Joseph Heller a Natural History Illustrator: Tuvia Kurz

Joseph Heller

Sea Snails A natural history Illustrator: Tuvia Kurz Sea Snails

Joseph Heller

Sea Snails A natural history

Illustrator: Tuvia Kurz Joseph Heller Evolution, Systematics and Ecology The Hebrew University of Jerusalem Jerusalem , Israel

ISBN 978-3-319-15451-0 ISBN 978-3-319-15452-7 (eBook) DOI 10.1007/978-3-319-15452-7

Library of Congress Control Number: 2015941284

Springer Cham Heidelberg New York Dordrecht London © Springer International Publishing Switzerland 2015 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifi cally the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfi lms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specifi c statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made.

Printed on acid-free paper

Springer International Publishing AG Switzerland is part of Springer Science+Business Media (www.springer.com) Contents

Part I A Background 1 What Is a Mollusc? ...... 3 Bibliography ...... 10 2 What Is a Snail? ...... 11 2.1 Defence: Shell and Operculum ...... 12 2.2 Attachment and Locomotion ...... 17 2.3 Respiration ...... 19 2.4 Feeding ...... 23 2.5 Reproduction and Embryonic Development ...... 26 2.6 Metamorphosis to Adult Form ...... 30 2.7 General Classiﬁ cation ...... 31 Bibliography ...... 33

Part II Primitive Sea Snails 3 Patellogastropoda: Limpets ...... 37 3.1 Holding on, Moving About and Resisting Desiccation ...... 40 3.2 Respiration ...... 43 3.3 Feeding ...... 44 3.4 Reproduction ...... 50 3.5 Predation and Competition ...... 50 3.6 Evolutionary Aspects and Classiﬁ cation ...... 52 Bibliography ...... 53 4 Vetigastropda: Brush Snails ...... 55 4.1 Functional Morphology in Evolutionary Perspective ...... 55 4.2 Fissurelloidea: Keyhole Limpets, Slit Limpets and Relatives ...... 61

v vi Contents

4.3 Lepetodriloidea and Neomphaloidea: Deep-Sea Brush-Snails ...... 63 4.4 Pleurotomarioidea: Slit-Whorls ...... 65 4.5 Haliotoidea: Abalones ...... 66 4.6 Trochoidea: Top Shells, Turbans and Allies ...... 68 Bibliography ...... 77 5 Neritimorpha: Nerites ...... 79 5.1 Sea-Dwelling Nerites ...... 81 5.2 Out of the Sea ...... 83 Bibliography ...... 85

Part III Advanced Sea Snails 6 Functional Morphology: An Evolutionary Perspective ...... 89 6.1 Reproductive System ...... 90 6.2 Embryonic Development ...... 93 6.3 Shell Structure ...... 94 6.4 Feeding ...... 95 6.5 Breathing ...... 96 6.6 Classiﬁ cation ...... 96 Bibliography ...... 98 7 Grazers and Filter Feeders ...... 99 7.1 Cerithioidea: Creepers, Ceriths and Cracked-Pipes ...... 99 7.2 Vermetoidea: Worm Snails ...... 104 7.3 Stromboidea: Pelican’s-Foots, Conchs and Relatives ...... 108 7.4 Calyptraeoidea: Cup-and-Saucers, Bonnets and Slippers ...... 116 7.5 Gill Filter Feeding: General Comments ...... 122 7.6 Littorinoidea: Winkles, Periwinkles and Their Allies ...... 125 7.6.1 Feeding ...... 133 7.6.2 Reproduction ...... 134 7.7 Cypraeoidea: Cowries, False-Cowries, Smallips and Relatives ...... 138 7.7.1 Mantle Flaps ...... 140 7.7.2 Breathing and Feeding ...... 141 7.7.3 Reproduction ...... 142 7.7.4 Cowry Predators ...... 143 7.7.5 Ovulidae, False Cowries ...... 144 7.7.6 Triviidae, Smallips ...... 145 Bibliography ...... 146 8 Predators ...... 149 8.1 Predator Functional Morphology from an Evolutionary Perspective ...... 149 8.2 Tonnoidea: Tuns, Helmet Shells and Trumpets ...... 154 8.3 Naticoidea: Moon Shells ...... 159 Contents vii

8.4 Heteropoda: Hoverers ...... 161 8.5 Epitonioidea: Wentletraps and Violet Shells ...... 164 8.5.1 Epitoniidae, Wentletraps ...... 164 8.5.2 Janthinidae, Violet Shells ...... 166 8.6 Eulimoidea: Parasitic Snails ...... 169 8.7 Buccinoidea: Whelks and Nutmegs ...... 174 8.8 Muricoidea: Murexes ...... 181 8.9 Conoidea: Turrids, Cones and Augers ...... 191 8.9.1 Terebridae, Augers ...... 197 Bibliography ...... 198

Part IV Away from the Basic Lifestyle 9 Shell Degeneration: Sea Slugs and Relatives ...... 203 9.1 Functional Morphology from an Evolutionary Perspective ...... 204 9.1.1 Life Cycles ...... 208 9.2 Cephalaspidea: Shield Slugs and Bubble Shells ...... 209 9.3 Anaspidea: Sea Hares ...... 215 9.3.1 Feeding ...... 216 9.3.2 Life Cycle ...... 218 9.3.3 Movement ...... 220 9.4 Thecosomata: Sea Butterﬂ ies ...... 222 9.5 Gymnosomata: Sea Angels ...... 225 9.6 Sacoglossa: Leaﬂ ets ...... 228 9.6.1 Feeding and Photosynthesising ...... 229 9.6.2 Reproduction ...... 232 9.6.3 Defence ...... 235 9.7 Pleurobrancha: Side-Gills ...... 236 9.8 Nudibranchia: Nudibranchs ...... 237 9.8.1 Anthobranchia: Dorids ...... 237 9.8.2 Aeolidina: Aeolids ...... 242 9.8.3 Dendronotina: Dendronotoids ...... 249 Bibliography ...... 252 10 Marine Ancestors of most Land Snails: Pulmonates ...... 257 10.1 Siphonarioidea, False Limpets ...... 259 10.2 Other Primitive Pulmonates ...... 261 Bibliography ...... 264

Part V Man-Snail Links 11 Magic, Status and Money ...... 267 11.1 Cowries ...... 268 11.2 Chank ...... 277 Bibliography ...... 283 viii Contents

12 In Palaces and Shrines: Purple and Blue and Shekhelet ...... 285 12.1 Purple ...... 286 12.2 Blue ...... 300 12.3 Shekhelet ...... 303 Bibliography ...... 305 13 Sacred Sounds from Sea Shells ...... 307 Bibliography ...... 317 14 Sexual Perversions ...... 319 Bibliography ...... 322

Glossary ...... 323

Index ...... 329

Subject Index 1: Defence ...... 341

Subject Index 2: Movement and Attachment ...... 343

Subject Index 3: Food and Feeding ...... 347

Subject Index 4: Reproduction ...... 351 About the Book

Abstract Shells are beautiful and sea snails – which build shells and dwell inside them – are spellbinding. This book presents the diversity and natural history of sea snail groups. By integrating aspects of morphology, ecology, evolution and behaviour, it describes how each group copes with problems of defence, locomotion, respiration, feeding, mating and embryonic development. Two chapters briefl y sketch general characteristics of the Mollusca, to which snails belong, and present characters by which snails (Gastropoda) differ from other molluscs. Three chapters present the primitive, predominantly grazing, sea snails: limpets (Patellogastropoda), brush snails (Vetigastropoda: top-shells, turbans and allies) and nerites (Neritimorpha), a small group with remarkably high variation in shell colour and in habitats, even in trees. Three chapters are devoted to advanced- snails (Caenogastropoda): the changes they underwent, the grazers and fi lter- feeders, and the many voracious predators, some which use venomous darts. Two chapters present groups with different life styles: sea slugs (Opisthobranchia), which have shifted from mechanical to chemical defence; some are herbivores and use their food to harness solar energy, others are predators that gain stinging cells and poisonous compounds from their food. Pulmonate ancestors have adapted to breathing fresh air, crawled out of the sea and have conquered land. The ending chapters present chosen aspects of sea snails in human culture: as sacred artefacts and objects of magic and money; as a source of the royal and sacred dyes of purple and blue; and as holy ceremonial trumpets; fi nally, I describe some damaging effects of pollution on sea snail sex.

Keywords Gastropod behaviour • Gastropod defence • Gastropod ecology • Gastropod embryonic development • Gastropod evolution • Gastropod feeding • Gastropod locomotion • Gastropod functional morphology • Gastropod respiration • Gastropod reproduction

Shells are beautiful. They are such an endlessly rich variety of fascinating shapes and textures and colours that capture our hearts; they are so beautiful that it is hard to stroll along the seashore without being tempted to pick up and collect every

ix x About the Book

single one. And the snails – those animals which build the shells and which dwell inside them – are ten times more spellbinding. Along the shore and in the sea itself there are, besides algae-grazing snails, also those that cast out huge nets to capture tiny creatures from the plankton and others that stab venom-loaded daggers into the bodies of fi shes. There are, besides those that defend themselves by retreating into the depths of a calcareous fort and those that mount stones into their shells like gems onto a ring, also others that defend themselves with a battery of toxic poisons, and others that can shed their tail and crawl away in moments of danger. There are, besides those that crawl leisurely over rocks on the sea fl oor, others that hover in the water column, and yet others that build tiny rafts to carry them over the waves. Furthermore, there are, along the seashores, those snails that have succeeded in harnessing the energy of the sun for their own use and others that glide over the sand with a foot swollen with seawater. It is the story of these sea snails that I wish to tell in this book. Several by-now classic books treat various aspects of the biology of sea snails. British Prosobranch Molluscs (Graham and Fretter 1962) is the most important comprehensive and detailed book written over the last century on the functional morphology and general ecology of any major group of sea snails. It is complemented by Biology of Opisthobranchs volumes I and II (Thompson 1976; Thompson and Brown 1984) and, at a more popular level, by Living Marine Molluscs (Yonge and Thompson 1976). Since these classic books and during the last four or fi ve decades, sea snail study has advanced so considerably and in so many aspects – classifi cation, functional morphology, reproductive biology, molecular biology, behaviour, and ecology – that the time seems ripe for a new book. This book is written with two main readerships in mind. First and foremost, it is for the general biologist (perhaps the general marine biologist), who seeks general knowledge about sea snails. As such it is for the biology teacher, the fi eld-school instructor, the interested pupil and the attracted amateur and keen naturalist. It is for this readership that the book is broad in scope and contains the more abundant snail groups, those one is likely to stumble across while strolling along the shore, while diving into the sea or diving into the literature; and it is for these readers that I have also made every attempt, throughout the book, to avoid heavy terminology and needless technical descriptions. That is why in this book they are called ‘sea snails’ and not ‘marine gastropods’ and that is also why, wherever possible, scientifi c names are accompanied by common or vernacular names. These common names are mostly gleaned from the literature, but in those cases in which a vernacular name was lacking (or existing but not very suitable) I took the liberty of coining a name of my own. I have attempted to form attractive names that are meaningful, in that they give some information about the snail, whether by describing a unique morphology, habitat or behaviour. I have avoided automatic translations or translit- erations of scientifi c names. To avoid word-trains, where possible, I have also avoided the broad term ‘snail’. Then, the book is also for advanced students making their fi rst steps into the research of sea snails and who, while delving into one rather limited topic, feel they would like to compliment their focal interest by gaining a broader perspective, a About the Book xi panoramic view of the group as a whole and of major evolutionary trends within it. It is for this reader that the book refers, besides to abundant snail groups, also to some rarely encountered groups such as those of the deep sea, and those found only inside the body of other organisms. For this reader the book contains also a few strokes of functional sea snail morphology, seen mainly from an evolutionary perspective. Some 40,000 snail species have been recorded from the seas of the world. I will concentrate on the natural history of the major groups, the better known but also some rare ones, in an approach which hopes to integrate various aspects of snail morphology, anatomy, ecology, evolution and behaviour. I present the manner in which each group, along its unique evolutionary path, copes with problems of survival, of movement, of feeding and of reproduction. The fi rst part of the book presents general background information about snails. Snails belong to a larger group of animals, the Mollusca, and the fi rst two chapters briefl y sketch out the general characteristics of this group, and present characters by which snails differ from other members of the molluscs. They deal with snails’ basic functional morphology in terms of how snails cope with problems of defence, locomotion, respiration, feeding, mating, and embryonic metamorphosis from larva to adult form. The second part (Chaps. 3 , 4 and 5 ) presents primitive, predominantly grazing, sea snails. This includes limpets, which cling to wave-beaten intertidal rocks into which they excavate home scars, vigorously defended from competitors. Equipped with strong iron-coated teeth, some limpets feed on algal gardens to which they tend and which they regularly crop. It also considers the vetigastropods, which include top shells, turbans, abalones and their allies. Their brush-shaped teeth enable the sweeping of soft food, and their shells are usually spirally coiled. Some dwell in the deep sea, others in shallow waters. Finally, the nerites are presented, a small group with remarkably high variation in shell colour and found in both shallow and deep seas, freshwaters, and even terrestrial trees. The third part (Chaps. 6 , 7 and 8 ) is devoted to the advanced-snails (caenogastro- pods), both herbivores and predators. It presents general differences (mainly in reproduction) between primitive and advanced-snails and deals with those advanced snails that feed by grazing or fi ltering minute particles from the surrounding sea. These include the pelican’s-foot which buries into soft sediment, the sponge-buried cracked-pipe, the rock-cemented worm-snails, as well as the leaping conchs, the winkles and the cowries. Most advanced snails are voracious predators and this part describes mechanisms which enable these slow animals to prey on various other animals. Predatory snails include the trumpet shell, moon shell, triton, violet shell, harp shell, murex, dog-whelk, and cone. The fourth part (Chaps. 9 and 10 ) is about two groups of sea snails that have abandoned the traditional life style, each in its unique way. First, it explores how sea slugs and their relatives (classically named Opisthobranchia) abandoned the mechanical defence strategy of a thick shell and shifted to chemical defence mechanisms. Some are herbivorous and use their food to harness solar energy; others are predators and gain stinging cells and poisonous compounds from their food. Then, xii About the Book this part also briefl y surveys the ancestors of one group of shelled sea snails, the pulmonates, which crawled out of the sea, adapted to breathing fresh air, and then conquered land. Snail-Man links, the subject of the last part of the book (Chaps. 11 , 12 , 13 and 14 ), presents chosen aspects of sea snails in human culture: as sacred artefacts and objects of magic and money, as a source of the royal and sacred dyes of purple and blue, and as holy trumpets. It also describes one of the (many) damaging effects of pollution on the sex of sea snails. To enhance fl uent reading I have adopted textbook rather than scientifi c style, and accordingly the text does not cite references every few sentences. When referring to species, their general range is given but higher ranks often range so very widely that a reference to their distribution seems pointless, in this general book. The book is as rich in illustrations as it could go, but not fully comprehensive and not representing every single group of snails in every sea. Readers are encouraged to also venture onto the internet in search of sites with colour photos of sea snails – they are easy to fi nd and invaluable as a means of visualising the stunning beauty of the many diverse groups of sea snails. This book could not have been written without the noble help of my brother Michael Hallel. He read the manuscript time and again and offered numerous suggestions, criticisms and emendations; his insights and questions led me to recast much of the book. A picture is worth a thousand words. I am enormously grateful to my longstand- ing partner Tuvia Kurz, whose 230 extraordinarily beautiful illustrations fl ood the book with light. I owe a great debt to my long-time research assistant and teammate Naomi Sivan for her enthusiastic cooperation and critical attention in brushing up the book, and in designing the graphics of the illustrations. My friend and colleague Dr. Nathalie Yonow has very kindly read several successive drafts of the entire manuscript and made many perceptive suggestions, helpful comments and corrections. Warm thanks to Hava Nowerstern of the National Library of Israel for helping me fi nd many sources of centuries-old books, for translating ancient Latin and Spanish texts and for granting me permission to publish texts and fi gures from books in the Edelstein Collection. My friend Tzameret Avivi generously painstakingly drew up the index; she also carried out a close reading. Sincere thanks to my publishers at Springer and particularly to Alexandrine Cheronet and Judith Terpos, for their editorial guidance and production skills. For her love, support, and affection I dedicate this book to Chava.

Joseph Heller About the Book xiii

Bibliography

Fretter V, Graham A (1962) British prosobranch molluscs. Ray Society, London Thompson TE (1976) Biology of opisthobranch molluscs, vol 1. Ray Society, London Thompson TE, Brown GH (1984) Biology of opisthobranch molluscs, vol 2. Ray Society, London Yonge CM, Thompson TE (1976) Living marine molluscs. Collins, London Part I A Background Chapter 1 What Is a Mollusc?

Abstract Molluscs differ from other animals in fi ve major aspects: (a) Two types of basic symmetry are involved in their body structure: a bilateral one as in groups moving about in active pursuit for food; and a radial one, as typical of sessile animals. (b) A protective calcareous external skeleton, the shell, is secreted from the back. (c) A rasping tongue (radula) in the mouth is drawn out by sliding it over a cartilage cushion, gathers food and carries it in. It consists of a narrow elastic ribbon beset with rows of teeth. Bivalves have no radula. (d) A soft rod in the digestive system rotates continuously, releasing digestive enzymes. (e) Embryonic development includes a unique larval stage, the veliger, which swims about aided by small lobes; eventually it sinks to the sea fl oor and metamorphoses into an adult that typically crawls on the sea fl oor, aided by a single foot. Living molluscs, estimated at up to 200,000 species, assemble into seven groups, one of which is the Gastropoda (snails and slugs), with up to 150,000 estimated living species.

Keywords Mollusc symmetry • Mollusc shell • Radula • Crystalline rod • Veliger

Molluscs exhibit such a rich and diverse variety of form and life style that they may not seem to cluster into one group of animals. Who would imagine, at fi rst glance, that snails, bivalves, squid and chitons all belong to the same group? In most phyla (a phylum is the highest rank of grouping within the animal kingdom) broad lines of external similarity are obvious between most animals and thus, for example, crabs are clearly somewhat similar to insects and to spiders in having segmented legs and all three groups form a natural phylum, the Arthropoda. Likewise, starfi sh externally resemble brittle-stars and sea urchins in having stiffened body walls and they form a different phylum, the Echinodermata. In the phylum Mollusca, however, external appearances (Fig. 1.8 ) do not bear immediate evidence as to the affi nity of its members to a single group, and only a deeper investigation will reveal common patterns. Snails, bivalves, octopus, squid and coat-of-mails are animals that represent the end-lines of different and very diverse evolutionary paths which split from

Fig. 1.1 Radial (circular ) symmetry

each other 500 million years ago (if not much earlier). And yet, Mollusca are the second largest phylum in the animal kingdom. What is a mollusc? Molluscs differ from other phyla of the animal kingdom in fi ve major characters, presented briefl y here; some of these will be expanded in the next chapter, devoted to defi ning snails. 1. The phylum Mollusca differs from other phyla in the basic structure of the body, as two types of symmetry are involved: the basic symmetry is bilateral, over which a different symmetry, a radial one, is imposed. Radial symmetry implies that there is a circular symmetrical arrangement of closely similar body organs of the animal around a central axis (Fig. 1.1 ). A predominantly radial symmetry occurs in those primitive groups of the animal world in which the adult is sedentary on the sea fl oor and fi lters tiny food particles from the water. This symmetry is found in corals, jellyfi sh, sea anemones and their relatives. Bilateral symmetry implies that there is a body end that contains many sensory organs (a head), and a body end with few sensory organs. A bilateral symmetry (Fig. 1.2 ) occurs in groups of the animal kingdom in which the adult moves over the sea fl oor in active pursuit for food. Already at the dawn of animal evolution, perhaps 600 million years ago, crawling locomotion forced upon the ancestor of these animals one body end which was always in front. This end always encountered new surroundings and therefore, many sensory organs developed in it, over eons of time evolving into a head. The end opposite this front end became the posterior (rear-) end, with fewer senses. Also, following the crawling mode of locomotion there evolved for the fi rst time a body surface that was always on the sea fl oor (ventral), which is how the abdomen evolved, and on the other side a body surface that always faced the water column (dorsal), which is how the back was 1 What Is a Mollusc? 5

Fig. 1.2 Bilateral symmetry

formed. The left side of the body remained, however, broadly similar to the right side, and this similarity was termed bilateral symmetry. The major signiﬁ cance of this term should, however, be understood as referring not to the left-right similarity but to the difference between the front of the body and its rear and between the back and the abdomen. This symmetry is found in worms, arthropods, chordates and other phyla, and to understand its importance in molluscs one must take a deep historical perspective. The ﬁ rst animals with bilateral symmetry were worm-like, very minute, and included also the ancestral forefathers of the molluscs. Eventually an increase in size was gained in the ancestors of the different phyla of animals with bilateral symmetry, in different ways. In the phylum Arthropoda it was gained by the budding off of repeated segments from the rear of the body, so that each segment now had limbs, muscles, and a genital and urinary system of its own. The ancestors of the molluscs increased their body size in their own way: instead of budding off repeated segments and of adding more and more limbs, they retained the original abdomen, as a single foot applied to the substratum (as in their worm- like ancestors); the worm-like body contained the digestive system, heart, genitalia and kidneys. As the abdomen-foot increased in size and reached a higher complex- ity of locomotion, it came to contain very many additional muscles that seem to have displaced, through evolution, all the viscera once contained in it. These displaced viscera became piled in a low hump carried above the foot, and it is the overall external shape of this hump that is characterised by a basic radial symmetry. During evolution this radial hump became covered by a protective calcareous external skeleton, the shell, secreted by glands arranged radially on the back of the hump. Accordingly, the shell, too, is characterised by a radial symmetry – as opposed to the foot which has a bilateral symmetry (Fig. 1.3 ). 6 1 What Is a Mollusc?

Fig. 1.3 Molluscs: combined bilateral and radial symmetry

Fig. 1.4 The shell and its position in a typical mollusk

2. The phylum Mollusca differs from other phyla in the presence of a protective calcareous external skeleton, the shell, which is secreted only from the back (Fig. 1.4 ). Early in their evolution, the mollusc ancestors secreted this protective structure only from the skin of the back (the ‘mantle proper’). Today, different groups of molluscs have different kinds of protective coverings. In very primitive mollusc groups the protective armour is secreted as numerous needles, in chitons it is deposited as eight large calcareous centres (‘valves’) around which there are many tiny calcareous needles. In bivalves it is deposited in two large centres (without calcareous needles) and in snails and cephalopods it is deposited in a single valve. In this manner the mollusc forms some kind of calcareous protective cover, the number of valves being almost always ﬁ xed within these major groups of molluscs. Later in evolution, the margins of the back of the viscera grew out and spread downward in some groups (snails, bivalves and cephalopods) and hung around the 1 What Is a Mollusc? 7 visceral hump like a skirt. Today, accordingly, the mantle of a mollusc consists of a mantle proper and a ‘mantle skirt’, also capable of secreting calcareous matter. The centre of the protective calcareous shield is thus formed both by secretions from the back of the visceral hump, the mantle proper, and from the mantle skirt. The partici- pation of the mantle skirt in secreting the protective skeleton increases the size of this external skeleton and enables the withdrawal into it of both the entire foot and the head, in most species. The mantle skirt (and with it, the protective body-covering armour of the shell) grows around all its margins, namely in radial symmetry. This is in contrast to the locomotive foot and the sensory head that, as explained above, both grow in bilateral symmetry. Many steps in the evolutionary history of molluscs stem from mutual interactions between these two parts of the body, the visceral hump and the foot- and- head, with their two different symmetries. The over-hanging mantle partly encloses an external space between it and the viscera, which is open to sea water, the space beneath the skirt. This space is named the ‘mantle cavity’ and located inside it are gills absorbing oxygen from the surrounding sea and ejecting bicarbonate (respiration). In bivalves, in addition to respiration, the gills function in feeding; and in cephalopods the mantle cavity functions as an organ for jet locomotion. In a few mollusc groups the mantle cavity is lost altogether. 3. Molluscs differ from other groups in the presence of a radula. This structure on the ﬂ oor of the mouth consists of a narrow, elastic ribbon beset with rows upon rows of hooked and pointed teeth. The radula is drawn out of the mouth by sliding it over a cushion of cartilage tissue, and its teeth scrape food from the surface of the rock, the plant or the prey (Fig. 1.5). When the radula is withdrawn into the mouth it carries the scraped food on its teeth. The radula is a key organ in the remarkable evolutionary success of many mollusc groups; however, it is lost in bivalves.

Fig. 1.5 The radula (Based on Solem 1974) 8 1 What Is a Mollusc?

4. Molluscs are characterised by the possible presence of a soft rod inside the digestive system, the ‘crystalline rod’. This rod rotates continuously around its long axis while releasing digestive enzymes (Fig. 1.6 ). 5. Molluscs differ from other phyla of the animal kingdom in that their mode of embryonic development includes a larval stage named the ‘veliger’ (Fig. 1.7 ).

Fig. 1.6 The crystalline rod in the digestive system

Fig. 1.7 Veliger 1 What Is a Mollusc? 9

The veliger swims in the sea aided by two or more small lobes that function as minute sails, or wings. After further embryonic development the veliger sinks to the sea fl oor (in most cases) and metamorphoses into an adult mollusc that crawls on the sea fl oor aided by a single foot. Any attempt to rigidly apply these fi ve basic characteristics to defi ne the Mollusca results in so many qualifi cations and exceptions as to be meaningless – not all fi ve characteristics are found in every single mollusc. Radial symmetry may be lost, the usually external shell may be internal or even absent, the radula and crystalline rod may be absent and the veliger replaced by direct development to a young adult. Rather than describing a group with sharply distinct morphology, the term Mollusca refers to a phylogenetic group with overall similarity. The word Mollusca, derived from Latin mollis meaning ‘soft’, is not a very suitable name for a group of animals with a characteristic hard, calcareous shell, indeed sometimes completely encasing the body as in bivalves. This name was fi rst used by Aristo (fourth century BC) for cuttlefi sh, squid and octopus, groups that have a reduced shell covered by the soft fl esh of the animal, or that lack a shell completely; 2,000 years later Linnaeus (1758 ) expanded the term and applied it also for land slugs and sea slugs. Since then, the evolutionary relationships of the more familiar shelled snails, bivalves, chitons and nautilus to the slugs, squid and octopus has been fi rmly established, and the group name Mollusca remained. Estimates of the number of living mollusc species range widely, with the minimum estimate around 40,000 and the maximum approaching 200,000. These species assemble into seven major groups, termed classes (Table 1.1 , Fig. 1.8 ; a class is a taxonomic rank immediately beneath the phylum). The structure of the body in the fi rst three classes resembles the presumed structure of the common ancestor of all molluscs more than in the last three, in which body structure is more derived and more complex. The Gastropoda (snails) outnumber other classes of the phylum Mollusca, and the number of their species is estimated as between 40,000 and 150,000.

Table 1.1 The phylum Phylum Mollusca Molluscs Mollusca, by its classes Class Aplacophora Aplacophorans Class Polyplacophora Coat-of-mails, chitons Class Monoplacophora Segmented Limpets Class Scaphopoda Sea Tusks (tusk shells) Class Gastropoda Snails and slugs Class Bivalvia Bivalves Class Cephalopoda Cephalopods (squid, octopus) 10 1 What Is a Mollusc?

Fig. 1.8 The seven classes of the phylum Mollusca

Bibliography

Fretter V, Graham A (1962) British prosobranch molluscs. Ray Society, London Linnaeus C (1758) Systema Naturae, 10th edn. Holmiae, Stockholm Ponder WF, Lindberg DR (eds) (2008) Phylogeny and evolution of the mollusca. University of California Press, Berkeley Yonge CM, Thompson TE (1976) Living marine molluscs. Collins, London Chapter 2 What Is a Snail?

Abstract Fundamentally the body consists of two storeys connected by a waist. The lower storey, for locomotion and ﬁ nding food, consists of a muscular foot and of a head, with senses and a mouth. The upper storey, for respiration, digestion, excretion and gamete production, also secretes the shell, which is attached to the snail by a well-developed muscle. Snails are also characterised by torsion: during embryonic development the visceral hump rotates 180° in relation to the foot; this huge change in the relationship between the major body parts is unique to snails in the entire animal kingdom. The head has one pair of eyes, one or two pairs of tentacles, an abdomen used as a crawling organ, and a shell, which may grow as a broad cone or coil spirally. The foot carries a hardened lid, the operculum, to prevent predators from penetrating the shell and water from leaking out, in intertidal habitats. To crawl, power supplied by muscular contractions of the foot is transferred to the substratum through sticky mucus – an energetically very costly locomotion with very low efﬁ ciency. The mantle cavity is usually a small area around the gills into which the viscera discharge their wastes. Digestive juices may contain cellulase – one of the very few cases throughout the animal kingdom of an animal producing its own decomposing enzyme.

Keywords Gastropod attachment • Gastropod defence • Gastropod embryonic development • Gastropod feeding • Gastropod locomotion • Gastropod metamorphosis • Gastropod operculum • Gastropod reproduction • Gastropod respiration • Gastropod shell

The class Gastropoda (snails and slugs) includes molluscs in which the abdomen is a creeping organ (the scientiﬁ c name means ‘those of a stomach and a foot’) with a head equipped with a pair of eyes, one or two pairs of tentacles and a chalky shell which permanently protects the viscera (in some groups the shell is secondarily lost). The foot usually carries a horny or calcareous shell lid, named the ‘operculum’, which can block the shell aperture after the animal has withdrawn into it. Internally, snails are also characterised by torsion: during embryonic development the visceral hump rotates by 180° in relation to the foot. Additionally, the mantle cavity is only a pocket-shaped space restricted to a small area around the gills and into which the

Fig. 2.1 A snail: major body systems viscera discharge their waste. Much of the evolution of sea snails takes place within this cavity. The body of a typical snail (Fig. 2.1 ) can best be understood as being organised in two storeys connected by a waist. The lower storey is responsible for locomotion and fi nding food, and consists of a fl at-soled muscular foot and a head with many sensory cells and a mouth. The upper storey of the body carries out all visceral functions of the body – respiration, digestion, excretion and production of gametes; it also secretes the shell, which permanently shelters the viscera. The shell is attached to the body of the snail by a well-developed (paired or single) muscle. This chapter presents the manner by which fi ve basic processes in the body of a snail – defence, locomotion, respiration, feeding and reproduction – have contributed to its morphological design.

2.1 Defence: Shell and Operculum

The shell offers refuge both from predators and from desiccation: during routine activity in the sea the snail extends its foot and head (the lower storey) beyond the shell’s limits, but in moments of danger they are quickly withdrawn and the snail is completely covered and protected by the shell. The shell consists mainly of calcium carbonate, with a small amount of protein. Formation of the shell already begins in the embryonic stage, when a soft delicate mesh of protein fi bres is secreted from the outer skin of the viscera and from the mantle. Very soon during embryonic life, secretion of the protein fi bres is followed by the secretion, from the same cells, of calcium carbonate (CaCO3 ) that nucleates 2.1 Defence: Shell and Operculum 13 and grows on the previously secreted fi bres as hard crystals of aragonite. The protein mesh thus serves a double function: as a mould that determines the position and direction of the calcium-carbonate crystals, and as a soft base which holds and binds the hard aggregate of mineral crystals together, giving the shell some possibility of fl exibility, without which it would be very brittle. After the embryonic stage, when the snail is already a miniature adult dwelling on the sea fl oor, the shell continues to grow by the addition of a protein mesh and calcium carbonate, mainly on its margin but also on its interior side. In a growing snail the embryonic shell (named the ‘protoconch’) becomes the shell apex. Shell building requires energy. The energetic cost of laying down the protein mesh, which by weight accounts for only 2 % of the shell, is about twenty times higher than that for laying the calcium carbonate component. In many primitive snails the shell consists mainly of mother-of-pearl: fl at calcium crystals deposited one on top of the other in an organised structure like a brick wall, and the face of these crystals parallels the surface of the shell. Each crystal is approximately 0.005 mm thick and all crystals are deposited in a thick matrix of protein. A shell made of mother-of-pearl is characterised by considerable fl exibility, but is rather weak. As a side effect, mother-of-pearl often glistens with a soft, silky lustre. Different light rays penetrate it to different depths, and when they are refl ected, the incorporation of the rays into each other causes a change in colour. Mother-of-pearl shells occur, beyond snails, also in other molluscs (bivalves and cephalopods), and is thus a very primitive character in the phylum Mollusca. It is of course also the microstructure of pearls. In some snail groups, the shell grows as a broad cone or a fl at saucer; in other groups the shell, while growing, coils spirally around its axis. A complete coil of the shell is termed a whorl. If the coiling spiral of the shell material is tightly wrapped around its central axis, a small calcium carbonate column is formed at the centre of the shell by the inner walls of the whorls, termed the ‘columella’ (Fig. 2.2 ). The columella is clearly visible as a structure when the shell is broken, sliced in half vertically, or in an X-ray. If the growing shell coils distantly around its axis, an open calcium-carbonate hollow cone is formed at the centre of the shell, rather than a solid column; it is termed the ‘umbilicus’. The umbilicus is clearly visible from the outside, by observing the shell when its opening faces the observer and its apex, the protoconch, faces away. Shell geometry may change during ontogeny and in many genera the juvenile shell has an umbilicus whereas adults do not. In most cases (more than 90 % of sea snails) the coiling of the shell’s whorls is clockwise, and such shells are termed ‘dextral (or ‘right’) shells’. In a small minority of sea snails the shell’s whorls coil in an anticlockwise direction, to the left, and such shells are termed ‘sinistral (or ‘left’) shells’. We as yet do not know of any survival value to the direction of coiling. The last whorl is the biggest, its interior space encompassing the gills when the snail is active, and also the head and foot when it withdraws. It is termed the ‘body whorl’. 14 2 What Is a Snail?

Fig. 2.2 Shell structure and terminology

Shell growth is not continuous and it often leaves distinct growth lines. Upon maturity the snail may cease growing, and with it the shell. The region around the aperture may then become thickened and strengthened. Inside the shell aperture there may be folds or ridges, mechanical obstacles to make it diffi cult for predators, such as crabs, to penetrate the shell. Shell growth is extremely sensitive to environmental conditions. In some cases the size of the teeth may be directly infl uenced by the presence of crabs in the surrounding water: chemicals leaking out from the crab spread in the water, and a snail sensing them may develop larger teeth and thereby improve the effi ciency of its defensive system. Avoiding predators is crucial for small, slow-moving sea snails. Protective shells are one way to deter predation, but are metabolically expensive to produce and they reduce speed. Furthermore, some predators can cut through the shell to reach the live snail. Faced with predators that are larger, faster and able to overcome the defensive qualities of shells, another possible defence strategy would be for sea snails to focus on the presence of chemical components of injured individuals of their own species. Chemical cues from extracts of conspecifi c animals in the water warn many sea snails of the proximity of predators and initiate behaviours to reduce predation. Sea snails thus grow more predator-resistant shells when exposed to a chemical stimulus from damaged con-specifi cs, and they may also stop motion and withdraw into their shells, or try to escape by leaving the place rapidly, over the substrate or in the water column. 2.1 Defence: Shell and Operculum 15

The surface of the shell sometimes consists of a complex sculpture of ribs and spines. It also may have a thin envelope of protein without calcareous matter, the ‘periostracum’, which covers the shell like an envelope. This is the outermost layer of the delicate protein mesh of fi bres, and it remains as such because the secreted calcareous matter does not reach it. This layer perhaps protects the snail from the damaging action of micro-organisms seeking to bore into the calcium-carbonate shell. It also appears to camoufl age the shell, which may protect it from predators. As a sea snail grows it enlarges its shell little by little. The enlarging shell produces a spatial shape that is fi xed (more or less) for each species. All shapes of all shells in the world may be described by a mathematical formula consisting of only four variables (Fig. 2.3 ):

(a) the shape of the coil in transect; (b) the distance between the coil and the axis of the shell; (c) the rate of increase in the size of the whorl as it coils around its shell axis; (d) The extent of overlap between each whorl and the whorl preceding it. A computer fed with data of these four variables can draw the general shape of the shell of any snail in the world; a computer fed with another dozen variables can draw its precise shape. This mathematical simplicity, which is the basis of all diversity in the shapes of all shells of all genera, families and orders, indicates that the evolution of the entire class Gastropoda could have been rendered by a small number of genetic changes in a small number of the mechanisms regulating the processes of embryonic development. Glandular cells containing colour pigments are positioned along the margin of the mantle and they secrete their contents immediately after the calcium-carbonate of the shell is secreted, so the colour is absorbed into the calcareous layer before it hardens. Among the known colour pigments, some consist of melanin (shades of black, brown, yellow) and others are porphyrins (green, red). A shell’s colour pattern results from the activity of these colour glands. If some glands secrete their

Fig. 2.3 Shells drawn by a computer (Based on Raup 1962 ) 16 2 What Is a Snail? contents continuously, a pattern of stripes will be formed on the shell; if they secrete their colour cyclically, the pattern formed will be of dots, dashes or blotches; if all glands of the mantle margin secrete their pigments simultaneously and continuously, a shell will have a uniform colour. If we put a shell to our ear when inside a room and near an open window, we may hear ‘the whisper of the sea’. This whisper results from air withheld inside the shell. When a slight background noise (such as a passing car) reaches the shell, the air withheld inside it echoes and ampliﬁ es the background noise. If we listen to the same shell in a place where there is no background noise, such as in a closed ward- robe full of clothes, the shell will not ‘whisper the sea’. The operculum, a ﬂ at plate consisting of horny matter, rests on the upper, dorsal side of the foot, usually near the back end (Figs. 2.4 and 2.5 ). When the snail actively moves, the operculum functions as a supporting pad for the shell. When the snail withdraws into its shell, the operculum blocks the aperture to serve two protective functions: it prevents penetration by predators and prevents water from leaking out

Fig. 2.4 Position of the operculum in a creeping snail (Left ) and up on withdrawal into shell ( Right )

Fig. 2.5 The operculum Left : operculum of Monodonta Centre: operculum in a withdrawn snail ( Littorina ), view into shell. Right : operculum in a crawling snail (Littorina ), view from above onto back of foot (Based on Fretter and Graham 1962 ) 2.2 Attachment and Locomotion 17 in exposed, intertidal habitats. The corneous matter at the centre of the operculum is almost as hard as human fi ngernails; its periphery is softer and more fl exible, enabling it to plug the aperture effectively as the sea snail retreats deeper and deeper into its shell. The operculum is secreted from a groove which transverses the dorsal side of the foot. Sometimes the right side of the groove secretes at a faster rate than the left one, and this difference forces the operculum to grow spirally (anti-clockwise) on the back of the foot; eventually the whole operculum takes the form of a wide, fl at coil rather than a fl at plate. There is considerable variation in the structure of the operculum. In some groups calcium carbonate is embedded into its protein layers. Such a calcareous operculum is not fl exible, but it is stronger than an all-protein operculum. In some groups the operculum forms a tight coil, in others the coil may be loose, or there may be no coil at all.

2.2 Attachment and Locomotion

In moments of danger a snail withdraws into its shell and adheres fi rmly to the substrate, so as not to be detached by waves or predators. A single muscle (in primitive groups, a pair of muscles) descends from its proximal point of attachment on the interior side of the shell through the upper parts of the body and down into its distal end in the foot, where it branches out into the foot’s deep tissues. When this muscle contracts it rapidly withdraws the foot and head into the shell and also brings the shell down over the whole body. In snails with coiled shells, the upper (proximal) point of muscle insertion inside the shell is onto the columella, and therefore this muscle is commonly named either the ‘shell muscle’ or the ‘columellar muscle’. The point of insertion on the columella, rather far up inside the shell, is the highest point to which a snail can withdraw when retreating. Upon contracting its shell muscle, a snail may also strongly press its foot against the substratum and attach to it by means of mucus. Sea snails could not function without producing a carpet of mucus that is used in attachment and in locomotion. The foot sole secretes a thin layer of sticky mucus (‘slime’) both from a large multi-cellular gland at the front of the sole and from many different types of unicellular glands, scattered all over the sole. There may be up to six types of unicellular glands in any one individual, and the mucus cocktail that the various glands secrete mixes as it is spread over the sole by cilia. The mucus is released from the glands in the form of tiny membrane-bound granules, 0.005 mm in size. The membrane bursts in response to a wide range of environmental factors (including mechanical force, and even minute levels of ATP) and the granules absorb surrounding seawater, thereby producing the functional mucus. Their capacity for absorption is remarkable, and they swell to up to 800 times their original volume. It is this mucus that enables a snail to stick to its place. Once secreted, the mucus keeps its stickiness for several hours until it gradually dissolves in the water; this is faster when strong waves pound upon it than when 18 2 What Is a Snail? the sea is calm. Mucus is further lost by microbial breakdown. The sticky mucus adhesive extends the snail’s range of muscular-moving to vertical faces and to overhangs. In the intertidal habitat mucus may dry at low tides, and its strength and stiffness then increase considerably. As the tide returns the mucus re-hydrates, though very slowly, regaining only approximately 15 % of its hydrated weight over a 6-h period. In the daily tidal cycle of nature, mucus is therefore unlikely to return to its fully hydrated state. In addition to its function in adhering to the substratum, the foot also serves in locomotion, and the mucus then acts as a medium in which cilia of the sole beat to propel the snail forward. Early ancestors of sea snails used to crawl mainly by use of cilia on the sole of their foot, all beating in the same direction; this cilia motion was assisted by the contraction of small muscles inside the foot. Certain recent sea snails also combine cilia outside the foot and muscles inside it to crawl. This ciliar locomotion is common in both small snails of less than 15 mm and also in those large snails that dwell on soft sediments, where they cannot lever muscular contraction. Muscular effort is usually of greater importance among larger sea snails. It is two to three times slower than cilia locomotion and is less economic in terms of energy. On the other hand, it is more powerful than ciliar locomotion, and also enables a fi rm grip on a hard substratum. To enable locomotion, the foot contains a system of dense longitudinal, transverse and diagonal muscles that entwine and interweave into each other in a complex muscular network (these foot muscles are not to be confused with the shell muscle, also present in the foot). Waves of contraction roll forward from the rear of the sole and push the snail forward over the substrate, or move backwards from the front of the sole and pull it along. Sometimes the two types of waves are operated simultaneously, alternating across each longitudinal half of the sole, thereby offering additional fl exibility in locomotion. In addition, an increase in the rate of the contracting waves along one longitudinal half in comparison to the other would enable a faster turning movement. The power for locomotion, supplied by the series of contractions of the foot, is transferred to the substratum through the 0.04 mm of sticky mucus. This sticky mucus has two disadvantages: the sea snail is compelled to overcome the stickiness so as to move, and it must form new mucus so as to adhere to the site that it has moved to. This means that muscular locomotion involving mucus exacts a very high energy cost. Snail crawling is the most costly form of locomotion throughout the whole animal kingdom, and its effi ciency is low. It is twelve times more expensive than that of a mouse running, and one hundred times more expensive than a fi sh swimming, in animals of similar weight. The expense of a snail’s mucus production alone may reach 30 % of the energy that it takes through its food. A snail devotes only 9 % of the overall energy devoted to muscular contraction, whereas it invests 35 % in mucus secretion and 55 % in overcoming mucus stickiness. The sticky mucus limits a snail’s speed of movement and thereby limits its ability to seek food, to mate or to fi nd shelter. Consisting mostly of water (80–94 %) and of proteins and carbohydrates possibly linked by electrovalent bands, mucus is one reason snails are slow, sluggish creatures. 2.3 Respiration 19

Depending upon the extent of stress applied to it, mucus may react as a viscous- elastic solid, forming an effective adhesive; or may yield to become a viscous liquid; and once the stress is released, the mucus heals and returns to its solid state. Under the leading edge of a muscular locomotion wave travelling along the sole of a snail the mucus beneath the sole is stressed and as a result fl ows, allowing the wave to progress. As the wave passes over the mucus the stress lessens and the vis- cosity of the mucus increases, providing the adhesive coupling between the substratum and the snail. As muscular locomotion waves pass along the foot, parts of the foot remain attached to the substrate while others are lifted. In those small areas where the foot is lifted the mucus is stressed to yielding, becoming liquid, so its adhesive capacity is lost and the wave moves along the foot over the liquid mucus. But the mucus heals quickly once a muscular locomotion wave has passed it, and those parts of the foot applied to the substrate rest on solid mucus, providing the adhesion necessary to attach the foot and to resist the forces generated by the passage of pedal waves. In addition to surface area of contact and the surface tension of the adhesive fl uid, other factors are also involved in determining the force of adhesion. One of these may well be muscular tension, as suggested by the fact that if limpets are caught ‘unawares’ they are comparatively easy to dislodge. Beyond attachment, mucus is of use in several other aspects of the natural history of sea snails. Trail-following, namely the crawling over existing mucus trails, will reduce the expense of producing a mucus trail. Mucus trails both stabilise the substratum and produce a smoother surface over which to move, so the amount of mucus produced can be reduced while snails are trail-following. When tracking over weathered trails, snails adjust their mucus production to recreate a convex trail profi le of similar shape and thickness to the trail as originally laid down. The mechanism by which the snails perceive the quality of a trail and thus are able to adjust their production of mucus is as yet unknown. Maximum benefi t from trail following in energy terms occurs when previous trails were laid down recently. Mucus trails might also be used in navigation, to home and to fi nd mates, and they might also assist in feeding, by trapping food particles from the water column.

2.3 Respiration

A cavity exists between the body of a snail and its overhanging mantle skirt, termed the mantle cavity (Fig. 2.1 ). Its fl oor is formed by the upper surface of the foot, its ceiling by the mantle skirt. Two feather-like gills protrude into the front part of the mantle cavity and it is in these thin-walled organs that oxygen absorption from the sea water takes place. Each gill consists of two rows of triangular leafl ets organised on either side of a central axis (Fig. 2.6 ). Complex routes of cilia cover the leafl ets, each route with a different function. Those cilia on the opposing surfaces of the leafl ets are of prime importance in respiration because it is the beating movement of 20 2 What Is a Snail?

Fig. 2.6 Part of a gill with eight leafl ets, alternating on either side of a central axis these cilia that forms the current that draws oxygen-rich sea water in from beneath the gills upwards so that it fl ows among the leafl ets. The cells of the leafl et walls absorb the oxygen molecules from the passing water and release molecules of carbon dioxide into the water. Streams of water from right and left converge along the median line over the anus and kidney openings and are ejected from the mantle cavity at the front. The newly absorbed oxygen in the gill leafl ets must now reach the body tissues. A duct that carries oxygen-poor blood enters the gill, passes along the upper part of the central axis, and branches off into smaller ducts that enter the upper part of each leafl et (Fig. 2.7 ). These smaller ducts are perforated, so the blood fl ows out of them and drips downwards, between the delicate walls of the leafl et. The dripping blood comes into close contact with the leafl et walls and receives the oxygen from them. The newly oxygen-loaded blood now collects in tributaries that unite to another duct, on the lower part of the axis that leads to the heart. The process of absorbing oxygen from the water is simple, but it involves overcoming three dangers. One is that the up-fl owing water current may contain 2.3 Respiration 21

Fig. 2.7 Blood system in one leafl e t chemical compounds toxic to the snail. A special chemosensory organ situated near the gill copes with this danger: termed the ‘osphradium’, its surface is covered with oar-shaped cilia that sense chemical materials dissolved in the water. If a toxic substance is detected, the shell muscle contracts and the mantle cavity of the snail closes for some time, as the head and foot are squeezed into the shell. Another danger is that the up-fl owing respiratory water current may contain solid particles, such as sand, that might block the small spaces between the leafl ets, scratch the delicate cells lining them and thereby sabotage the effi ciency of respiration. A complex system of ciliated mucus-producing cells deals with this danger. When the water current enters the mantle cavity, any sand grains present are swept upwards in the up-fl owing current until they reach the lower edge of the leafl ets. The sand contacting the cilia causes their cells to secrete large quantities of mucus in which the grain becomes entangled. Neighbouring cilia on this lower edge of the leafl et all beat in the same direction, thereby transporting the mucus mesh loaded with sand to the tip of the leafl et. Here it is dumped on the underlying fl oor of the mantle cavity, where supplementary cilia ‘cough it out’ by transporting it outside the body. The third danger is that the strong upward current might sway the delicate leaf- lets to such an extent that their surfaces might adhere one to another, and such a situation would limit the free movement of oxygen-bearing water between the leafl ets. This danger is overcome by a system of delicate skeletal cartilage rods inside the 22 2 What Is a Snail? lower part of each leafl et, where the upward current is the strongest. These rods are connected to additional rods along the axis of the gill. The whole system of skeletal rods is fl exible and muscles inside the axis can bend them, keeping the leafl ets apart. Snails’ blood contains haemocyanin, a copper-containing protein that can bind oxygen effectively. Thanks to this protein, the blood carried from the gills to the heart contains two to three times more oxygen than a physiological saline without haemocyanin. Heart pulsations push the oxygen-rich blood through a ‘closed system of arteries’ (their walls are built of epithelium, namely of a layer of closely- adhering cells that touch each other along a considerable part of their surfaces). This closed system leads the blood to a system of ‘open arteries’ without epithelial walls that surrounds the viscera and the muscles; in this manner all organs are bathed in oxygen-rich blood. The body organs receive the oxygen from the blood and release carbon dioxide into it, and the blood (now with little oxygen but rich in carbon dioxide) returns to the gills via a system of veins to release the carbon dioxide and again receive oxygen. Even when assisted by haemocyanin, the oxygen-carrying capacity of a snail’s blood is not high and therefore snails are, by and large, slow and clumsy animals. In addition to transporting oxygen to the body tissues, blood has several other functions. One of these is to transport nutritional compounds from the digestive gland to the various organs. Another function is to serve as an antagonist to the contraction of various muscles. For example, withdrawal into the shell involves rapid contraction of the shell muscle and this is accompanied by the rapid transfer of blood from the withdrawing foot into spaces deep inside the visceral mass. Later on, when the foot spreads out again, the shell muscle slowly relaxes, and other muscles within the body slowly push the blood from the inner spaces of the visceral mass into the head and the foot, and thereby push them out again. The tentacles may also be rapidly withdrawn and later slowly pushed out by muscular contraction and blood transport. The overall quantity of blood in the body is limited, and this enables the snail to withdraw the whole volume of all body organs, with all their blood, into the limited confi nes of the rigid shell. This constraint also limits the amount of haemocyanin in the blood and the amount of absorbed oxygen. All of these contribute to restriction of speed in a snail’s locomotion. The heart, containing only oxygenated blood, is inside a small sac, termed the ‘pericardium’. Waste materials in the blood fi lter into this sac, through minute pores in the walls of the heart. From here they are transferred into two ducts lined with cilia that drain into the mantle cavity. It is from these ducts that snails’ kidneys later evolved. Vital materials are re-absorbed from the waste in the kidneys back to the body, and fi nal waste materials are secreted from the kidney cells. This mixture of waste products drains to the mantle cavity from where it is fl ushed out by the respiratory current. Food waste, coming from the alimentary system, is also released into the mantle cavity. However, nitrogen waste, secreted as ammonia, leaves the blood and fi lters into the sea via the gills, not the kidneys. The blood of molluscs is usually termed ‘haemolymph’. 2.4 Feeding 23

2.4 Feeding

Sea snails show extraordinarily diverse feeding patterns, ranging from grazing on vegetation and fi ltering plankton from the sea column through scavenging on organic debris to raptorial feeding with poison darts. The ancestral feeding condition is an algal grazer feeding over rocks, and due to many morphological modifi cations of various organ systems, modern species have come to occupy a wide variety of feeding niches. The mouth cavity of snails contains the radula, a special rasping organ unique to molluscs (Chap. 1 ). It is a fl exible ribbon, on which successive rows upon rows of backwards-pointing teeth are mounted (Figs. 1.5 , 2.8, and 2.9). Beneath the fl exible ribbon, but not adhering tightly to it, is a cartilage cushion, the ‘odontophore’. A highly complex system of muscles moves the ribbon outwards and inwards, by sliding it over the tip of the cartilage. As they slide over the cartilage the teeth are erected and can scratch, pierce, tear, brush, sweep or rake objects with which they come into contact. In this manner, by a to-and-fro movement that involves alternate exposure and infolding of the teeth, food is collected. With the return movement of the radula, the teeth transport food into the mouth. The teeth themselves are almost as strong as human fi ngernails, and they crack, break and wear away during use, whether by the food itself or by the hard substratum from which the sea snail scrapes. The worn-out teeth are shed and new rows are formed in a special sac in the rear part of the radular complex. The whole radula, with its fl exible ribbon and rows of teeth, is renewed at a rate of two to fi ve rows a day, depending on the snail’s age, species and natural history. The teeth are arranged in transverse rows, each tooth in a row with a somewhat different function. Some are narrow and sharp and pierce the food, while others are wide and catch and rake it into the mouth cavity. Each repetitive row consists of a single central tooth

Fig. 2.8 Functional organs in the mouth cavity (longitudinal section) 24 2 What Is a Snail?

Fig. 2.9 Radula: a panoramic view from outside into the mouth

(in most species), on either side of which are the lateral teeth; fl anking these, on the margins of the fl exible ribbon, are the marginal teeth. The series of repeating teeth rows are broadly identical. There is considerable variation as to the number and shape of the teeth among different groups of sea snails. Predatory snails have but few large hooked teeth, whereas many herbivorous snails have many small fl at teeth. In view of this variation, it is not surprising that the radula offers key characters in snail classifi cation. For convenience of the description of teeth arrangement, it is customary to use a ‘radular formula’ that specifi es the number of each type of tooth on each side of the radula. For example, in the genus Littorina (a winkle) that feeds by scraping algae from rocky shores, the formula is 2.1.1.1.2: there is one central or median tooth and one lateral tooth on either of its sides and two marginal teeth on each fl ank; in Aplysia (a sea hare) that browses algae, the formula in some species is 80.50.1.50.80, namely one central tooth, 50 lateral teeth on each side and 80 marginal teeth on each fl ank; Hexaplex (a murex) that preys on sessile animals has the formula 0.1.1.1.0, with one central tooth, one lateral tooth on each side and no marginal teeth. Usually the teeth formula is broadly similar at the level of a family and even of an order, but it may change even in the same individual as its body grows in size. This instability in the radula formula is obvious especially in groups such as sea hares, that both grow very rapidly and have many teeth in each row. Many sea snails have a jaw in the front part of the roof of the mouth cavity, above the radula. It usually consists of two rigid plates of a hard corneous matter. By lifting the food-loaded radula complex and pressing it against the jaws, the food may be squashed and broken into particles. The jaw does not usually function in biting. Food particles gathered by the radula and squashed by the jaws are transported inward to the mouth cavity and from here back to the oesophagus (Figs. 2.9 and 2.10). Here the food is mixed with large quantities of saliva, pouring out from two 2.4 Feeding 25

Fig. 2.10 Digestive system (general view slightly spread out, roof of stomach removed) (Based on Fretter and Graham 1962 ) large salivary glands that discharge to the front of the oesophagus. This saliva serves as a convenient substrate for the activity of the digestive enzymes, secreted further on along the alimentary system. A certain extent of digestion begins already in the oesophagus, along which unicellular digesting glands are scattered, but most of it occurs in the stomach, into which the digestive gland secretes many digestive juices. These juices attack the food lump, causing its physical and chemical breakdown. Ciliated ridges on the stomach wall sort the partly digested particles by size, and small particles are directed into one of the two duct openings that lead to the digestive gland. The cells of the digestive gland both secrete the digestive enzymes and engulf the digested particles into intra-cellular vacuoles, and the process of digestion and absorption into the body is thereby completed. Upon completing the digestive process, the engulﬁ ng digestive gland cells reject waste remains back into the ducts, from where they are directed back into the stomach. Cilia direct these waste products to a gutter on the stomach ﬂ oor. This ciliated gutter starts at the outlet openings of the oesophagus and digestive glands, continues all along the stomach 26 2 What Is a Snail?

ﬂ oor and leads to the rather lengthy intestine. Here faeces are formed, enveloped in mucus and transported along to the anus that drains into the mantle cavity, in snails and some primitive sea slugs. The digestive juices of several herbivorous sea snails contain the enzyme cellulase which breaks down cellulose. This is one of the very few cases throughout the animal kingdom of an animal producing an enzyme capable of breaking down cellulose. Usually herbivorous animals must gather, store and maintain cellulose- digesting bacteria and protozoa inside the alimentary system. The stomach of some groups of sea snails feeding on vegetable matter contains a transparent soft rod consisting of muco-protein. Termed the ‘crystalline rod’ or ‘crystalline style’, it is secreted at its lower end from the walls of a special pouch in which it is contained. Cilia lining the pouch slowly rotate it around its longitudinal axis, and its upper end dissolves in response to the chemically acidic environment of the stomach. The rod also dissolves in response to mechanical rasping. A hardened region, the ‘stomach shield’, covers the rear walls of the stomach and has a hardened tubercle at its centre. The crystalline rod rubs against this tubercle and in doing so is worn down and enzymes are released. The rod is soaked with enzymes that break down starch, and upon being released from the dissolving rod they contribute to food digestion. The rod also serves as a food mixer. Formed and worn down in a daily rhythm, this rod is the most beautiful example throughout the animal kingdom of an organ that rotates continuously. The track of the alimentary system seems odd: beginning in front at the mouth, it rises back along the body to the stomach, but then, instead of continuing to the rear of the body, it loops and descends forwards to the anus at the front of the body, where it drains into the mantle cavity. The evolution and development of this strange loop will be elaborated on in the next heading, in the context of embryonic development. It is also somewhat odd that snails should secrete their faeces into their respiratory cavity. The far-reaching evolutionary consequences of this aspect will be discussed in Sect. 4.1 .

2.5 Reproduction and Embryonic Development

The sexes among sea snails are usually separate, but together in sea slugs. The lobes of the gonad, whether ovary or testis, lie near the apex of the visceral hump, among the lobes of the digestive gland, and they drain into the pericardium (the epithelium- lined sac surrounding the heart). In the basic condition, as still found in primitive sea snail groups, ova or sperm are ejected into the pericardium and carried via the kidneys into the mantle cavity, from where they are broadcast into the surrounding sea where fertilisation takes place. (For the unfertilised female gamete I use the term ‘ovum’ plural – ‘ova’, and the fertilised cell I term ‘egg’, throughout the book.) Male and female approach each other, often touching. The female sends out chemical signals, termed ‘pheromones’, and the male responds by discharging his sperm into the water; this, in turn, stimulates the female to spawn her as yet unfertilised ova. 2.5 Reproduction and Embryonic Development 27

Fig. 2.11 Trochophore

A thin layer of mucus envelopes each ovum and it swells upon contact with sea water. The ovum now secretes a substance that accelerates sperm movement towards it and the stimulated sperm hurriedly swims to reach and attach to it. The sperm then secretes a substance that dissolves part of the ovum’s envelope, penetrates and fertilises it. The fertilised egg develops within approximately a day (depending upon environmental, genetic and random factors) and becomes a larva, an embryonic form capable of independent locomotion. At this early embryonic stage the larva is a ‘trochophore’ (Fig. 2.11 ). This is a small ball of cells (approximately 0.1 mm in diameter ) surrounded at its equator by one or two rings of ciliated cells. The cilia beat synchronously so the trochophore moves in a rotating movement, always in clockwise direction. The upper pole of the trochophore bears a tuft of non-motile cilia, perhaps sensory organs for balancing in the water, and an additional, smaller tuft of cilia is often present on the lower pole. A mouth leads to a blind sac that, in this early embryonic stage, cannot receive food but will become the alimentary system. A trochophore type of larva is also found in other phyla of the animal kingdom such as arthropods and annelids. Attracted to light and swimming near the sea surface, the trochophore is a brief larval stage, and within another day or two it develops into a more advanced stage, the veliger (Fig. 2.12 ). The veliger, still a larva, differs noticeably from the trochophore in that it develops, out of either ﬂ ank of its mouth, a bi-lobed structure resembling a tiny sail (or veil, hence their scientiﬁ c term ‘velum’ and the broader term ‘veliger’ for this developmental stage). The veliger usually swims with its sail facing up and its viscera, enclosed in a tiny shell, hanging down in the water column. 28 2 What Is a Snail?

Fig. 2.12 Veliger

This sail-like structure develops from the frontal part of the equatorial ciliate ring containing the mouth whereas the cilia at the rear of the ring degenerate and are absorbed into the body. The blind sac at the back of the mouth grows and lengthens to the rear of the body to become the alimentary system, and a small opening is broken out, forming the anus. The skin on the veliger’s back secretes a tiny protective shell, which may coil slightly upon growing. Later a mantle, a mantle cavity, the gills, a radula and the foot develop. Indeed, the sail is the only larva-speciﬁ c organ, and the veliger bears the external appearance of a minute snail but for this veil. At metamorphosis the veliger ‘turns upside down’: the foot becomes ventral (and large) and the shell dorsal. However, soon after development of the sails something else happens, remarkably strange and very interesting: the back (dorsal) part of the upside-down veliger, containing the visceral mass, rotates in 180° anti-clockwise in relation to the head and foot. Details of the mechanism of this turning around (termed ‘torsion’) are beyond the scope of this book, but a cardinal consequence of this process is that the embryonic area destined to become the mantle cavity, including the gills inside it and the anus of the alimentary system and kidneys, are brought from a posterior position to an anterior one, so that the respiratory chamber (mantle cavity) is now just behind and above the head (Fig. 2.13 ). Only after torsion is completed can the veliger retreat into the mantle space of its embryonic shell. This huge change in the relationship between the major body parts is unique to sea slugs and snails in the entire animal kingdom. 2.5 Reproduction and Embryonic Development 29

Fig. 2.13 Position of the mantle cavity, digestive system and head. Above : primeval position; below : position after torsion

The veliger is a plankton-dwelling larva unique to the phylum Mollusca. Its sails are organs that serve only in embryonic locomotion, and are absorbed at metamorphosis into the adult form. The veliger in primitive sea snail groups feeds mainly on dissolved organic matter, especially amino acids, absorbed into the body through the surface of the rather small sails that protrude only slightly beyond the mouth as small lobes. Within just 1 h of being absorbed, 50 % of the dissolved organic matter may already be found in the proteins of the veliger’s body. In advanced sea snail groups, the veliger feeds also on tiny planktonic algae that are swallowed and then digested. In these snails, the sail is larger and consists of two layers of cells with blood spaces, muscles and a dense network of nerves between them. The cells lining the margins of each sail are densely covered with cilia, organised in three hoops. One, consisting of long and delicate cilia, gives the veliger its locomotion powers and creates the current that brings in food; a second hoop, of exceptionally long cilia, traps the food; and a third, of short cilia located in a shallow groove, transports the food towards the mouth. The embryonic shell is small, cap-like and constructed, at this early stage, only of transparent protein elements, without calcium carbonate crystals. As the visceral hump grows during embryonic development, the shell may coil slightly around its axis. A short coiled shell positioned beneath the sails of a larva swimming in the plankton enables better manoeuvrability than a long, cone-shaped shell, when currents 30 2 What Is a Snail? prevail or when the sea is wavy. In moments of danger the sail is quickly withdrawn into the small shell and the veliger sinks down the water column. The veliger has a fully developed and complete alimentary system. The embryonic digestive gland develops on either side of the stomach as two lobes containing albumen. This is the veliger’s main source of nutrition and it enables independence, especially in the early stages, from food. Later on the veliger may complement the albumen diet by also eating tiny algae fl oating in the water, capturing them on the cilia of the sail. A muscular lobe develops beneath the mouth, and at fi rst it licks food particles from the sail. Later on, in more advanced embryonic stages, it grows and develops into the snail’s massive foot, its sole covered by cilia. When the veliger retreats into its shell, the rear part of the foot is the last to be withdrawn; a protein plate that blocks the shell aperture, the operculum, develops on the back of this part. The veliger develops several sense organs. A pair of tentacles develops where the earlier trochophore once had its upper pole of ciliated tuft. An eye develops at the base of each tentacle, as a shallow pit containing cells sensitive to light in which there are also granules of black pigment. A pair of balance sense organs develops at the stem of the foot and they may perhaps offer some dim sense of hearing. The entire skin is, most probably, sensitive to odours in the water. Veligers usually grow in conditions of plentiful food. However, predation causes such heavy mortality among their ranks that chances of a single veliger surviving its fi rst month of life are very slim. Predators include a wide range of plankton-feeding animals, some dwelling in the plankton (molluscs, fi shes, arthropods) others on the sea fl oor (crustaceans, polychaetes, corals). The very few surviving veligers continue development and eventually seek a place to metamorphose into adult snails.

2.6 Metamorphosis to Adult Form

At an advanced stage of its life the larval veliger will metamorphose to an adult sea snail. Metamorphosis changes an embryonic larval organism adapted to a swimming existence in the water column, to an adult living on the sea fl oor with different locomotion, feeding and predator avoidance requirements. The transition between these two stages in the snail’s life cycle calls for a revolutionary morphological reorganisation that involves destroying parts of the larval morphology and building adult ones. Early indications of a veliger being ready for metamorphosis are that the mucus glands in the front part of the foot undergo accelerated growth, and that the foot grows correspondingly; the foot is preparing to take over the locomotory function. A veliger ready for metamorphosis alights on the sea fl oor and crawls over it in searching movements, exploring for suitable environmental conditions on which to settle. The veliger might swim away, alight at another place and repeat its explor- atory crawling, and only when it alights on a suitable substrate will metamorphosis actually begin. Sometimes the stimulation necessary for metamorphosis are merely specifi c conditions of light and water current velocity, but usually initiation of this process requires the presence of complex chemical compounds that leak from organisms on which the adult feeds, such as fi lms of specifi c bacteria or specifi c 2.7 General Classifi cation 31

Table 2.1 Limpet (Patella Time in caerulea ) developmental Activity or situation hours timetable (ambient sea Fertilisation 0 water 15 °C). Adapted from Fretter and Graham (1962 ) Trochophore larva begins swimming 8 A veliger larva develops with a shell 15 Operculum present 30 Torsion of visceral mass 40 Metamorphosis to a miniature adult 170 (7 days)

groups of algae or adult prey. In snail species living in colonies, chemical signals from individuals of the same species that have already settled may stimulate the planktonic veliger to settle nearby and join the colony. Upon ﬁ nding conditions suitable for settlement, the veliger stops crawling and remains stationary with spread- out sails. The sails are lost: their cilia begin beating out of synchrony, and their cells detach themselves from each other, swallowed by the metamorphosing veliger. Thus, for the ﬁ rst post-embryonic meal in its life the sea snail eats – itself. Other cells of the sail that are not swallowed and digested are incorporated into the head. It takes only 10–20 min for a sail to dismantle and be eaten or absorbed. The timetable for the entire embryonic process from fertilisation to metamorphosis depends mainly on the snail species and on the environmental water temperature. The timetable for a limpet (Patella caerulea ) at a temperature of 15 °C is presented in Table 2.1 . Metamorphosis ability lasts only a for a limited time and the veliger dies if it fails to metamorphose during this period. Having metamorphosed to a miniature adult, a sea snail may continue shell growth in either of two ways. The shell may continue to grow at an unequal rate at different sides of its aperture, coiling around itself as it did in its veliger phase, thus forming an adult coiled shell. Alternatively, it may change the embryonic pattern of coiling growth, and grow at an equal rate all around the shell aperture, thus forming an adult cone-shaped shell, with a tiny slightly coiled protoconch riding its top. Later on, during additional growth, such a cone-shaped snail might leave its embryonic whorls and dwell entirely in its newly formed cone, sealing off the new shell from the embryonic one by a calcareous partition.

2.7 General Classiﬁ cation

Moving from embryonic development into the dimension of evolutionary time, it is diffi cult to demonstrate that any fossil is a snail as we cannot directly observe torsion in fossils. Therefore, there are several views as to the fi rst appearance of snails in the fossil record. According to one view, fossil snails can be recognised in the early Cambrian (540–530 million years ago) with eight groups appearing in the 32 2 What Is a Snail? fossil record almost simultaneously. The most primitive of these snails had a simple, cap-shaped shell with a more-or-less central apex; in the morphologically more advanced forms, the shells had sinuses, grooves, buttresses or tubes. Some of these Cambrian groups also had spirally coiled shells and the most advanced coiled groups developed asymmetrical, spirally-descending shells. These early groups dwelt mostly in the shelter provided by rocks, stones, caves, crevices and so on, rather than on the open reefs or upon open rocks of that era; some, however, inhab- ited soft sea fl oor environments. Since those very early days of the Cambrian, sea snails have undergone an extraordinarily wide adaptive radiation. Much of our interest lies in seeing how the original morphology has been changed and modifi ed to permit different ways of life. Before presenting the general classifi cation of sea snails, this is the place for a very brief presentation of classic versus modern classifi cation methods, as concerns the Animal Kingdom. In the classic ‘formal’ classifi cation there are seven ranks: Kingdom, Phylum, Class, Order, Family, Genus and Species. Every group of animals is classifi ed into this hierarchy in which the ranks are nested one inside another: a species must belong to a genus, a genus must belong to a family, a family to an order, and so on. Beyond these seven compulsory ranks many zoologists, if they feel there is a reason to do so, may add as many intermediate ranks as they feel are necessary. Thus there may be a super-order, sub-order, infra-order, sub-genus and so on. Accordingly, a highly diversifi ed group may require use of the rank super-order whereas another, less diversifi ed group in the same class need not use this rank. Above the level of species, whether a particular group should be given rank of super-family or sub-order or order, is a matter of personal decision. In modern classifi cation the approach is completely different. Each group of animals has a sister-group, thus a species [a ] has a sister-group [b ], the combined group [ a + b ] has a sister-group [c ], the even-more combined group [a + b + c ] has a sister- group [ d ] and so on. Recent classifi cation is undoubtedly more true to the evolutionary dynamics of the evolutionary splitting off of groups from stem groups. It is, however, so very detailed and lengthy, consists of so very many ranks and steps, that one is easily lost in an almost infi nity of subgroups within sub-groups, far too cumbersome for an understanding of the natural history of sea snails. Therefore this book uses the classic rather than the modern system of classifi cation. Table 2.2 presents the general classifi cation of snail orders and super-orders mentioned in this book, and the following chapters present them in that order.

Table 2.2 The major groups of the class Gastropoda (snails) Class Gastropoda Snails Order Patellogastropoda Limpets Order Vetigastropoda Brush-snails (top shells, abalones) Order Neritimorpha Nerites Order Caenogastropoda Advanced-snails (winkle, cowries, cones) Super-order Opisthobranchia Sea slugs and relatives Super-order Pulmonata Pulmonates (land snails) Bibliography 33

Bibliography

Aktipis SW, Giribet G, Lindberg DR, Ponder WF (2008) Gastropoda: an overview and analysis. In: Ponder WF, Lindberg DR (eds) Phylogeny and evolution of the mollusca. University of California Press, Berkeley, pp 201–237 Fretter V, Graham A (1962) British prosobranch molluscs. Ray Society, London Frýda J, Nützel A, Wagner P (2008) Paleozoic gastropoda. In: Ponder WF, Lindberg DR (eds) Phylogeny and evolution of the mollusca. University of California Press, Berkeley, pp 239–270 Lindberg DR (2008) Patellogastropoda, Neritimorpha, and Cocculinoidea: the low-diversity gastropod clades. In: Ponder WF, Lindberg DR (eds) Phylogeny and evolution of the mollusca. University of California Press, Berkeley, pp 271–296 Parkhaev PY (2008) The early Cambrian radiation of mollusca. In: Ponder WF, Lindberg DR (eds) Phylogeny and evolution of the mollusca. University of California Press, Berkeley, pp 33–70 Ponder WF, Lindberg DR (eds) (2008) Phylogeny and evolution of the mollusca. University of California Press, Berkeley Raup DM (1962) Computer as aid in describing form in gastropod shells. Science 138:150–152 Vermeij GJ (1993) A natural history of shells. Princeton University Press, Princeton Yonge CM, Thompson TE (1976) Living marine molluscs. Collins, London Part II Primitive Sea Snails

Chapter 3 Patellogastropoda: Limpets

Abstract Limpets share many characteristics with primitive mollusc groups beyond gastropods, including shell micro-structure, morphology of the radula and eyes opening directly into the sea. Their shell is low, conical and with a broad aperture; vision is poor, but they have circumferential perception of their environment through sensory tentacles around the margin of the mantle. Limpets usually colonise intertidal wave-beaten rocky shores, to which they cling by a powerful muscle, by sticky mucus and, in some, by dissolving the rock and forming a pit (‘home scar’); a grazing limpet homes to its scar, in which predation and desiccation are reduced. Some intertidal limpets survive a 60 % loss of the water content in their body. Iron-oxide plated radular teeth remove hardened algal fi lms from rocks. Some limpets are generalist grazers, others feed on kelp; some farm gardens of red or brown algae from which they expel intruders and weed out other algae; in some, sticky mucous trails trap algae and stimulate algal growth so limpets retracing their trails capitalise on food-enhancing mucus. Primitive limpets respire through a gill, others through a cordon of fl aps hanging from the mantle around the foot and head. During mating, gonads swell to half the body weight. Many limpets are sequential hermaphrodites: males when young and females later. The externally fertilised egg fl oats in the sea, a trochophore hatches, becomes a veliger and eventually metamorphoses.

