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 (<2o), and probably function in chemoreception. Terminal organ A retractable bulb present at the posterior tip of the trunk in several larval sipunculans as well as in several adult Sipunculus species. It is under nervous control and has sensory cells and adhesive mucus-producing cells. This organ likely helps larvae select and attach to appropriate sediment at the time of settlement. Trunk (Body) The larger part of the worm, into which the introvert retracts. Ventral nerve cord An unpaired, unsegmented, midventral tract that goes from the ventral side of the circumesophageal connectives, along the inner surface of the body wall, to the posterior end of the trunk. Irregularly spaced lateral nerves are present along most of its length. Wing muscle A wing-shaped sheet of muscular connective tissue that anchors the terminal rectum to the body wall.
Part I
I
Systematics
Higher Taxa and User's Guide
This book is designed to be accessible to both nonspecialists and those more familiar with sipunculans. In an attempt to reduce redundancy while retaining clarity, I describe the higher taxa and their shared characters first, then provide keys to increasingly smaller subsets along with comments on the morphological characters relevant to that subset of taxa and their diagnoses. This design makes it unnecessary to repeat attributes of the genus, family, etc., for each species. Users should first familiarize themselves with the attributes of the family before moving on to the genus, and of the genus before going to the species level. Without prior knowledge of the class, order, family, and genus characters, the species description is not enough to make an identification.
Morphological Characters of Higher Taxa
Tentacles. As a general rule, the number of tentacles increases with the size and age of the individual. Also, within the same genus large species have more tentacles than small ones. Sipunculan tentacular crowns exhibit two basic patterns. In the class Sipunculidea the tentacles are arranged peripherally around the oral disk, encircling the central mouth. This circle may be inflected dorsally to form an arc that encloses the nuchal organ. A variety of tentacle arrangements occur within this class (Fig. 2B-E). The genus Thysanocardia exhibits the most complex crown. Adults often possess festoons consisting of several hundred peripheral tentacles, along with a nuchal array. Large Golfingia margaritacea have 100 or more tentacles, but most other Sipunculidea have fewer than 50 (e.g., Golfingia elongata with 20-34, or Nephasoma rimicola with 12-20; see Fig. 2). In some species only the primary tentacles are present, as in Onchnesoma squamatum with 8 and Nephasoma minutum with just 2.
Higher Taxa and User's Guide
i8
A
B
C
D
E
Figure 2. Sipunculan tentacles. A. Representative of the class Phascolosomatidea with dorsal crescent of nuchal, but no peripheral, tentacles. B-E. Peripheral tentacles of representatives of the class Sipunculidea (B-D illustrate the increasing complexity of the basic pattern within these genera, which is sometimes correlated with size). B. Nephasoma minutum. C. N. rimicola. D. Golfingia margaritacea. E. Connected flattened tentacles of Sipunculus, one variation in this class. See the genera Thysanocardia (Fig. 25) and Themiste (Fig. 37) for other variations. (From Gibbs and Cutler, 1987. © The Natural History Museum, London.)
Sometimes the peripheral tentacles are flattened and fused to form a continuous veil-like structure, as in Sipunculus (Fig. 2E). The crown of Themiste, with branching tentacles arising from four to eight stems, is another modification. The secondary tentacles, which are outgrowths of the oral disk, develop between the primary pairs resulting in an erect dendritic structure. The second general pattern is seen in the class Phascolosomatidea, wherein the tentacles are limited to a dorsal arc enclosing the nuchal organ and no peripheral tentacles are present (Fig. 2A). A prominent ridge, the cephalic collar, may be present around the margin of the oral disk. The six genera in this class have similar tentacular arrangements (i.e., a single arc of up to 30 short tentacles enclosing the nuchal organ). Two exceptions are Apionsoma trichocephalus, with no tentacles, and Antillesoma antillarum, which can have more than 40 well-developed tentacles. Hooks. A second character separating the Sipunculidea and Phascolosomatidea is the arrangement and structure of the hooks on the distal part of the introvert. In the former group, the hooks are variable when present but generally simple, arrayed in an unordered, dispersed fashion, and not sharply curved. In the latter class, the hooks usually have an internal
Morphological Characters
19
architecture and a markedly recurved shape, and they are closely packed in rings encircling the anterior introvert. Exceptions to both generalizations do exist, and some species have no hooks at all. In addition to arrangement and presence or absence, hook size and shape are important attributes in some genera. Anal Shield. All members of the Aspidosiphonidae have an anal shield, an aggregation of papillae that produces hardened protein or calcareous material around the anterior end of the trunk to form an operculum-like unit used to plug the open end of a burrow (it is weakly developed in a few Aspidosiphon species). Body Wall Musculature. The longitudinal and circular body wall musculature may form a continuous layer or may be divided into numerous bands or bundles either clearly separate or forming an anastomosing network. Nephridia. It is sometimes necessary to determine whether there are one or two saclike ventrolateral nephridia at the anterior end of the trunk (Fig. 1). Some Troublesome Attributes The following characters are sometimes, but not always, helpful in the identification process. Anyone working with sipunculans should be aware of the pitfalls of using them. Introvert Length. There are three potential problems with this measurement: (1) The relative length of the introvert and trunk changes with age, the introvert being a larger part of the whole in younger animals and decreasing in relative size owing to allometric growth. (2) Sipunculans, and especially the introvert, are extremely elastic in form. When the introvert is measured in the withdrawn condition, the value obtained will always be shorter than a measurement obtained from the same worm with a fully extended introvert. (3) Authors have not been consistent with regard to determining where the introvert begins. In this book the introvert is defined as beginning just anterior to the nephridiopores (or anus in the few taxa where that is the anterior orifice). Papillae. Several factors can affect papillae morphology: age (older worms have larger papillae), microhabitat (a close-fitting, hard dwelling stimulates larger papillae), and postmortem chemical history of the worm (bleaching of pigment). Nevertheless, papillae size and shape are useful diagnostic attributes in a few taxa.
Table 1. Usefulness of morphological characters for species identification Genus" Character Introvert hooks Size Shape Presence/absence Number rings Clear streak Basal elaboration Retractor origins Papillae Shape Size Platelets Trunk size, shape Tentacles Number Pigment Branching LMBs CVV morphology Introvert length Nephridia morphology Anal shield Gut coil Anus location Caudal appendage F3 origin, insertion Pigment on introvert Nephridia/anus location Spindle muscle Bifurcation Pigmented collar Nuchal organ shape Rectal caecum Attachment papillae Caudal shield Brain morphology Introvert-trunk angle Fusiform bodies Protractors
1
2
3
4
5
6
7
8
9
10
11
12
13
Total
2 3 3
2 3
1 1 1
-
3 2 1 1
-
-
2 2 3
-
3 2 1 1
2 2 2
3 2 1 1
-
-
-
-
1 2
-
-
1 2
-
-
-
-
2
-
2
3
1
1
-
-
15 15 14 5 3 3 14
-
-
3 3 2
2 3
-
1 1
1 1
3 3
-
-
-
1
2
2
2
2
1
1
-
1 1
-
-
3 3
-
-
-
-
-
-
-
1
-
-
2
3
2
3
-
-
-
-
2 3
2
-
-
-
-
-
-
-
2
2
-
-
3
3 1
-
1
-
2
2 3 1
-
-
2
3
-
-
-
2
-
2
3
2
1
-
2
-
2
-
1
-
-
2
2 1
3
-
-
-
-
-
-
-
2
-
2
-
-
-
-
-
2
-
1
—
3
-
— 3 -
3
-
-
2
2
-
-
1 1 1
1
-
-
-
-
2
-
-
2
-
-
-
-
-
-
-
-
-
-
- — -
-
2
-
1
1
-
2 1 1
16 15 2 11 11 4 3 11 7 7 7 6 5 4 4 3 3 3 3 2 2 2 2 2 2 2 1 1 1
Note: Characters arranged by total value of usefulness at subgenus or species level. 3 = broadly useful; 2 = some value, at least at subgeneric level; 1 = little import, only a few species; — = of no value in this genus. a 1 = Aspidosiphon, 2 = Lithacrosiphon, 3 = Phascolosoma, 4 = Apionsoma, 5 = Themiste, 6 = Thysanocardia, 7 = Golfingia, 8 = Nephasoma, 9 = Phascolion, 10 = Onchnesoma, 11 = Siphonosoma, 12 = Sipunculus, 13 = Xenosiphon. Genera with only one species not included (i.e., Siphonomecus, Phascolopsis, Antillesoma, Cloeosiphon).
Key to Classes and Families
21
Intestinal Coiling. The number of gut coils usually increases with age and is not species-specific. Usually there are 20-30 coils, but large worms may have as many as 100. Intestinal Fixing Muscles. According to published accounts, the number of fine, threadlike muscles attaching the gut coil to the body wall varies from zero to four or more. Although intestinal fixing muscles have been called a species-specific character, these very fragile structures can be easily broken or overlooked, and not every author mentions them. The number of muscles may vary within a single population (Gibbs, 1973; E. Cutler and Cutler, 1987a). Rectal Caecum. This structure is difficult to see in small individuals and is not always present. Some authors do not discuss its presence, but this should not be interpreted as meaning that it is absent. Table 1 lists the morphological characters used to identify sipunculans and indicates their usefulness for identifying species within multispecies genera. After keying a worm to genus, look down the appropriate column to learn which characters are important for keying animals to species. Key to Classes and Families 1. Tentacles in arc encircling dorsal nuchal organ; peripheral tentacles absent; hooks (when present) complex, in distinct rings Class Phascolosomatidea, 2 - Tentacles arranged peripherally encircling central mouth; may be carried on stemlike outgrowths of oral disk or reduced to single dorsal pair; hooks (when present) simple, usually scattered Class Sipunculidea, 3 2. Anal shield present
Family Aspidosiphonidae
- Anal shield absent
Family Phascolosomatidae
3. Longitudinal muscles of body wall gathered into separate or anastomosing bands Family Sipunculidae - Longitudinal muscle of body wall in uniform continuous layer
4
4. Branched tentacles carried on four to eight stemlike outgrowths of oral disk Family Themistidae - Unbranched tentacles not carried on stemlike outgrowths 5. A single nephridium present - Two nephridia present
5
Family Phascolionidae Family Golfingiidae
Table 2. Easily determined trunk attributes, habitat, and depth that suggest genera Genus" Character Trunk length of adult <10mm 10-40 mm >40mm Trunk shape Elongate/vermiform Spindle/tapered Filiform Spheroid Twisted Longitudinal muscle bands Anal shield Habitat Coral or rock Empty shell Sand or mud Depth <10m 10-200 m 200-2000 m >2000 m
1
+ -
2
3
+
4
+
+
+ + _
_ + + — _ — _ + _ + - + + +
_ + _ _ _
_ + _ _ _ - + + —
+ + +
+ _ -
+ _ +
+ _ +
+
+ + + _
+ + +
+ -
-
_
_
-
_
_
—
_ _ _ _
_ _ _
_ _
+
+ +
+ + +
+ +
_
+
_ + + + +
Note. Verify the genus using other keys and descriptions. a l = Aspidosiphon, 2 = Lithacrosiphon, 3 = Cloeosiphon, 4 = Phascolosoma, 5 = Apionsoma, 6 = Antillesoma, 7 = Themiste, 8 = Thysanocardia, 9 = Golfingia, 10 = Nephasoma, 11 = Phascolion, 12 = Onchnesoma, 13 = Phascolopsis, 14 = Siphonosoma, 15 = Siphonomecus, 16 = Sipunculus, 17 = Xenosiphon.
13
_ +
|
_
_ + _
_ ) +
+
+ + +
+
+ + -
+
_ _ _ +
_
_ _ +
+
+ _
_ _
-|_
+
_ _ _
_ _
_
_
_
_ + + +
_ _
_ + + +
_
_ +
-
_
_
_ _
+
+ -
_ +
+ _
16
_ +
_
-
+ + —
15
_ +
-
'
14
_
_
_ _
+
-
_
_
+
_
+
-
+
-
+ +
_
-
-
-
+ +
_ _ _
_
12
+ +
.
+
11
_
_ _ _
10
_
_ +
-
_
_
+ _
+ 4
_ +
+
_
+
+
+
9
+ +
+
_ + _ _ _ +
8
r _
_ + _ _ _ -
7
_
_
+ + _
6
+
_
+ _ -
_
5
_
17
_ +
+ _
+ _ _ _ + _
_ _ +
_ _ +
+ + + _
+ + _
_ _ _
Alternate Determination of Genera
23
An Alternate Way to Determine Sipunculan Genera
Table 2 provides another way to determine the genus of a sipunculan worm. It is not a precise tool (there are exceptions in almost every genus), but it should aid less-experienced biologists because the characters traditionally used in keys can be difficult to see. This alternative will help narrow the field of choices but must be used in conjunction with other keys and diagnoses.
2
The Sipunculids
Class Sipunculidea E. Cutler and Gibbs, 1985 Sipunculida E. Cutler and Gibbs, 1985:163 Sipunculidea Gibbs and Cutler, 1987:47 Sipuncula with peripheral tentacles on the oral disk, surrounding a central mouth. Introvert hooks (when present) usually irregularly distributed, unidentate, without internal compartments. Spindle muscle unattached posteriorly (except in 2 of the 11 genera, Siphonosoma and Siphonomecus). Order Sipunculiformes E. Cutler and Gibbs, 1985 Muscle layers in body wall gathered into bands (separate or anastomosing). Coelomic extensions, in the form of canals or sacs, present in body wall (except in Phascolopsis). Family Sipunculidae Rafinesque, 1814 Characters are those of the order. These elongate, cylindrical animals, commonly 10-20 cm long, inhabit unconsolidated sandy or sandy mud habitats. This family name has historically been attributed to Baird (1868); however, J. Saiz pointed out (pers. comm.) that Rafinesque was the first to designate the family Sipuncula for the genus Syrinx (see Sipunculus nudus) and thus deserves the credit. Familial Traits Body Wall. In three of the five genera the longitudinal muscle bands (LMBs) anastomose. The circular muscle bands (CMBs) are much more
Family Sipunculidae
25
variable, and the space between the individual bands is much smaller. In some species these spaces appear as fractures or splits in a semicontinuous layer, not as distinct bands. The opening between each pair of overlapping longitudinal and circular bands forms a functional pore allowing the coelomic fluid to be in direct contact with the skin to facilitate gas exchange. This pore leads into a closed space (sac) or into longitudinal canals extending along most of the length of the trunk. The following summary of this system in the Sipunculidae genera is from E. Cutler, 1982 and 1986. Phascolopsis (Fig. 3) has 26-40 LMBs, which are distinct but anastomose often. The circular muscle layer, however, is continuous so that no epidermal coelomic extensions exist. Siphonosoma (Fig. 3) has 18-33 LMBs, which anastomose occasionally. The circular layer is split or fractured into frequently anastomosing, ill-defined bands (with much variation among species). The pores thus created through the muscle layers open into small, irregular epidermal sacs, which are generally flattened spheres with irregular margins and diameter less than the width of one CMB. Siphonomecus (Fig. 3) has 16-23 anastomosing LMBs. The circular layer is divided into bands that are generally discrete, but splitting and fusion do occur. Short oblique muscle strands lie between the two layers. The trunk surface appears annulated. The internal pores open into a unique system consisting of a vestibule from which arise three or four short, small, parallel, longitudinal minicanals. Each canal system extends laterally from the center of one LMB to the center of its neighbor, and similarly from center to center of each pair of CMBs. Sipunculus (Fig. 3) has 20-50 separate and well-defined LMBs. The CMBs are also distinct and separate. Oblique muscle strands are present between the two layers. The pores open into longitudinal canals, one canal between each pair of LMBs. Each canal has numerous pores along its length, opening into it between each pair of CMBs. One species (S. longipapillosus) has slender, digitate papillae as extensions of these canals in the mid-trunk region. In the posterior end of the trunk (the glans region) the circular layer is continuous and the LMBs may change. In some species the LMBs become a continuous layer; in others each band subdivides into two; and in a few species the LMBs continue as single units (E. Cutler and Cutler, 1985b). Xenosiphon (Fig. 3) muscle layers are like those in Sipunculus, with 2937 LMBs and no anastomoses. The canal system consists of short, diagonal canals extending from corner to corner of a skin rectangle. Off this
Key to Sipunculidae Genera
27
small canal, in the mid-trunk region, there may be one to four elongate digitate papillae, analogous to the gill-like array on S. longipapillosus. Spindle Muscle. This threadlike muscle extends through the center of the gut coil from anterior to posterior end. It may be attached to the posterior end of the trunk, or its posterior termination may be within the gut coil. Introvert Hooks or Papillae. These are either arrayed in rings around the distal part of the introvert or arranged in a random, scattered manner. Phascolopsis had been thought to lack hooks, but E. Cutler (1986) observed them in small individuals (1-4 cm). The hooks apparently wear down or fall off and are lost in the early months of life. This observation reaffirms Gerould's remarks (1907:123) that worms whose total expanded length is 3-6 cm are "provided with a zone of hooks . . . arranged in a band which consists of six or eight irregular rows, are recurved slightly, and of a light brown color. Their arrangement suggests at once the circlet of hooks in Ph. [sic] vulgare." Small papillae in distinct rings persist after these deciduous hooks have been lost. Introvert Retractor Muscles. Two pairs of these short muscles extend from the head to the anterior trunk wall in all but Siphonomecus, which has only a single pair. Postesophageal Loop. In most genera the esophagus goes directly into the tightly wound gut coil as a straight tube, but Sipunculus species exhibit a long, loose loop before entering the coil. Key to the Sipunculidae Genera 1. Body wall circular muscle layer continuous - Body wall circular muscle layer gathered into bands
Phascolopsis 2
Figure 3. Body wall of the five Sipunculidae genera with differing degrees of separation of muscle layers into anastomosing and distinct bands. C, circular muscle. E, epidermis. L, longitudinal muscle. LC, longitudinal canal. M, minicanal. Oblique muscles appear on Sipunculus, between the two main layers. (From E. Cutler, 1986, courtesy of Bulletin of Marine Science.)
28
The Sipunculids
2. Body wall circular and longitudinal muscle bands anastomosing, spindle muscle attached to posterior trunk 3 - Body wall circular and longitudinal bands not anastomosing, spindle muscle not attached to posterior trunk 4 3. Four introvert retractor muscles
Siphonosoma
- Two introvert retractor muscles
Siphonomecus
4. Gut with postesophageal loop; coelom extends into body wall as parallel longitudinal canals running throughout most of trunk Sipunculus - Gut without postesophageal loop; coelom extends into body wall as short diagonal canals running across the width of one CMB Xenosiphon
Genus Sipunculus Linnaeus, 1766 Syrinx Bohadsch, 1761:93-97. Sipunculus Linnaeus, I766:i078.-de Quatrefages, i865b:6i3.-Selenka et al., i883:88.-Stephen and Edmonds, I972:2i.-E. Cutler and Cutler, 19850:232. DIAGNOSIS. Species usually large, trunk longer than 50 mm in adults. Introvert much shorter than trunk (5-30%), without hooks, covered with irregularly arranged triangular papillae. Trunk cylindrical and smooth or as if covered by swollen rectangular minipillows. Body wall contains coelomic extensions in the form of parallel longitudinal canals that lie between muscle bands and extend over most of the trunk. Longitudinal and circular muscle layers gathered into distinct bands. Oral disk carries tentacles arranged around the mouth, sometimes with an intertentacular membrane. Four introvert retractor muscles. Two contractile vessels, without villi. Gut with postesophageal loop; coil attached to body wall along most of its length by many connective tissue strands. Rectal caecum present. Spindle muscle not attached to the body wall posteriorly. Two nephridia (see Figs. 3 and 4). TYPE SPECIES. Sipunculus nudus Linnaeus, 1766. Morphological Characters of Sipunculus and Xenosiphon Longitudinal Muscle Bands. The number of LMBs is easily determined and is a useful character in this genus. The number of bands characteristic
Genus Sipunculus
A
29
B
D
Figure 4. Sipunculus. A. S. (Sipunculus) nudus. B. S. (Austrosiphon) indicus. C. Internal details of generalized S. (Sipunculus) with nephridiopores and spindle muscle attachment anterior to the anus. D. S. (Austrosiphon) with nephridiopores posterior to anus and spindle muscle ending on rectum. Both subgenera have the postesophageal loop (PEL). E. Detail of distal introvert showing large introvert papillae. Abbreviations as in Figure 1.
of any given species commonly has a within-species variation of ±5-8 (up to 14 in S. polymyotus). Observations made on Sipunculus from Brazil show the value of working with a large sample size (Ditadi, I982:fig. 12). No correlation between trunk size and number of LMBs is apparent within species; even larvae exhibit the adult number (Hatschek, 1883; Fisher, 1947; Akesson, 1961b).
30
The Sipunculids
Nephridiopore Location. The position of the nephridiopores relative to the anus, along the anterior-posterior axis, is of limited interest. In Xenosiphon branchiatus, S. mundanus, and S. indicus the nephridiopore is posterior to the anus by 1-4% of the trunk length, but in all other species it opens a short distance anterior to the anus, commonly 5-10% of the trunk length, occasionally less than 1% or as much as 15%. Nephridia Attachment and Length. Most Sipunculus species have free nephridia. The nephridia of S. indicus and X. branchiatus are attached by a mesentery to the body wall for 80-90% of their length. Two species (5. marcusi and S. nudus) have partially attached (15-50%) nephridia. In general, the nephridia length is 10-25% of the trunk length in species in these genera. The one exception is in S. mundanus, in which the nephridia length is less than 3% of the trunk length. Retractor Origins. The two pairs of introvert retractor muscles have their origins on the body wall at about the same anterior-posterior level, 20-30% of the distance toward the posterior end of the trunk. The particular LMBs over which the origins spread is of general interest. The ventral retractors begin close to the ventral nerve cord, commonly on the second LMB. The ventral edge of the dorsal retractors may be on LMBs 7-16, depending on the total number of LMBs in the worm (positive correlation for 63 individuals in the genus Sipunculus, shown by E. Cutler and Cutler, I985b:fig. 1). This information can be helpful as part of the overall picture, but there is some overlap among species with a similar number of LMBs, and retractor origin by itself is not a determinative feature. Brain and Brain Processes. In the median plane of the posterior and ventral surfaces there is a deep furrow that separates the brain into two lobes. This character is not always evident, and it can be difficult to discern if the specimen is not well preserved. In Sipunculus norvegicus the lobes are present but flattened, and the separation is not obvious (Akesson, 1958). The brain has anteriodorsal processes that form tufts or a fringe of digitate or threadlike extensions into the coelom; these probably have a neurosecretory function (Akesson, 1958). Sipunculus norvegicus and S. longipapillosus do not have digitate processes; those in S. robustus are distinctly elongate, thin, and threadlike; and in S. polymyotus they form elaborate arrays of leaflike and threadlike processes. The remainder of the
Genus Sipunculus
A
31
B
Figure 5. Sipunculus cerebral ganglia and digitate processes. A. S. nudus with anterior spongelike tuft (from Ditadi, 1982, courtesy of the Academia Brasileira de Ciencias). B. S. robustus with lateral stringlike processes.
species in these genera have some form of digitate extensions arranged in a frill or tuft on the brain (Fig. 5). The extensions vary within populations, and the differences between species are ill-defined. Glans Regions. The posterior tip of the trunk in a few Sipunculus species often exhibits an acornlike terminal "glans" region, sometimes set off from the rest of the trunk by an annular fold or ridge of skin. It is too variable in form to be of systematic value. The circular muscle layer in this region is continuous (i.e., the CMBs are not developed). The condition of the LMBs in the glans region was proposed as a new character by E. Cutler and Cutler (1985b). In most species the glans LMBs are poorly developed, becoming flatter and closer together. In some species the bands persist, but in others the LMB layer appears to be continuous. In three species (S. nudus, S. longipapillosus, and 5. polymyotus) there are twice as many LMBs, as if each band from the trunk has split in two (Fig. 6). Alimentary Canal. The spindle muscle begins on the dorsal body wall just anterior to the anus in Sipunculus (Sipunculus), but in Sipunculus (Austrosiphon) it begins on the distal portion of the rectum (Fig. 4C-D). This slender, threadlike muscle strand goes through the gut coil but does not extend beyond it. The gut coil is anchored to the body wall by many thin strands of connective tissue. In addition, the loop and rectum may be held by one to three fixing muscles.
32
The Sipunculids
Figure 6. Posterior glans region of the trunk of two Sipunculus species. A. The longitudinal muscle bands (LMB) continue to the tip as single, discrete units. B. Each LMB divides into two units. Key to Sipunculus Subgenera and Species Note. In the text the species are arranged alphabetically within subgenera. Descriptions of generic and subgeneric attributes are not repeated for each species. i. Nephridiopore posterior to anus; spindle muscle originates on rectum (Fig. 4D) S. (Austrosiphon), 2 - Nephridiopore anterior to anus; spindle muscle originates on body wall anterior to anus (Fig. 4C) S. (Sipunculus), 3 2
- 37-43 LMBs; no protractor muscles
- 27-31 LMBs; two dorsal protractor muscles
S. indicus 5. mundanus
Genus Sipunculus
33
3. Elongate, filiform papillae on mid-trunk, 24-30 LMBs.... S. longipapillosus - Trunk without elongate papillae
4
4. 35 or more LMBs
5
- 34 or less LMBs
7
5. 42 or more LMBs
5. polymyotus
- 41 or less LMBs
6
6. Retractor muscle origins united by continuous muscle sheet (Fig. 7A) S. marcusi - Retractor muscle origins separate
S. phalloid.es
(S. p. inclusus may have as few as 32 LMBs at some points on trunk) 7. 20-24 LMBs; brain flattened, length greater than width, without distinct processes S. norvegicus - 24-34 LMBs; brain rounded, width greater than length 8. Brain single lobed, no processes; at depth >20OO m
8 S. lomonossovi
- Brain bilobed; processes present; at depth <500 m
9
9. Nephridia unattached; brain processes lateral, long and stringlike (Fig. 5B) 5. robustus - Nephridia partially attached; brain processes dorsal and digitate or short, spongelike mass (Fig. 5A) S. nudus
Subgenus Sipunculus (Sipunculus) E. Cutler and Cutler, 1985 DIAGNOSIS. Nephridia anterior to anus. Spindle muscle originates on body wall anterior to anus (Fig. 4C). TYPE SPECIES. Sipunculus nudus Linnaeus, 1766.
Sipunculus lomonossovi Murina, 1968 Sipunculus lomonossovi Murina, 1968^198; 1978:121.-E. Cutler and Cutler, 1985^235-236. DESCRIPTION. The 28-34 LMBs are flat and thin, and the body wall is transparent, up to n o mm long. The brain is rounded, single lobed, and without elongate processes. The nephridia are partially attached, short, and have an irregular rough surface. The glans region is indistinctly set off; the
Figure 7. Retractor origins. A. Sipunculus marcusi with connecting muscular membrane (after Ditadi, 1976, courtesy of the editors of Boletim de Zoologia). B-D. S. nudus (after E. Cutler and Cutler, 1985b, courtesy of the Linnean Society). B. Normal ventral pair. C. Ventral pair with subdivided origins. D. Specimen with connective tissue linking origins together.
Genus Sipunculus
35
LMBs continue as distinct undivided bundles into this region, but the circular muscle layer is continuous. Differs from 5. nudus (similar LMB number) in habitat and shape of brain, and from 5. norvegicus (preferred depths overlap) in brain shape and number of LMBs. DISTRIBUTION. Found in cold, deep water (2500-4300 m) from the far South Pacific, the eastern Atlantic (20-34 0 N), and off Brazil.
Sipunculus longipapillosus Murina, 1968 Sipunculus longipapillosus Murina, I968b:i724-I725.-E. Cutler and Cutler, I979a:945; 1985^239. DESCRIPTION. The 24-30 (usually 27-29) LMBs double in number in the posterior end. The nephridia are unattached, and the brain is without digitate processes. Elongate papillae in the middle third of the body extend from the longitudinal epidermal canals. This species is easily distinguished from other members of the genus but is easily confused with Xenosiphon branchiatus because both have elongate papillae in the mid-trunk giving a fuzzy appearance. The absence of protractor muscles, the unattached nephridia posterior to the anus, and the spindle muscle originating from the body wall anterior to the anus in S. longipapillosus are clear differences. The diagnostic papillae are arranged in longitudinal rows along the coelomic canals between the LMBs; this differs from the diagonal pattern seen in X. branchiatus. DISTRIBUTION. The Red Sea and northwestern Indian Ocean, at 60-370 m.
Sipunculus marcusi Ditadi, 1976 Sipunculus marcusi Ditadi, 1976:81-84; i982:786-788.-E. Cutler and Cutler, I985b:235. DESCRIPTION. Worms of this species have 35-36 LMBs, and retractor muscle origins are continuous with each other around the periphery of the body cavity (Fig. 7A). The nephridia are attached to the body wall for up to 25% of their length. This Brazilian species is based on two specimens (trunk lengths 250 and 325 mm). It is possible that they are an aberrant subset of the larger sympatric 5. phalloides population. Aside from the peculiar united retractor origins and the partially attached nephridia, there are no clear distin-
36
The Sipunculids
guishing characteristics. Interconnected retractor origins occur in some populations of other Sipunculus species. DISTRIBUTION. Found intertidally near Sao Paulo, Brazil. Sipunculus norvegicus Danielssen, 1869 Sipunculus norvegicus Danielssen, 1869a: 541.-Stephen and Edmonds, 1972:29-32.-13. Cutler, I973:i28-I30.-E. Cutler and Cutler, 1980b: 449-451; i985b:239-240.-Saiz and Villafranca, 1990:1146.-Haldar, i99i:io-i2.-Saiz, 1993:44-45. Sipunculus priapuloides Koren and Danielssen, 1877:126-128. Sipunculus nitidus Sluiter, i90o:i4-i6.-Stephen and Edmonds, 1972:32. Sipunculus aequabilis Sluiter, 1902:7.-Stephen and Edmonds, 1972:2526.-E. Cutler and Cutler, 19793:944. Sipunculus infrons Sluiter, i902:io.-Stephen and Edmonds, 1972:28. Sipunculus priapuloides var. americana Gerould, 1913:429-432.-Stephen and Edmonds, 1972:31-32. DESCRIPTION. This species has 20-24 LMBs (commonly 21-22) and short, free nephridia. The ventral retractors originate in LMBs 3 and 4 (rarely just on 3 or on 2 and 3), and the dorsal retractors from LMBs 8 and 9 (rarely just on 8 or 9). The brain is elongated and flattened, and the lobes are not prominent. The brain processes are not developed. The glans region usually is marked off from the trunk by a ridge, which may or may not be interrupted ventrally by a furrow. The tentacular membrane is divided into 8-12 lappets or lobes (see Theel, 1905, for a detailed discussion of these last two characters). This small species (usually
Genus Sipunculus
37
1986^74-78; i993:45-47.-Ditadi, l982:792-796.-Haldar, 1991:1215Syrinx tesselatus Rafinesque, 1814:32. Sipunculus tesselatus Keferstein, i865b:420.-Shipley, 1893:327. Sipunculus nudus var. tesselatus Cuenot, 1922:15-16. Sipunculus nudus tesselatus Murina, 19773:168-169. Sipunculus balanophorus Delle Chiaje, 1823:1-24. Syrinx nudus Forbes, 1841:245-246. Sipunculus gigas de Quatrefages, i865b:6i4-6i5.-Stephen and Edmonds, I972:339.-Saiz, 19843:197. Sipunculus eximioclathratus Baird, 1868:81-82.-R.ice and Stephen, 1970:58Sipunculus titubans Selenka and Biilow, in Selenka et al., 1883:100-101.Stephen and Edmonds, i972:37-38.-E. Cutler and Cutler, 19793:946. Sipunculus titubans var. diptychus W. Fischer, 1895:7; 19143:61-62.Stephen and Edmonds, 1972:38. Sipunculus delphinus Murina, 1967^1336-1337. DESCRIPTION. Commonly 5-15 cm long, with 24-34 LMBs (usually 28-32). The nephridia are 10-40% attached (Fig. 4A). Digitate processes on the brain form a dorsal tuft and are divided to varying degrees, sometimes appearing spongelike or solid. The LMBs usually split in the glans region. E. Cutler and Cutler (1985b) observed that the origins of the four retractor muscles in a population from Florida are connected by a sheet of muscle (Fig. 7D). In some worms this is thin, mesentery-like, and seems to be separated from the origins; in others it is thicker and appears as a continuation or fanning out of the retractor muscles themselves, much as Ditadi described for 5. marcusi. In a few individuals there is a subdivision of each retractor origin into four or five fascicles connected to separate LMBs (Fig. 7C). NOTE. This most common member of the genus has been studied in detail by anatomists, physiologists, biochemists, and ecologists. Although common and well known, it is not a "typical" sipunculan. It is probably a highly derived species with an array of unique features, including several aspects of its embryology, the inability to regenerate the distal end of the introvert, a unique bulb on the posterior end of the ventral nerve cord, and the presence of free urn cell complexes. These unusual characters are discussed in more detail on pages 233-235. DISTRIBUTION. This cosmopolitan species is found in temperate, sub-
38
The Sipunculids
tropical, and tropical waters in all oceans. Most are intertidal to 30 m, but a few records are from 100-900 m.
Sipunculus phalloides phalloides (Pallas, 1774) Lumbricus phalloides Pallas, 1774:12-15. Sipunculus phalloides.—Stephen and Edmonds, I972:34~35.-Ditadi, 1982:796-799.-!}. Cutler and Cutler, 19870:71. Sipunculus phalloides phalloides E. Cutler and Cutler, 19850:234. Sipunculus multisulcatus W. Fischer, 1913:93-94.^6 Jorge et al., 1970: 163-164.-Stephen and Edmonds, 1972:28-29. Sipunculus galapagensis Fisher, i947:358-36o.-Stephen and Edmonds, 1972:26. DESCRIPTION. This large worm has 35-41 LMBs. The nephridiopores open somewhere between LMBs 4 and 8; the unattached nephridia are less than 25% of the trunk length and open 5-10% of the trunk length anterior to the anus. The ventral retractors originate in LMB 1 or 2 and extend over two to six bands; the dorsals start on LMBs 12-16 and spread over two to six bands. The LMBs do not subdivide in the glans region. The spindle muscle is weakly developed. DISTRIBUTION. An intertidal and shallow-water species in the Caribbean from the West Indies, Barbados, and Brazil; in the eastern Pacific, from Costa Rica and the Galapagos Islands. One specimen was collected 15 m off the Ivory Coast in the eastern Atlantic.
Sipunculus phalloides inclusus (Sluiter, 1902) Sipunculus inclusus Sluiter, I902:i36.-Stephen and Edmonds, 1972:26.E. Cutler et al., 1984:255. Sipunculus phalloides inclusus E. Cutler and Cutler, 1985^234-235. DESCRIPTION. The sole morphological character that sets this smaller subspecies (largest record is 90 mm) apart from the nominate form is the amount of variation in the number of LMBs within each worm; that is, there is more fusion (or splitting) of LMBs from anterior to posterior. The number of LMBs is also at or below the low end of the range of the nominate form (32-39 vs. 35-41). There is a geographical gap: the Pacific Ocean separates the two subspecies. DISTRIBUTION. Indonesia and southern Japan, at 1-370 m.
Genus Sipunculus
39
Sipunculus polymyotus Fisher, 1947 Sipunculus polymyotus Fisher, I947:354~358.-Stephen and Edmonds, 1972:35.-E. Cutler and Cutler, 19855:232-233. Sipunculus natans Fisher, i954b:238-240.-Stephen and Edmonds, 1972: 29.-Ditadi, 1982:788-792. DESCRIPTION. Large (up to 270 mm), with 42-55 LMBs and introvert commonly 25-30% of the total length. The tentacular membrane has two large ventral lobes and two smaller dorsal lobes (one of which may bifurcate, giving the appearance of three) with the margin greatly subdivided. The nephridia are dark and have irregular knobby surfaces. Ventral retractors span six or seven LMBs beginning on LMB 1 or 2, and the dorsal retractors span five to six LMBs beginning between LMB 13 and LMB 19 (usually 15 or 16). Most LMBs split and double in the posterior end (they do not in the Panamanian material). Digitate processes of the brain are large, conspicuous, leaflike flaps and long strings. DISTRIBUTION. From intertidal waters near Sao Paulo, Brazil; 3-30 m off the southeastern United States (South Carolina, around Florida, to Panama City, Fla., on the Gulf of Mexico); both sides of Costa Rica; west coast of Panama; off Baja California; and one peculiar record from the Tasman Sea. Sipunculus robustus Keferstein, 1865 Sipunculus robustus Keferstein, 1865^421.-Stephen and Edmonds, 1972: 36-37.-E. Cutler, i977a:i37.-Edmonds, i98o:9~io.-E. Cutler and Cutler, 1985^237-238.-Haldar, 1991:15-17. Sipunculus angasii Baird, i868:76.-Edmonds, i955:83-86.-Stephen and Edmonds, 1972:36-37. Sipunculus gravieri Herubel, i904a:478-479.-Stephen and Edmonds, 1972:39-41. DESCRIPTION. This species (variously defined in past years) has 26-30 LMBs (usually 28-29), and the nephridia are free. The digitate processes of the brain are lateral, long, and stringy. It is probable that in the past this name has been applied to S. nudus populations, and vice versa. The LMB number is within the 5. nudus range, but S. robustus is a distinct species. The two species are very closely related (Stephen and Edmonds, 1972:37). DISTRIBUTION. Warm waters in the Indo-West Pacific Ocean at shallow depths, also reported from the Red Sea and the Caribbean.
The Sipunculids
40
Subgenus Sipunculus (Austrosiphon) (Fisher, 1954) Xenosiphon (Austrosiphon) Fisher, 19543:314. Sipunculus (Austrosiphon) Gibbs and Cutler, 1987:49. Xenosiphon (Xenopsis) Johnson, 1969:44. Sipunculus (Contraporus) E. Cutler and Cutler, 1985^241. DIAGNOSIS. Nephridia posterior to anus. Spindle muscle originates from anterior ventral surface of rectum (Fig. 4D). TYPE SPECIES. Sipunculus indicus Peters, 1850. Sipunculus (Austrosiphon) indicus Peters, 1850 Sipunculus indicus Peters, i85o:382-383.-Edmonds, 1971:137-140; i98o:9.-Stephen and Edmonds, i972:27-28.-E. Cutler and Cutler, 19798:944; 1985^241-242. Sipunculus (Austrosiphon) indicus.—Haldar, 1991:19-21. Sipunculus porrectus Selenka, 1888:221-222.-Stephen and Edmonds, 1972:35-36. Sipunculus discrepans Sluiter, 1898:445-450. Xenosiphon (Xenopsis) indicus Johnson, 1969:44-46. DESCRIPTION. A large white worm (up to 45 cm) with 37-43 LMBs that do not split in the posterior end (Fig. 4B). The nephridia are 10-20% of the trunk length, attached for 80-100% of their length, and the nephridiopores are located 2-5% of the trunk length posterior to the anus. The introvert is 5-12% of the trunk length, relatively shorter in the larger worms. The longitudinal muscle layer continues as bands into the glans region, but the circular muscle layer is continuous there. A rectal caecum is present but not easily seen. DISTRIBUTION. Tropical Indian and far western Pacific oceans, from East Africa, Madagascar, through India and several islands, to the South China Sea, Guam, Palau, Indonesia, and western Australia, in shallow, sandy habitats. Sipunculus (Austrosiphon) mundanus Selenka and Biilow, 1883 Sipunculus mundanus Selenka and Biilow, in Selenka et al., 1883:108109.-E. Cutler and Cutler, 1985^242. Xenosiphon mundanum.—Fisher, i954a:3i4.-Tarifeno and Tomicic, 1973:107-1 io.-Edmonds, 1980: 12-14. Xenosiphon mundanus.—Stephen and Edmonds, 1972:42.
Genus Xenosiphon
41
Sipunculus maoricus Benham, 1904:303-305. DESCRIPTION. Worms with 27-31 LMBs, which occasionally anastomose, and two small dorsal protractor muscles. The trunk may be up to 27 cm long, and the short introvert has many scalelike papillae. The short nephridia (less than 2% of trunk length) are unattached, and the rectum is long. The bilobed brain has an anterior tufted process. DISTRIBUTION. Reported 10 times from the South Pacific (several Australian, probably shallow water), but only one record is from the eastern side of the Pacific (Chile).
Genus Xenosiphon Fisher, 1947 Xenosiphon Fisher, 1947:360; 1954a: 311.-Stephen and Edmonds, 1972: 38.-E. Cutler and Cutler, 1985^228. DIAGNOSIS. Medium to large worms with introvert much shorter than trunk; without hooks but covered with irregularly arranged triangular papillae. Body wall contains coelomic extensions in the form of short, diagonal canals limited in length to the width of one CMB. Longitudinal and circular muscle layers are divided into distinct bands. Oral disk carries tentacles arranged around the mouth. Four introvert retractor muscles and two thin protractor muscles are present. Gut without postesophageal loop, coil attached to body wall by connective tissue strands. Spindle muscle originates on ventral wall of rectum and is not attached to body wall posteriorly. Nephridiopores posterior to anus. TYPE SPECIES. Sipunculus mundanus var. branchiatus W. Fischer, 1895. Morphological Characters of Xenosiphon See Figures 3 and 8. Most characters are as for the genus Sipunculus (see Morphological Characters of Sipunculus and Xenosiphon, above). This taxon was revised by E. Cutler and Cutler (1985b), based on the assumption that the pair of protractor muscles, possibly a neotenic retention of larval muscles, arose independently on two occasions, making this an example of parallel or convergent evolution in two closely related genera (see Chap. 9). These authors also suggested that the nature of the subcutaneous canal system and the presence of a postesophageal loop are of greater significance and should be given more weight than allocated by previous authors.
Genus Xenosiphon
43
The gill-like trunk papillae of X. branchiatus look superficially like those of S. longipapillosus. They are undoubtedly analogous; in S. longipapillosus, however, the papillae are outgrowths from the continuous, parallel, longitudinal canals that all Sipunculus species have. In X. branchiatus they come off short, diagonal minicanals (Fig. 3). The revision of Xenosiphon placed all species with synapomorphies of gut and body wall into a single genuSv The genus thus resumes its original identity, sensu Fisher (1954), uncluttered by taxa with homoplastic features. The two known species are separated by most of the Pacific Ocean. Key to Xenosiphon Species 1. Elongate digitiform papillae on mid-trunk - Without elongate papillae in mid-trunk
X. branchiatus X. absconditus
Xenosiphon absconditus Saiz, 1984 Xenosiphon absconditus Saiz, 19846:63-66. Xenosiphon branchiatus nudus E. Cutler and Cutler, 1985b: 231-232. NOTE. Saiz (1984c) described this species based on two incomplete specimens in the Paris Museum that had previously been identified as Sipunculus gravieri. The descriptions did not mention the esophagus-gut region (loop) or the nature of the coelomic canals. Subsequent communication with J. Saiz confirmed the lack of a postesophageal loop, but the nature of the canals cannot be determined. Nevertheless, it now seems appropriate to combine these names. When Saiz's 1984 article was published, E. Cutler and Cutler's 1985 paper was in press. The collection site of Saiz's worms is uncertain but may be the Red Sea. This seems unlikely, however, because that area has been well sampled in recent decades (see Stephen, 1941b, 1965; Wesenberg-Lund, 1957c; Murina, 1967a, 1968c, 1971a), and no worms matching that description have been reported. DESCRIPTION. This species is very similar to X. branchiatus except that it lacks the gill-like trunk papillae. The trunk is 110-600 mm long. The middle third of the trunk skin has short diagonal ridges overlying the noncontinuous epidermal minicanals; minicanals lack elongate papillae. Figure 8. Xenosiphon. A. X. branchiatus. B and C. Magnified views of mid-trunk papillae (scale line = 1 mm). D. Internal view showing protractor muscles (PM). Abbreviations as in Figure I.
The Sipunculids
44
There are 33-37 LMBs, and the nephridia are up to 25% of the trunk length. In traumatized worms the LMBs can undergo partial separation from the body wall so that portions of these bands lie free in the coelom. DISTRIBUTION. Red Sea?, Palau, and Burma, from intertidal and shallow waters. Xenosiphon branchiatus (Fischer, 1895) Sipunculus mundanus var. branchiatus W. Fischer, 1895:3. Xenosiphon branchiatus.—Fisher, i947:36o-363.-Stephen and Edmonds, 1972: 39-41. Xenosiphon branchiatus branchiatus.—E. Cutler and Cutler, 1985^230-231. Xenosiphon caribaeum Fisher, I954a:3i2-3I4.-Stephen and Edmonds, 1972:41-42. DESCRIPTION. Worms with 29-37 LMBs (commonly 31-34) and gilllike, digitiform papillae along the middle 30-45% of the trunk (Fig. 8AC). The nephridia are 15-20% of the trunk length and attached for 8090% of their length. The ventral retractor muscles originate from LMBs 2-4 (rarely 1-4 or 1-3), and the dorsals have their ventral edge on LMB 8 or 9 (rarely 7 or 10) and span three to five LMBs. The small, paired protractor muscles insert into a pit or depression in the dorsal retractors, not a slit (Fig. 8D). The bilobed brain has a tuft of digitate processes. Fisher's (1947, 1954a) descriptions and drawings of this species, especially the epidermal coelomic extensions, are excellent and should be referred to for details. His specimens are 200-300 mm long, but a northern Florida population is only 20-30 mm. The smaller worms have more transparent skin, and the brain is relatively larger but with less well developed processes. In the smallest worms the elongate trunk papillae cover only 15-20% of the trunk, with a single papilla per minicanal or skin rectangle rather than the three or four papillae found in larger animals. This makes X. branchiatus appear even more similar to 5. longipapillosus. DISTRIBUTION. Shallow, warm waters off Ecuador, Costa Rica, California, Panama, Puerto Rico, and Florida. Genus Siphonosoma Spengel, 1912 Siphonosoma Spengel, I9i2:264.-Stephen and Edmonds, I972:43.-E. Cutler and Cutler, 1982:748.
Genus Siphonosoma
45
Siphonosoma (Dasmosiphon) Fisher, i95ob:8o5.-Stephen and Edmonds, 1972:44. Siphonosoma (Siphonosoma) Fisher, 1950^805.-Stephen and Edmonds, 1972:58. Siphonosoma (Hesperosiphon) Fisher, i95ob:8o5.-Stephen and Edmonds, I972:53DIAGNOSIS. Introvert much shorter than trunk, with prominent conical papillae (sometimes also hooks) arranged in rings. Body wall with small, irregular, saclike coelomic extensions; circular and longitudinal muscle layers gathered into anastomosing, sometimes indistinct bands. Tentacles arranged around mouth. Four introvert retractor muscles. Contractile vessel with or without villi. Spindle muscle attached posteriorly. Two nephridia. Usually large: trunk >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 (<75 u-m)
9
9. Contractile vessel simple, without bulbous swellings G. margaritacea - Contractile vessel with bulbous swellings or vesicles that are often orange; from southern Africa G. capensis
Subgenus Golfingia (Spinata) E. Cutler and Cutler, 1987 Golfingia (Spinata) E. Cutler and Cutler, 19873:740. DIAGNOSIS. Small to medium sized, with introvert longer than trunk. Small hooks arranged in rings, with basal spinelets. Slender retractor muscles about equal in size; both pairs very close to ventral nerve cord. Spindle muscle originates in the body wall just anterior to the anus. Two bilobed nephridia. TYPE SPECIES. Golfingia pectinatoides E. Cutler and Cutler, 1979. NOTE. Members of the single species of this subgenus share a suite of similar characters (retractors, hooks, and nephridia) with the four Apionsoma species, including A. (Edmondsius) pectinata. I propose that this suite represents an ancestral condition retained in these "living fossil" representatives of Sipunculidea and Phascolosomatidea. Golfingia (Spinata) pectinatoides E. Cutler and Cutler, 1979 Golfingia pectinatoida E. Cutler and Cutler, 19793:951-954. Golfingia (Spinata) pectinatoides E. Cutler and Cutler, 19873:740. DESCRIPTION. The distinctive characters are those of the subgenus. Externally this worm resembles a soft-skinned Phascolosoma with the rough,
68
The Golfingiids
papillose trunk tapering at both ends (lacking LMBs). The trunk has large, scattered papillae, but the animal itself is soft and pliable. The bilobed nephridia and the four thin, equal-sized introvert retractors originating from about the same level are easily discerned and diagnostic internal characteristics (Fig. 16B). Obtaining a few introvert hooks to mount on a slide can be difficult (the introvert is rarely extended sufficiently, and it has a very small diameter), but the shape and the few slender basal spinelets can help confirm the identity (Fig. 17B). The gut is in an irregular loose coil, and there are no fixing muscles. DISTRIBUTION. Madagascar and French Polynesia at intertidal depths in coral sand. Three worms collected in 1977 at Benthedi station 5124 from the Mozambique Channel (unpublished record) are from unknown depths.
Subgenus Golfingia (Golfingia) Lankester, 1885 Golfingia Lankester, 18853:469-471. Golfingia (Golfingia) Fisher, 19503:549; I952:390.-Stephen and Edmonds, i972:8i.-E. Cutler and Cutler, 19873:741. DIAGNOSIS. Introvert equal to or shorter than trunk. Simple hooks scattered, if present (forming rings in G. elongata). Anterior pair of retractor muscles with origins more dorsal than posterior ventral pair. Spindle muscle originates from wall of rectum (sometimes under wing muscle). Two unilobed nephridia. TYPE SPECIES. Sipunculus vulgaris (de Blainville, 1827). Golfingia anderssoni (Th6el, 1911) Phascolosoma anderssoni Theel, i9ii:28-29.-Stephen, 19413:250. Golfingia anderssoni.—Murina, 1957^992-993; i977:222-223.-Stephen and Edmonds, i972:84-85.-E. Cutler and Cutler, 19873:749. DESCRIPTION. These worms hsve 3 csudsl 3ppend3ge 3nd distinctive large papilke covering 3n area about 65-90% of the distsnce towsrd the posterior end of the trunk. In this they 3re strikingly simil3r to Nephasoma flagriferum. The trunk is up to 35 mm long, and the tail may be up to 8 mm. No hook-bearing specimens have been recorded, but smaller worms msy hsve hooks. DISTRIBUTION. Most records are from the fsr southern lstitudes 3t depths of 75-1880 m; one record from the equatorial Atlsntic Ocesn (around 180 S) is from 4300-4600 m (equatorisl submergence?). The two
Genus Golfingia
69
northern Pacific Ocean records (28 and 440 N) from deep water (3150 and 6135 m), each of a single specimen, are difficult to reconcile with the southern records. Golfingia birsteini Murina, 1973 Golfingia birsteini Murina, 1973b.-942-943.-E. Cutler and Cutler, 1987a: 750. DESCRIPTION. An elongate, slender worm (length up to 15 times the diameter) with reduced tentacles, thus resembling a few Nephasoma species (e.g., N. capilleforme or N. cutleri), but the latter are easily differentiated by having only one pair of retractors. The papillae are variable in shape, including pear shaped, and the posterior end is often cone shaped. The hooks are large (150 |xm) and scattered. 0 DISTRIBUTION. A single record from the northwest Pacific Ocean (58 N, 149° W) at 3200 m. Golfingia capensis (Teuscher, 1874) Phascolosoma capense Teuscher, 1874:488-489.-Stephen, 1942:251. Golfingia capensis.—Wesenberg-Lund, i959a:i8i-i82.-Stephen and Edmonds, I972:87.-E. Cutler, I977a:i39.-E. Cutler and Cutler, 1987a: 750. Dendrostoma stephensoni Stephen, 1942:252-253. Themiste stephensoni.—Stephen and Cutler, 1969:1 i6.-Stephen and Edmonds, 1972: 212-213. DESCRIPTION.
A localized but common, sturdy, and potentially large, cylindrical worm (trunk up to 200 mm). The contractile vessel has bulbous swellings or vesicles (sometimes orange) along a portion of its length, but these are not true villi (see E. Cutler and Cutler, 1982:750). This species resembles the shallow-water Australian and Japanese populations of G. margaritacea, which have similar bulbous contractile vessels. A few small individuals in both populations also bear small, deciduous hooks. DISTRIBUTION. South Africa (to Mombasa on the east coast), and lie St. Paul (400 S, 8o° E). Most records are from 1-100 m (deepest is 430 m). Golfingia elongata (Keferstein, 1862) Phascolosoma elongatum Keferstein, 1862^39. Golfingia elongata.— Akesson, 19613:51 i-530.-Stephen and Edmonds, i972:90-9i.-Gibbs,
70
The Golfingiids
1977b:io.-Saiz, 198615:18-20; i993:53-54.-E. Cutler and Cutler, 19873:751.-Saiz and Villafranca, 1990:1147. Phascolosoma cylindratum Keferstein, i865:428.-Gerould, 1913:382383. Golfingia cylindrata.—Stephen and Edmonds, 1972:89. Sipunculus obscurus de Quatrefages, i865b:6i6-6i7 (in part). Phascolosoma obscurum Baird, 1868:84. Phascolosoma forbesii Baird, 1868:83. Phascolosoma oxyurum Baird, 1868:83. Phascolosoma tenuicinctum Baird, 1868:83. Phascolosoma delagei Herubel, 19033:100. Phascolosoma charcoti Herubel, 19063:127-128. Golfingia charcoti.— Stephen and Edmonds, 1972:89. Phascolosoma teres Hutton, 1903:29-41. Phascolosoma derjugini Gadd, 1911:82-83. Golfingia derjugini.— Stephen and Edmonds, 1972:90. Phascolosoma abyssorum var. punctatum Herubel, 19253:261.-Saiz, 19840:193-197. Phascolosoma cluthensis Stephen, 1931:59-61. DESCRIPTION. The 8-10 rings of slender hooks chsracterize this wellfounded taxon. It is a smooth, slender, lustrous worm (Fig. 15C, D). The introvert is short (20-40% of the trunk length) and carries 20-36 tent3cles in a single disk. Ordinarily there is a normal set of four retractors (ventrals at 30-40% 3nd dorssls 3t 10% of the distance toward the posterior end), but this species exhibits occasion3l loss or fusion of one or two muscles (Gibbs, 1977b). DISTRIBUTION. The northwestern (Newfoundknd to Bermuds 3nd Cubs) 3nd northeastern Atlantic (Spitzbergen to Iberian Peninsula 3nd the Mediterranean), from intertidal depths to 400 m; the P3cific Ocesn from the East and South China seas at 90-590 m; and Vietnam, from depths of 1-12 m.
Golfingia iniqua (Sluiter, 1912) Phascolosoma iniquum Sliter, 1912:14. Golfingia iniqua.—Stephen and Edmonds, 1972:93.-Gibbs, I986:335.-E. Cutler 3nd Cutler, 19873: 751.-S31Z, 1993:58-60. Phascolosoma rugosum Southern, 1913:18-19. Golfingia rugosa.— Stephen and Edmonds, I972:i07.-Saiz, 1986^24-27.-Gibbs, 1986: 336.
Genus Golfingia
7i
Phascolosoma mutabile Southern, 1913:19-20. Golfingia mutabilis.— Stephen and Edmonds, i972:ioi.-Gibbs, 1986:336. DESCRIPTION. Deciduous hooks generally present, more numerous in small worms, sometimes absent in larger ones. This species shares many characters with G. margaritacea. A major difference is the shape of the trunk: G. iniqua is more robust, fat, and pear shaped, with its length (6-25 mm) almost always less than three times the width (Fig. 15B). The texture of the sometimes loose skin in worms larger than 10 mm is thick, with irregular wrinkles or a zigzag pattern. Smaller individuals do not have as thick a body wall in the midsection, but the width-to-length ratio is consistently lower than in other Golfingia species. DISTRIBUTION. Northeastern Atlantic Ocean, 29-52° N, 10-30° W, from 500-1800 m. Golfingia margaritacea margaritacea (Sars, 1851) Sipunculus margaritaceus Sars, 1851:196-197. Phascolosoma margaritaceum Danielssen and Koren, 1877:135.-Wesenberg-Lund, 1930: 25-28. Golfingia margaritacea.—Fisher, I952:39i.-Wesenberg-Lund, I955a:i99; I959b:209.-Gibbs, 1974:871-876; I977b:i2-I3.-E. Cutler et al., i984:263-264.-Saiz, i986b:2i-22; 1993:60-62. Golfingia margaritacea adelaidensis Edmonds, 1956:302-303; 1980:21.-Stephen and Edmonds, 1972:97. Golfingia margaritaceum californiensis Fisher, I 952:392-393--Stephen and Edmonds, 1972:97-98. Phascolosoma margaritacea finmarchica Theel, 1905:63—64. Golfingia margaritacea finmarchica.—Stephen and Edmonds, 1972:98. Phascolosoma margaritaceum forma sibirica Theel, 1905:64-65. Golfingia margaritacea sibirica.—Stephen and Edmonds, 1972:99. Golfingia margaritacea margaritacea.—E. Cutler and Cutler, I987a:743.-Saiz and Villafranca, 1990:1147. Homalosoma laeve Oersted, in Keferstein, 1865^436. Phascolosoma oerstedii Keferstein, 1865^436. Phascolosoma capsiforme Baird, 1868:83-84. Phascolosoma albidum Theel, i875b:8. Phascolosoma fulgens Theel, i875b:8. Phascolosoma hanseni Danielssen and Koren, 1881:9—13. Phascolosoma margaritaceum hanseni.—Stephen, 19413:253. Golfingia margaritacea hanseni.—Wesenberg-Lund, 19553:9. Stephanostoma barentsii Horst, 1882:39-40.
72
The Golfingiids
Phascolosoma antarcticum Michaelsen, 1889:73-74. Phascolosoma margaritaceum var. antarcticum.—W. Fischer, 1929:481. Golfingia margaritacea antarctica.—Stephen and Edmonds, 1972:97.-E. Cutler et al., 1984:265. Phascolosoma fuscom Michaelsen, 1889:76. Phascolosoma georgianum Michaelsen, 1889:78. Phascolosoma profundum Roule, 1898^385; 1906:74-77. Golfingia profunda.—Stephen and Edmonds, 1972:104. Phascolosoma japonicum Ikeda, 1904:5-7. Golfingia ikedai.—Fisher (nom. nov. pro Phascolosoma japonicum Ikeda, I904).-Stephen and Edmonds, 1972:92. Golfingia margaritacea ikedai.—E. Cutler et al., 1984:264-265. Phascolosoma okinoseanum Ikeda, 1904:9-12. Golfingia okinoseana.— Stephen and Edmonds, I972:i03.-E. Cutler et al., 1984:263. Phascolosoma trybomi Theel, 1905:69-70. Phascolosoma margaritaceum trybomi.—Fischer, 1924:72. Golfingia margaritacea trybomi.— Wesenberg-Lund, I955a:8.-Murina, 19773:232-233. Phascolosoma socium Lanchester, 1908:1. Phascolosoma nordenskjoldi Theel, 1911:30-31. Golfingia nordenskjoldi.—Wesenberg-Lund, 19553:9-1 i.-Murina, 1978:122. Phascolosoma margaritaceum var. meridionalis Gerould, 1913:382. Golfingia margaritacea meridionalis.—Stephen and Edmonds, 1972:9899Phascolosoma glossipapillosum Sato, 19343:10-12. Golfingia glossipapillosa.—Stephen and Edmonds, I972:9i.-E. Cutler and Cutler, 1981:61-62. Phascolosoma noto Sat6, 19343:14-16. Golfingia nota.—Stephen and Edmonds, I 9 7 2 : I O 2 . - E . Cutler 3nd Cutler, 1981:63. Phascolosoma signum Sato, 19343:16-17. Golfingia signa.—Stephen snd Edmonds, I 9 7 2 : I O 8 . - E . Cutler et al., 1984:266. Phascolosoma soyo Sat6, 19343:17-20. Golfingia soya.—Stephen 3nd Edmonds, 1972:109. Golfingia margaritacea soyo.—E. Cutler et al., 1984:265. Golfingia cantabriensis Edmonds, 1960:163-164; Stephen and Edmonds, 1972:86-87. NOTE. This is the most widespread and difficult to define species (superspecies?) in this genus. It has a long and complex nomenclatural history and has retained most of the plesiomorphic (ancestral) characters thought to be unique to this subgenus with no unique traits. A detsiled critique of the names previously considered to be varieties, forms, or subspecies of
Genus Golfingia
73
G. margaritacea, plus several changes in status, is presented in E. Cutler and Cutler, 1987a. What appears above is a condensed synonymy. DESCRIPTION. Aside from the generic and subgeneric characters, there is little to add. It is usually a smooth-skinned, cylindrical worm, commonly 10-30 mm long, but may be up to 150 mm long (Fig. 15 A). The introvert is less than half the trunk length, and small (20-35 M-m). pale hooks have been seen only in a few small, shallow-water individuals. The number of tentacles (8-100) varies with the size of the worm (Fig. 17C-E). The contractile vessel is enlarged and vesicular in some populations. DISTRIBUTION. Very widely distributed, found in all sectors of the Atlantic, Arctic, and Antarctic oceans (8o° N to 78° S); and the northern, southeastern, and southwestern Pacific (above 300 N and 300 S), sometimes at lower latitudes, but then in deep water (>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 (
74
The Golfingiids
Golfingia mirabilis Murina, 1969 Golfingia mirabilis Murina, 1969b: 1732-1733.-E. Cutler and Cutler, 19873:752. DESCRIPTION. The posterior end of the single specimen is somewhat contracted, dark, papillated, and rugose. The skin at the anterior end has faint zigzag ridges and is dark, but is not a shield. The 36-mm trunk has a short, nipplelike termination (not a tail). The hooks are large (at least 200 |xm tall), and the tentacles are especially numerous (>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 <25 mm), is easily distinguished by its caudsl appendage, which may be nipplelike in worms less than 5 mm and is commonly 20-35% of the trunk length (up to about 50% of trunk length in large worms; see Fig. 18E). Cylindrical papillae are present over part of the posterior. The nerve cord ends anterior to the tail. The skin is generally smooth, psle, 3nd translucent in small worms but dark and rugose in those more than 25 mm long. Deciduous hooks, up to 100 (xm tall, are present in small worms, but most have been lost by the time the animsl resches 5-10 mm long. The introvert is generally shorter than the trunk, with a normal array of 12 or more tentacles. DISTRIBUTION. Common at bathyal and abyssal depths in the North Atlantic from Cape Hstteras (one Caribbean record at 170 N from 4000 m) up to 5 8° N, across to Europe and West Africa (at 60-70 m in upwelling areas off Ivory Coast, but otherwise from 230-5000 m, 570 N to 320 S). It
Genus Golfingia
75
occurs down to South Africa and the Kerguelen and Bouvet islands, and up the east coast of Africa, through the Mozambique Channel, to Tanzania at bathyal depths; unknown from the rest of the Indian Ocean. In the North Pacific it has been recorded from British Columbia, around the Bering Sea, to Japan, at depths of 85-6860 m. Murina, 1978, the only record from the far southern Pacific, is based on six worms collected from around 550 S, 1590 E, at 4400-5400 m. Golfingia vulgaris vulgaris (de Blainville, 1827) Sipunculus vulgaris de Blainville, 1827:312-313. Phascolosoma vulgare. —Keferstein, i862b:39; i865b:429.-Selenka et al., 1883:20-23.Theel, i905:6o.-Stephen, 1934:169. Golfingia vulgaris.—WesenbergLund, I957c:4.-Stephen, I958:i3i.-Murina, I977a:2i7-2I9.-Gibbs, 1977b: 14-15.-E. Cutler et al., i984:266-267.-Saiz, 1986^27; 1993: 53. Golfingia vulgaris vulgaris.—Stephen and Edmonds, 1972:110. -E. Cutler and Cutler i987a:753.-Saiz and Villafranca, 1990:11471148. Phascolosoma vulgare var. astuta Selenka, 1885:11. Golfingia vulgaris astuta.—Stephen and Edmonds, 1972:111-112. Phascolosoma vulgare var. multipapillosum Herubel, I925a:26i. Golfingia vulgaris multipapillosa.—Stephen and Edmonds, 1972:112. Phascolosoma vulgare selenkae Lanchester, 1905^31-32. Golfingia vulgaris selenkae.—Stephen and Edmonds, 1972:112-113. Phascolosoma vulgare tropicum Sluiter, 1902:33-34. Golfingia vulgaris tropica.— Stephen and Edmonds, 1972:113. Golfingia vulgaris vesiculosus Murina, 19698:86. Phascolosoma longicolle Leuckart and Ruppell, i828:6.-Griibe, 1840:47; i868:644.-Diesing, 1851:64; i859:762.-Baird, i868:95.-Stephen and Edmonds, I972:339.-Saiz, 1989:208. Sipunculus papillosum Thompson, 1840:101 (in part). Syrinx harveyii Forbes, 1841:249. Phascolosoma harveii Baird, 1868:8283Sipunculus communis de Quatrefages, 1850:374. Sipunculus punctatissimus Gosse, 1853:125. Phascolosoma punctatissimum Diesing, 1859:763. Phascolosoma commune Keferstein 1863:39. Sipunculus obscurus de Quatrefages, 1865^616-617 (in part). Phascolosoma obscurum Baird, 1868:84. Phascolosoma luteum Theel, 1875^5-6. Phascolosoma dubium Theel, i875b:6.
76
The Golfingiids
Phascolosoma validum Th6el, i875b:7-8. Golfingia mackintoshii Lankester, 18853:469-471. Phascolosoma sanderi Collin, 1892:177. Golfingia sanderi.—Stephen and Edmonds, 1972:1 io.-Murina, I977a:210-211. Phascolosoma owstoni Ikeda, 1904:12-15. Golfingia owstoni.—Stephen and Edmonds, I972:i03-I04.-E. Cutler and Cutler, 1981:64-65. Phascolosoma kolense Gadd, 1911:80-81. Golfingia kolensis.—Stephen and Edmonds, I972:93.-E. Cutler and Murina, 1977:177-178. Phascolosoma solitarium Sluiter, 1912:15-16. Golfingia solitaria.— Stephen and Edmonds, 1972:108. Golfingia (Dushana) adriatica Murina, i975c:io85-io87.-Zavodnik and Murina, 1976:86. DESCRIPTION. Both ends of the trunk are distinct—dark brown or black and heavily papillated—while the mid-trunk is smooth and white. The trunk itself may be up to 200 mm long (commonly 20-50 mm), and the shorter introvert bears digitiform tentacles. The scattered large hooks (up to 150 jun) are dark and spinelike. The spindle muscle is well developed and originates under the wing muscle just posterior to the anus, sometimes from two branches. The nephridia open anterior to the anus. Although four retractors are the norm, worms with only three have been noted (E. Cutler et al., 1984). DISTRIBUTION. In the northeastern Atlantic Ocean including Greenland, Scandinavia, and the British Isles, and into the Mediterranean, Adriatic, and Red seas; south to the Azores, Canary Islands, Cape Verde Islands, and West Africa; the Indian Ocean off South Africa and Zanzibar; the Pacific Ocean in the Kurile-Kamchatka Trench, Japan, Malaya, Singapore, and one record (Frank, 1983) off British Columbia (the only one from the eastern Pacific). The depth range is 5-2000 m, but specimens from depths greater than 500 m are rare. There is one very deep record: from 5540 m in the Kurile-Kamchatka Trench. The absence of this species from the western Atlantic Ocean and its rarity in the eastern Pacific are noteworthy. The Indo-West Pacific warm-water specimens may actually belong to a distinct taxon (or the following subspecies). Golfingia vulgaris herdmani (Shipley, 1903) Centrosiphon herdmani Shipley, I903:i7i-I74.-Stephen and Edmonds, 1972:268-269. Golfingia herdmani Edmonds, 1980:19-21. Golfingia vulgaris herdmani E. Cutler and Cutler, 19873:755.
Genus Nephasoma
77
Golfingia vulgaris queenslandensis Edmonds, i956:303-305.-Stephen and Edmonds, 1972:1 i2.-Edmonds, 1980:21-22. Golfingia liochros E. Cutler and Cutler, 19793:950-951. DESCRIPTION. Animals belonging to this subspecies may be up to 60 mm long. This form differs from the nominate form by having modified caps or pseudoshields consisting of dark spherical papillae arranged in irregular radiating rows; these are especially evident on the posterior end but are also found on the anterior end (Fig. 18F). It has larger hooks (120200 (xm) associated with bulbous papillae, and its habitat (shallow, warm water) is also different from that of the nominate form. This construct may be an artificial amalgamation of two taxa (E. Cutler and Cutler, 1987a); another possibility is that Shipley's original material, now lost to science, may have belonged in the Aspidosiphonidae. DISTRIBUTION. Madagascar, Mozambique, Sri Lanka, Thailand, Great Barrier Reef, and South Australia; from intertidal depths (one from 300 m).
Genus Nephasoma Pergament, 1940 Nephasoma Pergament, 1940:1-3.-^ Cutler and Cutler, 1986:548. Golfingia (Phascoloides) Fisher, i95oa:550.-Stephen and Edmonds, 1972:131. DIAGNOSIS. Introvert about equal to or shorter than trunk. Hooks, when present, usually scattered (but arranged in rings in N. rimicola and in spirals in N. abyssorum). Body wall with continuous muscle layers. Tentacles arranged around the mouth but may be reduced in both size and number. Two introvert retractor muscles, often partially fused. Contractile vessel without villi. Spindle muscle not attached posteriorly. Two nephridia. Species generally small to medium sized (trunk <50 mm long). See Figures 19-24. TYPE SPECIES. Nephasoma marinki Pergament, 1940 = Onchnesoma glaciale Danielssen and Koren: E. Cutler and Murina, 1977; = Phascolosoma lilljeborgii Danielssen and Koren: Gibbs, 1982. NOMENCLATURAL NOTE. This genus contains the species previously assigned to the Golfingia subgenus Phascoloides Fisher, 1950, since Nephasoma Pergament has been shown to have priority over Phascoloides (E. Cutler and Murina, 1977). The convoluted nomenclatural history of this taxon was reviewed by N. Cutler and Cutler (1986), who modified the endings of some species names because Nephasoma is a neuter name.
7»
The Golfingiids
Morphological Characters of Nephasoma Introvert Hooks. A few earlier authors entertained the possibility of deciduous hooks in this genus (e.g., Selenka, 1885; Gerould, 1913; Southern, 1913), but most did not. It has been proposed (N. Cutler and Cutler, 1986) that three types of species exist within this genus: (1) those that never have hooks (e.g., N. eremita), (2) those that have hooks throughout their lives (e.g., N. abyssorum), and (3) those with deciduous hooks (e.g., N. wodjanizkii elisae). One might well ask whether a young specimen of N. eremita with hooks might not mistakenly be classified as a "hooked" species, or whether a large N. abyssorum that had lost its hooks might be identified as a "hookless" species. These possibilities prevent the mere presence or absence of hooks from being a completely diagnostic character. When they are present, however, hooks have attributes useful for identifying species (Fig. 21). A few species have characteristic shapes or sizes (N. confusum, N. constricticervix, and N. multiaraneusa) or unique arrangements (JV. abyssorum and N. rimicola). Most species have nondescript small, bluntly triangular, transparent, scattered hooks 20-40 jjim tall. Six species have hooks 50-150 jxm tall (N. abyssorum, N. confusum, N. cutleri, N. laetmophilum, N. rimicola, and N. schuettei), and two regularly have hooks more than 150 |xm tall (TV. vitjazi and N. constricticervix; both are deep-water species). Tentacles. Two general types of tentacular arrays appear in Nephasoma. About half the species have a "normal" crown of flattened, digitate tentacles (>io, number increasing with age; see Fig. 22A). The remaining species have a few (8 or less) short, lobate tentacles; some may have only two tentacles plus four to six small lobes (Fig. 22B). Two species have unique arrangements (N. novaezealandiae and N. (Cutlerensis) rutilofuscum; see Fig. 24). Tentacular arrays can be helpful characters if they are exFigure 19. Nephasoma body forms. A. N. eremita, a stout, smooth-skinned species up to 25 mm long (from Gerould, 1913). B. N. pellucida a heavily papillated species (<25 mm) showing portion of esophagus protruding through mouth. C. N. wodjanizkii, a long, very slender (30-50 by 1-2 mm) cold-water species with long introvert and small hooks. D. N. constricticervix, a small (5-15 mm) deep-water species with a short introvert and large hooks. E and F. N. flagriferum, a larger (
Genus Nephasoma
81
Figure 21. Introvert hooks of Nephasoma species, showing range of size and shapes. A. N. constricticervix (slender, 50-250 (im). B. N. abyssorum (stout, 50-150 yun). C. N. confusum (70-90 u.m). D. N. minutum (typical small, 25-40 u.m). E. N. multiaraneusa (unique, spiderlike, 15-30 yum). (From N. Cutler and Cutler, 1986, courtesy of the Biological Society of Washington.)
panded, but since most preserved specimens do not have fully extended introverts, it is difficult to accurately interpret these arrays from dissected material. Caudal Appendage. This is best exhibited in N. flagriferum as a thin tail. In N. bulbosum it is more like a narrowed, tapering portion of the trunk, not an appendage. The posterior end of the trunk in the other species may form a conical point like a dull pencil, but not a tail. Trunk Length-to-Width Ratio. Two general patterns exist: elongate, slender worms (trunk length > i o times the width); and shorter, stouter worms (length <6-8 times the width). There is, however, wide variation in this ratio within both populations and individuals. This character should be used only in a very general way; it can be misleading if interpreted too narrowly. Introvert Length. In most species the introvert is shorter than the trunk. The introvert length ranges from 20% of the trunk length in N. constric-
Figure 20. Nephasoma diaphanes, a very common, small (most < i o mm) deep-water worm. A. External form of typical smooth-skinned form. B. Enlarged portion of posterior trunk showing how the papillae may become well developed and dark. C-E. Internal organs showing variations in the position of retractor muscle origins in midtrunk to near the posterior end at 50, 65, and 95% of the distance toward the posterior end (from Theel, 1905). Abbreviations as in Figure 1.
