietinus, Paroligolophus agrestis, and Phalangium opilio

Sankey, 1949b

Neomys anomalus, N. fodiens, and N. fodiens bicolor

Opiliones

Churchfield, 1979; Kuvikova, 1985a,b; Churchfield et al., 1991

Solenodon cubanus

Cynorta sp.

Armas, 1987

Sorex alpinus, S. bendirii, S. pacificus, S. sylvaticus, S. trowbridgii, S. vagans, and Sorex spp.

Opiliones

Obrtel, 1976; Whitaker & Maser, 1976; Kuvikova, 1986; Churchfield & Brown, 1987

Sorex araneus

Opiliones, Carinostoma ornatum, Lacinius dentiger, Mitostoma chrysomelas, Nemastoma lugubre, Paroligolophus agrestis, Paranemastoma radewi, and Pyza bosnica

Bristowe, 1949; Rudge, 1968; Pernetta, 1976, 1977; Butterfield et al., 1981; Churchfield, 1982; Bauerová, 1982, 1984; Kuvikova, 1985a; Churchfield et al., 1991; Mitov, 1995

CLASS MAMMALIA, ORDER INSECTIVORA

(Continued)

354

Natural Enemies

Table 9.2 Continued Predator Sorex minutus

Opiliones prey

Source

Opiliones, Paranemastoma sp., and Paranemastoma radewi

Pernetta, 1976; Grainger & Fairley, 1978; Butterfield et al., 1981; Bauerová, 1982, 1984; Kuvikova, 1985a; Churchfield et al., 1991; Mitov, 1995

Apodemus flavicollis

Opiliones, Lacinius sp., Nemastoma sp., Oligolophus sp., and Platybunus sp.

Obrtel, 1973a, 1974, 1976; Obrtel & Holisˇ ová, 1974, 1980, 1983

Apodemus sylvaticus

Opiliones

Obrtel & Holisˇ ová, 1979, 1983

Clethrionomys glareolus

Opiliones

Obrtel, 1973b, 1974, 1976; Holisˇ ová & Obrtel, 1979; Obrtel & Holisˇ ová, 1974, 1983

Mus musculus

Phalangium opilio

Holmberg, 1970

CLASS MAMMALIA, ORDER RODENTIA

Onychomys torridus longicaudus

Opiliones

Horner et al., 1965

Peromyscus leucopus

Eumesosoma roeweri and Sclerobunus robustus robustus

J. C. Cokendolpher, pers. obs.

Opiliones

Cramp et al., 1985

Bonasa umbellus

Opiliones

Stewart, 1956

Colinus virginianus

Opiliones

Bristowe, 1949

Coturnix coturnix

Phalangium sp.

Mihaylov, 1995

Gallus domesticus

Phalangium opilio

Holmberg, 1970; Clark & Gage, 1997

Perdix perdix perdix

Opiliones

Glutz von Blotzheim et al., 1973

Charadrius mongolus

Opiliones

Zlotin, 1968

Cursorius curso

Opiliones

Cramp et al., 1983

Larus canus

Opiliones

Bakke, 1970; Glutz von Blotzheim & Bauer, 1982

Pluvialis apricarius

Opiliones

Andreeva, 1989

Vanellus vanellus

Opiliones

Cramp et al., 1983

Opiliones

McAtee, 1926, 1932; Bristowe, 1949

CLASS AVES, ORDER CORACIIFORMES Merops apiaster CLASS AVES, ORDER GALLIFORMES

CLASS AVES, ORDER CHARADRIIFORMES

CLASS AVES, ORDER CUCULIFORMES Coccyzus americanus and C. erythropthalmus

Natural Enemies

Predator

Opiliones prey

355

Source

CLASS AVES, ORDER GRUIFORMES Porphyrio porphyrio melanotus

Opiliones

Caroll, 1966; Glutz von Blotzheim et al., 1973

Acrocephalus arundinaceus, A. dumetorum, A. palustris, A. schoenobaenus, and A. scirpaceus

Opiliones

Cramp et al., 1992

Alauda arvensis

Opiliones

Cramp et al., 1988

Anthus campestris, A. cervinus, A. spinoletta, and A. trivialis

Opiliones

Cramp et al., 1988; Gajdosˇ & Krisˇ tín, 1997

Anthus pratensis

Opiliones and Mitopus morio

Skar et al., 1975; Hågvar & Østbye, 1976; Cramp et al., 1988

Certhia brachydactyla

Opiliones

Cramp et al., 1993

Certhia familiaris

Opiliones and Platybunus bucephalus

Krisˇ tín, 1992; Cramp et al., 1993; Krisˇ tín & Baumann, 1996; Gajdosˇ & Krisˇ tín, 1997; Szentkirályi & Krisˇ tín, 2002

Cettia cetti

Opiliones

Cramp et al., 1992

Corvus corone, C. frugilegus, and Corvus monedula

Opiliones and Phalangiidae

Cramp et al., 1994b

Cyanocorax caeruleus

Gonyleptidae

Reinert & Bornschein, 1998

Cyanopica cyanus

Opiliones

Cramp et al., 1994b

Dendroica magnolia

Opiliones

McAtee, 1926

Dolichonyx oryzivorus

Opiliones

Dillery, 1961; Wiens, 1969

Emberiza citronella, E. melanocephala, and E. schoeniclus

Opiliones

S. Simeonov, 1981; Cramp et al., 1994a

Erithacus rubecula

Opiliones and Lacinius ephippiatus

Krisˇ tín, 1992; Krisˇ tín & Baumann, 1996; Gajdosˇ & Krisˇ tín, 1997; Szentkirályi & Krisˇ tin, 2002

Ficedula albicollis

Opiliones, Mitopus sp., Platybunus bucephalus, and Platybunus sp.

Buresˇ , 1986; Krisˇ tín, 1992, 2002; Cramp et al., 1993; Krisˇ tín & Baumann, 1996; Gajdosˇ & Krisˇ tín, 1997; Szentkirályi & Krisˇ tin, 2002

Ficedula hypoleuca

Opiliones and Mitopus morio

Dornbusch, 1981; Sacher & Dornbusch, 1990; Cramp et al., 1993

Ficedula parva

Opiliones

Cramp et al., 1993

Fringilla coelebs and F. montifringilla

Opiliones

Prokofyeva, 1961; Daraktchiev, 1981; Cramp et al., 1994b; Krisˇ tín & Baumann, 1996

CLASS AVES, ORDER PASSERIFORMES

(Continued)

356

Natural Enemies

Table 9.2 Continued Predator

Opiliones prey

Source

Garrulus glandarius

Opiliones and Phalangiidae

Cramp et al., 1994b

Lanius collurio

Opiliones, Phalangiidae, Leiobunum rotundum, and Zachaeus crista

Cramp et al., 1993; Nikolov, 2002

Lanius excubitor, L. minor, and L. senator

Opiliones

Cramp et al., 1993

Locustella fluviatilis and L. naevia

Opiliones

Cramp et al., 1992

Lullula arborea

Opiliones

Cramp et al., 1988

Monticola solitarius

Opiliones

Glutz von Blotzheim & Bauer, 1988a

Montifringilla nivalis

Opiliones

Cramp et al., 1994b

Motacilla alba, M. cinerea, and M. flava

Opiliones

Daraktchiev, 1981; Cramp et al., 1988

Muscicapa striata

Opiliones

Cramp et al., 1993

Nannus hiemalis

Opiliones

McAtee, 1926

Oenanthe finschi, O. hispanica, O. isabellina, and O. oenanthe oenanthe

Opiliones

Belskaja, 1965; Wartmann, 1985; Cramp et al., 1988; Glutz von Blotzheim & Bauer, 1988a; Szentkirályi & Krisˇ tin, 2002

Parus ater and P. caeruleus

Opiliones and Mitopus morio

Sacher & Dornbusch, 1990; Krisˇ tín, 1992; Cramp et al., 1993; Krisˇ tín & Baumann, 1996; Mattes et al., 1996; Gajdosˇ & Krisˇ tín, 1997; Mihál, 1998; Szentkirályi & Krisˇ tin, 2002

Parus major

Opiliones, Mitopus morio, Nemastoma lugubre, and Rilaena triangularis

Betts, 1955; Dornbusch, 1981; Sacher & Dornbusch, 1990; Krisˇ tín, 1992; Cramp et al., 1993; Krisˇ tín & Baumann, 1996; Gajdosˇ & Krisˇ tín, 1997; Szentkirályi & Krisˇ tin, 2002

Passer domesticus

Opiliones, Opilio parietinus, and Phalangium opilio

S. D. Simeonov, 1964; Holmberg, 1970; MacMillan & Pollock, 1985; Ivanov, 1990; Gajdosˇ & Krisˇ tín, 1997

Passer montanus and Passer sp.

Opiliones

Cîrdei, 1958; S. D. Simeonov, 1963; Krisˇ tín, 1988b; Török, 1990; Cramp et al., 1993; Krisˇ tín & Baumann, 1996; Gajdosˇ & Krisˇ tín, 1997; Szentkirályi & Krisˇ tin, 2002

Passerculus sandwichensis

Opiliones and Phalangium opilio

Dillery, 1961; Wiens, 1969; Holmberg, 1970

Pastor roseus

Opiliones2

Dementjev et al., 1954

Penthestes atricapillus

Opiliones

McAtee, 1926

Pheucticus ludovicianus

Leiobunum aldrichi, L. vittatum, and L. calcar

Edgar, 1971

Phoenicurus ochruros

Opiliones and Platybunus bucephalus

Krisˇ tín & Baumann, 1996; Gajdosˇ & Krisˇ tín, 1997

Phoenicurus ochruros gibraltariensis and P. phoenicurus

Opiliones

Cramp et al., 1988; Glutz von Blotzheim & Bauer, 1988a

Natural Enemies

Predator

Opiliones prey

357

Source

Phoenicurus phoenicurus phoenicurus

Opiliones and Mitopus morio

Emmrich, 1975a; Glutz von Blotzheim & Bauer, 1988a; Sacher & Dornbusch, 1990

Phylloscopus borealis and P. trochilus

Opiliones

Cramp et al., 1992

Phylloscopus collybita

Opiliones and Phalangiidae

Krisˇ tín, 1988a, 1991, 1992; Krisˇ tín & Baumann, 1996; Gajdosˇ & Krisˇ tín, 1997; Szentkirályi & Krisˇ tin, 2002

Phylloscopus sibilatrix

Opiliones, Phalangiidae, and Platybunus bucephalus

Krisˇ tín, 1991, 1992; Cramp et al., 1992; Krisˇ tín & Baumann, 1996; Gajdosˇ & Krisˇ tín, 1997; Szentkirályi & Krisˇ tin, 2002

Pica pica

Opiliones, Phalangiidae, Phalangium opilio, and Rilaena triangularis

Petrusenko & Talposh, 1981; Cramp et al., 1994b

Pitangus sulphuratus

Opiliones

Argel-de-Oliveira et al., 1998

Prunella modularis

Opiliones, Phalangiidae, Lacinius ephippiatus, Mitopus morio, Oligolophus tridens, Platybunus bucephalus, and Platybunus spp.

Emmrich, 1975b; Cramp et al., 1988; Krisˇ tín, 1993b; Krisˇ tín & Baumann, 1996; Gajdosˇ & Krisˇ tín, 1997; Szentkirályi & Krisˇ tin, 2002

Prunella modularis modularis

Opiliones, Lacinius ephippiatus, Leiobunum rupestre, Mitopus morio, Oligolophus tridens, Paranemastoma quadripunctatum, and Platybunus bucephalus

Emmrich, 1975b; Tomek, 1988

Pyrrhocorax pyrrhocorax

Opiliones

Cramp et al., 1994b

Regulus ignicapillus

Opiliones and Platybunus sp.

Thaler-Kottek, 1973; Cramp et al., 1992

Regulus regulus and R. teneriffae

Opiliones

Löhrl & Thaler, 1980; Cramp et al., 1992

Remiz pendulinus

Opiliones

Szentkirályi & Krisˇ tin, 2002

Saxicola torquata

Opiliones

Krisˇ tín & Baumann, 1996

Seiurus aurocapillus

Opiliones

McAtee, 1926, 1932

Sitta europea

Opiliones, Phalangiidae, Lacinius ephippiatus, Mitopus morio, Platybunus bucephalus, P. pallidus, P. pinetorum, and Platybunus spp.

Daraktchiev, 1981; Krisˇ tín, 1992, 1993a, 1994; Cramp et al., 1993; Krisˇ tín & Baumann, 1996; Gajdosˇ & Krisˇ tín, 1997; Szentkirályi & Krisˇ tin, 2002

Sturnus roseus, S. unicolor, and S. vulgaris

Opiliones

Cramp et al., 1994b

Sylvia atricapilla, S. borin, S. curruca, S. nisoria, Sylvia sp., and Sylvia undata

Opiliones

Prokofyeva, 1961; Ganya & Zubkov, 1988; Cramp et al., 1992

Sylvia communis

Opiliones, Leiobunum sp., Mitopus sp., and Phalangium sp.

Emmrich, 1973, 1974; Cramp et al., 1992

Tarsiger cyanurus cyanurus

Opiliones

Glutz von Blotzheim & Bauer, 1988a

Tichodroma muraria

Opiliones

Cramp et al., 1993

Toxostoma rufum

Opiliones

McAtee, 1926 (Continued)

358

Natural Enemies

Table 9.2 Continued Predator

Opiliones prey

Source

Troglodytes troglodytes

Opiliones, Lacinius ephippiatus, and Mitopus morio

Prokofyeva, 1961; Sellin, 1969; Dallman, 1987; Cramp et al., 1988; Krisˇ tín, 1992; Krisˇ tín & Baumann, 1996; Gajdosˇ & Krisˇ tín, 1997; Szentkirályi & Krisˇ tin, 2002

Turdus merula and T. philomelos

Opiliones

Daraktchiev, 1981; Török, 1985; Cramp et al., 1988; Glutz von Blotzheim & Bauer, 1988b; Krisˇ tín, 1992; Krisˇ tín & Baumann, 1996; Gajdosˇ & Krisˇ tín, 1997; Szentkirályi & Krisˇ tin, 2002

Turdus pilaris

Opiliones and Phalangiidae

Daraktchiev, 1981; Lübcke & Furrer, 1985; Cramp et al., 1988; Glutz von Blotzheim & Bauer, 1988b

Vermivora chrysoptera

Opiliones

Edgar, 1971

Vireosylva philadelphica

Opiliones

McAtee, 1926

Xanthocephalus xanthocephalus

Opiliones

Orians, 1966

Zoothera sibirica

Opiliones

Moroschenko, 1986; Glutz von Blotzheim & Bauer, 1988b

Dendrocopos syriacus, D. major, and D. medius

Opiliones

Cramp et al., 1985; Szentkirályi & Krisˇ tin, 2002

Dryobates pubescens

Opiliones

McAtee, 1926

Picoides major

Opiliones and Platybunus bucephalus

Krisˇ tín & Baumann, 1996; Gajdosˇ & Krisˇ tín, 1997

Picoides medius, P. minor, P. syriacus, and P. tridactylus

Opiliones

Prokofyeva, 1961; Ruge, 1969; Glutz von Blotzheim & Bauer, 1980; Pechácˇek & Krisˇ tín, 1996; Gajdosˇ & Krisˇ tín, 1997; Mihál, 1998

Picus canus

Opiliones

Daraktchiev, 1981

Crex crex

Opiliones

Glutz von Blotzheim et al., 1973; Cramp et al., 1980

Gallinula chloropus

Opiliones and Lophopilio palpinalis

Cramp et al., 1980

Opiliones

Glutz von Blotzheim & Bauer, 1980; Cramp et al., 1985

CLASS AVES, ORDER PICIFORMES

CLASS AVES, ORDER RALLIFORMES

CLASS AVES, ORDER STRIGIFORMES Otus scops and Otus scops scops

Original source citations for many of the birds are listed in Cramp et al. (1983–1994). 1. Yadgarov (1974) listed arachnids as components of the food of the lizard Ophisaurus apodus—“Scorpionuy,” “Falangi,” “Pauki,” “Kleshi,” which translate to “Scorpiones, Araneae, Acari”—but it is not clear if the name “Falangi” is Opiliones or Solifugae. In older Russian literature on Arachnida “Phalangi” = Solifugae. 2. Dementjev et al. (1954) also listed “phalang” as food of the bird Pastor roseus. This too could possibly refer to Solifugae.

Natural Enemies

359

Table 9.3 Invertebrate predators of Opiliones Predator

Opiliones prey

Source

PHYLUM MOLLUSCA: CLASS GASTROPODA, ORDER STYLOMMATOPHORA Polygyra albolabris

Leiobunum aldrichi

Edgar, 1971

Gonyleptidae

Carbayo et al., 2002; Carbayo & Leal-Zanchet, 2003

Lithobius forficatus

Opiliones, Opilio parietinus, and Paroligolophus agrestis

Sankey, 1949b; Spoek, 1964

Lithobius sp.

Odiellus pictus and Phalangium opilio

Holmberg, 1970

Lithobius vulgaris

Leiobunum aldrichi, L. politum, and L. vittatum

Edgar, 1960; Holmberg, 1970

Opiliones

Barnes, 1968

Achaearanea lunata

Rilaena cf. serbica

P. G. Mitov, pers. obs.

Agelena sp.

Paroligolophus agrestis

Bristowe, 1941

Agelena naevia

Opiliones

Bilsing, 1920

Agelenopsis sp.

Leiobunum vittatum and Togwoteeus biceps

Holmberg, 1970; R. Macías-Ordóñez, pers. comm.

Amaurobius sp.

Dicranolasma scabrum

Gruber, 1993

Aranea cucurbitina

Leiobunum blackwalli

Bristowe, 1941

Araneus diadematus

Leiobunum rotundum and Paranemastoma aurigerum aurigerum

Bristowe, 1941; Mitov, 1995

Argiope argentata

Opiliones and Sclerobunus robustus

Robinson & Robinson, 1970; J. C. Cokendolpher, pers. obs.

Coelotes sp.

Dicranolasma scabrum

Gruber, 1993

Coelotes terrestris

Opiliones, Mitostoma chrysomelas, and Paranemastoma quadripunctatum

Petto, 1990

Corinnidae (Figure 9.3A)

Iporangaia pustulosa

B. A. Buzatto, pers. comm.

Ctenus fasciatus

Acutisoma longipes (eggs and adults) and Goniosoma spelaeum

Gnaspini-Netto, 1993; Gnaspini, 1996; Machado et al., 2000

Ctenus sp. 1

Bourguyia albiornata

Machado & Oliveira, 2002

PHYLUM PLATYHELMINTHES: ORDER TRICLADIDA Cephaloflexa araucariana

PHYLUM ARTHROPODA: CLASS CHILOPODA, ORDER LITHOBIOMORPHA

CLASS DIPLOPODA, ORDER NEMATOPHORA Undetermined species CLASS ARACHNIDA, ORDER ARANEAE

(Continued)

360

Natural Enemies

Table 9.3 Continued Predator

Opiliones prey

Source

Ctenus sp. 2 (Figure 9.3B)

Longiperna zonata

G. Machado, pers. comm.

Enoploctenus cyclothorax

Acutisoma longipes and Discocyrtus sp.

Willemart & Kaneto, 2004; G. Machado, pers. comm.

Gladicosa gulosa

Leiobunum aldrichi, L. politum, and L. vittatum

Holmberg, 1970

Hypochilus gertschi

Leiobunum sp.

Shear, 1969

Latrodectus geometricus (Figure 9.3C)

Opiliones and Cosmetidae

Weed, 1892; J. Warfel, pers. comm.

Latrodectus hesperus

Leiobunum townsendi

J. C. Cokendolpher, pers. obs.

Latrodectus variolus

Nelima elegans

W. Reeves, pers. comm.

Linyphia sp.

Rilaena balcanica

Mitov, 1995

Linyphiidae, Erigonidae

Opiliones

Nentwig, 1980, 1983

Lycosa sp.

Opilio parietinus

Sˇilhavy´, 1956

Meta merianae

Leiobunum blackwalli and Paroligolophus agrestis

Bristowe, 1941

Meta segmentata

Paranemastoma radewi

Mitov, 1995

Metellina merianae

Nelima aladjensis

P. G. Mitov, pers. obs.

Neriene clathrata

Mitostoma gracile

P. G. Mitov, pers. obs.

Pardosa fuscula

Opilio parietinus and Phalangium opilio

Holmberg, 1970

Pardosa groenlandica

Phalangium opilio

Holmberg, 1970

Pardosa mackenziana

Odiellus pictus and Phalangium opilio

Holmberg, 1970

Pardosa modica

Phalangium opilio

Holmberg, 1970

Pholcus phalangioides

Leiobunum blackwalli

Bristowe, 1941; Nentwig, 1983

Pholcus spp.

Mitopus morio and Paranemastoma quadripunctatum

Uhlenhaut, 2001

Phoneutria nigriventer

Bourguyia albiornata

Machado & Oliveira, 2002

Physocyclus enaulus

Leiobunum townsendi

J. C. Cokendolpher, pers. obs.

Pisaura sp.

Leiobunum blackwalli

Bristowe, 1941

Scytodes sp.

Mischonyx cuspidatus

Mestre & Pinto-da-Rocha, 2004

Steatoda bipunctata

Lacinius dentiger and Phalangium opilio

Mitov, 1995, 2000b

Steatoda castanea

Lacinius dentiger, Mitopus morio, and Phalangium opilio

Mitov, 1995

Steatoda sp.

Odiellus lendli and Opilio ruzickai

P. G. Mitov, pers. obs.

Steatoda triangulosa

Phalangium opilio

Mitov, 1995

Tidarren sisyphoides

Opiliones

P. H. Pache, pers. comm.

Tegenaria sp. ( juvs.)

Opilio parietinus

P. G. Mitov, pers. obs.

Tegenaria sp.

Lacinius dentiger, L. horridus, Leiobunum rumelicum, Mitopus morio, Nelima aladjensis, Oligolophus tridens, Opilio ruzickai, Phalangium opilio, and Trogulus tricarinatus

Sankey, 1949b; Mitov, 1995, 1997b, 2000b, pers. obs.

Tegenaria agrestis ( juvs.)

Odiellus lendli

P. G. Mitov, pers. obs.

Tegenaria agrestis

Phalangium opilio

Mitov, 1995, pers. obs.

Natural Enemies

Predator

Opiliones prey

361

Source

Tegenaria atrica

Leiobunum blackwalli

Bristowe, 1941

Tegenaria derhami

Phalangium opilio

Holmberg, 1970

Tegenaria ferruginea

Opiliones, Lacinius dentiger, Opilio ruzickai, Paranemastoma aurigerum aurigerum, and Phalangium opilio

Nentwig, 1983; Mitov, 1995, 2000b

Tegenaria nemorosa

Mitostoma gracile

P. G. Mitov, pers. obs.

Tegenaria silvestris

Mitopus morio and Paranemastoma aurigerum ryla

Mitov, 1995, 2000b

Thanatus imbecillius

Opiliones

Guseinov, 2004

Theridiidae

Opiliones and Mischonyx cuspidatus

Nentwig, 1980; Mestre & Pinto-daRocha, 2004

Theridiidae, Linyphiidae, and Erigonidae

Opiliones

Nentwig, 1980

Theridion pictum

Opiliones

Luczak & Dabrowski-Prot, 1970

Theridion sp.

Phalangium opilio

Mitov, 1995

Theridium frondeum

Phalangium opilio

Holmberg, 1970

Theridium ornatum

Phalangium opilio

Holmberg, 1970

Trechalea keyserlingi

Discocyrtus sp.

G. Machado, pers. comm.

Undetermined species

Opiliones, Bourguyia albiornata, Opilio ruzickai, Paranemastoma aurigerum aurigerum, Phalangium opilio, Siro sp., and Trogulus nepaeformis

Savory, 1928; Stipperger, 1928; Bristowe, 1941, 1949; Crome et al., 1969; Edgar, 1971; Mitov, 1995, 2000b; Machado & Oliveira, 2002

Xysticus bifasciatus

Leiobunum blackwalli

Bristowe, 1941

Xysticus viaticus

Leiobunum rotundum

Bristowe, 1941

Zilla thorelli

Opilio parietinus

P. G. Mitov, pers. obs.

Acanthopachylus aculeatus

Acanthopachylus aculeatus (only eggs)

Capocasale & Bruno-Trezza, 1964

CLASS ARACHNIDA, ORDER OPILIONES

Acutisoma longipes

Acutisoma longipes (only eggs)

Machado & Oliveira, 1998

Acutisoma proximum

Acutisoma proximum (only eggs)

Ramires & Giaretta, 1994

Bourguyia albiornata

Bourguyia albiornata (only eggs)

Machado & Oliveira, 2002

Dicranolasma scabrum

Dicranolasma scabrum

Gruber, 1993

Discocyrtus oliverioi

Discocyrtus oliverioi (only eggs)

Elpino-Campos et al., 2001

Erginulus clavotibialis

Erginulus clavotibialis (eggs and early nymphs)

Goodnight & Goodnight, 1976

Gagrellinae

Opiliones

Stare˛ga, 1976a

Ischyropsalis hellwigii

Leiobunum sp., Opilio parietinus

Verhoeff, 1900; Kästner, 1926

Lacinius dentiger

Lacinius dentiger

Mitov, 1988

Lacinius ephippiatus

Nemastoma lugubre

Todd, 1950

Lacinius horridus

Opiliones

Stare˛ga, 1976a

Laniatores

Laniatores

Mello-Leitão, 1932 (Continued)

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Table 9.3 Continued Predator

Opiliones prey

Source

Leiobuninae

Lacinius ephippiatus, L. horridus, Leiobunum sp., Opilio parietinus, Phalangium opilio, and Rilaena triangularis

Pfeifer, 1956

Leiobunum aldrichi

Leiobunum aldrichi

Edgar, 1971

Leiobunum blackwalli

Oligolophus tridens

Bristowe, 1949; Parisot, 1962

Leiobunum limbatum

Amilenus aurantiacus and Leiobunum limbatum

Stipperger, 1928

Leiobunum politum

Leiobunum politum

Edgar, 1971

Leiobunum rotundum

Leiobunum rotundum, Lacinius ephippiatus, Oligolophus tridens, and Phalangium opilio

Henking, 1888; Bristowe, 1949; Sˇilhavy´, 1956

Leiobunum vittatum

Leiobunum vittatum

Edgar, 1971

Metaplatybunus carneluttii

Metaplatybunus carneluttii

Karaman, 1995

Mitopus morio

Opiliones, Lacinius ephippiatus, Leiobunum rotundum, Mitopus morio, Oligolophus agrestis, Oligolophus sp., Oligolophus tridens, Paroligolophus agrestis, and Platybunus bucephalus

Kästner, 1931a; Bristowe, 1949; Todd, 1949; Phillipson, 1960a; Rüffer, 1966; Tischler, 1967; Stare˛ ga, 1976a; Littlewood & Littlewood, 1989

Nelima paessleri

Nelima paessleri

Holmberg et al., 1984; Angerilli & Holmberg, 1986

Odiellus troguloides

Odiellus troguloides

Juberthie, 1964

Oligolophus tridens

Opiliones, Leiobunum rotundum, Mitopus morio, Oligolophus tridens, and Phalangium opilio

Henking, 1888; Bristowe, 1949; Stare˛ ga, 1976a

Opilio parietinus

Opiliones, Leiobunum rotundum, Opilio parietinus, Oligolophus tridens, and Phalangium opilio

Henking, 1888; Roters, 1944; Rüffer, 1966; Stare˛ ga, 1976a

Opilio saxatilis

Opiliones

Stare˛ ga, 1976a

Opiliones

Opiliones

O. Pickard-Cambridge, 1890a; Heymons, 1915; Bristowe, 1949; Sankey, 1949a

Pachylus quinamavidensis

Pachylus quinamavidensis (only eggs)

Juberthie & Muñoz-Cuevas, 1971

Paranemastoma quadripunctatum

Paranemastoma quadripunctatum

Immel, 1954

Paroligolophus agrestis

Paroligolophus agrestis

Sankey, 1949b

Phalangiidae

Opiliones

Stare˛ga, 1976a

Phalangium opilio (nymphs and adults)

Opiliones, Leiobunum rotundum, Mitopus morio, Oligolophus tridens, Opilio parietinus, and Phalangium opilio (nymphs, eggs)

Henking, 1888; Rühm, 1926; Roters, 1944; Bristowe, 1949; Sˇilhavy´, 1956; Klee & Butcher, 1968; Edgar, 1971; Stare˛ga, 1976a; Mitov, 1988

Rilaena triangularis

Rilaena triangularis

Sankey, 1949b

Zachaeus crista

Phalangium opilio and Zachaeus crista

Mitov, 1988

Zygopachylus albomarginis

Zygopachylus albomarginis (only eggs)

Mora, 1990; Cokendolpher, 1993

Opiliones

Cloudsley-Thompson, 1958

CLASS ARACHNIDA, ORDER SCORPIONES Undetermined species

Natural Enemies

Predator

Opiliones prey

363

Source

CLASS INSECTA, ORDER COLEOPTERA Carabidae

Opiliones

Hillyard & Sankey, 1989

Carabus violaceus

Opiliones and Oligolophus sp.

Sankey, 1949b; Spoek, 1964

Pterostichus oblongopunctatus

Opiliones

Sergeeva & Grünthal, 1988

Sepedophilus sp. (larvae)

Goniosoma spelaeum (only eggs)

Gnaspini, 1995

Opiliones

Obrtel, 1976

Acutisoma longipes (only eggs)

Machado & Oliveira, 1998; Machado, 2002

Lygus sp.

Opiliones

Wheeler, 1976

Pentatoma prasina

Phalangium opilio

Sankey, 1949b

Reduvius personatus

Opiliones

Sankey, 1949b

Zelurus travassosi (nymphs and adults) (Figure 9.3D)

Acutisoma longipes (nymphs and eggs) and Goniosoma spelaeum (nymphs, adults, eggs)

Gnaspini-Netto, 1993; Gnaspini, 1995, 1996; Machado & Oliveira, 1998; Machado et al., 2000; Machado, 2002

Zelus sp.

Opiliones

Edgar, 1960, 1971

Camponotus abdominalis

Discocyrtus pectinifemur

Matthiesen, 1980

Formica balcanina

Opilio saxatilis

P. G. Mitov, pers. obs.

Formica cinerea

Phalangium opilio

Mitov, 1995

Formica lugubris

Mitopus morio, Mitostoma chrysomelas, Oligolophus tridens, Platybunus bucephalus, and Trogulus sp.

Cherix & Bourne, 1980

Formica pratensis

Lacinius horridus

Mitov, 1995

Formicidae

Opiliones, Bourguyia albiornata (only eggs), Gonyleptes saprophilus (only eggs), and Zygopachylus albomarginis (only eggs)

Stipperger, 1928; Bishop, 1950; Crome et al., 1969; Mora, 1987; Machado & Raimundo, 2001; Machado & Oliveira, 2002

Pachycondyla villosa (Figure 9.3E)

Bourguyia albiornata (only eggs)

Machado & Oliveira, 2002

Paravespula germanica

Opilio ruzickai

P. G. Mitov, pers. obs.

Opiliones

Iwasaki, 1998

CLASS INSECTA, ORDER DIPTERA Diptera CLASS INSECTA, ORDER ENSIFERA Strinatia sp. CLASS INSECTA, ORDER HEMIPTERA

CLASS INSECTA, ORDER HYMENOPTERA

CLASS INSECTA, ORDER MECOPTERA Bittacus mastrillii

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Natural Enemies

A

B

D

C

E

Figure 9.3. Invertebrate predators of Opiliones. (A–C) Spiders (both wandering and web builders) are the predominant invertebrate predators of harvestmen. (A) Iporangaia pustulosa (Gonyleptidae) being fed upon by a corinnid spider in southeastern Brazil (photo: B. A. Buzatto). (B) A female Longiperna zonata (Gonyleptidae) being eaten by a Ctenus sp. (Ctenidae) in southeastern Brazil (photo: G. Machado). (C) A cosmetid in the web of the spider Latrodectus geometricus (Theridiidae) in Trinidad (photo: J. G. Warfel). (D) A nymph of the assassin bug Zelurus travassosi (Reduviidae) preying on the harvestman Goniosoma spelaeum (Gonyleptidae) inside a cave in southeastern Brazil (photo: P. Gnaspini). (E) The ponerine ant Pachycondyla villosa preying on eggs of Bourguyia albiornata (Gonyleptidae) in southeastern Brazil (photo: G. Machado). Scale bars = 10 mm.

Natural Enemies

presumably expels all the defensive chemicals and then will be eaten (Holmberg, 1970; Machado et al., 2005). Because of the difficulty in observing direct predation of harvestmen, most records in the literature are based primarily on gut contents or feces of predators, eaten remains in or below webs of spiders, and feedings done with captive animals. Indeed, several of the predator/prey records listed in Table 9.3 are based upon captive feedings. Some of these events would never take place in nature because the predator and prey do not occur in the same habitat (e.g., the araneid spiders of the genus Argiope and triaenonychid harvestmen of the genus Sclerobunus) or because they are not a regular food item for the predator. For example, Argel-de-Oliveira et al. (1998) reported that a great kiskadee, Pitangus sulphuratus (Tyrannidae), offered a harvestman to a captive fledgling, but the item was refused. Some of the feeding studies in the laboratory can be misleading because a well-fed animal will not respond the same as a hungry animal. Some young, well-fed mammals will “play” with Opiliones rather than eat them (J. C. Cokendolpher, pers. obs.). From Tables 9.2 and 9.3 it appears that passerine birds are by far the most diverse group of predators on harvestmen. Frogs and toads (Figure 9.4A), insectivorous mammals, spiders, and other harvestmen are the other main documented predators. However, the predominance of one predator group over the other may be misleading because of the differences in the numbers of studies regarding foraging habits of each taxonomic group. Predation on harvestmen certainly occurs more often and by more predators than are reported herein. Most studies on predators of Opiliones are not intensive or recorded over a long period of time. In many other examples in Tables 9.2 and 9.3, harvestmen reportedly made up a very minor percentage of the prey items found. In these cases it is often difficult to determine if the harvestmen prey were rare because of the season when larger mobile harvestmen are rare or because they are not a normal prey item of a particular predator. Because larger predatory fish strike at any active arthropod on the water’s surface, the rarity of fish eating harvestmen almost certainly is because of the lack of harvestmen falling into water rather than the refusal of such food by aquatic predators. In some cases Opiliones were recorded in significant numbers: 23% of foodstuffs of the mouse Apodemus flavicollis (Muridae) were Opiliones (Obrtel, 1974); 42% of the prey examined from the scorpionfly Bittacus mastrillii (Bittacidae) were Opiliones (Iwasaki, 1998); and according to Hågvar and Østbye (1976), Opiliones were one of the most important (based on fresh weight) food sources for meadow-pipits Anthus pratensis (Motacillidae). The prevailing food sources for Phoenicurus ochruros gibraltariensis (Turdidae) are Opiliones, Araneae, and insects (Glutz von Blotzheim & Bauer, 1988a). Phalangiids, mainly Platybunus bucephalus, were among the most frequent and abundant prey species recorded for the nuthatch (Kristín, 1994) and the collared flycatcher (Kristín, 2002). The high percentage of this harvestman species in the food of these two birds corresponded with its highest abundance of harvestman species in fir-beech forest (Kristín, 2002). According to Butterfield et al. (1981), Sorex minutus (Soricidae) eats arthropods (harvestmen, spiders, beetles, flies, and caterpillars) almost exclusively. Bauerová (1982) also noted the importance of

365

366

Natural Enemies

A

B Figure 9.4. (A) The toad Bufo ictericus (Bufonidae) feeding on the gonyleptid harvestman Acutisoma proximum (photo: B. A. Buzatto). Note tips of two harvestman legs sticking out of mouth (arrow). (B) The marsupial Philander opossum (Didelphidae) is a widespread predator of several species of South American harvestmen, mainly those that live inside caves (photo: A. A. Giaretta). Scale bars = 5 cm.

Natural Enemies

arachnids (especially Opiliones) in the diet of this same shrew. Pernetta (1976) ranked the foods of this shrew and Sorex araneus, with Opiliones being one of the dominant components. Whereas the pigmy shrew ate mainly Nemastoma sp., the common shrew selected larger species of Opiliones. Examination of Philander opossum (Didelphidae) feces revealed that a harvestman from caves in Brazil (Goniosoma spelaeum) was an important food item, especially when foods on the surface (mainly fruits) were scarce (Pellegatti-Franco & Gnaspini, 1996; Figure 9.4B). This species of marsupial was observed to prey on up to 10 harvestmen during a single visit to the cave. One of the major food items was also Opiliones for the opossum Didelphis aurita (Cáceres & Monteiro-Filho, 2001). As reviewed in Chapter 8, cannibalism is common among Opiliones and their eggs. Cannibalism occurs more often upon earlier-instar juveniles and during or after molting, when the cuticle is soft and easily penetrated by the chelicerae of other harvestmen. According to Edgar (1971) and Machado and Oliveira (1998, 2002), cannibalism upon eggs is more common than upon juveniles and adults (see also Chapter 12).

PHORESY, ENDOZOISM, AND EPIZOISM Phoretic, endozoic, and epizoic associations are much more common than reported in the literature. Possibly these are the most common but unreported associations. The definitions of these three interactions are often given as anything living/riding in or on an animal, but for the purpose of this chapter, we are using definitions that are more restrictive. A phoretic association is one in which an organism receives carriage on the outside of a harvestman. It does not feed while riding on the harvestman and only receives a means of transport. This transport may be active (such as an insect riding a harvestman) or inactive (such as fungal spores). An endozoic association is one in which an organism passes through the digestive system of the Opiliones unharmed and thereby receives transport to a new location. We do not include internal parasites with this group because they were covered earlier under parasitic associations. An epizoic association is one in which the exterior of a harvestman provides an organism with a substrate for living, such as algae growing on the back of harvestmen. Because external parasites are treated under parasitic associations, they are not treated in the discussion of epizoic associations.

Phoresy Some phoretic and parasitic relationships with harvestmen are very old. The oldest records are from 40 million years ago, preserved in Baltic amber. Weitschat and Wichard (2002) show a fossil pseudoscorpion phoretically attached to the leg of a harvestman in amber. Likewise, a piece of Baltic amber is known that contains five collembolans holding on to the leg of a harvestman (G. Poinar, pers. comm.). Classical examples of phoretic riders of Opiliones are the pseudoscorpions. This

367

368

Natural Enemies

group of arachnids is well known to ride a variety of arthropods (Poinar et al., 1998). Interestingly, only three species of chernetid pseudoscorpions (Chelifer cancroides, Lamprochernes nodosus, and Pselaphochernes dubius) from Europe have been recorded from Opiliones, including phalangiids and sclerosomatids (W. W. Spicer, 1867; Savory, 1938; Vachon, 1947; Beier, 1948; Sankey, 1949b; CloudsleyThompson, 1956; Spoek, 1964; Poinar et al., 1998). It is difficult to understand why this is the case because chernetids and harvestmen are plentiful in the same habitats in other parts of the world. Perhaps, as stated by Muchmore (1971), “it is just that our fauna has not been studied as intensively as that of Europe and the association, occurring sporadically, has not yet been observed by an interested person.” Gruber (1993) also reported collembolans riding on the earth-encrusted surface of some soil-inhabiting harvestmen. Some mites and insect larvae also receive carriage. In the case of some mites, it is not clear if the mites are simply riding on the harvestmen or actually benefiting the harvestman by grooming it. Hunt (1979) found at least two species of mites on the exoskeleton of the triaenonychid harvestman Equitius doriae from southeastern Australia. While one of the species is parasitic, Hunt (1979) stated that the other species “may have a symbiotic relationship with the harvestman.” Concentrations frequently occur on the scutum near the openings of the odoriferous glands, and they may feed on nonvolatile components of their secretions. Presumably the mites have some “immunity” to the active component. A gonyleptid from Argentina, Pachyloidellus butleri, had numerous astigmatid mite deutonymphs located on its chelicerae and pedipalps (J. C. Cokendolpher, pers. obs.). Two species of mites were observed on the nemastomatid Ortholasma levipes from the western USA (J. C. Cokendolpher, pers. obs.). Some of the mites were the hypopal stage of an Anoetidae, whereas the second species remains unidentified. The anoetids were observed to move about freely on the chelicerae and the mouth area of the harvestmen. It seems odd that these mites would frequent an area where there might be food scraps if they did not feed during transport (see also Mitov, 1997a; Figure 9.5A). The second species of mite was found on the dorsum of the abdomen. These appeared to be “grazing” on the layer of dirt and fungi that is found on the surface of many soil-dwelling nemastomatids. It is possible that both of these species were feeding while in transport and therefore should more properly be considered as a form of epizoism. Several specimens of Cyphophthalmus aff. teyrovski collected in a Yugoslavian cave had what appear to be arthropod eggs attached to their appendages (Figure 9.5B). Additional photographs show that the end of the structure was open, suggesting that the eggs had hatched. Further research is needed to determine if this was an accidental event or the species laying the eggs normally chooses harvestmen to lay its eggs upon for transport. Cyphophthalmus aff. teyrovski is a small harvestman that is not highly mobile, suggesting that this might have been more of a chance encounter. Opiliones presumably carry many species of bacteria, fungal cleistothecia/spores, and plant pollen and seeds, which they pick up while crawling through their environ-

A

B

D C Figure 9.5. Epizoics of Opiliones. (A) Phoretic mite Anoetus sp. (Anoetidae) on the anal operculum of the sironid harvestman Siro sp. (photo: P. G. Mitov). (B) Unidentified arthropod egg on the sironid harvestman Cyphophthalmus aff. teyrovski (photo: I. M. Karaman). (C) Fern sporangia (Polystichum sp.) epizoically attached to the leg tarsus of the phalangiid harvestman Leptobunus parvulus (photo: J. C. Cokendolpher). (D) Phoretic Mallophaga attached to the leg tarsus of the sclerosomatid harvestman Leiobunum rumelicum (photo: P. G. Mitov).

370

Natural Enemies

ment (Machado et al., 2000; Mitov, 1992). Much of their grooming removes these items, but only after they transport them some distance. Because such transport generally can only be observed with a compound microscope, only a few fern sporangia/spores and fungal cleistothecia have been reported in the literature to be carried by harvestmen (Cokendolpher, 1985b; Figure 9.5C). Phoretic Mallophaga have also been recorded (Figure 9.5D).

Endozoism Unlike many arachnids, Opiliones lack a pumping stomach, and therefore they chew their food (see Chapters 2 and 8) and often consume oocysts, spores, and other contaminants on their foods. The frequent grooming of the legs by the harvestmen may also lead to the ingestion of other microorganisms. Although it is unreported in the literature, there is no doubt that harvestmen carry many species of bacteria, yeast, and fungal spores as they pass through the digestive system. Examination of the gut content of many harvestmen reveals the presence of a variety of yeasts and fungal spores and hyphae and bacteria (J. C. Cokendolpher, pers. obs.). It is unknown if these enter via food (contaminates on foods) or as food, or if they are ingested accidentally during grooming. Digestion does not seem to kill some of these organisms, and they remain active after being passed in the feces (J. C. Cokendolpher, pers. obs).

Epizoism Earlier under the heading “Phoresy,” collembolans and several mites were mentioned that might be more correctly listed here. Further study would have to be done to see if these animals were actually feeding. In the cases of photosynthetic cyanobacteria, algae, and liverworts reported from Opiliones (Gruber, 1993; Machado & Vital, 2001), there is no doubt that these organisms are using the surface of the harvestmen as a substrate for living (see also Figure 9.5C). Saprophytic fungi are also observed on harvestmen that are from very humid conditions. The mites may be beneficial to the harvestmen by grooming them, whereas the photosynthetic organisms possibly provide camouflage.

GENERAL PATTERNS Because of the great variety in habits and morphologies of Opiliones and the diverse habitats they occupy, it is no wonder that they are attacked by and associated with a wide variety of organisms. Most harvestmen share some characteristics that make them vulnerable to attack by certain enemies. Unlike most arachnids, all harvestmen masticate their food, ingesting particles rather than using a pumping stomach to eat liquefied diets. Because of this, they are exposed to parasites and pathogens that might otherwise be filtered out by the feeding mechanism of most other arachnids.

Natural Enemies

This is especially true of the gregarines, which are abundant in harvestmen and uncommon in other arachnids. The omnivorous feeding habits of many harvestmen place them in proximity to contaminated materials that could result in contact with pathogens or infective stages of some parasites (see Chapter 8). Although harvestmen occur in arid regions, most seem to prefer moister environments (see Chapter 7). Living in moist, dark situations provides suitable habitat for exposure to some pathogens such as fungi, as well as infective stages of some nematodes. Because of the activity of some harvestmen, they are exposed to detection by predators that hunt by sight or sound. Highly mobile harvestmen also seem to travel more and appear to be more vulnerable to attack by parasitic mites. Higher mobility is linked to longer legs, so this also results in greater exposure to aboveground predators and parasites. Harvestmen also share some characteristics that seem to prevent attack by some enemies. As already mentioned, a preference for moist habitats can be detrimental, but this detriment also occurs for other arthropods that might be predators or parasitoids of harvestmen. This preference can also be positive in that such environments generally offer complex habitats that provide a suitable substrate for hiding from some predators. Diurnal hunting predators are not as successful at hunting harvestmen as other arthropods because most harvestmen are nocturnal or cryptic, living under covering objects or within the litter (see Chapter 10). Whereas some morphological traits such as hardened cuticle and spines deter some predators, the use of exocrine secretions may have a dual result. Some exocrine secretions are antimicrobial in nature and could help rid the harvestmen of external pathogens and parasites, as well as serving as a defensive agent against larger attackers (see Chapter 10). Finally, all harvestmen are free-living and therefore have not hosted or transmitted the various rickettsial and viral diseases that have developed in parasitic arachnids (mites and ticks). Predators of harvestmen are in general the same as those that attack spiders. As with other arachnids, predators of harvestmen often show a preference for size, as well as time and site of activity. However, many major groups of parasites and parasitoids of spiders and harvestmen differ. Gregarines are commonly encountered in harvestmen, but not in spiders (Levine, 1985). Ectoparasitic mites are common on harvestmen, but much less so on spiders (Southcott, 1991; Cokendolpher, 1993, Foelix, 1996). Parasitoids of eggs and adult spiders, such as Diptera, Hymenoptera, and Mantispidae, are unknown from Opiliones. Like scorpions (McCormick & Polis, 1990), solifuges (Punzo, 1998), and spiders (Foelix, 1996), harvestmen are predators upon younger members of their own species, as well as other species of their order (see Chapter 8). The general lack of harvestman parasitoids is interesting because they are relatively common in other groups of arachnids (especially spiders). Harvestmen (adults and eggs) are not exploited by wasps, whereas spiders are attacked by a great number of parasitoids of eggs and adults, including representatives of the families Ichneumonidae, Sphecidae, Pompilidae, and Scelionidae, as well as of the superfamily Chalcidoidea (Shaw, 1994; Gibson et al., 1997; O’Neill, 2001). Some of these

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372

Natural Enemies

parasitoids also exploit some insects, but not harvestmen. The same situation apparently occurs with the dipteran egg predators (Chloropidae, Phoridae, and Ephydridae). The reason(s) why harvestmen are not often attacked by parasitoids is uncertain, but we might speculate here. Most harvestmen prefer moist and shady habitats. Possibly the parasitoids prefer more open conditions, which are possibly better for hunting and present fewer pathogenic fungi that might attack the wasps or flies. Most harvestmen have a small body size. This is an advantage that allows its occurrence in spatially restricted soil and litter microhabitats where it is not readily discernible by many predators and parasitoids. Possibly the smaller biomass of these small species is not enough for full development of parasitoid larvae. The long legs of most surface-active harvestmen would probably also be an obstacle for wasps to successfully attack the body or to manipulate the host. Most harvestmen are nocturnal, and some are active during other low-light events (clouds, mornings, evenings). Although harvestmen are capable of rapid movement, many will move over the landscape slowly, possibly not activating the attack behavior of the wasps. Possibly the answer is also in the exocrine gland chemicals and integumentary morphology (thick cuticle and hard armament) of harvestmen. Moreover, many harvestmen are cryptic, living in soil, under stones, and on tree trunks (see Chapter 7). Some of them are covered with soil fragments and so are well protected (see Chapter 10). The eggshells of harvestmen are thick, unlike the thin shell of spiders, and better defend the embryos. Harvestmen eggs are also generally placed in a jelly mass or are deposed in soils, under stones, in plant stems, or in voids such as empty gastropod shells (see Chapter 12).

CONCLUDING REMARKS Studies of enemies and phoretic and endozoic/epizoic associations, not mere listing of new parasite or predator records, constitute profitable fields for future research. Besides basic understanding of these interactions (life cycles and recognition of new species of parasites), studies of the impact of enemies and associates on harvestman individuals and populations are highly desirable. The relative ease of laboratory culture of harvestmen (see Chapter 15) suggests the potential for detailed laboratory studies on parasites and pathogens, but these would be less informative about predators.

ACKNOWLEDGMENTS We thank Dr. S. Keller and F. Gschmeidler of Ferdinand Berger und Sohne GMBH Verlag, Horn, for allowing the reproduction of Figure 9.2A; B. A. Buzatto, J. Warfel, and Drs. P. Gnaspini, G. Machado, and J. Spatafora for providing other photographs; Dr. G. Poinar for his photographs, literature, comments, and identifications of various pathogens and parasites; Dr. I. M. Karaman for providing Figure 9.5B, as well as new records and literature; J. Owen and Dr. G. Perry for allowing access to Cuban

Natural Enemies

tree frog data and gut contents; Dr. A. A. Giaretta for providing data on the diet of a leptodactylid frog; Dr. M. Prysby for sending living, parasitized Opiliones that appear in Figures 9.1A–C; Drs. C. Delchev, A. Gyonova, and T. Lyubomirov for identifying some spiders, ants, and wasps reported herein; A. Pérez González for identification of the host in Figure 9.2B; D. Palmer for observations and photographs of mites on Eurybunus harvestmen; Drs. T. Blick, J. Gruber, R. Holmberg, A. Kristín, G. Machado, R. Macías-Ordóñez, T. Michev, I. Mihál, P. H. Pache, R. J. Raven, W. Reeves, and V. Rtzicka for information, records, and literature (some very difficult to obtain) on harvestmen enemies; and Dr. B. P. Nikolov for his great effort in checking over 1,000 publications on the foods of birds—his help made our coverage on this topic very complete.

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CHAPTER

10

Defense Mechanisms Pedro Gnaspini and Marcos R. Hara

C

onsidering the large number of species in the order Opiliones, and that their defensive odors have been known for two centuries, relatively few studies exist on defense behavior in harvestmen. The earliest and most extensive studies dealt with species of the suborders Eupnoi and Dyspnoi, probably because they are common in the Northern Hemisphere, where most of these studies originated. Only since the 1970s has extensive work been done on Laniatores, mostly from the Neotropical region. Several types of behavioral, morphological, and chemical defense mechanisms have been assigned to the order Opiliones as a whole, although some of these characteristics are restricted to particular groups. The best-known defense behavior in harvestmen is the use of chemical secretions. Scent glands and their defense function have been studied in over 100 harvestman species, but in many cases the studies include only anecdotal observations and do not identify the species. In this chapter we summarize current knowledge on defense mechanisms in harvestmen.

PRIMARY AND SECONDARY DEFENSES Defense behaviors in animals may be divided into two main categories: (a) primary defenses, which operate regardless of the presence of a predator, thus decreasing the chance of encounter with a potential predator, and (b) secondary defenses, which operate when the prey has direct or indirect contact with a potential predator, thus increasing the chances of prey survival during an encounter (Edmunds, 1974). Primary defenses include cases where the predator may not detect the prey, such as crypsis and anachoresis, or cases where the predator fails to recognize the prey as edible, such as aposematism and mimicry (Batesian and Mullerian mimicry). Secondary defenses include evasive responses, such as thanatosis, deflection of an at374

Defense Mechanisms

tack, withdrawal to a prepared retreat, fleeing, and deimatic behavior, as well as contusive responses, such as retaliation. Many of these mechanisms are widespread among harvestmen, whereas others are more restricted and will be considered further afterward. Group living, which may also have defensive functions, will be treated in detail in Chapter 11.

Crypsis Crypsis is the resemblance of an animal to a part of its environment such that predators fail to distinguish it from the environment (Edmunds, 1974). A mottled pattern or disruptive color markings, generally represented by stripes, prevent precise identification of the animal’s contour. Cryptic coloration seems to be widespread among Opiliones, hindering the identification and exact location of the body. Bright white bands on the distal portions of two or more legs in some phalangiids and sclerosomatids, for instance, may disrupt the recognition of the leg outline, which may otherwise be a conspicuous recognition feature for a predator (J. C. Cokendolpher, pers. comm.). Likewise, the dark or patchy coloration of some Laniatores that remain motionless and concealed in their natural substrate may also serve as a camouflage (Gnaspini & Cavalheiro, 1998; Figure 10.1A). Certain camouflages are highly precise, such as that of the phalangiid Megabunus diadema, which blends well with the commonly present lichen in its habitat (Hillyard & Sankey, 1989; Figure 10.1B). Dicranopalpus ramosus (Phalangiidae) rests with its eight legs splayed out sideways along long blades of grass (R. Jones, 2003). Many species of the genus Leiobunum (Sclerosomatidae) show a cryptic coloration, and as the nymphs grow, they change coloration and also move to a substrate on which they are more cryptic (Edgar, 1971). In addition to the cryptic coloration, L. rupestre has been observed to sway with grass blades in the wind (Kästner, 1968). Several species belonging to different families are camouflaged with debris affixed by a secretion from the integument (Figure 10.1C). This is the case for several species that live in leaf litter, including Sclerosoma spp. (Sclerosomatidae), Anelasmocephalus cambridgei, Trogulus spp. (Trogulidae), Leytpodoctis oviger, Tandikudius rugosus, Vandaravua carli (Podoctidae), Pseudotrogulus spp. (Gonyleptidae), and all species of the tribe Adaeini (Triaenonychidae) (Loman, 1905; Roewer, 1929b; Pabst, 1953; Martens, 1993b; Firmo & Pinto-da-Rocha, 2002). These species have a very granular integument, with generally black or dark brown legs, and upon disturbance they promptly display thanatosis (discussed later). Camouflage with dirt is also observed in other arthropods, such as nymphs of some species of reduviids (Heteroptera). In this case experiments with three ant species showed that the debris coating impedes chemical and tactile recognition of the nymphs by worker ants. Additionally, the coating was shown to increase nymph survival in encounters with other predators, such as spiders, geckos, and centipedes (Brandt & Mashberg, 2002). Although it is possible that the debris cover in harvestmen may have a similar defensive function, this still remains to be experimentally tested.

375

A

B

C

E

D

F

Figure 10.1.(A) The dark coloration of the integument of the Amazonian Manaosbia scopulata (Manaosbiidae), which remains motionless on the ground when disturbed by a potential predator, is an example of crypsis associated with thanatosis in harvestmen (photo: G. Machado). (B) The phalangiid Megabunus diadema, a species widespread in Europe and commonly found among moss and lichens, presents a patchy coloration concealing the individual in its natural substrate (photo: D. J. Curtis). (C) The Austrian Dicranolasma scabrum (Dicranolasmatidae), an example of a harvestman disguised with dirt affixed by a secretion from the integument (photo: J. Gruber). (D) Pristocnemis farinosus (Gonyleptidae), a bright red harvestman with white spots near the posterior end of the body, which inhabits the Brazilian Atlantic forest (photo: R. Pinto-da-Rocha). (E) Female of the Brazilian harvestman Pseudopucrolia sp. (Gonyleptidae) in thanatosis with legs retracted (photo: B. A. Buzatto). (F) A male of the large gonyleptid Pachyloidellus goliath, from Argentina, showing the armature of legs IV, which can be used to pinch the offending agent (photo: G. Machado). Scale bars = 5 mm.

Defense Mechanisms

Anachoresis Some animals live concealed in a hole or other retreat, and although this behavior may be primarily related to the search for more appropriate microclimatic conditions, it may also be considered a defense mechanism since it reduces the probability of contact with potential predators (Edmunds, 1974). Many harvestmen, including most Laniatores, Dyspnoi, and Cyphophthalmi, spend the day under stones and/or logs, at cave entrances, and among leaf litter, leaving their shelters at night to forage (see Chapter 8). This behavior may be considered a case of anachoresis.

Aposematism and mimicry Aposematism may be simply defined as the correlation between conspicuous signals, such as bright coloration, and prey unprofitability (Edmunds, 1974). For aposematism to be advantageous, the predator must either sample some of the prey, learning from this encounter to avoid animals with similar appearance in the future, or display an innate avoidance response to the aposematic signal (Edmunds, 1974). The use of bright colors is considered to be a defense against diurnal and visual predators, but aposematism may also include strong odors or characteristic noises (Edmunds, 1974). Aposematic animals are often slow moving and gregarious and tend to have longer postreproductive lives compared with related cryptic animals (Edmunds, 1974). Besides the presence of chemical defenses, which make harvestmen unpalatable for a great variety of predators, many species of Opiliones also exhibit some or all of the features just mentioned. Several representatives of the family Gonyleptidae (mainly in the subfamilies Caelopyginae and Progonyleptoidellinae), for instance, are brightly colored, including red and black, yellow and black, and red and yellow color patterns (Figure 10.1D). Additionally, they have diurnal habits, may be seen walking slowly on the vegetation, and live at least one year as adults (Hoenen & Gnaspini, 1999; Machado et al., 2004). Bright coloration is also found among some sclerosomatids, which are orange or bright yellow. Although aposematic patterns of coloration and diurnal habits have been widely reported in harvestmen, no specific study has been conducted to test whether species that present these features are avoided by visually oriented predators, such as insectivorous birds or lizards. González et al. (2004) reported that the gonyleptid Parampheres ronae has a pair of orange markings on its carapace located where some other harvestmen discharge a yellowish defensive secretion containing a mixture of alkylated benzoquinones. The defensive secretion of P. ronae, however, is quinone-free and nearly translucent. The authors suggest that the orange markings on P. ronae are aposematic since they imitate the glandular emission of quinone-producing harvestmen, such as the syntopic species Pachyloides thorellii and Acanthopachylus aculeatus (both Gonyleptidae). Mimicry is the resemblance of one animal (the mimic) to another (the model) such that a third animal (the predator) is deceived by the similarity into confusing the two (Edmunds, 1974). The occurrence of this type of defense strategy in harvestmen remains largely unreported, probably because of the constraints of their

377

378

Defense Mechanisms

body design. The harvestman body is so compact, with the prosoma widely fused to some opisthosomal segments, that probably it has not been possible to resemble a suitable model, such as a wasp or an ant. In turn, Mullerian mimicry may be somewhat common, although this remains to be tested. For instance, bright orange Brazilian sclerosomatids formerly identified as “Holcobunus citrinus” are presently recognized as different species belonging to more than one genera, which suggests that they resemble each other due to convergent evolution related to Mullerian mimicry.

Thanatosis Some animals respond to an attack by a potential predator by feigning death, a behavior known as thanatosis (Edmunds, 1974). This defense behavior is widespread in arthropods, and among arachnids it has been recorded in some species of the orders Araneae (Edmunds & Edmunds, 1986) and Ricinulei (Beck, 1968). In Opiliones there are several reported cases within both Dyspnoi and Laniatores, including representatives of the families Dicranolasmatidae (Gruber, 1993), Trogulidae (Pabst, 1953), Cosmetidae (Kästner, 1968; Eisner et al., 1978), Escadabiidae (G. Machado, pers. comm.), Gonyleptidae (Elpino-Campos et al., 2001; Pereira et al., 2004; Figure 10.1E), and Manaosbiidae (Cokendolpher, 1987b; Figure 10.1A). When handled, these harvestmen become rigid, with their legs retracted or stretched out in a characteristic fashion (Kästner, 1968; Hillyard & Sankey, 1989). Regarding the duration of thanatosis, Pabst (1953) recorded that the trogulid Anelasmocephalus cambridgei shows the most pronounced reaction, staying rigid for 20 minutes in response to any environmental trauma. A similar prolonged reaction can be seen in representatives of the genera Baculigerus (Escadabiidae) and Discocyrtus (Gonyleptidae), in which the individuals may remain motionless with the legs retracted over the body for nearly 10 minutes (G. Machado, pers. comm.; P. Gnaspini, pers. obs.). Gruber (1993) noted that Dicranolasma scabrum (Dicranolasmatidae) becomes rigid for 1–2 minutes or up to half an hour when experiencing blowing or light; when white light is turned off and red light is turned on, they quickly move away. Nentwig (1987) recorded that many insects, as well as some harvestmen, use thanatosis when entangled in spider webs, but in most cases the resident spider will detect such prey because of modified thread tension in the web. Detailed studies are necessary in order to investigate when thanatosis is used by different species and also to evaluate the effectiveness of this defense behavior against visually and nonvisually oriented predators.

Deflection of an attack Another means of escaping an attack is to cause the predator to attack some part of the body where the attack is unlikely to be fatal (Edmunds, 1974). Among harvestmen, two defense behaviors may be included in this category: bobbing and appendotomy.

Bobbing. When disturbed, some long-legged harvestmen rapidly vibrate the body (Berland, 1949), a defense behavior called bobbing, which probably confuses the

Defense Mechanisms

identification and exact location of the harvestman’s body. Bobbing is very common in (and probably restricted to) long-legged representatives of the suborder Eupnoi, mainly the Phalangioidea. Dimmock (1882) was probably the first to record this behavior in Opiliones, but he interpreted it as a defensive mimicry. According to him, bobbing would deceive predators (mainly birds) by imitation of pholcid spiders (which exhibit similar behavior) and was not a defense behavior per se. Holmberg et al. (1984), studying the sclerosomatid Nelima paessleri, noticed that bobbing of some individuals of a disturbed aggregation could elicit a sudden dispersal of the entire aggregation, with individuals moving away from the disturbance or dropping to the ground (see also Chapter 11).

Appendotomy. Appendage separation was recorded early in Opiliones by Latreille (1802b). Although it is generally referred to as “autotomy,” Roth and Roth (1984) assert that “autospasy” should be the preferred term since it implies separation of appendages restrained by any external source, whereas autotomy implies instantaneous separation by a reflex action, without external assistance or resistance, which is not observed in harvestmen. Although autospasy has been recorded in some species of Dyspnoi, such as the nemastomatid Nemastoma lugubre bimaculatum (Immel, 1954), this defense behavior is apparently more frequent among the longlegged Eupnoi, for whom it has been suggested to be the most important evasive response (Berland, 1949; Cloudsley-Thompson, 1958; Savory, 1959; Kästner, 1968; Edgar, 1971; Eisner et al., 1978). Another type of appendotomy defined by Roth and Roth (1984) is autotilly, which is the self-removal of an appendage, which has been recorded only for certain species of Leiobunum (Edgar, 1971). When seized by a potential predator, the harvestman leg severs at the femoraltrochanter joint, without bleeding (Berland, 1949; Miller, 1977; Roth & Roth, 1984; Hillyard & Sankey, 1989). Healing is very rapid, but, unlike whip spiders (Weygoldt, 1984) and certain spiders (Foelix, 1996), the lost leg is not regenerated (CloudsleyThompson, 1958; Kästner, 1968; Miller, 1977). The erroneous statement that detachment areas occur between coxa and trochanter (Berland, 1949; CloudsleyThompson, 1958; Kästner, 1968), overlooked in subsequent reviews, was possibly a misinterpretation of harvestmen anatomy or a confusion caused by the process of “regeneration” of the detached region. Macías-Ordóñez (pers. comm.) observed that after a nymph has released its leg at the trochanter-femur joint, the trochanter does not develop during the next molt. Therefore, the lack of a trochanter may have induced early researchers to believe that the leg was released at the coxa-trochanter joint. Curiously, Roth and Roth (1984) noted that the leg detached near the base of the femur in Sclerobunus (Triaenonychidae), which constitutes the only record of autospasy among the Laniatores. After appendotomy the lost appendage twitches rhythmically (ca. 78 times/ minute) for a period ranging from 60 seconds to 1 hour (Berland, 1949; Miller, 1977; Roth & Roth, 1984; Hillyard & Sankey, 1989). Interestingly, Eupnoi legs have special spiracular openings that provide a subsidiary respiratory supply for the legs alone (Eisner et al., 1978; see also Figure 2.12e in Chapter 2). After autospasy this supply

379

380

Defense Mechanisms

contributes to maintenance of the twitching mechanism. Gaubert (1892) observed a nerve ganglion in the leg and suggested that while the leg is connected to the body, the ganglion is probably influenced by the central nervous system, but when the leg detaches, the ganglion independently produces the twitching limb movements. Subsequently, Miller (1977) confirmed this hypothesis in studying the sclerosomatid Leiobunum blackwalli and the phalangiids Mitopus morio, Odiellus spinosus, Oligolophus tridens, Paroligolophus agrestis, and Phalangium opilio, showing that rhythmic twitching activity continues only in isolated femora, and that the proximal part of the femur contains a region activated by damage of the leg nerve and essential for spontaneously generated activity of an isolated leg. He also noted that proprioception is not involved in either burst initiation or patterning, and he concluded that motor neurons contain independent pacemakers (see Chapter 2). Appendotomy in harvestmen was experimentally shown to be an effective defense behavior in tests with ants and spiders, diverting the potential predator while the prey escaped (Eisner et al., 1978). Despite the benefits, appendotomy costs an individual harvestman. Guffey (1998, 1999), studying Leiobunum nigripes and L. vittatum, noticed that the loss of legs reduces mobility, foraging ability, and sensory perception, especially after the loss of three or more limbs. Additionally, Macías-Ordóñez (1997) recorded that males of L. vittatum with fewer legs generally lose a territorial dispute with males with more legs (see Chapter 12).

Withdrawal to a prepared retreat Anachoretic animals emerging from their retreats to feed respond to the appearance of a predator by rapidly retreating into their hole (Edmunds, 1974). This defense behavior has never been specifically addressed, but seems to occur among harvestmen as well. For instance, when illuminated or touched by an observer, individuals of the gonyleptid Goniosoma spelaeum leaving a cave at night to forage may run rapidly back into their retreats.

Fleeing An animal that perceives a potential predator typically rapidly moves away from the stimulus source (Edmunds, 1974). Indeed, long-legged harvestmen of the suborders Eupnoi and Laniatores rapidly run away when disturbed (Latreille, 1802b; Edgar, 1971; Anuradha & Parthasarathy, 1976; Gnaspini & Cavalheiro, 1998; Machado et al., 2000, 2001). Bishop (1949b) recorded that individuals of Leiobunum aldrichi take to the water and run across the surface to escape. Anuradha and Parthasarathy (1976) also recorded that the individuals of Gagrellula saddlana (Sclerosomatidae) scatter suddenly from their aggregations if they are disturbed by any external stimuli, and that scattering may be a mechanism to perplex predators (see also Chapter 11). The simple possession of long legs by some species already constitutes a defense trait because such harvestmen have the ability to safely distance themselves from small predators, particularly in habitats such as deep grass and foliage (Hillyard & Sankey, 1989).

Defense Mechanisms

A special case of evasion is dropping to the ground when disturbed. In combination with cryptic coloration, after falling down, the animal remains motionless and concealed, avoiding detection (Bishop, 1949b; Edgar, 1971; Hillyard & Sankey, 1989; Gnaspini & Cavalheiro, 1998; Machado et al., 2000). Some very sensitive species often drop at the mere approach of an observer or a flashlight beam (e.g., Gnaspini & Cavalheiro, 1998). Bishop (1949b) recorded that individuals of Leiobunum aldrichi drop from considerable heights to escape.

Deimatic behavior and stridulation Deimatic behavior is the attempt to frighten potential predators, for instance, by suddenly displaying bright colors or eyespots or by adopting postures apparently designed to intimidate predators (Edmunds, 1974). These behavioral responses have not been reported so far in harvestmen. Moreover, colored hidden parts are unlikely on the compact body design of harvestmen. Noises, or stridulation, commonly combined with the sudden use of bright colors, may be considered a special case of deimatic behavior. Stridulatory organs occur in several species of Dyspnoi and Laniatores (e.g., Lawrence, 1937b; Juberthie, 1957b, 1968; Kratochvíl, 1959; Gruber, 1969b, 1976; Silhavy, 1978). These organs usually present a series of parallel ridges opposing a similar series or another form of scraper (see Chapter 2). They may occur on the basal inner surface or the chelicerae’s second segment, or the pedipalps’ femur’s inner surface (in this case, opposing either the chelicerae’s outer surface or the ocularium denticles). Stridulation was considered a means of intraspecific communication between sexes since many juveniles have no such apparatus (Hillyard & Sankey, 1989). However, in some species, juveniles have stridulatory organs, while in other species, males and females have similar structures (Gruber, 1969b). Although stridulation may be primarily used for intraspecific communication, this might well be a defense, as arachnids and many insects typically begin stridulating when seized by a potential predator, generally invoking the release of the seized individual (Dumortier, 1963; Masters, 1979). The use of stridulation as a defense mechanism has not been addressed so far by harvestmen specialists, although Gruber (1969b) suggested defense as a possible function on the basis of its role in other arachnids. The behavioral role of stridulation, both in a sexual and a defense context, surely deserves further investigation.

Retaliation Under attack, some animal species retaliate by attacking the predator with whatever weapons they possess (Edmunds, 1974). Among harvestmen, aggressive or contusive defenses include pinching and pedipalpal and cheliceral attacks, as well as releasing of chemical secretions. In this section information is presented on mechanical defenses alone, whereas chemical defenses will be treated in more detail in the next section. Some Gonyleptidae, when taken in hand, quickly flex their fourth legs to deliver

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Defense Mechanisms

a sharp pinch to the offending agent’s hand between the armature of both coxae and femora (Figure 10.1F). This has been reported for Acanthopachylus aculeatus, Gonyleptes pectinatus (Bristowe, 1925), and all goniosomatines studied so far (Machado, 2002). Although females also present the same behavior, it seems to be more effective among males because their spines are longer than those in females. The pinching may be painful, sometimes causing bleeding in humans. Capocasale and Bruno-Trezza (1964) recorded that during the nipping the median spine of area V of A. aculeatus may also penetrate the dermis of the offending agent. Although the records of nipping in the literature are scarce, this is probably a widespread behavior among armed Laniatores, especially gonyleptids (Figure 10.1F). When handled near the oral region, goniosomatines generally seize the observer’s fingers with their pedipalps, biting with their chelicerae, always harmless to humans (Gnaspini & Cavalheiro, 1998; Machado, 2002). Miyosi (1942) cites the use of the first segment of the chelicerae of Nipponopsalis abei (Nipponopsalididae) in defense/attack, noting its resemblance to an ancient instrument used in Japan for defense against robbers during the Tokugawa era. Additionally, Capocasale and Bruno-Trezza (1964) reported that A. aculeatus may use the pedipalpal claw in defense. The harvestman aligns the claw with the tibia and, depending on the pressure it experiences, tries to penetrate the offending agent. Other gonyleptids, such as Acutisoma longipes and Goniosoma catarina, frequently attack with the pedipalps before seizing or pinching the offending agent (Machado, 2002).

CHEMICAL DEFENSES The best-studied defense behavior of harvestmen, considered most effective in Cyphophthalmi and Laniatores, is the use of chemical secretions. The animals secrete compounds from a pair of exocrine glands, which can be called “scent glands,” “repugnatorial glands,” “odoriferous glands,” or “stink glands.” Among arachnids, chemical defenses have been recorded for Opiliones, Uropygi, and Schizomida (reviewed in Eisner et al., 1978). In the last two orders the exudate, which is mainly composed of acetic acid, is produced and released in a pair of glands located at the base of the flagellum (Schmidt et al., 2000). In harvestmen the gland openings (or ozopores) are located at the laterofrontal angles of the prosoma (see Chapter 2), and the exudate may be composed of several volatile secretions (discussed later).

A brief historical account Lawrence (1938) and Juberthie (1961d) presented historical accounts of studies on chemical defenses in harvestmen, of which a summary follows, quoting these authors. The earliest mention of a remarkable peculiar odor in harvestmen (“Phalangium”) was made by Latreille (1802b), who identified the openings of the glands as a second pair of spiracles. Treviranus (1816), Tulk (1843), and Leydig (1862) mistook the gland openings for eyes. Gervais (1849) was the first to relate odor to the

Defense Mechanisms

glands and to describe the scent glands from Laniatores (“Gonyleptes”). Krohn (1867) was the first to describe these glands (including histology) from Eupnoi, although he did not recognize their function. Several reports of peculiar smell followed (Simon, 1879a; Sørensen, 1879; Rößler, 1882; Bristowe, 1925; Stipperger, 1928). In the twentieth century an adequate historical summary of these glands was given by Hansen and Sørensen (1904), who described for the first time the glands of Cyphophthalmi and recorded that the pettalid Purcellia illustrans ejected a liquid through a short tube strongly resembling an eyestalk, situated on the prosoma side. Sørensen (1879, 1932), Kolosvary (1929), and Kästner (1935b) produced other early morphological descriptions. Lawrence (1938) fully described the morphology of triaenonychid Laniatores (Adaeulum robustum, Larifuga capensis, and Larifugella natalensis) and was the first to record harvestman jet emissions. Beginning at the end of the 1950s, numerous studies were undertaken that focused on chemical defenses, probably inspired by the first chemical identification of a defensive compound produced by a harvestman, the gonyleptidine produced by Acanthopachylus aculeatus (Estable et al., 1955). Researchers from the same laboratory made several additional studies on the pharmaceutical effects of these secretions (e.g., Ardao & Freyre, 1956; Freyre et al., 1958; Sáez & Drets, 1958). From the 1960s onward, studies relating morphology to function began to bloom (e.g., Juberthie, 1961c,d, 1976; Lopez et al., 1980; Cokendolpher, 1987b; Clawson, 1988; Juberthie et al., 1991; Acosta et al., 1993; Gnaspini & Cavalheiro, 1998). During the 1970s and 1980s numerous studies concerning the chemical identification of harvestmen defensive secretions were done, especially those by Eisner and colleagues (see references in Table 10.1). Although general behavioral studies were conducted in the 1960s and 1970s (e.g., Capocasale & Bruno-Trezza, 1964; Edgar, 1971), it was not until the mid-1980s and 1990s that behavioral studies were truly revived, especially among Laniatores (e.g., Cokendolpher, 1987b; Acosta et al., 1993; Gnaspini & Cavalheiro, 1998; Machado et al., 2000). Recently, the defensive secretions were demonstrated to also act as an alarm pheromone (Machado et al., 2002; see also Chapter 11). Likewise, an attempt to relate morphology, behavior, and chemical identification to phylogeny was conducted by Hara and Gnaspini (2003) and Hara et al. (2005).

Internal morphology of the gland and surroundings Like many other exocrine glands of arthropods, harvestman glands derive from the ectoderm (Faussek, 1892) and are actually infoldings of the body wall, consisting of three layers: an outer basal membrane near the hemolymph cavity, a glandular epithelium consisting of secretory and nonsecretory areas, and an inner membranous cuticular lining (Krohn, 1867; Faussek, 1892; Juberthie, 1961c,d; Clawson, 1988). The glandular epithelium appears to be constituted by secretory units, each consisting of two secretory cells joined by an intermediate cell, and connected by a chitinous duct to the general reservoir of the odoriferous gland (Juberthie, 1961c, 1976; Clawson, 1988). Extensive histological descriptions and dis-

383

Table 10.1 Opiliones studied chemically and compounds isolated from their secretions Taxa

Compounds

Reference

CYPHOPHTHALMI Cyphophthalmus duricorius

Tridecan-2-one

Raspotnig et al., 2005

7-tridecen-2-one 1,4-naphthoquinone 6-methyl-1,4-naphthoquinone Undecan-2-one 4-chloro-1,2-naphthoquinone 6-tridecen-2-one *10% Siro exilis

Tridecan-2-one

Raspotnig et al., 2005

7-tridecen-2-one 1,4-naphthoquinone 6-methyl-1,4-naphthoquinone 4-chloro-1,2-naphthoquinone Pentadecan-2-one 6-methyl-4-chloro-1,2-naphthoquinone 6-tridecen-2-one *13% EUPNOI Phalangiidae Phalangium opilio

1,4-naphthoquinone

Wiemer et al., 1978

6-methyl-1,4-naphthoquinone Sclerosomatidae Hadrobunus maculosus

4-methyl-3-heptanone

Jones et al., 1976

Leiobunum aldrichi

E-4,6-dimethyl-6-nonen-3-one

Jones et al., 1976

*10% Leiobunum calcar

E-4,6-dimethyl-6-octen-3-one

Jones et al., 1976, 1977

E,E-2,4-dimethylhexa-2,4-dien-1-ol *1–8% Leiobunum formosum

4-methyl-3-heptanone

Blum & Edgar, 1971

*30% Leiobunum leiopenis

4-methyl-3-heptanone E-4-methyl-4-hepten-3-one E,E-2,4-dimethylhexa-2,4-dien-1-ol E,E-2,4-dimethylhepta-2,4-dien-1-ol

Jones et al., 1977

Taxa Leiobunum nigripalpi

Compounds 4-methyl-3-hexanone

Reference Jones et al., 1977

4-methyl-3-hexanol E-4-methyl-4-hexen-3-one E-4-methyl-4-hepten-3-one E,E-2,4-dimethylhexa-2,4-dienal *traces Leiobunum speciosum

4-methyl-3-heptanone

Blum & Edgar, 1971

*30% Leiobunum townsendi

4-methyl-3-heptanone

Ekpa et al., 1985

4-methyl-3-heptanol 4-methyl-4-hepten-3-one E-4-methyl-4-hepten-3-ol Leiobunum ventricosum

4-methyl-3-heptanone

Jones et al., 1976

Leiobunum vittatum

4-methyl-3-heptanone

Meinwald et al., 1971

E-4,6-dimethyl-6-octen-3-one LANIATORES Cosmetidae Cynorta astora

2,3-dimethylphenol

Eisner et al., 1977

2-methyl-5-ethylphenol Eucynortula albipunctata

2,3-dimethylphenol

Roach et al., 1980

2-methyl-5-ethylphenol Eucynortula nannocornuta

2,3-dimethyl-1,4-benzoquinone

Roach et al., 1980

2,3,5-trimethyl-1,4-benzoquinone Paecilaema eutypa

2,3-dimethyl-1,4-benzoquinone

Eisner et al., 1977

2,5-dimethyl-1,4-benzoquinone 2,3,5-trimethyl-1,4-benzoquinone Paecilaemana quadripunctata

2,3-dimethyl-1,4-benzoquinone

Eisner et al., 1977

2,3,5-trimethyl-1,4-benzoquinone Vonones sayi

2,3-dimethyl-1,4-benzoquinone

Eisner et al., 1971

2,3,5-trimethyl-1,4-benzoquinone Gonyleptidae Acanthopachylus aculeatus

2,3-dimethyl-1,4-benzoquinone 2,5-dimethyl-1,4-benzoquinone

Estable et al., 1955; Fieser & Ardao, 1956

2,3,5-trimethyl-1,4-benzoquinone Goniosoma spelaeum

2,3,5-trimethyl-1,4-benzoquinone

Gnaspini & Cavalheiro, 1998

2-ethyl-1,4-benzoquinone (Continued)

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Defense Mechanisms

Table 10.1 Continued Taxa

Compounds

Nesopachylus monoceros

2,3-dimethyl-1,4-benzoquinone

Reference Roach et al., 1980

2,3,5-trimethyl-1,4-benzoquinone Pachyloidellus goliath

2,3-dimethyl-1,4-benzoquinone

Acosta et al., 1993

2,3,5-trimethyl-1,4-benzoquinone 2,3-dimethyl-5-ethyl-1,4-benzoquinone 2,3-dimethylphenol 2,3-dimethyl-5-ethylphenol 2-methyl-5-ethylphenol Manaosbiidae Zygopachylus albomarginis

2,3-dimethyl-1,4-benzoquinone 2,3,4-trimethylphenol

Eisner et al., 1977; Roach et al., 1980

2,3-dimethylphenol

Duffield et al., 1981

Stygnommatidae Stygnomma spiniferum

2,3-dimethyl-5-ethylphenol 2-methyl-5-ethylphenol Triaenonychidae Sclerobunus robustus

N,N-dimethyl-β-phenylethylamine

Ekpa et al., 1984

Nicotine Bornyl acetate Bornyl propionate Camphene Limonene The asterisk (*) indicates percentage of unidentified compounds. Hara et al. (2005) studied 22 additional species of Gonyleptidae and detected 37 different compounds. These results were not added to this table, but we suggest that the reader refer to the original paper.

cussions can be found in Holmberg (1970) and Clawson (1988), who studied several Eupnoi, Lopez et al. (1980), who studied Sabacon paradoxus (Sabaconidae), and Juberthie et al. (1991), who studied Ischyropsalis spp. (Ischyropsalididae). The glands are well developed and more visible among Cyphophthalmi and Laniatores than among Eupnoi and Dyspnoi. The gland sacs have no musculature, but there is an associated musculature (Berland, 1949). According to Juberthie (1961c,d), the most elaborate musculature is found in Cyphophthalmi, in which, in addition to special muscles associated with the valvular openings of the glands, the sac compressor muscles penetrate the glandular sacs. In Laniatores the muscular sheath of the sac and the muscle of the duct are present, but the ventral muscle that opens the duct has disappeared, and in Eupnoi and Dyspnoi the sac muscles are

Defense Mechanisms

missing altogether. Since these glands have no muscle system, Holmberg (1970) suggested that expansion of the digestive diverticulae by muscle contraction further down the alimentary canal and muscle contraction of the three major groups of muscles surrounding the glands indirectly constrict the glands, causing them to void their content. In contrast, Clawson (1988) hypothesized that secretion expulsion is under nervous and muscular control, and the propelling force for expulsion is presumably increased hydrostatic pressure brought about by muscles compressing the dorsal and ventral exoskeleton. The structure of the secretory cells of Leiobunum spp. suggests that two types of secretion occur: exocytosis of material contained in secretory granules, and transport of fluid through glandular cells from the hemocoel to the canaliculi (Clawson, 1988). Glandular control has been demonstrated in Cyphophthalmi (Juberthie, 1961d) and has also been suggested to occur in Eupnoi (Holmberg, 1970) and perhaps in Laniatores (Lawrence, 1938).

External morphology of the gland opening and surroundings The gland sac opens through an aperture (ozopore) located on the prosoma beside the lateral margins of coxae I in Eupnoi and Dyspnoi, or coxae II in Laniatores, and atop a tubercle (ozophore) located between coxae II and III in Cyphophthalmi (Juberthie, 1961c,d, 1976). Actually, in Cyphophthalmi it is often located lateral to a “smooth plate” located at the top of the tubercle, as in Figure 10.2A, but many other ozopore openings exist (see de Bivort & Giribet, 2004). In some Dyspnoi, especially among Ischyropsalididae, the opening is closed by a membrane (Juberthie, 1961c). The ozopore may be a single gland opening (e.g., Juberthie, 1961d, 1976; Blum & Edgar, 1971; Figures 10.2A–C), or the structure of the gland-opening region may be more complex in some Laniatores (e.g., Gnaspini & Cavalheiro, 1998; Figures 10.2D and 10.3). In the genus Leiobunum the outlets of the paired scent glands are located on the prosomal flanks. The outlet is a narrow slit located slightly off-center of the double-walled depression surrounding it (Blum & Edgar, 1971; Clawson, 1988; Figure 10.2B). In Neotropical gagrellines (Sclerosomatidae) the doublewalled depression is absent and the opening is “simple.” In some Gonyleptidae two outlets are located dorsolaterally: one anterior (a notch, AO) and one posterior (PO), with its internal integument covered with several small sharp projections (Gnaspini & Cavalheiro, 1998; Hara & Gnaspini, 2003; Figure 10.3). When there is only one opening, PO is absent (Hara & Gnaspini, 2003). In addition, AO is covered by a soft integumentary dome (ID) crossed by a slit (SL), extending from the area near the trochanter apophyses up to the apex of the integumentary dome. The posterior rim of this slit may present a V-shaped cut (VO). Unfortunately, internal release from these openings (AO and PO) was not observed through a microscope. The running fluid actually bathes the posterior opening when it comes from the lateral channel toward the lateral groove, but microscope observations did not clearly reveal whether this bath occurs over or through the posterior opening.

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A

B

C

D

Figure 10.2. General view of ozopores (OZ). Insets show a general view of the harvestman body, while the square shows the enlarged area (photos: P. Gnaspini). (A) Cyphophthalmi: lateral view of tubercle. (B) Eupnoi: dorsal view of Leiobunum townsendi (Sclerosomatidae). (C) Dyspnoi: lateral-anterior view of Ischyropsalis sp. (Ischyropsalididae); the ozopore is located just below a small tubercle (see inset). (D) Laniatores: lateral view of Stygnus multispinosus (Stygnidae); LC = lateral row of tubercles.

Fluid displacement The discharge of the glands in Laniatores generally mixes with enteric fluid, running from the mouth into channels that connect to the gland openings, although this was confirmed only in a few cases. Proof that the fluid was regurgitated was provided by feeding the animals with a diluted aqueous solution of a nonabsorbable dye with the subsequent production of defensive droplets of the same color as the dye (Eisner et al., 1971, using amaranth; Acosta et al., 1993, using Ponceau 4R). The

A

B

C Figure 10.3. (A) Dorsal and (B) ventral view of the anterior left region of a male Acutisoma longipes (Gonyleptidae), showing features related to chemical defense (photos: P. Gnaspini). Scale bars = 1 mm. (C) Detail of the right dorsal. Scale bar = 100 ␮m. Abbreviations: AO = anterior opening of the ozopore (gland opening); AP = apophyses of coxa II; CC = channels between coxae (pedipalp/leg I and leg I/leg II)—compare the latter to the suture between coxae II and III (SC); GS = glandular sacs (dotted lines indicating their position inside the animal); ID = integumentary dome; LC = lateral channel; MO = mouth; MS = margin of the scutum; PO = posterior opening of the ozopore; SL = slit of the integumentary dome; SP = sensorial peg; VC = vertical channel connecting CCs with LC; VO = V-shaped ornament on the posterior margin of the anterior opening of the ozopore.

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enteric fluid proved to be mostly aqueous and free of defensive secretions (Eisner et al., 1971; Acosta et al., 1993; Gnaspini & Cavalheiro, 1998). Afterward the enteric fluid reaches the gland openings by capillarity through a sequence of channels (e.g., Gnaspini & Cavalheiro, 1998; Figure 10.3). First, there are two pairs of ventral channels (CC): one located between the coxae of the pedipalps and legs I and the other between the coxae of legs I and II, its white color sharply contrasting with the yellowish coxae. Independently, these ventral channels connect to a horizontal lateral channel defined within the soft pleura between the dorsal scutum and the coxal insertions. Finally, immediately in front of the gland opening, there is a somewhat oblique vertical channel (VC) that connects with the lateral groove (LC). At this point the enteric fluid may collect the defensive secretions and may be displaced toward the end of the body through lateral channels or shallow slits (discussed later). This arrangement is very similar to that described for the cosmetids Cynorta astora, Paecilaema eutypa, Paecilaemana quadripunctata, and Vonones sayi (Eisner et al., 1971, 1977), as well as for the gonyleptid Pachyloidellus goliath (Acosta et al., 1993). A similar procedure was reported in the stygnommatid Stygnomma spiniferum (Duffield et al., 1981) and in the sclerosomatid Leiobunum vittatum (Clawson, 1988), although without a definitive demonstration. Interestingly, Acosta et al. (1993) observed that the chemical secretion is intermittently discharged into the enteric fluid, reaching by diffusion all areas previously occupied by the fluid, even running back to the mouth region through the same channels. The coxae near the ozopores may have apophyses (AP in Figure 10.3) (Acosta et al., 1993; Gnaspini & Cavalheiro, 1998) that might serve to block the overflow of fluid at this sharp turning point, although the role of these apophyses in liquid displacement remains to be investigated. The volume of running fluid is sometimes large, and the apophyses might serve to regulate the upper level, preventing overflow. Although Eupnoi have different behaviors than those of Laniatores, liquid displacements via processes on the coxae and the involvement of apophyses are also known to occur in them. However, in this group the liquid takes the reverse course. After discharge the defensive secretion covers the harvestman’s dorsal surface, and some of the liquid passes to the ventral surface. Apophyses on the inner margin of each coxae, whose pointed extremities lie at the anterior end of the gland opening, transfer the secretion to the lower surface of Leiobunum aldrichi (Bishop, 1950). From this point a groove connects to a channel between the first and second coxae. On the lower surface the coxae converge toward the midline, and the secretions of the two glands fuse to form a single large drop at the tips of the chelicerae. Holmberg (1970) also noted that the liquid between the coxae of the phalangiid Homolophus biceps often runs down the sides of the coxae, forming a drop of clear liquid near the opening of the mouth. Bishop (1950) noted that the secretion of L. aldrichi first appeared as a slightly viscid clear fluid and then, after further stimulation, as a milky fluid. This might be a mixture of oral fluid and secretion, although this has not been proved. Indeed, mixing between the oral fluid and defensive secretion was observed in L. vittatum (Clawson, 1988).

Defense Mechanisms

Figure 10.4. Scheme of the main chemical defense mechanisms of harvestmen recorded in the literature.

Behavior Various types of behavior related to secretion use have been recorded in the literature. We herein propose a new scheme for classification of behavioral defense traits among harvestmen (Figure 10.4) based on those previously proposed by Acosta et al. (1993) and Hara and Gnaspini (2003). The various types of behavior (and their respective steps) related to the use of secretions are briefly discussed as follows. Unfortunately, many early reviews provide little information that may augment our scheme. Studies before the 1980s reported only one type of behavioral mechanism per species. However, recent studies focusing on Laniatores (Gnaspini & Cavalheiro, 1998; Hara & Gnaspini, 2003) proved that individuals could vary the mechanism used in their defense. In addition, no preference for one delivery mechanism could be detected. For instance, the same specimen of Goniosoma spelaeum would either emit a jet, form a shield, or even attempt only to pinch the offending agent with no use of chemical compounds during subsequent handling (Gnaspini & Cavalheiro, 1998). Two basic types of defense behavior can be recognized (Figure 10.4). In the first type, which is the most diversified, the released secretion forms a chemical shield around the harvestman’s body, either in the form of vapor or of liquid. The latter can be released and afterwards transported to other parts of the body, enlarging the chemical shield. In the second type the secretion is actively transferred to the offending agent. The main mechanisms are briefly described as follows, and their evolution within Gonyleptidae is discussed in Hara and Gnaspini (2003).

(1) Creation of a chemical shield around the body (1.1) Exhalation of odor from the ozopore, with little or no emission of liquid. In Phalangiidae and Ischyropsalididae defensive secretions are emitted in gas form from a valve near the gland opening, differing from Laniatores and Cyphophthalmi (Holm-

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berg, 1970; Juberthie et al., 1991). Crystals are frequently found inside the gland sacs of Ischyropsalididae, and this may be related to the fact that only odors are detected, which may reflect the slow sublimation of these crystals (Juberthie et al., 1991). (1.2) Emission of a secretion globule at the gland opening and subsequent evaporation. In Eupnoi (Bishop, 1949a; Juberthie, 1961c) and Laniatores (Lawrence, 1938; Juberthie, 1961c; Hara & Gnaspini, 2003), a droplet formed at the opening can remain there, which seems to be a widespread phenomenon. A particular case is the retention of the droplet in a pebbled or shallow depression surrounding the ozopore (as in Figure 10.3B), providing either a larger surface area or a more retentive surface for the secretion, reported in Leiobunum spp. (Blum & Edgar, 1971; Clawson, 1988). (1.3) Emission of the secretion at the ozopore with subsequent transfer to other parts of the body. This is the most common and most diversified defense behavior observed among harvestmen. From the ozopore, with or without previous mixing with the enteric fluid, the defensive secretion is transferred to other parts of the body, forming a defensive chemical shield. (1.3.1) Emission as a fine spray that moistens the animal’s dorsum. This phenomenon was observed in many species of Leiobunum. A fine spray is emitted from the external slits, and the dorsal surface of the prosoma and opisthosoma is rather uniformly soaked (Bishop, 1950; Blum & Edgar, 1971; Meinwald et al., 1971). The coxae of the first pair of legs are pressed against the area proximate to the glandular outlets and appear to function by channeling the secretion along a groove between the first and second pair of coxae. The first pair of coxae bears enlarged triangular projections that can sit in the pit housing the glandular outlet, thus providing a means of transferring the secretion to the lower surface of the body. (1.3.2) Spreading of droplets over the body as a secondary result of jet emission. Hara and Gnaspini (2003) noticed that in many species of Gonyleptidae that squirt the secretion directly from the ozopore (see 2.3 below), droplets of pure defensive secretion appear on the harvestman’s body, probably functioning as a chemical shield. It is not possible to determine if this is a defense mechanism or solely a secondary event. (1.3.3) Fluid displacement from the gland-opening region through the lateral margin. In many Laniatores the fluid may run by capillarity through the lateral margin of the scutum, either by an integumentary groove (as in Figure 10.3C), a slit, a row of tubercles (as in Figure 10.2D), a row of granules, or a combination of these structures (Sørensen, 1932; Lawrence, 1938; Juberthie, 1961c; Duffield et al., 1981; Cokendolpher, 1987b; Acosta et al., 1993; Gnaspini & Cavalheiro, 1998; Machado et al., 2000; Hara & Gnaspini, 2003). The lateral groove may be well marked or smooth and very shallow. A series of several pegs (probably sensory, as their shape is similar to that of sensorial pegs of other arthropods) may be present along its

Defense Mechanisms

margin (SP, as in Figure 10.3). The exact function of these pegs has not been studied. The defensive fluid bathes these pegs as it runs along the groove. The lateral groove begins slightly anterior to the gland opening and comprises a continuous passage for the fluid flowing from the ventral channels via the vertical channel and the lateral groove (LC, as in Figure 10.3). Thus the secretion from the gland is released directly into the flowing enteric fluid from the mouth. It should be noted that mixing with the secretion may not occur (Gnaspini & Cavalheiro, 1998). Sometimes the coxal droplet contains enteric fluid alone, as indicated by its lack of both odor and color, as in Figure 10.5A. This droplet may remain clear; that is, the harvestman may not release secretion into it. This probably occurs when no secretion remains in the gland or the animal does not release it. Second, the secretion can be released after the droplet is formed. In this case, the clear droplet (Figure 10.5A) becomes turbid and yellowish (Figure 10.5B). Third, the secretion can be released while the enteric fluid runs in front of the gland opening. In this case the droplet that is formed, as well as the fluid over the lateral groove, is already turbid and yellowish (Figure 10.5B). Therefore, the same final turbid droplet may require one or two steps to be achieved. After flowing through the lateral margin, the defensive secretion may collect afterward, forming a droplet on coxae IV (Gnaspini & Cavalheiro, 1998), at the lateroposterior area of the body (Juberthie, 1961c; Duffield et al., 1981), at posterior spines (Cokendolpher, 1987b), and/or at the posterior end of the body (mainly free abdominal tergites) (Lawrence, 1938; Duffield et al., 1981; Machado et al., 2000; Hara & Gnaspini, 2003), where it evaporates. Bristowe (1925) reported that Brazilian gonyleptids exuded a drop of liquid from above coxae IV, and Capocasale and Bruno-Trezza (1964) noted the simultaneous emission of liquid from the prosomal glands and from legs IV, which were probably mistaken interpretations of the formation of a droplet on coxae IV after the defensive fluid has run through the lateral channel without the intermediate formation of a droplet near the ozopore. Once the droplet is formed, individuals of Zygopachylus albomarginis (Manaosbiidae) may bring leg II into contact with the fluid, resulting in a drop of secretion deposited near the base of each femur II, amplifying the chemical shield (Cokendolpher, 1987b). (1.3.4) Displacement of liquid through ventral integumentary grooves. Detected in several representatives of Eupnoi (Bishop, 1950; Holmberg, 1970), this mechanism is found in some cosmetids (Soares & Soares, 1984) and in some gonyleptids of the subfamilies Hernandariinae and Sodreaninae (Hara & Gnaspini, 2003). (1.3.5) Displacement through surface microsculpture. Cyphophthalmi show leg dabbing, which varies when different legs are seized by forceps (Juberthie, 1961d; mechanism 2.2 below). However, when seized by forceps, leg II moves toward the ozopore, and the defensive secretion covers the body surface. In Gonyleptes fragilis (Gonyleptidae) the liquid spreads over the body, including the ocularium, evaporating quickly (Hara & Gnaspini, 2003).

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A

B

C Figure 10.5. Defense of the gonyleptid Goniosoma spelaeum (photos: P. Gnaspini). (A) A male with two droplets (arrows) formed by enteric fluid alone. (B) A female with turbid droplet of secretion (arrow) formed by the mixture of enteric fluid and defensive secretion. (C) A male squirting two jets (white arrows) directly at the offending agent (forceps), which were covered with the defensive secretion (black arrows). Scale bars = 10 mm.

Defense Mechanisms

(2) Mechanisms that direct the liquid toward the offending agent (2.1) Delivering the secretion to the offending agent by retracting a leg toward the harvestman’s body. Leiobunum spp. frequently push a leg against their secretionmoistened body, consequently dousing, for instance, an ant worker that is gripping the leg of the harvestman (Blum & Edgar, 1971). (2.2) Emission of a secretion globule on the gland opening, directed to the offending agent with the legs. This type of emission, known as leg dabbing, has been independently observed in Cyphophthalmi and Laniatores (Cosmetidae). When forceps seize a harvestman leg or body, the animal discharges a droplet of secretion at the ozopore, collects it with a free leg of the same side (in the case of Cyphophthalmi) or the forelegs (for Cosmetidae), and then brushes the wet legs against the seized leg or the offending agent (Juberthie, 1961d; Eisner et al., 1971, 1977). These movements may be repeated while the leg continues to be seized. Duffield et al. (1981) commented that leg dabbing emphasizes the irritant function of some defensive secretions, whereas the use of a chemical shield (1.3.3) emphasizes a repellent or masking function, surrounding the organisms with a chemical shield. (2.3) Squirting the secretion as a fine jet. Independently observed in two families of Laniatores, Triaenonychidae and Gonyleptidae, this emission takes place directly from the gland opening. Therefore, it is probable that there is no previous mixing with the enteric fluid when squirting, a conclusion reinforced by the color of the jet, which resembles the original color of the discharged secretion (Figure 10.5C). This may be a more effective defense mechanism since it releases pure secretions directly onto the offending agent, but is costly since the secretions are not diluted. In Triaenonychidae the jet travels up to 2.5 cm above the carapace in a slightly backward direction (Lawrence, 1938; Maury, 1987). In Gonyleptidae, especially in the large goniosomatines, the jet extends at least 5 cm and very often 10 cm or more (Gnaspini & Cavalheiro, 1998; Machado et al., 2000; Hara & Gnaspini, 2003). It can be emitted in any direction, even forward. Whatever region of the harvestman’s body is handled, the jet emitted usually reaches the offending agent (as in Figure 10.5C). When seized by the fourth pair of legs, the animal may also quickly turn its body backward while emitting the jet, probably enhancing the chance of the secretion hitting and spreading upon the offending agent. As can be seen from Figure 10.5C, this emission occurs through the anterior opening of the ozopore (AO, as in Figure 10.3), specifically through the V-shaped notch (VO) of the slit of the integumentary dome (SL), and not through the posterior opening, as previously thought by Gnaspini and Cavalheiro (1998).

