The Sipuncula: Their Systematics, Biology, and Evolution

The Sipuncula Their Systematics, Biology, and Evolution Edward B. Cutler

The Sipuncula Their Systematics, Biology, and Evolution

E D W A R D B. C U T L E R 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

Contents

Vlll

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

11

12

13

14

15

Urn Cell Complex 265 Immune System 268 Encapsulation and Inactivation 268 Antibacterial and Cytotoxic Activity 269 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 Excretory System 276 Anatomy 276 Physiology 279 Nitrogen Excretion 279 Osmotic, Ionic, and Volume Regulation 279 Digestive System 282 Anatomy 282 Physiology 283 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 Reproduction and Regeneration 297 Sexual Reproductive System and Modes 297 Gonads and Gender 297 Gametes 298 Reproductive Cycles and Spawning 300

Contents

X

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 16

17

Zoogeography and Evolution

Zoogeography 313 The Quality of the Database 313 Species Value 314 Endemism and Centers of Origin 315 Dispersal, Boundaries, and Biogeographic Units Cosmopolitan Species 319

316

Generic Analyses: Distribution Summary and Cladogenesis 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

321

Contents 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

XI

Preface

This book is designed to bring together everything known about the Sipuncula, a phylum of marine worms. It can be viewed as the first replacement for Die Sipunculiden, eine systematische Monographic, the 1883 monograph 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 sipunculan 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 assumptions 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 given 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-

XIV

Preface

sions, and the most recent review(s) are provided. Other sources are included in the Bibliography. Since this book is the culmination of 25 years of work, it is impossible to name all who have helped me in its production. Although I have had no direct financial assistance with the preparation of this manuscript, much of my earlier work was subsidized by the U.S. National Science Foundation and Utica College of Syracuse University. Since 1989 I have been on long-term disability leave from my position as professor of biology at Utica College owing to a progressive hereditary eye problem, retinitis pigmentosa. While writing this book I have been the guest of Dr. H. Levi and the Museum of Comparative Zoology, Harvard University. The members of the Invertebrate Department—Ardis Johnston, Harlan Dean, Dianna Sherry, William Piel, Tila Perez, and especially Laura Leibensperger, who also assisted with the artwork—have provided me with an academic home, supporting me in many small but significant ways. The library staff at MCZ and Utica College have been most helpful in obtaining materials. Katherine Brown-Wing prepared the artwork in the systematics section. My visual impairment makes reading print material difficult and slow. The technical aid provided by the New York Commission for the Blind has made it possible for me to continue reading and writing. I am indebted to my rehabilitation counselor, John Hosford, for his 15 years of support and encouragement. Major and invaluable assistance came from four volunteer readers: Cal Cohen, Brian Space, Doris Mei, and Linda Khym, who came to me via the Massachusetts Association for the Blind. Anne Covert and Margaret Lashbrook also provided assistance, including the reading of printed material. I am indebted to Melinda Conner, copy editor, and to the editorial staff of Cornell University Press for their expertise, flexibility, and good humor. For many years my efforts to understand this group of worms were assisted by, and in recent years were made possible by, the collaboration of Norma J. Cutler. She continues to be available, on a limited basis, as a consultant to those needing assistance in identifying sipunculans and can be contacted at the Biology Department, Hamilton College, Clinton, N.Y. I3323EDWARD B. CUTLER

Museum of Comparative Zoology Harvard University Cambridge, Massachusetts

Checklist of the Sipunculan Species

Class Sipunculidea Order Sipunculiformes Family Sipunculidae . Sipunculus Sipunculus (Sipunculus) lomonossovi, longipapillosus, marcusi, norvegicus, nudus, phalloides phalloides, p. inclusus, polymyotus, robustus Sipunculus (Austrosiphon) indicus, mundanus • Xenosiphon absconditus, branchiatus -Siphonosoma arcassonense, australe australe, a. takatsukii, boholense, cumanense, dayi,funafuti, ingens, mourense, rotumanum, vastum • Siphonomecus multicinctus ' Phascolopsis gouldii Order Golfingiiformes Family Golfingiidae • Golfingia Golfingia (Spinata) pectinatoides Golfingia (Golfingia) anderssoni, birsteini, capensis, elongata, iniqua, margaritacea margaritacea, m. ohlini, mirabilis, muricaudata, vulgaris vulgaris, v. herdmani ' Nephasoma Nephasoma (Cutlerensis) rutilofuscum Nephasoma (Nephasoma) abyssorum abyssorum, a. benhami, bulbosum, capilleforme, confusum, constricticervix, constrictum, cutleri, diaphanes diaphanes, d. corrugatum, eremita,filiforme,flagriferum, laetmophilum, lilljeborgi, minutum, multiaraneusa, novaezealandiae, pellucidum pellucidum, p. subhamatum, rimicola, schuettei, tasmaniense, vitjazi, wodjanizkii wodjanizkii, w. elisae - Thysanocardia catharinae, nigra, procera

xvi

Checklist

Family Phascolionidae • Phascolion Phascolion (Isomya) convestitum, gerardi, hedraeum, lucifugax, microspheroidis, tuberculosum Phascolion (Lesenka) collare, cryptum, hupferi, rectum, valdiviae valdiviae, v. sumatrense Phascolion (Montuga) lutense, pacificum Phascolion (Phascolion) abnorme, bogorovi, caupo, hibridum, medusae, megaethi, pharetratum, psammophilus, robertsoni, strombus strombus, s. cronullae, ushakovi Phascolion (Villiophora) cirratum •> Onchnesoma intermedium, magnibathum, squamatum squamatum, s. oligopapillosum, steenstrupii steenstrupii, s. nudum Family Themistidae - Themiste Themiste (Themiste) alutacea, blanda, dyscrita, hennahi, pyroides Themiste (Lagenopsis) cymodoceae, dehamata, lageniformis, minor minor, m. huttoni, variospinosa Class Phascolosomatidea Order Phascolosomatiformes Family Phascolosomatidae • Phascolosoma Phascolosoma (Fisherana) capitatum, lobostomum Phascolosoma (Phascolosoma) agassizii agassizii, a. kurilense, albolineatum, annulatum, arcuatum, glabrum glabrum, g. multiannulatum, granulatum, maculatum, meteori, nigrescens, noduliferum, pacificum, perlucens, saprophagicum, scolops, stephensoni, turnerae • Antillesoma antillarum , Apionsoma Apionsoma (Apionsoma) misakianum, murinae murinae, m. bilobatae, trichocephalus Apionsoma (Edmondsius) pectinatum Order Aspidosiphoniformes Family Aspidosiphonidae Aspidosiphon Aspidosiphon (Akrikos) albus, mexicanus, thomassini, venabulum, zinni

Checklist

xvn

Aspidosiphon (Aspidosiphon) elegans, exiguus, gosnoldi, gracilis gracilis, g. schnehageni, misakiensis, muelleri, spiralis Aspidosiphon (Paraspidosiphon) coyi, fischeri, laevis, parvulus, planoscutatus, steenstrupii, tenuis Lithacrosiphon cristatus, cristatus lakshadweepensis, maldivensis Cloeosiphon aspergillus

The Sipuncula

Introduction

JJktoricalJIotes

The faxon Sipuncula has a complex hierarchical history, having been ranked as a family, order, class, and phylum at different times. The names and the other taxa linked with this relatively small group of worms have been reviewed in detail by Hyman (1959; see also table 1 in Stephen and Edmonds, 1972, for twentieth-century usage). Sipunculans were first illustrated in the mid-sixteenth century (Rondelet, 1555). Two centuries passed before they appeared in the literature again, as a new type of "zoophyte" named Syrinx by Bohadsch in 1761. Linnaeus (1766) applied the name Sipunculus, placing them within the Vermes Intestina. Three other reports appeared during the last half of the eighteenth century: Pallas, 1774; Barbut, 1783; and Martin, 1786. Many more works on sipunculans were produced during the nineteenth century. Early in the century, Rafinesque (1814) proposed the family name Sipuncula for Syrinx (= Sipunculus in part) within his class Proctolia, which included the nonsegmented worms with a complete gut. Soon thereafter Lamarck (1816) placed them in his Radiaires Echinodermes, a taxon that included the holothurians. In 1823 Delle Chiaje suggested the name Sifunculacei as a unique subset within the annelids. This name was soon , followed by de Blainville's (1827) Sipunculidia, which included the Pri- / apulida). The name that persisted the longest was Gephyrea ("bridge"), a group created by de Quatrefages (1847) that included the Echiura and Priapulida. A few other group names were offered in the later 1800s, including Sipunculacea (Hatschek, 1881), Podaxonia (Lankester, 1885b), and Prosopygia (Lang, 1888). At the close of the century, Sedgwick (1898) proposed the name Sipunculoidea for the group, which he considered a phylum. For some reason these later names were not adopted, and Gephyrea continued to be used into the mid-twentieth century. Perhaps the reason was, as

2

Introduction

Hyman stated when she proposed using Sipunculida for the phylum, that "adopting the concept Gephyrea offers an easy way of disposing of three groups of very uncertain affinities. But as all modern students of these groups are agreed that there is no close relationship between them the name and the concept Gephyrea must be obliterated from zoology" (Hyman, 1959; italics mine). The current spelling of the phylum, Sipuncula, and the use of "sipunculan" for the vernacular name (not sipunculid) was proposed by Stephen (1965) and restated by Stephen and Edmonds (1972). This rather dynamic nomenclatural history delayed the naming of intermediate taxa (families, orders, and classes). Pickford (1947) suggested that the genera should be arranged into four groups. Then Akesson (1958), using a different set of characters, recommended clustering the genera into three groups. Neither author offered taxon names or ranks for their groups, however, a void that was only partially filled when Stephen and Edmonds (1972) erected four families. These four families were employed by Murina (i975d) in her consideration of the evolutionary relationships between genera. E. Cutler and Gibbs (1985; Gibbs and Cutler, 1987) set forth a more complete arrangement of the 17 genera into two classes, four orders, and six families, based on a phylogenetic analysis. Two non-nomenclatural events have also been important in the history of sipunculan biology. In the late nineteenth century, several European biologists refocused their attention from external, macroscopic features to internal, microscopic traits. Major contributors in this new attention to details, based largely on dissections, included Keferstein (1862-67), Selenka (1875-97), and Shipley (1890-1903). While from today's perspective these anatomical studies may seem unglamorous, they were crucial to our detailed understanding of the organ systems and attributes of the various taxa and still serve as excellent models of solid science. Selenka, de Man, and Biilow's monograph (1883) brought much of this work together in a single volume and was a major milestone in codifying the diversity and order within the sipunculans. Stephen and Edmonds's 1972 monograph was the intellectual descendent of this nineteenth-century work. The second milestone event was the International Symposium on the Biology of the Sipuncula and Echiura held in Kotor, Yugoslavia, in 1970. This weeklong gathering brought together almost everyone in the world who had anything to say about these animals. The proceedings, published as two volumes in 1975-76, are a compendium of the knowledge on the

Overview of Biology

3

subject as of that date. The opportunity for sipunculan biologists to meet and communicate face to face was in many ways as valuable as the formal exchange of information.

Overview of Biology and Morphology

The phylum Sipuncula, the peanut worms, is a group of unsegmented, vermiform, marine coelomates. Closely related to the annelids and mollusks, the approximately 150 species live in a wide variety of oceanic habitats, at all depths, within unconsolidated sediments or inside protective shelters such as mollusk shells or coral. Sipunculans have two body regions: a trunk and a more slender retractable introvert (Fig. 1; see Glossary for definitions of terms). The adult trunk ranges in length from 3 to more than 400 mm, commonly 15-30 mm, and the shape varies from a slender cylinder, to spindle and flask shaped, to almost spherical. The particular shape of an individual worm may be molded by the microhabitat in which it lives (e.g., crevice, burrow, empty shell), but these epigenetic forces work within genetic constraints. Sipunculans have a variety of epidermal structures, such as papillae, hooks, and shields. The introvert length ranges from less than half the trunk length in some species to several times the trunk length in others. The mouth is at the tip of the introvert and is surrounded by tentacles in members of the class Sipunculidea. Behind the tentacular region is a zone that may bear posteriorly directed hooks, which are either scattered or—in the class Phascolosomatidea—arranged in regular rings. Internally, the esophagus and double-helix-shaped intestine spiral toward the posterior end of the body and then anteriorly, via a rectum, to the mid-dorsal anus. The anus is located at the anterior end of the trunk except in Onchnesoma and a few Phascolion species, where it is some distance out on the introvert. Near the anus in most species a threadlike spindle muscle originates from the body wall and extends down the center of the gut coil, thereby ensuring the proper orientation of the coil. In many genera, the spindle muscle extends to and attaches at the posterior end of the trunk; in some genera it terminates within the gut coil. A pair of simple, saclike metanephridia open ventrolaterally at the anterior end of the trunk {Phascolion and Onchnesoma have only one metanephridium). The longitudinal muscle layer on the inside of the body wall is divided into separate bundles in half the genera but forms a smooth,

4

Introduction

Figure i. Generalized sipunculan morphology. A. Internal amalgam. B. Aspidosiphonid. A, anus; AS, anal shield; CG, cerebral ganglion; CS, caudal shield; CVV, contractile vessel villi; DRM, dorsal retractor muscle; E, esophagus; FM, fixing muscle; G, gonad; H, hooks (scattered on A, in rings on B); I, introvert; LMB, longitudinal muscle bands; N, nephridia; P, papillae; PSM, posterior spindle muscle; (5) rectum; RC, rectal caecum; SM, spindle muscle; T, tentacles; TK, trunk; VNC, ventral nerve cord; VRM, ventral retractor muscle; WM, wing muscle.

Obtaining and Handling Sipunculans

5

uniform muscular layer in the others. Four retractor muscles control the withdrawal of the introvert. In some genera these are reduced and fused to form two or, rarely, a single muscle. A pair of cerebral ganglia form the brain, which connects to the ventral nerve cord via circumenteric connectives. When present, two or four pigmented eyespots occur on the cerebral ganglia, and a chemoreceptor, the nuchal organ, is usually present dorsal to the mouth. Almost all sipunculans are dioecious and lack sexual dimorphism. One species is known to be monoecious, one is facultatively parthenogenetic, and two are capable of reproducing asexually by transverse fission. Small gametes are produced from a transient strip of tissue at the base of the ventral retractor muscles. At an early stage in their development gametes are released into the coelom, where they undergo the remainder of their growth and differentiation. When mature, the gametes leave the body through the nephridiopores, and fertilization occurs externally. Most species produce free-swimming trochophore larvae, although the hermaphroditic Nephasoma minutum has been observed brooding early stages within its living space. The production of unique, long-lived pelagosphera larvae by some genera makes transoceanic dispersal possible. After metamorphosis, the juveniles settle on a suitable substratum, where they create a burrow and remain. Most sipunculans are deposit feeders, although a few are filter feeders with elaborate tentacular crowns (Jhemiste). All consume detritus and fecal material as well as bacteria, algae, and small invertebrates. They are in turn eaten by fish, mollusks, crabs, and other predators.

Obtaining and Handling Sipunculans

Collecting Because sipunculans live in such diverse habitats it is difficult to generalize about collecting techniques. In intertidal and shallow subtidal habitats it is possible to obtain representatives of several genera by digging in the sand or mud. The particular niche (combination of gravel, sand, and silt; organic matter; temperature range; wave action; etc.) for each species varies; some are much more stenotopic (have narrow physiological tolerances) than others. Since sipunculans are distributed in a patchy manner, one can spend much time searching without recovering many worms.

6

Introduction

Sipunculan holes are visible during low spring tides, but they are not easily differentiated from holes made by other worms, clams, or small crabs. Some species (e.g., Phascolopsis and small Siphonosoma) live just a few centimeters below the surface, but larger members of the Sipunculidae burrow down a meter or so, and extracting them requires a major excavation. Some of the best specimens of the latter were obtained from the sediment brought up by the U.S. Army Corps of Engineers when they dredged Florida channels (E. Cutler, 1986). Madagascar fishermen insert the midrib of certain palm leaves into the burrows of large Sipunculus indicus, then exert just enough pressure so that when the animal withdraws its introvert it also pulls the long, pencil-sized object inside, functionally paralyzing itself (E. Cutler, 1965). They then dig down parallel to the worm with the other hand and successfully withdraw the worm. A note to collectors: It is more cost-effective and much less frustrating to buy this "fish bait" from an experienced resident rather than attempting this on one's own. In this case as elsewhere, indigenous people can be very helpful. Material brought up with a shovel or clam fork should be placed on a sieve and washed. The mesh size of the sieve will be determined by the size of the worms one is looking for, but anything coarser than 2 mm is likely to lose an important part of the sample. When searching for the smaller interstitial worms such as Apionsoma, a mesh no larger than 1 mm must be used. Taxa such as Phascolosoma or Themiste, which live in sand-filled cracks, crevices, or pockets in the rocky intertidal, can be obtained only by using a small digging tool or one's fingers. Sipunculans may also be found tangled in algal holdfasts or byssal threads of mussels, wedged in masses of oysters, or under algal mats. Finding these species requires careful breaking apart of clumps that have first been placed in a tray to catch "dropouts." Coral and soft rocks provide living space for many taxa, including most of the Aspidosiphonidae, many Phascolosoma, and Antillesoma. The worms cannot be forced or pulled intact from rocks, but undamaged specimens can be obtained with careful use of a hammer and chisel to break apart the material. One alternative that sometimes works, if time and conditions permit, is to let the rock stand in a container of stale seawater for a day or two, after which some worms abandon their shelters. Many Phascolion and Aspidosiphon species inhabit empty mollusk shells, polychaete tubes, and the like, and it pays to examine seemingly

Obtaining and Handling Sipunculans

7

empty shells carefully. Removal of an intact sipunculan from a gastropod shell is difficult but not impossible. Careful use of a small hammer and a pair of forceps often works. Shells containing preserved animals can be soaked in a dilute acetic acid solution overnight. This dissolves the shell's matrix, exposing the worm, but may cause superficial changes in the worm's cuticle. Standard dredges, trawls, or grabs function well in collecting worms in subtidal waters. The depth that the device digs into the sediment determines which animals are obtained. If the trawl does not dig into the bottom for at least 2-3 cm, most of the larger infaunal sipunculans will be left behind. After the trawl sample is deposited on the deck, it must be washed through a sieve with a mesh of 1 mm or less, especially if one is collecting in deep water, where worm diameters tend to be in this size range. A nested stack of two or three sieves of differing mesh sizes is a good way of protecting the more fragile animals from damage by coarse material such as shell hash or gravel that is present in the sample. Sorting out the sipunculans from the other organisms brought up in a dredge haul can be difficult, especially as regards the smaller animals. Nonspecialists often confuse sipunculans with anthozoans, holothurians, phoronids, and other "vermes" such as nemerteans, echiurans, nematodes, or even polychaetes. One useful clue that works well for worms with transparent body walls is to look for the double-helix gut coil. If the animal is opaque, it may be necessary to open the body wall to check for this coil or the retracted introvert. If there is a body opening (mouth or anus) at both ends, the animal is not a sipunculan. Relaxing and Preserving Relaxing or narcotizing sipunculans before fixing them will greatly expedite subsequent identification. The tentacles and hooks at the distal tip of the introvert are critical characteristics in most genera, and, ideally, the introvert should be fully protruded before fixation. There is no single best way to achieve this. What works well for one taxon may not work at all for another. In general, if conditions permit, the worms should be placed in a shallow tray with just enough water to cover them so they can be easily observed and handled. Sprinkling a few crystals of menthol on the surface of the water or dissolving some menthol in alcohol and placing a few drops of this solution in the water is often enough to cause relaxation. A slow application of alcohol by itself may work, and substances such as MgCl2

8

Introduction

and propylene phenoxetol have met with some success. Placing the worms in a refrigerator works for some warm-water species. All these methods must be employed for 1-12 hours to be effective. Sometimes it is necessary to force the protrusion of the introvert by applying pressure to the trunk in the form of a gentle squeezing between the fingers—or forceps if the worm is a small one. Then, if necessary to keep the introvert from withdrawing, grasp the worm firmly behind the tentacles with forceps as it is placed in 5-10% formalin for fixation. (This "choke hold" is not necessary if the preceding narcotization was effective.) The relaxation success rate is lowest in the Aspidosiphonidae and species with long, slender introverts such as the Apionsoma. If the animal is large (diameter 1-2 cm), a small incision in the trunk wall will allow for better perfusion of the fixative. After a day or two of fixation, the worms should be transferred to 70% alcohol for storage. If scanning or transmission electron microscopy or any biochemical analyses are planned, then the fixation and preservation process must be consistent with that goal. Dissecting Small scissors or a scalpel can be used to open the body of a sipunculan, but scissors work better. If the anterior dorsal anus can be located, use that as a reference point and cut along the mid-dorsal line, passing just to one side of the anus. Be careful to keep the cutting tool close to the body wall to avoid any damage to internal organs. If the animal is pinned down or held open, it is possible to see the internal organs in their proper perspective. The torsion created in animals that lived in gastropod shells creates special problems for which there is no simple solution—just patience and persistence. The specimen should not be allowed to dry out during the dissection process. Coagulated gametes, if present, can usually be removed by a stream of fluid from a wash bottle. If the introvert is not fully extended, the retracted introvert must be opened to expose hooks and tentacles. In larger animals, begin cutting back into the animal from the opening formed where the introvert is turned in on itself, cutting a double layer of introvert wall until the head end is encountered. In smaller worms, locate the head by starting from the inside and following the retractor muscles anteriorly to the point where they fuse. The brain is often visible here (sometimes with pigmented eyespots), but in any case the texture and color of the region change. Once this region is

Glossary

9

located, the inverted tube can be carefully opened and laid back to uncover external attributes that are now on the inside. If the most distal hooks are not located and examined, serious mistakes in identification can result. A dissecting microscope is used to determine the shape and size of the hooks. First, cut off a small piece of introvert skin and place it on a glass slide in a drop of diluted glycerine. Using needles or fine forceps, tease away the underlying muscle layers. After that, the skin can be teased apart into fine strands with hooks mostly intact, although a few hooks will come loose and may be damaged in the process. Flatten the preparation by applying firm pressure with the cover slip. Under a compound microscope the slide will show a mix of orientations; usually only a few hooks will lie flat and unobstructed. Papillae can be examined similarly. Naming A species name may be either an adjective or a noun in apposition, from Greek, Latin, or modern roots, and therefore subject to different spelling rules with regard to gender agreement, case, declensions, etc. Confusion sometimes results when the generic "home" of the species is changed (this book does correct a few errors contained in earlier works). Consult the International Code of Zoological Nomenclature for details. The following list may help sipunculan systematists reduce their error rate, but it is only a starting point. Neuter genera: Antillesoma, Apionsoma, Nephasoma, Onchnesoma, Phascolion, Phascolosoma, and Siphonosoma. Masculine genera: Aspidosiphon, Cloeosiphon, Lithacrosiphon, Siphonomecus, Sipunculus, and Xenosiphon. Feminine genera: Golfingia, Themiste, and Thysanocardia. The enigmatic genus Phascolopsis is of uncertain gender.

Glossary

The following are very general definitions of structures found in adult sipunculans. Variations are discussed within the "Morphological Characters" section of the relevant taxa. Anal shield A hardened, caplike structure located at the anterior end of the trunk in the three Aspidosiphonidae genera. It is in the area between the anus and the introvert in Aspidosiphon and Litha-

10

Introduction

crosiphon, and terminally around the trunk in Cloeosiphon. It functions as a plug or operculum for worms that live in corals or mollusk shells. The dermal papillae produce varying amounts of horny protein or calcium carbonate (calcite or aragonite). The anal shields of some Aspidosiphon species are very weakly developed and not always easy to spot. Anus The terminus of the digestive tract is located on the mid-dorsal line at the anterior end of the trunk (base of the introvert) in most species. In Onchnesoma and a few Phascolion, it is located on the introvert 50-95% of the distance to the tip. In larger worms the anus is visible externally as a small pore. The anal sphincter muscle may create a pucker. Attachment papillae {See Holdfast papillae) Brain {See Cerebral ganglion) Caecum {See Rectal caecum) Caudal appendage (Tail) A few species have a distinct tail-like appendage that is significantly smaller in diameter than the trunk. The posterior end of the trunk is generally rounded, and the circular muscles can contract to produce a pointed end in some species, but this is not what is meant here. Caudal shield A circular or conical covering of horny protein, often grooved, found at the posterior end of the trunk in some Aspidosiphon. The shape of this shield is under the control of the body wall muscles; in preserved material it may assume a pagoda shape. Cephalic (Cerebral) tube A small tube connecting the outside to the cerebral organ in a few Sipunculus species. Cerebral ganglion (Brain) The large, bilobed aggregation of nerve bodies is connected to the ventral nerve cord by circumenteric connectives dorsal to the anterior end of the esophagus. Cerebral organ (Frontal organ) Within the cerebral ganglia, but separated from it by connective tissue, is an area composed of columnar epithelium. Its function is unknown, but it probably has secretory and sensory roles at different times in the worm's life. It is connected to the outside when a cerebral tube is present and is well developed only in Sipunculus. The distinction between this and the digitate processes, or frons (see below), has not always been clear. Circular muscles The circular muscles forming the outermost of the two muscle layers of the body and introvert are continuous in most families, but in most members of the Sipunculidae this layer divides into partially or completely separate bundles.

Glossary

II

Coelomic canals and sacs In species whose body wall is not formed of continuous sheets, the spaces between the muscle bands allow closer contact between the coelomic fluid and the seawater and thus facilitate gas exchange. In most members of the Sipunculidae these internal openings lead into enlarged subcuticular spaces or elongate canals (see E. Cutler, 1986). Collar A region of the introvert found a short distance behind the tentacles. In Themiste this region may be either white or dark blue, but otherwise it has no distinguishing qualities. In many of the Phascolosomatidae, most notably in Antillesoma, the collar is an unpigmented but protruding ring of tissue separating the "head" from the rest of the introvert. Contractile vessel (Compensatory sac, Dorsal or Polian vessel) A closed, fluid-filled vessel attached to the dorsal side of the esophagus and continuous with the tentacular coelom. In some members of the Sipunculidae it takes the form of a pair of lateral tubes. The dimensions vary with the size and complexity of the tentacular crown; it is very reduced in small worms with reduced tentacles. In some large worms the tube may have bulbous swellings or vesicles; in others, villi are present. The contractile vessel contains its own respiratory pigment and facilitates gas exchange between the internal and external environments. Since the wall of this vessel is muscular, it probably acts as a reservoir for the tentacular coelomic fluid when the introvert is withdrawn and helps maintain turgor when it is expanded. Some preexcretory filtration by podocytes occurs via this system also. Contractile vessel villi and tubules In several genera the surface area and fluid volume of the contractile vessel are increased by many digitiform villi along its length. These villi should not be confused with the bulbous swellings found in a few species. In the subgenus Themiste s.s. a few elongate threadlike tubules extend from the posterior end, not unlike Polian tubules in some echinoderms. Digitate processes (Frons) The anterior dorsal margin of the cerebral ganglia of Sipunculus species is elaborated as a spongy fringe or as digitate, rarely leaflike, extensions, which serve as sites for the storage and release of neurosecretory products. Dissepiments Within the body cavity in some Siphonosoma species are incomplete transverse partitions formed of thin connective tissue sheets that rarely cover more than the ventral third of the space and are extremely variable within populations.

12

Introduction

Esophagus The anterior end of the digestive tract between the mouth and the coiled or looped intestine. Eyespots These photoreceptors are pigment-cup ocelli embedded in the dorsal surface of the brain. They are not always pigmented and seem to be better developed in shallow-water species. Fixing muscles (Fastening muscles) Small, threadlike muscles that attach the digestive tract (commonly the esophagus or rectum) to the body wall. When present, they usually number less than four; they are not present in all species. Fusiform bodies A set of 2-5 very small spindle-shaped organs found in two species of Siphonosoma. The presence of secretory columnar cells and granular products in the lumen, which opens to the exterior at the posterior tip of the trunk, suggests a pheromone or excretory function. Glans The smooth posterior tip of the trunk in some members of the Sipunculidae is sometimes distinctly set off from the rest of the trunk by a ridge that resembles an acorn or the glans of a penis. Gonads A strip of tissue at the base of the ventral retractor muscles in which gametogenesis occurs. Gonads are not visible at nonbreeding times of the year. Holdfast papillae Certain trunk papillae in most Phascolion species produce large amounts of a horny protein (not chitin) that may be O, U, or V shaped. These calluslike, enlarged, darkened papillae appear to assist in anchoring the worm in its protective shelter, although this function has not been demonstrated. They have a house-cleaning function in P. strombus, which uses them to scrape bacteria from the inside of the shelter (Hylleberg, 1975). Hook Many variations in size, shape, distribution, and number of this basic unit are known, and hooks probably are not homologous across families. In general they are pointed, curved, thornlike, protein-based (not chitin) units distributed around the distal part of the introvert that assist in obtaining food. Introvert The retractable narrow, anterior part of the animal. The trunkintrovert border is usually distinct and is defined as the plane where the nephridiopores (and commonly the anus) are located. It varies in length from one-fourth to ten times the trunk length. Keferstein bodies Very small secretory structures on the inner body wall that exit to the outside via a duct and pore, found in a few Siphonosoma species. Neither the nature of their products nor the function of the bodies is known.

Glossary

13

Longitudinal muscle The innermost of two muscle layers of the body and introvert wall. In 8 of the 17 genera this layer divides into partially or completely separate bundles in the trunk, never in the introvert. In the other genera the layer is continuous. Nephridia, Nephridiopore, Nephrostome A pair of tubular, saclike metanephridia are located ventrolaterally at the anterior end of the trunk (two genera have only one nephridium). They open into the coelom via a ciliated funnel-shaped nephrostome, and after traversing a V-shaped course within the organ, the filtrate exits via the nephridiopores (which are commonly located at the trunk-introvert border). Some degree of excretion of nitrogenous wastes (mostly ammonia) and osmoregulation is accomplished. These organs also serve as gonoducts during the breeding season. Nuchal organ A ciliated chemoreceptor organ on the dorsal margin of the oral disk of most species. In some species this organ is very well developed and bears specialized tentacles; other species lack nuchal tentacles and an obvious pit. Oblique muscles A thin layer of muscle found in the body wall of larger members of the Sipunculidae; it lies at an angle to, and between, the circular and longitudinal layers. Ocelli (See Eyespots) Papillae Aggregations of epidermal glandular cells may form rounded or conical protuberances which are larger and more numerous toward either end of the trunk. The precise size and shape of the papillae vary too much within populations to be of widespread use taxonomically. Paraneural muscle A pair of longitudinal muscle strands that parallel the anterior portion of the ventral nerve cord in some members of the Sipunculidae. Postesophageal loop A loose loop of intestine between the esophagus and the tighter coil. Found only in Sipunculus. Protractor muscles A third pair of introvert muscles (in addition to the retractor muscles) present in the adults of three species. They insert near the brain and originate on the body wall at the anterior margin of the trunk. This arrangement presumably allows these muscles to assist in the eversion of the introvert. Similar muscles are present in a number of larvae. Pseudoshield A dense aggregation of dark papillae around the anterior end of the trunk, present in some Phascolion and Golfingia. Racemose glands (biischelformigen Korper, sensu Selenka) Tufted glan-

14

Introduction

dular organs on either side of the rectum, of unknown function, found in a few Sipunculus species. Rectal caecum A small, blind sac at the junction of the intestine and rectum, of unknown but possibly secretory function. The caecum is not present at all in some species; in others only some individuals have one. Rectum The terminal portion of the digestive tract, generally short and straight with well-developed circular muscle in the wall. Retractor muscles A set of muscles that originate on the body wall and insert near the brain at the distal end of the introvert; their function is to pull the introvert into the trunk. The basic pattern is two distinct pairs, a dorsal and a ventral, but loss or fusion has occurred more than once, and in adults of several genera only the ventral pair is detectable. Ontogenetic anomalies may produce worms with fewer than a full complement. Sipunculus loop (See Postesophageal loop) Skin bodies (Hautkorper) Aggregations of epidermal gland cells that form low subcuticular mounds, not distinct raised papillae. More common in the Sipunculidae genera. Spindle muscle A slender, threadlike strand of muscle that extends through the center of the intestinal coil. The anterior end generally connects to the body wall near the anus or to the rectum. The posterior end extends through the coil and attaches to the posterior end of the trunk in the Phascolosomatidea. In most Sipunculidea genera the spindle muscle ends within the gut coil itself, but in a few species it is poorly developed or missing. Spine (A) Small introvert hooks that are almost erect and pyramidal, not recurved type I hooks as seen in Phascolion. These may have narrow bases or blunt tips. (B) Pointed, more or less cone-shaped units on the anal shield of some Aspidosiphon species. Spinelets Small, pointed units found at the base of the introvert hooks in a few species (Apionsoma and Golfingia [Spinata]). Tail (See Caudal appendage) Tentacles Extensions of the body wall at the distal end of the introvert. (A) Peripheral tentacles surround the mouth and assist in food capture and gas exchange in most members of the class Sipunculidea. The extreme diversity in number, size, arrangement, and complexity cannot be treated here; refer to the appropriate section in each genus. (B) In several genera nuchal tentacles surround the

Glossary

15

nuchal organ dorsal to the mouth. These are generally small, few (20OO m

8 S. lomonossovi

- Brain bilobed; processes present; at depth 50 mm in adults. All 10 species inhabit intertidal or shallow subtidal sandy to muddy sand; seven in tropical and subtropical areas, three in temperate regions. See Figures 3 and 9-12. TYPE SPECIES. Phascolosoma australe Keferstein, 1865. NOMENCLATURAL NOTE. The subgeneric separations proposed by Fisher (1950b) are not supportable because the transverse dissepiments in the body cavity are extremely variable and multiple rectal caecae occur in only one species (E. Cutler and Cutler, 1982). A subdivision based on the presence or absence of contractile vessel villi would be more consistent with classification criteria used elsewhere in the phylum. Morphological Characters of Siphonosoma Introvert Hooks and Papillae. As in other genera the term hook has been used to describe a variety of epidermal structures. At one end of the Siphonosoma continuum are five species with no hooks and only secretory papillae on the introvert (5. boholense, S. cumanense, S.funafuti, S. ingens, and S. mourense). At the other end are 5. australe and S. vastum, which have large, pointed hooks (Fig. 10B). In between are 5. dayi and S. arcassonense, which have rings of chitinoid, tubular, scalelike papillae that lie flat along the introvert, arranged like (and probably homologous to) hooks (Fig. 10A). Finally, S. rotumanum has short, blunt hooks, each closely associated with a large papilla (Fig. 10C). Contractile Vessel Villi. The villi require careful examination and a clear understanding of terms. The tubular contractile vessel may be folded like a

46

The Sipunculids

Figure 9. Siphonosoma. A. Expanded S. cumanense (drawn by L. Leibensperger). B. Internal view (abbreviations as in Figure 1). C-E. Contractile vessels (from E. Cutler and Cutler, 1982, courtesy of the Biological Society of Washington). C. Side view with villi. D. Dorsal view of vessel as it sometimes appears in contracted introvert with pleats or folds. E. Side view of vessel with the bulbous swellings, not villi, present in some large individuals. F. An unnaturally short and fat 5. cumanense with a damaged posterior end and distorted introvert, probably damaged by a shovel during collection.

Genus Siphonosoma

47

Figure 10. Siphonosoma introvert hooks. A. S. dayi viewed from above, about 150 urn long. B. S. australe, height ca. 200 am. C. S. rotumanum hook and associated papillae, height 100-200 (xm.

Figure 11. Multiple rectal caecae (MRC) in S. vastum (may be less numerous than shown here). (After Selenka et al., 1883.)

The Sipunculids

Figure 12. Cluster of five tubular fusiform bodies (FB) in the posterior end of Siphonosoma ingens. (From E. Cutler and Cutler, 1982, courtesy of the Biological Society of Washington).

compressed accordion or may have bulbous pouches or vesicles (Fig. 9DE), but these structures are not villi. Villi are digitiform or clavate, small in diameter, and their length exceeds their width by several times. Villi are outgrowths from, not swellings of, the underlying vessel (Fig. 9C). Number of Longitudinal Muscle Bands. The degree of anastomosing makes a precise count impossible, but this attribute helps discriminate between S. funafuti and S. boholense. Multiple Rectal Caecae. Siphonosoma vastum has a rectum with numerous digitiform, appendix-like structures near the anus (Fig. 11). Origin of Introvert Retractor Muscles. In nine species the ventral pair originates posterior to the dorsal, but in 5. cumanense all four muscles originate at the same level along the anterior-posterior axis. Fusiform Bodies. Two species (S. arcassonense and S. ingens) have three to six small, thin, threadlike secretory bodies clustered in the very posterior tip of the trunk, where they open to the outside via pores. These are easily overlooked because they are so small (Fig. 12).

Genus Siphonosoma

49

Key to Siphonosoma Species 1. Contractile vessel without distinct villi (bulbous vesicles may be present) (Fig. 9E) 2 - Contractile vessel bears distinct villi (Fig. 9C)

6

2. Introvert with hooks or scalelike papillae

3

- Introvert without hooks or scalelike papillae

5

3. Introvert with rings of tubular scalelike papillae, not free-standing hooks (Fig. 10A) S. dayi - Introvert with distinct hooks (Fig. 10B) 4. Rectum with numerous caecae or diverticulae (Fig. 11)

4 S. vastum

- Rectum without numerous caecae

S. australe

5. Less than 22 longitudinal muscle bands

S. funafuti

- More than 28 longitudinal muscle bands

S. boholense

6. Introvert with rings of hooks or scalelike papillae

7

- Introvert without hooks or scalelike papillae

8

7. Scalelike chitinoid papillae on introvert; posterior end of trunk with internal fusiform bodies S. arcassonense - Short, blunt hooks on introvert; no fusiform bodies (Fig. 10C) 5. rotumanum 8. Retractor muscles originate at same level - Dorsal retractor muscles originate anterior to the ventral pair 9. Fusiform bodies in posterior end of trunk (Fig. 12) - Fusiform bodies absent

S. cumanense 9 S. ingens S. mourense

Siphonosoma arcassonense (Cuenot, 1902) Sipunculus arcassonensis Cuenot, 19023:15. Siphonosoma (Siphonosoma) arcassonense.—Stephen and Edmonds, 1972:60. Siphonosoma arcassonense.—E. Cutler and Cutler, 1982:753-754.-Saiz, 1986^71-73; 1993:48-49. DESCRIPTION. Trunk up to 240 mm long. With many crowded, welldeveloped, digitiform or shorter clavate villi along the contractile vessel. The three or four thin, pale, tubular fusiform bodies are about 4 - 7 mm long and more delicate than those of S. ingens (Fig. 12). Some preserved animals have the posterior tip of the trunk drawn in 2-3 mm. The ventral

50

The Sipunculids

nerve cord gives off numerous large, transverse nerves, forming a plexus near the posterior end. The scalelike "hooks" are arranged in up to 120 rings and are strikingly similar to S. dayi; that is, they are tubular, attached to the skin except for the very tip, and lack a sharp point (Fig. 10A). DISTRIBUTION. This active burrower is uncommon in beaches along the Atlantic coasts of France and Spain. Siphonosoma australe australe (Keferstein, 1865) Phascolosoma australe Keferstein, 1865^422-423. Sipunculus australis. —Selenka et al., i883:90.-Shipley, 1899^156. Siphonosoma australe. —Augener, I903:346.-Fisher, 1950^807.-E. Cutler and Cutler, 1979a: 949; i982:754.-Edmonds, 1955:95; 1980:16.-Haldar, 1991:22-24. Siphonosoma (Siphonosoma) australe.—Stephen and Edmonds, 1972:61. Sipunculus aeneus Baird, i868:76.-Rice and Stephen, 1970:57. DESCRIPTION. This well-known species may exceed 200 mm in length and has simple large, dark, pointed hooks 190-210 [im tall. Body wall musculature is often visible through the skin (15-20 LMBs), and the gut fixing muscle may have up to three branches. The contractile vessel and rectum are simple. DISTRIBUTION. Zanzibar, Madagascar, India, Indonesia, Vietnam, northern Australia, New Zealand, and several western Pacific islands; in shallow, muddy sand habitats. Siphonosoma australe takatsukii Sato, 1935 Siphonosoma takatsukii Sato, 1935:308-310; 1939:373.-E. Cutler and Cutler, 1982:759. Siphonosoma (Siphonosoma) takatsukii.—Stephen and Edmonds, 1972:73. Siphonosoma pescadolense Sato, i939:376-379.-Stephen and Edmonds, I972:70.-E. Cutler and Cutler, 1982:759. DESCRIPTION. Worms of this species differ from the nominate form because of their small, blunter hooks (130-140 pjn). DISTRIBUTION. Formosa and the Yap Islands. Siphonosoma boholense (Selenka et al., 1883) Sipunculus boholensis Selenka et al., 1883:109-111. Siphonosoma boholense.—Edmonds, i98o:i7.-E. Cutler and Cutler, 1982:754-755. Siphonosoma (Siphonsoma) boholense.—Stephen and Edmonds, 1972:63.