82
The Golfingiids
Figure 22. Nephasoma tentacles. A. Normal array in N. rimicola. B. Reduced array, as in N. minutum. (From Gibbs, 1977b, courtesy of the Linnean Society.)
Figure 23. Introvert and anterior end of three elongate, slender, deep-water Nephasoma species, drawn as if trunk lengths were equal to show comparative lengths of introverts. A. N. capilleforme. B. N. cutleri. C. N. tasmaniense. (From N. Cutler and Cutler, 1986, courtesy of the Biological Society of Washington.)
Genus Nephasoma
83
ticervix to 200% of the trunk length in a few species. When the introvert is retracted or only partially extended it appears shorter than it would if completely extended, owing to its extreme elasticity. If accurately determined, introvert length can be of some use to the taxonomist. One must remember, however, that the trunk grows faster than the introvert, and as a worm ages, the introvert represents a smaller fraction of the total length (see N. Cutler and Cutler, 1986). Anus-Nephridiopore Relationship. The anus is usually located at the anterior end of the trunk, as are the paired nephridiopores. The nephridiopores are at the level of the anus in most Nephasoma species, but in six species they are anterior to the anus, commonly by 3-10% of the trunk length (see N. Cutler and Cutler, ic;86:appendix). The nephridiopores in seven species are reported to be posterior to the anus. This determination is difficult and subjective in smaller worms, in which the distance may be less than 1 mm, but it does have some value as a character for identification. Anterior Trunk Papillae. The term shield has been inappropriately used to describe an aggregation of close-packed papillae around the distal end of the trunk that has a dark, rugose appearance. This condition is different from the true shield found in the Aspidosiphonidae, and its use with regard to Nephasoma is misleading. The epidermal papillae may be gathered into longitudinal ridges and darkly pigmented (e.g., in N. vitjazi and N. wodjanizkii). Spindle Muscle. In Nephasoma this muscle does not extend beyond the posterior end of the gut coil, and in most species it does not extend beyond the anterior end either. In some species it seems to originate from the wall of the rectum and can be seen going into the anterior coils. In a few species (e.g., N. flagriferum) the spindle muscle is well developed, sometimes branching, and sometimes begins anterior to the rectum on the body wall near or anterior to the anus. In a few others (e.g., N. abyssorum and N. lilljeborgi) it is rare to find any trace of the spindle muscle. There is variation within populations (see N. constrictum, in N. Cutler and Cutler, I986:appendix), and in small worms the spindle muscle is very difficult to find even when present. The value of this attribute to the taxonomist is minimal.
84
The Golfingiids
Introvert Retractor Muscles. Most commonly the retractors originate between 30 and 70% of the distance toward the posterior end of the trunk, although this relative position may vary randomly within a species (as in N. diaphanes; see Fig. 20C-E). As the worm grows and trunk length increases, the origin appears to move anteriad (see N. Cutler and Cutler, I986:appendix). Four species have retractor origins in the 15-30% range (N. constricticervix, N. novaezealandiae, N. tasmaniense, and N. vitjazi), and three have these origins between 75 and 90% of the distance to the posterior end of the trunk (N.filiforme, N. (C.) rutilofuscum, and N. wodjanizkii). Intestinal Coiling. In most Nephasoma species the gut is a tightly wound double helix, but in some of the elongate, slender species the helix is stretched out or loosely wound with obvious space between the individual coils. Rectal Caecum. The presence or absence of a small rectal caecum is not a dependable or consistent feature in most species, although a few (e.g., N. constrictum) seem to consistently lack one, while others seem consistently to have one (e.g., N.flagriferum). Thus in a few cases the presence or absence of a caecum may be helpful as a diagnostic character. Key to Nephasoma Species The identification of Nephasoma species is not easy owing to the small size of most worms (diameter is often < 1 mm) and the paucity of differentiating characters. Many of the useful features are on the distal end'of the introvert, which is rarely fully extended in preserved material. 1. Trunk rusty red N. (Cutlerensis) rutilofuscum - Trunk white, yellow, or brown, not red Nephasoma s. s., 2 2. Posterior end of trunk with caudal appendage (tail) 3 - Posterior end of trunk rounded or bluntly pointed 4 3. Posterior end of trunk with large papillae; "tail" thin, ratlike (Fig. 19E, F) N. flagriferum - Posterior end of trunk without large papillae; "tail" formed from narrowed portion of trunk N. bulbosum
Genus Nephasoma 4. Trunk with obvious pigmented, raised papillae
85 5
- Trunk may have papillae (skin bodies), but they are unpigmented and barely raised above surface 8 5. Worms often >50 mm long; large, very dark papillae; hooks >50 |xm tall N. schuettei - Worms usually <30 mm long; papillae moderately pigmented; hooks <4o fjtm tall
6
6. Tentacles present; papillae uniformly distributed over trunk; length rarely exceeds width by more than 8 times (stout cylinder or flask shaped); shallow to bathyal depths 7 - Tentacles reduced to lobes; papillae rare in mid-trunk; trunk length commonly exceeds width by more than eight times (slender cylinder); deep, cold water (Fig. 20) N. diaphanes 7. Trunk flask shaped; anus on narrowed anterior region, which usually also exhibits an indented constriction; nephridia posterior to anus N. constrictum - Trunk sausage shaped; nephridia not posterior to anus
N. pellucidum
8. Elongate, very slender transparent trunk, sometimes threadlike (trunk width usually less than one-tenth the length); gut with separated coils and no spindle muscle 9 - Cylindrical translucent or opaque trunk (trunk width rarely less than a tenth the length); gut coils close together, spindle muscle usually present 14 9. About 30 dark longitudinal epidermal ridges at anterior end of trunk, sometimes giving the impression of a hardened pseudoshield 10 - Anterior end of trunk without dark epidermal ridges
11
10. Retractor muscles originate in anterior third of trunk; introvert less than onethird the trunk length; distal hooks >I50 \xm tall N. vitjazi - Retractor muscles originate in posterior third of trunk; introvert one-half to seven times the trunk length (Fig. 19C); distal hooks <25 |xm tall N. wodjanizkii 11. Anterior end of trunk a short cone with epidermal ridge around base of cone (Fig. 23C) N. tasmaniense - Anterior end of trunk not cone shaped but often swollen around nephridiopores 12 12. Introvert longer than trunk (Fig. 23A); retractor muscles originate 35-50% of
The Golfingiids the distance to posterior end; hooks <30 |xm tall
iV. capilleforme
- Introvert shorter than trunk; retractor muscles originate 15-30% of the distance to posterior end; distal hooks >ioo jjum tall 13 13. Introvert length <25% of trunk length (Fig. 19D); distal hooks >20O |xm N. constricticervix - Introvert length 50-75% of trunk length (Fig. 23B); distal hooks 150 |xm or less N. cutleri 14. Hooks in distinct rings around introvert - Hooks, if present, not in rings
N. rimicola 15
15. Hooks with unusual series of radiating filaments from base (Fig. 21E) N. multiaraneusa - Hooks, if present, without basal filaments 16. Retractor muscles originate in posterior fourth of trunk - Retractor muscles originate in middle third of trunk 17. Tentacular crown reduced to short lobes, dorsal pair largest - Normal array of digitiform tentacles present
16 iV. filiforme 17 18 20
18. Hermaphroditic species from shallow northeastern Atlantic waters; trunk length usually four to five times diameter N. minutum - Dioecious; trunk length 6-10 times diameter 19. Larger; opaque; from bathyal depths
19 N. lilljeborgi
- Smaller than N. lilljeborgi; transparent to translucent; from bathyal and abyssal depths (Fig. 20) N. diaphanes 20. Medium-sized (>50 (xm) dark hooks present - Hooks apparently absent
21 23
21. Hooks have unique shape, arranged spirally, like a barber's pole (Fig. 21B) N. abyssorum (two subspecies) - Hooks scattered 22. Hooks robust and blunt (Fig. 21C) - Hooks tall, spinelike, with soft cortical layer
22 iV. confusum N. laetmophilum
23. Fewer than 50 digitiform tentacles; introvert one to two times trunk length JV. eremita - More than 50 threadlike tentacles; introvert less than half trunk length iV. novaezealandiae
Genus Nephasoma
87
Subgenus Nephasoma (Cutlerensis) (Popkov, 1991) Cutlerensis Popkov, 1991:132-134. DIAGNOSIS. Tentacles present only on the dorsal side of the distal tip of introvert, only a few around the mouth. TYPE SPECIES. Aspidosiphon rutilofuscus W. Fischer, 1916. NOMENCLATURAL NOTE. N. Cutler and Cutler (1986:564) indicated that the single species in this subgenus may merit separate generic rank. Their statement seems to have stimulated a Russian graduate student (Popkov, 1991) to reexamine a few Madagascar specimens from an earlier study (E. Cutler and Cutler, 1979a), and he placed N. rutilofuscus into a new genus, Cutlerensis, based on existing material and information and his own interpretation of the importance of the unique tentacular arrangement (and, secondarily, the animal's red color). The segregation of species into higher taxa is often done subjectively, and I feel that a generic level is inappropriate at this time. When new information becomes available (e.g., biochemical, developmental, histological), this issue should be reexamined. I therefore treat Nephasoma (Cutlerensis) as a subgenus. Nephasoma (Cutlerensis) rutilofuscum (W. Fischer, 1916) Aspidosiphon rutilofuscus W. Fischer, 1916:17. Golfingia rutilofusca.— Fisher, I952:395.-Stephen and Edmonds, I972:i53-I54.-E. Cutler, I977a:i43-I44.-E. Cutler and Cutler, 19793:958-961. Nephasoma rutilofuscum.—N. Cutler and Cutler, 1986:564. Cutlerensis rutilofuscus Popkov, 1991:132-134. Phascolosoma aspidosiphonoides W. Fischer, I922b:n-i2. DESCRIPTION. The rusty red color (some animals have irregular white patches) makes this hookless species easy to identify. The trunk is 2-15 mm, and the posterior end sometimes appears as a grooved, pointed "shield," but appearance varies with degree of body wall contraction, and the posterior may also be smooth and round (Fig. 24A-C). The introvert is five to six times the trunk length, and its distal half is unpigmented. At its tip, in a dorsal zone covering an area like the fingerprint part on a human finger, is a unique array of about 30 slender, unbranched tentacles (Fig. 24D). A few tentacles surround the terminal mouth. The two retractor muscles originate in the posterior 20% of the trunk, and the unattached
88
The Golfingiids
Figure 24. Nephasoma (Cutlerensis) rutilofuscum. A. Whole worm with reddish trunk and very pale introvert. B and C. Posterior end of two worms showing possible range of variation in form; width of trunk about 3 mm. D. Distal tip of introvert showing peculiar dorsal array of tentacles. (From E. Cutler and Cutler, 1979a, courtesy of the Museum National d'Histoire Naturelle.)
nephridia open a little anterior to the anus. The intestine is loosely coiled, and the spindle muscle has not been observed. DISTRIBUTION. Western Indian Ocean, from 1-1560 m.
Subgenus Nephasoma (Nephasoma) Pergament, 1940 DIAGNOSIS. Tentacles, sometimes few and small, arranged more or less uniformly around the periphery of the oral disk. Spindle muscle present but unattached posteriorly. NOTE. Since the early 1900s biologists have been troubled by one subset within this genus, the minutum section: worms with reduced tentacles; small, scattered, transparent, possibly deciduous hooks; normal body proportions; a nondistinct internal anatomy; and no unique external feature. N. Cutler and Cutler (1986) discussed the several names that have at various
Genus Nephasoma
89
times been placed in this complex, including N. minutum (sensu Gibbs, I 975» I977b), N. abyssorum, N. diaphanes (with its new subspecies), and N. lilljeborgi. Further studies employing new techniques may lead to conclusions different from those presented below and in N. Cutler and Cutler, 1986. When one has only a few animals, it is easy to separate them into subsets, but when one is working with hundreds of specimens (common in deep-water surveys), the distinctions blur and a continuum appears. In terms of almost all the standard characters, members of the minutum group are identical. Anyone conducting zoogeographical analyses of marine animals should omit these species—especially N. minutum—from consideration, as well as all their junior synonyms. Nephasoma abyssorum abyssorum (Koren and Danielssen, 1875) Phascolosoma abyssorum Koren and Danielssen, 1875:129-130.-Th6el, 1905:78. Golfingia abyssorum.—Wesenberg-Lund, 1955^201.Stephen and Edmonds, I972:i34-I35.-Gibbs, 1982:121.-E. Cutler et al., i984:268-269.-Saiz, 1984^182-183. Nephasoma abyssorum abyssorum.—N. Cutler and Cutler, i986:554.-Saiz and Villafranca, I990:ii49-H50.-Saiz, 1993:85-87. Phascolosoma incompositum Sluiter, 1912:16-17. Golfingia incomposita. —Stephen and Edmonds, 1972:145-146. Nephasoma incompositum.— Gibbs, 1986:339-340. DESCRIPTION. In general shape and appearance this smooth, white, sometimes iridescent worm, up to 45 mm long, is similar to N. lilljeborgi and N. minutum. It is distinguished by its short but fully developed digitiform tentacles and unique spirally arranged, medium-sized (50-150 (xm long), dark hooks (Fig. 21B). A spindle muscle (weakly developed) was observed within the gut coil in only two of the eleven specimens closely examined by N. Cutler and Cutler (1986). The retractors originate in the second quarter of the trunk. The trunk is usually 10-30 mm long, with low-profile, elliptical skin bodies, and some dome-shaped papillae at the posterior end. DISTRIBUTION. Common in the northeastern Atlantic and Arctic oceans; rare in the southeastern and northwestern Atlantic, the northwestern Pacific, and the Mediterranean Sea; found at bathyal to abyssal depths (5005300 m).
9o
The Golfingiids
Nephasoma abyssorum benhami (Stephen, 1948) Phascolosoma benhami Stephen, 1948:218-219. Golfingia benhami.— Stephen and Edmonds, 1972:135-136. Nephasoma abyssorum benhami N. Cutler and Cutler, 1986:586. DESCRIPTION. Like the nominate form, this subspecies has large, dark hooks and developed tentacles. The major morphological distinction between the subspecies is the strongly developed spindle muscle herein. The retractors originate in the middle third of the trunk, and the spindle muscle is within the gut coil but not on the rectum. Its disjunct distribution (there are no records of TV. a. abyssorum near the southern latitudes at which this taxon is found) also supports subspecific ranking for this population. DISTRIBUTION. Off Kemp Land, Antarctica, at 600 m. Nephasoma bulbosum (Southern, 1913) Phascolosoma bulbosum Southern, 1913:23-24. Golfingia bulbosa.— Stephen and Edmonds, I972:i36.-E. Cutler, 1973:152-153. Nephasoma bulbosum.—Gibbs, I986:337.-N. Cutler and Cutler, 1986:556. DESCRIPTION. This species is similar to TV.' flagriferum in having a "tail" and papillae on the posterior end of the trunk, but both structures are much smaller in this species. The tail is not really an appendage, more a narrowing of the trunk into a point. The nerve cord extends into the distal tip of this tail. Except for the shape of the body, this species resembles TV. eremita in many ways, including the apparent absence of hooks. DISTRIBUTION. North Atlantic (off Ireland and the northeastern United States) at bathyal depths. Nephasoma capilleforme (Murina, 1973) Golfingia capilleformis Murina, i973b:943-944.-Frank, 1983:14-15. Nephasoma capilleforme.—N. Cutler and Cutler, I986:556.-Saiz, 1993:69. Golfingia glacialis.—Murina, 19640:57-59, I974a:234.-E. Cutler and Cutler, i98ob:453-454. DESCRIPTION. This species is one of the group of slender deep-water worms with a loosely wound gut coil. The long introvert (one to two times the trunk length when extended) and small hooks (20-25 M-01) a r e diagnostic (Fig. 23A). This species has the most elongate, threadlike body of the
Genus Nephasoma
9i
genus (often
2000 m). Nephasoma confusion (Sluiter, 1902) Phascolosoma confusum Sluiter, 1902:38-39. Golfingia confusa.— Murina, 1957^993-994; 1978:123.-Stephen and Edmonds, 1972:138139.-E. Cutler and Cutler, 1980c: i99-200.-Ditadi and Migotto, I98i:i25-I34.-E. Cutler et al., 1984:269. Nephasoma confusum.—N. Cutler and Cutler, I986:556.-Saiz, 1993:87-89. Golfingia confusa zarenkovi Murina, 1974^1716-1717. DESCRIPTION. The scattered hooks are medium sized (70-90 p,m) and have a distinctive reinforcing rim (Fig. 21C). The body lacks papillae but does have round skin bodies and may be darker at the two ends with intersecting grooves. The introvert is about as long as the trunk. The detailed redescription by Ditadi and Migotto (1981) was based on 106 specimens ranging in length from 2.5 to 25 mm. DISTRIBUTION. More common in the Southern Hemisphere around Antarctica, southern Australia, and Indonesia, but also reported in the northwestern Pacific Ocean and off Brazil. Recent records from around Gibraltar in the northeastern Atlantic may be N. constrictum, as evidenced by the animals' larger papillae, much smaller hooks, and cryptobiotic lifestyle in that area (see Saiz and Villafranca, 1990). Nephasoma constricticervix (E. Cutler, 1969) Golfingia constricticervix E. Cutler, 1969:215-217.-E. Cutler and Cutler, i98oc:20o. Nephasoma constricticervix.—N. Cutler and Cutler, 1986: 557.-Saiz and Villafranca, 1990:1153.-Saiz, 1993:70-72. DESCRIPTION. This is one of the two Nephasoma species that have some hooks exceeding 200 u,m (Fig. 21A). It is a slender, elongate (5-15 mm), deep-water worm, and if the short introvert (20-45% O I " m e trunk length) is withdrawn or incomplete, it can be difficult to identify. The bulbous
92
The Golfingiids
region at the anterior end of the trunk tapers quickly into the constricted neck (Fig. 19D). The hooks on a single worm may range in size from 40 to 250 ixm; only the more distal hooks exceed 200 (jim. If only the smaller proximal hooks are seen, it is possible to mistake this for some other species (e.g., N. cutleri). DISTRIBUTION. Both sides of the northern Atlantic at 1200-5500 m, and south to 220 S on the eastern side. Nephasoma constrictum (Southern, 1913) Phq$colosoma constrictum Southern, 1913:25-27. Golfingia constricta.— Stephen and Edmonds, 1972:139. Nephasoma constrictum.—Gibbs, I986:337.-N. Cutler and Cutler, I986:557.-E. Cutler and Cutler, I987b:74.-Saiz and Villafranca, I990:ii53-H56.-Saiz, 1993:90-92. DESCRIPTION. This species is similar to N. pellucidum in most of its internal features, proportions (length 8-10 times width), and rough body covered with uniformly distributed dark papillae. It differs by having a flask-shaped trunk (up to 32 mm); about 12 short, stubby tentacles or lobes; and a narrowed constriction at the introvert-trunk junction in most worms. Pale hooks, not always present, are 20-40 \xm tall. When hooks are absent, the papillae in the bulbous region behind the tentacles are more apparent. A nipplelike posterior is evident in many worms. The nephridia open posterior to the anus, and the two retractor muscles originate in the trunk 50-70% of the distance to the posterior end. A spindle muscle is present in most animals, but it is weakly developed and does not extend anteriorly out of the gut coil along the rectum. DISTRIBUTION. Off Ireland at 1100-1300 m; elsewhere in the northeastern Atlantic Ocean and western Mediterranean (34-51° N) at 2002800 m (one from 4000 m). Lives a Phascolion-type lifestyle in empty gastropod and scaphopod shells or makes clay-mud tubes. Unpublished records from the French Safari collections extend this range, disjunctly, into the central Indian Ocean (2-8° S, 79-87 0 E, at 1100-4300 m). Nephasoma cutleri (Murina, 1975) Golfingia cutleri Murina, i975d:io87-io88; 1978:123. Nephasoma cutleri.—N. Cutler and Cutler, 1986:557. DESCRIPTION. Introvert length is 50-75% of the trunk length (not 20-
Genus Nephasoma
93
25%, as in the similar N. constricticervix), and the worm is very thin and fragile (Fig. 23B). The pale hooks are less than 150 jx,m tall. DISTRIBUTION. Pacific Ocean, scattered reports from 80° S to n ° N, 45-1780 E, at abyssal depths (2600-4600 m). Nephasoma diaphanes diaphanes (Gerould, 1913) Phascolosoma diaphanes Gerould, 1913:395. Golfingia diaphanes.—E. Cutler and Cutler, 1980^452-453; i98oc:20i-202.-E. Cutler et al., 1984:269-270. Nephasoma diaphanes diaphanes N. Cutler and Cutler, i986:557.-Saiz and Villafranca, 1990:1 i56-H58.-Saiz, 1993:79-84. Phascolosoma minutum.—Theel, I9ii:3i.-Wesenberg-Lund, 1937^1213. Golfingia minuta.—Wesenberg-Lund, 1955a: 11.-Murina, 1957b: 994-995; I978:i24.-Stephen and Edmonds, I972:i49-I50.-E. Cutler, I973:i55-I59--E. Cutler and Cutler, I979a:957~958.-Saiz, 1984b: 183. Phascolosoma anceps.—Sluiter, i9i2:io.-Wesenberg-Lund, 1925:90. Phascolosoma sabellariae.—Gerould, 1913:392-395. Phascolosoma improvisum.—Gerould, i9i3:395-396.-Wesenberg-Lund, 1930:32-34. Golfingia improvisa.—Wesenberg-Lund, 1955a: 11.-Stephen and Edmonds, i972:i45.-Edmonds, 1976:222-224. Phascolosoma cinctum Gerould, 1913:398-400. Golfingia cincta.—Stephen and Edmonds, 1972:137-138. Golfingia sectile Murina, i974a:228-230. DESCRIPTION. Animals of this taxon are similar to N. minutum and N. lilljeborgi but generally smaller (commonly around 5 mm; most are < 10 mm, but up to 55 mm reported). They have a transparent or translucent body wall, are widespread in deep water, and are dioecious (Fig. 20). The introvert is shorter than the trunk, with a few short tentacular lobes, and the scattered hooks are 20-30 |xm tall. This species often lives in arenaceous foraminiferan tests, small polychaete tubes, or scaphopod shells; larger shelter dwellers may have enlarged and darker posterior papillae (Fig. 20B). Nephasoma diaphanes is often the most common sipunculan in deep-sea communities (E. Cutler and Cutler, 1987b). Immature members of other species are easily mistaken for this species, so the literature has some unfortunate but unavoidable zoogeographical "noise." 0 DISTRIBUTION. Cosmopolitan (as far north as 82 N in the Atlantic) in cold water, most from bathyal and abyssal depths (down to 5300 m).
94
The Golfingiids
Nephasoma diaphanes corrugation N. Cutler and Cutler, 1986 Nephasoma diaphanes corrugatum N. Cutler and Cutler, 1986:558. Golfingia schuettei.—Murina, 1964^238-242; I978:i24.-E. Cutler and Cutler, i98ob:453; 19800:204. DESCRIPTION. Pear shaped to cylindrical; trunk usually 5-10 mm long (occasionally 20-30 mm). The skin is tan to grayish brown, translucent to opaque, with irregular, wavy, zigzag longitudinal epidermal ridges on the introvert base and the anterior part of the trunk. Often the papillae on the posterior end are darker than the surrounding skin. The introvert is usually about as long as the trunk (ranging from 50 to 150%) and bears small (2030 jjim), scattered, pale, triangular hooks. The tentacular crown consists of six to eight short lobes plus two longer dorsal tentacles. The ventral pair of retractor muscles originate near the posterior end (75-85% of the distance to the end) in small worms (<4 mm) but in the middle (50-70%) in larger ones. The weakly developed spindle muscle ends within the coil and does not extend onto the rectum. DISTRIBUTION. Broad latitudinal range from the Atlantic and Pacific oceans, plus the Mediterranean and Red seas. Collected at depths ranging from 80 to 5900 m, most > 1000 m.
Nephasoma eremita (Sars, 1851) Sipunculus eremita Sars, 1851:197. Phascolosoma eremita.—Selenka et al., i883:35-36.-Theel, 1905:72-74. Golfingia eremita.—Stephen and Edmonds, I972:i4i-I42.-E. Cutler, 1973:150-152.-E. Cutler and Cutler, i98oc:202-204.-N. Cutler and Cutler, 1986:559.-Frank, 1983: 16-17. Phascolosoma eremita scabra Gerould, 1913:387-388. Golfingia eremita scabra.—Stephen and Edmonds, 1972:142. Phascolosoma eremita australis Benham, 1922:17-18. Golfingia eremita var. australe.—Wesenberg-Lund, 1963:111.-Stephen and Edmonds, 1972: I4.-Murina, 19743:234. Golfingia eremita californica Fisher, 1952: 396-397.-Stephen and Edmonds, 1972:142. Sipunculus (Phascolosomum) borealis de Quatrefages, i865b:620. Phascolosoma boreale.—Keferstein, i865b:437-438.-Koren and Danielssen, 1877:134. Phascolosoma digitatum Theel, i875b:ii; 1905:72. Golfingia elachea Fisher, 1952:399-400. DESCRIPTION. This appears to be one of the few hookless Nephasoma species. If only juveniles have hooks, however, as is the case in some other
Genus Nephasoma
95
sipunculans, those individuals might have been misidentified as belonging to some other species. A study of the juvenile stages of this species would be instructive. Mature worms have a stocky, nonpapiUated trunk, often rugose, with transverse grooves in the thick body wall (Fig. 19A), and the tentacles are well developed. DISTRIBUTION. Frequently collected in small numbers in disjunct regions in the Arctic and North Atlantic oceans, present in the South Atlantic and Antarctic, rare in the eastern Pacific, from cold water and bathyal depths (20-2000 m).
Nephasomafiliforme(Sluiter, 1902) Phascolosoma filiforme Sluiter, 1902:37-38. Golfingia filiformis.—Stephen and Edmonds, 1972:143. NephasomafiliformeN. Cutler and Cutler, 1986:560. Phascolosoma mucidum Sluiter, 1902:40. Golfingia mucida.—Stephen and Edmonds, 1972:150. DESCRIPTION. The three known N. filiforme specimens vary, especially in the form of the papillae on the two ends of the trunk. Only one worm has long, hairlike papillae on the front end, and calling the posterior papillae mushroomlike is an oversimplification. According to Thompson (1980b), the anus and nephridiopores are on the introvert, and Sluiter (1902) reported the introvert length to be half that of the trunk. The confusion results from the fact that the circular muscles in the anterior part of the trunk and the proximal part of the introvert are strongly contracted, a situation that has caused confusion in descriptions of N. marinki also (see E. Cutler and Murina, 1977). The preceding definition of the trunk-introvert junction resolves the problem. According to that definition, the trunk in this worm is 40 mm long (not 60 mm), and the introvert is 1.2 times as long as the trunk. In the other two type specimens (trunk lengths 15 and 45 mm) the introvert is about 0.8 and 0.3 times the trunk length, respectively. The collection of more specimens would put this species on a firmer foundation. DISTRIBUTION. Off Indonesia at 1788 m. Nephasomaflagriferum(Selenka, 1885) Phascolosoma flagriferum Selenka, i885:i3-i6.-Sluiter, 1900:12.Gerould, 1913:391-392. Golfingia flagrifera.—Murina, 1968^196.Stephen and Edmonds, I972:i44.-E. Cutler, 1973:153-155; 1977a:
96
The Golfingiids
142-143.-E. Cutler and Cutler, 19805:453. Nephasoma flagriferum.— N. Cutler and Cutler, 1986:561.-Saiz, 1993:65. DESCRIPTION. The large vesicular, bulbous papillae on the posterior end of the trunk and the distinct caudal appendage (5-10% of the trunk length) make this species easy to identify (Fig. 19E, F). N. Cutler and Cutler, 1986, includes an appendix with comparative morphological information on 27 worms ranging in trunk length from 3.5 to 120 mm. The introvert length is about equal to the trunk length, and this is another of the few Nephasoma species without hooks. About 16 normal tentacles are present. DISTRIBUTION. An abyssal species (2500-5300 m) with a few records up to 1500 m. Common in the North Atlantic, present in the South Atlantic and the Pacific. Nephasoma laetmophilum (Fisher, 1952) Golflngia laetmophila Fisher, I952:397~399.-Stephen and Edmonds, 1972:148. Nephasoma laetmophilum.—N. Cutler and Cutler, 1986:561. DESCRIPTION. The single bathyal California specimen has many characters in common with the Atlantic species N. abyssorum. The many tentacles (40) and the "strong" wing muscle may be either important characters or artifacts of this animal's large size (39 mm). One striking difference is the nature of the hooks, which are spinelike and have a cortical layer that can be easily rubbed off. The absence of other records does raise concern about the validity of this construct, especially since it is based on a single worm. DISTRIBUTION. Off southern California, 1900 m. Nephasoma lilljeborgi (Danielssen and Koren, 1880) Phascolosoma lilljeborgii Danielssen and Koren, i88o:463-464.-Th6el, 1905:79-80. Golflngia lilljeborgi.—Wesenberg-Lund, 1954^9-10.Stephen and Edmonds, I972:i48.-Gibbs, 1982:121-122. Nephasoma lilljeborgi.—N. Cutler and Cutler, 1986:561.-Saiz and Villafranca, 1990:1158.-Saiz, i993:78-79Onchnesoma glaciale Danielssen and Koren, 1880:464. Phascolosoma glaciale.—Roule, i896:474.-Th6el, 1905:80-81. Golflngia glacialis. —Stephen and Edmonds, I972:i44.-Gibbs, 1982:119-120. Nephasoma marinki Pergament, i94o:i-3.-Stephen and Edmonds, 1972: 214-215.
Genus Nephasoma
97
DESCRIPTION. Very little differentiates this taxon from N. diaphanes or the hermaphroditic N. minutum, especially if gametes are not present in the coelom. Worms may be up to 30 mm long, but most are less than 15 mm, and all are more opaque than N. diaphanes and N. minutum. They have been collected from deeper water than N. minutum and do not live in foraminiferan tests, as many N. diaphanes do. The posterior end of the trunk may come to a blunt point or may have a nipple on a hemispherical base. This worm has a smooth, white to pale gray, slender trunk and reduced tentacles (two dorsal tentacles plus six lobes). The hooks are small, scattered, and triangular. 0 DISTRIBUTION. Far northeastern Atlantic Ocean (79-82 N) from bathyal depths. Recent records near Gibraltar (34-360 N, 6-8° W) were reported "with minor reservations" (Saiz and Villafranca, 1990:1158); if accurate, they significantly extend the range. Earlier reports from this more southern area have been found to be misidentified N. capilleforme, and it is possible that the same mistake was repeated (see N. Cutler and Cutler, 1986).
Nephasoma minutum (Keferstein, 1862) Phascolosoma minutum Keferstein, i862b:4o.-Stephen, 1934:167-168. Petalosoma minutum.—Selenka et al., 1883.-129.-Pau!, 1909:1-50. Golfingia minuta.—Akesson, i958:33-46.-Stephen and Edmonds, 1972:149-iso.-Gibbs, 1973:73-86; I977b:i6. Nephasoma minutum. —N. Cutler and Cutler, i986:562.-Saiz, 1993:74-77. Phascolosoma sabellariae Th6el, 1905:81. Phascolosoma improvisum TMel, i905:82-83.-Wesenberg-Lund, 1939a: 22. Golfingia improvisa.—Stephen and Edmonds, 1972:145. Phascolosoma anceps Th6el, i905:84-86.-Wesenberg-Lund, 1925:90. DESCRIPTION. Trunk is smooth, cylindrical, and up to 15 mm long. The introvert is tipped with two short dorsal tentacles plus two to six variably formed lobular projections. Simple hooks are few in number and may be totally absent in adults (Fig. 21D). The present restricted definition includes only animals from shallow water in the northeastern Atlantic Ocean that are hermaphroditic (see Paul, 1910; Akesson, 1958; and Gibbs, 1973). It is often difficult to differentiate among several populations (see my note following the key to Nephasoma, above), and it is likely that this name has often been used as a taxonomic wastebasket. The present definition still includes the N. impro-
98
The Golfingiids
visa morph, which has larger, darker papillae than the more common morph. DISTRIBUTION. North Atlantic Ocean (Sweden to Great Britain); from low tide depth to 50 m; in mud and sand or crevices. Nephasoma multiaraneusa (Murina, 1967) Golfingia multiaraneusa Murina, 1967c:I332-I333.-Stephen and Edmonds, 1972:151. Nephasoma multiaraneusa.—N. Cutler and Cutler, 1986:562. DESCRIPTION. The hooks are the unique attribute of this species based on a single worm. They are 15-30 |xm tall with a series of radiating filaments from the base that give each hook a spiderlike appearance (Fig. 21E).
The single 2-mm specimen is not a solid basis for a species, especially since the habitat in which it was collected is so unusual for this genus. The status of this very small individual should be reconsidered if future collections in this region do not yield additional material. DISTRIBUTION. Cuba, at 4 m. Nephasoma novaezealandiae (Benham, 1904) Phascolosoma novae-zealandiae Benham, 1904:301-303; 1909:82. Golfingia novae-zealandiae.—Edmonds, 1960:162-163. Golfingia novaezealandiae.—Stephen and Edmonds, 1972:151. Nephasoma novaezealandiae.—N. Cutler and Cutler, 1986:562. DESCRIPTION. Trunk length ranges from 25 to 235 mm; the introvert is shorter than the trunk and bears a large number (often >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 (<50 mm long) that commonly inhabit empty mollusk shells. See Figures 26-32. TYPE SPECIES. Sipunculus strombus Montagu, 1804. Morphological Characters of Phascolion Holdfast (Attachment) Papillae. Epidermal papillae in the mid or posterior region of the trunk may form these hardened structures, which are not uniform in size, shape, or distribution within a species (Th6el, 1875b; Wesenberg-Lund, 1929; E. Cutler and Cutler, 1985a). The genetic potential for holdfast production appears to be modified by environmental fac-
Genus Phascolion
109
Figure 26. Phascolion, external forms of subgenera. A. P. (Phascolion) strombus with protruding esophagus. B. P. (Lesenka) cryptum. C. P. (Montuga) lutense with gray anterior end. D. P. (Villiophora) cirratus. Abbreviations as in Figure I.
tors such as the physical nature of the shelter (Gerould, 1913), the availability of certain chemical elements (e.g., iron; see Gibbs, 1985), and the material deposited on the inside of the shell (Hylleberg, 1975). The ontogenetic stage of the specimen is also important. No young juvenile Phascolion has been reported with hardened holdfasts. Holdfasts are not developed in P. strombus that are 1 or 2 mm long, but they begin to be seen in 3- or 4-mra worms. The presence, number, form, and distribution of the holdfasts, even within a single species, are very difficult to quantify. Three general conditions exist. (1) A few species have no large glandular papillae in the midsection of the trunk (e.g., P. lutense; see Figs. 26C and 28D). (2) Some species have large, glandular papillae which appear as flattened spheres but have no horny deposits around their borders (e.g., P. tuberculosum; see Fig. 29A, B). (3) Most species have glandular papillae, and a few to many papillae secrete a hardened pale brown to black border, sometimes with a tooth or spine (Figs. 28, 29).
no
The Phascolionids
Figure 27. Phascolion internal arrangement.(X) General pattern, as shown by P. strombus: single nephridium and irregular intestinal loops; esophagus is partially hidden under ventral retractor muscle; rectum is cut (after Th6el, 1905)^) Posterior trunk of P. (P.) medusae showing large dorsal retractor originating very close to end of trunk (after E. Cutler and Cutler, 1980a, courtesy of the Institut Oceanogrdfico).(£^ Introvert retractor muscles and esophagus of Phascolion subgenera (from E. Cutler and Cutler, 1985a, courtesy of the Biological Society of Washington) .<(C)F. (Phascolion), ventral muscle considerably thinner than dorsal. (D) P. (homya), dorsal and ventral muscles approximately equal size(E) P. (Montuga), muscles partially fused, esophagus leaving before split, fg) P. (Lesenka) and P. (Villiophora), completely fused retractor column. Abbreviations as in Figure 1.
Genus Phascolion
in
Figure 28. Scanning electron micrographs of Phascolion skin and holdfast papillae (from E. Cutler and Cutler, 1985a, courtesy of the Biological Society of Washington). A. P. strombus from gastropod shell, with V-shaped holdfasts on upper right coil and epizoans on posterior end (scale line = 1 mm). B. Holdfast papilla of P. strombus (scale line = 20 u,m). C. Ventrolateral section of P. strombus showing variety of sizes and shapes (scale line = 1 mm). D. Skin of P. lutense showing absence of holdfast papillae. E and F. P. caupo's large holdfast papillae from different angles (scale line = 0.1 mm). G. P. collare holdfasts with o, I, and 2 teeth on papillae (scale line = 0.1 mm).
112
The Phascolionids
Figure 29. Scanning electron micrographs of holdfast papillae viewed from different angles. A and B. P. tuberculosum with bulbous nonhardened papillae. C and D. P. hedraeum papillae with border slightly proteinized. Scale = 200 u,m. (From E. Cutler and Cutler, 1985a, courtesy of the Biological Society of Washington.)
Introvert Retractor Muscles. Larval Phascolion exhibit two pairs of introvert retractor muscles (Akesson, 1958). Early in their ontogeny the left and right members of each pair (dorsal and ventral) fuse together for some part of their length, giving the appearance of only one or two muscles. One useful attribute is whether these fused muscles are of equal or unequal size. In some species the ventral muscle is slender, the dorsal being 2.5-10 times thicker. This difference appears only in worms more than 2 mm long; younger ones have retractors of equal size. It is easy to overlook the ventral retractor when it is thin (as in P. strombus) and erroneously conclude that only one muscle is present. The retractors are especially difficult to see when the worm is contracted and only 1-2 mm of the muscle is visible. The thin ventral retractor may
Genus
Phascolion
Figure 30. Phascolion introvert hooks (after E. Cutler and Cutler, 1985a, courtesy of the Biological Society of Washington). A. P. strombus (type I; scale = 100 u-m). B. P. microspheroidis (type I; scale = 20 (uun). C. P. bogorovi (type I; scale = 200 /xm). D. P. ushakovi (type I; scale = 200 urn). E. P. convestitum (type II; scale = 50 pin). F. P. tuberculosum (type II; scale = 50 pm). G. P. pharetratum (type II; scale = 50 pm; after Sluiter, 1902). H. P. collare (type III; scale = 50 pm). I. P. lucifugax (type III; scale = 50 (im). J. P. medusae (type III; scale = 50 pm).
114
The Phascolionids
be mistaken for a spindle or fixing muscle, and it is possible to destroy it during dissection. The ventral retractor origins are generally posterior to and slightly to the left of the nerve cord, although they occasionally are located anteriad, on the midline, or both. One must be especially careful during dissection to avoid damage to this fragile muscle. Esophagus Relative to Retractor Muscles. The esophagus comes from the mouth and follows the retractor muscle column for some distance before separating and going into the intestinal coil or loops. The point at which this separation occurs in relation to the fusion point of the retractors is a reference point at the subgeneric level (Fig. 27C-F). Contractile Vessel. This thin tube is generally about one quarter the diameter of the esophagus. P. cirratum is the only Phascolion with true villi. A few other species exhibit folds or vesicular pouches along some portion of the tube, but not villi. The size of the vessel and the extent of folding or vesicle formation seem to be correlated with the number of tentacles. Introvert Hooks. Most Phascolion species have scattered hooks on the distal introvert. A few individuals in any population may lack hooks (E. Cutler and Cutler, 1985a). A few "advanced" species, all with completely fused retractor muscles {P. cirratum, P. cryptum, P. hupferi, P. rectum, and P. valdiviae sumatrense), lack hooks as adults. Three general types of hooks exist, and they can facilitate species identification. Type I hooks (20-250 (xm) have been called claws or spines (Fig. 30AD). They have pointed, nonrecurved tips, and many have narrow bases. These are found on P. bogorovi, P. hedraeum, P. lutense, P. microspheroidis, P. pacificum, P. strombus, P. ushakovi, and P. valdiviae. Type II hooks (40-220 \xm) are broad based and heavy, with a recurved, pointed tip (Fig. 30E-G). They also show an internal light triangle when viewed under the light microscope. These are found on P. convestitum, P. hibridum, P. pharetratum, and P. tuberculosum. Type III hooks (20-70 (xm) are also broad based and recurved but have a round tip (Fig. 30H-J). They are present on P. abnorme, P. caupo, P. collare, P. lucifugax, P. medusae, P. megaethi, and P. robertsoni. Tentacular Crown. Four general types of tentacular crowns exist in Phascolion:
Genus
Phascolion
115
Figure 31. Phascolion tentacular crowns. A. Normal array from P. tuberculosum (after Thtel, 1905). B. P. medusae with about 50 thin tentacles (from E. Cutler and Cutler, 1980a, courtesy of the Institut Oceanogrifico). C. Distal tip off. cryptum showing the four primary tentacles and auxiliary tentacles on swollen part of introvert (from Hendrix, 1975, courtesy of Smithsonian Institution Press).
1. No distinct tentacles and only a few (
n6
The Phascolionids
oi y
,fA
'
i. Separate dorsal and ventral retractor muscles; esophagus continues along one of these, posterior to subdivision 2 - Retractor muscles fused for most or all of length; esophagus separates from retractor before any subdivision 3 2. Dorsal and ventral retractors of equal size (Fig. 27D); holdfasts weakly proteinized, if at all Subgenus Isomya - Ventral retractor muscle much thinner man dorsal (one-tenth to one-half; Fig. 27C); many with distinct proteinized borders on holdfast papillae Subgenus Phascolion s. s. 3. Fusion of retractor muscles incomplete, with three, rarely four, separate origins visible (Fig. 27E) Subgenus Montuga - Retractors fused into single column, but cleft in origin sometimes apparent (Fig. 27F) 4 4. Contractile vessel villi present; >40 tentacles
Subgenus Villiophora
- Contractile vessel villi absent; <30 tentacles
Subgenus Lesenka
Subgenus Phascolion (Isomya) E. Cutler and Cutler, 1985a Retractor column divided for most of its length. Esophagus detaches from retractor column posterior to the first separation of the retractor muscles. The diameters of dorsal and ventral retractor muscles are equal or nearly so. TYPE SPECIES. Phascolion tuberculosum Theel, 1875. DIAGNOSIS.
Key to Subgenus Phascolion (Isomya) Species 1. Anus at mid-introvert; no holdfast papillae
P. gerardi
- Anus at anterior of trunk; holdfast papillae present (may be weakly developed) 2
2. Holdfast papillae large but without proteinized borders
3
- Holdfast papillae with weak borders of hardened protein
5
3. Hooks 25-50 p,m, slightly recurved, sharply pointed (Fig. 30B); tentacles absent or reduced P. microspheroidis - Hooks >55 u,m, well-developed tentacles present
4
Genus Phascolion
117
4. Hooks 70-220 jxm, broad, recurved; 10-30 tentacles (Fig. 29A, B) P. tuberculosum - Hooks 60-70 u,m, blunt, strongly curved (Fig. 30I); >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 <4 mm; not living free in sand; holdfast papillae present, some-
126
The Phascolionids
times without hardened borders; anus at anterior trunk
2
2. Slender, digitiform tentacles, usually more than 35
3
- Broad-based, tapering tentacles, usually fewer than 35
4
3. U-shaped, proteinized holdfast papillae
P. robertsoni
- Bulbous holdfast papillae without hardened borders
P. medusae
4. Hardened holdfast papillae absent
5
- Hardened holdfast papillae present
7
5. Tall, spinelike type I hooks (Fig. 30D) - Broad-based type II hooks
P. ushakovi 6
6. Anterior of trunk with large, compact papillae, usually hardened; no helical coil in gut, loops only P. hibridum - Anterior of trunk without hardened papillae; helical coil present in gut (Fig. 30D) P. pharetratum 7. Hardened border of holdfast composed of discontinuous, granular units (Fig. 30C) P. bogorovi - Hardened border of holdfast as continuous, smooth margin
8
8. Hooks clawlike, pointed (type I)
9
- Hooks curved, bluntly rounded (type III)
10
9. Ventral retractor less than half dorsal width, origins usually at different anterior or posterior levels; anterior papillae with single tips (Fig. 28A-C) P. strombus strombus - Ventral retractor half to three-fourths width of dorsal, at same level; anterior papillae with one to four tips P. strombus cronullae 10. Holdfast papillae few and entirely covered by cone of hardened protein (Fig. 28E, F) P. caupo - Holdfast papillae with thin border of hardened protein; no cone
11
11. U-shaped holdfast papillae; ventral retractor origin anterior to dorsal P. abnorme - V-shaped holdfast papillae on posterior tip of trunk; ventral retractor origin posterior to dorsal P. megaethi Phascolion abnorme W. Fischer, 1895 Phascolion abnorme W. Fischer, i895:i69-i7o.-Stephen and Edmonds, I972:i69-I70.-E. Cutler and Cutler, 19853:822.
Genus Phascolion
127
Phascolion heteropapillosum Wesenberg-Lund, 1963:135-138.-Stephen and Edmonds, 1972:177-178. DESCRIPTION. This uncommon species has hardened holdfast papillae, 10-30 tentacles, and rounded, recurved, type III hooks. The intestine forms a spiral and loops. DISTRIBUTION. Off South Africa, in the Gulf of Aden, and the Red Sea at 30-180 m.
Phascolion bogorovi Murina, 1973 Phascolion bogorovi Murina, i973a:66-68.-E. Cutler and Cutler, 1985a: 823. DESCRIPTION. The single specimen is 28 mm long and has large (200250 |xm), slender, black hooks (Fig. 30C). The holdfast papillae have granular protein deposits, sometimes discontinuous, appearing as one to four "teeth" on some posterior papillae. The anterior end of the trunk is dark with large, clear, lemon-shaped papillae. The dorsal retractor is two or three times wider than the ventral, and the gut has both loops and coils. This individual resembles P. strombus except for the large, slender hooks and granular holdfast papillae. DISTRIBUTION. Peru-Chile Trench, at 3960 m.
Phascolion caupo Hendrix, 1975 Phascolion caupo Hendrix, I975:i33~i35.-E. Cutler and Cutler, I985a:824.-Saiz and Villafranca, 1990:1160-1161.-Saiz, 1993:96-98. DESCRIPTION. The introvert, about equal to the trunk in length, bears type III hooks (20-35 V*m tall). The cone-shaped holdfast papillae are dark, sparse (as few as 12 in a narrow band), and tall; when pressed flat they appear elongate (Fig. 28E, F). Some papillae on small worms are transparent. The dorsal muscle is five to seven times broader than the ventral one, which is easy to overlook since the dorsal may obscure it. The thin ventral muscle has two short origins just posterior to the end of the ventral nerve cord. In other ways the internal anatomy is like that of P. strombus. DISTRIBUTION. Originally collected from the southeastern United States at intertidal to shelf depths. The recent record of nine worms collected off southern Spain at 540-1380 m is a major extension of this known range.
128
The Phascolionids
Phascolion hibridum Murina, 1981 Phascolion hibridus Murina, 198^:348-349.-E. Cutler and Cutler, 19853:828. DESCRIPTION. The larger dorsal retractor is incompletely fused, and the broad-based type II hooks are pale and about 40 u,m tall. The mid-trunk is smooth and lacks holdfast papillae. The large, dark, mammiform, singletipped papillae on the anterior end of the trunk may give the false impression of a shield. DISTRIBUTION. Malaysia and Samoa at 1500-2380 m.
Phascolion medusae E. Cutler and Cutler, 1980 Phascolion medusae E. Cutler and Cutler, 19803:2-4; 19858:830. DESCRIPTION. The known representatives of this species are 2-20 mm long and have about 50 filamentous tentacles at the end of an introvert that is about equal in length to the trunk. The dorsal retractor originates posterior to the ventral, very close to the posterior end of the trunk. The unique 50-p.m introvert hooks (Fig. 30J), many slender tentacles, and large mushroom- or wartlike holdfast papillae without distinct borders are diagnostic. Most of the ventral retractor muscle is covered by the attached esophagus. The gut lacks coils, the anus is anterior to the nephridiopores, and the contractile vessel is vesicular. A number of similarities exist between P. medusae and P. robertsoni. DISTRIBUTION. Southern Brazil, at 170-338 m.
Phascolion megaethi E. Cutler and Cutler, 1979 Phascolion megaethi E. Cutler and Cutler, 19798:961-964; 19853:830. DESCRIPTION. The anterior trunk papillae of these 4-12-mm worms are 100-150 |xm tall and dark red. On casual observation the pspillae form 3 shieldlike 3rray. The introvert carries fewer than 15 tentacles. The gut lscks coils. This species is distinguished from other P. strombus-like members of this subgenus by the fused ventral retractor muscle, which originates posterior to the larger dorsal; the large, red snterior trunk pspillse; the smooth trunk (except for a few small, V-shaped holdfasts at the posterior tip); and its few blunt type III hooks, which are 30-35 u,m tall. DISTRIBUTION. Southern Madsgsscsr; intertidal, inhabits empty gastropod shells.
Genus Phascolion
129
Phascolion pharetratum Sluiter, 1902 Phascolion pharetratum Sluiter, I902:3i~32.-Stephen and Edmonds, I972:i86.-E. Cutler and Cutler, 19793:964; 19853:831. DESCRIPTION. Even though these worms live in gastropod shells they lack hardened holdfast papillae. The shape of the large, bent, dull, dark brown hooks is unique (Fig. 30G). The tentacles are filamentous. The introvert retractor muscles originate well anterior to the posterior end of the trunk. The intestinal coils form a regular spiral. DISTRIBUTION. Indonesia and southern Madagascar, from 1-91 m. Phascolion psammophilus Rice, 1993 Phascolion psammophilus Rice, 1993^594-599. DESCRIPTION. This species is based on careful study of more than 200 worms from a single population. The total length of expanded worms ranges from 1.5 to 7 mm (average, 4 mm), and the introvert is 1-2.4 (average, 1.7) times the trunk length. This means that the trunk is commonly only about 2 mm long. There are two to eight tentacles; the number depends on the size of the worm. The bluntly pointed, curved hooks appear large but are only about 30 u,m tall (i.e., small for this genus); they give the impression of being in one to four irregular rings. A ciliated pad on the dorsal tip of the introvert that is visible with a scanning electron microscope is probably the nuchal organ. Although no holdfast papillae are present, some of the trunk papillae do have a knob or cap at the apex. Other papillae have up to three apical pores. The retractor muscles originate from the same level very near the posterior end of the trunk. The intestine is not coiled and is attached to the body wall by a few fine fixing muscles. A caecum is present at the beginning of the long rectum, and the anus is located on the introvert about 20% of the distance toward the tip—unique in this subgenus. Just anterior to the nephridiopore is a pair of small glandular sacs that open to the exterior via pores. Mature gametes in the coelom affirm the adult and dioecious nature of these diminutive worms. The eggs are slightly elongate, averaging 124 by 111 \xm; when fertilized, they develop into trochophore larvae. These soon become lecithotrophic pelagosphera mat stay near or on the bottom, and within four days these metamorphose into juveniles. DISTRIBUTION. East coast of central Florida; interstitial in sand and shell hash, from 15-20 m.
130
The Phascolionids
Phascolion robertsoni Stephen and Robertson, 1952 Phascolion robertsoni Stephen and Robertson, I952:439~44i.-Stephen and Edmonds, 1972-.187.-E. Cutler and Cutler, 19853:832. DESCRIPTION. About 40 slender tentacles and many small (30-40 |xm), blunt type III hooks are present. The holdfasts are scattered, pale, 100-200 ujn wide, U or V shaped, and associated with large, bulbous papillae. Unique pale papillae with dark, hardened tips are located around the basal part of the introvert. The dorsal retractor is about three times larger than the ventral and originates a few millimeters anterior to the ventral, which is at the posterior end of the trunk. The gut has only loops, no spiral, and the nephridiopore is posterior to the anus. DISTRIBUTION. East and South Africa, at 1-60 m.
Phascolion strombus strombus (Montagu, 1804) Sipunculus strombus Montagu, 1804:74-76. Phascolion strombi.—Theel, 18753:1-7; Stephen and Edmonds, I 9 7 2 : I 8 7 - I 8 9 . - E . Cutler, 1973: i68-i73.-Gibbs, i977b:22-23.-Saiz, 1986^47-49. Phascolion strombus strombus.—E. Cutler and Cutler, I98sa:832.-Saiz and Villafranca, i99o:n62.-Saiz, 1993:98-102. Sipunculus dentalii Gray, i828:8.-Rice and Stephen, 1970:52. Sipunculus bernnhardus Forbes, 1841:251-253. Sipunculus capitatus Rathke, 1843:143-147. Sipunculus caementarius de Quatrefages, 1865^628. Phascolosoma hamulatum Packard, 1867:290. Phascolion spetsbergense Theel, 1875b: 16-17. Phascolosoma tubicola Verrill, 18733:99. Phascolion tubiculum Stephen and Edmonds, 1972:190-191. Sipunculus concharum Oersted, 1844:80. Phascolion alberti Sluiter, 1900:9-io.-Stephen and Edmonds, 1972:170171. Phascolion artificiosus Ikeda, 1904:18-20.-8316, 1939:413. Phascolion artificiosum.—Stephen 3nd Edmonds, 1972:171-172.-E. Cutler and Cutler, 1981:70-71. Phascolion mogadrense Sluiter, 1912:18-19. Phascolosoma intermedium Southern, 1913:3-5. Phascolion intermedia Gibbs, 1977a: 109-112. Phascolion africanum W. Fischer, I923a:5.-Stephen and Edmonds, 1972:
Genus Phascolion
131
170. Phascolion strombi africanum E. Cutler and Cutler, 1979^:964965; 1980c: 196. Phascolion brotzkajae Murina, i964c:68-70.-Stephen and Edmonds, 1972:172. Phascolion tortum Edmonds, 1976:218-222. Phascolion anomalus Murina, 1981^349-352. DESCRIPTION. The holdfast papillae have a variably shaped, hardened protein border (Fig. 28A-C). Sharp, clawlike, type I hooks (Fig. 30A) and 10-30 well-developed tentacles are usually present on the introvert, which is up to twice as long as the trunk. Some worms lack hooks, perhaps as the result of predation and regeneration of the introvert. There is usually an aggregation of large papillae around the anterior end of the trunk. The trunk length may reach 30-40 mm but is more commonly 5-20 mm (Fig. 26A). The ventral retractor is one-fourth to one-half the diameter of the dorsal and commonly straddles the ventral nerve cord near its posterior end. The intestine is in loose loops without a spiral. This species is very widespread and common, and many authors have discussed its extreme plasticity of form (e.g., Theel, 1875a, 1905; Gerould, 1913; W. Fischer, 1923a; and E. Cutler and Cutler, 1987b). At least two morphs are present in certain populations; these differ in holdfast shape, hook size, and place of origin of the ventral retractor. This species inhabits a wide variety of shelters, including mollusk shells, polychaete tubes, bone fragments, and clay tubes, and this may partially explain the different external morphologies. DISTRIBUTION. Very common and eurytopic in the North Atlantic and Arctic oceans, most numerous between 200 and 2000 m. It is also found in deep water in the Caribbean. There are scattered records from the Mediterranean, Red Sea, Gulf of Aden, Madagascar, and South Africa; two Antarctic records; and records from Argentina and Chile. Other Pacific Ocean records come from the South Pacific, New Zealand, and off Japan. It is known from depths of 1-4030 m. Phascolion strombus cronullae (Edmonds, 1980) Phascolion cronullae Edmonds, 1980:30-32. Phascolion strombus cronullae.—E. Cutler and Cutler, 19853:835. DESCRIPTION. About 25% of the anterior trunk papillae have two, three, or four tips or points, but most have a single point like that found in P. strombus. The dorsal retractor muscle is 1.5-2 times the size of the
132
The Phascolionids
ventral and originates at about the same level very near the posterior end of the trunk. Hooks, holdfast papillae, and other characters match those of the nominate form, but geographical isolation and the differences in retractor and papillae morphology set this subspecies apart. DISTRIBUTION. New South Wales, Australia, from gastropod shells in shallow water. Phascolion ushakovi Murina, 1974 Phascolion ushakovi Murina, I974c:284.-E. Cutler and Cutler, 1985a: 837DESCRIPTION. The distinctive characters of this species are the many tall, black, spinelike hooks (Fig. 30D); the very thin ventral retractor muscle (one-fifth to one-tenth the size of the dorsal); and the papillae. On both ends of the trunk are large, dark, mammiform papillae that resemble those of P. tuberculosum, but there are no holdfast papillae in the midtrunk, only flattened skin bodies. The gut coil is attached by several fixing muscles. The posterior muscle, which comes from inside the gut coil and has a large diameter, is not to be confused with a spindle muscle. DISTRIBUTION. Western Australia, at 330 m. Subgenus Phascolion (Villiophora) E. Cutler and Cutler, 1985 DIAGNOSIS. Retractor muscles completely fused over the whole length to give an entire retractor column. Contractile vessel with numerous distinct, true villi. TYPE SPECIES. P. cirratus Murina, 1968.
Phascolion (Villiophora) cirratum Murina, 1968 Phascolion cirratus Murina, 19680:1724; 19713:82. Phascolion (Villiophora) cirratum.—E. Cutler and Cutler, 19853:824. DESCRIPTION. The numerous tentacles appear branched, and numerous digitiform contractile vessel villi are present. These two characters are functionally linked as an adaptation to the low oxygen tension in the shallow, warm waters of the Red Sea (i.e., they increase the surface area for external and internal gas exchange). If the nephridiopore is used to mark the base of the introvert, the anus is located about 90% of the
Genus Onchnesoma
133
distance toward the tentacular crown. Although rugose, the trunk lacks hardened holdfast papillae and has a single fused retractor muscle (Fig. 26D). DISTRIBUTION. Red Sea and Arabian Gulf, at 1-70 m.
Genus Onchnesoma Koren and Danielssen, 1875 Onchnesoma Koren and Danielssen, 1875:133; i877:i42.-Selenka et al., i883:i30.-Theel, 1905:13.-Stephen and Edmonds, I 9 7 2 : I 6 I . - E . Cutler and Cutler, 19853:840. DIAGNOSIS. Small, trunk less than 10 mm long; introvert much longer than trunk. Body wall with continuous muscle layers. Fewer than 10 tentacles arranged around mouth, but tentacles may be reduced in size or entirely absent. Introvert retractor muscle system almost completely fused to form single retractor muscle column. Anus on distal half of introvert. Contractile vessel rarely apparent, without villi. Spindle muscle apparently absent. One nephridium. See Figures 33 and 34. TYPE SPECIES. Onchnesoma steenstrupii Koren and Danielssen, 1875.
Morphological Characters of Onchnesoma Introvert Length and Position of Anus. In this genus the introvert is always longer than the trunk, often many times longer. Accurate measurement of the introvert is possible only if it is completely extended, but that is rarely the case in preserved material. Measuring a contracted introvert results in a deceptively small value. Likewise, it is difficult to accurately measure the position of the anus unless the introvert is fully extended. In O. steenstrupii the anus is located 90-95% of the distance toward the mouth; in other species, 70-85%. Introvert Retractor Muscle. The retractor appears as a single muscle, probably as a result of fusion during early ontogeny. It originates on the posterior end of the trunk (Fig. 33C). Whether fusion is complete, so that there is a single origin (root), or incomplete, giving two origins, may be important to the systematist. The degree of fusion can be determined by carefully opening the posterior end of the trunk. The division between the two origins is much easier to see if the introvert is extended.
134
The Phascolionids
Figure 33. Onchnesoma. A. 0. steenstrupii with oral disc (OD) but no tentacles; anus is near distal tip of introvert. B. O. squamatum with few tentacles and large trunk papillae. C. Interior of O. steenstrupii with single fused retractor muscle and single nephridium. Abbreviations as in Figure 1. (After Th6el, 1905.)
Papillae. The presence, size, and distribution of these epidermal structures are obvious and useful characters for identification. Distinct differences among taxa exist, but there is also some variation within and between populations of the same taxon. In O. steenstrupii the papillae are small (12-18 |xm diameter) and arranged in rows that radiate out from the posterior end forming the "keels" described by earlier authors (Figs. 33A, 34E). In the subspecies O. steenstrupii nudum the keels are only folds in the skin, not papillae (Fig. 34D). Similar nonpapillated keels are found in O. magnibathum, and if the posterior quarter is contracted the ridges are accentuated (Fig. 34A, B). O. squamatum squamatum is uniformly covered with large, irregular papillae that are 80-120 |xm in diameter (Fig. 33B). The papillae are smaller and more scattered in the subspecies O. squamatum oligopapillosum. O. intermedium has ridges posteriorly but bears large papillae similar to those of
Figure 34. Scanning electron micrographs of posterior end of four Onchnesoma taxa. A and B. O. magnibathum in two different states of contraction. C. O. squamatum. D. O. steenstrupii nudum with keels or skin folds but no papillae. E. O. steenstrupii steenstrupii with keels of separate wartlike papillae. Scale = 0.5 mm. (From E. Cutler and Cutler, 1985a, courtesy of the Biological Society of Washington.)
136
The Phascolionids
O. squamatum on the remainder of the trunk. Papillae and keels are helpful in the identification process, but they must be used in conjunction with the entire suite of characters.
Key to Onchnesoma Species i. Trunk with papillae
2
- Trunk without papillae but with radiating folds of skin (keels) on posterior end (Fig. 34A, B) 5 2. Posterior end of trunk with well-defined radiating ridges or keels (Fig. 34E) 3 - Posterior end of trunk without well-defined radiating ridges or keels 4 3. Trunk with large papillae on anterior but not posterior; tentacles present 0. intermedium - Trunk with papillae on posterior, sometimes anterior; oral disk instead of tentacles O. steenstrupii steenstrupii 4. Trunk covered with many large papillae (Figs. 33B, 34C).... 0. squamatum squamatum - Trunk with few small, scattered papillae (may be absent on posterior or midtrunk) O. squamatum oligopapillosum 5. Trunk cylindrical, tapering gradually into narrower introvert (half to one-third trunk diameter); introvert length not more than twice trunk length; found at depths >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 (<30 mm) have fewer than 10; larger worms from the same population usually have more. The difference in number is ontogenetic, not speciesspecific. Similarly, the anastomosing network of the contractile vessel
Genus Themiste
143
sometimes seen around the esophagus is age dependent and rarely developed in smaller worms. Tentacular Crown. The dendritic branching pattern is unique within Sipuncula, and it simplifies identification to the generic level. Determining the number of tentacular "stems" is not always easy, however, and has led to some confusion. E. Cutler and Cutler (1988) defined the terms used to describe the crown as follows (Fig. 37): 1. Stem: the four structures arising from the oral disk 2. Branch: subdivision of a stem (primary, secondary, etc.) 3. Tentacule: the final subdivision or terminal unit 4. Tentacle: the entire array of subunits beginning with one stem plus all its branches and tentacules The basic plan in this genus is four stems, but the stems split at different times during growth in different species, giving rise to two adult patterns: either four or six stems, occasionally five. An early postlarval subdivision of the dorsal pair can result in five or six stems. E. Cutler and Cutler (1988) proposed an increase in complexity (i.e., more branches and more tentacules) of the tentacular crown as the worm increases in size (Fig. 37). In the subgenus T. (Lagenopsis) each of the four stems subdivides into smaller branches one to three times (Fig. 37C, D). Terminal tentacules are produced along the entire length of all branches as well as on the main stems. Tentacule length is consistent within species (T. lageniformis = 2-4 mm; T. cymodoceae = 1-2 mm; T. dehamata = 0.5-1 mm). In the subgenus Themiste s. s., each stem branches dichotomously several times and there are discrete internodes. The dendritic crown of worms less than 15 mm long has fewer branches and shorter internodes than the crown of larger worms. The terminal tentacules are present as clusters near the tips of the terminal branches, and other tentacules are widely spaced along the branches (Fig. 37A, B). This structure is helpful to the systematist only in particular species complexes when the dorsal and ventral stems are not equal in length (i.e., the ventral stems do or do not subdivide at the same place as dorsals). Fixing Muscle Attachments. In Themiste three thin muscles—Fi, F2, and F3—attach the digestive tract to the body wall. In the subgenus T. (Themiste), Fi connects the body wall of the mid-trunk to the esophagus in
144
The Themistids
Figure 37. Left dorsal tentacle from two Themiste species, each a different subgenus, showing size-related changes in branching patterns. A and B. T. (Themiste) hennahi with trunks 25 and 140 mm long. C and D. T. (Lagenopsis) lageniformis with trunks 6 and 30 mm long (scale = 1 mm; from E. Cutler and Cutler, 1988, courtesy of the Biological Society of Washington). E. Relationship of the four stems to the oral disc. Branching may occur near the base on one or two stems, giving an impression of more than four stems (from Gibbs and Cutler, 1987, © The Natural History Museum, London).
the area of the long contractile vessel villi. In T. (Lagenopsis), Fi anchors the esophagus near the posterior part of the trunk where the esophagus turns forward, and may take the form of several threads or a membrane. Muscle F2 generally attaches the posterior esophagus or first gut coil, and F3 is more often connected to the last intestinal coil or the rectum. The precise insertions of F2 and F3 are neither constant nor taxonomically meaningful. Introvert Hooks. In both subgenera some species bear scattered introvert hooks that are dark, hardened, and proteinaceous. Very little is known about the ontogeny of the species lacking hooks as adults. Hooks have been reported on very young T. lageniformis (
Genus Themiste
145
Figure 38. Different sizes and orientations of introvert hooks among Themiste species. A. T. minor minor. B. T pyroides. C. T. variospinosa. Scale = 200 \i.m. (From E. and Cutler, 1988, courtesy of the Biological Society of Washington.) han, 1935; Williams, 1977; Pilger, 1989), but adults are hookless. Also, Rice observed a row of hooks on one-month-old T. pyroides and T. alutacea (Rice, 1967, 1975a). E. Cutler and Cutler (1988) suggested that all juvenile Themiste have hooks that are quickly lost. Some species may never replace these "baby hooks," but others do so later (with "adult hooks") as they mature. This hypothesis needs more testing. Nevertheless, a presence/absence dichotomy in adult worms exists. Hook size increases with trunk size, the upper limit being about 450 p,m in Themiste. The adult hooks are sparse and arrayed over a wide band on the proximal one-third to two-thirds of the introvert (Fig. 38). The number of hooks is partly determined by the environment. Animals that live in areas with high wave energy—such as the open rocky intertidal—have fewer hooks that cover a smaller part of the introvert than other members of the same species from more protected areas or subtidal depths. Trunk Size and Shape. There seem to be two size classes for adults. Worms that inhabit soft substrata commonly have trunks longer than 60 mm, sometimes exceeding 200 mm. Those living in rock or coral crevices rarely exceed 30 mm, except for T. pyroides, which may reach 150 mm. Most small worms have a pyriform shape. Larger worms living in unconsolidated sediments are cylindrical and elongate. Those in rock fissures or coral crevices have stouter and more pyriform bodies. Worms that occupy holes made by boring bivalves take on the shape of the burrow (Fig. 39)-
Genus Themiste
147
Figure 40. Distal introvert of T. dyscrita (left) showing pigmented collar region, and T. hennahi (right) showing unpigmented collar. (From E. Cutler and Cutler, 1988, courtesy of the Biological Society of Washington.) Pigmentation on Tentacles and Introvert. A dark bluish collarlike band is present around the introvert of some species; some others have dark purple or blue patches on the tentacles (Fig. 40). The presence or absence of pigment on the introvert and the tentacules (not branches) of certain species is helpful in species identification. Key to Themiste Subgenera 1. Contractile vessel with few (<2o) long, threadlike tubular extensions (Fig. 36A) Subgenus T. (Themiste) - Contractile vessel with numerous (>40) short digitiform villi (Fig. 36B) . . . . Subgenus T. (Lagenopsis) Figure 39. Contracted and extended states of three Themiste specimens to illustrate how body shape can be influenced by epigenetic factors. A and B. T. dyscrita from vacated pholad bivalve holes in shale. C and D. Same species from burrows in sandstone, probably self-constructed. E and F. T. hennahi from unconsolidated coarse sand. (From E. Cutler and Cutler, 1988, courtesy of the Biological Society of Washington.)
The Themistids
148
Subgenus Themiste (Themiste) Edmonds, 1980 Themiste (Themiste) Edmonds, 1980:33. DIAGNOSIS. Contractile tubules (villi) few (<20), long, and threadlike. TYPE SPECIES. Themiste hennahi Gray, 1828.
Key to Themiste (Themiste) Species 1. Introvert without hooks
2
- Introvert bearing dark, scattered hooks (Fig. 38B)
3
2. Introvert collar purple (Fig. 40); tentacules white; lives in rocks T. dyscrita - Introvert collar unpigmented (Fig. 40); tentacules with pigment spots; lives in unconsolidated sediments T. hennahi 3. Introvert collar unpigmented; tentacules with pigment spots; Atlantic Ocean T. alutacea - Introvert collar purple; tentacules unpigmented; Pacific Ocean
4
4. Tentacular crown appears to have six stems, many subdivisions of branches, tentacules mainly at distal tips T. pyroides - Tentacular crown with four stems, each dividing once to give eight branches, tentacules appear all along branch T. blanda
Themiste alutacea (Griibe and Oersted, 1858) Dendrostomum alutaceum Griibe and Oersted, 1858:118. Themiste alutacea.—Baird, i868:98.-Stephen and Edmonds, 1972-.196-197.-E. Cutler and Cutler, 1988:755-756. Sipunculus (Phymosomum) orbiniensis de Quatrefages, i865b:622. Phascolosoma orbiniense.—Baird, 1868:93. Themiste (Themiste) orbiniensis.—Saiz, 19843:124-132. Dendrostomum petricolum Amor, 1964:463-467. Themiste petricola.— Stephen and Edmonds, 1972:209. Dendrostomum rosaceum Amor, 1964:459. Themiste rosacea.—Stephen and Edmonds, 1972:211-212. DESCRIPTION. Small hook-bearing worms in which the trunk is rarely longer than 25 mm and is commonly less than 15 mm long. In early juvenile stages the worm has a ring of introvert hooks, but these are soon lost and replaced by scattered adult hooks. Young worms have four ten-
Genus Themiste
149
tacular lobes, two long dorsals and two shorter ventrals (Rice, 1975a). Later, two of these stems may subdivide near the base, giving the appearance of six stems (occasionally five) in many adult worms. (In the similar T. blanda, the four primary stems divide into eight more or less equal branches.) The subsequent division of these branches is limited in small worms, and the thin tentacules, with pigment spots, are located all along each branch. The number of hooks in this species can be more than 100, but they are smaller (75-150 am) than hooks found in other members of this subgenus. This species has lecithotrophic pelagic larvae (Rice, 1975c). 0 DISTRIBUTION. Western Atlantic Ocean, from North Carolina (34 N) through the Caribbean to Argentina (42° S), in warm, temperate waters at depths less than 30 m. Inhabits hard substrates (e.g., crevices in coral, oyster beds, or soft rock). Themiste blanda (Selenka and de Man, 1883) Dendrostomum blandum Selenka and de Man, in Selenka et al., 1883:8586.-Sato, 1930:24-28. Themiste blanda.—Stephen and Edmonds, I972:i97.-E. Cutler and Cutler, 1988:756. DESCRIPTION. A small worm with an introvert less than half as long as the trunk and bearing dark hooks. It is very similar to the other two hookbearing members of this subgenus, T. alutacea and T. pyroides. It differs from the former in having four tentacular stems which divide symmetrically into eight, lacking pigment spots on its stouter tentacules, and by living in cool northern Pacific water. It differs from T. pyroides in two ways: (1) the tentacular crown has four stems, each dividing only once (as opposed to dividing two to four times), and the tentacules are longer and occur along each branch, giving the branches a somewhat pinnate appearance; and (2) it is considerably smaller; the upper limit of trunk size is about 25 mm (vs. 200 mm). DISTRIBUTION. Intertidal in Honshu and Hokkaido, Japan. Themiste dyscrita (Fisher, 1952) Dendrostomum dyscritum Fisher, 1952:417-419. Themiste dyscrita.— Stephen and Edmonds, I972:i99.-E. Cutler and Cutler, 1988:752-753. DESCRIPTION. The purple pigment on the smooth collar region and the absence of dark pigment on the tentacules distinguishes this species from T. hennahi, the other hookless member of this subgenus (Fig. 40). Another difference between T. dyscrita and T. hennahi is the subspherical trunk in
150
The Themistids
the former. The nephridiopores commonly open 2 - 3 % of the trunk length posterior to the anus. The retractor muscles usually originate 65-75% of the distance to the posterior end of the trunk. The body color ranges from pale cream in small worms to dark brown in larger ones. DISTRIBUTION. The west coast of the United States, from Oregon to southern California, at intertidal depths (one record at 18 m). T. dyscrita lives in burrows made by other animals, frequently pholad bivalves, in intertidal shales or sandstones (Fig. 39A-D). It does not appear to coexist with the hooked T. pyroides, which may live in the same area but inhabits a different microhabitat. Themiste hennahi Gray, 1828 Themiste hennahi Gray, i828:8.-Rice and Stephen, i970:53-56.-Amor, i97o:495-504.-Stephen and Edmonds, 1972:201-203.-Tarifefto, 1975: 251-266; i976:29-37.-Cutler and Cutler, 1988:753-755.-Haldar, i99i:38-39Sipunculus (Aedematosomum) rapa de Quatrefages, 1865^627. Phascolosoma rapa.—Baird, 1868:86. Dendrostomum ramosum de Quatrefages, 1865^629. Themiste ramosa.— Baird, 1868:98. Dendrostoma peruvianum Collin, 1892:179-180. Dendrostomum peruvianum.—Wesenberg-Lund, 1955a: 12-13. Dendrostoma mytheca Chamberlin, 19203:30. Dendrostoma zostericolum Chamberlin, 19203:30. Dendrostomum zoster icolum.—Fisher, 1952:411-415. Themiste zostericola.—Stephen and Edmonds, 1972:213-214. Dendrostoma perimeces Fisher, i928:i96-i98.-MacGinitie, 1935:681682. Themiste perimeces.—Stephen and Edmonds, 1972:207-209. Dendrostomum lissum Fisher, 1952:419-422. Themiste lissa.—Stephen and Edmonds, 1972:206. Dendrostomum schmitti Fisher, 1952:422. Themiste schmitti.—Amor, 1970:499DESCRIPTION. The trunk may exceed 200 mm, but most animals are 2 5 100 mm long, slender pyriform to cylindrical in shape, sometimes with a nipplelike posterior end (Fig. 39E, F). The retractor muscles usually originate 50-60% of the distance toward the posterior end of the trunk, and the introvert lacks a pigmented collar (see Rice and Stephen, 1970, for illustrations). The tentacular crown is asymmetrical, with the dorsal pair longer and splitting sooner than the ventral pair, giving the appearance of six
Genus Themiste
151
primary stems. The nephridiopores open 0-10% of the trunk length posterior to the anus. In large worms this distance is usually less than 2%. Tarifefio (1975, 1976) gave detailed ecological and behavioral information on a Chilean population. It is probable that animals occupying more optimal niches reach a larger size. This genotype seems to be better suited to higher latitudes; thus the smallest worms come from the Gulf of California, where the population may be isolated and gene flow restricted. DISTRIBUTION. Generally an eastern Pacific Ocean species (Chile and Peru, Gulf of California, and California); inhabiting intertidal gravelly to silty sand, including mudflats, eelgrass beds, and between or under turnable boulders. A surprising record is Haldar's three worms collected under boulders in the Nicobar Islands. It is hard to believe that this Indian Ocean population is really the same species, but no morphological differences can be discerned. Themiste pyroides (Chamberlin, 1920) Dendrostoma pyroides Chamberlin, 19203:31.-Fisher, 1952:406-409. Themiste pyroides.—Stephen and Edmonds, 1972:210.-E. Cutler and Cutler, 1988:756-757. Dendrostoma petraeum Fisher, 1928:195-196. Dendrostoma hexadactylum Sato, 1930:28-33. Dendrostomum hexadactylum.—Fisher, 1952:410-411. Themiste hexadactyla.—Stephen and Edmonds, 1972:203-204. DESCRIPTION. Differs from the two other hooked species in this subgenus (T alutacea and T. blanda) in having a pyriform shape with a bluntly pointed posterior end, regardless of trunk size (Fig. 35A). Another distinguishing character is the presence of four primary tentacular stems that divide close to the base into two, three, or four branches. As the worm grows, these branches continue to subdivide into smaller branches, producing unpigmented tentacules, most at the distal tips. Compared with samesize specimens of T. blanda or T. alutacea, the crown of T. pyroides is much more voluminous and has shorter terminal tentacules. Whereas many specimens from central California have trunks 20-40 mm long, those from the more northern latitudes, such as British Columbia and Hokkaido, are often 40-60 mm, and a few exceed 100 mm. The complexity of the contractile vessel increases with the worm's size (Fig. 36A). In small worms only 8 or 10 long tubules are developed at the terminal end of the contractile vessel, but larger worms (20-25 m m ) n a v e
The Themistids
152
branches off the main vessel adhering to the sides of the esophagus. In still larger worms (40 mm) these contractile vessel branches are more elaborate and surround the esophagus. This network becomes much more complex in 80-mm worms (e.g., like that in Fisher, I952:pl. 29, fig. 3). DISTRIBUTION. Japan (Honshu and Hokkaido) and west coast of North America from southern Alaska to Baja California, at intertidal depths, from crevices in and spaces under rocks.
