The Sipuncula Their Systematics, Biology, and Evolution Edward B. Cutler The Sipuncula Their Systematics, Biology, and Evolution EDWARD B. CUTLER Department of Biology Utica College of Syracuse University Comstock Publishing Associates a division of Cornell University Press Ithaca and London Copyright © 1994 by Cornell University All rights reserved. Except for brief quotations in a review, this book, or parts thereof, must not be reproduced in any form without permission in writing from the publisher. For information, address Cornell University Press, Sage House, 512 East State Street, Ithaca, New York 14850. First published 1994 by Cornell University Press. Printed in the United States of America © The paper in this book meets the minimum requirements of the American National Standard for Information Sciences—Permanence of Paper for Printed Library Materials, ANSI Z39.48-1984. Library of Congresss Cataloging-in-Publication Data Cutler, Edward Bayler. The Sipuncula : their systematics, biology, and evolution / Edward B. Cutler, p. cm. Includes bibliographical references (p. ) and indexes. ISBN 0-8014-2843-2 1. Sipuncula. I. Title. QL391.S5C87 1994 595-1'7—dc20 94-15505 This book is dedicated to Anthony Cordell, William Fales, Walter Nickel, and Arthur Sinclair—teachers, naturalists, and mentors who responded to my curiosity during my formative years by introducing me to the wonder of the natural world—and to the memory of my parents, Gladys Bayler and Edward Malcolm, whose love and support allowed me to be who I am. Contents Preface xiii Checklist of the Sipunculan Species xv Introduction I Historical Notes i OverView of Biology and Morphology 3 Obtaining and Handling Sipunculans 5 Collecting 5 Relaxing and Preserving 7 Dissecting 8 Naming 9 Glossary 9 Part I Systematics 1 Higher Taxa and User's Guide 17 Morphological Characters of Higher Taxa 17 Key to Classes and Families 21 An Alternate Way to Determine Sipunculan Genera 23 2 The Sipunculids 24 Genus Sipunculus 28 Genus Xenosiphon 41 Genus Siphonosoma 44 Genus Siphonomecus 55 Genus Phascolopsis 57 3 The Golfingiids 60 Genus Golfingia 61 Genus Nephasoma 77 Genus Thysanocardia 102 Vlll Contents 4 The Phascolionids 107 Genus Phascolion 108 Genus Onchnesoma 133 5 The Themistids 140 Genus Themiste 140 6 The Phascolosomatids 156 Genus Phascolosoma 159 Genus Antillesoma 186 Genus Apionsoma 189 7 The Aspidosiphonids 199 Genus Aspidosiphon 200 Genus Lithacrosiphon 227 Genus Cloeosiphon 230 Part II Sipunculan Biology: A Review 8 Ecology 236 Habitat 236 Sensitivity to Environmental Change 239 Behavior 239 Trophic Dynamics 241 Obtaining Energy 241 Sipunculans as Sources of Energy 243 Symbiotic Relationships 244 Mutualism 244 Commensalism 246 Parasitism 247 9 Integument and Muscle Systems 249 Integument 249 Fine Structure 249 Dermal Layers 251 Muscles 252 Anatomy 252 Physiology and Biochemistry 254 10 Coelomic Cells and Immune System 256 Coelomic Cells 256 Erythrocytes 257 Respiratory Pigments 258 Contents Urn Cell Complex 265 Immune System 268 Encapsulation and Inactivation 268 Antibacterial and Cytotoxic Activity 269 11 Respiration, Genetics, and Biochemistry 271 Respiration 271 Gas Exchange 271 Anaerobic Metabolism 272 Genetics 273 Chromatin 273 Genetic Variability 274 Miscellaneous Biochemical Attributes 275 Chemical Composition 275 Guanidine Compounds 275 Arginine Kinase 275 12 Excretory System 276 Anatomy 276 Physiology 279 Nitrogen Excretion 279 Osmotic, Ionic, and Volume Regulation 279 13 Digestive System 282 Anatomy 282 Physiology 283 14 Nervous System 286 Central Nervous System 286 Structure 286 Nerve Transmission 288 Sense Organs 288 Chemoreception 289 Photoreception 290 Gravity Reception 290 Neurosecretion 291 Keferstein Bodies 292 Fusiform Bodies 293 15 Reproduction and Regeneration 297 Sexual Reproductive System and Modes 297 Gonads and Gender 297 Gametes 298 Reproductive Cycles and Spawning 300 X Contents