Chemistry The chemical nature of the secretions varies when larger groups are compared and seems to be useful in taxonomic recognition (Table 10.1). In a broad sense, among Laniatores, Gonyleptoidea produce a variety of alkylated benzoquinones and phenols, and Travunioidea produce mainly terpenoids. In contrast, among Eupnoi,

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Sclerosomatidae secrete short-chain acyclic ketones and alcohols, whereas Phalangiidae produce naphthoquinones, considered to be rare as natural products (Roach et al., 1980). The only study available for species of Cyphophthalmi indicates the presence of a series of saturated and unsaturated methyl ketones and naphthoquinones (Raspotnig et al., 2005). As mentioned earlier, many harvestmen mix their defensive compound(s) into the aqueous enteric fluid. The mixture is needed for at least two reasons: (a) the animal may dilute the compound that is costly to produce and store it in a low concentration before its use, and (b) some compounds, such as benzoquinones, are unstable in water and hence are unsuitable for long-term storage in aqueous solution (Eisner et al., 1971). In addition, as seen from Table 10.1, most species use mixtures of chemical compounds. At least among Laniatores, the use of a mixture may also be adaptive since benzoquinones individually are crystalline at ambient temperatures and could not be stored alone. In mixture the melting point decreases, providing the animal with a fluid, and hence appropriately dispensable, glandular content (Eisner et al., 1971). However, in a few gonyleptid species only one compound has been detected (Hara et al., 2005).

Effectiveness of chemical defense against potential predators The main function attributed to the scent secretion is defense against predators (reviewed in Holmberg, 1986). Experiments in the laboratory have shown that ants are promptly repelled by harvestman secretions (Blum & Edgar, 1971; Eisner et al., 1971, 2004; Duffield et al., 1981). When worker ants encounter secretion, they immediately release their mandibles, move away, and begin wiping their mouthparts on the substrate. Naturalistic observations show that some spiders may also be deterred by the harvestman secretion (e.g., Cloudsley-Thompson, 1958; Juberthie, 1976; but see Bristowe, 1941; Immel, 1954). However, Eisner et al. (2004) experimentally demonstrated that the secretion of Acanthopachylus aculeatus was unable to deter the attack of a lycosid spider. Live individuals of A. aculeatus were consistently rejected by the spiders immediately on contact, even before they released their defensive secretions. The authors hypothesized that A. aculeatus may contain additional chemical factors on the integument that can be repellent to spiders. Previous studies have already reported that individuals of the ctenid spider Enoploctenus cyclothorax attack harvestmen, such as Goniosoma spp. and Discocyrtus spp., but immediately retreat, avoiding biting the prey (Sabino & Gnaspini, 1999; Machado et al., 2000; Willemart & Kaneto, 2004). Among vertebrates, scent-gland secretion effectiveness seems to vary according to the taxon of the predator. Certain frog species, for instance, present strong aversive responses (e.g., Edgar, 1971), whereas others regularly include harvestmen in their diet (see references in Chapter 9). Lizards of the genus Anolis (Polychrotidae) ignore Stygnomma spiniferum experimentally offered in the laboratory (Duffield et al., 1981). However, some mammals, such as the Neotropical opossums Didelphis spp. and Philander opossum (Didelphidae), are important harvestman predators (Pelle-

Defense Mechanisms

gatti-Franco & Gnaspini, 1996; Cáceres & Monteiro-Filho, 2001; Cáceres, 2002; see also Chapter 9). Young chicks generally take no phalangiids or sclerosomatids (Holmberg, 1970), but many bird species regularly feed on harvestmen and apparently have no aversive response to the secretion (references in Chapter 9).

Physiological, clastogenic, and antibiotic action of the defensive secretions After the first chemical identification of a harvestman defensive compound by Estable et al. (1955), researchers from the same laboratory made several studies on the effects of such compounds. Fieser and Ardao (1956) noticed that the mixture of benzoquinones has remarkable antibiotic properties, being bacteriostatic against Gram-positive and Gram-negative bacteria and protozoa. When given orally to mice infected with intestinal parasites, the compound is tolerated perfectly, destroying giardias, trichomonas, and hexamites (Estable et al., 1955). Cole et al. (1975) also recorded antifungal properties. Ardao and Freyre (1956) noted that benzoquinones increase respiration in mammalian erythrocytes, being evidently a catalyst in hexose monophosphate oxidation, but do not affect anaerobic glycolysis. Sáez and Drets (1958) recorded that benzoquinones interfere with cell metabolism, disturb and inhibit growth and cell division in both plants (onion meristem root-tip cells) and animals (orthopterans’ meiotic cells), and have important mutagenic properties. Freyre et al. (1958) recorded that doses as small as 10 mg/kg by intravenous and intraperitoneal injections are enough to kill a rat almost immediately because of respiratory failure and cyanosis, whereas subcutaneous and intramuscular injections only produce local reaction (including pain, inflammatory reaction, and necrosis). Administration directly into the stomach does not visibly harm rats and dogs, but doses higher than 100 mg/kg led to death. Drets et al. (1982) detected clastogenic action of benzoquinones in human peripheral leukocytes and in mouse bone-marrow cells, both in vitro and in vivo. However, it should be noted that the amount of secretion available in each live harvestman ranges from tens to hundreds of micrograms, which is much smaller than that used in laboratory tests (Fieser & Ardao, 1956; Eisner et al., 1971). These chemicals have been recorded to produce no reaction on human skin except intense dermal irritation (Capocasale & Bruno-Trezza, 1964). Consistent with this, direct contact during a two-year field study produced no skin reaction except harmless temporary stains, whereas when the nose mucosa was penetrated by the jet, it produced painful reactions (P. Gnaspini, pers. obs.).

Other uses of the scent-gland secretions Bishop (1950) was the first to suggest that scent-gland secretions in harvestmen could be used for intraspecific communication. He recorded two types of secretions from Leiobunum aldrichi: a clear one, probably the enteric fluid, and a milky one, probably the defensive secretion. According to him, the primary function of the clear

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secretion is not protective but, rather, a means of communication. The clear secretion appears as a transparent bubble at the gland opening and drains almost immediately to the lower side of the body, where it may come in contact with the surface over which the harvestman is moving. On the basis of this observation, Bishop (1950) proposed that individuals could deposit chemical signals on the ground as trail markers, but this has not been demonstrated experimentally. The hypothesis that the scent secretion could be used as a trail marker is consistent with the fact that different individuals sometimes follow the same route to a particular spot from distances of several yards, testing the ground before them with the tips of the second legs. Gnaspini (1996) also detected that individuals of Goniosoma spelaeum almost always follow the same routes when leaving from and returning to the caves where they spend the day. This behavior was considered to be related either to chemical marks or spatial memory; however, no harvestmen have ever been observed marking the substrate. Since crystals inside the gland sacs are found in larger numbers in cave-restricted species than in facultative ones, Juberthie et al. (1991) suggested that the defensive secretions could also be used for territorial delimitation and as aggregation or sexual pheromones. Holmberg (1986) also suggested that harvestman secretions could be used for sexual recognition. However, this hypothesis is unlikely since other glandular structures (on the chelicerae and legs) have been found that serve these functions (Martens & Schawaller, 1977; Martens, 1979). Moreover, no chemical difference exists between the secretions from males and females (Meinwald et al., 1971), as would be expected if these substances had a sexual role (Blum, 1985). Clawson (1988), however, observed that scent secretions of Leiobunum spp. may be used in a reproductive context. In this case females turn themselves over and rub the defense tubercle over the area on which they lay eggs. The secretion could be used for marking of egg sites and might also serve to repel other females and minimize multiple ovipositions in the same place (see Chapter 12). Many harvestmen species show gregarious habits and form dense diurnal aggregations consisting of nymphs and adults of both sexes (see Chapter 11). Wagner (1954) suggested that the secretions produced by the scent glands play a role in mutual attraction. This author discovered an aggregation of nearly 70,000 Leiobunum “cactorum” in the lowest fork of the branches of a candelabrum cactus. Since no aggregation was found in nearby cacti, he assumed that the scent glands release a pheromone that attracts other individuals over 5 meters’ distance. Animals that are forcibly removed attempt to reach the aggregation from as far as 30 meters away. The animals are not only attracted by a favorable location (the cactus protecting against adverse climatic conditions), but also by the community, thus coordinating their behavior to a certain extent. Again, no experimental demonstration was provided, so the aggregation pheromone function remains an untested hypothesis. It is also possible that upon disturbance of the group, the secretion could serve to elicit an alarm response. Indeed, group living is a prerequisite for the evolution of alarm signals, and these substances have been identified in many gregarious species of treehoppers, aphids, true bugs, water striders, and social insects, such as termites,

Defense Mechanisms

wasps, bees, and ants (Blum, 1969; Hölldobler, 1977). The alarm function of the scent-gland secretion in harvestmen was first proposed by Anuradha and Parthasarathy (1976), who studied aggregations of Gagrellula saddlana from India. These authors suggested that the secretion the harvestmen exuded when disturbed could act as an alarm pheromone and simultaneously function as a defense mechanism, because it often causes a localized disturbance. Indeed, scent-gland secretion has been experimentally demonstrated to contain alarm pheromones in aggregated Acutisoma aff. proximum (Machado et al., 2002; see also Chapter 11). Finally, Cloudsley-Thompson (1958) and Savory (1962) recorded that the defensive secretion seems to be anesthetic to specimens of the same species when many are kept together in a jar. However, this may simply reflect an artificial effect of the secretion as a fumigant.

CONCLUDING REMARKS Defenses of harvestmen constitute a wide field of scientific investigation that has already provided a great deal of information, as witnessed in this chapter. There is a clear bias toward studying chemical defense, which would be expected since the presence of defensive glands is one of the most conspicuous synapomorphies of Opiliones. Notwithstanding the detection of many morphological, behavioral, and chemical defense mechanisms, many are far from being functionally understood. Therefore, it would seem that the description and understanding of these features remain in a nascent stage. In addition to the need for detecting and studying defenses of neglected groups, phylogenetic analyses will also contribute to our understanding of the wide evolutionary diversity of the defense mechanisms in harvestmen. Many doors remain to be opened; however, more important, the first steps have already been taken.

ACKNOWLEDGMENTS We are deeply indebted to S. Hoenen, G. Machado, and three reviewers for their critical review of the manuscript, and to the researchers (B. A. Buzatto, D. J. Curtis, J. Gruber, G. Machado, and R. Pinto-da-Rocha) who kindly provided photographs to illustrate this chapter. C. F. Lerche helped with the translation of papers in German, and A. Jascow helped with the translation of papers in Russian. Dr. A. A. Ribeiro and E. Mattos allowed and helped in the use of the electron microscope (LMEIBUSP). P. Gnaspini is the recipient of a research grant from FAPESP (00/04686-4) and of a research fellowship from CNPq (300326/94-7), and M. R. Hara received a grant from FAPESP (99/15232-2).

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11

Social Behavior Glauco Machado and Rogelio Macías-Ordóñez

M

any animals live in groups for at least part of their lives, and a significant number of theoretical and experimental studies have considered the costs and benefits of such behavior (reviewed in Krause & Ruxton, 2002). Historically, however, most investigations on gregarious habits have focused on vertebrates and social insects (e.g., Wilson, 1975). A common idea among arachnologists is that most species of arachnids are highly intolerant to conspecifics and thus are predominantly solitary (Cloudsley-Thompson, 1958). Indeed, gregariousness or more complex social interactions are very rare in spiders (Foelix, 1996), scorpions (Brownell & Polis, 2001), solifuges (Punzo, 1998), pseudoscorpions (Weygoldt, 1969), and whip spiders (Weygoldt, 2000). Unlike these arachnid groups, many species of Opiliones seem to be much more sociable. The most widely reported form of sociality in harvestmen involves the tendency to form aggregations. Despite the frequent occurrence of gregarious behavior in the order Opiliones and its heuristic relevance in understanding the evolution of sociality, most reports on this topic are anecdotal. Studies on social behavior of harvestmen are scarce, and the ecological and evolutionary pressures that lead to gregariousness in the group are poorly understood. Nevertheless, several hypotheses have been proposed to explain the adaptive relevance of harvestman aggregations, including mating, defense, and hydro- and thermoregulation (Holmberg et al., 1984; Machado et al., 2000). In this chapter we describe general patterns of harvestman aggregations and also discuss current hypotheses used to explain the evolution of gregariousness in the order Opiliones.

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CHARACTERIZATION OF AGGREGATIONS Types of aggregations Harvestman aggregations consist of three or more motionless individuals, with their bodies 0–5 cm apart from each other and legs extensively overlapping (Machado et al., 2000). Holmberg et al. (1984) created two categories of aggregations based on the degree of compactness of the individuals. In loose aggregations the harvestman bodies are oriented in different directions with the legs held outstretched or flexed. This type of aggregation is common among Laniatores (Figures 11.1A,B) but is also found in several species of Eupnoi (Figure 11.1C). Dense or mass aggregations are characterized by a high density of individuals facing upward with their legs hanging down or intertwined (Figure 11.1D). Aggregations of this type generally consist of several layers of individuals, in which the innermost layer may cling to the substrate by the claws of their pedipalps and/or chelicerae. Individuals in

Figure 11.1. (A) Small aggregation of the gonyleptid Acutisoma proximum inside a cave in southeastern Brazil (photo: P. Gnaspini). (B) Small aggregation of the cosmetid Gryne coccineloides under a fallen tree trunk in Campinas, Brazil (photo: G. Machado). (C) Loose aggregation of a Gagrellinae harvestman on vegetation in Bolivia (photo: H. Höfler). (D) Dense overwintering aggregation of the sclerosomatid Nelima paessleri inside a cave in Canada (photo: R. G. Holmberg).

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the outer layers use their pedipalps and legs to attach to those underneath. Dense aggregations are found only among the Eupnoi, particularly sclerosomatids of the subfamilies Leiobuninae, Gagrellinae, and Gyinae. The density of individuals in harvestman aggregations is probably determined by microclimatic factors, so that under conditions of low temperature and humidity, individuals would tend to crowd (Holmberg et al., 1984). Support for this hypothesis comes from the gonyleptid Acanthopachylus aculeatus, in which the number of aggregations found in the field was negatively correlated with humidity (R2 = 0.56; F = 13.65; p = 0.004; original data from Capocasale & Bruno-Trezza, 1964). Thus, when air moisture decreases, the individuals tend to form fewer and probably denser aggregations. Similar results were experimentally obtained for cockroaches: in 2% relative humidity, individuals of Blattella germanica (Blattellidae) formed dense aggregations; in 30%, only loose aggregations were observed; and in 95–100% relative humidity, the individuals dispersed, not forming aggregations (Dambach & Goehlen, 1999). The reported number of individuals in loose aggregations ranges from 3 to nearly 2,000, and the density of individuals varies greatly. In general, dense aggregations have a greater number of individuals, and the density of harvestmen in this type of aggregation may reach 2.5 individuals/cm2 (Holmberg et al., 1984). The largest aggregation recorded so far belongs to the sclerosomatid Leiobunum “cactorum,” with nearly 70,000 individuals grouped on a candelabrum cactus in a Mexican desert (Wagner, 1954). Nelima paessleri (Sclerosomatidae) also forms large masses inside caves that may reach 20,000 individuals per aggregation (Holmberg et al., 1984; Figure 11.1D).

Composition Harvestman aggregations are mainly composed of subadults and adults of both sexes, and the presence of early instars is rare. In aggregations of Goniosoma albiscriptum and Acutisoma longipes (both Gonyleptidae), nymphs are usually absent and only occasionally account for up to 5% and 7% of the individuals in any group, respectively (Machado et al., 2000; Willemart & Gnaspini, 2004c). The mean sex ratio (么/乆) in aggregations of Acutisoma aff. proximum (1.1) and Leiobunum townsendi (1.0) showed no bias, in contrast to A. longipes (1.8), G. albiscriptum (2.4), and Acanthopachylus aculeatus (2.0), in which the sex ratio was female biased (references in Table 11.1). No precise information exists on the sex ratio for other species, but several studies report no apparent bias (e.g., Holmberg et al., 1984; Coddington et al., 1990). Although detailed molecular studies have not yet been conducted, three main reasons support the thesis that individuals in harvestman aggregations are not genetically related. First, in aggregations of some species, such as L. townsendi, Nelima paessleri, Prionostemma sp., Pachyloidellus goliath, and many Goniosomatinae (references in Table 11.1), individuals move from group to group. Among many social insects (Wilson, 1971) and some social spiders (Rowell & Avilés, 1995), individuals of a colony do not accept the presence of nonrelatives. To avoid mixing, social arthropods may develop complex mechanisms of kin recognition (Fellowes, 1998), and

Social Behavior

403

Table 11.1 Gregarious species of harvestmen, with description of group size and aggregation sites

Taxa

Number of individuals

Aggregation site

Source

EUPNOI Sclerosomatidae, Gagrellinae Cosmobunus granarius [Eu] Gagrellula saddlana [As]

ca. 400 25–1,500

On the walls of a well

Cloudsley-Thompson, 1985

Among bamboo shoots, below or between leaf fronds, and in rock crevices

Anuradha & Parthasarathy, 1976

Prionostemma sp. 1 [CA]

207

Crowns of spiny palms

Coddington et al., 1990

Prionostemma sp. 2 [CA]

107–300

In crannies on cliffs, in hollow tree trunks, on the stone wall of a cattle watering trough

Coddington et al., 1990

Prionostemma wagnerii [NA]

some hundreds

Along banks of water channels

Wagner, 1954

Sclerosomatidae, Leiobuninae Leiobunum aldrichi [NA]

3–58

On tree trunks, on the underside of a rock ledge

Bishop, 1950; Edgar, 1971; Cockerill, 1988

Leiobunum alvarezi [NA]

many

On vegetation

Soto, 1980

Under logs, within cavities of fallen trunks, and under fallen palmetto fronds

J. F. Anderson, 1993

Candelabrum cacti

Wagner, 1954

Leiobunum aurugineum [NA]

more than 20

Leiobunum “cactorum” [NA]

70,000

Leiobunum desertum [NA]

?

Along banks of water channels

Wagner, 1954

Leiobunum flavum [Eu]

?

?

Martens, 1978b

On vegetation

Dugés, 1884

?

Martens, 1978b

Leiobunum ischionotatum [NA] Leiobunum limbatum [Eu]

many several dozen

Leiobunum speciosum [NA]

100

Leiobunum townsendi [NA]

3–324

Nelima elegans [NA]

3–156

Nelima paessleri [NA]

1,520–20,0001

On the wall of a wooden shelter

Cockerill, 1988

On shaded walls of human constructions, on the underside of rock ledges, and cave entrances

McAlister, 1962; Mitchell & Reddell, 1971; Cockerill, 1988

Inside caves

Moseley & Hebda, 2001

Inside caves and mines

Holmberg et al., 1984

many

Inside caves

Martens, 1978b; T. Novak, pers. comm.

hundreds to thousands

Inside caves

Martens, 1978b

Trunk crevices, under rotting logs and stones

Parisot, 1962

Sclerosomatidae, Gyantinae Gyas annulatus [Eu]

Phalangiidae, Phalangiinae Amilenus aurantiacus [Eu] Phalangium opilio [Eu]

?

(Continued)

Table 11.1 Continued

Taxa

Number of individuals

Aggregation site

Source

LANIATORES Cosmetidae Erginulus clavotibialis [CA] Cynortoides cubanus [CA] Gryne orensis [SA]

Metalibitia argentina [SA]

15–20

Under rocks and rotting logs

Goodnight & Goodnight, 1976

?

Under rocks and rotting logs

Juberthie, 1972

Cavities in the ground, under rotting logs, and inside abandoned ant nests

Martínez, 1974

Cavities in the ground

Martínez, 1974

up to 125

ca. 219

Metavonones hispidus [NA]

few

Under rocks

Soto, 1980

Vonones ornatus [NA]

3–50

Under rotting logs, within cavities of fallen trunks, and under fallen palmetto fronds

Goodnight, 1958; J. F. Anderson, 1993

Inside tank bromeliads

Machado & Oliveira, 2002

Inside rock crevices along river margins

Machado, 2002

Gonyleptidae, Bourguyiinae Bourguyia albiornata [SA]

up to 12

Gonyleptidae, Goniosomatinae Acutisoma discolor [SA]

3–10

Acutisoma longipes [SA]

34.2 ± 22.0 (7–200)

Inside caves

Machado et al., 2000

?

Inside caves

M. C. Chelini, pers. comm.

Acutisoma aff. proximum [SA]

Acutisoma proximum [SA]

19.5 ± 18.4 (3–79)

Inside rock crevices along river margins

Machado et al., 2002

Goniosoma albiscriptum [SA]

5.06 ± 1.99 (3–10)

Inside caves

Willemart & Gnaspini, 2004c

Goniosoma aff. badium [SA]

9–34

Inside caves

Pinto-da-Rocha, 1993

Goniosoma catarina [SA]

16–37

Inside rock crevices along river margins

Machado et al., 2000

Goniosoma geniculatum [SA]

30–50

Inside caves

Machado, 2002

Goniosoma sp. [SA]

10–150

Inside caves

Machado et al., 2003

?

Inside caves

P. Gnaspini, pers. comm.

21

Under a rotting log

A. Pérez González, pers. comm.

?

Under rocks and rotting logs

Capocasale & Bruno-Trezza, 1964

3–60

Under rocks or inside rock crevices

Acosta et al., 1993, 1995

7–12

Inside cavities of tree trunks

G. Machado, unpub. data

Goniosoma spelaeum [SA] Gonyleptidae, Gonyleptinae Gonyleptes horridus [SA] Gonyleptidae, Pachylinae Acanthopachylus aculeatus [SA] Pachyloidellus goliath [SA] Stygnidae Protimesius longipalpis [SA]

When the sample size for the number of individuals per aggregation was smaller than 10, only the range (or the available information) is presented. In the remaining cases, the mean ± standard deviation is shown, with the range in parentheses. The geographic occurrence of each species is indicated in square brackets after the species name (As = Asia; CA = Central America; Eu = Europe; NA = North America; SA = South America). 1. This number refers only to dense aggregations.

Social Behavior

nonkin individuals are commonly expelled or cannibalized if they enter a strange group (e.g., Rowell & Avilés, 1995). Apparently, among harvestmen newcomers are tolerated and promptly accepted in the aggregations (Coddington et al., 1990). Second, in several gregarious harvestmen the group size is much greater than the maximum number of eggs laid by an individual female (see also Chapter 12). Finally, in all gregarious species newly hatched offspring disperse and spend at least five instars (2–10 months depending on the species) in solitary life before joining an aggregation. This time lag makes it unlikely that a group would be composed only of related individuals since it would require enormous rates of survivorship from nymphs to adults and also would demand precise mechanisms of kin recognition.

Resting sites and seasonality Harvestman aggregations are more frequently found during diurnal periods in humid, poorly illuminated places, such as under rocks and rotting logs, inside caves, and under dense vegetation (Table 11.1). Just before dusk the aggregations disperse, and the individuals leave their diurnal shelter to forage, a behavioral response that is probably related to the decrease in light intensity (see Chapter 14). Indeed, during a total solar eclipse individuals of the gregarious sclerosomatid Gagrellula sp. began dispersing and then, at the peak of the eclipse, completely evacuated the resting site (Bano, 1983). As recorded for other arthropods (e.g., Rasa, 1997), harvestman aggregations are more commonly found during dry and cold periods and/or in xeric environments. Aggregations of the sclerosomatids Leiobunum desertum, Nelima paessleri, and Prionostemma wagnerii are only found during winter (references in Table 11.1). This trend was also recorded for several gonyleptids, such as Acanthopachylus aculeatus, Cynortoides cubanus, Acutisoma longipes, Goniosoma albiscriptum, Pachyloidellus goliath, and Vonones ornatus (references in Table 11.1). Quantitative field data on a cavernicolous population of A. longipes showed the importance of climate to the tendency to form aggregations: the number of aggregations found per month is inversely correlated with rainfall. Moreover, during the drier periods aggregations of this harvestman migrate to wetter places, closer to the river that crosses the cave (Machado et al., 2000). Aggregations of N. paessleri also accomplish such movements, migrating deeper into the cave during the colder winter months, avoiding the physiological stress imposed by the external climate near the cave entrance (Holmberg et al., 1984). Overwintering aggregations are common among insects, but in Arachnida they are known only for harvestmen and some mites (e.g., Bergh & Judd, 1993). Among harvestmen this behavior is restricted to some members of Eupnoi that occur in temperate regions, where individuals face a rigorous period of snowfall. Unlike most species of the suborder that spend the winter as eggs (Martens, 1978b), Amilenus aurantiacus, Gyas annulatus, Nelima elegans, and N. paessleri spend the cold northern winter as adults. Individuals of these species overwinter inside caves and mines and form large aggregations throughout the snow period (Table 11.1).

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Multispecies aggregations Aggregations consisting of more than one species are very rare among arthropods and have been recorded only for some cockroaches, dermapterans, weevils, and gyrinid beetles (references in Sauphanor & Sureau, 1993; Karlsson et al., 1999). In harvestmen, however, this behavior seems to be common, as several cases have been reported for species of both Eupnoi and Laniatores (Table 11.2). The number of species found in these multispecies aggregations ranges from two to five (Table 11.2). Laboratory observations indicate that individuals of Discocyrtus oliverioi, Discocyrtus sp., and Mischonyx cuspidatus (all Gonyleptidae) collected as isolated individuals in the field always aggregated together, despite the presence of more than one shelter in the terrarium (Elpino-Campos et al., 2001). Generally, one or two very abundant species constitute the great majority of the aggregated individuals (Table 11.2). At least among existing reports on Laniatores, individuals of the predominant species rarely release scent-gland secretions when the aggregations are disturbed, relying mainly on fleeing or crypsis as defense. On the other hand, individuals of the less abundant species commonly release a strong charge of scent-gland secretions upon disturbance (Machado & Vasconcelos, 1998; Elpino-Campos et al., 2001). After discharge, individuals of all aggregated species abandon the resting site (Machado & Vasconcelos, 1998). The occasional presence of individuals of two or more nonsecreting species in aggregations of a species that promptly releases secretion may be interpreted as a means of taking advantage of the chemical volatiles and/or alarm signals produced by individuals of another species. This behavior has been experimentally demonstrated among fish (references in Mirza & Chivers, 2001), and its occurrence may be widespread in terrestrial animals. For species that secrete noxious chemicals, the main benefit of nonsecreting harvestmen in the aggregations may be the dilution effect (Machado & Vasconcelos, 1998). By living in groups, the chemically protected species may decrease the risk of being preyed upon since the probability that another individual may be a victim increases (see discussion later).

WHY DO HARVESTMEN AGGREGATE? The hypotheses proposed thus far to explain the adaptive value of harvestman aggregations may be grouped into three categories: the defensive hypothesis, the physiological hypothesis, and the mating-success-improvement hypothesis (Holmberg et al., 1984; Machado et al., 2000). In this section we will discuss these hypotheses in light of the available information on harvestman biology.

Defensive hypothesis The role of arthropod aggregations in protection from predation is equivocal. Although there is a great amount of information that provides evidence of protection (reviewed in Vulinec, 1990), naturalistic and experimental studies show that some

Table 11.2 Multispecies aggregations of harvestmen with percentage of occurrence of each species, aggregation site, and group size (when available)

Taxa

% of individuals

Aggregation site (group size)

ca. 90

Under the leaves of a campground shelter (25–300)

Source

EUPNOI+ EUPNOI Leiobunum flavum (Sclerosomatidae)

Cockerill, 1988

Leiobunum vittatum and ca. 10 Leiobunum townsendi (Sclerosomatidae) .......................................................................................................................................................................................................................... Leiobunum flavum and Leiobunum ? Under the leaves of a Cockerill, 1988 vittatum (Sclerosomatidae) campground shelter .......................................................................................................................................................................................................................... Platybunus bucephalus and Rilaena ? Trunk crevices, under rotting Parisot, 1962 triangularis (Phalangiidae) logs and stones LANIATORES + LANIATORES Encheiridium montanum (Gonyleptidae)

50.0

Holoversia nigra (Gonyleptidae)

4.8

In the base of clumps of roots (5–34)

Machado & Vasconcelos, 1998

Eugyndes sp. (Gonyleptidae) 45.2 .......................................................................................................................................................................................................................... Discocyrtus oliverioi (Gonyleptidae) 17.0 Under rocks and rotting logs Elpino-Campos et al., 2001; (8–66) Pereira et al., 2004 Discocyrtus sp. (Gonyleptidae)

9.5

Mischonyx cuspidatus (Gonyleptidae) 73.5 .......................................................................................................................................................................................................................... Acanthopachylus aculeatus Many Under rocks and rotting logs Capocasale & Bruno-Trezza, 1964 (Gonyleptidae) Pachyloides thorelli (Gonyleptidae) Few .......................................................................................................................................................................................................................... Mischonyx cuspidatus, ? Under rocks and rotting logs Mestre & Pinto-da-Rocha, 2004 Discocyrtus sp. 1 and sp. 2, Geraecormobius sp., and Tricommatinae sp. (all Gonyleptidae) EUPNOI + LANIATORES Holmbergiana weyenberghii (Sclerosomatidae)

?

Gryne orensis (Cosmetidae)

?

Metalibitia argentina (Cosmetidae) Hernandaria scabricula (Gonyleptidae)

Cavities in the ground and under rotting logs

Martínez, 1974

Many ?

Discocyrtus testudineus (Gonyleptidae) Few .......................................................................................................................................................................................................................... Leiobunum aurugineum ? Under fallen trunks J. F. Anderson, 1993 (Sclerosomatidae) and Vonones ornatus (Cosmetidae)

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vertebrate predators may feast on aggregated individuals (e.g., Mattson et al., 1991), and that larger groups suffer more severely from predation (Uetz & Hieber, 1994). Group living in harvestmen may confer defensive advantages to individuals in four ways (Machado, 2002). First, aggregations may strengthen the intensity of the repulsive signal of the scent-gland secretions toward predators (Holmberg et al., 1984; Machado et al., 2000). Chemical studies have shown that the secretions produced by harvestmen are mainly benzoquinones, phenols, alcohols, ketones, and aldehydes (Chapter 10), which are widespread predator deterrents among arthropods (Blum, 1981). If more than one individual is disturbed in an aggregation, they will collectively release defensive secretions (Holmberg et al., 1984; Machado et al., 2000). A similar behavior was observed among cockroaches inhabiting ground litter: individuals could use their defensive secretion to repulse nonswarming predators more effectively in a group than when isolated (Grandcolas, 1998). Second, gregariousness in harvestmen may enhance escape capabilities of aggregated individuals because of alarm communication after a predator attack (Machado et al., 2002). Aggregated individuals of Acutisoma aff. proximum experimentally stimulated by the gland exudate dispersed rapidly. Since the alarmed harvestmen bump into other individuals, the alarm reaction is also mechanically spread through the aggregation, resulting in a general erratic scattering of the group. A similar behavior occurs in tight aggregations of silverfish, aphids, and water striders, in which the disturbance promoted by body contacts is used as a cue for approaching danger (reviewed by Vulinec, 1990). It was also shown that larger groups of Acutisoma aff. proximum respond faster to the chemical stimulus, probably because of the increased number of sensorial legs used for surveillance. Finally, gregariousness in harvestmen may confer defense, reducing the rates of predator attacks by two additional means: through the encounter and dilution effects (Turner & Pitcher, 1986; Inman & Krebs, 1987). The encounter effect refers to decreasing the probability that the individuals are found by predators because aggregation reduces the overall frequency of prey occurrence, and because detection of large, three-dimensional groups does not increase proportionally with group size (Uetz & Hieber, 1994). The dilution effect favors being in an aggregation by decreasing the individual probability of being attacked once the predator finds the group (Krebs & Davies, 1993). When these two effects are considered together, operating simultaneously, they are known as the attack-abatement effect (Turner & Pitcher, 1986). If the attack-abatement effect also operates on harvestman aggregations, one may postulate that individuals will prefer to join larger groups. However, an experimental study on the gregarious Prionostemma sp. showed that individuals were indifferent to group size and tended to stay with the first group they encountered. The same study also demonstrated that individuals were not more likely to remain in larger aggregations, once chosen (Coddington et al., 1990). Since this study was conducted with captive specimens and was not designed to answer questions related to the attack-abatement effect, these results should be interpreted with caution. It is possible that the relative position of a harvestman within an aggregation may have

Social Behavior

an influence on its decision to remain in or to leave the group since individuals in the periphery of the group have a higher chance of being singled out by predators (Hamilton, 1971). Field experiments are needed to test the advantages of being in a group, as well as the risks faced by individuals in different positions within an aggregation.

Physiological hypothesis A serious problem for arthropods in dry environments is water loss by evaporation through the integument (Cloudsley-Thompson, 1988). Cuticular evaporation is directly proportional to body surface area, so that small animals with their relatively high surface/volume ratio tend to lose water quickly (Hadley, 1994). Harvestmen are more susceptible to dehydration than most other arachnids, probably because of their long legs, resulting in a high surface/volume ratio. This adds a strong selective pressure for the evolution of physiological and behavioral adaptations for reducing water loss (see Chapter 14). Gregariousness in harvestmen could act as a behavioral mechanism for reduction of evaporation among grouped individuals. The close body contact and the intertwining of legs may reduce airflow and thus reduce individual net water loss (Holmberg et al., 1984). Some aggregations of Eupnoi are extremely tight, with the bodies and legs so entangled that the individuals may take as much as 15 seconds to disentangle when disturbed (Coddington et al., 1990). The physiological advantage of gregariousness in water regulation has been recorded for several arthropods, including isopods (e.g., Friedlander, 1965), millipedes (e.g., Dangerfield, 1993), and many insects (e.g., Danks, 2002). Among harvestmen, however, this phenomenon remains to be experimentally tested. Additionally, gregariousness in harvestmen may contribute to a reduction in the metabolic rate of the individuals. At least for the cosmetid Vonones ornatus, the metabolism of aggregated individuals was 12% lower than that of single individuals (J. F. Anderson, 1993; see Chapter 14). A lower metabolic rate reduces energy expenditure and spiracular water loss in several tracheate arthropods, including arachnids (Hadley, 1994). A reduction in metabolism may also be important for extending food reserves in species that overwinter (Holmberg et al., 1984). More studies in the laboratory are necessary to investigate the physiological advantages of group living in harvestmen. In the field it would be important to investigate the importance of microclimatic factors in the choice of resting sites.

Mating-success-improvement hypothesis Aggregations of individuals during or immediately before the mating period may ensure that both sexes are in close proximity. The obvious benefits of group living for reproduction are related to opportunities to gain access to mates, to assess mate quality, and to reduce the search costs for mates. Aggregations, however, also have costs, including direct or indirect competition for access to mates and potential for egg or juvenile predation, which may lead to high variance in reproductive success

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among individuals (Lee, 1994). Many insects form aggregations during their reproductive periods, and the costs and benefits of this behavior have been intensely studied (reviewed in Shelly & Whittier, 1997). Unlike many insects, harvestmen aggregations do not seem to be related to reproduction since the aggregated individuals mostly remain stationary. Furthermore, no record exists of reproductive behavior in or near harvestman aggregations (references in Table 11.1), and no study has suggested any connection between gregariousness and mating behavior. On the contrary, males of some species become intolerant to other males and harass females during mating periods (Chapter 12). Holmberg et al. (1984) also discarded the mating-success-improvement hypothesis since they observed that individuals of Nelima paessleri could mate at the entrance of the overwintering sites without needing to form long-term aggregations. Finally, the period of reproduction in some species does not coincide with the season in which aggregations are found in the field. In Acutisoma longipes (Machado & Oliveira, 1998) and Goniosoma albiscriptum (Willemart & Gnaspini, 2004a), for instance, the reproductive season peaks during the warm and rainy season (October to March), whereas the aggregations are mainly found during the cold and dry season (April to September). Cockerill (1988) did not find evidence that the aggregations of Leiobunum aldrichi in the southern USA had a sexual role. He observed five attempts at copulation, but none were associated with aggregations. However, working with a population of the same species from the northeastern USA, Edgar (1971) recorded “clusters” of L. aldrichi on tree trunks containing from 3 to 58 individuals, composed of both males and females. Although two or more individuals were rarely seen with legs in contact, they were typically found within 10–15 cm of each other. Field observations on these clusters indicated that males occasionally encountered females and attempted to copulate. At the beginning of the reproductive season, females rigorously resisted the approach of the males at first, and when the frequency of copulation attempts increased, the females moved away from the clusters, often to places where clusters did not ordinarily occur (Edgar, 1971). In the middle of the reproductive season, however, females were encountered more frequently by males, and their resistance to mating eventually decreased (see also Chapter 12). According to Edgar (1971), when individuals of L. aldrichi become adults, they grow large enough to be conspicuous on the leaf litter; thus tree trunks appear to provide a more suitable resting place. Immediately before the beginning of the mating season, when most individuals have already developed into adults, females are scarce in the litter, but abundant on tree trunks. Therefore, the location of females is highly predictable, and males go to tree trunks, probably to search for mating pairs. In conclusion, northeastern populations of L. aldrichi do not form aggregations like those observed in the southern USA, and the clusters observed by Edgar (1971) probably resulted from the migration of adult females from the litter to the tree trunks, which served as mating sites.

Social Behavior

EVOLUTION OF SOCIAL BEHAVIOR Preadaptations The great majority of arachnid orders are composed of solitary, predatory species that need to modify their behavior in order to interact with conspecifics. Among spiders and scorpions in particular, this behavioral modification is based on a period of nonaggression or tolerance that, in most species, corresponds to the sexual and parental phases (Foelix, 1996; Mashberg, 2001). The few arachnid species that show social behavior are characterized by a suppression of cannibalistic habits among siblings and an extended association between parents and offspring (Avilés, 1997). At least among spiders (Avilés, 1997), scorpions (Mashberg, 2001), and many insects (see examples in Choe & Crespi, 1997), subsociality is the most common route for achieving more complex forms of social behavior. In harvestmen, however, apparently no direct connection exists between subsocial behavior and the evolution of gregariousness, which weakens the possibility of kinship selection as a selective pressure that could lead to gregariousness in the order. Perhaps the most important behavioral feature that differentiates harvestmen from spiders and scorpions is the lack of cannibalism among subadults and adults. Most records of cannibalism in harvestmen are of adults eating eggs or early instars (see Chapters 8 and 9). The noncannibalistic habits of adults may have favored conspecific tolerance and the evolution of gregarious behavior in harvestmen (Machado, 2002). In a similar way, tolerance to crowding is hypothesized to have an exaptive value in the evolution of gregariousness among cockroaches (Grandcolas, 1998).

Chemical cues Most harvestmen are nocturnally active, nonacoustical, and nonvisual and have a long, slender second pair of antenniform legs. The combination of these features suggests that chemical signals could be important for intraspecific communication in these animals (see discussion in Chapter 10). The finding that the scent-gland secretion may work as an alarm pheromone in some species (Machado et al., 2002) does not exclude the possibility that the very same secretion may have a role as an aggregation pheromone. At least in the leaf bug Nezara viridula (Pentatomidae), the scent secretion, primarily used for defense, can elicit alarm or attract conspecifics, depending on the concentration (Lockwood & Story, 1987). Indeed, Wagner (1954) postulated that individuals of Leiobunum “cactorum” could attract conspecifics to an appropriate resting site through the smell released by their scent-gland secretion. His study, however, did not provide any experimental evidence supporting the existence of an aggregation pheromone in this species. At least in other arthropod groups, such as cockroaches (e.g., Dambach & Goehlen, 1999) and spiders (e.g., Trabalon et al., 1995), aggregating behavior may be induced by a combination of chemical cues, including stimuli originating from the feces, from substrate impregnated with the conspecifics’ odor, from cuticular compounds, and from aggregation pheromones. Most of these stimuli might be used

411

412

Social Behavior

by harvestmen as chemical cues in the aggregation process, but their role in mutual attraction remains to be experimentally demonstrated. Another question to be answered in the future is whether harvestman scent-gland secretions function as an aggregation pheromone or another gland serves this function.

Integrating hypotheses The current hypotheses used to explain gregariousness in harvestmen highlight several adaptive advantages of group living. However, none of them offers an evolutionary route to explain the emergence of such behavior in the order. A hypothetical scenario has been proposed for the evolution of group living in harvestmen that integrates the physiological and the defensive hypotheses (Machado, 2002). Although this hypothesis was based only on data for the highly gregarious Goniosomatinae harvestmen, it can be extended and applied to all gregarious species of Opiliones. According to this hypothesis, physiological constraints acting on individual harvestmen would lead to the selection of sites with appropriate microclimatic conditions (Figure 11.2, step 1). Since sites that present high relative humidity, warm temperature, and dim lighting conditions are probably in limited supply, individuals tend to form aggregations in the few high-quality patches of the habitat (Figure 11.2, step 2). Therefore, microhabitat conditions are suggested as the most important ex-

Figure 11.2. Hypothetical scenario for the evolution of gregariousness in harvestmen (after Machado, 2002).

Social Behavior

ternal factors that promote group formation in harvestmen. Once a suitable site is found by a few individuals, aggregations may grow in size through preferential attachment of individuals, dwarfing the original physiological stimulus. The lack of cannibalism among individuals favors the tolerance among conspecifics, which may be considered a preadaptation to gregariousness (Figure 11.2, step 3). The aggregations composed of individuals with narrow body contact and legs intertwined could work as a behavioral mechanism to control water loss and to decrease energy wasting (Figure 11.2, step 4). Although gregariousness in harvestmen seems to be primarily driven by environmental factors, it may confer several defensive advantages, including strengthening of the defensive signal through the collective release of the scent-gland secretion, promptness to flee a predator attack in response to the alarm signal provided by the scent secretion, and the attack-abatement effect (Figure 11.2, step 5). Revising the extensive literature on insect aggregation, Vulinec (1990) also proposed that the defensive functions of gregariousness in many groups may have evolved as a byproduct of a primarily behavioral response to environmental stress. The defensive functions, allied with the physiological advantages of group living, could outweigh the costs of living in a group and could contribute to the maintenance of gregariousness in harvestmen (Figure 11.2, step 6).

CONCLUDING REMARKS By integrating the physiological and the defensive hypotheses, it is possible to visualize a putative scenario for the evolution of gregariousness in harvestmen. Some steps of the model, such as the existence of an aggregation pheromone and applicability of the attack-abatement effect for harvestmen, must be tested in the future. Moreover, additional studies on the physiological benefits of group living are required both in the laboratory and in the field. Finally, in order to better understand the evolution of gregarious behavior in harvestmen, it is necessary to determine the environmental factors that may trigger aggregation and the costs associated with group living. The inclusion of these costs in the model should make it more robust and realistic.

ACKNOWLEDGMENTS The authors are very grateful to H. Höfler, P. Gnaspini, and R. G. Holmberg for photos presented in this chapter and to T. Novak, A. Pérez González, M. C. Chelini, and P. Gnaspini for unpublished data on harvestman aggregations. The manuscript was greatly improved by comments of P. R. Guimarães Jr., A. J. Santos, B. A. Buzatto, G. R. Santos, M. O. Gonzaga, P. Grandcolas, and R. G. Holmberg. G. Machado is supported by a grant from FAPESP (02/00381-0), and R. Macías-Ordóñez has been supported by DGAPA-UNAM, Lehigh University, and Instituto de Ecología, A.C.

413

CHAPTER

12

Reproduction Glauco Machado and Rogelio Macías-Ordóñez

M

ost Opiliones, as sexually reproducing species, need a mate in order to reproduce. Both males and females must go through a long and hazardous reproductive process that begins with surviving to a reproductive age and involves finding or selecting a mate, persuading a mate to copulate, achieving fertilization and oviposition, and in some cases protecting eggs or young until dispersal. Collectively, all these events may be called mating, and throughout this chapter the actual interaction between male and female that involves genital coupling will be referred to as copulation. Like all arachnids, harvestman fertilization is internal, and females may lay their eggs immediately or even months after copulation. The forms of parental care may include the production of large and heavily yolky eggs, preparation of nests, choice of appropriate oviposition sites, and subsocial behavior. The study of the strategies used by harvestmen to deal with the environment in order to find, interact with, or compete for mates is probably the area that has received the least attention. Most available information consists of anecdotal observations, which frequently include information on their mating strategies. We will use this information in order to put together a giant jigsaw puzzle with most of the pieces missing. The reader is expected to obtain a collection of bits and pieces of what we know about harvestmen mating strategies, glued to a theoretical and systematic framework. Some gaps will be filled with suggested hypotheses ripe for testing, but many others will remain virgin fields for yet more predictions. Additionally, we will integrate life-history traits, sexual behavior, and morphology of the group in order to understand the evolution of maternal and paternal care in harvestmen. It is hoped that this chapter will stimulate the appetite of the readers for more answers.

414

Reproduction

WHY SEX AT ALL? In sexually reproducing species we call males those individuals belonging to the morph that produces small gametes, or sperm cells. Conversely, females are those that produce large gametes, or unfertilized eggs. Some species, however, reproduce asexually by parthenogenesis. Females of some populations in at least a dozen species of Opiliones asexually lay eggs that produce only females (e.g., Phillipson, 1959; Tsurusaki, 1986). At least for two Eupnoi species, Leiobunum manubriatum and L. globosum (Sclerosomatidae), it has been suggested that low vagility and environmental stability may promote parthenogenesis (Tsurusaki, 1986). The disadvantages of sexual reproduction have been reviewed extensively and include the actual costs associated with finding and being accepted by a suitable mate, the costs associated with rejecting unsuitable mates, predation risks associated with reproductive behavior, and the risk of infection by sexually transmitted diseases, to name a few (Johnstone & Keller, 2000). For those populations found in stable environments, in which individuals do not cover great distances, the disadvantages of sexual reproduction may outweigh its advantages in terms of genetic diversity. It is not unlikely that more parthenogenetic populations will be found in the future.

What do males and females look for? Females, by definition, produce larger gametes and therefore require more resources than males. However, this comparison needs to account for male requirements not only to produce gametes, but many other substances that frequently accompany sperm in ejaculates, which in some groups may be as costly as egg production (Birkhead & Møller, 1998; Simmons, 2001). Machado and Raimundo (2001) reviewed the investment of females in egg production in Opiliones. In some species more than half the volume of an ovigerous female may be assigned to eggs (discussed later). Male ejaculates do not seem to represent such a big investment. Although male investment in ejaculates has not been formally assessed in any species of Opiliones, the available information suggests that ejaculates are not particularly costly (reviewed in Juberthie & Manier, 1978). On the contrary, at least in some Eupnoi, such as the sclerosomatid Leiobunum vittatum, males do not seem to be sperm limited, because they may copulate with several females within a couple of hours (Macías-Ordóñez, 1997). Nevertheless, we lack enough data on natural male copulating frequencies and ejaculate costs to make a safer generalization for the entire order. Females may copulate even more often than males (Pabst, 1953; MacíasOrdóñez, 1997), but they do not produce more gametes every time. In all species studied so far, females seem to have control of how soon to lay eggs after one or several copulations with the same or different males, and except in the cases where there is male parental care, on where to lay them (see discussion later). Unlike females, the more males copulate, the more ejaculate they need to produce. In groups such as

415

416

Reproduction

harvestmen, in which there is little investment in ejaculate accessory material (Juberthie & Manier, 1978), ejaculates are relatively cheap. This leads to a pattern common to many animal-mating strategies: female distribution usually follows resource distribution, whereas male distribution usually follows female distribution, or the resources required by females (Emlen & Oring, 1977). It now becomes clear why we need to know the temporal and spatial distribution of resources in the environment if we attempt to understand what males and females do in order to reproduce. A key resource to start with is food, which in the case of Opiliones includes a wide range of items, from rotting fruit to dead arthropods (see Chapter 8). They are not strict predators like most other arachnids, which specialize in large prey and often are equipped with powerful (and costly) killing tools such as strong pedipalps, fangs, or/and venom. Prey availability is frequently a limiting factor for egg production in arthropod predators (e.g., Bradley, 1984; Smith, 1997; Kreiter & Wise, 2001). Thus the number of females that manage to gather enough resources to produce eggs and be receptive may also limit the reproductive opportunities of males. As a consequence, many or most males of these groups end up not mating at all, only a few mate once, and very few (if any) mate more than once (Elgar, 1998). Furthermore, being a tasty source of food, some males are cannibalized after mating. Conversely, Opiliones’ blueprint seems to be that of an omnivore/scavenger (see Chapter 8). Therefore, females seem to have a wider option of resources to gather enough protein and fat to produce eggs, and more receptive females may be available at any one time. Given these conditions, we can state that male Opiliones have a much wider potential to mate several times over their lifetime than other arachnids or predatory arthropods do. When few or no resources are invested in offspring, male reproductive success will be limited mainly by the number of eggs they can fertilize (Kokko & Jennions, 2003). Even in paternal species, offspring guarding may be a way to increase copulating success, as has been suggested in some Opiliones (Machado et al., 2004). Harvestman females, on the other hand, will rarely be limited by access to males and frequently will even sustain harassment costs. Their reproductive success will be limited by the rate of food acquisition and the availability of suitable egg-laying substrate.

THE CYPHOPHTHALMI SPERMATOPOSITOR Males of most arachnid orders use spermatophores and/or modified appendages (pedipalps or legs) to inseminate females. Although some Acari are known to have an aedeagus (Wooley, 1988), the order Opiliones is unique within arachnids in presenting intromittent genitalia derived from the male reproductive tract, at least in the Phalangida (see Chapter 2). No copulatory behavior had ever been observed in Cyphophthalmi until recently, and it has been suggested that members of this suborder might transfer sperm by means of sperm balls or spermatophores (Forster,

Reproduction

A

B

Figure 12.1. (A) Female of the sironid Cyphophthalmus serbicus with attached spermatophore (ventral view). (B) Microphotograph of the main portion of the spermatophore showing the globular structure of its contents and basal part of the tubular appendage with a content that could represent released sperm cells (arrow) (Illustrations: I. M. Karaman, reproduced with permission of the Revue suisse de Zoologie).

1948a, 1952; Juberthie & Manier, 1978; Martens, 1978b). A recent article by Karaman (2005) has confirmed that males of at least two species of Cyphophthalmi, the sironids Cyphophthalmus serbicus and Cyphophthalmus sp., produce a spermatophore that somehow ends up attached to the female (Figure 12.1A). A similar spermatophore has been observed attached to the gonopore of Stylocellus (Stylocellidae) females (Schwendinger & Giribet, 2005). Members of this suborder live in low densities among leaf litter, a complex and sensorially challenging environment, and do not move much. The male genitalia in Cyphophthalmi are not intromittent according to Karaman (2005), but are a spermatophore-laying structure, a spermatopositor (a term first proposed by van der Hammen, 1985). The spermatopositor of Cyphophthalmi is unique in being short, membranous, and undivided when compared with the homologous penis of the rest of Opiliones, which is long, chitinous, and divided into trunk and glans (Martens, 1986; see also Chapters 2 and 4). During spermatogenesis in Cyphophthalmi, spermatids go through a flagellated phase, and the axoneme then retracts and forms an intracytoplasmic ring of dou-

417

418

Reproduction

blets in the mature spermatozoa. This is followed by an aberrant spermatogenesis of half the spermatogonies of each cyst, characterized by spermatid formation subject to otherwise normal transformations, but without an acrosome or DNA. At the heart of each cyst the normal gametes and the atypical cells arrange themselves in a spermatic ball, composed of a central secretion product, an internal concentric layer of normal sperm, and an external concentric layer formed by the atypical cells, which may have a protective role. At this point these spermatic balls are entirely elaborated by the testis (Alberti, 2005); later they are wrapped by the secretion of two annex glands that end at the base of the penis. Thus they can be considered true spermatophores. The ovipositor of Cyphophthalmi is muscular, articulated, and in most species bears a paired sensory organ at the tip (Martens et al., 1981). These traits may enable females to find and assess spermatophores and to transfer sperm. Karaman (2005) noticed that the encapsulated sperm mass is too wide to pass through the duct that connects the spermatophore with the tip of the female ovipositor (Figure 12.1B). This implies at least some female role in sperm transfer through the spermatophore duct. The morphology of the ovipositor may also play a role in the choice of appropriate oviposition sites. In Siro rubens (Sironidae) females insert the long ovipositor into small natural cavities, where the eggs are laid singly and covered with soil debris. Females may lay 10 eggs in one year and up to 50 during their life (Juberthie, 1964). Thus parental investment in this species is restricted to the choice of appropriate oviposition sites. Given the position of Cyphophthalmi in the phylogeny of Opiliones (see Chapter 3), it is possible that egg hiding is the plesiomorphic form of parental investment in the order. There is another relevant fact in the evolutionary scenario of mating behavior in Opiliones. The duct of the spermatophore through which sperm seems to drain is attached to the female’s tip of the ovipositor just at the opening of one of two small paired structures present in most Opiliones, long ago named seminal receptacles (or receptacula seminis according to Blanc, 1880) and confirmed to serve this function at least in one species of Cyphophthalmi, where the sperm may remain viable at least for up to one year (Juberthie, 1964). In fact, the size and position of the seminal receptacles may have played a role in the evolution of immobile aflagellate sperm in Opiliones. Flagella are useless if sperm do not need to travel far inside the female reproductive tract, given that they are received and stored at the tip of the ovipositor. Furthermore, males can place more sperm inside the small sperm receptacles if they lack flagella (see review of the evolution of sperm aflagellarity in Morrow, 2004). Sperm immobility in Cyphophthalmi (as well as in all other Opiliones) implies that females have at least some control over sperm fate and probably fertilize the eggs just before oviposition, at the apex of the ovipositor. In some species males may have gone so far as to try to lay free spermatozoa near the female’s genital opening, approaching the intromittent role that male genitalia play in the remaining suborders of Opiliones. Schwendinger and Giribet (2005) published an anecdotal description of the copulation behavior of a pair of the cavernicolous Fangensis leclerci (Stylocellidae), in which the male hung on the underside of

Reproduction

the female, with his legs tightly embracing her body, male and female facing in opposite directions (Table 12.1). Most arachnid orders, as well as distantly related animals, including Zygentoma, Collembola, Chilopoda, Diplopoda, and plethodontid salamanders, lay spermatophores (reviewed in Proctor, 1998). In all these groups the male may interact with the female to various degrees during spermatophore transfer. In basal groups of Pseudoscorpiones, for instance, the male leaves the spermatophore for the female to find it, whereas in derived groups there is active male courtship. In the second case, males may increase the chances of insemination per spermatophore and reduce production costs (Thomas & Zeh, 1984). In Cyphophthalmi different species seem to do different things, ranging from those in which males abandon spermatophores for females to find them to those in which males play an active role (Schwendinger & Giribet, 2005). Fertilization by means of a spermatophore would imply that males and females may or may not need to find each other in order to reproduce. Only if males could monopolize resources needed by females and/or advertise themselves effectively (probably by using chemical stimuli) would females have to interact with them in order to obtain spermatophores. Given that the internal phylogeny of the suborder is reasonably well known (Giribet & Boyer, 2002), mapping the modes of spermatophore transfer may provide a hypothesis on the evolution of mating strategies within this group. A final implication of spermatophore production in Cyphophthalmi is that, relative to the adult size (Figure 12.1A), this structure seems to represent a large investment by the male because half the gamete production is allocated to protect the viable sperm, not to mention additional protective layers (Juberthie & Manier, 1978). Therefore, direct sperm transfer by means of an intromittent penis, as observed in F. leclerci and species of other suborders, may not only increase insemination success, but enable the male to increase the amount of fertile sperm production by eliminating the expense of potential gametes and other materials in protective layers. As will be evident in the following sections, male and female relative position during F. leclerci copulation sharply differs from that of other suborders. However, it shares two implications with that of other suborders, supported by details provided by Schwendinger and Giribet (2005) and reviewed in more depth in the suborders’ respective sections. One implication is that the male can perform copulatory courtship by “vividly palpitating the anal region of the female with his pedipalps in an alternating manner.” The other is a somewhat complex genital interaction, since after separation “the female dragged the male behind her for a short distance until he became loose,” presumably attached by the genitalia.

THE LONG PENIS AND THE SENSITIVE OVIPOSITOR OF EUPNOI Immobile sperm and internal fertilization All records on mating in the suborder Eupnoi include copulation by means of long and fully intromittent male genitalia through a very long ovipositor (Figure 12.2).

419

Access to females (?)

Rilaena triangularis [Eu]

?

?

Ischyropsalis hellwigii [Eu]

Ischyropsalis luteipes [Eu]

DYSPNOI

?

Mitopus morio [Eu]

Access to females and territories

?

Leiobunum calcar [NA]

Leiobunum vittatum [NA]

Access to females and maybe territories

?

Male fights for

Leiobunum aldrichi [NA]

EUPNOI

Fangensis leclerci [AS]

CYPHOPHTHALMI

Taxa

?

Male taps female with legs I and II and presents her the cheliceral glands

Male taps female with legs I and II and presents her the cheliceral glands

Male rubs the chelicerae on the female dorsum and mounts her

Male mounts the female dorsum

Male-female wrestling of variable duration

No (?)

Male mounts the female from behind while both are walking (?)

Precopulatory interaction

Table 12.1 General features of mating behavior in harvestmen

Dorsum (using legs I and II)

No grasping

Base of legs I (using the pedipalps)

?

Base of legs II (using the pedipalps)

Base of legs II (using the pedipalpal tarsus) and legs I (using the pedipalpal femoral spur)

Base of legs II (using the pedipalps)

Dorsum (probably using all legs)

Male grasping site

Cheliceral gland or pedipalps (using the chelicerae)

Cheliceral gland or at the pedipalps (using the chelicerae)

No grasping (?)

?

Chelicerae (using the chelicerae)1

?

?

?

Female grasping site

Face-to-face (between 90° and 180°)

Face-to-face (between 90° and 180°)

Face-to-face (ca. 90°)

Face-to-face

Face-to-face (ca. 90°)

Face-to-face

Face-to-face (ca. 90°)

Belly-to-belly (male and female facing in opposite directions)

Intromission

? ? ? ? ? ? ?

Access to females (?) Ownership of mud nests

Algidia spp. and Nuncia spp. [NZ]

Bourguyia albiornata [SA]

Discocyrtus oliverioi [SA]

Discocyrtus pectinifemur [SA]

Goniosoma albiscriptum [SA]

Goniosoma spelaeum [SA]

Promitobates ornatus [SA]

Zygopachylus albomarginis [CA]

Access to females

?

Acutisoma longipes [SA]

LANIATORES

Trogulus nepaeformis and T. tricarinatus [Eu]

Paranemastoma quadripunctatum2 [Eu]

Male and female tap each other

No (?)

?

?

Male briefly taps female with legs II

No interaction(?)

?

Male briefly taps female with legs II

?

Male briefly taps female with legs II

No interaction (?)

?

Base of pedipalps (using the pedipalps)

Base of pedipalps (using the pedipalps)

Base of pedipalps (using the pedipalps)

Base of legs II (using the pedipalps)3

Base of pedipalps (using the pedipalps)

Base of pedipalps (using the pedipalps)

Base of pedipalps (using the pedipalps)

Base of pedipalps (using the pedipalps)

Dorsum (using legs I and II) and chelicerae (using the chelicerae)

Pedipalps (using the pedipalps)

?

Pedipalps (using the pedipalps)

Along the dorsal scutum (using the pedipalps)

?

?

No grasping (?)

?

?

Pedipalps (using the pedipalps)

Chelicerae (using the chelicerae)

Pedipalps (using the pedipalps)

(Continued)

Face-to-face (ca. 90°)

Face-to-face (ca. 90°)

Face-to-face (between 90° and 180°)

Face-to-face (ca. 90°)

Face-to-face (ca. 90°)

Face-to-face (ca. 90°)

Face-to-face (ca. 90°)

Face-to-face (ca. 90°)

Face-to-face (ca. 90°)

Belly-to-belly

Face-to-face

?

Rilaena triangularis [Eu]

?

?

Trogulus nepaeformis and T. tricarinatus [Eu]

No (?)

Ischyropsalis luteipes [Eu]

Paranemastoma quadripunctatum2 [Eu]

No (?)

Ischyropsalis hellwigii [Eu]

DYSPNOI

?

Mitopus morio [Eu]

Yes

?

Leiobunum calcar [NA]

Leiobunum vittatum [NA]

?

?

Multiple intromissions

Leiobunum aldrichi [NA]

EUPNOI

Fangensis leclerci [AS]

CYPHOPHTHALMI

Taxa

Table 12.1 (continued)

Mutual cheliceral rubbing (male also taps female with his legs)

Male taps female dorsum with legs I

Mutual leg tapping

Mutual leg tapping

Mutual leg rubbing

?

Mutual cheliceral and leg rubbing

?

?

Male taps female anal region

Copulatory courtship

No guarding (?)

No (after copulation the mating pair flee from each other)

No guarding (?)

No guarding (?)

No guarding

?

The male holds a female leg (using leg I) and fights with males that approach her

No

Male taps female legs with his legs II

?

Mate guarding

?

?

?

?

?

?

Resource-defense polygyny

?

Resource-defense polygyny (?)

?

Mating system

No

No

No

No

No

No

No

No

No

No (?)

Parental care

Pabst, 1953

Immel, 1954

Martens, 1969c

Martens, 1969c

Immel, 1954; Parisot, 1962

CloudsleyThompson, 1948

Macías-Ordóñez, 1997, 2000 (see also Edgar, 1971)

Bishop, 1949a; Edgar, 1971

Bishop, 1950; Edgar, 1971

Schwendinger & Giribet, 2005

References

?

? ? ? ?

?

?

Bourguyia albiornata [SA]

Discocyrtus oliverioi [SA]

Discocyrtus pectinifemur [SA]

Goniosoma albiscriptum [SA]

Goniosoma spelaeum [SA]

Promitobates ornatus [SA]

Zygopachylus albomarginis [CA]

?

Male taps female dorsum with legs I

?

?

Male taps female dorsum with legs II

Male taps female dorsum with legs I and II

Male taps female dorsum with legs I and II

?

Male taps female dorsum with legs II

Male taps female dorsum and substrate around her

No guarding

Male waves legs II over female and taps her dorsum

Yes (no detailed description)

No guarding (?)

No guarding

Male waves legs II over female and taps her dorsum

?

Male waves legs II over female and taps her dorsum

Polyandrous

?

?

?

?

?

?

?

Harem

Paternal

No

Maternal

Maternal

Maternal

Maternal

Maternal

No

Maternal

Rodríguez & Guerrero, 1976; Mora, 1990

G. Machado & R. Macías-Ordóñez, unpub. data

Gnaspini, 1995

Willemart & Gnaspini, 2004a

Matthiesen, 1983

Elpino-Campos et al., 2001

Machado & Oliveira, 2002; G. Machado, unpub. data

Forster, 1954

Machado & Oliveira, 1998

The geographic occurrence of each species is indicated in square brackets after the species name (AS = Southeast Asia; CA = Central America; Eu = Europe; NA = North America; NZ = New Zealand; SA = South America). 1. Only during intromission (R. Macías-Ordóñez, pers. obs.). 2. Immel (1954) observed mating in Paranemastoma quadripunctatum with very weak light and did not record any evident precopulatory courtship. The species, however, presents cheliceral glands (cf. Sˇilhavy´ 1967b), and they may serve the same function as in Ischyropsalis hellwigi and I. luteipes (Martens, 1969c). In fact, Meijer (1972) observed that males of N. lugubre caught during the reproductive season presented a gelatinous secretion adhering to the hairs of the cheliceral apophysis. The same occurred with males of Mitostoma chrysomelas. 3. Matthiesen (1983) states that male grasping occurred at the base of legs I. He was probably influenced by the literature on Eupnoi (all that was available at the time of his article), and his description of the male grasping may be a mistake.

?

Yes

Algidia spp. and Nuncia spp. [NZ]

Acutisoma longipes [SA]

LANIATORES

424

Reproduction

A

B

D

C

E

F

Figure 12.2. (A) Female (left) of the sclerosomatid Leiobunum vittatum resisting male advances by keeping the frontal end close to the substrate and thus obstructing the entrance to the vagina. (B) Intromission and pedipalp grasping in L. vittatum. The female (right) taps the base of the male front legs with her pedipalps and the base of the penis with her chelicerae. Although not shown in this picture, their front legs are intertwined and rub each other. (C) When the grasping is released, the male guards the female by curling the terminal tarsi of his leg I around one of the female femurs (inset) and follows her as she probes potential oviposition sites. (D) Female inserting her long ovipositor in a rock fissure while searching for appropriate oviposition substrate (photos: J. G. Warfel). The inset shows the egg batch inside the rock fissure. Scale bars = 5 mm. (E) A schematic representation of the oviposition event of the same species showing the ovipositor inserted in the rock fissure (drawing by A. Midori). (F) Everted ovipositor of a Eupnoi harvestman (modified from Eisenbeis & Wichard, 1987; drawing by M. R. Hara).

Reproduction

As in other suborders of Opiliones, Eupnoi mature spermatozoa lack a flagellum and therefore the ability to move (Morrow, 2004). According to Blanc (1880), Eupnoi sperm travel inside the male by secretions of the epithelium cells to the muscular bag of the deferent channel. The sperm somehow end up near the tip of the ovipositor inside the seminal receptacles, at least in Cyphophthalmi (Juberthie & Manier, 1978) and Eupnoi (Blanc, 1880). The tip of the penis must then deploy the sperm near or inside the seminal receptacles, connected to the vagina by a very thin and short channel. According to de Graaf (1882b), in Eupnoi the seminal receptacles also receive the secretion of cementing glands located at the apical lobes, although this may require verification. This secretion could be a medium for sperm flow and also for egg attachment. On its way out, the egg forces expansion of the tip of the oviduct, and this pressure forces the secretion and the imbibed sperm out of the seminal receptacles, bringing them in contact with the egg. The sperm enters the egg through micropilar openings of the egg, after which a chorion is formed (Blanc, 1880; see also Chapter 13). As in Cyphophthalmi, females most likely have some control over the tailless immobile sperm and fertilize eggs just before they exit the ovipositor. A retracted ovipositor inside the female’s body, however, is an evolutionary challenge for males attempting insemination. We do not know how male Cyphophthalmi deal with that, but in the case of Eupnoi males seem to have ventured further in. Copula duration in Eupnoi is highly variable and can be very long (Edgar, 1971; Macías-Ordóñez, 1997; Okada & Tsurusaki, 2004), but in some cases it consists of repeated genital intromissions while male grasping is maintained (Table 12.1). This grasping is characteristic of Eupnoi: the male hooks his long, sexually dimorphic pedipalps by the base of legs II, near the trochanter (Figure 12.2B). In some species, such as the sclerosomatid Leiobunum calcar, the morphology of their long pedipalps is noticeably shaped, including a femoral spur that also holds the female’s leg I in a way that loosing that grasp seems especially difficult (Bishop, 1949a). Among 11 Japanese species of the curvipalpe group of Leiobunum, males of those species in which females may reproduce asexually (L. manubriatum and L. globosum) have larger and more powerful pedipalps than in congeneric species, presumably as a result of selection to counteract female reluctance to reproduce sexually (Tsurusaki, 2004).

Tactile courtship or forced copulation? Most reports mention lack of evident courtship but some female reluctance before copulation, or in some cases total rejection of the male advances by keeping the frontal end close to the substrate, obstructing the entrance to the vagina (e.g., Roters, 1944; Edgar, 1971; Macías-Ordóñez, 1997; Figure 12.2A). When copulation does occur, female cooperation seems to be evident in many cases, sometimes by simply making the genital opening accessible to the male (Immel, 1955; Edgar, 1971; Macías-Ordóñez, 1997), adopting a perpendicular position during intromission (Figure 12.2B; Table 12.1), or even manipulating the penis in a way that may appear to guide it (Parisot, 1962). This cooperation may not be forced by pedipalp

425

426

Reproduction

grasping since the female can still avoid intromission when grasped by lowering the genital opening (Edgar, 1971; Macías-Ordóñez, 1997) or by maintaining the genital operculum closed. Mutual stroking, rubbing, and pulling using legs, chelicerae, and pedipalps are also reported to occur during copulation, during and between intromissions in Leiobunum vittatum (Macías-Ordóñez, 1997; Table 12.1 and Figure 12.2B). Interactions between male genitalia or chelicerae and the female’s mouthparts, as well as female grasp of the male genitalia, may suggest that some kind of nuptial gift is also obtained by the female (W. G. Eberhard and J. W. Shultz, independent pers. comm.). This, however, remains to be confirmed. Most Eupnoi lack the ability to form images, and they are equipped, at best, with a pair of simple median eyes that allow them to perceive changes in light intensity (Curtis, 1970; Franklin, 1985). Moreover, no attempt to find any ability to detect airborne chemical or vibratory information in Eupnoi has been successful (Edgar, 1963). However, their very long legs are equipped with highly sensitive chemo- and mechanoreceptors (Willemart & Gnaspini, 2004b). Therefore, if there is any courtship, information is transmitted through channels that have gone unnoticed by humans. Once a male and a female establish physical contact, the flow of information may be abundant by means of chemical or vibratory cues transmitted through the legs. The period between first contact and female acceptance (or rejection) is usually brief (e.g., Parisot, 1962; Edgar, 1971; Macías-Ordóñez, 1997). This period usually includes wrestling (Macías-Ordóñez, 1997). To our (frequently biased) human eye, the male seems to be attempting to force copulation and the female seems reluctant (Cloudsley-Thompson, 1948; Parisot, 1962; Edgar, 1971; Macías-Ordóñez, 1997). The male grasp in Eupnoi seems hard to loosen (Figure 12.2B), but so far we have no way to know to what extent a female is really able to escape from it. Although short, the period between the first contact and the first intromission or rejection may be a period of tactile precopulatory courtship in Eupnoi and other harvestmen with similar traits. From this perspective, the line between honest courtship and dishonest seduction, or even all-out forced copulation, is blurry and has been the topic of much research and debate in evolutionary ecology in recent years (e.g., Birkhead, 2000; Eberhard, 2000; Kempenaers et al., 2000; Pitnick & Brown, 2000). Females are expected to be under strong selection to accept or reject male attempts in relation to the net benefit of this decision. We must highlight a crucial fact: females do not commit to fertilization of their gametes by merely accepting copulation. Once the male and the female interact inside the female reproductive tract, the female has more control over the fate of the male’s gametes, even more so once the male and his genitalia are not there any more (Eberhard, 1996). The elaborate and highly diverse male genitalia of Eupnoi and other Opiliones (see Chapters 2 and 4) could be expected under a process of cryptic female choice, a process strictly analogous to the choice exerted by the female to accept a male copulation, but in this case the decision does not involve copulation, but the actual fertilization of the egg. This decision is “cryptic” to the male and, obviously, to the observer.

Reproduction

Egg fertilization at the tip of the ovipositor just before it is laid, along with sperm lacking all movement, seems to be enough to suggest that females have at least some control over sperm fate. Female of some Cyphophthalmi species, however, may have even more control if they never must deal with an intromittent penis. Intromittent genitalia may promote insemination. The Eupnoi penis may be the male response to a “disadvantageous” lack of control over insemination in early Opiliones. Nevertheless, forcing gamete fertilization is a different story. Such a likely male evolutionary attempt to take sperm closer to the eggs by an intromittent penis apparently fell in “the female’s court” (sensu Eberhard, 1996), and consequently under the female’s rules. Morphological descriptions show the retracted ovipositor contained in a sheath that may be extended or reduced by muscular action and hydraulic pressure (Martens et al., 1981) and the action of its articulated walls (see Chapter 2). Nevertheless, the detailed interaction of the male penis with the female reproductive tract, and therefore, to what extent the tip of the penis may reach the seminal receptacles, is unknown. However, the diverse and elaborate ornamentation of male genitalia in Eupnoi is to be expected if female reproductive decisions are influenced by male stimulation of the female reproductive tract during intromission, an evolutionary process analogous to those that produce highly diverse visual and acoustical display ornamentations in animals in which females use such cues to evaluate potential mates. Female ovipositors are loaded with highly sensitive organs, especially at the apical lobes, probably the result of selection to find an optimal substrate for egg laying (discussed later). These lobes are the door to the vaginal lumen and its seminal receptacles. A likely scenario is that the tip of the male penis must “court” (stimulate) the sensitive apical lobes in order to open them. Furthermore, leg, pedipalp, and chelicera rubbing and stroking observed during copulation may be part of complex and simultaneous copulatory courtship, male attempts to influence female decisions and female attempts to get enough information to make a good decision herself. In short, given the facts that female Eupnoi cannot detect, much less assess, a potential mate before physical contact, and upon contact their chances to avoid grasping and probably intromission are at least somewhat reduced (or implicitly more costly in terms of energy, injury, or predation risk), it is to be expected that any trait that enables them to exert cryptic choice will be under strong selection. Unlike courtship in other arachnids in which males must first “persuade” the female not to consider them as prey, a process that may require a careful approach and a longdistance, elaborated, highly stereotyped, and species-specific visual or vibratory set of displays, courtship in Eupnoi and other suborders may be quick and tactile before intromission and extend during and after copulation.

Mating systems Field studies on Eupnoi reproductive strategies are scarce. Okada and Tsurusaki (2004) found a relationship between sex ratio and two aspects of mating behavior

427

428

Reproduction

among congeneric Leiobunum from Japan: in species with male-biased sex ratios, copulation and postcopulatory guarding last longer, presumably as a response to the intensity of cryptic female choice and sperm competition. In a population of Leiobunum vittatum in the eastern USA that has been the focus of a long-term study (Macías-Ordóñez, 1997, 2000), suitable substrate for oviposition is limited to cracks in rocks and fallen logs. This is a patchy resource that females seek during the short mating season (September and October) before the freezing temperatures that wipe out adults. As can be expected from this resource distribution, a resource-defense polygynic mating system has been adopted. Males actively patrol and fight other males for these rocks. There is no food or shelter on rocks, and their strong orange coloration (probably an aposematic warning of their bad taste; see Chapter 10) actually makes them quite conspicuous against the mossy background. Not only resource distribution, but also abundance plays a key role in mating. At any one time about half the rocks available are occupied. However, all rocks are suitable for egg laying, and all are occupied several times throughout the mating season. Males may remain on a single rock from one to four days and then descend to the leaf litter, probably to forage and regain fluids. The complex and ever-changing autumn leaf litter apparently makes it impossible for males or females to establish chemical trails, so when a male leaves a territory, it will usually find a different one within hours or days. As can be expected from the facts described here, in about half the rocks females find a male. Immediately upon contact the male attempts to grasp the female as described earlier (Figure 12.2B). Only at the beginning of the mating season are females expected to be virgin, in which case the advantages of finding males are evident. As the season progresses and females have had more than enough sperm to fertilize all their eggs, and even the opportunity to reject or copulate with more than one male, the advantages of finding new males on rocks are not obvious. When a rock without a male is encountered, females slowly go over the whole surface, inserting their sensitive ovipositors inside rock cracks many more times than the number of eggs they can carry, which suggests that they probe potential sites before laying one or many eggs. This behavior is unattainable when they encounter a male since, on contact, the male also detects the female and will eagerly attempt to grasp her and copulate. As mentioned earlier, the female may reject intromission, but grasping seems harder to avoid. Even if the female could escape grasping, she would need to abandon the rock to do so, thus abandoning also the opportunity to find a suitable oviposition substrate. If copulation proceeds, however, once the grasping is over, the male will guard the female. The guarding male wraps one or two female legs at the femur or tibia with the terminal tarsi of his own leg I (Figure 12.2C) and simply tags along by keeping this evidently weak grasp. The female seems free to probe the rock at will, undisturbed not only by this male, but by any other male, because the guardian will aggressively expel any other approaching male. A guarding male will not attempt copulation if another female is encountered and will only stop guarding when the female abandons the territory. All this implies that by accepting copulation, a female gains the opportunity to have full and harassment-free access to the scarce rock cracks where the eggs may safely spend

Reproduction

the winter. When the end of the season is near, females may encounter and copulate with two or three males within a few hours in their search for oviposition substrate. The protection offered by an accepted resident male may be worth taking and would imply yet stronger selection for cryptic mechanisms to influence the paternity of her eggs. In fact, mate guarding is expected and has been confirmed in animals with lastmale sperm precedence (Alcock, 1994). The work of Edgar (1971) on four species of Leiobunum is less detailed, but its comparative approach sheds yet more light on the relevance of the environmental context to mating strategies and highlights the importance of more field studies. In the population just described, adults of no other species are present during the mating season. In Edgar’s study site, 1,000 km away in central Michigan, four congeneric species coexist: L. aldrichi (77.4%), L. calcar (10.6%), L. vittatum (7.5%), and L. politum (4.5%). In this assemblage L. vittatum males adopt a different mating strategy. No territory defense takes place, nor does any postcopulatory female guarding. There is no mention of a patchy egg-laying resource since females use fissures on fallen trunks, which are widespread and abundant. Males of L. aldrichi, however, do fight among themselves for territories and females and will guard them after copulation, just as L. vittatum does in eastern Pennsylvania. Males of L. calcar copulate for periods of up to two hours with repeated intromissions like those observed in L. vittatum in Pennsylvania, but do not guard females. The presence of congeneric species probably influences, among other factors, resource availability and sperm competition risk and therefore has an effect on mating strategies. The temporal distribution of resources is also expected to play a key role; in less seasonal latitudes adults may be found for longer periods or even throughout the year (see Chapter 7), and the optimal conditions for egg laying may be quite different, all of which will imply different selective pressures on mating strategies. Reproductive strategies in Eupnoi could be extremely diverse. The described populations most likely represent a small and probably biased fraction of what can be found. Information as simple as how the male and the female genitalia interact during copulation, or the spatial and temporal distribution of their reproductive resources, would greatly help to better understand their mating systems. Most empirical tests on these ideas in groups with intromittent genitalia have been made on mammals and insects (e.g., Edwards, 1993; Eberhard, 1996; Birkhead & Møller, 1998). Since the male penis has independently evolved in Opiliones, the group offers an ideal opportunity to explore sexual selection theories in a phylogenetically independent clade.

Hiding eggs Eupnoi females seem to rely on their long and sensitive ovipositor in order to find suitable substrate and lay eggs deep in the substrate (Figures 12.2D–F). Leiobunum vittatum females insert the ovipositor inside many natural fissures, but only a fraction of these places are actually used for oviposition. Females of some Leiobunum species carefully search for fissures on fallen trunks (Edgar, 1971). A similar be-

429

430

Reproduction

havior is observed in females of Mitopus morio (Phalangiidae), which use small holes made by beetles and dipteran larvae to hide their eggs inside the hollow stems of three species of herbaceous plants (Tischler, 1967; Table 12.2). The choice of appropriate oviposition sites can be crucial for offspring survival. Low moisture may negatively affect egg development and lead to dehydration. However, eggs laid in very humid places may be more vulnerable to fungal attack. Eggs of Phalangium opilio (Phalangiidae), for instance, develop and hatch better when they are incubated at around 94% relative humidity. Eggs exposed to drier air lose too much moisture to develop completely, whereas fungi destroy those in higher humidity (Edgar, 1971). Females of some leiobunine species, such as L. vittatum and L. flavum, may also cover their egg batches with scent-gland substances before burying the eggs (Table 12.2). This behavior may prevent other females from ovipositing in the same place (Clawson, 1988) and may possibly also deter egg predators and pathogens, since harvestman secretion is known to work as a powerful bactericide and fungicide (see Chapter 10). These suggestions, however, remain to be experimentally tested.

THE TASTY GIFT AND THE ELUSIVE CHELICERAE OF DYSPNOI MALES Little is known about reproduction in Dyspnoi. The few descriptions of copulations, however, are fairly detailed and show similarities with Eupnoi, but also relevant differences (Table 12.1). The Eupnoi pedipalpal grasp is not present among the few described cases. At least among the superfamily Ischyropsalidoidea it is the chelicerae, not the pedipalps, that are sexually dimorphic and greatly enlarged in males. However, chelicerae are not used by the males to grasp females, at least in those species for which we have copulation descriptions (Figure 12.3). Even when the male attempts to hold the female, he uses the less powerful legs I and II (Pabst, 1953; Martens, 1969c). In at least some species of the genera Paranemastoma (Nemastomatidae) and Ischyropsalis (Ischyropsalididae), the base of the chelicerae is either offered or somewhat forced into the female’s mouth, after which the female obtains a secretion from glands found in this position (Martens, 1969c; Meijer, 1972; Figure 12.3A). Interestingly, in I. strandi apparently no “developed cheliceral gland” is found, and the female apparently does not obtain any secretion (Juberthie, 1964; Martens, 1969c). There are also reports of evident precopulatory interactions, including the male tapping on the female’s back (Table 12.1). The existence of stridulatory organs has been suggested in Nemastomatidae and Ischyropsalididae (Silhavy, 1978), but their actual role is unknown. There are reports of males fighting over females in the trogulids Trogulus nepaeformis and T. tricarinatus (Table 12.1). Given that a belly-tobelly position is required for full intromission in these species (Figure 12.3B), females can reject the male approach by lowering the frontal end, much as in Eupnoi. It is risky to make generalizations with such fragmentary information, but males

? ? 6

? 1–5 ? ? 6 5

Lacinius horridus [Eu]

Lophopilio palpinalis [Eu]

Mitopus morio [Eu]

Odiellus aspersus [Jp]

Odiellus gallicus [Eu]

Odiellus spinosus [Eu]

Oligolophus hanseni [Eu]

Oligolophus tridens [Eu]

Paroligolophus agrestis [Eu]

1–3

Phalangium opilio [Eu, NA]

3 1 (?)

Megabunus diadema [Eu]

Platybunus pinetorum [Eu]

Phalangiidae, Platybuninae

1–5

Opilio parietinus [Eu]

Phalangiidae, Phalangiinae

4

?

Number of batches/year

Lacinius ephippiatus [Eu]

Phalangiidae, Oligolophinae

Dicranopalpus ramosus [Eu]

Phalangiidae, Dicranopalpinae

EUPNOI

Taxa

276

27

23–200

20–60

26

27

?

?

EH EH

137.1 ± 17.8 138.0 ± 14.4

276

84.5 ± 13.8

400–600

EH

EH

EH

EH

EH

92.0 ± 9.13

100–200

EH

EH

201

X = 250

– X = 75

EH

229.3 ± 17.7

EH

EH

103.3 ± 19.0

79

EH

EH

EH

Form of parental care

86

94.0 ± 9.6

?

Fecundity (eggs/year)

?

37

?

?

26

?

Number of eggs/batch

Cavities in the soil and rocks

Probably among the leaf litter or on the soil

Under rocks, cavities in the soil and trunks, on the undersurface of leaves

In the mold layer

Probably among the leaf litter or in the soil

Probably among the leaf litter or in the soil

Probably among the leaf litter or in the soil

Probably among the leaf litter or on the soil

Cavities in the soil

Probably among the leaf litter or on the soil

Inside cavities in plant stems and probably among the leaf litter

Probably among the leaf litter or on the soil

Among the moss

Probably among the leaf litter or on the soil

Under rocks, among the moss, and in the soil

Oviposition site

Stipperger, 1928

Phillipson, 1959

(Continued)

Gueutal, 1944b; Edgar, 1971; Bachmann & Schaefer, 1983a

Holm, 1947; Rüffer, 1966

Phillipson, 1959

Phillipson, 1959

Phillipson, 1959

Sankey, 1949a

Juberthie, 1964

Tsurusaki, 2003

Phillipson, 1959; Tischler, 1967

Phillipson, 1959

Parisot, 1962

Phillipson, 1959

Brown, 1984

References

Table 12.2 Frequency of oviposition, fecundity, form of parental care, and oviposition site in species of the suborders Eupnoi, Dyspnoi, and Laniatores

1–5 ? 1–2 1–6 1–3

2 (?) 2 (?)

Leiobunum calcar [NA]

Leiobunum flavum [NA]

Leiobunum politum [NA]

Leiobunum rotundum [Eu, NA]

Leiobunum vittatum [NA]

Nelima genufusca [Jp]

Nelima suzukii [Jp]

Ischyropsalis hellwigii locantei [Eu]

Ischyropsalididae

Dicranolasma scabrum [Eu]

Dicranolasmatidae

5–10

Many

1–6

Leiobunum blackwalli [Eu]

DYSPNOI

1–4

?

?

1–4

Number of batches/year

Leiobunum aldrichi [NA]

Sclerosomatidae, Leiobuninae

Gyas annulatus and G. titanus [Eu]

Sclerosomatidae, Gyinae

Psathyropus tenuipes [Jp]

Sclerosomatidae, Gagrellinae

Rilaena triangularis [Eu]

Taxa

Table 12.2 Continued

– X = 16 (8–35)

1–7

8–10

80–160

10–20

18

46–86

X = 214

– X = 92

15–71

EH

EH + MP

EH + MP

EH

EH

EH + CS

EH

X = 41 149.0 ± 15.1

Under fallen trunks and rocks, among the moss

Inside holes on the ground and among moist fallen leaves

Probably among the leaf litter or on the soil

Probably among the leaf litter or on the soil

Cavities in the soil and rocks

Probably among the leaf litter or in the soil

Cavities in fallen trunks

Cavities in the soil, leaf litter Cavities in the soil, leaf litter

EH EH + CS

X = 185.5

?

Cavities in fallen trunks

Under rocks or inside rock cracks

Probably among the leaf litter or on the soil

Cavities in the soil and under rocks

Oviposition site

?

EH

EH

EH

Up to 150

X = 92.6

?

EH

EH

324 ± 56.8

143

Form of parental care

Fecundity (eggs/year)

– X = 28.7 – X = 23

?

– X = 25 – X = 54

– X = 45.4

?

?

78

Number of eggs/batch

Juberthie, 1964

Gruber, 1996

Tsurusaki, 2003

Tsurusaki, 2003

Edgar, 1971; Clawson, 1988; MacíasOrdóñez, 1997

Phillipson, 1959; Juberthie, 1964

Edgar, 1971

Clawson, 1988

Edgar, 1971

Juberthie, 1964

Bishop, 1950; Edgar, 1971

Martens, 1978b

Tsurusaki, 2003

Immel, 1955; Phillipson, 1959; Parisot, 1962

References

10 3–6 Many

Ischyropsalis nodifera [Eu]

Ischyropsalis pyrenaea [Eu]

Ischyropsalis strandi [Eu]

Many

Nemastoma lugubre [Eu]

Many

Trogulus tricarinatus [Eu]

Holoscotolemon querilhaci [Eu]

Cladonychiidae

Lepchana spinipalpis [As]

Assamiidae

Many

Many (?)

Many

Trogulus nepaeformis [Eu]

LANIATORES

Many

Anelasmocephalus cambridgei [Eu]

Trogulidae

?

Sabacon paradoxus and S. vizcayanus [Eu]

1

?

1–8

1–8

1–6

12–18

6 11.4 ± 3.8

? >2

? – X = 22.5 (6–35)

?

?

18–36

60–75

40–50

?

> 25

?

Up to 105

?

73.3 ± 7.3

2.3 ± 2.4

? 12–30

15.5 ± 9.7 – X=6

Sabacon imamurai [Jp]

1–3

30–60

– X = 10 60

200

– X = 20

1

130–240

– X = 15

Sabacon makinoi [Jp]

Sabaconidae

Paranemastoma quadripunctatum [Eu]

?

2–5

Nemastomella bacillifera [Eu]

Many

Mitostoma chrysomelas [Eu]

Mitostoma pyrenaeum [Eu]

Nemastomatidae

8–15

Ischyropsalis luteipes [Eu]

Inside empty snail shells

EH + MP

EH + EC

On the soil, moss, and rocks

Under rocks and bark

Inside empty snail shells

EH + MP

PC

Inside empty snail shells

Under fallen trunks and rocks, among the moss

EH + MP

EH + MP

Under stones and logs

EH + MP

Under stones and logs

Under stones

EH + MP

Cavities in the soil

EH + MP

Among the leaf litter

Cavities in the soil

Among the leaf litter

On rocks or inside rock cracks in caves

Under fallen trunks and on cave walls

Under fallen trunks and rocks, among the moss

Under fallen trunks and rocks, among the moss, on cave walls

EH + MP

EH

EH + MP

EH

EH

EH + MP

EH + MP

EH + MP

Juberthie, 1964

Martens, 1993b

Pabst, 1953

Pabst, 1953

Pabst, 1953

Juberthie, 1964

Tsurusaki, 2003

Tsurusaki, 2003

Immel, 1954

Juberthie, 1964

(Continued)

Phillipson, 1959; Meijer, 1972

Juberthie, 1964

Meijer, 1972, 1984

Juberthie, 1974

Juberthie, 1964

Juberthie, 1964

Juberthie, 1964

Many Many

Vonones ornatus [NA]

Vonones sayi [NA]

1 (?) 1 (?) 1–2

Acutisoma discolor [SA]

Acutisoma indistinctum [SA]

Acutisoma longipes [SA]

1 (?)

Many (?)

1–3

Acutisoma aff. proximum [SA]

Gonyleptidae, Goniosomatinae

Ampheres leucopheus [SA]

Gonyleptidae, Caelopyginae

Bourguyia albiornata [SA]

Gonyleptidae, Bourguyinae

Pseudobiantes japonicus [As]

Many

1 (?)

Santinezia sp. [SA]

Epedanidae, Sarasinicinae

1 (?)

Santinezia serratotibialis [SA]

Cranaidae

Many

Metalibitia paraguayensis [SA]

?

Eucynortula lata [NA] Many

1

Erginulus clavotibialis [CA]

Gryne orensis [SA]

Many

Number of batches/year

Cynortoides cubanus [CA]

Cosmetidae

Taxa

Table 12.2 Continued

97 ?

131.1 ± 38.6 (27–209)

26–93

95.1 ± 31.9 (38–165)

?

49–339

≥ 16

103

38–70

MC

MC

MC

MC

PC + MP

MC

EH (?)

MC

MC

EC + EH

≥ 85

On cave walls

On cave walls

Between rock gaps

Between rock gaps

On the undersurface of leaves

Inside tank bromeliads

On moss and herbaceous plants

Within a small natural cavity in a ravine

Within small damp pockets among tree roots exposed on ravines

Inside crevices of moist wood

Under fallen trunks and among the leaf litter

Under bark or rocks

EH + EC EH

Inside cavities of tree trunk Under bark or rocks

EH (?)

Under bark or in crevices

On the soil

Oviposition site

EH + EC

MC

EH + EC

Form of parental care

?

?

?

?

90–100

200–240

Fecundity (eggs/year)

97

26–93

95.1 ± 31.9 (38–165)

?

82.1 ± 38.1 (14–169)

1

103

38–70

1

1

1–2

1–2

?

90–100

1–2

Number of eggs/batch

Machado & Oliveira, 1998

Machado, 2002

Machado, 2002

Machado, 2002

Hara et al., 2003

Machado & Oliveira, 2002

Miyosi, 1941

Machado & Warfel, in press

Machado & Warfel, in press

Cokendolpher & Jones, 1991

Goodnight, 1958

Canals, 1936

Canals, 1936

Friebe & Adis, 1983

Goodnight & Goodnight, 1976

Juberthie, 1972

References

1–3 1 (?) 1 (?)

Goniosoma albiscriptum [SA]

Goniosoma catarina [SA]

Goniosoma geniculatum [SA]

1 (?)

Goniosoma sp. 2 [SA]

1 (?) Many

Neosadocus sp. 1 [SA]

Neosadocus sp. 2 [SA]

Many

Promitobates ornatus [SA]

Many 1–2

Discocyrtus dilatatus [SA]

Discocyrtus oliverioi [SA]

Acanthopachylus aculeatus [SA]

1

Many

Mitobates sp. [SA]

Gonyleptidae, Pachylinae

Many

Longiperna zonata [SA]

Gonyleptidae, Mitobatinae

Hernandaria scabricula [SA]

Many

Many

Mischonyx cuspidatus [SA]

Gonyleptidae, Hernandariinae

Many (?)

Gonyleptes saprophilus [SA]

Gonyleptidae, Gonyleptinae

1 (?)

Goniosoma sp. 1 [SA]

1

1 (?)

Goniosoma aff. badium [SA]

Goniosoma spelaeum [SA]

1–2

Acutisoma proximum [SA]

? 8–69

25.5 ± 32.3 (8–69)

~40

?

?

?

?

?

26–64

?

?

83–110

85–173

30–120

47–156

1

~40

1

1

1

1–2

?

26–64

1

?

83–110

85–173

30–120

47–156

~100

84–90

69.6 ± 26.9 (4–145) ~100

72–105

?

72–105

120.8 ± 28.2 (42–182)

MC + EC

EH

MC

EC

EH

EC

EH + EC

PC

MC (?)

EH + EC

PC

MC

MC

MC

MC

MC

MC

MC

MC

Under fallen trunks and rocks

Inside small fissures on fallen trunks and in rock crevices

Under fallen trunks and rocks

On the soil, among the moss

Inside small fissures of tree trunks, among the moss

Inside small fissures of tree trunks, among the moss

Under bark or rocks

Inside mud holes in ravines

On the vegetation

On the soil, under fallen trunks, among the leaf litter

Inside tree holes

On cave walls

Between rock gaps

On cave walls

On cave walls

Between rock gaps

On cave walls

On cave walls

On rocks and on the undersurface of leaves

(Continued)

Elpino-Campos et al., 2001

L. E. Acosta, unpub. data

Capocasale & BrunoTrezza, 1964

Willemart, 2001; G. Machado, unpub. data

G. Machado, unpub. data

G. Machado, unpub. data

Canals, 1936

Machado et al., 2004

Machado & Vital, 2001

Pereira et al., 2004

Machado & Raimundo, 2001; Machado et al., 2004

Machado et al., 2003

Machado, 2002

Gnaspini, 1995

Machado, 2002

Machado et al., 2001

Willemart & Gnaspini, 2004a

Pinto-da-Rocha, 1993

Ramires & Giaretta, 1994; Buzatto et al., 2003

1

Zygopachylus albomarginis [CA]

Manaosbiidae

Camarana flavipalpi [SA]

Gonyleptidae, Tricommatinae

Progonyleptoidellus orguensis [SA]

Iguapeia melanocephala, Iporangaia pustulosa, and Progonyleptoidellus striatus [SA]

Cadeadoius niger [SA]

Gonyleptidae, Progonyleptoidellinae

Many

Many (?)

?

Many (?)

?

Many

Many

Pachyloides thorelli [SA]

Pachylus quinamavidensis [SA]

Pygophalangodus canalsi [SA]

1

Many

Many

Discocyrtus prospicuus [SA]

Pachyloidellus goliath [SA]

Parapachyloides fontanensis [SA]

?

Number of batches/year

Discocyrtus pectinifemur [SA]

Taxa

Table 12.2 Continued

1–5

1

?

?

?

1–2

1–2

78–183

1–2

50–100

1–2

?

Number of eggs/batch

?

?

?

?

?

?

?

78–183

?

50–100

?

?

Fecundity (eggs/year)

PC

Inside mud nests on tree trunks

Inside small fissures of rocks, among the moss

On the undersurface of leaves

PC + MP

EH

On the undersurface of leaves

Under bark or rocks

EH + EC

PC + MP

Under bark or rocks

EH + EC

On the undersurface of leaves

On rocks and on the vegetation

PC + MP

Under bark or rocks

EH + EC

Under rocks, inside rock fissures

Under bark or rocks

Under fallen trunks and rocks

Oviposition site

MC + EC

MC

EH + EC

MC

Form of parental care

Rodríguez & Guerrero, 1976; Mora, 1990

G. Machado, unpub. data

R. Pinto-da-Rocha, unpub. data

Machado et al., 2004

Stefanini-Jim et al., 1987

Canals, 1936

Canals, 1936

Juberthie & MuñozCuevas, 1971

Canals, 1936

L. E. Acosta, unpub. data

Canals, 1936

Matthiesen, 1975

References

5

Scotolemon lucasi [Eu]

1–5

60–100

60–100

1

21–33

?

?

Up to 17

1

1–2

1

≥60

60–100

60–100

?

21–33

?

?

?

5

10–50

5–20

EH

Among leaf mold and in rotting wood

Under fallen trunks and rocks

PC

Under fallen trunks and rocks 1

On moss

On cave walls

Inside cavities in trunks or rocks

Inside cavities in tree trunks

PC1

EH (?)

MC

EH

EH (?)

Attached to the males’ legs

On the ground, moss, and rocks On the ground, moss, and rocks

EH + EC EH + EC

PC

On the ground, moss, and rocks

EH + EC

Forster, 1954

Machado, in press

Machado, in press

Juberthie, 1964

Mitchell, 1971

G. Machado, unpub. data

Friebe & Adis, 1983

Martens, 1993b; Kury & Machado, 2003

Juberthie, 1964

Juberthie, 1964

Juberthie, 1964

The geographic occurrence of each species is indicated in square brackets after the species name (As = Asia; CA = Central America; Eu = Europe; Jp = Japan; NA = North America; NZ = New Zealand; SA = South America). Whenever possible, the number of eggs is expressed as the mean ± SD. In the remaining cases only the range or the available information is presented. CS = chemical secretion released on the eggs; EC = egg covering; EH = egg hiding; MC = maternal care; MP = mucus production; PC = paternal care. 1. Although Forster (1954) states that species of these two genera present maternal care, the behavioral patterns described by him are identical to those of species presenting paternal care. Indeed, a photo published in a book on New Zealand arachnids (Forster & Forster, 2003) clearly shows a male of Karamea taking care of eggs in several stages of embryonic development (Machado, in press).

Hendea myersi [NZ]

Many

?

Soerensenella spp. [NZ]

Triaenonychidae, Triaenonychinae

?

Many

Karamea spp. [NZ]

Triaenonychidae, Soerensenellinae

Peltonychia clavigera [Eu]

Travuniidae

Hoplobunus boneti [CA]

1 (?)

?

Protimesius longipalpis [SA]

Stygnopsidae

?

Auranus parvus [SA]

Stygnidae

Leytpodoctis oviger and an undescribed species [As]

Many (?)

10–25

Scotolemon lespesi [Eu]

Podoctidae

5–20

Scotolemon doriae [Eu]

Phalangodidae

438

Reproduction

A

Figure 12.3. (A) Intromission in the ischyropsalidid Ischyropsalis hellwigi (left = male; right = female); both partners embrace with the tarsi of the first two pairs of legs (photo: J. Martens). Scale bar = 5 mm. (B) Belly-to-belly intromission in the trogulid Trogulus nepaeformis. The male moves rhythmically, and the mating pair rubs and taps each other with chelicerae and pedipalps (modified from Pabst, 1953; drawing by M. R. Hara).

乆

么

B

in this suborder seem to play a slightly less coercive role and the females a more active, or at least less cryptic, one. Unlike Cyphophthalmi and Eupnoi, the Dyspnoi ovipositor is short, and the lack of sensory organs at the tip (present in Cyphophthalmi and Eupnoi) suggests less sensitivity; the muscular array is different, and it lacks segmentation (Martens et al., 1981). However, the Dyspnoi penis is not too different from that of Eupnoi (see Chapters 2 and 4). Males in this suborder seem to rely less on a powerful grasping to negotiate with the female and more on precopulatory courtship, including nuptial gifts (Table 12.1).