Subgenus Themiste (Lagenopsis) Edmonds, 1980 Themiste (Lagenopsis) Edmonds, 1980:33. DIAGNOSIS. Contractile vessel villi many (>ioo), short, and digitiform. TYPE SPECIES. Themiste lageniformis Baird, 1868.
Key to Themiste (Lagenopsis) Species 1. Introvert without hooks
2
- Introvert bearing dark, scattered hooks
4
2. Small (trunk <35 mm); introvert with purple collar; lives in hard substrates (Fig. 35B) T. lageniformis - Large (trunk commonly >40 mm); unpigmented introvert collar; lives in sand or mud 3 3. Trunk pyriform; undivided tentacle stems of equal length and <4% of trunk length T. cymodoceae - Trunk elongate, cylindrical; undivided tentacle stems longer (>4_5% of trunk) and of unequal length (dorsal pair longer than ventrals) T. dehamata 4. Introvert hooks oriented posteriorly, 50-100 urn tall
T. minor
- Introvert hooks point in all directions, 30-400 u.m tall (Fig. 38C) T, variospinosa
Themiste (Lagenopsis) cymodoceae (Edmonds, 1956) Dendrostomum cymodoceae Edmonds, 1956:299-301. Themiste cymodoceae.—Stephen and Edmonds, 1972:197-198.-Edmonds, 1980:3840.-E. Cutler and Cutler, 1988:757-758.
Genus Themiste
153
DESCRIPTION. This hookless species is very similar to T. dehamata (e.g., both have pigmented tentacules but unpigmented collars), and the differences are not easily quantified. The trunk length in T. cymodoceae is 5090 mm but less than 5 times the width, and the body is flask shaped or pyriform. T. dehamata is slender and elongate (length at least 10 times the width). A second difference is in the nature of the tentacular crown: In T. cymodoceae the tentacular stems are shorter (2.5-4% of trunk length) and are of equal size, giving a bushy appearance. In T dehamata the stems are longer overall (4.5-7% of trunk length), and the dorsal stems are longer than the ventrals by 25-67%. DISTRIBUTION. South Australia, in unconsolidated sediments among roots in intertidal eelgrass beds.
Themiste (Lagenopsis) dehamata (Kesteven, 1903) Dendrostoma dehamatum Kesteven, 1903:69-73. Dendrostomum dehamatum.—Edmonds, 1956:296. Themiste dehamata.—Stephen and Edmonds, i972:i98-i99.-Edmonds, i98o:34~36.-E. Cutler and Cutler, 1988:758. Dendrostoma ellipticum Sato, 19343:20-22. Themiste elliptica.—Stephen and Edmonds, 1972:199-200. Dendrostomum fisheri Amor, 1964:467-469. Themiste fisheri.—Stephen and Edmonds, 1972:200. DESCRIPTION. Although on paper this hookless species resembles T. lageniformis, T. dehamata is distinct in several ways: It is larger (commonly >40 mm, up to 170 mm), more slender and cylindrical, and it lives in sand or mud. The four bushy tentacles are pigmented to some degree, and the dorsal stems may be longer than the ventral pair. DISTRIBUTION. New South Wales and southern Australia, in intertidal unconsolidated sediments. The single records from Japan and Argentina cannot be verified. Themiste (Lagenopsis) lageniformis (Baird, 1868) Themiste lageniformis Baird, 1868:98-99.-Rice and Stephen, 1970:6667.-Stephen and Edmonds, i972:205-2o6.-E. Cutler and Cutler, i988:758-76o.-Haldar, 1991:40-42. Dendrostoma signifer Selenka and de Man, in Selenka et al., 1883:86-87 (in part). Dendrostomum signifer.—Edmonds, 1956:297.
154
The Themistids
Phascolosoma glaucum Lanchester, 19050:32. Golfingia (Thysanocardia) glauca.—Stephen and Edmonds, 1972:123. Themiste glauca.—Gibbs et al., 1983:302. Phascolosoma pyriformis Lanchester, 1905^39. Golfingia pyriformis.— Murina, 19648:261. Golfingia (Thysanocardia) lanchesteri pro Phascolosoma pyriformis Lanchester, 1905b (preoccupied by Phascolosoma pyriforme Danielssen, in Theel 1875): Stephen and Edmonds, 1972:124. Themiste pyriformis Gibbs et al., 1983:302. Dendrostoma tropicum Sato, 1935:313-315. Dendrostomum tropicum.— Wesenberg-Lund, 1963:131-132. Themiste tropica.—Stephen and Edmonds, 1972:213.-Murina, 1981b: 13. Dendrostoma stephensoni Stephen, 1942:252-253 (in part). Dendrostoma minor.—Chin, 1947:100. Dendrostoma robertsoni Stephen and Robertson, 1952:438-439. Dendrostomum robertsoni.—Wesenberg-Lund, 1963:130. Themiste robertsoni.—Stephen and Edmonds, 1972:210-211. DESCRIPTION. Themiste lageniformis is rarely more than 35 mm long and lacks hooks after the early juvenile stages (Fig. 35B). It has a bluish introvert collar, occasionally very pale, and long tentacules (Fig. 37C, D). This species is the commonest and most widely distributed member of the genus. T. minor huttoni is very similar except that it bears hooks. DISTRIBUTION. Well established in the western Pacific from southern Japan to Australia and Hawaii, and throughout the Indian Ocean. Also recorded from South and Southwest Africa, Cuba, and Florida. It commonly lives in soft rock, old coral, or mussel beds. Themiste (Lagenopsis) minor minor (Ikeda, 1904) Dendrostoma minor Ikeda, 1904:57-59. Dendrostomum minor.—Wesenberg-Lund, 1963:128-129. Themiste minor.—Stephen and Edmonds, I972:207.-E. Cutler et al., 1984:284-285. Themiste minor minor.—E. Cutler and Cutler, 1988:760-761. Dendrostomum fuscum Edmonds, 1960:165-167. Themiste fusca.—Stephen and Edmonds, 1972:200-201. Golfingia coriacea.—Murina, 1972:298. DESCRIPTION. Except for the presence of introvert hooks (generally 5 0 200 |xm tall; Fig. 38A) and a more loosely wound gut coil, animals of this taxon are ecologically and morphologically similar to T lageniformis. The animals are small; trunk length is usually less than 20 mm, often 5-10 mm,
Genus Themiste
155
and 4-mm worms may be sexually mature. The introvert length is about one-third the trunk length, and the four tentacles may or may not have pigment. DISTRIBUTION. Japan, China, South Australia, southern Africa, and one questionable record from southern Argentina. A cool-temperate, intertidal and shallow subtidal species living in crevices in rocks. The few deepwater records are based on very small specimens and may represent either anomalies or confusion in collecting station data.
Themiste (Lagenopsis) minor huttoni (Benham, 1904) Phascolosoma huttoni Benham, 1903:177-184. Dendrostoma huttoni Benham, 1904:306-307. Dendrostomum huttoni.—Edmonds, 1960:164165. Themiste huttoni.—Stephen and Edmonds, i972:204.-Edmonds, 1980:36-38. Themiste minor huttoni.—E. Cutler and Cutler, 1988:761762. DESCRIPTION. This subspecies is longer than the nominate form (trunk length may reach 55 mm), has more hooks, and its hook-bearing region extends over more of the introvert (55-75% vs. 25-35%). These are not clear distinctions, and the differences may simply be genotypic expressions reflecting more optimal niches (e.g., larger size and more hooks produced or fewer rubbed off, like the situation with the California and Japanese T pyroides). DISTRIBUTION. Australia, New Zealand, and the Chatham Islands; in intertidal, hard substrates.
Themiste (Lagenopsis) variospinosa Edmonds, 1980 Themiste variospinosa Edmonds, i98o:42-43.-E. Cutler and Cutler, 1988:762. DESCRIPTION. The principal difference between this species and T. minor huttoni, which it resembles, is in the nature of the introvert hooks (Fig. 38C), which exhibit much greater variation in size on any given worm (30-400 u,m tall) and are pointed in diverse directions, not just posteriorly. This species may be no more than a localized variety of the surrounding population of T. minor huttoni, and additional material would more firmly establish the validity of this taxon. DISTRIBUTION. Queensland, Australia, in intertidal coral.
6
The Phascolosomatids
Class Phascolosomatidea E. Cutler and Gibbs, 1985 Phascolosomida E. Cutler and Gibbs, 1985:166. Phascolosomatidea Gibbs and Cutler, 1987:53. Sipuncula with tentacles confined to an arc enclosing the dorsal nuchal organ; peripheral circumoral tentacles absent (Fig. 41). Introvert hooks recurved, usually with an internal structure, and closely packed in regularly spaced rings (absent in two species). Spindle muscle attached posteriorly, except in subgenus Apionsoma (Edmondsius). Order Phascolosomatiformes E. Cutler and Gibbs, 1985 Phascolosomaformes, E. Cutler and Gibbs, 1985:166. Phascolosomatiformes, Gibbs and Cutler, 1987:53. Phascolosomatidea with anterior trunk not modified to form anal shield. Four introvert retractor muscles. Family Phascolosomatidae Stephen and Edmonds, 1972 Characters are those of the order. Contracted members of this family are probably responsible for the American common name, "peanut worms," as they resemble peanuts in size (often 1-3 cm), shape (plump pyriform), and color (light brown). The vast majority live in burrows, crevices, or sandy pockets in rocky, shallow warm waters. A few species live in cool water, one is found in deep water, and two Apionsoma species are part of the interstitial sand-dwelling fauna. Familial Traits Body Wall. The outer body wall is usually tough and well endowed with obvious papillae. The longitudinal muscle on the inner wall is well devel-
Family Phascolosomatidae
157
Figure 41. Tip of extended introvert in Phascolosoma illustrating characteristic nuchal tentacles (often less well developed) and discreteringsof hooks. Note collar between tentacles and hooks and absence of circumoral, peripheral tentacles. C, collar; M, mouth; NO, nuchal organ. (After Selenka et al., 1883.) oped and subdivided into bands which occasionally anastomose, except in two small subgenera in which this layer is thinner and continuous. Hooks. The general pattern is many hooks in distinct rings near the distal tip of the introvert (Fig. 41). The nature of the hooks appears to be species-specific and is discussed in detail below. Antillesoma antillarum and one Apionsoma species lack hooks altogether, at least in postjuvenile stages. Apionsoma hooks have a series of basal spinelets. Contractile Vessel. Only Antillesoma antillarum has true contractile vessel villi. In a few larger Phascolosoma the vessel itself may be large with bulbous pouches or swellings. Spindle Muscle. In all species but Apionsoma (Edmondsius) pectinatum the spindle muscle extends through the gut coil and inserts on the posterior end of the trunk (Fig. 42B). Introvert Retractor Muscles. All species in this family have two pairs, but there is considerable fusion in Antillesoma antillarum, in which the retractor muscles can appear as a single pair. In some Apionsoma species the muscles are very thin and originate at approximately equal distances from the ventral nerve cord, thus making the concept of dorsal and ventral pairs useless. Also, occasional loss or fusion occurs, giving worms the appearance of only two or three muscles.
158
The Phascolosomatids
A B Figure 42. Phascolosoma. A. External form of expanded P. stephensoni with rough papillated trunk and pigment patches on the introvert. B. Internal view of P. granulatum. ES, eyespots; other abbreviations as in Figure 1. (From Wesenberg-Lund, 1957b, reprinted by permission of Laser Pages Publishing [1992] Ltd.) Key to Phascolosomatidae Subgenera 1. Contractile vessel with villi; large array of tentacles; no hooks Antillesoma - Contractile vessel without villi; tentacles small to absent; hooks present (except in one species) 2 2. Introvert much longer than trunk; hooks (if present) with basal spinelets; nephridia usually bilobed Apionsoma, 3 - Introvert less than twice trunk length; hooks without basal spinelets; nephridia unilobed Phascolosoma, 4 3. Longitudinal muscle in body wall a uniform continuous layer A. (Apionsoma) - Longitudinal muscle in body wall gathered into bands
A. (Edmondsius)
Genus Phascolosoma
159
4. Longitudinal muscle in body wall a uniform continuous layer P. (Fisherana) - Longitudinal muscle in body wall gathered into bands ... P. (Phascolosoma)
Genus Phascolosoma Leuckart, 1828 Phascolosoma Leuckart, 1828:22.-Fisher, 19503:551; 1952:422.-Stephen and Edmonds, 1972:270-271.-Gibbs and Cutler, 1987:54.-]^. Cutler and Cutler, 1990:691. Phascolosomum Diesing, 1851:63 (in part). Phymosomum de Quatrefages, i865b:62i. Phymosoma Selenka et al., 1883:54. Physcosoma Selenka, 1897:460. DIAGNOSIS. Introvert variable in length, often equal to trunk, with numerous rings of recurved hooks. Fewer than 30 tentacles in crescent around nuchal organ (peripheral tentacles lacking). Contractile vessel without true villi. Four introvert retractor muscles, lateral pairs sometimes partially fused, rarely completely fused. Two unilobed nephridia. Body wall musculature in separate bands or continuous. See Figures 41-51. TYPE SPECIES. Phascolosoma granulatum Leuckart, 1828. NOMENCLATURAL NOTE. The genus Phascolosoma was erected in 1828, but between 1880 and 1950 the name was incorrectly used to replace Golfingia. During that period the names Phymosoma and Physcosoma were widely, but incorrectly, used for Phascolosoma species. Fisher (1950a) reestablished the correct usage of Phascolosoma and Golfingia, but some authors and biological supply houses continued to use the incorrect names through the 1970s. Stephen and Edmonds (1972) established four subgenera of Phascolosoma. Three of these (Antillesoma, Rueppellisoma, and Satonus) were reviewed by E. Cutler and Cutler (1983). All but Antillesoma were eliminated, and this subgenus was elevated to generic status. Only one P. (Satonus) species was retained, and none of the P. (Rueppellisoma) species. This action was reviewed by Gibbs and Cutler (1987), who redefined P. (Satonus), changing the name to P. (Edmondsius). In the present work the generic placement of this subgenus has been moved to Apionsoma Sluiter for reasons given below. At this time the genus group name Fisherana Stephen is resurrected as a subgenus and moved, with its two
Genus Phascolosoma
161
species (which had been in Apionsoma) into the genus Phascolosoma. The nominate subgenus was reviewed by N. Cutler and Cutler (1990). Morphological Characters of Phascolosoma Introvert Hooks. All Phascolosoma species bear laterally compressed, posteriorly directed hooks arranged in rings around the distal portion of the introvert (Fig. 43). It is not known whether hooks are produced throughout the life of a worm or if there is a species-specific upper limit to the number. Proximal rings may be partially or completely missing in some individuals, probably as a result of abrasion. About half the species have fewer than 50 hook rings (commonly 15-25), and the remainder have more than 50, often more than 100. Scattered hooks are present proximal to the rings of hooks in a few species. Phascolosoma hooks are typically 30-70 ujn from base to tip. Exceptions are P. pacificum (90-125 ujn), P. meteori, and P. saprophagicum (both 15-25 (xm). Small worms of all species tend to have smaller hooks than larger worms. Hook size can be helpful in identifying hooked species at the two ends of the size continuum. On the posterior edge (the concave side) of most hooks there is a secondary, or accessory, tooth, which is different from the bidentate Aspidosiphon hook. When present, this tooth ranges from small, fragile, and sharp to large, equal in thickness to the main part, and blunt (humplike). With the exception of P. nigrescens, this attribute is constant within species. The apical (distal) tip may also vary from an acute point to a rounded, blunt apex. Generally there is a consistent pattern within a species, but worn or rounded hooks may be found on an individual with normally pointed hooks, so several hooks must be examined on any specimen. The tip of the hook curves at an angle to the perpendicular, and this angle varies, both within and among populations. One can measure this angle as shown in Figure 44A. Line X is drawn perpendicular to the base through the most anterior part of the concave side, and Y is drawn from the tip to intersect X in the middle of the point. Some species have angles less than 900, others are in the 90-115 0 range. The latter group includes species
Figure 43. Scanning electron micrographs of hooks from Phascolosoma. A. P. granulatum. B. P. perlucens. C. P. scolops. D. P. albolineatum. E. P. glabrum glabrum. F. P. glabrum multiannulatum. Scale = 10 \x.m. (From N. Cutler and Cutler, 1990, courtesy of the Biological Society of Washington.)
162
The Phascolosomatids
3-
Figure 44. Introvert hook of Phascolosoma stephensoni. A. A, anterior; C, crescent; DT, distal tip; P, posterior; S, streak; ST, secondary tooth; T, triangle. The numbered lines (1, 2, and 3) indicate where the three adjacent transmission electron photomicrographs were taken. The angle formed between lines X and Y determines the tip angle, as used in the text. B. Light microscope view. C. Scanning electron micrograph of two rings of hooks. Scale = 20 u,m. (From N. Cutler and Cutler, 1990, courtesy of the Biological Society of Washington.)
Genus Phascolosoma
163
whose hooks appear to be bent at a right angle (e.g., P. albolineatum and P. glabrum). An internal clear streak (apical canal) and triangular spaces of differing opacities are visible when a hook is viewed via transmitted light. The paler, lighter regions are areas in which little or no organic material has been deposited (Fig. 44B). The hooks are open basally, so a hollow space, the clear streak, extends along the basal edge. (This may not always be apparent when hooks are removed from the tissue.) The clear streak extends upward from the base to near the apex. There may also be a triangular clear area in the anteriobasal corner, which may or may not be separated from the slender clear streak. A pale crescent posterior to the clear streak is present in P. stephensoni (Fig. 44). Using a combination of TEM, SEM, and light microscopy, N. Cutler and Cutler (1990) compared the internal architecture of newly formed hooks and more mature hooks. They proposed that Phascolosoma hooks begin with an open internal space into which partitions of reinforcing material are eventually secreted. A few distinctive morphs exist (e.g., P. nigrescens and P. stephensoni), but the large degree of variation found in many populations can be confusing. Used carefully, however, internal hook structure can be a helpful character. Finally, separate units of diverse shape at the posterior basal edge of most hooks can be seen through the light microscope (but not in P. arcuatum). These basal processes are part of the hook, but unpigmented areas are present between the main part of the hook and these smaller units. Three variations were identified by N. Cutler and Cutler (1990): (1) warts, as in P. stephansoni, are the most common condition (Fig. 45A); (2) rootlets are tall and thin, as in P. saprophagicum and P. turnerae; and (3) toes are processes on the side of the hook, as seen in P. glabrum (differing in the two subspecies; see Fig. 45B, C). Pigmented Introvert Bands or Stripes. The dorsal side of the introvert is often darker than the ventral side. The reddish brown color, when present, is in patches that vary in size from large and almost continuous in P. perlucens to irregular smaller bands (e.g., P. scolops or P. agassizii). The presence or absence of pigmented bands is consistent within species (except P. nigrescens). Nephridia Length and Attachment. The nephridia in most species extend back from the nephridiopore for 40-65% of the trunk length. A few
164
The Phascolosomatids
Figure 45. Scanning electron micrographs of basal elaborations of Phascolosoma hooks. A. Warts of P. stephensoni. B. Toes of P. glabrum glabrum. C. Toes of P. glabrum multiannulatum. Scale = 1 0 jj,m. (From N. Cutler and Cutler, 1990, courtesy of the Biological Society of Washington.)
species (e.g., P. pacificum and P. glabrum) have longer nephridia, 95100% of the trunk length, and a few other species (e.g., P. perlucens) have short nephridia that extend only 25-45% of the trunk length. Thin connective tissue strands connect the body wall to some portion of the nephridia. In most species the nephridia are about 50% attached, but the range within any population is 30-70%. In a few species (e.g., P. pacificum) the nephridia are attached to the body wall along almost their entire length. Nephridial length and degree of attachment are not usually helpful identification characteristics because most species fall in the broad mid-range. Papillae. Papillae occur in three general shapes: dome, mammillate, and cone. Many sipunculans have more than one type. The preanal papillae, around the base of the introvert, are useful for differentiating some species (Fig. 46). Transmitted light microscopy shows granular platelets of different sizes and shapes arranged in diverse patterns around the central pore of each secretory papilla (Fig. 47). Since the SEM shows the surface to be smooth, however, the platelets must be subcuticular. This attribute is unique and consistent in only a few species (e.g., P. noduliferum; Fig. 47E). In most species the size and distribution of platelets is too variable to be useful
Genus Phascolosoma
165
Figure 46. Scanning electron micrographs of preanal papillae from several Phascolosoma showing possible shapes. A. P. granulatum (dome; scale = 0.2 mm). B. P. scolops (mammillate; scale = 0.2 mm). C. P. albolineatum (dome; scale = 0.2 mm). D. P. perlucens (cone; scale = 0.2 mm). E. P. stephensoni (cone; scale = 0.2 mm)^) Posteriorly directed preanal papillae on P. perlucens. (A-E from N. Cutler and Cutler, 1990, courtesy of the Biological Society of Washington.) (Fig. 47A-D). The cuticle over the preanal papillae of a few species (e.g., P. stephensoni and P. perlucens) has a smooth, hardened appearance (not granular and rough) reminiscent of the holdfast papillae in some Phascolion species (Fig. 46D). Papillar size (height or basal diameter) is not very meaningful. Every worm has papillae of various sizes in the mid-trunk, and larger toward both ends; larger worms tend to have larger papillae. Retractor Muscle Origins. The paired dorsal muscles originate in the body wall about 45% of the distance toward the posterior end of the trunk
Genus Phascolosoma
167
in most species (interspecific range, 30-60%). The ventral pair originates more posteriorly, at about 65% (range 50-75%), or in the posterior quarter in P. saprophagicum. The terms dorsal and ventral cease to be helpful in this species and in P. arcuatum because both muscle pairs originate at about the same distance from the ventral nerve cord. Except for these two species, retractor origins are not helpful in identifying members of this genus. Subgenus Phascolosoma (Fisherana) (Stephen, 1964) Fisherana Stephen, ic;64:46o.-Stephen and Edmonds, 1972:329. Apionsoma Sluiter, 1902:42 sensu E. Cutler, 1979:382; Gibbs and Cutler, 1987:55 (in part). DIAGNOSIS. Longitudinal muscle layer continuous. TYPE SPECIES. Physcosoma capitatum Gerould, 1913. NOMENCLATURAL NOTE. The species in this subgenus were moved back into the genus originally proposed by their describers after a cladistic analysis of the genera and subgenera in the Phascolosomatidae showed that the only factor separating Phascolosoma and Fisherana is the nature of the body wall musculature. The homoplastic nature of this feature is discussed in E. Cutler and Gibbs, 1985. In all other ways these worms are more like the other members of Phascolosoma than Apionsoma. Their previous placement in the latter genus was determined by giving heavy weight to the condition of the longitudinal muscles. Concurrently, the subgenus Edmondsius is transferred to the genus Apionsoma. Key to Phascolosoma (Fisherana) Species 1. Ventral retractor muscle origins in posterior half of trunk
P. capitatum
- Ventral retractor muscle origins in middle or anterior part of trunk P. lobostomum
Figure 47. Trunk papillae in Phascolosoma. A-E. Different arrangements of platelets as seen by light microscopy (diameters 0.1-0.15 mm). A and B. P. scolops. C and D. P. nigrescens. (A-D after Selenka et al., 1883.) E. P. noduliferum (after Edmonds, 1956, courtesy of CSIRO Editorial Services). F and G. General form of papillae, as shown by SEM. F. P. scolops, a fairly typical member of the genus with dome or mammillate papillae, height
i68
The Phascolosomatids
Phascolosoma (Fisherana) capitatum (Gerould, 1913) Physcosoma capitatum Gerould, 1913:421-424. Fisherana capitata.— Stephen and Edmonds, 1972:331-332. Golfingia (Apionsoma) capitata. —E. Cutler, 1979:373-374. Apionsoma capitata.—E. Cutler and Cutler, I987b:73.-Saiz and Villafranca, i99o:ii65.-Saiz 1993:126. Physcosoma abyssorum Southern, 1913:12. Phascolosoma abyssorum Stephen and Edmonds 1972:292. Apionsoma abyssorum Gibbs, 1986:340. Golfingia (Fisherana) savalovi Murina, 19743:230. DESCRIPTION. The density and size of the papillae may vary in this species, but the posterior trunk generally has an array of conspicuous large, elongate papillae (Fig. 48). The epidermis is often loose and fragile; it rubs off easily to give a distinctive appearance. The pale whitish underlying muscle layer and the large papillae are the dominant features of these
Figure 48. Posterior trunk and large papillae 01 Phascolosoma (Fisherana) capitatum. A. Norma skin showing variable density of papillae (scale = 0.1 mm). B. Specimen with loose skin, possiblj due to postmortem chemical treatment (scale = 0.1 mm). C. Specimen with skin sloughed off exposing elongate papillae (ca. 0.2 mm long) anc underlying muscle layer. (From E. Cutler, 1979 courtesy of the Linnean Society.)
Genus Phascolosoma
169
worms, which are generally stout, pear shaped, pale to dark brown, and commonly up to 20 mm long. Introvert hooks are 30-35 p,m tall, and the introvert is shorter than the trunk. The retractor muscle origins are in the posterior half of the trunk but are quite variable in placement. In a small specimen the ventral retractors originate near the posterior end of the body, unlike the more anterior slender dorsal muscle. The origins of the dorsal pair vary widely, ranging from 33 to 75% of the distance toward the posterior end of the trunk. 0 0 DISTRIBUTION. Around the margin of the Atlantic Ocean (50 N to 53 S), at continental slope and rise depths from 650 to 4200 m. Phascolosoma (Fisherana) lobostomum W. Fischer, 1895 Phascolosoma lobostoma W. Fischer, 1895:14-15. Fisherana lobostoma. —Stephen and Edmonds, 1972:333. Golfingia (Apionsoma) lobostoma. —E. Cutler, 1979:376. Phascolosoma wasini Lanchester, 1905^32-33. Fisherana wasini.— Stephen and Edmonds, 1972:333-335. NOTE. This species is based on a very weak foundation. Only a few specimens were collected, and the original description of them was flawed. It may not merit species status at all and should be reevaluated in the light of any new collections. It is very possible that what is represented here are simply a few anomalous individuals, not a biological species (see E. Cutler, 1979). DESCRIPTION. A small (
Subgenus Phascolosoma (Phascolosoma) Leuckart, 1828 Phascolosoma (Phascolosoma) Stephen and Edmonds, 1972:289-291.Gibbs and Cutler, 1987:54.-1^. Cutler and Cutler, 1990:701. DIAGNOSIS. Body wall muscles separated into distinct bands. Spindle muscle attached posteriorly; introvert hooks without accessory spinelets.
170
The Phascolosomatids
Figure 49. Phascolosoma introvert hooks. A. P. pacificum. B. P. glabrum. C. P. turnerae. D. P. arcuatum. E. P. nigrescens. F. P. granulatum. G. P. meteori. H. P. saprophagicum. I. P. albolineatum. Scale = 20 (i,m. (From N. Cutler and Cutler, 1990, courtesy of the Biological Society of Washington.)
Genus Phascolosoma
171
Figure 50. Phascolosoma introvert hooks. A. P. perlucens. B. P. maculatum. C. P. annulatum. D and E. P. noduliferum (anterior and posterior). F. P. ,sc0/0p.sfG)and@ P. agassizii from incompletely erupted most distal ring and middle ring. Scale = 20 (Jim. (From N. Cutler and Cutler, 1990, courtesy of the Biological Society of Washington.)
172
The Phascolosomatids
Key to Phascolosoma s. s. Species Attributes of hooks refer only to those in complete rings, not those newly formed in the two or three distalmost rings or the worn and scattered proximal hooks. NOTE.
1. More than 50 complete and incomplete rings of hooks
2
- Less than 50 complete and incomplete rings of hooks
9
2. Most hooks >ioo \um tall; nephridia as long as trunk (Fig. 49A) P. pacificum - Hooks < 100 [Lin tall, nephridia shorter than trunk
3
3. Concave side of hook with large, rounded hump; toes present but not warts (2 subspecies, Fig. 49B) P. glabrum - Concave side of hook smoothly tapered or with small secondary tooth . . . 4 4. Hooks with long, thin basal processes (Fig. 49C) - Basal processes, if present, as normal warts 5. Hooks without basal warts (Fig. 49D) - Hooks with basal warts
P. turnerae 5 P. arcuatum 6
6. Clear streak of hook with swelling in middle of vertical and horizontal portion (Fig. 49E) P. nigrescens - Clear streak without abrupt swellings
7
7. Hooks with posterior crescent, many >75 u.m tall; preanal papillae are smooth cones; pigment bands on introvert (Fig. 44) P. stephensoni - Hooks without crescents, most <75 u.m tall; no pigment bands on introvert 8 8. Hooks with granular triangle (Fig. 49F); close-set, randomly distributed papillae platelets P. granulation - Hooks without triangle, posterior hooks with more triangular shape and narrower clear streak (Fig. 50D, E); papillae platelets around pore small and close-set, then abruptly more widespread (Fig. 47E) P. noduliferum 9. Hooks <25 p,m tall - Hooks >25 u.m tall 10. Fewer than 10 rings of inconspicuous hooks (Fig. 49G) - More than 15 hook rings (Fig. 49H) n . Angle of hook tip >90° (Fig. 49I)
10 n P. meteori P. saprophagicum P. albolineatum
Genus Phascolosoma - Angle of hook tip 900 or less
173 12
12. Large, rounded hump on concave side of hook; preanal papillae smooth, posteriorly directed, cone shaped (Fig. 50A) P. perlucens - Concave side of hook smooth or with small tooth 13. Hooks with separate anterior basal triangle - Hooks without triangles (Fig. 50B)
13 14 P. maculatum
14. Trunk papillae platelets extending onto interpapillae surfaces (Fig. 50C).... P. annulatum - Papillae platelets restricted to papillae surfaces
15
15. Hook with distinct triangle; narrow band of red cone-shaped preanal papillae (Fig. 50F) P. scolops - Hook triangle indistinct or absent; preanal papillae not distinct from domeshaped trunk papillae (Figs. 50G, H, and 51) P. agassizii
Phascolosoma agassizii agassizii Keferstein, 1866 Phascolosoma agassizii Keferstein, 1866:218-219.-Fisher, 1952:424430.-R.ice, 1973:1-51. Phymosoma agassizii.—Selenka et al., 1883: 78-79. Physcosoma agassizii.—W. Fischer, 1895:10. Phascolosoma (Phascolosoma) agassizii.—Stephen and Edmonds, 1972:292-293.Rice, i98o:492.-Frank, i983:23-24.-Saiz, i986b:52-55.-Haldar, 1991: 49-51. Phascolosoma (Phascolosoma) agassizii agassizii.—N. Cutler and Cutler, 1990:703-705. Phymosoma lordi Baird, 1868:92.-Rice and Stephen, 1970:62. Phascolosoma japonicum Griibe, 1877:73. Phymosoma japonicum.— Selenka et al., 1883:76-78. Physcosoma japonicum.—Selenka, 1888: 220. Phascolosoma (Phascolosoma) japonicum.—Stephen and Edmonds, 1972:309-310.-E. Cutler et al., i984:293-296.-Haldar, 1991: 58-60. Physcosoma yezoense Ikeda, 1924: 32-34. Phascolosoma (Phascolosoma) yezoense.—Stephen and Edmonds, 1972:328-329. Physcosoma glaucum Sato, 1930:15-17. Phascolosoma (Phascolosoma) glaucum.—Stephen and Edmonds, 1972:306. Physcosoma formosense Sato, 1939:398-401. Phascolosoma (Phascolosoma) formosense.—Stephen and Edmonds, 1972:304.
174
The Phascolosomatids
Phascolosoma (Rueppellisoma) golikovi Murina, 1975^54-55.-E. Cutler and Cutler, 1983:180. DESCRIPTION. The introvert has irregular dark pigment bands and is about as long as the trunk. Hooks are 30-70 ixm tall, in fewer than 30 rings. Each hook has a variable clear streak (not easily seen in worms smaller than 8 mm) and a triangle that is usually indistinct, and the secondary tooth is small or absent (Fig. 51). The medium to light brown trunk is covered with papillae (often darker than the skin). Papillae platelets are variable in size (3-9 lim) and distributed randomly. DISTRIBUTION. Common on both sides of the North Pacific from Mexico to Alaska on the eastern side and in Japanese waters in the west. Scattered records from Indian Ocean waters, including several Indian localities, as well as from south and west Africa in the Atlantic.
Phascolosoma agassizii kurilense (Sato, 1937) Physcosoma kurilense Sato, 1937a:! 17-120. Phascolosoma (Phascolosoma) kurilense.—Stephen and Edmonds, 1972:310-311. Phascolosoma (Phascolosoma) agassizii kurilense.—N. Cutler and Cutler, 1990: 706. DESCRIPTION. The presence of a small secondary lobe on the nephridia of mature worms is the sole morphological difference from the nominate form. DISTRIBUTION. Kurile Islands, northwestern Pacific.
Phascolosoma albolineatum (Baird, 1868) Phascolosoma albolineatum Baird, 1868:91-92. Phymosoma albolineatum.—Selenka et al., 1883:71-72. Physcosoma albolineatum.— W. Fischer, 1913:99. Phascolosoma (Phascolosoma) albolineatum.— Stephen and Edmonds, 1972:293-295.-!^. Cutler and Cutler, 1990: 706-707. Phymosoma microdontoton Sluiter, 1886:506. Phascolosoma (Phascolosoma) microdontoton.—Stephen and Edmonds, 1972:312-313. Phascolosoma multiannulata Wesenberg-Lund, 19543:378-383 (in part). Phascolosoma andamanensis Johnson, 1971:603-604. DESCRIPTION. This species is very similar to pale P. scolops, so hooks must be examined to avoid misidentification. The hooks, 25-65 ixm tall,
Genus Phascolosoma
175
Figure 51. Hooks from Phascolosoma agassizii showing variation in size and nature of clear streak. Height varies from 30 to 70 jun. (After Fisher, 1952, courtesy of Smithsonian Institution Press.)
are arranged in fewer than 40 rings, and the tip of each hook is bent at an angle greater than 900. On the concave side the hooks have a large bulge but no secondary tooth, so the base has a less triangular form than that seen in other species (Figs. 43D, 49I). The clear streak often does not extend beyond the midpoint. The introvert, usually with dark patches, is shorter than the trunk and has dome-shaped preanal papillae (Fig. 46C). The trunk may reach 35 mm but more often is 10-20 mm long. The nephridia are usually less than half the length of the trunk. Some members of this species have anomalous fused retractor muscles, thus appearing to have fewer than the full complement (E. Cutler et al. 1984:292). DISTRIBUTION. Widespread but not common in Indo-West Pacific tropical shallow waters. Phascolosoma annulatum (Hutton, 1879) Phascolosoma annulatum Hutton, 1879:278. Phascolosoma (Phascolosoma) annulatum.—Stephen and Edmonds, 1972:296-297.-]^. Cutler and Cutler, 1990:707. Physcosoma scolops var. mossambiciense.—Augener, 1903:339. Physcosoma scolops tasmaniense W. Fischer, 1914^3-4. Phascolosoma tasmaniense Edmonds, 1956:285-286. DESCRIPTION. The trunk is up to 50 mm long, and the introvert is one to two times the trunk length. The hooks are 45-60 p,m tall, arranged in up to 25 complete rings, and similar to P. scolops, but the separate clear triangular area is less distinct (Fig. 50C). Proximally the incomplete dorsal rings of smaller (30-35 |xm), more triangular hooks can be partially obscured by the papillae and pigment. The bases of the trunk papillae appear polygonal, not oval, and are covered by dark polygonal platelets, which spread out over the skin in the interpapillae spaces in a distinctive manner.
The Phascolosomatids
i76
DISTRIBUTION.
Southern Australia, New Zealand, and Campbell Island,
in cool waters. Phascolosoma arcuatum (Gray, 1828) Siphunculus arcuatus Gray, 1828:8.-Rice and Stephen, 1970:50-51. Phascolosoma (Phascolosoma) arcuatum arcuatum.—Stephen and Edmonds, 1972:297-298. Phascolosoma (Phascolosoma) arcuatum.— N. Cutler and Cutler, i990:707-7o8.-Haldar, 1991:54-56. Phymosoma lurco Selenka and de Man, in Selenka et al., 1883:61-63. Physcosoma lurco.—W. Fischer, 1895:12. Phascolosoma lurco.—Edmonds, 1956:290-291. Phymosoma lurco malaccensis Selenka and de Man, in Selenka et al., 1883:63. Physcosoma lurco malaccensis.— Sluiter, 1902:12. Phascolosoma arcuatum malaccense.—Stephen and Edmonds, 1972:298. Phascolosoma rhizophora Sluiter, 1891:119-121; 1902:13. Physcosoma ambonense W. Fischer, 1896:337-338. Phascolosoma (Phascolosoma) ambonense.—Stephen and Edmonds, 1972:295-296. Phymosoma deani Ikeda, 1905:171-172. Phascolosoma (Phascolosoma) deani.—Stephen and Edmonds, I972:299.-E. Cutler and Cutler, 1981: 88-89. Physcosoma esculenta Chen and Yeh, 1958:273-274. Phascolosoma esculenta.—Murina, 19643:263. Phascolosoma (Phascolosoma) esculentum.—Stephen and Edmonds, 1972:301. DESCRIPTION. A distinctive species with large, very dark papillae sharply set off from a light yellow-brown skin. The introvert is up to twice the trunk length and bears more than 100 complete and incomplete rings of hooks, 40-70 |xm tall, that lack secondary teeth, warts, or toes. The hooks are simple internally, the clear streak being greatly expanded basally (Fig. 49D). The retractor muscles are unusual in that the origins of the broad posterior (ventral) pair have shifted dorsally to LMBs 2 and 3, while the origins of the thinner anterior (dorsal) pair have shifted ventrally to LMB 1. In the contracted state the retractor complex may appear as a single column with four roots. The circular muscle layer is also divided into anastomosing bands. DISTRIBUTION. Northeastern India, Andaman Islands, southern China, Vietnam, Philippines, Malaysia, Indonesia, and northern Australia. Tolerates extended periods out of water and is found in brackish water (e.g., in mangrove estuaries) around the high tide line.
Genus Phascolosoma
177
Phascolosoma glabrum glabrum (Sluiter, 1902) Physcosoma glabrum Sluiter, 1902:14-15. Phascolosoma (Phascolosoma) glabrum.—Stephen and Edmonds, 1972:305. Phascolosoma glabrum glabrum.—N. Cutler and Cutler, 1990:708-709. Phymosoma microdontoton.—Shipley, 1898:471; 18993:56. Physcosoma funafutiense W. Fischer, 19140:6-8. Phascolosoma (Phascolosoma) funafutiense.—Stephen and Edmonds, 1972:304-305. -E. Cutler and Cutler, 19793:983-984. DESCRIPTION. Similar to P. pacificum in several characters; for example, nephridia are 75-100% of the trunk length, trunk papillae are evenly distributed and of equal size, and there are many hook rings. Phascolosoma g. glabrum is distinguished by having somewhat smaller hooks (6085 jx,m) with a different shape and internal structure (Figs. 43E, 45B, and 49B). This is the only species whose hooks have basal toes. The hooks also have a large hump on the posterior edge, and the clear streak has an apical expansion. Since the papillae are smaller and dome shaped, not tall cones, the skin feels smoother than that of P. pacificum. DISTRIBUTION. Scattered records from Indo-West Pacific islands (Diego Garcia, Indonesia, Eniwetok, Funafuti, Rotuma, and Christmas Island). Phascolosoma glabrum multiannulatum (Wesenberg-Lund, 1954) Phascolosoma multiannulata Wesenberg-Lund, 19543:378-383 (in part). Phascolosoma (Phascolosoma) multiannulatum.—Stephen and Edmonds, 1972:313-314. Phascolosoma glabrum multiannulatum.— N. Cutler and Cutler, 1990:709. DESCRIPTION. The differences between this and the nominate form are subtle. The hooks are smaller (<6o \im), the clear streak has no apical expansion, and there are about 12 toes on the left side (Figs. 43F, 45C). The rings of hooks are more widely spaced, and the trunk papillae are larger domes and sometimes in rectangles formed by folds of skin. DISTRIBUTION. On the eastern edge of the species' range at Hikueru, Tahiti, the type locality. Phascolosoma granulatum Leuckart, 1828 Phascolosoma granulatum Leuckart, 1828:22. Physcosoma granulatum. —Selenka et al., 1883:79. Phascolosoma (Phascolosoma) granulatum.—Stephen and Edmonds, i972:3o6-309.-Gibbs, I977b:28.
i78
The Phascolosomatids
-Saiz, 19860:55-62; 1993:118-122.-N. Cutler and Cutler, 1990:709710. Sipunculus flavus Risso, 1826:292. Sipunculus tigrinus Risso, 1826:292. Sipunculus genuensis de Blainville, 1827:313. Phascolosoma laeve Cuvier, 1830:243. Sipunculus verrucosus Cuvier, 1830:243. Sipunculus levis Cuvier, 1830:243-244. Sipunculus papillosum W. Thompson, 1840:101 (in part). Sipunculus multitorquatus de Quatrefages, 18650:621. Phascolosoma fasciatum Baird, 1868:89. Phascolosoma jeffreysii Baird, 1868:89. Phascolosoma loveni Koren and Danielssen, 1877:128-129. Physcosoma herouardi Herubel, 19033:107. Physcosoma lanzarotae Harms, 1921:307 (in part). DESCRIPTION. AS its name implies, the papillae of P. granulatum are granular and dome shaped; they are occasionally darker than the body wall and lack the taller, smoother, cone-shaped preanal papillae typical of the similar P. stephensoni (Fig. 46A). The introvert lacks dark pigmented bands, and the hooks are arranged in more than 50 rings, some incomplete. The hooks are 35-70 (xm tall and have a narrow clear streak with an indistinct granular triangle; the secondary tooth is ill-defined or lacking (Figs. 43A, 49F). The number of longitudinal muscle bands varies considerably from anterior to posterior in a single worm—around 18 anteriorly and 26 posteriorly. The paucity of apomorphic characters suggests that this may be an evolutionarily significant morphology, closest to the ancestral Phascolosoma stock. DISTRIBUTION. Common in the colder subtidal waters (occasionally intertidal) of the northeastern Atlantic Ocean from southern Norway along the coasts of Europe and the British Isles to northern Africa, out to the Azores and the Cape Verde Islands. It also extends into the Mediterranean and Adriatic seas. The Indian Ocean records are now considered to be P. stephensoni (N. Cutler and Cutler, 1990). Phascolosoma maculatum (Sluiter, 1886) Phymosoma maculatum Sluiter, 1886:511-512. Physcosoma maculatum. —Sluiter, 1902:11. Phascolosoma (Satonus) maculatum.—Stephen and Edmonds, I972:285.-E. Cutler and Cutler, 1983:185. Phascolosoma (Phascolosoma) maculatum.—N. Cutler and Cutler, 1990:710.
Genus Phascolosoma
179
DESCRIPTION. The distinctive hooks are 90-95 |xm tall, slender, and have a clear streak reaching one-half to two-thirds the distance to the tip and usually expanding into a broad basal triangle (Fig. 50B). Up to 12 basal warts are present, but only some of the hooks have a secondary tooth. The posterior trunk papillae are tall and cone shaped; the anterior papillae are mammiform. DISTRIBUTION. Only the type locality in Indonesia.
Phascolosoma meteori (Herubel, 1904) Phymosoma meteori Herubel, 19043:477-478. Physcosoma meteori.— Stephen, 194^:405. Phascolosoma meteori.—Wesenberg-Lund, 1957a: 12. Phascolosoma (Phascolosoma) meteori.—Stephen and Edmonds, 1972:312.-N. Cutler and Cutler, 1990:710-711. DESCRIPTION. The introvert is shorter than the trunk in these grayish worms. The trunk papillae are small domes, and the preanal papillae are in clusters of two to five, not uniformly distributed. Up to 10 incomplete rings of very small colorless hooks, 15-30 \ixn tall, are present but easily overlooked. Internally the hooks show a bent clear streak and anterior triangle. The contractile vessel is large and folded, with vesicular swellings, not villi, even in worms with the introvert completely extended. The combination of many tentacles and an enlarged contractile vessel to increase the surface area for gas exchange is seen in other sipunculans from this region {Sipunculus and Phascolion) as well. Some P. meteori live in mud tubes much like those inhabited by Phascolion lutense. DISTRIBUTION. Red Sea and Gulf of Aden, at 18-38 m.
Phascolosoma nigrescens (Keferstein, 1865) Phascolosoma nigrescens Keferstein, 1865^424. Phascolosoma (Phascolosoma) nigrescens.—Stephen and Edmonds, 1972:315-316.E. Cutler and -Cutler, 19793:984-985.-N. Cutler and Cutler, 1990: 77i-7i4.-Edmonds, 1980:59-61.-Saiz, 19843:208-210. Phymosoma nigrescens.—Selenka et al., 1883:73. Physcosoma nigrescens.— W. Fischer, 1913:98. Phascolosoma puntarenae Griibe and Oersted, 1858:13. Sipunculus (Phymosomum) puntarenae.—de Quatrefages, 1865^624. Phascolosoma (Phascolosoma) puntarenae.—Stephen and Edmonds, 1972:319-320. Sipunculus (Phymosomum) plicatus de Quatrefages, i865b:622. Phascolo-
i8o
The Phascolosomatids
soma plicatum Baird, i868:93.-Stephen and Edmonds, 1972:340.Saiz, I984a:209. Phascolosoma varians Keferstein, 18655:424-426. Phymosoma varians. —Selenka et al., 1883:69-70. Physcosoma varians.—Shipley, 1898: 468-473. Phascolosoma (Phascolosoma) varians.—Stephen and Edmonds, 1972:327-328. Phascolosoma agassizii Keferstein, 1867:46 (in part). Physcosoma agassizii var. puntarenae.—Selenka et al., 1883:79. Phascolosoma planispinosum Baird, i868:93.-Rice and Stephen, 1970: 65Phymosoma spengeli Sluiter, 1886:498-499. Physcosoma spengeli.— Shipley, 18995:156. Phascolosoma (Phascolosoma) spengeli.—Stephen and Edmonds, 1972:325. Phymosoma duplicigranulatum Sluiter, 1886:501-502. Physcosoma duplicigranulatum.—Shipley, 18995:155. Phascolosoma (Satonus) duplicigranulatum.—Stephen and Edmonds, 1972:283-284. Phymosoma lacteum Sluiter, 1886:507-508. Physcosoma lacteum.— Sluiter, 1902:13. Phascolosoma (Phascolosoma) lacteum.—Stephen and Edmonds, 1972:311-312. Phymosoma diaphanes Sluiter, 1886:509-510. Phascolosoma (Phascolosoma) diaphanes.—Stephen and Edmonds, 1972:299-300. Physcosoma extortum Sluiter, 1902:15-16. Phascolosoma (Phascolosoma) extortum.—Stephen and Edmonds, 1972:303-304. Physcosoma evisceratum Lanchester, 19055:31. Phascolosoma (Phascolosoma) evisceratum.—Stephen and Edmonds, 1972:301-303. Physcosoma minutum ten Broeke, 1925:87-88 (not Phascolosoma minutum Keferstein, 18625:40 = Golfingia minuta [Kef.]). Phascolosoma (Antillesoma) minutum.—Stephen and Edmonds, 1972:281. Physcosoma horsti ten Broeke, 1925:89. Phascolosoma (Antillesoma) horsti.—Stephen and Edmonds, i972:28o.-E. Cutler and Cutler, 1983: 178. DESCRIPTION. Hooks, 35-90 (xm tall, are arranged in more than 100 mostly incomplete rings. The clear streak expanded near the midpoint of the vertical and the middle of the horizontal portions of the hook is unique to this species (Fig. 49E). The angle of the point is usually less than 900 (as low as 650) hut may 5e larger. The secondary tooth is usually small hut may 5e large or missing altogether. The light hrown trunk, commonly 2040 mm 5ut sometimes larger, has uniform dome-shaped papillae. The introvert is longer than the trunk and may have pigmented hands. The
Genus Phascolosoma
181
contractile vessel may be enlarged with vesicular swellings, but there are no villi. DISTRIBUTION. Very widespread circumtropical species; generally between 30° N and 30° S, in shallow waters of the Indian, Pacific, and Atlantic oceans. Phascolosoma noduliferum Stimpson, 1855 Phascolosoma noduliferum Stimpson, 1855:390. Sipunculus (Phymosomum) noduliferus de Quatrefages, 1865^624. Phascolosoma (Phascolosoma) noduliferum.—Stephen and Edmonds, 1972:316-317.Edmonds, 1980:62.-N. Cutler and Cutler, 1990:714-715. Siphunculus tuberculatus Gray, 1828:8 (in part). Sipunculus (Phymosomum) nodulosus de Quatrefages, i865b:621-622. Sipunculus (Phymosomum) javenensis de Quatrefages, 1865^622 (in part). Phascolosoma javenense.—Baird, 1868:94 (in part). Phascolosoma grayi Baird, 1868:88. DESCRIPTION. The introvert lacks pigment bands, and the papillae are of uniform size and more crowded posteriorly. The uniqueness of the papillae lies in the arrangement of the platelets: around the central pore there is a narrow ring of close-set units that abruptly become much more dispersed but do not extend onto the interpapillae skin (Fig. 47E). Illustrations of the hooks in the literature appear to be of the posterior scattered hooks, or incomplete rings. The more anterior hooks resemble those of P. agassizii (Fig. 49D, E). In general, these hooks have a more narrow clear streak, lack a triangle, are 60-90 (xm tall, usually occur in more than 50 rings, and have no secondary tooth. The similarities to P. agassizii are marked, and the differences between the two species are in the hooks, papillae, and geographical distribution. DISTRIBUTION. Intertidal from southern Australia and Tasmania, plus deeper water off the Philippines, New Guinea, and New Zealand. Phascolosoma pacificum Keferstein, 1866 Phascolosoma pacificum Keferstein, 1866:8-9; 1867:49-50. Phymosoma pacificum.—Selenka et al., 1883:63-65. Physcosoma pacificum.— Shipley, 1898:470. Phascolosoma (Phascolosoma) pacificum.—Stephen and Edmonds, 1972:317-318.-E. Cutler and Cutler, I979a:985986.-N. Cutler and Cutler, i990:7i5-7i6.-Edmonds, 1980:62-63.
182
The Phascolosomatids
Sipunculus (Phymosomum) javenensis de Quatrefages, i865b:622 (in part). Phascolosoma javenense.—Baird, 1868:94. Phascolosoma asperum Griibe, 18680:642-643. Phymosoma asperum.— Selenka et al., 1883:61. DESCRIPTION. The tall, cone-shaped, uniformly distributed papillae give the skin a rough texture. These uniformly colored animals are among the largest of the Phascolosoma species, commonly up to 60 mm, occasionally 125 mm. The introvert length is one to two times the trunk length. The hooks are arranged in 80-200 rings, have a broad base, and are 70-125 pjn tall. The secondary tooth is humplike, and an irregular clear streak with a separate triangle is present (Fig. 49A). The nephridia are long (75125% of the trunk length) and attached to the body wall for most of their length. Up to 40 anastomosing longitudinal muscle bands are present. DISTRIBUTION. The Red Sea and throughout the Indian and western Pacific oceans, from southern Japan to northern Australia, including Indonesia and numerous western Pacific islands, at depths less than 3 m. Phascolosoma periucens Baird, 1868 Phascolosoma perlucens Baird, 1868:90-91.-Rice and Stephen, 1970: 63-64.-Rice, i975b:35-48.-Edmonds, 1980:63-64.-12. Cutler et al., 1984:297. Phascolosoma (Phascolosoma) perlucens.—Stephen and Edmonds, I972:3i8-3I9.-N. Cutler and Cutler, I990:7i6-7I7.-Haldar, 1991:65-68. Sipunculus (Phascolosomum) vermiculus de Quatrefages, 1865^621. Phascolosoma vermiculum.—Baird, 1868:85. Sipunculus vermiculus. —Stephen and Edmonds, 1972:339. Phascolosoma (Phascolosoma) vermiculus.—Saiz, I984a:90~97. Phymosoma dentigerum Selenka and de Man, in Selenka et al., 1883:6768. Phascolosoma dentigerum.—Fisher, 1952:432-434. Physcosoma thomense Augener, 1903:343-344. Phascolosoma thomense. —Murina, 1967^.44-45. Phascolosoma (Phascolosoma) thomense.— Stephen and Edmonds, 1972:327. Aspidosiphon insularis Lanchester, 1905^40. Paraspidosiphon insularis. —Stephen and Edmonds, 1972:247. Physcosoma microdentigerum ten Broeke, 1925:88-89. Phascolosoma (Antillesoma) microdentigerum.—Stephen and Edmonds, 1972:280281. Phascolosoma spinosum Johnson, 1971:601-602.
Genus Phascolosoma
183
DESCRIPTION. The reddish, conical, posteriorly directed preanal papillae on the dorsal base of the introvert characterize this species (Fig. 46D, F). The hooks are in 15-25 rings (8-10 rings in 5-mm worms), 30-60 (xm tall, and have a large, rounded secondary tooth (Figs. 43B, 50A). The internal triangle is separate from the clear streak. The often thin-walled trunk, through which the longitudinal muscle bands are visible, is commonly up to 35 mm long, rarely 45-50 mm. The introvert is equal to or shorter than the trunk and usually displays patches of dark reddish pigment on the dorsal surface. DISTRIBUTION. Common in the Caribbean (Venezuela to southern Florida) and the western Pacific (Queensland to Vietnam and central Japan); also recorded from many Indian Ocean locations and in the eastern Pacific off Panama and northern Mexico. Two eastern Atlantic records complete this circumtropical but patchy and disjunct distribution.
Phascolosoma saprophagicum Gibbs, 1987 Phascolosoma (Phascolosoma) saprophagicum Gibbs, 1987:135-137.N. Cutler and Cutler, 1990:717. DESCRIPTION. Hooks are small (20-25 |xm), bluntly rounded, with a simple narrow internal clear streak (Fig. 49H). The papillae are small and inconspicuous; the nephridiopores are anterior to the anus by up to 10% of the trunk length; and the ventral retractor muscles originate in the posterior quarter of the trunk. DISTRIBUTION. Chatham Islands, New Zealand, at 880 m, from a decaying whale skull. Phascolosoma scolops (Selenka and de Man, 1883) Phymosoma scolops Selenka and de Man, in Selenka et al., 1883:75-76. Physcosoma scolops.—Shipley, i898:470.-Sato, i 9 3 o : n - i 5 . - L e r o y , 1942:10-19. Phascolosoma scolops.—Wesenberg-Lund, 19573:5.-Stephen, i965:83.-Edmonds, 1980:55-60. Phascolosoma (Phascolosoma) scolops scolops.—Stephen and Edmonds, 1972:321-323. Phascolosoma (Phascolosoma) scolops.—E. Cutler, 1977c: 152-153.-E. Cutler and Cutler, 1979b: 108-109.-N. Cutler and Cutler, 1990:717-719.Saiz, 19843:206-208. Phymosoma scolops van mossambiciense Selenka, in Selenka et al., 1883:76. Physcosoma scolops var. mossambiciense.—Sluiter, 1898:
184
The Phascolosomatids
444. Phascolosoma (Phascolosoma) scolops mossambiciense.—Stephen and Edmonds, 1972:324. Physcosoma scolops var. adenticulatum Herubel, 1904^563. Phascolosoma (Phascolosoma) scolops adenticulatum.—Stephen and Edmonds, 1972:323-324. Phascolosoma carneum Leuckart and Ruppell, 1828:7. Sipunculus (Phymosomum) guttatus de Quatrefages, i865b:62i. Phascolosoma guttatum Stephen and Edmonds, I972:339.-Saiz, 19843:206. Phymosoma psaron Sluiter, 1886:505. Physcosoma psaron.—Sluiter, 1902:13. Phascolosoma (Phascolosoma) psaron.—Stephen and Edmonds, 1972:319. Physcosoma spongicola Sluiter, 1902:16-17. Phascolosoma (Phascolosoma) spongicolum.—Stephen and Edmonds, 1972:325-326. Phymosoma nahaense Ikeda, 1904:29-31. Phascolosoma (Rueppellisoma) nahaense.—Stephen and Edmonds, 1972:274. Physcosoma socium Lanchester, 19050:37-38. Phascolosoma (Phascolosoma) socium.—Stephen and Edmonds, 1972:324-325. Phascolosoma rottnesti Edmonds, 1956:282-284. Phascolosoma (Phascolosoma) rottnesti.—Stephen and Edmonds, 1972:320-321. Phascolosoma dunwichi Edmonds, 1956:292-293. Phascolosoma (Phascolosoma) dunwichi.—Stephen and Edmonds, 1972:300-301. Phascolosoma riukiuensis Murina, 1975^55-57. DESCRIPTION. Usually small (10-20 mm), pale worms with distinct reddish brown, dome-shaped to mammiform preanal papillae at the base of the introvert (Fig. 46B). The introvert is commonly shorter than the trunk and exhibits pigmented bands. The mid-trunk papillae are small and widely scattered, but their size, color, and density increase posteriorly. The hooks, 20-60 (xm tall, are arranged in fewer than 25 rings, and the secondary tooth is small if present (Figs. 43C, 50F). The clear streak is separate from the distinct triangle. Apart from hook morphology there are two minor internal differences from the similar P. albolineatum: a rectal caecum is present in more than half the worms (vs. 10% in P. albolineatum), and the ventral retractor origins are closer to the posterior end of the trunk (around 60% vs. 50%). There are reports of loss or fusion of dorsal retractors in this species and of nephridia with an anterior lobe (E. Cutler et al., 1984). DISTRIBUTION. Common throughout the Indo-West Pacific, including the Red Sea, north to northern Japan, south to northern Australia, and east to Hawaii. Usually found at intertidal and shallow depths (<30 m) in soft rocks. The 70 or so worms recorded from western Africa (Gulf of Guinea and south) cannot all be verified; at least some are P. stephensoni.
Genus Phascolosoma
185
Phascolosoma stephensoni (Stephen, 1942) Physcosoma stephensoni Stephen, 1942:250. Phascolosoma stephensoni. —Wesenberg-Lund, 1963:121-126. Phascolosoma (Phascolosoma) stephensoni.—Stephen and Edmonds, 1972:326-327.-Edmonds, 1980: 67-68.-Saiz, 19860:63-70; I993:i22-I25.-N. Cutler and Cutler, i99o:7i9-720.-Haldar, 1991:70-72. Phascolosoma laeve.—Keferstein, 18625:38-39 (in part). Sipunculus (Phymosomum) spinicauda de Quatrefages, 18650:621. Phascolosoma spinicauda Baird, 1868:93. Physcosoma lanzarotae Harms, 1921:307 (in part). Phascolosoma heronis Edmonds, 1956:293-295. Phascolosoma (Phascolosoma) heronis.—Stephen and Edmonds, 1972:309. Phascolosoma granulatum.—Murina, 1981:13-14. DESCRIPTION. The distinctive smooth, conelike preanal and posterior papillae distinguish P. stephensoni from the similar P. granulatum, which is sympatric for part of its range (Fig. 46E). Under the light microscope these papillae show none of the platelets typical of this genus. The smaller papillae in the mid-trunk have only very small granules of uniform size, not platelets. The introvert has irregular pigmented bands and more than 40 rings of hooks, 60-110 p,m tall. There may be only 10-20 complete rings; the rest are dorsal patches only. The internal clear streak is smooth, the triangular space is clear, and posterior to the clear streak is a distinct clear crescent (Fig. 44). The hooks vary in shape, the proximal ones being more scattered, blunter, smaller (30-45 |xm), and more triangular, and the crescentic clear area is often not present. In most hooks the secondary tooth is present and distinct. DISTRIBUTION. A somewhat disconnected distribution, from the Mediterranean Sea (Sicily and southern Spain), eastern Atlantic (Azores, Canaries, Gulf of Guinea to South Africa), western and northwestern Indian Ocean (Durban, Mozambique, Somalia, southwestern India), and western Pacific (northern Australia, Solomon Islands, and Hawaii).
Phascolosoma turnerae Rice, 1985 Phascolosoma turnerae Rice, 1985^54-60. Phascolosoma (Phascolosoma) turnerae.—N. Cutler and Cutler, 1990:720. Phascolosoma (Phascolosoma) kapalum Edmonds, 1985:43-44. DESCRIPTION. The sharply bent hooks, 45-80 \xm tall, have as many as 10 long posterior basal processes or rootlets. Under the light microscope
The Phascolosomatids
186
these look like warts (Fig. 49C), and the anterior base is drawn out into a thin, pronglike extension. The clear streak is close to the anterior side and often narrows toward the base. The trunk papillae appear large and mammillate with prominent apical protuberances. DISTRIBUTION. Gulf of Mexico off Florida, Alabama, and Louisiana, at 370-1200 m in wood or near cold-water seeps. Also found at 700 m off New South Wales. Genus Antillesoma (Stephen and Edmonds, 1972) Phascolosoma (Antillesoma) Stephen and Edmonds, I972:277.-E. Cutler and Cutler, 1983:176. Antillesoma.—E. Cutler and Gibbs, 1985:163.Gibbs and Cutler, 1987:55. DIAGNOSIS. Introvert variable in length, often about equal to trunk, adults without hooks. Body wall with longitudinal muscle layer divided into anastomosing bands. Numerous tentacles (>30 in adults) enclose the nuchal organ. Contractile vessel with many villi. Four introvert retractor muscles, lateral pairs often extensively fused. Spindle muscle attached posteriorly. Two nephridia. One species, small to medium sized, up to 80 mm long. TYPE SPECIES. Phascolosoma antillarum Griibe and Oersted, 1858. Morphological Characters of Antillesoma In general, the ecology and external morphology are very similar to those of several species of Phascolosoma. It is important not to confuse the real digitiform contractile vessel villi seen in this genus with the bulbous vesicular swellings present in a few Phascolosoma species. The number of retractor muscles is sometimes unclear. There is often a high degree of fusion along much of the length of each lateral pair (right and left), and as a result, it may appear as though there is only one muscle on each side, each with a small bifurcation near its origin. The degree of fusion or separation of these muscles is quite variable (Fig. 52D-F). Antillesoma antillarum (Griibe and Oersted, 1858) Phascolosoma antillarum Griibe and Oersted, 1858:117-118.-Fisher, 1952:434-436. Phymosoma antillarum.—Selenka et al., 1883:57. Physcosoma antillarum.—Gerould, 1913:420-421. Phascolosoma (Antil-
Figure 52. Antillesoma antillarum. A. Whole worm; note coarse papillae, especially around the anterior end of the trunk. B. Enlarged view of distal introvert showing absence of hooks in adult, smooth collar, and numerous nuchal tentacles (after E. Cutler and Cutler, 1981, courtesy of Seto Marine Biological Laboratory). C. Internal view with diagnostic contractile vessel villi; anastomosing longitudinal muscle bands omitted (after Keferstein, 1865; abbreviations as in Figure 1). D-F. Variations in retractor muscle configurations (from E. Cutler and Cutler, 1983, courtesy of the Linnean Society). D. Specimen with distinctly separated dorsal and ventral muscles. E. Specimen with very indistinct separation between dorsal and ventral origins. F. The left pair of retractor muscles from a worm showing very little separation between the dorsal and ventral origins; note three short subdivisions on the ventral muscle.
i88
The Phascolosomatids
lesoma) antillarum.—Stephen and Edmonds, l972:278-279.-Tarifeno andRojas, 1978:119-121.^. Cutler and Cutler, 1983:182-184. Antillesoma antillarum.—E. Cutler et al., I984:290.-Haldar, 1991:44-47. Phascolosoma fuscum.—Keferstein, 1862:67. Sipunculus (Aedematosomum) glans de Quatrefages, i86sb:626. Phascolosoma glans Baird, i868:96.-Stephen and Edmonds, 1972:339.Saiz, 19843:160-165, 217-218. Sipunculus (Aedematosomum) immodestus de Quatrefages, 1865^627. Phascolosoma immodestum Baird, i868:96.-Saiz, 19843:166-168; I984d:30-3i. Phascolosoma nigriceps Baird, 1868:90. Phymosoma asser Selenka and de Man, in Selenka et al., 1883:59-60. Physcosoma asser.—W. Fischer, 1895:12. Phascolosoma asser.—Stephen and Edmonds, i972:279~28o.-E. Cutler and Cutler, 1983:178. Phymosoma pelma Selenka and de Man, in Selenka et al., 1883:60. Physcosoma pelma.—Sluiter, 1902. Phascolosoma pelmum.—Stephen and Edmonds, i972:28i-282.-E. Cutler and Cutler, 1983:179. Physcosoma weldoni Shipley, 18923:77-78. Phascolosoma weldoni.— Stephen and Edmonds, 1972-.277.-E. Cutler and Cutler, 1983:182. Phymosoma onomichianum Ikeda, 1904:26-28. Physcosoma onomichianum.—Sato, 1934^247. Phascolosoma onomichianum.—WesenbergLund, I959c:67.-Stephen and Edmonds, 1972:275.-E. Cutler and Cutler, 1981:86-88; 1983:181. Physcosoma gaudens Lanchester, 1905^38. Phascolosoma gaudens.— Stephen and Edmonds, I972:274.-E. Cutler and Cutler, 1983:180. Physcosoma similis Chen and Yeh, 1958:274-276. Phascolosoma simile. —Stephen and Edmonds, I972:276.-E. Cutler and Cutler, 1983:182. Golfingia mokyevskii Murina, 1964:256-259. lAspidosiphon mokyevskii.— Gibbs et al., 1983:302.-E. Cutler and Cutler, 1989:838. Phascolosoma schmidti Murina, I975b:57.-E. Cutler and Cutler, 1983: 179. DESCRIPTION. The trunk is commonly 15-30 mm long but may be up to 80 mm; its width is equal to 10-25% of its length. The introvert length is 65-75% of the trunk length in living animals, but in preserved material it may appear to be only 20-25%. Th e trunk is yellow-brown with many large, dark papillae; these are especially large and crowded near the anterior end (Fig. 52A). The introvert also bears dark papillae on its proximal portion, but the distal part is smooth and white (Fig. 52B) and marked off by a distinctive collar. Numerous (30-200) digitiform tentacles surround
Genus Apionsoma
189
the dorsal nuchal organ. Tentacles vary in number according to the animal's size (E. Cutler and Cutler, 1981), and they have violet pigment (brown in preserved specimens) distributed in patches or stripes on each tentacle. This pigment usually extends onto the area around the nuchal organ. Hooks are absent in adults, but a few small, scattered hooks have been observed in very small individuals (
Genus Apionsoma Sluiter, 1902 Apionsoma Sluiter, 1902:42.-E. Cutler et al., I984:299.-Gibbs and Cutler, 1987:55. Golfingia (Apionsoma) Murina, I975d:i748.-E. Cutler, 1979: 382. Golfingia (Mitosiphon) Fisher, i95oa:55o.-Stephen and Edmonds, 1972: 113.-E. Cutler, 1973:139. Golfingia (Phascolana) Wesenberg-Lund, 1959a: 183.-Stephen and Edmonds, 1972:116. DIAGNOSIS. Tentacles forming a crescent around nuchal organ dorsal to mouth. Contractile vessel without villi. Four introvert retractor muscles. Introvert much longer than trunk, with rings of recurved hooks (absent in
190
The Phascolosomatids
A. trichocephalus) that have accessory spinelets at the bases. Two bilobed nephridia. Species small, most less than 20 mm in trunk length (but one up to 80 mm). Body wall musculature continuous or in separate bands. See Figures 53 and 54. TYPE SPECIES. Apionsoma trichocephalus Sluiter, 1902. NOMENCLATURAL NOTE. E. Cutler (1979) reviewed this taxon, which was later elevated to generic status by E. Cutler and Gibbs (1985). Included in Apionsoma are species previously assigned to the putative Golfingia subgenus Mitosiphon Fisher (see E. Cutler, 1973). The placement of these species within the genus Golfingia was based on the weight given to the continuous body wall musculature. Their present placement in Phascolosomatidae more heavily weights the tentacles, hooks, and spindle muscle attachment. The decision to move the former Fisherana species as a subgenus to Phascolosoma, and the former Phascolosoma subgenus Edmondsius into Apionsoma, was made after preparing a cladistic analysis and giving less significance to the homoplastic formation of bands in the body wall muscle layers. The two genera thus created are much more cohesive than previously. The following names are herein added to the list of species inquirenda. Reservations were expressed about their status in previous generic revisions, and no justification has emerged in the intervening years for retaining them as valid, meaningful entities. Apionsoma immunitum (Sluiter, 1902) Phascolosoma immunitum Sluiter, 1902:40-41. Golfingia (Siphonoides) immunita Murina, 1967^1334; Stephen and Edmonds, 1972:159. Golfingia (Apionsoma) immunita.—E. Cutler et al., 1983:670-671. This enigmatic species was most recently moved to Apionsoma, but the Figure 53. Apionsoma. A. A. trichocephalus. B. A. murinae with esophagus protruding through mouth and with nuchal tentacles. C. A. (Edmondsius) pectinatum with introvert partly retracted. D-F. Enlarged views of distal introverts with dorsal nuchal tentacles, esophagus protruding through mouth, and rings of hooks. D. Scanning electron micrograph of A. misakianum. E. A. murinae shown in B. F. A. (Edmondsius} pectinatum; although tentacles may appear to be a complete circle, they actually form an arc. E, esophagus; TC, tentacular crown. (A from E. Cutler, 1973, courtesy of the American Museum of Natural History; B and E after E. Cutler and Cutler, 1979a, courtesy of the Mus6um National d'Histoire Naturelle; D from E. Cutler, 1979, courtesy of the Linnean Society; C and F drawn by L. Leibensperger.)