Gametogenesis and Fertilization 301 Cleavage and Gastrulation 301 Larval Development 304 Larval Dispersal and Settlement 308 Asexual Reproduction 308 Parthenogenesis 308 Budding 308 Regeneration 310 Part III Zoogeography and Evolution 16 Zoogeography 313 The Quality of the Database 313 Species Value 314 Endemism and Centers of Origin 315 Dispersal, Boundaries, and Biogeographic Units 316 Cosmopolitan Species 319 17 Generic Analyses: Distribution Summary and Cladogenesis 321 Family Sipunculidae 321 Sipunculus and Xenosiphon 321 Siphonosoma 322 Siphonomecus and Phascolopsis 323 Family Golfingiidae 323 Golfingia 323 Nephasoma 324 Thysanocardia 326 Family Phascolionidae 326 Phascolion 326 Onchnesoma 328 Family Themistidae 328 Themiste 328 Family Phascolosomatidae 329 Phascolosoma 329 Antillesoma 331 Apionsoma 331 Family Aspidosiphonidae 331 Aspidosiphon 331 Cloeosiphon and Lithacrosiphon 333 Contents XI 18 Evolution and Phylogenetic Relationships 334 Direct Evidence: The Fossil Record 334 Indirect Evidence 336 Comparative Immunology 337 Comparative Biochemistry and Physiology 339 Comparative Fine Structure 342 Comparative Embryology 342 Conclusions 344 19 Within-Phylum Relationships 346 Morphological Data 349 Broadly Useful Characters 350 Limited-Use and New Characters 351 Karyological Data 354 Characters Not Used in Numerical Analyses 354 Embryological Data 357 Zoogeographical Data: Paleo-Oceanographic Analysis 360 Paleozoic (570-248 Ma) 363 Mesozoic (248-65 Ma) 363 Cenozoic (65 Ma-Present) 364 Cenozoic Subregional Events 368 Conclusions and Assumptions 373 20 Evolutionary Hypothesis 375 Appendix 1 Recent Species Inquirenda and Incertae Sedis 381 Appendix 2 Species Inquirenda and Incertae Sedis as in Stephen and Edmonds, 1972, with Current Status 385 Bibliography 387 Taxonomic Index 439 Subject Index 451 Preface This book is designed to bring together everything known about the Sipun- cula, a phylum of marine worms. It can be viewed as the first replacement for Die Sipunculiden, eine systematische Monographic, the 1883 mono graph by Selenka, de Man, and Biilow. The Introduction gives a concise overview of the phylum (also see E. Cutler, 1989), together with a brief history of the group, useful "how-to" information, and a glossary. Part I is an updated version of the invaluable systematic compilation by Stephen and Edmonds (1972). (I will supply an errata list for that book on request.) A major difference between that work and this one is that the present work incorporates critical revisions of the past 20 years such as the introduction of new higher taxa, redefinition of some genus groups, and the reduction of the number of species from more than 300 to 149. Part II updates and expands earlier surveys of sipunculan biology such as that provided in French by Tetry (1959) and in English by Hyman (1959). New information has been forthcoming from biochemists and physiologists. In addition, immunologists have learned a great deal about these worms' defense systems, and much has been added to our knowledge of sipunculan reproductive biology. A richly illustrated review of sipun culan microscopic anatomy was in process of publication (Rice, 1993a) as this book was being prepared. Part III provides a new perspective on the phylum's zoogeography and evolution and brings together information from a wide array of subject areas. Formulating this synthesis led me to change a few of my assump tions and thus produced an evolutionary scenario that differs in some aspects from earlier models, including those in E. Cutler and Gibbs, 1985. This book should be useful and accessible to biologists with a minimal background in marine invertebrates, to advanced students, and to marine ecologists who wish to identify specimens. Complete synonymies are giv en for most species. In the few cases when the list would be very long, however, only the original describer, a few key references including revi-