Genus Siphonosoma

51

DESCRIPTION. Contractile vessel villi are lacking, although the contractile vessel is large and exhibits bulbous vesicular or bubblelike swellings. Siphonosoma boholense lacks hooks, and its dorsal and ventral retractor muscles originate at different levels. Siphonosoma boholense is very similar to S. funafuti (largest specimen 120 mm long), although the latter species is said to have fewer than 20 LMBs, and S. boholense has 29-33. Only 10 specimens have been named S. boholense in the past century and all are more than 200 mm long. Thus it is possible that these worms are not a distinct species but only the older, larger individuals of a species that also includes 5. funafuti. An unanswered question is: Do small 5. boholense really have 29-33 LMBs, or do the LMBs split as the trunk size increases in older worms? It may be that organisms with trunk lengths between 120 and 200 mm are not represented in collections, thus creating a false dichotomy. DISTRIBUTION. Queensland, Australia, and north Borneo.

Siphonosoma cumanense (Keferstein, 1867) Phascolosoma cumanense Keferstein, 1867:53-55. Sipunculus cumanense. —Selenka et al., 1883:104. Siphonosoma cumanense.—Spengel, I9i2:263.-Sat6, I934b:246.-Wesenberg-Lund, 19543:376.-8. Cutler, 1965:56; i984:62-64.-E. Cutler and Cutler, 19793:946-949; 1982: 751 .-Edmonds, 1980:14-15.-E. Cutler et al., 1982:265.-Haldar, 1991:24-27. Siphonosoma (Damosiphon) cumanense cumanense.— Stephen and Edmonds, 1972:46-51. Lumbricus edulis Pallas, 1774:10-12. Sipunculus edulis.—Lamarck, i8i6:79.-Sluiter, 18818:148-150. Siphonosoma edule.—Spengel, 1912:263.-Sato, 1939:371-373.-E. Cutler and Cutler, 1982:751-752. Siphonosoma (Damosiphon) edule.—Stephen and Edmonds, 1972:5153Sipunculus deformis Baird, 1868.-Rice and Stephen, 1970:57. Sipunculus cumanensis vitreus Selenka and Biilow, in Selenka et al., 1883:105-106. Siphonosoma cumanense var. vitrea.—W. Fischer, 19213:3-4. Siphonosoma (Damosiphon) cumanense vitreum.—Stephen and Edmonds, 1972:50. Sipunculus cumanensis opacus Selenka and Biilow, in Selenka et al., 1883:106. Siphonosoma cumanense opaca.— Sato, 1935:304-305. Siphonosoma (Damosiphon) cumanense opacum. —Stephen and Edmonds, 1972:50. Phascolosoma semirugosum Griibe, i868a:8i-82. Sipunculus cumanensis

52

The Sipunculids

semirugosum.—Selenkaet al., 1883:106-107. Siphonosoma cumanense var. semirugosa.—Stephen and Robertson, 1952:435. Siphonosoma (Damosiphon) cumanense semirugosum.—Stephen and Edmonds, 1972: 50. Sipunculus billitonensis Sluiter, 1886:487-488. Siphonosoma billitonense.—Stephen, 194^:402. Siphonosoma (Damosiphon) billitonense.—Stephen and Edmonds, 1972:51. Sipunculus claviger Sluiter, 1902:7-8. Sipunculus novaepommeraniae W. Fischer, 1926:104-106. Siphonosoma novaepommeraniae.—Wesenberg-Lund, i959b:55-58.-Stephen and Edmonds, i972:69.-Edmonds, 1980:17.-E. Cutler and Cutler, 1982: 757Physcosoma hebes Sluiter, 1902:13. Phascolosoma (Satonus) hebes Stephen and Edmonds, 1972:285.-E. Cutler and Cutler, 1983:184. Siphonosoma carolinense W. Fischer, 1928:138-140. Siphonosoma (Damosiphon) carolinense.—Stephen and Edmonds, 1972:44-46. Siphonsoma cumanense var. yapense Sato, 1935:305. Siphonsoma (Damosiphon) cumanense yapense.—Stephen and Edmonds, 1972:51. Siphonosoma hataii Sato, 1935:305-308; 1939:373. Siphonosoma formosum Sato, 1939:375-376. Siphonosoma koreae Sato, 1939:379-381. Siphonosoma cumanense var. koreae.—Wesenberg-Lund, 19573:4. Siphonosoma (Damosiphon) cumanense koreae.—Stephen and Edmonds, 1972:49. Siphonosoma marchadi Stephen, 19603:515-5i6.-Stephen and Edmonds, 1972:54. DESCRIPTION. This species, the most common member of the genus, is morphologically quite plastic and hss 3 long and convoluted history in sipunculan literature (see E. Cutler and Cutler, 1979a, 1982). Siphonosoma cumanense includes worms with and without partial transverse dissepiments across the body cavity. Animals are commonly 100-200 mm long but may exceed 400 mm. The skin is generally smooth and whitish or some shade of gray, with 18-25 ansstomosing LMBs visible through the skin. The bilobed nuchal organ is located outside the ring of peripheral tentacles and is ridged with a parallel series of small pillows on each lobe, but no tentacles. This is the only Siphonosoma species in which the four retractor muscles originate at the same anterior-posterior level. The contractile vessel has msny villi, and the oocytes are 100-130 |xm in diameter. DISTRIBUTION. Widespread in tropical and subtropical oceans, from the western Atlantic (Venezuela to Florida), many locations in the western

Genus Siphonosoma

53

Pacific and Indian oceans, and the Red Sea. Absent in the eastern parts of both major oceans. Siphonosoma dayi Stephen, 1942 Siphonosoma dayi Stephen, i942:246-247.-E. Cutler and Cutler, 1982: 755. Siphonosoma (Siphonosoma) dayi.—Stephen and Edmonds, 1972:64-65. DESCRIPTION. The three specimens that have been given this name have scalelike introvert papillae as their unique feature. The unit is fixed to the skin along its entire length (130-170 jjum), not just basally as most hooks are, and there is an obvious pore at one end (Fig. 10A). These papillae may be developmentally modified or neotenous hooks (i.e., an intermediate stage in the development of the sympatric S. australe-type hooks). More data are needed to determine if these specimens do indeed represent a biological species. DISTRIBUTION. Natal, South Africa. Siphonosoma funafuti (Shipley, 1898) Sipunculus funafuti Shipley, 1898:469. Siphonosoma funafuti.—E. Cutler and Cutler, 1982:756. Siphonosoma (Siphonsoma) funafuti.—Stephen and Edmonds, 1972:65-66. Sipunculus amamiensis Ikeda, 1904:36-38. Siphonosoma amamiense.— Sato, 1939:371.-Stephen and Edmonds, i972:59-6o.-E. Cutler and Cutler, 1981:57-58; 1982:753. DESCRIPTION. The few worms on which this taxon is based are between 18 and 120 mm long, lack hooks, have thin body walls, and are rather fragile. The contractile vessel is without villi but may show vesicular swellings. The dorsal retractors are thinner than the ventrals, and there are 14-20 infrequently anastomosing LMBs. DISTRIBUTION. Southern Japanese islands and Funafuti. Siphonosoma ingens (Fisher, 1947) Siphonomecus ingens Fisher, 1947:365-368. Siphonosoma ingens.— Fisher, i952:382-385.-E. Cutler and Cutler, 1982:756. Siphonosoma (Siphonsoma) ingens.—Stephen and Edmonds, 1972:66. DESCRIPTION. Animals belonging to this species have fusiform bodies

54

The Sipunculids

and contractile vessel villi but lack introvert hooks. They are very similar to the Japanese S. mourense except for the presence of the two to six fusiform bodies (Fig. 12), spindle-shaped cylinders which may be 5 by 0.35 mm and open via a small pore through the posterior tip of the trunk (see Chap. 12 for further details). Histological examinations of these peculiar secretory structures suggest a pheromone-producing or excretory function (E. Cutler and DiMichele, 1982; and below). DISTRIBUTION. California. Siphonosoma mourense Sato, 1930 Siphonosoma mourense Sato, i930:6-8.-E. Cutler and Cutler, 1982:757.E. Cutler et al., 1984:260. Siphonosoma (Siphonosoma) mourense.— Stephen and Edmonds, 1972:67-68. DESCRIPTION. These hookless worms have trunks up to 350 mm long, contractile vessels with villi, and 20-25 LMBs. Although these animals are similar to the common S. cumanense in many respects, their ventral retractor muscles originate posterior to the dorsal pair. Siphonosoma mourense is also similar to S. ingens (these two could be western and eastern Pacific subspecies), but the latter has easily overlooked fusiform bodies inside the posterior end of the trunk. DISTRIBUTION. Northeast Honshu, Japan. Siphonosoma rotumanum (Shipley, 1898) Sipunculus rotumanus Shipley, 1898:469-470. Siphonosoma rotumanum. —Edmonds, 1971:143-144; 1980-.18.-E. Cutler and Christie, 1974: 109-110.-E. Cutler and Cutler, 1982:758-759.-Haldar, 1991:27-28. Siphonosoma (Siphonosoma) rotumanum.—Stephen and Edmonds, 1972:71. Siphonosoma enixvetoki Fisher, T95ob:8o5-8o8. Siphonosoma (Siphonosoma) eniwetoki.—Stephen and Edmonds, 1972:65. Siphonosoma hawaiense Edmonds, 1966^386-388. DESCRIPTION. The distinctive introvert hooks (100-200 (im tall) are closely associated with large papillae (Fig. 10C). When the skin is stretched, as in an expanded worm, the height of the papillae decreases. The sharpness of the hook appears to vary depending on the angle at which it is viewed. The contractile vessel villi are digitiform or clavate but distinct, even when small, and may be present only along the free part of the esophagus.

Genus Siphonomecus

55

Infrequent in the Indo-West Pacific from Cape Province, South Africa; Andhra Pradesh, India; Queensland, Australia; and a few islands east to Hawaii in shallow sandy habitats. DISTRIBUTION.

Siphonosoma vastum (Selenka and Biilow, 1883) Sipunculus vastus Selenka and Biilow, in Selenka et al., 1883:103-104. Siphonosoma vastum.—Wesenberg-Lund, i937a:2-5.-Edmonds, 1980: 15-16.-E. Cutler and Cutler, 1982:752-753.-Haldar, 1991:28-30. Siphonosoma (Hesperosiphon) vastum.—Stephen and Edmonds, 1972:55-57.-Murina, I98ib:i2. Sipunculus (Phascolosomum) violaceus de Quatrefages 1865^619. Phascolosoma violaceum Baird, 1868:85. Sipunculus violaceus Stephen and Edmonds I972:339.-Saiz 19843:202. Siphonosoma crassum Spengel, in Fischer, 19193:279. Siphonosoma parvum W. Fischer, 1928:141-143. Siphonosoma (Hesperosiphon) parvum.—Stephen and Edmonds, 1972:54-55. DESCRIPTION. The most striking feature of this species is the cluster of caecae on the rectum (Fig. 11), not to be mistaken for contractile vessel villi, which this species lacks. Otherwise it superficially resembles other small (50-100 mm) members of this genus. The introvert bears dark, claw-shaped hooks in rings and is longer than in many species (50-90% of the trunk length). DISTRIBUTION. Widespread in Indo-West Pacific tropical and subtropical waters as far north as Miyakijima, Japan. Recent collections from the Pacific coast of Costa Rica illustrate its ability to bridge the Eastern Pacific Barrier (N. Cutler et al., 1992).

Genus Siphonomecus Fisher, 1947 Siphonomecus Fisher, 1947:363.-Stephen and Edmonds, 1972:73.-E. Cutler, 1986:490. DIAGNOSIS. Introvert shorter than trunk with prominent hooks and conical papillae arranged in rings. Body wall with coelomic extensions (sacs); circular and longitudinal muscle layers gathered into anastomosing bands. Tentacles arranged around mouth. Two introvert retractor muscles. Contractile vessel without villi. Spindle muscle attached posteriorly. Two nephridia. Single species (Figs. 3 and 13). TYPE SPECIES. Siphonomecus multicinctus Fisher, 1947.

56

The Sipunculids

A B Figure 13. Siphonomecus multicinctus. A. Whole animal. B. Internal anatomy, showing small area of longitudinal and circular muscle bands. Abbreviations as in Figure 1. (After Fisher, 1947, courtesy of Smithsonian Institution Press.)

Siphonomecus multicinctus Fisher, 1947. Siphonomecus multicinctus Fisher, 1947:363-365.-E. Cutler, 1973:130; 1986:490. an_ DESCRIPTION. These large worms (up to 500 mm) have 16-23 astomosing LMBs and short oblique muscle strands between the longitudinal and circular layers. The trunk surface is often annulated, the external depressions located in the middle of each CMB. Internal pores open into a unique canal system within the body wall consisting of a vestibule from which extend three or four short, small, parallel, longitudinal minicanals. Each canal system goes laterally from the center of one LMB to center of its neighbor, and similarly from center to center of each pair of CMBs (E. Cutler, 1986). The introvert is about half the trunk length.

Genus Phascolopsis

57

DISTRIBUTION. Southeastern United States, Florida to South Carolina, shallow subtidal to 500 m.

Genus Phascolopsis (Fisher, 1950) Golfingia (Phascolopsis) Fisher, 19503:550. Phascolopsis.—Stephen, I964:459.-Stephen and Edmonds, I972:74.-E. Cutler, 1986:460. DIAGNOSIS. Introvert shorter than trunk, with small deciduous hooks present in juveniles but lost in adults. Body wall without coelomic extensions. Circular muscle layer continuous; longitudinal muscle layer gathered into anastomosing bands. Tentacles arranged around mouth, no nuchal tentacles. Four introvert retractor muscles. Contractile vessel without villi. Spindle muscle not attached posteriorly. Two nephridia. Single species (Figs. 3 and 14). TYPE SPECIES. Sipunculus gouldii Portal6s, 1851. Phascolopsis gouldii (Portales, 1851) Sipunculus gouldii Portales, 185140-4i.-Selenka et al., 1883:101-102. Phascolosomum gouldii.—Diesing, 1859:764-765. Phascolosoma gouldii.—Keferstein, i865a:434.-Andrews, i89ob:389-420.-Gerould, 1913: 380. Golfingia (Phascolopsis) gouldii.—Fisher, 19503:550. Phascolopsis gouldii.—Stephen, I965:459.-Stephen and Edmonds, I972:74.-E. Cutler, 1973:130-132; I977b:5.-Frank, 1983:10. DESCRIPTION. A slender, smooth, light brown worm (with skin bodies but no distinct papillae). The trunk may be up to 150 mm long but is more commonly 50-100 mm. The introvert is about one-third the trunk length, tipped with many peripheral tentacles (see Andrews, 1890b), and has no hooks after the worm reaches 3-4 cm long. The few hooks that are present in very young worms are 20-30 u,m tall, widely dispersed, and in illdefined rings (Fig. 14C). Distinct rings of small papillae are present on the distal part of the introvert. The 26-40 LMBs frequently anastomose. All four retractor muscles originate in the anterior half of the trunk, but the dorsal pair is anterior to the larger ventral pair (Fig. 14B). The two nephridia are unattached and open slightly anterior to the anus. This species has served the biological community for many years as a teaching and research resource. The changing generic appellation (three

Figure 14. Phascolopsis gouldii. A. External view (worms often appear smoother or have a less pointed posterior end). B. Interior organs, anastomosing longitudinal muscle bands not shown (see Figure 3; abbreviations as in Figure 1). C. Introvert hooks, from young worm, 20-30 u,m tall.

Genus Phascolopsis

59

names since 1950) has caused minor confusion for biological supply houses, experimental biologists, and biochemists. Specimens recently located in the Museum of Comparative Zoology, Harvard, appear to be the previously unacknowledged type material. DISTRIBUTION. The Atlantic coast of North America from Florida to Nova Scotia, rare south of Long Island (no sexually mature specimens recorded south of Cape Hatteras); from the low-tide line to shallow subtidal depths.

3

The Golfingiids

Order Golfingiiformes E. Cutler and Gibbs, 1985 Golfingiaformes E. Cutler and Gibbs, 1985:166. Golfingiiformes Gibbs and Cutler, 1987:50. Sipunculidea with body wall longitudinal muscle in a continuous layer, not gathered into bands. Family Golfingiidae Stephen and Edmonds, 1972 Golfingiiformes with two nephridia. Tentacles not on stemlike extensions of oral disk. Members of this family are commonly found in cold water and as infauna in fine sands or mixtures of sand, silt, and clay. Very few species exceed 30 mm in length. Familial Traits Body Wall. In general, the body is smooth despite the presence of papillae, which are usually small in both diameter and height (the few exceptions include Nephasoma flagriferum, which has very large posterior papillae). In worms more than 2 cm long, the body wall is opaque (often white or yellowish), but in smaller worms one can often see the internal organs through the transparent body wall. Tentacles. These are discussed under each genus. They vary too much to generalize about here, except to say that when present, they surround the mouth in a close-set array of digitiform or leaflike, unbranching units. Internal Anatomy. There is little to comment on aside from what has been said above for the class. The paired nephridia separate this family from the Phascolionidae, one of the other two families in this order. The

Genus Golfingia

61

contractile vessel is simple in two of the three genera but exhibits numerous villi in Thysanocardia. The full complement of two pairs of introvert retractor muscles is present in Golfingia, but the dorsal pair is absent in the other two genera. Key to Golfingiidae Genera i. Contractile vessel with numerous villi

Thysanocardia

- Contractile vessel without villi

2

2. Four introvert retractor muscles

Golfingia

- Two introvert retractor muscles

Nephasoma

Genus Golfingia Lankester, 1885 Golfingia Lankester, i885a:469~47i. Golfingia (Golfingia) Fisher, 1950a: 549. Golfingia (Dushana) Murina, 1975c: 1085. Themiste (Stephensonum) Edmonds, 1980:33. Centrosiphon Shipley, 1903:173.-Edmonds, 1980:19. DIAGNOSIS. Introvert about equal to or shorter than trunk. Hooks, when present, usually scattered (arranged in rings in G. elongata). Body wall with continuous muscle layers. Tentacles arranged around mouth. Four introvert retractor muscles. Contractile vessel without villi. Spindle muscle not attached posteriorly. Two nephridia. Worms small to medium sized. See Figures 15-18. TYPE SPECIES. Golfingia macintoshii Lankester, 1885a (= Sipunculus vulgaris sensu de Blainville, 1827). NOMENCLATURAL NOTE. This taxon traces its origins back to a golf outing on the greens of nineteenth-century St. Andrews: "And I have accordingly ventured to dedicate the new genus of Sipunculid worms indicated by this specimen to the local goddess whose cult is historically associated with the most ancient of Scottish seats of learning" (Lankester i885a:469). Subsequent confusion about the proper use of this name and the genus name Phascolosoma continued until 1950 when Fisher corrected the situation. The subgeneric names Golfingiella Stephen, 1964, and Siphonoides

62

The Golfingiids

Figure 15. Golfmgia external forms. A. G. margaritacea. B. G. iniqua (after Southern, 1913). C. G. elongata. D. Distal introvert of G. elongata with hooks in rings (from Th6el, 1905).

Murina, 1967c, used by Stephen and Edmonds (1972) have been declared void by E. Cutler et al. (1983) and thus are not used herein. Morphological Characters of Golfmgia Introvert Hooks. Most species have small (20-40 pjn), scattered, pale hooks. Two species have large (150-300 (xm), slender, spinelike hooks (G. birsteini and G. mirabilis). Between these two extremes are G. muricaudata (50-150 \xm in small worms) and G. vulgaris (dark hooks generally 50-120 |xm tall; see Fig. 17A). Saiz (1986b) reported hooks ranging from 20 to 275 (Jim in this species, and Edmonds (1956) reported hooks 120-200 |xm in his variety queenslandensis = G. vulgaris herdmani. Two species have hooks in rings: G. elongata (45-100 \im) and G. (Spinata) pectinatoides (25-30 |xm). The hooks of the latter are distinctive because

Genus Golfingia

63

Figure 16. Internal structures of the two Golfingia subgenera. A. G. (Golfingia) margaritacea, dissecting pin holding left dorsal retractor aside to expose nephridium (after Th6el, 1905); B. G. (Spinata) pectinatoides with bilobed nephridia (after E. Cutler and Cutler, 1979a, courtesy of the Museum National d'Histoire Naturelle). Abbreviations as in Figure 1.

they have a small comb of basal spinelets like those of Apionsoma species. Several species are known to have deciduous hooks, and this character is probably common within the Golfingia, The few reports of species entirely lacking hooks were based on individuals more than 10 mm long, and hooks probably were present in earlier stages of their development. The only hookless species in the present construct is G. anderssoni, but the

64

The Golfingiids

smallest specimen recorded has a 25-mm trunk, and younger individuals may have hooks. Tentacles. A series of digitate circumoral tentacles whose number and complexity increase with age is the rule in this genus (Fig. 17C-E; see also Theel, 1905^1. 14, figs. 192-195; or Gibbs, 1977b). Adult specimens commonly have 16-40 tentacles. The one exception is G. birsteini, which has 8-10 very short tentacles. In other species the number may exceed 40 in large worms (>ioo mm). The tentacular crown in G. (Spinata) pectinatoides may be unique (it has neither the standard circumoral array nor nuchal tentacles), but the small size and partially retracted state of the specimens preclude a definitive description. Caudal Appendage. In most species the posterior end of the trunk is bluntly rounded, although it may form a pencil point (Fig. 18). Two species (G. anderssoni and G. muricaudata) exhibit a distinct caudal appendage (tail) of variable length that is rudimentary in small worms (Fig. 18E). If the worm is damaged or less than 5 mm long, one can be misled by the absence of a tail. Trunk Length-to-Width Ratio. In most species the trunk is cylindrical and the length exceeds the diameter by 5-10 times. Trunks are very elastic muscular sacs, and selective contraction and relaxation of the circular and longitudinal muscle layers can greatly modify their proportions; thus these measurements should not be used alone as a distinguishing character. G. birsteini, however, is very elongated, with a trunk 15-20 times longer than wide. G. elongata has been reported to have similar proportions, but many individuals are less elongate. G. iniqua is almost always plump and stout with a length only about 3 times its diameter. Introvert Length. In most Golfingia species the introvert is 65-100% of the trunk length. G. (Spinata) pectinatoides has a significantly longer introvert (up to 200%). This character is not useful for differentiating species within subgenera. Papillae. The density, shape, and degree to which these protrude above the surface are extremely variable. In almost all species papillae are more numerous on the anterior and posterior 10-20% of the trunk. They are

Genus Golfingia

65

Figure 17. Golfingia hooks and tentacles. A. G. vulgaris, height 50-150 u,m (after Th6el, 1905). B. G. (Spinata) pectinatoides, height 25-30 u,m (from E. Cutler and Cutler, 1979a, courtesy of the Mus6um National d'Histoire Naturelle). C-E. G. margaritacea tentacles in small to large worms (from Th6el, 1905).

especially well developed on G. vulgaris and are quite large on the posterior end of G. anderssoni. Spindle Muscle. The origin of this muscle is either on the body wall anterior to the anus, as in G. (Spinata), or on the wall of the rectum, wing muscle, or a small flap of tissue just under it, as in G. (Golfingia). It terminates posteriorly within the gut coil. Retractor Muscles. The most common condition in Golfingia is for the ventral pair of retractor muscles to originate in the middle third (35-65% of the distance to the posterior end) of the trunk, and the dorsal pair to have more anterior origins (10-20%). Two apparent exceptions to this are some large G. muricaudata and the long, slender G. birsteini, in which the ventrals originate about 20% of the distance along the trunk. Other exceptions to this rule are G. mirabilis and G. (Spinata) pectinatoides, in which the dorsal origins are posterior to the ventrals, and both origins are in the anterior quarter.

66

The Golfingiids

Figure 18. Golfingia posterior trunk shapes. A-D. Four individuals from one population of G. margaritacea ohlini showing possible variations (after E. Cutler and Cutler, 1987a, courtesy of the Biological Society of Washington). E. G. muricaudata caudal appendage (from Murina, 1964b). F. G. vulgaris herdmani pseudoshield (from Edmonds, 1980, courtesy of S. J. Edmonds, South Australian Museum).

Key to Golfingia

Subgenera and Species

1. Nephridia bilobed; both pairs of retractors originate close to ventral nerve cord (Fig. 16B); hooks with basal spinelets G. (Spinata) pectinatoides - Nephridia unilobed; anterior retractors dorsolaterally displaced (Fig. 16A); hooks (if present) without basal spinelets subgenus Golfingia s. s., 2 2. Caudal appendage present

3

- Caudal appendage not present

4

3. Large bladderlike papillae at base of caudal appendage

G. anderssoni

- Base of caudal appendage with papillae, but not large and bladderlike . . . G. muricaudata

Genus Golfingia

67

4. Introvert hooks in rings (Fig. 15D)

G. elongata

- Introvert hooks scattered, if present

5

5. Anterior and posterior ends of trunk dark and coarsely papillated

6

- Ends of trunk not distinctly different in color or texture

7

6. Ventral retractor muscles originate posterior to dorsal pair G. vulgaris (two subspecies) - Ventral retractor muscles originate anterior to dorsal pair 7. Trunk length less than three times the width

G. mirabilis G. iniqua

- Trunk length more than three times the width 8. Reduced tentacles; large hooks (>i5o |i,m)

8 G. birsteini

- Normal tentacles; hooks small, if present (2000 m). The depth range is 1-5300 m, but most specimens have been collected from depths less than 300 m. The species is unknown from the Indian Ocean and Mediterranean Sea. Golfingia margaritacea ohlini (Theel, 1911) Phascolosoma ohlini Theel, 1911:29-30. Golfingia ohlini.—WesenbergLund, 1955a:io.-Stephen and Edmonds, 1972:102.-E. Cutler and Cutler, 1980c: 199. Golfingia margaritacea ohlini.—E. Cutler and Cutler, 19873:746. Phascolosoma pudicum Selenka, 1885:11-12. Golfingia pudica.—Stephen and Edmonds, 1972:104-105.-E. Cutler et al., 1983:671-672. Phascolosoma mawsoni Benham, 1922:13-17.-Stephen, 1948:218. Golfingia mawsoni.—Stephen and Edmonds, 1972:99-100. Golfingia vulgaris [sic] van antarctica Murina, 1957^996-997. Golfingia vulgaris murinae.—Stephen and Edmonds, 1972:111. DESCRIPTION. In morphological characters this taxon grades into G. margaritacea margaritacea. Two indistinct differences from that subspecies are the presence of hooks in some G. m. ohlini and the shape of the posterior end (pointed, not rounded). Hooks are present only in smaller animals (50 well-defined units). The ventral retractor muscles originate anterior to the origins of the dorsal pair by about 10% of the trunk length, a character unique to this species among the Golfingia. This specimen may be an anomalous G. vulgaris, and the validity of this taxon might be challenged. 0 DISTRIBUTION. Off Tanzania, 7 S, 40° E, at 800 m.

Golfingia muricaudata (Southern, 1913) Phascolosoma muricaudatum Southern, 1913:21. Golfingia muricaudata. —Murina, I964b:233~237.-E. Cutler, I973:i33-I34.-E. Cutler and Cutler, 1980^198-199; 19873:752.-E. Cutler et al., 1984:265-266.Saiz, i993:5i-53Phascolosoma hudsonianum Chamberlin, i92ob:3d-4d. Golfingia hudsoniana.—Stephen and Edmonds, 1972:91-92. Phascolosoma appendiculatum Sato, 19343:7-10. Golfingia appendiculata.—Stephen and Edmonds, I972:86.-E. Cutler et al., 1984:262. DESCRIPTION. This common deep-water species, which may be up to 70 mm long (most are 50 mm long; large, very dark papillae; hooks >50 |xm tall N. schuettei - Worms usually 50) of thin, threadlike tentacles. Although this taxon is similar to N. eremita, its geographic separation and large size support its separate status. The type was collected from the stomach of a dogfish shark. DISTRIBUTION. Off New Zealand and the Chatham Islands, from 65-70 m. Nephasoma pellucidum pellucidum (Keferstein, 1865) Phascolosoma pellucidum Keferstein, i865b:433.-Baird, i868:86.-Selenka et al., 1883:32-34. Sipunculus (Phascolosomum) pellucidus de Quatrefages, i865b:620. Golfingia pellucida.—Murina, 19683:421-

Genus Nephasoma

99

422.-Stephen and Edmonds, 1972:152-153.-E. Cutler, 1973:159-162; 1977a: 152.-E. Cutler and Cutler, 1979b: 105.-E. Cutler et al., 1984: 270.-Haldar, 1991:33-35. Nephasoma pellucidum pellucidum.—N. Cutler and Cutler, 1986:563. Phascolosoma riisei Keferstein, 1865^437.-Baird, 1868:96. Phascolosoma cinereum Gerould, 1913:396-398. Golfingia cinerea.— Stephen and Edmonds, 1972:138. Phascolosoma verrillii Gerould, 1908:488-489; 1913:388-391. Golfingia verrillii.—Murina, I964b:243~246.-Stephen and Edmonds, 1972:158. Phascolosoma sluiteri ten Broeke, 1925:84-86. Golfingia sluiteri.— Stephen and Edmonds, 1972:156-157.-E. Cutler and Murina, 1977: 177. Golfingia coriacea.—Fisher, 19503:551; 1952:396. Golfingia eremita van australe.—Wesenberg-Lund, 19593:181-182. DESCRIPTION. This species, whose members bear large, dark, uniformly distributed papillae that are not obvious in worms less than 5 mm long, is well founded and widely distributed. The trunk is translucent, cream or pale tan, rarely brown or gray, and measures up to 25 mm (more commonly 5-10 mm long; Fig. 19B). Haldar's two worms, measuring 80 and 86 mm, may be a separate Indian Ocean subspecies. The introvert carries 2030 tentacles (12-16 in small worms and 60 in the very large ones) and a zone of scattered hooks, which decrease in larger worms. The nephridia open at the level of the anus and are otherwise unattached. Pigmented eyespots are usually apparent on the brain. DISTRIBUTION. A shallow-water species, with a few bathyal records, from the western Atlantic and Caribbean south to Brazil. In the South Pacific and Indian oceans from Indonesia and Australia, southern Japan, and one record each from Cape Province and India. Nephasoma pellucidum subhamatum (Sluiter, 1902) Phascolosoma subhamatum Sluiter, 1902:35-36. Golfingia subhamata.— Stephen and Edmonds, 1972-.157.-E. Cutler et al., 1984:270-271. Nephasoma pellucidum subhamatum N. Cutler and Cutler, 1986:564. DESCRIPTION. The hooks in this form are larger (100 vs. 60 \xxa in the nominate form) and thinner. The worm is pear shaped to cylindrical, up to 20 mm long, with the introvert longer than the trunk. There may be transverse grooves around the posterior end, and both ends are dark and rough, covered with dense papillae.

IOO

The Golfingiids

DISTRIBUTION. This species differs from the nominate form in being a bathyal western Pacific population (not in shallow, warm water). From Malaya and Suruga Bay off Honshu, Japan, at 440-2050 m.

Nephasoma rimicola (Gibbs, 1973) Golfingia rimicola Gibbs, 1973:74-80; 1977b:i8.-Saiz, 1986^54-56. Nephasoma rimicola.—N. Cutler and Cutler, I986:564.-Saiz and Villafranca, i99o:ii58-n6o.-Saiz, 1993:72-74. DESCRIPTION. The hooks, arranged in distinct rings, differentiate this from species such as the very similar N. minutum. It is the only species in the genus with such a hook array (as is Golfingia elongata in its genus). The anus is posterior to the nephridiopores and it has distinct tentacles, while N. minutum has the opposite arrangement. DISTRIBUTION. Southwestern England and northern Spain in intertidal waters. Recent records show it to be in deeper water (350-720 m) off southern Spain. Nephasoma schuettei (Augener, 1903) Phascolosoma schuttei Augener, 1903:335-337. Golfingia schuettei.— Stephen and Edmonds, i972:i56.-Edmonds, 1980:25-27. Nephasoma schuttei.—N. Cutler and Cutler, 1986:564. NOTE. This name was misapplied by Murina and Cutler, who used it for a small, common, deep-water species (see N. diaphanes). Edmonds's material and excellent description are correctly based on Augener's species. The previous spelling of the species name by Cutler is corrected here. DESCRIPTION. The large, dark papillae and coarse skin of this light to golden brown worm are distinctive. It is one of the larger Nephasoma (up to 160 mm), with an introvert much shorter than the trunk (one-sixth to one-third the size) and tipped by a complex array of digitiform tentacles. The sharp hooks are larger distally, decreasing in size proximally. A welldeveloped wing muscle and a spindle muscle with two anterior roots are present. Edmonds, 1980, gives a detailed description and discusses the differences from and similarities to N. pellucidum. DISTRIBUTION. Southern and western Australian intertidal water. Nephasoma tasmaniense (Murina, 1964) Golfingia tasmaniensis Murina, i964b:242-243.-Stephen and Edmonds, 1972:157. Nephasoma tasmaniense.—N. Cutler and Cutler, 1986:565.

Genus Nephasoma

101

DESCRIPTION. Small, pale hooks and a few reduced tentacles are present on the swollen, bulblike terminus of the short introvert (less than half the trunk length). The anterior of the trunk is conical with a "collar" at the base of the cone (total trunk length is 18 mm in one complete specimen). The trunk-introvert junction is constricted into a narrow neck (Fig. 23C). In general size, shape, looseness of gut coil, constricted neck, and introvert characteristics, N. tasmaniense resembles N. constricticervix. The hooks are much smaller in this species, however, and the collar at the base of the anterior cone may be diagnostic. A fuller description based on a larger sample size is needed as this is not a well-established species. DISTRIBUTION. Tasman Sea, at 1330 m.

Nephasoma vitjazi (Murina, 1964) Golfingia vitjazi Murina, i964b:246-248.-Stephen and Edmonds, 1972: 158. Nephasoma vitjazi.—N. Cutler and Cutler, 1986:565. DESCRIPTION. The single specimen, 15 by 0.1 mm, is fragile and incomplete (the posterior end is missing). The anterior end of the trunk has 3035 parallel, longitudinal ridges radiating out from the introvert base forming a pseudoshield, and the 4-mm introvert bears large hooks (210-280 (xm). As with N. tasmaniense, a larger sample size would allow a more complete description. DISTRIBUTION. Northwestern Pacific Ocean, at 4150 m. Nephasoma wodjanizkii wodjanizkii (Murina, 1973) Golfingia wodjanizkii Murina, 1973^944-945; I973a:70.-Frank, 1983: 18-19. Nephasoma wodjanizkii wodjanizkii.—N. Cutler and Cutler, 1986:566. Golfingia nicolasi Thompson, 1980:951-956. DESCRIPTION. A very slender bathyal species. The nephridia are posterior to the anus, and the retractor muscles originate in the posterior one fifth of the trunk. In very young animals the introvert is shorter than the trunk. It measures two to three times the trunk length in mature worms, however, and in some populations may be six to seven times as long when completely extended (Fig. 19C). This pattern is the opposite of what one sees in most sipunculans (i.e., a relative shortening of the introvert with age). Small hooks (20-25 M-nO m a v be present or absent, and the reduced tentacles are few. Trunk lengths of the original two N. w. wodjanizkii specimens are 4 and 6 mm, but the more recently described California

The Golfingiids

102

population (Thompson, 1980b) consists of several hundred specimens with trunks ranging in size from 7 to 36 mm. The introvert and the anterior part of the trunk exhibit a series of longitudinally arranged fine brown lines or ridges in the epidermis. DISTRIBUTION. A bathyal species (1000-2400 m) from three widely separated Pacific Ocean localities: the Sea of Okhotsk, the Peru-Chile Trench, and southern California.

Nephasoma wodjanizkii elisae (Murina, 1977) Golfingia elisae Murina, 1977b: 133-134. Nephasoma elisae.—Gibbs, 1986:338-339. Nephasoma wodjanizkii elisae.—N. Cutler and Cutler, I986:566.-Saiz, 1993:66-68. DESCRIPTION. Deciduous hooks and an anterior pseudoshield of 25-30 longitudinal ridges are present. The transparent trunk may measure up to 48 by 2 mm and contain an intestinal spiral that is loosely wound in the posterior half. The differences from the nominate form center on the shorter introvert length (less than twice the trunk length) and the disjunct distribution (Atlantic vs. Pacific Ocean). DISTRIBUTION. An eastern Atlantic bathyal species; collected from the Gulf of Guinea at 1500 m, and from 43-58 0 N at 1600-2300 m.

Genus Thysanocardia (Fisher, 1950) Golfingia (Thysanocardia), Fisher, 19503:551-552; Stephen and Edmonds, 1972:120. Thysanocardia Gibbs et al., 1983:295. DIAGNOSIS. Introvert longer than trunk, without hooks. Body wall with continuous muscle layers. Well-developed tentacles arranged around mouth and enclosing nuchal organ. Two introvert retractor muscles. Contractile vessel with distinct villi. Spindle muscle not attached posteriorly. Two nephridia open anterior to anus. Species small to medium sized, adult trunk length generally less than 50 mm. TYPE SPECIES. Phascolosoma procerum Mobius, 1875. NOMENCLATURAL NOTE. Thysanocardia was erected as a subgenus when Fisher (1950a) resurrected the generic name Golfingia Lankester. The subgenus was elevated to generic rank and the number of species reduced from eleven to three in Gibbs et al., 1983. See Figure 25.

Genus Thysanocardia

103

Morphological Characters of Thysanocardia Tentacular Crown. The distal tip of the introvert must be examined for positive identification. While the crown is quite evident in an extended introvert (Fig. 25B, C), the necessary information can also be obtained from a retracted introvert through careful dissection. The form of the dorsal nuchal organ is distinct, and the pigmentation on the tentacles of T nigra is not hard to see.

Key to Thysanocardia Species 1. Nuchal organ consists of two oval lobes; small (trunk < i 5 mm); northeastern Atlantic T. procera - Nuchal organ a single lanceolate lobe; adults >I5 mm 2. Tentacular crown without dark pigment - Tentacular crown with dark pigment

2 T. catharinae T. nigra

Thysanocardia catharinae (Griibe, 1868) Phascolosoma catharinae Griibe, i868a:48.-Selenka et al., 1883:38-39. Golfingia catharinae.—Wesenberg-Lund, 1959a:i83.-Stephen and Edmonds, I972:i22.-E. Cutler, I973:i46-I50.-E. Cutler and Cutler, 1979b: 104. Thysanocardia catharinae.—Gibbs et al., 1983:298. Phascolosoma semperi Selenka and de Man, in Selenka et al., 1883:3738. Golfingia (Thysanocardia) semperi.—Stephen and Edmonds, 1972: i30.-Gibbs et al., 1983:298. Phascolosoma martensi Collin, 1901:302-304. Golfingia (Thysanocardia) martensi.—Stephen and Edmonds, I972:i27.-Gibbs et al., 1983:298. Phascolosoma procera.—Gerould, 1913:303. DESCRIPTION. Cylindrical trunk up to 70 mm, gray to white, with zigzag wrinkles in the skin usually visible (Fig. 25A). The trunk tapers at the posterior end, and the introvert can be up to twice the trunk length. In large specimens the tentacular array consists of 14-16 festoons, each with about 40 unpigmented tentacles, plus 15-20 tentacles encircling the lanceolate nuchal organ (Fig. 25B, C). Two strong retractor muscles originate in the trunk about 75-85% of the distance toward the posterior end. The size and complexity of the contractile vessel villi increase with the size of the worm.