Genus Apionsoma
193
condition of the single type specimen is imperfect, no new material has been collected, and even though the hooks are in rings with short spinelets, it otherwise more closely resembles Phascolosoma (Fisherana) capitatum. It is added to the list of species inquirenda pending future clarification. Apionsoma papilliferum (Keferstein, 1865) Phascolosoma papilliferum Keferstein, 1865^433-434. Fisherana papillifera.—Stephen and Edmonds, 1972:332. Golfingia (Apionsoma) papillifera.—E. Cutler, 1979:374-376. Phascolosoma dissors Selenka and de Man, 1883:31-32. The type material cannot be located, and there is good reason to doubt the validity of this taxon (see E. Cutler, 1979). Apionsoma reconditum (Sluiter, 1900) Phascolosoma reconditum Sluiter, 1900:11-12. Golfingia recondita.— Stephen and Edmonds, 1972:105. Golfingia (Apionsoma) recondita.— E. Cutler, 1979:372-373The original (and only) material is unavailable, and there are unanswerable questions about certain character states (see E. Cutler, 1979). Morphological Characters of Apionsoma Introvert Hooks. When present, hooks have the distinctive form with basal spinelets (Fig. 54A-C). The hooks are rather small and transparent, and thus easily overlooked. One must be sure to look very near to the distal end of the introvert because the area covered by the rings is often small.
Figure 54. Apionsoma. A. Hooks of A. misakianum showing first three rings in different stages of development; new ones are erupting at anterior margin. B. Hooks from the tenth ring on the worm shown in A (from E. Cutler and Cutler, 1979a, courtesy of the Museum National d'Histoire Naturelle). C. Introvert hook of A. (Edmondsius) pectinatum (ca. 50 u,m) with basal spinelets; the number may vary from 4 to 8. D. Internal organs of Apionsoma (Edmondsius) pectinatum; longitudinal muscle bands (LMB) are present but not shown here (from Fisher, 1952, courtesy of Smithsonian Institution Press). This basic organization exists in the other subgenus; however, LMBs are lacking and the spindle muscle attaches to the posterior end of the trunk. The length of the secondary nephridial lobe varies considerably. Abbreviations as in Figure 1.
The Phascolosomatids
194
Introvert Length. Obtaining an accurate measurement of this very elastic body region is not easy, and underestimates are common, especially in animals whose introvert is withdrawn. The introvert often exceeds the trunk length by more than three times. When the introvert is partially withdrawn, the "head" is located by following the retractor muscle and seeing where the nature of the inverted tube changes. It is often best to do this under a dissecting microscope with transmitted light. When comparing species, be sure to use comparable data, not values from contracted worms in one case and extended worms in the other. Papillae. The posterior trunk papillae range from barely perceptible to mammiform. This is a useful and rather distinctive attribute, but variation also occurs within populations since papillae size is correlated with the size of the individual. Key to Apionsoma Species i. Body wall muscles divided into separate bands A. (Edmondsius) pectinatum - Body wall with continuous muscle layers
A. (Apionsoma), 2
2. Papillae, hooks, and tentacles absent
A. trichocephalus
- Papillae, hooks, and tentacles present 3 3. Introvert usually more than nine times trunk length; body wall thin, semitransparent, with small papillae A. misakianum - Introvert less than seven times trunk length; body wall thick, opaque, with large papillae (Fig. 53B) A. murinae
Subgenus Apionsoma (Apionsoma) Sluiter, 1902 Apionsoma Sluiter, I902:42.-E. Cutler et al., 1984:299. Golfingia (Mitosiphon) Fisher, i95oa:550.-Stephen and Edmonds, 1972: 113Golfingia (Phascolana) Wesenberg-Lund, I959a:i83.-Stephen and Edmonds, 1972:116. DIAGNOSIS. Body wall with continuous muscle layers. Spindle muscle attached to posterior end of the trunk. TYPE SPECIES. Apionsoma trichocephalus Sluiter, 1902.
Genus Apionsoma
195
Apionsoma misakianum (Ikeda, 1904) Phascolosoma misakianum Ikeda, 1904:7-9. Golfingia (Mitosiphon) misakiana.—Stephen and Edmonds, 1972:115-116.-E. Cutler and Cutler, i979a:955-956.-Edmonds, 1980:22-23. Golfingia (Apionsoma) misakiana.—E. Cutler, 1979:370-372. Apionsoma misakiana.—E. Cutler et al., 1984:300-301. Phascolosoma hespera Chamberlain, 19203:31. Golfingia hespera.— Fisher, 1952:392-395.-Stephen and Edmonds, I972:ii3-H5.-E. Cutler, 1979:37°Golfingia (Phascolana) longirostris Wesenberg-Lund, 1959a: i86.-Stephen and Edmonds, I972:u6-H7.-E. Cutler, 1973:143-144. Golfingia (Phascolana) tenuissima Wesenberg-Lund, 19593:183-186.Stephen and Edmonds, 1972:117-118. DESCRIPTION. Small and spindle shaped, commonly 3-8 mm (one Indian worm is 49 mm), with thin skin and an introvert 7-10 times the trunk length (Fig. 53D). The posterior end of the trunk has numerous distinctive papillae. The most distal rings of small (15-25 am) hooks have six to eight basal spinelets, but proximal hooks have fewer, and some have none. According to an ontogenetic sequence suggested by E. Cutler (1979), hooks in young worms may not be in rings and may lack spinelets; succeeding hooks develop in rings and have more and more spinelets. The hooks near the tip are in early stages of their growth and are not yet fully erupted, and thus show less than their final complement of spinelets (Fig. 54A, B). The nephridia are bilobed in almost all adult worms, but in young animals the second lobe may not be developed. The four thin retractor muscles are about equidistant from the ventral nerve cord near the middle of the trunk. DISTRIBUTION. Widespread but not common in intertidal coral sands, coralline algae, under algal mats in tidal pools, and at shelf depths in tropical and subtropical waters of the Indian (East Africa, Madagascar, western India, western Australia), Pacific (Japan, French Polynesia, California, Peru), and western Atlantic oceans (Gulf of Mexico and Brazil).
Apionsoma murinae murinae (E. Cutler, 1969) Golfingia (Mitosiphon) murinae unilobatae E. Cutler, 1969:213-215. Golfingia (Mitosiphon) murinae murinae.—E. Cutler, 1973:145-146.-
196
The Phascolosomatids
Murina, 1973:67; 1978:123. Golfingia (Apionsoma) murinae murinae.—E. Cutler, I979:369~370.-E. Cutler and Cutler, 198015:451. Apionsoma murinae murinae.—E. Cutler and Cutler, 19875:73. Golfingia hespera.—Murina, 19645:228; 19670:1335; 196815:197. DESCRIPTION. These small, spindle-shaped worms (trunks
Genus Apionsoma
197
(Mitosiphon) trichocephala.—E. Cutler and Cutler, 19793:956-957.Edmonds, 1980:23. Golfingia (Apionsoma) trichocephala.—Murina, I 9 7 7 : I 8 O . - E . Cutler, 1979:373. Apionsoma trichocephala.—E. Cutler et al., 1984:301-302.-Haldar, 1991:73-75.-^ Cutler et al., 1992:156. Phascolosoma pusillum Sluiter, 1912:14. Golfingia (Golfmgiella) pusilla Stephen and Edmonds, I972:i20.-E. Cutler and Murina, 1977:177. DESCRIPTION. In size (<8 mm), shape (slender spindle), form (very long introvert, 8-14 times the trunk; see Fig. 53A), and habitat (tropical and subtropical intertidal sand) A. trichocephalus resembles A. misakianum, but the former apparently has neither hooks nor tentacles. The posterior end of the trunk is smooth and bears only scattered low, round, or elliptical papillae. The two pairs of retractor muscles are thin and attach equally close to the ventral nerve cord near the middle of the trunk, negating the appellations ventral and dorsal. The anus is shifted toward the middle of the trunk, so the nephridiopores are used to mark the anterior end. The two long lobes of each nephridium are usually of equal length, although occasionally one is shorter, especially in young worms. DISTRIBUTION. Southeastern United States and Gulf of Mexico, West and South Africa, Madagascar, Arabian Sea, Gulf of Aden, India, Vietnam, central and southern Japan, Indonesia, northern Australia, and New Zealand. Unknown from the central Pacific, but recently collected in Costa Rica. A circumtropical sand-dwelling species found at intertidal depths to 100 m.
Subgenus Apionsoma (Edmondsius) (Gibbs and Cutler, 1987) Phascolosoma (Edmondsius) Gibbs and Cutler, 1987:54.-!^. Cutler and Cutler, 1990:693. Phascolosoma (Satonus) Stephen and Edmonds, 1972:282 (in part). DIAGNOSIS. Body wall musculature divided into bundles. Spindle muscle not attached posteriorly. TYPE SPECIES. Phascolosoma pectinatum Keferstein, 1867. Apionsoma (Edmondsius) pectinatum (Keferstein, 1867) Phascolosoma pectinatum Keferstein, 1867:47-48. Phymosoma pectinatum.—Selenka et al., 1883:65-67. Physcosoma pectinatum.—W. Fischer, 1895:12. Phascolosoma (Satonus) pectinatum.—Stephen and
198
The Phascolosomatids
Edmonds, i972:287-289.-E. Cutler, 1977a: 150. Phascolosoma (Edmondsius) pectinatum.—N. Cutler and Cutler, 1990:693. Phascolosoma abnorme Sluiter, 1886:513. Golfingia (Golfingiella) abnormis Stephen and Edmonds, I972:n8.-E. Cutler and Murina, 1977:175. Siphonides rickettsi Fisher, 1952:386-388.-Wesenberg-Lund, 1959^6366.-Stephen and Edmonds, 1972:287. DESCRIPTION. This species is easily identified by the bilobed nephridia, spindle muscle not attached to the posterior end of the trunk, and hooks commonly with seven to nine basal spinelets (Figs. 53C, F; 54C, D). The introvert is two to four times longer than the trunk, which may be up to 80 mm long, and the longitudinal muscle bands, while present, are often soft or flabby. The skin is softer than that found in other members of the Phascolosomatidae and has large, dome-shaped papillae, which in larger worms may be in a square of folded skin. Some hooks may not have the basal spinelets, so one must examine several series to be certain of the identity. DISTRIBUTION. An uncommon circumtropical, shallow-water species from the Caribbean, Azores, Mauritius, Mayotte, Indonesia, Malaya, East China Sea, Panama, and Baja California.
7
The Aspidosiphonids
Order Aspidosiphoniformes E. Cutler and Gibbs, 1985 Phascolosomatidea with the anterior trunk hardened to form a horny or calcareous anal shield. Two retractor muscles. Family Aspidosiphonidae Baird, 1868 Characters are those of the order. Most species live in soft rock or coral burrows or in vacated mollusk shells in warm water. They are generally small (5-30 mm), with smooth trunks having some kind of cuticular elaborations at one or both ends. In all but one species the introvert protrudes at an angle of 45-90 0 ventral to the main axis of the trunk. If everted, the introvert provides a good clue to familial identity. Familial Traits Body Wall Musculature. The muscle layers are smooth and continuous in many members of this family (i.e., the one Cloeosiphon species and most Aspidosiphon species). The two Lithacrosiphon species and one subgenus of Aspidosiphon have the longitudinal muscle layer separated into anastomosing bundles. In several species this layer partially splits or fractures into bundles under or near the anal shield, but this is not a clear-cut character state in all worms. Anal Shield. The presence of some form of hardened structure at the anterior end of the trunk is assumed to be a shared derived character (synapomorphy); however, this calcareous or horny protein shield could be an example of parallel or convergent evolution (homoplasy). It clearly has adaptive value since it functions as a protective operculum to plug the opening of the worm's shelter when the introvert is withdrawn.
The Aspidosiphonids
200
Key to Aspidosiphonidae Genera i. Introvert protrudes from center of anal shield; shield calcareous (white) composed of numerous polygonal plates Cloeosiphon - Introvert protrudes from ventral margin of anal shield 2. Shield composed of single calcareous cap
2 Lithacrosiphon
- Shield composed of numerous horny (usually brown-black) plates Aspidosiphon
Genus Aspidosiphon Diesing, 1851 Aspidosiphon Diesing, 1851:67-68. Pseudaspidosiphon Baird, 1868:102 (in part). DIAGNOSIS. Introvert usually longer than trunk. Recurved hooks in numerous rings (absent in three species, scattered in two). Trunk with anal shield composed of hardened units which may be inconspicuous. Introvert protrudes from ventral margin of shield. Body wall either with continuous longitudinal muscle layer or with longitudinal muscle layer separated into anastomosing, sometimes ill-defined bundles. Tentacles enclose dorsal nuchal organ but not mouth. Contractile vessel without villi. Two introvert retractor muscles may be almost completely fused. Spindle muscle attaches posteriorly. Two nephridia. One species may exceed 100 mm, but most are less than 40 mm long. See Figures 55-63. TYPE SPECIES. Aspidosiphon muelleri Diesing, 1851. NOMENCLATURAL NOTE. The name Paraspidosiphon was proposed by Stephen (1964) as a genus for species with the longitudinal muscle layer separated into bundles. That genus was later reduced to subgeneric level (E. Cutler, 1973) along with Aspidosiphon s. s. A third subgenus (Akrikos)
Figure 55. External forms of two of the subgenera of Aspidosiphon. A. A. (Aspidosiphon) elegans, which lacks LMBs. Not all species have dark introvert papillae, and the introvert is commonly much thinner than the trunk. B. A. (Paraspidosiphon) steenstrupii; LMBs are usually visible through body wall. C. A. (A.) gosnoldi taken from gastropod shell. D. Anal shield of A. gosnoldi (width about 2 mm). E. Distal tip of introvert from A. muelleri showing dorsal crescent of nuchal tentacles. A, anus; AS, anal shield; C, collar; CS, caudal shield; H, hooks in rings; I, introvert; M, mouth. (C and D from E. Cutler, 1981, courtesy of the Biological Society of Washington; E from Gibbs, 1977b, courtesy of the Linnean Society.)
D
Figure 56. Two Aspidosiphon (Akrikos) species. A. A. zinni, a very small deep-sea worm, along with an enlarged portion of its fine-grained anal shield (scale = 0.5 mm). B. A. thomassini, with ill-defined and easily overlooked anal shield. C and D. Two extremes of anal shield development in A. thomassini. A, anus; AS, anal shield; IN, intestine. (A after E. Cutler, 1969, courtesy of the Biological Society of Washington; B-D from E. Cutler and Cutler, 1979a, courtesy of the Museum National d'Histoire Naturelle.)
Genus Aspidosiphon
203
Figure 57. Internal organization of Aspidosiphon. A. A. (Aspidosiphon) muelleri with splits or fractures in the longitudinal muscle layer in the anterior end of the trunk (after Gibbs, 1977b, courtesy of the Linnean Society). B. A. elegans with continuous muscle layers (from Selenka et al., 1883). Abbreviations as in Figure 1. was proposed for species that lack hooks in rings (E. Cutler and Cutler, 1989). Morphological Characters of Aspidosiphon Introvert Hooks and Spines. Most species have hooks arranged in regular rings around the distal introvert. These may be either unidentate or bidentate (i.e., with one or two pointed teeth). Some species also have scattered hooks proximally, and two, A. mexicanus and .A. zinni, have only scattered hooks. Epidermal structures of varying sizes and shapes, previously called spines, are arranged randomly on the proximal portion of some introverts. In this book, the term spine refers only to the conical pointed anal shield units. The hook apex points posteriorly, away from the mouth, so the convex curvature is anterior.
204
The Aspidosiphonids
Figure 58. SEM and light microscope photographs of Aspidosiphon introvert hooks. A. Compressed, bidentate, type A hooks of A. muelleri (scale = 10 \xm). B. Compressed, unidentate, type A hooks of A. misakiensis (scale = 10 u.m). C and D. Conical type C hooks of A. elegans (scale = 10 (im). E. Pyramidal type B hooks of A. parvulus (scale = 10 fxm). F. Pyramidal type B hooks of A. steenstrupii viewed from above (scale = 10 |Am). G. A. steenstrupii hooks viewed from a variety of angles (scale = 20 n-m). (From E. Cutler and Cutler, 1989, courtesy of the Biological Society of Washington.)
Genus Aspidosiphon
205
The three hook types are defined as follows (from E. Cutler and Cutler, 1989): TYPE A: COMPRESSED. Usually arranged in rings, occasionally scattered, laterally compressed, and with a distinct posterior curve in side view. Hooks may be unidentate or bidentate (Fig. 58A, B). When present, the secondary tooth can vary in size and is sometimes reduced to a small knob. Some species have a transition zone at the proximal end of the rings of hooks in which a gradual widening of the anterior base of the unidentate hooks is evident. TYPE B: PYRAMIDAL. Hooks with triangular bases, the anterior side of which is shorter than the lateral sides. They are usually less curved than type A or C hooks and are variably pigmented (dark to light) and translucent (Fig. 58E-G). The borderline between types A and B is not clear in all species. TYPE C: CONICAL. Hooks with a nearly circular cross section, a gentle posterior curve, and usually opaque and dark (Fig. 58C, D). This hook type is found on the dorsal side of the introvert in A. elegans. Orientation is important when introvert skin is removed and placed on a slide in a drop of glycerin for close examination. Viewed from the anterior or posterior instead of from the side, scattered unidentate compressed hooks can appear pyramidal. Hook size should not be considered in isolation from trunk size, since larger worms tend to have larger hooks. Despite this, a clear pattern does appear in certain species. For example, the hook-bearing members of the subgenus A. (Akrikos) always have small hooks (<30 (xm), and some species from other subgenera have only large hooks. On the other hand, many species have both large and small hooks. In summary, some species lack unidentate hooks and some lack bidentate hooks; some have both type A and type B hooks while others have only type A hooks; others have both unidentate and bidentate type A hooks and type B hooks. Hook morphology can be a useful characteristic if one examines distal rings of hooks and differentiates between unidentate type A and type B hooks, and hook size can help to identify a few species. Anal Shield. A few species (e.g., A. mexicanus and A. thomassini) have a shield composed of small, scattered units that resembles rough skin. At the other end of the continuum are species whose shield units are compacted to form a thick, dark, solid mass. A. laevis and most A. muelleri are in the latter group and are also among the species that have shields with
206
The Aspidosiphonids
A B Figure 59. Caudal shields of A. steenstrupii (from E. Cutler and Cutler, 1979a, courtesy of the Museum National d'Histoire Naturelle). A. Specimen with relaxed trunk muscles. B. Specimen with contracted circular muscles. well-developed longitudinal or transverse grooves, or both (Fig. 60B, C). Aggregations of units separated by grooves are called plates. The shield region nearest the mid-dorsal anus is considered the dorsal part, and that nearest the introvert is ventral. The nature of the shield units may change with age (see A. jukesii, in E. Cutler and Cutler, 19793:970), and the overall shape may be modified by the size or shape of the shelter occupied by the worm. Caudal Shield. The posterior end of the trunk in some species has an epidermal structure of horny protein. This pliable shield assumes various forms in living worms, and when preserved it can vary from rather flat to pointed or pagoda shaped. The degree of development or thickness varies within demes (Fig. 59). Some species always have a caudal shield; some never do. The caudal shield architecture has little value to the systematist, but its presence or absence can be a useful character. Introvert Retractor Muscles. One pair of muscles originates from the ventral trunk wall in the posterior third of the animal, and the location of their origins is sometimes a diagnostic character. In some species this value (percentage of the distance toward the posterior end of the trunk) remains reasonably constant over a wide range of trunk sizes. Other species exhibit variation that is clearly not correlated with size. This attribute may be useful for differentiating subsets within the genus, but it does not have value at the species level.
Genus Aspidosiphon
207
Figure 60. Anal shields of Aspidosiphon. A. Ungrooved shield of A. elegans (scale = 0.5 mm). B-C. Grooved shield of A. muelleri (scale = 0.5 mm). D. Cone-shaped units near ventral margin seen in many A. muelleri (scale = 0.1 mm). (From E. Cutler and Cutler, 1989, courtesy of the Biological Society of Washington.)
Nephridia Length. Distinct interspecific differences exist, although there is considerable within-species variation as well. Many species exhibit a broad range of nephridia lengths (e.g., 25-100% of the trunk length, or 45-85%), and the nephridia of six species are half the trunk length or less. A few species have only long nephridia (>85% of the trunk length). With a few exceptions, nephridia length has limited value in species identification.
208
The Aspidosiphonids
AAA
Figure 61. Unidentate type A hooks of several A. laevis from different populations showing variation in shape and size. Hook size is roughly correlated with trunk size (scale = 40 jjim). (After E. Cutler and Cutler, 1989, courtesy of the Biological Society of Washington.) Longitudinal Muscle. The longitudinal muscle layer in two of the three subgenera is an undivided sheet. In the subgenus A. (Paraspidosiphon) this layer is divided into separate bundles, but the dichotomy is not as clear as it sounds. Intermediate conditions of two general types exist. First, the muscle layer in the anterior dorsal trunk is fractured in some A. (Aspidosiphon). Usually this is limited to the area under the anal shield, but the fractures may continue beyond these boundaries for 10-20% of the trunk length. Second, the longitudinal muscle bands are not distinct in some A. (Paraspidosiphon) species. The variation in this regard is much greater than in other genera with muscle bundles. Several species have distinct rarely anastomosing bundles, many exhibit a modest degree of anastomosing, and others show frequent and broad cross-linkages. In the latter species the longitudinal muscle layer appears more like a continuous sheet that has split or fractured than like distinct bundles (e.g., A. fischeri). It is sometimes difficult, especially in small animals, to know whether one is looking at an A. (Paraspidosiphon) with frequently anastomosing bundles or an A. (Aspidosiphon) with fracturing of a continuous layer. This character state may be useful for separating subgenera but not species.
Genus Aspidosiphon
209
Figure 62. Aspidosiphon internal hook structure. A. A. elegans. B. A. steenstrupii. C. A. tenuis without tonguelike extension. Scale = 20 \im. (After E. Cutler and Cutler, 1989, courtesy of the Biological Society of Washington.)
Key to Aspidosiphon Subgenera and Species The subgenera with their included species are presented in a single key to make it easier for the user to cross-check if there is uncertainty about the precise hook arrangement or if there is any question about whether the body wall musculature is continuous or divided. The species descriptions that follow the key are arranged alphabetically within each subgenus. 1. Hooks arranged in rings on distal portion of introvert - Hooks not present, or if present not in rings
2 A. (Akrikos), 3
2. Longitudinal muscles in continuous layer (except under anal shield, Fig. 57) A. (Aspidosiphon), 7 - Longitudinal muscle layer divided into separate (or anastomosing) bundles A. (Paraspidosiphon), 13 3. Introvert hooks absent
4
- Scattered introvert hooks present
6
4. Anal shield of tightly packed, uniform-sized, pale, flat units with distinct angular margin A. albus - Anal shield of dispersed, often dark units, sometimes very poorly developed, with indistinct margin 5 5. Anal shield units distinct, dark, those around margin usually pointed cones A. venabulum - Anal shield units indistinct, widely spaced, flat, sometimes arranged in indistinct rings (Fig. 56B-D) A. thomassini
210
The Aspidosiphonids
6. Anal shield ill-defined and diffuse, trunk usually >5 mm; from shallow, warm water A. mexicanus - Anal shield well defined and compact, trunk usually <5 mm; from deep, cold water (Fig. 56A) A. zinni 7. Anal shield with extensive array of furrows present, not just around margin 8 - Anal shield with randomly distributed hardened units; lacking extensive grooves or furrows 9 8. Individual units form into longitudinal ridges over dorsal half of anal shield (Fig. 60B-D) A. muelleri - Individual units arranged in offset squares or rectangles
A. spiralis
9. All hooks unidentate; ill-defined anal shield
A. gracilis
- Distal hooks bidentate; anal shield distinct
10
10. All compressed hooks bidentate followed by dark conical hooks (Fig. 58C, D) A, elegans - Distal bidentate compressed hooks followed by proximal unidentate ones 11
11. Introvert two to five times the trunk length; nephridia 25-33% trunk length; interstitial habitats A. exiguus - Introvert one to three times trunk length, nephridia >50% of trunk length; occupies coral or shells, often subtidal 12 12. Normal gut helix; lives in gastropod shells; anal shield units not tightly packed and of approximately equal size (Fig. 55C) A. gosnoldi - Gut coils loose or absent; does not occupy gastropod shells; anal shield more solid with close-set, granular units of differing sizes A. misakiensis 13. Anal shield ungrooved or with short marginal grooves only - Anal shield with extensive grooves or furrows 14. Distal hooks bidentate - All hooks unidentate
14 18 15 A. planoscutatus
15. Compressed hooks bidentate followed by dark pyramidal hooks (Fig. 58F) A. steenstrupii - Both unidentate and bidentate type A hooks present, type B hooks pale if present 16 16. No pyramidal hooks; longitudinal muscle bands distinct; compressed hooks
Genus Aspidosiphon
211
>30 n-m tall; retractor origins 75-88% of the distance to the posterior end of the trunk A. tenuis - Pale pyramidal hooks present; longitudinal muscle bands indistinct, hooks <30 urn tall, retractor origins 95-100% 17 17. Anal shield becomes diffuse at margins, with cones or spikes; nephridia length more than half the trunk length A. parvulus - Anal shield with distinct margins, no cones or spikes; nephridia less than half die trunk length A. fischeri 18. All hooks unidentate (Fig. 61), retractor origins not at posterior end (60-80%) A. laevis - Distal hooks usually have very small secondary tooth, retractor origins at posterior end (95-100%) A. coyi
Subgenus Aspidosiphon (Akrikos) E. Cutler and Cutler, 1989 Aspidosiphon (Akrikos) E. Cutler and Cutler, 1989:839. DIAGNOSIS. Without compressed hooks in rings; hooks are either scattered and small (<30 |xm) or absent. Caudal shield absent or very diffuse; longitudinal muscle layer continuous. Not known to live in coral or rock. TYPE SPECIES. Aspidosiphon albus Murina, 1967.
Aspidosiphon (Akrikos) albus Murina, 1967 Aspidosiphon albus Murina, 1967^1330-1331.-Stephen and Edmonds, I972:2i9-22I.-E. Cutler, 1973:174-175. Aspidosiphon (Akrikos) albus.—E. Cutler and Cutler, 1989:839. Aspidosiphon hartmeyeri.—Wesenberg-Lund, 19578:7-8; 19598:197; I959b:2i2. DESCRIPTION. A smooth, white, hookless worm, apparently without tentacles. The trunk may be up to 45 mm long, and the introvert length is three to five times the trunk length. The anal shield is fine grained with small furrows around the margin, but it lacks grooves. A dorsoventral median stripe of darker units is often present on the shield. The nephridia length is 50-75% of the trunk length. DISTRIBUTION. The continental shelf (10-120 m) south from Cape Hatteras, the northern Gulf of Mexico, Cuba, and Brazil. This is the most
212
The Aspidosiphonids
common Aspidosiphon on the Brazilian shelf. Also in the eastern Atlantic from the Gulf of Guinea. Usually occupies discarded mollusk shells. Aspidosiphon (Akrikos) mexicanus (Murina, 1967) Golfingia mexicana Murina, 1967c: 1333-1334. Aspidosiphon mexicana.—E. Cutler et al., 1983:673. Aspidosiphon (Akrikos) mexicanus.—E. Cutler and Cutler, 1989:840. Aspidosiphon longirhyncus E. Cutler and Cutler, 19803:4-6. DESCRIPTION. This species does not clearly exhibit the typical aspidosiphonid appearance; the anal shield is very weakly developed with scattered, ill-defined platelets. The introvert is on a less acute angle to the main trunk axis (ca. 45-600), and the caudal shield is not discernible. The introvert length is four to five times the trunk length and bears scattered, small (<30 \xm), unidentate, compressed hooks. Nephridia are 35-75% of the trunk length. DISTRIBUTION. Southern Brazil, Cuba, and the southeastern United States at shelf depths (80-200 m), plus the Azores at 320 m. Aspidosiphon (Akrikos) thomassini E. Cutler and Cutler, 1979 Aspidosiphon thomassini E. Cutler and Cutler, 19793:971-973. Aspidosiphon (Akrikos) thomassini.—E. Cutler and Cutler, 1989:841. mm mat DESCRIPTION. A small worm (1.5-7 ) appears to have neither hooks nor tentacles on an introvert that is two to four times the trunk length. The retractor muscles are fused for most of their length, and the nephridia length is about 50% of the trunk length. These worms have no caudal shield, and the anal shield is very poorly developed (Fig. 56B-D). It is possible to misidentify this as a Nephasoma species because of the easily overlooked or absent shield and the smaller angle between the trunk and the introvert axis (40-450). DISTRIBUTION. Madagascar and French Polynesia, in intertidal coral sands. Aspidosiphon (Akrikos) venabulum Selenka and Biilow, 1883 Aspidosiphon venabulum Selenka and Biilow, in Selenka et al., 1883:123. Aspidosiphon (Akrikos) venabulum.—E. Cutler and Cutler, 1989:841. Aspidosiphon venabulus.—Stephen and Edmonds, 1972:237.
Genus Aspidosiphon
213
DESCRIPTION. Hookless, with an ungrooved anal shield made up of dark, pointed, conical units more widely scattered than in many species. The shield can resemble the anterior end of certain Phascolion species that have large anterior papillae. The retractor muscles extend to the posterior end, and the longitudinal muscle layer splits into a few bundles under the anal shield. The nephridia length is 60-95% of the trunk length, the latter being up to 30 mm. DISTRIBUTION. Most records are from western Africa, one report from southern Madagascar; at shelf depths (10-55 m> plus one record from the intertidal and one from 960 m).
Aspidosiphon (Akrikos) zinni E. Cutler, 1969 Aspidosiphon zinniE. Cutler, 1969:209-21 i.-E. Cutler and Cutler, 1987b: 73.-Saiz and Villafranca, 1990:1166-1167. Aspidosiphon (Akrikos) zinni.—E. Cutler and Cutler, 1989:841.-Saiz, 1993:141. DESCRIPTION. This slender worm is usually 2-4 mm long (but may be up to 7.5 mm) with a diameter one-tenth to one-fifteenth its length. The indistinct anal shield consists of very fine grained, pale units, and no caudal shield is evident (Fig. 56A). The small (15-20 |xm), scattered, unidentate, compressed hooks and the introvert shorter than the trunk are unusual in members of this genus. A dorsal cluster of small tentacles is present. The nephridia length is less than 25% of the trunk length. This species is often collected along with Nephasoma diaphanes, and since both may occupy foraminiferan tubes and are similar in size and shape, A. zinni can be overlooked, especially if the introvert is not protruding. The flattened anterior end with the pale golden shield does help distinguish these worms. DISTRIBUTION. Common in the northern Atlantic Ocean at depths of 1100-4400 m, plus two records from around 90 S off the Congo River and one in the Mozambique Channel (250 S, at 132 m). Often lives in arenaceous foraminiferan tests.
Subgenus Aspidosiphon (Aspidosiphon) (Diesing, 1851) Aspidosiphon Diesing, 1851:68 (in part). Aspidosiphon.—Stephen, 1964: 457.-Stephen and Edmonds, 1972:216. Aspidosiphon (Aspidosiphon) E. Cutler, I973:i74.-E. Cutler and Cutler, 1989:842.-Haldar, 1991:80.
214
The Aspidosiphonids
DIAGNOSIS. Introvert with compressed hooks in rings; longitudinal muscle layer continuous except near anal shield. Most do not bore in coral or rock. TYPE SPECIES. Aspidosiphon muelleri Diesing, 1851.
Aspidosiphon elegans (Chamisso and Eysenhardt, 1821) Sternaspis elegans Chamisso and Eysenhardt, 1821:351-352. Sipunculus elegans.—de Blainville, 1827:310. Loxosiphon elegans.—Diesing, 1851: 70. Phascolosoma (Aspidosiphon) elegans.—Griibe, i868b:645647. Aspidosiphon elegans.—Selenka et al., 1883:124-i26.-Migotto and Ditadi, 1988:248-250. Aspidosiphon (Aspidosiphon) elegans.— E. Cutler et al., I984:304.-E. Cutler and Cutler, 1989:842. Aspidosiphon elegans elegans.—Stephen and Edmonds, 1972:223.-Edmonds, 1980: 44-46. Aspidosiphon elegans var. yapense Sato, 1935: 316-318. Aspidosiphon elegans yapensis.—Stephen and Edmonds, 1972:224. Aspidosiphon ravus Sluiter, i886:495-496.-Stephen and Edmonds, 1972: 234Aspidosiphon exilis Sluiter, i886:497.-Stephen and Edmonds, 1972:224225. Aspidosiphon spinosus Sluiter, 1902:28.-Stephen and Edmonds, 1972: 235Aspidosiphon brocki Augener, 1903:328-330.-^06, 1970:1618-1620; I975b:44~45.-Stephen and Edmonds, 1972:221. Aspidosiphon spinalis Ikeda, 1904:47-49.-Stephen and Edmonds, 1972: 234-235.-E. Cutler and Cutler, 1981:79-81. Aspidosiphon carolinus Sato, I935:3i8~3i9.-Stephen and Edmonds, I972:222.-E. Cutler and Cutler, 1981:77-78. Aspidosiphon homomyarium Johnson, 1964:332-334. Aspidosiphon homomyarius.—Stephen and Edmonds, 1972:227. DESCRIPTION. This most common and widespread tropical A. (Aspidosiphon) has an ungrooved anal shield (Fig. 60A), bidentate compressed hooks in rings, plus characteristic dark, scattered, conical type C hooks (Figs. 55A, 62A). The within-deme variation in bidentate hook morphology is considerable. Commonly the worms are smooth, white, and 10-15 mm long, but specimens up to 57 mm have been recorded. Six to 12 short, stubby nuchal tentacles are present. The caudal shield is weakly developed and barely discernible in many worms. The longitudinal muscle layer often
Genus Aspidosiphon
215
splits in the area of the anal shield. About one in five worms has a caecum, and about one in twenty has a fixing muscle. The gut has the normal helical coil, but about half the worms have some looseness in this coil. The retractors originate about 85-95% of the distance toward the posterior end (Fig. 57B). DISTRIBUTION. Widespread and common in the Indian and western Pacific oceans, from south-central Japan to northern Australia to Hawaii, the Red Sea, and Israel. In the Caribbean from northern Brazil to the Florida Keys and Bermuda. Not known from the eastern Pacific or eastern Atlantic. Lives in dead coral and soft rock in shallow waters. Aspidosiphon exiguus Edmonds, 1974 Aspidosiphon exiguus Edmonds, 1974:187-192. Aspidosiphon (Aspidosiphon) exiguus.—E. Cutler and Cutler, 1989:844. DESCRIPTION. The largest known worm is less than 5 mm long, but all specimens bear bidentate hooks in rings as well as a few scattered unidentate compressed hooks. The introvert length is two to five times the trunk length, and no tentacles or gametes have yet been seen. The ungrooved anal shield consists of small, pale units. One to four conelike papillae are present at the anterior ventral border. This species differs from the very similar A. albus in having hooks and shorter nephridia (25-33% of the trunk length). The longitudinal muscle layer in the anterior 10% of the trunk is divided into bands visible through the body wall. The range of A. (Paraspidosiphon) parvulus overlaps, and the two species are similar in several ways. DISTRIBUTION. Cuba; intertidal, interstitial. Aspidosiphon gosnoldi E. Cutler, 1981 Aspidosiphon gosnoldi E. Cutler, i98i:445-449.-Migotto and Ditadi, 1988:253-254. Aspidosiphon (Aspidosiphon) gosnoldi.—E. Cutler and Cutler, 1989:844. Aspidosiphon spinalis.—E. Cutler, 1973:175-176.-E. Cutler and Cutler, 1979b: 107. DESCRIPTION. The anal shield is formed of randomly arranged flat units of approximately uniform size. The borders are usually distinct, but dark skin papillae may be present at the anterior end of the trunk, giving the impression of a transition zone (Fig. 55C, D). The introvert is 1.5-3 times
216
The Aspidosiphonids
the trunk length and has distal rings of bidentate hooks, 20-30 u>m tall. The secondary tooth is sometimes small and inconspicuous. Scattered, pale, pyramidal hooks are present on much of the proximal part of the introvert. This species belongs to the group whose longitudinal musculature commonly splits into irregular bundles under the anal shield. The retractor muscles originate on the caudal shield. The intestine forms a normal helical coil, and the nephridia length is 50-90% of the trunk length. DISTRIBUTION. Cape Hatteras to Florida and Brazil (to 23° S), living in gastropod shells at shelf depths (5-190 m). Aspidosiphon gracilis gracilis (Baird, 1868) Pseudaspidosiphon gracile Baird, 1868:103. Aspidosiphon gracilis.— Selenka et al., 1883:122-I23.-Rice and Stephen, I970:69.-Stephen and Edmonds, i972:225-226.-Edmonds, 1980:46-47.-Haldar, 1991: 85-86. Aspidosiphon (Aspidosiphon) gracilis gracilis.—E. Cutler and Cutler, 1989:845. DESCRIPTION. The very weakly developed anal shield is composed of noncontiguous brown papillae surrounded by darker platelets. These units are arranged in ill-defined longitudinal rows. The introvert comes off the trunk at about a 60° angle and is up to 1.5 times the trunk length. The slender trunk can be up to 15 times longer than wide and has uniformly distributed coarse papillae. The unidentate hooks are in rings and are broader than tall (up to 40 p,m tall) and followed by a proximal area of pyramidal hooks. The retractor muscles originate close to the posterior end, and the nephridia are as long as the trunk. DISTRIBUTION. Queensland, Indonesia, Philippines, Gulf of Aden, and the Andaman Islands off India, generally in intertidal coral rock. Aspidosiphon gracilis schnehageni (W. Fischer, 1913) Aspidosiphon schnehageni W. Fischer, i9i3:99-ioo.-Ditadi, 1975:200202. Paraspidosiphon schnehageni.—Stephen and Edmonds, 1972:252. Aspidosiphon (Aspidosiphon) gracilis schnehageni.—E. Cutler and Cutler, 1989:845. DESCRIPTION. W. Fischer (1913) described the anal shield as furrowed, but Ditadi's detailed redescription (1975) says the shield is composed of
Genus Aspidosiphon
217
randomly arranged plates. The units sometimes seem to be arranged in rows, giving an impression of indistinct ridges and furrows. The longitudinal musculature is partially separated into 10-14 anastomosing bundles in the anterior trunk but is continuous elsewhere. This species is one of several "borderline" taxa having indistinct bundles. The differences from the nominate form are not well defined. The hook shape is more triangular, the nephridia are shorter (33-50% vs. 100% of the trunk length), the trunk is stouter, (length < 8 times vs. 15 times the width), and the longitudinal muscle layer splits well beyond the anal shield area. The geographical gap between the populations (most of the Pacific Ocean), supports the morphological separation. The west coast of Central and South America is poorly represented in accessible curated collections. DISTRIBUTION. Chile and Pacific coast of Guatemala, in gastropod shells in shallow water down to 21 m. Aspidosiphon misakiensis Ikeda, 1904 Aspidosiphon misakiensis Ikeda, 1904:41-43.-Stephen and Edmonds, 1972:229-231. Aspidosiphon (Aspidosiphon) misakiensis.—E. Cutler et al., 1984:305.-E. Cutler and Cutler I989:845.-Saiz, 1993:133. Aspidosiphon hartmeyeri W. Fischer, i9i9b:28i-282.-Stephen and Edmonds, 1972:226-227. Aspidosiphon gerouldi ten Broeke, I925:93.-Stephen and Edmonds, 1972: 225.-E. Cutler and Cutler, 1979b: io6-i07.-Migotto and Ditadi, 1988: 251-253. Aspidosiphon speculator.—Saiz, 1986^11-14. DESCRIPTION. The anal shield is composed of closely packed, granular, irregular units with poorly delineated borders. Widely spaced square blocks of shieldlike material form a more gradual transition zone around the anterior quarter of the trunk. The caudal shield is granular with vague radial grooves. Bidentate hooks, 25-40 |xm tall, are present in distal rings, followed by scattered proximal hooks (25-60 |xm tall) that are unidentate and compressed (Fig. 58B). The secondary tooth has normal dimensions on the distal hooks but is very small in many proximal hooks. The introvert is two to three times the trunk length. The largest known worm is 25 mm, but most are about 10 mm. The longitudinal muscle layer has fractures or splits in some individuals, and the gut is loosely wound in ill-defined coils. The nephridia length is 50-100% of the trunk length, and the retractor muscles originate close to the caudal shield.
218
The Aspidosiphonids
DISTRIBUTION. In the Pacific from both sides of central Japan, at 1-50 m; South and Western Australia; and Kermadec Island. In the eastern Atlantic from the Azores, Cape Verde, and the Canary Islands to the Gulf of Guinea, at depths to 75 m; and the Spanish Mediterranean. In the western Atlantic, from Brazil (14-16° N), Haiti, and Cuba.
Aspidosiphon muelleri Diesing, 1851 Aspidosiphon muelleri Diesing, 1851:68.-Selenka et al., 1883:120-121.Southern, I9i3:3i~34.-Stephen and Edmonds, i972:23i.-Gibbs, 1977b: 3o-3i.-Konopka, 1979:220-223.-E. Cutler et al., 1984:306-307.Saiz, I 9 8 6 b : 9 - n . Aspidosiphon (Aspidosiphon) muelleri.—E. Cutler and Cutler, I989:847.-Saiz and Villafranca, 1990:1 i66.-Saiz, 1993: 135-140. Sipunculus scutatus J. Miiller, 1844:166-168.-Selenka et al., 1883:120. Aspidosiphon clavatus.—Diesing, i85i:68.-Voss-Foucart et al., 1977: 135. Pseudaspidosiphon clavatum.—Baird, 1868:103. Sipunculus cochlearius Valenciennes, i854:640.-Saiz, 19863:554. Lesinia farcimen Schmidt, 1854:2; 1865:56-66. Aspidosiphon eremita Diesing, 1859:768. Phascolosoma radiata Alder, i86o:75.-Southern, 1913:32. Sipunculus heterocyathi McDonald, 1862:78-81.-Saiz, 19863:554. Aspidosiphon jukesii Baird, i873:97.-Rice and Stephen, 1970:68-69.Stephen and Edmonds, 1972:228.-E. Cutler and Cutler, 19793:969970.-Saiz, 19863:551. Aspidosiphon mirabilis Theel, 18750:17.-Southern, 1913:31-33. Aspidosiphon armatum Danielssen and Koren, i88o:464.-Southern, 1913: 31-33Aspidosiphon tortus Selenka and Biilow, in Selenka et al., 1883:119-120.Stephen and Edmonds, 1972:236-237. Aspidosiphon heteropsammiarum—Bouvier, 1894:98.-Saiz, 19863:555557Aspidosiphon michelini Bouvier, 1894:98.-Saiz, 19863:557. Aspidosiphon corallicola Sluiter, 1902:19-22.-E. Cutler, 1965:58. Aspidosiphon imbellis Sluiter, 1902129.-Stephen and Edmonds, 1972: 227-228. Aspidosiphon inquilinus Sluiter, i902 - .29-30.-Stephen and Edmonds, 1972: 227.-Edmonds, 1980:47-49.
Genus Aspidosiphon
219
Aspidosiphon exhaustion Sluiter, 1912:20-21. Aspidosiphon exhaustus.— Stephen and Edmonds, 1972.-224.-E. Cutler et al., 1984:305. Aspidosiphon exhaustus mirus Murina, 1974^1715-1716. Aspidosiphon pygmaeus W. Fischer, i92ib:45-47.-Murina, 19713:78. Paraspidosiphon pygmaeus.—Stephen and Edmonds, 1972:251-252. Aspidosiphon kovaleskii Murina, i964c:5i-55.-Stephen and Edmonds, I972:229.-E. Cutler and Cutler, 19793:970-971. Aspidosiphon hispitrofus LiGreci, 1980:123-134. DESCRIPTION. The tan to almost black anal shields are formed of very small units arranged into various-sized plates partially separated by longitudinal furrows dorsally and by transverse furrows in the midsection. Ventrally the shield consists of raised wartlike or cone-shaped units (Fig. 60B-D). Some morphological characters of this species appear to be responses to environmental stimuli during growth (e.g., pressure, temperature, host shell shape); or perhaps random allelic frequency shifts result in ventral units of the anal shields' variability in degree of cone development. The trunk is commonly 10-30 mm, but worms up to 80 mm have been reported. Worms may be long and slender or short and fat, and may be either coiled or straight, depending on the form of the shelter, which is usually an empty gastropod or scaphopod shell. The introvert is one to three times the trunk length and tipped by 6-12 small nuchal tentacles (Fig. 55E). Hook morphology in this species has been a long-standing source of confusion (see Southern, 1913; Stephen and Edmonds, 1972). E. Cutler and Cutler (1989) analyzed the within-deme variation of compressed hooks and concluded that each worm has the ability to produce only unidentate hooks, only bidentate hooks, or some of both. Proximal to the zone of rings (on the distal third of the introvert), the scattered hooks change from compressed unidentate to pyramidal. SEM photomicrographs show small, comblike structures at the posterior base of the compressed hooks (Fig. 58A). The two retractor muscles originate from the caudal shield (95-100%), and the longitudinal muscle layer divides into separate bands underneath the anal shield (Fig. 57A). The nephridia open at, or just posterior to, the anus and are 25-100% of the trunk length. The gut forms a regular helical coil. The rectal caecum and fixing muscle are not present in all individuals. This is the most widespread, eurytopic, polymorphic Aspidosiphon, and thus comparable with Golfingia margaritacea, Phascolion strombus, or
220
The Aspidosiphonids
Sipunculus nudus, which are also species with a long list of junior synonyms and a morphology difficult to define with precision. DISTRIBUTION. Common in the northeastern Atlantic from Norway through the British Isles, the Azores, the Canary Islands, and West Africa (48-100 N). It extends through the Mediterranean, Adriatic, Aegean, and Red seas into the Gulf of Aden and along the coast of East Africa to Madagascar and South Africa. The records then skip to Sri Lanka, and there are sparse reports from central Japan through Thailand, Vietnam, Indonesia, and down to Australia, New Guinea, and the Kermadec Islands. It is not found in most of the Pacific Ocean; one record from Juan Fernandez Island off Chile (330 S) and one from southern Brazil (340 S) are the only reports from near the American continents. Inhabits shelf depths (5-400 m) throughout most of its range, but there are several records as deep as 1000 m and a few as deep as 2900 m. Most often found in discarded gastropod or scaphopod shells. Some from shallow, warm water live in the bases of solitary corals that have overgrown small gastropods, forming an interesting commensal relationship (Chapter 8). Aspidosiphon spiralis Sluiter, 1902 Aspidosiphon spiralis Sluiter, i902:25-26.-Stephen and Edmonds, 1972: 236. Aspidosiphon (Aspidosiphon) spiralis.—E. Cutler and Cutler, 1989:851. DESCRIPTION. Rings of small, 20-|xm bidentate and unidentate hooks are present, but the secondary point is not large and the distinction between the two types is not always clear (Fig. 63). The anal shield is divided into irregular squares overlain with horny protein. The retractor muscles originate from the posterior end of the trunk. This species, similar to A. muelleri
Figure 63. A. spiralis bidentate and unidentate compressed hooks with broad bases, both 20 u,m high. (After E. Cutler and Cutler, 1989, courtesy of the Biological Society of Washington.)
Genus Aspidosiphon
221
in many ways, is based on only four specimens and thus does not have a firm foundation. DISTRIBUTION. Indonesia, in gastropod shells, at 10-90 m.
Subgenus Aspidosiphon (Paraspidosiphon) (Stephen, 1964) Paraspidosiphon Stephen, 1964:459. Aspidosiphon (Paraspidosiphon) E. Cutler, 1973:168.-Saiz, 1983:172.Migotto and Ditadi, I988:250.-E. Cutler and Cutler, 1989:851. DIAGNOSIS. Introvert with compressed hooks in rings, longitudinal muscle layer divided into anastomosing bands. All bore in coral or rock. Aspidosiphon (Paraspidosiphon) coyi de Quatrefages, 1865 Aspidosiphon coyi de Quatrefages, 1865^608-609 (in part).-Baird, 1868: 101.-Stephen and Edmonds, I972:340.-Saiz, I984a:42. Aspidosiphon (Paraspidosiphon) coyi.—E. Cutler and Cutler, 1989:851. Phascolosoma truncatum Keferstein, 1867:50-53. Aspidosiphon truncatus.—Selenka et al., 1883:118-119.-E. Cutler et al., 1984:309. Paraspidosiphon truncatus.—Stephen and Edmonds, 1972:258. DESCRIPTION. Unlike A. laevis, the only other species in this subgenus with a grooved anal shield, A. coyi has distal rings of bidentate hooks 2535 |xm tall. The secondary teeth on these hooks are very small, however, and are not present on every hook. There may be unidentate compressed hooks in addition to thin pyramidal hooks. The papillae near both ends of the trunk are large and rugose. The longitudinal muscle layer can exhibit much anastomosing and is not always clearly in separate bundles. The retractor muscles originate from the posterior 95-100% of the trunk, the spindle muscle often bifurcates near the anus, and the wing muscle extends to near the ventral nerve cord. The nephridia length is 40-95% of the trunk length. The shield, retractors, and hooks are strikingly similar to those of A. (Aspidosiphon) muelleri, illustrating the less than clear gap between the two subgenera. DISTRIBUTION. Several locations in the western Indian and western Pacific oceans (central Japan through Okinawa, the Philippines, Indonesia, and the Kermadec Islands). Eastern Pacific locations from the Gulf of
222
The Aspidosiphonids
Panama and the Gulf of California are firm, but the type specimen of A. truncatus from Panama could be either east or west coast, and one worm said to be from San Salvador is probably from the Galapagos Islands. Generally from intertidal coral rock. Aspidosiphon (Paraspidosiphon) fischeri ten Broeke, 1925 Aspidosiphon fischeri ten Broeke, 1925:92-93. Aspidosiphon (Paraspidosiphon) fischeri.—Migotto and Ditadi, i988:250-25i.-E. Cutler and Cutler, 1989:851. Paraspidosiphon fischeri fischeri.—Stephen and Edmonds, 1972-.244-245.-R.ice and Maclntyre, 1979:311-319. Aspidosiphon fischeri cubanus Murina, 1967^39-42. Paraspidosiphon fischeri cubanus.—Stephen and Edmonds, 1972:245. DESCRIPTION. The smooth white body wall of these small worms (trunks up to 16 mm) is thin, but the longitudinal muscle bands are not easily seen through it, and it is thus easy to misidentify these worms as A. (Aspidosiphon) misakiensis or A. (Aspidosiphon) gosnoldi during initial sorting. The few ill-defined muscle bands anastomose frequently and in some worms appear to form a continuous sheet in the posterior trunk. The introvert is one to two times the trunk length and bears rings of compressed, bidentate hooks, 18-27 yum tall. Some hooks in the proximal rings have a very small secondary point and are mixed with unidentate hooks; or there may be a few rings of only unidentate hooks. Following these are scattered pale, pyramidal hooks 15-50 (xm tall. The retractor muscles are thin and originate at or very near the posterior end of the trunk (95-100%). The nephridia length is 33-50% of the trunk length. DISTRIBUTION. Common in the southern Caribbean from Cuba to Sao Paulo, Brazil, in shallow coral rock. Also from the Pacific coast of Panama, Ecuador, James and Hood islands, and the Galapagos Islands. Aspidosiphon (Paraspidosiphon) laevis de Quatrefages, 1865 Aspidosiphon laeve de Quatrefages, 1865^609.-Vaillant, 1875.-Saiz, 19843:55-62. Aspidosiphon laevis.—Stephen and Edmonds, 1972:340. Aspidosiphon (Paraspidosiphon) laevis.—E. Cutler and Cutler, 1989: 852. Aspidosiphon cumingii Baird, i868:i02.-Selenka et al., 1883:113-115.Rice and Stephen, 1970:67. Paraspidosiphon cumingii.—Stephen and Edmonds, i972:243-244.-Edmonds, 1980:50.
Genus Aspidosiphon
223
Aspidosiphon major Vaillant, i87i:270.-de Rochebrune, 1881:232. Aspidosiphon klunzingeri Selenka and Biilow, in Selenka et al., 1883:115— 116. Paraspidosiphon klunzingeri.—Stephen and Edmonds, 1972:247249. Aspidosiphon (Paraspidosiphon) klunzingeri.—E. Cutler and Cutler, 19793:974-975.-Haldar, 1991:89-91. Aspidosiphon gigas Sluiter, 1884:39-57. Paraspidosiphon gigas.—Stephen and Edmonds, 1972:246. Aspidosiphon angulatus Ikeda, 1904:45-47. Paraspidosiphon angulatus.—Stephen and Edmonds, 1972:241. Aspidosiphon (Paraspidosiphon) angulatus.—E. Cutler et al., 1984:308. Aspidosiphon speciosus Gerould, i9i3:426-427.-Migotto and Ditadi, 1988:254-257. Paraspidosiphon speciosus.—Stephen and Edmonds, 1972:253Aspidosiphon grandis Sato, 1939:414-419. Paraspidosiphon grandis.— Stephen and Edmonds, 1972:246-247. Aspidosiphon (Paraspidosiphon) grandis.—E. Cutler and Cutler, 1981:83-84. Aspidosiphon grandis obliquoscutatus Murina, 1974^1713-1715. Aspidosiphon pachydermatus Wesenberg-Lund, 19378:9-16. Paraspidosiphon pachydermatus.—Stephen and Edmonds, 1972:250-251. Aspidosiphon (Paraspidosiphon) pachydermatus.—Haldar, 1991:91-93. Aspidosiphon brasiliensis Cordero and Mello-Leitao, 1952:277-282, 288292. Paraspidosiphon brasiliensis.—Stephen and Edmonds, 1972:241243Paraspidosiphon johnstoni Edmonds, 1980:5i-53.-Lopez et al., 1984: 194-196. Aspidosiphon quatrefagesi Saiz, 19843:49-55. DESCRIPTION. The solid anal shield exhibits 10-15 longitudinal grooves. Bidentate hooks are lacking; the compressed hooks are unidentate, sharply pointed or blunt, and arranged in many rings (Fig. 61). The hook height (20-80 u,m) is generally correlated with trunk length. A few scattered, compressed hooks (called spines by some earlier authors) are present. Up to 24 tentacles surround the nuchal organ. The paired retractor muscles are fused for most of their length. Occasionally this fusion gives the impression of a single broad muscle with the ventral nerve cord passing through a notch in the base. The retractor muscles usually originate well in front of the caudal shield, 65-80% of the distance toward the posterior end of the trunk. Another distinctive feature is the bifurcation of the spindle muscle near its anterior end. One branch continues along the rectum into the connective tissue and wing muscle to join the body wall just anterior to the
224
The Aspidosiphonids
anus. The second, often larger branch leaves the posterior rectum and goes to the dorsal body wall posterior to the anus. In many specimens the contractile vessel has vesicular pouches or swellings along the portion that is united with the retractors, similar to those in some Golfingia specimens, and is sometimes confused with contractile vessel villi. The rectum usually has a caecum that can be either simple or complex with lateral branches or lappets. E. Cutler and Cutler (1989) discussed this at length and concluded that A. laevis has the genetic potential to produce a complex caecum, but this potential is not always expressed. The 25-35 longitudinal muscle bands can usually be seen through the skin and anastomose often. Some worms get rather large (Haldar, 1991, reports one measuring 138 by 42 mm), and those that grow to be longer than 50 mm develop opaque, thick, coarse skin, responsible for names like A. pachydermatus. The circular muscle layer subdivides into anastomosing bundles, but these are not always distinct. The nephridia are usually more than half the trunk length. DISTRIBUTION. Widespread, but low density, in warm waters in the Indo-West Pacific from Durban to the Red Sea, the Andaman Islands, Malaya to southern Japan, Indonesia, the Great Barrier Reef, and several islands east to Hawaii. Also present in the Caribbean and western Atlantic from 20° S to 31° N, then in the eastern Atlantic from the Canary and Cape Verde islands to the Gulf of Guinea. Inhabits shallow-water coral rock. Aspidosiphon (Paraspidosiphon) parvulus Gerould, 1913 Aspidosiphon parvulus Gerould, i9i3:425-426.-Stephen and Edmonds, I972:233~234.-E. Cutler, 1973:178-179. Aspidosiphon (Paraspidosiphon) parvulus.—E. Cutler and Cutler, 1989:856. Aspidosiphon spinoso-scutatus W. Fischer, 19223:13-14. Paraspidosiphon spinososcutatus.—Stephen and Edmonds, I972:254.-Rice, 1975b: 38-45. DESCRIPTION. Centrally the anal shield is made up of large, flat plates sometimes arranged in rows, giving the impression of ridges and grooves. Ventrally and laterally the shield units become smaller, scattered, and wart or cone shaped. There is a transition area where the shield units grade into coarse trunk papillae. At both ends these darker trunk papillae are situated in rectangles reminiscent of Sipunculus skin. This species is similar to A. fischeri in many ways, but the shield morphology is distinctive. The diverse hooks are 25-35 M-111 tall» bidentate and unidentate in rings, but also scattered unidentate; some are pyramidal (Fig. 58E). The 10-12 short tentacles appear linked by a thin membrane, and about 24 anastomosing
Genus Aspidosiphon
225
longitudinal muscle bands are present. These bundles are generally quite distinct in worms longer than 5 mm, more so toward the anterior end. The nephridia length is 50-75% of the trunk length. DISTRIBUTION. Western Atlantic Ocean from Cape Hatteras through the Caribbean to Venezuela; often living with Themiste alutacea and Nephasoma pellucidum in branching corals. Aspidosiphon (Paraspidosiphon) planoscutatus Murina, 1968 Aspidosiphon planoscutatus Murina, 1968c: 1722-1724; 19713:78. Aspidosiphon (Paraspidosiphon) planoscutatus.—E. Cutler and Cutler, 1989:856. DESCRIPTION. Only two specimens have been identified, and they are very similar to A. steenstrupii; however, this species has only unidentate compressed hooks on the introvert. The shield units are small and fine grained like those of A. zinni. The trunk is densely covered with skin bodies more obvious than those in A. steenstrupii, and the nephridia length is 85% of the trunk length. The lack of bidentate hooks on the introvert may be real, but this species needs verification based on a larger sample. DISTRIBUTION. Red Sea, at 40 m.
Aspidosiphon (Paraspidosiphon) steenstrupii Diesing, 1859 Aspidosiphon steenstrupii Diesing, i859:767.-Selenka et al., 1883:1161 i8.-Leroy, 1936:426; 1942:36-38. Par aspidosiphon steenstrupii steenstrupii.—Stephen and Edmonds, i972:254-255.-Edmonds, 1980:51. Aspidosiphon steenstrupii var. faciatus Augener, 1903:322-325. Paraspidosiphon steenstrupii fasciatus.—Stephen and Edmonds, 1972:255256. Aspidosiphon (Paraspidosiphon) steenstrupii—E. Cutler et al., i984:3o8-309.-Migotto and Ditadi, i988:259~26o.-E. Cutler and Cutler, 1989:857. Aspidosiphon fuscus Sluiter, i88ib:86-io8.-Selenka et al., 1883:116. Aspidosiphon speculator Selenka, i885:i9~20.-E. Cutler and Cutler, 19793:975-976 (in part). Paraspidosiphon speculator.—Stephen and Edmonds, 1972:253-254. Aspidosiphon semperi ten Broeke, I925:92.-Gibbs and Cutler, 1987:56. Paraspidosiphon semperi.—Stephen and Edmonds, 1972:252. Aspidosiphon makoensis Sato, 1939:419-421.-E. Cutler and Cutler, 1981: 82-83. Paraspidosiphon makoensis.—Stephen and Edmonds, 1972: 250.
226
The Aspidosiphonids
Aspidosiphon trinidensis Cordero and Mello-Leitao, 1952:283-286, 292294.-E. Cutler and Cutler, i98oc:2o6. Paraspidosiphon trinidensis.— Stephen and Edmonds, 1972:257-258. Aspidosiphon exostomum Johnson, 1964:331-332. Paraspidosiphon exostomus.—Stephen and Edmonds, 1972:244. Aspidosiphon ochrus E. Cutler and Cutler, I979a:976~979.-Edmonds, 1987:204. DESCRIPTION. The color of the ungrooved anal shield varies from almost white to almost black, and externally deposited calcium carbonate sometimes conceals the small, compact, uniform-sized underlying granular units. The Atlantic Ocean populations are generally dark, and the midPacific Ocean populations are pale. The Indian Ocean populations may be either; that is, dark shields seem more common in populations near continents and rare in mid-ocean island populations. The bidentate hooks are in rings and are 30-60 ftm tall on most 10-15-mm worms, but they may be up to 90 fj-m tall in worms 25-40 mm long. Haldar, 1991, reports worms measuring up to 66 by 26 mm. Most hooks have a tonguelike extension on the internal clear streak (Fig. 62B) and most worms lack unidentate compressed hooks. Many scattered, dark, pyramidal hooks (30-60 u-m) are present on the proximal introvert, reminiscent of A. (Aspidosiphon) elegans (Figs. 55B, 58F, G). The introvert is sometimes longer than the trunk. The paired retractor muscles originate about 70-85% of the distance to the posterior end of the trunk. The nephridia are usually 50-80% of the trunk length, and a rectal caecum is present in most worms. The longitudinal muscle bands number 14-22 anteriorly and 20-28 posteriorly; they anastomose, and the number of bands is independent of trunk size. DISTRIBUTION. Throughout the western and northern Indian Ocean, from northern Australia through Indonesia, Vietnam, and the South China Sea, to southern tropical Japan and out through the western Pacific islands to Hawaii. Also collected from numerous Caribbean locations; in the eastern Atlantic only from the Cape Verde Islands and the Gulf of Guinea. It lives in shallow-water coral rocks.
Aspidosiphon (Paraspidosiphon) tenuis Sluiter, 1886 Aspidosiphon tenuis Sluiter, 1886:491-492. Paraspidosiphon tenuis.— Stephen and Edmonds, 1972:257. Aspidosiphon (Paraspidosiphon) tenuis.—E. Cutler and Cutler, 1989:855.
Genus Lithacrosiphon
227
Aspidosiphon levis Sluiter, 1886:493-494. Paraspidosiphon levis.—Stephen and Edmonds, 1972:249-250. Aspidosiphon ambonensis Augener, 1903:325-328. Aspidosiphon steenstrupii van ambonensis W. Fischer, 19223:24-26. Paraspidosiphon ambonensis.—Stephen and Edmonds, 1972:240-241. Aspidosiphon (Paraspidosiphon) steenstrupii ambonensis.—Haldar, 1991:96-98. Aspidosiphon formosanus Sato, 1939:421-424.-E. Cutler and Cutler, 1981:81-83. Paraspidosiphon formosanus.—Edmonds, 1980:50-51.Stephen and Edmonds, 1972:245. Aspidosiphon havelockensis Haldar, 1978:37—41. DESCRIPTION. The anal shield is composed of very fine dark units and has a smooth overall appearance. A few very short grooves often appear around the margin. The distal rings of bidentate hooks (30-60 |xm tall) lack the distinct tongue on the clear streak seen in A. steenstrupii (Fig. 62C). Following these are scattered unidentate hooks, 25-60 (xm tall, the more distal ones with an internal clear streak. Proximally, the scattered unidentate structures have lateral reinforcing ridges. Dark pyramidal or conical hooks (as seen in A. steenstrupii) are absent. About 20% of the worms have a rectal caecum, and the nephridia length is less than half the trunk length. DISTRIBUTION. An Indo-West Pacific species found in the Andaman Islands to Thailand, Vietnam, Formosa, and Guam; east to the eastern Caroline Islands; and south through the Solomon Islands to the Great Barrier Reef and Indonesia. In shallow water, including shelf depths, generally 1-50 m.
Genus Lithacrosiphon Shipley, 1902 Lithacrosiphon Shipley, 1902:139.-W. Fischer, i922a:26-28.-Stephen and Edmonds, I972:259.-E. Cutler and Jurczak, 1975:242. DIAGNOSIS. Introvert about equal to trunk in length, with numerous rings of recurved hooks. Trunk with anal shield formed by subcuticular calcareous conical structure. Body wall with longitudinal muscle layer gathered into bands. Tentacles enclosing nuchal organ, not mouth. Contractile vessel without villi. Two introvert retractor muscles, often almost completely fused. Spindle muscle attached posteriorly. Two nephridia. Species small to medium sized, less than 40 mm in length, living in coral. TYPE SPECIES. Lithacrosiphon maldivensis Shipley, 1902.
The Aspidosiphonids
228
A D Figure 64. Lithacrosiphon. A. L. cristatus; whole animal with encrusting and filamentous algae living on anal shield (abbreviations as in Figure 1). B. Anal shield of L. cristatus. C. Anal shield of L. maldivense. D. Bidentate and unidentate hooks. Scale = 0.01 mm. (B-D from Cutler and Jurczak, 1975, courtesy of the Linnean Society.) The 1975 revision by E. Cutler and Jurczak and the more recent work by E. Cutler and Cutler (1981) determined that there are only two valid Lithacrosiphon species. One obvious and reliable morphological character that separates the two species is the architecture of the calcareous anal shield, although this is occasionally damaged, overgrown, or missing (Fig. 64). A second useful attribute is the number of longitudinal muscle bands (LMBs). NOMENCLATURAL NOTE.
Key to Lithacrosiphon Species 1. Anal shield with parallel grooves; <25 LMBs L. cristatus (two subspecies) - Anal shield ungrooved and granular; >30 LMBs
L. maldivensis
Genus Lithacrosiphon
229
Lithacrosiphon cristatus cristatus (Sluiter, 1902) Aspidosiphon cristatus Sluiter, 1902:26. Lithacrosiphon cristatus.—W. Fischer, I922a:27.-Stephen and Edmonds, i972:26o.-E. Cutler and Jurczak, 1975:243-245.-E. Cutler and Cutler, 1981:85.-E. Cutler etal., 1984:312. Aspidosiphon uniscutatus Ikeda, 1904:43. Lithacrosiphon uniscutatus.— W. Fischer, 19223:27.-Sato, 1939:429.-Stephen and Edmonds, 1972: 265.-E. Cutler and Jurczak, 1975:246-247. Lithacrosiphon kukenthali W. Fischer, 19195:289.-Stephen and Edmonds, 1972:263. Lithacrosiphon indicus W. Fischer, I922a:28.-Stephen and Edmonds, 1972:261. Lithacrosiphon odhneri W. Fischer, 19223:29.-Stephen and Edmonds, 1972:264. Lithacrosiphon alticonus ten Broeke, I925:90.-Stephen and Edmonds, i972:26o.-Rice and Maclntyre, 1979:316. Lithacrosiphon poritidis ten Broeke, 1925:91.-Stephen and Edmonds, 1972:264. Lithacrosiphon gurjanovae Murina, I967b:36.-Rice, 19755:43. DESCRIPTION. The anal shield is furrowed longitudinally with 30-50 grooves (Fig. 64A, B). The shield may have a sharp or blunt apex, perhaps as a result of the animal's boring. The anterior end may be covered by algae or calcareous deposits, which can mask the grooves. The trunk is light brown, translucent, 10-20 mm long (a few are up to 38 mm), and 1-3 mm wide. The introvert is not longer than the trunk, and the proximal introvert bears scattered unidentate hooks which range in height from 17 to 40 \juvn. Bidentate 19-48-ixm hooks are arranged in rings distally. The bidentate hooks are always larger than the unidentate hooks, and all hooks become smaller going back from the tip of the introvert (Fig. 64D). It is essential to examine the most distal rings of hooks, even when the introvert is not completely extended, to avoid mistakes in identification. The longitudinal muscle layer is divided into 13-24 anastomosing bands. The paired introvert retractor muscles are joined for 60-75% of their length. The nephridia length is commonly 50-100% of the trunk length but ranges from 25 to 150%. DISTRIBUTION. Wide tropical distribution in the Pacific Ocean from Malaya, Timor, southern Japan, and several Micronesian islands out to Hawaii, and Panama. In the southern Caribbean from the West Indies
The Aspidosiphonids
230
down to Curasao, Venezuela, and Brazil. No records from the Indian Ocean or the eastern Atlantic. Most specimens have been collected from shallow-water coral rock. Lithacrosiphon cristatus lakshadweepensis Haldar, 1991 Lithacrosiphon cristatus lakshadweepensis Haldar, 1991:102-103. DESCRIPTION. The five worms on which this subspecies is based are 1421 mm long and differ from the nominate form in having only 20-25 grooves in the anal shield (vs. 30-50) and 8-15 LMBs (vs. 13-24). The differences in retractor origins and amount of fusion are not significant. The disjunct western Indian Ocean distribution supports the subspecific designation. DISTRIBUTION. Arabian Sea off western India, from coral rock in shallow water. Lithacrosiphon maldivensis Shipley, 1902 Aspidosiphon maldivensis Shipley, 1902:139-140. Lithacrosiphon maldivensis.—Stephen and Edmonds, 1972:263.-Hughes, 1974:235-240.E. Cutler and Jurczak, 1975:245-246. DESCRIPTION. The unique granular, often golden, bullet-shaped anal shield distinguishes this form (Fig. 64C). The worms are tan with nearly opaque body walls, and trunk lengths ranging from 25 to 49 mm have been recorded. The introvert is about half the trunk length, but no fully extended introverts have yet been measured. The distal hooks are bidentate, arranged in rings, and 40-55 p,m tall. Ridges are present in the base of the hooks. Unidentate hooks occur proximally. The longitudinal muscles are gathered into 32-37 anastomosing bands. The nephridia length is 7 5 100% of the trunk length. DISTRIBUTION. The records from the Red Sea, the Maldives, CocosKeeling and Comoran islands, Saipan, and the Gilbert Islands indicate an Indo-West Pacific distribution, generally far from continental land masses. They occur at low densities in shallow-water coral rocks.
Genus Cloeosiphon Grube, 1868 Loxosiphon de Quatrefages, i865b:6o5 (in part). Cloeosiphon Grube, i868a:48-49.-Selenkaet al., i883:i26.-Stephenand Edmonds, 1972:267.
Genus Cloeosiphon
231
Figure 65. Cloeosiphon aspergillus. A. Whole animal with introvert slightly everted through center of white anal shield. B. Three different anal shields show potential variation in shape (scale = I mm). C. Introvert hook (scale = 0.05 mm). (B and C from E. Cutler, 1977a, courtesy of Galathea Reports; drawn by Paul Winther.)
232
The Aspidosiphonids
DIAGNOSIS. Introvert longer than trunk, with numerous rings of recurved hooks. Trunk with conspicuous anal shield composed of calcareous plates. Introvert protrudes through center of shield. Body wall with continuous muscle layers. Tentacles enclose nuchal organ but not mouth. Contractile vessel without villi. One pair of introvert retractor muscles, often almost completely fused. Spindle muscle attached posteriorly. Two nephridia. One species of medium-sized worms. TYPE SPECIES. Loxosiphon aspergillus de Quatrefages, 1865.
Cloeosiphon aspergillus (de Quatrefages, 1865) Loxosiphon aspergillus de Quatrefages, 1865b: 605. Cloeosiphon aspergillum.—Griibe, i868a:47-49.-Shipley, 1898:471-472.-8316, i935:32i-324.-Stephen and Edmonds, 1972:268.-E. Cutler and Cutler, i979a:98o.-E. Cutler et al., 1984:310-31 i.-Haldar, 1991:99-101. Echinosiphon aspergillum Sluiter, 1884:26-38. Cloeosiphon mollis Selenka and Biilow, in Selenka et al., 1883:128. Cloeosiphon javanicum Sluiter, 1886:473. Cloeosiphon japonicum Ikeda, 1904:49-53. Cloeosiphon carolinum Ikeda, 1924:34-37. DESCRIPTION. Its unique anal shield makes this the most easily identified of all sipunculans. The shield consists of white diamond-shaped calcareous units, each with a dark central pore (Fig. 65A, B). Each unit fits neatly against its neighbors, like mosaic tiles, and the overall shape, while variable, is generally a rounded dome (like a pineapple or acorn). Differences in the shape of this shield have led to the erroneous creation of "new" species in past decades. The introvert protrudes through the center of the shield, not at the ventral margin as in the other members of the Aspidosiphonidae. The smooth, pale trunk may exceed 90 mm, but most are 10-40 mm long. The continuous muscle layers and absence of a caudal shield give the impression of a Golfingiiformes worm if the anterior trunk is missing. The long introvert bears many rings of pointed bidentate hooks (Fig. 65C). DISTRIBUTION. The Indo-West Pacific from East Africa, Madagascar, India, Sri Lanka, the Maldive and Laccadive islands, Southeast Asia, southern Japan, Indonesia, the Philippines, northern Australia, New Hebrides, New Guinea, and many other western Pacific islands, but stopping short of Hawaii. Lives in coral rock, often Millipora species.
Part II
Sipunculan Biology: A Review
This part is an updated survey of sipunculan biology. The material presented here is generally from the period 1960-1992 with older references included when no new information exists. An illustrated review of sipunculan microanatomy (Rice, 1993a) that appeared while this book was in production is not included here. The following chapters assume a basic knowledge of the subject matter on the part of the reader. They are designed to provide an overview of the current state of knowledge and serve as a guide to the literature for those with more specific interests.