Reproduction

Copulatory courtship such as that reported in Eupnoi has been described in most studied species of Dyspnoi (Table 12.1), suggesting that females may also exert cryptic choice. The amount and quality of the secretion offered may be the subject of female evaluation and influence paternity. Whatever the composition, the secretion may represent costs that must be considered along with the ejaculate as the total male investment in mating. The fact that the enlarged sexually dimorphic male chelicerae are apparently not used during interaction with females is intriguing. Large male chelicerae may have been selected as fighting weapons. However, although fights are reported in at least some species of the genus Trogulus (Pabst, 1953), the chelicerae in Trogulidae are not sexually dimorphic. Given their short (and apparently less sensitive) ovipositor, Dyspnoi females cannot insert the eggs into protected places. Thus they are laid on substrates such as fallen leaves, wood, and rocks (Juberthie, 1964; Gruber, 1993; Tsurusaki, 2003). As occurs with Eupnoi, their eggs are extremely sensitive to temperature and air moisture (Pabst, 1953; Immel, 1954). However, Dyspnoi eggs are generally surrounded by a highly hygroscopic mucus coat secreted by the female’s ovipositor (Table 12.2), which maintains moisture around the eggs (Juberthie, 1964; Tsurusaki, 2003). This mucus coat probably protects the batches against dehydration and also provides freezing resistance, as occurs in some insects (Danks, 2002). Moreover, at least among gastropods, the mucus coat may also confer mechanical and antimicrobial protection (Beninger et al., 2001). Some Trogulidae (genera Trogulus and Anelasmocephalus) are specialized predators of gastropods that penetrate shells through the aperture and consume the soft tissues (see Chapter 8). Eggs are then laid in the empty shells and sealed by a protective weblike membrane secreted by the ovipositor (Table 12.2). This membrane seems to be important for egg protection since if it is imperfectly placed or artificially destroyed, the shell is invaded by egg predators, such as mites, springtails, and earthworms (Pabst, 1953). Like most species of Eupnoi, Dyspnoi females lay eggs in several different batches, usually with a time lag of some days between successive ovipositions (Table 12.2). As the risk of predation on unprotected eggs is probably high (Edgar, 1971; Tsurusaki, 2003), it may be advantageous to lay eggs in several batches or even scatter single or a few eggs over a very wide area, so that detection by natural enemies is reduced (Edmunds, 1974). This is probably more important in the case of Dyspnoi eggs because they are laid on exposed substrates.

THE PARENTAL AND WELL-ARMED LANIATORES Mating strategies and parental care As in other suborders, sperm in Laniatores lack a flagellum and are therefore immobile (Morrow, 2004). Their ovipositors are not strikingly different from those of

439

440

Reproduction

Dyspnoi; they are short and unsegmented, and the density of sensitive organs is low. Their musculature, however, is mainly formed by circular and not by longitudinal muscles, the vaginal symmetry is radial and not bilateral, and the cross section of the lumen is X shaped (Martens et al., 1981). The penis, on the other hand, is unique among Opiliones in showing a reduction of musculature (Martens, 1986) and a striking diversity and complexity of “ornaments” (see Chapters 2 and 4). Male strategies for direct insemination and enhanced female stimulation may have coevolved with female strategies to restrict accessibility to the seminal receptacles by means of ovipositor reduction, loss of sensibility, and even promotion of sperm competition, observed now in the form of male structures that probably remove sperm from previous males from the female reproductive tract (Thomas & Zeh, 1984; Eberhard, 1996; Birkhead & Møller, 1998). The implications of this alternative would be profound: cryptic female choice and male sperm competition would have been the forces behind changes in egg-laying structures and, therefore, oviposition and brooding strategies. Constrained by their short ovipositor, females are unable to hide eggs in wellprotected places. All species of Laniatores lay eggs on exposed substrates such as rocks, tree trunks, fallen logs, and vegetation. In the great majority eggs are laid singly in shallow natural cavities or are covered by debris by the female (Table 12.2). During the egg-covering process females scrape the substrate around the egg, picking up debris and attaching soil particles to it (detailed description in Willemart, 2001; Figures 12.4A,B). This behavior may last from 1 to 50 minutes per egg, and its function may be camouflage or dehydration prevention (Willemart, 2001; ElpinoCampos et al., 2001). In some species, however, females lay eggs in a single large batch and brood eggs throughout the embryonic development, remaining with the newly hatched nymphs for up to 14 days. Maternal care has been reported for many families of Laniatores, especially within the Neotropical superfamily Gonyleptoidea (Table 12.2; Figures 12.4C–F). Parental care is an important aspect in the evolution of mating strategies because the commitment of each sex to egg brooding may strongly influence their respective reproductive costs and benefits (Trivers, 1972; Andersson, 1994). An implication of maternal care is that females benefit from developing batches of simultaneously mature eggs, in which case development and eclosion will be synchronous. This allows the female to optimize periods of egg caring and recovery. The implication for males is that each receptive female potentially translates into more immediate reproductive success than if not all eggs developed at the same time. Furthermore, if egg laying occurs immediately after copulation, the risks of sperm competition for fertilization are reduced, although they remain if the female copulated previously. In such species we can expect strong male competition for females or for spatially aggregated zones of female nesting. Females are expected to be very selective, or, as suggested by Wiley and Poston (1996), simply by aggregating, females could intensify male competition and indirectly select the best males in a haremlike mating system. In either case we can also expect strong sexual dimorphism and interspecific male variation as a consequence of selection for male structures involved

A

C

E

B

D

F

f Figure 12.4. (A) Female of the gonyleptid Longiperna zonata laying an egg on a tree trunk in southeastern Brazil. (B) The same female picking up debris and attaching particles to the egg (photos: B. A. Buzatto). The inset shows a scheme of the egg covered with debris. (C) Female of Discocyrtus oliverioi (Gonyleptidae) taking care of eggs under a stone in Uberlândia, Brazil (photo: A. A. Giaretta). (D) Female of Erginulus clavotibialis (Cosmetidae) taking care of her eggs under a rotting log in Chiapas, Mexico (photo: R. Macías-Ordóñez). (E) Two females of Pachyloidellus goliath (Gonyleptidae) taking care of their eggs under a rock in xeric Pampa de Achala, Argentina (photo: C. Mattoni). (F) Female of Santinezia serratotibialis (Cranaidae) taking care of eggs and newly hatched nymphs in a small, damp pocket among tree roots in Trinidad (photo: J. G. Warfel). Scale bars = 10 mm.

442

Reproduction

in male-female interactions or in male fights. Male genitalia may be complex as a consequence of cryptic female choice, and therefore species-specific ornaments with the capacity to stimulate the female are also expected. Adults in the subfamily Goniosomatinae (Gonyleptidae) are among the largest in the order and present marked sexual dimorphism in the armature of leg IV (Gnaspini, 1995) and length of leg II (Machado et al., 2003). Most likely, all species present maternal care (Machado, 2002), and some studies include details on their mating strategies (Gnaspini, 1995; Machado & Oliveira, 1998; Willemart & Gnaspini, 2004a). A detailed study in the Brazilian Atlantic forest has revealed that at least some males of Acutisoma longipes defend territories on cave walls that are visited by ovigerous females seeking copulation and a nesting site. There is no information on precopulatory behavior, but during copulation the male intensively taps the dorsum and hind legs of his partner and may perform multiple intromissions. Oviposition occurs immediately after copulation, and during this process the male remains close to the female, waving his legs II over her and eventually tapping her legs and dorsum. Mate guarding may last more than 24 hours, during which the male often tries to copulate (and occasionally succeeds). There are harems composed of up to five guarded females, which the owner inspects frequently (Machado & Oliveira, 1998), and territorial fights have been recently recorded among males (G. Machado, pers. obs.). In another species of Goniosomatinae, Acutisoma proximum, males also defend harems by means of long and vigorous fights. Not surprisingly, these fights involve strikes with the sexually dimorphic long leg II and the armed leg IV (Buzatto et al., 2005). Since many other gonyleptid harvestmen show similar copulatory and postcopulatory behaviors (Table 12.1), the mating strategy just described may be widespread within the family (Figure 12.5). Exclusive postovipositional paternal care is the rarest form of parental care among arthropods, and all described cases in Arachnida are restricted to Opiliones, specifically to Laniatores. When males are in charge of egg brooding, they become a reproductive resource for females, and some degree of sex-role reversal may be expected (Owens & Thompson, 1994; Parker & Simmons, 1996). In such cases females should court males and fight among themselves for access to male services; males, in turn, are expected to be choosy. In short, male-male competition may be less intense, and no sexual dimorphism is expected. All of these features can be found in the case of the manaosbiid Zygopachylus albomarginis, a paternal species from Barro Colorado Island (Panama) studied in detail (Rodríguez & Guerrero, 1976; Mora, 1990, 1991). Males of this species build and defend mud nests that females seek for egg laying and fight for among themselves (Figure 12.6A). Females also court males, which sometimes reject (expel) females without copulating. After oviposition females leave the nests, and males guard eggs by removing fungi, chasing away potential predators, and preventing cannibalism. Sexual dimorphism is very subtle, and males are hardly distinguished from females; curiously, Z. albomarginis is the only manaosbiid in which males do not have the swollen first tarsal segment in leg I, a sexually dimorphic trait in the family (A. Pérez González, pers. comm.). Other interesting cases come from two sister subfamilies of Gonyleptidae in

Reproduction

A

C

B

D

Figure 12.5. (A) Two marked males of the gonyleptid Acutisoma proximum fighting over a reproductive territory on vegetation in southeastern Brazil (photo: B. A. Buzatto). (B) Intromission in A. proximum. The arrow indicates the interaction between female pedipalps and the male penis (photo: B. A. Buzatto). (C) Mate guarding in the same species: the male (right) waves his legs over the female and taps her dorsum while she oviposits (photo: B. A. Buzatto). (D) Harem of Goniosoma discolor showing three guarding females (arrows). The male is behind the leaves, not shown (photo: G. Machado). Scale bars = 10 mm.

which all species seem to show paternal care, Caelopyginae and Progonyleptoidellinae (Machado et al., 2004). Although most gonyleptids show strong sexual dimorphism, males being larger and more armed than females, in these two subfamilies the dimorphism is also very subtle since females of many species have legs with spines and apophyses as long as those of males (e.g., Pinto-da-Rocha, 2002; Figure 12.6B); in other cases neither sex has any leg armature at all (e.g., Kury & Pinto-daRocha, 1997; Figure 12.6C). However, strong sexual dimorphism may be found among paternal species in the subfamily Gonyleptinae. In this subfamily males of some species defend very specific sites (holes in ravines and trunks) as nesting sites, and the armature seems to be involved in defense of this scarce resource against other males (Machado et al., 2004; Figure 12.6D).

443

A

B

C

D

E

F

Figure 12.6. (A) Male of Zygopachylus albomarginis (Manaosbiidae) taking care of eggs (arrows) inside a mud nest in Barro Colorado, Panama (photo: C. Rodríguez). (B) Guarding male of the gonyleptid Ampheres leucopheus pushing and guiding the female with his pedipalps while she oviposits immediately after copulation (photo: B. A. Buzatto). (C) Male of Iporangaia pustulosa (Gonyleptidae) caring for eggs on the underside of a leaf in Intervales State Park, southeastern Brazil. Note that the male does not present the typical leg armature of the gonyleptids (photo: B. A. Buzatto). (D) Guarding male of Gonyleptes saprophilus (Gonyleptidae) attaking a forceps placed near the entrance of his nest in a trunk hole in Atibaia, Brazil (photo: G. Machado). (E) Male of Acutisoma proximum (Gonyleptidae) taking care of the offspring after one female of his harem was experimentally removed (photo: B. A. Buzatto). (F) Male of Leytpodoctis oviger (Podoctidae) from The Philippines carrying eggs attached to the legs (photo: J. Martens). Scale bars = 10 mm.

Reproduction

In paternal species we can also expect male strategies to ensure paternity, ranging from sophisticated structures for sperm removal in genitalia to repeated copulations and postcopulatory female guarding and coercion to lay eggs soon after copulation. There is no comparative study on genital morphology of groups presenting paternal care and their closely related relatives that present maternal care or no care. However, field observations on Ampheres leucopheus, a gonyleptid with paternal care (Hara et al., 2003), suggest that males indeed push and guide females to lay eggs just after copulation (G. Machado, unpub. data; Figure 12.6B). In species with no parental care, females may develop eggs asynchronously and lay one or a few at a time (Table 12.2). As will be suggested later, this may be the best strategy to maximize survival in the absence of parental care. In such cases predictions are similar to those in previous suborders. The existence of sexual dimorphism and the kind of male-female interaction will be the result of the amount and distribution of relevant resources and mates. There is no published study or description of any mating behavior in nonparental species of Laniatores, which probably encompass the great majority of species in the suborder. Unpublished observations on the gonyleptid Promitobates ornatus indicate that there are long male-male fights, but it is not clear if they are defending a resource or fighting for access to females. Copulation is not followed by mate guarding, oviposition does not occur immediately after insemination (Table 12.1), and, as would be expected, females lay one egg at a time (Table 12.2).

Costs and benefits of maternal care Costs of reproduction for parental females can be grouped as follows: (a) ecological costs associated with an increased exposure to predation (searching for oviposition sites, laying, or guarding) and (b) physiological costs from allocation of energy to egg production and other parental activities rather than to individual growth or maintenance (Bell, 1976). There is no study on the ecological costs of harvestman subsocial behavior in the field. It is known, however, that females of the gonyleptid Bourguyia albiornata oviposit almost exclusively inside the tank bromeliad Aechmea nudicaulis in Cardoso Island, Brazil, despite the fact that this species accounts for only 10% of all epiphytic bromeliads in the site (Figure 12.7A). This bromeliad accumulates water and provides protection from stressful climatic factors and moisture fluctuations for the offspring (Figure 12.7B). It is reasonable to suppose that females need to invest time and energy to search for an appropriate oviposition site and thus are exposed to predation (Machado & Oliveira, 2002). From a physiological standpoint, females first invest a great amount of energy to produce large and nutritionally rich eggs. In some subsocial species the total volume of a single egg batch may correspond to 50% of the total body volume of the female. Indirect evidence on the costs of egg production comes from the cavernicolous harvestman Goniosoma spelaeum (Gonyleptidae), whose ovigerous females leave the cave to forage outside on a daily basis, while adult males and nonovigerous females may remain inside the cave for several days (Gnaspini, 1996; see also Chapter 8). After oviposition

445

446

Reproduction

maternal care prevents foraging activities by females and reduces the intake of energy to produce additional eggs, a critical issue for iteroparous species (Tallamy & Brown, 1999). In fact, females of B. albiornata that produce more than one egg batch during the year present a significant decrease in fecundity during subsequent ovipositions, suggesting a trade-off between egg production and maternal care (Machado & Oliveira, 2002). All species of Laniatores that present maternal care aggregate eggs in time and space (Table 12.2), a behavioral pattern associated with evolution of subsocial behavior in other arthropod groups, including hemipterans (Tallamy & Schaefer,

A

C

B

D

Figure 12.7. (A) Comparison between the relative abundance of two species of bromeliad at Cardoso Island and the percentage of individuals used as oviposition sites by B. albiornata. (B) Comparison between the relative humidity inside and outside the tube of leaves of Aechmea nudicaulis (mean and standard error). The variation inside the bromeliad is smaller than outside, and humidity is lower during the warmer period of the day. (C) Effect of maternal care on egg survival in Acutisoma longipes after two weeks (mean and SE). Egg survivorship is significantly higher when batches are guarded by the female (data from Machado & Oliveira, 1998). (D) Intensity of fungal attack on caged egg batches of A. longipes after two weeks. Eggs are equally attacked by fungi, irrespective of the presence of the mother.

Reproduction

1997) and centipedes (Lewis, 1981; Machado & Raimundo, 2001). Moreover, females of the great majority of subsocial Laniatores seem limited to a single oviposition per breeding season or even during their lives (Table 12.2). There are a few exceptions, such as Acutisoma longipes, Goniosoma albiscriptum, and B. albiornata, but in these cases the percentages of the females that produced more than one batch in one year were 9%, 33%, and 16%, respectively (references in Table 12.2). These species may be opportunistically iteroparous, and constraints such as food and/or availability of nest sites make them functionally semelparous (see Tallamy & Brown, 1999). If environmental constraints reduce the success of subsequent ovipositions during a breeding season, the fecundity-related costs of maternal care are minimized, regardless of whether the female lives to produce another batch in the following breeding season (e.g., Kight, 1997; Eggert & Müller, 1997). Females constrained to produce only one batch in a given breeding season could increase their lifetime reproductive success by guarding the eggs that they have already laid, especially in environments with high egg and juvenile predation. There is no evidence that harvestman females can benefit their offspring by enhancing the feeding efficiency of the nymphs, or that parents are able to actively protect offspring against environmental stress, such as dehydration (Machado & Oliveira, 1998). However, field experiments demonstrated that maternal care may be crucial for preventing egg predation (Machado & Oliveira, 1998, 2002). Entire egg batches of B. albiornata were consumed by ants in a few hours when left unprotected. The effectiveness of maternal care was also shown for the cavernicolous A. longipes (Figure 12.7C). The most important predators were cave crickets and conspecific individuals capable of cannibalizing entire batches in a 24-hour period (Machado & Oliveira, 1998). Eggs of A. longipes are also attacked by fungi, especially during the wet and warm season, when nearly 50% may be infected (Machado & Oliveira, 1998). Although fungus-infected eggs did not develop, guarding females did not eat or remove such eggs. Indeed, field experiments in this species have shown that maternal care per se is unable to protect eggs against fungal attack (Figure 12.7D). Only one species, the paternal Zygopachylus albomarginis, is known to be able to control egg fungal attack (Mora, 1990), something probably very rare among Opiliones (Machado & Raimundo, 2001).

Maternal care in harvestmen: An apomorphic trait One important question in evolution of parental care is why this behavior has evolved in some species and not in others. The hypothesis first suggested by Wilson (1971) postulates that intense predation on eggs by conspecifics and ants and the high risk of fungal attack in tropical rain forests may have been the major forces favoring the evolution of arthropod subsocial behavior. Although this hypothesis may explain why maternal care is frequent among the tropical Gonyleptoidea, it does not provide an answer to the question just raised. Tallamy and Wood (1986) proposed that the answer involves many interacting morphological and physiological factors, as well as behavioral preadaptations and phylogenetic constraints. Although our

447

448

Reproduction

knowledge on harvestman behavior is incomplete and fragmented, several evolutionary patterns seem to emerge (Figure 12.8). The evolution of a piercing ovipositor and precocial eggs in insects allowed many lineages to hide eggs from predators and parasites by inserting them into protective plant tissues or soil (Zeh et al., 1989; Tallamy & Brown, 1999). In these groups there is evidence that maternal care is no more effective in protecting offspring than hiding eggs or spreading them through time and space (Tallamy & Schaefer, 1997). Females of the suborders Cyphophthalmi and Eupnoi have a long ovipositor that allows them to hide eggs from predators and parasites by inserting them into protective substrates (Edgar, 1971). This structure, analogous to the piercing ovipositor of insects (Tallamy & Brown, 1999; Tallamy & Schaefer, 1997), enables them to confer protection on the eggs and avoid the costs of maternal care (Figure 12.8). On the other hand, females of Dyspnoi and Laniatores have a short ovipositor, and thus

Figure 12.8. Hypothetical scenario for the evolution of the different forms of parental care in harvestmen. The two main ecological pressures favoring evolution and maintenance of subsociality are probably the constraint to produce only one egg batch per breeding season and severe predation on eggs and juveniles. The numbers after each feature in the boxes were mapped in the harvestmen phylogeny at the bottom of the figure (according to Giribet et al., 2002).

Reproduction

most species are unable to insert their eggs into sheltered places (Figure 12.8). Although trogulid eggs are well protected inside empty shells, the great majority of the species in these suborders deposit eggs on exposed surfaces or shallow cavities where the presence of a parental individual may enhance offspring survival. At least two distinctive life-history traits may offer an explanation of the causes of the evolution of maternal care within Laniatores compared with other suborders (Machado & Raimundo, 2001). Postovipositional parental care requires considerable adult longevity; parents must not only survive to oviposit but also live long enough to care for one or more clutches (Tallamy & Wood, 1986). The parents also need to present defensive postures and/or aggressive behaviors that effectively repel predators and increase offspring survival (Tallamy & Wood, 1986). Most species of Eupnoi develop quickly and die soon after oviposition (see Chapter 13). In the few species that live more than one year, mating takes place during a restricted period, usually in the fall. The constraint imposed by their short life span makes prolonged association between parents and offspring unlikely (Figure 12.8). Moreover, representatives of Eupnoi (especially Phalangioidea) are small and fragile, and their pedipalps, an important appendage used to repel egg predators in Laniatores (see Machado & Oliveira, 1998, 2002), are usually short and lack spines (Chapter 2). Common defensive adaptations among Eupnoi are leg appendotomy, the ability to flee rapidly, crypsis, and bobbing (see Chapter 10), all of which are unlikely to provide effective defense against potential egg predators (Figure 12.8). Among Laniatores most species live more than two years and reproduce throughout the year (see Chapters 7 and 13), making long-term associations between parents and offspring possible (Figure 12.8). Moreover, in large Laniatores, mainly Gonyleptidae, mechanical defense such as attacking with the pedipalps and pinching the aggressor between the sharp projections of the femur and trochanter IV are common (see Chapter 10). These defenses enable a subsocial harvestman to protect offspring against egg predators. Finally, the scent-gland secretion of Laniatores is mainly composed of quinones and phenols, which are known to be effective defensive compounds against invertebrate and vertebrate predators (Machado et al., 2005). According to Eisner et al. (1978), it seems likely that the quinone-producing Laniatores are better protected than Eupnoi species, whose secretion is composed of alcohols, ketones, or aldehydes (Figure 12.8). Under a phylogenetic perspective, maternal care is absent in Cyphophthalmi, Eupnoi, and Dyspnoi (Figure 12.8). Postovipositional parental care appears only in Laniatores, and within this suborder it seems to have evolved independently several times from a plesiomorphic state of egg covering or egg hiding (Machado & Raimundo, 2001). Thus there is no doubt that maternal care is an apomorphic trait in the order Opiliones. This result contrasts with the hypothesis of Tallamy and Schaefer (1997), who postulate that maternal care in arthropods is plesiomorphic, and that the derived state consists of more efficient and less costly strategies, such as egg hiding (see also Tallamy & Brown, 1999). Although this hypothesis seems to fit well in a few subsocial arthropod groups such as hemipterans (Tallamy & Schaefer,

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Reproduction

1997), there seem to be a number of exceptions, including centipedes (Edgecombe & Giribet, 2004) and solifuges (Punzo, 1998), as well as harvestmen (Machado & Raimundo, 2001).

Evolution of male care Diverse factors have been proposed to explain which sex is more likely to provide parental care (Queller, 1997). Anisogamy generates the conditions for sexual selection since numerically abundant male gametes compete for access to rare female gametes (Bulmer & Parker, 2002). This competition decreases confidence of paternity, especially among species with internal fertilization (Williams, 1975), as in all arachnid orders (Thomas & Zeh, 1984; Elgar, 1998). Moreover, direct male-male competition for access to females and/or female mate choice creates a male reproductive elite in the population, more likely to acquire mates (Bateman, 1948). Both low confidence of paternity and great variance in mating success (number of mates) may act against the evolution of paternal care relative to female care because they reduce the benefits and increase the costs of caring behavior, respectively (Kokko & Jennions, 2003). If males take care of offspring, they may lose additional mating opportunities (Magraph & Komdeur, 2003). The cost of paternal care is reduced when females oviposit on the male’s territory (Ridley, 1978; Zeh & Smith, 1985). If one sex defends a territory before fertilization, then that sex may be selected to care for the offspring as a consequence of territoriality (Williams, 1975). The model is not universal, but may have been important in the evolution of paternal care in several groups, such as fish (Ridley, 1978), anurans (Lehtinen & Nussbaum, 2003), and harvestmen (Machado & Raimundo, 2001). Mora (1990) was the first to propose a hypothetical scenario for the evolution of paternal care in harvestmen, using Zygopachylus albomarginis as a model organism. According to her, females would be attracted to suitable oviposition sites, which males would begin to defend against other males for acquiring mates. Males that defend a territory would increase their fitness because they also indirectly defend eggs against predation by conspecifics. A similar behavior was later described for the assamiid Lepchana spinipalpis (Martens, 1993b) and the gonyleptids Ampheres leucopheus (Hara et al., 2003), Gonyleptes saprophilus, Iporangaia pustulosa, Iguapeia melanocephala, Neosadocus sp., and Progonyleptoidellus striatus (Machado et al., 2004), whose males guard a multiple batch containing eggs in all developmental stages and even newly hatched nymphs. In all these cases more than one female contributes to the batch. Males of Acutisoma longipes may defend territories where females lay eggs and guard the egg batches (Machado & Oliveira, 1998). When females are experimentally removed from their batches, the male takes egg guarding for up to two weeks. Similar observations were later reported for Goniosoma albiscriptum (Willemart & Gnaspini, 2004a) and Acutisoma proximum (Buzatto et al., 2005; see also Figure 12.6E). Therefore, Goniosomatinae males may care for the brood when the guarding

Reproduction

females desert or die. Although egg guarding by males lasts only a few weeks, temporary paternal care may be crucial (especially just before hatching), since egg predators can consume entire batches in one night (Machado & Oliveira, 1998). This behavior is remarkably different from that of species with exclusive paternal care, but it constitutes additional support for the idea that postovipositional male care in harvestmen, even for short periods, can occur when males defend a territory that is also an oviposition site. Therefore, the association between the male and the offspring through the defense of oviposition sites may constitute the basis for the evolution of paternal assistance in most harvestmen species (Machado & Raimundo, 2001). Tallamy (2000, 2001) analyzed all described cases of exclusive paternal care in arthropods and proposed that male care could release females from the fecundity costs of maternal care and provide an honest signal of paternal intent and quality. Males willing to guard the offspring would become preferred mates and would achieve more copulations. Several life-history and behavioral traits are predicted to be found if the evolution of paternal care was driven by sexual selection: (a) females are iteroparous; (b) there are many mating opportunities for the males; (c) egg care interferes with female foraging; (d) eggs increase male attractiveness; (e) males may guard eggs laid by several females; (f) males are willing to guard unrelated eggs; and (g) the local female population is high (Tallamy, 2000, 2001). Data from 13 paternal harvestman species provide support for most, but not all, predictions. A general feature is that in all species females are indeed iteroparous. In at least 11 of these species males have many mating opportunities and guard eggs laid by more than one female. Information on the density of females is scarce, and the results obtained for some species seem not to support the prediction that females should be locally abundant (Machado et al., 2004). Finally, the evidence that males are willing to guard unrelated eggs is ambiguous. In at least two species, Z. albomarginis and I. pustulosa, vagrant males readily eat unprotected eggs (Mora, 1990; Machado et al., 2004). In Z. albomarginis vagrant males also fight for the ownership of the mud nest itself, probably the most important signal of male quality (Mora, 1990). In I. pustulosa females oviposit on the undersurface of leaves, and eggs are apparently the only attractiveness to females. Therefore, males should be willing to guard unrelated eggs, but contrary to the prediction, they eat some unprotected eggs and abandon the batches (Machado et al., 2004). Egg adoption is a crucial point of Tallamy’s hypothesis, and future studies should investigate this aspect more thoroughly. The decision to cannibalize an unprotected batch may depend on the number of eggs present (which may reflect the attractiveness of the site) or on ecological factors such as food abundance, operational sex ratio of the population, and availability of oviposition sites. There are several differences in the behavioral patterns of guarding females and guarding males in harvestmen that are probably a consequence of the different selective pressures leading to the evolution of maternal care (via natural selection) or paternal care (probably via sexual selection). Perhaps the most striking difference is that females guard batches containing eggs in only one stage of embryonic development, while males guard batches containing eggs in several stages of embryonic de-

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Reproduction

velopment, likely the result of different oviposition events. Additionally, total time spent by females guarding eggs and newly hatched nymphs varies among and within species, but usually does not exceed 60 days. Among paternal species, however, females continually add eggs to the batches, and parental activities may, therefore, last up to eight months (Machado et al., 2004). Moreover, females do not leave the egg batch to forage or undertake any other activity (e.g., Gnaspini, 1995; Machado & Oliveira, 1998, 2002). In contrast, guarding males frequently leave their egg batches and may be found as far as five meters from them (Hara et al., 2003; Machado et al., 2004). At least three nonmutually exclusive hypotheses may account for the males’ forays: (a) males may be unable to accumulate enough energy reserves for the long period of egg guarding, so they need to leave the batch to forage, (b) males may be patrolling the batches at a distance in order to repel predators and other competing males, and (c) during their walks males may increase their chances of finding additional mates (Machado et al., 2004). Two podoctids, Leytpodoctis oviger (Figure 12.6F) and an undescribed species from the Solomon Islands, present a distinctive strategy in which females attach 1 to 15 eggs to the third and fourth femora of the male (Martens, 1993b; Kury & Machado, 2003). Oviposition on such a limited space presupposes a precise movement by the female’s ovipositor, but there is no observation of egg laying for this family. The amount of biological information on these species is so limited that it is difficult to understand the selective forces leading to the evolution of this behavior. The main advantage to the male derives from his mobility, which may result in (a) a defensive ability against egg predators by fleeing, carrying the offspring, (b) a capacity to move to areas with suitable moisture and temperature conditions, which are crucial for egg development (see Martens, 1993b), and (c) autonomy to forage while brooding. The main disadvantage is probably a spatial limitation in the number of eggs they can carry. Moreover, the eggs are laid on the third and fourth leg femora, where it is impossible for the male to groom the batch for removing pathogens (Martens, 1993b). There are many gaps in our knowledge on paternal care in harvestmen. At this moment it is suggestive to infer that paternal care has evolved independently many times within the order since most paternal species are not closely related (see Chapters 3 and 4) and the forms of egg guarding are very different (see also Machado, in press). Behavioral data allied with phylogenetic information are also crucial to understand if male guarding has evolved from no care or from female care. Among all other arthropod groups with paternal care, this can be answered only in water bugs of the family Belostomatidae, for which there is a phylogenetic hypothesis (Mahner, 1993). In all nonbelostomatid representatives of the clade Nepomorpha, eggs develop in the absence of parental care, and thus it is possible to infer that paternal care among water bugs evolved from a plesiomorphic state of no care (Smith, 1997). This behavioral transition has been described for several vertebrate groups (reviewed in Reynolds et al., 2002), and harvestmen may provide additional and phylogenetically independent tests of this pattern.

Reproduction

CONCLUDING REMARKS Most of what we know about mating strategies in Opiliones may be framed as intersexual selection, although the role of intrasexual selection may still require further attention. Any sort of male-female interaction before, during, and after insemination that may affect the chances of specific males to fertilize the female’s gametes is a potential case of sexual selection by female choice, be it cryptic or not. Everywhere we look among harvestmen, we find different ways in which males and females deal with each other. Intersexual selection has been the focus of much research in evolutionary ecology during the last few decades. Current debate on several topics such as the relative importance of sexual conflict and cryptic female choice in the evolution of mating strategies (see Holland & Rice, 1998; Birkhead 2000; Eberhard, 2000; Kempenaers et al., 2000; Pitnick & Brown, 2000) are in desperate need of empirical research in phylogenetically independent taxa with intromittent male genitalia such as the Opiliones. In Tables 12.1 and 12.2 we have attempted to outline relevant aspects when describing mating strategies and parental investment. In any field study we should attempt to fill out all those columns with as much detail as possible. Awareness of spatial and temporal differences between and within populations is also important, as well as good assessment of variability of any morphological, physiological, or behavioral trait within a population. This implies appropriate sample sizes and, therefore, careful sampling design in order to optimize research resources. Behavioral observations should include frequencies and durations of several replicates of relevant behaviors, not only descriptions of the behavioral patterns based on averages or most frequent occurrences. The use of video equipment is strongly encouraged. Distinct individual tags with careful follow-up of individuals for all or most of their reproductive life will provide the opportunity for powerful data analyses. Numbers of offspring that survive to a reproductive age sired by individual males and females are ideal estimates of reproductive success. These estimates are very hard to achieve and usually require some method to assess paternity. Less accurate but more accessible and still useful estimates for females are numbers of eggs or hatchlings, and number of mates for males. Any effort to identify, quantify, map, and even manipulate distribution of relevant resources (e.g., egg-laying substrate, food, nesting sites) will also produce a more complete picture of ecological and evolutionary processes acting on the population. The biological information acquired, placed in the proper theoretical framework and phylogenetic context, will give us an always-sharper but still-challenging view of the evolution of reproductive strategies in Opiliones.

ACKNOWLEDGMENTS We are grateful to A. Dávila and M. R. Hara for helping with German and Japanese translations; to G. Giribet and H. Viadiu for help obtaining hard-to-find literature; to

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M. Draud, W. G. Eberhard, A. Edgar, M. Itzkowitz, and J. Shultz for stimulating discussions; to L. E. Acosta, B. A. Buzatto, P. Gnaspini, A. B. Kury, R. Pinto-da-Rocha, G. S. Requena, and R. H. Willemart for unpublished data; to P. C. Carrera, W. G. Eberhard, M. A. Elgar, M. O. Gonzaga, J. Gruber, A. J. Santos, D. W. Tallamy, and N. Tsurusaki for helpful comments on early drafts; to I. M. Karaman for providing a manuscript in press; to M. R. Hara and A. Midori for the hand drawings; and to B. A. Buzatto, A. A. Giaretta, I. Karaman, J. Martens, C. Mattoni, C. Rodríguez, and J. Warfel for generously facilitating photographs. G. Machado is supported by a research grant from FAPESP (02/00381-0), and R. Macías-Ordóñez has been supported by DGAPA-UNAM, Lehigh University, and the Instituto de Ecología, A.C.

CHAPTER

13

Development Pedro Gnaspini

T

he life cycle of a harvestman may be divided into two major phases, embryonic and postembryonic, which are separated by the hatching of the egg (eclosion). Postembryonic development is characterized by three phases: larval, nymphal, and adult (Juberthie, 1964). The larva hatches from the egg and molts to the first nymphal instar. The adult stage, defined by the capacity to reproduce, is reached after a variable number of molts. Van der Hammen (1978) discussed the terms used in postembryonic development of arachnids and suggested that the term nymph should be used only when the number of juvenile instars is constant within an order. Otherwise, when this number varies, as in the case of Opiliones, he suggested the use of the term nymphoid. Canard and Stockman (1993) compared life cycle patterns observed among different orders of arachnids while also attempting to standardize the terminology of the different types of immature instars occurring. They used immature juveniles instead of larvae and juveniles instead of nymphs. Here I follow the names already established among harvestmen specialists, namely, larva, nymph, and adult. There is a wide range of life cycles among harvestmen, with some species being stenochrone and others eurychrone (see Chapter 7). With regard to longevity of adults, there are annual species with two to three months of postembryonic duration and ephemeral adults, biennial species, and perennial species with one year of postembryonic duration and adults that live for more than three years (references in Table 13.1). This chapter presents information regarding embryonic and postembryonic development; phenology and reproductive biology are treated in Chapters 7 and 12, respectively.

455

—

Oligolophus tridens

Phalangium cinereum

—

0.53–0.56; 0.75–0.8

0.9

Odiellus gallicus

Opilio parietinus

—

—

Lacinius horridus

—

—

Lacinius ephippiatus

Lophopilio palpinalis

—

Homolophus biceps

Mitopus morio

—

Eumesosoma roeweri

Phalangiidae

EUPNOI

—

0.55–0.6

Parasiro coiffaiti

Siro rubens

—

Cyphophthalmus duricorius

Sironidae

CYPHOPHTHALMI

Taxa

—

0.56–0.82

—

1.08

—

—

—

—

—

—

—

—

—

—

180; 120–150

150–180 (30°C)

80 (11.5°C); 150 (21°C)

42–56 (20°C–22°C)

180

120 (20°C); 150

240 (20°C)

—

40 (~18°C)

60–90 (15°C)

—

—

Embryonic duration At oviposition At hatching (days)

Egg size (mm)

—

—

15 (21°C)

10–60

—

—

—

—

—

—

4–7

—

—

Larval phase duration (days)

—

—

5

5 (rarely 4)

5

4

—

5

—

—

5

—

—

Number of nymphs

Table 13.1 Summary of embryonic and postembryonic development in harvestmen

~2–3

5

3–3.5 (21°C)

2.5–3.5 (11.5°C); 4–6 (16°C)

—

3.5

3–3.5

3.5

—

—

24–48 (10°C–17°C)

—

—

—

—

—

2–3 (16°C)

—

< 1.5

4

3.5

~3

—

54–60 (10°C–17°C)

66–72 (10°C–17°C)

60–72 (10°C–17°C)

Nymphal phase duration Adult duration (months) (months)

Weed, 1897

Henking, 1886; Faussek, 1892; Holm, 1947; Pfeifer, 1956

Gueutal, 1943; Pfeifer, 1956; Naisse, 1959; Parisot, 1962

Juberthie, 1957a, 1960a, 1964, 1965; Naisse, 1959

Tischler, 1967

Pfeifer, 1956

Pfeifer, 1956; Parisot, 1962

Pfeifer, 1956; Winkler, 1957*

Schmoller, 1970

Cokendolpher, 1981b

Juberthie, 1960b, 1964, 1965

Juberthie, 1964, 1965

Juberthie, 1964, 1965

References

—

Leiobunum vittatum

— 0.85

0.9

Ischyropsalis hellwigii

Ischyropsalis luteipes1

Ischyropsalis nodifera1

Ischyropsalididae

Dicranolasma scabrum

Dicranolasmatidae 0.67 × 0.45

—

Leiobunum townsendi

DYSPNOI

~0.75

0.8

0.56–0.62

0.55

0.67–0.71

—

Leiobunum rotundum

Homalenotus quadridentatus1

Sclerosomatidae

Platybunus triangularis

Platybunus bucephalus

Phalangium opilio

Phalangium cornutum

—

—

—

—

—

—

—

—

—

0.64

—

—

50 (11.5°C)

44 (11.5°C)

102 (10°C–11°C)

35–42 (20°C)

—

40 (~18°C)

—

30 (10°C–17°C)

28–43; 43–53 (RT)

56 (RT); 45 (20°C–24°C)

28–42 (30°C); 40 (20°C); 30 (30°C)

45–60 (RT)

—

—

—

90 (15°C–20°C)

—

—

15 (21°C)

60–90

—

15–30 (20°C–24°C)

15

—

6

6 (rarely 5)

—

6

—

—

—

6

6

5

6–8 (rarely 5)

—

5–6 (11.5°C)

4–4.5 (11.5°C)

—

12–18 (15°C–20°C)

~2–3

—

—

—

7–8

2–3 (20°C–24°C)

2.5 (15°C); 2 (20°C)

—

6–8 (11.5°C)

6–8 (11.5°C)

—

24–36 (15°C–20°C)

—

—

—

6–10 (10°C–17°C)

—

—

—

—

(Continued)

Juberthie, 1964, 1965; Martens, 1965

Juberthie, 1964, 1965; Martens, 1965

Martens, 1965

Gruber, 1996

Weed, 1897

Cokendolpher, 1981b

Henking, 1886; Purcell, 1892; Naisse, 1959

Juberthie, 1957a, 1964, 1965

Todd, 1949; Pfeifer, 1956; Moritz, 1957*

Immel, 1955; Parisot, 1962

Gueutal, 1943; Todd, 1949; Pfeifer, 1956; Moritz, 1957, 1959; Winkler, 1957; Naisse, 1959; Parisot, 1962; Juberthie, 1964; Bachmann & Schaefer, 1983a

Faussek, 1892

0.85

Ischyropsalis superba1

—

1.1–1.5 × 0.4–0.8

Trogulus tricarinatus

0.95

1.1

Cynortoides cubanus

Erginulus clavotibialis

Cosmetidae

—

1.1–1.2

—

1.3–1.7 × 0.7–1.0

Trogulus nepaeformis

LANIATORES

—

—

—

0.8–1.1 × 0.3–0.4

—

—

—

—

—

Anelasmocephalus cambridgei

Trogulidae

Sabacon viscayanus

Sabaconidae

Nipponopsalis abei 2

Nipponopsalididae

0.65–0.75

0.85

Nemastoma quadripunctatum

Paranemastoma sillii

—

Mitostoma pyrenaeum1

Nemastomatidae

—

1.3 × 1.8

Ischyropsalis strandi 1.10

—

At oviposition At hatching

Egg size (mm)

1.4

Ischyropsalis pyrenaea1

Taxa

Table 13.1 Continued

23–27 (20°C); 13 (26°C)

16.5 (25°C); 27.5 (20°C)

42–207 (20°C)

44–226 (20°C)

47–206 (20°C)

—

—

27 (16°C)

56–60 (20°C–24°C)

—

—

142 (5°C–6.5°C)

58 (11.5°C)

Embryonic duration (days)

—

—

—

—

—

—

—

—

30–60 (20°C–24°C)

—

—

—

—

Larval phase duration (days)

6

6

5

5

4

—

6

6

6

—

6

—

6

Number of nymphs

4

2.5 (22°C–24.5°C)

4–5 (5°C–17°C)

3.5–8.5 (5°C–17°C)

1–6.5 (5°C–17°C)

—

3

—

30 (20°C–25°C)

15.5–35.5 (5°C–17°C)

12.5–25 (5°C–17°C)

23–34 (5°C–17°C)

12 (10°C–17°C)

—

—

> 14 (20°C–24°C)

> 2.5 (20°C–24°C) ~2.5 (5°C–21°C)

—

6–8 (11.5°C)

< 12 (11.5°C)

—

≥ 24 (5°C–6°C)

6–8 (11.5°C)

—

6–7 (11.5°C)

Nymphal phase duration Adult duration (months) (months)

Goodnight & Goodnight, 1976

Juberthie, 1972

Pabst, 1953

Pabst, 1953; Juberthie, 1964

Pabst, 1953

Juberthie, 1964, 1965

Miyosi, 1942

Avram, 1973

Immel, 1954

Juberthie, 1964

Juberthie, 1964, 1965

Juberthie, 1965, 1974

Juberthie, 1964; Martens, 1965

References

— —

Metalibitia paraguayensis

Vonones sayi

1.44 2.01 1.46 1.25 — — 1.52 1.58

Acutisoma longipes

Acutisoma proximum

Acutisoma aff. proximum

Discocyrtus oliverioi

Discocyrtus pectinifemur

Discocyrtus prospicuus

Goniosoma albiscriptum

Goniosoma geniculatum

1.51 — — — 1–1.3

Goniosoma sp.

Hernandaria scabricula

Holoscotolemon querilhaci1

Pachyloides thorelli

Pachylus quinamavidensis

2.1–2.3

1.44

Acutisoma discolor

Goniosoma spelaeum

1.02

Acanthopachylus aculeatus

Gonyleptidae

—

Gryne orensis

1.6

—

—

—

1.91

—

2.11

1.97

—

—

1.33

1.89

—

1.91

1.85

—

—

—

—

37 (20°C)

~30 (Lab)

40 (11°C–13°C)

~30 (Lab)

—

30–60

—

24–60

~30 (Lab)

—

—

—

—

45–64

—

~30 (Lab)

20–38 (5°C–20°C)

~30 (Lab)

~30 (Lab)

6

2–10 (20°C)

—

—

—

7

—

—

—

—

> 60 —

—

—

—

—

—

—

—

—

—

—

—

—

—

—

21–41

—

—

—

—

—

—

—

—

—

—

—

4 (18°C)

—

4–5 (10°C–17°C)

—

—

~18

—

—

—

—

—

—

—

—

—

—

—

—

—

36–48 (20°C)

—

18 (10°C–17°C)

—

—

> 24

—

—

—

≤ 36; 54 (Lab)

—

—

—

—

—

—

> 36 (5°C–20°C)

—

—

(Continued)

Juberthie & Muñoz-Cuevas, 1971; MuñozCuevas, 1971a,b,c, 1973

Canals, 1936

Juberthie, 1964, 1965

Canals, 1936

Machado, 2002

Gnaspini, 1995

Machado, 2002

Willemart & Gnaspini, 2004a

Canals, 1936

Matthiesen, 1985

Elpino-Campos et al., 2001

Machado, 2002

Ramires & Giaretta, 1994

Machado & Oliveira, 1998

Machado, 2002

Canals, 1936; Capocasale & Bruno-Trezza, 1964

Cokendolpher & Jones, 1991

Canals, 1936

Canals, 1936

— —

Scotolemon lespesi1

Scotolemon lucasi

2.0

—

—

—

—

—

—

—

—

—

—

—

68 (11°C–13°C)

55–70 (11.5°C)

30 (20°C)

—

15–20

~30 (Lab)

~30 (Lab)

Embryonic duration (days)

—

—

—

—

—

—

—

—

—

Larval phase duration (days)

—

—

—

5

—

—

—

—

—

Number of nymphs

—

—

—

5 (10°C–17°C)

4–6 (10°C–17°C)

—

—

—

—

—

—

18 (10°C–17°C)

24–30 (10°C–17°C)

24–42 (10°C–17°C)

—

—

—

—

Nymphal phase duration Adult duration (months) (months)

Mitchell, 1971

Martens, 1993b

Juberthie, 1964

Juberthie, 1964, 1965

Juberthie, 1964, 1965

Miyosi, 1941

Rodríguez & Guerrero, 1976

Canals, 1936

Canals, 1936

References

Dashes indicate lack of information. Species with complete descriptions of embryonic development are marked with an asterisk. Some data on the duration of developmental phases are followed by the temperature in which the eggs and/or nymphs were reared. RT = room temperature (without any explanation in the original data about the exact climatic condition). “Lab” indicates that the study was carried out in the laboratory, but no temperature was recorded. When not stated, data were obtained from field experiments. 1. Juberthie (1964) noted that the development of this species was primarily the same as that of other studied species. 2. Miyosi did not clearly state the number of nymphs, but 6 were deduced on the basis of his descriptions.

Hoplobunus boneti

Stygnopsidae

Leytpodoctis oviger

0.8–1.1

—

Scotolemon doriae

Podoctidae

0.7

Pseudobiantes japonicus

Phalangodidae

Zygopachylus albomarginis

—

—

Pygophalangodus canalsi

Manaosbiidae

—

At oviposition At hatching

Egg size (mm)

Parapachyloides fontanensis

Taxa

Table 13.1 Continued

Development

A BRIEF HISTORICAL ACCOUNT Balbiani (1872), who studied Phalangium cornutum (Phalangiidae), was the first to describe the embryology of harvestmen. Until the middle of the twentieth century, knowledge of the embryonic development of harvestmen was mainly based on the studies of Balbiani (1872) and Faussek (1892), who studied Opilio parietinus (Phalangiidae), and Schimkewitsch (1898), who studied an unidentified phalangiid. Other articles from the end of the nineteenth century, including Henking (1886) with O. parietinus and Leiobunum rotundum (Sclerosomatidae) and Purcell (1892) with L. hemisphaericum, did not provide an adequate account of the embryology of the group, and some of their data should be considered with caution. Holm (1947) conducted a more detailed study of O. parietinus and provided figures of its main stages, while Dawydoff (1949) provided an early review on embryology, but little was recorded about harvestmen. From the 1950s to the 1970s several studies (e.g., Pabst, 1953; Pfeifer, 1956; Moritz, 1957, 1959; Winkler, 1957; Juberthie, 1964; Muñoz-Cuevas, 1971b, 1973; Avram, 1973) and comparative reviews (D. T. Anderson, 1973; Yoshikura, 1975) were published that provided the basis for the current knowledge on harvestman embryology. Concerning postembryonic development, the first descriptive studies were probably those from Miyosi (1941, 1942), published in Japanese, but mostly neglected. The study by Gueutal (1943) dealt mainly with the duration of each nymph. Pabst (1953) and Immel (1954, 1955) presented more detailed surveys, but the first extensive reference is the published thesis of Juberthie (1964). Afterward a series of mainly descriptive and comparative articles followed (Edgar, 1971; Muñoz-Cuevas, 1971a,c; Goodnight & Goodnight, 1976; Gnaspini, 1995; Gruber, 1996). The most extensive developmental studies considered species of Eupnoi and Dyspnoi from the Northern Hemisphere; Laniatores, mostly from the Neotropical region, have only recently been studied in more detail (Table 13.1). Until now, approximately 35 species (2 Cyphophthalmi, 11 Eupnoi, 12 Dyspnoi, and 10 Laniatores) have been the subject of ontogenetic studies. This number would increase to at least 76 species (3 Cyphophthalmi, 26 Eupnoi, 19 Dyspnoi, and 28 Laniatores) if we added assorted information from articles not dealing specifically with development or from comments within studies on development.

EMBRYONIC PHASE Embryonic development begins just after oviposition and ends at the time of eclosion, when the larva hatches. Since larval organogenesis is the last phase during embryonic development, some authors prefer to consider the last embryonic phase as ending when the larva has formed inside the eggshell and the heart begins to beat (Muñoz-Cuevas, 1971b).

461

462

Development

Eggs Balbiani (1872) described the eggs of Phalangium cornutum as measuring 1.2 mm in diameter, being spheroidal and light yellowish in color in the beginning, and later becoming grayish because of pigmentation of the embryo. According to Balbiani (1872), the egg is surrounded by two membranes, an outer thin chorion and an inner thicker vitelline membrane. Holm (1947) also subsequently detected a structure resembling a micropyle. Many eggs are spheroidal; others may be ovoid or elongated and whitish to grayish white in color (Juberthie, 1964). In some species the egg batches are surrounded by mucus (Figure 13.1A), but not in others (Figure 13.1B), and the eggs

A

C

B

D

Figure 13.1. (A) Clutch of Iporangaia pustulosa (Gonyleptidae) on the undersurface of a leaf in southeastern Brazil, composed of eggs surrounded by an abundant mucus coating in different embryonic stages. (B) Clutch of Acutisoma proximum (Gonyleptidae) showing recently laid eggs without mucus coating on a rock in southeastern Brazil (photos: B. A. Buzatto). (C) Eggs from Goniosoma spelaeum (Gonyleptidae) near hatching on a cave wall in southeastern Brazil. Note that eyes, legs, and color patching of the body can be observed through the egg chorion. (D) View of eggs; a larva (L) with its curved and short legs; a larva molting into a first nymph (M), in which the legs still attached to the exuvium can be seen; and two first nymphs (N) from Goniosoma spelaeum still attached by the anal lobe to the exuvium (photos: P. Gnaspini). Scale bars = 10 mm.

Development

Figure 13.2. Embryonic development of the gonyleptid Pachylus quinamavidensis (Gonyleptidae). Roman numerals indicate the embryonic developmental phase, and L indicates the “larval phase,” beginning after the first heartbeat. For the same stage, S, A, V, and D indicate side, anterior, ventral, and dorsal views of embryo, respectively. Mouthparts are formed on the 21st day, while eyes, heart, and digestive caecum are formed on the 22nd day. Modified from Muñoz-Cuevas (1971b).

may be laid inside a substratum (mostly in soil) or on surfaces (see Chapter 12). Egg size varies among groups and species, generally between 0.5 and 2.3 mm. At the beginning of embryonic development the eggs increase in size and weight by absorbing water from the air and/or from the hygroscopic mucus that surrounds them, and they therefore need a high relative humidity (Henking, 1886; Juberthie, 1964, 1965). The size of eggs, both when laid and after growth by absorbing water, is compiled in Table 13.1.

Description of development Holm (1947), Moritz (1957), and Juberthie (1964, 1965) used different schemes to divide embryonic development into phases. Juberthie’s scheme, the most commonly used in recent descriptions, divides embryonic development into five phases (Figure 13.2): (1) cleavage; (2) formation of the germ band; (3) metamerization of the prosoma, when there are important cellular migrations, and cephalic and anal plates and appendage buds appear; (4) inversion, when abdominal somites, mouth, and eye-primordium appear, legs take the final length, the body wall is formed, and the genital plate migrates anteriad between the leg coxae; (5) larval organogenesis, including formation of the digestive diverticulum, the differentiation of eyes and heart and, after the first heartbeat, the larval period (for details, see Chapter 2). The duration of each phase is known only for the following three species:

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Development

the phalangiid Odiellus gallicus (6, 9, 5, 25, and 35 days, respectively), the ischyropsalidid Ischyropsalis luteipes (4, 6, 5, 10, and 15 days), and the gonyleptid Pachylus quinamavidensis (5, 5, 3, 8, and 16 days) (references in Table 13.1).

Duration Embryonic development generally takes around 30 to 60 days (Table 13.1), but greatly depends on season and temperature. For instance, the eggs of Opilio parietinus die if they are maintained at room temperature since they need to pass through a cold winter, and further development is achieved when they are placed upon the ground (Faussek, 1892). Eggs of many species from temperate regions hibernate, which is the case for the phalangiids Mitopus morio, Oligolophus spp., Opilio parietinus, and Phalangium opilio, the sclerosomatid Leiobunum rotundum, the nemastomatid Nemastoma lugubre, and several ischyropsalidids of the genus Ischyropsalis (Kästner, 1935b; Pfeifer, 1956; Phillipson, 1959; Martens, 1965; Bachmann & Schaefer, 1983a). In contrast to these species, trogulids reproduce year-round. Development may take from 5 to 8 weeks for summer eggs (June–August) to 12 to 15 weeks for hibernating winter eggs (February) (Pabst, 1953). However, winter and summer eggs develop at the same rate when artificially maintained at 20°C. Obligatory diapause induced by changes in temperature was described in a German population of M. morio in which eggs are laid during the late summer and hatching occurs in the spring (Tischler, 1967). Embryological development proceeds at summer temperatures until it is interrupted at a genetically predetermined stage. Development remains lapsed until low temperatures trigger completion of the second phase of embryogenesis. The last phase takes place only with the advent of warm spring weather. Thus the first and third phases take place only at higher temperatures, whereas the second phase demands lower temperatures. In this way untimely hatching in the fall and winter is prevented, and nymphs do not appear until adequate food is available in the spring. The effect of temperature on egg development has been reported for several species (see also Table 13.1). Development in Odiellus gallicus takes 162 days at 6°C, 146 days at 7°C, and 84 days at 11.5°C; minimum and maximum lethal temperatures are, respectively, 0°C and 20°C, but no mortality is detected between 6°C and 11.5°C (Juberthie, 1960a). In Pachylus quinamavidensis (Gonyleptidae) development takes 70 days at 12°C and 37 days at 20°C; development is abnormal below 8°C and above 25°C; no development occurs at 5°C (Muñoz-Cuevas, 1971b). In Paranemastoma sillii (Nemastomatidae) the hatching rate is reduced at higher temperatures from about 95% above 18°C to 0% at 20°C–21°C (Avram, 1973). Development of the eggs of P. opilio is strongly delayed at lower temperatures and not even possible at 10°C within 250 days, while taking 129 days at 15°C, 40 days at 20°C, and 30 days at 25°C, and at 11.8°C the development was estimated to be zero (Bachmann & Schaefer, 1983a). Juberthie (1964) and Avram (1973) presented further discussion about the influence of temperature and humidity on embryonic development.

Development

Anomalous development Anomalous specimens have been recorded and experimentally produced several times. Gynandromorphs and intersexual specimens were recorded in Mitopus morio (Cokendolpher & Sissom, 1988) and Phalangium opilio (Bl´aszak, 1968) and in the sclerosomatids Gagrellula ferruginea (Suzuki, 1980b), G. montana (Tsurusaki, 1982b), Leiobunum globosum (Suzuki, 1980a), and Melanopa grandis (Tsurusaki, 1982b). Andromorphy in females is a rarer phenomenon and was reported only for Nemastoma dentigerum (Chemini, 1984). Teratological specimens have been recorded and experimentally produced in Odiellus gallicus (see Figures 2.6e,f in Chapter 2).

LARVAL PHASE Close to hatching, in cases where the chorion is transparent, it is possible to see the developing larva (Figure 13.2). The larva is the first free instar after eclosion, presenting several incomplete features if compared with the first nymphs (see discussion in Juberthie, 1965). The legs typically bend around the body in order to fit inside the round eggs during development (Figure 13.2). In Eupnoi, Dyspnoi, and Laniatores the larva hatches in a more mature stage than in Cyphophthalmi and quickly molts into the first nymph (Table 13.1). In contrast, in Cyphophthalmi hatching occurs earlier in larval formation, and the hatchling spends four to seven days as a larva before molting into the first nymph (Juberthie, 1960b, 1965). The larvae of Cyphophthalmi, Eupnoi, and Dyspnoi are equipped with one or two frontally located egg teeth (at the median anterior margin of the prosoma, between the chelicerae) that help in breaking the eggshell. Egg teeth are lacking in nymphs. Balbiani (1872) was the first to record an egg tooth in a late harvestman embryo. Larvae of Eupnoi (e.g., Astrobunus grallator, Megabunus diadema, Odiellus gallicus, Oligolophus tridens, Paroligolophus agrestis, Phalangium opilio, Platybunus triangularis, Homalenotus quadridentatus, and Leiobunum spp.; Juberthie, 1957a, 1964; Naisse, 1959; Edgar, 1971), and most Dyspnoi (e.g., Paranemastoma sillii and Dicranolasma scabrum; Avram, 1973; Gruber, 1996) have one egg tooth. Dyspnoi of the family Ischyropsalididae, such as Ischyropsalis luteipes, I. nodifera, I. pyrenaea, and I. hellwigii locantei, have two egg teeth (Juberthie, 1964). The larva of the sironid Siro rubens also has two egg teeth (Juberthie, 1960b, 1964). No egg teeth occur in the cosmetids Erginulus clavotibialis (Goodnight & Goodnight, 1976) and Vonones sayi (Cokendolpher & Jones, 1991), or in the gonyleptid Pachylus quinamavidensis (Muñoz-Cuevas, 1971b). Absence of egg teeth may be the rule in Laniatores, at least among Grassatores.

465

466

Development

NYMPHAL PHASE The number of nymphs varies among the different harvestman species studied (sometimes even within the same species), being six in most cases, but ranging from four to eight in others (Table 13.1). The last nymphal stage is generally called the “subadult.” The number of nymphs is independent of the final size of the adult harvestman (Juberthie, 1964).

Growth During postembryonic development each molt results in a larger animal. Since body size may depend on the amount of food previously ingested, length and width measurements are generally not appropriate for documenting growth. In contrast, the appendages are adequate structures for documenting growth and have been used in most comparative studies. The percentage growth of some structures between consecutive instars of various species of harvestmen is given in Table 13.2. The three trogulids studied by Pabst (1953) show a change in body length of approximately 130% at each molt, being a little larger during the molt from larva to first nymph. Additionally, it should be mentioned that at least in Goniosoma spelaeum (Gonyleptidae), there is no clear allometric growth for the appendage segments, that is, they keep the same proportion through the successive nymphal and adult stages (Gnaspini, 1995). Juberthie (1964), referring to a “larval step,” noted especially rapid growth in phalangiids, sclerosomatids, and ischyropsalidids as a whole. The growth rate declines afterward to less than half the larva/first nymph growth rate. In the final molt to adulthood, he also noted that females of Homalenotus quadridentatus (Sclerosomatidae) have the same growth rate as nymphs, but males have an increased growth rate. These characteristics can be observed in other species (Table 13.2). The differential male/female growth at each instar in G. spelaeum can be observed in Figure 13.3. Another interesting characteristic of this species is that the growth rate from first to second nymph is much larger than the subsequent ones.

Morphological and morphometric nymphal changes during growth Many structures develop or increase in size and/or complexity during postembryonic development, as the following examples illustrate. Among Eupnoi and Dyspnoi the setae of the legs generally increase in number and size and may change shape. The shape of the body and ocularium may also change with age (A. Müller, 1925; Miyosi, 1942; Juberthie, 1957a, 1964). The nymphal stages of Phalangium opilio can be separated from one another by the number of tarsal joints (Bachmann & Schaefer, 1983a). In Paranemastoma sillii the pseudoarticulation of femora increases (Avram, 1973), and in Dicranolasma scabrum (Dicranolasmatidae) the hood progressively grows (Gruber, 1996). In Gonyleptidae and other Laniatores the armature of pedipalps and legs, as well as the number of tarsomeres, increases (MuñozCuevas, 1971a; Gnaspini, 1995). Secondary sexual characters are highly variable within harvestmen and may in-

Development

467

Table 13.2 Examples of percentage growth of different structures with age among harvestmen Taxa

Body part

to N1

to N2

to N3

to N4

to N5

to N6

to Adult

Reference

Phalangium opilio

Body

?

163

122

158

137

119

135F, 119M

Naisse, 1959

Homalenotus quadridentatus

LI

300

90

90

90

90

90

90F, 130M

Juberthie, 1964

LII

500

80

80

80

80

80

80F, 130M

LIII

300

70

70

70

70

70

70F, 180M

LIV

400

80

80

80

80

80

80F, 140M

Pedipalp

200

80

80

80

80

80

80F, 100M

Leiobunum calcar

LIV

?

?

?

?

?

156

146F, 143M

Edgar, 1971

Leiobunum longipes

LIV

?

?

158

174

169

156

175F, 155M

Edgar, 1971

LIV

?

?

?

?

?

161

150F, 144M

Edgar, 1971

Body

?

150

117

164

135

113

171F, 129M

Naisse, 1959

Leiobunum politum Leiobunum rotundum Leiobunum vittatum Dicranolasma scabrum

Nemastoma quadripunctatum

Paranemastoma sillii

Nipponopsalis abei1 Goniosoma spelaeum

LIV

?

?

?

?

150

156

161F, 150M

Edgar, 1971

LI

171

124

123

132

133

126F, 133M

137F, 142M

Gruber, 1996

LII

229

125

125

126

134

128F, 135M

135F, 141M

LIII

173

123

126

133

135

128F, 133M

138F, 143M

LIV

196

128

126

131

138

130F, 134M

141F, 147M

Body

117

136

127

130

132

134F, 133M

145F, 143M

LI

204

131

124

135

114

123

131

LII

244

127

124

137

110

105

153

LIII

189

127

133

129

114

131

140

LIV

240

125

135

143

104

115

142

Body

91

119

152

118

131

139

115

LI

219

131

134

104

138

169

133

LII

255

151

120

109

136

152

145

LIII

226

126

140

101

145

164

133

LIV

230

122

138

109

141

163

138

120

Body

100

138

Body

?

143

LI

?

177

139

117

116

150

170

155

129

140

?

142

126

131

102

LII

?

160

144

137

120

128

106

LIII

?

170

142

135

124

129

104

LIV

?

170

137

135

121

125

105

Pedipalp

?

169

133

139

129

129

109

Immel, 1954

Avram, 1973

Miyosi, 1942 Gnaspini, 1995

A question mark (?) indicates information not provided. N1 to N6 indicate nymphal stages from the first to the sixth. LI to LIV indicate legs from I to IV. 1. Miyosi did not clearly state the number of nymphs, but six nymphs were deduced on the basis of his descriptions. He did not provide data for the alleged third nymph; thus the percentage growth was added in the table from the second to the fourth nymph.

468

Development

Figure 13.3. Growth of appendages during the development of Goniosoma spelaeum (Gonyleptidae) for males (light gray) and females (dark gray). White boxes represent nymphs in which sex is not recognizable externally. Each box represents the average ± standard deviation, while the lines represent the upper and lower observed intervals. The numbers 1–5 = first to fifth nymphal instars; sA = subadult; A = adult. Modified from Gnaspini (1995).

clude color and the shape of body, chelicerae, pedipalps, genital opening, anal plate, sternites, tergites, and legs, among others (see Chapters 4 and 12). In Eupnoi and Dyspnoi these sexual characters commonly appear in the penultimate instar (or subadult) and seldom in the antepenultimate instar (Juberthie, 1964). In Laniatores secondary sexual characters are generally conspicuous and appear in the antepenultimate instar (Muñoz-Cuevas, 1971a; Gnaspini, 1995). Although most Opiliones have a single claw on each leg, Laniatores have complex claws on legs III and IV (see Chapter 4). Among Insidiatores (Travunioidea) legs III and IV have a complex claw, which is generally three-branched, but may have more side branches with a single insertion at the tarsus. A transformation series from a three-branched state to a complex peltonychium was discussed by Hunt and Hickman (1993) on the basis of species of Lomanella (Triaenonychidae). Among the Grassatores legs III and IV have two single claws independently inserted into the tarsus, although the claws may fuse at the base. Accessory structures between the

Development

two tarsal claws that differ in the nymphal and the adult phases are present in Grassatores. According to Muñoz-Cuevas (1971c), in all nymphal stages except the subadult, two typical “juvenile structures” are found ventrally in both third and fourth leg tarsi: one projection similar to a third tarsal claw, called a pseudonychium, and a fleshy projection, called an arolium (Figures 13.4A,B; see also Chapter 2). These structures grow during nymphal development but are not observed in either the last nymphal stage (the subadult) or in the adult (see Muñoz-Cuevas, 1971a,c; Gnaspini, 1995; Figures 13.4C,D). Conversely, a third structure in most Gonyleptoidea (Cosmetidae, Cranaidae, Gonyleptidae, Manaosbiidae, and Stygnidae), called

A

C

PS

B

D

Figure 13.4. Apex of tarsus IV of the cosmetid Cosmetus variolosus (photos: P. Gnaspini). (A–B) nymph: lateral and frontal views. (C–D) Adult: lateral and dorsofrontal views. AR = arolium; PS = pseudonychium; TC = tarsal claw; TP = tarsal process.

469

470

Development

a tarsal process, may grow gradually with each molt, but develops fully only in adults (Muñoz-Cuevas, 1971a,c). A dorsal projection on the apex of the last tarsomere generally bears a long and unusual seta (Figure 13.4C,D). These differences during growth have been well documented only in Pachylus quinamavidensis (MuñozCuevas, 1971a) and Goniosoma spelaeum (Gnaspini, 1995). Although not specifically studying development, Martens and Schwendinger (1998) illustrated oncopodid species in which the juvenile structures are lacking in the adults, whereas a well-developed arolium can be observed in the leg IV of a juvenile. In addition, Miyosi (1941) recorded “a structure similar to what is called an arolium” in Pseudobiantes japonicus (Epedanidae). Hence the juvenile structures probably occur in all Grassatores, whereas the tarsal process only occurs in certain families. Among Insidiatores differences in tarsal structures appear at different ages, that is the tarsus also changes through ontogeny (e.g., Muñoz-Cuevas & Vachon, 1979). However, the structures involved may be different, since the juvenile structures just discussed for Grassatores may be lacking among Insidiatores (e.g., Briggs, 1969, 1971a, for nymphs with and without arolium, respectively).

Molting The posture assumed during molting varies with the group. In most groups, especially the long-legged species, the animals hang from a substratum for molting. Eupnoi species hang by all four pairs of legs, while Laniatores use only those with an arolium (pairs III and IV), which enhance substrate adherence, even on glass (Juberthie, 1972). During molting the individual displays periodic body contractions and extends the legs while hanging from the exuvium, to which they are linked by the anal operculum (Parisot, 1962; Edgar, 1971; Gnaspini, 1995; Figure 13.5). When the process is complete, the animal hangs from the ceiling by its legs and detaches from the exuvium. Afterward many species (except Phalangiidae) take the exuvium in their pedipalps and manipulate it with their mouthparts, which probably allows recovery of water from the exuvial fluid. The larva and nymphs of Dicranolasma scabrum may hang, but generally remain on the ground, moving upward, releasing their legs vertically, and “sitting” on the anal lobe, which detaches last from the exuvium; finally the animal moves forward, standing on its legs (Gruber, 1996). Nymphs of Siro rubens build a molting chamber made within a fissure of the substratum, which they block with debris (Juberthie, 1960b).

Duration The duration of postembryonic development in different species is summarized in Table 13.1. It should be noted that the duration of the nymphal phase is not directly proportional to the final size of the adult (Juberthie, 1964). The postembryonic phase generally occurs within several months, although lengthier periods (over two to three years) have been recorded in Cyphophthalmi, Dicranolasmatidae, and some Gonyleptidae, not to mention specialized cave species (Juberthie, 1964; Gnaspini, 1995; Gruber, 1996).

Development

A

B

Figure 13.5. (A) Nymphs of Acutisoma proximum (Gonyleptidae) and (B) Jussara sp. (Sclerosomatidae) molting on vegetation in southeastern Brazil (photos: B. A. Buzatto). Scale bars = 10 mm.

Temperature also plays a role in the duration of postembryonic development. For instance, Bachmann and Schaefer (1983a) showed that no individual of Phalangium opilio reached adulthood at 10 °C. They also recorded a minimum of 75 days at 15°C and a minimum of 58 days at 20°C. Weed (1897) recorded Leiobunum ventricosum hibernating as nymphs (one-third the full-grown size).

ADULT PHASE It is widely considered that adult harvestmen do not molt. Indeed, this is the case for most groups with a genital operculum, in which the operculum generally appears (already open) only in adults (e.g., Juberthie, 1957a). However, Muñoz-Cuevas (1971a) and Gnaspini (1995) noticed that in some Grassatores species the genital operculum, which was fused to the body during the early nymphal stages, becomes free in the subadult, suggesting that the subadult is already sexually mature. Gnaspini et al. (2004) recorded the presence of a complete penis in subadult Grassatores and observed a subadult male copulating. Together with the morphological study of several species, Gnaspini et al. (2004) proposed that Grassatores have a unique life cycle among arachnids with two instars in the adult phase: the subadult and the adult. A similar life cycle is known only in mayflies (Ephemeroptera), which

471

472

Development

also reproduce as subadults. This hypothesis deserves further testing, and detailed studies of a more inclusive number of species are necessary. The duration of the adult phase for different species is listed in Table 13.1. In summary, Eupnoi generally have a short life span of a few months, whereas other groups, especially Cyphophthalmi and Laniatores, may live for several years as adults, even those species subjected to harsh winter conditions.

CONCLUDING REMARKS Despite the few species studied, development of harvestmen appears to be fairly homogeneous in different taxa. Although morphology and egg size vary greatly, embryological development generally takes one to two months, or a little longer in the case of temperate species that pass through winter egg diapause. The postembryonic phase, including a larva, a varied number of nymphs, and one or two reproductive stages, may take from a few months to several years.

ACKNOWLEDGMENTS The author is a recipient of a research grant from FAPESP (00/04686-4) and of a research fellowship from CNPq (300326/94-7). Dr. A. A. Ribeiro and E. Mattos allowed and facilitated the use of the electron microscope (LME-IBUSP). I am deeply indebted to C. F. Lerche, who helped with the translation of papers in German, to M. R. Hara, who helped with the translation of papers in Japanese, to B. A. Buzatto for providing photographs, and to S. Hoenen, G. Machado, and two reviewers for their critical review of the manuscript.

CHAPTER

14

Ecophysiology Flávio H. Santos

T

he main objective of ecophysiology is to reveal mechanisms that allow an organism to maintain efficient physiological function under different environmental conditions (Willmer et al., 2000). Because basic physiological challenges result from abiotic factors, the most interesting and remarkable physiological modifications are registered in extreme environments (Cloudsley-Thompson, 1988). Most harvestman species occur in temperate to warm, humid environments and may be less interesting for ecophysiological studies than those species that inhabit polar or desert areas. This may explain in part the small number of studies devoted to harvestman ecophysiology. A large number of harvestman species occur in tropical and subtropical areas, which in most cases are physiologically slightly stressful, with moderate variations of temperature and humidity throughout the year (Cloudsley-Thompson, 1988). Although harvestmen are also found in deserts, caves, and subarctic and subantarctic areas, these species have been rarely studied. Basic aspects of harvestman physiology are poorly known, and detailed morphological descriptions of certain internal organs are still necessary (see Chapter 2). Some classical studies on harvestman behavior and ecology also include remarks on ecophysiology, especially on biological rhythms. However, the ecophysiological data presented in these studies should be considered with care since knowledge in this area tends to become quickly outdated, mainly because of methodological improvements. Thus, in the absence of specific and updated information for harvestmen, generalizations must be derived from research on well-studied arachnids, such as spiders and scorpions. This chapter aims to present the basic functions of the main organ systems of harvestmen while examining their importance for survival in terrestrial environments. Some aspects of harvestman physiology are unclear, and in these cases the limits of our knowledge are presented and possible explanations are discussed. A detailed account of the morphology of the internal anatomy of harvestmen is addressed in Chapter 2. 473

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WATER BALANCE All terrestrial organisms continuously lose water to the environment, mainly through the integument and respiratory surfaces (Mantel, 1979). Moreover, maintenance of body water and proper ion concentration is one of the greatest challenges for terrestrial arthropods. Consequently, multiple organs and mechanisms are involved in minimizing water loss and improving water uptake. Since a general model of osmoregulation has never been proposed for harvestmen, the mechanisms of water gain and water loss are explained separately.

Integumentary water loss Few studies have focused specifically on the integument of harvestmen, and most concern histological aspects (Grainge & Pearson, 1966; see also Chapter 2). Consequently, part of the following discussion is based on spiders, scorpions, and insects, whose integument is very similar (Barth, 1969, 1970). The integument encompasses the cuticle, the epidermis, and the basal membrane. The cuticle is the main component, forming a barrier between the internal and external environments that reduces the rate at which water is lost from the animal. However, the presence of a cuticular exoskeleton also requires molting to allow growth, and results in a loss of waterproof protection during the exoskeleton change. During molting terrestrial arthropods become vulnerable, susceptible to predation and desiccation. Some harvestmen have developed particular behavioral mechanisms to avoid such problems (discussed later). The cuticle is a noncellular, heterogeneous layer secreted by epidermal cells. The cuticle of harvestmen (and all other arthropods) is divided into three main layers: epicuticle, exocuticle, and endocuticle (Murphree, 1988; see also Chapter 2). While the exocuticle and the endocuticle have elastic and structural functions, the epicuticle is responsible for the control of water loss (Cloudsley-Thompson, 1988). The epicuticle is composed of four distinct layers, of which the wax layer is the most significant waterproofing component. The disposition and thickness of the wax layer, which is directly related to the number and disposition of secretory cells located in the epidermis, plays an important role in the animal’s water-retention capacity. Nevertheless, the epicuticle does not provide complete protection against water loss, because the outward movement of water is facilitated by numerous fine openings, such as pore canals, pores of dermal glands, and sensory organs (Blomquist et al., 1987). The body surface is certainly the main route of water loss in arachnids (CloudsleyThompson, 1988); hence the large surface/volume ratio observed in some harvestman species is a clear disadvantage. Additional osmoregulatory mechanisms in the integument are required for controlling water balance. Osmoregulatory processes may occur in different levels of the integumentary layer. The first desiccation barrier is the wax layer, whose water permeability varies according to environmental humidity and temperature. Water can be lost when conformational changes in the wax layer cause epicuticular permeability to vary (Pulz,

Ecophysiology

1987). This layer is composed of bipolar lipid molecules, with their hydrophilic pole oriented toward the base of the epicuticule. Desiccation promotes additional glycoprotein and lipid deposition in the epicuticle, thus decreasing permeability across the body surface (Blomquist et al., 1987). The rate of water loss through the wax layer is directly correlated to environmental temperature, but the slope of this relationship is specific for each group of arthropods (e.g., Hadley, 1990). Another feature of the wax barrier in spiders, scorpions, and many other arthropods is an abrupt increase in the permeability of the lipid layer at a certain temperature, called the transition temperature. The transition temperature is species specific, ranging from 18°C to about 40°C (reviewed in Pulz, 1987). The explanation of this phenomenon remains controversial, because some authors believe that it is a consequence of a complete disorganization of the epicuticle by the melting of the lipid layer (Kirschner, 1987). In harvestmen neither variations among different taxa nor transitional temperatures have been described. However, the relationship between environmental humidity and cuticular permeability seems to be important to them and may determine seasonal and daily periods of activity, especially for species occurring in xeric environments (Edgar, 1971). Reduction of permeability at the apical membrane of the epidermal cells forms a second integumentary barrier to water loss (Mantel, 1979). In situations when the water-retaining efficiency of the wax layer decreases, such as high temperature or abrasion, osmoregulatory control is replaced by this barrier. However, wax-layer and apical-membrane mechanisms are not mutually exclusive and may act together to improve the osmoregulatory capability of the organism (Mantel, 1979). Some arachnids, such as ticks and whip spiders, have cuticular areas modified to absorb water vapor (Kaufman & Phillips, 1982). Harvestmen do not show this kind of water absorption and instead ingest water by drinking (Santos & Gnaspini, 2002).

Respiratory water loss Harvestmen have tube tracheae (Chapter 2; Figure 14.1A), and the distribution of tracheal branches is correlated with the anatomical distribution of organs with high oxygen demand (Höfer et al., 2000). Gas exchange occurs by diffusion through the tracheal wall along the length of the tracheae rather than at the tips of the tracheae, as occurs in insects (Schmitz & Perry, 2002). A great advantage of the tracheal system when compared with book lungs is rapid tissue oxygenation due to nearly direct contact between cells and oxygen. In groups with a combination of tracheae and book lungs, which include the vast majority of spiders, studies have demonstrated a relationship between morphology of the respiratory system and some behavioral aspects (Opell, 1998; Schmitz & Perry, 2000). In more active species the tracheal system is well developed, whereas the book lungs are reduced. The opposite relationship was observed in more sedentary species (Opell, 1998; Schmitz & Perry, 2000). Additionally, spiders that have only a tracheal system display metabolic rates higher than those of spiders that rely only on book

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A

B

Figure 14.1. (A) Dorsal view of the tracheal system of the gonyleptid Goniosoma sp. with the dorsal exoskeleton and digestive tube removed (photo: F. H. Santos). (B–C) Abdominal spiracles of the monoscutids (B) Pantopsalis sp. (entire left spiracle) and (C) Spinicrus sp. (entire right spiracle). Modified from Hunt (1990a).

C

Ecophysiology

lungs (J. F. Anderson, 1970). A similar study compared two species of harvestmen with different lifestyles. The tracheal supply to muscles in the slow-moving nemastomatid Nemastoma lugubre is less developed than in the more active sclerosomatid Leiobunum rotundum (Höfer et al., 2000). However, comparisons between distantly related species must be carefully interpreted because differences may result from phylogenetic distance or allometric bias and not from environmental or behavioral factors. Harvestmen do not perform abdominal ventilatory movements, and the rate at which tissues receive oxygen is determined by the rate of diffusion (Randall et al., 1997). Therefore, factors such as relative O2 pressure, length and diameter of tracheae, and air temperature determine the rate of gas exchange. It is unlikely that diffusion alone can provide enough oxygen to sustain very large or very active species, which may represent an important constraint on body size and metabolic rate in harvestmen (Randall et al., 1997). Comparative studies have demonstrated that the rate of water loss through tracheae is lower than the loss through book lungs (Lighton, 2002). This difference is mainly due to the presence of valvelike structures located at the end of the tracheae, which are responsible for air-flux and water-loss regulation, as well as protection against dust and parasites. In some harvestmen a partial reduction of the tracheal opening by a cuticle wall protected by spines forms a grill in the internal rim of the aperture (Figures 14.1B,C). These spines are relatively unbranched and tend to cluster into groups and fuse with one another (Hunt, 1990a). The spine length varies according to the taxonomic group and may be long enough to cover the entire tracheal opening (Figure 14.1B) or only part of it (Figure 14.1C). The tracheal opening, unlike arachnid book lungs or sieve tracheae, does not have associated musculature that may allow spiracular control (Höfer et al., 2000; Lighton, 2002). Arthropods that can control the opening and closing of their tracheal spiracles may display intermittent respiration, which consists of periodic ventilation by the opening of the spiracle, promoting the air exchange inside the tracheae. The intermittent respiration, observed in many arachnids, reduces water loss by restricting the period when the spiracle is opened. Lighton (2002), analyzing the kinetics of gas exchange in the desert harvestman Leiobunum townsendi, found no evidence of discontinuous gas exchange. Therefore, gas exchange in harvestmen is most likely to be dominated by simple diffusion without a prominent role for wide modulations of spiracular control. Modifications in size and form of tracheal openings, including the length and density of spines, when present, probably influence the rate of water loss. Nevertheless, a specific study to determine the contribution of the tracheal spiracle morphology to the water-loss rate has never been done. In spiders the contribution of the respiratory system varies from 1% to 12% of the total body-water loss (Lighton, 2002). However, reduction or loss of spiracle control may increase the water loss from the respiratory system to from 43% to 100% (Pulz, 1987). Thus it would seem that the low tolerance to dehydration observed in harvestmen in the laboratory (Edgar, 1971) and also in natural conditions (Santos, 2003) is a consequence of a weak osmoregulatory control of water loss in the tracheal system caused by the absence of an active spiracle.

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Digestive water loss Harvestmen have a complex arrangement of mouthparts that allows the ingestion of solid food (see Chapters 2 and 8). Nutrients are digested and absorbed in the anterior midgut, followed by indigestible components and excreta passing to the posterior midgut (Becker & Peters, 1985a,b). In the posterior midgut the wastes are compressed and surrounded by peritrophic membranes to form a fecal pellet. There is no evidence of digestive activity in the posterior midgut, which seems to serve mainly for reabsorbing water by transport cells (Becker & Peters, 1985a,b). Harvestmen have no Malpighian tubules associated with the digestive system, and concentrations of ions and water in the hemolymph are regulated mainly by coxal organs (Chapter 2). Although they have never been described, harvestmen may also have modifications in the terminal part of the rectum, at least for water reabsorption. This assumption is based on studies of Leiobunum vittatum, in which the anal fluid concentration becomes hyperosmotic in comparison with the hemolymph after dehydration (Riddle, 1985). This probably occurs for water reabsorption, suggesting the presence of an osmotic mechanism for water-loss reduction. Some invertebrates use the digestive system for water storage (Machin, 1981). Harvestmen have a characteristic enteric fluid used for releasing defensive substances (see details in Chapter 10). The enteric fluid is essentially composed of water, but its specific storage location in the digestive system is unknown (Gnaspini & Cavalheiro, 1998). Probably the enteric fluid is used for hemolymph-concentration maintenance in dehydrating conditions. The use of enteric fluid as a water source is likely since the frequency of enteric water elimination in 11 gonyleptid species decreased when the individuals became dehydrated (F. H. Santos, unpubl. data). The presence of a hypertonic anal fluid and a water-storage mechanism, which improves harvestman osmoregulation capacity, may have been an important adaptation for terrestrial life. According to histological analysis, there is a seasonal variation in spherites in the midgut gland of some harvestman species (Lipovsek et al., 2002). The spherites consist of an organic matrix composed of glycoproteins and proteoglycans (Chapter 2). The occurrence of an empty layer in the spherites after overwintering suggests that the organic matrix is used as an energy supply. Indeed, in a further study Lipovsek et al. (2004) found that lipids and glycogen are the two main sources of energy available in the midgut gland of Gyas annulatus and G. titanus (Sclerosomatidae) during overwintering. The rate of glycogen utilization seems to be species specific and may represent an adaptation to alpine environments (Novak et al., 2004). An energy reserve in midgut tissue, as well as behavioral changes during winter, which have been observed for species from temperate and tropical regions, suggests some kind of diapause (Lipovsek et al., 2002). However, this is speculative, and metabolic studies are still indispensable for further discussions.

Excretory water loss The physiology of nitrogen excretion in terrestrial arthropods is significantly influenced by water-conservation needs (Butt & Taylor, 1995). Excretory compounds

Ecophysiology

must be solid or highly concentrated. Most arachnids eliminate nitrogenous waste as water-insoluble guanine. No detailed studies exist on nitrogenous waste composition in Opiliones, but the elimination of nitrogen compounds via guanine excretion is sufficiently widespread in Arachnida (Haggag & Fouad, 1965; J. F. Anderson, 1966) to assume that harvestmen also use this mechanism. If this assumption is correct, water loss through nitrogenous excretion is probably minimal. Elimination of metabolic wastes in harvestmen is performed by a pair of coxal organs, although the morphology and physiology of these structures have never been well described (but see Chapter 2). In spiders and ticks the coxal organ is divided into a filtration membrane, a coxal tubule, a duct, and an opening situated near the coxa of a prosomal appendage (Butt & Taylor, 1995). The coxal fluid in spiders is produced by ultrafiltration when muscle contraction generates a negative pressure inside the filtration chamber. After primary filtration some compounds such as vital amino acids are reabsorbed in the coxal tubule (Kaufman & Phillips, 1982). These processes might also be applied to harvestmen. Additionally, harvestmen also have a group of cells involved in metabolic waste excretion and storage. These cells, called nephrocytes, are capable of taking waste products from the hemolymph and can be found scattered in the hemocoel or in groups in muscles and around the tracheal system and the heart (Zanger et al., 1991). In most arthropods the excretory system eliminates nitrogenous waste and also maintains osmotic and ionic balance (Butt & Taylor, 1995). In spiders the coxal fluid, produced only during feeding, is related to ion excretion (mainly Na+) taken from prey (Butt & Taylor, 1995). Another important ion (K+), also acquired during food ingestion, is eliminated by anal secretion. Therefore, it seems that feeding in some arachnids is not a water-replacing source because the ingestion of ions contained in the prey results in increases of osmotic and ionic hemolymph concentration. This may require ingestion of water to eliminate ions since spiders were observed to produce excretory fluids iso- or hyposmotic in relation to hemolymph. Therefore, replacement of body water by food occurs only when the osmotic pressure of the prey is lower than that of the predator (Butt & Taylor, 1995). When water is not available, the animal maintains high hemolymph osmotic pressure until water becomes available. On the basis of feeding preference studies, it is argued that food items consumed by harvestmen seem to be selected by prey size and its cuticular resistance, rather than factors such as water content (Santos & Gnaspini, 2002; see also Chapter 8). Water gain in harvestmen is achieved mainly by drinking, but another water source has been observed in some species of harvestmen that use their chelicerae to chew on the rim of leaves in order to obtain water (Acosta et al., 1995; Santos & Gnaspini, 2002). Harvestmen have a hemolymph with low osmotic concentration, and ions contained in food probably result in an increase in osmotic pressure during feeding similar to that observed in spiders. However, the composition of coxal fluid in harvestmen has never been examined, and the ion composition of the nitrogenous waste is unknown.

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Hemolymph and osmoregulation Apart from respiratory functions, the hemolymph is involved in osmoregulation and homeostasis of internal organs, transport of neuroendocrine factors, excretion, coagulating processes (Sutcliffe, 1963), and probably eversion of the ovipositor and penis (Chapter 2). Punzo (1983), using the hemolymph classification proposed by Sutcliffe (1963) and the phylogenetic position of Opiliones, predicted that harvestmen have a hemolymph composed mainly of sodium (Na+) and chloride (Cl−), with low concentrations of free amino acids and other organic compounds. However, it is important to stress that such statements are highly speculative, and detailed studies on the chemical composition of harvestman hemolymph are still necessary. One of the organic compounds dissolved in harvestman hemolymph is hemocyanin, a respiratory pigment. This substance transports oxygen to spaces not connected to tracheal branches, and its presence indicates that internal fluids are still involved in gas-exchange processes despite the existence of a well-developed tracheal system (Markl et al., 1986). The hemolymph has an osmotic pressure determined by its organic and inorganic components, presenting a remarkable role in osmoregulation capacity (Punzo, 1983). Burton (1984) compiled data on osmolarity of 13 species of spiders and 4 species of scorpions that showed mean values of 447 (range 320–536 mOsml/L) and 500 mOsml/L (range 426–536 mOsml/L), respectively. In contrast, harvestmen have a hemolymph with low osmotic concentration, ranging from 177 to 285 mOsml/L (Hebling-Beraldo & Mendes, 1980; Santos, 2003). In terrestrial environments the rate of water loss depends on difference between body-fluid concentration and the relative humidity of the air. Thus terrestrial organisms with diluted hemolymph are exposed to higher osmotic pressures to lose water than organisms with concentrated hemolymph in the same relative humidity, thus implying their greater osmoregulatory capability and/or a large tolerance to dehydration (Mantel, 1979). Several researchers have described an ability of a few harvestman species to maintain the hemolymph osmotic pressures stable during desiccation (e.g., HeblingBeraldo & Mendes, 1982; Riddle, 1985), including observations of several species in the family Gonyleptidae (Santos, 2003). The regulation of hemolymph concentration during dehydration is strong evidence of osmoregulatory mechanism activity. In many arthropods, including arachnids, the maintenance of hemolymph osmotic concentration is performed by solute tissue uptake, avoiding the increase in hemolymph concentration caused by water loss (Mantel, 1979). In addition, there is evidence of a low tolerance for decrease in the body-water contents in species of Phalangioidea (Riddle, 1985). Low tolerance to dehydration commonly implies the presence of efficient osmoregulatory mechanisms for body-water maintenance. Environmental hydric stress is a result of the difference between the osmotic concentration of hemolymph and the relative humidity of the air (Edney, 1982). Therefore, an increase in relative humidity generally results in a decrease of the environmental hydric stress. Species with hemolymph osmolarity similar to that observed in harvestmen, such as millipedes, are normally found in humid environments (Riddle,

Ecophysiology

1985). Despite the possible presence of an osmoregulatory control in harvestmen, their diluted hemolymph probably contributes to the common distribution related to wet environments presented by this group.

TEMPERATURE BALANCE A certain degree of thermal stress is inherent to life in most environments, and a wide variety of morphological, physiological, and behavioral mechanisms have evolved to sustain animal life (Randall et al., 1997). Ectothermic organisms are particularly dependent on environmental temperature because the physiological efficiency of a species is optimal at or near a specific body temperature. Thus species will select environmental temperatures that result in a specific body temperature (Buse et al., 2001). An increase in environmental temperature, apart from changes in the wax cuticular layer cited earlier, usually results an increase in metabolic rate (e.g., HeblingBeraldo & Mendes, 1980). However, an increase in metabolic rate in harvestmen does not result in an increase in tracheal spiracle opening or ventilatory movements since they have neither of these features. Thus metabolic rate variation produces no alteration in the water-loss rate. On the contrary, supercooling can enhance survival in extremely cold environments. Supercooling ability is weak in postembryonic stages of some species, but this ability is particularly evident in eggs. Bachmann and Schaefer (1983a) demonstrated that eggs of Phalangium opilio (Phalangiidae) are more tolerant of low temperatures than adults. Eggs were characterized by a mean supercooling point of −24.6°C, in contrast with −2.9°C presented by the adults. Supercooling ability was also demonstrated in different instars of the cosmetid Vonones sayi (Cokendolpher & Jones, 1991). Supercooling capacity is related to decrease of the freezing point of body fluids by the presence of high concentrations of antifreezing substances, such as glycerol (Randall et al., 1997). However, the presence and quantification of glycerol have never been sought in body fluids of Opiliones. This substance is widely established in arthropods, including arachnids, and it is probably present in harvestmen as well. Another means to withstand low temperatures is freezing tolerance, the ability to tolerate the formation of ice on body tissues and fluids. It is generally accepted that this freezing occurs extracellularly to prevent intracellular freezing (Leather et al., 1993). The extracellular fluids freeze more readily than the intracellular fluids because of the presence of substances that accelerate crystal ice formation. As ice forms in extracellular fluids, the unfrozen intracellular fluid becomes more concentrated with solutes. This process removes water from the cells and lowers the intracellular freezing point (Randall et al., 1997). However, freezing tolerance has never been observed in harvestmen. The species Vonones sayi showed no survival after body freezing (Cokendolpher & Jones, 1991).

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BEHAVIORAL RESPONSES Among arthropods several behavioral mechanisms are involved in avoiding or correcting physiological alterations in the internal environment. These behavioral mechanisms may act together or relieve physiological mechanisms. Preventive behaviors are generally related to survival under extreme and/or specific environmental conditions, such as adverse climatic seasons and periods with decreased food supply (Kirschner, 1987). Individuals of Goniosoma spelaeum (Gonyleptidae), for instance, travel deeper into caves to molt and lay eggs (Gnaspini, 1995). Movement to deeper zones may reduce dehydration during molting and may also provide a more protected site for oviposition. Moreover, the fact that most harvestmen are cryptozoic and are usually found in wet shelters such as crevices and caves and under wood or litter may already be considered an adaptation that provides appropriate conditions of humidity and heat (Cloudsley-Thompson, 1988). Although harvestman sensorial biology is a completely unexploited area (see Chapter 2), their capacity for perceiving different environmental stimuli and producing appropriate behavioral responses is widely known. Some studies have reported hygroreception in representatives of Eupnoi and Dyspnoi, which would be expected since humidity seems to be crucial for egg and nymph development, as well as for adults (see Chapters 12 and 13). Providing a humidity gradient inside closed chambers, laboratory studies have shown that all tested harvestman species prefer more humid conditions (Todd, 1949; Immel, 1954; Clingenpeel & Edgar, 1966; Edgar, 1971). Additionally, experiments using dry chambers to test harvestman resistance to dehydration demonstrated that they die in a few hours or days under conditions of low relative humidity (Table 14.1). These experiments have corroborated field observations that harvestmen prefer humid environments (Todd, 1949; Edgar, 1971; see Chapter 7 for more details). However, the sensorial structures involved in harvestman hygroreception are not known. Immel (1954) amputated the

Table 14.1 Responses of five North American harvestman species to desiccation in dry chambers Survival time (h) Species

Body-water loss (%)

Rate of body-water loss (%/h)

Males

Females

Males

Females

Males

Females

Leiobunum aldrichi

25.1

59.1

36.7

38.1

1.67

0.83

Leiobunum calcar

37.0

47.5

43.5

45.6

1.33

1.00

Leiobunum politum

18.4

38.6

40.0

44.6

2.76

1.36

Leiobunum vittatum

56.4

116.1

43.7

48.9

0.81

0.48

Phalangium opilio

75.6

120.0

48.3

57.6

0.72

0.52

Body-water loss was calculated at time of death. Modified from Edgar (1971).

Ecophysiology

pedipalps and walking-leg tarsi of the nemastomatid Paranemastoma quadripunctatum and found that tested harvestmen were able to choose places with relative humidity close to 100%, just like control individuals. Thermoreception was investigated using a protocol similar to that just described in which a temperature gradient was created inside closed chambers, maintaining constant humidity (Todd, 1949; Edgar, 1971). Again, representatives of both Eupnoi and Dyspnoi were studied, and the results obtained in the laboratory seem to be directly related to habitat use of the tested species under field conditions (see also Chapter 7). Species generally found in exposed habitats such as Phalangium opilio— which is mainly found in open fields—preferred high temperatures (> 27°C) and showed a wide range of temperature tolerance. Conversely, species generally found in shaded habitats, including Nemastoma lugubre (Nemastomatidae), Odiellus tridens, and Rilaena triangularis (both Phalangiidae), preferred low temperatures (< 12°C) and presented a narrow range of temperature tolerance (Todd, 1949; Edgar, 1971). No experiment has identified which sensorial structures are involved in thermoreception. Finally, photoreception has been tested in representatives of Eupnoi, Dyspnoi, and Laniatores, using light gradients or dark chambers in which the tested individuals were suddenly exposed to light (Pabst, 1953; Immel, 1954; Meyer-Rochow & Liddle, 1988, 2001). Once more, results obtained in the laboratory are consistent with field observations on the ecology of the species. Hence species from open habitats preferred higher light intensities than species living in shaded habitats (Clingenpeel & Edgar, 1966). Eyes are certainly the main sensory structure involved in photoreception, but no evidence of image formation exists (see Chapter 2). An interesting study on phototaxis was conducted with two cavernicolous species, Megalopsalis tumida (Monoscutidae) and Hendea myersi (Triaenonychidae), which feed almost exclusively on glowworms (Diptera). Both species have well-developed eyes, and behavioral tests in the laboratory showed positive phototaxis toward a dim artificial glowworm light and negative phototaxis towards ultraviolet light (MeyerRochow & Liddle, 1988, 2001; see also Chapter 8). Skototaxis has been experimentally demonstrated for trogulids, which are generally found among leaf litter and other dark microhabitats (Pabst, 1953). When exposed to intense light conditions in an arena containing some dark places, individuals of Anelasmocephalus cambridgei and Trogulus nepaeformis always retreat to these places.

Biological rhythms Biological rhythms are an example of a physiological-behavioral adaptation of the species to regular changes in the environment (Warburg & Polis, 1990). The temporal adjustment of the endogenous rhythm to the environment is possible because the biological clock is sensitive to external cycles, the so-called Zeitgebers (Aschoff, 1960). Zeitgebers are perceived by the sensorial system and transmitted to the “clock,” causing the synchronization of the rhythms (Saunders, 1982). For the great majority of terrestrial organisms, the light/dark cycle is the main Zeitgeber of

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the biological rhythms, and harvestmen seem to be no exception (CloudsleyThompson, 1978). The activity of most harvestman species begins with the approach of dusk and declines with the onset of dawn, apparently associated with the decrease in light intensity and perhaps the increase in humidity and the decrease in temperature (Todd, 1949; Cloudsley-Thompson, 1978; but see Bishop, 1950; Kästner, 1968). The first detailed study of the daily locomotor activity in harvestmen was conducted by Edgar and Yuan (1968), using Phalangium opilio and seven North American species of Leiobunum as model organisms. The individuals were tested under conditions of constant light (LL), constant dark (DD), and natural light/dark cycle (LD). The authors found a phase of low activity during the middle of the daylight period for all species tested under LD (Figure 14.2). Even under LL or DD there were well-defined phases of activity and rest (Figure 14.2), and the individuals maintained activity patterns similar to those shown under LD for several days, although with a smaller fluctuation in amplitude. These results clearly indicate the presence of an endogenous clock in the studied species. Additionally, Edgar and Yuan (1968) also showed that species that inhabit shadowed habitats, such as L. calcar (Figure 14.2A), presented smaller amplitude in the daily activity pattern than those species that live in places more exposed to sunlight and water loss, such as L. vittatum (Figure 14.2B). More recently, Hoenen and Gnaspini (1999) studied the activity rhythms of three gonyleptid species from Brazil: Iporangaia pustulosa and Iguapeia melanocephala (both Progonyleptoidellinae), which live on the vegetation, and Pachylospeleus strinatii (Pachylospeleinae), which is restricted to caves. Individuals of the three species were tested under continuous red light, which was equivalent to constant darkness for the harvestmen. Both epigean species presented a clear circadian rhythmicity and could be characterized as “diurnal” since their activity was clearly concentrated during the day. Indeed, species of the whole clade that includes the subfamilies Progonyleptoidellinae, Caelopyginae, and Sodreaninae (Pinto-da-Rocha, 2002) may be considered diurnal, which is an apomorphic trait within Gonyleptidae. The cavernicolous species also showed a marked circadian activity rhythm, with a bimodal pattern. The authors suggest that the scarcity of food in the cave habitat may have led the individuals to search more intensely and frequently for food, causing the plesiomorphic nocturnal expression of the activity to duplicate, resulting in bimodality. Although troglobites, which live in an environment without a light/dark cycle, generally lose temporal organization of their activities, some species maintain their circadian rhythm (e.g., Wilkens et al., 1990). The data for P. strinatii indicate an endogenous control underlying the expression of the activity, and, according to Hoenen and Gnaspini (1999), the circadian rhythmicity of the species may be considered a relictual feature. Only a few studies have investigated whether harvestman locomotor activity pattern is under endocrine control (Fowler & Gaines, 1984; see also Fowler & Goodnight, 1966, 1974). The authors related the production of the neurohormone 5-hydroxyptamine (serotonin) and the locomotion of Leiobunum aldrichi by manipulating the light regimes experimentally. Although the behavioral records were made with

Ecophysiology

A

B Figure 14.2. Daily percentage activity of the sclerosomatids (A) Leiobunum calcar and (B) Leiobunum vittatum in three light conditions: constant bright light (LL), constant dark (DD), and normal day-night photoperiod (LD). The total amount of movement of the caged individuals during a 24-hour period was divided in 3-hour intervals and expressed as a percentage for each species and light condition. Modified from Edgar and Yuan (1968).

several individuals at a time, the results are still useful as a characterization of the rhythmic pattern at the species level (see discussion in Packard & Stiverson, 1975). Both LL and DD altered the normal activity patterns, but did not change the pattern of serotonin secretion. Under LL an irregular level of activity was detected so that a rhythmic component could not be determined, and a complex activity pattern emerged under DD. The activity pattern in normal photoperiod (LD 14:10) showed two peaks of activity, one in the light phase and one in the dark phase. The rhythm of

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serotonin secretion, however, was clearly unimodal, with a peak in the middark phase. Therefore, the authors discarded the hypothesis that the light/dark cycle directs a peak of serotonin secretion, which in turn would initiate the activity of L. aldrichi. The most comprehensive field study on a harvestman biological rhythm was conducted with the gonyleptid Goniosoma spelaeum, which inhabits caves in southeastern Brazil (Gnaspini, 1996). Individuals were continuously followed from 4 p.m. to 10 p.m. and from 4 a.m. to 8 a.m. for three consecutive days each month for one year. During the day the harvestmen remained practically motionless inside the caves. In the afternoon some individuals began moving toward the entrance, where they concentrated before leaving the cave to forage exactly at or some time after dusk. The great majority of the individuals returned to the cave near dawn. On the basis of this pattern, the author suggested that the egress and ingress of individuals is determined by the epigean photoperiod (see also Machado et al., 2000). A subsequent study by Gnaspini et al. (2003) showed that older individuals of G. spelaeum (mainly subadults and adults) tend to rest deeper in the cave. They also assume an activity posture and start walking earlier, leave the cave later, return earlier, and assume a resting posture later when compared with individuals of earlier stages. In contrast, younger individuals tend to stay closer to the cave entrance, spending more time outside the cave. In fact, individuals of the three earlier stages leave the cave almost on a daily basis. Therefore, the available foraging time decreases with age so that the younger the individual, the more time it remains in the light, suggesting a higher tolerance for light in early nymphs. Additionally, exits from the cave in the winter (June/July) occur earlier than in the summer (December/January) because sunset occurs earlier, while returns occur later because sunrise occurs later (Figure 14.3). Therefore, the study presents evidence that the activity pattern of G. spelaeum is age dependent and that the light/dark cycle is the most important Zeitgeber. Seasonal changes in behavior can also be interpreted as preventive mechanisms (Kirschner, 1987). The synchrony between seasons and reproductive periods, allowing animals to survive through adverse climatic periods in a resistant egg, has been reported for harvestmen in desert areas (Cokendolpher et al., 1993) and cold winter areas (Clingenpeel & Edgar, 1966; Bachmann & Schaefer, 1983a). The formation of overwintering aggregations is one of the most typical seasonal behaviors of harvestmen (see Chapter 11). Microclimatic factors, such as relative humidity, temperature, and light conditions, may have a general influence on gregariousness in arthropods (Krause & Ruxton, 2002). For many insect groups, gregariousness is a behavioral strategy used primarily to reduce body-water loss since grouped individuals lose less water than solitary ones (Danks, 2002). There is no study demonstrating the physiological advantages of gregariousness in harvestmen as a means to prevent water loss (but see Chapter 11). However, it has been shown that the metabolism of aggregated individuals in the cosmetid Vonones ornatus is 12% lower than that of solitary individuals (J. F. Anderson, 1993), indicating that gregariousness in harvestmen may be a behavioral strategy to save energy.