Genus Thysanocardia

105

DISTRIBUTION. Northwestern and South Atlantic, East Africa, and Peru, along the outer shelf and upper slope (50-700 m). The 15 Vietnam worms (Murina, 1989) may well be a new species, possibly part of the same taxon referred to as Thysanocardia species in E. Cutler et al., 1984.

Thysanocardia nigra (Ikeda, 1904) Phascolosoma nigrum Ikeda, 1904:3. Golfingia nigra.—Stephen and Edmonds, I972:i27-I28.-E. Cutler and Cutler, 1981:68. Thysanocardia nigra.—Gibbs et al., 1983:298-300. Phascolosoma pavlenkoi Ostroumov, 1909:323. Golfingia pavlenkoi.— Stephen and Edmonds, 1972:152. Phascolosoma zenibakense Ikeda, 1924:29-30. Golfingia zenibakensis.— Stephen and Edmonds, 1972:130-131. Phascolosoma hyugensis Sat6, 19343:12-13. Golfingia hyugensis.— Stephen and Edmonds, 1972:124. Phascolosoma onagawa Sato, 1937b: 156-158. Golfingia onagawa.— Stephen and Edmonds, 1972:128. Phascolosoma hozawai Sato, 1937^158-160. Golfingia hozawai.— Stephen and Edmonds, 1972:123. Golfingia pugettensis Fisher, I952:40i.-Stephen and Edmonds, 1972: I29-I30.-Rice, 1974:295. Golfingia macginitiei Fisher, i952:402-404.-Stephen and Edmonds, 1972:125. Golfingia catharinae.—E. Cutler, 19770:152. DESCRIPTION. The gray (rarely black) trunk is commonly 30-60 mm (range 5-100 mm), and the introvert is 1.5-2 times the trunk length. In large specimens the tentacular crown has about 24-26 festoons, each with 60 tentacles (1500 total), and a separate set of 30 small tentacles enclose the lanceolate nuchal organ (Fig. 25D). The tentacles have a violet mauve

Figure 25. Thysanocardia. A. T. catharinae, commonly gray with minute zigzag wrinkles in the skin (after E. Cutler, 1973, courtesy of the American Museum of Natural History). B. Tentacles of T. catharinae showing nuchal organ (NO). C. One festoon of peripheral tentacles and all nuchal tentacles. D. Tentacular crown of T. nigra showing slightly protruding esophagus. E. Internal organs of T. nigra. F. Segment of esophagus enlarged to show contractile vessel with villi. Abbreviations as in Figure 1. (B and D after Gibbs et al., 1983, © 1983, with permission of Pergamon Press Ltd., Headington Hill Hall, Oxford 0X3 oBW, UK; E and F after Fisher, 1952, courtesy of Smithsonian Institution Press.)

io6

The Golfingiids

pigment in most specimens, but this may fade to brown in preserved specimens. The color usually appears on each tentacle, either as a circular patch in small specimens or as a longitudinal band in larger worms. The retractor muscles originate 55-75% of the distance to the posterior end of the body (Fig. 25E). The longest and most branched contractile vessel villi are toward the posterior of the array (Fig. 25F). DISTRIBUTION. Northern California to Washington, central and northern Japan, Philippines, Indonesia, and Singapore from subtidal and shelf waters (1-120 m). Thysanocardia procera (Mobius, 1875) Phascolosoma procerum Mobius, 1875:157.-Theel, i905:70.-Southern, 1913:24-25. Golfingia procera.—Stephen and Edmonds, 1972:129.Gibbs, I977b:20. Thysanocardia procera.—Gibbs et al., 1983:298.Saiz and Villafranca, i990:ii6o.-Saiz, 1993:92-94. Golfingia catharinae.—Sluiter, I9i2:8.-Saiz, 1986^57. DESCRIPTION. These worms are the smallest in the genus. Ten-millimeter specimens can be sexually mature, and specimens longer than 15 mm are rare. The introvert is two to four times the trunk length. The finely wrinkled skin has minute papillae. The tentacle crown is relatively simple, commonly with only eight short festoons, each with 6-10 tentacles, plus 6-10 small tentacles surrounding the bilobed nuchal organ. In preserved material the tentacles are generally colorless, but in a few specimens a faint rust brown line is present on the oral surface of the tentacle. T. procera''s nuchal organ, with two oval lobes separated by a longitudinal groove, is unique. The two retractor muscles are fused for much of their length and originate in the posterior third of the trunk. DISTRIBUTION. From shelf and upper slope depths (2-550 m) in the northeastern Atlantic Ocean, the Skagerrak, and the North, Celtic, and Mediterranean seas.

4

The Phascolionids

Family Phascolionidae E. Cutler and Gibbs, 1985 Golfingiiformes with only one nephridium (usually the right). Tentacles are not borne on stemlike extensions of oral disk, and the gut coil lacks a well-defined axial spindle muscle. Phascolionids are typically found in subtidal cold water, and often within a protective shelter. The degree of asymmetry (body coiling, single nephridium, irregular gut coil, and retractor muscles) is higher in this family than in others. NOMENCLATURAL NOTE. It has been pointed out (by A. Zarazago, of Madrid, via J. Saiz, pers. comm., 1992) that the technically correct spelling of this family is Phascoliidae because the root for the genus Phascolion is phascoli, from the Greek for "little bag." I nevertheless choose to retain the original spelling, because all the other family names unambiguously communicate the dominant member genus. Without the on in the heart of this name the genus referenced would be less clear. Familial Traits Introvert Retractor Muscles. The "standard" array of two dorsal and two ventral muscles is rarely seen. In some worms the two dorsals appear to be fused into one larger muscle, and the two ventrals fuse into a thin muscle that may straddle the ventral nerve cord or be offset to one side. In some forms the dorsal and ventral muscles appear as a single column with just a hint of multiple units near the origins on the body wall. Anus Location. The anus is at the anterior end of the trunk in most Phascolion species. In four Phascolion and all the Onchnesoma, however, the anus opens on the introvert 20-95% of the distance toward the distal tip.

The Phascolionids

io8

Holdfast Papillae. Most Phascolion species have specialized epidermal papillae capable of producing a dark, horny protein shaped like a U, V, or broken O. These structures, which are distributed around the trunk, usually in the mid-region, are assumed to be devices that anchor the worm in its protective shelter. Key to Phascolionidae Genera i. Anus usually situated on anterior trunk; epidermal holdfasts or attachment papillae often present; retractor muscles highly fused but usually two to four origins apparent Phascolion - Anus situated on distal half of introvert; epidermal attachment papillae absent; retractor muscles appear as single column without separate origins Onchnesoma

Genus Phascolion Theel, 1875 Phascolion Theel, i875b:i3.-Selenka et al., i883:4i.-Stephen and Edmonds, 1972:164. DIAGNOSIS. Introvert one-half to four times trunk length, with or without hooks. Trunk usually with modified holdfast papillae. Body wall with continuous muscle layers. Tentacles arranged around mouth. Introvert retractor muscle system modified by fusion of dorsal and ventral pairs; relative size and degree of fusion define the subgenera. Contractile vessel generally without villi (present in P. cirratum). Gut coiling generally loose, without axial spindle muscle. One nephridium (usually right). Small to medium-sized worms (35 tentacles P. lucifugax 5. Hooks blunt, spinelike, 30-90 (jum P. hedraeum - Hooks broad based and recurved, 50-100 |xm P. convestitum Phascolion (homya) convestitum Sluiter, 1902 Phascolion convestitus Sluiter, 1902:32-33. Phascolion convestitum Stephen and Edmonds, 1972:175-176. Phascolion (Isomya) convestitum. —E. Cutler and Cutler, I98sa:825. Phascolion mediterraneum W. Fischer, i922a:20-22.-Stephen and Edmonds, 1972:181-182.-Saiz, 19860:45-47. Phascolion beklemischevi Murina, 19640:65-68.-Stephen and Edmonds, 1972:172. DESCRIPTION. The dorsal retractor muscle is sometimes slightly larger than the ventral muscle. The dorsal muscle has a single origin, and the ventral has two origins which straddle the ventral nerve cord near its posterior end. The esophagus may be connected to the dorsal, not ventral, retractor muscle. The holdfast papillae are unusually variable, from large and bulbous to small and compact; some have granular material around the border as disjunct units, others are without hardened material, and still others have a smooth, slightly darker border. About 20-25 normal tentacles are present, with broad-based, recurved, pointed hooks (50-100 \im; Fig. 30E). The gut is in loops with a few loose coils. There is a short, strong fixing muscle (but no spindle muscle) at the posterior end of the coil attaching it to the body wall between the roots of the ventral retractor. The similarities to P. tuberculosum are striking, and this taxon may not deserve specific rank. DISTRIBUTION. Mediterranean, Red Sea, Gulf of Aden, and Indonesia, from 25-275 m. Phascolion (Isomya) gerardi Rice, 1993 Phascolion (Isomya) gerardi Rice, 1993^591-594. DESCRIPTION. A small worm (trunk < i o mm) with no holdfasts and introvert up to three times the trunk length. The cylindrical to spherical

u8

The Phascolionids

trunk is covered by prominent mammillate or elongate papillae, which are largest around the introvert base. These large papillae may have up to three tips, similar to those found in some P. tuberculosum specimens. There are as many as 24 well-formed digitiform tentacles, and the nuchal organ appears as a corrugated band on the dorsal tip of the introvert at the base of the tentacles. The simple curved hooks are about 20 (xm tall. While not easily located unless the introvert is fully extended, the anus is midway along the introvert, unique in this subgenus. The two ventral and single dorsal retractor muscles originate on the body wall at the posterior end of the trunk. The opaque eggs are spherical and quite large, averaging 257 |xm in diameter. Given this egg size, this species may have direct development. DISTRIBUTION. Littoral waters of the Bahamas, Belize, and the Yucatan coast of Mexico, collected from preexisting spaces in coralline limestone. Phascolion (Isomya) hedraeum Selenka and de Man, 1883 Phascolion hedraeum Selenka and de Man, in Selenka et al., 1883:4950.-Stephen and Edmonds, I972:i77.-E. Cutler and Cutler, i98oa:2. Phascolion (Isomya) hedraeum.—E. Cutler and Cutler, 19853:827. Phascolion dentalicola Sato, 1937^165-167. Phascolion dentalicolum.— Stephen and Edmonds, I972:i72.-E. Cutler and Cutler, 1981:72.-E. Cutler et al., 1984:274. Phascolion kurchatovi Murina, i974a:233-234.-E. Cutler and Cutler, 1980c: 194. DESCRIPTION. Most of the specimens are less than 20 mm long, but worms may reach up to 35 mm. The holdfast papillae are round with hardened protein around the anterior margin of the larger ones (80-300 |xm diameter). Commonly this protein forms a thin, pale border (Fig. 29C, D), but a darker border is present in some Antarctic worms. This denser material occasionally extends around the whole margin of the papillae. The bluntly pointed, slightly bent, spinelike type I hooks are 30-90 |xm tall and similar to those of P. strombus. The two retractor muscles originate at the same level, posterior to the end of the ventral nerve cord at the end of the trunk. The dorsal retractor has a single origin; the ventral retractor may have one origin also but more often has two. The esophagus follows the ventral retractor, and the gut is a spiral plus one or two loops. 0 DISTRIBUTION. Several Southern Hemisphere records from 65 S north to South Africa, Uruguay, and Brazil in the Atlantic; in the southern

Genus Phascolion

119

Pacific, including the Great Australian Bight and Tasman Sea, and also off Japan. Generally at shelf and slope depths but ranging from 7 to 4610 m, in gastropod or scaphopod shells. Phascolion (Isomya) lucifugax Selenka and de Man, 1883 Phascolion lucifugax Selenka and de Man, in Selenka et al., 1883:43-44.Stephen and Edmonds, 1972:180. Phascolion (Isomya) lucifugax.—E. Cutler and Cutler, 19853:829. DESCRIPTION. The longest of the three worms on which this species is based is 40 mm, and the intestine has only loops, no coils. The esophagus, which carries a large vesicular contractile vessel, is attached to the ventral retractor. Both retractors have their origins about 15% of the distance from the posterior end of the trunk; the ventral origin is slightly divided and posterior to the dorsal. The type III medium-sized hooks (65-70 |xm) are blunt (Fig. 30I), and more than 30 long, slender tentacles are present. The holdfast papillae do not produce hardened protein borders. This taxon is similar to P. tuberculosum, but the differences in tentacle number, hook shape, and retractor origins are significant. DISTRIBUTION. Philippines and northern Japan at unknown depths, but probably shelf. Phascolion (Isomya) microspheroidis E. Cutler and Duffy, 1972 Phascolion microspheroidi E. Cutler and Duffy, 1972:71-76. Phascolion microspheroides.—E. Cutler and Cutler, 1980^456. Phascolion (Isomya) microspheroidis.—E. Cutler and Cutler, 19853:831. DESCRIPTION. Small (trunk usually < 5 mm), without hardened holdfast papillae and with small, pointed hooks (Fig. 30B). The pair of ventral retractors often remain unfused for about one-fourth their length (longer than in most species in the subgenus). This species has not been recorded outside the northwestern Atlantic Ocean. Animals from the Bay of Biscay and Mediterranean Sea reported by E. Cutler and Cutler (1980a) are now considered P. tuberculosum (E. Cutler and Cutler, 1985a). Very small P. tuberculosum ( < 3 mm) resemble P. microspheroidis in many ways, but the former has larger anterior papillae, and the hooks are distinctive. 0 DISTRIBUTION. Eastern coast of the United States from 31° N to 40 N at 500-1700 m.

120

The Phascolionids

Figure 32. Papillae on anterior end of trunk of P. tuberculosum showing variable number of tips with apical pores (scale = 200 u-m). (From E. Cutler and Cutler, 1985a, courtesy of the Biological Society of Washington.)

Phascolion (Isomya) tuberculosum Theel, 1875 Phascolion tuberculosum Theel, i875b:i5-i6.-Stephen and Edmonds, I972:i90.-E. Cutler and Cutler, 1980^456-457. Phascolion (Isomya) tuberculosum.—E. Cutler and Cutler, 19853:835.-Saiz and Villafranca, I990:i962.-Saiz, 1993:102-105. Tylosoma lytkenii Koren and Danielssen, 1875:134. Phascolion pallidum Koren and Danielssen, i877:i32-i34.-Stephen and Edmonds, 1972:184. Phascolion hirondellei Sluiter, i900:7-9.-Stephen and Edmonds, 1972: 178. Phascolion temporariae Edmonds, 1976:217-218. DESCRIPTION. This largest Phascolion (up to 50 mm) has characteristic large (70-220 p.m), broad, recurved type II hooks (Fig. 30F). In a i-mm specimen the hooks are pale and only 35 (Jim tall, but they still have the same shape. The large holdfast papillae (80-330 p,m) are spherical and lack hardened borders (Fig. 29A, B). Occasionally some granular material

Genus Phascolion

121

is visible along the anterior margin. The two retractor muscles originate near the posterior end of the trunk at nearly the same level. The ventral occasionally originates 1-2 mm anterior to the dorsal. These muscles occasionally differ from one another in diameter by 25%. The large mammiform papillae around the anterior end of the trunk usually have one protruding tip, but some have two and a few have up to four tips (Fig. 32). Commensal epizoans are common around the anterior end of the trunk. DISTRIBUTION. Common in the northeastern Atlantic, including the Azores, Mid-Atlantic Ridge, Bay of Biscay, and Scandinavian waters, at bathyal depths (25-2700 m). The few specimens from Japan and New Zealand from 93-300 m suggest a low-density population in the Pacific. These worms are more common in scaphopod than gastropod shells.

Subgenus Phascolion (Lesenka) Gibbs, 1985 DIAGNOSIS. Retractor muscles completely fused over whole length to give an entire retractor column. TYPE SPECIES. Phascolion cryptus Hendrix, 1975.

Key to Phascolion (Lesenka) Species 1. Hardened holdfast papillae present

2

- Hardened holdfast papillae absent

4

2. Four primary tentacles plus many accessory ones - More than 15 normal tentacles, no accessory tentacles 3. Holdfast papillae with pale U- or V-shaped protein borders

P. cryptum 3 P. valdiviae

- Holdfast papillae with one to four tall, strongly proteinized and collapsed teeth or points (Fig. 28G) P. collare 4. Anus on anterior end of trunk

P. rectum

- Anus on distal half of introvert

P. hupferi

Phascolion (Lesenka) collare Selenka and de Man, 1883 Phascolion collare Selenka and de Man, in Selenka et al., 1883:45-46.Stephen and Edmonds, i972:i73-i74.-Edmonds, 1980:29-30. Phascolion (Lesenka) collare.—E. Cutler and Cutler, 19853:825.

122

The Phascolionids

Phascolion tridens Selenka and de Man, in Selenka et al., 1883:46-47.Stephen and Edmonds, I972:i89.-E. Cutler, I977b:i53~i54. DESCRIPTION. Animals with blunt hooks and well-defined holdfast papillae with hardened borders. The hardening material sometimes takes an unusual form, similar to that seen in P. caupo, resulting in a tall cone having a long, pointed apex. In this species, each holdfast papilla usually has a single point, but a papilla may have two, three, or four points (Fig. 28G). The type III hooks (Fig. 30H) are small and usually blunt. The intestine consists of loose loops. DISTRIBUTION. Malaysian Archipelago, western Australia, eastern Africa, Brazil, and North Carolina from 5-2000 m. Phascolion (Lesenka) cryptum Hendrix, 1975 Phascolion cryptus Hendrix, 1975:127-133. Phascolion (Lesenka) cryptum.—E. Cutler and Cutler, 19853:826. DESCRIPTION. The array of auxiliary tentacles where hooks are normally found, the four primary tentacles, and the pale, V-shaped holdfast papillae are characteristic of this species (Figs. 26B, 31C). With introvert withdrawn, this form is externally similar to P. strombus, so an examination of the tip of the introvert, the retractor column, or both is essential. Ecologically this species is distinct from P. strombus, but its range does overlap that of P. caupo. DISTRIBUTION. Southeastern United States at 1-100 m. Phascolion (Lesenka) hupferi W. Fischer, 1895 Phascolion hupferi W. Fischer, 1895:16-17.-Stephen and Edmonds, 1972: 179. Phascolion (Lesenka) hupferi.—E. Cutler and Cutler, 1985a: 828. Phascolion indicus Murina, i974c:282-283.-E. Cutler et al., 1984:275. DESCRIPTION. The anus is located 50-75% of the distance toward the mouth on the long introvert (1.5-4 times the trunk length). Often more than 12 tentacles are present, but hooks have not been reported. A few worms exhibit two retractor origins as a small cleft at the base of an otherwise fused column. The origins are from the posterior end of the trunk. The trunk papillae are variable in shape and size, but holdfast papillae are absent. DISTRIBUTION. Japan, Java, and western Africa, from 10-1010 m.

Genus Phascolion

123

Phascolion (Lesenka) rectum Ikeda, 1904 Phascolion rectus Ikeda, 1904:15-18. Phascolion rectum.—Stephen and Edmonds, 1972:186-187.-E. Cutler and Cutler, I98i:74.-E. Cutler et al., 1984:277. Phascolion (Lesenka) rectum.—E. Cutler and Cutler, i985a:832. DESCRIPTION. These are small worms (most < i o mm, although specimens up to 20 mm are on record) with neither hooks nor holdfast papillae. The gut has loose loops and a short spiral. Fewer than 12 tentacles crown the introvert, which is about 1.5 times the trunk length. Except for the anus location on the anterior trunk, P. rectum is very similar to the sympatric P. hupferi, which has its anus on the introvert. DISTRIBUTION. Central Japan, at 30-2600 m. Phascolion (Lesenka) valdiviae valdiviae W. Fischer, 1916 Phascolion valdiviae W. Fischer, I9i6:i6.-Stephen and Edmonds, 1972: 191-193.-E. Cutler and Cutler, 19793:965; I985a:837. DESCRIPTION. The retractor muscles are almost entirely fused into a single column; occasionally this fusion is complete. Pale type I hooks (7090 |xm) are usually but not always present. This subspecies has holdfast papillae, mostly semicircular, with little hardened protein. DISTRIBUTION. St. Paul's Island and off Durban, South Africa, at 130150 m. Phascolion (Lesenka) valdiviae sumatrense W. Fischer, 1916 Phascolion valdiviae var. sumatrense W. Fischer, 1916:17. Phascolion (Lesenka) valdiviae sumatrense, E. Cutler and Cutler, 19853:837. Phascolion sumatrense W. Fischer, 1922b:I3-I4.-Stephen and Edmonds, 1972:191. Phascolion murrayi Stephen, I94ib:407.-Stephen and Edmonds, 1972: 183-184. DESCRIPTION. This subspecies differs from the nominate form in the following characters: it has variably U-shaped, V-shaped, or circular hardened holdfast papillae on the posterior half of the trunk, except for the most terminal 10%; larger animals apparently lack hooks; and it occurs in a different part of the Indian Ocean. DISTRIBUTION. Sumatra and Gulf of Aden at 750-1295 m.

The Phascolionids

124

Subgenus Phascolion (Montuga) Gibbs, 1985 DIAGNOSIS. Retractor column divided only at posterior end. Esophagus detaches from retractor column at a point anterior to first separation of the retractor muscles. TYPE SPECIES. Phascolion lutense Selenka, 1885.

Key to Phascolion (Montuga) Species 1. Hardened holdfast papillae present - Hardened holdfast papillae absent

P. pacificum P. lutense

Phascolion (Montuga) lutense Selenka, 1885 Phascolion lutense Selenka, i885:i6-i7.-Stephen and Edmonds, 1972: 180-181. Phascolion (Montuga) lutense.—Gibbs, 1985:315.-E. Cutler and Cutler, I985a:829.-Saiz, 1993:105-107. Phascolion canum E. Cutler and Cutler, 1980^454-456. Phascolion species E. Cutler and Cutler, 1980c: 197. DESCRIPTION. Most individuals have sparsely distributed, pale, type I hooks, 40-150 p,m tall (although some specimens lack hooks altogether). The retractor muscles are fused for much of their length, but one can see three, sometimes four, distinct but very short origins. The trunk is smooth with small, densely packed papillae at the anterior end. Inconspicuous skin bodies in the mid-trunk can be seen in some worms, but not holdfast papillae (Fig. 26C). The smooth body, almost always with a gray anterior "cap," is characteristic. This smoother body wall may result from life in soft tubes of clay or mud rather than hard mollusk shells. Selenka (1885) reported that the tentacles are short and few, 16 at most. Specimens with extended introverts appear to have a continuous folded membrane surrounding the mouth, but it may actually be several lobes, as in P. pacificum. DISTRIBUTION. A deep-water species (1800-6860 m, most >2500 m) from the Southern Hemisphere (36-66° S) in the Pacific Ocean, 20-32° S in the southeastern Atlantic, off Argentina, and in the southeastern Indian Ocean. Also reported from the northwestern Pacific and the northeastern Atlantic in the Bay of Biscay, 47-56° N, but apparently absent in the lower latitudes; perhaps a bipolar species.

Genus Phascolion

125

Phascolion (Montuga) pacificum Murina, 1957 Phascolion pacificum Murina, I957a:i777-I78i; I978:i25.-Stephen and Edmonds, I972:i84.-E. Cutler et al., 1984:276. Phascolion (Montuga) pacificum.—E. Cutler and Cutler, 19853:831.-Saiz and Villafranca, 1990:1 i 6 2 - n 6 4 . - S a i z , 1993:107-109. DESCRIPTION. The retractor muscle column has two, three, or four separate origins as a result of differing degrees of fusion. Small, pale, type I hooks and holdfast papillae with a thin hardened border are present. The tentacles are reduced to lobes at the end of the introvert, which is about equal in length to the trunk. The anterior trunk papillae are mammiform or conical, often with the interpapillar spaces packed with mud, and the posterior end of the trunk may bear commensal epizoans. Most worms occupy empty gastropod or scaphopod shells and are 3-10 mm long, but known trunk length ranges from 1 to 19 mm. There are many external similarities to the P. strombus subset that has pale U- or V-shaped holdfasts of variable thickness, although the holdfasts do appear thinner and paler than on most P. strombus. Internally P. pacificum is very similar to P. lutense, but the latter lacks hardened holdfast papillae. DISTRIBUTION. This bathyal and abyssal species (300-6860 m) is widespread at high latitudes (bipolar?) in the northwestern and southwestern Pacific; the northeastern (up to 57 0 N), southeastern, and South Atlantic, and the sub-Antarctic Indian Ocean. The only records at lower latitudes are from the Peru-Chile Trench (5760-6860 m) and 28 0 N (1760 m) in the eastern Atlantic. Subgenus Phascolion (Phascolion) Theel, 1875 DIAGNOSIS. Retractor column divided for most of its length. Esophagus detaches from retractor column posterior to the first separation of the retractor muscles. The diameter of the dorsal retractor muscle is at least twice that of the ventral muscle. TYPE SPECIES. Sipunculus strombus Montagu, 1804.

Key to Phascolion (Phascolion) s. s. Species 1. Very small (trunk 1-3 mm); interstitial; without holdfasts; with anus on introvert P. psammophilus - Trunk rarely 25O0 m O. magnibathum - Spherical, with abrupt transition to very thin introvert (one-fifth to one-tenth trunk diameter); introvert greater than four times trunk length; found at depths < 1000 m (Fig. 34D) O. steenstrupii nudum

Onchnesoma intermedium Murina, 1976 Onchnesoma intermedium Murina, I976:63~64.-E. Cutler and Cutler, 19853:841. DESCRIPTION. There are 6-8 small tentacles, and the papillae are present only on the anterior one-third to two-thirds of the trunk. The nonpapillated posterior region exhibits longitudinal ridges and furrows. The anus is located at least 80% of the distance toward the distal end of the introvert. DISTRIBUTION. East China Sea, at 500 m.

Genus Onchnesoma

137

Onchnesoma magnibathum E. Cutler, 1969 Onchnesoma magnibatha E. Cutler, i969:7i-76.-E. Cutler and Cutler, 19800:204-205. Onchnesoma magnibathum.—E. Cutler and Cutler, I985a:843.-Saiz, 1993:113. DESCRIPTION. Nonpapillated, cylindrical in form, and up to 6 mm long. The posterior end has radiating keels and usually tapers to a point. The introvert is about twice the trunk length and broader than in other Onchnesoma, with a gradual taper into the trunk. The anus is located 70-80% of the distance toward the mouth. The retractor column has two short origins. 0 0 DISTRIBUTION. A widespread Atlantic Ocean species (22 S to 50 N on the eastern side) with one record from the Peru-Chile Trench in the southeastern Pacific. Generally lives at depths between 3000 and 5500 m, but there are a few records from as shallow as 2300 m. Onchnesoma squamatum squamatum (Koren and Danielssen, 1875) Phascolosoma squamatum Koren and Danielssen, 1875:129. Phascolion squamatum.—Selenka, 1885:15. Onchnesoma squamatum.—Th6el, i905:96-98.-Stephen and Edmonds, I972:i63.-E. Cutler, 1973:166.Gibbs, 19773:24-25. Onchnesoma squamatum squamatum.—E. Cutler and Cutler I985a:843.-Saiz and Villafranca I990:ii64.-Saiz, 1993: in. DESCRIPTION. Typically these worms resemble a ball on a string. The trunk, up to 5 mm long, is nearly spherical, and the thin introvert is up to five times the trunk length. The trunk is densely covered with large gray papillae, and 6-8 small tentacles are present. The anus is located 70-80% of the distance toward the mouth. The retractor column has two origins at the posterior end of the trunk. The single (right) nephridium is one-third to two-thirds the trunk length and is attached for most of its length to the body wall. The gut coil is a regular golfingiid spiral attached posteriorly by one of me fixing muscles. One population collected at 280 N, 140 W, at 1900 m is unique in that the trunks are cylindrical to spindle shaped, not spherical. In these worms the trunk tapers gradually into the narrower introvert rather than making an abrupt transition, and the body wall is covered with irregular, evenly distributed, golden tan papillae that are less dense than in the northern population.

138

The Phascolionids

DISTRIBUTION. Restricted to the northern Atlantic and Mediterranean Sea, generally at depths of 150-1400 m, but a few as deep as 2300 m. On the eastern side of its range it has been reported from the Canary Islands to Iceland (27-630 N); on the western side it is found from Florida to North Carolina (24-340 N). The Mediterranean records are from very shallow depths (10-55 m )-

Onchnesoma squamatum oligopapillosum E. Cutler et al., 1984 Onchnesoma squamatum oligopapillosum E. Cutler et al., 1984:28i.-E. Cutler and Cutler, 19853:843. DESCRIPTION. This Pacific Ocean population is geographically isolated from the nominate form. Morphologically (tentacles, introvert length, anus location, retractor origins, etc.) these worms, 3-4 mm in length, are quite similar to the nominate form, but they differ by having fewer, smaller, and more scattered papillae, which are almost absent from the mid-trunk region. DISTRIBUTION. Pacific side of Honshu, Japan, at 14-250 m. Onchnesoma steenstrupii steenstrupii Koren and Danielssen, 1875 Onchnesoma steenstrupii Koren and Danielssen, 1875:133.-Shipley, 1892b: 233-250.-Theel, I905:93~96.-Stephen and Edmonds, 1972: 163-164.-E. Cutler, 1973:164; i98oc:205-2o6. Onchnesoma steenstrupii steenstrupii E. Cutler and Cutler, 19853:844; I987b:76.-Saiz and Villafranca, 1990:1 i64.-Saiz, 1993:113-115. Phascolion dogieli Murina, 19640:70-71.-Stephen and Edmonds, 1972: 176. DESCRIPTION. The spherical or pear-shaped trunk, 1-4 mm long, is commonly gray, sometimes rusty red, and rarely tan, with a very long, thin introvert (5-10 times the trunk length) sharply set off from the trunk. Tentacles are not present; instead there is a flat, circular oral disc. The anus is located 90-98% of the distance toward the mouth. The trunk has 20-30 radiating keels consisting of small, scalelike papillae on the posterior onethird to three-fourths, their size decreasing anteriad. The retractor column is completely fused and originates from the posterior end. The gut consists of a few loose loops plus a spiral with a long rectum. DISTRIBUTION. Common in the northern Atlantic Ocean, but present in the southeastern Atlantic (230 S to 570 N), higher latitudes of the western

Genus Onchnesoma

139

Pacific, and the southwestern Indian Ocean. In general this species inhabits cool to cold waters at bathyal depths on continental slopes. Very few records are from depths less than 100 m or greater than 1600 m. Reports from shallow water include the Mediterranean at 40 m and off Ivory Coast (upwelling area) at 30 m. The few deep records (2100-3000 m) are from the eastern Atlantic Ocean. Onchnesoma steenstrupii nudum E. Cutler and Cutler, 1985 Onchnesoma steenstrupii nudum E. Cutler and Cutler, 19853:844. DESCRIPTION. Distinguished from the nominate form by the epidermis, which has a unique ridged appearance when viewed under the dissecting microscope. Theridgesdo not consist of scalelike papillae; instead, each is a fold or wrinkle in the skin (Fig. 34D). The introvert is commonly five to six times the trunk length (trunk = 0.5-2.0 mm) and terminates in an oral disk (one specimen has about six tentacular lobes). The internal organs are as in the nominate form. DISTRIBUTION. Known only from the southeastern Atlantic Ocean around 230 S, 13° E, at 460-1000 m. Onchnesoma s. steenstrupii is found nearby but in deeper water (2100-2500 m).

5

The Themistids

Family Themistidae E. Cutler and Gibbs, 1985 Golfingiiformes with two nephridia. Tentacles are borne on stemlike extensions of the oral disk.

Genus Themiste Gray, 1828 Themiste Gray, i828:8.-Baird, i868:98.-Stephen, I965:58.-Stephen and Edmonds, 1972:193. Dendrostomum Griibe and Oersted, i858:ii8.-de Quatrefages, 1865b: 629. Dendrostoma Keferstein, i86sb:438.-Selenka et al., 1883:83. DIAGNOSIS. Introvert shorter than trunk. Body wall with continuous muscle layers. Tentacles basically surrounding mouth but extending along branching stemlike outgrowths as the animal grows. With or without hooks. Two introvert retractor muscles; contractile vessel with villi or tubules. Spindle muscle adheres closely to rectum and is not attached posteriorly. Two nephridia. Animals small to large (adults 4-400 mm). See Figures 35-40. TYPE SPECIES. Themiste hennahi Gray, 1828. NOMENCLATURAL NOTE. Shortly after its introduction the name Themiste fell into disuse. The genus name Dendrostomum (Griibe and Oersted, 1858) took its place until 1964, when Stephen resurrected Gray's name. Stephen and Edmonds (1972) established six species groups, which Edmonds later (1980) transformed into three subgenera. These were evaluated by Gibbs and Cutler (1987), who determined that the subgenus Themiste (Stephensonum) was void. The worms named Phascolosoma coriaceum by Keferstein in 1865 are discussed in Stephen and Edmonds, 1972 {Golfingia); E. Cutler, 1973; and Gibbs et al., 1983 (moved from Thysanocardia to Themiste!), but they were overlooked in 1988 when Themiste was reviewed by E. Cutler and

Genus Themiste

A

141

B

Figure 35. Themiste, external forms of both subgenera. A. T. (Themiste) pyroides. B. T. (Lagenopsis) lageniformis. Cutler. The use of this name by Fisher (1950a) (= Nephasoma pellucida) and Murina (1972) (= Themiste minor) is noted elsewhere in this book. The name itself is hereby assigned to the list of species inquirenda since the type material cannot be located and there are still questions about its true nature. Another name here added to the list of species inquirenda is Golfingia (Thysanocardia) neimaniae Murina, 1976. After some discussion this species was designated IThemiste neimaniae by Gibbs et al. (1983:302). No new information has come forth to clarify the situation, so T. neimaniae is moved onto the list to reflect its present status. Morphological Characters of Themiste The common name for sipunculans in Japanese is hoshi-mushi, or "star-mouth," from the starlike appearance of Themiste tentacles viewed head-on.

142

The Themistids

Figure 36. Themiste internal anatomy. A. T. (Themiste) pyroides with few long, twisted contractile vessel tubules (CVT; other abbreviations as in Figure 1; from Fisher, 1952, courtesy of Smithsonian Institution Press). B. Segment of T. (Lagenopsis) contractile vessel with numerous short, digitiform, sometimes bifurcating villi.

Contractile Vessel Villi. Two different configurations occur (Fig. 36), and these are used to separate the two subgenera (Edmonds, 1980). (1) T. (Lagenopsis) has many short villi (>ioo), a pattern found in four other genera as well. These villi do bifurcate, most notably in the larger posterior villi of large worms. (2) In T. (Themiste) a different system exists: the villi consist of a few (usually 8-14) long, threadlike extensions off the posterior quarter of the contractile vessel, often with a corkscrew or beads-ona-string appearance. Some large specimens in this subgenus exhibit a complex branching, interconnecting network near the bases of these tubules. The exact number of tubules is difficult to determine: small worms (50,ooo; see Cushing et al., 1969). No inducible immune response has been demonstrated. Although it has no mechanism for rapid inactivation of phage, T. hennahi does seem to have the capacity to produce bactericidins, hemagglutinins, a hemolysin, and an inducible ciliate lysin in addition to the stop-factor. This species produced an inducible bactericidin after 90 minutes. The substance remained at a high titer for at least seven days and was inactivated by heat above 50°C (Evans et al., 1973). The coelomic amoebocytes in T. hennahi can develop tolerance to a phagocytic inhibitor (Cushing et al., 1970) present in bovine serum. The inhibitory molecule (molecular weight > 10,000) is heat-labile and occurs in the serum globulin fraction. Cells cultured in 10% bovine serum and seawater for three days survive, and the effects of the inhibitor are significantly reduced. Male T. hennahi can recognize untreated eggs of their own species as "self," even though egg cells are not normally present in males (Cushing and Boraker, 1975). When altered by staining or heating these same cells were quickly encapsulated as a foreign substance; however, frozen eggs, while dead, were not encapsulated, so the species-specific antigens were still present and serving as a recognition signal. In other words, tolerance of self does have a molecular basis in sipunculans as in most other animals. Antibacterial and Cytotoxic Activity Nonspecific antimicrobial substances are assumed to be common in the phylum Sipuncula, and a study of T. hennahi conducted by Johnson and Chapman (1970) supports this hypothesis. The coelomic fluid of T. pyroides and Phascolopsis gouldii is also known to exhibit antibacterial activity (Krassner and Flory, 1970). Trypsinization destroyed this activity, but pepsin, lipase, toluene, and freezing did not.

270

Coelomic Cells and Immune System

When specimens of P. gouldii were placed in i6°C seawater for 90 seconds the coelomic cells produced a cytotoxic material that was lethal both to untreated worms into which this fluid was injected and to sea urchin eggs (Chaet, 1955). The cytotoxic activity of the leucocytes that destroyed both allogenic (self) and xenogenic (nonself) erythrocytes in European Sipunculus nudus and Siphonosoma arcassonense shows that molecular changes occur in the leucocyte membrane induced by histocompatibility antigens (Valembois et al., 1978). Thus, in vitro sipunculan leucocytes are potentially good models for studies of differentiation of the molecular organization in cell membranes (e.g., surface receptors). Cooper's (1976) general review of cellular recognition of allografts and xenografts provides a context in which to view the sipunculans by outlining the three different types of antibody production in invertebrates. The review also proposes the following evolutionary rationale for antibody production: the protection from predation by microorganisms. The primitive nature of sipunculan immune responses can be demonstrated by repeated injections of xenogenic erythrocytes into the coelom, which suppresses the natural cytotoxic effects (i.e., the worm develops amnesia) (Valembois et al., 1977). The suppression of cytotoxic activity (increase in tolerance) is specific, showing that cytolysis is also specific. In oligochaetes and vertebrates, induced immunity can be transferred via coelomic fluids, but this is not the case in sipunculans, which demonstrate a specific, but amnesiac, immunorecognition response. A useful synopsis of the immune responses of invertebraj^s is the general review by Weinheimer (i97o:table 1). Not surprisingly, the sipunculan immune system is classified as intermediate between the most primitive (nonspecific recognition of self and nonself) and the most advanced (specific, anamnesiac immunity) systems found among invertebrates and vertebrates.