Sipunculus nudus: A Common but Unique Species
Many taxa contain species that have become well known because they are used as "guinea pigs" by developmental biologists, physiologists, or biochemists. From these species scientists have gathered information and then extrapolated to make sweeping general applications. Although certainly the natural sciences have progressed in this fashion, there are pitfalls in all uses of inductive logic. In the Sipuncula there are two such guinea pig species: the northwestern Atlantic endemic Phascolopsis gouldii and the widespread Sipunculus nudus, which has been extensively used by European scientists. The former has created confusion both because it has had four generic names— three between 1949 and 1965—and because its family affiliation is uncertain. One can make a good case for it being in either the Golfingiidae or the Sipunculidae. In other ways, however, P. gouldii does not seem peculiar. The same cannot be said about the second species. Since 5. nudus is a common and easily collected species along the Atlantic and Mediterranean coasts of southern Europe, it has been the subject of study for many decades (e.g., the 54-page Andreae, 1882). Although its name has not changed since Linnaeus named it in 1766, and
234
Sipunculan Biology: A Review
its placement within the higher taxa is unquestioned, S. nudus has an array of peculiarities that make it a poor candidate for "generalized sipunculan." These features are mentioned in relevant sections below, but I list them together here to show just how different S. nudus is. 1. Perhaps the most striking differences are evidenced in its developmental biology. It is the only sipunculan to have micromeres smaller than the macromeres. It is the only sipunculan to gastrulate via invagination alone. Its embryo, pelagosphera larvae, and metamorphosis are generally similar to those of other planktotrophic larvae but not the same (e.g., the pattern of ciliation and the fate of the egg envelope; see Chapter 15, this volume; Rice, 1988b). 2. From an anatomical perspective the ventral nerve cord has unique attributes; the most notable is the swollen bulb on the posterior end, unknown elsewhere in the phylum. 3. 5. nudus has unique free urn cell complexes. Although several species have fixed urn cells attached to the internal body wall, Phascolosoma agassizii is the only other species known to have free urn cells, and these are structurally different. 4. The regenerative powers of several sipunculans have been tested, and all except 5. nudus can regrow the distal end of the introvert. 5. In other sipunculans the level of potassium in the coelomic fluid is somewhat higher than in seawater, but in S. nudus it is much lower than the surrounding environment. 6. The diploid number of chromosomes appears to be 34, and the chromosomes are all very small. Most other sipunculan species have 20 chromosomes of varying sizes. 7. From a zoogeographical perspective, S. nudus is the only member of its genus (of 10 species) with a worldwide distribution in warm and warm temperate habitats. The characteristics described above make 5. nudus demonstrably different from other sipunculans. Other attributes of S. nudus may or may not be unique; they have not yet been looked for in other species. In this category are the nucleosomal DNA repeat length (number of base pairs), paramyosin in the body wall musculature and its ultrastructure, the ontogeny of the erythrocytes, the visible spectrum of the hemerythrin, bilirubin in the dermis, the nature and activity of arginine kinase, the neurosecretory system and its products, and 5. nudus's oxyconforming nature.
Sipunculus nudus: A Common but Unique Species
235
Simply because a certain attribute is exhibited by S. nudus, one should not assume that it is present throughout the phylum. This species may well contain a large number of derived characters, and it may be located far out on its own branch of the phylogenetic tree, not near the base.
8
Ecology
Habitat
Sipunculans occupy most marine habitats, from intertidal zones to abyssal depths and from polar to equatorial seas. Many species seek protective shelter in discarded mollusk shells (gastropod, scaphopod, or pteropod), polychaete tubes, foraminiferan tests, or even empty barnacles (Reimer, 1976). Some burrow in coarse or silty sands. Others live in crevices between and under rocks, within sponges or algal mats, and among byssal threads or algal holdfasts. Several species bore into coral (usually not the living portions), sedimentary rocks such as shale or sandstone, or unique material such as decaying whale skulls (Gibbs, 1987). The population density of sipunculans varies widely, from quite scattered (0.1-0.2/m2) to quite dense (almost 4000/m2; Rice et al., 1983). Many of the boring species—those in the genera Aspidosiphon, Cloeosiphon, and Lithacrosiphon—have an operculum-like anterior shield that plugs the opening of the hole and protects against predation and desiccation. Species in the genera Antillesoma, Phascolosoma, and Phascolion have a dense array of anterior trunk papillae that may function in a similar manner. Sipunculans' ability to withstand drying varies, but a generous supply of epidermal mucus glands to keep the skin moist is an important survival mechanism for intertidal species. Most shallow-water species survive well under laboratory conditions. Each species has tolerance limits and preferences for temperature, sediment type, oxygen, depth, and so on, and the species accounts in Part I include this information, when it is known. Although many accounts do include data about niche parameters (e.g., Herubel, 1907; Southern, 1913; E. Cutler, 1973; Tarifeno, 1976; Edmonds, 1980; and Saiz and Villafranca, 1990), niches have not been very well defined for most species. Hylleberg (1975) found that Phascolion strombus from Swedish waters
u Habitat
237
determines its lower vertical limit by sediment characteristics (it avoids soft clay), and its upper limit by temperature and salinity attributes. In some areas the availability of protective shells is a limiting factor. In addition to establishing P. strombus's need for shells, Hylleberg also discovered that worms of this species use their holdfast papillae to clean the interior of the occupied shell. Very few sipunculan species are restricted to cold water deeper than 3000 m, some live only in warm water less than 10 m deep, and a few are found between 10 and 4000 m over a wide range of temperatures (E. Cutler, 1973; E. Cutler and Cutler, 1987b). Some species live in clean, coarse sand (e.g., Siphonosoma cumanense) while others (S. australe) live only a few meters away in finer sand with more silt or clay (E. Cutler, 1965)Those that burrow in sand or mud secrete mucus to line the hole, but they produce no permanent tube-making material. The burrows do retain their integrity fairly well, however, as seen in 50-cm burrows recovered (with their producers, Nephasoma sp.) in box cores from depths of 12002000 m in Norwegian waters (Romero-Wetzel, 1987). These lebensspuren (life tracks) correspond well in size and shape with the fossil ichnogenus Trichichnus. The depth and orientation of the sand-mud burrows vary with the species. A 10-mm Apionsoma will be found very close to the surface, but a 25-cm Sipunculus makes a nearly vertical tunnel about a meter deep. Coral boring by sipunculans is important because it contributes to the bioerosion of reefs (E. Cutler, 1968a; Konopka, 1978). Sipunculans were the dominant bioerosive force in a Madagascar reef studied by PeyrotClausade and Brunei (1990) and in the nonliving part of the Pontes reefs of Moorea, French Polynesia (Peyrot-Clausade et al. 1992). The latter reefs contained up to 17 species of bioeroders, with Aspidosiphon species being the most common, although Lithacrosiphon and Phascolosoma species were also present. Similarly, in both recent and fossil (Quaternary) Red Sea Porites reefs, sipunculans and polychaetes were determined to be the most important bioeroders (Klein, 1991). The bioerosion process apparently combines the secretion of acidic fluids in the mucus to loosen the crystals with mechanical abrasion to remove the dislodged units (Williams and Margolis, 1974; Rice and Maclntyre, 1979). Sponges, bivalves, and polychaetes also participate in coral bioerosion. The amount of erosion varies according to the coral species present, and there is more erosion in dead than in live coral (Highsmith et al., 1983; Tsuchiya et al., 1986; Peyrot- Clausade et al., 1992). The species composi-
238
? vS
Ecology
tion of the bioerosion community is dynamic (Sammarco and Risk, 1990). For example, as the degree of grazing by damselfish increases, Cloeosiphon aspergillus becomes the dominant worm and polychaete numbers diminish (Sammarco et al., 1987). It has been proposed that Caribbean corals and their invertebrate bioeroder species differ from those in the Indo-West Pacific, and that these differences result from significantly different evolutionary histories (Scott, 1987). While this may be true for nonsipunculan taxa, the two named sipunculans {Phascolosoma perlucens and Lithacrosiphon cristatus) are widely distributed in both regions, thus providing no support for the hypothesis. Not only corals are eroded by sipunculans; soft rocks, commonly in warm-water intertidal zones, are also affected. In the northern Gulf of California the bioerosion community, which includes sipunculans, erodes calcareous rocks at a rate of about 0.3 m/1000 years (Stearley and Ekdale, 1989). Not all coral-sipunculan interactions are destructive. In a different type of association, a solitary coral of the genus Heteropsammia or Heterocyathus overgrows a gastropod shell occupied by Aspidosiphon muelleri, and the gastropod shell material is incorporated into the coral's matrix (see Mutualism, below). Sipunculans also live inside certain large sponges (e.g., the Demospongiae Spheciospongia). Westinga and Hoetjes (1981) applied the principles of island biogeography to explain the fact that sipunculan species diversity peaks and their biomass is greatest in large sponges in shallow water. Sipunculans appear to require fully saline water; they are not found in brackish waters. Species that live in the intertidal zones are quite eurytopic (i.e., able to withstand wide fluctuations in several abiotic variables). Unidentified sipunculans have been recorded from brine (200%o) at 70 m and from hydrocarbon seep communities at 400-500 m in the northern Gulf of Mexico (Bright et al., 1980; Rice, 1988a). Perhaps the most eurytopic conditions are those encountered by Phascolosoma arcuatum (ex. P. lurco), which lives in the mud among the roots of mangrove trees in intertidal zones of the Indo-West Pacific. Hyman's (1959) discussion of this species (drawn from Harms and Dragendorff, 1933) describes too narrow a niche (e.g., it is said to live just above the reach of high tide). Green (1975b) described P. arcuatum as a semiterrestrial sipunculan able to live below as well as above mean high water (MHW), where the salinity and temperature vary widely. During a three-
Behavior
239
year study of an Australian population Green noted that this sipunculan feeds by ingesting surface mud at night when the tide is out, and that those found above MHW are larger than those that live lower down. The worms are negatively phototactic, retract when touched, and can survive up to 10 months without eating.
Sensitivity to Environmental Change
Although sipunculans have not been used as specific indicator species of environmental deterioration, they were included in studies of the gross effects of pollution in Belfast Harbor (Parker, 1980) and pollution caused by tin mining in Thailand (Hylleberg and Nateewathana, 1983). The disappearance of Phascolion strombus from Narragansett Bay, Rhode Island, during the first half of the twentieth century (E. Cutler, 1973) was probably the result of human activity. A similar trend (i.e., species forced out of bays to offshore habitats) has been documented for a few species (e.g., Apionsoma misakiana) around the "outflow" side of Tokyo Bay since the 1940s (E. Cutler and Cutler, 1981). A study on the effects of 1979-1980 oil spills in the Gulf of Mexico included sipunculans because of their abundance (Lewbel, 1985). Some changes were noted in the "before" and "after" numbers of macrofauna along the Texas shelf, although they seemed to be correlated with changes in the sediment grain size, not oil content. Faunal shifts do occur naturally, most dramatically in areas of high wave energy, and it is not always easy to assign the proper cause when faunal changes are observed over time.
Behavior
Sipunculans have not been the subjects of many behavioral studies, but Hylleberg (1969) examined the irrigation activities of a Swedish population of Phascolion strombus living in discarded gastropod shells. This worm irrigates its residence by muscular means, and Hylleberg calculated the frequency of irrigation waves, the volume of water transported per wave, and the capacity of irrigation per gram, per hour. Continuous and discontinuous modes of irrigation exist, and the total irrigation was 15 ml-g^-h - 1 at temperatures between 15 and 22°C. Decapitated worms exhibited continuous irrigation for up to 13 days. Irrigation is assumed to
240
Ecology
aid respiration by maintaining oxygen-rich water around the body within the shelter. The burrowing and crawling behavior of sipunculans is very much like that of other vermiform coelomates. Hyman's statement (1959) that "most can crawl slowly by attaching the tentacular crown and then pulling the trunk forward" should be accepted only with reservations. The idea that sipunculans can attach their tentacules to anything implies grasping or adhesive ability, and this has never been observed or recorded in the primary literature. Most species have a limited ability to move outside the substrate, but they can move into or through sediment quite quickly by extruding the introvert, expanding and anchoring its tip, and contracting the introvert longitudinal muscles (not the retractors) if the substrate is suitable. It seems clear that sipunculans have well-developed tactile receptors on the distal portion of the introvert. Burrowing behavior was first described for Phascolopsis gouldi (Andrews, 1890b), but it has also been observed in two Themiste species (Peebles and Fox, 1933; Awati and Pradhan, 1935), and I have seen burrowing behavior in other genera. Tarifeno (1975b) examined the burrowing behavior of the Chilean Themiste hennahi in different kinds of sand and gravel substrata and found a correlation between interstice size and body diameter. Coelomic pressure during burrowing depends not on body size but on the kind of substrate and the particle size; that is, the amount of work required to burrow through it. My unpublished observations on Phascolopsis, Siphonosoma, Themiste, and Sipunculus and the work of Peebles and Fox (1933) show a quick and directed response to sediment (positive thigmotaxis). When a worm is removed from its normal habitat and placed into a container with only seawater, it soon ceases its probing or searching behavior, in which the introvert repeatedly extends and tests the surroundings, then retracts. If placed into a container with sand or gravel, however, it quickly burrows in; and if stones or coral are present, the worm will attempt to crawl under or inside them. When placed into a container with no sediment but only other worms, sipunculans entangle themselves into a twisted mass. When mechanically disturbed, a sipunculan quickly withdraws the introvert and contracts the body. This response is quickest if the "head" is touched, slower if the trunk is stimulated. The stronger and more continuous the stimulation, the stronger and longer the contraction of the body. The phototactic response of Themiste to bright light is strongly negative, but low light intensities do not appear to inhibit feeding activity. At least
Trophic Dynamics
241
some species are nocturnal, such as a swimming Sipunculus described by Fisher (1954b), and in fact many reef sipunculans probably feed at night. While this is not well documented, experienced collectors working in the daytime do not see extended tentacles in sand or coral habitats, thus supporting the supposition. Since the tentacles are very vulnerable to predators, it is logical to assume that sipunculans follow the nocturnal feeding pattern exhibited by many other coral reef invertebrates. Swimming consists of a nondirectional thrashing of the trunk, and this mode of locomotion is probably rare; it has been reported only in Sipunculus species. During swimming, the circular muscles are in a contracted state while the dorsal and ventral longitudinal bundles alternately contract and relax, suggesting that the animals swim on their sides (von Uexkiill, 1903; Herubel, 1907; Zukerkandl, 1950). Trophic Dynamics
Obtaining Energy Sipunculans obtain food in uiree main ways: filter feeding, ingestion of sediment and associated biomass, and scraping and picking up of material from surfaces (rock, sediment, etc.). Themiste species have elaborate dendritically branched tentacular crowns and are ciliary-mucus filter feeders (Pilger, 1982). Their tentacles are able to differentiate between food such as gelatin, meat extract-coated particles, or powdered egg white, and nonfood items such as plain sand grains (Peebles and Fox, 1933; Awati and Pradhan, 1935). Many Themiste live in habitats where there is high wave energy, so the particles of sand found in the gut are probably ingested incidentally, not intentionally, from the water column. The larger sand-dwelling species (Sipunculidae) may engulf some sediment as they tunnel through the sand, but it is doubtful that this is an important part of their food intake process. Once a burrow has been created, these species tend to stay in it. They do not tunnel continuously as earthworms do. The sipunculan lives in this burrow, whose upper part is more or less vertical, with the tentacular crown near the opening, and it nonselectively collects sand, detritus, diatoms, and smaller invertebrates that fall into the burrow during the day. The sand in the gut does not differ in its granulometric^attributes from that of the surroundings (Edmonds, 1962). Edmonds noted a large number of diatoms in the gut of Sipunculus nudus but asserted that these were
242
Ecology
probably not alive when ingested. The nitrogen content of the gut material he examined was twice that of the environment, but that may have been caused by the enzyme and mucus secretions of the gut itself. It is very likely (but has never been observed) that at night the introvert extends out of the burrow and explores the surrounding sediments, collecting additional material from the surface layer, including some sand, shell fragments, bits of coral, and so on. This mode of feeding is probably exhibited by many infaunal sipunculan genera (e.g., Golfingia, Onchnesoma, some Nephasoma, and Antillesoma). Walter (1973) studied the nutrition of Golfingia elongata and G. vulgaris from Swedish fjords (25 m, in silty sand) and Phascolosoma granulation (= P. stephensoni?) off southern France (25 m, in coralline algae). She used the phrase "passive selectivity" to describe these worms' feeding mode and said that they aimlessly draw in food from their surroundings. The most common meiofaunal components of the gut contents Walter examined were nematodes and crustaceans, especially copepods, a composition that matched the taxonomic composition of the surrounding biotope. Smaller sipunculans had smaller meiofauna in their intestines. Five years later, in a related study, Walter concluded that the meiofaunal component was not significant (see below; and Hansen, 1978). Epifaunal worms inhabiting discarded shells, tubes, or tests on the ocean floor (e.g., Phascolion, some Aspidosiphon, and a few Apionsoma and Nephasoma) often have reduced tentacular crowns. It is likely that these worms use the mucus secreted by the rich array of glands on the distal part of the introvert, which is more exposed in these animals, to pick up particulate matter from the surface of the sediment, along with some of the sediment. The materials so collected are moved into the mouth when the introvert is withdrawn. The third general feeding mode is utilized by coral- or rock-dwelling sipunculans that have no circumoral tentacles and only a few small nuchal tentacles. In these species (Phascolosoma, Lithacrosiphon, Cloeosiphon, and most Aspidosiphon), which remain in one place throughout their lives, the introvert, which is armed with posteriorly directed, curved hooks, repeatedly runs out and in, scraping and collecting algae, small invertebrates, and detritus from the surrounding surfaces. Sipunculans are not equipped to feed on larger invertebrates. The photograph of a Thysanocardia procera with its introvert stuck in the dorsal setae of the polychaete Aphrodite that Hyman (1959) attributed to Thorson is misleading. Hyman's statement that the sipunculan "quickly introduces the introvert tip through the body wall of the polychaete and sucks out
Trophic Dynamics
243
material while being dragged about by the victim" (1959:676) is not credible. Thorson did publish this view in 1957 and referred to T. procera as a temporary parasite. He made some observations on worms placed in an aquarium and drew conclusions about their ability to adhere by suction to the polychaete and then to pierce the body wall with the partially everted introvert. The host-parasite relationship was asserted to be speciesspecific. The anatomy of Thysanocardia simply does not allow this sort of attachment and penetration. The tentacular structure and gut contents clearly indicate that this sipunculan is a deposit feeder that picks up detritus or near-bottom particulate matter. It is easy to imagine the long introvert becoming inadvertently entangled in the plentiful spines of the "sea mouse," however, and if the polychaete were damaged, one can understand how the sipunculan introvert might find its way inside the polychaete via a wound or large pore. The likelihood of this happening in nature with healthy, intact animals is extremely small. ^ In this context I must mention Phascolosoma saprophagicum (Gibbs, 1987). Only one population is known, and it was found living on the flesh of a decomposing whale skull at 880 m. It is interesting to speculate about how the dynamics of this population changed once the available flesh was consumed. Fecal pellets of other invertebrates contain incompletely utilized nutrients and energy, and thus are a good food source for many sipunculans, especially deep-sea species (A. Khirpounoff, pers. comm.). Several aspects of the trophic dynamics of Sipunculus nudus and Golfingia vulgaris were analyzed by Hansen (1978), who measured the caloric content of the total food substrate as well as the meiofaunal and fecal pellet components (separately). Hansen also compared the sipunculans' fecal pellets with the substrate and found that 92% (150/165 KCal/m2) of the energy in the surface sediment comes from the fecal pellets of other animals. She suggested that the peritrophic membranes that surround the pellets and the microorganisms attached to them might be responsible for this "spec-^ tacularly high value." Of the remainder, 6% of the energy was from de- 1 tritus and protozoa and 2% was from the meiofauna. The energy content in the sipunculans' feces was too small to measure. / Sipunculans as Sources of Energy As noted above, sipunculans transform particulate food (algae, protista, meiofauna, detritus, fecal pellets) from the water column, sediment-water
Ecology
244
interface, rock surface, or the sediment itself into biomass. The worms are then available as food items for fish, gastropods, and people (Kohn, 1975). In addition, sipunculans are consumed by anemones, cephalopods, and crabs (W. Fischer, 1925). Sipunculans are an important component of the diet of Mexican mojarras (Gerreidae), a commercially important fish in tropical and subtropical lagoons (Aguirre-Leon and Yanez-Arancibia, 1986). The gray tilefish (Caulalotilus) found off the Carolinas also feed on sipunculans (Ross, 1982), as do the star-spotted dogfish (Mustellus) of Japan (Taniuchi et al., 1983). Other species that depend in significant ways on sipunculans are the American whitebone porgy (Calanus leucosteus; Sedberry, 1989), the Japanese yellow wrasse (Thalasoma lutescens; Gushima and Kakuta, 1991), and, less importantly, the red mullet (Mullus barbatus) from western Greece (Vassilopoulou and Papaconstantinou, 1993). Humans are known to use sipunculans as fish bait (E. Cutler, 1965). , Sipunculans are well-documented gastropod prey items (Kohn, 1978), but two reports are of particular interest. The diets of two out of seven species of Turridae from shallow-water rock surfaces in the British West Indies consist largely of sipunculans (Maes, 1983). Similarly, two out of seven species of the Indo-West Pacific predatory gastropod Drupa specialize in sipunculans, two others eat mostly polychaetes, and the remdnder are generalists (J. Taylor, 1983). As is true of other soft-bodied marine invertebrates, at least some sipunculans (e.g., P. gouldii) secrete repulsive chemicals from epithelial raucocytes (Prezent et al., 1981) that provide protection from a variety of predators, including fish and crabs. Human consumption of sipunculans is not widespread, but there are reports of people in the Indo-West Pacific eating Sipunculus and Siphonosoma species (Sluiter, 1881b; Sato, 1935). The Chinese are also known to eat Phascolosoma species (Chen and Yeh, 1958).
Symbiotic Relationships Mutualism
, r.
Although numerous sipunculans are involved in parasitic and commensal relationships, only one species is alleged to be mutualistic: Aspidosiphon muelleri (formerly A. corallicola and A. jukesii) (Baird, 1873;
Symbiotic Relationships
245
A B Figure 66. Symbiosis between the solitary coral Heteropsammia and the sipunculan Aspidosiphon muelleri. A. External view showing introvert protruding from hole in basal plate. B. Dorsal view of cross section showing worm with its anterior end near hole (H) to outside. Short straight lines represent pores (P) that allow water to circulate through the chamber. (B from Yonge, 1975, courtesy of Smithsonian Institution Press.) Bouvier, 1894, 1895; Sluiter, 1902; Shipley, 1903; Yonge, 1975; E. Cutler and Cutler, 1979a; Fisk, 1983; Hoeksema and Best, 1991). In the IndoWest Pacific region, juvenile worms of this species move into empty gastropod shells for shelter (typical behavior for many Aspidosiphon species). Planula larvae of solitary corals in the genera Heteropsammia and Heterocyathus then settle on the outside of the occupied shells. Eventually the coral overgrows and absorbs the shell's material into its own tissue, but the worm continues to exist in a coiled space within the coral (Fig. 66). The worm's shelter has an opening in the basal plate just large enough for the long introvert to protrude through for feeding, plus a series of smaller pores for irrigation. The worm benefits from this relationship by having a portable shelter. The coral benefits by being kept upright. If local conditions should deteriorate, the coral, with its worm locomotor, can migrate into a more suitable area of muddy sand. This relationship might more correctly be called commensalism (or perhaps facultative mutualism?), because while the sipunculan is not dependant on the coral (it can do quite well in an unadorned shell), the coral has not been recorded without a worm symbiont. The Aspidosiphon-cordA relationship has existed since early Neogene times (Gill and Coates, 1977) and perhaps since the Cretaceous (Yonge, 1975).
246
Ecology
Commensalism Commensalism often involves the use of one partner as a place of attachment for the other. As more or less sedentary animals, sipunculans provide a suitable surface to which smaller metazoans can attach. At least 19 species of hydroids and bryozoans live on the external surface of Phascolion strombus in what Hylleberg (1970) defined as neutral relationships. I have found deep-water Golfingia muricaudata living commensally with hydroids (probably Perigonimus) and entoprocts {Loxosomella fauvelil). A Mid-Atlantic Ridge collection of Phascolion tuberculosum showed many to be carrying colonies of hydroids (Eudendrium sp.), bryozoans (Triticella sp.), and Entoprocta (P. H. Emschermann, pers. comm.). The first report of commensal Loxosomatidae was Vogt's (1876) record from two North Atlantic Golfingia species. Hyman (1959) reviewed early Loxosomella records. Most were from Phascolion strombus, whose anterior end forms an operculum-like region when the introvert is withdrawn, thereby providing a suitable attachment surface for small metazoans. Bivalve mollusks have been known as commensals for some time (Bouvier, 1895; Shipley, 1903; Cuenot, 1922; Perez, 1924; Knudsen, 1944; E. Cutler, 1965; Gage, 1968). They are sometimes attached by byssal threads to the posterior end of the sipunculan's trunk, as in Siphonosoma cumanense from Madagascar (E. Cutler, 1965), but more commonly the clams are not attached to the worm; they merely share its burrow or shell. Gage (1968, 1979) described the ecology and behavior of two small members of the Montacutidae, Mysella cuneata and Tellimya (= Montacuta) phascolionis, species that live either embedded in the sediment around the opening or within the inhalant canal of discarded gastropod shells occupied by Phascolion strombus. Four to six different year classes are present, indicating that the clam's growth is slow, but also that the life V expectancy of the worm is at least that long. Sprat find new host worms by following an undetermined chemical produced by the worm. A new member of the bivalve genus Fronsella was found living on Sipunculus nudus in the Philippines (Habe and Kanazawa, 1981). Leptonacean bivalves were collected in the burrows of S. nudus (a Fronsella) and Siphonosoma cumanense (a Nipponmysella) from Hong Kong (Manning and Morton, 1987). The number of these bivalves per sipunculan ranges from 1 to 9 (mean = 5) and 1 to 7 (mean = 3.3), respectively. One or two pinnotherid crabs also coexist with the bivalves and worms.
Symbiotic Relationships
247
In addition to the bivalve Tellimya (= Montacuta) phascolionis, the pyramidellid gastropod Evalea (= Menestho) diaphana occurs in association with British and Spanish populations of Phascolion strombus. Epilepton clarkiae, another bivalve, is sometimes also present (Gibbs, 1978a; Thoncoso and Urgurri, 1992). Polychaetes such as the syllid Syllis cornuta (Thoncoso and Urgurri, 1992) also cohabitate with sipunculans in burrows or shells such as those occupied by Phascolion strombus or Aspidosiphon muelleri, and in mud tubes made by Phascolosoma meteori. Records of these syllids go back at least as far as Southern, 1913. The reverse dynamic may also be true. It may be the sipunculan that invades the space created and occupied by an animal such as a tubedwelling polychaete or a burrowing anemone.
Parasitism Parasites of sipunculans are quite diverse. Two reports from the early 1900s note holotrichous ciliates in the coelom and esophagus (Metalnikoff, 1900; Cuenot, 1900), but most parasitic Protoctista are sporozoans, usually gregarines living in the coelom, gut, or blood cells (see Hyman, !959> f° r a review). New species of intestinal and blood cell parasites have been found in the Caribbean sipunculans Antillesoma antillarum, Phascolosoma varians, and Siphonosoma cumanense (Jones, 1975; Jones and Schiess, 1975; Theodorides, 1975). The Apicomplexa Filipodium ozakii attaches to the inside of the intestine with its mucron and ingests the endoplasm of the host's epithelial cells by phagocytosis (Hoshide and Todd, 1992). Ormieres (1979) used an electron microscope to define the ultrastructure of an archigregarine living in Phascolosoma granulatum from the eastern Atlantic. Gunderson and Small (1986) found a new eugregarine in the intestine of the common California sipunculan P. agassizii. There are unpublished reports of two sympatric Californian Themiste species with different undescribed species of intestinal gregarines (F. G. Hochberg, pers. comm.). Using other host-parasite relationships as a guide, one could postulate that each sipunculan species has its own unique parasite fauna. The fact that rhabdocoel turbellarians are parasites on sipunculans has been known since 1900 (Dorler, 1900). The genus Collostoma seems to live only within sipunculans. Presently six Collostoma species are known. The two most recently discovered were found in an Argentinian Golfingia
248
Ecology
(Ponce de Leon and Man6-Garzon, 1980) and a Themiste from Oregon (Westervelt, 1981). There are no recent reports of Trematoda in sipunculans, and no adult trematodes have ever been found in them, but a few metacercariae and cercariae were reported in tissues of two Golfingia and in Phascolion strombus (Hyman, 1959). Records of Nematoda in sipunculans are scarce. Reports of a nematode inside Cloeosiphon (Augener, 1903), a larval worm inside a Phascolosoma nigrescens (Jones and Schiesse, 1975), and two worms inside a Phascolosoma (Fisherana) capitatum from the Walvis Ridge (E. Cutler and Cutler, 1987b) are all that we have. The report of a pyramidellid gastropod living as an obligate parasite in Swedish Phascolion strombus is unique (Hylleberg, 1970). These gastropods use a piercing stylet for feeding, and the adults usually die soon after spawning. Copepods have ecto- and endoparasitic forms associated with most phyla, and Sipuncula is no exception. A new external associate of Phascolion strombus was described by Lutzen in 1968, and there is an interesting report of an endoparasite that causes sterility in about a third of the Japanese Phascolosoma population it inhabits (Ho et al., 1981). The literature on sipunculan-copepod associations was reviewed by IUg (1975). who also corrected a few errors in Hyman's (1959) section on this topic. Although copepods have been found both internally and externally, Illg did raise questions about their parasitic nature. Suggesting that the relationship might not always be parasitism, he proposed the label "surface symbionts" as a replacement for "ectoparasite" when a negative impact on the host has not been demonstrated. The question of whether or not sipunculans function as temporary parasites is discussed and dismissed in Trophic Dynamics, above.
9
Integument and Muscle Systems
Integument
All sipunculans have a dermis, epidermis, and cuticle. The cuticle is secreted by epidermal glands and varies in thickness from 1-2 (xm on the soft, flexible tentacles, to 50-100 jjim on the body, to 350 |xm in localized regions where hardening has occurred. Even though it has been known for several decades that at least nine genera—Aspidosiphon, Lithacrosiphon, Cloeosiphon, Phascolosoma, Phascolion, Golfingia, Thysanocardia, Themiste, and Sipunculus—do not contain cuticular chitin (Ward, 1891; Carlisle, 1959; Manavalaramanujam, 1974; Voss-Foucart et al., 1977a, 1977b), the literature contains several erroneous references to chitinous hooks or holdfasts. One possible exception is the chitinous hooks of Cloeosiphon. The calcium-based anal shield of Cloeosiphon, consisting of both calcite and aragonite crystals, is also unique (Manavalaramanujam, 1974, 1982). Fine Structure Endoplasmic reticulum is present in very low densities in the epidermis of Phascolion strombus, but bundles of tonofilaments and basal plasmalemma with many simple upfoldings are plentiful (Fig. 67A). Epidermal microvilli and cilia are visible, and the cuticle contains layers of fibrils oriented at right angles over each other. The cuticle appears to be totally absent from the tentacles (Moritz and Storch, 1970). Electron microscope studies of the cuticle have detected three layers, not two, as earlier workers had proposed (Goffinet et al., 1978). Although there are differences between the two taxa so far studied (Sipunculus and Golfingia), the similarities are striking. The introvert cuticle is not significantly different from the trunk cuticle. The thin outer (epicuticle) region is an electron-opaque border underlain by a fibrillar mid-layer (mesocuticle)
250
Integument and Muscle
Figure 67. Sipunculan integument. A. Phascolion strombus; cuticle is made up of many fibrillar layers at right angles to one another overlying bundles of tonofilaments (T), enclosed by folded basal plasmalemma (BP) (from Moritz and Storch, 1970, courtesy of Springer-Verlag). B. Section through a papilla from the trunk of Phascolosoma nigrescens showing apical pore and large secretory cells (after Shipley, 1890). C. Neurosecretory and gland cells in the skin of Phascolion strombus tentacles (from Akesson, 1958). BM, basement membrane; C, cuticle; GC, gland cell; N, nerve; NU, nucleus.
Integument
251
of variable thickness. The laminated inner layer (endocuticle) is the thickest and is made up of layers of fiber bundles. Bundles within each layer are parallel, but the orientation of the bundles changes 900 with each layer so that they intersect each other at right angles. Microvilli from the subjacent epidermal layer penetrate into, but not through, the cuticle. The microvilli and fibrillar units are embedded within a granulo-filamentous matrix. This epidermal architecture is like that found in Pogonophora and Polychaeta. (See Rice, 1993a, for more information on this topic.) The principal components of the hardened cuticular structures are collagen, acid mucopolysaccharides, and hyaluronic acid. Unlike cuticle in other sipunculans and polychaetes, the amino acid composition of the collagen in Aspidosiphon anal shields has polypeptides complexed with large amounts of glycine and tyrosine. This is probably related to the hardening process, which is sometimes assisted by the deposition of calcium carbonate (Voss-Foucart et al., 1977a, 1977b). The tanning process in hardened areas may also involve changes in the disulfide bonds of the proteins, or, as in Cloeosiphon, quinone tanning may be involved (Manavalaramanujam, 1974, 1982). Dermal Layers The dermis is a layer, often very thin, of ill-defined connective tissue. In addition to the connective tissue cells there are fibrous cells, pigment cells, and amoebocytes. The epidermis consists mainly of cuboidal cells and some columnar cells. Cilia are present on some tentacle surfaces, and these assist in feeding by moving food trapped in the mucus toward the mouth. In postlarval sipunculans, external cilia have not been observed anywhere other than the oral area. Epidermal glands are numerous and diverse in their distribution, density, and size (from one- or two-celled to multicellular). The cells within these glands are commonly elongate, granular, vacuolated, and formed into a spherical mass with a common external pore (Fig. 67B). The pore is usually on a raised papilla, the mass of the glandular tissue pushing the cuticle upward like a minivolcano. The surface of these papillae may be simple and smooth or complex with thickening material (e.g., in Phascolosoma and PhascoUon). The multicellular glands are innervated and presumably under central nervous system control. Sensory "buds" are sometimes found in the papillae along with the
252
Integument and Muscle
gland cells (for detailed discussion and illustration of dermal glands and papillae see Andrews, 1890b; Shipley, 1890, 1891; Jourdan, 1891; Ward, 1891; Cuenot, 1900; Nickerson, 1900; or von Stehle, 1953). Shipley's 1890 paper is a detailed exposition of the external morphology of one population of Phascolosoma and a fine example of a nineteenth-century author taking note of variation within populations. The function of the glands has not been extensively investigated, but they are known to produce hooks and holdfasts. Other glands produce mucus to help obtain food or resist desiccation, and some produce repulsive antipredator compounds. Cuticular elaborations such as hooks and holdfast papillae are illustrated and discussed in detail in the species accounts in Part I. Introvert hooks, which are produced by secretory glands, assist in obtaining food. They are generally posteriorly bent; partially hollow; extremely variable in shape (straight, curved, pointed, or blunt), size (20-300 \ixa), number (dozens to thousands), and arrangement (in rings or scattered); and they have clearly evolved more than once in this phylum. The ontogeny of introvert hooks has not been well studied. Muscles
Anatomy There are three main muscle systems in sipunculans: (1) the body wall musculature, (2) the introvert retractor muscles, and (3) intestinal fasteners that anchor the digestive tract. Muscle fibers are also present in internal organs such as the digestive tube and nephridiatthese'are discussed later. Body Wall Muscles. The muscles in the body wall consist of smooth catch muscle in two layers: an outer layer of circular fibers and an inner layer of longitudinal fibers (Fig. 3). Some large species have a layer of diagonal muscle fibers between these two. The thickness of the layers is generally correlated with the size of the worm, from very thin and filmlike in small Nephasoma to quite thick in large Sipunculidae. In some genera the layers are continuous sheets; in others the layers are subdivided into anastomosing or distinct and separate bundles or bands. When subdivision occurs, it is restricted to the trunk; the introvert musculature remains continuous. Ultrastructural studies of the longitudinal muscle in the body wall of Sipunculus nudus showed the fibers to be oval or polygonal in cross
Muscles
253
section and about 2-15 (xm in diameter (de Eguileor and Valvassori, 1977). The thick and thin filaments in stretched and contracted fibers showed different patterns. The small mitochondria (0.1-1 jjim) were few (only 0.1% of the fiber cross-section area), suggesting that anaerobic pathways may be important. Vesicles and endoplasmic reticula were noted all along the periphery of the fibers, as were deep clefts like those seen in T systems. In general the longitudinal muscle fibers are comparable with helical fibers in annelids. Introvert Retractor Muscles. The retractor muscles in the body cavity extend from their origins on the body wall to their insertions just behind the cerebral ganglia (at the beginning of the esophagus). The common condition is one dorsal pair and one ventral pair, but several genera have only a single pair. The ventral pair originates close to the ventral nerve cord while the dorsal pair originates more laterally. These pairs may arise at the same distance from the end of the trunk, but more commonly the ventral pair is posteriad. Some populations exhibit anomalous ontogenetic loss of one or two retractors (Gibbs, 1977b; E. Cutler and Cutler, 1979a; E. Cutler et al., 1984). Wide variation in the degree of fusion is common within some species of Onchnesoma, in which a pair may appear as a single muscle, and Phascolion, in which the two pairs may appear as one or as a single weak dorsal muscle plus a single strong ventral muscle. In Sipunculus mundanus and Xenosiphon branchiatus a third pair of muscles, the protractor muscles, is connected near the brain (Fig. 8). The name protractor reflects the fact that these very small muscles run anteriorly when the introvert is withdrawn and presumably assist in protracting the distal introvert. The protractors may be larval muscles that are not completely lost during metamorphosis (i.e., they are an ontogenetic anomaly, not a normal condition) (E. Cutler and Cutler, 1985b); however, this condition may well have become fixed via a neotenic process. Intestinal Fasteners. The intestinal fasteners hold the gut coils in place. The principal component of this system is the long, thin spindle muscle, which is present in most sipunculan species. This muscle is fixed anteriorly to the body wall near the anus or to the distal portion of the rectum, sometimes with one or two branches to the body wall. The spindle muscle extends along the rectum and into the center of the gut coil, ending within the coil in some genera and continuing on to the posterior end of the trunk in others. Along the way, small branches attach to individual intestinal coils.
254
Integument and Muscle
Many species also have one to five fixing muscles, thin strands that connect the esophagus, rectum, or most anterior coils to the body wall. The number of such muscles is variable, even within a population. Finally, some Sipunculus species have membranous elastic connective tissue sheets that anchor the intestinal loops in place. Physiology and Biochemistry Early muscle-nerve physiology studies by von Uexkiill (1896, 1903) and Baglioni (1905) showed the body wall and retractor muscles to be under nervous control. When the central nerve cord is electrically stimulated, it sends slow (100-200 mm/sec) impulses to the body wall in both directions. The retractor muscles do not respond when the ventral nerve cord is directly stimulated; instead, they respond to stimulation of the tentacles or introvert via a nerve plexus. The long retractor muscles contract posterior to anterior in coordination with the introvert wall muscle layers. The transmission of the nerve impulse to the muscle depends on the neurotransmitter acetylcholine. Animals perceive the presence of this subjJ stance via one of two types of receptors that monitor the ion permeability of postsynaptic membranes: the muscarinic type and the nicotinic type (a cation-specific channel). Sipunculans, or at least the retractor muscles of Phascolosoma, have nicotinic-type receptors (Dardymov et al., 1970). Following a stimulus, muscle contraction depends on the interaction of two proteins, actin and myosin (or paramyosin in slower-acting smooth or catch muscle). Contraction also requires ATP, particular enzymes, and, in most cases, calcium ions. This reaction depends, however, on which of two control systems regulates the process. If the system is myosin controlled, calcium ions must be available for contraction to take place. If the system is actin controlled, contraction occurs without calcium. The external concentration of calcium ions affects retractor muscle contraction in Phascolosoma scolops (myosin controlled). When calcium is absent, the muscle fails to contract (Iwamoto et al., 1986). Electron micrographs and X-ray microanalysis of resting muscle cells showed precipitated calcium distributed along the inner surface of the sarcolemma and sarcoplasmic reticulum (SR), but in contracted cells the calcium was evenly distributed throughout the cytoplasm. This distribution suggests that calcium released from the SR supplements the calcium flowing in across the cell membrane and clearly plays a role in regulating retractor muscle contraction.
Muscles
255
Whether a muscle is subject to both actin and myosin control, or only one, depends on the species and the type of muscle (body wall or retractor). For example, Lehman and Szent-Gyorgyi's (1975) statement that sipunculan muscle contraction is subject to both actin and myosin control was based on pooled data from three species, although this oversimplifies a complex situation. One species (Themiste pyroides) has only actin control, and the validity of the Phascolosoma agassizii data, which showed only myosin control, is questionable. Only Phascolopsis gouldii has both actin-controlled and myosin-controlled systems. The actin control exhibited by T. pyroides is similar to muscle control in vertebrates and suggests a derived character state (assuming the loss of the ancestral dual, actin-myosin, option). The evolutionary implications of this are considered in Chapter 18. Lehman and Szent-Gyorgyi suggested that the potential to produce myosin has not been lost, even though only a small quantity is produced. They pointed out that paramyosin is absent from both quick muscle (retractor muscles) and vertebrate striated muscle and proposed that paramyosin is subject to fewer regulators. Paramyosin is, however, present in the body wall muscle of Sipunculus nudus. The axial and subaxial periodicities of the extracted soluble paramyosin protein (aggregated into paracrystals) were found to be 144 and 48 A, similar to the oligochaete Lumbricus terrestris. Paramyosin from S. nudus has an intrinsic sedimentation coefficient of 3.19 S, close to L. terrestris (3.29 S) and the polychaete Arenicola marina (3.41 S) (Camatini et al., 1976; Castellani et al., 1978). Schaeper's (1986) study of the same system (body wall muscles of S. nudus) demonstrated the presence of both actin and myosin control systems but focused on the myosin system and how it is affected by extrinsic factors. Calcium ion concentration again proved to be positively correlated with muscle contraction. The Hill coefficient of 3.45 demonstrated that efficient calcium binding sites are present within the fibers. Myosin from catch (= smooth) muscle showed a strong affinity for calcium ions. Catch muscle has exceptionally long myofilaments, slow shortening speed, high tension development, the ability to perform both phasic and tonic contraction, and a low metabolic rate (Achazi, 1982). Although much of Achazi's review article addresses the biochemistry of bivalve catch muscle, the same tissue type occurs in sipunculans, some gastropods, nematomorphs, and holothurians. Once catch muscle is contracted, it can remain that way for hours. Achazi concluded that catch muscle is a paramyosin-dependent system regulated by calcium concentration.
10
Coelomic Cells and Immune System
Coelomic Cells
The fluid-filled coelomic cavity contains a diverse population of freefloating cells for which a universal nomenclature has yet to be devised. Two nomenclature systems were proposed at the International Symposium on the Biology of Sipuncula in 1970 (also see Rice, 1993a). One system is based on light microscopy and identifies five cell types found in a single species {Phascolosoma agassizii): plate cells, small phagocytic cells, large phagocytic amoebocytes, free urn cells, and gametes (Towle, 1975). The other system is based on electron microscope studies of five species, each belonging to a different genus (Ochi, 1975). The cells designated in this system are erythrocytes (Fig. 68), leucocytes (with large and small basophilic granules), morula cells, leucocytes with fine granules, and vesicular cells (but not urn cells). Ochi proposed this system only as a preliminary one, stressing the need for further study to define the final classification of the leucocytes and their functions. Dybas (1981) combined light and electron microscopy with biochemical analyses to show that the uninucleate circulating granulocytes (= leucocytes or amoebocytes) of Phascolosoma agassizii are of two types: acidophilic and basophilic. Amoebocytes described by earlier workers include hyaline forms with or without fine granules and granulocytes with coarse granules that may be acidophilic, neutrophilic, or basophilic. Large multinucleated cells or multicellular bodies (corpuscles) were reported during the first half of the twentieth century (see Hyman, 1959). Whether these are real cell types, however, or a mixture of real entities and artifacts is uncertain. The hyaline amoebocytes may be early developmental stages of phagocytic granulocytes (Ochi, 1975). The ontogeny of coelomic cells is largely unknown (except for gametes and free urn cells), but cells in the peritoneal lining of the coelomic cavity are their likely progenitors.
Coelomic Cells
A
257
B
C
D
E
Figure 68. Diversity in sipunculan erythrocytes in five species, seen with optical (top) and electron (bottom) microscopy. A. Phascolosoma scolops with numerous slightly yellow granules. B. Themiste minor with a colorless vacuole. C. Thysanocardia nigra with several colorless vacuoles. D. Golfingia margaritacea with one yellow granule. E. Siphonosoma cumanense. Scale = 10 u.m. (From Ochi, 1975, courtesy of Smithsonian Institution Press.)
Ochi (1975) documented significant interspecific variation in types and numbers of cells. For example, leucocytes with large granules are rare in some species and common in others. The size and density of the lysosomes in the erythrocytes vary among species, and lysosomes are totally absent in Siphonosoma cumanense. Ochi noted similarities between the erythrocytes of S. cumanense and mammalian red blood cells: both lack lysosomes and neither stores glycogen (other sipunculans do). Erythrocytes The respiratory pigment hemerythrin is carried by cells called erythrocytes. Microscopic examination shows striking similarities in the erythrocytes of Sipuncula, Priapulida, and Brachiopoda (Franzen and Fange, 1962). The similarities preiswnl'bly reflect the groups' similar habitats and probably indicate some survival value. Golfingia erythrocytes are vacuolated, and Phascolion erythrocytes contain unique birefringent corpuscles that are square and very resistant to chemical and physical stresses. The oval to circular Themiste erythrocytes differ from those of the other genera examined. Few organelles exist except for occasional mitochondria, and the excentric nuclei are small. The coelomic erythrocytes are larger (19-32 |xm) and have membranous lamellae or tubules, and the cup-
258
Coelomic Cells and Immune System
shaped vascular cells are smaller (16-21 (xm in diameter) and without lamellae (Manwell, i960; Terwilliger et al., 1983). The review by Terwilliger et al. (1985), which contains practical instructions for maintaining Themiste in the laboratory and conducting cell studies, includes excellent illustrations of Themiste erythrocytes (Fig. 69). Few organelles exist, the excentric nuclei are small, and both types (coelomic and vascular) have mitochondria. The ontogeny of erythrocytes is not well understood, and it is possible that "different" erythrocytes are no more than different stages in the development of a single cell type. What we call vascular cells may mature into coelomic cells (Valembois and Boiledieu, 1980). In other words, the two cell types might be chronologically but not genetically different. Respiratory Pigments Bilirubin. Bilirubin is an antioxidant thought to modify the solubility of oxygen in the blood and is present in the dermis of Sipunculus nudus (Manavalaramanujam, 1971). It is contained in greenish yellow, refractive pigment cells, each with three to five nuclei, first described by Ward (1891). Hemerythrin. Chemists and biologists have used optical absorption, circular dichroism, fluorescence emission, resonance Raman spectroscopy, laser photolysis, X-ray microanalysis, and NMR probes to study the structure and function of the hemerythrin that sipunculans, some priapulids, brachiopods, and a few polychaetes use as a respiratory pigment. There are several good review papers on hemerythrin. Florkin's (1969a) historical overview covers the period from 1870 to i960 (when the older generic names were still in use). More recent general reviews are by Klotz et al. (1976), Hendrickson et al. (1985), and Terwilliger et al. (1985). Three types of hemerythrin molecules exist: (1) coelomic hemerythrin; (2) vascular hemerythrin, enclosed within the tentacular contractile vessel (a closed blood vascular system?); and (3) myohemerythrin, which is found in the retractor muscle tissue. Coelomic hemerythrin is slower to change form than vascular hemerythrin, which autoxidizes ten times faster (Manwell, i960). The coelomic and vascular pigments differ in their primary structures by one peptide, resulting in electrophoretically fast and slow forms in Phascolopsis gouldii and Themiste cymodoceae (Manwell, 1963). The intergeneric differences among any one of the three types of hemerythrin are less than the differences between the three types within a single species (Dunn et al., 1977; Terwilliger et al., 1985).
Coelomic Cells
259
- "ss .*T^<
Figure 69. Erythrocytes from Themiste dyscrita. A. Coelomic cells (shrinkage occurs during the preparation process). B. Contractile vessel cells. (Courtesy of E. Schabtach.)
26o
Coelomic Cells and Immune System
The secondary structure of hemerythrin consists of four helical polypeptides, which are folded into the tertiary structure, with iron in the center. The quaternary structure, which is the same in all the genera so far investigated, consists of a long pseudodiad axis with two subunits, each of which in turn consists of four units (Klotz et al., 1976). An electron-dense granule in Golfingia erythrocytes that carries iron is presumed to be a reservoir for the cell's metabolism (Ochi, 1977). Hemerythrin molecules are most often reported to be octomers, but they may occur as tetra-, tri-, di-, or monomelic molecules in different species or as the result of reversible disassociation. The monomers have a molecular weight of 13,000 or 13,500, and the reported octomers are thus in the 100,000-110,000 range (Ferrell and Kitto, 1970; Hendrickson and Klippenstein, 1974; Kurtz, 1986), quite large compared with vertebrate hemoglobins. Early workers such as Love (1957) reported hemerythrin weights in the 120,000-130,000 range; for example, the Phascolopsis gouldii tetramer has a molecular weight of 66,500 (its myohemerythrin octomer has been determined to be 108,000 by Hendrickson and Klippenstein [1974], and 110,632 [13,829 X 8] by Long et al. [1992], who included the active site). Each monomer contains two nonheme iron atoms in the binding (active) site, and each pair of iron atoms is capable of reversibly combining with one oxygen molecule (or one nitric oxide molecule, which binds reversibly in both the oxy- and deoxy- forms) (Nocek et al., 1988). The interspecific differences in binding sites and tertiary structure of the proteins are insignificant in the Phascolopsis, one Phascolosoma, and two Themiste that have been examined (Dunn et al., 1977). Differences in the quaternary structure leading to conformational changes in the protein (not differences in the binding site) are proposed as the explanation for differences in activity between sipunculan and brachiopod hemerythrin (Richardson et al., 1987). Each monomer in Sipunculus nudus, Phascolopsis gouldii, and Siphonosoma cumanense has 113 amino acid residues (Florkin, 1969a; Hendrickson and Klippenstein, 1974; Uchida, 1990). Themiste pyroides was reported to have 102 residues (Ferrell and Kitto, 1970), and Phascolosoma agassizii has 118 (Hendrickson and Klippenstein, 1974). When they compared the 35 terminal amino acid residues in T. pyroides and Phascolopsis gouldii, Ferrell and Kitto (1971) found only one difference, at position 9, where a valine-glycine shift had occurred, probably as the result of a single point mutation.
Coelomic Cells
261
The myohemerythrin of P. gouldii has two iso- forms, in which the N-terminal amino acid sequences differ and there are minor differences in the absorption spectra of the met- forms (Long et al., 1992). In his comprehensive review of the iron site structure, Kurtz (1986) described the shape (square doughnut) and size of each type of hemerythrin, the nature of the four branches of each subunit, and the terminal units (see Fig. 70A; see also Klotz et al., 1976). The ecological and physiological implications of having three different hemerythrins (coelomic, vascular, and myohemerythrin) have been explored by several biologists. The pigment in coelomic hemeryfhrin in Themiste hennahi (= Dendrostomum zostericolum) has a higher oxygen affinity than the vascular pigment in the tentacular contractile vessel system (Manwell, i960; Hendrickson et al., 1985; Fig. 70B). T. hennahi has a voluminous tentacular crown which is used for filter feeding and gas exchange. Siphonosoma ingens, a burrower that respires through the body wall and has a reduced tentacular crown, has oxygen affinities that are the reverse of those in T. hennahi—the vascular hemeryfhrin has the higher affinit
yg^rtt,* Clearly, the ecological conditions under which the two species live and their respiratory physiology (oxygen flowing from the tentacles in Themiste or from the coelomic fluid in Siphonosoma) are correlated, but the very different morphology of the two species plays a role as well. As Wells (1982:243) aptly stated, "The physiological properties of these pigments cannot be related to the availability of oxygen in the near environment, or to the habits of the animals, but appear to be dictated by the level of body organization, particularly with regard to the gas exchange surface." The fact that coelomic hemerythrin from P. gouldii has a lower partial pressure for oxygen at lower temperatures (Mangum and Kondon, 1975) is a reminder that data must be standardized before comparisons are
made.
^p„
Once a hemerythrin molecule has bound one molecule of oxygen, additional molecules tend to bind more easily. This allosteric effect is known as cooperativity in oxygen binding. The Bohr effect is a change in oxygen affinity correlated with a change in pH. Cooperativity and the Bohr effect have been shown in a brachiopod hemerythrin, but the evidence for their presence in all sipunculan speciesisjunclear. Based mostly on data ornamedwith X-ray crystallography, Kurtz (1986) concluded that allosteric interactions may exist. Interested readers should see this article for more details about the imidazole ligands, bridging
262
Coelomic Cells and Immune System
Coelomic Cells
263
carboxylates, helpful illustrations, and 49 citations on the subject. Richardson et al. (1983, 1987) could not confirm cooperativity (as contrasted with the brachiopod Lingula) but did note a change in the ligand affinity in response to the number of bound oxygen molecules. There is no consensus on whether or not cooperativity functions in sipunculans. Some scientists believe that the oxygenation of hemerythrin involves no subunit cooperativity (Ferrell and Kitto, 1971). Wells (1982) claimed that oxygen is cooperatively bound in Sipunculus mundanus (formerly Xenosiphori) and that there is a sigmoid binding curve. Furthermore, Wells asserted that oxygen release is regulated by pH, which means that the Bohr effect is active in that species. At a pH of 7.5 and a temperature of 20°C the P 50 is 7.0 mm Hg, which is relatively high. Under natural conditions P. gouldii lives in burrows in which the seawater Po2 is about 80 mm Hg. The coelomic fluid Po2 of this species ranges from 5 to 8 mm Hg, and it varies in direct relation to the ambient temperature (Mangum and Kondon, 1975). Perhaps the work of Mangum and Burnett (1987) contains the pivotal clue. Working with a larger number of variables, these authors concluded that the oxygen equilibrium properties of sipunculan hemerythrin, at least in Themiste hennahi, are influenced by intracellular effectors. For example, if the blood is extracted into media with higher concentrations of inorganic ions (Ca + + , Cl~), the oxygen affinity rises and cooperativity decreases. Increased C0 2 lowers oxygen affinity and increases cooperativity. Finally, Mangum and Burnett noted that these effects were obvious only in the tentacular pigment. The coelomic pigment responded very little, if at all. Mangum and Burnett (1987) concluded that the effects of intracellular effectors on the tentacular hemerythrin have significance in respiration:
Figure 70. Oxygen transport. A. Hemerythrin molecule in Phascolopsis gouldii showing tertiary and quaternary structure; two subunits have been omitted for clarity. P and Q, twofold axes; R, fourfold axis through this octomer; iron sites are represented by dark spheres (after Kurtz, 1986, courtesy of Springer-Verlag). B. Oxygen-binding equilibria for the three hemerythrins of Themiste hennahi. Values used for the power variable n and P J 0 (in the equation y/i - y = [Po2/P50]n) were, respectively: vascular, 1.1 and 42.0; coelomic, 1.3 and 4.5; myohemerythrin, 1.0 and 0.9 (from Hendrickson et al, 1985, courtesy of Springer-Verlag).
264
Coelomic Cells and Immune System
"Physiological variations in inorganic ions are very small but naturally low levels of Ca + + and Cl~ exaggerate the intrinsically lower 0 2 affinity of tentacular . . . hemerythnn, and thus enhance the routing of 0 2 from the ambient source to the tentacular compartment and from there to the coelomic compartment and then to metabolizing tissue." A molecule of hemerythrin can exist in a burgundy oxy-, a colorless deoxy-, or a yellow-green (acid pH) or brown (basic pH) methemerythrin state (Hendrickson et al., 1985). The visible spectra of both oxy- and deoxyhemerythrin from S. nudus suggest the rearrangement of an aromatic side chain, probably in the vicinity of the binding site, after the oxygen binds (Bossa et al., 1970). Kurtz's (1986) review of hemerythrin oxidation levels describes and illustrates the internal redox reactions (and their kinetics), transformation, the presence of a cytochrome similar to the mammalian b5, and coupling, among other things. Klotz et al. (1976) made some interesting comparisons between hemerythrin and hemoglobin that highlight both the fundamental unity and the diversity resulting from the evolution of physiologically important molecules. That they both use iron in the active site is only a superficial similarity (convergent evolution?), as is the fact that both are highly helical proteins that can be genetically and environmentally modified. The overall systems are quite different. Obviously, when a need arises, nature devises more than one good way to meet it. Biochemistry. Superoxide dismutase and NADH diaphorase, which are present in the erythrocytes of five sipunculan species (Manwell, 1977), inhibit autoxidation of hemoglobin to methemoglobin and the reduction of methemoglobin back to hemoglobin in mammals. The molecules appear to be dimers and are specific to the different blood pigments (muscular, vascular, and coelomic hemerythrins). Ingermann et al. (1985; Ingermann and Virgin, 1987) examined glycogen storage and glucose transport in Themiste erythrocytes. Glucose transport in this genus is rapid; the mechanism is independent of the Na+ gradient and similar to that found in mammals, but probably is affected and regulated by different inhibitors. About 50% of the total glycogen stores are in the erythrocytes, and the amount stored is sufficient to release glucose into a glucose-free medium for at least 24 hours. The main phosphorus metabolites in the hemerythrin of one species of Themiste and Phascolopsis gouldii are O-phosphorylethanolamine and 2-amino-ethylphosphonate, a combination unique to sipunculans (Robitaille and Kurtz, 1988).
Coelomic Cells
265
Soluble cytochrome b5 and a membrane-bound NADH-cytochrome-b5 reductase were purified from P. gouldii erythrocytes and characterized (Utecht and Kurtz, 1988; Bonomi et al., 1989). Both catalyze hemerythrin in electron-flow and redox reactions. The membrane-bound reductase has a molecular weight of 34,000 and contains FAD as the prosthetic group. The methemerythrin reduction system in sipunculans is analogous to the methemoglobin reduction system in vertebrate red blood cells. Urn Cell Complex Structure and Function. A few sipunculans contain unique cells known as the urn cell complex (UCC). Urn cells have attracted the attention of biologists for more than a century (Andrews, 1890a; Cuenot, 1902b, 1913; Metalnikoff, 1900; Herubel, 1902, 1907; Selensky, 1908; Buytendyk, 1909a; Harms, 1921). Hyman (1959:641) tnought they were "the most interesting element in the coelomic fluid" and remarked on their "lively" movement through the coelomic fluid. The UCC normally functions as a defense mechanism that entraps and engulfs pathogens. Free urn cells are known only from Sipunculus nudus and Phascolosoma agassizii (Towle, 1975); fixed urns have been reported in 5. nudus, P. granulatum, and some Golfingia and Aspidosiphon species (Hyman, 1959). Neither type of urn cell is present in Themiste hennahi (Triplett et al., 1958), Phascolosoma scolops, Themiste minor, Thysanocardia nigra, Golfingia margaritacea, or Siphonosoma cumanense (Ochi, 1975). The ontogeny of the UCC is not well understood, but UCC cells originate as fixed urn cells on the epithelial lining of the coelom (F. Bang and Bang, 1975). The fixed urns appear most often on stalks, sometimes two or three per stalk. They bud off from the peritoneal covering of the intestine, contractile vessel, or spindle muscle, often surrounded by chloragogen cells (Fig. 71 A, B). Cilia and large vacuoles are characteristic of fixed urns, but the cells' overall shape may differ from species to species. Published descriptions are not precise, however, and the probability of distortion due to postmortem chemical treatment is high. In S. nudus the free urn cell complex is bicellular and 20-60 p-m in diameter (F. Bang and Bang, 1975; Nicosia, 1979b); in P. agassizii it is multicellular with a 6o-jjim diameter (Dybas, 1976). 5. nudus has an anterior vesicular cell and a loosely attached, ciliated basal mucus-secreting cell complexed together by two marginal desmosomes. The basal cells have electron-dense secretory granules, 0.1-0.3 jxm in diameter, that re-
266
Coelomic Cells and Immune System
C D Figure 71. Urn cells. A. Fixed urns of Sipunculus nudus (after Selensky, 1908). B. Fixed urn among chloragogen cells on outer wall of Golflngia vulgaris intestine (after Cu6not, 1900). C and D. Cultured free-swimming urn cells of Sipunculus nudus (ca. 30 |xm across); C has a normal mucus tail, and D is hypersecreting mucus after stimulation, seen as a longer tail (after B. Bang and Bang, 1972, courtesy of J. P. Lippincott Co.). AD, accumulated cell debris; CC, chloragogen cells; CI, ciliated cell; CR, crescentic ciliated cell; CT, connective tissue; PC, peritoneal cells in stalk; V, vacuoles. lease mucus via exocytosis. The mucus is sequestered in the anterior vesicular cells until the proper stimulus causes its release. A comparison of the ultrastructure of unstimulated UCCs with UCCs stimulated by adding human fluids (Reissig et al., 1983) showed that both anterior and basal cells enclose a central extracellular cavity. In addition, a cluster of small mucus-secreting cells is attached to the surface of the ciliated cell. These secretory cells have rough endoplasmic reticulum (ER), membrane-bound vesicles, and star-shaped arrays of microtubulelike structures. Within one minute after human fluids were introduced into the suspension, the cisternae had filled and glycogen stores had decreased.
Coelomic Cells
267
This response indicates that the ciliated cells and the small secretory cells are both involved in the secretion of mucus tails (see below). The UCC in P. agassizii is composed of three cell types: (1) ciliated cells, which may capture* cell debris and foreign particles; (2) cupola cells, which are able to phagocytize latex particles; and (3) lobe cells, which phagocytize carbon particles. The lobe cells are separated from the ciliated cells by a semilunar area with mucoprotein-staining fibrils that appear to provide structural support for the complex. Both ciliated and lobe cells are attached to the semilunar area by hemidesmosomes (Dybas, 1976). The overall design of the UCC seems to be the same in 5. nudus and P. 1 agassizii; however, variations are apparent depending on the investigative ) tools and stains used and the species studied. J The mucus tail secreted by the UCC functions as a solid waste disposal system. Cell debris, foreign cells, and pathogens are accumulated by the sticky mucus for eventual removal via the nephridia. There is no evidence that digestion takes place within the UCC, and the mucus does not adhere to autologous cells (F. Bang and Bang, 1975). The length of the mucus tail increases in response to the introduction of foreign material (Fig. 71C, D). Biomedical Applications. The UCC bioassay, developed by B. G. Bang and F. B. Bang during the 1960s, 1970s, and 1980s using cells from S. nudus, is a valuable noninvasive in vitro technique in which measurable mucus secretion is used to detect the presence of certain foreign substances in humans and rabbits (Silverman et al., 1985). The UCC's usefulness rests in the fact that mucus production is stimulated by a variety of substances and can be produced by cultured cells, which remain viable for six weeks in vitro. Large molecules that stimulate hypersecretion of mucus in S. nudus have been found in a variety of mammalian fluids. Furthermore, the amount of mucus produced by the UCC (the tail length) can serve as an indication of a patient's health. The activity of the mucus-stimulating substance (MSS) is heat-invoked in serum and tears, but heat-labile in urine and saliva (B. Bang and Bang, 1974). Cultured human lymphoblastoid cells produce two different MSS fractions (Kulemann-Kloene et al., 1982). This activity is in the nuclear fraction and is trypsin-sensitive. Examples of human health problems that can be diagnosed using sipunculan mucus production are certain dry-eye disorders in which the mucus film that serves as a wetting agent in tears cannot form, shigella dysentery, acute cholera, and cystic fibrosis. Lacrimal secretions or stool filtrates are used in these bioassays (B. Bang and Bang, 1979; Franklin and Bang,
268
Coelomic Cells and Immune System
1980; B. Bang et al., 1983). The UCC system is sensitive enough to differentiate between homozygotes and heterozygotes for cystic fibrosis (Kurlandsky et al., 1980). In other words, one can quantitatively demonstrate the amount of MSS in sera of patients. It is possible to use a mixture of bacterial and human toxins to induce a worm to produce MSS (B. Bang and Bang, 1972). If this MSS is then introduced to cells from a second worm, the latter cells also produce mucus. The worm's MSS is heat-stable to 90°C and can withstand several freeze-thawings. The UCC system is also used to study sterility in women with high sperm antibody titers (Nicosia, 1979a). The condition of the cervical mucus is important in determining the survival of sperm, and normal mucus production is vital for successful fertilization and implantation. Urn cells exposed to sera produce tail lengths varying from 18 to 93 u,m, and this reaction has been used in determining the mechanisms involved in the release of normal and abnormal cervical mucus, especially the humoral factors, because mucus production is a contact-mediated process.
Immune System
Encapsulation and Inactivation Sipunculans do have an immune system, albeit a primitive one. The first experiments in a series of studies by Cushing and associates (Triplett et al., 1958), on Themiste hennahi (formerly Dendrostomum zostericolum), indicated that encapsulation of "self" and "nonself" substances is carried out by coelomic hemocytes. A worm's own tentacles placed in its coelom remained viable for up to 70 days in the encapsulated state, while nonencapsulated controls averaged 20 days of viability. A later study indicated that this encapsulation of "self" was caused by the presence of foreign microbes and adherents, not the tissue itself (Cushing and Boraker, 1975). Tentacles from anemones were also encapsulated, but they were partly digested after only five days. Coombe et al. (1984) reviewed immune responses in other invertebrates, including how they identify and eliminate foreign substances in the absence of antibodies (self-nonself recognition and phagocytosis). The granulocytes (= leucocytes, coelomocytes, or amoebocytes) of Phascolosoma agassizii are known to contain several enzymes (acid and
Immune System
269
alkaline phosphatase, lipases, and peroxidase). Once foreign material is trapped by fibrinlike strands and engulfed, the granuoles accumulate around the material, then degranulate into the phagocytic vacuole. New granules form from the Golgi complex (Dybas, 1981). T. hennahi lacks urn cells, but phagocytic, amoeboid, eosinophilic white blood cells are present in significant numbers. The coelomic fluid of T. hennahi hemolyzes human red blood cells, and it can quickly immobilize motile Protoctista (dinoflagellates) with a heat-labile, absorbable "stopfactor" that combines with the terminal flagella to stop the swimming of the flagellate (molecular weight >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.)
296
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).
300
Reproduction and Regeneration
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,
Sexual Reproduction
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
Sexual Reproduction
303
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.)
304
Reproduction and Regeneration
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.
Sexual Reproduction
305
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
Sexual Reproduction
307
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.
308
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.
314
Zoogeography
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-
Endemism and Centers of Origin
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
319
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
320
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-
322
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
324
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
328
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).
336
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
342
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
344
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
Zoogeographical Data
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).
Zoogeographical Data
369
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
370
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
Zoogeographical Data
371
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
374
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.
Bibliography
This bibliography does not include the works of everyone who wrote about sipunculans. I have omitted citations of very general nineteenth-century dictionaries and handbooks and brief localized lists of marine fauna containing neither new species descriptions nor new information about existing species. Items preceded by an asterisk are not cited in the text. I have included them in the Bibliography for historical completeness since some part of that author's contribution to sipunculan biology is included in this book. In other words, if I have cited an author, I have included all of that author's relevant writings, whether or not these are cited in the text. Achazi, R. K. 1982. Catch muscle. In B. M. Twarog, R. J. Levine, and M. M. Dewey, eds., Basic biology of muscles: A comparative approach. New York: Raven Press, pp. 291-308. (Adolph, E. F. 1936. Differential permeability to water and osmotic exchanges in the marine worm Phascolosoma. Journal of Cellular and Comparative Physiology 9:117-135. Aguirre-Leon, A., and A. Yanez-Arancibia. 1986. The mojarras from the Laguna de Terminos (Mexico): Taxonomy, biology, ecology and trophic dynamics (Pisces, Gerreidae). Anales del Instituto de Ciencias del Mar y Limnologia, ___ Universidad Nacional Autonoma de Mexico I3(i):369~444. Agur, Z., and U. N. Safriel. 1981. Why is the Mediterranean more readily colonized than the Red Sea, by organisms using the Suez Canal as a passageway? _ Oecologia 49:359-361. Akesson, B. 1958. A study of the nervous system of the sipunculoideae, with some remarks on the development of the two species Phascolion strombi Montagu and Golfingia minuta Keferstein. Undersokningar over Oresund (Lund) _ 38:1-249Akesson, B. 1961a. The development of Golfingia elongata Keferstein (Sipun~~ culidea) with some remarks on the development of neurosecretory cells in sipunculids. Arkiv for Zoologi I3(23):5ii-53i. Akesson, B. 1961b. Some observations on pelagosphaera larvae (Sipunculoidea). Galathea Report 5:7-17. Alder, J. i860. Description of a zoophyte and two species of Echinodermata new to Britain. Annals and Magazine of Natural History 5:73-75.
388
Bibliography
Amor, A. 1964. El genero Dendrostomum (Sipunculida) en la Argentina. Physis 24(68):457-470. Amor, A. 1970. A prop6sito del hallazgo de Themiste hennahi Gray en la Bahia Concepci6n, Chile (Sipuncula). Physis 29(79)1495-504. *Amor, A. 1975a. Notas sobre Sipuncula de la Argentina, Brasil y Peru. Physis 34(88):i 13-120. Amor, A. 1975b. El periodo de desove de Themiste petricola (Sipuncula, Golfingiidae) bajo condiciones de laboratorio. Physis 34(88):i85-i92. Amor, A. 1975c. El desarrollo de Themiste petricola (Amor, 1964) (Sipuncula, Golfingiidae). Physis 34(89):359~370. Amor, A. I975d. On the zoogeography of the Sipuncula fauna in South America. In M. E. Rice and M. Todorovic, eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Nau5no Delo Press, pp. 19-24. Andreae, J. 1881. Zur Anatomie des Sipunculus nudus L. Zoologischer Anzeiger 4:477-481. (Andreae, J. 1882. Beitrage zur Anatomie und Histologic des Sipunculus nudus L. _ Zeitschrift fur Wissenschaftliche Zoologie 36:201-255. (j^Andrews, E. A. 1889. Reproductive organs of Phascolosoma gouldii. Zoo^ logischer Anzeiger 12:140-142. Andrews, E. A. 1890a. Notes on the body-cavity liquid of Sipunculus gouldii. Johns Hopkins University Circulars 9:65. Andrews, E. A. 1890b. Notes on the anatomy of Sipunculus gouldi Pourtal6s. Studies of the Biological Laboratory of Johns Hopkins University 4:384430. Augener, H. 1903. Beitrage zur Kenntnis der Gephyreen nach Untersuchung der im Gottinger zoologischen Museum befindlichen Sipunculiden und Echiuriden. Archiv fur Naturgeschichte 69:297-371. * Augener, H. 1906. Westindische Polychaeten. Bulletin of the Museum of Comparative Zoology of Harvard University 43:191-196. Awati, P. R., and L. B. Pradhan. 1935. The anatomy of Dendrostoma signifer ^ Selenka et de Man 1883. Journal of the University of Bombay 3:102-113. (\Awati, P. R., and L. B. Pradhan. 1936. The anatomy of Dendrostoma signifer Selenka et de Man 1883. Journal of the University of Bombay 4:114-131. Baglioni, S. 1905. Uber das Sauerstoffbedurfnis des Zentralnervensystems bei Seetiere. Zeitschrift fur Allgemeine Physiologie 5. Baird, W. B. 1868. Monograph on the species of worms belonging to the subclass Gephyreae. Proceedings of the Zoological Society of London 1868:77-114. Baird, W. B. 1873. Descriptions of some new species of Annelida and Gephyrea in the collections of the British Museum. Journal of the Linnean Society of London, Zoology 11:94-97. Balakirev, E. S., and G. P. Manchenko. 1983. High level of intraspecific genetic variability in sipunculan Phascolosoma japonicum. Genetika i9(io):i6381643Balakirev, E. S., and D. V. Zaikin. 1988. Allozyme variability of formaldehyde dehydrogenase in marine invertebrates. Genetika 24(8):i504-i507.
