Lars CONAN a Ae RANA DIRE ANA A O a A Aa ECO AA A NANA ME O: EURE AE fain’ ME naar ба ETC ln pets ANA AMA AE om re M CROIENT PTE hon. LAP CE PAT ET ETES CORNE OE DORE SA pa CESTA na “m at mt emo, Se na, A ALOE A TETE on LUTTE ушей CONTES ACTES me Pra Mn ins RAM LA ук. in pe À AE EAN Bra A OB pre ve à Sala Me ALN mee желе 2 ee EEE Ber a ео я neunte ph str re nn A mL met MA Pl A ms Ru ann, DATE PPT 125008 був теб ath Реж A oe et itt ие GA neh nde neh ts um вл. AS Abe e OL GI teat oe men HOON AE nan nant ni Ad ze a main ор dm бл BETETE er dae On etat PEER EEE Tr ere >. ade м DIARIO Aran, Lau Ve мили улья, By A ie ran BIER Er ath LITE En an LEN DOUTER MAMA A D SEE ES cranes DO rea io tan Win HR tee САИ a m mt Setar зто doors ae D De D dr Seow " Ten чи ; А: ты ana Ne ee A N ot Ron ur RASE TE 0 dario az A da. MARA NA et A the on are na ¡DIRA A DE ses DOTE TEE an DELLE Mane are Pt en ao PRE Ann Canne Co 0 00 nn td a re Rae MD Pas fears param nn As cam mn MULLER: tn ie an Ay оны AA TR anne teat oi marne nimm rannte miles ma and HARVARD UNIVERSITY € Library of the Museum of Comparative Zoology , al Jogrnél à! 'Nnlacelany | lntermaciona! de Molimologia + i y À y A | | | р о LL еее. L | ae Hyena Manananorif wha) ach MOL. 32 1990, 1991 MALACOLOGIA International Journal of Malacology Revista Internacional de Malacologia Journal International de Malacologie Международный Журнал Малакологии Internationale Malakologische Zeitschrift Vol. Vol. Vol. Vol. Vol. Vol. Vol. Publication dates Me? ‚ No 19 January 1988 28 June 1988 16 Dec. 1988 1 Aug. 1989 29 Dec. 1989 28 May 1990 30 Nov. 1990 MALACOLOGIA, VOL. 32 CONTENTS RUDIGER BIELER & RICHARD E. PETIT On the Various Editions of Tetsuaki Kira’s “Coloured Illustrations of the Shells of Japan” and “Shells of the Western Pacific in Color Vol. |,” With an Annotated List of New Names Introduced ........................... PHILIPPE BOUCHET Turrid Genera and Mode of Development: The Use and Abuse of Pro- tOCONCRMONPhOlIOQ ME re Un epee ee: MALCOLM EDMUNDS INMTOQUCUON seis cis roe eee er ee ee E MALCOLM EDMUNDS Does Warning Coloration Occur in Nudibranchs? ...................... JOSE C. GARCIA-GOMEZ, ANTONIO MEDINA & RAFAEL COVENAS Study of the Anatomy and Histology of the Mantle Dermal Formations (MDFs) of Chromodoris and Hypselodoris (Opisthobranchia: EhromedenididaeW costa eee RI TERRENCE M. GOSLINER Morphological Parallelism in Opisthobranch Gastropods ............... GERHARD HASZPRUNAR Towards a Phylogenetic System of Gastropoda Part |: Traditional Meth- OOOO AGRE DI ante es a erat aon ge eee KATHE R. JENSEN Comparison of Alimentary Systems in Shelled and Non-Shelled Sacoglossa (+ Ascoglossa) (Gastropoda: Opisthobranchia) ........... ALAN R. KABAT Predatory Ecology of Naticid Gastropods with a Review of Shell Boring Predator RS LEN N YURI I. KANTOR Anatomical Basis for the Origin and Evolution of the Toxoglossan Mode OREBEÄNG trees ba E. ALISON KAY того гачпаз On Pacific Islands: EE ee ALAN J. KOHN Tempo and' Mode of Evolution in Conidae .:.::.........7............ JAMES NYBAKKEN Ontogenetic Change in the Conus Radula, its Form, Distribution Among the Radula Types, and Significance in Systematics and Ecology ...... JOSE ANGEL ALVAREZ PEREZ, MANUEL HAIMOVICI & JOAO CARLOS BRAHM COUSIN Sperm Storage Mechanisms and Fertilization in Females of Two South American Eledonids (Cephalopoda: Octopoda) ......................... 131 69 205 241 233 313 195 209 155 79 35 BERNARD E. PICTON Cumanotus beaumonti (Eliot, 1906), A Nudibranch Adapted for Life in a Shalew"Sañay Habitat? tao loa ее MATHIEU POULICEK, MARIE-FRANGOISE VOSS-FOUCART 4 CHARLES JEUNIAUX Regressive Shell Evolution Among Opisthobranch Gastropods ........ L. von SALVINI-PLAWEN The Status of the Rhodopidae (Gastropoda: Euthyneura) .............. ROGER R. SEAPY The Pelagic Family Atlantidae (Gastropoda: Heteropoda) From Hawai- ¡an Waters: A Faunistic Survey. оао оо GAMIL N. SOLIMAN A Comparative Review of the Spawning, Development and Metamorphosis of Prosobranch and Opisthobranch Gastropods with Special Reference to Those from the Northwestern Red Sea .......... JOHN D. TAYLOR INTOdUciON Taste o PAT UN LR Sone? Re UNS JOHN D. TAYLOR The Anatomy of the Foregut and Relationships in the Terebridae ..... CHRISTOPOHER D. TODD Larval Strategies of Nudibranch Molluscs: Similar Means to the SA A A A O RITA TRIEBSKORN & С. KUNAST Ultrastructural Changes in the Digestive System of Deroceras Reticula- tum (Mollusca; Gastropoda) Induced by Lethal and Sublethal Concen- trations of the Carbamate Molluscicide Cloethocarb .................... RICCARDO CATTANEO VIETTI & ANDREA BALDUZZI Relationship Between Radular Morphology and Food in the Doridina (Mollusca: Nudibranchia)) :.... se RICCARDO CATTANEO VIETTI 4 RENATO CHEMELLO The Opisthobranch Fauna of a Mediterranean Lagoon (Stagnone di Marsala, Western СПУ) oies en une 219 223 301 107 273 89 211 4 E MCZ 52 NO: 4 LIBRARY 1990 BEG Le) 1990 HARVARD UNIVERSITY ALACOLOGIA iternational Journal of Malacology ista Internacional de Malacologia 7 О rnal International de Malacologie _ Международный Журнал Малакологии 4 ale Malakologische Zeitschrift \ ra) i MALACOLOGIA Editor-in-Chief: GEORGE M. DAVIS Editorial and Subscription Offices: Department of Malacology The Academy of Natural Sciences of Philadelphia Nineteenth Street and the Parkway Philadelphia, Pennsylvania 19103, U.S.A. Co-Editors: p EUGENE COAN CAROL JONES California Academy of Sciences Payson, AZ San Francisco, CA Assistant Managing Editor: CARYL HESTERMAN Associate Editors: JOHN B. BURCH University of Michigan Ann Arbor ANNE GISMANN Maadi Egypt MALACOLOGIA is published by the INSTITUTE OF MALACOLOGY, the Sponsor Members of which (also serving as editors) are: KENNETH J. BOSS, JAMES NYBAKKEN, President Museum of Comparative Zoology Moss Landing Marine Laboratory Cambridge, Massachusetts. California JOHN BURCH, President-Elect CLYDE F. E. ROPER MELBOURNE R. CARRIKER и р University of Delaware, Lewes SON GEORGE M. DAVIS Sides ee Y Secretary and Treasurer У, SHI-KUEI WU CAROLE S. HICKMAN, Vice-President University of California, Berkeley University of Colorado Museum, UA Le Participating Members EDMUND GITTENBERGER JACKIE L. VAN GOETHEM Secretary, UNITAS MALACOLOGICA Treasurer, UNITAS MALACOLOGICA Rijksmuseum van Natuurlijke Koninklijk Belgisch Instituut Historie voor Natuurwetenschappen Leiden, Netherlands Brussel, Belgium | Emeritus Members J. FRANCIS ALLEN, Emerita ROBERT ROBERTSON Environmental Protection Agency The Academy of Natural Sciences Washington, D.C. Philadelphia, Pennsylvania ELMER G. BERRY, NORMAN F. SOHL Germantown, Maryland U.S. Geological Survey Reston, Virginia Copyright © 1990 by the Institute of Malacology 1990 EDITORIAL BOARD J. A. ALLEN Marine Biological Station Millport, United Kingdom E. E. BINDER Muséum d'Histoire Naturelle Genève, Switzerland A. J. CAIN University of Liverpool United Kingdom P. CALOW University of Sheffield United Kingdom A. H. CLARKE, Jr. Portland, Texas, U.S.A. B. C. CLARKE University of Nottingham United Kingdom R. DILLON College of Charleston SC, U.S.A. C. J. DUNCAN University of Liverpool United Kingdom E. FISCHER-PIETTE Muséum National d'Histoire Naturelle Paris, France VAEREIMER University of Reading United Kingdom E. GITTENBERGER Rijksmuseum van Natuurlijke Historie Leiden, Netherlands Е. GIUSTI Universita di Siena, Italy A. N. GOLIKOV Zoological Institute Leningrad, U.S.S.R. S. J. GOULD Harvard University Cambridge, Mass., U.S.A. A. V. GROSSU Universitatea Bucuresti Romania T. HABE Tokai University Shimizu, Japan R. HANLON Marine Biomedical Institute Galveston, Texas, U.S.A. A. D. HARRISON University of Waterloo Ontario, Canada J. A. HENDRICKSON, Jr. Academy of Natural Sciences Philadelphia, PA, U.S.A. K. E. HOAGLAND Association of Systematics Collections Washington, DC, U.S.A. B. HUBENDICK Naturhistoriska Museet Goteborg, Sweden S. HUNT University of Lancaster United Kingdom R. JANSSEN Forschungsinstitut Senckenberg, Frankfurt am Main, Germany (Federal Republic) В. М. KILBURN Natal Museum Pietermaritzburg, South Africa М. A. KLAPPENBACH Museo Nacional de Historia Natural Montevideo, Uruguay J. KNUDSEN Zoologisk Institut & Museum Kobenhavn, Denmark A. J. KOHN University of Washington Seattle, U.S.A. Y. KONDO A. LUCAS Faculté des Sciences Brest, France C. MEIER-BROOK Tropenmedizinisches Institut Tubingen, Germany (Federal Republic) H. K. MIENIS Hebrew University of Jerusalem Israel J. Е. MORTON The University Auckland, New Zealand J. J. MURRAY, Jr. University of Virginia Charlottesville, U.S.A. R. NATARAJAN Marine Biological Station Porto Novo, India J. OKLAND University of Oslo Norway T. OKUTANI University of Fisheries Tokyo, Japan W. L. PARAENSE Instituto Oswaldo Cruz, Rio de Janeiro Brazil J. J. PARODIZ Carnegie Museum Pittsburgh, U.S.A. М. Е. PONDER Australian Museum Sydney R. D. PURCHON Chelsea College of Science & Technology London, United Kingdom QRZ. Ne Academia Sinica Qingdao, People’s Republic of China М. W. RUNHAM University College of North Wales Bangor, United Kingdom S. G. SEGERSTRALE Institute of Marine Research Helsinki, Finland F. STARMUHLNER Zoologisches Institut der Universitat Wien, Austria У. |. STAROBOGATOV Zoological Institute Leningrad, U.S.S.R. W. STREIFF Université de Caen France J. STUARDO Universidad de Chile Valparaiso S. TILLIER Muséum National d’Histoire Naturelle Paris, France R. D. TURNER Harvard University Cambridge, Mass., U.S.A. W. $. $. VAN BENTHEM JUTTING Domburg, Netherlands J. A. VAN EEDEN Potchefstroom University South Africa N. H. VERDONK Rijksuniversiteit Utrecht, Netherlands B. R. WILSON Dept. Conservation and Land Management Netherlands, Western Australia H. ZEISSLER Leipzig, Germany (Democratic Republic) A. ZILCH Forschungsinstitut Senckenberg Frankfurt am Main, Germany (Federal Republic) UNITAS MALACOLOGICA 10th International Malacological Congress Symposium BIOLOGY AND EVOLUTION OF TOXOGLOSSAN GASTROPODS John D. Taylor Organizer 29 August & 1 September 1989, Tubingen, Federal Republic of Germany Malacologia Guest Editor John D. Taylor CONTENTS LRU TT LL SARA lo Lire (ins HIER a PRO CE A ки 1 Yu. |. Kantor. Anatomical basis for the origin and evolution of the toxoglossan etre AE, o N RO Shoe SEE SE VO ER vow Ga QU 3 J. D. Taylor. The anatomy of the foregut and relationships within IDO RETOUR aso N daR 19 J. Nybakken. Ontogenetic change in the Conus radula, its form, distribution amongst radula types, and significance in systematics ARSON ogi о о a RES ЕЕ NEO PERTE LE sia 35 А. J. Kohn. Tempo and mode of evolution in Conidae. ....................... 55 P. Bouchet. Turrid genera and mode of development: the use and abuse of BISIOBORICHEEHOTBEICHOGVE NS A Came eA PE AE 69 Е. A. Kay. ic AURAS or. PaCIRCHSIANdS LES 2, oi RE GA 79 MALACOLOGIA, 1990, 32(1): 1 INTRODUCTION John D. Taylor Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, U.K. The families of the Conoidea (= Toxoglo- ssa), namely the Turridae, Conidae, Tere- bridae and Pervicaciidae, are probably a monophyletic group, which share the autapo- morphy of possessing a venom gland and muscular bulb (presumed lost in some taxa). As is well known, many taxa also have highly modified, radular teeth which may be used singly at the proboscis tip for the hypodermic injection of venom. The relationships of the Conoidea to other prosobranch gastropods are uncertain, with some characters suggest- ing a relationship with the Neogastropoda, whilst others indicate a separate derivation from the mesogastropods. The four families differ greatly in the state of current knowledge. Much attention has been given to the species-level taxonomy of the Conidae, but the description of putative new species continues unabated. Far more is known about the biology and ecology of Co- nus than any other toxoglossan group, includ- ing details of their feeding, habitats and repro- duction. However, apart from the radula and the venom apparatus, there have been few anatomical studies, and there is no under- standing of relationships amongst the species groups or clades of Conus. For the Terebridae, there has been a recent taxonomic monograph, but little is known of the anatomy and biology of the family. Rela- tionships both within the family and with the other conoideans are uncertain. The anatom- ical data available suggest a lack of congru- ence between shell and anatomical charac- ters. Controversy surrounds the status of the Pervicaciidae, first proposed by Rudman for terebrid-like gastropods with solid radular teeth and no venom apparatus. The Turridae are an immensely diverse family with daunting taxonomic problems at all levels, with at least fifteen subfamilies in current use. The biology of only a few species is known in any detail, and the limited amount of anatomical work suggests an amazing di- versity of foregut structures within the family. These anatomical characters have yet to be incorporated into any phylogenetic analysis or classification. Further understanding of the origin and evolution of the toxoglossan feed- ing mechanism clearly depends upon further anatomical studies of more turrid species. It is clear from this brief summary that further progress in understanding the evolu- tion of the Conoidea depends upon a much more detailed knowledge of relationships, both within and between the conoidean fam- ilies. Shell characters have proved to be gen- erally unsatisfactory in determining relation- ships and much more attention needs to be given to the analysis of anatomical char- acters. In both the Turridae and Terebridae there are many examples of gastropods with similar shells having quite different internal anatomies. Concurrent studies on biology and feeding behaviour are essential to any understanding of the functional significance of both anatomical and shell characters. Addi- tionally, studies of larval development, partic- ularly in the Turridae and Conidae, are con- tributing data of both systematic and biogeographical importance. There has recently been an upsurge of in- terest in the systematics and evolution of tox- oglossan gastropods, and the objectives of the Tubingen Symposium were to bring together workers specializing in different groups and aspects of the Conoidea, to review present research, and to highlight areas of importance and interest for the future. Six of the nine pa- pers presented at the Symposium are pub- lished here. м MALACOLOGIA, 1990, 32(1): 3-18 ANATOMICAL BASIS FOR THE ORIGIN AND EVOLUTION OF THE TOXOGLOSSAN MODE OF FEEDING Yuri |. Kantor A.N.Severtzov Institute of Animal Evolutionary Morphology and Ecology, Academy of Sciences of the USSR, Leninski Prospekt 33, Moscow 117071, USSR ABSTRACT Five types of feeding mechanism can be recognized in the Toxoglossa. The mechanism by which separate marginal teeth are used at the proboscis tip for stabbing and poisoning the prey with secretions from the venom gland originated in “lower” turrids possessing a radular mem- brane, solid marginal teeth, a central tooth and sometimes lateral teeth. The morphological prerequisite of the appearance of toxoglossan mode of feeding was firstly the appearance of the venom gland, which initiated the formation of the specialized intraembolic type of proboscis with the buccal mass situated at its base. Hollow marginal teeth originated repeatedly and indepen- dently in different phylogenetic lineages of Toxoglossa. It is supposed that the ancestors of Toxoglossa were primitive mesogastropods with a short acrembolic proboscis and taenioglos- san radula. The separation of Toxoglossa from the Rachiglossa occurred at an early evolution- ary stage, when the common ancestor had seven radular teeth in each transverse row. Key words: Toxoglossa, evoiution, feeding, radula. INTRODUCTION The order Toxoglossa is large, diverse, and well differentiated from the other prosobranch gastropods. It includes four Recent families: Turridae, Conidae, Pervicaciidae, and Tere- bridae. One of the most outstanding and well- known features of the order is the specialized feeding mechanism of its higher representa- tives. That is the use of separate hollow mar- ginal teeth at the proboscis tip for stabbing and subsequent poisoning the prey, with the venom produced by a usually well-developed, tubular venom gland. Most representatives of the order (the “higher” Turridae, Conidae and part of the Terebridae) lack the radula mem- brane, and the radula itself consists of only hollow marginal teeth. The teeth being formed in the radula sheath are finally stored in the short arm of the radula sac, which is probably a homologue of the sublingual pouch. At the same time, many toxoglossans (mainly “lower” turrids) have a normally de- veloped radular membrane with two to five radular teeth per transverse row. Information on feeding mechanisms and the morphology of these “lower” toxoglossans is very limited, although the functional analysis of their diges- tive system and feeding mechanism may elu- cidate the pathways of origin and evolution of “toxoglossan” mode of feeding. One of the most interesting problems is the origin of “toxoglossan” feeding mechanism. Does it have a single or repeated origin in evolution, and what are the morphological prerequisites for its appearance? The main aim of this study was to clarify these prob- lems. MATERIALS AND METHODS Materials for the study were obtained mainly from the collections of the Zoological Museum of Moscow State University and In- stitute of Oceanology of the USSR Academy of Sciences (Moscow). Other material was kindly provided by Dr. James H. McLean (Los Angeles County Museum of Natural History, USA); the late Dr. Virginia O. Maes (Academy of Natural Sciences, Philadelphia, USA); Dr. Anders Warén (Naturhistoriska Riksmuseet, Sweden); and Dr. В. N. Kilburn (Natal Mu- seum, South Africa). The morphology of the digestive tract was studied using sections 8-10 pm thick, which were cut after dehydration and embedding in paraffin wax. The sections were usually stained with Masson’s triple stain. Its second solution, which contains orange-G and aniline blue, was used for staining the radula. Large specimens were also dissected under the ste- reomicroscope. In total, the morphology of 18 species of Turridae belonging to six subfam- ilies was studied. 4 KANTOR RESULTS AND DISCUSSION Within the Toxoglossa there is significant variability both in the morphology of the rad- ular teeth and their number in a transverse row (the radular formulae: 1-1-1-1-1, 1-0-1- 0-1, 1-1-0-1-1, 1-0-0-0-1). The morphological changes in the radular apparatus and associ- ated structures of the anterior digestive sys- tem form the main evolutionary trends of the order. Several authors have tried to classify the radular types of Toxoglossa according to both the morphology and probable mecha- nism of function (Thiele, 1929; Powell, 1966; Morrison, 1966; McLean, 1971). The most complex classification was proposed by Shimek & Kohn (1981), who isolated six func- tional types of toxoglossan radula, four of which are found in lower “non-toxoglossate” turrids (those with solid marginal teeth). How- ever, one can Say that only two general feed- ing mechanisms include all the isolated types: “toxoglossate” for those gastropods which have only hollow marginal teeth and lack a radular membrane, and “non-toxoglossate” for lower turrids. In the first feeding type, sep- arate, hollow marginal teeth are used at the proboscis tip for stabbing and poisoning the prey; in the second type, the radula is used as a whole organ only within the buccal cavity. In their analysis, Shimek & Kohn (1981) used mainly isolated radulae, without taking into account the morphology of the digestive tract, and this led to some misinterpretation (Sy- soev & Kantor, 1987). A functional morphological analysis of the digestive system of the species studied sug- gests that there are at least four different types of feeding mechanism for toxoglossans possessing a radula and one type for radula- less species. General Anatomy of Toxoglossa Before a more detailed analysis of the feed- ing mechanism, a brief description of the an- terior part of the digestive system of the Tox- oglossa is necessary. One of the outstanding features of the order is the specialized in- traembolic type of proboscis (Smith, 1967), which is characterized by the position of the buccal mass at the base of the proboscis or even behind it. This precludes the use of the radula as a whole organ for rasping and graz- ing, as in other gastropods. The second fea- ture is the presence of the well-developed tu- bular venom gland entering the anterior oesophagus behind the buccal cavity. It has been shown that the venom gland produces a venom that immobilizes or kills prey animals (Kline, 1956; Pearce, 1966; Miller, 1980; Shimek & Kohn, 1981; Kohn, 1956, 1959, 1968, many others). The buccal tube leads from the buccal cavity to the mouth, which opens at the proboscis tip. The buccal tube has thick muscular walls in “lower” toxoglos- sans, but is thin-walled and practically lacking muscular fibres in higher representatives. It should be noted that the functional anal- ysis was Carried out mainly using the anatom- ical evidence, because data on feeding be- haviour and diet are scarce and chiefly concern species of Conidae, Terebridae and some higher Turridae. As our knowledge of the morphology of turrids becomes more pre- cise, the proposed classification may change. Feeding Mechanism Type 1 The first functional type of digestive system and feeding mechanism, that in which the radula is used as a whole organ only within the buccal cavity, was found among species of Pseudomelatominae (Turridae). This is an endemic subfamily from central west Amer- ica, which includes three genera and several species (McLean, in Keen, 1971). The anat- omy of two species—Pseudomelatoma peni- cillata (Carpenter, 1864) and Hormospira maculosa (Sowerby, 1834)—indicates the isolated position of the group among the Tox- oglossa (Kantor, 1988). This is obvious, in particular, from the presence of long curve of the anterior part of the digestive tract, a rarely found and undoubtedly secondary feature in turrids. The curve is formed either by elonga- tion of the part of the oesophagus between the nerve ring and the buccal mass (in Pseudomelatoma penicillata (Fig. 1), the buc- cal mass is situated at the proboscis base and far ahead of the nerve ring) or by the elonga- tion of the posterior part of the buccal tube (in Hormospira maculosa, the buccal mass is sit- uated in front of the nerve ring, distant from the proboscis base). Both species have a well-developed venom gland, longer in H. maculosa (its length com- prises 0.5 of the shell height). Although the diet of Pseudomelatominae is unknown, the presence of the large venom gland testifies to predatory mode of feeding. The gastropods have a muscular proboscis with a wide oral opening in the form of triangular or transverse slit and lack an oral sphincter. The radula of EVOLUTION OF TOXOGLOSSAN FEEDING 5 00 <> а AC COF COCA» ES == X= Ws S N <= \ AN dine Ц И NN FIG. 1. Anatomy of Pseudomelatoma penicillata (Carpenter). A—semidiagrammatic longitudinal section of the anterior part of the molluscan body. Salivary glands with the duct and convolutions of the venom gland together with the nerve ring are not shown. B, C—organs of the body haemocoel (B: from the left, C: from above). Pseudomelatominae consists of a large and well-developed central tooth, flanked by large, sharply pointed, scythe-like marginal teeth. Thus, although the morphology of the marginal teeth is primitive, the absence of lateral teeth indicates that the group has deviated greatly from the toxoglossan ances- tor. From the morphology of the digestive tract, one can suggest that prey capture probably occurs with the aid of the proboscis tip and is facilitated by the presence of a wide and highly extensible oral opening. The enveno- mation of the prey probably occurs in the an- terior part of the proboscis, and this facilitates the transportation of the prey through the buccal tube into the buccal cavity by the peri- staltic movements of well-developed circular muscles in walls of the buccal tube. The pres- ence of a very large odontophore (the largest of all the turrids studied) suggests that the radula tears the prey in the buccal cavity. Thus, the radula of Pseudomelatominae is of the slicing-rasping type as determined by Shimek & Kohn (1981). The large inner vol- ume of the buccal cavity and the curve of the anterior part of the digestive tract suggests that the prey is partially digested in the ante- rior part of the digestive tract. In summary, the main features of this feed- ing mechanism are: prey capture with the aid of the proboscis tip, without using marginal teeth (since the oral opening lacks a sphincter and the shape of the marginal teeth prevents their being held at the proboscis tip); use of the large and powerful radula for slicing and rasping the prey; and, what is probably a sec- ondary feature, at least partial digestion of the prey in the anterior part of the digestive tract. This feeding mechanism is the true “non-tox- oglossate” and was probably characteristic of ancestors of the Toxoglossa. In my opinion, it is widespread among turrids, and occurs probably in the Clavinae and other taxa lack- ing an oral sphincter (for example, Clavatula diadema), although digestion of the prey in the anterior part of the digestive system is uncertain. 6 KANTOR г er ES à RTE rt a we FIG. 2. Morphology of the digestive system of Aforia spp. A—C: Aforia abyssalis Sysoev et Kantor (A— semidiagrammatic section of the anterior part of the digestive system; B—magnified tip of the proboscis; C—radula); D—magnified tip of the proboscis of Aforia kupriyanovi Sysoev et Kantor. Feeding Mechanism Type 2 The second functional type of digestive system is found in some turrids with a well- developed radular membrane (subfamilies Turriculinae, Clavinae) (Sysoev & Kantor, 1987, 1989). Its typical feature is the use of marginal teeth, which become detached from the radular membrane during its degeneration (in the sublingual pouch), at the proboscis tip for stabbing the prey. Meanwhile, the radula as a whole organ has a different function in the buccal cavity. This type of feeding mech- anism can be probably found amongst spe- cies of almost all subfamilies of Turridae, ex- cept the Pseudomelatominae, Zonulispirinae and probably the Clavatulinae. Since turrids belonging to this type have varied anatomies, it is difficult to distinguish morphological features common to all repre- sentatives of the group. For the species stud- ied (Aforia spp., Antiplanes spp., Splendrillia chathamensis Sysoev & Kantor, 1989) the fol- lowing features can be noted: a large or me- dium-sized odontophore, with well-developed radular muscles; a sac-like enlargement of the anterior part of the buccal tube; and a well-developed oral sphincter. Individual solid marginal teeth were found at the proboscis tip, either held by the oral sphincter as in Aforia (Fig. 2 B,D), or attached by their bases to the “mat” of epithelial cells in the enlargement of the buccal tube as in Splendrillia chathamensis (Fig. 3B). It should be noted that separate teeth were not found in the sublingual pouch. This seems to indicate that the marginal teeth are not used at the proboscis tip of Aforia in every feeding act. On the contrary, the mechanism of tooth fixation in Splendrillia testifies to the long-term occur- rence of the tooth at the proboscis tip, i.e. the enlargement of the anterior part of the buccal tube may be considered as a functional ana- logue of the short arm of the radular sac. EVOLUTION OF TOXOGLOSSAN FEEDING ih === == == = LER > DD S 2500220 QS == Cu FIG. 3. Anatomy of Splendrillia chatamensis Sysoev & Kantor. A—semidiagrammatic longitudinal section of the anterior part of molluscan body; B—magnified tip of the proboscis. Transportation of teeth to the proboscis tip in Aforia may occur with the flow of venom dur- ing contraction of the muscular bulb or also by peristaltic movements of circular muscle fi- bres of the buccal tube. Splendrillia chatha- mensis has an additional, well-developed sphincter in the middle part of the buccal tube (Fig. 3A, spt), which probably takes part in the transportation of the tooth. The marginal tooth is detached from the membrane and is pushed into the buccal cavity by the contract- ing walls of the buccal sac. The tooth length is about 1/3-1/4 of the contracted proboscis length. During the contraction of the proximal part of the proboscis, the tooth becomes held by the additional sphincter. When the distal part of the proboscis contracts, the tooth is passed into the oral sphincter. The function of the radula as a whole organ within the buccal cavity is most probably for the transport of food from the cavity to the oesophagus. This may be confirmed, in par- ticular, by the observations of Maes (1981), who noted the presence of intact sipunculans in the posterior part of the oesophagus of Dril- lia cydia (Bartsch, 1943) (Clavinae), although the large, pectinate lateral teeth might at first sight be thought to serve for tearing or rasping the prey. The use of marginal teeth at the proboscis tip in turrids with a well-developed radular membrane is probably a widespread phe- nomenon amongst the Turridae. This may ex- plain the origin of hollow marginal teeth in different groups possessing the radular mem- brane and odontophore. For example, /ma- clava (Clavinae), most probably also uses the teeth at the proboscis tip for stabbing the prey in a way similar to higher toxoglossans. In summary, the main features of this feed- ing mechanism are: the detachment of mar- ginal teeth from the radular membrane during its degeneration; transportation of the teeth to the proboscis tip; and their use for damaging and poisoning the prey with the venom. A fea- ture of the proboscis is the sac-like enlarge- ment of the anterior part of the buccal tube, with the sphincter holding the base or the mid- dle part of the tooth. The function of the radula as a whole organ is mainly for the transport of the food from the buccal cavity to the oesoph- agus, although in some turrids it may be used also for tearing and rasping. This could be confirmed by the investigation of the prey ob- 00 KANTOR = о Ge SS 37 o : m TRY à x IE \ FIG. 4. Morphology of the digestive system of Toxiclionella tumida (Sowerby). A—semidiagrammatic lon- gitudinal section of the anterior part of the digestive system. The convolution of the venom gland and posterior part of the radular sac are not shown, the arrow indicates the entrance of the venom gland in the oesophagus; B—marginal tooth; C—the tip of the tooth, enlarged. tained from the buccal cavity and anterior oe- sophagus. Thus, the slicing, slicing-rasping, and slicing-stabbing types of radula described by Shimek & Kohn (1981) belong principally to the same functional type, which may be named “stabbing-transporting” type. Feeding Mechanism Type 3 The third feeding mechanism has been found so far only in a single species of Tur- ridae, Toxiclionella tumida (Sowerby, 1870) (Clavatulinae), although it probably exists in other species of this endemic south African genus. A feature of the morphology of the di- gestive system is the position of the buccal mass, with the odontophore near the probos- cis tip (Fig. 4A). The oral sphincter is absent. The gastropod has a well-developed, long venom gland and an unpaired salivary gland with paired ducts, which is situated in the pos- terior part of the proboscis. The radula con- sists only of hollow, marginal teeth which are morphologically similar to the teeth of higher turrids (Fig. 4B,C); a radular membrane is present. The teeth are sufficiently long (the tooth, at the same scale, is figured above the proboscis on Fig. 4) that during protraction of the odontophore the tips would protrude through the oral opening. This leads to the conclusion that the mollusc uses the radula as a whole organ for stabbing the prey. The main difference of this mechanism from all others in which a marginal tooth is used for stabbing and poisoning the prey, is that the radula is used as a whole organ, not as separate teeth. It is possible that a similar mechanism occurs in Turricula nelliae spurius (Hedley, 1922) (Taylor, 1985), which has a similar proboscis morphology. Feeding Mechanism Type 4 The fourth feeding mechanism was found in higher toxoglossans that lack a radular membrane, i.e. higher Turridae, Conidae and some Terebridae. The main feature of the mechanism is the use of individual, hollow marginal teeth at the proboscis tip for stab- bing the prey, and the completely reduced function of the radula as a whole organ within the buccal cavity. The feeding and the diet of EVOLUTION OF TOXOGLOSSAN FEEDING 9 at Sa ran IZ < Е CES ES mom <4 yee Bina Ч igre A «НЕЕ < So, EL SS > San FIG. 5. Anatomy of Teretiopsis abyssalis Kantor & Sysoev. A—semidiagrammatic longitudinal section of the anterior part of the molluscan body; B—enlarged part of the section through the body wall and rhyn- chodaeum. species with this functional type is well known, and it is unnecessary to describe it in detail. Only the most important morphological features should be noted. These are the ves- tigial, or completely reduced, radular mem- brane; the absence of an odontophore; the presence of the short arm of the radular sac, where the fully formed marginal teeth are stored; and a well-developed, oral sphincter for tooth fixation. The radula is represented only by hollow marginal teeth, with the most specialized and complex morphology found within the prosobranchs. The tooth ligament (long flexible stalk attached to the tooth base) is probably the rudiment of the radular mem- brane. Amongst molluscs of this functional group, the enlarged rhynchostomal lips ap- peared. In some species, the lips are able to invert (i.e. to form a pseudoproboscis) and this is used in prey capture. It should be noted that in some representatives of the group— some vermivorous species of Conus (Marsh, 1970) and C. geographus L., 1758 (Johnson & Stablum, 1971)—stabbing is not a neces- sary part of each feeding act. Judging from the morphology of the diges- tive system, Zonulispirinae occupy an inter- mediate position between the gastropods of the second and the fourth functional groups. They have hollow marginal teeth, attached to a rather strong radular membrane. This may indicate that separate teeth are used at the proboscis tip. Moreover, the gastropods have very small odontophore (Maes, 1983); this in- dicates that the function of the radula as a whole organ within the buccal cavity is prob- ably rudimentary. Feeding Mechanism Type 5 The fifth and last functional type is found among those Toxoglossa lacking a radula. Gastropods of this group belong to higher Turridae (according to the shell morphology) and some Terebridae. The most important features are: a reduced or completely absent proboscis; and absence of a radular sac, and venom and salivary glands. Most representa- tives of this group have either well-developed rhynchostomal lips or a large pseudoprobos- cis (Terebridae—Miller, 1975; Philbertia lin- earls (Montagu), Turridae—Sheridan et al., 1973). Some turrids (Cenodagreutes spp.— Smith, 1967; Abyssobella atoxica Kantor & Sysoev—Kantor & Sysoev, 1986; Teretiopsis spp.—Kantor & Sysoev, 1989), lacking a pseudoproboscis, have a vast rhynchocoel and have developed a cavity between the rhynchodaeum and body walls, which are connected by numerous muscles in the cavity 10 KANTOR (Fig. 5). Species of the genus Taranis lack both a pseudoproboscis and a cavity. The feeding mechanism is known for tere- brids (Miller, 1970, 1975). Thus, species with a relatively short pseudoproboscis feed on the enteropneust Ptychodera flava, and spe- cies with a long pseudoproboscis feed on polychaetes. The capture and engulfment of the prey occurs with the aid of the pseudopro- boscis. Turrids lacking a pseudoproboscis, but with a cavity between the rhynchodaeum and the body walls, probably engulf the prey with the aid of negative pressure, which arises in the rhynchocoel during contraction of the radial muscle fibres (at that moment the inner volume of the rhynchocoel increases). It is difficult at present to say anything certain about the feeding mechanism of Taranis. The feeding of such aberrant groups as Strictispirinae (Turridae) is unclear. These gastropods lack a venom gland and have a very large odontophore. According to the fig- ure of Maes (1983), Strictispira paxillus (Reeve, 1845) has a short buccal tube. Thus, there is a possibility that it can protrude the radula through the mouth opening and use it pincer-like, tearing off small pieces of food. Origin of the Toxoglossan Mode of Feeding In my opinion, the development of the unique “toxoglossan” mode of feeding is con- nected with certain morphological prerequi- sites. These were the appearance of the venom gland and the intraembolic type of the proboscis. The mobile proboscis, which in the con- tracted state is situated in the special cavity of the body haemocoel, or proboscis-like struc- tures (for exampie, the extrovert formed by the walls of the buccal cavity in Janthinidae— Graham, 1965) appeared independently in different groups of marine predatory gastro- pods. The presence of the proboscis allows an increase in the mobility of the buccal mass, and this is achieved by its shift from the ven- tral side of the head (as in herbivorous gas- tropods) in the terminal (axial) position. This also allows “distant” feeding, i.e. to feed on prey hidden in burrows, crevices, etc., and also on animals with external skeletons, for example on bivalves (inserting the proboscis between the open valves or through a drilled hole). Usually three types of proboscis are de- fined: acrembolic, pleurembolic, and intraem- bolic, these are differentiated by the position of the buccal mass and the mode of eversion. Only the latter two types are found among Neogastropoda. In gastropods with the pleu- rembolic proboscis, the buccal mass with rad- ular sac is situated near the proboscis tip, and proboscis eversion occurs with the aid of the posterior invaginable part of the rhyn- chodaeum (wall of the proboscis sheath or rhynchocoel). In many neogastropods with this proboscis type, the entire or nearly entire rhynchodaeum takes part in proboscis ever- sion. On the contrary, in gastropods with the intraembolic proboscis, the buccal mass is sit- uated at the proboscis base or even behind it (Pseudomelatoma penicillata, Turridae—Fig. 1), the invaginable part of the rhynchodaeum is absent, and the proboscis eversion results only from its stretching. Recently, a proboscis somewhat intermediate between the typical pleurembolic and intraembolic types was de- scribed in Turricula nelliae spurius (Taylor, 1985) and Toxiclionella tumida (herein). In these gastropods, the buccal mass is situated near the proboscis tip, and the rhynchodaeum is capable of partial eversion. Usually, the Neogastropoda are considered as a monophyletic group (Ponder, 1973; Tay- lor & Morris, 1988). On the other hand, doubts on the monophyletic origin of neogastropods were expressed by Golikov & Starobogatov (1975), with moreover the Toxoglossa (sensu Golikov & Starobogatov who included Mitroi- dea along with Conoidea and Terebroidea in the order) were separated from the rest. The problem of the ancestral group is also essen- tial to the argument. Ponder (1973) consid- ered that the Neogastropoda originated from archaeogastropods or primitive mesogastro- pods. Thus, the proboscis of neogastropods in general and of Toxoglossa in particular should be considered as de novo structure. Taylor & Morris (1988), on the contrary, sug- gested the possibility of the origin of Neogas- tropoda from higher, advanced Mesogas- tropoda and their proboscides thus should be homologous with the pleurembolic proboscis of predatory Mesogastropoda. Finally, Sheri- dan et al. (1973) stated that the intraembolic type of the proboscis originated from the acrembolic type. For more careful consideration of the ques- tion some comments on the morphology of the buccal muscles are necessary. In archaeogastropods and primitive meso- gastropods lacking a proboscis, there are nu- merous buccal muscles that are connected to the columellar and pedal muscles. On the EVOLUTION OF TOXOGLOSSAN FEEDING 11 contrary, in Mesogastropoda and Neogas- tropoda with a developed pleurembolic pro- boscis, the buccal muscles have lost such a connection and are attached to the proboscis walls (Graham, 1973; herein). In a species of Clavinae, which are considered to be the least-derived Toxoglossans, there is such a connection of supramedian, radular tensor and columellar muscles (Fig. 3A). In my opin- ion, this undoubtedly confirms the original basal position of the buccal mass in Clavinae. In the opposite case, the connection of the buccal and columellar muscles would be lost. Thus, one can state that the intraembolic pro- boscis has evolved independently from the pleurembolic type and not from the latter (by the shift of the buccal mass to the proboscis base) and that the origin of Toxoglossa and all Neogastropoda in general (if they are consid- ered as a monophyletic group) from higher probosciferous mesogastropods is improba- ble. Proboscides of different groups of Neo- gastropoda probably appeared indepen- dently, and the detailed morphological studies of some poorly Known groups would corrobo- rate this supposition. The appearance of the intraembolic pro- boscis in Toxoglossa may be connected with appearance and development of the venom gland. It is very likely that toxoglossan ances- tors were carnivorous gastropods with a short acrembolic proboscis. The acrembolic pro- boscis is found among various primitive gas- tropods (for example, Naticidae, Triphoridae, Cerithiopsidae) and principally may be con- sidered as an elongated buccal tube that has an ability to evert through the mouth opening as a glove finger. In the inverted position, the buccal mass is situated at the base of the proboscis, while in an everted position it is located at the proboscis tip (Fig. 6 A). During proboscis eversion the oesophagus is pulled through the nerve ring. The elongation of the acrembolic proboscis allows gastropods to feed on animals hidden in deep burrows, crevices or tubes, for exam- ple on polychaetes. At the same time, the elongation of the proboscis limits the size of the oesophageal glands, which have to be pulled through the nerve ring during eversion. It could be suggested that at early evolu- tionary stages, these gastropods started to use the secretion produced by the dorsal glandular folds of the oesophagus and squirted through the mouth for immobilization of the prey. This simplified the capture and swallowing of actively moving prey. After the appearance of such feeding mechanism, the proboscis may have elongated by the devel- opment of a tube in front of the mouth open- ing, which was situated in the sheath formed by the walls of introvert of the acrembolic pro- boscis (Fig. 7B). The main function of the pro- boscis was not to move the buccal mass for- ward, but to form the tube through which the venom reaches the prey. Such elongation of the proboscis appears closely related to the enlargement of the dor- sal oesophageal folds; as the inner volume of the proboscis grew, more venom was neces- sary to fill it. Gradually the glandular folds stripped off from the oesophagus and formed a tube, i.e. the venom gland. In the initial stages of the formation of the new proboscis type, the introvert was probably able to evert, but the enlarged size of the venom gland pre- vented its being pulled through the nerve ring. Finally, this caused fixation of the buccal mass in front of the nerve ring at the probos- cis base, and the introvert ceased to evert. At that moment, the newly formed proboscis possessed all features of the intraembolic type (Fig. 6C). The functions of the radula were the same as in other gastropods (tearing and rasping the prey and its transportation to the oesophagus), but it acted only within the buccal cavity. If this proposed scheme of origin of the in- traembolic proboscis is accepted, then one can suppose that the rhynchodaeum is a ho- mologue of the introvert wall of the acrembolic proboscis and the proboscis itself is de novo structure that is not homologous with the pleurembolic proboscis of other neogastro- pods. The discovery of a mechanism by which individual solid marginal teeth are used at the proboscis tip in turrids with a well-developed radular membrane, allows us to reconstruct the development of the typical “toxoglossan” mode of feeding. In the process of radula growth, anterior (the oldest) rows of teeth are detached from the radular membrane, which in turn degenerates in the sublingual pouch. It is reasonable to suppose that some detached teeth are not removed through the digestive tract (as usually occurs in gastropods) but are somehow transported to the proboscis tip where they are used for damaging the prey integument. This intensifies the efficiency of venom action. Fixation of such a mechanism in evolution created the prerequisites and ne- cessity of the appearance of hollow marginal teeth. This was an important stage in toxo- 12 FIG. 6. А scheme for the origin and evolution of the proboscis of Toxoglossa. The dotted arrows indicate thetical connections. The hypothetical morphological stage is given on the dotted background. A— p; B—intermediate morphological stage between the acrembolic and intraembolic proboscis types; C—the basal type of the intraembolic proboscis; D— tomal lips; E—reduction of the proboscis, radula and venom and salivary glands; F—origin of pseudopro- boscis: G—reduction of the proboscis, radula and venom and salivary glands; H—displacement of the buccal mass toward the proboscis tip and formation of the curve of the digestive tract; I—formation of the hypo acrembolic proboscis of the ancestral grou KANTOR marginal teeth =, PQ > prr “BR radial folds at the proboscis base. origin of rhynchos- EVOLUTION OF TOXOGLOSSAN FEEDING 13 ГУ a a Go A cm m u N 40000 __ 0.05 mm | pr B FIG. 7. The anatomy of Benthobia n.sp. A—semidiagrammatic longitudinal section of the anterior part of the molluscan body; B—radula. glossan evolution. As the mechanism of prey stabbing and poisoning by the teeth at the proboscis tip improved, the functions of the radula as a whole organ within the buccal cavity became less and less important. This finally led to reduction of the odontophore, central and lateral teeth, and as a final stage, the radular membrane. Up until now the intraembolic proboscis has been found only amongst Toxoglossa. How- ever, a similar proboscis type was found by the author in a species of the family Pseudo- lividae (Fig. 7), Benthobia n.sp. The buccal mass in this species is situated at the probos- cis base; moreover, there is a connection of the buccal muscles with the columellar mus- 14 KANTOR cle (this confirms the primary position of the buccal mass, see above). This gastropod also has a very large gland of Leiblein. According to Ponder (1973), the venom gland of the Toxoglossa and the gland of Leiblein were formed independently, but in similar way, by the stripping off of the glandular folds from the oesophagus. Thus, one can state that Pseudolividae and Toxoglossa are not related groups, and the similar proboscis type ap- peared independently. The radular morphol- ogy of Benthobia (Fig. 7B) (very similar to Olividae), as well as details of the morphology of the anterior part of the digestive tract, indi- cates that the marginal teeth are not used at the proboscis tip by Benthobia. Thus, the de- velopment of the venom gland rather than the position of the buccal mass at the proboscis base, was the main factor conditioning the ap- pearance of “toxoglossan” mode of feeding in evolution. The origin of hollow marginal teeth took place repeatedly and independently in differ- ent phylogenetic lineages of Toxoglossa. Hol- low marginal teeth appeared at least twice among turrids, simultaneously with the reten- tion of the radular membrane and the central and sometimes lateral teeth. Radulae of this type are found among /maclava unimaculata (Sowerby, 1843) (Clavinae) (Shimek & Kohn, 1981) and Toxiclionella elstoni (Barnard, 1962) (Clavatulinae) (Kilburn, 1985). The main trends of subsequent evolution of the Toxoglossa are variable and character- ized by morphological changes in the anterior part of the digestive system. Thus, three main pathways of the morphological evolution of the proboscis may be defined. Some Toxo- glossa have circular folds formed by the pro- boscis in the contracted state (Fig. 61). This reduces the length of the contracted probos- cis, and probably simplifies the transportation of the individual marginal teeth from the rad- ular sac to the proboscis tip. The second lineage is connected with ori- gin and development of the mobile rhyncho- stomal lips, which take part in the prey cap- ture (Fig. 6D). The progressive development of lips into an introvert results in the pseudoproboscis (Fig. 6F) of some turrids and most Terebridae. The action of prey cap- ture gradually transferred from the proboscis to the rhynchostomal lips or pseudoprobos- cis, and this finally led to the complete reduc- tion of the true proboscis (Fig. 6E, G). The process is evolutionarily connected with the complete reduction of the radula, venom and salivary glands, a process that occurred inde- pendently in different phylogenetic lineages. Finally, the third, less studied trend is con- nected with the shift of the buccal mass to- ward the proboscis tip. Also the rhyn- chodaeum secondarily evolved the capability of partial eversion (this was made possible by the elongation of the oesophagus between the buccal mass and the nerve ring and for- mation of the curve of the oesophagus, as it takes place in Rachiglossa). The tendency is best seen in Turricula nelliae spurius (Turri- culinae) and Toxiclionella tumida (Clavatuli- nae). An intermediate morphological stage is found in Clavatula diadema (Kiener, 1840) (Fig. 8), in which the buccal mass is situated inside the proboscis nearer to its base, and the rhynchodaeum is capable of partial eversion. The presence of two consecutive morphological stages in the same subfamily confirms the secondary character of this ev- olutionary lineage. In conclusion, one more question should be discussed, the resolution of which may shed light on the ancestral group of Neogastropoda and Toxoglossa. Usually, the radula of Clav- inae (Turridae), with a central tooth, flanked by pairs of lateral and marginal teeth, is con- sidered as a plesiomorphic condition in neo- gastropods (Taylor & Morris, 1988). In pectini- branchiate gastropods, the radula is folded lengthways in the radular sac. The folds in the gastropods with differentiated groups of teeth are situated between the marginal and lateral teeth and between the lateral and central teeth. Thus, in gastropods with marginal and lateral teeth, there are two pairs of folds. A similar condition is observed in Olivella, ex- cept for the Clavinae, the only genus of neo- gastropods which has five teeth in a trans- verse row (Fig. 9A). Nevertheless, the clavine radula has only one pair of folds, which are situated between the central and lateral teeth (Fig. 9B). Species of the genus Antiplanes have the central formations which were con- sidered as a reduced central tooth. Investiga- tions of the radula indicate that it has only one fold (Fig. 9C). This may indicate that tradi- tional interpretation of the radular teeth of Clavinae is wrong and their radula is formed by central and two pairs of marginal teeth, which have become greatly differentiated in evolution. In Antiplanes, the central tooth is possibly completely reduced, and the central formations are the rudiments of the inner pair of the marginal teeth. Thus, one can suppose that the toxoglossan EVOLUTION OF TOXOGLOSSAN FEEDING ll, 9) PUES = = NUNG, N 55 | BS ER VE BONEN a“ pp QU ALA AS | FE N TE TER y) ES RIRE GG fe q = Ti = 2 PE) US od PO sd Le VW, wen > - A q ( = nn ce UNES) O a AR, ыы FIG. 8. The anatomy of Clavatula diadema (Kiener). A—semidiagrammatic longitudinal section of the an- terior part of the moliuscan body; B—magnified base part of the proboscis. 16 KANTOR FIG. 9. The radular folding in different Neogastropoda. At the left—the shape of radular teeth, at the right—diagrammatic transverse section of the radula sheath. A—Olivella; B—Splendrillia (Clavinae); C— Antiplanes (Turriculinae). radula originated from the taenioglossan (2- ular formula of Clavinae should be 2-0-1-0-2, 1-1-1-2) by the reduction of true lateral teeth of Antiplanes, 2-0-0-0-2.) On the contrary, in and differentiation of the marginals. (The rad- Olivella the radula is formed by the rudiments EVOLUTION OF TOXOGLOSSAN FEEDING 7 of the marginal teeth, Бу a pair of laterals and a central, i.e. it originated from the taenio- glossan by a reduction of the pair of marginal teeth (formula: 1-1-1-1-1). The present hy- pothesis supposes that if the Neogastropoda is a monophyletic group, their ancestor had the taenioglossan radula, and the derivation of Rachiglossa and Toxoglossa occurred at an early stage, when the ancestor had seven teeth per transverse row. CONCLUSIONS (1) The evolution of Toxoglossa as a sep- arate taxon was connected with the origin and development of the venom gland. The devel- opment of the venom gland determined the appearance of the specialized intraembolic type of proboscis and the specific “toxoglos- зап” mode of feeding. (2) The ancestors of Toxoglossa were probably lower mesogastropods with a short acrembolic proboscis and taenioglossan rad- ula. (3) In higher Toxoglossa, the specific “tox- oglossan” mode of feeding, using separate, hollow marginal teeth at the proboscis tip, has Originated repeatedly and independently in the Turridae. A similar feeding mechanism with the use of solid marginal teeth at the pro- boscis tip in some lower turrids with a well- developed radular membrane and odonto- phore may be considered as the intermediate evolutionary stage. (4) In “higher” Toxoglossa with well-devel- oped rhynchostomal lips or with a pseudopro- boscis, a decrease of the proboscis size usu- ally occurs and this leads finally to the complete reduction of the radula, venom and salivary glands. ABBREVIATIONS asg—accessory Salivary gland; bc—buccal cavity; bm—buccal mass; bt—buccal tube; cm—columellar muscle; cu—cuticle; ерт— “mat” of epithelial cells; gf—glandular folds of the oesophagus; m—buccal muscle, con- nected to the columellar muscle; mb—mus- cular bulb of the venom gland; nr—nerve ring; od—odontophore; oe—oesophagus; pg— venom gland; pr—proboscis; prr—proboscis retractor muscles; ps—proboscis sphincter; pw—proboscis wall; r—radula; rd—rhyn- chodaeum; rm—radial muscles, connecting the rhynchodaeum and the body wall; rs— radular sac; rt—marginal tooth, held at the proboscis tip; sd—salivary duct; sg—salivary gland; slp—sublingual pouch; spt—intermedi- ate sphincter of the buccal tube; sr—rhyncho- stomal sphincter. ACKNOWLEDGEMENTS The author is greatly indebted to Dmitri Ivanov, Zoological Museum of Moscow State University, James H. McLean (Los Angeles County Museum of Natural History), Anders Waren (Naturhistoriska Riksmuseet), and R. N. Kilburn (Natal Museum) who kindly pro- vided materials for the study, and to Dr. Alex- ander Sysoev for his valuable comments on the manuscript. LITERATURE CITED GOLIKOV, А.М. & У.1. STAROBOGATOV. 1975. Systematics of prosobranch gastropods. Malaco- logia, 15: 185—232. GRAHAM, A., 1965, The buccal mass of janthinid prosobranchs. Proceedings of the Malacological Society of London, 36: 323-338. GRAHAM, A., 1973, The anatomical basis of func- tion in the buccal mass of prosobranch and am- phineuran molluscs. Journal of Zoology, London, 169: 317-348. JOHNSON, C. R. & W. STABLUM, 1971, Observa- tions on the feeding behaviour of Conus geogra- phus (Gastropoda: Toxoglossa). Pacific Science, 25: 109-111. KANTOR, Yu. 1., 1988, On the anatomy of Pseudomelatominae (Gastropoda, Toxoglossa, Turridae) with notes on functional morphology and phylogeny of the subfamily. Apex, 3: 1-19. KANTOR, Yu. I. & A. V. SYSOEV, 1986, A new genus and new species from the family Turridae (Gastropoda, Toxoglossa) in the northern part of the Pacific Ocean. Zoologicheskij Zhurnal, 65: 485—498. (In Russian). KANTOR, Yu. | 8 А. V. SYSOEV, 1989, On the morphology of toxoglossan gastropods lacking a radula, with a description of new species and ge- nus of Turridae. Journal of Molluscan Studies, 55: 537—549. KILBURN, В. N., 1985, Turridae (Mollusca: Gas- tropoda) of southern Africa and Mozambique. Part 2. Subfamily Clavatulinae. Annals of Natal Museum, 26: 417—470. KLINE, P., 1956, Notes on the stinging operation of Conus. Nautilus, 69: 76-78. KOHN, A. J., 1956, Piscivorous gastropods of the genus Conus. Proceedings of the National Acad- emy of Sciences, 42: 168-171. 18 KANTOR KOHN, A. J., 1959, The ecology of Conus in Ha- май. Ecological Monographs, 29: 47-90. KOHN, А. J., 1968, Microhabitats, abundance and food of Conus on atoll reefs in the Maldive and Chagos Islands. Ecology, 49: 1046-1061. MAES, V. O., 1983, Observations on the systemat- ics and biology of a turrid assemblage in the Brit- ish Virgin Islands. Bulletin of Marine Sciences, 33: 305-335. MARSH, H., 1970, Preliminary studies of the ven- oms of some vermivorous Conidae. Toxicon, 8: 271-277. McLEAN, J. H., 1971, A revised classification of the family Turridae, with the proposal of new subfam- ilies, genera, and subgenera from the eastern Pacific. Veliger, 14: 114-130. McLEAN, J. N., 1971, Family Turridae. In KEEN, А. M. Sea shells of tropical West America; marine molluscs from Baja California to Peru. Second ed. Stanford: Stanford University Press, pp. 686— 766. MILLER, B. A., 1970, Studies on the biology of some Indo-Pacific Terebridae. Ph. D. thesis, Uni- versity of New Hampshire, Dover, 213 pp. MILLER, B. A., 1975, The biology of Terebra gouldi Deshayes and a discussion of life history similar- ities among other terebrids of similar proboscis type. Pacific Science, 29: 227-241. MILLER, В. A., 1980, The biology of Hastula incon- stans (Hinds, 1844) and a discussion of life his- tory similarities among other hastulas of similar proboscis type. Pacific Science, 33: 289-306. MORRISON, J. P. E., 1966, On the families of Tur- ridae. Annual Report of the American Malacolog- ical Union for 1965: 1-2. PEARCE, J. B., 1966, On Lora treveliana (Turton) (Gastropoda: Turridae). Ophelia, 3: 81-91. PONDER, W. F., 1973, Origin and evolution of the Neogastropoda. Malacologia, 12: 295-338. POWELL, A. W. B., 1966, The molluscan families Speightiidae and Turridae. An evaluation of the valid taxa, both Recent and fossil, with lists of characteristic species. Bulletin of the Auckland Institute and Museum, 5: 184 pp. SHERIDAN, R., J.-J. VAN MOL & J. BOUILLON, 1973, Etude morphologique du tube digestif de quelques Turridae de la région de Roscoff. Cah- ¡ers de Biologie Marine, 14: 159-188. SHIMEK, R. L. & A. J. KOHN, 1981, Functional morphology and evolution of the toxoglossan radula. Malacologia, 20: 423—438. SMITH, E. N., 1967, The proboscis and oesopha- gus of some British turrids. Transactions of the Royal Society of Edinburgh, 67: 1-22. SYSOEV, А. V. 8 Yu. I. КАМТОВ, 1987, Deep-sea gastropods of the genus Aforia (Turridae) of the Pacific: species composition, systematics, and functional morphology of the digestive system. Veliger, 30: 105-126. SYSOEV, A. V. & Yu. |. KANTOR, 1989, Anatomy of molluscs of genus Splendrillia (Gastropoda: Toxoglossa: Turridae) with description of two new bathyal species of the genus from New Zealand. New Zealand Journal of Zoology, 16: 205-214. TAYLOR, J. D., 1985, The anterior alimentary sys- tem and diet of Turricula nelliae spurius (Gas- tropoda: Turridae). In: MORTON, B. & D. DUD- GEON, eds., Proceedings of the Second International Workshop on the Malacofauna of Hong Kong and Southern China, Hong Kong 1983, Hong Kong University Press, pp. 175-190. TAYLOR, J. D. & N. J. MORRIS, 1988, Relation- ships of neogastropods. Malacological Review, Supplement 4: 167-179. THIELE, J., 1929 [-1931], Handbuch der system- atischen Weichtierkunde. Jena, Gustav Fischer, 1929—1935: 1154 pp. Revised Ms. accepted 21 June 1990 MALACOLOGIA, 1990, 32(1): 19-34 THE ANATOMY OF THE FOREGUT AND RELATIONSHIPS IN THE TEREBRIDAE John D. Taylor Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom ABSTRACT A study of foregut anatomy in the gastropod family Terebridae shows that two major groups of species are represented. Members of one group have hypodermic radular teeth, venom apparatus and an extensible buccal tube. Terebrids of the second group have a very short buccal tube, a radula consisting of two rows of solid, curved teeth and no venom apparatus. Furthermore, there are many terebrid species lacking a radula, venom apparatus and buccal tube and these could be derived from either group. It is suggested that the two groups of Terebridae were derived independently from the Tur- ridae, and each group should be given family status. This study confirms Rudmans's (1969) proposal of the family Pervicaciidae for Terebra tristis, and the family should now be extended to include perhaps all species of Duplicaria and a number of species currently referred to Terebra. Key words: Terebridae, anatomy, feeding, functional morphology, radula. INTRODUCTION The Terebridae is a family of conoidean gastropods characterised by high-spired, multiwhorled shells with relatively small aper- tures. There are about 300 living species which inhabit soft-substrate habitats at tropi- cal and sub-tropical latitudes (Bratcher & Cer- nohorsky, 1987). The family is particularly di- verse and abundant in shallow-water sandy habitats of Indo-Pacific coral reefs (Miller, 1970; Taylor, 1986). The biology of Tere- bridae has been little studied and not only is little Known about relationships within the family, but the relationship of terebrids with other conoideans is also obscure. Anatomical work on the Terebridae has been very limited. Details of individual spe- cies have been described by Risbec (1953), Marcus & Marcus (1960), Rudman (1969), Auffenberg & Lee (1988), and Taylor & Miller (1990). By far the most significant studies were by Miller (1970, 1971, 1975, 1979). As a result of these studies, Miller (1970, 1971) proposed a classification of proboscis types within the family Terebridae which he thought represented natural groupings, although he made no attempt to examine relationships within the family. Miller (1970, 1971) recognised three main proboscis types amongst the species he stud- ied. They are briefly defined as follows: 19 Type la species have a long, extensible la- bial tube or introvert, a short buccal tube, no radula, a pair of salivary glands, and no venom gland or muscular bulb. Type Ib species are simliar to type la in foregut anatomy, but have a very long labial tube, which is folded upon itself when re- tracted into the rhynchodeal cavity. Type lla species have a medium length la- bial tube, a long proboscis and buccal tube, a pair of fused salivary glands, а radula sac and caecum, with hollow hypodermic radular teeth, a large venom gland and muscular bulb. Type ИБ species are similar, but the buccal tube is shorter and the rhynchodeum may be partitioned by a septum. Type Ш species have a labial tube of me- dium length, a very short or no buccal tube, salivary glands are vestigial or absent, and there is no radular or venom apparatus. A fea- ture of this group of species is the presence of a club-shaped accessory feeding organ at- tached to the left wall of the rhynchodeal cav- ity. Since Miller's scheme was published, the anatomy of a number of terebrid species has been described that do not fit into the classi- fication, and it is clear that some reappraisal is necessary. Furthermore, the recent mono- graph by Bratcher & Cernohorsky (1987) has highlighted the inconsistencies and problems in the classification of the family, with apparent 20 TAYLOR incongruence between the anatomy and the shell characters used in the generic divi- sions. Apart from a phenetic study of Miocene species (Davoli, 1977), there have been no previous attempts to establish phylogenetic relationships within the Terebridae, and only very generalised comments on the relation- ship of the terebrids with other toxoglossans. Because a number of terebrid species pos- sess the toxoglossan feeding apparatus of hypodermic radular teeth, venom gland, and muscular bulb, the relationship with the fam- ilies Turridae and Conidae has long been es- tablished. However, many terebrid species lack a radular and venom apparatus, and the structures are presumed to have been evolu- tionarily lost. The Terebridae are usually as- sumed to have been derived from the Tur- ridae, although details of this relationship are obscure. Powell (1966, fig. 1) suggested, pre- sumably following Cossmann, 1896), a deri- vation from the turrid subfamily Clavatulinae, probably based upon the superficial similari- ties of the smooth, rather elongated shells of Pusionella with some terebrids. Because of the general uniformity of shell morphology, the Terebridae have been as- sumed to be monophyletic. The only serious dissenter from this view is Rudman (1969), who described the anatomy of the New Zealand and southern Australian species Pervicacia tristis (Deshayes, 1859) (Terebra tristis in Bratcher & Cernohorsky, 1987). This species has a radula consisting of two rows of short, solid and slightly curved marginal teeth and an odontophore, but lacks a venom ap- paratus. Rudman considered the species suf- ficiently distinct from other terebrids to justify the erection of a new family, the Pervicaci- idae, which he thought was derived from the Turridae independently from the rest of the terebrids. The latter together with the Conidae were derived from the Turridae after the evo- lution of the hypodermic type of radular teeth. Subsequently, other authors (Ponder, 1973; Bratcher & Cernohorsky, 1987) have consid- ered that the characters of Т. tristis fall within the range of other Terebridae and that the separation as a separate family was not jus- tified. The objectives of this paper are to review what is known of foregut anatomy in the Tere- bridae, and to examine the use of these an- atomical characters in determining relation- ships both within the family and with other conoideans. MATERIALS AND METHODS The basic data for this study were obtained from dissections and serial sections of the foregut made from 18 species of Terebridae. These are listed below, nomenclature follow- ing Bratcher & Cernohorsky, 1987, which for convenience is also followed throughout the paper: Hastula aciculina (Lamarck, 1822); H. albula Menke, 1843; H. bacillus (Deshayes, 1859); H. hectica (Linnaeus, 1758); H. sal- leana (Deshayes, 1859); H. solida (De- shayes, 1857); Terebra affinis Gray, 1834; T. babylonia Lamarck, 1822; T. capensis Smith, 1873; T. cerithina Lamarck, 1822; T. dimidiata (Linnaeus, 1758), T. funiculata Hinds, 1844; T. maculata Linnaeus, 1758; T. nassoides Hinds, 1844; Т. subulata (Linnaeus, 1758); T. tristis Deshayes, 1844; Duplicaria duplicata (Linnaeus, 1758); D. spectabilis (Hinds, 1844). REVIEW OF FOREGUT ANATOMY This section consists of brief descriptions of the major features of the foregut anatomy of a number of terebrid species chosen to repre- sent the variety of form so far known in the family. Further details of some of the species can be found in the publications cited. Hastula cinerea (Born, 1778), H. galleana, and H. inconstans (Hinds, 1844) (see Marcus & Marcus, 1960; Miller, 1979; Taylor, unpub.) These three species have a similar anat- omy and are characteristic of Miller's type Па foregut and of most other Hastula species. All three species have a short- to medium-length labial tube, a long buccal tube which can ex- tend outside the rhynchodeum, a radular sac and caecum with hollow, hypodermic radular teeth, a pair of salivary glands, and a well- developed venom gland and muscular bulb. Hastula hectica has a basically similar anatomy, but the labial tube is longer. The most interesting feature of this species is in the structure of the radular teeth. The large barbed and hollow radular teeth have an ap- parently unique feature. The mid-section of the tooth is formed of a network structure rather like chicken-wire (Figs. 1c, 2). The tooth is hollow but has a well-developed ori- fice near the tip which in other toxoglossans is where the venom emerges on penetration of the prey. The function of the perforated mid- section of the tooth is not known but may al- ANATOMY OF TEREBRIDAE 21 FIG. 1. Single radular teeth of a. Hastula bacillus x95; b. Terebra babylonia x217; с. Hastula hectica x718. low the delivery of venom along the full length of the tooth rather than just at the tip. Terebra imitatrix Auffenberg & Lee, 1988 This recently described species has a shell morphology very similar to species of the Hastula cinerea group but differs in anatomy. T. imitatrix has a large, spoon-shaped labial tube; a large, club-shaped accessory probos- cis structure with two rows of papillae on the ventral side; a very short buccal tube which probably cannot be extended out of the mouth of the rhynchodeum; a relatively short venom gland and a small muscular bulb. There is a radular sac and a caecum with rather elon- gate, slightly curved, barbless teeth. No sali- vary glands were located by the authors. Auffenberg & Lee (1988) were puzzled by the combination of characters in this species and for this reason hesitated to include it in the genus Hastula. The shell and much of the anatomy resembles that of other Hastula spe- cies, but the presence of the large accessory proboscis structure they thought to be a fea- h FIG. 2. Detail of mid-section of the middle shaft of the radular tooth of Hastula hectica. Scale bar 10 um. ture usually restricted to terebrids with Miller's Type Ill proboscis. However, species in this latter group lack a buccal tube, radular appa- ratus, salivary glands, venom gland, and muscular bulb. Hastula bacillus (see Taylor & Miller, 1990) This small species was found abundantly on the surf beaches of the western side of Phuket Island, Thailand. There is a short, ex- tensible labial tube, a long extensible buccal tube, and a large, muscular, branched acces- sory proboscis structure (aps), which is an- chored to the left wall of the rhynchodeum (Fig. 3). The aps can be extended some dis- tance out of the rhynchodeum, but when re- tracted is bent into an “s” shape within the cavity. Entering the buccal cavity is a radular sac, without a caecum. A small odontophore is present, and the radula consists of teeth that are scroll-like at the base but taper into a pointed barb-less, knife-like, blade at the tip (Fig. 1a). There is a pair of salivary glands and a single (right) accessory salivary gland. The venom gland is large, with a well-devel- oped muscular bulb. S.E.M. studies of the accessory proboscis structure show that regularly spaced tufts of short, stiff cilia are distributed over the suface. Associated with each tuft are pairs or triplets 22 TAYLOR aps FIG. 3. Dissection of the head of Hastula bacillus showing the extended accessory proboscis structure and extended labial tube. The buccal tube is retracted into the rhynchodeal cavity but can be extended beyond the mouth of the cavity. apm, accessory proboscis retractor muscles; aps, accessory proboscis structure; asg, accessory salivary gland; bc, buccal cavity; bt, buccal tube; m, mouth; mb, muscular bulb; ое, oesophagus; pm, proboscis retractor muscles; rs, radular sac; rw, rhynchodeal wall; vg, venom gland. ANATOMY OF TEREBRIDAE 23 FIG. 4. Branch of the accessory proboscis structure of Hastula bacillus showing the ciliary tufts with pairs and triplets of domes. SEM of critical point dried material. Scale bar 10 рт. FIG. 5. Detail of a ciliary tuft, showing short stiff cilia and the accompanying microvilli-covered domes. Scale bar 1 um. of microvilli-covered domes (Figs. 4, 5). The ciliary tufts are similar to those seen on the pallial or cephalic tentacles of other molluscs and which are thought to be either chemo- or mechanosensory in function. Because Has- tula bacillus lives in a wave-disturbed habitat, Taylor & Miller (1990) suggested that the ac- cessory proboscis structure was more likely to be chemosensory in function and used in finding the preferred prey of Scolepis, a spio- nid polycheate. Although similar in basic anatomy to Has- tula cinerea, H. bacillus shows a number of important differences. The presence of the odontophore and accessory salivary glands are plesiomorphic characters. The radular teeth are much simpler than the hollow, barbed, hypodermic teeth of H. cinerea. Ad- ditionally, the branched accessory proboscis structure is a unique feature, but almost cer- tainly homologous with the club-shaped struc- ture in Terebra imitatrix and T. affinis. Prior to its discovery in H. bacillus and T. imitatrix, the accessory proboscis structure was consid- ered an advanced character, found only in species with Miller's type Ш proboscis. Terebra subulata Along with T. babylonia and T. guttata, this species has a long multiwhorled shell of more than 18 whorls. These species have an anat- omy typical of Miller's type ПБ. Terebra subu- lata has a labial tube introvert; a long buccal tube; a septum dividing the rhynchodeal cav- ity (Fig. 13); a short radular sac; a radular caecum; long, thin, hypodermic radular teeth, with small barbs and a constricted neck near the base of the tooth (Fig. 12f); a pair of sal- ivary glands; a pair of accessory salivary glands (Fig. 6); and a large venom gland and muscular bulb. Terebra maculata (see Miller, 1970) This species possesses Miller's type Ib fo- regut. It has a very long labial tube introvert which is coiled within the rhynchodeal cavity (Fig. 13); a short buccal tube; a pair of sali- vary glands; no radula and no venom appa- ratus. Terebra gouldi Deshayes, 1857 (see Miller, 1975) This species which represents Miller's type la foregut has a medium length labial tube introvert; a very short buccal tube; a pair of salivary glands, with no radula or venom ap- paratus. 24 TAYLOR asg 2mm rs Sg FIG. 6. Main organs of the buccal mass of Terebra subulata. asg, accessory salivary glands; c, radular caecum; oe, oesophagus; rs, radular sac; sd, salivary duct; sg, salivary gland; vd, venom duct. Terebra affinis (see Miller, 1970) This species represents Miller's Type Ш foregut. It possesses a long labial tube intro- vert; no buccal tube; no salivary glands; no radula or venom apparatus. Arising from the left wall of the rhynchodeum is the accessory proboscis structure (Fig. 13), an extensible muscular stalk, with a mace-like, papillate head. Duplicaria spectabilis and D. duplicaria Both of these species lack eyes and ceph- alic tentacles. They possess a long labial tube introvert, but the buccal tube is extremely short (Figs. 7, 8). The buccal cavity is large, and opening into it is a small radular sac, with an odontophore with a radular ribbon consist- ing of two rows of solid, sickle-shaped radular teeth (Fig. 9). Salivary ducts from a pair of salivary glands open either side of where the radular sac joins the buccal cavity. There is no venom gland or muscular bulb. Terebra nassoides This is a Small species collected from inter- tidal sand patches in Oman. The anatomy is basically similar to that of the above Dupli- caria species. It has no eyes or cephalic ten- tacles. The labial tube is hood-shaped, the dorsal part being much larger than the ven- tral. The buccal tube is very short, and there is a small odontophore (Fig. 11) and short rad- ular ribbon with two rows of curved, solid teeth (Fig. 10). There are no salivary glands and no venom apparatus. Terebra tristis The anatomy of this New Zealand-southern Australian species was described by Rudman (1969) as Pervicacia tristis. There are no eyes ANATOMY OF TEREBRIDAE 25 oe FIG. 7. Longitudinal section through the extended labial tube and buccal mass of Duplicaria spectabilis. m, mouth; od, odontophore; oe, oesophagus; rc, rhynchodeal cavity; rd, radula; rm, mouth of rhynchodeum; rw, rhynchodeal wall; sm, sphincter muscle; sg, salivary gland. or tentacles. The dorsal part of the labial tube extends anteriorly over the ventral surface, forming a hood. Rudman stated that the labial tube appeared incapable of withdrawal, but sections of preserved specimens | have stud- ied show that both dorsal and ventral parts of the labial tube can be folded back into the rhynchodeum. The buccal tube is very short. There is a radula ribbon and odontophore with two rows of solid, slightly curved radular teeth. There is a pair of fused salivary glands, and two salivary ducts enter the buccal cavity. There is no venom apparatus. REVIEW OF FOREGUT CHARACTERS In this section | review the distribution and variation in the main organs of the foregut amongst the terebrid species for which the anatomy is known. Labial tube The possession of an extensible labial tube (introvert formed by the extension of the walls of the rhynchodeum) is perhaps characteristic of all species of the Terebridae. This charac- ter is not confined to the terebrids, but is found in some turrids (subfamily Daphnelli- nae) which have a polyembolic proboscis, such as Philbertia linearis (Sheridan et al., 1973) and Cenodagruetes (Smith, 1967). There are some differences in the form of the labial tube which may be important. In Te- rebra tristis and T. nassoides, the dorsal part of the tube is much larger than the ventral and when extended appears hood-like (Rudman 1967, Taylor, unpub. observ.). The ventral part of the tube in T. nassoides probably does not retract. Other variation mainly concerns the length of the tube. In those species having a long buccal tube and hypodermic radula, the labial tube is relatively short. However, in those forms with a short buccal tube and also lack- ing a radula, the labial tube is much longer, and in Terebra maculata and similar species the labial tube, when withdrawn, is folded on itself several times within the rhynchodeal cavity (Miller, 1970). In his account of feeding in Terebra gouldi, Miller (1975) has shown how this species, which lacks a radula and venom apparatus, and has only a very short buccal tube, uses the extensible labial tube to capture the en- teropneust Ptychodera and transfer the prey to the short buccal tube. Similarly, the long labial tube of T. maculata probes in the sand for the capitellid polychaete Dasybranchus. 26 TAYLOR 4 ) 28 y AVB era, q SY 4 RE a = IR a ef go 2 И 0, ee 3 as у Я i y — ZE Y LANA O =. NR АВ fe NE ] I iff || YA р Ir == fr) i \ ‘ZS = RN: 7///] в | == А | | yl AU l:. NIV N 19 E BAY А ae > Nf SS WR \ 84 === А \ YA A IIS — lH \ @ 9 _ \ 4 A GADEA + | |8 | | CE, = Pre GS) NN GER Te > / — \ | и. LAW ee Sty CAN SALA ‘ a YA rl AN \ NS i SE = brm FIG. 8. Section through the buccal mass of Duplicaria spectabilis showing the short, muscular, buccal tube, the odontophore and radular sac. brm, buccal retractor muscle, bt, buccal tube; iwr, inner wall of rhyncho- deum; m, mouth; od odontophore; odc odontophoral cartilage; ps, proboscis sheath; rdt, radular tooth; rs radular sac; sd, salivary duct. Buccal Tube radula teeth. During the feeding process sin- gle teeth are transferred from the radular cae- The buccal tube or true proboscis is long cum to the tip of the buccal tube, where they only in those species with hollow, hypodermic are gripped by the sphincter muscle (e.g. Has- ANATOMY OF TEREBRIDAE 27 FIG. 9. Disaggregated radular teeth of Duplicaria spectabilis. Scale bar 20 um. FIG. 10. Side view of part of row of radular teeth of Terebra nassoides. Scale bar 20 um. FIG. 11. Section through the odontophore of Tere- bra nassoides showing the pair of odontophoral cartilages. SEM of critical point dried material. Scale bar 30 um. tula inconstans; Miller, 1979). In these spe- cies, the proboscis wall is muscular and is capable of being extended well beyond the rhynchodeal cavity. Although they did not ob- serve any living animals, Auffenberg & Lee (1988) thought that the short, but muscular, buccal tube of Terebra imitatrix could not be extended out of the rhynchodeal cavity. Those terebrid species with solid radula teeth fixed on a ribbon have only a very short buccal tube (Fig. 13). This also applies to those species that have completely lost the radular apparatus. Accessory Proboscis Structure Miller (1970) described in Terebra affinis a retractile, club-shaped structure, which he called the accessory feeding organ. (Taylor & Miller [1990] prefer the functionally neutral term of accessory proboscis structure.) This consists of a muscular stalk with a distal papil- late head that is attached at the base to the posterior left side of the wall of the rhyn- chodeal cavity. This structure occurs in spe- cies otherwise lacking a buccal tube, radula, salivary glands and venom apparatus. Miller thought, but without direct observations, that the organ was involved in prey capture. The possession of the accessory proboscis structure is a major character defining Miller's Type III foregut. Miller (1970) mentioned, but did not illustrate, a number of other terebrids as having an aps. Recently, an accessory proboscis structure was described from two other terebrid spe- cies, Hastula bacillus (by Taylor & Miller, 28 TAYLOR 1990) and Terebra imitatrix (by Auffenberg & Lee, 1988). These species otherwise possess an extensible buccal tube, hypodermic radu- lar teeth, salivary glands and venom appara- tus. The anatomy is similar to other Hastula species and the Type На foregut of Miller (1970, 1971). Hastula bacillus has a long, branching aps, but in 7. imitatrix it is club shaped. Both muscular structures are at- tached to the left side of the rhynchodeal cav- ity and are probably homologous with the structure in Terebra affinis. As shown in Figures 4 and 5, the aps in Hastula bacillus possesses numerous ciliary tufts which T.E.M. analysis suggests are sen- sory, probably chemosensory, structures. Be- cause H. bacillus and T. imitatrix both have a long functional buccal tube (true proboscis) it seems more likely that the aps is a sensory device, rather than part of the food-gathering apparatus. However, the fine structure of the aps in 7. affinis and T. imitatrix has not been investigated. Nevertheless, it is now clear that the possession of an aps is not an autapo- morphy of terebrids having the Type Ill foregut, but it can occur in terebrids, which compared with the outgroups in the Turrridae (Miller, 1989), are the least derived for the family. Radula There are basically two main types of rad- ula found in the Terebridae: (1) radulas of solid, sickle or dagger-shaped teeth; (2) rad- ulas of hollow, harpoon-like hypodermic teeth. Additionally, there are many terebrid species that have no radular apparatus at all. Relatively few radulae of the solid-toothed variety have been described. Figures 9 and 10 illustrate the radula in two species, which are basically similar in morphology. The rad- ula consists of two rows of marginal teeth at- tached to the short radular ribbon. In all spe- cies there is an odontophore with two odontophoral cartilages (Fig. 11). In Terebra nassoides and T. tristis the teeth are solid, broader at the base and curved; in Duplicaria spectabilis and D. duplicaria they are sickle shaped. Additionally, teeth like those in T. tris- tis are found in Duplicaria kieneri and D. fictilis from South Australia (radula mounts in BM(NH)). Troschel (1866) illustrates an un- usual radula for Myurella lamarckii Kiener (= Duplicaria lamarckii, considered by Bratcher & Cernohorsky, 1987, as a form of D. dupli- cata). This has long sickle-shaped teeth as in D. duplicata, but with spur-like projections near the distal end of each tooth. | examined the radula of D. lamarcki from Kenya but found the teeth to be simple, with no sign of the spur-like cusps. The solid, sickle-shaped marginal teeth of these terebrids resemble those found in some turrids, particularly from the subfamily Pseudomelatominae (e.g. Tiariturris libya (Dall, 1919), Shimek & Kohn, 1981, fig. 2; Pseudomelatoma penicillata (Carpenter, 1864), Kantor, 1988, fig. 1D-F). However, these turrids also have a large, unicuspid cen- tral tooth. The marginal teeth are erected into a basket structure as the radular passes over the bending plane. Shimek & Kohn (1981) thought that the central tooth functions as a slicing tooth and that the marginal teeth lac- erate the prey, tearing off fragments and con- veying them to the oesophagus. Amongst those species having the hollow hypodermic teeth, there is some variety of form (Figs. 1, 12). Both the simplest and most complex forms are those of some Hastula species. In Hastula bacillus the teeth are rolled and hollow, but the anterior half con- sists of a knife-like blade. In Hastula cinerea, H. penicillata and H. salleana the teeth are robust with a harpoon-like, barbed tip, a large aperture near the tip and a broad base with a flared rim (Marcus & Marcus, 1960; Bandel, 1984). An additional feature of the teeth in these three species is the presence of “screw-thread”-like flanges separating the rolls of the tooth (Fig. 12). Bandel (1984) sug- gested that these flanges gave rigidity to the tooth by separating the rolls. Essentially sim- ilar teeth are seen in T. taurinus and T. pro- texta (Bandel, 1984, figs. 313, 314). The teeth of Hastula hectica with the perforated mid- section are apparently unique. In Terebra subulata, T. guttata, T. succinea, and T. anilis, the radula teeth are long and thin, with pointed tips and small barbs (Mills, 1977a; Bandel, 1984; personal observations). Those of Terebra babylonia are similar but lack the barbed tips (Fig. 1). Additionally, all these lat- ter species have a marked concavity near the base of the tooth produced by twisting of the tooth (Fig. 1b). Of the species with the hypo- dermic teeth, Hastula bacillus and H. acicu- lina are the only species so far found with an albeit small odontophore and odontophoral cartilages. In Hastula bacillus and H. aciculina, the radular sac is relatively long and there is no radular caecum for the storage of detached ANATOMY OF TEREBRIDAE 29 e f g h FIG. 12. Range of form found in the hypodermic-type radula teeth of Terebridae. Traced from original scanning electron micrographs or from references cited. a. Hastula bacillus, Thailand; b. H. cinerea Colom- bia (Bandel, 1984); c. H. hectica Kenya; d. Terebra protexta Colombia (Bandel, 1984); e. T. babylonia Guam; f. T. subulata Maldives; д. T. guttata Queensland (Mills, 1977a); h. T. taurinus Colombia (Bandel, 1984); i. T. succinea Queensland (Mills, 1977a). Not to scale. radular teeth. In other species (e.g. Hastula cinerea and H. inconstans), the radular sac is shorter and there is a well-developed caecum. In Terebra subulata and T. babylonia the rad- ular sac is very short, with a large caecum. The hollow barbed radular teeth found in some terebrids are similar in form to those found in the Conidae and some turrids (Sub- family Borsoninae) and which are considered to be the most derived type of radula to be found in the Conoidea. A great diversity of radular types is found in the Turridae, and Shimek & Kohn (1981) have developed an adaptive scenario to explain the evolution of the radula, from the primitive condition of five teeth in a row found in some Clavinae, to the advanced hypodermic marginal teeth of the Borsoninae. The main evolutionary elabora- tions concern the marginal teeth and include increasing size and complexity, with con- comitant loss of the central and lateral teeth. Although considerable variation is seen in the radula amongst the various subfamilies of Turridae (Powell, 1966; McLean, 1971; Shi- mek & Kohn, 1981), variation in both the Conidae and Terebridae is relatively small and concerns details of the form of the hypo- dermic teeth. Indeed, variation in the hypo- dermic teeth in the Terebridae is probably no greater than found in one subfamily of Tur- ridae, the Oenopotinae (Bogdanov, 1989). No convincing intermediate condition between the solid teeth and the hypodermic teeth of terebrids has been seen. The teeth in Hastula bacillus, with the hollow, rolled proximal end and the solid, blade-like distal end, might be an intermediate condition or a variant of the hypodermic tooth. Accessory salivary glands Accessory salivary glands are an apomor- phic character of the Neogastropoda and are known in some turrids and some Conus spe- cies (Ponder, 1973; Marsh, 1971; Schultz, 1983). Recently, a single accessory gland was found in Hastula bacillus (Taylor & Miller, 1990), but not in several other Hastula spe- cies examined. Furthermore, dissection and thin sections have also revealed a pair of ac- cessory glands in Terebra subulata (Fig. 6), but only single glands in Terebra babylonia and T. funiculata. Salivary glands A pair of salivary glands is present in most terebrids. The glands are usually partially 30 TAYLOR fused together and appear as two distinct lobes of one mass. Separate salivary ducts enter the buccal cavity at the base of the rad- ula sac, where this is present. Rudman (1969) described an apparently unusual feature of Pervicacia tristis where the salivary ducts fuse, entering the buccal cavity as a single duct. But my observations of serial sections of this species show two ducts entering the buc- cal cavity. Salivary glands and ducts are present in many terebrids where the radula, buccal tube and venom apparatus has been lost. They are however, absent in some of Miller's Туре Ш species, such as Тегебга affinis. Venom apparatus The venom apparatus of venom gland and muscular bulb is an autapomorphic character of the Conoidea (Taylor & Morris, 1988). In the Terebridae it is present only in those spe- cies with hollow, hypodermic radular teeth and a long buccal tube. There is some varia- tion in the length of the venom gland and the size of the muscular bulb. For instance, the venom apparatus is particularly large in Tere- bra subulata (Mills, 1977b). By contrast, Auffenberg & Lee (1988 p. 155) consider that the muscular bulb in Terebra imitatrix “... is weak, seemingly vestigial. . . .”. Mills (19775) reported differences in the secretory epithelia of the venom gland between Terebra and Co- nus, but these need further investigation. Rhynchodeal septum Miller (1970, 1971) briefly mentioned a sep- tum across the rhynchodeal cavity in some terebrids with his Type ИБ proboscis. In Tere- bra subulata, this structure divides the rhyn- chodeal cavity into two compartments. It con- sists of an invagination of the inner wall of the rhynchodeum with a central aperture. When withdrawn, the buccal tube lies to the poste- rior and the labial tube to the anterior of the septum. When extended, the buccal tube passes through the central aperture of the septum. The function of the septum is un- known, but may be concerned with retaining prey that has been pulled into the rhyncho- deum by the buccal tube. GEOLOGICAL HISTORY No adequate analysis has been made of the geological history of the Terebridae. Var- ious authors (Cossmann, 1896, Wenz, 1938; Taylor et al., 1980) have considered, with varying degrees of confidence, the Creta- ceous (Santonian) species “Fusus” cingula- tus Sowerby, from Gosau, Austria, to be an early terebrid (as Strioterebrum). However, the species appears to have an elongate si- phonal canal and is more likely to be a mem- ber of the Turridae. Otherwise, the earliest terebrids appear to be Hastula species from the Eocene of France and England (Coss- mann, 1896). The Terebridae diversified ex- tensively in the Miocene, with the appearance of many of the shell forms seen amongst Re- cent species (Davoli, 1977). DIET OF TEREBRIDAE Most available dietary information for the Terebridae is from the genus Hastula, and nearly all the species investigated seem to feed upon spionid polychaetes. Miller (1979) gives a detailed account of the Hawaiian spe- cies Hastula inconstans, which feeds exclu- sively upon Dispio magna. Also in Hawaii, H. hectica and H. strigillata feed upon Nerinides sp. and H. penicillata upon an unidentified spionid. Marcus & Marcus (1960) report H. cinerea as feeding upon Nerinides agilis, as does H. salleana (Stewart, in Miller, 1979) In Thailand, Hastula bacillus feeds upon Scolepis sp. (Taylor & Miller, 1990). The only exception to the spionid diet of Hastula is H. solida from Guam, which feeds upon a cirrat- ulid polychaete, probably Cirratula sp. (Tay- lor, unpub.). Species with Miller's foregut type ПБ also eat spionids. Miller (1970) reports Terebra textilis from Hawaii as eating Prionospio malmgreni, and from Guam Taylor (1987) re- ports T. cingulifera and T. subulata feeding upon Laonice cirrata. There is little dietary data available for tere- brids with solid radular teeth. Dissection of many Duplicaria spectabilis from Hong Kong revealed no recognisable food remains. The only information available is for Terebra nas- soides from Salalah, Oman, where three in- dividuals contained setae of a capitellid poly- chaete (Taylor, unpub.). Of the terebrids with no radula and venom apparatus, Miller (1975) has described feed- ing in Terebra gouldi, which eats the enterop- neust Ptychodera flava. This diet is shared by Terebra dimidiata, T. crenulata, and T. areo- lata. ANATOMY OF TEREBRIDAE 31 Amongst those species with a very long la- bial tube and no radula or venom apparatus, Terebra felina, T. maculata and T. chlorata all eat the capitellid polychaete Dasybranchus caducus (Miller, 1970, 1975). Finally, the diet of the species with an ac- cessory proboscis structure but no radula and venom apparatus is unknown. The digestive tract of Т. affinis frequently contains amor- phous red-brown material, which Miller (1970) and Taylor (1986) thought might be the bran- chial tentacles of cirratulid polychaetes. DISCUSSION & CONCLUSIONS From the foregoing descriptions it is clear that a wide range of foregut anatomies are present in the Terebridae (Summarized in Fig. 13). There is clearly more complexity to be accounted for than in Miller's (1970, 1971) classification. Furthermore, only a small pro- portion of the nearly 300 living species have been examined anatomically, and the discov- ery of further foregut types is to be expected. In considering the evolutionary relation- ships of the Terebridae, the first question to be asked is whether the family comprises a monophyletic group. Evidence from foregut anatomy suggests that there are two major divisions within the family. Firstly, there is the group of species with solid radular teeth, and a well-developed radular ribbon. These spe- cies have a short buccal tube, lack a venom apparatus and have no cephalic tentacles or eyes. Secondly, there is the group comprising the species possessing radular teeth of the hypodermic type. These species also pos- sess a venom apparatus and elongate buccal tube. Additionally, there are terebrids which lack a radula and venom apparatus and have a very short buccal tube. These species could be derived from one or other of the radulate groups. It is suggested that the two groups of tere- brids represent separate derivations from the Turridae. The group with solid teeth comprise some species classified in the genus Dupli- caria by Bratcher & Cernohorsky (1987), as well as Terebra nassoides, T. capensis and T. tristis, and probably many others. In their analysis of the toxoglossan radula, Shimek & Kohn (1981) considered that the most derived condition was the hypodermic type consisting of long, hollow, barbed mar- ginal teeth with only a vestigial radular mem- brane. The hypodermic radulae of such tere- brids as Hastula cinerea, H. salleana and Terebra subulata are similar to those found in the Conidae and Borsoniinae. However, Has- tula bacillus and H. aciculina have a less de- rived condition, with simpler radular teeth with no barbs, a small odontophore and odonto- phoral cartilages and a more substantial rad- ular membrane. In H. bacillus there is no cae- cum to the radular sac in which teeth can be stored. However, thin sections showed a rad- ular tooth held at the proboscis tip. This is similar to the situation in some turrids, where detached, non-hypodermic, solid marginal teeth are held at the proboscis tip (Sysoev & Kantor, 1987). The knife-like distal portion of the tooth is more likely a stabbing structure, rather than a true hypodermic tooth. The presence of this less-derived radular appara- tus in H. bacillus suggests that the hypoder- mic radulae of the Terebridae and Conidae are parallel but independent developments. Compared to outgroups in the Turridae and Conidae (Miller, 1989), species of the genus Hastula are the least derived for the family. They all possess the basic intraembolic pro- boscis condition, with a long buccal tube, venom apparatus, with in many species a true hypodermic radula. A major variant is seen in Hastula bacillus, which possesses an elon- gate, branching accessory proboscis struc- ture. This may be homologous with the club- shaped structure seen in Terebra imitatrix, which has a reduced buccal tube and a small venom apparatus. Terebra subulata and similar species (Т. guttata, T. babylonia, T. funiculata) have long, thin radular teeth, and shells with many (18 + ) whorls. This group of species can be simply derived from the Hastula condition. Many terebrids, however, lack a radula, venom apparatus and buccal tube, and the foregut provides less useful evidence of rela- tionships. The trend in terebrids for the loss of most of the foregut structures except for the labial tube introvert, results in the condition known as the polyembolic proboscis (Smith, 1967). The whole foregut is essentially sim- plified into a muscular tube that ingests prey. The extensible labial tube becomes the main organ of prey capture and ingestion, the true proboscis having disappeared. This trend is paralleled in the Turridae, where the poly- embolic proboscis occurs in some species of the subfamily Daphnellinae (Smith, 1967; Kantor & Sysoev, 1989). The simplified fore- gut of the terebrids could have been derived via a number of evolutionary routes. Corrob- 32 TAYLOR solid-toothed radula no radula FIG. 13. Diagrammatic representation of the main types of foregut found in the Terebridae, with radular teeth. Key to abbreviations: aps, accessory proboscis structure, asg, accessory salivary gland; rs, radu- lar зас; $, rhynchodeal septum; sg, salivary glands; sm, sphincter muscle at mouth of labial tube; va, venom apparatus. Key to species: a. Duplicaria spectabilis, b. Duplicaria duplicata, c. Hastula cinerea, d. Hastula bacillus, e. Terebra subulata, f. Terebra gouldi and Terebra dimidiata, g. Terebra maculata, h. Terebra affinis. ANATOMY OF TEREBRIDAE 33 orative evidence from other anatomical char- acters is needed to establish the relationships of these terebrids. For example, Terebra gouldi has the simplified foregut structure, but it has the shell characters of the genus Dupli- caria (placed there by Bratcher & Cerno- horsky, 1988) and may conceivably have been derived from the solid-toothed group of tere- brids. By contrast, Т. dimidiata and T. crenu- lata similarly have the simple foregut, but shell characters more like (perhaps superfi- cially) those in the Terebra subulata group of species. The mace-like accessory proboscis struc- ture described from Terebra affinis (Miller, 1970, 1971) occurs in a species that other- wise lacks a buccal tube, radula, venom ap- paratus or salivary glands. It was thought to be an autapomorphic character of Miller's type III proboscis. However, the discovery of prob- ably homologous structures in the otherwise less-derived Hastula bacillus (Taylor & Miller, 1990) and Terebra imitatrix (Auffenberg & Lee, 1988), suggests that this structure could be more widespread amongst the Terebridae. More species of Terebridae need to be ex- amined using more characters before an ad- equate phylogenetic analysis can be made. However, the main conclusion of this paper is that Rudman (1969) was essentially correct in separating the Pervicaciidae as a separate family. What is now clear is that the family should accommodate many more “terebrids,” perhaps all of the Duplicaria species and probably many others, such as Terebra nas- soides, T. capensis, T. kieneri, and T. fictilis. The family Terebridae should accomodate all the species with hypodermic radular teeth and venom apparatus and derivatives from these. The great range of morphology found in the terebrid foregut coupled with the appar- ent incongruence between shell characters and anatomy will make detailed classification of the families difficult. It is clear that shell characters are a poor guide to relationships in the Terebridae. A pressing problem concerns the anatomy, as yet unknown, of the south Australian spe- cies, T. albida Gray, 1834. This is the type species of the genus Acus Gray, 1847, on which the family Acusidae Gray, 1853, is based. If this species turns out to have solid radular teeth and no venom apparatus, then the name Acusidae will have priority over Per- vicaciidae. Additionally, anatomical material is needed of Pervicacia ustulata, the type species of the genus Pervicacia. ACKNOWLEDGEMENTS | am very grateful for the help of David Coo- per who made the sections. Kurt Auffenberg, Dick Kilburn, lan Loch, and Bruce Marshall generously donated specimens. Alison Kay, Bill Rudman and Yuri Kantor kindly read and commented on the mansucript. | thank John Miller, David Reid, Noel Morris, and Winston Ponder for useful discussion. LITERATURE CITED AUFFENBERG, K. & H. G. LEE, 1988. A new spe- cies of intertidal Terebra from Brazil. Nautilus, 102: 154—158. BANDEL, К., 1984. The radulae of Caribbean and other Mesogastropoda and Neogastropoda. Zo- ologische Verhandelingen, 214: 1-188. BOGDANOV, J. P., 1989. Morphological transfor- mation in radula and protoconch of Oenopotinae Bogdanov, 1987. La Conchiglia, 21: 237-240. BRATCHER, T. & W. O. CERNOHORSKY, 1987. Living terebras of the world. A monograph of the Recent Terebridae of the world. Melbourne, Flor- ida: American Malacologists Inc. COSSMANN, M., 1896. Essais de Paléoconcholo- gie comparée, 2: 1-179. DAVOLI, F., 1977. Terebridae (Gastropoda). Parte 1-1 Molluschi tortoniani di Montegibbio. Palaeon- tographica ltalica, 70: 135-169. KANTOR, Y. 1., 1988. On the anatomy of the Pseudomelatominae (Gastropoda, Toxoglossa, Turridae) with notes on functional morphology and phylogeny of the family. Apex, 3: 1-19. KANTOR, У. 1. & А. V. SYSOEV, 1989. The тог- phology of toxoglossan gastropods lacking a rad- ula, with a description of a new species and ge- nus of Turridae. Journal of Molluscan Studies, 55: 537-550. MCLEAN, J. H., A revised classification of the fam- ily Turridae, with the proposal of new subfamilies, genera, and subgenera from the eastern Pacific. Veliger 14:114-130. MARCUS, E. & E. Marcus, 1960. On Hastula ci- nerea. Boletim da Faculdade de Filosofia, Cien- cias e Letras. Universidade de Sao Paulo (Zoo- logia), 23:25—66. MARSH, H., 1971. The foregut glands of vermivo- rous cone shells. Australian Journal of Zoology, 19: 313-326. MILLER, B. A., 1970. Studies on the biology of Indo-Pacific Terebridae. Ph.D. Thesis. University of New Hampshire. Durham. 213pp. MILLER, B. A., 1971. Feeding mechanisms of the family Terebridae. Reports of the American Mal- acological Union AMU Pacific Division, 1970: 72-74. MILLER, В. A., 1975. The biology of Terebra gouldi Deshayes, 1859, and a discussion of life history 34 TAYLOR similarities among other terebrids of similar pro- boscis type. Pacific Science, 29: 227-241. MILLER, B. A., 1979. The biology of Hastula incon- stans (Hinds, 1844) and a discussion of life his- tory similarities among other hastulas of similar proboscis type. Pacific Science, 33: 289-306. MILLER, J. A., 1989. The toxoglossan proboscis: structure and function. Journal of Molluscan Studies, 55: 167-182. MILLS, P. M., 1977a. Radular tooth structure in three species of Terebridae. Veliger, 19: 259—265. MILLS, P. M., 1977b. On the venom gland of tere- brid molluscs. Proceedings of the Third Interna- tional Coral Reef Symposium, Miami, Florida: 631-637. PONDER, W. F., 1973. The origin and evolution of the Neogastropoda. Malacologia, 12: 295-338. POWELL, A. W. B., 1966. The molluscan families Speightiidae and Turridae. An evaluation of the valid taxa, both Recent and fossil, with lists of characteristic species. Bulletin of the Auckland Institute and Museum, 5: 1-184. RISBEC, J., 1953. Observations sur l'anatomie du Terebridae Néo-Calédonnais. Bulletin du Mu- seum National d'Histoire Naturelle. Paris, series 2, 25: 576-583. RUDMAN, W. B., 1969. Observations on Pervicacia tristis (Deshayes, 1859) and a comparison with other toxoglossan gastropods. Veliger, 12: 53— 64. SCHULTZ, M. C., 1983. A correlated light and elec- tron microscopic study of the structure and secre- tory activity of the accessory salivary glands of the marine gastropods, Conus flavidus and C. vexillum (Neogastropoda, Conacea). Journal of Morphology, 176: 89-111. SHERIDAN, R., J. J. VAN MOL & J. BOUILLON, 1973. Etude morphologique du tube digestif de quelques Turridae (Mollusca-Gastropoda-Proso- branchia-Toxoglossa) de la region de Roscoff. Cahiers de Biologie Marine, 14: 159-188. SHIMEK, В. 1. & А. J. KOHN, 1981. Functional morphology and evolution of the toxoglossan radula. Malacologia, 20: 423—438. SMITH, E. H., 1967. The proboscis and oesopha- gus of some British turrids. Transactions of the Royal Society of Edinburgh, 67: 1-22. SYSOEV, А. V. & Y. I. КАМТОВ, 1987. Deep-sea gastropods of the genus Aforia (Turridae) of the Pacific: species composition, systematics, and functional morphology of the digestive system. Veliger, 30: 105-126. TAYLOR, J. D., 1986. Diets of sand-living predatory gastropods at Piti Bay, Guam, Asian Marine Bi- ology, 3: 47-58. TAYLOR, J. D. & J. A. MILLER, 1990. A new type of gastropod proboscis; the fore-gut of Hastula bacillus (Deshayes) (Gastropoda: Terebridae). Journal of Zoology, 220: 603-617. TAYLOR, J. D. & N. J. MORRIS, 1988. Relation- ships of neogastropods. Malacological Review, Supplement 4: 167—179. TROSCHEL, Е. Н. 1866. Das Gebiss der Schnecken zur Begrundung einer naturlichen Classification, vol.2 Nicolai, Berlin. WENZ, W. 1938—1944. Gastropoda. Allegemeiner Teil und Prosobranchia. Handbuch der Paläozo- ologie, 6, part 1, 1639 pp. Revised Ms. accepted 21 June 1990 MALACOLOGIA, 1990, 32(1): 35-54 ONTOGENETIC CHANGE IN THE CONUS RADULA, ITS FORM, DISTRIBUTION AMONG THE RADULA TYPES, AND SIGNIFICANCE IN SYSTEMATICS AND ECOLOGY James Nybakken Moss Landing Marine Laboratories; Post Office Box 450; Moss Landing, California, U.S.A. 95039 ABSTRACT The radula teeth of some species of the carnivorous genus Conus undergo a morphological change during their ontogeny. This change is documented for four species in two feeding categories. The form of change differs in the different feeding types, but the initial juvenile tooth appears similar in all. The change from juvenile to adult tooth appears to occur quickly and presumably results from the initiation of the activity of the superior epithelial tissue. Not all species of Conus show an ontogenetic change in the radula tooth. For those species showing a change, however, there is a correlation of tooth morphology and diet that suggests a close coupling of the two. It is suggested that ontogenetic change in morphology will occur in those species in which there is a marked change in the diet between juveniles and the adult, but not in those in which the prey does not change. Key words: Conus, radula, ontogeny, diet, evolution. INTRODUCTION The radula morphology of prosobranch gastropods is known to show a certain amount of morphological variability within a species (Bandel, 1974; Borkowski, 1975; Car- riker, 1943; Cernohorsky, 1970; Houbrick, 1978; Howe, 1930; Merriman, 1967; Rosewa- ter, 1970). Such variability has been most of- ten reported for adult animals and has been occasionally correlated with sex (Arakawa, 1958, 1959; Maes, 1966; Robertson, 1971). Reports of the occurrence of morphological change in gastropod radular teeth during on- togeny have been less frequent. Reported on- togenetic changes in prosobranch and opisthobranch gastropods have included in- creases in number of teeth per row (Bertsch, 1976; Robertson, 1985) and alterations in the morphology of single teeth in a given row (Carriker, 1943; Fujioka, 1985; Hickman, 1980; Hollister, 1954; Page 4 Willan, 1988; Thompson & Brown, 1984). Despite these studies, until recently there do not appear to have been any studies that follow ontogenetic changes within a species from post-metamor- phic juveniles to adults to ascertain when and how rapidly the changes occur, and to try to ascertain the reason for the changes. Ontogenetic change in the radula of Conus 35 magus was reported by Nybakken & Perron (1988), and a second suspected case in Co- nus patricius was reported by Nybakken (1988). Rolan (1986) has also reported a dif- ference in radula tooth structure between ju- venile and adults of C. ermineus. Two of the three species for which ontoge- netic change has been demonstrated in Co- nus, C. magus, and C. ermineus, are pisci- vores in which the juvenile is too small to consume fish. Hence it is probably not unex- pected that the radula tooth morphology should change with change in diet as Nybak- ken & Perron (1988) have demonstrated for C. magus. However, the finding of a change in tooth morphology in a vermivore, С. patri- cius, suggests that ontogenetic change might be more widespread within the genus. This, coupled with the knowledge that the different radula types in Conus can be associated with certain diets (Lim, 1969; Nybakken, 1970), led me to embark on a study of the radula tooth morphology within a broad size range of Conus species representing as many of the different tooth types and feeding types as were available. The objects of this study were to see if | could uncover further instances of ontogenetic change, if these changes were correlated with a particular tooth type and diet or whether such changes were universal 36 NYBAKKEN throughout the genus, if the juvenile tooth was similar in all instances or different, and finally, to suggest or speculate as to the reasons for the observed changes. In order to accomplish the above tasks, it was necessary to establish a somewhat more elaborate scheme of classification of tooth types than that originally established by Lim (1969) in order to accommodate all the mor- phological types of teeth known to occur in Conus. METHODS AND MATERIALS The Conus specimens used in this study came from a number of sources; Conus ma- gus were furnished by Frank Perron and ei- ther collected by SCUBA in the field in Palau or raised in the laboratory from egg capsules; C. pennaceus were collected in Hawaii by Frank Perron. C. patricius specimens were obtained from the 1967 Pillsbury Expedition to the Gulf of Panama (Nybakken, 1971), and Los Angeles County Museum, the Academy of Natural Sciences of Philadelphia, and Alex Kerstitch; Conus fergusoni were obtained from the Los Angeles County Museum and Alex Kerstitch. Juvenile specimens of C. ebraeus, C. miliaris, and C. coronatus were furnished by Alan Kohn. Juvenile C. pulcher were furnished by Constance Boone. All other adult and juvenile specimens from the eastern Pacific were from the Pillsbury Expe- dition to the Gulf of Panama (Nybakken, 1971), or from the author’s collection from the Gulf of California (Nybakken, 1979) and the Galapagos (Nybakken, 1978). Indo-Pacific and West African specimens were either in the author's collection or from Alan Kohn. Each specimen was measured for total shell length with a vernier calipers. The shell was broken, the animal extracted, and the sex recorded. The radula sac was dissected out, transferred to a depression slide, and the rad- ula teeth freed by treatment with a solution of bleach. Freed teeth were washed in two rinses of water and mounted directly from wa- ter into a polyvinyl-alcohol lactophenol me- dium on standard glass slides. Radulae were examined under a compound microscope equipped either with a differential interference contrast system after Normarski or Hoffman Modulation Contrast optics. Drawings of indi- vidual teeth were made using a drawing tube. For specimens smaller than 2 mm in shell length, a different technique was employed. They were first measured using an eyepiece micrometer in a dissecting microscope. The shell was then broken away using a fine pair of forceps and the animal extracted entire. The whole animal was then transferred to the first depression on a spot plate and rinsed with water; then transferred to the next de- pression with acid fuchsin and left for 10-15 minutes to stain the radula. Next the animal was moved through four successive rinses of water, which removed much of the stain ex- cept from the radula. The animal was then soaked in tissue solubilizer (Beckman BTS- 450 0.5N Quaternary Ammonium Hydroxide in Toluene) and heated on a slide warming tray at 40-65°C for 2-4 hours. The animal was then transferred through Toluene into 70% ethanol where the radula was usually visible as a series of red dots. The radula sac was excised and mounted in PVA-K on a slide for observation. Radula teeth used for scanning electron mi- croscopy were removed from water, air dried, and placed on double stick tape on standard stubs. They were coated with gold in a Po- laron sputter-coater unit and examined with ап ISI SX30 SEM. The SEM mounts were used primarily to verify the three-dimensional structure of the Conus radula. A total of 89 species of Conus were exam- ined for the establishment of radula types in the genus. They represented species from all oceans. (A complete list of species and their radula type is found in Appendix 1.) In order to examine the ontogeny of the radula, | was more limited, both by time and by the availability of specimens. | used only specimens that | was able to identify or that were verified for me. Small specimens of any Conus species are not easy to come by; hence, this study is not as complete as | would have liked it to be. | was able to inves- tigate a complete size series of specimens from post-metamorphic juveniles to adult only for C. magus. The only other species for which post-metamorphic juveniles and adults were available was C. pennaceus, but here the series was not as complete. Other spe- cies for which size series were available were: С. arcuatus (16.3—41.9 mm), С. chal- deus (7.4-25.1 mm), С. coronatus (8.2-20.1 mm), С. ebraeus (7.5-32.5 mm), С. fergusoni (26.1-51.9 mm), С. lucidus (14.4-38.5 mm), С. patricius (27.1-83.5 mm), С. pulcher (11.6-80.7 mm), С. tornatus (8.2-20.1 mm), and С. virgatus (14.9-56.5 mm). Fortunately, these species encompass all of the common ONTOGENY OF CONUS RADULA 37 ANTERIOR Ligament ---- POSTERIOR FIG. 1: A diagrammatic Conus radula tooth illustrat- ing the various terms used in describing the mor- phology. radula types except Type 3, so it was possible to obtain a good overview of the potential changes in the different radula types. RESULTS Morphological Classification of the Conus Radula The individual Conus radula tooth is asym- metrical, three dimensional, and may be mor- phologically complex (Nybakken, 1970b). A system of terminology for the various parts of the tooth was provided by Nybakken (1970b) and Kohn et al. (1972) and is the one followed here. These terms are illustrated in Figure 1. Lim (1967) first recognized that there were three morphologically different groups of rad- ulae in Conus. These three groups were cor- related with the three different feeding types within the genus, piscivores, molluscivores, and vermivores. Of these three, the vermi- vores are the most numerous and also the most diverse in terms of tooth morphology. Whereas the structure of the teeth of both the molluscivores and piscivores is unique and consistent, that of the vermivores is not. Ver- mivores include a number of different mor- phological types, only one of which, that pos- sessed by those species which prey on amphinomid worms, has been directly corre- lated with a specific diet (Nybakken, 1970a). In order to undertake this study, it was nec- essary to attempt to group the various differ- ent radula morphologies into a few more man- ageable groups. Because this had already been done for the molluscivores and pisci- vores by Lim (1969), that left only the vermi- vores. Personal observation of the radulas of 89 species of Conus from all feeding types and oceans, coupled with the analysis of an- other 21 species that have been illustrated in the literature (Bergh, 1895; Piele, 1939; Warmke, 1960), plus an unpublished analysis of 179 species by Tucker (personal commu- nication), of which 113 were different from those | studied, suggested that the vermi- vores could be grouped into a relatively few morphological types, leaving only a few that did not fit and that | have chosen to call “unique” types. Those with which | am famil- iar are illustrated in Figure 2 and described here. Group 1 radulae are the most common among all Conus species and were found in 34 of the 89 species examined (Fig. 2a). The individual tooth has the anterior and posterior parts (demarcation by the waist) approxi- mately equal. The anterior half is terminated by a single barb and has opposite the barb, a blade that extends posteriorly more than half- way to the waist. It may or may not be termi- nated by a barb. A serration is present that extends posteriorly to the level of the end of the blade, or to the level of the waist. The serration usually terminates in a prominent cusp. Scanning electron microscopy shows that the serration and terminal cusp are in fact internal (Fig. 3). The posterior half of the tooth is usually slightly greater in diameter than the anterior and has a Slightly enlarged, usually rounded base bearing a prominent but small spur. For the 17 species for which the food is known, all are vermivores (Table 1). Two additional tooth types are similar to those of Group 1. In fact, Tucker groups them together with Group 1. However, they are both morphologically distinct and readily dis- 38 NYBAKKEN = 0.0625 mm 0.1 mm | FIG. 2: The major morphological groups of Conus radulae. a. Type 1. b. Type 1a. с. Type 1b. d. Type 2. e. Type 3. f. Type 4. g. Radula of C. ebraeus. ONTOGENY OF CONUS RADULA AA U a ES FIG. 3. a. Scanning electron micrograph of the tooth of C. virgatus showing the internal position of the serration. b. Scanning electron micrograph of the waist of a tooth of C. princeps showing the internal position of the cusp. 40 NYBAKKEN TABLE 1. Conus Radula Types and Reported Food Conus Species Radula Type 1 C. chaldeus C. miles C. abbreviatus C. sponsalis C. rattus C. tiaratus . litteratus . leopardus . taeniatus DIS) C. arenatus C. ceylanensis . scabriusculus . Capitaneus . vexillum . balteatus . miliaris ооо OO C. coronatus C. nux Food Platynereis dumerelii Palola siciliensis Palola siciliensis Lysidice collaris Eunice antennata Perinereis helleri Platynereis dumereli Lysidice collaris Eunice antennata Eunice cariboea Eunice filamentosa Marphysa sanguinea Lumbrinereis sarsi Arabella iricolor Nereis jacksoni Perenereis helleri Platynereis dumereli Lysidice collaris Eunice cariboea Lumbrinereis sarsi Perenereis helleri Eunice antennata Eunice afra Nereis jacksoni Neanthes spp. Eunice afra Eunice biannulata Lumbrinereis sp. Dasybranchus caducus Ptychodera flava Ceratonereis Platynereis Eunicidae Perinereis Ceratonereis Palola Perenereis Nereis Ceratonereis Lysidice Palola siciliensis Nereis Eunice afra Eunice australis Eunice afra Onuphis sp. Perinereis spp. Lysidice collaris Eunice afra Eunice rubra Palola siciliensis Eunice cariboea Palola siciliensis Lysidice collaris Arabella iricolor Glycera tessellata Nereidae Eunicidae Syllidae Reference Kohn, 1959 Kohn, 1959; Kohn & Nybakken, 1975 Kohn, 1959 Kohn, 1959 Kohn, 1959 Nybakken, 1978 Kohn, 1980 Kohn, 1980 Taylor & Reid, 1984 Kohn & Nybakken, 1975 Kohn & Nybakken, 1975 Kohn & Nybakken, 1975 Kohn & Nybakken, 1975 Kohn & Nybakken, 1975 Kohn & Nybakken, 1975 Kohn, 1968a Marsh, 1971 Kohn & Nybakken, 1975 Nybakken, 1979 Nybakken, 1971 TABLE 1. (Continued) Conus Species C. gladiator C. regularis C. pulicarius C. vexillum Radula Type la C. princeps C. flavidus C. frigidus C. virgo C. patricius C. ventricosus Radula Type 1b C. dalli C. pennaceus C. marmoreus C. textile C. episcopus Radula Type 2 C. catus C. striatus C. purpurascens C. magus Radula Type 3 C. brunneus C. zonatus C. imperialis Radula Type 4 C. lucidus C. arcuatus Radula Type—Unique C. ebraeus C. lividus Food Polynoidae Eunice afra Eunice filamentosa Platynereis polyscalma Nothria elegans Dasybranchus caducus Nematonereis unicornis Eunice antennata Marphysa sanguinea Eunice afra Eunice filamentosa Palola siciliensis Dasybranchus caducus Ampharetidae Capitellidae Maldanidae Terebellidae Eunicidae Dasybranchus caducus Terebellidae Loimia medusa Aphroditidae Spionidae Perinereis Palola Capitella gastropods Cypraea, Dolabrifera molluscs Conus gastropods fish fish fish fish amphinomid worms Eurythoe Eurythoe Ampharete Lygadamis Sabellariidae Sabellinae Capitellidae Nereidae Onuphidae Nereidae Terebellidae Nereidae Cirratulidae Ptychodera Platynereis Phyllodocidae Maldanidae ONTOGENY OF CONUS RADULA Reference Nybakken, 1979 Nybakken, 1979 Kohn, 1959 Taylor, 1986 Kohn, 1959 Nybakken, 1979 Marsh, 1971 Kohn, 1959 Kohn, 1968b Kohn & Nybakken, 1975 Nybakken, 1988 Taylor, 1987 Nybakken, 1968 Kohn & Nybakken, 1975 Kohn, 1980 Kohn, 1968 Kohn & Nybakken, 1975 Kohn & Nybakken, 1975 Kohn & Nybakken, 1975 Nybakken, 1967 Nybakken & Perron, 1988 41 Nybakken, 1970; Nybakken, 1979 Kohn & Nybakken, 1975 Kohn, 1959 Nybakken, 1978 Nybakken, 1979 Kohn & Nybakken, 1975 Kohn, 1959 Nybakken, 1979 (continued) 42 NYBAKKEN TABLE 1. (Continued) Conus Species Reference C. diadema Eunicidae Nybakken, 1979 Eurythoe Terebellidae gastropods C. californicus gastropods bivalves Kohn, 1966 cephalopods polychaetes amphipods fish C. tornatus cernable from Type 1; hence, | choose to give them separate status. The tooth type | have designated as Type 1a differs from Type 1 in that the anterior part of the tooth is elongated, the serration is proportionately longer, and the blade shorter than Type 1 (Fig. 2b). Usu- ally the cusp is more prominent also. As with Type 1, the serration is internal for most of its length. For the five species for which food is known, all are vermivores, usually taking tube-dwelling polychaetes. | found this type in 14 species investigated. The second related type, which | have des- ignated Type 1b, is more different from Type 1 than is Type 1a (Fig. 2c). In this radula type, the anterior portion is extremely elongated, usually several times the length of the poste- rior region, and the serration runs the entire length of the anterior part. The serration may be external, as in C. pennaceus (Fig. 4a), or completely internal, as in C. dalli (Fig. 4b). There is no waist. In addition, the anterior tip has two unequal-sized barbs, the smaller of which is inflated laterally so as to appear as a spear blade (Fig. 4c). There is no blade and no spur. This tooth type is characteristic mol- luscivores (Table 1). | found this radula in 14 species studied. The radula tooth type | have designated as Type 2 is unique to piscivorous Conus (Fig. 2d, Table 1). Each tooth is very large, con- sisting of a very elongated shaft with no evi- dence of a waist or a serration. The anterior tip of the tooth has an armature of two oppos- ing barbs followed posteriorly by a very large third barb that protrudes outward. There is no spur. There appears to be a slight difference in the teeth of Indo-Pacific piscivores and Nephtyidae Nybakken, 1979 those of the eastern Pacific and Atlantic. Those from the former have the tip of the large third barb recurved at the end, whereas those from the latter do not. | have found this tooth type in eight species. Another highly distinctive tooth type is that designated as Type 3 (Fig. 2e). Teeth of this morphological construction are characteristic of cones feeding on amphinomid worms (Ny- bakken, 1970a; Table 1). Diagnostic of these teeth is the presence of four barbs near the shortened anterior end. One of these barbs juts out from the tooth to form a prominent angle with the shaft. This barb also bears a short serration. The most prominent barb is the one with the greatest length and termi- nates a large blade. All barbs are pointed and none are recurved or hooked. Posterior to the barbs is a slight waist. Posterior to the waist the shaft expands to its maximum diameter and ends in a massive base that bears a large spur. There is no cusp. Tucker includes this tooth with Type 1. | have found this tooth type in eight species. The tooth type designated as Type 4 is characterized by a shortened anterior section that bears two or three barbs but no serration and no blade (Fig. 2f). The barb nearest the anterior tip is always pointed, but the remain- ing one or two may be pointed or blunt. In addition, these teeth usually show evidence of a peculiar anterior fold. The waist is usually prominent, and the posterior part of the shaft is uSually longer and broader than the anterior half. The base is very large and bears a very large spur. There is no cusp. Tucker has di- vided this group into two different groups based upon barb number. Conus species ONTOGENY OF CONUS RADULA 43 Skv 325 FIG. 4. a. Scanning electron micrograph of the anterior tip of the tooth of a C. pennaceus showing the external position of the serration. b. Scanning electron micrograph of the anterior tip of the tooth of a C. dalli showing the internal position of the serration. c. Scanning electron micrograph of the anterior tip of the tooth of a C. pennaceus, showing the inflated barb. 44 NYBAKKEN showing this radula type appear to be mainly deeper water dwellers on soft substrates. Food data for this tooth type are quite sparse, but they appear to feed on worms. | found this type in only five species, but this may be due to the lack of deeper water cones available for study. There are also some teeth that | would des- ignate as unique, apparently confined to one or two species. Those of which | am aware are shown in Figures 2g and 5. Of these, C. californicus has the most catholic diet, feed- ing upon molluscs, polychaetes, Crustacea and fish; C. ebraeus feeds on nereid polychae- tes; C. tornatus on nephtyid polychaetes; and C. lividus and C. diadema both feed primarily on polychaetes (Table 1). It is by no means certain that the above designations represent all the tooth types present in the living Conidae. However, given the probable number of species (350-380) and the total number of species examined here (110), it does not seem likely that any large radula group remains unrepresented. Radula Classification and Correlation with Food in the Vermivorous Conus Whereas the molluscivores and piscivores seem to each possess a single characteristic radula morphology, the same does not ap- pear to be true for vermivores. Types 1, 1a, 3, 4, and at least two of the unique types (C. lividus and C. ebraeus) are all tooth types as- sociated with vermivory (Table 1). With the exception of radula Type 3, which seems to be specific for polychaetes of the family Am- phinomidae, the other vermivores cannot be correlated with a single worm family. The rad- ula tooth type represented by C. tornatus may yet prove to be associated with a single poly- chaete family, because the only food remains found have been of the family Nephtyidae, a family otherwise not present in any other Co- nus for which food data are available (Nybak- ken, 1979). Analysis of Table 1 suggests that most of Conus species with Type 1 radulae feed on errant polychaetes primarily of the families Nereidae and Eunicidae. Those with Type 1a radulas feed more often on polychaetes of the families Terebellidae and Capitellidae. How- ever, because one species with this radula morphology, C. princeps, feeds on eunicids and nereids, this evidence is hardly conclu- sive. Food data are very scarce for Conus spe- cies with radula Type 4. The data for C. luci- dus indicated that cones with this tooth type are vermivores feeding on several families of sedentary polychaetes (Table 1). Conus lividus and C. diadema share a rad- ula tooth morphology that so far has not been found in any other Conus species. It is most like Type 1b but lacks a serration. For vermi- vores, these two species consume the widest variety of food taxa, six families of polychae- tes, both errant and sedentary, as well as en- teropneusts and other gastropods. The most catholic diet of any Conus is that of C. californicus, which is known to consume other gastropods, bivalves, fish, worms, and Crustacea. This species also has a unique radula tooth. Ontogenetic Change In order to attempt to document whether or not an ontogenetic change occurred within each of the major radula types, it was neces- sary to dissect as broad a size range of indi- viduals in each category as possible. Unfor- tunately, very small cones are not abundant in collections and immediate post-metamorphic specimens are even more rare. As a result of these difficulties, | was able to obtain post- metamorphic individuals of only radula Types 1b and 2. Good size ranges were available for some species of radula Types 1 and 1a, and that of C. ebraeus, but there were no small specimens of Type 3. The most conclusive data documenting a profound ontogenetic change in the radula are found in those Conus species that consume fish (Type 2 tooth). This change was docu- mented by Nybakken & Peron (1988) for Co- nus magus and Rolan (1986) for C. ermineus. Both showed that the juvenile radula differed from that of the adult in lacking all three barbs, in size, and in presence of a spur. Since that time, a set of post-metamorphic specimens of C. magus has become avail- able, and dissection of these animals, all be- low 2.0 mm in shell length, has revealed the presence of even more changes. The imme- diate post-metamorphic radula tooth is less than 0.08 mm in length (in an animal of 1.7 mm shell length), has no barbs or blades, and is only slightly folded such that the central lu- men appears to be at least partially open for the entire length. The base is large but lacks the spur found in the later juvenile tooth (Fig. 6). Analysis of a size series of Conus penna- ONTOGENY OF CONUS RADULA 45 | FIG. 5. Unique radula types. a. Radula of С. lividus and C. diadema. b. Radula of C. ximenes and C. mahogani. c. Radula of C. californicus. d. Radula of C. tornatus. ceus, a molluscivore, from 9.6 mm to 33.4 mm revealed no change in the radula mor- phology (Fig. 7a,b). However, a series of post-metamorphic Conus omaria was avail- able from Perron. These animals had shell lengths of about 1.4 mm. Dissection of these animals revealed a radula tooth almost iden- tical to that found in the post-metamorphic C. magus (Fig. 7c). This tooth was less than 0.06 mm in length, had no barbs, blades, or serra- tions, and the central lumen was open throughout its length. Although radula Type 1 is by far the most common, very small specimens of species exhibiting this type were difficult to come by. | 0.1mm N FIG. 6. Ontogeny of the radula tooth in C. magus. a. Radula tooth of a post-metamorphic juvenile. b. Radula tooth of a juvenile. c. Transitional radula tooth. d. Radula tooth of an adult. examined a series of teeth from C. virgatus ranging in size from 56.5 mm to 14.9 mm but found no change. | examined a series of C. chaldeus ranging in size from 25.1 mm down to 7.4 mm. In this series, the smallest individ- ual had a tooth that differed from the adult in lacking a serration and a blade (Fig. 8b). The tooth was folded but did have a very large anterior lumen. A series of specimens of C. ebraeus from 33.2 mm down to 7.5 mm in shell length was dissected. In this case, the smallest individual possessed a radula clearly of the juvenile type without serration, barb, or blade (Fig. 8c, d) and resembling the juvenile tooth of Types 1 and 1a. For radula tooth Type 1a, the presence of a juvenile tooth differing from the adult has been described for C. patricius by Nybakken (1988) (Fig. 9a, b). In this study two additional 46 NYBAKKEN N 0.02 mm FIG. 7. Ontogeny of the radula tooth in C. penna- ceus. a. Radula tooth of an adult (shell length 33.4 mm). b. Radula tooth of an animal of shell length 9.6 mm. c. Radula tooth of a post-metamorphic C. omaria of shell length 1.4 mm. | oon 0.0625 mm | 0.025 mm <) FIG. 8. a. Adult tooth of С. chaldeus. b. Juvenile tooth of C. chaldeus. c. Adult tooth of C. ebraeus. d. Juvenile tooth of C. ebraeus. species, C. pulcher and C. fergusoni, have also been discovered to have different juve- nile teeth (Figs. 10 and 11). In C. fergusoni, the smallest individual dissected was only 26.1 mm and the tooth was similar to tooth Type 1 (Fig. 10a). In C. pulcher the smallest specimen dissected was 11.6 mm. Each tooth in this specimen was more similar to that of the juvenile C. patricius and lacked a serra- tion, cusp, and blade and had a single barb (Figz Nic). 