11

Respiration, Genetics, and Biochemistry

Respiration

Gas Exchange The exchange of oxygen and C0 2 between seawater and coelomic fluid occurs both directly through the body wall and indirectly via the tentaclecontractile vessel complex. Only a few species (e.g., Themiste) have tentacular crowns voluminous enough to suggest a gill. Most members of the family Sipunculidae are large worms with rather thick body walls. These animals have diverticula that extend from the coelom through the muscle layers and out toward the epidermis (see family characters in Part I; Ruppert and Rice, 1990). These pouches or canals allow the coelomic fluid to circulate closer to the external medium, thus facilitating gas exchange. Special adaptations for life in low-oxygen environments include the elongate dermal extensions (digitiform papillae) connected with dermal canals carrying coelomic fluid that are present in Sipunculus longipapilosus and Xenosiphon branchiatus (Fig. 8), and the enlarged tentacular crown and contractile vessel villi complex in Phascolion (Villiophora) cirratus and Antillesoma antillarum, which increases the surface area for gas exchange (Fig. 52C). Many marine invertebrates lack a single-purpose respiratory system, especially those with limited mobility and modest energy needs. In most sipunculan species, many of which have very small tentacular crowns (e.g., the genera Aspidosiphon, Phascolosoma, Apionsoma, Nephasoma, and Onchnesoma), diffusion through the thin body wall provides sufficient oxygen to meet metabolic needs. The tentacular fluid circulates in a closed system between the tentacles and the contractile vessel (compensation sac, sensu Hyman, 1959) with the help of intrinsic muscle fibers, cilia, and the extension and contraction of the introvert. Within the coelom, the contractile vessel and its villi (when

272

Respiration, Genetics, and Biochemistry

present) provide an internal surface for gas exchange and diffusion of other molecules. As was described in Chapter 10, the hemerythrin in the coelomic and tentacular fluid stores and transports oxygen. Hemerythrin can carry about three times as much oxygen as seawater (i.e., 20 vs. 6 cc/1, according to Chaphaeu, 1928, and others). Edmonds (1957a) compared rates of oxygen consumption in juvenile and adult Themiste cymodoceae at 22°C and found a fivefold decrease with age (25 vs. 5 (xl-g wet weight- ••hr -1 ). Juveniles had a respiratory quotient of 0.55-0.67. S. nudus consumes 6-10 mg-ioo g _ 1 h r _ 1 oxygen at I5°C (Cohnheim, 1911). Values for Phascolopsis gouldii, which lives in burrows at Po2 values of 77-81 mm Hg, are similar. These worms have a coelomic fluid Po2 of 5-8 mm Hg at 23°C (Mangum and Kondon, 1975). These data are comparable with Wells's (1982) values for S. mundanus (formerly Xenosiphon mundanus), which had what Wells considered to be a high oxygen affinity: P 50 = 7.0 mm Hg at pH 7.5 and 2o°C. sacxcj? As the amount of available oxygen decreases, the energy expenditure and oxygen consumption of S. nudus also decrease in a linear manner that varies according to the size of the worm (Poertner et al., 1985). The positive correlation between ambient Po2 and coelomic Po2 makes this species an oxyconformer. Anaerobic Metabolism Themiste cymodoceae can live without oxygen for four to five days, and during these anaerobic periods it produces lactic acid as one of the end products of metabolism. In one study (Edmonds, 1957a), lactic acid increased from 7-12 to 45-61 (xg/ml blood after 60 hr. The ability to revert to anaerobic pathways for energy metabolism almost certainly has survival value for these worms, especially those living in intertidal environments that are periodically deprived of accessible oxygen (Edmonds, 1957a). Other aspects of anaerobic sipunculan respiration have been addressed by Poertner and associates (Livingstone et al. 1983; Poertner et al., 1984a, 1984b, 1984c, 1986a, 1986b, 1991; Poertner, 1986, 1987a, 1987b; Grieshaber and Kreutzer, 1986; Kreutzer et al., 1989; Hardewig, Addink, et al., 1991; Hardewig, Kreutzer, et al., 1991). Lim and Ip (1991a, 1991b), working with Phascolosoma arcuatum, have added to this body of knowledge. Most of the respiration studies cited above monitored intermediate metabolic enzymes, their kinetic properties, and accumulated products

Genetics

273

following artificially enhanced muscular activity and prolonged experimental hypoxia at different seasons of the year. Anaerobic glycolysis (Embden-Meyerhof pathway) is very important during prolonged anaerobiosis. As the rate of metabolism increases, so too does the amount of energy delivered. Phospho-L-arginine is the most important energy molecule (i.e., proton source) during anaerobic glycolysis, and octopine and strombine are the main end products. The products that accumulate depend on the concentrations of the corresponding amino acids and the experimental conditions (Kreutzer, et al., 1989). The coelomic fluid serves as a transient proton sink during long-term anaerobiosis, helping to maintain the acid-base balance as proton equivalent ions move from muscle tissue through the coelomic fluid and out into the surrounding seawater. Although 5. nudus is very efficient in transferring protons from the coelom to the environment, the transfer capacity of the energy-consuming translocation mechanism is limited by the amount of available energy. The control of intracellular pH seems to be a priority for sipunculans. While this balance system works well, it is limited since the defended pH is lower during facultative anaerobiosis than it is following recovery as oxygen becomes available. As the ambient oxygen level falls, oxygen uptake, heat production, and aerobically produced energy also decrease. S. nudus employs anaerobic metabolism when the ambient Po2 is between 8.7 and 2.7 kPa. Above this level aerobic processes are sufficient, each mode (aerobic and anaerobic) producing about one-half the total ATP at the lower extreme (Hardewig et al., 1991).

Genetics

Chromatin Most of the sipunculans that have been studied have 10 pairs of chromosomes (see Karyology, Chapter 19). Chromosomes are made up of DNA that is tightly bound to basic proteins called histones. There are five types (Hi, H2A, H2B, H3, H4) of histones, and these together with the DNA form chromatin. Two of these (H3 and H4) are highly conserved; the amino acid sequence remains nearly identical in all eukaryotes. The chromosomes in the erythrocyte nuclei of Sipunculus nudus have been the subject of recent interest. Although the lysine-rich histones are

Respiration, Genetics, and Biochemistry similar to vertebrate histones, there are enough other differences to suggest a unique chromatin. The histone H2B has a repeat length of 177 ± 5 units, shorter than that found in higher vertebrates (which have ca. 200 units) and close to that reported for some lower eukaryotes (Mazen and Champagne, 1976; Mazen et al., 1978). Histone H2A contains 123 amino acid residues, which have been completely sequenced using a staphylococcal protease digestion technique and limited hydrolysis of the protein with chymotrypsin. Compared with calf histone, S. nudus histone shows 6 deletions and 13 substitutions (Chauviere et al., 1980; Kmiecik et al., 1983). Six of the substitutions are nonconservative, and most of the changes are in the basic amino terminal and carboxy terminal regions of the molecule (i.e., the primary DNA binding sites). The high amount of phosphorylated H2A (60% on the amino terminal residue) may be related to the smaller repeat length of this nucleosomal DNA (177 base pairs; other taxa have from about 160 to 240), to nuclear inactivation, and to chromatin condensation. Genetic Variability Genetic mutations do not always result in the formation of new species. Nonlethal mutations often produce a protein such as an enzyme with a structurally modified form ("allozyme") that continues to perform the same function. Techniques such as gel electrophoresis are employed to discern this hidden variation. Intraspecific electrophoretic variation in numerous gene loci coding for enzymes and other proteins in a Phascolosoma was examined. The high variability discovered supports the view that invertebrates are more polymorphic than vertebrates. The large and time-stable nature of this sipunculan population in the northern Pacific contributes to its polymorphic condition. This follows the general pattern of very little polymorphism in small, isolated, or newly evolved populations; as a population or species increases in size and age, more polymorphisms appear (Balakirev and Manchenko, 1983). Manchenko and Balakirev (1985) also examined the allozymic variation of alanopine dehydrogenase for 24 loci in 32 species of marine invertebrates, including sipunculans, using starch-gel electrophoresis. Balakirev and Zaikin (1988), who continued this work by looking at the allozyme variability of formaldehyde dehydrogenase in 31 species, found extensive polymorphisms in 18 species. This dimeric enzyme could serve as a useful tool in studies of population genetics of marine invertebrates.

Miscellaneous Biochemical Attributes

275

Miscellaneous Biochemical Attributes

Chemical Composition De Jorge et al. (1970) analyzed the chemical composition of the Brazilian species Sipunculus natans and S. multisulcatus and came up with an extensive list of the inorganic ions and organic molecules present in the coelomic fluid. The highest levels of sodium and potassium are in the body wall; the esophagus is highest in iron; and the ventral nerve cord has the most calcium, magnesium, phosphorus, and sulfur. The high concentrations of iodine in the nephridia suggest a role in the metabolism of this element. Guanidine Compounds Two new guanidine compounds (used as phosphoryl acceptors) were characterized from Phascolion strombus and two species of Golfingia (the latter incorrectly called Phascolosoma): phascoline (N-[3-guanidinopropionyI]-2-hydroxy-«-heptylamine), and phascolosomine (N-[3-guanidinoisobutyryl]-2-methoxy-n-heptylamine) (Guillou, 1973). These compounds were concentrated in the intestine in amounts of 600-1100 mg/ioo g wet weight, but their biological significance is unknown. This concentration is two to four times the average total (free plus phosphorylated) amount of guanidine base found in the body wall and muscles of other animals. Phascoline and phascolosomine have been used by biomedical researchers to study the initiation mechanisms of seizures (Yokoi et al., 1989). Electroencephalograms of rats injected intracerebroventricularly with the two compounds showed that they cause seizures by disinhibiting the central nervous system. Arginine Kinase An arginine kinase (ATP:L-arginine phosphotransferases) in S. nudus characterized by Thiem et al. (1975) has a molecular weight of 84,000, 12 reactive thiol groups, 6 reactive histidine residues, and is very susceptible to oxidation. This enzyme was compared with a very similar one from the razor clam Solen, and the most significant difference between them was the way the spectrum of the sipunculan Mg++-ADP-enzyme complex is strongly intensified by L-arginine.

12

Excretory System

Anatomy

Most sipunculans have a pair of elongate, saclike, tubular metanephridia located ventrolaterally at the anterior end of the trunk; Phascolion and Onchnesoma species have only one. The ciliated, funnel-shaped nephrostome at the anterior end opens dorsally from the coelomic cavity into the anterior bladder (Metalnikoff, 1899). The simple nephridiopore is also at the anterior end of the nephridium, but ventral, and the opening from the secretory part to the outside is controlled by a sphincter muscle (Fig. 72A). Fluids (and gametes) pass posteriorly around the recurved V-shaped interior tube, aided by cilia and contractions of the muscular nephridial wall (Fig. 72B). The posterior, distal secretory portion, consisting of an open lumen, can be quite long. The organ is either connected to the body wall by a diaphanous membrane (or, occasionally, by fine muscle strands) or hangs free in the body cavity. The length is commonly 25-50% of the trunk but ranges from 5 to 125%. The outer layer (coelothelium) of the nephridium in Phascolosoma granulatum contains podocytes with small basal, footlike extensions called pedicles. The podocytes overlay the basal lamina and are separated by small slits which are bridged by diaphragms. The cells are joined in the Figure 72. Excretion and ion regulation. A and B. Nephridial anatomy of Phascolosoma nigrescens (from Shipley, 1890). A. Mid-sagittal section. B. Transverse section through secretory portion. C. Nephridial histology of Golfingia vulgaris (after H6rubel, 1907). D and E. Ionic regulation in coelomic fluid of Themiste dyscrita (circles; data from Hogue and Oglesby, 1972) and Phascolopsis gouldii (triangles; data from Oglesby, 1982). D. Isotonic balance of sodium ions. E. Hypertonic balance of potassium ions; chloride tends to be slightly hypotonic to the medium. B, bladder; BW, body wall; CC, cuboidal cells; CM, circular muscle fibers; DS, distal secretory part; LE, lining epithelium; LM, longitudinal muscle; NP, nephridiopore; NS, nephrostome; P, peritoneum; SG, secretory granules.

Anatomy

277

278

Excretory System

apical cytoplasm by the zonula adhaerens and septate desmosomes (Serrano et al., 1989). The middle layer of the excretory organ consists of longitudinal and circular muscle fibers arranged in an irregular connective tissue layer. The cells are filled with paramyosin myofilaments of three types (mean diameters 28, 42, and 58 |xm) and have peripheral organelles (Serrano et al., 1990). The middle layer is sandwiched between the outer peritoneum, made up of flat, glycogen-rich cells, and an inner folded epithelium of cuboidal cells which line the lumen (Fig. 72C). The cuboidal cells contain glycogen and large, brown-yellow granules whose color tinges the whole organ. The inner epithelial cells exhibit variable amounts of cilia and microvilli as apical surface specializations and basal labyrinths or long, slender projections as basal specializations (Storch and Welsch, 1972; Pinson and Ruppert, 1988). Excretion can be defined as either selective reabsorption or secretion to form urine by modification of a filtered vascular fluid. While there is little direct experimental evidence of excretion in sipunculans, the ultrastructure of the nephridium does support this function. The apical modifications aid absorption, and the basal changes are designed for secretion. In addition to external modifications, the cells have apical cytoplasm with coated and uncoated vesicles, tubules, endosomes, and putative lysosomes. Basally, the infolding and numerous mitochondria also suggest an excretory function. Tracer compounds injected into the coelom are engulfed endocytotically by cells lining the nephridia and stored in vesicles for later secretion (Pinson and Ruppert, 1988). Ocharan (1974) compared the nephridia of Phascolosoma granulation with the myxonephridia of polychaetes and suggested that the nephrostome has a dual origin, with the nonciliated part being possibly a remnant of the original coelomostome. Similarities between polychaetes and sipunculans include the ciliated inner epithelium with small pigment granules. The outer layer, as found in other sipunculan species, contains muscle fibers, granules, and connective tissue with mesothelial peritoneum. The pigmented epithelial cells are of two types: (1) flattened replacement cells, which give rise to (2) elongate apocrine secretory cells functionally similar to the cells of vertebrate adrenal glands. Ocharan (1974) concurred with Harms's (1921) hypothesis that the nephridia have some endocrine function but was not able to substantiate this idea experimentally. Ocharan's conclusion that nephridia are involved in the metabolism of iodine pro-

Physiology

279

teins, based on de Jorge's (1969, in Ocharan, 1974) observation of high levels of iodine there, is also speculative. An excretory role has been suggested for the contractile vessel. Pilger and Rice's (1987) ultrastructure studies on an unnamed species indicated the presence of podocytes on the outer wall of this vessel. This arrangement may result in the formation of a primary ultrafiltrate, which could be forced from the coelom of the tentacle-contractile vessel complex into the trunk coelom and could subsequently be converted to a secondary filtrate by the nephridia. In an addendum to their review paper, Ruppert and Smith (1988) cited the existence of these podocytes as support for the idea that contractile vessels are analogous to blood vessels in typical metanephridial systems.

Physiology

Sipunculan nephridia do appear to play a role in both the excretion of nitrogenous waste products and osmoregulation. Inert materials such as dyes are removed via the nephridia (Harms, 1921; Ocharan, 1974). Nitrogen Excretion Ammonia salts have been detected in nephridial fluids (Harms and Dragendorff, 1933), and Edmonds (1957b) found 83-90% of the excreted nitrogen to be in the form of ammonia (there was very little urea and no uric acid). This ammonia is the end product of purine degradation (Florkin, 1969b). Osmotic, Ionic, and Volume Regulation Oglesby's 1969 review of sipunculan osmotic and ionic regulation is still an excellent source. It includes information gathered by several authors about nine species. More recent articles are more limited in scope and do not contradict Oglesby's conclusions (e.g., Robertson, 1990). Sipunculans' ability to regulate volume is limited and varies both among and within species—an example of nonmorphological variation among individuals within a species. Some of the variation depends on how well the animal has been fed and whether or not gametogenesis is occurring.

280

Excretory System

Mechanisms for volume regulation involve the movement of water and salts, most importantly sodium and chloride (Foster, 1974; see also Hogue and Oglesby, 1972), across the body wall (Adolph, 1936; Gross, 1954). Water passes into the worm more easily than it passes out, and salts also move in and out at different rates. One mechanism used to maintain isoosmotic conditions is the substitution of small organic molecules, such as free amino acids or monosaccharides, for inorganic ions, although this plays only a small role in maintaining osmotic pressure. The control of sodium and chloride flow is one function of the nephridia. Essential salts are removed from the hyperosmotic coelomic fluid passing through the organs; excess water is then discharged. Sipunculans, especially the intertidal and shallow subtidal species living in euryhaline habitats, while largely osmoconformers, are not simple osmometers (Hogue and Oglesby, 1972; Oglesby, 1982). They are ionic and osmoconformers with limited regulatory capabilities that vary from one species to the next. The following generalizations about particular ions and their concentrations in the coelomic fluid are drawn from published data (Fig. 72D, E). Four ions occur in concentrations close to seawater concentrations: chloride (84-103%) and calcium (91-96%) may be just below, and sodium (100-108%) and potassium (103-130%) are slightly above, ambient concentrations. In contrast, magnesium (55-58%) and sulfate (35-84%) appear to be more highly regulated and are maintained at concentrations significantly lower than those in seawater. Phascolosoma arcuatum (formerly P. lured) is regularly exposed to the most eurytopic conditions of any sipunculan. Worms of this species live in intertidal Indian Ocean mangrove mudflats but can survive out of the water for up to seven days. A population of freshly collected Malaysian worms exhibited chloride ion concentrations (189-571 meq) and total osmotic content (396-1135 milliosmoles) ranging from hyper- to isoionic and osmotic. A laboratory population survived salinities of 40-100% for at least 64 hr and subsequently equilibrated to become isosmotic with seawater, showing very little evidence of regulatory ability. Their natural habitat (mud burrows) together with the mud in their intestines may help them buffer ionic changes and maintain the differential between internal and external ion concentrations (J. Green and Dunn, 1976, 1977). Siphonosoma cumanense maintained in the lab at 50-125% seawater showed a rapid change in weight for three hours, peaking at four to five

Physiology

281

hours (Thomas, 1972). Worms in 85 and 125% seawater functioned as osmometers, the coelomic fluid volume mirroring the changes in the external environment; however, worms placed in 50 and 70% seawater resisted further change and exhibited some volume regulation after eight hours. Thus a limited capacity for osmoregulating under extreme conditions does exist; however, none of the worms returned to its original weight after being replaced in normal seawater. Themiste dyscrita is a passive osmoconformer that does not survive very long in water with a salinity less than 50% of normal (Oglesby, 1968). Generally speaking, sipunculans are not well adapted to survive at environmental extremes.

13

i/f

"*kk ' ^

Digestive System

Anatomy

The sipunculan digestive system is basically a recurved gut twisted into a double helix. The mouth is in the center of the oral disc, at the tip of the Introvert. The oral disc in the class Sipunculida is surrounded bv tentacles, the size and number varying according to the species; a few have rudimentary or no tentacles (Fig. 2). In the class Phascolosomatidea. peripheral (oral) tentacles are lacking; only nuchal tentacles in a dorsal crescent are present. The anus is usually located at the anterior end of the trunk on the middorsal line. This pattern, which is similar to that found in lophophorate coelomates, is an adaptation to a sedentary mode of life in a closed tubular burrow that would quickly become uninhabitable if the worm had a posterior anus. In Onchnesoma and four Phascolion species, the anus has actually shifted out onto the introvert, 20-95% of the distance toward its tip. The tubular digestive tract has no clear external demarkation between the functional regions. When the introvert is extended, the esophagus is straight; that is, it does not form part of the helix. A poorly defined "stomach"—a short transitional region between the esophagus and the intestine—has been observed in three species: Phascolopsis gouldii, Nephasoma minutum, and Golfingia elongata (Andrews, 1890b; Paul, 1910; Stehle, 1953). Similarly, a few earlier authors referred to the region of the esophagus just inside the mouth as a pharynx. This term has not been used recently, and there seems to be no anatomical justification for its use. Sipunculus (but not Xenosiphon) species have a characteristic postesophageal loop of the intestine before the beginning of the helical coil (Fig. 4). The intestine is divided into descending and ascending halves, usually as a double helix coil, but in a third of the Phascolion, a few Aspidosiphon, and a few Nephasoma species it is a looser, more irregular series of loops

Physiology

283

and partial coils. Additionally, each half of the intestine can be subdivided physiologically into three parts (Di, D2, D3, and Ai, A2, A3; see Michel and DeVillez, 1983). The lining of the intestine is largely columnar ciliated epithelium with scattered glandular cells, underlain by connective tissue with some nerve fibers. In Golfingia elongata these secretory cells appear to be supplemented by thin extensions of the external intestinal wall into tubular glandular units that open into the lumen (Stehle, 1953). The gut wall may have contractile fibers—inner circular and outer longitudinal—which are strong in the esophagus but not well defined in the stomach or most of the intestine. In the rectum the circular layer may again become well developed. Extending through at least the ascending portion of the gut is a ciliated groove which appears to end near the junction of the intestine and the rectum. The presence of cilia and reports of a current going toward the anus suggest that the groove moves material through the gut in conjunction with the musculature in the intestinal wall (Andrews, 1890b; Cuenot, 1900). The rectum extends straight from the gut coil to the anus. There may be a small caecum at the junction of the intestine and rectum. More complex rectal appendages are present in Siphonosoma vastum and some, but not all, Aspidosiphon laevis. The function of the caecae is unknown. The most distal part of the rectum is almost always fixed to the body wall by a wing muscle in the form of a broad, flat sheet. Hyman (1959) suggested that this has a dilator function, but it seems more likely that it serves as a type of sphincter. The gut is kept in place by the spindle and fixing muscles, thin muscle strands described in Chapter 9 as intestinal fasteners.

Physiology Once food (and inorganic material) is ingested, digestion begins in the descending intestine. Studies of the digestive physiology of Phascolopsis gouldii have contributed greatly to our understanding of sipunculan digestion (Brown et al., 1979, 1982; Michel et al., 1980; Michel and DeVillez, 1983, 1984). The esophagus is not glandular, but the epithelium of the illdefined stomach has sparsely distributed gland cells (Fig. 73). This region secretes weakly acidic mucus and neutral mucopolysaccharides via exocytosis in a merocrine manner, but not enzymes.

284

Digestive System

Figure 73. Digestion. A and B. Cross sections of descending (A) and ascending (B) intestine of Phascolopsis gouldii (after Michel and de Villez, 1984, © 1984, with permission of Pergamon Press Ltd., Headington Hill Hall, Oxford 0X3 oBW, UK). C. Cross section of Phascolopsis gouldii stomach showing four ridges of radiating fibers that reduce the lumen to an X shape (from Andrews, 1890b). D. Glandular epithelium of Golfingia elongate intestine (after von Stehle, 1953). B, bleb; CC, chloragogue cells; CE, ciliated epithelium; CG, ciliary glandular gutter; CT, connective tissue; D, diverticulum; EC, enzymatic cell; GE, glandular epithelium; M, muscle; MF, mesentarial fibers; OC, ordinary intestinal cell; RC, replacement cells; RF, radial fibers.

The pH in the descending intestine is about 7.8. The rough endoplasmic reticulum produces zymogen granules. The granular material becomes an apocrine secretion from cells with apical microvilli and cilia. The enzyme becomes active toward the end of the descending coil and the beginning of the ascending coil. The ventral ciliated gutter in the ascending intestine appears to produce the necessary enzyme activator (Brown et al., 1984). All absorption takes place in the ascending intestine. Brown et al. (1984) hypothesized that "chymotryptic enzyme is secreted

Physiology

285

as an inactive proenzyme from the zymogen granules of the descending intestine, activated and subsequently associated with a glycocalyx secreted by cells in the ventral ciliary gutter of the anterior ascending intestine." A Phascolosoma species and two Golfingia species from the North Atlantic examined by Walter (1973) digested prey animals as they moved through the gut, although plant material was unaffected. The same author later showed that the energy content in the anterior intestine was ten times that of the nearby environment (Hansen, 1978). The energy loss between the anterior gut and the midgut was 70%, while the loss between the midgut and hindgut was only 19% (midgut in this context equates with the first part of the ascending intestine as used in the preceding paragraph). Earlier workers (see Jeuniaux, 1969) demonstrated the presence of enzymes such as chitinolytic polysaccharidase in Phascolion strombus and Sipunculus nudus. The nature of the cuboidal ciliated secretory cells in the digestive epithelium of Golfingia elongata generally concurs with the cytological observations of Michel and Brown discussed above (Stehle, 1953). If the rectal caecum, which is not present in all worms, has a function, it is unknown. Its epithelial lining includes cuboidal vesicular cells, so it is presumed to be secretory. It may be that the caecum is important only in juveniles. Metalnikoff (1900) noted that it is larger in younger Sipunculus nudus than in adults. This may explain why its presence is so unpredictable in adults of many species; that is, the caecum may degenerate or be reabsorbed partially in some worms and entirely in other individuals. Sipunculans have no liver or digestive glands, but there are reports of bulging, clavate chloragogue cells on the outer peritoneum of the esophagus and intestine (Stehle, 1953). Their morphology and yellow granular contents suggest a role in storage and metabolism of fats similar to that performed by chloragogue cells in annelids.

14

Nervous System

Central Nervous System

Structure The central nervous system of sipunculans consists of a dorsal bilobed cerebral ganglion (brain), circumenteric connectives, and a ventral nerve cord (Fig. 74). Attnough referred to as an annelid type by Hyman (1959), the nerve cord is neither segmented nor paired. The anterior part of the ventral nerve cord is separated from the body wall in some of the larger members of the Sipunculidae and may have longitudinal muscle strands on either side known as paraneural muscles. The peripheral nervous system consists of lateral nerves and their subdivisions off the ventral cord. These arise in an irregular manner, rarely opposite or alternate. Older general works that describe the nervous system include Andreae, 1881,1882; Andrews, 1890b; Ward, 1890; Cuenot, 1900; Metalnikoff, 1900; Awati and Pradhan, 1936; and Gerould, 1938. Anterior cerebral nerves connect with the nuchal organ, and nerves from the circumenteric ring go into the tentacles and may subdivide within each tentacle. Nerves from the circumenteric connectives also supply the anterior end of the digestive tract, and some extend on into a plexus within the gut wall. These nerves are most strongly developed along the rectum. The introvert retractor muscles are also innervated from this nerve ring. The lateral nerves pass through the circular muscle layer and radiate. Some branches continue around the body to the dorsal side, suggesting a complete ring, but Akesson (1958) maintained that the only complete ring nerve is at the anterior end of the introvert. Other branches enervate the longitudinal and circular musculature of the body wall, and branches off the circular (radial) nerves connect to the epidermal papillae and sensory cells. A nerve plexus occurs in the coelomic peritoneum; its function may be

Central Nervous System NN

287

DP

Figure 74. Central nervous systems in two sipunculans, showing variation in basic plan, especially in the elaboration of the cerebral ganglia, as in Sipunculus nudus (A) and Golfingia vulgaris (B). B, brain; CC, circumenteric connectives; DP, digitate processes; LN, lateral nerves; NN, nuchal nerve; OT, ocular tube; RM, nerve to retractor muscle; TN, tentacular nerves; VNC, ventral nerve cord. (A, after Metalnikoff, 1900; B, after Cu6not, 1900.)

to coordinate the cilia that line the coelom. The posterior end of the ventral nerve cord ends rather undramatically in one or two lateral branches, except in Sipunculus nudus, which has an enlarged bulb instead. This swelling may have only a protective function, but Akesson (1958) considered the bulb to be a terminal ganglion connecting with the secretory terminal organ. Layers of endothelium form a protective cushion around the nerve cord, and the brain is surrounded by a pericerebral sinus in addition to connective tissue. Axons that lie within the nerve cord lack myelin sheaths but are separated by connective tissue with a web of collagen fibers in Phascolosoma granulatum (Martinez, 1973). In S. nudus the cell bodies are ventral and the fibrous tracts are dorsal (Mack, 1902). As we have seen with regard to other systems, S. nudus has unique neural features as well; these are discussed below.

288

Nervous System

The brain's components are similar to those of the nerve cord, but the tracts are centrally located and the cell bodies are arranged all around this core. Three types of neurons are found in the brain: giant neurons, median cells (both acidophilic), and globular neurosecretory cells (in Siphonosoma australe and S. cumanense, Mainoya, 1974; and P. granulatum, Martinez, J 973)- The cell bodies of the first two types are concentrated in the posterodorsal part of the brain. The most comprehensive study of sipunculan nervous systems to date is that conducted by Akesson (1958), who examined 14 species from eight genera; his work should be consulted for details. In addition to what I have mentioned above, he demonstrated that the complexity of the brain is directly correlated with the size of the worm. In a few of the species Akesson examined, the brain sinks inward and posteriorly, away from the tentacular base, so that the external environment is perceived indirectly via a cephalic tube. Finally, he noted the presence in the ventral nerve cord of undifferentiated regenerative cells that probably play a role in damage repair. Nerve Transmission Transmission of signals is cholinergic (based on the presence of 46 u.g of acetylcholine per gram of wet weight in a Phascolosoma specimen; Ger et al., 1977). Cholinesterase activity in sipunculans is comparable to that seen in the brains of mollusks, arthropods, and mammals.

Sense Organs

"' S

Scattered epidermal sensory cells or glands are found on the body surface, denser near the tip of the introvert. These have been examined closely in Sipunculus nudus (Ward, 1891) and Phascolopsis gouldii (Nickerson, 1900). Sensory cilia are present, linked to the ventral nerve cord by bipolar nerve cells. Some organs have large secretory glands with external ducts. The sfencfei; bipolar sensory cells in P. gouldii have elongate, ovoid nuclei/(Gerould, 1938),.! A variety of sensory organs exist, including a heavily ciliated multicellular pit that can be protruded as a papilla. Simpler elongate fusiform sensory cells are more common, however, sometimes associated with multicellular glands that may form papillae. Akesson (1959) categorized three

Sense Organs

289

groups of epidermal organs: (1) the Golfingia group, with two types of cells and secretory products; (2) the Phascolosoma group, with only one type of cell and product; and (3) the Sipunculus group, with separate sensory and secretory cells and glands of two types, as in the first group .^(i.e., bi- and multicellular). / The inner end of the cephalic (cerebral) tube, in the few species that (•• have one, connects with the cerebral organ. The function of this organ has not yet been demonstrated, but its structure suggests a sensory role. The cerebral organ is present to some degree even when the cephalic tube is lacking. It contains a syncytial mass of nuclei without clear cell boundaries and is separated from the rest of the brain by a connective tissue envelope (Akesson, 1961a). The cerebral organ is well developed only in Sipunculus. During development the cerebral organ portion becomes separate from the rest of the brain but remains within the brain capsule, and its function changes from secretory to sensory. Akesson suggested a dual function, or different functions at different life stages, as in crustaceans or polychaetes. Chemoreception y r • >

Although hard evidence is still lacking, it seems likely that the nuchal organ, located on the dorsal margin of the oral disc, is a complex chemoreceptor. The external elaborations of this organ are extremely varied from genus to genus; in Thysanocardia and Antillesoma, for example, it is obvious and well developed, but in Nephasoma and Phascolion it is very difficult to locate (Fig. 25). In the class Phascolosomatidea the nuchal organ is surrounded by an incomplete ring of nuchal tentacles that accentuate its presence. Some kind of organ was present in all 14 of the species examined by Akesson (1958) (Fig. 75). The nuchal organ looks like a two- or four-part, slightly inflated cushion. The surface of the cushion may be smooth, or it may seem ridged, giving the impression of parallel rows of small tentacles that have not separated from the underlying matrix. Within the tissue of the nuchal organ, one or two pairs of nuchal nerves branch extensively. The nuchal organs in Siphonosoma cumanense and 5. australe are histologically similar but structurally different. The organ in the former is multilobulate, has four pairs of nerves, and secretes acidophilic granules. 5. australe'% nuchal organ is bilobed, has two pairs of nerves, and is not secretory (Mainoya, 1974).

290

Nervous System

Figure 75. Nuchal organ sensory cells in three species showing three stages of incorporation into the brain (from Akesson, 1958). A. Phascolosoma granulatum. B. Onchnesoma steenstrupii. C. Phascolion strombus. B, brain; CO, cerebral organ; NO, nuchal organ.

Photoreception Sipunculan photoreceptors, known as eyespots, are pigment-cup ocelli embedded in the dorsal surface of the cerebral ganglia. In some species the eyespots lie at the inner end of cuticle-lined ocular tubes (Fig. 76). Although an array of microvilli and cilia may be present, these are still regarded as rhabdomeric photoreceptors. Melanin-like granules are present in supporting cells, and the many tonofilaments present extend from the basal part to the apical microvilli (Hermans and Eakin, 1975). The eyespots develop from superficial cells on the apical plate that later become embedded in the brain as inverted ocelli. There appear to be two sets of ocelli: a larval set, which disappears, and an independently developed, permanent adult pair which develops in juveniles (Akesson, 1961a). Despite Gerould's (1938) claim that it exists, Akesson (1961a) was unable to find a connection between the larval ocelli and the adult ocular tubes. At least some species with more complex eyespots have a spindle-shaped refractive body or lens (Gerould, 1938; Akesson, 1958) (Figs. 76E, 77). Secondary tentacular eyespots may be present in Sipunculus.

Gravity Reception Rudimentary statocysts at the anterior end of the ventral nerve cord have been reported from three genera (Akesson, 1958), and are, one supposes, of doubtful significance,.

Neurosecretion

291

Figure 76. Ocular tubes in sipunculans (no evolutionary sequence is implied; reduction in complexity is plausible). A. Simple tube, as in Phascolion strombus, Nephasoma minutum, Onchnesoma steenstrupii, and Sipunculus species. B. Type found in Phascolosoma granulatum with secretion around the invaginated cuticle. C. Type found in Aspidosiphon muelleri and Thysanocardia procera. D. Type found in adult Golflngia margaritacea; invaginated portion is without connection to ectoderm. E. Type found in G. vulgaris, G. elongata, and Themiste cymodoceae with a refractive body. C, cuticle; RB, refractive body; S, secretion. (From Akesson, 1958.)

Neurosecretion

Neurosecretory cells have been identified in several sipunculan species, and in Sipunculus their products are stored in the digitate processes (Gabe, 1953; Akesson, 1958). The products are released into either the central neuropile (ganglia forming a network of associated motor and sensory fibers), the coelom, or the contractile vessel, depending on the species. Carlisle (1959) alleged that the neurosecretory system in S. nudus is structurally similar to the hypothalamo-hypophysial system in chordates and the endocrine systems of insects and crustaceans. In Akesson's (1961a) view, however, some of Carlisle's conclusions about phylogenetic relation-

292

Nervous System

Figure 77. Section through the ocular tube of Golfingia elongata. PE, pigmented epithelium; RB, refractive body; SC, sensory cells; Sn, secretion; ST, secretion threads. (From Akesson, 1958.) ships were based on erroneous data, and some of his axon traces were flawed. The secretory cells in Siphonosoma cumanense are quite similar in size to those in S. nudus. Bianchi (1974,1977) reexamined old data on the neurosecretory system of 5. nudus and added new information on the materials produced. The cerebral ganglia contain four types of cells. The pear-shaped giant neurons (40-60 |xm long) produce large amounts of lipids. The smaller spindleshaped bipolar neurons make peptides. Neither the smaller pear-shaped cells (18-20 Jim) nor the small unipolar cells (5 p,m long) showed any secretory activity. Keferstein Bodies A few species of Siphonosoma have small (0.1-0.5 mm), poorly known oval structures on the inner body wall that may have a neurosecretory function (Fig. 78). These were first described by Keferstein (1867), who

Neurosecretion

293

Figure 78. Keferstein body (vesicular organ) from the inside body wall of Siphonosoma cwnanense. CM, circular muscle; CT, cuticle; CV, cavity; GC, glandular cells; LMB, longitudinal muscle band. (From Akesson, 1958.) said they contain an insoluble hook or spine. Subsequent examination showed a muscular connective tissue sheath with glandular cells and a duct leading out of the central cavity to the exterior (Akesson, 1958). The large secretory granules are acidophilic, and the weak innervation has an effector function only. Fusiform Bodies Two of the ten Siphonosoma species (S. arcassonense from France and Spain, and 5. ingens from central California to Oregon) exhibit fusiform bodies. Very little information has followed the original descriptions by Cuenot (1902a) and Fisher (1947), although E. Cutler and DiMichele

294

Nervous System

(1982) published a preliminary report on the microanatomy and possible functions based on old museum material and basic light microscopy. An examination of freshly preserved material using modern techniques is needed. The fusiform bodies are small, terete cylinders (maximum size 7 X 0.35 mm) located in the posterior tip of the body. There are two to six of them, although the larger number occurs only in large worms (Fig. 12). Fisher aptly compared their appearance to a cluster of small nematodes. The central lumen of each fusiform body connects to the trunk coelom via a nonciliated, non-funnel-shaped coelomostome, which may be controlled by a rudimentary sphincter muscle. The opposite end opens to the outside via a small epidermal pore. The outer wall of each body consists of a thin peritoneal layer underlain by a muscular wall consisting of an outer longitudinal layer and an inner circular layer. This arrangement is the reverse of that found in the body wall, where the circular layer is on the outside. This suggests an ontogeny involving invagination. In larger animals (25 cm and above) the central lumen of the fusiform body is lined by a layer of columnar epithelial cells which contain dark-staining spherules of unknown composition. Five regions are discernible in large fusiform bodies (Fig. 79): (1) the coelomostome (5-10% of total length), with irregular muscle fibers; (2) the anterior transition zone (10-15%), with poorly developed columnar cells; (3) the secretory zone (60-70%), with well-developed columnar cells and secretory vesicles; (4) the posterior transitional zone (6-9%) with decreasing size and number of cells; and (5) the terminal zone (3-4%), which has a very small diameter as it passes through the body wall. The refractile granules in the secretory vesicles and lumen are 2-3 jjim in diameter and are most numerous in zone 3. Their absence from zone 1 (they are present but fewer in zones 2, 4, and 5) indicates a coelom-tooutside flow direction controlled by peristaltic contractions of the muscular wall. The two Siphonosoma species that have fusiform bodies live in the northeastern quadrant of the Pacific and Atlantic oceans, separated from all congeneric taxa by thousands of kilometers. These are the only two members of the genus whose ranges do not overlap the widespread S. cumanense. Seven of the eight Siphonosoma species that lack fusiform bodies are tropical or subtropical; the eighth is from northern Japan. The maximum trunk size of the species with fusiform bodies (40-50 cm) may be significant—it is two to three times the trunk size of the other 5/-

Figure 79. Fusiform body of Siphonosoma ingens; cross sections show anatomy of the five zones described in text. A. Coelomostome with irregular muscle fibers. B. Anterior transition zone. C and D. Secretory zone with well-developed columnar cells and secretory vesicles (C is enlarged portion of B showing muscle layers). E. Posterior transitional zone. F. Terminal zone passing through the body wall. Scale = 0.1 mm. BW, body wall; CM, circular muscle layer; LM, longitudinal muscle layer. (Drawn by J. Swartwout.)

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Nervous System

phonosoma species. Whether these two species are relicts of a broadly distributed ancestral population that had similar organs or the result of parallel evolution of two descendant species is unknown. The former view is the more conservative. Two plausible functions have been proposed for the fusiform bodies: excretion and external chemical communication. In support of excretion is the similarity of their form to excretory organs in other invertebrates (Pilgrim, 1978; K. White and Walker, 1981). The refractile spherules suggest the production and secretion of waste. Similar spherules have been described from sipunculan nephridia (Andrews, 1890b; Storch and Welsch, 1972; Ocharan, 1974) and from molluscan nephridia (Galtsoff, 1964; Pirie and George, 1979; George et al., 1980). Second, the fusiform bodies may be pheromone-producing organs. A pheromone-producing function for the terminal organ in the confamiliar genus Sipunculus was proposed by Akesson (1958), who thought that the secretion might serve as a signal to coordinate epidemic spawning. The Sipunculus terminal organ is located at the posterior tip, like the fusiform bodies, but structurally it is more complex and lobular. A reproductive function for fusiform bodies is supported by the fact that they do not develop secretory cells until the worm is quite large. Their presence in only these species that inhabit temperate waters, where spawning times are more restricted and coordination is more critical, may also be significant. Alternatively, the fusiform bodies may produce pheromones that signal conspecific planktonic larvae that the environment is suitable for settling or that warn neighbors of a threat.

IS

Reproduction and Regeneration

In the latter half of the twentieth century, authors have built on a foundation going back to Selenka (1875) and addressed the development of sipunculans from a variety of perspectives. Akesson's (1958, 1961a) study of Phascolion strombus, Nephasoma minutum, and Golfingia elongata included comparisons with earlier studies of G. vulgaris and Phascolopsis gouldii (see Gerould, 1903, 1904, and 1907 for the latter species). Rice described the development of Phascolosoma agassizii, Thysanocardia nigra, Themiste pyroides (1967), and Siphonosoma cumanense (1988b). The 1988 article includes an interesting comparison between S. cumanense and Sipunculus nudus, a member of the same family. The differences between the two species are striking. Amor (1975c) closely observed an Argentinian population of Themiste alutacea (formerly T. petricola). Most sipunculan species have been much less completely studied; only their later development, larval morphology, or larval behavior has been reported (see Rice, 1973, 1978). Rice's review article (1975c) gives one of the best overall summaries of sipunculan reproductive biology. For such a small phylum there is a wide diversity of routes from egg to adult.

Sexual Reproductive System and Modes

Gonads and Gender The gonads are small, transitory strips of tissue within a peritoneal envelope on the body wall just posterior to the origins of the ventral retractor muscles. They sometimes have the appearance of fluffy cotton or the fringe on a wool sweater. Gonadal tissue is obvious only when gametes are being produced. No external or internal sexual dimorphism is known within the phylum, but gender can be determined by examining gametes.