Ecophysiology

Figure 14.3. Frequency (measured as number of days) of the return time in relation to sunrise for individuals of the cave-dwelling Goniosoma spelaeum (Gonyleptidae): (A) first– third nymphs and (B) adults. In the x-axis, 0.0 represents the time of sunrise, negative values represent returns before sunrise, and positive values, returns after sunrise. Modified from Gnaspini et al. (2003).

CONCLUDING REMARKS Although knowledge of harvestman ecophysiology remains incipient and fragmentary, the number of studies on physiological mechanisms and their relationship to the environment has increased in the last two decades. These studies update the results of older publications and provide new information. The information available so far suggests that abiotic characteristics, such as temperature and mainly humidity, are probably restrictive for Opiliones, limiting the range of inhabitable envi-

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ronments. Despite the capacity to maintain internal homeostasis, strong evidence indicates that many species of harvestmen are ineffective at avoiding water loss. Some morphological and physiological characteristics of the group, such as a lack of spiracular control, low osmotic hemolymph concentration, and increased mortality under dry conditions, may partially explain why most species of the order are found in damp and shaded areas. Species that occur in extreme habitats, such as deserts and subarctic or subantarctic areas, should be studied in order to search for possible physiological modifications mainly related to reduced water loss, supercooling abilities, and other physiological processes. Although significant amounts of behavioral data have been reported for harvestmen, sufficient knowledge of behaviors triggered by physiological requirements is still lacking. Studies on behavioral responses related to physiological mechanisms are much needed since most observations available in the literature are more generic descriptions of natural history and ecology of the species than proper studies on ecophysiology.

ACKNOWLEDGMENTS I wish to thank M. N. Ferreira, M. E. Bichuette (IBUSP), and three anonymous reviewers for their helpful comments on the manuscript.

CHAPTER

15

Methods and Techniques of Study

B

ecause of their enormous diversity and cosmopolitan distribution, it is not uncommon to find locally abundant and conspicuous populations of harvestmen. Compared with other groups with these characteristics, their biology has been grossly overlooked and thus is still poorly understood. In many chapters of this book, different authors have stressed that harvestmen are perfect subjects for ecological, behavioral, and evolutionary studies. In this chapter experts on different subject areas provide an overview of the methodology and techniques they use to study harvestman biology both in the field and in the laboratory.

ECOLOGICAL SAMPLING David J. Curtis In this section a brief outline of methods used in capturing harvestmen in the field is presented, followed by discussion of case studies illustrating some of the difficulties in obtaining adequate data for ecological interpretation. Harvestmen are strictly terrestrial, wandering arthropods, and the methods used for their capture are those of the general arachnologist or entomologist, with details given in many standard textbooks. The methods are fairly few and apparently simple, but interpretation of the data generated is not straightforward. A summary list of methods is given in Table 15.1.

Hand collecting Visual searching of the environment and capture of animals by hand may be quantified by using unit effort, generating counts per searcher per hour (Duffey, 489

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Table 15.1 Summary outline of field methods used in ecological studies of Opiliones

Method

Habitat

Captured specimens

Frequency of use

HAND COLLECTING Visual searching

Any

Living

Sweep net

Low vegetation

Living

Beating tray

Low to tall vegetation

Living

Ground surface

Dead

21%

CONTINUOUS TRAPPING Pitfall traps Arboreal traps

Trees and bushes

Dead

Sticky traps

Tree trunks

Dead

Photoeclectors

Ground or vegetation

Dead/Living

Corrugated sheets

Ground surface

Living

Corrugated-paper traps

Tree trunks

Living

88%

BEHAVIORAL TRAPS

5%

EXTRACTION METHODS Suction samplers

Vegetation and leaf litter

Dead/Living

Berlese funnels

Soil

Dead/Living

Tullgren funnels

Leaf litter

Dead/Living

Platform extractor

Litter and turf

Dead/Living

10%

The frequency of use is based on 58 published sources included in Chapter 7.

2004) or per area (Bragagnolo & Pinto-da-Rocha, 2003). The efficiency of this method will vary with the visual acuity of the observer and will depend on the degree of cryptic coloration of the harvestmen being sought. The method will be less efficient in complex environments. In some cases it may be augmented with the use of ultraviolet light to show up the individuals, as occurs with the large gonyleptid Pachyloidellus goliath (Acosta et al., 1995). Other direct sampling methods involve the use of a sweep net, which is passed horizontally through vegetation to knock out any animals present. This can be crudely quantified by using a standard number of sweeps along transects of known length. Vegetation may also be sampled using a beating tray, which is simply a sheet of white material placed on the ground beneath trees or shrubs, which are then shaken or beaten so as to displace animals living there. This method is difficult to quantify. Capture of the specimens is best achieved simply by knocking animals into a

Methods and Techniques of Study

specimen tube, possibly using a small paintbrush; alternatively, an aspirator could be used to suck up small animals. Forceps should be used with caution, if at all, because they can easily cause damage to specimens. These methods have the advantage of providing live specimens, but they can only record harvestmen present at the time of sampling, in contrast to the next two approaches, which have the advantage of catching animals continuously during the intervals between sample collections.

Continuous trapping Pitfall traps are by far the most commonly used technique for the capture of harvestmen (see Table 15.1). They have a very long history of use and in much European literature are termed Barber traps, referring to a very early description of the method by Barber (1931) and subsequently by Stammer (1949), who stressed the importance of the method and mentioned many examples. Basically, a pitfall trap is usually a cylindrical container open at one end, with typical dimensions about 8 cm deep and 5 cm in diameter, sunk into the ground so that its opening is flush with the soil surface. The trap thus captures mainly surface-active species, but species from higher vegetation levels are caught as they wander down to the ground. A commonly used preservative fluid is ethylene glycol, which also prevents freezing, with a few drops of detergent, such a teepol, to ensure that animals sink into the fluid. The trapping fluid is initially only about 2 cm deep, and four equidistant holes drilled (easier, using a hot needle, with plastic traps than with glass) in the trap wall about 1.5 cm from the top allow drainage of rainwater so that the traps continue to function in wet weather. This arrangement can trap effectively for up to a month and provide good specimens, depending on weather conditions. It becomes easier for specimens to escape if the inner wall of the trap becomes scratched or dirty, and capture rates can be substantially reduced, so care is needed to clean or renew traps as required. Trap contents can be transferred to containers for return to the laboratory and sorting in trays, the specimens then being preserved best in 70% ethanol for future examination and species determination. These traps depend on the activity of the animals that fall in and then are unable to climb out. They do not, therefore, give a direct measure of population density, but rather a combination of level of activity (dependent on animals’ behavior and environmental conditions) and the number of animals present, which is sometimes termed “active density.” Both the behavior of the harvestmen and trap efficiency may be influenced markedly by the trapping fluid used, and some examples are discussed later. Modified traps similar to pitfalls, attached to horizontal branches on which a barrier causes animals to fall into the trap, may be used to sample arboreal populations (Koponen et al., 1997). Sticky traps, similar to the bands used by horticulturists to protect fruit trees, may also be used to catch harvestmen in trees and shrubs, though separation of animals from the glue may be difficult (possibly requiring the use of solvent) and result in damaged specimens.

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Behavioral traps While the previous methods simply rely on general activity of harvestmen, there are some techniques that exploit the specific tendency of harvestmen to move into dark, cool, and moist refuges. Exploiting harvestmen’s photophobic behavior, photoeclectors (Schaefer, 1980a,b) have dark collecting tubes (with or without preservative fluid) into which the animals may fall through a suitably sized funnel. Corrugated cardboard, as used in packaging, can provide a refuge attractive to harvestmen. It can be wrapped around tree trunks and branches (Curtis & Morton, 1974) or placed as sheets of standard size on the ground (Cutler, 2001) and left for a sufficient period of time for harvestmen to “take up residence.”

Extraction methods It is possible to use vacuum samplers, such as the D-Vac, to “hoover up” invertebrates from their environment (Mommertz et al., 1996). Although some living specimens may be provided by this method, many specimens are killed and may be badly damaged in the extraction process. Alternatively, one may remove a portion of the “field” back to the laboratory and use standard techniques (Berlese funnels, Tullgren funnels, or Winkler extractors) to extract the harvestmen, from soil and litter. These rely on the behavior of the harvestmen and in a Tullgren funnel this is aided by gravity as the animals move down through the litter sample away from the light and heat source (e.g., a warm electric lightbulb). Even samples of turf may be extracted in this way in a platform extractor with a centrally placed heating element and peripheral troughs with preservative fluid to catch the animals as they move laterally down the temperature gradient. There are advantages and disadvantages to all of these sampling methods, including pitfall traps, which are by far the most frequently used, as shown in Table 15.1. The following topic considers some of these problems, with some concentration on pitfall-traps, and gives some indication of their productiveness in terms of numbers of individuals and species that may be caught.

Cautionary tales It has long been known that estimating absolute population densities of terrestrial arthropods is fraught with difficulty and probably impossible. Efficiency varies with different sampling methods and even between habitats and species for a single trapping technique such as pitfalls (Curtis, 1980, 1981). Some recent comparative work on the sampling of epigeal arthropods has been reported by Mommertz et al. (1996), contrasting D-Vac suction sampling with pitfall traps, and Lang (2000), making comparisons between different kinds of pitfalls. Even the concentration of preservative used in pitfall traps can influence capture rate (Pekár, 2002), especially with regard to the repellent effect of increasing concentrations of formalin for harvestmen. The time of collecting can also determine which species are caught, especially whether night or day (Green, 1999) and even early or late night (Mestre & Pinto-da-Rocha, 2004).

Methods and Techniques of Study

So there are variations of trapping efficiency within a single trap type (pitfall traps), which are used for surface-active ground-living species. Even worse, other types of traps are needed to sample other habitats: tree branches, with the equivalent of an arboreal pitfall trap; tree trunks, by means of corrugated-paper traps, and surface-active fauna with an equivalent method; and bushes (beating trays, with or without knock-down gases) or field vegetation (sweep net), as well as hand collecting in all kinds of habitats. To make population comparisons between data from diverse trapping methods would be statistically foolish because it is impossible to distinguish the effect of trap efficiency from habitat- or species-caused variations. However, it is perhaps acceptable to pool such data to derive a more thorough description of species abundance in mixed or complex habitats (e.g., Curtis, 1973, 1978a,b; Schaefer, 1980a,b, 1986; Bachmann & Schaefer, 1983b; Hippa et al., 1984; Corey & Stout, 1990; Gruber, 1993; Koponen, 1995; Komposch, 1996, 1997a,b, 2000a). When relying on “active density” as our measure of effective abundance, as in the use of pitfall (or any other) traps that depend on the animals’ behavior to enter traps and then provide dead specimens, we need to equalize our sampling effort over the areas (or time periods) we wish to compare. This will not provide absolute population densities, but an indication of the numbers caught may be seen in data from oak woodland in western Scotland (site 1 of Curtis, 1978a). Here a grid of 20 pitfall traps within an area of just 1 m2 could catch, over a seven-day period in 1972, as many as 236 harvestmen, of which 215 belonged to the surface-active species Nemastoma bimaculatum (Nemastomatidae). Over a 12-month period the catch was dominated by this species, with 4,164 individuals out of a total of 6,403 harvestmen in these traps, which did not use any preservative/killing fluid. Another abundant species was Oligolophus tridens (Phalangiidae), with a total of 833 (maximum weekly count of 67). The absence of preservative effectively provides the traps with invertebrate carrion that acts as bait for N. bimaculatum; their capture rate is much lower in traps with formalin/teepol trapping fluid. At the same site over 12 months in 1976/1977 (Curtis, 1980) eight similar pitfall traps caught 306 N. bimaculatum, compared with only 73 in traps with teepol trapping fluid and 151 in traps with teepol/formalin; the aversive odor of the fluid possibly explains the reduced catch. This contrasts with just the opposite pattern in equivalent catches of O. tridens of 114, 279, and 299. Both species showed reduced catches of 123 and 18, respectively, when lids were used to keep the traps dry—the animals climb out again or simply run over the top. It is interesting to compare these results with those of Pedrocchi-Renault (1985) in the Spanish Pyrenees. He reported the greater efficiency of traps with water plus detergent (218 Opiliones caught, versus 57 in control traps) and the attractant effect of meat extract in the traps (269), but the highest catches (321) of harvestmen in traps containing wine. There are obvious differences in efficiency between the different sampling methods, and there will be variations between habitats and also between species. There must be adequate coverage of microhabitats in a sampled area, so regular (grid, transects) or random placements of traps may be appropriate only in homogeneous environments; in heterogeneous areas stratified random sampling will be better (traps

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placed randomly with numbers proportional to the relative area/complexity of different vegetation patches). The uncertain trap efficiency creates difficulties in interpretation of data because the precise relationship of trapped numbers to actual population numbers is never exactly known, although it can be estimated. The use of nested-cross arrays of pitfall traps may improve such density estimates (Perner & Schueler, 2004). If we can catch live animals, mark them, and then release them, we could use the proportion of recaptures as a way of calculating the full population size from our samples (Begon, 1979). These capture-mark-recapture techniques are difficult for smaller species living interstitially in soil and leaf litter, but they have been usefully applied to some harvestman populations, especially of large-bodied species of the family Gonyleptidae, using spots of enamel paint to color-code individual harvestmen (e.g., Gnaspini, 1996; Pinto-da-Rocha, 1996a,b; Mestre & Pinto-da-Rocha, 2004). Even without capture/recapture, for community studies pitfall traps are the best because they maximize the number of species recorded (Curtis, 1980, and other studies). In comparing communities, the problem of observed species richness varying with sample size can be overcome by mathematically estimating the species richness for a standard sample size, thus permitting valid comparison by calculating how many species one would find in the same number of individuals taken from each community (e.g., Heck et al., 1975; Toti et al., 2000). Species accumulation curves, plotting species richness (S) versus sample size (N), can help judge the adequacy of sampling. The species/sample size curves from more diverse communities will show a steep rise of S with N or a gentler rise to a high asymptote, whereas a low-diversity community will quickly reach a low asymptote. This approach features in Colwell’s (1994–2000) EstimateS software. For good, concise treatments, see Ugland et al. (2003) and Melo et al. (2003). As well as being predators, harvestmen are also prey and are often adapted to this by their cryptic coloration and shy habits. Even a member of a striking species such as Megabunus diadema (Phalangiidae), with its second legs as long as 35 mm, is almost invisible as it rests immobile against its usual background of lichen-covered rocks or tree trunks. Only when it moves does the animal reveal its presence to the observer. This applies when using visual searching for any species. Furthermore, all the other forms of trapping for harvestmen depend on active movement of the animals for their capture, and so, in effect, we almost depend on the animals’ cooperation for effective ecological sampling.

METHODS FOR TAXONOMIC STUDY Luis E. Acosta, Abel Pérez González and Ana Lúcia Tourinho Whereas most contributions on harvestmen deal with taxonomic issues, relatively few studies include explicit references to techniques. Different methodological strategies are required at various stages of the taxonomist’s work, depending on each specimen’s size, morphology, and habitat. This section presents an overview of

Methods and Techniques of Study

methods and criteria most frequently used by harvestman taxonomists. No standardization is aimed at here, but rather some guidelines and practical tips are given with our hope that they will be useful for the beginner.

Collecting for taxonomic purposes Most collecting methods mentioned in the previous section are also used in taxonomic studies. However, taxonomists will normally catch any specimen, regardless of quantification concerns, in a diverse set of habitats, using an array of methods in order to obtain a specific group of harvestmen or the whole community. Nocturnal species that hide during the day can be searched for by turning over leaves, stones, fallen bark, and logs and then carefully inspecting them. Many harvestmen are cryptic and remain motionless for a few minutes after their shelter is removed; they are often difficult to see until they start walking. Specimens can be collected with forceps or by hand, but minute, delicate forms are best collected with a moist brush or an aspirator. Long-legged Eupnoi, which may flee quickly, should be gently taken with the collector’s fingers, catching most or all legs together to prevent appendotomy. Sweeping or beating the foliage of trees or bushes provides good samples of specimens that are difficult to find by simply inspecting the vegetation, such as gagrellines, cosmetids, and zalmoxids. Beating usually produces less specimen damage than sweeping. Nocturnal harvestmen can be found active at night by using a white-light lantern, but seldom with ultraviolet light (Acosta, 1983). When collecting at night or in shady spots (such as caves or dense forests), it is advisable to use a head lantern, leaving the hands free for manipulation of specimens. Most night-active species are found motionless on leaves and logs, clinging on rocks or cliffs, or moving among blades of grass. Some nocturnal harvestmen can be found by baiting trails with jelly, nectars, or jam. A myriad of soil- and litter-dwelling harvestmen (Cyphophthalmi, triaenonychids, caddids, trogulids, phalangodids, zalmoxids and the like) are too small to be detected with the naked eye or using the methods previously described. To find them, the litter should be sieved through a 2–5 mm mesh, whereupon the sample can then be processed in different ways. A practical method is just to spread a handful of sifted leaf litter on a white tray or a white vinyl cloth and wait until the minute specimens start moving. Alternatively, several extracting devices for soil and litter arthropods are used to discover the smallest species (see details in the previous section). Two of these are Berlese funnels and Winkler bags, the latter of which are designed to be quite portable. Although primarily designed for ecological studies, these methods may represent the only source of the smallest harvestmen for taxonomic use. Pitfall trapping, though extensively used for ecological sampling of ground harvestmen, is not the best choice for taxonomists, mostly because the preservatives commonly used for pitfall traps (e.g., ethylene glycol or picric acid solution) may degrade the specimens by making them translucent and/or brittle. Ethanol is preferable, but the rate of evaporation should be taken into account.

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Fixation and preservation The traditional method of sacrificing and preserving specimens—simply dropping them into 70%–80% ethanol—gives good results for most species but has the disadvantage that DNA degrades rapidly (see the following section). In fieldwork it is advisable to employ 80% ethanol because this concentration will dilute through the water content of large specimens. Still, ethanol alone as the fixative for large gonyleptids or soft-bodied harvestmen may result in bad preservation of internal tissues, affecting the appearance of the integument. To avoid this effect, a formula containing formalin (12 parts), 99% ethanol (30 parts), glacial acetic acid (2 parts) and distilled water (56 parts) has given good results. Specimens should remain for up to 1.5–2 hours in this solution and then be transferred to 80% ethanol for final fixation and preservation (more time in the first fixative will harden the articulations too much). However, one should be careful when handling formalin, which is highly toxic and should not be mixed outside a flux hood. For male gonyleptids, one should gently move the IV coxa-trochanter joint when transferring to the 80% ethanol; otherwise this joint may become “locked” with the femur too difficult to move away from the body for study, sometimes resulting in a broken piece. Legs of long-legged Phalangioidea should be bundled together dorsally to save space and avoid leg detachment in the vial. Ethanol 70%–80% also serves as the preservation liquid for all harvestmen groups. As with other arachnids, harvestmen are usually kept in glass or plastic vials together with their labels. Each vial should have a hermetic closure or, preferably, be sealed by a cotton tuft and immersed in the preservation fluid, together with other tubes, in a larger jar.

Observation and description External morphology is studied with a stereomicroscope, a compound microscope, or a scanning electron microscope (SEM). Preparation for the different microscopic techniques can be specific for the instruments used. For the most common stereomicroscope examination, the specimens must be completely immersed in ethanol (of the same concentration as that used for preservation) in a Petri dish of adequate depth. Subtle ornamentation or scutal furrows are sometimes difficult to visualize while immersed, so it is often necessary to gently dry the surface with absorbing paper and observe as quickly as possible to avoid desiccation. A contrasting background (e.g., white, black, or blue, depending on the species) can enable better observation. It is advisable to illustrate all relevant features of the external morphology with digital images or scientific drawings. In general, the body should be illustrated in dorsal (Figure 15.1), ventral, and lateral views, although some of these views are not strictly necessary for different groups. Although the favorite illustration for Phalangida may be the dorsal view, for Cyphophthalmi, most informative characters are seen in the sternal region. If needed, appendages can be removed for better observation and drawing, and they should be kept in a small vial within the specimen’s tube to avoid losses. Sand on the bottom of the Petri dish will help keep the specimens in a

Methods and Techniques of Study

Figure 15.1. Selected examples of customary measurements of body parts in Opiliones. Ocularium of the gonyleptids Pachyloidellus (a) and Pygophalangodus (b), posterior view. The positioning is correct when both eyes and the apophysis tip are in focus; h, height; w, width. (c) Body general measurements of the triaenonychid Ceratomontia centralis (dorsal view): SL, scutum length; BL, total body length. Topology on the appendages: p, prolateral; r, retrolateral; m, medial (= mesal); 1, lateral (= ectal). (d) Right femur IV of Pachyloidellus fulvigranulatus (Gonyleptidae), prolateral (ectal) view. Lf, femur length.

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desired position. The dish can also be half filled with bee wax, paraffin, ethylene vinyl acetate, silicone, or polyurethane (the rest with alcohol) so as to position the specimen with the aid of entomological pins. Those who use digital cameras have the option of improving the depth of field with computer programs such as Combine-Z (Cokendolpher, 2004) or Automontage. Descriptions should be based on all available specimens, rather than on a single one (e.g., holotype), and the range of variable features (coloration and morphology) should be provided, too. Descriptions should include body features (carapace, scutum, free tergites, and ventral details), all appendages, and, in most cases, genital morphology. Reference to color may be subject to individual variations or the action of the fixatives, but color patterns (dots or stripes) often provide valuable characters, always with consideration of individual variability (e.g., Gruber & Martens, 1968). Authors should refer to live coloration, as well as coloration upon preservation, whenever possible. Special attention should be paid to sexually dimorphic features, which may range from slight to remarkable differences (see Chapter 4). As a general rule, and especially important for highly dimorphic groups, it is advisable not to describe new taxa based on females alone, in order to prevent those taxa from becoming dubious or unrecognizable. Regulations for naming species, as detailed in the International Commission of Zoological Nomenclature (ICZN), are to be strictly followed.

Tegumentary ornamentations The integument provides a rich variety of taxonomic features. Large cuticular projections such as spines, tubercles, or apophyses are the most conspicuous, but smaller ones (granules, denticles, warts, ridges, alveolae, setae), sometimes combined with the former, are of interest, too. In general, when large processes are present, authors refer to such body parts as being “armed”; parts that are either smooth, granulose, or rugose are deemed to be “unarmed” (Roewer, 1923). However, some of these structures frequently intergraduate in size so that objective limits between the two conditions are sometimes difficult to establish. Whether a body part is said to be “armed” or “unarmed” often depends more on the usage in a taxon than objective criteria across all harvestmen. Some authors, for instance, speak of the “armature” when referring to humble denticles on otherwise almost unarmed harvestmen (e.g., Tourinho-Davis & Kury, 2003 in Gagrellinae). This lack of precision may be especially misleading in Gonyleptidae, where the armature has played a major role in generic and specific diagnoses. Surface sculpturing is useful in systematics, but terminology is far from being universal (Murphree, 1988). According to Shear and Gruber (1983) and Murphree (1988), macrosculpture includes processes from 0.01 to 0.1 mm in size (anvil-shaped teeth, warts, tubercles, and spines), while microsculpture comprises denticles, granulation, and microtrichia below 0.01 mm. In addition, the integument bears a great variety of setae or sensillae, which are fairly easy to accurately identify. Elements that form the microsculpture give the cuticular surface a definite appearance (finely or coarsely granulose, rugose). Density of granulation is frequently mentioned in

Methods and Techniques of Study

species descriptions, although usually without precise definitions. As a possible solution, at least in the genus Ceratomontia (Triaenonychidae), Maury and Roig Alsina (1985) have published SEM micrographs to illustrate specific differences of granulation that are difficult to describe in words. In some taxa, such as the Neotropical gagrellines, the dorsal integument usually bears noticeable depressions (alveolae) instead of protuberances (Ringuelet, 1959). Additionally, in Cyphophthalmi there may be several glandular openings on the cuticle of the males, especially in the tergal anal region or in the anterior opisthosomal sternal region. The term “armature” normally refers to larger cuticular projections, either on the body or the appendages (Figures 15.1a–c). It includes the following basic categories: (1) apophyses, which are tall projections, either sharp or blunt tipped, emerging from the integument without a sharp limit, (2) spines, which are acute processes inserted in a tegumentary socket (therefore somewhat movable), and (3) tubercles, which are short projections without a sharp limit from the cuticle, roughly as wide as high, either round or acute. Again, differences of each type may not be as clear-cut as desirable, and some intergraduation toward smaller structures (granules, denticles, setae) also exists (Acosta, 1989). Roewer (1923) and Ringuelet (1959) used the term “spine” to refer to any process that is long and slender. However, as just stated, tall processes emerging from the integument without a limit (Figure 15.1) should be referred to as apophyses—“spinelike apophyses” if acute (Acosta, 1989)—restricting “spine” to projections articulated in a socket (e.g., those on pedipalps of Laniatores). Definitions are also obscured because of intraspecific variation, in many cases seemingly influenced by allometric variation; that is larger specimens bear even larger tubercles or apophyses, for instance (cf. Acosta, 2002a). Thus an armature consisting of “short apophyses” may take the appearance of “acute tubercles” in smaller individuals of the same species. Moreover, between “small tubercles” and “large grains” a smooth continuum often exists, so ultimately rigid definitions may prove useless (Acosta, 1989). The point is to discover the overall armature pattern (i.e., the assemblage of apophyses or tubercles) and to recognize the intraspecific variation of each single element, so illustrating such structures is often helpful.

Topological terms in appendages Different terminologies have been employed to describe the position of tegumentary processes on pedipalps and legs. The terms “internal” and “external,” used to mean “toward” or “opposite” the median line, should be avoided and restricted to structures inside and outside the integument (Roewer, 1923). More widespread, “medial” (= mesal, mesial) and “lateral” (= ectal) have proved to be adequate for chelicerae and pedipalps (Figure 15.1), but not as suitable for legs. These terms do not help reflect the homomerous nature of a structure, theoretically present on all leg pairs: the same feature, being mesal on leg I (oriented forward), would be called lateral on the backward-pointing leg IV. Furthermore, leg III in many taxa is roughly perpendicular to the body axis, rendering at least arbitrary the decision about which side is medial or lateral. The best alternative is to use “prolateral” and “retrolateral”

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(Figure 15.1), which can be easily combined with other position descriptors (e.g., prodorsal, retroventral, proapical). Note that mesal/ectal are not equivalent but an alternative to prolateral/retrolateral.

Mensuration Measurements have not played a central role in harvestman taxonomy, varying from a brief mention of the body size up to detailed tables containing measurements of different body parts, especially appendages. Explicit statements or drawings showing the way measurements were taken are strongly recommended, especially in comprehensive studies. It is advisable to state both the aspect (dorsal, ventral, lateral) and the landmarks used in each measure; otherwise results may differ, especially in curved segments (Figure 15.1d). Nonetheless, such statements are quite rare in the literature (but see Martens, 1969a; Cokendolpher, 1981c; Hunt, 1990a; Gruber, 1998). This situation contrasts with that in other groups: in scorpions, for instance, around 30 standard measurements have been proposed, each with precise landmarks (Sissom et al., 1990). No comparable standardization exists in the harvestman literature, with the exception of the modern papers on Cyphophthalmi. To reflect the animal’s size, the measurement most frequently referred to is the body length (Figure 15.1c). It is taken from the anterior carapace border up to the posterior edge of the body (often, but not always, represented by the dorsal anal operculum). Prosomal projections such as the supracheliceral lamellae or frontal apophyses, or the ocularium when projected anteriorly (e.g., Triaenonychidae, Ceratolasmatidae), should not be included in the total body length, but opisthosomal processes might be taken into account whenever both measurements (with/without process) are given. It is also suggested that the body-length range (maximal and minimal values) be provided, as well as the sample average. In Cyphophthalmi and Oncopodidae the first eight opisthosomal tergites coalesce with the carapace in a single scutum completum, whose length equals the body length. However, in most Laniatores and some Dyspnoi the dorsal scutum (scutum magnum) leaves the three last opisthosomal tergites free; since the length of the rear portion may depend on the nutritional condition or the presence of eggs in females, the dorsal scutum length, measuring rigid parts alone, is preferred over the total body length as a reference of the size. Dorsal scutum length and body length are independent measurements (Figure 15.1), but are sometimes confused. There are yet other harvestmen in which size varies with the abdominal expansion: either all opisthosomal sclerites are free (scutum laminatum, in some Ischyropsalididae, Sabaconidae, and Nipponopsalididae), or they partially fuse into a plate independent of the carapace (scutum parvum, in many Ischyropsalididae, Phalangioidea, and Sabaconidae, among others), or they are tenuous and no longer recognizable (scutum tenue, in many softbodied Eupnoi); in all these cases the body length is the only option to measure the overall size. Body width and distance between ozopore tips are also commonly provided for Cyphophthalmi. Detailed measurements are currently included in taxonomic descriptions,

Methods and Techniques of Study

though they are normally restricted to relevant specimens, mostly the holotype and its opposite gender. Such information accomplishes Recommendation 73C of the ICZN to publish all relevant data on the holotype. Taxonomically much more interesting is to provide measurements (and basic statistics) of a sample (Gnaspini, 1999). When few morphometric data are given, they are normally embodied within the text; to show measurements of all body parts (including separate segments of appendages), authors employ a gridlike table or arrange data as a list. The total length of each leg is obtained by adding the lengths of all segments (excluding the coxa, whose dimensions are related to the body). The total length of each pedipalp includes the apical claw, when present. In Phalangioidea total lengths of legs are difficult to measure, and just the lengths of all femora and tibiae are normally provided (but see Cokendolpher, 1981c). Morphometric differences have occasionally been used to support species identities. Measurements of selected features, or ratios, often add good diagnostic characters, but variability should always be taken into account (Ringuelet, 1953; Gnaspini, 1999). Graphs showing the average, maximal, and minimal values (sometimes also the standard error of the sample mean) have proved to be useful for pairwise comparisons (e.g., McGhee, 1977; Acosta, 1999; Gnaspini, 1999). Comparisons can be made on the actual measurements (such as dorsal scutum or femur length) or using relative values (e.g., total appendage length/dorsal scutum length). A relative measurement (femur length/body length, named femoral formula) was applied to some Eupnoi, and clinal variation was thereby detected (Ringuelet, 1953). Two selected measurements or ratios can be combined and plotted in a bidimensional graph, where conspecific individuals will group together if the measurements are good discriminants (e.g., Martens & Chemini, 1988; Acosta, 1993).

Meristics Discontinuous numerical descriptors, such as the number of tarsal segments or pseudoarticular nodules on legs, have been used in different notations in the literature; these notations are roughly similar, but they can vary considerably and are not always intuitive. Whichever notation is employed, authors should stress its meaning in the methods section of the paper. Variability of these features is best displayed in tables presenting frequency distributions. The number of tarsal segments of adults (“tarsal formula,” cf. Forster, 1954) is referred to for most groups, except for Phalangioidea (which have multisegmented tarsi) and Cyphophthalmi (which have uni- or bisegmented tarsi). Tarsomeres are most easily counted from a lateral view; incomplete tarsomere subdivisions, which are sometimes seen, should be recognized as an anomalous condition. The tarsal formula can be displayed as X1:X2:X3:X4, where Xi is the number of tarsal segments in each leg pair (e.g., 6:8:7:7). Intraspecific variation in a pair is expressed as a range (e.g., 6:8–10:7:7). For single individuals with asymmetrical counts in a pair, a slash can be used to separate the numbers on the left and the right tarsus, and a question mark to indicate missing data (anomalous or broken tarsus) (e.g., 6/5:7:6/?). Disti-

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tarsi I and II can have taxonomic value, and their counts are parenthesized, for example, 6(3):11(3):6:6, where (3) indicates distitarsomeres I–II, and 6 the whole number of tarsomeres on leg I. Classic authors (e.g., Roewer, 1923) misused the tarsal formula in taxonomy, using single differences to erect a separate genus (Acosta, 1999). When a count was higher than six, some authors used to state “more than six tarsomeres” (Roewer, 1923; Soares & Soares, 1954) or just “n” (Ringuelet, 1959), but the actual number should have been provided. The number of pseudoarticular nodules on leg femora is a variable character currently considered in the systematics of some Phalangioidea. Femora of nemastomatids bear similarly a pseudoarticular appearance, not by nodules but by paler cuticular constrictions instead. Pseudoarticular counts have been used in species or genus diagnoses, though their value is not universally accepted. Femoral nodule counts have been referred to as “femoral formula” (Tourinho-Davis, 2004b), but this should not be confused with the relative femur length. Because the number of nodules often shows asymmetry (Suzuki, 1949), a notation such as 1/0:4/5:1/1:2/3, with a slash separating the right and left counts for single specimens, is recommended (Ringuelet, 1953); for some authors, however, slashes separate leg pairs (e.g., Tourinho-Davis, 2003). If variation is found, a dash should separate the end values of the range, and the frequencies should be mentioned (e.g., Gruber & Martens, 1968). In Laniatores with armed pedipalps, the number, relative size, and sequence of ventrolateral spines or rigid setae on tibia and tarsus provide valuable features. In a simple notation (Kury & Maury, 1998) large spines are designated as “I” and small ones (less than half the size of the largest on the same row) as “i” (e.g., “tibia ectal of pedipalp, IiiI, mesal iiIi,” and so on).

Preparation of male and female genitalia The study of genital morphology has proved its systematic usefulness in almost all taxa of Opiliones. Although its importance was already demonstrated by Hansen and Sørensen (1904) and Silhavy (1938), most early authors ignored this source of characters. As a result, the genital morphology of a large number of nominal taxa is still unknown. Since a few decades ago, genital morphology has become a useful source of diagnostic characters for species or higher levels, as well as an important source of evidence for phylogenetic relationships (Martens, 1976, 1986; Martens et al., 1981). Almost all modern taxonomic studies of Laniatores, Eupnoi, and Dyspnoi include the description or illustrations of at least the male genitalia. It is worth noticing here, though, that the taxonomic value of genitalia is not equivalent in all groups. Some specimens occasionally die with the genitalia everted, but in most preserved materials penis and ovipositor have to be dissected out. The procedure should be done carefully, especially if types or small specimens are involved. It is best to make two slightly divergent incisions with a thin scalpel, posteriorly from the lateral angles of the genital opening; the integument can then be lifted, and the tubular

Methods and Techniques of Study

sheath containing the genitalia can be gently picked with thin-tipped forceps (Silhavy, 1969b). The insertions of the sheath to the angles of the operculum, when present, need also to be sectioned to extract the piece. Small or flat-bodied harvestmen (e.g., Trogulidae) should best be cut along the opisthosomal pleura, enabling the lifting of the entire abdominal plate (Silhavy, 1969b; Martens, 1978b). Cyphophthalmi, which are small and have thick cuticles, are dissected with a thin surgical scalpel. An alternative method for small-bodied Laniatores consists of lifting the anal operculum and introducing fine blunt forceps to “push” the genitalia and causing them to evert. The genital piece should be freed from its membranous covers (immersed in ethanol), using forceps and minute needles. A basal portion of the membranous sheath, if left unremoved, can facilitate the manipulation and rotation of the piece while it is examined under the microscope. Although normally discarded, the sheath penis has occasionally shown taxonomic usefulness (Gruber, 1998). The penis or ovipositor should be kept in a microvial stored within the specimen’s vial. Observations of genitalia are customarily carried out under an ordinary light or a compound microscope, using Nomarski optics if possible, with the genitalia immersed in a clearing agent in a nonpermanent excavated slide. Mounting the genitalia in a permanent preparation is not advisable, since this procedure limits the observation possibilities to one angle. For very small objects, a thicker medium may be needed to anchor the structure from any angle; K-Y Brand Jelly is suitable for this, and it is soluble in water and slowly soluble in 80% ethanol. For details of the components of the media and stains cited in the following sections, the reader is referred to classical laboratory handbooks (Barbosa, 1974; Krantz, 1975).

Clearing. In most cases the genital piece needs first to be cleared. There is no universal clearing agent, and the choice of one depends on the thickness, pigmentation, or degree of sclerotization and on the personal experience of the researcher. Glycerine is most widely used (Martens, 1978b) for most groups. The piece is simply transferred from the ethanol into a few drops of glycerol in the excavated slide and is allowed to clear for several minutes. After observation it can be directly restored to its microvial without further treatment. Carbol-xylol (one part of crystalline phenol with three to four parts of xylol) and clove oil are alternative clearing substances (Silhavy, 1969b; Martens, 1978b). Ovipositors in Phalangioidea and Dyspnoi, where the number and shape of the receptacula seminis are relevant, and penes of Laniatores have been examined using clove oil, creosote, or lactophenol (Cokendolpher, 1985b; Kury & Pinto-da-Rocha, 2002) and lactic acid (Gruber, 1998). The use of clove oil requires dehydration of the genitalia in a gradient of ethanol concentrations, a process that has to be reversed in order to store the piece after observation. While the genitalia are immersed in clove oil, they are very brittle and easily broken. Objects can be placed directly into lactophenol from ethanol, but should always be rinsed with ethanol before returning them to the microvial. Creosote is certainly a potent clearing agent, but it has a persistent, unpleasant smell; more important, it may be carcinogenic, and it causes eye and skin irritation after prolonged exposure. Clove oil and carbol-xylol may pose the same serious health

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risks. Thick muscle layers of penes sometimes should be removed with potassium hydroxide or sodium sulfide; ovipositors with densely pigmented cuticles can be treated with chlordioxyd (Martens, 1978b; Silhavy, 1969b). Muñoz-Cuevas (1969) proposed other methods, including the Marc André fluid, but when compared with the good results yielded by glycerol alone, most alternative procedures seem somewhat complicated and only justified for heavily sclerotized pieces.

Staining. When genital structures are tenuous, instead of being cleared, they need to be slightly stained for observation. In Triaenonychidae, for example, penes bear delicate membranous expansions that can be emphasized with Gage’s acid fuchsin for 12 hours, followed by 24 hours in distilled water to remove any excess dye (Maury, 1993). Observation and illustration. The piece is examined while immersed in the clearing agent in the slide, preferably with a cover slip. The cover slip may limit the ability to manipulate the piece, but it avoids image deformations and also prevents the accidental contact of solutions with the microscope lens. To facilitate observations, the penis or ovipositor should be placed perpendicular to the long side of the slide; this helps get the small piece to rotate through a gentle displacement of the coverglass (Hillyard & Sankey, 1989). A few cotton threads in the same fluid can be employed to prevent the displacement or drifting of the piece in the microscope field once a suitable position has been found. This also may help keep it in lateral position, especially when genitalia are not cylindrical (e.g., Eupnoi), and thus not as easy to rotate with the cover slip. Extremely small genitalia will not rotate in depressed slides and should be mounted with the aid of two fragments of cover slip placed on a nonexcavated slide, separated at about 1 cm. Two droplets of glycerol and the piece are placed in the space between the cover-slip pieces, and then they are all covered with another cover slip, which can be displaced to make the piece rotate (Figure 15.2). Relevant structures of the penis concentrate on the distal end, so penis illustrations are normally limited to that portion. A drawing of the entire piece should be given when the trunk bears either internal features, such as muscles (Insidiatores,

Figure 15.2. Mounting of small genitalia on a noncavity slide. The cover slip is placed over two additional small pieces of cover slip, the genitalia in between, immersed in glycerol. The cover slip can be gently displaced to both sides (thick arrow), causing the genital piece to rotate (circular arrows).

Methods and Techniques of Study

Eupnoi, Dyspnoi), or external expansions, such as “wings” or “sockets” (Eupnoi, Nemastomatidae), or the overall shape has taxonomic meaning (e.g., Eupnoi, Fissiphalliidae, Stygnommatidae, Kimulidae, Escadabiidae). Transverse sections of the penis shaft help understand the spatial relationships when this portion is not round or bears expansions or sockets (Martens, 1986). Penes with complex distal parts that are hidden or bent at rest (e.g., Phalangodidae, Oncopodidae, Assamiidae, Biantidae, Fissiphalliidae, Podoctidae) need to be placed first in hot lactic acid and then distilled water to expand those parts for observation (Schwendinger & Martens, 2002b); when put back in ethanol, the everted parts return to their resting position. Briggs (1974a) also recommends soaking in 10% KOH just long enough to expand the velum, then neutralizing with acetic acid. Detailed illustrations of both the expanded and unexpanded conditions should be shown (Martens, 1988).

Scanning electron microscopy (SEM). Although results obtained by light microscopy are good enough for standard taxonomic purposes, the use of SEM is recommended to uncover minute external details of the genitalia or get a better understanding of their structure in three dimensions. Unlike light microscopy, the piece prepared for conventional SEM cannot be restored to the original condition, and this method is indeed strongly inadvisable for type or unique material. The piece is prepared following the same general procedure as with any chitinous structure: (1) cleaning, (2) dehydration, (3) mounting, (4) metal coating, and (5) observation. Genital pieces can be observed under SEM without prior cleaning; however, since it is impossible to evaluate if the piece is dirty for SEM, and bad results may arise only after the whole procedure is completed, it is highly advisable not to skip this step in a standard SEM protocol. The piece is cleaned in a solution of distilled water and commercial detergent (3:1) in an ultrasound cleaner for around three minutes; one to two further minutes in distilled water alone in the ultrasound serve to eliminate the detergent. Thereafter the piece is dehydrated by transferring it to a series of increasing concentrations of ethanol up to 100%. Finally, for six hours in each fluid, the piece is immersed in two successive ethanol-xylol solutions (3:1, 1:1) and then in plain xylol. The final desiccation can be done by simply letting the xylol evaporate at room temperature (Pinto-da-Rocha, 1997). Hard pieces can be dried after cleaning by just immersing them in acetone of xylol for some minutes, followed by air drying (Pinto-da-Rocha, 2002). This air-dry procedure may result in the genital piece being distorted, especially if membranous parts are involved. That problem is completely avoided by using critical-point drying (recommended here as the standard procedure), which starts with the piece being dehydrated in 100% ethanol or acetone. Variable-pressure or high-pressure SEMs do not require the samples to be dried or coated with metal or carbon, but this equipment is still not widely available. With any SEM procedure, the piece is usually fixed perpendicular to the observation stub (directly glued on it or on a thin wire) to allow most views in equipment that rotates 90°; with lower rotation ability, the piece should be glued obliquely with the dorsal side upward. Once fixed to the stub, the piece must be coated with gold or palladium before examination.

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METHODS FOR MOLECULAR STUDIES IN SYSTEMATICS Sarah L. Boyer and Gonzalo Giribet Molecular phylogenetics has proved to be a powerful tool for research in systematics because sequencing of DNA can very quickly yield large quantities of data for phylogenetic analysis. In addition, sequence data are easily shared among researchers via online databases. Molecular phylogenetics can be applied to higherlevel problems, such as the phylogeny of chelicerate orders (Wheeler & Hayashi, 1998) and relationships among suborders/superfamilies (Giribet et al., 1999, 2002; Shultz & Regier, 2001), as well as investigations into the evolutionary relationships of closely related species of Opiliones (Boyer et al., 2005). Given the usefulness of molecular data for furthering the study of harvestman systematics and evolution, several technical considerations for the preservation of tissues and the analysis of sequence data are provided in this section. We follow a chronological order, beginning with considerations before collecting the specimens, continuing through preservation preferences, and concluding with a succinct description of the standard molecular methodology. All these topics are briefly summarized in order to give an overview appropriate for a book as broad as the one in the hands of the reader. Methods and protocols are the focus of several other books and extensive book chapters, and by no means can we attempt to substitute this brief chapter for those important texts. For that reason, we cite some relevant comprehensive references to guide the reader.

Collecting permits for molecular work Collecting fauna must be done in the most responsible manner, taking into account all legal issues. Many countries do not require specific collecting or exporting permits for collecting in nonprotected areas. Others have extensive regulation about what can be collected and even more restrictive laws about what can be exported to other countries; thus field collectors who want to sequence DNA from their specimens may face additional special permitting issues. Because genetic materials and data are used by many profitable biotechnology corporations, genetic resources are not considered to be a commodity that should be made available to any researcher without restriction, especially in developing countries. Therefore, researchers interested in working with molecular data should always look into this issue specifically before applying for permits in the country of interest and allow significant extra time (6–12 months) for the processing of collecting and export permits for specimens intended for molecular work. A more detailed account of unique permitting issues can be found in Prendini et al. (2001). It is particularly important to be able to trace all sequence data back to original voucher specimens, so all field collections to be used for molecular work should be meticulously labeled, documented, and stored in an organized and accessible fashion.

Methods and Techniques of Study

Tissue preservation Tissues have to be preserved in a particular way to allow extraction of DNA. Optimal storage conditions include 95%–100% ethanol, freezing, or RNAlater (useful for workers who are planning to extract RNA in addition to DNA). Tissues that have been preserved in 70% ethanol are generally not useful for DNA extraction, but 95% ethanol is inexpensive and can be packed in small vials so that animals collected in the field can be immediately preserved. This mode of preservation will cause a loss of appendages in many Phalangida, but animals that have been preserved in this manner can still be mounted for SEM. Cyphophthalmi, on the contrary, remain well preserved, with articulations still flexible. Freezing of tissues should be performed as soon as possible after collecting and as quickly as possible by dropping directly into liquid nitrogen or covering with dry ice. Alternatively, for short field trips it is useful to carry specimens alive to the laboratory and freeze them at −80°C. Labeling of frozen specimens is especially important since it becomes difficult to dig for frozen specimens in cold, dark freezers (Prendini et al., 2001). The mode of transportation of specimens after collection should also be considered when choosing a preservation technique. Airlines regulate the transport of alcohol, so researchers should always obtain relevant guidelines from their airline before planning to bring ethanol onto a plane. Alternative preservation media, such as RNAlater, are innocuous, and therefore there are no regulations that prevent their transportation. However, RNAlater is expensive, and animals kept in RNAlater need to be refrigerated soon after collecting, within a few days. For more details on processing specimens collected in RNAlater, see the manufacturer’s specifications (www.ambion.com/techlib/resources/RNAlater/).

Long-term storage of tissues DNA will remain stable in samples stored in 95%–100% ethanol at ambient temperature, but long-term storage of samples should be under fireproof conditions. The best safeguard against long-term DNA degradation is to store ethanol samples at − 20°C or colder. In our laboratory we keep all preserved specimens at −80°C. Samples should always be stored in well-sealed vials (Teflon lined), preferably glass, to avoid leakage of organic compounds from plastics and evaporation. For frozen tissues, optimal long-term storage conditions minimize variations in temperature, light, and volume. Most frozen-tissue repositories maintain samples at −130°C to −150°C, although they will remain indefinitely stable at −70°C to −80°C (Prendini et al., 2001). For long-term storage and distribution of frozen-tissue samples that go beyond the lives of single investigators, one should consider frozen-tissue collections in staffed museums. A state-of-the-art cryocollection is the Ambrose Monell Cryo Collection at the American Museum of Natural History (research.amnh.org/amcc/).

DNA extraction Contamination can be a serious problem for molecular systematists. Before extracting DNA from a specimen, the researcher should be sure to remove any con-

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taminating organisms (e.g., mites) from the surface of the subject animal. It is not necessary to destroy an entire specimen to successfully extract its DNA, an important consideration for researchers working on rare species. One leg, if fresh or properly preserved, provides a sufficient amount of tissue for extraction, even in the tiniest individuals, and this leg does not need to be crushed for use in manufacturerprepared extraction kits such as the DNeasy Tissue Kit from Qiagen. In robust animals, such as Cyphophthalmi, the leg may be incubated in lysis buffer overnight and remain intact, such that it can be removed from the buffer and returned to storage in ethanol (Boyer et al., 2005). Detailed protocols for DNA extraction of Opiliones and other organisms can be found in many reference sources (e.g., Hillis et al., 1996; Nishiguchi et al., 2002).

Polymerase chain reaction (PCR) To sequence a particular region of an organism’s genomic DNA, it is necessary to produce a vast number of copies of the region. This is accomplished by the polymerase chain reaction, commonly known as PCR, which takes place in thermal cyclers that repeatedly heat and cool reaction tubes containing genomic DNA, a polymerase enzyme, primers, dNTPs (a mix of single nucleotides), and buffer. There are three steps in PCR: the first step, denaturation, takes place at 95°C, melting the two strands of the genomic DNA’s double helix apart from one another. In the second step, annealing, the specific primers bind to the single-stranded DNA, generally between 40°C and 50°C. Primers are short oligonucleotides whose sequences reverse-complement a portion of the sequence of interest. In the third and final step of PCR, extension is performed at 72°C. In this step a polymerase originally isolated from the hot-spring bacterium Thermus aquaticus (Taq for short) adds nucleotides to construct a second strand of DNA, starting at each primer. This cycle, from denaturation through extension, is repeated nearly 30 times. With each cycle, the number of copies of the gene of interest grows exponentially, resulting in DNA in sufficient concentration for sequencing. Troubleshooting of PCR may involve designing new primers, modifying the reaction buffers, and adjusting the annealing temperature, and many of these conditions may also depend on the physical PCR machine available to the researcher. Older PCR machines used large Eppendorf tubes of 0.5 mL, but the new generation of PCR machines uses 200 ␮L tubes or smaller, with thinner walls that allow faster protocols and better amplifications. Palumbi (1996) provides a detailed chapter on PCR that will be useful to anyone using the approach for the first time. In general, when designing a PCR strategy for a new project, the best approach is to start with primers and protocols that have been used successfully in taxa closely related to the group of interest. Some projects will require cloning of PCR products or the use of reverse transcriptase (RT) PCR. Before the sequence reaction one must prepare the PCR product that is going to be sequenced by removing the excess of dNTPs, as well as the Taq polymerase, salts, and excess primers. Although there are numerous ways of cleaning up the PCR reactions, two main methods are used: sephadex-based cleaning protocols and enzy-

Methods and Techniques of Study

matic protocols. Sephadex columns for cleaning reactions are available commercially or can be easily made in the laboratory at a greatly reduced cost. The hydrolytic enzyme method is also inexpensive, and enzymes are commercially available in a reagent mixture such as Exo-SAP-IT from USB.

Sequencing Sequencing DNA involves two steps: the sequencing reaction and the reading of the sequence. The sequencing reaction is performed in a thermal cycler and is very similar to a PCR reaction, except that PCR-amplified product (rather than genomic DNA) is used as the template for the reaction, only one primer is used in each reaction tube, and a small proportion of the dNTPs are labeled with fluorescent molecules. When the dye-labeled larger dNTPs are incorporated into the sequence reaction, they terminate elongation of the DNA strand, as described in Sanger et al. (1977). As a result, the product of the sequencing reaction is a mix of strands of every length from one base (in addition to the primer) to the entire length of the target sequence, each of which is labeled with a fluorescent G, A, T, or C at one end. In modern automated sequencing machines, sequences are “read” as the product of the sequence reaction is run by a laser beam that excites the fluorescentlabeled nucleotide attached to the terminal end of the sequence. The product of the sequence reaction is run through a polymer; some sequencing machines use slab acrylamide gels, while others use tiny amounts of polymer that move through capillary tubes. Molecules travel through the polymer at different speeds according to their size, with short molecules traveling faster than long molecules. Therefore, the first molecule to traverse the fluorescent beam will correspond to the first base pair of the target sequence, and the last molecule to come through will correspond to the last base pair. Each nucleotide type (G, A, T, or C) emits a different frequency when excited in the machine, and these frequencies are read by the machine as the molecules pass through, resulting in a read of the entire PCR product. Researchers who do not have in-lab access to a sequencer may use centralized sequencing facilities at their home institution or private biotechnology companies that provide sequencing services. Currently many companies provide sequencing services at low cost.

Sequence databases Sequence data are easily uploaded to databases such as GenBank (www.ncbi .nlm.nih.gov/Genbank/index.html), EMBL (www.ebi.ac.uk/embl/), and DDBJ (www.ddbj.nig.ac.jp/). Sequences can be submitted one at a time; alternatively, the free downloadable program Sequin permits submission of sets of multiple sequences simultaneously. Sequences are usually released to the public domain after the relevant study has been published. Once they are made available, submitted sequences are linked to an accession number and can be downloaded by other researchers free of charge. Online sequence databases have taxonomy browsers that facilitate searches for se-

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quence data from specific groups. Another very useful service is the BLAST search engine, which allows researchers to paste in a single sequence or submit batches of sequences and retrieve the database sequences that are the closest match, an excellent method for screening new sequences for contamination. Alignment programs, protein databases, and molecular structure databases are just a few of the other services provided.

Phylogenetic analysis of molecular data Anyone who follows the systematics literature is well aware that methods of phylogenetic analysis are controversial and the subject of a great deal of unnecessary professional acrimony. One of the most important issues in the analysis of molecular data is alignment. Sequences from the same gene in two different animals may have different lengths, so a determination about where to insert gaps in the shorter sequence must be made, indicating the position of the insertion-deletion (indel) event responsible for the length difference. The most common approach to this problem is to use an automated alignment program such as CLUSTAL (Jeanmougin et al., 1998) or Malign (Wheeler & Gladstein, 1994). Static pre-fixed alignments are used by programs such as PAUP*4.0 (Swofford, 2000), TNT (Goloboff et al., 2003), and MrBayes (Huelsenbeck & Ronquist, 2001). The program POY (Wheeler et al., 2002) allows the researcher to input unaligned sequences and to optimize the alignment of the data and the tree topology simultaneously. Although some researchers still construct trees using distance-based methods, most use methods based on optimality criteria. Parsimony and likelihood are the two most widely used optimality criteria and are available in all commonly used software packages for phylogenetics. Further considerations include weighting schemes, substitution models, and measures of support and stability. Useful introductory books on phylogenetics include Biological Systematics (Schuh, 2000) and Inferring Phylogenies (Felsenstein, 2004). The reader is invited to enter the vast literature on theoretical and practical issues in systematics and to develop opinions about methodological issues. The application of molecular data to questions in Opiliones systematics has been fruitful to date, but is still in its infancy. There is no doubt that the number of Opiliones researchers using molecular data in phylogenetic analysis will increase in the near future. Although DNA sequences may be expensive to generate and may be challenging to analyze, they provide systematists with a powerful source of character data easily shared among researchers across the globe and ready to be combined with all the morphological wealth of knowledge on harvestman morphology accumulated during the last two centuries.

Methods and Techniques of Study

METHODS OF CHROMOSOME PREPARATION Nobuo Tsurusaki Traditionally, chromosomes of harvestmen were studied by paraffin sectioning or by a squashing technique, as in other animals. However, application of the airdrying technique developed in the 1960s (initially for the observation of human chromosomes) to harvestmen improved efficiency and resolution of chromosome observation dramatically. There are several modifications of the air-drying method. Of these, two techniques for observation of harvestman chromosomes are described here: one with the cell-dissociation procedure using lactic acid (modified from Takagi & Oshimura, 1973) and the other using 30% acetic acid for the same purpose (modified from Dietrich & Mulder, 1981). The two procedures have different merits and defects. The dissociation process with 30% acetic acid requires fewer skills than the one with lactic acid. However, the procedure results in some loss of chromosomal spreads during the replacements of solutions in Eppendorf tubes. It is detrimental especially when the material is scarce and expected yield of chromosome spreads is limited. On the other hand, the dissociation process with lactic acid requires more advanced skills, though the equipment needed is simpler. Furthermore, lactic acid, which is a viscous liquid, spoils chromosome slides if an excessive amount of the liquid is used.

Source of material Testes of adult males or juvenile males at later stages are the most frequently used material for studies on chromosomes in harvestmen, since they enable observation of chromosomes in both mitosis and meiosis. In most groups of insects, chromosome observation using fully matured adults is difficult because of earlier termination of spermatogenesis. In harvestmen, however, both mitotic metaphases and meiosis can be observed in adult males over a rather long period (especially in Eupnoi). It is likely that this reproductive trait relates to the protogenous propensity and repeated copulation of females in those members of harvestmen. The testis is a U-shaped and semitranslucent tubelike organ that a fine white thread of the trachea accompanies along the axis of the testis (see Chapter 2). Ovaries of penultimate or antepenultimate female juveniles and of adult females can also be used if the ovaries are not yet fully matured, although the yield of cells with countable chromosome spreads is extremely small. The ovary is a U-shaped aciniform tube and translucent before eggs start to accumulate yolk (see Chapter 2). Embryos in a developing stage with limb buds are also useful material for chromosome observation, though actual sex of the material cannot be determined in advance in this case.

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Air-drying technique with lactic acid treatment for cell dissociation Solutions 1. Hypotonic solution (1% sodium citrate) = 2.5 g Na citrate (Na3C6H5O7•2H2O) + 247.5 mL of distilled water. This solution can be stored about one month in a refrigerator. Instead of 1% Na citrate, 0.075 M KCL can also be used as a hypotonic solution. 2. 0.1% colchicine solution = 50 mg colchicine + 50 mL of distilled water. This solution can be stored in a refrigerator in a brown-colored glass bottle for up to three months. 3. Hypotonic solution (1% Na citrate) with colchicine = 19 mL of hypotonic solution (solution 1) + 1 mL of 0.1% colchicine solution (solution 2). Use of colchicine solution is recommended to obtain better results, though dispensable. 4. Fixative = Carnoy’s solution (three volumes of absolute methanol [99%] and one volume of glacial acetic acid [99%]). This solution cannot be preserved. Mix it just before the preparation. About 4 mL of this solution (3 mL of absolute methanol + 1 mL of glacial acetic acid) is needed for fixation of a testis (or ovary) from one individual. 5. 3:1 Glacial acetic acid / 50% lactic acid (= glacial acetic acid : lactic acid : distilled water = 6:1:1) = 3 mL of acetic acid + 0.5 mL of lactic acid + 0.5 mL of distilled water. Only a small amount is sufficient.

• • • • • • • •

• • •

Equipment Forceps. Dissecting needle with hooked tip. Two Pasteur pipettes for fixative and lactic acid or acetic acid solution, respectively. 2 mL graduated pipettes for methanol, acetic acid, hypotonic solution, and lactic acid. Thick depressed slide (three depressions). 10 mL glass vials with screw cap. Two 25 mL glass bottles with ground-in stopper, respectively for fixative and hypotonic solution with colchicine. Hematocrit glass capillaries. Two capillaries are available by pulling apart a hematocrit-capillary tube (75 mm/75 ␮L) after heating the middle part of the tube with an alcohol burner. Rubber suction tube for hematocrit capillary. Precleaned slide. Black plastic sheet. Placing the sheet under the depressed slide makes it easier to locate the almost transparent testis or ovary against the dark background.

Method (Figure 15.3). The procedure consists of three stages: hypotonic treatment for maceration of cells (steps 1–2), fixation (step 3), and spreading (steps 4–9).

Methods and Techniques of Study

(4) Transfer the fixed material together with fixative

n ~ 6:1:i=acetic ac1d/laotic acid! distilled water

1 or 2dro s

blow (7) Spreading

dissociated cells

ltJ/ lJ

fixative (acetic methanol)

5-10 drops

(9) Air dry (more than one day)

----..7

,---1~:....=.:..;--./,---.-.-::·~;

(10) Staining

Giemsa solution diluted in S0rensen's buffer

(11) Rinse for about one second in running tap water

(12) Drain and dry in the air, then stock as a permanent preparation

Figure 15.3. Steps of chromosome preparation with dissociation of cells using lactic acid. See text for detailed explanation.

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1. Dissect out required organs (testes or ovaries) in hypotonic solution (1% sodium citrate or 0.075 M KCL) and place in a depression of the depressed slide using a dissecting needle and forceps under a stereomicroscope (Figure 15.3, step 1). 2. Transfer organs to hypotonic solution on another depression of the slide using a dissecting needle with a hooked tip and leave for 10–15 min at room temperature (Figure 15.3, step 2). 3. Transfer the material to freshly prepared fixative (absolute acetic methanol, i.e., absolute methanol : glacial acetic acid = 3:1) in a vial and leave for more than 5 min (Figure 15.3, step 3). The material can be stored at this stage in a freezer (−20°C) for more than one year. 4. Transfer the fixed material together with a small amount of fixative onto another depressed slide using a pipette (Figure 15.3, step 4). 5. Place the slide under a dissecting microscope and add one or two drops of 3:1 glacial acetic acid / 50% lactic acid (= glacial acetic acid : lactic acid : distilled water = 6:1:1). This treatment dissociates the tissues into single cells and clumps of cells (Figure 15.3, step 5). 6. When the material becomes somewhat transparent and intercellular connection is sufficiently loose, transfer the material (with a small drop of the cell suspension if clumps of cells were already protruded out) onto a freshly wiped precleaned slide (washed in detergent solution, rinsed in distilled water, and stored in absolute ethanol) using a capillary tube with a rubber suction tube (Figure 15.3, steps 6 and 7). Attention should be paid not to transfer a large amount of the fixative-contained lactic acid onto the slide. The lactic acid treatment has both positive and negative effects for results. This treatment facilitates dissociation of cells and increases the available number of chromosomal spreads. However, high viscosity of the lactic acid hinders microscope observation if chromosomal spreads were covered with a layer of lactic acid. 7. Immediately (i.e., before the material dries) add two to three drops of freshly prepared fixative (3:1, absolute methanol / glacial acetic acid) on the material, scatter the cells by mincing and patting with a dissecting needle, and add a few more drops of fixative at appropriate intervals (Figure 15.3, step 8). If there are backrushes at both ends of the slide, remove surplus fixative using a slip of absorbent paper (filter paper). 8. Allow the slide to dry completely in the air at room temperature (if possible, more than 12 h) (Figure 15.3, step 9). Slides can be preserved for at least one to two years, though earlier examination (within half a year) is safer.

Air-dry method with dissociation of cells by using 30% acetic acid Solutions 1. Hypotonic solution (1% Na citrate). 2. 0.1% colchicine solution.

Methods and Techniques of Study

3. Hypotonic solution (1% Na citrate) with colchicine (= mixture of solutions 1 and 2). 4. Fixative = Carnoy’s solution (three volumes of absolute methanol [99%] and one volume of glacial acetic acid [99%]). 5. 30% acetic acid.

Equipment • • • • • • • • • • •

Forceps. Dissecting needle with hooked tip. Two Pasteur pipettes for fixative and lactic acid or acetic acid solution, respectively. Three 2 mL graduated pipettes for methanol, acetic acid, and hypotonic solution. Three 25 mL glass bottles with ground-in stoppers for fixative, hypotonic solution with colchicine, and 30% acetic acid solution. Precleaned slide. Black plastic sheet. Microcentrifuge. 1.5 mL microtubes (Eppendorf tubes). Micropipettes. Test-tube mixer (shaker).

Method. The procedure consists of three processes: (1) hypotonic treatment, (2) fixation, and (3) chromosome spreading. Of these, hypotonic treatment and fixation are the same as described in the methods for the air-drying dissociation using lactic acid already mentioned. Steps in chromosome spreading are as follows: 4. Transfer the fixed material into a microtube together with fixative using a Pasteur pipette. 5. Replace fixative with 200 ␮L of 30% acetic acid. 6. Mix for 2–10 sec using the shaker. This makes component tissue cells dissociate, which results in a suspension (dissociated cells + 30% acetic acid). 7. Centrifuge microtubes at about 5,000 rpm for 5 min and then discard the supernatant 30% acetic acid. 8. Pour 200 ␮L of fixative into the microtube and shake to resuspend (dissociated cells + fixative). 9. Centrifuge microtubes at about 5,000 rpm for 5 min and then discard the supernatant fixative. 10. Add 50 ␮L of fixative into the microtube and shake to resuspend. 11. Pipette 20 ␮L of the suspension onto a precleaned microslide glass by using a micropipette. Allow the slide to air-dry. A second slide can be prepared from an additional 20 ␮L of the solution, with the remaining 10 ␮L being discarded. Staining and observation of chromosome slides. Chromosome slides prepared by the air-drying method need Giemsa staining before microscopic observation (Figure 15.3). Steps are as follows:

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• Stain slide with freshly prepared Giemsa solution (Merck solution diluted 1:24 in tap water or M/15 Sørensen’s pH 6.8 buffer) in a Coplin glass staining jar for 10 min (Figure 15.3, step 10). • Rinse for about 1 sec (two washing strokes) in running tap water and allow to dry (Figure 15.3, steps 11 and 12). Use of M/15 Sørensen’s pH 6.8 buffer (KH2PO4 4.54 g + Na2HPO4 4.75 g + 1 L distilled water, stored in a refrigerator) is recommended when pH of tap water deviates much from 6.8. This solution easily nourishes bacteria if it becomes contaminated. Therefore, it should be replaced after 30 days. Staining of the slides with Giemsa solution diluted by the contaminated buffer extremely disturbs precise chromosome counts. Be careful not to allow invasion of bacteria into the bottle. No cover slips need to be mounted, though use of “no cover lens (×100)” is highly recommended in observation at high magnification (×1000). Immersion oil can be applied directly to stained slides without cover slips. Use of a green filter gives the highest resolution in microscope observation.

PRESERVATION OF PARASITES AND PATHOGENS James C. Cokendolpher When one discovers a parasite or pathogen of Opiliones, the first step is to resist the urge to prematurely preserve the evidence. Most parasites and pathogens cannot be identified to species from certain life stages. The goal is to properly rear or preserve the organism in a state so that it can later be identified or described as new. The life cycles of many of the parasites are complex and do not all occur on or within Opiliones (see Chapter 9). Whenever you discover a parasite/pathogen, it is recommended that you try to obtain several examples so that material from each life stage can be preserved. In addition, in the cases of some pathogens it will be necessary to reinfect the host species to verify that it is a pathogen and not a saprophytic species that invaded the Opiliones corpse after death. Whenever possible, try to keep the parasite/pathogen alive until you have consulted an arthropod parasitologist. Some methods are general and are listed in the following discussion. In all cases you should record the location on or within the host from which the parasite was obtained (be very specific as to the structure or tissue and placement on or within the structure), note how and where the host was found (some pathogens cause unusual behavior before death), and preserve the host Opiliones for later identification. In addition to the information presented here, there is much useful information in the publication by Poinar and Thomas (1984).

Viruses, rickettsias, and bacteria It is unlikely that a diseased Opiliones infected with a virus, rickettsia, or bacterium could be recognized in the field by anyone not trained in arthropod pathology.

Methods and Techniques of Study

If one of these pathogens is suspected, the dead or dying harvestman should be frozen dry (do not add water or other solution to the vial) as quickly as possible and saved for a microbiological examination.

Fungi If numerous specimens (fungus-covered hosts) are found in a specific locality, some specimens with the least fungal growth should go into alcohol for eventual identification of the host Opiliones. Additional specimens can be used for fungal identification, either grown on mycological media (see Poinar & Thomas, 1984) or preserved for shipment to a specialist. If fresh, the entire host and fungus should be gently but quickly dried. Place the specimen in a small envelope made of folded paper (or paper box; not aluminum foil or wax paper) and place in a sealed container with a desiccant (Drierite: CaSO4 or a similar compound). Do not allow the fungi to come in contact with the drying agent, and keep samples from each host separate. Fresh specimens should never be placed in moist, airtight containers; this will promote the growth of saprophytes and will almost certainly cause the destruction of any pathogen. Label each sample with specific locality, date, collector’s name, host’s name if known, description of habitat, and position of host (e.g., “host hanging onto upper side of willow leaf, near small stream”). If only one specimen is available, have the mycologist preserve at least half of the dried body (right or left side, preferably with the genitalia) and some appendages for identification by a specialist.

Protozoa Most of the protozoans (excluding the larger Apicomplexa) are minute and will only be discovered when examining internal tissues or hemolymph. Some of these will have to be examined alive, and others will be prepared for light and SEM examination. See Poinar and Thomas (1984) for some details on preparations. All known Apicomplexa parasites of Opiliones are septate eugregarines and as such have several features in common. Both sexual and asexual stages occur (gametogony and sporogony), but merogony is absent. Gametocytes are passed in the feces; no intermediate host or vector is needed. The mode of infection is ingestion of oocysts. The trophozoites attach to the lining of the gut and divide to form merozoites and gamonts. Because most species are believed to attach to intestinal epithelial cells, gregarines in Opiliones probably are not pathogenic. Gregarines can be discovered by cutting open the abdomen of living or recently killed harvestmen. The trophozoites and sporonts are large and often can be seen without a microscope (see Chapter 9). Rearing gregarines from harvestmen is a simple matter. Living, infected harvestmen are placed in a clean, clear glass or plastic container (even a plastic sac will work). A small amount of food (fruit or moist grain cereal) and water should be provided. Arthropods should not be provided as food because they may contain their own species of gregarines and other parasites. After a day or two the feces should be removed from the bottom/sides of the container and examined with a dissecting microscope. This is best accomplished by placing the

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feces in a few drops of water or Ringer’s solution on a microscopic slide. Gregarine gametocytes are quite large (about 300–500 ␮m), round, and generally creamy white in color (see Chapter 9). When the gametocytes are located, they should be transferred to a second clean slide with several drops of water or Ringer’s solution. Because the feces also contain numerous fungal spores (especially yeasts), it is best to isolate the gametocytes to avoid them being consumed by fungi. The slides should be stored on top of moist filter paper or paper toweling in a sealed container at room temperature. The gametocytes will produce thousands of oocysts (5–10 ␮m long) in about 5 to 10 days. Dissection of living harvestmen in Ringer’s solution is required to observe the trophozoites and sporonts. Maturing trophozoites are often large and can be detected without the use of a microscope. Trophozoites and sporonts will be located in the intestinal region (most of abdomen). In order to identify gregarines, you will need examples of all life stages, especially the sporonts and gametocytes. Simply placing the sporonts or trophozoites in 70%–80% ethanol will generally result in specimens that cannot be identified beyond that of “gregarine.” Specimens for light microscopic study should be killed and fixed in Carnoy’s acetic alcohol (1:3, glacial acetic acid: absolute ethanol), and those for scanning electron microscope (SEM) examination should be killed and fixed in 0.1% glutaraldehyde. Other methods regarding staining and coating for microscopic study can be found in Cokendolpher (1991).

Cestoda and Trematoda Immature stages (larvae and cysticercoids) are known from Opiliones (see Chapter 9). In these cases the harvestman is a substitute for an intermediate host. Such occurrences are very rare and will only be discovered when specifically looking for parasites within Opiliones.

Nematoda Proper identification of harvestman-parasitic nematodes requires adult material that is properly preserved. The chapter on nematodes in the laboratory guide by Poinar and Thomas (1984) is highly recommended. All species thus far discovered of Rhabditida nematodes carry a single species of symbiotic bacteria in the alimentary tract of the third-stage juvenile. The infective-stage nematodes occur on soil and have the ability to locate and enter arthropod hosts. To reach the hemolymph of the host, the nematodes enter via a natural opening and then penetrate through the gut or tracheal walls. Once inside the host, the nematode releases its associated bacteria, which kill the host within 48 hours. The nematodes mature into males and females inside the arthropod, and the females release eggs within the cadaver. Mermithid nematodes generally occur singularly within a host. One of the major problems in mermithid identifications is the lack of adult material. Postparasitic juveniles that have emerged from parasitized harvestmen must be reared to adulthood to be identified. The Opiliones should be held captive in a plastic or glass container until the emergence of the immature mermithid. The parasite can then be trans-

Methods and Techniques of Study

ferred to a small amount of water in a container with a layer of sand on the bottom. Within a month it should shed both cuticles in a single molt to reach adulthood. The water should be changed daily so bacteria and fungi will not accumulate and kill the mermithid. Adult nematodes are killed by placing them in water heated to 50°C– 60°C. After death they are fixed in 3% formalin or preferably 70% ethanol. Placing the specimens directly into alcohol without heat killing will damage or destroy the specimen for taxonomic studies.

Insects Like most parasites, parasitoid insects should be reared to adulthood before killing and preserving. It is tempting to preserve larvae and pupae when they are first noticed, but they should be left alone to mature. Harvestmen noted with insect parasitoids should be placed in a clean, sealed container with food and water. Harvestmen should be isolated; otherwise, other harvestmen may feed upon the parasitoid when it emerges. As with all parasite collections, the host remains should be preserved (70%–80% ethanol) and labeled in such a manner that they can be matched later with the parasite. The parasitoid should be labeled with the data covered under methods for fungal collections, as well as date of host capture, date of parasitoid pupation, date of emergence, and approximate temperature at which parasitoid was reared. Depending on the size of the parasitoid, it can be pinned, pointed, or preserved in 70%–80% ethanol.

Mites Larval erythraeid and trombidiid mites can be easily removed from harvestmen preserved in alcohol or freshly collected specimens by gently teasing the mites’ mouthparts (gnathosoma) out of the host tissue with a fine needle (or insect pin). A small brush can then be used to transfer the mite(s) into 70%–75 % ethanol. From dead/dried harvestmen the mite should be softened by applying alcohol (or water) directly to the mite(s) and surrounding tissue with a small brush. After several minutes the mite(s) can be removed and stored as described earlier. The standard collection data of the host (specific locality, date of collection, collector’s name), host identification (including catalogue number of host, if known, and museum where host is deposited), and site of attachment of mite should be included with preserved mites. Mites from different host or attachment sites should not be mixed. It is also a good idea to label the host with an indication that mites were removed. In this way it is easier to later associate host with mites when host identifications are verified. Mites known to be parasitic on harvestmen belong to the families Trombidiidae and Erythraeidae. Only the larval forms are parasitic (protelean parasites), while the nymphs and adults are predaceous on small insects. Because the larval and postlarval stages of these two families are heteromorphic, that is, they do not resemble each other (see Chapter 9), systematists have long used different scientific names for different stages of a single species. To rear larval mites to adulthood, the living harvestman with attached mites

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should be placed in a culture vial. The vial should be small enough so that the harvestman is not active. If the mites are very small and will require several days before leaving the host, the harvestman can be kept in a separate clean jar (with a high humidity) before being transferred to a culture vial. Food should only be given to the harvestman while the mites are small and the specimen is in a clean jar. Once the mites are larger (preferably before they leave the host), the harvestman and mites can be placed in a culture vial. The harvestman should be removed as soon as the engorged mites leave the host. Likewise, it is a good idea to keep only a single mite per culture vial. Once the mite has left the host, it will be active for a few days and then will become inactive (appearing dead) as it enters the protonymphal stage. In about two weeks the active eight-legged deutonymph will emerge from the larval cuticle. This nymph is predatory, and a supply of Collembola or other small insects should be provided. After feeding sufficiently as a deutonymph it will again appear dead as it enters the tritonymph stage. In the few studies conducted, it usually took another two weeks before an adult emerged. Culture vials can be made from any plastic or glass vial with a tight-fitting lid. The vial should be small enough so that the mite will not be lost and the contents can be examined with a dissecting microscope. Fill the vial about half to two-thirds full of a mixture (9:1 by weight or 12:1 by volume) of plaster of paris and powered charcoal, making sure that all sides are covered with a layer of the mixture. The charcoal should be of high grade so that fungi will not grow on any unburned impurities (reagent grade is good). A cheaper substitute can be made by crushing activated bone charcoal that is used in water purifiers for home and fish aquaria. A couple of grooves in the bottom of the vial will provide a retreat for the mite. Before using the vial, check to make sure that there is no fungal growth and that there is sufficient moisture to maintain a high humidity (near 100% relative humidity). By saving the exuviae, the larval and following stages can be associated and later described. When rearing mites, it is very important to keep accurate records and label each exuviae and specimen. In addition to standard collection data (specific locality, host, date of collection, collector’s name), notes should be added to the label on site of attachment of the mite and number of days for each developmental stage. The exuviae can be carefully placed in alcohol and saved or slide mounted with the specimen positioned dorsal side up and with the legs spread in Hoyers, CMC, PVA, or Euparal media.

REARING AND MAINTENANCE OF HARVESTMEN IN CAPTIVITY Rodrigo H. Willemart Harvestmen are very convenient animals to keep in captivity since many species are relatively easy to maintain and may live for several months or even years (see Chapter 13). These features make harvestmen an especially appropriate group of organisms for laboratory studies. For beginners, keeping harvestmen in captivity allows the observation of how these animals behave when resting, walking, or feeding. For professionals, the careful observation of captive harvestmen can provide

Methods and Techniques of Study

a large amount of behavioral information, which can be important in itself and also can serve as the initial step for further studies. In this section I discuss how to house harvestmen, the importance of temperature and humidity, how to feed these animals, and the special attention required by nymphs.

Terrarium Several types of containers can be used to house harvestmen under laboratory conditions. Empty Styrofoam boxes are appropriate for large Neotropical gonyleptids when one intends only to keep them alive, without observing their behavior. This material has the advantage that it allows the animals to rest on vertical and upsidedown substrates, which are the preferred positions of some species. In addition, these boxes are light, which makes them easy to transport and allows them to be stacked, an important consideration for small laboratories. Another possibility is to maintain harvestmen in a glass terrarium (e.g., Avram, 1973; Hoenen & Gnaspini, 1999; Elpino-Campos et al., 2001; Willemart, 2001, 2002; Pereira et al., 2004) or Petri dishes (e.g., Pabst, 1953; Parisot, 1962; Martens, 1969b; Muñoz-Cuevas, 1971c), in which it is possible to observe their behavior. Some plastic containers, even if translucent, are not as transparent as glass and are therefore not recommended if one wishes to make detailed behavioral observations. Containers, terraria, and Petri dishes will be collectively called terraria throughout this text. The bottom of the terrarium can be covered with different kinds of substrates, such as soil, sand, stones, and humus, which may be brought from the species’ natural habitat. For species used to climbing on vegetation, the terrarium should be provided with rough vertical and horizontal substrates. However, a balance must be found between maximizing the surface area of the terrarium and keeping the animals visible. In small terraria no more than two adjacent walls should be covered with opaque substratum; otherwise there may be difficulty in observing harvestmen on the walls. Materials such as rocks, plastic, or wood may be used for the walls. Wood has the disadvantage that fungi can easily proliferate on it after some days. Plastic and rocks can be glued with superbonder (Henkel Loctite) or simply rested against the walls of the terrarium. A refuge in which the harvestmen can rest should be provided. For some species, usually short legged, that rest on the ground, this refuge can be the size of the harvestman and can be made from wood, rocks, dry leaves, or tiles. Species that have the habit of climbing will often prefer to rest in large, narrow, vertical crevices that can be produced with thin pieces of rocks. These refuges should be the darkest place in the terrarium, since most harvestmen are photophobic (Hillyard & Sankey, 1989). If several individuals are to be kept in the same terrarium, it should be remembered that some species are gregarious (Chapter 11) and will require larger refuges. With regard to the size of the terrarium, bigger is not necessarily better, since it may be difficult to find the harvestmen in a large terrarium. In addition, small species may need to be observed under a stereomicroscope, which is easier in a small terrarium. For example, Juberthie (1972) kept pairs of Cynortoides cubanus (Cosmetidae) in plastic boxes 8 cm wide and 5 cm high. Species that climb vegetation

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tend to move upward whenever possible, so high terraria are better for them. Juberthie (1964) provides details on the rearing of epigean and cavernicolous species and discusses the sizes of the terraria he used. Generally, only one species should be kept in each terrarium. By doing this, you will be sure that individuals of this species did everything that happened in the terrarium. If eggs appear covered with debris, you will know the kind of parental care of this species; if juveniles appear, you will know the species to which they belong; if individuals appear with legs amputated, you know that it was due to intraspecific interactions. The identification of individuals is important when observing behavior, so if it is not possible to recognize each specimen in the terrarium, then a femur and/or the dorsum of the animals should be marked with colored enamel paint (Elpino-Campos et al., 2001; Pereira et al., 2004).

Temperature and humidity Once built, the terrarium must be kept humid (Martens, 1965), and this can be done in several ways. Pabst (1953) and Immel (1954) moistened porous stones or the soil on the bottom of the terrarium; the latter procedure has also been used with tropical species (Hoenen & Gnaspini, 1999; Willemart, 2002). Juberthie (1972) used humid filter paper or a glass tube filled with water and stopped with a piece of cotton. A piece of wet cotton can also be used (Willemart, 2001), or the terrarium may be sprinkled with water when necessary (Capocasale & Bruno-Trezza, 1964). However, care must be taken with excessive humidity in some species. Anuradha and Parthasarathy (1976) reported that the optimum relative humidity for Gagrellula saddlana (Sclerosomatidae) was around 60%, and that these harvestmen did not tolerate a relative humidity above 85%. The eggs can only develop in a relatively humid environment (Juberthie, 1965) or on a damp substrate (Holm, 1947; Immel, 1954; Parisot, 1962; Avram, 1973), from which they absorb water. Fungi in the terrarium always need to be removed since they may contaminate harvestmen and be lethal to eggs (Gueutal, 1944a). Temperature may also be decisive. Acosta et al. (1993) reported high mortality in animals from a cold, high-altitude (ca. 2,000 m) locality that were taken to a laboratory in a warm locality (ca. 300 m altitude). The problem was solved by keeping the terrarium outdoors during the night and maintaining it in a refrigerator (ca. 12°C) during part of the day. For species from temperate regions, the use of a refrigerator is also advisable (Martens, 1965). Thermostats are useful for maintaining constant temperatures (Martens, 1969b), particularly for cave-dwelling species (e.g., Juberthie, 1964). The temperature and its variations should simulate the natural habitat (Juberthie, 1964; see also Rüffer, 1966). For eggs, temperatures around the optimum are essential; otherwise, embryonic development will take much longer or the eggs will not survive, as shown for the phalangiid Odiellus gallicus (see Chapter 13). Within the acceptable temperature range, higher temperatures may accelerate embryonic development (Gueutal, 1943; Juberthie, 1972; Goodnight & Goodnight, 1976; Bachmann & Schaefer, 1983a), although for some species from temperate

Methods and Techniques of Study

areas low temperatures are necessary during the embryonic phase (see Chapter 13). In Ischyropsalis strandi (Ischyropsalididae), a European species restricted to caves in which the temperature varies between 3° and 8°C, adults tolerated a temperature of 12°C in the laboratory, but this temperature was lethal for the eggs (Juberthie, 1974). Juberthie (1965) also showed that temperature influenced the number of eggs laid by females of I. strandi and Scotolemon lespesi (Sabaconidae). Thus simulating the temperature in the natural environment increases the chances of the eggs hatching, and constant temperatures above the “natural” ones may accelerate hatching (Gueutal, 1943).

Feeding Feeding harvestmen in the laboratory is easy since many of them accept a large variety of food items. Freshly killed arthropods such as isopods, live springtails (Collembola) and mites, dipteran larvae, pieces of larvae from beetles such as Tenebrio and Tribolium, or even larger dead prey such as katydids, spiders, and cockroaches have been offered with success (see Chapter 8). Hard, sclerotized insects must be cut before offering them to harvestmen since, depending on the strength of their chelicerae, the harvestmen may not be able to break the prey cuticle and will therefore not have access to the prey body contents. Pieces of earthworms are also accepted (Avram, 1973; Elpino-Campos et al., 2001), and Anuradha and Parthasarathy (1977) showed that a balanced artificial diet reduced the mortality of captive Gagrellula saddlana when compared with two unbalanced artificial diets. Plant items such as bananas, apples, tomatoes, boiled beans, broccoli, carrots, lettuce, rice, and sugar beets, as well as industrial food such as bread, cooked ground beef, cream cheese, and even cappuccino mousse, are also accepted (see Chapter 8). Finally, trogulids and some species of Ischyropsalis are food specialists and prefer snails, although they also accept other arthropods in captivity (see Chapter 8). A Petri dish or any easy-to-clean dish may be used to place the food on (Immel, 1954; Parisot, 1962). There are no stringent rules regarding the frequency of feeding. Unless it is infested with parasites, a well-fed harvestman has an enlarged abdomen, which is a good indicator of whether food should be provided. Guffey (1999) fed adult Leiobunum (Sclerosomatidae) species ad libitum, Avram (1973) fed adult Paranemastoma (Nemastomatidae) every two days, and Hoenen and Gnaspini (1999) and Willemart (2001, 2002) did so once a week. Capocasale and Bruno-Trezza (1964) left adult Acanthopachylus aculeatus (Gonyleptidae) without food for a maximum of 90 days, although this is not advisable unless for a specific purpose. Since nymphs usually eat more frequently, food can also be provided ad libitum. Food not consumed should be removed from the terrarium to avoid contamination by fungi.

Caring for eggs and nymphs Rearing harvestmen from egg to adulthood is not easy (Parisot, 1962) and requires special attention. Adult females may lay eggs, but they may not be seen since several species cover their eggs with soil particles or place them in crevices (see

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Chapter 12). However, Gueutal (1944b) reported that Phalangium opilio (Phalangiidae) only laid eggs next to a hard substrate, such as the transparent walls of the terrarium, thus making them easy to detect. Putting dishes with soil into a “sterile” container may induce certain species to oviposit there, and trogulids lay their eggs in empty snail shells that can be recovered for observation (Pabst, 1953). Eggs may be left where found or may be transferred to a separate Petri dish with humid filter paper on the bottom (Juberthie, 1972). In some species late embryonic development may be observed without using any special technique since the chorion is translucid (see Chapter 13). When the chorion is opaque, observation of the embryo is facilitated by submerging the eggs in olive or paraffin oil. After observation the eggs are replaced on the filter paper (Holm, 1947; Juberthie, 1964). In some cases even first-instar nymphs (especially small forms) may not be seen if close attention is not paid to the darker areas of the terrarium, and juveniles may be reared without the keeper knowing about it. If the terrarium has small openings, the young might flee. They may also drown in the water container, in water at the bottom of the terrarium, or even in small water droplets. Once dead, harvestmen rapidly lose their form and are no longer useful for morphological studies. Thus care must be taken to detect the young as soon as possible, and once detected, they should be transferred to small terraria with fewer refuges. This will make it easier to observe the young and to remove and preserve them as they die. Since cannibalism occurs among conspecifics while a nymph is molting or shortly thereafter, when the cuticle is still soft (see Chapter 8), it is important to house juveniles in separate terraria. This will also make it easier to follow the development of each individual. Juberthie (1972) reared the early instars of the cosmetid Cynortoides cubanus in small plastic boxes (4.5 cm wide × 3 cm high). When rearing nymphs, special care must be taken to control the humidity. Juberthie (1964) reported a loss of nymphs due to high humidity, and Klee and Butcher (1968) had problems with the high mortality of third- to fourth-instar nymphs of Phalangium opilio, which they attributed to the constant humidity of the terrarium. By removing the terrarium’s cover for a period each day, thereby varying the relative humidity from 40% to 90%, these authors were able to rear specimens from eggs to adulthood. Forceps should not be used to move juveniles since this could injure the animals. Instead, robust species can be grasped with the fingers by legs II or IV, which are longer and easier to catch than the other legs. Small Laniatores, Dyspnoi, and Eupnoi can be induced to climb onto a sheet of paper by using a paintbrush. It is important to stress, however, that specimens of the latter group may lose their legs if grasped by these appendages. Although the information provided here may be useful for several species, it may not be ideal for species whose behavior is still unknown. In such cases the species should be observed in the field, and the terrarium should then be prepared on the basis of microhabitats used by the species.

References

Åbro, A. 1988. The mode of attachment of mite larvae (Leptus spp.) to harvestmen (Opiliones). J. Nat. Hist., 22:123–130. Absolon, K., & J. Kratochvíl. 1932a. Peltaeonychidae, une famille nouvelle des Opilionides aveugles des grottes balcaniques [1]. Príroda, 25:153–156. Absolon, K., & J. Kratochvíl. 1932b. Peltaeonychidae, une famille nouvelle des Opilionides aveugles des grottes balcaniques [2]. Príroda, 25:206–212. Absolon, K., & J. Kratochvíl. 1932c. Zur Kenntnis der höhlenbewohnenden Araneae der illyrischen Karstgebiete. Mitt. Höhlen- u. Karstforschung, 3:73–81. Acosta, L. E. 1983. Sobre la fluorescencia del tegumento en Opiliones (Arachnida). Hist. Nat., 3:193–195. Acosta, L. E. 1989. La fauna de escorpiones y opiliones (Arachnida) de la provincia de Córdoba. Ph.D. Thesis, Universidad Nacional de Córdoba, Córdoba, Argentina. Acosta, L. E. 1993. El género Pachyloidellus Müller, 1918 (Opiliones, Gonyleptidae, Pachylinae). Bonn. zool. Beitr., 44:1– 18. Acosta, L. E. 1999. The identity of Pachyloides tucumanus comb. nov. (ex Bosqia), with a proposal of generic synonymy and the new name Pachyloides yungarum (Arachnida, Opiliones, Gonyleptidae). J. Arachnol., 27:458–464. Acosta, L. E. 2002a. Acrographinotus mitmaj, a new harvestman species from central Peru (Opiliones, Gonyleptidae, Pachylinae). J. Arachnol., 30:78–83. Acosta, L. E. 2002b. Patrones zoogeográficos de los opiliones argentinos (Arachnida: Opiliones). Rev. Ibér. Aracnol., 6:69–84. Acosta, L. E., F. E. Pereyra, & R. A. Pizzi. 1995. Field observation on Pachyloidellus goliath (Opiliones, Gonyleptidae) in Pampa de Achala, province of Córdoba. Bull. Br. Arachnol. Soc., 10:23–28. Acosta, L. E., T. I. Poretti, & P. E. Mascarelli. 1993. The defensive secretions of Pachyloidellus goliath (Opiliones, Laniatores, Gonyleptidae). Bonn. zool. Beitr., 44:19–31. Adams, J. 1984. The habitat and feeding ecology of woodland harvestmen (Opiliones) in England. Oikos, 42:361–370. Adams, J. 1985. The definition and interpretation of guild structure in ecological communities. J. Anim. Ecol., 54:43– 59.

Adis, J. 2002. Amazonian Arachnida and Myriapoda. Pensoft Publishers, Sofia. Alberti, G. 1979. Licht- und elektronenmikroskopische Untersuchungen an Coxaldrüsen von Walzenspinnen (Arachnida: Solifugae). Zool. Anz., 203:48–64. Alberti, G. 2005. Double spermatogenesis in Chelicerata. J. Morphol., 266:281–297. Alberti, G., & L. B. Coons. 1999. Acari: mites. Pp. 515–1215 in Microscopic Anatomy of Invertebrates, vol. 8C: Chelicerate Arthropoda (F. W. Harrison & R. F. Foelix, eds.). Wiley-Liss, New York. Alcock, J. 1994. Postinsemination associations between males and females in insects: the mate-guarding hypothesis. Ann. Rev. Ent., 39:1–21. Alderweireldt, M., R. Bosmans, & L. Vanhercke. 1993. The Araneae and Opiliones of the forest of Houthulst (Western Flanders, Belgium): results of a six-year survey. Bull. Annls Soc. r. Belg. Ent., 129:284–291. Aldrovandus, U. 1603. De animalibus insectis libri septem. Bologna. Alexander, R. McN. 1982. Locomotion of Animals. Blackie & Son, Glasgow. Almeida-Neto, M., G. Machado, R. Pinto-da-Rocha, & A. A. Giaretta. 2006. Harvestman species distribution along three neotropical elevational gradients: an alternative rescue effect to explain Rapoport’s rule? J. Biogeog., 33:361–375. Almquist, S. 1984. Samhällen av spindlar och lockespindlar på Knisa myr, Öland. Ent. Tidsk., 105:143–150. Anderson, D. T. 1973. Embryology and Phylogeny in Annelids and Arthropods. Pergamon Press, New York. Anderson, J. D., & P. J. Martino. 1967. Food habits of Eurycea longicauda longicauda. Herpetologica, 23:105–108. Anderson, J. F. 1966. The excreta of spiders. Comp. Biochem. Physiol., 17:973–982. Anderson, J. F. 1970. Metabolic rates of spiders. Comp. Biochem. Physiol., 33:51–72. Anderson, J. F. 1993. Respiratory energetics of two Florida harvestmen. Comp. Biochem. Physiol., 105A:67–72. Andersson, M. 1994. Sexual Selection. Princeton University Press, Princeton, NJ. Andreeva, T. R. 1989. Trophic relations by shorebirds from

525

526

References

placor tundra of South Yamala. Pp. 129–152 in Birds in the Communities of the Tundra Zone (Y. I. Chernov, ed.). Nauka, Moscow. [In Russian] Angelov, P., B. Gruev, & V. Tomov. 1972a. Untersuchungen über die Nahrung von Lacerta agilis L. und Lacerta taurica Pall. aus dem Rodopi-Gebirge. Natura, Zoologie Université de Plovdiv “Paissi Hilendarski,” 5:121–122. Angelov, P., B. Gruev, & V. Tomov. 1972b. Untersuchungen über die Nahrung von Lacerta viridis in Bulgaria. Trav. Sci. Univ. Plovdiv “Paissi Hilendarski,” Biol., 10:155–161. [In Bulgarian with summaries in Russian and German] Angelov, P., V. Tomov, & B. Gruev. 1972c. Untersuchungen über die Nahrung von Lacerta muralis Laur. Trav. Sci. Univ. Plovdiv “Paissi Hilendarski,” Biol., 10:147–150. [In Bulgarian with summaries in Russian and German] Angerilli, N., & R. G. Holmberg. 1986. Harvestmen of the twilight zone. Can. Caver, 17:6–9. Anuradha, K., & M. D. Parthasarathy. 1976. Field studies on the ecology of Gagrellula saddlana Roewer (Palpatores, Opiliones, Arachnida) and its behaviour in the laboratory conditions. Bull. Ethol. Soc. India, 1:68–71. Anuradha, K., & M. D. Parthasarathy. 1977. Mortality as an index in formulation of artificial diet for opilionids (Arachnida). Indian J. Exp. Biol., 15:1233–1234. Ardao, M. I., & H. A. Freyre. 1956. Effect of gonyleptidine on the metabolism of mammalian erythrocytes. Arch. Biochem. Biophys., 63:334–342. Argel-de-Oliveira, M. M., N. A. Curi, & T. Passerini. 1998. Feeding of a fledgling great kiskadee, Pitangus sulphuratus (Linnaeus) (Passeriformes, Tyrannidae) in urban environment. Revta bras. Zool., 15:1103–1109. Armas, L. F. 1987. Depredación de arácnidos por dos vertebrados cubanos. Misc. Zool., 34:1–2. Aschoff, J. 1960. Exogenous and endogenous components in circadian rhythms. Pp. 11–28 in Cold Spring Harbor Symposia on Quantitative Biology, 25. Long Island Biological Association, New York. Ashby, J. W. 1974. A study of arthropod predation of Pieris rapae L. using serological and exclusion techniques. J. Appl. Ecol., 11:419–425. Avery, R. A. 1966. Food and feeding habits of the common lizard (Lacerta vivipara) in the west of England. J. Zool., 149:115–121. Avilés, L. 1997. Causes and consequences of cooperation and permanent-sociality in spiders. Pp. 476–498 in The Evolution of Social Behavior in Insects and Arachnids (J. Choe & B. Crespi, eds.). Cambridge University Press, Cambridge. Avram, S. 1973. Contribution à la connaisance du développement embryonnaire et postembryonnaire chez Nemastoma cf. sillii Herrman (Opiliones, Nemastomatidae). Pp. 269–303 in Livre du Cinquantenaire de l’Institut de Spéologie “Émile

Racovitza” (T. Orghidan, ed.). Editura Academiei Republicii Socialiste Romania, Bucharest. Avram, S. 1977. Recherches sur les Opilionides de Cuba. III. Genres et espèces nouveaux de Caribbiantinae (Biantidae, Gonyleptomorphi). Investigaciones sobre los Opilionides de Cuba. III. Género y especies nuevas de Caribbiantinae (Biantidae, Gonyleptomorphi). Research on Cuban Opilionids. III. New genera and species of Caribbiantinae (Biantidae, Gonyleptomorphi). Pp. 123–136 in Résultats des expéditions biospéologiques cubano-roumaines à Cuba, vol. 2. Editura Academiei Republicii Socialiste Romania, Bucharest. Avram, S., & H. E. M. Soares. 1983. Opilionides du Pérou et d’Argentine. Pp. 47–64 in Résultats des expédititions biospéologiques cubano-roumaines à Cuba, vol. 4. Editura Academiei Republicii Socialiste Romania, Bucharest. Ax, P. 2000. Multicellular Animals. Vol. 2: The Phylogenetic System of the Metazoa. Springer-Verlag, Berlin. Babu, K. S. 1985. Pattern of arrangement and connectivity in the central nervous system of arachnids. Pp. 3–19 in Neurobiology of Arachnids (F. G. Barth, ed.). Springer-Verlag, Berlin. Bachmann, E., & M. Schaefer. 1983a. Notes on the life cycle of Phalangium opilio (Arachnida: Opilionida). Verh. naturw. Ver. Hamb., 26:255–263. Bachmann, E., & M. Schaefer. 1983b. The Opilionid fauna of a beech wood and dry grassland on limestone (Arachnida: Opiionida). Verh. naturw. Ver. Hamb., 26:141–149. Baker, E. W., & G. W. Wharton. 1952. An Introduction to Acarology. Macmillan Co., New York. Bakke, T. A. 1970. Feeding habits of the common gull in the Agdenes area, Trondelag. Fauna, 23:253–271. Bal´azy, S. 1978. A new species of Entomophthotaceae (Mycophyta: Entomophthorales) from Poland. J. Invertebr. Pathol., 31:275–279. Balbiani, M. 1872. Mémoire sur le développement des Phalangides. Annls Sci. nat., 16:1–28. Banks, N. 1892. A new genus of Phalangiidae. Proc. Ent. Soc. Wash., 2:249–250. Banks, N. 1893. The Phalanginae of the United States. Canad. Entomol., 25:205–211. Banks, N. 1894. The Nemastomatidae and Trogulidae of the United States. I. Psyche, 7:11–12. Banks, N. 1900. New genera and species of American Phalangida. J. New York Entomol. Soc., 8:199–201. Banks, N. 1901. Synopses of North-American invertebrates. XVI. The Phalangida. Am. Nat., 35:669–679. Bano, K. 1983. Behavior of Gagrellula sp. (Palpatores, Opiliones, Arachnida) during total solar eclipse. Sci. Cult., 49:359–362. Barber, H. 1931. Traps for cave inhabiting insects. J. Elisha Mitchell Soc., 46:259–266.