0.02 mm FIG. 9. a. Tooth of an adult C. patricius. b. Tooth of a juvenile C. patricius. No very small Conus bearing Type 4 teeth were available for dissection. A size series of C. arcuatus from 41.9 mm down to 21.0 mm failed to reveal any radula change. Similarly, a size series from C. lucidus of 38.5 mm down to 14.4 mm also failed to reveal any radula change. Since no animals of 10 mm or less in shell length were available, we cannot at present assess if there is an ontogenetic change in this radula type. DISCUSSION These studies have established that there is an ontogenetic change in the radula of Co- nus species of a number of different tooth types that include all three main feeding types. These changes are documented for the greatest range of shell size for Type 1b (molluscivores) and Type 2 (piscivores) where immediate post-metamorphic juveniles were available for study. The striking similar- ity between the tooth types of the post-meta- morphic juveniles in these two otherwise very ONTOGENY OF CONUS RADULA 47 FIG. 10. a. Tooth of a juvenile C. fergusoni. b. Tooth of an adult C. fergusoni. different feeding groups, as opposed to the differences in the adult teeth, strongly sug- gests that perhaps all immediate post-meta- morphic juvenile Conus have similar teeth. It also suggests that the food may well be sim- ilar, because Nybakken & Perron (1988) have demonstrated that the food of juvenile C. ma- gus is worms, not fish. The post-metamorphic tooth does not ap- pear to be strongly chitinized, as it only weakly takes up dyes specific for chitin (acid fuchsin). Furthermore, it is only slightly rolled, such that the lumen is open for the entire length. Whether or not the tooth is functional is not known, but Shimek (personal commu- nication) has observed in certain turrids a similar type of tooth in which the tooth is rolled to form a tube by the proboscis before use. If the teeth of immediate post-metamorphic С. | \\\\ 0.025 mm 0.1mm FIG. 11. a. Radula tooth of an adult C. pulcher of shell length 79.2 mm. b. Radula tooth of an animal of shell length 27.8 mm. c. Radula tooth of a juve- nile of shell length 11.6 mm. specimens eventually prove to have the same structure in all Conus species, then the differ- ence in morphology observed among adult teeth would seem to be initiated in the juvenile teeth as this study suggests. Although teeth different in morphology from the adult were found in juveniles in all three major feeding types, the morphology of tooth was not the same in each juvenile. The most prevalent juvenile tooth type, and very similar in adult Types 1, 1a, 2, 4, is a tooth with a single fold closing the lumen but leaving a very large an- terior Opening; having no, or at most one, barb; no blade; no serration, and a large base. In C. magus, Nybakken & Perron 48 NYBAKKEN FIG. 12. Scanning electron micrograph of a juvenile C. will become the large, recurved barb of the adult. (1988) have demonstrated that this tooth is correlated with feeding on syllid polychaetes. In the molluscivores (Type 1b tooth), dissec- tion of a series of specimens of C. pennaceus from 33.4 down to 9.6 mm failed to reveal any change from the adult radula. Yet, as noted above, the immediate post-metamorphic ani- mals of a closely related species, C. omaria, have a very similar tooth to post-metamorphic C. magus of the same shell length. Perron (personal communication) has noted that ju- veniles of C. pennaceus feed on small gas- tropods, so the food type is similar to the adult. It is not in C. magus. Therefore, it may be suggested that the reason a different juve- nile tooth is not seen in C. pennaceus is that there is not significant change in diet such as seen in C. magus. However, until we can ex- amine radulae from specimens of C. penna- ceus between 9.0 mm and 2.0 mm, this must remain only a suggestion. In these juvenile teeth, although similar, magus showing the development of the bulge that there are indications of the morphological changes that will shape the adult teeth. Thus, in C. magus there is at this stage the devel- opment of a prominent bulge on the tooth at the level where the adult will have the characteristic recurved barb (Fig. 12). Conus patricius has an elongated anterior portion of the tooth corresponding to the elongated an- terior portion in the adult (Fig. 13). In C. fer- gusoni, although we lack small specimens, those with shell lengths of 26 mm show an advanced juvenile tooth indistinguishable from a Type 1 tooth (Fig. 10). In this case, the adult tooth would seem to be derived from the juvenile by simple differential growth of the anterior region. A significant gap in the current analysis is the unavailability of very small specimens of cones with radula Types 3 and 4. It is espe- cially unfortunate for radula Type 3 because of our knowledge that the adults consume only one family of polychaetes, Amphinomi- ONTOGENY OF CONUS RADULA 49 1Skuw 233 FIG. 13. Scanning electron micrograph of the juvenile tooth of C. patricius showing the slender, elongated anterior end. dae. Although a fairly good size series of spe- cies with Type 4 radula was available in C. arcuatus and C. lucidus, no change in tooth morphology was discernable; the need for smaller sizes and post-metamorphic speci- mens is apparent. Observation of all of the above radula types and comparison of the adult and juvenile sug- gests that the location of the greatest change from juvenile to adult is in the distal half of the tooth. The basal portion seems to change lit- tle from juvenile to adult (Figs 8-11), whereas the distal half undergoes significant changes. It is also significant to note that it appears that the serration, where it is present, may be external or internal. If internal, it is of little or no use in any cutting or penetrating action. Where it is exposed, such as in C. penna- ceus, it lies very close to the overlapping fold, suggesting that only a little change in growth or folding could make it internal. However, rel- atively few molluscivores were available for SEM work, so the extent of either internal or external serrations in this group is not known. It is also not known if this internal or external position of the serration correlates with any particular molluscan prey item. What initiates the radula change? This is unknown at present, but Marsh (1977) has shown that the Conus tooth is actually the product of two tissues, the odontoblasts, which make the initial tooth, and the superior epithelium which finishes the tooth. It is pos- sible that the form of the juvenile tooth is the product of the odontoblasts and that the adult tooth represents the finishing work of the su- perior epithelium. The establishment of the existence of a change in radula morphology within a single species with ontogeny and the finding that this change is widespread in the genus among all food types has implications for sys- tematics and ecology in Conus. In the first place, Nybakken & Perron (1987) and Nybakken (1988) have demon- strated that the change in radula morphology и. 50 NYBAKKEN can occur rapidly and within a narrow range of shell lengths. This means that specimens of different shell lengths that have different rad- ulas may not necessarily be different species. Now that we have established the likely mor- phology of the juvenile tooth in this study and that morphology seems to have certain rec- ognizable characteristics, it would seem that this should facilitate juvenile recognition and reduce errors with respect to use of the radula in taxonomy. It is also of importance, there- fore, to note the shell length of any specimens used in radula studies and when comparing specimens to compare only specimens of the same shell size. Given the fact that in C. pat- ricius the juvenile radula may persist into an- imals with shells and shell lengths of the adult aspect and morphology, this means there may be no a priori way to predict whether in some species a specimen of a given size will have the adult radula. However, this may be a feature restricted to only a few feeding types, because there is no evidence for it over a rather large size range in molluscivores (C. pennaceus) and some vermivores (C. luci- dus, C. virgatus, C. arcuatus). The fact that Nybakken & Perron (1988) conclusively demonstrated that the juvenile radula in piscivores is correlated with a differ- ent diet than the adults suggests that many of the other species in which the juvenile radula is different from the adult may also prey upon different food items when small. However, at this time no data exist to prove or disprove this contention. The results from Nybakken & Perron (1988) and Nybakken (1988) with C. magus and C. patricius, respectively, have also demon- strated that the observed radula change is not due to sexual dimorphism. Juvenile radulae were found in both sexes. Given the various radula types and their distribution among the species, which is likely the most primitive type and which are the de- rived? There are several ways of looking at this problem. The simplest is to employ the commonality principle, otherwise stated as “common equals primitive’ (Wiley, 1981). This principle simply states that if a character is widely distributed within a taxon, then the character is likely primitive. Employing this principle and considering that Type 1 is by far the most common type suggests it is also the most primitive. Another criterion for determining primitive or derived is that of ontogenetic precedence (Hennig, 1966). This criterion assumes that the ontogenetic transformation toward a par- ticular character reflects the phylogenetic de- velopment of that ontogeny. Employing this criterion and observing all the juveniles in this study suggests that the development of at least one anterior barb is a primitive feature and that it comes before the development of a serration. My tentative conclusion, therefore, is that a modified Type 1 tooth would seem to be the most primitive, perhaps without a serration, and that the others are derived. The likelihood that the primitive tooth is without a serration is also given support by the fact that the toxo- glossan teeth in the more primitive family Tur- ridae also lack a serration (Shimek & Kohn, 1981). LITERATURE CITED ARAKAWA, K. Y., 1958, On the remarkable sexual dimorphism of the radula of Drupella. Venus, 19: 206-214. ARAKAWA, K. Y., 1969, On some problems of sex- ually dimorphic radulae. Venus, 28:125. BANDEL, K. 1974. Studies on the Littorinidae from the Atlantic. Veliger, 17:92-114. BERGH, R., 1895, Beitrage zur Kenntniss der Coni- den. Nova Acta der Kaiserlich. Leopoldinisch- Carolinsch Deutschen Akademie der Naturfor- scher, 65(2):69-214; 13 pls. BERTSCH, H. 1976. Intraspecific and ontogenetic radula variation in opisthobranch systematics (Mollusca: Gastropoda). Systematic Zoology, 25: 117-122. BORKOWSKI, Т. V. 1975. Variability among Carib- bean Littorinidae. Veliger, 17:369—377. CARRIKER, M. R., 1943, Variability, developmental changes and denticle replacement in the radula of Lymnaea stagnalis appressa Say. Nautilus, 57:52-59. CERNOHORSKY, W. O., 1970, Systematics of the families Mitridae and Volutomitridae (Mollusca: Gastropods). Bulletin of the Auckland Institute and Museum, 8:1-190. FUJIOKA, Y., 1985, Seasonal abberant radular for- mation in Thais bronni (Dunker) and T. clavigera (Kunster) (Gastropods: Muricidae). Journal of Experimental Marine Biology and Ecology, 90: 43—54. HENNIG, W., 1966, Phylogenetic systematics. Uni- versity of Illinois Press, Urbana, 263 pp. HICKMAN, C. S., 1980, Gastropod radulae and the assessment of form in evolutionary paleontology. Paleobiology, 6:276-294. HOLLISTER, S. C., 1954, Some notes on the rad- ula. Nautilus, 68:44—46. HOUBRICK, R. S., 1978, The family Cerithiidae in the Indo-Pacific, Part 1. The genera Rhinoclavus, ONTOGENY OF CONUS RADULA 51 Pseudoverlagus and Clavocerithium. Mono- graphs of Marine Mollusca, 1:1-130. HOWE, S. W., 1930, A study of the variations in the radula of a snail with particular reference to the size of the median teeth. Nautilus, 44:53—56. KOHN, А. J., 1959, The ecology of Conus in Ha- waii. Ecological Monographs, 29:47—90. KOHN. A. J., 1966, Food specialization in Conus in Hawaii and California. Ecology, 47:1041—1043. KOHN, A. J., 1968a, Ecological shift and release in an isolated population: Conus miliaris at Easter Island. Ecological Monographs, 48:323—336. KOHN, A. J., 1968b, Microhabitats, abundance and food of Conus on atoll reefs in the Maldive and Chagos islands. Ecology, 49:1046-1062. KOHN, A. J., 1980, Abundance, diversity, and re- source use in an assemblage of Conus species in Eniwetak lagoon. Pacific Science, 34:359—367. KOHN, A. J. & J. NYBAKKEN 1975, Ecology of Conus on eastern Indian Ocean fringing reefs: diversity of species and resource utilization. Ma- rine Biology, 29:211-234. KOHN, A. J., J. W. NYBAKKEN & С. J. VAN MOL, 1972, Radula tooth structure of the gastropod Conus imperialis elucidated by scanning electron microscopy. Science, 176:49—51. LIM, C. F., 1969, Identification of the feeding types in the genus Conus Linnaeus. Veliger, 12:160- 164. MAES, V. O., 1966, Sexual dimorphism in the rad- ula of the genus Nassa. Nautilus, 79:73—80. MARSH, H., 1971, Observations on the food and feeding habits of some vermivorous Conus on the Great Barrier Reef. Veliger, 14:45—53. MARSH, H., 1977, The radula apparatus of Conus. Journal of Molluscan Studies, 43:1-11. MERRIMAN, J. A. 1967. Systematic implications of the radular structures of West Coast species of Tegula. Veliger, 9:399—403. NYBAKKEN, J., 1967, Preliminary observations on the feeding behavior of Conus purpurascens Bro- derip, 1833. Veliger, 10:55-57. NYBAKKEN, J., 1968, Notes on the food of Conus dalli Stearns, 1873. Veliger, 11:50. NYBAKKEN, J., 1970a, Correlation of radula tooth structure and food habits of three vermivorous species of Conus. Veliger, 12:316-318. NYBAKKEN, J., 1970b, Radular anatomy and sys- tematics of the West American Conidae. Ameri- can Museum of Natural History Novitates, 2414: 1-29. NYBAKKEN, J., 1971, The Conidae of the Pillsbury Expedition to the Gulf of Panama. Bulletin of Ma- rine Science, 21:93—110. NYBAKKEN, J., 1978, Population characteristics and food resource utilization of Conus in the Galapagos Islands. Pacific Science, 32:271- 280. NYBAKKEN, J., 1979, Population characteristics and food resource utilization of Conus in the Sea of Cortez and West Mexico. Journal of Molluscan Studies, 45:82-97. NYBAKKEN, J., 1988, Possible ontogenetic change in the radula of Conus patricius of the Eastern Pacific. Veliger, 31:222-225. NYBAKKEN, J. & F. PERRON, 1988, Ontogenetic change in the radula of Conus magus (Gas- tropoda). Marine Biology, 98:239-242. PAGE, A. J. & R. C. WILLAN, 1988, Ontogenetic change in the radula of the gastropod Epitonium billeeana (Prosobranchia: Epitoniidae). Veliger, 30:222-229. PIELE, A. J., 1939, Radula notes, VIII. Conus. Pro- ceedings of the Malacological Society of London, 23:348-356. ROBERTSON, R., 1971, Sexually dimorphic ar- chaeogastropods and radulae. Annual Report of the American Malacological Union for 1970: 75— 78. ROBERTSON, R., 1985, Archaeogastropod biol- ogy and the systematics of the genus Tricolia (Trochacea: Tricoliidae) in the Indo-West Pacific. Monographs of Marine Mollusca, 3:1—103. ROLAN, E., 1986, Estudio de la radula de Conus ermineus Born, 1778 desde el periodo juvenil al adulto. Publicacoes Ocasionais da Sociedade Portuguesa de Malacologia, 6:23—28. ROSEWATER, J., 1970, The family Littorinidae in the Indo-Pacific. Part 1. The subfamily Littorini- nae. Indo-Pacific Mollusca, 2:417-479. SHIMEK, R. L. & A. J. KOHN, 1981, Functional morphology and evolution of the toxoglossan radula. Malacologia, 20:423—438. TAYLOR, J. D., 1986, Diets of sand-living predatory gastropods at Piti Bay, Guam. Asian Marine Bi- ology, 3:47-58. TAYLOR, J. D., 1987, Feeding ecology of some common intertidal neogastropods at Djerba, Tu- nisia. Vie et Milieu, 37:13-20. TAYLOR, J. D. & D. G. REID, 1984, The abun- dance and trophic classification of molluscs upon coral reefs in the Sudanese Red Sea. Journal of Natural History, 18:175-209. THOMPSON, Т. E. & G. BROWN, 1984. Biology of opisthobranch molluscs, Vol. |. The Ray Society, London, 229 pp. WARMKE, С. L., 1960, Seven Puerto Rico cones: Notes and radulae. Nautilus, 73:119—124. WILEY, E. O. 1981. Phylogenetics, the theory and practice of phylogenetic systematics. John Wiley 8 Sons, New York, 439 pp. Revised Ms. accepted 21 June 1990 52 NDNNHDHANAHADNANANANANADHNANHDANANHDAHNHHAHNHAHAHNHHHHHHHOHHHHHHHHOH HHH HOHHHOHOH . abbreviatus . aemulus amadis . ambiguus araneosus archon arcuatus arenatus aurora balteatus bartschi brunneus bulbus . californicus . capitaneus catus centurio ceylanensis chaldeus coronatus dalli diadema dispar distans . dorriensis ebraeus elongatus emaciatus episcopus ermineus fergusoni frigidus furvus genuanus . geographus . gladiator gloriamaris gubernator imperialis litteratus lividus loroisi . lucidus magus . mahogoni . Marmoreus mercator miles miliaris monile . Natalensis . nicobaricus NYBAKKEN APPENDIX 1 Alphabetical List of Conus Species Examined for Radula Tooth Structure Type 1 9 Type 1b Type 1 Type 1b Type 3 Type 4 Type 1 Type 1 Type 1 Type 3 Type 3 2 Unique Type 1 Type 2 Type 4 Type 1 Type 1 Type 1 Type 1b Unique Type 1 Modified Type 3 Type 1 Type 5 Type 1 Type la Type 1b Type 2 Type la Type la Type 1b Type 3 Type 1b Type 1 Type 1b Type 2 Type 3 Type 1 Unique Type 1 Type 4 Type 2 Unique Type 1b 2 Type 1 Type 1 Type la Type 1b Type la Total Examined = 89 NMNHNHNHOHNHHHANHAHAANHAHANHONHHHHHHHHHOHHOOOD . nigropunctatus nux omaria orion paniculus patricius . pennaceus perplexus piperatus poormani princeps pulcher purpurasceus rattus recurvus regularis . scabriusculus . scalaris scitulus simplex stercomuscarum striatellus textile tiaratus tornatus tulipa varius . ventricosus venulatus vexillum victor victoriae vidua virgatus vittatus ximenes zonatus By Type: ? or unique Type 1 = 34 Туре la = 11 Type 1b = 15 Type 2 Type 3 Type 4 Type 5 нии | = Onn 9 Type 2 Type 1 Type 1b Type 1 Type 1b Type la Type 1b Type 4 Type 1 Type 1 Type la Type la Type 2 Type la Type 4 Type 1 Type 1 Type 1 Type 1 Type 1 Type 2 Type 1 Type 1b Type 1 Unique Type 1b Type 1 Type la Type 1 Type 1 Type 1 Type 1b Type la Type 1 Type 1 Unique Type 3 ONTOGENY OF CONUS RADULA 53 APPENDIX 2 Conus Radulae Studied from Drawings and Photos in the Literature C. acuminatus Type 1b (Piele, 1939) C. anemone Type la (Bergh, 1895, as C. maculosus) C. betulinus Type 1 (Piele, 1939) C. daucus Type 1 (Warmke, 1960) C. ermineus Type 2 (Warmke, 1960, as C. ranunculus) C. generalis Type la (Piele, 1939, as C. maldivus) C. inscriptus Type 4 (Piele, 1939) C. jaspideus Type 4 (Warmke, 1960) C. juliae Type 1 (Warmke, 1960) C. leopardus Type 1 (Bergh, 1895, as C. millipunctatus) C. mercator Type 1 (Bergh, 1895) C. mindanus Type 4 (Piele, 1939, as C. agassizil) C. monachus Type 2 (Piele, 1939) C. mucronatus Type 2 (Bergh, 1895) C. nussatella Type 1 (Piele, 1939) C. pulicarius Type 1 (Bergh, 1895) C. regius Type 3 (Warmke, 1960) C. spurius Type 1a (Warmke, 1960) C. striatus Type 2 (Bergh, 1895) C. taeniatus Type 1 (Bergh, 1895) C. tessulatus Type 1 (Piele, 1939) Total = 21 By Type Total Conus spp. examined = 110 1] =8 | ia = 3 HD 2. = al $ A AS Sr) MALACOLOGIA, 1990, 32(1): 55-67 TEMPO AND MODE OF EVOLUTION IN CONIDAE Alan J. Kohn Department of Zoology, University of Washington, Seattle, Washington 98195, U.S.A. ABSTRACT | examined the paleontological literature of the Conidae, here limited to the genus Conus, in order to detect temporal patterns in its evolutionary history. All 20 Mesozoic species originally described as Conus are likely opisthobranchs, or if Conus they are from strata now known to be of Eocene age. The few reports of Paleocene species are probably also incorrect. The earliest bona fide fossils of Conus appear to be from the Lower Eocene (50-55 mybp) of England and France, where the contemporaneous land flora indicates tropical climatic conditions. Collation of the paleontological literature places the first radiation of Conus in the Middle and Upper Eocene. Diversity decreased in the Oligocene, one or more major radiations occurred in the Miocene, and diversity decreased again in the Pliocene, followed by very rapid increase to the present ap- proximately 500 species. The observed pattern is compared with four alternative models of taxonomic diversification: exponential, logistic, and exponential interrupted by periods of stasis or by periods of reduced diversity. The data fit the last model most closely, as do gastropods and other fossilizable marine invertebrates in general from the same era. Important evolutionary trends in Conus include (1) increasing shell size, thickness, and ratio of diameter to length, and decreasing spire height, and (2) inhabiting shallower, higher-energy marine environments. Shell form may have been the most important innovation leading to the major radiations. Key words: fossil history, evolutionary origins, adaptive radiation, Conidae. “One finds very few papers that give us an objective account of the evolution and adaptive radiation of any group of Mollusca.” G. M. Davis (1981) INTRODUCTION During the past 35 years, comparative bio- logical studies of the Conidae have elucidated many aspects of the habitats and habits, feeding and reproductive biology, and diver- sity and community ecology of assemblages of co-occurring species (Table 1). This geo- logically youthful yet unusually species-rich family of gastropods is now probably as well known biologically as any tropical marine in- vertebrate taxon. Yet despite this wealth of neontological information, and the existence of a quite respectable fossil record, the origin and evolutionary history of the family, and the historical and ecological factors that have been important in its remarkable evolutionary radiation, remain virtually unknown. CLASSIFICATION OF THE FAMILY CONIDAE Conidae as a family-level taxon was first validly proposed by John Fleming (1822), and 55 has been generally accepted since about 1850, but its scope has been variably per- ceived. Twentieth-century workers generally consider the neogastropod Superfamily Co- noidea (or Conacea or Toxoglossa) to com- prise two families, Conidae and Terebridae, (Thiele, 1931; Seed, 1983), or three, with sep- aration of Turridae from Conidae (Wenz, 1942; Powell, 1966; Ponder & Warén, 1988). As this paper focuses on the evolution of Conidae in the narrower sense, | employ the latter classification here. Characterizing the distinction between Tur- ridae and Conidae is not straightforward. Several genera intermediate in shell form, most with extant representatives, appear to link the two families, and different authors have drawn different lines between them. Cossmann (1896) and Powell (1966) de- scribed each of these genera and noted their similarities and distinguishing features. Most 20th century authors include in the Conidae only Conus, and Hemiconus if they consider this extinct genus or subgenus (Table 2). 56 KOHN TABLE 1. Summary of comparative biology of Indo-Pacific Conus Aspect Patterns Geographic distribution Species ranges: narrowly endemic to entire Indo-Pacific region. Range extent: correlated with dispersal ability of planktonic larvae. Species diversity Lowest (1 species) in geographically peripheral regions. Low (5-9 species) in topographically simple, intertidal habitats. Highest (12-27 species) in complex subtidal coral reefs. Habitat occupation” Fine to coarse soft sediments; algal turfs; rubble to reef limestone. Some differential specialization by co-occurring species. Habits and activity Feeding biology” Infaunal to epifaunal. Nocturnally active; diurnally sheltered. Predators on worms (mainly polychaetes), gastropods, or fishes. Markedly differential specialization by co-occurring species. Reproductive biology” Embryonic period 7—24 days. Precompetent planktonic veliger larval period O—30 days. Strong gradients in developmental patterns related to egg size. "Species of Conus vary widely from specialists to generalists in these aspects. Cossmann's (1896) criteria that distinguish Coninae and Cryptoconinae are clear and applicable to both fossil and Recent forms. Partial resorption of inner walls, a hallmark of Conus (Kohn et al., 1979), also occurs in Conorbis and Hemiconus (Coninae) but not in Cryptoconus (Cryptoconinae). The spire and aperture in Cryptoconus each comprise about half the total shell length, whereas the spire of Conorbis is always shorter than the aperture length. In Coninae, shell form is gen- erally conic or biconic with the sides of the aperture parallel. Hemiconus and Conorbis thus share important shell features with Co- nus. Members of the Cryptoconinae do not resorb inner shell walls and have fusiform shells with ovate apertures. Here | follow Cossmann's (1896) distinction between Cryp- toconinae and Coninae, but in agreement with other 20th century workers | assign the Cryptoconinae to Turridae. | restrict the Conidae to the genera comprising the sub- family Coninae. Conorbis (Eocene-Miocene and the Recent C. coromandelicus Smith) and Hemiconus (Middle Eocene-Lower Miocene) each in- clude about 20 species (Glibert, 1960; Powell, 1966). Thus neither of these genera has un- dergone a striking radiation. Traditionally, they are considered the most closely related to Conus (e.g. Thiele, 1931; Powell, 1966), but we remain ignorant of the evolutionary history and phylogenetic relationships of these groups. | consider only Conus in the rest of this discussion. ORIGIN OF CONUS The oldest fossils described as Conus are from the Lias of Normandy near Caen; they are of Pliensbachian age (188—196 mybp; ab- solute dates in this paper are taken from Har- land et al., 1982, and Haq & Van Eysinga, 1987). Charles Lyell read an informal account of the discovery of these specimens in a pub- lication of the Linnaean Society of Normandy ([Eudes-Deslongchamps], 1837). He collect- ed at the site in 1840, and later that year (Lyell, 1840), in collaboration with G. B. Sowerby, he described Conus cadonensis and C. conca- vus. Deshayes & Milne Edwards (1845:7) questioned the assignment of these species to Conus, and soon d'Orbigny (1850, 1852) con- firmed their suspicion by demonstrating in sec- tioned specimens that the last whorls are thin and that internal shell walls are not resorbed. In Conus, the last whorl is thick and inner walls are often reduced to 50 um (Kohn et al., 1979), in Eocene as well as modern species (Kohn, 1982). Conus abbreviatus Eudes-Deslong- champs, 1849, and C. caumontii Eudes-Des- longchamps, 1849, were described later from the same formation. Conus minimus D'Ar- chiac, 1843, was described from the Middle Jurassic (Bajocian, 172-177 mybp) of Aisne, but it was assigned questionably to Conus. It is clearly an opistobranch, on the same grounds. D'Orbigny (1850, 1852) assigned all of these taxa to the opisthobranch genus Ac- taeonina, and they have generally been con- sidered members of the family Actaeonidae EVOLUTION OF CONIDAE TABLE 2. Boundaries between Turridae and Conidae of selected authors. ЭЙ Сепега: Genota Cryptoconus Conorbis Hemiconus Conus Geologic Eocene- Eocene- Eocene- Eocene- Eocene- Range: Recent Miocene Recent Pliocene Recent | CONIDAE: CRYPTOCONINAE ] | CONIDAE: CONINAE | Cossman (1896) CONIDAE: CYTHARINAE TURRIDAE: CRYPTOCONINAE [ TURRIDAE: CONORBIINAE [ TURRIDAE: CONORBIINAE ever since (Meek, 1863; Cossmann, 1895; Zilch, 1959) (Table 3). The remaining Mesozoic fossils originally described as Conus are all reported as Cre- taceous. The next oldest is C. verneuilli Vil- anova, from the Neocomian of Spain (123— 140 mybp). This also appears to be an opisthobranch (Tomlin, 1937). One species, C. primitivus Collignon, was described from the Albian (98-109 mybp) of Madagascar. Definitely Albian (N. Sohl, in МЕ), the single specimen is a partial internal mold lacking any shell material. It is too fragmentary to as- sign to any genus with confidence, but it is possibly an opisthobranch. The one Creta- ceous species described from Italy, C. schi- osensis Bóhm, 1895 (Cenomanian-Turonian; 89—98 mybp), is also an opisthobranch (Sohl & Kollmann, 1985). Three species of Conus were described from the Cretaceous of France, one Turonian (88—91 mybp) and two Santonian (83—86 mybp). Conus marticensis Matheron, 1843, was described from the Turonian at Mar- tigues. The original description and figures in Matheron (1843) do not permit its rejection from Conus, and its source formation, “Craie ligno-marneuse,” is definitely Cretaceous. One of the Santonian species, C. tubercula- tus Dujardin, 1837, from the Touraine, was the first Cretaceous Conus to be described. The great French protozoologist Dujardin de- scribed the species mainly from molds, but in the original figured specimen a partial cast replaced some of the original shell. This spec- | Il | | _ СОМРАЕ _ Thiele (1931) CONINAE CONIDAE Wenz (1942), Ne ] Glibert (1960) Powell (1966) [ CONIDAE ] Ponder & Warén (1988) imen is now assigned to the genus Gosavia, family Volutidae (Cossmann, 1896; Wenz, 1943). The second Santonian species, C. se- nessei Delpey, 1938, from Corbières, is prob- ably neither a conid nor a turrid. Three additional species described from the Upper Cretaceous, Conus cylindraceus Geinitz, 1850, from Silesia, C. semicostatus Goldfuss, 1843, from Westphalia, and C. /a- tus Eichwald, 1869, from the Crimea, are also opisthobranchs. Geinitz (1850) stated that his generic assignment of his 4 mm-long fossil was doubtful. Of the six remaining species originally de- scribed as Cretaceous Conus, C. canalis Conrad, 1858, from Mississippi is now placed in the Volutidae, and the remaining five (three from California and two from Brazil) are now known to be from Eocene and Miocene strata (Table 3). Finally, one Cretaceous species was origi- nally assigned to Conorbis. Powell (1966) re- tained this species, C. mcnairyensis Wade, 1917, in Conorbis and thus extended the range of that genus from Cretaceous to Re- cent. However, the shell aperture of C. mc- nairyensis is not straight and its sides are not parallel, and there is no evidence either of the exhalent sinus or the arcuate outer lip char- acteristic of the Turridae, including Conorbi- nae. Sohl (1964) retained С. mcnairyensis in the Turridae, questionably assigning it to Cryptoconus (Table 3). Thus all 20 species of Conus and the one of Conorbis originally described from Mesozoic KOHN 58 (£b61) zuaM ‘(968L) uueussog (4 ur) 140$ (5861) циеш|оу 3 140$ (ЗИ ur) 140$ (1561) uo] (2581) ÁUbIqIO p (0981) AuBigiO.p (0981) AuBigqiO.p (9961) yalız (0581) AuBiqio,p (5561) yalız (0981) AuBigiO.p ээиэла;эн UeIUOJUES UBILOJUES UBIuOJn] -UEILEWOUSN veigly ueiyoeqsual|d ueiyoeqsual|d UBIYORQsualld иецовазиана abe\s ueIUouaS UEIUOUSS & UBIWO208N ser] ser] ser] ser] ser 42093 рип} e jou Ajgeqoid snoa9e]a19 :SNUO)D jou (эерцподл) snoa9e]919 BIAPSOD) Sn0892}919 ésnuog (VIHONVHSOHLSIdO) Sn0992}919 — сиоэвроецол snoa9e]919 ayeulwiajapul (VIHONVHSOHLSIdO) ¿SNO39e]919 uoajoy (VIHONVHSOHLSIdO) oisseunr PUIUO9E)9Y (VIHONVHSOHLSIdO) SIsseinf PBUIUO8E)9Y (VIHONVHSOHLSIdO) olsseunr BUIUOBEIIY (VIHONVHSOHLSIdO) 9ISSBINP UOBPJIBUDD (VIHONVHSOHLSIdO) JIsseinf uO9BJI9EUON pollad snuao) $и011509$!А Juano ценой ценой UEIUOINL -UEIUEWOUSNY ueialy ueiooleg UBIyoeQqsualld UBIyoeqsualld ueiy9eqsual|d иецовазиана э6е}5 цешоэоэм 128609 sen sen sen ser] 42093 snoa9e]a19 $п099Е}э19 Sn0892]9179 Sn0992}9179 Sn0992}917 Sn0992}9179 oisseinf oisseunr oisseinr olsseunr oisseunr pouad eouei4 ‘S2181q109 e9ue14 ‘SINOL aoues4 ‘sandıueyy Ате ‘зам иецацал Jeoseßepeyy "Auonejeuy ‘М ureds “¿UO|[9Jseg aoues4 ‘ausiy aouel4 ‘uae Jesu goues4 ‘uaeg Jesu aouel4 ‘uaeg 1Peu gouel4 ‘uaeg 1Peu Ayye07 8561 ‘Aedieq 1681 ‘uipseing 5781 ‘иолэщеи\ 9681 'wyog 6+61 ‘чочбцоо 6581 ‘EAOUEIIA ev8! ‘2e1U91Y,Q 6781 ‘sdweyo -Buo¡sag-sapn3 6781 ‘sdweyo -Buo¡sag-sapn3 0781 'Áqiamos 9 9 11947 081 'Áqiamos ‘9 9 11847 ayeg ‘1ouny suoneubisag jeuibuC lassauas snjejnaiaqn} SISUADIIEW SISUISOIYIS snAn ud IJINQUIBA SNUWIUILW INUOWNEI snjeineiqge SNAPIUOI sisuauopeo salads (SIg10U0N pue) snuo) 910Z0S8N se Апешбио paquosap salsads jo uoljisodsip juasald ‘€ FIGWL og EVOLUTION OF CONIDAE (9961 ‘иэмоа) ueneoun Alı ey, i A Ñ _ —_— _—__—_— _ _—_ ÍÑ—_ _——_ _—_ —_ ———— (a ur) 140$ (au ur) 140$ (1261) Wemals (1261) Wemals (2161) Buuem (rr6L) uosueg $ u99y (2261) Wemals (7961) 1405 (1661) unwoL uelYyoujseeyy UBI9EIUOTD uenuoujseeyy 2aUSIOIN 2USIDOINN 2u9903 эиэ503 2USIDOIN -2U9903 ueluouas ey цеиоцас цеиоцэс tema] snuog tema] snuo) Алеша ¿Sau nans tema] snuog Алеша snuog (эерцтюдл) SN0992]919 un dedo!7 (VIHONVHYSOH1LSIdO) snoa9e]919 (VIHONVHIOH1SIdO) Sn0992]919 (VIHONVHSOHLSIdO) $п099Е}э1Э Puyo Ao snoa9e]919 ¿SNUOIOJAÁL) LEIIEIUOY UEIUOUSS snoa9e]Ja19 snoa9e]a19 snoa9e]a19 Sn0892]919 SN0992)919 $п099Е}э19 $п099е}э19) sn0892)919 Sn0892]919 sn0898}919 zeig ‘ered ‘sedeld Oly zeig “Ped ‘зеае!« Oly ‘4189 “09 u19y ‘uolo 104 Jeau ed ‘09 илэх ‘цоэ1 104 Jesu 4189 “09 uJay 'uole] 1104 Jesu IddiSSISSIN “09 yeddiy YSSN “eau Áueuao) “eljeydisam BINBno]s -OY4998ZD ‘ep -jemsbuljsaly ээззэциа1 "09 MIENIN $9481 “SUM $481 ‘SUM 7981 ‘qqed 7981 ‘qe 7981 ‘qqe5 8581 peiuo] 6981 'PIemyolg €v8! 'SSNIPIOD 0S8! ‘гише9 ($/9/0и0)) 2161 ‘эрем sninqisas SNUOJIPUOO snjenuls приошал MUJOY sıreued sme] snje]soaıwas Sn8921pPUIA9 sisuaÁneugu 60 KOHN strata are probably either not Mesozoic or not Conidae or both. | conclude that the family Conidae originated after the Cretaceous-Ter- tiary boundary. The few reports of Paleocene Conus are equally suspect. Only С. rouaulti D'Archiac, 1850, from the “Groupe Nummulitique” of southern France, occurs in beds that are mainly Eocene but may possibly include Thanetian material (Danizot, 1957). Conus rouaulti and the quite similar C. concinnus J. deC. Sowerby, 1821, from the Lower Eocene (Ypresian) of France and England respec- tively, seem to represent the earliest bona fide records of Conus, s.s. In addition, Lower Eocene fossils of two other species have been reported from Sind, Pakistan (Coss- mann & Pissarro, 1909). SMALL BEGINNINGS? New groups of animals tend to originate from small ancestors, and a common trend in the evolutionary history of a supra-specific taxon is increase in body size. This is Cope’s well known “law,” proposed for vertebrates but shown to hold quite generally as well for invertebrates with fossilizable hard structures (Newell, 1949). Does a pattern of increasing shell size characterize the evolutionary radia- tions within Conus? If so, does the overall dis- tribution of shell size in the genus shift up- ward, or, as Gould (1988) proposed as more likely, is apparent size increase due mainly to increasing variance in shell size? If C. concin- nus and C. rouaulti are accepted as early, if not the earliest, members of the genus, their size can be compared with later species, par- ticularly those at and just before the initiation of major radiations. Detailed analyses remain to be carried out, but preliminary data suggest trends. The type specimen of C. rouaulti is 11 mm, and that of C. concinnus is 14 mm, in shell length. The largest specimen of the lat- ter species in The Natural History Museum, London, is 32 mm, and the mean length of the largest specimen in five Lower Eocene (London Clay) lots is 26 mm. Although many Conus species of about the same size occur in Middle Eocene deposits, much larger species are also prominent then, the time of the first known radiation of the genus. For example, a syntype and several other specimens of C. edwardsi Cossmann in The Natural History Museum, London, from the Middle Eocene Bracklesham Beds in southern England are about 70 mm long. This species also has a relatively shorter spire than C. concinnus, averaging about 16% of total shell length vs. 30% in the latter species. While further analyses of the size fre- quency distributions of Paleogene and Neo- gene Conus remain to be carried out, the sizes of extant species, representing the most diverse radiation in the group's history, are reasonably well known. The size of modern Conus species varies markedly in different habitat types. In the Indo-Pacific region where most species occur, median shell lengths are 23 mm on intertidal benches, 35 mm on sub- tidal coral reefs, and 80 mm in subtidal sandy bays (Kohn, 1980, 1981). Species similar in size to the hypothesized ancestral species thus persist commonly today. Coral reef plat- forms support the highest modern diversity; these species are of somewhat larger body size. Shallow reef-associated lagoons rank next in Conus diversity; they support assem- blages mainly of even larger species (Kohn, 1981), including the largest extant species, with shell length of more than 200 mm. A few Indo-Pacific Conus species with maximum shell size less than the Lower Eocene species also occur today, and more exist in other parts of the geographic range of the genus. Thus size increase has characterized the evolution of Conus, in the sense of increasing upper size limits and increasing size variance. As in other groups of organisms to which Cope’s law applies (Bonner, 1988), small species not only persist but may be quite di- verse. PATTERNS OF EVOLUTION IN TIME AND SPACE Alternative Hypotheses of Diversity Patterns As a simplified model of diversification rates, Stanley (1979) plotted the logarithm of the number of extant species in a taxon against the time since its origin. The slope of a line drawn between this point and the origin (assuming a single species initiated each taxon) can be interpreted as the exponential rate of species proliferation. This method un- derestimates, as Stanley (1979) noted, be- cause it omits extinct species. Moreover, di- versification rates are unlikely to remain constant over long periods, for reasons in- volving earth history, ecological factors, and the inherent attributes of evolutionary lin- EVOLUTION OF CONIDAE 61 A B o Ta À о © ©: (dp) 5 5 0 0 ec D = FE о ==) 0 0 Time Since Origin of Taxon FIG. 1. Alternative patterns of species proliferation of a diversifying taxon in time; semilogarithmic plots. A, Exponential. dD/dt = r,D,. Speciation rate per species (г.) and species extinction rate (г.) are constant; г. = r,—re. В, Logistic. dD/dt = r,¿D (1—D/D). r, = initial diversification rate. D = equi- librium value. C, Periods of exponential diversifica- tion alternate with periods of stasis. г. varies, as г. = г.. D, Periods of diversification (г. > г.) alternate with periods of net extinction (г. < го). eages. Figure 1 shows several possible alter- native patterns. The simplest case is the ex- ponential or log-linear model (Stanley, 1975, 1979) (Fig. 1A), for speciation by each daugh- ter species at a constant rate and a constant species survival rate. A constant exponential rate of increase damped by the imposition of a saturation value results in a logistic curve (Sepkoski, 1978; Walker, 1985) (Fig. 1B). The remaining models in Figure 1 incorporate fac- tors that cause periods of diversification to al- ternate with periods of stasis or slow net change (Fig. 1C), or with periods of reduced diversity due to extinction rate exceeding spe- ciation rate (Fig. 1D). Temporal Characteristics of the Conus Fossil Record In order to determine the history of taxo- nomic diversification in Conus, | developed a database of all records | could locate in the paleontological literature (2,500 from 1792 to the present) that indicated stratigraphic age and geographic location of fossil Conus spe- cies. For Middle Eocene-Pleistocene records, | generally accepted at face value the species identification and stratigraphy of original au- thors; no effort has yet been made toward critical evaluation of the data, and all of the biases that characterize paleontological data in general apply (see e.g. Raup, 1976a). Fig- ure 2 shows the result in the form of a spindle diagram of the number of Conus species through the Cenozoic, including Lyellian per- centages for each epoch. At times when the number of species is increasing from stage to stage, turnover becomes an important aspect of diversification. Is increasing richness due to a modest number of originations combined with persistence of most species from the pre- vious stage, or to modest persistence and the origination of many new species? Figure 3 presents patterns of Conus spe- cies turnover during the Cenozoic; these data are also accepted uncritically from the pale- ontological literature. First and last appear- ances are expressed in absolute numbers (plotted on a logarithmic scale; Fig. 3A), rela- tive to the total number of species present during the interval (Fig. 3B), and as apparent rates of speciation and extinction (Fig. 3C). Figure 3D shows turnover calculated as the number of originations plus extinctions per species present and the rate of diversifica- tion per species per million years, because the intervals used vary considerably in abso- lute time. The notations used (after Sepkoski, 1978) are: S = number of first appearances in interval (apparent speciations); E = number of last appearances in interval (apparent extinctions); D = number of species present in interval (apparent diversity); At = duration of interval in millions of years; Turnover = (S+E)/D; Diversification rate = rg = г. — r where Rate of speciation r, = S/(DAt), and Rate of extinction г. = E/(DAt). The main aspects of the patterns that emerge from analyses of the data as origi- nally reported are: (1) The genus Conus originated during Lower Eocene time. Mesozoic and Paleocene records are rejected or dubious. (2) The first real radiation of the genus oc- curred in the Middle Eocene (Fig. 2). Many species persisted into the Upper Eocene, but 75% of all Upper Eocene species are first re- ported then (Fig. 3B). In all, about 100 spe- cies are recorded from this epoch. Species turnover was maximal in Middle Eocene be- cause of the large numbers of both origina- e) 62 KOHN No. of % Species, Extant и: | __Pleistocene | | 24.6 32.8 38.0 u 42.0 Eocene |M PA 50.5 50 Species FIG. 2. Kite diagram showing the number of species of Conus throughout Tertiary and Quaternary time, based on an uncritical analysis of the paleontological literature. Ages of epochs and subdivisions from Harland et al. (1982); the two columns at left give the total number of species reported from each epoch and the fraction extant. Numbers of species are: Lower Eocene: 5; Middle Eocene: 42; Upper Eocene: 42; Lower Oligocene: 28; Upper Oligocene: 19; Lower Miocene: 127; Middle Miocene: 111; Upper Miocene: 158; Lower Pliocene: 43; Upper Pliocene: 53; Pleistocene: 124. tions and disappearances (Fig. 3A), but be- cause the interval was long, the rate of diversification was low (Fig. 3D). “Per spe- cies” rates of origination and extinction were higher in the Upper Eocene (Fig. 3C). (3) Species diversity decreased in the Oli- gocene, a pattern common to the Gastropoda and marine invertebrates in general (Raup, 1976b). Numbers and rates of originations and extinctions declined (Figs. 3A,C), as did species turnover (Fig. 3D); about 70% of spe- cies present originated in the Lower and Up- per Oligocene while extinction rates were 52% and 32%, respectively (Fig. 3B). (4) One or more major radiations occurred in the Miocene. Nearly 300 species are re- corded from this epoch. Originations of new species increased to 82% of all species present in the Lower Miocene, when turnover was second only to the Middle Eocene (Figs. 3B,D). As in that radiation, the Lower Miocene diversification rate was low because the inter- val was long (Figs. 3C,D). The rates were higher although absolute and relative num- bers of originations and extinctions declined in the shorter Middle Miocene (Figs. 3A,B,C). Originations then declined to about 50% of species present by Upper Miocene, extinc- tions increased, but rates of both declined (Figs. 3A,B,C). (5) Species diversity again declined in the Pliocene (152 species recorded). Generally reduced diversity of gastropods and other in- vertebrates is characteristic of this epoch (Raup, 1976b). Both the numbers (Fig. 3A) and proportions (Fig. 3B) of originations and EVOLUTION OF CONIDAE 63 Log Number of First (e) and Last (a) Appearances Number of First (e) and Last (о) Appearances 5 5 Percent of Originations (®) and Extinctions (o) 0 t teten! Apparent Speciation (e) and Extinction (a) Rates (e) Turnover (о) Diversification Rate Eocene Oligocene Miocene Л Pliocene Pleistocene FIG. 3. A. The numbers of originations (e) and ex- tinctions (0) of Conus species, determined from re- ports of first and last appearances in the fossil record, throughout the Cenozoic. B. Species turn- over, calculated as the sum of the numbers of orig- inations (S) and extinctions (E) (from Fig. 3A) di- vided by the number of species reported during each interval (D) (see text). C. The apparent rates of speciation (origination) (г. = S/Dt; e) and extinc- tion (г. = E/Dt:c) during each interval. D. Species turnover ([S + E]/D; ©) and species diversification rate (rz = г.— rie). extinctions of Conus species declined, but their rates increased (Fig. 3C) in this tempo- rally brief epoch. (6) Very rapid speciation (Figs. 3A,B) and a large disparity between origination and ex- 1000 3 wo wn oO 2 ‘© о oO oO a 5 100 20 - о о > AS Ф e Ho] E = 2 = Wize O — | 0 Eocene Oligocene Miocene À Pliocene Pleistocene Recent FIG. 4. The numbers of species of Conus reported from Tertiary and Quaternary epochs and stages. Data from Fig. 2, plotted to conform with the models Е! 1 tinction rates (Fig. 3C) occurred during the even briefer Pleistocene, leading to modern high diversity. Nearly 65% of Pleistocene spe- cies are not known from earlier in the fossil record. (7) Only 11% and 33% respectively of Mi- ocene and Pliocene species survive, but 77% of Pleistocene species are extant. In his graph of nine extant radiating marine prosobranch clades according to model A (Fig. 1), Stanley (1979) gave a mean net ex- ponential rate г = 0.067 my '. At this rate, the number of species in a clade doubles in 10.3 my. For Conidae, he indicated 500 ex- tant species and an age of 70 my, orr = 0.103 my ', equivalent to a doubling time of 6.7 my. Taking the age of Conidae as 55 my based on the evidence presented here in- creases г to 0.113 my ' and decreases the doubling time to 6.1 my. As noted above, this model inevitably underestimates the rate of diversification. If the data in Figure 2 are replotted accord- ing to Figure 1, the resulting pattern ap- proaches model D most closely (Fig. 4); the fossil record of Conus indicates alternating periods of rapid radiation and of reduced di- versity. As this closely parallels the temporal diversity patterns of other marine invertebrate groups during Cenozoic time (Raup, 1976b), extrinsic environmental factors were likely im- portant causes. Geographic Features of the Conus Fossil Record Preliminary paleobiogeographic analysis of the Conus fossil record suggests that: 64 KOHN (1) The Lower Eocene origin of the genus is coastal European; the earliest verified records are from England and France. (2) The first real radiation, in the Middle Eocene, likely occurred in the same geo- graphic region; about 3/4 of Middle Eocene species are from Britain and Europe, but the genus also expanded its range broadly. Mid- dle Eocene species are also recorded from Egypt, Nigeria, Pakistan, California, and the U.S. Gulf Coast. (3) After the Middle Eocene, extinctions of Conus species outpaced originations in the European seas, but modest, localized diver- sity increases occurred on the Indo-Australian plate (Upper Eocene), and in the Asian region of the Eurasian plate (Upper Oligocene). Whether or not different Conus species as- semblages occurred in each geographic re- gion remains to be addressed. Piccoli (1984) concluded that Paleogene molluscan assem- blages of the Mediterranean region were gen- erally Indo-Pacific in composition; Rosen (1988) emphasized regional differences in contemporaneous corals and echinoids. (4) Europe and the Indo-Australian regions were the sites of major Miocene radiations, the latter predominantly early in the epoch and the former continuing throughout Mi- ocene time. (5) Throughout its history, the genus Conus appears to have been confined to warm seas, with all of the major radiations occurring in tropical conditions. In Britain, “in Eocene times the climate, as reflected in the land flora, was that of tropical lowlands such as those of south-east Asia today” (Melville & Freshney, 1982). The same likely applies to the Miocene seas occupied by the genus, and its modern geographic distribution remains predominantly tropical. (6) The data fail to reveal the geographic sources of the group’s most important radia- tion, resulting in several hundred extant spe- cies. Most species known as Pleistocene fos- sils are distributed similarly to their modern counterparts, with the majority in the Indo- Australian plate and western Pacific regions, and fewer but substantial numbers in the Americas. This remains a critical area for fu- ture investigation. NEW ADAPTIVE ZONES? KEY INNOVATIONS? Of necessity | address these topics with a high degree of speculation, and | urge others to gather relevant data to test the hypotheses advanced. New Adaptive Zones? An adaptive zone, as the concept was in- troduced by Simpson (1953) and clarified by Van Valen (1971), is the “niche” of a taxon above the species level. Its two basic, more or less independent components comprise the resources used by the members of the focal taxon, and their resistance to predation and parasitism. Did the evolutionary radiations of Conus depend on successful invasion of a different adaptive zone and different ways of acquiring resources and defending against enemies, from those of the ancestral and sis- ter taxa? The answer is by no means clear. During the early evolutionary history of Conus, the fossils are typically associated with fine sed- iments characteristic of continental shelf and greater depths, similar in general to the hab- itats of many species in the hypothetically an- cestral family Turridae. (Such habitats are also particularly favorable sites for fossiliza- tion.) Successful invasions of shallower bay and lagoon environments probably began in Middle Eocene time. The conical shape of the last whorl with the apex of the cone anterior would certainly facilitate locomotion by the gastropod through soft substrata. Evolution- ary trends toward (1) increased shell size, thickness and ratio of diameter to length, and decreased spire height, and (2) occupation of ever shallower and high energy marine envi- ronments probably occurred during all Middle Eocene and Miocene radiations of Conus but at present remain largely undocumented. These changes in shell form could well have expanded the taxonomic and size ranges of suitable prey organisms without sacrificing defensive shell strength. Simultaneously, the habitat shifts likely involved use of hard as well as soft but coarser substrata associated with coral reefs, a biogenic environment in- creasing in complexity and geographic extent contemporaneously with the radiations of Co- nus (Rosen, 1988). Key Innovations? The rapid evolutionary radiation of a taxon is often assumed and sometimes docu- mented (e.g. Liem, 1973) to be associated with the origin of key evolutionary novelties, i.e. the development of new, usually morpho- EVOLUTION OF CONIDAE 65 logical, attributes that satisfy several criteria (as modified from Herrera, 1989): (1) The novel feature is significant to the taxon and absent from its sister or ancestral groups; (2) Taxa with the feature diversify early in their evolutionary history; (3) Taxa with the feature become structur- ally and taxonomically more diverse than sis- ter taxa lacking it. Coddington (1988) uses a cladistic frame- work to test whether innovations are adapta- tions in the strict sense (of Gould & Vrba, 1982) of selection on a specific function pro- moting the origin, spread and maintenance of the innovative attribute, and driving taxo- nomic diversification. Lauder & Liem (1989) provide additional criteria and an explicit pro- cedure for testing the key innovation hypoth- esis. It involves mapping the hypothesized key innovation onto a phylogeny of the taxon and comparing morphometric analyses of this taxon and of outgroups. What innovative features of Conus might qualify? Hallmarks of the genus include: (1) the detachable, hollow, barbed, har- poon-like radular tooth individually injected via an extensile intraembolic proboscis during prey capture (Kohn et al., 1972); (2) the peptide venoms injected through the tooth that rapidly immobilize the prey (Olivera et al., 1985); (3) the characteristically broadly conical or biconical shell with parallel-sided aperture, typically with the last whorl covering most of the prior whorl so that the spire is quite low; and (4) the thick, heavy and strong crossed- lamellar last whorl of the shell, with the pro- tected inner walls later mainly dissolved away during extensive interior renovation (Kohn et al., 1979). At present, data are lacking in Conus to test these features against even those predictions of the key innovation hypothesis that do not require phylogenetic evidence. Moreover, the present lack of detailed comparative anatom- ical information on Conus means that other important innovative characters may remain to be discovered. At best we can indicate the present status of knowledge: (1) The general features of the Conus rad- ular tooth mentioned above are shared by nu- merous turrids, especially the subfamily Bor- soniinae; whether this is a sister taxon of Conus, its ancestral taxon, or neither is un- Known. The functional morphology of the pro- boscis of Conus and turrids is also very sim- ilar (Greene & Kohn, 1989; Kantor, 1990). (2) A venom apparatus morphologically similar to that of Conus also occurs in many taxa of Turridae, but nothing is Known of the chemical nature of the venom in the latter family. (3) Shell size, shape and thickness may meet all of the criteria. (4) Internal wall resorption occurs, but to a lesser extent than in Conus, in some Olividae as well as in Hemiconus and Conorbis. Key innovations may be quite subtle. As Mayr (1960) said, “Most evolutionary changes take place without the origin of new structures. . . . Most differences are merely shifts in proportions, fusions, losses, second- ary duplications, and similar changes,” that nevertheless can lead to “evolutionary ava- lanches.” In addition, the causal relationship of key innovations with subsequent taxonomic diversification may be quite indirect. Anatom- ical changes that provide selective advan- tages early in the evolution of a taxon may fortuitously support organisms of larger size at a later time in the evolution of a clade, as Bonner (1988) points out, as well as promoting speciation and the clade's radiation in a new adaptive zone. Shell form is the most likely candidate for the critical key evolutionary innovation of Co- nus. The depressed spire and broadly conical form permits the aperture to expand, particu- larly anteriorly and posteriorly. This in turn may have permitted thickening of the last whorl without reducing aperture size, and in- ternal wall thinning to retain a large living space within the shell, thus accommodating large prey organisms. The latter is likely es- pecially important in a predator that must en- gulf and swallow whole prey. A thick, resistant shell is an important defense against both crushing predators and physical factors in shallow, high-energy Cenozoic marine envi- ronments. The development of a shell form with these features, involving no anatomically new structures but mainly changes in propor- tions, and in combination with prior posses- sion of a well-developed harpoon-like radular tooth and venom apparatus, may have been the key innovation leading to the major radi- ations of Conus. At present this hypothesis is speculative, and tests, such as those pro- posed by Coddington (1988) and Lauder & Liem (1989), must await improved knowledge in an area presently completely unknown but certainly amenable to study, the phylogeny of 66 KOHN the Conidae. However, available evidence from the Paleogene and especially Neogene radiations suggest that strongly but stylishly shelled, Conus is a young, upwardly mobile, progressional genus, albeit at a snail's pace. ACKNOWLEDGMENTS This research was supported by NSF Grant BSR 8700523. | thank J. D. Taylor, R. J. Cleevely, C. P. Nuttall and N. J. Morris for discussion and for providing research facili- ties at The Natural History Museum, London, and N. F. Sohl, G. J. Vermeij and R. M. Lin- sley for helpful comments. LITERATURE CITED BONNER, J. T., 1988, The evolution of complexity. Princeton University Press, Princeton, 260 pp. CODDINGTON, J. A., 1988, Cladistic tests of ad- aptational hypotheses. Cladistics, 4: 3-22. COSSMANN, M., 1895-1896, Essais de paléoco- nchologie comparée, 1:58—69; 2:140-—163. Cossmann, Paris. COSSMANN, M. & G. PISSARRO, 1909, The Mol- lusca of the Ranikot Series. Memoirs of the Geo- logical Survey of India, New Series, 3: 1-83. DANIZOT, G., 1957, Nummulitique. Lexique Strati- graphique International, 1(4)a: 143-144. DAVIS, С. M., 1981, Introduction to the second In- ternational Symposium on Evolution and Adap- tive Radiation of Mollusca. Malacologia, 21: 1-4. DESHAYES, G. -P., & MILNE EDWARDS, H., 1845, Histoire naturelle des animaux sans ver- tèbres, 11. Paris, 665 pp. [EUDES-DESLONGCHAMPS, E.], 1837. Seance publique de la Societé Linnéenne de Normandie, tenue a Honfleur, le 28 juin 1837. Mémoires de la Societé Linneénne de Normandie, 6: 41-42. FISCHER, P., 1887, Manuel de conchyliologie. F. Savy, Paris, 1369 pp. FLEMING, J., 1822, The philosophy of zoology, or a general view of the structure, functions, and classification of animals. Archibald Constable & Co., Edinburgh, 565 pp. GEINITZ, H. B., 1850, Charakteristik der Schichten und Petrefacten des sachsisch-bohmischen Krei- degebirges. Arnold, Leipzig, 116 pp. GLIBERT, M., 1960, Les Conacea fossiles du cen- ozoïque etranger des collections de l'Institut Royal des Sciences Naturelles de Belgique. /n- stitut Royal des Sciences Naturelles de Belgique Memoires, 2nd ser., 64: 1-132. GOULD, S. J., 1988, Trends as changes in vari- ance: a new slant on progress and directionality in evolution. Journal of Paleontology, 62: 319— 329. GOULD, S. J. & E. S. VRBA, 1982, Exaptation—a missing term in the science of form. Paleobiol- ogy, 8: 4-15. GREENE, J. L. & A. J. KOHN, 1989, Functional morphology of the Conus proboscis (Mollusca: Gastropoda). Journal of Zoology, 219: 487—493. HAQ, B. U. & W. B. VAN EYSINGA, 1987, Geolog- ical time table, 4th ed. Elsevier, Amsterdam. HARLAND, W. B., A. V. COX, P. G. LLEWELLYN, C. A. G. PICKTON, A. G. SMITH & R. WAL- TERS, 1982, A geologic time scale. Cambridge University Press, Cambridge, 131 pp. HERRERA, C. M., 1989, Seed dispersal by ani- mals: a role in angiosperm diversification? Amer- ican Naturalist, 133: 309-322. KANTOR, Y., 1990, Anatomical basis of origin and evolution of toxoglossan mode of feeding. Mala- cologia, 32: 3-18. KEEN, A. M. & H. BENTSON, 1944, Check list of California Tertiary marine Mollusca. Geological Society of America Special Papers, 146: 1-280. KOHN, A. J., 1980, Conus kahiko, a new Pleis- tocene gastropod from Oahu, Hawaii. Journal of Paleontology, 54: 534-541. KOHN, A. J., 1981, Abundance, diversity, and re- source use in an assemblage of Conus species in Enewetak Lagoon. Pacific Science, 34: 359— 369. KOHN, A. J., 1982, Evolution of Indo-Pacific Conidae: A preliminary report. In KUSSAKIN, O. С. & A. |. KAFANOV, eds., Fauna and hydrogra- phy of the shelf zones of the Pacific Ocean. Pro- ceedings of the XIV Pacific Science Congress, Section ‘Marine Biology,’ Issue 4: 84-88. KOHN, А. J., Е. В. MYERS & V. В. MEENAKSHI, 1979, Interior remodeling of the shell by a gas- tropod mollusc. Proceedings of the National Academy of Sciences of the U.S.A., 76: 534— 541. KOHN, A. J., J. W. NYBAKKEN 4 J. J. VAN MOL, 1972, Radula tooth structure of the gastropod Conus imperialis elucidated by scanning electron microscopy. Science, 176: 49—51. LAUDER, G. V. & K. F. LIEM, 1989, The role of historical factors in the evolution of complex or- ganismal functions. In WAKE, D. B. & G. ROTH, eds., Complex organismal functions: integration and evolution in vertebrates, 63-78. Dahlem Konferenzen. Chichester: John Wiley & Sons. Ltd., in press. LIEM, K. F., 1973, Evolutionary strategies and mor- phological innovations: chichlid pharyngeal jaws. Systematic Zoology, 22: 425—441. LYELL, C., 1840, On the occurrence of two species of shells of the genus Conus in the Lias, or Infe- rior Oolite, near Caen in Normandy. The Annals and Magazine of Natural History, 6: 292-296. MATHERON, Р., 1842-1843, Catalogue méth- odique et descriptif des corps organisés fossiles due Département des Bouches-du-Rhone. Mar- seille, Carnaud, 269 pp. EVOLUTION OF CONIDAE 67 MAYR, E., 1960, The emergence of evolutionary novelties. In TAX, S., ed. Evolution after Darwin, 1: 349-380. Chicago, University of Chicago Press. MEEK, F. B., 1863, Remarks on the family Actae- onidae, with descriptions of some new genera and sub-genera. American Journal of Science, 2nd ser., 35: 84—94. MELVILLE, R. V. & E. C. FRESHNEY, 1982, The Hampshire basin and adjoining areas. British Re- gional Geology. Institute of Geological Sciences. London, HMSO, 146 pp. NEWELL, N. D., 1949, Phyletic size increase, an important trend illustrated by fossil invertebrates. Evolution, 3: 103-124. OLIVERA, B. M., W. R. GRAY, R. ZEIKUS, J. M. McINTOSH, J. VARGA, J. RIVIER, V. DeSAN- TOS & L. J. CRUZ, 1985, Peptide neurotoxins from fish-hunting cone snails. Science, 230: 1338—1343. D'ORBIGNY, A., 1850. Prodrome de paléontologie stratigraphique universelle des animaux mol- lusques & rayonnés, etc., V. |. V. Masson, Paris. D'ORBIGNY, A., 1852, Paléontologie francaise, 1re sér., 2:162-163. D'Orbigny, Paris. PICCOLI, G., 1984, Paleoecology and paleobio- geography: An example based on Paleogene shallow benthic mollusks from Venetian region (NE Italy). Geobios, Mémoire Spécial No. 8: 341— 347. PONDER, W. F. & A. WAREN, 1988, Classification of the Caenogastropoda and Heterostropha—A list of the family-group names and higher taxa. Malacological Review, Supplement 4: 288-317. POWELL, A. W. B., 1966, The molluscan families Speightiidae and Turridae. Bulletin of the Auck- land Institute and Museum, 2, 1-188. RAUP, D. M., 1976a, Species diversity in the Phan- erozoic: an interpretation. Paleobiology, 2: 289— 297. RAUP, D. M., 1976b, Species diversity in the Phan- erozoic: a tabulation. Paleobiology, 2: 279-288. ROSEN, B. R., 1988, Progress, problems and pat- terns in the biogeography of reef corals and other tropical marine organisms. Helgolánder Meere- suntersuchungen, 42: 269-301. SEED, R., 1983, Structural organization, adaptive radiation, and classification of molluscs. In НОСНАСНКА, P. W., ed., The Mollusca, 1: 1- 52. Academic Press, New York. SEPKOSKI, J. J. 1978. A kinetic model of Phaner- ozoic taxonomic diversity, |. Analysis of marine orders. Paleobiology, 4: 223-251. SIMPSON, G. G., 1953, The major features of ev- olution. New York. Columbia University Press, 434 pp. SOHL, N. F., 1964, Neogastropoda, Opisthobran- chia and Basommatophora from the Ripley, Owl Creek, and Prairie Bluff Formations. U.S. Geo- logical Survey Professional Paper, 331-B: 152- 344. ЗОНЕ, М. Е. & H. А. KOLLMANN, 1985, Creta- ceous actaeonellid gastropods from the western hemisphere. U.S. Geological Survey Profes- sional Paper, 1304: 1-104. STANLEY, S. M. 1975. A theory of evolution above the species level. Proceedings of the National Academy of Sciences, U.S.A. 72: 646-650. STANLEY, S. M., 1979, Macroevolution. W. H. Freeman, San Francisco. 332 pp. STEWART, R. B., 1927, Gabb's California fossil type gastropods. Proceedings of the Academy of Natural Sciences of Philadelphia, 78: 287-505. THIELE, J., 1931, Handbuch der systematischen Weichtierkunde, 1. Gustav Fischer, Jena, 778 pp. TOMLIN, J. R., leB., 1937, Catalogue of recent and fossil cones. Proceedings of the Malacological Society of London, 22: 205-330. VAN VALEN, L., 1971, Adaptive zones and the or- ders of mammals. Evolution, 25: 420—428. WALKER, T. D., 1985. Diversification functions and the rate of taxonomic evolution. In VALENTINE, J. W., ed., Phanerozoic diversity patterns, pp. 311-334. Princeton University Press, Princeton. WARING, C. A., 1917, Stratigraphic and faunal re- lations of the Martinez to the Chico and Tejon of Southern California. Proceedings of the Califor- nia Academy of Sciences, Series 4, 7: 41-124. WENZ, W., 1942, Gastropoda. Allgemeiner Teil und Prosobranchia. Handbuch der Paläozool- ogie, 6, part 1, 1639 pp. ZILCH, A., 1959—1960, Gastropoda. Teil 2. Euthy- neura. Handbuch der Paläzoologie, 6, part 2, 832 pp. Revised Ms. accepted 21 June 1990 MALACOLOGIA, 1990, 32(1): 69-77 TURRID GENERA AND MODE OF DEVELOPMENT: THE USE AND ABUSE OF PROTOCONCH MORPHOLOGY Philippe Bouchet Muséum National d'Histoire Naturelle, 55 Rue Buffon, 75005 Paris, France ABSTRACT Two contrasted protoconch morphologies (multispiral vs. paucispiral) are correlated in Tur- ridae, as in other Caenogastropoda, with modes of larval development (respectively plank- totrophic vs. non-planktotrophic). The multispiral vs. paucispiral dichotomy has been used ex- tensively to denote phylogeny and recognize genera, a practice unique to Turridae that resulted in Powell’s “phenomenon” of “turrid pairs.” Because planktotrophy can be lost repeatedly and independently from a given ancestor, Powell's system fails to provide a phylogenetic classifi- cation: it leads to artificial polyphyletic genera, each characterized by a single protoconch type, but not necessarily deriving from a common ancestor. A group of turrid species possessing multispiral and paucispiral protoconchs should not be split into different (sub)genera when their teleoconch, radula and anatomical characters otherwise indicate that a single clade is involved. However, sculptural types among planktotrophic type protoconchs are considered to have tax- onomic utility at supraspecific levels. Key words: Turridae, protoconch, larval development, taxonomy, phylogeny. INTRODUCTION With 679 genus-group taxa and probably as many as 10,000 Recent and fossil nominal species, the family Turridae ranks as the most speciose of all marine gastropods. Tryon (1884) was the last author to try to mono- graph the Recent species of the family world- wide. This task has probably been considered unrealistic by later authors, who have mostly been working on a regional and/or strati- graphic basis. Species-level taxonomy in the Turridae offers no more problem than in other marine gastropod families, except perhaps that large series of specimens are only rarely available for an appraisal of variation. By con- trast, considerable difficulty in recognizing good classificatory characters at supraspe- cific levels has been frequently expressed in the literature, emphasis being variously laid by different authors on conchological, radu- lar or anatomical characters. Controversy as to the value of the proto- conch as a guide to phylogeny has continued unabated over the years (Kilburn, 1983). In the present paper, | review how the proto- conch has been used by paleontologists and zoologists in supraspecific turrid taxonomy. | demonstrate that mode of larval development alone cannot be used to recognize genera or subgenera. | conclude that the so-called “turrid pairs” of genera are most likely to be polyphyletic and should be abandoned in 69 taxonomic practice in the family. Finally, | discuss the taxonomic utility of styles of orna- mentation and conclude that such morpholog- ical details are useful in planktotrophic proto- conchs. REVIEW The “Phenomenon” of “Turrid-pairs” As other marine prosobranchs, Turridae exhibit two major types of protoconchs: (a) a multispiral—Powell (1942) also used the term “polygyrate’—protoconch, with a small proto- conch |, and a protoconch II consisting of 2-5 whorls, often with an elaborate sculpture of ribs and cords; and (b) a paucispiral proto- conch, with no distinction between proto- conchs | and II, consisting of 1-2 whorls with a large nucleus, and a simpler, stouter sculp- ture, or no sculpture at all. Although protoconchs had been previously used by malacologists before in gastropod taxonomy, it was certainly Powell who first formalized a system using protoconchs in routine supraspecific taxonomy in the Tur- ridae. Through his monumental work on New Zealand and worldwide turrids (Powell, 1942, 1966), Powell has profoundly influenced modern taxonomic practice, and these two papers are cited in almost every paper on tur- 70 BOUCHET rid supraspecific taxonomy published in the last few decades. Powell's (1942) opinion is worth citing in full here: “A certain number of genera appear to occur in parallel series, being alike in adult shell features and evidently of common origin, but by their respective protoconchs they are separable into polygyrate and paucispiral se- ries. In all these instances | have treated these parallel developments as distinct gen- era, for differences in the embryo are surely of basic biological importance.” And further: “Much criticism has been levelled at the em- ployers of protoconch criteria in the family, but in all these objections the fault seems to lie in the failure of rigid application of these criteria. If we refuse to admit more than one style of protoconch in a genus these anomalies dis- appear.” On Роме! 5 authority, this opinion later be- came an established, almost unchallenged dogma entrenched in turrid taxonomic prac- tice, and genera have been and are being recognized based on this single character (e.g. Powell, 1942, 1964; van Aartsen & Fehr- de Wal, 1978; Gougerot & Le Renard, 1981; van Aartsen et al., 1984; Bernasconi & Robba, 1984; van Aartsen, 1988). Examples of such “turrid pairs” include: Mangelia Risso, 1826 (multispiral) / Mangi- liella Bucquoy, Dautzenberg & Dollfus, 1883 (paucispiral) (Fig. 1). Raphitoma Bellardi, 1847 (multispiral) / Philbertia Monterosato, 1884 (paucispiral). Bela Gray, 1847 (multispiral) / Fehria van Aartsen, 1988 (paucispiral). Lophiotoma Casey, 1904 (multispiral) / Lo- phioturris Powell, 1964 (paucispiral). Parasyrinx Finlay, 1924 (multispiral) / Lira- syrinx Powell, 1942 (paucispiral). Protoconch Morphology and Turrid Larval Development A general correlation between protoconch morphology and mode of larval development has been demonstrated (Thorson, 1946; Shuto, 1974; Robertson, 1976; Jablonski & Lutz, 1980, 1983) and may be examined here with reference to what is known of turrid larval biology. Most described turrid egg-capsules are ovoid and lenticular, with a central dorsal plug, and attached by the ventral side to the substrate (Lebour, 1934; Thorson, 1946; Knudsen, 1950; Bandel, 1976; Bouchet & Waren, 1980). A notable exception is the egg- capsules of the subfamily Clavatulinae, which are stalked and purse-shaped (Kilburn, 1985). A capsule contains several dozens to a few hundred eggs. Nurse eggs have not been reported. As is frequent with species with plank- totrophic larval development, the complete development, from oviposition to metamor- phosis, has not been followed for any single specimen, but evidence can be derived from numerous scattered and fragmentary data. Turrid veligers, although never abundant, are frequently recorded in meroplankton samples (Franc, 1950; Richter & Thorson, 1975; Le- bour, 1934; Thiriot-Quiévreux, 1969, 1972) and exhibit a broad range of morphological/ sculptural types (Kay, 1979, and personal observations). From published observations, the behaviour of such veligers is similar to that in other gastropod planktotrophic vel- igers, i.e. the larvae actively swim in the epi- pelagic layers of the water column while feed- ing on phytoplankton. These veligers have protoconchs of the multispiral type (Fig. 1a); the larvae of the many deep-sea turrids that undertake ontogenetic vertical migrations (Bouchet & Fontes, 1981; Killingley & Rex, 1985) enter into this category. The planktonic phase is a period of active feeding and very active growth, and the whole protoconch Il is secreted during this planktonic planktotrophic phase. The total length of the planktonic phase is not known with precision and cer- tainly varies between species, but by compar- ison with other prosobranch families a range from three to eight weeks is a likely estimate. The complete larval development of Oeno- pota levidensis (Carpenter, 1864), a species with paucispiral larval shell, has been de- scribed with considerable detail based on laboratory observations (Shimek, 1986). De- velopment to a veliger occurs within the egg- capsule in about 50 days. After hatching, the larvae swim actively for a period of a few days, and then live a demersal life on the bot- tom of the culture vessel. The larvae were experimentally fed with algal suspensions; shell and velar dimensions increase during the swimming phase, after which the veliger does not get appreciably larger, and by the 15th posthatching day, the protoconchs are fully formed. Demersal development then continues without shell growth and the veligers metamorphose after 25 days. Based on these observations, Shimek (1986) concludes that paucispiral proto- TURRID PROTOCONCH TA FIG. 1. The multispiral (1a) and paucispiral protoconch (1d) define respectively the genera Mangelia and Mangiliella. There is no evidence that Mangelia striolata Risso, 1826, (1b) and M. vauquelini (Payraudeau, 1826) (1c) are more closely related to each other than they are to Mangiliella multilineolata (Deshayes, 1833) (1е) or M. taeniata (Deshayes, 1833) (1f). Mangiliella should be synonymized with Mangelia. 1b = 7.8 тт; 1c = 9.0 mm; le = 5.7 mm; 1f = 5.5 mm. Scale lines 200 um. All specimens from Calvi, Corsica. conchs in turrids cannot be interpreted as ev- idence for lack of a planktonic stage, as claimed by Thorson (1935, 1946). A develop- ment with intracapsular metamorphosis had been inferred in Atlantic Arctic Oenopota by Thorson from the contents of egg capsules, because there is no appreciable size differ- ence between the shells of intracapsular em- bryos ready to hatch and the smallest benthic juveniles. Shimek’s observations certainly demonstrate that a long demersal phase may occur in species with paucispiral larval shells. However they do not, in my opinion, weaken the distinction between planktotrophic and non-planktotrophic larval development. | fully admit that the duration of the post-hatching phase in O. levidensis may probably equal the duration of some of the shorter-lived planktonic planktotrophic veligers. The short initial free-swimming planktonic phase aside (though this is admittedly important in terms of dispersal), the biology of the veliger of O. levidensis is markedly different from that of planktotrophic veligers: it does not swim, ex- cept for brief moments following artifical stim- ulation, and it does not grow or secrete pro- 72 BOUCHET toconch shell material. By contrast with species with multispiral protoconchs, the iso- topic composition of the shells of deep-water turrids with paucispiral protoconchs indicates that a vertical ontogenetic migration does not occur (Killingley & Rex, 1985). Just as the duration of the planktonic phase varies among species with planktotrophic de- velopment, the duration of the swimming and demersal phases may be expected to vary considerably between species with non- planktotrophic development. Whether the case of Oenopota levidensis represents an average duration or an extreme is not known. Kilburn's (1985) observation that in the pau- cispiral protoconch of Clavatula tripartita (Weinkauff, 1876) ‘the defining varix pre- cedes the veliconch lip by about one-sixth of a whorl” may be an indication that a swimming phase is also present. Clearly, more data are needed on the the larval biology of additional species. In particular, it would be of great interest to know if the larval biology of warm- water turrids with paucispiral larval shells con- forms to the pattern described for the cold- water Oenopota levidensis. Knudsen (1950) described the egg-capsules and contained embryos of several West African continental shelf turrids, and inferred lecithotrophic or “direct” development. Non-planktotrophic lar- val development has been inferred from pro- toconch morphology in numerous temperate, tropical and deep-water turrids. Available evidence in the family Turridae therefore confirms the general correlation be- tween protoconch morphology and mode of development. This correlation, which had been assumed by Powell (1942 and later pa- pers) based on the data then available in other prosobranch families, is applicable to Recent as well as fossil turrids. Polarity of Changes in Protoconch Morphology Although the mode of development, and hence protoconch morphology, is a species- specific character throughout the range of a species (Hoagland & Robertson, 1988; Bouchet, 1989), it is known to change through time in monophyletic lineages (see refer- ences below). Powell (1942), certainly influenced by Fin- lay (1931), believed the paucispiral proto- conch / “sedentary larva” type to represent the ancestral condition, and the multispiral protoconch / “free swimming larva” type to represent the derived condition. He moreover believed this change ot be irreversible: “When once the radical embryonic change from a sedentary to a free swimming larva takes place, both types appear to develop in- dependently, for there is no evidence sug- gesting indiscriminate change and rechange between these two types of embryos. It would seem rather that the ‘Sinusigera’ apex is an evolutionary culmination from the less effi- cient paucispiral type.” This is, | think, a good example of circular reasoning. How can changes in protoconch morphology be recog- nized if, by definition, they are used to distin- guish genera? Contrary to Powell's assumption, the evi- dence throughout marine invertebrates is that planktotrophic larval development represents the ancestral (plesiomorphic) condition and the loss of planktotrophy is a derived (apo- morphic) condition (Strathmann, 1978, 1985). Strathmann (1978), however, argues that the loss of planktotrophy is in theory reversible as long as the larval ciliary opposed band sys- tem of feeding is not lost during intracapsular development. Such is the case in Oenopota levidensis (Shimek, 1986), so that reacquisi- tion of planktotrophy is in theory possible in a descendant of that species. The final answer to this question can only be found in the study of modes of develop- ment in fossil and Recent species, because biological time is too short for an approach other than theoretical. However, in the Tur- ridae, there are presently no available data that combine (a) description of a small lineage through time, and (b) description of proto- conch types without a preconceived idea on their significance in classification. Fragmentary data are scattered throughout the taxonomic literature on Caenogas- tropoda: in Neogene to Recent eastern Atlan- tic Terebridae (Bouchet, 1981); in Paris Basin Eocene Triforis (Gougerot & Le Renard, 1980); in Pliocene to Recent Mediterranean nassariids (Martinell & Cuadras, 1977) and Trophon (Bouchet & Warén, 1985); in Neo- gene to Recent eastern American Ficus (Smith, 1945); in North American Paleogene Volutidae (Hansen, 1983). All these papers point out many examples of changes from multispiral to paucispiral protoconchs (loss of planktotrophy), but not a single case of change from paucispiral to multispiral proto- conchs (reacquisition of planktotrophy) is re- corded. Therefore, although reacquisition of planktotrophy is theoretically embryologically TURRID PROTOCONCH 73 feasable, evidence is still wanting, and in this paper my working hypothesis is that the loss of planktotrophy in Turridae is, as a rule, not a reversible phenomenon. Refutation of Mode of Development as a Generic Character If Powell’s system of genera was applicable to Turridae, it should equally be applicable, on the same basis, to other families of marine gastropods. As reviewed above, protoconch morphology correlates with mode of develop- ment. If the planktotrophic / non-plankto- trophic dichotomy is to be given generic value in the Turridae, then logically it should also be given the same value in other Caenogas- tropoda. However, there are many examples of genera (e.g. Nassarius, Chicoreus, Alva- nia, Littorina) that are believed to be mono- phyletic and that contain both species with planktotrophic and non-planktotrophic larval development. As a matter of fact, there are sibling species in many genera that are dis- tinguished only on the basis of their mode of development (Hoagland & Robertson, 1988; Bouchet, 1989). Recognition of genera based only on the paucispiral vs. multispiral dichot- omy has been explicitly rejected by Robert- son (1976) in general and by Marshall (1978, 1983) in the families Cerithiopsidae and Triphoridae. The practice is indeed quite re- stricted to Turridae (but has already been challenged by Kilburn, 1983), but it is not jus- tified by any larval biology feature that would be unique to turrids. Genera that are established on the pau- cispiral vs. multispiral dichotomy are prone to be artificial and polyphyletic. | have in Figures 2 and 3 presented a hypothetical evolutionary tree starting from an ancestor with multispiral larval shell. Through speciation and anage- netic evolution, this ancestral species (P 1) gives rise to local shorter-lived species that have lost planktotrophy (L 1 to L 4), and longer-lived species that retain planktotrophy (P 2 to P 5). That species with non-plank- totrophic development are more local and outlived by species with planktotrophic devel- opment has been both predicted (Scheltema, 1977), and noticed (Powell, 1942; Hansen, 1978, 1980, 1983; Jablonski, 1982, 1986) in the fossil record. Loss of planktotrophy can occur independently several times through various evolutionary scenarios, such as insu- lar endemism or relict distribution resulting from changes in the climatic and/or geo- FIGS. 2-3. Hypothetical evolutionary tree of a turrid lineage. In Powell's system of genera (Fig. 2, above), the species with paucispiral protoconchs are grouped in one genus, although they do not share a common ancestor, and the species with multispiral protoconchs in another genus. Such genera are respectively polyphyletic and paraphy- letic. In the absence of detailed knowledge on the tree (and this is by far the most frequent situation in Turridae), the most parsimonious solution is a sin- gle genus comprising species both with multispiral and paucispiral protoconchs (Fig. 3, below). 74 BOUCHET FIG. 4. Loss of planktotrophy may permit an adaptive radiation. This character may then be expressed in classification. A genus defined by a paucispiral protoconch is monophyletic and perfectly acceptable. All species with paucispiral protoconch are derived from a common ancestor. graphic environments. According to Роме! 5$ system, all species with paucispiral larval shells (L 1 to L 4) are classified into one ge- nus, and species with multispiral larval shells (P 1 to P 5) in another. It is obvious that any one of species L 1, L 2, or L 4 is more closely related to its immediate ancestor with multi- spiral larval shell than it is to other species with the same protoconch morphology. The genus L is not based on parental affinities and should therefore be rejected. | would there- fore regard as valid a single genus encom- passing all the species descended from P 1, whatever their mode of larval development. In other words, when teleoconch, radula and anatomical characters indicate that a sin- gle evolutionary clade is involved, protoconch morphology should not be used to split it into different genera based on the mode of devel- opment. Subgenera based on the same con- cept are no more acceptable, since their poly- phyletism would not be more justifiable. This view is not revolutionary in turrid taxonomy, and a number of authors have already al- lowed differing modes of development to co- exist within a single turrid genus (e.g. Bouchet & Warén, 1980; Kilburn, 1983; Maes, 1983). It may be worth noting, at this point, that even if the loss of planktotrophy was, contrary to my assumption, reversible, then the above conclusion remains valid. This does not of course necessarily mean that all turrid genera have or should have both species with paucispiral and species with multispiral protoconchs. Loss of planktotro- phy may represent the onset of an adaptive radiation, such as in an insular or polar envi- ronment (Fig. 4). All known Recent Oenopota have paucispiral protoconchs (Bogdanov, 1989), and all Pliocene Oenopota apparently already had the same mode of development (Harmer, 1914-19; Beets, 1946). Although | TURRID PROTOCONCH 75 fully expect that somewhere in the ancestry of Oenopota there is a species with multispiral larval shell, it is obvious that the loss of plank- totrophy has permitted an adaptive radiation in the arctic/subarctic environment where planktotrophy is selected against, and a pau- cispiral protoconch is now certainly a hallmark of Oenopota. Admittedly, each of the successive specia- tion events by loss of planktotrophy in Figure 2 represents a discrete radiation event, and one could imagine a nomenclature with L 1, L2 + L3, and L 4 each т a different genus. In my view, this should not be recommended in the present state of our knowlege: much of our genus-level and species-level taxon- omy is based on shell characters only, and this is all we will ever have in the many fossil taxa. The state of the art in turrid taxonomy is such that these discrete monophyletic genera cannot be easily recognized. Splitting and recognition of many monotypic genera with paucispiral larval shell will not help our under- standing of turrid evolution and, considering the sheer size of the family, is most likely to result in absolute chaos. What Future for the Turrid Protoconch as a Supraspecific Character? After all that has been said above, is there a future left for the use of protoconch in turrid taxonomy? That the paucispiral vs. multispiral dichotomy has no supraspecific taxonomical significance does not imply that just any kind of protoconch is to be expected in a turrid genus. The consequence of the genus concept ad- vocated here is that paucispiral protoconchs should only be compared with paucispiral pro- toconchs, and multispiral protoconchs with multispiral protoconchs. Accompanying the loss of planktotrophy, paucispiral protoconchs have few distinctive characters (See however Bodganov, 1989), and extensive parallelism and convergence between distant, unrelated taxa is the rule. It is very unlikely that these protoconchs have a promising future in turrid classification. By contrast, as has been noted above, the mor- phology and sculpture of planktotrophic turrid veligers is remarkably diverse and present a vast array of characters that have not yet been fully appreciated. | believe that different sculptural types within the multispiral proto- conch have a profound taxonomic meaning, just as teleoconch characters happen not to be random within a genus. Neopleuroto- moides was segregated from Pleurotomella despite extremely similar teleoconchs, be- cause the sculpture of their multispiral proto- conchs differ fundamentally (Shuto, 1971): re- spectively two spiral keels with axial pillars, and diagonal cancellation extending over most of the whorl. (It is worth noting here that, at this stage of our knowledge, a species with paucispiral larval shell cannot be attributed to Pleurotomella or Neopleurotomoides, an ob- vious difficulty with the genus concept advo- cated in the present paper.) What remains for the future is to identify what are the basic sculptural types, evaluate the degree of convergence (for instance, has the diagonally cancellated sculpture ap- peared only once?), and understand how sec- ondary sculptural types can be derived from more fundamental ones. There is certainly a rich and rewarding future use of turrid proto- conchs in taxonomy. LITERATURE CITED AARTSEN, J. J. van, 1988, European Mollusca: Notes on less well-known species. XII. Bela men- khorsti nom. nov. = Pleurotoma nana Scacchi, 1836 non Deshayes, 1835 and Fehria (nov. gen.) zenetouae nov. spec. La Conchiglia, 232/233: 30-31. AARTSEN, J. J. VAN & M. C. FEHR- DE WAL, 1978, The subfamily Mangeliinae Fischer, 1887 in the Mediterranean. Conchiglie, 14: 97-110. AARTSEN, J. J. van, H. P. MENKHORST 4 E. GIT- TENBERGER, 1984, The marine Mollusca of the Bay of Algeciras, Spain, with general notes on Mitrella, Marginellidae and Turridae. Basteria, supplement 2: 1-135. BANDEL, K., 1976, Spawning, development and ecology of some higher Neogastropoda from the Caribbean Sea of Colombia (South America). Veliger, 19: 176-193. BEETS, C., 1946, The Pliocene and lower Pleis- tocene gastropods in the collections of the Geo- logical Foundation in the Netherlands (with some remarks on other Dutch collections). Mededeelin- gen van de Geologische Stichting, (C, 4) 1 (6): 1-166, 6 pls. BERNASCONI, M. P. & E. ROBBA, 1984, The Pliocene Turridae from Western Liguria. 1. Cla- vinae, Turrinae, Turriculinae, Crassispirinae, Bor- soniinae, Clathurellinae. Bollettino del Museo Regionale di Scienze Naturali, Torino, 2: 257— 358: BOGDANOV, J. P., 1989, Morphological transfor- mation in radula and protoconch of Oenopotinae Bogdanov, 1987. La Conchiglia, 233/236: 35- 47. 76 BOUCHET BOUCHET, P., 1981, Evolution of larval develop- ment in eastern Atlantic Terebridae, Neogene to Recent. Malacologia, 21:363-369. BOUCHET, P., 1989, A review of poecilogony in gastropods. Journal of Molluscan Studies, 55: 67-78. BOUCHET, P. & J. C. FONTES, 1981, Migrations verticales des larves de gasteropodes abyssaux: arguments nouveaux dus à l'analyse isotopique de la coquille larvaire et postlarvaire. Comptes Rendus des Séances de l'Académie des Sci- ences, Paris, (3)292: 1005-1008. BOUCHET, P. & A. WAREN, 1980, Revision of the North-East Atlantic bathyal and abyssal Turridae. Journal of Molluscan Studies, supplement 8: 1— 120. BOUCHET, P. & A. WAREN, 1985, Revision of the Northeast Atlantic bathyal and abyssal Neogas- tropoda, excluding Turridae. Bollettino Malaco- logico, supplement 1: 121-296. FINLAY, H. J., 1931, On Austrosassia, Austro- harpa, and Austrolithes, new genera; with some remarks on the gastropod protoconch. Transac- tions of the New Zealand Institute, 62: 7-19. FRANC, A., 1950, Ponte et larves planctoniques de Philbertia purpurea (Montagu). Bulletin du Labo- ratoire Maritime de Dinard, 33: 23-25. GOUGEROT, L. & J. LERENARD, 1980, Clefs de détermination des petites espèces de gas- téropodes de | Eocene du bassin parisien. XII. La famille des Triphoridae. Cahiers des Naturalistes, 35: 41-59. GOUGEROT, L. & J. LERENARD, 1981, Clefs de determination des petites especes de gas- téropodes de l'Eocène du bassin parisien. XIX. Le genre Pleurotomella. Cahiers des Natura- listes, 37: 81-92. HANSEN, T., 1978, Larval dispersal and species longevity in lower Tertiary gastropods. Science, 199: 885-887. HANSEN, T., 1980, Influence of larval dispersal and geographic distribution on species longevity in neogastropods. Paleobiology, 6: 193-207. HANSEN, T., 1983, Modes of larval development and rates of speciation in early Tertiary neogas- tropods. Science, 204: 501-502. HARMER, Е. W., 1914-1919, The Pliocene Mol- lusca of Great Britain, volume 1. Palaeonto- graphical Society, London. HOAGLAND, K. E. & R. ROBERTSON, 1988, An assessment of poecilogony in marine inverte- brates: phenomenon or fantasy? Biological Bul- letin, 174: 109-125. JABLONSKI, D., 1982, Evolutionary rates and modes in late Cretaceous Gastropods: role of lar- val ecology. Proceedings of the Third North Amer- ican Paleontological Convention, 1: 257-262. JABLONSKI, D., 1986, Larval ecology and macro- evolution in marine invertebrates. Bulletin of Ma- rine Science, 39: 565-587. JABLONSKI, D. & R. LUTZ, 1980, Molluscan larval shell morphology. Ecological and paleontological applications. In RHOADS, D.C. & R. LUTZ, eds., Skeletal Growth of Aquatic Organisms, 323-377. Plenum Press, New York. JABLONSKI, D. & R. LUTZ, 1983, Larval ecology of marine benthic invertebrates: paleobiological im- plications. Biological Reviews, 58: 21-89. KAY, A., 1979, Hawaiian marine shells. В. P. Bishop Museum Special Publication, 64: 1-653. KILBURN, В. N., 1983, Turridae of southern Africa and Mozambique. Part 1. Subfamily Turrinae. Annals of the Natal Museum, 25: 549-585. KILBURN, В. N., 1985, Turridae of southern Africa and Mozambique. Part 2. Subfamily Clavatuli- nae. Annals of the Natal Museum, 26: 417—470. KILLINGLEY, J. & M. REX, 1985, Mode of larval development in some deep-sea gastropods indi- cated by oxygen-18 values of their carbonate shells. Deep Sea Research, 32:809-818. KNUDSEN, J., 1950, Egg capsules and develop- ment of some marine prosobranchs from tropical West Africa. Atlantide Report, 1: 85-130. LEBOUR, M., 1934, The eggs and larvae of some British Turridae. Journal of the Marine Biological Association of the United Kingdom, 19: 541-554. MAES, V. O., 1983, Observations on the systemat- ics and biology of a turrid gastropod assemblage in the British Virgin Islands. Bulletin of Marine Science, 33: 305-335. MARSHALL, B., 1978, Cerithiopsidae of New Zealand, and a provisional classification of the family. New Zealand Journal of Zoology, 5: 47— 120. MARSHALL, B., 1983, A revision of the Recent Triphoridae of Southern Australia. Records of the Australian Museum, supplement 2: 1-119. MARTINELL, J. & C. CUADRAS, 1977, Bioestadis- tica y analysis multivariable aplicados a la com- paracion de una poblacion actual y otra fosil, atribuidas a Sphaeronassa mutabilis (Linne): aportacion a la sistematica del genero Sphaero- nassa Locard, 1886. Studia Geologica (Sala- тапса), 13: 89-103. POWELL, A. W. B., 1942, The New Zealand Re- cent and fossil Mollusca of the family Turridae. Bulletin of the Auckland Institute and Museum, 2: 1-188. POWELL, A. W. B., 1964, The family Turridae in the Indo-Pacific. Part 1. The subfamily Turrinae. Indo-Pacific Mollusca, 1(5): 227-345. POWELL, A. W. B., 1966, The Molluscan families Speightiidae and Turridae. Bulletin of the Auck- land Institute and Museum, 5: 1-184, 23 pls. RICHTER, G. & G. THORSON, 1975, Pelagische Prosobranchier-Larven des Golfes von Neapel. Ophelia, 13: 109-185. ROBERTSON, R., 1976 (“1974”), Marine proso- branch gastropods: larval studies and systemat- ics. Thalassia Jugoslavica, 10: 213-238. SCHELTEMA, R., 1977, Dispersal of marine inver- tebrate organisms: paleobiogeographic and bio- stratigraphic implications. In KAUFFMANN, E. G. & J. E. HAZEL, eds., Concepts and Methods of Biostratigraphy, 78-122. Dowden, Hutchinson and Ross, Stroudsburg. TURRID PROTOCONCH 77 SHIMEK, В. L., 1986, The biology of the northwest- ern Pacific Turridae. V. Demersal development, synchronous settlement and other aspects of the larval biology of Oenopota levidensis. Interna- tional Journal of Invertebrate Reproduction and Development, 10: 313-333. SHUTO, T., 1971, Taxonomical notes on the turrids of the Siboga-collection originally described by М. М. Schepman, 1931 (part III). Venus, 30(1): 5=22. SHUTO, T., 1974, Larval ecology of prosobranch gastropods and its bearing on biogeography and paleontology. Lethaia, 7: 239—256. SMITH, B., 1945, Observations on gastropod pro- toconchs. Paleontographica Americana, 3: 1—48. STRATHMANN, R., 1978, The evolution and loss of feeding larval stages of marine invertebrates. Evolution, 32: 894—906. STRATHMANN, В., 1985, Feeding and nonfeeding larval development and life-history evolution in marine Invertebrates. Annual Review of Ecology and Systematics, 16: 339-361. THIRIOT-QUIEVREUX, C., 1969, Caractéristiques morphologiques des véligères planctoniques de gastéropodes de la région de Banyuls-sur-mer. Vie et Milieu, (B)20: 333-336. THIRIOT-QUIEVREUX, C., 1972, Microstructures de coquilles larvaires de prosobranches au mi- croscope électronique a balayage. Archives de Zoologie Expérimentale et Générale, 113: 553— 564. THORSON, G., 1935, Studies on the egg-capsules and development of arctic marine prosobranchs. Meddelelser om Gronland, 100: 1-71. THORSON, G., 1946, Reproduction and larval de- velopment of Danish marine bottom inverte- brates, with special reference to the planktonic larvae in the sound. Meddelelser fra Kommis- sionen for Danmarks Fiskeri- og Havunderso- gelser (Plankton), 4: 1-523. TRYON, G. W., 1884, Manual of Conchology, vol. VI. Conidae, Pleurotomidae. 413 pp., 34 pls. Phil- adelphia. Revised Ms. accepted 21 June 1990 MALACOLOGIA, 1990, 32(1): 79-87 TURRID FAUNAS OF PACIFIC ISLANDS E. Alison Kay Department of Zoology, University of Hawaii, Honolulu, Hawaii, U.S.A. 96822 ABSTRACT Of the more than 300 species in 45 genera and seven subfamilies of Turridae described or recorded from the shallow waters (<100 m) of the tropical Pacific, 160 species are recognized as occurring on the islands of the central Pacific. Compared with the turrids of continental shorelines (tropical west America and New Zealand), the Daphnellinae are better represented and the Clavinae less well represented on central Pacific islands. The turrids in general comprise a lesser proportion of the gastropod fauna, and shells in all turrid subfamilies are smaller on average. Species distribution is patchy and endemism is high in the Hawaiian Islands (47%) and at Easter Island (80%). Less than 30% of the central Pacific turrids are widespread in the Indo-Pacific, nearly 40% also occur in the western Pacific, and about 30% are known only from the Pacific Plate. Nearly 50% of the genera represented on the Pacific Plate apparently lack a fossil record. Key words: Turridae, biogeography, Indo-Pacific, distribution, island faunas. INTRODUCTION Members of the neogastropod family Tur- ridae are among the most numerous of ma- rine gastropods. The family may include as many as 2,000 Recent species (Kilburn, 1983), 550 (Powell, 1966; McLean, 1971) to 679 (Bouchet, 1990) generic and subgeneric units, and from 9 to 15 subfamilies (Powell, 1966; McLean, 1971). Turrids are found throughout the world from the poles to the tropics, and from intertidal coral reefs to depths of more than 5,000 m in the abyssal regions of the sea. They can be both abun- dant and speciose. In the deepwaters of the Atlantic, they are the most abundant mollusc group in terms of both number of specimens and number of species (Bouchet & Waren, 1980), and more than 30% of the described Alaskan, Arctic, and North Pacific boreal shal- low-water gastropods are turrids (Shimek, 1986). Turrids of the tropical Pacific Ocean are not so easily quantifiable, despite the fact that more than 900 species names have been proposed or recorded for turrids in that area. This study represents an initial analysis of turrid species composition and distribution in three major island groups in the central Pa- cific, the Marshall Islands (Enewetak), the Ha- waiian Islands, Tahiti and the Tuamotus (French Polynesia). The turrids from these is- lands are also examined in terms of several of the generalizations now recognized as per- taining to the distribution of marine organisms 79 in the Pacific (cf. Kay, 1980; Kay, 1984). Is there an attenuation of species and higher taxonomic groups from west to east across the Pacific? Are the relationships of Pacific island turrids to the west rather than the east? Is there a distinctive Pacific Plate element in the fauna? MATERIALS AND METHODS Collections A long-term study of the turrids of Pacific islands, particularly those of the Hawaiian Is- lands; Enewetak, Marshall Islands; Fanning Island, Line Islands; and Guam, Mariana Is- lands, has permitted collection in the field and comparison of field-collected material with type and reference collections in the Acad- emy of Natural Sciences Philadelphia (Pease and Garrett types); Australian Museum, Syd- ney (Hedley and Laseron collections); B. P. Bishop Museum, Honolulu, Hawaii (Thaanum collection of Okinawan turrids and material identified by Dall); The Natural History Mu- seum, London (Cuming collection, Reeve types, Melvill and Standen material); the Musée d'Histoire Naturelle, Paris (Hervier, Crosse and Souverbie types); the Museum of Comparative Zoology, Harvard University (Pease collection); the National Museum of Natural History, Smithsonian Institution, Washington, D.C. (Dall, Pease and Garrett 80 TABLE 1. Numbers of turrid species described from the Pacific 1800-present. Western Pacific includes the Philippines, Queensland, Malayan archipelago, Lifu, Fiji. Fossil species included. WESTERN PRINCIPAL CENTRAL PRINCIPAL YEAR PACIFIC AUTHORS PACIFIC AUTHORS 1800—1825 В Lamarck 1826—1850 138 Reeve, Hinds 14 Reeve 1851-1875 48 Garrett, Gould, Souverbie 61 Garrett, Pease, Dunker 1876-1900 203 Hervier, Melvill and Standen 8 Dall, Smith 1901-1925 241 Hedley, Schepmann 4 Dall 1926-Present 74 Ladd, McNeil, Shuto, Noda 26 Kay, Powell material; Ladd Enewetak and Bikini fossil types); and the National Museum of Wales, Cardiff (Tomlin collection). | rely also on the published work of Dautzenberg & Bouge (1933), Hedley (1922), Hervier (1896-1898), Melvill & Standen (1895-1897), and Richard (1982) to augment species lists compiled from museum and field collections. Turrid Taxonomy Turrid taxonomy remains a major problem inthe understanding of turrid systematics and distribution. The importance of radular studies in the Turridae has been discussed by McLean (1971) and Kilburn (1983, 1985, 1988). The nature of the material that serves as the bases for this study for the most part precluded study of radulae, and placement of turrids in subfamilies herein is largely based on conchological features recognized by Powell (1942, 1966), that is, position of the sutural gap and protoconch type. Although it is widely recognized that shell type can no longer be considered a valid generic or sub- generic criterion, | nevertheless find that pro- toconch form does seem to provide insight into subfamilial placement of many turrid spe- cies. Seven subfamilies are recognized here as occurring in the island Pacific, the Turrinae of Powell (1966, 1967, but excluding Turri- drupa); Crassipirinae (of Kilburn, 1983, in- cluding Turridrupa); the Drilliinae sensu McLean (1971) and Kilburn (1988); the Mangeliinae and Daphnellinae sensu Powell (1966); the Borsoniinae, as recognized by Kilburn (1986); and the Cochlespirinae (of Powell, 1966). To arrive at an estimate of the numbers of turrid species associated with the tropical Pa- cific sensu lato and specifically with the is- lands of the central Pacific, the number of tur- rid species described from the western Pacific (Philippines, Queensland, Lifu, New Caledonia, Fiji) and the central Pacific (Ha- waii, French Polynesia, Samoa, etc.) was counted, and other species referred to the Pa- cific included in the list. More than 850 turrid species have been described from the Pacific (sensu lato) since 1800, of which less than 15% were described from islands in the cen- tral Pacific (Table 1). An additional 75-100 species have been recorded from the tropical Indo-Pacific, for example species described from Réunion by Deshayes and the northern Indian Ocean by Nevill. The total list was then culled for synonyms and other errors and is here reduced to about 160 species referable to the central Pacific islands. Pacific Island Biogeography Definitions utilized to delimit the islands of the central Pacific and their associated bio- geographic regions, the Indo-Pacific and the western Pacific (Fig. 1) are as follows. By Indo-Pacific is meant “the Indian Ocean in- cluding contiguous seas, and the Pacific Ocean as far east as Easter Island but ex- cluding the area occupied by the coast and offshore islands . . . of the Western Hemi- sphere” (Springer, 1982). The western Pa- cific is distinguished as the Pacific Ocean west of the western margin of the Pacific litho- spheric plate which includes such inland seas as the South China Sea, Arafura Sea, and Coral Sea (Springer, 1982), and the islands of Lifu (Loyalty Islands), Fiji, Okinawa (Ryukyu Islands) and Guam (Mariana Islands). The “Pacific islands” of this study (Enewetak, Marshall Islands; Hawaii; and Tahiti and Tu- amotus, French Polynesia) are primarily on non-marginal portions of the Pacific Plate. THE TURRIDS OF PACIFIC ISLANDS The distribution of the currently recognized 160 species in six subfamilies is shown in Fig- TURRID FAUNAS OF PACIFIC ISLANDS 81 ap A . e “Drs Y A\zuits Midway. OGASAWARA ADALLOEN : »Minamı Той on ar Okino Tori MARIANA Wake :] 15 Hawall i> REVILLAGIGEDO 1$ -- * Johnston Buan MARSHALL Four : | DE SC €, Pal almyra Fars 49 Ки! o Baker Jarvis - 4 PHOENIX 4 CON | © Howland a 4 4 Soe: Jawa Sram, N NER % a) SIERT SE DC № 1S ES ——_- N COOK - :. MARQUESAS il ai LISTE “2. ISLANDS or, UN <>. 2 » . Rotuma ‘ . Uves SAM CA SOCIETY. : Is 3 sans $ “Fulda =" 2 Levy o Y Me С. S > ‘Niue ° Be: Tahiti ” a . News LOT Is © € Rarotonga - = | yo Ss areca “PITCAIRN 'S Pitcairn к Eg SD. У у an Celedonia «Tongatapu AUSTRALIA + Norfolk * KERMADEC IS Lord Howe NEW ZEALAN orth Island Le A TASMANIA | ) una + CHATHAM IS o 150 Stewart 180° FIG. 1. The Pacific Ocean showing the margins of the Pacific Plate and major island groups. ure 2. About 90% of the Pacific island turrids represent four subfamilies: the Mangeliinae (43%), the Daphnellinae (29%), the Drilliinae (9%), and Turrinae (7%). The remaining tur- rids include the Crassispirinae (7%), Borsoni- inae (4%), and Cochlespirinae (1%). Subfam- ily representation confirms Powell's (1966) summary of turrid distribution in the Pacific: “In the atolls, reefs and small isolated island groups of the Indo-Pacific, large turrids are either absent or poorly represented: Lo- phiotoma acuta is almost the only exception, the faunules being composed mainly of small mangelinids and daphnellids. The most char- acteristic mangelinid genera of the islands of the Indo-west Pacific are Eucithara, Lienar- dia, Etrema, Macteola, .. .”. More than 80% of the turrid species asso- ciated with central Pacific islands are small (<5 mm in length), and the shells are sturdy and colorful. Except in the turrines and the deep-water daphnellines, shell form is marked by a short siphonal canal and usually reinforced labial extremity. Most of the shells also represent subfamilies that are character- ized by elaborate protoconchs (i.e. Daphnel- linae and Mangeliinae). Veligers of daphnel- lines and mangelines in Hawaii have been raised for periods of several weeks (J. В. Tay- lor, 1975). /redalea exilis (Pease, 1868) (Dril- linae) among the shallow water turrids is the only species with the protoconch of the type associated with direct or lecithotrophic devel- opment. Most of the central Pacific island turrids are known from depths of less than 30 m, and are commonly found at depths of 10-20 т on the fore-reef in rubble and sand. Only one spe- cies, /redalea exilis, is frequently found in the intertidal on reef flats. Eleven species are re- corded from depths of more than 300 m, nine species dredged in the Hawaiian Islands and two-Pleurotomella dubia Schepmann, 1913, and P. allisoni Rehder & Ladd, 1973-dredged from depths of more than 1,000 m on guyots in the mid-Pacific mountains (Rehder & Ladd, 1973). The shallow water turrids of central Pacific islands are neither numerous nor abundant. Turrids feed mainly on polychaetes (J. D. Tay- lor, 1977; Maes, 1983), and they comprise about 15% of the predatory gastropod spe- 82 Subfamilies (%) w о КАУ 8 Turr = Mang Crass E Daph Drill Borson FIG. 2. Subfamily composition in Pacific Turridae. QLD, Queensland; OKIN, Okinawa; GUM, Guam; ENE, Enewetak, HAW, Hawaii; FPOL, French Polynesia. Turr, Turrinae; Crass, Crassispirinae; Drill, Drilliinae; Mang, Mangeliinae; Daph, Daphnellinae; Borson, Borsoniinae. cies, in contrast to 27% and 25% respectively in New South Wales and New Zealand (Ire- dale & McMichael, 1962; Powell, 1979); 31% on the tropical west American coast (Keen, 1971); and an average of 7% on islands in the Indian Ocean (J. D. Taylor, 1977). Little is known of turrid biology in the Pacific, although J. D. Taylor (1984, 1986) notes the polycha- ete diet of four species on Guam, and refers (J. D. Taylor, 1984) three species to the poly- chaete feeding guild in a partial food web ona fringing reef on Guam. The distribution of species among the is- lands is patchy (Table 2). Only 10 species (6%) are recorded from all three island groups. Enewetak and Hawaii share 19% of the 114 species occurring in both island groups, and French Polynesia and Hawaii share 15% of 123 species. From west to east across the Pacific, the numbers of turrid species decrease from 180 species recorded along the Queensland coast of Australia (Hedley, 1922) to 76 spe- cies in French Polynesia, and from 100 spe- cies in the Philippines and Okinawa (Kuroda, 1960) to about 70 species respectively at Enewetak (Kay & Johnson, 1987) and in the Hawaiian Islands (Kay, 1979) (Figure 3). The decrease in number of turrid species is not the same in all subfamilies. The Turrinae gradually increase in percentage composition across the Pacific from 5% on the Queens- land coast to 18% in Hawaii, but are appar- ently reduced in importance in French Poly- nesia, where only two species are recorded (Richard, 1982; Salvat & Rives, 1979). The Mangeliinae, representing 57% of the Queens- land turrid list decrease to 21% of the Hawai- ian list and increase to 39% of the list in French Polynesia (Fig. 2). Biogeographic Components Three biogeographical components are identified: 39% of the Pacific island turrids also occur in the western Pacific but are not reported further west in either the Indo-Ma- layan archipelago or the Indian Ocean; 31% are recorded only from the Pacific Plate; and 29% are widespread within the Indo-Pacific, many of them found as far west as the coast of Natal. Two species, Microdaphne trichodes Dall, 1910 (McLean, 1971), and Kermia mac- ulosa (Pease, 1860) (Shasky, 1983), also oc- cur on the west coast of the Americas; both appear to be Indo-Pacific species that have crossed the East Pacific Barrier. The relative importance of the subfamilies differ among the three regional components of the fauna: in the Indo-Pacific faunal com- ponent, 47% of the turrids are daphnellines; and in the western Pacific and Pacific Plate components, 45% and 35% of the turrids re- spectively are mangelines (Fig. 4). There is a conspicuous component of Pacific Plate en- demism in all the subfamilies, but it is espe- cially noticeable in the Turrinae (56%), all of which are endemic to the Hawaiian Islands. TURRID FAUNAS OF PACIFIC ISLANDS 83 TABLE 2. Distribution records for 25 turrid species recorded from central Pacific Islands. Single island occurrences are not included. Xs represent occurrence. ENEWETAK, SPECIES MARSHALL IS. Mitromorpha metula (Hinds, 1843) XXXXXXXXX Carinapex minutissima (Garrett, 1873) XXXXXXXXX Iredalea exilis (Pease, 1868) XXXXXXXXX Daphnella ornata (Hinds, 1844) XXXXXXXXX Lienardia crassicostata (Pease, 1860) XXXXXXXXX Daphnella flammea (Hinds, 1843) XXXXXXXXX Kermia clandestina (Deshayes, 1863) XXXXXXXXX Psudodaphnella tincta (Reeve, 1846) XXXXXXXXX Clavus pica (Reeve, 1843) XXXXXXXXX Xenuroturris cingulifera (Lamarck, 1822) XXXXXXXXX Lophiotoma acuta (Perry, 1811) XXXXXXXXX Xenuroturris kingae (Powell, 1964) XXXXXXXXX Turridrupa albofasciata (Smith, 1877) XXXXXXXXX Tritonoturris amabilis (Hinds, 1843) XXXXXXXXX Daphnella olyra (Reeve, 1845) XXXXXXXXX Mitromorpha alphonisana (Hervier, 1899) Kermia pumila (Mighels, 1845) Clavus exilis (Pease, 1868) Lienardia lutea (Pease, 1860) Lienardia mighelsi (Iredale, 1917) Guam, in the southern Marianas Islands, and Okinawa, both of which are on the Phil- ippine Plate, have turrid faunas that are sim- ilar in species composition and habit to those of the central Pacific islands (Fig. 2). As with the central Pacific island turrids, there is a strong Daphnellinae and Mangeliinae compo- nent in these faunas. Fossil Record There is no clear direction to the fossil record of Pacific island turrids, unless it is that about 50% of the genera represented in the HAWAIIAN FRENCH ISLANDS POLYNESIA XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX XXXXXXXXX islands of the central Pacific apparently lack a fossil record. There are Miocene and Plio- cene records for Mitromorpha (Borsoniinae) and Daphnella and Philbertia (Daphnellinae) in Okinawa and Europe respectively, for Inquisitor and Clavus (Drillinae) in the Plio- cene of Java and Miocene of Borneo respec- tively, for Anacithara, Etrema, Eucithara, and Lienardia (Mangeliinae), and Miocene and Pliocene records for Gemmula, Lophiotoma, Turris (Turrinae) and Turridrupa (Claviinae) (Powell, 1966; Robba, 1987; Shuto, 1984). Among the genera and subgenera for which a fossil record is apparently lacking are: Eucy- 84 KAY QLD 180 | | O Above Equator ae aoe @ Below Equator 160 0 140 120 Number of Species 100 80 60 FIG. 3. Numbers of turrid species from west to east across the Pacific. Locality abbreviations as in Figure 2 50 É Turr HH Daph => UA crass E3 Borson 40 Кони e 35 ЕЕ Mang ‘sro 2 Е 25 =, 20 = Ф 15 10 ü 7 0 Vs FIG. 4. Subfamily composition of Indo-Pacific species, Western Pacific species, and Pacific Plate species. IP, Indo-Pacific, WP, Western Pacific, PAC, Pacific Plate. Subfamily abbreviations as in Figure 2. clotoma, Kermia, Microdaphne, Pseudodaph- The evolution of the Indo-Pacific molluscan nella, Tritonoturris, Iredalea, Macteola, and fauna can be traced to the ancient Tethys Paramontana. seaway which, from Triassic to Miocene time, TURRID FAUNAS OF PACIFIC ISLANDS 85 connected the Mediterranean and Indo- Pacific across what is now the Middle East and Pakistan (Kay, in press). The seaway was closed in Early Miocene (Adams, 1981), and the faunas of the Mediterranean and the Indo-Pacific evolved separately. Among the earliest turrids of Pakistan-India are Drilliinae in the Palaeocene Cardita beaumonti beds of the Upper Ranikot of Pakistan. In Indonesia, the earliest recognizable molluscan faunas are middle Miocene (Shuto, 1976), and there are representatives of the Drilliinae, Turrinae, Borsoniinae in that area. In the Pacific, sev- eral Miocene turrids (Daphnella, Clavus, In- quisitor, Etrema, Anacithara, Eucithara, Lie- nardia, Gemmula, Lophiotoma, and Turris) are recorded from Fiji and Okinawa. Eu- clathurella, Gemmula, and Lophiotoma are all recorded from the Pliocene of Fiji. The fur- thest east that fossil turrids are Known is in the Marshall Islands, where Ladd (1982) de- scribed Eucithara marshellensis from the Mi- ocene of Bikini and Enewetak. DISCUSSION Pacific island turrid faunas are character- ized by a suite of characters consonant with insular coral reef habitats separated one from another by great distances. The relatively high proportions of mangelines and daphnel- lines result in faunas with small, sturdy shells and with protoconchs indicative of long larval life. Indeed, Kilburn (1988) has suggested that the shell form of short, sturdy shells with reinforced labial lips may have evolved as an adaptation to a reef or under-rock existence, as opposed to shells with a produced sipho- nal canal and non-reinforced labial extremity (the ‘turrid facies’) of the predominantly sand- dwelling Turrinae and Cochlespirinae. The Pacific island turrid assemblages, with their prominent daphnelline and mangeline com- ponents, with colorful shells and long larval lives, and comprising less than 15% of the predatory gastropods, contrast with a Carib- bean island assemblage described by Maes (1983), which is rich in drillines with dark shells, most of which apparently have direct development. The pattern of turrid distribution among Pa- cific islands follows a generally recognized pattern of a marine fauna of the Indo-Pacific (Kay, 1980): decreasing diversity west to east in the Pacific Ocean (Kay, 1980; Springer, 1982); patchy distribution (Kay, 1980; 1984); disproportionate representation in certain groups; and a recognizable component of species that are endemic to the Pacific Plate (Kay, 1980; Springer, 1982). On the Pacific Plate, the pattern of endemism follows that of other mollusks, with a group of species that is widespread, and with others of the turrids en- demic to two foci, the Hawaiian Islands where 60% of the turrids are reported as endemic, and French Polynesia with 9%. No single is- land endemics as distinguished by Springer (1972) have been identified. Although in broad outline the Pacific island turrid faunas fit the pattern of history and dis- tribution of other marine mollusks, three as- pects of the current review of Pacific island turrid faunas are vulnerable to the criticism of insufficient and biased collection: (1) the ap- parent concentration of species in the west- ern Pacific; (2) the records of patchy distribu- tion; and (3) the apparent lack of fossil record. The prominent western Pacific element in the distributional pattern may be an artifact of collecting simply because of the enormous numbers of species described from the Phil- ippines, Loyalty Islands, New Caledonia, and Queensland by Reeve, Hervier, Melvill and Standen, Hedley, and others. As the taxon- omy of the several hundred species is worked out, many of the species may be shown to be invalid, and new collecting records will possi- bly extend the presently known ranges. The apparent patchy distribution of turrid species among the islands may also be misleading and with further collection such anomalies as the virtual absence of Turrinae in Tahiti may be rectified. The fossil history of Pacific island turrids is similarly subject to criticism in that so few fossil are actually known from Pacific is- lands. ACKNOWLEDGMENTS | am particularly grateful to the many cura- tors and curatorial assistants who have so graciously allowed me to work with the turrid collections under their care: P. Bouchet (Paris), G. Oliver (Cardiff), W.F. Ponder (Syd- ney), the late Joseph Rosewater (Washing- ton, D. C.), G. Davis (Philadelphia), and K. Boss (Harvard). And again | must thank the staff in the Mollusca Section, BM(NH), for their patience and hospitality over the years as | have worked in the superb collections in that institution. 86 LITERATURE CITED ADAMS, C. G., 1981, Speciation, phylogenesis, tectonism, climate and eustacy: factors in the ev- olution of Cenozoic larger foraminiferal bioprov- inces. In L. R. M. COCKS, ed., The evolving Earth. British Museum (Natural History), London, and Cambridge University Press. pp. 255-289. BOUCHET, P. H., 1990, Turrid genera and mode of development: the use and abuse of protoconch morphology. Malacologia, 32: 69-77. BOUCHET, P. H. & A. WAREN, 1980, Revision of the north-east Atlantic bathyal and abyssal Tur- ridae (Mollusca, Gastropoda). Journal of Mollus- can Studies, Supplement 8:1-119. DAUTZENBERG, P. & J. L. BOUGE, 1933, Les mollusques testacés marins des établissements Français de l'Océanie. Journal de Conchyliolo- gie, 77:41-108; 145-326; 351-469. HEDLEY, C., 1922, A revision of the Australian Tur- ridae. Records of the Australian Museum, 13: 213-259. HERVIER, R. P. J., 1896, Descriptions d'espèces nouvelles de mollusques, provenant de l'Archipel de la Nouvelle-Calédonie. Journal de Conchyli- ologie, 44:51—96. HERVIER, R. P. J., 1897, Descriptions d'espèces nouvelles de mollusques, provenant de l'Archipel de la Nouvelle-Calédonie. Journal de Conchyli- ologie, 45:89-121; 165-191. HERVIER, R. P. J., 1898, Descriptions d’especes nouvelles de mollusques, provenant de l'Archipel de la Nouvelle-Calédonie. Journal de Conchyli- ologie, 45:225—248. IREDALE, Т. & D. Е. MCMICHAEL, 1962, A refer- ence list of the marine Mollusca of New South Wales. Memoirs of the Australian Museum, 11: 1-109. KAY, Е. A., 1979, Hawaiian marine shells. В. P. Bishop Museum Special Publication, 64(4): 1-653. KAY, E. A., 1980, Little worlds of the Pacific. An essay on Pacific Basin biogeography. Harold L. Lyon Arboretum Lecture No. 9. University of Ha- waii. 40 pp. KAY, Е. A., 1984, Patterns of speciation in the Indo- west Pacific. In P. H. RAVEN, F. J. RADOVSKY & S. H. SOHMER, eds., Biogeography of the tropical Pacific. Association of Systematics Col- lections and the Bernice P . Bishop Museum. pp. 15-31. KAY, E. A., In Press. Biogeography and Cenozoic history of the Cypraeidae of the Pacific. Bulletin of Marine Science. KAY, E. A. & S. JOHNSON, 1987, Mollusca of Enewetak Atoll. In D. M. DEVANEY, E. S. REESE, В. L. BURCH, & P. HELFRICH, The Ман ural History of Enewetak Atoll, Vol. 1 U. S. Dept. of Energy. pp. 105-148. KEEN, A. M., 1971, Sea shells of tropical west America. Stanford University Press. 1064 pp. KILBURN, R. N., 1983, Turridae (Mollusca: Gas- tropoda) of southern Africa and Mozambique. KAY Part 1. Subfamily Turrinae. Annals of the Natal Museum, 25:549-585. KILBURN, В. N., 1985, Turridae (Mollusca: Gas- tropoda) of southern Africa and Mozambique. Part 2. Subfamily Clavatulinae. Annals of the Na- tal Museum, 26:417—470. KILBURN, В. N., 1986, Turridae (Mollusca: Gas- tropoda) of southern Africa and Mozambique. Part 3. Subfamily Borsoniinae. Annals of the Na- tal Museum, 27:633—720. KILBURN, R. N., 1988, Turridae (Mollusca: Gas- tropoda) of southern Africa and Mozambique. Part 4. Subfamilies Drilliinae, Crassispirinae and Strictispirinae. Annals of the Natal Museum, 29: 167-320. KURODA, T., 1960, A catalogue of molluscan fauna of the Okinawa islands. Privately printed, Japan. LADD, H. S., 1982, Cenozoic fossil mollusks from western Pacific islands; gastropods (Eulimidae and Volutidae through Terebridae). U. S. Geolog- ical Survey Professional Paper, 1171:1-100. MAES, V. O., 1983, Observations on the systemat- ics and biology of a turrid gastropod assemblage in the British Virgin Islands. Bulletin of Marine Science, 33:305-335. MCLEAN, J. H., 1971, A revised classification of the family Turridae, with the proposal of new sub- families, genera and subgenera from the eastern Pacific. Veliger, 14:114—130. MELVILL, J. С. & В. STANDEN, 1895-1897, Notes on a collection of shells from Lifu and Uvea, Loy- alty Islands, formed by Rev. James and Mrs. Hadfield, with list of species. Journal of Conchol- ogy, 8:84—132; 273-315. POWELL, A. W. B., 1942, The New Zealand Re- cent and fossil Mollusca of the family Turridae. Bulletin of the Auckland Institute and Museum 2:1-192. POWELL, A. W. B., 1966. The molluscan families Speightiidae and Turridae. Bulletin of the Auck- land Institute and Museum, 5:1-184. POWELL, А. W. B., 1964-1967, The family Tur- ridae in the Indo-Pacific. Part 1. The subfamily Turrinae. Indo-Pacific Mollusca, 1:227-345; 409—443. POWELL, А. W. В., 1979. New Zealand Mollusca. Collins. 500 pp. REHDER, H. А. & H. $. LADD, 1973, Deep and shallow-water mollusks from the Central Pacific. Science Reports Tohoku University, 2nd Ser. 6: 37—49. RICHARD, G., 1982, Mollusques lagunaires et réc- ifaux de Polynésie francaise. Thesis for the Doc- teure of Science Naturelle, Universite Pierre et Marie Curie, Paris. ROBBA, E. 1987. The final occlusion of Tethys: its bearing on Mediterranean benthic Mollusca. In MCKENZIE, K.G., ed., Proceedings of the Inter- national Symposium on Shallow Tethys, A.A. Balkema, Rotterdam & Boston, pp. 405—426. SALVAT, B. & C. RIVES, 1975, Coquillages de TURRID FAUNAS OF PACIFIC ISLANDS 87 Polynesie. Editions du Pacifique Papeete: 391 pp. SHASKY, О. R., 1983, New records of Indo-Pacific Mollusca from Cocos Island, Costa Rica. Nau- tilus, 97:144—145. SHIMEK, R. L., 1986, The biology of the northeast- ern Pacific Turridae. V. Demersal development, synchronous settlement and other aspects of the larval biology of Oenopota levidensis. Interna- tional Journal of Invertebrate Reproduction and Development, 10:313-333. SHUTO, T., 1976, Correlation of Neogene forma- tions of Southeast and South Asia by means of molluscan faunas. Proceedings of the First Inter- national Congress on Pacific Neogene Stratigra- phy Tokyo. Science Council of Japan Geological Society of Japan. pp. 133-144. SHUTO, T., 1984, A revision of the Burmese Ter- tiary turrids. Memoirs of the Faculty of Sciences, Kyushu University Series D (Geology), 25:115- 1157 SPRINGER, V. G., 1982, Pacific Plate biogeogra- phy with special reference to shorefishes. Smith- sonian Contributions to Zoology, 367:1-182. TAYLOR, J. B., 1975, Planktonic prosobranch veligers of Kaneohe Bay. Ph.D. Dissertation. Uni- versity of Hawaii, Honolulu. TAYLOR, J. D., 1977, Food and habitats of preda- tory gastropods on coral reefs. Reports Under- water Association 2:17-34. TAYLOR, J. D., 1984, A partial food web involving predatory gastropods on a Pacific fringing reef. Journal of Experimental Marine Biology and Ecology 74:273-290. TAYLOR, J. D., 1986, Diets of sand-living predatory gastropods at Piti Bay, Guam. Asian Marine Bi- ology 3:47-58. Revised Ms. accepted 21 June 1990 MALACOLOGIA, 1990, 32(1): 89-106 ULTRASTRUCTURAL CHANGES IN THE DIGESTIVE SYSTEM OF DEROCERAS RETICULATUM (MOLLUSCA; GASTROPODA) INDUCED BY LETHAL AND SUBLETHAL CONCENTRATIONS OF THE CARBAMATE MOLLUSCICIDE CLOETHOCARB Rita Triebskorn' & C. Künast? ABSTRACT Specimens of the grey garden slug, Deroceras reticulatum, were fed lethal (2%, 1%, 0.5%, 0.1%) or sublethal concentrations (0.01%, 0.001%) of the carbamate molluscicide Cloethocarb (BASF) as either pellets or wheat-germ agar. To investigate the influence of the chemical on the ultrastructure of the cells in the digestive tract, samples of oesophagus, crop, stomach, intestine and hepatopancreas were taken at six time intervals. Reactions of lethal intoxication (e.g. elongation of cells, damage to nuclei and mitochondria, destruction of membranes) were dis- tinguished from those appearing most intensely after sublethal intoxication (e.g. reactions of the endoplasmic reticulum, Golgi apparatus, mucous cells) and finally from features that appear after both lethal and sublethal poisoning (e.g. reduction of storage products). It could be shown that higher concentrations of the pesticide do not necessarily produce stronger effects at the ultrastructural level. Because it is effective in elucidating cellular injury following lethal and sublethal intoxication, electron microscopy is a sensitive method for diag- nosing the animals’ response to stress. Key words: molluscicide, carbamate, ultrastructure, digestive tract, Gastropoda, Deroceras reticulatum. INTRODUCTION The increasing importance of slugs as field and garden pests (Martin & Kelly, 1986), de- mands continued efforts to identify and pro- duce more effective and selective mollusci- cides. For commercial reasons, however, most molluscicides have been detected only incidental to screening programmes for the development of insecticides (Henderson & Parker, 1986). It is highly probable, therefore, that most potential molluscicides will also be insecticides having considerable side-effects on useful animals, as soil arthropods and an- nelids. Little is known about the mollusc-specific effects of even the most widely used commer- cial molluscicides, metaldehyde and methio- carb, owing to the fact that most pesticide re- search is restricted to LD, tests, which provide information about lethal or non-lethal effects of the substances tested. Such acute toxicity tests have demonstrated the advan- tages of carbamate or metaldehyde applica- tion under specific conditions (Kemp & New- ell, 1985; Glen & Orsman, 1986; Prystupa et al., 1987), and have also revealed optimal molluscicidal concentrations for different ac- tive substances (Wright & Williams, 1980). Such tests, however, do not yield any further information about either the targets for the molluscicides or the mollusc-specific mecha- nisms induced in the slugs’ bodies. Because this knowledge is essential for the develop- ment of new, more selective substances, much basic research is required. Basic biochemical and physiological stud- ies, for instance, have shown the inhibitory effect of methiocarb on cholinesterases (Pessah & Sokolove, 1983; Young & Wilkins, 1989) and the influence of metaldehyde on feeding motoneurons in the buccal ganglia (Mills et al., 1989). In the present study, the influence of lethal (=0.1%) and sublethal (<0.01%) oral doses (OD) of the carbamate Cloethocarb on the cells of the digestive system of Deroceras re- ticulatum was investigated by electron mi- croscopy. Sublethal concentrations are de- fined as those not leading to any mortality during the test (up to 30 h). Diagnosis at the cellular level was chosen for its high sensitivity (Braunbeck, 1989), and for its providing information about reactions to 'Zoologisches Institut I, Universitat Heidelberg, Im Neuenheimer Feld 230, D-6900 Heidelberg, Germany “BASF Aktiengesellschaft, Landwirtschaftliche Versuchsstation, D-6703 Limburgerhof, Germany 90 TRIEBSKORN & KUNAST TABLE 1. Amount of ingested food containing various concentrations of Cloethocarb and calculated values for absolute quantity of active substance ingested / g wet weight. Food Active substance ingested ingested active substance (mg/g wet weight) (g/g wet weight) 2% Cloethocarb (pellet) 70.0=50.5 1400 2% Cloethocarb (agar) 69.0+25.2 1380 0.1% Cloethocarb 83.9+44.0 83.9 0.01% Cloethocarb 105.2+47.5 10.5 0.001% Cloethocarb 105.3=29:9 1.05 Control both lethal and sublethal intoxication. Thus, it should be possible to distinguish primary car- bamate-specific cell reactions from symptoms resulting from cell death, and to differentiate irreversible damage from such cellular injury that might be compensated by the animal's detoxification mechanisms. MATERIALS AND METHODS The carbamate molluscicide Cloethocarb (BASF) was given to laboratory-reared Dero- ceras reticulatum by a single feeding of either pellets produced by BASF containing 2% of the active substance, phenol-2-(2-chloro-1- methoxyethoxy)-methylcarbamate, or wheat- germ agar containing 2%, 1%, 0.5%, 0.1%, 0.01%, or 0.001% of this toxin. The amount of food ingested was determined by weighing the treated food, which was dried before and after feeding. Finally, the quantity of active sub- stance taken up with the food was calculated (Table 1). Doses in the 0.02% and 0.001% formulation proved to be sublethal. Behavioral and macroscopic changes of the animals were recorded during the first hour after the beginning of feeding. For deter- mination of cellular reactions, three animals feeding at each of the molluscicide concen- trations were dissected after 30 min, 1h, 3h, 5 h, 24 h and 30 h. For primary fixation of excised tissue, a 2% glutaraldehyde solution in cacodylate buffer (0.01 M, pH 7.4) was in- jected into the body cavity. The oesophagus, crop, stomach, intestine and hepatopancreas were isolated under fixative and fixed for 2 h at 4°C. The tissues were then rinsed in ca- codylate buffer and postfixed in 1% osmium ferrocyanide (Karnovsky, 1971) for 2 h at 4°C. After rinsing in cacodylate and maleate buffer (0.05 M, pH 5.2), the specimens were stained 102.8+38.3 — en bloc overnight in 1% uranyl acetate dis- solved in maleate buffer (0.05 M, pH 5.2) at 4°C. The samples were rinsed in maleate buffer, dehydrated and embedded in Spurr's medium (Spurr, 1969). Semithin and ultrathin sections were cut on a Reichert ultramicro- tome. Semithin sections were stained with methylene blue-azur (Richardson et al., 1960) and used for light microscope overviews. Ul- trathin sections were counterstained with lead citrate for 30 sec. The tissues were examined in a Zeiss EM 9. The following cell types of the digestive system were investigated: Oesophagus: storage cells, secretory cells of an eccrine type, secretory cells of a holo- crine type (mucous cells); Crop: storage cells; Stomach: storage cells, secretory cells of a holocrine type (mucous cells); Intestine: storage cells, secretory cells of an eccrine type, secretory cells of a holocrine type (mucous cells); Hepatopancreas: digestive cells, crypt cells, excretory cells. The muscle and nerve layers underlying the epithelia were also studied. RESULTS Macroscopic Observations Table 2 shows the mortality after Cloetho- carb application. More animals were killed af- ter the application of low lethal concentrations (0.1-1%) than after that of 2%. After ingestion of the 2% agar, however, animals died sooner than after that of all other concentrations. Fur- thermore, the mortality after 2% agar was higher than that after 2% pellets. The macroscopically visible reactions of animals to intoxication with Cloethocarb cor- EFFECT OF CARBAMATE TOXIN ON SNAIL GUT 91 TABLE 2. Mortality (absolute number of dead animals) after application of Cloethocarb. For each concentration, 20 animals were tested. Concentration =F — =; Ww =F Cloethocarb 0. Control 0.001% 0.01% 0.1% 0.5% 1% 2% agar 2% pellet SISISTSISTSISZSF EN 600 © © ©' © DISCO 010010 respond to typical symptoms of carbamate in- toxication (Godan, 1979): ten minutes after taking up pellets or wheat-germ agar contain- ing 2%, 1%, 0.5% or 0.1% of the poison, the animals show muscle convulsions that be- come more intense in the following 30 min- utes. During this period, they lose large amounts of a lucent mucus. Whereas during the first 30 minutes after intoxication, the an- imals still move actively, after 1 h, the animals are alternately active and immobile. The an- terior part of the body begins to swell while the posterior part flattens. After a period longer than 16 h, most of the animals lie mo- tionless on their sides and only occasionally move. Reactions to 0.1%, 0.5% and 1% OD are as intense as those to 2%, whereas be- havioral reactions to both sublethal concen- trations are absent. Electron Microscope Investigations Table 3 summarizes the most important re- actions of investigated components in cells of the digestive system of Deroceras reticulatum after intoxication with different concentrations of Cloethocarb. Thirty minutes after the onset of poisoning, reactions were confined to single cells and especially to the anterior part of the digestive tract (oesophagus and crop). During the fol- lowing hours, reactions spread over the epi- thelia, then appeared in the cells of the pos- terior part of the digestive system (stomach, intestine and hepatopancreas), with lapse of time corresponding to the rate of transport of toxic feedstuff by the alimentary canal or by the hemolymph (Triebskorn et al., 1990). In general, cells of the hepatopancreas are more strongly damaged than are those of the digestive tract. In the cells of the crop, the reactions are less severe than those in epi- a = Time 1 =; — = № =): (03) o DR o-000000 SIN) Ce) e Neo eee | © |=NMNWARWOOO]| + ar © thelia characterized by high percentages of mucous cells. In most cases, there are no differences in the cellular responses to 2%, 1%, 0.5% or 0.1% OD. Such differences as exist appear less intense after 2% than after 0.1% (Table 3: indented arrows). Cellular reactions of slugs exposed to pellets containing 2% of the carbamate substance are similar to those of animals fed the 2% treated agar. Cellular Outline In control animals, most of the epithelial cells of the digestive tract are columnar (Figs. 1, 2). Their apical surfaces are characterized by microvilli (storage and secretory cells of oesophagus and crop, digestive cells of the midgut gland; Figs. 6, 8) or by cilia and mi- crovilli (Storage and secretory cells of oesoph- agus, stomach and intestine; Fig. 9). Infold- ings of the basal surfaces of these cells are small or absent, and the basal membrane is very thin (Fig. 12). The mucus-producing cells of oesophagus, stomach and intestine are pyriform (Fig. 2). They bear small microvilli. Immature mucous cells do not reach the lumen. In the hepatopancreas, two other cell types can be distinguished in addition to the diges- tive cells: conical crypt cells (Fig. 3), with a microvillous border and a prominent basal labyrinth, and the bellied excretory cells, char- acterized by large excretory vacuoles and long microvilli. The molluscicide produces cytopathologi- cal changes in the general outline of cells and in their apical and basal surfaces. Most of the cells in the digestive system change their typical cellular outline after 5 п, and more intensely 24 h and 30 h after the application of food containing between 0.1% and 2% poison. The columnar cells of the di- 92 TRIEBSKORN & KÜNAST TABLE 3. The most striking reactions of cellular components after lethal and sublethal intoxication with Cloethocarb. CLOETHOCARB CONCENTRATIONS 2% 1% 0.5% 0.1% 0.001% | A A O AAA _ |] GEEE »>— Stretching of the cells — 4 OUTLINE »————— Irregular cell shape — € — p»—— Irregular shape of microvilli —— 8 CELL APEX »>——— Reduction of microvilli ——————————4 > Sunace) Вер ——— 2- D Surface coat Я | IA EA AS AA |e »————— Basal cell extensions — м »— Dilation of basal labyrinth — 4 >—_— Gaps —— 4 »————— Thickening of basal membrane ————————- Crystalline inclusions NUCLEI > Reduction of heterochromatin ———————4 = > Karyolysis — — 8 A АСЕ МПО- ды _ Swelling — 4 CHONDRIA > _—— Reduction of cristae 2 « D>— Rupture of membranes — чм Be EEE ERS »——- Degranulation, dilation of ER — « ENDOPLASMIC p»— Proliferation, vesiculation of ER ge Verba OS RETICULUM p— Tubular system —________L_L_______________~« Destruction, rupture of membranes Pe E »>——— Irregular arrangement of cisternae —-___________—_q GOLGI »———— Compression of the cis-face cisternae — 4“ APPARATUS Dilation of trans-face cisternae Destruction of membranes E A VACUOLAR D>— Increased fusion rate ———__________________—__qq D Increased membrane lability ————————=4 SYSTEM »——- Increased production of large mucous vacuoles — € DE EI RER STORAGE p»——— Decrease of storage products —— « PRODUCTS »————- Increase of electron-dense vesicles — € PRE NEN Eee p———— Muscle envelopes without filaments — MUSCLE = Fragmentation я — TISSUE »————— Irregular orientation of filaments — € NERVE EFFECT OF CARBAMATE TOXIN ON SNAIL GUT 93 FIG. 1. Crop (control). Storage (sc) and mucous cells (muc) in epithelium of crop. Storage cells contain large amounts of lipid (li) and bear microvilli (mv). LM. FIG. 2. Stomach (control). Storage (sc) and mucous cells (muc) in epithelium of stomach. c: cilia. LM. FIG. 3. Hepatopancreas (control). Light-microscopial overview of crypt cell characterized by round nucleus (n) with prominent nucleolus (nu) and numerous vesicles (v). FIG. 4. Crop (2% Cloethocarb, 5h). Epithelial cells elongated (arrows), nuclei condensed. nt = nerve tissue. FIG. 5. Stomach (2% Cloethocarb, 5h). Gap (arrow) between muscle tissue (mt) and epithelial cells. gestive tract become greatly elongated, espe- cially after 0.1% OD, and often gaps open between the epithelial cells and the underly- ing muscle and nerve tissue (Figs. 4, 5). The cells of the hepatopancreas are already irreg- ularly shaped after 1 h (Fig. 7). Sublethal con- centrations (0.01%, 0.001%) do not affect cell shape. The most striking reactions of the cell api- ces are reduction of microvilli, formation of surface blebs and production of a hyaline sur- face coat. Thirty minutes after the application of a lethal concentration, reduced microvilli and apical cytoplasmic protrusions (blebs) al- ready can be observed in the columnar cells of the oesophagus and crop. Both reactions occur in all epithelia of the digestive system after 5, 24 and 30 h (Fig. 10), most severely in the cells of the intestine 24 h after ingestion of 0.1% toxin and in the hepatopancreas as soon as 1 h after ingestion of any lethal con- centration. Food containing 0.01% poison leads to formation of small blebs and irregu- larly shaped microvilli in isolated cells. Inges- tion of food containing 0.001% poison pro- duced no evident reaction. A further phenomenon appearing after both sublethal and lethal intoxication is a surface coat consisting of a hyaline material overlying the microvilli or the cilia, or both (Fig. 11). This TRIEBSKORN & KUNAST 94 EFFECT OF CARBAMATE TOXIN ON SNAIL GUT 95 surface coat is less electron-dense in the di- gestive tract than in the hepatopancreas. It is already present in the anterior parts of the tract 1 h after administration of the poison and is very prominent in all regions of the diges- tive system after 5 h. Application of 0.001% of the molluscicidal agent does not produce a detectable surface coat. The most striking changes in the basal sur- face of the cell are development of basal cell extensions, thickening of the basement mem- brane, and development of gaps between the epithelium and the basement membrane. After 30 minutes, small basal infoldings al- ready have formed in the oesophagus, partic- ularly after 0.1% OD. After 5 and 24 h, how- ever, bases of the cells of the digestive tract, but not of the hepatopancreas, show consid- erable extensions (Figs. 13, 14). These ex- tensions are most prominent in the region of the stomach and intestine. In the hepatopancreas, the basal labyrinth of the crypt cells is extended. Thirty hours after the application of 0.01% OD the basal infold- ings are comparable to those in the oesoph- agus 30 minutes after lethal intoxication. From 24 h to 30 h after ingestion of lethal concentrations, gaps form between the basal parts of the epithelial cells and the underlying connective, muscle and nerve tissues (Fig. 115): A further reaction detectable after the in- gestion of sublethal concentrations is the thickening and increased electron-density of the basement membrane (Figs. 14, 16), which appears as early as 1 h after the inges- tion of food containing =0.01% Cloethocarb. Nuclei In the storage and secretory cells of the digestive tract and in the digestive cells of the hepatopancreas, the nuclei are ovoid (Fig. 17). In the crypt cells of the hepatopancreas and in the mucuous cells, however, they are roundish (Figs. 2, 3). The nuclei of the crypt cells are rich in heterochromatin and have a prominent, round nucleolus (Fig. 3). The most typical cytopathological changes in the nuclei are lightening of the karyoplasm, reduction of the heterochromatin, dilation of the nuclear envelope and formation of crys- talline inclusions. Thirty minutes after the onset of intoxica- tion, the nuclear envelope is locally dilated and the karyoplasm becomes more electron- lucent in individual cells. After 5 h these phe- nomena occur in many cells (Fig. 18). The nuclei show the effects of lytic processes. In the crypt cells the nucleoli assume irregular shapes. The most severe nuclear damage occurs in the posterior part of the digestive tract and in the cells of the hepatopancreas. Twenty-four hours after ingestion of food containing 0.1% or 0.01% of the molluscicide, large crystalline inclusions form in the nuclei, especially in the region of the stomach and the intestine (Fig. FIG. 6. Hepatopancreas (control). Digestive cells, characterized by microvillous border (mv) and system of digestive vacuoles (dv). FIG. 7. Hepatopancreas (0.1% Cloethocarb, 1h). Irregularly shaped digestive cells. Digestive vacuoles (dv) contain electron-dense material. mv: microvilli. FIG. 8. Crop (control). Apex of a storage cell bearing microvilli (mv). Beneath microvillous border mitochon- dria (mi) visible. FIG. 9. Stomach (control). Apices of two storage cells bearing microvilli (mv) and cilia (c). FIG. 10. Oesophagus (2% Cloethocarb, 5h). Apex of storage cell with reduced microvilli (mv) and surface blebs (sb). Mitochondria (mi) severely damaged. FIG. 11. Oesophagus (2% Cloethocarb, 1h). Storage cells with coat (co) overlying microvilli (mv). FIG. 12. Crop (control). Basal part of storage cell with thin basal membrane (bm). FIG. 13. Stomach (2% Cloethocarb, 5h). Basal parts of mucous (muc) and storage cells (sc) with basal cell extensions (arrows). FIG. 14. Crop (2% Cloethocarb, 24h). Storage cell with basal cell extensions (long arrows), electron-dense cytoplasm (cyt) and thickened basal membrane (bm, short arrows). FIG. 15. Crop (2% Cloethocarb, 30h). Gap between epithelium and basal membrane (bm, short arrows). FIG. 16. Intestine (0.1% Cloethocarb, 5h). Thickening of basal membrane (bm). FIG. 17. Oesophagus (control). Nucleus (n) of storage cell. FIG. 18. Stomach (2% Cloethocarb, 5h). Nuclei (n) with envelope dilated (arrows), karyoplasm lightened and heterochromatin reduced. FIG. 19. Stomach (0.1% Cloethocarb, 5h). Nucleus (n) with crystalline inclusion (ci). FIG. 20. Stomach (0.1% Cloethocarb, 5h). Crystalline inclusion (ci) filling greater part of karyoplasm. 