Keywords Limpet barnacles • Limpet feeding • Limpet gardening • Limpet home scar • Limpet locomotion • Limpet mucus • Limpet reproduction • Limpet respiration • Limpet territoriality • Patellogastropoda

Limpets (Patellogastropoda, Fig. 3.1 ) have a symmetrical shell that is low, conical, with a broad aperture, a forwardly-directed apex (Fig. 3.1 ) and in general somewhat resembling a kneecap (hence their scientiﬁ c name ‘patella’). The interior side of the shell bears a horseshoe-shaped muscle scar, open at the front. Limpets are further characterised by a large, wide and very powerful foot, and the absence of an operculum. Their anatomy suggests that limpets are the most primitive of living sea snails. For example, the eyes, at the base of the paired tentacles of the head, are merely shallow pits in which there are cells of one type only, both sensitive to light and

Fig. 3.1 Patella aspera (4 cm), from the eastern Mediterranean

Fig. 3.2 Eye of a limpet

containing black pigment granules (Fig. 3.2 ). The micro-structure of the shell (it contains a foliated layer) and of the radula are primitive in that they occur, beyond limpets, also in other primitive mollusc groups. We are fortunate in that we know the natural history of limpets more than that of most other sea snail groups. Their vision is poor, but limpets perceive their surrounding environment through other organs. The sensory organs on the mantle become very important since the head barely protrudes beyond the shell margins, by no more than the tentacle tips. The whole margin of the mantle is in equally close contact with the environment: the whole margin bears a series of small tentacles that can be withdrawn each into its sheath and readily extended, each one independently (Fig. 3.3). Some of these mantle tentacles are long, and are in continuous circular motion when extended in the water; others are shorter and tend to be held near the substrate or even touching it. The tip of each tentacle bears a crown of long cilia and its shaft bears tufts of short ones. In general, the mantle tentacles are sensitive to both tactile and chemical stimulation and also, to some extent, light. Limpets thus 3 Patellogastropoda: Limpets 39

Fig. 3.3 Patella : view from beneath with cordon of respiratory mantle ﬂ aps

have circumferential perception of the environment, by sight in front and by touch and chemical reaction in other directions. Many limpets are territorial and when approached by other individuals of their species, they extend their tentacles before attempting to remove the intruder. Limpets usually colonise intertidal or shallow subtidal wave-beaten rocky shores from which most other snails are excluded, and their defence against their harsh surroundings is achieved by a combination of a low broad silhouette with a strong foot. Their fl attened, conical shells are well shaped to protect them from being swept away by the waves. As another adaptation to life in the wave-crash zone, limpets cling to the substrate aided by their very powerful horse-shoe-shaped shell muscle, inserting on their shell and leading into their foot (Sect. 2.2 ). It is formed by the fusion, during larval development, of two shell muscles, one from either side. A limpet’s foot only pulls the shell down over the body rather than also withdrawing into the shell, as most other sea snails do. At the same time, they fi rmly clamp onto the rock with their large sole. This powerful grip on the rock is a limpet’s main defence during danger, because it cannot withdraw into its shallow shell. Such pulling down of the shell also keeps water inside the shell during low tide, to enable aquatic breathing through the gills. If the shell rim were not fi rmly and precisely attached to the rock beneath it, water would leak out. When not active, closure from the environment is gained by pulling the shell against the rocky substratum; during activity the body hardly extends beyond the shell. 40 3 Patellogastropoda: Limpets

3.1 Holding on, Moving About and Resisting Desiccation

The limpet’s way of life emphasises protection at the expense of mobility – they have an outstanding ability to adhere to the rocky substrates they usually live on. This strong adhesion is facilitated by sticky mucus secreted from the sole of the foot in a thin layer only a few microns thick. In the previous chapter (Sect. 2.2) the function of mucus in sea snail locomotion was briefl y introduced; here, its functions in adhesion and homing are presented. Strong adherence to the substrate is of prime importance because once overturned, whether by a strong breaking wave or by a predator, a limpet can never succeed in turning upright again. Their force of adhesion may reach fi ve kilograms per square centimetre, and the overall total force necessary for detachment may approach 100 kg. Strong adhesion also stabilises the limpet when contracting its shell muscles and pulling the shell down over itself. In general, the force of adhesion is a function of the surface area of contact and the surface tension of the adhesive fl uid. Any increase in the limpet’s foot surface area increases adhesion, and limpets have a very large foot sole relative to their body size. On the whole, the tenacity of limpets on the move is only 25–35 % of that when stationary, because when roaming only half of their foot is in contact with the substrate. The adhesive mucus consists of a cocktail of up to six different types of mucus produced by different cells scattered over the sole. Mucus qualities and quantities vary within limpet species, within an individual’s biological state and with variations in the environment. The mucus secreted by an actively moving limpet differs from that secreted by a stationary individual. The protein content of trail mucus may be only 6 % that of the mucus produced while stationary; and the protein content of a stationary snail’s mucus increases the longer the animal remains immobile. Mucus production varies also with the micro- topography of the substratum, with limpets laying more mucus on rough surfaces to fi ll pits and crevices than on smooth surfaces. Hence, crawling over rough surfaces requires the allotment of more energy to produce mucus. In addition to surface area of contact and the surface tension of the adhesive fl uid, other factors are also involved in determining the force of adhesion. One of these may well be muscular tension, as suggested by the fact that if limpets are caught ‘unawares’ they are comparatively easy to dislodge. Different limpet species seem to have evolved an ‘either-or’ policy: those with high tenacity have very low mobility while highly mobile species attach weakly. Seasonal changes in temperature and activity may also require changes in the relative components of mucus and in its quantity, because when temperatures are lower, muscular tonus decreases, the foot becomes more fl exible and tenacity declines. Humidity is also of importance. Patella vulgata , from the north-eastern Atlantic, secretes the maximal quantity of mucus in air with 100 % relative humidity, but only 40 % of its maximal quantity is secreted in air of 70 % relative humidity. This is signifi cant for the natural history of limpets, because in dry air the reduced secretion of mucus sets limits to the distance they are able to forage. The 3.1 Holding on, Moving About and Resisting Desiccation 41 quality of limpets’ mucus changes also during the mating season. It may then contain less carbonates and proteins because the limpet’s allocation of energy changes, from mucus production for adhesion and locomotion to gamete production and reproduction. Mucus production is costly and it is a dominant parameter in a limpet’s energy budget: it spends a quarter of the energy absorbed from its food on mucus secretion. The expense of producing the amount of mucus required for a mucus trail can be reduced by crawling over existing mucus trails, because mucus trails both stabilise the substratum and produce a smoother surface over which to move. In comparison, winkles, a group of advanced snails for which data are available, produced only 27 % of the mucus laid by marker snails when tracking over fresh trails laid by other individuals (Sect. 7.6). Most energy saving occurs when following recently laid trails that are little weathered. This saving of approximately 70 % of the energy costs on mucus and approximately 20 % of their total energy cost is considerable in an animal that expends much energy on mucus production. Additional fi rm attachment is gained, in some limpet species, by dissolving the rock and forming a pit that precisely conforms to the shape of its shell. Mucous glands in the foot contain muco-polysaccharides and the mantle periphery contains carbonic anhydrase, both capable of chemically etching and softening limestone rock. The limpet’s radula scrapes away at the softened rock until a shallow pit is formed, into which the margins of the shell fi t more precisely than elsewhere on the rock. This pit is called a ‘home scar’, and the limpet attaches more fi rmly to the rock when in it. An individual leaving its scar to graze over the rock eventually (within hours) homes back to its scar. Very little is known about the full range of mechanisms that enable scar homing. In some cases limpet homing mechanisms are based on their outgoing mucus trails. An individual leaving its scar to graze on the rock may track its way back by following its own outward paths. It does not always move precisely within these trails, but it tends to remain close to them. An individual can recognise its own trails if its path crosses those of other individuals of the same species, but it sticks to his own path. However, if an individual is transplanted well away from its scar, it will follow the mucus trails of other individuals of its species until it fi nds a vacant scar, which it will then occupy. Though homing to a fi xed scar on the rock surface is well known in limpets, there are considerable differences in homing behaviour among different limpet species, and even among individuals of the same species. Factors infl uencing homing behaviour include rock texture, rock stability, food availability and the extent of desiccation. In general, large individuals within a species home more readily than small individuals, and individuals of the upper parts of the shore home more accurately than those of lower shores. There are, however, low-shore and even subtidal species which have well-developed scars and homing behaviour. The limpet Cellana (Fig. 3.4 ) prepares no home scars, but there are resting sites, to which the individual returns from its journeys. On an evolutionary scale, once home scar formation and homing behaviour were included in the behavioural repertoire of a limpet, the way opened for an individual to take possession of the area surrounding the scar and to defend it from other 42 3 Patellogastropoda: Limpets

Fig. 3.4 Cellana rota (4 cm), ventral surface, Red Sea

individuals which may invade its territory. Territorial defence does indeed occur in some limpet species: the territory owner attacks an invader by pushing it, strongly butting into it with its shell or by stooping over the invader and then pulling its shell forcibly down over the invader’s mantle margins. Invasions and territorial attacks occur mainly during high tide when the limpets are under water, and usually the invader retreats. Another main function of the home scar is reducing desiccation. A limpet that leaves its scar to graze over the rock must return to this same scar, which precisely meets its size and shape, to avoid desiccation. Though unlikely to have a single function, this behaviour, also reduces desiccation. Notoacmaea petterdi , an extreme upper shore Australian species, has a very rigid homing behaviour, and limpets that were transplanted away from their scars in experiments suffered 93 % mortality; in comparison, controls that were lifted up and then replaced on their scars suffered only 17 % mortality. Living at the interface between sea and land where they are subject to repetitive wetting and drying during each tidal cycle, intertidal limpets are subject to stressful environmental conditions such as desiccation and extreme temperatures. A combination of these may have very severe consequences. Limpets are subject to unusually stressful desiccating conditions following successive days of calm combined with exceptionally hot weather, and mass mortality then occurs. Many limpets respond to hot dry conditions by moving down the shore, sometimes even abandon- ing their home scars, and retreating to damp crevices; conversely, during storms that wet the shore for longer than normal periods, they move upward. On a seasonal scale, some limpet species move progressively down the shore during summer, followed by an upward migration in winter. As one might expect, high-shore species have greater tolerance to desiccation stress, and their rate of water loss on any single shore may be only approximately one tenth of that of a lower-shore species. Different species survive different levels of desiccation stress, and whereas some 3.2 Respiration 43 can survive only a 30 % loss of the water content in their body, other species can survive up to 60 % water loss. Size has a strong infl uence on tolerance to desiccation in numerous limpet species. Patella granularis is a South African species that migrates up the shore; larger animals occur higher up the shore, have a higher tolerance to desiccation, but loose water at a proportionally slower rate. This is in accordance with the general rule that an increase in size results in a decrease in surface area relative to volume. Larger bodies loose water more slowly since water loss by evaporation depends on the surface area, while water content of a body depends on its volume. Shell shape also infl uences the rate of water loss. Patella vulgata from upper shore levels of European coasts have taller, more domed shells, because in dry desiccating habitats the limpet clamps down more tightly, pulling its mantle further in. If the mantle glands deposit additional shell while in this position, shell circumfer- ence will be reduced and the shell will form a yet higher dome. Desiccation clearly limits the upper zone on the shore of some limpet species, but as they dwell at the intertidal, limpets must cope also with high and very variable temperatures. It is of course diffi cult to separate the effects of desiccation from those of heat stress, as the two often act together, and heat may lower resistance to desiccation. Having said that, some limpet species can survive air temperatures of 42 °C. The body temperature range of an individual Patella vulgata on a single day may vary from 10 to 33 °C. Protection against extreme cold is more diffi cult. The Antarctic Nacella concinna produces a thick mucous sheath when trapped beneath ice. This lowers the limpet’s inter-cellular fl uid content and hinders the propagation of ice through the tissues.

3.2 Respiration

Respiratory mechanisms among limpets are diverse. Acmaea, a primitive limpet genus, possesses a single left gill that extends into the mantle cavity above the head and which, when fully extended, may project beyond the margin of the shell. This is the main respiratory organ, but in addition the mantle edge has a fi ne capillary network also capable of allowing oxygen exchange, as the blood, fl owing through this network, counters the currents created by local cilia. In upper shore species of Acmaea , the feather-like gill functions mainly in aquatic respiration and is relatively small; the blood vessels circumventing the mantle margins function in aerial respiration, and are consequently more important than in low-shore species. In the more advanced genus Patella , this gill is replaced by a cordon of thin- walled ciliated fl aps of tissue which, in association with a conspicuous encircling blood vessel, hang down from the roof of the mantle cavity in a groove between the foot and the mantle margin, completely surrounding both the foot and the head (Fig. 3.3 ). These fl aps function as respiratory organs. When the shell margins are raised, dense cilia on their outer margin create gentle sea water currents that run against the blood fl ow through the fl aps, and between these counter-currents the process of oxygen absorption and carbon-dioxide release take place. Lottia (Fig. 3.5 ) 44 3 Patellogastropoda: Limpets

Fig. 3.5 Lottia gigantea (6 cm), California

is intermediate between Acmaea and Patella as it has both a gill as in Acmaea and a cordon of secondary gills as in Patella. Lepeta, a deep water limpet (down to 1,100 m) with much reduced mantle tentacles (and eyes lacking pigment) has no gills whatsoever, and respiration is carried out through the body surface. Limpets must cope also with a lack of oxygen. Firm attachment to the rocky substratum requires applying considerable energy to the shell muscle that under normal conditions would be derived from aerial oxygen. However, limpet attachment may be so hermetic, especially when in a home scar, that the snail might run out of air. To withstand such prolonged periods of anoxia, some limpets have impressive anaerobic capabilities. Glycogen is the main fuel oxidised in the foot muscle of Patella and it serves as the main source for energy production (ATP); accordingly the foot has a complete sequence of glycolytic enzymes.

3.3 Feeding

Limpets are grazers. Their radula is empowered by strong muscles and it has a reduced number of enlarged strong, pointed teeth per row. These allow excavation of the surface they feed on, removing the superfi cial layers of even the most resistant algae and even scratching the surface of the rock. A few large, strong muscles insert onto the radula ribbon and upon contraction they extend the radula beyond the mouth like a rope over a pulley and apply it to the substratum, bulldozing into hardened algal fi lms and sometimes dislodging also sessile animals such as small hydroids, barnacles, bryozoans, and polychaetes. As the muscles are strong, 3.3 Feeding 45 considerable power is applied by each tooth onto the substrate. These are the only muscles in the body to be supplied with myoglobin, a molecule containing atoms of iron. Iron binds oxygen more effi ciently than copper (which is present in haemocyanin) so when the muscle is active it can exploit much more oxygen in a shorter time. Each row on the radula consists of only approximately a dozen teeth. The central tooth is reduced or absent, and it is fl anked by three lateral and three marginal teeth on either of its sides (3.3.1.3.3 or 3.3.0.3.3). While the marginal teeth are weak, the lateral teeth are formidable structures, giving in effect six strong teeth per row. Each of these lateral teeth is short, and its broad base enables a broad attachment to the fl exible underlying radular ribbon. Several rows of teeth are in contact with the substratum during each stroke of the radula, so a limpet is capable of excavating rock and removing micro-fl ora and fauna growing in the crevices or even embedded in the rock surface. Additionally the body of each tooth is made of protein fi bres and chitin. Hardness of the lateral teeth is also enhanced by fi bres of silicate (SiO2 ) embedded into them and furthermore, they are plated on their outside with iron oxide in the form of goethite (Fe2 O3 . H2 O). Such a tooth is as hard as a human tooth. In technical terms, such an iron-plated tooth measures 5 units on the Mohs scale of mineral hardness, while the teeth of other sea snails achieve only 2 units in strength. These iron-plated teeth are also harder than some types of rock. Moreover, the arrangement of the silicate fi bres and distribution of the iron oxide in each tooth is such that the hardness of the part leading in the cutting direction has twice as much iron oxide, and is approximately twice as hard as the trailing part. Therefore the trailing edge of each tooth erodes more quickly than the leading edge, and the tooth is self-sharpening. Many limpet species are generalist herbivorous grazers feeding on the organic fi lm covering rocks. These consist of algae (both spores and sporelings) and diatoms entwined and embedded in a medley of rotting organic material mixed with a rich variety of bacteria. Limpet grazing may be so intensive as to regulate the algal abundance on the shore. In a classical study in which all Patella vulgata were removed from a 10 × 110 m stretch of shore (on the Isle of Man, United Kingdom, in 1946), this transect was covered with a dense forest of green and brown algae within just 2 months. The limpets in adjacent areas were left untouched, and the algae in these areas remained sparse and patchy because of the continual grazing action of these organisms. Further studies revealed that limpet grazing is the most infl uential in regulating algal abundance in the middle and upper intertidal shores, whereas in the lower intertidal it does not overcome the high rates of algal settlement and growth. A signifi cant number of limpet species live and feed on very large algae. Patella pellucida of the north-eastern Atlantic coasts (Fig. 3.6 ) lives primarily on kelp ( Laminaria ) on the lower shore down to approximately 30 m. Its veligers settle and metamorphose on the algal frond where they feed on the kelp tissue, leaving small depressions in the frond. As the limpets grow, they migrate down the seaweed stipe towards the holdfast, where they establish themselves by excavating a depression. This can weaken the holdfast, eventually resulting in the seaweed being dislodged by storms. Such seaweed is often washed ashore with the limpets still in place. 46 3 Patellogastropoda: Limpets

Fig. 3.6 Patella pellucida (2 cm), north-eastern Atlantic

Patella argenvillei and Patella granatina of South Africa feed on micro- and macro-algae settling on the rocks but also on deeper water kelps (Ecklonia maxima and Laminaria pallida ), a common source of food for these two sea snail species. Indeed, kelp makes up more than 50 % of the total diet of each species. Patella granatina feeds on drifting kelp and seaweed debris that it captures while underwater, during incoming and outgoing tides: experimental exclusion of kelp from the limpet’s diet resulted in both a reduction of body mass and increased mortality. Patella argenvillei feeds on the fronds of attached kelp plants that it actively prunes during the tide. Subtidal production of kelp fronds thus subsidises populations of both these intertidal limpet species and is vital to the maintenance of their remarkably high biomasses. Patella compressa of South Africa is another settler on the fronds of the kelp Ecklonia maxima. As it ages, the limpet migrates down the stipe, and its shell becomes elongate to fi t the stipe. Its radular teeth are fl at and wide, and not pointed like those of most limpets, so it removes only the superfi cial epithelial layers of the alga. Adult P. compressa are territorial and act aggressively if they encounter another limpet, and so only solitary adults occur on a single stipe, and their grazing is never suffi cient to weaken it. Other specialised associations between grazing limpets and algae occur in territorial limpets, such as Scutellastra cochlear and Patella longicosta , both again from South Africa. These close relationships have such important consequences for both limpets and plants that they are presented here in some detail. Scutellastra cochlear (Fig. 3.7 , formerly Patella cochlear ) of South Africa is mildly territorial. It occupies a narrow zone at the bottom of the shore where it occurs in very crowded populations, up to 1,700 individuals per square metre. Each limpet is surrounded by a narrow fringe of fi ne red algae, mainly Herposiphonia 3.3 Feeding 47

Fig. 3.7 Scutellastra cochlear (5 cm), South Africa. Three adults on a rock (orange ), each surrounded by a fringing algal garden. Four juveniles ride these adults, of which three also have fringing algal gardens, on these adult shells heringii and Gelidium mictropterum, from which it excludes all other herbivores and most sea-weeds. This fringing garden is defended by the limpet which depends on and farms it for food. The limpet feeds by rotating on its scar and continually cropping the garden. The production of the red algae in these gardens closely matches the energy requirements of the limpet. Thus the very high densities of S. cochlear depend upon their relationship with highly productive but cultivated gardens of red algae. The Scutellastra cochlear populations are usually so very crowded that settling veligers survive only if they alight on shells of the territorial, garden- possessing individuals. Many juveniles survive by forming fringing gardens of their own on the backs of the host shell, and feeding on those. With growth, however, a point is reached where the juveniles become too large to occupy their host shells, and they must descend to the rock, which is covered by the encrusting coralline red alga Spongites yendoi. Grown juveniles will not establish their own gardens on the rock face unless sufﬁ cient space is available amongst the established adults, a rare situation in dense populations. Death of an adult leads to the immediate occu- pation of the vacant scar by one of the juveniles. There is another side to this coin: the red algae forming the garden actually depend on the limpets for their healthy maintenance. Removal of a limpet results in an initial ﬂ ourishing of the garden but the algae subsequently either die back and are 48 3 Patellogastropoda: Limpets

Fig. 3.8 Patella longicostata (6 cm), South Africa, on its Ralfsia garden grazed away by other invertebrates to local extinction, or become overgrown within 1–2 months. Consequently, one species of the red algae, Gelidium mictropterum , is found on the shore practically only when serving as limpet gardens. Furthermore, Scutellastra cochlear actively enhances the productivity of its algal gardens through the regeneration of limiting nutrients. During low-tide exposure the limpet produces nitrogenous excretions in the form of urea and ammonium, and these accumulate under its shell in close contact with the surrounding algal garden. The average amount of ammonium that a limpet excretes is similar to the amount of nitrogen the algal garden requires for its growth. Algal uptake rates of ammonium from these limpet excretions supply 30 % of the algal garden’s daily nitrogen growth requirements. It was once believed that the production and energy content of encrusting coralline alga is so low that it cannot alone support the energy needs of Scutellastra cochlear. Recent studies have shown, however, that the encrusting alga Spongites yendoi has an organic content broadly similar to that of the garden alga Gelidium micropterum ; and that the limpet fi nds in it an important substitute food source. It may perhaps be that the coralline and the garden alga fulfi ll different requirements, and that limpets with gardens maintain a mixed diet of algae. Patella longicosta (Fig. 3.8 ), also of South Africa is a highly territorial rock- dwelling limpet which feeds on the encrusting brown alga Ralfsia verrucosa . It defends its Ralfsia garden by expelling any intruding limpet, whether of its own or of any other species, and it weeds out all other algae threatening to overgrow its food plant. Patella longicosta does not overgraze its Ralfsia to elimination: it merely cuts spaced-out paths through its garden. Ralfsia grows more rapidly around its edges, so by cutting these paths the limpet creates more edges and increases the 3.3 Feeding 49 productivity of its algal garden, almost doubling the alga’s natural growth rate. The energy budget of P. longicosta closely coincides with the enhanced production rate of Ralfsia , and adult P. longicosta are found exclusively in association with R. verrucosa on which they feed. This limpet has a complex life cycle. Its juveniles are found on shells of other snails, such as the top shell Oxystyle , where they feed on algal encrustations. When the limpets reach a size at which the top shells are too small to support them, they leave and migrate onto the rock. For a period they feed only on the encrusting coralline Lithophyllum , they grow only very slowly, their body weight falls, and they do not mature sexually. During this period they await the death of a nearby territorial individual. When, eventually, an adult limpet dies, its vacated scar and Ralfsia garden are almost immediately taken over by a nearby juvenile. Only one juvenile becomes established in each vacated garden, which it then maintains and in which it now matures. The habitat shift that P. longicosta undergoes, from small, young juveniles occupying top shells, via advanced juveniles barely feeding on Lithophyllum , to sexually mature adults occupying Ralfsia gardens, effectively separates juvenile and adult habitats. In part the shift is forced by a scarcity of the preferred food plant, Ralfsia , outside the territorially defended areas. Looking at this limpet-alga link from its other end, Ralfsia occurs primarily (but not exclusively) in Patella longicosta territories. It benefi ts directly from the presence of P. longicosta, as the limpet’s grazing pattern creates secondary sites for its growth; accordingly, algal productivity is 30 % higher in the presence of the limpet than in its absence. Ralfsia additionally benefi ts from the territorial behaviour of this limpet because it is a poor competitor against other algae. If a limpet is removed from a Ralfsia fi eld and juveniles are experimentally prevented from entering it, other nearby groups of algae, such as the foliose green alga Ulva , rapidly overgrow the Ralfsia . Another possible outcome is that other grazing limpet species move in, such as Patella oculus and, having access to the Ralfsia , eliminate the garden by destructive over-grazing. This limpet-alga link is thus interdependent, and the limpet’s behaviour is tuned to maintaining its food plant. This explains why more than 95 % of the intertidal Ralfsia occurs in P. longicosta fi elds. The mucous trails secreted by certain intertidal limpets serve as adhesive traps for the micro-algae which are their primary food resources. The mucous trails of two solitary homing limpets, Lottia gigantea (Fig. 3.5 ) and Collisella scabra , occurring on north-eastern Pacifi c coastlines, also stimulate the growth of micro-algae, apparently through the various organic contents their faeces contain. Homing species have restricted home ranges and retrace their own mucous trails, capitalising on the production of food-enhancing mucus. One might perhaps expect limpet grazing to peak mainly in the evening when it is less exposed to desiccation and to sharp-eyed diurnal predators and when algae nutritional value is higher after a day of photosynthetic activity. In reality, however, a single limpet will carry out grazing expeditions during various parts of the day and night, related to the tidal cycle, climate, position of the individual in upper or lower parts of the shore, the spatial position of the rock (whether horizontal or vertical), the time of day and the physiological condition of the individual. 50 3 Patellogastropoda: Limpets

3.4 Reproduction

Limpet’s gonads swell in the mating season to up to half their body weight. Most individuals are males when young and become females later, the change of sex occurring between mating seasons. However, besides sex-changers (for whom the scientiﬁ c term is ‘consecutive hermaphrodites’) there are also individual limpets that do not change sex and remain males all their lives. The majority of limpets practice external fertilisation, the spawned female ovules remaining viable in the sea for 12–15 h after release. Gamete spawning is remarkably synchronised in some species, and 80 % of the population may spawn over a 2-day period. Also, the males and females in some species come together in pairs during spawning, and the mature snails of Nacella concinna , an Antarctic species, form temporary ‘stacks’ of two to six animals (males and females), that last only for the duration of the spawning. The 0.1 mm fertilised eggs ﬂ oat in the sea water column, a tiny trochophore hatches from each and gradually develops into a veliger. In some limpet groups the transition from trochophore to veliger is completed within the egg’s envelopes so that a veliger hatches directly. Within 5–6 days the embryonic shell is formed, slightly coiled, the operculum develops and torsion takes place. Approximately a fortnight after fertilisation, the veligers settle on the shore and metamorphose into adult form, loosing the operculum during this process. A young limpet which has just settled has a size of approximately 0.2 mm and hides in damp crevices. With each rising tide it produces and secretes a thin shell layer, the thickness depending upon nutrition and environmental temperature. Some two and a half months after metamorphosing the embryonic shell falls off and is replaced by a calcareous partition secreted across the base of the apex. The growth rate of individuals varies so considerably from one year to the next and from one site to the next that one cannot conclude, from shell size alone, the limpet’s age. Some individuals may live up to 17 years. A few limpet species have evolved parental brood protection, their eggs being retained in the mantle cavity where they are fertilised and develop into crawl-away young.

3.5 Predation and Competition

Limpets fall prey to a wide range of animals including starfi sh, crayfi sh, crabs, predatory snails, birds and, among fi shes, wrasse and gobies. Responses to slow invertebrate predators differ from those to rapidly-moving vertebrate predators (and perhaps also crabs). Many limpets respond to the presence of slow-moving invertebrates by ‘running’ up the shore. Upon approach of a starfi sh or predatory snail, the limpet Cellana (Fig. 3.4 ) deserts its resting site and fl ees up the rock some 10–20 cm. Small individuals of Patella oculus (South Africa) have a typical running 3.5 Predation and Competition 51 response to starfi sh and predatory snails. However, large P. oculus limpets react quite differently: they are aggressive, lifting their shells and smashing them down onto the slow predator. While escape responses and counter-attack are quite effective against slow- moving invertebrate predators, other measures are required against large, mobile, visually-hunting predators. Avoidance of detection is one such anti-predator strategy. Many limpets are concealed in their natural environment, their colour merging with that of their background. Furthermore, some limpet species have individuals with several differently coloured shells within a single population at one site: dark shells may be found mainly on dark rock, whereas pale shells are found among lighter-coloured barnacles. The substratum may actually determine an individual limpet’s colour, which changes because the ingested algal pigments and other materials (such as calcium carbonate) vary between substrata. Accordingly, the ability to achieve cryptic colouration may be determined by the geographic distributions of algae on which the limpets feed, or the geological composition of the substrate, rather than by intrinsic characteristics of the limpets. Homing to a scar also reduces predation. Homing is traditionally regarded only as reducing desiccation, but it also occurs in constantly wet subtidal species so it must have another function. The limpet-eating fi sh Chorisochismus dentex of South Africa only attacks moving limpets that are away from their scars. Limpets that adhere strongly to the rock and fi t closely to their scars are seldom eaten, and they suffer a much lower rate of predation than those lacking a scar or roaming on the rock. Barnacles are not predators of limpets, but they pose diffi culties to limpet movement over rocks. The irregular surfaces created by barnacles prevent limpets from effectively ‘sealing’ to the substratum, with subsequent high mortality rates due to desiccation. Accordingly, small, young limpets may still shelter among barnacles to reduce desiccation stress but larger, older ones are at a disadvantage among barnacles and their growth is considerably reduced. The more barnacles on the shore the slower the growth rate of a limpet, the lower its weight and the smaller its gonads. This is the reason behind the many wars of attrition and battles of annihilation between limpets and barnacles. The limpet prevents barnacle settlement by feeding on the larvae that land on the rock from the plankton. It also up-roots, crushes and dislodges, with its bulldozer-like radula, every minute barnacle that succeeds to settle. Once a barnacle has been overlooked and succeeds to settle, it grows rapidly and upon reaching a certain refuge-size the limpet can no longer uproot it. Places with high mid-shore barnacle density compel limpets to migrate to the upper zones of the shore where there are fewer barnacles, but also less food. If limpets are removed from a shore, barnacles will settle on it and cover it within a brief period. Not all limpets have an antagonistic relationship with barnacles. Patelloida latistrigata of eastern Australia (Fig. 3.9 ), which co-occurs with Cellana , is found exclusively in the barnacle zone. Being a small limpet, Patelloida moves freely among barnacles, where it gains protection from desiccation and wave action. Cellana out-competes Patelloida for space on the rock, but because of the adverse 52 3 Patellogastropoda: Limpets

Fig. 3.9 Patelloida latistrigata (1 cm), Australia

effects barnacles have on Cellana , Patelloida has a refuge from such competition among the barnacles. Interactions between limpets and barnacles are thus intricate, and it is impossible to generalise about limpet-barnacle interactions.

3.6 Evolutionary Aspects and Classiﬁ cation

Rocky intertidal animals are poor candidates for the fossil record. Switching from the natural history of recent limpets to the long timescale of evolution, several sea snail groups with limpet-like shells ﬁ rst appeared during the Ordovician (approximately 450 million years ago) and Carboniferous (approximately 330 million years ago) but it is not quite clear whether these should be attributed to the Patellogastropoda. The lineage of recent Patellogastropoda is estimated to have originated no later than the Late Jurassic, some 146 million years ago. We do not know who the direct ancestors of these recent limpets were, or whether they had either a slightly coiled or a cone-shaped adult shell with a tiny protoconch riding on top. Today the limpet order Patellogastropoda includes some 40 genera classiﬁ ed into 3 sub-orders: the primitive Eoacmeoidea and the more advanced Patelloidea and Lottioidea. Limpets are primitive in that they share many characters with primitive mollusc groups beyond the gastropods. These include foliated shell micro-structure, the overall morphology of the radula, eyes that open directly into the sea water, and many other details concerning both their micro-anatomy and molecular structure. They are, however, not the only primitive group. Another group of primitive sea snails is the Vetigastropoda, presented in the following chapter. Bibliography 53

Bibliography

Branch GM (1985) Limpets: evolution and adaptation. In: Trueman ER, Clarke MR (eds) The mollusca, vol 10 evolution. Academic, New York, pp 187–220 Davies MS, Hawkins SJ (1998) Mucus from marine molluscs. Adv Mar Biol 34:1–71 Fretter V, Graham A (1962) British prosobranch molluscs. Ray Society, London Fretter V, Graham A, McLean JH (1981) The anatomy of the galapagos rift limpet, Neomphalus fretterae. Malacologia 21:337–361 Hickman CS (1988) Archaeogastropod evolution, phylogeny and systematics; a re-evaluation. Malacol Rev Suppl 4:17–34 Hodgson AN, Hawkins AJ, Cross RHM, Dower K (1987) Comparision of the pallial tentacles of seven species of South African patellid limpets. J Molluscan Stud 53:229–240 Lindberg DR (1988) The Patellogastropoda. Malacol Rev Suppl 4:35–63 Chapter 4 Vetigastropda: Brush Snails

Abstract The radula has many bristle-like teeth and brushes the rock to collect spores and detritus; some brush snails also fi lter-feed. The shell often consists of mother-of-pearl: fl at calcium crystals on top of each other, embedded in a thick matrix of protein. Shell colours are sometimes determined by diet, not by genetic control. Many sensory tentacles may rise from the upper part of the foot; they regenerate if nipped off by predators. Hydrothermal vent limpets (Lepetodriloidea) feed by grazing, fi lter-feeding and digesting bacteria accumulating at the tips of their gills; they have cap-like conical shells. A slit in the conical shells of keyhole limpets (Fissurelloidea), sometimes closed into a hole, enables exit of waste products that would otherwise contaminate the gills and senses of the head. In many brush snails the shell coils spirally, dictating asymmetric morphology in which the left muscle and right gill are reduced: abalones (Haliotidae), which graze in the lower intertidal and in which the slit closes into several holes; and side-slits (Pleurotomarioidea), which feed on sponge in the deep. Topshells (Trochoidea), the largest and most diverse of brush snail groups, have spiral shells without a slit, and a single gill; in some the operculum forms a calcareous plug; and in some the rear of the foot breaks off in response to disturbance by predators. Crysomallon (Neomphaloidea) of deep waters is odd among snails in that the operculum has changed into a series of iron scales.

Keywords Abalone • Fissurelloidea • Vetigastropod functional morphology • Vetigastropod reproduction • Keyhole limpet • Lepetodriloidea • Neomphaloidea • Pleurotomarioidea • Trochoidea • Vetigastropoda

4.1 Functional Morphology in Evolutionary Perspective

Some 500 million years ago, during the Cambrian-Ordovician, another group of sea snails appeared in the sea – the Vetigastropoda. They differ from limpets in major structural aspects of the radula, of the mantle and of the shell. Vetigastropods are equipped with a radula with very many teeth in which there are no silicon ﬁ bres and no iron oxide covers. Each row has many long, weak teeth, with one central tooth, usually ﬁ ve pairs of lateral ones and up to a hundred marginal teeth (100.5.1.5.100), (Fig. 4.1). The central and lateral teeth are the more robust ones whereas the marginal teeth are slender, delicate, very long, and with a

Fig. 4.1 A single row of brushing teeth in a vetigatsropod’s radula

very narrow base compared to their length, actually they are more like bristles than like teeth. As the bristle-like teeth are very long, any slight change in the radula ribbon causes considerable change in the upper part of the bristle. The brushing, sweeping operation of such a radula requires only a modest degree of power, but it enables close adjustment of the radula to the contours of the substratum being swept. Many muscles attach to the ribbon and enable slight and complex changes in it and in its position; most importantly, they enable bending along the long axis of the ribbon. It can be spread out and rolled in like a narrow but very tall scroll. Within the mouth cavity the radula is rolled up, and rests in a groove above its cartilage cushion. During feeding it is pushed outward, un-rolled and spread out, its teeth are erected, and as this happens the lateral and marginal teeth also rotate laterally. When pressed to the substratum the area swept by the un-rolled radula is thus increased, as compared to the non-rolling radula of limpets. Only one or two rows are in contact with the substratum at any instant, and in them the lateral and central teeth crop and rake, while the many marginal teeth maximise the thoroughness of the sweeping. In sweeping movements of the radula, food is collected into a small food groove beneath the cusp of each marginal tooth. The power stroke is produced as the radula is pulled backward, the teeth become prone again and the radula ribbon is once again rolled in like a scroll. As the marginal teeth are long and thin, the power produced by each tooth against the substrate is not considerable. The teeth gently sweep over the rock rather than bulldoze into organic ﬁ lms limpet-style, and the food of a typical vetigastropod consists of surface spores and detritus. The brushing, sweeping action of the long, thin, bristle-like teeth prompts me to suggest ‘brush snails’ (or perhaps ‘toothbrush- snails’) as a vernacular name for the Vetigastropoda. Another major difference between brush snails and limpets concerns the mantle cavity, which during veliger-stage torsion is brought to a position just above the head. As the exit openings of the alimentary and urinary systems are inside the mantle cavity, post-torsion morphology poses a problem: faeces and urine would now be excreted on both the gills and the head, with its sensitive sense organs. In primitive brush-snail groups such as keyhole limpets, Fissurelloidea, this sanitation problem has been solved by the local folding-in of the mantle margin (and of the shell it secretes) in the front midline of the mantle cavity, thereby forming a deep slit (Fig. 4.2 ). Corresponding to the slit in the mantle, a slit is formed also in the shell. Faeces and urine leave the snail through this slit without interfering with the functioning of the senses in the head. Both the anus and the kidneys open near the upper part of the slit, and faeces from the intestine and urine from the kidneys ﬂ ow out in the upward current of water. During mating, both ovules and sperm are spawned into the sea through the midline slit. In some groups the slit is closed into 4.1 Functional Morphology in Evolutionary Perspective 57

Fig. 4.2 The shell slit (partly in transparency)

a series of holes, thereby more effectively separating the inward from the outward respiratory current. The mantle cavity also contains the gills (in primitive ones, a pair). Water is drawn into the mantle space below the gills and fl ows upwards among the gill leaf- lets. This current, now rich in carbon dioxide, then leaves the mantle cavity and is discharged to the surrounding sea through the midline slit or holes. A major difference between brush snails and limpets concerns changes in the shell. Understanding them and the resulting necessary adaptations in the visceral mass requires indulging into some detail. As mentioned previously the embryonic shell of the veliger is at fi rst small and cap-like. Later, during growth, the shell may coil slightly but it remains low, allowing the veliger better manoeuvrability when swimming in the plankton than a long, cone-shaped shell. Brush snail larvae only form a protoconch of nearly one whorl or, rarely, slightly more. After metamorphosis, visceral hump and shell of many brush-snails continue coiling around as in its veliger phase, thus forming and growing into an adult coiled shell, now carried on the snail’s back (Fig. 4.3b ). In the evolution of most brush snails, the adult shell continues coiling around itself as in its embryonic phases (Fig. 4.3b ). An adult coiled shell may thus be an originally embryonic characteristic, dragged into adult morphology. The evolution of a coiled shell might perhaps be related to a smaller foot relative to the visceral hump, perhaps following some delicate shift from a predominantly muscle-based mode of movement to a more cilia-based mode, perhaps following a subtle shift away from wave beaten rocks to other habitats at some early stage in snail evolution. The large visceral hump might perhaps have coiled to improve its balance over the smaller foot, and the coiled hump would have secreted a coiled shell. Had the visceral lump remained a tall conical pile, it would have formed a shell shaped as a very high cone that would have been dragged along behind the body and would have been diffi cult to cope with, even in slight sea currents (Fig. 4.3a ). This coiling process was enabled thanks to simple differences in the growth rates around the margin of the mantle, where new shell is added: to form a limpet-like shell, an equal growth rate in all parts around the mantle margin is required. More rapid growth in one part of the mantle formed a shell that bends over, and coils in the direction opposite the site of rapid growth. The result is a shell tube coiled in one (vertical) plane that has a low silhouette, lowers the resistance to 58 4 Vetigastropda: Brush Snails

Fig. 4.3 Evolutionary trends in shell design. Circles represent transects in mantle margins, circle thickness represents the amount of shell matter secreted in a unit of time: ( a) uniform secretion rate, the resulting shell is conical; ( b) secretion rate increases on one side (here – front ), the resulting shell coils to opposite side, in one plane; (c ) secretion rate increases in two neighbouring sides (here – front and left ), the resulting shell coils to opposite sides in spiral manner; (d ) spiral shell balanced above the foot water during movement, and is therefore easier to move about. This situation of symmetrically coiled shells (Fig. 4.3b ) was found in the Bellerophontida, a fossil group of snails that fi rst appeared in the late Cambrian (500 million years ago) and became extinct 215 million years ago. Among recent snails, it is found in such familiar fresh water snails totally unrelated to the Vetigastropoda as Planorbis, Anisus and their allies. At a later, more advanced stage in the speculated evolution of the brush snails, the shell changed from vertically coiled to spirally coiled (Fig. 4.3c ). This change was made possible by yet another simple change in the growth rate along the mantle margins. In addition to rapid growth in one place, an even more rapid point of growth developed nearby – and the shell coiled in the opposite direction, in an asymmetrical manner, thereby forming a spirally coiled shell. Such a shell had an even lower silhouette than a vertically coiled one, and the sea snail’s movement was therefore even easier. In the descending spiral of the shell, the inner fl ank of each coil was partly wrapped around the outer fl ank of the previous one and thereby formed a central axis, the columella (Fig. 2.2 ). 4.1 Functional Morphology in Evolutionary Perspective 59

However, the sea snail was now left with problems of balance. The spiral shape shifted the centre of the shell’s symmetry to the side (usually to the right). In this situation the shell’s centre of gravity was on the right of the foot rather than just above it and the snail, lacking balance, was liable to topple over. A fully-balanced posture was regained by heaving the shell apex from its position on the right of the snail to a more posterior, rear position above the midline of the foot (Fig. 4.3d ). In its adjusted position the shell was again above the foot, balanced more-or-less symmetrically. The shell’s height formed an axis paralleling (when seen from above) the long axis of the foot, and its shell aperture was positioned (more or less) parallel to the substratum. The evolution of the asymmetric spiral shell dictated an asymmetric rearrange- ment of the primitive pair of shell muscles responsible for withdrawing the foot into the shell. As the spiral shell inclined to the right, the left muscle usually became reduced and eventually was lost through evolution and only the right one remained. At one end this muscle branches out and inserts into the foot and at its other end it reaches out beyond the wall of the body and inserts on the columella of the shell (hence it is sometimes named the ‘columellar muscle’). At the site where the muscle inserts on the columella a small scar is sometimes formed, and this is the maximum depth into its shell that the snail can retreat. The adjusting heave of the shell backwards resulted in a change in the position of the two gills in relation to the inﬂ owing respiratory current (Fig. 4.4 ): the left gill was now closer to the entering current than the right one and derived more oxygen from the water. Because of this, through evolution the left gill became larger and right gill became smaller (Fig. 4.4c ). Due to further expansion of the left part of the mantle cavity at the expense of the right, the slit gradually moved more and more to the right of the mantle cavity and shell until it eventually disap- peared. These changes in shell and mantle cavity also gradually moved the anus

Fig. 4.4 Evolutionary trends in the respiration system: (a ) mantle cavity at posterior end of body, two gills (primitive situation, in archaic molluscs); ( b) mantle cavity at front of body, two gills, anus over gills (Diodora ); (c ) left gill well-developed, right gill small, anus over right gill (Haliotis ); ( d ) left gill only, right gill absent, anus on right side ( Monodonta ) 60 4 Vetigastropda: Brush Snails to the right side of the cavity. In advanced vetigastropod groups (such as the topshells, Trochoidea) only the left gill remains. Now water enters the mantle cavity on the left side and fl ows up and among the single gill’s leafl ets for respiration; from there the water reaches the rear of the mantle space and collects urine from the kidney openings; the current fi nally turns forward along the right wall of the cavity, where it passes over the anus and collects faeces just before it leaves the mantle space. Thus, in advanced vetigastropods a constant current is formed that enters on the left and exits on the right side. All brush snails have a special sensory organ in each leafl et of the gill, in the form of a small, elongated pouch positioned directly in the path of the main inhalant respiratory current fl owing between the leafl ets. This pouch is termed a ‘bursicle’, and tracts of cilia on both lateral faces of each leafl et direct a portion of the inhalant current into it. At its blind end the bursicle consists of cells with cilia having dilated membranes, forming so-called ‘paddles’. These paddle-like cilia are chemo-sensory receptors that assist the vetigastropod in detecting chemical traces of predators such as starfi sh. Bursicles are not found in any other group of snails. Many brush snails have a horizontal fold of the body wall that projects sideways along the upper (dorsal) part of the foot. Termed the ‘epipodium’, its margins are modifi ed into a battery of sensory structures including neck lobes, tentacles of the head, lateral tentacles and head lappets. These are presented in more detail further on (Sect. 4.6 ), in context of the topshells where they are especially elaborate. The reproductive system is usually strikingly simple, and the genital duct opens into the mantle cavity through the right kidney. There are no glandular tissues along the ovule duct or sperm duct (and also no penis, as in other sea snail groups; Sect. 6.1 ). Some of the evolutionary directions and steps just speculated are represented by the major brush snail groups. Keyhole limpets have solved the sanitation problem by having a slit in their saucer shaped shells; abalones have a coiled shell with a slit on the right side closed into a series of ejection holes, and two gills; whorl-slits have a coiled shell with a slit and two gills; topshells have completely coiled shells without a slit and possess a single gill. It should be stressed that this keyhole limpet-abalone- whorl-slit-top shell series presents no more than a sequence of broad morphological patterns. It should not be interpreted as presenting the full evolutionary lineage of these groups. These and other brush snail groups will now be considered (Table 4.1 ).

Table 4.1 Major sub-groups Order Vetigastropoda Brush-snails of the order Vetigastropoda Super- family Fissurelloidea Keyhole limpets, (brush snails) Slit-limpets Super- family Lepetodriloidea Lepetodrilus Super- family Neomphaloidea Crysomallon , iron-scale snails Super- family Pleurotomarioidea Slit-whorls Super- family Haliotidoidea Abalones Super- family Trochoidea Topshells, turbans 4.2 Fissurelloidea: Keyhole Limpets, Slit Limpets and Relatives 61

4.2 Fissurelloidea: Keyhole Limpets, Slit Limpets and Relatives

Keyhole limpets (Fissurelloidea) have a conical cap-like shell that is bilaterally symmetrical with an oval base. The front margin of the shell has a shallow indenta- tion, a deep slit or a window-like opening, either on the front slope of the shell or at the shell apex. The interior side of the shell (which is porcelain-like and lacks mother-of-pearl) has a horse-shoe shaped muscle scar. The adult lacks an operculum, which was shed at metamorphosis. There are two gills in the mantle cavity, one on either side of the slit. In general, keyhole limpets adhere to rocks where they usually feed on sessile organisms and detritus, usually in the low intertidal or subtidal. The group consists of forty genera. Emarginula (Fig. 4.5 ) has a cap-like shell that has a deep vertical slit along its front slope, and the back of their foot bears a circle of some twenty ‘foot tentacles’ (further described in Sects. 4.5 and 4.6 ). It dwells in crevices on the lower shore and subtidal and feeds on bryozoans, sponges, algae and detritus. Diodora (Fig. 4.6 ) undergoes considerable developmental changes during growth: the juvenile slit on the front of the shell gradually becomes an enclosed window at the apex, and the anus retreats to the top of the mantle space.

Fig. 4.5 Emarginula sicula (1 cm), northern Atlantic and Mediterranean 62 4 Vetigastropda: Brush Snails

Fig. 4.6 Diodora ruppelli (2 cm), Indo-Paciﬁ c

During reproduction the female broadcasts thousands of ovules into the sea. The number of ovules broadcasted in a season depends on female size and age and varies from 11,000 in a small female of 2 cm to 600,000 ovules in one of 7 cm. The ovules are fertilised in the sea and the fertilised eggs develop into veligers which eventually hatch. A shallow slit appears in the front rim of the shell after metamorphosis and it eventually partially closes into a hole near the apex. Later in life the diameter of the hole grows further by the dissolution of the surrounding shell. The snail’s mantle covers only the very margin of the shell (if at all) so the shell is almost entirely exposed. Diodora dwells in lower parts of the shore where it feeds on sponges and detritus; individuals may live up to 20 years. Starfi sh are potential predators of all keyhole-limpets. When encountering a starfi sh Diodora responds by extending its mantle, refl ecting it over the shell margin and covering most of its shell, so the starfi sh cannot hold onto it. The mantle- extending response that protects Diodora from falling prey to the its predator is evoked also by the chemicals in the seawater in which a starfi sh was previously kept, not only by actual contact with the potential predator. Scutus is another keyhole limpet. It is commonly called ‘shield-shell’ and both the scientifi c and the common name refl ect the fact that the shell resembles a Roman shield. Scutus has only a slight notch in the front of its fl at, wide shell, whereas other genera have a whole slit, or a keyhole opening at their apex. Species belonging to this genus have a mantle with large fl aps usually refl ected over the shell, covering it completely and making Scutus appear slug-like. The mantle fl aps are only sometimes partly withdrawn, exposing a portion of the shell. The shield shell dwells in underwater crevices, on rocks and on the underside of coral rubble and slabs where it grazes on algae. 4.3 Lepetodriloidea and Neomphaloidea: Deep-Sea Brush-Snails 63

4.3 Lepetodriloidea and Neomphaloidea: Deep-Sea Brush-Snails

Brush-snails invaded the deep sea time and again and today they occur in a variety of deep-sea environments, including hydrothermal vents, methane and sulphide seeps, sunken wood, and whalebone and crab skeletons. Their shells are often cap- shaped, sometimes with an overhanging apex slightly coiled and irregularly twisted to the side. The shell aperture often takes the shape of the substrate to which the snail may be clamped by a pair of well developed shell muscles rather than a single one. Many of these deep sea dwellers differ from other brush snails mainly in their reproductive system: the male has a penis and a prostate, and the female has a receptacle for the sperm she receives during mating. Ovules are probably fertilised within the mantle cavity which are then shed as fertilised eggs. The veliger may perhaps be capable of delaying settlement for a long time and of surviving by drifting with bottom currents in a hibernating condition, as do some deep-sea worms. At metamorphosis it loses the operculum. Altogether, some thirty brush snail genera inhabit the deep sea. They belong to several families and super-families, but their higher classifi cation is not yet stabilised. The focus here is on two genera, Lepetodrilus (Lepetodriloidea) and Crysomallon (Neomphaloidea). Lepetodrilus is widespread and found at most sea vents, where most species graze on detritus. Two closely related species abundantly found at hydrothermal vents of the northern Pacifi c, Lepetodrilus fucensis and L. gordensis, use a diverse array of feeding methods. The radula in these species is reduced in both cusp area and ribbon length, as is the stomach volume, and these organs are not used to the same extent as in shallow water species. Nevertheless, grazing does occur and the gut of some individuals is full of grit. The gill of these species has distinct features: dense spacing of enlarged leafl ets (unattached one to another) which remain broad at the tip and stabilised by junctions of cilia. These morphological modifi cations increase the gill’s surface area and infl uence fl uid velocities across it, thereby allowing effective fi lter-feeding of suspended food particles. Occasional active suspension feeding has been documented in these two species. Remarkably, these features are found also in those advanced snail groups beyond the vetigastropods which specialise in fi lter-feeding (Sect. 7.5 ). One might perhaps be impressed by the fact that these species feed either by grazing or by fi lter-feeding, but their feeding methods and diet are even more diverse. Bacteria accumulate at the tips of the gill leafl ets, where they are harvested and formed into a mass, which is moved by cilia to the neck. Here they are sorted into acceptable material, to be passed to the mouth via the right neck lobe, versus rejected material, to be discarded. Some Lepetodrilus fucensis and L. gordensis individuals thus harvest and ingest the bacteria dwelling on their gill (in possible symbiosis) and their gut is full of fi lamentous bacteria. Apparently those individuals positioned very close to thermal vents are primarily fi lter-feeders and/or bacteria- harvesters. Those individuals positioned in more peripheral locations, where suspended particle concentrations and chemical fl uxes are low, may fi nd grazing the 64 4 Vetigastropda: Brush Snails only feasible option. Some species can thus survive in a variety of habitats by applying a wide array of feeding methods to serve various available diets. In some hydrothermal vents Lepetodrilus fucensis and Lepetodrilus gordensis can reach densities of 100,000 specimens per square metre. At these high densities, the snails live in stacks of up to half a dozen individuals, a mode of life typical also for several advanced groups of fi lter-feeding gastropods. Stacking high above the sea fl oor provides better access to unfi ltered water and presumably also to sulphides for bacteria. Filter feeding, bacteria-harvesting, or both, largely supply the nutritional requirements of the sea snails in these stacks. Grazing of the substratum, on the other hand, is hardly possible when living at the top of a stack. Lepetodrilus ancestors fi rst colonised hydrothermal vents during the Eocene (56–34 million years ago) following a global anoxic event in the sea. Other brush snail lineages, consisting of very early vetigastropod offshoots, had colonised the vents already much earlier, during the Triassic (245–208 million years ago) if not before. One of these earlier colonisers is Crysomallon, which dwells in hydrothermal vent fl uids in the Indian Ocean, rich in dissolved minerals including sulphides and metals. It probably feeds by a combination of grazing and fi lter feeding, like Lepetodrilus . Crysomallon squamiferum , the iron-scale snail (Fig. 4.7 ) lives a sedentary life at the base of black smoker chimneys in the Indian Ocean. This species differs from all other snails, and indeed from all other molluscs: its foot is covered by scales of conchiolin mineralised with pyrite (FeS2 ) and greigite (Fe3 S4 ). Its scales, measuring up to 8 mm long, cover the sides of the foot in a roof-tile fashion; their outer mineralised layer is 0.2 mm thick. The dominant crystalline mineral is pyrite, whereas greigite is present in lower proportions. The interior of the scales is penetrated by a pulp of pedal tissue that extends almost to the tip. A layer of conchiolin, studded with minute iron sulphide granules and iron sulphur compounds, is located between the pulp and the outer mineralised layers. Those parts of the scales overlain by adjacent scales are covered by a coat of bacteria. The complete scale armour is homolo- gous to an operculum. The iron-plated multi-layered structure of the natural armour of C. squamiferum, that also includes iron sulphide as skeletal material, is unlike

Fig. 4.7 Crysomallon squamiferum (2 cm), central Indian Ocean, 2,400 m deep 4.4 Pleurotomarioidea: Slit-Whorls 65 any other natural armour in the animal kingdom. It is probably advantageous in resisting penetration by crabs, and by predatory snails, such as the turrid Phymorhynchus which is found in the same vicinity as Crysomallon . Recent studies place the Neomphaloidea outside the Vetigastropoda. Hydrothermal vents have accompanied the entire history of the earth, so the rift- vent habitat has been available for a long geologic period of time. In general across the animal kingdom, hydrothermal vent communities have multiple origins. Many have modern origins while some reflect ancient elements which have survived in hydrothermal vents as habitat refuges. Some are groups which have survived throughout the deep-sea, while others have survived only in sulphide-rich hydrothermal vents. Evolution of sulphide tolerance and symbioses with chemoau- totrophic bacteria may be threshold adaptations for the invasion of sulphide-rich environments, providing protection from predators and competitors unable to tolerate the harsh environments.

4.4 Pleurotomarioidea: Slit-Whorls

Slit-whorls (Pleurotomarioidea, Fig. 4.8 ) can be identiﬁ ed as having a coiled shell with a slit. The interior of the shell consists of mother-of-pearl, and the aperture is closed by a horny operculum. In the growing snail, the advancing slit-folded mantle edge continues forming the slit along the outer lip of the aperture, while the posterior parts of the mantle close up the earlier parts of the slit with shell matter. A band- like scar traces the closed slit and is evident throughout the shell, from behind the aperture up and along all whorls of the shell, almost to the protoconch. The mantle edge has long papillae along the margins of the slit, which may inter- digitise along the midline. A section of the slit is often functionally closed, except for a small opening at the posterior margin which serves as the exhalant opening of

Fig. 4.8 Mikadotrochus beyrichii (9 cm), China and Japan, 150 m deep 66 4 Vetigastropda: Brush Snails the mantle cavity. The size and positions of the opening may vary over time, and multiple openings are occasionally produced. The left gill is larger and longer than the right one. Each gill bears a double row of triangular leafl ets and is suspended from the sides of the mantle cavity by membranes containing the afferent and efferent blood vessels. Each leafl et is stiffened by a skeletal support rod. Slit-whorls dwell in the deep sea, from 100 m down to 1,000 m, where they are abundant in rocky and steep-walled environments. They feed mainly on sponges, sometimes supplementing their diet with crinoids and soft corals. Slit-whorls are preyed upon by both crustaceans and fi sh, but seem remarkably resistant to predator attacks despite their thin and fragile shells. When disturbed, and especially when the shell is damaged, they rapidly produce voluminous amounts of a thick bluish- white fl uid that emanate from the rear of the slit and coat the shell. This fl uid is secreted from a pair of glands in the roof of the mantle cavity, the hypobranchial glands; it is heavier than sea water and not readily soluble in it, and probably repels the predators. Secreting this repellent causes the grasping predator to release the slit-whorl. Given the steep-walled environment in which slit-whorls live, dropping a snail will often cause it to drop out of reach and sight of the predator. The Pleurotomarioidea are continuously present in the fossil record from the Late Cambrian (500 million years ago). During the Palaeozoic and early Mesozoic they dominated global shallow water snail faunas, fl ourished and achieved considerable morphological diversity with numerous genera. Some had right-coiled shells whereas others had left-coiled ones; some coiled only in one plane whereas others coiled spirally; some were turreted whereas others were disc-shaped or ear-shaped; some had a disjunctive last whorl whereas others were completely open-coiled. Most of these lineages did not survive the Permian extinction of 251 million years ago. All post-Jurassic Pleurotomarioidea (later than 146 million years ago) had a limited morphological repertoire consisting primarily of spiral, cone-shaped shells. By the end of the Cretaceous Extinction only a single family survived, restricted to deep water, and today the group is represented by only four genera. Some recent studies place the Pleurotomarioidea outside the Vetigastropoda.

4.5 Haliotoidea: Abalones

The abalones (Haliotidae, Figs. 4.9 , 4.10 , and 4.11 ) consist of a single genus, the abalone Haliotis which fi rst appeared in the fossil record during the Cretaceous, 70 million years ago. An abalone has an almost fl at shell, consisting of only three to four whorls. This form is reached by a very rapid widening of the shell, and the snail dwells almost entirely in the last, very large fl attened whorl. The front side of the shell has a row of four to seven holes, representing the slit. Each hole represents a different point of time in the abalone’s development: the more recently deposited parts of the shell continue to grow the slit; later on the mantle margins on either side of the slit approach each other, closing the distal end of the slit to a hole; at 4.5 Haliotoidea: Abalones 67

Fig. 4.9 Abalone, Haliotis pustulata (4 cm), Red Sea and western Indian Ocean

Fig. 4.10 Abalone, water currents passing through holes of the shell

approximately the same time the mantle grows forward beneath the earlier holes and fi lls them with calcareous matter. Thus the number of holes on the individual adult abalone’s shell remains more or less the same during its life span. Water rich in oxygen enters the mantle space in the region of the head and also through the front hole; water containing waste products and rich in carbon dioxide is expelled through the rear holes (Fig. 4.10 ). Each new hole fi rst serves as an opening for water entrance, later it will become an opening for water exit, and fi nally the hole will be blocked. Abalones have two shell muscles. The right one is very well-developed and forms a thick muscular pillar that rises from the centre of the foot and inserts on the middle of the shell, forming a very large muscle scar; the left muscle is much smaller and leaves only a small scar. In times of danger the foot grips the substrate so power- fully that it is easier to tear the shell off the abalone than to release its grip of the rock. The large size of the adult foot requires a large shell aperture and indeed, the aperture is so large that the small veliger operculum is of no defensive value and falls off during metamorphosis from veliger to adult form. When active, the abalone stretches out its two head tentacles and explores the environment. Many other tentacles also arise from the upper side of the foot (that rises to form a sort of platform, the ‘epipodium’) and they wave about slowly to receive chemical and mechanical stimuli from the environment. Tentacles rise also 68 4 Vetigastropda: Brush Snails

Fig. 4.11 Abalone, a view into the shell

from the upper side of the mantle and protrude through the holes of the shell. This rich array of tentacles bears evidence that the abalone relies heavily on its olfactory and taste senses to gain information from its environment. Vision, on the other hand, is less developed: an abalone’s eyes are only shallow pits that open to the sea, without any enclosing cornea, and the retinal cells secrete a round glassy lens. The eye is sensitive to changes in light and shadow, but not to colour. Abalones feed on algae and sporelings covering the rock. They do not exploit their food well: some 60 % of the energetic content of the food is lost in the excreted faeces; up to 35 % is invested in breathing; and only 5 % of the food’s energy remains available for growth and reproduction. Among juveniles, all this remaining energy is devoted to growth; as the individuals mature they devote less energy to growth and more to reproduction. During the reproductive season the male and female broadcast their gametes to the water. The veliger usually swims in close proximity to its parents. The veliger’s body is capable of absorbing dissolved organic material from the sea, to an extent that may reach 70 % of its metabolic requirements. Usually the veliger prefers to settle on mucus trails laid down by mature individuals of its own species. This behaviour leads to colonial settling, the veligers making use of the trails of the adults as a signal that environmental conditions at a speciﬁ c locality are favourable and will enable their survival.

4.6 Trochoidea: Top Shells, Turbans and Allies

The turbans and top shells presumably evolved from an early slit-limpet group. The fossil record of the group goes back to the Triassic, some 215 million years ago, but an early Palaeozoic (mid-Ordovician, 450 million years ago) origin is very likely. The Trochoidea are a very large and diverse group comprising 160 genera. The shell is complete and bears no trace of a slit or of holes. It is usually spirally coiled to a moderately-sized cone that gradually grows, and its interior usually consists of mother-of-pearl. While primitive Trochoidea have ordinary, round apertures, the more advanced groups usually have an aperture that is oblique, its plane tangent 4.6 Trochoidea: Top Shells, Turbans and Allies 69

Fig. 4.12 Phasianella solida (1.5 cm), Indo-Paciﬁ c

to the preceding whorl. A tangential aperture enables better balance of the shell over the foot when the animal is active. An oblique aperture is also advantageous in enabling the sea snail to clamp the shell down over the body on hard, rocky bottoms while applying the foot to maintain a strong contact with the substratum. The beautiful shell colour patterns that decorate the shell of many trochoideans are partly determined by diet rather than by genetic control. In some top shells ( Phasianella , Fig. 4.12 ; and Tricolia , often found in sea grass beds) colour patterns within populations are highly variable, partly reﬂ ecting differences in diet of individual snails. Turning from shell shape and colour to shell microstructure, most trochideans have a shell consisting of two predominant structural layers: an outer prismatic layer, through which, at the growing lip, the pigmentation pattern of the shell is visible; and an interior layer that consists of mother-of-pearl. Both layers are composed of aragonite. Trochus and other closely-related genera have a shell with an interior that glistens with mother-of-pearl. Some deep sea trochoideans (Gaza ) have a shell with a characteristic opalescent sheen due to the visibility of mother-of-pearl through the thin, translucent outer shell layer. In others ( Tricolia , Phasianella ) the shell is red due to the pigment porphyrin, which ﬂ uoresces under ultra-violet light. Some minute top shells, however, secondarily lose the mother-of-pearl structure of the interior layer. Adult turbans and top shells have a well-developed operculum (keyhole limpets, deep sea vetigastropods and abalones lose their operculum at metamorphosis). It is shaped as a spiral coil and functions both as a protective device to block the aperture when the snail withdraws into its shell and also as a supporting pad that cushions the shell during locomotion. The operculum in some groups consists only of corneous matter whereas in others it contains also calcium carbonate. Turbo and closely related genera (Phasianellidae and Turbinidae, the pheasant snails and turbans, Figs. 4.12 , 4.13 and 4.14 ), embed calcareous matter into the horny operculum, which is partly enveloped and embedded by tissues of the foot. When the foot is withdrawn, the operculum blocks the entrance to the shell as a hard calcareous plug. Trochus and closely related genera (Trochidae, Fig. 4.15 ), and also the Tegulidae (Fig. 4.16 ) 70 4 Vetigastropda: Brush Snails

Fig. 4.13 Turban, Turbo petholatus (5 cm), Indo-Paciﬁ c

Fig. 4.14 Turban, Turbo radiatus (5 cm), Red Sea, Indo-Paciﬁ c

Fig. 4.15 Topshell, Clanculus pharaonius (2 cm), Red Sea, western Indo-Paciﬁ c 4.6 Trochoidea: Top Shells, Turbans and Allies 71

Fig. 4.16 Topshell, Tectus dentatus (12 cm), Red Sea, north-western Indo-Paciﬁ c

do not embed calcareous matter into the corneous operculum, and it is not enveloped by tissues of the foot. When their foot is withdrawn, the operculum blocks the entrance to the shell as a fl exible corneous plug. The foot serves in locomotion over the substrate, in burying into it, in righting the top shell when overturned, as well as in ‘jumping’ and ‘swimming’, as part of a response to alarm signals. Its front may be bifi d and in some groups its frontal part forms lateral ‘horns’, the function of which is not yet clear. In several top shells ( Cantharidus , Clanculus ) the rear part of the foot is capable of breaking off in response to continued disturbance. The dorsal side of the foot is somewhat fl attened and its lateral margins project beyond the right and left sides of the body as a horizontal skin fold, like the edges of a platform. Termed the ‘epipodium’, it is modifi ed into a battery of sensory structures: neck lobes, tentacles of the head, lateral tentacles and head lappets. The neck lobes are fl aps of tissue that direct the inhalant (left) and exhalant (right) currents into and away from the mantle cavity. Cilia on the left lobe beat towards the mantle cavity and those on the right lobe beat away from it. Both lobes are sometimes capable of enrolling, thereby forming shallow troughs or functionally complete tubes, and their margins are often branched and elaborated into a series of digitations. The left neck lobe is usually more elaborate, its digitations functioning as a crude fi lter that prevents the entrance of large particles into the mantle cavity. The two head tentacles are highly expandable structures and there are short eye stalks at their outer bases, each bearing one eye. Each eye has a cornea that closes it off and prevents direct contact of its light-sensitive layer (the retina) 72 4 Vetigastropda: Brush Snails

Fig. 4.17 Chlorostoma funebralis (2 cm), north- eastern Paciﬁ c

with the sea. Lateral tentacles, which are highly extendable tactile structures, grow from the sides of the epipodium, and may surround the operculum. They are much thinner than the head tentacles and they are studded with sensory cells bearing cilia. They are usually paired, with the same number (three to six) on each side of the foot. There is only a left gill. Water enters the mantle cavity from its left side, fl ows between the leafl ets of the single gill, is sensed by the bursicles for traces of predators, delivers oxygen, absorbs carbon dioxide, collects urine and faeces and then exits from the right side. Some trochids have only one series of leafl ets on one side of the gill, resembling half a feather. Topshells cannot grip the rock surface very fi rmly so they are not well adapted to life in wave-beaten shores as are limpets. A dislodged top shell rapidly withdraws into its shell and blocks its aperture with the operculum. It remains inside it as long as the sea currents roll it about over the sea fl oor. When eventually it gets stuck in some corner, it slowly and carefully stretches and pokes a few lateral tentacles out into the water, through the narrow space between the operculum and the shell. These tentacles idly wave in the water to detect signals of danger. If a predator nips off the tentacles, the top shell delays its emergence. A nipped-off lateral tentacle is quickly regenerated. If all is safe after some time, the snail slowly emerges from its shell, rights itself (if overturned) and crawls away. Most trochoids sweep and brush their food off the rocky substrata on which they dwell, but other habitats and other diets are also common in this large and diversifi ed group. Some dwell on soft sediments and climb onto sea-weeds upon which they feed. Chlorostoma funebralis (Fig. 4.17 , formerly Tegula funebralis ) is common in kelp forests of north-eastern Pacifi c, where it feeds on kelp, algae and diatoms. This is remarkable because many brown algae contain high concentrations of phloro-tannins (poly-phenolic compounds) that increase the resistance of these algae to herbivores. Juvenile fronds of kelp are also coated with slippery mucus that deters the sea snails, but the mucus is lost with age and the top shells readily attack older kelp fronds. Other trochoids ( Calliostoma and related genera) feed on a variety of sessile invertebrates including coelenterates, sponges and tunicates. 4.6 Trochoidea: Top Shells, Turbans and Allies 73

Fig. 4.18 Umbonium vestarium embedded in sediment and peeping onto the surface

Another top shell of soft sediments, Solariella , is a deposit feeder. It has unusually long and tapered head tentacles and additional elongated tentacle-like processes near the mouth, which can grasp particles. These processes sweep and rake the sediment as the snail crawls along in its search of carrion, detritus and foraminiferans. Umbonium vestarium , a tropical Indian Ocean species, also lives on soft sediments, into which it rapidly burrows and through which it creeps (Figs. 4.18 and 4.19). The front end of its foot is bifi d and when crawling, the right and left halves spread out to the sides; their thin frontal edges re-curve, applying plough- share-like actions and lead the entire sea snail into the sand. Resistance of the shell is reduced as the spire is fl attened and the shell has a smooth surface lacking ribs, ridges or tubercles. Eventually the snail disappears from view. Eyes, head and tentacles may emerge later and remain as the only visible signs of the snail. The buried Umbonium thus maintains a fully infaunal mode of life. When in its sedentary feeding position in the soft sand, Umbonium continuously moves the head in search of food. The feeding mode of Umbonium is highly specialised and mixes suspension feeding by fi ltering the water above it, and deposit feeding by gathering from the surface. In accordance with this double source of food, the two head tentacles are asymmetrical in length, placement and function. The left tentacle is shorter, displaced to the left, held erect to the sediment and is enveloped, along with the left eye stalk, by the enrolled inhalant (left) large neck lobe. This tentacle sweeps the surface of the inhalant siphon, while the branched tentacles arise from the margins of this lobe and form a crude screen with an adjustable mesh. This prevents sedi- mentary particles which are too large from entering the mantle cavity and interfering with the normal respiratory function of the gill. The gill extends the whole length of the deep mantle cavity and the tips of its elongated, fi lament-like leafl ets overarch a ciliated food groove that runs along the fl oor of the mantle cavity. Along the gill is an epithelium band composed of alternating glandular and ciliated cells, 74 4 Vetigastropda: Brush Snails

Fig. 4.19 Umbonium vestarium (1 cm), tropical Indo-Paciﬁ c: variation in shell colour

which also secrete mucus. Water with small plankton organisms and inorganic particles fl ows into the mantle cavity and is caught on the gill leafl ets. The lateral cilia of the gill beat between the leafl ets and act as a sieve while the frontal cilia direct mucus from the band of cells towards the leafl et tips. The food particles are entangled and trapped in the mucus and dropped into the food groove, where food particles mixed with mucus are rolled into a cord, which is then directed by cilia across the fl oor of the mantle cavity towards the mouth. A short snout is present; it grasps the food with lips and jaws, and the radula directs the catch through the 4.6 Trochoidea: Top Shells, Turbans and Allies 75

Fig. 4.20 Shedfoot, Stomatella auricularia (1 cm), Red Sea

mouth cavity and into the gut. When food in suspension is scarce, Umbonium collects organic matter from the substratum. The longer, fl exible right tentacle rises from the centre of the head, and it fl icks particles of sand and detritus towards the mouth, which is displaced to the right of the midline of the snail. Meanwhile, movements of the frontal parts of the foot disturb sand and detritus in the vicinity of the snout and direct them to the head, where they are manipulated by the snout into the mouth. Umbonium populations reach unusually high densities of 9,000 individuals per square metre. The smooth highly polished shell of Umbonium is attractive, both because of its button-like shape and also on account of the wide variety of colour patterns to be found in a single population. It was exported from India to Europe in its millions during the early 1900s, when shell ornamentation on boxes was fashionable. Many top shells have strong shells to cope with crab predation, and some of them complement their strong shells for defence with the ability to detect chemical cues from injured conspecifi cs in the water. The topshell/crab, prey/predator system of Chlorostoma/Cancer exemplifi es the effect of damaged conspecifi cs on sea snails and furthermore, it demonstrates the ability of sea snails to differentiate between snail-fed predators and predators that have not recently consumed snails. Chlorostoma funebralis, a species of the northern Pacifi c, can differentiate between Chlorostoma -fed crabs and those that have not recently consumed these sea snails, whether they ate other groups or even other sea snail species. When exposed to water conditioned by extracts of snail-fed crabs, the snails responded by increasing climbing speed: Chlorostoma is capable of reaching high levels of the intertidal, whereas Cancer crab predators cannot. This response may be adaptive and allows the snails to differentiate between individual crabs that pose an immediate threat and crabs that do not. Avoidance behaviour is well documented for C. funebralis in the presence of octopus, starfi sh and crabs belonging to the genus Cancer. The genus Stomatella (Fig. 4.20 , shedfoots) has a low, fl at shell, slightly similar to that of an abalone (but without a row of holes). The foot is very large and cannot 76 4 Vetigastropda: Brush Snails

Fig. 4.21 Topshell, Osilinus turbinatus (4 cm), Mediterranean

be withdrawn into the shell; it has a special pouch that covers the front of the shell. The rear part of the foot has a breakage suture, along which Stomatella can break off and shed the rear of its foot in response to continued disturbance. The foot is then capable of regeneration. Stomatella is highly active and if the boulder beneath which they dwell is overturned, they rapidly glide back to the now under side. Trochoideans have three modes of reproduction. During the reproductive season, the female usually sheds her swarm of ovules into the sea and these meet a swarm of sperm. Fertilisation occurs and the fertilised egg develops to a trochophore and then to a veliger. The egg contains little albumen, the embryo is small and the embryonic stage is of short duration. For example Osilinus (Fig. 4.21 ) trochophores hatch within approximately 1 day and the veliger settles within 4–5 days, a stage at which the diameter of its shell is approximately 1 mm. This is the most common mode of reproduction among trochids. In some cases there is sexual dimorphism. The male Tricolia is small and he rides the large female during most of the reproductive season. The female lays up to 100 eggs in a gelatinous mass, in which the whole embryonic developmental cycle takes place. The young emerge from this mass as small adult-shaped sea snails and crawl on the sea ﬂ oor, a reproductive patter termed direct development. In a few other genera ( Calliostoma, Jujubinus) the mode of reproduction is different. The male discharges his sperm into the sea near the females. The female then produces a few hundred albumen-rich ovules that she spawns into mucous masses or ribbons. This mucus hardens soon after contact with sea water so sperm penetration must occur close to the time of ovule shedding. After fertilisation the two embryonic stages, trochophore and veliger, develop inside the mucus-embedded eggs, and they feed on the plentiful albumen inside. The young hatch within one week and crawl away as tiny adults, with a shell diameter of 0.3 mm. Brooding of young occurs in several trochoidean groups. In Spectamen multistriatum and S. gerula of South Africa, females brood up to 15 developing larvae in their mantle cavity; in Solariella plicatula and S. luteola of New Zealand Bibliography 77

Fig. 4.22 Topshell, Trochus erithraeus (5 cm), Red Sea

the eggs and developing young are brooded in the umbilicus. The sexes show such disparity of morphology in some species of Margarites that they were originally described as different species (e.g. Margarites vorticiferus); in Clanculus bertheloti of the Madeiran islands larvae are brooded on the base of the shell, in grooves between spiral cords. Greek mythology tells about the ‘trochos’ (Greek for a wheel), gigantic sea monsters that used to swim in large shoals near the sea surface with their spines sticking out above water. Upon hearing the oars of an approaching boat, a trochos would curl up into a wheel and dive to deep water; when danger had passed, it would open up again and return to the sea surface. To this day the Trochoidean genus Trochus (Fig. 4.22) preserves the Greek term for a wheel; and the genus Umbonium preserves the common name ‘wheel-shell’. With an estimated 3,700 modern species and a temporal record reaching back to the early Palaeozoic, the Vetigastropoda is a successful lineage. They by far outnumber another group of primitive sea snails that gained success in a different manner, the nerites.

Bibliography

Aktipo SW, Giribet G (2010) A phylogeny of Vetigastropoda and other “archaeogastropods”: reor- ganizing old gastropod clades. Adv Mar Biol 129:220–240 Bates AE (2007) Feeding strategy, morphological specialisation and presence of bacterial episym- bionts in lepetodrilid gastropods from hydrothermal vents. Mar Ecol Prog Ser 347:87–100 Geiger DL, Thacker CE (2005) Molecular phylogeny of Vetigastropoda reveals non-monophyletic Scissurellidae, Trochoidea, and Fissurelloidea. Moll Res 25:47–55 Geiger DL, Nützel A, Sasaki T (2008) Vetigastropoda. In: Ponder WF, Lindberg DR (eds) Phylogeny and evolution of the mollusca. University of California Press, Berkeley, pp 297–330 Harasewych MG (2002) Pleurotomarioidean gastropods. Adv Mar Biol 42:238–297 Harasewych MG, McArthur AG (2000) A molecular phylogeny of the Patellogastropoda (Mollusca:Gastropoda). Mar Biol 137:183–194 78 4 Vetigastropda: Brush Snails

Hickman CS, McLean JH (1990) Systematic revision and suprageneric classifi cation of Trochacean gastropods, vol 35. Natural History Museum, Los Angeles, Science series Jacobson HP, Stabell OB (2004) Antipredator behaviour mediated by chemical cues: the role of conspecifi c alarm signalling and predator labelling in the avoidance response of a marine gastropod. Oikos 104:43–50 McLean JH (1981) The Galapagos rift limpet Neomphalus: relevance to understanding the evolution of a major paleozoic-mesozoic radiation. Malacologia 21:291–336 Szal RA (1971) “New” sense organ in primitive gastropods. Nature (London) 229:490–492 Waren A, Bengston S, Goffredi SK, Van Dover CL (2003) A hot-vent gastropod with iron sulfi de dermal sclerites. Science 302:1007 Williams ST (2012) Advances in molecular systematics of the vetigastropod superfamily Trochoidea. Zool Scr 41:571–595 Chapter 5 Neritimorpha: Nerites

Abstract The radula with its bristle-like teeth is primitive, but reproduction is advanced. Fertilisation is internal, eggs often develop inside a special capsule and hatching veligers feed on plankton until metamorphosis. Typical shells are thick, semi-globular with several whorls; the inner partitions dissolve during development, forming one large shell cavity; in others the shell is thin, and in some it is lost and the snail slug-like. Shell colours are highly variable with hues of purple, red, yellow, white, brown and black in complex patterns. Nerites ﬂ ourish in intertidal and subtidal rocky shores but some inhabit submarine caves, interstices among coral rubble, deep seeps or sulphide-rich environments. Some live, mate and lay eggs in rivers; the hatching veligers are swept to the ocean where they feed, grow and disperse; when happening upon a river mouth they metamorphose, migrate upstream and mature. This life cycle (‘amphidromy’) is common in tropical islands; the upstream migration may occur in large aggregations. Some nerites spend all their lives in freshwater; here one embryo inside each capsule develops faster, canibalises its siblings, develops into a miniature adult and hatches. Others have become terrestrial by direct embryonic development inside albumen-rich eggs. Nerites are on the evolutionary road to advanced snails.

Keywords Amphidromy • Freshwater nerites • Gastropod egg capsule • Gastropod submarine caves • Nerites • Neritimorpha • Shell variation • Terrestrial nerites

The nerites (Neritimorpha, Fig. 5.1 ) have a radula with many weak, bristle- like teeth. Their shell interior consists of calcium carbonate and resembles porcelain, not mother-of-pearl. The nerite reproductive system is separate from the urinary system: the male has a penis and therefore fertilisation is internal. There are sterile sperm in addition to fertile sperm (further elaborated in Sect. 6.1 ), the egg develops inside a special egg capsule, and the hatching larva may feed in the plankton. Nerites are conservative in their dietary requirements and most are grazers on algal spores, diatoms, and detritus. Archaic in origin, the fossil record of the Neritimorpha deﬁ - nitely extends to the Triassic (215 million years ago), perhaps even to the Ordovician (450 million years ago). The modern Neritimorpha comprises some 25 living genera, arranged in 8 families (Table 5.1). They resemble vetigastropods in their radula but differ in other aspects, and resemble the advanced snails (Chaps. 6 and 7 ).