298

Reproduction and Regeneration

In some species the color of the gametes can be seen through the body wall; sperm are often pink. Only one species is known to be hermaphroditic, although there has been some confusion on the matter (Hyman, 1959). That species is Nephasoma minutum (formerly Golfingia minuta, in part), which inhabits shallow waters in the northeastern Atlantic Ocean (Gibbs, 1973; N. Cutler and Cutler, 1986). Eggs and sperm are produced simultaneously, not protandrously (Gibbs, 1975). Self-fertilization does occur, and the eggs are laid in the mother's burrow, a type of primitive brood protection (Akesson, 1958). Facultative parthenogenesis has been reported only in Themiste lageniformis, a species in which males are uncommon (Pilger, 1987). Published and unpublished reports indicate that the sex ratio in populations of this species can be biased toward females by an overwhelming factor of 60-200 times (Keferstein, 1867; Pilger, 1987). Whether or not this is related to environmental stresses, as is the case in some part-time parthenogenic invertebrates such as the cladoceran Daphnia, is not known. The suppression of both male and female gametes (i.e., sterility) was reported in a Japanese Phascolosoma population infected with an endoparasitic copepod. Infected individuals (34% of the population) showed no evidence of sexual activity during the study, which lasted from April through December (Ho et al., 1981). Gametes Gametes are released into the coelom, where they continue the maturation process. Maturation takes six or seven months for the oocytes of Phascolosoma arcuatum and Themiste lageniformis (W. Green, 1975a; Pilger, 1987), and longer in other species. In many populations, gametes at some stage of maturation are present in the coelom throughout the year; in others, such as the Australian P. arcuatum, sperm are present for only a few months of the year. There does not appear to be any correlation between egg size and size of the adult worm, but in an article with excellent illustrations, Rice (1989) pointed out the correlation between egg size and developmental mode. Her table 1 summarizes the egg size, shape, color, and developmental mode for 13 species representing eight genera and six families. Species with planktotrophic larvae tend to have smaller eggs ( < n o \xm) than those with

Sexual Reproduction

299

Figure 80. Sipunculan sperm. A. Themiste pyroides. B. Apionsoma misakianum. C. Aspidosiphon fischeri. Scale = 1 \x,m. (After Rice, 1989, courtesy of M. E. Rice and Olsen and Olsen Publishers and Printers.)

lecithotrophic larvae (125-175 (xm; see Larval Development, below). The three species with direct development have the largest eggs within their respective families (135-280 ji,m). Eggs produced by worms in the class Phascolosomatidea are ovoid, while most species in the class Sipunculidea produce spherical eggs. One exception is Nephasoma minutum, in which direct development occurs from a large but elongate egg. There are also interspecific differences in the amount of yolk, which is correlated with the larva's lifestyle. N. minutum eggs, for example, are both the richest in yolk and the largest, and the hatchling larva feeds on the yolk for two months (Akesson, 1961a). Sipunculan sperm have a primitive form, with a rounded head, a short mitochondrial midpiece with four to five spheres, and an elongate tail (Fig. 80). The form of the acrosomal cap varies somewhat among sipunculan species. The anchoring fiber apparatus in a species of Aspidosiphon resembles the metazoan prototype, with two cone-shaped secondary processes arising from each of the primary ones. This is slightly less complex than the apparatus in Cnidaria sperm and fits the trend toward simplification within the Protostomia. The mitochondria and the nature of the centrioles and basal body (9 + 2 microtubules) support the idea that sipunculan spermatozoa are like the original protostomial type (Klepal, 1987; Reunov and Rice, 1993).

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Reproductive Cycles and Spawning The age at sexual maturity in the ecologically unique species Phascolosoma arcuatum is about two years (W. Green, 1975a). In the more widespread and eurytopic Apionsoma misakiana, sexual maturity occurs at about nine months (Rice, 1981). Rice (i975c:table 1) summarized observations on the spawning cycles of several species in nine genera. The general picture is not unlike that seen in other marine invertebrates. In temperate waters there is a two- or three-month peak in reproductive activity during the summer or early fall; the timing varies with latitude. Phascolosoma agassizii, for example, breed from March to May off central California but from June to August off northern Washington (Rice, 1975c). P. arcuatum spawn during the austral summer (DecemberFebruary) (Green, 1975a), as do Themiste alutacea in Argentina (Amor, 1975b). Exceptions do occur. Thysanocardia nigra (formerly Golfingia pugettensis) off Washington spawn from October to January. The hermaphroditic Nephasoma minutum, which do not produce free-swimming larva, breed from September to November off Sweden and from November to January off England (Gibbs, 1975). Closer to the equator the breeding season extends over a longer period, and tropical populations may have some members breeding at different times throughout the year (Williams, 1977; Rice, 1975c; Rice et al., 1983). In general, sipunculans are more active at night, so it is not surprising that most breeding occurs then (Gerould, 1907; Akesson, 1961a), although daytime breeding sometimes occurs in artificially lighted laboratory populations (Rice, 1975c). The mature gametes collect in the nephridia, and in at least some species the sperm are released first (Gerould, 1907; Akesson, 1958). The presence of sperm in the water stimulates females to release their eggs, and fertilization occurs in the water. The order of release was reversed or random in Themiste lageniformis and Phascolosoma agassizii observed under natural conditions (Williams, 1977; Rice, 1975c). Laboratory observations of different species yielded no consensus on the sequence of gamete release. In some species the females release all their eggs at once, while the males are more conservative, releasing fractions of their sperm in small bursts over several days (Rice, 1988c). However, a female Themiste pyroides was observed to spawn eight times over a six-week period (Rice,

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301

1975c), and a female T. lageniformis spawned five times during a six-day period (Pilger, 1987). Since spawning in temperate latitudes is timed to occur in one season of the year (epidemic type), the existence of a biological clock seems likely. No experiments have been carried out to test this hypothesis, however, so one can only speculate about the roles played by exogenous factors such as temperature and photoperiod, and endogenous controls such as neurosecretory substances. Both types of factors may control spawning.

Gametogenesis and Fertilization Oocytes are in the diplotene stage of prophase I when they are released from the ovary, and the eggs have matured to metaphase I by the time they are laid (Gonse, 1956; Rice, 1975c). The intervening maturation occurs within the coelomic cavity over a period of three to eight months. The amount of yolk added to eggs varies significantly among species, resulting in the production of different-sized eggs as noted in the discussion of gametes above (Akesson, 1961a; Sawada, 1975; Rice, 1989). The egg envelope is made of layered mucoprotein with distinct pores (Fig. 81 A). Spermatozoa are produced in clusters which remain intact until late in the differentiation process. They leave a track through the thick jelly coat when they penetrate the egg envelope (Rice, 1975c). Following the sperm's penetration, the egg resumes meiosis, producing two polar bodies and the haploid female pronucleus. The fusion of the two pronuclei to form the zygote concludes the process of fertilization. The polar bodies mark the animal pole of the zygote.

Cleavage and Gastrulation Even the earliest accounts (e.g., Hatschek, 1883; Gerould, 1907) report that cleavage is spiral, unequal, and holoblastic. Early in the process—by the eight-cell stage—the micromeres of quadrants A, B, and C are equal to, or larger than, the macromeres, in all members of the class Sipunculidea except Sipunculus nudus, which is the only sipunculan known to have micromeres smaller than the macromeres. In the yolk-poor eggs of species in the class Phascolosomatidea the micromeres are the same size as the macromeres. The apical cross (Fig. 82A) in the 48-cell stage is in the

H

I

Figure 81. Development and metamorphosis of Apionsoma misakianum showing gut opening, the formation of coeloms and ciliation, how the egg envelope becomes the cuticle, and changes that occur after settling onto the substratum. A. Unfertilized egg. B. Two-cell stage. C. Trochophore at one day. D. Four-day, premetamorphosis. E. Early pelagosphera at five days. F and G. Pelagosphera larva collected at sea from the side (F) and the front (G). H and I. Lateral and frontal views of larva after two days in

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Figure 82. Early development in sipunculans. Golfingia vulgaris at 48-cell stage showing molluscan cross of the anterior hemisphere. Rosette cells are dotted, cross cells are unshaded, and intermediate cells are barred. Primary prototroch cells are on the periphery. (After Gerould, 1907, with correction.) radial direction, as in mollusks, rather than showing the interradial annelid condition (Rice, 1975c). The 46. cell gives rise to the entomesodermal tissue. Eight of the 10 Sipunculidea species that have been studied undergo gastrulation via simple epiboly (Rice, 1988c), but gastrulation does occur by invagination in S. nudus. A combination of invagination and epiboly is employed by the one Golfingia and the two Phascolosomatidea species that have been studied. The ventral pretrochal stomodeum opens near the site of the blastopore, and the mesodermal bands split to form coeloms via schizocoely (Fig. 83).

the substratum. J. Lateral view of worm after three days in the substratum, with head retracted. A, anus; BO, buccal organ; BR, brain; CU, cuticle; DRM, dorsal retractor muscle; EN, egg envelope; ES, esophagus; IN, intestine; L, lip; LG, lip gland; LP, lip pore; M, metatroch; MO, mouth; N, nephridium; P, prototroch; PRM, posterior retractor muscle; PSG, posterior sacciform gland; S, stomodaeum; SPH, post-metatrochal sphincter; ST, stomach; TO, terminal organ; VNC, ventral nerve cord; VRM, ventral retractor muscle. (After Rice, 1978, courtesy of M. E. Rice.)

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Figure 83. Later development in sipunculans (after Gerould, 1907). A. Surface view of Phascolopsis gouldii trochophore at 20 hours. B. Lateral view of P. gouldii at 48 hours, with egg envelope. C. Dorsal view of metamorphosing Golfingia vulgaris trochophore without egg envelope and prototrochal cilia. D. Lateral view of a 60-hour lecithotrophic pelagosphera G. vulgaris larva with incomplete intestine. E. Lateral view of Sipunculus nudus trochophore with egg envelope split at posterior end prior to shedding (from Hatschek, 1883). A, anus; AT, apical tuft; BO, buccal organ; CU, cuticle; E, eye; EN, egg envelope; IN, intestine; LG, lip gland; M, metatroch; MO, mouth; P, prototroch; PR, preoral cilia; S, stomodaeum; ST, stomach. Larval Development Larval development follows one of the four paths listed below (Fig. 84). Details and variations on these patterns are discussed in Rice, 1975c, 1981, 1988c, and 1993b.

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Figure 84. Four developmental pathways followed by various Sipuncula. Type 1. Direct development with no pelagic stage. Type 2. Pelagic lecithotrophic trochophore that becomes a vermiform phase. Type 3. The pelagic lecithotrophic trochophore metamorphoses into a lecithotrophic pelagosphera larva that subsequently changes into a vermiform phase. Type 4. The pelagic lecithotrophic trochophore metamorphoses into a planktotrophic pelagosphera larva. After an extended planktonic existence during which it increases in size, this metamorphoses a second time into a vermiform juvenile. (After Rice, 1975c, courtesy of M. E. Rice.)

I. Direct lecithotrophic development with no pelagic stage (D). Found in 3 species from three genera, representing all three families of the order Golfingiiformes. II. One lecithotrophic pelagic stage: trochophore (T). Found in 2 species, each representing one of the two orders in the class Sipunculidea. III. Two pelagic stages: trochophore and lecithotrophic pelagosphera (LP). In 7 species from four genera representing three families in the Golfingiiformes. IV. Two pelagic stages: trochophore and planktotrophic pelagosphera (PP). Found in 10 species; 3 from the class Sipunculidea, representing three genera in two families, one from each order. The remaining 7 examples are from four of the six genera in both orders and families of the class Phascolosomatidea (Table 3).

306

Reproduction and Regeneration Table 3. Larval developmental types, distributed by taxa Type

Class Sipunculidea Order Sipunculiformes Family Sipunculidae Sipunculus Siphonosoma Phascolopsis Order Golfingiiformes Family Golfingiidae Golfingia Nephasoma Thysanocardia Family Phascolionidae Phascolion Family Themistidae Themiste Class Phascolosomatidea Order Phascolosomatiformes Family Phascolosomatidae Phascolosoma Apionsoma Antillesoma Order Aspidosiphoniformes Family Aspidosiphonidae Aspidosiphon

I

II

III

IV

— — —

— — X

— — —

Xa X —

— X —

— — —

XX — X

— X —

X

X

X

—

X

—

XXX

—

— — —

— — —

— — —

XXX X X

—

—

—

XX

Notes: X = one species. No data for five genera. "Somewhat unique pattern.

Species with a trochophore larva commonly spend 2-4 days in this stage (8-10 days in a few species). The lecithotrophic larval stage lasts from 2 days to two weeks, and the planktotrophic stage, when present, lasts on the order of one to three months, occasionally up to six months. The trochophore is fairly typical. It has a broad equatorial prototroch, a ventral metatroch, an apical tuft of sensory cilia, and a complete tripartite mesodermal gut (Figs. 81, 82). The term trochophore can be confusing, and Salvini-Plawen (1973) proposed that it should be restricted to the Annelida and Echiura, a point of view that does not seem to have broad support. The trochophore larva has an ectodermally derived ventral nerve cord, inverted ocelli, and is positively phototaxic (Akesson, 1958, 1961). The details of ciliation and origins of various muscle systems vary from

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species to species. The larval cuticle is derived from the egg envelope in most species but is created de novo in others. From a trochophore, some species elongate posterior to the prototroch into a benthic vermiform juvenile. Those that metamorphose into planktonic pelagosphera larvae will later change into the juvenile worm (Figs. 81, 84). The pattern in 5. nudus is unique and is considered highly modified. Differences include the fate of the egg envelope (completely cast off during change to pelagosphera rather than becoming the cuticle), and the uniformly ciliated trochophore rather than the more usual narrow prototrochal band (Rice, 1988b). Read Hyman, 1959, for an interesting summary of the research on Sipunculus larvae, which were first named Pelagosphaera and treated as adults of a distinct genus. Much of the early work with these larvae was flawed because it was based on contracted preserved material with withdrawn anterior ends. One of the first to use fresh material was Jagersten (1963), who provided excellent drawings of what he characterized as hippopotamus-like heads. Two other Sipunculus species were drawn from living material by Murina (1965). Pelagosphera larvae have well-developed metatrochal cilia and a characteristic head. Besides the obvious behavioral and ecological differences, the internal morphological differences from the adult include the larger number of retractor muscles, eyespots, and body wall muscles. The final metamorphosis from pelagic larva to adult includes organogenesis of several systems, including the introvert and tentacles. The final metamorphosis can be induced in a competent larva by exposing it to sediment previously occupied by adults of the same species. Hall and Scheltema (1966, 1975b) described ten open-ocean planktonic sipunculan larvae. These authors focused on cuticular structures, but they also considered pigmentation and other organ systems such as the body wall musculature. They were unable to relate the larvae to specific adult forms, but among the larvae described were representatives of at least the genera Aspidosiphon, Phascolosoma, and Sipunculus. The presence of multiple retractor muscles in larvae (more pairs than in adults) is intriguing, but the question of whether this difference is due to fusion or to loss during metamorphosis is still unanswered. The larvae described by Hall and Scheltema were kept alive in the laboratory for several months, and a few did undergo metamorphosis. Among the interesting facts gleaned by those authors is that larvae do expend energy to maintain their vertical position in the water column.

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Reproduction and Regeneration

Larval Dispersal and Settlement Most shallow-water tropical and warm temperate species are widely dispersed by oceanic currents. The teleplanic larval stage lasts two to six months, adequate time to allow transoceanic transport or island colonization (Hall and Scheltema, 1975a; R. Scheltema, 1986a; R. Scheltema and Rice, 1990). During the period 1975-1990, R. Scheltema published seven articles on sipunculan larvae dispersal; the bulk of that work is discussed in Chapter 16 (see Zoogeography). Rice (1986) studied settlement and metamorphosis in a Florida population of Apionsoma misakiana. The settlement-inducing substance (SIS) is species-specific, stable for at least eight days, heat-labile (autoclaving destroys it but freezing has no effect), and has a molecular weight less than 500. Larvae responded to SIS in the seawater by settling, but the response was stronger if sediment was also present, and stronger still if adults were present in the sediment. The possibility that the SIS acts synergistically with bacterial film on the sediment has not been ruled out. Larvae can attach to sediment temporarily using the posterior retractile terminal organ, which has sensory cells and produces an adhesive mucus (Ruppert and Rice, 1983). Ruppert and Rice compared this organ with adhesive organs in other metazoans and concluded that the sipunculan terminal organ evolved independently within the phylum.

Asexual Reproduction

Parthenogenesis Parthenogenesis is a "partial" sexual process in that although meiosis occurs and oocytes are formed, no syngamy occurs, and it is thus, by definition, not sexual reproduction. Facultative parthenogenesis, the spontaneous development of unfertilized eggs into normal larvae, appears to be common in Florida Themiste lageniformis, where females outnumber males 24 to 1 (Pilger, 1987). This mode of reproduction is unknown in other members of the phylum. Budding Unequal transverse fission has been observed in two species: Aspidosiphon elegans (Rice, 1970) and a species belonging to the family Sipunculidae (Rajulu and Krishnan, 1969; Rajulu, 1975).

Asexual Reproduction

309

Figure 85. The dissected bud and posterior end of Aspidosiphon elegans showing internal organs of parent and offspring. The anterior parts of the offspring will develop from the epidermal invagination. C, collar; E, esophagus; EI, epidermal invaginations; IA, ascending intestine; ID, descending intestine; N, nephndium; RM, retractor muscle; S, internal acellular partition across the stricture; SM, spindle muscle; VNC, ventral nerve cord. (After Rice, 1970, courtesy of M. E. Rice, © 1970 by the AAAS.)

In A. elegans a constriction appears near the end of the trunk, and essential internal organs—including the introvert, retractor muscles, anterior intestine, and nephridia—are replicated in the smaller "daughter" part (Fig. 85). The anterior "parent" only needs to regenerate the posterior body wall as separation occurs. About 15% of the individuals collected in a Caribbean coral community were budding (E. Cutler, pers. observ.). Thus, this seems to be a natural phenomenon and not the result of laboratoryinduced stress. The budding Sipunculidae species was identified as Sipunculus robustus, but my superficial inspection of the specimen indicated that it may

3io

Reproduction and Regeneration

well be a Siphonosoma species, most likely S. cumanense. This speculation is supported by personal observations of living members of the latter species collected in Madagascar, which underwent a "pinching off" into subsets when kept for several days in stale seawater. Other than the fact that fission has not been observed in S. cumanense under natural conditions, and seems to occur only in response to environmental stress, it is similar to the sequence in Aspidosiphon. The "daughter" is the smaller posterior part, up to one-third of the trunk. The posterior half may form three to five buds, including lateral ones. The new central nervous system, contractile vessel, set of retractor muscles, and digestive system are produced before separation. The new introvert, tentacles, and anus are formed afterward. Based on thin sections made after three days, the beginning of this process involves the production of an elongate girdlelike "blastema" from coelomocytes that form around the gut. From this blastema the central nervous system develops first, quickly joining with the old ventral nerve cord. The digestive, muscular, and excretory systems develop later, and the final closing of the wound in the parent follows separation. The information on the clusters of lateral buds reported in a few worms is incomplete, and there appear to be minor differences in the sequence of events.

Regeneration

Although it is not a mode of reproduction, regeneration is a developmental process. Neuroblasts that function in regeneration have been identified between the two lateral strands of the ventral nerve cord in Golfingia elongata (Akesson, 1961a). Removal of the distal centimeter of introvert from Siphonosoma cumanense was followed one day later by the closure of the cut end by a blastema (Kido and Kishida, 1961). New epithelium grew from the old epithelium as a network over the blastema. Four cell types became evident. Although it proved impossible to follow their subsequent development, two seemed to be coelomic cells. By day 5 a new mouth had formed; muscle layers were partly differentiated by day 6. At this time the epithelium was in good order but no defined cuticle was visible. The nerve cord regeneration string in Phascolion strombus has electrondense granules with diameters of 5000 A (Storch and Moritz, 1970). When the introvert was amputated, the granule-bearing cells migrated anteriorly

Regeneration

3ii

to form a clublike mass of cells rich in glycogen and lipids. The inclusions were extruded as fibers in the interstitial spaces, and a new cuticle was formed from secretions of these cells. New epithelial cells rich in rough endoplasmic reticulum developed, and amoebocytes produced muscle tissue. This evidence substantiates observations dating back to the late 1800s (Biilow, 1883) on the ability of sipunculans to regenerate lost or removed parts, particularly the introvert, within a few weeks. This regeneration was observed in Phascolion strombus, Nephasoma minutum (Schleip, 1934a, 1934b), Aspidosiphon muelleri, Golfingia vulgaris, Phascolosoma granulation, and Sipunculus nudus (Wegener, 1938). All but one species replaced the distal end of the introvert. As in so many other areas, the exception is 5. nudus, which appears to lack this ability. If a section of the introvert was removed from a worm with a partly retracted introvert, however, the missing segment could be replaced, reconnecting the original head to the body with a new "neck." A repeat of this experiment would be useful since these results are so unlike those reported for other sipunculans. Wegener and Schleip (cited above) observed regenerative tissue associated with the ventral nerve cord. Damaged or cut posterior ends can also be regenerated, although the success rate is higher when the intestine is not involved (Andrews, 1890b; Spengel, 1912; Schleip, 1934a, 1934b).

Part III

16

Zoogeography and Evolution

Zoogeography

This chapter gathers together what is known about sipunculan endemism and centers of cladogenesis, including both data from the literature and my own assumptions. Chapter 17 applies this information to the individual genera, and Chapter 18 combines what is known about sipunculan evolution and phylogenetic relationships with a historical overview of the world's oceans in an attempt to weave the threads of our knowledge into the multicolored tapestry of sipunculan evolution through geological time. To paraphrase R. Scheltema (1989), the contemporary spatial distribution of sipunculan species is limited by their ecological history and by past accidents, among other factors. We can explain some of these variables (see Chapter 19), but much is still unknown.* What follows here is descriptive and general. More detailed analyses are planned for the future.

The Quality of the Database

The current picture of sipunculan distribution is fuzzy and full of holes, rather like an unfinished Impressionist painting. We have some idea of the overall pattern of sipunculan distribution, but only a few areas have been examined in sufficient detail to engender confidence about the subject. This is the inevitable result of nonuniform, nonrandom sampling by oceanographic expeditions and marine biologists, and it is true of many benthic marine invertebrates, especially the smaller, soft-bodied infaunal taxa. Nor is it only deep-water habitats that have been incompletely sampled. The * At the time of this writing, a database of specific collection locations of sipunculans that includes latitude, longitude, depth, date, source, and species name is being compiled in the DOS-compatible dBASE III Plus format. Interested readers may request copies from the author.

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shallow waters around much of South America, Indonesia, and the Philippines are poorly known as well. When one states where a species lives, what is actually being described is where that species has been collected. If an area has been thoroughly sampled, it is fairly safe to discuss species distributions in that area. To expand from the secure base of a particular bay or transect to describe distributions in the entire world, however, is to leap into partially unknown space. Having stated this, a leap of faith (assuming an ordered world) will now be undertaken.

Species Value

In past zoogeographical discussions, equal weight has been given to two rather different kinds of species: (i) taxa regularly collected over decades by more than one biologist and represented by many specimens, and (2) species known from only one or two individuals from a single location and reported by only one biologist. Thus, the available database contains two types of "endemic species." The first type might be called "tested, actual endemics"; that is, they are species whose endemicity has been tested at least once subsequent to the original observation. In addition one might include in this category species that have been reported only once, but by an experienced systematist who understands the biological species concept (i.e., who appreciates that variation is possible within a sipunculan deme), and are based on a significant number of individuals (i.e., more than three or four). The second type, "untested, potential endemics," are species that have been reported only once and are based on fewer than five worms, or species reported by a person lacking experience with sipunculans or one working within a typological species framework. When species in this category are included in zoogeographical analyses, an inflated and false impression of the number of endemic taxa can result. The diminished significance of untested endemics in this analysis and my inclusion of recent taxonomic revisions (resulting in about half the putative species being reduced to junior synonyms) have made the outcome of the present analysis different from earlier ones (Selenka et al., 1883; Herubel, 1903a, 1907; Murina, 1971c, 1975a; Amor, I975d; E. Cutler, 1975b).

Endemism and Centers of Origin

315

Endemism and Centers of Origin

An endemic taxon is one that lives only in a circumscribed area. The size of the area is arbitrarily defined by the investigator, and marine areas have historically been much larger, with less well defined boundaries, than terrestrial ones (Kay, 1979). Since the days of Darwin and Wallace, biogeographers have used the existence of a high percentage of endemic species in a given area to support the thesis that such an area is a "center of origin." This idea is based on the assumption that land masses have always been where they are today. Previous analyses of sipunculans seem to have implicitly made the same assumption. While the phylum Sipuncula undoubtedly originated in a particular place, it would be a mistake to assume that all sipunculan taxa originated in that same place. It is more useful to think in terms of many centers of origin, including origins of families or genera, not just species. One example of a group with no single center of origin but with rapid dispersal from several different places is the Cenozoic benthic foraminifera of North American waters (Buzas and Culver, 1986). One must also avoid thinking that the world's oceans and land masses in Paleozoic and Mesozoic times, when most of the higher sipunculan taxa came into existence, were like they are today. Three brief examples will serve to illustrate this point (Chapter 18 discusses the issue in greater detail). (1) Although the phylum Sipuncula has existed for 500 million years, the Caribbean has been separated from the Pacific for only the past 3.5 million years (less than 1 % of the time). (2) The present boundary area between the Pacific and Indian oceans (the Indo-Malayian region) was established less than 20 million years ago (4% of the time the phylum has existed). (3) An Atlantic Ocean extending from Arctic to Antarctic waters did not exist before some 60 million years ago. The work of historical biogeographers thus includes a consideration of time as well as temperature, depth, current direction, and sea level. What is continental shelf today may have been dry land several thousand years ago. What is temperate water today was tropical a few million years ago, and so on. Areas rich in species and including many endemics today may be rather new habitats that are not historically significant as centers of origin or distribution. Alternatively, species-rich areas may represent remnants of suitable habitats that were once much larger, as demonstrated by the post-Miocene

3i6

Zoogeography

reef corals of Australia and New Zealand (Fleming, 1978). The coral, sea grasses, and associated species extended over much larger areas during the Cretaceous when the Tethys Sea existed. The current pattern is the result of extinctions and range shrinkages caused by abiotic and biotic factors (Knox, 1978). The same scenario has been documented for marine crustaceans in the Southern Hemisphere (Newman, 1991). After examining five possible hypotheses, including vicariance events associated with plate tectonics that are relevant for terrestrial and freshwater fauna (e.g., Mayr, 1988, for birds), Newman concluded that the endemic forms are post-Mesozoic relicts of either formerly widespread tropical taxa or remnants left over after the extinction of the northern portions of amphitropical (i.e., occurring on both sides of the equator) barnacle species. Additionally, disjunct distributions may be the outcome of widespread local extinctions resulting from changing conditions such as periodic cooling during Pleistocene glaciations (Fleming, 1978), decline in primary productivity after the Miocene (Vermeij, 1989), or the demise of the Tethys Sea in the Paleogene (Kay, 1979). The likelihood of vicariance events being entirely responsible for bipolar or antitropical disjunct distributions was discounted by Lindberg (1991), who supported multiple mechanisms, including the probability of several biotic interchanges between the hemispheres during times when the tropics were less of a thermal barrier (i.e., during Neogene glaciations). There are other explanations for existing patterns of endemicity as well, especially for marine taxa without a fossil record. Without entering into the debate about the linkage between centers of endemism and centers of origin (see Knox, 1978), I judge the concept to be of such dubious value for sipunculans that I do not use it here. Dispersal, Boundaries, and Biogeographic Units Most sipunculans are capable of dispersing their planktonic larvae over hundreds or thousands of kilometers fairly quickly, and it is thus possible for these infaunal worms to be distributed over large areas. This makes the zoogeographical boundaries of a species's range difficult to define and delimit (Rice, 1981; R. Scheltema, 1975, 1986a, 1986b, 1988; R. Scheltema and Rice, 1990). Most often, ranges appear to be determined by water temperature, but bottom topography and water currents are important fac-

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317

tors, especially at bathyal and abyssal depths, where water temperature varies little with latitude. The importance of bottom topography and currents is evident at various points on the Atlantic continental slope but is best documented off Cape Lookout, N.C. (E. Cutler, 1968b, 1975a; E. Cutler and Doble, 1979; E. Cutler and Cutler, 1987b). It is difficult to generalize about sipunculans' dispersal ability because some taxa travel much greater distances than others. Although it may be true that the east Pacific barrier (EPB) is the most effective obstruction to the dispersal of contemporary shallow-water tropical fauna, it is not impermeable. Grigg and Hey (1992) found 4% of Pacific reef-building corals and 14% of the molluscs to be amphi-Pacific. It takes free-floating larvae 55-70 days to cross the shortest distance (Christmas Island to the Galapagos) and up to 155 days to cross elsewhere, and most coral larvae do not live that long. While the EPB is an effective filter barrier (R. Scheltema, 1986b), 11 shallow-water sipunculan species from seven genera are known to be amphi-Pacific (Sipunculus polymyotus, S. phalloides, S. nudus, Siphonosoma vastum, Phascolosoma (Edmondsius) pectinatum, P. nigrescens, P. perlucens, Antillesoma antillarum, Apionsoma misakianum, Aspidosiphon (Paraspidosiphon) coyi, Lithacrosiphon cristatus). Many more species are present in the western but not the eastern Pacific. Sipunculans do not actively migrate; rather, their larvae are passively transported within the currents that form the highways of the sea. Asymmetrical invasions brought about by passive transport in currents that are largely (but never entirely) unidirectional have been noted in several of the world's oceans; for example, from the Red Sea into the Mediterranean, from the North Pacific to the North Atlantic via the Arctic, from east to west in the North Atlantic, and from west to east in the tropical Pacific (Vermeij, 1991a, 1991b). These are generalizations, and there are exceptions. For example the near-shore flora in the Arctic Ocean does not follow the same pattern as the fauna (Dunton 1992). More than 120 species of Red Sea marine organisms (plants and animals) have colonized the eastern Mediterranean Sea since the Suez Canal opened in 1869, but migration in the reverse direction has been limited to 10 species. This is largely a reflection of the direction and rate of current flow at the time of year when reproduction occurs in many Red Sea species (Agur and Safriel, 1981). I should point out, however, that Por 0975) found no sipunculans or sipunculan larvae in the Suez Canal and

3i8

Zoogeography

strongly suggested that dispersal of sipunculans along this route was very unlikely—in either direction—because of the extreme euryosmotic habitat and lack of hard substrate for rock-boring taxa. R. Scheltema (1992) set forth several arguments to put to rest the confusion about the role of passive dispersal in determining the present distribution of benthic invertebrates (also see Kay, 1979). For example, the old generalization that most larvae have fixed and short lives was disproved by Scheltema's laboratory and field work. Sipunculan teleplanic larvae retain their competency to metamorphose for long periods (two to six months), and dispersion is not a random process. It occurs along distinct corridors formed by the major current systems. One outcome of this method of dispersal is the widely different degrees of endemism between terrestrial and marine island-dwelling invertebrates (high for the former, low for the latter). Finally, Scheltema challenged the assertion made by vicariance biogeographers that since species distributions are nonrandom, one cannot invoke dispersal processes to explain them (Nelson and Platnick, 1980). This idea is based on the assumption that dispersal is a random process; but clearly it is not. The three-dimensional nature of the oceans adds to the complexity of any analysis. To place a species that has been reported from 880 m off New Zealand (Phascolosoma saprophagicum) on the list of Indo-West Pacific endemics along with a species from intertidal coral off Queensland {Themiste variospinosa) is to ignore significant ecological differences. Adding to this list a species from shelf water in the Red Sea and northwestern Indian Ocean (Sipunculus longipapillosus) means ignoring the gap of thousands of kilometers between them. Such combined lists lose zoogeographical meaning. Meaningful units for analysis must be small, in both vertical and horizontal dimensions—but how small? One cannot neatly separate the shallow from the deep-water species, or warm-water from cold-water taxa. How cold is cold, and how deep is deep, and should one have separate categories for cold-shallow and cold-deep species, etc.? Clearly, marine worms cannot be made to fit into discrete analytical sets as can freshwater or island-dwelling organisms. Subdividing the world's oceans into quadrants or cubes for numerical (i.e., vicariance) analyses is artificial and subjective. Ekman (1967) and Briggs (1974) presented broad pictures of marine zoogeography, but to do so they had to dissect the oceans along arbitrary and ill-defined thermal,

Endemism and Centers of Origin

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vertical, and horizontal lines. At this writing I find no justification for submitting sipunculan data to this type of segregation. A good reason not to do so is provided by the striking difference between the sipunculans and the other taxa in the Hawaiian Islands. Ekman set these islands apart from the Central Pacific Island subregion based on the large number of endemic species, but there are no endemic sipunculans in this archipelago; most of those present have very wide ranges. The Mediterranean Sea is another example of a restricted region with no endemic sipunculans despite the presence of many endemic invertebrates of other taxa (e.g., the 15 endemic chalimid sponges; see de Weerdt, 1989). Looking at only the shallow-water species in an area, as is so often done, biases the data and could mask valuable evolutionary information. Given all these factors, no formal analysis of endemic species is presented here. Cosmopolitan Species If endemic species are at one end of a zoogeographical continuum, then cosmopolitan species are at the opposite end and are worthy of a brief comment. Taylor (1977), who studied Cambrian trilobites, questioned whether widespread species are widespread because their tolerances are broad (eurytopic) or because suitable habitats are readily available and cover large areas. The eight sipunculan genera with more than six species all contain one to three species that are much more widespread than their congeners. In some genera these species live in habitats typical of the genus: the widely dispersed Nephasoma species all live in cold water; Phascolion strombus is generally confined to cold water; and Siphonosoma cumanense and the three most cosmopolitan Phascolosoma species typically live in warm, shallow habitats. In several cases, however, cosmopolitan species are very eurytopic and live in habitats not typical for the genus as a whole. Widespread species that live in water cooler than most species in their genus prefer include Sipunculus nudus, Phascolosoma stephensoni, Aspidosiphon zinni, and A. muelleri. Alternatively, a few extend into warmer than "normal" habitats; for example, Golfingia margaritacea and Themiste lageniformis. The importance of cosmopolitan species in the evolutionary framework is uncertain. One could argue that they represent ancestral species that gave rise to descendants as they spread around the world, or that their

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Zoogeography

genes give them a selective advantage. In this phylum it appears that the latter is more often the case in species that live in normal or cooler than normal habitats. For reasons I will present later, however, the pair of species that live in warmer than normal habitats may well represent ancestral taxa. Finally, it is possible that more than one species is present within some very large populations. Cryptic and sibling species exist in other taxa, and there is no reason to assume that there are none in the phylum Sipuncula. Until appropriate objective tests are applied to such taxa, however, the true significance of cosmopolitan species must remain on the list of unsolved mysteries.

17

Generic Analyses: Distribution Summary and Cladogenesis

The analyses presented in this chapter depend on various ad hoc explanations, including dispersal and local extinctions. I have not attempted a vicariance analysis, both for the reasons stated in Chapter 16 and because there is a dearth of species-level cladograms. Given our current limited array of attributes, a severe shortage of synapomorphies exists. Someday this material should be approached again, when more diverse data are available. The analyses in this chapter include untested endemics (UE, as defined in Chapter 16), but these are identified as such. These are of doubtful zoogeographical significance and should be omitted from more quantitative analyses.

Family Sipunculidae

Sipunculus and Xenosiphon Of the 13 included species and subspecies, 6 (46%) live in shallow, warm waters of the western Atlantic, Caribbean, or eastern Pacific—the Atlanto-East Pacific (AEP) of Ekman (1967). Four are endemic there: S. marcusi, S. phalloides phalloides, S. polymyotus, and X. branchiatus. Only 2 species are also found outside this area: 5. nudus is circumsubtropicalwarm temperate, and S. robustus occurs in the tropical Indian and west Pacific oceans (IWP). Most of the remaining shallow warm-water taxa are quite restricted in distribution. S. longipapillosus is known from the northwestern Indian Ocean and the Red Sea, and S. phalloides inclusus is from Indonesia and southern Japan. 5. (Austrosiphon) indicus is widely distributed in the IWP, X. absconditus is scattered from the Red Sea across to the western Pacific, and 5. (A.) mundanus mundanus is limited to the western Pacific. There-

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Distribution and Cladogenesis

fore, there are seven species or subspecies (54%) in the IWP—five endemic to that region. The two deep cold-water species, anomalies in this family, are 5. norvegicus (100-3000 m) and 5. lomonossovi (2500-4300 m). Both occur in the North Atlantic and (less commonly) elsewhere, but not in the eastern Pacific, southern Atlantic, or Antarctic. Only the former extends into the Indian Ocean. Center of Cladogenesis. Significant cladogenesis seems to have occurred in two places: the shallow Indo-Malayian region during the early Cenozoic, for a part of the nominate subgenus and 5. (Austrosiphon); and, during the later Cenozoic, the American Tethys Sea, which subsequently became the Caribbean-tropical eastern Pacific. This area was important for several members of the nominate subgenus, possibly Xenosiphon, and, in its deeper part, the cold-water Sipunculus species. Siphonosoma Only one of the 10 shallow-water species is broadly distributed: S. cumanense is almost circumtropical but apparently absent from the eastern sides of the Atlantic and Pacific oceans. Three species have been reported from several localities in the IWP (S. australe, S. rotumanum, and S. vastum), and the last has also been collected on the Pacific coast of Costa Rica. In the western Pacific, S. funafuti and 5. boholense have been found at only a few locations. The four remaining species live in very limited areas of temperate shallow water: S. arcassonense (France and Spain), 5. ingens (California), S. mourense (central Japan), and S. dayi (Natal, South Africa). The first two species are separated from the other Siphonosoma species by thousands of kilometers, and they are the only two members of the genus whose ranges do not overlap with S. cumanense. They are also the only two sipunculans with the enigmatic fusiform bodies. An analysis of regional endemism in this genus quickly shows the IWP to be favored, with five of the ten species confined to this region. None are restricted to the AEP; only two widely dispersed species live there. Center of Cladogenesis. Siphonosoma clearly underwent most of its radiation in the central IWP. The number of cool-water endemic species (one each in Japan, California, and France) together with the possible descendant Phascolopsis, from the northeastern coast of the United States, is intriguing. A plausible scenario is the following: Each species could be descended from a single widespread polymorphic ancestor which lived in

Family Golfingiidae

323

northern latitudes during the Miocene or Pliocene when the water was considerably warmer. Speciation could have occurred as eurythermal remnants of this hypothetical population were left behind as the main thermophylic Siphonosoma stock was forced southward along with the warm water. As these ancestral demes were probably small, genetic drift may have played an important role. These new allopatric populations would have responded to different selective pressures that were working on different gene pools. Siphonomecus and Phascolopsis These genera are monotypic, and each has a very restricted range in the western Atlantic. S. multicinctus is known from the southeastern United States (South Carolina to western Florida). P. gouldii lives along the Atlantic coast of Canada and the northeastern United States (rare from Long Island to northern Florida). Center of Cladogenesis. No evident speciation has occurred within these genera. It is safe to assume that these two taxa originated in the western Atlantic where they presently reside, one in cool-temperate and one in subtropical water. It is possible that both taxa evolved from a nowextinct Siphonosoma population after the closing of the Panamanian land barrier in the Pliocene.