96 TRIEBSKORN & KUNAST 19). In some cases, these crystals occupy an appreciable part of the nucleus (Fig. 20). A molluscicide concentration of 0.001% failed to induce any reaction in the nuclei. Mitochondria The storage cells have a layer of mitochon- dria beneath the microvillous border (Figs. 8, 9), whereas in the other cells, these or- ganelles are irregularly dispersed throughout the cytoplasm. Reduction of cristae and swelling are the most important reactions of mitochondria to Cloethocarb intoxication. One hour after le- thal intoxication, the regular arrangement of mitochondria beneath the microvillous border begins to be disturbed. The organelles swell, the cristae become reduced (Figs. 21, 22), and after 5 h, the outer membranes rupture (Fig. 23). Damage to mitochondria is most se- vere in the stomach and intestine. After sublethal intoxication, changes in the mitochondria could not be observed. Endomembrane System Large amounts of granular endoplasmic re- ticulum (ER) occur in the secretory cells of the oesophagus and intestine, in the mucous cells of oesophagus, crop, stomach and in- testine (Fig. 24), and in the crypt cells of the hepatopancreas (Fig. 25). The cisternae are almost parallel, mostly within the basal or me- dio-basal parts of the cells. The granular endoplasmic reticulum of the mucous cell is of the wide-luminar type, the width of the cisternae ranging from 120 to 280 nm. In the lumen of the cisternae, there are typical tubular structures with an average di- ameter of 30 nm (Fig. 24). In the other cell types, only small amounts of granular endo- plasmic reticulum are present. Additionally, there are some cisternae of smooth endo- plasmic reticulum in the storage cells and ex- cretory cells. The most prominent cytopathological changes in the endoplasmic reticulum after Cloethocarb intoxication are dilations of the cisternae, degranulation of the granular ER, proliferation and vesiculation of ribosome-free ER, and formation of membrane whorls and tubular structures. Within 30 minutes after ingestion of lethal and sublethal concentrations, degranulation of the granular endoplasmic reticulum and di- lation of the cisternae occur (Fig. 26). After 1 h, the cisternae of both granular and degran- ulated/smooth endoplasmic reticulum are greatly dilated (Fig. 27). Furthermore, the amounts of degranulated/smooth endoplas- mic reticulum in the storage, secretory, crypt and excretory cells have increased. In the storage cells, the cisternae often touch (Fig. 28) or surround lipid droplets (Figs. 29, 30). After 5 h, vesicles of endoplasmic reticulum occur throughout the cytoplasm of storage, secretory and crypt cells. This reaction is also evident after 0.01% OD (Fig. 31), but is most intense after intoxication with the sublethal concentration of 0.001%. The proliferation be- comes stronger with time. In addition to the dilation of the cisternae, characteristic con- centric whorls of the endoplasmic reticulum and other membrane whorls form 5, 24 and 30 h after all lethal and both sublethal con- centrations (Figs. 29, 30). After ingestion of lethal concentrations, the membranes of the endoplasmic reticulum often rupture (Fig. 32). Another phenomenon appearing 5 h after both lethal and sublethal intoxication is a sys- tem of tubules arising from and connected with the degranulated/smooth endoplasmic reticulum (Figs. 33, 34). It occurs especially in the storage and excretory cells. After 0.001% OD, there are fewer tubules than after 0.01%, whereas their number after 0.01% is similar to that after lethal intoxication. Large Golgi fields characterize the mucous and crypt cells (Figs. 35, 36). In both kinds of cells, small vesicles originating from the gran- ular endoplasmic reticulum fuse with the cis- face cisternae. Most trans-face cisternae also fuse with small vesicles of unknown origin, become spherical, and finally as large vacu- oles become free from the Golgi fields. In the other cell types, the Golgi complex is less prominent. Disorganisation of the cisternae, compres- sion of the cis-face and dilation of the trans- face cisternae and destruction of membranes are the most common cytopathological re- sponses of the Golgi apparatus to Cloetho- carb. One hour after both lethal and sublethal concentrations of the toxin are ingested, the normally regular arrangement of the cisternae in large and small Golgi apparatus is dis- rupted. The cis-face cisternae become tightly stacked (Figs. 37, 40). In the mucous cells, very many mucous vacuoles originate from the trans-face cisternae, and vesicles arising from the endoplasmic reticulum become more numerous (Fig. 38). With sublethal intoxica- tion these reactions occur after 30 h. Five hours after lethal intoxication, how- EFFECT OF CARBAMATE TOXIN ON SNAIL GUT 97 ever, damage to large and small Golgi com- plexes becomes greater. The trans-face cis- ternae, especially those of the small Golgi apparatus in the storage and secretory cells, are grossly swollen (Fig. 39) and the mem- branes often rupture (Figs. 37, 41). Within the digestive cells of the hepatopan- creas are typical vacuolar and lysosomal sys- tems, the vacuoles of which fuse with each other and with lysosomes, vary in size, and are generally largest towards the basal re- gions of the cells (Fig. 42). The small endocy- totic vesicles, located in the most apical parts of the cells and the lysosomes, are more elec- tron-dense than the large vacuoles (Fig. 43). A second type of cell that is dominated by vacuoles is the mucous cell (Fig. 2). Its vac- uoles fuse on their way from the base to the apex and are thus largest towards the apical part of the cell. In immature mucous cells, only a few mu- cous vacuoles occur and seem not to fuse with one another. The most striking cytopathological reac- tions of the vacuolar system are the intensi- fied fusion of vacuoles and the increased la- bility of membranes. Within one hour after lethal intoxication, re- action of the digestive vacuoles and the ly- sosomes is already evident. Endocytotic ves- icles in the apical part of the cell are fewer, and the large vacuoles contain material of ap- preciable electron-density (Fig. 7). From 3 to 5 h, wide cisternae appear as a result of the intensified fusion of small vesicles and of small and large vacuoles (Figs. 44, 45). Whereas the membranes of the resulting large cisternae often rupture, those of the re- maining small vesicles remain intact. After 16 h, most of the vacuolar membranes are heavily damaged (Fig. 46) and the vacuolar system thus is disrupted. The molluscicide acts on the mucous cells to produce a greater number of cells entirely filled with mucous vacuoles. Furthermore, even in immature mucous cells, many large vacuoles fuse. This intensified production of mucous occurs after lethal oral dosage but is more intense after sublethal intoxication (Fig. 47). Storage Products In control animals, there are large deposits of lipid and glycogen in storage and crypt cells (Fig. 48), but few storage products occur in the secretory, digestive and excretory cells. In the storage cells, most lipid droplets are slightly electron-dense and only a few lipid- containing vesicles are totally electron-dense. Cloethocarb intoxication results in a reduc- tion of storage products and a concomitant increase in electron-dense vesicles. As soon as 1 h after ingestion of all lethal concentra- tions and of 0.01% Cloethocarb (Fig. 49), the glycogen content is slightly reduced in the storage cells of the oesophagus and crop, and lipid droplets fuse and appear less elec- tron-dense. After 3 h, lipid droplets have become fewer while electron-dense vesicles have become more numerous (Fig. 50). Peroxisomes are frequently associated with lipid droplets and ER cisternae surround them (Figs. 28-30). After 5, 16 and 24 h, the amount of storage products is obviously diminished. There is still some lipid present, but very little glycogen re- mains in the storage cells. The reduction of storage products is less intense after application of sublethal concen- trations than after that of any of the lethal con- centrations. Both the decrease in lipid and glycogen content and the increase in the number of electron-dense vesicles can be re- lated to the concentration of molluscicide in the food ingested. Muscle and Nerve Tissue In control animals, a conspicuous layer of muscle tissue, the filaments of which are lon- gitudinal and transverse, underlie the epithe- lia of the oesophagus, stomach and intestine (Fig. 51). The filamentous portions are sur- rounded by a plasma membrane and an en- velope of connective tissue. Underlying the epithelia of the crop and hepatopancreas is a very thin layer of muscle. Nerves, characterized by various neuro- secretory vesicles, lie close to the muscle tis- sue. The neurosecretory vesicles vary from electron-dense to electron-lucent and are sur- rounded by an electron-lucent halo. Connective tissue occurs between nerves, muscles and the epithelia of the digestive sys- tem. The most prominent cytopathological re- sponses of muscles and nerve tissues to the molluscicide are disorientation of muscle fila- ments, appearance of muscle envelopes de- void of muscle filaments and augmentation of neurosecretory vesicles. At 1, 3 and 5 h after lethal intoxication, the muscle filaments are irregularly oriented in the oesophagus, stomach and intestine (Fig. 52). After 24 h, the muscle tissue is frag- TRIEBSKORN & KUNAST { Е II to © | E IE: E о y EFFECT OF CARBAMATE TOXIN ON SNAIL GUT 99 mented and plasma membranes surround cy- toplasm lacking muscle filaments (Fig. 53). The most severe damage observed is in the stomach and the intestine. Furthermore, neurosecretory vesicles be- come more numerous (Figs. 54—56), and dense connections form between muscle and nerve tissue (Fig. 56). Intoxication with 0.01% molluscicide also disarrays the muscle fibers. In some cases, muscle envelopes without muscle fibres un- derlie the epithelium of the intestine after 24h and 30 h. The number of neurosecretory ves- icles also increase. After 0.001% OD, there is no apparent reaction of either muscle or nerve tissue. DISCUSSION The present paper was designed as a baseline study of cellular reactions in the slugs’ bodies to carbamate intoxication. Be- cause the molluscicide was orally applied, the cells of the digestive system were investi- gated as targets for effects of poisoning. Ina prior investigation, the passage of '*C- labeled Cloethocarb through the digestive system could be traced and labeled material could be shown to penetrate the cells (Trieb- skorn et al., 1990), thus indicating that all cells of the digestive tract are in direct contact with the poison. Whereas earlier workers report the influ- ence of carbamates on the nervous system alone (Pessah & Sokolove, 1983; Young & Wilkins, 1989), we showed that carbamate in- toxication produces conspicuous cellular re- actions in the digestive system as well, even though sublethal poisoning did not induce overt reactions at the macroscopic, organis- mic, level. The results of the study support the statement of Armstrong & Millemann (1974) that “damage to the nervous system through cholinesterase inhibition may not be the only or even the primary cause of death of ex- posed clams.” In the present study, three types of cellular reaction in the digestive system of Deroceras reticulatum can be distinguished: those that are detectable only after lethal intoxication, those that occur with the same intensity after lethal and sublethal poisoning, and reactions that are most intense after the application of sublethal concentrations. Reactions typical of lethal intoxication are damage to nuclei and mitochondria; alter- ations to the general cell outline, to the basal cell surfaces and to muscle and nerve tissue; and formation of clefts between the epithelia and the underlying connective, muscle and nerve tissues. Most of these reactions are ab- sent after 0.001% OD, but they appear at 0.1% OD in a few cells and with less intensity after 30 h. The fact that these reactions be- come visible only after lethal intoxication might indicate either that these cellular struc- tures have a lower sensitivity to the poison, or that those reactions are secondary responses of the cells. In the first case, only high con- centrations of the toxin would lead to unspe- cific stress reactions that finally induce cell FIG. 21. Oesophagus (control). Mitochondrion (mi) in storage cell (arrows: cristae). FIG. 22. Intestine (2% Cloethocarb, 1h). Mitochondria (mi) swollen, cristae (arrows) partly reduced. ger: granular endoplasmic reticulum. FIG. 23. Stomach (2% Cloethocarb, 5h). Mitochondria (mi) with ruptured membranes (arrows). FIG. 24. Intestine (control). Wide-luminar granular ER (ger) of mucous cell. FIG. 25. Hepatopancreas (control). Granular ER (ger) of crypt cell. n: nucleus. FIG. 26. Hepatopancreas (0.01% Cloethocarb, 1h). Degranulation of granular ER (ger) in crypt cell (arrows). FIG. 27. Oesophagus (2% Cloethocarb, 1h). Cisternae of granular ER (ger) in mucous cell grossly dilated. FIG. 28. Crop (2% Cloethocarb, 5h). Cisternae of ER (er) touching lipid droplet (li). FIG. 29. Hepatopancreas (2% Cloethocarb, 1h). Cisternae of ER (er) surrounding lipid droplet (li), mito- chondria (mi) and vesicles (v) in crypt cell. FIG. 30. Hepatopancreas (2% Cloethocarb, 16h). Membrane whorls of ER (er) surrounding lipid droplet (li) and vesicles (v). FIG. 31. Hepatopancreas (0.01% Cloethocarb, 5h). Vesicles of ER (arrows) in basal part of crypt cell. FIG. 32. Hepatopancreas (0.1% Cloethocarb, 30 min). Ruptured membranes (arrows) of ER. li: lipid; mi: mitochondrion. FIG. 33. Intestine (0.1% Cloethocarb, 5h). Transverse and longitudinal section of tubular system arising from ER. Arrows: lumen of cisternae. FIG. 34. Intestine (0.1% Cloethocarb, 5h). Transverse and longitudinal section of tubular system arising from ER. Tubules open into wide-luminar ER cisterna (er). 100 TRIEBSKORN & KUNAST Pe 0.5 um e e i Whey) Ke el fe EFFECT OF CARBAMATE TOXIN ON SNAIL GUT 101 death. In the second case, interaction of the toxin with other targets in the slug’s body might cause the reactions and these would follow other symptoms of cell death. Carbamates, as nerve toxins, induce un- controlled muscle contractions that do not ap- pear after sublethal concentrations. As a con- sequence of these muscle convulsions, the epithelial cells might be stretched, leading to basal cell extension, such as to induce detachment of the cells from the basal mem- brane. This phenomenon has also been de- scribed by Vogt (1986) for the hepatopan- creas of Penaeus monodon after exposure to dimethoate, which is also an inhibitor of cho- linesterases. It might be that the toxin distorts the cytoskeleton, thereby changing the shape of the cell and displacing the mitochondria. Besides damaged nuclei, fully intact nu- culei and others with conspicuous crystalline inclusions in the karyoplasm occur. This ob- servation accentuates the importance of the heterogeneity of the cellular reaction. The crystalline inclusions in the karyoplasm might result from either intensified productiv- ity Or serious injury to metabolic or regulatory processes. The reactions of the mitochondria, swelling and reduction of the cristae, are often consid- ered unspecific stress symptoms (Rez, 1986). We have demonstrated in earlier studies (Triebskorn, 1988; 1989a), however, that there are several other modes of mitochon- drial response to different molluscicides. Swelling of the organelles and reduction of cristae can ensue immediately upon intoxica- tion, but can also result from other reactions such as an increase in number or size of in- tramitochondrial granules or the appearance of glycogen-like particles in the matrix. Fur- thermore, swelling of the mitochondria could also be induced in other cellular systems, such as the fish liver, by poisoning or by cer- tain diets (Braunbeck et al., 1989; Segner et al., 1987). We assume, therefore, that swell- ing of the organelles and reduction of the cris- tae can be induced in various ways by exog- enous or endogenous stresses. Even if the symptoms are similar, the causes of the re- sponse might be totally different. One attempt to explain the reaction is that of Goyer & Rhyne (1975), who propose that the swelling of the organelles results from inhibition of ion transport and protein synthesis. It also seems possible that the toxin interacts with the mito- chondrial membrane so as to change its per- meability to ions. Reactions that are discernible after the sublethal molluscicide concentration of 0.01% and are intense after lethal intoxication are: reduction of microvilli, often associated with formation of apical protrusions of the cyto- plasm (surface blebs); presence of a coating upon the apical surfaces of the cells; thicken- ing of the basal membrane; intensification of fusion between small vesicles and vacuoles FIG. 35. Stomach (control). Golgi apparatus of mucous cell. Small vesicles (v) arising from granular ER (ger) fuse with cis-face cisternae. On trans-face (tf), small vesicles (v) and mucous vacuole (muv) are visible. FIG. 36. Hepatopancreas (control). Golgi apparatus producing large vacuoles (vac). cf: cis-face; tf: trans- face. FIG. 37. Crop (0.1% Cloethocarb, 5h). Golgi apparatus in mucous cell with cis-face cisternae (arrows) closely stacked. vac: vacuole. FIG. 38. Intestine (2% Cloethocarb, 5h). Increased number of small vesicles (arrows) surrounding Golgi apparatus in mucous cell. FIG. 39. Oesophagus (2% Cloethocarb, 5h). Storage cell. Trans-face cisternae of small Golgi apparatus greatly inflated (arrows). er: granular ER. FIG. 40. Oesophagus (2% Cloethocarb, 5h). Storage cell. Small Golgi apparatus with cis-face cisternae tightly stacked (arrows). FIG. 41. Oesophagus (2% Cloethocarb, 30h). Storage cell. Small Golgi apparatus with disorganized cister- nae; membranes irregularly arranged and sometimes ruptured (arrows). FIG. 42. Hepatopancreas (control). Apex of digestive cell with microvilli (mv), endocytotic channels (ec), endocytotic vesicles (env), lysosomes (ly) and digestive vacuoles (dv). FIG. 43. Hepatopancreas (control). Digestive vacuoles (dv) and lysosomes (ly) in digestive cell. FIG. 44. Hepatopancreas (0.1% Cloethocarb, 5h). Lysosomes (ly) fusing with vacuolar system (vac; arrows) in digestive cell. FIG. 45. Hepatopancreas (0.1% Cloethocarb, 5h). Fusion of lysosomes (ly) with vacuoles (arrows) in digestive cell. FIG. 46. Hepatopancreas (2% Cloethocarb, 16h). Autolytic digestive cell with severely damaged vacuolar system. (arrows: intact vacuoles; n: nucleus). 102 TRIEBSKORN & KUNAST > 4 + £ Kee / } + où . AR E er h QT EFFECT OF CARBAMATE TOXIN ON SNAIL GUT 103 in the digestive cells of the hepatopancreas; reduction of storage products; condensation of the cis-face stacks of the Golgi apparatus and formation of membrane whorls by ER cis- ternae. The first four reactions described are re- garded as effects induced by the direct con- tact of toxin and cell surfaces. The thicken- ing of the basement membrane and the formation of an apical coat protect the apical and basal surfaces of the cell, preventing fur- ther penetration of the toxin from either the lumen of the digestive tract or from the hemolymph space. The origin of the coat is not known. Perhaps the cells themselves produce it but maybe the mucous cells of the stomach and the intestine form it, inasmuch as exudation of mucus intensifies after intox- ication (Triebskorn & Ebert, 1989). The reduction of microvilli, the formation of blebs and the increased fusion of vesicles and vacuoles in the digestive cells of the hepatopancreas might result from the inter- action of the lipophilic molluscicide with membranes. This interaction might induce changes in composition, fluidity and finally stability of the membranes (Axiak et al., 1988; Moore, 1982, 1985; Moore et al., 1982). Although the reactions mentioned above have often been described as unspecific cell responses to any stress (Rez, 1986), e.g. starvation (Segner et al., 1987), we assume that the plasma and the lysosomal mem- branes are very unstable and sensitive sys- tems that react quickly to any alteration of cel- lular homeostasis. Lysosomal instability in mussels has been used as a measure of en- vironmental pollution (Moore, 1982, 1985; Moore et al., 1982; Lowe et al., 1981). In such studies, the reduction of membrane stability has been investigated with light mi- croscopy and enzyme-histochemistry but not with the electron microscope. In the present study, we could show that the membranes of the small vesicles in the digestive cells of the hepatopancreas were not affected. As a con- sequence of the intensified fusion between small and large vacuoles, the number of large vacuoles increases after intoxication. Moore et al. (1982) assumed that changes in mem- brane fluidity induce this altered rate of vesi- cle fusion. The membranes of the resulting large autolysosomes are less stable and often rupture. Bayne et al. (1985) distinguish be- tween these autolysosomes, a typical re- sponse to stress, and the heterophagosomes, large vacuoles involved in pinocytosis and in- tracellular digestion in untreated animals. The decrease in stability of the ER and Golgi membranes, especially after ingestion of lethal concentrations, might also result from the capacity of the carbamate to interact with membranes. The more important reac- tions of the ER, however, are those to suble- thal concentrations; these will be discussed later. An increased call upon energy resources to initiate protective or detoxification processes might lead to a quick reduction of lipid and glycogen in the storage cells. Recio et al. (1988) also describe a reduction of storage products in Arion ater induced by zinc. They characterize the reaction to intoxication as similar to the effects of starvation. Because in our recent study peroxisomes and ER cister- nae were often observed in close contact with lipid droplets, and because our histochemical enzyme tests revealed that catalase was in- duced by Cloethocarb (Triebskorn, 1989b), it seems possible that B-oxidation, or peroxida- FIG. 47. Oesophagus (0.001% Cloethocarb, 30 min). Increased number of mature mucous cells (muc). n: nucleus. FIG. 48. Crop (control). Lipid (li) and glycogen storage (gl) in storage cell. FIG. 49. Crop (2% Cloethocarb pellet, 1h). Reduction of glycogen, fusion of lipid droplets (li). FIG. 50. Oesophagus (2% Cloethocarb, 3h). Decrease of lipid storage (li) and increased numbers of elec- tron-dense vesicles (ev). FIG. 51. Oesophagus (control). Muscle (mt) and nerve tissues (nt) underlying epithelium. FIG. 52. Oesophagus (2% Cloethocarb, 5h). Irregularly oriented muscle filaments (arrows). FIG. 53. Crop (2% Cloethocarb, 24h). Fragmentation of muscle tissue (mt) and muscle envelope lacking muscle filaments (arrows). FIG. 54. Oesophagus (2% Cloethocarb, 30 min). Nerve with increased numbers of neurosecretory vesicles (nv). mt: muscle tissue. FIG. 55. Stomach (0.5% Cloethocarb, 5h). Nerve with increased number of neurosecretory vesicles (nv). FIG. 56. Oesophagus (2% Cloethocarb, 30 min). Dense connection between muscle (mt) and nerve tissues (nt; arrow). 104 TRIEBSKORN & KUNAST tive processes, or both, are involved in the reduction of lipid stores. Furthermore, there is perhaps a relation between peroxidation and membrane destruction, as has often been de- scribed for vertebrates (Tappel, 1975; Reck- nagel, 1967). The intensity of the alterations and damage after lethal intoxication are shown to be more severe than after sublethal intoxication. Al- though, in this case, a dose-response rela- tionship is obvious, no positive correlation could be found between dose and effect, if the reactions after low and high lethal concentra- tions were observed. That 0.1% OD fre- quently causes more severe damage than 2% could be explained by the fact that high con- centrations induce protective mechanisms or potential defense reactions, such as exuda- tion of mucus, more quickly than low concen- trations. Given the capacity of the mucus to dilute the toxin with the passage of time, the relative amount of the chemical in the lumen of the digestive tract might therefore be lower after 2% than after 0.1%, even if a higher con- centration were ingested. Furthermore, Bo- wen & Jones (1985) assume that high con- centrations of molluscicides prevent the animal from taking up lethal doses of the pes- ticide owing to quickly induced paralysis of the crop. A higher concentration of the pesti- cide thus might not be related necessarily to a higher efficiency as postulated by Fries & Tripp (1976). In the third category are responses to lethal oral doses that are more intense after suble- thal intoxication. Such is the case of degran- ulation and dilation of the granular endoplas- mic reticulum (ER), the proliferation and vesiculation of the ER, the formation of a tu- bular system and of membrane whorls by the ER and the production of large mucous vac- uoles. Reactions of the ER to intoxification similar to those described in this study have often been seen in both vertebrates (Sivarajah et al., 1978; Klaunig et al., 1979) and mussels (Nott & Moore, 1987). Because transitions be- tween smooth and granular ER were visible, especially in the crypt cells of the hepatopan- creas, and because Klaunig et al. (1979) de- scribe a continuity between two forms of ER, we hesitate to refer to degranulated ER as smooth ER. It is unclear, moreover, whether ribosome-free ER necessarily functions as smooth ER. Klaunig et al. (1979) interpret the circular arrays of ER as a response to sub- stances that induce enzymes of the mixed function oxygenases system. A similar con- clusion can be drawn from our enzyme-his- tochemical tests, which showed an increase of NADPH-neotetrazolium reductase in cell areas in which ER-proliferation and whorls of ER cisternae occurred (Triebskorn, 1989a, b). Reactions of the endoplasmic reticulum are stronger after sublethal intoxication than after a lethal dose, most probably because de- structive effects are less important than in- duced reactions of a potentially protective na- ture. Any new molluscicide developed should not induce such defence mechanisms. A second mechanism that intensifies after sublethal intoxication is the production of large mucous vacuoles owing to an increased activity of the secretory system (ER, Golgi ap- paratus). Such large mucous vacuoles oc- curred even in cells having the shape typical of immature mucous cells, which generally have prominent Golgi complexes, large amounts of granular ER and only few mucous vacuoles. Large amounts of mucus are ex- uded as an immediate response to the inges- tion of lethal doses of the molluscicide. As already mentioned above, the mucus might serve the animal to dilute the toxin. Moreover, as shown in an earlier study, the animals are capable both of increasing the quantity, and of varying the quality, i.e. the chemical com- position, of the mucus (Triebskorn & Ebert, 1989). In the case of Cloethocarb, the exuda- tion of acidic mucus can be regarded as a kind of incidental detoxification, because the toxin is less stable under acidic conditions (Kü- nast, pers. comm.). Nevertheless, the reason for the alteration in the chemical composition of the mucus is not known. Because we could demonstrate activity of y-glutamyltransferase and an increase in amount of SH-groups in the mucous cells of the digestive system (Triebskorn, 1988), we assume that conjuga- tion processes (glutathione conjugation) might be related to secretion of mucus. An increase in the number of mucous cells, such as described by Neff et al. (1987) as a re- sponse of Arctic marine bivalves to experi- mentally spilled oil, could not be detected. Although it might serve slugs as a defense mechanism, intensified exudation of mucus can also kill them; specific molluscicides can not only enhance secretion of mucus but also damage the ultrastructure of cells, especially immature ones. That is the reason that induc- tion of mucus secretion would finally lead to a desiccation of the animal and loss of mucous EFFECT OF CARBAMATE TOXIN ON SNAIL GUT 105 cells would prevent production of the very mu- cus that protects the surface of the animal from desiccation and that is necessary for di- gestion in the intestinal lumen. We therefore agree with the conclusions of Airey et al. (1989), who regard the mucous cells as one of the targets for specific molluscicial interfer- ence. Bowen & Jones (1985) also advocate pur- suing baseline studies in the development of new substances and suggest that mollusci- cides should be “packaged so as to effect a slow release and combined with a phagostim- ulant and pinocytosis inducer.” We think that such basic studies revealing specific sites with which molluscicides could interfere are a necessary adjunct to screening programs in industrial research, of which the objectives are the discovery of new, more specific and less hazardous molluscicides. ACKNOWLEDGMENTS This study was partly supported by the Ger- man Research Council (DFG Sto 75/9). Per- sonal thanks go to Thomas Braunbeck and to Gunter Vogt for the revision of the paper and to Rainer Günzler for his helpful assistance in the arrangement of the tables. LITERATURE CITED AIREY, W. J., |. Е. HENDERSON, J. A. PICKET, С. C. SCOTT, J. W. STEPHENSON & C. M. WOODCOCK, 1989, Novel chemical approaches to mollusc control. Proceedings of the British Crop Protection Council, 41: 301-308. ARMSTRONG, D. A. 8 R. E. MILLEMANN, 1974, Pathology of acute poisoning with the insecticide Sevin in the bent-nosed clam Macoma nasuta. Journal of Invertebrate Pathology, 24: 201-212. AXIAK, V., J. J. GEORGE & M. N. MOORE, 1988, Petroleum hydrocarbons in the marine bivalve Venus verrucosa: Accumulation and cellular re- sponse. Marine Biology, 97: 225-230. BAYNE, B. L., D. A. BROWN, K. BURNS, D. R. DIXON, A. IVANOVICI, D. R. LIVINGSTONE, D. М. LOWE, M. N. MOORE, А. В. D. STEBBING & J. WIDDOWS, 1985, The effects of stress and pollution on marine animals. Praeger Scientific, New York. BOWEN, J. D. & G. W. JONES, 1985, Getting pes- ticides into cells. Industrial Biotechnology (Wales), 5: 29-32. BRAUNBECK, T., V. STORCH & R. NAGEL, 1989, Sex-specific reactions of liver ultrastructure in ze- bra fish (Brachydanio rerio) after prolonged sub- lethal exposure to 4-nitrophenol. Aquatic Toxicol- ogy, 14: 185-202. BRAUNBECK, T., 1989, Cytopathologische Ve- ránderungen in der Fischleber durch Umwelt- chemikalien. Beitráge zur Okotoxikologie. Dis- sertation, Heidelberg. FRIES, C. & M. R. TRIPP, 1976, Effects of phenol on clams. Marine Fishery Reviews., 38: 10-11. GLEN, D. M. & J. A. ORSMAN, 1986, Comparison of molluscicides based on metaldehyde, methio- carb or aluminum sulphate. Crop Protection, 5: 371-375. GODAN, D., 1979, Schadschnecken. Ulmer Ver- lag, Stuttgart. GOYER RIVAS В. 6. RAYNE; 1975, Toxic changes in mitochondrial membranes and mito- chondrial function. Pp. 383—428 in: TRUMP, В. F. & A. U. ARSTILA, eds., Pathology of all mem- branes. Vol. 1, Academic Press, New York. HENDERSON, |. Е. & К. A. PARKER, 1986, Prob- lems in developing chemical control of slugs. As- pects of Applied Biology, 13: 341-347. KARNOVSKY, M. J., 1971, Use of ferrocyanide- reduced osmium tetroxide in electron micros- copy. Journal of Cell Biology, 51: 284. KEMP, N. J. & P. F. NEWELL, 1985, Laboratory observations on the effectiveness of methiocarb and metaldehyde baits against the slug Dero- ceras reticulatum (Muller). Journal of Molluscan Studies, 51: 228-230. KLAUNIG, J. E., M. M. LIPSKY, B. F. TRUMP & D. Е. HINTON, 1979, Biochemical and ultrastruc- tural changes in teleost liver following subacute exposure to PCB. Journal of Environmental Tox- icology, 2: 953-963. LOWE, D. М., М. N. MOORE & В. CLARKE, 1981, Effects of oil on digestive cells in mussels: quan- titative alterations in cellular and lysosomal struc- ture. Aquatic Toxicology, 1: 213-226. MARTIN, T. J., & J. В. KELLY, 1986, The effect of changing agriculture on slugs as pests of cereals. British Crop Protection Council of Pest Diseases, 411-424. MILLS, J. D., E. R. BAILEY, M. A. WEDGWOOD & C. R. McCROHAN, 1989, Effects of mollusci- cides on feeding behaviour and neuronal activity. Proceedings of the British Crop Protection Coun- cil, 41: 77—84. MOORE, M. N., 1982, Lysosomes and environ- mental stress. Marine Pollution Bulletin, 13: 42— 43. MOORE, М. М., В. К. PIPE & S. V. FARRAR, 1982, Lysosomal and microsomal responses to envi- ronmental factors in Littorina littorea from Sullom Voe. Marine Pollution Bulletin, 13: 340-345. MOORE, M. N., 1985, Cellular responses to pollut- ants. Marine Pollution Bulletin, 16(4): 134-139. NEFF, J. M., В. Е. HILLMANN, В. $. CARR, В. L. BUHL & J. J. LATHEY, 1987, Histopathological and biochemical responses in arctic marine bi- valve molluscs exposed to experimentally spilled oil. Arctic, 40, Supp.(1): 220-229. МОТТ, Ч. А., & M. N. MOORE, 1987, Effects of 106 TRIEBSKORN & KUNAST polycyclic aromatic hydrocarbons on molluscan lysosomes and endoplasmic reticulum. His- tochemical Journal, 19: 357-368. PESSAH, J. N. & P. G. SOKOLOVE, 1983, The interaction of organophosphate and carbamate insecticides with cholinesterases in the terrestrial pulmonate Limax maximus. Comparative Bio- chemistry and Physiology, 74C(2): 291-297. PORT, С. М. & С. В. PORT, 1986, The biology and behaviour of slugs in relation to crop damage and control. Agricultural Zoology Reviews, 1: 253— 297. PRYSTUPA, B. D., N. J. HOLLIDAY & R. B. WEB- STER, 1987, Molluscicide efficacy against the marsh slug Deroceras laeve (Stylommatophora; Limacidae) on strawberries in Manitoba. Journal of Economic Entomology, 80(4): 935-943. RECIO, A., J. A. MARIGOMEZ, E. ANGULO & J. MOYA, 1988, Zinc treatment of the digestive gland of the slug Arion ater L. 2. Sublethal effects at the histological level. Bulletin of Environmental Contamination and Toxicology, 41: 865-871. RECKNAGEL, R. O., 1967, Carbon tetrachloride hepatotoxicity. Pharmacological Reviews, 19: 145. REZ, G., 1986, Electron microscopic approaches to environmental toxicity. Acta Biologica Hungarica, 37(1): 31-45. RICHARDSON, K. C., L. JARRET & E. H. FINKE, 1960, Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol- ogy, 35: 313-328. SEGNER, H., P. BURKHARDT, E. M. AVILA, J. V. JUARIO & V. STORCH, 1987, Nutrition-related histopathology of the intestine of milkfish Chanos chanos fry. Diseases of Aquatic Organisms, 2: 99-107. SIVARAJAH, K., C. S. FRANKLIN & W. P. WILLIAMS, 1978, Some histopathological effects of Arochlor 1254 on the liver and gonads of rain- bow trout Salmo gairdneri and carp, Cyprinus carpio. Journal of Fish Biology, 13: 411-414. SPURR, А. R., 1969, A low viscosity embedding medium for electron microscopy. Journal of Ul- trastructural Research, 26: 31-43. TAPPEL, A. L., 1975, Lipid peroxidation and fluo- rescent molecular damage to membranes. In: TRUMP, B. F. & A. ARSTILA, eds., Pathobiology of all membranes. Vol. |. Academic Press, New York, pp. 145-170. TRIEBSKORN, R., 1988, Molluskizid-induzierte Reaktionen im Verdauungstrakt von Deroceras reticulatum (Muller). Verhandlungen der Deutsch- en Zoologischen Gesellschaft, 81: 332. TRIEBSKORN, R., 1989a, Ultrastructural changes in the digestive tract of Deroceras reticulatum in- duced by a carbamate molluscicide and by met- aldehyde. Malacologia, 31(1): 141-156. TRIEBSKORN, R., 1989b, The influence of a mol- luscicide on two Cell types in the digestive system of Deroceras reticulatum (Muller). 16th Interna- tional Malacological Congress, Tubingen, in prep. TRIEBSKORN, R. & D. EBERT, 1989, The impor- tance of mucus production in slugs’ reaction to molluscicides and the impact of molluscicides on the mucus producing system. Proceedings of the British Crop Protection Council, 41: 373-379. TRIEBSKORN, R., C. KUNAST, R. HUBER & G. ВВЕМ, 1990. The tracing of a '*C-labeled car- bamate molluscicide through the digestive sys- tem of Deroceras reticulatum (Muller). Pesticide Science, 28: 321-330. VOGT, G., 1986, Monitoring of environmental pol- lutants such as pesticides in prawn agriculture by histological diagnosis. Aquaculture, 67: 157-164. WRIGHT, A. A. & R. WILLIAMS, 1980, The effects of molluscicides on the consumption of bait by slugs. Journal of Molluscan Studies, 46: 265— 281. YOUNG, A. G. & R. M. WILKINS, 1989, The re- sponse of invertebrate acetylcholinesterase to molluscicides. Proceedings of the British Crop Protection Council, 41: 121-128. Revised Ms. accepted 13 February 1990 MALACOLOGIA, 1990, 32(1): 107-130 THE PELAGIC FAMILY ATLANTIDAE (GASTROPODA: HETEROPODA) FROM HAWAIIAN WATERS: A FAUNISTIC SURVEY Roger R. Seapy Department of Biological Science, California State University, Fullerton Fullerton, California 92634, U.S.A. ABSTRACT The atlantid heteropod fauna of Hawaiian waters is composed of 13 species, including Oxy- gyrus keraudreni, Protatlanta souleyeti and 11 species of Atlanta. Species characterizations are accompanied by scanning electron micrographs of the shells for all species, color photographs of six live species and a key to the Hawaiian atlantids. Key words: Atlantidae, Heteropoda, Hawaii, taxonomy, shell morphology, operculum morphol- ogy, eye morphology. INTRODUCTION Among the several groups of pelagic gas- tropods, the family Atlantidae (Heteropoda: Mesogastropoda) is perhaps the most poorly understood taxonomically by most zooplank- ton biologists. This is undoubtedly due to their highly similar shell morphologies and the fact that species identifications have been based almost entirely on shell structure. In addition, the atlantids are difficult to work with because of their microscopic size; shell diameters of most individuals from Hawaiian waters range from about 0.6-0.7 mm in recently metamor- phosed individuals to about 2 mm in adults, although two species are as much as 4 mm and one species is nearly 9 mm in diameter. Identifications are usually made under a dis- section microscope. The important taxonomic features of the shell spire (the number, shape and sculpture of the whorls) are often difficult to see, however, even at higher magnifica- tions. In this and other recent studies, dis- cussed below, the scanning electron micro- scope (SEM) has proven to be essential in resolving fine details of spire structure. The first comprehensive review ofthe taxon- omy of the atlantids was that of Tesch (1949). He reduced the number of recognized species from about 30 to ten based on the voluminous collections made during the Dana Expedition to the Atlantic, Pacific and Indian Oceans. Two ofthe genera, Oxygyrus and Protatlanta, inthe family Atlantidae were monotypic and re- mained unchanged, although Tesch reduced the number of species in the third genus, At- lanta, to eight. Since the monograph by Tesch, 107 only one major faunistic study (Richter, 1974) and one taxonomic review (van der Spoel, 1976) have been completed. In addition to the eight species recognized by Tesch, Richter (1974) included six others. Of these six, A. oligogyra Tesch, 1906, A. gibbosa Souleyet, 1852, and A. affinis Tesch, 1906, had been described prior to Tesch’s revision. The re- maining three, A. echinogyra Richter, 1972, A. plana Richter, 1972, and A. meteori Richter, 1972, were subsequently described. In his re- view of the atlantids in 1976, van der Spoel also added six species, A. pacifica Tokioka, 1955, A. peresi Frontier, 1966, A. gibbosa, A. tokiokai van der Spoel & Troost, 1972, A. echi- nogyra and A. plana, to the eight recognized by Tesch in 1949. Among these six, however, only three, A. gibbosa, A. echinogyra and A. plana, overlapped with those identified by Richter (1974) from the Indian Ocean. Identification of the various species of АН lanta has been based almost exclusively on shell morphology, although eye, opercular and radular morphology can be very impor- tant characteristics for the recognition of cer- tain species. Tokioka (1961) described the opercula of a number of atlantids. He found that the opercula of most species were similar and differed only in overall shape and location of the gyre (or spiral portion). In two species, however, the opercular gyres were uniquely ornamented. Tokioka characterized the oper- culum of A. inflata Souleyet, 1852, as having a spiral row of claw-like structures around the central portion of the gyre and that of A. tur- riculata d'Orbigny, 1836, as having two rows of short spines that spiral outward from the 108 SEAPY Type a Type b Type c FIG. 1. The three morphological types of opercula found in the Atlantidae (after Richter, 1974). The opercula were drawn from specimens collected during this study. A. Type a (macro-oligogyre) operculum is from a 1.6 mm Protatlanta souleyeti. B. Type b (micro-oligogyre) operculum is from a 2.2 mm Atlanta meteori. C. Type c (monogyre) operculum is from a 1.4 mm Atlanta helicinoides. G: opercular gyre. Scale bar is 0.2 mm. center of the gyre. Richter (1972) subse- quently showed that the operculum of A. in- flata lacked Spiral sculpture on the gyre, how- ever, and that Tokioka had actually figured the opercula of two undescribed species, which Richter had collected from the Indian Ocean and had named A. echinogyra and A. plana. Three basic types of opercula, termed macro-oligogyre, micro-oligogyre and mono- gyre, were recognized by Richter (1961). In his 1974 paper Richter termed these Types a, band с. They differ in overall shape and in the position and number of turns of the gyre (Fig. 1). Among the Indian Ocean species, seven had Type b opercula, while five had Type c and three had Type a opercula (Table 1). Eye morphology has been little used in dis- tinguishing the species of atlantids. This may be due to difficulties encountered in seeing details of eye structure through the shell of preserved animals, inasmuch as the shell can become very opaque following preservation. Van der Spoel (1972) described a procedure for clearing such specimens without destroy- ing the shell so that the soft parts can be seen. In this same paper van der Spoel illustrated the eyes of nine species of Atlanta, among which only one (A. helicinoides Souleyet, 1852) pos- sessed a distinctive morphology. This eye type was characterized by a very broad pigmented base into which the spherical lens was re- cessed. Richter (1974) concluded that three basic eye types (termed Types a, b and c) could be distinguished among the species of atlantids (Fig. 2). The broad-based eye of A. helicinoides (termed Type c) is markedly dif- ferent from the more cuboidal shape of the other two eye types. In all three eye types the lens rests in a cup of pigmented tissue. This pigmented tissue is continuous (Type c) or is interrupted by an approximately triangular, un- pigmented window (Types a and b). The latter two eye types are easily distinguished by the presence (Type b) or absence (Type a) of a narrow, transverse slit in the distal portion of the pigmented tissue (Fig. 2). Among those species identified by Richter (1974) from the Indian Ocean, Type c eyes occurred in only A. helicinoides and O. keraudreni, while Type a and b eyes were equally distributed among the remaining species (Table 1). Radular morphology has been largely dis- regarded as a taxonomic character in the At- lantidae (Tesch, 1949; van der Spoel, 1976), although Richter (1986, 1987, 1990) has used radular differences to separate species hav- ing very similar shell morphologies. Earlier, Richter (1961) characterized the radulae of nine species of Atlanta and concluded that two types (I and Il) could be distinguished HAWAIIAN ATLANTIDAE 109 TABLE 1. Species in the family Atlantidae recognized by Richter (1974, 1986, 1987, 1990). Whorl number refers to shell whorl in which whorl width increases rapidly (see text). Eye types (a, b and c) and opercular types (a, b and с) are those characterized by Richter (1974). Radular types (I and Il) are those described for nine species by Richter (1961). Whorl Eye Opercular Radular Species number type type type *Oxygyrus keraudreni (Lesueur, 1817) ÉS с ey | *Protatlanta souleyeti (Smith, 1888) 3 a a | “Atlanta lesueuri Souleyet, 1852 3 b b Il “Atlanta oligogyra Tesch, 1906 3 a b — “Atlanta peroni Lesueur, 1817 4 b b Il Atlanta gaudichaudi Souleyet, 1852 4 b b Il “Atlanta plana Richter, 1972 Ч а b —- “Atlanta echinogyra Richter, 1972 4 a С — *Atlanta fusca Souleyet, 1852 5 a a | *АНата turriculata d'Orbigny, 1836 5 а а — “Atlanta inflata Souleyet, 1852 5 a C | *Atlanta helicinoides Souleyet, 1852 5 С (© | Atlanta inclinata Souleyet, 1852 5 b € -- *Atlanta tokiokai van der Spoel & Troost, 1972 6 b € Il Atlanta gibbosa Souleyet, 1852 6 b b — “Atlanta meteori Richter, 1972 6 b b — *Denotes species identified from Hawaiian waters **Whorl counts not made because this species has involute spire ***Operculum broadly triangular to trapezoidal; not comparable with the opercula of Protatlanta and Atlanta L DP PP UW Туре а Туре с Туре b FIG. 2. The three morphological types of eyes found т the Atlantidae (after Richter, 1974). Illustrations of Type a and b eyes modified from drawings in Richter (1974, Fig. 3). Type с eye is from a specimen of Atlanta helicinoides (shell length = 1.6 mm) from Hawaiian waters. DP: distal portion of pigmented tissue; L: lens; PP: proximal portion of pigmented tissue; TS: transverse slit in distal pigment; UW: unpigmented window. Scale bar (0.2 mm) applies only to Type c eye. Sizes of Type a and b eyes not given by Richter (1974). (Table 1). These two species groups were also distinguished on the basis of eye and opercular morphology (Richter, 1974); those species with Type | radulae had Type a orc eyes and Type а or с opercula, while species with Type Il radulae had Type b eyes and Type b opercula, except for A. tokiokai, which had a Type c operculum. The present paper characterizes Oxygyrus keraudreni (Lesueur, 1817), Protatlanta soul- eyeti (Smith, 1888), and 11 species of Atlanta based on material from plankton net samples collected off the island of Oahu between 1984 and 1986. Species descriptions are accom- panied by scanning electron micrographs of all species and color photographs of live an- 110 SEAPY TABLE 2. Numbers of specimens per sample examined from plankton net tows taken during cruises off western coast of Oahu in April 1984, March 1986, August 1986, and November 1986, and off northern coast of island of Hawaii in August 1986. See text for types of nets used, depths and volumes of water filtered during tows. Apr Mar Aug Aug Nov Species 1984 1986 1986* 1986** 1986 Total Atlanta lesueuri 1,060 75 202 181 513 2,031 Atlanta turriculata 171 115 555 58 186 1,085 Atlanta plana 299 388 144 198 30 1,059 Atlanta inflata 352 274 209 104 ИЗ 1,052 Atlanta peroni 332 437 44 43 Uf 863 Protatlanta souleyeti 306 191 9 19 64 589 Atlanta meteori 120 75 Dit 90 2 338 Atlanta oligogyra 21 9 52 18 94 194 Atlanta helicinoides 58 35 42 8 30 173 Atlanta fusca 34 18 2 3 0 57 Atlanta echinogyra 0 0 27 1 19 47 Atlanta tokiokai 2 15 5 3 0 25 Oxygyrus keraudreni 11 3 0 0 0 14 *Oahu **Hawaii imals for six species. A key to the Hawaiian atlantids is included at the end of the paper. MATERIALS AND METHODS A total of 7,527 specimens of atlantids were examined (Table 2). The animals were re- moved from plankton samples collected dur- ing cruises of research vessels from the Uni- versity of Hawaii in waters off the western coast of Oahu (21°15'N, 158°20'W) and off the northwestern shore of Hawaii (19°43’N, 156°06’W). During a 10-14 April 1984 cruise off Oahu, 40 tows were taken with paired, opening-closing Bongo nets (70 cm mouth di- ameter), constructed of 0.5 mm mesh Nytex gauze. Oblique tows of 30 min duration were taken within 50 m depth intervals between the surface and 200 m and from 200 to 300 m. An average of 2,600 т? of water was filtered dur- ing each tow. During a 22-29 March 1986 cruise off Oahu, 15 oblique tows between the surface and about 300 m were taken with an open ring net (226 cm mouth diameter), con- structed of 0.5 mm mesh Nytex gauze. The tows averaged 35 min in duration, and an av- erage of 7,300 т? of water was filtered during each tow. Oblique tows to 300 m were taken using the 226 cm ring net during a 6-9 Au- gust 1986 cruise off Oahu (three tows) and off Hawaii (three tows). Average tow duration was 35 min, and the average volume of water filtered was 7,600 m°. During daytime hours on 23 November 1986 off Oahu, oblique tows to a target depth of 50 m were taken with the 226 cm ring net (three tows; average of 5,100 п? filtered) and open 70 cm Bongo nets (three tows; average of 1,800 т? filtered). Un- less used to obtain specimens for observation or photography, plankton samples were pre- served aboard ship in 4% formalin solution in buffered sea water immediately after collec- tion and were transferred to 40% isopropanol within 14 days. All shell measurements were made to the nearest 0.1 mm with an ocular micrometer in a Wild M5 dissection micro- scope. Because the keel of the shell was fre- quently damaged, all shell diameters were measured exclusive of the keel. During the March and August 1986 cruises, specimens were sorted from the fresh plank- ton samples for live photography using a Zeiss dissection microscope with Koda- chrome 64 color slide film and Kodak VRG 100 color negative film. Specimens were placed in filtered sea water in clear glass petri dishes. Vivitar 285 strobes were positioned on either side of the microscope stage and were angled obliquely to produce a dark background. A minimum of four specimens of each spe- cies were examined under a JEOL JSM-35CF scanning electron microscope (SEM). The shells were mounted on aluminum stubs to which double-sided tape had been attached, and were then cold sputter-coated with gold- palladium (60:40), 21 nm thickness, in a HAWAIIAN ATLANTIDAE 111 Pelco Model 3 sputter coater. Photographs were taken on Kodak T-MAX 120 black-and- white negative film. During preparation of specimens of Atlanta, drying did not produce any changes in the shape of the calcareous shell (composed of aragonite; Batten & Du- mont, 1976). However, because the adult shell and keel of Oxygyrus keraudreni and the keel of Protatlanta souleyeti are made of conchiolin (Richter, 1974; Batten & Dumont, 1976), drying resulted in shriveling and col- lapse of these organic shell components. To retain their original shape, a critical point dry- ing procedure was used prior to sputter- coating. Briefly, individual specimens were held between filter paper hats in specimen holders. They were transferred from ethanol solutions of 30% to 50% to 90% and to 100% (three times at each concentration), then placed in Freon 113 (transferred three times) and then critical point dried in carbon dioxide. Complete synonymies of the species char- acterized in this paper were given by van der Spoel (1976) and are not repeated here. Voucher specimens of each species were de- posited with the Bishop Museum, Honolulu, Hawaii, and the National Museum of Natural History, Smithsonian Institution, Washington, D.C. RESULTS AND DISCUSSION A total of 13 species of atlantids were re- corded from Hawaiian waters (Table 1). Two of the genera (Oxygyrus and Protatlanta) are monospecific, while the third (Atlanta) in- cludes the remaining eleven species. De- scriptions of these species are presented be- low. Because the shell morphologies of the lar- vae and adults of a species are quite different, and because the larvae and adults commonly occur together in plankton samples, shell dif- ferences are described here before proceed- ing to the species characterizations. The most conspicuous difference is that the keel of the adults is lacking in the larvae (Fig. 3A-D). In addition, the shell terminates in an apertural lip that is quite different in the adults and lar- vae. In adults the aperture is approximately triangular to oval in cross-sectional outline and is formed by the two halves of the outer- most (final) shell whorl and the base of the preceding shell whorl. In the larval shell the aperture is formed by two large lobes that are separated from the preceding shell whorl by broad lateral notches (Fig. 3A-D). The surface sculpture of the larval and adult shells of each species can be quite different. The larval shells of eight of the Hawaiian species pos- sess raised sculpture, which ranges in the ex- tent of development from simple (e.g. A. plana [Fig. 3A], with a small number of weakly-elevated spiral ridges) to complex (e.g. A. echinogyra [Fig. 3C], with prominent spiral ridges, angled cross-ridges and punc- tae). The postlarval whorls of the adult shell generally lack elevated ridges, although punctae are present in some species. Thus, the transition from the larval to the adult shell is often very distinct (e.g. A. echinogyra; Fig. 8E,F). Oxygyrus Benson, 1835 Oxygyrus keraudreni (Lesueur, 1817) (Fig. 3E-H) Material: A total of 14 specimens was ex- amined (Table 2), which ranged from larvae (less than 1.1 mm) to a 3.4 mm adult. Four individuals, ranging from 1.4 to 2.7 mm, were examined under the SEM. Species characterization: The adult shell and keel are of conchiolin, although the larval shell is calcareous and has prominent, zigzag spiral sculpture (Fig. 3E,G). The shell spire is involute (Fig. 3G). With age, the calcareous larval shell is overgrown by the conchiolin adult whorls. The conchiolin keel is tall and terminates abruptly at the shell aperture (Fig. 3E). Also, the keel is truncate along its ante- rior margin. The color of the adult shell and keel is a translucent, light bluish-purple. The eyes are large and Type c (Fig. 2C). The operculum (Richter, 1961: Fig. 18; van der Spoel, 1976: Fig. 133C) is very different from those of other atlantids. It is broadly triangular (nearly trapezoidal) and lacks the spiral por- tion (or gyre). Discussion: This species is collected infre- quently and in low numbers in Hawaiian wa- ters (Table 2). A maximal shell diameter of 10 mm was reported by Tesch (1949) and van der Spoel (1976). Richter (1982) recorded an- imals between 3 and 8 mm from the guts of immature dolphin fish. The largest specimen captured in the present study was only 3.4 mm. The shell of O. keraudreni is unique among the atlantids because it has an involute spire, rather than the outwardly-produced spire on the right side of the shell of the other two gen- 12 SEAPY FIG. 3. Scanning electron micrographs of larval shells of Atlanta plana (A,B) and A. echinogyra (C,D), and of adult shell of Oxygyrus keraudreni (E-H). All photographs are of right side of the shell taken either perpendicular to the shell plane or at a 60° tilt. Scale bars are 0.1 mm for larval shells: 0.5 mm for O. keraudreni at low magnification (E,F), and 0.1 ™m for O. keraudreni at high magnification (G,H). HAWAIIAN ATLANTIDAE 113 FIG. 4. Scanning electron micrographs of Protatlanta souleyeti (A-D) and Atlanta peroni (E-H). For each species four views are included; low magnification of right side of shell (upper left) and at 60° tilt (lower left); high magnification of spire (upper right) and at 60° tilt (lower right). Scale bars are 0.5 mm for low magni- fication, 0.1 mm for high magnification. 114 SEAPY era. Further, the adult shell is composed en- tirely of conchiolin (Richter, 1974; Batten & Dumont, 1976), the sclerotized protein that forms the outer periostracum layer of the gas- tropod shell (Hyman, 1967). In young individ- uals, such as the 1.9 mm shell illustrated by Tesch (1949: Fig. 1C) and in the 2.2 mm specimen shown here in Fig. 3E-H, the junc- tion between the larval and adult shell is clearly marked. During the critical point drying procedure used in this study, this junction was exaggerated by the partial elevation of the adult shell from the underlying larval shell. Protatlanta Tesch, 1908 Protatlanta souleyeti (Smith, 1888) (Figs. 1A, 4A-D, 5A) Material: A total of 589 specimens was ex- amined (Table 2), which ranged from larvae (less than 0.7 mm) to a 1.9 mm adult. Eight individuals, ranging from 0.9 to 1.7 mm were examined under the SEM. Species characterization: The shell is cal- careous and the keel is of conchiolin. The shell spire is smooth, lacking sculpture, and is slightly elevated (Fig. 4B,D). The keel has a glass-like transparency (Fig. 5A) and a curved, rectangular shape (Fig. 4A), extend- ing from the shell aperture to about one-half the circumference of the shell. The anterior margin of the keel is sharply truncate. The digestive gland is contained within the shell spire and is usually a light brownish-orange to reddish-brown (Fig. 5A). The eyes are Type a, and the operculum is Type a. Discussion: The maximal size of P. soul- eyeti in this study was only 1.9 mm, although this is greater than the adult size range of 1.0 to 1.5 mm cited by Tesch (1949) and van der Spoel (1976). The transparency and shape of the keel im- mediately distinguishes this species from all other atlantids. Protatlanta souleyeti is most similar in appearance to Atlanta lesueuri Soul- eyet, 1852, and A. oligogyra, for all three spe- cies have а compact spire comprised of a low number of smooth whorls. When the keel has broken off, as sometimes happened in the Hawaiian material, P. souleyeti can be some- what difficult to separate from these two spe- cies of Atlanta. In such instances the color of the shell spire can be used to separate P. souleyeti (brownish-orange to reddish-brown) from A. /esueuri (clear to light pink) and А. oligogyra (light violet). Atlanta Lesueur, 1817 The genus Atlanta differs from Oxygyrus and Protatlanta in having a shell and keel that are both calcareous. Separation of the species of Atlanta has been based largely on shell characteristics, as discussed above. One of the features of the shell that is easy to deter- mine and has been used commonly in the past is the total number of whorls comprising the adult shell. This number is not constant, how- ever, but increases with shell growth. Alterna- tively, the number of whorls comprising the inner portion of the shell is a feature that is not affected by the size of the adult animal at the time of capture. In her review of the hetero- pods, Thiriot-Quiévreux (1973) referred to the number of whorls comprising the spire for each of the atlantid species. In the present paper, a similar approach is used. Under the dissection microscope, the whorl in which the shell morphology of atlantids changes from that of the larva to that of the adult is often clearly demarcated. Even if this point of change cannot readily be detected, the dramatic increase in overall whorl size, indicated by a rapid increase in whorl width, that begins in the last larval whorl and contin- ues following metamorphosis is very distinc- tive. The shell whorl in which this region of rapid increase in whorl width occurs is used here as a taxonomic character. To make whorl counts, the shell must be oriented in a consistent manner. The specimen must be ro- tated until the protoconch is directed away from the viewer (Fig. 6). In A. /esueuri (Fig. 6A), for example, the protoconch comprises most of the first whorl and is followed by a narrow second whorl and a rapidly expanding third whorl. In A. peroni Lesueur, 1817 (Fig. 6C), on the other hand, the second and third whorls are narrow and the fourth whorl ex- pands rapidly. Among the 11 Hawaiian spe- cies, the whorl that expands rapidly is the third shell whorl in A. /esueuri (Fig. 6A) and А. oligogyra (Fig. 6B); the fourth whorl in A. per- oni (Fig. 6C), A. plana (Fig. 6E) and A. echi- nogyra (Fig. 6F); the fifth whorl in A. fusca Souleyet, 1852 (Fig. 6G), A. turriculata (Fig. 6H), A. inflata (Fig. 61) and A. helicinoides (Fig. 6J); and the sixth whorl in A. tokiokai (Fig. 6K) and A. meteori (Fig. 6L). For pur- poses of comparison with A. peroni and A. plana, a sketch of A. gaudichaudi Souleyet, 1852 (Fig. 6D), from Australian waters is in- cluded, although this species was not col- lected from Hawaiian waters. HAWAIIAN ATLANTIDAE FIG. 5. Laboratory photographs of live atlantids collected from southwest side of Oahu May 1987. A. Protatlanta souleyeti (0.8 mm). B. Atlanta lesueuri (1.2 mm). C. A. turriculata (0.9 mm). D. A. tokiokai (1.5 mm). Е. А. echinogyra (1.0 тт). Е. A. inflata (0.9 mm). 116 SEAPY FIG. 6. Sketches of atlantid shell spires viewed at right angles to axis of spire and oriented with protoconch directed upwards. Dashed line in each sketch to aid in counting of shell whorls. А. A. lesueuri. В. A. oligogyra. C. A. peroni. D. A. gaudichaudi. E. A. plana. F. A. echinogyra. G. A. fusca. H. A. turriculata. |. A. inflata. J. A. helicinoides. K. A. tokiokai. L. A. meteori. Scale bars are 0.5 mm. All sketches from specimens of atlantids collected off Hawaii, except for that of A. gaudichaudi, which was based on animals from Australian waters. Talay HAWAIIAN ATLANTIDAE FIG. 6G-L. 118 SEAPY Atlanta lesueuri Souleyet, 1852 (Figs. 5B, 6A, 7A-D) Material: A total of 2,031 specimens was examined (Table 2), which ranged from larvae (less than about 0.6 mm) to 1.9 mm adults. Seven specimens, ranging from 1.0 to 1.7 mm, were examined under the SEM. Species characterization: The shell spire is compact and low (Fig. 7B). The spire whorls are smooth, lacking any sculpture (Fig. 7C). The sutures between the whorls are incised (Fig. 7D). Rapid increase in whorl width oc- curs in the third shell whorl (Fig. 6A). The keel is high with a truncated anterior edge (Fig. 7A). Because it is quite fragile, however, the keel is commonly damaged and the truncated anterior margin might not be evident. The shell of the animal is clear (Fig. 5B), although the inner whorls can take on a light pink color (darkest in the sutures) in older specimens. The body is also clear (Fig. 5B), except for purple-red pigmentation at the end of the pro- boscis and at middle and distal locations on the opercular lobe. This pigmentation be- comes darker and more prominent in older individuals. The eyes are Type b, the opercu- lum is Type b. Discussion: Atlanta lesueuri is among the most abundant species of atlantids in Hawai- ian waters (Table 2). It resembles only one other species, A. oligogyra. Features that dis- tinguish the two species are discussed below under A. oligogyra. Atlanta oligogyra Tesch, 1906 (Fig. 7E-H) Material: A total of 194 specimens was ex- amined (Table 2), which ranged from larvae (less than 0.6 mm) to a 1.9 mm adult. Four specimens, ranging from 0.9 to 1.9 mm, were examined under the SEM. Species characterization: The shell spire is compact and low (Fig. 7F). The spire whorls are smooth, lacking any sculpture (Fig. 7G). The sutures between the first and second whorls are shallow, while those between the second and subsequent whorls are incised (Fig. 7G,H). The sutures have a very light vi- olet color. The keel is moderately tall and rounded in lateral profile (Fig. 7E). The eyes are Type a and the operculum is Type b. Discussion: The shell of A. oligogyra can be difficult to distinguish from that of the preced- ing species, А. lesueuri. Features used by Richter (1974) to characterize the shell of A. oligogyra and to separate it from that of A. lesueuri included a lower keel, a brown keel base and light violet inner surface of the ap- erture (in adults). The eyes of the two spe- cies, however, are distinctly different: Type a and small in A. oligogyra, and Type b and large in A. lesueuri. Despite these differ- ences, van der Spoel (1976) treated A. oli- gogyra as a synonym of А. lesueuri. In de- fense of his separation of the two species in his 1974 paper, Richter (1986) expanded on the species characterizations and included differences in the radulae. In the Hawaiian material, A. oligogyra could be distinguished from A. /esueuri on the basis of the Type a eyes (Type b in A. /esueuri), the relatively lower and more rounded keel (tall and truncated at the anterior edge in A. lesueuri), and the light violet color of the spire sutures (clear in A. /esueuri). The keel base of Hawaiian A. oligogyra is clear, not brown as reported by Richter for Indian Ocean speci- mens. Atlanta peroni Lesueur, 1817 (Figs. 4E-H, 6C) Material: A total of 863 specimens was ex- amined (Table 2), which ranged from larvae (less than about 0.7 mm) to an 8.4 mm adult. Six specimens, ranging from 1.6 to 3.8 mm, were examined under the SEM. Species characterization: The shell spire is low (Fig. 4H). The whorls comprising the spire are smooth, lacking any sculpture (Fig. 4G). The sutures between the first and second whorls are shallow, while those between sub- sequent whorls are deeply incised (Fig. 4H). Rapid increase in whorl width occurs in the fourth shell whorl (Fig. 6C). The moderately tall keel is rounded in profile (Fig. 4E). The keel base is clear in young individuals (i.e. less than about 2 mm), but changes from a light to a dark golden-brown in progressively older animals. The keel inserts between the fifth and sixth whorls in individuals greater than about 2 to 3 mm. The eyes are Type b, the operculum is Type b. Discussion: This species achieves the larg- est size (up to a diameter of 10 mm) in the genus Atlanta (Richter, 1974; van der Spoel, 1976). The largest specimen that | collected in Hawaiian waters was 8.4 mm, which ap- proaches a total diameter of 10 mm when the keel is included. Except for the golden-brown pigmentation that develops at the base of the keel with in- HAWAIIAN ATLANTIDAE An EEE ELECTRO FIG. 7. Scanning electron micrographs of Atlanta lesueuri (A-D) and A. oligogyra (E-H). Views and scale bars as in Fig. 4. 120 SEAPY creased age, most of the shells examined were clear. In some instances, however, the shell in juveniles was found to be light pink, which presumably persists and would ac- count for the light pink color seen in some adults (also reported by Thiriot-Quiévreux, 1973). The present characterization of the shell spire for Hawaiian A. peroni agrees with the descriptions of Tesch (1949) and van der Spoel (1976). In the A. peroni from the Indian Ocean examined by Richter (1974: Fig. 7), however, the whorls comprising the shell spire had an elevated, thin spiral ridge along the outer margin of each whorl. This elevated ridge was also indicated in the drawing by Frontier (1966: Fig. 4) of A. peroni from the Indian ocean. Such a ridge would appear to be lacking in the A. peroni from the Pacific and Atlantic oceans. Van der Spoel's de- scription of the species and illustrations of a specimen from the Atlantic Ocean (1976: Fig. 135A,B) do not include this ridge, nor does the scanning electron micrograph of a speci- men in Thiriot-Quiévreux (1973: Fig. 1C). Pre- sumably, the specimen used by Thiriot- Quiévreux came from the North Atlantic or the Mediterranean Sea. Tesch’s (1949) descrip- tion and drawing (1949; p. 16-17, Fig 9) of A. peroni also did not indicate such a ridge. The presence of an elevated spiral ridge on the shells of specimens collected from the Indian Ocean is problematical. The species identi- fied by Frontier and Richter as A. peroni could represent a morphological variant of A. peroni that is unique to the Indian Ocean. However, Richter (pers. comm.) now thinks that it is ei- ther an undescribed species or is a species that was described previously and is not cur- rently recognized. The shell morphology of A. peroni is close to that of only one other species from Hawai- ian waters, A. plana. Differences between these two species and A. gaudichaudi will be discussed below under A. plana. Atlanta plana Richter, 1972 (Figs. 3A-B, 6E, 8A-D, 9A-B) Material: A total of 1,059 specimens was examined (Table 2), which ranged from larvae (less than about 0.7 mm) to a 3.4 mm adult. Six specimens, ranging from 1.3 to 2.5 mm, were examined under the SEM. Species characterization: The shell spire forms a low cone (Fig. 8D). Under the dissec- tion microscope the spire can appear to lack spiral sculpture. Under the SEM, however, two weakly-developed spiral ridges are seen on the second and third whorls (Fig. 8C,D). In the last half of the third whorl, the spiral ridges break up and are replaced by spirally ar- ranged rows of small punctae (Fig. 8C). The sutures of the spire are violet. The shell whorl in which a rapid increase in width occurs is the fourth (Fig. 6E). The keel is rounded and somewhat low (Fig. 8A). The keel base is a copper-brown to golden-brown color. The eyes are Type a. The operculum is Type b (Fig. 9A) and possesses a low gyre with about 20 flattened, outwardly directed spines (Fig. 9B). Discussion: Like Richter (1974), | consider A. plana to be most similar in appearance to A. gaudichaudi. In turn, these two species are perhaps most similar to A. peroni. In all three species the shell whorl that expands rapidly in width is the fourth (Figs. 6C,D,E). All three species also have Type b opercula (Table 1). The operculum of A. plana is unique, how- ever, in that it has a spinose gyre (Fig. 9B). Further, the Type a eyes distinguish A. plana from A. gaudichaudi and A. peroni (Type b eyes), and the whorl sculpture (two weakly developed spiral lines) in A. plana is lacking in the other two species. The violet suture pig- mentation of the spire in A. gaudichaudi dis- tinguishes this species from A. peroni, which has clear to light pink sutures. Richter reported both A. gaudichaudi and A. plana from the Indian Ocean. Newman (pers. comm.) has recorded both species in waters off Heron and Lizard islands, Austra- lia, and has indicated that A. gaudichaudi is the most common species of atlantid. It is therefore surprising that | have never identi- fied A. gaudichaudi from Hawaiian waters, al- though | have routinely checked the eye type and, periodically, the operculum of specimens identified as A. plana. Atlanta echinogyra Richter, 1972 (Figs. 3C-D, 5E, 6F, 8E-H, 9C,D) Material: A total of 47 specimens was ex- amined (Table 2), which ranged from larvae (less than 0.7 mm) to a 1.7 mm adult. Four | specimens, ranging from 1.1 to 1.7 mm, were | examined under the SEM. Species characterization: The spire of this small species forms a low cone that can be slightly tilted relative to the shell plane (Fig. 8F,H). The shell whorl that expands rapidly is | HAWAIIAN ATLANTIDAE 121 \ \ E FIG. 8. Scanning electron micrographs of Atlanta plana (A-D) and A. echinogyra (E-H). Views and scale bars as in Fig. 4. 122 SEAPY > fl = = E 1 Jus mí do alt a Aa zu. ъ 3 ELA MS FIG. 9. Photographs of operculum and spiral portion (gyre) of operculum in Atlanta plana (A,B), A. echin- ogyra (C,D), A. turriculata (E,F). Scale bars are 0.1 mm. the fourth (Fig. 6F). The second, third and about half of the fourth whorl bear prominent spiral ridges and secondary sculpture (Fig. 8G,H). The shell spire is a uniform reddish- brown, whereas the remaining whorls of the shell and keel are clear (Fig. 5E). The eyes are Type a, and the operculum is Type c. The opercular gyre is elevated and bears about 12 broad-based spines (Fig. 9C,D). Discussion: This species is immediately recognized in fresh material by the moder- ately elevated, reddish-brown shell spire. The characteristic spire sculpture is also clear un- der the high magnification of a dissection mi- croscope. The elevated opercular gyre with the broad-based spines is also unique to this species. When the operculum is mounted on | a slide (for viewing beneath a compound mi- croscope), the tips of the spines bend under the pressure of the cover slip, causing them to have the hook-like appearance seen in Figure 9C,D. | | have collected А. echinogyra infrequently | and in comparatively low numbers from Ha- | waiian waters (Table 2). Richter (1974), how- ever, reported this species to be abundant in | the western Indian Ocean. Richter (1987) also recorded a larger maximum shell size HAWAIIAN ATLANTIDAE (2.5 mm) for A. echinogyra than | obtained from Hawaiian waters (1.7 mm). Atlanta fusca Souleyet, 1852 (Figs. 6G, 10A-D) Material: A total of 57 specimens was ex- amined (Table 2), which ranged from larvae (less than 0.6 mm) to a 1.9 mm adult. Four specimens, ranging from 1.0 to 1.6 mm, were examined under the SEM. Species characterization: The shell spire forms a strongly elevated cone (Fig. 10B,D) The spire whorls are sculptured by a complex pattern of ornamentation (Fig. 10C,D). A prominent spiral ridge is located along the outer margin of the spire whorls (Fig. 10C,D). This ridge is low on the second shell whorl and progressively increases in height to a maximum on the fourth and fifth whorls. The complex spire ornamentation ends on the lar- val shell and is replaced by rows of small punctae on the adult shell (Fig. 10A,C). The keel is tall and rounded (Fig. 10A). In animals larger than about 1.5 mm, such as the animal used in Fig. 10A-D, the keel inserts between the fifth and sixth shell whorls. The shell is yellowish-brown (amber) to brown. The eyes are Type a and the operculum is Type a. Discussion: The largest specimen of A. fusca collected in the present study ap- proaches the maximal size of 2 mm reported by Richter (1974) for this species from the Indian Ocean. Van der Spoel (1976) indicated an upper size limit of 4 mm, however. This species is distinguished by its conspic- uous brown to yellowish-brown color and by its tall, conical spire. The species that is most similar in appearance to A. fusca is A. turricu- lata (see below). Atlanta turriculata d'Orbigny, 1836 (Figs. 5C, 9E-F, 10E-H) Material: A total of 1,085 specimens was examined (Table 2), which ranged from larvae (less than 0.6 mm) to a 1.7 mm adult. Six specimens, ranging from 1.0 to 1.6 mm, were examined under the SEM. Species characterization: The shell spire protrudes laterally from the right side of the Shell as an elongate ‘turret’ (Fig 10F), formed by the strongly elevated second and third whorls capped by the protoconch (Fig. 10H). When the shell is viewed at right angles to the Shell plane (Fig. 10G), a prominent spiral 123 ridge is evident along the periphery of the spire whorls. When oriented in the plane of the shell (Fig. 10H), however, this spiral ridge is seen to be situated in the middle of the second and third whorls. The spiral ridge also increases in height to a maximum on the fourth and fifth whorls (Fig. 10H). The light reddish-brown color of the shell spire grades into a clear outer shell whorl and keel (Fig. 5C). The keel is well developed and rounded in lateral profile (Fig. 10E). The eyes are Type a, the operculum is Type a. The operculum is unique in having two parallel rows of numer- ous short spines that spiral outward from the gyre center (Fig. 9E,F). Discussion: The strongly turreted, light red- dish-brown shell spire and the spinose oper- culum immediately distinguish A. turriculata from the other species of atlantids. The spe- cies of atlantid that is most similar to A. tur- riculata in appearance is A. fusca. Both spe- cies are small (maximal size of 2.0 mm or less in Hawaiian waters), have pigmented spires, have an elevated ridge in the same position on the spire whorls and have Type a eyes and Type a opercula. Atlanta inflata Souleyet, 1852 (Figs. 5F, 61, 11A-D) Material: A total of 1,052 specimens was examined (Table 2), which ranged from larvae (less than 0.6 mm) to 1.5 mm adults. Twenty- eight specimens, ranging from 0.9 to 1.4 mm, were examined under the SEM. Species characterization: The shell of this small species is laterally inflated (shell width is about 40% of shell diameter). The spire is relatively flat (Fig. 11B,D). The shell whorl that increases rapidly in width is the fifth (Fig. 61). The spire whorls and sutures are weakly defined owing to the presence of thick, evenly spaced spiral ridges (Fig. 11A,C). The keel is tall (Fig. 11A) and its anterior margin is trun- cate in undamaged specimens (not shown by the specimen used in Figure 11A-D, but illus- trated clearly in Figure 4 of Richter, 1974). The digestive gland, contained within the shell spire, is mottled reddish-brown to yel- lowish-brown (Fig. 5F). The eyes are Type a, the operculum is Type c. Discussion: A second color morph of A. in- flata was common in the Hawaiian fauna. It was immediately distinguished in fresh and recently preserved specimens by a uniform violet to light purple color of the spire. This appears only to be a color variant, however, FIG. 10. Scanning electron micrographs of Atlanta fusca (A-D) and A. turriculata (E-H). Views and scale bars as in Fig. 4. HAWAIIAN ATLANTIDAE FIG. 11. Scanning electron micrographs of Atlanta inflata (A-D) and A. helicinoides (E-H bars as in Fig. 4. ). Views and scale 126 because eye and opercular morphologies were indistinguishable from those of typical A. inflata, as were the shells when viewed under the SEM. Like Richter (1987), | have observed con- siderable variability in the presence and de- gree of expression of the spiral ridges on the whorls of the shell spire. In the majority of the individuals that | examined under the SEM, however, the spiral ridges were well devel- oped. The shell spire of A. inflata is very sim- ilar in appearance to that of A. helicinoides, and these two species can be easily confused unless other taxonomic characters are used (discussed below). Atlanta helicinoides Souleyet, 1852 (Figs. 1C, 2C, 6J, 11E-H) Material: A total of 173 specimens was ex- amined (Table 2), which ranged from larvae (less than about 0.7 mm) to a 2.0 mm adult. Twelve specimens, ranging from 1.1 to 1.9 mm, were examined under the SEM. Species characterization: The shell of this small species is laterally inflated (shell width is about 40% of the shell diameter). The spire is slightly elevated (Fig. 11H). The shell whorl that increases rapidly in width is the fifth (Fig. 6J). The second through fourth whorls have evenly spaced, thin spiral ridges (Fig. 11G). Because the spiral ridges are relatively nar- row, the sutures can be clearly distinguished, particularly under a dissection microscope. On the fifth whorl the spiral ridges break down and are replaced by rows of low, small punc- tae (Fig. 11G). The keel is rounded and mod- erately tall in undamaged specimens. The eyes are Туре с and the operculum 1$ Туре с. Discussion: In the Hawaiian fauna two dis- tinct color morphs of A. helicinoides were en- countered in approximately equal propor- tions; а light yellow-tan form and а light purple-pink form. | could not see any struc- tural differences in eye, opercular or shell morphologies that would justify their taxo- nomic separation, however. Referring to A. helicinoides, Tesch (1949: 19) stated, “This species is at first sight so extremely like the preceding one (A. inflata) that it requires considerable attention to dis- tinguish them.” Richter (1987) also noted the strong similarities of the two species, particu- larly in the appearance of the shell spire. In SEM photographs (compare Figs. 11A, 116), the gross morphologies of the shells can be seen to be nearly identical. The spires are SEAPY relatively flat and about the same size, and the number and spacing of the spiral ridges on the spire whorls are the same (compare Figs. 11C, 11G). Further, both species are small and the shells are laterally inflated. The only obvious differences between the shells of the two species are, first, the spiral ridges on the spire whorls are thinner and less prom- inent in A. helicinoides than in A. inflata, with the result that the whorls comprising the spire are more clearly defined in A. helicinoides, and, second, the keel of A. helicinoides is somewhat low and rounded, whereas that of A. inflata is tall and truncate along the anterior edge. The two species can be immediately separated on the basis of their eyes, how- ever, which are Type c in A. helicinoides and Type b in A. inflata. Atlanta tokiokai van der Spoel & Troost, 1972 (Figs. 5D, 6K, 12A-D) Material: A total of 25 specimens was ex- amined (Table 2), which ranged from larvae (less than about 0.8 mm) to a 2.6 mm adult. Four specimens, ranging from 1.2 to 2.4 mm, were examined under the SEM. Species characterization: The shell spire is tilted (or inclined) relative to the shell plane (Fig. 12A). The spire is globose in side view (Fig. 12B,D), forming an apical angle of about 80°. Spirally arranged rows of small, low punctae are present on the spire (Fig. 12D). The punctae become more prominent on the last whorls of the spire. The shell whorl that increases rapidly in width is the sixth (Fig. 6K). The shell is a light yellow-tan color (Fig. 5D). The keel is tall and rounded (Fig. 12A). The eyes are Type b, and the operculum is Type c. Discussion: Specimens of A. tokiokai col- lected from Hawaiian waters were small; the largest individual measured only 2.6 mm. This maximal size is close to that (2.8 mm) re- — ported by Richter (1990). Prior to Richter's 1990 revision of the group of Atlanta species having tilted spires, he | (1974) and, subsequently, | (1990a, 1990b) | had identified this species as A. inclinata Soul- eyet, 1852. Among the atlantids from Hawai- ian waters, this and the next species, A. me- — teori, are the only two species belonging to | the group of four species having tilted spires. | Features that distinguish A. tokiokai from A. | meteori are given below under the latter spe- cies. The species that is most similar to Atlanta HAWAIIAN ATLANTIDAE 127. FIG. 12. Scanning electron micrographs of Atlanta tokiokai (A-D) and A. meteori (E-H). Views and scale bars as in Fig. 4. 128 SEAPY tokiokai is A. inclinata (Richter, 1990). Both species have a globose spire, with an apical angle of about 80°. However, the spire of A. inclinata consists of four whorls, while that of A. tokiokai is comprised of five whorls. In A. inclinata the last shell whorl is colorless and the spire is a weak rose color, whereas the entire shell of А. tokioka/ is a light yellow-tan. When viewed with the SEM, the prominent spiral rows of punctae on the spire whorls of A. tokiokai are greatly reduced or lacking on A. inclinata, with the result that the shell sur- face is essentially smooth. However, when viewed with the light microscope, the spire whorls of A. inclinata show fine radial mark- ings, which are due to the internal shell struc- ture. Lastly, A. inclinata attains a larger size (to 6 mm) than A. tokiokai (2.8 mm). Atlanta meteori Richter, 1972 (Figs. 1B, 6L, 12E-H) Material: A total of 338 specimens was ex- amined (Table 2), which ranged from larvae (less than about 0.7 mm) to a 3.7 mm adult. Nine specimens, ranging from 1.2 to 2.8 mm, were examined under the SEM. Species characterization: The shell spire is tall and strongly tilted (Fig. 12E). Viewed in the plane of the shell (Fig. 12F), the spire is conical and steep sided, with an apical angle of about 70°. The spire whorls are smooth and relatively flat, and are separated by very shal- low sutures that are difficult to resolve under the SEM (Fig. 12G,H). The shell whorl that increases rapidly in width is the sixth (Fig. 6L). The prominent keel is rounded in lateral pro- file, except at the anterior edge, where it is truncate (Fig. 12E). The eyes are Type b, the operculum is Type b. Discussion: In live material A. meteori is the clearest and most glass-like of the Hawaiian atlantids. Richter (1972, 1974) also com- mented upon this feature in A. meteori from the Indian Ocean. Atlanta meteori is most similar to A. gibbosa (Richter, 1990). Both species are clear and glass-like, but the spire of A. gibbosa forms a pointed cone (apical angle of about 85°), and the spire whorls are rounded with incised and distinct sutures. The umbilicus is conspicuously wider in A. gib- bosa than in A. meteori. As indicated above, the only two species in the Hawaiian fauna with distinctly tilted spires are A. meteori and A. tokiokai. In the former species the shell is clear, whereas in the latter species it is light yellowish-tan. Further, the spire of the former species forms a tall cone (about a 70° apical angle) and has smooth whorls, whereas that of the latter species is lower, globose (about an 80° apical angle) and is ornamented by spiral rows of numer- ous, small punctae. The opercula are also dif- ferent; Type b in A. meteori and Type c in A. tokiokal. CONCLUSIONS The atlantid fauna of Hawaiian waters is highly diverse, and includes 13 of the 16 spe- cies reported by Richter (1974) from the ex- tensive plankton sampling program of the Me- teor Expedition to the Indian Ocean. The number of worldwide species in the genus At- lanta is at least twice as many as the eight species recognized by Tesch in 1949. The total of 16 species does not include two spe- cies described since 1949 (A. peresi and A. pacifica), which were characterized in the tax- onomic review of van der Spoel (1976). Nei- ther species was reported from the Indian Ocean by Richter (1974) or from the central Pacific Ocean in the present study. In his study on atlantid opercula, Tokioka (1961) concluded that A. pacifica was not a valid species. The validity of these two species re- mains uncertain and confirming studies are needed. KEY TO HAWAIIAN ATLANTIDAE 1. a. Spire whorls involute, projecting spire lacking from right side of shell; adult shell and keel of conchiolin . . . Oxygyrus keraudreni (Fig. 3E-H) b. Spire projects laterally, to varying degrees, from the right side of the shell; adult shell calcareous; keel calcareous or of conchiolin ..... 2 2. a. Keel of conchiolin and transparent . . . Protatlanta souleyeti (Fig. 4A-D) b. Keel calcareous and translucent eae (genus Atlanta) 3. a. Shell whorl that increases rapidly in width. is the third 2." 4 b. Shell whorl that increases rapidly in width is the fourth, fifth or sixth ..5 4. a. Eyes Type b; shell and keel base unpigmented, although inner whorls can become light pink in older specimens; keel tall with anterior edge truncated... . A. lesueuri (Fig. 8A-D) 10. HAWAIIAN ATLANTIDAE 129 . Eyes Type a; shell unpigmented except spire whorls (faint violet) and sutures (light violet); keel moderately elevated and rounded . . A. oligogyra (Fig. 8E-H) . Shell whorl that rapidly increases in width is the fourth or fifth; axis of spire not inclined relative to the shell PIANO ees SRE cor à ELU 6 . Shell whorl that rapidly increases in width is the sixth; axis of spire inclined relative to the shell аи Moe ETRE 12 . Shell whorl that rapidly increases in Widths the fourth... 2.2... 002... 7 . Shell whorl that rapidly increases in Wich Satine: tikes ame ee een 2 . Spire whorls smooth, lacking spiral sculpture; spire slightly rounded; sutures of spire whorls unpigmented or light pink; eyes Type b . ..... A. peroni (Fig. 4E-H) . Spire whorls with weak to well-developed spiral ridges; spire forms a low cone; spire whorls clear with violet sutures or reddish-brown; ES LEER 8 . Spire weakly conical; second and third spire whorls with two weakly expressed spiral ridges and violet sutures; gyre of Type b operculum with about 20 narrow, projecting spines (Fig. 11B) . ... A. plana (Fig. 10A-D) . Spire forms a low cone; spire red- dish-brown, with well-developed spiral ridges and secondary sculpture on the second through fourth whorls; gyre of Type c operculum elevated, with about 12 broad-based, thick projecting spines (Fig. 11D) ...А. echinogyra (Fig. 10E-H) . Spire projects conspicuously as a high cone or a turret. ........ 10 . Spire flattened, not conical ог WUE Ste ERREUR 11 . Spire forms a high cone (spire angle about 65-75”); shell distinctive yel- lowish-brown (or amber) color; gyre of operculum lacking ornamenta- HONS: PR. A. fusca (Fig. 13A-D) . Spire turreted and steep-sided (spire angle about 35-45°); shell (especially the spire) light reddish-brown; gyre of operculum with double row of short, projecting spines (Fig. 11F) о А. turriculata (Fig. 13E-H) 11. a. Eyes Type a; spire with prominent spiral ridges on whorls; sutures separating second from third whorls and third from fourth whorls difficult to distinguish; keel tall, with anterior edge truncated .. ...... A. inflata (Fig. 12A-D) b. Eyes Type c; spire with weakly developed spiral ridges on whorls; sutures separating second from third whorls and third from fourth whorls distinct; keel moderately low and rounded in profile . . . A. helicinoides (Fig. 12E-H) 12. a. Shell light yellow-tan color; spire globular and moderately _ inclined relative to the shell plane; surface of spire whorls with numerous, small and regularly spaced spiral rows of punctae that are most strongly developed on the fourth and fifth whorls; operculum Туре с. ..... A. tokiokai (Fig. 9A-D) b. Shell clear and glass-like; spire tall, conical and steeply inclined relative to the shell plane; surface of whorls smooth, lacking punctate sculpture; operculum Type b ..... A. meteori (Fig. 9E-H) ACKNOWLEDGMENTS The support provided by the officers, crew and members of the scientific party during cruises of the R/V KANA KEOKI and R/V KILA, University of Hawaii, are gratefully ac- knowledged. | am especially indebted to Richard Young of the University of Hawaii for his collaboration and assistance in the collec- tion of the samples on which this study was based. For the loan of the Bongo nets used during two of the cruises, | thank Jed Hirota. My deep gratitude is extended to Steven Karl for operation of the SEM, critical-point prepa- ration of specimens, photography and print- ing. Specimens of Atlanta gaudichaudi were graciously provided by Leslie Newman. To Gotthard Richter | am most appreciative for the verification of my species identifications. Critical reviews of the manuscript were pro- vided by Richard Young, Leslie Newman and an anonymous reviewer. This study was sup- ported by National Science Foundation Grant OCE-8500593. 130 SEAPY LITERATURE CITED BATTEN, В. L. & M. P. DUMONT, 1976, Shell ul- trastructure of the Atlantidae (Heteropoda, Meso- gastropoda) Oxygyrus and Protatlanta, with com- ments on Atlanta inclinata. Bulletin of the American Museum of Natural History, 157:263— 310. FRONTIER, S., 1966, Notes morphologiques sur les Atlanta recoltees dans le plancton de Nosy Ве (Madagascar). Cahiers Office de la Re- cherche Scientifique et Technique Outre-Mer, Serie Océanographie, 4:131-139. HYMAN, L. H., 1967, The invertebrates. Volume VI. Mollusca I. McGraw-Hill, New York, 792 р. RICHTER, G., 1961, Die Radula der Atlantiden (Heteropoda, Prosobranchia) und ihre Bedeu- tung fur die Systematik und Evolution der Fami- lie. Zeitschrift fur Morphologie und Okologie der Tiere, 50:163-238. RICHTER, G., 1972, Zur Kenntnis der Gattung At- lanta (Heteropoda: Atlantidae). Archiv fur Mol- luskenkunde, 102:85-91. RICHTER, G., 1974, Die Heteropoden der “Ме- teor”-Expedition in den Indischen Ozean, 1964/ 65. “Meteor” Forschung-Ergebnisse, (D), 17:55— 78. RICHTER, G., 1982, Mageninhaltsuntersuchungen an Oxygyrus keraudreni (Lesueur) (Atlantidae, Heteropoda). Beispiel einer Nahrungskette im tropischen Pelagial. Senckenbergiana Maritima, 14:47-77. RICHTER, G., 1986, Zur Kenntnis der Gattung At- lanta (Il). Atlanta lesueuri Souleyet und Atlanta oligogyra Tesch. Archiv für Molluskenkunde, 117:19-31. RICHTER, G., 1987, Zur Kenntnis der Gattung Atlanta (Ш). Atlanta inflata, A. helicinoides, А. echinogyra und A. plana (Prosobranchia: Het- eropoda). Archiv für Molluskenkunde, 117:177- 201. RICHTER, G., 1990, Zur Kenntnis der Gattung At- lanta (IV). Die Atlanta inclinata-Gruppe (Proso- branchia: Heteropoda). Archiv für Mollusken- kunde, 119:259-275. SEAPY, R. R., 1990a, Patterns of vertical distribu- tion in epipelagic heteropod molluscs off Hawaii. Marine Ecology Progress Series, 60:235-246. SEAPY, R. R., 1990b, Sampling requirements for epipelagic heteropod molluscs. American Mala- cological Bulletin, 8:45—32. TESCH, J. J., 1949, Heteropoda. Dana-Report, 34: 54 pp., 5 pl. THIRIOT-QUIEVREUX, C., 1973, Heteropoda. Oceanography and Marine Biology, Annual Re- view, 11:237-261. TOKIOKA, T., 1961, The structure of the operculum of the species of Atlantidae (Gastropoda: Het- eropoda) as a taxonomic criterion, with records of some pelagic molluscs in the North Pacific. Pub- lications of Seto Marine Biological Laboratory, 9: 267-332. VAN DER SPOEL, S., 1972, Notes on the iden- tification and speciation of Heteropoda (Gas- tropoda). Zoologische Mededelingen Rijksmu- seum van Natuurlijke Historie te Leiden, 47: 545—560. VAN DER SPOEL, S., 1976, Pseudothecosomata, Gymnosomata and Heteropoda (Gastropoda). Bohn, Scheltema & Holkema, Utrecht, 484 p. Revised Ms. accepted 2 January 1990 MALACOLOGIA, 1990, 32(1): 131-145 ON THE VARIOUS EDITIONS OF TETSUAKI KIRA’S “COLOURED ILLUSTRATIONS OF THE SHELLS OF JAPAN” AND “SHELLS OF THE WESTERN PACIFIC IN COLOR VOL. 1,” WITH AN ANNOTATED LIST OF NEW NAMES INTRODUCED Rüdiger Bieler' & Richard Е. Petit” ABSTRACT At least 37 printings of Tetsuaki Kira’s “Coloured Illustrations of the Shells of Japan” (CISJ) and nine of its English-language version, “Shells of the Western Pacific in Color Vol. |” (SWPC), published between 1954 and 1989, are in existence. Some of the editions, often incorrectly dated on the title page, differ greatly in text and illustrations. They are of taxonomic importance as they contain descriptions of new taxa and so-called “manuscript names,” spanning 30 mol- luscan families. Of the 54 species-group and one genus-group names in question, five had been introduced before Kira's work, two are not available for taxonomic purposes, and eight were subsequently introduced by other authors after Kira had listed them as nude names only. The remaining 40 species-group names, only five of which were designated as new taxa, were made available with this work. The majority, 34 names, date from Kira (1959, CISJ), two from Kira (September 1954, CISJ), two from Kira (1960, CISJ), one from Kira (1962, SWPC), and one from Kira & Habe in Kira (1962, SWPC). New taxa and “manuscript names” are traced through the various editions, and annotated lists of the printings and of the nominal taxa are supplied. INTRODUCTION Tetsuaki Kira’s “Coloured Illustrations of the Shells of Japan,” first published in 1954, in Japanese, has become one of the standard reference works on Indo-Pacific mollusks. A revised edition in English, first published in 1962, is Known as “Shells of the Western Pa- cific in Color .” For convenience, they will hereafter be referred to as CISJ and SWPC, respectively. The work is of taxonomic interest as it contains the descriptions of at least 40 new species-group names. One new genus-group name appears, but is not validly introduced. However, the frequent use of manuscript names, the lack of dates given with the taxa, rampant misspellings, and the erratic use of parentheses around authors’ names, make use of the book extremely difficult and have resulted in many erroneous citations by subsequent authors. While working on such problems, we discovered that there are atleast 37 Japanese and nine English-language print- ings of this work, published between 1954 and 1989. Of the Japanese version, two editions are generally recognized, the original and the “enlarged & revised” edition, which was first published in 1959. We found, however, many of the so-called new printings to be revised editions. They were often newly typeset, and contained not only technical corrections and additions (such as indexes) but had major tax- Onomic changes in the figure captions, and figures were replaced or renumbered on some of the plates. Only five new species are clearly designated as such, but about 50 manuscript names, inconsistently assigned to various au- thors, appear in the different editions (there may be additional nude names or available descriptions of taxa wrongly assigned to other authors in this work that have escaped us). A further complicating fact is that the date on the English-language title page of the Japanese editions is often incorrect, as can be shown by the Japanese date (day, month and year of emperor Hirohito’s reign) in the colophon (in- scription at the end) of each copy. Some En- glish-language title pages were apparently used for a number of subsequent printings (1955,” for instance, still appears on the 1958 printing). Issues of CISJ and SWPC of the same year do not necessarily agree in taxo- nomic treatment, as the two were apparently independently revised and edited (Kira men- tions in the SWPC preface that “Dr. Habe took the trouble of revising the Latin names into the latest and authorized way of use”). The taxonomic mess created by author and publisher of this work proves the inappropri- ateness (1) of introducing manuscript names "Delaware Museum of Natural History. Current address: Field Museum of Natural History, Roosevelt Road at Lake Shore Drive, Chicago, Illinois 60605, U.S.A. P.O. Box 30, North Myrtle Beach, South Carolina 29582, U.S.A. 132 BIELER & PETIT into the literature, and (2) of describing new taxa in commercial book publications. LISTING OF NEW AND “MANUSCRIPT” NAMES (1) “Cantharidus kanekonis Oyama” (2) Gaza sericata Kira, 1959 (3) Pseudastralium henicus gloriosum Kira, 1959 (4) Galeoastraea millegranosa Kuroda & Habe in Habe, 1958 (5) Papyriscala bifasciata Kira & Habe in Kira, 1962 (6) Cirsotrema (Elegantiscala) kurodai Kira, 1960 (7) Canarium microurceum Kira, 1959 (8) Neverita (Glossaulax) hosoyai Kira, 1959 ) Simnia xanthochila Kuroda, 1928 ) Pustularia margarita tetsuakii Kira, 1959 ) Erosaria tomlini maturata Kira, 1959 ) Semicassis persimilis Kira, 1959 ) Bursa dunkeri Kira, 1959 ) ) ) — Eudolium inflatum Kuroda & Habe, 1952 Murex kiiensis Kira, 1959 Ceratostoma (Pteropurpura) vespertilio Kira, 1959 ) Coralliobia akibumii Kira, 1960 ) Coralliophila pyriformis Kira, 1959 ) Latiaxis kawamurai Kira, 1959 ) Babylonia pallida Kira, 1959 ) Neptunea fukueae Kira, 1959 ) Buccinum isaotakii Kira, 1959 ) Nassarius (Zeuxis) kiiensis Kira, 1959 ) Granulifusus kiranus Shuto, 1958 ) Fusinus gemmuliferus Kira, 1959 ) Fusinus crassiplicatus Kira, 1959 ) ) ) ) ) ) ) ) ) ae aaa ae DOAÁON00 Turrancilla apicalis Kira, 1959 Baryspira urasima Kira, 1959 Oliva hirasei Kuroda & Habe, 1952 Mitropifex hirasei Kira, 1962 Mitra (Cancilla) yagurai Kira, 1959 Ancistrosyrinx pulcherrissima Kira, 1959 Daphnella nobilis Kira, 1959 Chelyconus kinoshitai Kuroda, 1956 Asprella (Conasprella ?) ichinoseana Kuroda, 1956 (36) Euhadra roseoapicalis Kira, 1959 (37) Euhadra grata gratoides Kira, 1959 (38) Cadulus (Platyschides) novilunatus Kira, 1959 (39) Entalina majestica Kira, 1959 (40) Dentalium (Episiphon) candelatum Kira, 1959 (41) Dentalium (Pictodentalium) formosum hirasei Kira, 1959 VP@OD—-OOONDD O1 B © D — © © © Y e © © @ © À © D D D D D RD DD 22 (42) Genus-group name Pictodentalium (43) Acila schencki Habe, 1958 (44) Nuculana (Thestyleda) acinacea Habe, 1958 (45) Limopsis tajimae emphaticus Kira, 1959 (46) Fragum loochooanum Kira, 1959 (47) Clinocardium uchidai Habe, 1955 (48) Vasticardium compunctum Kira, 1959 (49) “Vasticardium serricostatum” (50) Leukoma japonica Kira, 1954 (51) Irus ishibashianus Kuroda 8 Habe, 1952 (52) Solecurtus dunkeri Kira, 1959 (53) Nuttallia solida Kira, 1953 (54) Heteromacoma oyamai Kira, 1954 (55) Lanceolaria oxyrhyncha cuspidata Kira, 1959 LISTING OF PRINTINGS AND REVISED EDITIONS Table 1 lists the various printings and edi- tions encountered by us. We were unable to examine in detail all of the printings for which we established printing dates. To properly date a copy, locate the bottom line of the date information in the colophon (e.g. “..35..6..5..”), and add 1925 to the first number which is the Year of the Showa Era; the second number is the month, and the third number is the day. This example translates to June 5th, 1960, which is the second printing of the second edition (the number of printing appears in kanji to the right of the last Arabic numeral; begin- ning with the tenth printing, the number of printing is shown in Arabic numerals). Table 1. List of printings and revised editions of Kira’s “Coloured Illustrations of the Shells of Japan” (CISJ) and “Shells of the Western Pacific’ (SWPC). Asterisks (*) mark those in which taxonomic names were first made avail- able. (a) Coloured Illustrations of the Shells of Japan All Japanese editions are cloth-bound oc- tavo volumes, with gold lettering in Japanese and a muricid-icon imprinted on the spine. The First Edition (before 1959) has a greenish cloth binding with photographs of three ranel- lid specimens on the front cover; the Second Edition has a blue binding featuring a Latiaxis photograph on the front cover. The dust cover has a small buccinid (Pusiostoma) photo- TETSUAKI KIRA’S ILLUSTRATIONS OF SHELLS 133 graph on the spine and a Spondylus photo- and Pleurotomaria shells, and in the Second graph in front; the cardboard slip case of the Edition photographs of an Architectonica and First Edition features photographs of Chlamys two Strombus shells. Printing Publication date Notes First Edition AU 1954a (September 5) L 2 1954b (November 1) 5 3 1955 (August 15) 9 4 1956 (June 1) 5 1957 (June 15) 4 6 1958 (May 1) > Second Edition | 1959 (March 10) © NO 2. 1960°(June 5) E 3 2 [not seen] 4 1961 (October 1) 5 Y [not seen] 6 1963 (February 5) 7-9 2 [not seen] 10 1965 (August 1) 2 111 1966 (August 1) 12 ? [not seen] 13 1968 (May 1) 14-15 р [not seen] 16 1971 (March 1) 2 7 ? [not seen] 18 1972 (October 1) 19 ? [not seen] 20 1974 (July 1) [not seen] 21-24 2% [not seen] 25 1979 (July 1) 26 ? [not seen] 27 1981 (April 1) 28-30 fy [not seen] 31 1989 (February 1) Notes: Contents (1954a): Japanese title page; [8 pp.] preface and introduction, dated August 1954; [1 p.] schematic drawings; рр. 1-135 figure captions [p. 1 = series title page], including 67 pls.; [p. 136 blank]; pp. 137-172 discussion of plates in Japanese, with black-and-white drawings (incl. description of two new taxa); pp. 1—4 index of family names in Latin and Japanese; pp. 5—24 index of figured taxa in Japanese. Apparently due to misnumbering, neither this nor any other printing of the first edition contains pages 41, 42, or 105, 106. 21954b. Changes from preceding (1954a): Correction of many printer's errors, correction of gender in Latin species names, re-identifications, change of genus-group names as well as authorships (affecting most plates); renumbering of figures (pls. 9, 29, 55, 65, 66); correction of transposed figure legends (pls. 27, 37); change of family names (pls. 23, 39); replacement of two figures by photographs of different specimens (Oliva emicator, Oliva erythrostoma; pl. 31 figs. 10, 14); change and introduction of manuscript names; slight changes in text and indexes reflecting changes in plates. STitle page design changed and title given in English for the first time. The Japanese title did not change, but the translation of the title of the first two printings was sometimes rendered as “Illustrations of Japanese Shells in Natural Colour” when cited by Japanese authors. Other changes from preceding printings: consecutive page numbering (pp. [8], 1-204), new index of generic names in Latin (рр. 177-184); very few corrections/changes in figure captions, most differences due to printer's error. 4Changes from 1955 (1956 not examined): minor correction in text (p. 36, Sulcerato); background color of plates changed from light-blue to gray or black (pl. 40). “Changes from preceding (1957): Minor technical adjustments (such as color of pl. 64). ®Japanese/English title page now stating “Enlarged & Revised Edition.” Contents: [4 pp.] + [1 р. new foreword in Japa- nese]; i-vii introduction in Japanese and index of family names in Japanese and Latin; [2 pp.] schematic drawings; рр. 1—195 figure captions, descriptions in Japanese (including black-and-white photographs and line drawings) plus 1 unnum- bered (rare cowries) and 71 numbered pls.; pp. 196-210, introduction to shell collecting (including line drawings and 134 BIELER & PETIT black-and-white photographs); pp. 211-218 index of generic names in Latin; pp. 219-239 index of figured taxa in Japanese + [241] colophon. Major changes from preceding (1958): Figure captions now containing descriptions; 5 additional color plates (1 unnum- bered, pls. 68—71); black-and-white photographs and line drawings in text; many re-identifications and new printer's errors; use of additional family names (e.g. Stomatiidae, p. 16, pl. 8); plates renumbered (pls. 16, 50); and many replacements of photographs in plates (pl. 4: Tugali gigas; pl. 7: Monodonta perplexa, M. neritoides; pl. 11: Clython sowerbyanus; pl. 12: Siliquaria cumingi, Serpulorbis imbricatus; pl. 14: Xenophora corrugata; pl. 15: Tibia fusus; pl. 20: Erronea hirasei replaced by E. caurica; pl. 21: Cassis cornuta; pl. 30: Baryspira urasima, Oliva emicator, O. erythrostoma; pl. 50: Spondylus cruentus, addition of Spondylus sanguineus; pl. 55: Tridacna squamosa; pl. 57: Sunetta concinna). "Changes from preceding (1959): re-identifications, frequently on the generic level, and corrections of typographic errors for most plates. “Figures 5-16 on plate 8 have been renumbered to accommodate Stomatia rubra in the Stomatiidae. “This is the first printing that we have seen which gives dates (years only) of previous printings on the verso of the title page. К is also the first printing seen which has “<>" added to the title. (b) Shells of the Western Pacific in Color All English-language editions are larger (quarto) cloth-bound volumes, with gold let- tering in English and a Latiaxis-icon imprinted on the front cover. The dust cover features color photographs of various gastropod and scaphopod shells. An odd feature of < >, in contrast to the later <> by Habe not covered here, is that the odd-num- bered pages are on the left instead of the right. In contrast to the many different Japanese versions of this work, the English-language “editions” do not differ from each other, with the exception of minor technical details (Such as the loss of figure-number 16 on plate 12 after 1962, probably due to printer’s error). Printing Publication date Notes First Edition ae yal 1962 (September) 2 1965 (November 1) 1 Second (or “Revised”) Edition — 1965 (October) [not seen]? Eu 1966 [not seen]? — 1967 $ — 1968 3 — 1970 Third (or “Second”) Edition a 1972 (May) 8 — 1975 2 Notes: "Inscribed “2nd printing, 1965” with copyright date of 1962. “The Revised Edition copyright date is October 1965. “From dates of printing listed in 1968 printing. “Stated to be “Third Edition January 1967,” but it bears only the 1962 copyright date and not the copyright date of the Second Edition. As the copyright date for a “Third Edition” is later given as “May 1972,” this is believed to be an error for “Third Printing,” but we have no explanation for the 1962 copyright date. This is the first printing seen which has “<>" appended to the title. ©The 1972 printing is referred to as the “Third Edition” on the verso of the title page, whereas the 1970 and earlier printings show “Revised Edition.” “The 1975 printing is again referred to as the “Second Edition” on the verso of the title page. Neither the new copyright date (1965), nor the term “Revised Edition” are understood by us, aS the 1962 and 1968 printings we have examined differ only in the 1968 (and later) being styled “<>,” but the 1967 printing still omits this addition to the title. TETSUAKI KIRA’S ILLUSTRATIONS OF SHELLS 135 ANNOTATED LISTING OF NEW TAXA AND “MANUSCRIPT NAMES” List of names that were recognized as ei- ther of Kira’s ог as “manuscript names” т Kira’s work, following Kira’s arrangement of molluscan families.? Such names were traced through the print- ings and editions available to us. If published elsewhere, the proper citation of the original description is given in brackets. Printings in which the new names were first made avail- able are indicated by asterisks (*). It should be noted that the listing is not a synonymy but reflects a chronological order of figure cap- tions. In cases where the first two printings of CISJ differ, they are marked as “1954a”-or “1954b.” GASTROPODA Trochidae (1) “Cantharidus kanekonis Oyama” [nomen nudum) 1954-1958 (CISJ): Cantharidus kanekonis Oyama, MS.; р. 15, pl. 7, fig. 5 [nom. nud.]. 1959 (CISJ): Cantharidus yokohamensis (Bock); PAIS РЁ И, MIG. 5. 1960-1989 (CISJ): Cantharidus (Kanekotro- chus) infuscatus (Gould); p. 13, pl. 7, fig. 5. 1962-1968 (SWPC): Cantharidus (Kanekotro- chus) infuscatus (Gould); p. 10, pl. 8, fig. 5. Taxonomic note: Apparently the name was never made available. (2) Gaza sericata Kira, 1959 1954-1958 (CISJ): Gaza sericata Kuroda, MS.; р. 16, pl. 8, fig. 13 [пот. nud.]. *1959 (CISJ): Gaza sericata Kuroda, MS.; р. 17, pl. 8, fig. 13 [with short description in Japa- nese]. 1960-1963 (CISJ): Gaza sericata Kira; р. 17, pl. 8, fig. 13. 1962-1968 (SWPC): Gaza sericata Kira; p. 14, pl. 9, fig. 12. 1965-1989 (CISJ): Gaza sericata Kira; р. 17, pl. 8, fig. 12. Turbinidae (3) Pseudastralium henicus gloriosum Kira, 1959 1954a (CISJ): Pseudastralium henicus gloriosa Kuroda et Habe, MS.; p. 20, pl. 10, fig. 2 [nom. nud.]. 1954b-1958 (CISJ): Pseudastralium henicus gloriosum Kuroda et Habe, MS.; p. 20, pl. 10, fig. 2 [nom. nud.]. *1959 (CISJ): Pseudastralium henicus gloriosum Kuroda et Habe, MS.; p. 19, pl. 10, fig. 2 [with short description in Japanese]. 1960-1961 (CISJ): Guildfor or dia [sic] (Pseu- dastralium) gloriosa Kira; p. 19, pl. 10, fig. 2. 1963 (CISJ): Guildforordia [sic] henicus glorio- sum Kira; p. 19, pl. 10, fig. 2. 1962-1968 (SWPC): Pseudastralium henicus gloriosum (Kira); p. 18, pl. 11, fig. 2. 1965-1989 (CISJ): Pseudastralium henicus glo- riosum (Kira); p. 19, pl. 10, fig. 2. (4) Galeoastraea millegranosa Kuroda & Habe in Habe, 1958 [1958a, Venus, 20(1): 45, pIASe 19. +] 1954-1958 (CISJ): Bolma ? millegranosa Kuroda et Habe, MS.; р. 20, pl. 10, fig. 3 [nom. nud.]. 1959 (CISJ): Bolma ? millegranosa Kuroda & Habe, MS. [sic]; p. 20, pl. 10, fig. 3. 1960-1963 (CISJ): Galeoastraea (Harisazaea) millegranosa Habe [sic]; p. 20, pl. 10, fig. 3. 1962-1968 (SWPC): Galeostraea [sic] millegra- nosa Habe [sic]; p. 18, pl. 11, fig. 3. 1965-1989 (CISJ): Galeoastraea millegranosa Habe [sic]; p. 20, pl. 10, fig. 3. Epitoniidae (5) Papyriscala bifasciata Kira & Habe in Kira, 1962 1954а (CISJ): Epitonium (Papyriscala) hali- mense Makiyama; p. 27, pl. 13, fig. 16. 1954b-1958 (CISJ): Epitonium (Papyriscala) sp.; р. 27, р! 13, ПО. WG: 1959-1963 (CISJ): Ерйотит (Papyriscala) sp.; р. 31, pl. 13; fig: 16. “1962 (SWPC): Papyriscala bifasciata Kira et Habe (n. sp.); p. 30, pl. 14, fig. 16. 1965—1968 (SWPC): Papyriscala bifasciata Kira et Habe (n. sp.) [sic]; p. 30, pl. 14, fig. 16. 1965-1989 (CISJ): Papyriscala bifasciata Kira et Habe; p. 31, pl. 13, fig. 16. Taxonomic note: Listed in synonymy of “Pa- pyriscala yokoyamai (Suzuki & Ichikawa, 1936)” by Kuroda et al. (1971: 257). Also listed this way by Inaba & Oyama (1977: 27), but authorship of P. yokoyamai is correctly given as “Suzuki & Ichimura, 1936.” °Kira’s collection is now located in the Osaka City Museum, Japan (Inaba & Oyama, 1977: 36). 136 BIELEER’&PETIT (6) Cirsotrema (Elegantiscala) kurodai Kira, 1960 1954-1958 (CISJ): Cirsotrema (Elegantiscala) Sp р. 27, pla 13) figs 17. 1959 (CISJ): Cirsotrema (Elegantiscala) sp.; p. 32, pl. 13, fig. 17. "1960 (CISJ): Cirsotrema (Elegantiscala) kurodai Kira; p. 32, pl. 13, fig. 17. 1961-1963 (CISJ): Cirsotrema (Elegantiscala) kurodai Kira; р. 32, pl. 13, fig. 17. 1962-1968 (SWPC): Cirsotrema (Elegantiscala) varicosum Kuroda; p. 30, pl. 14, fig. 17. 1965-1989 (CISJ): Cirsotrema (Elegantiscala) rugosum Kuroda et Ito; p. 32, pl. 13, fig. 17. Taxonomic note: In the original description of Cirsotrema (Elegantiscala) rugosum Kuroda & Ito, 1961, the authors list Cirsotrema (Elegan- tiscala) sp. of Kira in the synonymy. Hanshin Shell Club (1986: 100—101) does not mention Kira as one of those “persons who dedicated taxonomic names to Dr. T. Kuroda.” Strombidae (7) Canarium microurceum Kira, 1959 1954-1958 (CISJ): Canarium microurceum Kuroda, MS.; р. 31, pl. 15, fig. 5 [nom. nud.]. *1959 (CISJ): Canarium microurceum Kuroda, MS.; р. 35, pl. 15, fig. 5 [with short description in Japanese]. 1960-1989 (CISJ): Canarium microurceum Kira; р. 35, РЕ 15, fig’ 5: 1962-1968 (SWPC): Сапапит microurceum Kira; p. 34, pl. 16, fig. 5. Taxonomic note: Cited by Habe & Kosuge (1964a: 4) as of Kira (1958). Naticidae (8) Neverita (Glossaulax) hosoyai Kira, 1959 *1959 (CISJ): Neverita (Glossaulax) hosoyai Kuroda & Kira, MS.; p. 42 [with short descrip- tion in Japanese]. 1960-1989 (CISJ): Neverita (Glossaulax) ho- soyai Kira; p. 42. 1962-1968b (SWPC): Neverita (Glossaulax) ho- soyai Kira; p. 43. Taxonomic note: Listed as synonym of Glos- saulax didyma (Roding, 1798) by Majima (1987: 62). Amphiperatidae / Ovulidae [depending on printing] (9) Simnia xanthochila Kuroda, 1928 [Venus, 1(1): pl. 1, fig. 5; Venus, 1(3): 78 (1929)] 1954a (CISJ): Pellasimnia xanthochila Kuroda, MS. [sic]; p. 36, pl. 18, fig. 13. 1954b-1958 (CISJ): Pellasimnia hirasei xan- thochila (Kuroda); p. 36, pl. 18, fig. 13. 1959-1989 (CISJ): Pellasimnia hirasei xan- thochila (Kuroda); p. 44, pl. 18, fig. 13. 1962-1968 (SWPC): Pellasimnia hirasei xan- thochila (Kuroda); p. 45, pl. 19, fig. 13. Taxonomic note: Placed in genus Xandaro- vula Cate, 1973, by Cate (1973: 35) and Azuma (1976: 115). Cypraeidae (10) Pustularia margarita tetsuakii Kira, 1959 1954—1958 (CISJ): Pustularia margarita tetuakii [sic] Kuroda, MS.; p. 36, pl. 18, fig. 17 [nom. nud.]. “1959 (CISJ): Pustularia margarita tetsuakii Kuroda, MS.; p. 45, pl. 18, fig. 17 [with short description in Japanese]. 1960-1989 (CISJ): Pustularia margarita tetsuakii Kuroda [sic]; p. 45, pl. 18, fig. 17. 1962-1968 (SWPC): Pustularia margarita tet- suakii Kuroda [sic]; p. 46, pl. 19, fig. 17. Taxonomic note: Considered "Japanese- Hawaiian race” of Pustularia cicercula (Linné, 1758) by Cernohorsky (1967: 72). Listed as subspecies of Pustularia (Pustularia) globulus (Linné, 1758) by M. Schilder & F. A. Schilder (1971: 57). (11) Erosaria tomlini maturata Kira, 1959 1954-1958 (CISJ): Erosaria tomlini maturata Kuroda, MS.; р. 39, pl. 19, fig. 11 [nom. nud.). *1959 (CISJ): Erosaria tomlini maturata Kuroda, MS.; р. 47, pl. 19, fig. 11 [with short description in Japanese]. 1960-1963 (CISJ): Erosaria tomlini maturata Kira; p. 47, pl. 19, fig. 11. 1962-1968 (SWPC): Erosaria tomlini ogasawa- rensis Schilder; p. 48, pl. 20, fig. 11. 1965-1989 (CISJ): Erosaria tomlini ogasawaren- sis Schilder; p. 47, pl. 19, fig. 11. Taxonomic note: Listed in synonymy of Ero- saria tomlini ogasawarensis Schilder, 1944, by Kuroda et al. (1971: 105). Cassididae [Cassidae] (12) Semicassis persimilis Kira, 1959 1954a (CISJ): Semicassis persimile [sic] Kuroda, MS.; р. 43, pl. 21, fig. 3 [пот. nud.]. 1954b-1958 (CISJ): Semicassis persimilis Kuroda, MS.; р. 43, pl. 21, fig. 3 [nom. nud.]. *1959 (CISJ): Semicassis persimilis Kuroda, TETSUAKI KIRA’S ILLUSTRATIONS OF SHELLS 137 MS.; p. 52, pl. 21, fig. 3 [with short description in Japanese]. 1960-1963 (CISJ): Semicassis persimilis Kira; р. 52, pl. 21, fig. 3. 1962-1968 (SWPC): Semicassis persimilis Ku- roda [sic]; p. 54, pl. 22, fig. 3. 1965-1989 (CISJ): Semicassis persimilis Ku- roda [sic]; p. 52, pl. 21, fig. 3. Taxonomic note: Abbott (1968: 129) lists this as synonym of Phalium bisulcatum (Schubent 8 Wagner, 1829) and states “Kira's type of persimilis may be lost.” Bursidae (13) Bursa dunkeri Kira, 1959 1954-1958 (CISJ): Bursa dunkeri Kuroda, MS; р. 43, pl. 21, fig. 18 [пот. nud.]. “1959 (CISJ): Bursa dunkeri Kuroda, MS.; р. 54, pl. 21, fig. 18 [with short description in Japa- nese]. 1960-1989 (CISJ): Bursa dunkeri Kira; р. 54, pl. 21, fig. 18. 1962-1968 (SWPC): Bursa dunkeri Kira; p. 57, pl. 22, fig. 18. Taxonomic note: Listed as of Kira (1962) by Kuroda et al. (1971: 133). Tonnidae (14) Eudolium inflatum Kuroda & Habe, 1952 [Check List, p. 56] 1954а (CISJ): Eudolium lineatum Kuroda et Habe; p. 44, pl. 22, fig. 4. 1954b-1958 (CISJ): Eudolium lineatum inflatum Kuroda et Habe, MS. [sic]; p. 44, pl. 22, fig. 4. 1959-1960 (CISJ): Eudolium lineatum inflatum Kuroda et Habe, MS. [sic]; p. 55, pl. 22, fig. 4. 1963 (CISJ): Eudolium lineatum inflatum Kuroda et Habe; p. 55, pl. 22, fig. 4. 1962-1968 (SWPC): Eudolium inflatum Kuroda et Habe; p. 59, pl. 23, fig. 4. 1965-1989 (CISJ): Eudolium inflatum Kuroda et Habe; p. 55, pl. 22, fig. 4. inflatum Taxonomic note: Introduced by Kuroda & Habe (1952: 56) as anew name for Eudolium lineatum Schepman as figured by Osima (1943, Conch. Asiat. 1, pl. 5, fig. 1). As Osima’s figure is accompanied by a description, Ku- roda & Habe’s (1952) name can be accepted. Muricidae (15) Murex kiiensis Kira, 1959 1954-1958 (CISJ): Murex kiiensis Kuroda, MS.; р. 47, pl. 23, fig. 10 [nom. nud.]. *1959 (CISJ): Murex Kiiensis [sic] Kuroda, MS: p. 58, pl. 23, fig. 10 [with short description in Japanese]. 1960-1989 (CISJ): Murex kiiensis Kira; р. 58, pl. 23, 119710: 1962-1968 (SWPC): Murex kiiensis Kira; p. 63, pl. 24, fig. 10. Taxonomic note: Listed as of Kira (1962) by E. H. Vokes (1971: 62). (16) Ceratostoma (Pteropurpura) vespertilio Kira, 1959. 1954a (CISJ): Ceratostoma (Pteropurpura) ves- pertilis [sic] Kuroda, MS.; p. 48, pl. 24, fig. 10 [nom. nud.]. 1954b-1958 (CISJ): Ceratostoma (Pteropur- pura) vespertilio Kuroda, MS.; р. 48, pl. 24, fig. 10 [пот. nud.]. *1959 (CISJ): Ceratostoma (Pteropurpura) ves- pertilio Kuroda, MS.; p. 61, pl. 24, fig. 10 [with short description in Japanese]. 1960-1963 (CISJ): Ceratostoma (Pteropurpura) vespertilio Kira; p. 61, pl. 24, fig. 10. 1962-1968 (SWPC): Pteropurpura vespertilio Kira; p. 66, pl. 25, fig. 10. 1965-1989 (CISJ): Pteropurpura vespertilio (Kira); p. 61, pl. 24, fig. 10. Taxonomic note: Listed as of Kuroda in Kira (1955) by E. H. Vokes (1971: 115). Rapidae [Coralliophilidae] (17) Coralliobia akibumii Kira, 1960 1954a (CISJ): Coralliobia inflata (Dunker); p. 51, pl. 25, fig. 3. 1954b-1958 (CISJ): Coralliobia sp.; р. 51, pl. 25, ПО. 3. 1959 (CISJ): Coralliobia sp.; р. 63, pl. 25, fig. 3. *1960 (CISJ): Coralliobia akibumii Kira; p. 63, pl. 25, fig. 3 [with short description in Japanese]. 1961-1989 (CISJ): Coralliobia akibumii Kira; р. 63/pl 25, 16. 3. 1962-1968 (SWPC): Coralliobia akibumii Kira (п. sp.) [sic]; p. 68, pl. 26, fig. 3. Taxonomic note: Listed as of Kira (1959) in synonymy of Coralliophila inflata (Dunker, 1847) by Kosuge & Suzuki (1985: 34). (18) Coralliophila pyriformis Kira, 1959 1954-1958 (CISJ): Coralliophila pyriformis Kuroda, MS.; p. 51, pl. 25, fig. 12 [nom. nud.]. *1959 (CISJ): Coralliophila pyriformis Kuroda, MS.; р. 64, pl. 25, fig. 12 [with short description in Japanese]. 1960—1989 (CISJ): Coralliophila pyriformis Kira; р: 64, ple 25; 10: 12: 1965-1968 (SWPC): Coralliophila pyriformis Kira; p. 69, pl. 26, fig. 12. 138 BIELER Q/PETIT Taxonomic note: Listed in synonymy of Cor- alliophila radula (A. Adams, 1855) by Kosuge & Suzuki (1985: 39). (19) Latiaxis kawamurai Kira, 1959 1954—1958 (CISJ): Latiaxis kawamurai Kuroda, MS.; р. 51, pl. 25, fig. 20 [пот. nud.]. “1959 (CISJ): Latiaxis kawamurai Kuroda, MS; p. 65, pl. 25, fig. 20 [with short description in Japanese]. 1960 (CISJ): Latiaxis kawamurai Kira; p. 65, pl. 25, fig. 20. 1961-1989 (CISJ): Laticxis [sic] kawamurai Kira; p. 65, pl. 25, fig. 20. 1962-1968 (SWPC): Latiaxis kawamurai Kira; p. 70, pl. 26, fig. 20. Taxonomic note: Kuroda, in October 1958 [Venus, 20(2)], published an illustration and figure caption of what he intended to describe аз “Latiaxis kawamurai Kuroda, n.sp.” The text describing the new species appeared only in November 1959 [Venus, 20(4)], eight months after Kira had given a description in CISJ. Kuroda (1959), recognizing Kira’s prior- ity, correctly cited “Latiaxis kawamurai Kira, 1959” in the text (1959: 319). Placed in genus Babelomurex by Kosuge & Suzuki (1985: 14). Buccinidae (20) Babylonia pallida Kira, 1959 [preoccu- pied, replaced by B. kirana Habe, 1965] 1954-1958 (CISJ): Babylonia pallida Kuroda, MS.; р. 52, pl. 26, fig. 28 [nom. nud.]. “1959 (CISJ): Babylonia pallida Kuroda, MS.; р. 69, pl. 26, fig. 28 [with short description in Jap- anese]. 1960-1963 (CISJ): Babylonia pallida Kira; р. 69, pl. 26, fig. 28. 1962-1968 (SWPC): Babylonia pallida Kira; p. 75; Pl227, 119228. 1965-1989 (CISJ): Babylonia pallida Kuroda [sic]; p. 69, pl. 26, fig. 28. Taxonomic note: Placed in synonymy of Babylonia kirana n.sp. by Habe (1965: 119), who found Kira's name preoccupied by An- cilla pallida Perry, 1811 (secondary homon- ymy). Altena & Gittenberger (1981: 28-29) considered B. kirana as a nomen novum for B. pallida Kira, non Perry, and selected the shell figured by Kira (1959: pl. 26, fig. 28) as the lectotvpe of B. pallida Kira, and, conse- quently, of B. kirana Habe. However, ICZN Article 72(e) [a replacement name for a prior species-group name has the same name- bearing type] demands that “ап author pro- poses a new species group-name expressly as areplacement name for a prior one.” It can be argued that B. kirana Habe was not indi- cated “expressly as a replacement name,” as itis only after Habe (1965: 119) has illustrated and described the species and named a type specimen, that he mentions that the species had previously been named. Altena & Gitten- berger (1981: 29) also state that “B. pallida Hirase, 1934, and B. pallida Kira, 1959, have been introduced independently for the same species and, therefore, are primary hom- onyms and synonyms,” and they select the specimen figured by Hirase (1934: pl. 104, fig. 9) as the lectotype of B. pallida Hirase. The listing and illustration of B. pallida Hirase, 1934, however does not fulfill the require- ments of ICZN Article 13(a) [criteria of avail- ability to be satisfied by new names published after 1930] and has to be regarded as a nomen nudum. The nude name “Babylonia pallida Hirase” may have been what Kira meant when he first listed “Babylonia pallida Kuroda, MS.” (21) Neptunea fukueae Kira, 1959 1954-1958 (CISJ): Neptunea fukueae Kuroda, MS.; p. 55, pl. 27, fig. 4 [nom. nud.]. *1959 (CISJ): Neptunea fukueae Kuroda, MS.; p. 69, pl. 27, fig. 4 [with short description in Jap- апезе]. 1960—1963 (CISJ): Neptunea fukueae Kira; р. 69, pl. 27, fig. 4. 1962-1968 (SWPC): Neptunea fukueae Kira; p. 76, pl. 28, fig. 4. 1965-1989 (CISJ): Neptunea fukueae Kuroda [sic]; p. 69, pl. 27, fig. 4. Taxonomic note: Listed as of Kira (without date) by Habe & Sato (1973: 2) when they made it type species of the new genus Goli- kovia. (22) Buccinum isaotakii Kira, 1959 1954-1958 (CISJ): Buccinum (Lischke); p. 55, pl. 27, fig. 8. ‘1959 (CISJ): Buccinum isao-takii Oyama, MS.; p. 70, pl. 27, fig. 8 [with short description in Japanese]. 1960-1989 (CISJ): Buccinum isao-takii Kira; р. 70, pl. 27, fig. 8. 1962-1968 (SWPC): Buccinum isaotakii Kira; p. 76, pl. 28, fig. 8. leucostoma TETSUAKI KIRA’S ILLUSTRATIONS OF SHELLS Nassariidae (23) Nassarius (Zeuxis) kiiensis Kira, 1959 1954а (CISJ): Nassarius (Alectrion) kiiensis Kuroda, MS.; р. 56, pl. 28, fig. 21 [nom. пиа.]. 1954b-1958 (CISJ): Nassarius (Zeuxis) kilensis Kuroda, MS.; р. 56, pl. 28, fig. 21 [nom. nud.]. *1959 (CISJ): Nassarius (Zeuxis) kiiensis Kuroda, MS.; p. 73, pl. 28, fig. 21 [with short description in Japanese]. 1960-1963 (CISJ): Nassarius (Zeuxis) kiiensis Kira; p. 73, pl. 28, fig. 21. 1962-1968 (SWPC): Zeuxis kiiensis Kira; р. 81, pl. 29, fig. 21. 1965-1989 (CISJ): Zeuxis kiiensis (Kira); р. 73, pl. 28, fig. 21. Taxonomic note: Listed in synonymy of Nas- sarius castus (Gould, 1850) by Cernohorsky (1984: 131). Fasciolariidae (24) Granulifusus kiranus Shuto, 1958 [Trans. Proc. Paleont. Soc. Japan, 31: 258, pl. 38, fig. 1] 1954а (CISJ): Fusinus kirana [sic] Kuroda, MS.; р. 60, pl. 30, fig. 3 [пот. nud.]. 1954b-1958 (CISJ): Granulifusus kiranus Kuroda, MS.; p. 60, pl. 30, fig. 3 [nom. nud.]. 1959 (CISJ): Granulifusus kiranus Kuroda, MS. [sic]; p. 77, pl. 30, fig. 3. 1960—1989 (CISJ): Granulifusus kiranus Shuto; р: 77, pl. 30, fig. 3: 1962-1968 (SWPC): Granulifusus Shuto; р: 85, pl. 31, fig. 3. kiranus (25) Fusinus gemmuliferus Kira, 1959 1954-1958 (CISJ): Fusinus gemmuliferus Kuroda, MS.; p. 60, pl. 30, fig. 5 [nom. nud.]. “1959 (CISJ): Fusinus gemmuliferus Kuroda, MS.; р. 77, pl. 30, fig. 5 [with short description in Japanese]. 1960-1989 (CISJ): Fusinus gemmuliferus Kira; рт, р: 30, fig: 5. 1962-1968 (SWPC): Fusinus gemmuliferus Kira; 9: 85, pl. ЗТ, fig. 5. (26) Fusinus crassiplicatus Kira, 1959 1954-1958 (CISJ): Fusinus crassiplicatus Kuroda, MS.; р. 60, pl. 30, fig. 6 [пот. nud.]. “1959 (CISJ): Fusinus crassiplicatus Kuroda, MS.; р. 78, pl. 30, fig. 6 [with short description in Japanese]. 1960-1989 (CISJ): Fusinus crassiplicatus Kira; p. 78, pl. 30, fig. 6. 1962-1968 (SWPC): Fusinus crassiplicatus Kira; p. 85, pl. 31, fig. 6. 139 Olividae (27) Turrancilla apicalis Kira, 1959 1954-1958 (CISJ): Turrancilla apicalis 1$. Taki, MS.; p. 63, pl. 31, fig. 2 [nom. nud.]. *1959 (CISJ): Turrancilla apicalis Is. Taki, MS.; р. 79, pl. 31, fig. 2 [with short description in Jap- anese]. 1960-1989 (CISJ): Turrancilla suavis (Yo- koyama); p. 79, pl. 31, fig. 2. 1962-1968 (SWPC): Turrancilla suavis (Yo- koyama); p. 88, pl. 32, fig. 2. (28) Baryspira urasima Kira, 1959 1954a (CISJ): Baryspira hinomotoensis (Yokoyama); p. 63, pl. 31, fig. 3. 1954b-1958 (CISJ): Baryspira urasima 1$. Taki, MS.; p. 63, pl. 31, fig. 3 [nom. nud.]. *1959 (CISJ): Baryspira urasima 1$. Taki, MS.; р. 80, pl. 31, fig. 3. [From here on different shell figured! With short description in Japanese]. 1960-1989 (CISJ): Baryspira urasima Kira; p. 80, pl. 31, fig. 3. 1962-1968 (SWPC): Baryspira hinomotoensis (Yokoyama); p. 88, pl. 32, fig. 3. Taxonomic note: Listed as synonym of Baryspira hinomotoensis (Yokoyama, 1922) by Kuroda et al. (1971: 195). (29) Oliva hirasei Kuroda & Habe, 1952 [Check List, p. 74] 1954-1958 (CISJ): Oliva hirasei Kuroda, MS. [sic]; p. 63, pl. 31, fig. 8. 1959 (CISJ): Oliva hirasei Kuroda, MS. [sic]; p. 80, pl. 31, fig. 8. 1960-1989 (CISJ): Oliva hirasei Kira [sic]; р. 80, pl. 31, fig. 8. 1962-1968 (SWPC): Oliva hirasei Kira [sic]; р. 89, pl. 32, fig. 8. Taxonomic note: Kuroda & Habe (1952: 74) give this name for a figure in Hirase (1909: pl. 4, fig. 26). As Hirase’s work (1909: 45, 46) contains a description of the cited figure, “Oliva irisans Lam. Var. ?,” the name can be accepted as of Kuroda 8 Habe (1952) [ICZN Ап. 13(a)(ii)]. Petuch & Sargent (1986) list this name in their index as of Kuroda 4 Habe (1952), but in their text as of Kira (1959). Mitridae (30) Mitropifex hirasei Kira, 1962 1954a (CISJ): Mitra (Scabricola) japonica A. Ad- ams; p. 68, pl. 34, fig. 2. 1954b-1958 (CISJ): Vexillum (Uromitra) sp.; p. 68, pl. 34, fig. 2. 140 1959-1963 (CISJ): Vexillum (Uromitra) sp.; p. 88, pl. 34, fig. 2. *1962 (SWPC): Mitropifex hirasei Kira (n.sp.); р. 98, pl. 35, fig. 2. 1965-1968 (SWPC): Mitropifex hirasei Kira (n.sp.) [sic]; p. 98, pl. 35, fig. 2. 1965-1989 (CISJ): Mitropifex hirasei Kira; р. 88, pl. 34, fig. 2. (31) Mitra (Cancilla) yagurai Kira, 1959 1954a (CISJ): Mitra (Cancilla) yagurai Kuroda, MS.; р. 68, pl. 34, fig. 3 [nom. nud.]. 1954b-1958 (CISJ): Mitr [sic] (Cancilla) уадига! Kuroda, MS.; р. 68, pl. 34, fig. 3 [nom. nud.]. *1959 (CISJ): Mitra (Cancilla) yagurai Kuroda, MS.; p. 88, pl. 34, fig. 3 [with short description in Japanese]. 1960-1963 (CISJ): Mitra (Tiara) yagurai Kira; р. 88, pl. 34, fig. 3. 1962-1968 (SWPC): Tiara yagurai (Kira); р. 98, pl. 35, fig. 3. 1965—1989 (CISJ): Tiara уадига! (Kira); р. 88, pl. 34, fig. 3. Taxonomic note: Listed as synonym of Mitra interlirata Reeve, 1844, by Cernohorsky (1970: 46). Turridae (32) Ancistrosyrinx pulcherrissima Kira, 1959 1954a (CISJ): Ancistrosyrinx pulcherissima [sic] Kuroda, MS.; p. 71, pl. 35, fig. 1 [nom. nud.]. 1954b-1958 (CISJ): Ancistrosyrinx pulcherris- sima Kuroda, MS.; р. 71, pl. 35, fig. 1 [nom. nud.]. ‘1959 (CISJ): Ancistrosyrinx pulcherrissima Kuroda; p. 90, pl. 35, fig. 1 [with short descrip- tion in Japanese]. 1960-1963 (CISJ): Ancistrosyrinx pulcherris- sima Kira; p. 90, pl. 35, fig. 1. 1962-1968 (SWPC): Ancistrosyrinx pulcherrissi- mus Kira; p. 100, pl. 36, fig. 1. 1965-1989 (CISJ): Ancistrosyrinx pulcherrissi- mus Kira; p. 90, pl. 35, fig. 1. Taxonomic note: Listed as of Kuroda, 1958, by Powell (1966: 42). (33) Daphnella nobilis Kira, 1959 1954а (CISJ): Daphnella nofilis [sic] Kuroda, MS.; р. 71, pl. 35, fig. 4 [nom. nud.]. 1954b-1958 (CISJ): Daphnella nobilis Kuroda, MS.; р. 71, pl. 35, fig. 4 [пот. nud.]. “1959 (CISJ): Daphnella nobilis Kuroda, MS.; р. 90, pl. 35, fig. 4 [with short description in Jap- апезе]. 1960-1989 (CISJ): Daphnella nobilis Kira; р. 90, pl. 35, fig. 4. 1962-1968 (SWPC): Daphnella nobilis Kira; p. 100, pl. 36, fig. 4. BIELER & PETIT Conidae (34) Chelyconus kinoshitai Kuroda, 1956 [Ve- nus, 19(1): 6, text-fig. 7] 1954-1955 (CISJ): Floraconus ? kinoshitai Kuroda, MS.; р. 75, pl. 37, fig. 18 [nom. nud.]. 1957-1958 (CISJ): Floraconus ? kinoshitai Kuroda, MS. [sic]; p. 75, pl. 37, fig. 18. 1959-1989 (CISJ): Chelyconus kinoshitai Kuroda; p. 97, pl. 37, fig. 18. 1962-1968 (SWPC): Chelyconus kinoshitai (Kuroda); p. 108, pl. 38, fig. 18. (35) Asprella (Conasprella ?) ichinoseana Kuroda, 1956 [Venus, 19(1): 10, pl. 1, fig. 5] 1954a (CISJ): Asprella (Conasprella) ichinose- ana Kuroda [sic]; p. 76, pl. 38, fig. 3 [nom. nud.]. 1954b-1955 (CISJ): Asprella ichinoseana Kuroda, MS.; р. 76, pl. 38, fig. 3 [nom. nud.]. 1957-1958 (CISJ): Asprella ichinoseana Kuroda, MS. [sic]; p. 76, pl. 38, fig. 3. 1959-1989 (CISJ): Asprella (Conasprella) ichi- noseana Kuroda; p. 98, pl. 38, fig. 3. 1962-1968 (SWPC): Asprella (Conasprella) ichi- noseana Kuroda; p. 109, pl. 39, fig. 3. Bradybaenidae (36) Euhadra roseoapicalis Kira, 1959 1954a (CISJ): Euhadra brandtii (Kobelt); p. 132, pl. 66, fig. 16. 1954b-1958 (CISJ): Euhadra brandtii (Kobelt); p. 132, pl. 66, fig. 15 [renumbered]. *1959 (CISJ): Euhadra roseoapicalis Kuroda, MS.; р. 182, р. 66, fig. 15 [with short descrip- tion in Japanese]. 1960-1963 (CISJ): Euhadra brandti [sic] (Ko- belt); p. 182, pl. 66, fig. 15. 1962-1968 (SWPC): Euhadra brandti roseoapi- calis Kira; p. 197, pl. 67, fig. 15. 1965-1989 (CISJ): Euhadra brandti roseoapica- lis Kira; p. 182, pl. 66, fig. 15. (37) Euhadra grata gratoides Kira, 1959 1954a (CISJ): Euhadra grata gratoides Kira, М$.; | р. 132, pl. 66, fig. 19 [пот. nud.]. 1954b-1958 (CISJ): Euhadra grata gratoides Kira, MS.; p. 132, pl. 66, fig. 17 [renumbered] [nom. nud.]. *1959 (CISJ): Euhadra grata gratoides Kira; p. 182, pl. 66, fig. 17 [with short description in | Japanese]. 1960-1989 (CISJ): Euhadra grata gratoides | Kira; p. 182, pl. 66, fig. 17. 1962-1968 (SWPC): Euhadra grata gratoides Kira; p. 197, pl. 67, fig. 17. TETSUAKI KIRA’S ILLUSTRATIONS OF SHELLS 141 SCAPHOPODA Siphonodentaliidae (38) Cadulus (Platyschides) novilunatus Kira, 1959 1954а (CISJ): Gadila novilunata Kuroda, MS; р. 80, pl. 40, fig. 2 [пот. nud.]. 1954b-1958 (CISJ): Cadulus (Platyschides) novilunatus Kuroda, MS.; p. 80, pl. 40, fig. 2 [пот. nud.]. *1959 (CISJ): Cadulus (Platyschides) noviluna- tus Kuroda, MS.; р. 104, pl. 40, fig. 2 [with short description in Japanese]. 1960-1963 (CISJ): Cadulus (Platyschides) novilunatus Kira; p. 104, pl. 40, fig. 2. 1962-1968 (SWPC): Gadila (Platyschides) novilunata (Kira); p. 116, pl. 41, fig. 2. 1965-1989 (CISJ): Pulsellum virginalis (Boisse- vain); p. 104, pl. 40, fig. 2. Taxonomic note: Listed as “Gadila novilunata Kira, 1959,” in synonymy of Platyschides vir- ginalis (Boissevain, 1906) by Habe (1964: 49), and in synonymy of “Cadulus (Poly- schides) virginalis Biossevain [sic]” by Habe & Kosuge (1964b: 12); listed as “Gadila (Platyschides) noviluna [sic] Kira, 1959,” un- der Polyschides (Platyschides) virginalis by Habe (1977: 342). (39) Entalina majestica Kira, 1959 1954-1958 (CISJ): Entalina majestica Kuroda, MS.; р. 80, pl. 40, fig. 3 [пот. nud.]. *1959 (CISJ): Entalina majestica Kuroda, MS; р. | 105, pl. 40, fig. 3 [with short description in Jap- anese]. ‚1960-1963 (CISJ): Entalina majestica Kira; р. 105, pl. 40, fig. 3. | 1962-1968 (SWPC): Entalina majestica Kira; р. 116, pl. 41, fig. 3. 1965-1989 (CISJ): Entalina quadriangularis [sic] (Boissevain); p. 105, pl. 40, fig. 3. Taxonomic note: Listed as synonym of Enta- lina quadriangularis [error for quadrangularis] ‚Boissevain, 1906, by Habe (1964: 39; 1977: 1339), and of Е. quadrangularis by Habe & Ko- ‚suge (1964b: 8). Dentaliidae | (40) Dentalium (Episiphon) candelatum Kira, 1959 | 1954-1958 (CISJ): Dentalium (Episiphon) can- delatum Kuroda, MS.; р. 80, pl. 40, fig. 5 [nom. nud.]. "1959 (CISJ): Dentalium (Episiphon) candelatum Kuroda, MS.; p. 105, pl. 40, fig. 5 [with short description in Japanese]. 1960-1963 (CISJ): Dentalium (Episiphon) can- delatum Kira; p. 105, pl. 40, fig. 5. 1962-1968 (SWPC): Episiphon candelatum (Kira); p. 116, pl. 41, fig. 5. 1965-1989 (CISJ): Episiphon candelatum (Kira); p. 105, pl. 40, fig. 5. (41) Dentalium (Pictodentalium) formosum hirasei Kira, 1959 1954-1958 (CISJ): Dentalium formosum Adams et Reeve; p. 80, pl. 40, fig. 11. *1959 (CISJ): Dentalium (Pictodentalium) formo- sum hirasei Kuroda, MS.; р. 105, pl. 40, fig. 11 [with short description in Japanese]. 1960-1963 (CISJ): Dentalium (Pictodentalium) formosum hirasei Kira; p. 105, pl. 40, fig. 11. 1962-1968 (SWPC): Pictodentalium formosum hirasei (Kira); p. 117, pl. 41, fig. 11. 1965-1989 (CISJ): Dentalium (Pictodentalium) formosum hirasei (Kira); p. 105, pl. 40, fig. 11. Taxonomic note: Placed in synonymy of Den- talium formosum Adams & Reeve, 1850, by Habe (1964: 15; 1977: 332) and Habe & Ko- suge (1964b: 4). (42) Genus-group name Pictodentalium Taxonomic note: With his introduction of Den- talium formosum hirasei, Kira (1959 and following years, see above) used the genus- group name “Pictodentalium,” without de- scription or indication that it was new. Author- ship for this name was credited to Kira (1959) by Habe & Kosuge (1964b: 4) and Palmer (1974: 118); the latter lists D. formosum hirasei as type species. However, Kira's use of the name does not fulfill the ICZN require- ments [Articles 13(a),(e), criteria of availability to be satisfied by new names published after 1930], and Pictodentalium Kira has to be con- sidered a nomen nudum. As ICZN Article 13(a)(i) does not apply any degree to differ- entiation, the name might date from Palmer (1974: 118) who lists the name for a group comprising “the multicoloured dentaliids.” BIVALVIA Nuculidae (43) Acila schencki Habe, 1958 [1958b, Publ. Seto Mar. Biol. Lab., 6(3): 243] 1954—1958 (CISJ): Acila schencki Kuroda, MS.; р. 83, pl. 41, fig. 6 [пот. nud.]. 142 BIELER & PETIT 1959 (CISJ): Acila schencki Kuroda, MS. [sic]; p. 107, pl. 41, fig. 6. 1960—1963 (CISJ): Acila schencki Kira [sic]; р. 107, pl. 41, fig. 6. 1962-1968 (SWPC): Acila schencki Kira [sic]; p. 119, pl. 42, fig. 6. 1965-1989 (CISJ): Acila schencki Kuroda [sic]; p. 107, pl. 41, fig. 6. Taxonomic note: Habe (1958b: 243) lists this as “Acila schencki Kuroda (MS),” and in syn- onymy shows that it is “Acila divaricata sub- mirabilis Makiyama” Schenck, 1936, non Makiyama, 1926 (p. 151, pl. 12, fig. 9). As there is a description of submirabilis in Schenck (1936: 88-90), the name A. schencki is here considered valid as of Habe (1958) [ICZN Ан. 13(a)(ii)]. Habe (1977: 15) lists it as “Acila (Acila) divaricata schencki Kira, 1959.” Nuculanidae (44) Nuculana (Thestyleda) acinacea Habe, 1958 [1958b, Publ. Seto Mar. Biol. Lab., 6(3): 247] 1954-1958 (CISJ): Nuculana (Thestyleda?) aci- nacea Habe, MS.; p. 83, pl. 41, fig. 9 [nom. nud.]. 1959 (CISJ): Nuculana (Thestyleda?) acinacea Habe, MS. [sic]; p. 107, pl. 41, fig. 9. 1960-1963 (CISJ): Nuculana (Thestyleda?) aci- nacea Habe; p. 107, pl. 41, fig. 9. 1965-1989 (CISJ): Nuculana (Thestyleda) aci- nacea Habe; p. 107, pl. 41, fig. 9. 1962-1968 (SWPC): Nuculana (Thestyleda) acinacea Habe; p. 119, pl. 42, fig. 9. Limopsidae (45) Limopsis tajimae emphaticus Kira, 1959 1954a (CISJ): Limopsis tajimae emphaticus Kuroda, MS.; p. 88, pl. 44, fig. 4 [nom. nud.]. 1954b-1958 (CISJ): Limopsis tajimae emphati- cus Kira [sic], MS.; p. 88, pl. 44, fig. 4 [nom. nud.]. "1959 (CISJ): Limopsis tajimae emphaticus Kira; p. 112, pl. 44, fig. 4 [with short description in Japanese]. 1960-1989 (CISJ): Limopsis tajimae emphaticus Kira; p. 112, pl. 44, fig. 4. 1962-1968 (SWPC): Limopsis tajimae emphati- cus Kira; p. 125, pl. 45, fig. 4. Taxonomic note: Listed in synonymy of Limopsis tajimae Sowerby, 1914, by Kuroda et al. (1971: 338) and Habe (1977: 48). Cardiidae (46) Fragum loochooanum Kira, 1959 1954a (CISJ): Fragum loochooanus Kuroda, MS.; р. 108, pl. 54, fig. 13 [nom. nud.]. 1954b-1958 (CISJ): Fragum loochooanum Kuroda, MS.; р. 108, pl. 54, fig. 13 [пот. nud.]. ‘1959 (CISJ): Fragum loochooanum Kuroda, MS.; р. 137, pl. 54, fig. 13 [with short descrip- tion in Japanese]. 1960-1989 (CISJ): Fragun [sic] loochooanum Kira; p. 137, pl. 54, fig. 13. 1962-1968 (SWPC): Егадит loochooanum Kira; p. 154, pl. 55, fig. 13. (47) Clinocardium uchidai Habe, 1955 [Publ. Akkeshi Mar. Biol. Stat., 4: 11, pl. 2, figs. 5, 6] 1954—1955 (CISJ): Clinocardium uchidai Habe, MS.; р. 111, pl. 55, fig. 1 [nom. nud.]. 1957—1958 (CISJ): Clinocardium uchidai Habe, MS; [sic]; р. did, ple 55; Mig 1: 1959 (CISJ): Clinocardium uchidai Habe, MS. [Sic]? р: 138, р]. 55 gl: 1960-1989 (CISJ): Clinocardium uchidai Habe; p. 138, pl. 55, fig. 1. 