Fig. 5.1 Nerite, Nerita orbignyana (2 cm), Red Sea and Arabian Gulf; shell variation

Table 5.1 Families within Order Neritimorpha the Neritimorpha Family Helicinidae Family Hydrocenidae Family Neritidae Family Neritiliidae Family Neritopsidae Family Phenacolepadidae Family Proserpinellidae Family Proserpinidae

The scientifi c name of the group derives from the Greek Nerites’, who was a sea- dwelling god in ancient Greek mythology. The goddess Aphrodite transformed him into a sea snail to punish him for his refusal to leave the sea together with her and ascend to land. Nerite shells vary immensely in size, shape, ornamentation and colour. Their size ranges from minute snails of less than 2 mm to large ones of more than 150 mm. Shell shape varies from a low coiled spire to semi-globular, from saucer-form to absent. Shell ornamentation varies from smooth to spiny. Shell colours are also highly variable and come in rich hues of purple, red, yellow, white, brown and black, and in patterns which are so complex that it is often diffi cult to fi nd two similarly patterned shells in a single species within a single population. 5.1 Sea-Dwelling Nerites 81

5.1 Sea-Dwelling Nerites

Within the Neritimorpha, the Neritidae are probably the most familiar of the group and the better studied. They are characterised by a usually thick shell and the aperture is shaped like a half-moon with a calcareous pad near the inner lip. The semi- globular shell consists of three to four whorls, but the upper ones are largely covered by the last whorl, so they are barely recognisable from the outside. The inner partitions of the spiral whorls dissolve during development, so that one large globular cavity is formed within the shell. An operculum with a distinctive hook on its inner side is also characteristic of this family; in addition, there is only a single (left) gill. The Neritidae, a largely tropical family, fl ourish in the mid to low intertidal, often in places where rocks and boulders rest on sand, and in shallow subtidal zones, where they inhabit rocks, rubble, and mangroves and feed on diatoms, algae and algal spores (Nerita , Fig. 5.1 ), as well as the leaves of sea grasses (the emerald nerite Smaragdia , in which the glossy green shell, Fig. 5.2 , is very thin). The female lays her eggs in special hard capsules of tough conchiolin, laid on rocks, stones, wood, shells and other hard surfaces. These capsules, comparable in strength to eggshells of birds and reptiles, are the hardest egg capsules among molluscs; they are less susceptible to predation than the soft capsules produced by other groups. Each capsule is a fl attened sphere consisting of two approximately equal halves sutured together around the equator. The lower half is a shallow, thin-walled tambour consisting of a thin organic membrane that adheres to the substratum and has a raised, thickened rim. It is covered by the upper half, which is a more robust dome-shaped lid, fi tting over the tambour and enclosing the embryos within it. Its surface is sometimes reinforced by mineral particles supplied from the intestine and stored in a special sac, opening into the egg duct; from here they are poured onto the

Fig. 5.2 Smaragdia viridis (1 cm), Mediterranean 82 5 Neritimorpha: Nerites lid surface shortly after it is formed and while it is still sticky. The mineral particles are calcium-carbonate granules manufactured inside the female, sometimes mixed with foreign material obtained from the ooze taken in with the food and passed through the intestine including sand grains, diatoms and foraminifera. The capsule structure is a fi ne balance between the need for rigidity, to prevent it from collapsing on the embryos when out of the water at low tide, and the need for porosity, to ensure suffi cient but not excessive liquid and gaseous exchange, when under water. When the veliger larvae inside the capsule are ready to hatch, the lid opens. The mechanism of release is effected by internal pressure exerted by the distension of two thin transparent membranes on the inner walls of the lid and the tambour. The ballooning of the two membranes under pressure pushes the veligers out of the egg capsule and into the sea, where they swim and feed in the plankton until ready to settle and metamorphose. The number of veligers in each capsule varies from a few tens in Nerita chamaeleon and N. undata to more than a hundred (N. balteata, N. planospira ). Not all neritids are occupants of shallow waters, Bathynerita naticoidea dwells in depths of over 2,000 m, near cold seeps where oil and methane leak out of the seafl oor in the Gulf of Mexico. It usually lives on the mussel Bathymodiolus where it feeds on bacteria and detritus and on which it lays its egg capsules, each containing up to 180 eggs. Veligers hatch after 4 months, swim and feed in the plankton for 8 months and, when reaching 0.6 mm, sink to the deep sea where they settle on Bathymodiolus shells, and metamorphose. Other groups within the Neritimorpha dwell in uncommon sea habitats. Neritopsis (Neritopsidae) exclusively inhabits submarine caves and other cryptic voids in shallow seas. Titiscania , from the same family, dwells in small interstices under deeply buried coral rubble or on stones. It has lost its shell and become entirely slug-like. The back of this ‘slug’ bears defensive glands that discharge white threads when the animal is disturbed; these threads are probably repulsive and may compensate for the lack of a protective shell. Neritilia cavernicola (Neritiliidae) of the Philippines is an obligate groundwater dweller of gloomy to totally dark caves, located 30–100 m inland from the shore and which contain pools of brackish water. These pools have no surface connection with the sea but there are extensive subterranean connections, via entirely submerged cave passages, in which the water level fl uctuates tidally. Cave-adapted morphologies of N. cavernicola include un-pigmented skin, a colourless shell, and reduced eyes in the form of open vesicles lacking a lens, a vitreous body and a cornea, and with only a few dozen retinal cells. The adults, confi ned to caves presumably due to their competitive feebleness, lay egg capsules on stones in the water of the cave, and the veligers hatch about two weeks after deposition. When the tide goes out the veligers are swept through the subterranean passages and into the open ocean, where they feed on plankton and are dispersed; while drifting in this manner they may, by chance, encounter a suitable cave in which they will settle and metamorphose. All members of the Phenacolepadidae, a small family comprising only four genera, have thin, colourless, saucer-like shells with a backwardly-pointing apex 5.2 Out of the Sea 83 near the posterior end. They have a horseshoe-shaped muscle scar on their interior side, similar to limpets. They inhabit sulphide-rich environments which are poor in oxygen and are found on the under-surface of deeply embedded stones and decaying wood in soft sediments where they probably feed on chemosynthetic bacteria.

5.2 Out of the Sea

Some genera within the Neritidae have invaded the brackish and freshwaters ( Theodoxus , Clithon , Neritina, Septaria and others). Indeed there have been fi ve or six evolutionary colonisation shifts from the sea into brackish and freshwater habitats. Fossil evidence combined with molecular data suggests that some Neritimorpha invaded land and became fully terrestrial at least three times during the Late Palaeozoic (the Carboniferous) 360–300 million years ago. Some of these genera spend the veliger stage of their life cycle in the sea and their metamorphosed stage in brackish or freshwaters. The individual’s order of events in this compulsory life strategy, termed amphidromy (from the Greek, ‘both ways’) begins in the brackish waters of an estuary or the freshwaters of a stream, continues in the sea, makes a brief sojourn in brackish waters, and then goes on again in freshwater. Indeed, the freshwater stream fauna of many tropical islands is dominated by amphidromous species, perhaps because they are the only lotic species capable of regularly colonising these habitats. Upstream and downstream migration may perhaps be an evolutionary outgrowth of the tidal migration pattern of some intertidal animals. The adults of amphidromous nerites live, mate and lay egg capsules in the freshwater streams and rivers. The eggs develop into veligers which, as they hatch, are swept downstream to the ocean, where they feed on plankton, grow and are passively dispersed in the ocean. When the veligers happen upon a brackish estuary or a freshwater river mouth they settle and metamorphose to juveniles. These travel upstream, mature and the whole process repeats itself. Encountering a freshwater habitat is bound to be a rare event, but the veligers have a fl exible life duration and can extend their pelagic duration and delay metamorphosis, anywhere from 1 to 4 months (Neritina dilatatus ), till they drift to a river mouth. Such fl exible larval duration also enables widespread geographic distributions of a species over vast areas of the Pacifi c Ocean, in rivers of islands which may be thousands of kilometres apart. When eventually the veligers settle at the mouths of the streams and rivers and metamorphose, some of the juveniles may remain in the estuary where they mature, copulate and lay eggs. Many other juveniles, however, may migrate upstream over considerable distances, often of over 10 km, where they grow, copulate, lay eggs and spend the rest of their lives. Upstream migrations are carried out by younger juvenile snails, in contrast to the estuary residency of older ones. The energy cost of migration may perhaps be compensated by the increased upstream availability of food for these snails, all of which graze on microalgae; perhaps predation pressure is lower in the upper reaches of streams. 84 5 Neritimorpha: Nerites

Another amphidromous neritid, Clithon retropictus of Japan, has a 20 years life span and is one of the most long-lived freshwater snails. In many tropical and subtropical streams worldwide, the upstream migration of settled neritid juveniles occurs in large coordinated aggregations. In rivers of Costa Rica, at sites several kilometres from the river mouths, large numbers of Neritina latissima migrate in long narrow columns up to 32 m long and only a few individuals wide; these migration lines contain thousands of snails, with an average density of up to 140 snails per metre. In Neritina virginea and Neritina punctulata of Puerto Rico massive upstream migrations of up to 5,000 individuals per square metre occur during the rainy seasons and in response to fl oods. In Neritina punctulata maximum movement rate may reach 15 m per day and a migrating aggregation may cover a distance of 200 m in less than a month; with continuous upstream movement at constant maximum speed it would take an individual 3 years to reach the uppermost areas where the species is found, 15 km from the estuary. Neritina asperulata is a small amphidromous species of rapid streams in the Melanesian Islands. Small juveniles of N. aspertula attach to the shells of a larger amphidromous species with upstream migration behaviour, Neritina pulligera : the hitchhiking juveniles aggregate densely at the posterior side of the creeping host and attach fi rmly to the shell surface of the host. Hitchhiking is an obligatory behaviour of N. aspertula, with 99 % of its juveniles found on shells of the host species. With N. pulligera travelling at a mean rate of 7.3 m per day it would take host-plus- hitchhiker a year or two to migrate 4 km inland. The hitchhiking of N. aspertula seems to be benefi cial, in that it shifts the energy cost of migration to the larger species. Another plausible benefi t of the hitchhiking behaviour may be protection from stream-dwelling predators such as fi shes, crabs and prawns. Theodoxus has left the sea completely and spends all its life in fresh water. It lives on stones, sunken wood and aquatic plants in streams, rivers, lakes, and also in brackish water. As its sea dwelling relatives, it deposits its eggs into capsules that it fi xes to the substratum or onto the shells of other freshwater snails; the lid of the capsule, strengthened by a surface layer of sand grains and diatom cases, breaks open when the young are ready to leave. In contrast to its sea-dwelling relatives, one egg inside each Theodoxus capsule cleaves more readily than its neighbours; this precocious embryo feeds on the other eggs and embryos and develops into a miniature adult before it hatches. Neritodryas , also within the Neritidae, has become somewhat terrestrial and even arboreal, and is found on coastal trees or on vegetation near fresh and brackish water. However, it retains a veliger embryonic stage which feeds in the plankton and is thus not fully adapted to the land. Beyond the Neritidae, other groups within the Neritimorpha have invaded land and become fully terrestrial by evolving a tolerance to desiccation in association with direct embryonic development inside albumen-rich eggs. The Hydrocenidae and Helicinidae are exclusively terrestrial, with a lung instead of a gill and early intra-capsular development rather than a free-swimming veliger stage. Physiological evidence suggests that the Helicinidae reached the terrestrial habitat via an indirect, fresh water route. Bibliography 85

Nerites are a highly variable group. Some live at the bottom of the deep sea and others in the intertidal zone; yet others migrate between the sea and brackish or fresh waters, and some are even terrestrial. The Neritimorpha have a reproductive system separated from the urinary system and they practice internal fertilisation, their embryos complete their development in capsules and some of them, upon hatching, feed in the plankton. It is these characters that are typical of another, more advanced group among the sea snails, the subject of Chap. 6 .

Bibliography

Kano Y, Chiba S, Kase T (2002) Major adaptive radiation in neritopsine gastropods estimated from 28S rRNA sequences and fossil records. Proc R Soc Lond B 269:2457–2465 Tan KS, Lee SSC (2009) Neritid egg capsules: are they all that different? Steenstrupia 30:115–125 Part III Advanced Sea Snails Chapter 6 Functional Morphology: An Evolutionary Perspective

Abstract Advanced snails’ (Caenogastropoda) most prominent development is in reproduction. They fertilise internally, saving costs of vast gamete production. They also separate reproduction stages in time: copulation and sperm-transfer are separated from ova fertilisation, and fertilisation from spawning. Special pouches inside the female body store sperm, enable fertilisation and form capsules in which eggs and nutrients are deposited. These capsules spare the embryos plankton-life dangers, while they feed on the nutrients, and upon hatching they swim about, and grow by feeding on plankton. Embryonic development is sometimes entirely completed inside the female body, crawling juveniles emerging from the mother. On the other hand, some plankton-feeding species extend larval life and delay metamorphosis, roaming the plankton as veligers for months, thereby extending the species’ range. In addition to fertile sperm, advanced snail males have sterile sperm (‘parasperm’) which, when inside the female, may perhaps create a hostile environment for fertile sperm of competing males. The shell consists of calcium layers structured like plywood which prevents superﬁ cial cracks from penetrating the shell. Advanced snails often have an extensible trunk, which enables reaching food not as easily accessible as rock scrapings; this results in considerable diversity in diet: grazing, ﬁ lter-feeding, predation, and parasitism, with corresponding variation in morphology.

Keywords Caenogastropoda • Cross lamellar structure • Gastropod copulation • Gastropod egg capsule • Gastropod functional morphology • Gastropod internal fertilisation • Gastropod metamorphosis • Gastropod parasperm • Gastropod proboscis • Gastropod reproduction

Some 415 million years ago, during the Devonian period, a new group evolved, known as the advanced snails (Caenogastropoda), seemingly stemming from a common ancestor they shared with the nerites. Today, this is the dominant group of sea snails. Brush snails (Vetigastropoda), important elements as they may be of the intertidal, shallow subtidal and sea-grass meadow faunas, have invaded the soft sea- ﬂ oor sediment only to a minor extent and they are completely absent from the water column, freshwater and from land. It is the advanced snails that are the snail cham- pions of the sea, in terms both of morphological diversity and of the marine habitats they exploit. Viewing their success through the dimension of Time, from the Jurassic

(some 170 million years ago) onwards to modern times, soft-bottom shallow-water snail communities are dominated by advanced snails rather than by brush snails. From an aspect of modern global abundance, the advanced snails comprise approximately 60 % of all living sea snail species. As to local abundances, the situation is similar: in a tropical marine ecosystem in New Caledonia, the Caenogastropoda were found to comprise approximately 70 % of all marine snail species and individuals, whereas the Vetigastropoda contributed only 6 % of all species and only 16 % of all individuals. Some advanced snails dwell on the rocky sea ﬂ oor, whereas others have taken to the water column where they swim actively; others burrow into soft sediments or cement themselves to rocks or embed themselves in corals; many have invaded the freshwaters and even land. Advanced snails differ from primitive sea snail groups in their reproductive system, in their embryonic development, their shell material, in their feeding system, and in their respiration. They are more closely related to the nerites than to the limpets and brush snails.

6.1 Reproductive System

The most important difference between advanced snails and primitive groups is in the complex of genital and urinary systems. Typical primitive snails usually have a common outlet duct for these two systems, whereas advanced snails have completely separate systems: the genital system has its own outlet duct for discharging its products. This separation enables, by and large, the widespread use of internal fertilisation, which occurs inside special organs in the female; this carries three clear benefi ts for advanced snails. Firstly, there is no longer need for both sexual partners to produce such vast numbers of gametes, which might or might not meet in the sea. Another advantage is that the reproductive act can be separated into three distinct stages: the act of copulation and transfer of sperm to the female may be neatly separated in time from the fertilisation of her ova; and the act of fertilisation may be separated from the spawning of the young embryo. A third advantage is that internal fertilisation enables initial development of the embryo directly inside the female’s body, where it is more protected from small-sized predators, postponing the larval stage in the plankton to the veliger stage. In some advanced-snails the complete larval cycle takes place inside the female’s body, and young snails crawl out. This mode of reproduction, known as ‘direct development’, enables precise adaptation to local environmental conditions. Internal fertilisation calls for functional changes in the morphology of the reproductive systems of both sexes. The male (Fig. 6.1 ) has a deep ciliated groove that leads from the opening of the genital system at the rear of the mantle cavity, forwards across this cavity’s fl oor to a point behind the right tentacle. This is the ‘pallial sperm groove’ of the mantle fl oor, a term used to distinguish it from the sperm duct closer to the testis. In many advanced-snail groups the walls of this groove rise and close over it, forming a tube, the ‘pallial sperm duct’; a pouch in this duct develops 6.1 Reproductive System 91

Fig. 6.1 Male genitalia in an advanced snail

Fig. 6.2 Fertile sperm (left ) and sterile parasperm (right ), schematic presentation

into a prostate. A ﬂ eshy masculine organ may develop at the distal tip of the sperm groove, behind the right tentacle. This is the penis, which penetrates the female during copulation, deposits sperm inside her body, and fertilises her internally. Many advanced snails have, in addition to the usual fertile sperm cells that participate in fertilisation, also sterile sperm cells named ‘parasperm’. These sterile cells (not existent in most primitive snails but, however, occurring in the nerites) are formed inside the testis from the same tissue that germinates the fertile sperm cells. During development their nuclei, with all its hereditary contents, shrinks and eventually disintegrates; and yolk accumulates in the cytoplasm. The sterile sperm cell is much larger than the fertile sperm cell (Fig. 6.2 ). Numerous fertile sperm attach to a sterile sperm cell by their tips and the whole composite assemblage, a sterile sperm plus its clump of fertile sperm, is released from the testis and stored in a special sperm-reserve pouch in the male’s genitalia, the seminal vesicle. Variation in shapes of the sterile sperm is such that it may serve as a diagnostic feature for sub- genera, and in some cases it is even useful to differentiate between species. 92 6 Functional Morphology: An Evolutionary Perspective

Fig. 6.3 The transition from primitive to advanced snails: evolutionary trends in the female genitalia

Sterile sperm may perhaps function in nourishing the fertile sperm. They may also perhaps function in transporting it, as the coordinated beating of the ﬂ agella of the attached sperm may propel the unit more effectively. Furthermore, in a reality of competition among rival males, the sterile cells of one male, once inside the female genitalia, may create a hostile environment for the fertile sperm cells of other males (‘sperm competition’), and may perhaps contribute to establish the paternity of the individuals that formed them. The female genital duct of advanced snails (Fig. 6.3 ) also takes the form of a deep ciliated groove that leads from the opening of the genital system, forward across the ﬂ oor of the mantle cavity to a point behind the right tentacle. In some groups the deep groove remains open but in others its walls rise and close over the groove to form an enclosed continuation of the ovule duct; this additional section of the duct is termed the ‘pallial oviduct’. It is this novel morphological female structure that enables copulation with internal fertilisation. Three pouches open into the oviduct. One is the ‘sperm receptacle’ and serves to store the sperm received during copulation; in the second, fertilisation of the ova by sperm takes place; and in the third capsules are formed, in which the female deposits the fertilised eggs together with nutrients (albumen) necessary for growth and development. 6.2 Embryonic Development 93

6.2 Embryonic Development

The embryo inside its egg capsule feeds on the nutrients, ingesting them with ciliated cells of the embryonic sail. It develops within the internal capsule through the trochophore phase to that of a veliger that completes torsion, and this advanced larva eventually hatches. Thus, the sole independent larva in advanced snails is the advanced veliger, a rather powerful swimmer compared with the weakly swimming trochophore which is the fi rst larval stage in primitive sea snail groups (limpets, top shells). The veliger swims in the plankton, feeding fi rst on nutrients supplied by its mother and then, sometimes trapping and feeding on small unicellular algae. This plankton-feeding extends larval life and enables the veliger to grow to considerable dimensions. The veliger adds whorls and enlarges its shell, so that the growing body may have room to retreat during moments of danger. Accordingly, the shell of an adult individual of advanced snails may consist of whorls representing three stages in its development: the earliest whorls of the shell are formed while the embryo is still inside the egg capsule; additional whorls are formed while the veliger swims freely in the water; and the fi nal whorls are formed after metamorphosis when becoming a snail crawling along on the sea fl oor. Most veligers swim for only a week or two before metamorphosing but some species delay their metamorphosis if no appropriate settlement site is immediately available. This trend of delaying metamorphosis culminates in species that can live in the plankton as veligers for months, or even a year, attaining shell lengths of up to 6 mm. Such a long-living veliger has evolved independently in at least ten groups of the advanced snails, but also in the primitive nerites (Sect. 5.2 ). These long-living larvae drift in oceanic currents from the old to the new world and vice versa. This travelling occurs to such an extent that many populations on either side of the Atlantic are indistinguishable. Such long distance dispersal occurs also in the Pacifi c Ocean, accounting for the presence of coastal snails throughout Polynesian and western Pacifi c islands. Species with a long veliger stage usually have greater geographic ranges than species with a short duration in the plankton. Another factor of vital importance in the natural history of advanced snails is the amount of albumen available to the developing embryo. Three groups of embryos can be discerned: embryos developing without considerable quantities of albumen hatch as small veligers that swim in the plankton, where they feed and grow; they fully depend on the plankton for their survival. A single female with this mode of development may spawn half a million eggs. Embryos with medium yolk stores hatch as well-developed veligers that do not need much food from the plankton, and they metamorphose into adult forms within days and even hours of having hatched. A third group consists of embryos which have very large albumen stores. The embryo lingers inside the egg capsule for a considerable time, weeks or even months, going through all stages of the veliger, and completing its metamorphosis inside; it emerges from the capsule as a small juvenile resembling the adult, and 94 6 Functional Morphology: An Evolutionary Perspective crawls away on the sea fl oor. Females from such groups usually attach the capsules to the sea fl oor rather than leaving them fl oating in the plankton. The advantage of this method of development is that the individual is spared the dangers involved in living independently in the plankton, such as starvation due to sparse food supplies, predation, or being swept away in the waves and currents to the vast open sea where there is no reasonable substratum upon which it may metamorphose. However, the long time the embryo lingers inside the benthic capsule exposes it to dangers of sea fl oor dwelling predators. The females of some groups of advanced snails cope with this threat by forming very thick and strong egg capsules, so that the few embryos placed inside develop in greater security. There are several ways to help feed an embryo confi ned to its capsule. One way is by forming large eggs rich in yolk. However, large quantities of yolk inhibit cell divi- sion and the early embryonic stages become very lengthy. Another way of supplying food storage is by forming small eggs with little yolk, but by forming nutrients external to the egg. The female may place special nourishment cells full of albumen inside the egg capsule which serve as a food source. A hungry embryo has yet another available food source – to feed on dead embryos. Embryo death inside egg capsules is such a common occurrence among many advanced snails that it may encompass 50 % of the embryos in one capsule. In most cases the live embryos inside the capsule eat their dead or dying siblings by fi rst hugging and crushing them with their sails and then swallowing them. By doing so the embryo gains both an additional portion of albumen, and contributes to the sanitation of the capsule, thereby reducing the dangers of microbial infections. Additionally, it creates space inside the capsule for its own growth. An embryo that gains access to its ‘brotherly albumen’ in this manner will grow faster and hatch at a more advanced stage than an embryo that does not exploit this resource.

6.3 Shell Structure

Another important difference between the advanced snails and primitive groups is in the microscopic details of the material from which the shell is structured (Fig. 6.4 ). As mentioned earlier, in many primitive snail groups the interior of the shell consists of mother-of-pearl (nacre), which has considerable fl exibility. Advanced snails have a calcium shell that is structured in a different manner. It is composed of calcium layers deposited one on top of the other somewhat like plywood (termed ‘cross lamellar structure’): each layer consists of fl attened calcium crystals all lying in the same direction; in neighbouring layers the crystals are lying in different directions, and in all of them only a short facet of the crystal parallels the shell surface. The thickness of the crystal ply is approximately 0.01 mm and it does not contain much protein material. The plywood style structure, though less fl exible than organic-rich mother-of-pearl, is more effective in preventing superfi cial cracks from penetrating deeper into the shell; and less susceptible to abrasion. Further, as it contains only little protein it is energetically less costly to produce. Shells built of cross 6.4 Feeding 95

Fig. 6.4 Details of structure of the shell matter (in both illustrations the upper part parallels the inner surface of the shell) Above : mother-of- pearl, typical of many primitive snails: ﬂ at calcium carbonate crystals one above the other, with much organic matter between them Below : cross-lamellar structure, typical of advanced-snails: part of four layers, each of which is structured as a pile of crystals sheets all in the same direction; each layer has a different direction of piles

lamellar structure generally grow faster and require less time for repair. This is of importance because large individuals are generally less susceptible to predation than are small ones, as they face fewer would-be enemies. Finally, the number of offspring produced by an individual increases with body size. Thus, the premium that sea snails gain from plywood structuring their shells includes both mechanical advantages and beneﬁ ts resulting from rapid growth.

6.4 Feeding

One factor permitting a greater adaptive radiation of the advanced snails is the development of a trunk (‘proboscis’), as a progressive elongation and folding-in of the snout. A trunk enables sea snails to live also on food not as immediately accessible as the scrapings from the surfaces of rocks and weeds. The trunk, like the foot, is extruded by blood pressure. When not in use, it is retracted by muscles and completely withdrawn into the head, tip of the trunk ﬁ rst, and ‘the whole process is like turning a stocking outside-in by putting one’s hand in and pulling the toe towards the top’ (Fretter and Graham 1962 ). What then appears to be the mouth is actually a ‘false mouth’ providing an entrance into the cavity into which the trunk has been withdrawn. 96 6 Functional Morphology: An Evolutionary Perspective

Fig. 6.5 A row of teeth in an advanced snail’s radula with seven teeth per row

An additional difference is in the radula (Fig. 6.5 ). Many of the advanced snails have a more-or-less ﬁ xed number of teeth, usually seven per row: two marginal and one lateral on either side of the central tooth (2.1.1.1.2). These teeth are stronger than the delicate bristles in the radula of brush-snails and nerites, and typical advanced-snails collect food by rasping and raking hard plant material with increased strength. On the other hand, they lack the ability to brush or sweep small loose particles, and the radula also does not scroll in and out. The structure of seven teeth per row is very stable through the evolution of advanced-snails and it occurs even in those groups among the Caenogastropoda that have, in their natural history, moved from plant raking into very different modes of feeding. However, some groups of advanced snails have a radular formula that is considerably different and this point will be considered later.

6.5 Breathing

The transition to the more effective body organisation of an advanced-snail involved also the transition to a single (left) comb-like gill rather than a pair of feather-like gills. The typical gill of advanced snails is attached to the mantle and hangs from it, and the upper series of leaﬂ ets is lost (Fig. 6.6 ). The functional signiﬁ cance of the transition from a feather-like to a comb-like gill is as yet unknown. A large osphradium at the base of the gill smells the incoming water to test its chemical qualities. Finally, some advanced snails, like the primitive nerites, have invaded the freshwater and land habitats, something that no limpet or brush-snail has done.

6.6 Classiﬁ cation

Table 6.1 presents the major groups of advanced snails mentioned in this book. In the following two chapters the natural history of these groups is explored. Chapter 7 investigates the fi rst eight of these groups, which are grazing or fi lter-feeding advanced snails; Chap. 8 deals with the remaining eight, which are predating advanced snails. 6.6 Classifi cation 97

Fig. 6.6 A primitive snail’s feather-like gill ( right) and an advanced snail’s comb-like gill ( left ) (Based on Fretter and Graham 1962 )

Table 6.1 The order Caenogastropoda, classiﬁ cation into super-families Order Caenogastropda Advanced snails Super-family Cerithioidea Creepers, ceriths, cracked-pipes Super-family Vermetoidea Worm-snails Super-family Stromboidea Conchs Super-family Xenophoroidea Stone-collectors Super-family Calyptraeoidea Cup-and-saucers, bonnets, slippers Super-family Littorinoidea Winkles Super-family Cypraeoidea Cowries, false-cowries Super-family Velutinoidea Trivia Super-family Tonnoidea Tuns, helmet shells, trumpets Super-family Naticoidea Moon shells Super-family Heteropoda Hoverers Super-family Epitonioidea Wentletraps, violet shells Super-family Eulimoidea Parasitic snails Super-family Buccinoidea Whelks, nutmegs Super-family Muricoidea Murexes Super-family Conoidea Cones 98 6 Functional Morphology: An Evolutionary Perspective

Bibliography

Bouchet P, Lozouet P, Maestrati P, Heros V (2002) Assessing the magnitude of species richness in tropical marine environments: exceptionally high numbers of molluscs at New Caledonia. Biol J Linn Soc 75:421–436 Fretter V, Graham A (1962) British prosobranch molluscs. Ray Society, London Ponder WF, Colgan DJ, Healy JM, Nützel A, Simone LRL, Strong EE (2008) Caenogastropoda. In: Ponder WF, Lindberg DR (eds) Phylogeny and evolution of the mollusca. University of California Press, Berkeley, pp 331–383 Vermeij GJ (1993) A natural history of shells. Princeton University Press, Princeton Chapter 7 Grazers and Filter Feeders

Abstract Creepers (Cerithioidea), with many, tightly-coiled shells, mostly bury into muddy sand and fi lter detritus; others, with separate, irregular whorls, dwell within sponges. Worm snails (Vermetoidea), with shells lacking orderly coils, cement themselves to rocks. Some use gills to fi lter feed; others secrete mucus and form plankton trapping nets. Males shed spermatophores which, if trapped in a female’s net, are hauled in and fertilise the ova; some brood their offspring. Conchs (Stromboidea) often have a thick shell with a fl ared outer lip; a ‘breathing pipe’ draws in water; and they usually move by leaping. Stone-carriers (Xenophoroidea) actively camoufl age themselves by attaching objects to their growing shell, resembling a pile of pebbles. Bonnets and slippers (Calyptraeoidea) are sequential hermaphrodites. Winkles (Littorinoidea) mainly inhabit the littoral. High-intertidal winkles spend most of their lives inside their thin, light shells, glued to rocks; low- shore winkles have thicker shells, against crab predation. Some winkles are completely terrestrial. Some produce veligers, others bear live young. Cowries (Cypraeoidea) have domed shells, advantageous against attacking crabs. Flaps cover the shell, to prevent fouling organisms from settling on it; most are omnivores. False cowries (Ovulidae) feed on soft corals. Smallips (Velutinoidea) feed on sea-squirts and are simultaneous hermaphrodites; their shell may be enclosed within the fl aps. Detritus feeding is complemented by fi lter feeding, through modifi cation of cleansing mechanisms of the gill: mucus enmeshed with detritus is collected as it leaves the gills and pulled into the mouth, rather than coughing it out.

Keywords Calyptraeoidea • Cerithioidea • Cypraeoidea • Gastropod reproduction • Gastropod sex change • Kleptoparasite • Littorinoidea • Stromboidea • Vermetoidea • Xenophoroidea

7.1 Cerithioidea: Creepers, Ceriths and Cracked-Pipes

The creepers and their relatives (Cerithioidea) have tall, narrow shells, with many whorls usually in close contact with one another, a circular aperture and a horny operculum. The genital system of both sexes in this advanced-snail is still primitive, in that the male does not have a penis and his sperm crosses the mantle cavity ﬂ oor in an open groove rather than in a closed sperm duct. The sperm is packed into a protein purse, termed a spermatophore, which is launched into the sea and

Fig. 7.1 Archimediella maculata (7 cm), Indo-Paciﬁ c

from there, hopefully, to the female. Similarly, the female’s ovules cross the mantle cavity fl oor in an open groove rather than in a closed oviduct. Most creepers bury into soft sand and mud, and many of the 200 genera comprising the group have invaded fresh waters. The cerithioidean fossil record can be traced back to the early Triassic (250 million years ago) but they began radiating mainly in the Cretaceous. Turritella and its close relatives such as Archimediella (Fig. 7.1 ) have a dozen whorls or so, with a round aperture. When placed on a muddy sea fl oor an individual of this genus will extend its small foot and clumsily dig its way into the substratum. Once completely dug-in, it pushes its foot forwards and upwards towards the mud surface and forms a shallow pit, the walls of which it lines with mucus to prevent them from collapsing. Having fi nished this task it remains at the bottom of the pit for days on end, its shell aperture all the while facing upwards. The snails are thus buried in the mud and only the mantle cavity is visible. In this position it feeds on minute suspended organisms that it fi lters from the water column by means of the many cilia on its gills. The gill is very long and the cilia-covered leafl ets on it are large, so they create a rather strong inhalant current. This inhalant current brings also coarse particles that might damage the gill. The outer lip of the mantle is elaborated into a series of branching tentacles that spread as a sieve over the inhalant opening to prevent this. The left side of the mantle margins are pulled out into a short exhalant pipe, which protrudes from the shell and directs the exhalant water stream away from the pit. This prevents stirring up turbid clouds of ooze and mud particles in the immediate environment by the exhalant current. Food particles 7.1 Cerithioidea: Creepers, Ceriths and Cracked-Pipes 101

accumulating on the gill leaﬂ ets are transported by the movement of cilia (other than those creating the current) to the ﬂ oor of the mantle cavity. Here they drop into a deep ciliated gutter in which they are entrapped in a mesh of mucus. This food- laden mucous rope is transported forward by other cilia to the end of the gutter, where, at the entrance to the cavity, it piles up on a small spoon-shaped lobe from which the snail feeds. The radula is drawn out of the mouth at regular intervals, plucks pieces from the mucous rope on the spoon-shaped lobe and draws it into the mouth. Turritella communis lives in dense colonies of up to 600 individuals per square metre in the northern Atlantic and the Mediterranean. During the reproductive season, the female broadcasts a special male-attracting pheromone into the water; the nearby males respond by emerging from the mud and crawling towards her, even from distances of half a metre. They aggregate around her pit in small groups of up to half a dozen males, arranged in a star-shaped formation, and when so close that they can touch her, they each secrete ‘sperm purses’ or spermatophores into the water. The female inhales these purses into her mantle cavity with her strong inhalant current. Once inside her mantle cavity, the spermatophores burst open and all the sperm within them tumble out and ascend along the oviduct, to a special sperm-storage pouch, the sperm receptacle (‘receptaculum seminis ’). They wait here until ripe ova descend, and then proceed to the fertilisation-pouch to fertilise them. Internal fertilisation is thus achieved without a penis and without copulation. Each fertilised egg has a size of 0.1 mm and they are placed within capsules; each capsule contains some 30 eggs, and several capsules are laid together in a jelly mass. Veligers emerge from the eggs within a week. Cerithium and its allies (the ceriths, Fig. 7.2 ) have a well-developed notch at the lower part of the shell aperture, and in this character they differ from Turritella .

Fig. 7.2 Different Cerithioidea, from left : Cerithium adansonii (7 cm), Red Sea and western Indian Ocean; Rhinoclavis kochi (7 cm), Mediterranean; Clypeomurus petrosa (2 cm), Red Sea and western Indian Ocean 102 7 Grazers and Filter Feeders

Fig. 7.3 Cerithioidea: Planaxis sulcatus (2 cm), Indian Ocean

Fig. 7.4 Cerithioidea: the cracked-pipe, Tenagodus obtusus (22 cm), north-western Atlantic and Mediterranean

These genera dwell in lower zones of sheltered shores, sometimes in the shallow subtidal. They are incapable of holding strongly on to the substratum and therefore are absent from shores with strong, pounding waves. During low tide the cerith digs into the damp layer of sand or fi ne gravel that covers the underlying beach-rock, avoiding exposure to desiccation and predation. Planaxis sulcatus (Fig. 7.3 ) is a cerithioidean living in the rocky intertidal, widely distributed in the Indian Ocean where some populations consist of both males and females and other populations consist of females only. Its short shell and dark colour offer superfi cial resemblance to a winkle (described later in this chapter). The female has a special pouch in the mantle cavity in which the eggs develop to veliger stage, when they are released into the sea. Reproduction in the all-female populations may occur without a male. ‘Parthenogenesis’ is the term for this form of asexual reproduction found in species where growth and development of embryos occur without fertilisation by a male. Tenagodus has an elongate pipe-like shell (Fig. 7.4 ). Only the fi rst, uppermost whorls are organised in an orderly coil; the later whorls are separate, irregular and 7.1 Cerithioidea: Creepers, Ceriths and Cracked-Pipes 103 do not touch one another. There is a continuous cleft or sometimes a series of small openings along the longitudinal axis of the shell (a suitable vernacular name for this snail would be ‘cracked-pipe’; it has a large operculum. The cracked-pipe dwells within sponges and feeds by fi ltering particles from the sea. A veliger that settles on a sponge metamorphoses to adult form, and is buried into the sponge as the latter grows around and covers it. The sponge offers the cracked-pipe mechanical defence and sometimes also chemical defence, since many sponges are toxic. Also, the feeding current that the sponge creates for itself is available also for the snail. While fi ltering, the head and foot are spread out to enable entrance of water to the shell aperture. Cilia movement creates an inhalant current that enters the mantle cavity, passes over the gill and exits into the host sponge through the ‘cracks’ in the shell. Occasionally the snail withdraws rapidly into its shell and rapidly sucks water in, and then quickly pumps it out through the cracks in its shell. This rapid action fl ushes food particles from the mantle cavity, so the cracked-pipe reciprocates and also supplies the sponge with food. To fi lter its food, the cracked-pipe must constantly see to it that its shell is close to the outer wall of the sponge. This necessity constrains it to adapt the speed and direction of its growth to that of the sponge. Sponges may grow irregularly and in opportunistic and unpredictable directions, so the snail must be able to grow in ever- changing directions to maintain its aperture alignment with the wall of the sponge. That is why the shell of the cracked-pipe grows in an irregular manner, with whorls that appear as an open coil or without any coil what-so-ever. Another manner to cope with the sudden growth changes is by breaking the calcareous shell and sticking it on anew. The cracked-pipe cracks the margins of the shell’s last whorl, changes them into various shapes of wedges or pegs, pushes them outwards and sticks them into the protein mesh again, the pegs slightly distant and separated from one another. This increases the width of the shell and enables broadening the body without lengthening it. Tenagodus is also able to lengthen the shell without growth of the body: the individual forms a calcareous partition that seals off the rear parts of the shell, and shifts its whole body forwards so that it now protrudes forward out of the shell and no longer occupies the entire shell. This in turn encourages rapid shell growth and keeps up with the growth of the sponge host without supplementary growth of the soft body. In Tenagodus male and female are separate and fertilisation is internal. The egg capsules are brooded inside the female’s body. Sometimes veligers hatch from the eggs and swim out into the sea, but sometimes the entire embryonic development is completed within the brood pouch so that eventually tiny crawling snails emerge from the mantle cavity, crawl a little and settle, dwelling and growing within the same sponge in which they were born. Many genera of the Cerithioidea have invaded freshwaters, in the tropics of many continents: Melanoides , Pseudoplotia , Thiara , Melanopsis and many others. Their fascinating natural history is beyond the scope of this book. 104 7 Grazers and Filter Feeders

7.2 Vermetoidea: Worm Snails

Worm snails (Vermetoidea) cement their shell to rocks and resemble an irregular tube or pipe without orderly coils to such an extent that it is diffi cult to trace the external characteristics of a sea snail. Viewed from the outside, worm snails resemble cemented worms; indeed, the scientifi c name of the group means ‘worms’. The group is present in the fossil record since the Jurassic (200 to 146 million years ago) and today consists of seven genera, common on the lower shore and in the sub-tidal. Most species have an operculum, and this is one of the few reliable outward features of their genus-level classifi cation. Some worm snail groups are solitary and live as sparsely distributed individuals, each well-spaced from its neighbours by at least several tens of centimetres; in others the individuals are closely aggregated to such an extent that their shells entwine into a dense mass of irregularly coiled shells, with hundreds if not thousands of cemented worm snails per square metre. Wave-crash intertidal regions of the Mediterranean Sea have dense aggregates of Dendropoma petraeum (Fig. 7.5). Its shell is short and wide, cumbersome and well cemented throughout its entire length to the surface on which it grows, to prevent the pounding waves and breakers from tearing it off. It is equipped with a large, thick operculum, to defend the animal itself from the shattering effects of beating waves during rising tides, from desiccation during low tide, and from predators and parasites. The foot is rapidly withdrawn into the shell during moments of danger, and the large operculum then blocks the shell aperture completely; indeed it is so

Fig. 7.5 Worm snails: Dendropoma petraeum , a ﬁ lter-feeder. Above : a colony with hundreds of individuals entwined one into another; below : a single snail protruding from its shell 7.2 Vermetoidea: Worm Snails 105

Fig. 7.6 Worm snails: Vermetus sp., a net-feeder (4 cm high), Mediterranean. Right : shell of single snail. Left : a single snail protruding from its shell

large that it prevents the snail from retreating deep into its shell. Dendropoma petraeum feeds by fi ltering plankton, in a manner broadly similar to the feeding method employed by the certhioideans Turritella and Archimediella, mentioned above. The gill is large and covered by vast fi elds of beating cilia, causing a current to fl ow into the mantle cavity. Plankton particles entrapped by the gill are transferred by other cilia to a groove on the fl oor of the mantle cavity, in which the particles get entangled in a mesh of mucus. This mesh is then transferred forward along the groove to the front of the fl oor of the mantle cavity; here the extended radula plucks off chunks of food-laden mucus and passes them into the mouth. Vermetes triqueter populates calm sites along the Mediterranean Sea and each individual of this species is solitary. The shell is elongate and narrow, and only its fi rst, older parts are cemented to the rock surface while its opening is lifted up from the substrate. The operculum is reduced to a small button, enabling the snail to retreat deeply into the upper whorls of its shell during moments of danger (Fig. 7.6 ). Vermetes triqueter makes extensive use of the large mucus gland in the front part of the sole of the foot for feeding. In most sea snail groups the mucus secreted by this gland serves the snail in crawling. In sedentary V. triqueter, however, this gland grows to very considerable dimensions, and has been recruited for another function: mucus secreted from the gland forms a large net that gathers food. The gland sides have a pair of long delicate tentacles that face into the sea. These tentacles of the foot are in addition to the usual head tentacles and should not to be confused with them. Grooves along these tentacles are lined with cilia, which beat from the base of each tentacle to its tip. The currents that these cilia form carry the mucus which streams from the gland along the foot-tentacle grooves to their tips, from where it is spread as threads into the sea. The mucus threads fl oat in the sea and stick to one another, forming a net some 50 cm in diameter, in which small planktonic organisms get entangled. The net remains in the water for approximately 20 min and the radula then hauls it into the mouth. The oesophagus is fl exible and can extend to form a large storage cavity for the mucus, which is rapidly swallowed before its slower transfer into the stomach for digestion. Most of the mucus in the net is digested and 106 7 Grazers and Filter Feeders recycled, enabling considerable saving of energy expenditure. A new net is cast 3–4 min after the previous one was hauled in. Dendropoma maxima , which dwells in coral reefs of the Indian Ocean, cements the shell to the substratum along its whole length, even when half a metre long. In spite of its impressive shell length, the snail occupies only the more anterior newer parts of the shell, whereas the older parts are sealed off by calcareous partitions; accordingly the snail cannot retreat into its shell beyond a few centimetres. Whereas thread-feeding occurs in the Mediterranean Sea only in calm water habitats, in the Red Sea coral reefs it occurs also in wave-crash ones. Dendropoma maxima dwells mostly just below the intertidal, at the front edge of the reef table, where torrential waters promise an abundant supply of particulate food, thereby enabling a higher density of worm snails (up to 200 individuals per square metre). It seems that front edge waters provide an abundant supply of particulate food and enable a high density of worm snails. Dendropoma maxima also casts mucus nets that trap and stick to particles fl oating in the water. Most particles trapped in the nets consist of detritus, abundant on the reef table. The net is hauled into the mouth every 20 min in a process that lasts 6 min, and a new net appears a few minutes after the previous one was swallowed. The net’s capacity for trapping particles is amazing: one gram (dry weight) of net may trap one quarter of a gram (dry material) of particulate matter. Dendropoma maxima is active all hours of the day and night. Worm snails dwell in rocky habitats and feed on food particles suspended in the water: some species create an inhalant current into the mantle cavity that fi lters particulate matter by use of the gill, whereas some secrete and spread a net of sticky mucus threads into the water to collect food. By and large, there seems to be a connection between the mode of feeding and the habitat: gill-fi ltering species live in wave swept habitats with strong currents whereas net-spreading species occur in habitats with weaker currents, typical of calm lagoons and crevices. How does a snail fi xed to its place reproduce? The male worm snail creates a spermatophore (sperm purse) constructed of three small transparent capsules, one within the other (Fig. 7.7 ). The innermost capsule contains liquid with a high salt concentration, and a coiled tube arises from its inner wall into its cavity, like the turned-in fi nger of a glove; at the end of this tube a sperm mass is placed, consisting of both true fertilising sperm and sterile parasperm. The middle capsule adheres to the inner one, and the outer capsule is tapered at its two ends so that in shape the purse somewhat resembles a teardrop. When the walls of the outer capsule are intact, they prevent water from entering the entire purse. The male ejects spermatophores from the mantle cavity and they are swept into the sea; if they happen to be trapped by the net of a female, they are hauled into her mouth when the net is hauled in. The female holds on to the purse with her radula and jaws; as she squashes it and the sperm purse yields, sea water rapidly fl ows into the purse cavity, exercising considerable pressure. This pressure causes the coiled tube to turn inside-out and the sperm inside to be splashed into the female’s mouth cavity. From here the sperm is inhaled (in the respiratory current) into the mantle cavity just above the mouth; the ripe ova also descend into it, and it is here that fertilisation occurs. Thus worm snails, like creepers, manage to practice internal fertilisation without copulation. 7.2 Vermetoidea: Worm Snails 107

Fig. 7.7 Sperm purse (spermatophore) of a worm snail (Based on Hadﬁ eld and Hopper 1980 )

In general, worm snails brood their offspring inside the mantle cavity. The female genital system in Dendropoma petraeum can store the sperm for considerable periods of time. She lays the fertilised eggs in capsules that she broods freely in the mantle cavity. A female may brood up to 90 capsules simultaneously. Each capsule is 1 mm long, and usually there is only one egg in each capsule. When the brooding female withdraws into the shell during moments of danger, she takes her eggs with her. The developing embryo feeds on the nourishing yolk in the egg and completes its development there, so that eventually it hatches in the form of an active crawling individual 0.2 mm long. It adheres within a few hours, cements itself to the hard substratum and starts growing; in this way, a dense colony may eventually be formed, consisting of the descendants of the original female. Vermetes triqueter and allied species retreat deep into the shell, and this habit inﬂ uences the method of egg defence. The female’s mantle is deeply indented, thereby enabling the egg capsules to hang from the mantle cavity. The eggs are placed in a column of pear-shaped capsules, each hanging by a short stalk from the female’s shell-ceiling, close to the shell aperture. When rapidly retreating into the depths of the shell in moments of danger, the female abandons these egg capsules undefended close to the shell aperture and retreats without them. Had the eggs been lying freely in the mantle cavity, they would surely have been squashed and damaged upon retreat into the depth of the shell, since space is too narrow to contain the head and foot of the mother as well as her eggs. 108 7 Grazers and Filter Feeders

7.3 Stromboidea: Pelican’s-Foots, Conchs and Relatives

The Stromboidea is a small group of some ten genera. Conchs, pelican’s-foots and their close relatives all belong to the Stromboidea, advanced snails which rely on a massive shell for defence. The shell of a mature conch often has a fl ared outer lip from which long fi nger-like spines may protrude. The shell spire is more moderate and the aperture is more elongate than in creepers (Sect . 7.1 ). Stromboideans usually move along the sea fl oor by a series of ‘leaps’, as described below, whereas most snails glide steadily. A short tube, the ‘breathing pipe’ (termed ‘siphon’) develops from the mantle margin as a scroll and is used for drawing water into the mantle cavity. The siphon is held in front of and above the snail and is capable of considerable movement, swinging from side to side as it draws water in for respiration; the incoming water fl ows over the osphradium, a gill-like organ inside the mantle cavity that tests and detects scents of food, mates, and predators. (The siphon is further discussed in the context of those advanced-snails which have shifted to predatory feeding, Sect. 8.1 ). The oral region of the head is elongated into a prominent extendable muscular snout that contains the radula, and this enables the probing into areas that otherwise cannot be reached to collect food. The male conch has a penis, enabling copulation and effective internal fertilisation. The pelican’s-foot Aporrhais (Fig. 7.8) is the more primitive member of this advanced-snail group, having changed little since its ancestors fi rst appeared during the Jurassic, some 195 million years ago. The juvenile in this genus retains a turreted architecture with an elongate aperture and a smooth lip, whereas the adult has a widely fl ared lip. The shell has rows of axial tubercles that form fi nger-like processes at the lip of the aperture. Pelican’s-foot snails dwell upon the sandy mud of the sea fl oor or immediately beneath the surface. They have a large vertical range of habitats, found from 10 m down to depths of 2,000 m. When digging into the sea fl oor, a juvenile pelican’s-foot fi rst extends its foot downwards and pushes it through the sandy mud to obtain a hold, and then contracts its shell muscle, to pull also the shell beneath the surface. Having penetrated the mud, it uses its long fl exible

Fig. 7.8 Pelican’s-foot buried in sediment, with inhalant and exhalant currents (Based on Yonge and Thompson 1976 ) 7.3 Stromboidea: Pelican’s-Foots, Conchs and Relatives 109 trunk to build two breathing shafts that it stabilises with linings of mucus (Fig. 7.8 ). A constant current of water enters the front shaft, fl ows through the gills and exits through the rear shaft, enabling respiration. The juvenile snail remains in this position for many days without emerging to the surface. Upon reaching maturity it forms a fl ared outer lip and then tends to dwell also on the surface of the sandy mud rather than in it. When moving over the sea fl oor, an adult pelican’s-foot fi rst stretches its foot forwards while slightly lifting its shell from the substratum; then, by sudden strong muscular contraction, it heaves and throws the shell forward; the fl ared lip may stabilise the shell during these rapid ‘leaps’, the normal mode of adult locomotion. Leaping is not very fast under normal conditions and an adult advances at a rate of only 1 cm per minute. However, this rate increases considerably in the presence of a predator, when it may reach 14 cm per minute. Juvenile escape rate is only 5 cm per minute. To compare, the predatory snail Colus stimpsoni moves at a rate of 6 cm per minute, a little faster than an escaping juvenile but much slower than an escaping adult. When (in the lab) a pelican’s-foot is turned over with its aperture facing upwards it fi rst withdraws into its shell, but eventually attempts to turn over and right itself. When juveniles do this, they slowly protrude the foot from the shell aperture, extend it over the aperture to the left or to the right, and then dig the front part into the sandy mud; when a hold has been obtained, the shell muscle rapidly contracts and pulls the shell over. Juvenile shells roll freely and are easily righted, so that a righting attempt by use of this ‘foot-pull’ method takes approximately 45 s and requires on average two attempts. Adult pelican’s-foots usually use a different method when righting themselves. They commonly fi rst extend the foot behind the outer lip and then place its rear part on the sea fl oor, beneath the spire. Then the foot pushes down against the sandy mud with a quick motion, fl ipping the spire up and over. In this ‘kick’ method a righting attempt to turn the shell over takes 18 s and requires approximately three attempts (in the lab). If an adult pelican’s-foot were to apply the juvenile’s ‘foot-pull’ method, the snail would have to overcome the added weight of the fl aring outer lip; or, the added distance from the centre of gravity of the shell would have to move in order for the animal to right itself. In both cases, the foot would have a tendency to come free of the sandy sea fl oor when shell and foot muscles were contracted. When kicking, the weak attachment of the foot to the sandy mud is not a limiting factor. A kick is therefore a mechanically appropriate method of righting for adult pelican’s-foots with their fl ared outer lips. Pelican’s-foot patterns of activity seem to vary among species. Aporrhais occidentalis of the north-western Atlantic (Fig. 7.9 ) alternates seasonally between periods of above-surface feeding activity and below-surface quiescence. Individuals of this species tend to remain burrowed from autumn through winter, but are active on the surface of the sea fl oor through spring and summer. However, another species, Aporrhais pespelecani of the north-eastern Atlantic and Mediterranean (Fig. 7.10 ), may feed while burrowed. Sitting beneath the sheltered space of its tent-like shell day after day, the snail gropes and seeks detritus in its immediate surroundings 110 7 Grazers and Filter Feeders

Fig. 7.9 Pelican’s-foot: Aporrhais occidentalis (3 cm), north-western Atlantic

Fig. 7.10 Pelican’s-foot, Aporrhais pespelecani (4 cm): juvenile (left ) and adult ( right ), north- eastern Atlantic and Mediterranean 7.3 Stromboidea: Pelican’s-Foots, Conchs and Relatives 111

Fig. 7.11 Conch, Strombus (Conomurex) fasciatus (4 cm), Red Sea and north-western Indian Ocean

using its trunk. When food resources in reach of its trunk are exhausted, it shifts a little, settles down and starts feeding again. Both species have small eggs (0.25 mm) deposited singly or in small groups. The veligers feed and grow considerably in the plankton before settling and metamorphosing. Strombus and its close allies (Figs. 7.11 and 7.12), to which the name conch usually applies, have a deep notch on their shell aperture. The eyes are on long stalks, and the right eye peeps out through the notch. Another notch, at the base of the shell, accommodates the breathing tube. The operculum is often narrow, pointed and sickle-shaped, sometimes with a serrated edge. ‘ Strombus ’ comes from the Latin and was a Romans’ name used to describe a sea snail. Strombus conchs are predominantly plant grazers feeding on algae and sea- grasses. Accordingly, they are usually restricted to shallow water lagoons and sea-grass meadows down to depths of no more than 20 m, and they always dwell on top of the sea fl oor. Under normal conditions the conch advances by fi rst stretching its foot forwards and then strongly contracting the shell muscle, thereby heaving the shell forward and leaping (like the pelican’s-foot). When fl eeing from predators, however, it uses its long and dagger-like operculum as a lever. The operculum is stabbed into the sand and serves as a leverage point for the powerful muscular contraction that lifts and heaves the whole snail forwards or backwards so that it leaps (Fig. 7.13 ). Escaping conchs respond to the scent of the venomous predatory sea snail Conus 112 7 Grazers and Filter Feeders

Fig. 7.12 Conch, Strombus (Canarium) mutabilis (3 cm), Red Sea and western Indian Ocean

Fig. 7.13 Conch: leaping movement while sticking the operculum into sand textile by doubling their rate of leaping. Kick-leaping with the operculum yields faster movement than in pelican’s-foot snails: Strombus maculatus , a tropical Indo-Pacifi c shallow water species, can escape at a rate of 94 cm per minute, whereas a pelican’s-foot rate is only 14 cm. The long operculum also serves conchs when they are overturned: their fi rst response is to retreat into the shell and close the aperture; later the snail slowly stretches its foot out, bends it around the shell, and sticks the operculum into the sand beneath; suddenly and rapidly it contracts the shell muscle and fl ips the shell over. The use of the long operculum in fl eeing and in shell righting is an advanced behavioural trait, not present in the more primitive pelican’s-foot snails. Male conchs are often smaller than females. During reproduction the male follows the female, places the front of his shell on the back of her shell and copulates by extending his penis beneath her shell, inserting it into her genital opening and delivering sperm; fertilisation is thus internal. A female conch spawns some half a 7.3 Stromboidea: Pelican’s-Foots, Conchs and Relatives 113

Fig. 7.14 Conch: a veliger with a sail consisting of six lobes

million tiny encapsulated eggs into a long gelatinous strand that, if straightened out would reach a length of up to 20 m. She can fertilise and spawn either while still copulating, or store the sperm and delay fertilising and spawning till later. In some species the female guards her eggs beneath her shell until they hatch as tiny veligers that swim away and feed in the plankton. Early in its development the veliger has two sails; later it grows two more and fi nally it has six, thereby improving its fl oating abilities as it grows (Fig. 7.14 ). Two or three weeks after hatching, the veliger is fully developed and ready to alight on the sea fl oor to metamorphose. Metamorphosis ability lasts only a week and, as in most sea snails, the veliger dies if it fails to metamorphose during this period. A juvenile can perform the complete behavioural patterns associated with locomotion, feeding and righting of overturned shells immediately after metamorphosis. However, only 3 weeks later, at 2 mm long, can the juvenile perform the escape response to predators. From this age onwards, the complete response is released upon fi rst encounter with a predator. Lobatus galeatus of the eastern Pacifi c (Fig. 7.15 ) is a large strombid of up to 23 cm, which lives in sandy bottoms of the shallow subtidal on feeds on macroalgae and detritus. Snails of this species spend much of their lives buried in the sand but they may also move long distances, on the scale of several kilometres within a few months. During the mating season they form large aggregates in which they copulate and lay large egg masses. Shells of L. galeatus were used as trumpets by the Chavín culture of ancient Peru, dating back to between 1500 and 300 BC, as is further elaborated in Chap. 13 . The spider-conch Lambis (Fig. 7.16) has a very thick heavy shell, with four to seven hollow fi nger-like processes radiating from the outer lip; the outer lip of the shell has a deep notch through which the right eye peeps out on a long stalk. The eyes have a splendid ring-like pattern in colours of bluish green. Spider-conchs dwell in shallow tropical waters of the Indo-Pacifi c and feed on the fi lamentous algae that they collect with their long muscular trunks. They may heave their shell forward and crash into such predators as fi sh, crabs and octopus, to deter them. The long eye stalks of spider-conchs are frequently attacked by marine predators, but amputated tips of eye stalks regenerate quickly and a new fully formed eye develops within just one month. 114 7 Grazers and Filter Feeders

Fig. 7.15 Strombus galeatus (17 cm), Costa Rica

Bracelets manufactured from spider-conch shells have been found on 6,000-year-old skeletons at prehistoric sites in the Sinai Peninsula, at the north of the Red Sea; usually they were found on bones of the wrist. Spider-conch shells that perhaps served as ritual offerings have been found at other prehistoric sites in Sinai. Today, the spider-conch still serves the Bedouin of Sinai as a potion to treat impotence. The stone-carrier Xenophora (Fig. 7.17 ) also dwells on the surface of the sea ﬂ oor, and it may be found as deep down as 400 m in tropical waters throughout the world. Its group, the Xenophoroidea, is closely related to the conchs but has a tent- like shell. This sea snail remains in one place for long periods but occasionally shifts a little, by movements similar to those of the pelican’s-foot, conch and spider- conch. It gropes around the sea ﬂ oor beneath the shell’s space with its trunk seeking detritus, its main food. It has a strange habit of burying its faeces: the foot digs a small pit and the trunk later covers the deposited faeces. 7.3 Stromboidea: Pelican’s-Foots, Conchs and Relatives 115

Fig. 7.16 Spider-conch, Lambis truncatus (25 cm), Indo-Paciﬁ c

Fig. 7.17 Stone-carrier, Xenophora sp. (6 cm) 116 7 Grazers and Filter Feeders

The stone-carrier actively camoufl ages itself: during shell growth it attaches various hard objects to the mantle by using the calcium carbonate which it secretes when forming its shell. These objects include pebbles, coral skeletons, empty snail shells, or valves of bivalves which strangely, it usually attaches the valves with their inner part facing upwards. It fi rst cleans a pebble with its head and foot; then it attaches it to the margins of the mantle that secretes calcium carbonate, cementing the pebble to the shell; and fi nally it locates remaining holes between the mantle and pebble and blocks them with sand and other small objects that it glues to the shell. Sometimes it places its trunk beneath the glued pebble for support, and gently rocks it too and fro, to ensure that it is correctly stuck on and stable. If the pebble is large, the snail may remain in its place for more than 10 h, to ensure strong cementation. Eventually the stone-carrier resembles a small pile of pebbles and shell fragments, that makes it very difficult to distinguish from similar true piles strewn around on the sea fl oor. The foreign objects that the stone-carrier sticks to its shell may include also live coral, which remains alive for some time after having been cemented to the shell.

7.4 Calyptraeoidea: Cup-and-Saucers, Bonnets and Slippers

Cup-and-saucers, bonnets and slippers all belong to the Calyptraeoidea, in which the shell is shaped like a bilaterally symmetrical low and wide cone with a slightly frontal apex, and the aperture is wide; in fact it broadly resembles a limpet. The interior side of the shell has a shelf, also of shelly material. The foot has no operculum. Many snails in this group are sequential hermaphrodites: at a very early age, each individual functions as male, and later it turns into a female. To copulate the male crawls up to a female and positions himself so that his penis penetrates either her exhalant or inhalant current opening, and discharges his sperm into her. In the cup-and-saucer (Crucibulum , Fig. 7.18 ) the shell muscle attaches to a cup- shaped shelly structure beneath the shell’s apex, from which its ﬁ bres radiate to the foot. These snails cling to rocks, stones and dead coral below the low tide mark,

Fig. 7.18 Cup-and-saucer, Crucibulum spinosum (4 cm), eastern Pacifi c 7.4 Calyptraeoidea: Cup-and-Saucers, Bonnets and Slippers 117 usually in protected habitats with good water circulation. Although they may remain stationary for some days they are not sedentary, and young and old, male and female roam about, sometimes from one rock to another. Cup-and-saucers feed by both grazing and fi ltering. They rasp algae off the substratum with the radula and in addition they collect and fi lter food in suspension. Their gill is extensive and has elongate leafl ets, and the lateral cilia on them establish a feeding current that passes into the mantle cavity through a narrow inhalant opening. Incoming particles are trapped on the leafl ets and moved to their tips from where they drop into a food groove on the mantle fl oor and stick to mucus. Cilia roll the food-laden mucus into a strand that they advance to a point where the radula can pluck it off and pull it into the mouth. Crucibulum can fi lter-feed even when the shell is held close to the rock, for there is a slight upward curvature at the left front edge of the shell that enables the inhalant water current to pass to the mantle cavity; slightly lifting the shell from the substratum improves the inhalant current. Cup-and-saucers are sequential hermaphrodite. Most cup-and-saucers discharge veligers into the plankton but the female of some Crucibulum species brood their young. When ready to lay eggs the female of such species at fi rst remains stationary and secretes additional circumferential layers of shell. The shell now fi ts tightly to the substratum, and the entire shell forms a well-sealed brood chamber. The covered egg mass consists of 10–20 thin fl attened capsules, each with a stalk that attaches it to the hard substratum. Each capsule contains 10–20 embryos that hatch at crawling stage, possessing a well-developed foot and short tentacles with eyes located at their bases. Hoof snails ( Hipponix, Figs. 7.19 , 7.20, and 7.21) have a cap-like shell, the interior of which has a horseshoe-shaped muscle scar with the open end above the head. The front part of the foot enables movement, while the rear part often secretes a wide chalky horseshoe-shaped internal shelf beneath it, whose outer margins combine with the inner lip of the shell; this shelf (Fig. 7.19 ) is termed ‘septum’. This shelf protects the creature’s soft organs and also enables a better attachment

Fig. 7.19 A typical hoof snail with a shelf covering part of the shell aperture 118 7 Grazers and Filter Feeders

Fig. 7.20 Hoof snail Hipponix sp. (0.5 cm)

Fig. 7.21 Hipponix conicus (1 cm), Pacifi c to the site. Hoof snails are either sedentary snails of very limited relocation abilities or completely sessile. Some hoof snail species inhabit rocks, where they grope for and collect pieces of calcareous algae and detritus with a long, stretchable trunk. One such species is Hipponix cranoides, found on Californian coasts, that occupies small rounded depressions in the rock surface. It moves around early in life, but at a later stage settles permanently. It then proceeds to secrete a layer of calcareous matter onto the surface of the underlying rock. This cemented ‘ventral valve’ may eventually attain almost the same size and thickness of the true upper shell. It is formed by secreting calcium from the sole of the foot in the same way that the mantle produces the shell, and it too bears a horseshoe-shaped muscle scar, open towards the front. These two shells unite at the posterior end of the snail. Muscle contraction pulls the upper shell down fi rmly against the perfectly matching ‘ventral valve’, to protect the hoof snail inside against enemies, against the force of the sea and against the dangers of desiccation. This effective protection is clearly at the expense of mobility. The foot of the now sessile H. cranoides is not used for creeping, and is devoid of muscle. It consists of a thin membrane, much of which forms the fl oor of the mantle cavity. The foot’s sole extends peripherally so that it covers the same area 7.4 Calyptraeoidea: Cup-and-Saucers, Bonnets and Slippers 119 ventrally as the mantle does dorsally, above it. It is as though the animal has two mantle lobes, dorsal and ventral, that are nowhere connected. The ‘ventral valve’ is cemented fi rmly to the underlying rock and the shell muscles serve as adductors, closing the free ‘dorsal’ valve tightly over it. Some hoof snail species (Hipponix conicus, Fig. 7.21 , of broad Pacifi c distribution; and H. australis of southern Australia) actively choose to settle on other sea snails as their hosts, and there they specifi cally prefer to position themselves on the outer lip of the host’s shell. A wide variety of large and small snails serve as involuntary hosts including turbans, abalones, and also predatory and scavenging snail groups. The hoof snails’ shells assume the contours of the host sea snail surface and they erode a site on the host’s shell, the foot secreting a callus in the scar and even forming a small domed pad. Thus positioned on the outer lip of its host, the hoof snail lifts the anterior margin of its shell and, using its extendable and very mobile trunk, gropes about and grasps food particles from the sediment. It also somehow benefi ts from the fl ow of water leaving the mantle cavity of the host in the exhaling current. There may be one or very many hoof snail individuals on each host shell, frequently growing on top of each other. Although relatively immobile, hoof snails of these two species are capable of limited movement at any stage of life. They move slowly, the rate being determined by the (slow) rate of growth of the host, as they continuously need to keep up with the host shell’s growth rate to retain their position on its outer lip. If the host happens to burst into a sudden speedy rate of rapid growth, the hoof snail may fail to keep up and in such cases it trails along at a distance from the host’s shell lip (and remains hungry). Snail-dwelling hoof snails fulfi l and complete their life cycle while dwelling on the same individual host. Hoof snails change sex during their lifetime. At fi rst each individual is a male equipped with a long penis for delivering sperm, and later on he becomes a female in which the male copulating organ is absorbed into the body and a female system is developed. The new female now produces ova and receives sperm. Hoof snails resemble cup-and-saucers in this characteristic. The switch in sexual development is affected by the proximity of other individuals. An initial colonising veliger individual will settle on a host snail, presumably go through a brief male phase and then develop into a female (sometimes with a rudimentary penis). She will then attract other veligers, which after metamorphosis will become males. Later she will be fertilised, produce egg capsules and die, and a succeeding individual will change sex from male to female. Consequently, a single host snail may contain either solitary hoof snail females, small undifferentiated juvenile individuals, or clusters comprising a large female with smaller, younger attendant males and undifferentiated juveniles. The presence of a female induces adjacent individuals to develop as males, each with a large and elongate penis capable of extension well beyond the margin of the male shell. Males are usually attached on the right of the female, close to her genital pore, and they often erode a notch on the edge of her shell to allow easy copulation without shell lifting. A single female may carry two males, with a notch for each. Females of some hoof snail species brood the fertilised eggs inside the mantle space, and eventually they hatch as veligers that swim into the plankton. These veligers are unique among sea snails in that they have a double 120 7 Grazers and Filter Feeders

Fig. 7.22 Slipper-shell, Crepidula aculeata (3 cm), north-western Atlantic

embryonic shell: an ordinary embryonic shell consisting of a mesh of protein strengthened by calcareous matter and an additional, external shell that is thin, transparent and glassy, and consists of only protein mesh. This external shell is formed by detachment of the shell envelope (the periostracum) from the proper shell. This double shell structure may perhaps assist in fl oating. The young of other bonnet species hatch in their crawling stage (e.g. H. australis , H. cranoides of the north-eastern Pacifi c). These species have eggs that are large and yolky and are kept in fi ve to ten elongated brood sacs inside the mantle cavity, attached to the underlying foot. Some 20 embryos grow in each sac, the whole brood is at the same developmental stage, and the escaping juveniles settle on the mother’s host, around its shell’s outer lip. These young individuals have a spiral protoconch that, with increasing size, is eroded off the top of the shell, and a calcareous scar takes its place. Slipper-shells ( Crepidula, Figs. 7.22 and 7.23) also have a shell with a much reduced spire resembling a cap. The large aperture on its interior is covered by a fl at shelf extending half of its length from the rear of the body forwards, and attached to the shell along both sides of the aperture. Attachment of the shell muscle to the foot is across this transverse shelf and the foot is used as a sucker to adhere the animal to the underlying substratum, whether rock or another shell; hence, this sea snail also loses its creeping ability at an early age. Slipper-shells commonly live in stacks of up to 12 animals, with large snails at the bottom of the stack and becoming progressively smaller towards the top. Stacks of adults are attached to the substratum and are incapable of moving. The adults are active suspension feeders that depend solely on fi lter feeding to meet their nutritional requirements. By beating cilia on their large gill, they generate a water current through the mantle cavity and trap food particles on a mucous sheet lying across the frontal surface of the gill fi lament. Small juveniles of some species are, however, motile, and can scrape algae from the substrate in addition to fi ltering. Crepidula fornicata of the Atlantic (Fig. 7.23 ) lives in stacks where the large, old individuals at the base of the chain function as females, transitional individuals are in the middle and small, young individuals at the top function as males. This sexual 7.4 Calyptraeoidea: Cup-and-Saucers, Bonnets and Slippers 121

Fig. 7.23 A pile of eight slipper-shells, Crepidula fornicata (4 cm), north Atlantic

structure of the stack is due to the fact that slippers, like hoof snails, are sequential hermaphrodites: each individual starts off as a male and eventually becomes a female. Sex change is environmentally mediated, the timing of sex change depending upon the association with other individuals. The presence of a mature female infl uences associated juveniles to develop as males. If a juvenile settles alone on a rock rather than joining a colony, the male phase may be brief or even non-existent, or may persist only until a younger individual settles on it and induces the change to female. After being internally fertilised by males that stack on top of her, a female will brood her eggs. The hatching larvae swim into the plankton and eventually settle on hard substrata. Maturation from juvenile to male and the maintenance of the male state is promoted by pheromones released by neighbouring females. In the absence of such cues, juveniles pass through an accelerated male phase to become females sooner. The timing of sex change is fl exible and is greatly infl uenced by social interactions. The presence of more than one male in a stack results in multiple paternities and the ability of more than one male available to fertilise the ova of a single female leads to sperm competition. This competition of more than one male for the fertilisation of ovules could effectively reduce the reproductive success of males in a stack and may cause individual males to change sex earlier than they would in the absence of competition. It was recently found that in one stack, consisting of a single female and several males stacked on top of her, one male within the stack had fathered the majority of offspring in her brood, and that he was the largest male and the one closest to the brooding female. In general, the greater the number of mature males in the stack the lower the reproductive success of the 122 7 Grazers and Filter Feeders dominant male, suggesting that sperm competition could be a driving force in determining male reproductive success, and the timing of sex change in Crepidula fornicata . Though the older larger males closest to the female have a competitive advantage they can fall victim to decreased reproductive success, as a result of increased sperm competition. Some slipper species such as Crepidula convexa of the north-western Atlantic and C. aculeata from Florida (Fig. 7.22) brood their eggs to direct development. The capsules comprising the egg mass are compartmentalised in early development. Later, the compartment walls break down and there is a decrease in the number of embryos, perhaps suggesting the occurrence of cannibalism among the embryos. In Crepidula fecunda from southern Chile, which lives in stacks of up to ten individuals, there seems to be an association between the change in sex, the motile versus non-motile stage and the feeding strategy. The males move about around the stack copulating with the females, and while roaming about they graze the substratum. Females are completely sessile and form the base of each stack. The female deposits her egg capsules on the substratum beneath her shell and then cares for the capsules. Being sessile (perhaps because of this restriction imposed by parental care) she is unable to move about in search of new grazing areas; and accordingly she shifts from grazing, as she did when a juvenile, to suspension-feeding, that she now practices as an adult. Sessile slippers are prone to attacks by predatory sea snails such as Urosalpinx cinerea, the oyster-drill (Fig. 8.33). The slipper has certain behavioural defences against such predators. Crepidula fornicata may lift the edge of its shell, extend the head and prick or rasp with the radula at the foot of the approaching predating oyster-drill, which instantly retracts into its shell; after such repeated attacks on it, the oyster-drill usually moves away. Also, Crepidula fornicata mounted by an oyster-drill may slowly and repeatedly rotate its shell in a horizontal plane at a constant rate and through a constant arc. If this action brings the oyster-drill’s shell to bear against an obstacle, motion ceases and the slipper maintains the pressure until the oyster-drill is dislodged. These aggressive tactics are adaptive defensive measures for a nearly sessile prey that would otherwise be highly vulnerable to oyster- drill attack.

7.5 Gill Filter Feeding: General Comments

Five genera of gill fi lter-feeders have been described so far and as this mode of feeding will not be encountered again, this seems an appropriate place for a digression from the survey of specifi c sea snail groups to a review of some morphological adaptations which accompany this mode of life. Gill fi lter feeding has evolved in several sea snail groups (Table 7.1 , including some not covered in this book), which inhabit a variety of environments, from wave-beaten intertidal shores to deep-sea hydrothermal vents, and dwell on a variety of substrata from mud and sand to rocks and to sponges. Filter feeding also occurs in two fresh water groups, the Viviparidae and Bithyniidae. 7.5 Gill Filter Feeding: General Comments 123

Table 7.1 Filter feeding groups of sea snails mentioned in this book Order Super-family Family Genus Vetigastropoda Neomphaloidea Neomphalidae Neomphalus Vetigastropoda Trochoidea Trochidae Umbonium Caenogastropoda Cerithioidea Turritellidae Turritella Caenogastropoda Cerithioidea Siliquariidae Tenagodus Caenogastropoda Calyptraeoidea Calyptraeidae Crepidula Caenogastropoda Capuloidea Capulidae Capulus , Trichotropis Caenogastropoda Struthiolariidae Stromboidea Struthiolaria Caenogastropoda Vermetidae Vermetoidea Dendropoma

Fig. 7.24 The gill in a typical sea snail (left ) and in a ﬁ lter-feeder (right )

Gill fi lter feeding has evolved as a modifi cation of the cleansing mechanism of the gill. In a typical sea snail (Fig. 7.24 ) small fouling particles present in the respiratory current, such as sand grains, are swept upwards in the up-fl owing inhaling current until they reach the lower edge of the leafl ets, where ciliated mucus cells exist. The impact on these cilia by the fouling particles causes these cells to secrete large quantities of mucus, in which the particles become entangled. By beating all cilia along the leafl et edge in the same direction, the mucus mesh loaded with the particles is transported to the tip of the leafl et and dumped onto the underlying fl oor of the mantle cavity, where other cilia transport it outside the body as waste material that is ‘coughed out’ (Sect. 2.3). Filter feeding sea snails differ from typical ones in that they collect this mucus enmeshed with fouling particles as it leaves the mantle cavity and pull it into the mouth, rather than coughing it out. They do so to feed on those fouling particles of high nutritional value, such as organic-rich detritus and micro-algae. A distinctive suite of traits of the mantle cavity and digestive system is associated with the gill fi lter feeding. Filter feeding groups have a deeper mantle cavity than other groups of sea snails, and their entire cavity length is fi lled by an exceptionally elongated gill. The leafl ets on their gill are shaped into long fi laments while in other 124 7 Grazers and Filter Feeders non-fi lter feeding groups they are triangular sheets. As the number of the lateral cilia is thereby increased a more powerful current is created, so that more water moves over the gill per unit of time. The lateral cilia themselves may be elongated, and more numerous and longer cilia may be present to increase fl ow velocity. The tips of these fi lamentous leafl ets overhang a food groove on the fl oor of the mantle cavity that extends its whole length and ends on the right side of the head. Cilia in the groove move the food-laden mucus forward and the radula grasps the mucus and takes it. Merely plucking off of in-reach soft mucus is a rather limited action and this is refl ected in the rather small radula, jaws and accompanying musculature; these structures are much larger in other groups which have other modes of feeding. The oesophageal digesting glands (Sect. 2.4 ) are reduced or absent in fi lter feeders, but this is compensated for by a well-developed crystalline rod present in the stomach. It is a fl exible, gelatinous rod of muco-protein that rotates and continuously dissolves. As it dissolves, it releases amylases which break down carbohydrates and controls the stomach pH, so that the mucus holding the algal and detritus particles together is dissolved and the particles can be ingested. One might perhaps get the impression that fi lter-feeding is an all-or-nothing feeding strategy, but this is not so. In the Capuloidea, snails in which the shell is frequently covered by a thick, often spiky or hairy periostracum, the main distinguishing feature is a long lobe termed the ‘pseudoproboscis’ which is used for feeding. A modifi ed elongation of the lower lip with a groove along its upper side, this freely movable long lobe differs from the normal trunk in that it is a solid structure, not a tubular one. Among the Capuloidea, individuals of Trichotropis (Fig. 7.25) can either fi lter-feed living on small algae and other organic material fl oating in the water, or can steal food from tube-dwelling bristle-worms (Polychaeta) dwelling in the sea fl oor. Bristle-worms are also fi lter-feeders, passing water through a feathery crown of feeding tentacles and conveying particles caught on these tentacles towards the mouth, located at the base of the crown. Trichotropis steals from a wide range of bristle-worm genera including Serpula, Pseudopotamilla, Schizobranchia and Eudistylia . A stealer snail perches next to the opening of a tube-worm close to its mouth, extends its modifi ed lower lip (‘pseudoproboscis’) through the feeding tentacles of the worm and, by use of the cilia on this organ, diverts food from the worm’s mouth into its own. Although infested worms do not react to the stealing snail they grow more slowly than uninfected worms. For its part, the stealer snail grows faster when on a tube-dwelling worm than if restricted to fi lter-feeding alone, during which it barely grows at all. Trichotropis veligers dwell in the plankton where they feed on tiny algae, but perhaps their larval metamorphosis is induced by the presence of worms, and their juveniles can steal food from worms within a day of metamorphosis. This rapid onset of stealing behaviour is permitted by the development during the larval stage of the pseudoproboscis as a specialised feeding structure. Having settled on a tube and whilst growing, the juveniles remain on their worm tube, leaving it only as mature snails to mate, and this only during the reproduction season. Close relatives of Trichotropis also steal food. Capulus ungaricus , the cap-snail of the northern Atlantic and Mediterranean is a self-suffi cient fi lter-feeder in 7.6 Littorinoidea: Winkles, Periwinkles and Their Allies 125

Fig. 7.25 Trichotropis (2 cm)

food- rich waters but a thief in food-poor waters where it steals food from bivalves, other groups of ﬁ lter-feeding snails, tube worms and brachiopods. To easily reach food held on a clam’s gill C. ungaricus rasps a crescent-shaped hole along the edge of the host’s shell, so that even when the clam is shut tight the thieving snail can insert its lip and reach the food. This rasping is taken to a further extreme by related snails which drill through the central portion of the shell of scallops through the mantle and steal food from the scallop’s lips and food-gathering tracts. The parasites remain attached to the living host, with continuous access to the host’s food for such a long time that the parasite’s shell grows to mirror the shape of the host’s shell.