Bibliography
389
/ Baltzer, F. 1931. Sipunculida. Handbuch der Zoologie n(9):i5-6i. iSang, B. G., and F. B. Bang. 1972. Mucus hypersecretion induced in mucociliated epithelial cells by a factor in heated serum. American Journal of Pathology 68:407-417. Bang, B. G., and F. B. Bang. 1974. Invertebrate model for study of macromolecular regulators of mucus secretion. Lancet, November 30, 1292-1298. Bang, B. G., and F. B. Bang. 1979. Mucus-stimulating substances in human body fluid assayed in an invertebrate mucous cell system. Johns Hopkins Medical Journal i45(6):209-2i6. *Bang, B. G., and F. B. Bang. 1980. The urn cell complex of Sipunculus nudus: A model for study of mucus-stimulation substances. Biological Bulletin (Woods Hole) I59(3):57i-58i. Bang, B. G., F. B. Bang, and J. M. Failla. 1983. Differences in mucus-stimulating serum fractions of cystic fibrosis patients and controls. European Journal of Pediatrics 4o(i):22-26. Bang, F. B., and B. G. Bang. 1975. Cell recognition by mucus secreted by urn cell of Sipunculus nudus. Nature 253:634-635. Bang, F. B., and H. S. Shin. 1981. A lytic molecule active against a ciliate during a transmissible disease of Sipunculus nudus. Biological Bulletin 161:98-103. Banta, W. C, and M. E. Rice. 1976. A restudy of the Middle Cambrian Burgess Shale fossil worm, Ottoia prolifica. In M. E. Rice and M. Todorovid, eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: NauCno Delo Press, pp. 79-90. Barbut, J. 1783. The genera vermium exemplified by various specimens of the animals contained in the orders of the Intestina et Mollusca Linnaei. London: ^~ J. Sewell, 101 pp. C Barnes, R. B. 1985. Current perspectives on the origins and relationships of lower invertebrates. In S. C. Morris, J. D. George, R. Gibson, and H. M. Piatt, eds., The origins and relationships of lower invertebrates. Oxford: Oxford University Press, pp. 360-366. Barron, E. J., and W. H. Peterson. 1989. Model simulation of the Cretacous ocean circulation. Science 244:684-686. Barron, E. J., and W. H. Peterson. 1991. Mid-Cretaceous ocean circulation: A technical comment. Science 251:94-95. Benham, W. B. 1903. The Sipunculids of New Zealand. Transactions of the Royal Society of New Zealand 36:172-189. Benham, W. B. 1904. Further notes on the sipunculids of New Zealand. Transac^-*- tions^of the Royal Society of New Zealand 37:301-308. (jtenham, W) B. 1909. Annelida and Sipunculoidea. Records of the Canterbury ^__ Museum 1:71-82. *Benham, W. B. 1912. Report on sundry invertebrates from the Kermadec Islands. ,- Transactions and Proceedings of the New Zealand Institute 44:135-138. Benham, W. B. 1922. Gephyrea Inermia. Australasian Antarctic Expedition 191114. Scientific Reports Series C, Zoology and Botany 6(5):5-2i. Benson, R. H., R. E. Chapman, and L. T. Deck. 1984. Paleoceanographic events and deep-sea ostracodes. Science 224:1334-1336.
390
Bibliography
Berggren, W. A., and C. D. Hollister. 1974. Paleogeography, paleobiogeography and the history of circulation in the Atlantic Ocean. In W. W. Hay, ed., Studies in paleo-oceanography. Tulsa, Okla.: Society for Economic Paleontology and Mineralogy, pp. 126-149. Bianchi, S. 1974. Recherches histochimiques preliminaries sur les cellules neurosecretrices de Sipunculus nudus (Sipunculiens). Annals of Endocrinology 35(6):655-658. Bianchi, S. 1977. A new type of neurosecretion in the cerebral ganglion of a ^_ sipunculid. Experientia (Basel) 33(4):456-457. Blainville, H. M. D. de. 1827. Siponcle. In Dictionnaire des sciences naturelles, by Plusieurs Professeurs du Jardin du Roi, et des principales Ecoles de Paris. Paris: Levrault, 49:305-313. Blanchard, E. 1849. Recherches sur l'organisation des vers. Annales des Sciences Naturelles, ser. 3, 12:5-68. Bohadsch, J. B. 1761. De quibusdam animalibus marinis, eorumque propietatibus, orbit litterario vel nondum vel minus notis. Vol. 1. Dresden: C. C. Walther, 169 pp. Bonomi, R, R. C. Long, and D. M. Kurtz. 1989. Purification and properties of a membrane-bound NADH-cytochrome-B-5 reductase from erythrocytes of the sipunculid worm Phascolopsis gouldii. Biochimica et Biophysica Acta 999(2):i47-i56. Bossa, R, M. Brunori, G. W. Bates, E. Antonini, and P. Fasella. 1970. Studies on hemerythrin. Part 2: Circular dichroism and optical rotary dispersion of hemerythrin from Sipunculus nudus. Biochimica et Biophysica Acta ^ 207(i):4i-48. JBoucot, A. J., and J. Gray. 1983. A Paleozoic Pangaea. Science 222:571-580. Bousefield, E. L., and M. L. H. Thomas. 1975. Postglacial changes in distribution of littoral marine invertebrates in the Canadian Atlantic region. Proceedings ^ of the Nova Scotia Institute of Science 27(3):47-6o. Bouvier, E. L. 1894. Un nouveau cas de commensalisme: Association de vers du ~"~ genre Aspidosiphon avec des polypes madreporaires et un mollusque bivalve. _. Comptes Rendus, Acad6mie des Sciences, Paris 119:96-98. Bouvier, E. L. 1895. Le commensalisme chez certains polypes madreporaires. Annales des Sciences Naturelles, Zoologie et Biologie Animale, ser. 7, 20:132. Brandt, A. 1835. Prodromus descriptionis animalium ab H. Mertensio in orbis terrarum circumnavigatione observatorum 1:62. Also in Lamarck, Animaux sans vert6br6s 2, 3:472. Brett, C. E., and J. F. Cottrell. 1982. Substrate specificity in the Devonian tabulate coral Pleurodictyum. Lethaia I5(3):247~262. Brett, C. E., W. D. Liddell, and K. L. Derstler. 1983. Late Cambrian hard substrate communities from Montana/Wyoming: The oldest known hardground encrusters. Lethaia 16:281-289. Briggs, J. C. 1974. Marine zoogeography. New York: McGraw-Hill, 475 pp. Briggs, J. C. 1989. The historic biogeography of India: Isolation or contact? Systematic Zoology 38(4):322-332.
Bibliography
391
Bright, T. J., P. A. Larock, R. D. Lauer, and J. D. Brooks. 1980. Brine seep at the East Flower Garden Bank, northwestern Gulf of Mexico, USA. International Review Gesamten Hydrobiology 65(4):535~549. Broeke, A. ten. 1925. Westindische Sipunculiden und Echiuriden. Bijdragen tot de Dierkunde 24:81-96. *Broeke, A. ten. 1929. Sipunculoidea und Echiuroidea. Tierwelt Deutschlands und der angrenzenden Meeresteile 15:156-168. *Broeke, A. ten. 1933. Sipunculiden. Resultats scientifiques du voyage aux Indes Orientales N6erlandaises de LL. AA. RR. le Prince et Princesse Leopold de Belgique. Memoires du Musee Royal d'Histoire Naturelle de Belgique 2(i3):i-4. Brown, C. L., C. Michel, and E. J. DeVillez. 1979. Structural and biochemical observations on the sipunculid digestive tract. American Zoologist I9(3):908. Brown, C. L., C. Michel, and E. J. DeVillez. 1982. Properties and distribution of a chymotryptic-like enzyme from the sipunculan, Phascolopsis gouldii. Canadian Journal of Zoology 6o(3):361-367. Bulow, C. 1883. Uber anscheinend freiwillige und kiinstliche Theilung mit nachfolgender Regeneration bei Coelenteraten, Echidodermen und Wiirmer. Biologisches Zentralblatt 3:14-20. Buytendyk, F. J. 1909a. Zur Physiologie der Urnen von Sipunculus nudus. Biologisches Zentralblatt 29:365-369. *Buytendyk, F. J. 1909b. Beitrage zur Muskelphysiologie von Sipunculus nudus. Biologisches Zentralblatt 29:753-759. Buzas, M. A., and S. J. Culver. 1984. Species duration and evolution: Benthic foraminifera on the Atlantic continental margin of North America. Science 226:829-830. Buzas, M. A., and S. J. Culver. 1986. Geographic origin of foraminiferal species. Science 232:775-776. Camatini, M., L. Ceresa-Castellani, E. Franchi, G. Lanzavecchia, and L. Paoletti. 1976. Thick filaments and paramyosin of annelid muscles. Journal of Ultrastructure Research 55(3):433-447Carlisle, D. B. 1959. On the neurosecretory system of the brain and associated structures in Sipunculus nudus with a note on the cuticle. Gunma Journal of Medical Sciences 8:183-194. Castellani, L. C , A. Alberici, E. Bezzi, and C. Landoni. 1978. Structural and biochemical analysis of paramyosin from annelid muscles. Submicroscopic ^ Cytolology io(3):3i5-326. Cendrero, L. 1971. Los sipunculidos (phylum Sipunculida). In Zoologia ~~ Hispanoamericana—Invertebrados. Mexico: Borrua S.A., pp. 327-328. Chaet, A. B. 1955. Further studies on the toxic factor in Phascolosoma. Biological Bulletin (Woods Hole) 109:355. Chamberlin, R. V. 1920a. Notes on the sipunculids of Laguna Beach. Journal of Entomology and Zoology 12:30-31. Chamberlin, R. V. 1920b. Gephyrea. Report of the Canadian Arctic Expedition 1913-18 9(D):3-7.
392
Bibliography
Chamisso, A. de, and C. G. Eysenhardt. 1821. De animalibus quisbusdam e classe vermium linneana. Nova Acta Academia Caesarea Leopoldino 10:343-374. Chapheau, M. 1928. Recherches sur la respiration des Mmaties du Siponcle. Bulletin de la Station Biologique d'Arcachon 25:157-187. Chauviere, M., P. Sautiere, and P. Chevaillier. 1980. Histones from the testis of the crab Cancer pagurus. European Journal of Cell Biology 22(i):79. Chen, Y., and C. C. Yeh. 1958. Notes on some Gephyrea of China with descriptions of four new species. Acta Zoologica Sinica 10:265-278. Chin, T. G. 1947. Studies of Fukien Sipunculoidea. Biological Bulletin of Fukien Christian University 3:97-104. Chin, T. G., and C. S. Wu. 1950. Diatoms in the intestine of Amoy sipunculids (Annelida, Gephyrea). The food of Sipunculida. Lingnan Science Journal 23:43-52. Clark, R. B. 1969. Systematics and phylogeny: Annelida, Echiura, and Sipuncula. In M. Florkin and B. T. Scheer, eds., Chemical zoology. London: Academic Press, pp. 1-62. Cloud, P., and M. F. Glaessner. 1982. The Ediacarian period and system: Metazoa inherit the earth. Science 217:783-791. Cohnheim, 0.1911. Uber das Gaswechsel von Tieren mit glatter und quergestreifter Muskulatur. Zeitschrift fur Physiologie und Chemie 76. Collin, A. 1892. Gephyreen gesammelt von Herrn Stabsarzt Dr. Sander auf der Reise S.M.S. Prinz Adalbert. Archiv fur Naturgeschichte 58(i):i77-i82. Collin, A. 1901. Die Gephyreen der deutschen Expedition S.M.S. Gazelle. Archiv fur Naturgeschichte 67:299-306. Collins, D., D. Briggs, and S. C. Morris. 1983. New Burgess Shale fossil sites reveal Middle Cambrian faunal complex. Science 222:163-167. Coombe, D. R., P. L. Ey, and C. R. Jenkin. 1984. Self-non-self recognition in invertebrates. Quarterly Review of Biology 59(3^231-256. Cooper, E. L. 1976. Cellular recognition of allografts and xenografts in invertebrates. In J. J. Marchalonis, ed., Comparative immunology. New York: Halsted Press, pp. 36-79. Cordero, E. H., and Mello-Leitao. 1952. Duas novas ^species do genero Aspidosiphon da Ihla Trinidade. Mem6rias do Instituto Oswaldo Cruz 50:277295. Cronin, T. M., B. J. Szabo, T. A. Ager, J. E. Hazel, and J. P. Owens. 1981. Quaternary climates and sea levels of the U.S. Atlantic coastal plain. Science ,^— 211:233-240. / Cu6not, L. 1900. Le Phascolosome. In L. Boutan, ed., Zoologie descriptive— anatomie, histologic et dissection—des formes typiques d'invertebr6s. Paris: G. Doin et Cie, 1:386-422. Cu6not, L. 1902a. Contributions a la faune du bassin d'Arcachon. Echiuriens et Sipunculiens. Bulletin de la Soci&e Scientifique d'Arcachon 6:1-28. Cuenot, L. 1902b. Organes agglutinants et organes cilio-phagocytaires. Archives de Zoologie Experimentale et G6n6rale, ser. 3, 9:79. Cu6not, L. 1913. Excretion et phagocytose chez les sipunculiens. Comptes Rendus de Stances de la Soci&6 de Biologie et de Filiales 74:159-161.
Bibliography
393
Cu6not, L. 1922. Sipunculiens, Echiuriens, Priapuliens. Faune de France (Paris) 4:1-30. *Cuenot, L. 1927. Contributions a la faune du bassin d'Arcachon. Revue g6n6rale de la faune et bibliographic Bulletin de la Station Biologique d'Arcachon 24:229-308. Cushing, J. E., and D. K. Boraker. 1975. Some specific aspects of cell-surface recognition by sipunculid coelomocytes. Advances in Experimental Medicine and Biology 64:35-44. Cushing, J. E., J. L. McNeely, and M. R. Tripp. 1969. Comparative immunology of sipunculid coelomic fluid. Journal of Invertebrate Pathology 14:4-12. Cushing, J. E., M. R. Tripp, and S. Fuzessery. 1970. Adaptation of sipunculid amoebocytes to phagocytic inhibition by bovine serum. Federation Proceedings 29(2):77i. Cutler, E. B. 1965. Sipunculids of Madagascar. Extrait des cahiers ORSTOM, Oc6anographie 3(4):5i-63. Cutler, E. B. 1968a. A review of coral-inhabiting Sipuncula. American Zoologist 8(4):796. Cutler, E. B. 1968b. Zoogeographical barrier on the continental slope off North Carolina, II. American Zoologist 8(4):8o6. Cutler, E. B. 1969. New species of Sipuncula from the western North Atlantic. Proceedings of the Biological Society of Washington 82:209-218. Cutler, E. B. 1973. Sipuncula of the western North Atlantic. Bulletin of the American Museum of Natural History I52(3):i05~204. Cutler, E. B. 1975a. Zoogeographical barrier on the continental slope off Cape -Lookout, North Carolina. Deep-Sea Research 22:893-901. ^Cutler, E. B. 1975b. Distribution of non-tropical Atlantic Ocean Sipuncula. In M. E. Rice and M. Todorovid, eds., Proceedings of the International Symposium on the Biology of Sipuncula and Echiura. Belgrade: Nau£no Delo Press, PP- 25-33Cutler, E. B. 1975c. Pogonophora and Protostomia—a procrustean bed? Zeitschrift fur zoologische Systematik und Evolutionsforschung (Sonderheft). In A. Norrevang, ed., The phylogeny and systematic position of Pogonophora, proceedings of a symposium at Zoological Central Institute s~ Univ. Copenhagen. Hamburg: Paul Parey, pp. 112-122. Cutler, E. B. 1977a. The bathyal and abyssal Sipuncula. Galathea Report 14:135^ 156. Cutler, E. B. 1977b. Marine flora and fauna of the northeastern United States. Sipuncula. NOAA Technical Reports, NMFS Circular 403:1-7. Cutler, E. B. 1977c. Shallow water sipunculans collected by the Galathea Expedi^__^ tion (Sipuncula). Steenstrupia 4:151-155. ''Cutler, E. B. 1979. A reconsideration of the Golfingia subgenera Fisherana Stephen, Mitosiphon Fisher, and Apionsoma Sluiter (Sipuncula). Zoological C__ Journal of the Linnean Society 65:367-384. Cutler, E. B. 1980. A cladistic analysis of sipunculan higher taxa: An exercise in — futility? American Zoologist 20(4)1821. Cutler, E. B. 1981. A new species of Aspidosiphon (Sipuncula) from the western
394
Bibliography
Atlantic Ocean. Proceedings of the Biological Society of Washington 94(2):445-449. Cutler, E. B. 1982. Coelomic extensions (integumentary canals and sacs) as a taxonomic character in the family Sipunculidae (Sipuncula). American Zoologist 22(4):884. Cutler, E. B. 1984. Proposed conservation of Siphonosoma cumanense (Keferstein, 1867) over S. edule (Pallas, 1774) (Sipuncula). Bulletin of Zoological ^ _ Nomenclature 4i(i):62-64. ' Cutler, E. B. 1986. The family Sipunculidae (Sipuncula): Body wall structure and phylogenetic relationships. Bulletin of Marine Science 38(2):488-497. Cutler, E. B. 1989. Sipuncula. In S. P. Parker, ed., Encyclopedia of science and technology. 4th ed. New York: McGraw-Hill, p. 1742. Cutler, E. B., and N. Christie. 1974. New distribution records for two species of Siphonosoma (Sipuncula) collected using a diver-operated suction sampler. ^ ~ Transactions of the Royal Society of South Africa 4 i ( 2 ) : i o 9 - n o . Cutler, E. B., and N. J. Cutler. 1979a. Madagascar and Indian Ocean Sipuncula. ^— Bulletin du Museum National d'Histoire Naturelle de Paris 4(i):94i990. Cutler, E. B., and N. J. Cutler. 1979b. Campagnes de la Calypso au large des cotes Atlantiques Africaines (1956 et 1959) et Sud-Am6ricaines (1960-1961). 23. ^ - Sipuncula. Campagnes de la Calypso 11:103-109. ^Cutler, E. B., and N. J. Cutler. 1980a. Sipuncula from southern Brazil. Boletim do Institut Oceanogrffico (Sao Paulo) 29(i):i-8. Cutler, E. B., and N. J. Cutler. 1980b. Deep water Sipuncula from the Gulf of Gascogne. Journal of the Marine Biological Association of the United Kingdom 60:449-459. ^Cutler, E. B., and N. J. Cutler. 1980c. Sipuncula collected by the R/V Vema. Journal of Zoology (London) 190:193-209. ^Cutler, E. B., and N. J. Cutler. 1981. A reconsideration of Sipuncula named by I. Ikeda and H. Sato. Publications of the Seto Marine Biological Laboratory ^ 26:51-93. (' Cutler, E. B., and N. J. Cutler. 1982. A revision of the genus Siphonosoma (Sipuncula). Proceedings of the Biological Society of Washington 95(4)^48762. C__Cutler, E. B., and N. J. Cutler. 1983. An examination of the Phascolosoma subgenera Antillesoma, Rueppellisoma, and Satonus (Sipuncula). Zoological ^^, Journal of the Linnean Society 77:175-187. <^__Cutler, E. B., and N. J. Cutler. 1985a. A revision of the genera Phascolion Theel and Onchnesoma Koren and Danielssen (Sipuncula). Proceedings of the Bio„-« logical Society of Washington 98(4):8o9-8so. C^Cjrder, E. B., and N. J. Cutler. 1985b. A revision of the genera Sipunculus and Xenosiphon (Sipuncula). Zoological Journal of the Linnean Society 85:219^ 246. (^Cutler, E. B., and N. J. Cutler. 1987a. A revision of the genus Golfingia (Sipuncula: Golfingiidae). Proceedings of the Biological Society of Washington ioo(4):735-76i.
Bibliography
395
Cutler, E. B., and N. J. Cutler. 1987b. Deep-water Sipuncula from the eastern ^~ Atlantic Ocean. Sarsia 72:71-89. (jCutler, E. B., and N. J. Cutler. 1988. A revision of the genus Themiste (Sipuncula). Proceedings of the Biological Society of Washington ioi(4):74i-766. (^Cutler, E. B., and N. J. Cutler. 1989. A revision of the genus Aspidosiphon (Sipuncula, Aspidosiphonidae). Proceedings of the Biological Society of Washington i02(4):826-865. Cutler, E. B., N. J. Cutler, and P. E. Gibbs. 1983. A reconsideration of the Golfingia subgenera Golfingiella and Siphonoides (Sipuncula). Proceedings _„ of the Biological Society of Washington 96(4):669-694. Cutler, E. B., N. J. Cutler, and T. Nishikawa. 1982. Siphonosoma cumanense and S. edule (Sipuncula): A reevaluation of their separate status. Publications of ^^~ the Seto Marine Biological Laboratory 27(4-6):265-267. (s Cutler, E. B., N. J. Cutler, and T. Nishikawa. 1984. The Sipuncula of Japan: Their "" " systematics and distribution. Publications of the Seto Marine Biological Laboratory 29(4-6):249~322. Cutler, E. B., and M. DiMichele. 1982. The anatomy of the fusiform bodies in Siphonosoma (Sipuncula). American Zoologist 22(4)1951. Cutler, E. B., and K. Doble. 1979. North Carolina continental slope zoogeographical barrier. Deep-Sea Research 26A:85i-853. Cutler, E. B., and N. A. Duffy. 1972. A new species of Phascolion (Sipuncula) from the western North Atlantic. Proceedings of the Biological Society of ^_ Washington 8s(6):7i-76. (^Cutler, E. B., and P. E. Gibbs. 1985. A phylogenetic analysis of higher taxa in the phylum Sipuncula. Systematic Zoology 34:162-173. Cutler, E. B., and E. Jurczak. 1975. The sipunculan genus Lithacrosiphon Shipley, a taxonomic review. Zoological Journal of the Linnean Society 56(3)1235248. *Cutler, E. B., and E. Kirsteuer. 1968. Additional notes on some Sipuncula from Madagascar. Results of the Australian Indo-West Pacific Expedition, 1959- 60, part 12. Zoologischer Anzeiger 180:352-356. v Cutler, E. B., and V. V. Murina. 1977. On the sipunculan genus Golfingia Lankes„ . ter, 1885. Zoological Journal of the Linnean Society 60:173-186. (Cutler, N. J., and E. B. Cutler. 1986. A revision of the genus Nephasoma (Sipuncula, Golfingiidae). Proceedings of the Biological Society of Washington , - 99(4):547-573s^Cutler, N. J., and E. B. Cutler. 1990. A revision of the subgenus Phascoloma (Sipuncula, Phascolosoma). Proceedings of the Biological Society of Washington i03(3):69i-730. Cutler, N. J., E. B. Cutler, and J. A. Vargus. 1992. Peanut worms (Sipuncula) from Costa Rica. Revista de Biologia Tropical 4o(i):i53-i58. Cuvier, M. le Baron. 1830. Le regne animal. Vol. 3. Paris: Deterville et Crochard, 504 PPDanielssen, D. C. 1869a. Sipunculus norvegicus. Skandinaviske Naturforskeres mode. Forhandlinger ved de skandinaviske Naturforskeres (Kristiana) 10:541-542.
396
Bibliography
*Danielssen, D. C. 1869b. Beretning om en Zoologisk Reise, fonetagen i sommeren 1857. Nytt Magasin for Zoologi 11:1-58. Danielssen, D. C, and J. Koren. 1880. New northern Gephyrea. Annals and Magazine of Natural History, sen 5, 6:462-465. Danielssen, D. C, and J. Koren. 1881. Fra den norske Norhavsexpedition (18761878)—Gephyreer. Nytt Magasin for Naturvidenskapene 26:44-66. Dardymov, I. V., V. V. Lavrenteva, M. Y. Mikhelson, and B. A. Ger. 1970. Pharmacological characteristics of some muscles in sipunculids and annelids. Zhurnal Evolyutsionoi Biokhimii i Fiziologii 6(2):i87-i97. Delle Chiaje, S. 1823. Memorie sulla storia e notomia degli animali senza vertebre ^ del Regno di Napoli. Vol. 1. Naples: Fratelli Fernandes, 184 pp. Diesing, K. M. 1851. Systema Helminthum. Braumiiller, Vindobonae, 558 pp. "Biesing, K. M. 1859. Revision der Rhyngodeen. Sitzungsberichte der mathematischnaturwissenschaftliche Klasse, Akademie der Wissenschaften in Wien 37: 719-782. Ditadi, A. S. F. 1975. Aspidosiphon schnehageni (Sipuncula) inhabiting Tornatina shells. Veliger i8(2):20O-2O2. Ditadi, A. S. F. 1976. Sipunculus marcusi spec. nov. (Sipuncula) from southern Brazil. Boletim de Zoologia, Universidade de Sao Paulo 1:81-84. Ditadi, A. S. F. 1981. O filo Sipuncula. Ciencia e Cultura (Sao Paulo) 33(5):64i648. Ditadi, A. S. F. 1982. Intertidal sipunculans (Sipunculus) from southern Brazil. Revista Brasileira de Biologia 42(4):785-8oo. Ditadi, A. S. F., and A. E. Migotto. 1981. On the sipunculan Golfingia confusa (Sluiter, 1902). Papeis Avulsos de Zoologia (Sao Paulo) 34 (io):i25~i34. Dorler, A. 1900. Neue und wenig bekannte rhabdocole Turbellarien. Zeitschrift fiir Wissenschaftliche Zoologie 68. Dunn, J. B. R., A. W. Addison, R. E. Bruce, J. S. Loehr, and T. M. Loehr. 1977. Comparison of hemerythrins from four species of sipunculids by optical absorption, circular dichroism, fluorescence emission, and resonance Raman spectroscopy. Biochemistry i6(8):i743-i749. Dunton, K. 1992. Arctic biogeography: The paradox of the marine benthic fauna ^ and flora. Trends in Ecology and Evolution 7(6):i83-i89. Dybas, L. 1976. A light and electron microscopic study of the ciliated urn of ~ Phascolosoma agassizii (Sipunculida). Cell and Tissue Research 169:67-75. Dybas, L. K. 1981. Cellular defense reactions of Phascolosoma agassazii, a sipun~^ culan worm: Phagocytosis by granulocytes. Biological Bulletin (Woods Hole) 161:104-114.
Edmonds, S. J. 1955. Australian Sipunculoidea. I. The genera Sipunculus, Xenosiphon, and Siphonosoma. Australian Journal of Marine and Freshwater Research 6(i):82-97. Edmonds, S. J. 1956. Australian Sipunculoidea. II. The genera Phascolosoma, Dendrostomum, Golfingia, Aspidosiphon, and Cloeosiphon. Australian Journal of Marine and Freshwater Research 7(2):28i-3i5. Edmonds, S. J. 1957a. The respiratory metabolism of Dendrostomum cymodoceae
Bibliography
397
Edmonds (Sipunculoidea). Australian Journal of Marine and Freshwater Research 8(i):55-63. Edmonds, S. J. 1957b. The catabolism of nitrogen compounds in Dendrostomum cymodoceae Edmonds (Sipunculoidea). Australian Journal of Marine and Freshwater Research 8(2):i3i-i35. Edmonds, S. J. i960. Sipunculids from New Zealand and the Chatham Islands. New Zealand Department of Scientific and Industrial Research Bulletin I39(4):i59-i67*Edmonds, S. J. 1961. On Sipunculus aeneus Baird (Sipunculoidea). Annals and Magazine of Natural History, ser. 13, 4:217-220. Edmonds, S. J. 1962. Some notes on the abundance, environment, and nutrition of Sipunculus nudus L. (Sipunculoidea) at Morgat, Brittany. Cahiers de Biologie Marine 3:183-190. •Edmonds, S. J. 1965. Sipunculoidea of the Ross Sea. Fauna of the Ross Sea, part 4. New Zealand Department of Science and Industrial Research Bulletin 167:27-34. •Edmonds, S. J. 1966a. Port Phillip Survey 1957-1963. Sipunculoidea and Echiuroidea. Memoirs of the National Museum of Victoria 1966:175-178. Edmonds, S. J. 1966b. Siphonosoma hawaiense, a new sipunculoid from Hawaii ^_. (Sipunculoidea). Pacific Science 20(3):386-388. •Edmonds, S. J. 1969. Sipuncula and Echiura. Antarctic map folio series. New *""~ York, 11:23-24. Edmonds, S. J. 1971. Some sipunculans and echiurans, chiefly from Guam (Sipuncula and Echiura). Micronesica 7(i-2):i37-i5i. •Edmonds, S. J. 1972. Marine invertebrates from Adelie Land, collected by the 12th and 15th French Antarctic expeditions. Part 5. Sipuncula. T£thys Supplement 4:83-86. Edmonds, S. J. 1974. A new species of Sipuncula (Aspidosiphon exiguus) belonging to the interstitial fauna of marine beaches collected by Mr. Botosaneanu during the second Cuban-Romanian Biospeleological Expedition to Cuba 1973. International Journal of Speleology 6:187-192. Edmonds, S. J. 1976. Three sipunculan species (two new) from New Zealand. New Zealand Journal of Marine and Freshwater Research io(i):2i7-224. Edmonds, S. J. 1980. A revision of the systematics of Australian sipunculans (Sipuncula). Records of the South Australian Museum (Adelaide) i8(i):i74Edmonds, S. J. 1985. A new species of Phascolosoma (Sipuncula) from Australia. Transactions of the Royal Society of South Australia I09(2):43~44. Edmonds, S. J. 1987. Phyla Sipuncula and Echiura. In D. M. Devaney and L. G. Eldredge, eds., Reef and shore fauna of Hawaii. Honolulu: Bishop Museum Press, pp. 185-212. •Edmonds, S. J. 1991. Sipunculoidea and Echiuroidea: Sipunculans and echiurans from the Philippines and New Caledonia. In A. Crosnier, ed., R6sultats des Campagnes Musorston. M6moires du Mus6um National d'Histoire Naturelle de Paris 8A:83~90.
398
Bibliography
Eguileor, M. de, and R. Valvassori. 1977. Studies on the helical and paramyosinic muscles. VII. Fine structure of body wall muscles in Sipunculus nudus. Journal of Submicroscopic Cytology 9(4):363-372. Ekman, S. 1967. Zoogeography of the sea. London: Sidgwick and Jackson, 417 pp. Evans, E. E., J. E. Cushing, and M. L. Evans. 1973. Comparative imunology: Sipunculid bactericidal responses. Infectious Immunology 8(3):355-359. Ferrell, R. E., and G. B. Kitto. 1970. Characterization of Dendrostomum pyroides hemerythrin. Federation Proceedings 29(2):875. Ferrell, R. E.( and G. B. Kitto. 1971. The aminoterminal sequence of Dendrostomum pyroides hemerythrin. FEBS Letters I2(6):322~324. *Fischer, J. 1914. Die Sipunculoideen der Nord- und Ostsee, unter Beriicksichtigung von Formen des nordatlantischen Gebietes. Wissenschaftliche Meeresuntersuchungen Abteilung Kiel 16:85-125. *Fischer, W. 1892. Ubersicht der von Herrn Dr. F. Stuhlmann auf Sanzibar und an der gegeniiberliegenden Festlands-kiiste gesammelten Gephyreen. Jahrbuch der Hamburgischen Wissenschaftlichen Anstalten 9(2):79-89. *Fischer, W. 1893. Weitere Beitrage zur Anatomie und Histologic des Sipunculus indicus Peters. Jahrbuch der Hamburgischen Wissenschaftlichen Anstalten 10:1-12.
Fischer, W. 1895. Die Gephyreen des Naturhistorischen Museums zu Hamburg. Abhandlungen aus dem Gebiet der Naturwissenschaften (Hamburg) 13:124. Fischer, W. 1896. Gephyreen. In Semon, Zoologische Forschungsreisen im Australien und malayischen Archipel. Medizinisch-naturwissenschaftliche Gesellschaft zu Jena, Denkschriften 8:337-339. Fischer, W. 1913. Uber einige Sipunculiden des Naturhistorischen Museums zu Hamburg. Jahrbuch der Hamburgischen Wissenschaftlichen Anstalten 30(2):93-ioi. Fischer, W. 1914a. Gephyrea. Beitrage zur Kenntnis der Meeresfauna Westafrikas 1:57-84. Fischer, W. 1914b. Weitere Mitteilungen uber die Gephyreen des Naturhistorischen (Zoologischen) Museums zu Hamburg. Jahrbuch der Hamburgischen Wissenschaftlichen Anstalten 31:1-28. Fischer, W. 1916. Die Gephyreensausbeute der deutschen Tiefsee Expedition (1898-1899) Vorlaufige Mitteilung. Zoologischer Anzeiger 48:14-20. Fischer, W. 1919a. Gephyreen der Sudwestkuste Australiens. Zoologischer Anzeiger 50:277-285. Fischer, W. 1919b. Uber die Gattung Lithacrosiphon, eine neue SipunculidenGattung. Zoologischer Anzeiger 50:285-293. *Fischer, W. 1920. Gephyreen der antarktischen und sub-antarktischen Meere. Deutsche Siidpolar Expedition 16, Zoologie, 8:409-430. Fischer, W. 1921a. Results of Dr. E. Mjoberg's Swedish scientific expeditions to Australia, 1910-1913. 27. Gephyreen. Kungliga Svenska VetenskapsAkademiens Handlingar 61(8): 1-39.
Bibliography
399
Fischer, W. 1921b. Aspidosiphon pygmaeus n. sp., eine neue Gephyree aus Juan Fernandez. Natural History of Juan Fernandez and Easter Islands (Uppsala) 3:45-47Fischer, W. 1922a. Gephyreen des Reichsmuseums zu Stockholm. Arkiv for Zoologi i4(i9):i-39. Fischer, W. 1922b. Gephyreen der deutschen Tiefsee-Expedition, auf dem Dampfer "Valdivia" 1898-1899. Wissenschaftliche Ergebnisse der Deutschen Tiefsee-Expedition (Valdivia) 2 2 ( I ) : I - 2 6 . *Fischer, W. 1922c. Gephyreen der Arktischen Meere. Wissenschaftliche Meeresuntersuchungen Abteilung Helgoland 13:229-246. *Fischer, W. I922d. Westindische Gephyreen. Zoologischer Anzeiger 55:10-18. Fischer, W. 1923a. Zwei Sipunculiden des Kapgebietes nebst einer Zusammenstellung der bekannten Arten dieses Gebietes, und ihrer faunistischen Beziehung zur Ost- und Westkiiste. Goteborgs Kungliga Vetenskaps Vitterhets-Samhalles Handlingar 25(4):i-8. *Fischer, W. 1923b. Gephyreen des Golfes von Siam. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening 76:21-27. *Fischer, W. 1924. Beitrage zur Kenntnis der Sipunculiden. Uber die verwandtschaftlichen Beziehungen der Arten Phascolosoma margaritaceum Sars, Phascolion hanseni Koren und Danielssen und Phascolosoma trybomi Theel. Zoologischer Anzeiger 58:69-74. Fischer, W. 1925. Echuiriden, Sipunculiden, und Priapuliden. In G. Grimpe and E. Wagler, eds., Die Tierwelt der Nord- und Ostsee. Leipzig: Akademische Verlagsgesellschaft, pp. 1-55. Fischer, W. 1926. Sipunculiden und Echiuriden der Hamburger Siidsee Expedition 1908-1909. Mitteilungen aus dem Zoologischen Staatsinstitut und Zoologischen Museum in Hamburg 42:104-117. *Fischer, W. 1927. Sipunculoidea und Echiuroidea. In W. Michaelsen and R. Hartmeyer, eds., Die Fauna Sudwest-Australiens. Jena: Gustav Fischer, pp. 199-216. Fischer, W. 1928. Uber zwei neue Siphonosoma-Arten der Wurttembergischen Naturalien Sammlung zu Stuttgart. Zoologischer Anzeiger 76:138-143. Fischer, W. 1929. Die Sipunculiden, Priapuliden und Echiuriden der Arktis. In F. Romer and F. Schaudinn, eds., Fauna Arctica. Vol. 5. pp. 451-490. *Fischer, W. 1931. Sipunculidae. Mitteilungen aus dem Zoologischen Museum in Hamburg 44:130-140. Fisher, W. K. 1928. New Sipunculoidea from California. Annals and Magazine of Natural History, ser. 10, 1:194-199. Fisher, W. K. 1947. New genera and species of Echiuridae and sipunculid worms. Proceedings of the U.S. National Museum 97:351-372. Fisher, W. K. 1950a. The sipunculid genus Phascolosoma. Annals and Magazine of Natural History, ser. 12, 3:547-552. Fisher, W. K. 1950b. Two new subgenera and a new species of Siphonosoma (Sipunculoidea). Annals and Magazine of Natural History, ser. 12, 3:805808.
4oo
Bibliography
Fisher, W. K. 1952. The sipunculid worms of California and Baja California. ^-~ Proceedings of the U.S. National Museum 102:371-450. Fisher, W. K. 1954a. The genus Xenosiphon (Sipunculoidea). Annals and Maga" zine of Natural History, ser. 12, 7:311-315. Fisher, W. K. 1954b. A swimming Sipunculus. Annals and Magazine of Natural History, ser. 12, 7:238-240. Fisk, D. A. 1983. Free-living corals: Distributions according to sediments, hydrodynamic, depth and biological factors. Marine Biology (Berlin) 74(3):287~ 294. Fleming, C. A. 1978. Evolution of the South Pacific marine biota: The expanding fossil record. In Proceedings of the International Symposium of Marine Biogeography and Evolution in the Southern Hemisphere. New Zealand DSIR, Auckland, pp. 5-27. Florkin, M. 1969a. Respiratory proteins and oxygen transport. In M. Florkin and B. T. Scheer, eds., Chemical zoology. New York: Academic Press, pp. m - 1 3 2 . Florkin, M. 1969b. Nitrogen metabolism. In M. Florkin and B. T. Scheer, eds., *~r Chemical zoology. New York: Academic Press, pp. 147-160. Florkin, M. 1975. Biochemical evidence for the phylogenetic relationships of the ' Sipuncula. In M. E. Rice and M. Todorovic, eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Naudno Delo Press, pp. 95-110. Follmi, K. B., and M. Delamette, E. J. Barron, and W. H. Peterson. 1991. Model simulation of mid-Cretaceous ocean circulation. Science 251:94-95. Forbes, E. 1841. A history of British starfishes, and other animals of the class Echinodermata. London: J. van Voorst, 270 pp. Foster, R. C. 1974. Comparative biochemical studies of osmoregulation in Sipuncula. I. Steady-state characteristics of two sipunculids in full-strength sea ^ , water. Comparative Biochemistry and Physiology 47A:855-866. Frank, P. G. 1983. A checklist and bibliography of the Sipuncula from Canadian and adjacent waters. Syllogeus 46:1-47. Franklin, R. M. M., and B. G. Bang. 1980. Mucus stimulating factor in tears. Investigation in Opthalmology and Visual Science 9(4):430-432. Franzen, A., and R. Fange. 1962. Observation on haemerythrin-containing coelomocytes in invertebrates. Reports from the Third Scandinavian Conference on Cell Research. Freeman, G., and J. W. Lundelius. 1992. Evolutionary implications of the mode of D quadrant specification in coelomates with spiral cleavage. Journal of Evolutionary Biology 5(2):205-247. Frey, R. W., G. Pemberton, and J. A. Fagerstrom. 1984. Morphological, ethological and environmental significance of the ichnogenera Scoyenia and Ancorichnus. Journal of Paleonotology 58(2)1511-528. Gabe, M. 1953. Donn6es histologiques sur la neurosecretion chez quelques sipunculiens. Bulletin Laboratoire Maritime Dinard 38:3-15. Gadd, G. G. 1911. Verzeichnis der Gephyreen des Kolagolfes und zwei neue Species der Phascolosoma. Trudy Leningrad Obschchestva Estestvois Pytatelei 42:79-93.
Bibliography
401
Gage, J. 1968. The mode of life of Mysella cuneata, a bivalve "commensal" with Phascolion strombi (Sipunculoidea). Canadian Journal of Zoology 46:919934c^Gage, J. D. 1979. Mode of life and behavior of Montacuta phascolionis, a bivalve commensal with the sipunculan Phascolion strombi. Journal of the Marine Biological Association of the United Kingdom 59:635-658. Galtsoff, P. S. 1964. The American oyster, Crassostrea virginica. U.S. Fish and Wildlife Service Fishery Bulletin 64:1-480. Gebbinck, J. C. 1979. Some observations on concanavalin A receptors on free cells of marine invertebrates. American Zoologist 19:857. George, S. J., B. J. Pirie, and T. L. Coombs. 1980. Isolation and elemental analysis of metal-rich granules from the kidney of the scallop Pecten maximus. Journal of Experimental Marine Biology and Ecology 42:143-156. Ger, B. A., E. V. Zeimal, I. L. Kratskin, and V. V. Lavrenteva. 1977. Cholinergic mechanisms in the central nervous system of the sipunculid Physcosoma japonicum. Zhurnal Evolyutsionoi Biokhimii i Fiziologii I3(2):i79-i84. [English translation in Journal of Evolutionary Biochemistry and Physiology I3(2):i52-I56.] Jjerould, J. H. 1903. Studies on the embryology of the Sipunculidae. I. The embryonal envelope and its homologue. The Mark Anniversary Volume ^ 1903:437-452. (^Gerould, J. H. 1904. The development of Phascolosoma. Archives de Zoologie Exp^rimentale et G£n£rale 4(2): 17-29. •^Gerould, J. H. 1907. The development of Phascolosoma. Zoologische Jahrbiicher, Anatomie 2 3 ( I ) : 7 7 - I 6 2 .
Gerould, J. H. 1908. A comparison of the cephalic organs of certain Sipunculids. Science 27:488-489. Gerould, J. H. 1913. The sipunculids of the eastern coast of North America. Proceedings of the U.S. National Museum 44:373-437. Gerould, J. H. 1938. The eyes and nervous system of Phascolosoma verrillii and other sipunculids. Travaux Station zoologique de Wimereux 13:313-325. Gibbs, P. E. 1973. On the genus Golfingia (Sipuncula) in the Plymouth area with a description of a new species. Journal of the Marine Biological Association of the United Kingdom 53:73-86. Gibbs, P. E. 1974. Golfingia margaritacea (Sipuncula) in British waters. Journal of the Marine Biological Association of the United Kingdom 54:871-877. Gibbs, P. E. 1975. Gametogenesis and spawning in a hermaphroditic population of Golfingia minuta (Sipuncula). Journal of the Marine Biological Association of the United Kingdom 55:69-82. C*Gibbs, P. E. 1976. Notes on the reproductive cycles of several Golfingia species (Sipuncula). Journal of the Marine Biological Association of the United Kingdom 56:909-915. Gibbs, P. E. 1977a. On the status of Golfingia intermedia (Sipuncula). Journal of the Marine Biological Association of the United Kingdom 57:109-112. Gibbs, P. E. 1977b. British sipunculans. Synopses of the British Fauna 12. London: Linnean Society of London, 35 pp.
402
Bibliography
Gibbs, P. E. 1978a. Menestho diaphana (Gastropoda) and Montacuta phascolionis (Lamellibranchia) in association with the sipunculan Phascolion strombi in British waters. Journal of the Marine Biological Association of the United Kingdom 58:683-685. *Gibbs, P. E. 1978b. Macrofauna of the intertidal sand flats on low wooded islands, northern Great Barrier Reef. Philosophical Transactions of the Royal Society of London 284:81-97. Gibbs, P. E. 1982. The synonymy of the Golfingia species assigned to the Abyssorum section (Sipuncula). Sarsia 67:119-122. Gibbs, P. E. 1985. On the genus Phascolion with particular reference to the northeast Atlantic species. Journal of the Marine Biological Association of the United Kingdom 65:311 -323. ^uibbs, P. E. 1986. The taxonomy of some little-known Sipuncula from the north--— east Atlantic region including new records. Journal of the Marine Biological Association of the United Kingdom 66:335-341. Gibbs, P. E. 1987. A new species of Phascolosoma (Sipuncula) associated with a decaying whale's skull trawled at 880 m depth in the south-west Pacific. New ,-. Zealand Journal of Zoology 14:135-137. ''Gibbs, P. E., and E. B. Cutler. 1987. A classification of the phylum Sipuncula. ^ Bulletin of the British Museum of Natural History, Zoology 52(i):43~58. ^Gibbs, P. E., E. B. Cutler, and N. J. Cutler. 1983. A review of the genus Thy' sanocardia Fisher (Sipuncula). Zoologica Scripta i2(4):295-304. Gill, G. A., and A. G. Coates. 1977. Mobility, growth patterns, and substrate in some fossil and recent corals. Lethaia 10:119-134. Goffinet, G., M. F. Voss-Foucart, and S. Barzin. 1978. Ultrastructure of the cuticle of the sipunculans Golfingia vulgaris and Sipunculus nudus. Transactions of the American Microscopical Society 97(4):5I2~523. Gonse, P. 1956. L'ovogenese chez P. vulgare. II. Recherches biometriques sur les ovocytes. Acta Zoologica 37:225-233. Gosse, P. H. 1853. Notes on some new or little known marine animals. Annals and Magazine of Natural History, ser. 2, 12:124-128. Grant-Mackie, J. A. 1978. Cretaceous-Recent plate tectonic history and paleoceanographic development of the Southern Hemisphere. In Proceedings of the International Symposium on Marine Biogeography and Evolution in the Southern Hemisphere. New Zealand DSIR, Auckland, pp. 27-42. ^6ray, J. E. 1828. Spicilegia Zooligica. London: Treuttel Wurtz and Company, 12 ^ pp. Green, C. R., and P. R. Berquist. 1982. Phylogenetic relationships within the Invertebrata in relation to the structure of septate junctions and the development of occluding junctional types. Journal of Cell Science 53:279-306. Green, J. P., and D. F. Dunn. 1976. Chloride and osmotic balance in the euryhaline sipunculid Phascolosoma arcuatum from a Malaysian mangrove swamp. Biological Bulletin (Woods Hole) I50(2):2ii-22i. Green, J. P., and D. F. Dunn. 1977. Osmotic and ionic balance in the mangrove sipunculid, Phascolosoma arcuatum. Marine Research in Indonesia 18:61. Green, W. A. 1975a. The annual reproductive cycle of Phascolosoma lurco (Sipuncula). In M. E. Rice and M. Todorovic, eds., Proceedings of the Interna-
Bibliography
403
tional Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Nauciio Delo Press, pp. 161-168. Green, W. A. 1975b. Phascolosoma lurco: A semi-terrestrial sipunculan. In M. E. Rice and M. Todorovic, eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Nau£no Delo Press, pp. 267-280. Grieshaber, M. K., and U. Kreutzer. 1986. Opine formation in marine invertebrates. Zoologische Beitrage 3o(i-3):205-230. Grigg, R. W., and R. Hey. 1992. Paleoceanography of the tropical eastern Pacific Ocean. Science 255:172-178. Gross, W. J. 1954. Osmotic responses in the sipunculid Dendrostomum zostericolum. Journal of Experimental Biology 31:403-423. *Griibe, E. 1837. Versuch einer Anatomie des Sipunculus nudus. Archiv fur Anatomie und Physiologie (Leipzig) 1837:237-257. Griibe, E. 1840. Actinien, Echinodermen und Wiirmer des Adriatischen und Mittelmeers nach einigen Sammlungen beschrieben. Konigsberg: J. H. Bon. Griibe, E. 1868a. Naturwissenschaftliche Section mit einigen Sipunkuloiden bekannt und sprach namentlich iiber Loxosiphon, Cloeosiphon, und einige Phascolosomen. Jahres-Bericht der Schlesischen Gesellschaft fiir Vaterlandische Kultur 45:47-49. Griibe, E. 1868b. Beschreibungen einiger von Georg Ritter von Frauenfeld gesammelter Anneliden und Gephyreen des rothen Meeres. Verhandlungen der Kaiserlich-Koniglichen Zoologisch-Botanischen Gesellschaft in Wien 18: 629-650. *Griibe, E. 1870a. Bemerkungen iiber Anneliden des Pariser Museums. Archiv fiir Naturgeschichte (Berlin) 36(0:281-352. *Grube, E. 1870b. Ein Krankhafter bei Phascolosomen. Jahresbericht der Schlesischen Gesellschaft fiir Vaterlandische Cultur (Breslau) 47:70-71. ^Griibe, E. 1872. Mittheilungen Uber St. Malo und Roscoff und die dortige Meeres—besonders die Annelidenfauna. Abhandlungen der Schlesischen Gesellschaft fiir Vaterlandische Cultur. Abteilung fiir Naturwissenschaften und Medecin (Breslau) 1869-72:75-146. •Griibe, E. 1876. Einige neue Sipunculiden. Zeitschrift fiir die Gesammten Naturwissenschaften (Leipzig and Stuttgart) 48:46. Griibe, E. 1877. Vierundfunfzigster Jahresbericht der Schless. Gesellschaft fiir Vaterlandische Cultur (Breslau) 1877:73. Griibe, E., and A. S. Oersted. 1858. Annulata Oerstediana. Copenhagen: Videnskabelige Meddelelser fra Dansk naturhistorisk Forening i Kj0benhaven, pp. 105-120.
Guillou, Y. 1973. Phascoline (N-[3-guanidinopropionyl]-2-hydroxy-«-heptylamine) and phascolosomine (N-[3-guanidinoisobutyryl]-2-methoxy-n-heptylamine), two new guanidino compounds from sipunculid worms: Isolation and structure. Journal of Biological Chemistry 248(i6):5688-5672. Gunderson, J., and E. B. Small. 1986. Selenidium vivax, new species (Protozoa, Apicomplexa) from the sipunculid Phascolosoma agassizii. Journal of Parasitology 72(0:107-110. Gushima, K., and S. Kakuta. 1991. Growth-related changes in diet and foraging
Bibliography
404
behavior of the yellow wrasse Thalasoma lutescens at Kuchierabu Island. Japanese Journal of Ichthyology 38(3):307~3i4. Habe, T., and T. Kanazawa. 1981. A new commensal bivalve from the Philippines (Montacutidae). Venus, Japanese Journal of Malacology 40(3): 123-125. Hadzi, J. 1975. The position of the Sipuncula in the system of the animal kingdom. In M. E. Rice and M. Todorovid, eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: NauCno Delo Press, pp. 91-94. *Haldar, B. P. 1975. Sipuncula of the Indian Ocean in the collection of the Zoological Society of India. In M. E. Rice and M. Todorovid, eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: NauSno Delo Press, pp. 51-59. *Haldar, B. P. 1976. Sipuncula from the Andaman and Nicobar islands. Records of the Zoological Survey of India 70:109. Haldar, B. P. 1978. Aspidosiphon (Paraspidosiphon) havelockensis, a new Sipuncula from the Andamans, India. Bulletin of the Zoological Survey of India i(i):37-4i.
Haldar, B. P. 1991. Sipunculans of the Indian coast. Memoirs of the Zoological Survey of India I7(4):i-i69. *Haldar, B. P., and V. R. R. Koza. 1975. A note on Siphonosoma sp. a giant ^_ sipuncula from south India. Indian Journal of Zoology i6(3):i79-i8o. Hall, J. R., and R. S. Scheltema. 1966. Morphology of North Atlantic sipunculid larvae. American Zoologist 6(3):i93. Hall, J. R., and R. S. Scheltema. 1975a. The dispersal of pelagosphaera larvae by ocean currents and its relationship to the geographical distribution of sipunculans. In M. E. Rice and M. Todorovic\ eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Naucno Delo Press, pp. 103-116. Hall, J. R., and R. S. Scheltema. 1975b. Comparative morphology of open-ocean pelagosphaera. In M. E. Rice and M. Todorovi<5, eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Nau£no Delo Press, pp. 183-198. Hamilton, E. L. 1956. Sunken islands of the mid-Pacific mountains. Geology Society of America Memoirs 64:1-97. Hammond, A. L. 1976. Paleoceanography: Sea floor clues to earlier environments. Science 191:168-170. Hansen, M. D. 1978. Nahrung und Fressverhalten bei Sedimentfressem dargesteilt am Beispiel von Sipunculiden und Holothurien. Helgolander Wissenschaftliche Meeresuntersuchungen 31:191-221. Hardewig, I., A. D. F. Addink, M. K. Grieshaber, H. O. Poertner, and G. van den Thillart. 1991. Metabolic rates at different oxygen levels determined by direct and indirect calorimetry in the oxyconformer Sipunculus nudus. Journal of Experimental Biology 157:143-160. Hardewig, I., U. Kreutzer, H. O. Poertner, and M. K. Grieshaber. 1991. The role of phosphofructokinase in glycolytic control in the facultative anaerobe Sipunculus nudus. Journal of Comparative Physiology B i6i(6):58i-589.
Bibliography
405
Harms, J. W., and D. Dragendorff. 1933. Die Realisation von Genen und die consecutive Adaptation. 3 Mitteilung. Osmotische Untersuchungen an Physcosoma lurco Sel. et de Man, aus den Mangrove-Vorlandern der SundaInseln. Zeitschrift fur Wissenschaftliche Zoologie 143:262-322. Harms, W. 1921. Morphologische und kausal-analytische Untersuchungen iiber das Internephridialorgan von Physcosoma lanzarotae. Archiv fur Entwicklungsmechanik der Organismen 47:307-374. •Harms, W. 1922. Bauchnervenstrang und Spindelmuskel von Physcosoma in Anpassung an die Formveranderungen dieses Tieres. Zoologischer Anzeiger ^ 52:67-76. Hatschek, B. 1881. Entwicklungsgeschichte von Echiurus und die systematische Stellung der Echiuridae. Arbeiten der Zoologischen Institut der Universitat Wien 3:45-79Hatschek, B. 1883. Uber Entwicklung von Sipunculus nuds. Arbeiten aus dem Zoologischen Institut der Universitat Wien 5:61-140. Hayward, B. W. 1976. Lower Miocene bathyal and submarine canyon ichnocoenoses from Northland, New Zealand. Lethaia 9:149-162. Hendrickson, W. A., and G. L. Klippenstein. 1974. Crystals of myohemerythrin. Journal of Molecular Biology 87(i):i47-i49. Hendrickson, W. A., J. L. Smith, and S. Sheriff. 1985. Structure and function of hemeryfhrins. In J. Lamy, J. R Truch, and R. Gilles, eds., Respiratory pigments in animals. New York: Springer-Verlag, pp. 1-8. Hendrix, G. Y. 1975. A review of the genus Phascolion (Sipuncula) with the descriptions of two new species from the western Atlantic. In M. E. Rice and M. Todorovic, eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: NauCno Delo Press, pp. 117140. Henry, R. P. 1987. Invertebrate red blood cell carbonic anhydrase. Journal of Experimental Zoology 242(i):ii3-n6. Hermans, C. O., and R. M. Eakin. 1975. Sipunculan ocelli: Fine structure in Phascolosoma agassizii. In M. E. Rice and M. Todorovic, eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: NauSno Delo Press, pp. 229-240. Heiubel, M. A. 1902. Sur certains elements peritoneaux du phascolosome (Phascolosoma vulgare de Blainv.). Bulletin de la Societe Zoologique de France 27:105-114. Heiubel, M. A. 1903a. Sur la distribution et les affinites reciproques des Sipunculides. Bulletin de la Societe Zoologique de France 28:99-111. *H6rubel, M. A. 1903b. Premiere contribution a la morphologie et physiologie comparees et a la biostatique des Sipunculides. Bulletin de la Socieie' Zoologique de France 28:111-125. ^Heiubel, M. A. 1903c. Observations physiologiques et histologiques sur les G6phyriens (d6rives endotheliaux et granules pigmentaires). Comptes Rendus Hebdomadaires des Stances de l'Academie des Sciences (Paris) 136:971-973. Heiubel, M. A. 1904a. Sur les sipunculides nouveaux rapport^s de la mer rouge,
406
Bibliography
par M. Ch. Gravier (note preliminaire). Bulletin du Museum National d'Histoire Naturelle de Paris 10:476-480. Herubel, M. A. 1904b. Liste des sipunculides et des 6chiurides rapport^s par M. Ch. Gravier du Golfe de Tadjourah (Mer Rouge). Bulletin du Museum National d'Histoire Naturelle de Paris 10:562-565. *Herubel, M. A. 1904c. Sur une nouvelle espece du genre Sipunculus. International Congress of Zoology 6:690-695. *Herubel, M. A. 1905a. Sur les productions tegumentaires des sipunculides. Bulletin de la Societe Zoologique de France 30:90-97. *Herubel, M. A. 1905b. Sur un nouveau siponcle de la collection du museum (Sipunculus joubini sp. nov.). Bulletin du Museum National d'Histoire Naturelle de Paris 11:51-54. Herubel, M. A. 1906a. Sur les sipunculides rapportes par 1'Expedition Charcot. Note preliminaire. Bulletin du Museum National d'Histoire Naturelle de Paris 12:127-128. *Herubel, M. A. 1906b. A propos de l'anatomie compared des sipunculides. Comptes Rendus Academie des Sciences (Paris) 142:651-652. * Herubel, M. A. 1906c. Sur une tumeur chez un invertebre {Sipunculus nudus). Comptes Rendus, Hebdomadaires des Seances de l'Acad6mie des Sciences (Paris) 143:979-981. Herubel, M. A. 1907. Recherches sur les sipunculides. Memoires de la Soci6te Zoologique de France 20:107-418. *Herubel, M. A. 1908. Expedition antarctique francaise (1903-1905) commanded par le Dr. Jean Charcot. Gephyriens. Documents Scientifiques. Paris: Maison et Cie, 8:1-8. * Herubel, M. A. 1924. Quelques echirudes et sipunculides des cotes du Maroc et du Mauritanie. Bulletin de la Soci6te des Sciences Naturelles du Maroc 4:108-112. Herubel, M. A. 1925a. Quelques 6chiurides et sipunculides des cotes du Maroc. Bulletin de la Societe des Sciences Naturelle du Maroc 5:260-263. *Herubel, M. A. 1925b. Description de Phascolosoma reticulatum nov. sp. Bulletin de la Societe Zoologique de France 50:272-277. Highsmith, R. C, R. L. Leuptow, and S. C. Schonberg. 1983. Growth and bioerosion of 3 massive corals on the Belize barrier reef. Marine Ecology Program Series I 3 ( 2 - 3 ) : 2 6 I - 2 7 2 .
Ho, J. S., F. Katsumi, and Y. Honma. 1981. Coelotrophus nudus, new genus new species, an andoparasitic copepod causing sterility in sipunculan, Phascolosoma scolops from Sado Island, Japan. Parasitology 82(3):481-488. Hoeksema, B. W., and M. B. Best. 1991. New observations on scleractinian corals from Indonesia. 2. Sipunculan-associated species belonging to the genera Hetercyathus and Heteropsammia. Zoologische Mededelingen (Leiden) 65(i5):22i-245. Hogue, E. W., and L. C. Oglesby. 1972. Further observations on salt balance in the sipunculid worm Themiste dyscritum. Comparative Biochemistry and Physiology 42A:9i5~926. Horst, R. 1882. Die Gephyrea gesammelt wahrend der zwei ersten Fahrten des
Bibliography
407
William Barents. III. Sipunculida. Niederlandisches Archiv filr Zoologie i(4):39-40. Horst, R. 1899. Aspidosiphon cylindricus, n. sp. Notes from the Leyden Museum (Rijks Museem van natuurlijke historie) 20:195-198. Hoshide, K., and K. S. Todd, Jr. 1992. Structure and function of the mucron of Filipodium ozakii Hukui 1939 (Apicomplexa, Gregarina). Proceedings of the Zoological Society (Calcutta) 45:53-59. Hughes, R. N. 1974. A re-description of Lithacrosiphon maldivensis Shipley, 1902. Zoological Journal of the Linnean Society 55(3):235-240. Hutton, W. K. 1879. Additions to the list of New Zealand worms. Transactions of the Royal Society of New Zealand 12:277-278. Hutton, W. K. 1903. On the anatomy of the gephyreen Phascolosoma teres n. sp. Proceedings of the Zoological Society of London 1:29-41. Hylleberg, J. 1969. Irrigation in the sipunculid Phascolion strombi. Ophelia 7:101-112.
Hylleberg, J. 1970. Fauna associated with the sipunculid Phascolion strombi (Montagu), especially the parasitic gastropod Menestho diaphana (Jeffreys). Ophelia 7(2):257-276. Hylleberg, J. 1975. On the ecology of the sipunculan Phascolion strombi (Montagu). In M. E. Rice and M. Todorovic, eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Nau5no Delo Press, pp. 241-250. Hylleberg, J., and A. Nateewathana. 1983. Effects of offshore tin mining on benthos of the west coast of Phuket, Thailand. In Pacific Science Association, Fifteenth Congress Proceedings, pp. 110-111. Hyman, L. H. 1959. Phylum Sipunculida. In L. H. Hyman, The invertebrates. Vol. 5: Smaller coelomate groups. New York: McGraw-Hill, pp. 610-690. Ikeda, 1.1904. The Gephyrea of Japan. Journal of the College of Science, Imperial University of Tokyo 20(4):i-87. Ikeda, I. 1905. Gephyreans collected by Professor Dean at Manjuyodi, Southern Negros (Philippine Islands). Annotationes Zoologicae Japonenses 5:169Ikeda, I. 1924. Further notes on the Gephyrea of Japan, with descriptions of some ~ new species from the Marshall, Caroline, and Palau islands. Japanese Journal of Zoology 1:23-44. Illg, P. 1975. Copepod associates of Sipuncula and Echiura. In M. E. Rice and M. Todorovic\ eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Nau5no Delo Press, pp. 335342. Ingermann, R. L., R. E. Hall, J. M. Bissonnette, and R. C. Terwilliger. 1985. Monosaccharide transport into hemocytes of a sipunculan worm Themiste dyscrita. American Journal of Physiology 249:Ri39-Ri44. Ingermann, R. L., and G. L. Virgin. 1987. Glycogen content and release of glucose from red blood cells of the sipunculan worm Themiste dyscrita. Journal of Experimental Biology I29(4):i4i-i49. Ionescu-Varo, M., and M. Tufescu. 1982. Quantitative remarks on immune evolu-
408
Bibliography
tion in the animal series. Revue Roumaine de Biologie, Serie de Biologie Animale 27(i):29~39. Ivanov, A. V. 1983. Evolution and system of the coelomata. Zoologicheski Zhurnal 44--3-9Ivanov, A. V. 1988. Analysis of the embryonic development of Pogonophora in connection with the problems of phylogenetics. Zeitschrift fur zoologische Systematik und Evolutionsforschung 26:161-185. Ivanova-Kazas, O. M. 1985. The origin and phylogenetic significance of the trochophoran larvae. 2. Evolutionary significance of the larvae of coelomate worms and mollusks. Zoologicheski Zhurnal 64(5):6so-66o. Iwamoto, H., S. Suzuki, and H. Mizobe. 1986. Contraction and its regulation in the proboscis retractor muscle of a sipunculid. Zoological Science (Tokyo) 3(6):967. Jablonski, D., and D. J. Bottjer. 1991. Environmental patterns in the origins of higher taxa: The post-Paleozoic fossil record. Science 252:1831-1833. Jagersten, G. 1963. On morphology and behavior of pelagosphaera larvae (Sipunculoidea). Zoologiska Bidrag frfl Uppsala 36(0:27-36. Jansen, J. H. E, A. Kuijpers, and S. R. Troelstra. 1986. A mid-brunhes climatic event: Long-term changes in global atmosphere and ocean circulation. Science 232:619-622. Jeuniaux, C. 1969. Nutrition and digestion. In M. Florkin and B. T. Scheer, eds., Chemical zoology. London: Academic Press, pp. 88-89. Johnson, P. 1964. Two new species of Aspidosiphon (Sipunculoidea). Annals and Magazine of Natural History, ser. 13, 7:331-335. Johnson, P. 1969. A new subgenus of Xenosiphon (Sipunculiodae) and description of a new species from Indian waters. Journal of the Bombay Natural History Society 66(i):43-46. Johnson, P. 1971. On a collection of sipunculids from Indian waters. Journal of the Bombay Natural History Society 68(3):596-6o8. Johnson, P., and F. Chapman. 1970. Comparative studies on the in vitro response of bacteria to invertebrate body fluids. I. Dendrostomum zostericolum, a sipunculid worm. Journal of Invertebrate Pathology 16:127-138. Jones, I. 1975. Further studies on the distribution and morphology of intestinal sporozoa of Phascolosoma antillarum in the Caribbean and Florida. In M. E. Rice and M. Todorovic, eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Naudno Delo Press, PP- 349-355Jones, I., and M. C. Schiess. 1975. The occurrence of some intestinal and coelomic parasites of Phascolosoma varians of Puerto Rico. In M. E. Rice and M. Todorovic, eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Naucno Delo Press, pp. 343347Jorge, F. B. de, J. A. Petersen, and A. S. F. Ditadi. 1970. Comparative biochemical studies in Sipunculus natans and Sipunculus multisulcatus (Sipuncula). Comparative Biochemistry and Physiology 35:163-177.
Bibliography
409
Jourdan, E. 1891. Les corpuscles sensitifs et les glandes cutin6es des G6phyriens inermes. Annales des Sciences Naturelles, ser. 7, 12:1-13, Kay, E. A. 1979. Little worlds of the Pacific, an essay on Pacific Ocean biogeography. Harold Lyon Arboretum, University of Hawaii, Honolulu, 40 pp. *Keferstein, W. 1862a. Uber die Gattung Phascolosoma. Nachrichten von der Koniglichen Gesellschaft der Wissenschaften und der Georg-Augusts Universitat zu Gottingen 1862:65-67. *Keferstein, W. 1862b. Beitrage zur Kenntniss der Gattung Phascolosoma F. S. Leuckart. Zeitschrift fiir Wissenschaftliche Zoologie (Leipzig) 12:35-51, I39-I4IKeferstein, W. 1865a. Beitrage zur anatomischen und systematischen Kenntnis der Sipunculiden. Nachrichten von der Koniglichen Gesellschaft der Wissenschaften und der Georg-Augusts Universitat zu Gottingen 1865:189-209. Keferstein, W. 1865b. Beitrage zur anatomischen und systematischen Kenntniss der Sipunculiden. Zeitschrift fiir Wissenschaftliche Zoologie 15:404-445. Keferstein, W. 1866. Untersuchungen iiber einige amerikanische Sipunculiden. Nachrichten von der Koniglichen Gesellschaft der Wissenschaften und der Georg-Augusts Universitat zu Gottigen 14:215-228. Keferstein, W. 1867. Untersuchungen iiber einige amerikanische Sipunculiden. Zeitschrift fiir Wissenschaftliche Zoologie 17:44-55. (^Keferstein, W., and E. Ehlers. i860. Auszug aus den Untersuchungen iiber die ~ Anatomie des Sipunculus. Nachrichten von der Koniglichen Gesellschaft der Wissenschaften und der Georg-Augusts Universitat zu Gottingen 1860:282__ 286. CjKeferstein, W, and E. Ehlers. 1861. Untersuchungen uber die Anatomie des Sipunculus nudus. In Zoologisch Beitrage gesammelt im Winter 1859-60 in Neapel and Messina. Leipzig: Wilhelm Englemann, pp. 35-52. Keigwin, L. 1982. Isotrophic paleoceanography of the Caribbean and east Pacific: Role of Panama uplift in late Neogene time. Science 217:350-352. Kennett, J. P., and L. D. Stott. 1991. Abrupt deep sea warming, paleoceanographic changes in benthic extinctions at the end of the Paleocene. Nature 353:225229. Kesteven, H. L. 1903. A new species of Dendrostoma. Records of the Australian Museum 5:69-73. Kido, T., and Y. Kishida. 1961. Histological observation in the early regeneration of the introvert of Siphonosoma cumanense. Annal and Report of the Noto Marine Biological Laboratory 1:1-6. Klein, R., O. Mokady, and Y. Loya. 1991. Bioerosion in ancient and contemporary corals of the genus Pontes: Patterns and palaeoenvironmental implications. Marine Ecology Progress Series 77:245-251. Klepal, W. 1987. The anchoring fiber apparatus in the sperm of Aspidosiphon sp. (Sipunculida). European Journal of Cell Biology, supplement 18:18. Klotz, I. M., G. L. Klippenstein, and W. A. Hendrickson. 1976. Hemerythrin: Alternative oxygen carrier. Science 192:335-344. Kmiecik, D., M. Couppez, D. Belaiche, and P. Sautiere. 1983. Primary structure of
4io
Bibliography
histone H2A from nucleated erythrocyte of the marine worm Sipunculus nudus: Presence of 2 forms of H2A in the sipunculid chromatin. European Journal of Biochemistry I35(i):ii3-i22. Knox, G. A. 1978. Distribution patterns of Southern Hemisphere marine biotas: Some comments on their origin and evolution. In Proceedings of the International Symposium of Marine Biogeography and Evolution in the Southern Hemisphere. New Zealand DSIR, Auckland, pp. 43-83. Knudsen, J. 1944. A gephyean, a polychaete and a bivalve (Jousseaumiellia conchavum n. sp.) living together (commensalistically) in the Indo-Malayan seas. Videnskabelige Meddelelser fra Danske Naturhistorisk Forening 108:15-24. Kohn, A. J. 1975. Predation on sipunculans. In M. E. Rice and M. Todorovic, eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Nau&io Delo Press, pp. 313-334. Kohn, A. J. 1978. Gastropods as predators and prey at Easter Island. Pacific Science 32(0:35-38. Konopka, H. P. 1978. Endolithische Sipunculiden. Natur und Museum 108:137143Konopka, H. P. 1979. Zur geographischen Verbreitung von Aspidosiphon muelleri (Sipunculida). Zoologische Beitrage (Bonn) 3o(i-2):22o-223. Koren, J., and D. C. Danielssen. 1875. Bidrag til de norske Gephyrea naturhistorie. Nytt Magasin for Naturvidenskaberne 21:108-138. Koren, J., and D. C. Danielssen. 1877. The natural history of the Norwegian Gephyreae. In M. Sars, ed., Fauna Littoralis Norvegiae. Christiania: Druck und Verlag von Johann Dahl, pp. m - 1 5 6 . Kostetskii, E. Y. 1984. The phospholipid composition of Spongia, Coelenterata and free living Platyhelminthes, Nemertini, Annelida, Sipunculida and Echiurida. Bioloiya Morya (Vladivostok) 5:46-53. Kostetskii, E. Y., and U. A. Shchipunov. 1983. Evolution of phospholipid composition of marine invertebrates. Journal of Evolutionary Biochemistry and Physiology I9(i):n-i9. Krassner, S. M., and B. Flory. 1970. Antibacterial factors in the sipunculid worms Golfingia gouldii and Dendrostomum pyroides. Journal of Invertebrate Pathology i6(3):33i-338. Kreutzer, U., B. R. Siegmund, and M. K. Grieshaber. 1989. Parameters controlling opine formation during muscular activity and environmental hypoxia. Journal of Comparative Physiology B 159:617-628. Kulemann-Kloene, H., S. S. Krag, and F. B. Bang. 1982. Mucus secretionstimulating activity in human lymphoblastoid cells. Science 217:736-737. Kurlandsky, L. E., R. W. Berninger, and R. C. Talamo. 1980. Mucus-stimulating activity in the sera of patients with cystic fibrosis: Demonstration and preliminary fractionation. Pediatric Research I4(i):i263-i268. Kurtz, D. M. 1986. Structure, function, and oxidation levels of hemerythrin. In B. Linzen, ed., Invertebrate oxygen carriers: International conference. Berlin: Springer-Verlag, pp. 8-22. Laguna, J. E. 1987. Euraphia eastropacensis (Cirripedia, (Chthamaloidea), a new
Bibliography
411
species of barnacle from the tropical eastern Pacific: Morphological and electrophoretic comparisons with E. rhizophorae from the tropical western Atlantic and molecular evolution implication. Pacific Science 41:132-140. Lake, J. A. 1990. Origin of the Metazoa. Proceedings of the National Academy of Sciences U.S.A. 87:763-766. Lamarck, J. B. 1816. Histoire naturelle des animaux sans vertebres. Vol. 3: Radiaires, vers, crustac6s, insectes. Paris: Verdiere, 586 pp. *Lanchester, W. F. 1905a. On a collection of sipunculids made at Singapore and Malacca. Proceedings of the Zoological Society of London 1:26-28. Lanchester, W. F. 1905b. Gephyrea in the marine fauna of Zanzibar and British East Africa from the collections made by C. Crossland in 1901 -1902. Proceedings of the Zoological Society of London 1:28-35. Lanchester, W. F. 1905c. On the sipunculids and echiurids collected during the Skeat expedition to the Malay Peninsula. Proceedings of the Zoological Society of London 1:35-41. Lanchester, W. F. 1908. Sipunculoidea of the National Antarctic Expedition 1901^_ 1904. Natural History 4:1-6. Lang, A. 1888. Lehrbuch der vergleichenden Anatomie zum Gebrauche bei ver"~~ gleichenden anatomischen und zoologischen Vorlesungen. Neunte ganzlich umgearbeitete Auflage von E. O. Schmidt's Handbuch der vergleichenden Anatomie. Vol. 1. Jena, 290 pp. Lankester, E. R. 1885a. Golfingia mackintoshii, a new sipunculid from the coast of Scotland. Transactions of the Linnean Society of London, Zoology, ser. 2, ^ 11:469-474. Lankester, E. R. 1885b. Polyzoa. In Encylopaedia Britannica. 9th ed., vol. 19. *Lankester, E. R. 1908. The ciliated urns of the sipunculids. Nature 78:31. Lehman, W., and A. G. Szent-Gyorgyi. 1975. Regulation of muscular contraction: Distribution of actin control and myosin control in the animal kingdom. Journal of General Physiology 66(1): 1-30. Leroy, P. 1936. Les sipunculiens du Museum National d'Histoire Naturelle de Paris. Bulletin du Museum National d'Histoire Naturelle de Paris, ser. 2, 8:423-426. Leroy, P. 1942. Sipunculiens d'Indochine. Note, Institut Oceanographique de l'lndochine. Station Maritime de Cauda 40:1-51. Leuckart, F. S. 1828. Breves animalium quorundam maxima ex parte marinorum descriptiones. Heidelberg: Ausgusti Osswaldi, pp. 9-23. Leuckart, F. S., and W. P. S. Ruppell. 1828. Neue wirbellose Thiere des rothen Meers. In W. P. S. Ruppell, Atlas zu der Reise im nordlichen Africa, Zoologie 1:6-9. Lewbel, G. S. 1985. Strengths and weaknesses of damage assessment programs: The Ixtoc-I and Burmah Agate oil spills, and the benthic macroinfauna of the Texas (USA) continental shelf. Texas Journal of Science 37(4)1269-310. LiGreci, F. 1980. Sul rinvenimento di un sipunculidae del genere Aspidosiphon, Diesing 1851, sui fondali batiali della Sicilia occidentale. Rivista di Parassitologia 4 i ( i ) : i 2 3 - i 3 4 . Lim, R. W. L., and Y. K. Ip. 1991a. Alteration of kinetic properties of pyruvate
412
Bibliography
kinase in Phascolosoma arcuatum (Sipunculida) exposed to environmental anoxia. Journal of Experimental Marine Biology and Ecology 152(1): 123134Lim, R. W. L., and Y. K. Ip. 1991b. The involvement of phosphoenolpyruvate carboxykinase in succinate formation in Phascolosoma arcuatum (Sipuncula) exposed to environmental anoxia. Zoological Science (Tokyo) 8(4):673-68o. Lindberg, D. R. 1991. Marine biotic interchange between the Northern and Southern hemispheres. Paleobiology i7(3):3o8-324. Linnaeus, C. 1766. Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differetiis, synonymis, locis. Editio duodecima, reformata. Vol. 1: Regnum animale. Stockholm: Holmiae, 532 pp. Littler, M. M., D. S. Littler, S. M. Blair, and J. N. Norris. 1985. Speciation and stasis in marine ostracoda: Climatic modulation of evolution. Science 227:60-61. Livingstone, D. R., A. Dezwaan, M. Leopold, and E. Marteijn. 1983. Studies on the phylogenetic distribution of pyruvate oxidoreductases. Biochemical Systematics and Ecology i(4):4i5-425. Long, R. C, J. H. Zhang, D. M. Kurtz, A. Negri, G. Tedeschi, and F. Bomomi. 1992. Myohemerythrin from the sipunculid Phascolopsis gouldii: Purification, properties and amino acid sequence. Biochimica et Biophysica Acta H22(2):i36-i42. Lopez Rond6n, I. S., J. I. Saiz Salinas, and M. C. Diaz Vilela. 1984. Sobre la fauna de sipunculidos (Sipuncula) del Archipelago Canario. In V. MonteiroMarques, ed., Actas do IV simp6sio ib6rico de estudos do benthos marinho. Associacao de Estudantes da Faculdade de Ciencias de Lisboa, pp. 189196. Love, W. E. 1957. The X-ray molecular weight of hemeryfhrin from Phascolosoma gouldi and some notes on the oxygenation reaction. Biochimica et Biophysica 23:465-471. Lutzen, J. 1968. Heliogabalus phascolia, sp. n., an ectoparasitic copepod of Phascolion strombi (Montagu) off the coast of New England. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening i Kj0benhaven 131:209-216. McBride, E. E, and M. D. Picard. 1991. Facies implications of Trichichnus and Chondrites in turbidites and hemipelagites, Marnoso-arenacea formation (Miocene), northern Apennine, Italy. Palaios 6(3):281-290. McDonald, J. D. 1862. Observations on some Australian and Feegeean Heterocyathus and their parasitical Sipunculus. Natural History Review 1862:7881. MacGinitie, G. E. 1935. Ecological aspects of a California marine estuary. American Midland Naturalist 16:629-763. Mack, H. von. 1902. Das Centralnervensystem von Sipunculus nudus L. (Bauchstrang). Mit besonderer Berueksichtigung des Stutzgewebes. Eine histologische Untersuchung. Arbeiten aus dem Zoologischen Institut der Universitat Wien 13:237-334. Maes, V. O. 1983. Observations on the systematics and biology of a turrid gastro-
Bibliography
413
pod assemblage in the British Virgin Islands. Bulletin of Marine Science 33(2):305-335. Mainoya, J. R. 1974. Morphological and histochemical observations on the nervous systems of two sipuncuhd species, Siphonosoma australe and 5. cumanse. Marine Biology 27:275-280. Manavalaramanujam, R. 1971. Nature of the green pigment from the subepidermal connective tissue of Sipunculus nudus L., a sipunculan worm. Current Science 40:574-575. Manavalaramanujam, R. 1974. Studies of the cuticle and related structures in Sipuncula. Synopsis of unpublished thesis, Madras University. Manavalaramanujan, R. 1982. Mechanism of calcification of the anterior shield of Cloeosiphon aspergillus (Sipuncula). Journal of Animal Morphology and Physiology 29(1-2): 126-131.