Family Golfingiidae

Golfingia Most species in the nominate subgenus inhabit cold subtidal water at depths of 2-6800 m. The unique G. (Spinata) pectinatoides is very different: it lives in tropical coral sands in the IWP. A similar habitat is occupied by G. vulgaris herdmani in shallow Indian Ocean waters. A third exception is the least derived member of its subgenus, G. (G.) elongata, because some populations live in intertidal warm-temperate waters. Of particular interest is the common occurrence of two members of this genus (G. anderssoni and the endemic G. margaritacea ohlini) in the far southern seas at latitudes between 45 and 750 S. Less commonly one also finds G. margaritacea margaritacea and G. muricaudata in the far south. Two endemic species are scattered over the northeastern Atlantic (G. iniqua) and South Africa (G. capensis). Two species based on single records

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Distribution and Cladogenesis

(untested endemics) come from East Africa (G. mirabilis) and northwestern Pacific (G. birsteini). Eight of the 12 species and subspecies (67%) are found in some part of the Atlantic Ocean. The four non-Atlantic taxa are G. mirabilis (UE), G. birsteini (UE), G. vulgaris herdmani, and G. (S.) pectinatoides (one subspecies, one species from the non-nominate subgenus, and the two untested endemics). The five species in the Indian Ocean seem to be restricted to the eastern, southern, and western borders and are absent from the central and northern parts. The Pacific is home to nine Golfingia taxa (75%). The three that are absent (G. capensis, G. iniqua, and G. mirabilis [UE]) have very restricted ranges in the Atlantic or the western Indian Ocean. As is the case in other genera as well, the deeper-water taxa appear to be more widely dispersed; 60% of those collected more than once are found in both the Atlantic and Pacific oceans. The fact that Golfingia species live at greater depths in the lower latitudes (known as equatorial submergence) has led some biologists to suggest that some species are bipolar in distribution; however, this may be only an artifact of the difficulty of collecting low-density populations at great depths. For some species, amphitropical would be a more descriptive term than bipolar, since they are more common at middle latitudes than at polar ones. Center of Cladogenesis. It is likely that the ancestral subgenus G. (Spinata) originated in the warm, shallow Panthalassa (precursor of the Pacific, also called the Eo-Pacific) during the early Paleozoic. This taxon produced the nominate subgenus, which appears to have used the far southern seas as a major center of cladogenesis and then probably radiated northward, following the spread of cold water during the late Mesozoic and Tertiary. The absence in the southern and central Pacific Ocean of widespread species such as G. margaritacea and G. muricaudata poses a problem, but this can be explained by local extinctions. Alternatively one would have to assume a northward dispersal route through the Atlantic, across the Arctic (against the prevailing surface currents; perhaps they were benthipelagic larvae?) to the North Pacific. Nephasoma Six of the 27 species and subspecies are known from single reports, including N. abyssorum benhami, N.filiforme (UE), and N. tasmaniense

Family Golfingiidae

325

(UE), plus 3 based on single worms (N. laetmophilum [UE], N. multiaraneusa [UE], and N. vitjazi [UE]). Since most of these are untested endemics, their very limited ranges should not be seriously considered. Despite the fact that 13 "tested" taxa are restricted to one ocean, there does not appear to be any one center of endemism. The richest fauna is in the Atlantic, with 16 taxa (59%). Seven of the 16 live only in northern latitudes, and 6 are endemics: N. bulbosum, N. lilljeborgi, N. minutum, N. multiaraneusa (UE), N. rimicola, and N. wodjanizkii elisae. The seventh North Atlantic species, N. constrictum, has recently been recorded from the southwestern Indian Ocean. None of the other 9 Atlantic taxa is restricted to southern waters, although N. constricticervix has not been collected outside the Atlantic. Five taxa (N. abyssorum abyssorum, N. capilleforme, N. diaphanes corrugatum, and N. eremitd) live throughout the Atlantic and in the Pacific, and 3 (N. confusum, N. diaphanes diaphanes and N. pellucidum pellucidum) are found in these two oceans plus the Indian Ocean. Of the 13 taxa living in the Pacific Ocean (48%), 6 are endemic there (22%): N. cutleri, N. laetmophilum (UE), N. novaezealandiae, N. pellucidum subhamatum, N. vitjazi (UE), and N. wodjanizkii wodjanizkii. The remaining 7 species also occur in the Atlantic Ocean. Only 7 species (26%) have been collected in the Indian Ocean, but 4 of these are endemic: N. (Cutlerensis) rutilofuscum, N. filiforme (UE), N. schuttei, and N. tasmaniense (UE). The first is from the African margin (and the non-nominate subgenus), and the other 3 are from the AustraliaIndonesia region (only one tested endemic). Two Nephasoma live in the Antarctic, N. confusum and N. abyssorum benhami (the latter is found nowhere else). The Arctic is home for 3 taxa, but all are common in the North Atlantic and elsewhere as well. It is clear that Nephasoma is the deep-water genus, with 9 species occurring at depths greater than 4000 m and 21 (78%) at depths greater than 1000 m. Of the 6 remaining species, 3 have been collected only once, but 3 (N. minutum, N. rimicola, and N. schuttei) are clearly intertidal and shelf species. A few eurybathyal species fit both catagories: N. (C.) rutilofuscum, 1-1500 m; N. pellucidum, 1-1600 m; N. confusum, 4-4300 m; and N. eremita, 20-2000 m. Center of Cladogenesis. The species richness in the deeper parts of the northern Atlantic and Pacific oceans point to these cold bathyal and abyssal waters as areas of rapid speciation. Despite the probability that most speciation must have occurred after the oceans deepened and cooled in

326

Distribution and Cladogenesis

mid-Tertiary times, the genus probably originated in the Permian or Triassic. Thysanocardia The three species in this genus appear to have nonoverlapping ranges in cool shelf and upper slope waters. The most restricted is T. procera, which is found only in the northeastern Atlantic. The others are more broadly dispersed: T. catharinae in the rest of the Atlantic Ocean, off East Africa, and off Peru (Murina's 1989 Vietnam record may be a new species); and T. nigra in the northern and western Pacific Ocean. No records of this genus exist from Australian waters. Center of Cladogenesis. This primarily northern genus probably originated in the North Atlantic during the late Tertiary. It underwent limited cladogenesis as it spread, perhaps westward via the Tethys Sea, or possibly via subsurface Arctic currents. The reverse (Pacific origin and migration into the Atlantic via the Arctic) is not unthinkable.

Family Phascolionidae

Phascolion Three species taxa have significant populations in all three of the world's oceans, P. strombus strombus being the most widely distributed and eurytopic. Two deep-water species, P. (Montuga) lutense and P. (M.) pacificum, are close seconds throughout the northern and southern Atlantic and Pacific, but they have been found only in the southern Indian Ocean (i.e., they are absent from low latitudes). An additional three species (P. (Isomya) hedraeum, P. (Lesenka) hupferi, and P. (I.) tuberculosum) occur less broadly in both the Atlantic and Pacific oceans. In addition to the common and widespread occurrence of a few species in the Atlantic Ocean, 6 of the 13 species residing there are endemic along the western side, and these 6 have all been described since 1972: P. (L.) cryptum, P. (I.) gerardi, P. medusae, P. (I.) microspheroidis, P. psammophilus, and P. caupo. The last species also lives in the northeastern Atlantic. Surprisingly, 20 taxa (70%) have been recorded from the IWP, and 12 (43%) are endemic: P. hibridum, P. (I.) lucifugax, P. pharetratum, P. (L.)

Family Phascolionidae

327

rectum, P. strombus cronullae, P. ushakovi (UE), P. (L.) valdiviae summatrense, P. valdiviae valdiviae, P. abnorme, P. (Villiophora) cirratum, P. megaethi, and P. robertsoni; the last 4 live only in the western Indian Ocean and Red Sea. Of the 8 nonendemics, 7 extend into the Atlantic Ocean in deeper water, and 1, P. (I.) convestitum, only reaches into the Mediterranean Sea. Aside from the three widespread eurytopic deep-water species noted above, the eastern half of the Pacific Ocean is almost devoid of Phascolion. The single specimen of P. bogorovi (UE) collected from the Peru-Chile Trench is the only one known. Waters near the Indian subcontinent also appear to be unsuitable for Phascolion. This genus was once portrayed as a cold- and deeper-water taxon, but recent data disprove that notion. Almost equal numbers of taxa (14 and 12, respectively) live in shelf waters (1-300 m) and deeper water. Of the 14 shelf taxa, 7 may be intertidal but the remainder have not been collected at depths less than 15 m. Six taxa are known from both shelf and continental slope depths (300-3000 m), including P. (I.) hedraeum (7-4600 m) and the eurytopic P. strombus strombus (1-4030 m). Six taxa are known only from slope and deeper waters (300-6900 m), but only P. (M.) lutense and P. (M.) pacificum occur in significant numbers at abyssal depths (>4000 m) as well as on the slope. E. Cutler and Cutler (1985 a) described a possible rassenkreis ("race circle") in P. strombus. Certain Japanese populations exhibit two morphs that differ in holdfast shape, hook size, and origin of the ventral retractor muscle. These character states are within the range of variation seen in the diverse North Atlantic population but are at the two extremes of the continuum. Assuming a center of origin in the North Atlantic, it is possible that one population dispersed eastward over the Siberian-Asian Arctic, and a second went westward over the Canadian Arctic, and the two met in the North Pacific, where the two ends of the circle came into contact. It seems clear that gene frequencies shifted as semi-isolated populations spread around the globe, and the Japanese forms may be genetically isolated, although this remains to be tested. An alternative hypothesis is that the North Pacific populations are actually two species that both migrated to the North Atlantic, where they exist as a "superspecies" or a group of cryptic species not yet differentiated. Center of Cladogenesis. If one analyzes this genus by subgenus, the only thing that becomes evident is that the western Pacific Ocean is inhabited by representatives of all subgenera except the most derived—the

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Distribution and Cladogenesis

monotypic P. (Villiophora). The widespread species are in cold, usually deep, water and are generally absent from lower latitudes. The areas of endemism here are simply too large to be meaningful (e.g., the western Atlantic or IWP). When areas of analysis are defined more narrowly, scattered clusters of endemism appear along the western side of the Indian, Pacific, and Atlantic oceans. Thus it seems that there are multiple illdefined centers (or fragmentation of a broad Panthalassa population) for this diverse genus, which has probably existed since late Paleozoic times. Onchnesoma Four of the six species and subspecies live in the Atlantic Ocean. The North Atlantic appears to have the largest populations, although all except O. squamatum squamatum are also found in southern latitudes, and O. steenstrupii nuda is known only from one southeastern Atlantic area. The only known extension outside the Atlantic, by the deep-water 0. magnibathum, is a record from the Peru-Chile Trench. The most widespread member of this quartet, O. steenstrupii steenstrupii, has been collected throughout the Atlantic and in the southwestern Indian and southwestern Pacific oceans. The two taxa not known from the Atlantic (O. intermedium and O. squamatum oligopapillosum) are represented by very few individuals and are very close to being untested endemics in the northwestern Pacific Ocean. In terms of preferred depths, four species live along the continental slopes (100-2000 m), one is a shelf species (15-250 m), and one is abyssal (3000-5500 m). Center of Cladogenesis. The cold waters of the North Atlantic appear to be the ancestral home of this genus, dating back to the Paleogene. Subsequent speciation probably occurred here also, spreading via the high latitudes into neighboring waters.

Family Themistidae

Themiste Four of the six T. (Lagenopsis) species live only in the Australian region, and two of the five T. (Themiste) species are limited to the eastern Pacific. Until recently, T. (Themiste) hennahi was a third eastern Pacific

Family Phascolosomatidae

329

species, but Haldar's (1991) record from Indian waters changed that species's pattern. Unlike the two other uncommon T. (Themiste), which have very limited distributions (J. blanda in Japan and T. alutacea in the western Atlantic), the two uncommon T. (Lagenopsis) have broad distributions (T. minor minor is from the northwestern and southwestern Pacific and off South Africa, and T. lageniformis is circumtropical-subtropical). Ranges of the two subgenera overlap in three regions: (1) Honshu (central Japan), where T. (T.) blanda and T. (T.) pyroides are sympatric with T. (L.) minor, (2) the Caribbean and east coast of Florida, where T. (L.) lageniformis and T. (T.) alutacea coexist; and (3) the Nicobar Islands off India, where T. (L.) lageniformis coexists with T. (T) hennahi. Southern Argentina may be a fourth such place, but the database is too small to ascertain this. Another way to view this genus is as follows: all six of the T. (Lagenopsis) can be found in some part of the IWP (five are endemic), and three of the five T. (Themiste) are found only in the Pacific Ocean (a fourth is in the Indian also). Only two species (one of each subgenus) are found in the Atlantic Ocean; one is restricted to the western Atlantic and the other is nearly circumsubtropical. All Themiste live in intertidal or shallow subtidal water. Center of Cladogenesis. Each of the two subgenera appears to have its own center, one on each side of the Pacific Ocean, which suggests a Pacific origin for the genus. The cool Australian region is the center for T. (Lagenopsis), and the nontropical eastern Pacific coastline has been an active center for T. (Themiste). Since cooler south Australia did not detach from Antarctica until the Eocene, the genus probably postdates that time. Most speciations likely occurred after the Miocene.

Family Phascolosomatidae

Phascolosoma Six of the 19 Phascolosoma species and subspecies appear to have very restricted ranges, 4 in habitats unusual for this genus: P. meteori from the Red and Arabian seas (high salinity, low oxygen tension); P. turnerae from the Gulf of Mexico and off Australia (deep cold water, in wood or near cold-water seeps); P. saprophagicum from New Zealand (deep cold water, from rotting whale skull); and the cold-water P. agassizii kurilense from

330

Distribution and Cladogenesis

the far northwestern Pacific Ocean. In limited but more typical habitats one finds P. maculatum (UE) (Indonesia) and P. glabrum multiannulatum (Tahiti). Eleven of the remaining 13 Phascolosoma taxa, plus the two endemics (P. saprophagicum and P. maculatum [UE]) and P. turnerae, or 74% of all Phascolosoma species, occur in the border region between the Indian and Pacific oceans—the Indo-Malayan subregion. The species richness in this subregion is unparalleled by other sipunculan genera. The five species not found in the Indo-Malayan subregion include three endemics (P. meteori, P. agassizii kurilense, and P. glabrum multiannulatum [UE]) plus P. granulatum, which lives in the colder waters of the northeastern Atlantic Ocean and the Mediterranean Sea, and P. (Fisherana) capitatum, from bathyal waters of the Atlantic Ocean. A second noteworthy feature is that only three species of Phascolosoma live in the Caribbean basin: the restricted P. turnerae and the two circumtropical shallow-water species, P. perlucens and P. nigrescens. The latter two also occur in the central and southern regions of the eastern Atlantic along with P. agassizii agassizii and P. stephensoni. The last species extends through the IWP to Hawaii and also coexists in parts of the northeastern Atlantic with P. granulatum. In the eastern Pacific are found the two shallow-water Caribbean species just mentioned plus the cool-water P. agassizii agassizii and the warm-water P. scolops. These four are also found throughout the IWP. Five species do not extend outside the IWP: P. albolineatum, P. arcuatum, P. glabrum glabrum, P. pacificum, and P. (Fisherana) lobostomum; while P. noduliferum and P. annulatum are restricted to the boundary area between the Indian and western Pacific oceans. Ecologically, Phascolosoma tolerates wide extremes (this in addition to the unique niches of a few species known only from limited populations, noted above), ranging from the warm, very euryhaline mangrove mud habitat of P. arcuatum, through the euryhaline cold intertidal rocks of P. agassizii, to the cold, stenohaline Atlantic where P. granulatum and P. (F.) capitatum live. It is nonetheless true that most species select shallow warm-water habitats. Center of Cladogenesis. The Panthalassa precursor of the Indo-Malayan Archipelago seems to be where this genus originated and where most speciation occurred. The genus is probably of mid-Paleozoic age, but most extant species evolved in Cenozoic times, including the cold-water species.

Family Aspidosiphonidae

331

Antillesoma The one species in this genus, A. antillarum, is found around the world in tropical and subtropical shallow-water habitats, generally in crevices or burrows in dead coral or other soft rocks. Center of Cladogenesis. Given such an extensive range and only one extant species, it is difficult to be certain, but A. antillarum probably originated in the Mesozoic Panthalassa. Apionsoma The four species fall into two ecologically different subsets, which are reflected in their distributions. The two deep-water taxa (A murinae murinae and A. murinae bilobatae) occur in the Atlantic and Pacific oceans at slope to abyssal depths (300-5200 m). The second taxon is also found in the Mediterranean Sea and on both sides of the Indian Ocean at slope depths only (200-1200 m). The three shallow-water species (A. misakianum, A. trichocephalus, and A. (Edmondsius) pectinatum) are also widespread, but in shallow, warm waters. The first is known from the Indian Ocean and both sides of the Pacific, but only the western Atlantic, including the Gulf of Mexico. The second co-occurs in warm-water sandy habitats over most of this range plus the eastern Atlantic Ocean. The third is less common but circumtropical and has been collected on both sides of all three oceans. The broad distribution of Apionsoma in both shallow and deep habitats may be indicative of great age. Center of Cladogenesis. The shallow Paleozoic Panthalassa probably saw the first members of this genus and, according to the hypothesis presented in the next chapter, the first members of the phylum Sipuncula. The deep-water taxa are undoubtedly more recent additions, with origins in the mid-Cenozoic Atlantic Ocean.

Family Aspidosiphonidae

Aspidosiphon Ten of the 19 species (63%) live in the western Atlantic Ocean and Caribbean Sea, bounded by Cape Hatteras on the north and the Amazon delta on the south: A. exiguus, A. gosnoldi, A. (Akrikos) mexicanus, A.

332

Distribution and Cladogenesis

(Paraspidosiphon) parvulus, A. (P.) fischeri, A. (Ak.) albus, A. elegans, A. (P.) laevis, A. (P.) steenstrupi, and A. misakiensis. The first four species listed are endemic to the region. The fifth also lives in the eastern Pacific (Panama to the Galapagos). The range of the sixth extends in the other direction, into the eastern Atlantic (Iberia to the Gulf of Guinea). The next three species are circumtropical, and the last is found on both sides of the Atlantic and in the western Pacific Ocean. Two species found in the eastern Atlantic and elsewhere do not live in the western Atlantic: A. (Ak.) venabulum from both sides of Africa, and A muelleri (see below). A. (Ak.) zinni, the one bathyal-abyssal member of this genus, is also found in the north Atlantic (plus one record from the Mozambique Channel). A. muelleri, the most widespread species, is almost cosmopolitan in temperate to subtropical waters. Two apparent gaps are in the western Atlantic (one record off southern Brazil) and the eastern Pacific (one record off Chile). A. muelleri is also the most eurytopic member of the genus and lives in a wide variety of temperatures and depths. Six species (plus A. muelleri) are widely distributed within the IWP. A. (P.) coyi extends into the eastern Pacific Ocean. Three of the six are also found in the Caribbean (A. elegans, A. (P.) laevis, and A. (P.) steenstrupi). The remaining two do not exist in either Hawaiian waters or the Atlantic Ocean (A. gracilis gracilis and A. (P.) tenuis). Two species (A. [Ak.] thomassini and A. spiralis) are more restricted within the IWP, and A. (P.) planoscutatus (UE) is known only from a single collection (2 specimens) in the Red Sea. Finally, A. gracilis schnehageni is known only from the eastern Pacific Ocean. The roughly equal number of endemic taxa in the AEP (6) and the IWP (4, plus 1 UE) is noteworthy. Of the 19 taxa, 13 live somewhere in the Atlantic Ocean, 11 occupy some part of the IWP, and 6 live in both areas. Although some common widespread members of this genus do bore holes in coral or soft rock (including the entire subgenus A. [Paraspidosiphon] plus one A. [Aspidosiphon]), 11 species (58%) do not. These include all the members of the subgenus A. (Akrikos) and all but one A. (Aspidosiphon). The nonboring worms live in empty mollusk shells (8), arenaceous foraminiferan tests (1), or interstitially (2). Most species live between the intertidal zone and the edge of the continental shelf (200 m). Center of Cladogenesis. The data suggest two centers of origin and speciation: the IWP and the tropical AEP. The Paleozoic Panthalassa saw the origin of the genus in the form of the ancestral subgenus, A. (Aspi-

Family Aspidosiphonidae

333

dosiphon). Although not obvious, much speciation probably occurred in the Mesozoic Tethys Sea and the Cenozoic IWP. The IWP region was clearly the site of the late Mesozoic origin and Cenozoic speciations in the subgenus A. (Paraspidosiphon). The late Cenozoic warm-water Atlantic was the center for the other derived subgenus, A. (Akrikos). Cloeosiphon and Lithacrosiphon The three species of these two genera are tropical, shallow warm-water, coral-boring worms whose ranges overlap in the western Pacific islands. Cloeosiphon aspergillus is widely distributed in the IWP, from East Africa across the Indian Ocean to northern Australia and from many western Pacific islands west of Hawaii. From this shared space in the western Pacific, the more common Lithacrosiphon (L. cristatus) is found eastward to the eastern Pacific and into the Caribbean. A new subspecies, L. cristatus lakshadweepensis (Haider, 1991), was recorded from the far northwestern corner of the Indian Ocean in the Arabian Sea. The other species (L. maldivensis)fillsthe gap because its range westward is more continuous across the Indian Ocean into the Red Sea, generally far from continental land masses. Center of Cladogenesis. The mid-Cenozoic Indo-Malayan Archipelago appears to be the place of origin of these taxa.

18

Evolution and Phylogenetic Relationships

Direct Evidence: The Fossil Record

Despite recent work on the Ediacarian and Burgess shale faunas (Cloud and Glaessner, 1982; Collins et al., 1983), we have no definitive fossil sipunculan or any fossil that is an acceptable ancestor (Morris, 1985). The best candidate for a sipunculan ancestor among the wormlike Burgess shale fossils may be Ottoia prolifica (Banta and Rice, 1976), but this muddwelling, bilaterally symmetrical worm with a retractable proboscis is not ascribable to any extant phylum. Its posterior anus, posterior ventral hooks, and rows of anterior hooks and spines make it more like the Aschelminthes or Priapulida (Morris, 1989). Another possible ancestor is Hyolitha from the Cambrian of Antarctica and the Ordovician of France. Although this animal has molluscan attributes such as a calcareous cone-shaped exoskeleton and an operculum, the digestive tract with both mouth and anus at the anterior end, the body wall with both circular and longitudinal muscle layers, and a hydrostatic skeleton to evert the "head" of the animal are sipunculan-like. It is possible that this extinct group coexisted with Paleozoic mollusks and sipunculans and that all three taxa shared a common Pre-Cambrian ancestor (Runnegar et al., 1975)One way to address the difficulties of assigning extinct forms such as these to formal taxonomic categories is to create superphyla for metazoan coelomates such as those proposed by Valentine (1973). His system focuses on coelomic architecture, and his group Sipunculata includes unsegmented infaunal burrowers with introverts, which probably fed on detritus. Valentine's five superphyla—Sipunculata, Molluscata, Lophophorata, Deuterostomia, and Metameria—are viewed as ancestral to all modern coelomate phyla. Willmer (1990) supported this approach and favored retaining the Sipuncula as a separate higher taxon because it is monomeric and has no clear links to other protostome taxa.

Direct Evidence

335

The holes made by sipunculans seem to have fossilized much better than the worms themselves did. The ichnogenus Trypanites is absent from Cambrian hard-ground surfaces in Montana, but it is represented by macroborings from the late Cambrian of Labrador and by well-preserved fossil burrows from many Ordovician, Silurian, and Devonian locations. (An ichnogenus is a genus based on traces, such as fossilized burrows, rather than on fossils of the animals themselves. The Greek prefix ichnos means "footprint" or "track.") It is possible that the Cambrian holes were made by a separate group of organisms that became extinct along with their host reef-building organism (archaeocyathid) and that a second group of organisms that produced a very similar burrow appeared in the early Ordovician (Brett et al., 1983). The similarity of fossil borings to those made by modern sipunculans suggests that sipunculans were present by the mid-Paleozoic (Pemberton et al., 1980). Coral assemblages containing coral-boring sipunculans are known from Upper Jurassic, Miocene, Pliocene, and Pleistocene times (Hyman, .1959; Pisera, 1987). The Montana-Wyoming Cambrian sediment contains small, slightly tapered holes that appear to have been made in semilifhified micrites (finegrained sediments) prior to their deposition as clasts. It is possible that these holes were produced by "precursors of organisms . . . capable of excavating truly indurated sediment" (Brett et al., 1983:288). The sipunculan origin of these ancient burrows is supported by recent evidence that very similar Quaternary deep-sea burrows (Zoophycos) along the northwest African and Norwegian continental slopes were made by sipunculans belonging to the genus Nephasoma. These lebensspuren correspond to older burrows such as the upper Cretaceous ichnogenus Trichichnus and the Jurassic ichnogenus Ancorichnus from Denmark, both of which may be of sipunculan origin (Wetzel and Werner, 1981; Frey et al., 1984; Romero-Wetzel, 1987). Trichichnus was also reported from the Miocene in Italy by McBride and Picard (1991). The fossil burrows were most common in claystones but also present in sandstone formations. The burrows averaged 0.13 mm in diameter, were up to 160 cm long, and were spaced 0.4-50 cm apart. McBride and Picard's analysis suggested that the creators of these burrows had a high tolerance to low in situ oxygen levels. There are a few thin deep-water members of the genus Nephasoma that could have constructed burrows with these dimensions. Other possible sipunculan burrows include holes in Miocene deposits at depths of 10003000 m off New Zealand (Hayward, 1976).

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Evolution and Phylogeny

Many fossils of the Devonian tabulate coral Pleurodictyum contain overgrown gastropod shells, most of which were occupied by a secondary resident, possibly a sipunculan like the modern Aspidosiphon (Brett and Cottrell, 1982). Solitary corals with sipunculan symbionts are known from the upper Cretaceous (Wadeopsammia from Texas and Tennessee) and the Miocene (Symbiongia from Florida). The sipunculan is clearly an Aspidosiphon, probably A. muelleri (a taxon that now includes A. corallicola and A. jukesii). The modern hosts of this worm, the corals Heterocyathus and Heteropsammia, are known from the Miocene in France and the Neogene in the western Pacific (Gill and Coates, 1977). Although direct evidence is lacking, the above data support the following points: (1) a common sipunculan-molluscan ancestor existed in Ediacarian or earliest Paleozoic times; (2) sipunculans were living in softbottom burrows at least by the mid-Paleozoic (Devonian) and probably earlier (Cambrian); and (3) some sipunculans have lived in association with corals since mid-Paleozoic times and throughout the Mesozoic and Cenozoic. The Sipuncula thus seems to be an ancient taxon with an unknown history of divergence and retrenchment (escalation and extinction). It is a group that underwent early but conservative cladogenesis, and its members occupied diverse niches early in its history (hard/soft, shallow/deep, warm/cold) and persist in these niches at the present time.

Indirect Evidence

The phylum Sipuncula is usually considered most closely related to the annelids and mollusks, but there is no clear consensus as to its true sister group. First, a point about the clustering of phyla into yet higher taxa. The historically accepted constructs Protostomia and Deuterostomia have been broadly criticized in recent decades (e.g., Siewing, 1976). Siewing dismissed these two subkingdoms, as well as the concept of acoels and pseudocoels, and instead proposed the Archicoelomata as the ancestral group that gave rise to three modern groups: Spiralia, Chordata, and Pogonophora. The Spiralia includes the Sipuncula and most of the groups formerly placed in the Protostomia. Although other biologists also support a distinct status for the Pogonophora, no consensus has yet been reached on that issue (E. Cutler, 1975c; Ivanov, 1983, 1988).

Indirect Evidence

337

Nevertheless, some biologists continue to use Deuterostomia and Protostomia (e.g., Lake, 1990). In the following section I use the older terms— those used by the authors whose work is being discussed—when it is appropriate to do so. This is not meant to diminish the value of the Spiralia construct. The descriptive taxon Spiralia is used by many biologists, including Willmer (1990), even though he believes that sipunculans evolved from a hypothetical Protocoelomate group and considers them monomeric coelomates. The assertion that sipunculans are segmented (Ruppert and Carle, 1983) seems have its root in Siewing's (1976) idea that the tentacular coelom, which extends into the contractile vessel, is derived from the mesocoel. According to this unusual interpretation, sipunculans would be oligomerous. Siewing's system represents evolution within the Spiralia as follows. An ancestral Spiralian underwent cladogenesis to give rise to the early Sipuncula and its sister group, an ancestral Deutomere. The Deutomere gave rise to the Mollusca and an ancestral Articulata. The latter entity was the precursor of the Annelida and Arthropoda. We will return to this below. A paper presented at the 1970 Sipuncula symposium held in Kotor, Yugoslavia, proposed four eumetazoan phyla: Amelia, Polymeria, Oligomeria, and Chordoma (Hadzi, 1975). The most advanced class within the Oligomeria was the Sipunculidea, which had evolved from the annelids via the echiurans. This hypothesis has not received support from other biologists. Comparative Immunology The sipunculan immune system is thought to be intermediate between the most primitive systems and the most advanced (see Chapter 10). Ionescu-Varo and Tufescu (1982) used an iterative analysis (assuming no homoplasy) to survey 12 immunological characters of 9 invertebrate phyla and 12 vertebrate taxa. They postulated that the 12 characters arose sequentially as follows: 1. Recognition of self 2. Rejection of xenograft 3. Specialized leukocytes 4. Rejection of allograft

338

Evolution and Phylogeny

5. Immunological memory 6. Type T lymphocytes 7. Circulating antibodies 8. Organs (e.g., thymus and spleen) 9. Plasmocytes 10. Type B lymphocytes 11. Lymph nodes 12. Bursa fabricii, or Peyer's plates Sipunculans exhibit the first 7 characters. From this primary matrix the authors generated a secondary matrix using percentage similitude and differentiation, then used these data to plot a dendrogram of immune evolution along polar coordinates, giving seven evolutionary levels or stages. The analysis placed the sipunculans in stage 3, together with the Annelida and two non-Spiralia taxa, the Tunicata and Echinodermata. The sipunculans are the only protostomes with circulating antibodies, and no other invertebrate is known to have a more complex immune system. According to Ionescu-Varo and Tufescu's analysis, the mollusks and arthropods have regressed from stage 3 to a lower stage, closer to the coelenterates. This analysis is very interesting, but different interpretations of the data are possible. The arrangement of characters may be suspect because the reasoning used to create it was somewhat circular. The dendrogram suggests that the sipunculans share a common ancestor with annelids, echinoderms, and tunicates. If the arthropods and mollusks evolved from this ancestral group, as Ionescu-Varo and Tufescu believe, some regressive selective pressures must be postulated to have led to the loss of a useful defense mechanism. It is just as reasonable to propose that the arthropods and mollusks split off from a common stock before the sipunculan-annelid line evolved the more complex immune system, and that the deuterostome immune systems evolved independently but in a parallel manner. Siewing's (1976) phylogeny requires either three separate origins for the same defense mechanism or one very early origin and at least two subsequent losses. Neither of these possibilities is very parsimonious, and it is usually best to seek the simplest explanation. The suggestion that sipunculans are more advanced than other invertebrates, while perhaps true with regard to immune systems, may not apply more broadly. If they separated from the other Spiralia as early as Siewing suggested, however, the sipunculans have had sufficient time to evolve many unique attributes.

Indirect Evidence

339

Comparative Biochemistry and Physiology A number of biochemists and physiologists have looked at sipunculan systems (see Part 2), but the database for comparative work is not extensive. Clark's review of the systematics and phylogeny of sipunculans, echiurans, and annelids, in Chemical Zoology (1969), focuses on their developmental biology and supports separate phylum status for each of the three taxa, perhaps within the superphylum Trochozoa. Florkin reviewed the existing biochemical evidence for the phylogeny of the Sipuncula in 1970 (published as Florkin, 1975). Based largely on hemerythrin biochemistry, but also considering nitrogen metabolism and the lack of chitin in the group, Florkin concluded that the sipunculans are a distinct collateral evolutionary line of a preannelid stock. In her excellent review of the role played by physiology and biochemistry in the understanding of phylogeny, Mangum (1990) illustrated how simple generalizations become less credible as knowledge accumulates. Situations that were formerly clear dichotomies become less clear polychotomies. The more we learn, the less certain we are about absolute truths. The example Mangum used was the assertion, considered to be true well into the 1960s, that all invertebrates use arginine phosphate in ATP synthesis and all vertebrates use creatine phosphate. By 1970 exceptions had begun to accumulate, and this idea is no longer credible. New information about proteins, amino acid sequences, DNA hybridization, etc., has expanded our understanding of the evolution of molecules, but Mangum properly cautioned readers about equating the evolution of molecules with the evolution of taxa. In fact, many biochemical studies are applicable only to lower-level groupings of organisms such as demes, populations, or species. Mangum suggested that 16-18 S RNA studies may prove helpful at higher levels, but more time is needed to evaluate these methods. With these caveats as background, then, I will proceed. The fact that the level of carbonic anhydrase activity in the red blood cells is fairly high in sipunculans and annelids but not in mollusks led Henry (1987) to propose that mollusks are evolutionarily the more primitive group. A comparison of phospholipids from 59 species of invertebrates from seven phyla showed similarities between sipunculans and other marine worms, including annelids and echiurans (Kostetskii, 1984). The study did not include mollusks, however, and thus does not shed any light on the

340

Evolution and Phylogeny

sipunculan-mollusk relationship. Having similar phospholipids is not necessarily an indication of common ancestry. The types and directions of chemical changes (e.g., the replacement of polar groups, the types of bonds, and the relative amounts of different lipids) are known to respond to environmental factors such as temperature (Kostetskii and Shchipunov, 1983). Therefore, a similar phospholipid composition found in two taxa may reflect a similar habitat rather than similar phylogenetic histories. At least two sipunculan species have both actin and myosin regulation of muscle contraction, and thus are like many arthropods, annelids, and nematodes (Lehman and Szent-Gyorgyi, 1975). The mollusks, brachiopods, echinoderms, nemertines, and echiurans have lost the actin and have only myosin control, a more derived condition. Single control by actin, the system present in vertebrate striated muscles, occurs in fast muscles of decapods, in mysids, and in one sipunculan, Themiste pyroides (see Chapter 9). The interesting implication of these data, in an evolutionary context, is that sipunculans are similar to annelids but not mollusks— and not their presumed closest relatives, the echiurans. Evolution seems to be proceeding in two different directions, but both are away from dual- and toward single-control systems. The selective advantages of single-control over dual-control systems are unclear. The chromatin of eukaryotes is composed of repeating sequences known as nucleosomes. A DNA molecule can be cleaved into its nucleosomes, whose lengths can then be measured (see Chapter 11). The nucleosomal DNA repeat length (number of base pairs) in Sipunculus nudus red blood cells is 177, versus 212 for chickens, 200 for frogs, and 203 for trout (Wilheim and Wilheim, 1978). Other vertebrate tissues have values in the range of 195-210. On the basis of this information, Wilheim and Wilheim asserted that sipunculans are primitive eukaryotes, and that "the small repeat of 5. nudus could be correlated to the fact that this marine invertebrate forms an isolated ancestral phylum." A broader sipunculan database (i.e., more than one species) plus data on annelids and mollusks might make this information more useful for determining phylogenetic relationships. Aerobic respiration involves a variety of pyruvate oxidoreductases. Sipunculans—most invertebrates, in fact—use lactate dehydrogenase, among others. They also have alanopine and strombine dehydrogenase, as do annelids and mollusks but not arthropods or echinoderms (Livingstone et al., 1983). The one difference Livingstone et al. noted between sipunculans and annelids was the absence of octopine dehydrogenase from the latter, as well as from arthropods and echinoderms. This distribution of

Indirect Evidence

341

enzymes suggests that sipunculans are more closely related to mollusks than to annelids. Two types of biochemical information, both derived from single sipunculan species and described in Chapter n , are of no use within this context. The work on amino acid sequences is not useful due to the lack of comparative data, and the electrophoresis of gene loci revealed too much polymorphism. Lake (1990) applied rate invariant analysis of 18 S ribosomal RNA sequences as a means to understand phylogenetic relationships of 11 metazoan phyla and classes from the Cnidaria to the Chordata. His analysis was based on data generated by others and included only one sipunculan species, the phylogenetically enigmatic Phascolopsis gouldii, whose distribution is restricted to the northeastern coast of the United States (where it is endemic and not of great age), and whose developmental path and karyotype are of a derived type. Whether it is wise to extrapolate from one such species to the entire phylum is questionable, but Lake's conclusions were that sipunculans are the sister group of mollusks and that the annelids and the sipunculan-molluscan group share a common ancestor. In summary, biochemical and physiological information accumulated since 1970 indicates the following phylogenetic relationships: 1. Carbonic anhydrase: Mollusks are more primitive than sipunculans, and annelids are similar to sipunculans. 2. Phospholipids: Sipunculans are like other marine worms, and similarities in phospholipid concentrations may reflect ecological, not phylogenetic, similarities. 3. Actin and myosin control: Sipunculans are like annelids and unlike echiurans and mollusks. 4. Nucleosomal DNA: Sipunculans form an isolated ancestral phylum. 5. Pyruvate oxidoreductases: The respiratory enzymes of sipunculans are like those of most other invertebrates, but they have three enzymes lacking in arthropods and echinoderms and one enzyme that annelids lack. They show no differences from the mollusks. 6. Amino acid sequence and protein electrochemistry: No value. 7. Ribosomal RNA Sequence: Annelids diverged from a molluscansipunculan ancestor and the latter two are sister groups. These data generally point to a close relationship among sipunculans, annelids, and mollusks (i.e., all three probably evolved from a common ancestor) and suggest that mollusks may be less derived than sipunculans

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Evolution and Phylogeny

and annelids. Alternatively, the differences that mollusks evince in items i and 3 above could mean that mollusks are more derived. On the other hand, if rRNA sequencing is all that its proponents claim, then item 7 is all one needs to consider. In this regard, a larger database would generate much more confidence in these conclusions. Comparative Fine Structure The electron microscope has revealed details of cell structure that are useful for determining the degree of relatedness among taxa (Barnes, 1985). The evidence that concerns sipunculans is of three types, discussed below. Cells that line lumens or exterior surfaces have a belt around their apical circumference known as an intercellular junction. The precise nature of this junction varies (13 types have been identified), but in sipunculans and annelids it is a pleated septate junction of the "lower invertebrate" variety. Mollusks and arthropods have a "protostome" septate junction (C. Green and Berquist, 1982). The same authors interpreted this to mean that sipunculans are in the deuterostome lineage. Actually, the data could support the idea that sipunculans and annelids are closely related and more primitive than mollusks. It is also possible that the mollusks added this character after separating from the sipunculan-molluscan group. Nielsen's (1987) analysis of the feeding and swimming cilia in 15 phyla of invertebrates showed that the nature and position of the accessory centriole, which is perpendicular to the basal body and on the downstream side, links sipunculans to annelids and mollusks. The nature of the striated sperm anchoring fiber apparatus was mentioned in Chapter 15. In the present context it is worth noting Klepel's (1987) assertion that the sipunculan arrangement is like that of the original protostomial type. The anatomical data point to the conclusion that sipunculans are a primitive group related to both annelids and mollusks and probably less derived than either group (and therefore consistent with Siewing, 1976). Comparative Embryology The reproductive biology of sipunculans is discussed in Chapter 15, but there are several points worth reviewing here. While an understanding of developmental pathways can provide a good context in which to analyze

Indirect Evidence

343

relationships among taxa, linking ontogeny and phylogeny too rigidly can lead to false conclusions. One type of evidence that is universally considered to indicate monophyly is the manner in which the egg undergoes cleavage. Sipunculan eggs follow the spiral route, thus are placed in the Spiralia along with the annelids and mollusks (Siewing, 1976). Even though it has been suggested that the trochophore is probably a derived larval form that could have evolved independently more than once (Ivanova-Kazas, 1985), animals with this larval stage are still assumed to be related (Rice, 1985a). Strathmann (1978) expressed a similar concern with regard to cilia used as feeding structures in larvae and asserted that larval morphology should not be used to suggest a close relationship between sipunculans and annelids or mollusks. Rice (1985a) pointed to the following similarities as evidence of sipunculans' closer relationship to annelids: the prototroch and metatroch ciliary bands, the development of the larval cuticle from the egg envelope, and the development of the nervous system (see Chapter 16, Sense Organs, for details about the latter). One interesting similarity between sipunculan and molluscan embryology is the radial position of the cross cells in the apical plate. A major difference from the annelids is sipunculans' lack of metamerism at any stage in their ontogeny. Based on these points, Rice proposed that sipunculans are a primitive phylum that arose from an annelid-mollusk stem. Two other considerations of developmental attributes reached a different conclusion. Freeman and Lundelius (1992) proposed a close relationship between sipunculans and Mollusca (class Aplacophora) based on the mode of D quadrant specification (both taxa have unequal cleavage). Their argument that induction is the primitive mode of D quadrant specification rests on a series of assumptions, as follows: equal cleavage can be equated with induction; the more derived cytoplasmic localization is linked to unequal cleavage (as in sipunculans); the database is sufficiently complete (they included three sipunculans); the phylogenetic relationships of the groups they discussed were accurate (these were not complete). Freeman and Lundelius were unable to relate sipunculans and aplacophorans to other metazoan taxa in more than a tenuous manner, and they went on to say that these two groups are the only ones that do not fit their developmentevolutionary scenario. In other words, both taxa have unequal cleavage, which would translate into a derived mode, but Freeman and Lundelius resisted that conclusion.