7.6 Littorinoidea: Winkles, Periwinkles and Their Allies

Winkles and their allies are known as the Littorinoidea (Fig. 7.26 ) and have compact ovate to conical shells with a thin outer lip, a smooth concave columella, and no umbilicus. The foot has a thin, corneous operculum with only a few spiral whorls. Winkles form a very large group of 65 genera that are abundant dwellers of the littoral habitat; the term ‘littoral’ is incorporated into their scientiﬁ c name. Some species dwell exclusively on littoral rocky shores, others are found on littoral algae, 126 7 Grazers and Filter Feeders

Fig. 7.26 Dotted winkle, Melarhaphe punctata (1 cm), Mediterranean

in estuarine salt marshes or on mangrove trees. Some winkles occupy the lower littoral, whereas others can reach high up the shore, to the littoral fringe . In general, animals of the lowest littoral spend more than 80 % of their time in the moderated and constant marine environment and 20 % in extreme and mostly dry ones; the opposite is true for organisms living in the high tidal zone. The higher a marine animal is found on the shore, the more exposed it is to environmental stresses in terms of desiccation, temperature, and inundation by rain. As a general rule for littoral animals, environmental stress sets the upper limit to a species’ zone along the shore, while biological factors usually set its lower limit. Animals of the lower littoral grow bigger and reproduce better than those higher on the shore because they are immersed in the sea longer, have a longer time to feed, and spend less energy protecting themselves from environmental stresses. These benefi ts of the low littoral are, however, counteracted by a higher mortality rate from predation and from competition for space. Thus, the zone along the shore that a littoral organism occupies refl ects its responses to very steep physical gradients on the one hand, and to biological interactions on the other. Let us now leave littoral organisms in general and focus on winkles in particular, zooming in on the small winkle Melarhaphe neritoides, found in the Mediterranean and Black Seas and also in the northern Atlantic of Europe, from to the Canary islands up to Norway (Fig. 7.27 ). Their position marks the highest zone on rocky shores that marine molluscs may reach – the zone of wave spray that the tide reaches only twice a month, on days of full moon and no moon. These winkles benefi t from dwelling in the zone that is dry most of the time by being beyond the reach of many marine predators, but they spend most of their lives under diffi cult circumstances of dry conditions and direct sunshine in summer, and of biting cold, often freezing, in the winter. Once a fortnight the tide rises, approaches the zone of this high-shore winkle species, and only when the wave spray reaches them do the small winkles emerge and move to graze on the algae and lichen growing on and in the rocks. Their zone is usually fully covered by the tide only 2 % of the time. As dry conditions set in they once again withdraw into their shell behind a tightly fi tting operculum, and secrete a thin mucous fi lm by which they adhere to the rock. 7.6 Littorinoidea: Winkles, Periwinkles and Their Allies 127

Fig. 7.27 Small winkle, Melaraphe neritoides (1 cm), north-eastern Atlantic

The small winkle thus avoids desiccation by spending most of its life enclosed in its shell behind its operculum, glued to crevices in the rock by its mucus or hiding in empty barnacle shells. It can live for up to 5 months in this state of inactivity, in which the metabolic rate decreases to only one fi fth of that when active; upon the return of sea water, it returns to activity within an hour. It can survive reduction in body water content to 66 %. It can bear fl uctuating salinities and also remain in fresh water for 11 days, and can survive many days in tidal water pools with a salt concentration three times higher than normal. The pale shell colour of the small winkle refl ects light and thereby further increases its ability to survive heavy radiation. Adaptations to the very high, almost terrestrial intertidal, occur even in the mucus. The mucus holdfast by which Melarhaphe neritoides glues to the rock remains fl uid and its secretion is extremely copious; if dislodged, a snail may remain suspended by a thick string of mucus which it subsequently ascends to regain its position. The mucus holdfast conserves moisture that would be lost by evaporation had attachment depended only on adherence by the foot. The alternation between brief periods of moving on a carpet of mucus versus long periods of inactivity spent attached by mucus requires two types of mucus. The mucus secreted by the small winkle during attachment has an adhesiveness ten times stronger than that of the movement mucus. The ‘movement mucus’ contains, in addition to 95 % water, mainly large carbohydrates with only a small addition of light-weight proteins. The ‘attachment mucus’ contains carbohydrates and proteins in approximately equal portions, due to the addition of two light-weight proteins. By secreting these additional proteins, the winkle controls the mechanics of its mucus and thus its ability to move or to adhere. The south-American winkle Echinolittorina peruviana has a shell of differentiated length and width axes. Its lateral faces are approximately twice as large as its frontal and dorsal faces. On sunny summer days, winkles of this species face the sun with their small frontal or dorsal sides but not on overcast summer or on winter days. 128 7 Grazers and Filter Feeders

The body temperature of these winkles increases more rapidly and reaches higher equilibriums when the larger lateral sides face the sun than when they face the sun with either of the smaller sides. The orientation behaviour of E. peruviana is thus thermoregulatory and permits these winkles to maintain lower temperatures on hot days. At the other end of thermal stress are freezing conditions, and the south African winkle Afrolittorina knysnaensis is freeze-tolerant to an extent that it can survive temperatures of −8 °C. Not all winkles dwell in the extremely high littoral. On those north-eastern Atlantic rocky shores, on which Melarhaphe neritoides occupies the extremely high spray zone, two other winkle species are found lower on the shore, Littorina saxatilis and L. compressa . Still lower, the mid to lower littoral is occupied by the edible periwinkle Littorina littorea. Almost constantly submerged, the brown algae of these rocky shores are occupied by Littorina obtusata and Littorina fabalis . Winkle species on the same intertidal rocky shore are thus clearly zoned in their habitats. Such zoned distribution of winkles also occurs in mangrove forests in tropical and subtropical regions of the globe. Littoraria is abundant on the mangrove trees Avicennia and Rhizophora , always climbing vertically to avoid being fl ooded by the incoming tide. As many as ten species of mangrove winkles can be found in a single locality in the mangrove forests of south eastern Asia, each broadly zoned to different heights on the trees. Littoraria species of lower tidal levels may descend in the wake of the ebbing tide to feed on algae that settle on the trunk, but species of higher tidal levels often remain at high levels on the trees during low tide, and even at spring tide periods: Littoraria pilosa can be found up to 3.0 m above the ground as the tide recedes, Littoraria albicans to 3.5 m, Littoraria pallescens to 4.5 m and Littoraria philippiana higher up at 5.2 m above the ground. Those snails of the highest vertical levels are beyond the reaches of the tide, and female individuals descend to the tidal level only to release larvae. Such high-zoned mangrove winkle species are infl uenced more by rainfall, dew and humidity than by the tide. Those winkle species that dwell at upper shore levels have typically thin, light shells that minimise the danger of displacement while attached to the rock or tree only by mucus. ‘The higher you are the drier you are’, so a thin light shell easily held by a mucous fi lm for long periods of time is advantageous in the higher zone. But, winkles with thin shells could not survive the predatory pressures of the lower zones. Species of the low shore levels have thicker shells to withstand predation by crabs. As crabs have longer foraging times on a low shore than at an upper shore, because of the tidal cycle, winkle species zoned on the lower shore are susceptible to greater predation pressures than species at higher ones. Crabs reside in the sea and can move up the shore only by following the rising tide. Therefore they can reach the very high intertidal only once a fortnight, but can reach the lower intertidal with every incoming tide. The overall intensity of crab predation thus increases towards the lower shore and seems to account for variation in shell thickness of winkles. Viewing shell thickness from the other end, as winkles of the lower shore are covered by the tide 80 % of their time, the weight of their thick shell is borne by the tide for this period of time. Furthermore, as crabs prefer sheltered shores over exposed ones, winkles on such sheltered shores experience higher 7.6 Littorinoidea: Winkles, Periwinkles and Their Allies 129

Fig. 7.28 Flat winkle Littorina obtusata (1 cm), north-eastern Atlantic

predation pressures. Hence individuals of a winkle species in sheltered habitats have thicker shells than those at the same zone of exposed ones. Many winkle species show a two to threefold variation in adult shell size among individuals of the same species. Large size is attained in favourable habitats, so individuals from very sheltered shores or low level mangrove bushes in shady areas and low in the intertidal zone, tend to be large; therefore, individuals from unusual or extreme habitats, such as very exposed shores or upper level stunted mangrove bushes in full sunlight, tend to be small. Shell shape is also correlated with zone level, and those species from higher levels generally have narrower shells with a higher spire. This trend may be an adaptive response on tropical shores, reducing the relative area of the foot that conducts heat from the substrate and also reducing evaporation and water loss. In temperate regions, exposure to wave action is of more signiﬁ cance, and Littorina saxatilis from more exposed localities have lower spires and larger apertures than those from sheltered ones. A large aperture enables more surface of the (larger) foot and increases its ability to hang on to the rock and withstand wave action. A somewhat special case among winkles, the smooth globular shells of Littorina obtusata (Fig. 7.28) and of L. fabalis are of the same general size, shape and colour of the gas bladders common on the brown North Atlantic alga upon which they frequently live, the egg wrack Ascophyllum nodosum . Winkles have a wide range of shell colours. Shell colour is best described as consisting of a ground colour, either a shade of white-to-yellow or orange-to-pink, sometimes superimposed with a pattern of dark pigment, usually brown or black. Dark pigment may be deposited on the ground colour in the form of spiral dashes or continuous lines. 130 7 Grazers and Filter Feeders

Fig. 7.29 Littorina compressa (2 cm), north- eastern Atlantic

Differences in shell colour frequency in European winkle species can sometimes be explained by selection for concealment from visual predators. In Littorina compressa of Wales, U.K. (Fig. 7.29 ), populations with a high frequency of red shells are all from red sandstone, suggesting that visual selection is restricting their distribution to the background that they match most. Furthermore, red shells of this species are found mainly on red sandstone on sheltered shores; their frequency decreases and that of white shells increases on red sandstone shores that are more exposed. This difference may be because barnacles, which occupy the same vertical zone as L. compressa , are more abundant on exposed shores. Barnacles partly cover the red rock and create a partly white background upon which white shells, rather than red, are hidden. A dark-striped pattern breaks up the characteristic shape of the shell and also resembles the colour of the dark sutures between barnacle plates. Winkles with yellow shells are found mainly on sheltered shores, where the brown alga Fucus is abundant. When the tide is in and the algae are fl oating and spread out, a yellow shell located on the under surface is well concealed. The fl at winkle Littorina obtusata usually has a shell that is mainly green or brown-to-black, colours that conform to that of Ascophyllum nodosum, the dominant brown alga on which the snail is commonly found; yellow shells are only rarely found. The closely resembling species Littorina fabalis have a shell that is mainly yellow or brown-to-black, only rarely green. Visual predation from under water by blennies may well be an important agent in selecting for the different shell colours of L. fabalis . The yellow shell conceals the snail on a frond of F. serratus when viewed against the light from below, the attacking position of many fi sh and crabs. The dark, brown-to-black morph conceals the snail when it sits on top of the frond and is seen from above, the reconnaissance position of a bird. The relative activity 7.6 Littorinoidea: Winkles, Periwinkles and Their Allies 131

Fig. 7.30 Winkle, Littoraria intermedia (2 cm), Indo-Paciﬁ c

of these two predators determines a selective advantage of different colours of the different species. In general, both species are found on sheltered to moderately exposed shores. On sheltered shores, Littorina obtusata tends to be green and L. fabalis yellow; on exposed shores, both species tend to be brown-to-black. The frequency of Littoraria colour forms on tropical shores (Fig. 7.30 ) varies greatly between mangrove habitats in the tropical, with brown shells predominating on Rhizophora trees, while yellow and pink shells are most numerous on Avicennia and Sonneratia trees. Winkles fall prey to many groups of predators including birds, ﬁ shes (especially blennies), dog whelks and crabs. Green crabs (Carcinus maenas ), of northern Atlantic tide pools, consume individuals of the edible periwinkle Littorina littorea (Fig. 7.31 ) at night and along the shore at high tide during the day. The amount of time required for a green crab to consume a periwinkle depends on the snail’s size: small snails of up to 9 mm shell height are crushed and consumed within 3 min. Crabs cannot consume snails large than 18 mm, but they destroy medium-sized snails by cracking the shell, tearing off bits of tissue and then resuming shell cracking to expose more snail tissue. It takes a green crab about 10 min to break the shell and consume the snail within. Edible periwinkles have evolved alarm or escape responses to the juices produced by the injured tissues of crushed individuals of their own species. When crushed individuals of their own species (or their juices) were added to rocky intertidal pools, periwinkles crawled to protected niches such as rock crevices, under rocks and algal fronds, where they were less visible and the crab required more time to ﬁ nd and attack them. In responding to such juices they quadrupled their crawling 132 7 Grazers and Filter Feeders

Fig. 7.31 Periwinkle Littorina littorea (3 cm), north-eastern Atlantic

speed and hid within 10 min, and this approximately equals the 10-min predation time of a medium sized periwinkle. While small snails are crushed and eaten too quickly to allow nearby periwinkles the time to hide, increased distance from the predator gives the winkles time to fi nd shelter. Size is a winkle’s primary line of defence against predators such as birds, fi shes and crabs, and the alarm response is a complementary anti-predator behaviour. This response is not unique to winkles, occurring in other snail groups and in fi shes, amphibian tadpoles, sea urchins and sea anemones. Whereas one behavioural response to predators involves escape, another involves predator avoidance. The salt-marsh winkle Littoraria irrorata (Fig. 7.32 ) is very abundant in coastal salt marshes of the north western Atlantic, in which the main habitat plant is the smooth cord-grass Spartina alternifl ora. With each advancing tide this winkle climbs from the sediment onto the upright blades of dead cord- grass. Having better vision than most sea snails, it orientates itself towards stems of the cord-grass by visual clues. When placed on the sediment during a rising tide, it moves towards the nearest plants either up-shore or down-shore. Major predators of the salt-marsh winkle include the blue crab Callinectes sapidus and the predating snail Melongena corona (Buccinoidea, Sect. 8.7 ) and it is to avoid these predators that the winkle climbs up the cord-grass. Blue crabs swim to the surface of the water at high tide, plucking off and crushing only intermediately sized winkles, at or near the surface. Interestingly, winkle climbing is partly size-dependant, as the sizes most vulnerable to crabs are those more likely to climb. Approximately 25 % of the winkle population leaves water at high tide, where they are entirely beyond reach of the crabs. Predatory snails do not pluck winkles from the water surface, but they 7.6 Littorinoidea: Winkles, Periwinkles and Their Allies 133

Fig. 7.32 Marsh winkle Littoraria irrorata (2 cm), on smooth cord grass, north- western Atlantic

prey upon winkles that fall to the salt-marsh ﬂ oor, or that spend the high tide submerged on short plants. The winkle is attacked by pushing its operculum aside. Unsurprisingly, salt-marsh winkles placed in contact with Melongena corona or even with its mucus show a strong escape response, in lab results. Both predatory snails and crabs move faster than the salt-marsh winkle and its climbing behaviour at every advancing tide thus represents a form of avoidance behaviour to reduce predation that may come with the tide.

7.6.1 Feeding

The substratum upon which a winkle lives largely determines its diet. Rock-dwelling winkles are opportunistic grazers of the rock, taking in diatoms, spores and young green, brown and red algae. Winkles of the high shore also take in lichens. Plant- dwelling winkles, especially those living in mangroves, may eat dead and rotting material rather than live plants. The fl at winkle Littorina fabalis of the lower shore of the north eastern Atlantic lives on the fronds of the brown alga Fucus serratus (the saw wrack) where it feeds on micro-algae and sessile invertebrates (bryozoans, serpulid worms, barnacles and hydroids) that often settle on these large algae; it feeds also on Ascophylum nodosum (the egg wrack). In a broadly similar manner, in the shallow sea meadows of eel-grass Zostera marina of Nova Scotia (north eastern America), tiny winkles (perhaps of the species Littorina neglecta) reach enormous densities of 45,000 snails per square metre; and they control the amount of epiphytes 134 7 Grazers and Filter Feeders and detritus covering the eel-grass leaves. Species of Littoraria in mangrove forests dwell on the leaves of Rhizophora trees, frequently grazing on the bare hairs found on undersides of their leaves. Other mangrove species of Littoraria dwell on the trunks and stilt roots of Rhizophora trees, where they graze the surface layer, ingesting diatoms and other algae. In salt marshes along North America’s Atlantic coasts, the marsh winkle Littoraria irrorata actively grazes on live leaves of the salt marsh cordgrass Spartina alternifl ora , but it does so not to feed, but to prepare a favourable environment for fungal growth; and then to consume the invasive fungi. When grazing live plants the marsh winkle does not consume the live tissues; instead, it cuts and maintains long gashes into the leaf blades. As fungi (mainly the ascomycetes Phaeosphaeria and Mycosphaerella) settle and fl ourish in these gashes, the snails feed on these fungi. Further, the marsh winkle deposits its nitrogen-rich droppings (faecal pellets) on the fungus-infected wounds, thereby fertilising the fungus and enhancing its growth. Marsh winkles that eat much fungus thrive and also most of their progeny survive, whereas leaf-fed winkles hardly grow, and many of their progeny die. Another category consists of those plant-dwelling winkles that live upon large algae and feed on the mature plant itself. Littorina obtusata (Fig. 7.28 ) lives on the brown alga Ascophyllum nodosum (the north Eastern Atlantic egg wrack). Most winkle species avoid encountering it, as the alga produces noxious chemicals that repel grazers. Littorina obtusata is attracted to the alga, responding positively to the alga’s exudates, and is one of the few grazers capable of eating this plant. It actively rasps deep into the algal tissues, often leaving visible gouge marks in the frond. Littorina obtusata is even more strongly attracted to the bladder wrack Fucus vesiculosus. In a broadly similar manner those species of Littoraria in mangrove forests that dwell on the leaves of the Avicennia trees frequently graze on the bare hairs found on the undersides of their leaves. Mucus trails left by snails may also play a role in nutrition. A layer of mucus or of its degraded products covers much of the rock surface in intertidal habitats, and micro-algae stick to them. Mucus trails containing micro-algae induce trail- following by the edible periwinkle Littorina littorea, and increase its feeding rate in comparison to trails without micro-algae. Furthermore, when tracking over freshly laid trails by other individuals of the same species, the edible periwinkle produces only 27 % of the mucus laid by the marker snails. This saving of energy is considerable in the context of an animal which expends large amounts of energy on mucus production. Trail following may have the added benefi t of enhancing nutrition, because food particles may become embedded in the mucus.

7.6.2 Reproduction

Winkles fertilise internally, as do most advanced snails. The males, somewhat smaller than the females, have a large muscular penis enriched with various glands. When relaxed, the penis is folded back into the mantle cavity where it lies against the head and foot. During copulation, it enters the female’s genitalia and sperm 7.6 Littorinoidea: Winkles, Periwinkles and Their Allies 135 passes to her through a deep groove. Some genera (Littoraria ) also have a bulbous sucker-like structure on the penis, whose glandular secretions perhaps might secure the base of the penis when placed inside the female’s mantle cavity; or perhaps remove previous sperm. Penis morphology is highly variable between winkle species, but broadly fi xed within a single species. This might perhaps suggest that penis shape is of importance in species recognition and that it may perhaps be an isolating mechanism preventing inter-specifi c mating. Among many winkle species the males are rather indiscriminate in their choice of mates, and the success of copulation may depend on the recognition response of the female, a point discussed further on. In some winkle species the penis is shed after the mating season is over, and a new penis regenerates within 3–5 months, towards the next breeding season. Copulation occurs under moist conditions, during or after high tide, after rainfall, or early in the morning. Males search for females, often indiscriminately mounting the shell of any individual they encounter, as the mounted partner’s sex can only be determined by attempting to insert the penis into the female genitalia. If the shell beneath is of another male, the pair soon separates. If it is a receptive female, the pair copulates, the male inserting his penis under the lip of her shell aperture and into her genital opening. Competition among males for a female may occur. Male Littorina subrotundata of the northern Pacifi c preferentially copulate with larger females. Female fecundity increases with female body size, and males prefer to mate with larger females which are physically capable of producing either a greater number of clutches or more eggs per clutch. Males in another species, the edible periwinkle L. littorea , also mate with larger females; furthermore, they also spend more time copulating with healthy rather than with heavily parasitised females. Apparently male winkles do not indiscriminately distribute their sperm among as many females as possible; they strategically allocate sperm to females that will produce the greatest number of offspring. Large males of Littorina subrotundata physically out-compete smaller males for access to females. They are also more likely to copulate with virgin females than with females which have copulated recently, suggesting that males can detect the presence of rival male sperm within a female’s reproductive tract. Preferential copulation with virgin females is advantageous in mating systems in which the risk of sperm competition is high. Duration of copulation varies, and in some species may last up to four and a half hours. The male may remain attached to the female shell for several hours after copulation, in the copulation position but without genital contact. Prolonged mate guarding could be the male’s way of reducing the probability of female re-mating with other males and thereby ensuring that only his genes contribute to the offspring. Indeed, the guarding of reproductive females after copulation is a generalised advantageous behaviour in the animal kingdom. Females often copulate with more than one male and can store sperm for several months, resulting in a high degree of multiple paternities in the offspring. Inter-specifi c mating may occur during reproduction of winkles found in overlapping zones. Reid ( 1986) recorded copulation in fi ve winkle species in 136 7 Grazers and Filter Feeders

Queensland, Australia. Over one year, he found that, of 1,200 copulating pairs, the individuals belonged to different species in only 4 %. In a similar study on four species in Western Australia, he found that the frequency of inter-specifi c pairing was increased to 7 %. It is not known whether transfer of sperm occurs during inter- specifi c mating, but no hybrids with intermediate shell or anatomical characters have been discovered. This provides evidence supporting the theory that species we defi ne by morphological criteria may indeed be true biological species, namely isolated groups of interbreeding populations (Reid 1986 ). Spawning is highly diverse among different groups of winkles. In the more primitive genera of the Littorinoidea, such as Lacuna and Laevilittorina , the gravid female produces benthic jelly egg masses from which veligers hatch and swim into the plankton. In the more advanced genera (e.g. Melarhaphe ) the female forms many small capsules, each (usually) containing one egg. The female descends to lower intertidal regions during the spawning season and, when covered by the tide, she releases her egg capsules in which the egg develops, fi rst to a trochophore, then to a veliger which hatches from the capsule into the plankton. When ready to metamorphose it settles in a rock fi ssure or inside an empty barnacle on one of the rocks of the lower intertidal zone and metamorphoses to adult form. Within a day, the tiny snail begins creeping upwards and migrates to the upper intertidal zone. Winkle species of other advanced genera also produce egg capsules, and capsule shape is highly diverse. Each capsule in capsule-producing species of Littoraria is a more or less symmetrical biconvex disc of approximately 0.3 mm and typically contains a single egg. The capsule is often surrounded by a circumferential fl ange or lamella, which in some species is turned down to form a fl otation skirt. Capsules hatch within 1–7 days and the veligers feed in the plankton for 8–10 weeks before settlement. The female in other species of this genus may brood and keep her offspring as embryos among her gill leafl ets (inside her mantle cavity) to veliger stage. The duration of gill brooding varies from 4 days in tropical species to 17 days in temperate ones, and the female eventually releases early veligers into the plankton. Some Littorina species lay egg masses, but the offspring undergo their entire development in the egg capsule and eventually hatch as crawl-away miniature adults (direct development). Other species of this genus retain the capsules with their embryos within a special brood pouch, formed from the distal section of the egg duct, until after metamorphosis; eventually they too emerge as small juveniles and crawl away. Within the genus Littorina , a life history strategy that includes spawning eggs to the sea that hatch as veligers, swimming and feeding in the plankton, represents the ancestral reproductive condition, and that which includes direct development to juvenile snails is a derived spawning strategy and more advanced. It is remarkable that even in those winkle groups in which the entire development to a crawling sea snail occurs inside a capsule, the encapsulated embryo develops a large, ciliated velum. This large ‘feeding sail’ is not used for swimming: the embryo cannot swim if prematurely removed from the egg capsule. A large velum may provide a large surface for assimilating capsule nutrients. Unlike species with veligers which feed in the plankton, the velum of species with direct development 7.6 Littorinoidea: Winkles, Periwinkles and Their Allies 137 plays a substantial role in the uptake of nutrients inside the capsule. Ciliated cells on the velum, and also on the foot of the embryo, actively take up nutrients and enable intra-capsular growth and development through all embryonic phases to adult form. The velum cilia are shorter than in hatching veligers, and they rotate the embryo within the capsule to enhance oxygen diffusion through the benthic egg masses and to stir fl uids that enhance feeding. In the confi ned and more viscous environment of the egg capsule, short cilia probably function more effi ciently than long cilia which might not have the space to move effi ciently. These four methods of reproduction in winkles might be partly related to species dispersal and shell colour variation. In some winkle genera, those species which have plankton-dwelling larvae may have considerably less shell colour variation than those that produce miniature adults directly. Shell colour of some winkle species varies across localities and correlates with the colour of the substratum on which they are found, be it rock, plants or animals. It may well be that winkles which inhabit a very heterogeneous habitat produce adult offspring directly which remain near the parent, resulting in each small population having a shell colour more closely adjusted to its local environmental conditions (other factors remaining equal). Species with plankton-dwelling dispersal tend to have a narrow range of shell colours, whether because their habitat is more uniform or because they can tolerate the colour variations that occur in their habitats. Melarhaphe neritoides varies only from black to light grey (Fig. 7.27 ), and inhabits the spray zone of semi-exposed to exposed northern Atlantic shores where the rock is often uniformly covered with black lichen. One outcome of this widespread, relatively uniform shell colour is that snails from one site are able to colonise similarly coloured neighbouring sites, providing the species’ general ecological requirements are met. Therefore, in cases of either a local decrease in population size or a local expansion of favourable environmental conditions, plankton-dispersal enables rapid recruiting of new members and colonisation of suitable new habitats. Plankton-dispersal also enables a rapid spread of successful mutations. Among the species which lack a plankton-dwelling stage, some lay eggs whereas others bear live young. Live-bearing habits may perhaps be related to the fact that these species occupy the upper zone of the littoral. Eggs deposited in the upper littoral would be exposed to long periods of desiccation when the tide is out, and under such conditions live-bearing could be advantageous. The many adaptations of winkles to a near-terrestrial lifestyle might perhaps seem to make them suitable candidates for conquest of land. One family of the Littorinoidea, the Pomatiidae, has indeed liberated itself from dependence upon the sea and has evolved to live a completely terrestrial lifestyle. Pomatias (Fig. 7.33 ) is sometimes commonly named the ‘winkle-come-ashore’. Many details of its morphology still closely resemble that of winkles, but the gill has become reduced to a few mere folds of skin and the mantle cavity, equipped with many blood vessels, serves as the major breathing organ. The foot is divided into two parallel longitudinal sides that are lifted alternatively when in locomotion; when one side moves forward 138 7 Grazers and Filter Feeders

Fig. 7.33 Pomatias olivieri (3 cm), Levant. (From Heller 2009, courtesy Pensoft, Soﬁ a )

the other side is ﬁ xed to the substrate and serves as an anchor; the end result is somewhat similar to the scufﬂ ing walk of some terrestrial vertebrates. As in other winkles, the female is slightly larger than the male. After copulation she digs a small chamber in the soil into which she lays her eggs, covering each one with a coating of soil to serve as a source of calcium for the developing embryo. However, beyond Pomatias and its allies, winkles as a group are not the ancestors of the dominant group of land snails. Throughout evolution they have largely remained on the margin between sea and land, as if the biblical words to Moses referred to them, “For thou shalt see the Land afar off; but thou shalt not go there” (Deuteronomy 32: 52).

7.7 Cypraeoidea: Cowries, False-Cowries, Smallips and Relatives

Cowries (Cypraeoidea) have extremely smooth, symmetrical, domed shells with a glistening glaze; they lack a spire, and have a long slit-like aperture lined by a series of ridges on either side. The domed shape is due to all the early whorls being completely conﬁ ned inside the last whorl (Figs. 7.34 and 7.35 ). There is no operculum in these species. The cowry group consists of some 60 genera. Cowry shells’ highly polished and beautifully patterned upper surface and the elongated crevice-like aperture on their lower side have tremendous aesthetic appeal, and have been collected by peoples of widely different cultures over thousands of years. The ancient Romans, impressed by the fancied resemblance of the shell aperture to a woman’s genital oriﬁ ce, named this mysterious sea snail the ‘shell of the act of love’ ( Concha venerea, Fig. 7.36 ). Centuries later, its chubby, humped shape led the Italians to name it ‘a tiny piglet’ (Porcellana, Fig. 7.34 ). 7.7 Cypraeoidea: Cowries, False-Cowries, Smallips and Relatives 139

Fig. 7.34 Cowry, Lyncina camelopardalis (6 cm), Red Sea and western Indian Ocean

Fig. 7.35 Cowry, Erosaria annulus (2 cm), Indo-Paciﬁ c

Scientists name this sea snail shell ‘the one of Cyprus ( Cypraea)’ because Cyprus was the island of Aphrodite, the goddess of love of Greek mythology. The Hindu in India named it ‘kauri’ (a variant of the term ‘kaudi’ that originates in the Tamil language ‘kavatsi’), and from here the word ‘cowry’ in the English language. 140 7 Grazers and Filter Feeders

Fig. 7.36 Cowry, as described by Konrad Gesner (1560 ); “Porcellana” and “Conchae venereae” emphasized in yellow , by me (Courtesy of Hava Noverstern, curator of the Edelstein Collection, National Library of Israel)

Fig. 7.37 Cowry, Mauritia grayana (6 cm), Red Sea and western Indian Ocean

7.7.1 Mantle Flaps

Cowries differ from other groups not only in their unusual shell but also by their magnifi cent mantle with two huge fl aps, one on each side. These fl aps extend through the aperture, spread over the shell and cover most of the surface of the shell, keeping it shiny and preventing other organisms from settling on it. The upper surface of these fl aps is plain and smooth in some groups, but tuberculate or with small fi nger-like papillae in others, which branch or which fuse at their bases into a series of tufts (Figs. 7.37 and 7.38 ). When fully spread over the shell, these mantle fl aps with their tufts or other decoration disrupt the symmetric silhouette of the snail and aid to conceal and camoufl age its glistening shell. Most species have very thick and conspicuously coloured mantle fl aps. Thus Luria isabella has pitch black fl aps, and Cribrarula cribraria has red ones. Cowries such as Blasicrura teres and C. cribraria , in which the fl aps are orange to red, are frequently found on red or orange encrusting sponges; all these species are of the 7.7 Cypraeoidea: Cowries, False-Cowries, Smallips and Relatives 141

Fig. 7.38 Cowry, Erosaria nebrites (3 cm), Red Sea and Indian Ocean

Indo-Pacifi c. Talparia talpa (of the Indian Ocean and western Pacifi c) has a strongly tuberculate grey-green mantle that resembles certain sea-cucumbers distasteful to many fi shes. Some other species have fl aps that are so thin that the shell colour and pattern shows through them. When fully spread out, the two huge mantle fl aps cover only most of the surface of the shell but not all of it. A wavy line, the ‘mantle mark’, frequently cuts across the colour pattern of the hump of the shell and marks the line of the area the two fl aps leave exposed. The details of this stripe may vary among individuals within one species. The mantle fl aps of some species are glandular, and secrete a very acid liquid when the sea snail is molested. Further disturbance of the snail causes the cowry to gather its mantle fl aps, breathing tube and snout inside the aperture, thereby exposing its impenetrable shell. The polished, glazed surface of the shell is formed by the mantle fl aps. When covering the shell, they coat it with a layer of glossy chalk that they excrete. Pigments from special glands also located on the mantle fl aps are mixed into the glaze when it is formed. The pigments are attached to the protein component of the shell matter that is incorporated between the calcium carbonate crystals; different arrangements of pigment cells and different rates of secretion by the mantle produce different colours and patterns in the shell. A shell may be covered by two to three succeeding layers of glazed chalk, like the layers of a transparent lacquer. Each layer has its series of colour blotches in positions broadly similar to the preceding layers. Seen through the dark blotches of the youngest layer, those blotches of the older layers are often seen as pale shadows with slightly hazy borders.

7.7.2 Breathing and Feeding

Cowries are nocturnal sea snails which hide beneath boulders and rocks during the day and emerge only in the evening twilight to feed. The breathing tube protrudes in front; the incoming current enters the respiratory tube through the front part of 142 7 Grazers and Filter Feeders the aperture and the outgoing current is discharged from behind. There is a short trunk below the breathing tube that functions in feeding, but cowries lack jaws. Most cowries dwell on hard substrata of basalt, granite or coral, and are opportunistic omnivores that feed on a wide variety of sessile organisms settling and living on these substrata, such as green and red algae, sponges, worms, tiny snails and foraminiferans. Blasicrura teres feeds mainly on sponges whereas Monetaria annulus (Fig. 7.35 ) is predominantly herbivorous and dwells in sea grass beds found in soft substrata.

7.7.3 Reproduction

Sexes in cowries are separate, and during copulation, the male approaches the female and inserts his penis into her genital pore; fertilisation is internal. The female packs her eggs into small capsules and, when laying them, turns around in circles. The egg capsules appear through the posterior aperture of the shell, and muscular action then moves them along a groove formed by an infolding of the sole of the foot. When the capsules reach the middle of the foot they are pressed by her foot and attached to the substratum, of coral rubble or underneath boulders. Each capsule contains several hundred eggs and the capsules are embedded into the mucus in groups of several dozens to several hundreds, depending on the species. A female cowry’s entire egg mass may contain up to half a million fertilised eggs. The female guards her egg mass and attends it by sitting on it, cleaning it and responding aggressively to intruders. After 2–3 weeks of development, veligers hatch from the eggs and swim into the plankton where they feed on tiny phytoplankton fl oating in the sea and grow rapidly, adding another four whorls to their shell and growing, often to about 4 mm. From this age the veliger seeks to settle, alighting on a suitable substratum, and metamorphoses to a young snail. The shell now grows as each new whorl is secreted by the glandular surface of the mantle, developing spirally with thin elongate walls and a spire, as in other sea snails, and its colour is usually a dull uniform cream-to-grey or brown (Fig. 7.39 ). The left mantle fl ap partly covers the shell during the juvenile stage, the right fl ap remaining mainly within the shell aperture. Only when the individual matures and forms its last body whorl is the right fl ap extended most of the time. It is only then that the adult colour pattern is embedded on the shell. This whorl is exceptionally swollen; it encloses all previous whorls and its outer lip folds inwards towards the inner lip. Ridges are formed along the margins of the narrow aperture, and they both strengthen the base of the shell and channel the in-and-out movement of the mantle fl aps. Once the outer lip turns inwards, the cowry cannot grow any further. All subsequent secretions of chalk will be devoted only to coating the back of the shell with colour-patterned glazed, and to thickening the ridges on its ventral side. In a typical adult cowry the remnants of the spirally coiled juvenile shell can be distinguished only by sawing through the shell. 7.7 Cypraeoidea: Cowries, False-Cowries, Smallips and Relatives 143

Fig. 7.39 Cowry, stages in development of the shell, from juvenile to adult

Direct development to crawling juveniles occurs in some cowry genera, such as Zoila, Notocypraea and Austrocypraea of Australia, and in some Cypraea species of South Africa. The females of these genera lay egg masses among sponges, bryozoan colonies or on the undersides of rocks like other cowries, and brooding lasts 40–60 days. However, only one embryo develops in each capsule and it hatches at a crawling stage. A female usually lays 20–30 capsules during a single spawning event, thus producing a mere 20–30 crawl-away juveniles. These numbers should be compared with the 20,000 larvae produced each time by Cypraea helvola of the Indo-Paciﬁ c, a species producing veliger larvae.

7.7.4 Cowry Predators

Major predators of cowries are octopuses and fi shes. An octopus usually grasps the cowry and gouges a small hole into the shell by combined use of its radula and acidic secretions. When the hole is bored through the shell the octopus injects a paralysing venom through it. The venom weakens the shell muscle, and the octopus then pulls the snail out through the shell aperture. Many reef fi shes, such as wrasses (Labridae) are opportunistic omnivores that feed on cowries by crushing their shell. Predator snails also feed on cowries: Conus textile (Sect. 8.9, Fig. 8.49 ) fi rst injects venom into the cowry’s fl esh by use of its hollow radula tooth and then everts and extends its stomach into the shell through the slit of the aperture and ingests the fl esh completely. Some tropical crabs are able to break a cowry shell. Protection from predators is a major function of a sea snail’s shell, and the domed shape of the cowry’s shell is an inherently strong structure. Stresses impinging upon it tend to be transmitted throughout the plane of the shell rather than directly across the shell, thus avoiding fracturing at the points of stress. The domed shape of the 144 7 Grazers and Filter Feeders shell is more advantageous against attacking crabs which fi nd it diffi cult to grasp and manipulate with their claws. As a further anti-predator behaviour, some cowry species, such as Blasicrura teres , shed the tip of their own foot when molested, leaving it in the hands of the predator while they crawl away. Cowries have been used by man as ornamental objects, amulets, and as a form of money. The special status of cowries in human culture is presented in Sect. 11.1 .

7.7.5 Ovulidae, False Cowries

False cowries, known also as egg-cowries or spindle-cowries (Ovulidae) are closely related to the cowries, and generally the two groups’ shells resemble each other. However, the false cowrie’s shell is narrower and shaped like a pear, egg or lance, with a very long aperture. Usually it is entirely white but in some species it is a beautiful rich monochrome pink or red (Figs. 7.40 and 7.41 ). They resemble cowries in that the shell is smooth and shiny, the spire not seen outwardly, the outer lip faces inwards and two mantle ﬂ aps cover the shell. False cowries tend to occur at greater depths than most cowries, but the main difference between the groups concerns nutrition. Whereas cowries feed on a wide range of food types, false cowries specialise in feeding on the tissues of soft corals

Fig. 7.40 False-cowry, Ovula ovum (5 cm), Indo-Paciﬁ c. Above as viewed from beneath; below , shell with the dome removed, to present early whorls 7.7 Cypraeoidea: Cowries, False-Cowries, Smallips and Relatives 145

Fig. 7.41 Procalpurnus lacteus (2 cm), Indo-Paciﬁ c

and sea fans (Gorgonacea). They settle on soft corals as external parasites, and anchor themselves using a long narrow foot. The mantle completely covers the shell most of the time. They are well concealed because their fl eshy, brightly coloured and richly decorated mantle fl aps are strikingly similar to the outspread polyps of their host or the network of the coral. The close resemblance of the vivid coloured patterns of the mantle to the colour patterns of their hosts is due to the false cowries feeding on the host and obtaining its colour pigment. This specialised lifestyle gives them a remarkable camoufl age. False cowries are very aggressive and when two individuals are placed together in an aquarium, each rises on the rear of its foot and charges at the other with bites aimed at the head, tentacles, mantle and foot. The loser retreats or fl ees into its shell where it remains inactive for some time before re-emerging.

7.7.6 Triviidae, Smallips

Smallips, known also as trivias (Triviidae, 15 genera) are more distantly related to cowries than false cowries, and they are classifi ed in a different super-family, the Velutinoidea. The domed shell is broadly similar to that of a cowry but it is small and its outside is traversed by many horizontal ribs that descend towards the aperture (Fig. 7.42 ), an uncommon character among cowries and false cowries. There is no operculum, and the foot is withdrawn into the shell by two shell muscles (rather than a single one as is usual in advanced snails, including cowries). The mantle fl aps are partly fused into a girdle that surrounds and envelopes the shell when extended. The mantle girdles of certain species of Trivia are fi lled with seawater, creating additional hydrostatic rigidity of the fully expanded sea snail. Smallips feed on sessile compound sea-squirts or ascidians (Tunicata) and this diet is supported by their mouth morphology. They have strong well-developed jaws that enable them to bite through the tunic of their prey and reach the tissues on which they feed, unlike the cowries which lack jaws. 146 7 Grazers and Filter Feeders

Fig. 7.42 Smallips: Trivirostra sp. (0.5 cm)

They are simultaneous hermaphrodites: each individual’s male genitalia develop fi rst and he functions as a male; but later also the female genitalia develop, and the individual may now function simultaneously as both a male and a female. However, these hermaphroditic individuals are not capable of self-fertilisation and must undergo copulation with other individuals. The female lays vase-shaped egg capsules inside cavities that she bites out of the tunicate colony on which she feeds. Trivia monacha of Europe possesses a ventral gland that is used in moulding the egg capsules and a papilla on the sole of her foot that she uses to drive them into position. Each capsule contains 1–3,000 eggs and is sealed by a protective plug that is freed from the capsule once the larvae are ready to emerge. The smallips veliger has a double-layered shell, and it is thought that an accessory shell perhaps enables easier fl oating. It is absorbed during metamorphosis, and only the true shell remains. The tendency to cover the shell with mantle fl aps, as in cowries and smallips, has been taken to extremity by Lamellaria , of the same super-family as the smallips. This sea-snail’s shell is completely enclosed within the thick, fl eshy mantle that completely envelopes it from metamorphosis onwards. The now internal shell is thin, transparent and fragile, has two to three whorls and only a trace of a spire, somewhat resembling a human ear. Strangely, there are two shell muscles but their function is not clear since the sea snail does not withdraw into its shell. Lamellaria lacks a breathing tube; it too feeds on sea-squirts. It deposits its egg capsules, that resemble a vase, into the tunic of the ascidian on which it feeds, and its hatching veligers have a double shell, like smallips.

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Abstract Many sea snails are predators. Prey is often detected by a long breathing tube which brings odours to a large smelling organ; prey is grasped with an extendable trunk; hooked teeth hold on to it and rip its fl esh, or pointed hollow teeth stab prey and inject poison. Some Tuns (Tonnoidea) feed on sea urchins, dissolving the victim’s calcareous skeleton with acid. Moon shells (Naticoidea) glide over muddy- sandy sea fl oors with a foot swollen by sea water, capturing buried bivalves by digging and covering them with mucus, then boring through the valves. Hoverers (Heteropoda) hover, swim and hunt in the water column, feeding on planktonic creatures. Wentletraps and violet shells (Epitonioidea) feed on cnidarians, as external parasites of those on the sea fl oor or as predators of those in the water column, reached by fl oating beneath a bubble raft. Parasitic snails (Eulimoidea) infest echinoderms; their body may be worm-like, and without a digestive tract; reproduction is between large females and dwarf males. Whelks (Buccinoidea) often scavenge carrion, complimenting it with live prey, algae or dissolved organic matter; some suck blood of fi shes and rays. Many Murexes (Muricoidea) have long breathing tubes surrounded by calcareous gutters; some bore into sessile barnacles and bivalves, others feed upon corals and may cause widespread mortality to reefs. Cones (Conoidea) kill benthic creatures with a venom-fi lled tooth causing the victim continuous muscle twitch or paralysis or both. Their sting may be fatal to humans.

Keywords Buccinoidea • Caenogastropoda • Conoidea • Epitonioidea • Eulimoidea • Gastropod predator • Heteropoda • Muricoidea • Naticoidea • Tonnoidea

8.1 Predator Functional Morphology from an Evolutionary Perspective

Some 70–100 million years ago, towards the end of the Cretaceous, many marine animal communities became organised in a new way. A whole array of new animal forms now appear in this fossil record. Today’s modern marine fauna is broadly similar to that of the fossil record. One very impressive aspect of this new diversity was the appearance and rapid divergence of different groups of snail predators. These evolved among bony ﬁ shes, sea urchins and crabs – and also among sea

© Springer International Publishing Switzerland 2015 149 J. Heller, Sea Snails, DOI 10.1007/978-3-319-15452-7_8 150 8 Predators snails. Of course, various groups of predators such as brittle-stars, cephalopods, cartilaginous and bony fi shes, and even predatory sea snails, had existed in the sea before then, but not to the extent that appears in late fossil records: 17 of the 18 modern families of predatory sea snails appeared only from the Cretaceous onwards. In general, predation maintains preyed-upon species at low population densities. It prevents competitive displacement and encourages a high diversity of prey; this in turn encourages a high diversity of predator species that specialise in very specifi c prey types. Accordingly, an increase in the number of predatory species causes an increase in the general diversity of species: today, about half the sea snail species in the world are predators. The most important adaptation involved in seeking out prey is the development of an organ that can effectively detect possible prey. A short breathing tube as a continuation of the left side margins of the mantle (Fig. 8.1 ) already occurs among the conchs and the cowries. What a predator needs is such a very long and sensitive organ, and in reality, the breathing tube among typical predatory sea snails may be longer than the animal’s entire body length or even shell length. A notch at the base of the shell enables its convenient emergence beyond the shell. In some predatory sea snails, the notch may take the form of a lengthened gutter (Fig. 8.2 ). When a sea snail seeks prey this breathing tube (‘siphon’ in scientifi c terms) is held above the shell in front of the snail and turns in various directions, enabling detection of the direction of odour signals. Usually, it is structured as a gutter open along its ventral side, but in some cases it may be a closed pipe. Water inhaled into the breathing tube carries the smell of a possible prey to the smelling organ (‘nose’) situated within the mantle space, close to the base of the breathing (sometimes termed breathing pipe, Fig. 8.1 ). This organ (osphradium) is only of modest dimensions in herbivorous groups but is developed to such an extent that it looks like a small gill in predatory sea snails, with rows of leafl ets on each side of a fl at axis. It is an extremely sensitive organ and its chemo-sensitive cells can locate very small quantities of dissolved chemicals. The ability to detect chemical signals leaking out from a potential prey is inborn, and even newly emerged predatory sea snails in the laboratory crawl in the

Fig. 8.1 A predatory snail (shell removed) The osphradium and gill hang from roof of mantle and are seen by transparency 8.1 Predator Functional Morphology from an Evolutionary Perspective 151

Fig. 8.2 Notch in shell (left ) through which the breathing pipe protrudes (right )

direction of water in which there once was a prey; they respond in this manner even after the water is diluted by a factor of 200 times. The most important adaptation involved in grasping prey in predatory sea snails, is the development of a very long trunk around the mouth. Predatory sea snails move and seek prey at the remarkably slow speed of about half a metre per hour. Even when accelerating to catch a fl eeing prey, they can usually no more than double this speed. The foot remains the (slow) organ of movement of most predatory sea snails, and the ability to pounce upon and seize prey has evolved from the frontal parts of the digestive system. These telescope when quiescent, but are suddenly shot out well in advance of the head when active. A trunk has developed as the result of an elongation of the body wall surrounding the oral cavity: it contains the mouth cavity, radula and part of the oesophagus (Fig. 8.3 ; the trunk is also termed a ‘proboscis’). When not in use, the trunk is completely withdrawn into the head like the folded-in fi nger of a glove, with the mouth at its innermost part, and the entire structure then enclosed within a sac-like sheath. The opening of the sheath remaining at the front of the snail is actually a ‘false mouth’, giving entrance merely into the cavity into which the trunk has been withdrawn. During hunting and feeding the snail pumps blood into the trunk, infl ates it and pushes it out; this abolishes the false mouth and the inverted true mouth extends beyond the former front of the head to grasp the food. A set of retractor muscles pulls the trunk back inside its sheath when feeding is completed. This evolution has enabled sea snails to gain access to live food located at a distance, or to collect carrion. The trunk is a complex morphological adaptation to a carnivorous diet, and has evolved separately in at least four groups of advanced snails, each characterised by the presence of novel retractor muscles and different modifi cations. The trunk retractor muscles of moon shells (Sect. 8.3 ) are attached to the tip of the trunk near the mouth, so that withdrawal completely turns the trunk inside out, ‘turning a stocking outside-in by putting one’s hand in and pulling the toe towards the top’ (Fretter and Graham 1962 ). Murex 152 8 Predators

Fig. 8.3 Trunk of a predatory snail. left : trunk is withdrawn thereby forming a false mouth; right : trunk drawn out and the false mouth is gone (Based on Fretter and Graham 1962 )

retractor muscles, however, are attached further back behind the mouth and insert on the sides of the trunk, so that upon retraction only the posterior part turns outside-in, whereas the anterior part is not inverted and the mouth and radula remain facing forward (Fig. 8.3 ). Other important modifi cations for predator snail grasping of prey concern the radula and the digestive system. The radula contains hook-shaped teeth for holding on to the prey and ripping its fl esh, or pointed hollow teeth for stabbing it and inject- ing poison. The salivary glands of the oesophagus are usually very large and their secretions, that lubricate the fl esh of the prey, also contain digesting enzymes that start breaking down the fl esh on its way to the stomach. Some additional differences exist between predatory and herbivorous sea snails in details of the shell, but some of these stem from the fact that predatory sea snails themselves are predated upon. Many fi shes and crabs are predators and some of them crush snail shells with strong teeth or claws. Many predatory snails make life diffi cult for their shell-crushing predators such as wrasse (Labridae) and crabs. They have evolved shells with spines, ribs or ridges. These devices enlarge the overall dimensions of the shell, and spread the pressure applied by the jaws of the fi sh over a larger area thereby weakening it; they also injure the palate of the fi sh. Another adaptation is a thick shell to prevent crabs from operating their claws on weaker regions among the spines. Though all predatory snails belong to the large order of advanced snails (Caenogastropoda, see Table 8.1 ), they have highly diverse methods of predation and eating: some feed on dead animals whereas others bore into the thick armour of barnacles, some are parasites on and in animals considerably larger than themselves, 8.1 Predator Functional Morphology from an Evolutionary Perspective 153

Fig. 8.4 Salivary glands in a predatory snail (Based on Houbrick and Fretter 1969 )

Table 8.1 Predatory super-families of the order Caenogastropoda Order Caenogastropoda Advanced snails Super-family Tonnoidea Tuns, helmet shells, trumpets Super-family Naticoidea Moon shells Super-family Heteropoda Hoverers Super-family Epitonioidea Wentletraps, violets Super-family Eulimoidea Parasitic-snails Super-family Buccinoidea Whelks, nutmegs Super-family Muricoidea Murexes Super-family Conoidea Cones and some hunt crawling snails, burrowing bivalves or swimming ﬁ shes. Some of the adaptations to predation are unique to each snail group. This chapter explores some of the different groups of predator sea snails and their adaptations to a predatory way of life; additional predatory sea snails, among the Opisthobranchia, are described in Chap. 9 . 154 8 Predators

8.2 Tonnoidea: Tuns, Helmet Shells and Trumpets

The often large shell of tuns (Tonnoidea) have low spires and voluminous body whorls, the aperture has a notch through which the very large breathing tube (siphon) protrudes and the trunk is long. The radula has seven teeth per row (2.1.1.1.2), the salivary glands of the oesophagus reach gigantic dimensions and may contain venom. Contraction of special muscles surrounding the glands and the salivary ducts push the saliva, secreted by the glands and assist in rapidly emptying it into the trunk. A special gland in front of the stomach secretes digestive juices to break down the fl esh of the prey. Tuns are nocturnal predatory sea snails that bury into sand during the day. This is a large and diverse group consisting of several families, each of which may feed on different prey. The tun ( Tonna , Fig. 8.5 ) dwells in sandy sea fl oors where it feeds on sea-cucumbers. When quiescent it is buried in the sand, but when hunting it emerges from the sand and seeks prey by swinging its breathing tube from side to side. Upon locating a sea-cucumber, it quickly draws out its trunk and gropes over the body of the prey until reaching one of the sea-cucumber’s two ends; then, assisted by special hooks on its jaws, it swallows the cucumber whole; when it has fi nished its meal, it returns into the sand. A tun may swallow a 200 g sea-cucumber within several minutes, and a tun eats about one sea-cucumber per week. The helmet shell (Cassis and its relatives, Fig. 8.6 ) feeds almost exclusively on sea urchins. Its salivary gland produces a highly acidic secretion of pH 0.13 that consists largely of sulphuric acid which dissolves the calcareous skeleton of the sea urchin. How this acidic secretion is formed and how the salivary glands store it in

Fig. 8.5 Tun, Tonna galea (25 cm), Atlantic Ocean and Mediterranean 8.2 Tonnoidea: Tuns, Helmet Shells and Trumpets 155

Fig. 8.6 Helmet shell, Semicassis faurotis (5 cm), western Paciﬁ c and Red Sea

their cells without causing self-damage is, as yet, not known. Upon locating a sea urchin the helmet shell fully stretches its tentacles, lifts the front half of its foot in a high arch and steals up to the sea urchin on its rear half, until it is bent over the sea urchin with its head and front part of the foot. There is no contact beyond that of the tentacles, a point of some relevance since a sea urchin can move faster than a helmet shell and might fl ee if it notices its predator in time. Predation begins only when the sea urchin is completely covered. The helmet shell then descends on the sea urchin, holds it down with its foot and covers it with large quantities of thick sticky mucus secreted through the trunk and from the sole of the foot. Pressure of the snail’s foot and of the sticky layers of mucus spreads the sea urchin’s spines. It is then that the helmet shell begins penetration of the sea urchin’s body: at fi rst it detaches and removes the spines from an area around the radius of the trunk; then it attaches its mouth to this area and dissolves and scrapes out a shallow depression in the sea urchin’s skeleton, by chemical operation of sulphuric acid alternating with physical operation of the radula; next, the radula removes the chalky paste and exposes new layers of the prey’s calcareous skeleton to further secretions of sulphuric acid. The lips of the trunk seal the penetration area throughout the process to prevent the sea from diluting the acid. Within minutes the trunk presses this weakened area of the skeleton inwards. The helmet shell then secretes copious amounts of sulphuric acid, which pour in through the hole and weaken the sutures of the skeleton so that, the whole skeleton collapses. Now the helmet shell can eat away all the sea urchin’s tissues, including the viscera and the big muscles at the base of the spines. Helmet shells are of importance in the shell cameo industry. Cameos are relief medallions produced by taking a fl at plane where two contrasting colours meet and removing the entire fi rst colour except for the desired design, leaving it on a back- 156 8 Predators ground of contrasting colour. Designs commonly include portraits and silhouettes, scenes from Greek and Roman mythology and fl oral motifs. In Greek and Roman times cameos were carved out of semi-precious gems (agates) and it was only during the Renaissance, during the fi fteenth and sixteenth centuries, that shells were also introduced to the craft. Cowries were the fi rst shells to be used as cameos but from the mid-eighteenth century onwards also the king helmet shell, Cassis tuberosa , a species of shallow sandy beaches ranging throughout much of the western tropical Atlantic (Florida to Brazil), was brought over to Europe, and this sparked an immense increase in the number of shell-carved cameos. Demand for shell cameos grew even more during the nineteenth century as they became popular souvenirs amongst the European middle classes. Another species commonly used since the late nineteenth century is the bullmouth helmet shell Cypraecassis rufa widely distributed in the Pacifi c, in which the upper shell layer is whitish and the lower shell layer a rich orange-brown; it is imported from Madagascar and South Africa. Yet another highly prized species for cameo carving is the queen helmet shell Cassis madagascarensis (Fig. 8.7 ) widespread in the tropical western Atlantic (not Madagascar); its shell reaches 30 cm and has dark chestnut brown on the inside but perfect white on the outside. The colouration and thickness of queen helmet shell

Fig. 8.7 Cassis madagascarensis (18 cm), tropical western Atlantic 8.2 Tonnoidea: Tuns, Helmet Shells and Trumpets 157

Fig. 8.8 Cymatium aquatile (8 cm), Red Sea

make it ideal for carving cameos and furthermore, the shell somewhat resembles marble which adds to its beauty; indeed, some of the most valuable cameos in the world are carved from queen helmet shells (and also named sardonyx shells). Much of the hand-carving of cameo shells takes place in Torre del Greco, Italy, where several thousand people are currently employed. The Italian shell cameo industry (combined with that of corals) has an annual turnover of over 200 million dollars. Cymatium (Fig. 8.8 ) and its relatives prey mainly on other sea snails and bivalves. It carefully sneaks up to its prey, rapidly draws out its trunk and pushes it into the prey’s mantle cavity, where it secretes a paralysing venom. Pushing its trunk to the prey’s uppermost whorls, it eats everything except the operculum and the radula. If the very active trunk is injured or cut off during predation, a new trunk is soon regenerated. During the reproductive season the female lays her eggs in a batch that contains hundreds of elongated capsules, each with hundreds of embryos, amounting to half a million in one batch. The female shields her batch with her large foot until they hatch as small veligers and swim into the plankton. The diet of Distorsio (Figs. 8.9 and 8.10 ) is as yet not known. The veliger of this genus remains in the plankton for a lengthy period of time (probably a few months) 158 8 Predators

Fig. 8.9 Distorsio anus (5 cm), Red Sea

Fig. 8.10 Distorsio anus , shell of veliger (1 cm) (Based on Bandel et al. 1994 )

and its shell reaches considerable dimensions, up to 6 mm. A special lobe along the margins of the veliger’s mantle secretes protein fi bres that it glues to the shell envelope, the periostracum. Forming a relief of bristles or of spines (Fig. 8.10 ), these fi bres assist the veliger in fl oating and perhaps also in defence against small predators which also swim in the water. The lobe of the mantle margin is reabsorbed into the body before metamorphosis, and a normal shell forms after metamorphosis. The trumpet shell (Charonia , Fig. 8.11 ) feeds on starfi sh such as the crown-of- thorns, whose tissues contain high concentrations of tetrodo-toxin, a poison that offers defence from various predators. One adult trumpet consumes less than one crown-of-thorns per week. When encountering a sea star Charonia lampas (of the Mediterranean, eastern Atlantic and western Australia) feeds on it by holding and manipulating the prey with its foot, and using its elongate trunk and radula to scrape and engulf soft tissues and skeletal components of the sea star. It does not inject venom or acid into its prey, as do other predatory snails such as Cymatium or Bursa . The trumpet shell is among Man’s earliest wind-instruments (Chap. 13 ). 8.3 Naticoidea: Moon Shells 159

Fig. 8.11 Trumpet shell, Charonia tritonis (20 cm), Indo-Paciﬁ c

8.3 Naticoidea: Moon Shells

Moon shells (Naticoidea, Fig. 8.12 ) have a thick, almost spherical shell with a very slightly raised spire, a large body whorl often with a pronounced umbilicus; and the contour of the outer lip of the shell aperture resembles a half-moon, hence the vernacular name. Moon shells are an exception among predatory sea snails: they have no breathing tube (siphon) and, accordingly, no notch in the shell. A fold of skin 160 8 Predators

Fig. 8.12 Moon shell, Mammilla melanostomus (2 cm) extending its foot and covering its shell with a skin fold rising from the foot A view from above ( above ) and the left side (below )

rises from the front of the foot and covers the entrance to the mantle cavity, preventing the entrance of silt and sand. Moon shells dwell in sandy and muddy sea fl oors where they prey upon bivalves buried within the sediment. To locate a bivalve, a moon shell must actively move over the soft substratum. At fi rst sight, their globe-like shell seems highly unsuitable for blazing trails through mud, but things appear differently when it emerges from within its shell. Its foot has a special system of tunnels that open and become fi lled with sea water, when the moon shell emerges from the sea fl oor and stretches its foot. The foot swells further due to blood transferred from other parts of the body. The whole process lasts only a few minutes and when complete, a moon shell is three times its weight than when withdrawn. Once the foot is completely extended the area of contact with the soft substratum is very large, thereby reducing the snail’s pressure on it. This enables rapid gliding over soft muddy sand. During periods of inactivity, the moon shell’s foot remains stretched and swollen for many days, the openings of its water tunnels closed by strong sphincter muscles. In moments of distress, the moon shell relaxes the sphincter muscles, jets water out of the tunnels and withdraws its head and foot into the shell, closing the aperture with a small thin operculum. Upon locating a bivalve, the moon shell rapidly digs into the sand or mud beneath it and captures it by covering it with copious amounts of mucus to prevent the bivalve from opening its valves, pushing out its foot and fl eeing. The moon shell then envelopes the bivalve with the front of its foot and lowers its long trunk onto the valves. Boring is carried out by alternating action of the radula and of a special boring organ, a pillow-shaped gland on the ventral side of the trunk (the detailed structure of the boring organ is presented later on Sect. 8.8 ). At fi rst the radula rasps and removes a layer of chalk from the valve, then the boring organ is attached to the bore-site, usually near the apex of the shell, and secretes an acid solution that softens the valve, and the radula removes the softened layers. Penetration is slow and may take a few days, until eventually the radula can tear at the fl esh of the prey. 8.4 Heteropoda: Hoverers 161

A moon shell’s radula has seven hooked teeth in each row, as do the tuns (Tonnoidea, Sect. 8.2 ). Some moon shell species cover the bivalve completely in mucus and drag it along behind them on a rope of mucus until ready for a meal; others tuck the bivalve away into a special pouch formed by a fold of skin on the rear of the foot, and carry it with them wherever they go until they are hungry. Some moon shells prey on snails rather than on bivalves; thus Notocochlis gualteriana of the Indo-Pacifi c will seize a snail by rapidly stretching out its foot and by plugging the prey’s shell aperture with mucus. The prey, compelled to remain retracted in its shell, is then eaten. The boring habits of moon shells evolved 100 million years ago, during the Cretaceous. Moon shells prey on bivalves but are themselves prey for starfi sh. In defensive response to physical contact with a starfi sh, the moon shell lifts a special skin fold from the rear part of the foot and spreads it forward to completely cover its shell. Shell-covering takes approximately 1 min and when the moon shell is covered by a mucus-producing covering, the feet of the starfi sh cannot gain hold of it. The sexes are separate and fertilisation is internal. The spawn is a ribbon-shaped structure coiled in a spiral resembling a stiff collar, often with more than one turn; it consists of gelatinous mucus strengthened with sand grains, into which egg capsules are embedded. When laying eggs the female starts moving along a circular (clockwise) route, forcing her way through the sand. As the eggs are escaping from the genital aperture gelatinous mucus, produced from the front part of the foot, is passed into the mantle cavity and mixed with the egg capsules; when this mass of eggs and intervening mucous matrix is forced out of the mantle cavity, sand particles are incorporated into it. A large fold of skin covers the leading edge of the shell and the opening of the mantle cavity. The egg mass emerging between this fold and the shell is pressed between the two, so that the mass emerges in form of a fl at ribbon. Egg collars are initially produced within the sand but when completed the female pushes them up to the sand surface, where they are ultimately placed. Some nati- cids, including four Australian species of the genus Conuber , produce egg collars which are sand-free. A collar may contain many thousands of developing eggs. In some species, such as Polinices pulchellus of the north-eastern Atlantic, these eggs give rise to hatching larvae which swim and feed on tiny algae in the plankton; eventually they metamorphose to miniature adults, which are capable of hunting small prey already after 3 days. In other species, such Euspira catena, of the north-eastern Atlantic and Mediterranean, the developing eggs give rise to crawl away juveniles.

8.4 Heteropoda: Hoverers

The hoverers (Heteropoda) are snails adapted to hovering, swimming and hunting in the water column, from the sea surface down to depths of 500 m and more. They swim on their backs and have a muscular fi n that grows from their upward-facing foot: the group’s scientifi c name is derived from this character, as ‘heteropoda’ 162 8 Predators means ‘having a different foot’. Most genera of heteropods have an attachment organ on the fi n to hold on to their prey. Like many other organisms dwelling in the water column, the body is transparent. An eye at the base of each tentacle can turn in different directions. Its retina is unique as it resembles a long narrow ribbon with several hundred rows of photosensitive cells, all arranged in only three to six columns. Accordingly, their vision covers up to 180°, but in height it is limited to only a few degrees. To compensate for this constraint, the eye continuously scans its surroundings. Each eye is carried on a short stalk at the base of the tentacle, and can be retracted into a sort of capsule for defence. The hoverer is an ambush predator, waiting until prey reaches striking distance and then pouncing on it. This small group of predatory sea snails consists of eight genera in three families. The primitive hoverers include Atlanta (Fig. 8.13 ), Protatlanta and Oxygyrus . They are small, only up to 10 mm in length. The shell is very thin, coiled, and fl at. A well-developed keel protrudes along the entire midline of the shell and stabilises the sea snail during swimming. The shell and keel of some species consist of rather strong calcium carbonate, but in others they consist only of a protein mesh, which offers both camoufl aging transparency and buoyancy. Atlanta rests at depths of 100 m or more during the day, and fl oats up to close to the sea surface in the evening. The foot secretes up to half-metre long threads of mucus, to avoid sinking and to hover in the water. In moments of danger, the snail disengages itself from these threads, fully retreats into its shell, closes its operculum, and sinks to the depths. When the shell is held vertically and the keel faces downwards, sinking is rapid, up to 10 cm per second; when the shell is horizontal and the larger surface area of the shell and keel is exposed to the water below, sinking is slowed to only 1.5 cm per second. These changes in shell angle thus enable Atlanta to regulate its sinking speed in the sea.

Fig. 8.13 A primitive hoverer, Atlanta (0.5 cm) 8.4 Heteropoda: Hoverers 163

Fig. 8.14 An advanced hoverer, Carinaria (20 cm)

Atlanta and its allied genera feed mainly on sea-butterfl ies, the pteropods (a group of snails described in Sect. 9.4 ). When Atlanta notices a prey, it disengages itself from its threads and swims towards it by undulating movements of the foot at a speed of up to 6 cm per minute. It attaches itself to the prey by means of its attachment organ, penetrates the shell with its elongate head and grabs the body with its muscular trunk; it then tears fl esh off its prey by means of the radula which has seven strong hooked teeth in each row; digestion is completed within 24 h. The more advanced genera, such as Carinaria (Fig. 8.14 ), Pterosoma and Cardiapoma , are more adapted to a drifting style of life. Their body is very large, up to 220 mm in length; the shell, however, is too small to contain the body and accommodates only the viscera. An operculum would be useless in this situation, and is indeed absent. These genera have a coiled shell with a well-developed keel, but these are transparent, delicate and fragile, and very rarely found in their complete form – so rare that in 1913, shell collectors in England were prepared to pay 100 English pounds for one intact shell (a sum corresponding to approximately £ 5,000 sterling today). Carinaria swims with undulating movements of the foot, sometimes combined with rowing movements of the fi n, and can move forwards, backwards, upwards and downwards. However, swimming is not a continuous activity of Carinaria . It swims vigorously only when pursuing prey or fl eeing from predators; at other times it is curled up into a loose ball that hovers motionless in the sea. Carinaria and its allies feed on whatever lives in the plankton around them, such as tunicates, juvenile arthropod stages, fi sh larvae and other sea snails (including individuals of its own species). When Carinaria detects a prey nearby or the shadow of a prey hovering above it, it pounces; it is then capable of swimming up to 40 cm per second, an amazing speed for a predatory sea snail. The prey is swallowed intact, at fi rst stored in a large, extendable oesophagus, later to be rapidly digested. The body of the most advanced hoverers (Pterotrachea and Firoloida ) is even larger than that of Carinaria , up to 260 mm. They have no shell and the viscera are incorporated into the hind part of the foot. Gelatinous tissues in the body of this group have a density lower than that of seawater and assist in hovering. Both genera feed on medusas and bristle worm larvae. 164 8 Predators

In all heteropods the sexes are separate. The male transfers a spermatophore packed with sperm to the female during copulation, and fertilisation occurs within her body. The female lays eggs in a sleeve of mucus, which trails behind her in the sea to a distance of up to ﬁ ve times the length of her body. This sleeve contains embryos at different stages of development, from just a few cells in the end near the female to advanced veligers at the end furthest away from her. The hatching veliger released from the sleeve remains in the water column for a considerable time, probably a few months. At ﬁ rst it has only two sails, but the number increases with growth, to four and then six. The veliger uses these sails both to swim and to collect food, which consists of tiny algae drifting in the plankton. These sails are absorbed into the body during metamorphosis, and the individual shifts from algae-feeding by use of cilia to predation of small swimming organisms by muscular pursuit. As growth continues the hoverer shifts to the predation of larger organisms.

8.5 Epitonioidea: Wentletraps and Violet Shells

Wentletraps and violet shells (Epitonioidea) are best characterised by their radula, which has so many teeth in each row that the radula formula is often designated as ∞-0-∞. All teeth are hooked and turn backwards to enable the ripping apart of soft ﬂ esh. When not active, the teeth on both the left and the right sides of the radula fold into a deep cleft between two cartilages of the radular complex, intercon- nected by a muscular sheet. When active, the two cartilages are drawn out beyond the head as two globular bumps that carry the radula, and its teeth become erect. This radula of wentletraps and violet shells was formed, through evolution, by loss of the central tooth and by multiplying the number of marginal (perhaps also of the lateral) teeth. Wentletraps and violet shells feed upon cnidarians in different habitats: wentletraps feed on cnidarians of the sea ﬂ oor, violet shells on those of the water column.

8.5.1 Epitoniidae, Wentletraps

Wentletraps (Epitoniidae, Fig. 8.15 ) have a conically pointed shell with eight to nine well-rounded, loosely coiled whorls connected to each other by thin axial ribs; the separation of these ribs is so complete that there is no suture. They dwell on the sea ﬂ oor. The vernacular name comes from the Dutch word for a winding staircase. Wentletraps feed as external parasites on sessile cnidarians, mainly sea anemones. An external parasite is a typically small organism that lives on another, usually much larger organism, from which it obtains food without killing it. A wentletrap lives buried in the sand near a sea anemone and emerges in response to odours it produces. It then draws out a very long trunk, which may reach up to four times the 8.5 Epitonioidea: Wentletraps and Violet Shells 165

Fig. 8.15 Wentletrap, Epitonium scalare (4 cm), Red Sea and Indo-Paciﬁ c

length of its shell. Swinging its trunk this way and that while crawling, it eventually contacts the anemone. It then slips its trunk over an arm of the anemone, or gropes along the arm until fi nding a suitable point, and then draws out the radula and cuts off a part of the arm. Each of the two salivary ducts near the tip of the trunk opens into a short hardened style. The saliva contains narcotic substances that temporarily paralyse the sea anemone’s arm and prevent its natural contracting refl ex. The wentletrap cuts off pieces from the arm repeatedly in this manner, in a meal that may last 4–5 h. Sometimes the sea anemone responds to wentletrap attacks with a shower of stinging cells, but the wentletrap’s trunk is immune to them. Having completed its meal the wentletrap buries itself back into the sand at the foot of the anemone. Upon becoming hungry again, after 2 weeks to 2 months, it once again emerges from the substratum to feed on the same sea anemone. There are many wentletrap species in the world and there are many ways they feed on cnidarians. In addition to species that feed on the fl esh of cnidarians’ arms, there are those that rip off small pieces of tissue from the body. Others push their trunk into the sea anemone’s mouth and feed on surplus symbiotic algae that the sea anemone secretes into its body cavity, embedded in large quantities of mucus. Some wentletraps eat entire small sea anemones. Furthermore, some species feed only on one genus of sea anemones whereas others feed on a diverse variety of genera. Then, in addition to species that bury themselves at the foot of the sea anemone from which they have just fed, or others that move and bury themselves farther away, there are some that bury themselves in the anemone’s body. Epitonium millecostatum of the Indo-Pacifi c feeds on cnidarians of the genus Palythoa , that 166 8 Predators

Fig. 8.16 Egg capsule of a wentletrap

may spread as a carpet over corals. Young individuals of this wentletrap roam over the cnidarian carpet and actively seek their food, whereas adults, which crawl only with diffi culty, remain tucked beneath the margins of the Palythoa carpet within its tissues and do not move around. Wentletraps are consecutive hermaphrodites: each young individual matures fi rst as a male, and later on in life he becomes a female. The male is much smaller than the female and lacks a penis. During the reproductive season, he climbs her shell and settles upon it for many days. He produces gigantic sterile sperm cells up to 1 mm long, each with a large, fl at ‘head’ that can contract in undulating movements and vibrate, as well as a long, thick ‘tail’. The typical fertilising sperm, which carries the hereditary cargo, are less than the tenth of a millimetre long and anchor their heads into the tail of this giant sterile cell. How the giant cell, with hundreds and thousands of sperm anchored into it, penetrates the body of the female, is not known. The fertilised female lays egg capsules (Fig. 8.16 ) in the sand at the foot of her sea anemone, up to 100 capsules within one night. Each capsule contains up to 250 eggs surrounded by yolk. An elastic thread of mucus connects one capsule to another, thus forming an aggregate of capsules. Small veligers eventually hatch and swim into the water, where they will remain for at least a month. Eventually, they sink to the bottom and metamorphose to tiny adults, which grow at the rapid rate of two axial ribs per day. Some wentletraps secrete a purple substance, of unclear function. The wentletrap was once highly prized among shell collectors. At an auction in Paris in 1767, the shell of a wentletrap was auctioned for 900 francs; a painting by the Spanish painter el Greco was sold, at that very same auction, for 24 francs.

8.5.2 Janthinidae, Violet Shells

The violet shell Janthina (Fig. 8.17) dwells near the surface of the sea and preys upon cnidarians that ﬂ oat in the water, such as medusas. Its violet-coloured shell is thin, delicate and light, as one would indeed expect of an animal whose natural habit requires ﬂ oating. The violet shell builds a raft of bubbles (Fig. 8.18), in three stages. 8.5 Epitonioidea: Wentletraps and Violet Shells 167

Fig. 8.17 Violet shell, Janthina janthina (3 cm), worldwide in warm, tropical and temperate seas

Fig. 8.18 Violet shells: two bubble rafts

First, it lifts the front part of its foot above the surface of the sea as a spoon, captures a ‘foot-full’ of air, closes it in mucus secreted from the front part of the foot. The bubble is immediately coated with another, thicker and stiffer layer of mucus that fl ows from glands in the central section of the foot, and is moved forward by ciliary action. Then, it pulls the bubble underwater, forms a new bubble in the same manner, and sticks it to the previous bubble, that together form a raft. The whole process of creating a single bubble and adding it to the raft takes 1 min, and the building of an entire raft occurs in several bursts of activity; after forming approximately ten bubbles, the violet shell rests, forms another ten bubbles, rests, and so on. Eventually, the completed raft is approximately 10 cm long, 3 cm wide, and springy. The violet shell hangs on to its lower side, upside down. The violet shell has almost no advancing ability of its own, and if detached from its raft it will drown and die within a few hours, a few days at most. The upside-down position of the violet shell is expressed in the colours of its shell. In general, many organisms of the sea surface are coloured in a counter- shading pattern. Usually, their (upper) dorsal part is dark and offers good camoufl age from predators hovering above the water, whereas the (lower) ventral part is pale and offers effective camoufl age from predators within the sea. The violet shell, which fl oats upside down in the water, has a shell that is coloured in the opposite manner: its upper part is dark and its lower side is pale. 168 8 Predators

The violet shell preys on fl oating cnidarians and mainly on Velella , a medusa 2 cm in diameter equipped with a blue gelatine sail and long arms equipped with many stinging cells. This medusa feeds on fi shes and small crustaceans, which in turn feed on plankton, so the medusa-predating violet shell has a rather high level in the food chain of life at the sea surface. The violet shell lacks eyes (it can only distinguish light from dark by use of its light-sensitive tentacles) and can sense a medusa only when it is 5–10 cm away, probably by chemicals released in the seawater. When the violet senses a medusa, it starts wriggling and beating to reach its prey. Once contact with the medusa is made, it holds on to it by two corneous hooks at the tip of its thick short trunk, abandons its raft and climbs onto its prey. It then secretes a violet-coloured substance that perhaps neutralises the stinging cells and then, by the aid of its radula located at the end of its trunk, tears off the fl esh. It can consume an adult Velella within approximately 20 min and, upon fi nishing its meal, it creates a new raft, slides down and off the remnants of its victim into the waves, and once again drifts along in the vast sea. A violet shell will eat two Velella individuals per day. Though Velella is a favoured food, violet shells also eat other organisms, including cannibalising individuals of their own species. Violet shells, like wentletraps, are consecutive hermaphrodites. As in the wentletrap, the male has no penis, and he produces giant sterile sperm cells (Fig. 8.19 ) to

Fig. 8.19 Violet shells: a gigantic sterile parasperm transporting tiny fertile sperm (Based on Hodgson 2010 ) 8.6 Eulimoidea: Parasitic Snails 169 which the fertilising sperm attach. The ova in Janthina globosa , widespread throughout the temperate Atlantic, Mediterranean and in the Pacifi c, are fertilised while still in the egg duct and from there are transferred through the mantle cavity to special capsules formed by the fl exible foot. Each capsule is fi lled with 5,000 eggs and nourishing mucus secreted by the foot. Once eggs and mucus have been placed inside the capsule, it is sealed and attached to the lower part of the raft. At the end of this process a raft has a cargo of 300 capsules, nearly 1.5 million eggs. Eventually the young hatch and are released to the sea as small veligers equipped with an operculum, which is lost during embryonic development. The young veliger does not build a raft, but has a long, delicate thread of mucus containing tiny bubbles. These give the tiny violet shell a fl oating ability until it reaches a size at which it can produce a raft of its own. Janthina janthina , widespread in tropical, subtropical and warm seas, reproduces slightly differently. The fertilised eggs develop in the egg duct, and the young veligers emerge from it and enter the mantle cavity. They stay there for a period and develop into advanced veligers, perhaps even to tiny adults; only then are they released into the sea, in a cloud of dark purple substance.