References

Barbosa, P. 1974. Manual of Basic Techniques in Insect Histology. Palmer Journal Register/Autumn Publishers, Amherst, MA. Barden, A. 1943. Food of the basilisk lizard in Panama. Copeia, 1943:118–121. Barnes, R. D. 1968. Invertebrate Zoology. 2nd ed. W. B. Saunders Co., Philadelphia. Barr, T. C., Jr. 1968. Cave ecology and the evolution of troglobites. Evol. Biol., 2:3–102. Barth, F. G. 1969. Die Feinstruktur des Spinnenintegumentes. I. Die Cuticula des Laufbeins adulterhautungsferner Tiere (Cupiennius salei Keys.). Z. Zellforsch. mikrosk. Anat., 97:137– 159. Barth, F. G. 1970. Die Feinstruktur des Spinnenintegumentes. II. Die raumliche Anordnung der Mikrofasern in der lamellierten Cuticula and ihre Beziehung zur Gestalt der Porenkanale (Cupiennius salei Keys., adult, hautungsfern, Tarsus). Z. Zellforsch. mikrosk. Anat., 104:87–106. Barth, F. G. 1985. Slit sensilla and the measurements of cuticular strains. Pp. 162–188 in Neurobiology of Arachnids (F. G. Barth, ed.). Springer-Verlag, Berlin. Barth, F. G., & J. Stagl. 1976. The slit sense organs of arachnids: a comparative study of their topography on the walking legs (Chelicerata, Arachnida). Zoomorphol., 86:1–23. Barthel, M., & H. Hetzer. 1982. Bernstein-Inklusen aus dem Miozän des Bitterfelder Raumes. Z. angew. Geol., 28:314– 336. Barus, V., B. Král, O. Oliva, E. Opatrny, J. Rehák, Z. Rocek, P. Roth, Z. Spinar, & L. Vojtková. 1992a. Obojzivelnici—Amphibia. Fauna CSFR, vol. 25. Akademia, Praha. Barus, V., B. Král, O. Oliva, E. Opatrny, J. Rehák, Z. Rocek, P. Roth, Z. Spinar, & L. Vojtková. 1992b. Plazi—Reptilia. Fauna CSFR, vol. 26. Akademia, Praha. Bastawade, D. B. 1992. First report of an arachnid order Cyphophthalmi(da) from India in Arunachal Pradesh. J. Bombay Nat. Hist. Soc., 89:268–269. Bateman, A. J. 1948. Intra-sexual selection in Drosophila. Heredity, 2:349–368. Bauerová, Z. 1982. Príspfvek k poznání potravy rejskt (Soricidae) ve smrkovych monokulturách. Vertebrat. zprávy, 1982:50–52. Bauerová, Z. 1984. The food eaten by Sorex araneus and Sorex minutus in a spruce monoculture. Folia Zool., 33:125–132. Bauerová, Z. 1986. Contribution to the trophic bionomics of Myotis emarginatus. Folia Zool., 35:305–310. Bauerová, Z. 1988. The food of Crocidura suaveolens. Folia Zool., 37:301–308. Bauerová, Z., & J. Cerveny. 1986. Towards an understanding of the trophic ecology of Myotis nattereri. Folia Zool., 35:55– 61. Beall, B. S. 1986. Reinterpretation of the Kustarachnida. Am. Arachnol., 34:4.

527

Beall, B. S. 1997. Arachnida. Pp. 140–154 in Richardson’s Guide to the Fossil Fauna of Mazon Creek (W. Shabica, & A. A. Hay, eds.). Northeastern Illinois University Press, Chicago. Beck, V. L. 1968. Sobre a biologia de alguns aracnídeos na floresta tropical da Reserva Ducke (INPA, Manaus/Brasil). Amazoniana, 1:243–246. Becker, A., & W. Peters. 1985a. Fine structure of the midgut gland of Phalangium opilio (Chelicerata, Phalangida). Zoomorphol., 105:317–325. Becker, A., & W. Peters. 1985b. The ultrastructure of the midgut and the formation of peritrophic membranes in a harvestman, Phalangium opilio (Chelicerata, Phalangida). Zoomorphol., 105:326–332. Begon, M. 1979. Investigating Animal Abundance: CaptureRecapture for Biologists. Edward Arnold, London. Beier, M. 1948. Phoresie und Phagophilie bei Pseudoscorpionen. Öst. zool. Z., 1:441–497. Bell, G. 1976. On breeding more than once. Am. Nat., 110:57– 77. Belskaja, G. S. 1965. Die Ökologie des Isabellsteinschmätzers in Turkmenien. Izvestiya Akademii Nauk Turkmenskoi SSR, ser. Biol., 2:64–73. [In Russian with summary in German] Benavente, R., & R. Wettstein. 1980. Ultrastructural characterization of the sex chromosomes during spermatogenesis of spiders having holocentric chromosomes and a long diffuse stage. Chromosoma, 77:69–81. Beninger, P. G., R. Cannuel, J. L. Blin, S. Pien, & O. Richard. 2001. Reproductive characteristics of the archaeogastropod Megathura crenulata. J. Shell Res., 20:301–307. Berendt, G. C. 1830. Die Insekten im Bernstein: Ein Beitrag zur Thiergeschichte der Vorwelt. Danzig. Berendt, G. C. 1845. Die im Bernstein befindlichen organischen Reste der Vorwelt, gesammelt, in Verbindung mit Mehren bearbeitet und herausgegeben. Neues Jb. Mineral. Geog. Geol. Pet., 1845:864–879. Bergh, J. C., & G. J. R. Judd. 1993. Degree-day model for predicting emergence of pear rust mite (Acari, Eriophyidae) deutogynes from overwintering sites. Environ. Ent., 22:1325–1332. Berland, L. 1949. Ordre des Opilions. Pp. 761–793 in Traité de zoologie, vol. 6 (P. -P. Grassé, ed.). Masson et Cie., Paris. Berry, P. Y. 1970. The food of the giant toad Bufo asper. Zool. J. Linn. Soc., 49:61–68. Beshkov, V. 1970. Biologiya i razprostranenie na grutskata zhaba (Rana graeca Blgr.) v Bulgaria. I. Izsledvaniya vurhu hranata i hraneneto. Izvestiya na Zoologicheskiya Institut s Muzey, 31:5–17. Beshkov, V., & T. Tsonchev. 1963. Duzhdovnikut (Salamandra salamandra L.) na Vitosha. Izvestiya na Zoologicheskiya Institut s Muzey, 31:79–91.

528

References

Betts, M. M. 1955. The food of titmice in oak woodland. J. Anim. Ecol., 24:282–323. Bilsing, S. W. 1920. Quantitative studies in the food of spiders. Ohio J. Sci., 20:215–260. Birkhead, T. R. 2000. Defining and demonstrating postcopulatory female choice—again. Evolution, 54:1057–1060. Birkhead, T. R., & A. P. Møller. 1998. Sperm Competition and Sexual Selection. Academic Press, San Diego. Bishop, S. C. 1949a. The function of the spur on the femur of the palpus of male Leiobunum calcar (Wood) (Arachnida: Phalangida). Ent. News, 60:10–11. Bishop, S. C. 1949b. The Phalangida (Opiliones) of New York. Proc. Rochester Acad. Sci., 9:159–235. Bishop, S. C. 1950. The life of a harvestman. Nature Mag., 43:264–267, 276. Bishop, S. C., & C. R. Crosby. 1924. A fossil species of Caddo (Opiliones) from the Baltic amber, and its living relatives. NY State Mus.Bull., 253:83–84. Blackburn, T. M., & K. J. Gaston. 1996. Spatial patterns in the geographical range sizes of bird species in the New World. Phil. Trans. R. Soc. B, 351:897–912. Blanc, H. 1880. Anatomie et physiologie de l’appareil sexuel male des phalangides. Bull. Soc. vaudoise Sci. nat., 17:49– 78. Blaszak, C. 1968. Badania nad interseksami u kosarzy (Opiliones). Pol. Pismo Ent., 38:9–27. Blick, T., & P. Bliss. 1991. Spinnentiere und Laufkäfer am Waldrand (Arachnida: Araneae, Opiliones, Pseudoscorpiones; Insecta: Coleoptera: Carabidae). Bull. Soc. neuchâtel. Sci. nat., 116:25–34. Blickhan, R., & F. G. Barth. 1985. Strains in the exoskeleton of spiders. J. Comp. Physiol., 157:115–147. Bliss, P. 1982. Die Weberknechte (Arachnida, Opiliones) der Naturschutzgebiete Großer und Kleiner Hakel und angrenzender Waldgebiete. Hercynia, N. F., 19:85–96. Bliss, P. 1990. Leiobunum limbatum (Arachnida, Opiliones) in der DDR: Verbreitungsmuster, Synanthropie und Arealexpansion. Pp. 34–35 in Comptes rendus de la XIIe Colloque Européen d’Arachnologie (M. -L. Célérier, J. Heurtault, & C. Rollard, eds.). Paris. Bliss, P., & A. Arnold. 1983. Zur Vertikalverbreitung von Mitopus morio (Fabricius, 1799) im Riba-Gebirge (Arachnida, Opiliones). Ent. Nachr. Ber., 27:276. Bliss, P., S. Heimer, & F. Tietze. 1981. Zur Arthropodenfauna eines Flurgehölzes bei Halle/Saale (Arachnida: Opiliones, Araneae; Coleoptera: Carabidae). Hercynia, N. F., 18:434– 440. Bliss, P., & F. Tietze. 1984. Die Struktur der epedaphischen Weberknechtefauna (Arachnida, Opiliones) in unterschiedlich immissionsbelasteten Kiefernforsten der Dübener Heide. Pedobiologia, 26:25–36.

Blomquist, G. J., D. R. Nelson, & M. de Renobales. 1987. Chemistry, biochemistry, and physiology of insect cuticular lipids. Arch. Insect Biochem. Physiol., 6:227–265. Blum, M. S. 1969. Alarm pheromones. Ann. Rev. Ent., 14:57– 80. Blum, M. S. 1981. Chemical Defenses of Arthropods. Academic Press, New York. Blum, M. S. 1985. Exocrine systems. Pp. 535–579 in Fundamentals of Insect Physiology (M. S. Blum, ed.). John Wiley & Sons, New York. Blum, M. S., & A. L. Edgar. 1971. 4-methyl-3-heptanone: identification and role in opilionid exocrine secretions. Insect Biochem., 1:181–188. Bonnet, P. 1958. Bibliographia Araneorum. Vol. 2 (4me partie NS), pp. 3027–4230. Douladoure, Toulouse. Borek, V. 1958. K fenologii nasich sekácu (Opilionidea). Acta Soc. Entomol. Cechosloveniae, 55:297–298. Boudreaux, H. B. 1979. Significance of intersegmental tendon system in arthropod phylogeny and a monophyletic classification of Arthropoda. Pp. 551–586 in Arthropod Phylogeny (A. P. Gupta, ed.). Van Nostrand Reinhold, New York. Bowler, P. J. 1996. Life’s Splendid Drama. University of Chicago Press, Chicago. Boyer, S. L., & G. Giribet, 2003. A new Rakaia species (Opiliones, Cyphophthalmi, Pettalidae) from Otago, New Zealand. Zootaxa, 133:1–14. Boyer, S. L., I. Karaman, & G. Giribet. 2005. The genus Cyphophthalmus (Arachnida, Opiliones, Cyphophthalmi) in Europe: a phylogenetic approach to Balkan Peninsula biogeography. Mol. Phylog. Evol., 36:554–567. Bradley, R. A. 1984. The influence of the quantity of food on fecundity in the desert grassland scorpion (Paruroctonus utahensis) (Scorpionida, Vaejovidae): an experimental test. Oecologia, 62:53–56. Bragagnolo, C., & R. Pinto-da-Rocha. 2003. Diversidade de opiliões do Parque Nacional da Serra dos Órgãos, Rio de Janeiro, Brasil (Arachnida: Opiliones). Biota Neotrop., 3:1– 20. Brandon, R. A. 1965. Morphological variation and ecology of the salamander Phaeognathus hubrichti. Copeia, 1965:67– 71. Brandt, M., & D. Mashberg. 2002. Bugs with a backpack: the function of nymphal camouflage in the West African assassin bugs Paredocla and Acanthapsis spp. Anim. Behav., 63:277–284. Breidbach, O., & R. Wegerhoff. 1993. Neuroanatomy of the central nervous system of the harvestman, Rilaena triangularis (Herbst, 1799) (Arachnida; Opiliones)—principal organization, GABA-like and serotonin-immunohistochemistry. Zool. Anz., 230:55–81.

References

Brescovit, A. D., R. Bertani, R. Pinto-da-Rocha, & C. A. Rheims. 2004. Aracnídeos da Estação Ecológica Juréia-Itains: inventário preliminar e história natural. Pp. 198–221 in Estação Ecológica Juréia-Itains: Ambiente físico, flora e fauna (O. V. Marques & W. Duleba, eds.). Editora Holos, Ribeirão Preto. Briggs, T. S. 1968. Phalangids of the laniatorid genus Sitalcina (Phalangodidae: Opiliones). Proc. Calif. Acad. Sci., 36:1–32. Briggs, T. S. 1969. A new holarctic family of laniatorid phalangids (Opiliones). Pan-Pacif. Ent., 45:35–50. Briggs, T. S. 1971a. The harvestmen of family Triaenonychidae in North America (Opiliones). Occ. Pap. Calif. Acad. Sci., 90:1–43. Briggs, T. S. 1971b. Relict harvestmen from the Pacific Northwest (Opiliones). Pan-Pacif. Ent., 47:165–178. Briggs, T. S. 1974a. Phalangodidae from caves in the Sierra Nevada (California) with a redescription of the type genus (Opiliones: Phalangodidae). Occ. Pap. Calif. Acad. Sci., 108:1–15. Briggs, T. S. 1974b. Troglobitic harvestmen recently discovered in North American lava tubes (Travuniidae, Erebomastridae, Triaenonychidae: Opiliones). J. Arachnol., 1:205–214. Briggs, T. S., & D. Ubick. 1981. Studies on cave harvestmen of the central Sierra Nevada with descriptions of new species of Banksula. Proc. Calif. Acad. Sci., 42:315–322. Briggs, T. S., & D. Ubick. 1989. The harvestman family Phalangodidae. 2. The new genus, Microcina (Opiliones, Laniatores). J. Arachnol., 17:207–220. Brignoli, P. M. 1968. Note su Sironidae, Phalangodidae e Trogulidae Italiani, cavernicoli ed endogei (Opiliones). Frag. Entomol., 5:259–293. Bristowe, W. S. 1925. Notes on the habits of insects and spiders in Brazil. Trans. R. Ent. Soc. Lond., 1924:475–504. Bristowe, W. S. 1941. The Comity of Spiders. Vol. 2. Ray Society, London. Bristowe, W. S. 1949. The distribution of harvestmen (Phalangida) in Great Britain and Ireland, with notes on their names, enemies and food. J. Anim. Ecol., 18:100–114. Brown, D. 1984. Observations on the distribution and life cycle of Dicranopalpus ramosus (Simon, 1909): Opiliones. Newsl. Br. Arachnol. Soc., 40:7–8. Brownell, P., & G. A. Polis. 2001. Scorpion Biology and Research. Oxford University Press, New York. Bruno, S. 1973. Anfibi d’Italia: Caudata (Studi sulla fauna erpetologica italiana—XVII). Natura—Società italiana di Scienze naturali, del Museo civico di Storia naturale di Milano, del Civico planetario “Ulrico Hoepli” e dell’Acquario Civico di Milano, 64:209–450. Brust, G. E., B. R. Stinner, & D. A. McCartney. 1986. Predation by soil-inhabiting arthropods in intercropped and mono-

529

culture agroecosystems. Agric. Ecos. Environ., 18:145– 154. Bull, J. J. 1983. Evolution of Sex Determining Mechanisms. Benjamin Cummings Publishing Company, Menlo Park, CA. Bulmer, M. G., & G. A. Parker. 2002. The evolution of anisogamy: a game-theoretic approach. Proc. R. Soc. B, 269:2381–2388. Burda, H., & Z. Bauerová. 1985. Hearing adaptations and feeding ecology in Sorex araneus and Cerocidura suaveolens (Soricidae). Acta zool. fenn., 173:253–254. Bures, S. 1986. Composition of the diet and trophic ecology of the collared flycatcher (Ficedula albicollis albicollis) in three segments of groups of types of forest geobiocenoses in Central Moravia (Czechoslovakia). Folia Zool., 35:143– 155. Burton, R. F. 1984. Haemolymph composition in spiders and scorpions. Comp. Biochem. Physiol., 78A:613–616. Buse, A., D. Hadley, & T. Sparks. 2001. Arthropod distribution on an alpine elevational gradient: the relationship with preferred temperature and cold tolerance. Europ. J. Ent., 98:301–309. Butt, A. G., & H. H. Taylor. 1986. Salt and water balance in the spider, Porrhothele antipodiana (Mygalomorpha: Dipluridae): effects of feeding upon hydrated animals. J. Exp. Biol., 125:85–106. Butt, A. G., & H. H. Taylor. 1991. The function of spider coxal organs: effects of feeding and salt-loading on Porrhothele antipodiana (Mygalomorpha: Dipluridae). J. Exp. Biol., 158:439–461. Butt, A. G., & H. H. Taylor. 1995. Regulatory responses of the coxal organs and the anal excretory system to dehydration and feeding in the spider Porrhothele antipodiana (Mygalomorpha: Dipluridae). J. Exp. Biol., 198:1137–1149. Butterfield, J., J. C. Coulson, & S. Wanless. 1981. Studies on the distribution, food, breeding biology and relative abundance of the pygmy and common shrews (Sorex minutus and S. araneus) in upland areas of northern England. J. Zool., 195:169–180. Buxton, B. H. 1913. Coxal glands of the arachnids. Zool. Jb., suppl., 14:231–282. Buxton, B. H. 1917. Notes on the anatomy of arachnids. J. Morphol., 29:1–31. Buzatto, B. A., G. S. Requena, & G. Machado. 2003. Cuidado maternal no opilião Serracutisoma proximum (Opiliones: Gonyleptidae). P. 224 in Proceedings of IV Encontro de Aracnólogos do Cone Sul (G. Machado & A. D. Brescovit, eds.). São Pedro, São Paulo, Brazil. Buzatto, B. A., G. S. Requena, & G. Machado. 2005. Biologia reprodutiva do opilião Serracutisoma proximum (Opiliones: Gonyleptidae): escolha de sítio de oviposição e estratégias alternativas de acasalamento. P. 224 in Proceedings of I

530

References

Congresso Latino Americano de Aracnologia (C. A. ToscanoGadea, ed.). Minas, Lavalleja, Uruguay. Cáceres, N. C. 2002. Food habits and seed dispersal by the white-eared opossum Didelphis albiventris in southern Brazil. Stud. Neotrop. Fauna Environ., 37:97–104. Cáceres, N. C., & E. L. A. Monteiro-Filho. 2001. Food habits, home range and activity of Didelphis aurita (Mammalia, Marsupialia) in a forest fragment of southern Brazil. Stud. Neotrop. Fauna Environ., 36:85–92. Camacho, J. P. M. 2004. B Chromosomes in the Eukaryote Genome. Karger, Basel. Camacho, J. P. M., M. W. Shaw, M. D. López-León, M. C. Pardo, & J. Cabrero. 1997. Population dynamics of a selfish B chromosome neutralized by the standard genome in the grasshopper Eyprepocnemis plorans. Am. Nat., 149:1030–1050. Canals, J. 1936. Observaciones biológicas en arácnidos del orden Opiliones. Revta chil. Hist. nat., 40:61–63. Canard, A., & R. Stockman. 1993. Comparative postembryonic development of arachnids. Mem. Queensland Mus., 33:461– 468. Cannata, L. 1988. Observations sur les opilions de la tourbière du Cachot. Bull. Soc. neuchâtel. Sci. nat., 111:67–70. Capocasale, R. M. 2004. Nuevos datos sobre Acropsopilio chilensis Silvestri, 1904 (Opiliones, Caddidae) con la descripción del macho. Rev. Ibér. Aracnol., 9:287–290. Capocasale, R. M., & L. Bruno-Trezza. 1964. Biología de Acanthopachylus aculeatus (Kirby, 1819) (Opiliones: Pachylinae). Rev. Soc. Uruguaya Ent., 6:19–32. Capocasale, R. M., & E. Gudynas. 1993. La fauna de Opiliones (Arachnida) del criptozoos de Sierra de las Animas (Uruguay). Aracnología, 19/20:1–15. Caporiacco, L. di. 1951. Studi sugli Aracnidi del Venezuela racolti dalla sezione di Biologia (Universitá Centrale del Venezuela). I parte: Scorpiones, Solifuga, Opiliones e Chernetes. Acta Biol. Venez., 1:1–46. Carbayo, F., & A. M. Leal-Zanchet. 2003. Two new genera of geoplanid land planarians (Platyhelminthes: Tricladida: Terricola) of Brazil in the light of cephalic specialisations. Invertebr. Syst., 17:449–468. Carbayo, F., A. M. Leal-Zanchet, & E. M. Vieira. 2002. Terrestrial flatworm (Platyhelminthes: Tricladida: Terricola) diversity versus man-induced disturbance in an ombrophilous forest in southern Brazil. Biodiv. Conserv., 11:1091–1104. Caroll, A. L. K. 1966. Food habits of Pukeko (Porphyrio melanotus). Natornis, 13:133–141. Carter, N. E., & N. R. Brown. 1973. Seasonal abundance of certain soil arthropods in a fenitrothion-treated red spruce stand. Canad. Ent., 105:1065–1073. Castanho, L. M., & R. Pinto-da-Rocha. 2005. Harvestmen (Opiliones: Gonyleptidae) predating on treefrogs (Anura: Hylidae). Rev. Ibér. Aracnol., 11:43–45.

Cekalovic, K. T. 1974. Acropsopilio normae n.sp. de opilionido para la fauna Chilena (Arachnida, Opiliones, Acropsopilionidae). Boln Soc. Biol. Concepción, 48:23–31. Chemini, C. 1980. Phalangids by pitfall trapping from Fagona, Province of Bolzano, northern Italy. Studi Trentini Sci. Nat., 56:61–69. Chemini, C. 1981. The opilionid community of a hornbeam wood near Pergine, Trento, Italian Alps. Studi Trentini Sci. Nat., 57:67–73. Chemini, C. 1984. Andromorphy in a female Nemastoma dentigerum Canestrini (Opiliones) from Northern Italy. Newsl. Br. Arachnol. Soc., 40:56. Chemini, C. 1995. Arachnida Scorpiones, Palpigradi, Solifugae, Opiliones. Pp. 1–8 in Checklist delle specie della fauna italiana, vol. 21 (A. Minelli, S. Ruffo, & S. La Posta, eds.). Calderini, Bologna. Cherix, D., & J. D. Bourne. 1980. A field study on a super-colony of the red wood ant Formica lugubris Zett. in relation to other predatory arthropods (spiders, harvestmen and ants). Rev. suisse Zool., 87:955–973. Choe, J., & B. Crespi, eds. 1997. The Evolution of Social Behavior in Insects and Arachnids. Cambridge University Press, Cambridge. Churchfield, J. S. 1979. A note on the diet of the European water shrew, Neomys fodiens bicolor. J. Zool., 188:294–296. Churchfield, J. S. 1982. Food availability and the diet of the common shrew, Sorex araneus, in Britain. J. Anim. Ecol., 51:15–28. Churchfield, J. S., & V. K. Brown. 1987. The trophic impact of small mammals in successional grasslands. Biol. J. Linn. Soc., 31:273–290. Churchfield, J. S., J. Hollier, & V. K. Brown. 1991. The effects of small mammal predators on grassland invertebrates, investigated by field enclosure experiment. Oikos, 60:283–290. Ciccarone, C., & G. Campadelli. 1998. Un infrequente micoparassita di Opilionidi. Bollettino dell’Istituto di entomologia “Guido Grandi” della Università degli studi di Bologna, 52:47–53. Ciobanu, M. 1977. The Fossil Fauna of Oligocene in Piatra Neamq. Academiei Republicii Socialiste Romania, Bucharest. Cîrdei, F. 1958. K izucheniyu senokostsev (Opiliones) iz severozapadnoy chastuy RNR i verhnego rechnego basseyna Pruta. Analele stiintifice ale Universitˇatii “Al. I. Cuza,” 4:355–386. Clark, M. S., & S. H. Gage. 1997. The effects of free-range domestic birds on the abundance of epigeic predators and earthworms. Appl. Soil Ecol., 5:255–260. Clarke, K. U. 1979. Visceral anatomy and arthropod phylogeny. Pp. 467–549 in Arthropod Phylogeny (A. P. Gupta, ed.). Van Nostrand Reinhold, New York. Clarke, R. D. 1974. Food habitats of toads, genus Bufo (Amphibia: Bufonidae). Am. Mid. Nat., 91:140–147.

References

Clawson, R. L. 1988. Morphology of defense glands of the opilionids (daddy longlegs) Leiobunum vittatum and Leiobunum flavum (Arachnida: Opiliones: Palpatores: Phalangiidae). J. Morphol., 196:363–381. Clingenpeel, L. W., & A. L. Edgar. 1966. Certain ecological aspects of Phalangium opilio (Arthropoda: Opiliones). Pap. Mich. Acad. Sci., 51:119–126. Clopton, R. E. 2003. Nebraska Sandhills Gregarine Survey. Host Collections Data. http://science.peru.edu/gregarina/ html/opiliones.html#Lpacificus Cloudsley-Thompson, J. L. 1948. Notes on Arachnida. 4. Courtship behaviour of the harvester Mitopus morio. Ann. Mag. Nat. Hist., 11:809–810. Cloudsley-Thompson, J. L. 1956. Notes on Arachnida. 25. An unusual case of phoresy by false-scorpions. Ent. Mon. Mag., 92:71. Cloudsley-Thompson, J. L. 1958. Spiders, Scorpions, Centipedes and Mites. Pergamon Press, London. Cloudsley-Thompson, J. L. 1978. Biological clocks in Arachnida. Bul. Br. Arachnol. Soc., 4:184–191. Cloudsley-Thompson, J. L. 1985. An aggregation of Opiliones (Arachnida) in Southern Portugal. Ent. Mon. Mag., 123:238. Cloudsley-Thompson, J. L. 1988. Evolution and Adaptation of Terrestrial Arthropods. Springer-Verlag, Berlin. Cockerell, T. D. A. 1907. Some fossil arthropods from Florissant, Colorado. Bull. Am. Mus. Nat. Hist., 23:606–616. Cockerill, J. J. 1988. Notes on aggregations of Leiobunum (Opiliones) in the Southern U.S.A. J. Arachnol., 16:123–126. Coddington, J. A., G. Giribet, M. S. Harvey, L. Prendini, & D. E. Walter. 2004. Arachnida. Pp. 296–318 in Assembling the Tree of Life (J. Cracraft & M. J. Donoghue, eds.). Oxford University Press, New York. Coddington, J. A., M. Horner, & E. A. Soderstrom. 1990. Mass aggregations in tropical harvestmen (Opiliones, Gagrellidae: Prionostemma sp.). Rev. Arachnol., 8:213–219. Cokendolpher, J. C. 1980. Replacement name for Mesosoma Weed, 1892, with a revision of the genus (Opiliones, Phalangiidae, Leiobuninae). Occ. Pap. Mus., Texas Tech Univ., 66:19pp. Cokendolpher, J. C. 1981a. Can anyone add to his observations on the viability and hatching periods of the eggs of arachnids? Newsl. Br. Arachnol. Soc., 32:5. Cokendolpher, J. C. 1981b. The harvestman genus Liopilio Schenkel (Opiliones: Phalangiidae). J. Arachnol., 9:309–316. Cokendolpher, J. C. 1981c. Revision of the genus Trachyrhinus Weed (Opiliones, Phalangioidea). J. Arachnol., 9:1–18. Cokendolpher, J. C. 1982. Comments on some Leiobunum species of the USA (Opiliones; Palpatores, Leiobunidae). J. Arachnol., 10:89–90. Cokendolpher, J. C. 1984a. Homonyms of American and Euro-

531

pean Leiobunum (Opiliones, Palpatores, Leiobuninae). J. Arachnol., 12:118–119. Cokendolpher, J. C. 1984b. A new genus of North American harvestmen (Arachnida: Opiliones: Palpatores). Pp. 27–43 in Festschrift for Walter W. Dalquest in Honor of His Sixtysixth Birthday (N. V. Horner, ed.). Midwestern State University Press, Wichita Falls, TX. Cokendolpher, J. C. 1985a. Erebomastridae: replaced by Cladonychiidae (Arachnida: Opiliones). Ent. News, 96:36. Cokendolpher, J. C. 1985b. Revision of the harvestman genus Leptobunus and dismantlement of the Leptobunidae (Arachnida: Opiliones: Palpatores). J. New York Entomol. Soc., 92:371–402. Cokendolpher, J. C. 1987a. A new species of fossil Pellobunus from Dominican amber (Arachnida: Opiliones: Phalangodidae). Caribb. J. Sci., 22:205–211. Cokendolpher, J. C. 1987b. Observation on the defensive behavior of a neotropical Gonyleptidae (Arachnida, Opiliones). Rev. Arachnol., 7:59–63. Cokendolpher, J. C. 1991. Cosmetophilus vonones, N.g., N. sp., (Apicomplexa: Actinocephalidae) in the harvestman Vonones sayi (Arachnida: Cosmetidae). J. Protozool., 38:461–464. Cokendolpher, J. C. 1993. Pathogens and parasites of Opiliones (Arthropoda: Arachnida). J. Arachnol., 21:120–146. Cokendolpher, J. C. 2004. Revalidation of the harvestman genus Chinquipellobunus (Opiliones: Stygnopsidae). Texas Mem. Mus., Speleol. Monogr., 6:143–152. Cokendolpher, J. C., & J. D. Brown. 1985. Air-dry method for studying chromosomes of insects and arachnids. Ent. News, 96:114–118. Cokendolpher, J. C., & J. E. Cokendolpher. 1982. Reexamination of the Tertiary harvestmen from the Florissant Formation, Colorado (Arachnida: Opiliones: Palpatores). J. Paleont., 56:1213–1217. Cokendolpher, J. C., & J. E. Cokendolpher. 1984. A new genus of harvestmen from Costa Rica with comments on the status of the Neotropical Phalangiinae (Opiliones, Phalangiidae). Bul. Br. Arachnol. Soc., 6:167–172. Cokendolpher, J. C., & S. R. Jones. 1991. Karyotype and notes on the male reproductive system and natural history of the harvestman Vonones sayi (Simon) (Opiliones, Cosmetidae). Proc. Ent. Soc. Wash., 93:86–91. Cokendolpher, J. C., & L. D. Lanfranco. 1985. Opiliones from the Cape Horn Archipelago: new southern records for harvestmen. J. Arachnol., 13:311–320. Cokendolpher, J. C., & V. F. Lee 1993. Catalogue of the Cyphopalpatores and Bibliography of the Harvestmen (Arachnida, Opiliones) of Greenland, Canada, USA, and Mexico. Privately published, Lubbock, TX. Cokendolpher, J. C., W. P. MacKay, & M. H. Muma. 1993. Seasonal populations phenology and habitat preferences of

532

References

montane harvestmen (Arachnida: Opiliones) from southwestern New Mexico. SWest. Nat., 38:236–240. Cokendolpher, J. C., & G. O. Poinar Jr. 1992. Tertiary harvestmen from Dominican Republic amber (Arachnida: Opiliones: Phalangodidae). Bul. Br. Arachnol. Soc., 9:53– 56. Cokendolpher, J. C., & G. O. Poinar Jr. 1998. A new fossil harvestman from Dominican Republic amber (Opiliones, Samoidae, Hummelinckiolus). J. Arachnol., 26:9–13. Cokendolpher, J. C., & W. D. Sissom. 1988. New gynandromorphic Opiliones and Scorpiones. Bul. Br. Arachnol. Soc., 7:278–280. Cokendolpher, J. C., & W. D. Sissom. 2000. Further contributions to the study of Dalquestia (Opiliones: Sclerosomatidae). Ent. News, 111:243–249. Cole, L. K., M. S. Blum, & R. W. Roncadori. 1975. Antifungal properties of the insect alarm pheromones, citral, 2heptanone, and 4-methyl-3-heptanone. Mycologia, 67:701– 708. Colwell, R. K. 1994–2000. EstimateS: Statistical estimation of species richness and shared species from samples. Available at:viceroy.ebb.uconn.edu/estimates Corey, D. T., & I. J. Stout. 1990. Ground surface active arachnids in sandhill communities of Florida. J. Arachnol., 18:167–172. Cory, J. S., P. F. Entwistle, H. J. Killick, C. J. Doyle, & A. C. Forkner. 1988. Persistence and dispersal of pine beauty moth, Panolis flammea, nuclear polyhedrosis virus in pine forests in Scotland. Asp. Appl. Biol., 17:249–250. Cramp, S., D. J. Brooks, E. Dunn, R. Gillmor, J. Hall-Craggs, P. A. D. Hollom, E. M. Nicholson, M. A. Ogilvie, C. S. Roselaar, P. J. Sellar, K. E. L. Simmons, K. H. Voous, D. I. M. Wallace, & M. G. Wilson. 1988. Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Palearctic. Vol. 5: Tyrant Flycatchers to Thrushes. Oxford University Press, Oxford. Cramp, S., D. J. Brooks, E. Dunn, R. Gillmor, P. A. D. Hollom, R. Hudson, E. M. Nicholson, M. A. Ogilvie, P. J. S. Olney, C. S. Roselaar, K. E. L. Simmons, K. H. Voous, D. I. M. Wallace, J. Wattel, & M. G. Wilson. 1985. Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Palearctic. Vol. 4: Terns to Woodpeckers. Oxford University Press, Oxford. Cramp, S., J. B. Duncan, E. Dunn, R. Gillmor, J. Hall-Craggs, P. A. D. Hollom, E. M. Nicholson, M. A. Ogilvie, C. S. Roselaar, P. J. Sellar, K. E. L. Simmons, D. W. Snow, D. Vincent, K. H. Voous, D. I. M. Wallace, & M. G. Wilson. 1992. Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Palearctic. Vol. 6: Warblers. Oxford University Press, Oxford. Cramp, S., C. M. Perrins, D. J. Brooks, E. Dunn, R. Gillmor, J.

Hall-Craggs, B. Hillcoat, P. A. D. Hollom, E. M. Nicholson, C. S. Roselaar, W. T. C. Seale, P. J. Sellar, K. E. L. Simmons, D. W. Snow, D. Vincent, K. H. Voous, D. I. M. Wallace, & M. G. Wilson. 1993. Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Palearctic. Vol. 7: Flycatchers to Shrikes. Oxford University Press, Oxford. Cramp, S., C. M. Perrins, D. J. Brooks, E. Dunn, R. Gillmor, J. Hall-Craggs, B. Hillcoat, P. A. D. Hollom, E. M. Nicholson, C. S. Roselaar, W. T. C. Seale, P. J. Sellar, K. E. L. Simmons, D. W. Snow, D. Vincent, K. H. Voous, D. I. M. Wallace, & M. G. Wilson. 1994a. Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Palearctic. Vol. 9: Buntings and New World Warblers. Oxford University Press, Oxford. Cramp, S., C. M. Perrins, J. B. Duncan, E. Dunn, R. Gillmor, J. Hall-Craggs, B. Hillcoat, P. A. D. Hollom, E. M. Nicholson, C. S. Roselaar, W. T. C. Seale, P. J. Sellar, K. E. L. Simmons, D. W. Snow, D. Vincent, K. H. Voous, D. I. M. Wallace, & M. G. Wilson. 1994b. Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Palearctic. Vol. 8: Crows to Finches. Oxford University Press, Oxford. Cramp, S., K. E. L. Simmons, R. Gillmor, P. A. D. Hollom, R. Hudson, E. M. Nicholson, M. A. Ogilvie, P. J. S. Olney, C. S. Roselaar, K. H. Voous, D. I. M. Wallace, & J. Wattel. 1980. Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Palearctic. Vol. 2: Hawks to Bustards. Oxford University Press, Oxford. Cramp, S., K. E. L. Simmons, R. Gillmor, P. A. D. Hollom, R. Hudson, E. M. Nicholson, M. A. Ogilvie, P. J. S. Olney, C. S. Roselaar, K. H. Voous, D. I. M. Wallace, & J. Wattel. 1983. Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Palearctic. Vol. 3: Waders to Gulls. Oxford University Press, Oxford. Crawford, R. L. 1992. Catalogue of the genera and type species of the harvestman superfamily Phalangioidea (Arachnida). Burke Mus. Contr. Anthropol. Nat. Hist., 8:1–60. Crome, W., R. Gottschalk, H. Hanneman, G. Hatwich, & R. Kilias. 1969. Urania Tierreich, Wirbellose Tiere. 2 (Annelida bis Chaetognatha). Urania-Verlag, Leipzig. Crosby, C. R. 1911. A new species of Phalangida from Missouri. Canad. Ent., 43:20–22. Crosby, C. R., & S. C. Bishop. 1924. Notes on the Opiliones of the southeastern United States with descriptions of new species. J. Elisha Mitchell Soc., 40:8–26. Crossley, A. C. 1984. Nephrocytes and pericardial cells. Pp. 487–515 in Comprehensive Insect Physiology, Biochemistry and Pharmacology, vol. 3 (G. A. Kerkut & L. I. Gilbert, eds.). Pergamon Press, Oxford. Curry, S. J., W. F. Humphreys, L. E. Koch, & B. Y. Main. 1985.

References

Changes in arachnid communities resulting from forestry practices in karri forest, southwest Western Australia. Aust. Forest Res., 15:469–480. Curtis, D. J. 1969. The fine structure of photoreceptors in Mitopus morio (Phalangida). J. Cell Sci., 4:327–351. Curtis, D. J. 1970. Comparative aspects of fine structure of eyes of Phalangida (Arachnida) and certain correlations with habitat. J. Zool., 160:231–265. Curtis, D. J. 1973. Spiders and phalangids of Inchcailloch, Loch Lomond. I. General considerations. West. Nat., 2:29–39. Curtis, D. J. 1975. Spiders and phalangids of Inchcailloch, Loch Lomond. II. Seasonal activity of harvestmen. West. Nat., 4:114–119. Curtis, D. J. 1978a. Community parameters of the ground layer araneid—opilionid taxocene of a Scottish island. Symp. Zool. Soc. London, 42:149–159. Curtis, D. J. 1978b. Spiders and phalangids of Inchcailloch, Loch Lomond. III. Comparison with the mainland. West. Nat., 7:27–45. Curtis, D. J. 1980. Pitfalls in spider community studies. J. Arachnol., 8:271–280. Curtis, D. J. 1981. Describing communities of land invertebrates—attempting the impossible? Scott. Field Stud., 1981:18–27. Curtis, D. J., & E. Bignal. 1980. Variations in peat bog spider communities related to environmental heterogeneity. Pp. 81–86 in Proceedings of the 8th International Congress of Arachnology (J. Gruber, ed.). Verlag H. Egermann, Vienna. Curtis, D. J., E. J. Curtis, & D. B. A. Thompson. 1990. On the effect of trampling on montanne spiders and other arthropods. Pp. 103–109 in Comptes rendus de la XIIe Colloque Européen d’Arachnologie (M. -L. Célérier, J. Heurtault, & C. Rollard, eds.). Paris. Curtis, D. J., & E. Morton. 1974. Notes on spiders from tree trunks of different bark texture; with indices of diversity and overlap. Bul. Br. arachnol. Soc., 3:1–5. Cutler, B. 2001. Corrugated cardboard trapping for litter inhabiting spiders and other arthropods. Ent. News, 112:212–216. Dahl, F. 1903. Eine eigenartige Metamorphose der Troguliden, eine Verwandlung von Amopaum in Dicranolasma und von Metopoctea in Trogulus. Sber. Ges. naturf. Freunde Berlin, 1903:278–292. Dahl, M., H. Hedicke, A. Kästner, E. Marcus, E. P. Schulze, & H. Graf Vitzthum. 1935. Zur Kenntnis der Spinnentiere Schlesiens (Araneae, Opiliones, Pseudoscorpionida, Acarina, Tardigrada.). Sber. Ges. naturf. Freunde Berlin, 1935:337–357. Dallman, M. 1987. Der Zaunkönig: Troglodytes troglodytes. A. Ziemsen Verlag, Wittenberg Lutherstadt. Dambach, M., & B. Goehlen. 1999. Aggregation density and

533

longevity correlate with humidity in first-instar nymphs of the cockroach (Blatella germanica L., Dictyoptera). J. Insect Physiol., 45:423–429. Damen, W. G. M., M. Hausdorf, E-A. Seyfarth, & D. Tautz. 1998. A conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider. Proc. Natl. Acad. Sci. USA, 95:10665–10670. Dangerfield, J. M. 1993. Aggregation in the tropical millipede Alloporus uncinatus (Diplopoda: Spirostreptidae). J. Zool., 230:503–511. Dankittipakul, P., & S. Sonthichai. 2002. Ectoparasitic mites (Acari, Trombiculidae, Rombiculidae) on oplionids (Opiliones, Gagrellidae) in Northern Thailand. Nat. Hist. Bull. Siam, 52:239–243. Danks, H. V. 2002. Modification of adverse conditions by insects. Oikos, 99:10–24. Dannhorn, D. R., & K. A. Seitz. 1986. Ultrastructure and function of the circulatory organs of Leiobunum limbatum and two other species of harvestmen (Arachnida: Opiliones). J. Morphol., 190:93–107. Dannhorn, D. R., & K. A. Seitz. 1987. Hemocytes of Leiobunum limbatum and two other species of harvestmen (Arachnida, Opiliones) morphological classification and functional aspects. J. Morphol., 193:185–196. Daraktchiev, A. 1981. Sur la nourriture des oiseaux de la region Tchernatitza des Rhodopes. Trav. Sci. Univ. Plovdiv “Paissi Hilendarski,” Biol., 19:173–207. [In Bulgarian with summary in French] Darevskiy, I. S. 1953. O poleznoy roli zhivorodyashey yashtericuy v svyazi s voprosom ob ocenke hozyaystvennogo znacheniya yashteric nashey faunuy. Byulleten’ Moskovskogo obshchestva ispytalei priroduy, otdel biologicheskiy, n.s., 58:21–31. Davidson, J. A. 1956. Notes on the food habits of the slimy salamander Plethodon glutinosus glutinosus. Herpetologica, 12:129–131. Davis, N. B. K., & P. E. Jones. 1978. The ground arthropods of some chalk and limestone quarries in England. J. Biogeog., 5:159–171. Davis, N. W. 1937. A cyphophthalmid from South America. (Arachnida, Phalangida). J. New York Entomol. Soc., 45:133–137. Dawydoff, C. 1949. Développement embryonnaire des Arachnides. Pp. 320–385 in Traité de zoologie, vol. 6 (P.-P. Grassé, ed.). Masson et Cie, Paris. de Bivort, B. L., & G. Giribet. 2004. A new genus and species of cyphophthalmid from the Iberian Peninsula with a phylogenetic analysis of the Sironidae (Arachnida, Opiliones, Cyphophthalmi). Invertebr. Syst., 18:7–52. de Graaf, H. W. 1882. Over den bouw der geslachtsorganen bij de Phalangiden. E. J. Brill, Leiden.

534

References

Decleer, K., & R. Segers. 1989. The soil surface active Araneae, Opiliones, Carabidae and Staphylinidae of a wet meadow vegetation subject to dereliction and succession. Biol. Jb., 57:103–119. Delcomyn, F. 1985. Factors regulating insect walking. Ann. Rev. Ent., 30:239–256. Dementjev, G. P., N. A. Gladkov, A. M. Sudilovskaya, E. P. Spantenberg, L. B. Bjome, I. B. Volchanetskij, M. A. Voinstvenskij, N. N. Gorchakovskaja, M. N. Korelov, A. K. Rustamov. 1954. Birds of the Soviet Union. Vol. 5: Passeriformes. Sovetskaja Nauka, Moscow. [In Russian] Dennis, P., M. R. Young, & C. Bentley. 2001. The effects of varied grazing management on epigeal spiders, harvestmen and pseudoscorpions of Nardus stricta grassland in upland Scotland. Agr. Ecosyst. Environ., 86:39–57. Dietrich, A. J. J., & R. J. P. Mulder. 1981. A light microscopic study of the development and behaviour of the synaptonemal complex in spermatocytes of the mouse. Chromosoma, 83:409–418. Dillery, D. G. 1961. Food habits of savannah and grasshopper sparrows in relation to foods available. Ph.D. Thesis, Ohio State University, Columbus. Dimmock, G. 1882. Defensive mimicry in Phalangidae. Psyche, 3:299. Dixon, P. L., & R. G. McKinlay. 1989. Aphid predation by harvestmen in potato fields in Scotland. J. Arachnol., 17:253– 255. Docherty, M., & S. R. Leather. 1997. Structure and abundance of arachnid communities in Scots and lodgepole pine plantations. Forest Ecol. Manag., 95:197–207. Dornbusch, M. 1981. Die Ernährung einiger Kleinvogelarten in Kieferjungbestockungen. Beitr. Vogelk., 27:73–99. Dresco, E. 1966. Recherches sur les Opilions du genre Ischyropsalis (Fam. Ischyropsalidae). I. Les caractères systematiques. II. Ischyropsalis robusta Simon. Bull. Mus. Hist. nat. Paris, ser. 2, 38:586–602. Dresco, E. 1970. Recherches sur la variabilité et la phylogénie chez les Opilions du genre Ischyropsalis C. L. Koch (Fam. Ischyropsalidae), avec création de la famille nouvelle des Sabaconidae. Bull. Mus. Hist. nat. Paris, ser. 2, 41:1200– 1213. Drets, M. E., G. A. Folle, & A. Aznarez. 1982. Clastogenic action of a dimethyl p-benzoquinone of animal origin. Mutat. Res., 102:159–172. Drummond, F., Y. Suhaya, & E. Groden. 1990. Predation on the Colorado potato beetle (Coleoptera: Chrysomelidae) by Phalangium opilio (Opiliones: Phalangidae). J. Econ. Ent., 83:772–778. Duffey, E. 2004. The efficiency of timed hand-collecting combined with a habitat classification versus pitfall trapping

for studies of sand-dune spider faunas. Newsl. Br. Arachnol. Soc., 99:2–4. Duffield, R. M., O. Olubajo, J. W. Wheeler, & W. A. Shear. 1981. Alkylphenols in the defensive secretion of the Nearctic opilionid, Stygnomma spinifera (Arachnida: Opiliones). J. Chem. Ecol., 7:445–452. Dugés, A. 1884. Opilio ischionotatus—segador de ancas manchadas de blanco. Naturaleza, 7:194–197. Dumas, P. C. 1956. The ecological relations of sympatry in Plethodon dunni and Plethodon vehiculum. Ecology, 37:484– 495. Dumitrescu, D. 1974a. Contribution à l’étude de l’appareil digestif (intestin moyen) des opilions (Arachnida). Trav. Mus. Hist. nat. “Grigore Antipa,” 14:95–107. Dumitrescu, D. 1974b. Contribution à l’étude de l’appareil digestif (intestin moyen) des Trogulidae (Arachnida, Opilionida). Trav. Mus. Hist. nat. “Grigore Antipa,” 15:57–67. Dumitrescu, D. 1975a. Contribution à l’étude de l’appareil digestif (intestin moyen) des opilions. Pp. 150–154 in Proceedings of the 6th International Arachnological Congress (1974). Amsterdam. Dumitrescu, D. 1975b. Les glandes salivaires gnathocoxales des opilions (Arachnida). Trav. Mus. Hist. nat. “Grigore Antipa,” 16:121–128. Dumitrescu, D. 1975c. Observations concernant l’appareil digestif (intestin moyen) des opilions appartenant aux families des Sironidae, des Caddidae et des Neopilionidae (Arachnida). Trav. Mus. Hist. nat. “Grigore Antipa,” 16: 115–120. Dumitrescu, D. 1976. Recherches morphologiques sur l’appareil digestif (intestin moyen) des Gonyleptomorphi (Arachnida, Opiliones). Trav. Mus. Hist. nat. “Grigore Antipa,” 17:17–30. Dumitrescu, D. 1980. Recherches sur la morphologie de l’appareil digestif (intestin moyen) des Opilions (Arachnida). Trav. Mus. Hist. nat. “Grigore Antipa,” 21:43–50. Dumortier, B. 1963. Ethological and physiological study of sound emissions of Arthropoda. Pp. 583–654 in Acoustic Behaviour of Animals (R.-G. Busnel, ed.). Elsevier, Amsterdam. Dunlop, J. A. 1996a. Arácnidos fósiles (con exclusión de aranas y escorpiones). Boln SEA, vol. monográfico, 16:77–92. Dunlop, J. A. 1996b. Systematics of the fossil arachnids. Rev. suisse Zool., hors série: 173–184. Dunlop, J. A. 1999. A redescription of the Carboniferous arachnid Plesiosiro madeleyi Pocock, 1911 (Arachnida: Haptopoda). Trans. R. Soc. Edinb., Earth Sci., 90:29–47. Dunlop, J. A. 2004a. The enigmatic fossil arachnid Kustarachne tunuipes Scudder, 1890 is a harvestman. Pp. 17–25 in European Arachnology 2002 (F. Samu & C. Szinetár, eds). Plant Protection Institute & Berzsenyi College, Budapest.

References

Dunlop, J. A. 2004b. A spiny harvestman (Arachnida: Opiliones) from the Upper Carboniferous of Missouri, USA. Pp. 67–74 in European Arachnology 2003. Arthropoda Selecta, Special Issue No. 1 (D. V. Logunov & D. Penney, eds). KKM Scientific Press, Moscow. Dunlop, J. A. 2006. Baltic amber harvestman types (Arachnida: Opiliones: Eupnoi and Dyspnoi). Fossil Record. 9:167–182. Dunlop, J. A., & L. I. Anderson. 2005. A fossil harvestman (Arachnida, Opiliones) from the Misissippian of East Kirkton, Scotland. J. Arachnol., 33:482–489. Dunlop, J. A., L. I. Anderson, H. Kerp, & H. Hass. 2003. Preserved organs of Devonian harvestmen. Nature, 425:916. Dunlop, J. A., L. I. Anderson, H. Kerp, & H. Hass. 2004. A harvestman (Arachnida: Opiliones) from the Early Devonian Rhynie cherts, Aberdeenshire, Scotland. Trans. r. Soc. Edinb., Earth Sci., 94:341–354. Dunlop, J. A., & G. Giribet. 2003. The first fossil cyphophthalmid (Arachnida: Opiliones), from Bitterfeld amber, Germany. J. Arachnol., 31:371–378. Eberhard, W. G. 1996. Female Control: Sexual Selection by Cryptic Female Choice. Monographs in Behavior and Ecology. Princeton University Press, Princeton, NJ. Eberhard, W. G. 2000. Criteria for demonstrating postcopulatory female choice. Evolution, 54:1047–1050. Edgar, A. L. 1960. The biology of the order Phalangida in Michigan. Ph.D. Thesis, University of Michigan, Ann Arbor. Edgar, A. L. 1963. Proprioception in the legs of phalangids. Biol. Bull., 124:262–267. Edgar, A. L. 1971. Studies on the biology and ecology of Michigan Phalangida (Opiliones). Misc. Pub. Mus. Zool., Univ. Mich., 144:1–64. Edgar, A. L. 1990. Opiliones (Phalangida). Pp. 529–581 in Soil Biology Guide (D. L. Dindal, ed.). John Wiley & Sons, New York. Edgar, A. L., & H. A. Yuan. 1968. Daily locomotor activity in Phalangium opilio and seven species of Leiobunum (Arthropoda: Phalangida). Bios, 39:167–176. Edgecombe, G. D., & G. Giribet. 2004. Adding mitochondrial sequence data (16S rRNA and cytochrome c oxidase subunit I) to the phylogeny of centipedes (Myriapoda, Chilopoda): an analysis of morphology and four molecular loci. J. Zool. Syst. Evol. Res., 42:89–134. Edmunds, J., & M. Edmunds. 1986. The defensive mechanisms of orb weavers (Araneae: Araneidae) in Ghana, West Africa. Pp. 73–89 in Proceedings of the 9th International Arachnological Congress (W. G. Eberhard, Y. D. Lubin, & B. C. Robinson, eds.). Smithsonian Institution Press, Washington, DC. Edmunds, M. 1974. Defence in Animals: A Survey of Antipredator Defences. Longman, Harlow.

535

Edney, E. B. 1982. The truth about saturation deficiency—an historical perspective. J. Exp. Zool., 222:205–214. Edwards, R. 1993. Entomological and mammological perspectives on genital differentiation. Trends Ecol. Evol., 8:406– 408. Eggert, A. K., & J. K. Müller. 1997. Biparental care and social evolution in burying beetles: lessons from the larder. Pp. 216–236 in The Evolution of Social Behavior in Insects and Arachnids (J. C. Choe & B. J. Crespi, eds.). Cambridge University Press, Cambridge. Eisenbeis, G., & W. Wichard. 1987. Order: Opiliones-Harvestmen (Arachnida). Pp. 56–75 in Atlas on the Biology of Soil Arthropods (G. Eisenbeis & W. Wichard, eds.). SpringerVerlag, Berlin. Eisner, T., D. Alsop, & J. Meinwald. 1978. Secretions of opilionids, whip scorpions and pseudoscorpions. Pp. 87–99 in Handbook of Experimental Pharmacology (Arthropod Venoms), vol. 48 (S. Bettini, ed.). Springer-Verlag, Berlin. Eisner, T., T. H. Jones, K. Hicks, R. E. Silberglied, & J. Meinwald. 1977. Quinones and phenols in the defensive secretions of neotropical opilionids. J. Chem. Ecol., 3:321–329. Eisner, T., F. Kluge, J. E. Carrel, & J. Meinwald. 1971. Defense of phalangid: liquid repellent administered by leg dabbing. Science, 173:650–652. Eisner, T., C. Rossini, A. González, & M. Eisner. 2004. Chemical defense of an opilionid (Acanthopachylus aculeatus). J. Exp. Zool., 207:1313–1321. Ekpa, O., J. W. Wheeler, J. C. Cokendolpher, & R. M. Duffield. 1984. N,N-dimethyl-␤-phenylethylamine and bornyl esters from the harvestman Sclerobunus robustus (Arachnida: Opiliones). Tetrahedron Lett., 25:1315–1318. Ekpa, O., J. W. Wheeler, J. C. Cokendolpher, & R. M. Duffield. 1985. Ketones and alcohols in the defensive secretion of Leiobunum townsendi Weed and a review of the known exocrine secretions of Palpatores (Arachnida: Opiliones). Comp. Biochem. Physiol., 81B:555–557. Elgar, M. A. 1992. Sexual cannibalism in spiders and other arachnids. Pp. 128–155 in Cannibalism: Ecology and Evolution among Diverse Taxa (M. A. Elgar & B. J. Crespi, eds.). Oxford University Press, Oxford. Elgar, M. A. 1998. Sperm competition and sexual selection in spiders and other arachnids. Pp. 307–339 in Sperm Competition and Sexual Selection (T. R. Birkhead & A. P. Møller, eds.). Academic Press, San Diego. Elgar, M. A., & B. J. Crespi. 1992. Cannibalism: Ecology and Evolution among Diverse Taxa. Oxford University Press, Oxford. Ellis, E. A. 1956. Entomogenous fungi in Norfolk. Trans. Norfolk Norwich Nat. Soc., 18:23–28. Elpino-Campos, A., W. Pereira, K. Del-Claro, & G. Machado. 2001. Behavioural repertory and notes on natural history

536

References

of the Neotropical harvestman Discocyrtus oliverioi (Opiliones: Gonyleptidae). Bul. Br. Arachnol. Soc., 12:144–150. Emlen, S. T., & L. W. Oring. 1977. Ecology, sexual selection, and the evolution of mating systems. Science, 197:215–223. Emmrich, R. 1973. Das Nahrungsspektrum der Dorngrasmucke (Sylvia communis Lath.) in einem Gebusch-Biotop der Insel Hiddensee (Aves, Sylviidae) [I. Teil]. Zool. Abh. Mus. Tierkd. Dresden, 32:275–307. Emmrich, R. 1974. Das Nahrungsspektrum der Dorngrasmucke (Sylvia communis Lath.) in einem Gebusch-Biotop der Insel Hiddensee (Aves, Sylviidae) [II. Teil]. Zool. Abh. Mus. Tierkd. Dresden, 33:9–31. Emmrich, R. 1975a. Zur Nahrungsspektrum und zur Ernährungsbiologie des Gartenrotschwanzes. Beitr. Vogelk., 21:102–110. Emmrich, R. 1975b. Zur Nestlingsnahrung der Heckenbraunelle (Prunella modularis L.). Zool. Abh. Mus. Tierkd. Dresden, 33:245–249. Epstein, D. L., R. S. Zack, & J. F. Brunner. 2000. Effects of broadspectrum insecticides on epigeal arthropod biodiversity in Pacific Northwest apple orchards. Environ. Ent., 29:340–348. Estable, C., M. I. Ardao, N. P. Brasil, & L. F. Fieser. 1955. Gonyleptidine. J. Am. Chem. Soc., 77:4942. Evans, H. E. 1948. Biological notes on two species of Anoplius (Hymenoptera: Pompilidae). Ent. News, 59:180–184. Evans, H. E. 1953. Comparative ethology and the systematics of spider wasps. Syst. Zool., 2:155–172. Ewing, H. E. 1923. Holosiro acaroides, new genus and species: the only New World representative of the mite-like phalangids of the suborder Cyphophthalmi. Ann. Ent. Soc. Am., 16:387–390. Facure, K. G. 1996. Ecologia alimentar do cachorro-do-mato, Cerdocyon thous (Carnivora: Canidae), no Parque Florestal de Itapetinga, município de Atibaia, sudeste do Brasil. M.Sc. Thesis, Universidade Estadual de Campinas, Campinas, Brazil. Fahrenbach, W. H. 1999. Merostomata. Pp. 21–115 in Microscopic Anatomy of Invertebrates, Vol. 8A: (F. W. Harrison & R. F. Foeli, eds.). Wiley-Liss, New York. Fain, A. 1991. Two new larvae of the genus Leptus Latreille, 1796 (Acari, Erythraeidae) from Belgium. Int. J. Acarol., 17:107–111. Fain, A, & F. D’Amico. 1997. Observations on larval mites (Acari) parasitic on Opiliones from the French Pyrenees. Int. J. Acarol., 23:39–48. Farley, R. D. 1984. The ultrastructure of hemocytopoietic organs in the desert scorpion, Paruroctonus. Tissue Cell, 16:577–588. Farley, R. D. 1999. Scorpiones. Pp. 117–222 in Microscopic Anatomy of Invertebrates, vol. 8A: Chelicerate Arthropoda (F. W. Harrison & R. F. Foelix, eds.). Wiley-Liss, New York.

Faussek, V. 1892. On the anatomy and embryology of the Phalangiidae. Ann. Mag. Nat. Hist., 9:397–405. Fellowes, M. D. E. 1998. Do non-social insects get the (kin) recognition they deserve? Ecol. Ent., 23:223–227. Felsenstein, J. 2004. Inferring Phylogenies. Sinauer Associates, Sunderland. Ferdinand, W. 1982. Vergleichende Untersuchungen zur achtbeinigen Lokomotion bei Arthropoden. Ph.D. Thesis, Philipps-Universität, Marburg, Germany. Fieser, L. F., & M. I. Ardao. 1956. Investigation of the chemical nature of gonyleptidine. J. Chem. Ecol., 78:774–781. Firmo, C. L., & R. Pinto-da-Rocha. 2002. A new species of Pseudotrogulus Roewer and assignment of the genus to the Hernandariinae (Opiliones, Gonyleptidae). J. Arachnol., 30:173–176. Firstman, B. 1973. The relationship of the chelicerate arterial system to the evolution of the endosternite. J. Arachnol., 1:1–54. Flechtmann, C. H. W., & C. A. H. Flechtmann. 1984. Reproduction and chromosomes in the broad mite, Polypha gotarsonemus latus (Banks, 1904) (Acari, Prostigmata, Tarsonemidae). Pp. 455–456 in Acarology VI, vol. 1 (D. A. Griffiths & C. E. Bowman, ed.). John Wiley & Sons, New York. Fleishman, E., G. T. Austin, & A. D. Weiss. 1998. An empirical test of Rapoport’s rule: elevational gradients in montane butterfly communities. Ecology, 79:2482–2493. Fleissner, G., & G. Fleissner. 1999. Simple eyes of arachnids. Pp. 55–70 in Atlas of Arthropod Sensory Receptors (E. Eguchi & Y. Tominaga, eds.). Springer-Verlag, Tokyo. Flórez, E., & H. Sanchez. 1995. La diversidad de los arácnidos em Colombia—aproximación inicial. Pp. 327–372 in Colombia, Diversidad Biótica I (O. Rancel, ed.). Instituto de Ciencias Naturales, Inderena, Santafé de Bogotá. Foelix, R. F. 1975. Occurrence of synapses in peripheral sensory nerves of arachnids. Nature, 254:146–148. Foelix, R. F. 1985. Mechano- and chemoreceptive sensilla. Pp. 118–137 in Neurobiology of Arachnids (F. G. Barth, ed.). Springer-Verlag, Berlin. Foelix, R. F. 1996. Biology of Spiders. Oxford University Press, New York. Forster, R. R. 1948a. A new sub-family and species of New Zealand Opiliones. Rec. Auckland Inst. Mus., 3:313–318. Forster, R. R. 1948b. The sub-order Cyphophthalmi Simon in New Zealand. Dom. Mus. Rec. Entomol., 1:79–119. Forster, R. R. 1949. Australian Opiliones. Mem. Nat. Mus. Victoria, 16:59–89. Forster, R. R. 1952. Supplement to the sub-order Cyphophthalmi. Dom. Mus. Rec. Entomol., 1:179–211. Forster, R. R. 1954. The New Zealand harvestmen (sub-order Laniatores). Canterbury Mus. Bull., 2:1–329. Forster, R. R. 1964. The Araneae and Opiliones of the sub-

References

antarctic islands of New Zealand. Pac. Insects Monogr., 7:58–115. Forster, R. R., & L. Forster. 2003. Spiders of New Zealand and Their Worldwide Kin. University of Otago Press & Otago Museum, Dunedin, New Zealand. Fowler, D. J., & J. Gaines. 1984. The interrelationships between serotonin production and locomotion in different light regimes in southwestern Michigan opilionids, Leiobunum longipes. Chronobiologia, 11:1–9. Fowler, D. J., & C. J. Goodnight. 1966. The cyclic production of 5-hydroxitryptamine in the opilionid. Am. Zool., 6:187– 193. Fowler, D. J., & C. J. Goodnight. 1974. Physiological populations of the arachnid, Leiobunum longipes (Opiliones: Phalangiidae). Syst. Zool., 23:219–225. Frank, H. R. 1937. Histologische Untersuchungen über die Verdauung bei Weberknechten. Z. Morphol. Ökol. Tiere, 33:151–164. Franklin, R. F. 1985. The locomotion of hexapods on rough ground. Pp. 69–78 in Insect Locomotion (M. Gewecke & G. Wendler, eds.). Verlag Paul Parey, Berlin. Franz, V. 1904. Über die Struktur des Herzens und die Entstehung von Blutzellen bei Spinnen. Zool. Anz., 27:192–204. Freudenthaler, P. 1994a. Bodenbewohnende Spinnen und Weberknechte aus der Pleschinger Sandgrube bei Linz, Oberösterreich (Arachnida: Aranei, Opiliones). Naturkd. Jahrb. Stadt Linz, 37/39:393–427. Freudenthaler, P. 1994b. Epigäische Spinnen und Weberknechte an zwei Standorten im Bereich der “Linzer Pforte”, Oberösterreich (Arachnida: Aranei, Opiliones). Naturkd. Jahrb. Stadt Linz, 37/39:379–392. Freudenthaler, P. 1999. Epigäische Spinnen und Weberknechte zweier Blockschutt-Habitate im Ranna-Tal, Oberösterreich (Arachnida: Aranea, Opiliones). Beitr. Naturk. Oberösterreichs, 7:143–152. Freyre, H. A., M. Rovira, & M. I. Ardao. 1958. Toxicidad de metil1,4 benzoquinonas y metil-1,4 benzohidroquinonas. Archiv. Soc. Biol. Montevideo, 24:82–88. Friebe, B., & J. Adis. 1983. Entwicklungzyklen von Opiliones (Arachnida) im Schwarzwasser-Überschwemmungswald (Igapó) des Rio Tarumã Mirim (Zentralamazonien, Brasilien). Amazoniana, 8:101–110. Friedlander, C. P. 1965. Aggregation in Oniscus asellus. Anim. Behav., 13:342–346. Fritsch, A. 1904. Palaeozoische Arachniden. Eduard Grégar, Prague. Full, R. 1989. Mechanics and energetics of terrestrial locomotion: bipeds to polypeds. Pp. 175–182 in Energy Transformations in Cells and Organisms (W. Wieser & E. Gnaiger, eds.). Georg Thieme Verlag, Stuttgart. Gabe, M. 1954. Situations et connexions des cellules neu-

537

rosécrétices chez Phalangium opilio L. C. r. Acad. Sci., Paris, ser. D, 238:2450–2452. Gabe, M. 1955. Données histologiques sur la neurosécrétion chez les arachnides. Archives d’Anatomie Microscopique et de Morphologie Experimentale, 44:351–383. Gabrys, G. 1991. New data on the distribution and hosts of larvae of Erythraeidae (Acari, Actinedida) in Poland. Wiad. Parazytol., 37:103–105. Gajdos, P., & A. Kristín. 1997. Spiders (Araneae) as bird food. Pp. 91–105 in Proceedings of the 16th European Colloquium of Arachnology (M. M. Zabka, ed.). Siedlce, Poland. Ganya, I. M., & N. I. Zubkov. 1988. Adaptaciya ptic k usloviyam antropogennoy sreduyi. Pp. 34–55 in Adaptatsiia ptits i mlekopitaiushchikh k antropogennomu landshaftu (I. V. Averin, ed.). Institut zoologii i fiziologii, Akademiia de Shtiintse a RSSM, Kishinev, “Shtiintsa.” Gaubert, M. 1892. Sur un ganglion nerveux des pattes du Phalangium opilio. C. r. Acad. Sci., Paris, 115:960. Gervais, P. 1849. Falángidos. Pp. 18–28 in Historia Física y Política de Chile, vols. 3–4: Zoología (C. Gay, ed.). Paris. Gibson, G. A. P., J. T. Huber, & J. B. Woolley. 1997. Annotated Keys to the Genera of Nearctic Chalcidoidea (Hymenoptera). NCR Research, Ottawa. Giribet, G. 1997. Filogenia molecular de artrópodos basada en la secuencia de genes ribosomales. Ph.D. Thesis, Universitat de Barcelona, Barcelona, Spain. Giribet, G. 2000. Catalogue of the Cyphophthalmi of the world (Arachnida, Opiliones). Rev. Ibér. Aracnol., 2:49–76. Giribet, G. 2002. Stylocellus ramblae, a new stylocellid (Opiliones, Cyphophthalmi) from Singapore, with a discussion of the family Stylocellidae. J. Arachnol., 30:1–9. Giribet, G. 2003. Karripurcellia, a new pettalid genus (Arachnida, Opiliones, Cyphophthalmi) from Western Australia with a cladistic analysis of the family Pettalidae. Invertebr. Syst., 17:387–406. Giribet, G., & S. L. Boyer. 2002. A cladistic analysis of the cyphophthalmid genera (Opiliones, Cyphophthalmi). J. Arachnol., 30:110–128. Giribet, G., & J. A. Dunlop. 2005. First identifiable Mesozoic harvestmen (Opiliones: Dyspnoi) from Cretaceous Burmese amber. Proc. R. Soc. B, 272:1007–1013. Giribet, G., & G. D. Edgecombe. 2006. Conflict between data sets and phylogeny of centipedes: an analysis based on seven genes and morphology. Proceedings: Biological Sciences, 273:531–538. Giribet, G., G. D. Edgecombe, W. C. Wheeler, & C. Babbitt. 2002. Phylogeny and systematic position of Opiliones: a combined analysis of chelicerate relationships using morphological and molecular data. Cladistics, 18:5–70. Giribet, G., & C. E. Prieto. 2003. A new Afrotropical Ogovea (Opiliones, Cyphophthalmi) from Cameroon, with a dis-

538

References

cussion on the taxonomic characters in the family Ogoveidae. Zootaxa, 329:1–18. Giribet, G., M. Rambla, S. Carranza, M. Riutort, J. Baguñà, & C. Ribera. 1999. Phylogeny of the arachnid order Opiliones (Arthropoda) inferred from a combined approach of complete 18S, partial 28S ribosomal DNA sequences and morphology. Mol. Phylog. Evol., 11:296–307. Giribet, G., & W. C. Wheeler. 1999. On gaps. Mol. Phylog. Evol., 13:132–143. Glutz von Blotzheim, U. N., & K. M. Bauer. 1980. Handbuch der Vögel Mitteleuropas. Vol. 9: Columbiformes-Piciformes (3). Akademische Verlagsgesellschaft, Wiesbaden. Glutz von Blotzheim, U. N., & K. M. Bauer. 1982. Handbuch der Vögel Mitteleuropas. Vol. 8/I: Charadriiformes (3). Akademische Verlagsgesellschaft, Wiesbaden. Glutz von Blotzheim, U. N., & K. M. Bauer. 1988a. Handbuch der Vögel Mitteleuropas. Vol. 11/I: Passeriformes (2). AULAVerlag, Wiesbaden. Glutz von Blotzheim, U. N., & K. M. Bauer. 1988b. Handbuch der Vögel Mitteleuropas. Vol. 11/II: Passeriformes (2). AULAVerlag, Wiesbaden. Glutz von Blotzheim, U. N., K. M. Bauer, & E. Bezzel. 1973. Handbuch der Vögel Mitteleuropas. Vol. 5: Galliformes und Gruiformes. Akademische Verlagsgesellschaft, Wiesbaden. Gnaspini, P. 1995. Reproduction and postembryonic development of Goniosoma spelaeum, a cavernicolous harvestman from southeastern Brazil (Arachnida: Opiliones: Gonyleptidae). Invertebr. Reprod. Dev., 28:137–151. Gnaspini, P. 1996. Population ecology of Goniosoma spelaeum, a cavernicolous harvestman from southeastern Brazil (Arachnida: Opiliones: Gonyleptidae). J. Zool., 239:417–435. Gnaspini, P. 1999. The use of morphometric characteristics for the recognition of species among Goniosomatinae harvestmen (Arachnida, Opiliones, Gonyleptidae). J. Arachnol., 27:129–134. Gnaspini, P., & A. J. Cavalheiro. 1998. Chemical and behavioral defenses of a Neotropical cavernicolous harvestman Goniosoma spelaeum. J. Arachnol., 26:81–90. Gnaspini, P., F. H. Santos, & S. Hoenen. 2003. The occurrence of different phase angles between contrasting seasons in the activity patterns of the cave harvestman Goniosoma spelaeum (Arachnida, Opiliones). Biol. Rhythm Res., 34:31–49. Gnaspini, P., M. B. da Silva, & F. C. Pioker. 2004. The occurrence of two adult instars among Grassatores (Arachnida: Opiliones)—a new type of life cycle in arachnids. Invertebr. Reprod. Dev., 45:29–39. Gnaspini-Netto, P. 1993. Biologia de opiliões cavernícolas da Província Espeleológica do Vale do Ribeira, SP/PR (Arachnida: Opiliones). Ph.D. Thesis, Universidade de São Paulo, Instituto de Biociências, São Paulo, Brazil.

Goloboff, P. A., J. S. Farris, & K. Nixon. 2003. TNT: Tree Analysis Using New Technology. Version 1.0. Program and documentation available at http://www.zmuc.dk/public/ phylogeny/TNT/ González, A., C. Rossini, & T. Eisner. 2004. Mimicry: imitative depiction of discharged defensive secretion on carapace of an opilionid. Chemoecology, 14:5–7. González-Sponga, M. A. 1987. Arácnidos de Venezuela: Opiliones Laniatores I. Familias Phalangodidae y Agoristenidae. Academia de Ciencias Físicas, Matemáticas y Naturales, Caracas. González-Sponga, M. A. 1992a. Arácnidos de Venezuela: Nueva espécie del gênero Acropsopilio de la Cordillera de la Costa (Caddidae). Bol. Acad. Cienc. Fís. Mat. Nat., 52:43– 51. González-Sponga, M. A. 1992b. Arácnidos de Venezuela: Opiliones Laniatores II. Familia Cosmetidae. Academia de Ciencias Físicas, Matemáticas y Naturales, Caracas. González-Sponga, M. A. 1997. Arácnidos de Venezuela: Una nueva familia, dos nuevos géneros y dos nuevas especies de Opiliones Laniatores. Acta Biol. Venez., 17:51–58. Goodier, R. 1970. Notes on mountain spiders from Wales. I. Spiders caught in pitfall trap on the Snowdon National Nature Reserve. Bul. Br. Arachnol. Soc., 1:85–87. Goodnight, C. J. 1958. Two representatives of a tropical suborder of opilionids (Arachnida) found in Indiana. Proc. Indiana Acad. Sci., 67:322–323. Goodnight, C. J., & M. L. Goodnight. 1942a. New Phalangodidae (Phalangida) from the United States. Am. Mus. Novit., 1188:1–18. Goodnight, C. J., & M. L. Goodnight. 1942b. Phalangida from Mexico. Am. Mus. Novit., 1211:1–18. Goodnight, C. J., & M. L. Goodnight. 1942c. Phalangids from Central America and the West Indies. Am. Mus. Novit., 1184:1–23. Goodnight, C. J., & M. L. Goodnight. 1943. Three new phalangids from Tropical America. Am. Mus. Novit., 1228:1–4. Goodnight, C. J., & M. L. Goodnight. 1944. More phalangida from Mexico. Am. Mus. Novit., 1249:1–13. Goodnight, C. J., & M. L. Goodnight. 1945. Phalangida from the United States. J. New York Entomol. Soc., 53:239–245. Goodnight, C. J., & M. L. Goodnight. 1946. Additional studies of the phalangid fauna of Mexico. 1. Am. Mus. Novit., 1310:1–17. Goodnight, C. J., & M. L. Goodnight. 1951. The genus Stygnomma (Phalangida). Am. Mus. Novit., 1491:1–20. Goodnight, C. J., & M. L. Goodnight. 1953a. The opilionid fauna of Chiapas, Mexico, and adjacent areas (Arachnoidea, Opiliones). Am. Mus. Novit., 1610:1–81. Goodnight, C. J., & M. L. Goodnight. 1953b. Taxonomic recognition of variation in Opiliones. Syst. Zool., 2:173–179.

References

Goodnight, C. J., & M. L. Goodnight. 1960. Speciation among cave opilionids of the United States. Am. Mid. Nat., 64:34– 38. Goodnight, C. J., & M. L. Goodnight. 1976. Observations on the systematics, development and habits of Erginulus clavotibialis (Opiliones: Cosmetidae). Trans. Am. micr. Soc., 95:654–664. Goodnight, C. J., & M. L. Goodnight. 1980. Metagovea philipi, n.sp., a new cyphophthalmid (Arachnida) from Ecuador. Trans. Am. micr. Soc., 99:128–131. Goodnight, C. J., & M. L. Goodnight. 1983. Opiliones of the family Phalangodidae found in Costa Rica. J. Arachnol., 11:201–242. Gorlov, I. P., O. Y. Gorlova, & D. V. Logunov. 1995. Cytogenetic studies on Siberian spiders. Hereditas, 122:211–220. Gorlov, I. P., & N. Tsurusaki. 2000a. Analysis of the phenotypic effects of B chromosomes in a natural population of Metagagrella tenuipes (Arachnida: Opiliones). Heredity, 84:209–217. Gorlov, I. P., & N. Tsurusaki. 2000b. Morphology and meiotic/mitotic behavior of B chromosomes in a Japanese harvestman, Metagagrella tenuipes (Arachnida: Opiliones): no evidence for B accumulation mechanisms. Zool. Sci., 17:349–355. Gorlov, I. P., & N. Tsurusaki. 2000c. Staggered clines in a hybrid zone between two chromosome races of the harvestman Gagrellopsis nodulifera (Arachnida: Opiliones). Evolution, 54:176–190. Gorlova, O. Y., I. P. Gorlov, E. Nevo, & D. V. Logunov. 1997. Cytogenetic studies on seventeen spider species from Israel. Bul. Br. arachnol. Soc., 10:249–252. Gourret, P. 1886. Recherches sur les arachnides Tertiares d’Aix en Provence. Rec. zool. suisse, 4:431–496. Grainge, C. A., & R. G. Pearson. 1966. Cuticular structure in the Phalangida. Nature, 211:866. Grainger, J. P., & J. S. Fairley. 1978. Studies on the biology of the pygmy shrew Sorex minutus in the west of Ireland. J. Zool., 186:109–141. Grandcolas, P. 1998. The evolutionary interplay of social behavior, resource use and anti-predator behavior in Zetoborinae + Blaberinae + Gyninae + Diplopterinae cockroaches: a phylogenetic analysis. Cladistics, 14:117–127. Gravenhorst, J. L. C. 1835. Bericht der entomologische Section. Uebersicht der Arbeiten und Veränderungen der Schleisischen Gesellschaft für vaterländische Kultur, 1834:88–95. Green, J. 1999. Sampling method and time determines composition of spider collections. J. Arachnol., 27:176–182. Greenstone, M. H., C. M. Ignoffo, & R. A. Samson. 1988. Susceptibility of spider species to fungus Nomuraea atypicola. J. Arachnol., 15:266–268. Gregory, K. M. 1994. Palaeoclimate and palaeoelevation of the 35 MA Florissant Flora, Front Range, Colorado. Palaeoclimates, 1:23–57.

539

Grimaldi, D., M. S. Engel, & P. Nascimbene. 2002. Fossiliferous Cretaceous amber from Burma (Myanmar): its rediscovery, biotic diversity and paleontological significance. Am. Mus. Novit., 3361:1–71. Gruber, J. 1968. Ergebnisse zoologischer Sammelreisen in der Türkei: Calathocratus beieri, ein neuer Trogulide aus Anatolien (Opiliones, Arachnida). Annln naturh. Mus. Wien, 72:435–441. Gruber, J. 1969a. Bemerkungen zur Genitalmorphologie und systematischen Stellung Metopilio australis (Banks) (Phalangiidae: Opiliones, Arachnida). Annln naturh. Mus. Wien, 73:271–274. Gruber, J. 1969b. Über Stridulationsorgane bei einem Ischyropsalididen: Ceratolasma tricantha Goodnight & Goodnight (Opiliones, Arachnida). Anz. österr. Akad. Wiss., Math.-Naturwiss., 11:1–7. Gruber, J. 1970. Die “Nemastoma”—Arten Nordamerikas (Ischyropsalididae, Opiliones, Arachnida). Annln naturh. Mus. Wien, 74:129–144. Gruber, J. 1974. Ein Beitrag zur Systematik, Morphologie und Bionomie der Gattung Dicranolasma Soerensen (Arachnida: Opiliones). Ph.D. Thesis, Universität Wien, Vienna. Gruber, J. 1975. Bemerkungen zur Morphologie und systematischen Stellung von Caddo, Acropsopilio und verwandter Formen (Opiliones, Arachnida). Annln naturh. Mus. Wien, 78:237–259. Gruber, J. 1976. Ergebnisse zoologischer Sammelreisen in der Türkei: Zwei neue Nemastomatidenarten mit Stridulationsorganen, nebst Anmerkungen zur systematischen Gliederung der Familie (Opiliones, Arachnida). Annln naturh. Mus. Wien, 80:781–801. Gruber, J. 1978. Redescription of Ceratolasma tricantha Goodnight and Goodnight, with notes on the family Ischyropsalidae (Opiliones, Palpatores). J. Arachnol., 6:105–124. Gruber, J. 1979. Ergebnisse zoologischer Sammelreisen in der Türkei: Über Nemastomatiden-Arten aus der Verwandtschaft von Pyza aus Südwestasien und Südosteuropa (Opiliones, Arachnida). Annln naturh. Mus. Wien, 82:559–577. Gruber, J. 1993. Beobachtungen zur Ökologie und Biologie von Dicranolasma scabrum (Herbst) (Arachnida: Opiliones). Teil I. Annln naturh. Mus. Wien, 94/95B:393–426. Gruber, J. 1996. Beobachtungen zur Ökologie und Biologe von Dicranolasma scabrum (Herbst, 1799). Teil II. Fortpflanzung, Entwicklung und Wachstum. Annln naturh. Mus. Wien, 98B:71–110. Gruber, J. 1998. Beiträge zur Systematik der Gattung Dicranolasma (Arachnida: Opiliones, Dicranolasmatidae). I. Dicranolasma thracium Starega und verwandte Formen aus Südosteuropa und Südwestasien. Annln naturh. Mus. Wien, 100B:489–537.

540

References

Gruber, J. 2003. Origin and gender of the name Sabacon Simon, 1879 (Opiliones, Palpatores, Ischyropsalidoidea). Newsl. Br. Arachnol. Soc., 96:6. Gruber, J., & G. S. Hunt. 1973. Nelima doriae (Canestrini), a south European harvestman in Australia and New Zealand (Arachnida, Opiliones, Phalangiidae). Rec. Aust. Mus., 28:383–392. Gruber, J., & J. Martens 1968. Morphologie, Systematik und Ökologie der Gattung Nemastoma C. L. Koch (s.str.) (Opiliones, Nemastomatidae). Senckenbergiana Biol., 49:137–172. Gueutal, J. 1943. Du développement postembryonnaire de Phalangium opilio L. Bull. Soc. zool. Fr., 68:98–100. Gueutal, J. 1944a. De l’éclosion chez un opilion: Phalangium opilio L. Bull. Soc. zool. Fr., 69:24–26. Gueutal, J. 1944b. La ponte chez un opilion: Phalangium opilio Linné. Revue fr. ent., 11:6–9. Guffey, C. 1998. The behavioral ecology of two species of harvestmen (Arachnida: Opiliones): the effects of leg autotomy, parasitism by mites, and aggregation (Leiobunum nigripes, Leiobunum vittatum). Ph.D. Thesis, University of Southwestern Louisiana, Lafayette. Guffey, C. 1999. Costs associated with leg autotomy in the harvestmen Leiobunum nigripes and Leiobunum vittatum (Arachnida: Opiliones). Canad. J. Zool., 77:824–830. Guffey, C. V. R. Townsend Jr., & B. E. Felgenhauer. 2000. External morphology and ultrastructure of the prehensile region of the legs of Leiobuunum nigripes (Arachnida, Opiliones). J. Arachnol., 28:231–236. Guseinov, E. F. 2004. Prey composition of three Thanatus species (Philodromidae, Araneae): indication of relationship between psammophily and myrmecophagy. Pp. 103– 108 in Proceedings of the 20th European Colloquium of Arachnology (F. Samu & C. Szinetár, eds.). Plant Protection Institute & Berzsenyi College, Budapest. Gupta, A. P. 1983. Neurohemal Organs of Arthropods. Charles C. Thomas, Springfield, IL. Hackman, W. 1948. Chromosomenstudien an Araneen mit besonderer Berücksichtigung der Geschlechtschromosomen. Acta zool. fenn., 54:1–87. Hadley, N. F. 1990. Environmental physiology. Pp. 321–340 in The Biology of Scorpions (G. A. Polis, ed.). Stanford University Press, Stanford, CA. Hadley, N. F. 1994. Water Relations of Terrestrial Arthropods. Academic Press, San Diego. Hadzi, J. 1928. Opilioni Schmidtove zbirke: Prilog poznavanju slovenackih opilionida. Glasnik Muzejskega drustva za Slovenijo, 7–8:1–49. Hadzi, J. 1935. Ein eigentümlicher neuer Hölen-Opilionid aus Nord-Amerika, Cladonychium corii g.n. sp.n. Biologia gen., 11:49–72.

Hadzi, J. 1942. Raziskovanja o ishiropsalih (Opiliones). Razprave Matematicno-prirodoslovnega Razreda Akademije Znanosti in Umetnosti v Ljubljani, 2:5–114. Hadzi, J. 1954. Nadaljnja raziskavanja o ishiropsalidih (Opiliones). Slovenska Akad. Znanosti in Umetnosti, 2:141–196. Hadzi, J. 1973. Novi taksoni suhih juzin (Opilionidea) v Jugoslaviji. Slovenska Akad. Znanosti in Umetnosti, 16:1–120. Haggag, G., & Y. Fouad. 1965. Nitrogenous excretion in Arachnids. Nature, 207:1004–1005. Hågvar, S., & E. Østbye. 1976. Food habits of the meadow pipit, Anthus pratensis (L.), in alpine habitats at Hardangervidda, south Norway. Norweg. J. Zool., 24:53–64. Haitlinger, R. 1990. Two new species of Leptus Latreille, 1796 (Acari, Prostigmata, Erythraeidae) from Tenebrionidae (Coleoptera) with a key to European and North African species. Pol. Pismo Ent., 60:45–58. Halaj, J., & A. B. Cady. 2000. Diet composition and significance of earthworms as food of harvestmen (Arachnida: Opiliones). Am. Mid. Nat., 143:487–491. Hall, R. J. 1976. Summer foods of the salamander, Plethodon wehrlei (Amphibia, Urodela, Plethodontidae). J. Herpetol., 10:129–131. Hamilton, W. D. 1971. The geometry for the selfish herd. J. Theor. Biol., 31:295–311. Hancock, A. J., & D. M. Rowell. 1995. A chromosomal hybrid zone in the Australian huntsman spider, Delena cancerides (Araneae: Sparassidae). Aust. J. Zool., 43:173–180. Hansen, H. J. 1893. Organs and characters in different orders of arachnids. Ent. Medd., 4:137–251. Hansen, H. J. 1921. Studies on Arthropoda I: The Pedipalpi, Ricinulei, and Opiliones (Exc. Op. Laniatores) Collected by Mr. Leonardo Fea in Tropical West Africa and Adjacent Islands. Gyldendalske Boghandel, Copenhagen. Hansen, H. J., & W. Sørensen. 1904. On Two Orders of Arachnida: Opiliones, Especially the Suborder Cyphophthalmi, and Ricinulei, Namely the Family Cryptostemmatoidae. Cambridge University Press, Cambridge. Hanström, B. 1923. Further notes on the central nervous system of arachnids: scorpions, phalangids, and trap-door spiders. J. Comp. Neurol., 35:249–272. Hara, M. R., A. J. Cavalheiro, P. Gnaspini, & D. Y. A. C. Santos. 2005. A comparative analysis of the chemical nature of defensive secretions of Gonyleptidae (Arachnida: Opiliones: Laniatores). Biochem. Syst. Ecol., 33:1210– 1225. Hara, M. R., & P. Gnaspini, 2003. Comparative study of the defensive behavior and morphology of the gland opening area among harvestmen (Arachnida, Opiliones, Gonyleptidae) under a phylogenetic perspective. Arthrop. Struct. Dev., 32:257–275.

References

Hara, M. R., P. Gnaspini, & G. Machado. 2003. Male guarding behavior in the Neotropical harvestman Ampheres leucopheus (Mello-Leitão, 1922) (Opiliones, Laniatores, Gonyleptidae). J. Arachnol., 31:441–444. Hartmann, T., H. Häggström, C. Theuring, R. Lindigkeit, & M. Rahier. 2003. Detoxification of pyrrolizidine alkaloids by the harvestman Mitopus morio (Phalangidae), a predator of alkaloid defended leaf beetles. Chemoecology, 13:123–127. Harvey, M. S. 2002. The neglected cousins: what do we know about the smaller arachnid orders? J. Arachnol., 30:357– 372. Haupt, H. 1956. Beitrag zu Kenntnis der eözanen Arthropodenfauna des Gieseltales. Nova Acta Leop., n.s., 128:1–90. Haupt, H. 1957. Eine spinnenartige Arthropode aus dem Rotligenden: Rhabdotarachnoides simoni n.gen. n.sp. Hallesches Jahrbuch für mitteldeutsche Erdgeschichte, 2:246–247. Haupt, J. 2000. Fungal and rickettsial infections of some East Asian trapdoor spiders. Pp. 45–49 in European Arachnology 2000 (S. Toft & N. Scharff, eds.). Aarhus University Press, Aarhus, Denmark. Haws, P. 1995. Getting to know spiders. J. Pestic. Reform, 15:22–23. Heath, E. F. 1914. A phalangid drinks milk. Canad. Ent., 46:120. Hebling-Beraldo, M. J. A., & E. G. Mendes. 1980. The respiratory metabolism of Discocyrtus pectinifemur Mello-Leitão, 1937 (Opiliones, Gonyleptidae): The influence of size, sex and temperature. Bol. Fisiol. Anim., 4:123–132. Hebling-Beraldo, M. J. A., & E. G. Mendes. 1982. Tolerance to vapour pressure deficits and thermal preferences in Discocyrtus pectinifemur Mello-Leitão, 1937 (Opiliones, Gonyleptidae). Bol. Fisiol. Anim., 6:57–71. Heck, K. L., Jr., C. Van Belle, & D. Simberloff. 1975. Explicit calculation of the rarefaction diversity measurement and the determination of sufficient sample size. Ecology, 56:1459– 1461. Helle, W., H. R. Bolland, S. H. M. Jeurissen, & G. A. van Seventer. 1984. Chromosome data on the Actinedida, Tarsonemida and Oribatida. Pp. 449–454 in Acarology VI, vol. 1 (D. A. Griffiths & C. E. Bowman, ed.). John Wiley & Sons, New York. Helle, W., & Pijnacker, L. P. 1985. Parthenogenesis, chromosomes and sex. Pp. 129–139 in World Crop Pests: Spider Mites; Their Biology, Natural Enemies and Control., vol. 1A (W. Helle & M. W. Sabelis, ed.). Elsevier, Amsterdam. Henking, H. 1886. Unterschungen über die Entwicklung der Phalangiden. Part I. Z. wiss. Zool., 45:86–175. Henking, H. 1888. Biologische Beobachtungen an Phalangiden. Zool. Jb., Abt. Syst., 3:319–335. Herlant-Meewis, H., & J. Naisse. 1957. Phénomènes neu-

541

rosécrétoires et glandes endocrines chez les opilions. C. r. Acad. Sci., Paris, ser. D, 245:858–860. Hewitt, G. M., T. M. East, & M. W. Shaw. 1987. Sperm dysfunction produced by B-chromosomes in the grasshopper Myrmeleotettix maculatus. Heredity, 58:59–68. Heymons, R. 1915. Die Vielfüßler, Insekten und Spinnenkerfe. Brehms Tierleben, Leipzig. Band 2. Hickman, V. V. 1958. Some Tasmanian harvestmen of the family Triaenonychidae (sub-order Laniatores). Pap. Proc. R. Soc. Tasman., 92:1–116. Hicks, B. J., F. McKenzie, D. Cosens, & A. D. Watt. 2003. Harvestmen abundance and diversity within lodgepole and Scots pine plantations of Scotland and their impact on pine beauty moth populations. Forest Ecol. Manag., 182:355–361. Hillis, D. M., C. Moritz, & B. K. Mable. 1996. Molecular Systematics. Sinauer Associates, Sunderland. Hillyard, P. D. 1981. Coleosoma floridanum Banks (Araneae: Theridiidae) and Boeorix manducus Thorell (Opiliones: Assamiidae): two tropical arachnids in botanical gardens. Newsl. Br. Arachnol. Soc., 31:3–4. Hillyard, P. D., & J. H. P. Sankey. 1989. Harvestmen: keys and notes for the identification of the species. Pp. 1–119 in Synopses of the British Fauna, no. 4 (D. M. Kermack & R. S. K. Barnes, eds.). E. J. Brill, Leiden. Hinton, B. E. 1938. A key to the genera of the suborder Cyphophthalmi with a description and figures of Neogovea immsi, gen. et sp.n. (Arachnida, Opiliones). Ann. Mag. Nat. Hist., ser. 11, 2:331–338. Hippa, H., S. Koponen, & R. Mannila. 1984. Invertebrates of Scandinavian caves. I. Araneae, Opiliones and Pseudoscorpionida (Arachnida). Annls ent. fenn., 50:23–29. Hoenen, S., & P. Gnaspini. 1999. Activity rhythms and behavioral characterization of two epigean and one cavernicolous harvestmen (Arachnida, Opiliones, Gonyleptidae). J. Arachnol., 27:159–164. Höfer, A. M., S. F. Perry, & A. Schmitz. 2000. Respiratory system of arachnids II: morphology of the tracheal system of Leiobunum rotundum and Nemastoma lugubre (Arachnida, Opiliones). Arthrop. Struct. Dev., 29:13–21. Hoffman, R. L. 1963. A new phalangid of the genus Siro from Eastern United States, and taxonomic notes on other American sironids (Arach., Opiliones). Senckenbergiana biologica, 44:129–139. Hoheisel, U. 1980. Anatomie und taxonomische Bedeutung der Legerohre der Opiliones. Pp. 315–318 in Proceedings of the 8th International Congress of Arachnology (J. Gruber, ed.). Verlag H. Egermann, Vienna. Holisová, V., & R. Obrtel. 1979. The food eaten by Clethrionomys glareolus in a spruce monoculture. Folia Zool., 28:219–230.

542

References

Holland, B., & W. R. Rice. 1998. Chase-away sexual selection: antagonistic seduction versus resistance. Evolution, 52:1– 7. Hölldobler, B. 1977. Communication in social Hymenoptera. Pp. 418–471 in How Animals Communicate (T. A. Sebeok, ed.). Indiana University Press, Bloomington. Holm, Å. 1947. On the development of Opilio parietinus Deg. Zool. bidrag Uppsala, 25:409–422. Holmberg, R. G. 1970. The odoriferous glands of some Palpatores Phalangida (Opiliones) (Arachnida). M.Sc. Thesis, University of Saskatchewan, Saskatoon, Canada. Holmberg, R. G. 1986. The scent glands of Opiliones: a review of their function. Pp. 131–133 in Proceedings of the 9th International Arachnological Congress (W. G. Eberhard, Y. D. Lubin, & B. C. Robinson, eds.). Smithsonian Institution Press, Washington, DC. Holmberg, R. G., N. Angerilli, & L. Lacase. 1984. Overwintering aggregations of Leiobunum paessleri in caves and mines (Arachnida, Opiliones). J. Arachnol., 12:195–204. Holmberg, R. G., & J. C. Cokendolpher. 1997. Re-description of Togwoteeus biceps (Arachnida, Opiliones, Sclerosomatidae) with notes on its morphology, karyology and phenology. J. Arachnol., 25:229–244. Holmgren, N. 1916. Zur vergleichenden Anatomie des Gehirns von Polychaeten, Onychophoren, Xiphosuren, Arachniden, Crustaceen, Myriapoden und Insecten. Bihang Till K. Svenska Vet.-Akad. Handlingar, 56:1–303. Hooke, R. 1665. Micrographia. London. Hope, F. W. 1837. On a new Arachnida, uniting the genera Gonyleptes and Phalangium. Trans. Linn. Soc. Lond. Zool., 17:397–399. Hopkin, S. P. 1989. Ecophysiology of Metals in Terrestrial Invertebrates. Elsevier Applied Science, London. Horner, B. E., J. M. Taylor, & H. A. Padykula. 1965. Food habits and gastric morphology of the grasshopper mouse. J. Mammal., 45:513–535. Houston, W. W. K. 1973. The food of the common frog Rana temporaria, on high moorland in northern England. J. Zool., 171:153–165. Hristova, T. 1962. Prouchvane na biologiyata i ekologiyata na bezopashati zemnovodni (Anura) kato vrediteli v durzhavnoto ribovudno stopanstvo—Chelopechene. Annuaire de l’Université de Sofia, Faculté de Biologie, Géologie et Géographie, livre 1, Biologie (Zoologie), 54/55:247–301. Huelsenbeck, J. P., & F. Ronquist. 2001. MrBayes: Bayesian inference of phylogenetic trees. Biometrics, 17:754–755. Humber, R. A., & K. S. Hansen. 2001. Index: Isolates Listed by Fungus, Geographical Origin, and Host (Host-LocationFungus). ARSEF USDA-ARS Collection of Entomopathogenic Fungal Cultures, Ithaca, NY. Hunt, G. S. 1972. A new cavernicolous harvestman from

Western Australia (Arachnida: Opiliones: Triaenonychidae). J. Aust. ent. Soc., 11:232–236. Hunt, G. S. 1979. Male dimorphism and geographic variation in the genus Equitius Simon (Arachnida, Opiliones). Ph.D. Thesis, University of New South Wales, Sidney, Australia. Hunt, G. S. 1985. Taxonomy and distribution of Equitius in Eastern Australia (Opiliones, Laniatores, Triaenonychidae). Rec. Aust. Mus., 36:107–125. Hunt, G. S. 1990a. Hickmanoxyomma, a new genus of cavernicolous harvestmen from Tasmania (Opiliones: Triaenonychidae). Rec. Aust. Mus., 42:45–68. Hunt, G. S. 1990b. Taxonomic value of spiracle microstructure in the Megalopsalididae (Opiliones, Phalangioidea). Acta zool. fenn., 190:187–194. Hunt, G. S. 1991. Harvestmen (Opiliones) in arid and semi-arid Australia. Aust. Arachnol., 41:3–5. Hunt, G. S. 1992. Revision of the genus Holonucia Forster (Arachnida, Opiliones, Triaenonychidae) with description of cavernicolous and epigean species from eastern Australia. Rec. Aust. Mus., 44:135–163. Hunt, G. S. 1993. A new cavernicolous harvestman from lava tube caves in tropical Australia (Arachnida: Opiliones: Phalangodidae). Mem. Queensland Mus., 33:217–219. Hunt, G. S., & J. C. Cokendolpher. 1991. Ballarinae, a new subfamily of harvestmen from the Southern Hemisphere (Arachnida, Opiliones, Neopilionidae). Rec. Aust. Mus., 43:131–169. Hunt, G. S., & J. L. Hickman. 1993. A revision of the genus Lomanella Pocock and its implications for family level classification in the Travunioidea (Arachnida: Opiliones: Triaenonychidae). Rec. Aust. Mus., 45:81–119. Hutchison, V. H. 1958. The distribution and ecology of the cave salamander, Eurycea lucifuga. Ecol. Monogr., 28:1–20. Huzita, M. 1936. On the feeding habit of few Opiliones. Acta arachnol., 1:103–105. [In Japanese] Immel, V. 1954. Zur Biologie und Physiologie von Nemastoma quadripunctatum (Opiliones, Dyspnoi). Zool. Jb., Abt. Syst., 83:129–184. Immel, V. 1955. Einige Bemerkungen zur Biologie von Platybunus bucephalus (Opiliones, Eupnoi). Zool. Jb., Abt. Syst., 83:475–484. Inman, A. J., & J. Krebs. 1987. Predation and group living. Trends Ecol. Evol., 2:31–32. International Commission on Zoological Nomenclature. 1999. International Code of Zoological Nomenclature. 4th ed. International Trust for Zoological Nomenclature, London. Iturralde-Vinent, M. A., & R. D. E. MacPhee. 1996. Age and palaeogeographical origin of Dominican amber. Science, 273:1850–1852. Ivanov, B. 1990. Diet of house sparrow (Passer domesticus L.) nestlings at a livestock farm near Sofia, Bulgaria. Pp. 179–

References

197 in Granivorous Birds in the Agricultural Landscape (J. Pinowski & J. D. Summers-Smith, eds.). PWN-Polish Scientific Publishers, Warsaw. Iwasaki, Y. 1998. Variation in hunting and mating behavior in two populations of the Japanese hangingfly Bittacus mastrillii (Mecoptera: Bittacidae). Ann. Ent. Soc. Am., 91:235–238. Jaeger, E. C. 1959. A Source-book of Biological Names and Terms. 3rd ed. Charles C. Thomas, Springfield, IL. Janczyk, F. S. W. 1956. Anatomie von Siro duricorius Joseph im Vergleich mit anderen Opilioniden. Sitzungsberichte Österreichischen Akademie der Wissenschaften, Mathematischnaturwissenschaftliche Klasse, 165:474–522. Janetschek, H. 1957. Zur Landtierwelt der Dolomiten. Der Schlern, 31:71–86. Jeanmougin, F., J. D. Thompson, M. Gouy, D. G. Higgins, & T. J. Gibson. 1998. Multiple sequence alignment with Clustal X. Trends Biochem. Sci., 23:403–405. Jeannel, R. 1926. Faune cavernicole de la France avec une étude des conditions d’existence dans le domaine souterrain. Encycl. Ent., 7:1–334. Jell, P. A., & P. M. Duncan. 1986. Invertebrates, mainly insects, from the freshwater Lower Cretaceous Koonwarra Fossil Bed (Korumburra Group), South Gippsland, Victoria. Mem. Assoc. Aust. Paleontol., 3:111–205. Jennings, A. L. 1982. A new species of harvestman of the genus Mitopus in Britain. J. Zool., 198:1–14. Jennings, A. L. 1983. Biogeographical variation in the harvestman Mitopus morio (Opiliones, Arachnida). J. Zool., 200:367–380. Jennings, D. T., M. W. Houseweart, & J. C. Cokendolpher. 1984. Phalangids (Arachnida: Opiliones) associated with strip clear-cut and dense spruce-fir forests of Maine. Environ. Ent., 13:1306–1311. Jenssen, T. A., & W. D. Klimstra. 1966. Food habits of the green frog, Rana clamitans, in southern Illinois. Am. Mid. Nat., 76:169–182. Johnson, J. K., & W. C. Gordon. 1990. Screening pigment granule formation in Eumesosoma roeweri (Arachnida: Opiliones). J. Morphol., 203:211–217. Johnson, P. T. 1968. An Annotated Bibliography of Pathology in Invertebrates Other than Insects. Burgess Publishing Co., Minneapolis, MN. Johnstone, R. A., & L. Keller. 2000. How males can gain by harming their mates: sexual conflict, seminal toxins, and the cost of mating. Am. Nat., 156:368–377. Jones, J. C. 1962. Current concepts concerning insect hemocytes. Am. Zool., 2:209–246. Jones, R. 2003. Learn to spy on your garden microlife. Wildlife Mag., 2003:11. Jones, R. N. 1991. B-chromosome drive. Am. Nat., 137:430– 442.