Manchenko, G. P., and E. S. Balakirev. 1985. Allozymic variation of alanopine dehydrogenase: A new genie marker in marine invertebrates. Genetika 2i(3):397-40i. Mangum, C. P. 1990. The role of physiology and biochemistry in understanding animal phylogeny. Proceedings of the Biological Society of Washington i03(i):235-247. Mangum, C. P., and L. E. Burnett. 1987. Responses of sipuncuhd hemerythrins to inorganic ions and C0 2 . Journal of Experimental Zoology 244:59-65. Mangum, C. P., and M. Kondon. 1975. The role of coelomic hemerythrin in the sipuncuhd worm Phascolopsis gouldii. Comparative Biochemistry and Physiology 50A:7778-7785. Manning, R. B., and B. Morton. 1987. Pinnotherids (Crustacea: Decapoda) and Leptonaceans (Mollusca: Bivalvia) associated with sipunculan worms in Hong Kong. Proceedings of the Biological Society of Washington ioo(3):543-55i. Manwell, C. i960. Oxygen transfer systems involving haemerythrins in sipuncuhd worms of different ecologies. Comparative Biochemistry and Physiology 1:277-285. Manwell, C. 1963. Genetic control of haemerythrin specificity in a marine worm. Science 139:755-758. Manwell, C. 1977. Superoxide dismutase and NADH diaphorase in haemerythrocytes of sipunculans. Comparative Biochemistry and Physiology 58B(4):33i-338Martin, M. 1786. Observations on marine worms, insects, etc. [Cited by Hyman, 1959:690.] Martinez, J. L. 1973. Notas sobre la histologia y ultrastructura del sistema nervioso de Phascolosoma granulation (Sipunculoidea). Separata de la Revista de la Facultad de Ciencias (Oviedo) I4(2):i23-i32. Mayr, E. 1988. Plattentektonik und die Geschichte der Vogelfaunen. Proceedings of the International 100 DO-G Meeting, Current Topics in Avian Biology, Bonn 100:1-17. Mazen, A., and M. Champagne. 1976. Histones from nucleolated erythrocytes of the marine invertebrate Sipunculus nudus. Cell Research 103(1):! 19-125.
414
Bibliography
Mazen, A. M. C, M. Wilhelm, and F. X. Wilhelm. 1978. The structure of Sipunculus nudus erythrocyte chromatin. Experimental Cell Research 117(2)1431^ 43«Metalnikoff, S. J. 1899. Das Blut und die Excretionsorgane von Sipunculus nudus. ~^L Stazione Zoologica (Naples) 13:440-447. Metalnikoff, S. J. 1900. Sipunculus nudus. Zeitschrift fiir Wissenschaftliche Zoologie 68:261-322. Michaelsen, W. 1889. Die Gephyreen von Sud-Georgien nach der Ausbeute der deutschen Station von 1882-1883. Jahrbuch der Hamburgischen Wissenschaftliche Anstalten 6:73-84. Michel, C, C. L. Brown, E. J. DeVillez, and C. H. U. Xavier-Bichat. 1980. Properties and secretion of chymotrypsin of the sipunculan Phascolopsis gouldii. American Zoologist 20(4):796. Michel, C, and E. J. DeVillez. 1983. Etude cytologique, histochimique et immunobiochimique du tube digestif du Sipunculide Phascolopsis gouldii. Bulletin de la Societe Zoologique de France io8(4):69i-692. Michel, C, and E. J. DeVillez. 1984. Cytological and histochemical observations on the secretions in the digestive tract of the sipunculan Phascolopsis gouldii. Cellular and Molecular Biology 30(3):257-268. Migotto, A. E., and A. S. F. Ditadi. 1988. Aspidosiphonidae (Sipuncula) from the northern and northeastern coast of Brazil. Revista Brasileira de Biologia 48(2):245-263. Mobius, K. 1875. V. Vermes. Kommission zur wissenschaftlichen Untersuchung des deutschen Meeres in Kiel 1872-1873, pp. 150-170. Montagu, G. 1804. Description of several marine animals found on the south coast of Devonshire. Transactions of the Linnean Society of London 7:61-85. Moritz, K., and V. Storch. 1970. The fine structure of the integument of priapulids and sipunculids (Priapulus caudatus, Phascolion strombi). Zeitschrift fiir Zellforschung und Mikroskopische Anatomie, Histochemie i05(i):55-64. Morris, S. C. 1985. Non-skeletalized lower invertebrate fossils: A review. In S. C. Morris, J. D. George, R. Gibson, and H. M. Piatt, eds., The origins and relationships of lower invertebrates. Oxford: Oxford University Press, PP- 343-359Morris, S. C. 1989. Burgess Shale faunas and the Cambrian explosion. Science 246:339-346. Miiller, J. 1844. Uber einem neuen Wurm Sipunculus (Phascolosoma) scutatus. Archiv fiir Naturgeschichte 10:166-168. Murina, V. V. 1957a. Abyssal sipunculids (genus Phascolion Th6el) of the northwestern part of the Pacific collected by Vitjaz expeditions in 1950-1955. Zoologicheskii Zhurnal 36(i2):i777-i79i. Murina, V. V. 1957b. Sipunculids collected on the first trip of the complex Antarctic expedition on the Ob in 1956. Zoologicheskii Zhurnal 36(7)-.992-998. *Murina, V. V. 1958. On the systematics of two closely related species of the deepwater sipunculids of the genus Golfingia according to the materials of the Vitjaz expeditions in 1950-1955. Zoologicheskii Zhurnal 37:1624-1633.
Bibliography
415
*Murina, V. V. 1961. On the geographic distribution of the abyssal sipunculid Phascolion lutense. Okeanologii (Academii Nauk SSSR) 1:140-142. Murina, V. V. 1964a. Report on the sipunculid worms from the coast of South Chinese Sea. Trudy Instituta Okeanologii Academii Nauk SSSR 69:254-270. Murina, V. V. 1964b. New and rare species of sipunculids of the genus Golfingia. Trudy Instituta Okeanologii Akademii Nauk SSSR 69:216-253. Murina, V. V. 1964c. Sipunculid fauna of the Mediterranean Sea. Trudy Sevastapol Biologicheskoi Statsii 17:51-76. Murina, V. V. 1965. Some data on the structure of pelagosphere sipunculid larvae. Zoologicheskii Zhurnal 44:1610-1619. •Murina, V. V. 1967a. New facts about the distribution of marine sipunculid worms in the Red Sea and the Gulf of Aden. In Some results of Expedition III to the Red Sea Inbuma. Express information, Academy of Sciences Ukrainian SSR, pp. 52-56. Murina, V. V. 1967b. On the sipunculid fauna of the littoral of Cuba. Zoologicheskii Zhurnal 46:35-47. Murina, V. V. 1967c. Report on the sipunculid worms from the sublitoral zone of Cuba and the Gulf of Mexico. Zoologicheskii Zhurnal 54(9): 1329-1339. Murina, V. V. 1968a. On the distribution of new sipunculid fauna from Cuba and the Gulf of Mexico. Revue Roumaine de Biologie, S6rie de Zoologie 13(6)421-423. Murina, V. V. 1968b. New data concerning the occurrence of abyssal sipunculids in the Atlantic Ocean. Zoologicheskii Zhurnal 47(2): 195-199. Murina, V. V. 1968c. New species of Sipuncula from the Red Sea. Zoologicheskii Zhurnal 47:1722-1725. *Murina, V. V. 1969a. Sipunculoidea and Priapuloidea. In Biology of the Pacific Ocean. Moscow: Publisher of Science, 2:84-89. Murina, V. V. 1969b. Two new species of sipunculids (Sipunculida) of the Pacific and Indian oceans. Zoologicheskii Zhurnal 48:1732-1734. *Murina, V. V. 1970. Contributions to the fauna of sipunculid worms from the Aden Gulf. Vestnik Zoologii 2:65-71. Murina, V. V. 1971a. On the species composition and ecology of sipunculids of the Red Sea. In A. O. Kovalevski, ed., Shelf benthos of the Red Sea. Moscow: Akademii Nauk SSSR, pp. 76-88. *Murina, V. V. 1971b. On the occurrence of deep-sea sipunculids and priapulids in the Kurile-Kamchatka Trench. Trudy Instituta Okeanologii Akademii Nauk SSSR 92:41-45. Murina, V. V. 1971c. Geographical distribution of marine worms of the phylum Sipuncula in the world ocean. Zoologicheskii Zhurnal 50:184-192. *Murina, V. V. 197id. International Symposium on the Biology of Sipuncula. 2r Zoologicheskii Zhurnal 50:310-311. *Murina, V. V. 1972. Contribution of the sipunculid fauna of the Southern Hemi~~" sphere. Zoologii Instituta Akademii Nauk SSSR n(i9):294-3i4. Murina, V. V. 1973a. The fauna of sipunculids from the Peruvian-Chilean Trench. Zoologicheskii Zhurnal 5:66-71.
4i6
Bibliography
Murina, V. V. 1973b. New species of Pacific Ocean sipunculids. Zoologicheskii Zhurnal 52:942-945. Murina, V. V. 1974a. Contributions to the knowledge of the fauna of sipunculid worms from the South Atlantic based on data of the Akademik Kurchatov expedition in 1971. Trudy Instituta Okeanologii Akademii Nauk SSSR 98:228-239. Murina, V. V. 1974b. New subspecies of sipunculid worms. Zoologicheskii Zhurnal 53:I7I3-I7I7Murina, V. V. 1974c. New species of the sipunculid genus Phascolion. Zoologicheskii Zhurnal 53:282-285. Murina, V. V. 1975a. The geographical distribution of marine worms of the phylum Sipuncula of the world ocean. In M. E. Mice and M. Todorovid, eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Nau£no Delo Press, pp. 3-18. Murina, V. V. 1975b. New species of genus Phascolosoma (Sipuncula). Vestnik Zoologii i97:54-59Murina, V. V. 1975c. New taxa of the genus Golfingia. Zoologicheskii Zhurnal 54:1085-1089. Murina, V. V. I975d. Ways of evolution and phylogeny of the phylum Sipuncula. Zoologicheskii Zhurnal 54:1747-1758. Murina, V. V. 1976. New and rare species of sipunculids from the East China Sea. Vestnik Zoologii 2:62-67. Murina, V. V. 1977a. Marine worms of the Arctic and boreal waters of Europe. Works on the fauna of the USSR. Leningrad: Akademii Nauk SSSR, 283 pp. Murina, V. V. 1977b. A new species of Sipuncula from the Atlantic Ocean. Galathea Report 14:133-134. Murina, V. V. 1978. On the sipunculid and priapulid fauna of the southern Pacific. Trudy Instituta Okeanologii Akademii Nauk SSSR 113:120-131. Murina, V. V. 1981a. Researches on the coast of Somalia. The shore and the dune of Sar Uanle. 29. A small collection of Sipuncula and Echiura. Monitore Zoologico Italiano I4(2):7-I5. Murina, V. V. 1981b. First report of the sea worms Sipuncula and Echiura from littoral Somali. Vestnik Zoologii 1:11-18. Murina, V. V. 1981c. New species of the genus Phascolion (Sipuncula) from the shells of Scaphopoda. Zoologicheskii Zhurnal 60:348-352. Murina, V. V. 1982. Sipuncula and Echiura from the Mediterranean Sea and Iberian Bay. Trudy Instituta Okeanologii Akademii Nauk SSSR 117:178191. Murina, V. V. 1984. Ecology of Sipuncula. Marine Ecology Progress Series 17:17•Murina, V. V. 1985. Sipunculids of the Chukchi Sea. In P. P. Shirshov, ed., Ecology of the ocean coastal zone benthic fauna and flora. Moscow: Academii Nauk SSSR, pp. 36-46. *Murina, V. V. 1989. The fauna of sipunculids of the coastal waters of southern Vietnam. In A. V. Zhirmunsky and L. T. Phan, eds., Biology of the coastal
Bibliography
417
waters of Vietnam. Benthic invertebrates of southern Vietnam. Vladivostok: Akademii Nauk SSSR, pp. 73-83. *Murina, V. V., and D. Zavodnik. 1979. Cruises of the research vessel Vila Velebita in the Kvarner region of the Adriatic Sea. XVI. Sipuncula. Thalassia Jugoslavia i5(3-4):245-255. Nelson, G., and N. I. Platnick. 1980. A vicariance approach to historical biogeography. Bioscience 3o(5):339-343Newman, W. A. 1991. Origins of Southern Hemisphere endemism, especially among marine Crustacea. Memoirs of the Queensland Museum 31:51-76. *Nickerson, M. L. 1899a. Intracellular canals in the skin of Phascolosoma. Zoologische Jahrbucher, Anatomie 13:191-196. *Nickerson, M. L. 1899b. Intercellular differentiations in gland cells of Phascolosoma gouldii. Science 9:365. Nickerson, M. L. 1900. Sensory and glandular epidermal organs in Phascolosoma gouldii. Journal of Morphology 17:381-398. Nicosia, S. V. 1979a. Urn cells: An experimental model for cervical mucus secretion. Laboratory Investigation 40(2) :27s. Nicosia, S. V. 1979b. Lectin-induced mucus release in the urn cell complex of the marine invertebrate Sipunculus nudus (Linnaeus). Science 206:698-700. Nielsen, C. 1987. Structure and function of metazoan ciliary bands and their phylogenetic significance. Acta Zoology (Stockholm) 68(4):205-262. Nishikawa, T. 1977. Sipuncula. Nature Study 23(4):47~48. Nocek, J. M., D. M. Kurtz, J. T. Sage, Y. M. Xia, P. Debrunner, A. K. Shiemke, J. Sanders-Loehr, and T. M. Loehr. 1988. Nitric oxide adducts of the binuclear iron site of hemerythrin: Spectroscopy and reactivity. Biochemistry 27(3):ioi4-i024. Ocharan, F. J. 1974. Sobre los nefridios de Phascolosoma granulatum (Sipuncula). Separata de la Revista de la Facultad de Ciencias (Oviedo) I5(i):2i~40. *Ocharan, F. J. 1980. Primeros datos sobre los sipunculidos del litoral N. y N.W. de Espana (Santander, Asturias y Galicia). Boletin de Ciencias de la Naturaleza I.D.E.A. 26:111-119. Ochi, O. 1975. An electron microscopic study on the coelomic cells of some Japanese Sipuncula. In M. E. Rice and M. Todorovid, eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Nau£no Delo Press, pp. 219-228. Ochi, 0.1977. X-ray microanalysis on the erythrocytes of sipunculids. Cell Structure and Function 2(1)151-54. O'Connor, B. D. S. 1988. Marine fauna of County Wexford 9—littoral and benthic Echinodermata and Sipunculida. Irish Naturalists' Journal 22(9)^85388. Oersted, A. S. 1844. De regionibis marinis. Hauniae, 88 pp. Oglesby, L. C. 1968. Some osmotic responses of the sipunculid worm Themiste dyscritum. Comparative Biochemistry and Physiology 26:155-177. Oglesby, L. C. 1969. Inorganic components and metabolism; ionic and osmotic regulation: Annelida, Sipuncula, and Echiura. In M. Florkin, ed., Chemical zoology. New York: Academic Press, pp. 211-301.
4i8
Bibliography
Oglesby, L. C. 1982. Salt and water balance in the sipunculan Phascolopsis gouldi, is any animal a "simple osmometer"? Comparative Biochemistry and Physiology 7 ^ : 3 6 3 - 3 6 8 . Ormieres, R. 1979. Selenidium cantoui, new species, a parasitic archigregarine from Physcosoma granulatum (Sipunculoidea). An ultrastructural study. Zeitschrift fiir Parasitenkunde 6 i ( i ) : i 3 - 2 0 . Ostroumov, A. 1909. Sur les gephyriens du nord de la mer du Japan. Ezhegodnik Zoologischeskii Muzei 14:319-321. Packard, A. S. 1866-69. Observations on the glacial phenomena of Labrador and Maine, with a view of the recent invertebrate fauna of Labrador. Memoirs of the Boston Society of Natural History i(2):2io-303. Pallas, P. S. 1774. Lumbricus. In Spicilegia zoologica. Berlin: Lange, pp. 1—15. Parker, J. G. 1980. Effects of pollution upon the benthos of Belfast Slough, Northern Ireland, U.K. Marine Pollution Bulletin n(3):8o-83. Paul, G. 1910. Uber Petalostoma minutum Keferstein und verwandte Arten. Zoologische Jahrbucher, Abteilung fiir Anatomie 29:1-50. Peebles, E, and D. L. Fox. 1933. The structure, functions and general reactions of the marine sipunculid worm Dendrostoma zostericola. Bulletin of the Scripps Institution of Oceanography 3(9):20i-224. Pemberton, S. G., D. R. Kobluk, R. K. Yeo, and M. J. Risk. 1980. Boring Trypanites at the Silurian-Devonian disconformity in southern Ontario, Canada. Journal of Paleontology 54(6): 1258-1266. Perez, C. 1924. Le complexe ethologique de la Turritelle et du Phascolion strombi. Bulletin de la Societe Zoologique de France 49:341-343. Pergament, T. S. 1940. On a new genus Nephasoma from the Arctic Ocean. Results of cruising expedition on icebreaker G. Sedov 1937-1940. Arctic Scientific Institute of Arctic Sea Route. Council of Ministry USSR, pp. 1-3. [Reprinted, 1946, in Trudy ekspedition Sedov Moskva-Leningrad, 3:189I93-] Peters, W. 1850. Uber die Fortpflanzungsorgane des Sipunculus. Archiv fiir Anatomie und Physiologie 1850:382-385. Peyrot-Clausade, M., and J. F. Brunei. 1990. Distribution patterns of macro-boring organisms on Tulear reef flats southwest Madagascar. Marine Ecology Progress Series 6 i ( i - 2 ) : i 3 3 - i 4 4 . Peyrot-Clausade, M., P. Hutchings, and G. Richard. 1992. Temporal variations of macroborers in massive Pontes lobata on Moorea, French Polynesia. Coral Reefs I I ( 3 ) : I 6 I - I 6 6 .
Pickford, G. E. 1947. Echiurida and Sipunculida. Encyclopaedia Britannica 20:717-718. Pilger, J. F. 1982. Ultrastructure of the tentacles of Themiste lageniformis (Sipuncula). Zoomorphology 100:143-156. Pilger, J. F. 1987. Reproductive biology and development of Themiste lageniformis, a parthenogenic sipunculan. Bulletin of Marine Science 4i(i):59-67. Pilger, J. F. 1989. A cytophotometric study of parthenogenesis in Themiste lageniformis (Sipuncula). Bulletin of Marine Science 45(2):4i5-424.
Bibliography
419
Pilger, J. R, and M. E. Rice. 1987. Ultrastructural evidence for the contractile -^ vessel of sipunculans as a possible ultrafiltration site. American Zoologist ~ 27:810a. Pilgrim, M. 1978. The anatomy and histology of the nervous system and secretory -""^ system of the Maldanid polychaetes Clymenella torquata and Euclymene _ oerstedi. Journal of Morphology I55(3):3i 1-325. Pinson, D. Y., and E. E. Ruppert. 1988. The excretory role of metanephridia in — Themiste alutacea (Sipuncula). American Zoologist 28(4):i4ia. Pirie, B. J. S., and S. G. George. 1979. infrastructure of the heart and excretory system of Mytilus edulus. Journal of the Marine Biological Association of the United Kingdom 59(4):8i9-829. Pisera, A. 1987. Boring and nestling organisms from Upper Jurassic coral colonies from northern Poland. Acta Palaeontologica Polonica 32(i-2):83-i04. Poertner, H. 0.1986. Proton balance of anaerobic and post-anaerobic metabolism: Interrelations with pH regulation in marine invertebrates. Zoologische Beitrage 3o(i~3):23i-248. Poertner, H. O. 1987a. Contributions of anaerobic metabolism to pH regulation in animal tissues: Theory. Journal of Experimental Biology 131:69-87. Poertner, H. O. 1987b. Anaerobic metabolism and changes in acid-base status: Quantitative interrelationships and pH regulation in the marine worm Sipunculus nudus. Journal of Experimental Biology 131:89-105. Poertner, H. O., N. A. Anderson, and N. Heisler. 1991. Proton-equivalent ion transfer in Sipunculus nudus as a function of ambient oxygen tension: Relationship with energy metabolism. Journal of Experimental Biology 156:2140. Poertner, H. O., M. K. Grieshaber, and N. Heisler. 1984. Anaerobiosis and acidbase status in marine invertebrates: Effect of environmental hypoxia on extracellular and intracellular pH in Sipunculus nudus. Journal of Comparative Physiology 1556:13-20. Poertner, H. O., N. Heisler, and M. K. Grieshaber. 1984. Anaerobiosis and acidbase status in marine invertebrates: A theoretical analysis of proton generation by anaerobic metabolism. Journal of Comparative Physiology 1556:112.
Poertner, H. O., N. Heisler, and M. K. Grieshaber. 1985. Oxygen consumption and mode of energy production in the intertidal worm Sipunculus nudus: Definition and characterization of the critical Po 2 for an oxyconformer. Respiration Physiology 59:361-377Poertner, H. O., U. Kreutzer, B. Siegmund, N. Heisler, and M. K. Grieshaber. 1984. Metabolic adaptation of the intertidal worm Sipunculus nudus to functional and environmental hypoxia. Marine Biology 79:237-247. Poertner, H. O., S. Vogeler, and M. K. Grieshaber. 1986a. Recovery from anaerobiosis in the intertidal worm Sipunculus nudus. I. Restoration of aerobic, steady-state energy metabolism. Journal of Experimental Biology 122:3750. Poertner, H. O., S. Vogeler, and M. K. Grieshaber. 1986b. Recovery from anaero-
420
Bibliography
biosis in the intertidal worm Sipunculus nudus. II. Gas exchange and changes in the intracellular and extracellular acid-base status. Journal of Experimental Biology 122:51-64. Ponce de Le6n, R., and F. Man6-Garz6n. 1980. Collastoma wahli, new species (Turbellaria, Rhabdocoela), an intestinal symbiont of a South Atlantic Sipun,~ cula. Revista de Biologia del Uruguay 7(2):89~ioo. Popkov, D. V. 1991. New sipunculan genus Cutlerensis gen. n. for the species ""-" Aspidosiphon rutilofuscus (Sipuncula, Golfingiidae). Zoologicheski Zhurnal 70(u):i32-i34. Por, F. D. 1975. Boring species of Aspidosiphon (Sipuncula) on the coasts of Israel. In M. E. Rice and M. Todorovi<5, eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: NauSno Delo Press, pp. 301-304. Pourtates, L. F. de. 1851. On the Gephyrea of the Atlantic coast of the United States. Proceedings of the Fifth Meeting of the American Association for the Advancement of Science, 5:39-42. Prell, W. L., J. V. Gardner, A. W. H. Be, and J. D. Hays. 1976. Equatorial Atlantic and Caribbean foraminiferal assemblages, temperatures, and circulation: Interglacial and glacial comparisons. Geological Society of America Memoirs 145:247-266. Prezant, R. S., B. Gruber, and C. L. Counts. 1981. Predator repellents of benthic macro invertebrates. American Zoologist 21(4): 1022. Quatrefages, M. A. de. 1847a. Etudes sur les types inferieurs de I'embranchement des Annelds. Comptes Rendus Hebdomadaires des Stances de l'Academie des Sciences (Paris) 24(i8):776-779. Quatrefages, M. A. de. 1847b. Etudes sur les types inferieurs de I'embranchement des AnnelSs. M6moire sur l'echiure de Gaertner (Echiurus Gaetnerii NOB.). Annales des Sciences Naturelles, ser. 3 (Paris), 7:307-343. Quatrefages, M. A. de. 1850. Etudes sur les types inferieurs de I'embranchement des Anneles. Annales des Sciences Naturelles, ser. 3, Zoologie (Paris) 14:329-398. Quatrefages, M. A. de. 1865a. Zoologie. Anneles. Note sur la classification des Annelides. Comptes Rendus, Acad6mie des Sciences de Paris 60:586-600. Quatrefages, M. A. de. 1865b. Gephyriens inermes. Histoire Naturelle des Anneles Matins et d'Eau Douce (Paris) 2:599-632. Rabinowitz, P. D., M. F. Coffin, and D. Falvey. 1983. The separation of Madagascar and Africa. Science 220:67-69. Rafinesque-Schmaltz, C. S. 1814. Precis des d6couvertes et travaux somiologiques ou zoologiques et botaniques. Palerme: Royale Tipographie Militaire, 55 pp. Rajulu, S. G. 1975. Asexual reproduction by budding in the Sipuncula. In M. E. Rice and M. Todorovic, eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Naudno Delo Press, pp. 177-182. Rajulu, S. G., and N. Krishnan. 1969. Occurrence of asexual reproduction by budding in Sipunculida. Nature 223:186-187.
Bibliography
421
Rathke, J. 1843. Beitrage zur Fauna Norwegens. Novorun Actorum Academiae Caesarea Leopoldino-Carolinae naturae Curiosorun, Vratislaviae et Bonnae 20(I):I-264.
Reimer, A. A. 1976. Description of a Tetraclita stalactifera panamensis community on a rocky intertidal Pacific shore of Panama. Marine Biology (Berlin) 35(3):225-238. Reissig, M., B. G. Bang, and F. B. Bang. 1983. Mucus secretion in the urn complex of Sipunculus nudus. Cell Biology 2(2):433a. Reunov, A., and M. E. Rice. 1993. Ultrastructural observations on spermatogensis in Phascolion cryptus (Sipuncula). Transactions of the American Microscopical Society H2(3):i95-207. Rice, M. E. 1967. A comparative study of the development of Phascolosoma agassizii, Golfingia pugettensis, and Themiste pyroides with a discussion of developmental patterns in the Sipuncula. Ophelia 4:143-171. Rice, M. E. 1970. Asexual reproduction in a sipunculan worm. Science 167:16181620. Rice, M. E. 1973. Morphology, behavior and histogenesis of the pelagosphera larva of Phascolosoma agassizii (Sipuncula). Smithsonian Contributions to Zoology 132:1-51. Rice, M. E. 1974. Gametogenesis in three species of Sipuncula: Phascolosoma agassizii, Golfingia pugettensis, and Themiste pyroides. La Cellule 70(23):295-3i3. Rice, M. E. 1975a. Observations on the development of six species of Caribbean Sipuncula with a review of development in the phylum. In M. E. Rice and M. Todorovic, eds., Proceedings of the International Symposium on the Biology of Sipuncula and Echiura. Belgrade: NauCno Delo Press, pp. 141-160. Rice, M. E. 1975b. Survey of the Sipuncula of the coral and beach rock communities of the Caribbean Sea. In M. E. Rice and M. Todorovic, eds., Proceedings of the International Symposium on the Biology of Sipuncula and Echiura. Belgrade: Nau£no Delo Press, pp. 35-49. Rice, M. E. 1975c. Sipuncula. In Reproduction of marine invertebrates. Vol. 2. New York: Academic Press, pp. 67-127. *Rice, M. E. 1976a. Larval development and metamorphosis in Sipuncula. American Zoologist 16:563-571. *Rice, M. E. 1976b. Sipunculans associated with coral communities. Micronesica 12:119-132. Rice, M. E. 1978. Morphological and behavioral changes at metamorphosis in the Sipuncula. In Rice and Chia, eds., Settlement and metamorphosis of marine invertebrate larvae. Amsterdam: Elsevier-North Holland Biomedical, pp. 83-102. Rice, M. E. 1980. Sipuncula and Echiura. In R. H. Morris, D. P. Abbott, and E. C. Haderlie, eds., Intertidal invertebrates of California. Stanford: Stanford University Press, pp. 490-498. Rice, M. E. 1981. Larvae adrift: Patterns and problems in life histories of sipunculans. American Zoologist 21 (3)1605-619.
Bibliography
422
Rice, M. E. 1983. Sipuncula. In K. G. Adiyodi and R. G. Adiyodi, eds., Reproductive biology of invertebrates: Oogenesis, oviposition and oosorption. New _ York: John Wiley and Sons, pp. 283-296. Rice, M. E. 1985a. 18. Sipuncula: Developmental evidence for phylogenetic infer—' ence. In S. C. Morris, J. D. George, R. Gibson, and H. M. Piatt, eds., The origins and relationships of lower invertebrates. Oxford: Oxford University Press, pp. 274-296. Rice, M. E. 1985b. Description of a wood dwelling sipunculan, Phascolosoma turnerae, new species. Proceedings of the Biological Society of Washington 98:54-60. Rice, M. E. 1986. Factors influencing larval metamorphosis in Golfingia misakiana (Sipuncula). Bulletin of Marine Science 39(2):362-375. Rice, M. E. 1988a. Sipunculan associates of the deep-sea hydrocarbon seep community. American Zoologist 28(4): 150A. *Rice, M. E. 1988b. Observations on development and metamorphosis of Siphonosoma cumanense with comparative remarks on Sipunculus nudus (Sipuncula, Sipunculidae). Bulletin of Marine Science 42(i):i-i5. Rice, M. E. 1988c. Sipuncula. In K. G. Adiyodi and R. G. Adiyodi, eds., Reproductive biology of invertebrates. Kerala: Oxford and IBH, pp. 263-280. Rice, M. E. 1989. Comparative observations of gametes, fertilization, and maturation in sipunculans. In J. S. Ryland and P. A. Tyler, eds., Reproduction, genetics and distributions of marine invertebrates. Twenty-third European Marine Biology Symposium. Fredensborg: Olsen and Olsen, pp. 167182.
Rice, M. E. 1993a. Sipuncula. In F. W. Harrison and M. E. Rice, eds., Microscopic anatomy of invertebrates. Vol. 12: Onychophora, Chilopoda, and Lesser Protostomata. New York: Wiley-Liss, pp. 238-325. Rice, M. E. 1993b. Two new species of Phascolion (Sipuncula: Phascolionidae) from tropical and subtropical waters of the central western Atlantic. Proceedings of the Biological Society of Washington io6(3):59i-6oi. Rice, M. E., and I. G. Maclntyre. 1972. A preliminary study of sipunculan burrows in rock thin sections. Caribbean Journal of Science i2(i-2):4i-44. Rice, M. E., and I. G. Maclntyre. 1979. Distribution of Sipuncula in the coral reef community, Carrie Bow Cay, Belize. Smithsonian Contributions to Marine Sciences 12:311-320. Rice, M. E., J. Piraino, and H. F. Reichardt. 1983. Observations on the ecology and reproduction of the sipunculan Phascolion cryptus in the Indian River lagoon. Florida Scientist 46(3-4):382-396. *Rice, M. E., and D. S. Putnam. 1972. A comparative study of the functional morphology of some pelagosphera larvae (Sipuncula). American Zoologist 12(4)1723.
*Rice, M. E., and H. F. Reichardt. 1984. Larval development and metamorphosis of Siphonosoma cumanense (Keferstein, 1867). American Zoologist 24:47a. Rice, M. E., and A. C. Stephen. 1970. The type specimens of Sipuncula and Echiura described by J. E. Gray and W. Baird in the collections of the British
Bibliography
423
Museum of Natural History. Bulletin of the British Museum of Natural History 2o(2):49-72. Richardson, D. E., M. Emad, R. C. Reem, and E. I. Soloman. 1987. Allosteric interactions in sipunculid and brachiopod hemerythrin. Biochemistry 26(4):ioo3-ioi3. Richardson, D. E., R. C. Reem, and E. I. Solomon. 1983. Cooperativity in oxygen binding to Lingula reevii hemerythrin: Spectroscopic comparison to the sipunculid hemerythrin coupled bi-nuclear iron active site. Journal of the American Chemical Society i05(26):778o-778i. (Risso, A. 1826. Historie naturelle de l'Europe meiidionale. Paris and Strasbourg, 5:1-403. Robertson, J. D. 1990. Ionic composition of the coelomic fluid of three marine worms, Priapulus caudatus, Sipunculus nudus, and Golfingia vulgaris. Comparative Biochemistry and Physiology 97A(i):87-90. Robitaille, P.-M. L., and D. M. Kurtz. 1988. P 3 1 NMR Probes of sipunculan erythrocytes containing the 0 2 -carrying protein hemerythrin. Biochemistry 27:4458-4465. Romero-Wetzel, M. B. 1987. Sipunculans as inhabitants of very deep narrow burrows in deep-sea sediments. Marine Biology (Berlin) 96(i):87~92. Rondelet, G. 1555. Universae aquatilium historiae pars altera, cum veris ipsorum Imaginibue. Lugduni: M. Bonhome. 242 pp. Ross, J. L. 1982. Feeding habits of the gray tilefish Caulolatilus microps from North and South Carolina. Bulletin of Marine Science 32(2):448-454. Ross, R. M., and W. D. Allman. 1991. Causes of evolution. Chicago: University of Chicago Press, 479 pp. Roule, L. 1896. Gephyriens. Resultats scientifiques de la campagne du Caudan dans le golfe de Gascogne, 1895. Annales de FUniversite de Lyon 26:473474*Roule, L. 1898a. Sur les gephyriens des grands fonds de la mer, recueillies par le Travailleur et le Talisman. Note de M. L. Roule, presentee par M. A. MilneEdwards. Comptes Rendus de l'Acaddmie des Sciences de Paris 127:197199. Roule, L. 1898b. Notice preliminaire sur les especes de gephyriens recueillies dans les explorations sous-marines du Talisman et du Travailleur. Bulletin du Mus6um National d'Histoire Naturelle de Paris 4:384-387. Roule, L. 1906. Annelides et gephyriens. Expeditions scientifiques du Travailleur et du Talisman 8:1-102. Runnegar, B., B. Pojeta, N. J. Morris, J. D. Taylor, M. E. Taylor, and G. McClung. ^ ^ ^ 1975. Biology of the Hyolitha. Lethaia 8(2):i8i-i92. (Ruppert, E. E., and K. J. Carle. 1983. Morphology of metazoan circulatory systems. Zoomorphology 102:193-208. Ruppert, E. E., and M. E. Rice. 1983. Structure, ultrastructure, and function of the terminal organ of a pelagosphera larva (Sipuncula). Zoomorphology 102:143-163. Ruppert, E. E., and M. E. Rice. 1990. Microanatomy and ultrastructure of sub-
424
Bibliography
epidermal coelomic canals in Sipunculus nudus (Sipuncula). American Zool. ..ogist 30:115a. Ruppert, E. E., and P. R. Smith. 1988. The functional organization of filtration ^~ nephridia. Biological Review 63:231-258. *Saiz Salinas, J. I. 1982. Nuevos datos sobre los sipunciilidos de costas espanolas y de mares adyacentes. Actas del Primer Simposio IbeVico de Estudios del Bentos Marino 3:193-201. *Saiz Salinas, J. I. 1983. Aspidosiphon (Paraspidosiphon) major (Vaillant, 1871): A sipunculan not compiled in the literature of the phylum and closely related to Aspidosiphon (Paraspidosiphon) laevis (de Quatrefages, 1865). Kobie (Bilbao) 13:171-173. Saiz Salinas, J. I. 1984a. Los tipos de sipunciilidos de De Quatrefages del Museo de Paris. Bilbao: Servicio Editorial Universidad del Pais Vasco, 258 pp. Saiz Salinas, J. I. 1984b. Gusanos sipunciilidos (Sipuncula) de varias localidades de la costa de Portugal. In V. Monteiro-Marques, ed., Actas do IV Simposio Ib6rico de Estudos do Benthos Marinho. Associa9ao de Estudantes da Faculdade de Ciencias de Lisboa, pp. 177-188. Saiz Salinas, J. I. 1984c. Reconsideraci6n taxondmica de Phascolosoma abyssorum var. punctatum (Hfrubel, 1925) (Sipuncula). Cuadernos Marisqueros, Publicaci6n T6cnica 7:193-197. Saiz Salinas, J. I. I984d. Sipunculus (Phascolosoma) vermiculus de Quatrefages, 1865, and Aedematosomum de Quatrefages, 1865: Validated by the application of the law of priority (Sipuncula). Cuadernos de Investigacidn Biologica (Bilbao) 5:29-32. Saiz, J. I. 1984c El problema del taxon Sipunculus gravieri (HeYubel, 1904a) y la descripcidn de una nueva especie para el g£nero Xenosiphon (Sipuncula, Sipunculidae). Miscellania Zoologica (Barcelona) 8:63-66. Saiz Salinas, J. I. 1986a. The overlooked species of sipunculans commensal of solitary corals (Sipuncula). Bulletin du Mus6um National d'Histoire Naturelle de Paris, ser. 4, sec. A, 8(3):55i-565. Saiz Salinas, J. I. 1986b. Los gusanos sipunciilidos (Sipuncula) de los fondos litorales y circalitorales de las costas de la peninsula Ib6rica, Islas Baleares, Canarias y mares adyacentes. Monograffas Instituto Espanol de Oceanografia (Madrid) 1:1-84. *Saiz Salinas, J. 1.1987. Proposed conservation of four sipunculan specific names. Bulletin of Zoological Nomenclature 44(2):89. *Saiz Salinas, J. I. 1988a. Sipunculid worms from several locations off the southwestern coast of Africa (Sipuncula). Monograffas de Zoologia Marina 3:159176. Saiz Salinas, J. I. 1988b. Sipunculiden (Sipuncula) des ostlichen Nordatlantik, gesammelt wahrend der Fahrten des FS Meteor. Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 85:7-23. Saiz Salinas, J. 1.1989. Die Typen und Typoide des Natur-Museums Senckenberg, 80 Sipuncula. Die von Ruppell and Leuckart 1828 beschriebenen Arten. Senckenbergiana Biologia 689(i-3):207-2i2.
Bibliography
425
Saiz Salinas, J. I. 1993. Sipuncula. In M. A. Ramos et al., eds., Fauna Ib6rica, vol. 4. Madrid: Museo Nacional de Ciencias Naturales CSIC, 200 pp. *Saiz Salinas, J. I., and A. R. Grass. 1980. Sipunculidos litorales de costas Ib6ricas. Primera cita de Golfingia (Nephasoma) rimicola Gibbs, 1973, fuera de su localidad-tipo en el sudoeste de Inglaterra. Boletfn de la Real Sociedad Espanola de Historia Natural, Biol6gica 78:113-120. *Saiz, J. I., and V. V. Murina. 1982. Lista de especies de sipunculidos de las costas ibdricas y de mares adyacentes. Actas del Primer Simposio Iberico de Estudios del Bentos Marino 3:203-212. *Saiz, J. I., A. Rallo, F. Rodriguez, and E. Gutierrez. 1979. Sipuncula y Echiura de la costa Vizcafna. Actas del Primer Simposio Ib6rico de Estudios del Bentos Marino 1:207-221. Saiz Salinas, J. I., and L. Villafranca Urchegui. 1988. Gusanos sipunculidos (Sipuncula) de las zonas adyacentes al estrecho de Gibraltar. Biologfa Ambiental Congreso Mundial Vasco 2:57-63. Saiz Salinas, J. I., and L. Villafranca Urchegui. 1990. The Sipuncula from the Alboran Sea and Ibero-Moroccan Bay. Journal of Natural History 24:11431177. Salvini-Plawen, L. 1973. Toward a clarification of the concept trochophora. Experientia (Basel) 29(n):i434-i436. Sammarco, P. W., and M. J. Risk. 1990. Large-scale patterns in internal bioerosion of Porites: Cross continental shelf trends on the Great Barrier Reef (Australia). Marine Ecology Progress Series 59(i-2):i45-i56. Sammarco, P. W., M. J. Risk, and C. Rose. 1987. Effects of grazing and damselfish territoriality on internal bioerosion of dead corals: Indirect effects. Journal of Experimental Marine Biology and Ecology I2(2):i85-i99. Sanders, H. L. 1968. Marine benthic diversity: A comparative study. American Naturalist i02(925):243-282. Sanders, H. J., and R. R. Hessler. 1969. Ecology of the deep-sea benthos. Science 163:1419-1424. Sars, M. 1851. Beretning om en i Sommeren 1849 foretagen zoologisk Reise i Lofoten og Finmarken. Nytt Magasin for Naturvidenskapene 6:121-125, 190-211.
Sat6, H. 1930. Report on the biological survey of Mutsu Bay. 15. Sipunculoidea. Science Reports, ser. 4, Biology, 5:1-40. Sato, H. 1934a. Report on the Sipunculoidea, Echiuroidea, and Priapuloidea collected by the Soyo-Maru expedition of 1922-1930. Science Reports of the Tohoku University 4:1-32. Sato, H. 1934b. Sipunculoidea and Echiuroidea obtained in Onomichi Bay. Zoological Magazine (Tokyo) 46:245-252. Sat6, H. 1935. Sipunculoidea and Echiuroidea of the West Caroline Islands. Tohoku Daigaku, Sendai, Science Reports, ser. 4, 10:299-329. Sato, H. 1937a. Note on a new sipunculid, Physcosoma kurilense n. sp., found in Shumshir Island. Annotationes Zoologicae Japonenses 16:117-120. Sato, H. 1937b. Echiuroidea, Sipunculoidea, and Priapulaidea obtained in north-
426
east Honshu, Japan. Saito Ho-on Kai Museum, Researc 176. Sato, H. 1939. Studies on the Echiuridea, Sipunculidae, and Pi Science Reports of Tohoku Imperial University I4(4):33 Sawada, N. 1975. An electron microscopic study on the oogei worms. In M. E. Rice and M. Todorovic\ eds., Proceedings al Symposium on the Biology of the Sipuncula and Echiui no Delo Press, pp. 169-176. Schaeper, M. A. 1986. Obliquely striated muscle of Sipunculu of tension development. Journal of Muscle Research ; 7(i)=79Scheltema, A. H. 1993. Aplacophora as progenetic aculiferans origin of mollusks as the sister taxon of Sipuncula. B (Woods Hole) I 8 4 ( I ) : 5 7 - 7 8 . Scheltema, R. S. 1975. The frequency of long-distance larval dis in determinining the rate of gene-flow between widely sepa of sipunculans. In M. E. Rice and M. Todorovic, eds., Pi International Symposium on the Biology of the Sipuncula < grade: Naucno Delo Press, pp. 199-210. Scheltema, R. S. 1986a. Long-distance dispersal by planktonic water benthic invertebrates among central Pacific islands. B Science 39(2):24i-256. Scheltema, R. S. 1986b. Epipelagic meroplankton of tropical sea; biogeography of sublittoral species. In Pelagic biogeogr; Technical Papers in Marine Science. Amsterdam: UNESCO Scheltema, R. S. 1988. Initial evidence for the transport of telej benthic invertebrates across the east Pacific barrier. Biol 174:145-152. Scheltema, R. S. 1989. On the children of benthic invertebrates:". and migrations in time and space. In E. Spanier, Y. Steinberge: eds., Environmental quality and ecosystem stability. Jerusj pp. 93-112. Scheltema, R. S. 1992. Passive dispersal of planktonic larvae and phy of tropical sublittoral invertebrate species. In G. Colom V. U. Ceccherelli, and R. Rossi, eds., Marine eutrophication < dynamics. Fredensborg: Olsen and Olsen, pp. 195-202. Scheltema, R. S., and M. E. Rice. 1990. Occurrence of teleplanic larvae of sipunculans in tropical regions of the Pacific and 1 Bulletin of Marine Science 47(i):i59-i8i. Schleip, W. 1934a. Die Regeneration des Riissels von Phascolion sti (Sipunculidae). Zeitschrift fur Wissenschaftliche Zoologie 145 *Schleip, W. 1934b. Die Regenerationsstrang bei Phascolosoma m (Sipunculidae). Zeitschrift fur Wissenschaftliche Zoologie 146 *Schleip, W. 1935. Die Reparationsvorgange nach Amputation des von Phascolosoma minutum (Kef.) (Sipunculidae). Zeitschrift schaftliche Zoologie 147:59-76.
Bibliography
427
Schmidt, O. 1854. Uber Sipunculoiden (Gephyrea Quatrfgs.). Zeitschrift fur die Gesammten Naturwissenschaften (Leipzig and Stuttgart) 3(1)11-7. Schmidt, 0.1865. Ober den Bau und die systematische Stellung von Aspidosiphon muelleri Diesing (Lesinia farcimen Schmidt). Mitteilungen des Naturwissenschaftlichen Vereines fiir Steiermark 3:56-66. Scott, P. J. B. 1987. Associations between corals and macro-infaunal invertebrates in Jamaica, with a list of Caribbean and Atlantic coral associates. Bulletin of Marine Science 4o(2):27i-286. Sedberry, G. R. 1989. Feeding habits of whitebone porgy, Calanus leucosteus (Teleostei: Sparidae), associated with hard bottom reefs off southeastern USA. U.S. Marine Fisheries Service Fishery Bulletin 87(4):935~944. Sedgwick, A. 1898. Sipunculoidea (Gephyrea, Achaeta). In A student's textbook of zoology. London: Swan Sonnenschein, 1:534-539. Selenka, E. 1875. Eifurchung und Larvenbildung von Phascolosoma elongatum. Zeitschrift fiir Wissenschaftliche Zoologie 25: 442-450. Selenka, E. 1885. Report on the Gephyrea collected by H.M.S. Challenger during 1873-76. Report of scientific results of the Voyage of Challenger, Zoology, i3(36):i-25. Selenka, E. 1888. On the Gephyrea of the Mergui Archipelago collected for the trustees of the Indian Museum. Journal of the Linnean Society of London, ^_ Zoology, 21:220-222.
VSelenka, E. 1897. Die Sipunculiden-Gattung Phymosoma. Zoologischer Anzeiger ..^ 20:460. (Selenka, E., J. G. de Man, and C. Biilow. 1883. Die Sipunculiden, eine systematische Monographic 2, vol. 4. Reisen in Archipel Phillippinen von Dr. C. s~-\ Semper. Wiesbaden, 131 pp. \*Selensky, W. 1907. Uber den Bau und die Entwicklung der sogenannten Urnen der Sipunculiden. Zoologischer Anzeiger 32:329-336. Selensky, W. 1908. Untersuchungen uber die sogenannten Urnen der Sipunculiden. Zeitschrift fiir Wissenschaftliche Zoologie 90:436-595. ^Serrano, T., E. Angulo, A. Mateo, and J. Moya. 1989. The fine structure of the ^ nephridial coelothelium of Phascolosoma granulatum Leukart 1828 (Sipuncula, Phascolosomatidae). Zeitschrift fiir Mikroskopisch-Anatomische For/ -— schung (Leipzig) 103:414-424. \Serrano, M. T., E. Angulo, M. A. Sevillano, and J. Moya. 1990. Three types of thick myofilaments in the nephridial muscle cells of the sipunculan f~~~- Phascolosoma granulatum. Cell Structure and Function i5(2):73-78. \§hipley, A. E. 1890. On Phymosoma varians. Quarterly Journal of Microscopical Science 31:1-27. Shipley, A. E. 1891. On a new species of Phymosoma, with a synopsis of the genus and some account of its geographical distribution. Quarterly Journal of Microscopical Science 32:111-126. Shipley, A. E. 1892a. On a new species of Phymosoma. Proceedings of the Cambridge Philosophical Society 7:77-78. Shipley, A. E. 1892b. On Onchnesoma steenstrupii. Quarterly Journal of Microscopical Science 33(2):233-250.
428
Biblioj
*Shipley, A. E. 1893. Notes on the genus Sipunculus. Proceedings of the Zo cal Society of London 1893:326-333. Shipley, A. E. 1898. Report on the gephyrean worms collected by Mr. J. Si Gardiner at Rotuma and Funafuti. Journal of Zoology 1898:468-473. Shipley, A. E. 1899a. On gephyrean worms from Christmas Island. Proceedir the Zoological Society of London 22:54-57. Shipley, A. E. 1899b. A report on the Sipunculoidea collected by Dr. Willey < Loyalty Islands and in New Britain. In A. Willey, ed., Zoological re based on material from New Britain, New Guinea, Loyalty Islands and where collected 1985-1897 by A. Willey. Cambridge: Cambridge Unive Press, pp. 151-160. •Shipley, A. E. 1899c. A list of the gephyrean worms of Funafuti. Austra Museum, Sydney Memoire 3(8):53i. *Shipley, A. E. 1901a. The abyssal fauna of the Antarctic region. In The Antar manual. London: W. Clowes and Sons, pp. 241-275. \^Sn"ipley, A. E. 1901b. Gephyrea and Phoronis. In S. F. Harmer and A. E. Shipl eds., Cambridge natural history. London: Macmillan, pp. 411-449. Shipley, A. E. 1902. Sipunculoidea, with an account of a new gei Lithacrosiphon. In J. S. Gardiner, ed., Fauna and geography of the Maldi and Laccadive archipelagoes. Cambridge: Cambridge University Pre pp. 131-140. Shipley, A. E. 1903. Report on the Gephyrea collected by Prof. Herdman Ceylon in 1902. Ceylon Pearl Oyster Fisheries Supplementary Repoi 3:169-176. Shorey, H. H. 1976. Animal communication by pheromones. New York: Aw demic Press, 167 pp. Siesser, W. G. 1980. Late Miocene origin of the Benguela upswelling system ol northern Namibia. Science 208:283-285. CSiewing, R. 1976. Problems and new results in the classification of invertebrates In Phylogenetic systematics. Verhandlung der Deutschen Zoologischen Ge sellschaft. Stuttgart: Gustav Fischer, 59-83. Silverman, B. A., R. A. Benninger, R. C. Talamo, and F. B. Bang. 1985. The use ol the urn cell complexes of Sipunculus nudus for the detection of the presence of mucus stimulating substances in the serum of rabbits with mucoid enteritis. Biological Bulletin (Woods Hole) i68(3):46i-470. Silverstein, J. T. 1986. Karyotypes of some Pacific sipunculans. American Zoologist 26:103a. Singhal, R. N. 1988. Distribution of Sipuncula and Echiura in the Gulf of Kahchh, northwest coast of India. Indian Journal of Marine Science I7(2):i70-i7i. *Sluiter, C. P. 1881a. Beitrage zu der Kenntniss der Gephyreen aus dem Malayischen Archipel. Zweite Mittheilung. Natuurkundig Tijdschrift voor Nederlandisch-Indie 41:148-171. JSluiter, C. P. 1881b. Beitrage zu der Kenntnis der Gephyreen aus dem Malay ischen Archipel. Natuurkundig Tijdschrift voor Nederlandisch-Indie 41:84-108.
Bibliography
429
•Sluiter, C. P. 1883. Uber die Segmentalorgane und Geschlechts-driisen einiger Sipunculiden des Malayischen Archipels. Zoologischer Anzeiger 6:523-527. Sluiter, C. P. 1884. Beitrage der Gephyreen aus dem Malayischen Archipel. Natuurkunding Tijdschrift voor Nederlandisch-Indie' 43:26-88. Sluiter, C. P. 1886. Beitrage zu der Kenntnis der Gephyreen aus dem Malayischen Archipel. Natuurkundig Tijdschrift voor Nederlandisch-Indie 45:472-517. Sluiter, C. P. 1891. Die Evertebraten aus der Sammlung des Koniglichen naturwissenschaftlichen Vereins in Nederlandisch-Indien in Batavia. Natuurkundig Tijdschrift voor Nederlandisch-Indie 50:102-123. Sluiter, C. P. 1898. Gephyreen von Siid-Africa. Zoologische Jahrbiicher, Systematik 11:442-450. Sluiter, C. P. 1900. Gephyriens (Sipunculides et Echiurides) provenant des campagnes de YHirondelle et de la Princesse Alice, 1886-1897. R6sultats des Campagnes Scientifique accomplies sur son yacht par Albert I, Prince Souverain de Monaco 15:1-29. Sluiter, C. P. 1902. Die Sipunculiden und Echiuriden der Siboga Expedition, nebst Zusammenstellung der Ueberdies aus den indischen Archipel bekannten Arten. Siboga Expeditie, Monographic 25:1-53. Sluiter, C. P. 1912. G6phyriens (Sipunculides et Echiurides) provenant des campagnes de la Princesse Alice, 1898-1910. R6sultats des Campagnes Scientifique accomplies sur son yacht par Albert I, Prince Souverain de Monaco 36:1-36. Smith, A. G., A. M. Hurley, and J. C. Briden. 1981. Phanerozoic paleocontinental world maps. Cambridge: Cambridge University Press, 102 pp. Smith, P. L., and G. E. Westermann. 1990. Paleobiogeography of the ancient Pacific. Science 249:678-679. Southern, R. 1913. Gephyrea of the coasts of Ireland. Scientific Investigations of the Fisheries Branch, Department of Agriculture for Ireland 3:1-46. *Spengel, J. W. 1898. Der Name Physcosoma. Zoologischer Anzeiger 21:50. *Spengel, J. W. 1907. Eine verkannte Sipunculus Larve. Zoologischer Anzeiger - ^ 3i:97-99Spengel, J. W. 1912. Einige Organisationsverhaltnisse von Sipunculusarten und ihre Bedeutung fur die Systematik dieser Tiere. Deutsche Zoologische Gesellschaft 22:261-272. ^Spengel, J. W. 1913a. Sipunculidea. Handworterbuch der Naturwissenschaften 9:97-106. *Spengel, J. W. 1913b. Zur organisation und systematik der Gattung Sipunculus. Verhandlungen der Deutschen Zoologischen Gesellschaft 23:68-78. Stearley, R. R, and A. A. Ekdale. 1989. Modern marine bioerosion by macroinvertebrates from the northern Gulf of California. Palaios 4:453-467. *Stehle, G. von. 1952. Differenzierungen des Verdauungstraktus von Phascolosoma elongatum. Annales Universitat Saraviensis (Saarbriicken) 1 (4)1309314Stehle, G. von. 1953. Anatomie and Histologic von Phascolosoma elongatum. Annales Universistat Saraviensis (Saarbriicken) 2(3):204-256.
430
Bibliography
*Stehle, G. von. 1954. Die gewebezerstorende Wirkung von Cercarien im Riissel und Gehirn verschiedener Sipunculiden. Zeitschrift fiir Parasitenkunde 16:253-262. *Stephen, A. C. 1929. A sipunculid worm (Physcosoma granulatwri) new to the Scottish fauna. Scottish Naturalist (Edinburgh) 1929:59-60. Stephen, A. C. 1931. A new sipunculid worm (Phascolosoma cluthensis) from the Firth of Clyde. Scottish Naturalist (Edinburgh) 1931:56-61. Stephen, A. C. 1934. The Echiuridae, Sipunculidae, and Priapulidae of Scottish and adjacent waters. Proceedings of the Royal Society of Edinburgh 22:159186. *Stephen, A. C. 1940. On a sipunculid from the Congo coast. Revue de Zoologie et de Botanique Africaines 33:124. Stephen, A. C. 1941a. The Echiuridae, Sipunculidae, and Priapulidae collected by the ships of the Discovery Committee during the years 1926-1937. Discovery Reports 21:235-260. Stephen, A. C. 1941b. Sipunculids and Echiurids of the John Murray Expedition to the Red Sea and Indian Ocean 1933-34. Scientific Reports of the John Murray Expedition 7:401-409. Stephen, A. C. 1942. The South African intertidal zone and its relation to ocean currents. Notes on the intertidal sipunculids of Cape Province and Natal. Annals of the Natal Museum io(2):245-256. Stephen, A. C. 1948. Sipunculids. British, Australian, New Zealand Antarctic Research Expedition Reports, ser. B, 5(4):2i3-220. •Stephen, A. C. 1952. Gephyrea. The Manihine expedition to the Gulf of Aqaba. Bulletin of the British Museum (Natural History) 1:181-182. •Stephen, A. C. 1958. The sipunculids of Haifa Bay and neighborhood. Bulletin of the Research Council of Israel 78(3-4): 129-136. Stephen, A. C. 1960a. Echiuroidea and Sipunculoidea from Senegal, West Africa. Bulletin de lTnstitut Francais d'Afrique Noire 22A(2):5I2~520. •Stephen, A. C. 1960b. British echiurids (Echiuroidea), sipunculids (Sipunculoidea), and priapulids (Priapuloidea). Synopses of British Fauna 12. London: Linnean Society of London, 27 pp. Stephen, A. C. 1964. A revision of the classification of the phylum Sipuncula. Annals and Magazine of Natural History, ser. 13, 7:457-462. Stephen, A. C. 1965. Echiura and Sipuncula from the Israel south Red Sea Expedition. Sea Fisheries Research Station Haifa Bulletin 40:79-83. •Stephen, A. C. 1966. A collection of Sipuncula taken on the summit of the Vema sea-mount, South Atlantic Ocean. Annals and Magazine of Natural History, ser. 13, 9:145-148. •Stephen, A. C. 1967. Notes on a collection of sipunculids from Peru. Acta Zoologica Lilloana (Tucuman) 21:91-94. Stephen, A. C, and E. B. Cutler. 1969. On a collection of Sipuncula, Echiura, and Priapulida from South African waters. Transactions of the Royal Society of ^-^_ South Africa 38(2): 111 -121. Stephen, A. C, and S. J. Edmonds. 1972. The phyla Sipuncula and Echiura. — London: Trustees of the British Museum (Natural History), 528 pp.
Bibliography
431
Stephen, A. C, and J. D. Robertson. 1952. A preliminary report on the Echiuridae and Sipunculidae of Zanzibar. Proceedings of the Royal Society of Edinburgh 64(4)426-444. Stimpson, W. 1855. Description of some new marine invertebrates from the Chinese and Japanese seas. Gephyrea. Proceedings of the Academy of Natural Sciences of Philadelphia 7:390-391. Storch, V., and K. Moritz. 1970. The regeneration of the integument by cells in the ventral nerve cord of Phascolion strombi (Montagu) (Sipunculida). Zeitschrift fur Zellforschung und Mikroskopische Anatomie, Histochemie no(2):258-267. Storch, V., and U. Welsch. 1972. Zur Ultrastruktur der Metanephridien des landlebenden Sipunculiden Phascolosoma (Physcosoma) lurco. Kieler MeeresForschungen 28(2)1227-231. Strathmann, R. R. 1978. The evolution and loss of feeding larval stages of marine invertebrates. Evolution 32(4):894~9o6. Taniuchi, T., N. Kuroda, and Y. Nose. 1983. Age, growth, reproduction and food habits of the star-spotted dogfish Mustelus manazo collected from Choshi [Japan]. Bulletin of the Japanese Society of Fisheries Science 49(9)113251334Tarifeno, E. S. 1975. Burrowing pattern and its variation with different kinds of substratum in the Chilean sipunculan Themiste hennahi Gray 1828 (syn. Dendrostomum peruvianum Collin 1892). In M. E. Rice and M. Todorovic, eds., Proceedings of the International Symposium on the Biology of Sipuncula and Echiura. Belgrade: Nau5no Delo Press, pp. 251-266. Tarifeno, E. S. 1976. Resistance to environmental stress of temperature and salinity in the Chilean sipunculan Themiste hennahi Gray 1828 (syn. Dendrostomum peruvianum Collin 1892). In M. E. Rice and M. Todorovid, eds., Proceedings of the International Symposium on the Biology of Sipuncula and Echiura. Belgrade: NauCno Delo Press, pp. 29-38. Tarifeno, E. S., and M. Rojas. 1978. El phylum Sipuncula en Chile. Studies on Neotropical Fauna and Environment 13:93-134. Tarifeno, E. S., and J. Tomicic. 1973. Primer registro en el Pacifico sur oriental para Xenosiphon mundanum (Selenka, de Man and Biilow, 1883) (Sipuncula, Sipunculidae). Revista de Biologia Marina i5(i):i07-no. Taylor, J. D. 1983. The food of coral-reef Drupa Gastropoda. Zoological Journal of the Linnean Society 78(4):299~3i6. Taylor, M. E. 1977. Late Cambrian of western North America: Trilobite biofacies, environmental significance, and biostratigraphic implications. In E. G. Kauffman and J. E. Hazel, eds., Concepts and methods of biostratigraphy. Stroudsburg, Pa.: Dowden, Hutchinson, and Ross, pp. 397-425. Terwilliger, N. B., R. D. Terwilliger, and E. Schabtach. 1985. Intercellular respiratory proteins of Sipuncula, Echiura, and Annelida. In W. D. Cohen, ed., MBL lectures in biology: Blood cells of marine invertebrates. New York: Liss, pp. 193-226. T6try, A. 1959. Classe des sipunculiens. In P. P. Grasse\ ed., Trait6 de zoologie. Anatomie, Systematique, Biologic Paris: Masson et Cie., Editeurs.
432
Bibliography
Teuscher, R. 1874. Notiz iiber Sipunculus und Phascolosoma. Jenaische Zeitschrift fur Naturwissenschaft 8:488-499. Tbiel, H. 1875a. Le Phascolion {Phascolosoma) strombi (Mont.). Bihang Till Kungliga Svenska Vetenskaps-Akademiens Handlingar 3(3): 1-7. Theel, H. 1875b. Etudes sur les gephyriens inermes des mers de la Scandinavie, du Spitzberg et du GroSnland. Bihang Till Kungliga Svenska VetenskapsAkademiens Handlingar 3(6): 1-30. Theel, H. 1905. Northern and Arctic invertebrates in the collection of the Swedish State Museum. I. Sipunculids. Kungliga Svenska Vetenskaps-Akademiens Handlingar 39(i):i-i30. Theel, H. 1911. Priapulids and sipunculids dredged by the Swedish Antarctic expedition 1901-1903 and the phenomenon of bipolarity. Kungliga Svenska Vetenskaps-Akademiens Handlingar 47(i):3-36. Theodorides, J. 1975. Identity de Lithocystis parguerae I. Jones 1971. Gregarine parasite de Sipunculidae, avec Filipodium ozakii Hukui 1930. Annales de Parasitologic Humaine et Compared 5o(i):i4i. Thiem, N. V, G. Lacombe, and N. V. Thoal. 1975. Comparative study of two ATP:L-arginine phosphotransferases of molecular weight 84,000. Biochimica et Biophysica Acta 377(i):95-i02. Thomas, P. 1972. Osmotic responses and neurosecretion in Siphonosoma cumanense (Sipunculida). Zoological Magazine, Zoological Society of Japan 8i(4):355Thompson, B. E. 1980a. Sipuncula and Echiura. AHF Technical Report. Southern California Marine Invertebrates 3:257-262. Thompson, B. E. 1980b. A new bathyal sipunculan from southern California, with ecological notes. Deep-Sea Research 27A:95i-957. Thompson, W. 1840. Contributions towards a knowledge of Mollusca Nudibranchia and Mollusca Tunicata of Ireland, with descriptions of some apparently new species of Invertebrata. Annals of Natural History or Magazine of Zoology, Botany and Geology (London) 5:84-102. Thoncoso, J. S., and V. Urgurri. 1992. The association between Tellimya phascolionis (Dautzenberg et Fischer, 1925) (Bivalvia, Montacutidae) and the sipunculan Phascolion strombi (Montagu, 1804) in the Ria of Ares and Betanzos (Galicia, northwest Spain). Boletfn de la Real Sociedad Espanola de Historia Natural, Biol6gica 88:189-194. Thorson, G. 1957. Parasitism in the sipunculid Golfingia procerum (Mobius). Journal of the Faculty of Science of Hokkaido University, ser. 4, Zoology, 13:128-132. Towle, A. 1975. Cell types in the coelomic fluid of Phascolosoma agassizii. In M. E. Rice and M. Todorovid, eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Naudno Delo .—^_ Press, pp. 211-218. ^Towle, A., and A. C. Giese. 1966. Biological changes during reproduction and starvation in the sipunculid worm, Phascolosoma agassizii. Comparative Biochemistry and Physiology 19:667-680.
Bibliography
433
*Towle, A., and A. C. Giese. 1967. The annual reproductive cycle of the sipunculid Phascolosoma agassizii. Physiological Zoology 40:229-237. Triplett, E. L., J. E. Cushing, and G. L. Durall. 1958. Observations on some immune reactions of the sipunculid worm Dendrostomum zostericolum. American Naturalist 92(866):287-293. Tsuchiya, M., Y. Nakasone, and M. Nishihira. 1986. Community structure of coral associated invertebrates of the hermatypic coral, Pavona frondifera, in the Gulf of Thailand. Galaxea 5:129-140. Uchida, T., H. Yano, K. Satake, I. Kubota, and A. Tsugita. 1990. The amino acid sequence of hemerythrin from Siphonosoma cumanense. Protein Sequences and Data Analysis 3(2): 141-148. Uexkiill, J. von. 1896. Zur Muskel und Nervenphysiologie von Sipunculus nudus. Zeitschrift fur Biologie, ser. 9, I5(2):i. Uexkiill, J. von. 1903. Die biologische Bauplan von Sipunculus nudus. Zeitschrift fur Biologie 44:269-344. Utecht, R. E., and D. M. Kurtz. 1988. Cytochrome b5 and NADH-cytochrome-b5 reductase from sipunculan erythrocytes: A methemerythrin reduction system from Phascolopsis gouldii. Biochimica et Biophysica Acta 953:164-178. Vail, P. R., R. M. Mitchum, Jr., and S. Thompson. 1978. Seismic stratigraphy and global changes of sea level. Part 4: Global cycles of relative changes of sea level. In E. Payton, Seismic stratigraphy: Applications to hydrocarbon exploration. American Association of Petroleum Geology Memoirs 26:83-97. *Vaillant, L. 1871. Note sur quelques g6phyriens de Saint-Vincent du Cap-Vert. In L. de Folin and L. P6rier, dirs., Les fonds de la mer. Etude internationale sur les particularitds nouvelles des regions sous-marines. Paris: Savy, 1:268-276. Vaillant, L. 1875. G6phyriens. In L. de Folin and L. P6rier, dirs., Les fonds, vol. 2. Paris: Savy, sec. 4. Valembois, P., and D. Boiledieu. 1980. Fine structure and functions of hemerythrocytes and leucocytes of Sipunculus nudus. Journal of Morphology I63(I):69-78.
Valembois, P., D. Boiledieu, and P. Roch. 1978. Membrane modifications induced by histocompatibility antigens and mitogens in some invertebrate leukocytes. Bulletin de la Soci6te" Zoologique de France i03(3):30i-3o8. Valembois, P., P. Roch, and D. Boiledieu. 1977. Specificity and anamnesty in invertebrates. American Zoologist 17:892. Valembois, P., P. Roch, and D. Boiledieu. 1980. Natural and induced cytotoxicities in sipunculids and annelids. In M. J. Manning, ed., Developments in immunology, phylogeny of immunological memory. Amsterdam: Elsevier-North Holland Biomedical, pp. 47-56. Valenciennes, A. 1854. Remarques sur le m6moire de M. Eugene Robert. Comptes Rendus Hebdomadaires des Stances de l'Acad6mie des Sciences (Paris) 39:640-643. ^lentine, J. W. 1973. Coelomate superphyla. Systematic Zoology 22(2):97-i02. Valentine, J. W. 1984. Neogene marine climate trends: Implications for biogeography and evolution of the shallow-sea biota. Geology 12:647-650.
Bibliography
434
Vassilopoulou, V., and C. Papaconstantinou. 1993. Feeding habits of red mullet (Mullus barbatus) in a gulf in western Greece. Fisheries Research (Amsterdam)
I6(I):69-83.
Vermeij, G. J. 1987. Evolution and escalation. Princeton: Princeton University Press, 527 pp. Vermeij, G. J. 1989. Geographical restriction as a guide to the causes of extinction: The case of the cold northern oceans during the Neogene. Paleobiology 15:335-356. Vermeij, G. J. 1991a. When biotas meet: Understanding biotic interchange. Science 253:1099-1103. Vermeij, G. J. 1991b. Anatomy of an invasion: The trans-Arctic interchange. Paleobiology 17:281-307. Verrill, A. E. 1873a. Results of recent dredging expedition on the coast of New England. American Journal of Science and Arts 3(5):98-io6. * Verrill, A. E. 1873b. Reports on animals from Vineyard Sound and adjacent waters. Report of the U.S. Commission of Fish and Fisheries 1:295-778. * Verrill, A. E. 1874. Brief contributions to zoology. Museum of Yale College, no. 28. Results of recent dredging expeditions on the coast of New England, no. 6. American Journal of Science and Arts, ser. 3 (New Haven) 7(4o):405~4i4. * Verrill, A. E. 1879. Recent additions to the marine invertebrates of north eastern America. Proceedings of the U.S. National Museum 2:163-205. * Verrill, A. E. 1900. Additions to the Turbellaria, Nematoda and Annelida of Bermuda, with revision of some New England genera and species. Transactions of the Connecticut Academy of Arts and Sciences 10:595-671. * Verrill, A. E. 1904. Additions to the fauna of the Bermudas from the Yale Expedition of 1901. Transactions of the Connecticut Academy of Arts and Sciences 11 (2): 15-62. Vogt, C. 1876. Sur le loxosome des phascolosomes. Archives de Zoologie Experimental et Gen6rale 5:304-356. Voss-Foucart, M. R, S. Barzin, C. Jeuniaux, and J. C. Bussers. 1977a. Etude compared de la composition chimique des regions souples et durcies de la cuticule de quatre especes de sipunculiens. Cahiers de Biologie Marine 18:135-145. Voss-Foucart, M. R, S. Barzin, and C. L. Toussaint. 1977b. Etude comparee de la composition en acides amin6s d'extraits peptidiques de la cuticule de siponculiens et d'annelides polychetes. Archives de Zoologie Exp6rimentale et Generale 118:457-470. Walter, M. D. 1973. Fressverhalten und Darminhaltsuntersuchungen bei Sipunculiden. Helgolander Wissenschaftliche Meeresuntersuchungen 25:486-494. Ward, H. B. 1891. On some points in the anatomy and histology of Sipunculus nudus, L. Bulletin of the Museum of Comparative Zoology of Harvard University 21:143-182. Weerdt, W. H. de. 1989. Phylogeny and vicariance biogeography of North Atlantic Chalinidae (Haplosclerida, Demospongiae). Beaufortia 39:55-86. Wegener, F. 1938. Beitrag zur Kenntnis der Riisselregeneration der Sipunculiden. Zeitschrift fur Wissenschaftliche Zoologie 150.