8.6 Eulimoidea: Parasitic Snails

Parasitic snails (Eulimoidea) are a group of advanced snails infesting sea urchins, sea cucumbers, feather stars and starfi sh. Genera of this group vary in their physical characteristics. Usually their shells are highly polished, colourless or yellowish brown, but some genera lack a shell. The more primitive genera have a radula that consists of up to 90 canine-shaped teeth per row, but some genera lack a radula entirely. Indeed, the more primitive parasite snails have all the organ systems characteristic of a snail, but the advanced groups may lack most of them. Parasitism is accomplished by a series of morphological and anatomical changes. One change concerns disappearance of the shell, and correspondingly the parasitic snail becomes elongate and worm-like. Another change concerns the digestive tract, that may retain both a mouth and an anus, or a mouth but without an anus; the digestive tract may disappear entirely and nutrition will then be by absorbing low molecular-weight nutrients through the skin. Finally, a complex mode of reproduction may evolve in which one individual, functioning as a female, may control the growth and sexual development of another nearby individual, forcing it to become either a dwarf male in her immediate vicinity or engulfi ng it completely, whereby, as a parasite-within-a-parasite, he loses all but his testis, and a functionally self- fertilising hermaphrodite is thereby formed. Some other parasitic snail groups are consecutive hermaphrodites. The group consists of some forty genera, which vary in the way they parasitise on their host and in their adaptations to this lifestyle. Some are external parasites, anchored only temporarily to the host’s integument by mucus threads that fl ow out from large mucus glands in the foot; others are sessile, anchored permanently or 170 8 Predators

Fig. 8.20 Echineulima mittrei (3 mm), Red Sea (Based on Lützen and Nielsen 1975 )

even buried into the integument; many groups make galls in the host and still others are completely internal parasites, dwelling in the depths of the host’s body. Some species parasitise only on a single host species: thus Melanella frieli of northern Europe lives only on the sea-cucumber species Mesothuria intestinalis ; Sabinella troglodytes of the Caribbean makes galls only in the spines of the sea urchin species Eucidaris tribuloides. Other species of parasitic snails are not so rigidly host-specifi c. Echineulima (Fig. 8.20) is a parasite of various sea urchins, on which it fi rmly attaches by its powerful snout; the long trunk inserts and extends deep into the body of the host through a hole it excavates in the test, reaching most organs in the sea urchin’s cavity and sucking them up. As this parasitic snail has neither a radula nor jaws, penetration of the test is probably by chemical means. The foot plays no role in host attachment, but is capable of locomotion. The snail may thus leave its site on the host and crawl around in search of a better site. Echineulima is an external parasite on a wide range of sea urchin groups. Monogamus is specifi c to the common Indo-Pacifi c reef dwelling sea urchin Echinometra . It lives within the tube feet, and the infested tube foot becomes deformed, appearing as an irregularly-shaped protrusion with one or two openings through which parts of the snails’ shells project. Monogamus inserts its snout deeply into the tube foot so that it occupies almost the entire internal cavity. The posterior end of the snout is retrofl exed, forming a bell-shaped sac that surrounds much of the snail 8.6 Eulimoidea: Parasitic Snails 171 on all sides, presumably to protect it from the sea urchin tissues. The remainder of the snout is directed towards the sea urchin’s test, and has a small glandular area producing a secretion that glues the snail fi rmly to the host’s test. The foot, lacking a creeping sole, is reduced to a fl eshy lobe not capable of locomotion. Monogamus is thus a sessile external parasite that reaches its site as a veliger, metamorphoses, and then does not move about. It usually occurs in male-female pairs, and the larger female bears egg capsules, each attached by a short stalk that emerges between its foot and shell. Robillardia , like Monogamus, infests Echinometra . It reaches a height of up to 10 mm; its pink body can be seen through its glassy fragile shell, and it is equipped with a large trunk. However, in contrast to Monogamus , Robillardia is an internal parasite that dwells inside the body of the sea urchin, within its rectum. Attaching itself to the wall of the rectum, it inserts its long trunk and pokes around the sea urchin’s organs, in search of the ovaries and testis on which it feeds. The rectum of the sea urchin is very poor in oxygen, and to survive in this hostile environment Robillardia is equipped with a very long siphon that extends outside the sea urchin’s body and enables breathing of oxygen-rich seawater. Robillardia has two large skin fl aps, one on each side of the head and foot, which meet and fuse on the rear part of the shell, enveloping the fragile shell and protecting it from the abrading activity of the host’s faeces. The sexes are separate. The female (up to 10 mm) has two large skin folds, and her right fold is rolled to form a brooding pouch for her egg capsules. The brood pouch opening faces the internal opening of the long breathing pipe, so fresh water enters it directly and the capsules benefi t from good aeration. Each capsule contains 300–500 eggs and the female can simultaneously carry up to 26 capsules, containing more than 10,000 eggs and embryos at different developmental stages. These hatch as veligers which leave, fi rst the body of the female and then the body of the sea urchin host (via the faeces) and swim into the plankton. Male Robillardia, on the other hand, are merely 2 mm long, their siphon is shorter, and the skin folds of the brood pouch are very small; instead, a large penis emerges from the right side of the head. This dwarf male is permanently positioned within the female’s brood pouch and males are only found escorting females, one male per female; a male is never found alone. Stilifer is an internal parasite in the skin of starfi sh. It forms galls, each containing two to four sea snails. Its trunk secretes acid that dissolves some of the starfi sh’s calcareous plates, thereby gaining access to softer tissues. A collar-shaped enlarge- ment of its snout forms a sac-like structure that wraps and envelopes most of the sea snail’s body and shell, separating it from the host’s tissues. The trunk is long and is inserted deep into the body or rays of the starfi sh, but Stilifer ’s body remains quite close to the starfi sh’s integument. Stilifer is a consecutive hermaphrodite. Enteroxenos (Fig. 8.21 ) is an internal shell-less parasite snail on sea cucumbers, whose individuals enter the host’s body through the intestinal wall, not the integument, and mainly infest the oesophagus (the scientifi c name of the genus means ‘foreigner in the gut’). These parasitic snails cast off their veliger shell at metamorphosis and the body becomes worm-like, reaching a length of 10 cm. The long body of the female is completely clothed by the peritoneum of the host. It is attached to its host by a tapering stalk with a longitudinal narrow internal tubule. One end of the 172 8 Predators

Fig. 8.21 Enteroxenos oestergreni Left : female in situ , cut open along its long axis, showing the central cavity. Right : male implantation into female receptaculum masculinum (Based on Lützen 1979 )

tubule communicates with the lumen of the host’s viscera and the other opens into a spacious central cavity that occupies the rest of the snail’s body. Enteroxenos has no digestive tract and it feeds by absorbing nutrients of low molecular weight directly through its skin. In Enteroxenos the sexes are separate. The female has a body wall that is thickened into an ovary protruding into her central cavity. It has many branched tubules and a U-shaped oviduct, the distal part of which, the uterus, opens into the central cavity. The ova mature in the ovary, travel down the oviduct where they are fertilised, and the eggs enter the uterus. Capsules are produced in the uterus and deposited in the central cavity. Each female produces only one batch of egg capsules in her life. Before or shortly after releasing the capsules, she detaches from the host sea cucumber’s viscera and becomes free in its body cavity. The capsules are probably expelled during the host’s annual evisceration (some sea cucumbers seasonally cast out and regenerate their viscera). Larval development takes approximately 1 year, spent mostly within the capsule, and veliger life is very short. The female- to-be veliger infests a sea cucumber and metamorphoses inside it, casting off her larval shell and operculum. A male Enteroxenos veliger completes his metamorphosis on a special epithelial cushion inside the female’s central cavity: this is possible only after he successfully concludes an Odyssean journey. Having identifi ed, reached and penetrated the gut of a host sea cucumber, he must discover the female’s special ciliated tubule, inject himself through it and pass from the lumen of the host’s gut into the female’s central 8.6 Eulimoidea: Parasitic Snails 173 cavity. Once inside her body, the ciliated tubule closes behind the male veliger preventing both his escape and the entrance of additional veligers. Inside the central cavity of her body, he is lured to alight on a (seemingly perfumed) cushion. Once he does so, the young male is doomed to loose all his tissues except his rudimentary testis. This organ now grows and expands considerably, with a small area developing into a sperm duct, whereas most other body tissues degenerate and disappear. Finally the enlarged testis is completely incorporated in the cushion in the female’s central cavity. The adult male thus loses all characteristics of an individual, becoming in effect just a testis grafted onto tissues of the female. The sperm of this male, after being released from the testis, moves through the fl uid of the female’s central cavity, enters the aperture of the uterus and accumulates in her oviduct. The ova are fertilised as they pass from the ovary through the oviduct and are afterwards encapsulated in the uterus, in thin-walled capsules produced by its wall. The capsules, each containing numerous eggs (100–450), are then passed to the central cavity of the body, where they fl oat about freely. A single Enteroxenos may carry as many as 135,000 eggs. Each female seems to produce only one batch of egg capsules in her life, suggesting that the batches are released all together. Before or shortly after releasing the capsules, she detaches from the host’s viscera, the capsules are expelled probably during the annual evisceration of the host, the female dies and the cycle of life thereby repeats itself. Thyonicola is closely related to this genus, and has an even more worm-like body (Fig. 8.22 ). This tendency toward an elongated worm-like shape reaches its peak in the extraordinary Parenteroxenos dogieli of the north-western Pacifi c, a parasite of sea cucumbers that reaches 1.3 m long when unrolled – the longest snail known from the sea.

Fig. 8.22 Thyonicola dogieli , the female about 22 cm, the male (not to scale) only 0.3 cm (Based on Lützen 1979 ) 174 8 Predators

8.7 Buccinoidea: Whelks and Nutmegs

The radula in the groups of predatory sea snails presented up to this point in the book consists of either seven teeth per row (tuns, moon shells, hoverers) or of very many teeth per row (violet shells, wentletraps, primitive parasitic snails). In two other groups of predatory sea snails, the whelks (Buccinoidea) and the murexes (Muricoidea, Sect. 8.8 ) there are no more than three teeth in each row: two lateral teeth between which there is only one central tooth (0-1-1-1-0, Fig. 8.23 ). These large, hooked teeth enable the sea snail both to hold on to the fl esh and to tear it apart. Whelks and murexes also have numerous digestive glands in the oesophagus which are concentrated in a distinct separate gland known as the ‘Leiblen’s gland,’ whereas among primitive groups they are fewer in number and spread along the inner wall of the oesophagus. The digestive Leiblen’s gland empties into the oesophagus through a narrow duct and secretes protein-digesting enzymes. The Buccinoidea evolved from an ancestor close to that of the moon shells. They clearly differ from moon shells in that they have a spiral shell that is usually conical to spindle-shaped; the base of their shell aperture has a notch which is often elongated to form a well-defi ned calcareous canal, for extension of their long siphon. In addition they possess a well-developed trunk; their radula contains only three teeth per row, there is no jaw, and they usually lack a boring organ. Their often very wide and fl attened foot (sometimes with a pair of small fi laments or slender appendages on its rear termed ‘cirri’ and sometimes with an elaborate system of water tunnels) enables these sea snails to glide over soft substrata. Though they and the moon shells share a common ancestor, the Buccinoidea also differ from moon shells in their feeding style. As they have no organ with which to bore through the armour of a prey to reach its soft tissues, many of them are scavengers that tend to feed on carrion and sometimes even on detritus. A very large and diverse group, the Buccinoidea consist of some 200 genera. The natural history of the group is presented here, focussing on two species, Bullia digitalis and Buccinum undatum . The surf-whelk Bullia digitalis of South Africa (Fig. 8.24 ) dwells in high-energy sandy beaches, and seeks carrion. A predominantly intertidal snail, it exploits waves and currents by spreading its thin, fl attened agile foot and surfi ng up and down the shore. It buries into the sand at low tide, with only the tip of its breathing-pipe

Fig. 8.23 Single row of typical buccinoidean radula, with three teeth only 8.7 Buccinoidea: Whelks and Nutmegs 175

Fig. 8.24 Surf-whelk, Bullia digitalis (4 cm), South Africa

protruding above the sand; as the tide comes in, it emerges from the sand, turns on its back and spreads its foot, vigorously turning and twisting it from side to side. The foot now functions as an underwater sail that ‘catches the wave’, and the whelk, foot above and shell below, is drawn up and later down the sandy shore. It carries out these tidal migrations during both the day and night, each time moving distances that may reach 45 m. Even slight water currents stimulate emergence from the sand and expansion of the foot. The whelk’s surfi ng behaviour is a highly active process with a high energy cost per unit of time, as the extreme turgidity of the foot demands continuous muscular contraction to prevent blood fl owing out of the foot; it is, however, balanced by the low cost in terms of distance travelled and therefore prey possibilities. The surf-whelk is a carnivorous scavenger that feeds mainly on carrion. A variety of stranded jellyfi sh species and Portuguese-man-o’-war (Physalia ) form its staple diet. The bodies of sea-squirts (tunicates) and bivalves commonly washed up during storms are also avidly eaten. As an adaptation to their carrion-feeding life style, surf-whelks have evolved a high sensitivity to organic chemicals that emanate from rotting fl esh, such as tri-methyl-amine; such substances are detected from afar by the osphradium. In response to the smell of a carcass, the surf-whelk emerges from the sand and sails into the wash and up the shore. With its siphon held out in front, it crawls in the direction of the carrion. Extremely rapid locomotion, involving not only surfi ng but also crawling, allows the surf-whelk to reach its food quickly. Crawling is achieved by alternate movement and anchorage of the front and rear parts of the foot. The posterior part of the foot is anchored into the sand and the front part is raised slightly and thrust forward; then the front part becomes anchored and the rear part of the foot is drawn forward. The surf-whelk cannot see its prey because it lacks eyes and has only a dim sense of light and dark. Feeding behaviour is initiated upon contact. Once reached, the carrion is sensed by contact receptors on the leading edge of the surf-whelk’s foot, and only in the presence of amino acids does it extend its trunk and thrust it into the carcass. When eating jellyfi sh, the bell is usually attacked fi rst and the surf-whelk thrusts its trunk deep into its tissues; when eating Physalia the tentacles are attacked fi rst, despite the stinging cells they contain, and the fl oat is avoided. Carrion-feeding demands special feeding habits. Carrion usually reaches a shore very infrequently, but once washed up in the surf, it contains fl esh in vast quantities that greatly exceed what can be eaten by the population before it is pushed further 176 8 Predators up the shore by the next high tide. A carrion-eating sea snail must therefore be adapted both to surviving long periods without feeding and also to gorging itself on the fl esh during that brief period in which carrion is available. An individual snail can consume fl esh quantities reaching one third its own tissue weight during a single 10-min meal. This gorging ability is made possible by powerful radula movements, and also by the snail’s ability to ingest rapidly by suction, using its trunk. While feeding the surf-whelk tends to anchor itself to its food, to prevent being washed away from it by waves and wash. If the food is hard (for example a bivalve) anchorage is achieved by suction provided by the sole of the foot; if the food is large but soft (a medusa) the trunk itself provides anchorage by being thrust deep into the tissues; if it consists of small pieces, the food may be dragged below the surface of the sand and consumed there. Carrion is a spatially and temporarily infrequent food source in the sea, as only few marine animals die as a consequence of natural senescence and become available as carrion for scavengers. Most deaths result from predation, so that only scraps are available for scavengers. Carrion is a nutritious food, but its availability is highly unpredictable and it is available only for a short time before bacterial decomposition renders it inedible for most scavengers. As it is an infrequent food source, carrion has favoured the evolution of facultative rather than obligate sea scavengers. Carrion feeding must therefore be complimented by other methods of feeding, whether catching live prey, consuming algae or detritus, or sucking blood. Close relatives of Bullia can survive more than 120 days without food. The surf-whelk on occasion becomes an active predator, attacking living members of the sandy-beach commu- nity such as tiny crustaceans, worms, bivalves and prawns. When attacking a small prey, the surf-whelk fi rst crawls over it, then folds its foot around the animal, introducing the trunk into the fold from the side to eat the prey. As an additional supplementary food source, the surf-whelk can also take up dissolved organic matter, such as amino acids, directly from seawater, to such an extent that it may reach up to 15 % of its energetic needs. Such substances are absorbed mainly through the wide foot, which remains expanded for many days or even weeks, and through the mantle. Nassarius circumcinctus (Fig. 8.25), of sub-tidal sandy habitats in the Mediterranean, probably has a broadly similar manner of feeding.

Fig. 8.25 Whelk, Nassarius circumcinctus (1 cm), Mediterranean 8.7 Buccinoidea: Whelks and Nutmegs 177

Additionally, the surf-whelk can also graze plant material. Green algae grow on the upper surface of its shell, especially on the last whorl. This part of the shell receives the most light, for when the sea snail is buried it is closest to the surface of the sand or is frequently exposed. The single (as yet undetermined) green alga species growing on the shell is regularly cropped by the surf-whelk, by extending its long mobile trunk over its head and onto this algal garden, moving the trunk tip over it and plucking the alga. Virtually all surf-whelk individuals possess an algal garden and use it as a supplementary food source. Females surf-whelks outnumber males and may become much larger. Fertilisation is internal and the egg capsules are contained in a single large case that is deposited below the surface of the sand, usually in the shallow sub-tidal. Although the eggs are not attached to the parent nor to any other object, the mother broods over them until they hatch as veligers. Development in some other species closely related to Bullia digitalis is direct, and the young hatch as small crawl-away snails. The common whelk Buccinum undatum is an inhabitant of coastal areas of the northern Atlantic Ocean, where it is most frequently found on mud and sand at depths of between 5 and 200 m. It is a carnivore that attacks sedentary animals, mainly bivalves (scallops, mussels, oysters, cockles) using its foot to asphyxiate them or to pull the shell valves apart. The trunk, extendable to twice the length of the shell, is then inserted and the soft tissues are attacked. In turn, the common whelk is preyed upon by fi shes, and forty shells have been reported from the stomach of a single cod. It is also a highly opportunistic scavenger and will attack moribund animals and fresh corpses. The amount of carrion available may sometimes be insuffi cient to meet the needs of common whelks, so an interaction with starfi sh may contribute to its diet. Common whelks frequently approach starfi sh extracting bivalves from sediment bottoms, and may benefi t by feeding on prey remains left by the starfi sh. This point will be mentioned again soon. Common whelks have separate sexes. The female attracts the male by pheromones she releases into the water, and fertilisation is internal. The female produces a large number of eggs that she embeds in albumen inside capsules; when laying she piles the capsules into a mass of hundreds, which she sometimes lays on a pile prepared by another female. The embryos develop within the egg capsule by eating non-developing eggs, known as nurse eggs; indistinguishable from normal eggs when laid, they serve as an extra-embryonic source of nutrition. Embryonic development is direct into juvenile adult form, but only 1 % of the eggs deposited in the capsules eventually hatch as crawling juveniles, which emerge through a hole in the capsule after two and a half months. The juveniles leave the capsule in search of food and gradually grow, reaching sexual maturity at approximately 6–8 years, and may live for 10–15 years. Whereas the common whelk develops directly into a juvenile sea snail, in some other whelks (Colus stimpsoni , Buccinum cyaneum), feeding on nurse eggs is followed by a short larval phase in the plankton. The common whelk’s mode of reproduction is not representative of whelks in general. Natural enemies of the common whelk include starfi sh. When attacked by the predatory starfi sh Leptasterias polaris in North America, the whelk responds by vigorous escape behaviour including rapid fl ight, shell rocking and foot contortions; 178 8 Predators these behaviours are also displayed when a starfi sh is detected at a distance. However, when the starfi sh feeds on a large bivalve, nearby whelks will often aggregate in the vicinity of their predator waiting for leftovers, and at times even crawl alongside the starfi sh in search of openings to insert their trunk and steal fragments of the prey. Whelks in such aggregations generally remain outside the starfi sh’s reach and occasionally display defensive behaviours, indicating that they have detected both the predator and its prey. Interestingly, only large sexually mature whelks participate in these feeding aggregations; juveniles do not come near a feeding starfi sh. This tendency of adults to take great risks in obtaining food may be due to their increased energy requirements for reproduction. Reproductive costs are likely to be particularly important for females, in whom the ‘reproductive effort’ is more than six times greater than that of males. Females form the vast majority of adult whelks approaching feeding starfi sh, and furthermore, females attracted to feeding starfi sh have smaller reproductive organs than the average of the population at large. Thus, females with the greatest potential for reproductive gain are more likely to feed in the face of predation risk. The Buccinoidea is a large and diverse group that consists, in addition to Bullia and Buccinum , also many other genera (Figs. 8.26 , 8.27 and 8.28 ), each often having specifi c feeding habits. Voluta envelopes bivalves with its large foot until they are suffocated; when the dying bivalve relaxes its valve-locking muscles, the sea snail inserts its trunk and feeds on its fl esh. The harp shell Harpa (Fig. 8.29 ) envelopes small crustaceans with paralysing mucus secreted from its foot. Other genera are external parasites; thus Colubrarium , which has no radula and no oesophageal gland, is a parasite of fi sh. It prefers parrotfi sh, and sucks their blood with its extendable trunk. The sea snail inserts it into the mouth of the fi sh, and the trunk may stretch up to two to three times the size of its shell. Nutmegs, a small group of about six sand-dwelling genera of the sub-littoral (Cancellaria , Fig. 8.30 ) are external parasites. They feed mainly on rays, responding perhaps to some substance in the mucus covering the ray’s skin. When rays are not present, the nutmeg remains buried motionless in the sand, but when it detects a ray (from a distance of up to 24 m) it emerges and moves rapidly towards its victim. The

Fig. 8.26 Whelk, Engina mendicaria (1 cm), Red Sea and Indian Ocean 8.7 Buccinoidea: Whelks and Nutmegs 179

Fig. 8.27 Babylonia spirata (5 cm), tropical and temperate Indo-Paciﬁ c

Fig. 8.28 Whelk, Vasum turbinellus (6 cm), Indian Ocean and Red Sea nutmeg approaches the ray with outstretched tentacles and drawn out trunk and pierces its skin, causing a small wound through which it inserts its trunk. It then sucks the ray’s blood. The nutmeg may also penetrate the ray through the gill slits or the anus. Nutmegs have a huge jaw that spreads down from the mouth ceiling along the sides of the mouth. These two slopes meet in the front part of the mouth and form a tube, and the radula is drawn out through this jaw-tube to stab the victim. Some nutmegs which lack a radula use the jaw-tube itself as a piercing needle. Well- developed salivary glands behind the radula may perhaps contain a substance preventing coagulation of the victim’s blood. 180 8 Predators

Fig. 8.29 Harp shell, Harpa ventricosa (6 cm), East Africa and Red Sea

Fig. 8.30 Nutmeg, Cancellaria reticulata (4 cm), Caribbean Sea 8.8 Muricoidea: Murexes 181

8.8 Muricoidea: Murexes

The murexes (Muricoidea) like the whelks evolved from an ancestor close to the moon shells and share certain characteristics with these groups. Like the Buccinoidea, they have a radula with only three teeth per row and their mouths lack jaws; their shell, too, has a notch at the base of the aperture, often elongated into a canal, for their siphon (breathing-tube). Unlike the whelks they have ‘inherited’ a boring organ from their common ancestor with the moon shells, but they did not inherit a wide foot which generates water tunnels. This rather narrow foot constrains many murexes to dwell on hard substrata such as stones, boulders and coral reefs rather than on sand and soft mud. In addition, various murex genera have a shell covered with many rows of protective long spines or prominent ribs, compared with the overall smooth shell of moon shells and whelks. Many murexes have a long siphon surrounded by a long and narrow calcareous gutter that protrudes from the front of the shell and opens facing downwards. This sheath-like gutter affords the siphon greater protection than the exposed tube of whelks but it consequently lacks ﬂ exibility. Murexes feed on a wide range of organisms, including bivalves, snails, barnacles, small crustaceans and other individuals of their species. When in stress many murexes secrete a liquid that quickly becomes blue-purple. This liquid is the source of the blue and purple dyes of ancient days, and the historic importance of murexes in producing these dyes is discussed in Chap. 12 . The special boring organ enables many murexes to bore through the calcareous armour of their prey and reach the live ﬂ esh. This organ (Fig. 8.31 ) is located on the sole of the foot, structured as a pillow, and its outer surface has a single layer

Fig. 8.31 Boring organ in the sole of a muricoidean’s foot (Based on Carriker 1969 ) 182 8 Predators

Fig. 8.32 Oyster-drill, Urosalpinx cinerea (2 cm), north-western Atlantic to Florida

of secreting cells. Muscles, blood capillaries and nerves originating deep in the foot branch out into the pillow and reach the base of these cells. Pumping blood into the pillow causes it to be pushed down and pressed against the prey, and the contraction of special muscles pulls it back. A furrow crosses the sole of the foot from right to left in front of the boring organ, which serves to drain seawater from the bore site. The oyster-drill Urosalpinx (Fig. 8.32 ) is a murex sensitive to very minute quantities of substances that leak out from between the valves of bivalves, and upon locating a leaking bivalve it crawls and climbs onto it. Once positioned on the bivalve, it holds on to it strongly with the rear part of its foot, which serves as an anchor; it remains in this anchored position until the boring process is completed. The front part of the foot now retreats, the trunk with its radula is drawn out and the oyster-drill begins to rasp and scratch a low depression in the hard valve of its prey. After a brief bout lasting 1–2 min, the trunk is folded in and the oyster-drill now pushes the front part of its foot above the shallow depression, presses the furrow of its sole onto the valve and slides it over the shallow pit over and over again. This activity drains sea water from the pit, the foot sealing the pit off and preventing entrance of water from the surrounding sea. Once water and rasped material have been removed from the pit the oyster-drill pumps blood into the chemical boring organ, lets it down and presses it into the shallow depression for 30–40 min. The 8.8 Muricoidea: Murexes 183 layer of cells on the boring organ secretes a viscid substance, containing both protein-attacking enzymes to dissolve the organic components of the armour of the prey and chloric acid to soften the calcareous component. The secreted substance is only slightly acidic (pH = 4.0) and the amount secreted in one bout of letting down the boring organ is suffi cient only to dissolve the scratch marks left by the radula. The repetitive cycles of rasping-scratching the prey’s shell with the radula, removing sea water from the pit with the furrow, and of dissolving the shell by materials secreted from the boring organ, occur repeatedly. In each cycle yet another thin layer is dissolved and the oyster-drill slowly deepens the depression it bores into the bivalve’s valve. Controlled removal of sea water from the depression reduces the dilution of the substance secreted from the boring organ. The boring process may take 3 days to be completed, during which the snail hardly moves from its position. When a hole large enough is eventually formed, the oyster-drill pushes its trunk through, tears at the fl esh of its prey and begins its meal. The boring organ enables murexes to prey on a wide array of species much larger than themselves which are protected by thick calcareous armour. Boring methods in moon shells (Sect. 8.3 ) and murexes are similar, but there are signifi cant differences in their prey and in the way they handle them. The moon shell usually feeds on bivalves and snails that are not attached to the sandy substratum and therefore, it must stabilise its prey during the boring process. The front part of its foot carries out this function, as it envelopes the prey and holds it stable. Consequently the moon shell’s prey must be small to enable it to be held and stabilised. The murex, however, usually feeds on prey that is sessile and stable, that it can hold onto with only the rear part of its foot. It tends to choose a large prey, in which there is a due reward for the considerable effort it invests in the boring process. Juvenile murexes can bore into a small prey the moment they hatch from their eggs. In some genera, such as Stramonita (Fig. 8.33 ), only young snails bore large holes in their prey in the manner of the oyster-drill. The adult bores only a small hole into the bivalve, through which it injects paralysing venom into its victim: this causes complete relaxation of muscles and a consequent gaping of the valves. The sea snail then inserts its trunk between the valves to reach the fl esh. Usually Stramonita prefers the mussel Mytilus over other bivalve genera, and individuals of 1–2 mm are preferred. Some other genera feed on barnacles, boring through the armour plates or through the inter-plate sutures. A large and highly diverse group, the Muracoidea consist of some 120 genera (Figs. 8.34 , 8.35 , 8.36 , 8.37 , 8.38 , and 8.39 ). Concholepas has a wide, almost fl at shell, like an abalone, with a very large aperture. It relies on its strong foot to remain in place and cannot completely hide inside its shell if over-turned; it also has no operculum. Living on wave-beaten shores in Chile, it feeds predominantly on barnacles and mussels, using a variety of techniques to dislodge and open its prey, including bulldozing, suction, envelopment with its large foot, and boring or smashing the armour. A Concholepas individual can eat approximately 12 barnacles a day, so this genus has considerable impact on intertidal and subtidal communities. 184 8 Predators

Fig. 8.33 Murex, Stramonita haemastoma (9 cm), Atlantic and Mediterranean

Fig. 8.34 Murex, Bolinus brandaris (7 cm), Mediterranean 8.8 Muricoidea: Murexes 185

Fig. 8.35 Murex, Hexaplex trunculus (7 cm), Mediterranean, and Atlantic coasts of Spain and northern Africa

Fig. 8.36 Common whelk Nucella lapillus (3 cm), northern Atlantic 186 8 Predators

Fig. 8.37 Murex, Homalocantha dovpeledi (5 cm), Red Sea

Fig. 8.38 Black-ﬁ ngers, Drupina lobata (4 cm), Red Sea and Indo-Paciﬁ c

Fig. 8.39 Drupe, Drupa ricinus (4 cm), Red Sea and Indo-Paciﬁ c 8.8 Muricoidea: Murexes 187

Another genus with considerable impact on subtidal communities is the coral- killer Drupella (Fig. 8.40 ) that feeds upon corals, mainly on the coral Acropora and, to a lesser extent, on Porites in the tropical Indo-West Pacifi c. It is often found in concentrations of hundreds of individuals and its infl uence is so destructive that its population outbreaks cause widespread mortality of reef corals. Drupella is attracted mainly to injured corals, which it locates with its well-developed sense of smell, and crawls towards them from a distance of up to 2 m within one night. During the day it hides around the base of the coral or among its branches, and when evening falls it climbs onto the branches. It prefers feeding on the transitional zones between live and dead areas on the coral. The coral-killer does not bore, but its radula has long thin teeth that tear away at coral tissues. The front part of its digestive tract is covered with a thick hardened layer, which blocks the venomous threads of the coral’s stinging cells from reaching its sensitive inner tissues. Viscous mucus is secreted all along the digestive system, and this further contributes to blocking the venom threads; the precise method is not known, but it may perhaps contain a substance that neutralises the venom. Drupella activity may reduce the coral cover of a reef by 75 % and completely change the reef landscape. In addition to destroying the live tissues they eat, the coral-killers damage the coral skeleton by breaking its branches, when they push around on their way up and down among the colony. It is damaged yet further because fi lamentous green algae subsequently cover the dead coral skeleton. With the coral’s death and the destruction of its skeleton, the fi sh fauna around it also changes – butterfl y fi sh that feed on corals leave it, as does that huge variety of small

Fig. 8.40 Coral-killer, Drupella cornus (3 cm), Red Sea and Indo-Paciﬁ c 188 8 Predators

fi shes for which the coral offers shelter. They are replaced by groups of large fi shes such as parrotfi sh, which graze on the algae. While grazing they also bite into the coral skeleton, which rapidly wears down and crumbles in a heap of rubble. Causes for population outbursts of Drupella are unknown, neither is the time it takes a reef to recover from the destruction and ruins left by a coral-killer attack (but it should be measured in decades). Some muricid genera (of the Mitridae, Figs. 8.41 and 8.42 ; named after the mitre, the tall head-dress of bishops) feed on worms that shelter inside soft substrata

Fig. 8.41 Miter, Scabricola ﬁ ssurata (4 cm), Red Sea and Indo-Paciﬁ c

Fig. 8.42 Mitridae: anterior part of digestive system (Based on West 1990 ) 8.8 Muricoidea: Murexes 189

Fig. 8.43 Coral-lover, Coralliophila erosa (2 cm), Red Sea and Indo-Paciﬁ c

or in tubes of other animals. The miter has a J-shaped muscular rod beneath the radular complex (Fig. 8.40) positioned within a double system of muscular sheaths. Upon contracting, they cause it to be drawn out. When a miter preys on a worm, it fi rst rasps a hole in its skin by use of the radula and then inserts the muscular rod through it; next, the rod grasps the worm’s intestine and pulls it out through the hole in the worm and into its mouth. In addition to the murex groups that hunt, other murex groups parasitise a single animal, whether it be sessile or mobile. The coral-lover Coralliophila (Fig. 8.43 ) lives as an external parasite on Porites corals in the Indo-Pacifi c, whose tissues it sucks. As an adaptation to this style of life, its radula is very much reduced or completely absent. In common with many parasitic sea snails (Sect. 8.6 ), an individual coral-lover goes through a sex change during its life. A young individual develops fi rst into an adult male and later into a female, but in presence of another female the sex reversal process is inhibited and he remains a male. After mating and fertilisation, the female lays her egg capsules in her mantle space. They are stored, and from here tiny veligers will hatch, each with four tiny sails. Margin snails (Marginellidae, Fig. 8.44) are a small group of some 25 genera, some of which drill into the calcareous armour of various invertebrates, whereas others are external parasites of coral reef fi shes. Their egg-shaped shell is glossy and smooth with prominent folds on the columella. In most species, the aperture lip thickens with growth (thereby forming the ‘margin’ from which the family name derives). Mantle fl aps spread and cover most of its highly polished shell and protect it, somewhat as in cowries (Sect. 7.7 ). During the night the parasitic margin snails climb on and over a sleeping fi sh and insert their trunk, which may stretch two to three times the height of their shell, into the fi sh’s body. Insertion is between the fi sh’s scales, near the eyes, mouth, gills or the fi ns. Once the trunk 190 8 Predators

Fig. 8.44 Margin-snail, Prunum terverianum (1 cm), Red Sea, southern Arabia and east Africa

penetrates live tissue, the snail sucks its blood. Parrotfi sh are the favoured host, perhaps because they tend to return each night to the same lair in the reef. At dawn they descend from the parrotfi sh and hide in crevices or in the sandy fl oor, where they spend their day. Primitive margin snail genera may have three teeth in each row of the radula; in other genera only the central tooth remains, but it is membranous so small and that it is doubtful whether it has a signifi cant function. Many murexes, whelks and cones (Sect. 8.9 ) differ from other sea snail groups in the considerable paternal investment of the mother in her descendants after they are laid. Copulation is internal, and immediately upon fertilisation, while still in the mother’s egg duct, the eggs are wrapped up in primary, transparent membranous capsules. Each such unfi nished capsule is laid and immediately transferred along a temporary fold in the sole of the foot to the opening of a special hardening pouch (usually positioned behind the female’s boring organ). The pouch cavity is deep, many glands drain into it, and a system of muscles surrounds both the glands and the walls of the pouch. The unfi nished capsule is inserted into the pouch and held there tightly for a few minutes, during which its walls are hardened and thickened by secretions of the pouch. Eventually the hardened capsule is ejected from the pouch and pressed onto a rock or boulder; the female then lifts and shifts her foot a little, to insert, harden and attach the next capsule. The hardened capsule is very costly in terms of energy expenditure, its calorifi c content being only slightly less than that of the eggs it contains, but it protects the embryos developing within from predators as well as preventing the settlement of algae and fungi. 8.9 Conoidea: Turrids, Cones and Augers 191

8.9 Conoidea: Turrids, Cones and Augers

Murexes, which penetrate their prey’s armour by means of a sophisticated boring organ, are one of the peaks in the evolution of predatory snails. Another evolutionary peak is reached by the cones (Conoidea), which kill their prey by using a special venom-fi lled tooth, resembling a hollow harpoon or an injection needle. Most primitive among the Conoidea are the turrids (Turridae, Figs. 8.45 and 8.46 ) which fi rst appear in the fossil record of some 120 million years ago (during the Cretaceous period) and whose origin is in a group of sea snails with seven teeth in each row of the radula. This large family consists of some 70 genera. Turrids have a tall spire with a slit on the upper end of the outer aperture lip, and often a long canal at the base of the shell aperture, which accommodates the siphon. Turrids feed mainly upon bristle worms. Evolutionary trends within this group are refl ected in the teeth and radula: the most primitive genera still have fi ve teeth per row (two marginal teeth, two lateral ones and one central one, giving a formula of 1.1.1.1.1). In slightly more advanced genera there is a tendency to have only marginal teeth (1.0.0.0.1); in genera of yet more advanced evolutionary stages, each row has only one marginal tooth, either on the left or the right side, in alternating rows, so that only one tooth remains in each row. In the most advanced turrids, this single tooth tends to be elongate and to roll over itself into a scroll, forming a shape similar to a sharp hollow harpoon or hypodermic needle with hooks on its outside. This hollow tooth is loaded with venom.

Fig. 8.45 Turris, Xenoturris cingulifera (6 cm), Indo- Paciﬁ c, juvenile on left, adult on right 192 8 Predators

Fig. 8.46 Turris, Turris babylonia (7 cm), western Paciﬁ c

Fig. 8.47 Cone: a venom tooth

This evolutionary trend is completed in the closely related Conidae. They have no solid radular membrane and all that remains is a thin thread, which is torn when the tooth is launched from the radula sac to the mouth cavity. The cartilages underlying the radula are very much reduced, too, and often only connective tissues remain in their place. Each of a cone’s scrolled hollow teeth has one opening close to the distal, sharp end of the tube and another at its base (Fig. 8.47 ). The sharp end penetrates the prey’s body, and rigid barbs and dentate ridges along the shaft anchor the tooth inside it. Venom is then transferred from the tooth cavity through the opening near the sharp end and into the prey. A thick tubercle at the base of the tooth enables the trunk to keep a strong grip of the tooth once it is stabbed into the prey; it later serves as an additional lever to pull stung worms out of their burrows. Cone’s teeth are located inside the radular sac, which is positioned above the digestive system (Fig. 8.48) and not below it as in other snails. Some species have a radular sac divided into two zones, one in which the teeth are produced and the other in which they are stored. One tooth at a time is detached from the thread connecting it to the radula membrane in the production region, transferred to the storage region, then to the digestive system and trunk. How this transfer is carried out is as yet unknown. A long tubular venom gland, with a large liquid-ﬁ lled muscular bladder (‘bulb’) at its end, opens near the opening of the radula sac. The poison gland is 8.9 Conoidea: Turrids, Cones and Augers 193

Fig. 8.48 Cone: the venom apparatus derived from the oesophageal gland, as in whelks and murexes (Sects. 8.7 and 8.8 ). As a tooth leaves the sac and is moved towards the trunk, the bladder contracts and squeezes, and expels the venom of the tubular gland into the tooth cavity. When the venom-loaded tooth reaches the trunk, its lips hold onto the tooth at its base, and a circular muscle prevents it from slipping back. The tooth is now a ready-to-use poison dagger, to be stabbed into the prey when necessary. Usually, each tooth is used only once and a new tooth is transferred to the lips of the trunk from the storage zone. If the prey is killed and eaten, the tooth is swallowed with it. Some snail-hunting cone species stab their prey not once but with up to six successive daggers. Conidae is a large family of 500 species, all classifi ed within the single genus Conus, the earliest fossils of which date back to 50–55 million years ago (Eocene). The shell is heavy, conical and with a lower spire than turrids; the aperture is long and fairly narrow and there is no aperture-slit (as in the Turridae); the operculum, when present, is narrow and conforms to the narrow shape of the aperture. Species diversity is very broad and a single reef in the Indo-Pacifi c may support more than 20 different species of Conus. Most cone species feed on worms but some hunt sea snails, and approximately 10 % feed on fi shes; only a few species are generalists. Focussing on the fauna of the Red Sea, the diet of 13 of the 18 species consists of worms, three cones (including the poisonous species Conus textile ) feed on snails and two species on fi shes ( C. striatus and C. geographus ). Conus is a nocturnal creature. It spends its days buried in sand or beneath boulders, and at sunset emerges from its shelter and searches for prey. The food of fi sh- hunting cones includes blennies, gobies and other small fi shes of the sea fl oor. Upon locating a fi sh, the cone crawls towards it at a speed that is slow, even in terms of snail-speed, approximately 2 cm per minute. When a few centimetres from its victim, it gradually draws out its trunk, stretches it very slowly, and then – suddenly – it stabs the venomous dagger into the fi sh. Within seconds the venom is effective and the fi sh lies paralysed and helpless on the sea fl oor. The cone then draws out the front part of its mouth cavity, surrounds the prey and swallows it whole. Only when the meal is over does the trunk shrink and return into the body. The venom of fi sh-feeding Conus striatus of the Indo-Pacifi c (Fig. 8.49 ) contains a substance causing continuous muscle twitch. Nerve cells in the animal kingdom 194 8 Predators

Fig. 8.49 Cone, Conus striatus (9 cm), Indo-Paciﬁ c

generally function due to their ability to maintain an electric gap between their inside and their surrounding. This gap is maintained by two systems of tiny cellular gates in the cell membrane that, upon opening, enable controlled alternating out- leakage of sodium and potassium. The cone’s venom prevents the prey from closing the sodium gates and opening the potassium gates and thereby disrupts the electric signals that leave the nerve cell. The result is a continuous paralysing twitch of all body muscles (broadly similar to that caused by a continuous electric shock) and the fi sh soon dies with rigidly spread fi ns. Other fi sh-hunting species may have other venom components. Conus geographus, also of the Indo-Pacifi c (Fig. 8.50 ), has venom that contains a substance that sedates the fi sh; Conus purpurascens of the north-eastern Pacifi c (Fig. 8.51) has venom that contains a cocktail of several components, each with a different effect on the victim. Most active venom components of cones are small, highly structured peptides, each encoded by a separate gene. Every cone species has its own distinct repertoire of 100–200 venom peptides, each presumably having a physiologically relevant target in the prey species. The remarkable inter-specifi c divergence in venom peptide genes might perhaps suggest that cone-prey biotic interactions are species-specifi c to a certain extent. As all 500 cone species are classifi ed in a single genus, this suggests that their evolutionary diversifi cation took place mainly at the level of venom composition and of its molecular structure, rather than at the level of external morphological diversity, as in other snail groups. A cone sting may be fatal also to humans. Early symptoms among humans include sharp pain and a local paralysis; these later spread to the lips and mouth; eyesight is blurred, much saliva is secreted and the mechanism of voluntary 8.9 Conoidea: Turrids, Cones and Augers 195

Fig. 8.50 Cone, Conus geographus (8 cm), Red Sea, western Indian Ocean

Fig. 8.51 Cone, Conus purpurascens (4 cm), Eastern Paciﬁ c, from Mexico to Peru

muscles is paralysed; in severe cases also heart and lung activity is disrupted, and death may occur within 4 h of the sting. About forty cone sting fatalities have been recorded in the medical literature, to which the number of unrecorded cases must be added. Cones with stings fatal to humans include Conus textile (Fig. 8.52 ) and C. geographus. Others, such as C. arenatus (Fig. 8.53 ) of sandy sub-tidal habitats, and C. taeniatus (Fig. 8.54 ) of rubble habitats in the intertidal, are not fatal. Cone fertilisation is internal and the female lays a large cluster of hardened egg capsules which she ﬁ xes to boulders, rocks and stones. Some species attach each 196 8 Predators

Fig. 8.52 Cone, Conus textile (7 cm), Indo-west Paciﬁ c

Fig. 8.53 Cone, Conus arenatus (5 cm), Indo-Paciﬁ c

Fig. 8.54 Cone, Conus taeniatus (3 cm), Red Sea 8.9 Conoidea: Turrids, Cones and Augers 197

Fig. 8.55 Cone shell: vertical section; The inner walls are largely dissolved and are thin, thereby enlarging space inside the shell. The outer wall is reinforced, thereby adding defence

capsule to the boulder separately, and the whole cluster consists of several short rows, each consisting of several capsules; other species attach only some capsules to a boulder, and the remainder to the fi rst capsules. The egg capsule is shaped like a fl attened vase with convex margins, has a semi-transparent emergence window in its upper part, and a slender stalk with a wide base that attaches it to the boulder. The capsule is thick and strong, especially in species having only few large eggs, with a longer development time. The larger the egg the longer its embryonic development within the capsule, the more developed the emerging veliger and the shorter its stay in the plankton. The eggs inside the capsule develop into embryos, and veligers hatch after approximately 2 weeks. Veligers about to hatch are attracted to the semi- transparent emergence window at the top of the capsule, perhaps to the light that penetrates through it, and they break their way through the window into the sea. Eventually, the veliger descends to the sea fl oor and metamorphoses to its adult form. During growth, the inner space of the shell is continually reorganised (Fig. 8.55 ) with chalky material being added to the last whorl, to the inner side of the spire and to the front part of the columella; correspondingly, previous whorls are partially dissolved, leaving only narrow partitions. This continuous shell reorganisation results in both a strong external wall that increases defence ability against shell-crushing predators, and in an increase in space inside the shell for the growing body.

8.9.1 Terebridae, Augers

The augers (family Terebridae, with ﬁ fteen genera) are closely related to the Conidae. They have shells with an extremely long, slender spire consisting of many whorls, and a small aperture (Fig. 8.56 ). The long shell of an auger resembles that of the distantly related Turritella (Sect. 7.1 ) from which it differs in the short notch at the base of its aperture. The auger dwells in the sand and feeds on worms which it stuns with its venom gland, thereby immobilising them and then drawing them out 198 8 Predators

Fig. 8.56 Auger-shell, Terebra crenulata (10 cm), Indo-Paciﬁ c of their burrows. Some augers (Terebra ) have radular teeth and a venom apparatus similar to those of the cone, but their venom is weaker, different in its molecular structure, and there are no records of humans dying from their sting. In some augers ( Acus ) the venom apparatus is absent.

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Abstract Sea slugs (Opisthobranchia) use chemical defence instead of the shell’s mechanical protection. The shell is reduced or absent, the viscera are in the foot and the gill at the rear; most are simultaneous hermaphrodites, fertilisation is internal. Shield slugs (Cephalaspidea) are predators or herbivores. Mating partners usually alternate sexual roles; but sometimes copulations are outcomes of stabbing contests: rapidly stabbing partners mate as males, others as females. Sea hares (Anaspidea) feed on algae; for defence they produce ink. When mating, one partner is a sperm donor, the other a receiver. If a third joins, the receiver becomes a donor. Sea butterfl ies (Thecosomata) produce mucus nets to trap plankton; they copulate when all are males; upon becoming females, their stored sperm fertilises the ova. Sea angels (Gymnosomata) prey on sea butterfl ies. Leafl ets (Sacoglossa) suck algae, taking in chloroplasts which henceforth capture solar energy to produce carbon compounds for the leafl et. Mating partners practice hypodermic insemination: each thrusts his penis through the recipient’s skin and injects sperm into its body, which eventually reaches and fertilises ova. Side-gills (Pleurobranchidea) feed on sponges, taking in and storing calcareous needles in their skin; some secrete sulphuric acid. Nudibranchs (Nudibranchia) include dorids (Anthobranchia), who feed on sponges; some lose the penis after copulation. Aeolids’ (Aeolidina) lobes contain a branch of digestive gland ending in a ‘cnidosac’, to which cnidarian venom capsules are transferred; when attacked the sacs burst, and venom capsules discharge. Dendronotoids (Dendronotina) feed mainly on cnidarians; when in stress, some self-amputate their lobes.

Keywords Aeolidina • Anaspidea • Anthobranchia • Cephalaspidea • Gymnosomata • Nudibranchia • Opisthobranch defence • Opisthobranch evolution • Opisthobranch reproduction • Sacoglossa

The calcareous shell is of cardinal importance for survival in ever so many groups of sea snails because an endangered snail can retreat into it as a strong protective fort, ‘closing the gates’ behind it by blocking the aperture with a rigid operculum. However, one group of sea snails, the sea slugs and their allies (super-order Opisthobranchia) uses a completely different strategic approach to defence. The key to both individual and evolutionary success in these snails involves partial or complete negation of the shell as the main defence instrument, and its substitution by active chemical and biological defence. The peak of their success and evolutionary

© Springer International Publishing Switzerland 2015 203 J. Heller, Sea Snails, DOI 10.1007/978-3-319-15452-7_9 204 9 Shell Degeneration: Sea Slugs and Relatives progress is a sleek, elongated, worm-like, nude body, in which one must seek carefully to ﬁ nd any remnant of an external shell; if present, it is usually so reduced as to be of no importance in defence. The life style that accompanies this alternative is completely different from that of those sea snail groups discussed in previous pages. All in all, there are some 6,000 species of sea slugs and their allies. They occur in all seas of the world, in a wide array of habitats. The more primitive ones still have a functional shell; in other genera it is frail, reduced and imbedded into the body, partly or completely; but in most, the embryonic shell is completely lost each generation anew during metamorphosis. In numbers these 6,000 species cannot rival the 34,000 shelled species of sea snails but they surpass them by far in their morphological diversity, behaviour, diet, defensive adaptations, and in the ﬂ amboy- ance and extravagance of their body ornamentation. Indeed, they are among the most aesthetic and beautiful of all invertebrate animals. Considerable reduction or even complete loss of the shell occurs here and there among previously described groups, such as hoverers (Sect. 8.4) or certain parasite snails (Sect. 8.6 ); it also frequently occurs among land-dwelling snails (Pulmonata, Chap. 10 ). A slug body form has developed time and again, independently among different snail groups. Only in the opisthobranchs, however, has the slug form achieved such success in terms of body and species diversity. We do not know the precise age of the evolutionary track covered by opisthobranchs. There are fossils dating back 190 million years (the Jurassic) but because of the basic trend in this group to reduce and even to loose the shell, its ancestors do not stand high chances of remaining as fossils. Therefore, we must rely less on the fossil record in reconstructing the evolution of this super-order and more on comparative biology among the modern opisthobranch groups.

9.1 Functional Morphology from an Evolutionary Perspective

Early ancestors of the sea slugs that lived some hundreds of millions of years ago were, most probably, sea snails that fed in the upper layers of the sea fl oor. These early ancestors were probably shelled organisms that burrowed through soft mud in search of the rich diet to be found there, consisting of worms and other slow moving semi-sessile animals. As an adaptation to moving through such sediment, the head in these ancestral forms changed and became a fl attened spade-like shield (Fig. 9.1 ). The tentacles on top of the head (their usual position among sea snails) hindered burrowing, and over time shifted to the sides or rear of the head, or even merged with the head itself, becoming lost as distinct organs. Two large fl eshy fl aps evolved, one on each side of the foot, termed ‘parapodia’, and raising them prevented the entrance of sediment particles into the mantle cavity. Additional fl aps evolved from the nape of the head, and together they all overlapped the entire shell aperture. 9.1 Functional Morphology from an Evolutionary Perspective 205

Fig. 9.1 A primitive sea-slug (right ) compared to a typical marine snail (left ): the head resembles a shield for blazing a trail through soft sediment; tentacles are missing and eyes are small; the shell is covered by the parapodia and also by ﬂ aps arising from the nape and a ﬂ ap from the posterior part of the foot; the gill is behind the heart

The post-torsion mantle cavity and the fragile gill inside it shifted during evolution from their original front position more and more to the rear, until they reached a position behind the heart. (This character gives the group its scientifi c name Opisthobranchia, meaning ‘those with a rear gill’.) The now rear mantle cavity and gill location further prevented their clogging with sediment during burrowing. In virtually all Opisthobranchia, both the mantle cavity and the anus are positioned in the rear end of the body (or on the right side). The sea slugs are thus sea snails that have undergone ‘de-torsion’; namely they have reversed back to the original archaic condition of those sea snail ancestors in which their viscera, not yet twisted, opened at the rear of the body. As a word of caution before continuing: The taxonomy of opisthobranchs is currently in a state of turmoil, to such an extent that the very existence of the concept of Opisthobranchia as a natural group has recently been questioned; and so too have opisthobranch relationships with the Pulmonata (described in the next chapter). Until the taxonomy of those sea snail groups traditionally included in the opisthobranchs becomes more stabilised, in this book I present them in a classical, if somewhat outdated manner. We return to the shell, now enveloped by large fl aps rising as fl eshy folds of skin from the foot and nape. In this situation, the calcareous shell, instead of being external to the body and defending it from predators, is covered by parts of the body and is of little value as a defensive device. Deprived of its functional use, the shell 206 9 Shell Degeneration: Sea Slugs and Relatives gradually became reduced during evolution until in many groups it was lost; the now-exposed viscera were afforded some defence by becoming incorporated into the foot. Today, opisthobranchs in which the shell was not entirely lost have one that is a far more frail, transparent and fragile structure than in a typical sea snail. The operculum, present in those primitive sea snail stem groups from which the Opisthobranchia eventually evolved, falls off when the veliger settles and metamorphoses, in the vast majority. As a consequence of these evolutionary changes, advanced opisthobranchs have both external and internal bilateral symmetry of all body systems (Chap. 2) but for the reproductive apparatus, which remains predominantly on the right side of the body. In the adult sea slug no trace is left of the viscera’s radial symmetry, which, by its combination with the body’s bilateral symmetry, is one of the defi ning characteristics of the basic body structure of the phylum Mollusca (Chap. 1 ). The eyes are sessile, typically just below the translucent skin on the upper surface of the head, never stalked or extensible as in other sea and land snails. Many sea slugs are distatesteful to potential natural predators such as fi shes, crabs and lobsters; and the various manners in which these repulsive tastes are achieved are presented in this chapter. Also, many sea slugs are coloured in such fl amboyant ways as to foster the idea that their colours serve as a warning against the bearers of these repulsive tastes. On the other hand, the body of some other sea slugs, such as sea hares and leaf- lets, resembles their background so perfectly as to support the hypothesis that body colour and pattern form a highly effi cient camoufl age against predators. Not surpris- ingly, their have been many arguments as to the signifi cance of colour in sea slugs. Among opisthobranchs in general, in many instances, the more basal members of a specifi c group are more drably coloured while the more derived ones are more brightly coloured; corresponding data about the relative toxicity within these groups are currently not available. In contrast to most other sea snails in which the sexes are separate or the individual is a sequential hermaphrodite, all Opisthobranchia are simultaneous hermaphrodites. This means that each individual possesses, at the same time, both male and female fully developed reproductive systems, and that during copulation both systems usually operate simultaneously, so copulation may be mutual. Both the male and the female systems generally open on the right side of the snail, and fertilisation is internal. Each individual sea slug, although a simultaneous hermaphrodite, is usually incapable of self-fertilisation. Copulation between two individuals is often mutual, but it need not lead to immediate fertilisation. Maturation of the sea slug’s male system slightly precedes that of its female system. The male system as a whole is rather complex. It begins with a tube leading from the continuously sperm-producing male gonad (the testis); along its way, a section of the tube secretes nutrition for the down-streaming sperm and perhaps also substances which might appeal to the partner (this part is termed the ‘prostate’); the sperm continues along the tube until they reach the mantle cavity. From here the sperm is transferred, along a closed duct or an open ciliated groove, to the tip of the penis; this is a retractable organ, usually turned in like the fi nger of a glove and turned out only during sexual activity, when it is extended and erected by blood 9.1 Functional Morphology from an Evolutionary Perspective 207 engorgement. A sperm-storing sac often exists at the base of the penis to enable accumulation of the sperm between copulation bouts. Sperm accumulating in this sac are not motile and are incapable of fertilisation. Their activation and the attain- ment of fertilising power occur only after the sperm are transferred during copulation to another individual. It is this phenomenon of delayed sperm vitality which prevents self-fertilisation. During copulation, the penis penetrates the partner’s reproductive system through the female genital pore. The female system must cope with two functions, reception of foreign sperm from a mating partner and the laying of eggs. The female system has a vagina, from which two sacs arise to store sperm received from a partner at copulation. The sac close to the genital opening (the ‘bursa copulatrix’) is thin- walled and serves for short-term sperm storage, for digesting surplus sperm and for dissolving waste reproductive products. The sac closer to the ovule-producing gonad (sperm receptacle, also termed ‘seminal receptacle’ or ‘receptaculum seminis’) is thick-walled and serves for storing sperm for a longer time, and here the sperm gain nourishment, sometimes by embedding their heads in the sac’s thick walls. At the onset of fertilisation, multitudes of ripe ova leave the ovary and stream down the female oviduct. As they reach the oviduct, the nourished sperm rush out of the seminal receptacle and fertilise the ova. The female reproductive system also includes glands that coat the fertilised egg with mucus, albumen and membranes as protective layers around the eggs prior to spawning. The opisthobranch’s double reproductive system is morphologically extremely complex. The very complex structure is functionally focussed on the separation of two activities, that of the male and female gametes, and that of the routes followed by the individual’s own sperm to be delivered, and the sperm it receives from a mate. The precise details of the structure and organisation of the reproductive systems vary according to species, genus and maybe even family. In some primitive sea slug groups, the spawn takes the form of an ovoid or globular jelly bag in which the eggs are enclosed, and the bag is attached to the substratum by a gelatinous stalk. In other, more advanced groups, the spawn is in the form of a ribbon attached along one edge, or the spawn masses are cylindrical, capsule- fi lled cords attached along one side by a thin capsule-free sheet, or in the form of a small kidney-shaped jelly bag attached by one side. Large sized species tend to produce larger eggs and in greater numbers (up to a million); within any species, the larger individuals tend to produce more eggs than do smaller individuals. Finally, an individual produces its largest egg masses early in the breeding season, whereas later masses contain smaller numbers of eggs. The veligers hatch from the egg mass and swim upwards. The veligers of some species feed while swimming, the beating of the long velar cilia serving the dual purpose of imparting a forward movement and of bringing in a constantly renewed supply of sea water. Particles in the water are conducted swiftly towards and into the mouth by additional sets of cilia. Eventually the veliger descends to the sea fl oor and metamorphoses. Metamorphosis is usually triggered by the presence of adult food, but for many species the trigger is not known. During this development to a young adult, the larval shell and operculum are often cast off. 208 9 Shell Degeneration: Sea Slugs and Relatives

9.1.1 Life Cycles

Most sea slugs live only one year, usually no more than two, whereas other sea snails may live for many years (indeed, several decades in some cases). I do not know why sea slug longevity is so brief. Furthermore, some sea slug species have only one breeding period during their annual life cycle, while others produce numerous generations of offspring that year. Single-breeding species tend to feed on organisms that are abundant and stable all year round, such as corals and sponges, whereas those which produce several generations feed on more-or-less transitory prey, such as hydroids, that may spring up seasonally on sea surfaces and be cropped to extinction within a few days or weeks. Sea slugs that attack such organisms are active and voracious, and many of them attack a wide variety of food organisms; they mature very rapidly, thereby reducing the risk of dying without progeny, and spawning tends to occur throughout much of the year. A distinct lack of synchrony of the life cycles of the individuals of a population is characteristic of these hydroid- eating sea slugs, so juveniles and adults are often found side by side. This situation is contrary to the orderly, rather synchronous sexual development and spawning behaviour of sponge- and coral-feeding sea slugs, many of which feed on a single prey organism throughout the benthic phase of their life cycle. The evolutionary motivation behind the shift to a way of life characterised by burrowing through the soft mud was the rich diet to be found there. Several descendants of those fi rst sea slug groups emerged from this ancestral subterranean habitat to dwell on the surface of the sea fl oor, where they evolved into several major groups, each with its more-or-less specifi c diet. Some still dwell on the sea fl oor whereas others fl oat; some are herbivores whereas most others are carnivores. Table 9.1 presents the major orders and suborders of the super-order Opisthobranchia, the sea slugs. I repeat the word of caution mentioned previously in this section: the concept of Opisthobranchia as a natural group has recently been questioned. In this book I present them as a natural group in the classical, if somewhat outdated manner, until further research stabilised one of the recently suggested taxonomies.

Table 9.1 Major groups of Taxonomic Opisthobranchia, as described rank Opisthobranchia Sea slugs in this book Order Cephalaspidea Shield slugs, bubble shells Order Anaspidea Sea hares Order Thecosomata Sea butterﬂ ies Order Gymnosomata Sea angels Order Sacoglossa Leaﬂ ets Order Pleurobranchidea Side-gills Order Nudibranchia Nudibranchs Suborder Anthobranchia Dorids Suborder Aeolidina Aeolids Suborder Dendronotina Dendronotoids 9.2 Cephalaspidea: Shield Slugs and Bubble Shells 209

9.2 Cephalaspidea: Shield Slugs and Bubble Shells

The shield slugs (Cephalaspidea) are primitive sea slugs. Most dwell within the upper layers of the sea fl oor. Their head resembles a shield (the scientifi c name of the order, Cephalaspidea, means head-shield) and during crawling it is often positioned slightly beneath the surface of the sediment. A delicate, thin scarf of mucus mixed with mud is often thrown upwards, onto its back. In this manner a continuous collapsing mucus tunnel may be formed, that trails behind the slowly advancing sea slug. The more primitive shield slugs still have a shell of some sort. In some it is even quite prominent and resembles that of other sea snail groups. Many other shield slugs have only a frail, swollen, transparent shell in which the calcium content is low and the organic content high, proportions lending the thin shell fl exibility rather than strength. The spire is hidden beneath the younger whorls and the aperture is wide open; there is (usually) no operculum. Some shield slugs have an internal shell ( Chelidonura, Navanax ). Shield slugs form a large order with 85 genera. One of the more primitive shield slug genera is Acteon , living on the northeastern Atlantic coasts. Its shell is external, solid, thick and has a distinct spire, its foot carries an elongate operculum and its gill is in a forward position. These characters bring Acteon close to many sea snails of other groups, but the fact that it is a simultaneous hermaphrodite that possesses a dual reproductive system with a penis that folds inwards like the fi nger-of-a-glove, reveal that it is a stem group on the evolutionary road leading to the Opisthobranchia. Acteon dwells in shores of sand and mud. It uses its fl at head to furrow its way into the upper centimetres of the sea-fl oor in search of bristle worms, which it locates by the clusters of sensory cells spread along the front of its head. Upon locating a worm it burrows down to a depth of 5–10 cm, seizes it with its radula and swallows it whole. During reproduction, Acteon lays fi ve to ten clusters, each containing 200,000 eggs. Another primitive genus is Hydatina (Fig. 9.2 ) that, like Acteon, has a calcareous shell containing the viscera. Hydatina differs from Acteon in its thinner, swollen and spire-less shell, in lacking an operculum and in its huge foot. It, too, feeds on bristle worms but is found in the Indo-Pacifi c in shallow waters.

Fig. 9.2 Shield-slug, Hydatina physis (9 cm), Indo-West Paciﬁ c 210 9 Shell Degeneration: Sea Slugs and Relatives

Fig. 9.3 Bubble shell, Bulla arabica (7 cm), Red Sea and Arabian Seas

Fig. 9.4 Shield slug, Atys semistriatus (2 cm), Indo-West Paciﬁ c shell

Molecular studies suggest that Acteon and Hydatina , forming the distinct group Acteonoidea, may be only distantly related to other shield slugs. The genus Bulla (Fig. 9.3 ) has a well developed solid shell into which the snail retreats in times of danger. Upon retreating it secretes a substance poisonous to ﬁ sh and crabs from a special white gland along the margins of its mantle. Unlike Acteon and Hydatina , Bulla is herbivorous. It is presumably from this group of herbivorous shield slugs that another herbivorous group of sea slugs eventually evolved, the sea hares, discussed in the next section. Atys (Fig. 9.4 ) has a swollen external shell containing all the viscera, though it is reduced and forms only a soft, transparent, delicate envelope. The parapodia and the rear ends of the nape ﬂ aps cover the entrance to the mantle cavity and prevent sediment particles from entering. Very little is known about its habits. Haminoea , a genus close to Atys , tends to plough over the soft sediment rather than to burrow into it. It can adapt its body colour to slight changes in the surrounding substratum colour resulting from changes in location, by use of special pigment cells distributed beneath its skin that 9.2 Cephalaspidea: Shield Slugs and Bubble Shells 211

Fig. 9.5 Shield slug, Phanerophthalmus albocollaris (1 cm), Indo-west Paciﬁ c

Fig. 9.6 Shield-slug, Colpodaspis thompsoni (0.5 cm), Indo-west Paciﬁ c

contract under nerve control. The process of a radical change in body colour from black to white takes some 10 days; this may seem a long period, but the substratum over which Haminoea crawls in nature probably does not change at a greater speed. Sediment particles sticking to the mucus cover of the body also help conceal the snail. During the reproductive season many Haminoea individuals gather in groups, and may crawl one behind the other in a fi le along a mucus path, following some individual that just happens to be fi rst. In case of stress, one individual secretes a special substance from a gland in its skin, and other individuals in the vicinity respond by fl eeing. This ‘alarm substance’ might reduce predation during the reproductive season when the individuals are gathered in high numbers. Haminoea is a herbivorous sea slug feeding on fi lamentous algae, unicellular algae and detritus gathered while ploughing through the sediment. Phanerophthalmus (Fig. 9.5 ) has a reduced external shell, connected to the rear of the body as though it were a transparent, fragile fi nger-nail and the visceral mass is incorporated into the back. In Colpodaspis (Fig. 9.6 ) the shell is entirely internal. 212 9 Shell Degeneration: Sea Slugs and Relatives

Fig. 9.7 Shield-slug, Chelidonura ﬂ avolobata (7 cm), Red Sea

Another group of shield slugs is the Aglajidae, including Chelidonura (Fig. 9.7 ). The reduced, cap-shaped shell is internal and completely covered by the posterior section of the body; the mantle cavity faces the rear end of the body. Aglajids are voracious predatory shield slugs that attack sea hares, shield-slugs of other groups, and also small individuals of their own species. The eyes are large and the mouth is surrounded by clusters of sensory cilia, enabling fi rst to sense the presence of the prey and then to locate it by groping along its mucus path. Philinopsis feeds on prey twice its size, including the shield slug Bulla . This prey is swallowed whole and digested within a few hours, after which the empty shell is vomited. When under stress, an aglajid releases a yellow substance from a special yellow gland that causes a fl ight response among other individuals of the species. The fl ight-substance in this secretion is not produced autonomously by the aglajid itself, but by its victims; during predation the aglajid swallows these substances and transfers them to special glands in its skin. Secondary use of these substances helps an aglajid avoid being preyed upon. Some shield slug species copulate by alternating their sexual roles consecutively, and some alternate between roles several times. Pairs of other species copulate, or try to copulate, playing both sexual roles simultaneously; but are sexually satisfi ed if they manage to complete their male role fi rst; they then may refuse to play female. The aglajid Navanax inermis (Fig. 9.8), found in the north-eastern Pacifi c, tends to copulate in bouts, the members of a pair alternating sexual roles. A bout is initiated by the individual who will act as a male during the fi rst copulation, and courtship is largely a male activity. That individual turns to and follows the mucous trail of another individual, who will fi rst play the female role. Upon reaching the ‘female’ ‘he’ touches her tails and follows ‘her’. When fi rst contacted the ‘female’ continues crawling but gradually ‘she’ unfolds her parapodia and spreads them aside, and the male goes on and explores her parapodia and back. She now raises the 9.2 Cephalaspidea: Shield Slugs and Bubble Shells 213

Fig. 9.8 Navanax inermis (22 cm), north-eastern Paciﬁ c

Fig. 9.9 Siphopteron quadrispinosum (0.5 cm), Indo-Paciﬁ c

posterior end of her body to make her genital pore accessible and eventually she stops crawling and remains motionless while the male pushes out his penis, reaches the female’s genital pore and copulates. Then the roles are reversed, as the up-to- now-‘female’ individual begins ‘male’ courtship behaviour towards the up-to-now- ‘male’, who assumes the female role. This courtship leads to a second copulation, with reversed sexual roles. This may be followed by a third copulation with sexual roles reversed yet again, and so on. The pair may reverse sexual roles and copulate up to six times, each bout with strict sexual role alternation. All Navanax inermis individuals copulate over equal times and for equal lengths of time as male and female, and do not tend to specialise in one sexual role. Egg masses are laid on seaweeds, such as Sargassum and Cystoseira . The shield slug Siphopteron quadrispinosum (Philinidae) of the Indo-Pacifi c (Figs. 9.9 and 9.10 ) has a unique mating mechanism whereby copulations are the outcome of a stabbing contest that precedes copulation. This shield slug has a peculiar reproductive anatomy, the male copulating organ consisting of two, not one, eversible structures: a muscular penis equipped with two to fi ve large spines and a series of small spines to anchor the penis within the genital pore, and a tubular branch diverging from the prostate and ending in a papilla with an eversible terminal style, to plant sperm-nourishing liquid into the female. Following accidental encounters, these shield slugs respond by head retraction, vigorous parapodial fl ap- ping, swimming, and attacking of the partner with the eversible pharynx. If sexually motivated by these activities, the individuals continue to the next phase, circling clockwise. During this movement each individual everts the tubular branch and the penis towards the other and probes the partner’s ventral side with the style, and the female genital pore with the penis. Then they start style stabbing and piercing. Both 214 9 Shell Degeneration: Sea Slugs and Relatives

Fig. 9.10 Siphopteron quadrispinosum , everted male genitalia (Based on Anthes and Michiels 2007 )

individuals keep their front ends turned away from the mate and shake their parapodia laterally to hold off the partner’s style and penis. If both partners’ sexual drives are balanced and style-stabbing is synchronous, these interactions will lead to mutual style and penis insertion resulting in mutual insemination. Each individual fi rst inserts the style into the other’s female organs and injects prostate fl uids into the other individual. Both then inseminate each other by inserting the ‘true’ penis into the other’s genital pore and transferring sperm. If, however, despite a strong male mating drive in both partners, one partner successfully stabs more rapidly while the other tends to probe rather than to stab, a one-sided mating will ensue. In this case the more active individual will continue shaking its parapodia whenever approached by the partner’s male organ, and will keep the partner at a distance by its inserted and infl ated male apparatus. The less successful partner fails to insert and is thereby enforced to fulfi l the female role only. It may still attempt style and penis insertion but, after a couple of minutes, these attempts gradually cease. Withdrawal requires considerable pulling to disengage the penis spines anchored in the genital chamber. If copulation was mutual, both partners crawl apart upon withdrawal without extra mating attempts. If copulation was one-sided, the insemi- nated individual follows the partner’s withdrawal by vigorous continued attempts at stabbing and penis intromission, to fulfi l its male sexual role. However, the insemi- nating individual thwarts these belated attempts by shaking its parapodia, by penis infl ation, rapid circling, by minimal exposure of the ventral side and by departing immediately without an incentive to be in the receptive role. Consequently, these attempts of the receiver to function also as a donor are usually not successful. Aggressive stabbing thus serves to bias copulations in favour of the animal’s own male function. The benefi ts of this to the individual is not yet understood. 9.3 Anaspidea: Sea Hares 215

9.3 Anaspidea: Sea Hares

Sea hares (Anaspidea, Fig. 9.11 ) live on the surface of the sea fl oor and not inside it, as do many shield slugs. The head does not plough through the sediment and does not resemble a fl at shield (the scientifi c name of the order, Anaspidea, means ‘lacking a shield’). Two rolled tentacles, termed ‘rhinophores’, stand out from the top of the head and serve for chemical sensing. In evolutionary perspective they are a new organ not present in shield slugs, the group from which the sea hare ancestors evolved, and they are of a different embryonic source than the usual head tentacles of other sea snails. Large parapodia cover the mantle cavity, which is positioned on the rear of the body. The primitive sea hare Akera still has an external shell resembling that of a shield slug; most other sea hare genera have a much reduced internal shell and all that is left of it is a small plate completely hidden within the mantle; indeed some species have no shell whatso-ever. The humped body of this sea slug, combined with its ear-shaped rhinophores, form a silhouette somewhat similar to a crouching hare. The name Lepus marinus (=sea hare) was coined by the Romans, and over the centuries translated to many other languages. The sea hare order includes ten genera, including Dolabella (Fig. 9.12 ).

Fig. 9.11 The sea hare Aplysia californica (50 cm), north-eastern Paciﬁ c

Fig. 9.12 Sea hare, Dolabella auricularia (30 cm), Indian Ocean and north-western Paciﬁ c 216 9 Shell Degeneration: Sea Slugs and Relatives

9.3.1 Feeding

Sea hares are herbivores throughout their lives, and are found in tidal zones and in shallow waters where light penetrates and algae grow, in a wide variety of rocky, sandy and muddy substrata. Algae are not a very nutritious food, but they may occur in abundance. Most sea hares feed on a wide array of green and red algae, and a single species may exhibit considerable variation in its diet, during its life, over the seasons and over different habitats. A sea hare responds to the presence of algae by crawling in the direction of food while waving its head from side to side. Touching the food causes a refl ex chain-response of biting and swallowing, accompanied by an increase in heart pace and fl ow of blood. Sea hares are voracious animals that devote several hours a day to feeding, and they can consume a quantity of food reaching one third of their body weight each day. Accordingly, sea hares may reach the amazing weight of 6 kg and more. They bite off algae with their jaws and radula and transfer chunks of alga tissue into a large storing oesophagus (Fig. 9.13 ) that may contain up to 10 % of the body weight during feeding. The food is transferred from here to a gizzard in which there are two chambers: the fi rst has large gizzard plates that grind the food and crush it, and the second has delicate teeth on the wall and strains the food. The resulting pulp is transferred to the digestive gland for digestion, and then goes through the intestine for absorption of nutrients and is excreted as faeces. Sea hares are among the few sea snails capable of coping with large chunks of plant matter. A sea hare receives all the energy it requires for growth and for reproduction from these algae.

Fig. 9.13 Digestive system of a sea hare (Based on Thompson 1976 ) 9.3 Anaspidea: Sea Hares 217

In addition to energy, the sea hare may receive a remarkably strange and interesting substance from the algae: ink. The ink originates in red algae and the sea hare concentrates it in a special gland that opens into the mantle cavity. The gland contains red, purple and blue pigments. The purple pigment (its formula is C34 H40 N4 O7 ) originates in the photosynthetic pigment. When a sea hare feeds on a red alga, its photosynthetic organelles (named ‘rhodoplasts’) are released from the alga cells into the sea hare’s stomach. They are then transferred to special cells in its digestive gland, in which they are transferred to special intra-cellular vacuoles. Here the red pigment, phycoerythrin, is released from the photosynthesising organelle, undergoes a chemical change and enters the blood system. It is transported through the blood system and eventually reaches the sea hare’s ink gland, where it accumulates in giant cells surrounded by a layer of muscles. Ink ejection (Fig. 9.14 ) is on an all- or- nothing basis, namely the gland either empties its entire contents or does not empty even a drop. Upon being exposed to air and to light the pigment changes colour from red-purple to dirty-brown. Replenishment of the ink storage tank takes 2–3 days. Aplysia depilans has no gland and therefore accumulates no ink; Aplysia fasciata ejects ink mainly when disturbed during copulation. Ink considerably reduces the palatability of sea hares to a diversity of potential predators including ﬁ shes, birds, crustaceans, and sea anemones. It also contains alarm signals that evoke escape behaviour in nearby individuals.

Fig. 9.14 The sea hare Aplysia californica inking 218 9 Shell Degeneration: Sea Slugs and Relatives

Sea hares also possess an odour-producing gland, the ‘opaline’ gland, positioned on the ﬂ oor of the mantle cavity. Its secretions consist of a clear-to-whitish liquid (opaline) which polymerises and becomes highly viscous upon contact with water. Both the ink and opaline glands are under neural control and release their secretions only when the sea hare is attacked by a predator, suggesting that these glands function mainly in chemical defence. These secretions contain some chemical compounds at extremely high concentrations, in both ink and opaline. Other compounds occur in ink alone or in opaline alone, and still other compounds are generated only when ink and opaline are co- secreted, and mixed in the mantle cavity. Escapin is present only in the ink gland whereas its substrate L-lysine is present only in the opaline gland; the enzyme and its substrate are mixed only when ink and opaline are co-released. Mixing and formation of the defensive secretion then takes place in the mantle cavity. Such mixing of two inactive chemicals that react to form an active deterrent is a mechanism for generating deterrent compounds only when needed and in this manner defensive compounds can be packaged to prevent auto-toxicity. The ink-opaline mixture produces a variety of responses in potential predators, thus spiny lobsters avoid the mixture and produce escape responses. The mixture also acts as an alarm that evokes escape behaviour (rapid turning and escape locomotion) in neighbouring individuals when a nearby sea hare is attacked; the response is especially prevalent in juveniles.

9.3.2 Life Cycle

Sea hares have an annual life cycle, which may, however, vary from half a year to 16 months, depending on environmental conditions. Scent secreted into the water by one sea hare infl uences other individuals, and they gather in large groups. Usually copulation is not mutual: one individual functions as a sperm donor (the ‘male’) and the other as the sperm receiver (the ‘female’). It begins when one individual moves towards another, waving its head as when moving towards a source of food. The approaching animal climbs onto the approached individual, inserts his masculine organ and donates sperm. Copulation sexually stimulates the sperm recipient (the female) and after a few minutes she crawls away, amidst head waving and the ‘male’ individual riding on the top rear, and seeks another individual, with whom to copulate. Once a third individual is found, the second, ‘female’ individual changes role to that of a sperm donor, namely to a ‘male’. In this manner, a chain of copulating sea hares begins, which can reach up to 20 individuals; all serve simultaneously as male and as female, but for the fi rst leading individual which serves only as a female, and the last, rear-guard individual that functions only as a male. Furthermore, two ‘males’ may happen to simultaneously copulate with one ‘female’, so the possibility is open for branching chains of copulating sea hares crawling along the sea fl oor in a Y-shaped parade. There may be high turnover within such a chain and only a third of the individuals participating in a copulating group may be there also on the 9.3 Anaspidea: Sea Hares 219 following day. When only two individuals copulate, there is a certain tendency for young individuals to function mainly as males and for older ones to function largely as females. Some time after copulation the sea hare, as a female, begins laying eggs, and she may produce more than 100 million eggs throughout her life. The sea hare has enormous reproduction potential, the extent of which depends on many factors. Depending upon temperature, light and food (that hasten maturity) adult sea hares will begin egg-laying only 2–3 months after having alighted from the plankton and metamorphosed, and they will lay many times throughout their lives. Spawning need not occur immediately after copulation. A special organ, the sperm receptacle (‘receptaculum seminis’) can store sperm of another individual for several months, until the ova are ripe. When ripe they pass over this pouch, and the sperm rush out, swim vigorously to the ova and fertilise them. Soon after fertilisation, the eggs are coated with albumen that provides nutrients for the developing embryo; they are enveloped in a delicate membrane, and then packed into capsules. Usually there is only one egg per capsule, but sometimes there are more, up to 45. There is considerable variation even within the same batch. Before the capsules emerge from the female reproductive opening, they are covered with thick layers of mucous jelly that combines and sticks them together into a long cylindrical thread; this egg thread is ejected from the common sex groove. The sea hare sticks these egg threads onto boulders or a nearby alga with movements of the head, and the embryos will develop here until hatching. A single thread may reach 40 m long and contain 26 million eggs. The mere presence of an egg thread may encourage other individuals to lay their threads on it, so that sometimes a big mass of threads is formed. A single copulation provides enough sperm for several egg batches. Therefore, egg laying may continue for days and weeks after copulation, without necessitating further copulations; one individual may lay 100 million eggs before its store of acquired sperm is completely depleted. Under stress conditions, such as lack of food, the sea hare devotes considerable time to egg laying and spawns day and night. Under conditions of plentiful food, it devotes only about half that time to reproduction and spawns only during the day. This behavioural plasticity has survival value, since under conditions of plenty, the sea hare can devote considerable effort to its own growth, which leads to more eggs; under deprived conditions, she will immediately produce descendants that will be carried far away, where perhaps food will be found. After hatching, the veliger swims upwards into the illuminated layers of the water, where there is an abundance of tiny unicellular algae that serve as its food. Here it is also carried away by horizontal currents, which carry it far from the site where it hatched. The time it dwells in the plankton is infl uenced by temperature and food, perhaps also salinity. In general, some 30 days after hatching, growth ceases and the veliger is ready for metamorphosis to adult form. If a suitable substratum is found, it settles and metamorphoses, and if not – it will continue to live in the plankton, keeping its option to metamorphose for up to another 200 days, before dying. 220 9 Shell Degeneration: Sea Slugs and Relatives

When life in the plankton is so long, currents may carry the veliger thousands of kilometres, and therefore the range of some species is very extensive. However, lingering in the plankton goes together with high mortality: predation, lack of food or being swept away into the sea, far from any shore and seaweed. Only one thousand parts of 1 % of sea hare veligers that hatch survive the life phase in the plankton, and are lucky enough to settle and metamorphose. The veliger gets the chemical cues to settle and metamorphose from substances present in green and red algae, and this increases the settlement and recruitment of the individuals to a population under conditions of plentiful food. The chemical identity of the metamorphosis-inducing substances is as yet unknown. Veligers of different sea hare species prefer different algae, but the range of preferences is broad and veligers of many species will settle in response to any algae of the genera Ulva , Enteromorpha and Caulerpa. The growing veliger metamorphoses and becomes a juvenile sea hare crawling over the sea ﬂ oor and eating algae. Growth is rapid and maturity is reached within a short time. During maturity, most activity hours are devoted to feeding, copulation and egg-laying. Little is known about the causes of senescence. After 3–16 months of life the individual looses weight, lays fewer eggs, its parapodia shrink, body pigment is lost, the sole of its foot swells, the extent of response to external stimulations decreases, and the heart responds less to food stimulations; eventually the sea hare dies. One consequence of the dependence of sea hares on algae is that their life cycle is dependent upon that of the algae upon which they feed, and when the algae disappear so do the sea hares.