543

Jones, R. N. & Rees, H. 1982. B Chromosomes. Academic Press, London. Jones, T. H., W. E. Conner, A. F. Kluge, T. Eisner, & J. Meinwald. 1976. Defensive substances of opilionids. Experientia, 32:1234–1235. Jones, T. H., J. Meinwald, K. Hicks, & T. Eisner. 1977. Characterization and synthesis of volatile compounds from the defensive secretions of some “daddy longlegs” (Arachnida: Opiliones: Leiobunum spp.). Proc. Natl. Acad. Sci. USA, 74:419–422. Joseph, G. 1868a. Cyphophthalmus duricorius, eine neue Arachniden-Gattung aus einer neuen Familie der Arthrogastren-Ordnung entdeckt in der Luëger Grotte in Krain. Berl. entomol. Z., 12:241–250. Joseph, G. 1868b. Nachtrag zur Beschreibung von Cyphophthalmus duricorius S. 241 seq. Berl. entomol. Z., 12:269–272. Juberthie, C. 1956. Nombres chromosomiques chez les Sironidae, Trogulidae, Ischyropsalidae, Phalangiidae (Opiliones). C. r. Acad. Sci., Paris, 242:2860–2862. Juberthie, C. 1957a. Développement de deux Opilions Phalangiidae, Odiellus gallicus E. Simon, et Homalenotus quadridentatus Cuvier. C. r. Acad. Sci., Paris, 244:2747–2750. Juberthie, C. 1957b. Presence d’organes de stridulation chez deux Nemastomatidae (Opilions). Bull. Mus. Hist. nat. Paris, 29:210–212. Juberthie, C. 1958. Révision du genre Parasiro (Opilions, Sironidae) et descriptions de Parasiro minor n. sp. Bull. Mus. Hist. nat. Paris, 30:159–166. Juberthie, C. 1960a. Action de différentes températures constantes sur le développement des oeufs de l’Opilion Odiellus gallicus E.S. C. r. Acad. Sci., Paris, 250:2079–2081. Juberthie, C. 1960b. Sur la biologie d’un Opilion endogé, Siro rubens Latr. (Cyphophthalmes). C. r. Acad. Sci., Paris, 251:1674–1676. Juberthie, C. 1961a. Données sur la biologie des Ischyropsalis C.L.K. (Opilions, Palpatores, Ischyropsalidae). Ann. Spéléol., 16:381–395. Juberthie, C. 1961b. Étude des Opilions Cyphophthalmes (Arachnides) du Portugal: description d’Odontosiro lusitanicus gen.n., sp.n. Bull. Mus. Hist. nat. Paris, 33:512–519. Juberthie, C. 1961c. Structure et fonction des glandes odorantes chez quelques opilions (Arachnida). Zool. Anz., 25:533–537. Juberthie, C. 1961d. Structures des glandes odorantes et modalités d’utilisation de leur sécrétion chez deux opilions cyphophthalmes. Bull. Soc. zool. Fr., 86:106–116. Juberthie, C. 1962. Étude des opilions cyphophthalmes Stylocellinae du Portugal. Description de Paramiopsalis ramulosus gen.n., sp.n. Bull. Mus. Hist. nat. Paris, 34:267–275. Juberthie, C. 1964. Recherches sur la biologie des opilions. Ann. Spéléol., 19:1–244.

544

References

Juberthie, C. 1965. Données sur l’écologie, le développement et la reproduction des Opilions. Rev. Ecol. Biol. Sol, 2:377– 396. Juberthie, C. 1967. Siro rubens (Opilion, Cyphophthalme). Rev. Ecol. Biol. Sol, 4:155–171. Juberthie, C. 1968. Organes de stridulation chez un opilion cavernicole, Abasola sarea (Travuniidae). Ann. Spéléol., 23:479–482. Juberthie, C. 1969. Sur les opilions cyphophthalmes Stylocellinae du Gabon. Biologia Gabonica, 5:79–92. Juberthie, C. 1970a. Les genres d’opilions Sironinae (Cyphophthalmes). Bull. Mus. Hist. nat. Paris, 41:1371–1390. Juberthie, C. 1970b. Sur Suzukielus sauteri (Roewer, 1916) opilion cyphophthalme du Japon. Rev. Ecol. Biol. Sol, 7:563–569. Juberthie, C. 1971. Les opilions cyphophthalmes cavernicoles. Notes sur Speleosiro argasiformis Lawrence. Bull. Mus. Hist. nat. Paris, 42:864–871. Juberthie, C. 1972. Reproduction et développement d’un opilion Cosmetidae, Cynorta cubana (Banks), de Cuba. Ann. Spéléol., 27:773–785. Juberthie, C. 1974. Ponte, durée du développement embryonnaire et biogéographie de l’opilion troglobie, Ischyropsalis strandi Kratochvíl. Ann. Spéléol., 29:47–51. Juberthie, C. 1976. Chemical defence in soil opiliones. Rev. Ecol. Biol. Sol, 13:155–160. Juberthie, C. 1979. Un cyphophthalme nouveau d’une grotte de Nouvelle-Caledonie: Troglosiro aelleni n.gen., n.sp. (Opilion, Sironinae). Rev. suisse Zool., 86:221–231. Juberthie, C. 1983. Neurosecretory systems and neurohemal organs of terrestrial Chelicerata (Arachnida). Pp. 149– 203 in Neurohemal Organs of Arthropods (A. P. Gupta, ed.). Charles C. Thomas, Springfield, IL. Juberthie, C. 1988. Un nouvel opilion cyphophthalme aveugle d’Australie: Austropurcellia gen. nov., scoparia n.sp. Mém. Biospéol., 15:133–140. Juberthie, C. 1989. Rakaia daviesae sp.nov. (Opiliones, Cyphophthalmi, Pettalidae) from Australia. Mem. Queensland Mus., 27:499–507. Juberthie, C., & L. Juberthie-Jupeau. 1974. Ultrastructure of neurohemal organs (paraganglionic plates) of Trogulus nepaeformis (Scopoli) (Opiliones, Trogulidae) and release of neurosecretory material. Cell Tissue Res., 150:67–78. Juberthie, C., A. Lopez, & L. Juberthie-Jupeau. 1981a. Étude ultrastructurale des sensilles thoraciques dorsales et paramédianes chez Sabacon paradoxum Simon (Palpatores, Sabaconidae). Att. Soc. Toscana Sci. Nat. Mem., ser. B, 88(suppl.):27–33. Juberthie, C., A. Lopez, & L. Juberthie-Jupeau. 1981b. Sur l’equipement adéno-sensorial du pédipalpe de l’opilion troglophile Sabacon paradoxum Simon (Palpatores, Saba-

conidae). Pp. 810–813 in Proceedings of the 8th International Congress of Speleology. Bowling Green, KY. Juberthie, C., A. Lopez, & L. Juberthie-Jupeau. 1991. Les glandes odorantes des Ischyropsalidae souterrains (Opilions): ultrastructure et role. Mém. Biospéol., 18:39–46. Juberthie, C., & J. F. Manier 1977. Étude ultrastructurale de la spermiogenèse de deux Opilions Laniatores: Cynorta cubana Banks (Cosmetidae) et Strisilvea cavicola Roewer (Phalangodidae). Rev. Arachnol., 1:103–115. Juberthie, C., & J. F. Manier. 1978. Étude ultrastructurale comparée de la spermiogenèse des opilions et son intérêt phylétique. Symp. Zool. Soc. London, 42:407–416. Juberthie, C., & A. Muñoz-Cuevas. 1970. Revision de Chileogovea oedipus Roewer (Opiliones: Cyphophthalmi: Sironinae). Senckenbergiana Biol., 51:109–118. Juberthie, C., & A. Muñoz-Cuevas. 1971. Sur la ponte de Pachylus quinamavidensis (Opilion, Gonyleptidae). Bull. Soc. Hist. Nat. Toulouse, 107:468–474. Juberthie, C., & A. Muñoz-Cuevas. 1973. Le problème de la regressión de l’appareil visuel chez les opilions. Ann. Spéléol., 28:147–157. Karaman, I. M. 1993. Contribution to the knowledge of the genus Siro (Arachnida, Opiliones) from the Balkan Peninsula: Siro minutus Kratochvíl, 1937. Proc. Nat. Sci., Matica Srpska, 84:19–25. Karaman, I. M. 1995. Fauna opiliona (Arachnida, Opiliones) Durmitorskog podrucja. M.Sc. Thesis, University of Novi Sad, Novi Sad, Serbia. Karaman, I. M. 2005. Evidence of spermatophores in Cyphophthalmi (Arachnida, Opiliones). Rev. suisse Zool., 112:3–11. Karaman, I. M., M. Bokorov, & D. Stevanovid. 1994. Taxonomical significance of SEM morphology of the species complex Siro duricorius (Joseph, 1868) (Cyphophthalmi, Opiliones). Pp. 117–118 in I Kongres Elektronske Mikroskopije. Novi Sad, Serbia. Karlsson, A. K. B., B. I. Henrikson, C. Härlin, P. Ivarsson, J. A. E. Stenson, & B. W. Svensson. 1999 The possible role of volatile secretions as intra- and interspecific alarm signals in Gyrinus species. Oikos, 87:220–227. Karsch, F. 1880. Arachnologische Blätter (Decas I). IX. Neue Phalangiden des Berliner Museums. Zeitschrift für die gesamten Naturwissenschaften, 53:373–409. Karsch, F. 1892. Arachniden von Ceylon und von Minikoy, gesammelt von den Herren Doctoren P. und F. Sarasin. Dtsch. ent. Z., 36:267–310. Kästner, A. 1925. Studien zur Ernährung der Arachniden. I. Die Nahrungsaufnahme einiger Phalangiden. Zool. Anz., 62:212–214. Kästner, A. 1926. Opiliones: Weberknechte. Pp. 1–55 in Biologie der Tiere Deutschlands, Lieferung 18, Teil 19 (P. Schulze, ed.). Verlag von Gebrüder Borntraeger, Berlin.

References

Kästner, A. 1931a. Biologische Beobachtungen an Phalangiden. Zool. Anz., 95:293–302. Kästner, A. 1931b. Die Hüfte und ihre Umformung zu Mundwerkzeugen bei den Arachniden! Versuch einer Organgeschichte. Z. Morph. Ökol. Tiere, 22:721–758. Kästner, A. 1933. Verdauungs- und Atmungsorgane der Weberknechte Opilio parietinus De Greer und Phalangium opilio L. Z. Morph. Ökol. Tiere, 27:587–623. Kästner, A. 1934. Die stammesgeschichtliche Entwicklung der Darmblindsäcke bei den Opiliones. Zool. Anz., 106:257– 272. Kästner, A. 1935a. Die Funktion der sogenannten sympathischen Ganglien und die Exkretion bei den Phalangiiden. Zool. Anz., 109:273–288. Kästner, A. 1935b. Opiliones Sundevall: Weberknechte. Pp. 300–393 in Handbuch der Zoologie: Eine Naturgeschichte der Stamme des Tierreiches III, 2. Hälfte, 1. Teil (W. Kukenthal, ed.). Walter de Gruyter & Co., Berlin. Kästner, A. 1941. Opiliones: Nachträge und Berichtigungen. Pp. 187–194 in Handbuch der Zoologie: Eine Naturgeschichte der Stamme des Tierreiches, III, 2. Hälfte, 3. Teil (T. Krumbach, ed.). Walter de Gruyter & Co., Berlin. Kästner, A. 1968. Order Opiliones, Harvestmen. Pp. 229–247 in Invertebrate Zoology, vol. 2. Wiley, New York. Katayama, R. W., & R. L. Post. 1974. Phalangida of North Dakota. North Dakota Insects, 9:1–40. Kaufman, W. R., & J. E. Phillips. 1982. Ion and water balance in the ixodid tick Dermacetor andersoni. J. Exp. Biol., 58:523– 536. Kauri, H. 1961. Opiliones. Pp. 9–197 in South African Animal Life! Results of the Lund University Expedition in 1950– 1951, vol. 8 (B. Hanström, P. Brinck, & G. Rudebeck, eds.). Almquist & Wiksell, Uppsala. Kauri, H. 1985. Opiliones from central Africa. Ann. Mus. R. Afr. Cent. (Sci. Zool.), 245:1–168. Kauri, H. 1989. External ultrastructure of sensory organs in the subfamily Irumuinae (Arachnida, Opiliones, Assamiidae). Zool. Scripta, 18:289–294. Keilbach, R. 1982. Bibliographie und Liste der Arten tierischer Einschlüsse in fossilen Harzen sowie ihrer Aufbewahrungsorte. Dtsch. ent. Z., N. F., 29:129–286, 301–491. Keller, S. 1987. Arthropod-pathogenic Entomophthorales of Switzerland. I. Conidiobolus, Entomophaga and Entomophthora. Sydowia, 40:122–167. Kempenaers, B., K. Foerster, S. Questiau, B. C. Robertson, & E. L. M. Vermeirssen. 2000. Distinguishing between female sperm choice versus male sperm competition: a comment on Birkhead. Evolution, 54:1050–1052. Kight, S. L. 1997. Factors influencing maternal behaviour a in burrower bug, Sehiurus cinctus (Heteroptera: Cydnidae). Anim. Behav., 53:105–112.

545

Kilby, J. D. 1945. A biological analysis of the food and feeding habits of two frogs, Hyla cinerea cinerea and Rana pipiens sphenocephala. Q. J. Fla Acad. Sci., 8:71–104. Kirby, W. 1818. A century of insects, including several new genera described from his cabinet. Trans. Linn. Soc. Lond., 12:375–453. Kirschner, W. 1987. Behavioural and physiological adaptations to cold. Pp. 66–77 in Ecophysiology of Spiders (W. Nentwig, ed.). Springer-Verlag, Berlin. Klee, G. E., & J. W. Butcher. 1968. Laboratory rearing of Phalangium opilio (Arachnida: Opiliones). Michigan Entomol., 1:275–278. Klewen, R. 1988. Die Landsalamander Europas. Teil 1. Die Neue Brehm-Bucherei, 584:1–184. Kobulej, T. 1957. Beiträge zur Trombidiidenfauna ungrns. 1. Feststellung der Identität der Trombidiumlarve. Acta Vet. Acad. Sci. Hung., 7:175–184. Koch, C. L. 1839. Übersicht des Arachnidensystems. Vol. 1. C. H. Zeh’sche Buchhandlung, Nürnberg. Koch, C. L. 1850. Übersicht des Arachnidensystems. Vol. 5. C. H. Zeh’sche Buchhandlung, Nürnberg. Koch, C. L., & G. C. Berendt. 1854. Die im Bernstein befindlichen Crustaceen, Myriapoden, Arachniden und Apteren der Vorwelt. Pp. 1–24 in Die im Berstein befindlichen organischen Reste der Vorwelt, 1. Band, 2 (G. C. Berendt, ed.). Abteilung Buchhandlung Nicolai, Berlin. Koch, L. 1867. Zur Arachniden- und Myriopoden-Fauna SüdEuropas. Verh. k.-k. zool.-bot. Ges. Wien, 17:857–900. Koch, L. 1879. Arachniden aus Sibirien und Novaja Semlja eingesammelt von der schwedischen Expedition im Jahre 1875. Bihang Till K. Svenska Vet.- Akad. Handlingar, 16:1– 36. Köhler, H.-R. 2002. Localization of metals in cells of saprophagous soil arthropods (Isopoda, Diplopoda, Collembola). Microsc. Res. Tech., 56:393–401. Kokko, H., & M. Jennions. 2003. It takes two to tango. Trends Ecol. Evol., 18:103–104. Kolosváry, G. von. 1929. Die Weberknechte Ungarns. StudiumVerlag, Budapest. Kolosváry, G. von. 1934. Neue Weberknecht-Studien. I. Beiträge zur Teratologie der Phalangium opilio L. Acta biol., 3:1–5. Komposch, C. 1992. Morphologie, Verbreitung und Bionomie des Weberknechtes Anelasmocephalus hadzii Martens, 1978 (Arachnida, Opiliones). Ph.D. Thesis, Universität Graz, Graz, Austria. Komposch, C. 1993. Neue synanthrope Arachniden für Kärnten und die Steiermark. Carinthia II, 183/103:803– 814. Komposch, C. 1996. Arachnological investigations on primary succession of an artificial island in southern Austria

546

References

(Arachnida: Opiliones, Araneae). Proceedings of the 13th International Congress of Arachnology, Rev. suisse Zool., vol. hors série:327–334. Komposch, C. 1997a. The arachnid fauna of different stages of succession in the Schütt rockslip area, Dobratsch, southern Austria (Arachnida: Scorpiones, Opiliones, Araneae). Pp. 139–149 in Proceedings of the 16th European Colloquium of Arachnology (M. M. Zabka, ed.). Siedlce, Poland. Komposch, C. 1997b. Die Weberknechtfauna (Opiliones) des Nationalparks Hohe Tauern: Faunistisch-okologische Untersuchungen von der Montan- bis zur Nivalstufe unter besonderer Berücksichtiung des Gossnitztales. Wiss. Mitteilungen a. d. Nationalpark Höhe Tauern, 3:73–96. Komposch, C. 2000a. Harvestmen and spiders in the Austrian wetland “Hörfeld-Moor” (Arachnida: Opiliones, Araneae). Ekológia, 19(suppl. 4):65–77. Komposch, C. 2000b. Trogulus falcipenis, spec. nov., ein neuer Brettkanker aus den Alpen und dem Dinarischen Gebirge (Arachnida, Opiliones, Trogulidae). Spixiana, 23:1–14. Komposch, C., & J. Gruber. 1999. Vertical distribution of harvestmen in the Eastern Alps (Arachnida: Opiliones). Bul. Br. Arachnol. Soc., 11:131–135. Koponen, S. 1994. Ground-living spiders, opilionids and pseudoscorpions of peatlands in Québec. Mem. Ent. Soc. Canad., 169:41–60. Koponen, S. 1995. Quelques opilions (Arachnida) de la Province de Québec. Fabrieres, 20:1–5. Koponen, S., V. Rinne, & T. Clayhills. 1997. Arthropods on oak branches in SW Finland, collected by a new trap type. Ent. Fennica, 8:177–183. Korodi Gál, J. 1969. Beiträge zur Kenntnis der Brutbiologie und Brutnahrung der Neuntöter (Lanius collurio L.). Zool. Abh. Mus. Tierkd. Dresden, 30:57–82. Kosmowska-Ceranowicz, B. 2001. The old Gdansk amber collection. Prace Muzeum Ziemi, 46:81–106. Koval, E. Z. 1974. Guidebook to Entomophilic Fungi of the USSR. Naukova Dumka, Kiev. [In Russian] Kovoor, J. 1978. Natural calcification of the prosomatic endosternite in the Phalangiidae (Arachnida: Opiliones). Calcif. Tissue Res., 26:267–269. Krantz, G. W. 1975. A Manual of Acarology. Oregon State University Book Stores, Corvallis. Kratochvíl, J. 1937. Lola insularis nov. gen. nov. spec. (Fam. Phalangodidae) a Travunia (?) jandai nov. spec. (Fam. Travuniidae), dva noví jeskynní sekáci z jihodalmatskych ostrovt. Folia ent., 1:44–54. Kratochvíl, J. 1958a. Die Höhlenweberknechte Bulgariens (Cyphophthalmi und Laniatores). Acta Acad. Sci. Cechoslovenicae Basis Brunensis, 30:372–396. Kratochvíl, J. 1958b. Höhlenweberknechte Bulgariens (Palpa-

tores-Nemastomatidae). Acta Acad. Sci. Cechoslovenicae Basis Brunensis, 30:523–576. Kratochvíl, J. 1959. Novoie podcemeistvo cenocostzev (Giljaroviinae, Nemastomatidae) c opredelitelnoi tablitzei rodov Nemastomatidae. Zool. Zhurnal, 38:1344–1352. Kraus, O. 1961. Die Weberknechte der Iberischen Halbinsel (Arach., Opiliones). Senckenbergiana Biol., 42:331–363. Krause, J., & G. D. Ruxton. 2002. Living in Groups. Oxford Series in Ecology and Evolution. Oxford University Press, Oxford. Krebs, J. R., & N. B. Davies. 1993. Behavioural Ecology: An Evolutionary Approach. Blackwell, Oxford. Kreiter, N. A., & D. H. Wise. 2001. Prey availability limits fecundity and influences the movement pattern of female fishing spiders. Oecologia, 127:417–424. Kristín, A. 1988a. Modifikation des Bedeutungsindexes von Nahrungskomponenten und seine Verwendung. Biologia, 43:935–939. Kristín, A. 1988b. Nahrungsansprüche der Nestlinge Pica pica und Passer montanus in den Windbrechern der Schüttinsel. Folia Zool., 37:343–356. Kristín, A. 1991. Ernährung der Nestlinge von Phylloscpopus collybita und Phylloscopus sibilatrix in den Eichen-Buchen Wäldern der Zentralslowakei. Acta Facultatis Rerum Naturalium Universitatis Comenianae Zoologia, 35:137–142. Kristín, A. 1992. Trophische Beziehungen zwischen Singvögeln und Wirbellosen im Eichen-Buchenwald zur Brutzeit. Ornithol. Beobachter, 89:157–169. Kristín, A. 1993a. Die Nestlingsnahrung des Kleibers (Sitta europaea L.) in Buchenwäldern. Acta Ornithoecol., 2:341– 349. Kristín, A. 1993b. Präferenzen in der Nestlingsnahrung der Heckenbraunelle Prunella modularis in verschiedenen Waldvegetationsstufen. Vogelwelt, 114:72–82. Kristín, A. 1994. Food variability of nuthatch nestlings (Sitta europaea) in mixed beech forests: Where are limits of its polyphagy? Biologia, 49:773–779. Kristín, A. 2002. Food variability of collared flycatcher nestlings (Ficedula albicollis) in mixed beech forests. Ekólogia, 21(suppl. 2):159–164. Kristín, A., & T. Baumann. 1996. Opilionids in the diet of bird nestlings. Arachnol. Mitt., 11:43–46. Krohn, A. 1867. Über die Anwesenheit zweier Drüsensäcke im Cephalothorax der Phalangiden. Arch. Naturgesch., 33:79–83. Kupryjanowicz, J. 2001. Arthropods in Baltic amber and their photographic record. Pp. 19–72 in The Amber Treasure Trove, pt. 1: The Tadeusz Giecewicz’s Collection at the Museum of the Earth, Polish Academy of Sciences, Warsaw (B. Kosmowska-Ceranowicz, ed.). Museum of the Earth Documentary Studies, Warsaw. Kury, A. B. 1991. Análise filogenética de Mitobatinae (Opil-

References

iones, Laniatores, Gonyleptidae). M.Sc. Thesis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil. Kury, A. B. 1992a. The false Cranainae of the Brazilian Atlantic forest (Opiliones, Gonyleptidae). Trop. Zool., 5:279–291. Kury, A. B. 1992b. The genus Spinopilar Mello-Leitão, 1940, with notes on the status of the family Tricommatidae (Arachnida, Opiliones). Steenstrupia, 18:93–99. Kury, A. B. 1993a. Análise filogenética de Gonyleptoidea (Arachnida, Opiliones, Laniatores). Ph.D. Thesis, Universidade de São Paulo, São Paulo, Brazil. Kury, A. B. 1993b. Leptostygnus leptochirus Mello-Leitão, 1940: the first record of the family Agoristenidae from Colombia (Opiliones: Laniatores: Gonyleptoidea). Bull. Br. Arachnol. Soc., 9:129–131. Kury, A. B. 1994a. Early lineages of Gonyleptidae (Arachnida, Opiliones, Laniatores). Trop. Zool., 7:343–353. Kury, A. B. 1994b. The genus Yania and other presumed Tricommatidae from South American highlands (Opiliones, Cranaidae, Prostygninae). Rev. Arachnol., 10:137–145. Kury, A. B. 1997a. The genera Saramacia Roewer and Syncranaus Roewer, with notes on the status of the Manaosbiidae (Opiliones, Laniatores). Bol. Mus. Nac., n.s., Zool., 374:1–22. Kury, A. B. 1997b. A new subfamily of Agoristenidae, with comments on suprageneric relationships of the family (Arachnida, Opiliones, Laniatores). Trop. Zool., 10:333– 346. Kury, A. B. 1997c. Os Stygnopsidae na filogenia de Gonyleptoidea, com comentários sobre a biogeografia da superfamília. P. 30 in Actas del Primer Encuentro de Aracnólogos del Cono Sur. Montevideo, Uruguay. Kury, A. B. 2002. Intercontinental relationships among Southern Gondwanian Triaenonychidae (Opiliones, Laniatores, Insidiatores). In Abstracts of 7th African Arachnological Colloquium (unnumbered page). Durban, South Africa. Kury, A. B. 2003. Annotated catalogue of the Laniatores of the New World (Arachnida, Opiliones). Rev. Ibér. Aracnol., vol. especial monográfico, 1:1–337. Kury, A. B., & J. C. Cokendolpher. 2000. Opiliones. Pp. 137– 157 in Biodiversidad, taxonomía y biogeografía de artópodos de México: Hacia una síntesis de su conocimiento, vol. 2 (J. E. Llorente-B., E. González-S., & N. Papavero, eds.). Universidad Nacional Autónoma de México, Mexico DF, Mexico. Kury, A. B., & G. Machado. 2003. Transporte de ovos pelos machos: uma sinapomorfia comportamental para os opiliões da família Podoctidae (Opiliones: Laniatores). P. 127 in IV Encontro de Aracnólogos do Cone Sul (G. Machado & A. D. Brescovit, eds.). São Pedro, São Paulo, Brazil. Kury, A. B., & E. A. Maury. 1998. A new genus and five new species of Metasarcinae from Peru (Arachnida, Opiliones, Gonyleptidae). Zool. J. Linn. Soc., 123:143–162.

547

Kury, A. B., & A. Pérez G. 2002. A new family of Laniatores from northwestern South America (Arachnida, Opiliones). Rev. Ibér. Aracnol., 6:3–11. Kury, A. B., & R. Pinto-da-Rocha. 1997. Notes on the Brazilian harvestmen genera Progonyleptoidellus Piza and Iporangaia Mello-Leitão (Opiliones: Gonyleptidae). Revta bras. Ent., 41:109–115. Kury, A. B., & R. Pinto-da-Rocha. 2002. Opiliones. Pp. 345– 362 in Amazonian Arachnida and Myriapoda (J. Adis, ed.). Pensoft Publishers, Sofia. Kuvikova, A. 1985a. The food of some species of the family Soricidae (Insectivora) in the alder forest of the Jursky Sur wetland. Biologia, 40:181–187. Kuvikova, A. 1985b. Zur Nahrung der Wasserspitzmaus, Neomys fodiens (Pennant, 1771) in der Slowakei. Biologia, 40:563–672. Kuvikova, A. 1986. Nahrung und Nahrungsansprüche der Alpenspitzmaus (Sorex alpinus, Mammalia, Soricidae) unter den Bedingungen der Tschechoslowakischen Karpaten. Folia Zool., 35:117–125. Lagerheim, G. 1898. Mykologische Studien. I. Beiträge zur Kenntnis der parasitischen Pilze, 1–3. Bihang Till K. Svenska Vet.-Akad. Handlingar, Bd. 24, Afd. 3, 4:3–22. Lane, J. 1947. A biologia e taxonomia de algumas espécies dos grupos Forcipomya e Culicoides (Diptera, Ceratopogonidae [Heleidae]). Arquivos da Faculdade de Higiene e Saúde Pública da Universidade de São Paulo, 1:159–170. Lang, A. 2000. The pitfalls of pitfalls: a comparison of pitfall trap catches and absolute density estimates of epigeal invertebrate predators in arable land. J. Pest Sci., 73:99–106. Lankester, E. R., W. Benham, & E. Beck. 1885. On the muscular and endoskeletal systems of Limulus and Scorpio. Trans. Zool. Soc. Lond., 11:311–384. Larsson, S. G. 1978. Baltic Amber: A Palaeobiological Study. Entomonograph, vol. 1. Scandinavian Science Press, Klampenborg, Denmark. Latreille, P. A. 1796. Précis des caractères génériques des insectes, disposés dans un ordre naturel. Prévot, Paris. Latreille, P. A. 1802a. Histoire naturelle, générale et particulière, des crustacés et des insectes: Familles naturelles des genres. Vol. 3. F. Duart, Paris. Latreille, P. A. 1802b. Mémoire pour servir de suite à l’histoire naturelle des insectes connus sous le nom de Faucheurs. Pp. 354–384 in Histoire naturelle des fourmis, et recueil de mémoires et d’observations sur les abeilles, les araignées, les faucheurs, et autres insectes. Crapelet, Paris. Latreille, P. A. 1804. Histoire naturelle générale et particulière, des crustacés et des insectes. Vol. 7. F. Duart, Paris. Latreille, P. A. 1806. Genera crustaceorum et insectorum secundum ordinem naturalem in familias disposita, iconibus exemplisque plurimis explicata. A. Koenig, Paris.

548

References

Latreille, P. A. 1829. Règne animal, distribué d’après son organisation: Crustacés, Arachnides et partie des Insectes. Pp. 279–283 in Le règne animal, distribué d’après son organisation, pour servir de base a l’histoire naturelle des animaux et d’introduction a l’anatomie comparée, vol. 4 (G. Cuvier, ed.). Déterville Libraire et Crochard Libraire, Paris. Lawrence, R. F. 1931. The harvest-spiders (Opiliones) of South Africa. Ann. S. African Mus., 29:341–508. Lawrence, R. F. 1933. The harvest-spiders (Opiliones) of Natal. Ann. Natal Mus., 7:211–241. Lawrence, R. F. 1937a. The external sexual characteristics of South African harvest-spiders. Trans. R. Soc. S. Africa, 24:331–337. Lawrence, R. F. 1937b. A stridulating organ in harvest-spiders. Ann. Mag. Nat. Hist., 20:364–369. Lawrence, R. F. 1938. The odoriferous glands of some South African harvest-spiders. Trans. R. Soc. S. Africa, 25:333– 342. Lawrence, R. F. 1939. A contribution to the opilionid fauna of Natal and Zululand. Ann. Natal Mus., 9:225–243. Lawrence, R. F. 1959. Arachnides-Opilions. Faune de Madagascar, Publications de L’Institut de Recherche Scientifique Tananarive, 9:1–121. Lawrence, R. F. 1963. The Opiliones of the Transvaal. Ann. Transvaal Mus., 24:275–304. Leather, S. R., K. F. A. Walters, & J. S. Bale. 1993. The Ecology of Insect Overwintering. Cambridge University Press, Cambridge. Leatherdale, D. 1958. A host catalogue of British entomogenous fungi. Ent. Mon. Mag., 94:103–105. Leatherdale, D. 1970. The arthropod hosts of entomogenous fungi in Britain. Entomophaga, 15:419–435. Lee, P. C. 1994. Social structure and evolution. Pp. 266–303 in Behaviour and Evolution (P. Slater & T. Halliday, eds.). Cambridge University Press, Cambridge. Legendre, R., & G. Morel. 1980. Data on the role of rickettsial and viral disease in the regulation of arachnids populations. Pp. 183–185 in Proceedings of the 8th International Congress of Arachnology (J. Gruber, ed.). Verlag H. Egermann, Vienna. Legg, G. 1990. Parogovia pabsgarnoni, sp. n. (Arachnida, Opiliones, Cyphophthalmi) from Sierra Leone, with notes on other African species of Parogovia. Bul. Br. Arachnol. Soc., 8:113–121. Legg, G., & Pabs-Garnon, E. B. 1989. The life history of a tropical forest cyphophthalmid from Sierra Leone (Arachnida: Opiliones). Pp. 222–230 in XI Europäisches Arachnologisches Colloquium (J. Haupt, ed.). Technische Universität Berlin, Berlin. Lehtinen, R. M., & R. A. Nussbaum 2003. Parental care: a phylogenetic perspective. Pp. 343–386 in Reproductive Bi-

ology and Phylogeny of Anura, vol. 2 (B. G. M. Jamieson, ed.). Science Publications, Plymouth. Leonard, M. D. 1933. Notes on the giant toad, Bufo marinus (L.), in Puerto Rico. J. Econ. Ent., 26:67–72. Levine, N. D. 1985. Phylum Apicomplexa Levine, 1970. Pp. 322–374 in An Illustrated Guide to the Protozoa (J. J. Lee, S. H. Hutner, & E. C. Bovee, eds.). Society of Protozoologists, Lawrence, KS. Lewis, J. G. E. 1981. The Biology of Centipedes. Cambridge University Press, Cambridge. Leydig, F. 1862. Über das Nervensystem der Afterspinne (Phalangium). Archiv f. Anat. Physiol. und wiss. Medizin, 1862:196–202. Lighton, J. R. B. 2002. Lack of discontinuous gas exchange in a tracheate arthropod, Leiobunum townsendi (Arachnida, Opiliones). Physio. Ent., 27:170–174. Linnaeus, C. 1758. Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Vol. 1. Laurentii Salvii, Stockholm. Lipovsek, S., I. Letofsky-Papst, F. Hofer, & M. A. Pabst. 2002. Seasonal and age-related changes of the structure and chemical composition of the spherites in the midgut gland of the harvestmen Gyas annulatus (Opiliones). Micron, 33:647–654. Lipovsek, S., T. Novak, F. Janzekovic, L. Sencic, & M. A. Pabst. 2004. A contribution to the functional morphology of the midgut gland in phalangiid harvestmen Gyas annulatus and Gyas titanus during their life cycle. Tissue Cell, 36:275– 282. Littlewood, P. M. H., & F. M. Littlewood. 1989. Cannibalism in Mitopus morio (F.) (Arachnida, Opiliones) observed in the field. Ent. Mon. Mag., 125:256. Loch, R. 1999. A survey of harvestmen (Arachnida, Opiliones) in a burned pine forest in southwest Germany. Arachnol. Mitt., 17:20–32. Locke, M., & V. Wrightnour Russell. 1998. Pericardial cells or athrocytes. Pp. 687–709 in Microscopic Anatomy of Invertebrates, vol. 11B: Insecta (F. W. Harrison & M. Locke, eds.). Wiley-Liss, New York. Lockwood, J. A., & R. N. Story. 1987. Defensive secretion of the southern green stink bug (Hemiptera: Pentatomidae) as an alarm pheromone. Ann. Ent. Soc. Am., 80:686–691. Löhrl, H., & E. Thaler. 1980. Das Teneriffa-Goldhähnchen Regulus (regulus) teneriffae: Zur Biologie, Ethologie und Systematik. Bonn. zool. Beitr., 31:78–96. Loman, J. C. C. 1896. On the secondary spiracles on the leg of Opilionidae. Zool. Anz., 19:221–222. Loman, J. C. C. 1900. Ueber die geographische Verbreitung der Opilioniden. Zool. Jb., Abt. Syst., Ökol. u. Geog. Tiere, 13:71– 104.

References

Loman, J. C. C. 1902. Neue aussereuropaische Opilioniden. Zool. Jb., Abt. Syst., Ökol. u. Geog. Tiere, 16:163–216. Loman, J. C. C. 1903a. On the classification of Opiliones. Tijd. ned. dierk. Vereen., 8:62–66. Loman, J. C. C. 1903b. Vergleichende anatomische Untersuchungen an chilenischen und andern Opilioniden. Zool. Jb., Abt. Syst., Ökol. u. Geog. Tiere, suppl. 6:117–200. Loman, J. C. C. 1905. Ein farbiges Hautsecret bei den Opilioniden. Zool. Jb., Abt. Syst., Ökol. u. Geog. Tiere, 22:755–758. Loman, J. C. C. 1906. Opilioniden aus Neu-Guinea. Pp. 1–8 in Nova Guinea: Résultats de l’expédition scientifique néenlandaise à la Nouvelle-Guinée en 1903, sous les auspices de Arthur Wichmann, chef de l’expédition, vol. 5. E. J. Brill, Leiden. Lopez, A., M. Emerit, & M. Rambla. 1980. Contribution a l’étude de Sabacon paradoxum Simon 1879 (Opiliones, Palpatores, Ischyropsalididae): Stations nouvelles, particularités électromicroscopiques du prosoma et de ses appendices. Pp. 147–161 in Comptes rendus de la Ve Colloque d’Arachnologie d’Expression Française. Barcelona, Spain. Lopez, A., R. Mazel, F. Marcou, J. Faure, J. Guilhaumon, & J. Delabie 1978. Recherches sur la faune cavernicole de l’arrondissement Béziers–Saint-Pons. Deuxième note (Arachnides, Insectes). Bull. Soc. Sci. nat. Béziers, N.S., 6:4–37. Löser, S. 1980. Zur tageszeitlichen Aktivitätsverteilung von Arthropoda der Bodenstreu (Coleoptera, Diplopoda, Isopoda, Opiliones, Aranae) eines Buchen-Eichen-Waldes (Fago-Quercetum). Ent. generalis, 6:169–180. Lübcke, W. & R. K. Furrer. 1985. Die Wacholderdrossel. Neue Brehm-Bücherei, Bd. 569. Ziemsen, Wittenberg Lutherstadt. Luczak, J., & E. Dabrowski-Prot. 1970. Preliminary observations on the food of the spider Theridion pictum (Walck.) and its predators. Bul. Br. arachnol. Soc., 1:109–111. Ludwig, M., & G. Alberti. 1992. Ultrastructure and function of the midgut of camel-spiders (Arachnida: Solifugae). Zool. Anz., 228:1–11. Luque, C. G. 1991. Los Ischyropsalidoidea de la Cornisa Cantábrica, Cantabria, Arquenas. In Fauna Ibérica Subterránea, Cantabria, vol. 1. Editorial Impresión, Santander. Machado, G. 2002. Maternal care, defensive behavior, and sociality in Neotropical Goniosoma harvestmen (Arachnida, Opiliones). Insectes Sociaux, 49:1–6. Machado, G. (in press). Maternal or paternal egg guarding? Revisiting paternal care in triaenonychid harvestmen (Opiliones). J. Arachnol. Machado, G., V. Bonato, & P. S. Oliveira. 2002. Alarm communication: a new function for the scent gland secretion in harvestmen (Arachnida: Opiliones). Naturwissenschaften, 89:357–360. Machado, G., P. C. Carrera, A. M. Pomini, & A. J. Marsaioli. 2005. Chemical defense in harvestmen (Arachnida: Opil-

549

iones): do benzoquinone secretions deter invertebrate and vertebrate predators? J. Chem. Ecol., 31:2519–2539. Machado, G., A. A. Giaretta, & R. Pinto-da-Rocha. 2001. Notes on the taxonomy and biology of the Neotropical harvestman Goniosoma catarina sp.n. (Opiliones: Gonyleptidae). Rev. Ibér. Aracnol., 4:17–22. Machado, G., & P. S. Oliveira. 1998. Reproductive biology of the Neotropical harvestman Goniosoma longipes (Arachnida, Opiliones: Gonyleptidae): mating and oviposition behaviour, brood mortality, and parental care. J. Zool., 246:359–367. Machado, G., & P. S. Oliveira. 2002. Maternal care in the Neotropical harvestman Bourguyia albiornata (Arachnida, Opiliones): oviposition site selection and egg protection. Behaviour, 139:1509–1524. Machado, G., & M. A. Pizo. 2000. The use of fruits by the Neotropical harvestman Neosaducus variabilis (Opiliones, Laniatores, Gonyleptidae). J. Arachnol., 28:357–360. Machado, G., & R. L. G. Raimundo. 2001. Parental investment and the evolution of subsocial behaviour in harvestmen (Arachnida: Opiliones). Ethol. Ecol. Evol., 13:133–150. Machado, G., R. L. G. Raimundo, & P. S. Oliveira. 2000. Daily activity schedule, gregariousness, and defensive behaviour in the Neotropical harvestman Goniosoma longipes (Opiliones: Gonyleptidae). J. Nat. Hist., 34:587–596. Machado, G., G. S. Requena, B. A. Buzatto, F. Osses, & L. M. Rossetto. 2004. Five new cases of paternal care in harvestmen (Arachnida: Opiliones): implications for the evolution of male guarding in the Neotropical family Gonyleptidae. Sociobiology, 44:577–598. Machado, G., & C. H. F. Vasconcelos. 1998. Multi-species aggregations in Neotropical harvestmen (Arachnida: Opiliones: Gonyleptidae). J. Arachnol., 26:89–391. Machado, G., &. D. M. Vital. 2001. On the occurrence of epizoic algae and liverworts on the harvestmen Neosadocus aff. variabilis (Opiliones: Gonyleptidae). Biotropica, 33:535–538. Machado, G., & J. G. Warfel. 2006. First case of maternal care in the family Cranaidae (Opiliones: Laniatores). J. Arachnol. 34:269–272. Machado, S. F., R. L. Ferreira, & R. P. Martins. 2003. Aspects of the population ecology of Goniosoma sp. (Arachnida, Opiliones, Gonyleptidae) in limestone caves in southeastern Brazil. Trop. Zool., 16:13–31. Machin, J. 1981. Water compartmentalisation in insects. J. Exp. Zool., 215:327–333. Macías-Ordóñez, R. 1997. The mating system of Leiobunum vittatum Say, 1821 (Arachnida: Opiliones: Palpatores): resource defense polygyny in the striped harvestman. Ph.D. Thesis, Lehigh University, Bethlehem, PA. Macías-Ordóñez, R. 2000. Touchy harvestmen. Nat. Hist., 109:58–61. MacKay, W., C. Grimsley, & J. C. Cokendolpher. 1992. Seasonal

550

References

changes in a population of desert harvestmen, Trachyrhinus marmoratus (Arachnida: Opiliones), from western Texas. Psyche, 99:207–213. MacMillan, B. W. H., & B. J. Pollock. 1985. Food of nestling house sparrows (Passer domesticus) in mixed farmland of Hawke’s Bay, New Zealand. N. Z. J. Zool., 12:307–317. Maddison, W. P. 1982. XXXY sex chromosomes in males of the jumping spider genus Pellenes (Araneae: Salticidae). Chromosoma, 85:23–37. Magraph, M. J. L., & J. Komdeur. 2003. Is male care compromised by additional mating opportunity? Trends Ecol. Evol., 18:424–430. Mahner, M. 1993. Systema Cryptoceratorum phylogeneticum (Insecta: Heteroptera). Zoologica, 143:1–302. Mains, E. B. 1950. Entomogenous species of Akanthomyces, Hymenostilbe and Insecticola in North America. Mycologia, 42:566–589. Mantel, L. H. 1979. Terrestrial invertebrates other than insects. Pp. 175–218 in Comparative Physiology of Osmoregulation in Animals, vol. 1 (G. M. O. Maloiy, ed.). Academic Press, London. Manton, S. M. 1952. The evolution of arthropodan locomotory mechanisms. Part 2. General introduction to the locomotory mechanisms of the Arthropoda. Zool. J. Linn. Soc., 42:93–117. Marcellino, I. 1982. Opilioni cavernicoli italiani. Lav. Soc. Ital. Biogeogr., n.s., 7:33–53. Markl, J., W. Stöcker, R. Runzler, & E. Precht. 1986. Immunological correspondences between the hemocyanin subunits of 86 arthropods: evolution of a multigene protein family. Pp. 281–292 in Invertebrate Oxygen Carriers (B. Linzen, ed.). Springer, Berlin. Martens, J. 1965. Verbreitung und Biologie des Schneckenkankers Ischyropsalis hellwigi. Natur u. Mus., 95:143–149. Martens, J. 1969a. Die Artabgrenzung von Biospezies auf biologisch-ethologischer und morphologischer Grundlage am Beispiel der Gattung Ischyropsalis C. L. Koch 1839 (Opiliones, Ischyropsalididae). Zool. Jb., Abt. Syst., Ökol. u. Geog. Tiere, 96:133–264. Martens, J. 1969b. Cyphophthalmi aus Brasilien (Opiliones). Beitr. Neotrop. Fauna, 6:109–119. Martens, J. 1969c. Die Sekretdarbietung während des Paarungsverhaltens von Ischyropsalis C. L. Koch (Opiliones). Z. Tierpsychol., 26:513–523. Martens, J. 1972a. Ausobskya athos, der erste Krallenweberknecht aus Griechenland (Opiliones: Phalangodidae). Senckenbergiana Biol., 53:431–440. Martens, J. 1972b. Opiliones aus dem Nepal-Himalaya. I. Das Genus Sabacon Simon (Arachnida: Ischyropsalididae). Senckenbergiana Biol., 53:307–323.

Martens, J. 1973. Opiliones aus dem Nepal-Himalaya. II. Phalangiidae und Sclerosomatidae (Arachnida). Senckenbergiana Biol., 54:181–217. Martens, J. 1975a. Ischyropsalis hellwigi (Opiliones): Nahrungsauf nahme. Encyclopaedia Cinematographica, Film E 2129:1–7. Institut für den wissenschaftlichen Film, Göttingen. Martens, J. 1975b. Ischyropsalis hellwigi (Opiliones): Paarungsver halten. Encylopaedia Cinematographica, Film E 2128, Beiheft 1–11. Institut für den wissenschaftlichen Film, Göttingen. Martens, J. 1975c. Ischyropsalis kollari (Opiliones). Nahrungsaufnahme. Encyclopaedia Cinematographica, Film E 2130:1–6. Institut für den wissenschaftlichen Film, Göttingen. Martens, J. 1976. Genitalmorphologie, System und Phylogenie der Weberknechte (Arachnida: Opiliones). Ent. Germanica, 3:51–68. Martens, J. 1977. Opiliones aus dem Nepal-Himalaya. III. Oncopodidae, Phalangodidae, Assamiidae. Senckenbergiana Biol., 57:295–340. Martens, J. 1978a. Opiliones aus dem Nepal-Himalaya. IV. Biantidae. Senckenbergiana Biol., 58:347–414. Martens, J. 1978b. Spinnentiere, Arachnida: Weberknechte, Opiliones. Pp. 1–464 in Die Tierwelt Deutschlands, vol. 64, (K. Senglaub, H.-J. Hannemann, & H. Schumann, eds.). Gustav Fischer, Jena. Martens, J. 1979. Feinstruktur der Tarsal-Drüse von Siro duricorius (Joseph) (Opiliones: Sironidae). Zoomorphol., 92:77–93. Martens, J. 1980. Versuch eines phylogenetischen Systems der Opiliones. Pp. 355–360 in Proceedings of the 8th International Congress of Arachnology (J. Gruber, ed.). Verlag H. Egermann, Vienna. Martens, J. 1982. Opiliones aus dem Nepal-Himalaya. V. Gyantinae (Arachnida: Phalangiidae). Senckenbergiana Biol., 62:313–348. Martens, J. 1983. Europäische Arten der Gattung Sabacon Simon 1879 (Arachnida: Opiliones: Sabaconidae). Senckenbergiana Biol., 63:265–296. Martens, J. 1984. Vertical distribution of Palaearctic and Oriental faunal components in the Nepal Himalayas. Erdweiss. Forschung., 18:321–336. Martens, J. 1986. Die Gro␤gliederung der Opiliones und die Evolution der Ordnung (Arachnida). Pp. 289–310 in Proceedings of the 10th International Congress of Arachnology (J. A. Barrientos, ed.). Instituto Pirenaico de Ecología & Grupo de Aracnología, Barcelona, Spain. Martens, J. 1987. Opiliones aus dem Nepal-Himalaya. VI. Gagrellinae (Arachnida: Phalangiidae). Courier Forschungsinstitut Senckenberg, 93:87–202. Martens, J. 1988. Fissiphaliidae, a new family of South American laniatorean harvestmen (Arachnida: Opiliones). Z. Zool. Syst. Evolut.-forsch., 26:114–127.

References

Martens, J. 1989. Sibirische Arten der Gattung Sabacon Simon, 1879 (Arachnida: Opiliones: Sabaconidae). Senckenbergiana Biol., 69:369–377. Martens, J. 1993a. Bodenlebende Arthropoda im zentralen Himalaya: Bestandsaufnahme, Wege zur Viefalt und ökologische Nischen. Pp. 231–250 in Neue Forschungen im Himalaya (U. Scheinfurth, ed.). F. Steiner, Stuttgart. Martens, J. 1993b. Further cases of paternal care in Opiliones (Arachnida). Trop. Zool., 6:97–107. Martens, J., & C. Chemini 1988. Die Gattung Anelasmocephalus Simon, 1879—Biogeographie, Artgrenzen und Biospezies-Konzept (Opiliones: Trogulidae). Zool. Jb., Abt. Syst., Ökol. u. Geog. Tiere, 115:1–48. Martens, J., U. Hoheisel, & M. Götze. 1981. Vergleichende Anatomie der Legeröhren der Opiliones als Beitrag zur Phylogenie der Ordnung (Arachnida). Zool. Jb., Abt. Anat. u. Ont. Tiere, 105:13–76. Martens, J., & M. Lingnau. 1985. Die Weberknechte Scotolemon lespesi Lucas und Scotolemon lucasi Simon aus den Pyrenäen—zwei valide Arten? (Arachnida: Opiliones: Phalangodidae). Mém. Biospéol., 12:111–126. Martens, J., & W. Schawaller. 1977. Die Cheliceren-Drüsen der Weberknechte nach rasteroptischen und lichtoptischen Befunden (Arachnida: Opiliones). Zoomorphol., 86:223– 250. Martens, J., & P. J. Schwendinger. 1998. A taxonomic revision of the family Oncopodidae. I. New genera and new species of Gnomulus Thorell (Opiliones, Laniatores). Rev. suisse Zool., 105:499–555. Martens, J., & S. Suzuki 1966. Zur systematischen Stellung ostasiatischer Ischyropsalididen-Arten (Arachnoidea, Opiliones, Ischyropsalididae). Annot. Zool. Jap., 39:215– 221. Martínez, S. V. de 1974. Consideraciones ecológicas sobre algunas especies de opiliones (Arachnida) hallados en el Departamento Capital (Santa Fe, Argentina). Comunicaciones del Museo Provincial de Ciencias Naturales Florentino Ameghino, (Zoología), 7:11pp. (without pagination). Mashberg, D. 2001. Brood care and social behavior. Pp. 257– 277 in Scorpion Biology and Research (P. Brownell & G. A. Polis, eds.). Oxford University Press, New York. Masters, W. M. 1979. Insect disturbance stridulation: its defensive role. Behav. Ecol. Sociobiol., 5:187–200. Mastororill, V. I. 1965. I fossili Quaternari del Bacino diatomico di Riano (Roma) nella collezione del Museo Civico di Scienze naturali “G. Doria” in Genova. Atti dell’Istituto di Geologia della Università di Genova, 3:1–245. Mattes, S., J. Tumbrick, & M. Fischbacher. 1996. Die Nestlingsnahrung von Kohl-, Tannen-, Alpen- und

551

Haubenmeisen im Larcher-Arvenwald des Engadins. Ornithol. Beobachter, 93:293–314. Matthiesen, F. A. 1975. Sobre a postura de Discocyrtus pectinifemur Mello-Leitão, 1937 (Opiliones, Gonyleptidae). Cienc. Cult., 27 suppl. 372. Matthiesen, F. A. 1980. Sará-sará, formiga predadora de escorpiões e opiliões. Revta Agric., 55:239–241. Matthiesen, F. A. 1983. Comportamento sexual de um opilião brasileiro Discocyrtus pectinifemur Mello-Leitão, 1937 (Opiliones: Gonyleptidae). Cienc. Cult., 35:1339–1341. Matthiesen, F. A. 1985. Notas biológicas sobre opiliões brasileiros (Discocyrtus pectinifemur) Mello-Leitão, 1937 (Opiliones, Gonyleptidae). Pp. 48–49 in Actas do XII Congresso Brasileiro de Zoologia. Sociedade Brasileira de Zoologia, Campinas, Brazil. Mattson, D. J., C. M. Gillin, S. A. Benson, & R. R. Knight. 1991. Bear feeding activity at alpine insect aggregation sites in the Yellowstone ecosystem. Canad. J. Zool., 69:2430–2435. Maury, E. A. 1987. Triaenonychidae sudamericanos. IV. El género Triaenonychoides H. Soares, 1968 (Opiliones, Laniatores). Boln Soc. Biol. Concepción, 58:95–106. Maury, E. A. 1988. Triaenonychidae sudamericanos. V. Un nuevo género de opiliones cavernícolas de la Patagonia (Opiliones, Laniatores). Mém. Biospéol., 15:117–131. Maury, E. A. 1993. Triaenonychidae sudamericanos. VII. Redescripción de Araucanobunus juberthiei Muñoz-Cuevas 1973 (Opiliones, Laniatores). Boln Soc. Biol. Concepción, 64:105–111. Maury, E. A., & A. Pilati. 1996. Comensalismo de Riosegundo birabeni (Canals, 1943) (Opiliones, Gonyleptidae) en hormigueros de Acromyrmex lobicornis (Emery, 1887) (Hymenoptera, Formicidae). Revista del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia,” 142:1–7. Maury, E. A., R. Pinto-da-Rocha, & J. J. Morrone. 1996. Distribution of Acropsopilio chilensis Silvestri, 1904 in southern South America (Opiliones, Palpatores, Caddidae). Biogeographica, 72:127–132. Maury, E. A., & A. H. Roig Alsina. 1985. Triaenonychidae sudamericanos. I. El género Ceratomontia Roewer, 1915 (Opiliones, Laniatores). Hist. Nat., 5:77–92. McAlister, W. H. 1962. Local movements of the harvestman Leiobunum townsendi (Arachnida: Phalandida). Tex. J. Sci., 14:167–173. McAloon, F. M., & L. A. Durden. 2000. Attachment sites and frequency distribution of erythraeid mites, Leptus indianensis (Acari: Prostigmata), ectoparasitic on harvestmen, Leiobunum formosum (Opiliones). Exp. Appl. Acarol., 24:561–567. McAtee, W. L. 1926. The relation of birds to woodlots in New York State. Roosevelt Wildlife Bull., 4:7–152.

552

References

McAtee, W. L. 1932. Effectiveness in nature of the so-called protective adaptations in the animal kingdom, chiefly as illustrated by the food habits of Nearctic birds. Smithson. Misc. Collns, 85:1–201. McCormick, S. J., & G. A. Polis. 1990. Prey, predators, and parasites. Pp. 294–320 in The Biology of Scorpions (G. A. Polis, ed.). Stanford University Press, Stanford, CA. McGhee, C. R. 1977. Observations on the use of measurements in the systematic study of Leiobunum (Arachnida: Phalangida). J. Arachnol., 5:169–178. McMahon, T. A. 1985. The role of compliance in mammalian running gaits. J. Exp. Biol., 115:263–282. Meeûs, T. de, & F. Renaud. 2002. Parasites within the new phylogeny of eukaryotes. Trends Parasitol., 18:247–251. Meijer, J. 1972. Some data on the phenology and the activity patterns of Nemastoma lugubre (Müller) and Mitostoma chrysomelas (Herman) (Nemastomatidae: Opilionida: Arachnida). Neth. J. Zool., 22:105–118. Meijer, J. 1984. Different phenological strategies in two nemastomatid harvestmen (Arachnida: Opilionida: Nemastomatidae). Bul. Br. Arachnol. Soc., 6:211–216. Meinwald J., A. F. Kluge, J. E. Carrel, & T. Eisner. 1971. Acyclic ketones in the defensive secretion of a daddy longlegs (Leiobunum vittatum) (Arachnida: Opiliones). Proc. Natl. Acad. Sci. USA, 68:1467–1468. Melander, A. L. 1903. Some additions to the Carboniferous terrestrial arthropod fauna of Illinois. J. Geol., 11:178–198. Mello-Leitão, C. F. 1931. Notas sobre Arachnideos argentinos. Annais Acad. bras. Cienc., 3:83–97. Mello-Leitão, C. F. 1932. Opiliões do Brasil. Revta Mus. paul., 17:1–505. Mello-Leitão, C. F. 1933a. Notas sobre os opiliões do Brasil descritos na obra póstuma de Sörensen: “Descriptiones Laniatorum.” Bolm Museu nac. Rio de J., 9:99–114. Mello-Leitão, C. F. 1933b. Quatro novos Palpatores neotropicos. Annais Acad. bras. Cienc., 5:99–103. Mello-Leitão, C. F. 1936. Distribution et phylogénie des faucheurs Sud-Américains. Pp. 1217–1228 in Comptes rendus du XIIe Congrès Internacional de Zoologie (1935), vol. 2. Lisbon, Portugal. Mello-Leitão, C. F. 1938. Considerações sobre os Phalangodoidea Soer. com descrição de novas formas. Annais Acad. bras. Cienc., 10:135–145. Mello-Leitão, C. F. 1944. Comentários a respeito da possível filogenia dos opiliões. Annais Acad. bras. Cienc., 16:197– 209. Mello-Leitão, C. F. 1949. Famílias, subfamílias, espécies e gêneros novos de opiliões e notas de sinonímia. Bolm. Mus. nac. Rio de J., 94:1–33. Melo, A. S., R. A. S. Pereira, A. J Santos, G. J. Shepherd, G. Machado, H. F. Medeiros, & R. J. Sawaya. 2003. Comparing

species richness among assemblages using sample units: why not use extrapolation methods to standardize different sample sizes? Oikos, 101:398–410. Menge, A. 1850. Über die Lebensweise der Afterspinnen. Schriften der naturforschenden Gesellschaft in Danzig, 4:54– 56. Menge, A. 1854. Lebenszeichen vorweltlicher im Bernstein eingeschlossener Tiere. Programm der Petrischule, Danzig. Mestre, L. A., & R. Pinto-da-Rocha. 2004. Population dynamics of an isolated population of the harvestman Ilhaia cuspidata (Opiliones, Gonyleptidae), in Araucaria Forest (Curitiba, Paraná, Brazil). J. Arachnol., 32:208–220. Meyer-Rochow, V. B., & A. R. Liddle. 1988. Structure and function of the eyes of two species of opilionid from New Zealand glow-worm caves (Megalopsalis tumida: Palpatores, and Hendea myersi cavernicola: Laniatores). Proc. R. Soc. B, 233:293–319. Meyer-Rochow, V. B., & A. R. Liddle. 2001. Some ecological and ethological observations on Hendea myersi cavernicola (Chelicerata: Arachnida: Opiliones), a seeing troglobite. Nat. Croat., 10:133–140. Mihál, I. 1998. Harvestmen (Opiliones) of the forest stands and meadows in the Polana Mountain (Slovakia). Ochr. prírody, 16:119–124. [In Slovak] Mihaylov, H. D. 1995. Prouchvane vurhu ekologiyata i biologiyata na pudpuduka—Coturnix coturnix (L.) vuv visokite poleta na Zapadna Bulgaria. Ph.D. Thesis, University of Forestry (LTU), Sofia, Bulgaria. Miller, P. L. 1977. Neurogenic pacemakers in the legs of Opiliones. Physiol. Ent., 2:213–224. Millot, J. 1926. Contribution à l’histophysiologie des Aranéides. Bull. Biol. Fr. Belg., suppl. 8:1–238. Millot, J. 1949. Morphologie générale et anatomie interne. Pp. 263–319 in Traité de Zoologie, vol. 6 (P-P. Grassé, ed.). Masson et Cie, Paris. Millot, J., & O. Tuzet. 1934. La spermatogenèse chez les pédipalpes. Bull. Biol. Fr. Belg., 68:77–83. Milstead, W. W. 1958. A list of the arthropods found in the stomachs of whiptail lizards from four stations in southwestern Texas. Tex. J. Sci., 10:443–446. Mirza, R. S., & D. P. Chivers. 2001. Learned recognition of heterospecific alarm signals: the importance of a mixed predator diet. Ethology, 107:1007–1018. Mitchell, R. W. 1971. Egg and young guarding by a cavedwelling harvestman, Hoplobunus boneti (Arachnida). SWest. Nat., 15:392–395. Mitchell, R. W., & J. R. Reddell. 1971. The invertebrate fauna of Texas caves. Pp. 35–90 in Natural History of Texas Caves (E. L. Lundelius & B. H. Slaughter, eds.). Gulf Natural History, Dallas. Mitov, P. G. 1988. Contribution to the study of the food spec-

References

trum of Opiliones. Trav. Sci. Univ. Plovdiv “Paissi Hilendarski,” Biol., 26:483–488. [In Bulgarian with summary in English] Mitov, P. G. 1992. Harvestmen (Opiliones, Arachnida)—carriers of plant and fungus spores. Acta zool. bulg., 43:75– 77. Mitov, P. G. 1993. Opiliones (Arachnida) from the Kindo Peninsula in Russia. Pp. 69–72 in Second National Scientific Conference of Entomology (G. Tsankov, V. Pelov, V. Beshovski, & A. Popov, eds.). Sofia, Bulgaria. Mitov, P. G. 1995. Opiliones (Arachnida) as a component of the food stuffs of some animals. Annuaire de l’Université de Sofia, Faculté de Biologie, livre 1, Zoologie, 86–87:67–74. Mitov, P. G. 1997a. Einige neue und interessante Phoresie-Fälle bei bulgarischen Opiliones (Arachnida). Arachnol. Mag., 5:1–6. Mitov, P. G. 1997b. Eine neue Nelima Roewer aus Bulgarien (Arachnida, Opiliones, Phalangiidae). Spixiana, 20:97–105. Mitov, P. G. 2000a. Contribution to the knowledge of the harvestmen (Arachnida: Opiliones) of Albania. Ekológia, 19(suppl. 3):159–170. Mitov, P. G. 2000b. Faunistic, biological and ecological investigations on the Opiliones from Vitosha Mt. with some zoogeographical notes. Ph.D. Thesis, University of Plovdiv “Paissi Hilendarski,” Plovdiv, Bulgaria. Mitov, P. G. 2003. Rare and endemic harvestmen (Opiliones, Arachnida) species from the Balkan Peninsula. II. Three species new for the Bulgarian fauna with zoogeographical notes. Linzer biol. Beitr., 35:273–288. Mitov, P. G. 2004. Harvestmen (Arachnida: Opiliones) of the Eastern Rhodopes (Bulgaria). Pp. 167–179 in Biodiversity of Bulgaria, vol. 2: Biodiversity of Eastern Rhodopes (Bulgaria and Greece) (P. Beron & A. Popov, eds.). Pensoft & National Museum of Natural History, Sofia. Mitov, P. G., & I. L. Stoyanov. 2004. The harvestmen-fauna (Opiliones, Arachnida) of the city of Sofia (Bulgaria) and its surroundings. Pp. 319–354 in Ecology of the City of Sofia: Species and Communities in an Urban Environment (L. Penev, J. Niemela, J. Kotze, & N. Chipev, eds.). Pensoft Publishers, Sofia. Mittmann, B., & G. Scholtz. 2003. Development of the nervous system in the “head” of Limulus polyphemus (Chelicerata: Xiphosura): morphological evidence for the correspondence between the segments of the chelicera and of the (first) antennae of Mandibulates. Develop. Genes Evol., 213:9–17. Miura, I., H. Ohtani, M. Nakamura, Y. Ichikawa, & K. Saitoh. 1998. The origin and differentiation of the heteromorphic sex chromosomes Z, W, X and Y of the frog Rana rugosa, inferred from the sequences of a sex-linked gene, ADP/ATP translocase. Mol. Biol. Evol., 15:1612–1619.

553

Miyosi, Y. 1941. Reproduction and post-embryonic development in the Japanese laniatorid Pseudobiantes japonicus. Acta arachnol., 6:98–107. [In Japanese] Miyosi, Y. 1942. Morphological modifications through growth of Ischyropsalis abei Sato & Suzuki. Acta arachnol., 7:109– 120. [In Japanese] Moffett, T. 1634. Insectorum, sive, Minimorum animalium theatrum. Olim ab Edoardo Wottono, Conrado Gesnero, Thomaque Pennio. Londini: Ex officinâ typographicâ Thom. Cotes, 1634. Möller, A. 1901. Phycomyceten und Ascomyceten: Untersuchungen aus Brasilien. Pp. 1–319 in Botanische Mittheilungen aus den Tropen, vol. 9 (A. F. W. Schimper, ed.). Gustav Fischer, Jena. Mommertz, S., C. Schauer, N. Kösters, A. Lang, & J. Filser. 1996. A comparison of D-Vac suction, fenced and unfenced trap sampling of epigeal arthropods in agroecosystems. Annls ent. fenn., 33:117–124. Moore, J. E., & E. H. Strickland. 1954. Notes on the food of three species of Alberta amphibians. Am. Mid. Nat., 52:221– 224. Mora, G. 1987. Male egg-guarding behavior in the Neotropical harvestman, Zygopachylus albomarginis (Opiliones: Gonyleptidae). M.Sc. Thesis, University of Florida, Gainesville. Mora, G. 1990. Parental care in a Neotropical harvestman, Zygopachylus albomarginis (Arachnida, Opiliones: Gonyleptidae). Anim. Behav., 39:582–593. Mora, G. 1991. Site-based mating system in a tropical harvestman. Ph.D. Thesis, University of Florida, Gainesville. Morel, G. 1978. Les maladies microbiennes des arachnids (Acariens exceptés). Symp. Zool. Soc. London, 42:477–481. Moritz, M. 1957. Zur Embryonalentwicklung der Phalangiiden (Opiliones, Palpatores) unter besonderer Berücksichtigung der ausseren Morphologie, der Bildung des Mitteldarmes und der Genitalanlage. Zool. Jb., Abt. Anat. u. Ont. Tiere, 76:331–370. Moritz, M. 1959. Zur embryonalentwicklung der Phalangiiden (Opiliones; Palpatores). II. Die Anlage und Entwicklung der Coxaldrüse bei Phalangium opilio L. Zool. Jb., Abt. Anat. u. Ont. Tiere, 77:229–240. Moritz, M. 1993. Ordnung Opiliones, Weberknechte, Kanker. Pp. 402–421 in Lehrbuch der speziellen Zoologie, vol. 1, (pt. 4: Arthropoda, ohne Insekten (H.-E. Gruner, ed.). Gustav Fischer, Jena. Moroschenko, N. W. 1986. The biology of the Siberian thrush’s breeding in the south seaboard of Lake Baikal. Vestnik Leningrad Univ., ser. 3, 2:19–24. [In Russian] Morrone, J. J. 2001. Biogeografía de América Latina y el Caribe. M&T—Manuales & Tesis SEA, vol. 3. Zaragoza. Morrow, E. H. 2004. How the sperm lost its tail: the evolution of anagellate sperm. Biol. Rev. 79:795–814.

554

References

Morse, D. H. 2001. Harvestmen as commensals of crab spiders. J. Arachnol., 29:273–275. Moseley, M., & A. Hebda. 2001. Overwintering Leiobunum elegans (Opiliones: Phalangiidae) in caves and mines in Nova Scotia. Proc. NS Inst. Sci., 41:216–218. Muchmore, W. B. 1971. Phoresy by North and Central American pseudoscorpions. Proc. Rochester Acad. Sci., 12:79– 97. Müller, A. 1924. Zur Anatomie einiger Arten des Genus Ischyropsalis C. L. Koch nebst vergleichend-anatomischen Betrachtungen. Zool. Jb., Abt. Anat. u. Ont. Tiere, 45:405– 518. Müller, A. 1925. Zur Kenntnis der Jugendformen einiger Opilioniden. Senckenbergiana, 7:210–224. Müller, H. J. 1925. Why polyploidy is rarer in animals than in plants. Am. Nat., 59:346–353. Muñoz, E., F. Perfectti, A. Martin-Alganza, & J. P. M. Camacho. 1998. Parallel effects of a B chromosome and a mite that decrease female fitness in the grasshopper Eyprepocnemis plorans. Proc. R. Soc. B, 265:1903–1909. Muñoz-Cuevas, A. 1969. Recherches sur les opilions (Arachnida, Gonyleptidae) du Chili. I. Description d’une nouvelle espèce: Pachylus quinamavidensis et remarques sur la morphologie génitale du genre Pachylus C. L. Koch. Bull. Mus. Hist. nat. Paris, ser. 2, 41:490–497. Muñoz-Cuevas, A. 1971a. Contribution à l’étude du développement postembryonnaire de Pachylus quinamavidensis Muñoz Cuevas (Arachnides, Opilions, Laniatores). Bull. Mus. Hist. nat. Paris, ser. 3, 12:629–641. Muñoz-Cuevas, A. 1971b. Étude du développement embryonnaire chez Pachylus quinamavidensis (Arachnida, Opiliones, Laniatores). Bull. Mus. Hist. nat. Paris, ser. 2, 42:1238– 1250. Muñoz-Cuevas, A. 1971c. Étude du tarse, de l’apotele et de la formation des griffes au cours du développement postembryonnaire chez Pachylus quinamavidensis (Arachnida, Opiliones, Gonyleptidae). Bull. Mus. Hist. nat. Paris, ser. 2, 42:1027–1036. Muñoz-Cuevas, A. 1973. Embryogenèse, organogenèse et rôle des organes ventraux et neuraux de Pachylus quinamavidensis Muñoz (Arachnides, Opilions, Gonyleptidae): Comparaison avec les Annélides et d’autres Arthropodes. Bull. Mus. Hist. nat. Paris, ser. 3, 196:1517–1537. Muñoz-Cuevas, A. 1978. Différenciation cellulaire du système dioptrique chez Ischyropsalis luteipes (Opiliones, Arachnida). Symp. Zool. Soc. London, 42:399–405. Muñoz-Cuevas, A. 1981. Développement, rudimentation et regression de l’oeil chez les opilions (Arachnida): Recherches morphologiques, physiologiques et experimentes. Mem. Mus. Hist. nat. Paris, ser. A, Zoologie, 120:1–117. Muñoz-Cuevas, A., & M. Vachon. 1979. Données sur le

dévelopement postembryonnaire du tarse chez les Triaenonychidae et considérations sur la phylogénie de cette famille dans l’Amérique australe (Opilions, Arachnida). Rev. Arachnol., 2:253–257. Münster, G. von. 1836. Mitteilungen, an Professor Bronn gerichtet. Neues Jahrbuch für Mineralogie, Geognosie, Geologie und Petrefaktenkunde, 1836:580–583. Murphree, C. S. 1987. Two leaf litter phalangids from Short Mountain (Cannon County), Tennessee. J. Tenn. Acad. Sci., 62:93–94. Murphree, C. S. 1988. Morphology of the dorsal integument of ten opilionid species (Arachnida, Opiliones). J. Arachnol., 16:237–252. Naisse, J. 1959. Neurosécrétion et glandes endocrines chez les opilions. Arch. Biol., 70:217–264. Nawar, M. S., G. M. Shereef, & M. A. Ahmed. 1993. Influence of food on development and reproduction of Hypoaspis solimani n.sp. (Acari, Laelapidae). Insect Sci. Appl., 14:343– 349. Nechaev, V. A. 1974. Trudy Biologicheskogo—pochvenn. Instituta, Akad. Nauk SSSR, 17:120–135. Nentwig, W. 1980. Zur ökologischen Bedeutung des Beutefanges netzbauender Spinnen. Pp. 139–143 in Proceedings of the 8th International Congress of Arachnology (J. Gruber, ed.). Verlag H. Egermann, Vienna. Nentwig, W. 1983. The prey of web-building spiders compared with feeding experiments (Araneae: Araneidae, Linyphiidae, Pholcidae, Agelenidae). Oecologia, 56:132–139. Nentwig, W., ed. 1987. Ecophysiology of Spiders. SpringerVerlag, Berlin. Newell, I. M. 1943. A new sironid from North America (Opiliones, Cyphophthalmi, Sironidae). Trans. Am. Micr. Soc., 62:416–422. Newell, I. M. 1947. The rediscovery and clarification of Siro acaroides (Ewing) (Opiliones, Cyphophthalmi, Sironidae). Trans. Am. Micr. Soc., 66:354–365. Newton, B. L., & K. V. Yeargan. 2001. Predation of Helicoverpa zea (Lepidoptera: Noctuidae) eggs and first instars by Phalangium opilio (Opiliones: Phalangiidae). J. Kans. Ent. Soc., 74:199–204. Nikolov, B. P. 2002. Diet of the red-backed shrike Lanius collurio in Bulgaria. Acrocephalus, 23:21–26. Nishiguchi, M. K., P. Doukakis, M. Egan, D. Kizirian, A. Phillips, L. Prendini, H. C. Rosenbaum, E. Torres, Y. Wyner, R. DeSalle, & G. Giribet. 2002. DNA isolation procedures. Pp. 247–287 in Techniques in Molecular Systematics and Evolution (R. DeSalle, G. Giribet, & W. Wheeler, eds.). Birkhäuser Verlag, Basel. Novak, T., & J. Gruber. 2000. Remarks on published data on harvestmen (Arachnida: Opiliones) from Slovenia. Annales (Koper) Ser. hist. nat., 2:281–308.

References

Novak, T., J. Gruber, & L. Slana. 1985. Remarks on Opiliones from cavities in Slovenia (Yugoslavia). Mém. Biospéol., 11:185–197. Novak, T., S. Lipovsek, L. Sencic, M. A. Pabst, & F. Janzekovic. 2004. Adaptations in phalangiid harvestmen Gyas annulatus and Gyas titanus to their prefered water current adjacent habitats. Acta Oecol., 26:45–53. Novak, T., L. Slana, N. Cervek, M. Mlakar, N. Zmaher, & J. Gruber. 2002. Harvestmen (Opiliones) in human settlements of Slovenia. Acta Ent. Slovenica, 10:133–156. Nyffeler, M., & W. O. C. Symondson. 2001. Spiders and harvestmen as gastropod predators. Ecol. Ent., 26:617–628. Obrtel, R. 1973a. Animal food of Apodemus flavicollis in a lowland forest. Zool. Listy, 22:15–30. Obrtel, R. 1973b. Animal food of Clethrionomys glareolus in a lowland forest. Zool. Listy, 22:111–126. Obrtel, R. 1974. Comparison of animal food eaten by Apodemus flavicollis and Clethrionomys glareolus in a lowland forest. Zool. Listy, 23:35–46. Obrtel, R. 1976. Soil surface harvestmen (Opilionidea) in a lowland forest. Acta Sc. Nat. Brno, 10:1–34. Obrtel, R., & V. Holisová. 1974. Trophic niches of Apodemus flavicollis and Clethrionomys glareolus in a lowland forest. Acta Sc. Nat. Brno, 8:1–37. Obrtel, R., & V. Holisová. 1979. The food eaten by Apodemus sylvaticus in a spruce monoculture. Folia Zool., 28:299–310. Obrtel, R., & V. Holisová. 1980. The food eaten by Apodemus flavicollis in a spruce monoculture. Folia Zool., 29:21–32. Obrtel, R., & V. Holisová. 1983. Winter and spring diets of three coexisting Apodemus spp. Folia Zool., 32:291–302. Ohno, S., 1970. Evolution by Gene Duplication. Springer-Verlag, Berlin. Okada, T., & N. Tsurusaki. 2004. Interspecific variation of sex ratio, copulatory duration, and duration of postcopulatory mate guarding in gagrellid harvestmen and its implications for the evolution of post-copulatory mate guarding and sexual isolation. P. 83 in 16th International Congress of Arachnology. Ghent, Belgium. Økland, S., A. Tjonneland, & B. Midtun. 1983. Heart ultrastructure in Mitopus morio L. (Chelicerata, Opiliones). Zool. Anz., 210:145–154. Oliveira, R. M., A. A. Zacaro, D. M. Cella, P. Gnaspini, & R. Pinto-da-Rocha. 2000. Mitotic and meiotic chromosomes of three harvestmen species, Goniosoma spelaeum, Neosadocus sp. and Pseudopachylus sp. (Arachnida, Opiliones, Laniatores), using standard and silver staining. Genet. Mol. Biol., 23:41. Oliver, J. H., Jr. 1981. Sex chromosomes, parthenogenesis, and polyploidy in ticks. Pp. 66–77 in Evolution and Speciation: Essays in Honor of M. J. D. White (W. A. Atchley & D. S. Woodruff, eds.). Cambridge University Press, Cambridge.

555

Oliver, J. H., Jr. 1989. Biology and systematics of ticks (Acari: Ixodidae). Ann. Rev. Ecol. Syst., 20:397–430. O’Neill, K. M. 2001. Solitary Wasps: Behavior and Natural History. Cornell University Press, Ithaca, NY. Opell, B. D. 1998. The respiratory complementarity of spider book lung and tracheal systems. J. Morphol., 236:57–64. Orians, G. H. 1966. Food of nestling yellow-headed blackbirds, Cariboo Parklands, British Columbia. Condor, 68:321– 337. Oromí, P., & I. Izquierdo. 1994. Canary Islands. Pp. 631–639 in Encyclopaedia biospeologica (C. Juberthie & V. Decu, eds.). Société de Biospéologie, Moulis. Owen, D. F. 1991. Opiliones (Arachnida) at a single site: ten years of monitoring. Ent. Mon. Mag., 127:107–108. Owens, I. P. E., & D. B. A. Thompson. 1994. Sex differences, sex ratios and sex roles. Proc. R. Soc. B, 258:93–99. Pabs-Garnon, E. B. 1977. The external morphology and life history of Ogovea grossa (Cyphophthalmi, Opiliones, Arachnida). M.Sc. Thesis, University of Sierra Leone, Freetown, Sierra Leone. Pabst, W. 1953. Zur Biologie der mitteleuropäischen Troguliden. Zool. Jb., Abt. Syst., Ökol. u. Geog. Tiere, 82:1– 156. Packard, A. S. 1884. New cave arachnids. Am. Nat., 18:202– 204. Packard, G. C., & R. K. Stiverson. 1975. Geographic variation in physiological characters of the arachnid Leiobunum longipes: has a case been made? Syst. Zool., 24:111–113. Painter, T. S. 1914. Spermatogenesis in spiders. Zool. Jb., Abt. Anat. u. Ont. Tiere, 38:509–571. Palumbi, S. R. 1996. Nucleic acids II: the polymerase chain reaction. Pp. 205–247 in Molecular Systematics, 2nd ed. (D. M. Hillis, C. Moritz, & B. K. Mable, eds.). Sinauer Associates, Sunderland. Panzer, G. W. F. 1794. Phalangium hellwigii: Die hellwigsche Afterspinne. Faunae Insectorum Germanicae Initia oder Deutschlands Insecten, 13:18. Parisot, C. 1962. Étude de quelques opilions de Lorraine. Vie et Milieu, 13:179–197. Parker, G., & L. Simmons. 1996. Parental investment and the control of sexual selection: predicting the direction of sexual competition. Proc. R. Soc. B, 263:315–321. Parthasarathy, M. D., & C. J. Goodnight. 1958. The chromosomal patterns of some Opiliones (Arachnidae). Trans. Am. Micr. Soc., 77:353–364. Paulus, H. F. 1979. Eye structure and the monophyly of Arthropoda. Pp. 299–383 in Arthropod Phylogeny (A. P. Gupta, ed.). Van Nostrand Reinhold, New York. Pavesi, P. 1899. Un nuovo Nemastomide Americano. Rendiconti, Reale Istituto Lombardo di Scienze e Lettere, ser. 2, 32:530–533.

556

References

Pearson, R. G., & E. White. 1964. The phenology of some surface-active arthropods of moorland country in North Wales. J. Anim. Ecol., 33:245–258. Pechácek, P., & A. Kristín. 1996. Zur Ernährung und Nahrungsökologie des Dreizehnspechts Picoides tridactylus während der Nestligsperiode. Ornithol. Beobachter, 93: 259–266. Peck, S. B. 1974. The food of the salamanders Eurycea lucifuga and Plethodon glutinosus in caves. Nat. Speleol. Soc. Bull., 36:7–10. Peck, S. B., & B. L. Richardson. 1976. Feeding ecology of the salamander Eurycea lucifuga in the entrance, twilight, and dark zones of caves. Ann. Spéléol., 31:175–182. Pedrocchi-Renault, C. 1985. Los artópodos epigeos del macizo de San Juan de Peña (Jaca, Huesca). I. Introducción general a su estudio. Pirineos, 124:5–52. Pekár, S. 1997a. Effect of liquid fertilizer (UAN) combined with deltamethrin on beneficial arthropods in spring barley. Ochr. Rostl., 33:257–264. Pekár, S. 1997b. Short-term effect of liquid fertilizer (UAN) on beneficial arthropods (Aranea, Opilionida, Carabidae, Staphylinidae) in winter wheat. Ochr. Rostl., 33:17–24. Pekár, S. 2002. Differential effects of formaldehyde concentration and detergent on the catching efficiency of surface active arthropods by pitfall traps. Pedobiologia, 46:539– 547. Pekár, S., J. Kazda, & K. Veverka. 1997. Effect of an organophosphate insecticide combined with a liquid fertiliser (UAN) on some pests (Aphidoidea, Chrysomelidae) and beneficial arthropods (Araneae, Opiliones) in winter wheat stands. Sci. Agric. Bohemica, 28:271–281. Pellegatti-Franco, F., & P. Gnaspini. 1996. Use of caves by Philander opossum (Mammalia: Didelphidae) in southeastern Brazil. Papéis Avulsos Zool., 39:351–364. Penney, D. 1999. Hypotheses for the recent Hispaniolan spider fauna based on the Dominican Republic amber spider fauna. J. Arachnol., 27:64–70. Pereira, W., A. Elpino-Campos, K. Del-Claro, & G. Machado. 2004. Behavioral repertory of the Neotropical harvestman Ilhaia cuspidata (Opiliones, Gonyleptidae). J. Arachnol., 32:22–30. Pérez G., A., & A. B. Kury. 2002. A new remarkable troglomorphic gonyleptid from Brazil (Arachnida, Opiliones, Laniatores). Rev. Ibér. Aracnol., 5:43–50. Pérez González, A., & L. F. de Armas. 2000. A new species of the genus Kimula (Opiliones, Minuidae) from the Dominican Republic. J. Arachnol., 28:257–260. Perner, J., & S. Schueler. 2004. Estimating the density of ground-dwelling arthropods with pitfall traps using a nested-cross array. J. Anim. Ecol., 73:469–477. Pernetta, J. C. 1976. Diets of the shrews Sorex araneus L. and

Sorex minutus L. in Wytham grassland. J. Anim. Ecol., 45:899–912. Pernetta, J. C. 1977. Anatomical and behavioural specialisations of shrews in relation to their diet. Canad. J. Zool., 55:1442–1453. Perrier, R. 1929. La faune de la France en tableaux synoptiques illustrés. Fasc. 2: Arachnides et crustacés. Delagrave, Paris. Perty, M. 1833. Delectus animalium articulatorum quae in itinere per Brasiliam annis 1817–1820 peracta collegerunt J. B. de Spix et C. F. Ph. de Martius. Munich. Peters, W. 1967. Bildung und Struktur peritrophischer Membranen bei Phalangiiden (Opiliones, Chelicerata). Z. Morph. und Ökol. Tiere, 59:134–142. Peters, W. 1992. Peritrophic Membranes. Springer-Verlag, Berlin. Petranka, J. W. 1998. Salamanders of the United States and Canada. Smithsonian Institution Press, Washington, DC. Petrochenko, V. I. 1992. O pitanii turkestanskoy agamuy. Byulleten’ Moskovskogo Obshchestva Ispytatelei Priroduy, Otdel Biologicheskii, 97:26–33. Petrunkevitch, A. I. 1913. A monograph of the terrestrial Palaeozoic Arachnida of North America. Trans. Conn. Acad. Arts Sci., 18:1–137. Petrunkevitch, A. I. 1922. Tertiary spiders and opilionids of North America. Trans. Conn. Acad. Arts Sci., 25:211–279. Petrunkevitch, A. I. 1949. A study of Palaeozoic Arachnida. Trans. Conn. Acad. Arts Sci., 37:69–315. Petrunkevitch, A. I. 1953. Paleozoic and Mesozoic Arachnida of Europe. Mem. Geol. Soc. Am., 53:1–125. Petrunkevitch, A. I. 1955. Arachnida. Pp. 42–162 in Treatise on Invertebrate Palaeontology, pt. P, Arthropoda 2 (R. C. Moore, ed.). Geological Society of America & University of Kansas Press, Lawrence. Petrunkevitch, A. I. 1958. Amber spiders in European collections. Trans. Conn. Acad. Arts Sci., 41:97–400. Petrusenko, A. A., & V. S. Talposh. 1981. Ekologicheskie osebennosti pitaniya ptentsov soroki—Pica pica (L.) v usloviyah zapadnogo Podolya. Vestnik Zool., 5:52–57. Petto, R. 1990. Abundance and prey of Coelotes terrestris (Wider) (Araneae, Agelenidae) in hedges. Bul. Br. Arachnol. Soc., 8:185–193. Pfeifer, H. 1956. Zur Ökologie und Larvalsystematik der Weberknechte. Mitt. naturh. Mus. Berlin, 32:59–104. Phillipson, J. 1959. The seasonal occurrence, life histories and fecundity of harvest-spiders (Phalangida, Arachnida) in the neighborhood of Durham City. Ent. Mon. Mag., 95:134–138. Phillipson, J. 1960a. A contribution to the feeding biology of Mitopus morio (F.) (Phalangida). J. Anim. Ecol., 29:35–43.

References

Phillipson, J. 1960b. The food consumption of different instars of Mitopus morio (F.) (Phalangida) under natural conditions. J. Anim. Ecol., 29:299–307. Phillipson, J. 1961. Histological changes in the gut of Mitopus morio (Phalangiida) during protein digestion. Q. J. Microsc. Sci., 102:217–226. Phillipson, J. 1962a. Histological changes in the gut and associated tissues of Mitopus morio (Phalangiida) during digestion of lipid and carbohydrate. Q. J. Microsc. Sci., 103:85– 91. Phillipson, J. 1962b. Respirometry and the study of energy turnover in natural systems with particular reference to harvestspiders (Phalangida). Oikos, 13:311–322. Phillipson, J. 1963. The use of respirometry data in estimating annual respiratory metabolism, with particular reference to Leiobunum rotundum (Latr.) (Phalangida) Oikos, 14:212–223. Pickard-Cambridge, O. 1890a. Monograph of the British Phalangidea or Harvestmen. Sime, Dorchester. Pickard-Cambridge, O. 1890b. On the British species of Phalangidea, or harvestmen. Proc. Dorset Nat. Hist. Field Club, 11:163–216. Pickard-Cambridge, P. 1875. On three new and curious forms of Arachnida. Ann. Mag. Nat. Hist., ser. 4, 16:383–390. Pijnacker, L. P., & M. A. Ferwerda. 1975. Maturation divisions with double the somatic chromosome number in the privet mite Brecipalpus oboratus. Experientia, 31:421–422. Pinto-da-Rocha, R. 1993. Invertebrados cavernícolas da porção meridional da Província Espeleológica do Vale do Ribeira, Sul do Brasil. Revta bras. Zool., 10:229–255. Pinto-da-Rocha, R. 1995a. Redescription of Stenostygnus pusio Simon and synonymy of Caribbiantinae with Stenostygninae (Opiliones: Laniatores, Biantidae). J. Arachnol., 23:194–198. Pinto-da-Rocha, R. 1995b. Sinopse da fauna cavernícola do Brasil. Papéis Avulsos Zool., 39:61–173. Pinto-da-Rocha, R. 1996a. Biological notes on and population size of Pachylospeleus strinatii Silhavy, 1974 in the Gruta das Areias de Cima, Iporanga, south-eastern Brazil (Arachnida, Opiliones, Gonyleptidae). Bul. Br. Arachnol. Soc., 10:189–192. Pinto-da-Rocha, R. 1996b. Description of the male of Daguerreia inermis Soares & Soares, with biological notes on population size in the Gruta da Lancinha, Paraná, Brazil (Arachnida, Opiliones, Gonyleptidae). Revta bras. Zool., 13:833–842. Pinto-da-Rocha, R. 1996c. Notes on Vima insignis Hirst, 1912, revalidation of Trinella Goodnight & Goodnight, 1947 with description of three new species (Arachnida, Opiliones, Agoristenidae). Revta bras. Ent., 40:315–323. Pinto-da-Rocha, R. 1997. Systematic review of the Neotrop-

557

ical family Stygnidae (Opiliones, Laniatores, Gonyleptoidea). Arq. Zool., 33:163–342. Pinto-da-Rocha, R. 1999. Opiliones. Pp. 35–44 in Biodiversidade do Estado de São Paulo, Brasil: Invertebrados terrestres (C. R. F. Brandão & E. M. Cancello, eds.). FAPESP, São Paulo. Pinto-da-Rocha, R. 2002. Systematic review and cladistic analysis of the Caelopyginae (Opiliones, Gonyleptidae). Arq. Zool., 36:357–464. Pinto-da-Rocha, R. 2004. A new Fissiphaliidae from Brazilian Amazon rain forest (Arachnida; Opiliones). Zootaxa, 640:1–6. Pinto-da-Rocha, R., & A. B. Kury 2003a. Phylogenetic analysis of Santinezia with description of five new species (Opiliones, Laniatores, Cranaidae). J. Arachnol., 31:173–208. Pinto-da-Rocha, R., & A. B. Kury 2003b. Third species of Guasiniidae (Opiliones, Laniatores) with comments on familial relationships. J. Arachnol., 31:394–399. Pinto-da-Rocha, R., M. B. da Silva, & C. Bragagnolo. 2005. Faunistic similarity and biogeography of the harvestmen of southern and southeastern Atlantic rain forest of Brazil. J. Arachnol., 33:290–299. Pitnick, S., & W. D. Brown. 2000. Criteria for demonstrating female sperm choice. Evolution, 54:1052–1056. Plowman, A. B., & S. M. Bougourd. 1994. Selectively advantageous effects of B chromosomes on germination behaviour in Allium schoenoprasum L. Heredity, 72:587–593. Pocock, R. I. 1902a. On some new harvest-spiders of the order Opiliones from the southern continents. Proc. Zool. Soc. Lond., 1902:392–413. Pocock, R. I. 1902b. Some points in the morphology and classification of the Opiliones. Ann. Mag. Nat. Hist., ser. 7, 10:504–516. Pocock, R. I. 1902c. Studies on the arachnid endosternite. Q. J. Microsc. Sci., 46:225–262. Pocock, R. I. 1911. A Monograph of the Terrestrial Carboniferous Arachnida of Great Britain. Monographs of the Palaeontographical Society, London. Poinar, G. O., Jr. 1985. Mermethid (Nematoda) parasites of spiders and harvestmen. J. Arachnol., 13:121–128. Poinar, G. O., Jr., 1992. Life in Amber. Stanford University Press, Stanford, CA. Poinar, G. O., Jr., B. P. M. Curcic, & J. C. Cokendolpher. 1998. Arthropod phoresy involving pseudoscorpions in the past and present. Acta arachnol., 47:79–96. Poinar, G. O., Jr., B. P. M. Curcic, I. M. Karaman, J. C. Cokendolpher, & P. G. Mitov. 2000. Nematode parasitism of harvestmen (Opiliones: Arachnida). Nematology, 2:587–590. Poinar, G. O., Jr., & J. W. Early. 1990. Aranimermis giganteus n.sp. (Mermithidae: Nematoda), a parasite of New Zealand spiders (Araneae: Arachnida). Rev. Nématol., 13:403–410.