1965-1968b (SWPC): Clinocardium uchidai Habe; p. 156, pl. 56, fig. 1. Taxonomic note: Placed in synonymy of Cli- nocardium californiense (Deshayes, 1839) by Habe (1977: 172). (48) Vasticardium compunctum Kira, 1959 1954-1958 (CISJ): Vasticardium compunctum Kuroda, MS.; р. 111, pl. 55, fig. 9 [пот. nud.]. “1959 (CISJ): Vasticardium compunctum Kuroda, MS.; p. 139, pl. 50, fig. 9 [with short description in Japanese]. 1960-1989 (CISJ): Vasticardium compunctum Kira; p. 139, pl. 55, fig. 9. 1962-1968 (SWPC): Vasticardium compunctum Kira; p. 156, pl. 56, fig. 9. (49) “Vasticardium serricostatum” 1954-1958 (CISJ): Vasticardium serricostatum Kuroda, MS.; р. 111, pl. 55, fig. 11 [пот. nud.]. 1959 (CISJ): Vasticardium serricostatum Kuroda, MS.; p. 139, pl. 55, fig. 11 [with short descrip- tion in Japanese]. 1960-1963 (CISJ): Vasticardium serricostatum Melvill et Standen [sic], var.; p. 139, pl. 55, fig. I. 1962-1968 (SWPC): Vasticardium okinawaense Kuroda; p. 157, pl. 56, fig. 11. 1965-1989 (CISJ): Vasticardium okinawaense Kuroda; p. 139, pl. 55, fig. 11. Taxonomic note: The name “serricostatum Kuroda” is an error for what was meant to be described as a variety of Cardium (Trachycar- TETSUAKI KIRA'S ILLUSTRATIONS OF SHELLS 143 dium) serricostatum Melvill & Standen, 1899 (p. 191, pl. 11, fig. 20). It was subsequently named by Kuroda (1960: 82) as “Trachy- cardium (Acrosterigma) {serricostatum Melvill & Standen var?) okinawaense Kuroda (nov.),” referring to Kira’s illustration (1959: pl. 55, fig. 11). Peculiarly, Fischer-Piette (1977) lists “Vasticardium serricostatum Kuroda’ as il- lustrated by Kira (1955) in the synonymy of Laevicardium (Vasticardium) flavum (Linné, 1758), but has “Vasticardium okinawaense Kuroda” as illustrated by Kira (1962), using the same figure, in synonymy with Cardium enode Sowerby, 1834. Veneridae (50) Leukoma japonica Kira, 1954 1954a (CISJ): Leucoma [sic] japonica Kira, MS.; р. 115, pl. 57, fig. 17 [пот. nud.]. *1954a (CISJ): Leukoma japoniac [sic] sp. nov.; p. 163. 1954b-1958 (CISJ): Leukoma japonica Kira, MS. SICA plo tig! 17 1954b-1958 (CISJ): Leukoma japonica Kira sp. nov. [sic]; p. 163. 1959-1963 (CISJ): Leukoma japonica Kira; p. 147, pl. 57, fig. 17. 1962-1968 (SWPC): Glycydonta marica japo- nica (Kira); p. 164, pl. 58, fig. 17. 1965-1989 (CISJ): Glycydonta marica japonica (Kira); p. 147, pl. 57, fig. 17. Taxonomic note: As “Leuboma [sic] marica japonica Kira, 1954,” placed in synonymy of Glycodonta marica (Linné, 1758) by Habe (1977: 250). (51) Irus ishibashianus Kuroda & Habe, 1952 [Check List: 21] 1954—1958 (CISJ): /rus ishibashianus Kuroda et Habe; p. 115, pl. 57, fig. 25. 1959 (CISJ): /rus ishibashianus Kuroda, MS. [sic]; p. 148, pl. 57, fig. 25. 1960—1963 (CISJ): /rus ishibashianus Kuroda et Habe; p. 148, pl. 57, fig. 25. 1962-1968 (SWPC): Notirus ishibashianus (Kuroda et Habe); p. 165, pl. 58, fig. 25. 1965-1989 (CISJ): Notirus ishibashianus Kuroda et Habe; p. 148, pl. 57, fig. 25. Taxonomic note: Kuroda & Habe (1952: 21) introduced this as a new name for “ Venerupis irus (Linné),” Yokoyama, 1924 (1924: 44, pl. 2, fig. 23), non Donax irus Linné, 1758. Kuroda et al. (1971: 427), Hanshin Shell Club (1986: 45), Inaba & Oyama (1977: 52), and Habe (1977: 268) list it as of Kuroda & Habe, 1952. Habe (1981: 166) lists it as of Kira (1959). Asaphidae/Psammobiidae [depending on printing] (52) Solecurtus dunkeri Kira, 1959 1954—1958 (CISJ): Solecurtus dunkeri Kuroda, MS.; р. 116, pl. 58, fig. 22 [пот. nud.]. *1959 (CISJ): Solecurtus dunkeri Kuroda, MS .; р. 152, pl. 58, fig. 22 [with short description in Japanese]. 1960-1963 (CISJ): Solecurtus dunkeri Kira; р. 152 р! 158; 19: 22. 1962-1968 (SWPC): Solecurtus dunkeri Kira; р. 169, pl. 59, fig. 22. 1965—1989 (CISJ): Solecurtus dunkeri Kuroda, MS. [sic]; p. 152, pl. 58, fig. 22. Taxonomic note: Listed in synonymy of Sole- curtus divaricatus (Lischke, 1869) by Habe (1977: 224). (53) Nuttallia solida Kira, 1953 [Venus, 17(3): 149, figs. 1c, 1d, 2c] 1954-1958 (CISJ): Nuttallia solida Kira; р. 119, pl. 59, fig. 10. 1959-1989 (CISJ): Nuttallia solida Kira; р. 154, pl. 59, fig. 10. 1962-1968 (SWPC): Nuttallia solida Kira; p. 171, pl. 60, fig. 10. Taxonomic note: Listed in synonymy of Nut- tallia japonica (Reeve, 1857) by Habe (1977: 224). Tellinidae (54) Heteromacoma oyamai Kira, 1954 1954a (CISJ): Heteromacoma oyamai Kira, MS.; p. 119, pl. 59, fig. 21 [nom. nud.]. *1954а (CISJ): Heteromacoma oyamai sp. nov.; p. 164. 1954b-1958 (CISJ): Heteromacoma oyamai Kira, MS. [sic]; p. 119, pl. 59, fig. 21. 1954b-1958 (CISJ): Heteromacoma oyamai Kira sp. nov. [sic]; p. 164. 1959 (CISJ): Heteromacoma oyamai Kira; р. 155, pls 59, fig. 21. 1960-1963 (CISJ): Macoma oyamai (Kira); р. 159 р 5989 2 1962-1968 (SWPC): Heteromacoma оуата! Kira; p. 172, pl. 60, fig. 21. 1965-1989 (CISJ): Heteromacoma oyamai (Kira); p. 155, pl. 59, fig. 21. Taxonomic note: Listed as Heteromacoma irus oyamai Kira, 1959, by Habe (1977: 210). 144 BIELER SPENT Unionidae (55) Lanceolaria oxyrhyncha cuspidata Kira, 1959 1954-1958 (CISJ): Lanceolaria oxyrhyncha cus- pidata Kuroda, MS.; 127, pl. 63, fig. 18 [пот. nud.]. “1959 (CISJ): Lanceolaria oxyrhyncha cuspidata Kuroda, MS.; p. 172, pl. 63, fig. 18 [with short description in Japanese]. 1960-1989 (CISJ): Lanceolaria oxyrhyncha cus- pidata Kira; p. 172, pl. 63, fig. 18. 1962-1968 (SWPC): Lanceolaria oxyrhyncha cuspidata Kira; p. 187, pl. 64, fig. 18. Taxonomic note: Listed in synonymy of Lan- ceolaria grayana (Lea, 1834) by Habe (1977: 115). ACKNOWLEDGEMENTS The following made copies of Kira publica- tions available or otherwise responded to re- quests for data: Dr. Arthur E. Bogan, Dr. Phi- lippe Bouchet, Mr. Richard В. Forrer, Dr. Michael G. Hadfield, Dr. Richard S. Houbrick, Dr. Ronald Janssen, Ms. Anne Joffe, Dr. E. Alison Kay, Mr. José H. Leal, Mrs. Jo Anne Little, Dr. James H. McLean, Ms. Paula M. Mikkelsen, Mr. Edward Nieburger, Mr. David M. Pugh, Dr. Robert Robertson, Mr. Walter E. Sage Ill, Mr. Paul H. Scott, Dr. Donald R. Shasky, and Dr. Emily H. Vokes. For provid- ing translations and other data, we are in- debted to Dr. Akihiko Matsukuma, National Science Museum, Tokyo, Japan. Also, we thank two anonymous reviewers for construc- tive criticism on the manuscript. The publish- ing company (Hoikusha, Osaka) did not re- spond to our inquiries. LITERATURE CITED ABBOTT, R. T., 1968, The helmet shells of the world (Cassidae). Part 1. Indo-Pacific Mollusca, 2(9): 15-202. ALTENA, C. O. VAN REGTEREN & E. GITTEN- BERGER, 1981, The genus Babylonia (Proso- branchia, Buccinidae). Zoologische Verhandelin- gen uitgegeven door het Rijksmuseum van Natuurlijke Historie te Leiden, 188: 1-57, pls. 1— ie AZUMA, M., 1976, Systematic studies on the Re- cent Japanese family Ovulidae (Gastropoda)— IV. Venus, 35(3): 106-117, pl. 1. CATE, C. N., 1973, A systematic revision of the Recent cypraeid family Ovulidae (Mollusca: Gas- tropoda). The Veliger, 15, Supplement, iv + 116 pp., 51 pls. CERNOHORSKY, W. O., 1967, Marine shells of the Pacific. Pacific Publications Pty. Ltd., Syd- ney. 248 pp., illus. CERNOHORSKY, W. O., 1970, Systematics of the families Mitridae & Volutomitridae (Mollusca: Gastropoda). Bulletin of the Auckland Institute and Museum, 8: i-iv, 1-190. CERNOHORSKY, W. O., 1984, Systematics of the family Nassariidae (Mollusca: Gastropoda). Bul- letin of the Auckland Institute and Museum, 14: iv + 356 pp. (incl. 51 pls.). FISCHER-PIETTE, E., 1977, Révision des Cardi- idae (Mollusques Lamellibranches). Mémoires du Muséum National d'Histoire Naturelle, Nou- velle Série, série A, Zoologie, 101: 1-212, pls. 1-12. HABE, T., 1955, Fauna of Akkeshi Bay XXI. Pele- cypoda and Scaphopoda. Publications of the Akkeshi Marine Biological Station, 4: 1-31, pls. 1-7. HABE, T., 1958a, On the radulae of Japanese ma- rine gastropods (4). Venus, 20(1): 43-60, pls. 2-3. HABE, T., 1958b, Report on the Mollusca chiefly collected by the S.S. Sôyô-Maru of the Imperial Fisheries Experimental Station on the continental shelf bordering Japan during the years 1922- 1930. Part 3. Lamellibranchia (1). Publications of the Seto Marine Biological Laboratory, 6(3): 241— 280, pls. 11-13. HABE, T., 1964, Fauna Japonica. Scaphopoda (Mollusca). Biogeographical Society of Japan. 59 pp., 5 pls. HABE, T., 1965, Notes on the ivory shell genus Babylonia Schluter (Mollusca). Bulletin of the Na- tional Science Museum Tokyo, 8(2): 115-124, pl. 1. HABE, T., 1977, Systematics of Mollusca in Japan. Bivalvia and Scaphopoda. Japan. xiii + 372 pp. HABE, T., 1981, A catalogue of molluscs of Wakayama Prefecture, the Province of Kii. |. Bi- valvia, Scaphopoda and Cephalopoda; based on the Kuroda’s manuscript and supervised by Tadashige Habe. Publications of the Seto Marine Biological Laboratory, Special Publications Se- ries, 7(1): i-xx, 1-301. HABE, T. & S. KOSUGE, 1964a, A list of the Indo- Pacific molluscs, concerning to the Japanese molluscan fauna (2). Class Gastropoda (Super- family Stromboidea). National Science Museum, Tokyo. 14 pp. HABE, Т. & S. KOSUGE, 19645, A list of the Indo- Pacific molluscs, concerning to the Japanese molluscan fauna (3). Class Scaphopoda. Na- tional Science Museum, Tokyo. 14 pp. HABE, T. & J. SATO, 1973, A classification of the family Buccinidae from the North Pacific. Pro- ceedings of the Japanese Society of Systematic Zoology, 8: 1-8, pls. 1-2 (“1972”, published in 1973 teste Inaba & Oyama, 1977). HANSHIN SHELL CLUB, 1986, Bibliography of Dr. TETSUAKI KIRA’S ILLUSTRATIONS OF SHELLS 145 Tokubei Kuroda (for commemoration of his 99th birthday). Nishinomya, 103 pp., 33 pls. HIRASE, Y., 1909, On Japanese marine Mollusca (XXV). The Conchological Magazine, 3(2): 41— 46, pl. 4. HIRASE, S., 1934, [See HIRASE, S. 1936]. HIRASE, S., 1936, A collection of Japanese shells with illustrations in natural colors. Fifth edition. Tokyo, pp. 1-14, 1—2, pls. 1-129, pp. 1-217 [The 1936 printing seen by us is titled “Fifth Edition” but contains a 1934 preface. As it is unlikely that this work went through five editions in this period of time, the “edition” probably means printing. We were unable to procure a copy of the 1934 printing and assume, as did Altena & Gitten- berger (1981), that the two printings do not differ substantially]. [ICZN] International Commission on Zoological No- menclature, 1985, International Code of Zoolog- ical Nomenclature, Third Edition. London, Berke- ley, and Los Angeles, xx + 338 pp. INABA, T. & K. OYAMA, (compilers), 1977, Cata- logue of molluscan taxa described by Tadashige Habe during 1939-1975, with illustrations of hith- erto unfigured species (for commemoration of his sixtieth birthday). 185 pp. (incl. 7 pls.); Tokyo. KIRA, T., 1953, On the Japanese species of the genus Nuttallia (Pelecypoda). Venus, 17(3): 144— 15111 KIRA, T., 1954, [Coloured illustrations of the shells of Japan]. [vill] + 172 + 24 pp., 67 pls.; Hoikusha, Osaka [title in Japanese; additional printings listed in this paper]. KIRA, T., 1959, Coloured illustrations of the shells of Japan. Enlarged and Revised Edition. [6] + vii + [1] + 239 pp., [1] + 71 pls.; Hoikusha, Osaka [additional printings listed in this paper]. KIRA, T., 1962, Shells of the western Pacific in color. [vii] + 224 pp., 72 pls.; Hoikusha, Osaka [additional printings listed in this paper]. KOSUGE, S. & M. SUZUKI, 1985, Illustrated cata- logue of Latiaxis and its related groups. Family Coralliophilidae. /nstitute of Malacology of Tokyo Special Publication, 1: 18 pp., 50 pls. KURODA, T., 1928, [plate only]. The Venus, 1(1): pl. 1 (November). KURODA, T., 1929, New Japanese shells. |. The Venus, 1(3): 77-82 (May). KURODA, T., 1956, New species of the Conidae (Gastropoda) from Japan. Venus, 19(1): 1-16, pl. ИЕ KURODA, T., 1958, [plates only]. Venus, 20(2): pls. 20-21 (October). KURODA, T., 1959, Descriptions of new species of marine shells from Japan. Venus, 20(4): 317- 335 (November). KURODA, T., 1960, A catalogue of molluscan fauna of the Okinawa Islands (exclusive of Ceph- alopoda). iv + 104 pp., 3 pls. KURODA, T. & T. HABE, 1952, Check list and bib- liography of the Recent marine Mollusca of Ja- pan. L. W. Satch, Tokyo, 210 pp. KURODA, T., T. HABE & K. OYAMA, 1971, The sea shells of Sagami Bay. Maruzen, Tokyo. xix + 741 pp. [in Jap.], pls. 1-121, 489 pp. [in Engl.], 51 pp. index, map. KURODA, T. & K. ITO, 1961, Molluscan shells from southern Ки. Venus, 21(3): 243-267, pls. 16-18. MAKIYAMA, J., 1926, Tertiary fossils from North Kankyö-dö, Korea. Memoirs of the College of Science, Kyoto Imperial University, (B)2(3): 143— 160, pls. 12-13. MAJIMA, R., 1987, Taxonomic study of Japanese species of Glossaulax (Gastropoda: Naticidae). Venus, 46(2): 57-74. MELVILL, J. C. 4 R. STANDEN, 1899, Report on the marine Mollusca obtained during the first ex- pedition of Prof. A. C. Haddon to the Torres Straits, in 1888-89. Journal of the Linnean So- ciety of London, Zoology, 27: 150-206, pls. 10— ale OSIMA, K., 1943, Familia Tonnidae. Conchologia Asiatica, 1(4): 111-136, pls. 1-5. PALMER, С. P., 1974, A supraspecific classification of the scaphopod Mollusca. The Veliger, 17(2): 115-123. PETUCH, E. J. & D. M. SARGENT, 1986, Atlas of the. living olive shells of the world. The Coastal Education & Research Foundation, Charlottes- ville, Virginia. pp. xiii, 253. POWELL, A. W. B., 1966, The molluscan families Speightiidae and Turridae. An evaluation of the valid taxa, both Recent and fossil, with lists of characteristic species. Bulletin of the Auckland Institute and Museum, 5: 1-184, pls. 1-23. SCHENCK, H. G., 1936, Nuculid bivalves of the genus Acila. Geological Society of America, Spe- cial Papers, 4: i-xiv, 1-149, pls. 1-18. SCHILDER, M. & F. A. SCHILDER, 1971. A cata- logue of living and fossil cowries. Taxonomy and bibliography of Triviacea and Cypraeacea (Gas- tropoda Prosobranchia). /nstitut Royal des Sci- ences Naturelles de Belgique Mémoires, (2)85: 1-246. SHUTO, T., 1958, Granulifusus from the Miyazaki group (Palaeontological study of the Miyazaki group — V). Transactions and Proceedings of the Palaeontological Society of Japan, N.S. 31: 253— 264, pl. 38. VOKES, E. H., 1971, Catalogue of the genus Murex Linné (Mollusca: Gastropoda); Muricinae, Ocenebrinae. Bulletins of American Paleontol- ogy, 61(268): 1-141. YOKOYAMA, M., 1924, Mollusca from the coral- bed of Awa. Journal of the College of Science, Tokyo Imperial University, 45(1): 1-62, pls. 1-5. Revised Ms. accepted 19 March 1990 MALACOLOGIA, 1990, 32(1): 147-154 SPERM STORAGE MECHANISMS AND FERTILIZATION IN FEMALES OF TWO SOUTH AMERICAN ELEDONIDS (CEPHALOPODA:OCTOPODA). José Angel Alvarez Perez', Manuel Haimovici? & Joao Carlos Brahm Cousin ABSTRACT Octopod species of the genus Eledone do not have spermathecae in the oviducal glands. Sperm masses are found within the ovary, where fertilization takes place. In two South American species, Eledone massyae and Eledone gaucha, unusual filamentous structures were observed in the animal pole of the oocyte and were entangled greatly with the sperm masses. These structures are extensions of the surrounding layers of the oocytes. The sperm penetrate the filaments forming agglomerates surrounded by a layer of follicular cells. The filaments shorten as the oocyte grows, drawing the enclosed spermatozoa to the ooplasm, in which fertilization occurs. These filaments allow sperm to be stored for long periods and might be analogous to spermathecae in the oviducal gland of Octopodinae. Key words: Cephalopoda, Eledone, fertilization, sperm storage, Octopodidae, Brazil. INTRODUCTION Female incirrate octopods can store sperm for a long time after mating. In two of the four Octopodidae subfamilies, the Octopodinae and Bathypolypodinae, internal sperm stor- age mechanisms and fertilization have been described (Petersen, 1959; Froesch & Mar- thy, 1975; Wells & Wells, 1977, O'Dor & Ma- lacaster, 1983). Less is known about the Ele- doninae and Graneledoninae. In Eledone cirrhosa, a time lag between copulation and spawning has been established in aquaria ex- periments (Mangold et al., 1971) but mecha- nisms of sperm storage are uncertain (Boyle, 1983). Eledone massyae Voss, 1964, and Ele- done gaucha Haimovici, 1988, were described recently and are little known. Haimovici & An- driguetto (1986) and Haimovici (1988) de- scribed morphological differences between these species and commented on their appar- ent geographical coexistence on the southern Brazilian shelf. Some unusual oocyte struc- tures were observed in the ovaries of both species. In this paper these structures are de- scribed and evidence is given for their in- volvement in sperm storage and fertilization. MATERIAL AND METHODS Reproductive organs of nine females of Eledone massyae and four females of E. gaucha were examined (Table 1). Octopuses were collected with a bottom trawl and fixed in 10% formalin or seawater Bouin solution. Oocytes and oviducal glands were dissected and embedded in paraffin (58°C) according to standard histological techniques (Gabe, 1968). Longitudinal and transverse sections (5 to 7 um) were stained with Harry's hema- toxilin-eosin. Terms applied to cephalopods and used in this paper: Spermatangia: Also called sperm sac. Evaginated spermatophores; bladders en- closing the sperm mass. Spermatophore: Complex sperm package used for transfer of sperm from male to fe- male. Spermatheca: Seminal receptacle. Pouch in females in which male gametes are stored at mating. RESULTS Oocytes Maturing oocytes remain attached by stalks to the inner epithelium of the ovary (Fig. 1A). Each oocyte is enveloped by three layers: ex- ternally, a stratified epithelium of squamous cells; internally, a layer of follicular cells; and between these, a layer of connective tissue "Biology Department, Dalhousie University, Halifax, Nova Scotia, ВЗН 4J1, Canada “Departamento de Oceanografia, Fundacáo Universidade do Rio Grande, Cx. P. 474, Rio Grande, 96200 RS, Brasil 3Departamento de Ciéncias Morfobiológicas, Fundacáo Universidade do Rio Grande, Cx. P. 474, Rio Grande, 96200 RS, Brasil 148 PEREZ, HAIMOVICI & COUSIN TABLE |. Females of Eledone massyae Voss, 1964, and Eledone gaucha Haimovici, 1988, used for histological analyses. Species Number Locality Date E. massyae 5 off Rio Grande Oct. 1988 do Sul state E. massyae 4 off Rio de Nov. 1988 Janeiro state E. gaucha 4 off Rio Grande April 1983 do Sul state E. gaucha 1 à Nov. 1983 DML range Oocyte length (mm) range (mm) Fixative 25.0-65.0 0.7-10.0 Formalin 10% 64.0-73.3 3.8-6.6 Seawater Bouin 25.0-39.0 0.5-5.4 Formalin 10% 36.0 5.8 Formalin 10% with cells of different sizes and shapes, fibro- blasts and blood vessels. The follicular cells proliferate and penetrate the ooplasm, form- ing longitudinal folds that give the oocyte a striped appearance. At final stages of oogen- esis these cells secret the chorion. At the stalked end of the oocyte the chorion be- comes drawn out into a stalk (Fig. 2d). At the animal pole, opposite the stalked end, there is a conical filamentous projection (Fig. 1B). Filament sizes range from twice the length of a 3 mm long oocyte to one-fourth that of the 11 mm long oocytes. Microscopi- cally, the oocyte-surrounding layers are drawn out from the oocyte to form these ex- tensions (Fig. 3D). The external epithelium and the intermediate connective tissue line the filament throughout its length. The follicu- lar cells of the inner layer differentiate and penetrate the filament, filling it as a compact tissue. In the initial stages of maturation (Fig. 3A), follicular cells are dispersed irregularly and are fusiform with elongated nuclei. As maturation advances, these cells become regularly dispersed and cuboidal with large oval nuclei (Fig. 3B). Finally, in advanced stages of maturity, they have smaller nuclei with dense chromatin, which suggests a de- generation of the tissue (Fig. 3C). Oviducal glands In the mid-portion of each oviduct is an oviducal gland structurally divided into two concentric glands around the oviduct and separated by a thin sheet of connective tissue (Fig. 3E). Spermatheca are absent (Fig. 4), as in E. cirrhosa and E. moschata (Froesch & Marthy, 1975). The peripheral gland is formed by groups of concentric cells with basal nuclei and a central lumen; in females close to ma- turity their cytoplasm is densely packed with reddish grains. The central gland is com- posed of 22-23 ducts around the oviduct, each lined by an epithelium with ciliated cells having superficial nuclei and glandular cells having basal nuclei. Spermatozoa were not seen to be associated with the oviducts. Sperm storage and fertilization In females that had mated, spermatangia and free sperm were seen within the ovaries. As many as seven spermatangia were inside an ovary, often attached to the head of the spermatophoric tunic (Fig. 1D). Free sperm masses occurred around the oocytes and were much entangled with the oocyte apical filaments (Fig. 1 С, 1D). Sperm were attached to the filament tips, and apparently penetrated them. Longitudinal sections of apical fila- ments of the oocyte showed hair-like masses of spermatozoa, regularly dispersed and sur- rounded by flattened differentiated follicular cells forming dark purple agglomerates along the filament (Fig. 3 G, H; Fig. 5). During de- velopment, the evolving layers degenerate, thus shortening the filament. The filament-en- closed spermatozoa are thus drawn to the ooplasm, in which fertilization occurs, proba- bly very shortly before spawning (Fig. 2). Oocytes in females of Eledone massyae bearing spermatangia, free sperm and traces of fertilization ranged from 3.0 to 9.0 mm. In E. gaucha they ranged from 0.8 to 5.0 mm. In the former, the largest oocyte, although striped, was 12.0 mm; in the latter, it was 7.5 mm (Perez & Haimovici, MS). DISCUSSION The potential for storage of sperm is known for octopods of the subfamilies Octopodinae and Bathypolypodinae. The sperm released into the oviducts after the “spermatophoric re- SPERM STORAGE IN SOUTH AMERICAN ELEDONIDS 149 FIG. 1. Photomicrographs of ovary and maturing oocytes of Brazilian Eledone species. A. Cluster of ma- turing oocytes. B. General view of ovary. C. Detail of apical filament attachment to free sperm mass. D. Ovary of mated female. Spermatangia, spermatophore tunics and free sperm mass present. Arrow indicates apical filament attached to sperm mass. Scale bar= 1 mm. af, apical filament; s, stalk; sf, spermatophore tunic; sg, spermatangium; sm, sperm mass. 150 PEREZ, HAIMOVICI & COUSIN C. FIG. 2. Schematic diagram of fertilization in Eledone massyae and Eledone gaucha. a. Oocyte in early stage of maturation. Apical filament is almost twice oocyte length. b. Maturing oocyte. Apical filament as long as oocyte and attached to free sperm mass. c. Maturing oocyte. Sperm mass penetrates filament and is surrounded by modified follicular cells. d. Oocyte in advanced stage of maturation. At this stage, apical filament is very short and sperm mass close to ooplasm. Note position at which it will form chorionic stalk. ee, external epithelium; fe, follicular epithelium; mfc, modified folicular cells; о, ooplasm; ое, ovarian epi- thelium; sm, sperm mass. action” (Mann et al., 1970) enter the oviducal glands, where they remain attached to the ep- ithelium of the spermatheca (Froesch & Mar- thy, 1975). Spermatozoa can be maintained as long as ten months, as observed in Bathy- polypus arcticus (O’Dor & Malacaster, 1983); thus, mating can occur long before matura- tion. Mature eggs are fertilized in the lumina of the oviducal glands just before spawning. There is evidence of sperm storage in both European and South American species of Eledone. Aquaria observations of Mediterra- nean E. cirrosa suggested that sperm might be stored for at least six weeks (Mangold et SPERM STORAGE IN SOUTH AMERICAN ELEDONIDS 151 FIG. 3. Photomicrographs of cross-sections of apical filaments, oviducal glands and oocytes of Brazilian Eledone species. A-C. Differentiation of follicular cells at base of apical filament, at successive stages of maturation. A,B, scale bar= 20um; С, scale bar= 100um. D. Oocytes in initial maturation stages showing oocyte surrounding layers forming apical filaments. Scale bar= 300um. E. Transverse section of oviducal glands. Scale bar= 300um. Е. Apical filament tip in contact with free sperm mass. Scale bar= 140um. G. Longitudinal sections of apical filament showing surrounding layers and enclosed sperm mass. Scale bar = 300um. H. Transverse section of apical filament showing three surrounding layers and central spermatozoa. Scale bar = 70mm. cg, central gland; cl, connective layer; ee, external epithelium, fc, follicular cells; fsm, free sperm mass; mfc, modified follicular cells; 00, oocyte; ov, oviduct; pg, peripheral gland; sm, sperm mass. 152 PEREZ, HAIMOVICI & COUSIN pg FIG. 4. Schematic diagram of longitudinal cut of oviducal gland of South American Eledone. c, cen- tral cavity of oviducal gland; cg, central gland; dov, distal oviduct; pg, peripheral gland; pov, proximal oviduct. al., 1971). A maximal lapse of three months between copulation and spawning was esti- mated for E. massyae (Perez 8 Haimovici, MS). Maturing females bearing spermatangia within their ovaries were observed in South American species of Eledone and Mediterra- nean E. cirrosa (Mangold-Wirz, 1963). In pop- ulations of E. cirrosa in the North Sea (Boyle & Knobloch, 1983) and E. moschata in the Mediterranean (Mangold, 1983) mating was assumed to occur just before spawning be- cause females bearing spermatangia within their ovaries were scarce and nearly mature. The absence of spermathecae in the ovi- ducal glands seems to be a consistent char- acteristic of the genus Eledone since it was observed in four species. Spermatophores penetrate the oviducts and oviducal glands reaching the ovarian cavity, in which the sper- matophoric reaction takes place. Sperm masses occur either freely around the oocytes or enclosed in bladders known as spermatangia (Fort, 1937; Mangold-Wirz, 1963) or sperm sacs (Boyle, 1983; Mangold, 1986). In Eledone massyae and Eledone gaucha, the apical filaments provide a site for sperm storage and a fertilization mechanism. Modified follicular cells surrounding the sperm mass inside the filament are supposed to keep spermatozoa viable until oocytes are ripe. Whether the apical-filament mechanism is an adaptation of the entire genus is still unclear. In E. cirrhosa and E. moschata, sites and timing of fertilization, as well as the means to keep sperm viable, are not known. Early descriptions of the reproductive system of E. cirrhosa (Insgrove, 1909; Morales, 1958) do not mention structures similar to the apical filaments. Photographs of ovarian eggs of the same species in Mangold-Wirz (1963: plate II, d, e, f) show delicate expansions at the ani- mal pole of the eggs, although they are quite different from those of the South American species (Fig. 1B). Boyle (pers. comm.) ob- served white masses of sperm attached to the apical end of each egg. Whether these struc- tures indeed form part of the egg-surrounding layers is not known. Comparisons could not be made with the three remaining but poorly- known described species of the genus, E. ca- parti Adam, 1950, E. thysanophora Voss, 1962, and E. nigra (Hoyle, 1910) from the West African coast. In species of Eledone that have been stud- ied, as well as in most Octopodinae and Bathypolypodinae, males mature earlier and remain sexually active for a greater part of life than do females. The ability of females to store sperm means that mating can occur long before spawning. Histological study of E. massyae and E. gaucha shows that at least in the South American eledonids, females can copulate a considerable time before matura- tion and store sperm until fertilization shortly before spawning. The apical filament and the oviducal glands’ spermatheca both allow stor- age of sperm and are important facets of the reproductive strategy of these octopods. There are some slight differences between these adaptations, however. In the Octopodi- nae and Bathypolypodinae, each mature oocyte is fertilized as it descends through the lumen of the oviducal gland (Froesch & Mar- thy, 1975). Spermatozoa stored in the outer parts of the spermathecae will compete to fer- tilize the eggs; the last male to copulate with the female will be most likely to sire the off- spring. In the South American eledonids the sperm of the first male to copulate are likely to fertilize most of the eggs. This fact could ex- plain the difference in body sizes of the sexes of E. massyae at maturity (Perez & Haimovici, MS). If they can mate successfully, young SPERM STORAGE IN SOUTH AMERICAN ELEDONIDS 153 FIG. 5. Longitudinal sections of oocyte apical filament of Eledone massyae showing surrounding layers and enclosed sperm mass. cl, connective layer; ee, external epithelium; mfc, modified follicular cells; sm, sperm mass. Scale bar= 40 um. males need not grow so large or live so long as females. Indirectly this difference in size could be particularly advantageous during the spawning and brooding seasons because males would not be in the same areas at the same time with mature females; this separa- tion would not only reduce intraspecific com- petition for food but also avoid cannibalism on the hatchlings. ACKNOWLEDGMENTS We gratefully acknowledge Paulo A. S. Costa for collection of the Rio de Janeiro specimens and José Milton Andriguetto Fo, Dr. Albino Sakakibara and colleagues of the Laboratory of Genetics of Universidade do Parana for valuable help with the photomi- crography. We also thank Dr. Sigurd v. Bo- letzky and Dr. Peter Boyle for comments on the manuscript and anonymous reviewers for valuable suggestions for the discussion. LITERATURE CITED ADAM, W., 1950, Notes sur les cephalopodes XXII. Deux nouvelles especes de la côte Africaine oc- cidentale. Bulletin, Institut Royal des Sciences Na- turelles de Belgique 26:1-9. BOYLE, P. R., 1983, Eledone cirrhosa. Pp. 365— 386 in: BOYLE, P. R., ed., Cephalopod life cy- cles. Vol |. Academic Press London. BOYLE, P. R. & D. KNOBLOCH, 1983, The female reproductive cycle of Eledone cirrhosa. Journal of the Marine Biological Association of the United Kingdom, 63:71-83. FORT, G., 1937, Le spermatophore des cephalo- podes. Etude du spermatophore d'Eledone cir- rhosa (Lamarck, 1799). Bulletin Biologique de la France et de la Belgique. 71:357-373. FROESCH, D. & H.-J. MARTHY, 1975, The struc- ture and function of the oviducal gland in octo- pods (Cephalopoda). Proceedings of the Royal Society, Series B, 188:95-101. GABE, N., 1968, Techniques histologiques. Mas- son et Cie, Paris, 1113 pp. HAIMOVICI, M., 1988, Eledone gaucha, a new spe- cies of eledonid octopod (Cephalopoda: Octopo- didae) from southern Brazil. Nautilus 102(2):82— 87. 154 PEREZ, HAIMOVICI & COUSIN HAIMOVICI, M. & J. M. ANDRIGUETTO Fo, 1986, Cefalopodes costeiros capturados na pesca de arrasto do litoral Sul do Brasil. Arquivos de Bio- logia e Tecnologia, 29(3):473—495. HOYLE, W. E., 1910, Mollusca: Cephalopoda. Pp. 261-268 in SCHULTZE, Zoologische und An- thropologische Ergebnisse einer Forschungsre- ise im westlichen und zentralen Sudafrika, 1903— 1905, Band 4. Gustav Fischer, Jena. INSGROVE,A., 1909, Eledone. Liverpool Marine Biological Committee Memoirs, 18:105 pp. MANN, T., A. W. MARTIN, jr. & J. B. THIERSCH, 1970, Male reproductive tract, spermatophores and spermatophoric reaction in the giant octopus of the North Pacific, Octopus dofleini martini. Proceedings of the Royal Society, Series B, 175: 31-61. MANGOLD-WIRZ, K., 1963, Biologie des ceph- alopodes benthiques et nectoniques de la Mer Catalane. Vie et Milieu, 13 (suppl.):1-285. MANGOLD, K., 1983, Eledone moschata. Pp. 387— 400 in: BOYLE, P. R., ed., Cephalopod life cy- cles. Vol. |. Academic Press, London. MANGOLD, K., 1986, Reproduction. Pp. 157-200 in: BOYLE, P. R., ed., Cephalopod life cycles. Vol. Il. Academic Press, London. MANGOLD, K., S. v. BOLETZKY, D. FROESCH, 1971, Reproductive biology and embryonic de- velopment of Eledone cirrhosa (Cephalopoda: Octopoda). Marine Biology, 8:109-117. MORALES, E., 1958, Sobre la morfologia del aparato genital de Eledone aldrovandi (Rafin.) = Eledone cirrhosa (Lamarck). Commission Infor- mational pour l'Exploration Scientifique de la Mer Méditerranée, Rapports et Procès-Verbaux des Reunions, 14:389-394, 2 figs. О’ООВ, В. К. & Е. G. MALACASTER, 1983, Bathypolypus arcticus. Pp. 401—410. т: BOYLE, P. R., ed., Cephalopod life cycles. Vol |. Aca- demic Press, London. PEREZ, А. А.Р. & M. HAIMOVICI, 1990, Maturation and reproductive cycle of Eledone massyae (Cephalopoda: Octopodidae) in southern Brazil. Bulletin of Marine Sciences, in press. PETERSEN, R. P., 1959, The anatomy and histol- ogy of the reproductive systems of Octopus bi- maculoides. Journal of Morphology, 104, 61-82. VOSS, G., 1962, South African cephalopods. Transactions of the Royal Society of South Africa 36:245-272. VOSS, G., 1964, A note on some cephalopods from Brazil with a description of a new species of oc- topod: Eledone massyae. Bulletin of Marine Sci- ence of the Gulf and Caribbean 14:511-516. WELLS, M. J. & J. WELLS, 1977, Cephalopoda: Octopoda. Pp. 291-336 in: GIESE, A. C. & J. S. PEARSE, eds., Reproduction of marine inverte- brates Vol. 4. Academic Press, London. Revised Ms. accepted 19 March 1990 MALACOLOGIA, 1990, 32(1): 155-193 PREDATORY ECOLOGY OF NATICID GASTROPODS WITH A REVIEW OF SHELL BORING PREDATION Alan R. Kabat Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02138 U.S.A. ABSTRACT This review provides a critical synthesis and analysis of the extensive body of knowledge of predation by the Naticidae, a cosmopolitan family of burrowing marine gastropods. First, the diversity of shell boring predation is reviewed and documented for ten taxa (nine marine, one terrestrial), in order to facilitate comparative analyses. These predators are: Naticidae, Muri- cidae, Cassidae and Capulidae (Gastropoda, Prosobranchia); Okadaia (Gastropoda, Opistho- branchia); Aegopinella (Gastropoda, Pulmonata); Octopus (Cephalopoda); Pseudostylochus (Turbellaria); Nematoda; and Asemichthys (Pisces). Second, the proximate mechanisms of naticid predation are explicated. Third, the known prey of naticids are tabulated; over 80 families of gastropods and bivalves are subject to naticid predation which is essentially restricted to soft-substrate prey taxa. Fourth, the fossil record of naticid predation is summarized; this pre- dation dates from the Cretaceous, with a possible boring “experiment” in the early Triassic. The diagnostic countersunk naticid boreholes are recognizable in fossil and Recent faunas; naticid predation is a readily documented aspect of the otherwise elusive soft-bottom food web. Fifth, the studies on physiology and ecology of naticid predation are integrated into a conceptual framework. These aspects of naticid predation (energy budgets, prey size and species choice, unsuccessful predation) indicate a successful albeit rather stereotyped mode of predation. The macroevolutionary implications (escalation, or “arms races”) suggest generalized predator-prey coevolution. Key words: Naticidae, predation, boring. DIVERSITY OF BORING PREDATION In the Mollusca, many of the post-Paleozoic Gastropoda are predators, and an extensive body of research has developed around var- ious aspects of predation by mollusks (Kohn, 1983). Most of these studies treat Recent mol- lusks, including the community ecology, be- havior and physiology of predation. Other, more restricted, studies on fossils analyzed those elements of predation revealed by fossil shells (boreholes and other signs of shell dam- age and repair) (Kohn, 1985). Among the predatory gastropods, several families include shell borers which excavate a hole in the prey shell to provide access to the prey flesh. Ear- lier overviews of boring by gastropods by Fis- cher (1922, 1966), Carriker (1961), Fatton & Roger (1968), Sohl (1969), Bishop (1975), Boucot (1981: 200 ff.), Bromley (1981), Ben- ton (1986) and Vermeij (1987) have зитта- rized some of this research. More general re- views of gastropod feeding biology were provided by Ankel (1938), Fretter & Graham (1962: 240-262), Taylor et al. (1980), Kohn (1983) and Tsikhon-Lukanina (1987). Inevita- 155 bly, numerous previous studies have been overlooked by subsequent researchers; this paper seeks to provide some unity and a co- herent framework to the body of knowledge of shell boring predation by gastropods of the family Naticidae. The objectives of this paper are: (1) to doc- ument the diversity of shell boring predation and related phenomena; (2) to summarize the mechanical or proximate aspects of naticid prey capture and boring; (3) to tabulate the known naticid prey taxa in order to indicate the prey diversity in relation to the overall di- versity of marine mollusks; (4) to review the fossil record of naticid predation in the Meso- zoic and Cenozoic; and (5) to integrate and synthesize the ecological and evolutionary aspects of naticid predation into a broader conceptual framework. The diversity of molluscan shell boring predators is briefly reviewed, in order to be able to distinguish amongst the traces of pre- dation left by the various taxonomic groups of predators. Based on this review, it is obvious that predation by boring in taxa other than the Naticidae and Muricidae is seldom studied. 156 KABAT Shell breaking predators, particularly crusta- ceans and fish, represent an entire field of study in themselves; valuable reviews are provided by Vermeij (1978, 1983c). Not men- tioned herein are the diverse groups of sym- biotic (non-predatory) epibionts and endolithic shell burrowers, such as certain cyanobacte- ria, fungi, algae, sponges, polychaetes, sip- unculans, barnacles, lithophagid and pho- ladid bivalves, brachiopods and bryozoans (reviewed by Boekschoten, 1966, and the 1969 American Zoologist [vol. 9, #3] sympo- sium on calcibiocavitology). Generally speak- ing, the latter “Боге holes” can be recognized by their large number on a single shell, the lack of complete penetration, and their obvi- ous burrowing aspect. An exception is the pedicle attachment scar of brachiopods, which may show complete penetration in the host shell (often another brachiopod); these scars or holes (common in the Paleozoic) could be confused with those of other, un- known, Paleozoic borers. Within the Prosobranchia, there are two major groups of shell boring (or drilling) pred- ators, the Naticidae (Mesogastropoda) and the Muricidae (Neogastropoda). | have sum- marized only a small part of the extensive re- search on muricid predation, and have limited it to the principal means of distinguishing their predation from naticid predation. A compre- hensive review of muricid predation will be most useful but remains to be written. An heuristic definition of gastropod bore- holes was provided by Carriker & Yochelson (1968: 2) as “an excavation of characteristic size and form drilled by a predatory snail in the calcareous exoskeleton of a prey organ- ism by means of chemical weakening and radular abrasion of the prey shell for the pur- poses of obtaining food.” Refinements of this definition were provided by Chatterton & Whitehead (1987: 68). Specifically, naticid boreholes are parabolic holes (straight or oblique), formally referred to as a “truncated spherical paraboloid”; the borehole is coun- tersunk (i.e., the enlarged outer margin is beveled or tapered, forming a chamfer) (Fig. 1), and incomplete naticid boreholes are characterized by a prominent central boss (rounded elevation) on the bottom surface (Fig. 2). The Muricoidea (Neogastropoda) is a di- verse group containing a variety of eclectic predators, including shell borers, carrion feeders, and other specialized predators, as well as several herbivores. The majority of muricids are shell borers and are distin- guished by the presence of the accessory boring organ (ABO) in the sole of the foot. The muricid borehole is cylindrical, with nearly straight edges (Fig. 3); the naticid borehole, in contrast, has a more parabolic form and bev- eled edges. Much of the research carried out on the oyster drill, Urosalpinx cinerea, and other shellish pests by Carriker, along with research on other muricoideans by Taylor, has greatly added to our knowledge of the feeding biology of this superfamily (Carriker, 1981; Taylor et al., 1980). The Nassariidae, or mudsnails, are carniv- orous or Scavenging members of the Neogas- tropoda. Fischer (1962a: 75) and Reyment (1966: 34) stated in passing that nassariids are shell borers. Subsequently, Ипа (1987: 23) also mentioned that they probably are shell borers. This appears to be mistaken, as no documentation has ever been provided for boring by mudsnails. Similarly, Stevanovic (1950) thought that the boreholes in mollusks from the Serbian Upper Miocene were caused by the hydrobiid gastropod Sandria [= Pseudamnicola] atava; Шпа (1987: 25) re- jected this conclusion and attributed the bore- holes to the naticid Euspira helicina. The Cassidae (Tonnoidea, Mesogas- tropoda) are important predators of tropical echinoids, using sulfuric acid from their pro- boscis gland along with the radula to pene- trate the echinoid test (by cutting out a disc, rather than drilling a hole) (Fig. 4). Hughes & Hughes (1981) provided a comprehensive re- view of the biology and ecology of cassid pre- dation, and pointed out that other tonnoide- ans which feed on mollusks do so without boring (i.e., by penetrating between the gas- tropod operculum and shell, or between the valves of a clam). The numerous unique as- pects of cassid predation clearly suggest an independent origin from that of naticids or mu- ricids. Tertiary echinoids with cassid holes were documented by Sohl (1969: figs. 7-8) and Beu et al. (1972). The Capulidae (Mesogastropoda) are spe- cialized ectoparasitic symbionts of mollusks and echinoderms. They are known to drill holes into the shell of their mollusk host for the purpose of obtaining small amounts of flu- ids from the host's feeding current for nutri- tion. Matsukuma (1978) reviewed shell boring by capulids and recorded several fossil records of capulid boreholes: these are sharp-sided cylindrical holes, similar to those produced by muricids. However, capulid NATICID PREDATION 157 boreholes can be recognized by the sur- rounding attachment scar on the host shell, where the edge of the capulid shell had slightly worn away the host shell (Figs. 5, 6). In the Opisthobranchia, the nudibranch Okadaia elegans (Vayssiereidae) is known to drill holes into the calcareous tubes of serpulid and spirorbid polychaete annelids (Young, 1969). These minute bore holes (Figs. 7, 8) are similar in shape to those of muricids; however, muricids are not known to prey on these poly- chaetes, whereas Okadaia does not feed on mollusks. In the Pulmonata, the terrestrial Ae- gopinella (Zonitidae) are known as shell- boring predators of other gastropods. Mordan (1977: 65) described predation by A. nitidula, in which prey snails (typically other zonitids) are first attacked through the aperture (fol- lowed by consumption of the head-foot); sub- sequently, a quite irregular hole on the umbil- ical surface of the last whorl is bored (Fig. 11), allowing the predator access to the rest of the prey flesh. Pulmonate shell boring may have evolved from simple shell “radulation,” or the scraping of the outer surface of prey shells (Mordan, 1977: 70-1). In the Cephalopoda, the octopuses are shell boring predators of a variety of marine shelled mollusks (Ambrose, 1986; Nixon & Maconnachie, 1988). Octopus boreholes can be recognized by their distinctly irregular or oval (but not circular) outline and their ex- tremely small inner borehole diameter, in con- trast to the large outer borehole diameter (Ambrose et al., 1988) (Fig. 9). Furthermore, the purpose of the hole is solely for the injec- tion of venom to relax or kill the prey, which is then extracted through the aperture or valve opening. One problem with the analysis of oc- topus predation is that octopuses frequently break open the shell or otherwise capture the prey without drilling the shell (Ambrose, 1986: table 1). Hence, octopus boreholes represent only part of their trophic activities. Probable octopus boreholes from the Pliocene were re- ported by Robba & Ostinelli (1975: 338-344). An unusual polyclad turbellarian flatworm, Pseudstylochus ostreophagus, is known to bore a hole in the shell of juvenile oysters (spat), effecting separation (or relaxation) of the prey adductor muscle, which causes the shell valves to gape, facilitating entry of the predator between the valves leading to prey consumption. The irregular oval holes are quite small (typically 150 х 190 шт); further details are provided by Woelke (1957). Many polyclads are known predators of mollusks, but shell boring has not been shown for other species (Galleni et al., 1980: table 1). Nematode worms are known to prey upon the microscopic Foraminifera (Granuloreticu- losa), boring one or more holes in the test, entering the chamber, and slowly consuming the prey. In the past, such holes were thought to be produced by juvenile gastropods (Livan, 1937: 149; Saidova & Beklemishev, 1953; but see Fischer, 1962a: 70-1); however, their size (less than 60 um in diameter) is smaller than those produced by newly hatched pred- atory gastropods (boreholes 100-160 um in diameter). Sliter (1971) found that nematodes were responsible for this predation, and illus- trated the various borehole morphologies (ir- regular oval to bevelled round). Subse- quently, Arnold et al. (1985) described even larger boreholes (10-125 um in diameter) in Foraminifera from the Galapagos hydrother- mal vent mounds, and concluded that naticid gastropods were probably responsible (de- spite the fact that naticids are not known from such habitats). These are also likely to be the product of nematodes. Decapod crustacean predation on mollusks is well known, and typically takes the form of shell breaking or cracking followed by extrac- tion of the prey. Occasionally, the prey is able to escape and repair the broken shell, leaving diagnostic shell repair scars (Fig. 10) as a sign of unsuccessful predation (Schafer, 1972: 408-411; Vale & Rex, 1988). Usually, the shell is fragmented; in a few cases, the predator may only effect a smaller, very irreg- ular hole in the otherwise intact prey shell. Papp et al. (1947), provided an extensive dis- cussion of crab predation; subsequent au- thors have documented the presence of shell fragments or subsequent shell repair attribut- able to predation attempts (successful and unsuccessful, respectively) by crabs and other decapods. However, because of frag- mentation, one cannot account for all the re- mains of such predation. Shell fragmentation may also occur because of wave action; Cadée (1968: 87-88) noted that this is usu- ally accompanied by signs of abrasion and fragmentation in subtidal shells is probably re- stricted to predation. A most novel recent discovery is that of Norton (1988) who documented holes made in gastropod shells by a marine cottid fish, Asemichthys taylori. This species has a spe- cial set of vomeral teeth that are used to punch a hole or series of holes in the prey KABAT 158 FIGS. 1-6. NATICID PREDATION 159 shell (Fig. 12). The holes (which are not truly “bored”) allow the entry of digestive enzymes while the shell is in the digestive tract of the fish. Shells which are unpunched generally pass through undigested and emerge alive (except, of course, for limpets which have an exposed ventral aspect). Similar rows of punctures in Paleozoic brachiopods, conulari- ids and nautiloids were attributed to shark predation (Mapes et al., 1989, and references therein). Shell boring or burrowing is little Known in the freshwater environment, with a few ex- ceptions, such as the endolithic burrowing polychaete Caobangia (Jones, 1969). Re- cently, the Soviet paleontologist Шпа (1987) found shells of Unio and Viviparus (fresh- water mollusks) with regular, round boreholes, one to four per shell, with an outer diameter up to 2 mm and an inner diameter from 1.0 to 1.5 mm. llina (1987: 29) suggested that these holes were made Бу“... ants that for reasons not yet known use their formic acid to etch perforations in the shells of molluscs . . .”; Е. O. Wilson (in litt.) stated that “| don't know of any documented cases of ants boring mol- lusk shells, and | doubt very much if they do ... It’s hard to imagine their cutting through a clam shell even with the aid of formic acid.” In any case, since ants are terrestrial, it seems unlikely that these freshwater mollusks were drilled and consumed in situ; it is more likely that empty shells were washed ashore and (post-mortem) excavated by some other or- ganism, perhaps for a refuge. Further study is clearly indicated. Finally, there is an extensive and scattered literature on shell borings in Paleozoic fossils. While providing lengthy descriptions of the bore holes and of the prey organisms, these studies generally have not elucidated the na- ture of the predator (known predatory gastro- pods did not evolve until the Mesozoic). Car- riker & Yochelson (1968) suggested that these holes were made by soft-bodied, ses- sile, non-predatory organisms of unknown taxonomic affinity (this hypothesis is essen- tially non-testable!); Sohl (1969: 728-9) fur- ther discussed this problem. More recently, Smith et al. (1985) and Chatterton & White- head (1987) reviewed the Paleozoic bore- holes and suggested that they were, indeed, predatory in origin although the identity of the predator remains unknown. Vermeij (1987: 176-7) hypothesized that ectoparasitic pla- tyceratid gastropods (ecologically analogous to capulids) were the Paleozoic borers. The remainder of this paper is restricted to analysis of predation by naticids. The preced- ing review of the diversity of shell borers in- dicates that predation by boring has evolved independently in a number of taxa; any simi- larities are undoubtedly cases of convergent evolution. The following section, on the prox- imate mechanisms, demonstrates the numer- Ous unique (derived) aspects of naticid pre- dation, and should be compared with what is known for other shell-boring taxa. MECHANISMS OF NATICID PREDATION For a detailed review and critique of the previous morphological studies on naticid feeding mechanisms, see Carriker (1981). Essentially, early controversies concerning naticid boring involved the means of boring: i.e., was it solely by mechanical means (rad- ular rasping of the prey shell) or did it also involve chemical action (acid secretion). It was the careful work of Carriker and col- leagues (Carriker, 1981) which demonstrated that the latter hypothesis is the case for nati- cids and muricids. FIG. 1. Naticid bore hole (complete) in valve of Dosinia discus (Reeve, 1850) [Cocoa Beach, Florida; MCZ 145801]. Shell dimensions 52.7 mm x 48.8 mm; outer bore hole diameter 5.2 mm; inner borehole diameter 2.8 mm. FIG. 2. Naticid bore hole (incomplete) in valve of Dosinia concentrica (Born, 1778) [Punta Guanajibo, Puerto Rico; MCZ 212607]. Shell dimensions 55.7 mm x 52.3 mm; outer bore hole diameter 2.7 mm. FIG. 3. Muricid bore holes [presumably by Urosalpinx or Eupleura] in adjacent valves of Crassostrea virginica (Gmelin, 1791) [Stono River, South Carolina; MCZ 226338]. Shell lengths 86 mm and 65 mm; outer bore hole diameter 2.5 mm; inner bore hole diameter 2.3 mm. FIG. 4. Cassid bore hole in Cassidulus pacificus (A. Agassiz, 1863) [Punta Pescadero, Baja California Sur, Mexico; USNM 32907]. Test dimensions 34.9 mm x 28.9 mm, height 16.1 mm; bore hole diameter 2.1 mm. FIG. 5, 6. Capulus danieli (Crosse, 1858) bore hole in valve of Comptopallium vexillum (Reeve, 1853) [Noumea, New Caledonia; ANSP 272383]. Scallop shell dimensions 32.5 mm x 29.5 mm; outer bore hole diameter 1.75 mm; capulid shell dimensions 4.9 mm x 15.0 mm. 160 KABAT 1: E 1 ee dé sd à der ASI éd à бита * FIG. 7, 8. Okadaia elegans Baba, 1930 [Nudibranchia] bore hole in tube of spirorbid polychaete [Oahu, Hawaii]. Bore hole diameter ca. 115 рт; worm tube diameter at bore hole ca. 300 jm. SEM photographs courtesy J. D. Taylor. [Magnifications; Figure 7 at 110 x; Figure 8 at 350 x]. FIG. 9. Octopus bimaculatus Verrill, 1883 bore hole in Ventricolaria fordi (Yates, 1890) [Anacapa Island, off Ventura, California; MCZ 298337]. Shell dimensions 33.7 mm х 31.2 mm; outer bore hole diameter 2.2 mm, inner bore hole diameter 0.6 mm. Specimen courtesy R. F. Ambrose. FIG. 10. Unsuccessful crustacean predation: shell repair scars in Architectonica nobilis Roding, 1798 [Puerto Plata, Dominican Republic; MCZ 106825]. Shell dimensions 8.8 mm x 17.5 mm. A fundamental and little studied problem “chemical odors” by the osphradium) is typi- concerns the methods by which naticids de- cally the initial mechanism for determining the tect their prey. For many predatory gastro- presence and direction of potential prey pods, chemoreception (detection of prey (Kohn, 1961; Croll, 1983). With infaunal nati- NATICID PREDATION 161 cids, the sediment habitat not only decreases the diffusion rate of chemical substances, but also may perturb its directionality; hence nat- icids may forage with the siphon extending to the surface where diffusion is more direct and rapid. Kitching & Pearson (1981) found that the Australian “Polinices” [= Conuber] incei responded to artificial sound waves directed through the substrate, which presumably mimicked the vibration of burrowing prey. Mechanoreception may well serve as an ad- ditional prey detection mechanism for the nat- icids. Regardless of how the prey are initially de- tected, one can analyze the behavioral per- spective: namely, recognition of suitable prey serves as a releasing mechanism which elic- its a stereotyped sequence of behaviors.{= fixed action patterns] (Ansell, 1960). Naticids have been little studied with respect to clas- sical ethological principles, probably because most activity occurs while they are buried. Edwards (1969), Schafer (1972: 242-3), Stenzler & Atema (1977) and Hughes (1985) discussed the sequence of prey capture events: the prey is detected, evaluated, seized, covered and immobilized with copious pedal mucus, wrapped in the dilated foot of the naticid, dragged for some distance, and finally carried deep into the sand for com- mencement of boring. The mechanism of naticid boring involves a complex sequence of events. There is alter- nate application of the predator’s radula and accessory boring organ (ABO) to the bore hole site on the prey shell. The ABO is found on the ventral surface of the proboscis in nat- icids (but in the sole of the muricid foot); the two ABO types represent a case of conver- gent evolution and no homologues in other taxa are known. The ABO histology was de- scribed by Bernard & Bagshaw (1969), who characterized it as a “fungiform papilla” con- taining numerous epithelial secretory cells. The biochemistry of ABO secretions was dis- cussed by Carriker & Williams (1978). The ABO secretes a complex mixture of pre- sumed enzymes, chelators, and inorganic acid (HCl) in a saline, hypertonic solution which effects dissolution of the prey shell layers (both calcareous and organic matrix). During boring, the proboscis becomes engorged, everting both the radula and the ABO. The radula is protracted and scrapes at the sur- face of the bore hole. The proboscis is rotated in 90° sectors and the scraping is from the outer edge to the center, resulting in the di- agnostic boss in the center of incomplete bore holes (Ziegelmeier, 1954: fig. 7; Carriker, 1981: 410). The prey shell fragments are in- gested but subsequently excreted without di- gestion (Carriker, 1981: 411). The prey tissue is ingested by the proboscis through the bore- hole; Reid & Gustafson (1989) determined that external digestion does not occur. Most studies have documented that natic- ids capture and consume their prey entirely within the sediment. Previous reports of nati- cid predation on the sediment surface were usually a result of aquaria studies wherein the sediment depth was too shallow and conse- quently abnormal behavior patterns were manifested. Recently, field observations of Natica gualteriana from the Philippines (Savazzi & Reyment, 1989) have docu- mented that this species was capable of searching for and capturing its prey on sand bars at low tide (i.e., while exposed to the air). Further study is needed to ascertain whether other naticid species can also feed on the sediment surface (exposed or subtidally). As such, this would result in greater competitive interactions between those naticids and the epifaunal muricids. For temperate and boreal naticids, the wa- ter temperature can determine the active pe- riods of feeding. Hanks (1953) showed that the northwest Atlantic Neverita duplicata and Euspira heros had a marked temperature- dependence, with no feeding at temperatures below 5°C and 2°C, respectively. Similarly, salinity (brackish or estuarine waters) also af- fects feeding rates; these two naticid species did not feed at artificial salinities below 10% (normal seawater about 35%o). For the calculation of energy budgets, the rates of shell boring and of prey tissue inges- tion must be determined. Determining the time for infaunal prey capture and subjugation would be extremely difficult and yields vari- able results (here, especially, aquaria studies would be of little value). In general, the rela- tive sizes of predator and prey (both dimen- sional and shell thickness) must be taken into account; there will undoubtedly be great inter- specific variation in these rates. Ziegelmeier (1954) found a boring rate of 0.6 mm/day, or 0.025 mm/hour by Euspira nitida. Similarly, Kitchell et al. (1981: fig. 2) observed that in Neverita duplicata preying on various bi- valves, the boring rate was a nearly constant 0.0223 mm/hour, regardless of prey species, predator size, or elapsed time. Bayliss (1986) noted that for Mya and Spisula prey, Euspira 162 KABAT FIGS 11 12: NATICID PREDATION 163 alderi bored at an average rate of 0.0097 mm per hour; the prey tissue was consumed in 19.5 hours (M. arenaria), 21.5 hours (S. sub- truncata), or 60 hours (S. elliptica). For the analysis of naticid boring predation, especially in fossils, the primary source of data for the predator is the size of the bore- hole. Kitchell et al. (1981: 539, fig. 4) proved that the borehole diameter is constant for a given predator size, regardless of the prey size. Most studies have used the inner bore- hole diameter as the basis for analysis, as this represents the size of the predator's probos- cis. Wiltse (1980a: 189, fig. 1) used the diam- eter “. . . at the junction of the prismatic and nacreous shell layers”; this does not facilitate comparisons with other prey taxa (given that the depth of this junction is not constant for'all taxa). Usually, the outer borehole diameter is also directly proportional to the predator size; but due to the chamfered borehole edge, it is more difficult to measure. However, for cor- bulid bivalve prey, there is an exception in that the outer borehole is disproportionately much larger than the inner borehole; this re- flects the conchiolin layer in the prey shell (De Cauwer, 1985). Arua & Hoque (1989b), based solely on analysis of outer borehole sizes, concluded that the opening was more oval than circular; regrettably, their data on inner borehole sizes was not presented. It is unfortunate that a recent paleoecolog- ical study (Arua & Hoque, 1989a, 1989c) seems to have confused several muricid boreholes with those of naticids, and vice versa. Their “hole types” A, B and D were claimedto be muricid; C, EandF asnaticid. The authors had stated that naticid boreholes are countersunk, with tapering sides, and incom- plete ones have a central boss; yet, they claimed that their “hole type E,” which lacks а boss and has vertical sides, was naticid! My re-analysis of their descriptions leads to the conclusion that their “hole types” E and (maybe) A are muricid; whereas B, C, D, and F are naticid. This confusion undoubtedly has arisen in other studies, and should be consid- ered when interpreting community-level anal- yses (because the variety of observed bore- holes are rarely illustrated therein). A more general aspect of naticid predation is the suitability of the substrate for naticid locomotion. It is well Known that naticids are restricted to infaunal sedimentary habitats; it is less appreciated that extremely fine or smooth grained substrates (silt-mud-clay) are precluded because they are too tightly packed to burrow through readily, in contrast to coarser sand substrates (Yochelson et al., 1983: 12; Maxwell, 1988: 31). Vermeij (1980) and Ansell & Morton (1987) discovered that the tropical Polinices “ш- midus” [= mammilla], after wrapping its prey in a mucus coat within the foot, retained the prey until suffocation and gaping occurred. Subsequently, the prey was consumed with- out boring. Ansell & Morton (1987: 117) sug- gested that a “narcotizing toxin” may play а role in causing prey gaping, such as by thai- dine gastropods preying on barnacles. This was questioned by Reid & Gustafson (1989), who determined that prey suffocation alone caused shell gaping. The ecological and ev- olutionary implications of this non-boring pre- dation will be discussed below. A preposterous view of the evolution of nat- icid feeding mechanisms was advanced by Stafford (1988), who claimed that naticids Originated at Ediacaran-Cambrian times (570 million years ago), as Swimming filter feeders, and gradually shifted to benthic feeding en- tailing eversion of the stomach (as in aster- oids) to effect external digestion of the prey. To summarize the proximate mechanisms of naticid shell boring: (a) Prey are detected by chemoreception using the osphradium, though mechanoreception may also play a role. (b) Suitable prey are seized, covered with pedal mucus and wrapped in the foot. (c) The proboscoideal acid-enzyme secretory ac- cessory boring organ (ABO) together with the radula is used to excavate a countersunk (bevelled) hole in the prey shell, and the prey tissues are extracted through this borehole. The size of the borehole (inner diameter) is FIG. 11. Aegopinella nitidula (Draparnaud, 1805) [Zonitidae] bore holes in (left) A. pura (Alder, 1830) [bore hole 1.5 mm x 0.7 mm] and (right) A. nitidula [bore hole 1.6 mm x 1.0 mm] [Monks Wood, England]. Photographic negative courtesy P. B. Mordan; original in the Biological Journal of the Linnean Society (1977), 9: 65, plate 1A. [Copyright 1977 by The Linnean Society of London]. FIG. 12. Asemichthys taylori Gilbert, 1912 [Pisces], punched holes in Margarita sp. [San Juan Island, Washington]. Shell width ca. 2 mm. Maximum hole diameters: 165 рт; 350 um; 380 um. SEM negative courtesy S. F. Norton; original in Science (1988), 241(1): cover. [Copyright 1988 by the AAAS]. 164 KABAT positively correlated with predator size. (d) Some tropical Indo-Pacific naticids are able to immobilize their bivalve prey until shell gaping occurs, allowing direct access to the prey tis- sues; thus, no borehole need be made. THE PREY OF NATICIDS The Appendix tabulates the known prey of naticid gastropods (fossil and Recent). The genera are arranged alphabetically by family; the reference is given in brackets following the species name [n.b. this is not the author of the taxon!]; some species were reported in several studies but only one such is indicated herein. This compilation includes an unpub- lished data set on Fijian Pleistocene mollusks collected by A. J. Kohn. | have corrected for obvious changes in generic nomenclature; species names were not given for several re- ports, as indicated by an asterisk. Many records of naticid predation are purely inci- dental or even parenthetical (e.g., “Бу the way, some of the shells of X were bored .. .”), which does not facilitate critical comparative analyses. Generally, the records herein are limited to ecological or paleoecological studies empha- sizing predation; it is too time-consuming to search through the general systematic and faunistic literature for scattered records of naticid predation (which are usually not thor- oughly documented in such papers). Need- less to say, aquarium studies of naticid feed- ing should be based on prey found in the same habitat as naticids. Unfortunately, some papers (Hayasaka, 1933; Fischer, 1966; Sander & Lalli, 1982; and De Cauwer, 1985) provided lists of taxa with gastropod bore- holes, but without specifying naticid or muricid boreholes. Nonetheless, based on the avail- able data, it appears that naticids prey on the majority of benthic, infaunal shelled mollusks. A. Class Gastropoda Since most archaeogastropods (e.g. Pleu- rotomaroidea, Fissurelloidea and Pate!loidea) are rocky-habitat dwellers, they are not sub- ject to naticid predation. Beebe (1932: 212, fig.) made the unusual statement that, in Ber- muda, Natica canrena preyed upon the rocky intertidal limpet Fissurella barbadensis, leav- ing a diagnostic borehole in the limpet shell. My subsequent re-analysis of this situation re- veals that Beebe had confounded the excur- rent slit or foramen (‘keyhole’) of these lim- pets with naticid boreholes and erroneously assumed that naticid predation was responsi- ble for the limpet keyholes! Many of the soft-substrate taxa in the Me- sogastropoda are subject to naticid preda- tion. Not included herein are the extensive re- ports of confamilial predation on naticids themselves (sometimes referred to as “сап- nibalism”) (Kabat & Kohn, 1986). Reports of naticid boreholes in Xenophora [Xeno- phoridae] and Lamellaria [Lamellariidae] by Adegoke & Tevesz (1974) are questionable, given the epifaunal habitat of these taxa. While it may appear that neogastropod gen- era are more frequent in the list, this could be a taxonomic artifact of generic lumping vs. splitting. Most of the neogastropods are active pred- ators themselves; the epifaunal and rocky- habitat species generally escape naticid pre- dation. It is entirely possible that some of these records, especially of Muricidae, are of misidentified muricid boreholes. B. Class Bivalvia Most infaunal bivalves are subject to naticid predation. In particular, the venerids, tellinids, and lucinids (the last two often with relatively thin or little-sculptured shells) are frequent victims. The infaunal Solemyidae live in re- ducing sediments where naticids are not found. Bivalve taxa that are in rocky habitats, epifaunal byssate or cemented (Dimyoidea, Plicatuloidea, Anomioidea, Chamoidea, Lep- tonoidea and Cyamioidea) effectively escape naticid predation; the few cases of naticid boreholes in the Pterioidea, Limoidea, Os- treoidea and Pectinoidea are unusual excep- tions. Those that are rock or wood burrowers (Lithophagidae, Gastrochaenoidea and Pho- ladoidea) are also inaccessible to naticids. The Pinnoidea and Tridacnoidea have en- crusted and sculptured shells; the Glos- soidea, Clavagelloidea and Pholadomyoidea are too rare to have been reported in this con- text: C. Class Scaphopoda A thorough review of naticid predation on scaphopods by Yochelson et al. (1983) found that scaphopods were the occasional prey of naticids from the Late Cretaceous to the Re- cent. Usually, there is moderate stereotypy of borehole siting, with most being laterodorsal NATICID PREDATION 165 and about midway along the shell axis. It was found that coarse-ribbed scaphopods (which live in coarse sediments) were much more likely to be bored; those with smooth (or no) ribs, living in fine sediments, escaped naticid predation by virtue of their habitat which is inimical to active naticid burrowing (Yoch- elson et al., 1983). D. Other Mollusk classes Naticid predation has not been recorded on the Aplacophora, Monoplacophora, Polypla- cophora, or the Cephalopoda. The shell-less Aplacophora would not leave traces of naticid predation. The Monoplacophora (clay-mud habitats) and the Polyplacophora (rocky hab- itats) are usually not encountered by naticids. The epifaunal and pelagic cephalopods, pred- ators themselves, are unlikely to be captured by the slower naticids. E. Polychaetes Paine (1963: 69) found one specimen of Neverita duplicata from Florida that fed on the polychaete Owenia fusiformis; this is the only known record of naticids preying on annelids. It is not clear whether this represents normal behavior or a single, aberrant event. F. Crustaceans Significantly, Gonor (1965: 229) found that naticids would not feed on hermit crab occu- pied shells. This is of importance as it indi- cates that not only can naticids recognize such “prey” (of course, the active epibenthal hermit crabs may be beyond the range of nat- icids), but also that boreholes found in shells with recognizable signs of hermit crab occu- pancy (worn lips, unrepaired damage, epi- bionts) were the cause of the gastropod mor- tality, freeing the shell for hermit crab use. Ostracods represent a potentially important prey source for juvenile naticids. Livan (1937) and Reyment (1966, 1967) attributed numer- ous boreholes in ostracods to predatory gastropods. Maddocks (1988) reviewed the various types of boreholes in ostracods (Cre- taceous to Holocene of Texas) and concluded that juvenile naticids were responsible for most. However, because of the thin ostracod test, there is a wide variety of “holes” and it is difficult to attribute them to known causes (Reyment et al., 1987). G. Brachiopods Most articulate brachiopods live in rocky habitats (rock walls or boulder grounds), thereby escaping naticid predation because of habitat incompatibility. However, Witman & Cooper (1983: 71, figs. 8c—d) reported “nati- cid” boreholes in values of Terebratulina sep- tentrionalis from the Gulf of Maine, which they attributed to either Natica clausa or N. pusilla. The illustrated boreholes resemble those of muricids (albeit with slightly sloping sides); further study is recommended. H. Pisces Perry (1940: 116) reported that the tropical western Atlantic Naticarius canrena ‘preys on bivalves and has been seen to devour dead fish.” This remarkable observation, if true, represents the only known record of pi- scivory in the Naticidae. However, if it is based on aquarium observations, then it may simply reflect aberrant behavior by starved in- dividuals (see the next paragraph). |. Scavenging Most studies have shown that naticids will only feed on fresh prey; carrion-feeding (as in the neogastropod Buccinidae and Nassari- idae) is not manifested. A few studies (typi- cally in aquaria) have shown that gaping (dying) bivalve prey may be consumed di- rectly without boring (Ansell & Morton, 1985). It is not clear if this laboratory behavior is also shown in the field. J. Egg Capsules Several authors have reported “naticid” boreholes in the egg capsules of various deep-sea organisms. These observations in- clude Thorson (1935: 12-13, figs. 4a—c) in egg capsules of the neogastropod buccinid Sipho [= Colus] curtus from East Greenland; Jensen (1951, fig. 1) in egg capsules of the ray (Raia) from Davis Strait (the boreholes ranged from 0.75 to 2.5 mm in diameter; a few capsules had multiple boreholes); and Ansell (1961) in egg capsules of the dogfish (Scyl- liorhinus canicula) with countersunk bore- holes. It must be emphasized that naticids were not observed boring these holes; these authors had merely conjectured that naticids were the most likely causative agents. These boreholes were clearly effected from the out- 166 KABAT side (i.e., they are not the hatching-out holes of the juveniles within). First, for the buccinid egg capsules, it is probable that a muricid bored the holes, as is known for some other muricids (Abe, 1985). Second, for the elas- mobranch egg cases, a more likely predator is the unusual deep-sea archaeogastropod family Choristellidae, which are typically as- sociated with skate egg capsules upon which they feed (Hickman, 1983: 86). The primary prey sources for naticids are infaunal gastropods and bivalves. The data [Appendix] document that 47 gastropod fam- ilies (out of 129 shelled marine gastropod families) and 35 bivalve families (out of 109 marine bivalve families) are known to be sub- ject to naticid predation. The major gastropod prey sources are the Turritellidae and Nati- cidae (Mesogastropoda) and the Turridae (Neogastropoda). The major bivalve prey sources are the Lucinidae, Tellinidae and Veneridae (Heterodonta). FOSSIL RECORD OF NATICID PREDATION This section tabulates the reports of fossil naticid predation and is arranged by geologi- cal time period. In general, only brief summa- ries are provided; discussion of any broader ecological aspects is deferred to the following section in combination with related conclu- sions from Recent studies. It must be empha- sized that it is difficult to track down all the paleoecological studies, especially those that are “buried” within lengthy systematic mono- graphs (no attempt has been made to search through the latter). Indeed, it seems better that extensive paleoecological researches should be published separately from narrower taxonomic studies, in order to bring them to wider notice. A. Triassic Fursich & Wendt (1977: 299) mentioned “naticid” boreholes from the Cassian Forma- tion of northern Italy (Tirol). Subsequently, Fursich & Jablonski (1984) illustrated the boreholes, showing the diagnostic counter- sunk appearance of incomplete boreholes, and discussed the implications thereof. The bivalve prey were Cassianella and Palaeonu- cula; the gastropod predators were referred to several species of the naticid genus “Ampul- lina.” Newton (1983; Newton et al., 1987: fig. 25.2) independently documented ‘naticid” boreholes in the epibyssate а Mysid- ioptera from the Wallowa Terrane of the Hells Canyon (Oregon-Idaho); this suggests that the Triassic borers were somewhat wide- spread, before becoming extinct. However, the taxonomy of Triassic “naticids” remains a morass, and their familial assignment is still uncertain. Further discussion of the evolution- ary consequences of Triassic boring preda- tion is deferred to the next section. Indeed, if these countersunk Triassic boreholes are not those of naticids, then it remains uncertain whether all the younger occurrences of coun- tersunk boreholes are correctly attributed to naticid predation. Sohl (1969: 726) expressed some doubt as to whether the Triassic forms were true nati- cids; in any event, his spindle diagram of nat- icid clade diversity (his fig. 1) clearly shows that from the Triassic to the mid-Cretaceous, there are never more than five genera in any epoch; naticid diversification did not com- mence until the Upper Cretaceous, with the evolution of the boring habit. Bandel (1988: 270) claimed that “Thus Triassic ‘naticids,’ to a large extent, are neritoideans, some belong to other groups, but none appear to be natic- ids’; this needs further documentation. B. Jurassic Sohl (1969: 729) searched through various paleontological monographs and collections of Jurassic mollusks and found no signs of molluscan boreholes. Fursich & Jablonski (1984) also concluded that there were no gas- tropod borers in the Jurassic. C. Cretaceous Fischer (1962a) reviewed some reports of Cretaceous boreholes and attributed most to naticids, as there were relatively few muricids at that time. Subsequently, Sohl (1969: 731) more carefully analyzed Cretaceous bore- holes and found a few from the Cenomanian (100 myr) and a much greater abundance from the Campanian (75 myr). The Ripley Formation (Campanian) was studied т greater detail by Vermeij & Dudley (1982) who also found extensive shell repair and a size refuge from boring predation. The oldest Cre- taceous records were shifted further back by Taylor et al. (1983) who documented naticid predation from the Blackdown Greensand of NATICID PREDATION 167 England (Albian, 105 myr). They found that the vast majority (92%) of boreholes were naticid, with a nearly equal ratio of gastropod to bivalve prey (in contrast to the few muricid boreholes, found primarily on bivalve prey). The diversification of naticids (and other mod- ern marine families) at this time represents the “Mesozoic marine revolution” of Vermeij (1977), and is discussed in the next section. Vermeij & Dudley (1982) reported no pre- dation on naticids in the Ripley Formation (Tennessee); subsequently, Kitchell et al. (1986: 293, fig. 1h) found a multiple-bored specimen of Euspira rectilabrum, from the same outcrops. This is the earliest record of confamilial naticid predation in the fossil record. D. Paleocene | have not found any paleoecological stud- ies from the Paleocene reporting on naticid boreholes. Naticids were present then; future studies of these faunas would be most worth- while. E. Eocene Fischer (1960, 1962a, 1963) reported on naticid predation in the Lutétien Stage of France and found that for the bivalve Petun- culus [= Glycymeris], 4.6% of the specimens were bored, primarily the smaller ones. For the gastropod Mesalia, 70.9% were bored by naticids (of which only 7.7% were incomplete holes), and some had multiple complete or incomplete boreholes. For Corbula spp., there was a rather high rate of boring failure (to 26% of the specimens). This fauna was also analysed by Taylor (1970) who found nu- merous naticid and muricid boreholes and an overall confamilial naticid predation rate of 11.3%. Siler (1965) briefly reported on the Gosport Formation of Texas and found both naticid and muricid boreholes on the bivalve Lirodis- cus tellinoides. A more comprehensive study on the Stone City Formation of Texas (Stanton & Nelson, 1980; Stanton et al., 1981) recorded a naticid mortality rate of 15% and a crustacean mortality rate of 20% for molluscan prey. The latter studies entailed considerable efforts to reconstruct the food web and paleocommunity structure. Several studies were carried out on the Ameki Formation of Nigeria by Adegoke & Tevesz (1974), Arua (1989) and Arua & Hoque (1987, 1989a, 1989c). They found that turrids and terebrids were the preferred gas- tropod prey; the latter authors also found ex- tensive predation on bivalves. However, as discussed earlier, some of the boreholes seem to have been misidentified (vis a vis naticid vs. muricid) by Arua & Hoque. An anal- ysis of bivalve prey (Arcopsis and Limopsis) from the Pallinup Siltstone in Western Austra- lia found that 9.2% of the bivalves had gas- tropod boreholes, one fifth naticid and four fifths muricid (Darragh & Kendrick, 1980). F. Oligocene Klahn (1932) analyzed naticid predation on other naticids from the Sternberg Formation of Germany and found high predation rates from 53.3% (the second smallest prey size class) to 15%-26% (the other classes); the documentation provided does not facilitate further analysis. G. Miocene Hoffman et al. (1974) conducted an exten- sive study on the Korytnica clays of Poland and found a confamilial naticid predation rate of about 10%; unfortunately, their data (table 1) do not fully partition the boreholes by nat- icid or muricid sources. Subsequently, Hoff- man (1976a) attributed most of the bivalve mortality to sedimentation, rather than preda- tion; similarly, abiotic factors accounted for much of the gastropod mortality (Hoffman, 1976b). Other Miocene outcrops from Poland were studied by Hoffman & Szubzda (1976), primarily with respect to food webs and com- munity structure. Kojumdjieva (1974) studied the Tortonian and Sarmatian outcrops of Bul- garia and found a variety of naticid and muri- cid prey taxa; very few unsuccessful or mul- tiple boreholes were observed. Thomas (1976) analyzed naticid predation on glycymerid bivalves from various Neogene (Miocene-Pliocene) outcrops in the eastern United States and concluded that predation rates in the Miocene were comparable to those on Recent glycymerids; however, the size-se- lectivity data seemed questionable. This re- search was reanalyzed by Kitchell et al. (1981: 545—548), who determined that the seemingly contradictory results of Thomas could be ex- plained by the fact that there were actually two different naticid predators (of markedly differ- ent sizes) in the various fossil faunas; this meant that the observed “changes” in preda- 168 KABAT tion intensity or prey size were merely an ar- tifact of which naticid predator was present. A series of studies on the Chesapeake Group of Maryland was conducted by Kelley (1982a-1989b), with an emphasis on bivalve prey. Nearly three-fourths of the mortality could be attributed to naticid predation; for some prey there was an increase (over geo- logical time) of prey size and shell thickness. This was hypothesized to be an evolutionary response to naticid predation. Dudley & Dud- ley (1980) made a briefer analysis of boring predation on three mollusk species from these outcrops, and observed a size refuge from predation for the two bivalves studied. Colbath (1985) reported on the outcrops of the Astoria Formation of Oregon and noted extensive naticid predation, primarily of bi- valves; other predation sources were not an- alyzed. The Wimer Formation of northern California was analyzed by Watkins (1974), who found low levels of naticid predation on several bivalves. Maxwell provided a thorough systematic and paleoecological analysis of the Stillwater Mudstone of New Zealand and observed con- siderable naticid predation on various gastro- pods and bivalves. The data were used to reconstruct food webs (Maxwell, 1988: 34, fig. 3) as part of an overall trophic analysis which also considered non-fossilized aspects of the community. There was extensive confamilial naticid predation, especially of the smaller- sized species. This monograph is an excel- lent model of integrating systematics with pa- leocommunity reconstructions. H. Pliocene Boekschoten (1967) studied the fauna of the Tielrode Sands of Belgium and reported some confamilial naticid predation, although crustacean predation was a far more impor- tant source of mortality for the naticids. The Emporda of Spain was analyzed by Hoffman & Martinell (1984), who observed high selec- tivity in prey size and borehole site choices. Guerrero & Reyment (1988b) used multivari- ate analysis to differentiate between naticid and muricid boreholes in Chlamys from the Lower Pliocene near Malaga, Spain. Robba & Ostinelli (1975) analyzed gastropod, cephalo- pod and crustacean predation in the Albenga outcrops of Italy and noted that 13.9% of all specimens were bored, nearly all by naticids. Hingston (1985) reported on the Muddy Creek assemblage from Victoria, Australia, and determined that about 75% of the bore- holes were naticid and the remainder muricid; edge drilling of bivalves was rare, and prey shell sculpture resulted in a greater frequency of unsuccessful boreholes. |. Pleistocene Kabat & Kohn (1986) analyzed predation on naticids from the Nakasi Beds of Fiji and observed rather high naticid predation rates on Natica spp., but considerably lower con- familal predation on species of Polinices and Sinum. Unsuccessful crustacean predation was quite common; successful crustacean predation probably accounted for a greater amount of mortality than did confamilial pre- dation. Berg & Nishenko (1975) found that 26% of the shells of Nassarius perpinguis from the San Pedro deposits of California showed naticid boreholes; stereotypy of bore- hole siting was shown, although no data on predator or prey sizes were given. A much more detailed analysis of the nearly contem- poraneous Puerto Libertad deposits of So- nora, Mexico, and a thorough trophic web re- construction was conducted by Stump (1975: fig. 18). J. Sub-Holocene Yochelson et al. (1983) analyzed naticid predation on scaphopods from the elevated “mud lumps,” or diapir structures from the Mississippi River delta (ca. 15,000 years old), and found (in two large samples) that almost 58% of Dentalium laqueatum had boreholes. They noted that other scaphopod assem- blages (fossil and Recent) showed far fewer naticid boreholes (usually less than 10%); this assemblage undoubtedly reflected excep- tional naticid feeding. Since the end of the Early Cretaceous (Al- bian), naticid predation has been documented through Holocene faunas (except for the Pa- leocene), although probable naticids are known from the Jurassic. Potential “natici- form” boreholes from the Triassic are known; the evidence is not conclusive as to whether or not the Triassic predators actually were naticids. The available data do not show any clear trends in the rates of gastropod boring predation since the Cretaceous (Vermeij, 1987: fig. 7.6); however, comparisons be- tween assemblages should be based on eco- logically analogous taxa, and studies of a sin- NATICID PREDATION 169 gle prey family need to consider possible changes in defense mechanisms (especially shell form) over time. Another area of interest is the use of bore holes in the field of ichnology, or the study of trace fossils. Most paleontologists recognize animal locomotory tracks as trace fossils; however, this field includes any and all re- mains of the activities of living organisms. Thus, a borehole found in a fossil specimen is, per se, a trace fossil, and can be described and discussed in the absence of exact knowl- edge of the causative agent. Needless to say, there has been some controversy over the “nomenclature” of trace fossils; the Interna- tional Code of Zoological Nomenclature (ICZN, 1985: Articles 1d, 10d, 42b) currently does recognize “ichnotaxon names,” as a parallel nomenclatural system. Hantzschel (1975), Warme & McHuron (1978) and Ekdale et al. (1984) provided excellent reviews of trace fossils. Predatory boreholes in fossil specimens can be referred to the ichnotaxon “Praedich- па” Ekdale, 1985; those produced specifi- cally by mollusks to the ichnotaxon “Oichnus” Bromley, 1981; and those identical with nati- cid boreholes to the ichnotaxon “Ojchnus pa- raboloides” Bromley, 1981. Maddocks (1988: 641-2) “arbitrarily defined” 20 “ichnophena” corresponding to different forms of boreholes in ostracod tests; this diversity is unrealistic and meaningless. These names have no heu- ristic value: if they can be attributed to a known predator, then they should be referred to as “borehole of ”, whereas those of unknown predators should not be given for- mal names. ECOLOGICAL ASPECTS OF NATICID PREDATION This section attempts to integrate and syn- thesize, from an ecological perspective, the varied aspects of naticid predation. It is hoped that this will not only indicate what has been well documented but also reveal promising (or neglected!) areas for future research. | have not attempted statistically to re-analyze previous studies or to provide detailed criti- cisms of previous methodologies, unless it seemed directly warranted. Subsequent re- searchers would be well advised to re-check the relevant previous studies. My section on “Mechanisms of naticid predation” above in- cluded the more proximate aspects of naticid prey detection, capture and boring; this sec- tion covers the broader, ultimate aspects of naticid predation, as well as several topics from the “prey's viewpoint.” A. Prey Size and Species Choice The embryos of naticids feed on dissolved Organic matter (DOM); some species have yolk reserves or infertile nurse eggs which serve as additional food resources, especially for those with direct development. Naticid species with planktotrophic larvae feed on the phytoplankton while in the swimming stage; those with lecithotrophic larvae undoubtedly rely on DOM in addition to their yolk reserves (Ansell, 1982c). The feeding habits of juvenile naticids have been much less studied. For example, Ansell (1982c) reported that they ate various un- specified gastropods or bivalves of small size; Berg (1976) was able to feed them Bittium and Rissoella, although this was limited to aquarium studies. Wiltse (1980a) found that juvenile Neverita duplicata at Barnstable Har- bor (Massachusetts) consumed the diminu- tive venerid Gemma gemma; because of the high density of the latter, naticid predation ac- counted for less than 15% of total prey mor- tality. Maddocks (1988) concluded that juve- nile naticids represented significant predators of ostracods; with ontogeny, the naticids shift to larger-sized molluscan prey. Adegoke & Tevesz (1974: 22) claimed that “no direct correlation was found between prey size and predator size”; but no statistical data were presented to support this statement. Other studies, however, have shown that there is usually a good correlation between predator size (as determined by the inner borehole diameter) and the prey size (e.g. Ansell 1960; Bayliss, 1986; Griffiths, 1981; Kabat & Kohn, 1986; Kitchell et al., 1981; Mace, 1978; Martinell & De Porta, 1982; Robba & Ostinelli, 1975; Selin et al., 1986; Wiltse, 1980a). Colbath (1985) reported little correlation between borehole diameter and prey size, except for Katherinella prey. How- ever, these results are a consequence of Col- bath's use of bivalve shell “width” rather than the more conventional length as the dimen- sional measure. Also of importance is the relative size of the prey taxa and the naticid predators. Large prey species are often less susceptible to pre- 170 KABAT dation by naticids than are small prey spe- cies. Similarly, within a species, smaller indi- viduals usually suffer greater naticid mortality (e.g. Franz, 1977; Jackson, 1972). Penney & Griffiths (1984) used three-dimensional pre- dation contour diagrams to display the rela- tionships between predator size, prey size, and quantity of prey consumed. Alternatively, Hoffman (1976b: 296) showed no size-selec- tivity for some (but not all) gastropod prey from the Poland Miocene. However, Green (1968) found that mortality from naticid boring of the bivalve Notospisula parva actually in- creased with prey shell size; similar results were shown by Mukai (1973) and Wilson (1988). As discussed below, increased prey size over geological time may represent an evolutionary response to naticid predation (or is of adaptive value to escape predation) (Kelley, 1984, 1989b). Prey switching, or prey choice, has been a contentious point; the fundamental question of “why” a given naticid will pick a certain prey species given an equal choice of several species can lead to teleological explana- tions. Ansell (1983) found that dietary switch- ing will not occur and suggested that “рге- conditioning” may play a rôle in species choice. Broom (1983) found that younger Nat- ica maculosa fed on Pelecyora trigona, whereas older predators fed on Anadara gra- nosa; ontogenetic dietary switching thus oc- curred. Several studies, using a variety of prey items, have determined a hierarchy of pre- ferred prey choices. For Euspira alderi, Bayliss (1986: 40) found that the preferred bivalve prey, in descending order, were: Mya, Spisula, Cerastoderma and Parvicardium; Arctica and Corbula were not preyed upon. Similarly, George (1965) found that mortality due to nat- icids was most prevalent in Glycymeris gly- cymeris, and less so in Donax semistriatus and D. trunculus (the latter the larger species). Kitchell et al. (1981) found that for Neverita duplicata, the preferred prey, in descending order, were: Mya, Mercenaria, Mytilus and Ne- verita. Although Neverita was actually the highest in energetic value, the handling costs were such that only much smaller conspecific prey could be captured by the naticid predator. Kelley (1989a) found that bivalve prey from the Maryland Miocene were preferentially bored, in descending order, as: Eucrassatella, Ana- dara, Astarte (the latter two roughly equiva- lent) and Corbula, with slight differences from one formation to another. The same naticid species, in different local- ities, may have markedly different diets. Thus, Natica maculosa in Penang (Malaya) feeds wholly on gastropod prey, especially the tro- chid Umbonium vestiarium, whereas this spe- cies at Kuala Selangor (Sumatra) feeds on bivalve prey, particularly Anadara granosa. In this case, it is the relative availability of prey taxa which determines (in part) the diet of a given naticid species (Broom, 1982; Berry, 1982). A recent series of studies by Kitchell and colleagues (Kitchell et al., 1981; DeAngelis et al., 1984, 1985, 1989) have attempted to model the energetic and coevolutionary as- pects of naticid ecology. The first study was of value in providing a useful model for the test- ing of naticid predation; however, the subse- quent papers incorporated multiple assump- tions which decreased their representation of the real world into a series of parameters couched in advanced equations. This reduc- tionist approach cannot account for complex, stochastic, and hierarchial ecological commu- nities. It is worthwhile to elaborate briefly the basic principles of the Kitchell models. Essentially, the cost:benefit ratio for various prey species is determined (costs being the time and en- ergy to recognize, capture/subdue, bore, and digest the prey; benefits the energetic value or gain of prey tissues) and related to both prey size and predator size, given that the cost of a specific prey will vary according to the predator size. From this, one can graphi- cally represent the cost-benefit functions with prey size as the dependent variable and cost: benefit ratios as the independent variable. The lowest curve represents the optimal prey choice. These curves show that optimum prey are of intermediate sizes; too-small prey are of low energy value and too-large prey can usually escape the predator. Kitchell (1987) found that these models lead to the prediction that ‘larger naticid predators should be more highly selective than smaller-sized naticids,” all other factors being equal. Discussion of their later models, dealing primarily with pred- ator-prey coevolution has been deferred to section F, under the evolutionary aspects. Kelley (1982b, 1987, 1989a—b) used these methods to analyze naticid predation in the Maryland Miocene fauna, and confirmed that the models predict prey selection patterns, but with some exceptions. She found that over time, bivalve prey shell thickness (= cost) increased while there was no overall NATICID PREDATION 171 trend in shell volume (= benefit). Commito (1987) questioned the validity of the Kitchell models and noted that their assumptions ne- glected several important factors with respect to prey defense strategies (or adaptations): ignored were the possibilities of depth ref- uges, shell ornamentation, chemical de- fenses, or behavioral responses, all of which could deter naticid predation. DeAngelis et al. (1987) acknowledged these criticisms and suggested that yet further modelling would be able to incorporate these aspects of prey bi- ology. It is difficult to account fully for all the parameters or variables that determine or in- fluence predation processes; any model that attempts to do so would likely be so unwieldy or incomprehensible as to be of little heuristic value. ' Interestingly, Ansell (1982b) found that Eu- spira alderi would not feed on opened bi- valves—only live, closed prey items were chosen. These same results were found by Kitchell et al. (1986: 297) for Neverita dupli- cata. This suggests that the stereotypy of prey choice restricts the naticids to fresh prey, and rules out scavenging or carrion-feeding. Predation by naticids on other naticids can be quite widespread and represents a signif- icant source of naticid mortality. Although oc- casionally referred to as ‘cannibalism,’ that term is inappropriate since this predation does not necessarily involve conspecifics. Studies from the Nigerian Eocene showed that about 15% of naticid shells had naticid boreholes (Adegoke & Tevesz, 1974); Col- bath (1985) observed only 2.7% such in the Oregon Miocene; Hoffman et al. (1974) noted 10% such in the Poland Miocene. Boekscho- ten (1967) found that 7.8% of the naticids from the Belgian Pliocene had naticid bore- holes. Kabat & Kohn (1986) determined that in the Fijian Pleistocene, naticid predation on Natica spp. accounted for 27% of mortality, whereas that on Polinices and Sinum spp., for only 3% of mortality. The latter genera have more globose shells and a larger foot which may provide faster locomotion and hence fa- cilitate escape from confamilial predators. Maxwell (1988) concluded that smaller-sized naticids of the New Zealand Miocene had much higher naticid predation rates, confirm- ing size-selectivity aspects of naticid preda- tion. Several studies on Recent naticids have also shown extensive confamilial predation (Burch & Burch, 1986; Fretter & Manly, 1979). Obviously, there is considerable variation as to the extent of confamilial naticid predation; disease and predation by fish or crustaceans may represent more important naticid mortal- ity pressures. B. Stereotypy of Boring on Prey Shell For gastropod prey, there has been some confusion among studies with respect to the siting of successful boreholes, with some “results” actually of no consequence. Thus, Arua & Hoque (1989a: 55) emphasized that the “preferred drilling site” on the apertural side was on the last whorl; however, because of whorl overlap, most of the exposed prey shell surface is the last whorl, and thus purely non-random borehole siting would lead to most boreholes located there (their other re- sults combine 11 prey species into a single table which does not facilitate further analy- sis). Yet, for some gastropod prey, there is a predominance of predation on the dorsal (abapertural) side over the ventral (apertural) side; this reflects the increased ability of the prey to escape in the latter position (Adegoke & Tevesz, 1974). However, other studies suggested that predation on the ventral side is preferred since the predator's foot seals off the aperture, blocking escape (Berg, 1976: 3; Berry, 1982). Some studies have shown that certain gastropod prey are preferentially bored on the penultimate whorl (rather than the last whorl); this, too, reflects prey handling factors (Dudley & Dudley, 1980; Hoffman & Martinell, 1984). Boreholes that are at either extreme end (apical or abapical) may not al- low the proboscis to penetrate the entire shell; more centrally located boreholes may facili- tate complete consumption of the prey tis- sues. For gastropod prey, it is convenient to an- alyze the stereotypy of borehole siting by the various geometrical subsets of the shell. Not only can one distinguish between the outer (body) whorl and the older, apical whorls [1.е. the horizontal dimension], but one can also partition the prey gastropod shell whorls into semicircular sectors, or longitudinal zones [i.e. the vertical, or axial dimension]. Thus, Berg (1976) and Berg & Nishenko (1975) de- veloped two conflicting numbering schemes for the latter division. In the 1975 paper (their figure 1b), the sectors (numbered 1-8) started with the apertural plane and pro- ceeded counterclockwise (when viewed from the apex); thus, their clockwise “pie chart” (their figure 1c) of the sectors is actually viewed abapically. But, in the 1976 paper (his 172 KABAT figure 2a) the sectors (also numbered 1-8) started with the apertural plane and pro- ceeded clockwise (when viewed from the apex); their clockwise “pie chart” (his figure 2b) is, this time, viewed apically! It is not clear what has been done here; my recommenda- tion is that future investigators explicitly spec- ify which scheme they are using. Kabat & Kohn (1986: fig. 4), using the first scheme, observed that for naticid prey, bore- holes were found in four of the eight shell sec- tors, with nearly 90% occurring in two 90° sec- tors; however, there was little overall evidence for stereotypy of borehole siting. Robba & Ostinelli (1975: 327) independently depicted an angular measurement system which corresponds to the first scheme of Berg. Stump (1975: figs. 19-21) devised ап elaborate “equal-area projections” system to show frequency-contours (in percentages) of borehole siting on the various prey shells. Regrettably, this method is difficult to visualize and does not lend itself to comparison with the other, more direct schemes; it does not seem to have been used by subsequent au- thors. Some studies have shown that most boring occurs near the shell margin of bivalve prey, where the shell is thinner and there is no sculpture (e.g., Ansell, 1960; Ansell & Morton, 1985). Other studies, however, have shown a preference by other naticids for boring near the umbones (e.g. Ansell & Morton, 1985; Arua & Hoque, 1989; Bernard, 1967; Colbath, 1985; George, 1965; Jacobson, 1968; Kitchell et al., 1981; Leidy, 1878; Matsukuma, 1976; Negus, 1975; Piéron, 1933; Thomas, 1976; Vignali & Galleni, 1986); or in the mid-region (Bayliss, 1986; Griffiths, 1981; Vermeij et al., 1989). The strongly inequilateral Periploma margaritaceum was primarily bored on the anterior slope, due to its shell form (Rose- water, 1980). Some earlier studies had sug- gested that naticids preferentially bored near the prey gonads or digestive tissues (Pelse- neer, 1924; Verlaine, 1936); however, bore- hole siting is primarily a function of the ma- nipulation of the prey during boring and may depend on the prey shell morphology. In a few cases, little stereotypy is manifested. Berg & Porter (1974) found that, for the same bivalve prey, there were significant differ- ences between naticid species as to the pre- ferred borehole position; Berg (1975) sug- gested that behavioral differences in prey capture and handling influenced species-spe- cific patterns. Probably of greater importance are (1) the size of the prey relative to the predator; (2) the shell thickness and presence or absence of sculptural elements; (3) the relative convexity of the prey shell; (4) other factors relating to the predator's manipulation of the prey. Based on this review, no one element solely determines the locus of borehole siting among bivalve prey. The majority of studies have shown little preference for right vs. left valves of bivalve prey, as would be expected given the equiv- alve nature of most infaunal bivalves. Some studies have shown 10—20% “differences” in the frequency of boreholes between valves, but no clear trends are apparent. Needless to say, for each valve with a borehole, there is a matching, unbored valve; hence the naticid mortality rate is twice the number of bored valves divided into the total number of valves. It is incomprehensible as to what Lever et al. (1961: 341) meant when they stated that “the percentual mortality may in some cases ex- ceed 100 [%].” Adegoke & Tevesz (1974) stated that Var- icorbula from the Nigerian Eocene was pleu- rothetic and invariably bored on the right valve which is closer to the surface. However, as noted below, the left valve of corbulids has a thick periostracum which deters boring pre- dation; the position of the corbulid shell in the substrate is of less import (De Cauwer, 1985). More generally, since naticids usually manip- ulate their prey prior to boring, the life position may be of little relevance. Newton (1983) found that the Triassic limid Mysidioptera was always bored through the left valve; this taxa is an epibyssate recliner and the left valve is adjacent to the substrate (Newton et al., 1987: 11g. 27). С. Incomplete and Multiple Boreholes; Non-boring Predation Incomplete boreholes are usually inter- preted to represent a sign of interruption of predation, whether by prey escape, arrival of another predator, or other disturbance. In some cases, the same naticid (or another) will recapture the prey and commence boring a new borehole, elsewhere on the prey shell. Sometimes the new hole will coincidentally overlap the older hole; but studies have shown that naticids cannot recognize their own previous borehole and resume drilling there (thereby saving considerable time) (Kitchell et al., 1981: 539). The related prob- NATICID PREDATION 173 lem of multiple complete boreholes again suggests interruption of predation after the completion of a borehole. Obviously there is an evolutionary disadvantage in not recogniz- ing previous boreholes (complete or incom- plete); the stereotypy of naticid predatory pat- terns may not be sufficiently flexible (Vermeij, 1982: 707; Kitchell et al., 1986). In an analysis of the Miocene Strioterebrum monidum from the Caribbean, Kitchell et al. (1986: 294-5) found extremely large num- bers of shells with multiple boreholes; one such had 15, of which 12 were incomplete and three had penetrated the prey shell but were not sufficiently wide to allow passage of the proboscis. Further studies on living tere- brids by these authors confirmed that some species of this prey family are highly agile and can repeatedly escape naticid predation dur- ing the boring actions. Earlier, Vermeij et al. (1980: table 2) showed rather high rates (to 40%) of incomplete boreholes in various Re- cent terebrids; G. J. Vermeij (in litt.) sug- gested that the pungent odor of terebrids and olivids may represent a chemical defense against predation. Fischer (1962b: 97) found that in a large sample (n = 1,126) of the Eocene turritellid Mesalia, 70.9% had naticid boreholes. Of the bored specimens, 84.8% had a single com- plete borehole (of which a tenth also had one to several incomplete boreholes); 4.2% had multiple complete boreholes; 8.7% had a sin- gle incomplete borehole; and 2.3% had mul- tiple incomplete boreholes. Kitchell et al. (1981: 542) observed that the lucinid Pseudomiltha floridana had a ratio of incom- plete to complete boreholes of 0.54:1. This taxon was stated to be polymorphic for shell thickness; the thicker shells were more likely to have incomplete boreholes. An important recent discovery was that some bivalve prey, primarily in the tropics, are preferentially bored through the edge of the valves (Taylor, 1980: 175; Vermeij, 1980: 330); not only is the shell thinner there, but also the prey shell is unsculptured and easier to bore (Ansell & Morton, 1985). The latter authors found that some species (i.e. of Po- linices) regularly edge-bored Bassina, while Glossaulax did not; that genus may preferen- tially bore other prey taxa. Some elements of “learning” (conditioning) may be involved in these responses to shell sculpture. The razor clams (Ensis, Solen) have been shown to be typically consumed by naticids without boring, because when the valves are contracted, there are still sizable pedal and siphonal gapes through which the naticid pro- boscis can be inserted (Turner, 1955; Ed- wards, 1975; Schneider, 1981; Frey et al., 1987); this was also shown for Tresus (Reid & Fiesen, 1980: 32). Edwards & Huebner (1977) noted that Mya was not consumed di- rectly through its large siphonal gape; т- stead, naticids always bored through the valve; possibly the siphonal tissue deters feeding activities. Earlier, Agersborg (1920: 421) had claimed that Mya and various other clams could be suffocated and directly con- sumed by Euspira lewisii; this now seems doubtful. Vermeij & Veil (1978) found that the frequency of gaping bivalves in marine faunas decreased from the Arctic to the tropics and noted that this was correlated with the in- crease in shell boring and other predation sources in warmer habitats. Some gastropod prey can be attacked through the aperture, as the corneous oper- culum is flexible enough for the proboscis to be inserted around the margins (Hughes, 1985). Edwards (1969: 327) found that some Olivella prey were consumed without boring, and suggested that either the naticid could force the operculum, or else the prey “зиНо- cates while wrapped in the predator's foot and relaxes,” allowing the predator direct access to prey tissues. Interestingly, Yochelson et al. (1983: 11) speculated that the stereotypy of naticid boring precluded their attacking sca- phopods directly through the open apertural end; but they suggested that it was more likely that once the scaphopod had retracted posteriorly, the naticid proboscis would not be able to reach the prey tissues. As mentioned earlier, the tropical Indo- Pacific Polinices mammilla is able to “suf- focate” and consume bivalve prey without boring. Ansell & Morton (1987) documented that this non-boring predation, in aquarium experiments, accounted for 14% to 54% of the bivalve mortality (according to prey spe- cies). This example, and those in the preced- ing two paragraphs, would greatly complicate community analyses (especially of fossils!) since no “traces” of naticid predation would be left on the post-mortem prey shell. It should be noted that the results of several studies of naticid predation were misinter- preted as concluding that a significant num- ber of the prey were consumed without boring (Kitchell et al., 1986: 297). Thus, Edwards (1975: 17) found that about 75% of the prey were bored and the remainder died of other 174 KABAT causes; Taylor et al. (1980: 397) erroneously took this to mean that the latter 25% of the prey were consumed (by naticids) without be- ing bored. Similarly, Medcof & Thurber (1958) misinterpreted their own data to assume that all the empty, non-bored bivalve prey shells were consumed by naticid predators without boring; this overlooked other mortality sources. Another study (Bernard, 1967) stated that “in limited aquarium observation, over 60% of Saxidomus consumed showed no drill marks” (р. 9); and, again, “... in aquaria tests 25% of clams [Saxidomus gi- ganteus] consumed by Polinices [= Euspira] lewisi bore no marks at all” (p. 10); the dis- crepancy in numbers is irreconcilable and all bivalve mortality was erroneously attributed to naticid predation. D. Prey Defense Mechanisms Ansell (1969) and Carter (1968) provided a general overview of defense mechanisms in various marine mollusks. Many bivalves show leaping or rapid burrowing in response to con- tact by naticids. Laws & Laws (1972: fig. 1) described the escape response of the Austra- lian Donacilla angusta, which leaps or pops out onto the surface, thereby evading the bur- rowing naticid predator; similar responses were shown for Ensis directus (Turner, 1955; Schneider, 1982) and Ruditapes philippi- narum (Rodrigues, 1986). Either rapid or deep burrowing (or both), can serve as an escape mechanism (Vermeij, 1983a) for bi- valve prey. Ansell & Morton (1985: 656) found that the anomalodesmatan bivalves Lyonsia and Pan- dora seemed to escape naticid predation “by coating the posterior edge of the shell with mucus to which sand grains adhere’; pre- sumably this somehow deterred naticid pre- dation. Corbulid bivalves have been the object of several paleoecological studies; corbulids are noteworthy for their well-developed conchiolin layer (within the valve) which serves as a fairly effective deterrent to gastropod preda- tion (Lewy & Samtleben, 1979). Furthermore, most successful boreholes are in the right valve, since there is well-developed perios- tracum on the left valve of corbulids which also deters predators. Complete boreholes in corbulid valves have a special form, with a considerably narrowed inner margin below the conchiolin layer (De Cauwer, 1985: figs. 1d, 1e). Kelley (1989a: 446-7) also found considerably reduced successful predation on Corbula and suggested that the low level of selectivity of prey size and borehole siting may also account for the high rate of unsuc- cessful predation (60% of boreholes nonfunc- tional). Lewy & Samtleben (1979: 350) sug- gested that the conchiolin layer serves as a compensation for the slow mobility and shal- low burrowing of corbulids. Alternative “defense” strategies of two bi- valves were discussed by Commito (1982): Mya arenaria grows rapidly to a large size (and deferring reproduction until then), thereby escaping naticid predation [= size refuge], whereas Macoma balthica instead grows slowly, reproduces early, and escapes most naticid predation by deep burrowing [= spatial refuge]. Of course, Mya is subject to naticid predation while it is still small. The former mechanism was used by Hutchings & Haedrich (1984) to explain the size structure of deep-water nuculanids subject to naticid and fish predation. Actually, these “alter- native” life history patterns may represent phylogenetic constraints rather than direct ad- aptations to naticid predation, per se. Ansell & Morton (1985) discovered that re- moval of the sculptural lamellae on the shells of the venerid Bassina led to increased boring predation through the shell sides. Otherwise the naticids bored through the valve edges which do not have sculpture. This experimen- tal observation demonstrated the function of sculpture as a prey shell defense mechanism in addition to stabilizing the bivalve in soft sediments. Bayliss (1986) found that among bivalve prey, the species with the thinnest shell was preferentially preyed upon by naticids. Hing- ston (1985: table 4) noted that increased prey shell sculpture led to increased frequency of unsuccessful (incomplete) boreholes. Dudley & Vermeij (1978: 439) concluded that strong spiral ribs usually deterred boring in turritel- lids. Kelley (1982a: 46) reported that uncrenu- lated (male) shells of Astarte were more likely to be bored than were crenulated (female) shells; however this genus is protandrous, and the resulting size differences (between sexes) may be sufficient to explain differ- ences in predation rate (given that the smaller males are less likely to escape predation). Boggs et al. (1984), using Mercenaria mer- cenaria prey, artificially ground-down the shell surface to half the normal thickness, and tested the effects on predation by Neverita duplicata. They found that naticids could not NATICID PREDATION 175 learn to differentiate between normal and thin-shelled prey, although the latter took con- siderably less time to bore. The same results were found by Rodrigues et al. (1987) for Ne- verita didyma preying on Ruditapes philippi- narum. In some respects, these studies are of questionable value since it has not been shown that gastropods have any sensory mechanism for “determining” shell thickness (or shell weight). It is true that preying on thin- ner prey freed up additional time for foraging; surely the snails are incapable of this realiza- tion because they have no method for recog- nizing the thinner prey. This is an interesting case of a hypothetical coevolutionary re- sponse that does not initiate an “arms race.” E. Food Webs, Energy Flow and Physiological Efficiencies Food webs are attempts to diagram the overall trophic structure of an ecological com- munity (predators, herbivores, primary pro- ducers, detritivores). Elucidation of the struc- ture of a food web and the strength (or quantity of interactions) of each link (chain) facilitates analyses of community energy flow and population dynamics. As infaunal preda- tors, naticids (with other infaunal polychaetes, crustaceans, and nemerteans) represent an often overlooked level of predation, in addi- tion to the more conspicuous epibenthic pred- ators (asteroids, fish and crabs) (Commito & Ambrose, 1985). An example of the complex- ity involved is that both asteroids and naticids _prey on bivalves, whereas some asteroids also prey on naticids (Christenson, 1970: 67); the same multiple interactions also occur with respect to crabs and fishes. Relatively little research has been done on determining the complete food webs for soft-bottom commu- nities, in contrast to better-known rocky inter- tidal communities; this reflects the ease of ac- cess and analysis of the latter fauna. Several paleocological studies have at- tempted to elucidate community structure and food webs, based primarily on an analysis of shell boring and breaking predation (Hoffman 8 Szubzda, 1976; Stanton & Nelson, 1980; Stanton et al., 1981; Stump, 1975; Taylor et al., 1983). While of great heuristic value in facilitating comparisons between fossil com- munities (as well as with Recent communi- ties), these studies are limited by the indeter- minate nature of mortality that leaves no “traces,” as well as shell-removing agents, the latter skewing the results towards the re- maining predatory agents. It is important to realize that naticid preda- tion represents only a part of the sum of all predation in soft-bottom communities; several authors have carefully reviewed the diversity and importance of other predators in these habitats (Cadée, 1968; Carter, 1968; Vermeij, 1978). Thus, Green (1969) found that naticids accounted for 9% of the mortality of the tropical bivalve Notospisula parva; shell-crushing skates were responsible for over 60% of the mortality; the remainder was due to other fac- tors (disease or abiotic agents). The latter, non-predatory sources of mortality are just as important but virtually impossible to determine precisely from fossil or beach assemblages (i.e., an empty, undamaged shell may be the outcome of parasitism, other disease, sedi- mentation, or other agents) (Hoffman, 1976a). A series of excellent physiological studies was conducted by Ansell and Macé on the European Euspira alderi. Distinct periods of shell growth were followed by egg collar pro- duction; feeding was considerably greater during the latter stage, since over 90% of non-respired assimilated energy is used for reproduction (Ansell & Macé, 1978; Ansell, 1982a—b). Predation rates increased with temperature (Macé, 1981a); and oxygen con- sumption rates (= respiration) were affected by the prey type and quantity (Macé, 1981b; Mace & Ansell, 1982). Each week, an adult naticid consumed up to its own (dry) weight in prey tissue [Tellina tenius] (Ansell, 1982a); this is limited by the extensive time spent in obtaining suitable prey. Macé (1981c) found that energy assimilation efficiency is about 60% during reproductive periods, and only 40% at other times. About 50-60% of the consumed energy is, however, “lost”: not ac- counted for by growth, respiration (mainte- nance) or reproduction. Ansell (1982b) sug- gested that some of this may be accounted for by the mucus that is essential for prey cap- ture and predator avoidance; much of the re- mainder is represented by feces and uncon- sumed prey tissue, but Berry (1983) was unable to calculate the energetic costs or losses due to mucus or feces. Bayliss (1986), using tre same naticid species, found that about 24% of the time was spent drilling, 11%-18% ingesting prey tissue, and the re- maining time in other activities, typically qui- escent. Related physiological studies on the tem- perate Neverita duplicata (in Massachusetts) 176 KABAT showed that the feeding season was only about 35 weeks, during which approximately 1.85 prey (Mya arenaria) were consumed per week. The naticids consumed about 1% of their body weight in prey on a daily basis, and the overall growth efficiency rates (snail growth in kilojoules per clam tissue consumed in kilojoules) declined from almost 50% in young Snails to 16% in older snails (Edwards & Huebner, 1977; Huebner & Edwards, 1981). Another factor of importance in calculating energy budgets is whether or not all the prey tissue is consumed. Thus, for a high-spired gastropod prey, some of the apical tissues may not be reached by the proboscis. Ed- wards & Huebner (1977) found that when feeding on Mya, only about 80% of the prey tissues were consumed (i.e. the “energy rich, low-ash content tissues’); proboscoidal ас- cess is not at issue here and this may reflect the less-palatable nature of the mantle edge and siphonal tissues of Mya. Broom (1982) determined the “сопзитр- tion rate” equation of feeding efficiency: this represents the mg dry weight of prey con- sumed per day, as a function of predator body (wet) weight. Thus, for Natica maculosa feed- ing on Anadara granosa, the allometric equa- tion was CW = 9.13 (W)'°°8°, where W = predator wet weight (in grams). Similarly, Grif- fiths (1981) found that the consumption rates (of bivalve prey, Choromytilus meriodionalis) increased 4.5 fold over a 55% increase in predator (Natica tecta) size. Many of these studies were based on lab- oratory (aquaria) observations. These, of course, are a simplification or modification of reality (field behavior). Bayliss (1986: 46) co- gently noted that “the artificial and enclosed environment in an aquarium increases the predator's ability to detect and capture a prey item as well as reducing the prey’s ability to avoid and escape from the predator.” Also, intertidal naticids are usually quiescent during low tide; in aquaria where they are continually submerged, the duration of activity is more extensive. Many laboratory studies (e.g. Rod- rigues, 1986) used an aquarium sand depth barely greater than the prey or predator size; this does not allow for normal burrowing pat- terns. Kitchell et al. (1986: 297) noted that in their aquaria, the prey frequently “die, gape and decompose without the predator taking any part in the process’; this suggests that their prey were usually moribund or otherwise unhealthy, and leads one to question the va- lidity of predation studies on these weakened prey. These caveats should be considered when calculating feeding rates, energy bud- gets, and related trophic measurements based on laboratory studies. A typical example of the effects of naticid predation on prey population dynamics is that of Ansell (1960) who found that of first-year Venus [= Chamelea] striatula, 40% of the to- tal mortality [= 15% of all individuals] was due to naticids; for the second-year cohort, only 15% of all mortality [= 5% of the cohort] was naticid predation; and for the third-year cohort [the last], only about 1% of all mortality was due to naticids. Clearly, predation by Eu- spira alderi affects primarily the younger co- horts; disease or other predators affect the older cohorts. Another interesting taphonomic-ecological phenomenon is that of “beach sorting” or the differential post-mortem ‘“survivai” of valves of different bivalves (interspecific and in- traspecific analyses), comparing both right vs. left valves and bored vs. unbored valves (Lever et al., 1961; Lever & Thijssen, 1968; Martinell & De Porta, 1980). The critical ques- tion is whether or not bored valves are differ- entially susceptible to post-mortem damage which would affect their representation in the fossil (or “beach shell”) assemblage (Dudley & Vermeij, 1978: 437). One must also deter- mine the extent of other shell-breaking preda- tion that wholly removes the shells from the assemblage. The studies of Lever and colleagues found that valves with boreholes (natural or artifi- cial) traveled shorter distances but were more likely to end up higher on the shore (than non- bored valves), because of the biomechanics of fluid flow through and around bored valves. Thus, the “hole effect” is the upward transport of bored valves. The differential transport of right and left valves may also occur, resulting in greatly distorted ratios thereof in a beach assemblage. Indeed, it is possible that some paleontological studies showing “differences” in boring rates between valves may actually be a consequence of this differential sorting. A problem with such studies is that the hydro- dynamic properties of bivalve shells can vary between taxa, and the biomechanical effects of one shell morphology may well be the op- posite of those of a different morphology. F. Enemies and Control of Naticids Asteroids (starfishes or seastars) are im- portant predators of naticids (Agersborg, NATICID PREDATION 177 1920; Christenson, 1970); some naticid prey will ward off the asteroid by extension of the foot over the shell followed by mucus secre- tion (Ansell, 1969; Margolin, 1975). The latter author documented that Natica stercusmus- carum could respond to Astropecten by rasp- ing off the spines and consuming the tube feet, deterring the starfish. Clarke (1956) noted that Nassarius trivittatus feeds upon the egg collars of Euspira heros, serving as a means of control. Ironically, this nassariid is, in turn, preyed upon by adult naticids! Frequently, naticids are “blamed” for ob- served declines in populations of commercial shellfish (soft shell clams, quahogs, etc.), and oyster beds may be disrupted as naticids bur- row through them in search of other prey items (Agersborg, 1920: 420). Because oys- ters are now more commonly cultivated on stakes or lines off the substrate, this may now be less of a problem. Edwards & Huebner (1977: 1231) cogently noted that ‘bored shells ... are thus an exaggerated indicator of [naticid] mortality . . .” because other preda- tors (arthropods, fish, birds, humans) remove or otherwise destroy bivalve shells. These au- thors further stated that naticid predators are an easy scapegoat to take the blame for “... human exploitation patterns, a sensitive issue.” The various mechanisms and their success (or lack thereof) for the control of “pests” of shellfish were reviewed by Kor- ringa (1952: 347-351); hand collecting is par- ticularly ineffective (Turner et al., 1948; Med- cof & Thurber, 1958). Carriker (1981: 417) suggested that ecological control, involving species-specific pheromones or deterrents, might be successful. There remains the often unacknowledged dilemma that not only is it impractical (or even impossible) to eliminate these predators, but also the resulting impact on the overall community structure and food web may actually be more deleterious than the effects of the predators themselves on the shellfish. G. Macroevolutionary Patterns and Evolutionary Escalation If, as claimed by Fursich & Jablonski (1984), the Triassic boreholes are attributable to naticids, then the parallel evolution of the naticid boring habit twice (Triassic and Creta- ceous) undoubtedly reflected the canalization or phylogenetic constraints of shell-boring: there are only so many ways a shell can be bored, and the underlying mechanisms may have remained quiescent in the Naticidae during the Jurassic. However, it remains un- clear whether the Triassic predators are in- deed naticids, or how the Jurassic naticids may have fed (possibly as scavengers). Taylor et al. (1980: fig. 16) presented a hypothetical scenario of the evolutionary radi- ation of gastropod predation. Generalized proboscis probing was subsequently supple- mented by pedal manipulation, which led var- iously to shell boring, wedging, chipping, or pedal suffocation. It can be assumed that these initial stages represented preadapta- tions to shell boring; however, the specific or- igins of the complex accessory boring organ remain uncertain. The independent evolution of shell boring in a number of molluscan taxa represents convergent evolution; the struc- tures and processes are not necessarily ho- mologous. (See “Diversity of Boring Preda- tion” above for further comparisons). The Cretaceous radiation of naticids is part of the Mesozoic marine revolution, involving the increase in diversity of many modern ma- rine predators as a consequence of the “in- crease in shelled food supply resulting from the occupation of new adaptive zones by in- faunal bivalves and by shell-inhabiting hermit crabs” (Vermeij, 1977: 245). Specifically, the shift of bivalves from predominantely epifau- nal and byssate forms to infaunal, siphonate forms served as an escape from the then- dominant epifaunal and pelagic predators [cephalopods, asteroids, sharks and marine reptiles] (see also Taylor, 1981: 236) and sub- sequently led to selection favoring infaunal predators. If the early Mesozoic naticids were not burrowers (as suggested by their shell morphology), then burrowing in combination with shell boring would have opened up a new adaptive zone for the Cretaceous naticids. At the same time, the diversification of other sandy-habitat gastropods (especially turritel- lids, turrids and terebrids) provided further in- faunal prey for naticids (Taylor et al., 1980: 399). An important biogeographical phenomenon is the pattern of latitudinal diversity (pole— equator) of predatory prosobranch gastro- pods. For most of these marine families, in- cluding the Naticidae, there is a strong increase in species diversity from the poles to the tropical regions (the two exceptions are the Buccinidae and Turridae) (Taylor & Tay- lor, 1977; Taylor et al., 1980: 381-3). Corre- lated with this gradient, Dudley & Vermeij (1978: 439) showed a marked equatorward 178 KABAT increase in boring predation in Turritella. Sub- sequently Vermeij et al. (1989), for bivalve prey, actually observed an equatorward de- crease in the frequency of complete bore- holes (and a correlated equatorward increase in the frequency of incomplete boreholes); they suggested that the turritellids were an unexplained exception to this more general pattern. It appears that since the Cretaceous, the general mechanisms and consequences of naticid predation have not greatly changed. To be sure, the prey sources have changed, not only due to origination and extinction of prey taxa, but also because of changes in prey defense mechanisms. However, the overall “strategy” of naticid predation has per- sisted for the last 100 million years (Kitchell, 1987). It is possible that the naticids, following their late Cretaceous—early Tertiary adaptive radiation, have now reached their maximum taxonomic diversity (e.g. Sohl, 1969: fig. 1) and are at stasis which may lead to eventual decline in the absence of evolutionary inno- vations facilitating further expansion. The highly stereotyped nature of naticid predation suggests that their canalization may be so great as to preclude further breakthroughs (but consider the non-boring, suffocation pre- dation of Polinices mammilla). With the rise of muricids in the later Ter- tiary, the naticids may have shifted from gas- tropod to bivalve prey, as suggested by Ade- goke & Tevesz (1974). Hoffman et al. (1974) noted that in a Miocene assemblage, naticid boreholes were found mostly in smooth prey whereas muricid boreholes were primarily in ribbed (sculptured) prey; however the former prey are more likely to be infaunal than the latter, which may affect these results. Within the Maryland Miocene, Kelley (1982a) found that naticid predation shifted from predomi- nantly bivalve prey in the Calvert and Chop- tank formations to gastropod prey in the St. Marys Formation, correlated with the increase in diversity of prey gastropods in the latter formation. Kelley's results may be а preser- vational artifact, as the St. Mary’s has a much better representation of gastropods than do the earlier formations (С. J. Vermeij, т litt.). Clearly, one also needs to account for changes in the relative abundances of infau- nal prey sources; trends as suggested by Adegoke & Tevesz (1974) may not be appli- cable on a global scale. In addition, the study of naticids has been primarily in a few re- stricted habitats; more comprehensive analy- ses of tropical sub-littoral communities may show other naticid predation patterns. Kelley (1982a) suggested that extensive naticid and other predation on bivalves in- creased prey species diversity, perhaps by reducing competitive interactions. Although ecologists recognize several factors that af- fect species diversity, predation is undoubt- edly one of the more important, and one that can be easily recognized in the fossil record. Perturbation experiments involving predator- exclusion cages were used by Wiltse (1980b) to analyze the role of the western Atlantic Ne- verita duplicata in its community structure; she found that snail predation and distur- bance (due to burrowing) actually decreased the community species diversity by eliminat- ing the rare species and blocking strong com- petitive interactions. Kitchell and colleagues (Kitchell et al., 1981; Kitchell, 1982, 1983, 1986; DeAngelis et al., 1984, 1985, 1989) expanded upon their model of the energetics of naticid predation to de- velop models of coevolution of naticids and their prey. Coevolution, or the reciprocal evolutionary interactions of two taxa, is an im- portant, albeit difficult to quantify, aspect of evolutionary biology. There has been consid- erable disagreement as to how tightly or broadly coevolution should be defined or re- stricted. Indeed, almost any evolutionary trend can be “explained” as part of a coevolutionary process (Vermeij, 1982: 711-2). Instead of recognizing coevolution as “all evolution re- sulting from biological interactions,” it is much more useful to restrict it to “reciprocal adap- tation involving the heritable traits of two or more species” (Vermeij, 1983b: 311). These models of naticid-prey coevolution are sub- ject to the same caveats mentioned earlier under the discussion of the previous models. Nevertheless, | shall attempt to summarize their scenarios. First, one can hypothesize that some sorts of evolutionary “arms races” are involved, with the prey evolving various antipredatory adaptations, but with the predator also evolv- ing new or changed features. One conse- quence is that “multiple adaptive tactics pro- duce multiple directionality” (Kitchell et al., 1981: 550), meaning that diversity may result as different prey follow alternative strategies and the same is true for different predators. This may result in character displacement or other isolating mechanisms resulting in spe- ciation (Kitchell, 1983). A direct test of these coevolutionary pro- NATICID PREDATION 179 cesses, at least for naticid predators, was con- ducted by Kitchell (1982) who analyzed Marin- covich’s stratigraphic data for the eastern Pacific Neogene naticid fauna and concluded that predator “efficiency” increased over geo- logical time. Specifically, size, globosity and streamlining of the shell all increased, as did the proportion of apertural area to shell area and the general diversification of morphology (the latter not fully explained). In some re- spects these are all a consequence of general phyletic size increase, and may not be directly due to coevolution. Further refinements of their coevolutionary models predicted that in the absence of pred- ators, prey will reproduce early (i.e., at small sizes); whereas in the presence of predators, prey will show delayed reproduction at larger sizes (DeAngelis et al., 1984). More complex age-structured models tested the prey energy- allocation functions (growth vs. reproduction) as a consequence of predation levels, and resulted in three alternative ecological strate- gies for bivalve prey as coevolutionary re- sponses: delayed reproduction to large size, early reproduction, or increased shell thick- ness. Needless to say, the numerous assump- tions (DeAngelis et al., 1985: 836) severely constrain the value of their coevolutionary model. In particular, they assume that no other factors affect the population dynamics of the naticids or their prey; this overlooks other predators, disease and parasitism, and abiotic mortality sources, all of which (together and severally) are often of greater importance to the prey than are naticids, as has been doc- umented in the other studies discussed herein. Of course, with respect to the evolution of shell morphology, the latter factors are not easily measured or of great significance. The results of their models largely corroborated the con- clusions of previous ecological studies. Edge-boring of bivalve prey represents an escalation in the evolutionary “arms race” as an adaptive response to the presence of prey sculptural elements and shell-thicken- ing. Similarly, non-boring predation (suffoca- tion) also represents an alternative strategy (Ansell & Morton, 1987: 117); the selective advantages presumably entail a reduction in the energetic costs of boring. Further study should reveal whether some prey taxa are re- sistant to these novel predation mechanisms. The phylogenetic correlations of these two traits remain uncertain; at the present time, they are only known for a few species from the tropical Indo-Pacific. To briefly summarize these ecological stud- ies: (a) There is a general positive correlation between predator and prey size; size selec- tivity is shown as larger prey often have a size refuge from predation. (b) Prey defense mechanisms not only help prevent prey cap- ture, but also may lead to interruptions of predation as shown by incomplete boreholes in the prey shell. (c) The successful mode of naticid predation is limited by its seem- ing stereotypy (inflexibility). (d) The intrigu- ing possibilities of predator-prey coevolution (arms races) remain unproven for specific cases. FUTURE DIRECTIONS This review has suggested several areas needing further research. They are tabulated below; readers will undoubtedly recognize yet other problems amenable to future studies. The detection of prey by naticids remains a puzzle: elucidation of the potential interac- tions of chemosensory mechanisms (osphra- dium) vs. echolocation (Kitching & Pearson, 1981). Arelated mechanistic problem is to de- termine the precise biochemical constituents of the accessory boring organ secretion in naticids and the mode of function of shell dis- solution. More ecologically oriented approaches could include sophisticated field analyses of prey choice, entailing controlled manipula- tions and perturbation experiments (remove one species at a time). Further quantification of the various links of soft-bottom community food webs to determine more precisely the quantitative role of naticids in this habitat. De- velopment of methods of ecological control of naticid predators of shellfish. Paleontologists could analyze Paleocene faunas for gastropod boring predation; and conduct more detailed studies of Jurassic and Early Cretaceous faunas to supply informa- tion on changes in predation and shell form during that time (Vermeij, 1987: 238-9). Fur- ther study of the phylogenetic position of the Triassic shell borers and the early fossil record of naticids to unravel the complexities of the origin(s) of shell boring of the naticid type. Study of boring predation from the cold temperature southern oceans and the sub- Antarctic would be most desirable. The pres- ence of several phylogenetically primitive nat- 180 KABAT icid taxa in those faunas would provide further clues as to the relationships between naticid phylogeny and boring predation. It remains uncertain whether the most primitive subfam- ily, the Ampullospirinae [Triassic?