Evolution and Phylogeny

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In an article devoted largely to the proposition that these same wormlike aplacophorans comprise a primitive taxon within the Mollusca, A. Scheltema (1993) postulated that Sipuncula and Mollusca are sister groups. This argument is based on similarities in early development (the molluscan cross) and a few transitory features of pelageosphera larvae (lip gland and buccal organs). Scheltema also postulated that, like mollusks, the sipunculans must have appeared early in the evolution of the metazoans. The fact that sipunculans and some mollusks, which are known to have originated in the Cambrian, all use hemerythrin as an oxygen transport molecule supports an early origin for sipunculans.

Conclusions

Although the evidence is not totally congruent, there is consensus that there was an ancestral form common to the sipunculans, annelids, and mollusks in existence by the earliest Paleozoic. From this point there are three possibilities, each supported by some part of the data: (1) the annelids separated from an ancestor that later gave rise to the sipunculans and mollusks; (2) the molluscan stock diverged first, followed by the sipunculan-annelid separation; or (3) the sipunculans diverged from a stock that subsequently became the common ancestor to the mollusks and annelids. Table 4. Possible phylogenies for Annelida, Mollusca, and Sipuncula

Paleontology Immunology Biochemistry Fine Structure Embryology Notes: A = Annelida, M = Mollusca, S = Sipuncula; X = supports most strongly, + = permits (no contradiction).

Conclusions

345

The third model is consistent with Siewing, 1976. The third and second models are each supported by one, and permitted by the remaining four types of evidence just discussed. The first model is supported by the paleontological, biochemical, and embryological data and is permitted by the immunological and finestructure data (see Table 4). Based on my evaluation of the evidence, model 1 appears to be the most probable, although I acknowledge the limited nature of some parts of the database. I must also restate that this is really linking the most primitive of the molluscan taxa (according to A. Scheltema, 1993) with the least derived of the sipunculans as defined in Chapter 19.

19

Within-Phylum Relationships

Phylogenetic relationships among the taxa within the phylum Sipuncula are considered in E. Cutler, 1980, and E. Cutler and Gibbs, 1985. A formal presentation of the resulting classification, with a few corrected spellings, followed a short time later (Gibbs and Cutler, 1987). Readers interested in the philosophy and details of the numerical methods used to determine relationships should see the 1985 work. An abbreviated discussion of the characters used in the analysis is presented below, together with some new information and a reevaluation of some assumptions about character state polarities (Table 5). The suprageneric taxa as used earlier remain unchanged, but the proposed historical relationships among taxa are radically different in a few of the aspects described below. When the plesiomorphic/apomorphic (i.e., ancestral/derived) character states of the 12 morphological characters used in earlier analyses were described, the polarities were rooted in a hypothetical ancestral sipunculan (HAS). That model is redefined here. The nature of sipunculans imposes severe limitations on character analysis. Their elastic, soft bodies have almost nothing meaningful to measure or count, there is no fossil record, there is no good out-group to help root characters when attempting to polarize, and the number of useful characters is modest. All the available morphological information on sipunculans has been recoded and used as input for the PAUP phylogenetic analysis program. In general, the end products (cladograms) do not differ from already published configurations (e.g., E. Cutler and Gibbs, I985:fig. 1). My computer analyses used five different data sets: family-level data, from the six families, followed by runs for each of the four orders at the subgeneric level. The later runs used more restricted and appropriate data (see Tables 6-10). The paucity of characters available for analysis resulted in dendrograms

Morphological Data

347

Table 5. Attributes used in cladistic analyses 1. Tentacles: 0, nuchal only; 1, nuchal and peripheral; 2, peripheral only; 3, dendritic peripherals 2. Nephridia: 0, pair, bilobed; 1, pair, unilobed; 2, single 3. Coelomic extensions: 0, none; 1, pouches; 2, canals 4. Introvert-trunk junction: 0, straight; 1, angle 5. Postesophageal loop: 0, absent; 1, present 6. Anus location: 0, anterior of trunk; 1, on introvert 7. Anal shield: 0, none; 1, simple (Aspidosiphon); 2, massive (Lithacrosiphon); 3*, Cloeosiphon 8. Spindle muscle: 0, attached posteriorly to body wall; 1, ends within gut posteriorly; 2, absent Homoplastic characters, for within-family analyses 9. Introvert hooks: 0, in rings, with basal spinelets; 1, in rings, no spinelets; 2, in rings of very young, absent in adults; 3, none in adult or young; 4, none in rings, replaced with scattered hooks 10. Body wall muscle layers: 0, both continuous; 1, longitudinal layer divided into bundles, some anastomosing; 2, both layers with anastomosing bundles; 3, both layers divided into distinct bands 11. Contractile vessel villi: 0, absent; 1*, many short digitiform units; 2*, few long stringy tubular units 12. Introvert retractor muscles:" 0, two equal pairs; 1, ventral pair only; 2, fused ventral pair only; 3, all there but fusion of dorsal to dorsal and ventral to ventral; 4, fusion and reduction of ventrals; 5, incomplete fusion of all four; 6, complete fusion of all four. 13. Nephridiopores relative to anus (in Sipunculidae): 0, anterior; 1, posterior Note: Character state polarity coding; asterisk indicates unordered components (o is always the ancestral, or plesiomorphic, state). "Possible sequences: 0-1-2, 0-3-4, 0-3-5-6.

Table 6. Character states of sipunculan families Attribute 1 Sipunculidae Golfingiidae Themistidae Phascolionidae Phascolosomatidae Aspidosiphonidae

2 1,2 3 2 0 0

2 1 1 1 2 0, 1 1

3

4

5

6

7

8

1,2 0 0 0 0 0

0 0 0 0 0 0, 1

0, 1 0 0 0 0 0

0 0 0 0, 1 0 0

0 0 0 0 0 1, 2, 3

0, 1 1 1 2 0 0

Note: Attribute numbers are numbers 1-8 in Table 5. Character states are those used in Table 5.

Table 7. Character states of sipunculiformes genera and subgenera Attribute

Sipunculus S. (Austrosiphon) Xenosiphon Siphonosoma Siphonomecus Phascolopsis

3

5

8

9

10

12

13

2 2 3 1 1 0

1 1 0 0 0 0

1 1 1 0 0 1

3 3 3 1 1 2

3 3 3 2 2 1

0 0 0 0 1 0

0 1 1 0 0 0

Note: Attribute numbers are those listed in Table 5.

Table 8. Character states of Golfingiiformes genera and subgenera Attribute

Golfingia G. (Spinata) Nephasoma N. (Cutterensis) Thysanocardia Themiste T. (Lagenopsis) Phascolion P. (Isomya) P. (Montuga) P. (Villiophora) P. (Lesenka) Onchnesoma

1

2

6

g

9

11

12

2 2 2 4 1 3 3 2 2 2 2 2 2

1 0

0 0 0 0 0 0 0 0 0 0 1 0* 1

1 1 1 2 1 1 1 2 2 2 2 2 2

4* 0 4* 3 3 4* 4* 4 4 4 3 3* 3

0 0 0 0 1 2 1 0 0 0 3 0 0

0 0

2 2 2 2 2 2

3 2 4 5 5 6

Note: Attribute numbers are those listed in Table 5. * = Polymorphic, but most species exhibit indicated state. States 1, 2, or 3 are present in one to several species for character 9.

Table 9. Character states of Phascolosomatiformes genera and subgenera Attribute

Phascolosoma P. (Fisherana) Antillesoma Apionsoma A. (Edmondsius)

2

8

9

10

11

1 1 1 0 0

0 0 0 0 1

1 1 2 0 0

1 0 1 0 1

0 0 1 0 0

Note: Attribute numbers are those listed in Table 5.

Morphological Data

349

Table 10. Character states of Aspidosiphoniformes genera and subgenera Attribute

Aspidosiphon A. (Paraspidosiphon) A. (Akrikos) Lithacrosiphon Cloeosiphon

4

7

9

10

1 1 1 1 0

1 1 1 2 3

1 1 4 1 1

0 1 0 1 0

Note: Attribute numbers are those listed in Table 5.

that are not worth presenting here. The many polychotomies (i.e., unresolved branch points) and the artificial and arbitrary nature of the methodology, as pointed out by E. Cutler and Gibbs (1985), are other reasons for not presenting dendrograms. As more information becomes available the conclusions presented below should be tested and, if necessary, modified. I encourage others to use the data in Tables 6-10 in appropriate analyses.

Morphological Data

Changes in applicability and character state polarity from that presented in Cutler and Gibbs, 1985, are as follows. 1. Tentacles: Nuchal tentacles now considered ancestral to peripherals. 2. Spindle muscle: Posterior attachment (complete) is now ancestral; unattached and absent are derived states. 3. Introvert hooks: (A) Complex hooks in rings are ancestral; scattered or absent hooks are derived and homoplastic (i.e., they evolved more than once in different lineages; this may result in either parallel or convergent evolution, but most importantly such characters are not homologous and thus do not indicate a shared common ancestor). (B) Hooks with basal spinelets are ancestral. 4. Longitudinal muscle bands: Presence is homoplastic above family level. 5. Contractile vessel villi: Presence is homoplastic above family level. 6. Introvert retractor muscles: Loss or fusion is homoplastic above family level.

35o

Within-Phylum Relationships

Broadly Useful Characters The following eight morphological attributes can be used to analyze relationships among all of the families and genera. It is assumed that they originated only once and therefore are not homoplastic. i. Tentacle arrangement. The oral disks, with their tentacular crowns, are diverse, but when the misleading descriptions are corrected, two general types are recognizable: type P, in the class Phascolosomatidea, and type S, in the class Sipunculidea. Type P tentacles are simple and small, arranged in a dorsal arc around the nuchal organ, and number 10-30 in most species. Type S tentacles are arranged peripherally on the oral disk encircling the mouth. They are especially well developed in Thysanocardia, reduced in other genera, and significantly modified in Themiste. The dorsal nuchal organ in some type S arrays may be encircled by an arc of small nuchal tentacles. The variations on these themes are described in the sections on morphological characters throughout Part I. It had been proposed that type S is ancestral to type P (E. Cutler and Gibbs, 1985). Alternatively, the peripheral tentacles may represent a later adaptation for feeding, and the reverse polarity is proposed here. The cephalic collar below the oral disk in the Phascolosomatidea is now considered to be the precursor of the peripheral tentacles, not the remnant. The evolutionary sequence now proposed is from an ancestor with only nuchal tentacles to a form with both peripheral (feeding) and nuchal (chemoreception) tentacles, to forms with only peripheral tentacles; that is, a gradual reduction of one set and elaboration of the other. The external feeding apparatus is subject to direct selection pressures (predation), and its efficacy directly affects the success of the genotype. The wide variety of types between and within genera suggests a faster rate of change in tentacles than in the general body plan. This opens the way for convergent or parallel trends as well as reductions in complexity or reemergence of previously suppressed complex phenotypes. 2. Nephridia number. Most sipunculans are bilaterally symmetrical and have two nephridia. The apomorphic loss of one nephridium has occurred in Phascolion and Onchnesoma. 3. Coelomic extensions. In most Sipunculidae, the coelom connects to epidermal canals or sacs via small pores through the muscle layers. The nature of the synapomorphy (i.e., shared derived character) varies among the four genera. For more details see Chapter 2, in this volume, and E. Cutler, 1986).

Morphological Data

35i

4. Introvert-trunk junction. The anterior-posterior axis of the introvert is a continuation of the main trunk axis in most genera, and the ancestral condition. The anal shield present in Aspidosiphon and Lithacrosiphon forces the introvert ventrally to an angle ranging from 40 to 900. 5. Postesophageal loop. The esophagus leads directly into the double helix of the gut coil in most genera. A derived condition is seen in the genus Sipunculus, which has a separate and distinct anterior loop between the straight esophagus and the double-coiled gut. 6. Anus location. The anus is located mid-dorsally very near the anterior end of the trunk in most genera. In Onchnesoma and four species of Phascolion the anus is located on the introvert, at least 20% of the distance toward its tip, an apomorphic condition. 7. Anal shield. A horny or calcareous shieldlike structure occurs at the anterior end of the trunk in three coral-inhabiting genera. The form of this shield varies considerably, and homoplasy is likely. Aspidosiphon represents one independent line, with Lithacrosiphon being a modification of this apomorphic state. The anal shield in Cloeosiphon is very different from the other two and is assumed to have evolved independently. 8. Posterior attachment of spindle muscle. The threadlike spindle muscle extends through the gut coil to the posterior end of the trunk in some genera (ancestral), but in others it terminates within the coil (derived). This reduction or loss continues to a second derived state in Phascolion and Onchnesoma, in which its total loss has left only fixing muscles to anchor the gut. Limited-Use and New Characters The following characters have been determined to be misleading if used to determine relationships above the family level. One previously unused character is presented here as well. 9. Introvert hooks. Various kinds of hooks and spinelike structures grow on the distal half of the introvert. The phascolosomatid type of hook, which exhibits an internal complexity and is arrayed in distinct rings, was considered apomorphic (E. Cutler and Gibbs, 1985), but now there is good reason (as tentatively proposed in E. Cutler and Cutler, 1988) to consider the reverse more likely; that is, complex hooks in rings are plesiomorphic. The primary reason for this reversal is the discovery of such hooks in very young members of species previously thought to be hookless, including one Themiste, the single Antillesoma species, and Phascolosoma meteori. Phascolopsis gouldii juveniles have hooks, but the arrangement is not

352

Within-Phylum Relationships

clearly in rings. In some polymorphic genera (e.g., Siphonosoma or Apionsoma), species without hooks have rings of small papillae where hooks are found in congeners. Furthermore, the presence of hooks in an ordered array appeared early (in the evolutionary and paleontological sense) in related taxa such as the enigmatic Cambrian Ottoia and several groups of extant worms such as some acanthocephalans, kinorhynchs, and priapulids. The loss of regular rings of hooks in adults has probably occurred several times (homoplasy) and via different genetic mechanisms, because in modern sipunculans the loss occurs at different times during the ontogeny and results in diverse end products. The loss is often, but not always, followed ontogenetically by replacement with a scattered array of some other type of hook. In some species, though, the animal remains hookless for the remainder of its life. While the absence of hooks in rings may be apomorphic, this character should not be used as an indication of common ancestry (synapomorphy) above the genus level. In an analysis based on phenetic (rather than cladistic) methods, the synplesiomorphy (i.e., shared ancestral character state) of hooks in rings might be of value. Another major change that concerns hooks is the inclusion of hooks with basal spinelets as plesiomorphic (Fig. 54). This position is counter to earlier assertions that these hooks and the bilobed nephridia and very long introverts found in the Apionsoma species, as well as the monotypic subgenus Golfingia (Spinata), are unique derived character states (E. Cutler, 1979; E. Cutler and Cutler, 1987a; N. Cutler and Cutler, 1990). Rather than considering these traits to be recently evolved, specialized traits that arose independently and convergently in two different genera— and therefore omitting them from phylogenetic analyses—it is now proposed that these traits are ancestral and have been retained in a few "living fossils." The presence of complex ornamented or pectinate hooks, teeth, and spines in other living worms, such as some polychaetes, priapulids, and kinorhynchs, and in some Burgess shale fossils (e.g., the proboscis spinules of Ottoia), supports this character polarity. Figure 86 suggests how an Ottoia-type structure might have undergone a folding along the midline to become an Apionsoma type of hook. The presumed evolutionary sequence is thus from ringed hooks with basal spinelets, to ringed hooks without spinelets, to the loss of hooks in adults, followed by loss in both juveniles and adults, which then either stay hookless or develop new scattered hooks. 10. Body wall muscle layers. The two layers of musculature in the body

Morphological Data

353

A B C Figure 86. Possible sequence in the early evolution of sipunculan hooks. A. Proboscis spinules of the Cambrian Ottoia (after Banta and Rice, 1976). B. Hypothetical intermediate stage with the lateral edges folding together. C. Apionsoma hook with basal spinelets (see also Fig. 54B). wall are continuous layers in the ancestral state. In some genera, however, the longitudinal muscle layer of the body wall has split into more or less distinct bands. Although this attribute is considered apomorphic and is used as an indication of common ancestry, it has undoubtedly occurred more than once (homoplasy). The circular layer may further divide into partially separated bundles, an even more derived state. Within the Sipunculidae both layers form distinct, separate muscle bands as the most derived condition. 11. Contractile vessel villi. The contractile vessel is spacious and has digitiform villous outpouchings in a number of species. It seems likely that this is an apomorphic but homoplastic condition that has appeared independently, along with complex and voluminous tentacular crowns, in five of the six families. The simple contractile vessel without villi is plesiomorphic. In Themiste, two types of villi evolved. One subgenus, T. (Themiste), has few long, thin, threadlike extensions, and E. Cutler and Cutler (1988) questioned the presumption of homology. T. (Lagenopsis) has the same type of contractile vessel villi as those found in the other genera that possess them. 12. Introvert retractor muscles. The extended introvert is retracted by muscles whose origins are on the trunk wall and insertions are behind the cerebral ganglia. The plesiomorphic state is two equal-sized pairs—a ventral and a dorsal. A number of genera have only one pair. This reduction probably occurred at least once in each class, possibly four times altogether. Muscle fusion also occurs, commonly in Phascolion, and involves fu-

354

Within-Phylum Relationships

sion of dorsal to dorsal or ventral to ventral. In a few species— Onchnesoma, for example—so much fusion (and reduction?) has occurred that only a single muscle is apparent. 13. Nephridiopores-anus relationship. For most taxa this relationship is not of phylogenetic value. Within the family Sipunculidae, however, the nephridia open just anterior to the anus in all but three species, where this relationship is reversed in the derived state. Characters Not Used in Numerical Analyses Epidermal Glands. One rather general observation not used in previous discussions but which supports these phylogenetic conclusions was made by Akesson (1958). In the context of a detailed commentary on sipunculan epidermal organs, he identified three groups: (1) the Golfingia group, with two types of cells and secretory products; (2) the Phascolosoma group, with only one type of cell and product; and (3) the Sipunculus group, with separate sensory and secretory cells and glands of two types like group 1 (bi- and multicellular). A plausible and parsimonious evolutionary sequence could begin with the simplest (second) type (Phascolosoma) as the ancestral form, which then led to the apomorphic type 1 (Golfingia), which in turn could have given rise to the most derived type, the third (Sipunculus).

Karyological Data "Evolution is essentially a cytogenetic process," and ignoring this fact "makes for a weak and incomplete analysis." With these words of M. White (1973:759) setting forth the consensus viewpoint, the little that is known about sipunculan genetics is presented below. This is fertile ground for future work. The chromosomal morphology of 14 species of sipunculans as determined by J. Silverstein (1986, and pers. comm., 1991) is summarized in Table n . The diploid number is 20 for all five members of the class Phascolosomatidea included in the table, and for six of the nine sipunculideans. Most species show a gradual transition from small to large chromosomes; a few exhibit a bimodal pattern. The four species in the order Phascolosomatiformes show a strong tendency toward asymmetrical arm length; that is, 70-100% of the chro-

Table 11. Karyotypes of sipunculans Chromosomal morphology

Phascolosomatidea (2N = 20) Phascolosomatiformes 1. Phascolosoma pacificum 2. Phascolosoma scolops 3. Phascolosoma perlucens 4. Antillesoma antillarum Aspidosiphoniformes 5. Aspidosiphon steenstrupii Sipunculidea Golfingiiformes (2N = 20) 6. Golfingia margaritacea 7. Thysanocardia nigra 8. Themiste hennahi 9. Themiste dyscritta 10. Themiste pyroides Sipunculiformes (2N = 18-34) 11. Phascolopsis gouldii 12. Siphonosama au.stra.le 13. Siphonosoma cumanense, Okayama 14. Siphonosoma cumanense, Okinawa 15. Sipunculus nudus

Metacentric

Submetacentric

Subtelocentric

Telocentric

—

3

7 6 + few

— most

4

+

4

1

4

1

7 8 9 10 10

2 — 1

1 2 —

— — —

6 7 6 1 15

3 3 3 — 1

1 1 — 2 1

— — — 9 —

Source: Data provided by J. Silverstein. Note: Collection locations were as follows: 1. Sesoko, Okinawa, Japan (beach near marine lab); 2. Oki Island, on Japan Sea; 3. Ft. Pierce, Ha. (near Harbor Branch Lab); 4. same as 3 and Curasao; 5. same as 1; 6. Shimoda, Japan (near marine lab); 7. Ushimado, Okayama, Japan; 8. Santa Barbara, Calif, (near Pt. Conception); 9. Hollister Ranch near Gaviota, Calif.; 10. Carmel Pt., Monteray Bay, Calif.; 11. Woods Hole, Mass.; 12. Suva, Fiji; 13. Ushimado, Okayama, Japan; 14. same as 1; 15. same as 1.

356

Within-Phylum Relationships

mosomes are telocentric or subtelocentric, and none are metacentric. The single Aspidosiphoniformes species analyzed has 50% telocentric or subtelocentric and 50% metacentric or submetacentric chromosomes. In contrast, 80-100% of the chromosomes in the nine species from six genera in the class Sipunculidea are metacentric or submetacentric; that is, they exhibit much greater symmetry of arm length. An apparent anomaly exists in one population of the widespread Siphonosoma cumanense. The Okinawa subpopulation of this species (2N = 24) appears to have mostly telocentric chromosomes, while the Okayama subpopulation (2N =18) has none. The latter group is like all three Themiste species, which also have no telocentric or subtelocentric chromosomes. The five Golfingiiformes species are much more stable (all with 2N = 20) than their four Sipunculiformes counterparts, of whom only Phascolopsis gouldii has 10 pairs of chromosomes. In addition to S. cumanense mentioned above, 5. australe has 22, and Sipunculus nudus appears to have 34 miniaturized chromosomes. It would be interesting to know the karyotypes of two highly derived members of this order, the hermaphroditic Nephasoma minutum and the parthenogenetic Themiste lageniformis. Given that telocentric chromosomes have only one arm and metacentric chromosomes have two, a comment about arm number and recombination is in order. The frequency of chiasmata formation and crossing over during Prophase I of meiosis is different in the two configurations. The probability of genetic recombination increases with the number of arms. A pair of telocentric chromosomes, with only two arms per homologous pair, is less likely to experience crossing over than is a similar pair of metacentric chromosomes with four arms (M. White, 1973). Genetic recombination rarely produces new species. More commonly it provides morphological or physiological variation (polymorphism) within a species. Extending this generalization to the sipunculan data may explain the great physiological polymorphism in the eurytopic sand- and muddwelling Sipunculidea. Although the worms whose karyotypes are known are all intertidal species, the rock-boring Phascolosomatidea taxa all live in thermally stable habitats and are exposed to insignificant fluctuations in salinity. One could speculate that the Sipunculidea is a more rapidly evolving group, able to respond to changing conditions, and therefore more common in geologically more recent (cold, deep) habitats. Most members of the Phascolosomatidea, on the other hand, are slower evolving and largely restricted to geologically older (warm, shallow) habitats.

Embryological Data

357

Finally, a correlation between chromosomal symmetry and asymmetry and apomorphic versus plesiomorphic character states is fairly well established for plants and some insects (M. White, 1973). It seems clear that ancestral taxa have high proportions of telocentric chromosomes (8 of 9 in grasshoppers), and more derived taxa have high numbers of metacentric chromosomes (20 of 23 in ladybird beetles). Assuming this to be true for sipunculans as well, and incorporating the information presented above, I propose the following evolutionary hypothesis for this phylum, one that is consistent with other information: The ancestral population had little or no chromosomal symmetry (i.e., they were phascolosomatids). Some of these telocentric units experienced a redistribution of material in a more symmetrical fashion. These mutated chromosomes produced new taxa within the Phascolosomatidea (e.g., the aspidosiphonids). Larger differences in chromosomal morphology (more chromosomes with equal arm length) led to larger differences in adult worm morphology and even a new class, the Sipunculidea, with mostly metacentric chromosomes.

Embryological Data Rice's (1985a) model for the evolution of sipunculan larval forms begins with a presipunculan ancestor having an egg with a simple envelope and low yolk content that developed into a planktotrophic trochophore larva. From this stock evolved an ancestral primitive sipunculan with a moderately yolky egg, a thick egg envelope, a nonfeeding trochophore with a persistent egg envelope (retarding planktotrophy), and a planktotrophic pelageosphera stage. The increased yolk and thickness of the egg envelope were the two major evolutionary trends leading to the original pelagosphera. From this hypothetical starting point Rice envisioned a bifurcating evolutionary street to the extant forms, one branch leading toward an increase in yolk and a decrease in the length of the pelagic stage, the other leading to a decrease in yolk and an increase in the length of planktotrophic pelagic life. I suggest that there is a less complex, more parsimonious model (Table 12, Fig. 87). It requires a single nonbranching path, with no reversals, from a single presipunculan ancestor, in the direction of gradual increases in

Within-Phylum Relationships

358

Table 12. Summary of sipunculan developmental pathways Type" Number of species Vermiform juvenile Pelagosphera larva Planktotrophic Lecithotrophic Trochophore Planktonic life Egg Size Yolk content Envelope Cladogenic eventsb

PP (IV)

LP (III)

T(ID

D(I)

10 X

7 X

2 X

3 X

X

—

—

X X Weeks X Medium Medium Medium

— —

— — —

X Months X Small Low Thin A

X Days X Medium Medium Medium B

None X Large High Thick C

Note: Presented in an evolutionary context presuming a loss or simplification at each step. a PP = planktotrophic pelagosphera; LP = lecithotrophic pelagosphera; T = trochophore; D = direct. The number in parentheses is Rice's (1985a) type number. b A = yolk content of egg increases, egg envelope thickens, egg size increases, larva unable to feed on plankton, shorter time in plantkon; B = yolk content increases, egg envelope thickens, egg size increases, loss of pelagosphera, shorter time in plankton; C = yolk content of egg increases, egg envelope thickens, egg size increases, direct development, no larval life.

yolk content, thickening of the egg envelope, and decrease in time of planktonic existence. Larval lifestyles went from long-lived planktotrophic, to shorter lecithotrophic pelagosphera, to trochophore only; and in a few special cases on to direct development (Rice's types IV, III, II, and I). This model requires the extension of the larval life of the presipunculan through the addition of the novel pelagosphera—as does Rice's model— but without the immediate increase in yolk and thickening of the egg envelope that Rice's model postulates (1985a). The available data, reinterpreted this way and combined with other, nonembryological, research, lend support to the new model. Four of the six genera in the less-derived class, Phascolosomatidea, are known to have the least derived ontogeny (Rice's type IV), including the species Phascolosoma agassizii, P. perlucens, P. nigrescens, Antillesoma antillarum, Apio soma misakianum, Aspidosiphon parvulus, and A.fischeri. No members of this class are known to have any type of larvae other than Rice's type IV (long-lived planktotrophic). Representatives of the class Sipunculidea exhibit all four developmental types. Two members of the family Sipunculidae (Sipunculus nudus and Siphonosoma cumanense) have type IV development, as does the

Embryological Data

359

t

t

t

«

o

o

O

Figure 87. Proposed evolutionary sequence of sipunculan developmental patterns, from left to right, incorporating text discussion and Table II. Each drawing in this figure is represented by an X in Table 11.

golfingiid Nephasoma pellucida. Three other golfingiids (G. vulgaris, G. elongata, and Thysanocardia nigra) and two themistids (T. alutacea, T. lageniformis) exhibit type III development (no planktotrophic stage). Phascolion strombus has type II development (trochophore only), as does the enigmatic Phascolopsis gouldii, whose familial affinity is ambiguous but is currently considered to be Sipunculidae (formerly Golfingiidae).

360

Within-Phylum Relationships

pyroides, Phascolion cryptus, and the hermaphroditic Nephasoma minuta; each is in a different family within the order Golfingiiformes. It seems very probable that the class Sipunculidea began with type IV development, and that types III, II, and I each evolved more than once, within different genera, during subsequent cladogenic events (homoplasy). Therefore, developmental pathways can be used as a guide to the evolution of sipunculan higher taxa, but they must be used with caution and preferably in conjunction with other kinds of information.

Zoogeographical Data: Paleo-Oceanographic Analysis

As I asserted above, some early sipunculans probably existed in Paleozoic times, more than 500 million years ago (Ma). (In pre-i98os literature, Ma was abbreviated as MYBP, million years before present, and a few recent works use Ma BP). The genesis of clades was not instantaneous, however, and the present distribution patterns around certain geologically important regions are informative. Theories about the size, shape, position, and movements of the land masses on this planet have been produced under the rubric of plate tectonics or continental drift, mostly since i960. Although most of this work has focused on land masses, it is possible to infer information about the surrounding oceans, and since 1970 a few authors have concentrated their studies on the ocean basins. Authors' opinions and conclusions vary, and the literature is not consistent with regard to dates and shapes. The precision lessens as one goes back in time. Table 13 presents the names and dates of the geological time units along with major tectonic events (also see Fig. 88). The following overview is based partly on A. Smith et al., 1981, and Weijermars, 1989, which incorporate and modify data published only a decade earlier in works such as Fleming, 1978, and Grant-Mackie, 1978. The literature on the probable times and rates of extinction and speciation in different parts of the oceans is far too complex to be adequately considered in this small space. Part of the confusion centers on definitions of terms such as old and young and whether one is dealing with plants or animals; plankton, nekton, or benthos; infauna or epifauna. An Eocene event is old if one is talking about the deep Atlantic Ocean but very young in terms of life in the Pacific. A simplistic summary is this: taxa found in high-stress, unstable habitats

36i

Zoogeographical Data Table 13. Geological time in the Phanerozoic eon and zoogeographically significant paleo-oceanographic events Paleozoic periods Ediacarian Cambrian Ordovician Silurian Devonian Carboniferous Permian Mesozoic periods Triassic Jurassic Cretaceous

675 570 505 438 408 360 286 248 213 140

Cenozoic periods and epochs Tertiary (Paleogene) Paleocene 65 Eocene

55

Oligocene

38

(Neogene) Miocene

25

Pliocene Quaternary Pleistocene Holocene

2 0.01

Pangea forms.

Pangea splits and Tethys Sea forms; Madagascar splits from Africa. Early: Atlantic begins to form; Tethys at maximum size; Madagascar arrives at present location; India splits from Africa. Late: N and S Atlantic join; Bering Strait closed by land bridge.

New Zealand breaks away from Australia-Antarctica; North Atlantic opens to Arctic; deep sea warming. Australia splits from Antarctica; deep water connections between N and S Atlantic form; India arrives at present location; present biogeographic provinces begin to form along with polar ice; land north of Australia fragmenting and adjacent seas forming. Atlantic reaches present depth; Australia arrives, and there is deep water between it and Antarctica; Antarctic sea ice forms. Early: Drake Passage opens; Africa meets Eurasia, closing eastern Mediterranean; Antarctic ice cap grows and deep Pacific cools. Late: broad IWP shelf; upwelling off SW Africa; Iberian portal closes. Panama isthmus closes; Bering Strait reopens; glaciation with permanent ice at both poles. Biogeographic provinces well formed; periodic glaciation. Continued temperature and sea level fluctuations.

Note: Numbers are million years since the start of the period or epoch.

(temperate, intertidal) are younger than those found in more stable areas (deep sea, tropical). Differing viewpoints do exist, of course. Some authors suggested that the tropics are no older or more stable than the Arctic. Both areas underwent significant Miocene thermal changes, and Valentine

Zoogeographical Data

363

(1984:649) argued that "if there are any shallow-sea regions likely to harbor particularly large numbers of old species, they might be the temperate and subtropical zones." Many references to the antiquity of marine taxa apply only within Cenozoic, or even Neogene, times. A safe guideline is to assume this to be what the author meant unless it is specifically stated otherwise. Paleozoic (570-248 Ma) During the Paleozoic period the land was formed into three separate continents: Gondwanaland (the southern land masses), Laurasia (North America and Europe west of the Urals), and eastern Eurasia. These masses migrated over the surface of the earth to the Southern Hemisphere, where eventually they coalesced into a single supercontinent, Pangaea, sometime late in the Paleozoic (Boucot and Gray, 1983). Mesozoic (248-65 Ma) Pangaea persisted for at least 100 million years (280-180 Ma), during the Triassic and part of the Jurassic. A single continent meant a single surrounding ocean, the Eo-Pacific, or Panthalassa, which was much larger than today's Pacific. The Pacific Ocean has been shrinking since its formation, partly because it is surrounded by subduction zones (where one tectonic plate slides down and under another) that consume ocean floor 2 4 cm/yr faster than it is being produced along the spreading zones. The change in dimensions has occurred asymmetrically because the subduction along the eastern margin is faster than on the western end, and the principal spreading zone that was the Mid-Pacific Ridge of 65 Ma is now the East Pacific Rise. Viewed on a geological time scale, the ocean floor has not been a static habitat for benthic invertebrates. There is no place where the floor is older than 180 million years (Jurassic), and 60% of it is less than 65 million years old (end of Cretaceous). About 180 Ma Pangaea split into two parts: Laurasia (northern) and Gondwanaland (southern). The two land masses were separated by a shallow, warm ocean called the Tethys Sea. This sea reached its maximum size during the Cretaceous, about 140-135 Ma. Its growth ceased when Gondwanaland broke apart, beginning the creation of the Atlantic Ocean. During this period the Tethys linked the Gulf of Mexico to the northern Pacific

364

Within-Phylum Relationships

Ocean. It was not until the end of the Mesozoic that the Bering land bridge separated the Arctic regions from subtropical waters (Dunton, 1992). While there is some disagreement over the matter, depending on which data are more heavily weighted, the Tethys probably had a net eastward flow (Barron and Peterson, 1989; P. Smith and Westermann, 1990; Follmi et al., 1991). The Tethys shrank but persisted until the Miocene, about 18 Ma (earlier authors placed this at 36 Ma in the Oligocene), when Africa collided with Eurasia along a complex subduction line in the Mediterranean region. Fragments of the uplifted (obducted) Mesozoic Tethys Sea floor (18085 Ma) appear as ophiolites along the Alpine chain between the western Mediterranean and the Indian Ocean. Much of the widespread Cretaceous Tethys marine fauna disappeared before the Miocene, but many Pacific islands functioned as refugia for some of these Mesozoic taxa (Kay, 1979). Elsewhere, in the late Jurassic (165 Ma) Madagascar split off from East Africa in the region of Kenya-Somalia and moved southeast, arriving at its present position 125 Ma, in the early Cretaceous (Rabinowitz et al., 1983). India began a longer move at about this time. It broke away from southeastern Africa in the Cretaceous (145-120 Ma), moved northward, and collided with Asia during the Eocene (50-40 Ma). However, its long isolation did not result in significant development of endemic marine species (Briggs, 1989). Cenozoic (65 Ma-Present) Much more information is available about the Cenozoic period. Rather than examining the entire planet, I focus below on subsets of the world ocean system and track events in those regions independently—keeping in mind their interdependence. First, however, I present an overview. On a geological time scale, the present array of temperatures and levels of the world's oceans are neither of long duration nor likely to remain as they are indefinitely. In other words, global warming and cooling are not new phenomena, as even a cursory inspection of the more recent literature on global dynamics shows. The overall pattern of temperature changes has been known for decades (see Ekman, 1967; Briggs, 1974). For example, the Mesozoic polar seas were temperate ( I 6 - I 7 ° C ) , and the early Tertiary European Atlantic Ocean shelf fauna was clearly tropical, as evidenced by fossil remains of

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365

the reef-building corals, echinoderms, mollusks, etc. During the Miocene and Pliocene, however, there was a dramatic shift in the fauna to more temperate forms. This coincided with the growth of the polar ice caps, which had begun in the Oligocene, and the partitioning of the Tethys Sea, which resulted in the separation of the Indian and Atlantic oceans by the Mediterranean. The present thermally defined biogeographical provinces began to form around 50-40 Ma along with the polar ice but did not become well established with a polar fauna and cold, deep water until about 2 Ma (Berggren and Hollister, 1974; Benson et al., 1984). Cenozoic Temperature. An abrupt but short-lived deep-sea warming occurred 57 Ma at the end of the Paleocene (Kennett and Stott, 1991). During the Paleocene and Eocene (65-38 Ma) the surface water of the Antarctic was I3-I4°C and the bottom water was about io°C, significantly warmer than today's near-zero water (sea water freezes at — 2°C). The decoupling of the benthic and planktonic ecosystems is indicated by the extinction of 72% of the larger benthic foraminiferans and the lack of impact on their shallow-water counterparts. A similar warming and mass extinction of benthic forams occurred at the same time in the far northern Atlantic as the seaway opened between Norway and Greenland. There is evidence to suggest global warming, or a greenhouse effect, resulting from the buildup of C0 2 as a side effect of volcanic activity associated with plate tectonics. The rapid warming, which took less than 3000 years, resulted from salty, dense Tethys Sea water replacing the colder polar water present in the deep sea. The resulting drop in oxygen and rise in salinity and temperature formed a combination lethal for many taxa. The change in ocean circulation and the increasing instability of the water column's abiotic attributes might have resulted from an early greenhouse warming event. If benthic forams were so dramatically affected, it is hard to imagine that sipunculan populations survived unscathed, despite Vermeij's suggestion that warming generally causes fewer extinctions than comparable cooling (Vermeij, 1987). These events of 57 Ma were the reverse of the extinction events seen a relatively short time earlier, at the beginning of the Tertiary (K-T boundary, 65 Ma), when the shallow fauna was greatly affected and the deep fauna experienced very little change. Zinsmeister and Feldmann's (1984) historical analysis of five classes of marine invertebrates approaches the Tertiary ocean system from a different

366

Within-Phylum Relationships

perspective. The authors noted an early warming trend in the southern mid-latitudes and suggested that the shallow Antarctic waters functioned as a Paleocene "holding tank" for ancestral taxa. During cooler times in the Oligocene and Miocene (38-5 Ma), these taxa migrated northward toward the equator, diversifying as they went. This latitudinal and taxonomic expansion continued more broadly into the Pliocene and Pleistocene, and some previously shallow taxa adapted to deeper habitats. The deeper Atlantic Ocean was clearly warmer than it is today until the early Oligocene (35 Ma), when Antarctic sea ice formed (Hammond, 1976). The growth of the Antarctic ice cap caused the cooling of the deep tropical western Pacific and a distinct change in benthic foraminiferan communities there (Woodruff et al., 1981). The Arctic surface water cooled to below 5°C about 12 Ma (Dunton, 1992). Cenozoic cooling was significant in the lower latitudes, especially in shallow waters, which dropped from around 25°C to around I5°C between 55 and 35 Ma (Valentine, 1984). Tropical waters remained cool until about 20 Ma, when they began warming back to the present temperature of 2830°C. One important conclusion to be drawn from this information is that today's tropical regions are not geologically old; like high-latitude climates, they are mostly of Neogene age. Later in the Miocene (10 Ma), along the coast of Namibia (southwestern Africa), an upwelling of cold, nutrient-rich water provided a biologically productive environment. Microfossil populations indicate that this productivity dropped sharply at the end of the Miocene (Siesser, 1980), suggesting that most deep-sea species are of geologically recent age. Briggs (1974) supported this idea on the basis of the assumption that earlier, during the Mesozoic, the deep sea was largely anaerobic and therefore not a suitable habitat for most metazoans. The inflow of warm Tethian water from the Mediterranean into the deep Atlantic slowed and was finally cut off about 6 Ma during the Pliocene when the Iberian portal formed. The resultant cooling of the Atlantic in the east was complemented from the west when the Panamanian connection between the tropical Atlantic and Pacific closed (about 3.5 Ma). The subsequent Pleistocene glaciations between 3.5 and 1.8 Ma and the permanent sea ice at both poles accelerated the cooling process. As a result of this cooling, the deeper ostracods became more cosmopolitan in their distribution as they became separated from the more restricted shallow-water species. A similar historical sequence is likely for sipuncu-

Zoogeographical Data

367

lans—that is, deeper-water species became widespread. Also during this time (in the Pliocene, 5-2 Ma) 50-75% of the North Atlantic bivalve species became extinct (Jablonski and Bottjer, 1991). Periodic glaciations continued during the Pleistocene (2-0 Ma), separated by periods of warmth similar to present conditions. These repeated fluctuations resulted in local extinctions and disjunct distributions (Fleming, 1978). The sea ice and periodic glaciation in the Arctic between 2 and 0.7 Ma were major cladogenic forces (Dunton, 1992). During the late Cenozoic, oscillations between glacial and interglacial thermal and water circulation patterns occurred in the eastern Atlantic with a periodicity of 30,000 to 40,000 years (Jansen et al., 1986). A view of temperature and circulation patterns in the Atlantic (tropical and Caribbean), determined by examining fossil foraminiferans, indicates three incursions of cool water over the last 135,000 years (Prell et al., 1976). The impact of such climatic catastrophes on sipunculans may well have been dampened by the fact that they are low-energy infauna. Many species feed largely on decomposing organic material rather than depending directly on living plants, and they are generally small-bodied. Thus, they are less likely to be affected by short-term fluctuations and possibly less prone to extinction (see Vermeij, 1987). Cenozoic Sea Level. Ninety-six sea level changes occurred during the 600 million years of the Phanerozoic eon, and these can be grouped into three levels of magnitude and frequency (Vail et al., 1978). The sea was at its highest level in the late Cretaceous (about 350 m higher than present), creating extensive epicontinental seas. Before and after this the level was much lower—about 150-250 m below present levels in the early Jurassic, the mid-Oligocene, and the late Miocene. These fluctuations are attributed to geotectonic and glacial events. As a result of Quaternary glaciations, the Arctic Ocean experienced periodic changes of sea level every 10,000-20,000 years. The level dropped about 85 m each time, exposing large areas of continental shelf and resulting in local extinctions of shelf fauna (Dunton, 1992). Using fossils of Pleistocene ostracods and pollen from along the east coast of the United States as indicators, Cronin et al. (1981) identified at least five warm intervals over the past 500,000 years when the sea level was 6-7 m higher than present. The glaciated Canadian and New England Atlantic coast continued to undergo change during the past 15,000 years, and today's shallow subtidal

368

Within-Phylum Relationships

configuration was not reached until about 3000 years ago (Bousefield and Thomas, 1975). During the previous 12,000 years the sea level was much lower and the temperature was cooler. Cenozoic Subregional Events The Atlantic Ocean. The Atlantic first appeared during the Cretaceous and achieved significant size about 100 Ma when the North and South Atlantic oceans merged at shallow depths. During the early Cenozoic, the Atlantic continued to spread outward from the Mid-Atlantic Ridge, further separating South America from Africa, and North America from Europe (Boucot and Gray, 1983). That spreading continues today. In the far north, between Norway and Greenland, the Atlantic became connected with the Arctic Ocean about 57 Ma. Deep-water connections between the North and South Atlantic did not form until about 50 Ma (Hammond, 1976). Mediterranean Sea and Northeastern Atlantic. The modern Mediterranean Sea is a remnant of the Tethys Sea. It began to form when the eastern end of the Tethys closed, about 18 Ma. The western end of the Mediterranean was at least partially closed by the formation of the Iberian portal about 6 Ma, near the end of the Miocene. This effectively cut off access to and from the eastern deep-water Atlantic Ocean (Keigwin, 1982; Benson et al., 1984). The Mediterranean may have been totally closed off between 6 and 5 Ma, when much evaporation occurred (the Messinian salinity crisis). The basin refilled when the Gibraltar gate opened at the end of this period (Hammond, 1976; de Weerdt, 1989). Shallow-water marine taxa that lived in the Tethys during Paleogene times could still persist today in both the eastern Atlantic-Mediterranean and the western Indian oceans (see Table 14). Although some taxa may have migrated around the tip of South Africa, it is safe to assume that most Indo-Atlantic species are older than 18 million years. Conversely, species now found on only one side of this 18-million-year-old land barrier probably evolved after the barrier formed; that is, are younger taxa. This last view is based on the assumption that there have been no abiotir or biotic changes since that time that were lethal to past generations of the taxa under study. Such local extinctions are known to have occurred in other marine taxa, and these restricted sipunculan populations may actually represent relicts of once broadly distributed, older species (see Valentine, 1984).