9.3.3 Movement

Sea hares move mainly by crawling. Sometimes they dig and bury themselves into soft mud substrata, mainly during the day. This might serve as a protective step against both the damaging effects of ultraviolet radiation and also from desiccation, at low tide. An individual may remain buried for any length of time, from 1 h to several weeks. Digging by one individual often inspires digging by neighbouring individuals; likewise, one individual leaving its trench will be accompanied by neighbouring individuals leaving their trenches. Sometimes massive copulations occur just after arising from the sand. Sea hares sometimes swim. The parapodia are spread, waves of contraction pass from the front of the parapodia to their rear and synchronic swimming movements begin. A sea hare may swim when food reserves in its environment are depleted and it explores new surroundings. Indeed, hunger encourages swimming and a satiated individual will not swim. Aplysia fasciata of the Atlantic Ocean and Mediterranean Sea swims only when the sea is calm and usually only for brief periods of time, but a swim lasting half an hour has also been recorded. Sea hares tend to swim more during the night than during daytime, and when food is scarce rather than plentiful. 9.3 Anaspidea: Sea Hares 221

Fig. 9.15 Jet-hare, Notarchus indicus (6 cm), Indo-Paciﬁ c, Red Sea, Mediterranean

Fig. 9.16 Jet swimming in Notarchus indicus (Based on Schuhmacher 1973 )

The increasing importance of the parapodia in swimming has lead to the evolution of jet swimming in the tropical sea hare Notarchus (Fig. 9.15 ). Its two parapodia are fused above the back, except for a short slit. The parapodia margins bordering on the slit are fl exible and the parapodia can rise above the mantle and constrict to form two openings, the one in front for sea water entrance and the rear for water expulsion. Coordinated alternate opening and closing of the two parapodia ends propels Notarchus in a somersaulting fashion. When swimming, the sea hare fi rst closes the rear opening and opens the front one to let water into the large cavity formed beneath the parapodia, so the entire body becomes globular; the front opening is then closed; next the rear opening is opened, and muscular contraction of the parapodia causes the water in the cavity to be squeezed out in a strong jet. As the rear opening is directed downwards, the jet lifts the snail steeply in the water column (Fig. 9.16 ). Once this phase is completed, the snail somersaults in the water, while taking in more water into the parapodia cavity. Repeated rising in the water by propulsion accompanied by somersaults enables the sea hare dispersal also as an adult and not only as a veliger (as in most sea slugs). Short-term swimming, as in sea hares, probably led to the evolution of long-term swimming of another, distantly related group of sea slugs, the sea butterfl ies. 222 9 Shell Degeneration: Sea Slugs and Relatives

9.4 Thecosomata: Sea Butterﬂ ies

The sea butterﬂ ies (Thecosomata; Figs. 9.17 , 9.18 , 9.19 , and 9.20 ) are an order of sea slugs adapted to life in the water column, and they migrate daily between two strata of the sea, the deep abyss and the sea surface. Many sea butterﬂ ies have a shell, a very light one. The group comprises 15 genera. Some of these genera ( Limacina , Peraclis ) have a shell that is coiled leftwards and closed by an operculum, in others it is symmetrical and without an operculum. In some of the symmetrically-shelled genera the shell is narrow, wedge-like and pointed ( Creseis ) while in others it has the form of a broad wedge (Clio ) and in others still the wedge is considerably reduced and the margins of the mantle rise and form a swollen, globular structure ( Cavolina). All these genera have a very thin shell (one hundredth

Fig. 9.17 Sea-butterﬂ ies: (a ) shell of Cavolina, front and lateral views; ( b ) shell of Peraclis (Based on Van der Spoel 1976 )

Fig. 9.18 Pseudo-conch of Cymbalia (Based on Van der Spoel 1976 ) 9.4 Thecosomata: Sea Butterﬂ ies 223

Fig. 9.19 The sea-butterﬂ y Cavolina while feeding (Based on Gilmer and Harbison 1986 )

to one tenth of a millimetre thick) that weighs very little, as an adaptation to life in the plankton. Sea butterfl ies are further characterised by the many fl aps that extend and project from their body and help them rise to the sea surface: two pairs of muscular parapodia (that may fuse to form a single platform) and another four fl aps drawn out of the mantle. Cavolina has some fl aps that protrude through special slits in the shell and some that trail behind them in the sea like long threadlike trains. Spreading all fl aps and trains increases the snail’s buoyancy and changing the extent of the spread regu- lates its fl oatability. Some sea butterfl ies have protruding fl aps on the back that arch upwards, so that a small space is formed between them and the small thin shell. This external space is fi lled with a jelly substance, which also adds to the snail’s buoyancy. Both Gleba and Cymbulia have no shell, but have an internal ‘pseudo-conch’: a large mass of jelly within which there is a deep depression containing the snail’s viscera; the outer side of the pseudo-conch may be covered with spines or tubercles (Fig. 9.18 ). Some sea butterfl y genera migrate hundreds of vertical metres daily: during the day they dwell in the abyss, and at night they rise to the sea surface to feed. This reveals another advantage of the fl aps: their inner surfaces are covered with many mucus-discharging glands as well as with cilia. When feeding during the night, the butterfl y spreads all its lobes (Figs. 9.19 and 9.20 ) and remains motionless in the water column in an upside-down position, its back facing downwards. Some of the fl aps orient themselves around the mouth as a funnel and, assisted by a large mucus gland at the mantle cavity opening, discharge a net of mucus from their inner surfaces. This net is spread above the upside-down snail like the canopy of a parachute. The net, which may reach over 2 m in diameter, traps various tiny organisms fl oating in the plankton, sized up to one tenth of a millimetre. Sometimes the fl ap margins are coloured, perhaps to serve as bait that lures the tiny plankton organisms to the 224 9 Shell Degeneration: Sea Slugs and Relatives

Fig. 9.20 The sea-butterﬂ y Peraclis while feeding (Based on Gilmer and Harbison 1986 )

net. Cilia constantly move new mucus threads to two grooves on special lobes of the foot; they afford additional assurance of continued contact between the mouth and the net when actual feeding takes place. The plankton-loaded mucus net is hauled in towards the grooves of the trunk every 20 min. Here it is worked into a strand of mucus that is pulled towards the mouth. First it is transferred into the fl ap funnel, the movement of its cilia then pulls the net towards special fl aps on the foot. A certain sorting of the particles occurs on these fl aps: some of the catch is thrown back to the sea as pseudo-faeces and the rest is transferred into the mouth. The food consists of tiny planktonic organisms, so there is no need for a powerful radula and accordingly the radula is reduced, or even absent, as in Gleba. A large crop with chitinous pro- jections in the front part of the digestive system enables the temporary storage of the engulfed mucus nets and the crushing of the hard skeletal parts of the tiny food trapped on it. Sea butterfl ies spend most of their time passively fl oating upside-down in the water, parapodia above and shell below. They are thus “spiders of the plankton” that make a living by netting prey. Sea butterfl ies actively swim when in fl ight. First they detach themselves from the net; then they move by rowing movements of the parapodia. They can also rapidly retreat into the shell by contraction of the shell muscle, or lift the parapodia vertically above the body to sink to deeper waters. Sea butterfl ies are consecutive hermaphrodites: Each individual juvenile develops fi rst into a male with a sperm-producing gonad, a penis and prostate; after some time the penis and prostate are absorbed into the body and the individual becomes a female, with the gonad now producing ova and the genital duct glands producing albumen. Accordingly Limacina trochiformis individuals copulate when all individuals are in their masculine phase. Each individual both donates 9.5 Gymnosomata: Sea Angels 225 and receives sperm, which he stores in his sperm receptacle. Upon reaching the female phase, this individual’s ripe ova descend along the female tract and are fertilised. The eggs are cast into a capsule containing albumen, enveloped in mucus, and laid in a mass that fl oats in the water. The veligers hatch with small fl aps on either side of the foot. Eventually, when the sails are absorbed into the veliger’s body, these fl aps develop into parapodia that will carry out the sea butterfl y’s locomotory function. Limacina infl ata, from circum-tropical and circum-temperate waters, has no penis in the male phase, and neither albumen nor mucus glands in the female phase. The eggs are fertilised in the common sex duct and then released to the mantle cavity where they continue their embryonic development. A female contains approximately 45 juveniles, which are eventually released as well-developed veligers. Cavolina may sometimes aggregate near shores in dense swarms of up to 100 individuals per cubic metre of sea water. The individuals copulate in shallow water, and spawn. The adult individuals die a few days after egg spawning, and their empty shells are washed up the shore where they form a dense belt. However, swarming is rare both in this genus and in sea butterfl ies in general, and may perhaps be related to specifi c changes in the local marine environment. A butterfl y swarm was observed in the Red Sea a few days after a rare torrential rain had swept much silt and allu- vium from the surrounding desert mountains into the sea.

9.5 Gymnosomata: Sea Angels

Sea angels (Gymnosomata) spend their lives actively swimming in the sea. This group of sea snails has a gelatinous, mostly transparent body that completely lacks a shell (Fig. 9.21 ; the scientifi c name of the group means- having a naked body). Furthermore, they have no mantle cavity and the parapodia are small; therefore their rowing motion is slow, but more controlled than that of the sea butterfl ies. Indeed, without this controlled movement that enables considerable manoeuvrability, sea angels would not be able to catch their main prey – the sea butterfl ies. Sea angels are an order comprising approximately 20 genera. They and the sea butterfl ies may be sister groups, which together are closely related to the sea hares. Different sea angel species specialise in preying on different sea butterfl y species, and three examples are discussed briefl y here. Clione limacina, a polar species of the Arctic, is a 7 cm-long sea angel with an elongate, symmetrical body. The head bears a pair of tentacles and the body bears a foot that is divided into three lobes. The slug has no gills and all respiration is carried out through the skin. Swimming is perpetual, throughout the life of the sea slug. While swimming, the parapodia beat in concert. Clione limacina has two suites of swimming muscles, those that contract 226 9 Shell Degeneration: Sea Slugs and Relatives

Fig. 9.21 A sea angel Clione limacina (7 cm), Arctic Ocean, northern Paciﬁ c and northern Atlantic

slowly and fatigue slowly, and those that contract quickly but also tire quickly. This dual muscular system enables the sea angel’s energetic swimming adaptations to function in several ‘gears’. This sea angel feeds on the butterfl y Limacina , and when offered an individual of this genus (in the lab) it immediately extends six hunting arms (Fig. 9.22) from special pouches in the front part of its body. The arms wind around the prey very rapidly (within 50–70 thousandths of a second) and hold on to it; a sticky substance fl ows out from small papillae on their surface, enabling the sea angel to adhere to its prey’s shell and grasp it. When the prey ceases struggling and gives up escape attempts, or when it withdraws into its shell and blocks it with its operculum, the predator’s hunting arms turn the shell around until its aperture faces the predator’s mouth. The sea angel now pushes the prey’s operculum aside and draws out another set of organs from within its mouth: a radula with hook-like teeth and a pair of muscular sheaths, each containing ten small hooks. These hooks are drawn out, erected, and driven into the fl esh of the prey, and at the same time the radula is extended (each row has 11 teeth, one central and fi ve laterals on each side, 0.5.1.5.0). The hooks and the radula pull the prey from the depths of its shell, and it is swallowed, entire, within approximately 40 min. The ‘stomach’ in which the prey is digested is actually formed by two spacious digestive gland diverticula, which have replaced the true stomach. A sea angel eats up its sea butterfl y in a hurry, lest neighbouring angels gather around and rob it of its food. Having fi n- ished its meal, the angel disposes of the empty shell, and within minutes it is ready to predate its next sea butterfl y. 9.5 Gymnosomata: Sea Angels 227

Fig. 9.22 The sea angel Clione predating the sea-butterﬂ y Limacina (Based on Lalli 1970 )

Pneumodermopsis paucidens of the northern Atlantic and Mediterranean (size 0.5 cm) has a clasping set that includes arms with special fl at adhering cushions, onto which it concentrates sticky material fl owing from the papillae. The set includes one large central arm with fi ve large adhesive cushions carried on short stalks, and several short arms arranged in a semi-circle, with small adhesive cushions. A long trunk extends from the front of the mouth. This sea angel specialises in the sea butterfl y Creseis . The prey is grasped by the adhesive cushions, the trunk is inserted into the shell aperture and the radula, aided by the hooks, tears the victim’s columellar muscle to pieces; the sea angel then pulls out and swallows its prey. Pneumodermopsis canephora, also of the northern Atlantic and Mediterranean (size 1 cm) has a huge adhesive cushion on the central arm, and fi ve small cushions. It also has two lateral arms, each with an adhesive cushion carried on a thick stalk. This species’ locomotion is assisted by cilia arranged on three hoops around the ‘waist’ of the snail. Respiration is assisted by an elongate skin fl ap along the side of the body that increases the respiratory surface, somewhat like a gill. This angel feeds on the sea butterfl y Cavolina . Upon forming contact with the sea butterfl y’s trap-net, the sea angel stops swimming and remains motionless on the net. As the sea butterfl y hauls in its net, the angel is also gradually hauled in. Upon making contact, the angel immediately sticks its large adhesive cushion onto Cavolina ’s shell; it then inserts its long trunk through the aperture, tears away the shell muscle and eats its prey, eventually leaving only an empty shell. 228 9 Shell Degeneration: Sea Slugs and Relatives

The extreme specialisation of sea angels to a diet consisting of only a single group of sea butterfl ies has its advantages. When the diet is specifi c, the feeding process can become more effi cient, so as to gain maximum energy from the food as compared to the energy invested in the process. Sensory organs can develop high specialisation for identifying and locating the single prey species from among the many organisms surrounding it in the open sea. Morphological mechanisms for pulling this specifi c prey rather than another out of its shell can develop, improve and reach perfection, so as to overcome the very specifi c morphological shapes and sizes of a single type of prey. Little energy is lost within the digestive system over sorting out desired food and rejecting unwanted prey, since only the desired food is present. Accordingly, the digestive system may be simplifi ed and indeed, sea angels have no sorting region and no stomach. Digestion is effi cient and the food is well exploited: angels eat all fl esh off their prey and utilise 90 % of the carbon and almost 100 % of the nitrogen in their food. This extreme dietary specialisation also comes with several disadvantages. On an immediate time scale, there is severe competition within the population and aggres- sion rises to extreme levels. On the time-scale of a season, the sea angel must be present at the same time and place as an abundance of its single sea butterfl y species or genus; otherwise it will starve to death. This problem can be overcome if the sea angel can survive long periods without food; an individual of the genus Clione can survive up to 1 month without food in the lab. On a longer time scale, the life cycle of the sea angel is similar to that of its sea butterfl y prey: angel egg laying and hatching times overlap those of its butterfl y prey (which in turn overlap those of the plankton). In addition, both larvae and adults of prey and predator are swept and carried away through the sea by the same currents. Clione antarctica of Antarctica, defends itself from predators by synthesising a fi sh-deterring chemical compound, pteroenone. Local densities of this species may reach very high densities, of up to 300 animals per cubic meter. Sea angels are simultaneous hermaphrodites and copulate only when fully mature, having reached the stage in which both sex systems are fully developed (sea butterfl ies are consecutive hermaphrodites). The eggs are laid in clumps that fl oat in the water, and small veligers with a thimble-like shell and a two-lobed sail hatch within 3–4 days. Within 2 weeks the shell is cast off, the sail is absorbed and the body becomes elongated. The parapodia develop only at a later embryonic stage; until then the embryo swims by use of three hoops of cilia that surround its ‘waist’. In some species these hoops of cilia also remain in the adult.

9.6 Sacoglossa: Leaﬂ ets

We now leave the water column and return to the sea ﬂ oor. The Sacoglossa (Figs. 9.23 , 9.24 , 9.25 , 9.26 , 9.27 , 9.28, and 9.29) are an order of herbivorous sea slugs which feed on green algae. They are mostly small, only up to a few centimetres in length, usually green, sometimes resembling a green leaf. They are 9.6 Sacoglossa: Leaﬂ ets 229

Fig. 9.23 Leaﬂ et, Elysia decorata (2 cm), Red Sea

simultaneous hermaphrodites, and have a singular method of copulation. The primitive genera are equipped with a large shell, the more advanced genera have a much reduced shell that covers only the viscera, while the most advanced genera completely lack a shell and these are equipped with large parapodia, or may have large ﬁ nger-like lobes arising from the back. Leaﬂ ets are a small group of some 30 genera, of which Elysia (Fig. 9.23 ) is rather typical.

9.6.1 Feeding and Photosynthesising

Leafl ets puncture individual algal cells and suck up the cytoplasm, on which they feed. Although any plant cell may potentially be punctured and sucked up in this manner, suction feeding reaps its highest reward when the sacoglossan punctures large cells which are continuous. The puncture of just one very large algal cell is suffi cient to gain access to a wealth of food, as each such cell contains much cytoplasm, and many nuclei and chloroplasts. (Chloroplasts are green cellular organelles that enable plant cells to convert sunlight into energy, a process named photosynthesis). The feeding apparatus of the sacoglossan is well adapted to puncturing plant cells and sucking their sap. Only the central tooth has remained in each row of the radula, sharp at its point and along its margins, somewhat like a letter-opener (Fig. 9.24 ). Leafl ets have a special collection sac beneath their radula, into which the worn teeth are shed when replaced by new ones. This is in contrast to all other snails, in which worn teeth are shed into the cavity of the digestive system and eventually ejected from the body. This character, as yet of unknown biological signifi cance, has given the sacoglossans their scientifi c name, with ‘Sacus ’ meaning a sac and ‘glossus ’ meaning a tongue, in reference to a storage sac beneath the tongue-like radula. Upon piercing the cell, the sacoglossan attaches its lips to the wound, preventing contact between the algal cytoplasm and the sea water. Algal cytoplasm usually agglutinates upon contact with sea water, so by preventing this contact, the sacoglossan ensures a smoother fl ow of the cytoplasm directly into its mouth. This fl ow is assisted by two pharyngeal pouches behind the mouth, which actively suck at the algal sap. Although all contents of the algal cell are sucked up, most are discarded. The chloroplasts, however, are transferred into the snail’s digestive gland, that ramifi es 230 9 Shell Degeneration: Sea Slugs and Relatives

Fig. 9.24 Leaﬂ ets: the radula, a series of three teeth (Based on Thompson 1976 )

throughout the body and has ducts lined with digestive cells. These cells engulf the chloroplasts, enclose them in food vacuoles and digest only the old, non-functional (or dead) ones. The functional chloroplasts are not digested and remain intact inside the extensively branched digestive gland. As they are positioned just one cell layer beneath the transparent skin of their host, their green colour causes the leafl et to blend well into the green algal bed on which it feeds. What is far more remarkable, however, is that these chloroplasts continue both to capture available light energy and fuel CO2 fi xation to produce carbon compounds such as glucose, as they did when in the alga. Henceforth, these plant organelles will serve their new host, the sea slug. The transfer of such photosynthetic products from the chloroplasts into the tissues of the leafl et occurs rapidly: they are already present in the ducts of the digestive gland within 1 h from the moment they were formed, and within 2 h in the mucus gland of the foot. A leafl et has a branching system of veins that spread along the back from the parapodia and meet near the heart. These absorb bicarbonate for chloroplast activity and secrete surplus oxygen formed during photosynthesis. The chloroplasts function inside the leafl et for many months, but once outside the alga in which they were originally formed they cannot grow, cannot multiply and cannot form many of the molecules required for photosynthesis such as DNA, fats and enzymes, so their photosynthetic activity gradually declines. To keep up a high level of photosynthesis, the leafl et must replace old, degenerating chloroplasts with new ones. Degenerate chloroplasts are transferred into special intra-cellular vacuoles and digested. The vast majority of the Sacoglossa are primarily green, indicating the widespread nature of chloroplast-feeding in this group. Primitive leafl ets, still possessing a shell, feed on green algae, but tend to digest all chloroplasts they swallow immediately, both the functional and the non-functional ones. Some of the advanced leaf- lets, without a shell, tend to retain their chloroplasts for about a week; other advanced leafl ets retain them for more than one month. There seems to be a sequential pro- gression from short- to long-term use of chloroplasts which coincides with the gradual reduction of the shell, with different adaptations involved in each step. Initially, short-term retention of chloroplasts perhaps evolved from a defi ciency in plastid digestion, to yield additional energy via the release of fi xed carbon. The subsequent evolution of parapodia afforded the chloroplasts protection against high radiation, thereby prolonging plastid survival. Leafl et species containing chloroplasts often orientate towards the light, whereas avoidance of too high irradiance may be met by rolling up the parapodia to shade the chloroplasts. 9.6 Sacoglossa: Leafl ets 231

The chloroplasts in the leafl et-chloroplast relationship come from a broad spectrum of algae, including various groups of Chlorophyta (green algae, such as Codium, Caulerpa , Acetabularia, and Halimeda ) and Chromophyta (green- yellow algae, such as Vaucheria ). The adaptations necessary for long-term chloroplast survival may have arisen independently in leafl et species feeding on different algal hosts. Whatever its evolutionary origin, today the long-lived functionality of the chloroplasts enables leafl ets to survive prolonged periods of food scarcity. During such periods, carbon products formed by the chloroplasts may totally sus- tain the leafl et for several months. The record longevity of leafl ets feeding on nothing but maintained under the correct light wavelengths for photosynthesis is 10 months. While the chloroplasts may provide carbon products to their host during these long periods, this situation could rapidly lead to nitrogen starvation. Fortunately, when under light, the chloroplasts are active also in uptake and assimilation of dissolved nitrogen. The ability to assimilate dissolved nitrogen benefi ts a leafl et when food is scarce; indeed any de novo protein synthesis occurring after 8–9 months of starvation would be unlikely without an external supply of nitrogen. Chloroplast nitrogen assimilation may thus constitute an additional contribution to the unique and long-lived functionality of this symbiosis. The ability of sea opisthobranchs to maintain active cell organelles of plants for their own benefi t is a unique phenomenon in the animal kingdom. Symbiotic associations between organisms are rather common, and the association is almost always between two intact organisms, each retaining its complete cellular genetic makeup. The sacoglossan–chloroplast symbiosis is unique because one of the symbiotic partners is only an organelle sustained inside the cells of the other, which is a complete organism. With the retention of these organelles, the host sea slug acquires a completely new metabolic capability involving the use of sunlight. Sacoglossans are thus solar-powered sea snails broadly resembling, from this aspect, the leaf of a plant. Being mobile and capable of moving, some semi-popular papers appropri- ately term them ‘crawling leaves’. Chloroplasts are not inherited: each newly metamorphosed sacoglossan must acquire them afresh. Young leafl ets feed upon algae immediately upon landing from the plankton, but cannot maintain chloroplasts at this stage, perhaps because their digestive gland has not yet matured to some required level. Upon metamorphosis to the adult stage the digestive gland is still a simple two-lobed mass, and any chloroplasts transferred into it at this developmental stage are rapidly digested. Only approximately 1 week later does the gland begin ramifying into a complex system of many lobes, beneath the surface of the parapodia; and only with the fi nal complete maturation of the cells within these newly developed lobes does the maintenance of live chloroplasts become possible, though the manner of this maintenance is not clear. The fact that live chloroplasts remain intact in the cells of the leafl et’s digestive gland suggests that certain digestive enzymes might be suppressed or not activated. Perhaps the continuous leakage of metabolites from live chloroplasts sup- presses activation of these enzymes. When a chloroplast grows old or dies and stops functioning, such leakage ceases, and the now-activated enzymes digest it. 232 9 Shell Degeneration: Sea Slugs and Relatives

When in their original alga, chloroplasts contain only enough DNA to encode approximately 10 % of the proteins needed to keep them functional. The other necessary genes are within the nuclear DNA of the alga. How do the chloroplasts continue functioning inside the leafl et cells when lacking all these proteins? Had the sea slug swallowed and used the algal chloroplast alone, it would not have all the genes needed for photosynthesis. Recent studies suggest that when eating and sucking up the sap of the alga, leafl ets may perhaps also be taking up chloroplast-maintaining genes, which are then incorporated into the leafl et’s own DNA; this allows it to produce all necessary proteins for the stolen chloroplasts to continue working. The survival and growth of a leafl et partly depends upon its many photosynthetic chloroplasts, the survival of which, in turn, depends upon light. The leafl et is attracted to light, and spreads out its parapodia to expose its chloroplasts or enrols them according to surrounding light intensity. The parapodia are closed in high light intensities or in damaging light wave-lengths to protect the chloroplasts from radiation damages. The leafl et also has a special enzyme that repairs DNA damage caused by strong radiation or ultra-violet light.

9.6.2 Reproduction

Like most sea slugs, leaﬂ ets are simultaneous hermaphrodites that must mate to reproduce, both partners mutually donating and receiving sperm. Each individual has two genital pores, one for the male system (that lets the penis out to eject sperm) and the other for the female system (that serves only to release the string of fertilised eggs). During copulation leaﬂ ets practice hypodermic insemination: each donating individual thrusts the penis (Fig. 9.25 ) through the recipient’s skin and simply injects sperm into its body cavity. Some species inject sperm through the skin directly into the receptive organs; others may inject their sperm anywhere into the partner’s blood spaces, from where they eventually reach the genitalia. How the

Fig. 9.25 Leaﬂ ets: a penis (Based on Thompson 1976 ) 9.6 Sacoglossa: Leaﬂ ets 233

Fig. 9.26 Alderia modesta (1 cm), Northern Atlantic and Northern Paciﬁ c

sperm travel from these spaces to the ovules and fertilise them is as yet unknown. Many species have a special penis armature to assist in hypodermic insemination, in the form of a sharp style, formed by the sperm duct protruding beyond the penis as a hypodermic needle, its tip hardened by chitin. Widespread though it is, hypodermic insemination is not unique to leafl ets, and has evolved independently also in a number of other simultaneous hermaphrodites, such as nudibranch sea slugs (Sect. 9.8 ), fl atworms and leeches. A minority of leafl et species mate either by hypodermic injections or by standard insemination into the female aperture, as do most sea slugs. Alderia modesta (Fig. 9.26 ), which feeds on the alga Vaucheria in the north Atlantic and has also been recorded from the western Pacifi c, has a penis equipped with a sharp style to pierce the skin and carry out hypodermic insemination. Its genital system, particularly the gonad, occupies most of the internal body space. Alderia has poor vision and probably uses both chemical and tactile cues to fi nd potential mates. When two individuals make contact they typically push against each other and move their oral tentacles over the other’s body, perhaps to assess the size. Only then does each extend its penis, inject its style and transfer sperm. The entire mating process lasts 5 min. Hypodermic injections and sperm transfer across all sections of the body wall successfully fertilise the ovules and there is no tendency for style injections to be in any particular section of the body. Mutual injections are more common than one-sided injections, especially in larger partners. Sperm are produced and transferred at a remarkably young age and therefore small size. In experiments, 50 % of Alderia modesta individuals exposed to same- age individuals for only the fi rst 2 days after metamorphosis went on to produce fertilised eggs when kept in isolation, indicating that mating in the roles of both sperm donor and sperm recipient, sperm transfer and sperm storage occur in juveniles of merely 0.5 mm. However, though these very young small leafl ets can already store sperm received from a mate, the onset of ovule production occurs only approximately 10 days after metamorphosis, only at a larger size of approximately 1.2 mm, thereby demonstrating delayed complete female function. Field- 234 9 Shell Degeneration: Sea Slugs and Relatives

Fig. 9.27 Elysia timida (1 cm), Mediterranean

collected Alderia seem to have enough stored sperm to fertilise all ovules produced within the fi rst few days in isolation, but the fertilised proportion drops to below 50 % after 2 weeks in isolation, refl ecting a sperm depletion rate of approximately 5 % per day. Elysia timida (Fig. 9.27 ) lives in the Mediterranean, where it feeds on the highly seasonal alga Acetabularia . Its penis lacks any form of armature, having neither style or hooks, and its mating behaviour is very unusual: it performs a unique combination of a long series of interrupted hypodermic injections into the back of its partner, followed by insemination directly into the female genital aperture. Two E. timida individuals initiate mating by meeting head-to-head, and each immediately erects its penis. Next, each partner stretches its penis towards the front third of the back of the partner, which it attempts to stab. It seems that in many of these stabbings the penis injects prostate secretions into the partner. After each stab, the penis is withdrawn and the individuals start a synchronous, stereotypic circling movement in a counter-clockwise direction. Resuming head-to-head position, a new hypodermic stabbing attempt begins. Such stabbing attempts may alternate with circling movements some twelve times during a single mating sequence. Hypodermic stabbing might serve as part of a ritualised courtship aimed at synchrony and reciprocity. The ‘cooperative’ and ritualised behaviour lacks signs of avoidance and might suggest that the stabbed individual gains some benefi t from being injected by prostate secretions, or is assured of the partner’s virility. Eventually sperm is transferred into the E. timida female genital aperture. The individuals again take up a head-to-head position, but this time they touch the partner’s female aperture with their penises several times, as though ‘waiting’ for the partner to respond. Final insemination is almost always mutual and approximately simultaneous, with each individual inserting its penis into the partner’s female 9.6 Sacoglossa: Leafl ets 235

aperture and transferring sperm. The individuals then withdraw, separate, and crawl off in different directions. A complete mating sequence lasts nearly 40 min. The sexual behaviour of Elysia timida, combining repeated hypodermic injections into the back with standard sperm transfer into a female genital aperture, is very synchronised and balanced between partners. Individual mating decisions depend on what the partner does, hence the long duration of the whole mating sequence. Shifting from Elysia timida’s mating behaviour to its production of progeny, each individual subsequently deposits eggs in a viscous mass of albumen. The developmental strategy of E. timida changes during the year. Winter provides an abundance of food and larval development to juvenile adults is direct, but in spring and summer, when food is scarce, veligers hatch and swim into the plankton, where they feed on unicellular algae for approximately 2 weeks before metamorphosing.

9.6.3 Defence

Not nearly enough is known about leafl et defence mechanisms. Oxynoe panamensis of mangrove swamps in the eastern Pacifi c (Fig. 9.28 ) is a primitive leafl et; its visceral hump is enclosed in a lightly calcifi ed, globular shell partly covered by parapodia, and it has a long, muscular tail, like other species in its genus. Within a few seconds of being molested or irritated, it begins to secrete a milky mucus from its skin; initially it is tasteless, but within a few seconds the mucus tastes caustic and astringent to the tongue. This secretion is poisonous to fi sh. One-quarter of the discharge from a single slug diluted and mixed in 100 ml of seawater can kill a 5-g herring fi sh ( Harengula , family Clupeidae) within 15 min; one-fi ftieth of a discharge mixed in 2 ml of pond water can kill a small guppy (Lebistes reticulatus, family Poecilidae) within 30 min. The mucus from Oxynoe seems to contain a neu- rotoxin because the symptoms exhibited by these fi shes include convulsive movements of the body, irregular activity of the gill opercula, paroxysms, and a few seconds of tremor leading to death. When persistently irritated, Oxynoe may respond

Fig. 9.28 Oxynoe panamensis (3 cm), tropical West Atlantic 236 9 Shell Degeneration: Sea Slugs and Relatives

Fig. 9.29 Lobiger viridis (2 cm), tropical Paciﬁ c

by strong twisting of its tail, which is eventually detached at a ﬁ xed point behind the visceral hump. This self-detachment of the tail is mediated by a ring muscle in that region, and the detached tail continues to twitch sporadically for several minutes, presumably to distract a predator and draw its attention away from the animal itself. Similar self-detachment of the tail in response to molestation occurs also in Lobiger (Fig. 9.29 ), another primitive leaﬂ et.

9.7 Pleurobrancha: Side-Gills

Side-gills (Pleurobranchidea, Fig. 9.30 ) are an order with members bearing a large plume-like gill between the mantle and the foot on the right side of the body, giving rise to their scientifi c name, ‘Pleuro ’ – side, ‘branchia ’ – gill. The head bears rolled rhinophores, often joined at their bases, and an oral veil with rolled oral tentacles. The shell, often reduced to a thin internal plate sunk into the body, is absent in some groups. Side-gills are a small group of about ten genera. Side-gills dwell on the sea fl oor where they are predators, mainly of sponges and tunicates, occasionally of corals. They secrete concentrated sulphuric acid (pH = 1, more or less) for defence in moments of stress. Berthellina secretes strong acid from all parts of the skin during times of danger, even from the shaft of the gill. Layers of skin deeper than the acid cells often contain calcareous needles coming from the sponges upon which these sea snails feed. Thus, in addition to chemical defence, side-gills also have secondary mechanical defences. As a further mechanical defence Berthella martensi of the tropical Indo-Pacifi c can autotomise sections of its mantle, along pre-determined lines. Tylodina and Umbraculum were once placed together with the side-gills in a group named Notaspida; however, recent studies suggest that these two genera, characterised by their large foot and reduced external umbrella-like shell covering only the viscera, but which also feed on sponges, are only distantly related to the Pleurobranchidea. On the other hand, side-gills are closely related to the nudibranchs, the largest group among the sea slugs. In fact, they are so close that they have recently been placed together in a single large group, the Nudipleura. 9.8 Nudibranchia: Nudibranchs 237

Fig. 9.30 Side-gill, Berthellina citrina (7 cm), Indo-Paciﬁ c and Red Sea

9.8 Nudibranchia: Nudibranchs

The Nudibranchia, with 280 genera, is the largest of the sea slug orders. The scientifi c name of the group (nudi – naked; branchia – gills) refers to the exposed gills of the larger group of nudibranchs, the Anthobranchia. Adult nudibranchs have no remnant of the shell nor of the operculum, which are shed at metamorphosis. Neither is there any remnant of a mantle cavity, and the body is elongated, bilaterally symmetrical and fl exible. Rhinophores stand out on top of the head, often as wrinkled, lamellate or branched structures that are usually retractable into sometimes quite elaborate sheaths. Most nudibranchs dwell on the sea fl oor, where they are grazing predators, but some live in the water column. The Order Nudibranchia is divided into three major groups, the Anthobranchia (dorids) and Aeolidina (eolids) and the Dendronotina (denronotoids).

9.8.1 Anthobranchia: Dorids

Anthobranchia, also named Euctenidiacea, are sea slugs which almost always carry a bouquet of secondary gills around the anus on the back of their body to assist in respiration. These gills are large, often retractable and sometimes even capable of retreating into special gill pouches. A few Anthobranchia are exceptional in that they do not have the secondary gill bouquet ( Phyllidia and close genera). A large group, they include 150 genera (Figs. 9.31 , 9.32 , 9.33 , 9.34 , 9.35 , 9.36 , and 9.37 ). The spanish dancer Hexabranchus sanguineus (Fig. 9.31) of the Indo-Paciﬁ c is perhaps the most impressive representative of the group. This sea slug is capable of swimming by moving its whole body in rhythmic motion (hence its common name), its spontaneous swim bouts involving up-down bending of the body in one rhythm, combined dorso-ventral undulations of the lateral margins of the mantle in another. 238 9 Shell Degeneration: Sea Slugs and Relatives

Fig. 9.31 Dorid, the spanish dancer, Hexabranchus sanguineus (22 cm), Indo-Paciﬁ c and Red Sea

Fig. 9.32 Dorid, Chromodoris africana (7 cm), Red Sea and western Indian Ocean

Fig. 9.33 Dorid, Nembrotha megalocera (7 cm), Red Sea (Based on Yonow 2008 ) 9.8 Nudibranchia: Nudibranchs 239

Fig. 9.34 Dorid, Chromodoris britoi (7 cm), Mediterranean and north- eastern Atlantic

Fig. 9.35 Dorid, Phyllidia multituberculata (7 cm), western Indian Ocean and Red Sea

Fig. 9.36 Dorid, Ceratosoma trilobatum (20 cm), Indo-Paciﬁ c

Fig. 9.37 Dorid, Hypselodoris infucata (7 cm), western Indian Ocean, Red Sea and Mediterranean 240 9 Shell Degeneration: Sea Slugs and Relatives

Dorids usually feed on sponges, but also on bryozoans, ascidians and barnacles, and they all have a chitinous radula to aid in feeding. Some have a muscular elongation of the mouth complex to assist in suction feeding, and these species do not have a radula, such as Phyllidia and its close relatives (Fig. 9.35 ). Some species have a highly specifi c diet. Thus, Archidoris pseudoargus of the western Atlantic and the Mediterranean is completely dependent on a single sponge species Halichondria panacea; the Mediterranean dorid Peltodoris atromaculata is closely dependent on the sponge Petrosia dura, and Onchidoris bilamellata of the northern Atlantic feeds mainly on the acorn barnacles Elminius and Balanus . Most species, however, do not have a such a rigidly specifi c diet and take a variety of prey. Dorids defend themselves against predators by applying a strategy of chemical defences: when feeding on sponges they take in poisonous substances from the sponge and store them in cells of their skin. The poisons are secreted if the slug is attacked, and they are potent to such an extent that they may kill crabs and fi shes within minutes. Other dorids produce chemical substances autonomously. Thus, Discodoris planata of the northern Atlantic forms and stores sulphuric acid in special glands on its back. This sea slug spends most of its life under sponge covered rocks, and if nosed out by an inquisitive fi sh expels large quantities of the acid to deter the fi sh (all fi shes have a common abhorrence of anything tasting acidic). Some dorids also have a mechanical defence: their skin is often embedded with calcareous dagger-shaped spikes; these are in fact the sponge spicules, which it ingests and then rearranges for its own defence. They may be aggregated into prickly papillae on the back of the mantle or simply aligned to fi t within the skin of the mantle. Sometimes, as in the Pacifi c species Laila cockerelli, these papillae may take the form of elongated fi nger-like processes with brilliantly coloured tips. Phyllidia and its close relatives form a compact group, the Phyllidiidae. The vast majority of phyllidiid species (they possess defensive chemical compounds seques- tered from their sponge food) are brightly coloured with a contrasting pattern of orange, black, and white. These species, in the genera Phyllidia , Fryeria , Phyllidopsis and Reticulida , are highly conspicuous in exposed situations and easily visible in their open natural surroundings during daylight where they can easily be experi- enced by potential predators. They only uncommonly occur in protected, cryptic habitats such as caves or crevices, under ledges, on the underside of rocks or coral rubble. Most phyllidiid species possessing contrasting colouration and chemical defence are thus conspicuous behaviourally. Dorids are simultaneous hermaphrodites and normally copulate reciprocally, with the penis of one inserted into the vaginal opening of the other. Palio differs from other dorids as its vagina is no more than a small blind pocket, with no trace of any connection continuing internally (Fig. 9.38). Lacking a vaginal duct, Palio copulates differently from most dorids. Copulation is usually mutual and lasts approximately 5 min, but involves stabbing of the body wall with an eversible cirrus of the penis equipped with barbs. During copulation, the cirrus turns out like the inverted fi nger of a glove, its barbs roll over the lip, and they tear a hole in the body wall of the partner. The barbs then anchor in the skin as the cirrus continues to unfold; they hold the penis in place even if the partner starts moving away. Usually 9.8 Nudibranchia: Nudibranchs 241

Fig. 9.38 Palio genitalia, as compared with Polycera . Dorsal view; only major organs are labeled; the gonad is inside the visceral mass (Based on Rivest 1984 )

the cirrus penetrates the partner’s body wall in the posterior right fl ank of the body, and, as the gonad lies a short distance beneath the body wall, the piercing cirrus is likely to penetrate the gonad. Peristaltic action of the muscular sperm duct during copulation moves sperm through the cirrus, and masses of sperm are deposited within the body wall and blood spaces of the partner. The cirrus often stabs several times at new locations during a copulation bout. To inject sperm right into a partner’s gonad, the cirrus must penetrate the body wall, traverse part of the blood spaces, penetrate the tissue covering the visceral mass and puncture a lobe of the gonad. This is a minimal distance of 0.1 mm; the length of the cirrus is 1 mm (in an 8 mm-long slug). If the male organ fails to reach the gonad itself and injects sperm into the body wall or the blood spaces instead, the sperm are engulfed and destroyed. If the cirrus succeeds in penetrating the gonad, the injected sperm travels down the genitalia and eventually is stored in the sperm receptacle, ready for fertilisation. Chromodoris reticulata of the western Pacifi c (Philippines, Japan) has a peculiar mating behaviour: After fi nishing copulation each of the partners crawls away with its penis still extruded from its body and, some 20 min later, the external, 1 cm long portion of this penis breaks off. Within a day this portion regrows from the rest of the penis (which remains coiled up within the body), so the individual can copulate 242 9 Shell Degeneration: Sea Slugs and Relatives again within 24 h, using a new penis tip. No other animal is known to repeatedly copulate using such “disposable penises” as one-shot organs.

9.8.2 Aeolidina: Aeolids

Aeolidina are long, narrow-bodied nudibranchs (Figs. 9.39 and 9.40 ) which have prominent rhinophores protruding from the front of the head. In addition, a pair of conspicuous tentacles stands out sideways on either side of the mouth. Many lobes rise out of the back and stand in an erect position (Fig. 9.39, these are named ‘cerata’). Each ceras contains a tubular branch of the digestive gland and is usually

Fig. 9.39 Aeolid, a generalised ﬁ gure

Fig. 9.40 Aeolid, Caloria indica (3 cm), Indo-Pacifi c, Mediterranean 9.8 Nudibranchia: Nudibranchs 243 movable, to some extent. Aeolids lack gills: the cerata have thin skin, and through it a continuous rapid exchange of oxygen and carbon dioxide occurs between the cerata and the surrounding sea water. Oxygen is transferred directly to the blood system within each lobe and from there to the rest of the body. In this manner, they can exist without gills. Near the tip of each lobe, the end of each tubular digestive branch usually consists of a small sac, the ‘stinging sac’ (‘ cnidosac’ in scientifi c terminology). The radula almost always has only one or few teeth per row. A pair of well-developed upper jaws, consisting of chitin, assists in tearing off parts of the prey. The group consists of some 125 genera. Aeolids prey mainly on members of the phylum Cnidaria, including sea- anemones, corals, medusas and their many relatives. The aeolids must of course defend themselves from the prey’s nematocysts, or risk their own injury or death. Nematocysts from non-prey cnidarians can kill a nudibranch, and even the prey species can be dangerous if the individual is large enough. Defences that might protect an aeolid from nematocysts include behaviours that limit its contact with the prey, morphological adaptations such as ellipsoid vacuolate cells of the epithelium or a cuticle that lines the mouth region of the nudibranch, and copious mucous secretions. When an aeolid fi rst makes contact with a sea anemone, the anemone usually responds by a mild shot of its stinging cells, perhaps even by clasping the nudibranch. The substance in the anemone’s stinging cells contains the cell dissolving enzyme phospholipase, which dissolves the outer skin cells. Within a few minutes, however, the anemone’s clasp weakens and the aeolid is set free. It then crawls freely over the body of the anemone, biting into it without the latter responding by more stinging cell release. The change in the anemone’s defensive activity may seem strange as it is not paralysed by the predator and there is no change in its fi ring ability. Furthermore, it sometimes even attempts to crawl away, self-amputating the tentacle that the aeolid is biting into. The solution lies with the attacking sea slug: skin cells of some species are packed with vacuoles containing tiny stick-like and disc-like structures, each approximately 5 thousandths of a millimetre long. The aeolid skin cells, disintegrating from the anemone’s sting substance, release their vacuoles into the sea, and these burst open and the sticks and discs disperse into the sea water. These, in turn, curb and break the anemone’s attack at some distance from the aeolid, perhaps by absorbing the venomous substances. The aeolid’s skin is renewed and healed within 1 day or two after the attack. The situation may, however, be more complex. Cratena peregrina of the Mediterranean regularly crawls and feeds on the polyps of the hydroid Eudendrium racemosum (Cnidaria: Hydrozoa), which lives in large colonies. It approaches a polyp from its proximal end, separates it from the stalk and sucks it in; in a feeding cycle of 1 h Cratena can eat 25 polyps, one about every 2–3 min. When doing so C. peregrina is exposed to fi ring stinging cells, and the polyps of E. racemosum possess these in two size-classes. Small stinging cells occur on the thread-like tentacles of all polyps and serve for capturing prey, such as small planktonic organisms. Large stinging cells, nearly twice the size of the small ones, occur on only one of fi ve 244 9 Shell Degeneration: Sea Slugs and Relatives

polyps of a colony, which also possesses a very large appendage. Originating at the base of the polyp this appendage is four times thicker than a tentacle and may be fi ve times longer than the entire polyp; it is termed the ‘cnidophore’, and its large stinging cells are three times more numerous (per area) than those of the tentacles. They also form rings at the base of some of the polyps and function as defensive organs. When the hydroid discharges both stinging cells in response to Cratena predation, the skin of the slug’s body is not damaged by the small stinging cells because its skin contains vacuoles with stick- and disc-like structures. In contrast, however, the contact of the slug’s skin with the cnidophore is very damaging to the aeolid. Masses of the large nematocysts of the cnidophores discharge, penetrate the snail’s skin and within seconds they cause dissolution of the epidermis down to the basal lamina. The predominant event is the lysis of extra- and intra-cellular membranes, probably due to the action of the venoms, of which phospholipase A2 is one of the major components. These large stinging cells do not damage the alimentary canal of Cratena , which is lined with a thick protective cuticle. Also a sea slug’s mucus may serve as a protective barrier against nematocysts. A few sea slugs are highly specialised and feed exclusively on one prey species, but most aeolid species can feed on several species. Monophagous species might have defensive mucus that works well against the nematocysts of a single prey species, but the more generalist feeders need an effective defence against a number of cnidarian species, with many different nematocyst types. Such sea slugs would require defensive mucus that changes properties depending upon which prey is being consumed. Aeolidia papillosa of New England feeds almost exclusively on sea anemones. In its sub-tidal habitat it is frequently found among populations of the sea anemone Metridium senile, but is also found associated with a variety of other sea anemone species. Mucus from Aeolidia papillosa specifi cally inhibits the discharge of nematocysts from this sea anemone’s tentacles. This inhibition of nematocyst discharge is limited to the anemone species on which the sea-slug has been feeding. Moreover, the mucus changes to inhibit the nematocyst discharge of a different sea anemone species, if the sea slug begins to feed on that new species. Laboratory experiments reveal that if Aeolidia papillosa is fed two different species of sea anemone, its mucus inhibits nematocyst discharge from both prey species. Thus, mucus from sea slugs that had been fed the sea anemone Metridium senile greatly inhibits nematocyst discharge from M. senile, but not from Urticina felina or Aulactinia stella. Likewise, mucus from sea slugs that had been fed Urticina felina inhibits nematocyst discharge from U. felina, but not from the other species. Within 10 days after the prey of Aeolidia papillosa is changed from U. felina to M. senile, the mucus of Aeolidia papillosa no longer inhibits nematocyst discharge from U. felina, but does inhibit nematocyst discharge from M. senile . After 2 weeks of being fed, the mucus of the sea slug inhibits nematocyst discharge from both. Overall, A. papillosa mucus reduces nematocyst discharge from all prey anemones by 60 % below control levels. Usually aeolids predate sessile cnidarians but at least one species, Cuthona nana of the north Atlantic, preys on a highly mobile cnidarian, Hydractina polyclina , the sea anemone which lives on and is moved by the hermit crab Pagurus . Young individuals dwell upon the hermit crab anemone and feed on it for many days, descend- 9.8 Nudibranchia: Nudibranchs 245 ing from it only to copulate and lay eggs upon reaching maturity. These eggs are rich in yolk and, accordingly, the embryos inside develop and hatch directly into small crawling sea slugs. This mode of reproduction without a free-swimming veliger, direct development, occurs throughout the Opisthobranchia. The long arms of the hermit crab anemone trail along and sweep the sea fl oor while the hermit crab beneath it runs about, so the nudibranchs on the sea bed are given an opportunity to climb aboard the anemone, renew their clinging and resume their predating. Some aeolids feed upon sea anemones containing symbiotic single-celled algae that photosynthesis light, called zooxanthellae. For example, Aeolida papillosa feeds on the anemone Anthopleura elegentissima in the north Atlantic. The aeolid swallows these unicellular photosynthesising algae when sucking up the cell sap of the anemone, and transfers them into its cerata. Here the cells continue photosynthesis, but the compounds produced are now available to their new host, like in the Sacoglossa (Sect. 9.6 ). Although the sea slug benefi ts from the continued activity of algal cells in its body, it does not tend to them; without maintenance, some of the zooxanthellae die within a short time and the aeolid digests them. The supply is replenished by renewed feeding. Another species, Phyllodesmium hyalinum in the Red Sea, feeds on Xenia and Heteroxenia , a group of soft corals which compliment nourishment from symbiotic algae. Upon predating these corals, it extracts and takes these photosynthesising symbiotic algae from the coral, and makes use of the compounds they produce. The cerata of certain Phyllodesmium species have evolved into large wide plates with a large surface, and these function as effective light receivers. Branches of the ramifying digestive system are present in all body parts exposed to light, including the foot and tentacles, and these enable maximal exposure of these algae to light. As they die within a brief time of having been eaten, Phyllodesmium must swallow live algae frequently. Fortunately for this aeolid, each arm in Xenia contains up to 13,000 symbiotic algae, more than enough to last one individual Phyllodesmium all its life. In addition to the use made by Phyllodesmium of the compounds produced by the live algae, it also digests the dying and dead algal cells (as does Aeolida papillosa ). The genus Phyllodesmium differs from most aeolids in that it lacks sting sacs; for defence, it relies instead on camoufl age, with the cerata of many species resembling the tentacles of their alcyonarian prey. Two different functional photosynthetic systems are thus found in sea slugs. One, involving the incorporation and maintenance of functional chloroplasts after intake of algal tissue is known only from the Sacoglossa (Sect. 9.6 ). The second system, involving the incorporation of zooxanthellae and the use of their metabolites, is known mainly from the aeolid nudibranchs. Some aeolid genera have, during evolution, turned to living out their life in the water column, where they seek cnidarians that also fl oat near the sea surface. The fl oating aeolid Glaucus (Fig. 9.41 ) spends its entire life in the upper layers of the open sea (somewhat like the violet shells, Sect. 8.5 ) where it feeds on such plankton- dwelling cnidarians as Velella, Porpita and Physalia. It fl oats by swallowing an air bubble from the surface of the water, keeping it within its digestive system and preventing its escape by means of strongly contracting ring muscles. Glaucus fl oats 246 9 Shell Degeneration: Sea Slugs and Relatives

Fig. 9.41 Aeolid, Glaucus atlanticus (6 cm), all oceans

on its back, the blue and silver colours of its body offering it counter-shading camoufl age; since its posture is upside down, the upper-positioned sole is blue and the lower-positioned back is silver. The scientifi c name of this genus refers to the sea idol Glaucus in Greek mythology: one day a fi sherman discovered a magic plant which grew on a particular shore that would bring his fi sh spoils back to life, as though they were immortal. When pouring his fi sh catch on the ground, upon contact with this plant his fi sh would begin wriggling and turning from side to side; they would then glide across the ground and eventually make off, back to the sea. Upon tasting the plant himself he too became immortal, but he also grew sea-blue fi ns instead of arms and a tail instead of legs; he was then doomed to live forever in the sea. When feeding on Physalia (the Portuguese man o’ war) Glaucus retains only the largest (and probably most virulent) stinging cells of that prey for its defence; consequently Glaucus are somewhat dangerous for humans to handle without protection, and have caused painful stings to bathers in Australia. Not all aeolids feed on cnidarians: some are egg-consumers. Favorinus branchialis of the eastern Atlantic and Mediterranean takes the eggs of other Opisthobranchia, such as sea hares and nudibranchs, devouring up to 20 eggs per minute; however, juveniles of this species eat hydroids such as Obelia . Another aeolid, Calma glaucoides with a similar geographical range, feeds on the eggs of fi shes and cephalopods. The anal opening is closed off after metamorphosis in this species, because only little solid waste remains after the digestion of such yolky food. Egg-feeding aeolids have a very pale colour, and pass unnoticed among cream-coloured or white eggs. The defence mechanism of most aeolids is based on the secondary use of stinging cells, ‘nematocytes’ swallowed when eating the cnidarians on which it feeds (Figs. 9.42 , 9.43 and 9.44 ). These cells are unique to the phylum Cnidaria, and contain an internal capsule fi lled with strong venom. They function by killing tiny prey; the amounts of venom are so small that they are fatal to Man only in large quantities, on rare occasions. Upon reaching the body of an aeolid that has eaten a 9.8 Nudibranchia: Nudibranchs 247

Fig. 9.42 A stinging cell

Fig. 9.43 Stages in fi ring of a stinging cell cnidarian a secondary use of these capsules is ensured. Both cells containing mature (‘ripe’) and non-mature venom capsules reach the aeolid’s stomach. Those capsules that were ripe while still in the anemone’s body are activated (‘fi red’) and digested together with other cells and tissues of the prey; those capsules that were not yet ripe and incapable of being fi red are fi rst transferred to the tubular branch of the digestive gland that extends into each lobe (‘ceras’). They are then transferred through a narrow ciliated tube at the end of the upper part of that branch and into the storage sac above it, the sting sac (‘cnidosac’, Fig. 9.44 ). Sting sacs are muscle-bounded 248 9 Shell Degeneration: Sea Slugs and Relatives

Fig. 9.44 Aeolids; left : a single lobe (ceras) with a branch of the digestive system and a sting sac (cnidosac); right : transect through the tip of the lobe (Based on Thompson 1976 ) repositories in the tips of dorsal appendages, the cerata, which are fi lled with latent (un-discharged) stinging cells, derived from the cnidarian prey. In aeolids a single sting sac forms the tip of each lobe. During transfer the capsules are engulfed by special large engulfi ng cells (‘cnidophages’) of the digestive system. A single cnidosac will eventually contain some 3,000 stinging cells. The arrangement of the stinging cells inside the engulfi ng cells varies between species, and may be aligned in parallel columns or in circles. Here they ripen within special intracellular vacuoles, thanks to nourishment in the form of ATP supplied by the engulfi ng cells, and here they are stored for long periods. New engulfi ng cells beneath them push these loaded and packed cells upwards along the walls of the sac. The apex of the sac does not contain muscles and is sealed with thin cells; the basis of the sac, connected to the ciliated tubule of the digestive gland, is surrounded by a circular muscle that contracts when the sac is shot out and prevents stinging cells in the sac from slipping back into lower regions of the digestive gland. Sting sacs containing stinging cells are stored for lengthy periods of time. The sting sacs are defence organs, directed especially against predatory fi sh. Upon being attacked, an aeolid fi rst erects its lobes (cerata) and may even muster them together and aim them towards the attacker, thereby drawing the attacker’s attention to the conspicuously coloured tips (Fig. 9.40 ), and away from the vital organs, such as rhinophores. Next it contracts special longitudinal muscles, tearing the apices of the cnidosacs open. Clouds of engulfi ng cells tumble out of the sac into the sea, and the 9.8 Nudibranchia: Nudibranchs 249 stinging cells within them are released and discharged. After some time, the tissue wounds at the cnidosac apex heal and a new acquisition of stinging cells begins. If damaged, the entire ceras may be rapidly regenerated. The ability of opisthobranch groups, such as leafl ets and aeolids, to take active organelles from another animal phylum and use them for its own benefi t, is a unique phenomenon in the animal kingdom. As in most sea slugs, copulation with mutual penis penetration into the female pore and mutual transfer of sperm is the rule. However, Aeolidiella glauca of the north-eastern Atlantic transfers sperm by attaching an external spermatophore onto the partner’s back. The very large unarmed penis bears a series of three to four hook-shaped lobes. Courtship involves moving in circles followed by resting in a head-to-head position, reciprocally touching each other with the tentacles. Eventually the sea slugs glide into a position where the genitalia are in contact. Each slug draws out its huge penis, strokes its partner’s back with the penis and then deposits a spermatophore onto the partner’s back. In most mating events the spermatophores are exchanged mutually. Shortly after transfer onto the partner’s back the spermatophore cover dissolves and sperm gather on the recipient’s skin. A few sperm may penetrate the skin, occasionally causing considerable damage, but most sperm migrate along the body surface towards and into the genital pore, a journey lasting 4–5 h. As ova production is very high and sperm from a single mating may not suffi ce to fertilise all ova, they readily mate with several partners. Interestingly, Aeolidiella avoids mating with an individual already carrying a spermatophore; avoiding a recently mated partner perhaps reduces a sperm donor’s risk of being subjected to sperm competition.

9.8.3 Dendronotina: Dendronotoids

Dendronotina is a small order of nudibranchs in which secondary gills are aligned in a paired series on their back. These gills may be large and bushy, or reduced to small fi laments protected by fl aps, or completely reduced to small fl aps. There is always a frontal veil, which may be divided into sensory fi ngers. Furthermore, they possess a mid-lateral anal papilla and distinct, often elaborate, sheaths in which to retract the rhinophores upon alarm. The Dendronotina and Aeolidina are closely related and the two are sometimes placed in a single group, the Cladobranchia. In general, dendronotoid species feed on cnidarian polyps. Most of them lack cnidosacs, and special digestive cells in the branches of the digestive gland digest the prey’s stinging cells; this has been well-studied in Doto acuta of the Mediterranean. Two other dendronotoids of the Mediterranean, Hancockia uncinata and H. schoeferti, also feeds on cnidarian polyps, but they do have cnidosacs. As in aeolids, these are terminal digestive gland repositories with a muscular sphincter, containing stinging cells. Each lobe has many small sting sacs (cnidosacs), and in that Hancockia differs from aeolids. It further differs in that most of the stinging cells eaten are engulfed intact by large engulfi ng cells (cnidophages) in the digestive gland, and are then transported via narrow connecting channels to the sting sacs. 250 9 Shell Degeneration: Sea Slugs and Relatives

Also, each small stinging sac contains only two-three stinging cells. The limited storage capacity of the small sting sacs and the pressure of additional engulfi ng cells with additional incoming food necessitate a frequent emptying of the sting sacs; consequently, their storage times are short. Sting sacs in Hancockia thus function in the elimination of stinging cells, and when these accumulate in the distal-most digestive cells, the slug expels them into the surrounding sea. From both structural and functional points of view, Doto acuta represents a basic condition in which a limited number of stinging cells are digested by each cell of the digestive gland. This basic condition seems to be exceeded when, as in Hancockia and aeolids, stinging cells of the prey accumulate in the digestive cells in quantities so large that the cells are unable to digest them; this may be due to a switch to a prey with more stinging cells, or to increased food consumption. Removal of surplus stinging cells from the digestive system may have been the original function of sting sacs. However, from the very beginning Hancockia’s masses of stinging cells, in the sting sacs at the tips of its cerata, are also likely to have offered a defensive advantage. Firing stinging cells into the mouth of a fi sh biting into cerata of Hancockia would be deleterious to the fi sh. In Hancockia the features of sting sacs favourable for defence are mild as compared to aeolids. The aeolid large sting sac which engulfs and stores large masses of stinging cells and functions in defence, may have evolved from small nematocyst-storing organs endowed with expulsive capacity, similar to those found today in Hancockia . Phylliroe (Fig. 9.45 ) has a highly developed swimming ability, and its entire life is spent in the water column. This slug has a fl at elongated body resembling a leaf

Fig. 9.45 A medusa with a Phylliroe inside 9.8 Nudibranchia: Nudibranchs 251

Fig. 9.46 Hood-slug, Melibe rangii (9 cm), Red Sea; an individual in which many of the cerata have been lost

(‘ Phyll’ in Greek refers to a leaf) and extended at its rear to a small tail. The foot is reduced to little more than a glandular remnant sunk into the ventral side. During swimming, continuous undulating muscular waves going from the head backwards push the body forwards in a snake-like movement. The body is largely transparent, but has glistening patches of colour originating in special glandular cells spread all over the surface. The digestive gland lobes are of a golden colour, shining brilliantly through the transparent body and adding to the overall colour of the Phylliroe . The signifi cance of this amazing colour is not known. Phylliroe preys on medusas: it swims into the medusa’s bell, attaches to it with its small foot and eats the tissue by combining biting movements of its hard jaws with suction movements of its muscular oesophagus. All parts of the medusa are eaten, including the tentacles and their stinging cells. Growth is rapid, and cases are known of an individual Phyllyroe growing from 1 to 10 mm within just 10 days. Upon having fi nished eating the tissues of its prey, Phylliroe swims away, sometimes with remnants of the medusa still attached to its foot. One of the most fascinating sea slugs is the hood slug Melibe (Fig. 9.46 ) that dwells on sea grasses such as Zosteria and Posidonia . There, the young hooded slugs feed on fi lamentous algae that settle on the grasses, and the adults feed on tiny crustaceans they capture either from the water column or the sea grass blades, aided by a special convex hood-like organ in front of the mouth. This organ contains a wealth of diagonal, circular and straight muscle cells which give it much fl exibility, as well as nerve cells which enable a coordinated and accurate response. There are two circles of tentacles around the margins of the hood. The mouth is positioned inside the hood and lacks a radula, as one would expect from a sea slug with a plankton diet. The hood is spread facing the water current; when an organism of the plankton is swept into it and touches its inner side, it immediately closes; the tentacles rapidly interlock to prevent the prey from fl eeing, and the entire hood contracts to push the prey to the mouth. The hood responds not only to prey contact, but also to movements in the water and to prey odour. In addition, it opens and closes rhythmically without any stimulus. The higher the density of the prey in the surrounding sea water, the faster these rhythmic movements. The embryonic source of the hood is the veliger’s sails, that fuse in front of the mouth during metamorphosis. Melibe has a unique mechanism of defence: when in stress, it self-amputates some of the cerata on its back. After loss, the amputated cerata vigorously bend and 252 9 Shell Degeneration: Sea Slugs and Relatives twist for some minutes, distracting the predator. As the cerata are all sticky, their amputation is a repelling mechanism against predators (‘you have been warned, all of me is sticky in this repelling manner’). The site of this self amputation is fi xed: each lobe has a pre-prepared amputation plane with a circular muscle. A strong stimulus of the ceras, such as a bite or pinch, results in strong contraction of the circular muscle and coordinated contract of longitudinal muscles within – and the ceras is cast off. Healing of the wound is obtained by a strong and continuous contraction of the circular muscle. It is not known whether a new ceras grows following self amputation. In addition to amputating its cerata Melibe can react to stress by detaching itself from the substratum and fl oating motionless in the water, or by swimming, wriggling its body from side to side.

Bibliography

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Abstract Marine pulmonates (Pulmonata) can aquire oxygen from open air; they are hermaphrodites. Siphonaria, of intertidal rocky shores, breathes by gill when tides rise, by lung when tides recede; copulation is mutual or one-sided, eggs are laid in capsules from which veligers hatch; in some, embryonic development occurs within the capsule and crawling juveniles emerge. Gadinalea , of mid-tidal caves, produces a mucus curtain in which plankton is trapped. Amphibola , a detritus-feeder of mud ﬂ ats high up the shore, breathes both aerial and aquatic oxygen; it can cope with freshwater for considerable periods. Onchidiidae are air-breathing sea (and land) slugs of intertidal rocky coasts which feed during low tide; some live in rainforests. Myosotella , of salt marshes, breathes only through a lung and drowns if kept underwater; eggs are deposited in capsules, in which veligers develop and metamorphose, eventually hatching as crawling juveniles. Carychium, a primitive air- breathing pulmonate of damp river bank litter, lays eggs which develop directly to a miniature adult. Advanced pulmonate land snails lay enormous eggs with much yolk and water, enabling complete development of the embryo within the egg and hatching as a crawling juvenile; each egg may be 50,000 times larger than that of a sea snail.

Keywords Amphibola • False limpet • Gadinalea • Marine pulmonates • Myosotella • Onchidiidae • Pulmonata • Pulmonate adaptation • Pulmonate lung • Siphonarioidea

Marine pulmonates (Pulmonata) resemble the Opisthobranchia so closely in certain details of their morphology that they are clearly and undoubtedly closely related. Like sea slugs, pulmonates are hermaphrodites, and they too lack an operculum. The two groups closely also resemble each other in many details of their nervous systems. However, pulmonates differ from opisthobranchs in that their mantle cavity still lies above the head and faces forward. As to their habitat, whereas sea slugs dwell in the sea, the ancestral environments of pulmonates seem to be on the border between sea and land, in tidal zones and estuaries. Both these environments are harsh habitats for marine-conﬁ ned animals. Two major adaptations help pulmonates survive in these environments. One is the ability to receive oxygen from the air by means of a closed breathing cavity inside the body, namely a lung (the scientiﬁ c name of the super-order, Pulmonata,

© Springer International Publishing Switzerland 2015 257 J. Heller, Sea Snails, DOI 10.1007/978-3-319-15452-7_10 258 10 Marine Ancestors of most Land Snails: Pulmonates means ‘those who have a lung’). Most sea snail groups have a mantle cavity that is open and thereby exposed to dangers of desiccation when not constantly dampened by the sea. Pulmonates have a mantle with margins which gradually fused with the body wall through evolution, narrowing the opening of the sea-inhaling mantle cavity. It has become almost completely enclosed and internal, with only a small pore remaining to connect it with the external world. From this evolutionary stage the mantle cavity is termed the ‘lung cavity’ or the ‘lung’, and its opening is termed the ‘lung pore’. The enclosure considerably reduces desiccation rates when the pulmonate is not covered by the sea. Oxygen-rich air is drawn in through the lung opening, and oxygen molecules are absorbed into blood vessels densely ramifi ed in the lung’s ceiling. Primitive pulmonates still have a gill that receives oxygen molecules from the seawater, and these marine pulmonates can thus breathe both when under water and when out in the air. The ability to absorb oxygen from the air by use of a lung, the ability to periodically reduce metabolic processes when not under water, and the total emancipation from a larval developmental stage helped the ancestors of modern pulmonates to leave the sea and conquer the land and fresh water. With 30,000 living species worldwide, pulmonates represent by far the most signifi cant invasion of non-marine environments by the Mollusca. The second major adaptation to life on the border between sea and land in these ancestors was the ability to periodically reduce metabolic processes to a minimum, at the same time stopping normal activity. This reduction occurs when the physical environment is exceptionally harsh, such as under extreme conditions of desiccation and of heat. Pulmonates are not the only group of land and fresh water snails; there have been fi ve or six evolutionary colonisation shifts from the sea into brackish and fresh waters, also among the nerites (Chap. 5 ). Some, although inhabiting coastal trees or vegetation in the vicinity of fresh and brackish water, still retain a veliger that feeds in the plankton and are thus not fully limited and restricted to the land. Other groups have become fully terrestrial by evolving a lung instead of a gill, tolerance to desiccation, and a direct early intra-capsular embryonic development inside albumen- rich eggs, rather than a free-swimming veliger stage. Among winkles, one group (Pomatiidae) has evolved to live a completely terrestrial lifestyle (Sect . 7.6 ), with a gill reduced to a few mere folds of skin, the mantle cavity serving as the major breathing organ and the female laying eggs in which the embryo completes its development. There are also several other groups of land snails, but pulmonates are the dominant group. As a word of caution before continuing: the classifi cation of many primitive pulmonates is far from being stabilised. Some researchers place some groups of the ‘primitive pulmonates’ at the base of the Pulmonata, while others place these same groups at the base of the Opisthobranchia or even within the Opisthobranchia, and others place them in a separate group as the common source from which both the Pulmonata and the Opisthobranchia eventually diverged. 10.1 Siphonarioidea, False Limpets 259

10.1 Siphonarioidea, False Limpets

The marine pulmonate Siphonaria (Siphonarioidea, Figs. 10.1 and 10.2 ) lives almost entirely in the sea. It dwells on rocky intertidal shores and its fl attened low conical shell is so similar to that of a limpet of the Patelloidea (‘true limpets’, Chap. 3 ) to which it is not even closely related, that a comparison between the two is warranted. Siphonaria , commonly named a ‘false limpet’, has a lung on the right side of its body, with one opening for inhaling and another for exhaling water. When the tide rises and it is submerged under water it breathes by means of a gill at the ceiling of the water-fi lled lung cavity. Beating cilia on the gill and walls of the lung cavity form a current of sea water that fl ows into the lung and between the gill leaf- lets through an inhalant lung opening; oxygen molecules are absorbed from the water and carbon dioxide molecules are discharged into the current. The water is then expelled through an exhalant opening. False limpets have a slightly asymmetrical shell to accommodate the two lung openings, and there is a calloused area to the right front margin of the shell, under which the entrance to the lung is positioned.

Fig. 10.1 A pulmonate limpet, Siphonaria, seen from below. Arrows indicate entrance and exit of water to lung

Fig. 10.2 Pulmonate-limpet, Siphonaria sp (2 cm) 260 10 Marine Ancestors of most Land Snails: Pulmonates

Oxygen absorption from the atmosphere is one third higher than from water. When the tide recedes and the shore is exposed, Siphonaria shifts to oxygen absorption from the air: during atmospheric respiration, the lung opening remains constantly wide open and the mantle cavity functions as a lung without any active ventilation movements. After 4–8 h of aerial exposure Siphonaria gradually reduces its metabolic rate (as do limpets and winkles) moving from a heart-beat rate of 50 beats per minute down to less than 20 pulses per minute. Reduction in the overall metabolic rate may reach as low as only 18 % of the normal rate. This metabolic reduction is accompanied by a closure of the lung opening. Siphonaria can remain in this position for at least 72 h, waiting out periods of exposure to air and potential lethal temperatures (for example, if low tide is in the middle of the day) until the sea once again returns and fl oods it. Heart and oxygen consumption rates return to their sea phase and level within minutes. Siphonaria has a radula which contains many small weak teeth, that lack the iron coating and silicon fi bres of true limpets. Their weak radula dictates a soft diet and grazing on delicate algae rather than hard food from the substratum. The weak radula is perhaps the cause for the false-limpet’s inferiority in competing with true limpets: in their presence its growth rate decreases and mortality rate increases. Physiological adaptations coincide with behavioural levels of adaptation. As a period of inactivity approaches, Siphonaria retreats to its home scar, a shallow pit it forms on the rock into which its shell fi ts closely; upon attaching, it can reduce the danger of being uprooted by pounding waves of high tide, or desiccation due to exposure at low tide. Adhesion to the rock is by sticky mucus, but the adhesive abilities of its mucus reach only one half to one seventh that of the mucus of many true limpets. This may further explain why false-limpets inhabit calm parts of the rocky shore and are still active when the tide is low, returning to their scar with the incoming high tide, whereas true limpets occur also in heavy wave-break shores and are active also when the waves pound the rocks. Like true limpets and winkles, the false limpet copes well with extreme temperatures, surviving environmental temperatures of up to 46 °C and loss of 60–70 % of its water content. On the other hand, Siphonaria does better in defence against predators than true limpets because its skin contains multi-cellular glands that discharge a poisonous sticky white substance during stress, the taste of which is bitter and repulsive and avoided by predators. Due to this chemical defence Siphonaria is predated to a lesser extent than true limpets. Unlike true limpets, in which the sexes are separate and fertilisation is external, false limpets are hermaphrodites and practice internal fertilisation, like their close relatives the opisthobranchs. When mating one individual follows the mucus path of another individual, and upon reaching it the two snails align themselves so that their heads face one another and their genital openings come into contact. During copulation, each individual draws out its penis, penetrates the genital opening of the partner and transfers the sperm to the partner’s female genital system. Copulation may be mutual or one-sided. The eggs are placed in capsules, embedded into gelatinous ribbons each containing up to 20,000 eggs and laid in shallow cracks and crevices. A veliger with an operculum, a two-lobed sail and a globular shell 10.2 Other Primitive Pulmonates 261 develops in each egg. Having completed torsion and used up most of its albumen, the veliger hatches and swims away; eventually it settles and metamorphoses to adult form. In some species, such as Siphonaria serrata from South African shores, all embryonic development occurs within the capsule and crawling juveniles emerge after 3–4 weeks.

10.2 Other Primitive Pulmonates

Some primitive pulmonates lead a very different way of life. Gadinalea , a limpet- like snail of Australia and New Zealand, lives at mid-tidal level on rocky shores exposed to heavy surge, in caves with high water turbulence or in small concavities under ledges but always away from light. Living in closely aggregated colonies, it does not normally move around. Algal food is scarce in the absence of light, and the snail does not abrade the substratum with its radula. Its feeding method involves making use of the turbulence of the water. Positioned so that the water current enters from behind, it hangs upside-down and “lowers” its shell. Copious quantities of mucus are produced from glands of the mantle edge and sides of the foot, forming a curtain in front of the head that balloons out as the water passes beneath the shell in which particles of phytoplankton are trapped; once laden with particles, it is ingested. The radula is small and the teeth are more delicate than those of Siphonaria . Closely related Trimusculus of caves or narrow crevices along the Chilean coast feeds in a similar manner, ingesting particles adhering to mucus produced by the mantle, the head and the front of the foot. Its extended mantle is capable of releasing a white secretion that deters predatory starfi sh. Some Trimusculus species concentrate special chemicals (diterpenoids) in their mantle, foot and mucus, which are toxic to various larvae, such as those of the reef-building tube-worm Phragmatopoma. Other primitive pulmonates have a coiled rather than a fl at limpet-shaped shell. Amphibola crenata of New Zealand is a detritus-feeding pulmonate. Possessing an operculum and reproducing through a veliger larva, Amphibola is clearly an archaic pulmonate inhabiting a transitional habitat. It lives high up the shore on mud fl ats in sheltered bays, inlets and estuaries, where it is submerged for only 1 or 2 h in any tidal cycle; in many cases the snails are not covered by sea water during each tidal cycle and may remain exposed to the air for several days. As the tide rises, the snails tend to burrow into mud or sand, remaining there until the tide recedes. Occupying this transitional habitat between sea and land conditions, Amphibola can use aerial and aquatic oxygen equally well, and there is no difference between their rates of consumption in air and water. A. crenata also lives in areas covered with fresh water for considerable periods, and the snails can carry on their normal activities during these periods, including mating and deposition of egg masses. Amphibola crenata is unusual among pulmonates for embedding its embryos in collars formed of sediment, with the embryos being deposited between two layers of mud or sand. Among sea snails this reproductive characteristic is otherwise known only from moon shells (Sect. 8.3). The adults of A. crenata form their egg 262 10 Marine Ancestors of most Land Snails: Pulmonates collars on intertidal mudfl ats and sandfl ats. Individuals lay about 15 collars per season, and some 18,000 free swimming veligers emerge from each collar. The Onchidiidae are small, air-breathing sea (and land) slugs most of which live in tropical and temperate seas. The adults lack both shell and operculum, although both are present at the larval stage. The mantle cavity is reduced and has shifted to the rear of the body, where it gives rise to a lung; in addition, some species possess external dorsal papillae which are likely to help gas exchange when the animal is submerged, thus functioning as gills. As in most pulmonates the head bears a pair of retractile tentacles, with apical eyes. The family consists of some 25 genera. Most species inhabit the intertidal zone of rocky coasts where they move around exposed and feed during low tide, breathing fresh air; three species live in rainforests. Another primitive pulmonate dwelling between sea and land, the ellobiid Myosotella myosotis of Europe and the Mediterranean (Fig. 10.3 ; also named Ovatella myosotis), also has a coiled rather than a fl at limpet-shaped cone. It dwells in salt marshes beyond the intertidal zone and in river outlets, often under dense vegetation such as the rush, Juncus , and it can endure extreme fl uctuations in salinity, from fresh waters to three times that of sea water. Myosotella draws in water from the environment because salts are maintained in its blood at very high concentrations. It breathes through a lung richly supplied with blood vessels, and its extent of oxygen absorption on land is ten times that when under water. Indeed, it has no gill, and if forced to remain beneath water for over 48 h, it drowns. Eggs are deposited in capsules, in which the veligers develop and metamorphose; eventually a miniature adult hatches and reaches maturity, within about half a year.