—Recent] are shell borers. Further research on the geographical and phylogenetic extent of epifaunal predation, non-boring suffocation, and edge-boring would also add to our knowledge of the phy- logenetic correlations of predation mecha- nisms. CONCLUSIONS (A) Bored or punched holes in prey shells are made by nine taxa of marine predators: naticid, muricid & capulid snails, octopods, Pseudostylochus (Turbellaria) and Asemich- thys (Pisces), all in mollusk shells; cassid snails in echinoids; Okadaia (Nudibranchia) in calcareous polychaete tubes; and nematodes in foraminiferal tests. Some terrestrial zonitid snails are also shell-borers. Shell-crushing predators (sharks, crustaceans) sometimes leave holes in otherwise intact prey shells. (B) Following prey capture, naticid boring is accomplished by alternate application to the prey shell of the radula and the proboscoideal secretory accessory boring organ. The dis- tinctive naticid borehole is countersunk, with beveled edges. (C) The data on naticid prey show that many soft-bottom families of bivalves and gastropods are subject to naticid predation. Rocky-habitat taxa escape the infaunal natic- ids. (D) Boring predation potentially attributable to naticids originated in the Triassic but shortly became extinct. The naticid boring habit definitively evolved in the Late Creta- ceous and has been documented through Ho- locene faunas, with an unstudied gap in the Paleocene. No clear trends in rates of boring predation since the Cretaceous are obvious. (E) Most studies have shown a positive cor- relation between predator size and prey size; also, smaller prey are usually subject to higher rates of naticid predation. Incomplete boreholes reflect interruptions of predation; multiple boreholes demonstrate inflexible ste- reotypy of naticid boring. Prey defense can take several forms: leaping or burrowing; thick or sculptured shells; chemical defenses; growth to large size; and the corbulid con- chiolin layer. Non-boring predation, either through gaping shells or pedal suffocation, greatly confounds ecological studies since no signs of predation are left on the prey shell. (F) Naticid predation is an important and easily documented link in the food web of ma- rine soft-bottom communities; other predators often crush or remove their prey without leav- ing recognizable remains. (G) The evolution of naticid boring preda- tion is part of the Mesozoic marine revolution entailing the diversification of infaunal bi- valves and other gastropods which greatly in- creased naticid prey sources. Evolutionary escalation (defenses) on the part of prey taxa may have occurred since the Cretaceous; at- tempts to prove specific coevolutionary trends have been unsuccessful. ACKNOWLEDGEMENTS Preparation of this paper has been facili- tated by numerous colleagues who kindly pro- vided reprints of their papers on shell boring and related aspects of molluscan predation. For the loan of specimens, photographs, or negatives, | thank R. F. Ambrose (U.C. Santa Barbara), A. Garback (Academy of Natural Sciences, Philadelphia), R. Mooi (National Museum of Natural History, Washington, D.C.), P. B. Mordan and J. D. Taylor (British Museum (Natural History)) and S. F. Norton (Friday Harbor Laboratories). S. P. Kool, G. Rosenberg, S. Vogel and E. O. Wilson pro- vided helpful comments on several aspects of this paper. | greatly appreciate the extensive discussion and review of the manuscript by K. J. Boss, A. H. Knoll, A. J. Kohn, J. D. Taylor, R. D. Turner, G. J. Vermeij and an anony- mous reviewer. LITERATURE CITED ABE, N., 1985, Breeding of Thais clavigera (Kuster) and predation of its eggs by Cronia margariticola (Broderip). Pp. 381-392, in, Proceedings of the Second International Workshop on the Malaco- fauna of Hong Kong and Southern China. (Eds. B. Morton & D. Dudgeon). Hong Kong: Hong Kong University Press. ADEGOKE, О. S. & М. J. $. TEVESZ, 1974. Gas- tropod predation patterns in the Eocene of Nige- ria. Lethaia, 7:17-24. AGERSBORG, H. P. K. 1920, The utilization of echinoderms and of gasteropod mollusks. The American Naturalist, 54: 414—426. AITKEN, A. E. & M. J. RISK, 1988, Biotic interac- NATICID PREDATION 181 tions revealed by macroborings in Arctic bivalve molluscs. Lethaia, 21: 339-350. AMBROSE, R. F. 1986, Effects of octopus preda- tion on motile invertebrates in a rocky subtidal community. Marine Ecology—Progress Series, 30: 261-273. AMBROSE, R. F., B. J. LEIGHTON & E. B. HARTWICK, 1988, Characterization of boreholes by Octopus dofleini in the bivalve Saxidomus gi- ganteus. Journal of Zoology, 214: 491-503. ANKEL, W. E., 1938, Erwerb und Aufnahme der Nahrung bei den Gastropoden. Zoologischer An- zeiger, Supplementband 11, Verhandlungen der Deutschen Zoologischen Gesellschaft, 40: 223— 295. ANSELL, A. D., 1960, Observations on predation of Venus striatula (Da Costa) by Natica alderi (Forbes). Proceedings of the Malacological Soci- ety of London, 34: 157-164, pl. 9. ANSELL, A. D., 1961, Egg capsules of the dogfish (Scylliorhinus canicula, Linn.) bored by Natica (Gastropoda, Prosobranchia). Proceedings of the Malacological Society of London, 34: 248— 249. ANSELL, A. D., 1969, Defensive adaptations to predation in the Mollusca. Proceedings of the Symposium on Mollusca, Cochin, 2: 487-512. Mandapam: Marine Biological Association of In- dia. ANSELL, A. D., 1982a, Experimental studies of a benthic predator-prey relationship. |. Feeding, growth, and egg-collar production in long-term cultures of the gastropod drill Polinices alderi (Forbes) feeding on the bivalve Tellina tenuis (da Costa). Journal of Experimental Marine Biology and Ecology, 56: 235-255. ANSELL, A. D., 1982b, Experimental studies of a benthic predator-prey relationship. Il. Energetics of growth and reproduction, and food-conversion efficiencies, in long-term cultures of the gastro- pod drill Polinices alderi (Forbes) feeding on the bivalve Tellina tenuis (da Costa). Journal of Ex- perimental Marine Biology and Ecology, 61: 1- 29. ANSELL, A. D., 1982c, Experimental studies of a benthic predator-prey relationship: Ш. Factors affecting rates of predation and growth in juve- niles of the gastropod drill Polinices catena (da Costa) in laboratory cultures. Malacologia, 22: 367-375. ANSELL, A. D., 1983, Prey selection by the naticid gastropod, Polinices catena. Journal of Mollus- can Studies, Supplement, 12A: 1. ANSELL, A. D. & A.-M. MACE, 1978, Comparative studies of the gastropod, Polinices alderi from Mediterranean and North Atlantic populations. Haliotis, 9: 65-72. ANSELL, A. D. & B. MORTON, 1985, Aspects of naticid predation in Hong Kong with special ref- erence to the defensive adaptations of Bassina (Callanaitis) calophylla (Bivalvia). Pp. 635-660, in, Proceedings of the Second International Workshop on the Malacofauna of Hong Kong and Southern China. (Eds. B. Morton & D. Dudgeon). Hong Kong: Hong Kong University Press. ANSELL, A. D. & B. MORTON, 1987, Alternative predation tactics of a tropical naticid gastropod. Journal of Experimental Marine Biology and Ecology, 111: 109-119. ARNOLD, A. J., F. D'ESCRIVAN & W. C. PARKER, 1985, Predation and avoidance responses in the Foraminifera of the Galapagos hydrothermal mounds. Journal of Foraminiferal Research, 15: 38—42. ARUA, I., 1989, Gastropod predators and their di- etary preference in an Eocene molluscan fauna from Nigeria. Palaeogeography, Palaeoclimatol- ogy, Palaeoecology, 72: 283-290. ARUA, I. & M. HOQUE, 1987, Predation intensity in an Eocene molluscan assemblage from south- eastern Nigeria. Geologie en Mijnbouw, 66: 293— 296. ARUA, |. & M. HOQUE, 1989a, Predatory gastro- pod boreholes in an Eocene molluscan assem- blage from Nigeria. Lethaia, 22: 49-59. ARUA, |. & M. HOQUE, 1989b, Study of the shape of naticid and muricid borings in plan view in Eocene prey from Southeastern Nigeria. Palae- ogeography, Palaeoclimatology, Palaeoecology, 72: 357-362. ARUA, |. & М. HOQUE, 1989c, Fossil predaceous gastropod borings from Nigeria. Palaeogeogra- phy, Palaeoclimatology, Palaeoecology, 73: 175—183. BANDEL, K., 1988, Early ontogenetic shell and shell structure as aids to unravel gastropod phy- logeny and evolution. Malacological Review, Supplement, 4: 267-722. BAYLISS, D. E., 1986, Selective feeding on bi- valves by Polinices alderi (Forbes) (Gastropoda). Ophelia, 25: 33-47. BEEBE, W., 1932, Snail folk. Nature Magazine, 19: 207-212, 262-263. [Reprinted, pp. 204-223, in Nonsuch: land of water. New York: Blue Ribbon Books]. BENTON, M. J., 1986, Predation by drilling gastro- pods. Nature, 321: 110-111. BERG, C. J., Jr., 1975, A comparison of adaptive strategies of predation among naticid gastro- pods. Biological Bulletin, 149(2): 420—421. BERG, C. J., Jr., 1976, Ontogeny of predatory be- havior in marine snails (Prosobranchia: Nati- cidae). The Nautilus, 90: 1—4. BERG, С. J., Jr. & $. NISHENKO, 1975, Stereotypy of predatory boring behavior of Pleistocene nat- icid gastropods. Paleobiology, 1: 258-260. BERG, C. J., Jr. & M. J. PORTER, 1974, A com- parison of predatory behaviors amoung the nat- icid gastropods Lunatia heros, Lunatia triseriata and Polinices duplicatus. Biological Bulletin, 147: 469—470. BERNARD, Е. R., 1967, Studies on the biology of the naticid clam drill Polinices lewisi (Gould) (Gastropoda Prosobranchiata). Fisheries Re- search Board of Canada, Technical Report, 42: 1-41. 182 KABAT BERNARD, F. R. & J. W. BAGSHAW, 1969, His- tology and fine structure of the accessory boring organ of Polinices lewisi (Gastropoda, Proso- branchiata). Journal of the Fisheries Research Board of Canada, 26: 1451-1457. BERRY, A. J., 1982, Predation by Natica maculosa Lamarck (Naticidae: Gastropoda) upon the tro- chacean gastropod Umbonium vestiarium (L.) on a Malaysian shore. Journal of Experimental Ma- rine Biology and Ecology, 64: 71-89. BERRY, A. J., 1983, Oxygen consumption and as- pects of energetics in a Malaysian population of Natica maculosa Lamarck (Gastropoda) feeding on the trochacean gastropod Umbonium vestia- rium (L.). Journal of Experimental Marine Biology and Ecology, 66: 93-100. BEU, A. G., В. А. HENDERSON & С. $. NELSON, 1972, Notes on the taphonomy and paleoecology of New Zealand Tertiary Spatangoida. New Zealand Journal of Geology and Geophysics, 15: 275-286. BISHOP, G. A., 1975, Traces of Predation. Pp. 261-281, in, The study of trace fossils. (Ed. В. W. Frey). New York: Springer-Verlag. BOEKSCHOTEN, G. J., 1966, Shell borings of ses- sile epibiontic organisms as palaeoecological guides (with examples from the Dutch coast). Palaeogeography, Palaeoclimatology, Palaeo- ecology, 2: 333-379. BOEKSCHOTEN, G. J., 1967, Palaeoecology of some Mollusca from the Tielrode Sands (Pliocene, Belgium). Palaeogeography, Palaeo- climatology, Palaeoecology, 3: 311-362. BOGGS, С. H., J. A. RICE, J. A. KITCHELL & J. F. KITCHELL, 1984, Predation at a snail’s pace: what's time to a gastropod? Oecologia, 62: 13— 17. BOUCOT, A. J., 1981, Principles of benthic marine paleoecology. New York: Academic Press. xvi + 463 pp. BROMLEY, R. G., 1981, Concepts in ichnotaxon- omy illustrated by small round holes in shells. Acta Geológica Hispánica, 16: 55-64. BROOM, M. J., 1982, Size-selection, consumption rates and growth of the gastropods Natica mac- ulosa (Lamarck) and Thais carinifera (Lamarck) preying on the bivalve, Anadara granosa (L.). Journal of Experimental Marine Biology and Ecology, 56: 213-233. BROOM, M. J., 1983, A preliminary investigation into prey species preference by the tropical gas- tropods Natica maculosa Lamarck and Thais car- inifera (Lamarck). Journal of Molluscan Studies, 49: 43-52. BURCH, B. & T. A. BURCH, 1986, Predation by Naticidae after a devastating storm in Pinna beds of Waikiki, Oahu, Hawaii 1980. Western Society of Malacologists, Annual Report, 18: 9. CADEE, G. C., 1968, Molluscan biocoenoses and thanatocoenoses in the Ria de Arosa, Galicia, Spain. Zoologische Verhandelingen, 95: 1-121, 6 pls. CARRIKER, M. R., 1961, Comparative functional morphology of boring mechanisms in gastro- pods. American Zoologist, 1: 263-266. CARRIKER, M. R., 1981, Shell penetration and feeding by naticacean and muricacean predatory gastropods: a synthesis. Malacologia, 20: 403— 422. CARRIKER, M. R. & L. G. WILLIAMS, 1978, The chemical mechanism of shell dissolution by pred- atory boring gastropods: a review and an hypoth- esis. Malacologia, 17: 143-156. CARRIKER, M. В. & Е. |. YOCHELSON, 1968, Recent gastropod boreholes and Ordovician cy- lindrical borings. U. S. Geological Survey, Pro- fessional Paper, 593-B: 1-26, pls. 1-5. CARTER, R. M. 1968, On the biology and palae- ontology of some predators of bivalved Mollusca. Palaeogeography, Palaeoclimatology, Palaeo- ecology, 4: 29-65. CHATTERTON, B. D. E. & H. L. WHITEHEAD, 1987, Predatory borings in the inarticulate bra- chiopod Artiotreta from the Silurian of Oklahoma. Lethaia, 20: 67-74. CHRISTENSEN, A. M., 1970, Feeding biology of the sea-star Astropecten irregularis Pennant. Ophelia, 8: 1-134. CLARKE, А. H., Jr., 1956, Natural biological control of a Mya predator. The Nautilus, 70: 37-38. COLBATH, S. L., 1985, Gastropod predation and depositional environments of two molluscan communities from the Miocene Astoria Formation at Beverly Beach State Park, Oregon. Journal of Paleontology, 59: 849-869. COMMITO, J. A., 1982, Effects of Lunatia heros predation on the population dynamics of Mya arenaria and Macoma balthica in Maine, USA. Marine Biology, 69: 187—193. COMMITO, J. A., 1987, Polinices predation pat- terns and Mercenaria morphology models. The American Naturalist, 129: 449—451. COMMITO, J. A. & W. G. AMBROSE, Jr., 1985, Predatory infauna and trophic complexity in soft- bottom communities. Pp. 323-333, in, Proceed- ings of the Nineteenth European Marine Biology Symposium. (Ed. P. E. Gibbs). Cambridge: Cam- bridge University Press. CROLL, R. P., 1983, Gastropod chemoreception. Biological Reviews, 58: 293-319. DARRAGH, T. A. & G. W. KENDRICK, 1980, Eocene bivalves from the Pallinup Siltstone near Walpole, Western Australia. Journal of the Royal Society of Western Australia, 63: 5-20. DEANGELIS, D. L., J. A. KITCHELL & W. M. POST, 1985, The influence of naticid predation on evolutionary strategies of bivalve prey: con- clusions from a model. The American Naturalist, 126: 817-842. DEANGELIS, D. L., J. A. KITCHELL & W. M. POST, 1987, Reply to Commito. The American Naturalist, 130: 458—460. ОЕАМСЕЦ$, D. L., J. A. KITCHELL & W. M. POST, 1989, The nature of stasis and change: potential coevolutionary dynamics. In, Coevolu- NATICID PREDATION 183 tion of Ecosystems. (Ed. N. Stenseth). Cam- bridge: Cambridge University Press. DEANGELIS, D. L., J. A. KITCHELL, W. M. POST & C. C. TRAVIS, 1984, A model of naticid gas- tropod predator-prey coevolution. Mathematical Ecology, 54: 120-135. DE CAUWER, G., 1985, Gastropod predation on corbulid bivalves: palaeoecology or taphonomy? Annales de la Société Royale Zoologique de Bel- gique, 115: 183-196. DUDLEY, E. C. & E. C. DUDLEY, 1980, Drilling predation on some Miocene marine mollusks. The Nautilus, 94: 63—66. DUDLEY, Е. С. & С. J. VERMEIJ, 1978, Predation in time and space: drilling in the gastropod Tur- ritella. Paleobiology, 4: 436-441. EDWARDS, D. C., 1969, Predators on Olivella bi- plicata, including a species-specific predator avoidance response. The Veliger, 11: 326-333, pl. 51. EDWARDS, D. C., 1975, Preferred prey of Polin- ices duplicatus in Cape Cod inlets. Bulletin of the American Malacological Union, Inc., 40: 17-20. EDWARDS, D. C. & J. D. HUEBNER, 1977, Feed- ing and growth rates of Polinices duplicatus prey- ing on Mya arenaria at Barnstable Harbor, Mas- sachusetts. Ecology, 58: 1218-1236. EKDALE, A. A., R. G. BROMLEY & S. G. PEM- BERTON, 1984, Ichnology: the use of trace fos- sils in sedimentology and stratigraphy. Society of Economic Paleontologists and Mineralogists, Short Course, 15: 1-317. FANKBONER, P. V., 1969, Naticid predation on Dentalium complexum (Dentaliidae, Sca- phopoda). Hawaiian Shell News, 17(6): 3. FATTON, E. & J. ROGER, 1968, Les organismes perforants: vue d'ensemble sur les actuels et les fossiles. Université de Paris, Faculté des Sci- ences d'Orsay, Travaux du Laboratoire de Pale- ontologie, 13-53. FISCHER, P.-H., 1922, Sur les gastéropodes per- ceurs. Journal de Conchyliologie, 67: 1-56. FISCHER, P.-H., 1960, Action des gastéropodes perceurs sur un bivalve de l'Etage Lutétien. Jour- nal de Conchyliologie, 100: 129-131. FISCHER, P.-H., 1962a, Perforations de fossiles Pré-Tertiaries attribuées a des gastéropodes pré- dateurs. Journal de Conchyliologie, 102: 68-78. FISCHER, P.-H., 1962b, Action des gastéropodes perceurs sur des Mesalia de l'Etage Lutétien. Journal de Conchyliologie, 102: 95-97. FISCHER, P.-H., 1963, Corbules fossiles perforées par des gastéropodes prédateurs. Journal de Conchyliologie, 103: 29-31. FISCHER, P.-H., 1966, Perforations de fossiles Tertiaires par des gastéropodes prédateurs. Journal de Conchyliologie, 105: 66-96. FLOWER, F. B., 1954, A new enemy of the oyster drill. Science, 120: 231-232. FRANZ, D. R., 1977, Size and age-specific preda- tion by Lunatia heros (Say, 1822) on the surf clam Spisula solidissima (Dillwyn, 1817) off Western Long Island, New York. The Veliger, 20: 144-150. FRETTER, V. 8 A. GRAHAM, 1962, British proso- branch molluscs: their functional anatomy and ecology. London: The Ray Society. xvi + 755 pp. FRETTER, V. & В. MANLY, 1979, Observations on the biology of some sublittoral prosobranchs. Journal of Molluscan Studies, 45: 209-218. FREY, В. W., J. D. HOWARD 4 J.-S. HONG, 1987 ["1986”], Naticid gastropods may kill solenid bi- valves without boring: ichnologic and taphonomic consequences. Palaios, 1: 610—612. FURSICH, F. T., & D. JABLONSKI, 1984, Late Tri- assic naticid drillholes: carnivorous gastropods gain a major adaptation but fail to radiate. Sci- ence, 224: 78-80. FURSICH, Е. Т., & J. WENDT, 1977, Biostratinomy and palaeoecology of the Cassian Formation (Triassic) of the Southern Alps. Palaeogeogra- phy, Palaeoclimatology, Palaeoecology, 22: 257-323. GALLENI, L., P. TONGIORGI, E. FERRERO & U. SALGHETTI, 1980, Stylochus mediterraneus (Turbellaria: Polycladia), predator on the mussel Mytilus galloprovincialis. Marine Biology, 55: 317-326. GEORGE, C. J., 1965, The use of beached valves of the lamellibranch molluscs Glycimeris glycim- eris (L.), Donax semistriatus Poli and Donax trun- culus L. for the determination of percentage mor- tality by Natica spp. Doriana, Supplemento agli Annali del Museo Civico di Storia Naturale “G. Doria”, 4(164): 1-8. GONOR, J. J., 1965, Predator-prey reactions be- tween two marine prosobranch gastropods. The Veliger, 7: 228-232. GREEN, В. H., 1968, Mortality and stability in a low diversity subtropical intertidal community. Ecol- ogy, 49: 848—854. GRIFFITHS, R. J., 1981, Predation on the bivalve Choromytilus meridionalis (Kr.) by the gastropod Natica (Tectonatica) tecta Anton. Journal of Mol- luscan Studies, 47: 112-120. GUERRERO, S. 8 R. A. REYMENT, 1988a, Pre- dation and feeding in the naticid gastropod Nati- carius intricatoides (Hidalgo). Palaeogeography, Palaeoclimatology, Palaeoecology, 68: 49-52. GUERRERO, S. & R. A. REYMENT, 1988b, Differ- entiation between the traces of predation of mu- ricids and naticids in Spanish Pliocene Chlamys. Estudios Geológicos, Instituto de Investigaciones Geológicas “Lucas Mallada”, Madrid, 44(3-4): 317-328. HANKS, J. E., 1953, The effect of changes in water temperature and salinity on the feeding habits of the boring snails, Polinices heros and Polinices duplicata. Fifth Report on Investigations of the Shellfisheries of Massachusetts, pp. 33—47. HANTZCHEL, W., 1975, Trace fossils and problem- atica, second edition. In Treatise on Invertebrate Paleontology, Part W, Miscellanea, Supplement, 1: xxii + W1-W269. (Ed. С. Teichert). Boulder: Geological Society of America. 184 KABAT HAYASAKA, |., 1933, Fossil occurrence of pelecy- pod shells bored by certain gastropods. Memoirs of the Faculty of Science and Agriculture, Taihoku Imperial University, 6(4): 65-70, pls. 1[XV111]-4[XX1]. HICKMAN, C. S., 1983, Radular patterns, system- atics, diversity, and ecology of deep-sea limpets. The Veliger, 26: 73-92. HINGSTON, J. P., 1985, Predation patterns among molluscs in the Victorian Tertiary. Proceedings of the Royal Society of Victoria, 97: 49-57. HOFFMAN, A., 1967a, Mortality patterns of some bivalves from the Badenian (Miocene) Korytnica Clays, Poland. Neues Jahrbuch fúr Geologie und Paläontologie, Monatshefte, 1976(5): 337— 349. HOFFMAN, A., 1976b, Mortality patterns of some gastropods from the Badenian (Miocene) Koryt- nica Clays, Poland. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen, 152: 293- 306. HOFFMAN, A. & J. MARTINELL, 1984, Prey selec- tion by naticid gastropods in the Pliocene of Em- porda (Northeast Spain). Neues Jahrbuch für Geologie und Paläontologie, Monatshefte, 1984(7): 393-399. HOFFMAN, A. & B. SZUBZDA, 1976, Paleoecol- ogy of some molluscan assemblages from the Badenian (Miocene) marine sandy facies of Po- land. Palaeogeography, Palaeoclimatology, Palaeoecology, 20: 307-332. HOFFMAN, A., A. PISERA & M. RYSZKIEWICZ, 1974, Predation by muricid and naticid gastro- pods on the Lower Tortonian mollusks from the Korytnica clays. Acta Geologica Polonica, 24: 249-260, pls. 1-4. HUEBNER, J. D. & D.C. EDWARDS, 1981, Energy budget of the predatory marine gastropod Polin- ices duplicatus. Marine Biology, 61: 221-226. HUGHES, В. N., 1985, Predatory behaviour of Nat- ica unifasciata feeding intertidally on gastropods. Journal of Molluscan Studies, 51: 331-335. HUGHES, В. М. & H. P. 1. HUGHES, 1981, Mor- phological and behavioural aspects of feeding in the Cassidae (Tonnacea, Mesogastropoda). Ma- lacologia, 20: 385—402. HUTCHINGS, J. A. & R. L. HAEDRICH, 1984, Growth and population structure in two species of bivalves (Nuculanidae) from the deep sea. Ma- rine Ecology Progress Series, 17: 135-142. ILINA, L. G., 1987, Evidence of boring in shells of brackish-water gastropods. Paleontological Jour- nal, 21(3): 23-30. (ICZN) INTERNATIONAL COMMISSION ON ZOO- LOGICAL NOMENCLATURE, 1985, Interna- tional Code of Zoological Nomenclature, Third Edition. Berkeley: University of California Press. xx + 338 pages. JACKSON, J. B. C., 1972, The ecology of the mol- luscs of Thalassia communities, Jamaica, West Indies. |. Molluscan population variability along an environmental stress gradient. Marine Biol- ogy, 14: 304-337. JACOBSON, M. K., 1965, Double-drilled clams. New York Shell Club Notes, 111: 5-6. JACOBSON, M. K., 1968, Preliminary results of a study on the placement of Polinices holes in the shells of Spisula solidissima at Rockaway, N.Y. New York Shell Club Notes, 140: 6-7. JENSEN, A. S., 1951, Do the Naticidae (Gas- tropoda Prosobranchia) drill by chemical or by mechanical means? Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening, Kobenhavn, 113: 251-261. JONES, M. L., 1969, Boring of shell by Caobangia in freshwater snails of southeast Asia. American Zoologist, 9: 829-835. КАВАТ, А. В. & A. J. KOHN, 1986, Predation on Early Pleistocene naticid gastropods in Fiji. Palaeogeography, Palaeoclimatology, Palaeo- ecology, 53: 255-269. KELLEY, P. H., 1982a, The effect of predation on Miocene mollusc populations of the Chesapeake Group. Florida Bureau of Geology, Special Pub- lication, 25: 35—48. KELLEY, P. H., 1982b, Prey preference of naticid gastropods of the Chesapeake Group: taxonomic and stratigraphic patterns. Geological Society of America Abstracts with Programs, 14: 527. KELLEY, Р. H., 1984, Coevolution in a naticid gas- tropod predator-prey system: relation of preda- tion intensity to rates of prey evolution. Geologi- cal Society of America Abstracts with Programs, 162557 KELLEY, P. H., 1987, Naticid gastropod prey pref- erence and predator-avoidance strategies of Chesapeake Group bivalves. Geological Society of America Abstracts with Programs, 19: 724. KELLEY, P. H., 1989a ["1988”], Predation by Mi- ocene gastropods of the Chesapeake Group: stereotyped and predictable. Palaios, 3: 436— 448. KELLEY, P. H., 1989b, Evolutionary trends within bivalve prey of Chesapeake Group naticid gas- tropods. Historical Biology, 2: 139-156. KITCHELL, J. A., 1982, Coevolution in a predator- prey system. Third North American Paleontolog- ical Convention, Proceedings, 2: 301-305. KITCHELL, J. A., 1983, An evolutionary model of predator-mediated divergence and coexistence. Geological Society of America Abstracts with Programs, 15: 614. KITCHELL, J. A., 1986, The evolution of predator- prey behavior: naticid gastropods and their mol- luscan prey. Pp. 88-110, in Evolution of Animal Behavior: Paleontological and Field Approaches. (Eds. M. H. Nitecki & J. A. Kitchell). New York: Oxford University Press. KITCHELL, J. A., 1987, Naticid predation within Cenozoic molluscan communities. American Ma- lacological Union Program and Abstracts, 53rd Annual Meeting, p. 14. KITCHELL, J. A., C. H. BOGGS, J. F. KITCHELL & J. A. RICE, 1981, Prey selection by naticid gas- tropods: experimental tests and application to the fossil record. Paleobiology, 7: 533-552. NATICID PREDATION 185 KITCHELL, J. А., С. Н. BOGGS, J. A. RICE, J. Е. KITCHELL, A. HOFFMAN & J. MARTINELL, 1986, Anomalies in naticid predatory behavior: a critique and experimental observations. Malaco- logia, 27: 291-298. KITCHING, В. L. & J. PEARSON, 1981, Prey loca- tion by sound in a predatory intertidal gastropod. Marine Biology Letters, 2: 313-321. KLÄHN, H., 1932, Der Bohrakt fossiler bohrender Schnecken und das Vernichtungsmass durch ráuberische Gastropoden des Sternberger Oli- gozáns. Sitzungsberichte und Abhhandlungen der Naturforschenden Gesellschaft zu Rostock, 3: 89-103. KOHN, A. J., 1961, Chemoreception т gastropod molluscs. American Zoologist, 1: 291-308. KOHN, A. J., 1983, Feeding biology of gastropods. Pp. 1-63, in, The Mollusca, 5, Physiology, Part 2. (Eds. A. S. M. Saleuddin 8 K. M. Wilbur). New York: Academic Press. ° KOHN, А. J., 1985, Gastropod paleoecology. Pp. 174—189, in, Mollusks: Notes for a short course. University of Tennessee, Studies in Geology, 13. (Eds. D. J. Bottjer et al.). KOJUMDJIEVA, E., 1974, Les Gasteropodes per- ceurs et leurs victimes du Miocene de Bulgarie du Nord-Ouest. Bulgarian Academy of Sciences, Bulletin of the Geological Institute, Series Pale- ontology, 23: 5—24, pls. 1—4. KORNICKER, L. S., C. D. WISE & J. M. WISE, 1963, Factors affecting the distribution of oppos- ing mollusk valves. Journal of Sedimentary Pe- trology, 33: 703-712. KORRINGA, P., 1952, Recent advances in oyster biology. Quarterly Review of Biology, 27: 266-— 308, 339-365. LAWS, H. M. & D. F. LAWS, 1972, The escape response of Donacilla angusta Reeve (Mollusca: Bivalvia) in the presence of a naticid predator. The Veliger, 14: 289-290. LEIDY, J., 1878, Remarks on Mactra. Proceedings of the Academy of Natural Sciences of Philadel- рта for 1878: 332-333. LEVER, J. & В. THIJSSEN, 1968, Sorting phenom- ena during the transport of shell valves on sandy beaches studied with the use of artificial valves. Pp. 259-271, in, Studies in the structure, physi- ology, and ecology of molluscs. Symposia of the Zoological Society of London, 22. (Ed. V. Fretter). LEVER, J., A. KESSLER, P. VAN OVERBEEKE & R. THIJSSEN, 1961, Quantitative beach re- search. Il. The “hole effect”: a second mode of sorting of lamellibranch valves on sandy beaches. Netherlands Journal of Sea Research, 1: 339-358. LEWY, Z. & C. SAMTLEBEN, 1979, Functional morphology and palaeontological significance of the conchiolin layers in corbulid pelecypods. Lethaia, 12: 341-351. LIVAN, M., 1937, Uber Bohr-Lôcher an rezenten und fossilen Invertebraten. Senckenbergiana, 19: 138—150, 314. MACE, A.-M., 1978, Note préliminaire sur les fac- teurs influegant la sélection des proies chez le gastéropode perceur Polinices alderi (Forbes). Haliotis, 9: 61-64. _ MACE, A.-M., 1981a, Etude expérimentale de l'éc- ophysiologie d'un gastéropode perceur, Polin- ices alderi (Forbes). 1. Alimentation, Croissance, Reproduction. Téthys, 10: 63-72. MACE, A.-M., 1981b, Etude expérimentale de Гес- ophysiologie d'un gastéropode perceur, Polin- ices alderi (Forbes). 2. Respiration et Excrétion azotée. Téthys, 10: 73-82. MACE, A.-M., 1981c, Etude expérimentale de Гес- ophysiologie d'un gastéropode perceur, Polin- ¡ces alderi (Forbes). 3. Bilan énergétique. Téthys, 10: 117—120. MACE, A.-M. & А. D. ANSELL, 1982, Respiration and nitrogen excretion of Polinices alderi (Forbes) and Polinices catena (da Costa) (Gas- tropoda: Naticidae). Journal of Experimental Ma- rine Biology and Ecology, 60: 275-292. MADDOCKS, R. F., 1988, One hundred million years of predation on ostracods: the fossil record in Texas. Pp. 637—657, in, Evolutionary Biology of Ostracoda. Developments in Palaeontology and Stratigraphy, 11. (Eds. T. Hanai et al.). Am- sterdam: Elsevier. MAPES, РВ. H., Т. В. FAHRER & L. Е. BABCOCK, 1989, Sublethal and lethal injuries of Pennsylva- nian conulariids from Oklahoma. Journal of Pa- leontology, 63: 34-37. MARGOLIN, A. S., 1975, Responses to sea stars by three naticid gastropods. Ophelia, 14: 85-92. MARTINELL, J. & M. J. MARQUINA, 1980 ["1978"], Señales de depredación en los Gas- tropoda procedentes de un yacimiento pliocénico de Molins de Rei (Barcelona).—Implicaciones paleoecológicas. Acta Geológica Hispánica, 13(4): 125-128. MARTINELL, J. & J. DE PORTA 1980, Observa- ciones sobre la depredación en Chamelea gall- ina (Linne) procedentes de Salou (Tarragona). Comunicaciones del Primer Congreso Nacional de Malacologia (1979), Madrid: 75-78. MARTINELL, J. & J. DE PORTA, 1982, Observa- tions on the molluscan thanatocoenoses from Platja Llarga (Salou, Spain). Malacologia, 22: 587-591. MATSUKUMA, A., 1976, Predation by Recent nat- icid snails of two species of Glycymeris (Bi- valvia). Report of Fishery Research Laboratory, Kyushu University, Fukuoka, 3: 15-31. MATSUKUMA, A., 1978, Fossil boreholes made by shell-boring predators or commensals. |. Bore- holes of capulid gastropods. Venus, 37: 29—45. MAXWELL, P. A., 1988, Late Miocene deep-water Mollusca from the Stillwater Mudstone at Grey- mouth, Westland, New Zealand: paleoecology and systematics. New Zealand Geological Sur- vey Paleontological Bulletin, 55: 1-120, 13 pls. MEDCOF, J. С. 8 L. W. THURBER, 1958, Trial control of the greater clam drill (Lunatia heros) by manual collection. Journal of the Fisheries Re- search Board of Canada, 15: 1355-1369. 186 KABAT MORDAN, P. B., 1977, Factors affecting the distri- bution and abundance of Aegopinella and Neso- vitrea (Pulmonata: Zonitidae) at Monks Wood National Nature Reserve, Huntingdonshire. Bio- logical Journal of the Linnean Society, 9: 59-72. MUKAI, H., 1973, Predators of the benthic bivalves on the muddy bottom in the Inland Sea of Japan. |. The effect of the predation of Neverita reiniana (Dunker) on Veremolpa micra (Pilsbry). Venus, 31: 147-156. NAKAMINE, T. & T. HABE, 1983, Shells. of Tellinella virgata (Linnaeus) bored by the moon shell. Chirobotan, 14: 26. [in Japanese]. NEGUS, M., 1975, An analysis of boreholes drilled by Natica catena (da Costa) in the valves of Donax vittatus (da Costa). Proceedings of the Malacological Society of London, 41: 353-356. NEWTON, C. R., 1983, Triassic origin of shell- boring gastropods. Geological Society of Amer- ica Abstracts with Programs, 15: 652-653. NEWTON, С. R., M. T. WHALEN, J. В. THOMP- SON, N. PRINS & D. DELALLA, 1987, System- atics and paleoecology of Norian (Late Triassic) bivalves from a tropical island arc: Wallowa Ter- rane, Oregon. The Paleontological Society Mem- oir 22, Journal of Paleontology, 61(4), Supple- ment: 1-83. NIXON, M. & E. MACONNACHIE, 1988, Drilling by Octopus vulgaris (Mollusca: Cephalopoda) in the Mediterranean. Journal of Zoology, 216: 687- 716. NORTON, S. F., 1988, Role of the gastropod shell and operculum in inhibiting predation by fishes. Science, 241: cover, 92-94. PAINE, R. T., 1963, Trophic relationships of 8 sym- patric predatory gastropods. Ecology, 44: 63-73. PAPP, A., H. ZAPFE, F. BACHMAYER & A. F. TAUBER, 1947, Lebensspuren mariner Krebse. Akademie der Wissenschaften in Wien, Mathe- matisch-naturwissenschaftliche Klasse, Sit- zungsberichte, Abteilung I, Mineralogie, Biologie, Erdkunde, 155: 281-317. PELSENEER, P., 1924, Comment mangent divers gastropodes aquatiques. |—gastropodes marins carnivores Natica et Purpura. Annales de la So- ciété Royale Zoologique de Belgique, 55: 31-43. PENNEY, A. J. & C. L. GRIFFITHS, 1984, Prey selection and the impact of the starfish Marthas- terias glacialis (L.) and other predators on the mussel Choromytilus meridionalis (Krauss). Journal of Experimental Marine Biology and Ecology, 75: 19-36. PERRY, L. M., 1940, Marine shells of the southwest coast of Florida. Bulletins of American Paleontol- ogy, 26(95): 1-260, pls. 1-40. PETERSON, C. H., 1982, The importance of pre- dation and intra- and interspecific competition in the population biology of two infaunal suspen- sion-feeding bivalves, Protothaca staminea and Chione undatella. Ecological Monographs, 52: 437-475. PIERON, H., 1933, Notes ethologiques sur les gas- téropodes perceurs et leur comportement avec utilisation de méthodes statistiques. Archives de Zoologie Expérimentale et Générale, 75(1): 1- 20, pl. 1. REID, В. С. В. 8 В. D. GUSTAFSON, 1989, Update on feeding and digestion in the moon snail Polin- ices lewisii (Gould, 1847). The Veliger, 32: 327. REID, R. С. В. & J. A. FRIESEN, 1980, The diges- tive system of the moon snail Polinices lewisii (Gould, 1847) with emphasis on the role of the oesophageal gland. The Veliger, 23: 25-34. REYMENT, R. A., 1966, Preliminary observations on gastropod predation in the western Niger delta. Palaeogeography, Palaeoclimatology, Palaeoecology, 2: 81-102. ВЕУМЕМТ, В. A., 1967, Paleoethology and fossil drilling gastropods. Transactions of the Kansas Academy of Sciences, 70: 33-50. REYMENT, R. А., Е. В. REYMENT & A. НОМС- STEIN, 1987, Predation by boring gastropods on Late Cretaceous and Early Palaeocene ostra- cods. Cretaceous Research, 8: 189-209. RICHTER, G., 1962, Beobachtungen zum Beute- fang der marinen Bohrschnecke Lunatia nitida. Natur und Museum, 92: 186-192. ROBBA, E. & F. OSTINELLI, 1975, Studi paleoeco- logici sul Pliocene Ligure. |. Testimonianze di predazione sui molluschi Pliocenici di Albenga. Rivista Italiana di Paleontologia e Stratigrafia, 81: 309-372, pls. 41—48. RODRIGUES, C. L., 1986, Predation of the naticid gastropod, Neverita didyma (Roding), on the bi- valve, Ruditapes philippinarum (Adams & Reeve): evidence for a preference linked func- tional response. Publications from the Amakusa Marine Biological Laboratory, Kyushu University, 8: 125-141. RODRIGUES, C. L., S. NOJIMA & T. KIKUCHI, 1987, Mechanics of prey size preference in the gastropod Neverita didyma preying on the bi- valve Ruditapes philippinarum. Marine Ecology Progress Series, 40: 87-93. ROSEWATER, J., 1980, Predator boreholes in Periploma margaritaceum with a brief survey of other Periplomatidae (Bivalvia: Anomalodes- mata). The Veliger, 22: 248—251, 1 pl. SAIDOVA, Н. M. & К. V. BEKLEMISHEV, 1953, [On the presence in marine sediments of foraminifer- ans drilled by young gastropods]. Doklady Aka- demia Nauk SSSR, Leningrad, 92: 1061-1063. [in Russian]. SANDER, F. & C. M. LALLI, 1982, A comparative study of mollusk communities on the shelf-slope margin of Barbados, West Indies. The Veliger, 24: 309-318. SAVAZZI, Е. & В. А. REYMENT, 1989, Subaerial hunting behaviour in Natica gualteriana (Naticid Gastropod). Palaeogeography, Palaeoclimatol- ogy, Palaeoecology, 74: 355-364. SCHAFER, W., 1972, Ecology and palaeoecology of marine environments. [transl. |. Oertel]. Chi- cago: University of Chicago Press. xiv + 568 pp., pls. 1-39. SCHNEIDER, D., 1982, Escape response of an in- NATICID PREDATION 187 faunal claim Ensis directus Conrad, 1843 to a predatory snail, Polinices duplicatus Say, 1822. The Veliger, 24: 371-372. SELIN, N. |, S. К. PONUROVSKY & M. Zh. CHERNYAEV, 1986, [The effect of the predatory gastropod Cryptonatica janthostoma on popula- tion structure of the bivalve Ruditapes philippi- пагит]. Biologiya Morya, 1986(5): 72-74. [In Russian]. SILER, W. L., 1965, Feeding habits of some Eocene carnivorous gastropods. The Texas Journal of Science, 17: 213-218. SLITER, W. V., 1971, Predation on benthic foramin- ifers. Journal of Foraminiferal Research, 1: 20— 29, pls. 1-3. SMITH, J. E., 1932, The shell gravel deposits, and the infauna of the Eddystone grounds. Journal of the Marine Biological Association of the United Kingdom, 18: 243-278. SMITH, S. A., С. W. THAYER € С. E. BREFT, 1985, Predation in the Paleozoic: gastropod-like drillholes in Devonian brachiopods. Science, 230: 1033-1035. SOHL, N. F., 1969, The fossil record of shell boring by snails. American Zoologist, 9: 725—734. STAFFORD, W. L., 1988, Polinices through the ages. Fossils Quarterly, 7: 18-22. STANTON, R. J., Jr., & P. C. NELSON, 1980, Re- construction of the trophic web in paleontology: community structure in the Stone City Formation (Middle Eocene, Texas). Journal of Paleontol- ogy, 54: 118-135. STANTON, R. J., Jr., E. N. POWELL 4 P. C. NEL- SON, 1981, The role of carnivorous gastropods in the trophic analysis of a fossil community. Ma- lacologia, 20: 451-469. STENZLER, D. & J. ATEMA, 1977, Alarm response of the marine mud snail, Nassarius obsoletus: specificity and behavioral priority. Journal of Chemical Ecology, 3: 159—171. STEVANOVIC, P., 1950, [Sur les coquilles perforés des mollusques du Sarmatien, Méotien et de Ceux de Bouglowka en Serbie]. Annales Gé- ologiques de la Péninsule Balkanique, 18: 129— 142, pls. 1—4. [in Serbian; Russian and French abstracts]. STUMP, T. E., 1975, Pleistocene molluscan paleo- ecology and community structure of the Puerto Libertad Region, Sonora, Mexico. Palaeogeogra- phy, Palaeoclimatology, Palaeoecology, 17: 177-226. TAYLOR, J. D., 1970, Feeding habits of predatory gastropods in a Tertiary (Eocene) molluscan as- semblage from the Paris Basin. Palaeontology, 13: 254-260, pl. 46. TAYLOR, J. D., 1980, Diets and habitats of shallow water predatory gastropods around Tolo Chan- nel, Hong Kong. Pp. 163-180, in, The malaco- fauna of Hong Kong and southern China: Pro- ceedings of the first international workshop. (Ed. B. Morton). Hong Kong: Hong Kong University Press. TAYLOR, J. D., 1981, The evolution of predators in the late Cretaceous and their ecological signifi- cance. Pp. 229-240, in, The evolving biosphere. (Ed. P. L. Forey). Cambridge: Cambridge Univer- sity Press. TAYLOR, J. D. & C. N. TAYLOR, 1977, Latitudinal distribution of predatory gastropods on the east- ern Atlantic shelf. Journal of Biogeography, 4: 73-81. TAYLOR, J. D., В. J. CLEEVELY & N. J. MORRIS, 1983, Predatory gastropods and their activities in the Blackdown Greensand (Albian) of England. Palaeontology, 26: 521-553. TAYLOR, J. D., М. J. MORRIS & С. М. TAYLOR, 1980, Food specialization and the evolution of predatory prosobranch gastropods. Palaeontol- ogy, 23: 375—409. THOMAS, R. D. K., 1976, Gastropod predation on sympatric Neogene species of Glycymeris (Bi- valvia) from the Eastern United States. Journal of Paleontology, 50: 488—499, pl. 1. THORSON G. [A.W.], 1935, Studies on the egg- capsules and development of Arctic marine prosobranchs. Meddelelser om Gronland, 100(5): 1-71. TSIKHON-LUKANINA, Е. A., 1987, [Trophobiology of aquatic mollusks.] Moscow: Akademiia Nauka SSSR. 176 pp. [in Russian]. TURNER, H. J., Jr., 1955, How clam drills capture razor clams. The Nautilus, 69: 20-22. TURNER, Hew Ur 4 С AYERS С. TE WHEELER, 1948, The horseshoe crab and bor- ing snail as factors limiting the abundance of the soft-shell clam. Pp. 43—45, in, Report on inves- tigations of the propagation of the soft-shell clam, Mya arenaria. (Ed. H. J. Turner, Jr.). Woods Hole Oceanographic Institution, Contribution 462. VALE, F. K. & M. A. REX, 1988, Repaired shell damage in deep-sea prosobranch gastropods from the western North Atlantic. Malacologia, 28: 65-79. VERLAINE, L., 1936, L'instinct et l'intelligence chez les mollusques. Les gastéropodes perceurs de coquilles. Mémoires du Musée Royal d'Histoire Naturelle de Belgique (ser. 2) 3: 387-394. VERMEIlJ, С. J., 1977, The Mesozoic marine rev- olution: evidence from snails, predators and grazers. Paleobiology, 3: 245-258. VERMEIL, С. J., 1978, Biogeography and adapta- tion: patterns of marine life. Cambridge: Harvard University Press. xvi + 322 pp. VERMEIJ, С. J., 1980, Drilling predation of bivalves in Guam: some paleoecological considerations. Malacologia, 19: 329-334. VERMEIJ, С. J., 1982, Unsuccessful predation and evolution. The American Naturalist, 120: 701- 720. VERMElJ, С. J., 1983a, Traces and trends of pre- dation, with special reference to bivalved ani- mals. Palaeontology, 26: 455-465. VERMEIL, С. J., 1983b, Intimate associations and coevolution in the sea. Pp. 311-327, in Coevo- lution. (Eds. D. J. Futuyma & M. Slatkin). Sun- derland, MA: Sinauer Associates. 188 KABAT VERMEIlJ, С. J., 1983c, Shell-breaking predation through time. Pp. 649—669, in, Biotic interactions in recent and fossil benthic communities. (Eds. M. J. S. Tevesz & P. L. McCall). New York: Ple- num Press. VERMEIJ, С. J., 1987, Evolution and escalation: an ecological history of life. Princeton: Princeton University Press. xv + 527 pp. VERMEIJ, С. J. & E. С. DUDLEY, 1982, Shell re- pair and drilling in some gastropods from the Ripley Formation (Upper Cretaceous) of the Southeastern U.S.A. Cretaceous Research, 3: 397—403. VERMEIJ, С. J. & J. А. VEIL, 1978, A latitudinal pattern in bivalve shell gaping. Malacologia, 17: 57-61. VERMEI, С. J., Е. С. DUDLEY & E. ZIPSER, 1989, Successful and unsuccessful drilling pre- dation in Recent pelecypods. The Veliger, 32: 266-273. VERMEN, С. J., Е. ZIPSER & Е. С. DUDLEY, 1980, Predation in time and space: peeling and drilling in terebrid gastropods. Paleobiology, 6: 352-364. VIGNALI, R. & L. GALLENI, 1986, Naticid predation on soft bottom bivalves: a study on a beach shell assemblage. Oebalia, 13: 157-177. VIGNALI, В. & L. GALLENI, 1987 [1986], The beach shell assemblage of Pontedoro: a prelim- inary list of mollusc species with some notes on predation phenomena. Atti della Societa Toscana di Scienze Naturali, Memorie, Serie B, 93: 241— 250. WARME, J. E. & E. J. MCHURON, 1978, Marine borers: trace fossils and geological significance. Pp. 77-131, in, Trace Fossil Concepts. Society of Economic Paleontologists and Mineralogists, Short Course, 5. (Ed. P. B. Basan). WATKINS, R., 1974, Molluscan paleobiology of the Miocene Wimer Formation, Del Norte County, California. Journal of Paleontology, 48: 1264— 1282. WILSON, J. G., 1988, Resource partitioning and predation as а limit to size т Nucula turgida (Leck- enby & Marshall). Functional Ecology, 2: 63-66. WILTSE, W. 1., 1980a, Predation by juvenile Polin- ices duplicatus (Say) on Gemma gemma (Tot- ten). Journal of Experimental Marine Biology and Ecology, 42: 187-199. WILTSE, W. 1. 1980b, Effects of Polinices duplica- tus (Gastropoda: Naticidae) on infaunal commu- nity structure at Barnstable Harbor, Massachu- setts, USA. Marine Biology, 56: 301-310. WITMAN, J. D. & R. A. COOPER, 1983, Distur- bance and contrasting patterns of population structure in the brachiopod Terebratulina septen- trionalis (Couthouy) from two subtidal habitats. Journal of Experimental Marine Biology and Ecology, 73: 57-79. WOELKE, C. E., 1957, The flatworm Pseudostylo- chus ostreophagus Hyman, a predator of oys- ters. Proceedings of the National Shellfisheries Association, 47: 62-67. YOCHELSON, E. L., D. DOCKERY & H. WOLF, 1983, Predation on sub-Holocene scaphopod mollusks from Southern Louisiana. U. S. Geolog- ical Survey, Professional Paper, 1282: 1-13, pls. 1-4. YOUNG, D. K., 1969, Okadaia elegans, a tube- boring nudibranch mollusc from the central and west Pacific. American Zoologist, 9: 903-907. ZIEGELMEIER, E., 1954, Beobachtungen über den Nahrungserwerb bei der Naticide Lunatia nitida Donovan (Gastropoda Prosobranchia). Helgo- länder Wissenschaftliche Meeresuntersuchun- gen 5: 1=33: Revised Ms. accepted 24 April 1990 APPENDIX An * indicates that no species was given; “spp.” indicates that more than two species of that genus were reported on in one reference. | have not included the taxa reported on by Arua (1989) ог Arua & Hoque (1989a—c) due to the questionable nature of their borehole determinations. A. Class Gastropoda. Subclass Prosobranchia. Order Archaeogastropoda. Trochoidea. Trochidae: Calliostoma laugieiri [Vignali & Galleni, 1987] Gibbula varia [Vignali & Galleni, 1987] Helicocryptus radiatus [Taylor et al., 1983] Jujubinus exasperatus [Vignali & Galleni, 1987] Margarites monolifera [Taylor et al., 1983] Monilea* [Kohn, unpub.] Umbonium vestiarium [Berry, 1982] Cyclostrematidae: Pseudoliotina* [Taylor et al., 1983] Turbinidae: Turbo* [Kohn, unpub.] Neritoidea. Neritidae: Nerita funiculata [Hughes, 1985] N. scabricosta [Hughes, 1985] Neritina virginea [Jackson, 1972] Theodoxus luteofasciatus [Stump, 1975] Order Mesogastropoda. Littorinoidea. Littorinidae: Littorina littorea [Edwards, 1975] Rissoidea. Hydrobiidae: Hydrobia andrussowi [Kojumajieva, 1974] Rissoidae: Alvania alexandrae [Hoffman et al., 1974] Ihungia ponderi (Maxwell, 1988] Mohrensternia angulata [Kojumdjieva, 1974] M. inflata [Kojumdjieva, 1974] Rissoa inconspicua [Fretter 8 Manly, 1979] Rissoina podolica (Hoffman et al., 1974] NATICID PREDATION 189 Caecidae: Caecum glabrum [Hoffman et al., 1974] Vitrinellidae: Circulus* [Hoffman et al., 1974] Cerithioidea. Cerithiidae: Argyropeza* [Kohn, unpub.] Bittium* [Berg, 1976; Taylor, 1970] B. reticulatum [Hoffman et al., 1974] Cerithium europeum [Kojumdjieva, 1974] C. variabile [Jackson, 1972] C. vulgatum [Vignali & Galleni, 1987] Rhinoclavis* [Kohn, unpub.] Procerithiidae: Cirsocerithium gracile [Taylor et al., 1983] Diastomatidae: Sandbergeria perpusilla [Hoffman et al., 1974] Fossariidae: “Fossarus” granosus [Taylor et al., 1983] Turritellidae: , Archimediella spirata [Robba 8 Ostinelli, 1975] Mesalia spp. [Fischer, 1962] М. amekiensis [Adegoke 8 Tevesz, 1974] M. regularis [Taylor, 1970] Turritella spp. [Dudley & Vermeij, 1978] T. badensis [Kojumdjieva, 1974] T. bieniaszi [Kojumdjieva, 1974] T. granulata [Taylor et al., 1983] T. subangulata [Kojumdjieva, 1974] T. tricarinata [Hoffman & Martinell, 1984] Stromboidea. Aporrhaidae: Aporrhais pespelecani [Martinell & Marquina, 1980] A. uttingerianus [Martinell & Marquina, 1980] Drepanocheilus calcarata [Taylor et al., 1983] D. neglecta [Taylor et al., 1983] Strombidae: Rimella fissurella [Taylor, 1970] Strombus* [Kohn, unpub.] Tibia unidigitata [Adegoke & Tevesz, 1974] Hipponicoidea. Hipponicidae: Hipponix* [Kohn, unpub.] Vanikoriidae: “Vanikoropsis” cf. albus [Taylor et al., 1983] Tonnoidea. Cassidae: Semicassis wannoensis [Hingston, 1985] Cymatiidae: Cymatium* [Kohn, unpub.] Suborder Heteroglossa. Cerithiopsioidea. Cerithi- opsidae: Cerithiopsis tubercularis [Hoffman et al., 1974] Triphoroidea. Triphoridae: Triphora perversa [Hoffman et al., 1974] Epitonioidea. Epitoniidae: Confusiscala fittoni [Taylor et al., 1983] Epitonium spinosa [Hoffman et al., 1974] Eulimoidea. Eulimidae: Eulima subulata [Hoffman et al., 1974] Strombiformis glaber [Vignali & Galleni, 1987] Rissoelloidea. Rissoellidae: Rissoella* [Berg, 1976] Order Neogastropoda. Muricoidea. Muricidae: Blackdownea quadrata [Taylor et al., 1983] Eupleura caudata [Flower, 1954] Hadriania craticulata [Martinell & Marquina, 1980] Hexaplex benedeica [Adegoke & Tevesz, 1974] Morula* [Kohn, unpub.] Nassa restitutiana [Kojumajieva, 1974] N. dujardini [Hoffman et al., 1974] Paramorea lineata [Taylor et al., 1983] Pterynotus* [Adegoke 8 Tevesz, 1974] Terefundus lamelliferus [Maxwell, 1988] Urosalpinx [Flower, 1954] Buccinidae: Cantharus* [Kohn, unpub.] Phos* [Kohn, unpub.] Siphonalia* [Kohn, unpub.] Columbellidae: Mitrella* [Adegoke 8 Tevesz, 1974] M. minor [Hoffman & Martinell, 1984] M. nassoides [Kojumdjieva, 1974] Nassariidae: Amyclina spp. [Robba & Ostinelli, 1975] Cyllene* [Adegoke & Tevesz, 1974] Dorsanum duplicatum [Kojumdjieva, 1974] Nassarius elatus [Hoffman & Martinell, 1984] . italicus [Martinell & Marquina, 1980] . obsoletus [Edwards, 1975] . perpinguis [Berg & Nishenko, 1975] . pygmaeus [Hoffman & Martinell, 1984] . semistriatus [Hoffman & Martinell, 1984] . tiarula [Stump, 1795] . trivittatus [Edwards, 1975] Niotha crassigranosa [Hingston, 1985] Plicarcularia leptospira [Broom, 1983] Fasciolariidae: Colubraria* [Kohn, unpub.] Falsicolus tangituensis [Maxwell, 1988] Fusinus* [Kohn, unpub.] Granulifusus* [Kohn, unpub.] Iscafusus rigidus [Taylor et al., 1983] Latirus moorei [Stanton et al., 1981] Peristernia* [Kohn, unpub.] Turbinellidae [= Vasidae]: Exilla wellmani (Maxwell, 1988] Olividae: Alocospira papillata [Hingston, 1985] Ancilla buccinoides [Taylor, 1970] Olivella biplicata (Edwards, 1969] Marginellidae: Marginella spp. [Taylor, 1970] Protoginella bembix (Maxwell, 1988] Mitridae: Cancilla* [Kohn, unpub.] Mitra orientalis [Kojumajieva, 1974] Scabricola* [Kohn, unpub.] Subcancilla* [Kohn, unpub.] Volutomitridae: Microvoluta nodulata [Maxwell, 1988] 2222222 190 KABAT Costellariidae [= Vexillidae]: Austromitra* [Hingston, 1985] Vexillium* [Kohn, unpub.] Cancellarioidea. Cancellariidae: Bonellitia amekiensis [Adegoke & Tevesz, 1974] B. serrata [Martinell & Marquina, 1980] Inglisella parva [Maxwell, 1988] |. allophyla [Maxwell, 1988] Sydaphera wannonensis [Hingston, 1985] Conoidea. Conidae: Conus dujardini [Kojumdjieva, 1974] C. parisiensis [Taylor, 1970] Turridae: Bela brachystoma [Hoffman & Martinell, 1984] B. vulpecula [Hoffman & Martinell, 1984] Brachytoma obtusangula [Martinell & Marquina, 1980] Clavatula* [Adegoke & Tevesz, 1974] Clavus spp. [Robba & Ostinelli, 1975] Comitas nana [Maxwell, 1988] Crassispira* [Kohn, unpub.] Cythara subcylindrata [Hoffman et al., 1974] Eopleurotoma spp. [Adegoke & Tevesz, 1974] Gemmula* [Kohn, unpub.] Genota ramosa [Kojumdjieva, 1974] Hesperiturris nodocarinatus [Stanton et al., 1981] Heterocithara marwicki [Maxwell, 1988] Lophitoma* [Kohn, unpub.] Mauidrillia occidentalis [Maxwell, 1988] Michela trabeatoides [Stanton et al., 1981] Mioawateria personata [Maxwell, 1988] Paracomitas beui [Maxwell, 1988] Pleurotoma* [Adegoke & Tevesz, 1974] Raphitoma hispidula [Hoffman et al., 1974] Rugobela* [Maxwell, 1988] Splendrillia vellai [Maxwell, 1988] Tomopleura* [Maxwell, 1988] Turricula africana [Adegoke & Tevesz, 1974] T. dimidiata [Martinell & Marquina, 1980] Viridoturris powelli [Maxwell, 1988] Terebridae: Gemmaterebra catenifera [Hingston, 1985] Strioterebrum monidum [Kitchell et al., 1986] S. pliocenicum [Martinell & Marquina, 1980] Terebra spp. [Vermeij et al., 1980] T. dislocata [Kitchell et al., 1986] Zeacuminia viapollentia [Maxwell, 1988] Subclass Heterobranchia. Superorder Allogas- tropoda. Architectonicoidea. Architectonicidae: Architectonica bendeica [Adegoke & Tevesz, 1974] A. olicatum [Taylor, 1970] Philippia meditteranea [Vignali & Galleni, 1987] Pyramidelloidea. Pyramidellidae: Eulimella conulus [Hoffman et al., 1974] Evelynella doliella [Maxwell, 1988] Odostomia* [Adegoke & Tevesz, 1974] O. conoidea [Hoffman & Martinell, 1984] Pyramidella digitalis [Hoffman et al., 1974] P. plicosa [Hoffman & Martinell, 1984] Pyrgulina interstincta [Hoffman et al., 1974] Tubonilla rufa [Hoffman & Martinell, 1984] T. zesulcata [Maxwell, 1988] Waikura elevata [Maxwell, 1988] Subclass Opisthobranchia. Order Cephalaspidea. Philinoidea. Acteonidae: Acteon reussi [Hoffman et al., 1974] A. semistriatus [Hoffman & Martinell, 1984] A. tornatilis [Vignali & Galleni, 1987] Tornatellaea affinis [Taylor et al., 1983] T. unisulcata [Taylor et al., 1983] Ringiculidae: Avellana incrassata [Taylor, et al., 1983] Ringicula auriculata [Hoffman et al., 1974] R. buccinea [Hoffman & Martinell, 1984] Scaphandridae: Acteocina lajonkaireana [Kojumdjieva, 1974] Cylichna melitopolitana [Kojumdjieva, 1974] C. rubignosum [Kojumdjieva, 1974] Scaphander [Adegoke & Tevesz, 1974] Tornatina heraclitica [Hoffman et al., 1974] T. trunculata [Hoffman et al., 1974] Hamineidae: Atys miliaris [Hoffman et al., 1974] Retusidae: Retusa kelloggi [Stanton et al., 1981] R. truncatula [Hoffman & Martinell, 1984]. B. Class Bivalvia. Subclass Protobranchia. Order Nuculoida. Nuculoidea. Nuculidae: Acila conradi [Colbath, 1985] Ennucula kalimnae [Hingston, 1985] Nucula antiquata [Taylor et al., 1983] N. mixta [Taylor, 1970] N. nucleus [Hoffman & Szubzda, 1976] N. obtusa [Taylor et al., 1983] N. turgida [Wilson, 1988] Palaeonucula strigilata [Fürsich & Jablonski, 1984] Nuculanoidea. Nuculanidae: Mesosaccella angulata [Taylor et al., 1983] M. lineata [Taylor et al., 1983] Nuculana* [Adegoke & Tevesz, 1974] Nuculana spp. [Colbath, 1985] N. fragilis [Kojumdjieva, 1974] N. pella [Vignali & Galleni, 1987] N. pernula [Hutchings & Haedrich, 1984] Yoldiidae: Yoldia* [Colbath, 1985] Y. thraciaeformis [Hutchings & Haedrich, 1984] Malletiidae: Malletia* [Kohn, unpub.] Subclass Pteriomorphia. Order Mytlioida. Mytiloidea. Mytilidae: Choromytilus meriodionalis (Griffiths, 1981] Crenella orbicularis [Taylor et al., 1983] Modiolus auriculatus [Vermeij, 1980] M. reversa [Taylor et al., 1983] Mytilus edulis [Edwards, 1975] NATICID PREDATION 191 Order Arcoida. Arcoidea. Arcidae: Anadara spp. [Kelley, 1989a] A. elevata [Dudley & Dudley, 1980] A. granosa [Вгоот, 1982] A devincta [Colbath, 1985] A. diluvii [Kojumdjieva, 1974] A. thisphila [Dudley & Dudley, 1980] Barbatia irregularis [Taylor, 1970] Bathyarca* (Maxwell, 1988] Noetiidae: Arcopsis dissimilis [Darragh & Kendrick, 1980] Pachecoa declivis [Kitchell, 1982] Cucullaeidae: Idonearca glabra [Taylor et al., 1983] Limopsoidea. Limopsidae: Limopsis chapmani [Darragh & Kendrick, 1980] L. beaumarisensis (Hingston, 1985] L. minuta [Kojumdjieva, 1974]. Glycymerididae: Glycymeris spp. [Thomas, 1976] С. albolineata [Matsukuma, 1977] G. halli (Hingston, 1985] G. insubrica [Vignali & Galleni, 1987] G. pulvinata [Taylor, 1970] G. vestita [Matsukuma, 1977] Glycymerita sublaevis [Taylor et al., 1983] G. umbonata [Taylor et al., 1983] Pterioida. Pterioidea. Cassianellidae: Cassianella ampezzana [Fursich & Jablonski, 1984] Order Limoida. Limoidea. Limidae: Mysidioptera williamsi [Newton, 1983] Order Ostreoida. Ostreoidea. Gryphaeidae: Amphidonte obliquata [Taylor et al., 1983]. Pectinoidea. Pectinidae: Chlamys radians [Guerrero & Reyment, 1988] Pectin opercularis [Boekschoten, 1967] Pseudamussium similis [Smith, 1932]. Subclass Paleoheterodonta. Order Trigonioida. Trigonioidea. Trigoniidae: Rutitrigonia eccentrica [Taylor et al., 1983] Subclass Heterodonta. Order Veneroida. Lucinoidea. Lucinidae: Codakia bella [Vermeij, 1980] С. orbicularis (Jackson, 1972] Ctena decussata [Vignali & Galleni, 1987] С. orbiculata [Jackson, 1972] Divaricella ornata [Kojumdjieva, 1974] D. divaricata [Vignali & Galleni, 1987] Epicodakia* [Kohn, unpub.] Loripes dentatus [Hoffman et al., 1974] L. lacteus [Vignali & Galleni, 1987] Lucina anodonta [Kelley, 1989a] L. approximata [Stump, 1975] L. spinifera [Kojumajieva, 1974] Lucinella divaricata [Hoffman & Martinell, 1984] Myrtea papatikiensis [Maxwell, 1988] Parvilucina costata (Jackson, 1972] Pseudomiltha floridana [Kitchell et al., 1981] Wallucina* [Vermeij, 1980] Fimbriidae: Mutiella canaliculata [Taylor et al., 1983] Ungulinidae: Diplodonta subquadrata [Vermeij et al., 1989] Carditoidea. Carditidae: Beguina diversicosta [Kojumdjieva, 1974] Cardita spp. [Adegoke & Tevesz, 1974] C. chamaeformis [Boekschoeten, 1967] Cyclocardia subtenta [Colbath, 1985] Venericardia greggiana [Kitchell, 1982] V. serrulata [Taylor, 1970] Vetericardiella* [Kitchell, 1986] Crassatelloidea. Astartidae: Astarte spp. [Boekschoten, 1967; Kelley, 1989a] Astarte triangularis [Smith, 1932] Eriphyla striata [Taylor et al., 1983] Lirodiscus tellinoides [Siler, 1965] Nicaniella formosa [Taylor et al., 1983] Crassatellidae: Crassatella spp. [Taylor, 1970] C. vadosa [Sohl, 1969] Crassatellites* [Kohn, unpub.] Eucrassatella spp. [Kelley, 1982a] Cardioidea. Cardiidae: Acanthocardia tuberculata [Vignali & Galleni, 1986] Cardium spp. [Smith, 1932] С. politionanei [Kojumajieva, 1974] Cerastoderma edule [Bayliss, 1986] Clinocardium nuttallii [Bernard, 1967] Dinocardium robustum [Kornicker et al., 1963] Fragum fragum [Vermeij, 1980] Laevicardium elenense [Vermeij et al., 1989] Loxocardium bouei [Taylor, 1970] Parvicardium scabrum [Bayliss, 1986] Protocardia hillana [Taylor et al., 1983] Thetis laevigata [Taylor et al., 1983] Mactroidea. Mactridae: Mactra angulata [Taylor et al., 1983] M. australis [Laws & Laws, 1972] M. chinensis [Vermeij et al., 1989] M. fragilis [Paine, 1963] M. stultorum [Vignali & Galleni, 1987] Mactrellona exoleta [Vermeij et al., 1989] Notospisula parva [Green, 1968] Pseudocardium sachalinense [Vermeij et al., 1989] Spisula elliptica [Bayliss, 1986] S. solidissima [Franz, 1977] S. subtruncata [Bayliss, 1986] Tresus nuttallii [Reid & Friesen, 1980] Mesodesmatidae: Atactodea striata [Ansell & Morton, 1987] Coecella chinensis [Ansell & Morton, 1987] Donacilla angusta [Laws & Laws, 1972] Ervilia ousilla [Hoffman & Szubzda, 1976] Е. dissita [Kojumajieva, 1974] 192 KABAT Solenoidea. Solenidae: Ensis directus [Schneider, 1982] Solen conradi [Colbath, 1985] S. strictus [Frey et al., 1987]. Tellinoidea. Donacidae: Donax spp. [Vermeij et al., 1989] D. faba [Ansell & Morton, 1987] D. semistriata [Vignali & Galleni, 1987] D. trunculus [Vignali 4 Galleni, 1987] D. vittatus [Negus, 1975] Plebidonax deltoides [Kitching & Pearson, 1981] Psammobiidae: Gari hamiltonensis (Hingston, 1985] Tagelus peruvianus [Vermeij et al., 1989] Scrobiculariidae: Scrobicularia plana [Richter, 1962] Solecurtidae: Solecurtus antiquatus [Kojumdjieva, 1974] Tellinidae: Arcopagia robusta [Vermeij, 1980] Macoma albaria [Colbath, 1985] M. arctata [Colbath, 1985] M. balthica [Commito, 1982] M. calcarea [Aiken & Risk, 1988] M. nasuta [Reid & Gustafson, 1989] Palaeomoera inaequalis [Taylor et al., 1983] Peronidia venulosa [Vermeij et al., 1989] Quidnipagus palatam [Vermeij, 1980] Scissulina* (Vermeij, 1980] Tellina spp. [Vermeij et al., 1989] T. donacina [Vignali & Galleni, 1987] T. emacerata [Colbath, 1985] T. lux [Broom, 1983] T. planata [Kojumdjieva, 1974] T. pudica [Broom, 1983] T. pulchella [Vignali & Galleni, 1987] T. tenuis [Ansell, 1982a—c] Tellinella virgata [Nakamine & Habe, 1983] Temnoconcha cognata [Vermeij et al., 1989] Arcticoidea. Arcticidae: Arctica islandica [Christensen, 1970] Epicyprina angulata [Taylor et al., 1983] E. subtruncata [Taylor et al., 1983] Venilicardia lineolata [Taylor, et al., 1983] Veneroidea. Veneridae: Anomalocardia squamosa [Ansell & Morton, 1987] A. squamosa [Taylor, 1980] Aphrodina nitidula [Taylor, 1970] Bassina calophylla [Ansell & Morton, 1985] Callistina plana [Taylor et al., 1983] Calpitaria distincta [Taylor, 1970] Calva subrotunda [Taylor et al., 1983] Chamelea gallina [Guerrero & Reyment, 1988a] Chimela caperata [Taylor et al., 1983] Chione spp. [Smith, 1932] . basteroti [Kojumdjieva, 1974] . californensis [Stump, 1975] . cancellata [Paine, 1963] . subrugosa [Vermeij et al., 1989] . undatella [Peterson, 1982] MAD Circomphalus subplicatus [Hoffman & Szubzda, 1976] Costacallista laevigata [Taylor, 1970] Dosinia dunkeri [Vermeij et al., 1989] D. lupinus [Vignali & Galleni, 1987] Flaventia ovalis [Taylor et al., 1983] Gafrarium minimum [Smith, 1932] G. pectinatum [Vermeij, 1980] Gemma gemma [Wiltse, 1980a] Gouldia minima [Vignali & Galleni, 1987] Katelysia scalarina [Laws & Laws, 1972] Katherinella angustifrons [Colbath, 1985] Macrocallista nimbosa [Paine, 1963] Медарйапа squalida [Vermeij et al., 1989] Mercenaria mercenaria [Berg & Porter, 1974] M. campechiensis [Paine, 1963] Meretrix lusoria [Vermeij et al., 1989] Paraesa faba [Taylor et al., 1983] Pelecyora trigona [Broom, 1983] Periglypta reticulate [Vermeij, 1980] Pitar spp. [Vermeij et al., 1989] Р. morrhuana [Jacobson, 1965] Placamen subroboratum [Hingston, 1985] Protothaca spp. [Vermeij et al., 1989] P. staminea [Peterson, 1982] Ruditapes philippinarum (Rodrigues, 1986] Saxidomus giganteus [Bernard, 1967] Sunetta gibberula [Hingston, 1985] Tapes japonica [Hamada, 1961] T. philippinarum [Ansell & Morton, 1987] Timoclea marica [Vermeij, 1980] Tivela spp. [Vermeij et al., 1989] Venerupis aurea [Vignali & Galleni, 1987] V. senegalensis [Vignali & Galleni, 1987] Venus multilamella [Kojumdjieva, 1974] V. striatula [Ansell, 1960] V. verrucosa [Vignali & Galleni, 1987] Veremolpa micra [Mukai, 1973] Glauconomidae: Glauconome chinensis [Ansell & Morton, 1987] Order Myoida. Myoidea. Myidae: Cryptomya californica [Watkins, 1974] Mya arenaria (Edwards, 1975] Corbulidae: Caestocorbula* [Kitchell, 1986] Caryocorbula deusseni [Kitchell, 1982] Corbula spp. [De Cauwer, 1985] Corbula carinata [Kojumajieva, 1974] C. elegans [Taylor et al., 1983] C. gibba [Vignali & Galleni, 1987] C. idonea [Kelley, 1989a] C. rugosa [Taylor, 1970] C. truncata [Taylor et al., 1983] Notocorbula ephamilla [Hingston, 1985] N. innerans [Maxwell, 1988] Varicorbula amekiensis [Adegoke & Tevesz, 1974] Vokesula aldrichi [Kitchell, 1982] Hiatelloidea. Hiatellidae: Hiatella arctica [Aitken & Risk, 1988] Panopea mandibula [Taylor et al., 1983] NATICID PREDATION 193 Subclass Anomalodesmata. Pandoroidea. Periplo- matidae: Cochlodesma leanum [Rosewater, 1980] Periploma spp. [Rosewater, 1980] Poromyoidea. Cuspidariidae: Cuspidaria cuspidata [Hoffman & Martinell, 1984] C. Scaphopoda. Dentaliidae: Dentalium complexum [Fankboner, 1969] D. bedensis [Kojumajieva, 1974] D. spp. [Yochelson et al., 1983] Fustiaria miocaenica [Hoffman et al., 1974] Entalinidae: Entaliopis brevis [Yochelson et al., 1983] Gadilidae: Cadulus* [Yochelson et al., 1983] MALACOLOGIA, 1990, 32(1): 195-202 LETIERS TC THE EDITOR TOWARDS A PHYLOGENETIC SYSTEM OF GASTROPODA PART 1: TRADITIONAL METHODOLOGY—A REPLY Gerhard Haszprunar Institut fur Zoologie der Universitat Innsbruck Technikerstrasse 25, A-6020 Innsbruck, Austria ABSTRACT Bieler (1990) provides a critique of the methodology of a phylogenetic analysis of the Gas- tropoda by Haszprunar (1988). His criticism of an incomplete and inconsistent presentation of character-states and methodology is answered by explaining by examples the way in which the character analysis and the construction of the cladogram were done. | argue that any maximum parsimony analysis with equal weighting of characters will fail to produce the “true” phylogeny because of the high degree of parallelism and convergence within the group. The method presented applies a priori criteria for estimating the probabilities of homology and apomorphy (i.e. significance) of characters and constructs the cladogram according to that significance. In the proposed classification, higher taxa are thought to reflect stem-lines of high probability. Key words: Gastropoda, systematics, classification, phylogeny, cladistics, critique. INTRODUCTION Bieler (1990) gives a critique of the meth- odology of the recently published phyloge- netic analysis of streptoneuran Gastropoda by Haszprunar (1988) from a strictly cladistic point of view. Here | want, first, to correct cer- tain points of the original paper (Haszprunar, 1988; cf. appendix); second, to explain briefly the reasons that the analysis was not done by application of accepted cladistic methodol- ogy; and third, to provide significant examples of the way in which | weighted the characters and did the analysis. Doing the latter, | accept the major points of Bieler’s (1990) critique— no one is perfect. Thus, | agree with Bieler (1990) that for any “scientific question, it is an integral part of any study to present the data unambiguously, to employ reproducible methods, and to offer testable hypotheses.” Maybe | have underes- timated the difficulty of following my argu- ments. | therefore wish at least to show the principles. PRESENTATION OF DATA Bieler (1990) is correct in assuming that my analysis was not done by computer, because 195 during the original study adequate hardware to run phylogenetic software was unavail- able. Since then, adequate hardware has be- come available, and | have become familiar with the advantages and disadvantages of programs like PHYLIP, PAUP and in particu- lar HENNIG’86. Admittedly there are some mistakes in the text, tables and figures, all of which are of minor importance, however. Nevertheless, | welcome this opportunity to correct those of which | am aware. Bieler (1990) criticized the fact that | did not provide a comprehensive data-matrix. The way in which | did the analysis, however, does not require a data-matrix (see below), and the main results of the character-analysis have been presented (Haszprunar, 1988: table 2). THEORETICAL CONSIDERATIONS Character analysis is the basis of any phy- logenetic analysis. Typically plesiomorphic versus apomorphic states are estimated by application of the rules of Hennig (1966) such as outgroup-comparison, data on fossils, on- togenetic sequences, and the like. Often, however, there is no clear outgroup available 196 HASZPRUNAR (e.g. Houbrick, 1988; Reid, 1989), and the use of fossils and ontogenetic data has been criticized (Alberch, 1985). The problem of homology, i.e. the problem of the frequency of change from plesiomor- phic to apomorphic character state during phylogeny, seems to be overcome by appli- cation of a “maximum-parsimony” analysis, whether by hand or by computer. The working hypothesis of parsimony minimizes the num- ber of analogies (homoplasies) and can pro- duce one (or many) ‘most parsimonious” tree(s). Colless (1983) has pointed out that the principle of parsimony, which is an oper- ational concept rather than an empirical fact of evolution, does work with negligible rates of failure only if the probability of change in each character-state is very low. As outlined by Gosliner & Ghiselin (1984) for primitive opisthobranchs and identified by Davis (1989) in the Hydrobiidae and in my work on the streptoneurans, however, there is a very large degree of convergence, that is, parallelism, in the data. With an increase in the number of taxa the degree of homoplasy increases (Sanderson & Donoghue, 1989), moreover, suggesting a more or less constant rate of homoplasy among taxa. Indeed, the neces- sity of a parsimony analysis implies that the basic data matrix is controversial with respect to its proposed synapomorphies. Accordingly, the problem of homology cannot be overcome by parsimony analysis. The recent cladistic study (done with PAUP) of the Littorinidae by Reid (1989) also shows many cases of homoplasy. Indeed, “59.2% of the character state changes could be ascribed to homoplasy” (Reid, 1989: 59), and this is logically a minimal (“most parsimo- nious”) estimate. Significantly, a final cla- dogram that differs in certain points from the consenus tree is preferred because “some character-state reconstructions are more likely than others” (Reid, 1989: 63). As stated (Haszprunar 1988: 399), the main problem of any phylogenetic study is that of homology. As reviewed by Riedl (1975, 1978), Ruppert (1982) and Neff (1986), a priori criteria for in- ference of homology have been provided by Remane (1952, 1954). More recently, Rieger & Tyler (1979, 1985; see also Westheide & Rieger, 1987; Tyler, 1988) have formulated criteria for the counter-version, i.e. the esti- mation of convergence. Both sets of criteria should be applied to any analysis (see below). | want to stress that both types of character analysis (homology versus analogy, apomor- phy versus plesiomorphy) must be done prior to construction of the tree, and that both are principially inductive by application of the cri- teria of Remane (1952) and Hennig (1966) among others. Accordingly, each proposed synapomorphy includes a two-fold degree of probability, one with respect to apomorphy (“-apo-"), and one with respect to homology (“syn-”) (Haszprunar, 1989). In the case of character-states, even two analyses of ho- mology are necessary: first, whether all the states belong to the same (homologous) character; secondly, with respect to the ho- mology of the advanced state. For example, in an analysis of the gills of gastropod groups and in particular the (plicate) gill of primitive opisthobranchs, two questions of homology must be answered (for detailed discussion, see Haszprunar, 1985: 20-21; Haszprunar, 1988: 382): (1) Is the opisthobranch gill a ho- mologue of the prosobranch gill (i.e. a ctenid- ium)? (2) If so, is the plicatid gill homologous in all opisthobranchs? | believe that these probabilities must be used to “weight” the characters used in the analysis. In other words, the “weight” is not a feature of the character itself, but the degree of likelihood in the present analysis (cf. also Bryant, 1989). There is no escape from the weighting of characters. Also, the usual analysis involving maximal parsimony weights characters by se- lecting them (characters not selected lack weight) and by giving each selected character equal weight. Insofar as the degree of ho- moplasy is great, differentiated weighting of selected characters becomes essential, how- ever. Although Remane (1952) has indicated the way to infer distinct probabilities for a pro- posed homology, there is still no clear proce- dure for quantitative a priori weighting of char- acters (e.g. Neff, 1986; Westheide & Rieger, 1987; Bryant, 1989). In using computer algo- rithms, one possibility would be to include in the analysis only characters with high signifi- cance; another is to establish a system of dif- ferential weighting (e.g. 1/3/5 corresponding “low/ medium/ high” significance). These considerations shed light on data presentation as well. For instance, the fre- quency and circumstances of transformation of coiled shells into asymmetrical limpet-like ones are unimportant; the statement “many” shows that the significance of this character is very low in this phylogenetic analysis. (Its sig- nificance might be high in another one, how- ever.) GASTROPOD SYSTEMATICS: REPLY TO BIELER 197 PRACTICAL CONSEQUENCES General Remarks In this section | wish to show by examples the way in which the character analysis and the construction of the cladogram were done in the original paper. For character analysis, | have selected two examples, the number of gills and the conditions of the anterior nerve ring, the significance of which differ consider- ably. These significances are estimated prior to construction of any cladogram by applica- tion of the rules of Remane (1952), Rieger & Tyler (1979, 1985), Neff (1986), Westheide & Rieger (1987) and Tyler (1988). Two groups, Neritimorpha and Pyramidelloidea have been selected to demonstrate the construction .of the cladogram. It was assumed a priori that the taxa used in the study all were holophyletic (i.e. mono- phyletic sensu Hennig, 1966), implying that changes within a taxon are secondary phe- nomena. This approach also concerned the Euthyneura the holophyly of which has been shown earlier (Haszprunar, 1985a,b). It will be shown that in one case (Allogastropoda) this assumption did not work and necessi- tated the consideration of the subtaxa (see below). Number of Ctenidia The question of ctenidial homology throughout the gastropods has been dis- cussed at length by Haszprunar (1985a: 20—22; 1988: 377-383). Whereas the gills of Cocculiniformia, of Valvatoidea, of the allo- gastropod groups and the Euthyneura were considered to be secondary structures, the gills of the remaining streptoneuran groups were assumed to represent homologues. Outgroup comparison (Cephalopoda, Try- blidiida) makes it nearly certain that the pres- ence of paired pallial organs is the primitive condition among gastropods. This conclusion is supported by the facts that even gastro- pods with two gills often have reduced the right one, and that in the Trochoidea and Lep- etodriloidea the blood supply of the right gill is retained although the gill itself has been lost. The probability for the hypothesis “plesio- morphy: two ctenidia; apomorphy: one (left) ctenidium” is therefore very high. Next the probability was considered whether the change from two ctenidia to one occurred once or often in gastropod evolution. Two functional gills are present only in veti- gastropod groups (“zeugobranchs”), and even within this group two subgroups have lost the right ctenidium. Anatomical features in Neritimorpha, in which most species have a diotocardian heart and certain species even have a gill-rudiment (Fretter, 1965) and Doco- glossa—Patellidae (with two osphradia) like- wise suggest an original condition of two ctenidia in these taxa. Functional morphology shows that a change from two to one ctenidium results in advantages for the animal with respect to wa- ter currents in the mantle cavity (Yonge, 1947). Indeed, the presence of two ctenidia necessitates a slit or hole(s) in the shell for passage of waste. Finally, because in zeugo- branch gastropods, such as Haliotis, the left ctenidium is formed first in ontogeny (Crofts, 1937), a heterochronic process might easily result in a loss of the right ctenidium. On the whole, | concluded that the change from two to one (left) ctenidium probably oc- curred several times in gastropod evolution. Thus the probability of the respective syn— apomorphy, i.e. the probability of the homol- ogy of the change from plesiomorphic to apo- morphic condition, is low. Anterior Nervous System The homology of the main ganglia of the anterior nerve ring in gastropods is well es- tablished by identical relative positions and interconnections and by identical fields of in- nervation. Among the Streptoneura, two conditions of the anterior nerve ring with respect to the rel- ative position of the ganglia can be distin- guished: the pleural ganglion might be close to the pedal one (hypoathroid condition) or close to the cerebral one (epiathroid condi- tion). Outgroup comparison is unsatisfactory, because the Tryblidiida lack pleural ganglia and the Cephalopoda have a highly concen- trated nervous system. Ingroup comparison reveals, however, that the hypoathroid condi- tion is generally correlated with other plesio- morphic characters, such as presence of na- cre, paired pallial and excretory organs, or external fertilization. The hypothesis “plesio- morphic: hypoathroid condition—apomorphic: epiathroid condition” therefore appears well founded. Again it is now necessary to estimate the number of changes from the hypo- to the epi- athroid condition. There is not a single strep- 198 HASZPRUNAR toneuran taxon in which a mixture of the two conditions occurs (for Viviparidae cf. Hasz- prunar, 1988: 395). In addition, the distribu- tion of both character states is largely corre- lated with the ability to produce planktotrophic larvae (exception: certain Neritoidea). On the other hand, a selection pressure that could force such a change is unknown. Moreover, both conditions are uneffected by concentra- tion of the nervous system. Summarizing the argument, | assumed the syn—apomorphy “epiathroid nerve ring” to be of very high sig- nificance for streptoneuran phylogeny. Position of Neritimorpha Based on the results of the character anal- ysis, estimation of the systematic position of the Neritimorpha starts with consideration of the characters with the highest significance, such as the hypoathroid nervous system. This step alone reduces drastically the number of possible trees. Starting the analy- sis with 28 taxa (Haszprunar, 1988: fig. 5) 1.6 x 10% trees are possible. Accepting “epia- throid nervous system” as a synapomorphy leaves 18 taxa and thus 6.3 x 10'® possible trees [x = (2n—3)!/2 ®(n—2)!; in which п is the number of taxa]. Among those “Archaeo-” gastropods, there are two sequences of radular types, each of them again with high significance (stereoglos- sate—flexoglossate; rhipidoglossate—tae- nioglossate; Haszprunar, 1988: 390-391). This places the Docoglossa (= Patellogas- tropoda) and hot-vent group C below and the architaenioglossate groups above the Neriti- morpha. The number of possible trees involv- ing the Neritimorpha is further reduced to 3.2 х 10'' (13 taxa remain). Upon consideration of the distribution of ctenidial skeletal support (Haszprunar, 1988: 377-381), Neomphalus, the Vetigastropoda and the Seguenzioidea are placed above the neritimorph clade. The number of possible trees is now 15 (4 taxa remain). The Cocculiniformia share many ple- siomorphic characters with the Docoglossa, including the primary limpet shell (Haszpru- nar, 1988: 370-372); thus they are grouped below the Neritimorpha. Finally, Melano- drymia shares several characters, such as radula type and protoconch features, with Neomphalus and the Vetigastropoda, and is therefore placed above the neritimorph off- shoot. This solution agrees with several character sequences of high significance. The assump- tion that the Neritimorpha belong among the higher gastropods is based, however, on character stages each of which is correlated with reproductive biology, namely internal fer- tilization and planktotrophic veligers. The probability of convergent evolution of the fea- tures of neritimorph reproductive biology is very high: first, details of the respective char- acters differ considerably between Neritimor- pha and higher groups (genital system, sperm structure, protoconch features); and second, there are numerous examples of internal fer- tilization within other archaeogastropod clades, and larval planktotrophy has been es- tablished through parallel evolution among the Bivalvia. Position of Pyramidelloidea Again, the analysis begins with consider- ation of neural conditions. Earlier the Pyra- midelloidea were placed together with the Architectonicoidea in a clade called Allogas- tropoda (Haszprunar, 1985a). The epiathroid condition of the anterior nerve ring placed the Allogastropoda among the “Apo-"gastropoda, the lack of parietal ganglia and the retention of (at least osphradial) streptoneury (Hasz- prunar, 1988: 394) suggest a grouping of the Allogastropoda below the euthyneuran level of organization. On the other hand, the Pyramidelloidea and the Euthyneura share synapomorphies of high significance, such as giant nerve cells, a rhinophoral and a lateral nerve and charac- ters of the sperm (Haszprunar, 1988: 396— 397; Healy, 1988a,b). Such proposed syn- apomorphies were in direct contrast to the Originally assumed synapomorphies of the Al- logastropoda, namely a shared gill position to the right of the dorsal ciliary tract, an acrem- bolic proboscis of distinct type (shifted posi- tion of buccal ganglia) and spermatophores (Haszprunar, 1985a). Meanwhile, however, pyramidelloids with a different position of the gills (Amathinidae; Ponder, 1987) and a mathildid with the usual placement of buccal ganglia (Geganyia; Haszprunar, 1985b) were described. This leaves the spermatophores with very low significance. As a conclusion, | corrected my earlier opinion and regard the *Allogastropoda* now as a distinct grade rather than a clade. Within this grade, the Pyramidelloidea are placed closest to the Euthyneura, and both taxa rep- resent a sister-group relationship. GASTROPOD SYSTEMATICS: REPLY TO BIELER 199 CLASSIFICATION In my approach, the final cladogramis a the- orem of probability with very different degrees of likelihood in the various stem-lines of taxa. It is essential to note that a reconstruction of phylogeny should be translated into a clas- sification, and not the phylogeny itself. In an attempt to base the classification on the same principle as the analysis (probabilities), the central taxa should reflect the highest degrees of certainty in the analysis. A similar point of view was made by Wiley (1979, 1981) in claim- ing to retain “important” taxa, which very often reflect stem-lines with high probabilities. Evolutionary systematists often claimed the inclusion of the “anagenetic component” into the classification (e.g. Mayr, 1981). Taxa_of high rank are interpreted as an expression of major evolutionary gaps. This array can be real if caused by fast adaptive radiations and a lack of intermediate forms. | interpret taxa of high rank as reflecting stem lines with very likely monophyly. This interpretation equals the distinction between apomorphy and plesi- omorphy and gaps between character states (in a reconstruction). In this way, clado- and anagenesis are considered by correlating each with some probability. Whereas many authors prefer Wiley’s (1979, 1981) sequential method of classifica- tion, other cladists still use the dichotomic Hennigian way (e.g. Ax, 1984, 1987; Berthold & Engeser, 1987). | prefer the former, and regard my own proposal as a modification of Wiley’s (1981) methodology. Gauthier (1986) has proposed marking so-called “metataxa” (i.e. taxa, the holo- or paraphyletic status of which cannot be given at present) by an asterisk ({ахоп*). In combin- ing my original mode of marking grades as “taxa” (Haszprunar, 1986) with Gauthier's (1986) ideas, | have more recently proposed to mark grades by asterisks (*taxa*) and to mark metataxa (e.g. “Architaenioglossa”, *Cerithiimorpha*) by a combination of aster- isks and sedis mutabilis in the subtaxa (Salvini-Plawen & Haszprunar, 1987; Hasz- prunar, 1988). This enables a better con- versation of a metataxon into an para- or hol- ophyletic taxon upon addition of new data. At the time the study was finished, the Cerithio- idea was an example of a metataxon. | regard Bieler’s (1990) solution of omitting the Cer- ithioidea from the classification as less ac- ceptable than my proposal of marking the taxon unequivocally. PRESERVATION OF TRADITIONAL NAMES In the earliest phase of my phylogenetic work (Haszprunar, 1985a,b), | frequently cre- ated new taxa of high rank. However, “nobody can hinder me to become wiser,” and several of my friends (see Acknowledge- ments) have convinced me that preservation of traditional names is a better way. As out- lined in Haszprunar (1988: 370), certain new taxa still appear necessary to present phylog- eny unequivocally or to reflect taxa with high propabilities. | consider the Archaeogas- tropoda in its traditional, paraphyletic (ortho- phyletic) sense still useful in systematics, be- cause in many cases only shells (and radulae) are available, which do not allow for a more specific classification. Thiele's Meso- gastropoda is a paraphyletic group—it inde- pendently gives rise to both the Stenoglossa and Euthyneura—and therefore has been abandoned. | also regard the Neotaenioglo- ssa (again paraphyletic) as a provisional con- struct which should be abandoned in the fu- ture. CONCLUSION | have responded Bieler's (1990) critique on the mode of my phylogenetic analysis on streptoneuran gastropods as follows: (a) | have provided arguments against do- ing a maximum-parsimony analysis with equal weighting of characters. (b) | have pre- sented examples of the character analysis and of placement of taxa to demonstrate the method used in the analysis. Proposed syn- apomorphies are considered as two-fold hy- potheses with distinct degrees of likelinood. Accordingly the cladogram is regarded as a theorem of probability, and taxa of high rank are thought to reflect stem-lines of high cer- tainty. (c) | have explained the use of certain taxa in the proposed classification. ACKNOWLEDGEMENTS | thank Rudiger Bieler for the critical review of my papers, in particular with respect to de- tection of mistakes made, as well as for open- ing this discussion. | thank an anonymous ref- eree for very helpful criticism of an earlier draft of this manuscript. | am indebted to David Lindberg (University of California, Ber- 200 HASZPRUNAR keley), who introduced me in the field of com- puter-cladistics. | particularly acknowledge the kindness of James H. McLean (Los An- geles County Museum of Natural History) who detected my nomenclatorial mistakes. | am also grateful to Winston F. Ponder (Aus- tralia Museum, Sydney) and Anders Waren (National Museum of Sweden, Stockholm) for our discussions on preservation of taxa. REFERENCES ALBERCH, P., 1985, Problems with the interpreta- tion of developmental sequences. Systematic Zoology, 34: 46-58. AX, P., 1984, Das phylogenetische System. Sys- tematisierung der lebenden Natur Auf Grund ihrer Phylogenese. Gustav Fischer Verlag, Stutt- gart. AX, P., 1987, The phylogenetic system. The sys- tematization of organisms on the basis of their phylogenesis (Translation of Ax, 1984, by R. P.S. Jefferies). John Wiley & Sons, New York. BERTHOLD, T. & T. ENGESER, 1987, Phyloge- netic analysis and systematization of the Ceph- alopoda. Verhandlungen des Naturwissenschatt- lichen Vereins Hamburg, (NF) 29: 187-220. BIELER, R., 1988, Phylogenetic relationships in the gastropod family Architectonicidae, with notes on the family Mathildidae. Pp. 205-240 In: PON- DER, W. F., ed., Prosobranch phylogeny. Mala- cological Review Supplement, 4. BIELER, ВР. 1990, Haszprunars “clado- evolutionary” classification of the Gastropoda—a critique. Malacologia, 31:371-380. BIELER, R. & P. M. MIKKELSEN, 1988, Anatomy and reproductive biology of two Western Atlantic species of Vitrinellidae, with a case of protan- drous hermaphroditism in Rissoacea. Nautilus, 102: 1-29. BRYANT, H. N., 1989, An evaluation of cladistic and character analyses as hypothetico-deductive procedures, and the consequences for character weighting. Systematic Zoology, 38: 214-227. COLLESS, D. H., 1983, Wagner trees in theory and praxis. Pp. 259-278 In: FELSENSTEIN, J., ed., Numerical taxonomy. NATO ASI Series G1. Springer Verlag, Heidelberg. CROFTS, О. R., 1937, The development of Haliotis tuberculata, with special reference to the organo- genesis during torsion. Philosophical Transac- tions of the Royal Society of London, B208: 219— 268. DAVIS, G. M., 1989, Character analysis, conver- gence, taxonomy and evolution of the Hydrobi- idae. Abstracts of the 10th International Malaco- logical Congress, Tubingen 1989: 56. FRETTER, V., 1965, Functional studies of the anat- omy of some neritid prosobranchs. Journal of Zo- ology, London, 147: 46-74. GAUTHIER, J., 1986, Saurischian monophyly and the origin of birds. Pp. 1-55 In: PADIAN, K., ed., The origin of birds and the evolution of flight. Memoirs of the Californian Academy of Sci- ences, 8: 98 pp. GOSLINER, T. M. & M. T. GHISELIN, 1984, Paral- lel evolution in opisthobranch gastropods and its implications for phylogenetic methodology. Sys- tematic Zoology, 33: 255-274. HASZPRUNAR, G., 1985a, The Heterobranchia— a new concept for the phylogeny of the higher Gastropoda. Zeitschrift fur Zoologische System- atik und Evolutionsforschung, 23: 15-37. HASZPRUNAR, G., 1985b, On the anatomy and systematic position of the Mathildidae (Mollusca, Allogastropoda). Zoologica Scripta, 14: 201-213. HASZPRUNAR, G., 1986, Die klado-evolutionare Klassifikation—Versuch einer Synthese. Zeit- schrift fur Zoologische Systematik und Evolution- sforschung, 24: 89-109. HASZPRUNAR, G., 1988, On the origins and evo- lution of major gastropod groups, with special ref- erence to the Streptoneura. Journal of Molluscan Studies, 54: 367-441. HASZPRUNAR, G., 1989, Estimation of homology: implications for the methodologies of classifica- tion. Abstracts of the 2nd European Society of Evolutionary Biology Congress, Roma 1989,: 31. HEALY, J. M., 1988a, The ultrastructure of sperma- tozoa and spermiogenesis in pyramidellid gastro- pods, and its systematic importance. Helgo- lander Meeresuntersuchungen, 42: 303-318. HEALY, J. M., 1988b, Sperm morphology and its systematic importance in the Gastropoda. Pp. 251-266 In: PONDER, W. F., ed., Prosobranch phylogeny. Malacological Review Supplement, 4. HENNIG, W., 1966, Phylogenetic systematics. Uni- versity of Illinois Press, Urbana, 263 pp. HOUBRICK, R. S., 1988, Cerithioidean phylogeny. Pp. 88-128 In: PONDER, W. F., ed., Proso- branch phylogeny. Malacological Review Sup- plement, 4. HOUBRICK, В. S., 1989, Campanile revisited: Im- plications for cerithioidean phylogeny. American Malacological Bulletin, 7: 1-6. LINDBERG, D. R., 1988, The Patellogastropoda. Pp. 35-63 In: PONDER, W. F., ed., Prosobranch phylogeny. Malacological Review Supplement, 4. MACKIE, С. L., 1984, Bivalves. Pp. 351—418 In: TOMPA, A. S., N. H. VERDONK & J. A. M. VAN DEN BIGGELAAR, eds., The Mollusca. Vol. 7: Reproduction. Academic Press, London. MAYR, E., 1981, Biological classification: Towards a synthesis of opposing methodologies. Science, 214: 510-514. NEFF, N. A., 1986, A rational basis for a priori char- acter weighting. Systematic Zoology, 35: 11- 123: PONDER, W. F., 1987, The anatomy and relation- ships of the pyramidellacean limpet Amathina tri- carinata (Mollusca: Gastropoda). Asian Marine Biology, 4: 1-34. PONDER, W. F., 1988, The truncatelloidean GASTROPOD SYSTEMATICS: REPLY TO BIELER 201 (=rissoacean) radiation—a preliminary phylog- eny. Pp. 129-164 In: PONDER, W. F., ed., Prosobranch phylogeny. Malacological Review Supplement, 4. PONDER, W. F. & A. WAREN, 1988, Appendix. Classification of the Caenogastropoda and Het- erostropha—a list of the family-group names and higher taxa. Pp. 288-326 In: PONDER, W. F., ed., Prosobranch phylogeny. Malacological Re- view Supplement, 4. REID, D. G., 1989, The comparative morphology, phylogeny and evolution of the gastropod family Littorinidae. Philosophical Transactions of the Royal Society of London, B324: 1-110. REMANE, A. 1952, Die Grundlagen des natürlichen Systems, der vergleichen-den Anat- omie und der Phylogenetik. Akademische Ver- lagsgesellschaft Geest & Portig, Leipzig. REMANE, A., 1954, Morphologie als Homologien- forschung. Verhandlungen der Deutschen Zool- ogischen Gesellschaft, 1954: 159—183. RIEDL, R., 1975 Die Ordnung des Lebendigen. Systembedingungen der Evolution. Paul Parey, Hamburg & Berlin. RIEDL, R., 1978, Order in living organisms. A sys- tems analysis of evolution (Translation of Riedl, 1975, by R. P. D. Jefferies), Wiley Interscience, New York. RIEGER, R.M. & S. TYLER, 1979, The homology theorem in ultrastructure research. American Zo- ologist, 19: 655—664. RIEGER, R. М. & $. TYLER, 1985, Das Homologi- etheorem in der Ultrastruktur Forschung. Pp. 21— 36 In: OTT, J. А., G. P. WAGNER & Е. M. WUKETITS, eds., Evolution, Ordnung und Erkenntnis. Parey Verlag, Berlin & Hamburg. RUPPERT, E. E., 1982, Homology recognition as a basis for comparative biology. Pp. 31-54 In: Рго- ceedings of the Third International Symposium on the Tardigrada. East Tennessee State Univer- sity Press. SALVINI-PLAWEN, L. V. & G. HASZPRUNAR, 1987, The Vetigastropoda and the systematics of streptoneurous gastropods (Mollusca). Journal of Zoology, London, A211: 747-770. SANDERSON, M. J. & M. J. DONOGHUE, 1989, Patterns of variation in levels of homoplasy. Ev- olution, 43: 1781—1795. TYLER, S., 1988, The role of function in determi- nation of homology and convergence— examples from invertebrate adhesive organs. Fortschritte der Zoologie, 36: 331-347. WESTHEIDE, W. & R. M. RIEGER, 1987, System- atics of the amphi-Atlantic Microphthalmus- listensis-species group (Polychaeta: Hesion- idae). Facts and concepts for reconstruction of phylogeny and speciation. Zeitschrift für Zoolo- gische Systematik und Evolutionsforschung, 25: 12-39. WILEY, E. O., 1979, An annotated Linnean hierar- chy, with comments on natural taxa and compet- ing systems. Systematic Zoology, 28: 308-337. WILEY, E. O., 1981, Phylogenetics. The theory and practise of phylogenetic systematics. John Wiley & Sons, New York, 439pp. YONGE, C. M., 1947, The pallial organs in the as- pidobranch gastropods and their evolution throughout the Mollusca. Philosophical Transac- tions of the Royal Society of London, B232: 443— 518, 1 pl. APPENDIX Corrections of Haszprunar (1988) (1) p. 377: replace “McLean, 1987” by “McLean, 1988”. (2) р. 378/legend Fig. 1: Replace “Ponder, 1987” by “Ponder, 1988a”. (3) p. 381: So far as is known Truncatel- loidea—Vitrinellidae have monopectinate gills (e.g. Bieler & Mikkelsen, 1988). (4) p. 389, p. 400/Table 2, p. 416: As re- cently outlined by Houbrick (1989), | have misinterpreted his earlier data on Campanile symbolicum, listing “eggs connected by cha- lazae” for this taxon. In fact, campanilid egg- mass connections resemble those found in the Epitoniidae. True chalazae are present in the Valvatidae, however. (5) р. 400/Table 2: A loss of teleoconch oc- curs also in numerous euthyneuran taxa. (6) p. 401/Table 2: Tubular salivary glands with ducts occur in patelloid Docoglossa (Pa- tellogastropoda), but not in Lepetelloidea. (7) р. 401/Table 2: А cord-like visceral loop throughout its length is restricted to the Patel- loidea and Nacelloidea (Neolepetopsidae?). (8) p. 401/Table 2: Eyes with a lens also occur in the Fissurellidae and Scissurellidae. (9) p. 413: Replace “Haszprunar, 1988” by “Haszprunar, 1989”. (10) p. 420: Bieler (1988) found some more diagnostic differences between Archi- tectonicidae and Mathildidae. (11) p. 424/Fig. 5: Points 41 and 42 should be interchanged. (12) p. 428/Table 5a: The arrangement and subordination of “Superfamily Hot-Vent group А (Melanodrymia)” and “Superfamily Neomphaloidea” might appear to include them in the Neritimorpha. Judged from text (pp. 412-414) and phylogram (р. 424/Fig. 5), it should be clear that this is not the case, however. (13) р. 428/Table 5a: Change “Nacel- loidea Lindberg, 1988” to “Nacelloidea Thiele, 1891”; “Helicinoidea Thompson, 1980” to “Helicinoidea Férrusac, 1822”; and 202 HASZPRUNAR “Scissurelloidea McLean & Haszprunar, 1988” to “Scissurelloidea Gray, 1847.” Ac- cording to Ponder and Warén (1988) it should be “Ampullarioidea Gray, 1824”; “Janthi- noidea Lamarck, 1810”; “Littorinoidea Gray, 1840”; “Tonnoidea Suter, 1913”; and “Ptero- trachoidea Férrusac, 1821” should be re- placed by “Carinarioidea Blainville, 1818.” (14) p. 430/Table 5d: The wrong (printer's error) ranking should be corrected so that N. N. (“Helicoida”) becomes superior to Neriti- morpha and N. N. (“Euhelicoida”). (15) p. 436: Mackie (1984) was missing in the reference list. (16) The symposium-volume, “Proso- branch phylogeny,” was published in late 1988, and there are differences between the published papers and the manuscripts and ab- stracts that were made available to me prior to publication (Bieler, 1988; Healy, 1988b; Hou- brick, 1988; Lindberg, 1988; Ponder, 1988; Ponder 8 Warén, 1988). For example, Pon- der's (1988) “Cingulopsoidea Fretter & Patil, 1958” was not included in my classification, for nomenclatorial corrections; see (13). The editor-in-chief of Malacologia welcomes letters that comment on vital issues of general importance to the field of Malacology, or that comment on the content of the journal. Publication is dependent on discretion, space available and, in some cases, re- view. 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TAYLOR A InTOdUCHON По eee a RB ET SE RUN. YURI I. KANTOR JOHN D. TAYLOR The Anatomy of the Foregut and Relationships in the Terebridae JAMES NYBAKKEN Ontogenetic Change in the Conus Radula, its Form, Distribution the Radula Types, and Significance in Systematics and Ecolo ALAN J. KOHN A Tempo and Mode of Evolution in Conidae ..... O pa PHILIPPE BOUCHET = Turrid Genera and Mode of a fae The Use ae Abuse ‹ toconch Morphology .. НЫЕ я Е. ALISON KAY | jie Turrid Faunas of Pacific Islands... . 2-50)... ties а MALACOLOGIA CONTRIBUTED PAPERS т RITA TRIEBSKORN & С. KUNAST TAN RE Ultrastructural Changes in the Digestive System of Deroceras tum (Mollusca; Gastropoda) Induced by Lethal and S trations of the Carbamate Molluscicide Cloethocarb .. ROGER R. ES ian Waters: A Dre ee Re ee ral he Ape RUDIGER BIELER & RICHARD E. PETIT On the Various Editions of Tetsuaki Kira’s “Colourec Shells of Japan” and “Shells of the Western Paci i an Annotated List of New Names Introduced . JOSE ANGEL ALVAREZ PEREZ, MANUEL HAIMOVICI a JOAO CANTOS BRAHM COUSIN ARC Eledonids (Cephalopoda: Octopoda) ALAN R. KABAT Predatory Ecology of Naticid Ta ON with a ЕР ие AE RER EE ES CEE EE Letters to the East HN GERHARD HASZPRUNAR | ag à Towards a i ee tae ch of Gastropoda F odology—A Reply .. BE don'ts Te. ое ЗА В очен НЯ en у A h Ñ у 3 ЩИ 4 Hu ternational Journal of Malaco о } Lu ‚Journal International de hr of A} air: + _ Международный Журнал Manako Internationale MALACOLOGIA Editor-in-Chief: GEORGE M. DAVIS Editorial and Subscription Offices: Department of Malacology The Academy of Natural Sciences of Philadelphia Nineteenth Street and the Parkway Philadelphia, Pennsylvania 19103, U.S.A. Co-Editors: EUGENE COAN CAROL JONES California Academy of Sciences Dundalk, MD San Francisco, CA Assistant Managing Editor: CARYL HESTERMAN Associate Editors: JOHN B. BURCH University of Michigan Ann Arbor ANNE GISMANN Maadi Egypt MALACOLOGIA is published by the INSTITUTE OF MALACOLOGY, the Sponsor Members of which (also serving as editors) are: KENNETH J. BOSS, JAMES NYBAKKEN, President Museum of Comparative Zoology Moss Landing Marine Laboratory Cambridge, Massachusetts California JOHN BURCH, President-Elect CLYDE F. E. ROPER Smithsonian Institution MELBOURNE R. CARRIKER University of Delaware, Lewes Wasmngion, I: GEORGE M. DAVIS W. D. RUSSELL-HUNTER Secretary and Treasurer Syracuse University, New York | SHI-KUEI WU CAROLE S. HICKMAN, Vice-President Year: University of California, Berkeley University of Colorado Museum, Boulder Participating Members EDMUND GITTENBERGER JACKIE L. VAN GOETHEM Secretary, UNITAS MALACOLOGICA Treasurer, UNITAS MALACOLOGICA Rijksmuseum van Natuurlijke Koninklijk Belgisch Instituut Historie voor Natuurwetenschappen Leiden, Netherlands Brussel, Belgium Emeritus Members J. FRANCIS ALLEN, Emerita ROBERT ROBERTSON Environmental Protection Agency The Academy of Natural Sciences Washington, D.C. Philadelphia, Pennsylvania ELMER G. BERRY, NORMAN F. SOHL Germantown, Maryland U.S. Geological Survey Reston, Virginia Copyright © 1991 by the Institute of Malacology 1991 EDITORIAL BOARD J. A. ALLEN Marine Biological Station Millport, United Kingdom E. E. BINDER Muséum d'Histoire Naturelle Genève, Switzerland A. J. CAIN University of Liverpool United Kingdom P. CALOW University of Sheffield United Kingdom A. H. CLARKE, Jr. Portland, Texas, U.S.A. B. C. CLARKE University of Nottingham United Kingdom R. DILLON College of Charleston SC, U.S.A. C. J. DUNCAN University of Liverpool United Kingdom E. FISCHER-PIETTE VAERERTER University of Reading United Kingdom E. GITTENBERGER Rijksmuseum van Natuurlijke Historie Leiden, Netherlands F. GIUSTI Universita di Siena, Italy A. N. GOLIKOV Zoological Institute Leningrad, U.S.S.R. S. J. GOULD Harvard University Cambridge, Mass., U.S.A. | 11 YO} YUI es | 77 A. V. GROSSU Universitatea Bucuresti, , Romania UN re J1M1 Y L...1 T. HABE Tokai University Shimizu, Japan R. HANLON Marine Biomedical Institute Galveston, Texas, U.S.A. J. A. HENDRICKSON, Jr. Academy of Natural Sciences Philadelphia, PA, U.S.A. K. E. HOAGLAND Association of Systematics Collections Washington, DC, U.S.A. B. HUBENDICK Naturhistoriska Museet Góteborg, Sweden S. HUNT University of Lancaster United Kingdom R. JANSSEN Forschungsinstitut Senckenberg, Frankfurt am Main, Germany (Federal Republic) В. М. KILBURN Natal Museum Pietermaritzburg, South Africa М. А. KLAPPENBACH Museo Nacional de Historia Natural Montevideo, Uruguay J. KNUDSEN Zoologisk Institut & Museum Kobenhavn, Denmark A. J. KOHN University of Washington Seattle, U.S.A. A. LUCAS Faculté des Sciences Brest, France C. MEIER-BROOK Tropenmedizinisches Institut Tubingen, Germany (Federal Republic) H. K. MIENIS Hebrew University of Jerusalem Israel J. E. MORTON The University Auckland, New Zealand J. J. MURRAY, Jr. University of Virginia Charlottesville, U.S.A. R. NATARAJAN Marine Biological Station Porto Novo, India J. VKLAND University of Oslo Norway T. OKUTANI University of Fisheries Tokyo, Japan W. L. PARAENSE Instituto Oswaldo Cruz, Rio de Janeiro Brazil J. J. PARODIZ Carnegie Museum Pittsburgh, U.S.A. W. F. PONDER Australian Museum Sydney R. D. PURCHON Chelsea College of Science & Technology London, United Kingdom У: Academia Sinica Qingdao, People’s Republic of China N. W. RUNHAM University College of North Wales Bangor, United Kingdom S. G. SEGERSTRALE Institute of Marine Research Helsinki, Finland F. STARMUHLNER Zoologisches Institut der Universitat Wien, Austria У. |. STAROBOGATOV Zoological Institute Leningrad, U.S.S.R. W. STREIFF Université de Caen France J. STUARDO Universidad de Chile Valparaiso S. TILLIER Muséum National d'Histoire Naturelle Paris, France R. D. TURNER Harvard University Cambridge, Mass., U.S.A. W. S. S. VAN BENTHEM JUTTING J. A. VAN EEDEN Potchefstroom University South Africa N. H. VERDONK Rijksuniversiteit Utrecht, Netherlands B. R. WILSON Dept. Conservation and Land Management Netherlands, Western Australia H. ZEISSLER Leipzig, Germany (Democratic Republic) A. ZILCH Forschungsinstitut Senckenberg Frankfurt am Main, Germany (Federal Republic) UNITAS MALACOLOGICA Ninth International Malacological Congress Symposium Edinburgh, Scotland 1986 EVOLUTIONARY BIOLOGY OF OPISTHOBRANCHS Malcolm Edmunds Organizer and Editor Department of Applied Biology Lancashire Polytechnic Preston, United Kingdom Malacologia Guest Editor Christopher D. Todd Gatty Marine Laboratory University of St. Andrews Scotland MALACOLOGIA, 1991, 32(2): 203 EDITOR’S NOTE | accepted these papers for publication on 2 January 1991. Due to problems beyond the control of UNITAS this symposium was in danger of not being published. As the result of the concerted efforts of Malcolm Edmunds and Chris Todd in the fall of 1990, the manu- scripts were provided to Malacologia on com- puter disc. In order to expedite the publication of this symposium and to better serve UNITAS in a timely fashion, the publication of this sympo- 203 sium has not been delayed. Accordingly, lim- ited attempt has been made to make all pro- cedures for this publication conform exactly to Malacologia specifications. Our sympathy is with the authors and UNITAS. George M. Davis Editor-in-Chief Malacologia MALACOLOGIA, 1991, 32(2): 205-207 INTRODUCTION Malcolm Edmunds Department of Applied Biology, Lancashire Polytechnic, Preston In suggesting the title for this Symposium ‘Evolutionary Biology of Opisthobranchs’ | was aware of the wealth of recent studies on taxonomy, comparative morphology, neuro- physiology, zoogeography, faunistics and ecology; but while comparative morphology papers usually have an evolutionary theme, papers on zoogeography and neurophysiol- ogy rarely do. | was also aware that some talks (e.g. very specialized or narrowly taxo- nomic papers) can be tedious to listen to un- less one is just as badly bitten with the same enthusiasm bug as the speaker. | therefore decided to encourage papers from as wide a field of study as possible but united by an evolutionary theme. | hoped that this would make the Symposium of interest to the non- specialist biologist as well as to opistho- branch aficionados, and | hoped too that it might stimulate new approaches to those fields of study that have hitherto lacked an evolutionary approach. Did this strategy succeed? It is hardly for me to judge, but there are certainly some gaps in the range of subjects covered. There is nothing on neurophysiology, for example, but there are papers on comparative morphol- ogy, development and ecology. Most papers concentrate on the ever popular Nudibranchia and Ascoglossa, but there are others which deal with the Bullomorpha and the Aplysio- morpha, and there is even one which reviews current knowledge of a very little-known group, the Rhodopidae. The names used for the major taxa of opisthobranchs are still very far from being agreed by all workers. There is still contro- versy aver the most appropriate names for several of the orders: Bullomorpha or Ceph- alaspidea, Aplysiomorpha or Anaspidea, and Ascoglossa or Sacoglossa. Possible confu- sion with chordate class names together with the advantage of a name that relates to a typ- ical genus in the group suggest that use of Bullomorpha and Aplysiomorpha should be encouraged. But Ascoglossa versus Sacoglos- sa is more of a problem: both names relate to the radular sac or ascus. Having used Saco- 205 glossa for a quarter of a century the word As- coglossa still sticks in my gullet (or perhaps in my ascus like a discarded radular tooth), but since most of the recognized authorities on the group now prefer Ascoglossa, | guess | must discard my old preference into my ascus and accept the change. A century ago comparative morphology was the central plank of zoology. It was also used as an aid to devising a systematic arrangement, but there was rarely any discussion of evolution. Today comparative morphology is much more functional in its approach. It is still important, but primarily for the light it sheds on evolution, and only secondarily for the help it gives with classifi- cation. Classification today is an exercise in trying to devise a system that reflects the evolution of the group, while recognizing the limitations imposed by a rigid hierarchy of taxa which can never adequately take ac- count of the realities of the different evolu- tionary rates of different species. Similarly classical zoogeography was really little more than putting dots on maps whereas today one looks for causes of the geographical range of a particular species. These causes can be found in the animals physiology, ecology or development (Clark, 1975; Ed- munds, 1977), while a more detailed study gives insight into the process of speciation (Edmunds, 1982). Evolution occurs by means of natural selection, and the forces of natural selection have been studied exten- sively by observing changes in morph fre- quency in terrestrial gastropods such as Cepaea nemoralis (reviewed by Jones et al., 1977; Clark et al., 1978; and Cain, 1983), and also in some marine gastropods such as Littorina spp. (reviewed by Berger, 1983; and Raffaelli, 1982). No such studies have been made on opisthobranchs. Two reasons for this are the lack of a hard shell with easily quantifiable characters, and the difficulty of monitoring individuals and populations of such small animals in the sea. Yet such studies are now possible: many opistho- branch workers are expert SCUBA divers, 206 EDMUNDS and several polymorphic species of opistho- branch are now known which are ideal for such a study, for example the widespread Eu- ropean aeolid Eubranchus farrani (Forbes & Goodsir) (Edmunds & Kress, 1969), and the Indo-Pacific Phestilla minor Rudman (Rud- man, 1981). This Symposium includes papers that cover a variety of different aspects of the evolutionary biology of opisthobranchs. First there are three papers on food and feeding habits. Each major taxon of opisthobranchs is associated with a particular type of food: sponges for dorids, coelenterates for aeolids and dendronotaceans, and green algae for sacoglossans (sorry, ascoglossans). While some species of opisthobranch are eurypha- gous in their choice of food, others are stenophagous to the extreme of eating just a single species of prey. Jensen’s paper is essentially a comparative morphology study of the evolution of feeding structures in the Ascoglossa. While the fine details of feeding structures are closely linked to specific foods, Jensen is able to tease out those anatomical characters that indicate evolutionary relation- ships and which can also be used т classification. The second paper, by Cat- taneo Vietti and Balduzzi, reviews the food and radular characteristics of the Mediterra- nean genera of dorids. It then applies a method of correspondence analysis to the data set-and attempts to relate food to radular structure. A clear correlation is found be- tween radula width and diet, but the relation- ship between finer details of radular tooth shape and diet is not so evident. The third paper in this section by Picton examines food and feeding habits from yet a third viewpoint. It describes the feeding habits of a single species, the aberrant aeolid Cumanotus beaumonti, and relates this to its behaviour and ecology. The next group of papers relate to defence. The molluscan shell probably evolved as a defensive adaptation in a sluggish, benthic animal that would otherwise have been vul- nerable to faster moving, jawed predators (Edmunds, 1974). But the shell also has its disadvantages: it is cumbersome to carry around, its formation requires a lot of energy (which could perhaps be better expended in reproduction), it locks up a lot of calcium so that the animal can only live where there is a supply of this mineral, and it has a regu- larity of shape such that it is difficult to cam- ouflage from predators. With all these disad- vantages it is hardly surprising that some representatives of all three gastropod sub- classes have reduced and lost the shell. But it is in the opisthobranchs that shell reduction has occurred most often and been so out- standingly successful as judged by the diver- sity of form and number of species that are extant. Shell reduction and loss can only oc- cur provided that an animal has other means of defence including bodily appendages, col- oration and glandular secretions (Edmunds, 1966). The paper by Poulicek, Voss-Foucart and Jeuniaux presents the results of a de- tailed analysis of the chemical constitution of shells from a variety of opisthobranchs, some with well-developed shells, and others with reduced shells. It attempts to draw functional conclusions relating chemical constitution to the development (or reduction) of the shell, but precisely why one shell should have more chitin or lysine than another remains un- known. The second paper in this section by Garcia-Gömez, Medina and Covenas de- scribes the histology of the large mantle ‘glands’ of chromodorids. These are wide- spread in the family and their precise location has been used as a taxonomic character (Rudman, 1984). But this careful study shows that, far from being typical defensive glands opening on the dorsal mantle surface, they do not open to the exterior at all, hence the au- thors call them ‘mantle dermal formations’ rather than glands. Nevertheless they must surely have a defensive function (as evi- denced by their location), but whether they can only affect a predator that tears open the mantle, or whether appropriate stimulation causes the contents to burst out in the same way that nematocysts burst out of the cni- dosac of an aeolid even though it initially has no opening, is not known. The final paper in this section by Edmunds examines the evi- dence for the occurrence of warning colora- tion in nudibranchs. It concludes that some species probably are aposematic, it predicts likely consequences of aposematism which could be tested experimentally and it dis- cusses how aposematism may have evolved in nudibranchs. The third section of the Symposium covers embryological development and larval ecol- ogy. Soliman reviews the patterns of de- velopment of opisthobranchs with particular reference to those from the Red Sea, and compares these with the developmental pat- terns of prosobranchs. Todd reviews data on the development and larval ecology of Onchi- INTRODUCTION 207 doris bilamellata, and shows that the meta- morphosed juveniles spend several weeks feeding on detritus before they are large enough to attack the definitive adult prey (bar- nacles). The evolution of different modes of larval development is reviewed in the light of larval and adult feeding habits and prey avail- ability. The fourth section of the Symposium comprises a single ecological faunistic paper by Cattaneo Vietti and Chemello on the opisthobranch fauna of one particular habitat. Besides giving a list of the species found in one Mediterranean lagoon, this paper also reviews the species recorded from other lagoons in the Mediterranean. While the data are inevitably very incomplete, this is the sort of habitat that would be ideal to select for an investigation into the origin of an entire fauna. With knowledge of preferred foods, devel- opmental pattern, salinity tolerances and other physiological factors of the various species in the neighbouring sea, it should be possible to explain why some species are commonly found in lagoons while others are absent. The final section of the Symposium con- tains two papers on comparative morphol- ogy. The first, by Salvini-Plawen, is in classical mould using every available piece of anatomical information to build up a picture of the evolutionary relationships of a very little-known group of molluscs, the Rhodop- idae. A new genus, Helminthope, is de- scribed which has several differences from Rhodope. lt is now possible to argue the phylogenetic relationships of this group with much more confidence than has been possi- ble in the past, but, perhaps surprisingly, their systematic position still remains obscure. The final paper by Gosliner reviews the numerous examples of parallel evolution in opistho- branchs but here the comparative approach follows the phylogenetic cladistic method advocated by Hennig (1966) of uniting groups on the basis of shared derived (apomorphic) characters. Arguments con- cerning the relative merits of traditional evolutionary classification and of phylo- genetic cladistic methods are summarized by Ridley (1986). The conclusions reached on the basis of Gosliners analysis do not agree with those of all recent authors, some of whom link groups into taxa on the basis of shared ancestral (plesiomorphic) charac- ters. LITERATURE CITED BERGER, E. M., 1983, Population genetics of ma- rine gastropods and bivalves, pp. 563-596. In: RUSSELL-HUNTER, W. D. (ed.), Ecology. The Mollusca (ed. K. Wilbur) 6. Academic Press, Lon- don & New York. CAIN, A. J., 1983, Ecology and ecogenetics of ter- restrial molluscan populations, pp. 597—647. In: RUSSELL-HUNTER, W. D. (ed.). Ecology. The Mollusca (ed. K. Wilbur) 6. Academic Press, Lon- don & New York. CLARK, K. B., 1975, Nudibranch life cycles in the Northwest Atlantic and their relationship to the ecology of fouling communities, Helgolander wis- senschaftliche Meeresuntersuchungen, 27: 28— 69. CLARKE, B., ARTHUR, W., HORSLEY, D. T. & PARKIN, D. T., 1978, Genetic variation and nat- ural selection in pulmonate molluscs, pp. 219- 270. In: FRETTER, V. & PEAKE, J. (eds.), Sys- tematics, Evolution and Ecology. Pulmonates 2A. Academic Press, London & New York. EDMUNDS, M., 1966, Defensive adaptations of Stiliger vanellus Marcus, with a discussion on the evolution of ‘nudibranch’ molluscs. Proceedings of the Malacological Society of London, 37: 73— 81. EDMUNDS, M., 1974, Defence in animals: a survey of anti-predator defences. Longman, Harlow, 357 Pp. EDMUNDS, M., 1977, Larval development, oceanic currents, and origins of the opisthobranch fauna of Ghana. Journal of Molluscan Studies, 43: 301-308. EDMUNDS, M., 1982, Speciation in chromodorid nudibranchs in Ghana. Malacologia 22: 515-— 522: EDMUNDS, M. & KRESS, A., 1969, On the Euro- pean species of Eubranchus (Mollusca Opistho- branchia). Journal of the Marine Biological Asso- ciation of the United Kingdom, 49: 879-912. HENNIG, W., 1966, Phylogenetic Systematics. Uni- versity of Illinois Press, Urbana. JONES, J. S., LEITH, B. H. & RAWLINGS, P., 1977, Polymorphism in Cepaea: a problem with too many solutions? Annual Reviews of Ecology and Systematics, 8: 109-143. RAFFAELLI, D., 1982, Recent ecological research on some European species of Littorina. Journal of Molluscan Studies, 48: 342-354. RIDLEY, M., 1986, Evolution and Classification. Longman, London & New York, 201 pp. RUDMAN, W. В., 1981, Further studies on the anat- omy and ecology of opisthobranch molluscs feeding on the scleractinian coral Porites. Zoo- logical Journal of the Linnean Society, 71: 343— 412. RUDMAN, W. B., 1984, The Chromodorididae (Opisthobranchia: Mollusca) of the Indo-West Pacific: a review of the genera. Zoological Jour- nal of the Linnean Society, 81: 115-273. MALACOLOGIA, 1991, 32(2): 209 COMPARISON OF ALIMENTARY SYSTEMS IN SHELLED AND NON-SHELLED SACOGLOSSA (=ASCOGLOSSA) (GASTROPODA: OPISTHOBRANCHIA) Kathe R. Jensen Zoological Museum, Universitetsparken 15, DK-2100 Copenhagen ©, Denmark ABSTRACT The Sacoglossa comprise a “complete” evolutionary series from species with a large shell into which the animal can withdraw completely, over species with a reduced shell covering only the visceral mass, to shell-less (“nudibranchiate”) forms some of which have lateral wing-like ex- tensions, parapodia, others bearing leaf-like or cylindrical dorsal appendages, cerata. Phylogeny has been based on the morphology of the central nervous system and, in part, the reproductive system. It is surprising that the organ system most characteristic of the Sacoglossa, the alimen- tary system, has never been used when attempting to deduce phylogenetic relationships within the group. The Sacoglossa are all specialized suctorial feeders, and almost all are stenopha- gous herbivores. Hence, many anatomical adaptations to a particular food occur in the alimen- tary system. However, a number of characters seem to reflect phylogenetic relationships as well. The present study compares the alimentary system of 17 species of Sacoglossa. The characters which have phylogenetic importance are: Pharyngeal pouches (presence/ absence, size and shape), mode of attachment of the descending limb of the radula and its surrounding ascus-muscle, shape of radular teeth, branching pattern of digestive gland, and position of anus. Pharyngeal pouches occur in all genera of shelled Sacoglossa. Pharyngeal pouches also occur in all genera of the non-shelled Polybranchiidae (= Caliphyllidae), in some, but not all, species of Bosellia and Costasiella, and in Plakobranchus. Very few species of the family Elysiidae have pharyngeal pouches, and they are completely absent in the Stiligeridae and Hermaeidae. In these families the descending limb of the radula and its surrounding ascus- muscle is only attached to the pharynx anteriorly. In other sacoglossans the ascus-muscle is attached throughout its length. Three basic types of radular teeth occur in the Sacoglossa: Teeth with a ventral concavity and lateral denticles, blade-shaped teeth with or without denticles on the median cutting edge, and sabot-shaped teeth with a scoop-like cusp and a dorsal keel over which the preceding tooth fits. The first type of tooth resembles the central tooth of some cephalaspideans, hence must be plesiomorphic. Blade-shaped teeth occur in some shelled species as well as most non-shelled families, hence may have evolved more than once. Sabot-shaped teeth occur only in hermaeids and stiligerids. From the original solid digestive gland found in the shelled Sacoglossa and in the non-shelled Cyerce, forms evolved with two lateral main ducts. In the shelled genera Volvatella and Berthe- linia some digestive gland tubules extend into the mantle. In the cerata-bearing genera the digestive gland is composed of long, wide main tubules, sending lateral branches into the cerata, dorsal body surface and head region. In the Elysiidae, Plakobranchus and Bosellia the digestive gland consists of short main ducts sending a dense network of narrow branches throughout the body, including the head and parapodia. In the shelled Sacoglossa the anus is located in the posterior part of the mantle cavity. In the majority of unshelled species the anus is located at the anterior right corner of the pericardium. In some polybranchiids the anus is located laterally, below the anterior rows of cerata, and many hermaeids and stiligerids have an anal spout on top of the pericardium. 209 MALACOLOGIA, 1991, 32(2): 211-217 RELATIONSHIP BETWEEN RADULAR MORPHOLOGY AND FOOD IN THE DORIDINA (MOLLUSCA: NUDIBRANCHIA) Riccardo Cattaneo Vietti & Andrea Balduzzi Istituto di Zoologia dell’Universita degli Studi di Genova, Via Balbi 5, I- 16126 Genova, Italy ABSTRACT The diet of nudibranchs has been the subject of numerous reports and it is well known that different suborders select different types of prey. In the case of the Doridina, these are usually sponges, bryozoans and ascidians. The relationship between morphological characteristics of the prey and the functional mor- phology of radular structure has been studied in 28 genera of Doridina. These were put into 12 groups according to different radular models. These groups were identified by the combination of three different characteristics: number of teeth per half-row, shape of the teeth and their uniformity in each row. Employing literature data and original reports, it was possible to relate these 12 radular models with 136 species of prey, re-grouped under 23 different taxa, using correspondence analysis. First, the analysis discriminated the broad-radula groups, sponge eaters, from the narrow- and very narrow-radula groups, which have a more catholic diet. The narrow radular groups feed mainly on softer food (Ctenostomata Carnosa and Cheilostomata Anasca), while the groups with a very narrow radula feed more on harder organisms (Cheilostomata Ascophora, Cirripedia and solitary ascidians). The relationship of tooth shape to diet is less clear, while other anatomical characteristics, such as the presence of a suctorial apparatus or a caecate gut, are more clearly related to specific foods. INTRODUCTION The predator-prey relationship of dorida- ceans has been studied from a variety of view- points. Thompson (1958) demonstrated the role of food availability for dorid metamorpho- sis, while Miller (1961) and Bouchet & Tardy (1976) showed the importance of the prey in species distribution. Yoshioka (1982) de- scribed one prey’s response to predation while Harvell (1984) considered nudibranchs to be ‘prudent predators’ of bryozoan colonies. Elvin (1976) studied the role of chemotaxis, while several authors (Ros, 1974; Nybakken & East- man, 1977; Bloom, 1981; Chadwick & Thorpe, 1981) analysed the interspecific competition for food among sympatric species. Ros (1979, 1980) also gave evidence that doridacean stenophagy can be related to their K-selected ecological strategy. The radula may be a species-specific tool adapted to the animal’s particular prey. Feed- ing regimes for most species are quite narrow and the shapes of radulae correspond well to food preference (Nybakken & McDonald, 1981). Todd (1981), in his review of nudi- branch ecology, distinguished four trophic groups: sponge-grazers (dorids), bryozoan- 2 grazers (mainly dorids), hydroid-grazers (ae- olids) and ‘miscellaneous’ groups (including representatives of all nudibranch suborders). Generally the radula of a dorid which eats sponges differs markedly from that of a dorid feeding on sessile acorn barnacles or en- crusting bryozoans, but difficulties arise when trying to find the relationships between radu- lar morphology and prey within these two groups. In this paper an attempt is made to point out the relationship between morphological char- acters of the prey and functional morpholog- ical aspects of radular structure in 28 genera of Doridina. MATERIALS AND METHODS Data available in literature were used to- gether with original data collected by one of us (R.C.V.). We have used mainly the data reported by Miller (1961), Swennen (1961), Thompson (1964), McBeth (1971), Clark (1975), Ros (1975, 1978), Barletta (1976), Bloom (1976), Ryland (1976), McDonald & Nybakken (1978, 1980), Behrens (1980), Chadwick & Thorpe (1981), Todd (1981), Garcia & Bobo (1984), Thompson & Brown 212 CATTANEO VIETTI 8 BALDUZZI (1984), Millen (1985) and Millen 4 Gosliner (1985). In all, 28 genera of Doridina which occur in the Mediterranean Sea were used in the analysis, together with 136 species of prey from all over the world. The dorid genera have been divided according to their radular structure (Table 1). We have discriminated, first of all, broad (B), narrow (N) and very narrow (V) radulae, with >30, 4-30 and <4 teeth per half-row respec- tively. It is known that there are intraspecific and ontogenetic radular variations (Bertsch, 1976; Nybakken & McDonald, 1981) and that the number of teeth per row is statistically re- lated to the specimen’s weight (Bloom & Bloom, 1977), but in the genera considered here the number of teeth per half-row has a quite narrow range of variation. Moreover the differences in food between adult and young specimens were not taken into consideration. Secondly we have discriminated the tooth shape, considering separately simple hooked teeth (S), complex hooked teeth (C) and other teeth (O). In this last category we put all types of teeth difficult to catalogue as, for example, the long serrated ones of Aldisa, the flat ones of Ancula and those of Crimora. According to Bloom (1976) the curvature of the hook seems to be important in predation. In this work it is not considered because we have often seen variation in the hooks in the same row. Finally the similarity (A) or dissimilarity (D) in the shape of the teeth in the same row was considered. The prey data for each radular group of genera were first studied qualitatively as pres- ence or absence of a particular prey in the diet of each radular group. These data were then quantified to give a weighted predation value (V) for each prey, on the basis of the frequency of reports on diet of each nudi- branch species in the literature, according to the following formula: V; k= Nit , N, where Vi, k = weighted predation value by the k-th radular group on the i-th prey; №к = number of bibliographic rec- ords of predation by the k-th radular group on the i-th prey; N, =total number of bibliographic records of predation by the k-th radular group on the whole prey set. Both qualitative and weighted data were used for statistical analysis by a method of factorial analysis (correspondence analysis, Benzécri et al., 1973) which allows one to evaluate at the same time both the diet differ- ences between radular groups and the rela- tionship between these groups and different kinds of prey. Following the first analysis which treated all the prey species separately, further analyses were Carried out after re-grouping these spe- cies into 23 different taxa (generally orders) (Table 2), to reduce the noise of errors or dis- agreements in the prey determinations at a specific level. RESULTS Fig. 1a gives the results of a correspon- dence analysis of the presence/absence of particular prey in the diet of each radular group, keeping separated the data on all 136 prey species. It shows the expected discrim- ination between dorids with broad radulae (B) and a sponge diet, and those with narrow (N) or very narrow radulae (V) and a more cath- olic diet. This discrimination is very evident along the first axis, while along the 2nd, 3rd and 4th axes (these last two not represented in the figure) only three radular groups (NSA, VCA and NOD) are dispersed, all with a very specialized diet. The variances yielded by the first four axes are, however, low (11.5% for each axis): in fact the heterogeneity of the data and the al- ready mentioned problems of specific deter- mination of prey make the significance of this analysis doubtful. The results of the second group of analy- ses, carried out on the prey records put into 23 systematic groups and utilizing the weighted data, confirm many of the preceding observations. Three well-defined clusters are formed (Fig. 1b): the B cluster, with broad rad- ulae feeding nearly exclusively on demo- sponges; the N-V cluster, with narrow radulae and a non-sponge diet, and the NSA cluster, with narrow radulae feeding on calcareous sponges. The two radular groups VCA and NOD, which in the first analysis remained dis- criminate along different axes, in this case fall together in the N-V cluster: in fact, their diet is very unusual only at a specific level. It is clear that in this second analysis there is no dis- crimination between the finer differences of radula and diet within both the B cluster and RADULAR MORPHOLOGY AND FOOD IN DORIDINA 213 TABLE 1. Diet and anatomy in the Doridina. For details of radular models, see text. For each prey group the number of species present in the diet of every radular model is reported in parentheses. The other anatomical characters are: A = acaecate; C = caecate; NS = non-suctorian; S = suctorian. In the final columns: N = total number of single bibliographic records, and V = weighted value for each prey group (see text for derivation). Other Radular anatomical Prey groups models Dorid genera characters (number of species) N V BSA Doris, Archidoris, C, A Porifera Calcarea (1) 1 .01 Discodoris (= Anisodoris), Porifera Choristida (1) 1 .01 Peltodoris, Jorunna, Porifera Hadromerida (4) 5 .06 Platydoris, Carminodoris Porifera Halichondrida (6) 34 .47 Porifera Poecilosclerida (6) 11 15 Porifera Spirophorida (1) 1 .01 Porifera Haplosclerida (5) 15 .20 Porifera Dictyoceratida (1) 1 .01 Bryozoa Cheilostomata Ascophora (3) 3 .04 BCA Cadlina, Chromodoris, Porifera Homosclerophorida (1) 1 .02 Hypselodoris Porifera Choristida (1) 4 .08 Porifera Halichondrida (3) 4 .08 Porifera Poecilosclerida (3) 4 .08 Porifera Axinellida (1) 2 .04 Porifera Haplosclerida (2) 8 a7 Porifera Dictyoceratida (8) 15 .33 Porifera Dendroceratida (2) 7 15, BCD Rostanga A Porifera Halichondrida (2) 2 12 Porifera Poecilosclerida (11) 12 75 Porifera Haplosclerida (2) 2 12 BOA Aldisa A Porifera Halichondrida (1) 1 ale Porifera Poecilosclerida (5) Us .87 NSA Aegires NS Porifera Calcarea (3) 4 1 NSD Polycera, Greilada, Palio, NS Cnidaria Anthozoa Gorgonacea (1) 1 .02 Limacia, Thecacera Bryozoa Ctenostomata Stolonifera (3) 5 .14 Bryozoa Cheilostomata Anasca (12) 21 .60 Bryozoa Cheilostomata Gymnocystidea (1) 1 .02 Bryozoa Cheilostomata Ascophora (5) 6 alt Bryozoa Cyclostomata (1) 1 .02 NCD Acanthodoris, Adalaria $ Bryozoa Ctenostomata Carnosa (6) 15 57. Bryozoa Cheilostomata Anasca (4) 6 .23 Bryozoa Cheilostomata Ascophora (4) 5 19 NOD Crimora NS Bryozoa Cheilostomata Anasca (3) 3 1 VSA Polycerella NS Bryozoa Ctenostomata Stolonifera (4) 4 .80 Bryozoa Cheilostomata Anasca (1) 1 .20 VCA Trapania $ Entoprocta (1) 1 1 VCD Onchidoris, Goniodoris, $ Bryozoa Ctenostomata Stolonifera (1) 2 .02 Okenia, Diaphorodoris Bryozoa Ctenostomata Carnosa (4) 5 .07 Bryozoa Cheilostomata Anasca (9) 11 16 Bryozoa Cheilostomata Cribrimorpha (1) 1 .01 Bryozoa Cheilostomata Gymnocystidea (2) 2 .02 Bryozoa Cheilostomata Ascophora (14) 23 34 Bryozoa Cyclostomata (2) 2 .02 Crustacea Cirripedia (4) 5 .07 Ascidiacea (solitary ascidians) (6) 7, .10 Ascidiacea (colonial ascidians) (5) 9 ae! VOD Ancula S Entoprocta (1) 2 133 Bryozoa Ctenostomata Stolonifera (1) 1 116 Ascidiacea (colonial ascidians) (3) 3 .50 214 CATTANEO VIETTI & BALDUZZI TABLE 2. List of systematic groups of prey which have been regrouped for some analyses. Number of Prey groups species Porifera Calcarea Porifera Homosclerophorida Porifera Choristida Porifera Hadromerida Porifera Halichondrida Porifera Poecilosclerida 2 Porifera Axinellida Porifera Spirophorida Porifera Haplosclerida Porifera Dictyoceratida Porifera Dendroceratida — © © © -J O O1 BR OC) ND — ND © © — — D OO À D = BR bh mb 12 Cnidaria Gorgonacea 13 Entoprocta № — 14 Bryozoa Ctenostomata Stolonifera 6 15 Bryozoa Ctenostomata Carnosa 7 16 Bryozoa Cheilostomata Anasca 21 17 Bryozoa Cheilostomata Cribrimorpha 1 18 Bryozoa Cheilostomata Gymnocystidea 2 19 Bryozoa Cheilostomata Ascophora 18 20 Bryozoa Cyclostomata 3 21 Crustacea Cirripedia 4 22 Tunicata (solitary ascidians) 6 23 Tunicata (colonial ascidians) 5 Total number of species 136 the N-V cluster. Further analyses were there- fore carried out for these groups. From the analysis carried out on B groups only (Fig. 1c), it is now possible to discrimi- nate three of the four broad-radular models along the first axis (which is the only very sig- nificant one in this analysis). BCA radulae, feeding mainly on horny demosponges (Dic- tyoceratida and Dendroceratida), form a dis- tinct cluster at one extreme of the diagram. BCD and BOA radulae, linked to Poeciloscler- ida, form a second very discrete cluster at the other extreme. BSA radulae, with a more gen- eralized diet, form an intermediate group dis- persed along the second axis. The prey point of ascophoran bryozoans (no. 19) falls in this last cluster too, as the supposed diet of Platy- doris argo is the bryozoan Sertella. Fig. 1d presents the analysis carried out on the radular groups of the non-sponge eating genera. Radular groups VCA (Trapania) and VOD (Ancula) are clearly separated from the main group of genera: both include ento- procts in their diet. Trapania has no other food, while Ancula also feeds on colonial ascidians and bryozoans. VSA and NCD groups, both eating principally ctenostoma- tous bryozoans, are also well separated, showing a good relationship with Stolonifera and Carnosa respectively. The remaining radular groups form two clusters with just two intermediate points. The first cluster (VCD) shows a close relationship with ascophoran bryozoans, barnacles and solitary ascidians, and the second (NOD and NSD) with gorgo- naceans and anascan bryozoans. DISCUSSION The study of the relationship between rad- ular morphology and food in the Doridina still has many unresolved problems. Literature re- ports sometimes indicate as prey the organ- ism on which the nudibranch was crawling when it was collected: this makes some of the data unreliable. On the other hand widely dis- tributed nudibranchs may have different pref- erences in different geographical locations (McDonald & Nybakken, 1978): for example Goniodoris nodosa feeds on the ascidian Dendrodoa grossularia along the Atlantic French coast (Bouchet & Tardy, 1976), yet in England (Thompson & Brown, 1984) it feeds on fleshy ctenostomes. Other data appear surprising: for example, as mentioned above, Platydoris argo in the Mediterranean Sea (Ros & Gili, 1984) feeds on the bryozoan Sertella, but has a typical sponge-eating radula; Polycera atra grazes on the gorgonian Lophogorgia chilensis (Lew- bel & Lance, 1975), but other members of this genus feed exclusively on bryozoans. More- over, according to Ryland (1976), some dorida- ceans associated with bryozoans are not nec- essarily predators: sometimes they can feed on bacterial films and detritus. The investigation of gut contents can also create errors: while grazing on a sponge, a nudibranch can ingest other casual food such as polychaete larvae, copepods and algal fil- aments (Aboul-Ela, 1959). These prey are sometimes given a greater importance than the sponge itself. It is also surprising that some very common species, such as bryozoans of the genera Flustra, Chartella and Sertella or the sponge Petrosia ficiformis, have only one predator: this is probably due to scarcity of data. In spite of these problems this study con- firms the relationship between radula and RADULAR MORPHOLOGY AND FOOD IN DORIDINA 215 12 RADULAR MODELS 136 PREY SPECIES у, = 11.5% у) = 11.5% NSD NCD VSA NOD BOA BCD BCA BSA VOD NSA 4 RADULAR MODELS 12 PREY GROUPS = 62.8% „= 35.9% 12 RADULAR MODELS 23 PREY GROUPS 7 RADULAR MODELS 12 PREY GROUPS 34.0% 23.2% у 1 V2 FIG. 1. Diagrams to show the results of the ordination models along the 1st (x) and 2nd (y) axes, using correspondence analysis: a. on all 12 radular models and 136 prey species; b. on all 12 radular models and 23 prey groups; c. on 4 radular models that feed on 12 prey groups (demosponges and bryozoans); d. on 7 radular models that feed on 12 non-sponge prey groups. In each diagram the variance percentages yielded by the axes (v1 and v2 respectively) are reported. Radular model points are indicated by the same abbre- viations used in Table 1 (see text for explanation). Prey points are indicated by dots: in diagrams b, c and d numbers refer to the prey groups listed in Table 2. diet: dorids with broad radulae prey exclu- sively on sponges while those with narrow and very narrow radulae eat mainly soft (Bry- ozoa Anasca and Carnosa) and hard prey (Cirripedia, Bryozoa Ascophora, solitary as- cidians) respectively. Aegires, grazing on Cal- carea (Bertsch, 1980), is unusual among sponge-eaters in having a narrow radula, but with more than 20 teeth per row it is really intermediate between the broad- and narrow- radula groups. The relationship between tooth shape and diet remains unclear: in the most complex group (VCD) it is possible to find species feeding on barnacles (Onchidoris bilamel- lata), on a large variety of bryozoans (O. mu- ricata) and on tunicates (Goniodoris castanea and Okenia elegans). Only in the sponge- eaters can we note that complex hooked teeth (C) are used mainly on horny sponges, while the simple hooked teeth (S) are used on a much wider variety of sponges. This last 216 CATTANEO VIETTI & BALDUZZI type of tooth can also be found both in spe- cialist species (e.g. Peltodoris atromaculata which feeds exclusively on Petrosia ficiformis) and in more generalist species such as Archi- doris pseudoargus. In addition to these correlations between radular teeth and diet there are other anatom- ical and physiological adaptations to different foods. Among the anadoridaceans there are two types of feeding behaviour, linked to the presence or absence of a suctorial pump con- nected to the buccal mass. The non-suctorial groups (Polycera and allied genera, Crimora and Polycerella) are rasping feeders and have a diet based mainly on soft bryozoans, while the suctorial ones, such as Onchidoris or Goniodoris, are sucking feeders, which prey principally on harder organisms such as barnacles, solitary tunicates and strongly cal- cified bryozoans. Within the sponge-eating groups the gen- era Chromodoris, Hypselodoris and Cadlina graze mainly on horny sponges and have a caecate gut, while Rostanga and Aldisa feed mainly on the Poecilosclerida and have an acaecate gut. Probably this difference is linked to the different nature of the extra-cel- lular collagen matrix in the various demo- sponges (Bergquist, 1978) or to differences in the skeletal organization (Bloom, 1981). ACKNOWLEDGEMENTS We offer grateful thanks to Prof. M. Ed- munds (Lancashire Polytechnic, Preston) and Prof. M. Sara (University of Genoa) for their criticisms and to our colleagues F. Boero, M. Pansini and G. Pulitzer-Finali for their useful suggestions. LITERATURE CITED ABOUL-ELA, 1.