Bibliography
435
Weijermars, R. 1989. Global tectonics since the breakup of Pangea 180 million years ago: Evolution maps and lithospheric budget. Earth Science Review 26:113-162. Weinheimer, P. F. 1970. Immunophylogeny. A review of immune-like mechanisms of invertebrate species. Alabama Journal of Medical Sciences 7(4):451-460. Wells, R. M. G. 1982. Respiratory characteristics of the blood pigment of 3 worms from an intertidal mudflat. New Zealand Journal of Zoology 9(2):243-248. Wesenberg-Lund, E. 1925. Gephyreer. Conspectus Faunae Groenlandicae Bianco Lunos Bogtrykkeri (Copenhagen) 23:81-91. * Wesenberg-Lund, E. 1928. Gephyrea and Sternapsidae. Zoology of the Faroes (Copenhagen) i928(2o):i-5. ^Wjssenberg-Lund, E. 1929. Some anatomical features subject to variation in Phascolion strombi. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening i Kj0benhaven 88:155-164. Wesenberg-Lund, E. 1930. Priapulidae and Sipunculidae. The Danish /ngo//Expedition 4(7): 1-44. *Wesenberg-Lund, E. 1932. The Godthaab Expedition 1928. Gephyrea. Meddelelser om Gr0nland 79(3): 1-18. *Wesenberg-Lund, E. 1933. The collection of gephyreans in the Royal Museum of Natural History, Belgium. Bulletin du Musee Royal d'Histoire Naturelle de Belgique 9(6): 1-16. *Wesenberg-Lund, E. 1934. Gephyreans and Annelids. The Scoresby Sound Committee's Second East Greenland Expedition in 1932 to King Christian 9th's Land. Meddelelser om Gr0nland I 0 4 ( I 4 ) : I - 3 8 . Wesenberg-Lund, E. 1937a. Gephyrea. Bulletin du Mus6e Royal d'Histoire Naturelle de Belgique i3(36):i-23. Wesenberg-Lund, E. 1937b. The zoology of east Greenland gephyreans. Meddelelser om Gr0nland I2i(i):i~25. *Wesenberg-Lund, E. 1937c. Gephyrea. Zoology of Iceland 2 ( 2 3 ) : I - I 6 . *Wesenberg-Lund, E. 1938. Norwegian Gephyrea from the collections of the Zoological Museum of Trondheim. Kongelige Norske Videnskabers Selskabs Forhandlinger I I ( 7 ) : 2 6 - 2 9 .
Wesenberg-Lund, E. 1939a. Gephyreans from Swedish waters in the Museum of Natural History of Gothenburg. GQteborgs Kungliga Vetenskaps VitterhetsSamhalles Handlingar 6(6):3~35. * Wesenberg-Lund, E. 1939b. Polychetes et gephyriens de Tunisie. Station Oceanographique de Salammbo Bulletin 39:3-20. *Wesenberg-Lund, E. 1939c. P0lseorme (Gephyrea). Sipunculider. Priapulider. Echiurider. In Danmarks fauna, vol. 45. Copenhagen, 60 pp. Wesenberg-Lund, E. 1954a. Sipunculids and echiurids collected by Mr. G. Ranson in Oceania in 1952. Bulletin du Museum National d'Histoire Naturelle de Paris 26:376-384. Wesenberg-Lund, E. 1954b. Priapuloidea, Sipunculoidea and Echiuroidea. Bulletin, Institut Royal des Sciences Naturelles de Belgique 3o(i6):i-i8. Wesenberg-Lund, E. 1955a. Reports of Lund University Chile Expedition, 194849. 19. Gephyrea from Chile. Lunds Universitets Arsskrift 5i(io):i-23.
436
Bibliography
Wesenberg-Lund, E. 1955b. Sipunculidae. Reports of the Swedish deep-sea expedition. Zoology 2(i5):i99-20i. Wesenberg-Lund, E. 1957a. Sipunculoidea and Echiuroidea from West Africa together with a bibliography on Gephyrea after 1920. Bulletin, Institut Royal des Sciences Naturelles de Belgique 33(42): 1-24. Wesenberg-Lund, E. 1957b. Sipunculoidea from the coast of Israel. Bulletin of the Research Council of Israel 6B(3~4): 193-200. *Wesenberg-Lund, E. 1957c. Sipunculoidea and Echiuroidea from the Red Sea. Contributions to the Knowledge of the Red Sea, no. 3. Sea Fisheries Research Station Haifa Bulletin 14:1-15. Wesenberg-Lund, E. 1959a. Sipunculoidea and Echiuroidea from Tropical West Africa. Atlantide Report 5:177-210. Wesenberg-Lund, E. 1959b. Campagne de la Calypso: Golfe de Guin6e. 7. Sipunculoidea and Echiuroidea. R6sultats Scientifiques des Campagnes de la Calypso 4:207-217. Wesenberg-Lund, E. 1959c. Sipunculoidea and Echiuroidea from Mauritius. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening i K0benhavn 121:53-73. Wesenberg-Lund, E. 1963. South African sipunculids and echiuroids from coastal waters. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening i K0benhavn 125:101-146. Westervelt, C. A. 1981. Collastoma kozloffi, new species of neorhabdocoel turbellarian from the intestine of the sipunculan Themiste dyscrita. Journal of Parasitology 67(4):574~577. Westinga, E., and P. C. Hoetjes. 1981. The intrasponge fauna of Spheciospongia desparia (Porifera, Demospongiae) at Curacao and Bonaire, Netherlands Antilles (West Indies). Marine Biology (Berlin) 62(2-3): 139-150. Wetzel, A., and F. Werner. 1981. Morphology and ecological significance of Zoophycos in deep-sea sediments off northwest Africa. Palaeogeography Palaeoclimatology Palaeoecology 32(3-4): 185-212. White, K. N., and G. Walker. 1981. The barnacle excretory organ. Journal of the Marine Biological Association of the United Kingdom 6i(2):529~547. White, M. J. D. 1973. Animal cytology and evolution. London: Cambridge University Press, 933 pp. Wilheim, M. L., and F. X. Wilheim. 1978. Subunit structure of erythroid cells chromatin. Studia Biophysica 67:105-106. Williams, J. A. 1972. Development of a rock burrowing sipunculid inhabiting stony coral. American Zoologist I2(4):723. Williams, J. A. 1977. Functional development in four species of the Sipuncula. Ph.D. dissertation, University of Hawaii, 218 pp. Williams, J. A., and S. V. Margolis. 1974. Sipunculid burrows in coral reefs: Evidence for chemical and mechanical excavation. Pacific Science 28(4): 357-359Willmer, P. 1990. Invertebrate relationships: Patterns in animal evolution. Cambridge: Cambridge University Press, 362 pp.
Bibliography
437
Woodruff, E, S. M. Savin, and R. G. Douglas. 1981. Miocene stable isotope record: A detailed deep Pacific Ocean study and its paleoclimatic implications. Science 212:665-668. Yokoi, I., H. Kaboto, Y. Kawakami, A. Mori, and Y. Robin. 1989. Effects of phascoline and phascolosomine on the rat electroencephalograms. Neurosciences i5(4):351-358. Yonge, C. M. 1975. A note on mutualism between sipunculans and scleractinian corals. In M. E. Rice and M. Todorovid, eds., Proceedings of the International Symposium on the Biology of Sipuncula and Echiura. Belgrade: NauCno Delo Press, pp. 305-312. *Zavodnik, D. 1975. Contribution to the ecology and zoogeography of north Adriatic sipunculans. In M. E. Rice and M. Todorovic\ eds., Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura. Belgrade: Nau£no Delo Press, pp. 93-102. *Zavodnik, D., and V. G. Murina. 1975. Contribution to Sipuncula of north Adriatic insular region. Rapports et proces-verbaux des Reunions, Commission Internationale pour 1'Exploration Scientifique de la Mer M6diterran6e 23(2):i27-i28. Zavodnik, D., and V. G. Murina. 1976. Sipuncula of the region of Rovinj (north Adriatic Sea). Biosistematika 2(i):79-89. Zinsmeister, W. J., and R. M. Feldmann. 1984. Cenozoic high latitude heterochroneity of Southern Hemisphere marine faunas. Science 224:281-283. Zukerkandl, E. 1950. Coelomic pressures in Sipunculus nudus. Biological Bulletin (Woods Hole) 98:161-173.
Taxonomic Index
Currently valid genus and species group names are in roman type. Names not currently considered valid senior synonyms, or archaic spellings of current names, are in italics. Subgenera are in parentheses, and names of suprageneric taxa are in capital letters. Descriptions of currently valid taxa begin on the pages listed; when more than one page number is given, the description begins on the page number in boldface type. abnorme, Phascolion, 114, 126 abnormel-is, PhascolosomalGolfingia, 198 absconditus, Xenosiphon, 43 abyssorum: Nephasoma, Phascolosoma, Golfingia, 78, 83, 89, 96 abyssorum: Physcosoma, Phascolosoma, Apionsoma, 168 adelaidensis, Golfingia margaritacea, 71 adenticulatum: Physcosoma scolops, Phascolosoma scolops, 184 adriatica, Golfingia, 76 (Aedematosomum), Sipunculus, 188 aeneus, Sipunculus, 50 aequabilis, Sipunculus, 36 africanum, Phascolion, 130 agassizii: Phascolosoma, Phymosoma, Physcosoma, 163, 173 (Akrikos), Aspidosiphon, 201, 205, 211 alberti, Phascolion, 130 albidum, Phascolosoma, 71 albolineatum: Phascolosoma, Phymosoma, Physcosoma, 163, 174, 184 albus, Aspidosiphon, 211, 215 alticonus, Lithacrosiphon, 229 alutacea/-wm, Themiste/Dendrostomum, 145, 148, 149, 151 amamiensisl-e, Sipunculus I Siphonosoma, 53 ambiguum, Phascolosoma, 385 ambonense: Phascolosoma, Physcosoma, 176 ambonensis, Aspidosiphon, 227 ambonensis: Aspidosiphon steenstrupii, Paraspidosiphon steenstrupii, 227 anceps, Phascolosoma, 93, 97 andamanensis, Phascolosoma, 174 anderssoni: Golfingia, Phascolosoma, 63, 64, 65,68
angasii, Sipunculus, 39 anguineuml-a, Phascolosomal Golfingia, 381 angulatus, Aspidosiphon, 223 annulatum, Phascolosoma, 175 anomalus, Phascolion, 131 antarctical-um, Golfingia margaritacea/Phascolosoma margaritacea, 72 antarcticum, Phascolosoma, 72 antillarum: Antillesoma, Phymosoma, Physcosoma, Phascolosoma, 157, 159, 186 Antillesoma, 186; antillarum, 157, 159, 186 (Antillesoma), Phascolosoma, 159, 186 Apionsoma, 157, 159, 167, 189, 194; abyssorum, 168; capitata, 168; immunitum, 190, 382; misakianum/-«, 195; murinae bilobatae, 196; murinae murinae, 195; papilliferum, 193, 383; pectinatum, 157, 197; reconditum, 193; trichocephalus, 196 (Apionsoma), Golfingia, 189 appendiculatal -urn, Golfingia/Phascolosoma, 74 approximatuml-a, Phascolosomal Golfingia, 381 arcassonense/-ii, Siphonosoma/Sip«nc«/«i, 45. 48, 49 arcuatum/-M.s, Phascolosoma/Si/Juncw/Mi, 163, 167, 176 armatum, Aspidosiphon, 218 artificiosusl-um, Phascolion, 130 aspergillus/-«/n: Cloeosiphon, Loxosiphon/Echinosiphon, 232 asperum: Phascolosoma, Phymosoma, 182 Aspidosiphon, 200; albus, 211, 215; ambonensis, 227; angulatus, 223; armatum, 218; brasiliensis, 223; brocki, 214; carolinus, 214; clavatus, 218; corallicola, 218; coyi, 221, 386; cristatus, 229; cumingii, 222; cy-
440 Aspidosiphon (cont.y. lindricus, 381; elegans, 205, 214, 226; elegans elegans, 214; elegans yapensel-is, 214; eremital-us, 218, 386; exhaustuml-us, 218; exhaustus mirus, 219; exiguus, 215; exilis, 214; exostomuml-us, 226; fischeri, 222; fischeri cubanus, 222; formosanus, 227; fitscus, 225; gerouldi, 217; gigas, 223; gosnoldi, 215; gracilis gracilis, 216; gracilis schnehageni, 216; grandis, 223; grandis obliquoscutatus, 223; hartmeyeri, 211, 217; havelockensis, 227; heteropsammiarum, 218; hispitrofus, 219; homomyariuml-us, 214; imbellis, 218; mquilinus, 218; insularis, 182; jukesii, 206, 218; klunzingeri, 223; kovaleskii, 219; laevis/-e, 205, 221, 222, 386; /evi's, 227; longirhyncus, 212; macer, 382; major, 223; makoensis, 225; mexicanus, 203, 205, 212; michelini, 218; mirabilis, 218; misakiensis, 217, 222; mokyevskii, 188; muelleri, 205, 218, 220, 231; ochrus, 226; pachydermatus, 223; parvulus, 215, 224; pygmaeus, 218; planoscutatus, 225; <7«<»refagesi, 223; ravus, 214; rhyssapsis, 386; rutilofuscus, 87; semperi, 225; speciosus, 223; speculator, 217, 225; spinalis, 214, 215; spinososcutatus, 224; spinosus, 214; spiralis, 220; steenstrupii, 225, 227; steenstrupii fasciatus, 225; tenuis, 226; thomassini, 205, 212; ?ortui, 219; trinidensis, 226; truncatus, 221; uniscutatus, 229; venabulum/-Hs, 212; zinni, 203, 213 ASPIDOSIPHONIDAE, 199 ASPIDOSIPHONIFORMES, 199 aspidosiphonoides, Phascolosoma, 87 osser: Phymosoma, Physcosoma, Phascolosoma, 188 astuta: Phascolosoma vulgare, Golfingia vulgaris, 75 australe, Siphonosoma, 45, 50 australel-is, Phascolosoma!Sipunculus, 50 australel-is, Golfingia eremitalPhascolosoma eremita, 94, 99 (Austrosiphon): Sipunculus, Xenosiphon, 31, 40 balanophorus, Sipunculus, yj barentsii, Stephanostoma, 71 beklemischevi, Phascolion, 117 benhami: Nephasoma abyssorum, Phascolosoma, Golfingia, 90 bernnhardus, Sipunculus, 130 billitonensel-is, SiphonosomalSipunculus, 52 bilobatae: Apionsoma murinae, Golfingia murinae, 196
Taxonomic Index birsteini, Golfingia, 62, 64, 65, 69 blanda/-«m, Themiste/Dendrostomunj, 149, 151 bogorovi, Phascolion, 114, 127 boholense/-w, Siphonosoma/Sip«ncM/«i, 45, 50 bonhourei: Sipunculus, Siphonosoma, 381 borealel-is, Phascolosoma!Sipunculus, 94 botulusl-um, Phascolion, 381 branchiatus, Xenosiphon, 30, 35, 41, 44 brasiliensis: Aspidosiphon, Paraspidosiphon, 223 brocki, Aspidosiphon, 214 brotzkajae, Phascolion, 131 bulbosum, Nephasoma, 81, 90 bulbosuml-a, Phascolosoma!Golfingia, 90 caementarius, Sipunculus, 130 californica, Golfingia eremita, 94 californiensis, Golfingia margaritacea, 71 cantabriensis, Golfingia, 72 canum, Phascolion, 124 capensis/-e, Golfingia/Z'fta.sco/o.soma, 69 capilleforme/-i.s, Nephasoma/Go//inji'a, 69, 90,97 capitata: Fisherana, Golfingia, Apionsoma, 168 capitatum: Phascolosoma, Physcosoma, 168 capitatus, Sipunculus, 130 capsiforme, Phascolosoma, 71 caribaeum, Xenosiphon, 44 carneum, Phascolosoma, 184, 385 carolinense, Siphonosoma, 52 carolinum, Cloeosiphon, 232 carolinus, Aspidosiphon, 214 catharinae: Thysanocardia, Phascolosoma, Golfingia, 103, 105, 106 caupo, Phascolion, 114, 122, 127 Centrosiphon, 61; herdmani, 76 Chamissoi, Diesingia, 381 charcoti: Phascolosoma, Golfingia, 70 cAuni: Phascolosoma, Golfingia, Nephasoma, 38l cinctal-um, Golfingia!Phascolosoma, 93 cinereal-um, Golfingia!Phascolosoma, 99 cirratum/-«i, Phascolion, 114, 132 clavatusl-um, Aspidosiphon! Pseudaspidosiphon, 218 clavatus, Sipunculus, 385 claviger, Sipunculus, 52 Cloeosiphon, 230; aspergillus/-«m, 232; carolinum, 232; japonicum, 232; javanicum, 232; mollis, 232 cluthensis, Phascolosoma, 70 cochlearium, Phascolosoma, 385 cochlearius, Sipunculus, 218 collare, Phascolion, 114, 121
Taxonomic Index commune, Phascolosoma, 75 communis, Sipunculus, 75 concharum, Sipunculus, 130 confusum, Nephasoma, 78, 91 confusuml-a, Phascolosoma/Golfingia, 91 constellatum, Phascolosoma, 385 constricticervix, Nephasoma, 78, 81, 84, 91, 93. 101 constrictum, Nephasoma, 83, 84, 91, 92 constrictuml-a, Phascolosoma/Golfingia, 92 (Contraporus), Sipunculus, 40 convestitum/-«i, Phascolion, 114, 117 corallicola, Aspidosiphon, 218 corallicola/-um, Physcosoma/Phascolosoma, 381 corallicolus, Sipunculus, 385 coriacea, ?Themiste, 381 coriaceuml-a, Phascolosoma/Golfingia, 99, 154. 381 corrugatum, Nephasoma diaphanes, 94 coyi, Aspidosiphon, 221, 386 crassum, Siphonosoma, 55 cristatus, Lilhacro&iphon/Aspidosiphon, 229 cronullae, Phascolion strombus, 131 cryptum/-«5, Phascolion, 114, 115, 122 cubanus, Aspidosiphon fischeri, 222 cumanense: Siphonosoma, Phascolosoma, Sipunculus, 45, 48, 51, 54 cumingii, Aspidosiphon, 222 cupulifera, Diesingia, 381 (Cutlerensis), Nephasoma, 78, 87 cutleri: Nephasoma, Golfingia, 69, 78, 92 cylindratal-um, Golfingia/Phascolosoma, 70 cylindricus, Aspidosiphon, 381 cymodoceae: Themiste, Dendrostomum, 143, 152 (Dasmosiphon), Siphonosoma, 44 dayi, Siphonosoma, 45, 50, 53 deani: Phymosoma, Phascolosoma, lit deformis, Sipunculus, 51 dehamata/-wm, Themiste/Dendrostomum, 143. 153 delagei: Phascolosoma, Golfingia, Nephasoma, 70, 382 delphinus, Sipunculus, 37 demanni: Physcosoma, Phascolosoma, 382 Dendrostomal-um, 140; alutaceum, 148; blandum, 151; cymodoceae, 152; dehamatum, 153; dyscritum, 149; ellipticum, 153; fisheri, 153; fuscum, 154; hexadactylum, 151; huttoni, 156; lissum, 150; w(nor, 154; mytheca, 150; perimeces, 150; peruvianum, 150; petraeum, 151; pefricolum, 148; pinnifolia, 383; pyroides, 151; ramosum, 150; robertsoni, 154; rosaceum, 148; schmitti, 150; signifer, 153; spinifer,
441 383; stephensoni, 69, 154; tropicum, 154; zostericolum, 150 dentalii, Sipunculus, 130 dentalicolal-um, Phascolion, 118 dentigerum: Phascolosoma, Physcosoma, 182 depressa, Golfingia, 382 depressum: Phascolosoma, Nephasoma, 382 derjugini: Phascolosoma, Golfingia, 70 diaphanes: Nephasoma, Phascolosoma, Golfingia, 84, 89, 93, 97, 100 diaphanes: Phymosoma, Phascolosoma, 180 Diesingia, 381; Chamissoi, 381; cupulifera, 381 digitatum, Phascolosoma, 94 diptychus, Sipunculus titubans, 37 discrepans, Sipunculus, 40 dissors, Phascolosoma, 193 dogieli, Phascolion, 138 dubium, Phascolosoma, 75 dunwichi, Phascolosoma, 184 duplicigranulatum: Phascolosoma, Phymosoma, Physcosoma, 180 (Dushana), Golfingia, 61 dyscrita/-wm, Themiste/Dendrostomum, 149 echinorhynchus, Sipunculus, 385 Echinosiphon aspergillum, 232 (Edmondsius): Apionsoma, Phascolosoma, 159, 167, 190, 197 edu/e, Siphonosoma, 51 edulis: Sipunculus, Lumbricus, 51 elachea, Golfingia, 94 elegans: Aspidosiphon, Sternapsis, Sipunculus, Loxosiphon, Phascolosoma, 205, 214, 226 elisae: Nephasoma wodjanizkii, Golfingia, Nephasoma, 78, 102 elliptical-um, Themiste/Dendrostomum, 153 elongata/-Mm, Golfingia/P/iajco/oioma, 61, 62, 64, 69, 100 eniwetoki, Siphonosoma, 54 eremita: Nephasoma, Sipunculus, Phascolosoma, Golfingia, 78, 90, 94, 98 eremital-us, Aspidosiphon, 218, 386 esculental-um, Physcosoma/Phascolosoma, 176 evisceratum: Phascolosoma, Physcosoma, 180 exasperatum, Phascolosoma, 385 exhaustuml-us, Aspidosiphon, 219 exiguus, Aspidosiphon, 215 OCI/M, Aspidosiphon, 214
eximioclathratus, Sipunculus, 37 exostomuml-us, Aspidosiphon/Paraspidosiphon, 226 extortum: Phascolosoma, Physcosoma, 180
442 falcidentatum, Phascolosoma, 382 falcidentatus: Phymosoma, Physcosoma, 382 farcimen, Lesinia, 218 fasciatum, Phascolosoma, 178 fasciatus: Aspidosiphon steenstrupii, Paraspidosiphon steenstrupii, 225 fasciolatum, Phascolosoma, 385 filiforme, Nephasoma, 84, 95 filiformel-is, Phascolosoma!Golfingia, 95 fimbriatal-um, Golfingia/Nephasoma, 382 fimbriatum, Phascolosma, 382 finmarchica: Phascolosoma, Golfingia margaritacea, 71 fischeri, Aspidosiphon, 222 Fisherana, 159, 167; capitata, 168; lobostoma, 169; papillifera, 193, 383; wasini, 169 (Fisherana), Phascolosoma, Golfingia, 159, 167 fisheri: Dendrostomum, Themiste, 153 flagriferum, Nephasoma, 60, 68, 81, 83, 84, 90,95 flagriferum/-a, Phascolosoma/Golfingia, 95 flavus, Sipunculus, 178 forbesi, Phascolosoma, 70 formosanus: Aspidosiphon, Paraspidosiphon, 227
formosense: Phascolosoma, Physcosoma, 173 formosum, Siphonosoma, 52 fulgens, Phascolosoma, 71 funafuti: Siphonosoma, Sipunculus, 45, 48, 51,53 funafutiense: Physcosoma, Phascolosoma, 177 fuscal-um, Themiste I Dendrostomum, 154 fuscum, Phascolosoma, 72, 188 fuscus: Aspidosiphon, Paraspidosiphon, 225 galapagensis, Sipunculus, 38 gaudens: Physcosoma, Phascolosoma, 188 genuensis, Sipunculus, 178 georgianum, Phascolosoma, 72 gerardi, Phascolion, 117 gerouldi, Aspidosiphon, 217 g/gas: Aspidosiphon, Paraspidosiphon, 223 gigas, Sipunculus, 37, 385 glabrum: Phascolosoma, Physcosoma, 163, 164, 177 glaciale: Onchnesoma, Phascolosoma, 96 glacialis, Golfingia, 90, 96 j/nnj: Sipunculus, Phascolosoma, 188, 385 glauca: Golfingia, Themiste, 154 glaucum: Phascolosoma, Physcosoma, 154, 173 glossipapillosal -um,
Taxonomic Index Golfingia/Phascolosoma, 72 Golfingia, 61, 67, 68, 159; abnormis, 198; abyssorum, 89; adriatica, 76; anderssoni, 63, 64x65, 68; anguinea, 381; appendiculata,'i^; approximata, 381; benhami, 90; birsteini, 62, 64, 65, 69; bulbosa, 90; cantabriensis, 72; capensis, 69; capilleformis, 90; capitata, 168; catharinae, 103; charcoti, 70; churn, 381; cincta, 93; a w rea, 99; confusua, 91; confusa zarenkovi, 91; constricta, 92; constricticervix, 91; coriaceal-um, 99, 140, 154, 381; cutleri, 92; cylindrata, 70; delagei, 382; depressa, 382; derjugini, 70; diaphanes, 93; elachea, 94; efoae, 102; elongata, 61, 62, 64, 69, 100; eremita, 94; eremita australe, 94, 99; eremita californica, 94; eremita scabra, 94; filiformis, 95; fimbriata, 382; /7agrifera, 95; glacialis, 90, 96; glauca, 154; glossipapillosa, 72; hespera, 195, 196; hozawai, 105; hudsoniana, 74; hyugensis, 105; immunita, 190, 382; improvisa, 93, 97; incomposita, 89; iniqua, 64, 70; m«ojcla, 382; kolensis, 76; laetmophila, 96; /agensis, 382; lanchesteri, 154; lilljeborgii, 96; liochros, 77; lobostoma, 169; Zongirostris, 195; macginitiei, 105; mackintoshii, 76; macra, 382; margaritacea, 69, 71, 74; margaritacea adelaidensis, 71; margaritacea antarctica, 72; margaritacea californiensis, 71; margaritacea finmarchica, 71; margaritacea hanseni, 71; margaritacea ikedai, 72; margaritacea meridionalis, 72; margaritacea ohlini, 73; margaritacea sibirica, 71; margaritacea trybomi, 72; martensi, 103; mawioni, 73; mexicana, 212; minuta, 88, 89, 93, 97, 100; mirabilis, 62, 65, 74; misakiana, 195; mokyevskii, 188; mucida, 95; mw/riaraneusa, 98; muricaudata, 62, 64, 65, 74; murinae, 195; murinae bilobatae, 196; murinae unilobatae, 195; mutabilis, 71; neimaniae, 141, 382; nicolasi, 101; nigra, 105; nordenskjoldi, 72; «ofcz, 72; «ovaezealandiae, 98; okinoseana, 72; o«agawa, 105; owstoni, 76; papillifera, 193, 383; pavlenkoi, 105; pectinatoides, 62, 64, 67; pellucida, 98; procera, 106; profunda, 72; pudica, 73; pugettensis, 105; pusilla, 197; pyriformis, 154; quadrata, 383; recondita, 193, 383; reticulata, 383; ri/m'co/a, 100; rugosa, 70; rugosa mauritaniensis, 383; rutilofusca, 87; sanderi, 76; sarsii, 383; sava/ovi, 168; schuettei, 100; scutiger, 383; sectile, 93; semperi, 103; sewelli, 383; ii'gna, 72; sluiteri, 99; solitaria, 76;
Taxonomic Index soya, 72; tasmaniensis, 100; tenuissima, 195; trichocephala, 196; verrillii, 99; vitjazi, 101; vitrea, 384; vulgaris, 62, 65, 74, 75; vulgaris astuta, 75; vulgaris herdmani, 62, 76; vulgaris multipapillosa, 75; v«/garw murinae, 73; vulgaris queenslandensis, 77; vulgaris selenkae, 75; vulgaris tropica, 75; vulgaris vesiculosus, 75; wodjanizkii, 101; zenibakensis, 105 GOLFINGIAFORMES, 60 (Golfingiella), Golfingia, 61 GOLFINGIIDAE, 60 GOLFINGIIFORMES, 60 golikovi, Phascolosoma, 174 gosnoldi, Aspidosiphon, 215 gouldii: Phascolopsis, Sipunculus, Phascolosoma, Golfingia, 57 gracilis/-e, Aspidosiphon/Psewda.spjdosipfton, 216
grandis: Aspidosiphon, Paraspidosiphon, 223 granulatum: Phascolosoma, Physcosoma, 177 gravieri, Sipunculus, 39, 43 £rayi, Phascolosoma, 181 gurjanovae, Lithacrosiphon, 229 guttatusl-um, Sipunculus/Phascolosoma, 184, 385 hamulatum, Phascolosoma, 130 hanseni: Phascolosoma margaritacea, Golfingia margaritacea, 71 hartmeyeri, Aspidosiphon, 211, 217 harveyi: Syrinx, Phascolosoma, 75 taai'j, Siphonosoma, 52 havelockensis, Aspidosiphon, 227 hawaiense, Siphonosoma, 54 hebes: Physcosoma, Phascolosoma, 52 hedraeum, Phascolion, 114, 118 hennahi, Themiste, 149, 150 herdmani: Centrosiphon, Golfingia vulgaris, 62, 76 heronis, Phascolosoma, 185 herouardi, Physcosoma, 178 hespera: Phascolosoma, Golfingia, 195, 196 (Hesperosiphon), Siphonosoma, 44 heterocyathi, Sipunculus, 218 heteropapillosum, Phascolion, 127 heteropsammiarum, Aspidosiphon, 218 hexadactylal-um, Themiste I Dendrostomum, 151 hibridum/-ui, Phascolion, 114, 128 hirondellei, Phascolion, 120 hispitrofus, Aspidosiphon, 219 Homalosoma laeve, 71 homomyariuml-us, Aspidosiphon, 214 horsti: Physcosoma, Phascolosoma, 180 ftozawa/: Phascolosoma, Golfingia, 105
443 hudsonianal-um, GolfingialPhascolosoma, 74 hupferi, Phascolion, 114, 122 huttoni: Themiste minor, Phascolosoma, Dendrostomum, 154, 155 hyugensis: Phascolosoma, Golfingia, 105 ikedai, Golfingia margaritacea, 72 ikedai, Phascolion, 382 imbellis, Aspidosiphon, 218 immodestusl-um, Sipunculus/Phascolosoma, 188 immunituml -a, Phascolosoma)'Golfingia, 190, 382 improvisual-um, Golfingial Phascolosoma, 93,97 inclusus, Sipunculus phalloides, 38 incomposita, Golfingia, 89 incompositum: Phascolosoma, Nephasoma, 89 indicus, Lithacrosiphon, 229 indicus, Phascolion, 122 indicus, Sipunculus, 30, 40 indicus, Xenosiphon (Xenopsis), 40 infrons, Sipunculus, 36 ingens: Siphonosoma, Siphonomecus, 45, 48, 53.54 iniqua/-wm, Golfingia/Z'Aasco/asoma, 64, 70 innoxiuml-a, Phascolosoma/Golfingia, 382 inquilinus, Aspidosiphon, 218 insularis: Aspidosiphon, Paraspidosiphon, 182
intermedial-um, Phascolion/Phascolosoma, 130 intermedium, Onchnesoma, 134, 136 (Isomya), Phascolion, 116 japonicum, Cloeosiphon, 232 japonicum: Phascolosoma, Phymosoma, Physcosoma, 173 javanicum, Cloeosiphon, 232 javenensel-is, Phascolosoma/Sipunculus, 181, 182, 385 Jeffreysii, Phascolosoma, 178 johnstoni, Paraspidosiphon, 223 johnstoni, Phascolosoma, 385 joubini: Sipunculus, Siphonosoma, 382 jukesii, Aspidosiphon, 206, 218 kapalum, Phascolosoma, 185 klunzingeri, Aspidosiphon, 223 kolensel-is, Phascolosoma!Golfingia, 76 koreae, Siphonosoma, 52 kovaleskii, Aspidosiphon, 219 kukenthali, Lithacrosiphon, 229 kurchatovi, Phascolion, 118
Taxonomic Index
444 kurilense: Phascolosoma agassizii, Physcosoma, 174 lacteum: Phascolosoma, Phymosoma, Physcosoma, 180 laetmophilum/-a, Nephasomn/Golfingia, 78, 96 laeve, Homalosoma, 71 laeve, Phascolosoma, 178, 185 laevis/-e, Aspidosiphon, 205, 221, 222, 386 lageniformis, Themiste, 143, 144, 153 (Lagenopsis), Themiste, 142, 143, 144, 152 lagensel-is, Phascolosoma!Golfingia, 382 lakshadweepensis, Lithacrosiphon cristatus, 230 lanchesteri, Golfingia, 154 lanzarotae, Physcosoma, 178, 185 leachii, Phascolosoma, 385 (Lesenka), Phascolion, 121 Lesinia farcimen, 218 levis: Aspidosiphon, Paraspidosiphon, 227 levis, Sipunculus, 178 lilljeborgi: Nephasoma, Phascolosoma, Golfingia, 83, 89, 93, 96 liochros, Golfingia, 77 lissal-um, ThemistelDendrostomum, 150 Lithacrosiphon, 227; alticonus, 229; cristatus, 229; cristatus lakshadweepensis, 230; gurjanovae, 229; indicus, 229; kukenthali, 229; maldivensis, 230; odhneri, 229; poritidis, 229; uniscutatus, 229 lobostoma: Phascolosoma, Fisherana, Golfingia, 169 lobostomum, Phascolosoma, 169 lomonossovi, Sipunculus, 33 longicolle, Phascolosoma, 75, 386 longipapillosus, Sipunculus, 25, 27, 30, 31, 35. 43. 44 longirhyncus, Aspidosiphon, 212 longirostris, Golfingia, 195 lordi, Phymosoma, 173 loricatum, Phascolosoma, 386 loveni, Phascolosoma, 178 Loxosiphon aspergillus, 232; elegans, 214 lucifugax, Phascolion, 114, 119 Lumbricus edulis, 51; phalloides, 38 /wrco: Phascolosoma, Phymosoma, Physcosoma, 176 lutense, Phascolion, 109, 114, 115, 124 luteum, Phascolosoma, 75 lutulenta, Themiste, 386 lytkenii, Tylosoma, 120 macer: Phascolosoma, Aspidosiphon, 382 macginitiei, Golfingia, 105 mackintoshii, Golfingia, 76
macra, Golfingia, 382 macrorhynchus, Sipunculus, 385 maculatum: Phascolosoma, Phymosoma, Physcosoma, 178 magnibathum/-a, Onchnesoma, 134, 137 major, Aspidosiphon, 223 makoensis: Aspidosiphon, Paraspidosiphon, 225
malaccensis, Phascolosoma arcuatum, 176 malaccensis: Phymosoma lurco, Physcosoma lurco, 176 maldivensis, Lithacrosiphon, 230 manceps, Phascolion, 382 maoricus, Sipunculus, 41 marchadi, Siphonosoma, 52 marcusi, Sipunculus, 30, 35 margaritacea: Golfingia, Phascolosoma, 69, 71 margaritaceum: Golfingia, Phascolosoma, 71 margaritaceus, Sipunculus, 71 marinki, Nephasoma, 95, 96 martensi: Phascolosoma, Golfingia, 103 mauritaniensel-is, Phascolosoma rugosumlGolfingia rugosa, 383 mauritaniense: Physcosoma, Phascolosoma, 382 ntOMVORi: Phascolosoma, Golfingia, 73 mediterraneum, Phascolion, 117 medusae, Phascolion, 114, 115, 128 megaethi, Phascolion, 114, 128 meridionalis: Phascolosoma margaritacea, Golfingia margaritacea, 72 meteori: Phascolosoma, Phymosoma, Physcosoma, 161, 179 mexicanus/-a, Aspidosiphon/GoZ/ingia, 203, 205, 212
michelini, Aspidosiphon, 218 microdentigerum: Phascolosoma, Physcosoma, 182 microdontoton: Phascolosoma, Phymosoma, 174. 177 microrhynchus, Sipunculus, 385 microspheroidis/-c/-cs, Phascolion, 114, 119 minor: Themiste, Dendrostomum, 141, 154 minuta, Golfingia, 97 minutum: Nephasoma, Phascolosoma, Petalosoma, 88, 89, 93, 97, 100 minutum: Physcosoma, Phascolosoma, 180 mirabilis, Aspidosiphon, 218 mirabilis, Golfingia, 62, 65, 74 mirus, Aspidosiphon exhaustus, 219 misakiana: Apionsoma, Golfingia, 195 misakianum: Apionsoma, Phascolosoma, 195 misakiensis, Aspidosiphon, 214, 222 (Mitosiphon), Golfingia, 189, 190, 194 mogadrense, Phascolion, 130
Taxonomic Index mokyevskii: Golfingia, ?Aspidosiphon, 188 mollis, Cloeosiphon, 232 (Montuga), Phascolion, 124 moskalevi, Phascolion, 382 mossambiciense: Phymosoma scolops, Physcosoma scolops, Phascolosoma scolops, 175, 183 mourense, Siphonosoma, 45, 54 mucidal-um, Golfingia/Phascolosoma, 95 muelleri, Aspidosiphon, 205, 218, 220, 231 multiannulata, Phascolosoma, 174, 177 multiannulatura, Phascolosoma glabrum, 177 multiaraneusa, Nephasoma, 78, 98 multicinctus, Siphonomecus, 56 multipapillosalum, Golfingia vulgaris!Phascolosoma vulgare, 75 multisulcatus, Sipunculus, 38 multitorquatus, Sipunculus, 178 mundanus: Sipunculus, Xenosiphon, 30, 40 muricaudata/-Mj«, Golfingia/'Phascolosoma, 62, 64, 65, 74 murinae: Apionsoma, Golfingia, 195 murinae, Golfingia vulgaris, 73 murrayi, Phascolion, 123 mutabilel-is, Phascolosoma) Golfingia, 71 mytheca, Dendrostomum, 150 nahaense: Phymosoma, Phascolosoma, 184 nutans, Sipunculus, 39 neimaniae: Golfingia, ?Themiste, 141, 383 Nephasoma, 77, 88; abyssorum, 78, 83, 89, 96; abyssorum benhami, 90; bulbosum, 81, 90; capilleforme, 69, 90, 97; chuni, 381; confusum, 78, 91; constricticervix, 78, 81, 84, 91, 93, 101; constrictum, 83, 84, 91, 92; cutleri, 69, 78, 92; delagei, 382; depressum, 382; diaphanes, 84, 89, 93, 97, 100; diaphanes corrugatum, 94; eremita, 78, 90, 94, 98; filiforme, 84, 95; fimbriatum, 382; flagriferum, 60, 68, 81, 83, 84, 90, 95; incompositum, 89; laetmophilum, 78, 96; lilljeborgi, 83, 89, 93, 96; marinki, 95, 96; minutum, 88, 89, 93, 97, 100; multiaraneusa, 78, 98; novaezealandiae, 78, 84, 98; pellucidum, 92, 98, 99, 100; pellucidum subhamatum, 99; rimicola, 78, 100; rutilofuscum, 78, 84, 87; schuettei, 78, 94, 100; sewelli, 383; tasmaniense, 84, 100, 101; vitjazi, 78, 83, 84, «H; vitreum, 384; wodjanizkii, 83, 84, 101; wodjanizkii elisae, 78, 102 nicolasi, Golfingia, 101 nigra, Thysanocardia, 103, 105 nigral-um, Golfingia/Phascolosoma, 105 nigrescens: Phascolosoma, Phymosoma, Physcosoma, 161, 163, 179
445 nigriceps, Phascolosoma, 188 nigritorquatum: Phymosoma, Physcosoma, Phascolosoma, 383 nitidus, Sipunculus, 36 noduliferum/-Mi, Phascolosoma/Sipunc«/Hi, 164, 181 nodulosus, Sipunculus, 181 nordenskjoldi: Golfingia, Phascolosoma, 72 nordfolcense, Phascolosoma, 386 norvegicus, Sipunculus, 30, 35, 36 notal-o, Golfingia/Phascolosoma, 72 novaepommeraniae: Sipunculus, Siphonosoma, 52 novaezealandiae, Nephasoma, 78, 84, 98 nudum, Onchnesoma steenstrupii, 134, 139 nudus, Sipunculus, 30, 31, 35, 36, 39 nudus, Syrinx, 37 nudus, Xenosiphon branchiatus, 43 obliquoscutatus, Aspidosiphon grandis, 223 obscuruml-us, PhascolosomalSipunculus, 70, 75 ochrus, Aspidosiphon, 226 odhneri, Lithacrosiphon, 229 oerstedii, Phascolosoma, 71 ohlini: Golfingia margaritacea, Phascolosoma, 73 okinoseanal-um, Golfingia/Phascolosoma, 72 oligopapillosum, Onchnesoma squamatum, 134. 138 onagawa: Phascolosoma, Golfingia, 105 Onchnesoma, 133; glaciate, 96; intermedium, 134, 136; magnibathum/-a, 134, 137; sarsii, 383; squamatum, 134, 136, 137; squamatum oligopapillosum, 134, 138; steenstrupii, 133, 134, 138; steenstrupii nudum, 134. 139 onomichianum: Phymosoma, Physcosoma, Phascolosoma, 188 opacal-um, Siphonosoma cumanense, 51 opacus, Sipunculus cumanense, 51 orbiniense, Phascolosoma, 148, 386 orbiniensis: Sipunculus, Themiste, 148, 386 owstoni: Golfingia, Phascolosoma, 76 oxyurum, Phascolosoma, 70 pachydermatus, Aspidosiphon, 223 pacificum, Phascolion, 114, 125 pacificum: Phascolosoma, Phymosoma, Physcosoma, 161, 164, 177, 181 pallidum, Phascolion, 120 papillifera: Fisherana, Golfingia, 193, 383 papilliferum: Apionsoma, Phascolosoma, 193. 383 papillosum, Sipunculus, 75, 178
446 Paraspidosiphon, 201, 221; ambonensis, 227; angulatus, 223; brasiliensis, 223; cumingii, 222; exostomus, 226; fischeri, 222; fischeri cubanus, 222; formosanus, 227; gigas, 223; grandis, 223; insularis, 182; yoAnrfo/ii, 223; klunzingeri, 223; /evw, 227; makoensis, 225; pachydermatus, 223; pygmaeus, 218; schnehageni, 216; semperi, 225; speciosus, 223; speculator, 217, 225; spinososcutatus, 224; steenstrupii, 225; steenstrupii fasciatus, 225; tenuis, 226; trinidensis, 226; truncatus, 221 (Paraspidosiphon), Aspidosiphon, 200, 208, 221 parvulus, Aspidosiphon, 215, 224 parvum, Siphonosoma, 55 parvus!-um, Phascolion, 383 pavlenkoi: Phascolosoma, Golfingia, 105 pectinatoides, Golfingia, 62, 64, 67 pectinatum: Apionsoma, Phymosoma, Physcosoma, Phascolosoma, 157, 197 pellucidal-us, Golfingia!Sipunculus, 98 pellucidum: Nephasoma, Phascolosoma, 92, 98, 99, 100 pellucidusl -um, Sipunculus ISiphonosoma, 383 pelma: Phymosoma, Physcosoma, 188 pelmum, Phascolosoma, 188 perimeces: Themiste, Dendrostomum, 150 perlucens, Phascolosoma, 163, 164, 165, 182 peruvianum, Dendrostomum, 150 pescadolense, Siphonosoma, 50 Petalosoma minutum, 97 petraeum, Dendrostomum, 151 petricolal-um, ThemistelDendrostomum, 148 phalloides: Sipunculus, Lumbricus, 38 pharetratum, Phascolion, 114, 129 (Phascolana), Golfingia, 189, 194 Phascolion, 108, 124, 125; abnorme, 114, 126; africanum, 130; alberti, 130; a«omalus, 131; artificiosusl -um, 130; fceklemischevi, 117; bogorovi, 114, 127; botulusl-um, 381; brotzkajae, 131; canum, 124; caupo, 114, 122, 127; cirratum/-«i, 114, 132; collare, 114, 121; convestitum/-«i, 114, 117; cryptum/-M.s, 114, 115, 122; dentalicolal-urn, 118; dogieli, 138; gerardi, 117; hedraeum, 114, 118; heteropapillosum, 127; hibridum/-«i, 114, 128; hirondellei, 120; hupferi, 114, 122; ikedai, 382; indicus, 122; intermedia, 130; fcurcteovi, 118; lucifugax, 114, 119; lutense, 109, 114, 115, 124; manceps, 382; mediterraneum, 117; medusae, 114, 115, 128; megaethi, 114, 128; microspheroidis/e/-«, 114, 119; mogadrense, 130; mo-
Taxonomic Index skalevi, 382; murrayi, 123; pacificum, 114, 125; pallidum, 120; parvuml-us, 383; pharetratum, 114, 129; psammophilus, 129; rectum/-us, 114, 123; robertsoni, 114, 115, 128, 130; sandvichi, 383; jpeMbergense, 130; squamatum, 137; strombus/-i, 109, 112, 114, 115, 118, 122, 125, 127, 130; strombus cronullae, 131; temporariae, 120; tortum, 131; tridens, 122; tuberculosum, 109, 114, 115, 117, 118, 119, 120, 132; tubiculum, 130; ushakovi, 114, 132; valdiviae, 114, 123; valdiviae sumatrense, 114, 123 PHASCOLIONIDAE, 107 (Phascoloides), Golfingia, 77 Phascolopsis, 57; gouldii, 57 Phascolosoma, 159, 169; abnorme, 198; abyssorum, 89; abyssorum punctatum, 70; agassizii, 163, 173; agassizii kurilense, 174; albidum, 71; albolineatum, 163, 174, 184; ambiguum, 385; ambonense, 176; ance/w, 93, 97; andamanensis, 174; andersoni, 68; angumeum, 381; annulatum, 175; antillarum, 186; appendiculatum, 74; approximatum, 381; arcuatum, 163, 167, 176; arcuatum malaccensis, 176; asperum, 182; aspidosiphonoides, 87; awer, 188; <w.sfra/e, 50; benhami, 90; boreale, 94; bulbosum, 90; capense, 69; capitatum, 168; capsiforme, 71; carneum, 184, 385; catharinae, 103; charcoti, 70; c/zwm, 381; cinctum, 93; cinereum, 99; cluthensis, 70; cochlearium, 385; commune, 75; confusum, 91; constellatum, 385; constrictum, 92; corallicolum, 381; coriaceum, 140, 381; cumanense, 51; cylindratum, 70; deani, 176; delagei, 70; demanni, 382; dentigerum, 182; depressum, 382; dcrjugini, 70; diaphanes, 180; digitatum, 94; dissors, 193; dubium, 75; dunwichi, 184; duplicigranulatum, 180; elegans, 214; elongatum, 69; eremita, 94; esculental-um, 176; evisceration, 180; exasperatum, 385; exfoMwm, 180; falcidentatum, 382; /izsciatum, 178; fasciolatum, 385; filiforme, 95; fimbriatum, 382; flagriferum, 95; /or6ejH, 70; formosense, ijy, fulgens, 71; funafutiense, 177; fuscum, 72, 188; gaudens, 188; georgianum, 72; glabrum, 163, 164, 177; glabrum multiannulatum, 177; glaciale, 96; gtow, 188; glaucum, 154. J73; glossipapillosum, 72; golikovi, 174; gouldii, 57; granulatum, 177; gray!, 181; guttatum, 184, 385; hamulatum, 130; harveyii, 75; hebes, 52; heronis, 185; hespera, 195, 196; Aorrfj, 180; hozawai.
Taxonomic Index 105; hudsonianum, 74; huttoni, 155; hyugensis, 105; immodestum, 188; immunitum, 190, 382; improvisum, 97; incompositum, 89; iniquum, 70; innoxium, 382; intermedium, 130; japonicum, 173; javenense, 181, 182; jeffreysii, 178;johnstoni, 385; kapalum, 185; kolense, 76; ta> te«m, 180; /aeve, 178, 185; lagense, 382; leachii, 385; lilljeborgii, 96; lobostomum, 169; longicolle, 75, 386; loricatum, 386; loveni, 178; forco, 176; luteum, 75; macer, 382; maculatum, 178; margaritacea, 71; margaritacea antarcticum, 72; margaritacea hanseni, 71; margaritacea meridionalis, 72; margaritacea trybomi, 72; martensi, 103; mauritaniense, 382; raawttwii, 73; meteori, 161, 179; microdentigerum, 182; microdontoton, 177; minutum, 93, 97, 180; misakianum, 195; mucidum, 95; multiannulatal-um, 174, 177; muricaudatum, 74; mutabile, 71; nahaense, 184; nigrescens, 161, 163, 179; nigriceps, 188; nigritorquatum, 383; nigrum, 105; noduliferum, 164, 181; nordenskjoldi, 72; nordfolcense, 386; now, 72; novae-zealandiae, 98; obscurum, 70, 75; oerstedii, 71; ohlini, 73; okinoseanum, 72; onagawa, 105; onomichianum, 188; orbiniense, 148, 386; owstoni, 76; oxyura/w, 70; pacificum, 161, 164, 177, 181; papilliferum, 193, 383; papillosum, 193, 383; pavlenkoi, 105; pectinatum, 197; pe/lucidum, 98; pelmum, 188; perlucens, 163, 164, 165, 182; placostegi, 386; p/a/iispinosum, 180; plicatum, 179, 386; powrra/eri, 386; procerum, 103, 106; profundum, 72; psaron, 184; pudicum, 73; punctatissimum, 75; puntarenae, 179; pusillum, 197; pygmaeum, 386; pyriformis, 154; quadratum, 383; radiata, 218; rap<2, 150; reconditum, 193, 383; reticulatum, 383; rhizophora, 176; nisei, 99; riukiuensis, 184; rottnesti, 184; rueppellii, 383; rugosa mauritaniense, 383; rugosum, 70; sabellariae, 93, 97; sanderi, 76; saprophagicum, 161, 163, 167, 183; sarsii, 383; schmidti, 188; schuttei, 100; scolops, 163, 174, 183; scolops adenticulatum, 184; scolops mossambiciense, 183; scutiger, 383; semicinctum, 386; semirugosum, 52; semperi, 103; sewelli, 383; signum, 72; simile, 188; sluiteri, 99; socium, 72, 184; solitarium, 76; soyo, 72; spengeli, 180; spinicauda, 185; spinosum, 182; spongicolum, 184; squamatum, 137; stephensoni, 163, 165, 178, 184, 185; subhamatum, 99;
447 tasmaniense, 175; tenuicinctum, 70; teres, 70; thomense, 182; truncatum, 221; tubicula, 130; tumerae, 163, 185; validum, 76; varians, 180; vermiculusl-um, 182; verrillii, 99; violaceum, 55; vitreum, 384; vulgare, 75; vulgare astuta, 75; vulgare multipapillosum, 75; vulgare selenkae, 75; vulgare tropicum, 75; wasini, 169; weWon«, 188; yezoense, i~jy, zenibakense, 105 PHASCOLOSOMAFORMES, 156 PHASCOLOSOMATIDAE, 156 PHASCOLOSOMATIDEA, 156 PHASCOLOSOMATIFORMES, 156 PHASCOLOSOMIDA, 156 Phascolosomum, 159 Phymosomal-um, 159; agassizii, 173; a/oolineatum, 174; antillarum, 186; asperum, 182; asser, 188; deani, 176; dentigerum, 182; diaphanes, 180; duplicigranulatum, 180; falcidentatus, 382; japonicum, 173; lacteum, 180; /ordj, 173; /urco, 176; /«rco malaccensis, 176; maculatum, 178; meteori, 179; microdontoton, 174, 177; nahaense, 184; nigrescens, 179; nigritorquatum, 383; onomichianum, 188; pacificum, 1S1; pectinatum, 197; pelma, 188; psaron, 184; scolops, 183; scolops mossambiciense, 183; spengeli, 180; varians, 180 Physcosomal-um, 159; abyssorum, 168; agassizii, 173; albolineatum, 174; ambonense, 176; antillarum, 186; tme/-, 188; capitatum, 168; corallicola, 381; demanni, 382; duplicigranulatum, 180; esculenta, 176; evisceratum, 180; extortum, 180; falcidentatus, 382; formosense, 173; funafutiense, 177; gaudens, 188; glabrum, 177; glaucum, 173; granulatum, 177;fceftes,52; herouardi, 178; /wrsri, 180; japonicum, 173; kurilense, 174; lacteum, 180; /anzarotae, 178, 185; /arco, 176; /«/ro malaccensis, 176; maculatum, 178; mauritaniense, 382; meteori, 179; microdentigerum, 182; minutum, 180; nigrescens, 179; nigritorquatum, 383; onomichianum, 188; pacificum, 181; pectinatum, 197; pe/mwm, 188; psaron, 184; rueppellii, 383; scolops, 183; scolops adenticulatum, 184; scolops mossambiciense, 175, 183; scolops tasmaniense, 175; similis, 188; socium, 184; spengeli, 180; spongicola, 184; stephensoni, 185; thomense, 182; varians, 180; weldoni, 188; yezoense, 173 pinnifolial-um, Dendrostomum/Themiste, 383 placostegi, Phascolosoma, 386 planispinosum, Phascolosoma, 180 planoscutatus, Aspidosiphon, 225
448 plicatusl-um, Sipunculus!Phascolosoma, 179, 386 polymyotus, Sipunculus, 29, 30, 31, 39 poritidis, Lithacrosiphon, 229 porrectus, Sipunculus, 40 pourtalesi, Phascolosoma, 386 priapuloides, Sipunculus, 36 procera: Thysanocardia, Phascolosoma, Golfingia, 103, 106 procerum, Phascolosoma, 106 profunda/-um, GolfingialPhascolosoma, 72 psammophilus, Phascolion, 129 psaron: Phymosoma, Physcosoma, Phascolosoma, 184 Pseudaspidosiphon, 200; gracile, 216; clavatum, 218 pudical-um, Golfingial Phascolosoma, 73 pugettensis, Golfingia, 105 punctatissimuml-us, PhascolosomalSipunculus, 75 punctatum, Phascolosoma abyssorum, 70 puntarenae: Phascolosoma, Sipunculus, 179 pusilluml-a, Phascolosomal Golfingia, 197 pygmaeum, Phascolosoma, 386 pygmaeus: Aspidosiphon, Paraspidosiphon, 218 pyriformis: Phascolosoma, Golfingia, Themiste, 154 pyroides: Themiste, Dendrostomum, 145, 149. 150, 151, 155 quadratumi -a, Phascolosomal Golfingia, 383 quatrefagesi, Aspidosiphon, 223 queenslandensis, Golfingia vulgaris, JJ radiata, Phascolosoma, 218 ramosal -um, Themiste IDendrostomum, 150, 386 rapa: Sipunculus, Phascolosoma, 150, 385 ravus, Aspidosiphon, 214 recondita, Golfingia, 193, 383 reconditum, Apionsoma, Phascolosoma, 193, 383 rectum/-i«, Phascolion, 114, 123 reticulatuml -a, Phascolosomal Golfingia, 383 rhizophora, Phascolosoma, 176 rhyssapsis, Aspidosiphon, 386 rickettsi, Siphonides, 198 riuei, Phascolosoma, 99 rimicola: Nephasoma, Golfingia, 78, 100 riukiuensis, Phascolosoma, 184 robertsoni: Dendrostomum, Themiste, 154 robertsoni, Phascolion, 114, 115, 128, 130 robustus, Sipunculus, 30, 39 rosaceal-um, ThemisteIDendrostomum, 148
Taxonomic Index rotumanum/-MJ, Siphonosoma/Sip««c«/«i, 45,54 rottnesti, Phascolosoma, 184 rubens, Sipunculus, 385 rueppellii: Phascolosoma, Physcosoma, 383 (Rueppellisoma), Phascolosoma, 159 rufofimbriatus, Sipunculus, 385 rugosal-um, Golfingial Phascolosoma, 70 rutilofuscum, Nephasoma, 78, 84, 87 rutilofuscusl-a, Aspidosiphon!Golfingia, 87 sabellariae, Phascolosoma, 93, 97 saccatus, Sipunculus, 385 sanderi: Phascolosoma, Golfingia, 76 sandvichi, Phascolion, 383 saprophagicum, Phascolosoma, 161, 163, 167, 183 sarsii: Onchnesoma, Phascolosoma, Golfingia, 383 (Satonus), Phascolosoma, 159, 197 savalovi, Golfingia, 168 scabra: Phascolosoma eremita, Golfingia eremita, 94 schmidti, Phascolosoma, 188 schmitti: Themiste, Dendrostomum, 150 schnehageni: Aspidosiphon gracilis, Paraspidosiphon, 216 schuettei: Nephasoma, Golfingia, 78, 94, 100 schiittei, Phascolosoma, 100 scolops: Phascolosoma, Phymosoma, Physcosoma, 163, 174, 183 scutatus, Sipunculus, 218 scutiger. Phascolosoma, Golfingia, 383 sectile, Golfingia, 93 selenkae: Phascolosoma vulgare, Golfingia vulgaris, 75 semicinctum, Phascolosoma, 386 semirugosum: Phascolosoma, Siphonosoma cumanense, 51, 52 semperi: Aspidosiphon, Paraspidosiphon, 225 semperi: Phascolosoma, Golfingia, 103 sewelli: Phascolosoma, Golfingia, Nephasoma, 383 sibirica: Phascolosoma margaritacea, Golfingia margaritacea, 71 signal-um, Golfingial Phascolosoma, 72 signifer, Dendrostomum, 153 similisl-e, Physcosoma/Phascolosoma, 188 Siphonides rickettsi, 198 (Siphonoides), Golfingia, 61 Siphonomecus, 55; ingens, 53; multicinctus, 56 Siphonosoma, 44; amamiense, 53; arcassonense, 45, 48, 49; australe, 45, 50; australe takatsukii, 50; billitonense, 52; bo-
Taxonomic Index holense, 45, 48, 50; bonhourei, 81; carolinense, 52; crassum, 55; cumanense, 45, 48, 51, 54; cumanense opacal-um, 51; cumanense semirugosum, 52; cumanense vitreum, 51; cumanense yapense, 51; dayi, 45. 50. 53; edule, 51; eniwetoki, 54; formosum, 52; ftinaftiti, 45, 48, 51, 53; hataii, 52; hawaiense, 54; ingens, 45, 48, 53, 54; joubini, 382; koreae, 52; marchadi, 52; mourense, 45, 54; novaepommeraniae, 52; parvum, 55; pellucidum, 383; pescadolense, 50; rotumanum, 45, 54; vastum, 45, 48, 55 SIPUNCUUDA, 24 SIPUNCULIDAE, 24 SIPUNCULIDEA, 24 SIPUNCULIFORMES, 24 Sipunculus, 28; aeneus, 50; aequabilis, 36; amamiense, 53; angasii, 39; arcassonensis, 49; arcuatuu, 176; australis, 50; fta/anophorus, 37; bernnhardis, 130; M/litonensis, 52; boholensis, 50; bonhourei, 381; borealis, 94; caementarius, 130; capitatus, 130; clavatus, 385; claviger, 52; communis, 75; cochlearius, 218; concharum, 130; corallicolus, 385; CMmanense, 51; cumanensis opacus, 51; deformis, 51; delphinus, 37; dentalii, 130; discrepans, 40; echinorhynchus, 385; e
449 grinus, 37; titubans, 37; titubans diptychus, 37; tuberculatus, 180; vastus, 55; vermiculus, 182, 385; verrucosus, 178; Wolaceus, 55, 385; vulgaris, 75; zenkevitchi, 384 sluiteri: Phascolosoma, Golfingia, 99 socium: Physcosoma, Phascolosoma, 72, 184 solitarial-um, Golfingia/Phascolosoma, 76 soyal-o, Golfingia/Phascolosoma, 72 speciosus: Aspidosiphon, Paraspidosiphon, 223
speculator: Aspidosiphon, Paraspidosiphon, 217, 225 spengeli: Phascolosoma, Phymosoma, Physcosoma, 180 spetsbergense, Phascolion, 130 spinalis, Aspidosiphon, 214, 215 (Spinata), Golfingia, 65, 67 spinicauda!-um, Sipunculus/Phascolosoma, 185 spinifera: Dendrostoma, Themiste, 383 spinososcutatus: Aspidosiphon, Paraspidosiphon, 224 spinosum, Phascolosoma, 182 spinosus, Aspidosiphon, 214 spiralis, Aspidosiphon, 220 spongicolal -um, Physcosoma/Phascolosoma, 184 squamatum: Onchnesoma, Phascolosoma, Phascolion, 134, 136, 137 steenstrupii, Aspidosiphon, 225, 227 steenstrupii, Onchnesoma, 133, 134, 138 Stephanostoma barentsii, 71 stephensoni, Dendrostoma, 69, 154 stephensoni: Phascolosoma, Physcosoma, 163, 165, 178, 184, 185 (Stephensonum), Themiste, 61, 140 Sternaspis elegans, 214 strombus, Sipunculus, 130 strombus/-!, Phascolion, 109, 112, 114, 115, 118, 122, 125, 127, 130 subhamatal-um, Golfingia/Phascolosoma, 99 subhamatum, Nephasoma pellucidum, 99 sumatrense, Phascolion valdiviae, 114, 123 Syrinx, 28; harveyii, 75; nudus, 37; ferselatus, 37 takatsukii, Siphonosoma australe, 50 tasmaniense/-i.s, Nephasoma/GoZ/mgia, 84, 100, 101
tasmaniense: Phascolosoma, Physcosoma scolops, 175 temporariae, Phascolion, 120 tenuicinctum, Phascolosoma, 70 tenuis: Aspidosiphon, Paraspidosiphon, 226
Taxonomic Index
45o tenuissima, Golfingia, 195 teres, Phascolosoma, 70 tesselatus, Syrinx, 37 Themiste, 140, 148; alutacea, 145, 148, 149, 151; blanda, 149, 151; cymodoceae, 143, 152; dehamata, 143, 153; dyscrita, 149; elliptica, 153; fisheri, 153; fusca, 154; glauca, 154; hennahi, 149, 150; hexadactyla, 151; lageniformis, 143, 144, 153; lissa, 150; lutulenta, 386; minor, 141, 154; minor huttoni, 154, 155; neimaniae, 141, 383; orbiniensis, 148; perimeces, 150; petricola, 148; pinnifolium, 383; pyriformis, 154; pyroides, 145, 149, 150, 151, 155; ramosa, 150, 386; robertsoni, 154; rosacea, 148; schmitti, 150; spinifer, 383; stephensoni, 68, 154; tropica, 154; variospinosa, 155; zostericola, 150 THEMISTIDAE, 140 thomassini, Aspidosiphon, 205, 212 thomense: Phascolosoma, Physcosoma, 182 Thysanocardia, 102; catharinae, 103, 105, 106; nigra, 103, 105; procera, 103, 106 tigrinus, Sipunculus, 178 titubans, Sipunculus, 37 tortum, Phascolion, 131 tortus, Aspidosiphon, 218 trichoeephalus/-a, Apionsoma/Go//mg!'a, 196 tridens, Phascolion, 122 trinidensis: Aspidosiphon, Paraspidosiphon, 226 tropica, Golfingia vulgaris, 75 tropical -um, Themiste I Dendrostomum, 154 tropicum, Phascolosoma vulgare, 75 truncatum, Phascolosoma, 221 truncatus, Aspidosiphon/Paraspidosiphon,
valdiviae, Phascolion, 114, 123 validum, Phascolosoma, 76 varians: Phascolosoma, Phymosoma, Physcosoma, 180 variospinosa, Themiste, 155 vastum/-Mj, Svphonosom&lSipunculus, 45, 48, 55 venabulum/-«i, Aspidosiphon, 212 vermiculus: Sipunculus, Phascolosoma, 182, 385 verrillii: Phascolosoma, Golfingia, 99 verrucosus, Sipunculus, 178 vesiculosus, Golfingia vulgare, 75 (Villiophora), Phascolion, 132 violaceum, Phascolosoma, 55 violaceus, Sipunculus, 55, 385 vitjazi: Nephasoma, Golfingia, 78, 83, 84, 101
vitrea, Golfingia, 384 vitreum: Phascolosoma, Nephasoma, 384 vitreum, Siphonosoma cumanense, 51 vulgare, Phascolosoma, 75 vulgaris: Golfingia, Sipunculus, 62, 65, 74, 75 wasini, Phascolosoma, 169 weldoni: Physcosoma, Phascolosoma, 188 wodjanizkii: Nephasoma, Golfingia, 83, 84, 101
(Xenopsis), Xenosiphon, 40 Xenosiphon, 41; absconditus, 43; branchiatus, 30, 35, 41, 44; branchiatus nudus, 43; caribaeum, 44; indicus, 40; mundanum, 40
221
trybomi: Phascolosoma, Golfingia, 72 tuberculatus, Sipunculus, 181 tuberculosum, Phascolion, 109, 114, 115, 117, 118, 119, 120, 132 tubiculal -um, Phascolosoma/Phascolion, 130 turnerae, Phascolosoma, 163, 185 Tylosoma lytkenii, 120
yapensel-is, Aspidosiphon elegans, 214 yapense, Siphonosoma cumanense, 51 yezoense: Phascolosoma, Physcosoma, 173 zarenkovi, Golfingia confusa, 91 zenibakensel-is, Phascolosoma!'Golfingia, 105
unilobatae, Golfingia murinae, 195 uniscutatus: Aspidosiphon, Lithacrosiphon, 229 ushakovi, Phascolion, 114, 132
zenkevitchi, Sipunculus, 384 zinni, Aspidosiphon, 203, 213 zostericola/-um, Themiste/Dendrostomum, 150
Subject Index
actin control, 254-255 amoebocytes, 256, 268-269 amphi-American taxa, 369 amphitropical taxa, 324 anaerobic metabolism, 272-273 ancestral sipunculan (RHAS), revised hypothetical, 375 Ancorichnus, 335 Annelida, 253, 286, 303, 306, 336-344 antibacterial activity, 269 antibody production, 268-270 antiquity of taxa, 363, 371-374 Aphrodite, 242 Aplacophora, 343-344 Archicoelomata, 336 Arenicola, 255 arginine kinase, 275 asexual reproduction, 308-310 barriers, zoogeographical, 317, 323, 368369, 372 behavior, 239-241, 246 Bering land bridge, 364, 372 bilirubin, 258 bioerosion of reefs (coral boring), 237-238 biomedical uses of urn cells, 267-268 boundaries, zoogeographical, 316, 330, 372 Brachiopoda, 257, 258, 260, 261, 263, 340 breeding cycles, 300-301 budding, 308-309 burrows, burrowing, 237, 240-241 calcium carbonate, 249, 251 calcium ions, 254-255, 280 Cambrian, 319, 334-336, 344, 352, 375 carbonic anhydrase, 339 catch muscle, 252, 254-255 Caulalotilus, 244 Cenozoic, 322, 330, 331, 333, 336, 374, 377, 378, 379; sea level, 367-368; sea temperatures, 365-367; subregional oceanic events: Australia to Southeast Asia, 371; Eastern Pacific Barrier, 372; Mediterra-
nean Sea and northeastern Atlantic, 368; North Pacific, Arctic, and Far North Atlantic, 372-373; South Atlantic, 369; western Atlantic and eastern Pacific, 369371 center of origin, 315-316, 371-372 cerebral organ, 289 character state polarities, 346-354 chemoreception, 289 chromatin, 273-274, 340 chromosomal number/morphology, 354-357 cilia, 251 cladogenesis/speciation centers and events: Aspidosiphomformes, 332; Golfingiiformes, 324-329; Phascolosomatiformes, 330-331; Sipunculiformes, 322-323 cleavage, 301 coelomic cells, 256-257 Collostoma, 247 commensals, 246-247; mollusks, 246; polychaetes, 247; small metazoans, 246 corals, 238, 245, 331, 332, 335-336. 372. 378 cosmopolitan species, 319-320 crabs, 244, 246 Cretaceous, 316, 363, 364, 367, 368, 372; fossils, 335, 336 Crustacea, 242, 289, 291, 316 currents/ocean circulation, 365, 367, 369, 371-372 cuticle, 249-251 cytochromes, 264-265 cytotoxic activity, 270 Daphnia, 298 dermis, 251 Devonian, 335, 336 digestive system: anatomy, 282-283; physiology, 283-285 disjunct distributions, 316, 367, 388 dispersal, 316-319, 372 Drupa, 244
Subject Index
452 Echinodermata, 338, 340, 365, 369 Echiura, 306, 337, 339-340 encapsulation, 268-269 endemic taxa, 314-316, 318-319; Phascolosomatidea, 330, 332; Sipunculidea, 321-329 Entoprocta, 246 environmental deterioration/pollution indicators, 239 Eocene, 360, 364-365, 371 erythrocytes, 256-258, 264-265 Eudendrium, 246 excretory system: anatomy, 276-279; physiology, 279-281 extinctions, 360, 365, 370; local, 316, 321, 324, 367-368, 372-373 feeding, 239, 241-243 food for predators, 243-244 Foraminifera, 315, 332, 365, 366, 367, 369 fossil record, 334-336 Fronsella, 246 fusiform bodies, 293-296 gametes, 298-299 gas exchange, 271-272 gastrulation, 303 genetic variability (enzymes), 274 glands, epidermal, 251-252 glycogen storage, 264 Gondwanaland, 363 granulocytes, 256-257, 268 gravity reception, 290 guanidine compounds, 275 habitat, 236-239 hemerythrins: function, 261-264; oxidation levels, 264; structure, 258-261 hermaphroditism, 298 Heterocyathus, Heteropsammia, 238, 245 histones, 273-274 hooks, 249, 252 Hydrozoa (hydroids), 246 Hyolitha, 334 immune system, 268-270 inactivation, 263-269 integument/epidermis, 249-252 intercellular junction, 342 intestine, 282-283 irrigation of shelter, 239, 245 Jurassic, 335, 363, 364, 367 karyotypes, 354-357 Keferstein bodies, 292-293
larval development, 304-307 Laurasia, 363 leucocytes, 256-257, 270 Lingula, 263 Loxosomella, 246 Lumbricus, 255 Menestho, 247 Mesozoic, 315, 363-364, 371, 372; cladogenic events, 324, 331, 333, 373. 377. 378 Miocene: cladogenic events, 323, 329, 374, 379; fossils, 335-336; oceanic conditions, 316, 361, 364-372 Mollusca, 246, 288, 296, 303, 317, 334, 336-345. 365. 369, 372 Montacuta, 246-247 mucus-stimulating substance, 267-268 muscle physiology and biochemistry, 254255. 340 muscle systems, 252; body wall, 252; intestinal fasteners, 253-254; introvert retractors, 253; protractors, 253 Mustellus, 244 mutualism, 244-245 NADH diaphorase, 264 Nematoda, 248, 340 Neogene, 366, 373, 377, 378-380 nephridia, 276-279 nerve transmission, 288 nervous system, structure of, 286-288 neurosecretion, 291-292 niches, 236, 330, 336 nicotinic type receptor, 254 Nipponmysella, 246 nuchal organ, 289 numerical (phylogenetic) analysis, 346-349 Oligocene, 364-367, 371 Oligochaeta, 255, 270 Ordovician, 334-335, 377 osmoregulation, 279-281 Ostracoda, 366-367 Ottoia prolifica, 334, 352 Paleocene, 365, 366, 371 Paleogene, 316, 328, 368 Paleozoic: cladogenic events, 324, 328, 330332, 373, 376-379; fossils, 334-336; oceanic conditions, 360, 363 Panamanian area, 323, 366, 369, 372 Pangaea, 363 Panthalassa (Eo-Pacific), 324, 328, 330-332, 363, 371 paramyosin, 254-255
Subject Index parasitism, 243, 247-248 parthenogenesis, 298, 308 passive transport of larvae, 317-318 pelagosphera larva, 305-307 Perigonimus, 246 Permian, 326 phagocytosis, 256, 267-269 pheromone, 296 phospholipids, 339-340 phosphorus metabolites, 264 photoreception, 290 phototaxis, 239-240 plate tectonics, 360-364, 368-373 Pleistocene conditions, 316, 335, 366-367, 369, 373 Pleurodictyum, 336 Pliocene: cladogenic events, 323, 335, 374, 377; oceanic conditions, 365-367, 369, 372 Pogonophora, 251, 336 Polychaeta, 237-238, 242-243, 244, 247, 251, 255, 278 prey items, 243-244 Priapulida, 257, 258, 334, 352 Protoctista, 247, 269 Protostomia, 299, 336-338, 342 pyruvate catabolism, 340 Quaternary, 335, 367 quick muscle, 255 recognition of self/nonself, 268-270 regeneration, 310-311 respiration, 271-272 ribosomal RNA, 339, 341
453 sea level, 367-368 sense organs, 288-290 settlement of larvae, 308 sexual reproduction, 308-310 Silurian, 335 species concepts, 314 species-rich areas, 315 sperm anchoring fiber, 299, 342 Spheciospongia, 238 Spiralia, 336-338, 343 sterility, 248, 299 superoxide dismutase, 264 superphyla, 334, 339 Symbiongia, 336 symbiotic relationships, 244-248 temperature changes, 364-367 Tertiary, 324, 326, 364, 365 tested endemics, 314 Tethys Sea, 316, 322, 333, 363-365, 368 Triassic, 326, 363 Trichichnus, 237, 335 Triticella, 246 trochophore, 306-307 trophic dynamics, 241-244 Trypanites, 335 untested endemics, 314, 321, 324, 325, 328 urn cell complex (UCC), 265-268; biomedical applications, 267-268 vicariance, 316, 318, 321 Wadeopsammia, 336