558

References

Poinar, G. O., Jr., & G. M. Thomas. 1984. Laboratory Guide to Insect Pathogens and Parasites. Plenum Press, New York. Poinar, G. O., Jr., & G. M. Thomas. 1985. Laboratory infection of spiders and harvestmen (Arachnida: Araneae and Opiliones) with Neoaplectana and Heterorhabditis nematodes (Rhabditoidea). J. Arachnol., 13:297–302. Polis, G. A. 1981. The evolution and dynamics of intraspecific predation. Ann. Rev. Ecol. Syst., 12:225–251. Polis, G. A. 1990. Ecology. Pp. 247–293 in The Biology of Scorpions (G. A. Polis, ed.). Stanford University Press, Stanford, CA. Polis, G. A. 1993. Scorpions as model vehicles to advance theories of population and community ecology: the role of scorpions in desert communities. Mem. Queensland Mus., 33:401–410. Pollard, S. D., & R. R. Jackson. 2004. Gastropod predation in spiders (Araneae). Pp. 497–503 in Natural Enemies of Terrestrial Molluscs (G. M. Barker, ed.). Oxford University Press, Oxford. Polz, H. 1975. Zur Unterscheidung von Phyllosomen und deren Exuvien aus den Solnhofener Plattenkalken. Neues Jahrbuch für Mineralogie, Geognosie, Geologie und Petrefaktenkunde, 1975:40–50. Pope, C. H. 1950. A statistical and ecological study of the salamander Plethodon yonahlossee. Bull. Chicago Acad. Sci., 9:79–106. Powders, V. N., & W. L. Tietjen. 1974. The comparative food habits of sympatric and allopatric salamanders, Plethodon glutinosus and Plethodon jordani in eastern Tennessee and adjacent areas. Herpetologica, 30:167–175. Prendini, L., R. Hanner, & R. DeSalle. 2001. Obtaining, storing, and archiving specimens and tissue samples for use in molecular studies. Pp. 176–248 in Techniques in Molecular Systematics and Evolution (R. DeSalle, G. Giribet, & W. Wheeler, eds.). Birkhauser Verlag, Basel. Presl, J. S. 1822. Additamenta ad faunam protogaeam, sistens descriptiones aliquot animalium in succino inclusorum. In Deliciae Pragenses historiam naturalem spectantes (J. S. Presl & C. B. Presl, eds.). Prague. Prieto, C. E. 1990a. The genus Ischyropsalis C. L. Koch (Opiliones, Ischyropsalididae) on the Iberian Peninsula. I. Nontroglobitic species. Acta zool. fenn., 190:315–320. Prieto, C. E. 1990b. The genus Ischyropsalis C. L. Koch (Opiliones, Ischyropsalididae) on the Iberian Peninsula. II: Troglobitic species. Bull. Soc. Europ. Arachnol., hors série, 1:286–292. Prieto, C. E. 2004. El género Nemastomella Mello-Leitao 1936 (Opiliones: Dyspnoi: Nemastomatidae) en la Península Ibérica, con descripción de la primera especie de Andalucía. Rev. Ibér. Aracnol., 9:107–121. Prieto Trueba, D., & E. Bauzá Ferré. 1999. Primer registro de la

familia Erythraeidae (Acari: Prostigmata) para Cuba. Cocuyo, 8:21. Proctor, H. C. 1998. Indirect sperm transfer in arthropods: behavioral and evolutionary trends. Ann. Rev. Ent., 43:153– 74. Prokofyeva, I. V. 1961. O doli razlichnuyh bespozvonochnuyh i pozvonochnuyh zhivotnuyh v pitanii ptencov nekotoruyh lesnuyh ptic. Doklady Akademii nauk SSSR, Izd. AN SSSR, M., Zoologiya, 136:497–499. Pugsley, C. W. 1984. Ecology of the New Zealand glowworm (Arachnocampa luminosa) (Diptera: Keroplatidae), in the glowworm cave at Waitomo. JR Soc. NZ, 14:387–407. Pulz, R. 1987. Thermal and water relations. Pp. 26–55 in Ecophysiology of Spiders (W. Nentwig, ed.). Springer-Verlag, Berlin. Punzo, F. 1983. Hemolymph chemistry of the spiders, Heteropoda venatoria (Sparassidae), Pisaurina mira (Pisauridae) and Amaurobius benetti (Amaurobiidae). Comp. Biochem. Physiol., 75A:647–652. Punzo, F. 1998. The Biology of Camel Spiders (Arachnida, Solifugae). Kluwer Academic Publishers, The Netherlands. Purcell, W. F. 1892. Über den Bau und die Entwicklung der Phalangiden-Augen. Zool. Anz., 15:461–465. Purcell, W. F. 1894. Über den Bau der Phalangidenaugen. Z. wiss. Zool., 58:1–53. Queller, D. C. 1997. Why do females care more than males? Proc. R. Soc. B, 264:1555–1557. Rabitsch, W. B. 1995. Metal accumulation in arthropods near a lead/zinc smelter in Arnoldstein, Austria. III. Arachnida. Environ. Pollut., 90:249–257. Rambla, M. 1968. Sobre el género Crosbycus Roewer, 1914 (Opiliones, fam. Nemastomatidae). Publicaciones del Instituto de Biologia Aplicada, 44:65–80. Rambla, M. 1972. Opiliones (Arach.) de las Baleares. Rapport et proces-verbal des reunions, Commission internationale pour l’exploration scientifique de la Mer Méditerranée, 21:89–92. Rambla, M. 1973. Contribución al conocimiento de los Opiliones de la fauna ibérica: estudio de los subórdenes Laniatores y Palpatores (pars.). Resumen de la Tesis Doctoral. Secretaría Pública de la Universidad de Barcelona, España. Rambla, M. 1974. Los Opiliones (Arachnida), 1a parte. Graelsia, 28:123–145. Rambla, M. 1977. Un nuevo Scotolemon cavernícola de la isla de Mallorca. Speleon, 23:7–13. Rambla, M. 1980a. Les Nemastomatidae (Arachnida, Opilions) de la Péninsule Ibérique. V. Nemastoma scabriculum Simon, 1979 et Nemastoma hankiewiczii Kulczynski, 1909. Pp. 147–158 in Comptes rendus de la Ve Colloque d’Arachnologie d’Expression Française (1979). Barcelona, Spain. Rambla, M. 1980b. Neoteny in Opiliones. Pp. 489–492 in Pro-

References

ceedings of the 8th International Congress of Arachnology (J. Gruber, ed.). Verlag H. Egermann, Vienna. Rambla, M. 1983. Sobre los Nemastomatidae (Arachnida, Opiliones) de la Península Ibérica. VI. Acromitostoma rhinocerus y Acromitostoma hispanum (nueva combinación). Speleon, 26–27:21–27. Rambla, M. 1984. Contributions a l’étude de la faune terrestre des îles granitiques de l’archipel des Sechelles (Mission P. L. G. Benoit–J. J. van Mol, 1972): Opiliones (Arachnida). Annalen Koninklijk Museum voor Midden-Afrika Tervuren, Reeks in 8, Zoologische wetenschappen, 242:1–86. Rambla, M. 1985. Artrópodos epigeos del macizo de San Juan de la Peña (Jaca, Huesca). IV. Opiliones. Pirineos, 124:87– 168. Rambla, M. 1991. A new Stylocellus from some caves of Borneo, Malaysia (Opiliones, Cyphophthalmi, Stylocellidae). Mém. Biospéol., 18:227–232. Rambla, M. 1993. Maiorerus randoi n.gen., n.sp., the first laniatorid from a Canary Island cave (Opiliones, Phalangodidae). Mém. Biospéol., 20:177–182. Rambla, M. 1994. Un nouveau Cyphophthalme du sud-est asiatique, Fangensis leclerci n.gen. n.sp. (Opiliones, Sironidae). Mém. Biospéol., 21:109–114. Rambla, M., & C. Juberthie 1994. Opiliones. Pp. 215–230 in Encyclopaedia Biospeologica, vol. 1 (C. Juberthie & V. Decu, ed.). Société de Biospéologie, Moulis. Ramires, E.N., & A. A. Giaretta. 1994. Maternal care in a Neotropical harvestman, Acutisoma proximum (Opiliones, Gonyleptidae). J. Arachnol., 22:179–180. Randall, D. W., W. Buggren, & K. French. 1997. Eckert Animal Physiology: Mechanisms and Adaptations. W. H. Freeman and Co., New York. Rasa, O. A. E. 1997. Aggregation in a desert tenebrionid beetle: a cost/benefit analysis. Ethology, 103:466–487. Raspotnig, G., G. Fauler, M. Leis, & H.-J. Leis. 2005. Chemical profiles of scent gland secretions in the cyphophthalmid opilionid harvestmen, Siro duricorius and S. exilis. J. Chem. Ecol., 31:1353–1368. Raykov, B. E., & M. N. Rimskiy-Korsakov. 1948. Zoologicheskie ekskursii. Uchpedgiz, Moscow. Reddell, J. R., & J. C. Cokendolpher. 2001. Ants (Hymenoptera: Formicidae) from the caves of Belize, Mexico, and California and Texas (USA). Texas Mem. Mus., Speleol. Monogr., 5:129–154. Reinert, B. L., & M. R. Bornschein. 1998. Alimentação da gralha azul (Cyanocorax caeruleus, Corvidae). Ornit. Neotrop., 9:213–217. Reissland, A., & P. Görner 1985. Trichobothria. Pp.138–161 in Neurobiology of Arachnids (F.G. Barth, ed.). Springer-Verlag, Berlin. Reynolds, J. D., N. B. Goodwin, & R. P. Freckleton. 2002. Evolu-

559

tionary transitions in parental care and live bearing in vertebrates. Philos. Trans. R. Soc. Land B. Biol. Sci., 357:269–281. Rice, C. M., N. H. Trewin, & L. I. Anderson. 2002. Geological setting of the early Devonian Rhynie cherts, Aberdeenshire, Scotland: an early terrestrial hot spring system. J. Geol. Soc., 159:203–214. Riddle, W. A. 1985. Hemolymph osmoregulation in several myriapods and arachnids. Comp. Biochem. Physiol., 80A: 313–323. Ridley, M. 1978. Paternal care. Anim. Behav., 20:904–932. Riechert, S. E., & J. Luczak. 1982. Spider foraging: behavioral responses to prey. Pp. 353–385 in Spider Communication: Mechanisms and Ecological Significance (P.N. Witt & J. S. Rovner, eds.). Princeton University Press, Princeton, NJ. Rimsky-Korsakow, A. P. 1924. Die Kugelhaare von Nemastoma lugubre Mull. Zool. Anz., 60:1–16. Ringuelet, R. A. 1953. Opiliones de la Argentina: rehabilitación de los géneros Sympathica M.-L. y Varinodulia C. con la descripción de una especie nueva (Palpatores, Gagrellidae). Revta Soc. ent. argent., 16:37–41. Ringuelet, R. A. 1959. Los arácnidos Argentinos del orden Opiliones. Revista del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia,” 5:127–439. Ringuelet, R. A. 1962. Notas sobre Opiliones. I. Acropsopilio ogloblini Canals en la selva marginal de Punta Lara y la ubicación taxinómica del género Acropsopilio Silvestri. Physis, 23:77–80. Roach, B., T. Eisner, & J. Meinwald. 1980. Defensive substances of opilionids. J. Chem. Ecol., 6:511–516. Robinson, M. 1981. The whistling spider Selenocosmia crassipes (L. Koch, 1874) feeding on raw meat. Newsl. Br. Arachnol. Soc., 32:3–4. Robinson, M. H., & B. Robinson. 1970. Prey caught by a sample population of the spider Argiope argentata (Araneae: Araneidae) in Panama: a year’s census data. Zool. J. Linn. Soc., 49:345–358. Robinson, W. R., & Hewitt, G. 1976. Annual cycles in the incidence of B chromosomes in the grasshopper Myrmeleotettix maculatus (Acrididae—Orthoptera). Heredity, 36:399–412. Rodríguez, C.A., & S. Guerrero. 1976. La historia natural y el comportamiento de Zygopachylus albomarginis (Chamberlin) (Arachnida: Opiliones: Gonyleptidae). Biotropica, 8: 242–247. Roewer, C. F. 1910. Revision der Opiliones Plagiostethi (= Opiliones Palpatores). I. Teil: Familie der Phalangiidae. (Subfamilien: Gagrellini, Liobunini, Leptobunini). Abh. Gebiete Naturwiss. Naturwiss. Verein Hamburg, 19:1–294. Roewer, C. F. 1911. Übersicht der Genera der Subfamilie der Phalangiini der Opiliones Palpatores nebst Beschreibung einiger neuer Gattungen und Arten. Arch. Naturgesch., pt. 1, 77(suppl. 2):1–106.

560

References

Roewer, C. F. 1912a. Die Familie der Cosmetiden der OpilionesLaniatores. Arch. Naturgesch., 78:1–122. Roewer, C. F. 1912b. Die Familien der Assamiiden und Phalangodiden der Opiliones-Laniatores (= Assamiden, Dampetriden, Phalangodiden, Epedaniden, Biantiden, Zalmoxiden, Samoiden, Palpipediden anderer Autoren). Arch. Naturgesch., 78:1–242. Roewer, C. F. 1912c. Revision der Opiliones Palpatores (= Opiliones Plagiostethi). II. Teil: Familie der Phalangiidae (Subfamilien Sclerosomini, Oligolophini, Phalangiini). Abh. Gebiete Naturwiss. Naturwiss. Verein Hamburg, 20:1–295. Roewer, C. F. 1913. Die Familie der Gonyleptiden der Opiliones Laniatores. Arch. Naturgesch., 79:1–473. Roewer, C. F. 1914a. Die Familien der Ischyropsalidae und Nemastomatidae der Opiliones-Palpatores. Arch. Naturgesch., 80:99–169. Roewer, C. F. 1914b. Fünfzehn neue Opilioniden. Arch. Naturgesch., 80:106–132. Roewer, C. F. 1915a. 106 neue Opilioniden. Arch. Naturgesch., 81:1–152. Roewer, C. F. 1915b. Die Familie Triaenonychidae der Opiliones-Laniatores. Arch. Naturgesch., 80:61–168. Roewer, C. F. 1919. Über Nemastomatiden und ihre Verbreitung. Arch. Naturgesch., 83:140–160. Roewer, C. F. 1923. Die Weberknechte der Erde: Systematische Bearbeitung der bisher bekannten Opiliones. Gustav Fischer, Jena. Roewer, C. F. 1927. Weitere Weberknechte I (1. Ergänzung der Weberknechte der Erde, 1923). Abh. naturw. Ver. Bremen, 26:261–402. Roewer, C. F. 1929a. Süd-indische Skorpione, Cheloneti und Opilioniden. Rev. suisse Zool., 36:609–639. Roewer, C. F. 1929b. Weitere Weberknechte III (3. Ergänzung der Weberknechte der Erde, 1923). Abh. naturw. Ver. Bremen, 27:179–290. Roewer, C. F. 1931. Über Triaenonychiden (6. Ergänzung der Weberknechte der Erde, 1923). Z. wiss. Zool., 138:137–185. Roewer, C. F. 1932. Weitere Weberknechte VII (7. Ergänzung der Weberknechte der Erde, 1923). Arch. Naturgesch., 1: 275–350. Roewer, C. F. 1935a. Opiliones (Funfte Serie)—Zugleich eine Revision aller bisher bekannten europäischen Laniatores: LXII Biospeleologica. Arch. Zool. exp. gen., 62:1–96. Roewer, C. F. 1935b. Weitere Weberknechte VIII: Alte und neue Assamiidae. Veröff. Deutsch. Kolonial u. Übersee Mus. Bremen, 1:1–168. Roewer, C. F. 1938. Weitere Weberknechte IX: Über Acrobuninae, Epedaninae und Sarasinicinae. Veröff. Deutsch. Kolonial u. Übersee Mus. Bremen, 2:81–169. Roewer, C. F. 1939. Opilioniden im Bernstein. Palaeobiologica, 7: 1–5. Roewer, C. F. 1940. Neue Assamiidae und Trogulidae: Weitere

Weberknechte X (10. Ergänzung der “Weberknechte der Erde” 1923). Veröff. Deutsch. Kolonial u. Übersee Mus. Bremen, 3:1–31. Roewer, C. F. 1943. Weitere Weberknechte XI: Über Gonyleptiden. Senckenbergiana, 26:12–68. Roewer, C. F. 1947. Diagnosen neuer Gattungen und Arten der Opiliones Laniatores (Arachn.) aus C. F. Roewer’s Sammlung im Senckenberg-Museum. 1. Cosmetidae [Weitere Weberknechte XII]. Senckenbergiana, 28:7–57. Roewer, C. F. 1949. Über Phalangodiden I: Subfam. Phalangodinae, Tricommatinae, Samoinae; Weitere Weberknechte XIII. Senckenbergiana, 30:11–61. Roewer, C. F. 1950. Über Ischyropsalididae und Trogulidae: Weitere Weberknechte XV. Senckenbergiana, 31:11–56. Roewer, C. F. 1951. Über Nemastomatiden: Weitere Weberknechte XVI. Senckenbergiana, 32:96–153. Roewer, C. F. 1952. Neotropische Arachnida Arthrogastra, zumeist aus Peru. Senckenbergiana, 33:37–58. Roewer, C. F. 1953. Neotropische Gagrellinae (Opiliones, Arachnidae) (Weitere Weberknechte XVII). Mitt. zool. Mus. Berl., 29:180–265. Roewer, C. F. 1957a. Arachnida Arthrogastra aus Peru, III. Senckenbergiana Biol., 38:67–94. Roewer, C. F. 1957b. Über Oligolophinae, Caddoinae, Sclerosomatinae, Leiobuninae, Neopilioninae und Leptobuninae (Phalangiidae, Opiliones Palpatores) (Weitere Weberknechte XX). Senckenbergiana Biol., 38:323–358. Roewer, C. F. 1963. Opiliones aus Peru und Colombia (Arachnida Arthrogastra aus Peru V). Senckenbergiana Biol., 44:45–72. Roger, J. 1946. Résultates scientifiques de la mission C. Arambourg en Syrie et en Iran (1938–39): Les invertébrés des Couches à Poissons du Crétacé supérieur du Liban—étude palébiologique des gisements. Mém. Soc. Géol. Fr., Paléontol., 51:60–64. Rolfe, W. D. I., G. P. Durant, W. J. Baird, C. Chaplin, R. L. Paton, & R. J. Reekie. 1994. The East Kirkton Limestone, Viséan, of West Lothian, Scotland: Introduction and stratigraphy. Trans. R. Soc. Edinb., Earth Sci., 84:177–188. Romer, F. 1991. The oenocytes of insects: differentiation, changes during molting and their possible involvement in the secretion of molting hormone. Pp. 542–567 in Morphogenetic Hormones of Arthropods: Roles in Histogenesis, Organogenesis and Morphogenesis (A. P. Gupta, ed.). Rutgers University Press, New Brunswick, NJ. Romer, F., & W. Gnatzy. 1981. Arachnid oenocytes: ecdysone synthesis in the legs of harvestmen (Opilionidae). Cell Tissue Res., 216:449–453. Rosas Costa, J. A. 1950. Sinopsis de los géneros de Sironinae, con la descripción de dos géneros y una especie nuevos (Opiliones, Cyphophthalmi). Arthropoda, 1:127–151.

References

Röschmann, F. 1997. Ökofaunistischer Vergleich von Nematoceren-Faunaen (Insecta; Diptera: Sciaridae und Ceratopogonidae) des baltischen und sächsischen Bernsteins (Tertiär, Oligozän-Miozän). Paläontol. Z., 71:79–87. Ross, A. 1998. Amber, the Natural Time Capsule. NHM Publishing, London. Ross, K. G. 1981. Report of necrophagy in the black widow spider, Latrodectus hesperus (Araneae, Theridiidae). J. Arachnol., 9:109. Rößler, R. 1882. Beiträge zur Anatomie der Phalangiden. Z. wiss. Biol., 36:671–702. Rößler, R., J. A. Dunlop, & J. W. Schneider. 2003. A redescription of some poorly known arachnids from the Lower Permian (Asselian) of the Ilfeld and Thuringian Forest Basins, Germany. Paläontol. Z., 77:417–427. Roters, M. 1944. Observations on British harvestmen. J. Quekett Microsc. Club, ser. 4, 2:23–25. Roth, V. D., & B. M. Roth. 1984. A review of appendotomy in spiders and other arachnids. Bul. Br. Arachnol. Soc., 6:137– 146. Rowell, D. M. 1985. Complex sex-linked fusion heterozygosity in the Australian huntsman spider Delena cancerides (Araneae: Sparassidae). Chromosoma, 93:169–176. Rowell, D. M., & L. Avilés. 1995. Sociality in a bark-dwelling huntsman spider from Australia, Delena cancerides (Araneae: Sparassidae). Insectes Sociaux, 42:287–302. Rudge, M. R. 1968. The food of the common shrew Sorex araneus L. (Insectivora: Soricidae) in Britain. J. Anim. Ecol., 37:565–581. Rüffer, H. 1966. Beiträge zur Kenntnis der Entwicklungsbiologie der Weberknechte. Zool. Anz., 176:160–175. Ruge, K. 1969. Beobachtungen am Blutspecht im Burgenland. Vogelwelt, 90:201–223. Rühm, J. 1926. Über die Nahrung von Phalangium L. Zool. Anz., 68:154–158. Rtzicka, V., J. Hajer, & M. Zacharda. 1995. Arachnid population patterns in underground cavities of a stony debris field (Araneae, Opiliones, Pseudoscorpionidea, Acari: Prostigmata, Rhagidiidae). Pedobiologia, 39:42–51. Sabino, J., & P. Gnaspini. 1999. Harvestman (Opiliones, Gonyleptidae) takes prey from a spider (Araneae, Ctenidae). J. Arachnol., 27:675–678. Sacher, P., & G. Dornbusch. 1990. Nachweis von Spinnentieren (Opiliones, Araneae) in der Nestlingsnahrung einiger Singvögel. Ent. Nachr. Ber., 34:43–44. Sáez, F. A., & M. E. Drets. 1958. The action of gonyleptidine on the mitotic and meiotic chromosomes and on the interphase nucleus. Portug. Acta Biol., 5:287–296. Sanders, N. J. 2002. Elevational gradients in ant species richness: area, geometry, and Rapoport’s rule. Ecography, 25:25–32.

561

Sanders, N. J., J. Moss, & D. Wagner. 2003. Patterns of ant species richness along elevational gradients in an arid ecosystem. Global Ecology and Biogeography, 12:93–102. Sanger, F., S. Nicklen, & A. R. Coulsen. 1977. DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. Sci. USA, 74:5463–5468. Sankey, J. H. P. 1949a. British harvest-spiders. Essex Nat., 28:181–191. Sankey, J. H. P. 1949b. Observations on food, enemies and parasites of British harvest-spiders (Arachnida, Opiliones). Ent. Mon. Mag., 85:246–247. Santori, R. T., D. A. Moraes, C. E. V. Grelle, & R. Cerqueira. 1997. Natural diet at a restinga forest and laboratory food preferences of the opossum Philander frenata in Brazil. Stud. Neotrop. Fauna Environ., 32:12–16. Santos, F. H. 2003. Estudo de parâmetros fisiológicos relacionados ao modo de vida cavernícola em Goniosomatinae (Opiliones, Gonyleptidae). Ph.D. Thesis, Universidade de São Paulo, São Paulo, Brazil. Santos, F. H., & P. Gnaspini. 2002. Notes on the foraging behavior of the Brazilian cave harvestman Goniosoma spelaeum (Opiliones, Gonyleptidae) J. Arachnol., 30:177– 180. Sato, I. 1940. Studies on the cytoplasmic phenomena in the spermatogenesis of the oriental scorpion, Buthus martensii, with special reference to the structure of the chondriosome ring and the dictyokinesis. J. Sci. Hiroshima Univ., B1, 8:1–116. Sato, I., & S. Suzuki. 1939. Eine merkwürdige neue Ischyropsaliden-Art aus Japan. Zool. Anz., 126:29–32. Saunders, D. S. 1982. Insect Clocks. Pergamon Press, London. Sauphanor, B., & F. Sureau. 1993. Aggregation behaviour and interspecific relationships in Dermaptera. Oecologia, 96: 360–364. Savory, T. H. 1928. The Biology of Spiders. Sidgwick & Jackson, London. Savory, T. H. 1938. Notes on the biology of harvestmen. J. Quekett Microsc. Club, 1:89–94. Savory, T. H. 1959. Instinctive Living: A Study of Invertebrate Behaviour. Pergamon Press, London. Savory, T. H. 1961. Spiders, Men, and Scorpions. University of London Press, London. Savory, T. H. 1962. Daddy longlegs. Scient. Am., 207:119–128. Savory, T. H. 1977. Cyphophthalmi: the case for promotion. Biol. J. Linn. Soc., 9:299–304. Sayer, J., & T. Whitmore. 1991. Tropical moist forests—destruction and species extinction. Biological Conservation, 55:199–213. Schaefer, M. 1980a. Effects of an extensive fire on the fauna of spiders and harvestmen (Araneida and Opilionida) in pine forests. Pp. 103–108 in Proceedings of the 8th International

562

References

Congress of Arachnology (J. Gruber, ed.). Verlag H. Egermann, Vienna. Schaefer, M. 1980b. Sukzession von Arthropoden in verbrannten Kiefernforsten. II. Spinnen (Araneida) und Weberknechte (Opilionida). Forstwiss. Centralblatt, 99:341– 356. Schaefer, M. 1986. Studies on the role of opilionids as predators in a beech wood ecosystem. Pp. 255–260 in Proceedings of the 9th International Arachnological Congress (W. G. Eberhard, Y. D. Lubin, & B. C. Robinson, eds.). Smithsonian Institution Press, Washington, DC. Schimkewitsch, W. 1898. Über die Entwicklung des Darmkanals bei einigen Arachniden. Trav. Soc. Imp. Sci. Nat. St Pétersbourg, 29:25. Schlee, D. 1990. Das Bernstein-Kabinett. Stuttgart. Beitr. Naturk., ser. C, 28:1–100. Schlee, D., & W. Glöckner. 1978. Bernstein: Bernsteine und Bernstein Fossilien. Stuttgart. Beitr. Naturk., ser. C, 8:1–72. Schliwa, M. 1979. The retina of the phalangid, Opilio ravennae, with particular reference to arhabdomeric cells. Cell Tissue Res., 204:473–495. Schlotheim, E. F. von 1820. Die Petrefactenkunde auf ihrem jetzigen Standpunkte durch die Beschreibung einer Sammlung versteinerter und fossiler Überreste der Tier- und Pflanzenreichs der Vorwelt erläutert. Gotha. Schlüter, T. 1978. Zur Systematik und Palökologie harzkonservierter Arthropoda eine Tapzönose aus dem Cenomanium von NW-Frankreich. Berliner Geowissenschaftliche Abhandlungen, ser. A, 9:150pp. (without pagination). Schmidt, J., M. Garcia, R. C. Razo, P. Holmes, & R. J. Full. 2002. Dynamics and stability of legged locomotion in the horizontal plane: a test case using insects. Biol. Cybern., 86:343–353. Schmidt, J. O., F. R. Dani, G. R. Jones, & E. D. Morgan. 2000. Chemistry, ontogeny, and role of pygidial gland secretions of the vinegaroon Mastigoproctus giganteus (Arachnida: Uropygi). J. Insect Physiol., 46:443–450. Schmitz, A., & S. F. Perry. 2000. Respiratory system of arachnids I: Morphology of the respiratory system of Salticus scenicus and Euophrys lanigera (Arachnida, Araneae, Salticidae). Arthrop. Struct. Dev., 29:3–12. Schmitz, A., & S. F. Perry. 2002. Morphometric analysis of the tracheal walls of the harvestmen Nemastoma lugubre (Arachnida, Opiliones, Nemastomatidae). Arthrop. Struct. Dev., 30:229–241. Schmoller, R. 1970. Life histories of alpine tundra Arachnida in Colorado. Am. Mid. Nat., 83:119–133. Schoener, T. W. 1971. Theory of feeding strategies. Ann. Rev. Ecol. Syst., 2:369–404. Schuh, R. T. 2000. Biological Systematics: Principles and Applications. Cornell University Press, Ithaca, NY.

Schumann, H., & H. Wendt. 1989. Zur Kenntnis der tierischen Inklusen des sächsischen Bernsteins. Dtsch. ent. Z., N.F., 36:33–44. Schwendinger, P. J. 1992. New Oncopodidae (Opiliones, Laniatores) from Southeast Asia. Rev. suisse Zool., 99:177–199. Schwendinger, P. J. 2006. A taxonomic revision of the family Oncopodidae VI. Martensiellus, a new genus from Borneo, and the discovery of a tarsal pore organ in Oncopodidae (Opiliones: Laniatores). In Ornithology, Arachnology and Asian Mountain Ranges—A Tribute to the Work of Prof. Dr. Jochen Martens (P. Jäger, M. Päckert, & P. J. Schwendinger, eds.). Zootaxa, 1325:255–256. Schwendinger, P. J., & G. Giribet, 2005. The systematics of the south-east Asian genus Fangensis Rambla, 1994 (Opiliones: Cyphophthalmi: Stylocellidae). Invertebr. Syst., 19:297–323. Schwendinger, P. J., G. Giribet, & H. Steiner. 2004. A remarkable new cave-dwelling Stylocellus (Opiliones, Cyphophthalmi) from peninsular Malaysia, with a discussion on taxonomic characters in the family Stylocellidae. J. Nat. Hist., 38:1421–1435. Schwendinger, P. J., & J. Gruber. 1992. A new Dendrolasma (Opiliones, Nemastomatidae) from Thailand. Bul. Br. Arachnol. Soc., 9:57–60. Schwendinger, P. J., & J. Martens. 1999. A taxonomic revision of the family Oncopodidae II. The genus Gnomulus Thorell (Opiliones, Laniatores). Rev. suisse Zool., 106:945–982. Schwendinger, P. J., & J. Martens. 2002a. Penis morphology in Oncopodidae (Opiliones, Laniatores): evolutionary trends and relationships. J. Arachnol., 30:425–434. Schwendinger, P. J., & J. Martens. 2002b. A taxonomic revision of the family Oncopodidae III: Further new species of Gnomulus Thorell (Opiliones, Laniatores). Rev. suisse Zool., 109:47–113. Schwendinger, P. J., & J. Martens. 2004. A taxonomic revision of the family Oncopodidae IV: The genus Oncopus Thorell (Opiliones, Laniatores). Rev. suisse Zool., 111:139–174. Schwendinger, P. J., & J. Martens. 2006. A taxonomic revision of the family Oncopodidae V. Gnomulus from Vietnam and China, with the description of five new species (Opiliones, Laniatores). Rev. suisse Zool. 113:595–615. Scudder, S. H. 1891. Index to known fossil insects of the world including myriapods and arachnids. Reports of the United States Geological Survey, 71:1–744. Searle, J. B. 1991. A hybrid zone comprising staggered chromosomal clines in the house mouse (Mus musculus domesticus). Proc. R. Soc. B, 246:47–52. Searle, J. B. 1993. Chromosomal hybrid zones in eutherian mammals. Pp. 309–353 in Hybrid Zones and the Evolutionary Process (R. G. Harrison, ed.). Oxford University Press, New York.

References

Seitz, K. A. 1972. Zur Histologie und Feinstruktur des Herzens und der Hämocyten von Cupiennius salei Keys. (Araneae, Ctenidae). I. Herzwandung, Bildung und Differenzierung der Hämocyten. Zool. Jb., Abt. Anat. u. Ont. Tiere, 89:351–384. Selden, P. A. 1993a. Arthropoda (Aglaspidida, Pycnogonida and Chelicerata). Pp. 297–320 in The Fossil Record, vol. 2 (M. J. Benton, ed.). Chapman & Hall, London. Selden, P. A. 1993b. Fossil arachnids—recent advances and future prospects. Mem. Queensland Mus., 33:389–400. Selden, P. A. & J. A. Dunlop. 1998. Fossil taxa and relationships of chelicerates. Pp. 303–331 in Arthropod Fossils and Phylogeny (G. Edgecombe, ed.). Columbia University Press, New York. Sellin, D. 1969. Beobachtungen an einem ZaunkönigKuckuck. Falke, 16:238–241. Sensenig, A., & J. W. Shultz. 2003. Mechanics of cuticular elastic energy storage in leg joints lacking extensor muscles in arachnids. J. Exp. Biol., 206:771–784. Sensenig, A., & J. W. Shultz. 2004. Mechanics of elastic extension in the pedipalpal joints of scorpions and solifuges (Arachnida: Scorpiones, Solifugae). J. Arachnol., 32:1–10. Sensenig, A., & J. W. Shultz. (in press). Mechanical energy oscillations during locomotion in the harvestman Leiobunum vittatum (Opiliones). J. Arachnol. Sergeeva, T. K., & S. Y. Grünthal. 1988. Seasonal trophic dynamics of Pterostichus oblongopunctatus (Coleoptera, Carabidae). Zool. Zhurnal, 67:548–556. [In Russian] Shanahan, C. M. 1989a. Cytogenetics of Australian scorpiones. I. Interchange polymorphism in the family Buthidae. Genome, 32:882–889. Shanahan, C. M. 1989b. Cytogenetics of Australian scorpiones. II. Chromosome polymorphism in species of Urodacus (family Scorpionidae). Genome, 32:890–900. Sharma, G. P., & G. P. Dutta. 1959. On the male heterogamety in Melanopa unicolor Roewer (Opiliones-Arachnida). Panjab Univ. Res. Bull., 10:209–213. Sharma, P., & G. Giribet. 2005. A new Troglosiro species (Opiliones, Cyphophthalmi, Pettalidae) from New Caledonia. Zootaxa, 1053:47–60. Sharma, P., & G. Giribet. 2006. A new Pettalus species (Opiliones, Cyphophthalmi, Pettalidae) from Sri Lanka with a discussion on the evolution of eyes in Cyphophthalmi. J. Arachnol. Shaw, M. R. 1994. Parasitoid host ranges. Pp. 111–144 in Parasitoid Community Ecology (B.A. Hawkins & W. Sheehan, eds.). Oxford University Press, Oxford. Shaw, M. W. & G. M. Hewitt. 1990. B-chromosomes, selfish DNA and theoretical models: where next? Pp. 197–223 in Oxford Surveys in Evolutionary Biology, vol. 7 (D. J. Futuyma & J. Antonovics, eds.). Oxford University Press, New York. Shear, W. A. 1969. Observations on the predatory behavior of

563

the spider Hypochilus gertschi Hoffman (Hypochilidae). Psyche, 76:407–417. Shear, W. A. 1975a. The opilionid family Caddidae in North America, with notes on species from other regions (Opiliones, Palpatores, Caddoidea). J. Arachnol., 2:65–88. Shear, W. A. 1975b. The opilionid genera Sabacon and Tomicomerus in America (Opiliones, Troguloidea, Ischyropsalidae). J. Arachnol., 3:5–29. Shear, W. A. 1977. The opilionid genus Neogovea Hinton, with a description of the first troglobitic cyphophthalmid from the Western Hemisphere (Opiliones, Cyphophthalmi). J. Arachnol., 3:165–175. Shear, W. A. 1979a. Huitaca ventralis, n.gen., n.sp., with a description of a gland complex new to cyphophthalmids (Opiliones, Cyphophthalmi). J. Arachnol., 7:237–243. Shear, W. A. 1979b. Stylocellus sedgwicki n.sp., from Penang Island, Malaysia (Opiliones, Cyphophthalmida, Stylocellidae). Bul. Br. Arachnol. Soc., 4:356–360. Shear, W. A. 1980. A review of the Cyphophthalmi of the United States and Mexico, with a proposed reclassification of the suborder (Arachnida, Opiliones). Am. Mus. Novit., 2705:1–34. Shear, W. A. 1982. Opiliones. Pp. 104–110 in Synopsis and Classification of Living Organisms, vol. 2 (S. P. Parker, ed.). McGraw-Hill, New York. Shear, W. A. 1985. Marwe coarctata, a remarkable new cyphophthalmid from a limestone cave in Kenya (Arachnida, Opiliones). Am. Mus. Novit., 2830:1–6. Shear, W. A. 1986. A cladistic analysis of the opilionid superfamily Ischyropsalidoidea, with descriptions of the new family Ceratolasmatidae, the new genus Acuclavella, and four new species. Am. Mus. Novit., 2844:1–29. Shear, W. A. 1993a. The genus Chileogovea (Opiliones, Cyphophthalmi, Petallidae). J. Arachnol., 21:73–78. Shear, W. A. 1993b. The genus Troglosiro and the new family Troglosironidae (Opiliones, Cyphophthalmi). J. Arachnol., 21:81–90. Shear, W. A. 1993c. New species in the opilionid genus Stylocellus from Malaysia, Indonesia and the Philippines (Opiliones, Cyphophthalmi, Stylocellidae). Bul. Br. Arachnol. Soc., 9:174–188. Shear, W. A. 1996. Hesperopilio mainae, a new genus and species of harvestman from Western Australia (Opiliones: Caddidae: Acropsopilioninae). Rec. West. Aust. Mus., 17:455–460. Shear, W. A. 2004. Description of the female of Acropsopilio chomulae (Goodnight & Goodnight 1948) from Chiapas, Mexico (Opiliones, Caddidae, Acropsopilioninae). J. Arachnol., 32:432–435. Shear, W. A., & J. Gruber. 1983. The opilionid subfamily Ortholasmatinae (Opiliones, Troguloidea, Nemastomatidae). Am. Mus. Novit., 2757:1– 65.

564

References

Shear, W. A., & J. Gruber. 1996. Cyphophthalmid opilionids new to Madagascar: two new genera (Opiliones, Cyphophthalmi, ?Pettalidae). Bul. Br. Arachnol. Soc., 10:181–186. Shear, W. A., & J. Kukalová-Peck. 1990. The ecology of Paleozoic terrestrial arthropods: the fossil evidence. Canad. J. Zool., 68:1807–1834. Shelly, T. E., & T. S. Whittier. 1997. Lek behavior of insects. Pp. 273–293 in The Evolution of Mating Systems in Insects and Arachnids (J. C. Choe & B. J. Crespi, eds.). Cambridge University Press, Cambridge. Shultz, J. W. 1989. Morphology of locomotor appendages in Arachnida: evolutionary trends and phylogenetic implications. Zool. J. Linn. Soc., 97:1–56. Shultz, J. W. 1990. Evolutionary morphology and phylogeny of Arachnida. Cladistics, 6:1–38. Shultz, J. W. 1991. Evolution of locomotion in Arachnida: the hydraulic pressure pump of the giant whipscorpion, Mastigoproctus giganteus (Uropygi). J. Morphol., 210:13– 31. Shultz, J. W. 1998. Phylogeny of Opiliones (Arachnida): an assessment of the “Cyphopalpatores” concept. J. Arachnol., 26:257–272. Shultz, J. W. 2000. Skeletomuscular anatomy of the harvestman Leiobunum aldrichi (Weed, 1893) (Arachnida: Opiliones) and its evolutionary significance. Zool. J. Linn. Soc., 128:401–438. Shultz, J. W. 2001. Gross muscular anatomy of Limulus polyphemus (Xiphosura, Chelicerata) and its bearing on evolution in the Arachnida. J. Arachnol., 29:283–303. Shultz, J. W., & T. Cekalovic. 2003. First species of Austropsopilio (Opiliones, Caddoidea, Caddidae) from South America. J. Arachnol., 31:20–27. Shultz, J. W., & J. C. Regier. 2001. Phylogenetic analysis of Phalangida (Arachnida, Opiliones) using two nuclear proteinencoding genes supports monophyly of Palpatores. J. Arachnol., 29:189–200. Shultz, J. W., & J. C. Regier. 2004. Molecular phylogeny of Caddo and the timing of phylogenetic evidence in Caddidae (Opiliones). Am. Arachnol., 68:17–18. Silhavy, V. 1938. Sur l’importance de la forme de l’appareil sexuel pour le système des Opilions et révision de quelques espèces européennes du genre Opilio Herbst. Sborník prirodovedny Klubu Trebic, 3:7–20. Silhavy, V. 1942. Sekáci, zijící na plodnicích hub. Folia ent., 5:69–70. Silhavy, V. 1956. Sekáci—Opilionidea. Fauna CSR, vol. 7. Ceskoslovenská Akademie Ved, Praha. Silhavy, V. 1957. Potrava plosíka vetsiho [Trogulus nepaeformis (Scop.)] Arachnoidea, Opiliones. Vlastived Sborník Vysociny, 1:79–83. Silhavy, V. 1960. Stempellia weiseri n.sp., eine neue Mikrospori-

dienart aus dem Weberknechte Opilio parietinus (De Geer). Vestník csl. spol. Zool., 24:50–53. Silhavy, V. 1961. Die Grundsätze der modernen Weberknechttaxonomie und Revision des bisherigen Systems der Opilioniden. Pp. 262–267 in Verhandlungen des 11. Internationalen Kongresses für Entomologie in Wien, vol. 1 (H. Strouhal & M. Beier, eds). C. Reisser’s Söhne, Wien. Silhavy, V. 1966a. Ökologische und genitalmorphologische Bemerkungen über einige Arten der Familie Cosmetidae Simon aus Kuba (Arachnoidea, Opilionidea). Dtsch. ent. Z., N.F., 13:263–266. Silhavy, V. 1966b. Über die Genitalmorphologie der Nemastomatidae (Arach., Opiliones). Senckenbergiana Biol., 47:67–72. Silhavy, V. 1967a. Anarthrotarsus martensi, ein neuer Weberknecht aus Griechenland (Arach., Opiliones). Senckenbergiana Biol., 48:175–178. Silhavy, V. 1967b. Über eine Sekretmündung am ersten Chelicerenglied der Nemastomatiden und ihre Anwendung in der Taxonomie (Opilionidae). Acta ent. bohemoslovaca, 64:319–321. Silhavy, V. 1969a. Ibantila cubana gen. nov. spec. nov., the first representative of subfamily Ibaloniinae Roewer (Arach., Opilionidea) from America. Acta ent. bohemoslovaca, 33:372–376. Silhavy, V. 1969b. Über die Präparation der Genitalien der Weberknechte. Dtsch. ent. Z., 16:141–145. Silhavy, V. 1970. Nouvelles recherches sur la famille des Neopilionidae Lawrence. Bull. Mus. Hist. nat. Paris, ser. 2, 41(suppl. 1):171–175. Silhavy, V. 1973. Two new systematic groups of gonyleptomorphid phalangids from the Antillean-Caribbean Region, Agoristenidae Fam. N., and Caribbiantinae Subfam. N. (Arachn.: Opilionidea). Vestník csl. spol. Zool., 37:110–143. Silhavy, V. 1974. Cavernicolous opilionids from Mexico: subterranean fauna of Mexico, part II. Quad. Acc. Naz. Lincei. 370:175–194. Silhavy, V. 1976. Zwei neue Ausobskya-Arten aus Griechenland: A. mahnerti sp.n. und A. hauseri sp.n. (Arachnoidea, Opiliones). Rev. suisse Zool., 83:263–271. Silhavy, V. 1977. Further cavernicolous opilionids from Mexico: subterranean fauna of Mexico, part III. Quad. Acc. Naz. Lincei, 171:219–233. Silhavy, V. 1978. Minuides milleri sp.n., an opilionid with an unusual maner of stridulation (Phalangodidae). Acta ent. bohemoslovaca, 75:58–63. Silhavy, V. 1979. New American representatives of the subfamily Samoinae (Opiliones: Phalangodidae). Annotnes Zool. & Bot., 130:1–27. Silva, M. B. da. 2002. Análise filogenética e biogeográfica de Goniosomatinae (Arachnida, Opiliones, Gonyleptidae). M.Sc. Thesis, Universidade de São Paulo, São Paulo, Brazil.

References

Silvestri, F. 1905. Note aracnologiche. II. Descrizione di un nuovo genere di Opilionidi del Chile. Redia, 2:254–256. Simeonov, S. 1981. Untersuchung über die Nahrung der Goldammer (Emberiza citrinella) in Bulgarien. Annuaire de l’Université de Sofia, Faculté de Biologie, livre 1, Zoologie, 72/73:69–79. [In Bulgarian with summary in German] Simeonov, S. D. 1963. Investigation on the food of tree sparrow (Passer montanus L.) in Sofia-region. Izvestiya na Zoologicheskiya Institut s Muzey, 14:93–109. [In Bulgarian with summaries in Russian and German] Simeonov, S. D. 1964. Investigation on the feeding of House Sparrow (Passer domesticus L.) in Sofia-region. Annuaire de l’Université de Sofia, Faculté de Biologie, Géologie et Géographie, livre 1, Biologie (Zoologie), 56(1961/1962): 239–275. [In Bulgarian with summaries in Russian and German] Simmons, L. W. 2001. Sperm Competition and Its Evolutionary Consequences in the Insects. Monographs in Behavior and Ecology. Princeton University Press, Princeton, NJ. Simon, E. 1872a. Notice complémentaire sur les Arachnides cavernicoles et hypogés. Annls Soc. ent. Fr., ser. 5, 2:473–488. Simon, E. 1872b. Notice sur les Arachnides cavernicoles et hypogés. Annls Soc. ent. Fr., ser. 5, 2:215–244. Simon, E. 1879a. Les Arachnides de France. VII. Contenant les Ordres des Chernetes, Scorpiones et Opiliones. Librairie Encyclopèdique de Roret, Paris. Simon, E. 1879b. Essai d’une classification des Opiliones Mecostethi: Remarques synonymiques et descriptions d’espèces nouvelles. Annls Soc. ent. Fr., 22:183–241. Simon, E. 1879c. Opiliones. in Les Arachnides de France. VII. Contenant les Ordres des Chernetes, Scorpiones et Opiliones. Pp. 116–332. Librairie Encyclopèdique de Roret, Paris. Sirbu, D. F. 1977. Contribution to studying the food of the viviparous lizard in the Apuseni Mountains. Studia Universitatis Babes-Bolyal, 2:77–80. [In Romanian with summary in English] Sissom, W. D., G. A. Polis, & D. D. Watt. 1990. Field and laboratory methods. Pp. 445–461 in The Biology of Scorpions (G. A. Polis, ed.). Stanford University Press, Stanford, CA. Skar, H.-J., S. Hågvar, A. Hagen, & E. Østbye. 1975. Food habits and body composition of adult and juvenile meadow pipit [Anthus praensis (L.)]. Pp. 159–169 in Fennoscandian Tundra Ecosystems, pt. 2: Animals and Systems Analysis, vol. 17. Springer-Verlag, Berlin. Slagsvold, T. 1976. The phenology of Mitopus morio (Fabr.) (Opiliones) in Norway. Norw. J. Ent., 23:7–16. Smallwood, W. M. 1928. Notes on the food of some Onondaga Urodela. Copeia, 169:89–98. Smith, C. C., & A. N. Bragg. 1949. Observations on the ecology and natural history of Anura. VII. Food and feeding habits of the common species of toads in Oklahoma. Ecology, 30:333–349.

565

Smith, R. L. 1997. Evolution of paternal care in the giant water bugs (Heteroptera: Belostomatidae). Pp. 116–149 in The Evolution of Social Behavior in Insects and Arachnids (J. C. Choe & B. J. Crespi, eds.). Cambridge University Press, Cambridge. Snodgrass, R. E. 1948. The feeding organs of the Arachnida, including mites and ticks. Smithson. Misc. Collns, 110:1– 93. Soares, B. A. M., & H. E. M. Soares. 1954. Monografia dos gêneros de opiliões neotrópicos. Arq. Zool., 8:225–302. Soares, H. E. M. 1974. Nota sobre Cynorta phalerata (C. L. Koch, 1839) (Opiliones, Cosmetidae). Physis, 33:13–18. Soares, H. E. M. 1978. Opera Opiliologica Varia XIV (Opiliones, Phalangodidae). Papéis Zool. S. Paulo, 32:141–144. Soares, H. E. M., 1979. Opera Opiliologica Varia X (Opiliones, Phalangodidae). Revta bras. Biol., 39:161–167. Soares, H. E. M., & S. Avram. 1981. Opilionides du Venezuela. Trav. Inst. Spéol. “É. Racovitza,” 20:1–21. Soares, H. E. M., & B. A. M. Soares. 1979. Opera Opiliologica Varia. XVI. Novo gênero de Gonyleptidae e presença de Triaenonychidae no Brasil (Opiliones). Revta bras. Ent., 23:169–173. Soares, H. E. M., & B. A. M. Soares. 1984. Opera Opiliologica Varia XXV (Opiliones, Gonyleptidae). Revta bras. Ent., 28:301–314. Soares, H. E. M., & B. A. M. Soares. 1985. Opera Opiliologica Varia XXII (Opiliones: Gonyleptidae). Naturalia, 10:157– 200. Sokolow, I. 1929. Untersuchungen über die Spermatogenese bei den Arachniden. III. Über die Spermatogenese von Nemastoma lugubre (Opiliones). Z. Zellforsch. mikrosk. Anat., 8:617–654. Sokolow, I. 1930. Untersuchungen über die Spermatogenese bei den Arachniden. IV. Über die Spermatogenese von Phalangiden (Opiliones). Z. Zellforsch. mikrosk. Anat., 10:164– 194. Solem, J. O., & E. Hauge. 1973. Araneae and Opiliones in light traps at Målsjøenm Sør-Trøndelag. Norsk ent. Tidsskr., 20:275–279. Sørensen, W. 1873. Bidrag til Phalangidernes morphologi og systematik samt beskrivelse af nogle nye, herhen hoerende former. Naturhist. Tidsskr., ser. 3, 8:489–526. Sørensen, W. 1879. Om bygningen af Gonyleptiderne, en type af Arachnidernes classe. Naturhist. Tidsskr., ser. 3, 8:97– 222. Sørensen, W. 1884. Opiliones Laniatores (Gonyleptides W.S. olim) Musei Hauniensis. Naturhist. Tidsskr., ser. 3, 14:555– 646. Sørensen, W. 1886. Opiliones. Pp. 53–86 in Die Arachniden Australiens nach der Natur beschrieben und abgebildet, vol. 2(33) (L. Koch & E. von Keyserling, eds.). Nürnberg.

566

References

Sørensen, W. 1932. Descriptiones Laniatorum (Opus posthumum recognovit et edidit K. L. Henriksen). Kong. Danske Vidensk. Selsk. Skr., Naturvidensk. Math. Afd., ser. 9, 3:199–422. Soto, M. M. 1980. Contribución al conocimiento de los Opiliones de la República Mexicana (Arácnida: Phalangida). Undergraduate Thesis, Universidad Nacional Autónoma de México, DF, Mexico. Southcott, R. V. 1961. Studies on the systematics and biology of the Erythraeoidea (Acarina), with a critical revision of the genera and subfamilies. Aust. J. Zool. 9:367–610. Southcott, R. V. 1991. A further revision of Charletonia (Acarina: Erythraeidae) based on larvae, protonymphs and deutonymphs. Invertebr. Taxon., 5:61–131. Southcott, R. V. 1994. Two new larval Erythraeidae (Acarina) from Thailand, with keys to the larvae of Leptus for Asia and New Guinea, and world larvae of Hauptmannia. Steenstrupia, 20:165–176. Spicer, G. S. 1987. Scanning electron microscopy of the palp sense organs of the harvestman Leiobunum townsendi (Arachnida: Opiliones). Trans. Am. Micr. Soc., 106:232–239. Spicer, W. W. 1867. Helps to distribution. Hardwickes ScienceGossip, 1:244–245. Spirito, F. 1998. The role of chromosomal changes in speciation. Pp. 320–329 in Endless Forms: Species and Speciation (D. J. Howard & S. H. Berlocher, eds.). Oxford University Press, New York. Spoek, G. L. 1963. The opilionida (Arachnida), of the Netherlands. Zool. Verh., 63:1–70. Spoek, G. L. 1964. Spinachtigen-Arachnida. III. De Hooiwagens (Opilionida) van Nederland. Wet. Med. Koninklijke Nederl. Natuurhist. Vereniging, 50:1–28. Stadler, H., & E. Schenkel. 1940. Die Spinnentiere (Arachniden) Mainfrankens. Mitt. naturwiss. Mus. Stadt Aschaffenburg, 2:1–33. Stahlavsky, F., & J. Kral. 2004. Karyotype analysis and achiasmatic meiosis in pseudoscorpons of the family Chthoniidae (Arachnida: Pseudoscorpiones). Hereditas, 140:49–60. Stammer, H. J. 1949. Die Bedeutung der Aethylenglykolfallen für tierökologische und phänologische Untersuchungen. Verh. Ges. dtsch. Zool., 13:387–391. Stare˛ ga, W. 1973. Bemerkungen über einige westpaläaktische Webernechte (Opiliones). Annales Zoologici 30:361–373. Starega, W. 1976a. Opiliones Kosarze (Arachnoidea): Fauna Polski. Polska Akad. Nauk Inst. Zool., 5:1–197. Starega, W. 1976b. Die Weberknechte (Opiliones, excl. Sironidae) Bulgariens. Annls zool., 33:287–433. Starega, W. 1984. Revision der Phalangiidae (Opiliones). III. Die afrikanischen Gattungen der Phalangiinae, nebst Katalog aller afrikanischen Arten der Familie. Annls zool., 38:1–79.

Starega, W. 1986. Eine neue Art der Nemastomatidae (Opiliones) aus dem Pamir, nebst nomenklatorisch-taxonomischen Anmerkungen. Bull. Pol. Acad. Sci., 34:301–305. Starega, W. 1988. A new species of Caddella (Opiliones) from South Africa. Ann. Natal Mus., 29:529–532. Starega, W. 1989. Harvestmen (Opiliones) from the Mascarene Islands and resurrection of the family Zalmoxidae. Ann. Natal Mus., 30:1–8. Starega, W. 1992. An annotated check-list of harvestmen, excluding Phalangiidae, of the Afrotropical region (Opiliones). Ann. Natal Mus., 33:271–336. Starega, W. 2002a. Baltic amber harvestmen (Opiliones) from Polish collections. Annls zool., 52:601–604. Starega, W. 2003. On the identity and synonymies of some Asiatic Opilioninae (Opiliones: Phalangiidae). Acta arachnol., 52:91–102. Stefanini-Jim, R. L., H. E. M. Soares, & J. Jim. 1987. Notas sobre a biologia de Cadeadoius niger (Mello-Leitão, 1935) (Opiliones, Gonyleptidae, Progonyleptoidellinae) P. 24 in Anais do XX Encontro Brasileiro de Etologia. Botucatu, São Paulo, Brazil. Steinböck, O. 1931. Zur Lebensweise einiger Tiere des Ewigschneegebietes. Z. Morphol. Ökol. Tiere, 20:707–718. Stewart, R. E. 1956. Ecological study of ruffed grouse broods in Virginia. Auk, 73:33–41. Stinglhammer, H. R. G. 1987. Studies on factors affecting the structure of arachnid communities on peat bogs. Ph.D. Thesis, University of Paisley, Paisley, Scotland. Stipperger, H. 1928. Biologie und Verbreitung der Opilioniden Nord-Tirols. Arb. Zool. Inst. Univ. Innsbruck, 3:12–79. Streble, H. 1966. Untersuchungen über das hormonale System der Spinnentiere (Chelicerata) unter besonderer Berücksichtigung des endokrinen “Gewebes” der Spinnen (Araneae). Zool. Jb., Abt. allg. Zool. Physiol. Tiere, 72:157– 234. Sunderland, K. D., & S. L. Sutton. 1980. A serological study of arthropod predation on woodlice in a dune grassland ecosystem. J. Anim. Ecol., 49:987–1004. Sundevall, K. J. 1833. Conspectus Arachnidum. C. F. Berling, London. Suomalainen, E., A. Saura, & J. Lokki. 1987. Cytology and Evolution in Parthenogenesis. CRC Press, Boca Raton, FL. Sutcliffe, D. W. 1963. The chemical composition of the hemolymph in insects and some other arthropods in relation to their phylogeny. Comp. Biochem. Physiol., 9:121–135. Suzuki, S. 1940. Über das Vorkommen des Männchens von Ischyropsalis abei Sato et Suzuki (Opiliones) und seine weitere Verbreitung in Japan. J. Sci. Hiroshima Univ., B1, 7:209– 219. Suzuki, S. 1941. On the chromosomes of some opilionids. J. Sci. Hiroshima Univ., B1, 9:239–248.

References

Suzuki, S. 1949. Studies on the Japanese harvesters. II. Harvesters from Hokkaido, with special reference to variation. J. Sci. Hiroshima Univ., B1, 11:13–29. Suzuki, S. 1954. Cytological studies in spiders. III. Studies on the chromosomes of fifty-seven species of spiders belonging to seventeen families, with general considerations on chromosomal evolution. J. Sci. Hiroshima Univ., B1, 15:2, 23–136. Suzuki, S. 1956. Systematics and karyological studies of Japanese species of Gagrellula. Zool. Mag., 65:161. [In Japanese] Suzuki, S. 1957. On the three closely related forms of the genus Liobunum (Phalangiidae, Opiliones). J. Fac. Sci., Hokkaido Univ., ser. 6, Zoology, 13:109–117. Suzuki, S. 1958. A remarkable new phalangid, Ischyropsalis yezoensis (Ischyropsalidae, Opiliones), from Hokkaido. Annot. Zool. Jap., 31:167–170. Suzuki, S. 1959. Cytotaxonomy of Gagrellula from Shikoku (abstract). Zool. Mag., 68:133–134. [In Japanese] Suzuki, S. 1964a. A new representative of the Erecananinae from Japan. Annot. Zool. Jap., 37:221–225. Suzuki, S. 1964b. A remarkable new phalangodid Dongmoa oshimensis from Japan. Annot. Zool. Jap., 37:163–167. Suzuki, S. 1965. Three species of Ischyropsalidae (Phalangida) from Hokkaido. Annot. Zool. Jap., 38:39–44. Suzuki, S. 1966a. Four remarkable phalangids from Korea. Annot. Zool. Jap., 39:95–106. Suzuki, S. 1966b. Opiliones. Pp. 90–139 in Systematic Zoology, vol. 7(2A) (T. Uchida, ed.). Nakayama-shoten Press, Tokyo. [In Japanese] Suzuki, S. 1967. Zoogeographical distribution of the Japanese harvestmen. Hiroshima-Mushi-no Kai Zappo, 13:16–18. [In Japanese] Suzuki, S. 1969. On a collection of opilionids from Southeast Asia. J. Sci. Hiroshima Univ., B1, 22:11–77. Suzuki, S. 1970. Report on a collection of Opiliones from Nepal. Journal of Science of the Hiroshima University, Ser. B, Div. 1 (Zoology) 23:29–57. Suzuki, S. 1971. Opiliones of the Ryukyus. J. Sci. Hiroshima Univ., B1, 23:187–213. Suzuki, S. 1972a. Geographical variation in Melanopa grandis Roewer of East Asia (Arach., Opiliones). Pp. 65–70 in Proceedings of the 5th International Congress of Arachnology (C. Folk, ed.). Czechoslovak Academy of Science, Brno. Suzuki, S. 1972b. On the discontinuous distribution in some Opiliones. Acta arachnol., 24:1–8. [In Japanese with summary in English]. Suzuki, S. 1972c. Report on a collection of Opiliones from Poroshiri-dake, Hokkaido. Mem. Nat. Sci. Mus., 5:37–44. Suzuki, S. 1973. Opiliones from the south-west Islands, Japan. J. Sci. Hiroshima Univ., B1, 24:205–279.

567

Suzuki, S. 1974. The Japanese species of the genus Sabacon (Arachnida, Opiliones, Ischyropsalididae). J. Sci. Hiroshima Univ., B1, 25:83–108. Suzuki, S. 1975a. The harvestmen of family Travuniidae from Japan. J. Sci. Hiroshima Univ., B1, 26:53–63. Suzuki, S. 1975b. The harvestmen of family Triaenonychidae in Japan and Korea. J. Sci. Hiroshima Univ., B1, 26:65– 101. Suzuki, S. 1976a. Cytotaxonomy in some species of the genus Leiobunum (Opiliones, Arachnida). Proc. Japan Acad., 52: 134–136. Suzuki, S. 1976b. The genus Leiobunum C. L. Koch of Japan and adjacent countries (Leiobunidae, Opiliones, Arachnida). J. Sci. Hiroshima Univ., B1, 26:187–260. Suzuki, S. 1976c. The harvestmen of family Caddidae in Japan (Opiliones, Palpatores, Caddoidea). J. Sci. Hiroshima Univ., B1, 26:261–273. Suzuki, S. 1976d. Report on a collection of opilionids from Pasoh Forest Reserve, west Malaysia. Nature and Life in Southeast Asia, 7:9–38. Suzuki, S. 1976e. Two triaenonychid harvestmen from Northeast Japan. J. Sci. Hiroshima Univ., B1, 26:177–185. Suzuki, S. 1977a. Disjunct distribution in Opiliones. Zool. Mag., 86:531. [In Japanese] Suzuki, S. 1977b. Report on a collection of opilionids from the Philippines. J. Sci. Hiroshima Univ., B1, 27:1–120. Suzuki, S. 1980a. Four gynandromorphous specimens of the harvestman Leiobunum globosum Suzuki. Zool. Mag., 89: 111–117. [In Japanese] Suzuki, S. 1980b. An intersex of the harvestman Gagrellula ferruginea (Loman). Acta arachnol., 29:43–46. [In Japanese] Suzuki, S. 1986. Opiliones of Hiroshima Prefecture (Arachnida). J. Hiba Soc. Nat. Hist., 132:7–45. Suzuki, S., & T. Kunita. 1972. Opiliones of Ehime Pref., Shikoku. Pp. 89–94 in Animals and Plants of Ehime Prefecture. Seibutsu, Matsuyama. [In Japanese] Suzuki, S., K. Tomishima, S. Yano & N. Tsurusaki. 1977. Discontinuous distributions in relict harvestmen (Opiliones, Arachnida). Acta arachnol., 27(special number):121–138. [In Japanese] Suzuki, S., & N. Tsurusaki. 1983. Opilionid fauna of Hokkaido and its adjacent areas. J. Fac. Sci., Hokkaido Univ., ser. 6, Zoology, 23:195–243. Swofford, D. L. 2000. PAUP 4.0*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Sinauer Associates, Sunderland. Szentkirályi, F., & A. Kristín. 2002. Lacewings and snakeflies (Neuroptera, Raphidioptera) as prey for bird nestlings in Slovakian forest habitats. Acta zool. Acad. Sci. hung., 48(suppl. 2):329–340. Takagi, N., & M. Oshimura. 1973. Fluorescence and Giemsa

568

References

banding studies of the allocyclic X chromosome in embryonic and adult mouse cells. Exp. Cell Res., 78:127–135. Tallamy, D. W. 2000. Sexual selection and evolution of exclusive paternal care in arthropods. Anim. Behav., 60:559–567. Tallamy, D. W. 2001. Evolution of exclusive paternal care in arthropods. Ann. Rev. Ent., 46:139–165. Tallamy, D. W. & W. P. Brown. 1999. Semelparity and the evolution of maternal care in insects. Anim. Behav., 57:727–730. Tallamy, D. W., & C. Schaefer. 1997. Maternal care in the Hemiptera: ancestry, alternatives, and current adaptive value. Pp. 94–115 in The Evolution of Social Behavior in Insects and Arachnids (J. C. Choe & B. J. Crespi, eds.). Cambridge University Press, Cambridge. Tallamy, D. W., & T. K. Wood. 1986. Convergence patterns in subsocial insects. Ann. Rev. Ent., 31:369–390. Taylor, C. K. 2004. New Zealand harvestmen of the subfamily Megalopsalidinae (Opiliones: Monoscutidae)—the genus Pantopsalis. Tuhinga, 15:53–76. Tchemeris, A.N. 2000. Contribution to the knowledge of the harvestman fauna in the Russian Far East and Eastern Siberia (Arachnida: Opiliones). Arthropoda Selecta, 9:31–49. Tchemeris, A. N., D. V. Logunov, & N. Tsurusaki. 1998. A contribution to the knowledge of the harvestman fauna of Siberia (Arachnida: Opiliones). Arthropoda Selecta, 7:189–199. Tedeschi, M., & R. Sciaky. 1994. Three new Italian species of the genus Holoscotolemon (Arachnida, Opiliones, Erebomastridae). Bollettino del Museo civico di Storia naturale di Verona, 18:1–10. Telford, M. J., & R. H. Thomas. 1998. Expression of homeobox genes shows chelicerate arthropods retain their deutocerebral segment. Proc. Natl. Acad. Sci. USA, 95:10671–10675. Terra, W. 2001. The origin and functions of the insect peritrophic membrane and peritrophic gel. Arch. Insect Biochem. Physiol., 47:47–61. Thaler, K. 1996. Neue Funde europäischer Krallenweberknechte (Arachnida, Opiliones: Phalangodidae, Travuniidae). Berichte d. Naturwiss.-Medizin. Vereins Innsbruck, 83:135–148. Thaler, K., & B. Knoflach. 2001. Funde hochalpiner Spinnen in den mittleren “Ostalpen” (Tirol, Graubünden) 1997– 2000 und Beifänge. Veröffentlichungen des Tiroler Landesmuseums Ferdinandeum, 81:195–203. Thaler-Kottek, E. 1973. Über Haltung und Verhalten unserer Goldhähnchen (Eingewöhnung, Nestbau, Eiablage und Zucht). Gefiederte Welt, 97:81–84, 103–107. Thevenin, A. 1901. Sur la découverte d’arachnides dans le terrain houiller de Commentry. Bull. Soc. Géol. Fr., ser. 4, 1: 605–611. Thomas, J. D. 1962. The food and growth of brown trout (Salmo trutta L.) and its feeding relationship with the salmon parr (Salmo salar L.) and the eel (Anguilla anguilla

(L.)) in the River Teify, West Wales. J. Anim. Ecol., 31:175– 205. Thomas, R. H., & D. W. Zeh. 1984. Sperm transfer and utilization strategies in arachnids: ecological and morphological constraints. Pp. 179–221 in Sperm Competition and the Evolution of Animal Mating Systems (R. L. Smith, ed.). Academic Press, London. Thorell, T. T. T. 1876. Sopra alcuni Opilioni (Phalangidea) d’Europa e dell’Asia occidentale, con un quadro dei generi europei di quest’ordine. Ann. Mus. Civ. Stor. Nat. Genova, 8: 452–508. Thorell, T. T. T. 1877. Descrizione di alcune specie di Opilioni dell’Archipelago Malese, appartenenti al Museo Civico di Genova. Ann. Mus. Civ. Stor. Nat. Genova, 9:111–138. Thorell, T. T. T. 1882. Descrizione di alcuni arachnidi inferiori dell’Archipelago Malese. Ann. Mus. Civ. Stor. Nat. Genova, 18:5–69. Thorell, T. T. T. 1889. Viaggio di Leonardo Fea in Birmania e regione vicine. XXI. Aracnidi Artrogastri Birmani. Ann. Mus. Civ. Stor. Nat. Genova, 27:521–729. Thorell, T. T. T. 1890. Aracnidi di Nias e di Sumatra raccolti nel 1886 dal Sig. E. Modigliani. Ann. Mus. Civ. Stor. Nat. Genova, ser. 2, 10:5–106. Thorell, T. T. T. 1891. Opilioni nuovi o poco conosciuti dell’Arcipelago Malese. Ann. Mus. Civ. Stor. Nat. Genova, 30: 669–770. Thorell, T. T. T. 1892. On an apparently new arachnid belonging to the family Cryptostemmoidae Westw. Bihang Till K. Svenska Vet.-Akad. Handlingar, 17:1–17. Tischler, W. 1967. Zur Biologie und Ökologie des Opilioniden Mitopus morio F. Biol. Zentralblatt, 86:473–484. Todd, V. 1949. The habits and ecology of the British harvestmen (Arachnida, Opiliones) with special reference to those of the Oxford District. J. Anim. Ecol., 18:209–229. Todd, V. 1950. Prey of harvestmen (Arachnida, Opiliones). Ent. Mon. Mag., 86:252–259. Toft, S. 2004. Mejerne. Natur og Museum, Naturhistorisk Museum, 3:2–35. Tomek, T. 1988. The breeding biology of the Dunnock Prunella modularis modularis (Linnaeus, 1758) in the Ojców National Park (South Poland). Acta Zool. Cracoviensia, 31: 115–166. Tomohiro, M. 1940. On the chromosomes of the harvester, Gagrellopsis nodulifera. J. Sci. Hiroshima Univ., B1, 7:157– 168. Tomov, V. 1990. On the food of Bufo viridis Laur. Trav. Sci. Univ. Plovdiv “Paissi Hilendarski,” Biol., 28:121–129. [In Bulgarian with summaries in Russian and English] Török, J. 1985. Comparative ecological studies on blackbird and song thrush populations. I. Nutritional Ecology. Opuscula Zoologica, 21:105–135.

References

Török, J. 1990. The impact of insecticides on the feeding of the tree sparrows [Passer montanus (L.)] in orchards during the parental care period. Pp. 199–210 in Granivorous Birds in the Agricultural Landscape (J. Pinowski & J. D. SummersSmith, eds.). PWN–Polish Scientific Publishers, Warsaw. Toti, D.S., F. A. Coyle, & J. A. Miller. 2000. A structured inventory of Appalachian grass bald and heath bald spider assemblages and a test of species richness estimator performance. J. Arachnol., 28:329–345. Tourinho, A. L. M., & A. B. Kury. 2001. Notes on Holcobunus Roewer, 1910, with two new generic synonymies (Arachnida, Opiliones, Sclerosomatidae). Bolm. Mus. nac. Rio de J., n.s., Zoologia, 461:1–22. Tourinho-Davis, A. L. M. 2003. On the dubious identity of Bastioides Mello-Leitão, 1931 (Eupnoi, Sclerosomatidae, Gagrellinae). Rev. Ibér. Aracnol., 7:241–245. Tourinho-Davis, A.L.M. 2004a. A new genus of Gagrellinae from Brazil, with a comparative study of some of the southermost tropical and subtropical South American species (Eupnoi, Sclerosomatidae, Gagrellinae). Rev. Ibér. Aracnol., 9:157–177. Tourinho-Davis, A. L. M. 2004b. The third South American species of Pectenobunus Roewer, with a new synonym for the genus (Opiliones, Eupnoi, Sclerosomatidae, Gagrellinae). Zootaxa, 405:1–16. Tourinho-Davis, A. L. M., & A. B. Kury. 2003. A review of Jussara, with descriptions of six new species (Arachnida, Opiliones, Sclerosomatidae) from Brazil. Trop. Zool., 16:209–275. Trabalon, M., A. G. Bagnères, N. Hartmann, & A. M. Vallet. 1995. Changes in cuticular compounds composition during the gregarious period and after dispersal of the young in Tegenaria atrica (Araneae, Agelenidae). Insect Biochem. Mol. Biol., 26:77–84. Treviranus, G. R. 1816. Die Afterspinne (Phalangium Latr.). Göttingen. Trivers, R. L. 1972. Parental investment and sexual selection. Pp. 136–179 in Sexual Selection and the Descent of Man (B. Campbell, ed.). Aldine, Chicago. Troiano, G. 1990. Karyotype and male meiosis of four species of Roncus L. Koch, 1973 (Pseudoscorpionida, Neobisiidae). Biol. Zool., 57:1–9. Troiano, G. 1997. Further studies on the karyology of the Pseudoscorpions of the gen. Roncus: the karyotype of Roncus gestroi and Roncus belluatii. Caryologia, 50:271– 279. Tsurusaki, N. 1982a. Chromosomes of the Japanese gagrellid, Paraumbogrella huzitai Suzuki (Gagrellidae, Opiliones, Arachnida). Bul. Br. Arachnol. Soc., 5:397–398. Tsurusaki, N. 1982b. Intersexuality and gynandromorphism in gagrellid harvestmen (Palpatores, Opiliones, Arachnida). Acta arachnol., 31:7–16.

569

Tsurusaki, N. 1985a. Geographic variation of chromosomes and external morphology in the montanum-subgroup of the Leiobunum curvipalpe-group (Arachnida, Opiliones, Phalangiidae) with special reference to its presumable process of raciation. Zool. Sci., 2:767–783. Tsurusaki, N. 1985b. Taxonomic revision of the Leiobunum curvipalpe-group (Arachnida, Opiliones, Phalangiidae). I. Hikocola-, hiasai-, kohyai-, and platypenis-subgroups. J. Sci. Hiroshima Univ., B1, 24:1–42. Tsurusaki, N. 1986. Parthenogenesis and geographic variation of sex ratio in two species of Leiobunum (Arachnida, Opiliones). Zool. Sci., 3:517–532. Tsurusaki, N. 1987. Two species of Homolophus newly found from Hokkaido, Japan (Arachnida: Opiliones: Phalangiidae). Acta arachnol., 35:97–107. Tsurusaki, N. 1989. Geographic variation of chromosomes in Sabacon makinoi Suzuki (Arachnida, Opiliones, Sabaconidae). Bull. Biogeogr. Soc. Japan, 44:111–116. Tsurusaki, N. 1990. Taxonomic revision of the Leiobunum curvipalpe group (Arachnida, Opiliones, Phalangiidae). III. Leiobunum curvipalpe subgroup. Japan. J. Entomol., 58:761– 780. Tsurusaki, N. 1993. Geographic variation of the number of Bchromosomes in Metagagrella tenuipes (Opiliones, Phalangiidae, Gagrellinae). Mem. Queensland Mus., 33:659– 665. Tsurusaki, N. 1999. Soil arthropod diversity on fragmented woodlands in the Tottori Plains, Honshu, Japan, and its conservation. J. Fac. Educ. & Region. Sci., Tottori Univ., 1:57–68. [In Japanese] Tsurusaki, N. 2003. Phenology and biology of harvestmen in and near Sapporo, Hokkaido, Japan, with some taxonomical notes on Nelima suzukii n.sp. and allies (Arachnida: Opiliones). Acta arachnol., 52:5–24. Tsurusaki, N. 2004. Are parthenogenetic females willing to mate with males? Implications of exaggerated male palpi in two thelytokous harvestmen. P. 163 in 16th International Congress of Arachnology. Ghent, Belgium. Tsurusaki, N., & J. C. Cokendolpher. 1990. Chromosomes of sixteen species of harvestmen (Arachnida, Opiliones, Caddidae and Phalangiidae). J. Arachnol., 18:151–166. Tsurusaki, N., & R. G. Holmberg. 1986. Chromosomes of Leiobunum japonicum japonicum and Leiobunum paessleri (Arachnida, Opiliones). J. Arachnol., 14:123–125. Tsurusaki, N., Y. Ihara, & T. Arita. 1993. Chromosomes of the funnel web spider Agelena limbata (Araneae, Agelenidae). Zool. Sci., 10:43–46. Tsurusaki, N., M. Murakami, & K. Shimokawa. 1991. Geographic variation of chromosomes in the Japanese harvestman, Gagrellopsis nodulifera, with special reference to a hybrid zone in western Honshu. Zool. Sci., 8:265–275.

570

References

Tsurusaki, N., & T. Shimada. 2004. Geographic and seasonal variations of the number of B chromosomes and external morphology in Psathyropus tenuipes (Arachnida: Opiliones). Cytogenet. Genome Res., 106:365–375. Tsurusaki, N., & D. Song. 1993. Occurrence of Crosbycus dasycnemus (Crosby) (Opiliones, Palpatores, Ceratolasmatidae) in China. Japan. J. Entomol., 61:175–176. Tsurusaki, N., & D. Song. 2000. Order Opiliones. Pp. 155–162, 523–527 in Pictorial Keys to Soil Animals of China (W.Y. Yin, ed.). Science Press, Beijing. Tsurusaki, N., A. N. Tchemeris, & D. V. Logunov. 2000a. Redescription of Scleropilio insolens from southern Siberia with comments on the genus Scleropilio (Arachnida: Opiliones: Phalangiidae). Acta arachnol., 49:87–94. Tsurusaki, N., A. N. Tchemeris, & D. V. Logunov. 2000b. Two new species of Opiliones from southern Siberia and Mongolia, with an establishment of a new genus and redefinition of the genus Homolophus (Arachnida: Opiliones: Phalangiidae). Acta arachnol., 49:73–86. Tugmon, C. R., J. D. Brown, & N. V. Horner. 1990. Karyotypes of seventeen USA spider species (Araneae, Araneidae, Gnaphosidae, Loxoscelidae, Lycosidae, Oxyopidae, Philodromidae, Salticidae and Theridiidae). J. Arachnol., 18:41– 48. Tulk, A. 1843. Upon the anatomy of Phalangium opilio. Ann. Mag. Nat. Hist., 12:153–165, 243–253, 318–331. Turner, G. F., & T. J. Pitcher. 1986. Attack abatement: a model for group protection by combined avoidance and dilution. Am. Nat., 128:228–240. Ubick, D., & T. S. Briggs. 1989. The harvestman family Phalangodidae. 1. The new genus Calicina, with notes on Sitalcina (Opiliones: Laniatores). Proc. Calif. Acad. Sci., 46:95–136. Ubick, D., & T. S. Briggs. 1992. The harvestman family Phalangodidae. 3. Revision of Texella Goodnight & Goodnight (Opiliones: Laniatores). Texas Mem. Mus., Speleol. Monogr., 3:155–240. Ubick, D., & T. S. Briggs. 2002. The harvestman family Phalangodidae. 4. A review of the genus Banksula (Opiliones, Laniatores). J. Arachnol., 30:435–451. Ubick, D., & T. S. Briggs. 2004. The harvestman family Phalangodidae. 5. New records and species of Texella Goodnight & Goodnight (Opiliones: Laniatores). Texas Mem. Mus., Speleol. Monogr., 6:101–141. Ubick, D., & J. A. Dunlop. 2005. On the placement of the Baltic amber harvestman Gonyleptes nemastomoides Koch & Berendt, 1854, with notes on the phylogeny of Cladonychiidae (Opiliones, Laniatores, Travunioidea). Mitt. Mus. Naturk. Berlin, Geowiss. Reihe, 8:75–82. Uetz, G. W., & C. S. Hieber. 1994. Group size and predation risk in colonial web-building spiders: analysis of attack abatement mechanisms. Behav. Ecol., 5:326–333.

Uetz, G. W., & C. S. Hieber. 1997. Colonial web-building spiders: balancing the costs and benefits of group-living. Pp. 458– 475 in The Evolution of Social Behavior in Insects and Arachnids (J. Choe & B. Crespi, eds.). Cambridge University Press, Cambridge. Ugland, K. I., J. S. Gray, & K. E. Ellingsen. 2003. The speciesaccumulation curve and estimation of species richness. J. Anim. Ecol., 72:888–897. Uhlenhaut, H. 2001. Beobachtungen zum Beutespektrum von Zitterspinnen (Pholcidae). Arachnol. Mitt., 22:37–41. Uyemura, T. 1935. Food-habit of a harvester, Gagrellula ferruginea (Loman). Journal of Zoology and Botany of Kishu-area, Wakayama, 1:19–21. [In Japanese] Vachon, M. 1944. L’appendice arachnidien et son évoluton: note préliminaire. Bull. Soc. zool. Fr., 69:172–177. Vachon, M. 1947. Nouvelles remarques à propos de la phorésie des Pseudoscorpions. Bull. Mus. Hist. nat. Paris, 19:84– 87. Vachon, M. 1976. Rudimentation et arthrogenèse des appendices de quelques arthropodes arachnides. Bull. Soc. zool. Fr., 101(suppl. 1):4–12. van der Borght, O. 1966. Peritrophic membranes in Arachnida (Arthropoda). Nature, 210:751–752. van der Hammen, L. 1978. The evolution of the chelicerate life-cycle. Acta biotheor., 27:44–60. van der Hammen, L. 1985. Comparative studies in Chelicerata. III. Opilionida. Zool. Verhand., 220:1–60. van der Hammen, L. 1986. Acarological and arachnological notes. Zool. Medel., 60:217–230. van der Hammen, L. 1989. An Introduction to Comparative Arachnology. SPB Academic Publishing, The Hague. Vázquez, I. M., & J. C. Cokendolpher. 1997. Guerrobunus vallensis, a new species of Harvestman (Opiliones: Phalangodidae), from a cave in Valle de Bravo, State of México, México. J. Arachnol., 25:257–261. Verhoeff, C. W. 1900. Zur Biologie von Ischyropsalis. Zool. Anz., 23:106–107. Vink, C. J., S. M. Thomas, P. Paquin, C. Y. Hayashi, & M. Hedin. 2005. The effects of preservatives and temperatures on arachnid DNA. Invertebr. Syst., 19:99–104. Vitt, L. J., & J. P. Caldwell. 2003. NSF Project DEB-9505518. Raw diet data from lizards collected near the Rio Juruá at Porto Walter, Acre during 1996. www.omnh.ou.edu/ per sonnel/her petology/NSF/DEB_9505518/Acre LizDiets.html Vitt, L. J., S. S. Sartorius, T. C. S. Avila-Pires, & M. C. Espósito. 1998. Use of time, space, and food by the gymnophthalmid lizard Prionodactylus eigenmanni from the western Amazon of Brazil. Canad. J. Zool., 76:1681–1688. Vulinec, K. 1990. Collective security: aggregation by insects as a defense. Pp. 251–288 in Insect Defenses: Adaptive Mecha-

References

nisms and Strategies of Prey and Predators (D. L. Evans & J. O. Schmidt, eds.). State University of New York Press, Albany. Vyas, A. B. 1974. The cheliceral muscles of the scorpion Heterometrus fulvipes. Bull. South. Calif. Acad. Sci., 73:9–14. Wachmann, E. 1970. Der Feinbau der sog. Kugelhaare der Fadenkanker (Opiliones, Nemastomatidae). Z. Zellforsch. mikrosk. Anat., 103:518–525. Wagner, H. O. 1954. Massenansammlungen von Weberknechten. Z. Tierpsychol., 11:348–352. Wainwright, S. A., W. D. Biggs, J. D. Currey, & J. M. Gosline. 1976. Mechanical Design in Organisms. Princeton University Press, Princeton, NJ. Walker, D. 1860. Notes on the zoology of the last Arctic expedition under Captain Sir F. M. L. M’Clintock. JR Dublin Soc., 3:61–77. Walker, M. E. 1928. A revision of the order Phalangida of Ohio. Bull. Ohio Biol. Survey, 4:150–175. Warburg, M. R., & G. A. Polis. 1990. Behavioral responses, rhythms, and activity patterns. Pp. 224–246 in The Biology of Scorpions (G. A. Polis, ed.). Stanford University Press, Stanford, CA. Wartmann, B. A. 1985. Vergleichende Untersuchungen zur Populations-, Brut- und Nahrungsökologie von Wasserpieper und Steinschmätzer im Dischmatal GR. Ph.D. Thesis, University of Zürich, Zürich, Switzerland. Wasgestian-Schaller, C. 1967. Die Autotomie-Mechanismen an den Laufbeinen der Weberknechte (Arach., Opil.). Ph.D. Thesis, Johann-Wolfgang-Goethe-Universität, Frankfurt am Main, Germany. Weed, C. M. 1892. The ash-gray harvest-spider. Am. Nat., 26:32–36. Weed, C. M. 1893a. An American species of Sabacon. Am. Nat., 27:574–576. Weed, C. M. 1893b. The cinnamon harvest-spider and its variations. Am. Nat., 27:534–541. Weed, C. M. 1897. Life Histories of American Insects. Macmillan Co., New York. Weiss, I. 1975. Untersuchungen über die Arthropodenfauna xerothermer Standorte im südsiebenbürgischen Hügelland. II. Weberknechte (Opiliones, Arachnida). Muzeul Brukenthal, Sibiu, Studii si Comunicari, Stiinte Naturale, 19:263–271. Weitschat, W., & W. Wichard. 2002. Atlas of Plants and Animals in Baltic Amber. Verlag Dr. Friedrich Pfeil, Scientific Publishers, Munich. Werren, J. H., U. Nur, & C-I. Wu. 1988. Selfish genetic elements. Trends Ecol. Evol., 3:297–302. Westheide, W., & R. M. Rieger. 1996. Spezielle Zoologie. Vol. 1: Einzeller und Wirbellose Tiere. Gustav Fischer Verlag, Stuttgart. Westwood, J. O. 1874. Thesaurus Entomologicus Oxoniensis (= Il-

571

lustrations of New, Rare, and Interesting Insects, for the Most Part Contained in the Collections Presented to the University of Oxford by the Rev. F. W. Hope, with Forty Plates from Drawings by the Author). Clarendon Press, Oxford. Weyenbergh, H., Jr. 1869. Sur les insectes du calcaire jurassique de la Bavière, qui se trouvent au Musée Teyler. Archiv. Mus. Teyler, 2:247–294. Weyenbergh, H., Jr. 1874. Notes sur quelques insectes du calcaire jurassique de la Bavière. Archiv. Mus. Teyler, 3:234– 236. Weygoldt, P. 1969. The Biology of Pseudoscorpions. Harvard University Press, Cambridge, MA. Weygoldt, P. 1984. L’autotomie chez les Amblypyges. Rev. Arachnol., 5:321–327. Weygoldt, P. 1985. Ontogeny of the arachnid nervous system. Pp. 20–37 in Neurobiology of Arachnids (F. G. Barth, ed.). Springer-Verlag, Berlin. Weygoldt, P. 2000. Whip Spiders (Chelicerata: Amblypygi): Their Biology, Morphology, and Systematics. Apollo Books, Stenstrup. Weygoldt, P., & H. F. Paulus. 1979. Untersuchungen zur Morphologie, Taxonomie und Phylogenie der Chelicerata. Z. zool. Syst. u. Evolut.-Forsch., 17:85–116, 177–200. Wheeler, A. G., Jr. 1976. Lygus bugs as facultative predators. Pp. 28–35 in Lygus Bug: Host Plant Interactions: Proceedings of a Workshop at the XV International Congress of Entomology (D. R. Scott & L. E. O’Keeffe, eds.). University Press of Idaho, Moscow. Wheeler, W. C., & D. S. Gladstein. 1994. MALIGN: a multiple sequence alignment program. J. Hered., 85:417–418. Wheeler, W. C., D. S. Gladstein, & J. DeLaet. 2002. POY version 3.0. Program and documentation available at ftp.amnh.org/pub/molecular. American Museum of Natural History. Wheeler, W. C., & C. Y. Hayashi. 1998. The phylogeny of the extant chelicerate orders. Cladistics, 14:173–192. Whitaker, J. O., Jr., & C. Maser. 1976. Food habits of five western Oregon shrews. Northwest Scie., 50:102–107. Whitaker, J. O., Jr., C. Maser, & L. E. Keller. 1977. Food habits of bats of western Oregon. Northwest Scie., 51:46–55. Whitaker, J. O., Jr., C. Maser; R. M. Storm, & J. J. Beatty. 1986. Food habits of clouded salamanders (Aneides ferreus) in Curry County, Oregon (Amphibia: Caudata: Plethodontidae). Great Basin Nat., 46:228–240. White, M. J. D. 1973. Animal Cytology and Evolution. 3rd ed. Cambridge University Press, Cambridge. Whiteley, D. A. A. 1961. Unusual feeding habits of a harvestman (Opiliones). Ent. Mon. Mag., 97:187. Wickham, H. F. 1918. Feeding habits of a harvest spider (Phalangida). Ent. News, 29:115. Wiemer, D. F., K. Hicks, J. Meinwald, & T. Eisner. 1978. Naph-

572

References

thoquinones in defensive secretion of an opilionid. Experientia, 34:969–970. Wiens, J. A. 1969. An approach to the study of ecological relationships among grassland birds. Ornithol. Monogr., 8:1– 93. Wiens, J. J., & M. J. Donoghue. 2004. Historical biogeography, ecology and species richness. Trends Ecol. Evol., 19:639– 644. Wiley, R. H., & J. Poston. 1996. Indirect mate choice, competition for mates, and coevolution of the sexes. Evolution, 50:1371–1381. Wilkens, H., J. Parzefall, & A. Ribowski. 1990. Population biology and larvae of the anchialine crab Munidopsis polymorpha (Galatheidae) from Lanzarote (Canary Islands). J. Crust. Biol., 10:667–675. Willemart, R. H. 2001. Egg covering behavior of the neotropical harvestman Promitobates ornatus (Opiliones, Gonyleptidae). J. Arachnol., 28:249–252. Willemart, R. H., 2002. Cases of intra- and inter-specific food competition among Brazilian harvestmen, in captivity (Opiliones, Laniatores, Gonyleptidae). Rev. Arachnol., 14:49–58. Willemart, R. H., & P. Gnaspini. 2004a. Breeding biology of the cavernicolous harvestman Goniosoma albiscriptum (Arachnida, Opiliones, Laniatores): sites of oviposition, egg batches characteristics and subsocial behaviour. Invertebr. Reprod. Dev., 45:15–28. Willemart, R. H., & P. Gnaspini. 2004b. Comparative density of hair sensilla on the legs of cavernicolous and epigean harvestmen (Arachnida: Opiliones). Zool. Anz., 242:353–366. Willemart, R. H., & P. Gnaspini. 2004c. Spatial distribution, displacement, gregariousness and defensive behavior in the Brazilian cave harvestman Goniosoma albiscriptum (Arachnida, Opiliones, Laniatores). Anim. Biol., 54:221– 235. Willemart, R. H., & G. E. Kaneto. 2004. On the natural history of the Neotropical spider Enoploctenus cyclothorax (Araneae, Ctenidae). Bul. Br. Arachnol. Soc., 13:53–59. Williams, G. C. 1962. Seasonal and diurnal activity of harvestmen (Phalangida) and spiders (Araneida) in contrasted habitats. J. Anim. Ecol., 31:23–42. Williams, G. C. 1975. Sex and Evolution. Princeton, University Press, Princeton, NJ. Willmer, P., G. Stone, & I. Johnston. 2000. Environmental Physiology of Animals. Blackwell Science, Oxford. Wilson, A. G., Jr., & J. H. Larsen Jr. 1988. Activity and diet in seepage-dwelling Coeur d’Alene salamanders (Plethodon vandykei idahoensis). Northwest Sci., 62:211–217. Wilson, E. O. 1971. The Insect Societies. Belknap Press, Cambridge, MA.

Wilson, E. O. 1975. Sociobiology: The New Synthesis. Belknap Press, Cambridge, MA. Winkler, D. 1957. Die Entwicklung der äusseren Körpergestalt bei den Phalangiidae (Opiliones). Mitt. zool. Mus. Berl., 33:355–389. Wise, D. H. 1993. Spiders in Ecological Webs. Cambridge University Press, Cambridge. Wolz, I. 1992. Zur Ökologie der Bechsteinfledermaus Myotis bechsteini (Kuhl, 1818) (Mammalia: Chiroptera). Ph.D. Thesis, Universität Erlangen-Nürnberg, Nuremberg, Germany. Wood, S. P., A. L. Panchen, & T. R. Smithson. 1985. A terrestrial fauna from the Scottish Lower Carboniferous. Nature, 314:355–356. Wooley, T. A. 1988. Acarology: Mites and Human Welfare. John Wiley & Sons, New York. Wrensch, D. L., J. B. Kethley, & R. A. Norton. 1994. Cytogenetics of holokinetic chromosomes and inverted meiosis: keys to the evolutionary success of mites, with generalizations on eukatyotes. Pp. 282–343 in Mites: Ecological and Evolutionary Analysis of Life-History Patterns (M. A. Houck, ed.). Chapman & Hall, New York. Wunderlich, J. 2004. General findings and conclusions. In Fossil Spiders in Amber and Copal (J. Wunderlich, ed.). Beitr. Araneol., 3A:321–329. Yadgarov, T. 1974. Feeding of the scheltopusik Ophisaurus apodus (Pallas) in the basin of the Surkhandarya river. Uzbekskiy Biol. Zhurnal, 1974:68–70. [In Russian] Yadgarov, T. 1977. Feeding of the gecko Teratoscincus scincus in the Kyzyl Kum Desert. Uzbekskiy Biol. Zhurnal, 1977:58–60. [In Russian] Yamazaki, K., H. Yahata, N. Kobayashi, & T. Makioka. 2001. Egg maturation and parthenogenetic recovery of diploidy in the scorpion Liocheles australasiae (Fabricius) (Scorpions, Ischnuridae). J. Morphol., 247:39–50. Yiyit, S., M. Tosunoglu, & A. Hüseyin. 1999. Feeding biology in Bufo viridis (Anura: Bufonidae) populations of the vicinity of Izmir. Turk. J. Zool., 23(suppl. 1):279–287. [In Turkish] Yoshikura, M. 1975. Comparative embryology and phylogeny of Arachnida. Kumamoto J. Sci., Biol., 12:71–142. Young, O. P., & T. C. Lockley. 1985. The striped lynx spider, Oxyopes salticus, in agroecosystems. Entomophaga, 30:329– 346. Zanger, K. 1995. Immunocytochemical localization of lysozyme in the nephrocytes of the harvestman, Leiobunum rotundum. Tissue Cell, 27:299–308. Zanger, K., D. R. Dannhorn; K. A. Seitz, & W. Peters. 1991. Nephrocytes of harvestmen, Leiobunum libatum and L. rotundum. Tissue Cell, 23:7–15.

References

Zeh, D. W., & R. L. Smith. 1985. Paternal investment by terrestrial arthropods. Am. Zool., 25:785–805. Zeh, D. W., J. A. Zeh, & R. L. Smith. 1989. Ovipositors, amnions and egg shell architecture in the diversification of terrestrial arthropods. Q. Rev. Biol., 64:147–168.

573

Zingerle, V. 1999. Spider and harvestman communities along a glaciation transect in the Italian Dolomites. J. Arachnol., 27:222–228. Zlotin, R. I. 1968. Materialuy po trophicheskim svyasam ptits v sujrtah Tyan’-Shanja. Ornitologiya, 9:158–163.

Taxonomic Index Note: Only valid names appearing in the text are cited. Suprageneric taxa are in upper case; non-harvestmen taxa cited in Tables 8.1 and 9.1–9.3 were omitted here. Terms marked with an asterisk can be found in the Subject Index.