А., 1959, On the food of nudi- branchs. Biological Bulletin of the Marine Biolog- ical Laboratory, Woods Hole, 117: 439—442. BARLETTA, G., 1976, Considerazioni sulla biono- mia dei Nudibranchi e sulla loro alimentazione. Conchiglie, 12: 117-128. BEHRENS, D.W., 1980, Pacific Coast Nudi- branchs. A Guide to the Opistobranchs of the Northeastern Pacific. Sea Challengers, Los Osos, California, 1-112 p. BENZECRI, J.L. et alii [35 authors], 1973, L’ana- lyse des correspondences. L'analyse des don- nées 2. Dunod, Paris, 1-619 р. BERGQUIST, P.R., 1978, Sponges. Hutchinson, London, 1-268 р. BERTSCH, H., 1976, Intraspecific and ontogenetic radular variation in opisthobranch systematics (Mollusca: Gastropoda). Systematic Zoology, 25: 117-122. BERTSCH, H., 1980, The nudibranch Aegires al- bopunctatus (Polyceratacea: Aegiretidae) preys on Leucilla nuttingi (Porifera: Calcarea). The Veliger, 22: 222-224. BLOOM, S.A., 1976, Morphological correlations be- tween dorid nudibranch predators and sponge prey. The Veliger, 18: 289-301. BLOOM, S.A., 1981, Specialization and noncom- petitive resource partitioning among sponge- eating dorid nudibranchs. Oecologia, Berlin, 49: 305-315. BLOOM, S.A. & C.F. BLOOM, 1977, Radular vari- ation in two species of sponge-rasping dorid nudibranchs. Journal of Molluscan Studies, 43: 296-300. BOUCHET, P. & J. TARDY, 1976, Faunistique et biogeographie des nudibranches des cötes fran- çaises de l'Atlantique et de la Manche. Annales de l'Institut Océanographique, Paris, 52: 205— 213. CHADWICK, S.R. & J.P. THORPE, 1981, An inves- tigation of some aspects of bryozoan predation by dorid nudibranchs (Mollusca: Opisthobran- chia). In: LARWOOD, G. P. & C. NIELSEN, eds., Recent and Fossil Bryozoa. Olsen & Olsen, Fre- densborg, Denmark, p. 51—58. CLARK, K.B., 1975, Nudibranch life cycles in the Northwest Atlantic and their relationship to the ecology of fouling communities. Helgolaender wissenschaftliche Meeresuntersuchungen, 27: 28-69. ELVIN, D.W., 1976, Feeding of a dorid nudibranch, Diaulula sandiegensis, on the sponge Haliclona permollis. The Veliger, 19: 194-198. GARCIA, J.C. 8 A. BOBO, 1984, Una nueva espe- cie de Polycera Cuvier (Mollusca: Nudibranchia) del litoral iberico. Cahiers de Biologie Marine, 25: 361-373. HARVELL, D., 1984, Why nudibranchs are partial predators: intracolonial variation in bryozoan pal- atability. Ecology, 65: 716-724. LEWBEL, G.S., & J.R. LANCE, 1975, Detached epidermal sheaths of Lophogorgia chilensis as a food source for Polycera atra (Mollusca: Opistho- branchia). The Veliger, 17: 346. McBETH, J.W., 1971, Studies on the food of nudi- branchs. The Veliger, 14: 158—161. McDONALD, G.R. & J.W. NYBAKKEN, 1978, Ad- ditional notes on the food of some California nudibranchs with a summary of known food hab- its of California species. The Veliger, 21: 110- 119. McDONALD, С.В. & J.W. NYBAKKEN, 1980, Guide to the Nudibranchs of California. American Malacologists Inc., Florida, 1-72 р. MILLEN, S.V., 1985, The nudibranch genera On- chidoris and Diaphorodoris (Mollusca, Opistho- RADULAR MORPHOLOGY AND FOOD IN DORIDINA 2, branchia) in the Northeastern Pacific. The Veli- ger, 28: 80-93. MILLEN, S.V. & T.M. GOSLINER, 1985, Four new species of dorid nudibranchs belonging to the ge- nus Aldisa (Mollusca: Opisthobranchia), with a revision of the genus. Zoological Journal of the Linnaean Society, 84: 195-233. MILLER, M.C., 1961, Distribution and food of the nudibranchiate Mollusca of the south of the Isle of Man. Journal of Animal Ecology, 30: 95-116. NYBAKKEN, J. & J. EASTMAN, 1977, Food pref- erence, food availability and resource partitioning in Triopha maculata and Triopha carpenteri. The Veliger, 19: 279-289. NYBAKKEN, J. & С. MCDONALD, 1981, Feeding mechanisms of West American nudibranchs feeding on Bryozoa, Cnidaria and Ascidiacea, with special respect to the radula. Malacologia, 20: 439—449. ROS, J.D., 1974, Competència i evolucié en es- pècies veines de gasterdpodes marins. Colloquis de la Societat Catalana de Biologia, 7: 101-121. ROS, J.D., 1975, Opistobranquios (Gastropoda: Euthyneura) del litoral ibérico. Investigacion pesquera, 39: 269-372. ROS, J.D., 1978, La alimentación y el sustrato en los opistobranquios ibéricos. Oecol. aquat., 3: 153-166. ROS, J.D., 1979, Tipos biológicos en los opisto- branquios. Actas 1° Simposio Iberico de Estudios del Benthos Marino, San Sebastian, р. 413- 440. ROS, J.D., 1980, Estrategias ecologicas en los Opistobranquios. Comunicaciones 1° Congreso Nacional de Malacologia, Madrid, 85-93. ROS, J.D. & J.M. GILI, 1984, Opisthobranches des grottes sous-marines de l'óle de Majorque (Balé- ares). Rapports et Procès-Verbaux des Ré- unions. Commission Internationale pour l'Ex- ploration Scientifique de la Mer Méditerranée Monaco, 29: 141-145. RYLAND, J.S., 1976, Physiology and ecology of marine bryozoans. Advances in Marine Biology, 14: 285-443. SWENNEN, C., 1961, Data on the distribution, re- production and ecology of the nudibranchiate molluscs occurring in the Netherlands. Nether- lands Journal of Sea Research, 1: 191-240. THOMPSON, T.E., 1958, The natural history, em- bryology, larval biology and post-larval develop- ment of Adalaria proxima (Alder 8 Hancock). Philosophical Transactions of the Royal Society of London, Series B, 242: 1-58. THOMPSON, T.E., 1964, Grazing and the life cy- cles of British nudibranchs. In: CRISP, D.J., ed., Grazing in Terrestrial and Marine Environments. Blackwell, Oxford, p. 275-297. THOMPSON, T.E. 8 G. BROWN, 1984, Biology of Opisthobranch Molluscs, volume 2. Ray Society, London, 1-229 p. TODD, C.D., 1981, The ecology of nudibranch mol- luscs. Oceanography and Marine Biology, An- nual Review, 19: 141-234. YOSHIOKA, P.M., 1982, Predator-induced poly- morphism in the bryozoan Membranipora mem- branacea. Journal of Experimental Marine Biol- ogy and Ecology, 61: 233-242. MALACOLOGIA, 1991, 32(2): 219-221 Cumanotus beaumonti (ELIOT, 1906), A NUDIBRANCH ADAPTED FOR LIFE IN A SHALLOW SANDY HABITAT? Bernard E. Picton Ulster Museum, Belfast BT9 5AB, U.K. ABSTRACT Many of the anatomical peculiarities of the family Cumanotidae are possibly explained by the ecology of the species. New observations on the habitat and diet of the species Cumanotus beaumonti suggest that the broad foot, long muscular cerata modified for swimming and unusual spawn coil are adaptive features which enable Cumanotus to be successful in a shallow sandy environment feeding on the hydroid Corymorpha nutans. INTRODUCTION The aeolid nudibranch Cumanotus beau- monti has been rather enigmatic since its al- most simultaneous discovery in southern En- gland and Norway during the first decade of this century. Recent publications describing the British fauna have relied on the original descriptions of this species, and little was known about its habitat and ecology. The dis- covery of populations in Northern Ireland dur- ing 1985 and direct observations by SCUBA diving have provided new information about this attractive aeolid. Synonymy Coryphella beaumonti Eliot, 1906 Cumanotus laticeps Odhner, 1907 Description The body is 20-25 mm long in mature specimens and the foot is broad, about 8 mm wide. There are prominent propodial tenta- cles at the front corners of the foot and small oral tentacles on the anterior corners of the head. Two smooth erect rhinophores are placed close together on the top of the head; they are shorter than the surrounding cerata (Fig. 1). The cerata are long and numerous, exceeding three-quarters of the body length; the anterior ones arise in front of the rhino- phores. The cerata are arranged in rows, 6 rows of up to 9 cerata arise from the anterior liver ducts and 6-7 single rows of up to 8 cerata arise from the posterior liver. Elongate cnidosacs can be seen at the tips of the cer- ata. The anal papilla is on the right side of the 219 body, between the cerata arising from the an- terior and posterior liver. The coloration of the body is pellucid white, becoming rosy pink in the dorsal and head region. The digestive gland is purple in colour. The dorsal surface and cerata are speckled with gold-coloured pigment, concentrated in the head region. The reproductive system consists of a coiled ampulla, two bursae, and a coiled vas deferens leading to a large penial sheath con- taining an extensively coiled penis. There are two distinctive rosettes of tubercles tipped with tiny chitinous hooks alongside the female aperture, as noted by previous authors. The radula of a 20 mm preserved specimen consisted of 20 rows of teeth of formula 1— 1—1. The central tooth is horseshoe-shaped, with a strong central denticle and 11—16 small denticles on either side. The lateral teeth also have strong main denticles and cutting edges of 13—20 small denticles. The radula tapers rapidly from the oldest row with central tooth 50 um wide to the youngest row, with central tooth 200 um wide. Biology Fifteen specimens were collected in June 1985 in Church Bay and one from Arkill Bay on Rathlin Island, Co Antrim, Northern Ire- land. The animals were either crawling on a sea-bed of medium sand in 15 m of water or were at the tops of the stalks of the hydroid Corymorpha nutans M Sars, 1835, which was common on the sand. This hydroid consists of a solitary stem, 50-100 mm tall, bearing a single large polyp which measures 15-20 mm across the ring of long, undulating tenta- cles. Animals on the Corymorpha stems were 220 PICTON Fig. 1. Cumanotus beaumonti, dorsal view of a living specimen (length 20 mm). in the process of devouring the polyps, and were inconspicuous, with their long, flowing cerata looking very similar to the tentacles of the hydroid. Spawn coils of Cumanotus were more numerous than the animals, and con- sisted of two to four turns of egg-bearing jelly attached to the sand by a long, string-like por- tion covered with sand grains. Specimens were seen to swim vigorously by moving their cerata in a co-ordinated back and forth motion when collected or disturbed. DISCUSSION Two other species of the family Cumano- tidae have been described: Cumanotus cue- noti Pruvot-Fol, 1936, and Cumanotus fer- ECOLOGY OF CUMANOTUS BEAUMONT] 221 naldi Thompson & Brown, 1984. Cumanotus cuenoti has recently been redescribed by Tardy & Gantes (1980) and is a smaller ani- mal with no trace of oral tentacles or propodial tentacles and only 5—9 denticles on the cen- tral and lateral teeth. It has no surface pig- mentation apart from a small orange mark on the head of some individuals. Cumanotus fer- naldi was proposed as a new name for the species described as Cumanotus beaumonti by Hurst (1957) from the Pacific coast of North America. This species is illustrated by Thompson (1976), Thompson & Brown (1976), Behrens (1980) and McDonald & Ny- bakken (1980). It differs from C. beaumonti in colouration, having white apical bands of pig- ment on the cerata, yellowish-brown digestive gland and none of the gold speckling of C. beaumonti. Thompson (1984) reports that the radula is also different, with a slender central cusp flanked by up to 26 denticles on the cen- tral tooth and a short cusp on the lateral tooth flanked by 28 denticles. All known species of Cumanotidae appear to feed on athecate hydroids. The present species feeds on Corymorpha nutans as re- ported above, C. cuenoti feeds on Ectopleura dumortieri and Tubularia according to Tardy & Gantès (1980), and Behrens (1980) reports that C. fernaldi feeds on Tubularia. Cumano- tus species have a number of unusual fea- tures in which they differ from most other ae- olid nudibranchs. Several of these features could be adaptations to life on unstable sed- imentary sea-beds, feeding on transitional populations of hydroids. Tardy & Gantès (1980) point out the resemblance between the ceratal morphology, broad foot and spawn coils in Cumanotus and Cerberilla and sug- gest that Cumanotus may be capable of bur- rowing. The ability to swim up into the water column was reported for C. fernaldi and C. cuenoti, and is shared by the C. beaumonti populations reported here. Tardy & Gantès speculate on the possibility that this enables Cumanotus populations to follow medusae of their reproducing prey to areas down-current where new populations are being established. There is some evidence from the present ob- servations that this may actually happen. On Rathlin Island there was a steady current of 0.5—1 knot and many more spawn coils than seemed possible for the observed population of Cumanotus. At sites off Kilkeel, Co Down, in May 1984 numerous spawn coils and stalks of Corymorpha nutans were seen on the muddy sand sea-bed, but no adult animals could be found despite extensive searching. Is it possible that the animals had exhausted their food supply at this site and dispersed en masse in search of new pastures? ACKNOWLEDGEMENTS | would like to thank my diving companions Christine Howson and Dave Connor for sup- port in the field when these observations were made. The work was carried out during a sur- vey of the Northern Ireland coastline financed by the Conservation Branch of the Depart- ment of the Environment (N.l.) and directed by David Erwin of the Ulster Museum. Thanks are also due to Heather White of the Ulster Museum for the illustration. LITERATURE CITED BEHRENS, D. W., 1980, Pacific Coast Nudi- branchs. Sea Challengers, Los Osos, California, 1-112 p. ELIOT, С. М. E., 1906, Notes on some British nudi- branchs. Journal of the Marine Biological Asso- ciation, U.K., 7: 333-382. ELIOT, C. N. E., 1908, On the genus Cumanotus. Journal of the Marine Biological Association, U.K., 8: 313. McDONALD, G.R. & J.W. NYBAKKEN, 1980, Guide to the nudibranchs of California. American Malacologists Inc., Melbourne, Florida, 1-72 р. TARDY, J. & H. GANTES, 1980, Un mollusque nudibranche peu connue: Cumanotus cuenoti A. Pruvot-Fol, 1948; redescription, biologie. Bulletin de la Sociéte zoologique Française, 105: 199— 207. THOMPSON, T.E., 1976, Nudibranchs. T. F. H. Publications, Inc., New Jersey, 1—96 p. THOMPSON, T.E. & G.H. BROWN, 1976, British opisthobranch molluscs. Synopses of the British Fauna (New Series), No. 8, 1-203 р. THOMPSON, T.E. & G.H. BROWN, 1984, Biology of Opisthobranch Molluscs, volume 2. Ray Soci- ety, London, 1-229 р. MALACOLOGIA, 1991, 32(2): 223-232 REGRESSIVE SHELL EVOLUTION AMONG OPISTHOBRANCH GASTROPODS Mathieu Poulicek,''* Marie-Françoise Voss-Foucart? & Charles Jeuniaux? ABSTRACT Many opisthobranch molluscs have reduced or lost their shells during evolution. This paper discusses the microstructural and chemical changes associated with shell regression in opistho- branchs. All shells of benthic species examined so far (twelve species belonging to Pyramidel- lacea, Cephalaspidea and Anaspidea) show the same features: two thick layers of complex crossed-lamellar material below one thin external layer of granular or homogeneous structure. The shells of thecosomatous pteropods (six species with a planktonic mode of life) show an inner helicoidal structure surmounted by a thin granular layer. An intermediate condition is found in the most primitive pteropods (Limacina) with a complex crossed-acicular fabric under the granular one. The degree of calcification, chitin content and amino acid composition of both acid-soluble and insoluble fractions of shells of 20 species belonging to Cephalaspidea, Pyra- midellacea, Anaspidea, Notaspidea, Sacoglossa and Pteropoda are presented. The degree of calcification shows a marked tendency to decrease and the chitin content to increase from the primitive to the more advanced species. The amino acid content of both protein fractions ap- pears relatively stable in all species, and very similar to that of prosobranchs, although there are some minor variations. All these features can be correlated with the need for suppleness in very thin reduced shells that would otherwise be too brittle. These features are polyphyletic and convergent with shells of other molluscs showing the same tendency to reduce the shell (ceph- alopods, heteropods, pulmonate slugs, Polyplacophora). INTRODUCTION The Opisthobranchia are not defined by a set of features common to all members of the subclass but by certain marked tendencies, one of which is the tendency to lose or to reduce the shell in the course of evolution. Some of them still retain the shell and even the operculum (e.g. the Pyramidellidae and Acteonidae); in others, the shell has become greatly reduced, either remaining external, or internal and covered by two folds of the man- tle that may fuse dorsally. In the majority of Opisthobranchia, the shell disappears at the end of larval life. “No doubt some of the early evolutionary experiments along these lines ended in failure, but many more were partially or totally successful and we are fortunate in that modern oceans contain about three thou- sand species of gastropods which show inter- mediate stages in the general trend outlined above” (Yonge & Thompson, 1976). The goal of this paper is to try to describe and understand the process of shell regres- sion at a microstructural and biochemical level. This 'neo-conchological' approach will take into account the principles of Florkin (1966), i.e. that the molecular aspects of ad- aptation and phylogeny must rely upon rela- tionships established following ‘classical’ methods (anatomy, embryology, etc.) in order to detect molecular convergences. So we base this paper on the approach of Ghiselin (1966) in which “the comparative and func- tional anatomy of the reproductive system throughout the subclass is treated critically to provide a sounder basis for phylogenetic studies”. We will attempt to outline the ways the shell has changed along some of the main evolutionary lines of the phylogenetic tree proposed by Ghiselin (1966) (Fig. 1). The phylogeny of thecosomatous pteropods adopted here is that of Rampal (1973) (Fig. 2). The authors wish to dedicate this paper to the memory of Professor C. M. Yonge in rec- ognition of his long-standing interest in, and contribution to, malacology. MATERIALS AND METHODS All molluscs studied were collected alive. After removal of the soft parts, the shells were ‘Senior Research Assistant of the National Fund for Scientific Research of Belgium (FNRS) 2Department of Morphology, Systematics and Animal Ecology, Zoological Institute, State University of Liège, 22 quai Van Beneden, B-4020 Liège, Belgium 224 POULICEK, VOSS-FOUCART & JEUNIAUX UMBRACULIDAE PLEUROBRANCHIDAE THECOSOMATOUS PTEROPODS PHILINIDAE SCAPHANDRIDAE ATYIDAE BULLIDAE PTEROPODA RETUSIDAE СЕРН^ Py, KA MID ELT a CEA APLYSIIDAE AKERATIDAE : à OXYNOACEA 5 < coh ey Ng а 5 Q a 5 = HYDATINIDAE ACTEONIDAE UN FIG. 1. Phylogeny of opisthobranch gastropods (simplified from Ghiselin, 1966). cleaned from the periostracal layers with a rotatory metal brush, washed in distilled water and either preserved dried (for SEM) or in 70% ethanol (for biochemical analyses). Scanning electron microscopy (SEM) Pieces of shell were cut from the last whorl, some distance away from the aperture and either broken under the dissecting micro- scope (fracture surfaces) or cut perpendicu- larly to the growth axis, polished and etched with 0.05N HCI. The material was fixed in 4% glutaraldehyde in 0.2M cacodylate buffer pH 7.4 (2 h), washed and postfixed in OsO, (2%) in the same buffer (2 h). After dehydration through graded ethanol series, the dried ma- terial was orientated and mounted onto Al- stubs with silver or nickel print, coated with 10nm Au-Pd in a cool-diode sputter coater (Balzers SCD 030). The material was ob- served with a Cambridge Scientific Instru- ments Stereoscan or a Siemens ETEC Auto- scan electron microscope operated at 20 kV. Biochemical analyses The shell material was ground and decalci- fied with 0.5N НС! at ambient temperature. REGRESSIVE SHELL EVOLUTION 225 STYIOLA = CRESEIS HYALOCYLIX ie LIMACINA CAVOLINIA CUVIERINA DIACRIA EUCLIO FIG. 2. Phylogeny of thecosomatous pteropods (redrawn from Rampal, 1973). The organic remains were centrifuged (18,000 rpm), washed and dried to constant weight. The supernatants were dialysed against H2O (min. 1/360 V/V) and the acid- soluble material recovered by evaporation in vacuum in a rotatory evaporator. For amino acid determinations, the material was hydrol- ysed with 6N НС! for 24 h at 105°C in vacuum. The amino acid patterns were analysed by automatic ion exchange chromatography (single column procedure according to Deve- nyi (1971)). The method gives reproducible results of better than 1% at the 10—8M level for identical runs (Ghiselin et al., 1967). Chitin was estimated by the specific enzymatic method of Jeuniaux (1965). Its accuracy is better than 4% for chitin weights above 15 yg. RESULTS Scanning electron microscopy Fractures and etched polished surfaces of shells of 18 species belonging to Cephalaspi- dea (9), Pyramidellacea (1), Anaspidea (2) and Pteropoda (6) were examined with SEM. The shells of all the twelve benthic species examined (Pyramidella terebelloides (A. Ad- ams), Acteon tornatilis (L.), Hydatina physis (L.), H. zonata (Gmelin), Bulla ampulla L., B. punctulata A. Adams, Scaphander lignarius (L.), Atys cylindricum Hinds, Haminoea hyda- tis (L.), Philine aperta (L.), Aplysia depilans Gmelin, A. punctata Cuvier) are aragonitic in nature and mainly of crossed-lamellar fabric, typical of more advanced gastropods. The shells of Pyramidellacea and Cephalaspidea are three-layered, with two thick layers of crossed-lamellar structure under a thin layer of homogeneous or granular material. The first order lamellae of the two crossed- lamellar layers are perpendicular to each other. The internal shells of Anaspidea (Apl- ysia spp.) are much less calcified except in the apex area where poorly organized cross- lamellar elements are obvious (Fig. 3). The shells of the six pelagic species exam- ined so far (Limacina inflata (Orbigny), Cre- seis acicula Rang, Hyalocylis striata (Rang), Euclio pyramidata (L.), Diacria trispinosa (Lesueur), Cavolinia longirostris (Lesueur)) look quite different. Apart from Limacina in- flata, the shells are built following the same scheme: under a thin granular layer, there is a crossed-acicular layer progressively becom- ing helicoidal close to the inner side of the shells (Fig. 4). These observations are con- sistent with the works of Be et al. (1972) and Bandel (1977) on the shells of Cuvierina col- umella and Cavolinia tridentata. The shell of Limacina inflata occupies an intermediate po- 226 POULICEK, VOSS-FOUCART & JEUNIAUX FIG. 3. SEM picture of the crossed-lamellar fabric at the apex of the shell of Aplysia punctata. Scale: 10um. FIG. 4. SEM picture of the helicoidal fabric at the inner side of the shell of Cavolinia longirostris. Scale: 10um. sition: under a thin granular layer, there are two poorly individualized layers of somewhat disorganized crossed-acicular fabric. This is consistent with the view that the Limacinidae are the most primitive pteropods (Rampal, 1973) (Fig. 2). Chitin and degree of calcification We have previously shown that the degree of calcification and the chitin content of mol- lusc shells can be discussed in an evolution- ary perspective (Goffinet & Jeuniaux, 1979; Poulicek, 1982; Poulicek & Kreusch, 1986). We have estimated the degree of calcification and the chitin content of the shells of 20 spe- cies of opisthobranchs, some with external shells, others with different degrees of shell reduction. The results are given in Table 1. Except in the case of Aplysia, Oxynoe and the Notaspidea, the organic content of the shells is low (< 1% of the dry calcified weight) as previously shown for other gastropod shells with crossed-lamellar fabric (Poulicek, 1982). The high organic content of Retusa is probably due to contamination since it is par- ticularly difficult to get rid of the periostracum in such tiny shells. Nevertheless there is a slight tendency for organic content to in- crease with shell regression, particularly in the internal shells. The chitin content data display the same features: low level (<1% of the insoluble or- ganic matter) in the external shells and higher levels of the chitin content in species with smaller internal shells. This tendency is par- ticularly obvious in the internal shells within each of the taxa Cephalaspidea, Anaspidea and Notaspidea: the chitin content is always >1% of the organic matter, close to 8% in Aplysia, Berthella and Berthellina. Amino acid composition Table 2 shows the amino acid composition of the proteins of the insoluble fraction of the shells of eleven species. The patterns are typical of ‘conchiolins’ with very high acidic amino acid content (Asp and Glu), and much Gly, Ala, Ser and Leu. The sum of these last six amino acids constitutes more than 60% of the total amounts of the residues in the insol- uble protein fraction of the shells. There is little Cys in most species and no OH-Pro (ex- cept in the case of Akera and Oxynoe (De- gens et al., 1967)). The variability between the different spe- cies is low, probably because they are all fairly closely related. The primitive Pyramidel- lacea and Cephalaspidea are characterized by high levels of Asp, whereas the shells of the notaspidean Umbraculum appear some- what peculiar with very high Pro content, and REGRESSIVE SHELL EVOLUTION 227 TABLE 1. Organic matter and chitin content in the shells of 20 species of Opisthobranchia. Calcified Decalcified Organic Weight of Chitin as % Type of weight weight content chitin of organic Opisthobranch species shell (mg) (mg) (%) (1.9) matter PYRAMIDELLACEA Pyramidella terebelloides external 3361.1 12.1 0.36 46.33 0.38 (A. Adams) CEPHALASPIDEA Acteon tornatilis (L.) external 2355.2 17.9 0.76 53.09 0.30 Нудайпа zonata (Lightfoot) external 1658.2 13.1 0.79 21.26 0.16 Retusa obtusa (Montagu) external 374.0 11.4 3.05 (4.32) (0.04) Bulla punctulata A. Adams external 3882.4 13:2 0.34 37.43 0.28 Scaphander lignarius (L.) external 1955.9 11.9 0.61 14.57 0.12 Atys cylindricum Hinds external 2533.3 11.4 0.45 41.16 0.36 Haminoea navicula (da Costa) external 1200.0 10.8 0.90 51.19 0.47 Philine aperta (L.) internal 493.2 3.2 0.65 42.80 1.34 ANASPIDEA ' Akera bullata Muller external 352.9 2.4 0.68 17.52 0.73 Aplysia punctata Cuvier internal 796.4 121.4 15.24 10234.02 8.43 A. depilans Gmelin(1) internal 224.4 32.7 14.57 2346.00 7.17 Dolabella auricularia (Lightfoot) internal 8386.2 9.6 0.11 369.89 3.85 NOTASPIDEA Umbraculum mediterraneum external 4583.6 71.9 1:57 582.39 0.81 (Lamarck) Tylodina citrina Joannis external 1552.5 29.2 1.88 289.08 0.99 Berthella plumula (Montagu) internal 1072.7 125.8 11273 9497.90 7.55 Berthellina citrina Ruppell & internal 361.0 38.0 10.52 3005.82 7.91 Leuckart SACOGLOSSA Oxynoe olivacea Rafinesque external 325.1 5.7 1575 41.04 0.72 THECOSOMATA Cavolinia longirostris (Lesueur) external 6307.7 16.4 0.25 56.50 0.34 C. tridentata (Niebuhr) external 1131.8 5.3 0.47 26.07 0.49 much Leu whereas Iso and Val are less abun- dant than in other shells. As far as amino acid composition of shell insoluble proteins is concerned, the evolu- tionary trends are not obvious. The ratio Gly/ Ala appears to increase in the course of ev- olution: it is 0.95 and 0.93 respectively in the shells of Pyramidella and Acteon, it reaches 1.31 in Philine and Aplysia and even 1.57 in Umbraculum. At the same time, the Leu and Iso content diminishes slightly with the reduc- tion of the shell, except in Umbraculum. Table 3 shows the amino acid composition of the proteins of the acid-soluble fraction of the shells of nine species. Once again, the typical molluscan shell pattern of soluble pro- teins is well shown: the sum of Asp, Gly, Ser and Glu residues amounts to 60 to 70% of the total amino acid residues. There is much less basic amino acid (Arg, Leu and His) than in the insoluble fraction. In opisthobranch shells, the relatively low concentration of Asp is com- pensated for by higher levels of Glu and very high amounts of Ser, which is much more abundant than in the acid-soluble fractions of prosobranch shells. The variability in the soluble proteins be- tween the different species is higher than in the case of the insoluble fraction. This vari- ability in composition may be related to its heterogeneity (Weiner et al., 1977; Samata et al., 1980; Poulicek, 1982; Poulicek et al., 1986), since it is composed of macromolecu- lar assemblages of several proteins, peptides and glycoproteins which differ from species to species (Krampitz, pers. comm.). This vari- POULICEK, VOSS-FOUCART & JEUNIAUX 228 2861 'A90INNOY Bas 'SADINOS SNOWeA шоц palidwod (2) ‘9961 ‘Iaouads y зиэбэа шод веа (1) 'ввиарщ ешиоле) ‘YO, ‘5щзолбио| вицолву ‘| D, :еаэелио SOLÁXO `о`О. :шпаивиеиреш шпповлашп ‘шп. чхоэим вау ‘M'Y, ‘EINIOS елаху “Sy, ‘euade эица “e'd, ‘вещз ejıng `3`8, “ejejound eyıng '9’8. :$/1еил0} иову “VY, :5арюэдале в/эршелАд ‘Vd. i mm __-=> q _ _ ———— (25-60) 72 Ole + POS О 96 zer 0 12274 622 vee 97€ v9'p c6 + Lov OHV (9’1-1'0) €'0 LEOFERO 860 +++ 9790 410 9£ 0 0,0 +++ 290 +++ +++ 140 SIH (L’r-21)9 2 88°0 + 192 SLe Loe LL'E DS 262 902 98'L lov 97€ ere ge 2 SAT (er-rı)r2 тир + 225 v02 09% LEE Sit 612 Lve 00'p 690 viv Ly'v G9'+ 3Hd (yr2-S'0) I'L eESO FELL ЛЬ 291 zer €90 68°0 €9'1 +++ М G9' | 96 0 990 HAL (001-197) FZ 19 = 128 62S 068 559 5600, 098 01'8 891 GL'L 96 8 69'6 816 na (9p-0'Z) LE LOL+ 607 vee 195 20% 991 29$ cov £6 € ege 96 + Lvs 85'6 OSI (L'€-9'0) УЕ Ур = гр Ge +++ 10 £65 [ем GAL +++ OL +++ 60+ +++ 13W (69-+v'€) 8 + LT +919 16S 019 209 #972 897 68'9 v8'9 119 26°9 85'9 9£ 9 WA (€'2-p"0) 60 vtg0+F6S0 el + E02 le 810 sro + вес + 2 4h SA (€°S1-2°S) 6°8 261 +516 SZ 866 cEbL 688 91'8 GO'OL S06 LE 028 078 68'8 Viv (8 ec-66)£ SL ca + 50711 bbbl 15 606 965+ 0Z'0L PLL” S8LE себ 100 "SgZ Gt'8 AD (2:01-9'€) 1'9 ESZF6GES 999 05 569 621 88% z8 9 lov 809 ce € 8172 862 Oud (Sv1-2'S) 28 УЕ + СЕКСЕ 296 L6 LL SZtL ZpOk 29+ ге: 4165. 990, 6pEL PLEL SEEL m5 (p'Z1-8'S) 9'8 УЕ = 196 9598 608 S06 I90L +06 I9'IL Se6 веер S28 68'6 $/`6 y3S (9'/-98'2) 9'p 06`0 + 24'S og ¿09 6/5 08S LoS e8'€ 8/9 5/9 v8'9 219 Le'9 HHL (s'81-6'9) pL OG Sel 6 Вр Beer TALL eect Убе 695 oOrzlt cect ZE9L 199% dSv 09 = М LL = М FO, TO ‘OO. “WN. (mv (у. “Bd. (isa. ‘d'a ‘Tv. ча, Salov (Sanjea эшэдха) ивэ/ ‘PS + чеэи ОМИУ (Z)VIHONVHIOSOHd VIHONVHSOHLSIdO a nn ——— ‘(SanpiSai H0L/aNPISal yy se passaidxe) BIYDURIGOSOJ, JO JEU} цим рэледилоэ elyoue1qou}sidO jo saisads || JO siiays ay, jo чоцоелз эатози! oiueB10 eu} JO uoljisodwoo рюе oulwy “2 37191 229 REGRESSIVE SHELL EVOLUTION ejejound eishidy ‘d'y :5щ5олбио] BIUIJOARD ‘| 9 :виаае эица “e y ‘snueubl sapueydedg ‘|S ‘шпэпви sÁy ‘uy “ejejnjound eng ‘d'a ‘ввиог eunep/H ‘Z'H SIHEUIO) иозу “Y Y ‘зэрюадэлэ ерарише.^а ‘Vd, 2861 'NSoI]noy ass 'sasinos зпомел WO} pelIduo) (1) 96 0 + Es 460 + 4611 877 eve ar SP oP oP 09'0 ner ur Sur Sur G6 1 9G'0 66 C SHV 950 + 201 930 + E05 cv | 65 081 g87 897 sl 081 9,7 ve L SIH ISO + le? 85`0 + S6'L 691 ¡a ZSil 651 (HEL 291 Secc 802 18'S SAT 650 + £l'C 9S°0 + 19+ 91° ve"! 6c 1 Lol ell ec! Ss6'! G6 0 157.407 3Hd 8r0 + 20 10 + 260 6c 1 16'0 sg0 960 er 08`0 sol 98`0 Oc"! 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ТУ, та, Sdlov ‘ps + UESW ‘ps + UESW ОМУ (L)VIHONVHIOSOHd VIHONVYEOHLSIdO (senpises 001/anpisa y y se passaldxa) ely9ue1qosold jo jeu} цим pajeduoo elyoueiqou}sidO jo saiads 6 jo sjeys ay, jo чоцоец ajqnjos-pioe omebio eu} jo uonisoduo9 рюе ouwy ‘€ 3191 230 POULICEK, VOSS-FOUCART & JEUNIAUX ability in amino acid composition is associ- ated with comparable variability in the pro- teins, peptides and glycoproteins of the different species. The reason why shells should be so variable in composition is prob- ably because each species’ shell is adapted to quite specific environmental conditions (temperature, salinity, sand or mud particle size, etc.), but the precise significance of this variation remains unknown or must await fur- ther data (Degens & Spencer, 1966; Degens et al., 1967; Ghiselin et al., 1967; Meenakshi et al., 1971; Gregoire, 1972; Poulicek, 1982). The only evolutionary conclusion that can be drawn from Table 3 is that a decrease of the Lys content of the fraction correlates with a reduction in calcification of the shells (Degens et al., 1967). Some amino sugars other than chitin are present in both fractions. The amount of car- bohydrate (mainly glucosamine and galac- tosamine) varies considerably throughout the phylum (Ghiselin et al., 1967), but in most mollusc classes the relative proportion of car- bohydrate to protein seems to have de- creased progressively with the evolution of the shells (Poulicek, 1982). This seems to be true also in the Cephalaspidea where those species with well-developed shells have high hexosamine/amino acid ratios and those with reduced shells have low ratios (Table 4). The primitive shelled Pyramidella also has a high ratio whereas the more advanced Thecoso- mata have a low ratio. The Notaspidea, Anaspidea and Sacoglossa are linked by their very high amino sugar content, even if chitin is not taken into account, and irrespective of whether the shell is external or internal. Table 4 also shows that the hexosamine/amino acid ratio is always higher in the insoluble fraction of the organic matrix than in the acid-soluble one. DISCUSSION AND CONCLUSIONS The Euthyneura are characterized by her- maphroditism, a tendency to lose the effects of torsion, a distinctive type of spermatozoon, a peculiar structure of the pallial complex and a heterostrophic larval shell (Ghiselin et al., 1967). But the most striking external feature of the whole group is a tendency towards shell regression, affecting all evolutionary lines of the opisthobranchs as well as some lines of pulmonates quite independently. Despite the regressive features altering the TABLE 4. Estimate of the ratio (hexosamines/ amino acids) x 100 in the acid-soluble and insoluble fractions of the shell organic matrix of 14 species of Opisthobranchia. Chitin was not taken into account in computing the hexosamines of the insoluble fraction. Insoluble Acid- fraction soluble (chitin Opisthobranch species PYRAMIDELLACEA Pyramidella terebelloides 1.86 4.38 fraction excluded) CEPHALASPIDEA Acteon tornatilis 1.88 4.20 Hydatina zonata 1.44 — H. physis (1) — 3.73 Bulla punctulata 1.38 3.94 B. striata (1) = 2.93 Philine aperta 0.67 2.81 ANASPIDEA Akera soluta (1) — 5.40 Aplysia punctata 3.48 = A. willcoxi (1) — 4.55 NOTASPIDEA Umbraculum mediterraneum — 3.99 SACOGLOSSA Oxynoe olivacea — 3.04 THECOSOMATA Cavolinia longirostris 0.22 — C. tridentata — 2.12 (1) Computed from data in Degens et al., 1967. (1) Data from Jeuniaux, 1963; remainder original (2) Data from Degens & Spencer, 1966. (3) Compiled from various sources, see Poulicek, 1982 shells macroscopically, there is no fundamen- tal reworking of shell structure nor of the chemical composition of its organic matrix. The crossed-lamellar architecture of all shells of benthic opisthobranch species examined is typical of gastropods with a similar level of complexity (i.e. similar to that of mesogastro- pod and neogastropod prosobranchs) (Pou- licek, 1982). Even the most altered internal shells (as in Aplysia) exhibit the same kind of crossed-lamellar fabric. The helicoidal micro- structure of thecosomatous pteropod shells is presumably adaptive, but can be directly de- rived from the crossed-lamellar type via some kind of crossed-acicular microstructure. The most primitive Thecosomata (Limacina) ac- tually exhibit such intermediate microstruc- tural features. A helicoidal fabric of the same REGRESSIVE SHELL EVOLUTION 231 type is also found in shells of the phylogenet- ically unrelated heteropods (prosobranchs with a similar planktonic mode of life) (Batten & Dumont, 1976). The organic matrix isolated from the shells is composed of an insoluble chitin-protein complex and an acid-soluble glycoprotein fraction whose amino acid patterns are typical of ‘conchiolins’ isolated from shells of crossed-lamellar fabric, whatever the origin of the shell. In both prosobranchs and opistho- branchs it appears that as one goes from primitive to more advanced species, the hex- osamine content decreases, the Gly/Ala ratio increases, and the Lys content, which is linked to the degree of calcification, de- creases. However, the covariant groups of amino acids described by Degens et al. (1967) are not found here, thus confirming the close relationship of the species. The chitin content and degree of calcification have been shown to be linked in the evolution of mollusc shells (Poulicek, 1982; Poulicek et al., 1986). This relationship is confirmed here: as opisthobranch shells get smaller so their chitin content increases and the degree of calcification decreases. Prosobranchs, by contrast, show a tendency to develop lower chitin content and higher levels of calcifica- tion. This variation in chemical composition of shells must have some adaptive (functional) significance, and where parallel changes in composition occur in unrelated groups it is reasonable to seek for similar causes. In most molluscs, the essential functions of the or- ganic matrix of the shells (contributing to its strength) are carbonate nucleation, shell min- eralization and maintenance of shell integrity (Degens et al., 1967; Poulicek, 1982; Pou- licek & Voss-Foucart, 1984; Poulicek et al., 1986). While shells may vary in the organic matrix, these key features are retained. In opisthobranchs, however, the shells become thinner and a further decrease in organic con- tent would cause them to become brittle. This brittleness has been avoided by opistho- branchs in three different ways: 1. Incorporation of OH-Pro in the insoluble protein matrices of Anaspidea and Sa- coglossa. This probably makes the shell more flexible (Ghiselin et al., 1967), par- ticularly as these shells generally have a high protein content. 2. Increase of the chitin content of the shells in Cephalaspidea, Anaspidea and Notaspidea. Chitin can be considered to form a ‘skeleton’ of the organic matrix onto which intercrystalline carrier pro- teins are polymerized (Poulicek et al., 1986). An increase of the chitin content could thus thicken the wall between crystallites and thus provide some sup- pleness to the structure. An increased chitin content also occurs in other unre- lated species with internal reduced shells (Cephalopoda, Polyplacophora, Prosobranchia, Pulmonata) (Poulicek, 1982; Poulicek & Kreusch, 1986; Pou- licek et al., 1986). 3. Development of a peculiar helicoidal mi- crostructure in thecosomatous ptero- pods. The mechanical characteristics of these very light shells allow flexibility and reduce their brittleness. A similar microstructure has evolved in the unre- lated heteropods with similar light shells and similar mode of life (Batten & Du- mont, 1976). Thus the main features characteristic of the regressive evolution of opisthobranch shells can be considered to be adaptive and corre- lated with the need for suppleness in very thin, calcified shells that otherwise would be too brittle. These features are polyphyletic and convergent with shells of other molluscs showing similar reduction of the shell or the same mode of life. ACKNOWLEDGEMENTS The authors wish to express their thanks to Prof. M. Edmunds for correcting the English and critical reading of the manuscript. Most analyses were conducted with the technical assistance of Miss Claudine Toussaint. This work was supported by Research Grant no. 1.5.622.79 F and FRFC Grant no. 2.4506.83 of the National Fund for Scientific Research of Belgium (FNRS). LITERATURE CITED BANDEL, K., 1977, Die Herausbildung der Schraubenschicht der Pteropoden. Biomineral- ization Research Reports, 9: 73-85. BATTEN, R.L. & M.P. DUMONT, 1976, Shell ultra- structure of the Atlantidae (Heteropoda, Meso- gastropoda) Oxygyrus and Protatlanta, with com- ments on Atlanta inclinata. Bulletin of the 232 POULICEK, VOSS-FOUCART & JEUNIAUX American Museum of Natural History, 157: 263— 310. BE, A.W.H., C. MacCLINTOCK & D.C. CURRIE, 1972, Helical shell structure and growth of the pteropod Cuvierina columella (Rang) (Mollusca, Gastropoda). Biomineralization Research Re- ports, 4: 47-79. DEGENS, E.T. & D.W. SPENCER, 1966, Data file on aminoacid distribution in calcified and uncal- cified tissues of shell-forming organisms. Techni- cal Report of the Woods Hole Oceanographic In- stitution No.66, 27. 120 tables. 1-32 р. DEGENS, E.T., D.W. SPENCER & R.H. PARKER, 1967, Paleobiochemistry of molluscan shell pro- teins. Comparative Biochemistry and Physiology, 20: 553=579. DEVENYI, T., 1971, Single column procedure for the automatic analysis of aminoacids. Acta Bio- chimica Biophysica (Hungarian Academy of Sci- ences), 3: 429—432. FLORKIN, M., 1966, Aspects moléculaires de l'ad- aptation et de la phylogénie. Masson, Paris, 1— 258p. GHISELIN, M.T., 1966, Reproductive function and the phylogeny of opisthobranch gastropods. Ma- lacologia, 3: 327-378. GHISELIN, M.T., E.T. DEGENS, D.W. SPENCER & R.H. PARKER, 1967, A phylogenetic survey of molluscan shell matrix proteins. Breviora, 262: 1-35. GOFFINET, С. & С. JEUNIAUX, 1979, Distribution et importance quantitative de la chitine dans les coquilles de mollusques. Cahiers de Biologie Ma- rine, 20: 341-349. GREGOIRE, C., 1972, Structure of the molluscan shell. In: FLORKIN, M. & B. T. SCHEER, eds., Chemical Zoology, volume 7. Academic Press, New York & London, р. 45-102. JEUNIAUX, C., 1963, Chitine et chitinolyse, un chapitre de la biologie moléculaire. Masson, Paris, 1-183 р. JEUNIAUX, C., 1965, Chitine et phylogénie: appli- cation d'une méthode enzymatique de dosagede la chitine. Bulletin de la Société de Chimie Bi- ologique, 45: 2267-2278. MEENAKSHI, V.R., Р.Е. HARE, & K.M. WILBUR, 1971, Aminoacids of the organic matrix of neo- gastropod shells. Comparative Biochemistry and Physiology, 40B: 1037-1043. POULICEK, M., 1982, Coquilles et autres struc- tures squelettiques des mollusques—composi- tion chimique, biomasse et biodégradation en mi- lieu marin. Unpubl. PhD Thesis, University of Liege, 1-180 р. POULICEK, M. & B. KREUSCH, 1986, Evolution- ary trends in skeletal structures of Polyplacoph- ora. Proceedings of the VIIIth international mal- acological congress (Budapest, 1983), р. 207- 212. POULICEK, M. & M.F. VOSS-FOUCART, 1984, Approche fonctionnelle de l'évolution microstruc- turale des coquilles de mollusques. Annales de la Société Royale Zoologique de Belgique, 115: 89-90. POULICEK, M., M.F. VOSS-FOUCART & C. JEU- NIAUX, 1986, Chitinoproteic complexes and min- eralization in mollusk skeletal structures. In: MUZZARELLI, R. A. A., C. JEUNIAUX & G. GOODAY, eds., Chitin in Nature and Technology. Plenum, New York, p. 7-12. RAMPAL, J., 1973, Phylogenie des pteropodes thecosomes d’après la structure de la coquille et la morphologie du manteau. Comptes-renduc Hebdomadaires des Séances de l'Académie des Sciences de Paris, 277: 1345-1348. SAMATA, T., P. SANGUANSRI, C. CAZAUX, M. HAMM, J. ENGELS & G. KRAMPITZ, 1980, Bio- chemical studies on components of mollusc shells. In: OMORI, M. & N. WATABE, eds., The Mechanisms of Biomineralization in Animal and Plants. Tokai University Press, Tokyo, р. 37— 48. WEINER, S., H.A. LOWENSTAM, & L. HOOD, 1977, Discrete molecular weight components of the organic matrices of mollusk shells. Journal of Experimental Marine Biology and Ecology, 30: 45-51. YONGE, C.M. & T.E. THOMPSON, 1976, Living Marine Molluscs. Collins, London, 1-288 р. MALACOLOGIA, 1991, 32(2): 233-240 STUDY OF THE ANATOMY AND HISTOLOGY OF THE MANTLE DERMAL FORMATIONS (MDFs) OF CHROMODORIS AND HYPSELODORIS (OPISTHOBRANCHIA: CHROMODORIDIDAE) José С. Garcia-Gömez', Antonio Medina? & Rafael Covenas® ABSTRACT Mantle dermal formations (MDFs) were studied in 12 European species of Chromodoris and Hypselodoris. In Chromodoris the MDFs are small, numerous and irregular in shape, and are located in a band around the mantle edge. In Hypselodoris the MDFs are larger, less numerous and spherical. They are usually located in the anterior and posterior regions, although the anterior, or both anterior and posterior, MDFs may be absent in certain species. Therefore, the presence/ absence, location and shape of the MDFs may be of taxonomic importance to separate certain European species, in particular of the genus Hypselodoris. The main histological difference between the MDFs of Chromodoris and Hypselodoris is the presence of a thick, muscular capsule enveloping the MDFs in the latter genus: The strategic location and unpleasant taste of the MDFs suggest that they play a defensive role, but they do not appear to open externally. INTRODUCTION The loss of the shell in the Nudibranchia is compensated by the appearance of other de- fensive mechanisms which are frequently as- sociated with warning coloration. The family Chromodorididae includes many colourful species and, although recent works (see Dis- cussion) show that they possess substances of presumed defensive value, the almost uni- versal presence of dermal formations located in the mantle of the Chromodorididae has re- ceived scant attention. Only a few reports deal with such structures (Bergh, 1890; Marcus, 1955; Thompson, 1960, 1972; Edmunds, 1981; Rudman, 1984). The valuable paper of Rudman (1984) thoroughly describes the ‘mantle glands’ in chromodorid nudibranchs from the Indo-West-Pacific, although from an anatomical and taxonomic viewpoint. In the present paper we study the anatomy and his- tology of the mantle dermal formations (MDFs) of 12 European species of the nudibranch gen- era Chromodoris and Hypselodoris, and com- pare them with similar formations in other opisthobranchs. MATERIALS AND METHODS Most of the specimens studied were col- lected by SCUBA diving in waters of the Straits of Gibraltar. A few specimens were collected in the intertidal zone of Cadiz (Spain). For the anatomical examination of the MDFs the animals were frozen and subse- quently fixed and preserved in 4% formalde- hyde. For the histological study MDFs were re- moved from specimens of Chromodoris pur- purea, C. luteorosea, C. krohni, Hypselodoris elegans, H. tricolor and H. cantabrica. They were immediately fixed in 2.5% glutaralde- hyde in 0.1 M Millonig’s buffer (pH 7.3) for 3h, dehydrated through an ascending series of alcohols or acetones, and embedded in par- affin or Spurr’s resin (Spurr, 1969). After fix- ation in glutaraldehyde, some MDFs were postfixed in 1% osmium tetroxide. Semi-thin sections were cut on ап LKB Ш ultramicro- tome and stained with toluidine blue. Paraffin and semi-thin sections were sub- jected to histochemical tests for the demon- stration of neutral mucosubstances (Periodic Acid-Schiff, PAS), acid mucosubstances (Al- cian Blue at pH 2.5, AB) and proteins (Nin- hidrin-Schiff, NS) (Pearse, 1968). RESULTS Anatomy and location of MDFs in different species: A. Genus Chromodoris “Single submarginal row of ramifying man- tle glands opening dorsally” (in ‘diagnosis’ of the genus Chromodoris, Rudman, 1984). Laboratorio de Biologia, Marina, Facultad de Biología, Universidad de Sevilla; “Laboratorio de Biología, Facultad de Ciencias del Mar, Universidad de Cadiz; “Departamento de Biología Celular, Facultad de Biología, Universidad de Sala- manca. 234 GARCIA-GOMEZ, MEDINA & COVENAS In the European species of Chromodoris mantle dermal formations (MDFs) are present in all the specimens we have examined. They are distributed along the edge of the mantle, including the cephalic region in some species (Fig. 1A), whereas in others they are absent in front of the inter-rhinophoral plane (Fig. 1B). Their shape and size are quite variable, even in animals of the same species. When the mantle skin is torn with forceps at the level of the MDFs, numerous spherical structures (10-40 um in diameter) are released. These structures (as revealed by histological exam- ination) correspond to vacuolar cells. In some species, such as C. luteorosea, C. luteopunctata and C. britoi, the MDFs are densely packed, which results in an almost uniform distribution along the periphery of the mantle. In others, the MDFs are less dense and sometimes quite isolated (e.g. C. pur- purea, C. krohni). In these two species the young animals usually have fewer MDFs than the adults. The MDFs are opaque white, usually clearly visible because of the transparency of the mantle, and unlike the posterior MDFs in Hypselodoris, they hardly distort the edge of the mantle. C. luteorosea (Rapp, 1827) (5 specimens) The MDFs are located along the whole edge of the mantle, except in front of the rhi- nophores, forming blurred radial bands. Their vacuolar cells are 30-40 um in diameter. C. purpurea (Laurillard, 1831) (8 specimens) The MDFs are distributed all along the edge of the mantle. Even the smallest speci- mens (10-13 mm) show MDFs in front of the rhinophores . The MDFs are usually rounded and the vacuolar cells they contain are nor- mally spherical and quite uniform in size (20 um), though they are sometimes egg-shaped and measure 30-40 um. C. krohni (Vérany, 1846) (12 specimens) The edge of the mantle is densely packed with MDFs though in small specimens (6-7 mm) they may be absent in front of the rhino- phores. The MDFs are usually rounded and the vacuolar cells are very small and usually spherical (10-20 um). FIG. 1. Diagram to show the location of MDFs in A: Chromodoris purpurea and C. krohni; B: C. luteo- rosea, C. luteopunctata and C. britoi. C. luteopunctata (Gantes, 1962) (4 specimens) MDFs are present along the whole edge of the mantle, except in front of the rhinophores. They form dense white accumulations, which are usually long and irregular in shape. Vac- uolar cells, however, have not been distin- guished. C. britoi (Ortea & Pérez, 1983) (1 specimen) MDFs are found all along the edge of the mantle, except in front of the rhinophores. They are similar to those in С. /uteorosea, though the vacuolar cells, also spherical, measure 10-20 um. B. Genus Hypselodoris “The mantle glands are single and occur along the edge of the mantle opening at the edge. Posteriorly the glands are greatly en- larged and closely packed and on preserva- tion are partly extruded” (in ‘diagnosis’ of the genus Hypselodoris, Rudman, 1984). In the European Hypselodoris' the location of the MDFs varies depending on the species. They may be completely absent (Fig. 2E), present simultaneously at the rear of the man- tle and on both sides of the cephalic region (Figs. 2А-С), or confined to the extreme pos- terior region of the mantle (Fig. 2D). When anterior and posterior MDFs are present, the posterior MDFs are always larger. However, the smallest posterior MDFs may be similar in size to the largest anterior MDFs. As a general rule, the posterior MDFs increase in size towards the posterior end of ‘The ‘diagnosis’ of the mantle glands in Chromodoris and Hypselodoris by Rudman (1984) is based on species from the Indo-West Pacific. MANTLE DERMAL FORMATIONS OF CHROMODORIDS 235 A B D E FIG. 2. Diagram to show the location of MDFs in species of Hypselodoris. A: H. elegans; B: H. villafranca; С: H. bilineata; D: H. cf. tricolor; E: H. cf. messinensis. the mantle, causing a deformation of its ven- tral surface (Fig. 3). Although the MDFs are often close together and may appear to be partially fused, each one is a separate, dis- crete structure. The MDFs are opaque white in colour, and easily visible because of the transparency of the mantle. The number of MDFs located close to each rhinophore varies: for example a specimen of H. elegans, 60 mm in length, possessed four MDFs on the left and 12 on the right. The distribution is more balanced in the posterior MDFs. In young and adult ani- mals belonging to the same species a similar distribution of the MDFs has been observed, though the size and number of them tend to increase with the size of the animal. Occa- sionally, however, it has been observed that large specimens have fewer MDFs than smaller specimens of the same species. H. villafranca (Risso, 1818) (26 specimens) Anterior and posterior MDFs are present. In the smallest specimens observed (4—5 mm) there are one to four MDFs (50 um) close to each rhinophore, and four (250 jm) in the rear region of the mantle. In the largest spec- imens (15-25 mm) there are one to four MDFs (300 рт) on each side of the head and four to eight (700 tm) at the caudal end of the mantle (Fig. 2B). OR FIG. 3. Caudal region of Hypselodoris showing the position of the posterior MDFs (arrowheads). Note the large size of the posterior MDFs which causes deformation of the mantle edge. H. elegans (Cantraine, 1835) (8 specimens) Anterior and posterior MDFs are present. In the smallest specimens examined (60—65 mm) 2-12 MDFs (450 um) are found close to each rhinophore, and 7-24 (1300 um) in the rear region (Fig. 2A). In the largest specimens (110—130 mm) there are 15-18 MDFs (1000 um) close to each rhinophore, and 14-20 (2000 um) in the rear region. 236 GARCIA-GOMEZ, MEDINA & COVENAS H. cf. tricolor (Cantraine, 1835)° (8 specimens) Only posterior MDFs are present. In the smallest specimens (10 mm) there are two MDFs (500 um), and in the largest ones (14— 20 mm) 4 (900 um) (Fig. 2D). H. coelestis (Deshayes, 1866) (34 specimens) Only posterior MDFs are found. In the small- est specimens (8—9 mm) 1-5 MDF s (400 um) are present, while in the largest specimens (13-17 mm) there are 2-5 (500 um). H. cf. messinensis (lhering, 1880) (7 specimens) There are no MDFs (Fig. 2E). H. bilineata (Pruvot-Fol, 1953) (12 specimens) In the smallest specimens (5-10 mm) there are no anterior MDFs but two to four (180 рт) are present posteriorly. In the largest speci- mens (13-20 mm) two or three MDFs (200 um) are present close to each rhinophore, and four or five (450 рт) in the rear region (Fig. 2C). H. cantabrica (Bouchet & Ortea, 1980) (5 specimens) Anterior and posterior MDFs are present. In the smallest specimens (13-25 mm) there are one to three MDFs (300 рт) close to each rhinophore, and three to six (1900 pm) in the rear region. In the largest specimens (40-45 mm) three or four MDFs (600 рт) are located close to each rhinophore, and seven (1400 рт) posteriorly. Histology of the MDFs A. Genus Chromodoris For the histological examination of the MDFs in Chromodoris, three species have been examined: C. purpurea, C. krohni and C. luteorosea. The present description is valid for all these species. The MDFs in Chromodoris are small and irregular structures which are embedded in the subepidermal connective tissue. They consist of an outer cell layer enclosing an in- ner accumulation of vacuolar cells (Fig. 4A). The cytoplasm of the cells in the outer layer appears to contain neutral mucosubstances, since it is strongly stained by the PAS proce- dure. Curiously, cells with the same histolog- ical and histochemical features are present in the epidermis. A thorough microscopic exam- ination of the MDFs shows that their outer layer is continuous and hence they do not ap- pear to discharge into the external medium. Consequently, the term ‘gland’, which has so far been applied to these formations, could lead to an erroneous interpretation of their functioning, since this terminology suggests an active secretion of substances. The vacuolar cells show a peripheral cyto- plasmic ring surrounding a big central vacuole which occupies nearly the whole cell volume. The nucleus is displaced towards the periph- ery of the cell. The content of the central vac- uole is weakly stained by toluidine blue when the tissue is post-fixed with osmium tetroxide. The histochemical tests used for the demon- stration of neutral (PAS) and acid (AB) muco- substances, and proteins (NS) gave negative results in the vacuolar cells. On occasions, the cellular organization in the centre of the largest MDFs is lost (Fig. 4A). When the tissue is post-fixed in osmium tetroxide, the central area is weakly stained, so it seems likely that it is filled with sub- stances from the surrounding vacuolar cells. In the subepidermal connective tissue and between epidermal cells of the mantle of Chromodoris, free vacuolar cells, some of which appear to open onto the dorsal surface of the mantle, are present (Fig. 4B). B. Genus Hypselodoris The histology of the MDFs has been stud- ied in three species of Hypselodoris: H. ele- gans, H. cantabrica and H. tricolor. Since the histology of the MDFs in all these species is similar, we shall describe in detail the obser- vations made on H. elegans, and then draw attention to significant differences in the other two species. The MDFs in H. elegans are spherical structures consisting of a thick outer capsule which completely surrounds an accumulation of vacuolar cells (Fig. 4C). The capsule is mainly formed by muscle fibres (Fig. 4D) which, as shown by tangential sections, are oriented in all directions. In H. cantabrica and 2The identification of these three species will be discussed in a paper currently in preparation by Ortea, Bouchet and Garcia-Gömez. It will show that H. coelestis is a distinct species, and that the other two are hitherto undescribed species which resemble H. tricolor and H. messinensis. MANTLE DERMAL FORMATIONS OF CHROMODORIDS 237 г Nas # МА. € FIG. 4.A: Semi-thin section of MDFs of Chromodoris purpurea fixed in glutaraldehyde and stained with toluidine blue. Note the vacuolar cells (VC), the surrounding single cell layer (arrowed), and the central area lacking vacuolar cells (asterisk). x190. B: Section of MDFs and mantle epidermis of C. purpurea. Note connective tissue (CT), and vacuolar cells in epidermis (arrowheads), one of which opens onto the dorsal surface of the mantle (double arrowhead). Fixation and staining as for 1a (above). x480. C: Semi-thin section of a MDF of Hypselodoris elegans fixed in gluteraldehyde, post-fixed in osmium tetroxide, and stained with toluidine blue. VC, vacuolar cells; M, muscular capsule; arrowheads, granular cells. x75. D: Portion of MDF of H. elegans fixed and stained as for 1C (above). Note vacuolar cells (VC) with contents weakly stained by toluidine blue. M, muscular capsule; SL, surrounding cell layer; arrow, granular cell. x480. 238 GARCIA-GOMEZ, MEDINA & COVENAS H. cf. tricolor the capsule is identical in struc- ture, but thinner. Beneath the capsule there is a continuous cell layer (Fig. 4C,D) which ap- pears to be equivalent to the cell layer sur- rounding the vacuolar cells in Chromodoris. In this layer some nuclei are seen, but no defi- nite intercellular limits can be distinguished. The vacuolar cells are similar to those de- scribed in Chromodoris, but they are more closely packed. These cells are always clearly identifiable, even in the centre of the largest MDFs. In H. elegans and H. tricolor some cells containing dense cytoplasmic granules (Fig. 4C,D) are located between the vacuolar cells. This type of cell is not present in H. cantabrica nor in the genus Chromo- doris. In all the species of Hypselodoris studied, free vacuolar cells are located in the subepi- dermal connective tissue and in the epider- mis. DISCUSSION The loss of the shell in opisthobranchs rep- resents an important defensive disadvantage which must be compensated by the acqui- sition of other methods of defense. In the shell-less opisthobranchs numerous protec- tive mechanisms have evolved (Edmunds, 1966a,b) which vary from defensive behav- iour to the presence of protective structures, such as glands or spicules, in the skin. Many pleurobranchids and dorids secrete acid substances (pH 1 or 2) of possible de- fensive function when they are molested (Ed- munds, 1968; Thompson, 1969,1983; Mar- bach & Tsurnamal, 1973). The release of these substances has been attributed to epi- dermal glandular cells (called ‘acid’ or ‘clear’ cells) and subepidermal multicellular glands. The epidermal glandular cells are prismatic and show a clear polarity: their nucleus occu- pies the basal region of the cell and the apical portion is vacuolar (Thompson, 1969). In con- trast, the vacuolar cells of the multicellular glands do not show such a polarity, their shape is more spherical and most of their cy- toplasm appears clear (Edmunds, 1968). The multicellular glands of Berthellina (Thompson & Colman, 1984), Discodoris (referred as An- isodoris by Edmunds) stellifera, D. pusae and D. tema (Edmunds, 1968) are similar to the MDFs of Hypselodoris in that they are formed by an accumulation of vacuolar cells envel- oped by a muscular sheath, but both types of structures differ in that the multicellular glands are scattered all over the mantle, possess a central lumen and open onto the dorsal sur- face of the mantle. When some Hypselodoris (e.g. H. vil- lafranca and H. cf. messinensis) are mo- lested, the release of an opaque substance from the mantle can be observed. This sub- stance is probably mixed with mucus and thus remains around the body of the animal. This phenomenon was previously suggested to occur in dorids by Potts (1981). The unpleas- ant taste and neutral pH of the substance se- creted are similar to those of the MDFs, so that it is reasonable to suppose that the con- tent of the MDFs and the substance released from the mantle are similar in chemical com- position. The distasteful substance is proba- bly responsible for the fact that predatory fish (e.g. some species of Blennius) and opistho- branchs (e.g. Pleurobranchaea теске!) re- ject Hypselodoris as food, while other nudi- branchs left in the same aquarium are immediately devoured (pers. obs.). Since the MDFs are internal structures and do not open on the surface, they do not appear to be in- volved in the discharge of the repulsive sub- stance. However, inserted between epider- mal cells of Chromodoris and Hypselodoris are free vacuolar cells. This cell type could thus be responsible for the secretion of the repulsive substance. Ros (1977) points out that Chromodoris and Hypselodoris do not release acid sub- stances, but he assumes that they must pro- duce repulsive secretions. In this connection, recent work has shown the presence in these genera of substances which could be ob- tained from the diet and utilized as chemical defence against potential predators (Hoch- lowski & Faulkner, 1981; Hochlowski et al. 1982; Faulkner & Ghiselin, 1983; Faulkner, 1984; Okuda & Scheuer, 1985). These stud- ies have not demonstrated the precise loca- tion of these substances, so we cannot defi- nitely conclude that they are present in the MDFs. The strategic location of the MDFs in the cephalic and caudal regions of many Hypselodoris species, as well as their un- pleasant taste, suggest that they may play a defensive role. Such formations could thus protect the most important external organs (head, rhinophores and gills) from attack by other animals. Although the MDFs of Chro- modoris are apparently different from those of Hypselodoris, the study of both under the mi- MANTLE DERMAL FORMATIONS OF CHROMODORIDS 239 croscope shows that their cells share similar histological features. This does not prove that the MDFs perform the same function in both genera, but the phylogenetic proximity of these genera suggests a similar function for the MDFs. In Chromodoris and Hypselodoris the pre- sumed defensive region (the edge of the mantle) is associated with a striking coloured band which contrasts with the general colour of the body. This peripheral band is yellow in the adult of all the species, except H. coeles- tis in which it is white. The band is also white in the young specimens of C. krohni and some Hypselodoris. The observations noted above (i.e. the re- lease of repulsive substances by some Hyp- selodoris; the distastefulness of the content of the MDFs and their strategic location; the contrasting coloration associated with the MDFs; the presence of metabolites in numer- ous Chromodoris and Hypselodoris species which, according to several authors may act as deterrent substances) lead us to think that, as suggested by Ros (1976)°, in the Euro- pean species of Chromodoris and Hypselo- doris aposematic circles, corresponding to a Müllerian mimicry, occur. The ‘diagnosis’ of the mantle glands (= MDFs) of Chromodoris and Hypselodoris given by Rudman (1984) is based on species from the Indo-West Pacific. Our observations on European species of these genera provide additional data which may be used in taxon- omy. Thus, in Hypselodoris the MDFs may be extruded through the ventral surface of the mantle as the animal dies (1); they may be present simultaneously on both sides of the cephalic region and in the posterior region of the mantle (2), only in the posterior region of the mantle (3), or completely absent (4). Rud- man (1984) also reported that “mantle glands appear to be absent around the anterior end”, which concurs with our own observations. The MDFs of Chromodoris and Hypselo- doris are isolated and do not open onto the surface of the mantle. However, in some pre- served specimens of both genera whole MDFs appear to be extruded through orifices formed in the skin of the mantle. Rudman (1984) made the same observation on pre- served specimens of Chromodoris and Hypselodoris. Unfortunately, in very few specimens were we able to investigate the possible extrusion of MDFs in living animals, and in no case did we find this phenomenon to occur. Furthermore, the MDFs were not ex- truded when specimens of some Hypselo- doris (e.g. H. gracilis, H. bilineata and H. ele- gans) were prodded. The extrusion occurs only when the MDFs themselves are pressed, which also justifies the hypothesis that they could be defensive structures. In Hypselo- doris extrusion was most often observed in the largest MDFs. The MDFs might therefore be storage vessels which would slowly accu- mulate material and then extrude it when they were full. This explanation of their activity would imply an excretory rather than a defen- sive function. Recently, Rudman (1984) discussed the phylogeny of the different genera of Chromo- dorididae by taking into consideration the dis- tribution of the MDFs. The observations of Rudman and ourselves show that in Hypselo- doris the MDFs may be completely absent (H. cf. messinensis), or located along the entire edge of the mantle (H. bennetti), with a range of intermediate situations present in other species. Following Rudman's hypothesis (1984), H. cf. messinensis would represent the final stage in the evolutionary loss of MDFs in the European species of Hypselo- doris. ACKNOWLEDGEMENTS We thank Prof. M. Edmunds for the helpful critical reading of the manuscript. LITERATURE CITED BERGH, R., 1980, Reports on the results of dredg- ing... . in the Gulf of Mexico (1877-78) and in the Caribbean Sea (1879-80), by the U.S. Coast Survey Steamer “Blake”... . XXXII. Report on the nudibranchs. Bulletin of the Museum of Com- parative Zoology, Harvard, 19: 155-181. EDMUNDS, M., 1966a, Protective mechanisms in the Eolidacea (Mollusca Nudibranchia). Zoologi- cal Journal of the Linnaean Society, 46: 27—71. EDMUNDS, M., 1966b, Defensive adaptations of Stiliger vanellus Marcus, with a discussion on the evolution of nudibranch molluscs. Proceedings of the Malacological Society of London, 37: 73— 81. Ros (1976,1977) referred to species of both Chromodoris and Hypselodoris under the generic name Glossodoris. 240 GARCIA-GOMEZ, MEDINA & COVENAS EDMUNDS, M., 1968, Acid secretion in some spe- cies of Doridacea (Mollusca, Nudibranchia). Pro- ceedings of the Malacological Society of London, 38: 121-133. EDMUNDS, M., 1981, Opisthobranchiate Mollusca from Ghana: Chromodorididae. Zoological Jour- nal of the Linnaean Society, 72: 175-201. FAULKNER, D.J., 1984, Marine natural products— metabolites of marine invertebrates. Natural Products Research, 1: 551-598. FAULKNER, 0... & M.T. GHISELIN, 1983, Chem- ical defense and evolutionary ecology of dorid nudibranchs and some other opisthobranch gas- tropods. Marine Ecology Progress Series, 13: 295—301. HOCHLOWSKI, J.E. & 0... FAULKNER, 1981, Chemical constituents of the nudibranch Chro- modoris marislae. Tetrahedron Letters, 22: 271— 274. HOCHLOWSKI, J.E., В.Р. WALKER, С. IRELAND & D.J. FAULKNER, 1982, Metabolites of four nudibranchs of the genus Hypselodoris. Journal of Organic Chemistry, 47: 88-91. MARBACH, A. & M. TSURNAMAL, 1973, On the biology of Berthellina citrina (Gastropoda: Opisthobranchia) and its defensive acid secre- tion. Marine Biology, Berlin, 21: 331-339. MARCUS, E., 1955, Opisthobranchia from Brazil. Boletim da Faculdade de Filosofia, Ciencias e Letras da Universidade de Sao Paulo, Zoologia, 20: 89-261. OKUDA, В.К. & P.J. SCHEUER, 1985, Latrunculin- A, ichthyotoxic constituent of the nudibranch Chromodoris elisabethina. Experientia, 41: 1355-— 1356. PEARSE, A.G.E., 1968, Histochemistry: Theoreti- cal and Applied, volume 1. 3rd edn. Churchill, Edinburgh, 1—759 p. POTTS, G.W., 1981, The anatomy of respiratory structures in the dorid nudibranchs, Onchidoris bilamellata and Archidoris pseudoargus, with de- tails of the epidermal glands. Journal of the Ma- rine Biological Association, U.K., 61: 959-982. ROS, J., 1976, Sistemas de defensa de los opisto- branquios. Oecologia Aquatica, 2: 41-77. ROS, J., 1977, La defensa en los opistobranquios. Investigacion y Ciencia, 12: 48—60. RUDMAN, W.B., 1984, The Chromodorididae (Opisthobranchia: Mollusca) of the Indo-West Pacific: a review of the genera. Zoological Jour- nal of the Linnaean Society, 81: 115-273. SPURR, A.R., 1969, A low-viscosity epoxy resin embedding medium for electron microscopy. Journal of Ultrastructure Research, 26: 31—43. THOMPSON, T.E., 1960, Defensive adaptations in opisthobranchs. Journal of the Marine Biological Association, U.K., 39: 123-134. THOMPSON, T.E., 1969, Acid secretion in Pacific Ocean gastropods. Australian Journal of Zool- ogy, 17: 755-764. THOMPSON, T.E., 1972, Chromodorid nudi- branchs from eastern Australia (Gastropoda, Opisthobranchia). Journal of Zoology, London, 166: 391—409. THOMPSON, T.E., 1983, Detection of epithelial acid secretions in marine molluscs: review of techniques and new analytical methods. Com- parative Biochemistry and Physiology, 74 (A): 615-621. THOMPSON, T.E. & J.G. COLMAN, 1984, Histol- ogy of acid glands in Pleurobranchomorpha. Journal of Molluscan Studies, 50: 65-67. MALACOLOGIA, 1991, 32(2): 241-255 DOES WARNING COLORATION OCCUR IN NUDIBRANCHS? Malcolm Edmunds Department of Applied Biology, Lancashire Polytechnic, Corporation Street, Preston, Lancs PR1 2TQ, UK ABSTRACT Direct evidence for the occurrence of aposematic (warning) coloration in nudibranch molluscs is reviewed and is shown to be inconclusive. Many species are conspicuously coloured and are distasteful to possible predators, but there is very little evidence that they are avoided by predators because of their colours or that these colours give better protection than would cryptic colours. Indirect evidence for aposematism can be obtained by assuming that it occurs, pre- dicting the consequences of this assumption, and then testing these predictions. Information to test most of these predictions is either not available or is inconclusive, but the strongest support for aposematism is the widespread occurrence of Batesian and/or Mullerian mimicry. It is con- cluded that warning coloration does occur in nudibranchs but that there is much scope for further experimental studies. INTRODUCTION The occurrence of warning coloration in in- sects is well established (Cott, 1940), but the possibility of its occurrence in opisthobranch molluscs is more controversial (Thompson, 1960; Harris, 1973; Edmunds, 1974; Todd, 1981). Nearly one hundred years ago Wal- lace (1889), Garstang (1889, 1890), Herdman (1890) and Herdman & Clubb (1890) sug- gested that many nudibranchs have warning colours, and further possible examples of warningly coloured species are given by Hecht (1896), Crossland (1911) and by numerous more recent authors (e.g. Harris, 1973). Warning coloration was first given a scientific (Greek) name by Poulton (1890) who defined aposematic coloration as: “... an appearance which warns off enemies because it denotes something unpleasant or dangerous; or which directs the attention of an enemy to some specially defended, or merely non-vital part; or which warns off other individuals of the same species.” The last two parts of this definition make the concept of aposematic coloration very wide and today most authors restrict it to the first clause. Edmunds (1974), for example, gives the following definition: “Animals which have dangerous or unpleasant attributes, and which advertise this fact by means of charac- teristic structures, colours or other signals so that some predators avoid attacking them, are said to be aposematic, and the phenomenon is called aposematism.” Despite the fact that 241 it is nearly a hundred years since it was sug- gested that nudibranchs have warning co- lours, there is still considerable uncertainty as to whether any nudibranchs are really apose- matic. This is due to lack of evidence. This paper reviews the current state of knowledge, and suggests the type of evidence that needs to be sought in order to establish if a nudi- branch is aposematic. Criteria Necessary for Aposematism If the definition given above is accepted then in order to demonstrate that a particular species is aposematic it is necessary to es- tablish that it fulfils four criteria (Edmunds, 1987): 1. it is sufficiently noxious that some pred- ators will not eat it; it is conspicuously coloured, or adver- tises itself by means of some other sig- nals; some predators avoid attacking it be- cause of its signals; these conspicuous signals provide bet- ter protection to the individual or to its genes than would other (e.g. cryptic) signals. 2. Only if all these criteria are met will there be selective advantage to an animal in possess- ing warning colours (Edmunds, 1987). If cri- terion 4 is not met then an animal would be better protected if it were cryptic and apose- 242 EDMUNDS matic colours could not evolve. Do any nudi- branchs fulfil these four criteria? Criterion 1: Are any nudibranchs sufficiently noxious that predators will not eat them? Many nudibranchs have noxious dermal and epidermal glandular secretions and ae- olids retain nematocysts from their food and store them in their cerata; both have a defen- sive function (Thompson, 1960; Edmunds, 1966). Herdman & Clubb (1890), Crossland (1911), Crozier (1916) and Thompson (1960) have all established that some brightly co- loured nudibranchs are unpalatable to fish. The animals were usually dropped into an aquarium or into the sea and were immedi- ately attacked by fish as they fell through the water column. Almost all the nudibranchs sur- vived although they were snapped up and spat out several times before reaching the substrate after which the fish ignored them. Herdman & Clubb (1890) and Thompson (1960) also showed that many cryptically co- loured nudibranchs were unpalatable to fish. Harris (1973) obtained similar results with Phestilla melanobranchia Bergh, but he found that Р. sibogae Bergh (= P. lugubris Bergh) was usually eaten as it fell through the water. This was because repeated ingestion and spitting out by fish caused it to autotomize all of its cerata so that the “naked” nudibranch was eventually palatable. These simple ex- periments clearly show that many nudi- branchs are unpalatable to some species of predatory fish. Criterion 2: Are any nudibranchs conspicuously coloured? It has been suggested that the following nudibranchs may have warning colours: Limacia clavigera (Müller), Polycera quadrilin- eata (Muller), Facelina coronata (Forbes & Goodsir) and Eubranchus tricolor Forbes from Europe (Hecht, 1896); Chromodoris re- ticulata (Pease), С. diardii (Kelaart) and Phyl- lidia varicosa Lamarck from the Indo-Pacific (Crossland, 1911; Harris, 1973); and Triopha carpenteri Stearns and Diaulula sandiegensis (Cooper) from the north-west Pacific (Harris, 1973). These are all brightly coloured and so fulfil criterion 2. Perusal of recent mono- graphs with colour illustrations of nudibranchs (Behrens, 1980; Bertsch & Johnson, 1981; Schmekel & Portmann, 1982; Thompson & Brown, 1984; Willan & Coleman, 1984; Just & Edmunds, 1985) indicates that a very large number of nudibranchs are brightly coloured and conspicuous on unnatural backgrounds. Garstang (1890), Hecht (1896) and Thomp- son (1960), however, have all pointed out that some brightly coloured species are actually cryptic in their natural environment. For ex- ample Rostanga pulchra McFarland is red but usually lives close to the red sponge Ophlita- spongia pennata Lambe (Cook, 1962) while Catriona gymnota (Couthouy) is also red but lives almost exclusively on the red hydroid Tu- bularia spp. (Edmunds, 1987). It is also well Known that as light penetrates the sea the red end of the spectrum is ab- sorbed much more quickly than the blue (Hardy, 1956). In consequence many animals that are red actually appear black or brown at the depths they normally inhabit. Dr H. Bertsch (pers. comm.) informs me that Chro- modoris petechialis (Gould) and Hexabran- chus sanguineus Ruppell & Leuckart appear brown and cryptic at 18 m depth. But why should these species be red rather than brown or black, since if they were to move into well-lit, shallower waters they could be very conspicuous? The answer to this question may be that it is economically cheaper to evolve red pigment, because red carotenoids are easily sequestered from the animal's food, whereas browns and blacks may have to be synthesized de novo. Criterion 3: Do any predators avoid attacking nudibranchs because of their colour (or because of some other signal)? There is evidence that some fish and some cephalopods can learn to avoid prey that pro- vide aversive stimuli yet still attack other pal- atable prey which are of different appearance (i.e. have different signals) (Summarized in Edmunds, 1974), but only very preliminary experiments along these lines have been car- ried out with nudibranchs as prey. These showed that grey mullet (Mugil labrosus) quickly learned to avoid the red aeolid Coryphella pellucida (Alder & Hancock). They also learned to avoid a papillate model cou- pled with an aversive stimulus while continu- ing to attack a similar but non-papillate model coupled with food (Edmunds, 1974). Criterion 4: Do conspicuous colours provide better protection than cryptic colours? Guilford (1990) has recently reviewed the possible ways in which warning colours work. For example, they may be more memor- WARNING COLORATION IN NUDIBRANCHS 243 able than cryptic colours because they are conspicuous or because they are unfamiliar; they may increase the rate of capture and hence of aversive learning; they may reduce recognition errors in experienced predators; or they may provide frequent reminders of a noxious experience. Gittleman & Harvey (1980) showed that chicks learn more readily to avoid noxious crumbs if these are conspic- uous than if they are cryptic, and similar ex- periments have been carried out by Schuler & Hesse (1985), Sillen-Tullberg (1985) and oth- ers (see Guilford, 1990). No comparable ex- periments have been undertaken using fish or other marine animals as predators. However, if some nudibranchs are aposematic to cer- tain species of fish, then a knowledge of the behaviour of these fish is crucial to our un- derstanding of how the aposematism has evolved. Since different species of predators may respond differently to aposematic prey, the evolution of aposematic nudibranchs may have followed several routes. The direct evidence for aposematism in nudibranchs is thus not conclusive. There is evidence that some nudibranchs fulfil criteria 1 and 2, although further field observations are also required. Much more experimental work needs to be undertaken to see if criteria 3 and 4, which relate to the behaviour of the predator, are applicable. However, it is also possible to look for indirect evidence for aposematism in nudibranchs. Indirect Evidence for Aposematism The indirect evidence for aposematism in nudibranchs is obtained by assuming that it does occur, predicting the consequences of this assumption and then testing these pre- dictions. 1. Evolution of especially noxious qualities and of ability to survive attacks Because of its bright colours an aposematic animal is more likely to be found and attacked than is a cryptic animal, and so there will be stronger selection pressure on it favouring more effective noxious qualities and greater resilience to attack. For monarch butterflies (Danaus plexippus) this has led to sequester- ing cardenolides from their food which are emetic to their avian predators, and emesis is a particularly effective way of negatively con- ditioning a bird (Brower et al., 1968, 1970). For nudibranchs | know of no evidence that the defences of aposematic species are any more effective than those of cryptic ones. Many nudibranchs are resilient to attack with autotomizable papillae and good powers of regeneration, but again | know of no evidence that this resilience is more pronounced in brightly coloured species. 2. Evolution of Batesian and Müllerian mimicry Aposematic animals may suffer injury or death while predators learn their colour pat- tern, so selection will favour individuals of dif- ferent species having the same pattern. Pred- ators need then learn only one pattern for individuals of both species to be protected, and the chances of any one animal being killed will be reduced. This is Mullerian mim- icry. Selection will also favour the evolution of Batesian mimicry, that is of animals with the same colour pattern as the aposematic model, but which are palatable to those pred- ators which avoid the model. Mimicry is common among nudibranchs; Ros (1976, 1977) lists five mimetic groups from the Mediterranean, including blue and gold chromodorids and orange and white nudibranchs. There are groups of blue and gold chromodorids from the Pacific coast of North America (Bertsch, 1978a,b,c), and nu- merous colour groups of chromodorids have been described from the Indo-Pacific by Rud- man (Summarized by Edmunds, 1987). Each mimicry group comprises species belonging to more than one genus, so similarity of colour is not due simply to recent speciation. Some of these mimicry groups are listed in Table 1. Not all mimetic species of a single group oc- cur in any one habitat, for example on the reef off Tema, Ghana, only Mexichromis tricolor and Hypselodoris bilineata have been found (Edmunds, 1981). The occurrence of mimicry in these species is almost impossible to ex- plain unless some of them are aposematic. It is not Known which species in each group are Müllerian and which are Batesian because no experiments involving naturally occurring predators have been carried out, but all of the relevant nudibranchs appear to have glandu- lar or nematocyst defences which could make them unpalatable. Most are therefore proba- bly Müllerian mimics though some could be Batesian, at least towards some predators (Edmunds, 1987). There are, however, some problems. Eubranchus farrani (Alder & Han- cock) is typically orange and white, conspic- 244 EDMUNDS TABLE 1. Presumed mimetic groups of nudi- branchs Blue and gold group from Mediterranean and east Atlantic (Ros, 1977; Edmunds, 1987) Chromodoris krohni (Verany) Hypselodoris bilineata (Pruvot-Fol) Hypselodoris cantabrica (Bouchet 8 Ortea) Hypselodoris messinensis (lhering) Hypselodoris tema (Edmunds) Hypselodoris valenciennesi (Cantraine) Hypselodoris villafranca (Risso) Hypselodoris webbi (Orbigny) Mexichromis tricolor (Cantraine) Orange and white group from Mediterranean and northern Europe (Ros, 1977; Edmunds, 1987) Ancula gibbosa Risso Chromodoris elegantula Philippi Crimora papillata Alder & Hancock Diaphorodoris papillata Portmann & Sandmeier Eubranchus farrani (Alder & Hancock) Limacia clavigera (Muller) Polycera faeroensis Lemche Polycera quadrilineata (Muller) Trapania maculata Haefelfinger Blue chromodorids from western America (Bertsch, 1978a,b,c) Chromodoris mcfarlandi Cockerell Hypselodoris agassizii (Bergh) Hypselodoris californiensis (Bergh) Hypselodoris ghiselini Bertsch Hypselodoris lapislazuli (Bertsch & Ferreira) Mexichromis antonii (Bertsch) Mexichromis porterae (Cockerell) Mexichromis tura (Marcus & Marcus) White chromodorids with gold border from Indo-Pacific (Rudman, 1985) Ardeadoris egretta Rudman Cadlina nigrobranchiata Rudman Cadlina willani Miller Chromodoris aureomarginata Cheeseman Glossodoris averni Rudman Glossodoris pallida (Ruppell & Leuckart) Glossodoris undaurum Rudman Hypselodoris kulomba (Burn) Noumea nivalis Baba Noumea sudanica Rudman Thorunna africana Rudman Thorunna furtiva Bergh uous, and so presumably aposematic, but some populations are polymorphic (Edmunds & Kress, 1969). Polymorphism has clear ad- vantages for cryptic animals, but it is difficult to see any advantage for an aposematic spe- cies (Edmunds, 1974, 1987). 3. Evolution of kin selection The individuals who gain from aposema- tism can be the ones attacked by the potential predator or they can be other individuals in the vicinity. Where an aposematic animal is always killed during the educational experi- ence of the predator, the animals that benefit from the aposematism must share genes with the individual sacrificed: this is kin selection. It applies to social Hymenoptera and other gre- garious species which live in family groups or in colonies of related individuals. By contrast, where the aposematic animal survives the ex- perience of sampling by a predator, the se- lective advantage is gained by this individual (individual selection), and there is no neces- sary requirement that it should be gregarious. The question of whether aposematism can only evolve through kin selection or whether it can also evolve through individual selection has generated a series of papers in recent years (e.g. Harvey & Paxton, 1981a, b; Harvey et al., 1982; Jarvi et al., 1981; Sillen- Tullberg & Bryant, 1983; review in Guilford, 1990). In nudibranchs the defensive glands and nematocysts are superficial, some ani- mals have survived being taken into the mouth and spat out by fish, and most species have planktonic larvae so that the probability that two individuals that happen to settle on the same substrate are genetically related is slight. Aposematism is therefore most likely to have evolved because of the selective advan- tage it gives to the aposematic individuals themselves rather than to their kin. Neverthe- less, assuming the same level of predator sampling, kin selection clearly gives greater protection to an individual’s genes in terms of inclusive fitness (Hamilton, 1984) than indi- vidual selection, so we might predict the ex- istence of kin selection in aposematic nudi- branchs. Is there any evidence of kin selection in aposematic nudibranchs? Kin selection can only occur in aposematic animals if they live in groups of related individuals. In nudi- branchs it can only occur in species lacking planktonic larvae because this will enable the young grow up close to the parent. A cryp- tic animal, on the other hand, is more likely to benefit by having a planktonic larva to ensure wide dispersal so that predators will be less likely to acquire a searching image for its pat- WARNING COLORATION IN NUDIBRANCHS 245 tern. | therefore predict a higher incidence of non-planktonic development in presumed aposematic than in cryptic nudibranchs. It should be possible to test this prediction since the developmental pattern of more than 150 species of nudibranch is known. Table 2 summarizes the results, but there are prob- lems with this analysis. First, developmental type has adaptive significance in terms of a species’ life cycle and ecological habit (Todd, 1983) which may be of much greater impor- tance than its possible consequences relating to kin selection. Thus the development of two species of arminid is known, but since most of their life is probably spent burrowing it is un- likely that developmental mode is related to colouration. The same argument can be ap- plied to the burrowing aeolid Cerberilla and to intersitial acochlidiaceans. These species have been omitted from Table 2. Second, while planktotrophic larvae clearly have planktonic development and direct de- veloping eggs have non-planktonic develop- ment, lecithotrophic larvae include some with planktonic and others with non-planktonic de- velopment. It is possible that for some leci- thotrophic species the planktonic stage is obligatory while for others it is facultative so that the larvae usually settle close to the egg ribbon. Such information is rarely published because it is trivial in terms of the develop- ment although of crucial importance to the possible occurrence of kin selection. In Tenel- lia fuscata (Gould) the veliger stage may never leave the egg or it may swim for up to a day (Harris et al., 1980). In Cuthona nana (Alder & Hancock) and Tenellia adspersa (Nordmann) (= T. pallida (Alder & Hancock)) the occurrence of planktonic or non- planktonic larvae varies with population or with environmental conditions (Harris et al., 1975; Rivest, 1976; Roginskaya, 1970; Ey- ster, 1979). These three species have also been omitted from the analysis. Two other species reported by one worker to have planktonic larvae and by another to have non-planktonic development are Doriopsilla miniata (Alder & Hancock) and Cuthona pus- tulata (Alder & Hancock) (Shyamasundari & Najbuddin, 1976; Thompson, 1975; Rogin- skaya, 1962; Gosliner & Millen, 1984). These conflicting reports may be explained by vari- ation in developmental mode, or they may im- ply that the different workers were actually studying different species. These two species have also been omitted from Table 2, but sim- ilar plasticity of developmental mode may oc- cur in some of the other species included in this table. Moridilla brockii Bergh and Favori- nus argentimaculatus Rao have also been omitted from the table because although they have veliger larvae, these metamorphose a few hours after liberation (K.P. Rao, 1965; K.V. Rao, 1970); thus it is not clear if the de- velopmental mode is effectively planktonic or non-plankton. Finally, while the colour of these animals is known, it is not always easy to decide whether they are cryptic or aposematic. In this table | have assumed that all chromodorids are aposematic while most other doridaceans are cryptic. The decision is even more difficult for some aeolids: red Coryphella and Flabel- lina spp. could be cryptic on Tubularia or in deep water, or they could be conspicuous and aposematic; and Aeolidiella and Spurilla spp. could be cryptic or mimetic among sea anem- ones or they could be conspicuous and aposematic. | have left these species with a ‘?’ in Table 2. What conclusions can be drawn from Table 2? In the dorids (including chromodorids) there are 45 cryptic and 22 conspicuous spe- cies with planktonic development compared with 8 and 7 with non-planktonic develop- ment. These figures are not significant (x? =0.51). However, if the chromodorids are all considered to be conspicuous and are compared with the other doridaceans (most of which are cryptic), we get the following: 53 dorids and 14 chromodorids have planktonic development compared with 8 and 7 with non-planktonic development. This gives a x =3.03 which is still not significant, but is close to the 5% level. For aeolids 41 cryptic and 9 aposematic species have planktonic development compared with 4 cryptic and 0 aposematic species without planktonic devel- opment. This difference is obviously not sig- nificant . Whether we assume that the species whose colour is entered with a ‘?’ are cryptic or conspicuous makes little difference: the fig- ures are still not significantly different. There is therefore no evidence from a study of de- velopmental mode that kin selection occurs in nudibranchs. Kin selection should also favour apose- matic species with non-planktonic develop- ment living longer post-reproductively than cryptic species. If a predator learns the colour pattern by killing a senile animal, this will re- duce the chances of that individual’s offspring or siblings being taken by a predator, and this will increase the chances of the individual's 246 TABLE 2. Type of development and colour of nudibranchs. Development is classed as with or without planktonic larvae. Colour is assessed as cryptic (С), conspicuous (i.e. aposematic, A), or uncertain (7). Only one reference has been given for each species to economize on space. WITH PLANKTONIC LARVAE Species Colour Reference Doridacea minus Chromodorididae Acanthodoris brunnea MacFarland Hurst, 1967 Acanthodoris nanaimoensis O'Donoghue Hurst, 1967 Acanthodoris pilosa (Muller) Adalaria proxima (Alder & Hancock) Aegires sublaevis Odhner Aegires punctilucens (Orbigny) Aldisa cooperi Robilliard & Baba Aldisa tara Millen Ancula evelinae Marcus Ancula gibbosa (Risso) Anisodoris prea Marcus & Marcus Archidoris montereyensis (Cooper) Archidoris odhneri (MacFarland) Archidoris pseudoargus (Rapp) Asteronotus caespitosus (van Hasselt) Crimora papillata Alder & Hancock Dendrodoris fumata (Rüppell & Leuckart) Dendrodoris krebsi (Môrch) Diaphorodoris lirulatocauda Millen Diaulula sandiegensis (Cooper) Discodoris concinna (Alder & Hancock) Discodoris erythraeensis Vayssiere Doridella obscura Verrill Doridella steinbergae (Lance) Doriopsis aurantiaca (Eliot) Doriopsis viridis Pease Doris ocelligera Bergh Goniodoris castanea Alder & Hancock Goniodoris nodosa (Montagu) Goniodoris sugashimae Baba Gymnodoris bicolor (Alder & Hancock) Gymnodoris citrina (Bergh) Halgerda rubicunda Baba Hexabranchus sanguineus Ruppell & Leuckart Homoiodoris japonica Bergh Jorunna tomentosa (Cuvier) Nembrotha limaciformis Eliot Okenia ascidicola Morse Okenia impexa Marcus Onchidoris bilamellata (Linnaeus) Onchidoris muricata (Müller) Onchidoris neapolitana (Chiaje) Peltodoris hummelincki Marcus Phyllidia varicosa Lamarck Platydoris scabra (Cuvier) Polycera quadrilineata (Muller) Polycerella emertoni Verrill Rostanga pulchra MacFarland Sebadoris crosslandi (Eliot) Taringa telopia Marcus Thordisa filix Pruvot-Fol Triopha catalinae (Cooper) Trippa areolata (Alder & Hancock) O»00000>0>000000>0000>>00000000000000>00000>000000000 Thompson, 1967 Thompson, 1958 Schmekel & Portmann, 1982 Thiriot-Quievreux, 1972 Millen & Gosliner, 1985 Millen & Gosliner, 1985 Eyster, 1980 Thompson & Brown, 1984 Eyster, 1980 McGowan & Pratt, 1954 Hurst, 1967 Thompson, 1967 Gohar & Soliman, 1967e Schmekel & Portmann, 1982 Gohar & Soliman, 1967a Bandel, 1976 Goddard, 1984 Hurst, 1967 Gohar & Soliman, 1967f Gohar & Aboul-Ela, 1959 Perron & Turner, 1977 Bickell & Chia, 1979 Hamatani, 1961b Hamatani, 1961b Schmekel & Portmann, 1982 Schmekel & Portmann, 1982 Thompson, 1967 Hamatani, 1961a Hamatani, 1960a Young, 1967 Hamatani, 1960b Gohar & Soliman, 1963 Hamatani, 1962 Thompson, 1967 Soliman, 1991 Morse, 1972 Eyster, 1980 Thompson, 1967 Thompson, 1967 Schmekel & Portmann, 1982 Bandel, 1976 Soliman, 1986 Soliman, 1978 Thompson, 1967 Franz & Clark, 1972 Chia & Koss, 1978 Soliman, 1980 Bandel, 1976 Schmekel & Portmann, 1982 Hurst, 1967 Gohar & Soliman, 1967g WARNING COLORATION IN NUDIBRANCHS 247 TABLE 2. (Continued) Species Colour Reference Doridacea Chromodorididae Chromodoris africana Eliot A Gohar & Aboul-Ela, 1959 Chromodoris amoena Chesseman A Thompson, 1972a Chromodoris annulata Eliot A Gohar & Aboul-Ela, 1957b Chromodoris clenchi (Russell) A Bandel, 1976 Chromodoris inornata Pease A Gohar & Soliman, 1967b Chromodoris luteopunctata (Gantès) A Gantès, 1962 Chromodoris perola Marcus A Bandel, 1976 Chromodoris pulchella (Rúppell & Leuckart) A Gohar & Aboul-Ela, 1957b Chromodoris tinctoria (Rúppell & Leuckart) A Gohar & Soliman, 1967c Glossodoris atromarginata (Cuvier) A Gohar & Aboul-Ela, 1959 Glossodoris pallida (Ruppell & Leuckart) A Soliman, 1991 Hypselodoris bilineata Pruvot-Fol A Gantès, 1962 Hypselodoris elegans (Cantraine) A Rho, 1888 Hypselodoris kayae Young A Young, 1967 Aeolidiacea Aeolidia papillosa (Linnaeus) Williams, 1980 Aeolidiella glauca (Alder & Hancock) Aeolidiella mannarensis (Rao & Alagarswami) Aeolidiella sanguinea (Norman) Antonietta luteorufa Schmekel Austraeolis catina (Marcus & Marcus) Berghia benteva (Marcus) Berghia coerulescens (Laurillard) Berghia verrucicornis (Costa) Catriona gymnota (Couthouy) Coryphella browni Picton Coryphella fusca O’Donoghue Coryphella gracilis (Alder & Hancock) Coryphella lineata (Lovén) Coryphella nobilis Verrill Coryphella parva Hadfield Coryphella pedata (Montagu) Coryphella pellucida (Alder & Hancock) Coryphella trilineata O'Donoghue Coryphella verrucosa (Sars) Cratena peregrina (Gmelin) Cratena pilata (Gould) Cumanotus beaumonti (Eliot) Cuthona adyarensis Rao Cuthona albocrusta (MacFarland) Cuthona albopunctata (Schmekel) Cuthona coerulea (Montagu) Cuthona futairo Baba Cuthona genovae (O’Donoghue) Cuthona ilonae (Schmekel) Cuthona miniostriata (Schmekel) Cuthona ocellata (Schmekel) Cuthona ornata Baba Cuthona pinnifera (Baba) Dicata odhneri Schmekel Dondice occidentalis (Engel) Dondice paguerensis Brandon & Cutress Embletonia pulchra (Alder & Hancock) Eubranchus cingulatus (Alder & Hancock) OOOOOOPOOOOOPOOOOOPIDIDINDONDNDDNOOPPOANONANNDOO Hadfield, 1963a Rao & Alagarswami, 1960 Tardy, 1969a Schmekel & Portmann, 1982 Clark & Goetzfried, 1978 Eyster, 1980 Tardy, 1962c Tardy, 1962c Clark, 1975 Thompson & Brown, 1984 Roginskaya, 1969 Kuzirian, 1979 Thompson, 1967 Kuzirian, 1977 Hadfield, 1963b Schmekel & Portmann, 1982 Kuzirian, 1979 Bridges & Blake, 1972 Kuzirian, 1979 Schmekel & Portmann, 1982 Eyster, 1980 Hurst, 1967 Rao, 1962 Hurst, 1967 Schmekel & Portmann, 1982 Schmekel & Portmann, 1982 Hamatani, 1960b Schmekel & Portmann, 1982 Schmekel & Portmann, 1982 Schmekel & Portmann, 1982 Schmekel, 1966 Hamatani, 1960b Hamatani, 1960b Schmekel & Portmann, 1982 Eyster, 1980 Brandon & Cutress, 1985 Schmekel & Portmann, 1982 Tardy, 1970 (continued) 248 TABLE 2. (Continued) Species Eubranchus doriae (Trinchese) Eubranchus exiguus (Alder & Hancock) Eubranchus farrani (Alder & Hancock) Eubranchus misakiensis Baba Eubranchus olivaceus (O’Donoghue) Eubranchus pallidus (Alder & Hancock) Facelina annulicornis (Chamisso & Eysenhardt) Facelina coronata (Forbes & Goodsir) Facelina dubia Pruvot-Fol Facelina fusca Schmekel Favorinus auritulus Marcus Favorinus branchialis (Rathke) Fiona pinnata (Eschscholtz) Flabellina affinis (Gmelin) Flabellina engeli Marcus Hermissenda crassicornis (Eschscholtz) Limenandra nodosa Haefelfinger & Stamm Phestilla lugubris Bergh Phestilla melanobranchia Bergh Phidiana lynceus Bergh Phyllodesmium xenia Gohar & Aboul-Ela Piseinotecus sphaeriferus (Schmekel) Pruvotfolia pselliotes (Labbé) Spurilla japonica (Eliot) Spurilla neapolitana (Chiaje) Dendronotacea Dendronotus albopunctatus Robilliard Dendronotus frondosus (Ascanius) Dendronotus iris Cooper Dendronotus rufus O’Donoghue Dendronotus subramosus MacFarland Doto coronata (Gmelin) Doto doerga Marcus & Marcus Doto fragilis (Forbes) Doto japonica Odhner Doto paulinae Trinchese Doto pinnatifida (Montagu) Doto rosea Trinchese Doto yongei Thompson Hancockia burni Thompson Hancockia uncinata (Hesse) Lomanotus stauberi Clark & Goetzfried Melibe fimbriata Alder & Hancock Melibe leonina (Gould) Tritonia cincta Pruvot-Fol Tritonia diomedea Bergh Tritonia hombergi Cuvier Tritonia plebeia Johnston Arminacea Dirona albolineata Cockerell & Eliot Dirona aurantia Hurst Hero formosa (Lovén) Janolus cristatus (Chiaje) Colour ФЛ - OQOOr IYO OOOOrOODO>oOo® SHLÄPUPK PL SL ELF DIE PH EI EL EI EKD eK EI E I SI EX) ооо Reference Tardy, 1962a Hadfield, 1963a Thompson, 1967 Hamatani, 1961b Hurst, 1967 Hadfield, 1963a Thompson & Brown, 1984 Tardy, 1970 Schmekel & Portmann, 1982 Schmekel & Portmann, 1982 Clark & Goetzfried, 1978 Haefelfinger, 1962 Holleman, 1972 Schmekel & Portmann, 1982 Bandel, 1976 Harrigan & Alkon, 1978 Schmekel & Portmann, 1982 Harris, 1975 Harris, 1975 Clark & Goetzfried, 1978 Gohar & Aboul-Ela, 1957a Schmekel & Portmann, 1982 Tardy, 1969b Hamatani, 1967 Clark & Goetzfried, 1978 Robilliard, 1972 Miller, 1958 Robilliard, 1970 Robilliard, 1970 Robilliard, 1970 Thompson, 1967 Schmekel & Portmann, 1982 Kress, 1975 Hamatani, 1963 Schmekel & Portmann, 1982 Kress, 1975 Schmekel & Portmann, 1982 Thompson,’ 19726 Thompson, 1972b Schmekel & Portmann, 1982 Clark & Goetzfried, 1978 Thompson & Crampton, 1984 Bickell & Kempf, 1983 Schmekel & Portmann, 1982 Kempf & Willows, 1977 Thompson, 1962 Thompson, 1967 Hurst, 1967 Hurst, 1967 Thompson, 1967 Thompson & Brown, 1984 WARNING COLORATION IN NUDIBRANCHS 249 TABLE 2. (Continued) WITHOUT PLANKTONIC LARVAE Species Doridacea minus Chromodorididae Austrodoris macmurdensis Odhner Dendrodoris krebsi (Mórch) Dendrodoris limbata (Cuvier) Discodoris rosi Ortea Doriopsilla pharpa Marcus Okadaia elegans Baba Trippa spongiosa (Kelaart) Vayssieria caledonica (Risbec) Doridacea Chromodorididae Cadlina laevis (Linnaeus) Chromodoris loringi (Angas) Glossodoris obsoleta (Rüppell & Leuckart) Glossodoris sibogae (Bergh) Hypselodoris bennetti (Angas) Hypselodoris villafranca (Risso) Mexichromis tricolor (Cantraine) Aeolidacea Aeolidiella alder (Cocks) Coryphella salmonacea (Couthouy) Cuthona granosa Schmekel Cuthona poritophages Rudman Embletonia gracilis Risbec Herviella mietta Marcus & Burch own genes contributing to the next genera- tion. Conversely if a cryptic animal dies soon after reproducing this will reduce the chances of a predator finding it, acquiring a searching image for its patttern, and then hunting out similarly coloured prey in the vicinity. This ar- gument was first used by Blest (1963) and was supported by evidence from saturniid moths. It should be possible to test this pre- diction by comparing the times survived after the last oviposition by cryptic and by apose- matic nudibranchs with non-planktonic devel- opment. Unfortunately although this informa- tion is probably available in the files of the many workers who have studied oviposition and development in nudibranchs it has never been published. 4. Evolution of innate responses of predators Until recently it was assumed that the pred- ators which avoid aposematic prey had to learn through experience to associate unpal- Colour Reference Gibson et al. 1970 Clark & Goetzfried, 1978 Si, 1931 Ortea, 1979 Clark & Goetzfried, 1978 Baba, 1937 Gohar & Soliman, 1967g Risbec, 1953 CCOO Thompson, 1967 Thompson, 1972a Gohar 8 Soliman, 1967d Usuki, 1967 Thompson, 1972a Gantès, 1962 Haefelfinger, 1969 >>>>>>> Tardy, 1962b Morse, 1971 Schmekel, 1966 Rudman, 1979 Gosliner & Griffiths, 1981 Young, 1967 MOIMIONSLS atability with colour or with other specific sig- nals, but several predators are now known which have innate aversion responses to spe- cific signals (see Edmunds, 1974). These predators include certain species of birds (Smith, 1975,1977; Caldwell & Rubinoff, 1983) and fish (Rubinoff & Kropach, 1970), but other species of predator which do not experience the specific aposematic signals in their normal environment lack innate aver- sions (Smith, 1980). An animal is most un- likely to evolve an innate aversion to a stim- ulus unless there is clear advantage т avoiding that stimulus, otherwise several Ba- tesian mimics would quickly evolve to exploit the situation (Guildford, 1990). Such aversive responses evolved when the predators origi- nally developed learned aversions, but where there was selective advantage in minimizing the time spent, or the danger, in having to learn. It follows from this argument that innate aversive responses imply a long evolutionary history of behaviour in response to a specific aposematic signal. 250 EDMUNDS It is known that some fish have innate aver- sive responses to sea snakes (Rubinoff & Kropach, 1970), but no such response is known towards any nudibranch, and the ex- periments of feeding nudibranchs to fish indi- cate that the aversive responses have to be learned. However, no critical experiments have been undertaken, and where fish ap- pear to ignore nudibranchs crawling around in aquaria it is possible that they actually see and then deliberately avoid them innately. The Evolution of Aposematism in Nudibranchs Assuming that a particular nudibranch is aposematic the question arises of which evolved first, unpalatability or warning co- lours? The first possibility is supported by the fact that many cryptic nudibranchs are unpal- atable to fish (Thompson, 1960). In addition, conspicuous colours will only evolve in a pal- atable animal, or one that is only slightly un- palatable, if they confer some selective ad- vantage which is greater than the liability of attracting predators. Thus they might evolve because they confer an advantage in intraspe- cific encounters (e.g. sexual, territorial, etc.). However, there is no evidence that colour has such a function in nudibranchs. Colour can also be of value in interspecific contexts (Batesian mimicry, deimatic and flash co- lours), but these are comparatively rare in nudibranchs (Edmunds, 1987), so | consider it highly improbable that bright colours evolved before unpalatability. | therefore conclude that if aposematic nudibranchs occur, they have evolved through individual selection from ini- tially cryptic but relatively unpalatable species. CONCLUSIONS | conclude from this review that aposema- tism does occur in some nudibranchs and that the evidence for it is particularly strong in those species which are conspicuously co- loured in their natural habitat, are unpalatable to some predators, and are part of a mimetic group of species. Clearly there is plenty of scope for more detailed experimental studies of aposematism in nudibranch molluscs, and the purpose of this paper is to raise some of the issues that might usefully be addressed in such an investigation. There are also many anomalies that need further study; one exam- ple which | gave recently is Polycera elegans (Bergh) which is a brilliantly coloured species that is rare (Edmunds, 1987). Unless an ani- mal is exceptionally noxious and resilient to sampling by a predator, it is difficult to see the selective advantage for a rare species of be- ing conspicuous instead of being cryptic. | hope that this review will stimulate further ex- perimental work on the significance of brilliant colours in nudibranchs. ACKNOWLEDGEMENTS | wish to thank Professor Arthur Cain and Dr. Janet Edmunds for critically reading the paper, Dr. Hans Bertsch for permission to publish some of his observations, and numerous other nudibranch enthusiasts for discussions on the functions of colours in these animals. LITERATURE CITED BABA, K., 1937, Contribution to the knowledge of a nudibranch Okadaia elegans Baba. Japanese Journal of Zoology, 7: 147-190. BANDEL, K., 1976, Egg masses of 27 Caribbean opisthobranchs from Santa Marta, Columbia. Studies on Neotropical Fauna and Environment, 11: 87-118. BEHRENS, D.W., 1980, Pacific Coast Nudi- branchs. Sea Challengers, Los Osos, California, 112 pp. BERTSCH, H., 1978a, The Chromodoridinae nudi- branchs from the Pacific coast of America. Part Il. The genus Chromodoris, Veliger, 20: 307-327. BERTSCH, H., 1978b, The Chromodoridinae nudi- branchs from the Pacific coast of America. Part Ш. The genera Chromolaichma and Mexi- chromis. Veliger, 21: 70-86. BERTSCH, H., 1978c, The Chromodoridinae nudi- branchs from the Pacific coast of America. Part IV. The genus Hypselodoris. Veliger, 21: 236- 250. BERTSCH, H. & S. JOHNSON, 1981, Hawaiian nudibranchs. Oriental Publishing Co., Honolulu, Hawaii. 112 pp. BICKELL, L.R. & F.S. CHIA, 1979, Organogenesis and histogenesis in the planktonic veliger of Doridella steinbergae (Opisthobranchia: Nudi- branchia). Marine Biology, Berlin 52: 291-313. BICKELL, L.R. & S.C. KEMPF, 1983, Larval and metamorphic morphogenesis in the nudibranch Melibe leonina (Mollusca: Opisthobranchia). Bio- logical Bulletin. Marine Biological Laboratory, Woods Hole, 165: 119-138. BLEST, A.D., 1963, Longevity, palatability and nat- ural selection in five species of New World sat- urniid moth. Nature, 197: 1183-1186. BRANDON, M. & C.E. CUTRESS, 1985, A new WARNING COLORATION IN NUDIBRANCHS 251 Dondice (Opisthobranchia: Favorinidae), preda- tor of Cassiopea in southwest Puerto Rico. Bul- letin of Marine Science, 36: 139—144. BRIDGES, C. & J.A. BLAKE, 1972, Embryology and larval development of Coryphella trilineata O'Donoghue, 1921 (Gastropoda: Nudibranchia). Veliger, 14: 293-297. BROWER, L.P., F.H. POUGH & H.R. MECK, 1970, Theoretical investigations of automimicry, 1. Sin- gle trial learning. Proceedings of the National Academy of Sciences of the United States of America, 66: 1059-1066. BROWER, L.P., W.N. RYERSON, L.L. COP- PINGER & S.C. GLAZIER., 1968, Ecological chemistry and the palatability spectrum. Science, 161: 1349-1351. CALDWELL, G.S. & R.W. RUBINOFF, 1983, Avoidance of venomous sea snakes by naive herons and egrets. Auk, 100: 195-198. CHIA, F.S. & R. KOSS, 1978, Development and metamorphosis of Rostanga pulchra (Mollusca: Nudibranchia). Marine Biology, Berlin 46: 109— 120. CLARK, K.B., 1975, Nudibranch life cycles in the northwest Atlantic and their relationship to the ecology of fouling communities. Helgoländer wis- senschaftliche Meeresuntersuchungen, 27: 28— 69. CLARK, K.B. & A. GOETZFRIED, 1978, Zoogeo- graphic influences on development patterns of north Atlantic Ascoglossa and Nudibranchia, with a discussion of factors affecting egg size and number. Journal of Molluscan Studies, 44: 283— 294. COOK, E.F., 1962, A study of food choices of two opisthobranchs, Rostanga pulchra McFarland and Archidoris montereyensis (Cooper). Veliger, 4: 194-196. COTT, H.B., 1940. Adaptive coloration in animals. Methuen, London. 508 pp. CROSSLAND, C., 1911, Warning coloration in a nudibranch mollusc and in a chamaeleon. Pro- ceedings of the Zoological Society of London, 79: 1062-1067. CROZIER, W.J., 1916, On the immunity coloration of some nudibranchs. Proceedings of the Na- tional Academy of Sciences of the United States of America, 2: 672-675. EDMUNDS, M., 1966, Protective mechanisms in the Eolidacea (Mollusca Nudibranchia). Journal of the Linnean Society (Zoology), 46: 27-71. EDMUNDS, M., 1974, Defence in Animals. Long- man, Harlow. 357 pp. EDMUNDS, M., 1981, Opisthobranchiate Mollusca from Ghana: Chromodorididae. Zoological Jour- nal of the Linnean Society, 72: 175-201. EDMUNDS, M., 1987, Color in opisthobranchs. American Malacological Bulletin, 5: 185-196. EDMUNDS, M. & A. KRESS, 1969, On the Euro- pean species of Eubranchus (Mollusca Opis- thobranchia). Journal of the Marine Biological Association of the United Kingdom, 49: 879-912. EYSTER, L.S., 1979, Reproduction and develop- mental variability in the opisthobranch Tenellia pallida. Marine Biology, Berlin 51: 133-140. EYSTER, L.S., 1980, Distribution and reproduction of shell-less opisthobranchs from South Carolina. Bulletin of Marine Science, 30: 580-599. FRANZ, D.R. & K.B. CLARK, 1972, A discussion of the systematics, reproductive biology, and zoo- geography of Polycerella emertoni and related species (Gastropoda: Nudibranchia). Veliger, 14: 265-270. GANTES, H., 1962, Recherches sur quelques larves de Glossodorididae (Mollusques Opistho- branches). Bulletin de la Société des Sciences naturelles et physiques du Maroc, 42: 267-277. GARSTANG, W., 1889, Report on the nudibranchi- ate Mollusca of Plymouth Sound. Journal of the Marine Biological Association of the United King- dom, 1: 173-198. GARSTANG, W., 1890, A complete list of the opisthobranchiate Mollusca found at Plymouth. Journal of the Marine Biological Association of the United Kingdom, 1: 399-457. GIBSON, R., T.E. THOMPSON & G.A. ROBIL- LIARD, 1970, Structure of the spawn of an Ant- arctic dorid nudibranch Austrodoris macmurden- sis Odhner. Proceedings of the Malacological Society of London, 39: 221-225. GITTLEMAN, J.L. & P.H. HARVEY, 1980, Why are distasteful prey not cryptic? Nature, 286: 149— 150. GODDARD, J.H.R., 1984, The opisthobranchs of Cape Arago, Oregon, with notes on their biology and a summary of benthic opisthobranchs known from Oregon. Veliger, 27: 143-163. GOHAR, H.A.F. & 1.A. ABOUL-ELA, 1957a, On a new nudibranch “Phyllodesmium хета” (from the Red Sea, with a description of its develop- ment). Publications of the Marine Biological Sta- tion, Ghardaga, 9: 131-144. GOHAR, H.A.F., 1975b, The development of three chromodorids (with the description of a new spe- cies). Publications of the Marine Biological Sta- tion, Ghardaga, 9: 203-228. GOHAR, H.A.F. & 1.A. ABOUL-ELA, 1959, On the biology and development of three nudibranchs (from the Red Sea). Publications of the Marine Biological Station, Ghardaga, 10: 41-62. GOHAR, H.A.F. 8 С.М. SOLIMAN, 1963, The biol- ogy and development of Hexabranchus san- guineus (Rupp. and Leuck.) (Gastropoda, Nudi- branchiata). Publications of the Marine Biological Station, Ghardaga, 12: 219-248. GOHAR, H.A.F. & G.N. SOLIMAN, 1967a, The biology and development of Dendrodoris (= Doridopsis) fumata (Rupp. and Leuck.) (Gas- tropoda, Nudibranchia). Publications of the Ma- rine Biological Station, Ghardaga, 14: 31-54. GOHAR, H.A.F. & G.N. SOLIMAN, 1967b, The bi- ology and development of Chromodoris inornata Pease (Gastropoda, Nudibranchia). Publications of the Marine Biological Station, Ghardaga, 14: 77-94. GOHAR, H.A.F. & G.N. SOLIMAN, 1967c, The bi- 252 EDMUNDS ology and development of the nudibranch Chro- modoris tinctoria (Rupp. and Leuck.) (with refer- ence to the taxonomic value of spawning characters). Publications of the Marine Biological Station, Ghardaga, 14: 95-108. GOHAR, H.A.F. & G.N. SOLIMAN, 1967d, The di- rect development of the nudibranch Casella ob- soleta (Rupp. and Leuck.) (with remarks on the metamorphosis). Publications of the Marine Bio- logical Station, Ghardaga, 14: 149-166. GOHAR, H.A.F. & G.N. SOLIMAN, 1967e, The bi- ology and development of Asteronotus cespito- sus (van Hasselt) (Gastropoda, Nudibranchia). Publications of the Marine Biological Station, Ghardaga, 14: 177-195. GOHAR, H.A.F. & G.N. SOLIMAN, 1967f, The bi- ology and development of Discodoris concinna (Alder and Hancock) (Gastropoda, Nudibran- chia). Publications of the Marine Biological Sta- tion, Ghardaga, 14: 197-214. GOHAR, H.A.F. & G.N. SOLIMAN, 1967g, On two rare nudibranchs of the genus Trippa Bergh (of different developmental behaviour). Publications of the Marine Biological Station, Ghardaga, 14: 269-293. GOSLINER, Т.М. & RJ. GRIFFITHS, 1981, De- scription and revision of some South African ae- olidacean Nudibranchia (Mollusca, Gastropoda). Annals of the South African Museum, 84: 105- 150. GOSLINER, T.M. & S.V. MILLEN, 1984, Records of Cuthona pustulata (Alder & Hancock, 1854) from the Canadian Pacific. Veliger, 26: 183-187. GUILDFORD, T, 1990. The evolution of aposema- tism. In: Insect Defenses, ed. D.L. Evans 4 J.O. Schmidt, SUNY Press, New York, pp 23-61. HADFIELD, M.G. 1963a, The biology of nudibranch larvae. Oikos, 14: 85-95. HADFIELD, M.G., 1963b, Coryphella parva n. sp., a new nudibranchiate mollusc from the Oresund. Videnskabelige Meddelelser fra Dansk naturhis- torisk Forening, 125: 371-376. HAEFELFINGER, H.R., 1962, Quelques faits con- cernant la nutrition chez Favorinus branchialis (Rathke 1806) et Stiliger vesiculosus (Deshayes 1864), deux mollusques opisthobranches. Revue suisse de zoologie, 69: 312-316. HAEFELFINGER, H.R., 1969, Contribution a la systématique des glossodoridiens méditerra- néens (Gastropoda, Opisthobranchia). Revue suisse de zoologie, 76: 703-710. HAMATANI, |., 1960a, Notes on veligers of Japa- nese opisthobranchs (1). Publications of the Seto Marine Biological Laboratory, 8: 55-70. HAMATANI, |., 1960b, Notes on veligers of Japa- nese opisthobranchs (2). Publications of the Seto Marine Biological Laboratory, 8: 307-315. HAMATANI, |., 1961a, notes on veligers of Japa- nese opisthobranchs (3). Publications of the Seto Marine Biological Laboratory, 9: 67-79. HAMATANI, |., 1961b, Notes on veligers of Japa- nese opisthobranchs (4). Publications of the Seto Marine Biological Laboratory, 9: 353-361. HAMATANI, |., 1962, Notes on veligers of Japa- nese opisthobranchs (5). Publications of the Seto Marine Biological Laboratory, 10: 283-292. HAMATANI, I., 1963, Notes on veligers of Japa- nese opisthobranchs (6) Publications of the Seto Marine Biological Laboratory, 11: 125-130. HAMATANI, 1967., Notes on veligers of Japanese opisthobranchs (7). Publications of the Seto Ma- rine Biological Laboratory, 15: 121-131. HAMILTON, W.D., 1964, The genetical evolution of social behaviour. I-Il. Journal of Theoretical Biol- ogy, 7: 1-52. HARDY, A.C., 1956, The open sea. Its natural his- tory: the world of plankton. Collins, London, 335 pp. (New Naturalist 34). HARRIGAN, J.F. & D.L. ALKON, 1978, Larval rear- ing, metamorphosis, growth and reproduction of the eolid nudibranch Hermissenda crassicornis (Eschscholtz, 1831) (Gastropoda: Opisthobran- chia). Biological Bulletin. Marine Biological Lab- oratory, Woods Hole, 154: 430—439. HARRIS, L.G., 1973, Nudibranch associations. Current Topics in Comparative Pathobiology, 2: 213-315. HARRIS, L.G., 1975, Studies on the life history of two coral-eating nudibranchs of the genus Phe- stilla. Biological Bulletin. Marine Biological Labo- ratory, Woods hole, 149: 539-550. HARRIS, L.G., M. POWERS & J. RYAN, 1980, Life history studies of the estuarine nudibranch Tenel- lia fuscata (Gould, 1870). Veliger, 23: 70-74. HARRIS, L.G., L.W. WRIGHT & B.R. RIVEST, 1975, Observations on the occurrence and biol- ogy of the aeolid nudibranch Cuthona nana in New England waters. Veliger, 17: 264-268. HARVEY, P.H., J.J. BULL., M. PEMBERTON & R.J. PAXTON, 1982, The evolution of apose- matic coloration in distateful prey: a family model. American Naturalist, 119: 710-719. HARVEY, P.H. & R.J. PAXTON, 1981a, The evolu- tion of aposematic coloration. Oikos, 37: 391-— 393. HARVEY, Р.Н. & R.J. PAXTON, 1981b, On apose- matic coloration: a rejoinder. Oikos, 37: 395- 396. HECHT, E., 1896, Contribution a l'étude des nudi- branches. Mémoires de la Société de Zoologique de France, 8: 537-711. HERDMAN, W.A. 1890, On the structure and func- tion of the cerata or dorsal papillae in some nudi- branchiate Mollusca. Quarterly Journal of Micro- scopical Science, 31: 41-63. HERDMAN, W.A. & J.A. CLUBB, 1890, Third report on the Nudibranchiata of the L.M.B.C. district. Proceedings and Transactions of the Liverpool Biological Society, 4: 131-169. HOLLEMAN, J.J., 1972, Observations on growth, feeding, reproduction and development in the opisthobranch Fiona pinnata (Eschscholtz). Veliger, 15: 142-146. HURST, A., 1967, The egg masses and veligers of thirty northeast Pacific opisthobranchs. Veliger, 9: 255—288. WARNING COLORATION IN NUDIBRANCHS 253 JARVI, T., B. SILLEN-TULLBERG & C. WIKLUND, 1981, The cost of being aposematic. An experi- mental study of predation on larvae of Papilio machaon by the great tit Parus major. Oikos, 36: 267-272. JUST, H. & M. EDMUNDS, 1985, North Atlantic nudibranchs (Mollusca) seen by Henning Lem- che. Ophelia supplement 2, 170 pp. KEMPF, S.C. 8 A.O.D. WILLOWS, 1977, Labora- tory culture of the nudibranch Tritonia diomedea Bergh (Tritoniidae: Opisthobranchia) and some aspects of its behavioral development. Journal of Experimental Marine Biology and Ecology, 30: 261-276. KRESS, A., 1975, Observations during embryonic development in the genus Doto (Gastropoda, Opisthobranchia). Journal of the Marine Biologi- cal Association of the United Kingdom, 55: 691— 701. KUZIRIAN, A.M., 1977, The rediscovery and biol- ogy of Coryphella nobilis Verrill, 1880 in New En- gland (Gastropoda: Opisthobranchia). Journal of Molluscan Studies, 43: 230-240. KUZIRIAN, A.M., 1979, Taxonomy and biology of four New England coryphellid nudibranchs (Gas- tropoda: Opisthobranchia). Journal of Molluscan Studies, 45: 239-261. McGOWAN, J.A. & I. PRATT, 1954, The reproduc- tive system and early embryology of the nudi- branch Archidoris montereyensis (Cooper). Bul- letin of the Museum of Comparative Zoology at Harvard, 111: 261-276. MILLEN, S.V. & T.M. GOSLINER, 1985, Four new species of dorid nudibranchs belonging to the ge- nus Aldisa (Mollusca: Opisthobranchia), with a revision of the genus. Zoological Journal of the Linnean Society, 84: 195-233. MORSE, М.Р., 1971, Biology and life history of the nudibranch mollusc, Coryphella stimpsoni (Verrill 1879). Biological Bulletin. Marine Biological Lab- oratory, Woods Hole, 140: 84-94. MORSE, M.P., 1972, Biology of Okenia ascidicola spec. nov. (Gastropoda: Nudibranchia). Veliger, 15: 97-101. ORTEA, J.A., 1979, Deux nouveaux doridiens (Mollusca, Nudibranchiata) de la côte nord d'Espagne. Bulletin du Museum national d'his- toire naturelle, Paris (4) 1 (A): 575-588. PERRON, F.E. & R.D. TURNER, 1977, Develop- ment, metamorphosis, and natural history of the nudibranch Doridella obscura Verrill (Coram- bidae: Opisthobranchia). Journal of Experimental Marine Biology and Ecology, 27: 171-185. POULTON, E.B., 1890, The Colours of Animals. Their Meaning and Use, especially considered in the Case of Insects. Kegan Paul, Trench, Trub- ner, London. 360 pp (International Scientific Se- ries 68). RAO, K.P., 1965, Moridella brockii Bergh 1888, re- described with notes on anatomy and early de- velopment. Journal of the Marine Biological As- sociation of India, 7: 61-68. RAO, K.V., 1962, Development and life history of a nudibranchiate gastropod Cuthona adyarensis Rao. Journal of Marine Biological Association of India, 3: 186—197. RAO, K.V., 1970, On the structure and life-history of a new aeolid, Favorinus argentimaculatus from Рак Bay. pp 1009-1016. in: Proceedings of the Symposium on Mollusca (Cochin, 1968). Sympo- sium Ser. Marine Biological Association of India, 3. RAO, K.V. & K. ALAGARSWAMI, 1960, An account of the structure and early development of a new species of a nudibranchiate gastropod, Eolidina (Eolidina) mannarensis. Journal of the Marine Bi- ological Association of India, 2: 6-16. RHO, F., 1888, Studii sullo sviluppo della Chromo- doris elegans. Atti dell’ Accademia delle scienze fisiche e matematiche, Napoli (2) 1 App. 3: 1-7. RISBEC, J., 1953, Mollusques nudibranches de la Nouvelle-Calédonie. Faune de l'Union français 15: 1-189. RIVEST, B.R., 1978, Development of the eolid nudibranch Cuthona nana (Alder and Hancock, 1842), and its relationship with a hydreid and a hermit crab. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 154: 157-175. ROBILLIARD, G.A., 1970, The systematics and some aspects of the ecology of the genus Den- dronotus (Gastropoda: Nudibranchia). Veliger, 12: 433-479. ROBILLIARD, G.A, 1972, A new species of Den- dronotus from the northeastern Pacific with notes on Dendronotus nanus and Dendronotus robus- tus (Mollusca: Opisthobranchia). Canadian Jour- nal of Zoology, 50: 421-432. ROGINSKAYA, 1.S., 1962, The egg-masses of nudibranchs of the White Sea. Reporis of the White Sea Biological Station of the State Univer- sity of Moscow, 1: 201-214. ROGINSKAYA, I.S., 1969, Taxonomy and ecology of the nudibranch mollusc Coryphella fusca. Zoo- logicheskii zhurnal, 48: 1614—1617. ROGINSKAYA, 1970, Tenellia adspersa, a nudi- branch new to the Azov Sea, with notes on its taxonomy and ecology. Malacological Review, 3: 167-174. ROS, J., 1976, Sistemas de defensa en los opisto- branquios. Oecologia aquatica, 2: 41-77. ROS, J., 1977, La defensa en los opistobranquios. Investigacion y Ciencia, 12: 48—60. RUBINOFF, I. & С. KROPACH, 1970, Differential reactions of Atlantic and Pacific predators to sea snakes. Nature, Lond. 228: 1288-1290. RUDMAN, W.B., 1979, The ecology and anatomy of a new species of aeolid opisthobranch mol- lusc; a predator of the scleractinian coral Porites. Zoological Journal of the Linnean Society, 65: 339-350. RUDMAN, W.B., 1985, The Chromodorididae (Opisthobranchia: Mollusca) of the Indo-West Pacific: Chromodoris aureomarginata, C. verrieri and C. fidelis colour groups. Zoological Journal of the Linnean Society, 83: 241-299. SCHMEKEL, L., 1966, Zwei neue Arten der Familie 254 EDMUNDS Cuthonidae aus dem Golf von Neapel: Trinchesia granosa n. sp. und Trinchesia ocellata n. sp. (Gastr. Opisthobranchia). Pubblicazioni della Stazione zoologica di Napoli, 35: 13-28. SCHMEKEL, L. & A. PORTMANN, 1982, Opistho- branchia des Mittelmeeres. Springer-Verlag, Ber- lin. 410 pp. SCHULER, W. & Е. HESSE, 1985, On the function of warning coloration: a black and yellow pattern inhibits prey-attack by naive domestic chicks. Be- havioral Ecology and Sociobiology, 16: 249-255. SHYAMASUNDARI, К. & NAJBUDDIN, M., 1976, Experimental investigations of salinity and tem- perature effects on early developmental stages in Dendrodoris (Doriopsilla) miniata (Alder & Han- cock) (Gastropoda Opisthobranchia). Monitore Zoologico Italiano, 10: 93-94. SI, T., 1931, Un nouveau cas de condensation em- bryogénique chez un nudibranche (Doridopsis limbata Cuvier). Compte rendu hebdomadaire des séances de l'Académie des sciences, Paris 192: 302-304. SILLEN-TULLBERG, B., 1985, Higher survival of an aposematic than of a cryptic form of a distate- ful bug. Oecologia, 67: 411-415. SILLEN-TULLBERG, B. & E.H. BRYANT, 1983, The evolution of aposematic coloration in distate- ful prey: an individual selection model. Evolution, 37: 993-1000. SMITH, S.M., 1975, Innate recognition of coral snake pattern by a possible avian predator. Sci- ence, N.Y., 187: 759-760. SMITH, S.M., 1977, Coral-snake pattern recogni- tion and stimulus generalisation by naive great kiskadees (Aves: Tyrannidae). Nature, Lond. 265: 535-536. SMITH, S.M., 1980, Responses of naive temperate birds to warning coloration. American Midland Naturalist, 103: 346-352. SOLIMAN, G.N., 1978, The redescription, repro- duction and development of the dorid nudibranch Platydoris scabra (Cuvier) from the northwestern Red Sea. Journal of Molluscan Studies, 44: 151— 165. SOLIMAN, G.N., 1980, On the dorid nudibranch Sebadoris crosslandi (Eliot) from the northwest- ern Red Sea. Journal of Molluscan Studies, 46: 227-238. SOLIMAN, G.N., 1986, The reproduction and de- velopment of the dorid nudibranch Phyllidia var- icosa Lamarck 1801 from the northern Red Sea. Proceedings of the 8th International Malacologi- cal Congress,.Budapest, 1983, 255-260. SOLIMAN, G.N., 1991, A comparative review of the spawning, development and metamorphosis of prosobranch and opisthobranch gastropods with special reference to those from the north- western Red Sea. In: Edmunds, M (ed.), Evolutionary biology of opisthobranchs. Proceed- ings of the 9th International Malacological Con- gress, Edinburgh, 1986, Malacologia, 32(2): 257-271. TARDY, J., 1962a, Observations et expériences sur la métamorphose et la croissance de Capel- linia exigua. (Ald. et H.) (Mollusque Nudi- branche). Compte rendu hebdomadaire des sé- ances de l'Académie des sciences, Paris 254: 2242-2244. TARDY, J., 1962b, Cycle biologique et métamor- phose d’Aaeolidina alderi (Gastéropode, Nudi- branche). Compte rendu hebdomadaire des sé- ances de l'Académie des sciences, Paris 255: 3250-3252. TARDY, J., 1962c, A propos des especes de Berghia (Gastéropodes Nudibranches) des cotes de France et de leur biologie. Bulletin de l'Institut océanographique, Monaco 59 (1255): 1-20. TARDY, J., 1969a, Etude systématique et bi- ologique sur trois espèces d’Aeolidielles des côtes européenes (Gastéropodes Nudibranches). Bul- letin de l'Institut océanographique. Monaco 68 (1389): 1-40. TARDY, J., 1969b, Un nouveau genre de nudi- branche méconnu des cótes atlantique et de la Manche: Pruvotfolia (nov. g.) pselliotes (Labbé), 1923. Vie et Milieu, 20: 327-346. TARDY, J., 1970, Contribution a la connaissance de la biologie chez les nudibranches: développ- ement et métamorphose; vie prédatrice: 1. Facelina coronata (Forbes) et Aeolis sp. Bulletin de la Société zoologique de France, 95: 765- le THIRIOT-QUIEVREUX, C., 1977, Véligere plancto- trophe du doridien Aegires punctilucens (d'Or- bigny) (Mollusca: Nudibranchia: Notodorididae): description et métamorphose. Journal of Experi- mental Marine Biology and Ecology, 26: 177- 190. THOMPSON, T.E., 1958, The natural history, em- bryology, larval biology and post-larval develop- ment of Adalaria proxima (Alder and Hancock) (Gastropoda Opisthobranchia). Philosophical Transactions of the Royal Society, series B, 242: 1-58. THOMPSON, T.E., 1960, Defensive adaptations in opisthobranchs. Journal of the Marine Biological Association of the United Kingdom, 39: 123-134. THOMPSON, T.E., 1962, Studies on the ontogeny of Tritonia hombergi Cuvier (Gastropoda Opisthobranchia). Philosophical Transactions of the Royal Society series B, 245: 171-218. THOMPSON, T.E., 1967, Direct development in a nudibranch, Cadlina laevis, with a discussion of developmental processes in Opisthobranchia. Journal of the Marine Biological Association of the United Kingdom, 47: 1-22. THOMPSON, T.E., 1972a, Chromodorid nudi- branchs from eastern Australia (Gastropoda, Opisthobranchia). Journal of Zoology, London, 166: 391—409. THOMPSON, T.E., 19725, Eastern Australian Den- dronotoidea (Gastropoda: Opisthobranchia). Zoological Journal of the Linnean Society, 51: 63-77. THOMPSON, T.E., 1975, Dorid nudibranchs from eastern Australia (Gastropoda, Opisthobran- WARNING COLORATION IN NUDIBRANCHS 255 chia). Journal of Zoology, London, 176: 477- IZA THOMPSON, T.E. & G.H. BROWN, 1984, Biology of Opisthobranch Molluscs 2. Ray Society, Lon- don, 229 pp. THOMPSON, T.E. & D.M. CRAMPTON, 1984, Bi- ology of Melibe fimbriata, a conspicuous opistho- branch mollusc of the Indian Ocean, which has now invaded the Mediterranean Sea. Journal of Molluscan Studies, 50: 113-121. TODD, C.D., 1981, The ecology of nudibranch mol- luscs. Oceanography and Marine Biology Annual Reviews, 19: 141-234. TODD, C.D., 1983, Reproductive and trophic ecol- ogy of nudibranch molluscs. pp. 225-259. In: Russell-Hunter, W.D. (ed.), Ecology. The Mol- lusca (ed. K. Wilbur) 6, Academic Press, London & New York. USUKI, 1., 1967, The direct development and the single cup-shaped larval shell of a nudibranch Glossodoris sibogae (Bergh). Scientific Reports of Niigata University, Series D (Biology), 4:.75-— 85. WALLACE, A.R., 1889, Darwinism. Macmillan, London. 494 pp. WILLAN, R.C. & N. COLEMAN, 1984, Nudibranchs of Australia. Australasian Marine Photographic Index, Sydney. 56 pp. WILLIAMS, L.G., 1980, Development and feeding of larvae of the nudibranch gastropods Hermis- senda crassicornis and Aeolidia papillosa. Mala- cologia, 20: 99-116. YOUNG, D.K., 1967, New records of Nudibranchia (Gastropoda: Opisthobranchia) from the central and west-central Pacific with a description of a new species. Veliger, 10: 159-173. MALACOLOGIA, 1991, 32(2): 257-271 A COMPARATIVE REVIEW OF THE SPAWNING, DEVELOPMENT AND METAMORPHOSIS OF PROSOBRANCH AND OPISTHOBRANCH GASTROPODS WITH SPECIAL REFERENCE TO THOSE FROM THE NORTHWESTERN RED SEA Gamil N. Soliman Department of Zoology, Faculty of Science, University of Cairo, Egypt ABSTRACT Aspects of spawning, development and metamorphosis of 50 prosobranch and opisthobranch gastropods from the northwestern Red Sea are reviewed. For almost every species, data are given of the breeding season, size and number of eggs laid, and period and type of develop- ment. The early embryology, larval structure and behaviour, and post-larval development are summarized. Only the nudibranch Casella obsoleta has direct development. In agreement with Thorson's rule, most species have pelagic development, although prosobranchs (neogastro- pods in particular) show a tendency towards lecithotrophy and rapid metamorphosis. The in- trinsic and extrinsic factors affecting the type of development are discussed. INTRODUCTION In an attempt to review reproduction in prosobranchs and opisthobranchs, a study of their egg masses has recently been made (Soliman, 1987). The present paper aims to extend the comparative study to other as- pects of reproduction, namely egg size and number, early embryology, larval structure and behaviour, and the type of reproduction, and to review the factors which affect devel- opment and metamorphosis. This paper also aims to find out to what extent the patterns of molluscan development in the northwestern Red Sea agree with Thorson’s rule (1950) and to compare our results with those re- ported from other areas lying more or less within the same latitudes. The present study, like the former, is based mainly on new data and on studies made on Red Sea gastropods during the last 30 years (Gohar & Aboul-Ela, 1957, 1959; Gohar & Eisawy, 1963,1967; Gohar & Soliman, 1963, 1967; Eisawy & Sorial, 1968, 1974, 1976; Eisawy, 1970; Soliman, 1977, 1978, 1980, 1983, 1986) together with data from other sources. SPAWNING, EMBRYOLOGY AND LARVAL DEVELOPMENT Egg Capsules Primitively, gastropod eggs are laid singly, uncovered and they are externally fertilized. 257 In most gastropods, however, eggs are en closed either singly or in groups (up to hun dreds) in transparent thin-walled cases, ir leathery sacs or hard capsules. Cases may be dispersed freely becoming planktonic Most often they are embedded in a gelatinous matrix and moulded in thin sheets, ovoid о! globular jelly masses (or without a definite shape), cords or ribbons (Soliman, 1987). In opisthobranchs, egg cases may lie di- rectly in the spawn jelly or, as in many nudi- branch egg ribbons, may be primarily en- closed in tubes of thick mucus winding in the spawn matrix in variable fashion. Thus in small ribbons the tubes run in a closely parallel man- ner (Fig. 1A), but they radiate peripherally in massive undulating ones (Fig. 1B). In some species, each egg case within the tube may be isolated in a thin-walled compartment of var- ious shapes (Fig. 1C,D). The egg string of Strombus tricornis (Eisawy & Sorial, 1968) has a similar construction with the egg cases each enclosed in a gelatinous compartment that is finally coated by the egg string (Fig. 1E). The size limits of opisthobranch egg cases (and the numbers of eggs enclosed) are gen- erally lower than those recorded for proso- branch capsules (Table 1). In the former, cases measure 0.1—0.3 mm on average, but cases up to 0.6 mm across are not uncom- mon. The largest cases encountered in some masses of the nudibranch Hexabranchus sanguineus (2 x 0.6 mm, with more than 100 eggs) (Gohar & Soliman, 1963b) are still far smaller than what exists in certain proso- 258 SOLIMAN FIG. 1. Patterns of egg case arrangement in the jelly matrix in Red Sea gastropods. A. Trippa spongiosa: part of two parallel egg cords in jelly with no compartments (after Gohar & Soliman, 1967g). B. Discodoris concinna: enlarged portion of spawn ribbon with cords radiating and winding distally (modified after Gohar & Soliman, 1967f). C. Asteronotus cespitosus: segmented egg cord with one case in each segment (after Gohar & Soliman, 1967e). D. Chromodoris inornata: egg cases with each enclosed in a separate compart- ment (after Gohar & Soliman, 1967b). E. Strombus tricornis: similar arrangement to D, but eggs are in cords, not in a common jelly (after Eisawy & Sorial, 1968). branchs (19-35 x 5-9 mm in Pleuroploca tra- pezium with up to 400 eggs, and 8-9 x 3.5 mm in Nassa francolina with up to 1678 eggs) (Gohar & Eisawy, 1967b). Size and number of eggs The number of eggs laid by a gastropod is inversely proportional to egg size. According to the available data, the maximal size at- tained in prosobranchs markedly exceeds that in opisthobranchs (up to 0.75 mm in Co- nus (Natarajan, 1957), 0.44 mm in Strombus tricornis (Eisawy & Sorial, 1968) and 0.42 mm in Pleuroploca trapezium (Gohar & Eisawy, 1967b), against only 0.39 mm in Cadlina lae- vis (Thompson, 1967) and 0.33 mm in Ca- sella obsoleta (Gohar & Soliman, 1967d)). As DEVELOPMENT OF RED SEA GASTROPODS 259 anticipated, the number of eggs in a spawn deposited by an opisthobranch substantially surpasses what is recorded for prosobranchs (apart from certain archaeogastropods). 