Fig. 10.3 Primitive pulmonate, Myosotella myosotis (1 cm), north- eastern Atlantic and Mediterranean (From Heller 2009 , courtesy Pensoft, Soﬁ a ) 10.2 Other Primitive Pulmonates 263

Representing a more advanced step in the evolutionary transition from sea onto land, Carychium is a completely land-living primitive pulmonate, dwelling many kilometres from the sea, in damp litter along banks of rivers and streams; like Myosotella it lays eggs in which development to a miniature adult is direct. Advanced pulmonate land snails lay a small number of very large eggs, each of which contains much yolk, enabling the embryo to complete the whole embryonic stage within the egg and to hatch as an individual closely resembling the adult. The egg also supplies the developing embryo with water. Accordingly, the desert- dwelling Sphincterochila zonata of the Land of Israel (Fig. 10.4 ) lays only 50 eggs per season; each egg is 4.3 mm in diameter and has a volume 50,000 times that of Siphonaria . A snail requires calcium to form a protective shell, whether to avoid desiccation or to avoid predation. On land the source of calcium is from the water that dissolves calcium from the soil and rock in the snail’s immediate surroundings; accordingly, the distribution of calcium, or geology, limits and dictates the geographic distribution of land snails. In some pulmonate groups there is an evolutionary tendency to reduce the shell considerably, sometimes to its complete loss. A slug is a land snail that completely lacks a shell, or in which the shell is reduced to a small remnant buried within its mantle. With the degeneration and evolutionary loss of the shell, the viscera are transferred to the foot and a slug thus very superﬁ cially resembles a fat worm. The main advantage of this form is its ability to live in habitats in which calcium concentrations are too low to be suitable for shelled species. The main disadvantage is that a slug is subject to high desiccation rates and therefore limited to damp habitats. Another disadvantage is that, due to the absence of a physical or mechanical defense, the slug becomes easy prey. However, the bodies of some slug species are covered by a mucus with repellent taste which offers, to some extent, a defense and in this they resemble their distant relatives, the sea slugs.

Fig. 10.4 Advanced pulmonate land snail, Sphincterochila zonata (2 cm), Land of Israel (From Heller 2009 , courtesy Pensoft, Soﬁ a ) 264 10 Marine Ancestors of most Land Snails: Pulmonates

Bibliography

Heller J (2009) Land snails of the land of Israel, natural history and a ﬁ eld guide. Pensoft, Soﬁ a Hodgson AN (1999) The biology of siphonariid limpets (Gastropoda: Pulmonata). Oceanogr Mar Biol Annu Rev 37:245–314 Pechenik JA, Marsden ID, Pechenik O (2003) Effects of temperature, salinity, and air exposure on the estuarine pulmonate gastropod Amphibola crenata . J Exp Mar Biol Ecol 292:159–176 Ruthensteiner B, Stocker B (2008) Genital system anatomy and development of Ovatella myositis by three-dimensional computer visualisation. Acta Zool 90:166–178 Shumway SE (1981) Factors determining oxygen consumption in the marine pulmonate Amphibola crenata . Biol Bull 160:332–347 Walsby JR, Morton JE, Croxall JP (1973) The feeding mechanism and ecology of the New Zealand pulmonate limpet, Gadinalea nivea . J Zool 171:141–283 Part V Man-Snail Links Chapter 11 Magic, Status and Money

Abstract Cowries resemble a woman’s genitalia, generating belief in their ability to increase fertility. In Greek mythology Aphrodite was born inside a shell; in Japan midwives gave cowries to women in labour to ensure safe birth; and in Africa women wore aprons, with cowries over the pubis. Cowries against the evil eye were attached to harnesses of camels and elephants; sailors lowered cowry strings from boats for cowry ‘eyes’ to navigate; and in tribes considering war, priests cast cowries: apertures-up – make peace, apertures-down – make war. Men in Himalaya wore cowry belts as badges of status, reﬂ ecting that they had cut off an enemy’s hand or foot or killed him. In some African tribes only the king and his family were entitled to wear cowries. Cowries were used as money, in Africa to buy slaves and in China to pay taxes, the Chinese symbol for cowry being incorporated into writing symbols for ‘purchase’. Vishnu, with a ‘chank’ ( Turbinella pyrum) in his left hand, is sacred to the Hindu in India. Chank served as battle trumpets and as baby feeding spouts. At weddings, chank served to pour water over the hands of the couple; chank was hung on the bride’s neck; and chank bracelets placed on her wrist. Chank symbols were branded into the shoulder or stamped over the body in religious rites, and temple girls were branded with chank symbols marking dedication to their temple. As a royal emblem, chank appeared on Travancore’s coat of arms, ﬂ ag, coins and stamps.

Keywords Cowries ancient civilisation • Cowries magic • Cowries status • Cowries money • Chank

This book is devoted mainly to the natural history of sea snails, but its closing chapters deal with interactions between sea snails and Man. Since the early dawn of human culture, a chief preoccupation of prehistoric man was the need to ﬁ nd enough to eat, and snails of the sea were a rich, reliable and lasting source of protein. The empty shells were discarded onto a domestic waste pile, and today huge shell waste piles of early cultures are found along the coasts in Brazil, dating back 3,600 to 2,000 years ago, in western Canada at 5,400 years ago and in Australia, 2,000 to 235 years ago. Sea shells were also collected by early man because of his urge to possess objects of beauty, rareness and mystery, often even to wear them. Such objects may perhaps bestow upon the wearer a feeling of having a magic means of protection against

© Springer International Publishing Switzerland 2015 267 J. Heller, Sea Snails, DOI 10.1007/978-3-319-15452-7_11 268 11 Magic, Status and Money unknown powers of evil, and their beauty may have added to the beauty of the bearer. Sea shells were collected along beaches and carried inland by wandering tribes, and traded to other tribes who might never have seen the sea. This imparted qualities to the shells, and they became strange, beautiful and supernatural objects. The earliest modern humans who lived 30,000 years ago in France wore necklaces of sea shells: in graves of that period and locality, Indo-Paciﬁ c helmet shells ( Cypraecassis rufa) were found, which could only have reached there by trade. Some shells were considered sacred, and were placed in graves and ancient temples together with sacred images, ﬁ gurines and other cult objects. In Chaps. 11 , 12 , 13 and 14 we focus on several aspects of the Man-Snail link: the diverse uses of cowries in various cultures; the use of the chank shell in Hindu culture; the use of sea snails in the dye industry in ancient cultures of the Mediterranean and Central America; their use in religious rites, as a source of sacred colour, sacred scent, and as trumpets producing sacred music; and the sterilising effects of pollution on sea snail populations. Of all the sea snail groups, the cowries have captured the fancy of Man since the early dawn of human culture and until modern days. Cowries were involved in magic, status, art and as a currency.

11.1 Cowries

Belief in the magical properties of a cowry shell probably fi rst began when some prehistoric Man lifted a shell along some sea shore, noticed its resemblance to a woman’s genitalia and concluded that in some mysterious way the shell would be able to infl uence these organs. It is probably from this that the belief developed in a cowry’s ability to increase fertility, protect against sterility and encourage new life. The cowry shell became a symbol of femininity, a source of life, a construction inside which some divine deity dwells, one who is capable of giving a woman her children, a deity whose voice emits from inside the shell and whom one can hear, when putting a large shell to the ear. The shell itself was not always worshipped directly, but it was revered as an amulet or as a symbol of some goddesses. Aphrodite, the goddess of love and fertility in Greek mythology, was born from sea-foam sizzling inside a shell of some kind (in art of the fi fteenth and sixteenth centuries this shell is often pictured as a scallop). The shell carried her to an island, Cyprus, and it was the goddess herself who gave the island its name, Cypraea, the scientifi c name of cowries to this very day. In a similar manner, the people of the Vanuatu islands (east of Australia) believed that the fi rst woman ever to have existed, the mother of all mothers, was born from a cowry. The Ojibwa are a tribe that lived in the Great Lakes region of northern America until the beginning of the twentieth century. Cowry shells were brought to this region by European colonialists, as a commodity with which they bartered with the Ojibwa. These cowries, Monetaria moneta (Fig. 11.1 ) of the Indian Ocean are 11.1 Cowries 269

Fig. 11.1 Money cowry, Monetaria moneta (2 cm), Indian Ocean

not among the original fauna of dry land northern America nor even of the Great Lakes. Nevertheless, Ojibwa belief maintained that the shells were brought to the tribe by the spirit of a huge mythological bear that swam a Great Ocean and which, upon emerging onto the land, was covered by many cowry shells, which dropped off when the bear lay down to rest. The belief that cowry shells were blessed with spell and magic connected to birth was reﬂ ected in customs of many cultures. Midwives in Japan would place a cowry in each hand of a woman in labour to ensure an easy and safe birth; accordingly a cowry in Japanese is named koyasu-gai , meaning an easy birth. Likewise, shells were presented as appropriate gifts for a girl reaching puberty or a maiden just married, and they were worn on women’s dresses to ensure that she would bear many children. Two thousand years ago, cowries were worn by the women of Pompeii as charms to prevent sterility. In medieval times, women of France and England made similar use of the shells. The women of the Baganda tribe in Uganda would decorate themselves with an apron wrapped around their waist in which the cowry shell, as a fertility charm, was positioned right in front over her pubis. Among the Turkana tribes of Kenya cowry shells were reserved only for married women. An unmarried girl would decorate her clothes with beads of ostrich egg shells; upon marrying she would remove these beads and replace them with cowry shells. Belief in the magic power of a cowry as a giver of life developed in some cultures into a faith that it may revive the dead. People in various places in the world had the custom to place cowry shells inside a grave, even in the deceased person’s mouth, as a charm to ensure the continued existence of the deceased until the day when the dead would rise and return to life. Cowry shells are frequently found in very ancient graves in Egypt, from periods long before the era of the pharaohs. It was customary to use cowry shells as eyes in Egyptian mummies, and they were also placed in the orbits of the deceased people. An 8,000–9,000 years old plastered skull has been found in Jericho, Israel, in which cowry shells were set in both eye sockets, the shells embedded so that the slit of the shell aperture appears as a half-open eye. 270 11 Magic, Status and Money

Fig. 11.2 A Kuba chief

According to an ancient Chinese manuscript, it was habitual to place cowry shells in a deceased nobleman’s mouth, their precise number varying according to rank: nine cowry shells were put inside the mouth of a deceased Emperor, seven in the mouth of an important noble, fi ve in the mouth of a high offi cial, three shells in the mouth of an ordinary offi cial – and rice in the mouth of an ordinary man. When a Kuba king (in Zaire, Congo; Fig. 11.2) died he was covered with shrouds embroi- dered with cowries, and was buried in much pomp with many of his valuable pos- sessions, including cowries (and also an unfortunate slave, who was buried alive). Among the Egba (Nigeria, on the western coast of Africa) it was usual that when a distinguished person died several slaves were slaughtered and buried with him, to serve him in the netherworld. The slaves were dressed in beautiful clothes laden with cowries, beer was poured down their throats until they were drunk, and then they were slaughtered. 11.1 Cowries 271

Fig. 11.3 A mask set with cowry shells

Cowry shells also frequently served against the evil eye in many societies, presumably because the shell aperture resembles a half-closed eye (Fig. 11.3 ). In India, Persia and Egypt, it was traditional practice to attach shells to the harnesses of camels, elephants and fi shing nets; sailors in Arab countries would lower cowry strings from their boats so that their ‘eyes’ would navigate the boat across the sea waves, and Bedouin women of Hadramaut (Yemen) would wear cowry shells as defence against the evil eye. In Borneo, man-hunters of the Dyaka tribe used to put cowries into the eye sockets of human skulls which were then strung from the pillars of their houses, in the belief that this would strengthen the essence of life and communal spirit of the tribe. Cowries still serve as an element of the permanent equipment of the witchdoctor in various places in Africa. When the Egba tribe was debating whether to go to war or not, an Egba priest would throw 16 cowry shells upwards, towards the sky. If most of the shells fell with their apertures facing upwards this was taken as an omen to make peace; if a larger number fell with their aperture facing downwards, this was an omen that conditions were ripe to go to war. The cowry still serves in telling the future in southern India of today. The soothsayer marks a special pattern on the ground over which he pours a bag of cowry shells. The soothsayer mutters special incantations that give the cowries supernatural powers, and they then tell him where to place them on the pattern and how to interpret the results. Applying another method, the soothsayer fi lls a straw tray with cow dung, into which he sinks cowry 272 11 Magic, Status and Money shells that he covers with rice and leaves. He then leads the hand of the client over the cowries, chants incantations and tells the future. The Yoruba are a tribe in Nigeria, numbering 15 million, they are distinguished from other tribes by their language, history, religion and rituals; they are mainly farmers, who toil the land. The Yoruba give cowry shells one to another as messages through which they express feelings, desires and wishes. This is a language of symbols, and the number of shells and the way they are strung express a range of ideas and feelings. A single cowry strung on a short string means failure. Two shells strung facing one another mean intimacy and a meeting; if strung back to back, they mean separation and hostility. Two shells and a feather mean an urgent meeting; three shells facing the same direction together with remnants of a crocodile mean cheating, and six shells mean friendship. This use of cowries to express feelings is of special interest, because strung cowry shells with charms written on papyrus attached to them were found also in Egypt, dating back to the eighteenth through to the twenty-fi fth pharaoh dynasties (1575–656 BC). The Yoruba distinguish between two species, Monetaria moneta and Monetaria annulus (Fig. 11.4 ). Monetaria moneta was brought over by Arab merchants in very early days and today represents gods and deities responsible for the creation of Man, fertility of Woman, success of the harvest and general fertility of the land. Monetaria annulus was brought over much later, only in the nineteenth century, and has a lower value than M. moneta . It decorates objects related to Eshu, the god and deity of cheating, who is also the god of the markets in which M. moneta served as a means of payment. It also serves as a messenger between Man and the Spirits.

Fig. 11.4 Ring cowry, Monetaria annulus (2 cm), Indian and West Paciﬁ c oceans, Red Sea 11.1 Cowries 273

Fig. 11.5 A Naga warrior

Cowry shells also served as symbols of status. In the nineteenth century the Naga tribes, found in the eastern Himalayas near the Indian-Burmese border, considered cowry decorations a symbol of a man’s military achievements (Fig. 11.5 ). Three cowry strings on a warrior’s skirt stood for a successful warrior; a fourth string symbolised an outstanding warrior; an arm bracelet set with cowries was evidence that the warrior had cut off the hand of an enemy as spoils of war; an ankle bracelet decorated with cowries meant he had chopped off an enemy’s foot in battle; a chest- plate set with cowry shells meant that the warrior had killed an enemy in battle. The cowry served as a symbol of status also in Africa. The Kuba tribe in Zaire (Congo) even used it as a title of royalty in the nineteenth and the early twentieth centuries. The king and his family were called Ba’apash, meaning ‘cowry men’, because only they were entitled to wear cowries on their clothes. The number and position of the cowries represented the details of their status: all members of the royal family were entitled to wear cowry-bearing hand bracelets, but only the 274 11 Magic, Status and Money higher-ranking among them were permitted to incorporate these shells into ankle bracelets or hats. The king of the Kuba was considered a God on earth and his throne was a stool set with cowries: while sitting on it, the nobles were demanded to bring him cowry tributes and oblations as a symbol of their loyalty. Perhaps the best known use of cowries is as money. In general, and in any trade, a standard means of payment must be uniform in shape and structure, easy to carry, endurable, straightforward to count and diffi cult to counterfeit. Cowries as a group fulfi l these demands. In addition, the means of payment must be suffi ciently common to enable active trade, at least on a minor scale. This last requirement is also fulfi lled by a cowry species highly abundant in different parts of the Indian Ocean, Monetaria moneta (Fig. 11.1 ). The scientifi c name commemorates the Roman goddess Juno Moneta, in whose temple the fi rst mint of Rome was placed. The advantage of the cowry over other means of payment, such as those based on metals, is that it is very diffi cult to fake. Its disadvantage is that one cannot create a single unit of payment from a cowry that would be ten or a hundred or a thousand times more valuable than a single shell, for use in wide-scale commerce (as silver is for copper, and gold for silver, and a large coin compared to a small one). Trade in very expensive commodities requires very large amounts of single shells, and these are rather cumbersome to carry about. Their use probably began in ancient China, where both Monetaria annulus and Monetaria moneta were used as money. The shells fi rst appeared in north-western China some 4,000–5,000 years ago, during the earliest bronze cultures. They probably reached ancient China along trade routes which crossed the Eurasian and Mongolian steppes. First reaching bronze cultures in the far western inland of China, cowries later dispersed into other regions. However, even at its peak, ‘cowry- land’ of the Chinese Bronze Age ranged almost exclusively north of the Yangtze River; it was not an essential part of the culture of southern or south-eastern parts of the country, at that time. The use of cowries as means of payment in China peaked some 4,000 to 3,000 years ago, during the Shang and Western Zhou dynasties, 1600 to 770 BC. The highly valued cowries were, together with bronze, present among the royal gifts most frequently awarded, so frequent indeed that the word ‘to award’ was written in two forms, one with an added cowry sign, the other with an added metal one (Fig. 11.6 ). Cowry fi gurines made of bone, ivory, stone, clay, bronze, silver and gold also appear in the (northern) Chinese culture of this period. Their use as currency ceased in 345 BC when metal coins became common, but because coins were easily imitated, the cowries were returned to use 300 years later; in Yunnan province they were used until the fourteenth century. In certain provinces of China the use of cowries in those days was indeed so common that the king’s taxes were paid only in sea shells. In the thirteenth century, Marco Polo returned from his lengthy journey to China with beautifully glazed chinaware; the exited people of Venice were impressed that the glistening glaze of the chinaware resem- bled that of cowries, ‘porcellani’, hence the English word porcelain. In today’s Chinese writing the symbol for a cowry is incorporated into writing symbols for richness, plenty, value and purchase (Fig. 11.7 ); the ideogram combining pictures of ‘cowry + divide’ means poor; and that combining ‘cowry + few’ means cheap. 11.1 Cowries 275

Fig. 11.6 Ancient Chinese. The words ‘to award’ written in two forms, with an added cowry sign (above , in black , bold ), and with an added metal sign (below ) (Based on Peng and Zhu 1995 )

Fig. 11.7 Modern Chinese. The symbol for cowry is part of several other writing symbols denot- ing riches, oblation, of high value, and purchase (Based on Jackson 1917 )

The use of cowries as means of payment was common also in India. Here is a question in mathematics gleaned from a seventh century AD manuscript: ‘a beggar asked alms from a nobleman. The nobleman was a miser and gave him cowry shells, the value of which was 1/4 of 1/16 of 2/3 of 1/2 of a coin. How many cowries did the beggar receive?’ 276 11 Magic, Status and Money

A lively trade of cowries existed between India and China over many centuries. The cowries reached China mainly from the Maldives, islands lying to the south- west of India. The queen of the islands would send her maidens to the sea shore with coconut palms, and these were placed in shallow water so that the cowries would crawl and climb onto to them. The cowry-laden palms were brought to the shore, the cowries were left to dry out and later were sent to India, on their way to China. Seventeenth century Portuguese ships sailed from China to Bengal laden with rice, where the cargo was exchanged for shells. Each ship carried huge baskets each containing 12,000 shells, sold to the ship-owners by weight, some 9,000–10,000 shells for one rupee; upon reaching the ports of China the value of these shells doubled and tripled. In the mid eighteenth century, 6,000 cowry shells were worth one rupee. In 1842, an English gentleman built himself a stately house, the value of which was then 400 English pounds; the entire sum was paid in cowries, altogether 2.4 million shells. In 1767, cowries were the only means of paying taxes in southern Bengal and many ships sailed down the river to the town of Decca, each carrying 50 tonnes of shells. In 1801, all taxes to the British Crown were still collected in cowries, and their use came to an end only at the beginning of the twentieth century. The Hindustani word for these shells is ‘kauri’ and from here the English word cowry. Indian cowry shells were also carried westwards. Arab merchants carried them in boats across the Indian Ocean and then by caravan all the way to western Africa, where they were sold for a huge profi t. A cowry in Nigeria cost one thousand times its price in the Maldives, its land of origin. The Arabs sold their shells for gold, which fl owed into the courts of the Caliphs in Cairo and Baghdad. Centuries later, Portuguese, Arab, Dutch, French and English ships also left India for Africa, selling cowries for slaves, who were purchased for the American market; the price of a healthy slave was 20,000 shells. The huge extent of this shells-for-slaves commerce is refl ected in the fact that in 1849 alone, 300 tonnes of shells from India passed through the port of Liverpool on their way to Africa. In the seventeenth and eighteenth century, Dutch ships also sailed from Sri Lanka (Ceylon) to Amsterdam laden with Monetaria moneta shells for the slave markets of western Africa. Some ships were wrecked off the shores of Holland, and cowry shells are washed ashore to this day. In the mid nineteenth century, German merchants discovered that they could cut their costs if they introduced a new, similar species of closer origin. Accordingly, instead of bringing Monetaria moneta all the way from the distant Maldives to Africa, they entered the shell-slave market with a slightly different cowry species, one found also on the coasts of nearby eastern Africa: Monetaria annulus . This cowry is characterised by an orange-yellow ring surrounding the convex part of the shell (Fig. 11.4 ). The huge extent of the slave trade, the prosperity of the merchant routes to the Far East and the entrance of an additional cowry species as a means of payment – all combined to cause a surge, and billions of shells poured into Africa, which resulted in a rapid decrease in the value of the shells. When cowry shells fi rst appeared among the Baganda people of Uganda, one could buy a wife for two shells; merely two generations later, one needed 10,000 shells (a cow was sold for 2,500 shells, 11.2 Chank 277 a goat for 500, a tobacco pipe for 100, and a hen for 25 shells); in the mid nineteenth century, to buy a wife demanded the outrageous amount of 60,000–100,000 shells. Similarly in Zaire, the price of a hen was 10 shells and bride-dowry was 30 shells in 1850; by 1870 a hen cost 500 shells and bride-dowry had climbed to 2,500 shells. The value of cowry shells dropped and the value of metal coins rose considerably also in India; in southern Bengal, whereas one rupee was worth 2,400 shells in 1740, it was worth only 6,500 shells one 100 years later. In this reality, in which the value of the shells plunged so deep that they no longer suited even local trade, the use of cowries as a means of payment collapsed. By the beginning of the twentieth century its use still survived in remote places, but today nothing is left.

11.2 Chank

In India the large, thick shell of the whelk Turbinella pyrum (Vasidae, Fig. 11.8 ) with its rough brown periostracum has been sacred to the Hindu for thousands of years. The Tamil people, who fi sh for it in the shallow waters of the south of India and of Sri Lanka, name it sangu , and the people of northern India name it sankha , from which comes the English term chank . In Indian legends the chank was carried by the god Vishnu as a symbol of his victory over the evil marine demon Panchajana. This evil demon lived inside a chank at the bottom of the sea and Vishnu decided to destroy him. A long and terrible battle ensued and when it ended Vishnu was the winner. He killed Panchajana and upon arising from the sea he took the shell dwelling of the demon with him, as symbol of his victory. Ever since, the god Vishnu is represented in Hindu art with a chank in his left hand; and from his chank he also derives several alternative titles such as Chankapani , the “chank-armed”, and Chankamenthi , the “chank-bearer”. The Hindu remove the brown periostracum thereby exposing the white shell, and the chank is then used as a sacred item. In days of old, in the very distant past, the use of chank seems to have been as a battle shell trumpet. Early evidence of this is found in the Ramayana and the Mahabharata, two great Indian epics in which each great hero had his specifi c shell trumpet, distinguished by some high-sounding name such as God Given, Eternal Victory, Sweet Voice or Jewel Blossom; this is somewhat reminiscent of the European one-time custom of giving a specifi c name to the legendary swords of Arthur (Excalibur ) Charlemagne (Joeuse ) and the Viking heroes (Tyrfi ng). In an epic Hindu dynastic succession struggle between groups of cousins in the legendry kingdom of Kuru, the prelude to battle between the opposing hosts was the deafen- ing clamour sounded by the contesting leaders on their mighty shell trumpets (Mahabharata verses 11–19). Eventually the use of the chank spread to many other aspects of life. Today the chank is widely used also in north-eastern India, Nepal and Tibet (in which Buddhism prevails), but no longer as a battle trumpet. It is blown as a ceremonial trumpet during eclipses and earthquakes, to frighten away evil spirits intent on 278 11 Magic, Status and Money

Fig. 11.8 Chank, Turbinella pyrum (16 cm), Indian Ocean

devouring the sun or moon or on shaking the foundations of the world. The deep sonorous boom of the chank might perhaps be the origin of the sacred syllable “om” or “aum”, the primeval sound from which creation begun. This section presents (in present tense) the traditional use of chank in pre- modern India as described at the beginning of the twentieth century by James Hornell (1865–1949), a marine biologist and superintendent of ﬁ sheries in Sri Lanka (then Ceylon) and southern India, who travelled the Indian sub-continent extensively. 11.2 Chank 279

Fig. 11.9 Making children’s feeding spouts from chank shells, in Madras (Based on Hornell 1914 )

The many-sided contacts of the chank with the peoples of India may start at a very young age: Among the Tamil of southern India many babies, when being weaned, are fed from a small chank which is adapted to serve as a feeding spout: parts of the terminal whorls, just inside the shell aperture, are broken away, the central part of the columella is removed, the siphonal gutter is deepened to form a rude spout; the exterior of the shell is rubbed down, and eventually the shell receives a thin coating of fi ne whitewash, to conceal imperfections and to improve its colour (Fig. 11.9 ). The chank is of importance also at marriage. The Thandan Pulaya Tamils ascer- tain whether a marriage will be happy by spinning a chank like a top. If it falls to the north, it predicts good fortune; if to the east or west, the omens are favourable; if to the south, very unfavourable. At weddings the chank serves to pour water over the hands-in-hands of the bride and groom; and another chank, perforated to serve as a trumpet, announces the joyous event and its blasts protect the young couple from evil demons; the guests then call out “let the waters of the Ganges and the chank of the sea bring prosperity and happiness to the groom and bride”. The tali, a badge tied around the neck of the bride as a symbol of her now being married, is often composed of either a piece of chank (sankhu tali ) or of a metal ornament in the form of a miniature chank. The marriage ceremony further requires the placing of a bracelet of red-lacquered chank pieces on the left wrist of the bride, an alternative for the wedding ring used in western cultures. A wife considers it improper to appear before her husband or in public without the bracelet. If she accidentally breaks her bracelet, she replaces it at the earliest opportunity and until then she must remain indoors. If any Chanku Vellala woman appears in public without her chank 280 11 Magic, Status and Money bracelet, she is outcast and not readmitted until a fi ne is paid, which goes to cover the costs of a ceremonial dinner given to the village elders. A widow’s chank bracelets are broken and thrown upon the pyre (or upon the grave as the case may be), when her husband dies, and the dolorous clamour of the chank-blower expresses his family’s grief. When a man builds a home and the foundation trenches for a new house are dug, a ceremony is performed to assure that good fortune will become him who inhabits the house: a chank is laid into the foundation trench and pieces of fi ve metals are placed inside it (gold, silver, copper, iron and lead). Water spiced with turmeric and sandalwood is then sprinkled over the shell, it is covered with sweet-smelling fl owers, and only now is the fi rst stone of the new house lowered into the trench and placed over the chank. In spite of every precaution, sometimes an unfavourable site for building the house appears to have been chosen, as shown by a sequence of misfortunes falling upon the householder. In such cases, to remedy the misfortune a special ceremony is performed during which a chank is fi lled with water and incantations are made for 45 days, after which the chank is buried under a wall of the house. The Parawa of the Gulf of Mannar avert misfortune from a household by burying a chank almost completely in the fl oor, just inside the threshold. A little of the back of the shell shows up on the surface, in a position which ensures that when inmates of the house leave home, they must pass over it, usually touching it and thereby ensuring immunity from misfortune. The chank serves also in religious rites. The orthodox Brahman daily holds the chank in his hand and recites: “Oh chank, you who was produced by the sea and are held by Vishnu in his hand, you who are worshipped by all the Gods, receive our homage.” In a Brahman sect of southern India the men, women and children are branded with heated copper seals made in forms of the various symbols of Vishnu, and in this context a representation of a chank is burned into the skin on their left shoulder. In addition to this branding, members of the Madhva Brahmans are required to stamp fi ve religious symbols on various parts of the body each day; a yellowish paste made of white kaolin mixed with sandalwood is used. The chank is one of these symbols and it is stamped fi ve times: twice on the right side of the chest, in two places on the left arm and once on the left temple. The branding of Tamil temple girls (devadasi ) with symbols of chank is an essential feature in the ceremonies which mark their dedication to the god of their temple. In Hindu temples chank serve as libation vessels (jhal shanka ) to pour out water for washing the statues of the gods. When a new temple is built, or when a new shrine is established or a statue of an additional god added to the number already possessed in a temple, the dedicatory ceremonies include a special libation from the mouths of 108 chank shells, or, still more auspicious, from 1,008 chanks if so many can be afforded – all fi lled with water and fl owers. The operculum of the chank is also used in religious service, among the people of southern India. It is dried, ground to powder and stored for future use. When the time comes this powder is soaked, in water together with powdered sandalwood and other sweet smelling material, and formed into an aromatic paste with which the incense sticks are coated before being burnt in the shrines. 11.2 Chank 281

Fig. 11.10 Chank representing Royalty: on the national emblem of Travancore. Chank representing Royalty: on the ﬂ ag of Travancore

Chank represents royalty. In 1750 the maharaja of Travancore dedicated his kingdom to Lord Vishnu and endorsed the chank as his royal emblem. Accordingly, the chank appears (Fig. 11.10) on the coat of arms of Travancore, on its royal seals and letterheads and also on its ﬂ ag (a silver chank on a red background) on coins and on stamps. Chank also served a secular function: it was used as currency among the Naga tribes of Assam, before the advent of the rupee as uniform coinage throughout India, in 1831. A male slave was worth one cow plus three chanks and a female slave as much as three cows plus four or ﬁ ve chanks; a cow was valued at ten chanks, a goat at two. Some ethnic groups of eastern and north-eastern India have a very different atti- tude towards the chank. The Santal people practice totemistic rites and members of one of its clans, the Sankh , may not cut, burn, nor use the chank, nor may the women wear it as a personal ornament. Similarly the Sankhawar clan, of the Kurmi, are prohibited from wearing chank ornaments; and members of the Samudrala clan of the Koravas, nomads who wander throughout India, may not use chank in any way. 282 11 Magic, Status and Money

Fig. 11.11 Chank bangle patterns (Based on Hornell 1914 )

The chank industry is very ancient and traces of chank workshops have been discovered all over India dating back more than 4,000 years. In those faraway days the people of India and Sri Lanka would dive, collect and bring up whelks from the sea, and an industry of sawing the shell into bracelets then thrived on nearby beaches. With the invasion of India by Muslim tribes from the north during the fi f- teenth century, the chank-cutting industry in southern India dwindled. Eventually it recovered, but only in north-eastern India. Shells fi shed from the sea in southern India and Sri Lanka were brought to Decca, a city that became a centre for chank sawing (now Dhaka, Bangladesh). Century after century, millions of bracelets were distributed from here throughout the subcontinent and were worn by millions of women in India, Assam and Tibet. Poor women made do with simple bracelets whereas the rich had polished ones, lavishly carved (Fig. 11.11 ) and set with precious gems. The extent of the bracelet industry was so considerable that in the mid-seventeenth century four to fi ve million shells were fi shed every year in Bibliography 283

Sri Lanka alone. Gradually the industry began dying out. On the one hand chank populations became impoverished due to over-fi shing and on the other hand demand declined, as rich women began preferring gold and glass bracelets over those made of shell. By 1910 the number of specimens fi shed every year in Sri Lanka had dropped to only one and a half million, and today it is certainly much lower. In addition, the use of chank used in sacred rites dropped, and here yet another aspect must be noted. The shells of most sea snail species have whorls which coil to the right, but on very rare occasions a freak shell may be found in such a species, which coils to the left: In Turbinella pyrum only one such a left shell is to be found in a million. (In Indian cultures the left coiling is actually considered to be a right coiling, because the direction of a shell’s coiling is measured with the siphonal gutter pointing upwards, the opposite orientation to that which malacologists use when assigning coiling direction to a shell). A left-coiled chank (valampuri ) is revered by the Hindu as especially sacred and they carve beautiful fi gures on it, set it with precious gems, and mount it on a pedestal of gold; this whelk eventually reaches prestigious temples and the shrines of kings. At one time the value of these left-coiled shells was assessed at their weight in gold and to this day the Sakaya Monastery in Tibet keeps a left-coiled chank donated by the Tartar monarch Kublai Khan, in the thirteenth century. However, all individuals of the whelk Buscyon contrarium (Buccinidae) found in the waters off Florida have a left-whorled shell. The Hindu, with their fondness of left shells, import this American shell to India and place it in their shrines and temples. Consequently, demand for the original holy chank is declining. A century has passed since James Hornell so meticulously described the use of chank in India. In the 1980’s David Heppell found only 500 families involved in the chank trade in Dhaka; and another 500 in all the rest of Bangladesh. The chank culture is changing.

Bibliography

Buijse JA (1993) Species composition and origin of tropical cowries used in a round game in Zeeland, the Netherlands. Basteria 57:115–124 Heppell D (2001) The chank shell industry in modern India. Princely State Rep 2:8 Hornell J (1914) The sacred chank of India: a monograph of the Indian conch Turbinella pyrym . Madras Fish Bur Bull 7:1–181 Hornell J (1942) The Indian chank in folklore and religion. Folklore 53:113–125 Jackson JW (1917) Shells as evidence of the migrations of the early culture. Manchester University Press, Manchester Peng K, Zhu Y (1995) New research on the origin of cowries used in ancient China. Sino-Platonic Pap 68:1–21 Rose KD (1974) The religious use of Turbinella pyrum (Linnaeus), the Indian chank. Nautilus 88:1–5 Safer JF, Gill FM (1982) Spirals from the sea. Clarkson Potter, New York Saul M (1974) Shells. An illustrated guide to a timeless and fascinating world. Country Life, London Chapter 12 In Palaces and Shrines: Purple and Blue and Shekhelet

Abstract Ancient purple and blue dyes and shekhelet were produced from snails. Purple clothes were a symbol of social status. Only emperors in Rome wore all- purple clothes; others were permitted only purple in garment margins or on stripes. The purple dye industry in Tyre was private property of the emperor, it produced ‘imperial’ purple, and private production of purple-dyed cloth was a crime. ‘Born in purple’ was a title of honour in the Byzantine Empire, conferred only upon a child of an Emperor and Empress born in the special ‘purple chamber’ veneered with Imperial Porphyry. The royal purple industry began dying out in the sixteenth century. Pre-hispanic Indians of America exploited the sea snail Plicopurpura pansa for purple dye. Eventually the dye industry dwindled because of snail over-exploitation. Also blue dye was produced from sea snails. It was used in the biblical tabernacle drapings, high priest’s garments and in the veil of the Holy of Holies in King Solomon’s temple. Blue had religious biblical signiﬁ cance: to remember and obey the Lord’s commandments. Its manufacturing technique was lost during Byzantine times. An operculum consists of horny, claw-like matter and in some snails it resembles a claw. Biblical Shekhelet, put into holy incense, is translated in Greek to a claw – perhaps an operculum. Linnaeus mentions (Latin) ‘an odorous claw from the operculum of the purple murex’. The link between a claw and an odorous operculum, may also link to the biblical shekhelet .

Keywords Bolinus purple • Hexaplex purple • Plicopurpura purple • Purple culture • Royal purple • Shekhelet • Shell blue dye • Shell purple dye • Stramonita purple • Tekhelet

In ancient times the process of dying cloth was so time-consuming, diffi cult and costly that coloured clothes were a luxury enjoyed only by royalty, priests and the very rich. Some of the ancient dyes used for colouring cotton, wool and linen were extracted from trees, fl owers and fruit, but the processes of extracting dye from plants was restricted to the seasons when the plants were ripe and ready for use. Thus, orange-yellow, for example, was produced from crocus plants which fl ower only in the late autumn (in south-west Asia); the orange-yellow dye can be extracted only during the 24-h blooming period of each fl ower. Accordingly dying was a

© Springer International Publishing Switzerland 2015 285 J. Heller, Sea Snails, DOI 10.1007/978-3-319-15452-7_12 286 12 In Palaces and Shrines: Purple and Blue and Shekhelet skilled job, so much so that often a dyer would specialise in just one particular colour. The time-consuming nature of the ‘dye harvest’ made the dyes valuable commodities and dye production was an important source of income for ancient communities. Animal-based dyes, especially the purples and blues, were extracted from sea snails.

12.1 Purple

In Ancient civilisations of the Old World purple colours were produced from three muricid sea snails, Hexaplex trunculus, Bolinus brandaris and Stramonita haemastoma (Fig. 12.1 ). The source of the dye is a small gland in the mantle cavity close to the gill (the ‘hypobranchial gland’) and little is known about its function in the sea snails’ natural history. Our knowledge about the gland’s signiﬁ cance in human culture is more extensive, as it has been used to produce a dye since time immemorial. When its colourless or white-to-creamy secretions are smeared on a white cloth of wool or silk, the cloth gradually changes colour. First it acquires a shade of green, then it turns blue, afterwards it becomes red, and ﬁ nally, purple. The purple colour is gained from the molecule bromo-indigo containing two bromine atoms (Fig. 12.2 ), and it is from this substance that a purple inclining to the red was produced in ancient days. The people of the coastal town of Tyre (south-western Lebanon of today), where purple was manufactured in ancient times, referred the discovery of the dye to

Fig. 12.1 Dye producing muricids: Hexaplex trunculus, (7 cm), Mediterranean, and Atlantic coasts of Spain and northern Africa; Bolinus brandaris, (7 cm), Mediterranean; Stramonita haemastoma (9 cm), Atlantic and Mediterranean 12.1 Purple 287

Fig. 12.2 Formula of bromo-indigo, the purple pigment (above ) and of indigo, the blue pigment ( below )

Malkart, the patron of the town. Once he was strolling along the shore in the com- pany of Tyros, a very beautiful nymph whom he deeply loved. A dog happened to be trotting nearby and, coming upon a stranded sea snail, he bit into it, where upon the fur around his mouth became stained in a beautiful brilliant purple. On noticing this, Tyros declared that she would marry Malkart only if he would bring her a garment of the same beautiful colour. Malkart quickly collected as many snails as he needed, extracted their dye and dyed what was to become the ﬁ rst purple garment recorded in human history. Malkart thus gained the nymph, Tyros gained the purple garment and the people of Tyre gained the skill for producing royal purple; the dog gained nothing (Fig. 12.3 ; in some sources Malkart is named Herakles-Malkart or Hercules-of-Tyre). Purple cloths were one of the most expensive commodities of the ancient world. Only two drops of raw material could be produced from each sea snail, and this quantity was further reduced during processing. No less than 70,000 sea snails were required to dye a cloth weighing 1 kg. Purple was produced in dye industries mainly in the town of Tyre, but subsequently in many other Phoenician and Greek towns 288 12 In Palaces and Shrines: Purple and Blue and Shekhelet

Fig. 12.3 Malkart of Tyre and the dog, its paw on the shell and its fur stained with drops of purple; by Canals 1779 , the engraving is based on a painting by Rubens (1636) along the north-eastern shores of the Mediterranean Sea, in today’s Israel, Lebanon, Syria, Turkey, Greece and southern Italy. The techniques for producing purple and for using it for dyeing wool are described both by Aristotle (350–300 BC) and Pliny (approximately 50 AD). In very distant days, at the very dawn of the purple dye manufacture, snail-fi shers would lower ropes from boats to the sea-fl oor to which they had tied baits of fl esh, and the murexes, being predatory sea snails, were attracted to the strong odour, and clung on to the bait; after some time the ropes would be hauled up. One disadvantage of this fi shing method was that although many sea snails would reach the bait and probe into it, many of them would detach from the bait upon hauling the rope up and drop back to the sea fl oor, so that in the end the catch was poor. Some generations later this problem in the purple dye industry was overcome by lowering down a woven basket into which the bait was placed. Using this improved fi shing method, all murexes attracted to the bait would crawl into the basket and would remain in it when the rope was hauled up. The sea snail species fi shed and sacrifi ced for the purple-dye industry were, in the words of Pliny, of two kinds: the whelk is a smaller shell resembling the one which gives out the sound of a trumpet, whence the reason of its name, by means of the round mouth incised in its edge; the other is called the purple, with a channelled beak jutting out and the side of the channel tube-shaped inwards, through which the tongue can shoot out; moreover it is prickly all around, with approximately seven spikes forming a ring, that are not found in the whelk, though both shells have as many rings as they are years old… 12.1 Purple 289

In Pliny’s description, the trumpet-like whelk with its incised mouth refers most probably to the genus Stramonita, while the snail with a channelled beak and prickly spikes refers to the two genera Hexaplex and Bolinus . The sea snails were then concentrated in other baskets that were left in the sea, or in cisterns quarried out of intertidal rocks along the shore that were fl ushed by the sea with the rising tide. This concentration was necessary because the dyeing process required an enormous number of snails, many more than could be fi shed during a single day. It was also important that the gland be extracted from the sea snail while it was still alive, otherwise the sea snail would, in the words of Aristotle, ‘vomit its colour’ and could no longer be used to produce the dye. The collected sea snails were kept together for several weeks, during which, under these conditions of unnaturally high densities and of continued hunger, the stronger sea snails would start boring holes into the shells of the weaker ones and eat them. Eventually, after suffi cient sea snails had been gathered, craftsmen of the industry would smash all the shells, extract the snails and cover them with salt to prevent their fl esh from rotting. When crushed, the colour glands secrete a colourless product that oxidises upon contact with air and gradually changes into purple; at the same time, the product precipitates. Precipitation is slowed in presence of an alkali, while acidity and heat speed it up; acid and heat indeed may cause an immediate precipitation and appearance of the dye. These characteristics of the dye were refl ected in its production in ancient times. Wool was dyed by fi rst boiling water (to remove oxygen-containing air bubbles) and after it had cooled, pouring it into a large lead cauldron. The colour glands were separated from the crushed sea snails, added to the water and stirred. If left at room temperature, the solution would turn violet within a few hours. The pot was heated for a few days above an oven with hot air beneath it, brought from a nearby furnace by pipe (this indirect heating enabled a more precise control over the pot temperatures than if it had been placed directly over a fi re). It was then decanted, fi ltered through a fi ne cloth, and the quality of the colour was examined by dipping a strand of wool into the dye. When the desired colour was achieved, larger quantities of wool were soaked in the solution for several hours or days. Different shades of purple, to red or to blue, were achieved by dilution or by mixing glands taken from different snail genera, those of Hexaplex with those taken from Bolinus or Stramonita . The wool was then taken out of the bath and, to fi x the dye, was immersed in vinegar at room temperature for an hour. Alkalinity, so essential for the dyeing process, was provided by forming a mixture of wood ash and water. This mixture can reach a pH of 12 due to the wood ash’s potassium content, which forms potassium hydroxide. The mixture was then decanted and added to the cauldron. Another way of providing alkalinity was by fermenting urine for a week at room temperature until urea converted into ammonia, reaching a pH of 9.10. This solution was then added to the cauldron. Not surpris- ingly the purple-dye craftsman was, as vividly described in an Egyptian Papyrus of 1400 BC, one whose ‘hands stink, they have the smell of decaying fi sh; his eyes are overcome with exhaustion’. 290 12 In Palaces and Shrines: Purple and Blue and Shekhelet

Because of their stability, beauty and high price, clothes of purple were a symbol of social status throughout the ancient world. Remains of the industry from the nineteenth to the second centuries BC have been excavated along shores throughout the Levant, in context with Minoan, Egyptian, Phoenician, Israelite, Persian and Hellenic cultures. The remains include vast assemblages of smashed shells of Hexaplex , Bolinus and Stramonita, many of which had bored holes, evidence that they were starved to cannibalism before being smashed for use. Large pottery vats have also been found, still with traces of purple colour (bromo-indigo) along their inner rim. Purple dye was extracted from murex shells along coastal lagoons of eastern Italy (Coppa Nevigata) already by 1800 BC (the Bronze Age), but production at the site sharply dropped off by the twelfth century BC. In the Minoan civilisation of Crete (3000–1000 BC) houses were decorated with frescoes using murex-purple as paint, crushed murex shells were used to strengthen earthen fl oors and murex shells were a common design motif on pottery and carved gemstones. Minoan textiles have not as yet been excavated but the frescoes bear evidence that the Minoans wove fi ne wool cloth, profusely patterned and coloured. Murex dye was produced also off the eastern coast of ancient Greece, from the sixteenth through the tenth centuries BC, by people of the Mycenaean culture (Bronze to early Iron Age), who prepared multi-coloured garments. Purple dye production at Troy began in the mid eighteenth century BC. During the siege of Troy (c. 1200 BC) Iris, goddess of the rainbow, found Helen in her room “working at a great web of purple linen, on which she was embroidering the battle between the Trojans and Achaeans” (Iliad, book 3, 125–128). In conclusion, the manufacture of purple dye from Murex snails was a Middle Bronze Age Aegean invention, beginning in the early eighteenth century BC, if not earlier. In Syria remnants of purple dye were found in a Bronze Age tomb in which some royal person was buried for over 300 years, prior to destruction of the palace above it in 1340 BC. At around 1000 BC the Phoenicians of Tyre, a nation of seafaring traders, became the masters of their days in the murex-purple dye and in its trade. They developed, promoted and maintained the thriving, far-fl ung luxury commerce of murex-purple dyed wool; indeed, the name ‘Phoenician’ is derived from the Greek phoinikas , meaning purple-red. Excavations in the ancient town of Sidon, near Tyre, have revealed a pile of discarded murex shells near an ancient dyeing industry; it was 3 m high, 25 m wide and 100 m long. In sections of this murex pile, Hexaplex was separated from Bolinus, perhaps indicating a dyeing of purple that was separated from that of blue. Weights for looms were also found, evidence of a nearby spinning and weaving industry. From the days of the Persian king Darius (approximately 500 BC) a large plastered marble jar was found, the entire exterior of which was painted in royal murex- purple; words of praise to Darius were carved onto the jar, which probably served as a royal present from the king to someone dear to him. This jar is, however, an exception, and the most frequent use of royal purple was as a textile dye. The oldest known direct evidence of a murex-dyed textile is a fi ne wool tapestry woven during the fi fth to fourth centuries BC in Persia. Fragments of cloaks from graves in 12.1 Purple 291

Palmyra, Syria, from the fourth and third centuries BC were dyed murex purple-red. Coins struck in Tyre in the fi fth century BC present murex shells, often together with dolphins. In Biblical times, the kings of Midian defeated by Gideon wore clothes of purple, and later on, part of King Solomon’s chariot was purple. In the sixth century, during the fi nal days of the Babylonian Empire, King Balthazar was giving a banquet when, suddenly, the fi ngers of a human hand appeared which wrote four words on the palace wall: ‘Mene mene tekel u-pharsin’. Trembling with fear, the king announced that he who could explain this writing ‘shall be robed in purple’. It was the prophet Daniel who interpreted the four words and he was, indeed as the king had promised, clothed in purple. (The words meant that God had numbered the days of Balthazar’s kingdom, the king was weighed in the balances and found wanting, and his kingdom would be divided and given to the Medes and the Persians). A century later, the Persian Emperor Ahasuerus (or Xerxes, son of king Darius) used purple cords in his royal pavilion and decorated Mordechai with a cloak of purple. The Biblical word for purple is argaman or argavan , resembling the Acadian argamanu and argawanu , and the Sanskrit ragaman . Purple garments were of royal signifi cance also in Hellenic culture. In the fourth century BC Greece conquered the Levant and in 324 BC the troops of Alexander the Great, when they took the Persian town of Susa and looted the royal treasury, were surprised to fi nd that it contained a vast store of purple robes. The Greek incorporated the Phoenician cities into their empire and the Phoenician dyeing and textile skills continued to fl ourish. Thus in 165 BC Judas Maccabeus looted ‘sea-purple’ from the camps of his Greek enemies and a few years later his brother Jonathan was granted clothes of purple during his diplomatic activities. Clothes of purple were in use also among the people of Rome from the days of Romulus, the mythological founder of the town. In faraway days, when Rome was still a republic, only people of high rank and glory (such as the two censors, and army generals rich in conquests) would wear clothes all of purple; other, ordinary legion commanders would have to do with offi cial garments in which only the margins were purple. Senators would wear a tunic (a shirt resembling a short frock) in which there were broad stripes of purple, while people of lower rank would have only narrow purple stripes. When Rome became an empire, in the fi rst century BC, a toga (an external loose garment worn for public appearances) dyed all in purple was to become exclusively the garment of the Emperor; it was Nero who, wearing an all-purple robe, issued a decree that anyone else who did so would be executed. High offi cials wore togas in which only the margins were purple, over a tunic decorated in purple stripes; lower offi cials wore garments with progressively less purple. The offi cial status was thus refl ected in the quantity of purple on the offi cial dress. The cloth industry of Rome in the fi rst century AD used two types of fi bre, fl ax and wool. Flax was the more widespread of the two in the hot Mediterranean climate, but colour dyes did not bind to it very well. To have both convenient clothes and symbols of status, the Romans of the day wore fl ax tunics decorated in rich colours, including purple produced from sea snails, and this was achieved by adding strips of wool to the margins or as longitudinal strips woven through the fabric. 292 12 In Palaces and Shrines: Purple and Blue and Shekhelet

Towards the end of the third century AD, the rich people of Rome began adorn- ing themselves in clothes made of silk, a fi bre that enhanced the purple dye. Silk and wool are both protein fi bres obtained from animals and as such, both have carboxyl and amino groups available to which dyestuffs can bond, unlike plant fi bres such as cotton, linen and fl ax. Silk is also highly absorbent, which makes it easier to dye than any other fi bre and requires less dye to achieve more effect. The Roman emperor Aurelian (270–275 AD) refused to let his wife Severina buy a purple-dyed silk garment, as it cost its weight in gold. At some point between the years 284–305 AD, the purple industry in the town of Tyre became the private property of the emperor Diocletian (Fig. 12.4 ) and the dye of Tyre became known as ‘royal’ or ‘imperial’ purple. Texts dating from those days tell us that the price of half a kilogram of purple-dyed wool was then worth 50,000 silver coins (‘denarii’) and half a kilogram of purple-dyed silk was 150,000 silver coins; for comparison, the wages of a baker amounted to 50 silver coins a day. Many Roman coins struck at Tyre throughout the third century AD present murex shells, as did coins struck in Tyre 600 years earlier, in the fi fth century BC (Fig. 12.5 ). Cheap imitations of snail-purple were produced from two insects that also provided a reddish purple colour, but their colours were not stable and therefore fetched a much lower price. One colour, named kermes by the Romans (hence the modern term crimson; karmil in the Bible, in the book of Daniel) was produced from the aphid Coccus illicus living on the oak Quercus coccifera and was sold for only 3,000 silver coins per kilogram, while the other colour, termed orchil (produced from the insect Rocella tintoria) was sold for even less, 600–1,200 silver coins. At the end of the fourth century and beginning of the fi fth century AD, imperial orders declared that the private commercial production of purple-dyed wool and silk from sea snails was a crime, and that all commercial production was to be carried out exclusively in the dyeing factories and looms owned by the emperor. Furthermore,

Fig. 12.4 Diocletian 12.1 Purple 293

Fig. 12.5 Coins with shells, from Tyre: ( a ) Phoenician, 430 BC: a shell, sea waves and a dolphin ( b ) Roman, 200 AD: dog and shell (After Amatius 1784 ) (c ) Roman, 215: murex shell between the legs of an eagle 294 12 In Palaces and Shrines: Purple and Blue and Shekhelet even the private acquisition of snail-purple dyed silk (or of any colour imitating it) became illegal. Only the Emperor and his family were permitted to wear silk of this majestic colour. Later in history, these harsh laws were modifi ed. It was in the eastern Roman Empire of Byzantium (founded in 395 AD) that the murex-purple fashion reached its all-time peak. The Byzantine emperors considered themselves Romans, but the term ‘Byzantine’ more accurately describes their very different culture. The eastern Roman realm differed from the western empire in that it was heir to the Hellenic civilisation, a blending of Greek, Syrian and Persian elements dating back to the conquests of Alexander the Great. It was more commercial, more urban, and more rich than the west. The Byzantine emperors embraced the symbolism of purple, and prestigious silks of both purple and purple woven with gold thread, were imperial monopolies. In the days of Justinian the Great (527–565 AD, Fig. 12.6 ) citizens were permitted to wear purple silk of low quality, but not to possess the ‘forbidden silk’, the silk dyed in high-quality murex-purple, which was worn only by the emperors. Another decree prevailed, that all royal documents “shall not be of any other colour than purple, made of the ashes of two kinds of shell-fi sh called murex and conchylus… It shall not be lawful for, or permitted to anyone, to have or to seek for any dye of this kind, or to expect to obtain it from any source, and he who auda- ciously violates this rule shall be condemned to death, after the confi scation of all his property.” (Justinian Codex Book 1 Title XX111: 1.23.6). Fishermen of purple were state employees, and by Byzantine law “if any one dares to use a ship assigned for gathering the purple fi sh, he shall pay two pounds of gold to the treasury” (Book X1 Title V111: 11.8.9). Eventually, the production of purple became a zealously-kept secret among the courts of the emperors of Byzantium. A document dating from the ninth century detailing the regulations for silk production at commercial levels stated that any

Fig. 12.6 Justinian 12.1 Purple 295 private dying of purple silk (of high-quality Tyre-purple) was illegal, under punish- ment of chopping off a hand; one was only allowed to weave low-quality purple garments, and that in limited amounts. Furthermore, in the Byzantine Empire ‘born in the purple’ ( porphyrogenitos ) was a title of honour given to a son or daughter of a reigning Emperor and reigning Empress, not merely the child of a concubine. The most signifi cant condition of being one born in purple was that the child be born in the ‘purple chamber’ ( porphýra), a pavilion in the Great Palace of Constantinople in which the walls, fl oor and ceiling were completely veneered with Imperial Porphyry; no child born anywhere else could receive this honorary title. Several Byzantine diplomatic mis- sions were concluded successfully only on the condition of a porphyrogenita bride being sent to solidify the bargain, or in reverse, of a foreign princess coming to Byzantium to seal a treaty, only on the condition of marrying a porphyrogenitos . The signifi cance of purple as a royal colour reached far beyond the Byzantine royal palace. Among Jewish circles of the Byzantine Empire, approximately in 850 AD, an interesting myth circulated, that the Lord in Heaven himself wore a cloak of royal purple. Seated on His throne on the Day of Atonement when the Devil comes as prosecutor, God ‘takes their sins from the scales of justice and places them beneath his purple robes’ (the word used being porphyria ; Psikta Rabbatti 45). Furthermore, the ancient Greek story of Helen of Troy weaving killed warriors into a robe is echoed in several Jewish ancient and medieval texts. An early medieval text written around the sixth century (Midrash Tehillim) writes that “each and every massacred Jew is woven into the Lord’s purple cloak” (again, the word is porphyria ). Ephraim Ben Yitzhak (twelfth century, Germany) writes in Hebrew “engrave all the avenged, on your porphyria ”. According to the Zohar, a book of Jewish mysticism written in Spain (thirteenth century, in Aramaic), an angel takes the icons of all massacred Jews, and engraves them into his robes of scorching fl ame; the angel then takes these robes to Heaven and the Lord then takes and engraves them into his own royal purple mantle, the porphyrias . Thus the idea of the murex purple cloak as a sign of extreme dignity swirls up from the real world of classical ancient Greek legends to the metaphysical realms of the Jewish Kabbalah. Purple was still manufactured along some eastern shores of the Mediterranean in Medieval times, and the crusaders called the town of Haifa ‘the purple town’ ( Porphyra Novissima , represented as Porphyrion in a map from the nineteenth century, Fig. 12.7 ). Throughout the Byzantine Empire, as in Roman and Greek times centuries before, purple meant glamour, royalty, aristocracy, wealth and power. Then, in 1453 the Byzantine Empire fell to the Ottoman Turks. For the Turks and Arabs, who were Muslims, purple did not carry the same symbolic signifi cance as for the Byzantines and the murex-purple industry began its decline. Soon another blow fell on the industry: in 1467 a papal decree stated that the murex purple previously used on cardinal’s robes should be replaced by scarlet, a colour intended to bring the cardinals onto a level equal with kings. The new ‘cardinal purple’ was a mixture of indigo and the dye of the crimson beetle kermes . By this colour shift, said the pope, the Ottomans would lose valuable revenue and the church would gain it. Yet another blow to the murex industry lay ahead: with the discovery of America 296 12 In Palaces and Shrines: Purple and Blue and Shekhelet

Fig. 12.7 Porphyrion on the outskirts of Haifa, Israel (A map from the early nineteenth century)

Fig. 12.8 Purple producing shells in Wales, UK (From Cole 1685 )

(1492) cochineal, a cheaper crimson obtained from the local insect Dactylopius coccus, was brought from the New to the Old World. From the sixteenth century onwards, dyers began mixing the cheaper dye with indigo to obtain shades formerly obtained from the snails. The royal murex purple industry was dying out. In later years murex-purple served minor purposes and there were attempts to revive the industry here and there throughout Europe. In England and Ireland during the seventeenth century, it was habitual to mark linen with the initials of the owner, and in 1684 a certain William Cole of the Philosophical Society of Oxford produced purple dye from sea snails he collected in south western Wales (Fig. 12.8 ); he used 12.1 Purple 297

Fig. 12.9 Purple producing shells on which to found a dye industry in Spain (From Canals 1779 ) the dye to mark names on linen by use of the stiff point of a horsehair pencil. With the idea of setting up an industry of purple dye along the coasts of Britain, he sent cloth marked with letters and names to the Royal Society in London, that appointed a gentleman “to wait on his late Majesty with them, who with divers persons of honour to whom they were shown was much pleased with the sight, and relation of the discovery, as new onto him”. In spite of this positive response by his Majesty King Charles II, industries of purple dye were never set up along the British coasts. A similar initiative met the same fate in Spain one century later. Marti Canals was director general of the Spanish state dye-works and state offi cial in all matters concerning the cultivation, production and use of natural dyestuffs: he sought to rein- troduce the purple dyeing industry into Spain for the country’s economic benefi t (Fig. 12.9 ). But, as in England a century earlier, no snail-purple industries were set up along the Spanish coasts. However, even though the signifi cance of purple obtained from snails has declined, the esteem of purple as a colour of status has remained and, centuries after 298 12 In Palaces and Shrines: Purple and Blue and Shekhelet

Fig. 12.10 Plicopurpura pansa (5 cm), eastern Paciﬁ c (Mexico to Peru)

the snail-dye industry had become extinct, purple garments are still of importance in churches and in universities. To this very day, western Cardinals, eastern Patriarchs (such as the Maronite Patriarch of Lebanon) and many university Rectors in Europe, all clothe themselves in one shade or another of purple at festive events. It is remarkable that the use of purple shell-dye in the Old World was paralleled in the New World, in Central America and Mexico. Here the main sea snail exploited for purple production was Plicopurpura pansa (Fig. 12.10 , formerly Purpura pansa ) an inhabitant of intertidal rocks that ranges along the eastern Pacifi c coast from Mexico down to Peru. At low tides this ‘purple snail’ is easily gathered and ejects its dye-producing liquid in such a quantity that there is no need to kill the animal to obtain the ink. Furthermore, the dye-producing gland is so active that the snails can be periodically ‘milked’. The secretion is a milky-white liquid which turns, on exposure to air and light, fi rst yellow, then greenish, bluish, and fi nally purple. Approximately 300 snails must be milked to dye cotton threads suffi cient for one traditional skirt. 12.1 Purple 299

Direct evidence as to the beginnings of the use of shell dye in the New World is meagre, because textile conservation is poor in the humid tropical climate of Mexico and Central America. Among Mayan textile fragments found in a sealed jar in Mexico and perhaps dating to the Spanish conquest, one fragment was painted purple with a brush on both sides, the pigment probably coming from Plicopurpura pansa. A screen-fold book of deer hide from Mexico recording the genealogies, alliances and conquests of several eleventh and twelfth-century rulers of a small city-state in highland Mexico, has many pages painted with vivid little scenes and date glyphs in bright colours; it is termed the ‘Codex Nuttall’. Purple from an as-yet undetermined source was applied as paint, and distinguished ladies dressed in purple skirts, ponchos, and coats are shown all stained with the same colour; so too are chiefs wearing purple aprons and headdresses. Additionally, according to this manuscript, purple was probably used as a body colorant for priests. It is as yet not clear when this pre-Hispanic book was produced. Written European evidence on the use of purple shell-dye for dyeing cloth on the Pacifi c Coasts of Mexico and of Central America begins in the seventeenth century, with the English preacher Thomas Gage who noted that in Costa Rica there were Indians who were treated like slaves and used by the Spaniards to collect Purpura snails along the shore during the spring and make purple dyed threads, and such dyed cloth “is sold at fi ve or six pounds the yard, and used only by the greatest Dons of Spain” (Gage 1655 in Naegel 2004 ; the Dons of Spain were most probably Spaniards living in the Americas, since during this time shell-dye purple was not used any more in Europe). A century later the Spaniard Antonio Ulloa (1748 ) described the production and use of shell-dye purple from sea snails collected along coasts in Central America. Indians would kill the snail to extract its purple-yielding juice and discard the dead animal. Others, however, would keep it alive, only pressing it to cause its juice to be ejected and then returning it to the shore to recover; then after some time they would collect the same snail again, and ‘milk’ it. “…a group of dyers would spend a month working from one bay to the next, and return during the following moon to “milk” the same animals again. In either case, once they had collected a suffi cient quantity they would draw the thread to be dyed through the liquid. At fi rst the thread would become milky-white, then green and fi nally purple. One man could dye as much as a quarter of a pound of yarn in a single tide or, in theory, 15 pounds a month. However, little work was done for a week or so near new moon, when it was thought that the dye was too thin or too meagre. It was believed that both the weight and colour of shellfi sh-dyed thread varied according to the time of day, and sellers and buyers agreed upon a specifi c hour for their transactions” (Ulloa 1748 , in Naegel 2004 ). The fi nest purple, coming from the coasts of Ecuador, was a lively and dura- ble colour which did not lose its lustre by frequent washing and did not fade through continued use and exposure. This dyed yarn, highly prized on account of its fi ne and rare colour, was used in making ribbons and lace. Another century went by, and the process of purple dyeing as practiced by the Indian communities of Central America was again reported, this time by Squier ( 1852 : 286–287) who emphasized that 300 12 In Palaces and Shrines: Purple and Blue and Shekhelet

The process of dyeing the thread illustrates the patient assiduity of the Indians. It is taken to the seaside, when a suffi cient number of shells are collected, which being dried from the sea water, the work is commenced. Each shell is taken up singly, and a slight pressure upon the valve which closes its mouth forces out a few drops of the colouring fl uid, which is then almost destitute of colour. In this each thread is dipped singly, and after absorbing enough of the precious liquid is carefully drawn out between the thumb and fi nger, and laid aside to dry. Whole days and nights are spent in this tedious process, until the work is completed. Eventually, over-exploitation of the purple snails resulted in a severe reduction of local snail populations and the fi shermen were forced to collect the snails over hundreds of kilometres along the coastline. Their scarcity, the great numbers of snails required to produce a dye and the time, patience, and labour required, all resulted in the high price of fi ve gold dollars for one hand-woven skirt by 1909. By the end of the nineteenth century the shell-purple dye industry had dwindled considerably and today it survives only in remote regions of Mexico and Costa Rica. Not only the purple industry, also the purple snail Plicopurpura pansa itself has declined, to such an extent that in Mexico in 1988 it was declared a species under special protection. Today only specifi c Indian communities are permitted to fi sh the purple shell for the traditional dying of purple cloth.

12.2 Blue

Another dye produced from murex snails was blue. Whereas the purple colour was gained from bromo-indigo, blue was formed by a molecule of indigo, which has two atoms of hydrogen instead of the two bromine atoms in bromo-indigo (Fig. 12.2 ). Indigo is found only in the hypobranchial glands of Hexaplex trunculus , which can thus be used to produce both colours and also all the many shades in-between. The Biblical word for blue is ‘ tekhelet’, resembling the Acadian takiltu (Greek and Latin do not have a word resembling tekhelet). Blue is often mentioned in Biblical texts together with purple. Together, blue and purple were used in the drapings of the tabernacle and also in the ministerial garments of the high priest. When King Solomon built his temple, King Hiram of neighbouring Sour (biblical Tyre), sent him a craftsman skilled in works of purple and tekhelet , and eventually when Solomon’s temple was completed the veil of the Holy of Holies was all blue and purple. These two colours differed in their cultural connotations. Whereas purple was an international symbol of regal status, blue had deep religious signiﬁ cance. “You must make tassels on the corners of your garments, you and your children’s children. Into this tassel you shall work a blue thread (petil tekhelet) and whenever you see this in the tassel, you shall remember all the Lord’s commandments and obey them” (Numbers 15, 38–39). Neither the Greeks and Romans mention the possibility of producing blue from sea snails. The use of blue from a sea snail is indeed very odd because an abundant, cheap and ever-renewing source of blue was available throughout the ancient 12.2 Blue 301

Biblical world in form of the true indigo shrub Indigofera tinctora , widespread in the ancient East. Indigo dye was obtained by soaking the plant’s leaves in water and then leaving them to ferment; this converted the glycoside-indicant naturally present in the plant to the blue dye indigotin; the precipitate from the fermented leaf solution was then mixed with a strong base such as lye, pressed into cakes, dried, and powdered; the powder, when mixed with various substances, would produce different shades of blue. There was therefore no need for other sources of blue, especially not from a source as rare and expensive as a sea snail. Of all nations of the ancient world only the People of Israel revered the blue as holy, because of the divine commandment concerning the blue thread; and in Biblical times blue was produced from a sea snail. In Jerusalem, Hexaplex trunculus shells were found in excavations of a priest’s house dating to the days of the second Temple (the days of Jesus Christ), suggesting that the priests of those days were familiar with this tekhelet-producing snail. The Talmud offers a description of the sea snail from which tekhelet was produced: “This snail, its body is like the sea and it is like a fi sh and it rises from the sea once in 70 years, and from its blood tekhelet dye is produced and therefore its bloods are expensive” (Babylonian Talmud, Berakhot, 44-A). Elsewhere, the colour of tekhelet is indicated: “Tekhelet resembles the sea and the sea resembles the heavens and the heavens resemble the sapphire stone and the sapphire stone resembles the throne of the Lord” (Babylonian Talmud, Hulin, 89-A). Another two other sources in Talmudic literature claim to describe the precise hue of tekhelet (Jerusalem Talmud, Berakhot, 2-A; Midrash Tehilim, 24). They differ in their defi nitions as to the colour of this dye, but both claim tekhelet resembles ‘the throne of the Lord’. It is possible that the exact colour of tekhelet was by then not known any more, but its holy signifi cance is stressed. A noteworthy point in these descriptions is that the sea snail rises from the sea only once in 70 years. This suggests that over very long periods covering very many years, the snail was too rare to be fi shed in commercial quantities, and that they were available to snail-fi shers only for brief times during the irregular appearance of dense populations. Such extreme fl uctuations in snail abundance may well have been caused by over-exploiting the local population for the dye industry. After a brief season of heavy over-fi shing, snail populations at shores near local dye industries would become impoverished; the Phoenicians of Tyre and of nearby Sidon would then sail around the shores of the eastern Mediterranean, to seek new shores of as-yet unexploited snail populations and collect dye-producible quantities. Their supply of sea snails for the dye industry thus came by import from all over the Mediterranean Sea. Meanwhile, the local Hexaplex trunculus population would slowly recover, ‘once in seventy years’, and was then over-fi shed once again; during other times it had to be imported, and therefore ‘its bloods are expensive’. Snail-fi shermen were very poor and their profession involved great risk. A sage of Talmudic times, Rabbi Yossi, wrote that he was once strolling along the shore “when I met an old man… and I asked him: from what do you make your living? And he answered – from this snail. I asked him: my son, is it abundant? And he answered: Good heavens! The snail lies in many mountains inside the sea and semammiot (sea-monsters?) surround it, and there is nobody who goes there with- 302 12 In Palaces and Shrines: Purple and Blue and Shekhelet out the semammiot biting him and he dies from suffocation on the spot…” (Sifrei Devarim, written in the third century AD). Having collected suffi cient quantities of the ‘blood’ of the sea snails, it was cooked in a special pot to which special herbs were added, until the correct blue tekhelet was produced. To test for the precise colour, a small amount of the broth was put into an eggshell into which a small strand of wool was dipped; the eggshell was then discarded and the strand of wool burnt (Babylonian Talmud, Menahot: 42-B). Because of the high expense involved in collecting the sea snails to prepare the original tekhelet, there were several attempts, already in ancient times, to produce easily obtainable imitations of the holy blue. One such imitation was ‘kela-illan ’, a dye formed by mixing blue from the vegetable source of the indigo plant with red from the female of the aphid Coccus illicus. During early Talmudic times, the use of kela-illan in the ceremonial religious thread was prohibited: ‘tekhelet is not permitted unless coming from the sea snail. If coming not from the sea snail it is disquali- fi ed’ (Babylonian Talmud Tossafta, Menahot 9, 6); ‘one does not dye tekhelet but from a sea snail’ (Babylonian Talmud, Tzitzit, 20). Later on, however, when it became exceptionally diffi cult to obtain the rare and expensive snail-tekhelet , imitation-tekhelet dyes became common. A blue-purple dyed wool was found in caves along the Dead Sea wrapped in a piece of woollen cloth together with a few unfi nished tassels (from approximately 130 AD, the Bar-Kokhba revolt). Modern chemical analysis has revealed that the dye in this fl eece was the imitation-blue, not the true tekhelet . In those days, it was impossible to distinguish between a thread dyed from the sea snail and one dyed from the plant, and hence between true tekhelet and the imitation; only a reliable and expert merchant could confi rm that the source of the blue was according to the religious commandment. Accordingly, it was ruled that ‘tekhelet is impossible to examine’, and that ‘one does not buy tekhelet but from the hands of the expert’ (Babylonian Talmud, Menakhot: 42-A). From reading the Talmud, one is impressed that in later times there was an extent of leniency for the use of kela-illan , on condition that the user did not declare it to be the true tekhelet ; the Lord shall punish ‘him who hangs kela-illan onto his clothes and says this is tekhelet ’ (Babylonian Talmud, Bava Metzia 60-A, 70-B). The Talmud also mentions that tekhelet was once smuggled from Tyre by two scholars from Tiberias, but they were caught by the Roman authorities (yet somehow they got away with it; Sanhedrin, 12). The secret of manufacturing the tekhelet was lost probably during Byzantine times and since approximately 750 AD was no longer available. Later, sages ruled that ‘tekhelet has left this world’ and knowledge of its precise shade of the blue was lost forever. It was then ruled for a tassel to be appropriate without a thread of blue, and since then Jews may wear all-white tassels. Since medieval times, Jewish scholars speculated as to the precise shade of blue of the tekhelet . In the eleventh century Rabbi Shlomo Yitzhaki (Rashi) thought that it was ‘like the sky darkening towards evening’. In the twelfth century Moshe Ben Maimon (Maimonides) thought that it ‘is the image of the sky seen by the eye when it is crystal clear’ and this is the opinion commonly held today. Various opinions 12.3 Shekhelet 303 have been expressed as to the identity of the sea snails from which the holy blue was produced. Medieval Kabalist sages believed that tekhelet was produced from snails living in the fresh water Lake Kinneret; in the seventeenth century it was suggested that tekhelet was produced from ‘the blood of a fi sh named porphyr ’ (Haim Bakhrach, Mekor Haim, 99); in the nineteenth century the Radzin Jews believed that the colour came from the ink of cuttlefi sh; in the early twentieth century Yitshak Herzog, Chief Rabbi of Ireland and eventually of Israel, believed that tekhelet could perhaps be produced from Janthina sea snails stranded on the shore. Today most scholars accept that tekhelet was produced from murexes, and experiments reveal that to produce blue in suffi cient quantities to dye four threads, 30–40 murex snails must be sacrifi ced. A budding tekhelet industry in Israel seeks to re-introduce the blue snail dye tekhelet into the Jewish religion, so that a blue thread could once again be worked into the tassels of the corners of the garments; the murex snails for this industry are imported from various Mediterranean countries. The colour of the two blue stripes on the fl ag of the State of Israel commemorates the blue tekhelet in the tassels.

12.3 Shekhelet

From the purple and the tekhelet we move on to the mystery of the shekhelet . What is this shekhelet , that the people of Israel were commanded to put into the holy incense? The Lord said to Moses, take fragrant spice: mastic resin and shekhelet and galbanum; add pure frankincense to the spices in equal proportions. Make it into incense, perfume made by the perfumers-craft, salted and pure, a holy thing (Exodus 30: 34–35). The Greek (Septuagint) translated this Biblical term into the Greek ‘onychia’ meaning a claw, and also an early Aramaic translation (Onkelos) translated shekhelet as a claw. What then was the claw? It well may be that shekhelet -claw was the operculum of a sea snail. This operculum consists of horny matter (similar to a claw) and furthermore, in some snail species in which the shell aperture is elongate, the operculum itself is in the shape of a claw (Fig. 12.11 ). For example, the operculum of Fusus and of Strombus and their allies are rounded above and pointed below, in shape of a claw. The operculum of some species produces a strong, pleasant odour when roasted. Women in Libya and Upper Egypt used to roast them over smouldering coal together with other spices such as cinnamon and ginger and to use them during a steam bath. Early Arab medical literature mentions a spice named al ’ thaphar al ’tib (the medi- cine claw) as coming from the Persian Gulf and Red Sea and giving out a pleasant smell when placed in incense. The smoke of incense was thought to have healing qualities against an ailing stomach, diseases of the liver, epilepsies and menstrua- tion disorders. Identiﬁ cation of the claw with a sea snail is hinted at in the works of Moshe ben Nachman (1195–1270) “and the shekhelet is a claw coming out of the sea”. 304 12 In Palaces and Shrines: Purple and Blue and Shekhelet

Fig. 12.11 Operculum of Strombus , shaped like a claw

Fig. 12.12 “Blacte bizantia ” from the German herbal book Gart der Gesundheit (1485) (This is not a recognisable species)

Fig. 12.13 The operculum of shells as described by Gesner, sixteenth century (Courtesy of Hava Noverstern, curator of the Edelstein Collection, National Library of Israel)

A sea snail by the name of Blacte bizantia is described as a synonym of the aromatic claw Ungula aromatica, in a book of medical plants dated 1485 (Fig. 12.12 ). The snail was imported from India and its high-quality perfume originated from the odorous plant Nardostachys grandiﬂ ora (spikenard), on which the snail would feed. The snail was collected during the summer (‘when the water evaporates because of the heat’) and when its operculum was roasted, it gave out a scent ‘as strong as the scent from the glands of a beaver.’ This scented smoke served, in those distant days of 500 years ago, as a remedy against epilepsies and for cleaning the uterus after giving birth; and powdered operculum of the snail, when inhaled together with acid, would cure those suffering from diseases of the spleen. During the Renaissance Guillaume Rondeletus (1507–1566) of southern France referred to the operculum of purple-producing snails as Blatta byzanthia ; and the swiss naturalist Konrad Gesner (1516–1565), in discussing the nomenclature of the operculum, wrote (Fig. 12.13 , here in loose translation from Latin-Greek) that “The operculum of Purpura Bibliography 305

(according to Rondeletiu) is Blatta Byzantion or Byzante, as it should more properly be named. The real Blatte Byzantium Arabum does not differ from the operculum of shells. Our pharmacists use the operculum of the Buccinorum shell and they sell it under license, under the name of Blattas Byzantias . The opercula of Buccinorum are round, whereas those of Blattas Byzantias are elongate. Onychem , as described by Diosccorides, is currently named Unguem of the shell because its shape resembles the claw of a raptor bird… Another group, Concha integra and which resemble Onyx , are named Dactylus ”. In the seventeenth century a Jewish scholar Avraham Ben David noted that the term Blatte in Greek refers to “a sea animal called Porphyra and this is the snail by which tekhelet is dyed”. In the eighteenth century, the Swedish naturalist Carl Linnaeus wrote in his Systema Naturae, while describing sea snail species: “ Unguis odoratus est operculum Muricum Purpurarum s. frondescentum”, meaning ‘an odorous claw from the operculum of the purple murex’. I do not know what snail species Linnaeus had in mind, but this sentence expresses the link between a claw and the odorous operculum of some sea snail, and perhaps also the biblical shekhelet .