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South Atlantic. At the beginning of the Miocene (25 Ma), the Drake Passage opened between Antarctica and South America, allowing an eastward-flowing circumpolar current, an event that had global significance. The current gained in intensity until the Pleistocene (Fleming, 1978; Vermeij, 1991a). The fossil record of mollusks and echinoderms illustrates how, during the late Cenozoic, as temperatures cooled, some taxa with planktonic larvae successfully migrated from the eastern Atlantic and Mediterranean, across the Indian Ocean, and into the western Pacific. The same record shows how other taxa took advantage of this late Cenozoic cooling to migrate from western Europe or western North America southward past Africa or South America, eastward via the circumpolar current, and then northward past Australia to Japan (Fleming, 1978). Western Atlantic and Eastern Pacific. The connection between the western Atlantic and eastern Pacific oceans closed during the Pliocene (about 3.5 Ma) when Central America uplifted and formed the Panamanian land barrier. Applying the same logic as was used above, taxa now on both sides of Central America may be presumed to have been in existence for more than 3.5 million years (see Table 14). The significance of taxa restricted to one side of this barrier is less certain, however, since the present habitats are different. On the Pacific side, for example, there is coastal upwelling of cold water, a paucity of coral reefs and sedimentary rock, and a scarcity of macroalgae. Nevertheless, in the absence of a fossil record, these patterns may be useful for dating cladogenic events. Thus, taxa on only one side of the Panamanian isthmus may be among the youngest in the phylum. One exception that may prove the rule was reported by Laguna (1987). Electrophoretic studies of two closely related trans-Panamic, endemic barnacle species show a greater genetic distance between the two than expected. The molecular clock suggests speciation in the upper Miocene, well before the formation of the land barrier. Laguna offered no mechanism by which this sympatric speciation might have occurred. After studying invertebrate taxa such as crabs and echinoderms, which have a fossil record that can be dated, Ekman (1967) asserted that there are more amphi-American genera than species, and that amphi-American species are demonstrably older than species found on only one side of the Panamanian barrier. If it is safe to extrapolate from benthic foraminiferans to sipunculans, then shelf-dwelling species are younger than deeper taxa along the east

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Within-Phylum Relationships

Table 14. Sipunculans living in historically significant areas from shallow (1-100 m) or upper slope (100-1000 m) depths 1.

Eastern Atlantic and western Indian Oceans Antillesoma antillarum, Apionsoma murinae bilobatae," Apionsoma trichocephalus, Apionsoma {Ed.) pectinatum, Aspidosiphon muelleri,b Aspidosiphon (Pa.) laevis, Aspidosiphon (Pa.) steenstrupii, Golfingia vulgaris? Phascolosoma nigrescens, Phascolosoma perlucens, Phascolosoma stephensoni,b Phascolosoma (Fi.) capitatum? Phascolion (Is.) convestitum,b Sipunculus nudus,h Sipunculus norvegicus*

A.

Eastern Atlantic and Mediterranean but not NW Indian Ocean Apionsoma murinae murinae? Phascolosoma (Fi.) capitatum," Aspidosiphon (Ak.) albus, Aspidosiphon (Ak.) venabulum, Aspidosiphon (Ak.) zinnia Golfingia elongata, Onchnesoma steenstrupii,^b Onchnesoma squamatum,^ Phascolosoma granulatum, Phascolion (Is.) tuberculosum,"* Phascolion (Le.) hupferi, Siphonosoma arcassonense,0 Thysanocardia procera0

B.

NW Indian Ocean and/or Red Sea, but not Mediterranean or eastern Atlantic Apionsoma misakianum, Aspidosiphon coyi, Aspidosiphon elegans, Aspidosiphon gracilis, Aspidosiphon (Pa.) planoscutatus,c Cloeosiphon aspergillus, Lithacrosiphon maldivensis, Nephasoma rutilofuscum,c Phascolosoma albolineatum, Phascolosoma meteorif Phascolosoma pacificum, Phascolosoma scolops, Phascolosoma (Fi.) lobostomum, Phascolion abnorme, Phascolion robertsoni, Phascolion (Le.) valdiviae sumatrense? Phascolion (Vi.) cirratum," Sipunculus longipapillosus, Sipunculus robustus, Sipunculus (Au.) indicus, Siphonosoma australe, Siphonosoma cumanense, Themiste (La.) lageniformis

2.

Both sides of Central America (all are also amphi-Pacific) Antillesoma antillarum,6 Apionsoma misakianum, Apionsoma trichocephalus,6 Apionsoma (Ed.) pectinatum,6 Aspidosiphon (Pa.) fischeri, Lithacrosiphon cristatus, Phascolosoma nigrescens,6 Phascolosoma perlucens,6 Sipunculus nudus,6 Sipunculus phalloides, Sipunculus polymyotus, Xenosiphon branchiatus

A.

Atlantic side of Central America, but not the Pacific Phascolosoma (Fi.) capilatum," Aspidosiphon exiguus? Aspidosiphon gosnoldif Aspidosiphon elegans, Aspidosiphon misakiensis, Aspidosiphon (Ak.) mexicanus, Aspidosiphon (Ak.) albus, Aspidosiphon (Ak.) zinni? Aspidosiphon (Pa.) parvulus,c Golfingia elongata, Nephasoma pellucidum, Phascolion caupo,c Phascolion medusae? Phascolion (Is.) microspheroidis? Phascolion (Le.) cryptum? Sipunculus norvegicus? Sipunculus robustus, Siphonomecus multicinctus,c Siphonosoma cumanense, Themiste alutacea,0 Themiste (La.) lageniformis, Thysanocardia catharinae*

B.

Pacific side of Central America, but not the Atlantic Aspidosiphon gracilis schnehageni,0 Siphonosoma vastum "Primarily a slope species. b In the Mediterranean also. c Endemic. d Also in group 1, above.

coast of the United States. Furthermore, northern North American species are likely to be younger than southern ones (Buzas and Culver, 1984). The idea that extinction and cladogenesis of higher taxa occur more rapidly in stressful habitats or where long-term stasis is disturbed is not

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new (see Littler et al., 1985; Ross and Allman, 1991). The same principle may support the proposition that temperate, shallow-water species within eurytopic sipunculan genera are younger than those that live in stable habitats such as the tropics or the deep sea. This does not contradict the fact that stable areas have greater taxonomic diversity (see Sanders, 1968; Sanders and Hessler, 1969). The debate about the antiquity of taxa in the deep sea continues, but Vermeij (1987) is among those making a strong case for the deep sea serving as a haven for ancestral or relict species that were driven out of shallower habitats by biotic and/or abiotic forces. He pointed to the high number of adaptively anachronistic species that are defensively inferior and went on to assert that these deep-sea stocks do not serve as sources of genetic material for the reinvasion of shallower habitats. The infaunal habitat itself is a kind of haven, and deep-sea infaunal sipunculans thus are especially well protected. Endolithic animals (e.g., Lithacrosiphon or Cloeosiphon) are also well protected and are presumed to have evolved from infaunal ancestors. Indo-Malayan Region and the Pacific Ocean. An area of particular interest to marine biogeographers is the current Indo-West Pacific (IWP), especially the Indo-Malayan Archipelago, which is asserted to be the center of origin and dispersal for many taxa. If one traces this region back through geological time, one sees significant changes from the early Mesozoic, when it was the open western part of the Panthalassa. Australia to Southeast Asia. Of particular interest is the movement of Australia, which was part of the Antarctic land mass until the end of the Paleocene (55 Ma). New Zealand had broken off at least 5 million years before Australia began its 20-million-year journey northward through temperate seas. The separation from Antarctica became complete enough for deep currents to run south of Australia about 30 Ma. The Tasman and Coral Sea basins were formed by this time, and additional fragments of the Australian land mass began to splinter off. During the Eocene and Oligocene (45-29 Ma) the New Hebrides, Norfolk, and South Fiji basins formed; the North Fiji basin formed since the late Miocene, less than 10 Ma. Much of this activity involved Sumatra and Java as well as the Malay Peninsula (Grant-Mackie, 1978). The string of islands from Australia-Papuasia to Southeast Asia developed in conjunction with a southern movement of Southeast Asia (Mayr, 1988). It was not until the upper Miocene, however, less than 10 Ma, that the present broad, shallow shelf and archipelago configuration was in

372

Within-Phylum Relationships

place to form the incomplete and permeable boundary between the Pacific and Indian oceans (Newman, 1991). Thus, the Indian Ocean, as a region distinct from the western Pacific, is geologically recent. The formation of the Andaman Sea and the opening of the Sunda Strait (between Java and Sumatra) did not occur until 2 Ma. Therefore, any cladogenic events in this tropical archipelago cannot be much older than a few million years. An interesting observation about the exaggerated importance of the Indo-Malayan region as a center of origin of marine taxa was made by Ekman (i967:chap. 4), whose examination of the fossil record suggested that before the end of the Cretaceous there were no significant differences in diversity between the IWP and the Atlanto-East Pacific (AEP). The present-day difference is the result of significant climatic cooling experienced by the AEP during the Miocene, which led to local extinctions and emigration of many taxa. The IWP, which experienced no such trauma, preserved its earlier diversity and added to it in later times. This statement assumes a barrier between the western and eastern Pacific regions. Eastern Pacific. The Eastern Pacific Barrier (EPB) is acknowledged to be a very effective filter but not an impassible barrier. As an example, only 4% of the Hawaiian mollusks, and 16% of the Hawaiian coral fauna, reaches the west coast of the Americas (Vermeij, 1991a). The question of the EPB's antiquity was addressed by Grigg and Hey (1992). Their analysis of Mesozoic and Cenozoic fossil corals showed that no barrier existed throughout the Cretaceous, and dispersal was from east to west. This dispersal was aided by stepping-stones—central Pacific islands that subsequently drowned (guyots). Hamilton's (1956) work on tropical corals provided the first demonstration of this Cretaceous phenomenon, but the complete explanation had to await an understanding of plate tectonics. The present island groups are not good stepping-stones, given their placement relative to the main current systems. Thus, the EPB did not exist before Cenozoic times, and isolation permitting allopatric speciation was less likely then, despite the wider ocean basin. North Pacific, Arctic, and Far North Atlantic. In the mid-Pliocene (43.5 Ma), when the Panamanian isthmus formed a barrier in the tropics, the Bering land bridge between Asia and North America was breaking up. The bridge, a barrier between the Pacific and Arctic oceans, had existed since 65 Ma. When it ceased to exist, a new migration route was opened. Most species seem to have migrated from the northern Pacific to the

Conclusions and Assumptions

373

Atlantic Ocean (Vermeij, 1991a, 1991b; Dunton, 1992). The Arctic Ocean fauna located between the two major oceans is young and of mixed origins. Most of the nearshore fauna (but not the flora) has Pacific ancestry. This youth (less than 3.5 million years) is attributed to repeated Pleistocene glaciations that were lethal to inhabitants (Dunton, 1992).

Conclusions and Assumptions

Based on the paleo-oceanographic information and the zoogeographical data summarized earlier and in Table 14, at least four of the five Phascolosomatidae genus groups are more than 18 million years old, and probably much older {Phascolosoma [Fisherana] being a possible exception; i.e., younger). In the Aspidosiphonidae, only two of the three Aspidosiphon subgenera have pre-Miocene origins, but considerable cladogenesis has occurred since then. The subgenus A. (Akrikos) is less than 18 million and possibly less than 3 million years old. Lithacrosiphon evolved in the interval between 18 and 3 Ma, and Cloeosiphon is at least that young, probably first appearing less than 3 Ma (Fig. 89). Within the class Sipunculidea, it appears that Sipunculus is more than 18 million years old. Active cladogenesis occurred between 18 and 3 Ma, including the genesis of the closely related Xenosiphon. The proposed early appearance (400 Ma) of Siphonosoma is not supported by these data unless one invokes local extinctions in the eastern Atlantic and eastern Pacific, where this genus is absent. The remaining genera of the order Sipunculiformes—the monotypic Phascolopsis and Siphonomecus—are the youngest, probably less than 3 million years old. The Golfingiiformes genera Golfingia and Phascolion are much older, from the Paleozoic, but speciation was probably common during the Neogene. Thysanocardia, Themiste, and many shallow-water Nephasoma appear younger, on the order of 3-15 million years old. Most of the Nephasoma and Onchnesoma species are found in cold, deep water. It appears likely that while Nephasoma originated in the late Paleozoic, significant speciation in that genus and the first appearance of Onchnesoma probably occurred 15-3 Ma in the Neogene. In summary, I propose that the phylum Sipuncula had its origins in the earliest Paleozoic, and that by the late Paleozoic representatives of five of the six extant families existed, living in all of the then-available oceanic habitats. By the mid-Mesozoic, eight of the modern genera existed, and

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Within-Phylum Relationships

this situation persisted until mid-Cenozoic times. By the end of the Miocene, all except three genera were present, and these appeared during the Pliocene (Fig. 89). Without a fossil record we cannot know whether the single species in a monotypic genus represents a remnant of a once polytypic genus or is the only one that ever existed. A genus with a single extant species may well have contained 10 species before the end of the Cretaceous. While the data cannot be used to propose extinction events or rates, there is no reason to believe that sipunculans are immune to the environmental changes that have had negative impacts on other benthic marine invertebrates. The fact that they are infaunal or endolithic animals may provide some protection, but one can only assume that what we see today is a very incomplete picture of the diversity present in the phylum throughout time.

20

Evolutionary Hypothesis

In this chapter items currently considered to have the opposite polarity of that presented in Cutler and Gibbs, 1985, are marked with an asterisk, and new items are marked with a double asterisk. What follows is a synthesis of all the material presented in this book. Ancestor

The revised hypothetical ancestral sipunculan (RHAS) had a body wall with a continuous longitudinal muscle layer and no epidermal coelomic extensions. The anterior end of the trunk bore the anus, was without a horny shield, and tapered into the introvert along the same axis. The introvert carried *regular rings of sculptured proteinaceous hooks with **basal spinelets, and the tentacular crown consisted of a *crescent of small nuchal tentacles plus a circumoral collar (cuticular fold) that was the precursor of a set of peripheral tentacles. Internally, the contractile vessel was small and did not have villi. Also present were two pairs of unfused, equal-sized introvert retractor muscles, two nephridia, *possibly bilobed, and a complete spindle muscle ^attached to the posterior end of the trunk. **The epidermal organs consisted of only one cell type and one secretory product. This Cambrian population lived in shallow, warm seas and **had 10 pairs of mostly telocentric chromosomes (2N = 20). The RHAS produced an egg with very little yolk and a thin egg envelope that developed into a trochophore. **This larva grew into a rather long-lived planktotrophic pelageosphera stage (type IV) and eventually settled to become a juvenile worm. Process A plausible and parsimonious evolutionary scenario beginning with the RHAS is shown as a dendrogram in Figure 89. That figure stops at the

376 Genus Extant species Holocene Pleistocene Quaternary Pliocene Miocene Oligocene (c) Eocene Paleocene Tertiary CENOZOIC Cretaceous Jurassic Triassic MESOZOIC Permian Carboniferous Devonian Silurian Ordovician Cambrian Ediacarian PALEOZOIC

Evolutionary Hypothesis Li As CI An Ph Ap Xe Si Sm Sh 2 19 1 1 16 6 2 10 1 10

Ps 1

Go Ne Ty Th 12 23 3 10

Pn On 23 4

RHAS

Abbreviations: Li = Lithacrosiphon, As = Aspidosiphon, CI = Cloeosiphon, An = Antillesoma, Ph = Phascolosoma, Ap = Apionsoma, Xe = Xenosiphon, Si = Sipunculus, Sm = Siphonomecus, Sh = Siphonosoma, Ps = Phascolopsis, Go = Golfingia, Ne = Nephasoma, Ty = Thysanocardia, Th = Themiste, Pn = Phascolion, On = Onchnesoma.

Figure 89. Plausible historical representation of cladogenic events leading to extant sipunculan genera. The events occurred at nodes labeled with letters and are described in text.

generic level, but the text takes the process one step further, to subgenera. Although the scenario below is written as if it were fact, it is, at present, a working hypothesis. Early in the Paleozoic (node A on Fig. 89) a major cladogenic event resulted in the production of peripheral tentacles around the mouth and a reduction of nuchal tentacles. Concurrently the posterior spindle muscle shortened, terminating within the gut coil, and the epidermal glands became more complex with two types of cells and secretions. Significant alterations of the genetic material involving a replacement of telocentric chromosomes with chromosomes of more equal arm length (metacentric) also occurred. These changes led to a golfingiid ancestor of the class Sipunculidea.

Evolutionary Hypothesis

377

The group that retained the ancestral traits was the ancestor of the class Phascolosomidea (node A). Within this class, a major change associated with the occupation of new niches (empty mollusk shells, soft rock, and coral) was the development of a hardened, operculum-like shield at the anterior end of the trunk. At the same time this Ordovician stock experienced the loss of the dorsal retractor muscles and the loss of the basal spinelets on the hooks. Underlying these changes was the conversion of several telocentric to metacentric chromosomes. This gave rise to the ancestor of the order Aspidosiphoniformes, family Aspidosiphonidae (node B). The anterior trunk papillae, which produce the shield matrix, increased their activity, but not evenly, so that eventually the introvert axis shifted ventrally. The shield eventually came to consist of separate hardened, noncalcareous units (Aspidosiphon). Much later, a Neogene population lost the hooks in rings, giving rise to the subgenus A. (Akrikos), some of whose members remained hookless while others produced scattered hooks. Within the main stock of A. (Aspidosiphon), another line developed into the subgenus A. (Paraspidosiphon) when the longitudinal muscle layer split into more or less separate bundles during the Mesozoic. From a mid-Cenozoic member of this last subgenus a type of shield evolved in which the secreted material produced a single solid calcareous mass (Lithacrosiphon, node C). A Pliocene branch of the family lacking longitudinal muscle bands (LMBs) developed a very different anal shield made up of thick, separate, diamond-shaped, calcareous units dispersed in an ordered manner that allowed the introvert to remain on the same axis as the trunk (Cloeosiphon, node D). The main branch in the class Phascolosomidea retained more of the ancestral attributes and led to the order Phascolosomatiformes, family Phascolosomatidae (node B). The stock that changed least from the RHAS became the present-day genus Apionsoma. The development of muscle banding in some part of this stock led to the monotypic subgenus A. (Edmondsius). A split occurred when part of the early Paleozoic Apionsoma stock lost the basal spinelets on the hooks and the secondary nephridial lobes, thus leading to Phascolosoma (node E). An early dichotomy occurred within this genus when the nominate subgenus developed LMBs, leaving the small subgenus P. (Fisherana) with the plesiomorphic trait. The monotypic genus Antillesoma evolved during the Mesozoic from Phascolosoma by losing the adult hooks and gaining the linked attributes of contractile vessel villi and a larger array of tentacles (node F). Only modest changes in the developmental sequence occurred within

378

Evolutionary Hypothesis

this class; most retained the type IV mode. Some species might have produced eggs with more yolk, had a shorter pelagosphera life, or both. The other main stock at node A was the ancestor to the class Sipunculidea. This Paleozoic stock split when one branch leading to the order Sipunculiformes (node G) experienced the partial division of the body wall muscles into anastomosing bands and developed epidermal organs that had not only two types of secretory cells and products but, eventually, separate sensory and secretory cells. Coelomic extensions into the epidermis began to develop, and a wide variety of chromosomal configurations appeared within the family (e.g., 2N ranged from 18 to 34). One part of the Mesozoic Sipunculidae stock (node H) reexpressed (or redeveloped) the posterior attachment of the spindle muscle, leading to Siphonosoma, which retains all four retractor muscles. Two monotypic genera developed from Neogene Siphonosoma populations. Siphonomecus resulted from the loss of the dorsal retractors. At about the same time (node I) Phascolopsis arose from another Siphonosoma ancestor whose circular muscle layer was still an undivided sheet with no coelomic extensions. In this stock the adult hooks were lost, leaving hooks in ill-defined rings only in juvenile worms, and larval stages were limited to a trochophore only. This cladogenesis probably occurred while the marine habitat was fluctuating during the late Cenozoic glaciations. The cooling forced the stenothermal warm-water Siphonosoma ancestor to retreat into warmer water, leaving behind this relict. This situation resembles that of the corals reported in Jablonski and Bottjer, 1991. It must be noted, however, that as good a case can be made for Phascolopsis having a golfingiid ancestor (see below). The Mesozoic clade that diverged at node H lost all hooks but developed distinct, separate longitudinal and circular muscle bands and more extensive epidermal coelomic canals. This line gave rise to Sipunculus, which developed the postesophageal loop. From the nominate stock developed the small subgenus S. (Austrosiphon), in which the nephridia shifted posterior to the anus and the anterior attachment of the spindle muscle shifted from the body wall to the rectum. This latter Neogene stock also gave rise to Xenosiphon by losing the postesophageal loop and changing the nature of the coelomic extensions (node J). Returning to node G, the Paleozoic Sipunculidea stock that did not develop LMBs was ancestral to the order Golfingiiformes. Within this group the chromosomal number remained more constant (2N = 20), but a greater variety of developmental options with shorter larval lives appeared at different times in various lineages (types III, II, and I).

Evolutionary Hypothesis

379

The late Paleozoic Golfingiiformes stock split when one group lost the nuchal tentacles and one nephridium, the spindle muscle underwent vast reduction or complete loss, and the retractor muscles experienced significant fusion, leading to the family Phascolionidae (node K). A series of changes occurred within Phascolion that eventually led to five subgenera. Most of the changes involved the retractor muscles and probably are of Cenozoic age. The least derived extant taxon is P. (Isomya), which exhibits very little fusion between the equal-sized dorsal and ventral muscles. The nominate subgenus resulted from a significant reduction in the diameter of the fused ventral retractor to only half to one-fourth that of the dorsal. A significant amount of fusion of the dorsal and ventral retractors into an almost solid column led to the subgenus P. (Montuga). These three subgenera and part of P. (Lesenka) exhibit apomorphic scattered hooks. The remainder lack hooks altogether. The complete fusion of the retractors into a single muscle column produced the subgenus P. (Lesenka). From a part of this subgenus that shifted its anus out on the introvert, the monotypic subgenus P. (Villiophora) developed by adding contractile vessel villi. From some Miocene Phascolion stock, possibly a hookless P. (Lesenka), the genus Onchnesoma appeared (node L) when the dorsal retractors were lost, the ventral pair fused for almost their entire length, and the anus shifted out toward the distal end of the very long introvert. At node K, the Golfingiiformes stock that retained the spindle muscle and both nephridia gave rise to the family Golfingiidae. The main stock led to the modern genus Golfingia and its two subgenera: the monotypic G. (Spinata), which retains the plesiomorphic bilobed nephridia and hooks in rings with basal spinelets; and the nominate (but derived) subgenus, which has unilobed nephridia and some species with no hooks, some with scattered hooks, and a few with hooks in rings. This golfingiid branch divided during the late Paleozoic (node M) when a clade lost the dorsal retractor muscles, producing the ancestor to the diverse genus Nephasoma, which has many external morphological parallels to Golfingia, including the same amount of hook polymorphism. As I noted above, it is possible that Phascolopsis had a Neogene Golfingia with deciduous hooks as an ancestor; the only change required (at node N) is for the longitudinal musculature to partially divide into anastomosing bundles. From the Nephasoma stock two more groups arose. The monogeneric family Themistidae originated in the Neogene when unique stemlike extensions carrying dendritically branched peripheral tentacles appeared (node O). The genus underwent rapid cladogenesis and divided into sub-

38o

Evolutionary Hypothesis

genera having two different types of contractile vessel villi: T. (Themiste), with a few long, threadlike tubules, unique in this phylum; and T. (Lagenopsis), with the more common numerous digitiform villi. The possibility that the genus is not monophyletic (i.e., that the subgenera might have had separate origins) is not out of the question, especially given the largely disjunct distributions. Finally (node P), Thysanocardia arose from a Neogene Nephasoma stock after acquiring contractile vessel villi. This clade developed an extensive tentacular crown with an elaborate array of peripheral tentacles in addition to well-developed nuchal tentacles. This chapter contains some speculation; nevertheless, it is based on a broad synthesis of the existing knowledge interpreted by a mind that has had 30 years of experience with thousands of these animals, living and dead. Most of the patches in this patchwork quilt are real. However, there may be other ways to arrange the patches to create different end results. This compendium of information and ideas is still incomplete, and there is the need for biologists to give more attention to this small, one might say peanut-sized, group of worms. Especially helpful would be the application of newer biochemical and genetic approaches by students of evolutionary biology. Relatively few phyla exist that are small enough to be treated in their entirety as a natural group. Much phylogenetic work is necessarily restricted to one family or order; not so here—this phylum is of manageable size. I hope that the clues presented here will encourage others to unravel the remaining evolutionary mysteries.

Appendix I

Recent Species Inquirenda

and Incertae Sedis

The following is a list of recent species inquirenda (A) and incertae sedis (B) determined since Stephen and Edmonds, 1972. The list is alphabetized by species name and includes only the original description, the first use of subsequent combinations, and the publication where the current status was first proposed. (A) Phascolosoma anguineum Sluiter, 1902:36. Golfingia anguinea.— Stephen and Edmonds, i972:85.-E. Cutler and Cutler, 19878:756. (A) Phascolosomum approximatum Roule, 1898^385. Golfingia (Golfingiella) approximata Stephen and Edmonds, 1972:119.-E. Cutler et al., 1983:670. (B) Sipunculus bonhourei Herubel, 19048:479. Siphonosoma bonhourei Stephen and Edmonds, i972:64.-E. Cutler and Cutler, 1982:755. (B) Phascolion botulus Selenka, 1885:18. Phascolion botulum Stephen and Edmonds, I972:i73.-E. Cutler and Cutler, 19858:838. (B) Diesingia Chamissoi de Quatrefages, i865b:6o6.-Saiz, 19843:41. (B) Phascolosoma chuni W. Fischer, 1916:15. Golfingia chuni.—Stephen and Edmonds, 1972:136. Nephasoma chuni N. Cutler and Cutler, 1986:567. (B) Physcosoma corallicola ten Broeke, 1925:90. Phascolosoma corallicolum.—Stephen and Edmonds, 1972:298-299.-]^. Cutler and Cutler, 1990:701. (A) Phascolosoma coriaceum Keferstein, 1865^432-433. Golfingia (Thysanocardia) coriaceum Stephen and Edmonds, 1972:122. IThemiste coriacea Gibbs et al., 1983:301-302. Herein, p. 141. (B) Diesingia cupulifera de Quatrefages, 1865^607.-Saiz, 19848:41. (A) Aspidosiphon cylindricus Horst, 1899:195-198.-E. Cutler and Cutler, 1989:837.

3 82

Appendix 1

(B) Phascolosoma delagei Herubel, 19033:100. Golfingia delagei.—Stephen and Edmonds, 1972:139-140. Nephasoma delagei N. Cutler and Cutler, 1986:567. (B) Physcosoma demanni Sluiter, 1891:121. Phascolosoma (Satonus) demanni Stephen and Edmonds, I972:283.-E. Cutler and Cutler, 1983: 184. (A) Phascolosoma depressum Sluiter, 1902:39-40. Golfingia depressa.— Murina, 19643:227. Nephasoma depressum N. Cutler and Cutler, 1986:567. (B) Phymosoma falcidentatus Sluiter, 1881 a: 150. Physcosoma falcidentatus Sluiter, 1902:13. Phascolosoma (Satonus) falcidentatum Stephen and Edmonds, I972:284.-E. Cutler and Cutler, 1983:185. (A) Phascolosoma fimbriatum Sluiter, 1902:34-35. Golfingia fimbriata. —Stephen and Edmonds, 1972:143. Nephasoma fimbriatum N. Cutler and Cutler, 1986:567. (A) Phascolion ikedai Sato, i93o:20-23.-E. Cutler and Cutler, 1985a: 838. (A) Phascolosoma immunitum Sluiter, 1902:40. Golfingia (Siphonoides) immunita.—Murina, 19670:1334. Golfingia (Golfingiella) immunita.— Cutler and Murina, 1977:180. Golfingia (Apionsoma) immunita.— Cutler et al., 1983:670. Apionsoma immunitum Herein, p. 190. (A) Phascolosoma innoxium Sluiter, 1912:13. Golfingia (Golfingiella) innoxia.—Stephen and Edmonds, 1972:119.-E. Cutler et al., 1983:671. (B) Sipunculus joubini Herubel, 1905^51-54. Siphonosoma joubini Stephen and Edmonds, I972:66.-E. Cutler and Cutler, 1982:757. (B) Phascolosoma lagense W. Fischer, 1895:13-14. Golfingia lagensis.— Stephen and Edmonds, 1972:93.-E. Cutler and Cutler, 19873:756. (A) Phascolosoma macer Sluiter, 1891:114-115. Golfingia macra.— Stephen and Edmonds, 1972:149.-E. Cutler and Murina, 1977:183. Aspidosiphon macer.—N. Cutler and Cutler, 1986:568; E. Cutler and Cutler, 1989:838. (B) Phascolion manceps Selenka et al., 1883:44-45.-E. Cutler and Cutler 19853:838. (B) Physcosoma mauritaniense Herubel, 1924:110. Phascolosoma (Satonus) mauritaniense Stephen and Edmonds, I972:286.-E. Cutler and Cutler, 1983:186. (A) Phascolion moskalevi Murina, i964b:255-256.-E. Cutler 3nd Cutler 19853:839.

Appendix 1

383

(A) Golfingia (Thysanocardia) neimaniae Murina, 1976:62-63. IThemiste neimaniae Gibbs et al., 1983:302. Herein, p. 141. (B) Phymosoma nigritorquatum Sluiter, 18813:151-152. Physcosoma nigritorquatum.—Sluiter, 1902:13. Phascolosoma nigritorquatum.— Stephen and Edmonds, I972:286.-N. Cutler and Cutler, 1990:701. (A) Phascolosoma papilliferum Keferstein, 1865^433. Fisherana papillifera.—Stephen and Edmonds, 1972:332. Golfingia (Apionsoma) papillifera.—E. Cutler, 1979:174-I76.-Herein, p. 193. (A) Phascolion parvus Sluiter 1902:30-31. Phascolion parvum Stephen and Edmonds I972:i85.-E. Cutler and Cutler, 19853:839. (A) Sipunculus pellucidus Sluiter, 1902:9-10. Siphonosoma pellucidum Stephen and Edmonds, I972:69.-E. Cutler and Cutler 1982:758. (B) Dendrostoma pinnifolium Keferstein, 1865^429. Themiste pinnifolia.—Stephen and Edmonds, 1972:209.-Gibbs and Cutler, 1987:53. (B) Phascolosoma quadratum Ikeda, 1905:170-171. Golfingia (Siphonides) quadrata Murina, 1967^1335.-E. Cutler et al. 1983:673. (A) Phascolosoma reconditum Sluiter, 1900:11-12. Golfingia recondita. —Stephen and Edmonds, 1972:105. Golfingia (Apionsoma) recondita. —Cutler, 1979:372.-Herein, p. 193. (B) Phascolosoma reticulatum Herubel, 19253:262. Golfingia reticulata. —Stephen and Edmonds, 1972:105.-E. Cutler and Cutler 19873:756. (B) Phascolosoma rueppellii Griibe, i868b:643. Physcosoma ruppellii Shipley, 1902:135. Phascolosoma (Rueppellisoma) rueppellii Stephen and Edmonds, 1972:275.-E. Cutler and Cutler, 1983:181. (B) Phascolosoma rugosum var. mauritaniense Herubel, 19253:262. Golfingia (Golfingia) rugosa mauritaniensis Stephen and Edmonds, 1972:107.-E. Cutler and Cutler, 19873:752. (A) Phascolion sandvichi Murina, I974b:283~284.-E. Cutler and Cutler 19853:839. (B) Onchnesoma Sarsii Koren and Dsnielssen, 1877:143-144. Phascolosoma Sarsii Theel, 1905:83. Golfingia sarsi Gibbs 1982:121. (B) Phascolosoma scutiger Roule, 1906:81-86. Golfingia scutiger.— Murins, 19750:1085-1089.-E. Cutler and Cutler, 19873:756. (A) Physcosoma sewelli Stephen, 194^:405-407. Phascolosoma sewelli. —Stephen and Edmonds, 1972:276. INephasoma sewelli E. Cutler 3nd Cutler, 1983:181-182. (B) Dendrostoma spinifera Sluiter, 1902:41. Themiste spinifera.—Stephen snd Edmonds, 1972:212.-E. Cutler and Cutler, 1988:741.

384

Appendix 1

(B) Phascolosoma vitreum Roule, 18980:386. Golfingia vitrea.—Stephen and Edmonds, 1972:158-159. Nephasoma vitreum N. Cutler and Cutler, 1986:568. (A) Sipunculus zenkevitchi Murina, 19690:1733- 1734.-E. Cutler and Cutler 1985b: 240.

Appendix 2

Species Inquirenda and Incertae Sedis

as in Stephen and Edmonds, 1972, with Current Status

Names are as presented in Stephen and Edmonds, 1972:339-340, not always as in the original description. Sipunculus clavatus de Blainville, 1827—same. Sipunculus corallicolus Pourtales, 1851—same. Sipunculus echinorhynchus Delle Chiaje, 1823—same. Sipunculus gigas de Quatrefages, 1865b—Sipunculus nudus. Sipunculus glans de Quatrefages, 1865b—Antillesoma antillarum. Sipunculus javensis de Quatrefages, 1865b—Phascolosoma noduliferum and P. pacificum (part in each). Sipunculus macrorhynchus de Blainville, 1827—same. Sipunculus microrhynchus de Blainville, 1827—same. Sipunculus rapa de Quatrefages, 1865b—Themiste hennahi. Sipunculus rubens Costa, i860—same. Sipunculus rufo-fimbriatus Blanchard, 1849—same. Sipunculus saccatus Linnaeus, 1767—same. Sipunculus vermiculus de Quatrefages, 1865b—Phascolosoma perlucens. Sipunculus violaceus de Quatrefages, 1865b—Siphonosoma vastum. Phascolosoma ambiguum (Brandt, 1835)—same. Phascolosoma carneum Leuckart and Riippell, 1828—P. scolops. Phascolosoma cochlearium (Valenciennes, 1854)—Aspidosiphon muelleri. Phascolosoma constellatum de Quatrefages, 1865b—same. Phascolosoma exasperatum Simpson, 1865—same. Phascolosoma fasciolatum (Brandt, 1835)—same. Phascolosoma guttatum (Quatrefages, 1865b)—P. scolops. Phascolosoma johnstoni (Forbes, 1841)—same. Phascolosoma leachii (de Blainville, 1827)—same.

386

Appendix 2

Phascolosoma longicolle Leuckart and Riippell, 1828—Golfingia vulgaris. Phascolosoma loricatum (de Quatrefages, 1865b)—same. Phascolosoma nordfolcense (Brandt, 1835)—same. Phascolosoma orbiniense de Quatrefages, 1865b—Themiste alutacea. Phascolosoma placostegi Baird, 1868—nomen dubium. Phascolosoma plicatum (de Quatrefages, 1865b)—P. nigrescens. Phascolosoma pourtalesi (Pourtales, 1851)—same. Phascolosoma pygmaeum (Quatrefages, 1865b)—same. Phascolosoma semicinctum Stimpson, 1855—same. Themiste ramosa (de Quatrefages, 1865b)—T. hennahi. Themiste lutulenta (Hutton, 1879)—same. Aspidosiphon coyi de Quatrefages, 1865b—now a valid senior synonym including A. truncatus. Aspidosiphon eremitus Diesing, 1859—A. muelleri. Aspidosiphon laevis de Quatrefages, 1865b—now a valid senior synonym for A. cuimingii, A. klunzingeri, and others. Aspidosiphon rhyssapsis Diesing, 1859—same.

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