148 million eggs were recorded laid by Aplysia californica (MacGinitie, 1934) and a little less than 5 million by the nudibranch Asteronotus cespitosus (Gohar & Soliman, 1967e). However, in many prosobranchs (princi- pally neogastropods) the majority of eggs laid act as nurse cells subserving as food for the very small fraction of viable eggs which pro- ceed to full development (15% in Pleuroploca trapezium, < 6% in Chicoreus ramosus (Go- har & Eisawy, 1967b), 3% in Fusinus tuber- culata (Eisawy & Sorial, 1976a), 2% in Chicoreus virgineus (Gohar & Eisawy, 1967b), and even less in certain other spe- cies). According to Thorson (1940) 50,000 - 100,000 nurse eggs may exist per embryo in Volutopsius norwegicus. Nurse cells are not reported to exist in opisthobranchs. Cleavage and early embryology In the majority of opisthobranchs, the two initial divisions of the egg invariably bring about the formation of nearly equal mac- romeres which proceed thereafter in typical spiral cleavage (Fig. 2A). Unequal division is, however, typical of large, yolky prosobranch eggs. Actually such division is mainly depen- dent on the amount of yolk in the egg irre- spective of its size. Thus while the initial divi- sion of Tonna olearium eggs (0.25 mm in diameter) gives rise to nearly equal mac- romeres (Gohar & Eisawy, 1967a), similar or even smaller eggs of other species (0.18— 0.22 mm, Chicoreus virgineus; 0.25 mm, C. ramosus (Gohar & Eisawy, 1967b)) exhibit markedly unequal division with the mac- romeres A-C appearing as if budding from the giant D cell (Fig. 2B). The subsequent divi- sions do not much affect the relative disparity in the size of the macromeres. In contrast to the opacity of most gastropod embryos and larvae developing from leci- thotrophic eggs, planktonic larvae are rela- tively transparent. It is not uncommon never- theless to come across opaque embryos arising from comparatively small eggs (70 um, Sebadoris crosslandi (Soliman, 1980)) or, conversely, lecithotrophic larvae (Trippa spongiosa, egg 0.2 mm across (Gohar & Soli- man, 1967g)) or veliger and metamorphosing stages of directly developed species (Acte- ocina atrata (Mikkelsen & Mikkelsen, 1984)) with markedly clear structure. Generally, how- ever, as far as the planktotrophic Red Sea gastropods are concerned, the developmen- tal stages of opisthobranchs are much more transparent than are those of prosobranchs. Particularly in Hexabranchus sanguineus (Gohar & Soliman, 1963b), with intensely red yolk globules mostly condensed at the vege- tative side of the egg, it is possible to follow, in whole live embryos, the formation of the 4d mesoblast and its division into two cells (Fig. 2C), which remain visible even after their mi- gration inwards between the future ectoderm and endoderm. In fact, H. sanguineus, be- cause of its abundance, the huge number of eggs it lays, and the clarity of its cells, is ideal material for live study of spiral cleavage, cell lineage and germ layer formation in molluscs. Among the structures to appear early in opisthobranch embryos are the anal cells. These are initially posteroventral and slightly to the left. Their gradual shifting to the anterior right side (with the future proctodeal invagi- nation and anus) is the only ontogenetic evi- dence of torsion, which is thus much less than 180°. Casella obsoleta exhibits detorsion (Fig. 5D) (Gohar & Soliman, 1967d), with the anal cells and associated organs migrating poste- riorly (with the hind gut) during metamorpho- sis, until they reach their final position in the middle line just in front of the secondary larval kidney. They persist for 7-10 days after hatching and eventually vanish. This differs from Bonar's (1976) report that the anal cells disappear by the time the secondary kidneys develop. The mouth in some cases forms shortly be- fore the complete closure of the blastopore. In a number of species (Dendrodoris fumata (Fig. 4A), Chromodoris inornata) the second- ary larval kidney develops as early as the anal cells (Gohar 8 Soliman, 1967a,b). It attains its maximal development structurally and func- tionally during larval life. It is still encountered in the hatching juvenile of Casella obsoleta, but gradually diminishes in size and disap- pears in three weeks, i.e. after the disappear- ance of the anal cells. Hatching and larval behaviour At hatching, the whole upper wall of the neritid capsule detaches, thus liberating the larvae (Soliman, 1987). In neogastropods in particular (and certain mesogastropods, e.g. Tonna olearium (Gohar & Eisawy, 1967a)), 260 SOLIMAN TABLE 1. Breeding season, size, number and type of development of eggs of Red Sea prosobranchs and opisthobranchs. Species PROSOBRANCHS Trochus erythraeus Trochus dentatus Turbo radiatus Nerita forskali Lambis truncata* Strombus tricornis Strombus gibberulus Strombus fasciatus Polinices mammilla* Polinices melanostoma* Tonna olearium* Chicoreus virgineus* Chicoreus ramosus* Nassa francolina* Thais savignyi Leptoconchus cumingii Leptoconchus globosus Magilopsis lamarckii Pleuroploca trapezium* Fusinus tuberculatus* Conus sp. Conus sp. OPISTHOBRANCHS Aplysia dactylomela Dolabella auricularia Berthellina citrina Phyllobranchillus orientalis Elysia olivaceus Nembrotha limaciformis Gymnodoris sp. Hexabranchus sanguineus Chromodoris quadricolor Chromodoris pulchella Chromodoris annulata Chromodoris ghardagana Chromodoris inornata Chromodoris tinctoria Chromodoris pallida Casella atromarginata Casella obsoleta Asteronotus cespitosus Platydoris scabra Discodoris erythraeensis Discodoris concinna Discodoris sp. Trippa areolata Trippa spongiosa Sebadoris crosslandi Dendrodoris fumata Phyllidia varicosa Phyllodesmium xeniae “Nomenclature updated. Breeding season May—Aug Apr—Jul Feb—May Jan-Oct Apr—Jul May-Aug Aug-Sep Aug-Sep Apr-Jul Apr-May Jul-Dec Aug-Nov Feb-Nov Feb-Nov Feb-Nov Apr-May Feb-May Apr-Oct Apr-Oct Annual Jun-? May-Aug Jun-Aug Jun-Sep Annual Mar-Sep Mar-Apr Jul-? May-Nov Jun-Jul Jun-? Jun-Aug May-Sep May-Sep May-Sep Feb-Sep May-Sep Jul-? May-Nov Jun-? Jun—Jul Annual Jul-Oct May-Oct Dimension(s) of egg-case or capsule (mm) 0.124—0.15 х 0.148—0.17 0.4,0.48 x 0.43 av. 1.4-1.9 x 1-1.5 12-20 x 10-12 15-21 x 5-7 8-9 x 3.5 3.5-3.7 x 2.2-3 6-9 x 3.7-6.3 7-8 x 5-6 5-7 x 3.5-4.5 19-35 x 5-9 хи 0.38-0.44 0.09 0.09 x 0.075 0.19 x 0.22 av. 0.3-0.7, 0.6-1 x 0.2-0.4 upto2x0.6 0.1-0.135 0.1 0.15 0125 0.52-0.58 0.18-0.24 0.16 x 0.23 0.24—0.25 0.11=0.126 0.11 0.26—0.3 0.12 0.11-0.135 0.13-0.14 Number of eggs per case or capsule 1-2 18-35 1036-2511 300-346 1390-1723 250-500 600-1600 700-1800 500-1400 70-400 | № AN o AA A 5 dl dl dl dl dl dl dl — Max. number of eggs deposited 11,200 21,750 2,800 157,000 580,000 61,000 625,000 13,450 1,720 15,000 11,250 70,000 >1,000,000 >5,000,000 23,760 117,000 75,600 61,500 4,063,500 DEVELOPMENT OF RED SEA GASTROPODS 261 Period to Egg veliger diameter formation (mm) (d) 75 3—4 200-225 24h 200 8-9 120 -— 210-260 7 410-440 10-11 90 3-4 130 — = 8 240-250 25 180-200 40-45 250 35-38 180 30-32 185-190 30-60 200 — 400-420 45-47 180-200 30-50 80 7-10 92 8-11 200-250 7. 60 TV 65 412 140 8 110-120 6-12 70-90 12 120-170 6 120-160 6% 80 7-9/2 100 6—6 130-140 10 300—330 13—14 65—70 4-52 90-100 5-5% 140 11% 75 45 93 75 100 4-54 200 7 70 7 100 5%-17 100 10 95 4 ТР, planktotrophic; L, lecithotrophic; D, direct development. Temperature of culture (°С) 28 Туре of develop- ment! 4 im Mite ое O awit ра долее ries allie le qe} aes qe) до) a) ime оо) UU UU 0500 00/0050 0 || 00-0 Reference Gohar 8 Eisawy, 1963 Eisawy, 1970 Eisawy & Sorial, 1974a Pers. obs. Gohar 8 Eisawy, 1967a Eisawy & Sorial, 1968 Eisawy & Sorial, 1976b Eisawy & Sorial, 1976b Gohar & Eisawy, 1967a Gohar & Eisawy, 1967a Gohar & Eisawy, 1967a Gohar & Eisawy, 1967b Gohar & Eisawy, 1967b Gohar & Eisawy, 1967b Eisawy & Sorial, 1974b Gohar & Soliman, 1963a Gohar & Soliman, 1963a Gohar & Soliman, 1963a Gohar & Eisawy, 1967b Eisawy & Sorial, 1976a Gohar & Eisawy, 1967b Gohar & Eisawy, 1967b Pers. obs. Pers. obs. Gohar & Aboul-Ela, 1957a Pers. obs. Pers. obs. Pers. obs. Pers. obs. Gohar & Soliman, 1963b Gohar & Aboul-Ela, 1957c Gohar & Aboul-Ela, 1957c Gohar & Aboul-Ela, 1957c Gohar & Aboul-Ela, 1957c Gohar & Soliman, 1967b Gohar & Soliman, 1967c Pers. obs. Gohar & Aboul-Ela, 1959 Gohar & Soliman, 1967d Gohar & Soliman, 1967e Soliman, 1978 Gohar & Aboul-Ela, 1959 Gohar & Soliman, 1967f Pers. obs. Gohar & Soliman, 1967g Gohar & Soliman, 1967g Soliman, 1980 Gohar & Soliman, 1967a Soliman, 1986 Gohar & Aboul-Ela, 1957b 262 SOLIMAN 100 pm 50 um FIG. 2. Early embryology of Red Sea gastropods. А. Hexabranchus sanguineus: spiral cleavage, first quartette of micromeres formed (after Gohar & Soliman, 1963b). B. Chicoreus virgineus: unequal cleavage of egg in a lecithotrophic prosobranch (after Gohar & Eisawy, 1967b). C. Hexabranchus sanguineus: for- mation of mesoderm mother cell (the mesoblast 4d) (after Gohar & Soliman, 1963b). the egg capsule has an exit hole with fixed shape and position. The exit hole remains closed throughout development but opens at hatching to permit the release of larvae or succeeding stages. Empty capsules remain intact with firm walls. No comparable exit holes are encountered in opisthobranchs. In the Red Sea opisthobranch species studied, as development proceeds, the embryonic capsules gradually increase in size becoming DEVELOPMENT OF RED SEA GASTROPODS 263 turgid with extremely thin walls (apparently due to increased intracapsular osmotic pres- sure). This allows for an easy penetration by the hatching stages. In only a few cases did the perforated capsules retain their contour. Generally, however, they become collapsed, deformed or entirely ruptured and so can be barely detected in the jelly matrix. This latter in turn may either remain intact, become wrin- kled, dissociate into fragments or be con- verted into thick mucus. The wide temperature range (16-30°C) and high salinity (around 40%.) of Red Sea waters directly affect the development and larval behaviour of the gastropods studied. In species with extended breeding, the develop- mental time varies much with temperature (e.g. Thais savignyi, 30 d at 28°C, 38 d at 26°C and 45 d at 24.2°C (Eisawy & Sorial, 1974b); Fusinus tuberculatus, 30-32 d at 27°C and 45-50 d at 22°C (Eisawy & Sorial, 1976a); Hexabranchus sanguineus, 6 d at 27°C and 10 d at 23.5°C (Gohar & Soliman, 1963b); Dendrodoris fumata, 5/2 d at 28°C and 17 d at 17°C (Gohar & Soliman, 1967a)). The latter species is interesting since the length of the developmental period varies with the slight thermal changes within the same month: 152 h at 26.2°C, 156 h at 25.6°C and 164 h at 25°C. Being a shore species subject to substantial fluctuations in temperature and salinity, its larvae display remarkable toler- ance to salinity changes (surviving for several days in 30%. and for 40 h in 50%). At hatching, planktotrophic larvae develop for some time marked positive phototaxis, pursuing phytoplankton for food, and negative geotaxis to effect larval dispersal. Thereafter they become positively geotactic, invariably moving near the bottom but without displaying any tendency to metamorphose for reasons discussed later. Lecithotrophic larvae may re- main planktonic for days or hours; they even- tually settle and metamorphose. The newly emerging juveniles of Casella obsoleta, like the adults, are nocturnal in habit (Gohar & Soliman, 1967d). Light has a decisive effect on the degree of pigmentation of the veliger shell, and in turn on the general colour of the spawn mass. Even in the same ribbon of D. fumata, parts exposed to more light appear darker (Gohar & Soliman, 1967a). Light affects the whole pro- cess of development: in the total absence of light it has been shown experimentally that development is retarded or completely inhib- ited. Larval Structure The velum, foot and shell are among the most conspicuous gastropod larval organs which can be of outstanding taxonomic value in prosobranchs. The enlargement and subdivision of the ve- lum into 4, 6 or more lobes is a common char- acter of large prosobranch larvae (of ad- vanced mesogastropods and neogastropods) which helps them meet their needs for buoy- ancy and food (Fig. 3A). A large or subdivided velum is not an indication of a long planktonic existence as is sometimes stated (Gohar & Eisawy, 1967a, in the case of Polinices mel- anostoma). Many such larvae have only a short pelagic life, becoming benthic one or two days after hatching; the velar lobes are eventually resorbed (e.g. Strombus tricornis (Eisawy & Sorial, 1968), Chicoreus ramosus (Fig. 3B, C), Pleuroploca trapezium (Gohar & Eisawy, 1967b), Fusinus tuberculata (Eisawy & Sorial, 1976a)). A multilobed velum is re- ported to exist in the larvae of only one opisthobranch, Philine denticulata (Horikoshi, 1967). In lecithotrophic and directly-devel- oping opisthobranchs in general, the velum is relatively reduced in size and mobility. During metamorphosis, it may take part in the forma- tion of the juvenile rhinophores (Casella ob- soleta, Gohar & Soliman, 1967d). A pedal operculum does not form in di- rectly-developing opisthobranchs. It is lost in early juvenile development in aplysiids (Swit- zer-Dunlap & Hadfield, 1977), or during meta- morphosis in all other opisthobranchs, but in prosobranchs it is only lost in a few non-oper- culate species. With only a few exceptions, the larval shell is dextral in prosobranchs, with 172 to 3 whorls (Chicoreus ramosus, Gohar & Eisawy, 1967b). In opisthobranch larvae, it may be cup-shaped, inflated or incipiently sinistrally coiled (hyperstrophic) with 34-172 whorls. Anomalous larvae possessing large tubular uncoiled shells are commonly observed in those opisthobranchs laying millions of eggs (H. sanguineus, Asteronotus cespitosus (Go- har & Soliman, 1963b, 1967e), Platydoris scabra (Soliman, 1978)). While the larval shell is retained in shelled opisthobranchs, it is cast off during metamorphosis in the re- maining opisthobranch groups. Except for Casella obsoleta and Phyllodes- mium xeniae (Gohar & Aboul-Ela, 1957b), the veliger shells of all other Red Sea opistho- branchs studied belong to type B of Vester- 264 SOLIMAN 1 mm FIG. 3. Larval structure and development of Red Sea prosobranchs. A. Lambis truncata: veliger larva with 6-lobed velum (after Gohar & Eisawy, 1967a). B. Chicoreus ramosus: newly hatched veliger with 4-lobed velum (after Gohar & Eisawy, 1967b). C. Chicoreus ramosus: postlarva showing degeneration of velum during metamorphosis (after Gohar & Eisawy, 1967b). VI, velum. gaard & Thorson (1938) and Thorson (1946). While the larval shell type of P. xeniae was not reported, that of C. obsoleta is of type A. The validity of the latter type was a matter of controversy (Soliman, 1977). It has been re- jected by Thompson (1961) on the basis of its possession only by premature abnormal larvae. Its occurrence in the directly develop- ing species C. obsoleta and Glossodoris si- bogae (Usuki, 1967) was considered as evi- dence for the view that such larval shells are vestigial, pertaining only to capsular devel- opment (Hadfield & Switzer-Dunlap, 1984). However, cup-shaped larval shells have been recently reported from planktonic veligers of two lecithotrophic gymnodorid nudibranchs (Boucher, 1986). The still rare occurrence of this type of larval shell and its primitive con- struction do not preclude its recognition as a valid type. The variable sculpture and shape of proso- branch larval shells can provide a basis for their identification, but this is not possible with opisthobranch larval shells. Among these, only a few have roughened surfaces and they rarely have characteristic patterns (Hurst, 1967). Colour and exact measurements can nevertheless be reliable characters in certain DEVELOPMENT OF RED SEA GASTROPODS 265 rot Le > Car a 50 um FIG. 4. Embryology and larval development of Red Sea opisthobranchs. A. Dendrodoris fumata: early formation of secondary (larval) kidney in gastrula; anal cells in pretorsional position (after Gohar & Soliman, 1967а). В. Dendrodoris fumata: 7/2 d old embryo. Note excretory structures: nephrocyst, secondary (larval) kidney, and excretory vesicles (after Gohar & Soliman, 1967a). C. Hexabranchus sanguineus: newly hatched larva. Note secondary (larval) kidney discharging a large droplet of fluid (modified after Gohar & Soliman, 1963b). D. Chromodoris inornata: 7 d old embryo. Note larval kidney and excretory vesicles with attenuated blunt ends (after Gohar & Soliman, 1967b). E. Chromodoris inornata: newly hatched veliger with separated excretory vesicles discharging droplets of excretory fluid (after Gohar & Soliman, 1967b). AC, anal cells; H, heart; K, secondary (larval) kidney; M, midgut; MD, midgut diverticula; N, nephrocyst; Vc, excretory vesicle(s). 266 SOLIMAN cases (Gohar & Soliman, 1967g; Soliman, 1978). As with the early embryological stages, live opisthobranch veligers are ideal material for studying the internal structure of gastropod larvae, e.g. gut, midgut diverticula, retractor muscle, heart, excretory and nervous ele- ments. A heart is said to exist only occasion- ally in opisthobranch larvae and to have been reported among nudibranchs only for Adalaria proxima (Bonar, 1978). In the present mate- rial, a pulsatile heart has been described in the nudibranchs Hexabranchus sanguineus, Dendrodoris fumata, Chromodoris inornata and Casella obsoleta (with 20-21 beats.min- 1 in the latter) (Gohar & Soliman, 1963b, 1967a,b,d) (Figs. 4, 5D). Among the conspicuous larval excretory structures in many nudibranch species are the nephrocysts (symmetrically placed on the anterolateral aspect), the secondary larval kidney, and the large excretory vesicles (lo- cated on the right side in the close neighbour- hood of the kidney (Fig. 4)). The larval kidney of H. sanguineus is highly distinctive by its deep red colour, and clearly has a neck and aperture through which fluid drops are dis- charged (Fig. 4C). The larval kidney seems to function not only during embryonic and larval life, but also for some time after the juvenile stage is attained (Casella obsoleta, Fig. 5D; Philine denticulata, Horikoshi, 1967). Very lit- tle is known about the excretory vesicles, but the extrusion of hyaline droplets in certain cases (Chromodoris inornata, Fig. 4E) sug- gests they may have an excretory function. Eyes and tentacles are typical of proso- branch larvae. Their presence in newly hatched opisthobranch planktotrophic velig- ers is very unusual (Thorson, 1946). They de- velop 6 days after hatching in Phyllodesmium xeniae (pers. obs.), and some time during the larval phase in aplysiids (Switzer-Dunlap & Hadfield, 1977). Some cephalaspids hatch with only the right eye present (Acteocina canaliculata (Franz, 1971)), the left eye de- veloping a few days later. Eyes are, however, discernible in the veliger stages of leci- thotrophic and directly developing species (Berthellina citrina, Discodoris erythraeensis (Gohar & Aboul-Ela, 1957a, 1959), Trippa spongiosa, Casella obsoleta (Gohar & Soli- man, 1967g,d)) (Fig. 5). The statocysts develop earlier than the eyes. They are virtually the earliest embryonic nervous elements to develop during gastro- pod ontogeny and are retained in adult life. DISCUSSION Based on the studies of Thorson (1946, 1950), Thompson (1967), Mileikovsky (1971) and Todd (1981) and data of the present study (Table 1), the main types of develop- mental patterns among gastropods (applica- ble also to other molluscs) are: 1. Planktotrophic development, with typical veliger larvae feeding during their short or long pelagic existence; 2. Lecithotrophic development, which may be pelagic or non-pelagic; and 3. Direct or capsular development. Each developmental type is correlated with a specific egg size range. In the present ma- terial the egg diameter range for the three types was 60-80 um, 140-440 um and 300-330 um, respectively. This last figure for direct development is, however, based on in- adequate data (just a single species, Casella obsoleta). Certain factors may, however, in- tervene allowing relatively small eggs to go through lecithotrophic or direct development, e.g. rich yolk content, rich albumen content of FIG. 5. Metamorphosis of Red Sea non-planktotrophic opisthobranchs with selected stages of development. A. Discodoris erythraeensis: pelagic lecithotrophy in a dorid nudibranch (modified after Gohar & Aboul-Ela, 1959). From left to right: 7 d old embryo; metamorphosing postlarva with reflected mantle fold and no shell; juvenile. B. Berthellina citrina: non-pelagic lecithotrophy in a notaspidean (modified after Gohar & Aboul-Ela, 1957a). From left to right: intracapsular veliger stage; newly hatched swimming-crawling stage; pediveliger with absorbed velum and enlarged foot; juvenile with internal shell. C. Trippa spongiosa: non-pelagic leci- thotrophy in a dorid nudibranch (after Gohar & Soliman, 1967g). From left to right: intracapsular veliger stage; metamorphosing stage; hatching stage deserting its shell; juvenile. D. Casella obsoleta: direct de- velopment in a dorid nudibranch (after Gohar & Soliman, 1967d). From left to right: intracapsular veliger stage; metamorphosing stage with enlarged foot, subvelar ridge, and reflected mantle fold; embryo, 2 d before hatching, without velum or shell, with anal cells and larval kidney reaching their final detorsional position; juvenile. AC, anal cells; F, foot; H, heart; K, larval kidney; P, reflected mantle fold; R, rhinophore; S, shell; T, tentacle; Vc, excretory vesicle(s); VI, velum; Vs, subvelum. 267 DEVELOPMENT OF RED SEA GASTROPODS 268 SOLIMAN exceptionally large egg capsules, extracapsu- lar yolk, or presence of nurse cells. Clark & Goetzfried (1978) report even smaller egg di- ameters of 91.9 um and 97.7 um, for the as- coglossans Elysia papillosa and Costasiella Шапае which develop lecithotrophically and directly, respectively, being provided with ex- trazygotic food reserves. Extracapsular yolk has been previously described in the spawn ribbons of Chromodoris tinctoria (Gohar & Soliman, 1967c). Here, although the egg is 100 um across, and extracapsular yolk has been shown to be almost depleted before hatching, yet lecithotrophic development was not encountered. Since egg masses were laid in the laboratory only during June and July, animals may proceed to lecithotrophic devel- opment at other periods of the year. The de- velopment of Elysia cauze (Clark & Goetz- fried, 1978) is seasonally variable and is apparently controlled by variable utilization of the extracapsular yolk. It is noticeable, how- ever, that in C. tinctoria, the newly hatched larvae attained a relatively large size com- pared with larvae of other species developing from eggs of the same size but having no extrazygotic yolk. Lecithotrophic development involves a typ- ical veliger stage (which may be the hatching stage) that remains pelagic for a variable pe- riod of time, usually not exceeding two weeks (in Lambis truncata (Gohar & Eisawy, 1967a) (Fig. ЗА); 7 ат Discodoris erythraeensis (Go- har & Aboul-Ela, 1959) (Fig. 5A); 4-6 d in Chicoreus ramosus (Fig. 3B); 2-3 d in C. vir- gineus (Gohar & Eisawy, 1967b); 2 а in Strombus tricornis and 1-2 а in Fusinus tu- berculatus (Eisawy & Sorial, 1968, 1976a)). During their planktonic existence, which pri- marily effects their dispersal, the larvae may, but do not necessarily have to, feed. In non- pelagic lecithotrophic development, the veliger stage is passed intracapsularly, and on hatching already metamorphosing swim- crawling or crawling pediveligers are liberated which shortly attain the young stage (Berthell- ina citrina, Trippa spongiosa (Fig. 5B,C); Cu- thona nana (Rivest, 1978)). It is not uncommon nevertheless to have pelagic and non-pelagic lecithotrophy occur- ring in the same species (e.g. Chicoreus vir- gineus (Gohar & Eisawy, 1967b); Fusinus tu- berculatus (Eisawy & Sorial, 1976a)). In such cases, while the majority of embryos hatch as proper planktonic larvae which start to meta- morphose 1-2 d later, a few, having their hatching delayed (possibly due to culture con- ditions), proceed in development intracapsu- larly emerging as creeping stages. In the third type, the whole development and metamorphosis takes place in the embry- onic capsule. The veliger stage is either nor- mal, although the velum is not well developed (Retusa obtusa (Smith, 1967); Phyllaplysia taylori (Bridges, 1975)), or is suppressed to varying degrees (Casella obsoleta (Fig. 5D); Cadlina laevis (Thompson, 1967)). Bonar (1978) designates the direct type of development with no proper veliger stage as ametamorphic, exemplified by the dorid Okadaia elegans described as having no trace of shell or velum during development (Baba, 1937). This is, however, different from the case of Casella obsoleta (included by Bo- nar among species with ametamorphic devel- opment). In this species the veliger stage pos- sesses a reduced but distinct velum, bearing short cilia and a subvelar ridge, and a cup- shaped shell (Fig. 5D). Because metamor- phosis does not only affect the locomotory and other external organs, but also (particu- larly in opisthobranchs) several internal or- gans including the gut and nervous elements, the use of the term ‘ametamorphic’ in this context is misleading as it implies that there is no process of metamorphosis. It should ap- propriately be replaced by ‘incomplete’ or ‘re- duced’ metamorphosis (i.e. heterometamor- phic). Veliger stages with reduced velar lobes, meanwhile, are not restricted to directly de- veloping species, but have also been re- ported in lecithotrophic species (Cuthona nana (Rivest, 1978)) the ontogeny of which could equally be described as involving re- duced metamorphosis. From the above review, the major factors affecting metamorphosis are, in chronological sequence: food conditions, acquiring compe- tence for metamorphosis, and suitable sub- strata for settlement and metamorphosis. Planktotrophs and pelagic lecithotrophs pass through an obligatory planktonic (precompe- tent) phase for dispersal and feeding (essen- tial for the former category). Therefore, in lab- oratory cultures, such larvae should be supplied with suitable food to maintain their survival until after becoming competent to metamorphose. п Acteocina canaliculata, only the fed larvae normally metamorphose in culture (Franz, 1971; Mikkelsen & Mikkelsen, 1984). Death of larvae, however, is not only a result of starvation but also of infection by bacteria and ciliates. This has been success- fully controlled in laboratories by the use of DEVELOPMENT OF RED SEA GASTROPODS 269 selected antibiotics (Bonar & Hadfield, 1974; Hadfield, 1984), ultrafiltration, and/or boiling of sea water before use. Finally, a suitable substratum is essential for metamorphosis in some species. The proximal cue to settlement is probably the presence of specific chemicals which trigger the onset of metamorphosis (Bonar, 1976; Hadfield, 1984), but the advan- tage of this behaviour is that the settled mol- lusc has an assured supply of food. Prey or- ganisms of the adult have been frequently reported to be necessary to elicit meta- morphosis, while a particular alga must be provided to stimulate settlement and meta- morphosis in aplysiids (Switzer-Dunlap & Hadfield, 1977). The specific substratum could also be associated with certain individ- uals or may provide substances essential for adult life, beside affording optimal conditions for the species. In many species, however, planktotrophic and lecithotrophic larvae, after a period of pelagic existence, normally settle and metamorphose in the absence of a spe- cific substratum (e.g. Discodoris erythraeen- sis (Gohar & Aboul-Ela, 1959); Acteocina canaliculata (Franz, 1971); Pleuroploca tra- pezium (Gohar & Eisawy, 1967a), among others). Other defects in laboratory conditions can possibly also prohibit metamorphosis directly or indirectly. In the present study, rendering the adult’s prey or substratum available to the postlarvae of several planktotrophic species (of which many had already become posi- tively geotactic) was unsuccessful in inducing metamorphosis. This involved the use of the definitive coral species bored by the adult in the case of coralliophilids, dead coral pieces for many dorids, the alcyonarian Sarcophy- tum in the case of Hexabranchus sanguineus (on which the adults feed, at least in part), and the alcyonarian Heteroxenia among whose polyps the aeolid Phyllodesmium xeniae lives. Improving laboratory conditions can in- duce metamorphosis of such larvae develop- ing from large yolked eggs (e.g. Tonna olear- ium (Gohar & Eisawy, 1967a); Thais savignyi (Eisawy & Sorial, 1974b)) which otherwise die a few days (6-12) after hatching, and it can help metamorphosing larvae to complete this process successfully (e.g. Lambis truncata, whose postlarvae often perish before attain- ing the young stage (Gohar & Eisawy, 1967a)). Non-pelagic lecithotrophy and direct devel- opment are thus successful modes of mollus- can development having advantages over planktotrophy and pelagic lecithotrophy. For the former the dangers of free planktonic ex- istence (e.g. mortality due to predation, star- vation, and drifting far from any suitable sub- stratum) are minimized, and no external source of food or a specific substratum for settling and metamorphosing is required. While pelagic lecithotrophic larvae have over- come the food crisis often faced by plank- totrophic larvae, they still share with them these other problems. The danger of failing to find a suitable settling ground is even more critical for them than for planktotrophic larvae, because their length of planktonic life is de- pendent upon their limited yolk supply (Smith, 1967). Non-pelagic lecithotrophs and directly developing species nonetheless have the dis- advantages of limited distribution, possible overcrowding and genetic isolation. The present data agree in general with Thorson's rule (1950) that among benthic in- vertebrates there is an increase in species with pelagic larvae from the poles towards the tropics and equator. Accordingly, among the 50 species of Red Sea gastropods whose on- togeny has been studied, 35 species (70%) have planktotrophic development, 14 are lec- ithotrophic and only one (a nudibranch) has direct development. The percentage of pe- lagic species would appear substantially higher if pelagic lecithotrophic species are taken into consideration. However, within the prosobranchs, the non-planktotrophic species represent a relatively high percentage, i.e. 50% (previously also recorded in the Baha- mas (D’Asaro, 1970)), against only 14.3% for opisthobranchs. This may indicate a tendency to planktotrophy among Red Sea opistho- branchs, and to suppress planktonic in favour of non-pelagic development among neogas- tropods. There are, however, counter views which suggest that ecological conditions in the tropics (Florida, 17-32°C) favour direct development in nudibranchs and Ascoglossa (and probably all opisthobranchs) rather than planktotrophy (Clark & Goetzfried, 1978). While 87% of the nudibranchs studied from our area are planktotrophic, the limited num- ber of species and higher taxa examined do not permit arriving at firm conclusions on this point. LITERATURE CITED BABA, K., 1937, Contribution to the knowledge of a nudibranch, Okadaia elegans Baba. Japanese Journal of Zoology, 7: 147-190. 270 SOLIMAN BONAR, D. B., 1976, Molluscan metamorphosis: a study in tissue transformation. American Zoolo- gist, 16: 573-591. BONAR, D. B., 1978, Morphogenesis at meta- morphosis in opisthobranch molluscs. In: CHIA, Е. $. & M. Е. RICE, eds., Settlement and meta- morphosis of marine invertebrate larvae. Elsevier/North Holland Biomedical Press, New York, p.177-196. BONAR, D. B. & M. G. HADFIELD, 1974, Metamor- phosis of the marine gastropod Phestilla sibogae Bergh (Nudibranchia: Aeolidacea). |. Light and electron microscopic analysis of larval and meta- morphic stages. Journal of Experimental Marine Biology and Ecology, 16: 227-255. BOUCHER, L. M., 1986, Vestigial larval shells in planktonic veligers of two gymnodorid nudi- branchs. Journal of Molluscan Studies, 52: 30— 34. BRIDGES, C., 1975, Larval development of Phyl- laplysia taylori Dall, with a discussion of develop- ment in the Anaspidea (Opisthobranchiata: Anaspidea). Ophelia, 14: 161-184. CLARK, K. B. & A. GOETZFRIED, 1978, Zoogeo- graphic influences on development patterns of North Atlantic Ascoglossa and Nudibranchia, with a discussion of factors affecting egg size and number. Journal of Molluscan Studies, 44: 283— 294. D'ASARO, C. N., 1970, Egg capsules of proso- branch molluscs from South Florida and the Ba- hamas and notes on spawning in the laboratory. Bulletin of Marine Science, 20: 414—440. EISAWY, A. M., 1970, Spawning, development and metamorphosis of Trochus dentatus Forskal. Bulletin of the Institute of Oceanography and Fisheries, Egypt, 1: 379-393. EISAWY, A. M. & A. E. SORIAL, 1968, The egg masses, development and metamorphosis of Strombus tricornis Lamarck. Proceedings of the Malacological Society of London, 38: 13-26. EISAWY, A. M. & A. E. SORIAL, 1974a, The egg masses and development of Turbo radiatus Gmelin. Bulletin of the Institute of Oceanography and Fisheries, Egypt, 4: 221-235. EISAWY, A. M. & A. E. SORIAL, 1974b, Egg cap- sules and development of Thais savignyi De- shayes. Bulletin of the Institute of Oceanography and Fisheries, Egypt, 4: 237-258. EISAWY, A. M. & A. E. SORIAL, 1976a, Egg cap- sules and development of Fusus tuberculatus Chemnitz. Bulletin of the Institute of Oceanogra- phy and Fisheries, Egypt, 6: 215-237. EISAWY, A. M. & A. E. SORIAL, 1976b, Studies on the development of two species of Strombidae from the Red Sea. Bulletin of the Institute of Oceanography and Fisheries, Egypt, 6: 257-274. FRANZ, D. R., 1971, Development and metamor- phosis of the gastropod Acteocina canaliculata (Say). Transactions of the American Microscopi- cal Society, 90: 174- 182. GOHAR, H. А. Е. & 1. А. ABOUL-ELA, 1957a, The development of Berthellina citrina. Publications of the Marine Biological Station, Al-Ghardaga, Egypt, 9: 69-84. GOHAR, Н. А. Е. & 1. А. ABOUL-ELA, 1957b, On a new nudibranch, “Phyllodesmium хетае”. Pub- lications of the Marine Biological Station, Al- Ghardaga, Egypt, 9: 131-144. GOHAR, Н. А. Е. & I. А. ABOUL-ELA, 1957c, The development of three chromodorids. Publications of the Marine Biological Station, Al-Ghardaga, Egypt, 9: 203-228. GOHAR, Н. А. Е. & 1. А. ABOUL-ELA, 1959, On the biology and development of three nudibranchs (from the Red Sea). Publications of the Marine Biological Station, Al-Ghardaga, Egypt, 10: 41- 62. GOHAR, H. А. Е. 8 А. М. EISAWY, 1963, The egg masses and development of Trochus erythraeus Brocchi. Publications of the Marine Biological Station, Al-Ghardaga, Egypt, 12: 191-204. GOHAR, Н. А. Е. 8 A. M. EISAWY, 1967a, The egg masses of four taenioglossan prosobranchs from the Red Sea. Publications of the Marine Biolog- ical Station, Al-Ghardaga, Egypt, 14: 109-148. GOHAR, H. А. Е. & A. M. EISAWY, 1967b, The egg masses and development of five rachiglossan prosobranchs from the Red Sea. Publications of the Marine Biological Station, Al-Ghardaga, Egypt, 14: 215-268. GOHAR, Н. А. Е. & G. М. SOLIMAN, 1963a, On the biology of three coralliophilids boring in living cor- als. Publications of the Marine Biological Station, Al-Ghardaga, Egypt, 12: 99-126. GOHAR, H. А. Е. & G. М. SOLIMAN, 1963b, On the biology and development of Hexabranchus san- guineus (Rüppell & Leuckart). Publications of the Marine Biological Station, Al-Ghardaga, Egypt, 12: 219-248. GOHAR, H. A. F. & G. N. SOLIMAN, 1967a, The biology and development of Dendrodoris fumata (Rüppell & Leuckart). Publications of the Marine Biological Station, Al-Ghardaga, Egypt, 14: 31- 54. GOHAR, H. A. F. & G. N. SOLIMAN, 1967b, The biology and development of Chromodoris inor- nata Pease. Publications of the Marine Biological Station, Al-Ghardaga, Egypt, 14: 77-94. GOHAR, H. A. F. & G. N. SOLIMAN, 1967c, The biology and development of Chromodoris tincto- ria (Rüppell & Leuckart). Publications of the Ma- rine Biological Station, Al-Ghardaga, Egypt, 14: 95-108. GOHAR, H. A. F. & G. N. SOLIMAN, 1967d, The direct development of the nudibranch Casella ob- soleta (Rúppell & Leuckart). Publications of the Marine Biological Station, Al-Ghardaga, Egypt, 14: 149—166. GOHAR, H. A. F. & G. N. SOLIMAN, 1967e, The biology and development of Asteronotus cespito- sus (Van Hasselt). Publications of the Marine Bi- ological Station, Al-Ghardaga, Egypt, 14: 177- 196. GOHAR, H. A. F. & G. N. SOLIMAN, 1967f, The biology and development of Discodoris concinna DEVELOPMENT OF RED SEA GASTROPODS 271 (Alder & Hancock). Publications of the Marine Bi- ological Station, Al-Ghardaga, Egypt, 14: 197- 214. GOHAR, H. A. F. & G. N. SOLIMAN, 1967g, On two rare nudibranchs of the genus Тирра Bergh of different developmental behaviour. Publications of the Marine Biological Station, Al-Ghardaga, Egypt, 14: 269- 293. HADFIELD, M. G., 1984, Settlement requirements of molluscan larvae: new data on chemical and genetic roles. Aquaculture, 39: 283-298. HADFIELD, M. G. & M. SWITZER-DUNLAP, Opisthobranchs. In: TOMPA, A. S., N. H. VER- DONK & J. A. M. van den BIGGELAAR, eds., Reproduction. The Mollusca (WILBUR, K. ed.) volume 7. Academic Press, Orlando & London, p. 209-350. HORIKOSHI, M., 1967, Reproduction, larval fea- tures and life history of Philine denticulata (J Ad- ams) (Mollusca—Tectibranchia). Ophelia, 4: 43— 84. HURST, A., 1967, The egg masses and veligers of thirty Northeast Pacific opisthobranchs. The Veliger, 9: 255-288. MacGINITIE, G. E., 1934, The egg laying activities of the sea hare Tethys californicus (Cooper). Bi- ological Bulletin of the Marine Biological Labora- tory, Woods Hole, 67: 300-303. MIKKELSEN, P. S. & P. M. MIKKELSEN, 1984, A comparison of Acteocina canaliculata (Say, 1826), A. candei (d’Orbigny, 1841) and A. atrata spec. nov. (Gastropoda: Cephalaspidea). The Veliger, 27: 164-192. MILEIKOVSKY, S. A., 1971, Types of larval devel- opment in marine bottom invertebrates, their dis- tribution and ecological significance: a re-evalu- ation. Marine Biology, Berlin, 10: 193-213. NATARAJAN, A. V., 1957, Studies on the egg masses and larval development of some proso- branchs from the Gulf of Mannar and the Palk Bay. Proceedings of the Indian Academy of Sci- ence, 46 (В): 170-228. RIVEST, B. R., 1978, Development of the eolid nudibranch Cuthona nana (Alder & Hancock, 1842) and its relationship with a hydroid and a hermit crab. Biological Bulletin of the Marine Biological Laboratory, Woods Hole, 154: 157- 175% SMITH, S. T., 1967, The development of Retusa obtusa (Montagu) (Gastropoda, Opisthobran- chia). Canadian Journal of Zoology, 45: 737- 764. SOLIMAN, G. N., 1977, A discussion of the sys- tems of classification of dorid nudibranch veliger shells and their taxonomic significance. Journal of Molluscan Studies, 43: 313-318. SOLIMAN, G. N., 1978, The redescription, repro- duction and development of the dorid nudibranch Platydoris scabra. Journal of Molluscan Studies, 44: 151-165. SOLIMAN, G. N., 1980, On the dorid nudibranch Sebadoris crosslandi. Journal of Molluscan Stud- ies, 46: 227-238. SOLIMAN, С. N., 1983, The discodorid nudi- branchs of the northwestern Red Sea. Journal of Molluscan Studies, Supplement, 12а: 179- 184. SOLIMAN, G. N., 1986, The reproduction and de- velopment of the dorid nudibranch Phyllidia var- icosa from the northwestern Red Sea. Proceed- ings of the 8th International Malacological Congress (Budapest, 1983): 255-260. SOLIMAN, G. N., 1987, A scheme for classifying gastropod egg masses with special reference to those from the northwestern Red Sea. Journal of Molluscan Studies, 53: 1-12. SWITZER-DUNLAP, M. & M. G. HADFIELD, 1977, Observations on development, larval growth and metamorphosis of four species of Aplysiidae (Gastropoda: Opisthobranchia) in laboratory cul- ture. Journal of Experimental Marine Biology and Ecology, 29: 245-261. THOMPSON, T. E., 1961, The importance of the larval shell in the classification of the Sacoglossa and the Acoela (Gastropoda, Opisthobranchia). Proceedings of the Malacological Society of Lon- don, 34: 233-238. THOMPSON, T. E., 1967, Direct development in a nudibranch, Cadlina laevis, with a discussion of developmental processes in Opisthobranchia. Journal of the Marine Biological Association, U.K., 47: 1-22. THORSON, G., 1940, Notes on the egg capsules of some North Atlantic prosobranchs of the genus Troschelia, Chrysodomus, Volutopsis, Sipho and Trophon. Videnskabelige Meddelelser fra dansk naturhistorisk Forening, 104: 251-265. THORSON, G. 1946, Reproduction and larval de- velopment of Danish marine bottom inverte- brates with special reference to the planktonic larvae in the Sound (@resund). Meddelelser fra Kommissionen for Danmarks Fiskeri-og Ha- vundersogelser, Serie Plankton, 4: 1-523. THORSON, G., 1950, Reproduction and larval ecology of marine bottom invertebrates. Biologi- cal Reviews, 25: 1—45. TODD, C. D., 1981, The ecology of nudibranch molluscs. Oceanography and Marine Biology, an Annual Review, 19: 141-234. USUKI, |., 1967, The direct development and the single cup-shaped larval shell of a nudibranch, Glossodoris sibogae (Bergh). Scientific Reports of Niigata University, (D) 4: 75-85. . VESTERGAARD, К. & С. THORSON, 1938, Uber den Laich und die Larven von Duvaucelia ple- beja, Polycera quadrilineata, Eubranchus palli- dus und Limapontia capitata (Gastropoda, Opisthobranchiata). Zoologischer Anzeiger, 124: 129—138. MALACOLOGIA, 1991, 32(2): 273-289 LARVAL STRATEGIES OF NUDIBRANCH MOLLUSCS: SIMILAR MEANS TO THE SAME END? Christopher D. Todd University of St Andrews, Gatty Marine Laboratory, St Andrews, Fife KY16 8LB, U.K. ABSTRACT Growth, development and metamorphosis of the planktotrophic larvae of Onchidoris bilamel- lata (L.) were followed in the laboratory at a range of culture temperatures and on a variety of microalgal diets. Successful culture of the nudibranch larvae at 5°C (approximating field tem- peratures) indicated developmental periods in agreement with previous estimations. Thus, pre- dictions of the coincident timing of settlement and metamorphosis of О. bilamellata and the prey (Semibalanus balanoides (L.)) barnacles in the field are upheld. In this respect Todd & Doyle’s (1981) “settlement-timing” hypothesis—as an explanation for the observed larval strategy of O. bilamellata—appears tenable. However, juveniles were observed to subsist on detritus for sev- eral weeks prior to their ability to prey upon S. balanoides. This precludes the validity of inferring a close matching of predator and prey settlement in explaining the specific larval strategy. In the light of other published data on larval/post-larval development, growth and feeding an alternative hypothesis, concerned with selective ‘opportunities’ in the evolution of nudibranch larval strat- egies, is outlined. INTRODUCTION It is apparent, for a wide variety of marine invertebrate phyla (Strathmann, 1978,1985), that reproduction by means of small eggs giv- ing rise to planktotrophic larvae is the primi- tive (or ancestral) mode of development, and that pelagic, and thence non-pelagic, leci- thotrophy are more advanced evolutionary derivatives. Evolutionary re-acquisition of lost larval feeding structures appears to be com- paratively infrequent and we are thus con- fronted with an essentially uni-directional se- quence of events. While there may remain debate over this generalization with respect to particular groups (even the Mollusca as a phylum), there can be little doubt (see Had- field & Switzer-Dunlap, 1984) that such a trend pertains to the subclass Opisthobran- chia. What remain to be ascertained, how- ever, are the selective factors that have dic- tated a shift away from planktotrophy (which requires a more or less extended period of feeding, growth and development of the pe- lagic larva prior to metamorphosis), toward lecithotrophy (in which all reserves necessary for the completion of development of the benthic juvenile are provided within the egg by the parent). At present a consensus ap- pears lacking (see Jablonski & Lutz, 1983; Day & McEdward, 1984; Hadfield & Switzer- Dunlap, 1984; Grahame & Branch, 1985; 273 Todd, 1985a for reviews). Indeed, even if it is accepted that non-feeding larval forms have evolved from planktotrophic counterparts, it is likely that the selective regimes for such evo- lutionary shifts will comprise ‘special cases’ for many particular species. In a previous study concerning the repro- ductive strategy of the Boreo-Arctic dorid nudibranch Onchidoris bilamellata (L.) (Todd & Doyle, 1981), emphasis was placed on the possible significance of the differing egg-to- benthic juvenile periods conferred by the three fundamental larval strategies of plank- totrophy, pelagic lecithotrophy and non- pelagic lecithotrophy (or ‘direct’ develop- ment). Spawning of this specialist barnacle predator occurs at the coldest time of year and our hypothesis highlighted the approxi- mately 3%2-month time gap between peak spawning of the adult nudibranchs (January) and cyprid settlement of Semibalanus bal- anoides (L.) (May), the major prey species. Having a strictly annual and semelparous life- history, these nudibranchs have only the one reproductive opportunity: embryonic and/or larval failure is, therefore, absolute. Of central importance here is the presumably crucial co- incidence of newly-metamorphosed molluscs with the establishment of the smallest phase of the barnacle life-cycle, bearing in mind that settlement of barnacles is restricted (but vari- able) both spatially and temporally. Data then 274 TODD available suggested that only long-term pe- lagic planktotrophy could bridge the gap be- tween the empirically predicted optimal time for adults to spawn and the observed optimal time for the veligers to settle and metamor- phose. Development data for other British dorids indicated that both the pelagic and non-pelagic lecithotrophic strategies would result in juvenile nudibranchs establishing on the shore some weeks in advance of the availability of post-metamorph barnacle prey. It was perhaps surprising to note that pelagic lecithotrophy resulted in by far the shortest egg-to-juvenile interval, and that non-pelagic development was intermediate in duration. Our settlement-timing hypothesis was based on a number of assumptions, foremost of which were the prediction of larval devel- opmental periods in the field (from artificial laboratory culture observations at higher tem- peratures), and the immediate dependence of juvenile O. bilamellata upon the smallest post-metamorphic barnacles as prey. Criti- cisms of the original report (Grant & William- son, 1985) were defended (Todd, 1985b) on the strength of available information while, in- dependently, yet further specific reservations as to the validity of the principle were also being expressed (e.g. Hadfield & Switzer- Dunlap, 1984; Strathmann et al., 1984). Prior to this, more detailed evaluations of the lar- val and post-larval development of O. bila- mellata had been initiated, and it is upon these that | report here. My primary objec- tives were to determine the duration of the pelagic phase at ambient field temperatures (~ 5°C), and thereby to obtain further obser- vations of post-larval dependence on barna- cle spat. (Previous culturing had resulted in post-metamorph dorids in advance of S. bal- anoides settlement in the field.). | also exam- ined the developmental effects of particular algal dietary species on growth and meta- morphosis success in the laboratory. Culture conditions are by definition artificial (espe- cially in terms of algal species and concentra- tions thereof) and the pitfalls of extrapolation to the field situation are self-evident. Never- theless, by rearing larvae on a range of mono- cultures and combinations of phytoplankters ecologically realistic predictions may be made. | show here that the original hypothesis does not provide an adequate descriptor of the behaviour of the nudibranch, but offer an alternative model for nudibranchs which cen- tres upon larval and post-larval nutrition. It should be emphasized that this hypothesis explains only certain adaptive features of nudibranch reproductive strategies. It does not in itself provide an all-embracing frame- work of selection for particular larval types, which (if tenable) would also require an ap- praisal of the bioenergetic constraints and genetic implications of particular life-cycle, life-history and larval strategies (Todd, 1985a, 1987; Havenhand & Todd, 1988a,b,c; Todd & Havenhand, 1988, 1990; Todd et al., 1989). MATERIALS AND METHODS Larval culture of Onchidoris bilamellata has been undertaken from spawn masses depos- ited in the laboratory by field-collected adults. Throughout spawning, the nudibranchs were maintained on Semibalanus balanoides at ambient field temperatures. Culture methods are outlined elsewhere (Todd & Havenhand, 1984), but the salient features are зитта- rized here. All flagellate larval diets were raised from inocula obtained from the Cam- bridge Collection of Algae and Protozoa, with the exception of /sochrysis galbana Parke, which was supplied by SMBA, Oban. Other algae employed were Rhodomonas sp., Pav- lova lutheri (Droop) and Tetraselmis sp. Lar- vae were reared in glass beakers of 250- 1000 т! volume, according to the number of veligers present, at an approximate concen- tration of 3 larvae.ml-1 and a total algal con- centration of 50 cells ul *. Where mixtures of algal species were provided as the larval diet these were presented in equal numerical pro- portions. This is particularly pertinent for Rhodomonas which, at approximately 15 ¡ym diameter, is much the largest of the species used. Larvae were cultured in 0.22 ¡um filtered seawater with the antibiotics Streptomycin sulphate and Penicillin G (50 and 60 g.ml ' respectively) added to control any bacterial and ciliate infestations. Cultures were changed every 5 days by concentrating the veligers in a mesh-bottomed filter and pipet- ting them into freshly prepared beakers. All items of glassware were washed in hot fresh water only, or autoclaved, and at no time were detergents or disinfectants used. Temperatures of the larval cultures (5, 10, 15 and 18°C) were controlled to within 0.2°C by immersing the vessels in thermostatically controlled water-baths and all were subjected to constant illumination in order to preclude possible complications of variable photope- LARVAL STRATEGIES OF NUDIBRANCHS 275 SHELL LENGTH, pm 25 35 DAYS POST-HATCHING 45 55 65 75 85 FIG. 1. Growth and development of the planktotrophic larvae of Onchidoris bilamellata in laboratory culture on a 1:1:1 mixture of the flagellates Rhodomonas, Isochrysis and Pavlova at 5°C and 15°C. Mean (with 95% confidence limits), maximum and minimum shell lengths are shown at each change of medium. Occurrence of first metamorphosis is indicated by arrows. riod. The flagellate diets were, however, all raised at room temperature (= 20°C), a factor which may be of some importance to the colder larval cultures (see below). In view of our previous lack of success in precluding ‘rafting’ of the larvae in the surface film (Todd, 1981; Todd & Havenhand, 1984), no such preventive steps were taken. Instead, entrapped larvae were resuspended by pipet- ting small drops of water onto the culture sur- faces; this was undertaken at least once daily. ‘Rafting’ was usually only a problem in the early periods of development, when upward swimming is particularly marked. Periodic measurements of larvae were made to the nearest 3 um with between 10 and 20 veligers sampled for this purpose. All mea- surements are of the maximum shell dimen- sion taken from the aperture lip. ‘Compe- tence’ to metamorphose is visibly assessable from the overall size of the veliger, the pres- ence of eyes, the larval ‘heart’, a well-formed propodium, and the ability of the larva to crawl across a substratum. Once pediveligers were detected within a culture, subsamples were removed to glass dishes containing live adult Semibalanus balanoides (or S. crenatus (Bru- guière)). If competent, the pediveligers gen- erally commenced metamorphosis within a few hours. Further observations of post- larvae were made by maintaining these at 8°C (12 h light, 12 h dark) in plastic petri-dishes, within which field-collected cyprids of S. bal- anoides had previously been triggered to metamorphose. The SEM preparations of S. balanoides plates were critical-point dried and gold sput- ter-coated in the standard manner, and were photographed on a JEOL JSM-35CF scan- ning electron microscope. RESULTS The initial success in rearing the larvae of this nudibranch species (Todd, 1981) was ob- tained in cultures containing a 1:1:1:1 mix of Isochrysis, Pavlova, Rhodomonas and Tetra- selmis. Subsequently only the first three flagellates have been used, either as mono- cultures or equal mixtures (total concentration 50 cells pl *). The selected algal concen- trations appear to promote maximal growth and metamorphosis success in a range of opisthobranch species (e.g. Chia & Koss, 1978; Bickell & Kempf, 1983). Fig. 1 shows 276 TODD the growth and development of O. bilamellata larvae maintained on 1:1:1 mixtures of /so- chrysis, Pavlova and Rhodomonas at 5°C and 15°C: several striking similarities and con- trasts are apparent. First, larvae maintained at both temperatures showed qualitatively similar sigmoid growth curves (a feature prob- ably characteristic of opisthobranchs [see e.g. Perron & Turner, 1977; Bickell & Chia, 1979; Bickell & Kempf, 1983], bearing in mind the geometry of shell growth), and attained simi- lar sizes at metamorphosis. (A cessation of shell, but not tissue, growth is generally noted some days before development of the propo- dium, and competence to metamorphose.) Second, larvae at the lower temperature (ap- proximating to ambient field conditions (see Todd, 1985b)) developed at a very much slower rate: 79 days at 5°C versus 31 days at 15°C. Third, in both cases there is consider- able variation in size at a given age, and hence individual growth rates, within each culture. Between-culture variation in growth and successful completion of development is in- evitable (see e.g. Pechenik & Lima, 1984, and references therein), particularly at lower tem- peratures where development is so pro- longed. But of greater concern, particularly when evaluating the efficacy of differing di- etary regimes, is the invariably high within- culture variation. This will be due, in part, to inherent differences amongst the larvae, but the major source of the variance is undoubt- edly experimental. Rafting is almost certainly responsible for much of the observed reduc- tion in growth for many larvae. For example, larvae reared on a mixture of /sochrysis and Rhodomonas show, at any age, marked di- vergences in overall size and in the colour of the left digestive diverticulum: small slow- growing larvae are invariably green, while the larger fast-growing larvae have dark-red di- gestive glands. The former are undoubtedly veligers which have persistently become en- trapped and which encounter difficulty in ob- taining sufficient food. Moreover, Rhodomo- nas, which is a larger, less motile flagellate, tends to precipitate to the bottom of still cul- tures and is of markedly reduced availability to rafted veligers. Nevertheless Rhodomonas alone can promote growth and development equal, or even superior, to that in mixtures (see below). Because development rates are usually expressed in terms of time to first metamorphosis, it is perhaps ecologically valid to compare growth in terms of the fastest growing individuals, rather than the notional ‘average individual’. Certainly, it is usual to note a rapid increase in minimum sizes, in the later stages of development, due to the de- mise of slower-growing individuals and/or those that persistently became entrapped. Fig. 2 summarizes the successful culture, through to metamorphosis, of O. bilamellata at a range of temperatures and on a variety of dietary regimes. It should be emphasized that the majority of cultures were attempted at 5°C and the presented data relate only to those cultures in which growth and development were seen to proceed ‘normally’. Data for many other cultures in which survivorship, growth and metamorphosis success were considered unsatisfactory (or were not at- tained), have not been included. Attention should also be drawn to the extent of the pe- lagic phase: even assuming no inherent mor- tality, the fact that only ~ 90% of larvae can be successfully transferred at each change of culture medium results in an 80% loss of veligers over, say, 11 weeks of rearing. De- spite the incompleteness of the data sufficient observations are available to make some comment on the effects of both diet and tem- perature. Effects of algal diet In general, mixtures of flagellates, even of only Rhodomonas and Isochrysis, promoted the highest growth rates and greatest meta- morphosis success. Nevertheless, based upon these (and other) cultures it is apparent that Rhodomonas alone is almost equally ef- ficacious and, indeed, routine culture of meta- morphs is now undertaken on Rhodomonas monocultures. Even in mixtures, larvae evi- dently ingest and digest Rhodomonas more than other algae—veligers frequently regurgi- tate this flagellate when being measured on glass slides, and it colours the digestive di- verticula dark red. Whether the above obser- vations arise from differential selection or availability remains unclear, although the former appears more likely. Two other obser- vations are perhaps substantive; first, larvae reared on monocultures of Pavlova (at all temperatures) never achieved competence, and second, larvae reared on /sochrysis alone were only successfully raised to meta- morphosis on one occasion (at 5°C). Larvae on Pavlova invariably grew well, but devel- oped very dark concretions in the left diges- tive diverticulum some time prior to death at a LARVAL STRATEGIES OF NUDIBRANCHS 277 ] RHODOMONAS, PAVLOVA, TETRASELMIS, ISOCHRYSIS G 2 RHODOMONAS, ISOCHRYSIS 11 10 9 6 4 RHODOMONAS ONLY 12 8 5 RHODOMONAS, ISOCHRYSIS, PAVLOVA 7 90 © ® DAYS POST-HATCHING 5 10 ISOCHRYSIS ONLY 15 18 TEMPERATURE °C FIG. 2. Time to first metamorphosis of Onchidoris bilamellata larvae in culture at a range of temperatures and dietary regimes. pre-competent stage. Such concretions were also observed in larvae from ‘mixed’ cultures containing Pavlova, and for this reason use of this flagellate was discontinued. The general inadequacy of /sochrysis was manifest in sur- vivorship, growth and metamorphosis suc- cess. For /sochrysis monocultures at 15°C growth and development appeared to pro- ceed normally. Eyed veligers were noted after 25 days of culture, cessation of shell growth between 25 and 30 days, and propodial de- velopment after 30 days. Larvae were reared for a further 31 days, during which time they were never observed to crawl and would not metamorphose. Moreover, many larvae (which had completed shell growth) continued 278 TODD —-1.5 log (days 345 350 355 360 эк x 10° FIG. 3. Arrhenius plot of the data from Fig. 2. The О.о is derived from the fitted regression equation. to grow somatically, with the tissues finally bulging from the shell. At 10°C, on /sochrysis alone, the veligers grew well and rapidly, de- veloped eyes within 26 days, propodia within 29 days and commenced crawling within 36 days. Nevertheless, metamorphosis was never achieved and larvae either died or evacuated the shell spontaneously. It there- fore remains possible that /sochrysis is an ad- equate (if not ideal) diet at low temperature, but at higher temperatures its biochemical composition and nutritive value are radically or critically altered. Effects of temperature Fig. 3 shows the conventional Arrhenius plot for the data in Fig. 2. Several points re- quire emphasis here: first, no culture at a tem- perature below 5°C proved successful. Sec- ond, only the one culture was attempted at 18°C (a temperature probably at the physio- logical limit for this species (Todd, 1979a)), and third, there is considerable between-cul- ture variation—even at the same temperature and with the same diet (see, for example, Cul- tures 9 and 11, Fig. 2). Nevertheless, least squares regression analysis for these data (comprising a range of dietary regimes) shows a very significant relationship (Р < .001), from which the Q,, is derived as 2.40. Undoubtedly a more complete data set is nec- essary to properly distinguish this quotient, but it is perhaps relevant that the Q,, for em- bryonic development for O. bilamellata (upon which basis the pelagic phase duration at field temperatures was previously predicted) was found to be 2.34 (Todd & Doyle, 1981). De- spite possible dietary inadequacy, it is clear that at field temperatures (~ 5°C) the embry- onic and larval developmental phases would concur with the predictions made initially (Todd & Doyle, 1981), and that thus far the settlement-timing hypothesis appears at least tenable. That is, with peak spawning in mid- January, embryonic (pre-hatching) and pe- lagic larval development would require a total of (39 + 73 =) 112 days, resulting in peak larval settlement by early May. Our initial es- timation of the larval period in the field (based LARVAL STRATEGIES OF NUDIBRANCHS 279 on a cultured pelagic phase of 32 days at 15°C, corrected by an observed embryonic Q, of 2.34) was 69 days. Observations of post-larval development Precise timetables for post-larval ontogeny and development toward the functional pred- atory juvenile cannot be ascertained; the fol- lowing is a composite summary of observa- tions of post-larvae reared on various larval diets. At the completion of metamorphosis (when the mantle is fused anteriorly and pos- teriorly, and the anus has adopted its defini- tive medial posterior position) the dorsum is both tuberculate and spiculate, but the rhino- phores and gills are lacking. Mantle length is ~ 0.6 mm. The rhinophores are differentiated at 0.85-0.90 mm mantle length, but the gills only become evident at ~1.7 mm length (ap- proximately one month post-metamorphosis). Throughout this first month of growth and continued development no predation on bar- nacle cyprids or spat has been noted. Never- theless, juveniles were seen to be consis- tently (if not exclusively) associated with the lateral calcareous plates of juvenile S. bal- anoides, in a manner suggestive of thigmot- actic ‘refuging’ behaviour. Pigmentation of the digevuve gland (attributable to the larval di- etary flagellates) is progressively lost over the first few weeks of benthic life and is suc- ceeded by a uniform green-brown coloration. This, in turn, becomes less visible as the mantle tissues thicken. Close inspection of the dorids showed that the buccal mass is, in fact, functional from very early on, and that rather than simply refuging against the barna- cles the juvenile nudibranchs were actually grazing on diatoms and/or detritus from the plate surfaces. Similar feeding was subse- quently observed on field-collected plates of dead adult S. balanoides, which are invariably colonized by a considerable microflora. How- ever, metamorphosis will only occur following contact with live barnacles. Figs. 4 and 5 il- lustrate a portion of the calcareous plates of a laboratory-metamorphosed $. balanoides, and here can be seen a radula tooth presum- ably lost by a juvenile О. bilamellata which had been consistently associated with that barnacle. The dorid Cadlina laevis undergoes non- pelagic lecithotrophic development and hatches as a fully-formed juvenile at = 0.8 mm length. ‘Growth’, by up to 0.2 mm over the first 10 days of benthic life in the absence of FIG. 4. SEM of the lateral calcareous plates of a metamorphosed Semibalanus balanoides (aper- ture plates to right) with which a juvenile Onchidoris bilamellata had been associated. Scale: 100 um. feeding, was reported by Thompson (1967). However, Cadlina juveniles continue to sub- sist on stored yolk which is externally visible by its opacity. Indeed, feeding on the defini- tive poriferan diet (Halisarca dujardini (John- son)) will only proceed after the complete ex- haustion of these reserves, perhaps up to 3— 4 weeks post-hatching (pers. obs.). The smallest O. bilamellata to be seen to penetrate the valve-plates of S. balanoides and consume the barnacle tissues measured 1.9 mm (approximately 4-6 weeks post- metamorphosis), and there is no doubt that the juvenile dorids are incapable of tackling live prey up to this time, but choose to graze the surfaces of the calcareous plates. Clearly, therefore, this extended obligatory period of 280 TODD A à = RN FIG. 5. SEM detail of radula tooth of Onchidoris bilamellata arrowed in Fig. 4. Scale: 10 рт. detrital grazing—preparatory to stenopha- gous predation on the definitive barnacle diet—precludes the necessity to infer a close matching of settlement-timing between pred- ator and prey in accounting for the observed ecological association and the predator repro- ductive strategy. Thus, the settlement-timing hypothesis is inappropriate. DISCUSSION Successful laboratory culture of plank- totrophic nudibranch veligers has been de- tailed for 11 species (see Hadfield & Switzer- Dunlap, 1984), but perhaps the most elegant and comprehensive studies of opisthobranch larval biology concern the tropical aeolid Phe- stilla sibogae (Harris, 1973, 1975; Bonar & Hadfield, 1974; Hadfield, 1977, 1978, 1984; Bonar, 1978a,b; Hadfield & Scheuer, 1985; Kempf & Hadfield, 1985; Hirata & Hadfield, 1986; Miller & Hadfield, 1986; Yool et al., 1986). This species hatches as a pelagic lec- ithotrophic veliger which may metamorphose without feeding within 1—2 days of release from the benthic capsule. Furthermore, larvae of Phestilla will ingest and digest flagellates, if available, and this led Kempf & Hadfield (1985) to use the term “facultative planktotro- phy” to distinguish this form of larval behav- iour from what would be conventionally un- derstood as a truly pelagic (obligatory) lecithotrophic strategy. In this respect Phes- tila sibogae and the British dorid Adalaria proxima are very similar. Both hatch from in- termediate-sized eggs, undergo an obligatory 1-2 day (‘pre-competent’) period, will meta- morphose (with or without prior feeding) on contact with the live adult prey, and can delay metamorphosis in the absence of this cue (Thompson, 1958; Kempf & Hadfield, 1985; Kempf & Todd, 1987; Todd et al., 1991). A survey of the literature shows that re- markably few phytoplankters have been used in the culture of opisthobranch veligers, and that /sochrysis galbana (often in combination with another flagellate or a diatom) features particularly prominently. It is clear that differ- ent larval diets yield strikingly different devel- opmental outcomes (see e.g. Pilkington & Fretter, 1970; Lucas & Costlow, 1979 for prosobranchs; Switzer-Dunlap & Hadfield, 1977; Chia & Koss, 1978 for opisthobranchs). Interestingly, Switzer-Dunlap & Hadfield (1977) found Pavlova lutheri to confer the highest growth and survival in sub-tropical anaspideans, but also noted /sochrysis gal- bana to be quite suitable. Similarly, Chia & Koss (1978) also found Pavlova and Isochry- sis to provide the best results, and encoun- tered success with other (unspecified) organ- isms. It is relevant, therefore, that for O. bilamellata, Pavlova was found to be totally unsuitable and /sochrysis of only limited effi- cacy, with Rhodomonas so markedly supe- rior. Care should, therefore, be taken in ex- trapolating such observations of growth, survivorship or development to the field. Notwithstanding the above, the present de- velopmental data uphold the original predic- tions with respect to the duration of the pe- lagic phase of O. bilamellata. While not overstating the case it is perhaps noteworthy LARVAL STRATEGIES OF NUDIBRANCHS 281 that the presently derived Q,, for the larval stage is remarkably close to that previously determined (Todd & Doyle, 1981) for the intra- capsular embryonic phase. This may not be a trivial result, especially if it proved to be char- acteristic of opisthobranch development. Em- bryonic development data are not difficult to obtain and, on the strength of only a single successful larval culture on a mixture of flagellates and at a realistic temperature, it may be possible to confidently predict the nat- ural egg-to-juvenile period. The extended 4-6 week obligatory period of post-metamorphic detrital grazing in O. bi- lamellata clearly confounds the criteria for support of the settlement-timing hypothesis. Indeed, intermediate detrital feeding appears to be widespread—if not actually predom- inant—amongst those species for which developmental data are available. Thus, Doridella obscura obligatorily grazes detritus for up to 5 days, before the juveniles (~ 1 mm) handle Membranipora crustulenta, the definitive anascan bryozoan diet (Perron & Turner, 1977). D. obscura attains some 230 шт in length at metamorphosis (Table 1) and it is thus curious that its congener D. steinber- gae (210 am) does not apparently feed at all for the first three days post-settling, but there- after handles the adult diet Membranipora spp. (Bickell & Chia, 1979; Bickell et al., 1981). For the small, short-lived aeolid Tenel- lia pallida, Eyster (1979) recorded feeding of juveniles on “debris” from hydroid surfaces, but adults preying directly upon Eudendrium. My own observations at field ambient tem- peratures include obligatory feeding of post- larval Onchidoris muricata (Müller) and Ad- alaria proxima (Alder & Hancock) (Todd & Havenhand, unpublished; cf. Thompson, 1958) on detritus for perhaps 1-3 weeks prior to their being capable of handling Electra pilosa zooids. Furthermore, Archidoris pseu- doargus (Rapp) post-metamorphs also graze detritus and microalgae for an as yet unspec- ified but certainly prolonged period. Although competent larvae of Archidoris may metamor- phose (Todd 8 Havenhand, 1984) in the pres- ence of the adult prey sponge, Halichondria panicea (Pallas), recent observations (Todd & Davies, unpublished) show that this sponge is not the metamorphosis trigger. Pediveligers are most reluctant to crawl on, or otherwise associate with, this heavily-spiculate sponge and may well subsist on detritus for an ex- tended period, not dissimilar to O. bilamellata, before taking the definitive prey species. Despite the above findings there are nu- merous records of post-metamorphs not tak- ing any intermediate dietary material before handling the definitive adult prey (Table 1). Relative sizes at metamorphosis are almost impossible to compare inter-specifically, due to the lack of mass measurements. Length data are, however, available which, albeit im- precisely, permit some contrasts to be drawn. Table 1 shows that there is remarkable simi- larity of post-larval sizes, but three species are exceptional: Tritonia diomedea attains perhaps 440 um and O. bilamellata 470 wm at metamorphosis, while Cadlina laevis (non- pelagic lecithotrophic) measures approxi- mately 800 um at hatching. Moreover, corre- lations between metamorph size, whether or not intermediate ‘detritus’ grazing is under- taken, and adult prey type are also apparent. Thus, species in which grazing does not oc- cur prior to specialist predation include cni- darian (7. diomedea, T. hombergi, P. melano- branchia, P. sibogae, C. salmonacea), and spiculate (Rostanga) or slime (Cadlina) sponge associates. Melibe leonina juveniles attack ciliates and subsequently microcrusta- cea (as do adults), but this is a highly special- ized species. Those which clearly do graze detritus as an intermediate diet include the bryozoan grazers (D. obscura, A. proxima, O. muricata) and the one barnacle predator (О. bilamellata). Data for Archidoris pseudoargus are clearly at variance with Rostanga, as are data for Tenellia with Phestilla spp. Neverthe- less, Tenellia is very small (= 150 um) at metamorphosis and Eudendrium is probably a well-defended prey item to this small aeolid. The conclusion from these data is that with the exception of D. steinbergae, those spe- cies which encounter considerable (perhaps overwhelming) prey-size constraints appear to undertake a more or less extended period of post-larval feeding (and growth) on detritus prior to switching to the definitive prey. Cer- tainly bryozoan zooids and barnacles present few problems to the adult forms, but to the meiofaunal-sized juveniles the size differen- tial is enormous (see e.g. Bickell et al., 1981: their Plate 10, ‘inset’). On the strength of the foregoing, and in ac- knowledging the redundancy of the settle- ment-timing hypothesis, | offer the following argument to account for the evolutionary ‘op- portunities’ and constraints for selection away from the ancestral state amongst nudi- branchs. Fig. 6 provides a schematic sum- mary. TODD 282 ‘dds eiodiuesqway Alesedse Ayunyew 'sueozoAig O} AM У-6 [Pe]ON wroız= (0.51-21) P92-s2 eebiequieys виериоа 6/61 ‘elUD 3 119x918 ejue/nsnio PJOdIUEIQUEN 1161 Анеюэд$э “JOUIN| Y UOMO ‘542020418 р 9г ps se им 05е= (9.SZ) P 6 EINISIO 2/|эриоа Buiyoyey Buimol|o} alydo1jou}I98] Spio1pAu ((uosdwus) 1/61 “SSION oıbejad-uoN spioupAy Ajqeqoid eyep ON UO Spee} ‘ON вер ON — P99PUOU/ES eJJeydA101 ‘sqo 'sıad 91ydo1J0yy99] ıuıpselnp евэлезуен [1104 uo ‘1961 ‘uosdwoy| oıbejad-uoN Ajuo ‘ue19J104 JK G-p SYOOM £-2] ON und 008= — SIA8E] ви/ре) salsads oiydosoy4ue|d eeoiued SYoOM 7861 JO, 9618] вириоцоиен jeıanas ‘риециален Y PpOL ‘un Qs} azıs 663 ÁJUO ‘ue19}104 JAZ Aiqeqoid ‘san un 005= (9.01) P Z€ snBeopnasd s110pIy91Y esoJid 819913 "540 'sıad A\jeioedsa SHO9M ‘8S6L 'wosdwoyj эчдодоциуэв| эбеез ‘sueozoAg OW 01-6 e-1 'seA шт 00€— (9.01-8) P 2-1 ешихола виверу 299U919/9H S}UBWLWOD Aaid aniyiuyeq ay9Á9-ay17] [poued 9715 JIyJuag aseud oibejad $915э4$ Suipaaj-uou] pouad + Buizes6 ¡eyuag ‘papnjoul uaaq элец эаеиеле эле зиоцеллэзао pajiejap цощм 10} seidads asoy] ÁjUO ‘зэюэ4$ youelqipnu jo эбие! e 10}; ефер |елле|-1з0о4 pue эцаиэбоио jo Алешитб “| 3718V1 283 LARVAL STRATEGIES OF NUDIBRANCHS 2961 ‘uosduiou | 1161 ‘SMOIIIM 3 ¡dway 6/61 ‘181SA3 8/61 'ssoy $ BIUD 9/61 ‘6/61 ‘зшен $161 ‘6/61 ‘зшен 7861 ‘PUBUUSAEH $ PPOL 1861 ‘e140q 3 PPOL ‘1861 ‘PPOL 5861 ‘due 3 |194919 1861 'PPOL эчалошеэш Jeinsdeg [2914041 [2914041 виверу ‘0 Jaded sıyı ‘ pooy,, 1210 anbıun sisoudiowejJeu s196611) Byejnaiuab eljago wineybip LUINILOAD|yY Кио ‘ueweuoho\y sueade¡njeuuad SNOLIBA ‘ds wnupuapny pyeuuad вбиод$е//чао Ajuo ‘иелаоа ‘dds зао“ 'SIEI09 ‘dds в/Ицаолриаа ‘S|2109 esojid 21198/3 A\ye\oadsa 'sueozoAig snuejeqiwas Aıleıoadsa ‘sajoeusreg SUE99P}SN19019IU1 ‘uoyyue|doo7 eunjd eluaydoe¡Dy pioipAH Аг ¿¡enuuy syaom Me) Y élenuuy ош Spy OW sp ош 01-6 OW 01-6 eyep ON jenuuegns Ajqeqold [paye]s jou] ON [р $] ON proJpÁy uo пидар UO бирээ; элвиз]ха ‘SOA [paje]s jou] ON ejep ON ejep ON SHOOM 5—г sdeued ‘sa, SHOOM 9—+ ‘SOA [р £-2] ON ejep ON шт 0у8= wr Opp= шт OS} ~ шт 092— шт 00€— un Gaz un 00€— wn 0/9= wri Gee~ un вуё= (9.01-8) р 2-1 (9.21 =) р Lb-p€ (9.5101) р 07-65 (092-2) р 2-1 (992-2) P 8 (9.01) P 69-89 (9.9) P OZ (Osr1-z1) р 85-08 (9.21-01) P b> IBsaquioy eluo}11 варэшо!р ешо ври/еа enjoua eıyaınd ебие]504 эебод! e||}S8Ud вциелдоие|эш BIINSOYd BJEIUNW зиорцэио ве//эше!!4 SUOPIYIUO вишиоа! agılaW jueuey snyouesqng 284 TODD = Rostanga pulchra No E prey-size —L Tritonia hombergi VELIGER constraint Le Pl Sp Cadlina laevis ‘POST LARVA! a P + DG Onchidoris bilamellata EMBRYO LL. Pe a y . —L +DG Adalaria proxima constraint Sy FIG. 6. Schematic summary of the relationship between post-larval prey-size constraints and reproductive strategy ‘opportunities’ for evolution away from the primitive, or ancestral, status of planktotrophy amongst nudibranchs. It is assumed that the potential for detritus-grazing by post-larval planktotrophs has always remained, but may not be expressed where it is not required. (P: planktotrophy; L: (pelagic) lecithotrophy; D: direct (non-pelagic) development; D [struck through]: direct development not supportable; + DG: plus detrital grazing). Assumptions 1 The production of small eggs hatching as pelagic planktotrophic larvae is the primitive or ancestral condition, as is detritivory by the immediate post-meta- morph. Pelagic lecithotrophy is a consequential derivative from 1 (above) and is attained essentially by increasing the nutritive (yolk) reserves and protection of the em- bryo. Pelagic lecithotrophic larvae ap- pear otherwise very similar to compe- tent planktotrophs. Non-pelagic lecithotrophy—whether as capsular metamorphosis (e.g. Aeoli- diella alderi, Tardy, 1970; Tenellia pall- ida, Eyster, 1979), or truly vestigial, in- tra-capsular development (e.g. Cadlina laevis, Thompson, 1967)—is a deriva- tive of 2., and С. laevis represents the extreme of embryogenesis, i.e. opposite to 1. (See Todd, 1981; Hadfield & Swit- zer-Dunlap, 1984 for qualifying reviews and discussion of the above.) Planktotrophy is a highly conservative mode of development. It is displayed by the overwhelming majority of nudi- branch species. There is considerable intra-specific vari- ation in egg-size (see Todd, 1987) and this provides scope for at least the initial stage on the path to establishing leci- thotrophy. . The primary function of pelagic larvae is not necessarily dispersal (Strathmann, 1978,1985; Todd, 1985a; Todd et al., 1988): rather dispersal, which may or may not be advantageous to particular organisms, should be viewed as an un- avoidable consequence of the ancestral larval strategy. . Opisthobranch larvae, as opposed to prosobranchs, apparently cease growth on attaining competence (see Kempf, 1981; Pechenik & Lima, 1984) [possibly related to biophysical size constraints in detorting?]: nudibranch metamorphic size potential therefore seems more or less specifically fixed. . Nudibranchs of all developmental strat- egies are characteristically of broadly similar post-larval sizes; even Cadlina laevis at 800 ¡ym is small by contrast to, for example, many of the larger muricid prosobranch hatchlings. Almost without exception, nudibranch embryos are pro- vided only with zygotic yolk (but see Boucher, 1983). Conjecture A. If no post-metamorphic prey-size con- straints apply, the ancestral planktotrophic LARVAL STRATEGIES OF NUDIBRANCHS 285 pattern may well suffice for establishment of the benthic phase (e.g. Tritonia diomedea, Phestilla melanobranchia). B. If such prey-size constraints do apply, some increase in post-larval size may derive from extended planktotrophy (as shown by O. bilamellata), but this alone may Бе inade- quate: in such cases (e.g. O. muricata) an intermediate diet is expedient. Nudibranchs are typically specialist predators. If such a pu- tative intermediate diet were another inverte- brate this scenario would require two suitable prey species to be consistently and reliably sympatric and adjacent, because post-larvae lack both the reserves and motility to under- take extensive searching. Furthermore, which species (intermediate or definitive?) should comprise the metamorphosis stimulus? Se- lection ought to favour specific cueing to the definitive prey, and thus detritus perfectly fits the intermediate requirements if only due to its ubiquity and non-specificity. C. Neither detritivory, nor microalgal graz- ing, demand morphological or physiological specializations—the larval gut is, after all, adapted for phytoplanktivorous microphagy (Bickell & Chia, 1979; Bickell et al., 1981; Bickell & Kempf, 1983) and, with the present exception of Melibe, post-larval stages bear a radula. In essence, post-larval detritivory by planktotrophic forms necessitates only an on- togenetic delay in the reorganization to ac- commodate the carnivorous status. Evidence Here, | confine my argument to those spe- cies from the British Isles with which | have previous experience: these embrace the full spectrum of fundamental larval strategies. 1. Onchidoris muricata. Following meta- morphosis, this species encounters size constraints in handling Electra pilosa. Planktotrophy plus post-larval detrital feeding appears to suffice, and the an- cestral larval form is retained. 2. Onchidoris bilamellata. As outlined and discussed above this species has criti- cal juvenile prey-size constraints. Direct development would not yield hatchlings sufficiently large to handle barnacle spat and, furthermore, that strategy pre- cludes detritivory because a larval gut is not differentiated (see Cadlina below). With the possible exception of ‘faculta- tive’ planktotrophy (see Adalaria below) only long-term planktotrophy plus detri- tivory appears to provide the necessary growth potential. Of all cultured plank- totrophic nudibranchs, О. bilamellata has the largest post-metamorphic size. In the absence of putative genetic or en- ergetic constraints there appears to be no obvious adaptive advantage to be gained from, or which demandés, a shift from the ancestral planktotrophic condi- tion in this species. . Adalaria proxima. Like О. muricata, this dorid is a specialist bryozoan predator which preferentially takes Electra pilosa. We have shown that O. muricata and A. proxima display an extraordinarily high degree of genetic similarity, and that they undoubtedly share a recent common ev- olutionary ancestry (Havenhand et al., 1986). Adalaria is presumed to be the more advanced derivative because of its pelagic lecithotrophy. Selection away from planktotrophy appears to have been dictated by the unpredictability of energy flux divertible toward reproduc- tion by individual adults (see Todd, 1979b, 1987; Todd & Havenhand, 1983; 1988, 1990; Havenhand & Todd, 1988a,b,c). Here, lecithotrophy is viewed as enhancing individual fitness, com- pared with long-term planktotrophy, by reducing reproductive variance as a re- sult of the higher probabilities of larval survival and metamorphisis. Nonethe- less post-larval prey-size constraints persist, as for O. muricata, since these two dorids both metamorphose at similar sizes (= 300 um). Adalaria larvae can feed (Thompson, 1958), but despite di- gestion of flagellates in culture it is evi- dent that somatic degrowth occurs, just as it does on starvation (Kempf & Todd, 1989). The question as to why Adalaria retains a functional larval gut therefore appears to relate to this species’ require- ment to undertake post-larval particulate or detrital feeding prior to definitive bry- ozoan grazing. The retention of an ap- parently functionless, explicitly larval, structure to perform a strictly post-larval activity is, | believe, a deduction of fun- damental importance which supports the hypothesis. . Tritonia hombergi. This species has lec- ithotrophic larvae which apparently lack a functional gut (Thompson, 1962), al- though some larvae in culture clearly in- 286 TODD gest flagellates (Kempf & Todd, 1989). Current investigations of the biennial life-cycle and reproductive energetics of this dendronotid are not yet complete so it is premature to speculate on why it has become lecithotrophic. However, in contrast to A. proxima, no prey-size con- straints are encountered by post-larvae, and grazing immediately ensues on the alcyonarian prey ectoderm once the ju- venile gut structures become organized. 5. Cadlina laevis. Despite undergoing ves- tigial ‘larval’ development, embryos still transiently differentiate typical larval gastropod features such as a shell and velum (Thompson, 1967). Juveniles hatch and complete development to- ward the adult form, but subsist entirely on stored yolk for a few weeks before preying only upon the slime sponge Hal- isarca dujardini (Johnson). Here a func- tional larval gut is not differentiated, but it is not required because prey-size constraints do not apply. Similarly, Cory- phella salmonacea commences preying upon hydroids immediately on hatching (Morse, 1971). If one’s perspective of the evolution of nudi- branch larval types were confined to the pre- juvenile period it would appear intuitively sen- sible to suggest that the sequence is one of planktotrophy — (non-feeding) lecithotrophy — non-pelagic lecithotrophy. Thus, the reten- tion of a functional larval gut by Adalaria prox- ima (and Phestilla sibogae) would be sugges- tive of only an intermediate step along the path to true lecithotrophy (see Kempf & Had- field, 1985; Kempf & Todd, 1989). Alterna- tively, one has to infer an adaptive advantage to such feeding because of the resource de- mands in differentiation of the larval gut; but this confounds the a priori assumption of se- lection to circumvent the (redundant) larval di- gestive system in the shift from planktotrophy to true lecithotrophy. The detritus hypothesis obviates this non sequitur. Nevertheless, Phestilla sibogae presents an as yet intractable obstacle: fed larvae (in contrast to starved larvae) at least maintain somatic tissues during the facultative pelagic phase, in addition to better retaining compe- tence to metamorphose (Kempf & Hadfield, 1985). Here, some adaptive advantage is de- ducible, but despite this the undoubtedly high levels of planktonic mortality may still render the (smaller) earlier-settling P. sibogae larvae of higher mean fitness. In outlining the detri- tus-feeding hypothesis | emphasized the im- probability of a sympatric intermediate prey organism, but one aeolid species appears to show just such an adaptation. The leci- thotrophic veligers of Eubranchus farrani would not metamorphose in response to the adult prey hydroid Aglaophenia pluma, but did so on encountering Obelia geniculata (Todd, 1981). Obelia, by contrast to Aglaophenia, has a wide aperture to the hydratheca which presents no size constraint to post- metamorphs gaining access to the tissues of individual polyps. With regard to the reproductive strategy of Onchidoris bilamellata, it has proven that Hadfield (1963) showed remarkable foresight in predicting that “small adults may depend entirely on grazing of algae and sessile cili- ates until they reach sufficient size to feed on barnacles”. In withdrawing the settlement- timing hypothesis | have presented an alter- native argument predicting selection in favour of particular larval strategies amongst nudi- branchs. But this should not be interpreted as an adaptive explanation of evolutionary shifts along the axis highlighted in Assumptions 1— 3. Rather, it defines which larval types are possible under given circumstances. Thus, for example, because there appear to be con- strained upper (cf. muricid prosobranchs with nurse eggs) and lower limits to nudibranch post-metamorph/hatchling sizes, this hypoth- esis would not predict truly direct develop- ment in a species which encounters major prey-size constraints following metamorpho- sis. However, either of planktotrophy or pe- lagic lecithotrophy would be supportable if de- trital grazing potential were retained. It has long been my contention (Todd, 1979a,b, 1981, 1985a, 1986; Todd & Havenhand, 1983, 1988; Havenhand & Todd, 1988a,b,c) that absolute energetic allocations and parti- tioning within the individual’s budget may be important, if not actually uppermost, in deter- mining the scope for such evolutionary shifts. Selection acts on the differential production of offspring among genotypes and this is inevi- tably some function of energetic capacity and the manner in which this is partitioned. With- out wishing specifically to resurrect the settle- ment-timing hypothesis, one final point should also be stressed. Although planktotrophy and lecithotrophy appear equivalent, in terms of size and level of development at metamor- phosis, they do differ markedly in their con- ferred egg-to-benthic juvenile periods. Both LARVAL STRATEGIES OF NUDIBRANCHS 287 the temperate and tropical lecithotrophic spe- cies discussed above attain their benthic sta- tus more rapidly, and so the three fundamen- tal larval strategies cannot be viewed as essentially similar means to the same end. Questions relating to the adaptive signifi- cance of this intriguing feature of larval biol- ogy remain very much open. ACKNOWLEDGEMENTS This work was supported, in part, by grant no. GR3/4487 from the Natural Environment Research Council. For many hours of thoughtful discussion | thank in particular Steve Hall, Jon Havenhand, Steve Kempf.and Jon Davies. To all | am grateful. LITERATURE CITED BICKELL, L.R. & F.S. CHIA, 1979, Organogenesis and histogenesis in the planktotrophic veliger of Doridella steinbergae (Opisthobranchia: Nudi- branchia). Marine Biology, Berlin, 52: 291-313. BICKELL, L.R., F.S. CHIA, & B.J. CRAWFORD, 1981, Morphogenesis of the digestive system during metamorphosis of the nudibranch Doridella steinbergae (Gastropoda): conversion from phytoplanktivore to carnivore. Marine Biol- ogy, Berlin, 62: 1-16. BICKELL, L.R. & S.C. KEMPF, 1983, Larval and metamorphic morphogenesis in the nudibranch Melibe leonina (Mollusca: Opisthobranchia). Bio- logical Bulletin of the Marine Biological Labora- tory, Woods Hole, 165: 119-138. BONAR, D.B., 1978a, Fine structure of muscle in- sertions on the larval shell and operculum of the nudibranch Phestilla sibogae (Mollusca: Gas- tropoda) before and during metamorphosis. Tis- sue and Cell, 10: 143-152. BONAR, D.B., 1978b, Ultrastructure of a cephalic sensory organ of the gastropod Phestilla sibogae (Aeolidacea, Nudibranchia). Tissue and Cell, 10: 153-265. BONAR, D.B., 1978c, Morphogenesis at metamor- phosis in opisthobranch molluscs. In: CHIA, F.S. & M.E. RICE, eds., Settlement and Metamorpho- sis of Marine Invertebrate Larvae. Elsevier/North- Holland Biomedical Press, New York, р. 177- 196. BONAR, D.B. & M.G. HADFIELD, 1974, Metamor- phosis of the marine gastropod Phestilla sibogae Bergh (Nudibranchia: Aeolidacea). |. Light and electron microscopic analysis of larval and meta- morphic stages. Journal of Experimental Marine Biology and Ecology, 16: 227-255. BOUCHER, L.M., 1983, Extra-capsular yolk bodies in the egg masses of some tropical Opisthobran- chia. Journal of Molluscan Studies, 49: 232-241. CHIA, F.S. & R. KOSS, 1978, Development and metamorphosis of the planktotrophic larvae of Rostanga pulchra (Mollusca: Nudibranchia). Ma- rine Biology, Berlin, 46: 109—119. DAY, R. & L. MCEDWARD, 1984, Aspects of the physiology and ecology of pelagic larvae of ma- rine benthic invertebrates. In: STEIDINGER, K.A. & Е.М. WALKER, eds., Marine Plankton Life Cycle Strategies. CRC Press, Boca Raton, Florida, p. 93-120. EYSTER, L.S., 1979, Reproduction and develop- mental variability in the opisthobranch Tenellia pallida. Marine Biology, Berlin, 51: 133-140. GRANT, A. & P. WILLIAMSON, 1985, The settle- ment-timing hypothesis: a critique. Marine Ecol- ogy-Progress Series, 23: 75-83. HADFIELD, M.G., 1963, The biology of nudibranch larvae. Oikos, 14: 85-95. HADFIELD, M.G., 1977, Chemical interactions in larval settling of a marine gastropod. In: FAULKNER, D.J. & W.H. FENICAL, eds., Marine Natural Products Chemistry. Plenum, New York, p. 403-413. HADFIELD, M.G., 1978, Metamorphosis in marine molluscan larvae: and analysis of stimulus and response. In: CHIA, F.S. & M.E. RICE, eds., Set- tlement and Metamorphosis of Marine Inverte- brate Larvae. Elsevier/North-Holland Biomedical Press, New York, p. 165-175. HADFIELD, M.G., 1984, Settlement requirements of molluscan larvae: new data on chemical and genetic roles. Aquaculture, 39: 283-298. HADFIELD, M.G.& D. SCHEUER, 1985, Evidence for a soluble metamorphic inducer in Phestilla: ecological, chemical and biological data. Bulletin of Marine Science, 37: 556-566. HADFIELD, M.G.& M. SWITZER-DUNLAP, 1984, Opisthobranchs. In: TOMPA, A.S., N.H. VER- DONK & J.A.M. van den BIGGELAAR, eds., The Mollusca, volume 7, Reproduction. Academic Press, Orlando & London, p.209-350. HARRIS, L.G., 1973, Nudibranch associations. Current Topics in Comparative Pathobiology, 2: 213-315. HARRIS, L.G., 1975, Studies on the life history of two coral-eating nudibranchs of the genus Phe- stilla. Biological Bulletin of the Marine Biological Laboratory, Woods Hole, 149: 539-550. HAVENHAND, J.N. 8 C.D. TODD, 1988a, The physiological ecology of Adalaria proxima (Alder 8 Hancock) and Onchidoris muricata (Múller) (Gastropoda: Nudibranchia). |. Feeding, growth and respiration. Journal of Experimental Marine Biology and Ecology, 118: 151-172. HAVENHAND, J.N. & C.D. TODD, 1988b, The physiological ecology of Adalaria proxima (Alder & Hancock) and Onchidoris muricata (Müller) (Gastropoda: Nudibranchia).!l. Reproduction. Journal of Experimental Marine Biology and Ecology, 118: 173-189. HAVENHAND, J.N. & C.D. TODD, 1988c. Repro- 288 TODD ductive effort of the nudibranch molluscs Adalaria proxima (Alder & Hancock) and Onchidoris mu- ricata (Muller): an evaluation of techniques. Functional Ecology, 3: 153-169. HAVENHAND, J.N., J.P. THORPE, & C.D. TODD, 1986, Estimates of biochemical genetic diversity within and between the nudibranch molluscs Ад- alaria proxima (Alder & Hancock) and Onchidoris muricata (Muller) (Doridacea: Onchidorididae). Journal of Experimental Marine Biology and Ecology, 95: 105-111. HIRATA, K.Y. & M.G. HADFIELD, 1986, The role of choline in metamorphic induction of Phestilla (Gastropoda: Nudibranchia). Comparative Bio- chemistry and Physiology, 84C: 15-21. JABLONSKI, D. & R.A. LUTZ, 1983, Larval ecology of marine benthic invertebrates: paleobiological implications. Biological Reviews, 58: 21-89. KEMPF, S.C., 1981, Long-lived larvae of the gas- tropod Aplysia juliana: do they disperse and metamorphose or just slowly fade away? Marine Ecology-Progress Series, 6: 61-65. KEMPF, S.C.& A.O.D. WILLOWS, 1977, Labora- tory culture of the nudibranch Tritonia diomedea Bergh (Tritoniidae: Opisthobranchia) and some aspects of its behavioural development. Journal of Experimental Marine Biology and Ecology, 30: 261-276. KEMPF, S.C.& M.G. HADFIELD, 1985, Planktotro- phy by the lecithotrophic larvae of a nudibranch, Phestilla sibogae (Gastropoda). Biological Bulle- tin of the Marine Biological Laboratory, Woods Hole, 169: 119-130. KEMPF, S.C. & C.D. TODD, 1989, Feeding poten- tial in the lecithotrophic larvae of Adalaria prox- ima and Tritonia hombergi: an evolutionary per- spective. Journal of the Marine Biological Association, U. K., 69: 659—682. LUCAS, J.S. & J.D. COSTLOW, 1979, Effects of various temperature cycles on the larval devel- opment of the gastropod mollusc Crepidula for- пса. Marine Biology, Berlin, 51: 111-117. MILLER, S.E. & M.G. HADFIELD, 1986, Ontogeny of phototaxis and metamorphic competence in larvae of the nudibranch Phestilla sibogae Bergh (Gastropoda: Opisthobranchia). Journal of Ex- perimental Marine Biology and Ecology, 97: 95— 112. MORSE, M.P., 1971, Biology and life history of the nudibranch mollusc, Coryphella stimpsoni (Ver- rill, 1879). Biological Bulletin of the Marine Bio- logical Laboratory, Woods Hole, 140: 84—94. PECHENIK, J. & G.M. LIMA, 1984, Relationship between growth, differentiation, and length of lar- val life for individually reared larvae of the marine gastropod, Crepidula fornicata. Journal of Exper- imental Marine Biology and Ecology, 166: 537— 549. PERRON, F.B. & R.D. TURNER, 1977, Develop- ment, metamorphosis, and natural history of the nudibranch Doridella obscura Verrill (Coram- bidae: Opisthobranchia). Journal of Experimental Marine Biology and Ecology, 27: 171-185. PILKINGTON, M.C. & V. FRETTER, 1970, Some factors affecting the growth of prosobranch veligers. Helgolander wissenschaftliche Meere- suntersuchungden, 20: 576-598. STRATHMANN, R.R., 1978, The evolution and loss of feeding larval stages of marine invertebrates. Evolution, 32: 894-906. STRATHMANN, R.R., 1985, Feeding and non- feeding larval development and life-history evo- lution in marine invertebrates. Annual Review of Ecology and Systematics, 16: 339-361. STRATHMANN, R.R., M.F. STRATHMANN & В.Н. EMSON, 1984, Does limited brood capacity link adult size, brooding, and simultaneous hermaph- roditism? A test with the starfish Asterina phylac- tica. American Naturalist, 123: 796-818. SWITZER-DUNLAP, M. 8 M.G. HADFIELD, 1977, Observations on development, larval growth and metamorphosis of four species of Aplysiidae (Gastropoda: Opisthobranchia) in laboratory cul- ture. Journal of Experimental Marine Biology and Ecology, 47: 245-261. TARDY, J., 1970, Contribution à l'étude des méta- morphoses chez les nudibranches. Annales des Sciences Naturelle (Zoologie et Biologie Ani- male), 12: 299-370. THOMPSON, T.E., 1958, The natural history, em- bryology, larval biology and post-larval develop- ment of Adalaria proxima (Alder & Hancock) (Gastropoda Opisthobranchia). Philosophical Transactions of the Royal Society of London, Se- ries B, 242: 1-58. THOMPSON, T.E., 1962, Studies on the ontogeny of Tritonia hombergi Cuvier (Gastropoda, Opis- thobranchia). Philosophical Transactions of the Royal Society of London, Series В, 245: 171- 218. THOMPSON, T.E., 1967, Direct development in a nudibranch, Cadlina laevis, with a discussion of developmental processes in Opisthobranchia. Journal of the Marine Biological Association, U. K., 47: 1-22. TODD, C.D., 1979a, The population ecology of On- chidoris bilamellata (L.). Journal of Experimental Marine Biology and Ecology, 41: 213-255. TODD, C.D., 1979b, Reproductive energetics of two species of dorid nudibranchs with plank- totrophic and lecithotrophic larval strategies. Ma- rine Biology, Berlin, 53: 57-68. TODD, C.D., 1981, Ecology of nudibranch mol- luscs. Oceanography and Marine Biology, an An- nual Review, 19: 141-234. TODD, C.D., 1985a, Reproductive strategies of north temperate rocky shore invertebrates. In: MOORE, P.G. & R. SEED, eds., Ecology of Rocky Coasts. Hodder & Stoughton, Sevenoaks, p. 203-219. TODD, C.D., 1985b, Settlement-timing hypothesis: reply to Grant & Williamson. Marine Ecology- Progress Series, 23: 197-202. TODD, C.D., 1987, Reproductive energetics and larval strategies of nudibranch molluscs: effects of ration level during the spawning period in On- LARVAL STRATEGIES OF NUDIBRANCHS 289 chidoris muricata (Müller) and Adalaria proxima (Alder and Hancock). American Malacological Bulletin, 5: 293-301. TODD, C.D.& R.W. DOYLE, 1981, Reproductive strategies of marine benthic invertebrates: a set- tlement-timing hypothesis. Marine Ecology- Progress Series, 4: 75-83. TODD, C.D. & J.N. HAVENHAND, 1983, Repro- ductive effort: its definition, measurement and in- terpretation in relation to molluscan life history strategies. Journal of Molluscan Studies, Supple- ment, 12A: 203-208. TODD, C.D & J.N. HAVENHAND, 1984, Prelimi- nary observations on the embryonic and larval development of three dorid nudibranchs. Journal of Molluscan Studies, 51: 97-99. TODD, C.D. & J.N. HAVENHAND, 1988, The phys- iological ecology of Adalaria proxima (Alder & Hancock) and Onchidoris muricata (Müller) (Gas- tropoda: Nudibranchia).lll. Energy budgets. Jour- nal of Experimental Marine Biology and Ecology, 118: 191-205. TODD, C.D. & J.N. HAVENHAND, 1990, Верго- ductive effort and larval strategies of benthic ma- rine invertebrates: is there any relationship? Functional Ecology, 4: 132-133. TODD, C.D., J.N. HAVENHAND & J.P. THORPE, 1989, Genetic differentiation, pelagic larval trans- port and gene flow between local populations of the intertidal marine mollusc Adalaria proxima (Alder & Hancock). Functional Ecology, 2: 441— 451 TODD, C.D., M.G. BENTLEY & J.N. HAVENHAND, 1991, Larval metamorphosis of the nudibranch Adalaria proxima (Gastropoda: Nudibranchia): the effects of choline and elevated potassium ion concentration. Journal of the Marine Biological Association, U.K. 71:53-72. YOOL, A.J., $.М. GRAU, M.G. HADFIELD, R.A. JENSEN, D.A. MARKELL & D.E. MORSE, 1986, Excess potassium induces larval metamorphosis in four marine invertebrate species. Biological Bulletin of the Marine Biological Laboratory, Woods Hole, 170: 255-266. MALACOLOGIA, 1991, 32(2): 291-299 THE OPISTHOBRANCH FAUNA OF A MEDITERRANEAN LAGOON (STAGNONE DI MARSALA, WESTERN SICILY) Riccardo Cattaneo Vietti' & Renato Chemello? ABSTRACT The opisthobranch fauna present in a lagoon (Stagnone di Marsala) near Marsala (western Sicily) is described. There is a rich opisthobranch fauna, with more than 20 species, some of which are very abundant. Bullomorpha, with several species often very common in this particular ecosystem, are well represented, but the species of Sacoglossa and Nudibranchia are quite different from those in other Mediterranean lagoons. Many species, which are usually common in similar environments, are rare or absent, e.g. several aeolids and anadorids, but a rich sponge population supports the presence of several eudoridaceans, including the little-known Paradoris granulata and Doriopsilla rarispina. Elysia timida, Hypselodoris villafranca and Dendrodoris limbata can, perhaps, be considered euryhaline species as they were frequently collected in brackish or lightly polluted waters. Finally, the opisthobranch fauna present in Mediterranean lagoon waters is reviewed. INTRODUCTION Brackish water lagoons in the Mediterra- nean have considerable annual variations in temperature and salinity (Colombo, 1977; Sacchi, 1979; Barnes, 1980; Guelorget & Perthuisot, 1983) and this therefore poses major physiological problems for animals liv- ing there. Opisthobranchs from brackish wa- ters in the Mediterranean are known from several studies (see Table 2) but there have been few detailed systematic investigations of opisthobranchs in this habitat. The purposes of this paper are to present the results of a 3-year study of opistho- branchs in the Marsala Lagoon and to review the opisthobranchs living in this habitat throughout the Mediterranean. The Marsala Lagoon, which is called ‘Stag- none’, extends for 2000 ha in western Sicily and has been extensively studied (Cavallaro et al., 1977; Calvo et al. 1982). Information on its malacological fauna has been reported by Cavallaro et al. (1977) and Sparla (1985). The Marsala Lagoon is morphologically di- vided into two basins (Fig. 1). The southern basin is connected with the open sea by a large channel, between Punta d’Alga and the Isola Grande. The northern basin, the true ‘Stagnone’, has markedly more lagoon char- acteristics such as shallow waters, irregular water movements and variable salinity and temperature. There is, moreover, a progres- sive silting up because the Birgi River, re- cently deviated southward, was canalized near the ‘Tramontana’ mouth, and so dis- charges its abundant waste into the lagoon. Sampling Stations The average depth of the northern basin of the Marsala lagoon is around 0.5-1.0 m, with a maximum of 3 m near Isola Grande. Most of the specimens were collected by snorkeling in different periods of the years 1984-86, near sparse shoots of Posidonia oceanica (Sta- tions A,E), in Cymodocea nodosa prairies, under or on small hard objects or animals (stones, anchor logs, sponges) and on Rytiphloea tinctoria aegagropyla forms near Mozia (Stns A,E,G), Punta Grassellino (Stn C), Punta Palermo (Stns B,F), Saline (Stn D), between Mozia and Punta Palermo (Stns H,]) and near Punta d’Alga (Stn L). The average depth of the samples taken was at 0.5-1.5 m. The species collected and the numbers of specimens are reported in Table 1. The opisthobranch fauna of the Marsala Lagoon The opisthobranch fauna in the Marsala la- goon is quite rich (Table 1), with more than 20 species, compared with about 60 species re- corded from all other Mediterranean lagoons. “Istituto di Zoologia dell'Università degli Studi di Genova, via Balbi 5, I-16126 Genova, Italy Istituto di Zoologia dell'Università degli Studi di Palermo, via Archirafi 18, |-90123 Palermo, Italy. 292 CATTANEO VIETTI & CHEMELLO © =" F. BIRGI 2» FIG. 1. The Marsala Lagoon (western Sicily). Sampling areas: А, Е, G: Mozia Isle; В, Е: Punta Palermo; С: Punta Grassellino; О: Saline; H, I: between Mozia Isle and Punta Palermo; L: Punta d'Alga. This richness could be due to the presence of at least five habitats: Posidonia beds, Cymo- docea prairies, sandy bottoms, the peculiar ‘microhabitat’ of aegagropyla forms of Rytiph- loea tinctoria (Sparla & Riggio, 1984; Riggio 8 Sparla, 1985), and hard substrates made up, above all, of tufaceous outcrops and calcare- ous red algae (Lithothamnium fruticulosum, L. calcareum, and pleustophytic forms of Meso- phyllum lichenoides). On the mud beds, Bullomorpha are com- mon with well-known euryhaline species, such as Mamilloretusa mammillata, Bulla stri- ata and Haminoea hydatis, while Haminoea OPISTHOBRANCHS OF A MEDITERRANEAN LAGOON 293 TABLE 1. Opisthobranch molluscs present in the Marsala Lagoon (western Sicily). For the sampling areas see the legend to Fig. 1. Species A B C Retusa semisulcata' — — = Retusa truncatula' = Mamilloretusa mammillata’ 2 Bulla striata? 3 Haminoea hydatis'? 2 Haminoea cymoelium — Elysia timida — — Aplysia fasciata' Berthella aurantiaca Berthella stellata Doris verrucosa’ -- —- — Doris sp.' — — — Glossodoris sp.' — Chromodoris sp. 5 Hypselodoris villafranca 10+ — — Hypselodoris elegans 1 2 Hypselodoris messinensis — — 10+ Paradoris granulata Wer — 4 Platydoris argo — — Dendrodoris limbata 2 Dendrodoris grandiflora” 1 — — Doriopsilla rarispina 13 Spurilla neapolitana 1 Total number of 52+ 1 31 + specimens + = more specimens were observed than collected recorded by Cavallaro et al., 1977 recorded by Sparla, 1985 (unpublished data, thesis) 1 2 cymoelium should probably be considered a young H. hydatis. The only common notaspidean in the Marsala lagoon is Berthella aurantiaca. The species composition of Sacoglossa and Nudibranchia in this lagoon is quite dif- ferent from that known from other Mediterra- nean lagoons. Among the Sacoglossa, Elysia timida is very common on hard artificial bot- toms at 0.2 m depth, near Acetabularia ace- tabulum, on which it feeds (Ros & Rodriguez, 1985). This easily-recognized white species with red spots (Bouchet, 1984) seems to pre- fer shallow and euryhaline waters. It has also been found in other brackish waters such as Strea Lagoon (lonian Sea), Oristano (Sardi- nia) and S. Marco Cape near Sciacca (Sicily). A rich sponge population (Corriero, 1984) supports the presence of several eudor- idaceans, some of them also of considerable scientific interest. Doriopsilla rarispina, a very rare species recently re-described by Perrone (1986) from the lonian Sea, has been found Sites sampled D Е Я G H | В 1 a ee 4 | | | | | о-хо<а | + | | | wn | | > | | | wo + and there is a large population of Paradoris granulata. This beautifully-camouflaged spe- cies is easily found inside the sponge Ircinia variabilis or in its oscula. There is also what is probably a new, undescribed species of chro- modorid in the Marsala Lagoon. It is a few centimetres long and presents a translucid pale white colour with characteristic pale azure-white ocelli surrounded by an opaque white ring. It lives at the base of Cystoseira barbata brown algae, on the sponge Tedania anelans. Many young specimens of Hypselodoris vil- lafranca and H. messinensis were collected among Aytiphloea_ tinctoria aegagropyla forms which seem to be ‘nurseries’ for these nudibranchs. On the other hand, some common eury- haline or widely-distributed species (Polycera quadrilineata, Favorinus branchialis, Cory- phella pedata and Cratena peregrina) are ab- sent, probably due to the sparseness of hard bottoms with few hydroids and bryozoans. 294 CATTANEO VIETTI & CHEMELLO FIG. 2. Mediterranean Sea: brackish waters in which opisthobranchs were found (see Table 2)— SPAIN: 1. Mar Menor; 2. Salinas de Calblanque. FRANCE: 3. Salses; 4. Sigean; 5. Thau (or Séte); 6. Berre; 7. Brusc; ITALY: 8. Orbetello; 9. Oristano; 10. Lungo; 11. Caprolace; 12. Fogliano; 13. Patria; 14. Fusaro; 15. Faro and Ganzirri; 16. Tindari; 17. Stagnone of Marsala; 18. Sciacca; 19. Vendicari; 20. Mar Piccolo of Taranto; 21. Strea of Porto Cesareo; 22. Venezia; 23. Grado and Marano; USSR: 24. Azov Sea; ISRAEL: 25. Dor; 26. Mikhmoret. EGYPT: 27. Bardawil. TUNISIA: 28. Biban; 29. Bizerte; 30. Tunis; MOROCCO: 31. Nador. The rarity of Spurilla neapolitana and the ab- sence of the common euryhaline Aeolidiella spp. are surprising since their food, Para- stephanauge pauxii is very common on Cy- modocea leaves. Finally, the common Mediterranean spe- cies Elysia timida, Hypselodoris villafranca and Dendrodoris limbata can be considered euryhaline, because they were frequently seen also in other brackish habitats such as the ‘Strea’ of Porto Cesareo (Taranto) and Oristano lagoon. According to Perrone (1984), Dendrodoris limbata can live in pol- luted waters and this fact confirms its adapt- ability to environmental changes. Review of opisthobranchs in Mediterranean brackish waters The Opisthobranch fauna present in Medi- terranean brackish waters is still not well known (Fig. 2). There are useful reports by Barletta (1980) and Torelli (1982), while Gue- lorget (1985), in his review of the parhalic do- main, considered Akera bullata an exclusively brackish species, while Aplysia depilans and Philine aperta are the most common opistho- branchs present in Mediterranean lagoons. Additional information is available from gen- eral studies carried out on the malacological fauna of lagoons, even though nudibranchs were often ignored. A summary of opistho- branch records in Mediterranean lagoons is given in Table 2. Many opisthobranchs can live in this pecu- liar habitat which is subject to considerable variation in the main physico-chemical condi- tions such as salinity, temperature, oxygen saturation, pH, etc. The Bullomorpha, living on soft bottoms, are widespread and include euryhaline species such as Retusa trunca- tula, Haminoea navicula, Bulla striata, Philine aperta and Akera bullata. Many Sacoglossa are present in the lagoon ecosystem but they only inhabit areas where food plants occur. Oxynoe and Lobiger, for example, are confined to Caulerpa prairies (sometimes living in outer zones of the la- goons). The majority of other species are linked to the distribution of the green algae Bryopsis and Cladophora. Only Limapontia capitata, found in the Fusaro Lake (Naples), seems to occur exclusively in brackish waters (Jensen, 1977). The occurrence of Alderia modesta, an Atlantic euryhaline species (Adam & Leloup, 1939; Engel et al., 1940), is still uncertain in the Mediterranean Sea. Algal availability is also important for aplysi- omorphs: they are sometimes abundant in the zones where Ulvales flourish while Bursatella leachii, in the Mediterranean Sea, was always recorded in still-water areas like lagoons. OPISTHOBRANCHS OF A MEDITERRANEAN LAGOON 295 TABLE 2. Opisthobranch molluscs present in Mediterranean lagoons. Species BULLOMORPHA Acteon tornatilis (L.) Cylichnina girardi (Audouin) Retusa semisulcata (Philippi) В. perstriata (Cerulli Irelli) R. truncatula (Bruguiére) R. umbilicata (Montagu) Retusa spp. Mamilloretusa mammillata (Philippi) Ringicula auriculata (Menard de la Groye) R. conformis (Monterosato) Bulla striata Bruguière Atys blainvilliana (Récluz) Haminoea hydatis (L.) H. navicula (Da Costa) H. orbignyana (Férussac) Akera bullata Muller Philine aperta (L.) Philine cf. scabra (Muller) APLYSIOMORPHA Aplysia depilans Gmelin Locality (Reference) France: Berre (Mars, 1966) Italy: Venice (Coen, 1928); Grado, Marano (Zucchi Stolfa, 1977) Egypt: Bardawil (Mienis, 1976; Barash & Danin, 1982) Italy: Marsala (Cavallaro et al., 1977); Grado, Marano (Zucchi Stolfa, 1977) Italy: Grado, Marano (Zucchi Stolfa, 1977) France: Salses, Sigean, Thau, Berre (Mars, 1966) Italy: Orbetello (Mari, 1976); Marsala (Cavallaro et al., 1977) Tunisia: Tunis (Zaouali, 1981) Morocco: Nador (Saubade, 1979) France: Berre (Mars, 1966) Egypt: Bardawil (Barash & Danin, 1982) Italy: Marsala (Cavallaro et al., 1977); Mar Piccolo (Tortonici & Panetta, 1977) Italian Lagoons (Torelli, 1982) Italy: Porto Cesareo (Parenzan, 1970) France: Berre (Mars, 1966) Italy: Orbetello (Mari, 1976); Caprolace (Ardizzone, 1985); Faro, Ganzirri (Giudice, pers. comm.); Marsala (Sparla, 1985—thesis); Vendicari (Chemello, pers. obs.); Mar Piccolo (Parenzan, 1969; Tortorici & Panetta, 1977) Egypt: Bardawil (Barash & Danin, 1982) Tunisia: Bizerte (Zaouali, 1979) Morocco: Nador (Saubade, 1979) Egypt: Bardawil (Barash & Danin, 1982) Spain: Mar Menor (Olmo & Ros, 1984) Italy: Lungo, Caprolace, Fogliano (Ardizzone, 1985); Fusaro (Ferro & Russo, 1981); Faro, Ganzirri (Scordia, 1927; Parenzan, 1979); Tindari (Chemello, pers. obs.); Marsala (Cavallaro et al., 1977; Sparla, 1985—thesis); Venice (Coen, 1933,1938; Vatova, 1940); Grado, Marano (Zucchi Stolfa, 1977) Egypt: Bardawil (Barash & Danin, 1982) Spain: Mar Menor (Olmo & Ros, 1984); Salinas de Calblanque (Templado et al., 1983) France: Sigean, Thau, Berre (Mars, 1966) Italy: Orbetello (Mari, 1976); Faro, Ganzirri (Parenzan, 1979); Mar Piccolo (Tortorici & Panetta, 1977); Venice (Coen, 1933;1938) Tunisia: Biban (Zaouali & Baeten, 1985); Bizerte (Zaouali, 1979); Tunis (Zaouali, 1974,1981) Morocco: Nador (Saubade, 1979) Spain: Mar Menor (Murillo & Talavera, 1983; Olmo & Ros, 1984); Salinas de Calblanque (Templado et al., 1983) Spain: Salinas de Calblanque (Templado et al., 1983) France: Thau, Berre (Mars, 1966) Italy: Venice (Coen, 1933) Spain: Mar Menor (Olmo & Ros, 1984) France: Thau, Berre (Mars, 1966) Italy: Mar Piccolo (Parenzan, 1969; Tortorici & Panetta, 1977) Tunisia: Bizerte (Zaouali, 1979) Italy: Grado, Marano (Zucchi Stolfa, 1977) France: Thau (Mars, 1966) Italy: Venice (Coen, 1938) Tunisia: Bizerte (Zaouali, 1979); Tunis (Zaouali, 1974) (continued) 296 TABLE 2. (Continued) Species A. fasciata Poiret A. punctata Cuvier Bursatella leachii leachii Blainville В. |. savignyi Audouin Notarchus punctatus Philippi NOTASPIDEA Pleurobranchaea meckelii Leue Berthella aurantiaca (Risso) SACOGLOSSA Oxynoe olivacea Rafinesque Lobiger serradifalci (Calcara) Elysia viridis (Montagu) E. timida (Risso) Calliopaea bellula d'Orbigny Placida viridis (Trinchese) P. dendritica (Alder & Hancock) Ercolania funerea (Costa) Limapontia capitata (Müller) Alderia modesta (Lovén) NUDIBRANCHIA Doridina Okenia elegans (Leuckart) Doris verrucosa L. D. bicolor (Bergh) Hypselodoris villafranca (Risso) Chromodoris krohnii (Verany) Polycera quadrilineata (Müller) P. dubia Sars Polycerella emertoni Verrill Limacia clavigera (Müller) Dendrodoris limbata (Cuvier) CATTANEO VIETTI & CHEMELLO Locality (Reference) Spain: Salinas de Calblanque (Templado et al., 1983) France: Thau, Berre (Mars, 1966) Italy: Orbetello (Mari, 1976); Patria (Sacchi, 1961); Faro, Ganzirri (5.1.М. comm.); Marsala (Cavallaro et al., 1977); Porto Сезагео (Cattaneo Vietti, pers. obs.) France: Thau, Berre (Mars, 1966) Italy: Venice (Coen, 1933) Italy: Venice (Cesari et al., 1986) Italy: Mar Piccolo (Tortorici & Panetta, 1977) Israel: Dor, Mikhmoret (Barash & Danin, 1972) Italy: Mar Piccolo (Parenzan, 1969) Italy: Mar Piccolo (Parenzan, 1969) Tunisia: Bizerte (Zaouali, 1979) Iteiy: Mar Piccolo (Parenzan, 1969,1970; Tortorici & Panetta, 1977) Italy: Orbetello (Mari, 1976); Mar Piccolo (Parenzan, 1969; Tortorici & Panetta, 1977) Spain: Mar Menor (Olmo & Ros, 1984) France: Thau (Mars, 1966) Italy: Fusaro (Schmekel, 1968) Spain: Mar Menor (Ros & Rodriguez, 1985) Italy: Oristano (Cattaneo Vietti, pers. obs.); Sciacca (Chemello, pers. obs.); Porto Cesareo (Cattaneo Vietti, pers. obs.) Spain: Salinas de Calblanque (Templado et al., 1983) Italy: Fusaro (Schmekel, 1968) Italy: Fusaro (Schmekel, 1968) Italy: Fusaro (Schmekel, 1968) Italy: Fusaro (Schmekel, 1968) Italy: Fusaro (Schmekel, 1968) — (Pruvot-Fol, 1954) Italy: Fusaro (Toscano, pers. comm.) France: Thau (Mars, 1966) Italy: Orbetello (Mari, 1976); Marsala (Cavallaro et al., 1977) Tunisia: Bizerte (Zaouali, 1979) Italy: Venice (Coen, 1938) Italy: Orbetello (Mari, 1976); Porto Cesareo (Cattaneo Vietti, pers. obs.) Italy: Orbetello (Mari, 1976) France: Canaux de Sète (Mars, 1966) Italy: Orbetello (Mari, 1976); Fusaro (Schmekel, 1968; Toscano, pers. comm.) Italy: Fusaro (Schmekel, 1968) Italy: Fusaro (Schmekel, 1968) Italy: Fusaro (Toscano, pers. comm.) Italy: Faro, Ganzirri (Giudice, pers. comm.); Porto Cesareo (Cattaneo Vietti, pers. obs.) OPISTHOBRANCHS OF A MEDITERRANEAN LAGOON TABLE 2. (Continued) Species NUDIBRANCHIA Arminina Janolus cristatus (Delle Chiaje) NUDIBRANCHIA Aeolidina Coryphella pedata (Montagu) C. lineata (Lovén) Calmella cavolinii (Verany) Facelina coronata (Forbes & Goodsir) F. annulicornis (Chamisso & Eysenhardt) Cratena peregrina (Gmelin) Favorinus branchialis (Rathke) Eubranchus exiguus (Alder & Hancock) Cuthona caerulea (Montagu) Tenellia adspersa (Nordmann) Calma glaucoides (Alder & Hancock) Aeolidiella alderi (Cocks) Locality (Reference) 297 Italy: Orbetello (Mari, 1976); Fusaro (Schmekel, 1968; Toscano, pers. comm.) France: Canaux de Sète (Mars, 1966) Italy: Fusaro (Toscano, pers. comm.) France: Canaux de Séte (Mars, 1966) Italy: Orbetello (Mari, 1976) France: Thau (Mars, 1966) France: Thau (Mars, 1966) France: Canaux de Sète (Mars, 1966) Italy: Orbetello (Mari, 1976) France: Brusc (Riva & Vicente, 1976) Italy: Fusaro (Schmekel, 1968) Italy: Fusaro (Schmekel, 1968) France: Canaux de Sète (Mars, 1966) USSR: Azov Sea (Roginskaya, 1970) Tunisia: Tunis (Zaouali, 1974) France: Brusc (Riva & Vicente, 1976) Italy: Ризаго (Schmekel & Portmann, 1982); Porto Cesareo (Cattaneo Vietti, pers. obs.) A. rubra (Cantraine) Baeolidia nodosa (Haefelfinger & Stamm) Spurilla neapolitana (Delle Chiaje) France: Thau, Berre (Mars, 1966) Spain: Salinas de Calblanque (Templado et al., 1983) Spain: Salinas de Calblanque (Templado et al., 1983) France: Thau (Mars, 1966); Brusc (Riva & Vicente, 1976) Italy: Caprolace (Ardizzone, 1985); Fusaro (Schmekel, 1968) Berghia verrucicornis (Costa) Italy: Orbetello (Mari, 1976) Many species of nudibranchs occur in the lagoons. Species which are characteristic of shallow water and tide-pools (e.g. Polycera quadrilineata, Polycerella emertoni, Calmella cavolinii, Doris verrucosa) can also thrive in brackish waters. When hydroids settle on hard bottoms, aeolids are commonly found on them (e.g. Coryphella spp., Facelina spp., Cratena peregrina and Cuthona coerulea). Typical euryhaline species are Spurilla nea- politana, Aeolidiella spp., Favorinus branchi- alis and Tenellia adspersa. Finally, Tergipes tergipes and Embletonia pulchra, which are euryhaline species along the Atlantic coasts (Pruvot-Fol, 1954; Thompson & Brown, 1984), have rarely been recorded in the Med- iterranean Sea and do not appear to be as- sociated with any particular ecological condi- tions. Mediterranean lagoons vary in their spe- cies composition of hydroids (Morri & Bianchi, 1983), serpulids (Bianchi et al., 1984; Bianchi, 1985) and prosobranchs (Torelli, 1983), and doubtless similar variation will be found to oc- cur in opisthobranchs. One might expect the North Atlantic type lagoons of the north Adri- atic to have a very different fauna from the xero-Mediterranean lagoons of Sicily and north Africa, but data even for the better known Bullomorpha are too poor to enable any such conclusions to be made. ACKNOWLEDGEMENTS We offer grateful thanks to Prof. M. Ed- munds (Lancashire Polytechnic, Preston) for his criticism and to Prof. S. Riggio, M.P. Sparla, G. Corriero, A. Giudice and F. Tos- cano for their help. 298 CATTANEO VIETTI & CHEMELLO LITERATURE CITED ADAM, W. & E. LELOUP, 1939, Sur la presence d'Alderia modesta (Lovén, 1844) en Belgique. Bulletin Museum Royal Histoire naturelle du Bel- gique, 15 (64): 1-13. ARDIZZONE, G. 1985, Zoologia. In: Seminario in- formativo sui risultati del progetto ‘Laghi costieri’ (Terracina, 1985). Amministrazione Provinciale di Latina e Université degli Studi ‘La Sapienza’, Rome, 1-77 р. BARASH, А. & Z. DANIN, 1971, Opisthobranchs from Mediterranean waters of Israel. /srael Jour- nal of Zoology, 20: 151-200. BARASH, A. & Z. DANIN, 1972, The Indo-Pacific species of Mollusca in the Mediterranean and notes on a collection from the Suez Canal. /srael Journal of Zoology, 21: 301- 374. BARASH, A. & Z. DANIN, 1977, Additions to the knowledge of Indo-Pacific Mollusca in the Medi- terranean. Conchiglie, 13: 85-116. BARASH, A. & Z. DANIN, 1982, Contribution to the knowledge of Mollusca in the Bardawil lagoon. Bollettino malacologico, Milano, 18: 107-128. BARLETTA, G., 1980, Gasteropodi marini nudi. Guide per il riconoscimento delle specie animali delle acque lagunari e costiere italiane 3. CNR, Rome, 1-124 р. BARNES, R.S.K., 1980, Coastal Lagoons. Cam- bridge University Press, Cambridge, 1-106 р. BIANCHI, C.N., 1985, Biogéographie des lagunes méditerranéenes d'aprés la distribution des Poly- chétes Serpuloidea. Rapport de la Commission International pour l'Etude de la Mer Méditerra- née, 29 (4): 39—40. BIANCHI, C.N., L.A. CHESSA & C. MORRI, 1984, Serpuloidea (Annelida, Polychaeta) della Sarde- gna, con particolare riguardo alle lagune cos- tiere. Rendiconti del Seminario della Facolta di Scienze dell Universita di Cagliari, 54 (Suppl.): 49-58. BOUCHET, P., 1984, Les Elysiidae de Méditer- ranée (Gastropoda, Opisthobranchiata). Annales de l'Institut Océanographique de Paris, 60: 19— 28. CALVO, S., G. GIACCONE & S. RAGONESE, 1982, Tipologia della vegetazione sommersa dello stagnone di Marsala (TP). Naturalista Sicil- iano, 6: 187-196. CAVALLARO, G. et al., 1978, Studio di un ambi- ente lagunare: lo Stagnone di Marsala. In: Ambi- enti umidi costieri. Atti 11? Convegno Siciliano di Ecologia (Noto). р. 47-69. CESARI, P., L. MIZZAN & E. MOTTA, 1986, Rinvenimento di Bursatella leachi leachi Blain- ville 1817 in Laguna di Venezia. Prima segnalazi- one adriatica. Lavori Societa Veneziana di Sci- enze Naturali, 11: 5-16. COEN, G., 1933, Saggio di una sylloge mollusco- rum adriaticum. Memorie Regio Comitato talas- sografico italia. 192. 1-186 p. COEN, G., 1938, Nota sui molluschi della Laguna veneta. Atti della Societa Italiana per il Progresso delle Scienze, 26: 114-123. COLOMBO, G., 1977, Lagoons. In: BARNES, R. S. K., ed., The Coastline. Wiley, London & New York, p. 63-81. CORRIERO, G., 1984, Note sul popolamento di poriferi dello Stagnone di Marsala (Sicilia). Nova Thalassia, 6 (Suppl.): 213-223. ENGEL, H., S.J. GEERTS, & C.O. VAN REG- TEREN ALTERA, 1940, Alderia modesta (Lovén) and Limapontia depressa Alder & Hancock in the brackish waters of the Dutch coast. Basteria, 5: 6-34. FERRO, R. & G.F. RUSSO, 1981, Aspetti di parti- colare interesse nella malacofauna del lago Fusaro. Bollettino malacologico, Milano, 17: 191-198. GUELORGET, O., 1985, Entre mer et continent. Contribution a l'étude du domaine paralique. Un- published. These, Universite de Sciences et Techniques de Languedoc, Montpellier, 1-721 р. GUELORGET, O. 4 J.P. PERTHUISOT, 1983, Le domaine paralique. Travaux du Laboratoire de Geologie de Paris, 16: 1-136. JENSEN, K., 1977, Optimal salinity and tempera- ture intervals of Limapontia capitata (Opistho- branchia, Sacoglossa) determined by growth and heart rate measurements. Ophelia, 16: 175-185. MARI, M., 1976, Osservazioni sulla malacofauna delle lagune di Orbetello. Memorie della Societa Toscana di Scienze naturali, (B) 83: 190-204. MARS, P., 1966, Recherches sur quelques étangs du littoral méditerranéen français et sur leurs faunes malacologiques. Vie et Milieu, 20 (Suppl.): 1-359. MIENIS, H.K., 1976, Ventomnestia girardi (Au- douin, 1827) from the Mediterranean. Conchiglie, 12: 209-210. MORRI, С. & С.М. BIANCHI, 1983, Contributo alla conoscenza degli idrozoi lagunari italiani: idropo- lipi del Delta del Po (nord Adriatico). Atti del Mu- seo civico di Storia naturale di Trieste, 35: 185— 205. MURILLO, L. & P. TALAVERA, 1983, Contribución al conocimiento de la malacofauna do Mar Menor (Murcia). /berus, 3: 15-28. OLMO, R. & J.D. ROS, 1984, Las malacocenosis del Mar Menor. Estudio y comparación con co- munidades de medios lagunares semejantes. Actas 6” Simposio lbérico del Estudio del Benthos Marino, Lisboa, 1: 253-260. PARENZAN, P., 1969, ll Mar Piccolo e il Mar Grande di Taranto. Thalassia salentina, 3: 19— 34. PARENZAN, P., 1970, Gasteropodi. Carta d'iden- tita delle conchiglie del Mediterraneo. 1. Bios- Taras, Taranto. 1-283 p. PARENZAN, P., 1979. Fauna malacologica dei laghi di Ganzirri e del Faro (Messina). Thalassia salentina, 9: 67-78. PERRONE, A., 1983, Opistobranchi (Aplysiomor- pha, Pleurobranchomorpha, Sacoglossa, Nudi- branchia) del litorale salentino (Mar lonio) OPISTHOBRANCHS OF A MEDITERRANEAN LAGOON 299 (Elenco-Contributo primo). Thalassia salentina, 13: 118-144. PERRONE, A., 1986, Il genere Doriopsilla Bergh 1880 in Mediterraneo: descrizione di Doriopsilla rarispina Pruvot-Fol 1951 (Opisthobranchia: Nudibranchia). Bollettino malacologico, Milano, 22: 97-112. PRUVOT-FOL, A., 1954, Mollusques opistho- branches. Faune de France, 58. 1-460 p. RIGGIO, S. 8 M.P. SPARLA, 1985, A survey of the invertebrate populations inhabiting Rytiphloea tinctoria (Clem.) C. Ag. aegagropyla in the Stag- none Sound (Western Sicily). Rapport de la Commission International pour l'Etude de la Mer Méditerranée, 29 (4): 143-144. RIVA, A. & N. VICENTE, 1976, Influence des fac- teurs du milieu sur la biologie de trois espèces de nudibranches: Aeolidiella alderi, Spurilla neapo- litana et Favorinus branchialis. |. Haliotis, 7: 39— 43. ROGINSKAYA, I.S., 1970, Tenellia adspersa, a nudibranch new to the Azov Sea, with notes on its taxonomy and ecology. Malacological Review, 3: 167- 174. ROS, J.D. & J. RODRIGUEZ, 1985, La simbiosis algal en Elysia timida Risso 1818. Primeros re- sultados. Anales de Biologia, Universidad de Murcia, 4: 37—47. SACCHI, C.F., 1961, Vivificazione marina e mala- cofauna nel lago salmastro litoraneo di Patria (Napoli-Caserta). Annuario dell'Istituto e Museo Zoologico dell’ Universita di Napoli, 13 (6): 1-37. SAUBADE, A.M., 1979, La malacofaune actuelle (Bivalves et Gastéropodes) de la lagune de Na- dor (cóte méditerranéene du Maroc). Bulletin de l'Institut Geologique du Bassin d'Aquitaine, 26: 69-90. SCHMEKEL, L., 1968, Ascoglossa, Notaspidea und Nudibranchia im Litoral des Golfes von Ne- apel. Revue Suisse de Zoologie, 75: 103-155. SCHMEKEL, L. & A. PORTMANN, 1982, Opistho- branchia des Mittelmeeres. Springer-Verlag, Ber- lin, 1-410 p. SCORDIA, C., 1927, La eurialinita di un mollusco opistobranchio allo stato giovanile. Rivista di Bio- logia, Milano, 9 (1): 3-42. SPARLA, M.P. & S. RIGGIO, 1984, Notes on the invertebrate fauna associated to the red alga Rytiphloea tinctoria (Clem.) C. Ag. aegagropyla in the Stagnone sound. Nova Thalassia, 6 (Suppl.): 105-111. TEMPLADO, J., P. TALAVERA & L. MURILLO, 1983, Adiciones a la fauna de Opistobranquios del Cabo de Palos (Murcia). |. /berus, 3: 47-50. THOMPSON, Т.Е. 8 С.Н. BROWN, 1984, Biology of Opisthobranch Molluscs, 2: Ray Society, Lon- don, 1-229 p. TORELLI, A., 1982, Gasteropodi conchigliati. Guide per il riconoscimento delle specie animali delle acque lagunari e costiere italiane. 8. CNR, Rome, 1-235 p. TORELLI, A., 1983, Notes malacologiques sur les étangs sales de la Sardaigne méridionale. Rap- port de la Commission International pour l'Etude de la Mer Méditerranée, 28 (6): 229-230. TORTORICI, В. 8 P. PANETTA, 1977, Notizie eco- logiche su alcuni Opistobranchi raccolti nel Golfo di Taranto. Atti Societa Italiana di Scienze Nat- urali, 118 (2): 249-257. VATOVA, A., 1940, Le zoocenosi della Laguna veneta. Thalassia, 3 (10): 1-25. ZAOUALI, J., 1974, La faune malacologique du Lac de Tunis (parties nord et sud) et de ses canaux (Canal Central, Canal Nord et Canal Sud). Hali- otis, 4: 179-186. ZAOUALI, J., 1979, Etude écologique du Lac de Bizerte. Bulletin de l'Office National de la Péche, Tunisie, 3 (2): 107-140. ZAOUALI, J., 1981, Etude malacologique de la frange côtière sud du Lac de Tunis nord. Haliotis, 11: 241-250. ZAOUALI, J., 8 S. BAETEN, 1985, Étude des pe- uplements animaux macro-benthiques de la zone centrale et du bassin oriental de la Mer du Bibans (Tunisie méridionale) par la méthode de l'analyse factorielle des correspondances. Rap- port de la Commission International pour l'Etude de la Mer Méditerranée, 29 (4): 199-203. ZUCCHI STOLFA, M.L., 1977, Gasteropodi recent delle lagune di Grado e Marano. Atti Societa Ital- jana di Scienze Naturali, 118 (2): 144-164. MALACOLOGIA, 1991, 32(2): 301-311 THE STATUS OF THE RHODOPIDAE (GASTROPODA: EUTHYNEURA) L. von Salvini-Plawen Institut fur Zoologie, Universitat Wien, A-1090 Wien IX, AlthanstraBe 14, Austria ABSTRACT Based on investigations of Rhodope veranii, R. transtrosa sp. nov. and Helminthope psam- mobionta gen. et sp. nov., the organization of the Rhodopidae is reconsidered. Helminthope is characterized by a slender body, by typical verrucose rods, by lack of a radula, stomach and dorso-rostral caecum, and especially by five free ganglia on the visceral loop. The animals inhabit the interstitia of subtidal sands. The number of ganglia confirms earlier developmental investigations in А. veranii with respect to the pentaganglionate (= euthyneurous) level. The shift of the visceral ganglion to the left side, as well as the lack of special vacuolar bodies in the epidermal cells, argue against a classification of the Rhodopidae within the Anthobranchia (= Doridacea) and the Nudibranchia. The lack of both a paired procerebrum and cerebral gland excludes a direct relationship of the Rhodopidae with the Gymnomorpha (Onchidiacea, Sole- olifera) and Pulmonata. Furthermore, the free visceral ganglion in Helminthope and the monauly preclude a classification of the Rhodopidae amidst higher tectibranch groups (= Paratectibran- chia). Consequently, the Rhodopidae, (including Helminthope and five presumed species of Rhodope) remain as a taxon Rhodopemorpha, of uncertain systematic rank and affinity, as a specialized off-shoot from the lower opisthobranchs. INTRODUCTION At the present time, the Rhodopidae are scientifically known only by the Mediterra- nean Rhodope veranii Kólliker and by the southwest Atlantic R. marcusi (see p. 308). Since the original description of Я. veranii (Kôlliker, 1847), few additional specimens have been found. Due to the investigations of Graff (1883), Böhmig (1983), and Riedl (1959,1960), however, we are fairly well in- formed about the anatomy, histology, biology, and development of this species; Marcus & Marcus (1952) supplemented this knowledge by the description of a closely related form (see p. 308). The central question about Rhodope concerns its phylogenetic affinities. After the definitive classification of the spe- cies as an euthyneurous gastropod (Riedl, 1960), its affinities within that subclass still remain uncertain (cf. Oberzeller, 1969; Sal- vini-Plawen, 1970; Tillier, 1984: 359). Further recent findings of Rhodope veranii, R. tran- strosa, and Helminthope psammobionta en- large our knowledge of the Rhodopidae and permit a re-evaluation of its systematic rela- tionships. Rhodope veranii Kôlliker Fifteen Rhodope veranii were recently found in one of the marine aquaria of the Zoo- 301 logical Institute (Universitat Wien) filled with sediment and secondary hard-bottom mate- rial from the Northern Adriatic Sea and the Gulf of Naples. In nature, Я. veranii appears to inhabit shallow subtidal areas with stones and Ulva growth (Graff, 1883: p.74; F Star- mühlner, pers. comm., for Rovigno/Istria; Sal- vini-Plawen in Arnaud et al., 1986: p 158). All specimens beyond 1 mm in length are char- acterised by the more or less distinctly T- shaped dorsal orange-red pigmentation (Riedl, 1960). In contrast to previously found animals with a maximum length of 4 mm (Graff, 1883: p.74; Riedl, 1960: p.297), the present individuals were distinctly larger, rang- ing up to 8 mm in length. The subepithelial spicules and the inconspicuous eyes are typ- ical. However, there is remarkable variation in the location of the genital opening: Graff (1883: p.79) confused the protonephridiopore with the male gonopore and the anus with the female opening (both located at the right pos- terior border of the transverse pigment bar, i.e. anterior to the middle of the body). Riedl (1959: his Fig. 2) located the genital opening at the right anterior border of the transverse pigment bar, irrespective of the state of contraction of the animals. Apparently the location of the go- nopore varies in different individuals. The ex- amination of six serially sectioned specimens (Riedl's and the present material) revealed that only one specimen possessed the genital 302 SALVINI-PLAWEN FIG. 1. Rhodope veranii: Two successive cross sections through the cerebral nervous ring in a specimen with the foregut (fg) outside the pedal commissure (pc). oc eye, sta statocyst. opening in the location indicated by Riedl; two animals show the gonopore laterally at the level of the perioesophageal central nervous mass (with embedded eyes visible, see Fig. 1), while three individuals show the genital opening distinctly anterior to the ganglia com- plex, viz. anterior to the eyes (in one the go- nopore is even located at the level of the mouth). In the concentrated nervous system the closely adjoining cerebro-pleuro-parieto- intestinal ganglia (cf. Riedl, 1960; Oberzeller, 1969) have a short cerebral commissure and the eyes as well as optical ganglia incorpo- rated (Fig. 1); the optical connective itself has its origin in the pleuropedal connective. Be- sides the buccal connectives, there are three pairs of rostral nerves, the two medial ones with a common (?) root running to the oral region (labial nerves). The most lateral one at each side corresponds to the Hancock’s or rhinophoral nerve in other opisthobranchs and has a basal swelling which shows a dou- ble root in the cerebral ganglion; there is no head-shield-tentacle nerve (Huber, 1987). In addition, a strong lateral nerve, with bifur- cated root in both the (cerebro-) pleural gan- glion and the pedal ganglion, runs anterior- laterally to the body flanks; at the right it also innervates the copulatory organ. The two ab- dominal ‘nerves’ (right-visceral and left-gen- ital) running ventrally close to the body end are regularly provided with nuclei, thus as- suming the aspect of weak medullary cords. A peculiarity was noticed in one of the speci- mens: instead of being surrounded by the mass of the concentrated ganglia, the oe- sophagus runs outside (i.e. below) the pedal comissure (Fig. 1). The midgut shows the usual, somewhat winding, rostral caecum or right midgut gland (Riedl, 1960: p. 284). Close to the junction of the short intestine and the voluminous midgut there is a narrow pouch or small diverticulum. In both Riedl’ s and the present material, this pouch is lined with a low, ciliated epithelium that is histologically continuous with the intes- tinal epithelium. In contrast to Böhmig (1893: p.56 & Fig. 13), however, this pouch is well separated from the adjacent intestine, and, in agreement with Riedl (1960: pp.284-285), it corresponds to the remnant of the true stom- ach. The chromosome number of Я. veranii is 2n=32 (pers. comm. Claudia R. Schweizer, Wien). The spermatozoa, with a spiralated head, have a characteristic shape and fine structure; in some aspects they appear to be fairly primitive and similar to prosobranch sperm (pers. comm. F. Giusti di Massa, Siena). Rhodope transtrosa sp. nov. A single specimen (Fig. 2A) was collected from an aquarium (Ehrmann Zoo, Wien XII) filled with phytal material from the tropical Indo-Pacific (Ceylon/Sri Lanka ?). The living animal measured 1.65 mm x 160 um maxi- mum. The anterior third of its whitish body is provided with a characteristic dorsal trans- verse bar (transtrum) of orange-reddish pig- mentation (about 160 „um in length). The an- teriormost section is markedly elongated and STATUS OF THE RHODOPIDAE i 4 il N 1 , wre OV ag eS 1 AR D 2 ETS ns 30m FIG. 2. Rhodope transtrosa: A: living animal (1.65 mm); B: semi-preserved animal; C: contracted animal; D: arrangement of organs as seen from the right side in preserved animal; E: spicules. a anus, ag adhesive gland, e eye, fg foregut, gg genital gland, go genital opening, o outlet of oral glands, ov ovarial sac, p protonephridiopore, sc spermatocyst, so hermaphroditic duct, t testicle, vg visceral ganglion. acts as a highly-bendable snout with subfron- tal mouth opening; in the contracted state this snout may be retracted far into the subse- quent, still pre-ocular section. The eyes are clearly visible in life. The body is somewhat truncated terminally due to the distinct adhe- sive organ. The spicules are fairly densely ar- ranged and are slightly curved with a faintly 303 304 SALVINI-PLAWEN verrucose surface. They measure 150-170 um x 14-17 рт (Fig. 2E). The internal organization closely resem- bles that of Я. veranii, but there are some distinct differences. Ventral to the subterminal mouth, a short median sac bearing the pe- ripherally arranged oral glands opens (the glands are arranged as a paired cluster in Я. уегапй and R. marcusi). The foregut shows а precerebral enlargement with taller epithe- lium, but no pharyngeal bulb. This section re- ceives the salivary glands in paired arrange- ment. Immediately behind the central nervous complex the foregut leads dorsally into the sac-like midgut (midgut-gland). The latter forms an elongated organ extending from above the foregut to the posterior end of the body; in the preserved animal, there are sev- eral contraction-folds along its course, but no actual winding. Somewhat behind the mid-length of the body, the short intestine emerges dorsally from the sac-like midgut and runs directly, without any winding, to the right. It opens laterodorsally closely behind the laterodorsal protonephridiopore, both be- ing located (in contrast to Я. veranii and R. marcusi) posterior to the middle of the body (preserved animal). Immediately adjacent, and to the left of the intestine, a small but distinct posteriorly directed pouch or divertic- ulum is present; this corresponds to the rem- nant of the true stomach in Я. уегапи. The nervous system largely resembles that of R. veranii with respect to the general ar- rangement of the ganglia and, on each side, the two proximally joined labial nerves, the double root of the rhinophoral nerve, the bi- furcated (pleural and pedal) root of the lateral nerve, and the optical ganglion emerging with its connective from the pleuropedal con- nective. Differences are evident in the less concentrated state of the ganglia with the dis- crete statocysts between the cerebro-pleuro- parieto-intestinal ganglia and the pedal gan- glia, the discrete optic ganglia, the strong parapedal commissure, the fairly free and median visceral ganglion, as well as the sym- metrical origin of the right visceral and left genital medullary nerves (cf. Huber, 1987). In the hermaphroditic genital system there is a 55 x 45 um terminal testicle and a much larger testicle (70 x 50 рт) more anteriorly on the left. The median hermaphroditic duct then connects two ovarial sacs on the left, one on the right, and two more on the left (these be- ing located anterior to the anal region of the body). Approximately half way between the intestine and the central ganglia complex the spermoviduct turns to the right and continues in the form of a narrow connection with an enlarged portion filled with sperm. In contrast to Я. veranii and more similar to Я. marcusi, this sac represents a distinct elaboration (spermatheca) rather than a simple enlarge- ment of the spermoviduct (as in Я. veranii). It opens anteriorly into a three-lobed glandular complex (albumen and mucus glands) from which the genital duct runs antero-laterally to open on the right at the level of the cerebral ganglia and eyes. In contrast to R. veranii and R. marcusi, no copulatory organ is developed in the present specimen. Helminthope psammobionta gen. et sp. nov. This mesopsammic species comes from the western North Atlantic. Specimens were collected by R. Rieger (Innsbruck) and W. Sterrer (Bermuda) from Bermuda (North Rock reef and Tobacco Bay, at 8-10 т depth), North Carolina (30 т depth) and Georgia (2 т depth). They inhabit fairly clean, coarse sub- tidal sands (cf. Rieger & Sterrer, 1975: pp. 263-264 & their Figs. 34-35). The present animals ranged between 1 mm and about 2.5 mm in length (Figs. 3—4) and are circular in cross section (diameter 60-150 um), but are able to contract by 30-50%. They are whitish with black eyes; in transmitted light they ap- pear transparent-colourless with a darker, somewhat greenish tinge to the midgut. The body openings are almost invisible as two cil- iated patches arranged one close behind the other on the right anterior side. These patches indicate the sites of the protonephrid- iopore and the anus. The genital opening could not be seen. Because of its internal or- ganization (below), the present specimens are defined as Helminthope psammobionta gen. et sp. nov. (Figs. 3—4). All three specimens sectioned were unfor- tunately poorly preserved for histological ex- amination, so only an outline of the body or- ganization can be given. The entire body is covered by ciliated epidermal cells among which gland cells are interspersed. In no ani- mal could a definite terminal gland be seen (in contrast to Rhodope veranii, R. marcusi and R. transtrosa; see Fig. 2D). The loosely and irregularly arranged spicules measure be- tween 45 x 5.5 um and 70 x 7 рт, and they are weakly curved to slightly angled or geni- culate in shape (Fig. 4C). Towards their tips the spicular surface is generally roughened, STATUS OF THE RHODOPIDAE 305 FIG. 3. Helminthope psammobionta: living specimen (about 1.5 mm in size) from Bermuda. and some spicules seem to be hollow (Rieger & Sterrer, 1975: Fig. 34). The spicules are situated in the fibrous connective tissue di- rectly below the epidermis and are sur- rounded by a spicule-forming cell (Rieger & Sterrer, 1975: Fig. 35). In addition to the elon- gate spicules (similar to those in Я. veranii (Graff, 1883: p.75-76) or Я. transtrosa (Fig. 2E)) very small and platelet-like elements are embedded subepithelially. As indicated by the high contractility of the body, there is a well- defined longitudinal musculature; no regular circular fibres could be seen. The alimentary canal begins with a subter- minal mouth. This leads into a narrow foregut which soon widens and is lined with a tall ciliated epithelium surrounded by circular muscle fibres (pharynx). A pair of ill-defined salivary glands accompany the foregut dor- solaterally. In the region of the cerebral ner- 306 SALVINI-PLAWEN mo cer 50 um mc FIG. 4. Helminthope psammobionta: specimen from North Carolina gliding (A) and in contracted state below cover glass (B); C: spicules; D: main internal organization. acc accessory ganglia, anc right abdominal nerve cord (= visceral nerve), buc buccal ganglion, cer cerebro-pleural ganglion, gl epidermal glands, gt genital tube (spermoviduct), mc area of (reduced) mantle cavity, mg midgut, mo mouth opening, opt optic ganglion, par parietal ganglion, ped pedal ganglion, ph pharynx, sbi sub-intestinal ganglion, spi supra-intestinal gan- glion, sta statocyst, vis visceral ganglion. STATUS OF THE RHODOPIDAE 307 vous ring the foregut narrows again. Behind the pedal ganglia the oesophagus connects to the midgut. There is no antero-dorsal cae- cum (right digestive gland). The midgut rep- resents a homogeneous tube-like organ with high glandular epithelium extending the length of the body. There is no histological break during the course of the midgut except for the almost total disappearance of the lumen in the terminal portion (representing the posterior = left midgut gland?). The lu- men is also restricted to a somewhat nar- rower space posteriorly due to the genital or- gans. The intestine emerges from the midgut dorsolaterally (approximately 100 jm behind the visceral ganglion) and runs obliquely di- rect to the lateral anus. Only in one specimen could an organ closely associated with.