Abasola borisi, 238 Abasola troglodytes, 238 Absonus, 244 Acanthocranaus, 187 Acanthomegabunus sibiricus, 124 Acanthopachylus aculeatus, 294, 322, 332, 361, 377, 382–383, 385, 396, 402, 404–405, 407, 435, 459, 523 Acanthoprocta pustulata, 345 ACARI, 3, 15, 51, 62, 64, 109, 266, 272, 416. See also Mites*; Ticks* Acihasta, 111 ACROBUNINAE, 76, 164, 166 Acrogonyleptes unus, 29 Acrographinotus, 53 Acromyrmex lobicornis, 285 Acropsopilio, 80, 115, 117 Acropsopilio boopis, 116 Acropsopilio chilensis, 110, 115 Acropsopilio chomulae, 115 Acropsopilio neozealandiae, 116 ACROPSOPILIONIDAE, 109 ACROPSOPILIONINAE, 60, 71, 84, 86, 89, 110, 113, 115, 117 Acuclavella, 73, 133–134, 136–137, 148 Acutisoma aff. proximum, 399, 402, 408 Acutisoma discolor, 326, 333, 404, 434, 443, 459 Acutisoma ensifer, 200 Acutisoma indistinctum, 434 Acutisoma longipes, 295, 314, 324, 331, 333, 335–336, 345, 353, 359–361, 363, 382, 389, 402, 404–405, 410, 420, 422, 434, 459 Acutisoma proximum, 325, 349, 351, 361, 366, 401, 404, 435, 459, 462, 471

Acutisoma unicolor, 197 ADAEINAE, 375 ADAEINI, 76, 164, 239, 243, 375 Adaeulum, 75 Adaeulum robustum, 383 Adaeum, 161 ADENOPHOREA, 343 AGORISTENIDAE, 76, 82, 167, 168, 171–173 AGORISTENINAE, 90, 171–173 Akdalima, 224, 226 Akdalima jamaicana, 224 Alausius, 185 Algidia, 421 Algidia viridata, 285 Allocranaus, 185 Amauropilio atavus, 249 Amauropilio lacoei, 249 Ambatoiella vigilans, 183 AMBLYPYGI, 51, 63, 254, 266. See also Whip spiders* Americovibone lanfrancoae, 121–122 Amilenus, 21, 113, 130–131 Amilenus aurantiacus, 129, 287, 362, 403, 405 Ampheres, 196 Ampheres leucopheus, 434 Amphitrogulus sternalis, 263 AMPYCINAE, 91, 168, 196, 198–199, 203 Ampycus telifer, 200 Anduzeia punctata, 184 Anelasmocephalus, 132, 157 Anelasmocephalus cambridgei, 158, 293, 303, 314, 351, 375, 378, 433, 458 Anelasmocephalus hadzii, 314, 330 Ankaratra, 101 ANOETIDAE, 368 Anoetus, 369 Anolis, 396

Anthracosiro, 254 Anthus pratensis, 365 ANURA, 351, 450. See also Frogs*; Toads* APHIDAE, 329, 336, 398, 408 APICOMPLEXA, 342, 517 Apodemus flavicollis, 365 ARACHNIDA, 25, 62–65, 272, 344–345, 359–362, 479 Arachnocampa luminosa, 326 ARANEAE, 3–4, 51, 62, 254, 260, 272, 316, 365, 378. See also Spiders* ARANEOMORPHAE, 317 Archaeometa, 256 Arganotus, 224 Argiope, 365 Arion, 318 ARIONIDAE, 317 Assamia westermanni, 173 ASSAMIIDAE, 75–76, 81–84, 86, 90, 162–166, 169, 173, 175–176, 185, 221, 234, 505 ASSAMIINAE, 164, 175–176 Astrobunus grallator, 465 Astrobunus laevipes, 39, 269, 287, 305 Auranus parvus, 294, 296, 437 Ausobskya, 220 Austrapurcellia, 101 Austropsopilio, 80, 115, 117–118 Austropsopilio sudamericanus, 116 AVES, 354–355, 358. See also Birds* Baculigerus, 192, 245, 378 Baculigerus littoris, 192, 285 Badessa, 224, 226 Ballarra alpina, 122 Ballarra longipalpus, 122 BALLARRINAE, 90, 110–111, 121–123 Banksula, 220, 221

575

576

Taxonomic Index

BELLOSTOMATIDAE, 452 Benoitinus, 82, 226 Berlesecaptus convexus, 196 Biantes, 163 Biantes albimanus, 176 Biantes parvulus, 176 Biantes sherpa, 179 BIANTIDAE, 56, 76, 82–84, 163, 166–167, 169, 176, 179, 204, 221, 226, 232, 505 BIANTINAE, 86, 90, 164, 166, 176–177, 179 BIANTOIDEA, 76, 204, 224 Biantoncopus, 213–214 Biantoncopus fuscus, 212 Bishopella, 220 Bishopella laciniosa, 219, 352 Bittacus mastrillii, 365 Blattella germanica, 402 Blechroscelis, 336 Bogdana ingenua, 200 Bolama, 175 Bolama spinosa, 175 Bourguyia albiornata, 285, 359–361, 363–364, 404, 421, 423, 434 BOURGUYIINAE, 91, 196, 198–200, 203 Brasiloctis bucki, 222 Brasilogovea, 93 Brigantibunum listoni, 248 Bufo ictericus, 366 Bufo marinus, 350 Bunochelis canariana, 344 Buparellus, 221 Bupares, 221 Caddella, 80, 115, 117–118 Caddella africana, 117 Caddella capensis, 116 CADDIDAE, 71, 80, 83, 110, 113, 115, 118, 259, 495 CADDINAE, 71, 84, 86, 89, 109–110, 113, 117–119 Caddo, 80, 110, 115, 117–118, 259, 264 Caddo agilis, 16, 21, 110, 116–118, 267, 270, 287, 324, 327 Caddo dentipalpis, 248, 258, 261 Caddo pepperella, 117 CADDOIDEA, 17–18, 22, 43, 67, 71, 73, 110, 118 Cadeadoius niger, 200, 436 CAELOPYGINAE, 78, 91, 161–162, 164, 168, 198–199, 201, 203, 283, 377, 443, 484

Caenoncopus, 212–214 Caenoncopus cuspidatus, 212–213 Calathocratus beieri, 158 Calicina, 219–221 Calicina digita, 219 Calicina minor, 307 Calicina serpentinea, 219 Camarana, 199 Camarana flavipalpi, 436 CARABIDAE, 302, 330, 363 Caribbiantes, 179 Carinostoma ornatum, 342, 353 CARNIVORA, 353 CAUDATA, 352. See also Salamanders* Centetostoma bacilliferum, 287 Ceratolasma, 19, 133–134, 136–137, 141, 148 Ceratolasma tricantha, 39, 134, 137–138 CERATOLASMATIDAE, 72–73, 77, 81, 84, 88, 90, 133–139, 141, 147, 500 Ceratomontia centralis, 497 CERATOPOGONIDAE, 345, 347 Cersa kratochvili, 244 CESTODA, 343, 518 CHALCIDOIDEA, 371 CHARADRIIFORMES, 354 Cheiromachus coriaceus, 249, 260 Chelifer cancroides, 259 CHERNETIDAE, 368 Chileogovea, 26, 34, 69, 99–101 Chileogovea oedipus, 27, 100 CHILOPODA, 359, 375, 419. See also Centipedes* CHIROPTERA, 353 CHLOROPIDAE, 372 CHRYSOMELIDAE, 336 CLADONYCHIIDAE, 76, 81, 90, 165, 170, 179–182, 216, 217, 239, 260 CLAUSILIIDAE, 317, 330 Cobania picea, 197, 200 COBANIINAE, 91, 168, 196, 199, 202 COLEOPTERA, 272, 363. See also Beetles* COLLEMBOLA, 323, 328, 332, 367–368, 419, 520, 523 CORACIIFORMES, 354 CORINNIDAE, 359 COSMETIDAE, 5, 16, 73, 75–76, 82–83, 160–166, 169, 182–185, 188, 203, 229, 320,

360, 364, 378, 393, 395, 469, 495 COSMETINAE, 90, 161, 164, 184 Cosmetus, 160, 336 Cosmetus peruvicus, 183 Cosmetus variolosus, 469 Cosmobunus granarius, 44, 403 Costabrimma, 245 CRANAIDAE, 76, 78, 82, 91, 168, 169, 185, 188, 203, 229, 469 CRANAINAE, 91, 164, 168, 185–188 Cranaus, 187 Cristina lettowi, 344 Crosbycus, 73, 132–137, 141, 142 Crosbycus dasycnemus, 140–141 Crosbyella, 220 Crosbyella inermichela, 226 CRUSTACEA, 257 Cryptomaster, 180 CRYPTOSTEMMATOIDAE, 63 Ctenus, 364 CUCULIFORMES, 354 Cupiennius, 54 Cutervolus, 185, 187 Cychrus, 330 CYCLOPHYLLIDEA, 343 Cynorta, 344, 353 Cynorta astora, 385, 390 Cynorta roeweri, 344 Cynortoides cubanus, 404–405, 434, 521, 524 Cynortula oblongata, 183 CYPHOPHTHALMI, 5, 8, 11, 15, 18, 21–31, 35, 41–45, 49, 51, 56, 60, 63, 66–70, 75, 77–82, 92–95, 160, 163, 264, 283, 296, 306, 328, 377, 382–383, 386–387, 391–396, 416–418, 425, 427, 438, 448–449, 461, 465, 470, 472, 495, 496, 499–503, 507–508 Cyphophthalmus, 103–104, 132 Cyphophthalmus aff. teyroski, 368, 369 Cyphophthalmus cimiciformis, 94 Cyphophthalmus corsicus, 92 Cyphophthalmus duricorius, 39, 56, 89, 103, 311, 384, 456 CYPRINIFORMES, 351 Daguerreia inermis, 283, 284 Dalquestia, 71, 126, 128 Dalquestia formosa, 129, 131, 267, 287 DAMPETRINAE, 164, 175

Taxonomic Index

DEINOPIDAE, 324 Delena cancerides, 274 Dendrolasma mirabile, 149 Dendrolasma parvula, 284 DIBUNINAE, 164–167, 189, 191 Dibunus albitarsus, 191 Dicranolasma, 132, 142, 145, 151, 321 Dicranolasma cristatum, 144 Dicranolasma hirtum, 144 Dicranolasma pauper, 144 Dicranolasma scabrum, 39, 293, 313, 328, 342, 345, 359, 361, 376, 378, 432, 457, 465–467, 470 Dicranolasma soerenseni, 269 DICRANOLASMATIDAE, 19, 22, 73, 81, 83–84, 90, 133, 136, 142–145, 151, 159, 327, 328, 334, 378, 470 Dicranopalpus, 113, 126, 129, 130–131, 264 Dicranopalpus gasteinensis, 293 Dicranopalpus ramiger, 260 Dicranopalpus ramosus, 375, 431 DIDELPHIMORPHIA, 353 Didelphis, 396 Didelphis aurita, 367 Digalistes, 187 DIGENEA, 343 Dinopilio gigas, 254, 255 DIPLOPODA, 359, 419. See also Millipedes* DIPTERA, 316–317, 327, 345, 363. See also Flies* Discocyrtoides nigricans, 17 Discocyrtus, 196–197, 294, 360–361, 378, 396, 406–407 Discocyrtus dilatatus, 435 Discocyrtus invalidus, 39, 306, 345 Discocyrtus oliverioi, 306, 331–333, 361, 406–407, 421, 423, 435, 459 Discocyrtus pectinifemur, 363, 421, 423, 436, 459 Discocyrtus prospicuus, 326, 436, 459 Discocyrtus testudineus, 200, 407 Discosoma, 160 DISCOSOMATICINAE, 90, 164, 184 DROMOPODA, 4, 64, 65 DYSDERIDAE, 271 DYSPNOI, 5, 8, 17–31, 41–43, 51, 60, 63, 66–76, 81, 83, 86–89, 110, 115–118, 131–132,

135, 160, 163, 165, 256, 264, 270, 296, 299, 310, 328, 374, 377–381, 386, 387, 430, 438–440, 448–449, 461, 465–468, 482–483, 500–505, 524 DYSPNOLANIATORES, 67–68, 72, 87 Echinopustulus samuelnelsoni, 248, 253, 255 Egaenus, 123, 125 Egaenus convexus, 300, 345 ENANTIOBUNINAE, 90, 110–111, 114, 121–123, 126 Enantiobunus, 111 Encheiridium montanum, 407 ENCHYTREIDAE, 317 Engyodonthium aranearum, 348 enigmaticus, 93 Enoploctenus cyclothorax, 335–336, 396 ENSIFERA, 363 Entomophaga batkoi, 348–349 Eophalangium, 40 Eophalangium sheari, 248, 252 EOPHRYNIDAE, 254 EOTROGULIDAE, 255 Eotrogulus fayoli, 248, 253, 255 EPEDANIDAE, 81, 84, 91, 162–165, 168–170, 188–191, 221, 234 EPEDANINAE, 76, 164, 166 EPEDANOIDEA, 76 EPHEMEROPTERA, 327, 471 EPHYDRIDAE, 372 Equitius, 76 Equitius doriae, 342, 345, 368 Erebomaster, 180 Erebomaster acanthina, 181 Erebomaster flavescens, 314 ERECANANINAE, 164–166 Erginulus, 319 Erginulus clavotibialis, 361, 404, 434, 458, 465 ERYTHRAEIDAE, 347, 519 ESCADABIIDAE, 82, 85, 91, 168, 170, 179, 191, 209, 232, 245, 378, 505 Escadabius, 191, 193 Escadabius ventricalcaratus, 192 Ethobunus, 245 Ethobunus cubensis, 244 Eubaeorix, 175 Eubaeorix gravelyi, 175 Eubalta meridionalis, 345

Eucynortula albipunctata, 385 Eucynortula lata, 295–296, 434 Eucynortula metatarsalis, 183 Eucynortula nannocornuta, 385 EUGREGARINORIDA, 342 Eugyndes, 407 Eumeces fasciatus, 319 Eumesosoma nigrum, 351 Eumesosoma roeweri, 268, 345, 354, 456 EUPNOI, 5, 8, 10, 17–31, 41–42, 51, 60, 63, 66–83, 87–89, 108–119, 160, 163, 165, 251, 257, 264–265, 270, 282, 296, 299, 310, 379–383, 386–395, 401–402, 405, 419, 425–430, 438, 448, 461, 465–468, 470, 472, 482–483, 495, 500–505, 511 Eurybunus, 126, 345 EURYPTERIDA, 64, 253. See also Eurypterids* Eusarcus, 160 Eutimesius, 227 Euzaleptus minutus, 287 Fageibiantes bispina, 176 Fangensis, 92–93, 104–106 Fangensis cavernarus, 105 Fangensis leclerci, 70, 420, 422 Feretrius, 224 Ferkeria vestita, 183 FISSIPHALLIIDAE, 76, 82, 91, 167, 170, 194–196, 207, 245, 505 Fissiphallius martensi, 194–195 Fissiphallius sturmi, 195 Flirtea, 183 Floridogovea, 93 Fudeci, 208 Fudeci curvifemur, 208 Fumontana, 75–76, 81 Gagrella, 344 Gagrella alba, 345 Gagrella curvispina, 345 Gagrella formosae, 345 Gagrella sexmaculata, 345 Gagrella varians, 287, 297 GAGRELLINAE, 80–84, 90, 109–114, 126, 128, 130–131, 270, 361, 387, 401–402 Gagrellopsis, 131 Gagrellopsis nodulifera, 131, 268, 274–276, 345 Gagrellula, 344, 405

577

578

Taxonomic Index

Gagrellula ferruginea, 268, 274, 312, 321, 345, 465 Gagrellula montana, 465 Gagrellula saddlana, 322, 342, 380, 399, 403, 522–523 Galeodes, 63 Galibrotus carlotanus, 179 GALLIFORMES, 354 GASTROPODA, 316, 359. See also Gastropods*; Snails and slugs* Geaya, 129 Geraecormobius, 407 Gertia hatschbachi, 197 Gilarovia turcica, 149 Giupponia chagasi, 306 Gjellerupia, 244 Globipes, 126, 287, 345 Gnomulus, 213–214 Gnomulus asli, 211 Gnomulus baharu, 212 Gnomulus crassipes, 214 Gnomulus imadatei, 213 Gnomulus rostratus, 212 Gnomulus sumatranus, 212 Goniosoma, 160, 345, 382, 396, 435, 459 Goniosoma aff. badium, 35 Goniosoma albiscriptum, 402, 404–405, 410, 421, 423, 435, 459 Goniosoma catarina, 382, 404, 435 Goniosoma geniculatum, 404, 435, 459 Goniosoma spelaeum, 270–271, 295, 310, 314, 322–324, 331, 333, 345, 353, 359, 363–364, 367, 380, 385, 391, 394, 398, 404, 421, 423, 435, 459, 462, 466–468, 470 GONIOSOMATINAE, 78, 91, 196, 198–199, 201, 203, 283, 324, 331, 333, 382, 395, 402, 412, 442, 450 GONYASSAMIINAE, 91, 203 Gonyleptes, 160, 383 Gonyleptes curticornis, 270 Gonyleptes fragilis, 343, 393 Gonyleptes horridus, 73, 404 Gonyleptes pectinatus, 382 Gonyleptes saprophilus, 363, 435 GONYLEPTIDAE, 5, 51, 73, 75–76, 78, 82, 87, 161–170, 185, 188, 196, 198, 203, 229, 283, 315, 324, 328, 333–334, 348, 377–378, 380–381,

391–393, 395–396, 449, 466, 470, 480, 484, 494, 498, 521 GONYLEPTINAE, 91, 161–162, 164, 196, 198, 202–203, 283, 443 GONYLEPTOIDEA, 74–76, 81, 85–86, 165, 173, 176–177, 184–185, 191, 193, 208, 211, 224, 229, 234, 395, 440, 447, 469 Graecophalangium atticum, 342 Gragellula niveata, 344 Granulosoma, 130 Graphinotus, 201 GRASSATORES, 17, 31, 42–43, 51, 60, 66, 75–76, 81, 83, 163, 168, 176, 214, 221, 224, 465, 468, 471 GRUIFORMES, 355 Gryne coccineloides, 401 Gryne orensis, 404, 407, 434, 459 Guasinia delgadoi, 195 Guasinia persephone, 195 GUASINIIDAE, 76, 82, 91, 167–168, 196, 204, 207 Guerrobunus, 220 Gyas, 39, 283 Gyas annulatus, 129, 287, 403, 405, 432 Gyas titanus, 129, 344, 432 GYINAE, 80, 90, 110, 112, 114, 126, 130–131, 402 Haasus, 220 Hadogenes troglodytes, 317 Hadrobunus maculosus, 312, 384 Halitherses grimaldii, 248 HAPLOCNEMATA, 64 Harmanda instructa, 287, 297 Harmanda kanoi, 287 Harmanda nigrolineata, 287, 297 Hasseltides primigenius, 257 HELICIDAE, 317 Helicoverpa zea, 336 HEMIPTERA, 363, 446, 449 Hendea myersi, 315, 437 Hendea myersi cavernicola, 315, 326 Hernandaria scabricula, 407, 435, 459 HERNANDARIINAE, 91, 162, 164–165, 167, 196, 199, 202–203, 283, 393 Hesperonemastoma, 73, 133–134, 136–137, 139–142, 148, 156 Hesperonemastoma modestum, 39, 139

Hesperopilio, 80, 115, 117–118 Hesperopilio mainae, 117 HETEROCRANAINAE, 91, 164, 168, 187–188 Heteromitobates discolor, 199 HETEROPACHYLINAE, 91, 168, 198–199, 201 Heteropodoctis quinquespinosus, 223 HETEROSTYGNINAE, 91, 164, 227, 229 Himalphalangium dolpoense, 287, 297 Himalphalangium nepalense, 287, 297 Himalphalangium palpale, 287 Himalphalangium spinulatus, 124 Himalphalangium suzukii, 287 Hinzuanius, 163 Histricostoma, 264 Histricostoma drenskii, 313 Histricostoma tuberculatum, 260–261 Histricostoma (?) tuberculatum, 258 Holmbergiana weyenberghi, 407 Holoscotolemon, 81, 180 Holoscotolemon querilhaci, 433, 460 Holoscotolemon unicolor, 76, 181 Holosiro, 93 Holoversia nigra, 407 Homalenotus quadridentatus, 129, 269, 287, 313, 457, 465–467 Homolophus, 125, 263 Homolophus arcticus, 124, 267 Homolophus biceps, 390, 456 Hoplobunus, 232, 234 Hoplobunus boneti, 233, 437, 460 Hoplobunus queretarius, 233 Hoplodino hoogstraali, 223 Hovabiantes, 176–177 Hovanoceros, 82 Huitaca, 69, 93–98 Huitaca ventralis, 96 Hummelinckiolus silhavyi, 248 HYMENOPTERA, 316, 345, 363. See also Wasps* Hymenostilbe verrucosa, 348 Iandumoema uai, 306 IBALONIINAE, 164–166 Ibantila cubana, 222 Iberosiro, 68, 104 Icaleptes malkini, 206 ICALEPTIDAE, 76, 82, 91, 167, 170, 196, 205, 207, 245 ICHNEUMONIDAE, 371 Iguapeia melanocephala, 436

Taxonomic Index

Innoxius magnus, 228 INSECTIVORA, 353 INSIDIATORES, 17, 31, 42, 43, 60, 66, 74–76, 81, 162–163, 167–168, 468, 470 Iporangaia, 201 Iporangaia pustulosa, 284, 320, 345, 359, 364, 462 ISCHYROPSALIDIDAE, 22, 37, 71–72, 81, 83–84, 131, 133–136, 141, 145, 310, 322, 328, 387, 391, 430, 466, 500 ISCHYROPSALIDOIDEA, 18, 26, 42–43, 67, 72, 131, 133–134, 141–142, 147, 430 Ischyropsalis, 22, 58, 132–137, 147, 153–154, 300, 321, 330, 386, 388, 464, 523 Ischyropsalis apuana, 352 Ischyropsalis hadzii, 146 Ischyropsalis hellwigii, 146, 293, 313, 322, 327, 352, 361, 420, 422, 457 Ischyropsalis hellwigii hellwigii, 313, 317–318, 329–330 Ischyropsalis hellwigii lucantei, 317, 433, 465 Ischyropsalis hellwigii mulleneri, 57 Ischyropsalis kollari, 16, 147, 293, 313, 317, 328 Ischyropsalis luteipes, 57, 146, 269, 317, 420, 422, 432, 457, 464–465 Ischyropsalis manicata, 37, 39, 146 Ischyropsalis nodifera, 145, 433, 457, 465 Ischyropsalis pyrenaea, 269, 313, 317, 433, 458, 465 Ischyropsalis ravasinii, 146 Ischyropsalis strandi, 57, 58, 317, 433, 458, 523 Isolachus, 216–217 ISOPODA, 316. See also Isopods* Jim, 191 Jussara, 471 Jussara flamengo, 17, 130 Jussara luteovariata, 129 Jussara rosea, 17, 19, 24, 29 Kainonychus, 216–217 Kalominua, 224, 226 KAOLINONYCHINAE, 92, 242 Karamea, 437 Karos, 232, 234 Karos rugosus, 233

Karripurcellia, 99–101 Karripurcellia peckorum, 100 Kimula, 207–208, 248, 261 Kimula cokendolpheri, 208–209 Kimula elongata, 206 KIMULIDAE, 91, 170, 179, 193, 204, 207–209, 245, 261 Krusa, 345 Kustarachne, 256 Kustarachne conica, 256 Kustarachne extincta, 256 Kustarachne tenuipes, 248, 253, 256 KUSTARACHNIDA, 256 Lacinius, 303, 354 Lacinius dentiger, 320, 342–345, 351, 353, 360–361 Lacinius ephippiatus, 267, 286, 288, 302–303, 305, 311, 320–321, 342, 345, 351, 355, 357–358, 361–362, 431, 456 Lacinius horridus, 288, 311, 342–343, 345–346, 351–352, 360–363, 431, 456 Lacinius insularis, 342 Lacurbs, 179 Lacurbs spinosa, 179 LACURBSINAE, 85, 90, 167, 176–177 Lamprochernes nodosus, 368 LANIATORES, 5, 8, 63, 67–78, 81–82, 86–89, 159–168, 193, 205, 214, 234, 259, 264, 285, 351, 353, 361, 380–383, 387, 390–392, 395–396, 406, 439, 440, 445–449, 465–472, 483, 499–503, 524 Lanthanopilio, 126 Larifuga, 75 Larifuga capensis, 383 Larifugella natalensis, 383 Latrodectus geometricus, 364 Latrodectus hasselti, 4 LEIOBUNINAE, 80, 83, 90, 110–114, 126, 128, 130–131, 262, 270, 310, 315, 320–322, 328, 331, 337, 362, 402 Leiobunum, 21, 26–30, 34–35, 46–49, 254, 260, 271, 274, 282, 285, 289, 301, 313, 315, 320, 341, 344–346, 351–352, 357, 360–362, 375, 379, 387, 392, 395, 398, 465, 523 Leiobunum aff. depressum, 345

Leiobunum aldrichi, 282, 286, 312, 321, 324, 344, 345, 356, 359–362, 380–381, 384, 390, 397, 403, 410, 420, 422, 432, 482 Leiobunum alvarezi, 403 Leiobunum aurugineum, 351, 403, 407 Leiobunum blackwalli, 268, 288, 301, 303, 312, 342, 344, 351, 353, 359–362, 380, 432 Leiobunum “cactorum,” 402, 411 Leiobunum calcar, 19, 286, 304, 312, 344, 351, 356, 384, 420, 422, 432, 467, 482 Leiobunum crassipalpe, 268 Leiobunum curvipalpe, 268 Leiobunum desertum, 403, 405 Leiobunum flavum, 345, 403, 407, 432 Leiobunum formosum, 344, 347, 384 Leiobunum globosum, 268, 272, 288, 322–323, 342–343, 465 Leiobunum hemisphaericum, 457, 461 Leiobunum hiasai, 268 Leiobunum hikocola, 268 Leiobunum ischionotatum, 403 Leiobunum japanense, 268 Leiobunum japonicum, 268, 288 Leiobunum japonicum tawanum, 129 Leiobunum kohyai, 268 Leiobunum leiopenis, 384 Leiobunum limbatum, 268, 306, 312, 362, 403 Leiobunum longipes, 249, 260, 467 Leiobunum manubriatum, 268, 272, 288, 322–323, 342–343 Leiobunum montanum, 268, 274, 345 Leiobunum nigripalpi, 385 Leiobunum nigripes, 29, 268, 312, 327, 334, 341–342, 344–345, 380 Leiobunum oharai, 129 Leiobunum politum, 282, 286, 312, 341–342, 345, 359–360, 362, 467, 482 Leiobunum rotundum, 268, 285, 288, 301, 303, 306, 312, 320, 323, 331, 336, 342–345, 351, 353, 356, 359, 361, 362, 432, 457, 461, 464, 467 Leiobunum rumelicum, 342, 360, 369

579

580

Taxonomic Index

Leiobunum rupestre, 268, 288, 357, 375 Leiobunum sadoense, 268 Leiobunum speciosum, 344, 385, 403 Leiobunum tohokuense, 268, 274 Leiobunum townsendi, 288, 341, 345, 360, 385, 388, 402–403, 407, 457 Leiobunum ventricosum, 269, 282, 313, 344–345, 385, 471 Leiobunum vittatum, 32–33, 282, 285, 313, 319, 344–345, 356, 359–360, 362, 380, 385, 390, 407, 420, 422, 432, 457, 467, 482 LEIOSTENINAE, 82, 90, 168, 171, 173 Lepchana spinipalpis, 433 LEPIDOPTERA, 327, 336 LEPTOBUNINAE, 109, 112 Leptobunus, 125 Leptobunus parvulus, 369 Leptostygnus leptochirus, 172 Leptus, 341 Leuronychus pacificus, 342 Leytpodoctis oviger, 375, 436, 460 Lichirtes, 171 Licornus, 185 LIMACIDAE, 317 Limulus, 25, 28, 39, 48, 58 Liopilio yukon, 112 LISSAMPHIBIA, 351–352. See also Amphibians* LITHOBIOMORPHA, 359 Lola, 220–221 Lomanella, 217, 239, 468 Lomanius longipalpus mindanaoensis, 223 Longiperna zonata, 360, 364, 435 Lophopilio, 303, 327 Lophopilio palpinalis, 268, 289, 300, 302–303, 312, 321, 342–345, 358, 431, 456 LYCOSIDAE, 302, 324, 336, 396 Maevia inclemens, 278 Maiorerus, 220 Maiorerus randoi, 306 MALLOPHAGA, 369–370 Manangotria, 101 Manaosbia, 210 Manaosbia scopulata, 376 MANAOSBIIDAE, 76, 78, 91, 168–169, 209–211, 348, 349, 378, 469

MANTISPIDAE, 371 Marthana nigerrima, 345 Marwe, 93, 104 Marwe coarctata, 82, 103 MECOPTERA, 363 Megabunus, 327 Megabunus diadema, 268, 289, 312, 342, 344, 375–376, 431, 465, 494 MEGALOPSALIDINAE, 90, 110, 113, 118–120 Megalopsalis, 111 Megalopsalis tumida, 311, 326 Melanopa, 312, 321 Melanopa grandis, 130, 268, 278, 465 Melanopa unicolor, 268 Mermerus, 175 MERMITHIDAE, 340–346, 518, 519 Metabiantes, 82, 177 Metacynortoides obscurus, 350, 351 Metagagrella tenuipes, 344 Metagovea, 93–97 Metagryne albireticulata, 183 Metagyndes pulchella, 345 Metakimula, 206–209 Metalibitia, 184 Metalibitia argentina, 404, 407 Metalibitia paraguayensis, 434 Metamarthana fusca, 345 Metaplatybunus carneluttii, 362 Metaplatybunus grandissimus, 342 Metaplatybunus hypanicus, 112 Metarrhizium anisopliae, 348 METASARCINAE, 82, 91, 168, 185, 196, 198–199, 201, 203 Metasiro, 93–95, 97, 104 Metasiro americanus, 17, 19, 24, 29, 44, 96–97 Metasiro philipi, 96 Metavonones hispidus, 404 Metavononoides, 183–184, 336 Meterginus, 185 Metopilio, 80, 112, 126, 128–131, 289 Microcina, 220, 307 Microcina homi, 219 MICROSPORIDA, 340, 342 Microsporidium weiseri, 347 Minuella, 206–208 Minuella dimorpha, 206 MINUIDAE, 76, 82, 85, 165–166, 207 Minuides, 207, 245 Minuides milleri, 244

MINUINAE, 166 Miopsalis, 92, 104, 106 Mischonyx cuspidatus, 270, 295, 306, 331, 360–361, 406–407, 435 Misumena vatia, 320, 336 Mitobates, 160, 196, 435 Mitobates triangulus, 5, 196 MITOBATINAE, 73, 78, 91, 161, 164, 198–199, 202 Mitobatula, 196 Mitopus, 46–47, 126, 301, 303, 342, 355, 357 Mitopus ericaeus, 267 Mitopus glacialis, 289, 311, 323, 332 Mitopus morio, 39, 42, 126, 267, 272, 282, 284–285, 289, 300–303, 305, 311, 315, 320–321, 323–324, 327, 330, 332, 336, 342–347, 351–353, 355–358, 360–363, 380, 420, 422, 431, 456, 464–465 Mitostoma, 150 Mitostoma chrysomelas, 269, 289, 351, 353, 359, 363, 423, 433 Mitostoma gracile, 149, 360, 361 Mitostoma pyrenaeum, 433, 458 Mitraceras, 82, 226 MOLLUSCA, 359 MONOSCUTIDAE, 71, 84, 86, 109–110, 113, 118, 120, 125 MONOSCUTINAE, 90, 110, 113, 118–120 Monoscutum, 111 Musca domestica, 272 Muscicola picta, 285 MYGALOMORPHAE, 317 MYRIAPODA, 310, 316 Nelima, 81, 301, 345 Nelima aladjensis, 360 Nelima elegans, 360, 403, 405 Nelima genufusca, 269, 290, 432 Nelima gothica, 301 Nelima nigricoxa, 269, 274–275, 322–323, 345 Nelima paessleri, 269, 313, 345, 362, 379, 401–403, 405, 410 Nelima satoi, 269, 274 Nelima semproni, 290, 305–306, 313 Nelima silvatica, 269, 344 Nelima similis, 269 Nelima suzukii, 290, 432

Taxonomic Index

Nemastoma, 132–135, 255, 303, 354, 367 Nemastoma bidentatum sparsum, 149, 306 Nemastoma bimaculatum, 286, 293, 297, 300, 303, 313, 320–321, 493 Nemastoma dentigerum, 269, 465 Nemastoma incerrtum, 249 Nemastoma lugubre, 17, 19, 24, 27, 266, 269, 293, 300, 311, 313, 351, 353, 356, 361, 423, 433, 464 Nemastoma lugubre bimaculatum, 379 Nemastoma quadripunctatum, 294, 458, 467 Nemastoma triste, 149, 294 NEMASTOMATIDAE, 18–19, 26, 28, 71, 73, 81, 131, 133–136, 144–151, 159–160, 255, 259, 283, 310, 315, 322, 328, 334, 352, 368, 430, 502, 505 NEMASTOMATINAE, 84, 90, 132, 150–151 Nemastomella bacillifera, 433 Nemastomoides, 255 Nemastomoides depressus, 255 Nemastomoides elaveris, 248, 255 Nemastomoides longipes, 248, 253, 255 NEMASTOMOIDIDAE, 255 NEMATODA, 343, 518. See also Nematodes* NEMATOPHORA, 359 Neocranaus, 187 Neogovea, 93–97 Neogovea kartabo, 93 Neogovea mexasca, 83, 94, 103 Neogovea microphaga, 95 NEOGOVEIDAE, 68–70, 79–86, 89, 93–95, 106, 108 Neopilio, 111 Neopilio australis, 122 NEOPILIONIDAE, 71, 80, 84, 86, 109–113, 120–121, 125–126 NEOPILIONINAE, 90, 110–111, 114, 121, 123 Neopurcellia, 101 Neosadocus, 197, 435 Neosadocus maximus, 284 Neosadocus aff. variabilis, 314, 319–321, 325, 332–333 Neoscotolemon, 226 Neosiro, 93 Nephila, 256

Nesopachylus monoceros, 386 Nezara viridula, 411 Nilgirius scaber, 175 NIPPONONYCHINAE, 92, 242 NIPPONOPSALIDIDAE, 73, 81–84, 90, 133, 136, 145, 151, 153, 159, 500 Nipponopsalis, 153 Nipponopsalis abei, 152–153, 269, 382, 458, 467 Nipponopsalis abei longipes, 153 Nipponopsalis coreana, 152–153 Nipponopsalis yezoensis, 153 NOCTUIDAE, 320 Nomoclastes, 227 Nomoclastes quasimodo, 228 Nomoclastes taedifer, 228 NOMOCLASTINAE, 91, 227–229 Nomuraea atypicola, 348 NOVOGENUATA, 64 Nuncia, 75, 421 Odiellus, 301 Odiellus aspersus, 267, 272, 290, 431 Odiellus gallicus, 27, 57, 431, 456, 464–465, 522 Odiellus lendli, 342, 345, 360 Odiellus pictus, 342, 345, 351, 359, 360 Odiellus spinosus, 300–301, 311, 342, 353, 380, 431 Odiellus tridens, 493 Odiellus troguloides, 290, 300, 362 Odontobunus, 125 Odontosiro, 102, 104 Ogovea, 69, 92–93, 95, 98 Ogovea cameroonensis, 98 OGOVEIDAE, 68–70, 79–82, 85, 89, 93–97 Ogovia, 93 OLIGOCHAETA, 311, 316. See also Earthworms* OLIGOLOPHINAE, 81, 90, 109–110, 114, 125 Oligolophus, 301, 303, 354, 362–363, 464 Oligolophus hanseni, 267, 290, 303, 344, 431 Oligolophus tridens, 32, 267, 290–291, 300–301, 303, 305, 311–312, 320, 332, 342, 344–345, 349, 353, 357, 360, 362–363, 380, 431, 456, 465, 493 Oligovonones brunneus, 184

ONCOPODIDAE, 21, 31, 66, 75–76, 81–84, 91, 161–169, 211, 214 ONCOPODOIDEA, 74–75, 167 Oncopus, 161, 213–214 Oncopus acanthochelis, 214 Oncopus feae, 212 Oncopus truncatus, 211–212, 214 Opilio, 46–47, 49, 57, 125, 259, 301, 343–344, 362 Opilio canestrinii, 57, 267, 306, 344 Opilio dinaricus, 291, 342, 345 Opilio ovalis, 249 Opilio parietinus, 21, 44, 125, 267, 301, 306, 311, 320, 336, 342–345, 352–353, 356, 359–362, 431, 456, 461, 464 Opilio pentaspinulatus, 344 Opilio ravennae, 291 Opilio ruzickai, 267, 306, 342, 344–345, 360–361, 363 Opilio saxatilis, 291, 301, 306, 312, 336, 342, 362, 363 OPILIONINAE, 80, 90, 110, 112, 114, 123, 125–126 Opiliotarbus, 254 Opistophthalmus carinatus, 317 Oppalnia, 342 Oreina cacaliae, 330 Orsa daphne, 224 Ortholasma levipes, 368 Ortholasma rugosum, 149 ORTHOLASMATINAE, 22, 73, 81, 83–84, 90, 133, 148, 150–151, 257 ORTHOPTERA, 272, 397 OSTEICHTHYES, 351 Osteopilus septentrionalis, 350 Ostracidium, 160 Oxyopes salticus, 337 Pachycondyla villosa, 364 Pachylicus, 245 PACHYLINAE, 91, 164, 196, 198–199, 201, 203 Pachyloidellus, 497 Pachyloidellus borellii, 307 Pachyloidellus butleri, 368 Pachyloidellus fulvigranulatus, 307 Pachyloidellus goliath, 295–296, 314, 324, 326, 331, 334–345, 351, 376, 386, 390, 402, 404–405, 436, 490 Pachyloides thorelli, 377, 436, 459

581

582

Taxonomic Index

PACHYLOSPELEINAE, 91, 198, 203 Pachylospeleus strinatii, 306, 314 Pachylus quinamavidensis, 41, 362, 436, 459, 463–465, 470 Paecilaema eutypa, 385, 390 Paecilaema pectinigerum, 183 Paecilaemana quadripunctata, 343, 385, 390 Palaeoncopus, 211, 213–214 Palaeoncopus gunung, 212 PALPATORES, 63, 66–68, 70–71, 73, 77, 109, 131, 160, 162–163, 165, 257 PALPIGRADI, 21, 264 Pandora phalangicida, 348 Panolis, 348 Pantopsalis, 111, 120 Parabalta, 199 Parabeloniscus, 221 Paragovia, 93–97 Paragovia sironoides, 93, 95–96 Paraligolophus meadi, 112 Paralola, 217, 220–221 Paramiopsalis, 68, 102, 104 Paramiopsalis ramulosus, 103 Paramitraceras, 232, 234 Paramitraceras granulatus, 233 Parampheres, 199 Parampheres ronae, 377 Paranemastoma, 351, 354, 523 Paranemastoma aurigerum aurigerum, 359, 361 Paranemastoma aurigerum ryla, 342, 345, 361 Paranemastoma bicuspidatum, 291 Paranemastoma kochi, 39 Paranemastoma quadripunctatum, 291, 300, 313, 320–324, 326, 328, 357, 359–360, 362, 420, 422–423, 433, 483 Paranemastoma radewi, 313, 341–343, 345, 353–354, 360 Paranemastoma sillii, 458, 464–467 Paranemastoma superbum, 149 PARANONYCHINAE, 76, 81, 83, 92, 242–243 Paranonychus, 75, 216–217 Paranuncia, 75 Paranuncia ingens, 39 Parapachyloides fontanensis, 436, 459 Parapurcellia, 101, 108 Parasiro, 92, 94, 102, 104

Parasiro coiffaiti, 103, 267, 270, 311, 456 Parasiro minor, 102–103 Paraumbogrella pumilio, 130, 268, 291 Pardosa lugubris, 305 Parogovia pabsgarnoni, 287, 296 Paroligolophus agrestis, 112, 291, 301, 303, 305, 311, 334, 336, 344–345, 351, 353, 359, 362, 380, 431, 465 Paroligolophus meadii, 112, 291 Pashokia yamadai, 175 Pasohnus bispinosus, 191 PASSERIFORMES, 355 Peladoius, 185 Pellenes, 272 Pellobunus, 224, 226 Pellobunus proavus, 249 Peltonychia, 75, 239 Peltonychia clavigera, 76, 238, 437 Peltonychia leprieuri, 238 Peltonychia postumicola, 238 PENTANYCHIDAE, 75–76, 81, 83, 91, 171, 182, 214, 216–217, 239 Pentanychus, 75, 182, 216–217 Pentanychus bilobatus, 215 Pentanychus hamatus, 215 Petrunkevitchiana oculata, 249, 258, 262 PETTALIDAE, 68–70, 80–87, 89, 95, 99 Pettalus, 69, 92–94, 99, 101 Pettalus cf. brevicauda, 16 Pettalus lampetides, 100 PHALANGIDA, 15, 23, 25, 30–33, 43, 46, 50, 56, 60, 63, 67–70, 77, 160, 507 PHALANGIIDAE, 37, 45, 71, 80, 84, 86, 109–114, 118, 120, 123, 126, 128, 160, 163, 259, 261, 270, 285, 310, 315–316, 321–322, 328, 331, 336, 342, 343, 352–353, 355–358, 362, 375, 391, 396–397, 416, 466, 470 PHALANGIINAE, 78, 80, 82, 90, 109–110, 112, 114, 125–126 Phalangillum hirsutum, 263 PHALANGIOIDEA, 17, 22, 30–33, 36, 40, 42–46, 49, 51, 67, 71–72, 77, 109–111, 120, 125–128, 160, 251, 262, 379, 449, 480, 496, 500–503

PHALANGIOTARBIDA, 254–255, 264 Phalangites, 247 Phalangites priscus, 257 Phalangium, 49, 57, 63, 123, 125, 132, 134, 160, 249, 254, 259, 263, 301, 309, 343–345, 354, 357, 382 Phalangium cinereum, 456 Phalangium cornutum, 457, 461 Phalangium crassum, 342 Phalangium opilio, 4, 15, 21, 36–37, 40–41, 44, 50–51, 53–54, 109, 124–125, 259, 267, 274, 285, 291, 300–301, 304–306, 312, 320, 322, 329, 336, 341–345, 351–354, 356–357, 359–363, 380, 384, 403, 431, 457, 464–467, 471, 482, 524 Phalangium succineum, 248, 259 Phalangodes, 220–221 Phalangodes armata, 352 PHALANGODIDAE, 73–76, 81, 84, 86, 91, 161–170, 217–221, 261, 322, 495, 505 Phalangodinella, 207 PHALANGODOIDEA, 75–76, 165 Phalangopus subtilis, 260 Phareicranaus, 185, 187 Philacarus hispaniolensis, 248 Philander opossum, 366–367, 396 Phoenicurus ochruros, 365 Phoenicurus ochruros gibraltariensis, 365 PHOLCIDAE, 4, 379 PHORIDAE, 345, 347–348, 372 Phrynus, 63 Piassagera brieni, 197 PICIFORMES, 358 Pickeliana, 227 Picunchenops, 76, 239 Picunchenops spelaeus, 75 Pieris rapae, 336 Pitangus sulphuratus, 365 Plato, 331 PLATYBUNINAE, 81, 90, 110, 112, 114, 125–126 Platybunus, 327, 354–355, 357 Platybunus bucephalus, 292, 302, 312, 321, 327, 342–345, 355–358, 362–363, 365, 407, 457 Platybunus pallidus, 357 Platybunus pinetorum, 312, 343, 352, 357

Taxonomic Index

Platybunus triangularis, 457, 465 Platycynorta clavifemur, 183 PLATYHELMINTHES, 343, 347, 359 Plesiosiro madeleyi, 254 PODOCTIDAE, 76, 82–86, 91, 164–166, 169, 221–222, 232, 505 Pokhara occidentalis, 292 Polystichum, 369 POMPILIDAE, 340, 371 Porrhothele, 51 Prionostemma, 402–403, 408 Prionostemma farinosum, 129 Prionostemma panama, 345 Prionostemma wagnerii, 403, 405 Pristocnemis farinosus, 376 Procerus, 330 PROGONYLEPTOIDELLINAE, 91, 167, 198–199, 201, 203, 283, 377 Progonyleptoidellus orguensis, 436 Progonyleptoidellus striatus, 270, 436 Proholoscotolemon nemastomoides, 249 Promitobates ornatus, 197, 421, 423, 435 Prosclerosoma hispanicum, 269 Proscorpius, 64 Proscotolemon, 220 PROSTYGNINAE, 91, 164, 168, 185, 187, 188 Prostygnus, 187 Prostygnus vestitus, 187 Protimesius, 227 Protimesius laevis, 228 Protimesius longipalpis, 404, 437 Protodiasia saltensis, 244 PROTOLOPHIDAE, 71, 80, 90, 110–114, 127–128, 270 Protolophus, 112, 127, 343 Protolophus singularis, 119, 292, 345 Protolophus tuberculatus, 268, 278 Protopilio, 255 Psathyropus tenuipes, 268, 273–274, 292, 432 Pselaphochernes dubius, 368 Pseudastrobunus, 130 Pseudobiantes japonicus, 270–271, 434, 460, 470 Pseudogagrella, 131 Pseudogyndesoides, 17, 19, 24, 44 Pseudomelanopa, 131 Pseudopachylus, 199, 202

Pseudopachylus longipes, 19, 200, 270 Pseudopucrolia, 376 Pseudopucrolia mutica, 200 PSEUDOSCORPIONES, 15, 63, 64, 266, 272, 419. See also Pseudoscorpions* Pseudotrogulus, 375 PSOCOPTERA, 316 Ptychosoma, 220 Puna, 185 Purcellia, 92, 94, 99, 101 Purcellia ilustrans, 383 PYCNOGONIDA, 56, 257 Pygobunus okadai, 129 Pygophalangodus, 497 Pygophalangodus canalsi, 436, 460 Pyza bosnica, 342, 345, 352–353 Rakaia, 100–101 Rakaia macra, 100 RALLIFORMES, 358 Rana rugosa, 272 Recifesius pernambucanus, 194 REDUVIIDAE, 375 Reventula, 224, 226 Reventula amabilis, 224 Rezendesius lanei, 197 RHABDITIDA, 340, 343, 518 Rhabdotarachnoides simoni, 255 Rhampsinitus, 125 Rhaucus vulneratus, 184 RICINULEI, 20, 51, 63–64, 254, 256, 378 Rilaena, 46, 54, 125 Rilaena balcanica, 125, 342–343, 360 Rilaena cf. serbica, 342–343, 345–346, 359 Rilaena serbica, 342 Rilaena triangularis, 53, 268, 292, 300, 312, 320–321, 324, 327, 342–344, 351–352, 356–357, 362, 407, 420, 422, 432 Riosegundo birabeni, 285 RODENTIA, 354 Roeweria virescens, 16 Roquettea singularis, 184 Ruschia, 196 Sabacon, 136, 141, 154, 156 Sabacon claviger, 249 Sabacon crassipalpis, 155 Sabacon dentipalpis, 155 Sabacon imamurai, 155, 294, 433

Sabacon makinoi, 269, 274, 294, 433 Sabacon paradoxus, 155, 269, 328, 386, 433 Sabacon pygmaeus, 39, 269 Sabacon vizcayanus, 433, 458 SABACONIDAE, 22, 26, 28, 71–73, 77, 81, 84, 86, 90, 133–135, 154–156, 259, 500 Sadocus, 196 Sadocus funestus, 344 Sadocus ingens, 196 SALMONIFORMES, 351 SALTICIDAE, 324 Samoa, 224 Samoa variabilis, 224, 226 SAMOIDAE, 76, 78, 82–86, 91, 162, 165, 170, 179, 224, 226, 232, 261 SAMOOIDEA, 76, 179, 193, 209, 226, 232 Santinezia, 185, 187, 434 Santinezia hermosa, 187 Santinezia serratotibialis, 434 Saramacia, 210 SARASINICINAE, 76, 164, 166 Sbordonia, 232, 234 Scabrobunus, 175 Scabrobunus filipes, 175 SCELIONIDAE, 371 SCHIZOMIDA, 21, 264, 382 SCLEROBUNINAE, 81, 83, 92, 242 Sclerobunus, 75–76, 365, 379 Sclerobunus nondimorphicus, 39 Sclerobunus robustus, 292, 354, 359, 386 Scleropilio, 111, 123 Scleropilio insolens, 124 Sclerosoma, 128, 375 SCLEROSOMATIDAE, 5, 45, 71, 80, 84, 86, 110, 120, 126–131, 270, 285, 297, 310, 345, 375, 377, 396, 397, 466 SCLEROSOMATINAE, 80, 90, 109–114, 126–131, 270 SCORPIONES, 15, 63–65, 254, 271. See also Scorpions* Scotolemon, 73, 219, 220, 264, 327 Scotolemon doriae, 436, 460 Scotolemon lespesi, 436, 460, 523 Scotolemon lucasi, 436, 460 Scotolemon nemastomoides, 260 SCYTODIDAE, 260 SECERNENTIA, 343 SEGESTRIDAE, 271

583

584

Taxonomic Index

Sickesia, 227 Siro, 63, 94, 101–102, 104, 108–109, 254, 361, 369 Siro acaroides, 93 Siro aff. teyrovski, 368–369 Siro exilis, 384 Siro kamiakensis, 93, 103 Siro kartabo, 93 Siro minutus, 343 Siro platypedibus, 249, 258, 261 Siro rubens, 56, 89, 267, 311, 456, 465, 470 Siro sonoma, 103 SIRONIDAE, 63, 66–70, 77–80, 84, 86, 89, 95, 101–104, 322 Sirula, 93 Sitalcina, 219–220 Sodreana sodreana, 19, 27, 325 SODREANINAE, 91, 167, 198–203, 283, 393 Soerensenella, 437 SOERENSENELLINAE, 92 Soledadiella macrochelae, 245 Solenopsis invicta, 306 SOLIFUGAE, 15, 20, 51, 63, 64, 254. See also Solifuges* SØRENSENELLINAE, 242 Sorex araneus, 367 Sorex minutus, 365 Spaeleoleptes spaeleus, 306 Spaeloleptes, 193 Speleomaster, 180 Speleomaster lexi, 181 Speleonychia, 75, 239 Speleosiro, 99–101 Sphaerobunus, 198 SPHECIDAE, 371 Sphoeroforma familiaris, 244 Spinicranaus diabolicus, 187 Spinicrus, 111, 120 Spinicrus nigricans, 39 Spinivunus, 185 SPOROZOASIDA, 342 SQUAMATA, 352, 375. See also Lizards* STAPHYLINIDAE, 302 Steinernema carpocapsae, 341 STENOSTYGNINAE, 90, 164, 168, 176–177, 179, 226 Stenostygnus, 177 Stenostygnus pusio, 177 Stenotrogulus, 254 STRIGIFORMES, 358 STYGNICRANAINAE, 91, 168, 185, 187–188

STYGNIDAE, 75–76, 82, 165, 169, 203, 226–229, 469 STYGNINAE, 91, 161, 164, 227, 229 Stygnoleptes analis, 243 Stygnomma spiniferum, 386, 396 STYGNOMMATIDAE, 76, 78, 82–85, 91, 164–168, 179, 204, 229–232, 505 Stygnoplus clavotibialis, 228 STYGNOPSIDAE, 75–76, 81–85, 91, 165–167, 170, 173, 176, 232–234 Stygnopsis, 232, 234 Stygnopsis valida, 233 Stygnus, 160, 227, 325 Stygnus luteus, 228 Stygnus multispinosus, 388 Stygnus pectinipes, 228 STYLOCELLIDAE, 68–70, 79, 80, 83, 84, 89, 94, 98, 104–106 Stylocellus, 56, 70, 92–93, 104, 106 Stylocellus globosus, 105 Stylocellus ramblae, 105 Stylocellus sumatranus, 70, 104 Styloleptes conspersus, 29 STYLOMMATOPHORA, 359 Suzukielus, 93, 101–104 Suzukielus sauteri, 103 Syncranaus cribum, 209 Synthetonychia, 75 Synthetonychia acuta, 236 Synthetonychia cornua, 236 Synthetonychia glacialis, 236 Synthetonychia minuta, 236 Synthetonychia oparara, 236 SYNTHETONYCHIIDAE, 42, 75–76, 81, 86, 92, 167–168, 216, 235, 239, 243, 343, 345 Systenocentrus japonicus, 130, 268 Takaoia, 191 Tandikudius rugosus, 375 Taracus, 73, 131, 133–135, 141, 148, 154, 156 Taracus birsteini, 155 Tasmanonyx, 75 Tasmanopilio, 80, 115, 117, 118 Tasmanopilio fuscus, 39, 116–117 Tegipiolus, 207 Tegipiolus pachypus, 208–209 TEMPEROPHTHALMI, 68–69, 101 Tenebrio, 523 Tenebrio molitor, 317 TETRAPULMONATA, 64 Texella, 219–221, 283, 306

Texella cokendolpheri, 284, 306 Texella mulaiki, 219 Texella reddelli, 306 Texella reyesi, 219, 306 Texella spinoperca, 219 Thaumatocranaus, 185 Thelyphonus, 63 Thereza, 196 Thereza speciosa, 197 Thermus aquaticus, 508 Theromaster, 180 Theromaster brunnea, 76 THOMISIDAE, 324 Thrasychirus, 111, 122–123, 343 Thrasychirus dentichelis, 122, 345 Thrasychirus modestus, 122, 345 THROMBIDIIDAE, 347 Togwoteeus biceps, 269, 313, 343, 345, 351, 359 Tolus, 220 Tomicomerus, 141, 154, 156 Torrubiella gonylepticida, 349 Trachyrhinus marmoratus, 282, 292, 345 Trachyrhinus rectipalpus, 345, 352 Traiania, 243 Tranteeva, 104 Travunia, 237 Travunia anophthalma, 238 TRAVUNIIDAE, 74–76, 81, 83, 92, 165–168, 171, 180, 216, 235–239, 243 TRAVUNIOIDEA, 73–76, 81, 84, 86, 167, 180, 235, 239, 395, 468 TREMATODA, 343, 518 TRIAENOBUNINI, 74, 76, 165 Triaenobunus, 76 TRIAENONYCHIDAE, 31, 42, 74–78, 81–83, 86, 162–167, 170, 216, 222, 235, 239, 242, 243–343, 345, 395, 495, 499, 500, 504 TRIAENONYCHINAE, 92, 164, 239, 242 TRIAENONYCHINI, 243 TRIAENONYCHOIDEA, 75–76, 81, 84, 86 Tribolium, 523 TRICLADIDA, 359 TRICOMMATINAE, 78, 91, 164–167, 170, 196, 198, 199, 202–203, 295, 407 TRIGONOTARBIDA, 64, 254–257 Trinella bubonica, 172 Trinella matintaperera, 172

Taxonomic Index

Tripilatus, 185 Troglosiro, 69, 94, 108 Troglosiro aelleni, 94 Troglosiro juberthiei, 107 Troglosiro longifossa, 107 Troglosiro raveni, 108 TROGLOSIRONIDAE, 68–70, 80, 84, 86, 89, 93–94, 106 TROGULIDAE, 19, 31, 43, 71, 73, 81, 84, 90, 131–136, 144, 157, 159–160, 255, 263, 286, 300, 317, 322, 328, 334, 352, 378, 464, 524 TROGULOIDEA, 18, 22, 26, 30, 45, 61, 67, 71–73, 131–132, 135, 145, 153, 159, 264 Trogulus, 36, 55, 63, 132, 145, 151, 157, 160, 255, 269, 351, 363, 375 Trogulus closanicus, 269 Trogulus coriziformis, 352 Trogulus gypseus, 39 Trogulus longipes, 248, 263 Trogulus nepaeformis, 39, 53, 269, 294, 306, 314, 317, 361, 420, 422, 433, 458 Trogulus tingiformis, 16 Trogulus torosus, 5 Trogulus tricarinatus, 4, 158–159, 294, 314, 342, 360, 420, 422, 433, 458 TROMBICULIDAE, 345, 347 TROMBIDIIDAE, 519

TROPICOPHTHALMI, 68, 69, 98, 106 Tryferos elegans, 187 Tryferus, 187 Typhlobunus, 175 Typhlobunus troglodytes, 175 Undulus, 220 UROPYGI, 63, 254, 256, 266, 382. See also Whip scorpions* Vandaravua carli, 375 Ventrifurca, 185 Ventrisudis mira, 187 Ventrivomer ancyrophorus, 187 Vibone, 111 VITRINIDAE, 317 Vonones, 184 Vonones octotuberculatus, 183 Vonones ornatus, 404–405, 407, 409, 434 Vonones sayi, 270–271, 342, 345, 351, 385, 390, 434, 459, 465 Wespus, 220 Xerogrella dolpensis, 293 XIPHOSURA, 64. See also Horseshoe crabs* Yania, 187 Yania metatarsalis, 187

Yapacana, 227 Yuria, 216, 239 Zachaeus anatolicus, 342, 345 Zachaeus crista, 342–345, 347, 352, 356, 362 Zachaeus hebraicus, 345 Zacheus, 125 Zairebiantes, 176 Zairebiantes microphthalmus, 179 ZAIREBIANTINAE, 90, 167, 177, 179 Zaleptiolus implicatus, 293 Zalmopsylla, 205 Zalmopsylla platnicki, 206 ZALMOXIDAE, 5, 31, 76, 82–86, 92, 162, 163, 170, 196, 205, 207, 243–246, 495 Zalmoxis lavacaverna, 244 Zalmoxista, 224 ZALMOXOIDEA, 76, 82, 85, 207, 226 Zamora vulcana, 172 ZAMORINAE, 90, 168, 171–173 Zelurus travassosi, 364 ZONITIDAE, 317 Zortalia inscripta, 200 Zuma, 75–76 Zygopachylus, 210 Zygopachylus albomarginis, 362–363, 386, 393, 421, 423, 436, 460

585

Subject Index Note: Terms marked with an asterisk can be found in the Taxonomic Index.

Abdomen. See Opisthosoma Abiotic factors and activity patterns, 296–298, 331–332, 482–487 and distribution, 8, 282–283, 285–286, 475, 480–481 and gregariousness, 402, 405, 409, 412–413 Acetic acid, 382, 496, 505, 511, 512, 514, 515, 518 Active hunting, 9, 323–326, 332–333. See also Foraging Activity pattern, 331–332, 333, 371, 484–487 Adaptation, 126, 283, 300, 330, 409, 411, 412–413, 449, 478, 482–483 Adenostyle, 70, 95, 96, 98, 101, 102, 103, 105, 106, 107, 108 Adhesive organs, 20, 328. See also Glandular setae Africa, 5, 6, 78, 79, 80, 81, 82, 84, 85, 86, 93, 97, 98, 112, 118, 130, 144, 151, 159, 167, 179, 222, 226, 245, 282, 307 Afrotropical region, 78, 82 Aggregation, 11, 379, 380, 398, 400 attack-abatement effect, 408–409, 412–413 composition, 402, 405 defense, 406, 408–409 dense or mass, 401–402 dilution effect, 406, 408–409 loose, 401–402 multi-species, 406, 407 pheromone, 398, 411–412 reproduction, 409–410 resting sites, 403–404, 405 seasonality, 405, 486 sex ratio, 402 Agroecosystems, 336–337 Alarm pheromone, 11, 383,

398–399, 406, 408, 411, 413 Alcohol, 384, 385, 396, 408, 449, 507, 517, 519, 520 Aldehyde, 385, 408, 449 Algae, 312, 339, 367, 370 Alpine habitat, 282, 478 Alps, 80, 144, 156, 282 Altitude, 78, 80, 123, 184, 191, 282, 296, 297–298, 522. See also Vertical distribution Amazon forest, 188, 196, 211, 229, 296 Amazonian region, 82, 97, 184, 203, 231 Amber, 247, 261–263 Baltic, 80, 248, 249, 250, 257–260, 264–265, 367 Bitterfeld, 249, 258, 261 Dominican, 248, 249, 258, 260–261 Lebanese, 257, 261 Myanmar, 248, 257, 258 Ambush, 9, 323–324, 325, 332–333. See also Foraging Amphibians, 322. See also LISSAMPHIBIA* Amphinotic distribution, 79, 80 Amphipacific distribution, 79, 80, 151 Anachoresis, 374, 377, 380 Anal gland, 69, 70, 94, 95, 97, 101, 102, 104, 106, 108 Anal operculum, 18, 19, 25–26, 152, 182, 194, 205, 216, 220, 369, 470, 503 Anatolia, 81, 151 Andean region, 82, 184, 203 Andes, 97, 203, 211 Ant nests, 8, 285, 404 Antarctica, 8, 79, 280 Antifreezing, 439, 481, 491 Antilles, 130, 167, 173, 176, 179, 211, 229 Ants, 10, 282, 306, 311, 312, 314,

350, 364, 375, 378, 380, 395, 396, 399, 447. See also Taxonomic Index for specific taxa Anus. See Anal operculum Aposematism, 374, 376, 377–378, 428 Appendotomy, 21, 28, 30, 31, 46, 54, 259, 378, 379–380, 449, 495 Arboreal species, 283–285, 315–317, 333, 377, 484, 490–491, 495, 521 Arculi genitals, 25, 34 Argentina, 2, 3, 78, 80, 82, 84, 85, 118, 123, 184, 203, 241, 243, 244, 285, 295, 296, 307, 331, 334, 368, 376, 441 Armature. See Integumentary ornamentations Arolium, 31, 180, 215, 216, 469–470 Articulations, 19, 20, 28–31, 64, 68, 496 Asia, 5, 6, 74, 79, 80, 81, 82, 83, 84, 85, 93, 106, 125, 126, 130, 142, 151, 153, 156, 159, 176, 179, 191, 214, 216, 222, 282, 307, 315, 404, 437 Astragalus, 19, 30–31, 171, 230, 231 Atlantic forest, 78, 87, 184, 281, 319, 376, 442 Atlas, 81, 151 Australia, 1, 2, 4, 69, 79, 80, 81, 82, 84, 85, 86, 94, 101, 111, 118, 120, 122, 123, 125, 162, 175, 176, 222, 226, 240, 241, 243, 244, 245, 248, 257, 305, 350, 368 Australian region, 78, 83 Austria, 3, 267, 268, 269, 287, 288, 289, 290, 291, 292, 293, 294, 300, 304, 306

587

588

Subject Index

Autospasy. See Appendotomy Autotilly. See Appendotomy Autotomy. See Appendotomy Bacteria, 47–48, 49, 339, 346, 348, 368, 370, 397, 516–517, 518–519 Balkan Peninsula, 81, 104 Bangladesh, 176 Banks, Nathan, 5 Basitarsus. See Metatarsus Beetles, 3, 263, 302, 311, 312, 313, 314, 315, 322, 327, 330, 336, 365, 406, 430, 523. See also COLEOPTERA* Belize, 81, 231, 234 Benzoquinones, 377, 385, 386, 395, 396, 397, 408 Bhutan, 156, 176 Biological control, 336–337 Biological rhythms. See Activity pattern Biomass, 301–302, 340, 372 Birds, 9, 265, 305, 311, 312, 320, 322, 334, 350, 365, 377, 379, 397. See also AVES* Blood. See Hemolymph Bobbing, 9, 378–379, 449 Body-size, 5, 8, 42–43, 68, 282–283, 300, 327–328, 340, 372, 466, 477, 500–501. See also Taxonomic Index for specific taxa Bogs, 282, 285, 304 Bolivia, 118, 183, 188, 401 Book lungs, 46, 254, 475–477 Borneo, 79, 106 Bosnia and Herzegovina, 3, 147, 237 Brain. See Nervous system Brazil, 2, 3, 9, 73, 80, 118, 123, 173, 183, 184, 188, 191, 193, 203, 204, 209, 210, 211, 231, 243, 245, 257, 270, 281, 283, 284, 285, 294, 295, 296, 306, 319, 364, 367, 401, 441, 443, 444, 445, 462, 471, 484, 486 British Virgin Islands, 350 Bromeliad dwellers, 285, 404, 434, 445–446 Brood care. See Parental care Bulgaria, 346, 347 Burma. See Myanmar

Caatinga, 203 Calcaneus, 19, 30–31, 153, 157, 199, 201, 225, 230, 231, 232 Calcium carbonate, 33, 39, 286, 317–318 Cameroon, 98, 179 Camouflage, 9, 19, 285, 339, 370, 375, 440. See also Crypsis Campaniform sensilla, 19, 20–21 Canada, 80, 117, 118, 156, 243, 269, 282, 401 Canary Islands, 220, 306 Cannibalism, 321–322, 331, 367, 411, 442, 447, 451, 524 Captivity, 12, 310, 322–323, 331, 332–333, 365, 518–519, 520–524 Carapace, 18, 21–23 mesopeltidium, 21, 151, 256 metapeltidium, 21, 136, 141, 151, 154, 256 propeltidium, 21, 110, 115, 256 Carboniferous, 248, 250, 252, 253, 254, 255–256, 264 Caribbean region, 82, 84, 85, 184, 226, 261 Carpathians, 144, 147 Caucasus, 80, 81, 144, 151, 159 Cave dwellers, 8, 12, 22, 56, 58, 75, 283, 284, 306, 307, 326, 327, 331, 332–333, 367, 380, 398, 401, 402, 403, 404, 405, 432, 433, 434, 435, 437, 442, 445–446, 447, 462, 482, 483, 484, 486–487, 522, 523. See also Troglobites; Troglophiles; Trogloxens Cementing glands, 425 Cenozoic, 248–249, 257–263, 264, 265 Centipedes, 72, 302, 319, 375, 447, 450. See also CHILOPODA* Central America, 6, 184, 211, 403, 404, 423, 437 Cephalothorax. See Prosoma Cerrado, 203 Chaco, 82, 203 Chelicerae, 18–19 bulla, 224 function, 310, 315, 317–318, 323, 327–328, 329–330, 333, 337, 381–382,

420–423, 426, 430, 438–439, 479 morphology, 26–27 sexual dimorphism, 430, 439 See also Taxonomic Index for specific taxa Cheliceral glands, 11, 26, 27, 72, 137, 139, 141, 142, 143, 147, 150, 156, 420, 423, 430, 438 Chemical secretion, 3, 9–10, 11, 350, 374, 381, 382–383, 406, 408, 430 chemistry, 384–386, 395–396, 408, 448–449 effectiveness, 396–397, 448–449 emission, 291–395 fluid displacement, 210, 388–391 pharmaceutical effects, 383 pheromonal role, 397–399, 406, 411–412 physiological, clastogenic and antibiotic action, 397 Chemical shield, 391–394, 395 Chemoreception, 20, 326–327 Chile, 69, 80, 82, 84, 85, 101, 118, 122, 123, 203, 240, 241, 243 China, 2, 78, 81, 126, 135, 156, 191, 214 Chitin, 40, 329 Chorion, 425, 462 Chromosome, 11, 266, 278 B chromosomes, 272–274 geographic variation, 274– 277 hybrid zones, 26, 274–277 number, 266–271 polymorphism, 274, 277–278 polyploidy, 272 preparation techniques, 511–516 sex system, 11, 271–272 structure, 271 Circulatory system, 46–47 Cladistics, 64, 67, 68–69, 72, 74, 76, 77, 94, 97, 98, 101, 104, 106, 108, 131, 133, 137, 141, 147–148, 156, 167–168, 176, 191. See also Phylogeny Cline, 277, 501. See also Geographic variation Coal measures, 254–256

Subject Index

Cockroaches, 402, 406, 408, 411, 523 Cold resistance, 405, 464, 481, 522–523 Collection beating tray, 490, 493, 495 behavioral traps, 490, 492 Berlese funnels, 490, 492, 495 continuous trapping, 490, 491 corrugated cardboards, 490, 492, 493 ecological sampling, 489–494 extraction methods, 490, 492 hand collecting, 489–491 permits for molecular work, 506 photoeclectors, 490, 491 pitfall traps, 305, 490, 491, 492–494, 495 sticky traps, 490, 493 suction samplers, 490, 492 sweep net, 490, 493, 495 taxonomical purposes, 495 Tullgren funnels, 490, 492 visual searching, 489–490, 494 Winkler extractors, 492, 495 Colombia, 78, 93, 167, 173, 184, 187, 188, 196, 203, 205, 206, 209, 211, 229, 230, 231, 234, 282 Color patterns, 3, 8, 285, 339, 375–376, 377–378, 381, 490, 494, 498. See also Taxonomic Index for specific taxa Common names, 1–4, 9–11 Communication, 381, 397–399, 408, 411–412 Community, 298–303 density of individuals, 302 energy flow, 301–302, 320 human impact, 12, 303–307 relative abundance, 298–301 resource partition, 302–303 species dominance, 299–300 species richness, 281–282, 298–301 Competition, 300–301, 303, 328–329 Conservation, 12, 303–307 Constraints ecological, 416, 447 phylogenetic, 296, 377–378, 440, 447–450 physiological, 412–413, 477

Contusive responses. See Retaliation Copulation, 11, 251, 410, 414, 419, 427, 443, 445, 451 cooperation, 425–426, 428 duration, 425–426, 429 forced, 425–426 grasping, 420–421, 423, 424, 425–427, 428, 438 multiple intromissions, 422–423, 429, 442 position, 418–419, 420–421, 424, 425–426, 430, 438, 443 rejection, 424, 425–426, 428, 430, 442 wrestling, 420, 426 Corona analis, 26, 95, 97, 102, 107, 121, 128, 137, 139, 141, 143, 146, 148, 152, 157 Cosmopolitan species, 282, 285–286, 300, 306, 336 Costa Rica, 3, 9, 80, 82, 126, 188, 203, 231, 245, 319 Costs of appendotomy, 380 of chemical defenses, 395, 396 of egg production, 445–446 of gregariouness, 409–410, 413 of maternal care, 445–447, 448–450 of paternal care, 450–452 of sexual reproduction, 415–416, 427, 439 of spermatophore production, 419 Courtship, 11, 26, 419, 425–427 copulatory, 419, 422–423, 427, 439, 442 precopulatory, 420–421, 426, 430, 438, 442 Coxal organs (= coxal glands), 37, 46, 49–52 coxal fluid, 51, 479 development, 51–52, 64 function, 49–51, 478, 479 Coxapophyses, 23–25, 28, 34. See also Taxonomic Index for specific taxa Crato Formation, 257, 264 Cretaceous, 250, 257 Croatia, 3 Crypsis, 19, 145, 264, 339, 371,

372, 374, 375–376, 381, 406, 449, 490, 494, 495. See also Camouflage Cryptic female choice, 426, 427, 428, 429, 439, 440, 442, 453. See also Sexual: selection Cuba, 179, 184, 206, 222, 231, 244 Cuticle, 18–21, 251, 283, 346, 371, 372, 474–475 Cuticular sculpture. See Integumentary ornamentations Czech Republic, 3, 250, 254, 287, 294, 304 Dalí, Salvador, 9–11 Debris, 8, 9, 19, 280, 285, 375, 418, 440, 441, 470, 522 Defensive glands. See Scent glands Defensive odor. See Chemical secretion Dehydration. See Water loss Deimatic behavior, 375, 381 Denmark, 2 Desert dwellers, 282, 292, 297, 306–307, 402, 477, 486, 488 Desiccation. See Water loss Development adult phase, 456–460, 471–472 anomalies, 465, 501 embryonic phase, 456–460, 461–465 larval phase, 456–460, 465 nymphal phase, 31, 456–460, 466–471 Devonian, 4, 40, 62, 248, 250–251, 263–265 Diapause, 464, 472, 478 Diaphanous teeth, 26, 139, 143, 150, 153, 157 Diet in captivity, 310, 311–315, 317, 322–323, 523 composition, 309–323 flexibility, 315–317 See also Food Digestion, 36–37, 39, 329. See also Food: ingestion and assimilation Digestive system, 35–43, 330, 463, 478 Discontinuous gas exchange, 477

589

590

Subject Index

Dispersal ability. See Vagility Dissection, 502–503, 514, 518 Distal tarsus (= distitarsus), 28, 30–31. See also Taxonomic Index for specific taxa Distribution. See Geographic distribution Diurnal activity, 324, 331–332, 333, 377, 384 DNA, 69, 273, 418, 496, 506–510 Dominican Republic, 260 Dorsal sclerites, 18, 21–22 scutum completum, 21, 22, 35, 99, 102, 104, 211, 500 scutum dissectum, 152, 153, 154 scutum laminatum, 22, 146, 147, 152, 153, 154, 500 scutum magnum, 22, 139, 143, 148, 157, 500 scutum parvum, 22, 128, 137, 141, 146, 147, 148, 151, 153, 154, 156, 500 See also Taxonomic Index for specific taxa Dorsal scute. See Carapace Drinking, 323, 475, 479 Earthworms, 310, 311, 312, 313, 314, 319, 334, 337, 439, 523. See also OLIGOCHAETA* Ecdysis. See Molting Ecdysone, 49 Eclosion, 11, 296, 430, 455, 461, 462, 464, 465, 523 Ectoparasites, 340, 347–348, 371 Ecuador, 167, 183, 187, 188, 203, 205, 206, 211, 230, 231 Edaphic conditions, 286 Effeminate males, 127, 277–278 Egg, 11–12, 296–298, 398, 425, 427, 428, 439, 450–452, 462–463, 464, 481, 522–523, 523–524 covering, 418, 430, 433, 434, 435, 436, 440, 441, 448–449, 522–523 diapause, 464, 472 guarding (see Parental care) hiding, 318, 372, 418, 424, 429–430, 431, 432, 433, 434, 435, 436, 437, 448–449 laying (see Oviposition)

morphology, 462–463 mortality by fungi, 348, 349, 430, 446, 447 number (see Fecundity) parasitism, 346, 371–372 predation, 322, 331, 350, 359, 361, 362, 363, 364, 367, 411, 439, 446–450, 451 production, 331, 414, 415, 416, 440, 445–446 size, 456–460, 462–463 tooth, 465 Ejaculates, 415–416, 439 El Mamey Formation, 261 El Salvador, 234 Embryo, 41, 273, 372, 462, 463, 465, 511, 524 Embryology. See Development Endangered species, 12, 306–307 Endemism, 8, 78, 87, 188, 203. See also Stenotopic species Endocuticle, 18, 474 Endoparasites, 340–341, 346–347, 370–371 Endosternite, 28, 33–35, 50, 64 Endozoism, 339, 367, 370, 372 England, 1, 4, 256, 267, 286, 288, 289, 290, 291, 292, 293, 300, 302, 303 Enteric fluid, 388, 390, 392–393, 394, 395, 396, 397, 478 Eocene, 48, 249, 250, 259, 261, 263, 264 Epicuticle, 49, 474–475 Epistome, 23, 24, 26, 34, 36, 154 Epizoism, 339, 367, 368, 369, 370, 372 Equatorial Guinea, 93, 98, 306 Esophagus, 34, 36, 46, 52, 53, 54 Ethogram, 331 Europe, 1, 6, 8, 14, 78, 81, 83, 84, 85, 103, 109, 111, 112, 126, 130, 133, 147, 151, 156, 159, 175, 220, 238, 254, 264, 274, 281, 282, 283, 298, 315, 368, 376, 403, 404, 420, 422, 423, 431, 432, 433, 436, 437 Eurychrone species, 286–298, 455 Eurypterids, 64, 253. See also EURYPTERIDA* Eurytopic species. See Cosmopolitan species Evasive responses, 374–375, 448–449

Evolution of gregariousness, 411–413 of maternal care, 447–450 of paternal care, 450–452 Excretion, 39, 478–479, 480 Exocrine glands, 93, 95, 96, 97, 98, 101, 107. See also Scent glands Exocuticle, 18, 184, 474 Exudate. See Chemical secretion Exuvium, 462, 470–471, 520 Eye mound. See Ocularium Eyes, 18, 22, 55–58 image formation (see Vision) light detection (see Photoreception) retina, 55–58, 383 retinula, 56–58 rhabdom, 56–58 simplification, 22, 58, 139, 173, 218–219, 283, 284 structure, 56–58 tapetum, 55–56, 69 See also Taxonomic Index for specific taxa Feces, 329, 330, 340, 341, 346, 348, 370, 517–518 Fecundity, 300, 418, 431–437, 447 Femoral formula, 501–502 Fertilization, 11, 414, 418, 419, 425, 426, 427, 450 Fertilizers, 304 Fights, 321–322, 333, 420–421, 422, 428–429, 430, 439, 442, 443, 445, 451 Finland, 2 Fire, 12, 305 Fixation and preservation, 496 Fleeing, 375, 380–381, 406, 413, 449, 452 Flies, 272, 313, 317, 324, 327, 328, 347–348, 365, 372. See also DIPTERA* Flooding, 251, 296 Florissant Formation, 247, 249, 258, 262–263, 265 Fluorescence, 16, 20, 490 Folklore, 3–4, 10–11 Food detection, 323–327 detoxification, 330 ingestion and assimilation, 23, 329–330 preferences, 9, 309–310, 315–317, 320–321

Subject Index

robbing and stealing, 328–329, 333–336 sharing, 329, 333–334, 336 transport, 328–329 Food-web, 337 Foraging, 331–333, 486 Foregut, 35–36, 329 Forested habitats, 254, 262, 263, 281–282, 297, 299–300, 304 Forestry, 12, 304 Forests, 8, 296, 305, 307, 447, 495 Fossil record, 4, 64, 247, 248–249, 250, 363–365 France, 2, 10, 14, 89, 134, 135, 147, 156, 180, 248, 250, 253, 255, 256, 257, 263, 267, 268, 269 Free tergites, 21–22, 500. See also Opisthosoma; see also Taxonomic Index for specific taxa French Guyana, 173, 183, 188, 211 Frogs, 9, 272, 314, 319, 350, 365, 396. See also ANURA* Frugivory, 320–321 Fungivory, 320–321 Fungus, 312, 314, 320–321, 348, 349, 367, 368, 370, 371, 397, 517, 518, 521, 522, 523. See also Egg: mortality by fungi Gabon, 93, 98 Gametes, 276–277, 415–416, 418, 419, 426–427, 450, 453 Gardens, 222, 282, 300, 301, 306 Gastropods, 310, 311, 312, 313, 314, 317–318, 322, 329–330, 332, 372, 439. See also GASTROPODA* Genital operculum, 18, 19, 24, 25, 34, 60–61, 255, 425–426, 471. See also Taxonomic Index for specific taxa Genitalia clearing techniques, 503–504 morphology, 59–61, 70, 73 observation and illustration, 504–505 preparation techniques, 502–505

staining techniques, 504 See also Taxonomic Index for specific taxa Geographic distribution, 5, 8, 77–86, 280–281, 282–283, 286, 300, 306 disjunct, 78, 80, 81, 117, 118, 151, 156, 209, 220, 245, 282 opiliofaunal relationships, 86 relictual, 81, 193 See also Taxonomic Index for specific taxa Geographic variation in chromosome number, 273–277 in morphology, 282–283 in phenology, 297–298 Germany, 2, 3, 147, 248, 249, 250, 255, 257, 258, 261, 263, 267, 268, 269, 274, 288, 289, 290, 291, 292, 293, 294, 300, 302, 304, 305, 306 Glandular setae (= glandular hairs), 19, 115–117, 137, 139, 142, 143, 147, 150, 154, 214, 328 Glycerol, 481, 503–504 Glycogen, 36, 37, 39, 40, 49, 478 Gonads, 59–60 Gondwana, 86, 118, 264 temperate, 79, 80, 81, 84, 85, 86, 94, 101 tropical, 79, 81, 82, 84, 85, 86 Gonopore. See Genital operculum Gonostome, 24, 99, 108 Gonyleptidine. See Benzoquinones González-Sponga, Manuel, 5, 7 Goodnight, Marie Louise and Clarence, 5, 7 Grasslands, 282, 287, 288, 289, 290, 291, 292, 293, 294, 297, 305, 307 Great Britain, 1, 2, 3 Gregarines, 9, 247, 339, 340–341, 342–343, 346, 371, 517–518 Gregariousness. See Aggregation Grooming, 26, 247, 325, 329, 333, 346, 370, 452 Ground dwellers, 15, 19, 22, 23, 31, 56, 58, 130, 132, 167, 175, 208, 264, 280, 283–284, 286, 302,

315–317, 368, 372, 376, 491–492, 493, 495, 521 Group living. See Aggregation Growth, 282–283, 466–471 Guanine, 49, 479 Guano, 314 Guatemala, 80, 82, 85, 203, 234 Gulf of Guinea, 80, 82, 97, 98 Guyana, 93, 173, 188, 211, 349 Habitat, 8, 12, 280, 297, 299–300, 370–372, 490, 492–494 fragmentation, 304, 306 use, 8, 280–286, 297, 303, 315–317, 375, 483–484, 521 See also Microhabitat Hansen’s organ, 95, 97, 98 Harem. See Mating strategies Hatching. See Eclosion Heart, 37, 46–47, 48, 49, 50, 461, 463, 479 aorta, 45, 46–47, 53, 56 epicardium, 46–47 muscles, 46–47 myocardium, 46–47 ostia, 46 Hemocoel, 35, 36, 48, 387, 479 Hemocyanin, 45, 480 Hemocytes, 47–48 adipohemocytes, 47 coagulocytes, 47–48 granulocytes, 47–48 plasmatocytes, 47 prohemocytes, 47 spherulocytes, 47–48 Hemocytopoietic organs, 48, 54 Hemolymph, 8, 45, 47–48, 49–50, 478–479, 480–481, 488 Hibernation, 283, 296, 464, 471 Himalayas, 5, 151, 156, 214, 282, 287, 292, 293, 297, 298 Hindgut, 36, 43 Historical account on chemical defenses, 382–383 on development, 461 Historical systematic synopsis of cyphophthalmi, 89, 92–94 of dyspnoi, 131–135 of eupnoi, 108–113 of laniatores, 159–168 Holarctic region, 79, 81, 118, 133, 151, 156, 306 Holotype, 498, 500–501 Hood, 22, 132, 142, 143, 145, 148, 157, 159, 466

591

592

Subject Index

Horseshoe crabs, 25, 28, 39, 58 Host site selection, 347 Humidity, 8, 282, 285–286, 297, 300, 331–332, 370, 402, 405, 412–413, 430, 446, 463, 464, 473, 474–475, 480–481, 482–483, 484, 486, 487–488, 522–523, 524 Hungary, 2 Hunting. See Foraging Hydrostatic pressure (= hydraulic pressure), 30, 59, 60, 213, 214, 387, 427 Hygroreception, 482–483 Iberian Peninsula, 81, 134, 147, 156 Immature. See Nymphs India, 79, 82, 83, 84, 85, 86, 106, 162, 173, 175, 176, 179, 222, 268, 399 Indo-Malayan region, 78, 79, 80, 81, 83, 106, 245 Indonesia, 78, 85, 86, 176, 191, 226, 245 Insecticides, 304 Insects, 40, 45, 47, 49, 261, 262, 263, 265, 272, 281, 309, 310, 313, 314, 315, 317, 321, 322, 324, 336, 337, 340, 347, 348, 365, 367, 368, 372, 378, 381, 398, 400, 402, 405, 409, 410, 411, 413, 429, 439, 448, 474, 475, 486, 511, 519, 520, 523. See also Taxonomic Index for specific taxa Insemination. See Fertilization Instars. See Development Integument, 18–21, 375–376, 387, 474–475, 498–499. See also Cuticle; see also Taxonomic Index for specific taxa Integumentary ornamentations, 18–20, 387, 389, 395, 498–499 apophyses, 18, 389, 390, 443, 497, 499 denticles, 18, 28, 381, 498–499 granules, 375, 392, 498–499 setae, 18, 19, 20, 28, 31, 60, 73, 251, 262, 466, 470, 498–499, 502

spines, 18, 20, 22, 28, 45, 60, 111, 255, 260, 262, 327, 371, 382, 443, 448–449, 477, 498–499, 502 teeth, 26, 31, 94, 498 tubercles, 18, 31, 111, 388, 392, 498–499 See also Taxonomic Index for specific taxa Intertidal zone, 285 Intraspecific variation, 12, 271, 273–277, 282–283, 297, 315–317, 427–428, 499, 501 Introduced species, 80, 81, 125, 151, 159, 222, 306, 336 Invertebrates, 9, 50, 54, 304, 307, 309, 315, 337, 359–364, 449, 478, 492, 493. See also Taxonomic Index for specific taxa Iraq, 81, 144 Isopods, 310, 311, 312, 313, 314, 409, 523. See also ISOPODA* Italy, 156, 189, 249, 263 Iteroparity, 431–437, 445–447, 451 Jamaica, 231 Japan, 3, 9, 78, 79, 80, 81, 83, 84, 85, 93, 103, 117, 118, 133, 135, 140, 151, 153, 156, 191, 220, 222, 231, 238, 243, 267, 268, 269, 270, 272, 273, 274, 276, 278, 281, 284, 287, 288, 290, 291, 292, 294, 296, 319, 346, 382, 428, 432, 437 Java, 79, 106, 214 Jurassic, 94, 250, 257 Juveniles. See Nymphs Karyotype, 271, 272, 273, 274–277, 278 Kenya, 82, 93, 175 Ketones, 384–385, 395–396, 408, 448–449 Keys to families and subfamilies of Eupnoi, 113–114 to families of Cyphophthalmi, 94–95 to families of Laniatores, 168–171 to main groups of Dyspnoi, 135–136

to subfamilies of Agoristenidae, 173 to subfamilies of Biantidae, 177, 179 to subfamilies of Cranaidae, 187–188 to subfamilies of Epedanidae, 189, 191 to subfamilies of Gonyleptidae, 201–203 to subfamilies of Nemastomatidae, 150 to subfamilies of Stygnidae, 227 to subfamilies of Triaenonychidae, 242–243 to suborders of Opiliones, 89 Kin recognition, 402, 405 Kleptoparasitism, 336 Korea, 2, 81, 83, 133, 153, 156, 243 Labium, 23–25, 34, 115, 137, 139, 141, 146, 152 Lamina suprachelicerales, 34, 143, 145, 148, 153, 154, 157 Larva arachnid, 455, 456–460, 461, 462, 465 insect, 311, 312, 313, 314, 315, 317, 321, 326, 327, 330, 336–337, 340, 363, 368, 372, 430, 519, 523 Laurasia, 79, 86, 87, 103 Lawrence, Reginald Frederick, 5, 7 Leaf litter dwellers, 8, 58, 82, 280, 283, 284, 285, 286, 302, 375, 377, 417, 483, 494, 495 Lebanon, 250, 257 Leg dabbing, 393, 395 Leg threading. See Grooming Legs, 1–3, 9, 18, 28–33 morphology, 28–31 muscles, 34–35 sensorial, 4, 9, 21, 32–33, 308, 324, 325, 329, 332, 335, 408, 411 sexual dimorphism, 442–443 solea, 95, 98, 102 walking, 32–33, 45, 283, 284, 327, 482–483 See also Taxonomic Index for specific taxa Lichens, 312, 314, 375, 376, 494

Subject Index

Life cycle, 296–298, 305, 455, 471–472 Lifespan, 377, 448–449, 455, 472 Light conditions, 58, 372, 405, 412–413, 483–487. See also Photoperiod Lipids, 36, 37, 39, 40, 320–321, 475, 478 Liverworts, 339, 370 Lizards, 319, 350, 377, 396. See also SQUAMATA* Locomotion, 31–33 Locomotor activity, 331–332, 333, 484–487. See also Activity pattern Longevity. See Lifespan Long-legged species, 1–3, 5, 9, 11, 15, 30, 31, 32, 252, 255, 257, 265, 284, 286, 304, 315, 327, 378–379, 380, 470, 495, 496 Macedonia, 3 Madagascar, 79, 82, 85, 86, 94, 101, 167, 175, 177, 179, 222, 226, 241, 243, 245 Malacophagy, 317–318, 328, 329–330, 332 Malaysia, 78, 106, 176, 191, 231 Malpighian tubules, 478 Mammals, 9, 43, 262, 265, 320, 350, 365, 396, 397, 429. See also Taxonomic Index for specific taxa Marking techniques, 522 Martens, Jochen, 5, 7, 66, 67, 71 Mate guarding, 11, 422–423, 424, 427–429, 445 Maternal care, 11–12, 331, 423, 434, 435, 436, 437, 440–442, 445–450, 451–452 Mating strategies, 11, 409–410, 415–416, 419, 422–423, 427–429, 439–445, 453 harem, 422, 440, 442, 443, 444 polyandry, 423, 442–443, 445, 450–452 polygyny, 416, 422, 427–429, 445 Mauritius Islands, 222, 245 Maxillary lobes, 23, 127, 232, 329 Mechanoreception, 20–21, 324, 426

Mediterranean region, 80, 81, 86, 133, 144, 159, 220 Meiosis, 271, 273, 275–277, 511 Melanesia, 85, 86, 222, 226 Mello-Leitão, Cândido Firmino de, 5, 7, 66, 78, 166 Mensuration, 500–501 Meristics, 501–502 Mesenteron. See Midgut Mesic environments, 282, 285–286, 297, 371, 473, 481 Mesozoic, 247, 248, 256–257, 258, 261 Metabolism, 37, 330, 332, 397, 409, 477, 479, 481, 486 Metatarsus (= basitarsus), 28–31. See also Taxonomic Index for specific taxa Mexican region, 84, 85 Mexico, 2, 3, 78, 80, 81, 83, 118, 128, 151, 183, 184, 226, 231, 233, 234, 402, 441 Microhabitat, 8, 283, 285, 315–317, 412–413, 493–494 Micronesia, 85, 222 Micropyle, 462 Microtrichia, 73, 96, 98, 100, 102, 106, 108, 115, 137, 139, 142, 147, 153, 154, 157, 498 Midgut, 36–43, 132, 167, 478 comparative morphology, 41–42 diverticula, 36–39 phylogenetic importance, 42–43 postventriculs, 40 ventricula, 36–39 Migration, 264, 317, 405, 410 Millipedes, 251, 311, 312, 409, 480. See also DIPLOPODA* Mimicry, 374, 377–378 Mineral spherites, 37, 39–40 Miocene, 135, 249, 260, 261, 264 Mites, 3, 15, 40, 52, 64, 109, 132, 250, 251, 254, 257, 263, 264, 271, 311, 312, 313, 318, 320, 321, 329, 339, 340, 341, 345, 347, 368, 369, 370, 371, 405, 439, 508, 519–520, 523. See also ACARI* Mitochondria, 37, 39, 40, 49, 58

Mitosis, 511 Mobility. See Vagility Moisture. See Humidity Molecular techniques, 506–510 DNA extraction, 507–508 GenBank, 509 phylogenetic analysis, 510 polymerase chain reaction (PCR), 508–509 RNAlater, 507 sequence databases, 509–510 sequencing, 509 tissue preservation, 507 tissue storage, 507 Molting, 39, 54–55, 321, 367, 455, 462, 465, 466–471, 474, 482 Molting chamber, 470 Mongolia, 126 Montane habitats, 282, 287, 288, 289, 290, 291, 292, 293, 294, 297 Moss dwellers, 8, 280, 285, 331, 376 Mountain, 147, 151, 188, 203, 275, 277, 306–307 Mouthparts, 4, 15, 323, 326, 329, 463, 478 Mucus, 317, 326, 330, 432, 433, 434, 436, 439, 462–463 Muscular system, 33–35 opisthosomal muscles, 35 prosomal muscles, 33–35 Myanmar, 83, 175, 176, 191, 257 Myriapods, 310, 311, 312, 313, 316. See also Taxonomic Index for specific taxa Naphthoquinones, 384, 396 Nearctic region, 78, 80, 81, 83, 180, 220, 221, 231, 234 Necrophagy. See Scavenging Nectar, 320, 340, 395 Nematodes, 340, 341, 346–347, 371, 518–519. See also NEMATODA* Neotropical region, 78, 79, 80, 81, 82, 83, 179, 231, 234, 245, 374, 461 Nepal, 80, 81, 85, 86, 156, 175, 176, 179, 191, 214 Nephrocytes, 48–49, 479 Nervous system, 34, 45, 52–55, 379–380 abdominal ganglia, 48, 54

593

594

Subject Index

Nervous system (continued) central nervous system, 34, 36, 45, 52–55, 380 cheliceral ganglion (= deutocerebrum), 52, 53, 54 esophageal ganglia, 53, 54 neurohemal organs, 54–55 neuropils (= synaptic centers), 53–54 neurosecretions, 53, 54–55 pacemaker neurons, 54, 380 paraganglionic plates, 53, 55 peripheral nervous system, 54 protocerebrum, 52–54 subesophageal ganglion, 49, 52–55 supraesophageal ganglion, 34, 52–55, 56 supraesophageal neurosecretory system, 55 Netherlands, 1, 2, 147, 290, 293 New Caledonia, 79, 80, 82, 85, 86, 93, 94, 108 New Zealand, 78, 79, 80, 81, 85, 86, 99, 101, 118, 119, 120, 125, 166, 235, 236, 241, 243, 306, 315, 322, 336, 423, 437 Nipping, 376, 381–382, 449 Nocturnal activity, 302, 331–332, 333, 371, 372, 377, 380, 411, 484–487, 495 North America, 1, 6, 79, 103, 111, 112, 117, 118, 125, 130, 134, 135, 137, 140, 141, 142, 148, 151, 156, 159, 254, 264, 274, 281, 312, 313, 314, 315, 403, 404, 420, 422, 423, 431, 432, 434, 437 Norway, 2, 3, 289, 292 Nuptial gift, 11, 426, 430, 438 Nymphs, 58, 285, 296–298, 328, 330, 331, 375, 402, 452, 455–460, 462, 466–471, 486–487, 523–524 Oceania, 6, 78, 83 Ocelli. See Eyes Ocularium, 22, 34, 466, 500. See also Taxonomic Index for specific taxa Odoriferous glands. See Scent glands Oenocytes, 47, 49 Oligocene, 249, 250, 262, 263

Ontogeny. See Development Open habitats, 281–282, 285–286, 297, 299–300, 305, 346, 483 Opisthosoma, 4, 18, 21–22, 25–26, 34–35, 500. See also Taxonomic Index for specific taxa Osmoregulation, 474–475, 477, 478, 479, 480–481 Ovaries, 59, 323, 511, 512, 514 Overwintering, 8, 39, 296, 297, 401, 405, 409, 410, 478, 486 Oviduct, 59, 425 Oviposition, 76, 318, 414, 424, 439, 440, 445, 446, 452 choice of sites, 418, 427, 428–430, 431–437, 439, 442, 445–446, 450–451 frequency, 418, 431–437, 445–446, 447 Ovipositor, 34, 59–61, 70, 72, 73, 76, 251–252, 418, 419, 424–425, 427, 428, 429–430, 438, 439–440, 448–450, 480, 502–503. See also Taxonomic Index for specific taxa Ozophore, 22–23, 34, 56, 95, 97, 99, 102, 104, 105, 107, 121, 387 Ozopore, 18, 22–23, 382, 387–388, 389 Palaearctic region, 78, 80, 81, 83, 84, 85, 132, 144, 151, 159, 180, 220, 221, 231 Paleozoic, 64, 248, 250–256, 257, 264, 265 Pampa de Achala, 296, 331, 334, 441 Panama, 188, 211, 231, 442, 444 Pantanal, 203 Papua New Guinea, 80, 85, 106, 175, 176, 214, 222, 223, 244, 245 Páramos, 188, 282 Paraná region, 82 Parasites, 9, 40, 274, 339, 340–348, 367, 368, 370–371 preservation techniques, 516–520 Parasitoids, 340–348, 371–372 preservation techniques, 519

Parental care, 11–12, 322, 414–416, 418, 422–423, 431–437, 440–452 Parthenogenesis, 11, 60, 117, 272, 415, 425 Paternal care, 11–12, 415–416, 423, 433, 434, 435, 436, 437, 442–445, 447, 450–452 Pathogens, 9, 40, 339, 346, 348–349, 370–372 preservation techniques, 516–517 Pedipalps, 17–19, 26–27, 499, 501, 502 claw, 27, 28, 72, 263, 325, 327–328, 382, 401, 501 function, 310, 315, 323–325, 326, 327–328, 331, 381–382, 401–402, 419, 420–421, 424, 425–426, 438, 443, 444, 448–449, 482–483 morphology, 28, 29 sexual dimorphism, 425 See also Taxonomic Index for specific taxa Penis, 16, 19, 59–60, 73, 74, 75, 76, 111, 251–252, 419, 424, 425, 427, 429, 438, 440, 443, 471, 480, 502–503 calyx, 230 capsula externa, 225, 244 capsula interna, 225 conductors, 178, 230 dorsal process, 186 follis, 230 glans, 60, 137, 146, 175, 184, 186, 199, 212, 233 lamina ventralis, 245 pars basalis, 230 pars distalis, 225, 230 pergula, 244, 245 rutrum, 244, 245 shaft, 130 stragulum (see Penis: capsula externa) stylus, 137, 244 titillators, 117, 178, 204 truncus, 244 ventral plate, 186, 244 See also Spermatopositor; see also Taxonomic Index for specific taxa Peritrophic membrane, 37, 40, 478

Subject Index

Permian, 250, 255, 256 Peru, 173, 183, 187, 188, 203, 211, 231 Pest control. See Biological control Pesticides, 12, 304 Pharynx, 23–25, 34, 35–36, 49 Phenology, 8, 286–298, 302, 303 Phenols, 385, 386, 395, 408, 448–449 Pheromones, 49, 383, 397–399, 411–412 Philippines, 85, 106, 191, 214, 223, 245, 444 Phoresy, 367–370 Photoperiod, 484–486 Photophobia, 378, 381, 492, 521 Photoreception, 56–58, 326, 426, 483 Phototaxis, 483 Phylogeny, 42–43, 78, 93, 94, 118, 126, 133, 145, 151, 153, 235, 237, 383, 418, 419, 448, 449, 506 relationship between arachnid orders, 62–65 relationship between Opiliones suborders, 66–77 See also Cladistics Pinching. See Nipping Pitfall traps. See Collection Poland, 2, 147, 249 Pollution, 12, 304–305, 306 Polyandry. See Mating strategies Polygyny. See Mating strategies Polynesia, 84, 85, 226 Polyphagy, 9, 309–310, 311–315 Population size, 494 Portugal, 147 Predation intraspecific (see Cannibalism) risk, 415, 427, 439, 445, 447, 451, 474 Predators, 9, 305, 339, 350–367, 371, 374–375, 377, 378, 379, 380, 381, 396–397, 408–409, 447, 449 Preoral chamber. See Stomothecha Preservation and fixation, 491, 492–493, 495, 496, 507, 516–520 Prey capture, 327–328 detection, 323–327 selection, 310, 315–317 Primary defenses, 347–375

Proctodeum. See Hindgut Proprioception, 21, 380 Prosoma, 4, 18, 21, 22–25, 33–35. See also Taxonomic Index for specific taxa Pseudoarticulation (= pseudoarticular nodules), 121, 123, 127, 129, 130, 150, 153, 154, 466, 501–502 Pseudonychium, 31, 175, 234, 469 Pseudoscorpions, 4, 21, 30, 257, 259, 264, 305, 367–368, 400. See also PSEUDOSCORPIONES* Puerto Rico, 206, 231, 350 Pyrenees, 147, 156, 270, 493 Quaternary, 249, 263 Quinones, 377, 448–449. See also Benzoquinones; Naphthoquinones Rambla’s organ, 105, 106 Rapoport effect, 282 Rearing methods, 520–524 Regeneration, 31, 379 Relative humidity. See Humidity Reproduction asexual (see Parthenogenesis) seasonality, 259, 296, 410, 427–429, 464 sexual, 11, 414, 415, 425 Repugnatorial glands. See Scent glands Respiratory system, 18, 25, 43–46, 475–477 Retaliation, 374–375, 381–382, 448–449 Rhynie chert, 248, 250–252, 253, 254, 265 RNA, 64, 68, 69, 72, 507 Rocks, 8, 254, 280, 285, 307, 331, 403, 404, 405, 407, 424, 428–429, 431, 432, 433, 434, 435, 436, 437, 439, 440, 441, 462, 494, 495, 521 Rocky habitats, 282, 289, 290, 291, 293, 294, 295, 297 Roewer, Karl Friederich, 5, 6, 7, 74, 78, 161, 165 Romania, 180, 250, 263 Rotting logs, 403, 404, 405, 407, 437 Russia, 3, 153, 267, 268, 269, 274

Salamanders, 419. See also CAUDATA* Salivary glands, 24–25, 51 Salivation, 51 Sandhills, 286 Savanna, 219 Scanning electron microscopy (SEM), 18, 40, 46, 56–57, 496, 505, 518 Scavenging, 309, 318–320, 327, 332, 337, 416 Scent glands, 3, 9–10, 382–383 external morphology, 387–388, 389 (see also Ozopore) internal morphology, 383, 386–387 Scent-gland secretion. See Chemical secretion Scopula, 99, 101, 178–179, 189, 198, 209, 224–225, 226, 229 Scorpions, 4, 20, 23, 25, 26, 30, 36, 46, 48, 58, 64, 250, 253, 257, 264, 266, 285, 286, 299, 300, 302, 315, 317, 322, 327, 329, 330, 371, 400, 411, 473, 474, 475, 480, 500. See also SCORPIONES* Scotland, 248, 250, 252, 253, 288, 289, 290, 291, 292, 293, 297, 300, 302, 305, 336, 493 Seasonality, 8, 259, 273, 282–283, 286–298, 302–303, 405, 429, 475, 478, 486 Seasons autumn, 296, 346, 428 spring, 8, 39, 275, 296, 302, 464 summer, 8, 39, 296, 302, 303, 331, 348, 464, 486 winter, 283, 296, 303, 304, 405, 429, 464, 472, 478, 486 Secondary defenses, 374–375 Semelparity, 434–436, 446–447 Seminal receptacles (= receptacula seminis), 60, 117, 119, 120, 123, 127, 142, 143, 144, 147, 153, 418, 425, 427, 440, 503 Sensilla chaetica, 19, 20, 326 Sensilla trichodea, 19, 20, 324 Sensorial legs. See Legs: sensorial

595

596

Subject Index

Sensory cones, 72–73, 117, 154, 156 pegs, 196, 389, 392–393 setae (= hairs), 20, 70, 98, 324, 328 Serbia and Montenegro, 3, 180 Serotonin, 484–486 Serpentine rocks, 307 Sex ratio, 402, 427–428 Sexual cannibalism, 321–322, 416 dimorphism, 11, 425, 430, 439, 440, 442–445, 498 (see also Taxonomic Index for specific taxa) pheromone, 398 selection, 11–12, 426, 427, 429, 440, 442, 450–452, 453 Seychelles, 82, 84, 85, 86, 176, 222, 226, 245 Shell, 318, 329–330, 372, 433, 439 breakers, 330 intruders, 330 Shelters, 283, 328–329, 331, 377, 405, 406, 482, 495 Short-legged species, 3, 31, 132, 283, 284, 286, 304, 521 Sierra Leone, 97, 296 Silurian, 250, 264 Simon, Eugène, 5 Singapore, 106, 306 Slit sensilla, 19, 20–21, 120, 123, 127 Slovakia, 2 Slovenia, 2, 3, 147, 238 Snails and slugs, 3, 9, 286, 300, 311, 312, 313, 317–318, 326, 327, 329–330, 433, 523. See also GASTROPODA* Snow, 282–283, 405 Soares, Hélia Eller Monteiro, 5, 7 Soil dwellers. See Ground dwellers Solifuges, 4, 30, 36, 109, 123, 257, 315, 324, 328, 371, 400, 450. See also SOLIFUGAE* Solomon Islands, 452 Sørensen, William, 5, 7 Sound production. See Stridulation South Africa, 1, 2, 80, 82, 84, 85, 86, 94, 99, 101, 111, 118, 122, 123, 125, 161, 175, 241, 306 South America, 3, 5, 6, 12, 78, 79,

80, 82, 84, 85, 86, 93, 97, 118, 130, 161, 162, 167, 179, 184, 188, 203, 229, 281, 315, 404, 420, 421, 422, 423, 434, 435, 436, 437 Spain, 1, 2, 3, 81, 287, 288, 290, 291, 293, 306, 493 Sperm, 276, 417–418 aflagellate, 418, 419, 425, 439 balls (see Spermatophore) competition, 418, 427–428, 429, 440, 442, 445 displacement, 440, 445 duct, 59, 60, 153 precedence, 428–429 transfer, 11, 416–417, 418, 419, 425 Spermathecae. See Seminal receptacles Spermatids, 417–418 Spermatogenesis, 266, 417–418, 511 Spermatophore, 11, 63, 70, 416–419 Spermatopositor, 59, 60, 70, 416–419. See also Penis; see also Taxonomic Index for specific taxa Spherites, 37, 39–40, 478 Spiders, 3, 4, 9, 18, 20, 21, 28, 30, 40, 46, 48, 51, 52, 54, 249, 250, 254, 256, 257, 259, 261, 262, 263, 264, 266, 271, 272, 274, 278, 285, 302, 304, 305, 311, 312, 313, 314, 315, 317, 320, 322, 324, 327, 330, 331, 335, 336, 337, 340, 346, 350, 364, 365, 371, 372, 375, 378, 379, 380, 396, 400, 402, 411, 473, 474, 475, 477, 479, 480, 523. See also ARANEAE* Spiracles, 4, 25, 43–45, 64, 476, 477 Spores, 339, 367, 368–370 Spurs, 112, 115, 120, 121, 124, 125, 127, 180, 219, 220, 227, 420, 425 Sri Lanka, 69, 79, 83, 85, 94, 101, 176, 222, 306 Starvation, 320, 330, 331–332, 523 Stenochrone species, 286–298, 445

Stenotopic species, 283–285. See also Endemism Sternal glands, 69, 70, 93, 95, 96, 107, 108 Stigmata. See Spiracles Stomotheca, 23–25, 34, 64, 329 Stridulation, 18–19, 381 Stridulatory structures, 18–19, 137, 149, 198, 204, 245, 381, 430 Subsocial behavior. See Parental care Sulawesi, 79, 106 Sumatra, 79, 81, 106 Sundaland, 79, 80, 81, 82, 84, 85 Supercooling, 481, 488 Surface/volume relationship, 8, 42–43, 409, 474 Surinam, 173 Survivorship, 285–286, 308, 317, 330, 405, 430, 445, 446, 449, 453, 481, 482–483, 522–523 Suzuki, Seisho, 5, 7 Sweden, 2 Switzerland, 3 Synanthropic species, 125, 305–306 Tarsal claw, 29, 31, 111, 167, 468–470 formula, 132, 501–502 process, 29, 31, 166, 469–470 segments (= tarsomeres), 31, 283, 284, 466, 501 See also Taxonomic Index for specific taxa Tasmania, 80, 85, 86, 118, 120, 243 Tegument. See Integument Temperate region, 5, 8, 17, 74, 80, 103, 111, 126, 135, 243, 270, 280, 281, 282, 337, 405, 464, 473, 478, 522 Temperature and balance, 481 and development, 464, 471 and mortality, 428, 475, 522 and preference, 285–286, 483 and rearing, 522–523 Teratology. See Development: anomalies Termites, 321, 332, 398 Terpenoids, 395

Subject Index

Terrarium, 521–522. See also Rearing methods Territorial behavior, 11, 380, 398, 420, 428–429, 442–443, 450–451 Tertiary, 118, 258, 261, 263 Testis, 59–60, 418, 511, 512 Thailand, 70, 80, 81, 84, 85, 93, 104, 106, 135, 151, 191, 214 Thanatosis, 9, 374, 375, 376, 378 Thermoreception, 483 Thorell, Tord Tamerlan Theodor, 5 Threatened species. See Endangered species Tibial spiracles, 31, 44, 45–46 Ticks, 3, 40, 250, 257, 371, 475, 479. See also ACARI* Toads, 9, 350, 365, 366. See also ANURA* Topological terms, 497, 499–500 Tracheae, 43–46, 56, 251–252, 475–477 Tracheal system. See Respiratory system Trail marking pheromone, 326, 331, 397–398 Trichobothria, 20, 324 Trinidad and Tobago, 95, 167, 211, 229, 231, 364, 441 Troglobites, 139, 146, 147, 148, 180, 193, 208, 219, 231, 238, 239, 283, 306, 326, 484. See also Cave dwellers Troglophiles, 283, 284, 331 Trogloxens, 283–284, 331, 332–333, 380, 405, 445–446, 482, 486–487 Tropical region, 3, 5, 8, 12, 93, 97, 106, 135, 281, 282, 296, 337, 473, 478

Tundra, 282 Turkey, 3, 81 Ukraine, 2 Ultraviolet light, 16, 20, 326, 483, 490, 495 United States (USA), 2, 4, 11, 80, 81, 82, 83, 84, 85, 109, 117, 118, 119, 128, 140, 156, 180, 184, 216, 231, 234, 238, 243, 248, 249, 250, 253, 255, 258, 262, 263, 267, 268, 269, 270, 282, 283, 285, 286, 287, 288, 289, 292, 304, 305, 306–307, 319, 334, 347, 368, 410, 428 Urban habitats, 305–306 Uruguay, 118, 294 Vagility, 77–78, 274, 278, 415 Vegetation, 58, 280–281, 283–286, 304–305, 315–317, 490–491, 493–494 Venezuela, 5, 80, 95, 96, 118, 167, 173, 184, 187, 188, 204, 205, 206, 209, 211, 226, 230, 231, 244 Venom, 4, 327, 416 Vertebrates, 9, 254, 281, 310, 311, 312, 313, 320, 351–358, 396, 400, 408, 449, 452. See also Taxonomic Index for specific taxa Vertical distribution, 184, 282, 297–298 Vietnam, 85, 191, 214 Virgin Islands, 231, 350 Virus, 348, 516 Vision, 324, 326

Wales, 2, 3, 156, 288, 289, 290, 291, 292, 293 Walking legs. See Legs: walking Wallacea, 79, 80, 81, 82, 84, 85 Wasps, 309, 312, 313, 314, 320, 340, 348, 371, 372, 378, 399. See also HYMENOPTERA* Water loss, 8, 285–286, 300, 409, 413, 430, 439, 440, 447, 474, 480–481, 482–483, 484, 486, 487–488 digestive, 478 excretory, 478–479 integumentary, 474–475 respiratory, 475–477 Wax layer, 184, 199, 474–475, 481 Web, 4, 336, 364, 365, 378 Whip scorpions, 20, 25, 28, 46, 254, 257. See also UROPYGI* Whip spiders, 46, 109, 254, 257, 324, 328, 379, 400, 475. See also AMBLYPYGI* Woodlands, 282, 285–286, 287, 288, 289, 290, 291, 292, 293, 294, 295, 297, 300, 302–303, 304, 305, 307, 493 Woodlice. See Isopods Xeric environments, 125–126, 203, 282, 405, 409, 441, 475 Yolk, 11, 36, 37, 41, 414, 511 Yugoslavia, 368 Zeitgebers, 483, 486 Zoogeographic realms, 78

597