-the anus and extending a short distance anteri- orly be discerned, probably the protonephrid- ium. In the nervous system apart from the cere- bro-pleural complex all ganglia are separate (Fig. 4D). The fused cerebro-pleural ganglia still show a mid-dorsal incisure and a distinct cerebral commissure; the pleural portion is separated by an accumulation of nuclei. An- teriorly, at least two pairs of cerebral nerves (the labial and the Hancock’s/rhinophoral) leave the ganglia. Very characteristic is the presence at each side of two complexes of accessory ganglia. These appear to be incor- porated in the course of the cerebral nerves, each complex assuming two to three swel- lings. A short connective runs from each cerebral ganglion to the respective pedal ganglion and a strong, terminal cerebropleural connective splits to connect with the optic, the parietal, and the pedal ganglion, as well as the buccal ganglion at each side. The buccal ganglia themselves are well separated and lie behind the statocysts. The small optic ganglia with the embedded eyes are separate from the ce- rebral ganglia and are located above the pedal ganglia (Figs. 4A,D). Each of the latter is very prominent and shows an anterior lobe. A lateral nerve of the pedal ganglion emerges at each side close to the pleuropedal connec- tive. The statocysts, each with a single stato- lith, are close by, but they are separate from the ganglia and main nerves. The parietal ganglia are widely separated from the cere- bral complex. On the right a strong connec- tion exists to the supra-intestinal ganglion la- teroventrally to the midgut, and to the left a much longer connective leads to the (ventro) lateral sub-intestinal ganglion. Both connec- tives unite in the mid-ventral visceral or ab- dominal ganglion, which appears to be lo- cated at a fairly constant distance of about 135 jm from the beginning of the cerebral ganglia. In histological continuation of the right (supra-intestinal) connective the strong genital 'nerve' emerges from the left portion of the ganglion and runs posteriorly as the left cord, and the left connective continues into the right cord (visceral nerve). Thus, there is a chiasma of fibres in the visceral/abdominal ganglion reflecting the only remaining trace of streptoneury. Furthermore, both abdominal ‘nerves’ terminate together with the midgut- sac and exhibit a regular coat of nuclei. They thus assume the aspect of medullary cords and each gives off a strong anterior branch (Fig. 4D). The genital system is absent in one speci- men, is represented only by the rudiment of a simple tube extending below the midgut in a second specimen, and is not fully differenti- ated in the third sectioned individual. In the latter two individuals, the anteriormost part of the genital system is represented by a narrow tube extending posteriorly from between the buccal ganglia; the outer portion and genital Opening could not be discerned and still ap- pear to be absent. The genital tube (sperm- oviduct) gradually enlarges posteriorly where it is lined with a high, glandular epithelium without a _ well-defined lumen (prostate gland?). The tube then continues posteriorly between the midgut and nervous system, its epithelium decreasing again in size toward the anal region. More posteriorly, approxi- mately 850 um from the anterior tip of the body (about 600 um behind the visceral gan- glion or 500 um behind the anal region), the simple tube enlarges again to become a weakly ciliated vesicle filled with spermatozoa (spermatheca). This vesicle opens dorsally with its terminal narrowed portion into a volu- minous (albumen and mucus) gland, the an- terior region of which is lined by densely granulated and ciliated cells which are then replaced posteriorly by large slime cells. A narrow, ciliated duct continues from this gland and appears to become a ramified germ gland. This latter condition could not, how- ever, be ascertained in detail, and only some accumulation of sperm in vesicles (testicles) were observed. Thus, as is Rhodope veranii (Riedl, 1960:p.299), the present new species also appears to be protandric (gonochorism is also possible). 308 SALVINI-PLAWEN Systematic Discussion of the Rhodopidae In contrast to Rhodope veranii, R. tran- strosa and R. marcusi (see pp. 300, 302), the new type Helminthope psammobionta is cha- racterized and defined by the wide nervous system with free ganglia and the differentia- tion of precerebral (= accessory) ganglia, by the axial connection of the foregut and midgut without anterior caecum, and by the lack of a ventroterminal adhesive gland. These cha- racteristics indicate that it belongs to a distinct genus. It is also characterized by the elongate body without pigmentation, the less verrucose and smaller spicules, the far posterior location of the spermatheca and the presence of the albumen/mucus genital gland behind it, as well as the interstitial habitat. There is, how- ever, no doubt that He/minthope is a rhodopid characterized by a pentaganglionate visceral loop with medullary visceral and genital nerves, subepidermal spicules, reduced mant- le cavity on the right side (anus and proto- nephridiopore), lack of a shell, radula, jaws, stomach, heart, and head-shield/tentacles. The systematic roundabout of the Rhodo- pidae is summarized in Riedl (1959). With re- spect to the developmental characters and the pentaganglionate visceral loop, the family definitely belongs to the Pentaganglionata = Euthyneura (Riedl, 1960: pp.303-312; Sal- vini-Plawen, 1970; Haszprunar, 1985). A more precise classification has assumed a close affinity to the Soleolifera and Onchidia- cea with the inclusion of all three groups within a separate euthyneuran subclass Gym- nomorpha (cf. Riedl, 1960; Oberzeller, 1959; Salvini-Plawen, 1970; Arnaud et al., 1986). Such a classification cannot, however, be up- held because the present investigations de- monstrate that neither Rhodope nor Hel- minthope possess a procerebrum and/or cerebral glands. This special neurosecretory/ neurohaemal system is characteristic of the Pulmonata and Gymnomorpha (cf. Haszpru- nar, 1985). In addition, both groups (= clade of Aeropneusta) are characterized by the ab- sence of a postero-lateral cerebral nerve equivalent to the Hancock’s or rhinophoral nerve present in Rhodopidae as in all other opisthobranchs (Huber, 1987). Thus, the Rhodopidae cannot be included within one of these two supra-orders (Fig. 5). On the other hand, the slug Smeagol manneringi (Climo, 1980), which due to the (inaccurate) original description had been excluded from the Gym- nomorpha (Haszprunar, 1985; Arnaud et al., 1986), in fact belongs to the supra-order Gymnomorpha: a re-examination has re- vealed the presence of a procerebrum and of cerebral glands which, together with other characters, place the species in closer affinity to the Onchidiidae (pers. comm. G Haszpru- nar; cf. Arnaud et al., 1986: p.175). An ultrastructural investigation of the inte- gument of Rhodope veranii (pers. obs.) and Helminthope (Rieger & Sterrer, 1975: their Fig. 35) demonstrates that there are no special vacuolar cells provided with vesicles (amphidisk-like inclusion; cf. Schmekel, 1982,1985) and consequently the Rhodo- pidae cannot be classified within the Nudi- branchia s.s. (= less Doridacea). Because, on the other hand, investigated members of Pseudovermis (Aeolidacea: Heteroprocta) possess vacuolar cells (pers. obs.), their lack in Rhodopidae could perhaps be correlated with the diminutive size (as accessory ganglia appear to be) or the special habitat. An iden- tical argument would be valid with respect to the Anthobranchia (= Doridacea or Holohe- patica or ‘(Eu-)Ctenidiacea’ ) which have special vacuolar cells in the rhinophores (cf. Kress, 1981; Schmekel, 1985); because, however, all tentacles are reduced in the Rhodopidae no comparison is possible here. Up to the present, the configuration of the nervous system provided a valid argument to exclude Rhodope from the Anthobranchia (as well as from Pleurobranchomorpha and Nudi- branchia s.s.; cf. Salvini-Plawen, 1970). The presence of the visceral/abdominal ganglion in Rhodope veranii on the left side, or almost fused with the sub-intestinal ganglion (Riedl, 1960; Oberzeller, 1969), is the opposite of the condition found in the Eleutherobranchia (Pleurobranchomorpha, Anthobranchia and Nudibranchia; cf. Haszprunar, 1985). Against this argument, however, the more conserva- tive configuration in Helminthope (Fig. 4) and even in Я. transtrosa still makes any concen- tration possible. This is a renewed confirma- tion that the position of the visceral ganglion on the left side is a convergence. On the other hand, the visceral ganglion in Bullomorpha, Aplysiomorpha = Anaspidea, and Sacco- glossa (except the Cylindrobullidae, cf. Burn, 1966), as well as in Umbraculomorpha, Ac- ochlidiomorpha, and Gymnosomata, is al- ready fused to the left side (generally with the sub-intestinal ganglion). Because Я. tran- strosa and Helminthope show а well- separated visceral ganglion, no link can be proposed among these more advanced tecti- STATUS OF THE RHODOPIDAE 309 PRARREABTA RACE TE ABARCA UN OCAH LOA ЕЕ ТНЕВОВВАМСНТА СУММОМОВРНА PULMONATA | Bullomorpha Saccoglossa Anthobranchia Thecosomata Acochlidiomorpha Nudibranchia [prespióss Umbraculomorpha | Gymnosomata | | | | | | | | | Pleurobranchomorpha | | | | U d'avanu le | without blood gland with blood gland | | ARCHITECTIBRANCHIA e monaulic Rhodopemorpha СЕМ töhlyän eu ra) Pyramidellomorpha (Streptoneura) FIG. 5. Relationship of Rhodopemorpha within pentaganglionate (= euthyneurous) gastropods: 1 = Strep- toneura with epiathroid nervous system, tentacle nerves bifurcated, parapedal commissure; heterostrophy; mantle cavity with two opposed ciliary tracts and devoid of ctenidia; eggs united by chalazae, spiral type of sperm with glycogen helices within midpiece. 2 = Eyes median of tentacles; cerebral ganglia with giant cells, pedal ganglia with lateral nerve; with paired rhinophoral (= Hancock's) nerve; small animals with reduction of paired oralis nerve. 3 = Elongation of head-pedal complex with parietal ganglia; with pallial caecum and repugnatorial glands. 4 = Opisthobranchia: Head-shield with bifurcated tentacle (= clypeo-capitis) nerves; Hancock’s sense organs with external branch of labiotentacularis nerve. 5 = Procerebrum with cerebral glands and dorsal bodies; small animals (= without oralis nerves), anterior shift of female genital opening outside the mantle cavity and restriction of the opening of mantle cavity: Aeropneusta; loss of paired rhinophoral nerve. 6 = Anterior gizzard. 7 = Disintegration of head-shield; visceral ganglion migrates to the right side to fuse primarily with the supra-intestinal ganglion; chromosomes restricted to generally 12-13 pairs. 8 = Mantle cavity reduced to ‘cloaca’, or lost; loss of shell, pedunculated eyes. 9 = Mantle cavity becomes a ‘lung’. branchs (= Paratectibranchia, below). Fi- nally, the bifurcated lateral nerve in Rhodope (see p. 300), the chromosome number in Rhodope veranii with n= 16 appears to be of (see pp. 300 and 302) has a similar origin in several Nudibranchia. However, because it corresponds to the purely latero-pedal nerve in Helminthope and other Euthyneura (Huber, 1987; see Fig. 5), this similarity between Rhodope and those nudibranchs appears to be convergent due to concentration. Whereas the structure of the spermatozoa gives little evidence of phylogenetic value more interest. The general chromosome numbers in Eleutherobranchia are n=12 (Pleurobranchomorpha) or n=13 (Antho- branchia and Nudibranchia), in Saccoglossa n=17 (except for Bosellia : n=7), and in other Tectibranchia likewise n=17 (see Burch, 1967; Schmekel, 1985; Vitturi et al., 1985). Exceptions (so far as known) include the cephalaspideans Scaphander, Hami- 310 SALVINI-PLAWEN noea, Philine aperta and two Smaragdinel- lidae with n=18, Philinoglossa with n=13, the anthobranch Platydoris with n=12, two Aplysia species (Anaspidea) with n= 16, as well as the dendronotacean nudibranch Tethys leporina with n=16 (see Curini-Gal- etti, 1985; Vitturi et al., 1985). These two latter exceptions, as well as the chromosome num- ber n= 16 in Veronicella (Gymnomorpha) and the lower pulmonates Siphonaria and Baker- ilymnaea (cf. Burch, 1967), are of special in- terest since they demonstrate a polyphyletic decrease of the chromosome number n= 17 along with anagenesis (in higher pulmonates, the number of chromosomes is generally in- creased; cf. Burch, 1967). Thus, the number n=16 in Rhodope appears to show that the Rhodopidae cannot be directly linked with one of the present orders, but rather it de- monstrates the primitive level still reflected in some Anaspidea, Nudibranchia, Gymnomor- pha, and lower Pulmonata. The monauly in the genital apparatus of Helminthope as well as of Rhodope (though with possible incipient functional diauly in А. veranii; cf. Böhmig, 1893: p.81) excludes a closer relationship to the diaulic Eleuthero- branchia, Sacoglossa, and Anaspidea (see Fig. 5). In addition, it is interesting to note that the gonad includes separate testicles and ovaria, a condition only known in several Streptoneura. In conclusion, the pentaganglionate Rho- dopidae cannot, on the one hand, be directly linked with Gymnomorpha and Pulmonata, nor, on the other hand, can they be classified within the Eleutherobranchia (Pleurobrancho- morpha, Anthobranchia, and Nudibranchia), Saccoglossa, or Anaspidea. The Rhodopidae share only a general level of organization with several tectibranch gastropods. According to a recent analysis by Haszprunar (1985), how- ever, the tectibranchs should be subdivided into the conservative group of Architectibran- chia (Diaphanoidea, Ringiculoidea, Acteo- noidea) and the other more advanced tecti- branchs (Fig. 5); this latter group preferably should be named Paratectibranchia (Salvini- Plawen, 1988), and are monophyletically characterized by a gizzard (if not secondarily reduced). Since the two proximally joined labial nerves on each side in Rhodope (ac- cording to Huber 1987) correspond to the in- ternal plus external branch of the labiotenta- cularis nerve, such condition would the Rhodopidae unequivocally classify within the opisthobranchs (i.e. above the level 4 in Fig. 5). At the present time, the characters of the Rhodopidae only permit this family to be classified as a taxon Rhodopemorpha nov. of uncertain systematic rank representing a highly specialized offshoot of the lower opisthobranchs (Fig. 5). Recent Rhodopemorpha, with at present the single family Rhodopidae, include the fol- lowing three phytal and three interstitial mem- bers (cf. Rieger & Sterrer, 1975: p.262-265; Arnaud et al., 1986: p.158,171): 1. Rhodope veranii Kólliker, 1847, from the Adriatic Sea and the adjacent Mediterranean, measures 1—8 mm and inhabits shallow sub- tidal areas with stones and Ulva. It is charac- terized by an orange-red, roughly T-shaped dorsal pigmentation as well as by verrucose and more pointed, slightly bent spicules of 90-200 um length. Reduced mantle cavity anterior to the middle of the body. 2. Rhodope marcusi sp. nov. (= R. veranyi Marcus & Marcus, 1952, nec Kólliker, 1847; = Rhodope species A in Arnaud et al., 1986: p.158) comes from the Bay of Santos (Brazil, off Sao Paulo) and lives in the rocky or stony tidal zone among Sargassum stenophyllum and Padina. In contrast to Я. veranii Kólliker, and to Я. transtrosa (below), the с. 2 mm long specimens are characterized by the lack of orange-red pigmentation, by the crescent shaped spicules, and by the position of the reduced mantle cavity with anus and proto- nephridiopore in the mid-length of the body (cf. Marcus & Marcus, 1952). 3. Rhodope transtrosa sp. nov. is at present known only by a single specimen from an aquarium filled with phytal material from trop- ical Indo-Pacific waters. It is characterized by an orange-red transverse bar at the anterior third of the 1.65 mm long and slender body, as well as by scarcely verrucose, slightly curved spicules of 150-170 x 14-17 ¡um size. The reduced mantle cavity is located some- what posterior to the middle of the body; differences in the internal characters are as indicated above. Type: Naturhistorisches Mu- seum, Wien, No. 83438. 4. Rhodope species D was recorded from coarse shell-sand at 25 m off Bergen, Norway by Karling (1966). This colourless specimen is 1.5 mm long and accordingly should al- ready possess the reddish T-pigmentation if conspecific with Я. veranii. It is possibly con- specific with the specimens found in shell- sand at 50 m by Swedmark (1958: p.61) and off Madeira by Langerhans (in Graff, 1883: p.74-75). This eastern Atlantic species pos- STATUS OF THE RHODOPIDAE 311 sesses slightly curved verrucose rods (65— 100 рт) and pointed spicules similar to R. veranii, as well as ramified elements (cf. Kar- ling, 1966). 5. Rhodope (?) crucispiculata sp. nov. (= Rhodope «species С in Arnaud et al. 1986) was collected by Christine Schöpfer- Sterrer from subtidal sand at 14 m from the coast of Tunisia (cf. Rieger & Sterrer, 1975: p.262, 265). Though certainly immature (400 um in size), this species is defined and easily recognizible by the densely arranged, regu- larly cross-shaped spicules (25-60 um) with central hole. 6. Helminthope psammobionta gen. et sp. nov. (= Rhodope species B in Arnaud et al., 1986). The new genus and species is characterized as described above. Type: Naturhistorisches Museum, Wien, No. 83439. LITERATURE CITED ARNAUD, P.M., C. POIZAT, & L. von SALVINI- PLAWEN, 1986, Marine-interstitial Gastropoda. In: BOTOSANEANU, L. ed., Stygofauna mundi. Brill, Leiden, p. 153-176. BOHMIG, L., 1893, Zur feineren Anatomie von Rhodope veranii Kólliker. Zeitschrift für wissen- schaftliche Zoologie, 56: 40-116. BURCH, J.B., 1967, Cytological relationships of some Pacific gastropods. Venus, 25: 118-135. BURN, R., 1966, The opisthobranchs of a cauler- pan microfauna from Fiji. Proceedings of the Ma- lacological Society of London, 37: 45-65. CLIMO, F M, 1980, Smeagolida, a new order of gymnomorph molluscs from New Zealand based оп a new genus and species. New Zealand Jour- nal of Zoology, 7: 513-522. CURINI-GALETTI, M.C., 1985, Chromosome mor- phology of Philinoglossa praelongata (Gas- tropoda Cephalaspidea). Journal of Molluscan Studies, 51: 220-222. GRAFF, L у, 1883, Uber Rhodope veranii Kólliker. Morphologisches Jahrbuch, 8: 73—84. HASZPRUNAR, G., 1985, The Heterobranchia—a new concept of the phylogeny of the higher Gas- tropoda. Zeitschrift für zoologische Systematik und Evolutions-forschung, 23: 15-37. HUBER, G., 1987, Zum cerebralen Nervensystem mariner Heterobranchia (Gastropoda). Unpub- lished Dissertation an der Formal- und Naturwis- senschaftlichen Fakultat der Universitat Wien. KARLING, T., 1966, Rhodope veranyi (Gastro- poda, Euthyneura) von der norwegischen Küste. Sarsia, 24: 33-35. KOLLIKER, A., 1847, Rhodope, nuovo genere dei Gastropodi. Giornale del’ |. R. Instituto Lombardo di science, lettere ed arti, 16: 239-249. KRESS, A., 1981, A scanning electron microscope study of notum structures in some dorid nudi- branchs (Gastropoda, Opisthobranchia). Journal of the Marine Biological Association, U.K., 61: 177-191. MARCUS, Е. du B.-R., & Е. MARCUS, 1952, The nudibranch Rhodope from South America. Co- municaciones zoologicas del Museo de Historia natural de Montevideo, 4 (68): 1-8. OBERZELLER, E., 1969, Die Verwandtschaftsbez- iehungen der Rhodope veranii Kólliker zu den Oncidiidae, Vaginulidae und Rathousiidae in Be- zug auf das Nervensystem. Malacologia, 9: 282— 283. RIEDL, R., 1959, Beitráge zur Kenntnis der Rhodope veranii. Teil |, Geschichte und Biologie. Zoologischer Anzeiger, 163: 107-122. RIEDL, R., 1960. Beitráge zur Kenntnis der Rhodope veranii. Teil Il, Entwicklung. Zeitschrift für wissenschaftliche Zoologie, 163: 237-316. RIEGER, R., & W. STERRER, 1975, New spicular skeletons in Turbellaria, and the occurrence of spicules in marine meiofauna (Part I). Zeitschrft fur zoologische Systematik und Evolutionsfor- schung, 13: 207-248. SALVINI-PLAWEN, L. von, 1970, Zur systematis- chen Stellung von Soleolifera und Rhodope (Gastropoda, Euthyneura). Zoologisches Jahr- buch (Abt. Systematik), 97: 285-299. SALVINI-PLAWEN, L. von, 1988. The structure and function of molluscan digestive systems. In: TRUEMAN, E.R. & M. R. CLARKE, eds., The Mollusca, volume 11, Form and Function. Aca- demic Press, San Diego & London, p. 301-379. SCHMEKEL, L., 1982, Vonkommen und Feinstruk- tur der Vakuolenepidermis von Nudibranchiern (Gastropoda Opisthobranchia). Malacologia, 22: 631-635. SCHMEKEL, L., 1985. Aspects of evolution within the opisthobranchs. In: TRUEMAN, E. R. & M. R. CLARKE, eds., The Mollusca, volume 10. Evolu- tion. Academic Press, Orlando, Fla & London, p. 221—267. SWEDMARK, B., 1958. Psammodriloides fauveli n. gen., п. sp. et la famille des Psammodrilidae (Polychaeta, Sedentaria). Arkiv for Zoologi, (2) 12: 55—65. TILLIER, $, 1984. Relationships of gymnomorph gastropods (Mollusca: Gastropoda). Zoological Journal of the Linnaean Society, 82: 345-362. VITTURI, R., E. CATALANO, M. MACALUSO & N. PARRINELLO, 1985, The chromosomes in cer- tain species of the sub-class Opisthobranchia (Mollusca, Gastropoda). Biologisches Zentral- blatt, 104: 701-710. MALACOLOGIA, 1991, 32(2): 313-327 MORPHOLOGICAL PARALLELISM IN OPISTHOBRANCH GASTROPODS Terrence M Gosliner Department of Invertebrate Zoology and Geology, California Academy of Sciences, Golden Gate Park, San Francisco, California 94118, U.S.A. ABSTRACT Opisthobranch gastropods exhibit parallel evolution in most of their organ systems. Levels of 60-80% parallelism of characters are not uncommon in many opisthobranch taxa. High levels of parallelism have traditionally produced difficulties in the classification of opisthobranchs and persist when modern phenetic and cladistic methods are employed. Examples from many ceph- alaspidean taxa demonstrate the minimum levels of parallelism present in opisthobranchs when parsimony methods are used. Strict adherence to statistically parsimonious evolution may yield phylogenies that are not parsimonious from a functional or adaptive point of view. Classification of opisthobranchs, at all systematic levels, is profoundly affected by parallelism. Historical dif- ficulties of classifying some Sacoglossa with aeolid nudibranchs is a manifestation of parallel evolution. Cladistic classification of members of several families of cephalaspideans by parsimony methods produces erroneous relationships that reflects grades of organization rather than phy- logeny. The subdivision of the aeolid nudibranch family Aeolidiidae into genera is also problematic owing to parallel evolution. On the basis of synapomorphy, the Akeridae must be regarded as anaspideans rather than cephalaspideans. Schmekel’s separation of the Umbraculomorpha as a distinct order is unwarranted, and is based upon erroneous assumptions of monophyletic change of the reproductive and central nervous systems within the opisthobranchs. INTRODUCTION Recent studies on parallel evolution in opis- thobranch gastropods (Gosliner & Ghiselin, 1984; Gosliner, 1985a) have focused on the theoretical aspects of parallelism and their im- plications to phylogenetic methodology. While these papers provide examples of parallelism in the opisthobranchs, the morphological de- tails of much of this work have yet to be pre- sented. As previously discussed (Gosliner & Ghiselin, 1984), parallelism occurs in most major organ systems within the Opisthobran- chia and may occur at all systematic levels. Interpretations of parallelism have led to dif- fering views of the classification and phylog- eny of the opisthobranchs. Examples include the Opisthobranchia in general (Ghiselin, 1966; Schmekel, 1985), the Sacoglossa (Rus- sell, 1929) and the aeolidiid nudibranchs (Gos- liner, 1985b). A review of the organ systems within the Opisthobranchia is here provided to demon- strate the morphological diversity present within the subclass and to suggest the extent to which parallel evolution has occurred. METHODS In the present study a wide variety of opisthobranch taxa were dissected both to 313 verify published morphological observations and to provide additional data (Table 1). Whenever possible, morphological observa- tions described in the literature were verified. Most major organ systems were examined, including the shell, operculum, mantle com- plex, digestive system, central nervous sys- tem and reproductive system. The variability of structures within and between taxa was com- pared. Polarity of some morphological characters in the Opisthobranchia has been previously discussed (Gosliner, 1981a; Schmekel, 1985). In order to further ascertain the polarity of mor- phological transformation series, outgroup comparison was employed at a variety of sys- tematic levels. The outgroups utilized for the entire Opisthobranchia include the probable sister group of the opisthobranchs, the Pul- monata. Other taxa used as outgroups were the Heterogastropoda and various other me- sogastropods. Functional arguments to estab- lish polarity, as advocated by Gosliner & Ghis- elin (1984), ontological sequences and palaeontological data were also employed to augment outgroup comparison methods of de- termining polarity. RESULTS The morphological variability of the various organ systems within the Opisthobranchia is 314 GOSLINER TABLE 1. Summary of taxa studied. [* indicates type species of genus]. Sources of material: ANSP Academy of Natural Sciences, Philadelphia, Pennsylvania. CAS California Academy of Sciences, San Francisco, California. EM Dr Eveline du Bois Reymond Marcus, University of Sao Paulo, Brazil. GCW Dr Gary C Williams, South African Museum, Cape Town. HB Dr Hans Bertsch. KM Ms Kaniaulono Meyer, University of Cincinnati, Ohio. LACM Los Angeles County Museum, California. LGH Dr Larry G Harris, University of New Hampshire, Durham, New Hampshire. MCZ Museum of Comparative Zoology, Harvard University, Cambridge,Massachusetts. MLG Mr Michael L Gosliner, Takoma Park, Maryland. MNHN Muséum National d'Histoire Naturelle, Paris, France. RB Dr Robert Beeman, San Francisco State University, California. SM Ms Sandra Millen, University of British Columbia, Vancouver, Canada. YPM Peabody Museum, Yale University, New Haven, Connecticut. Taxon Locality Source of Material Order CEPHALASPIDEA Family Ringiculidae Ringicula nitida Verrill, 1872 Family Acteonidae Acteon hebes Verrill, 1885 *Rictaxis punctocaelatus (Carpenter, 1864) Pupa nitidula (Lamarck, 1816) Psp: P. sp. Il Family Hydatinidae *Hydatina physis (Linnaeus, 1758) H. zonata (Lightfoot, 1786) *Micromelo undata (Bruguière, 1792) *Parvamplustrum tenerum Powell, 1961 Family Scaphandridae *Scaphander lignarius (Linnaeus, 1758) S. punctostriatus (Mighels, 1841) S. mundus Watson, 1883 S. gracilis Watson, 1883 S. nobilis Verrill, 1884 Acteocina. bidentata (Orbigny, 1841) A. canaliculata (Say, 1826) A. inculta (Gould, 1856) A. cerealis (Gould, 1852) A. culcitella (Gould, 1852) A. oryza (Totten, 1835) Cylichna alba (Brown, 1827) C. attonsa (Carpenter, 1864) “Mamillocylichna richardi (Dautzenberg, 1889) Cylichnium africanum (Locard, 1897) ‘Bulla’ semilaevis Seguenza, 1880 ‘Bulla’ simplex Locard, 1897 Family Philinidae Philine alba Mattox, 1958 P. bakeri Dall, 1919 P. finmarchica Sars, 1858 N. Atlantic N. Atlantic California Seychelles Seychelles Seychelles Madagascar, Seychelles Okinawa Florida N. Atlantic Scotland N. Atlantic Atlantic, S. Africa N. Atlantic N. Atlantic Brazil New York—Nova Scotia California California, British Columbia California Connecticut New Hampshire, Maine British Columbia N. Atlantic N. Atlantic N. Atlantic N. Atlantic California California New Hampshire MCZ MCZ LGH, TMG ANSP ANSP ANSP ANSP, GCW, MLG ANSP TMG MCZ MCZ, MNHN MNHN, YPM MCZ, MNHN MNHN CAS, GCW CAS MCZ, TMG MORPHOLOGICAL PARALLELISM TABLE 1. (Continued) 315 Taxon P. infundibulum Dall, 1889 P. lima (Brown, 1825) P. quadrata (Wood, 1839) P. sp. Family Aglajidae *Aglaja tricolorata Renier, 1807 . ocelligera (Bergh, 1894) . orientalis Baba, 1949 . regiscorona Bertsch, 1972 . unsa? Marcus & Marcus, 1969 A. sp. *Chelidonura hirundinina (Quoy & Gaimard, 1832) C. fulvipunctata Baba, 1938 C. inornata Baba, 1949 C. pallida Risbec, 1951 C. sp. *Melanochlamys cylindrica Cheeseman, 1881 M. diomedea (Bergh, 1893) *Navanax inermis (Cooper, 1862) N. aenigmaticus (Bergh, 1894) ъььь N. polyalphos (Gosliner & Williams, 1972) *Philinopsis speciosa Pease, 1860 P. cyanea (Martens, 1879) P. depicta (Renier, 1807) P. pilsbryi (Eliot, 1900) P. cf. pelsunca Family Gastropteridae Gastropteron pacificum Bergh, 1894 Siphopteron michaeli (Gosliner & Williams, 1988) Family Retusidae *Retusa obtusa (Montagu, 1807) Volvulella cylindrica (Carpenter, 1864) Family Bullidae “Bulla ampulla Linnaeus, 1758 B. striata Bruguière, 1792 B. gouldiana Pilsbry, 1895 Family Haminoeidae Atys cylindrica (Helbling,1779) A. sp. Haminoea vesicula Gould, 1855 H. virescens (Sowerby, 1833) H. strongi Baker & Hanna, 1927 H. solitaria (Say, 1822) H. elegans (Gray, 1825) *Roxania utriculus (Brocchi, 1814) Phanerophthalmus sp. Haminoeidae sp. Family Diaphanidae “Diaphana minuta (Brown, 1827) D. californica Dall, 1919 Locality N. Atlantic New Hampshire N. Atlantic Hawaii Italy California Hawaii Gulf of California Brazil Florida Hawaii Hawaii Madagascar Palau, Malaysia Madagascar Hawaii California California tropical Americas Gulf of California Hawaii Australia Italy Hawaii Italy California, Washington Réunion Island New Hampshire—Maine British Columbia Zanzibar Florida California Seychelles Zanzibar California California Gulf of California Connecticut—Massachusetts, Nova Scotia Yucatan Peninsula N. Atlantic Madagascar Hawaii New Hampshire California Source of material MCZ TMG MCZ TMG CAS TMG TMG CAS EM YPM TMG TMG ANSP CAS, LGH ANSP TMG TMG TMG ANSP, HB, LACM, KM, TMG LACM TMG LGH MCZ TMG CAS CAS, TMG GCW, MLG TMG SM MCZ TMG CAS ANSP MCZ CAS, TMG CAS, TMG CAS KM, TMG TMG MCZ ANSP TMG TMG TMG (continued) 316 GOSLINER TABLE 1. (Continued) Taxon D. sp. | D. sp. Il Order THECOSOMATA Family Limacinidae Limacina retroversa (Fleming, 1823) Family Cavoliniidae Cavolinia tridentata (Niebuhr, 1775) Order SACOGLOSSA Family Cylindrobullidae “Ascobulla ulla (Marcus & Marcus, 1970) A. californica Hamatani, 1971 Volvatella sp. Order ANASPIDEA Family Akeridae "Akera bullata Muller, 1776 A. sp. | A. sp. Il Order NOTASPIDEA Family Umbraculidae *Umbraculum sinicum (Gmelin, 1791) Tylodina fungina Gabb, 1865 presented with a discussion of the phyloge- netic relevance of this variability. Shell The shell in opisthobranchs is exceedingly variable (Fig. 1). In its least derived form it is thickly calcified with a well-elevated apex. It may be modified into a variety of forms within the holoplanktonic Thecosomata (Spoel, 1967) but exhibits less variability within the remainder of the subclass. In most opistho- branchs, where a shell is present in the adult, either it is bulloid with an involuted spire or else it is an internal flattened plate. In the majority of opisthobranch species the shell is entirely lost at metamorphosis from a plank- tonic to benthic existence. Bulloid shells are derived from shells with an elevated spire and, similarly, internal flattened plates proba- bly represent modifications of bulloid shells. The transformation of these shells into more derived structures has occurred many times within separate clades of opisthobranchs (Table 2). A bulloid shell has evolved from a shell with an elevated spire at least six differ- ent times. In each of these cases, both the Locality Source of material N. Atlantic MCZ N. Atlantic MCZ New Hampshire TMG N. Atlantic YPM Brazil EM Gulf of California CAS Hawaii TMG England RB Enewetak Atoll ANSP Madagascar ANSP Hawaii, Zanzibar MCZ, TMG California CAS, TMG ancestral and derived character states occur within members of distinct clades, and in Re- tusa and Acteocina within single genera. Re- duction and internalization of the shell has similarly occurred a minimum of six times within the Opisthobranchia. These same trends in shell reduction and loss also occur in parallel within the sister group of the opisthobranchs, the Pulmonata. Prosobranch gastropods of the Cypraeacea, Lamellariacea and Naticidae also have repre- sentatives with bulloid shells and reduced in- ternal shell plates. A shell is entirely absent in the adults of many derived opisthobranchs, including all members of the Gymnosomata and Nudi- branchia. The presence of a shell and its sub- sequent loss within distinct clades (Table 3) indicates that this has occurred independently at least five times within the Opisthobranchia. Operculum A chitinous operculum is present in virtually all members of the Prosobranchia, but is ab- sent in most opisthobranchs and all but one pulmonate (Hubendick, 1945). All opistho- MORPHOLOGICAL PARALLELISM 317 FIG. 1. Shell variation in opisthobranch gastropods. A: Japonateon sp.; B: Cylichna tubulosa Gould, 1859: C: Melanochlamys sp. TABLE 2. Variation in shell morphology in representative opisthobranchs. Taxon Elevated spire Reduced external shell Internal flattened plate Acteonacea Acteon, Pupa Hydatina, Micromelo — Acteocina A. inculta, A. canaliculata A. oryza, À. bidentata — Philinacea Meloscaphander Cylichna, Scaphander Philine, Gastropteridae, Aglajidae Diaphanidae Toledonia Diaphana Colpodaspis Haminoeidae- — Haminoea, Atys Phanerophthalmus, Runcinidae Runcinidae Retusidae Retusa obtusa R. truncatula — Anaspidea = Akera Aplysia, Petalifera Thecosomata Limacina Cuvierina — Sacoglossa — Cylindrobulla, Ascobulla Lophopleurella Notaspidea = Tylodina, Umbraculum Berthella, Pleurobranchus TABLE 3. Shell loss in opisthobranchs. Taxon Present Absent Cephalaspidea Gastropteron rubrum Siphopteron citrinum Notaspidea Umbraculidae, Pleurobranchidae Pleurobranchaea, Euselenops Philinoglossidae Pluscula Sapha, Philinoglossa Acochlidiacea — all members Sacoglossa Cylindrobullidae, Oxynoidae Elysiidae, Hermaeidae Anaspidea Akeridae, most aplysiids Stylocheilus, some Phyllaplysia Nudibranchia — all members Gymnosomata — all members 318 TABLE 4. Presence of operculum in opisthobranchs. GOSLINER Taxon Present Absent Acteonacea most Acteonidae, Bullinidae Rictaxis, Hydatinidae Retusidae Retusa operculata R. obtusa Scaphandridae ‘Bulla’ semilaevis most Scaphandridae Thecosomata Limacinidae Cavoliniidae, Peraclidae branchs with shelled larvae possess an oper- culum at this stage, but only a few primitive forms retain it as adults (Table 4). Distribution of the presence and loss of the operculum within distinct clades indicates that within the opisthobranchs it has been lost in- dependently at least four times. Mantle complex Within the opisthobranchs a partial or com- plete detorsion of the mantle complex com- monly occurs (Gosliner, 1981a; Gosliner & Ghiselin, 1984). In a few cephalaspidean opisthobranchs the mantle cavity is directed anteriorly, but in most of them it is placed on the right side of the body. In the more highly derived Runcinidae, the mantle cavity has un- dergone complete detorsion and is situated at the posterior end of the animal. From the dis- tribution of this transformation series in opisthobranchs (Table 5) it is apparent that these changes have occurred several times in distinct clades. In other opisthobranch taxa, the mantle cavity has been altered in a variety of different ways. In the Anaspidea the position of the mantle cavity, on the right side of the body, remains essentially unchanged, despite the radical transformation of the body form from the Akeridae to the Aplysiacea. In the ceph- alaspidean family Gastropteridae and No- taspidea the ctenidium is situated on the right side of the body, but is not enclosed within a mantle cavity. The form of the ctenidium varies consider- ably within the Opisthobranchia. Fretter & Graham (1962) and Brace (1977) have sug- gested that in opisthobranchs the ctenidium is primitively absent and a gill has evolved sec- ondarily in some clades. This has been dis- counted by Hoffmann (1940) and Gosliner (1981a), who both suggested that the pres- ence of a gill is plesiomorphic in opistho- branchs and that the opisthobranch gill is homologous to that of prosobranchs. A sec- ondarily bipectinate ctenidium is found in opisthobranchs such as Navanax and the No- taspidea. This merely represents an elabora- tion of the plicate condition found in less-de- rived cephalaspideans. Gills are entirely absent in a variety of derived opisthobranchs and gas exchange occurs through the body surface. While gill loss is often associated with reduced body size, as in the dorid nudi- branch Okadaia (Baba, 1931), some taxa with large representatives also lack gills. These in- clude some members of the Sacoglossa, Arminacea and Aeolidacea. It is apparent that loss of the ctenidium has occurred in several different lineages of opisthobranchs. Buccal mass The presence of paired jaws and a radula are the plesiomorphic states within the Opis- thobranchia. The configuration of the radula varies greatly within and between clades of opisthobranchs and does not characterize ma- jor monophyletic groups as it does within the Prosobranchia. For example, within the Acteonidae the radula may be exceedingly broad with numerous simple teeth or there may be few highly-specialized teeth (Fig. 2). In this case, it is exceedingly difficult to establish which condition is plesiomorphic. Similarly, there is too much variability in radular mor- phology among extant primitive opistho- branchs to suggest an ancestral condition. Within a few major clades such as the Sa- coglossa and the aeolidacean nudibranchs the radula is less variable and has a charac- teristic morphology. Within the Aeolidacea one can suggest plesiomorphic and apomor- phic states. The presence of lateral teeth in the more primitive representatives of the two major clades of aeolids (Table 6), and their subsequent loss, provides an example of parallel reduction in radular teeth within the opisthobranchs. Within several lineages of opisthobranchs the radula has been entirely lost. This has occurred within the Retusidae, the Aglajidae and the dendrodorid, phyllidiid and tethyid nudibranchs. An increase in the number of radular teeth by addition of both number of radular rows MORPHOLOGICAL PARALLELISM 319 TABLE 5. Placement of the mantle cavity in various opisthobranchs. Taxon Anterior Right Posterior Acteonacea Acteonidae Hydatinidae _- Ringiculidae Ringicula nitida R. buccinea, R. conformis = Philinacea ‘Bulla’ semilaevis Acteocina, Scaphander Philinidae, Aglajidae Bullacea — Atys, Haminoea Phanerophthalmus, Runcina and number of teeth per row is likely to be a derived feature within the Notaspidea and perhaps also in cryptobranch dorid nudi- branchs. Gizzard plates In many opisthobranchs the esophagus is expanded into a highly muscularized region which contains chitinous triturating plates. Gosliner (1981a) stated that opisthobranchs probably lacked gizzard plates ancestrally, al- though many primitive opisthobranchs do in fact possess them. This suggestion was based largely on the facts that none of the outgroups of opisthobranchs contain any chitinous structures within the oesophagus, and some primitive opisthobranchs, such as the Ringiculidae and Acteonidae, lack gizzard plates. What is unclear is whether the lin- eages that do possess gizzard plates repre- sent a monophyletic group or whether gizzard plates have evolved within the opistho- branchs on more than one occasion. The fact that ‘Bulla’ semilaevis, which is a primitive member of the Philinacea, lacks gizzard plates, but retains an operculum suggests that absence of a gizzard may be a plesio- morphic condition within the Philinacea. If this is indeed the case, then gizzard plates have evolved at least twice within the Opisthobran- chia. The issue is further complicated by the fact that several lineages of opisthobranchs have secondarily lost the gizzard. This has occurred in the Philinidae and Aglajidae, both of which contain some species with a gizzard and some without. In other cases, such as in the Gastropteridae, it is impossible to suggest whether absence of a gizzard is plesiomor- phic or apomorphic, since all members of the taxon lack a gizzard. The morphology of gizzard plates within various clades of opisthobranchs has under- gone some evolutionary transformations that have increased the efficiency of mastication of prey. The ancestral condition of the gizzard in opisthobranchs may be a series of numer- ous randomly-placed plates of various sizes, as is found in the Akeridae and the remainder of the Anaspidea. Alternatively, the ancestral gizzard may have consisted of three simple plates of equal size. This configuration is found in the Bullidae, Haminoeidae and some members of the Retusidae and Philinacea. Within the Thecosomata and the Runcinidae there are four rather than three gizzard plates. This is considered to be derived from the ple- siomorphic, three-plate condition, and ap- pears to have occurred independently within the two taxa. In the Runcinidae the plates are highly ridged as in the Haminoeidae, while the thecosome gizzard plates have a high dorsal keel, which appears to be a unique innovation within that taxon. The greatest variation in the morphology of the gizzard plates occurs in the Philinacea (Rudman, 1978; Gosliner, 1980). From a con- figuration of three simply-rounded plates of equal size, several parallel changes have oc- curred that are directly related to feeding spe- cializations. This plesiomorphic condition is found in Cylichna, Cylichnium, Mamillocyl- ichna, Philine alba, P. gibba and P. falk- landica. Most members of this order feed on hard-shelled mollusks and Foraminifera. In order to crush the shells of their prey, many philinaceans have increased the relative size and strength of the gizzard plates. This has led to the development of elaborately ridged plates of several different forms. In several species there are pores present in the plates. In some taxa the plates have become differ- entiated and are no longer equal in size. This has occurred independently in Scaphander, Acteocina and in some species of Philine. In the Retusidae the gizzard plates are tubercu- late. In herbivorous taxa such as the Bullidae, Haminoeidae and Runcinidae, the gizzard plates have serrated ridges which facilitate the breakdown of algal tissue. Stomach As in the case of the gizzard of opistho- branchs, the stomach may become highly 320 GOSLINER FIG. 2. Scanning electron micrographs of acteonid radulae. A: Acteon traski Stearns, 1897; B: Hydatina physis (Linnaeus, 1758). muscularized and may contain chitinous structures. This has occurred in the Ringicu- lidae (Fretter, 1960) and in several genera of dendronotacean nudibranchs (Odhner, 1936). Odhner believed that the presence of cuticular plates in the stomach represented a derived condition within the Dendronotacea. However, a chitinous lining of the stomach with large conical plates is present in some members of most families of the suborder, and is therefore considered to represent the plesiomorphic state. Within the Dendronota- cea, both plesiomorphic and apomorphic states are present in different families. In the MORPHOLOGICAL PARALLELISM 321 TABLE 6. Loss of lateral teeth in aeolid nudibranchs. Taxon Several laterals Notaeolidiidae Notaeolidia Flabellinidae Flabellina islandica Eubranchidae-Tergipedidae — Tritoniidae and Tethyidae large chitinous plates are present in some species, but are entirely absent in others. It appears that loss of stomach plates has occurred indepen- dently in different dendronotacean lineages. Digestive gland Within opisthobranchs, the digestive gland may be elaborated with branches entéring epidermal structures called cerata. Cerata have evolved independently in four lineages of opisthobranchs: the Sacoglossa, the aeol- idacean, dendronotacean and arminacean nudibranchs. In the Janolidae the ancestral condition is present in Bonisa, but is apomor- phic in the remainder of the genera (Gosliner, 1981b). Streptoneury/Euthyneury Primitively, the lateral nerve cords are twisted and cross each other, resulting in a streptoneurous arrangement of the central nervous system. As a result of detorsion, the cords become untwisted and are then consid- ered to be euthyneurous (Gosliner, 1981a; Gosliner & Ghiselin, 1984). Euthyneury has evolved from streptoneury on numerous oc- casions within the opisthobranchs (Table 7). Similarly, euthyneury has evolved indepen- dently in the cypraeid and triviid prosobranchs (Gosliner & Liltved, 1985) and in the Pulmo- nata (Marker, 1913). Cephalization Independent of the changes in the config- uration of the central nervous system, caused by detorsion, is the trend towards the concen- tration of the central nervous system and fu- sion of ganglia. Both concentration and fusion are parts of the process of cephalization. One of the most obvious changes that occurs is the shortening of the visceral loop. In the ple- siomorphic state the visceral loop is elongate and the visceral, subintestinal, supraintestinal and genital ganglia are situated at the poste- Single pair of laterals No laterals remainder of family — Eubranchidae Tergipedidae rior end of the body cavity. In derived opistho- branchs there is a shortening of the visceral loop, such that all the ganglia are situated in the circumoesophageal nerve ring. Both the ancestral and derived states are present in members of at least four distinct clades (Table 8). Several trends occur in the movement and fusion of ganglia (Fig. 3). In many taxa, one of the first transformations that takes place fol- lowing development of euthyneury is the movement of the supraintestinal ganglion an- teriorly until it is adjacent to the right pleural ganglion. This has occurred independently in several lineages of opisthobranchs, including the Philinidae and Haminoeidae. In Philine, the plesiomorphic condition is present in P. lima, P. quadrata, P. alba, P. falklandica and P. gibba, while the apomorphic state is present in P. finmarchica, P. aperta, P. auri- formis and P. powelli (Rudman, 1972a; present study). In the Haminoeidae the an- cestral state is present т Atys and Haminoea and the derived state is present in Phaner- opthalmus and Smaragdinella (Rudman, 1972b; present study). Similarly, the genital ganglion may be distinct or it may be fused with the visceral ganglion. Again, this change has occurred in- dependently in several lineages. The plesio- morphic state is present in Philine auriformis, P. angasi and P. aperta but the ganglia are fused in the remainder of the species studied (Rudman, 1972a; present study). Fusion of the genital ganglion with the visceral ganglion also has occurred at least twice within the Aglajidae, where both the plesiomorphic and apomorphic states are present in members of the genera Melanochlamys and Chelidonura (Gosliner, 1980). This same fusion of ganglia has occurred in the Haminoeidae, where the plesiomorphic state is present in Atys, Hami- noea and Smaragdinella and the apomorphic state is present in Phanerophthalmus (Rud- man, 1972b; present study). In many different clades of opisthobranchs there has been a partial or complete fusion of the cerebral and pleural ganglia (Table 9). 322 GOSLINER TABLE 7. Evolution of euthyneury in opisthobranch clades. Taxon Streptoneurous Acteocina most of genus Scaphander S. punctostriatus, S. lignarius Retusa R. operculata (Minichev, 1967) Haminoeidae Atys, Haminoea Anaspidea Akeridae Ringiculidae Ringicula Euthyneurous A. oryza S. mundus, S. nobilis R. obtusa, Volvulella Smaragdinella, Phanerophthalmus Aplysiidae Ringiculoides (Minichev, 1967) TABLE 8. Shortening of the visceral loop in opisthobranchs. Taxon Visceral loop long Visceral loop short Philinacea Scaphandridae, Philinidae, Aglajidae Gastropteridae Bullacea Bullidae, Haminoeidae Runcinidae Sacoglossa Cylindrobullidae remainder of order Anaspidea Akeridae, Aplysiinae Dolabriferinae This has occurred independently at least five times. Separation of Genital ducts Ghiselin (1966) described the functional advantage of various configurations of the hermaphroditic reproductive system of opis- thobranchs and discussed the phylogeny of the subclass. He concluded that the plesio- morphic state was a monaulic system, where all exogenous and endogenous ga- metes are transported through a single geni- tal duct. From this configuration oodiaulic and androdiaulic systems developed. A triaulic system represents a further modification of an androdiaulic arrangement. Rudman (1978) maintained that an oodiaulic system is plesi- omorphic in the Opisthobranchia, but this has been discounted by Gosliner (1980,1981a) and Schmekel (1985). In discussions of the phylogeny of the Phil- inacea, Rudman (1978) placed considerable phylogenetic weight on whether the hermaph- roditic duct branches to the female glands prior to entering the genital atrium. He termed this an oodiaulic arrangement. Within the Philinacea there is considerable variation in the branching of the hermaphroditic duct (Gosliner, 1980; present study). An un- branched duct is considered to be plesiomor- phic because of its functional simplicity. Pres- ence of both the ancestral and derived states within the Philinidae and Aglajidae indicate that a branched duct has evolved from an un- branched one more than once within the Phil- inacea. The branched duct of the anaspide- ans, where oodiauly is more pronounced, appears to be yet another instance of inde- pendent acquisition of the derived condition. An androdiaulic arrangement of reproduc- tive organs occurs in a variety of opistho- branch taxa and it appears to have evolved independently on several occasions. Within the Ringiculidae, monaulic and androdiaulic configurations are present. The Acteonidae, Bullinidae and Hyda- tinidae are exclusively androdiaulic, but differ fundamentally from all other opisthobranchs in that the non-protrusible penis is located at the opening of the mantle cavity rather than on the right anterior portion of the head. This appears to be a morphologically and evolu- tionarily unique form of an androdiaulic con- figuration within the Opisthobranchia. In the Sacoglossa, all extant representa- tives are either androdiaulic or triaulic. Within the Cylindrobullidae, however, а vestigial sperm groove is present even though the tu- bular vas deferens is internal (Marcus & Mar- cus, 1970; present study). This suggests that sacoglossans evolved from a monaulic an- cestor rather than one which was already an- drodiaulic. Within the Notaspidea there is considerable variation in the anatomy of the reproductive system. In the Tylodinidae the reproductive system is monaulic and is the most plesio- morphic condition among extant opistho- branchs (Gosliner, 1981; Schmekel, 1985). In the Berthellinae and Pleurobranchaeidae the reproductive system is androdiaulic, while it is triaulic in the Pleurobranchinae (Marcus & MORPHOLOGICAL PARALLELISM 323 FIG. 3. Variation in the central nervous system of Philine. A: P. finmarchica Sars, 1858, P. infundibulum Dall, 1889; B: P. lima (Brown, 1825); C: P. quadrata (Wood, 1830); D: P. alba Mattox, 1958; E: Philine sp. c cerebral ganglia, pa parietal ganglion, pg pedal ganglia, pl pleural ganglia, sb subintestinal ganglion, sp supraintestinal ganglion, v visceral ganglion. Gosliner, 1984). Thus it appears that the an- drodiaulic arrangement of reproductive or- gans has evolved at least four times within the Opisthobranchia. Similarly, it appears that a triaulic arrange- ment has evolved from an androdiaulic con- figuration at least three times, since represen- tatives of the Sacoglossa, Notaspidea and Nudibranchia possess both the ancestral and derived form. Position of Receptaculum seminis and Bursa copulatrix Ghiselin (1966) and Gosliner (1981) have suggested that the presence of a proximal re- ceptaculum seminis and a distal bursa copu- latrix represents the plesiomorphic state Within the Opisthobranchia. In many in- stances one of these sperm receptacles may be absent (Table 10). The distribution of the ancestral and derived conditions within vari- ous clades of opisthobranchs suggests that the receptaculum seminis and the bursa cop- ulatrix have been lost on numerous occasions within independent lineages of opistho- branchs. DISCUSSION The widespread nature of parallelism in opisthobranchs has been well documented (Ghiselin, 1966; Gosliner, 1981; Gosliner & Ghiselin, 1984), but its extent within every or- gan system has not been precisely estab- lished. What has not received adequate attention is the question of how differing interpretations of which characters have undergone indepen- dent change and which are truly monophyletic may alter dramatically one’s perception of phylogeny and systematics. Gosliner & Ghis- elin (1984) described two historical examples 324 GOSLINER TABLE 9. Fusion of cerebral and pleural ganglia in opisthobranch clades. Taxon Separate Ringiculidae Ringicula Retusidae Retusa obtusa Haminoeidae remainder of family Notaspidea Umbraculidae Janolidae of conflicting scenarios of opisthobranch phy- logeny. The placement of cerata-bearing sa- coglossans and aeolid nudibranchs in the same taxon by early workers was disputed by Russell (1929) because there are significant differences in the arrangement of ganglia be- tween sacoglossans and nudibranchs, de- spite the fact that they are at approximately the same level of cephalization. In sacoglos- sans the visceral ganglion is located on the left side of the circumoesophageal nerve ring, while it is on the right side in nudibranchs. The second example involved Boettger's (1954) study of the phylogeny of the Euthy- neura (opisthobranchs and pulmonates). By placing organisms at the same level of orga- nization in the same clades, he produced a classification scheme that contained poly- phyletic grades rather than clades. More recently, Gosliner (1985b) addressed problems in the classification of the nudi- branch family Aeolidiidae. Differences in the systematics of the family are related to diver- gent opinions as to whether rhinophoral struc- ture or ceratal arrangement is monophyletic within the family. The two characters produce contradictory affinities of the genus Berghia to either Spurilla or Baeolidia. Schmekel (1985) recently discussed the anatomy and phylogeny of the opisthobranch taxa. She provided much new synthetic ma- terial, particularly relating to our knowledge of the Nudibranchia and Sacoglossa. Her con- clusions differ significantly from the scenarios presented by Ghiselin (1966) and Gosliner (1981a). This is a direct result of the fact that her conclusions are based on different as- sumptions about the monophyletic or poly- phyletic evolution of various characters within the Opisthobranchia and uniting taxa based on symplesiomorphy rather than apomorphy. The systematic placement of the Akeridae has been the subject of controversy for al- most a century. Several workers (Thiele, 1931; Franc, 1968; Marcus, 1970; Thompson, 1976; Schmekel, 1985) have considered Ak- era as belonging to the Cephalaspidea, while Janolus cristatus, J. longidentatus Fused Ringiculoides (Minichev, 1967) R. operculata (Minichev, 1967) Phanerophthalmus Pleurobranchidae J. capensis, J. australis others (Guiart, 1901; Boettger, 1954; Ghise- lin, 1966; Morton, 1972; Beeman, 1977) sug- gested that it was better placed in the Anaspi- dea. Ghiselin (1966: p.369-370) stated that “the placement of the Akeratidae among the Anaspidea (Guiart, 1901) is well supported by the structure of the reproductive system, as well as by numerous other similarities, and is no longer disputed”. While | believe that Ghis- elin was correct in ascribing the Akeridae to the Anaspidea, he was incorrect in assuming that the controversy had been resolved. Thompson (1976: p.129) stated that “in some ways, notably in features of the alimentary ca- nal, the spermatozoa, and the defensive glands, Akera exhibits aplysiomorph charac- ters, but on balance it seems best to retain the akerids as a bullomorph family, by virtue of their possession of a large external shell, parapodia continuous with the pedal sole, a non-tentaculate spatulate cephalic shield, or- gans of Hancock, posterior pallial lobe and long visceral connectives”. Schmekel (1985) made similar arguments in suggesting that Akera is not an anaspidean. Thompson and Schmekel placed Akera in the Cephalaspidea solely because it shares numerous symplesi- omorphies with that group. None of the char- acters suggested by either of these workers are apomorphic. Schmekel erroneously as- cribed an androdiaulic reproductive system to Akera and suggested that this was apomor- phic with some cephalaspideans. When one examines the morphology of Akera and anaspideans (Guiart, 1901; Beeman, 1977; present study) there are numerous synapo- morphies in common: similar defensive glands, jaws with elongate rod-like elements, a broad radula with multidentate rachidian tooth and denticulate laterals, a gizzard com- posed of numerous conical teeth, a central nervous system with the pleural ganglia situ- ated closer to the pedal ganglia than to the cerebral ganglia, an oodiaulic reproductive system, a distinct genital atrial gland (reser- voir seminal of Guiart), a cephalic penis armed with chitinous spines and spermatozoa MORPHOLOGICAL PARALLELISM 325 TABLE 10. Configuration of bursa copulatrix and receptaculum seminis in the Opisthobranchia. Taxon Bursa and receptaculum present Receptaculum absent Bursa absent Acteonidae Pupa Acteon, Rictaxis — Diaphanidae Toledonia Diaphana Facelinidae Hermosita — Facelina Flabellinidae Flabellina bicolor F. iodinea F. babai Tergipedidae Cuthona divae, C. concinna rest of family — Pleurobranchaeidae most species Pleurobranchaea californica — Janolus J. longidentatus J. hyalinus = Hancockia H. californica H. uncinata — with an elongate helical nucleus (Franzén, 1955; Thompson, 1973). Many of these de- rived features are unique to Akera and other anaspideans. If one subscribes to Hennig’s (1966) philosophy that derived features are the only ones which can phylogenetically link taxa, and that taxa should be monophyletic rather than paraphyletic, there is no alterna- tive but to consider the Akeridae as anaspi- deans. Schmekel (1985) based most of her hy- potheses about the phylogeny of the opistho- branchs on the argument that there are two basic lineages. There is one lineage derived from monaulic cephalaspideans that have re- mained monaulic or have developed oodi- auly. Within this lineage the cerebral and pleural ganglia have remained separate. The second lineage arose from androdiaulic ceph- alaspideans and includes all androdiaulic and triaulic taxa. In this clade the cerebral and pleural ganglia have been fused. Implicit to this scenario of opisthobranch phylogeny are the assumptions that androdiauly and fusion of the cerebral and pleural ganglia have evolved only once within the opisthobranchs. As described above there are difficulties with these assumptions. First of all, it appears that androdiauly has evolved at least four separate times within the opisthobranchs, within the Ringiculidae, Acteonidae, Sacoglo- ssa and notaspidean-nudibranch clade. There are distinct morphological differences between the various androdiaulic forms. For example, the pallial penis in the Acteonacea differs markedly from the cephalic penis found in the Sacoglossa and the Ringiculidae. The fact that the diaulic Cylindrobullidae re- tain an external sperm groove suggests that they arose from monaulic ancestors, rather than from an androdiaulic form such as an acteonacean. Secondly, it does not appear that fusion of the cerebral and pleural ganglia is monophyletic within the Opisthobranchia (Table 9). Presence of both ancestral and de- rived states within such clearly monophyletic taxa as the Haminoeidae and the Janolidae demonstrates polyphyly of this character. Similarly, janolids, which may have either separate or fused cerebral and pleural gan- glia, are members of the lineage which is pre- sumed to possess only fused ganglia. The phylogenetic hypotheses presented by Schmekel are not consistent with the tradi- tional systematic placement of the Umbracu- lacea within the Notaspidea. Members of this taxon have a monaulic reproductive system and separate cerebral and pleural ganglia, while the remainder of the Notaspidea are an- drodiaulic or triaulic and have fused ganglia. To resolve this inconsistency Schmekel re- moved the Umbraculacea from the Notaspi- dea and placed them in their own order, the Umbraculomorpha. Schmekel stated that the characters uniting the Umbraculacea with the Notaspidea are all plesiomorphic. However, there are several features which are shared by members of these taxa which appear to be apomorphic. The gill in both taxa is pinnate and is not enclosed by a mantle cavity. The labial cuticle is chitinous and possesses po- lygonal elements, although these are poorly developed in most umbraculaceans. The as- sociation of the visceral ganglion with the right side of the body is characteristic of members of the notaspidean-nudibranch clade. These synapomorphies link the Umbraculacea to the remainder of the notaspideans. While consid- erable phenetic distance separates the Um- braculacea from the Pleurobranchacea, to- gether with the Nudibranchia, they form a cladistically monophyletic taxon and should be united with these taxa, following Willan (1987). Discussions of parallel evolution in opistho- branchs led one cladist colleague to suggest 326 GOSLINER that if the opisthobranchs really do possess that much parallel evolution, then it might be more prudent to work on another group of or- ganisms! While the preponderance of paral- lelism in all organ systems of opisthobranchs presents problems in dealing with their phy- logeny and systematics, the situation is not as hopeless as it might appear. Though most of the organ systems do exhibit polyphyly within the Opisthobranchia as a whole, one must at- tempt to determine at what level these changes are monophyletic and employ those synapomorphies as a basis for construction of phylogenetic hypotheses. By combining this methodology with placing greater qualitative weight to uniquely derived and divergent fea- tures, as advocated by Gosliner and Ghiselin (1984) one can successfully produce phylog- enies of opisthobranchs that can be further tested. As virtually all of these parallel changes are responses to similar selection pressures it is also fruitful to ascertain the possible adaptive significance of these mor- phological transformation series. This is not only useful in determining the polarity of these changes, but also places the major changes in a hypothetical evolutionary perspective that is consistent with the data. AKNOWLEDGEMENTS | thank Michael T. Ghiselin for critically re- viewing the manuscript and for providing valu- able suggestions for its improvement. LITERATURE CITED BABA, K., 1931, A noteworthy gill-less holohepatic nudibranch Okadaia elegans Baba, with refer- ence to its internal anatomy. Annotationes Zoo- logicae Japonenses, 13: 63-89. BEEMAN, R., 1977, Gastropoda: Opisthobranchia. In: GIESE, A & J. PEARSE, eds., Reproduction of marine invertebrates 4. Academic Press, New York, р. 115-179. BOETTGER, С., 1954, Die Systematik der euthy- neuren Schneken. Zoologischer Anzeiger, (Suppl.) 17: 253-279. BRACE, R., 1977, The functional anatomy of the mantle complex and columellar muscle of tecti- branch molluscs (Gastropoda, Opisthobranchia). Philosophical Transactions of the Royal Society of London, Series B, 277: 1-56. FRANC, A., 1968, Mollusques gastéropodes et scaphopodes. In: GRASSE, P., ed., Traité de Zo- ologie, 5(3). Masson, Paris, p. 1-1083. FRANZEN, A., 1955, Comparative morphological investigations into the spermiogenesis among Mollusca. Zooliska Bidrag fran Uppsala, 30: 399-456. FRETTER, V., 1960, Observations on the tecti- branch Ringicula buccinea. Proceedings of the Zoological Society of London, 135: 537-549. FRETTER, V., 8 A. GRAHAM, 1962, British Proso- branch Molluscs. Ray Society, London, 1-755 р. GHISELIN, M., 1966, Reproductive function and the phylogeny of opisthobranch gastropods. Ma- lacologia, 3: 327-378. GOSLINER, T., 1980, Systematics and phylogeny of the Aglajidae (Opisthobranchia: Mollusca). Zoological Journal of the Linnean Society, 68: 325-360. GOSLINER, Т., 1981a, Origins and relationships of primitive members of the Opisthobranchia (Mol- lusca: Gastropoda). Biological Journal of the Lin- naean Society, 16: 197- 225. GOSLINER, T., 1981b, The South African Janol- idae (Mollusca, Nudibranchia) with the descrip- tion of anew genus and two new species. Annals of the South African Museum, 86: 1-42. GOSLINER, T., 1985a, Parallelism, parsimony and the testing of phylogenetic hypotheses: the case of opisthobranch gastropods. In: VRBA, Е , ed., Species and Speciation. Transvaal Museum Monographs, 4, р. 105-107. GOSLINER, Т., 19855, The aeolid nudibranch fam- ily Aeolidiidae (Gastropoda, Opisthobranchia) from tropical southern Africa. Annals of the South African Museum, 95: 233-267. GOSLINER, T. & M. GHISELIN, 1984, Parallel ev- olution in opisthobranch gastropods and its impli- cations for phylogenetic methodology. System- atic Zoology, 33: 255- 274. GOSLINER, T. & W. LILTVED, 1985, Aspects of the morphology of the endemic South African Cy- praeidae with a discussion of the evolution of the Cypraeacea and Lamellariacea. Annals of the South African Museum, 96: 67-122. GUIART, J., 1901, Contribution à l'étude des gas- téropodes opisthobranches et en particulier des cephalaspides. Mémoires de la Société de Zoo- lologie France, 14: 1-219. HENNIG, W., 1966, Phylogenetic systematics. Uni- versity of Illinois Press, Urbana, 1-263. HOFFMANN, H., 1940, Opisthobranchia. Bronn's Klassen und Ordungen des Tierreiches, 3 (Abt. 2, Buch 3, Teil 2): 1-90. HUBENDICK, B., 1945, On the family Amphibol- idae. Proceedings of the Malacological Society of London, 26, 103-110. MARCUS, E., 1970, Opisthobranchs from northern Brazil. Bulletin of Marine Science, 20: 922-951. MARKER, E., 1913, Nervenkreuzungen als folgen einer Chiastoneuri bei den Pulmonaten Gas- tropoden und die zweifache Art ihrer Rückbil- dung. Zoologischer Anzeiger, 41: 337-354. MORTON, J., 1972, The form and functioning of the pallial organs in the opisthobranch Akera bullata with a discussion on the nature of the gill in No- MORPHOLOGICAL PARALLELISM 327 taspidea and other tectibranchs. The Veliger, 14: 337-350. RUDMAN, W., 1972a, The genus Philine (Opistho- branchia, Gastropoda). Proceedings of the Mal- acological Society of London, 40: 171-187. RUDMAN, W., 1972b, The herbivorous opistho- branch genera Phaneropthalmus A. Adams and Smaragdinella A. Adams. Proceedings of the Malacological Society of London, 40: 189-210. RUDMAN, W., 1978, A new species and genus of the Aglajidae and the evolution of the philinacean opisthobranch molluscs. Zoological Journal of the Linnean Society, 62: 89-107. RUSSELL, L., 1929, The comparative morphology of the elysioid and aeolidoid types of the mollus- can nervous system, and its bearing on the rela- tionship of the ascoglossan nudibranchs. Pro- ceedings of the Zoological Society of London, 14: 196-233. SCHMEKEL, L., 1985, Aspects of evolution within the opisthobranchs. In: TRUEMAN, E.R. & M.R. CLARKE, eds., The Mollusca , volume 10, Evo- lution. Academic Press, Orlando, Fla & London, p. 221-267. SPOEL, S. VAN DER 1967, Euthecosomata, a group with remarkable developmental stages (Gastropoda, Pteropoda). J. Noorduijn en zoon, Gorinchem. pp 1-375. THIELE, J., 1931, Gastropoda. Il: Opisthobranchia. Handbuch der systematischen Weichtierkunde (2): 377—461. Gustav Fischer, Jena. THOMPSON, T.E., 1973, Euthyneuran and other molluscan spermatozoa. Malacologia, 14: 167— 206. THOMPSON, T.E., 1976, Biology of Opisthobranch Molluscs, volume 1. Ray Society, London, р. 1— 207. WILLAN, R., 1987, Phylogenetic systematics of the Notaspidea (Opisthobranchia) with reappraisal of families and genera. American Malacological Bulletin, 5, 215-241. MALACOLOGIA, 1991, 32(1-2):329-352 INDEX Taxa in bold are new; page numbers in Aegopinella 157 bold indicate pages on which new taxa are nitidula 157, 162, borehole 162 described; pages in italics indicate page Aegopinella pura 162 numbers on which appear figured taxa. aemulus, Conus 52 aenigmaticus, Navanax 315 abbreviatus, Actaeonina 58 Aeolidacea 318 abbreviatus, Conus 40, 52, 56 Aeolidia papillosa 247 abyssalis, Aforia 6 Aeolidiella 245, 294, 297 abyssalis, Teretiopsis 9 alderi 249, 284, 297 Abyssobella atoxica 9 glauca 247 Acanthocardia tuberculata 191 mannarensis 247 Acanthodoris 213 rubra 297 brunnea 246 sanguinea 247 nanaimoensis 246 Aeolidiidae 324 pilosa 246 affinis, Atlanta 107 Achochlidiomorpha 308 affinis, Flabellina 248 acicula, Creseis 225 affinis, Terebra 20, 23, 24, 27, 28, 30, 32, aciculina, Hastula 20, 28, 31 33 Acila conradi 190 affinis, Tornatellaea 190 divaricata submirabilis 142 Aforia abyssalis 6 divaricata schencki 132, 141-142 kupriyanovi 6 acinacea, Nuculana (Thestyleda) 132, 142 africana, Chromodoris 247 Acochlidiacea 317 africana, Thorunna 244 Acropsis dissimilis 191 africana, Turricula 190 Acrosterigma 143 africanum, Cylichnium 314 Actaeonina 56 agassizii, Conus 53 Actaeonina abbreviatus 58 agassizii, Hypselodoris 244 саитоп 58 Aglaja 315 minimus 58 ocelligera 315 actava, Pseudamnicola 156 orientalis 315 Acteocina 316, 317, 319, 322 regiscorona 315 atrata 259 tricolorata 315 bidentata 314, 317 unsa 315 canaliculata 266, 268, 269, 314, 317 ee 315, 317-319, 322 cerealis 314 era 226, 316, 317, 324, 325 culcitella 314 bullata 227, 294, 295, 316 inculta 314, 317 soluta 228, 230 lajonkaireana 190 Akeratidae 224, 324, 325 oryza 314, 317, 322 Akeridae 316-318, 322, 324 Acteon 227, 317, 325 akibumii, Coralliobia 132, 137 hebes 314 alba, Cylichna 314 reussi 190 alba, Philine 314, 319, 321, 323 semistriatus 190 albaria, Macoma 192 tornatilis 190, 225, 227-230, 295 albocrusta, Cuthona 247 traski 320 albofasciata, Turridrupa 83 verneuilli 58 albolineata, Dirona 248 Acteonacea 317-319 albolineata, Glycymeris 191 Acteonidae 59, 223, 224, 314, 318, 319, albopunctata, Cuthona 247 325 albopunctatus, Dendronotus 248 Acteonoidea 310 albula, Hastula 20 acuminatus, Conus 53 albus, Vanikoropsis 189 Acus 33 alderi, Aeolidiella 249, 284, 297 Acusidae 33 alderi, Euspira 161, 163, 170, 171, 175, acuta, Lophiotoma 81, 83 176 Adalaria 213 Alderia modesta 296 proxima 246, 266, 280-282, 285, 286 Aldisa 212, 213, 216 adspersa, Tenellia 245, 297 cooperi 246 adyarensis, Cuthona 247 tara 246 Aegires 213, 215 aldrichi, Vokesula 192 punctilucens 246 Alectrion 139 sublaevis 246 alexandrae, Alvania 188 329 330 INDEX allisoni, Pleurotomella 81 Allogastropoda 197, 198 allophyla, Inglisella 190 Alocospira papillata 189 alphonisana, Mitromorpha 83 Alvania 73 alexandrae 188 amabilis, Tritonoturris 83 amadis, Conus 52 Amathinidae 198 ambiguus, Conus 52 amekiensis, Bonellitia 190 amekiensis, Mesalia 189 amekiensis, Varicorbula 192 amoena, Chromodoris 247 ampezzana, Cassianella 191 Amphidonte obliquata 191 Ampulina 166 ampulla, Bulla 225, 315 Ampullarioidea 202 Ampullospirinae 180 Amyclina 189 Anacithara 83, 85 Anadara 170, 191 devincta 191 diluvii 191 elevata 191 granosa 170, 176, 191 thisphila 191 Anaspidea 205, 224, 226, 308-310, 317- 319, 321, 322, 324 Ancilla buccinoides 189 pallida 138 Ancistrosyrinx pulcherrissima 132, 140 Ancula 212-214 Ancula evelinae 246 gibbosa 244, 246 andrussowi, Hydrobia 188 anemone, Conus 53 angasi, Philine 321 angulata, Epicyprina 192 angulata, Mactra 191 angulata, Mesosaccella 190 angulata, Mohrensternia 188 angusta, Donacilla 174, 191 angustifrons, Katherinella 192 anilis, Terebra 28 Anisodoris 213 prea 246 stellilfera 238 annulata, Chromodoris 247, 260-261 annulicornis, Facelina 248, 297 anodonta, Lucina 191 Anomalocardia squamosa 192 Anomioidea 164 Anthobranchia 308-310 Antiplanes 6, 14, 16, 16 antiquata, Nucula 190 antiquatus, Solecurtus 192 Antonietta luteorufa 247 antonii, Mexichromis 244 aperta, Philine 225, 227-230, 294, 298, 310, 321 Aphrodina nitidula 192 apicalis, Turrancilla 132, 139 Aplacophora 165 Aplysia 226, 227, 230, 310,317 californica 259 dactylomela 260-261 depilans 225, 227, 294, 295 fasciata 293, 296 punctata 225, 226, 227, 229, 230, 296 willcoxi 228, 230 Aplysiacea 318, 322 Aplysiidae 224, 317, 322 Aplysiomorpha 205, 308 Aporrhais pespelecani 189 uttingerianus 189 approximata, Lucina 191 araneosus, Conus 52 Archidoris 213 montereyensis 246 odhneri 246 seudoargus 216, 246, 281, 282 Archimediella spirata 189 Architaenioglossa 199 Architectibranchia 309, 310 Architectonica 133 benedeica 190 nobilis 160 olicatum 190 Architectonicidae 201 Architectonicoidea 198 Arcopagia robusta 192 Arcopsis 167 arctata, Macoma 192 Arctica 170 islandica 192 arctica, Hiatella 192 arcticus, Bathypolypus 150 arcuatus, Conus 36, 41, 46, 49, 50 Ardeadoris egretta 244 arenaria, Mya 163, 174, 176, 192 arenatus, Conus 40, 52 areolata, Terebra 30 areolata, Trippa 246, 260-261 argentimaculatus, Favorinus 245 argo, Platydoris 213, 293 Argyropeza 189 Arminacea 318 ascidicola, Okenia 246 Ascobulla 317 Ascobulla californica 316 Ascobulla ulla 316 Ascoglossa 205, 209 Asprella (Conasprella?) ichinoseana 132, 140 Astarte 170, 174, 191 triangularis 191 Asteronotus cespitosus 246, 258, 259-261, 263 Astropecten 177 Atactodea striata 191 atava, Sandria 156 Atlanta 107, 111, 114 affinis 107 echinogyra 107-111, 112, 114, 115, 116, 120, 121, 122.123, 129 fusca 109, 110, 117, 123, 124, 129 gaudichaudi 109, 114, 116, 120 ibbosa 107, 109 elicinoides 108, 108, 109, 109, 110, INDEX 114, 117, 125, 126, 129 inclinata 109, 128 inflata 107-110, 114, 115, 117, 123, 125, 126, 129 lesueuri 109, 110, 114, 115, 116, 118, 119, 128 meteori 107, 108, 109, 110, 114, 127, 128, 129 oligogyra 107, 109, 110, 114, 116, 118, 119, 129 pacifica 107 peresi 107 peroni 109, 110, 112, 114, 116, 118, 120, 129 plana 107-111, 112, 114, 116, 120, 121, 122, 129 tokiokai 107, 109, 110, 114, 115, 117, 126, 127, 128, 129 turriculata 107, 109, 110, 114, 115, 117, 122, 123, 124, 129 : Atlantidae 107-130 key to 128-129 atoxica, Abyssobella 9 atra, Polycera 213 atrata, Acteocina 259 atromaculata, Peltodoris 216 atromarginata, Casella 260-261 atromarginata, Glossodoris 247 attonsa, Cylichna 314 Atyidae 224 Atys 315, 317, 319, 321, 322 blainvilliana 295 cyclindrica 225, 227, 315 miliaris 190 naukum 229 aurantiaca, Berthella 293, 296 aurantiaca, Doriopsis 246 auratia, Dirona 248 aurea, Venerupis 192 aureomarginata, Chromodoris 244 auricularia, Dolabella 227, 260-261 auriculata, Ringicula 190, 295 auriculatus, Modiolus 190 auriformis, Philine 321 auritulus, Favorinus 248 aurora, Conus 52 Austaeolis catina 247 australis, Janolus 324 australis, Mactra 191 Austrodoris macmurdensis 249 Austromitra 190 Avellana incrassata 190 avemi, Glossodoris 244 babai, Flabellina 325 Babelomurex 138 Babylonia kirana 138 pallida 132, 138 babylonia, Terebra 20, 21, 28, 29, 29, 31 bacillus, Hastula 20, 21 21-23, 22, 23, 27- 29729731, 32: 33 badensis, Turritella 189 Baeolidia 324 nodosa 297 bakeri, Philine 314 Bakerilymnaea 310 331 balteatus, Conus 40, 52 balthica, Macoma 174, 192 barbadensis, Fissurella 164 Barbatia irregularis 191 bartschi, Conus 52 Baryspira hinomotoensis 139 urasima 132, 134, 139 Bassina 173, 174 calophylla 192 basteroti, Chione 192 Bathyarca 191 Bathypolypodinae 147, 152 Bathypolypus arcticus 150 beaumarisensis, Limopsis 191 beaumonti, Cardita 85 beaumonti, Cumanotus 206, 219-221, 220, 247 bedensis, Dentalium 193 Beguina diversicosta 191 Bela 70 brachystoma 190 vulpecula 190 bella, Codakia 191 dellula, Calliopaea 296 bembix, Protoginella 189 benedeica, Architectonica 190 benedeica, Hexaplex 189 bennetti, Hypselodoris 239, 249 benteva, Berghia 247 Benthobia 13, 13, 14 Berghia 324 benteva 247 coerulescens 247 verrucicornis 247, 297 Berthelinia 209 Berthella 317 aurantiaca 293, 296 plumula 227 Berthellina 226, 238 citrina 227, 260-261, 266, 267, 268 Berthellinae 322 betulinus, Conus 53 beui, Paracomitas 190 bicolor, Doris 296 bicolor, Flabellina 325 bicolor, Gymnodoris 246 bidentata, Acteocina 314, 317 bieniaszi, Turritella 189 bifasciata, Papyriscala 132, 135 bilamellata, Onchidoris 206-207, 215, 246, 273-289, 283, 285 bilineata, Hypselodoris 236, 239, 243, 244, 247 bimaculatus, Octopus [borehole] 160 biplicata, Olivella 189 bisulcatum, Phalium 137 Bittium 169, 189 reticulatum 189 Blackdownea quadrata 189 blainvilliana, Atys 295 Blennius 238 Bonellitia amekiensis 190 serrata 190 Bonisa 321 Borsoniinae 29, 31, 80-85 Bosellia 209, 309 332 INDEX bouei, Loxocardium 191 brachystoma, Bela 190 Brachytoma obtusangula 190 branchialis, Favorinus 248, 293, 297 brandtii, Euhadra 140 brevis, Entaliopis 193 britoi, Chromodoris 234 brockii, Moridilla 245 browni, Coryphella 247 brunnea, Acanthodoris 246 brunneus, Conus 41, 52 buccinea, Ringicula 190, 319 Buccinidae 165, 177 buccinoides, Ancilla 189 Buccinum isaotakii 132, 138 leucostoma 138 bulbus, Conus 52 Bulla ampulla 225, 315 gouldiana 315 punctata 228 punctulata 225, 227, 229, 230 Striata 228, 230, 292-295, 315 "Bulla" semilaevis314, 318, 319 simplex314 Bullacea 319, 322 bullata, Akera 227, 294, 295, 316 Bullidae 224, 315, 319, 322 Bullinidae 318 Bullomorpha 205, 308, 309 burni, Hancockia 248 Bursa dunkeri 132, 137 Bursatella leachii leachii 294, 296 leachii savignyi 296 Cadilina 213 laevis 249, 258, 268, 279, 281, 282, 284, 286 nigrobranchiata 244 willani 244 cadonensis, Conactaeon 58 cadonensis, Conus 56 Cadulus 193 Cadulus (Platyschides) novilunatus 132, 141 Caecum glabrum 189 caerulea, Cuthona 297 Caestocorbula 192 calcarata, Drepanocheilus 189 calcarea, Macoma 192 caledonica, Vayssieria 249 californensis, Chione 192 californica, Aplysia 259 californica, Ascobulla 316 californica, Cryptomya 192 californica, Diaphana 315 californica, Hancockia 325 californica, Pleurobranchaea 325 californicus, Conus 42, 44, 45, 52 californiense, Clinocardium 142 californiensis, Hypselodoris 244 Caliphyllidae 209 Calipitaria distincta 192 Calliopaea bellula 296 Calliostoma laugieri 188 Callistina plana 192 Calma glaucoides 297 Calmella cavolinii 297 calophylla, Bassina 192 Calva subrotunda 192 Campanile symbolicum 201 campechiensis, Mercenaria 192 canaliculata, Acteocina 266, 268, 269, 314 317 canaliculata, Mutiella 191 canalis, Conus 57 canalis, Liopeplum 59 Canarium microurceum 132, 136 cancellata, Chione 192 Cancilla 132, 140, 189 candelatum, Dentalium (Episiphon) 132, 141 candelatum, Episiphon 141 canrena, Natica 164 cantabrica, Hypselodoris 233, 236, 244 Cantharidus (Kanekotrochus) infuscatus 135 "Cantharidus kanekonis" [nom. nud.] 132, 135 Cantharidus yokohamensis 135 Cantharus 189 caparti, Eledone 152 capensis, Janolus 324 capensis, Terebra 20, 33 caperata, Chimela 192 capitaneus, Conus 40, 52 capitata, Limapontia 294, 296 Capulidae 156 Capulus danieli [borehole] 158 Cardita 191 beaumonti 85 chamaeformis 191 Cardium 191 enode 143 politionanei 191 Cardium (Trachycardium) serricostatum 142-143 Carinapex minutissima 83 Carinarioidea 202 Carminodoris 213 carpenteri, Triopha 242 Caryocorbula deusseni 192 Casella atromarginata 260-261 obsoleta 258-261, 263, 264, 266, 267, 268 Cassianella 166 ampezzana 191 Cassidae 156 Cassidulus pacificus 158 Cassis comuta 134 castanea, Goniodoris 215, 246 castus, Nassarius 139 catelinae, Triopha 246 catenifera, Gemmaterebra 190 catina, Austaeolis 247 Catriona gymnota 242, 247 catus, Conus 41, 52 caudata, Eupleura 189 caumonti, Actaeonina 58 caumontii, Conus 56 caurica, Erronea 134 cauze, Elysia 268 Cavolinia 225 INDEX longirostris 225, 226, 227-230 tridentata 225, 227, 228, 230, 316 cavolinii, Calmella 297 Cavoliniidae 316, 318 Cenodagruetes 9, 25 centurio, Conus 52 Cepaea nemoralis 205 Cephalaspidea 205, 224, 226, 317, 324 Cephalopoda 157, 165 Cerastoderma 170 edule 191 Ceratostoma (Pteropurpura) vespertilio 132, 137 Cerberilla 221 cerealis, Acteocina 314 Cerithiimorpha 199 cerithina, Terebra 20 Cerithiopsidae 11, 73 Cerithiopsis tubercularis 189 Cerithium europeum 189 variabile 189 vulgatum 189 cespitosus, Asteronotus 246, 258, 259-261, 263 ceylanensis, Conus 40, 52 chaldeus, Conus 36, 40, 46, 52 chamaeformis, Cardita 191 Chamelea gallina 192 striatula 176 Chamoidea 164 chapmani, Limopsis 191 chathamensis, Splendrilla 6, 7, 7 Chelidonura 315, 321 fulvipunctata 315 hirundinina 315 inomata 315 pallida 315 Chelyconus kinoshitai 132, 140 Chicoreus 73 ramosus 259-261, 263, 264, 268 virgineus 259, 260-261, 262, 268 Chimela caperata 192 chinensis, Coecella 191 chinensis, Glauconome 192 chinensis, Mactra 191 Chione 192 basteroti 192 californensis 192 cancellata 192 subrugosa 192 undatella 192 Chlamys 133, 168 radians 191 Choromytilus meridionalis 176, 190 Chromodorididae 233 Chromodoris 213, 233-240, 293 africana 247 amoena 247 annulata 247, 260-261 aureomarginata 244 britoi 234 clenchi 247 diardii 242 elegantula 244 ghardaqana 260-261 Inomata 247, 258, 259-61, 265, 266 333 krohni 233, 234, 236, 239, 244, 296 loringi 249 luteopunctata 234, 247 luteorosea 233, 234, 236 mcfarlandi 244 pallida 260-261 perola 247 petechialis 242 pulchella 247, 260-261 purpurea 233, 234, 236, 237 quadricolor 260-261 reticulata 242 tinctoria 247, 260-261, 268 cicercula, Pustularia 136 cincta, Tritonia 248 cinerea, Hastula 20, 29 cinerea, Urosalpinx 156 cingulatus, "Fusus" 30 cingulatus, Eubranchus 247 cingulifera, Terebra 30 cingulifera, Xenuroturris 83 Cingulopsoidea 202 Circomphalus subplicatus 192 Circulus 189 cirrhosa, Eledone 147, 148, 152 Cirsocerithium gracile 189 Cirsotrema (Elegantiscala) kurodai 132, 136 rugosum 136 varicosum 136 citrina, Berthellina 227, 260-261, 266, 267, 268 citrina, Gymnodoris 246 citrina, Tylodina 227 citrinum, Siphopteron 317 clandestina, Kermia 83 clausa, Natica 165 Clavagelloidea 164 Clavatula 190 diadema 5, 14, 15 tripartita 72 Clavatulinae 20 clavigera, Limacia 242, 244, 296 Clavinae 5, 6, 11, 14, 83 Clavus 83, 85, 190 exilis 83 pica 83 clenchi, Chromodoris 247 Clinocardium californiense 142 nuttallii 191 uchidai 132, 142 Clython sowerbyanus 134 Cocculiniformia 197, 198 Cochlespirinae 80-82, 85 Cochlodesma leanum 193 Codakia bella 191 orbicularis 191 Coecella chinensis 191 coelestis, Hypselodoris 236, 239 coerulea, Cuthona 247, 297 coerulescens, Berghia 247 cognata, Temnoconcha 192 Colpodaspis 317 Colubraria 189 columella, Cuvierina 225 Colus curtus 165 Comitas nana 190 334 INDEX complexum, Dentalium 193 Comptopallium vexillum 158 compunctum, Vasticardium 132, 142 Conactaeon cadonensis 58 concavus 58 Conaspirella 132, 140 concavus, Conactaeon 58 concavus, Conus 56 concentrica, Dosinia 158 concinna, Cuthona 325 concinna, Discodoris 246, 258, 260-261 concinna, Sunetta 134 concinnus, Conus 60 conditorius, Conus 59 conformis, Ringicula 295, 319 Confusiscala fittoni 189 Conidae 1, 3, 20, 29, 31, 55-67 Conoidea 1-202 conoidea, Odostomia 190 Conorbinae 57 Conorbis 57, 65 coromandelicus 56 menairyensis 57 conradi, Acila 190 conradi, Solen 192 Conuber incei 161 conulus, Eulimella 190 Conus 1, 9, 29, 30, 35-67, 258, 260 abbreviatus 40, 52, 56 acuminatus 53 aemulus 52 agassizii 53 amadis 52 ambiguus 52 anemone 53 araneosus 52 arcuatus 36, 41, 46, 49, 50 arenatus 40, 52 aurora 52 balteatus 40, 52 bartschi 52 betulinus 53 brunneus 41, 52 bulbus 52 cadonensis 56 californicus 42, 44, 45, 52 canalis 57 capitaneus 40, 52 catus 41, 52 caumonti 56 centurio 52 ceylanensis 40, 52 chaldeus 36, 40, 46, 52 concavus 56 concinnus 60 conditorius 59 coronatus 36, 40, 52 cylindraceus 57 alli 41, 42, 43, 52 daucus 53 diadema 42, 44, 45, 52 dispar 52 distans 52 dorriensis 52 dujardini 190 ebraeus 36, 38, 41, 44, 45, 46 edwardsi 60 elongatus 52 emaciatus 52 episcopus 41, 52 ermineus 35, 44, 52, 53 fergusoni 36, 46, 47, 48, 52 flavidus 41 frigidus 41, 52 furvus 52 generalis 53 genuanus 52 geographus 9, 52 gladiator 41, 52 gloriamaris 52 ubernator 52 ornii 59 imperialis 41, 52 inscriptus 53 jaspideus 53 juliae 53 latus 57, 59 leopardus 40, 53 litteratus 40, 52 lividus 41, 44, 45, 52 loroisi 52 lucidus 41, 46, 49, 50, 52 maculosus 53 magus 35, 36, 41, 44, 45, 45, 47, 48, 48, 50, 52 mahogani 45, 52 maldivus 53 marmoreus 41, 52 marticensis 57 mercator 52, 53 miles 40, 52 miliaris 36, 40, 52 millipunctatus 53 mindanus 53 minimus 56 monachus 53 monile 52 mucronatus 53 natalensis 52 nicobaricus 52 nigropunctatus 52 nussatella 53 nux 40, 52 omaria 48, 52 orion 52 paniculus 52 parisiensis 190 patricius 35, 36, 41, 45, 46, 46, 48, 49, 5052 pennaceus 36, 41, 42, 43, 44-45, 46, 48-50, 52 perplexus 52 piperatus 52 poormani 52 primitivus 57, 58 princeps 39, 41, 52 pulcher 36, 46, 47, 52 pulicarius 41, 53 purpurascens 41, 52 ranunculus 53 rattus 40, 52 recurvus 52 INDEX regius 53 regularis 41, 52 remondii 59 restitutus 59 rouaulti 60 scabriusculus 40, 52 scalaris 52 scitulus 52 semicostatus 57, 59 senessei 57, 58 simplex 52 sponsalis 40 spurius 53 stercomuscarum 52 Striatellus 52 Striatus 41, 53 taeniatus 40, 53 tessulatus 53 textile 41, 52 tiaratus 40, 52 tornatus 36, 42, 44, 45, 52 tuberculatus 57 Пра 52 varius 52 ventricosus 41, 52 venulatus 52 verneuilli 57 vexillum 40, 52 victor 52 victoriae 52 vidua 52 virgatus 36, 39, 45, 50, 52 virgo 41 vittatus 52 ximenes 45, 52 zonatus 41, 52 cooperi, Aldisa 246 Coralliobia akibumii 132, 137 inflata 137 Coralliophila inflata 137 pyriformis 132, 137-138 radula 138 Corbula 167, 170, 174, 192 elegans 192 gib 192 idonea 192 rugosa 192 truncata 192 cornuta, Cassis 134 coromandelicus, Conorbis 56 coronata, Doto 248 coronata, Facelina 242, 248, 297 coronatus, Conus 36, 40, 52 corrugata, Xenophora 134 Coryphella 245, 297 browni 247 fusca 247 racilis 247 ineata 247, 297 nobilis 247 parva 247 pedata 247, 293, 297 pellucida 242, 247 salmonacea 249, 281, 282, 286 stimpsoni 282 trilineata 247 335 verrucosa 247 Costacallista laevigata 192 Costasiella 209 Шапае 268 costata, Parvilucina 191 Crassatella 191 vadosa 191 Crassatellites 191 crassicomis, Hermissenda 248 crassicostata, Lienardia 83 crassigranosa, Niotha 189 Crassipirinae 80-84 crassiplicatus, Fusinus 132, 139 Crassispira 190 Crassostrea virginica 158 Cratena peregrina 247, 293, 297 pilata 24 craticulata, Hadriania 189 Crenella orbicularis 190 crenulata, Terebra 30, 33 Creseis 225 acicula 225 Crimora 212, 213, 216 papillata 244, 246 cristatus, Janolus 248, 297, 324 crosslandi, Sebadoris 246, 259-261 crucispiculata, Rhodope 311 cruentus, Spondylus 134 Cryptoconinae 56, 57 Cryptoconus 56, 57 mcnairyensis 59 Cryptomya californica 192 Ctena decussata 191 orbiculata 191 Ctenidiacea 308 cuenoti, Cumanotus 220 culcitella, Acteocina 314 Cumanotus beaumonti 206, 219-221, 220, 247 cuenoti 220 fernaldi 220-221 laticeps 219 cumingi, Siliquaria 134 cumingii, Leptoconchus 260-261 curtus, Colus 165 curtus, Sipho 165 Cuspidaria cuspidata 193 cuspidata, Cuspidaria 193 cuspidata, Lanceolaria oxyrhyncha 132, 144 Cuthona adyarensis 247 albocrusta 247 albopunctata 247 caerulea 297 coerulea 247, 297 concinna 325 divae 325 futairo 247 genovae 247 ranosa 249 llonae 247 miniostriata 247 nana 245, 268 ocellata 247 omata 247 pinnifera 247 poritophages 249 336 INDEX pustulata 245 Cuvierina 225, 317 columella 225 Cyamioidea 164 cyanea, Phylinopsis 315 cyclindraceus, Cylichna 59 cyclindrica, Atys 225, 227, 315 yclocardia subtenta 191 cydia, Dillia 7 yerce 209 Cylichna 317, 319 alba 314 attonsa 314 cyclindraceus 59 melitopolitana 190 rubignosum 190 tubulosa 317 Cylichnina girardi 295 Cylichnium 319 africanum 314 cylindraceus, Conus 57 cylindrica, Malanochlamys 315 cylindrica, Volvulella 315 ylindrobulla 317 Cylindrobullidae 308, 316, 317, 322, 325 Cyllene 189 Cymatium 189 cymoelium, Haminoea 292-293 Cypraeacea 316 Cythara subcylindricata 190 Cytharinae 57 dactylomela, Aplysia 260-261 dalli, Conus 41, 42, 43, 52 danieli, Capulus [borehole] 158 Daphnella 83, 85 flammea 83 nobilis 132, 140 olyra 83 omata 83 Daphnellinae 25, 31, 80-84 daucus, Conus 53 declivis, Pachecoa 191 decussata, Ctena 191 deltoides, Plebidonax 192 dendritica, Placida 296 Dendrodoris fumata 246, 259-261, 263, 265, 266 randiflora 293 rebsi 246, 249 limbata 249, 293, 294, 296 Dendronotacea 320 Dendronotus albopunctatus 248 frondosus 248 iris 248 subramosus 248 Dentalium 193 bedensis 193 complexum 193 formosum 132, 141 laqueatum 168 Dentalium (Episiphon) candelatum 132, 141 Dentalium (Pictodentalium) formosum hirasei 132, 141 dentatus, Loripes 191 dentatus, Trochus 260-261 denticulata, Philine 263, 266 depilans, Aplysia 225, 227, 294, 295 Deroceras reticulatum 89-106 deusseni, Caryocorbula 192 devincta, Anadara 191 Diacria 225 trispinosa 225 diadema, Clavatula 5, 14, 15 diadema, Conus 42, 44, 45, 52 Diaphana 316, 317, 325 californica 315 minuta 315 Diaphanidae 315-317, 325 Diaphanoidea 310 Diaphorodoris 213 lirulatocauda 246 papillata 244 diardii, Chromodoris 242 Diaulula sandiegensis 242, 246 Dicata odhneri 247 na: Glossaulax 136 didyma, Neverita 175 digitalis, Pyramidella 190 Dillia cydia 7 diluvii, Anadara 191 dimidiata, Terebra 20, 30, 32, 33 dimidiata, Turricula 190 Dimyoidea 164 Dinocardium robustum 191 diomedea, Melanochlamys 315 diomedea, Tritonia 248, 281, 283, 285 Diplodonta subquadrata 191 directus, Ensis 174, 192 Dirona albolineata 248 auratia 248 Discodoris 213, 238, 260-261 concinna 246, 258, 260-261 erythraeensis 246, 260-261, 266, 267, 268, 269 pusae 238 rosi 249 tema 238 discus, Dosinia 158 dislocata, Terebra 190 dispar, Conus 52 dissimilis, Acropsis 191 dissita, Ervilia 191 distans, Conus 52 distincta, Calipitaria 192 divae, Cuthona 325 divaricata, Acila 142 divaricata, Divaricella 191 divaricata, Lucinella 191 Divaricella divaricata 191 ornata 191 diversicosta, Beguina 191 Docoglossa 197, 198, 201 doerga, Doto 248 Dolabella auricularia 227, 260-261 Dolabriferinae 322 doliella, Evelynella 190 Donacilla angusta 174, 191 donacina, Tellina 192 Donax 192 faba 192 INDEX irus 143 semistriatus 170, 192 trunculus 170, 192 vittatus 192 Dondice occidentalis 247 paguerensis 247 doriae, Eubranchus 248 Doridella 308 minus 246, 249 obscura 246, 281, 282 steinbergae 246, 281, 282 Doridina 211-217 Doriopsilla miniata 245 pharpa 249 rarispina 293 Doriopsis aurantiaca 246 viridis 246 Doris 213, 293 bicolor 296 ocelligera 246 verrucosa 293, 296, 297 dorriensis, Conus 52 Dorsanum duplicatum 189 Dosinia concentrica 158 discus 158 dunkeri 192 lupinus 192 Doto coronata 248 doerga 248 fragilis 248 japonica 248 paulinae 248 pinnatifida 248 rosea 248 yongei 248 Drepanocheilus calcarata 189 neglecta 189 Drilliinae 80-85 dubia, Facelina 248 dubia, Pleurotomella 81 dubia, Polycera 296 dujardini, Conus 190 dujardini, Nassa 189 dunkeri, Bursa 132, 137 dunkeri, Dosinia 192 dunkeri, Solecurtus 132, 143 Duplicaria 33 duplicata 20, 28, 32 fictilis 28 kieneri 28 lamarckii 28 spectabilis 20, 24, 25-27, 28, 32 duplicata, Duplicaria 20, 28, 32 duplicata, Neverita 161, 165, 169-171, 174, 175. 178 duplicatum, Dorsanum 189 ebraeus, Conus 36, 38, 41, 44, 45, 46 eccentrica, Rutitrigonia 191 echinogyra, Atlanta 107-111, 112, 114, 115, 116, 120, 121, 122, 123, 129 edule, Cerastoderma 191 edulis, Mytilus 190 edwardsi, Conus 60 egretta, Ardeadoris 244 elatus, Nassarius 189 337 Eledone 149, 151, 152 caparti 152 cirrhosa 147, 148, 152 gaucha 147, 148, 150, 152 massyae 147, 148, 150, 152, 153 moschata 148, 152 nigra 152 thysanophora 152 Eledoninae 147-154 Eleganiscala 132, 136 elegans, Corbula 192 elegans, Haminoea 315 elegans, Hypselodoris 233, 235, 236, 237, 238, 239, 247, 293 elegans, Okadaia 157, 249; borehole 160 elegans, Okenia 215, 296 elegantula, Chromodoris 244 elenense, Laevicardium 191 Eleutherobranchia 309, 310 elevata, Anadara 191 elliptica, Spisula 163, 191 elongatus, Conus 52 elstoni, Toxiclionella 14 Elysia cauze 268 olivaceus 260-261 papillosa 268 timida 293, 296 viridis 296 Elysiidae 209, 317 emacerata, Tellina 192 emaciatus, Conus 52 Embletonia gracilis 249 pulchra 247, 297 emertoni, Polycerella 246, 296, 297 emicator, Oliva 133, 134 emphaticus, Limopsis tajimae 132, 142 engeli, Flabellina 248 Ennucula kalimnae 190 enode, Cardium 143 Ensis 173 directus 174, 192 Entalina majestica 132,141 quadrangularis 141 Entaliopis brevis 193 Eopleurotoma 190 ephamilla, Notocorbula 192 Epicodakia 191 Epicyprina angulata 192 subtruncata 192 episcopus, Conus 41, 52 Episiphon 132, 141 candelatum 141 Epitonium spinosa 189 Epitonium (Papyriscala) halimense 135 Ercolania funerea 296 Eriphyla striata 191 ermineus, Conus 35, 44, 52, 53 Erosaria tomlini maturata 132, 136 tomlini ogasawarensis 136 Erronea caurica 134 hirasei 134 Ervilia dissita 191 ousilla 191 erythraeensis, Discodoris 246, 260-261, 266, 267, 268, 269 erythraeus, Trochus 260-261 338 INDEX erythrostoma, Oliva 133, 134 Etrema 81, 83, 85 Eubranchidae 321 Eubranchus cingulatus 247 doriae 248 exiguus 248, 297 farrani 206, 243, 244, 248, 283, 286 misakiensis 248 olivaceus 248 pallidus 248 tricolor 242 Eucithara 81, 83, 85 marshellensis 85 Euclathurella 85 Euclio 225 pyramidata 225 Eucrassatella 170, 191 Eucyclotoma 83-84 Eudolium inflatum 132, 137 lineatum inflatum 137 Euhadra brandtii roseoapicalis 140 grata gratoides 132, 140 Euhelicoida 202 Eulima subulata 189 Eulimella conulus 190 Eupleura caudata 189 Eupleura [borehole] 158 europeum, Cerithium 189 Euselenops 317 Euspira alderi 161, 163, 170, 171, 175, 176 helicina 156 heros 161, 177 lewisii 173, 174 nitida 161 rectilabrum 167 Euthyneura 197, 198, 308, 309 "(Eu-)Ctenidiacea" 308 evelinae, Ancula 246 Evelynella doliella 190 exasperatus, Jujubinus 188 exiguus, Eubranchus 248, 297 exilis, Clavus 83 exilis, Iredalea 81, 83 Exilla wellmani 189 exoleta, Mactrellona 191 faba, Donax 192 faba, Paraesa 192 Facelina 297, 325 annulicornis 248, 297 coronata 242, 248, 297 dubia 248 fusca 248 Facelinidae 325 faeroensis, Polycera 244 falklandica, Philine 319, 321 Falsicolus tangituensis 189 farrani, Eubranchus 206, 243, 244, 248, 283, 286 fasciata, Aplysia 293, 296 fasciatus, Strombus 260-261 Favorinus argentimaculatus 245 auritulus 248 branchialis 248, 293, 297 Fehria 70 fergusoni, Conus 36, 46, 47, 48, 52 fernaldi, Cumanotus 220-221 fictilis, Duplicaria 28 fictilis, Terbra 33 Ficus 72 filix, Thordisa 246 fimbriata, Melibe 248 finmarchica, Philine 314, 321, 323 Fiona pinnata 248 Fissurella barbadensis 164 fissurella, Rimella 189 Fissurellidae 201 Fissurelloidea 164 fittoni, Confusiscala 189 Flabellina 245 affinis 248 babai 325 oT 325 engeli 248 ns 325 islandica 321 Flabellinidae 321, 325 flammea, Daphnella 83 flava, Ptychodera 10 Flaventia ovalis 192 flavidus, Conus 41 flavum, Laevicardium (Vasticardium) 143 "Floraconus? kinoshitaf' [nom. nud.] 140 floridana, Pseudomiltha 173, 191 fordi, Ventricolaria 160 formosa, Hero 248 formosa, Nicaniella 191 formosum, Dentalium (Pictodentalium) 132, 141 forskali, Nerita 260-261 Fossarus granosus 189 fragilis, Doto 248 fragilis, Mactra 191 fragilis, Nuculana 190 Fragum fragum 191 Fragum loochooanum 132, 142 fragum, Fragum 191 francolina, Nassa 258, 260-261 frigidus, Conus 41, 52 frondosus, Dendronotus 248 fukueae, Neptunea 132, 138 fulvipunctata, Chelidonura 315 fumata, Dendrodoris 246, 259-261, 263, 265, 266 funerea, Ercolania 296 fungina, Tylodina 316 funiculata, Nerita 188 funiculata, Terebra 20, 29, 31 furtiva, Thorunna 244 furvus, Conus 52 fusca, Atlanta 109, 110, 117, 123, 124, 129 fusca, Coryphella 247 fusca, Facelina 248 fuscata, Tenellia 245 Fusinus 189 crassiplicatus 132, 139 gemmuliferus 132, 139 tuberculata 259, 260-261, 263, 268 "Fusinus kirana" [MS.] 139 Fustiaria miocaenica 193 "Fusus" cingulatus 30 INDEX fusus, Tibia 134 futairo, Cuthona 247 "Gadila novilunata" [nom. nud.] 141 Gafrarium minimum 192 pectinatum 192 Galeoastraea millegranosa 132, 135 Galeoastraea (Hansazaea) millegranosa 135 galleana, Hastula 20 gallina, Chamelea 192 Gari hamiltonensis 192 Gastrochaenoidea 164 Gastropteridae 315, 317-319, 322 Gastropteron citrinum 317 pacificum 315 rubrum 317 gaucha, Eledone 147, 148, 150, 152 gaudichaudi, Atlanta 109, 114, 176, 120 Gaza sericata 132, 135 Geganyia 198 Gemma gemma 169, 192 gemma, Gemma 169, 192 Gemmaterebra catenifera 190 Gemmula 83, 85, 190 gemmuliferus, Fusinus 132, 139 generalis, Conus 53 Genota 57 ramosa 190 genovae, Cuthona 247 genuanus, Conus 52 geographus, Conus 9, 52 ghardaqana, Chromodoris 260-261 ghiselini, Hypselodoris 244 gibba, Corbula 192 gibba, Philine 319, 321 gibberula, Sunetta 192 gibberulus, Strombus 260-261 gibbosa, Ancula 244, 246 gibbosa, Atlanta 107, 109 Gibbula varia 188 giganteus, Saxidomus 174, 192 gigas, Tugali 134 girardi, Cylichnina 295 glaber, Strombiformis 189 glabra, Idonearca 191 glabrum, Caecum 189 gladiator, Conus 41, 52 glauca, Aeolidiella 247 glaucoides, Calma 297 Glauconome chinensis 192 globosus, Leptoconchus 260-261 globulus, Pustularia (Pustularia) 136 gloriamaris, Conus 52 gloriosum, Guildfordia henicus 135 GENE. Pseudastralium henicus 132, Glossaulax 132, 136, 173 didyma 136 Glossodoris 293 atromarginata 247 averni 244 obsoleta 249 pallida 244, 247 sibogae 249, 264 undaurum 244 Glossoidea 164 ae marica japonica 143 Glycymeris 167, 191 albolineata 191 lycymeris 170 Рай 191 insubrica 191 pulvinata 191 vestita 191 glycymeris, Glycymeris 170 Glycymerita sublaevis 191 umbonata 191 Golikovia 138 Goniodoris 213, 216 castanea 215, 246 nodosa 214, 246 sugashimae 246 Gosavia 57 tuberculatus 58 gouldi, Terebra 23, 25, 30, 32, 33 Gouldia minima 192 gouldiana, Bulla 315 gracile, Cirsocerithium 189 gracilis, eels 247 gracilis, Embletonia 249 gracilis, Hypselodoris 239 gracilis, Scaphander 314 grandiflora, Dendrodoris 293 Graneledoninae 147 grannulata, Paradoris 293 granosa, Anadara 170, 176, 191 granosa, Cuthona 249 granosus, Fossarus 189 granulata, Turritella 189 Granulifusus 189 kiranus 132, 139 grata, Euhadra 132, 140 gratoides, Euhadra grata 132, 140 grayana, Lanceolaria 144 greggiana, Venericardia 191 Greilada 213 gualteriana, Natica 161 gubernator, Conus 52 Guildfordia henicus gloriosum 135 guttata, Terebra 28, 29, 31 Gymnodoris 260-261 bicolor 246 citrina 246 Gymnomorpha 308-310 Gymnosomata 308, 316, 317 gymnota, Catriona 242, 247 Hadriania craticulata 189 Halgerda rubicunda 246 halimense, Epitonium (Papyriscala) 135 Haliotis 197 halli, Glycymeris 191 hamiltonensis, Gari 192 Haminoea 309-310, 317, 319, 321, 322 cymoelium 292-293 elegans 315 hydatis 225, 292, 293, 295 navicula 227, 294, 295 orbignyana 295 solitaria 315 strongi 315 339 340 INDEX vesicula 315 virescens 315 Haminoeidae 315, 317, 319, 321, 322, 324 Hancockia 325 burni 248 californica 325 uncinata 248, 325 Hastula 28-30 aciculina 20, 28, 31 albula 20 bacillus 20, 21 21-23, 22, 23, 27-29, 29 31, 32:33 cinerea 20, 29 alleana 20 ectica 20, 29 inconstans 20, 26-27, 30 penicillata 28, 30 salleana 20, 28, 30, 31 solida 20 strigillata 30 hebes, Acteon 314 hectica, Hastula 20, 29 hectica, Terebra 20, 21 helicina, Euspira 156 Helicinoidea 201 helicinoides, Atlanta 108, 108, 109, 109, 110, 114, 117, 125, 126, 129 Helicocryptus radiatus 188 Helicoida 202 Helminthope 207, 304-307, 308, 310 psammobionta 301, 304-307, 305, 306, 308, 311 Hemiconus 55-57, 65 henicus, Pseudastralium 132, 135 heraclitica, Tornatina 190 Hermaeidae 209, 317 Hermissenda crassicomis 248 Hermosita 325 Hero formosa 248 heros, Euspira 161, 177 Herviella mietta 249 Hesperiturris nodocarinatus 190 Heterocithara marwicki 190 Heteromacoma irus oyamai 143 Hexabranchus sanguineus 242, 246, 257, 259-261, 262, 263, 265, 266, 269 Hexaplex benedeica 189 Hiatella arctica 192 hillana, Protocardia 191 hinomotoensis, Baryspira 139 Hipponix 189 hirasei, Dentalium (Pictodentalium) formosum 132, 141 hirasei, Erronea 134 hirasei, Mitropifex 132, 139-140 hirasei, Oliva 132, 139 Hirisazaea 135 hirundinina, Chelidonura 315 hispidula, Raphitoma 190 Holohepatica 308 hombergi, Tritonia 248, 281, 283, 285 Homoiodoris japonica 246 Hormospira maculosa 4 hornii, Conus 59 hosoyai, Neverita (Glossaulax) 132, 136 hummelincki, Peltodoris 246 hyalinus, Janolus 325 fi haces pr striata 225 A bare a 225 ydatina 317 physis 225, 230, 314, 320 zonata 225, 227, 229, 230, 314 Hydatinidae 224, 314, 318, 319, 322 hydatis, Haminoea 225, 292, 293, 295 'ydrobia andrussowi 188 Hydrobiidae 196 ypselodoris 213, 233-240 agassizii 244 bennetti 239, 249 bilineata 236, 239, 243, 244, 247 californiensis 244 cantabrica 233, 236, 244 coelestis 236, 239 elegans 233, 235, 236, 237, 238, 239, 247, 293 ghiselini 244 racilis 239 ayae 247 kulomba 244 lapislazuli 244 messinensis 236, 238, 239, 244, 293 tema 244 tricolor 233, 236, 238 valenciennesi 244 villafranca 235, 238, 244, 249, 293, 296 webbi 244 ichinoseana, Asprella (Conasprella?) 132, 140 idonea, Corbula 192 Idonearca glabra 191 lhungia ponderi 188 ilonae, Cuthona 247 Imaclava 7 Imaclava unimaculata 14 imbricatus, Serpulorbis 134 imitatrix, Terebra 21, 23, 27, 28, 30, 31, 33 imperialis, Conus 41, 52 impexa, Okenia 246 inaequalis, Palaeomoera 192 incei, Conuber 161 incei, Polinices 161 inclinata, Atlanta 109, 128 inconspicula, Rissoa 188 inconstans, Hastula 20, 26-27, 30 incrassata, Avellana 190 inculta, Acteocina 314, 317 inermis, Navanax 315 inflata, Atlanta 107-110, 114, 115, 117, 123, 125, 126, 129 inflata, Coralliobia 137 inflata, Coralliophila 137 inflata, Limacina 225 inflata, Mohrensternia 188 inflatum, Eudolium 132, 137 inflatum, Eudolium lineatum 137 infundibulum, Philine 315, 323 infuscatus, Cantharidus (Kanekotrochus) 135 Inglisella allophyla 190 parva 190 innerans, Notocorbula 192 INDEX inomata, Chelidonura 315 inomata, Chromodoris 247, 258, 259-61, 265, 266 Inquisitor 83, 85 inscriptus, Conus 53 insubrica, Glycymeris 191 interlirata, Mitra 140 interstincta, Pyrgulina 190 iodinea, Flabellina 325 Iredalea 84 exilis 81, 83 iris, Dendronotus 248 irisans, Oliva 139 irregularis, Barbatia 191 irus, Donax 143 irus, Heteromacoma 143 Irus ishibashianus 132, 143 irus, Venerupis 143 isaotakii, Buccinum 132, 138 Iscafusus rigidus 189 ishibashianus, Irus 132, 143 ishibashianus, Notirus 143 islandica, Arctica 192 islandica, Flabellina 321 italicus, Nassarius 189 Janolidae 321, 324 Janolus 325 australis 324 capensis 324 cristatus 248, 297, 324 hyalinus 325 longidentatus 324, 325 Japonateon 317 japonica, Doto 248 Japonica, Glycydonta marica 143 Japonica, Homoiodoris 246 Japonica, Leukoma 132, 143 Japonica, Leukoma marica 143 japonica, Mitra (Scabricola) 139 Japonica, Spurilla 248 japonica, Tapes 192 jaspideus, Conus 53 Jorunna 213 tomentosa 246 Jujubinus exasperatus 188 juliae, Conus 53 kalimnae, Ennucula 190 anne, Cantharidus" [nom. nud.] 132, 1 Kanekotrochus 135 Katelysia scalarina 192 Katherinella 169 angustifrons 192 kawamurai, Latiaxis 132, 138 kayae, Hypselodoris 247 kelloggi, Retusa 190 keraudreni, Oxygyrus 108-111, 112, 128 Kermia 84 clandestina 83 maculosa 82 pumila 83 kieneri, Duplicaria 28 kieneri, Terebra 33 kiiensis, Murex 132, 137 341 kiiensis, Nassarius (Alectrion) 139 kiiensis, Nassarius (Zeuxis) 132, 139 kingae, Xenuroturris 83 kinoshitai, Chelyconus 132, 140 "kinoshitai, Floraconus?" [nom. nud.] 140 kirana, Babylonia 138 kiranus, Granulifusus 132, 139 krebsi, Dendrodoris 246, 249 krohni, Chromodoris 233, 234, 236, 239, 244, 296 kulomba, Hypselodoris 244 kupriyanovi, Aforia 6 kurodai, Cirsotrema (Elegantiscala) 132, 136 lacteus, Loripes 191 Laevicardium elenense 191 Laevicardium (Vasticardium) flavum 143 laevigata, Costacallista 192 laevigata, Thetis 191 laevis, Cadlina 249, 258, 268, 279, 281, 282, 284, 286 lajonkaireana, Acteocina 190 lamarckii, Duplicaria 28 lamarckii, Magilopsis 260-261 lamarckii, Myurella 28 Lambis truncata 260-261, 264, 268, 269 Lamellaria 164 Lamellariacea 316 Lamellariidae 164 lamelliferus, Terefundus 189 Lanceolaria grayana 144 oxyrhyncha cuspidata 132, 144 lapislazuli, Hypselodoris 244 laqueatum, Dentalium 168 Latiaxis 132 kawamurai 132, 138 laticeps, Cumanotus 219 Latirus moorei 189 latus, Conus 57, 59 laugieri, Calliostoma 188 leachii, Bursatella leachii 294, 296 leanum, Cochlodesma 193 leonina, Melibe 248, 283 leopardus, Conus 40, 53 Lepetelloidea 201 leporina, Tethys 310 Leptoconchus cumingii 260-261 globosus 260-261 Leptonoidea 164 leptospira, Plicarcularia 189 lesueuri, Atlanta 109, 110, 114, 115, 116, 118, 179, 128 leucostoma, Buccinum 138 Leukoma japonica 132, 143 marica Japonica 143 levidensis, Oenopota 70-72 lewisii, Euspira 173, 174 lewisii, Polinices 174 libya, Tiariturris 28 Lienardia 81, 83, 85 crassicostata 83 lutea 83 mighelsi 83 lignarius, Scaphander 225, 227, 229, 314, 322 342 INDEX lilianae, Costasiella 268 lima, Philine 315, 321, 323 Limacia 213 clavigera 242, 244, 296 limaciformis, Nembrotha 246, 260-261 Limacina 225, 230, 317 inflata 225 retroversa 316 Limacinidae 226, 316, 318 Limapontia capitata 294, 296 limbata, Dendrodoris 249, 293, 294, 296 Limenandra nodosa 248 Limoidea 164 Limopsis 167 beaumarisensis 191 chapmani 191 minuta 191 tajimae emphaticus 132, 142 linearis, Philbertia 9, 25 lineata, Coryphella 247, 297 lineata, Mesosaccella 190 lineata, Paramorea 189 lineatum, Eudolium 137 lineolata, Venilicardia 192 Liopeplum canalis 59 Lirasyrinx 70 Lirodiscus tellinoides 167, 191 lirulatocauda, Diaphorodoris 246 Lithophagidae 164 litteratus, Conus 40, 52 littorea, Littorina 188 Littorina 73, 205 littorea 188 Littorinoidea 202 lividus, Conus 41, 44, 45, 52 Lobiger 294 serradifalci 296 Lomanotus stauberi 248 longidentatus, Janolus 324, 325 longirostris, Cavolinia 225, 226, 227-230 loochooanum, Fragum 132, 142 Lophiotoma 70, 83, 85 acuta 81, 83 Lophioturris 70 Lophitoma 190 Lophopleurella 317 loringi, Chromodoris 249 Loripes dentatus 191 lacteus 191 loroisi, Conus 52 Loxocardium bouei 191 lucidus, Conus 41, 46, 49, 50, 52 Lucina anodonta 191 approximata 191 spinifera 191 Lucinella divaricata 191 Lucinidae 166 lugubris, Phestilla 242, 248 lupinus, Dosinia 192 lusoria, Meretrix 192 lutea, Lienardia 83 luteofasciatus, Theodoxus 188 luteopunctata, Chromodoris 234, 247 luteorosea, Chromodoris 233, 234, 236 luteorufa, Antonietta 247 lux, Tellina 192 lynceus, Phidiana 248 yonsia 174 macmurdensis, Austrodoris 249 Macoma albaria 192 arctata 192 balthica 174, 192 calcarea 192 nasuta 192 oyamai 143 Macrocallista nimbosa 192 Macteola 81, 84 Mactra angulata 191 australis 191 chinensis 191 fragilis 191 stultorum 191 Mactrellona exoleta 191 maculata, Terebra 20, 23, 25, 32 maculata, Trapania 244 maculosa, Hormospira 4 maculosa, Kermia 82 maculosa, Natica 170, 176 maculosus, Conus 53 Magilopsis lamarckii 260-261 magus, Conus 35, 36, 41, 44, 45, 45, 47, 48, 48, 50, 52 mahogani, Conus 45, 52 majestica, Entalina 132, 141 Malanochlamys cylindrica 315 maldivus, Conus 53 Mamillocylichna 319 richardi 314 Mamilloretusa mammillata 292, 293, 295 mammilla, Polinices 163, 173, 178, 260- 261 mammillata, Mamilloretusa 292, 293, 295 mandibula, Panopea 192 Mangelia 70 striolata 71 vauquelini 71 Mangeliinae 80-84 Mangiliella 70 multilineolata 71 taeniata 71 mannarensis, Aeolidiella 247 manneringi, Smeagol 308 marcusi, Rhodope 301, 308, 310 Margarita 163 margarita, Pustularia 132, 136 margaritaceum, Periploma 172 Margarites monolifera 188 Marginella 189 marica, Glycydonta 143 marica, Leukoma 143 marica, Timoclea 192 marmoreus, Conus 41, 52 marshellensis, Eucithara 85 marticensis, Conus 57 marwicki, Heterocithara 190 massyae, Eledone 147, 148, 150, 152, 153 Mathildidae 201 maturata, Erosaria tomlini 132, 136 Mauidrillia occidentalis 190 mcfarlandi, Chromodoris 244 mcnairyensis, Conorbis 57 INDEX menairyensis, Cryptoconus 59 meckelii, Pleurobranchaea 238, 296 mediterraneum, Umbraculum 227, 228, 230 meditteranea, Philippia 190 ЕЕ squalida 192 melanobranchia, Phestilla 242,248, 281, 283, 285 Melanochlamys 317, 321 diomedea 315 Melanodrymia 198, 201 melanostoma, Polinices 260-261, 263 Melibe fimbriata 248 leonina 248, 283 melitopolitana, Cylichna 190 Melletia 190 Meloscaphander 317 mercator, Conus 52, 53 Mercenaria 170 campechiensis 192 mercenaria 174, 192 mercenaria, Mercenaria 174, 192 Meretrix lusoria 192 meridionalis, Choromytilus 176, 190 Mesalia 173, 189 amekiensis 189 regularis 189 Mesogastropoda 10 Mesosaccella angulata 190 lineata 190 messinensis, Hypselodoris 236, 238, 239, 244, 293 meteori, Atlanta 107, 108, 109, 110, 114, 127, 128, 129 metula, Mitromorpha 83 Mexichromis antonii 244 porterae 244 tricolor 243, 244, 249 tura 244 michaeli, Siphopteron 315 Michela trabeatoides 190 micra, Veremolpa 192 Microdaphne 84 trichodes 82 Micromelo 317 undata 314 microurceum, Canarium 132, 136 Microvoluta nodulata 189 mietta, Herviella 249 mighelsi, Lienardia 83 miles, Conus 40, 52 miliaris, Atys 190 miliaris, Conus 36, 40, 52 millegranosa, Galeoastraea (Harisazaea) 135 millipunctatus, Conus 53 mindanus, Conus 53 miniata, Doriopsilla 245 minima, Gouldia 192 minimum, Gafrarium 192 minimus, Actaeonina 58 minimus, Conus 56 miniostriata, Cuthona 247 minor, Mitrella 189 minor, Phestilla 206 minus, Doridella 246, 249 minuta, Diaphana 315 343 minuta, Limopsis 191 minutissima, Carinapex 83 Mioawateria personata 190 miocaenica, Fustiaria 193 misakiensis, Eubranchus 248 Mitra interlirata 140 orientalis 189 Mitra (Cancilla) yagurai 132, 140 Mitra (Scabricola) japonica 139 Mitra (Tiara) yagurai 140 Mitrella 189 minor 189 nassoides 189 Mitromorpha 83 alphonisana 83 metula 83 Mitropifex hirasei 132, 139-140 mixta, Nucula 190 modesta, Alderia 296 Modiolus auriculatus 190 reversa 190 Mohrensternia angulata 188 inflata 188 monachus, Conus 53 monidum, Strioterebrum 173, 190 monile, Conus 52 Monilea 188 Monodonta neritoides 134 perplexa 134 monolifera, Margarites 188 Monoplacophora 165 montereyensis, Archidoris 246 moorei, Latirus 189 Moridilla brockii 245 morrhuana, Pitar 192 Morula 189 moschata, Eledone 148, 152 mucronatus, Conus 53 multilamella, Venus 192 multilineolata, Mangiliella 71 mundus, Scaphander 314, 322 Murex kiiensis 132, 137 muricata, Onchidoris 215, 246, 281, 283, 285 Muricidae 156, 164 Muricoidea 156 Mutiella canaliculata 191 Mya 161, 170, 173 arenaria 163, 174, 176, 192 Me papitikiensis 191 'ysidioptera 166, 172 williamsi 191 Mytilus 170 edulis 190 Myurella lamarckii 28 Nacelloidea 201 nana, Comitas 190 nana, Cuthona 245, 268 nanaimoensis, Acanthodoris 246 Nassa dujardini 189 francolina 258, 260-261 restitutiana 189 Nassariidae 165 Nassarius 73 castus 139 344 INDEX elatus 189 italicus 189 obsoletus 189 perpinguis 168, 189 pygmaeus 189 semistriatus 189 tiarula 189 trivittatus 177, 189 Nassarius (Alectrion) kiiensis 139 Nassarius (Zeuxis) kiiensis 132, 139 nassoides, Mitrella 189 nassoides, Terebra 20, 24, 25, 27, 28, 30, 33 nasuta, Macoma 192 natalensis, Conus 52 Natica 168, 171 canrena 164 clausa 165 gualteriana 161 maculosa 170, 176 pusilla 165 stercusmuscarum 177 tecta 176 Naticidae 11, 155-193, 316 naukum, Atys 229 Navanax 318 aenigmaticus 315 inermis 315 a 315 navicula, Haminoea 227, 294, 295 neapolitana, Onchidoris 246 neapolitana, Spurilla 248, 293, 294, 297 neglecta, Drepanocheilus 189 nelliae, Turricula 8, 10, 14 Nembrotha limaciformis 246, 260-261 nemoralis, Cepaea 205 Neogastropoda 11, 17 Neolepetopsidae 201 Neomphalus 198 Neopleurotomoides 75 Neptunea fukueae 132, 138 Nerita forskali 260-261 funiculata 188 scabricosta 188 Neritimorpha 197, 198, 202 Neritina virginea 188 neritoides, Monodonta 134 Neverita 170 didyma 175 duplicata 161, 165, 169-171, 174, 175, 178 Neverita (Glossaulax) hosoyai 132, 136 Nicaniella formosa 191 nicobaricus, Conus 52 nigra, Eledone 152 nigrobranchiata, Cadlina 244 nigropunctatus, Conus 52 nimbosa, Macrocallista 192 Niotha crassigranosa 189 nitida, Euspira 161 nitida, Ringicula 314, 319 nitidula, Aegopinella 157, 162; borehole 162 nitidula, Aphrodina 192 nitidula, Pupa 314 nivalis, Noumea 244 nobilis, Architectonica 160 nobilis, Coryphella 247 nobilis, Daphnella 132, 140 nobilis, Scaphander 314, 322 nodocarinatus, Hesperiturris 190 nodosa, Baeolidia 297 nodosa, Goniodoris 214, 246 nodosa, Limenandra 248 nodulata, Microvoluta 189 norwegicus, Volutopsius 259 Notaeolidia 321 Notaeolidiidae 321 Notarchus punctatus 296 Notaspidea 224, 226, 317, 318, 322, 323- 325 Notirus ishibashianus 143 Notocorbula ephamilla 192 innerans 192 Notospisula parva 170, 175, 191 Noumea nivalis 244 sudanica 244 Novanax 318 "novilunata, Gadila" [nom. nud.] 141 novilunatus, Cadulus (Platyschides) 132, 141 nucleus, Nucula 190 Nucula antiquata 190 mixta 190 nucleus 190 obtusa 190 turgida 190 Nuculana 190 fragilis 190 pella 190 pernula 190 Nuculana (Thestyleda) acinacea 132, 142 Nudibranchia 205, 241-255, 273-289, 308- 310, 316, 317, 323-325 nussatella, Conus 53 Nuttallia solida 132, 143 nuttallii, Clinocardium 191 nuttallii, Tresus 191 nux, Conus 40, 52 obliquata, Amphidonte 191 obscura, Doridella 246, 281, 282 obsoleta, Casella 258-261, 263, 264, 266, 267, 268 obsoleta, Glossodoris 249 obsoletus, Nassarius 189 obtusa, Nucula 190 obtusa, Retusa 227, 268, 315, 317, 318, 322, 324 obtusangula, Brachytoma 190 occidentalis, Dondice 247 occidentalis, Mauidrillia 190 ocellata, Cuthona 247 ocelligera, Aglaja 315 ocelligera, Doris 246 Octopodidae 147-154 Octopus bimaculatus [borehole] 160 odhnen, Archidoris 246 odhnen, Dicata 247 Odostomia 190 conoidea 190 Oenopota 71, 74, 75 INDEX levidensis 70-72 ogasawarensis, Erosaria tomlini 136 Oichnus paraboloides [ichnotaxon] 169 Okadaia 180, 318 elegans 157, 249; borehole 160 Okenia 213 ascidicola 246 elegans 215, 296 impexa 246 okinawaense, Vasticardium 142, 143 olearium, Tonna 259, 260-261 olicatum, Architectonica 190 oligogyra, Atlanta 107, 109, 110, 114, 116, 118, 119, 129 Oliva emicator 133, 134 erythrostoma 133, 134 hirasei 132, 139 irisans 139 olivacea, Oxynoe 227, 228, 230, 296 olivaceus, Elysia 260-261 olivaceus, Eubranchus 248 Olivella 14, 16, 16, 173 biplicata 189 Olividae 14, 65 olyra, Daphnella 83 omaria, Conus 48, 52 Onchidiacea 308 Onchidoris 213, 216 bilamellata 206-207, 215, 246, 273- 289, 283, 285 muricata 215, 246, 281, 283, 285 neapolitana 246 opercularis, Pecten 191 operculata, Retusa 318, 322, 324 Opisthobranchia 157, 201-327 orbicularis, Codakia 191 orbicularis, Crenella 190 orbiculata, Ctena 191 orbignyana, Haminoea 295 orientalis, Aglaja 315 orientalis, Mitra 189 orientalis, Phyllobranchillus 260-261 orion, Conus 52 omata, Cuthona 247 omata, Daphnella 83 omata, Divaricella 191 oryza, Acteocina 314, 317, 322 Ostreoidea 164 ousilla, Ervilia 191 ovalis, Flaventia 192 Oxygyrus 107, 111, 114 eraudreni 108-111, 112, 128 Oxynoacea 224 Oxynoe 226, 294 olivacea 227, 228, 230, 296 Oxynoidae 317 oxyrhyncha, Lanceolaria 132, 144 oyamai, Heteromacoma 132, 143 oyamai, Heteromacoma irus 143 oyamai, Macoma 143 Pachecoa declivis 191 pacifica, Atlanta 107 pacificum, Gastropteron 315 pacificus, Cassidulus 158 Paeltodoris 213 345 paguerensis, Dondice 247 Palaeomoera inaequalis 192 Palaeonucula 166 Strigilata 190 palatam, Quidnipagus 192 Palio 213 pallida, Ancilla 138 pallida, Babylonia 132, 138 pallida, Chelidonura 315 pallida, Chromodoris 260-261 pallida, Glossodoris 244, 247 pallida, Tenellia 245, 283, 284 pallidus, Eubranchus 248 Pandora 174 paniculus, Conus 52 Panopea mandibula 192 papillata, Alocospira 189 papillata, Crimora 244, 246 papillata, Diaphorodoris 244 papillosa, Aeolidia 247 papillosa, Elysia 268 papitikiensis, Myrtea 191 Papyriscala 135 bifasciata 132, 135 yokoyamai 135 paraboloides, Oichnus [ichnotaxon] 169 Paracomitas beui 190 Paradoris grannulata 293 Paraesa faba 192 Paramontana 84 Paramorea lineata 189 Parasyrinx 70 Paratectibranchia 309, 310 parisiensis, Conus 190 parva, Cor dae 247 parva, Inglisella 190 parva, Notospisula 170, 175, 191 Parvamplustrum tenerum 314 Parvicardium 170 scabrum 191 Parvilucina costata 191 Patellidae 197 Patellogastropoda 198 Patelloidea 164, 201 patricius, Conus 35, 36, 41, 45, 46, 46, 48, 49, 50, 52 paulinae, Doto 248 paxillus, Stricispira 10 Pecten opercularis 191 pectinatum, Gafrarium 192 Pectinoidea 164 pedata, Coryphella 247, 293, 297 Pelecyora trigona 170, 192 pella, Nuculana 190 pellucida, an 242, 247 pelsunca, Philinopsis 315 Peltodoris atromaculata 216 hummelincki 246 penicillata, Hastula 28, 30 penicillata, Pseudomelatoma 4, 5, 10; 28 pennaceus, Conus 36, 41, 42, 43, 44-45, 46, 48-50, 52 Pentaganglionata 308 Peraclidae 318 peregrina, Cratena 247, 293, 297 peresi, Atlanta 107 346 INDEX Periglypta reticulate 192 Periploma 193 margaritaceum 172 Peristernia 189 pernula, Nuculana 190 perola, Chromodoris 247 peroni, Atlanta 109, 110, 112, 114, 116, 118, 120, 129 Peronidia venulosa 192 perpinguis, Nassarius 168, 189 perplexa, Monodonta 134 perplexus, Conus 52 perpusilla, Sandbergeria 189 persimilis, Semicassis 132, 136-137 personata, Mioawateria 190 perstriata, Retusa 295 peruvianus, Tagelus 192 perversa, Triphora 189 Pervicacia 33 tristis 20, 24, 30 ustulata 33 Pervicaciidae 1, 3, 33 pespelecani, Aporrhais 189 Petalifera 317 petechialis, Chromodoris 242 Petunculus 167 Phalium bisulcatum 137 Phanerophthalmus 315, 317, 319, 321, 322, 324 pharpa, Doriopsilla 249 Phestilla 281 lugubris 242, 248 melanobranchia 242,248, 281, 283, 285 minor 206 sibogae 242, 280, 281, 283, 286 Phidiana lynceus 248 Philbertia 70, 83 linearis 9, 25 Philinacea 317, 319, 322 Philine 227, 315, 317, 319, 321, 323 alba 314, 319, 321, 323 angasi 321 aperta 225, 227-230, 294, 295, 310, 321 auriformis 321 bakeri 314 denticulata 263, 266 falklandica 319, 321 finmarchica 314, 321, 323 ibba 319, 321 infundibulum 315, 323 lima 315, 321, 323 powelli 321 quadrata 315, 321, 323 scabra 295 Philinidae 224, 314-315, 319, 321, 322 Philinoglossa 310, 317 Philinoglossidae 317 Philinopsis depicta 315 pelsunca 315 pilsbryi 315 speciosa 315 Philippia meditteranea 190 philippinarum, Ruditapes 174, 175, 192 philippinarum, Tapes 192 Pholadoidea 164 Pholadomyoidea 164 Phos 189 Phylinopsis cyanea 315 Phyllaplysia 317 taylori 268 Phyllidia varicosa 242, 246, 260-261 Phyllobranchillus orientalis 260-261 Phyllodesmium xeniae 248, 260-261, 263, 264, 266, 269 physis, Hydatina 225, 230, 314, 320 pica, Clavus 83 Pictodentalium 132, 141 formosum 141 pilata, Cratena 247 pilosa, Acanthodoris 246 pilsbryi, Philinopsis 315 pinnata, Fiona 248 pinnatifida, Doto 248 pinnifera, Cuthona 247 Pinnoidea 164 piperatus, Conus 52 Piseinotecus sphaeiferus 248 Pitar 192 morrhuana 192 Placamen subroboratum 192 Placida dendritica 296 viridis 296 Plakobranchus 209 plana, Atlanta 107-111, 112, 114, 116, 120, 121, 122, 129 plana, Callistina 192 plana, Scrobicularia 192 planata, Tellina 192 Platydoris 310 argo 213, 293 scabra 246, 260-261, 263 Platyschides 132, 141 virginalis 141 plebeia, Tritonia 248 Plebidonax deltoides 192 Pleurobranchacea 325 Pleurobranchaea 317 californica 325 meckelii 238, 296 Pleurobranchaeidae 322, 325 Pleurobranchidae 224, 317, 324 Pleurobranchinae 322 Pleurobranchomorpha 308-310 Pleurobranchus 317 Pleuroploca trapezium 258, 259, 260-261, 263, 269 Pleurotoma 190 Pleurotomaria 133 Pleurotomaroidea 164 Pleurotomella 75 allisoni 81 dubia 81 Plicarcularia leptospira 189 Plicatuloidea 164 plicosa, Pyramidella 190 pliocenicum, Strioterebrum 190 plumula, Berthella 227 podolica, Rissoina 188 Polinices 168, 171, 173 incei 161 INDEX lewisii 174 mammilla 163, 173, 178, 260-261 melanostoma 260-261, 263 tumidus 163 Bobalphen Navanax 315 Po erase 209 Polycera 213, 216 atra 213 dubia 296 faeroensis 244 quadrilineata 242, 244, 246, 293, 296, 297 Folycerella 213, 216 emertoni 246, 296, 297 Polyplacophora 165 ponderi, lhungia 188 poormani, Conus 52 poritophages, Cuthona 249 porterae, Mexichromis 244 powelli, Philine 321 powelli, Viridoturris 190 prea, Anisodoris 246 primitivus, Conus 57, 58 princeps, Conus 39, 41, 52 Prosobranchia 156, 257-271, 316, 318 Protatlanta 107, 111 souleyeti 108, 109-111, 112, 113, 175, 128 protexta, Terebra 29 Protocardia hillana 191 Protoginella bembix 189 Protothaca 192 staminea 192 proxima, Adalaria 246, 266, 280-282, 285, 286 Pruvotfolia pselliotes 248 psammobionta, Helminthope 301, 304- 307, 305, 306, 308, 311 pselliotes, Pruvotfolia 248 Pseudamnicola actava 156 Pseudamussium similis 191 Pseudastralium henicus gloriosum 132, 135 pseudoargus, Archidoris 216, 246, 281, 282 Pseudocardium sachalinense 191 Pseudodaphnella 84 tincta 83 Pseudoliotina 188 Pseudomelatoma penicillata 4, 5, 10, 28 Pseudomelatominae 4, 5, 28 Pseudomiltha floridana 173, 191 Pterioidea 164 Pteropoda 224 Pteropurpura 132, 137 vespertilio 137 Pterynotus 189 Ptychodera flava 10 pudica, Tellina 192 pulchella, Chromodoris 247, 260-261 pulchella, Tellina 192 pulcher, Conus 36, 46, 47, 52 pulcherrissima, Ancistrosyrinx 132, 140 pulchra, Embletonia 247, 297 pulchra, Rostanga 242, 246, 283 pulicarius, Conus 41, 53 347 Pulmonata 157, 308-310, 316 pulvinata, Glycymeris 191 pumila, Kermia 83 punctata, Aplysia 225, 226, 227, 229, 230, 296 punctata, Bulla 228 punctatus, Notarchus 296 punctilucens, Aegires 246 punctocaelatus, Rictaxis 314 punctostriatus, Scaphander 314, 322 punctulata, Bulla 225, 227, 229, 230 Pupa 314, 317, 325 nitidula 314 pura, Aegopinella 162 purpurascens, Conus 41, 52 purpurea, Chromodoris 233, 234, 236, 237 pusae, Discodoris 238 pusilla, Natica 165 Pusionella 20, 132 Pustularia cicercula 136 margarita tetsuakii 132, 136 Pustularia (Pustularia) globulus 136 pustulata, Cuthona 245 pygmaeus, Nassarius 189 pyramidata, Euclio 225 yramidella 227, 230 digitalis 190 plicosa 190 terebelloides 225, 227-230 Pyramidellacea 224, 226 Pyramidellidae 223, 224 Pyramidelloidea 197, 198 Pyramidellomorpha 309 Pyrgulina interstincta 190 pyriformis, Coralliophila 132, 137-138 quadrangularis, Entalina 141 quadrata, Blackdownea 189 quadrata, Philine 315, 321, 323 quadricolor, Chromodoris 260-261 quadrilineata, Polycera 242, 244, 246, 293, 296, 297 Quidnipagus palatam 192 Rachiglossa 17 radians, Chlamys 191 radiatus, Helicocryptus 188 radiatus, Turbo 260-261 radula, Coralliophila 138 ramosa, Genota 190 ramosus, Chicoreus 259-261, 263, 264, 268 ranunculus, Conus 53 Raphitoma 70 hispidula 190 rarispina, Doriopsilla 293 rattus, Conus 40, 52 rectilabrum, Euspira 167 recurvus, Conus 52 regiscorona, Aglaja 315 regius, Conus 53 regularis, Conus 41, 52 regularis, Мезайа 189 remondii, Conus 59 restitutiana, Nassa 189 restitutus, Conus 59 348 INDEX reticulata, Chromodoris 242 reticulate, Periglypta 192 reticulatum, Bittium 189 reticulatum, Deroceras 89-106 retroversa, Limacina 316 Retusa 226, 295, 316, 322 kelloggi 190 obtusa 227, 268, 315, 317, 318, 322, 324 operculata 318, 322, 324 perstriata 295 semisulcata 293, 295 truncatula 190, 293-295, 317 umbilicata 295 Retusidae 224, 315, 317, 318, 324 reussi, Acteon 190 reversa, Modiolus 190 Rhinoclavis 189 Rhinoclavis 189 Rhodope 207, 308, 309 crucispiculata 311 marcusi 301, 308, 310 transtrosa 301, 302-304, 308, 310 veranii 301-302, 302, 307-310 Rhodopemorpha 310 Rhodopidae 205, 301-311 richardi, Mamillocylichna 314 Rictaxis 318, 325 punctocaelatus 314 rigidus, Iscafusus 189 imella fissurella 189 Ringicula 322, 324 auriculata 190, 295 buccinea 190, 319 conformis 295, 319 nitida 314, 319 Ringiculidae 314, 319-321, 324, 325 Ringiculoidea 310 Ringiculoides 322, 324 Rissoa inconspicula 188 Rissoella 169, 189 Rissoina podolica 188 robusta, Arcopagia 192 robustum, Dinocardium 191 rosea, Doto 248 roseoapicalis, Euhadra 132, 140 roseoapicalis, Euhadra brandtii 140 rosi, Discodoris 249 Rostanga 213, 216 pulchra 242, 246, 283 rouaulti, Conus 60 Roxania utriculus 315 rubicunda, Halgerda 246 rubignosum, Cylichna 190 rubra, Aeolidiella 297 rubra, Stomatia 134 rubrum, Gastropteron 317 Ruditapes philippinarum 174, 175, 192 rufa, Tubonilla 190 Rugobela 190 rugosa, Corbula 192 rugosum, Cirsotrema (Elegantiscala) 136 Runcina 319 Runcinidae 317, 318, 322 Rutitrigonia eccentrica 191 sachalinense, Pseudocardium 191 Sacoglossa 205, 209, 224, 308-310, 313, 317, 318, 322-325 salleana, Hastula 20, 28, 30, 31 salmonacea, Coryphella 249, 281, 282, 286 Sandbergeria perpusilla 189 sandiegensis, Diaulula 242, 246 Sandria atava 156 sanguinea, Aeolidiella 247 sanguineus, Hexabranchus 242, 246, 257, 259-261, 262, 263, 265, 266, 269 sanguineus, Spondylus 134 Sapha 317 savignyi, Bursatella leachii 296 savignyi, Thais 260-261, 263, 269 Saxidomus giganteus 174, 192 scabra, Philine 295 scabra, Platydoris 246, 260-261, 263 Scabricola 139, 189 scabricosta, Nerita 188 scabriusculus, Conus 40, 52 scabrum, Parvicardium 191 scalarina, Katelysia 192 scalaris, Conus 52 Scaphander 190, 309, 317, 319, 322 racilis 314 ignarius 225, 227, 229, 314, 322 mundus 314, 322 nobilis 314, 322 punctostriatus 314, 322 Scaphandridae 224, 314, 318, 322 schencki, Acila divaricata 132, 141-142 schiosensis, Trochactaeon 58 Scissulina 192 Scissurellidae 201 Scissurelloidea 202 scitulus, Conus 52 Scrobicularia plana 192 Sebadoris crosslandi 246, 259-261 Seguenzioidea 198 Semicassis persimilis 132, 136-137 wannoensis 189 semicostatus, Conus 57, 59 semilaevis, "Bulla" 314, 318, 319 semistriatus, Acteon 190 semistriatus, Donax 170, 192 semistriatus, Nassarius 189 semisulcata, Retusa 293, 295 senegalensis, Venerupis 192 senessei, Conus 57, 58 sericata, Gaza 132, 135 Serpulorbis imbricatus 134 serradifalci, Lobiger 296 serrata, Bonellitia 190 serricostatum, Cardium (Trachycardium) 142-143 "serricostatum, Vasticardium" [пот. nud.] 132, 142-143 serrulata, Venericardia 191 sibogae, Glossodoris 249, 264 sibogae, Phestilla 242, 280, 281, 283, 286 Siliquaria cumingi 134 similis, Pseudamussium 191 Simnia xanthochila 132, 136 simplex, "Bulla" 314 simplex, Conus 52 INDEX sinicum, Umbraculum 316 sinuatus, Surculites 59 Sinum 168, 171 Sipho curtus 165 Siphonalia 189 Siphonaria 310 Siphonopteron citrinum 317 michaeli 315 Smaragdinella 321, 322 Smaragdinellidae 310 Smeagol manneringi 308 Solecurtus antiquatus 192 dunkeri 132, 143 Solemyidae 164 Solen 173 conradi 192 Strictus 192 Soleolifera 308 solida, Hastula 20 solida, Nuttallia 132, 143 solidissima, Spisula 191 solitaria, Haminoea 315 soluta, Akera 228, 230 souleyeti, Protatianta 108, 109-111, 112, 1137115128 sowerbyanus, Clython 134 speciosa, Philinopsis 315 spectabilis, Duplicaria 20, 24, 25-27, 28, 32 sphaeiferus, Piseinotecus 248 spinifera, Lucina 191 spinosa, Epitonium 189 spirata, Archimediella 189 Spisula 161, 170 elliptica 163, 191 solidissima 191 subtruncata 163, 191 Splendrilla 16 chathamensis 6, 7, 7 Splendrillia vellai 190 Spondylus 133 cruentus 134 sanguineus 134 Bong Trippa 249, 260-261, 266, 267, sponsalis, Conus 40 Spurilla 245, 324 japonica 248 neapolitana 248, 293, 294, 297 spurius, Conus 53 spurius, Turricula nelliae 8, 10, 14 squalida, Megapitaria 192 squamosa, Anomalocardia 192 squamosa, Tridacna 134 staminea, Protothaca 192 stauberi, Lomanotus 248 steinbergae, Doridella 246, 281, 282 stellilfera, Anisodoris 238 stercomuscarum, Conus 52 stercusmuscarum, Natica 177 stimpsoni, Coryphella 282 Stomatia rubra 134 Stomatiidae 134 Streptoneura 197, 309 striata, Atactodea 191 striata, Bulla 228, 230, 292-295, 315 349 striata, Eriphyla 191 striata, Hyalocylis 225 striatellus, Conus 52 striatula, Chamelea 176 striatula, Venus 176, 192 striatus, Conus 41, 53 Stricispira paxillus 10 Strictispirinae 10 strictus, Solen 192 Strigilata, Palaeonucula 190 Strigillata, Hastula 30 Striolata, Mangelia 71 Strioterebrum 30 monidum 173, 190 pliocenicum 190 Strombiformis glaber 189 Strombus 133, 189 fasciatus 260-261 gibberulus 260-261 tricornis 257, 258, 258, 260-261, 263, 268 strongi, Haminoea 315 stultorum, Mactra 191 Styiola 225 Stylocheilus 317 suavis, Turrancilla 139 subangulata, Turritella 189 Subcancilla 189 subcylindricata, Cythara 190 sublaevis, Aegires 246 sublaevis, Glycymerita 191 submirabilis, Acila divaricata 142 subplicatus, Circomphalus 192 subquadrata, Diplodonta 191 subramosus, Dendronotus 248 subroboratum, Placamen 192 subrotunda, Calva 192 subrugosa, Chione 192 subtenta, Cyclocardia 191 subtruncata, Epicyprina 192 subtruncata, Spisula 163, 191 subulata, Eulima 189 subulata, Terebra 20, 23, 24, 28, 29, 30, 3132033 succinea, Terebra 28, 29 sudanica, Noumea 244 sugashimae, Goniodoris 246 Sulcerata 133 Sunetta concinna 134 gibberula 192 Surculites sinuatus 59 Sydaphera wannonensis 190 symbolicum, Campanile 201 taeniata, Mangiliella 71 taeniatus, Conus 40, 53 Tagelus peruvianus 192 tajimae, Limopsis 132, 142 tangituensis, Falsicolus 189 Tapes japonica 192 philippinarum 192 tara, Aldisa 246 Taranis 10 Taringa telopia 246 taurinus, Terebra 29 taylori, Phyllaplysia 268 350 INDEX tecta, Natica 176 Tectibranchia 309 Tellina 192 donacina 192 emacerata 192 lux 192 planata 192 pudica 192 pulchella 192 tenius 175, 192 Tellinella virgata 192 Tellinidae 166 tellinoides, Lirodiscus 167, 191 telopia, Taringa 246 tema, Discodoris 238 tema, Hypselodoris 244 Temnoconcha cognata 192 Tenellia 281 adspersa 245, 297 fuscata 245 pallida 245, 283, 284 tenerum, Parvamplustrum 314 tenius, Tellina 175, 192 terebelloides, Pyramidella 225, 227-230 Terebra 190 affinis 20, 23, 24, 27, 28, 30, 32, 33 anilis 28 areolata 30 babylonia 20, 21, 28, 29, 29, 31 capensis 20, 33 cerithina 20 cingulifera 30 crenulata 30, 33 dimidiata 20, 30, 32, 33 dislocata 190 fictilis 33 funiculata 20, 29, 31 gouldi 23, 25, 30, 32, 33 uttata 28, 29, 31 ectica 20, 21 imitatrix 21, 23, 27, 28, 30, 31, 33 kieneri 33 maculata 20, 23, 25, 32 nassoides 20, 24, 25, 27, 28, 30, 33 protexta 29 subulata 20, 23, 24, 28, 29, 30, 31, 32, 33 succinea 28, 29 taurinus 29 textilis 30 tristis 20, 24-25, 28 Terebridae 3, 9, 19-34, 72 Terefundus lamelliferus 189 Teretiopsis 9 abyssalis 9 Tergipedidae 321, 325 Tergipes tergipes 297 tergipes, Tergipes 297 tessulatus, Conus 53 Tethys leporina 310 tetsuakii, Pustularia margarita 132, 136 textile, Conus 41, 52 textilis, Terebra 30 Thais savignyi 260-261, 263, 269 Thecacera 213 Thecosomata 230, 309, 316-318 Theodoxus luteofasciatus 188 Thestyleda 132, 142 Thestyleda 132, 142 Thetis laevigata 191 thisphila, Anadara 191 Thordisa filix 246 Thorunna africana 244 furtiva 244 thraciaeformis, Yoldia 190 thysanophora, Eledone 152 lara 140 yagurai 140 tiaratus, Conus 40, 52 Tiariturris libya 28 tiarula, Nassarius 189 Tibia fusus 134 unidigitata 189 timida, Elysia 293, 296 Timoclea marica 192 tincta, Pseudodaphnella 83 tinctoria, Chromodoris 247, 260-261, 268 Tivela 192 tokiokai, Atlanta 107, 109, 110, 114, 115, 117, 126, 127, 128, 129 Toledonia 317, 325 tomentosa, Jorunna 246 tomlini, Erosaria 132, 136 Tomopleura 190 Tonna olearium 259, 260-261 Tonnoidea 202 Tornatellaea affinis 190 unisulcata 190 tornatilis, Acteon 190, 225, 227-230, 295 Tornatina heraclitica 190 trunculata 190 tornatus, Conus 36, 42, 44, 45, 52 Toxiclionella elstoni 14 tumida 8, 8, 10, 14 Toxoglossa 1-202 trabeatoides, Michela 190 Trachycardium 142-143 transtrosa, Rhodope 301, 302-304, 308, 310 Trapania 213, 214 maculata 244 trapezium, Pleuroploca 258, 259, 260-261, 263, 269 traski, Acteon 320 Tresus 173 nuttallii 191 triangularis, Astarte 191 tricarinata, Turritella 189 trichodes, Microdaphne 82 tricolor, Eubranchus 242 tricolor, pipe mare 233, 236, 238 tricolor, Mexichromis 243, 244, 249 tricolorata, Aglaja 315 tricornis, Strombus 257, 258, 258, 260-261, 263, 268 Tridacna squamosa 134 Tridacnoidea 164 tridentata, Cavolinia 225, 227, 228, 230, 316 Triforis 72 trigona, Pelecyora 170, 192 тега, Coryphella 247 INDEX Triopha carpenteri 242 catelinae 246 Triphora perversa 189 Triphoridae 11, 73 Trippa areolata 246, 260-261 spongiosa 249, 260-261, 266, 267, 268 trispinosa, Diacria 225 tristis, Pervicacia 20, 24, 30 tristis, Terebra 20, 24-25, 28 Tritonia cincta 248 diomedea 248, 281, 283, 285 hombergi 248, 281, 283, 285 plebeia 248 Tritonoturris 84 amabilis 83 trivittatus, Nassarius 177, 189 Trochactaeon schiosensis 58 Trochus dentatus 260-261 erythraeus 260-261 Trophon 72 truncata, Corbula 192 truncata, Lambis 260-261, 264, 268, 269 truncatula, Retusa 190, 293-295, 317 trunculata, Tornatina 190 trunculus, Donax 170, 192 Tryblidiida 197 tubercularis, Cerithiopsis 189 tuberculata, Acanthocardia 191 tuberculata, Fusinus 259, 260-261, 263, 268 tuberculatus, Conus 57 tuberculatus, Gosvia 58 Tubonilla rufa 190 zesulcata 190 tubulosa, Cylichna 317 Tugali gigas 134 tulıpa, Conus 52 tumida, Toxiclionella 8, 8, 10, 14 tumidus, Polinices 163 tura, Mexichromis 244 Turbo 188 radiatus 260-261 turgida, Nucula 190 Turrancilla apicalis 132, 139 suavis 139 Turricula africana 190 dimidiata 190 nelliae 8, 10, 14 nelliae spurius 8, 10, 14 turriculata, Atlanta 107, 109, 110, 114, 115, 117, 122, 123, 124, 129 Turriculinae 6 Turridae 1, 3, 20, 29, 55-57, 65, 69-87, 166, 177 Turridrupa 80, 83 albofasciata 83 Turrinae 80-85 Turris 83, 85 Turritella 178, 189 badensis 189 bieniaszi 189 granulata 189 subangulata 189 tricarinata 189 Turritellidae 166 Tylodina 317 351 citrina 227 fungina 316 uchidai, Clinocardium 132, 142 ulla, Ascobulla 316 umbilicata, Retusa 295 umbonata, Glycymerita 191 Umbonium vestiarium 170, 188 Umbraculacea 325 Umbraculidae 224, 316, 317, 324 Umbraculomorpha 308, 309 Umbraculum 226, 227, 317 mediterraneum 227, 228, 230 sinicum 316 uncinata, Hancockia 248, 325 undata, Micromelo 314 undatella, Chione 192 undaurum, Glossodoris 244 unidigitata, Tibia 189 unimaculata, Imaclava 14 Unio 158 unisulcata, Tornatellaea 190 unsa, Aglaja 315 urasima, Baryspira 132, 134, 139 Uromitra 139 Urosalpinx 189; borehole 158 cinerea 156 ustulata, Pervicacia 33 utriculus, Roxania 315 uttingerianus, Aporrhais 189 vadosa, Crassatella 191 valenciennesi, ee 244 Valvatoidea 19 Vanikoropsis albus 189 varia, Gibbula 188 variabile, Cerithium 189 Varicorbula 172 amekiensis 192 varicosa, Phyllidia 242, 246, 260-261 varicosum, Cirsotrema (Elegantiscala) 136 varius, Conus 52 Vasticardium 143 compunctum 132, 142 okinawaense 142, 143 "Vasticardium serricostatum" [nom. nud.] 132, 142-143 vauquelini, Mangelia 71 Vayssiereidae 157 Vayssieria caledonica 249 vellai, Splendrillia 190 Venericardia greggiana 191 serrulata 191 Veneridae 166 Venerupis aurea 192 irus 143 senegalensis 192 Venilicardia lineolata 192 Ventricolaria fordi 160 ventricosus, Conus 41, 52 venulatus, Conus 52 venulosa, Peronidia 192 Venus multilamella 192 striatula 176, 192 verrucosa 192 veranii, Rhodope 301-302, 302, 307-310 352 INDEX Veremolpa micra 192 verneuilli, Acteon 58 verneuilli, Conus 57 Veronicella 310 verrucicornis, Berghia 247, 297 verrucosa, Coryphella 247 verrucosa, Doris 293, 296, 297 verrucosa, Venus 192 vesicula, Haminoea 315 vespertilio, Ceratostoma (Pteropurpura) 132: 137 vespertilio, Pteropurpura 137 vestiarium, Umbonium 170, 188 vestita, OR eris 191 Vetericordiella 191 Vetigastropoda 198 Vexillum 190 Vexillum (Uromitra) 139 vexillum, Comptopallium 158 vexillum, Conus 40, 52 viapollentia, Zeacuminia 190 victor, Conus 52 victoriae, Conus 52 vidua, Conus 52 villafranca, Hypselodoris 235, 238, 244, 249, 293, 296 virescens, Haminoea 315 virgata, Tellinella 192 virgatus, Conus 36, 39, 45, 50, 52 virginalis, Platyschides 141 virginea, Neritina 188 virgineus, Chicoreus 259, 260-261, 262, 268 virginica, Crassostrea 158 virgo, Conus 41 viridis, Doriopsis 246 viridis, Elysia 296 viridis, Placida 296 Viridoturris powelli 190 vittatus, Conus 52 vittatus, Donax 192 Viviparus 158 Vokesula aldrichi 192 Volutidae 57, 72 Volutopsius norwegicus 259 Volvatella 209, 316 Volvulella 322 cylindrica 315 vulgatum, Cerithium 189 vulpecula, Bela 190 Wallucina 191 wannoensis, Semicassis 189 wannonensis, Sydaphera 190 webbi, Hypselodoris 244 wellmani, Exilla 189 willani, Cadlina 244 willcoxi, Aplysia 228, 230 williamsi, Mysidioptera 191 Xandarovula 136 xanthochila, Simnia 132, 136 xeniae, Phyllodesmium 248, 260-261, 263, 264, 266, 269 Xenophora 164 corrugata 134 Xenophoridae 164 Xenuroturris cingulifera 83 kingae 83 ximenes, Conus 45, 52 yagurai, Mitra (Cancilla) 132, 140 yagurai, Mitra (Tiara) 140 yagurai, Tiara 140 yokohamensis, Cantharidus 135 yokoyamai, Papyriscala 135 Yoldia 190 thraciaeformis 190 yongei, Doto 248 Zeacuminia viapollentia 190 zesulcata, Tubonilla 190 Zeuxis 132, 139 kiiensis 139 zonata, Hydatina 225, 227, 229, 230, 314 zonatus, Conus 41, 52 Zonitidae 157 WHY NOT SUBSCRIBE TO MALACOLOGIA? 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Address inquiries to the Subscription Office. x a Horno à and 3 Food à ln the Dora nar eee. amade eve Г Г. i ny 1508, A Nucbranch Adapted for Lite in a | .. if ah POULICEK, MARIE: FRANCOISE voss- FOUCART a q. CHARLES, JEUNIAUX a We Regressive Shell Evolution Among Opisthobranch RER VE PR ate Be с. ¡GARCIA GÓMEZ, ANTONIO MEDINA & RAFAEL COVEÑAS TER NR Study of the Anatomy and Histology of the Mantle Dermal. Formations de ART _ (МОР) of REN se elisa ts ao И | 5e KO va _ Chromodorididae) .. O E И. da | MALCOLM EDMUNDS | Does Warning Coloration Occur in Nudibranchs? | NS Ак. y | GAMIL N. SOLIMAN - al ES JA Caio Review of the Spawning, Re a FR Metamorphosis of Prosobranch and Opisthobranch Gastropods with fe A, _ Special Reference to Those from the Noriiwestem Red.Sea......., _ CHRISTOPOHER D. TODD. ; UL. Larval aber Bis of vik iy si da at Similar Nan to the _ Same End? .. 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