Bibliography

Amatius P (1784) Libellus de Restitutione Purpurarum, 3rd edn. G. Blasinii, Cesena Aristotle (1907) The history of animals (trans: Thompson D’AW). John Bell, London Bakhrach YH (1982) (from 17th century script) Source of life. Makhon Yerushalayim, Jerusalem (Hebrew) Ben David A (1612) Shields of the mighty. Mantua (Hebrew) Canals MJP (1779) Memorios Sobre la Púrpura de los Antiguas, Restaurada en España que de Orden de la Real Junta General de Comercio, y Moneda se Dan al Público. B. Roman, Madrid Cole W (1685) A letter from Mr William Cole, member of the Bristol, to the Phil. Society of Oxford; containing his observations on the purple-fi sh. Philos Trans 15:1278–1286 Dedekind A (1898, 1908, 1911) Ein beitrag zur Purpurkinde. Mayer and Müller, Berlin Doumet J (1980) A study on the ancient purple colour. Impremière Catholique, Beirut Gage T (1655) A new survey of the West-Indies. J. Sweeting, London Juan DJ, de Ulloa A (1748) Relacion Historica del Viaje a la America Meridional. A. Marin, Madrid Koren ZC (2005) The fi rst optimal all-Murex all-natural purple dyeing in the Eastern Mediterranean in a millennium and a half. J Dyes Hist Archaeol 20:136–149 Koren ZC (2008) Archaeo-chemical analysis of royal purple on a Darius 1 stone jar. Microchim Acta 162:381–392 Longo O (1998) La Porpora. Instituto Veneto di Scienze, Lettere et Arti, Venice Naegel LCA (2004) Plicopurpura pansa (Gould, 1853) from the Pacifi c coast of Mexico and Central America: a traditional source of Tyrian purple. J Shellfi sh Res 23:211–214 Plinius the Elder G (Pliny) (1956) Natural history, English edition (1956) (trans: Page TE). Harvard University Press, London, pp 77–82 Scott P (2006) Millennia of Murex. Saudi Aramco World 57:30–37 Spanier E (1987) The royal purple and the biblical blue, argaman and tekhelet. Keter, Jerusalem Squier EG (1852) Nicaragua: its people, scenery, monuments, and the proposed interoceanic canal. Longman, Brown, Green and Longmans, London Chapter 13 Sacred Sounds from Sea Shells

Abstract In Greek mythology, Triton blew Charonia trumpets to terrify giants during battles between them and the gods. Another myth tells how Tyrrhenus and his companions would feast on human fl esh, so people fl ed and nobody came to a funeral when a comrade had died. Tyrrhenus avoided this by blowing a shell trumpet, thereby declaring they now intended not to devour them. In line with this myth, Romans depicted shell trumpets in tombs and sarcophages. The Chavín culture in Peru (1500–300 BC) blew Lobatus galeatus trumpets in rituals in which shell trumpets would blast around people from unseen directions as they walked through dark labyrinths. The Aztecs of Mexico (1325–1521 AD) used Lobatus gigas as trumpet shells. Quetzalcoat, God of Dawn and rising Venus, created Man by travelling to the underworld and retrieving human bones of previous worlds. The God of Death would give him bones on condition that Quetzalcoatl encircled the underworld four times, blasting from a shell. [A perhaps missing text: without drilling holes in it, without blowing it himself.] Quetzalcoatl turned the shell into a trumpet by calling worms to drill holes into it, and by calling humming bees to enter it and make it roar. He then shed blood from wounds he infl icted on himself on the retrieved bones, thereby spawning Man. Aztec priests blew shell trumpets fi ve times a night to call people to the bloodletting rites.

Keywords Trumpet ancient culture • Trumpet ancient civilisation • Trumpet ancient Greek • Sacred trumpet shell • Trumpet Aztec • Trumpet Charonia • Trumpet Lobatus • Trumpet Maya • Trumpet • Triplofusus

Sea snail shells have served as raw material for the production of wind instruments since ancient times, in both the Old World and the New. Their use in sacred rites is known from legends, artifacts found in archaeological sites and written eye witness reports. The trumpet’s shell Charonia (Fig. 13.1 ) is among Man’s earliest wind- instruments and its use as a trumpet dates back to the Neolthic (of Italy) some 6,000 years ago, as indicated by the presence at archaeological sites of whole shells with their apexes intentionally removed. Many of these shells have been found near

Fig. 13.1 Trumpet, Charonia tritonis (20 cm), Indo-Paciﬁ c

human bones, giving us reason to suppose that they were blown in connection with Neolithic religious rites. In Greek mythology Triton, one of the sons of the great sea-god Poseidon, carried a shell that served him as a trumpet. Triton had the head and trunk of a man and the double tail of a ﬁ sh, and would ride the waves on horses and on sea monsters, blowing his trumpet to calm a storm, or to cause retreat of a ﬂ ood. Triton blew his shell trumpet also as a war-cry during the great battle between the gods and the giants to terrify the giants, and the loud blast would roll from one corner of the sea to another. Coins minted in Sicily at circa 400 BC show Triton about to blow a trumpet shell held in his two hands (Fig. 13.2 ). 13 Sacred Sounds from Sea Shells 309

Fig. 13.2 A coin from Sicily, 425–406 BC: triton blowing a trumpet shell

Fig. 13.3 Seal from Crete, 1600–1400 BC: a priestess blowing a trumpet shell, over a horned altar (Based on Younger 1988 )

Greek mythology also tells about the king of Crete, who once offered a gener- ous prize to the person who would succeed in taking a cord of fl ax through the whorls of the trumpet shell, from apex to aperture, without use of his hands. The eventual winner was a man who fi rst drilled a tiny hole into the apex of the shell; then stuck a spider’s thread onto an ant’s foot; then lowered the ant through the hole; while smearing a thin layer of honey around the shell aperture, so the sweet smell would tempt the ant to continue its journey; and fi nally, when the ant appeared in the aperture with the spider’s thread dangling from its foot, he attached the cord of fl ax to the spider’s thread thereby letting the ant pull it through the shell. Figure 13.3 shows a seal from Crete (1600–1400 BC) presenting a priestess blowing a trumpet shell over a horned altar. Remnants of trumpet shells have turned up at sites of ancient Hellenic civilisations in Greece and its islands and in countries around the Mediterranean; in Israel they have been found in several Philistine sites from circa 1100 BC. Triton blowing a trumpet was a common motif also in Roman culture. In another Greek myth it was Tyrrhenus, son of Hercules, who fi rst invented the shell trumpet. As he and his comrades had the habit of feasting on human fl esh, people would fl ee from them. Consequently, when one of the comrades died, nobody would come to attend his funeral. To avoid this, when any of the comrades died Tyrrhenus would blow a shell trumpet, thereby declaring that they were burying a deceased, had no intention of devouring anybody, and all people are invited to the funeral (Hyginus, Fabulae 274). The Romans, in line with this myth, frequently depicted shell trumpets in tombs, sarcophages, monuments and other funeral contexts. They seem to have believed in the existence of tritons, for Pliny 310 13 Sacred Sounds from Sea Shells

Fig. 13.4 Lobatus galeatus (15 cm), eastern Paciﬁ c

(23–79 AD) writes that “An embassy from Lisbon sent for the purpose reported to the Emperor Tiberius that a Triton had been seen and heard playing on a shell in a certain cave, and that he had the well-known shape” ( Natural History Book 4: 4). From the Rennesaince onwards, Tritons blowing shell trumpets are a frequent motif in Italian art. Shells other than Charonia were used as trumpets among ancient cultures of southern and northern America. The Chavín culture of ancient Peru (dating back between 1500 and 300 BC) used Lobatus galeatus as trumpets, a tropical species up to 21 cm living off the Pacifi c coasts from Ecuador to Costa Rica (Fig. 13.4 ; formerly Strombus galeatus). In order to convert a shell into a trumpet, they fi rst culled its apex and then ground or polished the resulting opening. Each shell- trumpet was additionally modifi ed with a characteristic V-shaped notch, carved into the opening of the shell and thereby changing its sonic qualities. Some trumpets were also engraved with elaborate patterns. Chavín de Huántar, the major 13 Sacred Sounds from Sea Shells 311 temple complex of the Chavín culture, consists of a number of temples honey- combed with underground corridors, staircases, shafts, and drains. This carefully constructed stone-walled underground architecture with its twisting tunnels, hidden alcoves and ventilation shafts, form a unique acoustic construction with very unique sonic characteristics, where the source of a sound is diffi cult to localise. It was here, in this underground labyrinth, that the Chavín people conducted religious rituals. By blowing into the giant conch shells, high priests of this culture produced thunderous sounds with eerie distortions, created as the sound travelled through the twists and turns of this structure, greatly amplifi ed by a deep tonal resonance. Within the complex maze, the trumpeted conch shells created the dis- orienting impression of sounds coming from several different directions at the same time. There is evidence at Chavín de Huántar of the use of psychoactive drugs, derived from a native plant (Echinopsis pacchaoni , the san-pedro cactus). A religious ritual would have begun, most likely, by taking a hallucinogenic drug. Then, as the Chavín subjects walked through the dark, cramped halls of the temple, the sound of shell trumpets echoed around them from some unseen source; water poured through channels beneath their feet (or overhead) produced a thundering noise, amplifi ed by the effect of the drugs. Mirrors placed in ventilation ducts to refl ect the sun poured brilliant shafts of light into the subterranean hallways, only to be “turned off,” thrusting the occupant into complete darkness. By putting worshippers through these terrifying ritual experiences, Chavín priests convinced their followers that they, the Chavín priests, had supernatural powers and authority. Conch trumpets were used also by the Inca of Peru (1400–1525 AD) who named them ‘Huaylla quepa ’. They differed from the Chavín trumpets in that a mouthpiece of metal or cane was sometimes fi tted into the perforated shell apex. The pitch of the sounds produced by these shell trumpets could be changed by introducing and alter- ing the depth of the hand in the shell aperture. The Inca decorated their shell trumpets with turquoise stones, or polished them and engraved ceremonial motifs on them. As the Andes-dwelling Inca had to obtain the shells for their trumpets through trade, conch shells were often imitated by creating ceramic ones. Trumpet shells were abundantly used by imperial runners (chasquis ), each of whom carried a conch trumpet to announce his arrival; and they were used also by military chiefs, by high priests and clergy. Shell trumpets were also blown to gather people and assemble them on important issues, and also served as emergency notes. In the late eighteenth century, following the revolt of Tupac Amaru II, the Spanish rulers of Peru banished the use of shell trumpets; however, today named ‘ pututu ’, they still continue to be blown in some remote villages of Peru. Shell trumpets were also widely used in North America. In Mexico they were means of audible communication with the supernatural realm, as they were able to call on specifi c gods, or on the spirits of ancestors, and they played a major role in priestly ceremonies for centuries (Fig. 13.5 ). During Mexico’s Classical period (100 BC to 600–700 AD; Teotihuacan and Tetitla being the main archaeological sites) shell trumpets made of the buccinoideans Triplofusus princeps and Triplofusus 312 13 Sacred Sounds from Sea Shells

Fig. 13.5 Mexico, a priest carrying a trumpet shell (Based on Fuente 1996 ) giganteus (Figs. 13.6 and 13.7 ; formerly Pleuroploca princeps and P. gigantea ) were found, as were also shell-shaped ceramic trumpets. Ceramic mouth-pieces were attached to these shell instruments, with bee wax or with gum resin glue, in order to allow a more precise playing technique. Some shell trumpets were adorned with long green feathers representing the iridescent tail plumes of the sacred Quetzal Bird Pharomacros mocinno. The precious feathers, obtained through long distance trade reaching southwards as far as Guatemala, were glued to the shell’s lip and siphonal canal, and probably represented the crest and tail of a supernatural bird. Shell trumpets with mouthpieces and feather decoration were sculpted on monumental stone reliefs on the entrance to temples, and were a common motif in murals. One mural of the Classical period presents shell trumpets with sound scrolls and water sprouts, fl anking a male deity (Tlaloc ?) who holds a water lily (Nymphaea odorata ) in his mouth, as a symbol for terrestrial water, cyclic regeneration and life. Shell trumpets were indeed played in processions dedicated to the god of water and fertility. Another mural presents priests as jaguars blowing shell trumpets; each priest holding a shell trumpet in its left paw, from which three drops of a precious liquid (blood?) are dripping. In centuries to come, among the Aztecs (mentioned further on) the sound of the shell trumpet would represent the roar of the jaguar, as an echo of some remote past. The use of shell trumpets in ritual human sacrifi ce is indicated in a mural presenting a priest carrying a shell trumpet with a mouth piece and decorated with feathers, with symbolic signs of sound emitting from both the aperture and mouth piece, as well as from the priest’s mouth (Fig. 13.5 ). Nearby murals present priests dancing with sacrifi cial knives in their hands, and a proces- sion of felines devouring human hearts. During the Maya culture of Mexico (150–900 AD) shell trumpets were made predominantly from Triplofusus gigantea and decorated with incised portraits, cir- 13 Sacred Sounds from Sea Shells 313

Fig. 13.6 Triplofusus principes (23 cm), Peru

cular symbols, glyphs and hieroglyphic inscriptions. One or two fi nger holes were drilled into some shells to allow a precisely fi xed pitch; and small holes were drilled into the siphonal canal and lip of the shell, in order to enable suspension of the shell trumpet from the neck or arm. One of the excavated shells represents Uc-Zip , the Maya god of hunting. The body of the shell forms his head and headdress, his nose is formed by one of the spines and the right eye is represented by one of the fi nger holes. The second fi nger hole is held by an incised fi gure sitting on a throne, at the centre of the moon sign. The fi gure, named Balam U-Xib (“Jaguar Moon Lord”), represents one of the twin brothers who, in Maya culture, defeated the lords of the underworld, and then became the moon. 314 13 Sacred Sounds from Sea Shells

Fig. 13.7 Triplofusus giganteus (26 cm), south east USA

Serpents were important in the Mayan religion. Och-Chan , the Vision Serpent, was called upon in bloodletting vision rites in which participants would communi- cate with ancestors or gods. In these visions the god who was being contacted would emerge from the serpent’s mouth. Shell trumpets were also closely related to Bacab , one of the four old gods of the underworld who held up the sky. In a scene on a vase from Guatemala, Bacab is being pulled out of the shell and sacrifi ced. With this ceremony the Lords of the Underworld were defeated, and the eventual creation of 13 Sacred Sounds from Sea Shells 315 humankind was made possible. Trumpet shells were ritually killed and then offered to the gods and the opening of the shell by means of a sacrifi cial knife of stone, may have symbolised the killing of Bacab . A painting from the period of the Maya shows a naked shell trumpet player, with a perforated penis, playing in the presence of spear-carrying warriors and their cap- tives in a rite of victory (Kerr 1989 –1997, vol. 1: 57). The conceptual analogy between war and the hunt is demonstrated by the illustrations of successful hunters sounding shell trumpets in processions, while bringing home their prey. During the Aztec culture (1325–1521 AD) trumpet shells were often made of the queen conch Lobatus gigas (formerly Strombus gigas ), and generally they were not ornamented. They were found in excavations along with objects associated with Water, the Earth and the Underworld, and also with material related to sacrifi cial rites such as human skulls, bloodletting bones and sacrifi cial knives. These shell trumpets were most probably associated with Tlaloc, the Aztec god of rain and fertility. Trumpet shells also appear in several Aztec myths. Emphasizing the importance of shell trumpets in Aztec ceremonialism, a monumental (87 cm long) votive stone sculpture of a queen conch with perforated apex, was found on an altar near a Temple. No other votive representation of a musical instrument of that size has ever been found. In Aztec cosmogony, the shell trumpet came from the underworld and was brought to our world by Quetzalcoatl (“feathered serpent”), God of the Dawn and of Venus. The Aztecs believed in four previous worlds (‘suns’) which were destroyed by fl ood and fi re; our current world is the fi fth sun. Quetzalcoatl , after having restored the sky and earth, decided to create people to inhabit the new world. He travelled down to the underworld to retrieve the bones of humans of previous worlds, so that he would create our (fi fth-world), mankind from them, when mixed with his own blood. Mictlantecuhtli , God of Death and Lord of the Underworld, agreed to give up the precious bones on condition that Quetzalcoatl would travel around the underworld four times, while sounding blasts from a shell that he would supply him. [In my personal opinion, at this point a missing text would have mentioned two further conditions: that Quetzalcoatl was not permitted to drill holes in the shell, nor permitted to blow the trumpet himself]. Quetzalcoatl turned the shell into a trumpet by calling upon worms to drill holes in the shell, and he made it sound by calling upon humming bees to enter the trumpet and make it roar. Having completed this task, Quetzalcoatl grinded the bones into powder, shed some drops of his own blood on them from wounds he infl icted on his earlobes, calves, tongue, and penis; and this addition of blood imbued the bones with new life – and spawned the peoples of today. In another myth Quetzalcoatl had to play the shell trumpet four times in all directions around the precious circular greenstone [i.e. the centre of the world]. This metaphor represents a mythological explanation according to which the trumpet had to be played towards the four cardinal points and in addition towards the centre of the world, to obtain a positive result of the ritual. 316 13 Sacred Sounds from Sea Shells

One of the most important functions of the shell trumpet was its use, by specialised priests, fi ve times during the course of the night, to call to the bloodletting rites and also to announce the rising of Venus. Queen conches were played by priests in processions dedicated to different deities, such as Chalchiuhtlicue , the goddess of terrestrial water, or Xochipilli, the god of hallucinogenic plants, music and dance. During the ceremony in honour of Tlaloc , shell trumpets and copper gongs were struck and played in the course of ritual cleansing. Trumpet shells were blown by priests during the offering of incense in the Teteo-Eco ceremony, as a sign that gods had arrived, and during the ritual sacrifi ce of Chalchiuhtlicue , as an announcement that her heart was being offered to the gods. Shell trumpets were also played in battle as a sign instrument and a noise-maker to terrify the enemy. Pitch modulation may have been achieved by inserting the right hand into the shell. Shell trumpets are still played by some ethnic groups in Mexico. Reports about the Huichol of western Mexico from 1898 describe their sowing ceremony, held shortly before the summer rainy season. “When the heap of tamales is dedicated to the gods by the shamans, some of the people are appointed to blow into such shells fi ve times in the daytime and fi ve times at night. This is done as a signal to all the gods. After the feast, the shells are carried to Mesa del Nayarit, where they remain through the wet season, to be afterwards brought back again for the next ceremony of the same kind…. According to tradition, the Chichimecas brought them fi rst from the part of the coast where San Blas is today”. The spiral of the shell symbol- ises the wind, specifi cally the god Nia’ariwame , the “Rain Serpent”. Among the Huichol one of the men, considered to embody the god of the wind, blows the shell trumpet to invite the gods to join the sowing ceremony. This is done after a bull is sacrifi ced and a ceremonial stick with burning fl owers is directed to the fi ve wind directions. Reports from 1907 about another ethnic group, the Lacandon of tropical forests of eastern Chiapas in southern Mexico, describe their use of the queen conch Lobatus gigas (Fig. 13.8 ) in the renewal rite of incense burners. Before the ritual feeding of the defi ed burners is carried out, the leader of the ceremony “goes to the eastward of the hut, and blows fi ve long blasts on the conch shell, thus calling the gods to come in person.” The sound of the shell trumpet consequently gives life to the sacred incense burners and the ceremonial drum, indicating a close relation to creation and cyclical regeneration. In conclusion, the shell trumpet has a long, very eventful history in various cultures of the Mediterranean and in prehispanic and present America. Bibliography 317

Fig. 13.8 Lobatus gigas (16 cm), Bahamas

Bibliography

Abel JS, Rick JW, Huang PP, Kolar MA, Smith JO, Chowning JM (2005) On the acoustics of the underground galleries of ancient Chavin de Huántar, Peru. In: Proceedings of the acoustics 2008, Paris, pp 4167–4172 Both AA (2004) Shell trumpets in Mesoamerica. In: Hickmann E, Eichmann R (eds) Studien zur Musikarchäologie 4. Leidorf, Rahden/Westfalen, pp 261–277 Fuente B (1996) La Pintura Mural Prehispanica en Mexico: Teotihuacan, 2 vols. Universidad Nacional Autonomia de Mexico City, Mexico City Hyginus (1960) The myths of Hyginus, Fabulae 274 (trans: Grant M). Kansas University Press, Lawrence 318 13 Sacred Sounds from Sea Shells

Kerr J (1989–1997) The Maya vase book. A corpus of rollout photographs of Maya vases, 5 vols. Kerr Associates, New York Rick JW (2005) The evolution of authority and power at Chavin de Huántar, Peru. Archaeol Pap Am Anthropol Ass 14:71–89 Skeqtes R (1991) Triton’s trumpet: a neolithic symbol in Italy. Oxf J Archaeol 10:17–31 Younger JG (1988) The iconography of late Minoan and Mycenaean sealstones and ﬁ nger rings. Bristol Classical Press, Bristol Chapter 14 Sexual Perversions

Abstract An important human-induced change in sea snails in recent decades concerns the rapid spread of pathological disorders within populations, causing them to cease reproduction. Named ‘imposex’, these disorders are expressed in females by growth of a male system which blocks the outlet of the female tract, thereby preventing both copulation and egg laying; thus, these females become sterile. Imposex results from widespread use of Tributyltin (TBT), an antifouling compound in paints for boats and harbour installations, which disrupts the hormone system of sea snails. It induces also another hormonal disorder, ‘inter-sex’, in which the female tract is transformed into a non-functional prostate gland, and she too becomes sterile. Imposex is currently known in over a 100 sea and freshwater snail species. A worldwide ban on TBT was introduced in 2003, and today many sea snail populations formerly suffering from high imposex levels are recovering.

Keywords Imposex • Intersex • Marine pollution • TBT gastropod effects • Tributyltin gastropod effects

Human activity has brought about many changes in sea snails in recent decades; an important one is the rapid spread of pathological and morphological changes within populations of a single species, causing them to cease reproduction. At ﬁ rst, these changes cause extinctions only at local levels, but the combined affect of many local extinctions may eventually lead to extinction of an entire species. These pathological changes, occurring today throughout the world, were ﬁ rst discovered among the dog-whelk Nucella lapillus , a predatory sea snail (Fig. 14.1 , family Muricidae) found in the North Atlantic. Normally this genus, as other genera of its family, has separate sexes and the male is easily recognised by his large penis, aligned along the right side of his body. In the 1970s, a very strange phenomenon was discovered in Plymouth, England: some dog-whelk females were found to also possess a rudimentary penis. It was obvious that this pathological phenomenon was caused by some toxic matter in the seawater that had a disrupting effect on the snails’ hormone system. The phenomenon itself was named ‘imposex’, as the entire female genital system was conserved but had been superimposed by male organs. Since this early observation, the extent of snails suffering imposex in Plymouth and along many other shores in the United Kingdom soon became far more severe: whereas the extent of imposex in the

Fig. 14.1 Nucella lapillus (5 cm), northern Atlantic

Plymouth population in 1970 was less than 5 %, by 1978 it had already reached 67 %. It was found that imposex resulted from the widespread use of Tributyltin (TBT), an active antifouling compound used in preparing paints for yachts, boats, ships and harbour installations. It is used also as a biocide in wood preservatives, textiles, agricultural pesticides and as an anti-ultra-violet mechanism in many plas- tics. The increase in the leisure culture of modern days has caused an increase in the number of yachts and speedboats, followed by an increase in the number of marinas in which these vessels are maintained and painted. It is this maintenance and painting that has caused a sharp increase in TBT concentrations in littoral and offshore seas. The disruption in the sea snail’s hormone system is expressed by the growth of a masculine system in the female: at fi rst the fl oor of the mantle forms a short gutter near the female genital opening which soon closes into a rudimentary sperm duct; a rudimentary penis develops near the right tentacle; the sperm duct then lengthens and grows forward until it reaches the base of the rudimentary penis, which in turn rapidly grows to dimensions of a large penis as in normal males; fi nally, a malignant growth is formed at the base of the sperm duct that blocks the outlet of the egg duct (Fig. 14.2 ). Such an imposex female still produces ovules in her gonad but cannot copulate or lay eggs because her female genital duct is blocked, and she is thus doomed to sterility. TBT has impacts not only on dog-whelks, and imposex is currently known in 116 sea and fresh water snail species worldwide. While TBT-contaminated water induces imposex in dog-whelk females, it may induce a different hormonal change, termed ‘inter-sex’, in other species. This condition is only documented in the periwinkle Littorina littorea found on north-eastern Atlantic shores (Fig. 14.3 ). Inter-sex is characterised by a phenotypic disturbance of 14 Sexual Perversions 321

Fig. 14.2 Stages in imposex. The mantle has been removed, to expose the front section of the egg duct and neighbouring organs ( a) A normal female; (b) A female in which a sperm duct is present in the opening of the female genitalia and grows forwards; ( c ) A female in which there is a penis at the front of the body; ( d) A female in which the sperm duct has connected to the penis; (e ) A female in which tissues grow and block the female genital opening; the egg capsules do not have an exit and are reabsorbed into the body (Based on Gibbs and Bryan 1986 )

Fig. 14.3 Periwinkle Littorina littorea (3 cm), northern Atlantic

sex determination between the gonad and the genital tract, with the female sea snail undergoing a gradual transformation of its oviduct into a non-functional prostate gland. During this transformation, the female genital opening is fi rst enlarged by a proximal slit, and the pouch in which it receives sperm (‘ bursa copulatorix’, Sect. 8.1) is opened; later the whole oviduct is opened, exposing the internal lobes; then 322 14 Sexual Perversions the pallial oviduct glands are partially or totally supplanted by a prostate gland; and fi nally, a penis and a seminal groove are developed. The female becomes sterile, both because eggs and capsular material leak into the mantle cavity and because she now lacks the glands for the formation of the egg capsules; needless to say, she produces no sperm. Inter-sex and imposex are irreversible pathological and morphological develop- ments occurring in both marine and freshwater snails. Even if the affected dog- whelk females are kept under TBT-free conditions for long periods, once an imposex stage is attained it cannot be returned to its former normal condition. However, although the ultimate effect of both imposex and inter-sex is the sterilisation of individual females, there are differences between dog-whelk and periwinkle female sterility at the population and the ecosystem levels. The dog-whelk Nucella lapillus produces benthic egg capsules and the offspring complete their development within the capsule, hatch and crawl onto the shore without undergoing a pelagic larval stage. Because of the absence of this pelagic dispersal stage, dog-whelk populations are confi ned to localities and will die out if all females in a population become ster- ilised. Periwinkle sterilization due to inter-sex development does not necessarily lead to local extinction, because this species has egg capsules and planktonic larvae which are able to disperse; therefore, un-affected periwinkles from other populations can contribute to local survival, even in highly contaminated areas. Furthermore, periwinkles are far less sensitive to TBT than dog-whelks, and inter-sex sterility develops only under TBT concentrations ten times higher than those which cause imposex in dog-whelks. As both imposex and inter-sex are irreversible conditions provoking female sterility, many TBT-affected estuarine and coastal gastropod populations declined considerably or even became extinct over the last decades. These devastating effects of TBT as an antifouling agent led to banning its use on boats less than 25 m long in Europe, USA, Canada, Australia, New Zealand, Japan and Hong Kong during the late 1980s and early 1990s. A worldwide ban by the International Maritime Organisation followed in 2003. It is encouraging that in very many areas where coastal TBT concentrations could be reduced by legislative actions, sea snail populations formerly suffering from high imposex levels have rapidly recovered.

Bibliography

Gibbs PE, Bryan G (1986) Reproductive failure in populations of the dog-whelk Nucella lapillus , caused by imposex induced by tributyltin from antifouling paints. J Mar Biol Assoc UK 66:767–777 Oehlmann J, Bauer B, Minchin D, Schulte- Oehlmann U, Fioroni P, Markert B (1998) Imposex in Nucella lapillus and intersex in Littorina littorea : interspeciﬁ c comparison of two TBT-induced effects and their geographical uniformity. Hydrobiologia 378:199–213 Glossary

Albumen nutritious matter surrounding an embryo. Amphidromy a life cycle in which a freshwater larva migrates seawards and live for a while in sea water; eventually it returns to freshwater where it metamorphoses, matures, and reproduces. Aperture the shell opening through which a snail emerges when active. Apex the fi rst formed, upper end of a shell; it is formed in the egg during embryonic development. ATP (Adenine-5′-tri-phosphate) a molecule able to store and transport energy within cells. Axis an imaginary line between the centre of the apex and the left lip of the aperture, around which the shell is coiled. Bilateral Symmetry when the body’s left side is an almost exact mirror image of the right side. Body whorl the last and lowest complete coil of the shell immediately above the aperture, containing most of the body of a snail. Breathing tube in many sea snails, a pipe or tube for drawing water into the mantle cavity; scientifi cally termed siphon . Bristle worms Polychaeta; an animal phylum in which the body usually possesses short external bristles, and is divided into a series of cylindrical segments. Brood pouch a body cavity inside which eggs develop, either to advanced embryos or to adult form. Bursa copulatorix a sperm-accepting pouch in the female genitalia. Bursicle in gill leafl ets of Vetigastropoda, a pouch lined by chemo-sensory receptors. Calcareous made of calcium carbonate, chalky. Callus a ridge of pale shell matter that sometimes coats part of the shell. Cerata in Opisthobranchia, fi nger-like extensions of the back containing ramifi cations of the digestive system and functioning in digestion, respiration and defence (single: ceras ). Chloroplast a green cellular organelle that enables plant cells to convert sunlight into energy, in a process named photosynthesis.

Cilium a hair-like organelle in some cells, sometimes capable of undulating movement (plural: cilia ). Cirrus a slender appendage of the body, often resembling a tentacle (plural: cirri ). Class a natural group of organisms consisting of one or several orders and belonging to a higher classifi cation, the phylum. The class Gastropoda belongs to the phylum Mollusca. Cnidophage in the Opisthobranchia, a cell in the digestive system engulfi ng and storing cnidarian nematocysts (=stinging-capsules); also an engulfi ng-cell . Cnidosac in Opisthobranchia, a sac in the uppermost part of the branch of the digestive system inside a ceras, the cells of which contain stinging cells originating from the cnidarian food of the sea slug; also sting-sac . Coiled to the left (sinistral) a shell in which the aperture is on the left of its axis, when the shell is held with its apex pointing upwards and the aperture faces the observer. Coiled to the right (dextral) a shell in which the aperture is on the right of its axis, when the shell is held so that its apex points upwards and the aperture faces the observer. Columella a calcareous pillar, solid or hollow, that surrounds the imaginary axis of a coiled shell; it is formed by the inner walls of the whorls. The lower part of the columella forms the columellar lip of the aperture. Columellar lip that part of the aperture formed by the lower part of the columella. Consecutive hermaphrodite an organism having functional male and female reproductive organs which mature at different times (either the male organs mature fi rst or the female organs). Corneous made of chitin, a non-calcareous substance. Crystalline rod a soft, continuously rotated rod located in the stomach of some snails, containing digestive enzymes; also termed crystalline style . Detorsion Following initial torsion (rotation through 180°) of the internal organs, which occurs in the larvae of all gastropods, detorsion is the rotation of the internal organs of the larvae of certain gastropods through 90° or 180°, back towards their initial position. Direct development a mode of embryonic development in which the complete larval cycle takes place inside the female’s body and the young, emerging from their mother’s body, resemble miniature adults. Egg a fertilised female gamete (ovule). Epipodium in Vetigastropoda, a fold of the body wall along the upper margin of the foot, frequently bearing many sensory structures. Family a natural grouping of organisms consisting of one or several genera and belonging to a higher group, the Order. Fauna the list of the animal or plant groups in a given geographical area. Genus a natural group of organisms consisting of one or several species and belonging to a higher group, the family. Gill a respiratory organ. Growth lines Surface markings left in older positions of the outer edge of the aperture. Glossary 325

Haemolymph The circulatory fl uid of molluscs, and also of such other invertebrates as arthropods. Hermaphrodite An animal with both male and female reproductive organs. Home scar a pit on intertidal rocks into which a snail fi ts closely and to which it returns after foraging. Hypobranchial gland a gland in the roof of the mantle cavity, of as yet unclear function. Inhalant current the stream of water entering the mantle cavity; exhalent current leaves the mantle cavity. Larva an embryo capable of independent movement. Leiblen’s gland a gland of the oesophagus secreting enzymes that break up proteins in some predatory snails (e.g. Buccinoidea, Muricoidea). Lichen a symbiotic association of a fungus with a partner (a green alga or cyanobacterium) which can produce food for the fungus from sunlight. Lip a thickened part of the aperture in the adult shell of some snail species. Littoral intertidal zone of the sea shore. Mantle the skin that secretes the shell. Mantle cavity The space between a snail’s mantle skirt and its body; in pulmonates it is closed into a sac-like structure and serves as a lung. Metamorphosis the abrupt change from larval to adult morphology. Mother-of-pearl a shell layer, or the inner lining of a shell, displaying a pearly (nacreous) surface. Mucus a slimy secretion of the body. Nematocyte in the Cnidaria, a cell in the skin containing a nematocyst (=sting-capsule). Odontophore a cartilaginous cushion beneath the radula and over which the radula glides when extruded. Opaline gland in the Opisthobranchia, more particularly the Anaspidea, a gland in the mantle cavity that secretes a milky substance of defensive signifi cance. Operculum a corneous or calcareous disk on the back of the foot of some snails, that seals the aperture when the snail withdraws into its shell. Oral veil a membrane extending above the mouth. Order a natural group of organisms consisting of one or several families and belonging to a higher group, the Class. Osphradium an organ inside the mantle cavity, which senses the chemical quality of the incoming respiratory current. Outer lip that part of the aperture that reaches from the suture to the base of the columella. Ovule an unfertilised female gamete. Pallial oviduct that part of the oviduct formed by the mantle fl oor. Pallial sperm duct that part of the sperm duct formed by the mantle fl oor. Papilla a structure resembling a nipple (plural: papillae ). Parapodia in some Opisthobranchia, a pair of fl eshy fl aps on either side of the body, rising from the foot (single: parapodium ). 326 Glossary

Parasite An organism (typically small) that lives on or inside another organism (typically much larger and termed a host) from which it obtains food without killing it. Parasperm large sterile cells formed in the testis and which may perhaps nourish fertile sperm or eggs, or transport them to the female, or contribute to sperm competition. Parthenogenesis a form of asexual reproduction found in females, where growth and development of embryos occurs without fertilisation by a male. Pericardium an epithelial sac surrounding the heart. Periostracum a layer of horny protein that covers the calcareous shell of some species. Pharynx the part of the gut immediately behind the mouth cavity. Phylum a natural group of organisms consisting of one or several classes and belonging to a higher group, the Kingdom. The phylum Mollusca belongs to the Kingdom Animalia. Polychaeta bristle worms; an animal phylum in which the body usually possesses short external bristles, and is divided into a series of cylindrical segments. Proboscis a tubular protrusion from the front of an animal. Protoconch those whorls of the shell formed in the egg during embryonic development; in hatched snails they form the apex of the shell. Pseudoconch in certain Opisthobranchia, a large mass of jelly substance fi lling the space between arched fl aps protruding from the body and which adds to the snail’s buoyancy. Pseudoproboscis in certain gastropods (Capuloidea) a modifi ed, movable elongation of the lower lip used for feeding. Radial symmetry when body organs are an exact counterpart on any radius around a central axis. Radula a tooth-bearing fl exible membrane in the oral cavity that rasps, licks, or stabs food. Refl ected turned outwards at the margin, referring to aperture edge. Rhinophores paired chemosensory tentacles on the head of many Opisthobranchia. Rhodoplast a plastid found in red algae, containing red pigment as well as chlorophyll Rib a projecting radial (= transverse) ridge on the outer surface of the shell. Sculpture a relief pattern on the shell’s surface. Segment a serially repeating set of organs. Seminal receptacle in some snails, a pouch in the female genitalia close to the gonad, into which sperm from the sperm receptacle is transferred and temporarily stored. Also: receptaculum seminis . Sequential hermaphrodite a type of hermaphroditism whereby an individual is born one sex, and changes sex at some point in its life. This change can be from male to female or from female to male. Shell a hard calcareous structure permanently encasing the viscera, and into which the foot and head may temporarily be withdrawn. Glossary 327

Shell muscle the muscle attaching a snail to its shell and which, upon contracting, withdraws the head and foot into the shell. Shoulder an angle of a whorl, near its upper part. Siphon see breathing tube . Slug a snail in which the shell is internal or lacking. Species an isolated group of interbreeding populations in which individual members resemble each other more than they resemble other groups. Sperm duct a duct through the body that conveys sperm from the testis to the outside. Sperm receptacle a pouch in the female genitalia close to the genital oriﬁ ce, in which sperm from another individual is temporarily stored; also receptaculum seminalis Spermatophore a sperm purse consisting of protein and packed with sperm. Spire all the whorls comprising a spirally coiled shell, except for the last whorl (the body whorl). Sting-sac in certain Opisthobranchia, a sac of the digestive system near the tip of the lobe, into which sting-capsules taken from the prey are placed, stored and nourished, for future use in defence; also cnidosac . Suture in a shell, the continuous spiral line along which successive whorls adjoin. Symbiosis A long-term interaction between individuals of different species that live together in close association. In some sea snails: a close long-term interaction between an individual sea snail and the organelles of another animal or plant species. Torsion the process, in snail veligers, whereby the viscera are twisted around, back-to-front in relation to the head and foot. Trochophore a larva of globular shape, with cilia at its apex and around its equator, and which (in molluscs) eventually develops into a more advanced larva, the veliger. Trunk (proboscis) an elongated, movable appendage of the head terminating in the mouth. Tubercle a knob. Umbilicus the cavity around which a growing shell coils, and which opens at the base of the shell. Veliger an advanced larva unique to molluscs, which develops from a trochophore and which eventually metamorphoses to adult form. It is equipped with large sails, a digestive system and embryonic shell. Velum a large, ciliated sail consisting of one or several lobes, which surrounds the mouth of a veliger. Viscera the complex of digestive, reproductive and excretory organs. Whorl in a spirally coiled shell: one complete coil of the shell around its axis. Zooxanthellae single-celled plants living in the tissue of other organisms where they continue to photosynthesise (single: zooxanthella ) . Index

A Anoxia , 44 Abalones , 32, 60, 66–69, 75, 119, 183 Anthobranchia , 208, 237–242 Acmaea , 43, 44 Aperture , 11, 14, 16, 17, 30, 31, 37, 59, 63, 65, Acteon , 209, 210 67–69, 72, 81, 99–101, 103, 104, Adenine-5′-tri-phosphate (ATP) , 17, 44, 248 107–109, 111, 112, 116, 117, 120, 129, Adhere , 17, 18, 21, 40, 51, 61, 81, 106, 107, 135, 138, 140–145, 154, 159–161, 173, 120, 126, 127, 226 174, 181, 183, 189, 191, 193, 197, 203, Adhesion , 19, 40, 41, 260 204, 209, 226, 227, 233–235, 269, 271, Adhesive , 18, 19, 40, 49, 227, 260 279, 303, 309, 311, 312 Advanced-snails , 32, 41, 79, 89–97, 99, 108, Apex , 13, 26, 32, 37, 50, 59, 61–63, 82, 116, 134, 145, 151–153, 169 160, 248, 249, 307, 309–311, 315 Aeolidia papillosa , 244, 245 Aplysia depilans , 217 Aeolidiella glauca , 249 Aplysia fasciata , 217, 220 Aeolidina , 208, 237, 242–249 Aporrhais , 108 Aeolids , 208, 242–250 Aporrhais occidentalis , 109, 110 Afrolittorina knysnaensis , 128 Aporrhais pespelecani , 109, 110 Air temperature , 43 Archidoris pseudoargus , 240 Akera , 215 Archimediella , 100, 105 Albumen , 30, 76, 84, 92–94, 117, 207, 219, Asymmetric , 32, 58, 59, 73, 259 224, 225, 235, 258, 261 Atlanta , 162, 163 Alderia modesta , 233 ATP see Adenine-5′-tri-phosphate (ATP) Algae(Algal) , 24, 29–31, 44–49, 51, 61, 62, Attachment , 17–19, 41, 44, 45, 109, 117, 120, 68, 72, 81, 93, 111, 113, 117, 118, 120, 127, 162, 163, 170 123–125, 128, 130, 133, 142, 161, 164, Atys , 210 165, 176, 177, 187, 188, 190, 211, 216, Augers , 191–198 217, 219, 220, 228, 230, 231, 235, 245, Austrocypraea , 143 251, 260 Amino acids , 29, 175, 176 Amphibola , 261 B Amphibola crenata , 261 Bacteria , 26, 30, 45, 63–65, 82, 83, 176 Amphidromous , 83, 84 Barnacle(s) , 44, 51, 52, 127, 130, 133, 136, Amphidromy , 83, 84 152, 181, 183, 240 Amylase(s) , 124 Bathynerita naticoidea , 82 Anaerobic , 44 Bellerophontida , 58 Anaspidea , 208, 215–221 Berthella martensi , 236 Anisus , 58 Berthellina , 236, 237

Bilateral symmetry , 4–7, 61, 116, 206, 237 Capsule(s) , 79, 81–85, 92–94, 101, 103, 106, Blasicrura teres , 140, 142, 144 107, 117, 119, 122, 136, 137, 142, 143, Blood , 20–22, 29, 43, 66, 95, 137, 151, 146, 157, 161, 162, 166, 169, 171–173, 160, 175, 176, 178, 179, 182, 190, 177, 189, 190, 195, 197, 207, 219, 225, 206, 216, 217, 232, 241, 243, 258, 246–248, 260–262, 321, 322 262, 268, 301–303, 312, Capulidae , 123 314–316 Capuloidea , 123, 124 Blue , 132, 168, 181, 217, 246, 285–305 Capulus ungaricus , 124, 125 Blue thread , 300, 301, 303 Carbohydrates , 18, 124, 127

Body whorl , 13, 142, 154, 159 Carbon dioxide (CO2 ) , 20, 22, 43, 57, 67, 72, Bolinus brandaris , 184, 286 230, 243, 259 Bonnet(s) , 97, 116–122 Carbonic anhydrase , 41 Boring organ , 160, 174, 180–183, 190, 191 Carboniferous , 52, 83 Born in the purple , 295 Cardiapoma , 163 Breathing pipe , 108, 150, 151, 171, 174 Carinaria , 163 Breathing tube , 111, 141, 142, 146, 150, 154, Carrion-feeding , 175, 176 159, 181 Cartilage , 7, 21, 23, 56, 164, 192 Bromo-indigo , 286, 287, 290, 300 Carychium , 263 Brood pouch , 103, 136, 171 Cassis , 154, 156 Brooding , 51, 76, 107, 136, 141, 171 Cassis madagascarensis , 156 Brush-snails , 32, 55–77, 89, 90, 96 Cavolina , 222, 223, 225, 227 Bubble shell(s) , 208–214 Cellana , 41, 42, 50–52 Buccinoidea , 97, 132, 153, 174–181, 311 Cellulase , 26 Buccinum cyaneum , 177 Cellulose , 26 Buccinum undatum , 174, 177 Cephalaspidea , 208–214 Bulla , 210, 212 Ceras , 242, 247–249, 252 Bullia digitalis , 174, 175, 177 Cerata , 242, 243, 245, 248, 250–252 Bursa , 158 Cerithioidea , 97, 99–103, 123 Bursa copulatorix , 321 Cerithium , 101 Bursicle , 60, 72 Ceriths , 97, 99–103 Buscyon contrarium , 283 Chank , 268, 277–283 Charonia , 158, 159, 307, 308 Chelidonura , 212 C Chemical defence , 103, 218, 236, 240, 260 C. aculeata see Crepidula aculeata Chloroplast , 229–232, 245 C. cribraria see Cribrarula cribraria Chlorostoma , 75 C. funebralis see Chlorostoma funebralis Chlorostoma funebralis , 72, 75 C. geographus see Conus geographus Chromodoris reticulata , 180, 241 C. striatus see Conus striatus Cilia(Cilium) , 17–22, 25–31, 38, 43, 57, 60, C. ungaricus see Capulus ungaricus 63, 71–74, 100, 101, 103, 105, 117, Caenogastropoda , 32, 89, 90, 96, 97, 120, 123, 124, 137, 164, 207, 212, 123, 152, 153 223, 224, 227, 228, 247, 259 Calcium carbonate , 12, 13, 15, 17, 29, 51, 69, Clanculus , 71 75, 82, 95, 116, 141, 162 Clanculus bertheloti , 77 Calliostoma , 72, 76 Class , 9–11, 15, 32, 156, 243 Calma glaucoides , 246 Classiﬁ cation , 24, 31–32, 52, 63, 96–97, Calyptraeidae , 123 104, 258 Calyptraeoidea , 97, 116–122 Clio , 222 Cambrian , 31, 32, 55, 58, 66 Clione antarctica , 228 Cameo , 155–157 Clione limacina , 225, 226 Cancellaria , 178 Clithon , 83 Cantharidus , 71 Clithon retropictus , 84 Index 331

Cnidophage , 248, 249 Creeper(s) , 97, 99–103, 106, 108 Cnidosac , 243, 247–249 Crepidula , 120, 123 Coiling , 13, 15, 17, 28, 29, 31, 32, 50, 52, Crepidula aculeata , 120, 122 57, 58, 60, 63, 65, 66, 68, 69, 80, Crepidula convexa , 122 102–104, 106, 142, 161–163, 222, Crepidula fecunda , 122 241, 261, 262, 283 Crepidula fornicata , 120–122 Collisella scabra , 49 Creseis , 222, 227 Colour , 13, 15, 16, 51, 68, 69, 74, 75, 80, 82, Cretaceous , 66, 100, 149, 150, 161, 191 102, 113, 127, 129–131, 137, 140–142, Cretaceous Extinction , 66 145, 155, 156, 166–169, 206, 210, 211, Cribrarula cribraria , 140 217, 223, 230, 240, 246, 248, 251, 268, Cross lamellar structure , 94, 95 279, 285–287, 289–292, 294, 295, 297, Crucibulum , 116, 117 299–303 Cryptic colouration , 51 Columella , 13, 17, 58, 59, 125, 189, 197, 279 Crysomallon , 60, 63–65 Columellar muscle , 17, 59, 227 Crysomallon squamiferum , 64 Colus stimpsoni , 109, 177 Crystalline rod , 8, 9, 26, 124 Common whelk , 177, 185 Crystalline style , 26 Conch(s) , 97, 108–116, 150, 305, 311, Cup-and-saucer , 97, 116–122 315, 316 Cuthona nana , 244 Conchiolin , 64, 81 Cymatium , 157, 158 Concholepas , 183 Cymbulia , 223 Cones , 13, 29, 31, 32, 52, 57, 66, 68, 97, 116, Cypraea , 139, 143 153, 190–198, 262 Cypraecassis rufa , 156, 268 Conidae , 192, 193, 197 Cypraeoidea , 97, 138–146 Conoidea , 97, 153, 191–198 Consecutive hermaphrodites , 50, 166, 168, 169, 171, 224, 228 D Conuber , 161 D. maxima see Dendropoma maxima Conus , 193 D. petraeum see Dendropoma petraeum Conus geographus , 193–195 Dactylopius coccus , 296 Conus striatus , 193, 194 Defence , 12–17, 39, 42, 75, 103, 107, 108, Conus textile , 111–112, 143, 193, 195, 196 122, 132, 158, 162, 197, 203, 204, 206, Copulation , 90–92, 101, 106, 108, 119, 134, 218, 235–236, 240, 243–246, 248, 250, 135, 138, 142, 146, 164, 190, 206, 207, 251, 260, 271 212–214, 217–220, 229, 232, 240, 241, Dendronotina , 8, 237, 249–252 249, 260 Dendropoma , 123 Coral reefs , 106, 181, 189 Dendropoma maxima , 106 Coral-killer , 187, 188 Dendropoma petraeum , 104, 105, 107 Coralliophila , 189 Deposit feeding , 73 Coral-lover , 189 Desiccation , 12, 40–43, 49, 51, 84, 102, Cowry(ies) , 32, 97, 138–146, 150, 156, 189, 104, 118, 126, 127, 137, 220, 258, 268–277 260, 263 Cracked-pipe , 97, 99–103 Detritus , 56, 61–63, 73, 75, 79, 82, 106, 109, Cratena , 243 113, 114, 118, 123, 124, 134, 174, 176, Cratena peregrina , 243 211, 261 Crawl(s)(ing) , 4, 9, 16, 18, 19, 30, 31, 40, 41, Devonian period , 89 50, 72, 73, 76, 90, 93, 94, 101, 103, Diet , 30, 46, 48, 49, 63, 64, 66, 69, 72, 79, 105, 107, 116, 117, 120, 131, 136, 143, 133, 145, 151, 157, 175, 177, 193, 144, 150, 153, 161, 165, 166, 170, 204, 208, 216, 228, 240, 251, 260 175–178, 182, 187, 193, 209, 211–214, Digestion , 12, 25, 26, 105, 163, 216, 228, 216, 218, 220, 231, 235, 241, 243, 245, 230, 246 261, 276, 288, 322 Digestive enzymes , 8, 25, 231 332 Index

Digestive gland , 22, 25, 26, 30, 174, 216, 217, Extreme temperature , 42, 260 226, 229–231, 242, 247–251 Eye(s) , 11, 30, 37, 38, 44, 49, 52, 68, 71, 73, Diodora , 59, 61, 62 82, 111, 113, 117, 162, 168, 175, 189, Direct development , 9, 76, 90, 122, 136, 205, 206, 212, 262, 269, 271, 289, 302, 243, 245 307, 313 Discodoris planata , 240 Dissolved organic matter , 29, 68, 176 Distorsio , 157, 158 F DNA , 230, 232 Faece(s) , 26, 49, 56, 60, 68, 72, 114, 171, Dog-whelk , 131, 319, 320, 322 216, 224 Dorids , 208, 237–242 False cowries , 97, 138–146 Doto acuta , 249, 250 False limpet , 259–261 Drupella , 187, 188 False mouth , 95, 151, 152 Dye , 181, 268, 285–292, 294–303, 305 Favorinus branchialis , 246 Feeding , 7, 12, 19, 23–26, 30, 44–49, 51, 56, 63, 64, 73, 90, 93, 95–96, 103, 105, E 106, 108, 109, 111, 113, 117, 120, E. peruviana see Echinolittorina peruviana 122–125, 133–134, 136, 137, 141–142, Echineulima , 170 144, 145, 151, 164, 174–178, 187, 193, Echinolittorina peruviana , 127, 128 208, 211, 216–218, 220, 223, 224, Egg , 26, 27, 50, 62, 63, 76, 77, 79, 81–84, 228–232, 240, 243–246, 261, 279, 316 92–94, 101–103, 107, 111, 113, 117, Female(s) , 26, 50, 62, 63, 68, 76, 81, 82, 119–122, 129, 133–138, 142–144, 146, 90–94, 100–103, 106, 107, 112, 113, 157, 161, 164, 166, 169, 171–173, 177, 116, 117, 119–122, 128, 134–136, 138, 183, 189, 190, 195, 197, 207, 209, 213, 142, 143, 146, 157, 161, 164, 166, 169, 219, 220, 225, 228, 232, 233, 235, 245, 171–173, 177, 178, 189, 190, 195, 206, 246, 258, 260–263, 269, 320–322 207, 212–214, 218, 219, 224, 225, Egg capsules , 79, 81–83, 93, 94, 107, 119, 232–235, 249, 258, 260, 281, 302, 122, 136, 137, 142, 146, 161, 166, 319–322 171–173, 177, 189, 195, 197, 321, 322 Fertilisation , 26, 31, 50, 76, 79, 85, 90–92, Egg capsules yolk , 94, 107, 120, 166, 245, 263 101–103, 106, 108, 112, 121, 142, 146, Egg-cowries , 144 161, 164, 177, 189, 190, 195, 206, 207, Elysia timida , 234, 235 219, 241, 260 Emarginula , 61 Fertility , 268, 269, 272, 312, 315 Embryo , 76, 81, 82, 84, 85, 90, 93, 94, 102, Filter-feeding , 63, 64, 96, 120, 122–125 107, 117, 120, 122, 136–138, 143, 157, Filtering , 23, 73, 103, 105, 106, 117, 120 164, 171, 177, 190, 197, 219, 228, 258, Firoloida , 163 261, 263 Fissurelloidea , 56, 61–62 Embryonic development , 8, 9, 11, 15, 26–31, Flat winkle , 129, 130, 133 76, 84, 90, 93–94, 103, 169, 177, 197, Food , 4, 7, 12, 18, 19, 22–27, 29, 30, 43, 225, 258, 261 46–49, 51, 56, 63, 68, 72–75, 82, 83, Enteroxenos , 171–173 93–96, 100, 101, 103, 105, 106, 108, Eoacmeoidea , 52 111, 114, 117, 119, 120, 124, 125, 134, Epipodium , 60, 67, 71, 72 144, 151, 164, 166, 168, 175–179, 193, Epitoniidae , 164–166 207, 208, 216, 218–220, 224, 226, Epitonium millecostatum , 165 228–231, 235, 240, 246, 250, 260, 261 Erosaria annulus , 139 Foot , 5, 7, 9, 11–13, 16–19, 21, 22, 28, 30, 37, Euctenidiacea , 237 39–41, 43, 44, 57–61, 64, 67, 69, Eulimoidea , 97, 159, 169–173 71–73, 75, 76, 95, 100, 103–105, Euspira catena , 161 107–120, 122, 125, 127, 129, 134, 137, Evil eye , 271 142, 144–146, 151, 155, 157, 160–163, External fertilisation , 50 165–167, 169–171, 174–178, 181–183, External parasites , 145, 164, 169–171, 190, 204–206, 209, 220, 224, 225, 230, 178, 189 236, 245, 251, 261, 263, 273, 309 Index 333

Freshwater , 83, 84, 89, 90, 96, 103, 322 H. schoeferti see Hancockia schoeferti Frontal veil , 249 Haemocyanin , 22, 45 Fryeria , 240 Haemolymph , 22 Functional morphology , 55–60, 89–97, Halichondria panacea , 240 149–153, 204–208 Haliotidae , 66 Haliotoidea , 66–68 Haminoea , 210, 211 G Hancockia , 249, 250 Gadinalea , 261 Hancockia schoeferti , 249 Gamete , 12, 26, 41, 50, 68, 90, 207 Hancockia uncinata , 249 Garden , 47–49, 177 Harpa , 178 Gaza , 69 Head , 4, 7, 11–13, 17, 21, 22, 26, 28, 29, Genital , 5, 60, 90–92, 99, 107, 112, 119, 135, 31, 37, 38, 43, 56, 60, 67, 71–73, 138, 142, 146, 161, 207, 213, 214, 224, 75, 95, 103, 105, 107–109, 116, 117, 232–235, 249, 260, 319–321 122, 124, 134, 145, 151, 155, 160, Genus , 24, 32, 43, 62, 66, 75, 77, 100, 163, 164, 166, 171, 177, 188, 204–207, 104, 108, 123, 136, 157, 161, 165, 209, 213, 215, 216, 218, 219, 225, 234, 171, 173, 183, 187, 193, 194, 207, 236, 237, 242, 249, 251, 257, 260–262, 209, 210, 225, 226, 228, 235, 245, 308, 313 246, 289, 319 Heart , 5, 20, 22, 26, 195, 205, 216, 220, 230, Gill(s) , 7, 11, 13, 19–22, 28, 39, 43, 44, 56, 260, 312, 316 57, 59–61, 63, 66, 72–74, 81, 84, 96, Helicinidae , 80, 84 97, 100, 101, 103, 105, 106, 108, 109, Helmet shells , 97, 153–159, 268 111, 117, 120, 122–125, 136, 137, 150, Herbivorous , 24, 26, 45, 142, 150, 152, 210, 179, 189, 205, 208, 209, 225, 227, 211, 228 235–237, 243, 249, 258, 259, 262, 286 Hermaphrodite , 50, 116, 117, 121, 146, 166, Gill fi lter feeding , 106, 122–125 168, 169, 171, 206, 209, 224, 228, 229, Gill fi lter-feeders , 122 233, 235, 240, 257, 260 Gill-fi ltering , 106 Heteropoda , 97, 153, 161–164 Gland , 5, 15–17, 22, 25, 26, 29, 30, 41, 43, 60, Hexabranchus sanguineus , 237, 238 66, 73, 82, 105, 124, 134, 141, 146, Hexaplex trunculus , 185, 286, 300, 301 152–154, 160, 167, 169, 174, 178, 179, Hindu , 139, 268, 277, 280, 283 190, 192, 193, 197, 207, 210–212, Hipponix , 117 216–218, 223–226, 229–231, 240, 242, Hipponix australis , 119, 120 247–251, 260, 261, 286, 289, 298, 300, Hipponix conicus , 118, 119 304, 321, 322 Hipponix cranoides , 118, 120 Glaucus , 245, 246 Home scar , 41, 42, 44, 260 Gleba , 223, 224 Homing , 4340–42, 49, 51 Glycogen , 44 Hoof snail(s) , 117–119, 121 Goethite , 45 Hoverers , 97, 153, 161–164, 174, 204 Gonad(s) , 26, 50, 51, 206, 207, 224, 233, 241, Humidity , 40, 128 320, 321 Hydatina , 209, 210 Grazer(s) , 23, 44, 45, 79, 99–146 Hydrocenidae , 80, 84 Grazing , 23, 45, 46, 49, 63, 64, 96, 117, 122, Hydrothermal vents , 63–65, 122 134, 188, 237, 260 Hypobranchial gland , 66, 286, 300 Greek mythology , 77, 80, 139, 246, 268, 308, Hypodermic insemination , 232, 233 309 Greigite , 64 Gymnosomata , 208, 225–228 I Imposex , 319–322 Ink , 217, 218, 298, 303 H Internal fertilisation , 85, 90, 92, 101, 106, H. australis see Hipponix australis 108, 260 H. cranoides see Hipponix cranoides Inter-specifi c mating , 135 334 Index

Intertidal , 17, 18, 39, 42, 43, 45, 46, 49, 52, Lepeta , 44 61, 75, 81, 83, 85, 89, 102, 104, 106, Lepetodriloidea , 60, 63–65 122, 127, 131, 134, 136, 174, 183, 195, Lepetodrilus , 61, 63 259, 262, 289, 298 Lepetodrilus fucensis , 63, 64 Iron oxide , 45, 55 Lepetodrilus gordensis , 63, 64 Iron sulphide , 64 Lepus marinus , 215 Iron sulphur , 64 Life cycle , 30, 49, 83, 119, 208, 218–220, 228 Limacina , 222, 226, 227 Limacina inﬂ ata , 225 J Limacina trochiformis , 224 J. globosa see Janthina globosa Limpet(s) , 9, 19, 31, 32, 37–52, 55–57, J. janthina see Janthina janthina 60–62, 68, 69, 72, 83, 90, 93, 96, Janthina , 166, 303 116, 259–262 Janthina globosa , 169 Littoraria , 128, 131, 134–136 Janthina janthina , 167, 169 Littoraria albicans , 128 Jaw , 24, 74, 106, 124, 142, 145, 152, 154, 170, Littoraria irrorata , 132–134 174, 179, 181, 216, 243, 251 Littoraria pallescens , 128 Jujubinus , 76 Littoraria philippiana , 128 Jurassic , 52, 66, 89, 104, 108, 204 Littoraria pilosa , 128 Juvenile , 13, 47, 49, 61, 68, 72, 83, 84, 93, Littorina compressa , 128, 130 108–110, 113, 119–122, 124, 136, 142, Littorina fabalis , 128–131, 133 143, 161, 163, 177, 178, 183, 191, 208, Littorina littorea , 128, 131, 132, 134, 135, 218, 220, 224, 225, 233, 235, 246, 261 320, 321 Littorina obtusata , 128–131, 134 Littorina saxatilis , 128, 129 K Littorina subrotundata , 135 Kelp , 45, 46, 72 Littorinoidea , 97, 125–138 Kermes , 292, 295 Lobatus gigas (formerly Strombus gigas ) , 315 Keyhole limpets , 56, 60–62, 69 Lobe , 9, 26, 27, 29, 30, 60, 63, 71, 73, 101, Kidneys , 5, 20, 22, 26, 28, 56, 60, 207 113, 119, 124, 158, 171, 223–225, 228, Kingdom , 3, 4, 8, 18, 26–28, 32, 45, 65, 135, 229, 231, 241–243, 247–249, 251, 252, 193, 231, 249, 277, 281, 291, 319 260, 321 Lobiger , 236 Lobtaus galeatus , 113, 114, 310 L Locomotion , 4, 5, 7, 12, 17–19, 22, 27, 29, 30, L. compressa see Littorina compressa 40, 41, 69, 71, 109, 113, 137, 170, 171, L. fabalis see Littorina fabalis 175, 218, 227 L. gordensis see Lepetodrilus gordensis Locomotory , 30, 225 L. littorea see Littorina littorea Longevity , 208, 231 Lacuna , 136 Lottia , 43 Laevilittorina , 136 Lottia gigantea , 44, 49 Laila cockerelli , 240 Lottioidea , 52 Lambis , 113, 115 Lung , 84, 195, 257–260, 262 Lamellaria , 146 Luria isabella , 140 Land snails , 32, 138, 206, 257–263 Larva , 27– 31, 79, 93, 261 Larvae , 52, 57, 76, 77, 82, 93, 121, 128, 137, M 143, 146, 161, 163, 228, 261, 322 M. myosotis see Myosotella myosotis Larval , 8, 27, 30, 39, 83, 90, 93, 124, 172, M. neritoides see Melarhaphe neritoides 177, 207, 235, 258, 262, 322 Males , 26, 50, 63, 68, 76, 79, 90–92, 99, Leaﬂ ets , 19–22, 57, 60, 63, 66, 72–74, 96, 101–103, 106, 108, 112, 116, 117, 100, 101, 117, 123, 124, 136, 150, 206, 119–122, 134, 135, 138, 142, 146, 164, 208, 228–233, 235, 236, 249, 259 166, 168, 169, 171–173, 177, 178, 189, Leaping , 109, 111, 112 206, 207, 212–214, 218, 219, 224, 225, Leiblen’s gland , 174 232, 241, 281, 312, 319, 320 Index 335

Mantle , 6, 7, 11, 12, 15, 16, 19–22, 26, 28, Mucus , 17–19, 21, 26, 27, 30, 40, 41, 49, 68, 29, 31, 38, 39, 41–44, 55–63, 65–68, 72, 74, 76, 100, 101, 105, 106, 109, 71–74, 76, 90, 92, 96, 99–103, 105–108, 117, 123, 124, 127, 128, 133, 134, 142, 116–120, 123–125, 134–137, 140–142, 155, 160–162, 164–167, 169, 178, 187, 144–146, 150, 157, 158, 160, 161, 169, 207, 209, 211, 212, 223–225, 230, 235, 176, 189, 204–206, 210, 212, 215, 217, 244, 260, 261, 263 218, 221–223, 225, 236, 237, 240, 257, Mucus glands , 30, 105, 169, 223, 225, 230 258, 260–263, 286, 295, 320–322 Mucus trails , 19, 41, 68, 134 Mantle cavity , 7, 11, 19–22, 26, 28, 29, 43, 50, Murex , 151, 290, 294 56, 57, 59–61, 63, 66, 71–74, 76, 90, Murex(es) , 24, 97, 151, 153, 174, 181–191, 92, 99–103, 105–108, 117–120, 123, 193, 288, 290–296, 300, 303, 305 124, 134–137, 157, 160, 161, 169, Muricoidea , 97, 153, 174, 181–190 204–206, 210, 212, 215, 217, 218, 223, Muscle , 5, 12, 17, 18, 21–23, 29, 37, 39, 40, 225, 237, 257, 258, 260, 262, 286, 322 44, 45, 56, 57, 59, 61, 63, 67, 83, 95, Mantle ﬂ aps , 39, 62, 90, 117, 140–142, 108, 109, 111, 112, 116–120, 143, 145, 144–146, 189 146, 151, 152, 154, 155, 160, 178, 182, Margarites , 77 190, 193–195, 217, 224, 225, 227, 236, Margarites vorticiferus , 77 245, 247, 248, 251, 252 Margin snail(s) , 189, 190 Myoglobin , 45 Marginellidae , 189 Myosotella , 262, 263 Marsh winkle , 132–134 Myosotella myosotis , 262 Mechanical defence , 103, 236, 240, 263 Melanella frieli , 170 Melanoides , 103 N Melanopsis , 103 N. balteata see Nerita balteata Melarhaphe , 136 N. planospira see Nerita planospira Melarhaphe neritoides , 126–128 N. undata see Nerita undata Melibe , 251, 252 Nacella concinna , 43, 50 Melongena corona , 132, 133 Nacre , 94 Metabolic rate , 127, 260 Naticoidea , 97, 153, 159–161 Metamorphose , 9, 30, 31, 45, 50, 82, 83, 93, Navanax , 209 94, 103, 113, 136, 142, 161, 166, 171, Navanax inermis , 212, 213 172, 196, 206, 207, 219, 220, 231, Nematocyst , 243, 244, 250 261, 262 Neomphalidae , 123 Metamorphosing (metamorphosis) , 9, 28–31, Neomphaloidea , 60, 63–65, 123 50, 57, 61–63, 67, 69, 83, 93,111, 113, Neomphalus , 123 119, 124, 136, 158, 164, 171, 172, 204, Nerita , 81 207, 219, 220, 231, 233, 235, 237, Nerita balteata , 82 246, 251 Nerita chamaeleon , 82 Methane , 63, 82 Nerita planospira , 82 Mitridae , 188 Nerita undata , 82 Mobility , 40, 118 Nerites , 32, 77, 79–85, 89–91, 93, 96, 258 Mollusca , 3, 4, 6, 9, 10, 13, 29, 206, 258 Neritidae , 80, 81, 83, 84 Molluscs , 3–9, 11, 13, 22, 23, 30, 59, 64, 81, Neritilia cavernicola , 82 126 Neritiliidae , 80, 82 Monetaria moneta , 268, 269, 272, 274, 276 Neritimorpha , 32, 79–85 Money , 144, 267–283 Neritina , 83 Monogamus , 170, 171 Neritina asperulata , 84 Moon shells , 97, 151, 153, 159–161, 174, 181, Neritina dilatatus , 83 183, 261 Neritina pulligera , 84 Mortality , 30, 42, 46, 51, 126, 187, 220 Neritodryas , 84 Mother-of-pearl , 13, 61, 65, 68, 69, 79, 94, 95 Neritopsidae , 80, 82 Mouth cavity , 23, 24, 56, 75, 106, 151, Neritopsis , 82 192, 193 Nitrogen , 22, 48, 134, 228, 231 Muco-protein , 26, 124 Notarchus , 221 336 Index

Notoacmaea petterdi , 42 Pallial sperm duct , 90 Notocochilis gualteriana , 161 Pallial sperm groove , 90 Notocypraea , 143 Parapodia , 204, 205, 210, 213–215, 220, 221, Nucella lapillus , 185, 319, 320, 322 223–225, 228–232, 235 Nudibranchia , 208, 237–252 Parasitic-snails , 97, 153, 169–174, 189 Nudibranchs , 208, 236–252 Parasperm , 91, 106, 168 Nutmegs , 97, 174–180 Parenteroxenos dogieli , 173 Nutrition , 30, 50, 134, 144, 169, 177, 206 Parthenogenesis , 102 Patella , 37, 39, 43, 44 Patella argenvillei , 46 O Patella caerulea , 31 Oesophageal digesting glands , 124 Patella cochlear , 46 Oesophagus , 24, 25, 105, 151, 152, 154, 163, Patella compressa , 46 171, 174, 216, 251 Patella granatina , 46 Onchidiidae , 262 Patella granularis , 43 Onchidoris bilamellata , 240 Patella longicosta , 46, 48, 49 Opaline gland , 218 Patella oculus , 49–51 Operculum , 11–17, 30, 31, 37, 50, 61, 63–65, Patella pellucida , 45, 46 67, 69, 71, 72, 99, 103–105, 111, 112, Patella vulgata , 40, 43, 45 115, 125–127, 133, 138, 145, 157, 160, Patellogastropoda , 32, 37–52 162, 163, 169, 172, 183, 193, 203, 206, Patelloida , 51, 52 207, 209, 222, 226, 237, 257, 260–262, Patelloida latistrigata , 51, 52 280, 303–305 Patelloidea , 52, 259 Opisthobranchia , 32, 153, 203, 205, 206, 208, Pelican’s-foot , 108–116 209, 245, 246, 257, 258 Peltodoris atromaculat , 240 Oral veil , 236 Penis , 60, 63, 79, 91, 99, 101, 108, 112, 116, Order , 15, 24, 32, 52, 60, 80, 83, 97, 109, 123, 119, 134, 135, 142, 166, 168, 171, 206, 152, 153, 203, 204, 208, 209, 215, 222, 207, 209, 213, 223–225, 232–234, 225, 228, 236, 238, 249, 257, 292, 310, 240–242, 249, 260, 315, 319–322 312, 313 Peraclis , 222, 224 Ordovician , 52, 55, 68, 79 Pericardium , 22, 26 Osilinus , 76 Periostracum , 15, 120, 124, 158, 277 Osphradium , 21, 96, 108, 150, 175 Petil tekhelet , 300 Ova , 26, 90, 92, 101, 106, 119, 121, 169, 172, Phanerophthalmus , 211 173, 207, 219, 224, 225, 249 Phasianella , 69 Ovary , 26, 171–173, 207 Phasianellidae , 69 Oviduct , 92, 100, 101, 172, 173, 207, 321, 322 Pheasant snails , 69 Ovule(s) , 50, 56, 60, 62, 63, 76, 92, 100, 121, Phenacolepadidae , 80, 82 207, 233, 234, 320 Pheromones , 26, 101, 121, 177 Ovulidae , 144–145 Philinopsis , 212 Ovum , 26, 27 Photosynthetic , 49, 217, 230, 232, 245 Oxygen , 7, 19–22, 43–45, 59, 67, 72, 83, 137, Phycoerythrin , 217 171, 230, 243, 257–262, 289 Phyllidia , 237, 240 Oxygyrus , 162 Phyllidiidae , 240 Oxynoe panamensis , 235 Phyllidopsis , 240 Oxystyle , 49 Phylliroe , 250, 251 Oyster-drill , 122, 182, 183 Phyllodesmium , 245 Phyllodesmium hyalinum , 245 Phylum , 3–6, 9, 10, 13, 29, 206, 243, 246, 249 P Phymorhynchus , 65 P. gigantea see Pleuroploca gigantea Pigments , 15, 16, 30, 38, 44, 51, 69, 129, 141, Palio , 240, 241 145, 210, 220, 287, 299 Pallial oviduct , 92, 322 Planaxis sulcatus , 102 Index 337

Plankton , 23, 29–31, 51, 57, 74, 79, 82–85, 90, Protein , 12, 13, 15, 17, 18, 22, 26, 29, 30, 40, 93, 94, 105, 111, 113, 117, 119, 121, 41, 45, 94, 99, 103, 120, 124, 127, 141, 124, 136, 137, 157, 161, 163, 164, 168, 158, 162, 174, 183, 231, 232, 267, 292 171, 177, 197, 219, 220, 223, 224, 228, Protoconch , 13, 31, 52, 57, 65, 120 231, 235, 243, 251, 258 Pseudo-conch , 222, 223 Planorbis , 58 Pseudoplotia , 103 Pleurobranchidea , 208, 236 Pseudoproboscis , 124 Pleuroploca gigantea, 312 see also Triplofusus Pterosoma , 163 Pleuroploca princeps , 312 Pterotrachea , 163 Pleurotomarioidea , 60, 65–66 Pulmonata , 32, 204, 205, 257, 258 Plicopurpura pansa , 298–300 Pulmonates , 32, 257–263 Pneumodermopsis canephora , 227 Purple , 80, 166, 169, 181, 217, 285–307 Pneumodermopsis paucidens , 227 Purple chamber , 295 Poison darts , 23 The purple dye industry , 288, 297, 300 Polinices pulchellus , 161 Purpura pansa , 298–300 Pomatias , 137, 138 Pyrite , 64 Pomatiidae , 137, 258 Porphyra Novissima , 295 Porphyrin , 15, 69 Q Porphyrogenitos , 295 Queen conch , 315, 316 Predation , 14, 30, 50–52, 76, 81, 83, 94, 95, Queen helmet shell , 157, 158 102, 126, 128–130, 132, 133, 150, 152, 153, 155, 157, 164, 176, 178, 211, 212, 220, 244, 263 R Predators , 12, 14–17, 24, 30, 40, 49–51, Radial symmetry , 4–7, 9, 206 60, 62, 65, 66, 72, 75, 84, 90, 94, Radula , 7, 9, 23, 24, 28, 38, 41, 44–46, 52, 55, 104, 108, 109, 111, 113, 119, 122, 56, 63, 74, 79, 96, 101, 105, 106, 108, 126, 128, 130–133, 143–144, 149–198, 117, 122, 124, 143, 151, 152, 154, 155, 205, 206, 212, 217, 218, 226, 228, 157, 158, 160, 161, 163–165, 168–170, 236, 237, 240, 243, 248, 252, 260, 174, 176, 178, 179, 181, 182, 187, 261, 288, 319 189–192, 198, 209, 216, 224, 226, 227, Predatory , 24, 50, 51, 65, 108, 109, 111, 119, 229, 230, 240, 243, 251, 260, 261 122, 128, 132, 133, 150–154, 158, 159, Radular formula , 24, 96 162, 163, 174, 177, 191, 212, 248, 261, Receptaculum seminis , 101, 207, 219 288, 319 Reproduction , 12, 26–30, 41, 50, 62, 68, 76, Prey , 7, 24, 30, 50, 62, 66, 75, 122, 131, 133, 90, 102, 112, 124, 134–138, 142–143, 145, 150–152, 154, 155, 157, 158, 169, 177, 178, 209, 216, 219, 232–235, 160–163, 166, 168, 174–178, 181, 183, 245, 319 189, 191–194, 208, 212, 224–228, 240, Respiration , 7, 12, 19–22, 43–44, 59, 60, 90, 243–251, 263, 315 108, 109, 225, 227, 237, 260 Primitive , 4, 6, 13, 17, 26, 29, 32, 37, 38, 43, Respiratory organ , 43 52, 56, 57, 59, 68, 77, 90–97, 99, 108, Reticulida , 240 112, 136, 162, 169, 174, 190, 191, Robillardia , 171 204–207, 209, 215, 229, 230, 235, 236, 258, 261–263 Proboscis , 95, 124, 151 S Proserpinellidae , 80 S. gerula see Spectamen gerula Proserpinidae , 80 S. luteola see Solariella luteola Prostate , 63, 91, 206, 213, 214, 224, 234, 321, Sabinella troglodytes , 170 322 Sacoglossa , 208, 228–236, 245 Protatlanta , 162 Sacred colour , 268 Protection , 40, 43, 50, 51, 65, 84, 118, 143, Sacred music , 268 181, 230, 246, 247, 300 Sacred scent , 268 338 Index

Saliva , 24, 25, 154, 165, 194 Spawn , 26, 50, 56, 76, 90, 93, 112, 113, 136, Salivary glands , 25, 152, 154, 179 143, 161, 207, 208, 219, 225, 315 Salt-marsh winkle , 132, 133 Species , 7, 9, 14, 15, 23, 24, 31, 32, 39–43, 45, Scavenger , 174–177 46, 48–51, 62–64, 68, 73, 75, 77, 80, Scavenging , 23, 119 83, 84, 90, 91, 93, 102, 104–107, 109, Scutellastra cochlear , 46–48 111–113, 117–120, 122, 125–131, Scutus , 62 133–138, 140–145, 150, 156, 161–163, Sea angels , 206, 225–228 165, 168, 170, 174, 175, 181, 183, 189, Sea butterﬂ y(ies) , 163, 208, 221–228 192–195, 197, 204, 207, 208, 212, 215, Sea hares , 24, 206, 208, 210, 212, 215–221, 216, 220, 225, 227, 228, 230–233, 235, 225, 246 240, 243–246, 248, 249, 258, 261–263, Sea slugs , 9, 26, 28, 32, 203–252, 257, 263 272, 274, 276, 283, 288, 300, 303–305, Seminal receptacle , 207 310, 319, 320, 322 Senescence , 176, 220 Spectamen gerula , 76 Sense organs , 30, 56 Spectamen multistriatum , 76 Sensory organs , 4, 27, 38, 60, 228 Sperm , 26, 27, 56, 60, 63, 76, 79, 90–92, 99, Septaria , 83 101, 106, 107, 112, 113, 116, 119, 121, Sequential hermaphrodite , 116, 117, 121, 206 122, 134–136, 164, 166, 168, 169, 173, Sex change , 50, 121, 122, 189 206, 207, 213, 214, 218, 219, 224, 225, Shekhelet , 285–305 232–235, 241, 249, 260, 320–322 Shell apex , 13, 59, 61, 311 Sperm competition , 91, 121, 122, 135, 249 Shell colour , 69, 74, 80, 127, 129, 130, 137, Sperm duct , 60, 90, 99, 173, 233, 241, 141 320, 321 Shell degeneration , 203–252 Sperm groove , 90, 91 Shell microstructure , 52, 69 Sperm purse , 101, 106, 107 Shell muscle , 17, 18, 21, 22, 39, 40, 44, 59, Sperm receptacle , 92, 101, 207, 219, 225, 241 63, 67, 108, 109, 111, 112, 116, 119, Spermatophore , 99, 101, 106, 107, 164, 249 120, 143, 145, 160, 224, 277 Spider-conch , 113–115 Shell structure , 14, 94–95, 120 Spindle-cowries , 144 Shield slug(s) , 208–221 Spiral shell , 58, 59, 174 Side-gills , 208, 236–237 Spirally coiled , 32, 58, 68, 142 Siliquariidae , 123 Sterility , 268, 269, 320, 322 Simultaneous hermaphrodites , 146, 206, 209, Stilifer , 171 228, 229, 232, 233, 240 Stinging cells , 165, 168, 175, 187, 243, 244, Siphon , 73, 108, 150, 154, 159, 171, 174, 175, 246–251 181, 191 Sting(ing) sac , 243, 245, 247–250 Siphonaria , 259–261, 263 Stomach , 11, 25, 26, 29, 63, 105, 124, 143, Siphonaria serrata , 261 152, 154, 177, 217, 226, 228, 247, 303 Siphonarioidea , 259–261 Stomach shield , 26 Siphopteron quadrispinosum , 213, 214 Stomatella , 75, 76 Slippers , 97, 116–122 Stone-collectors , 97 Slipper-shells , 120, 121 Stramonita , 183, 289, 290 Slit-whorls , 60, 65–66 Stramonita haemastoma , 184, 286 Slug , 9, 11, 18, 26, 28, 32, 62, 82, 203–252, Stromboidea , 97, 108–116, 123 257, 262, 263 Strombus , 111, 303, 304 Small winkle , 126, 127 Strombus gigas , 315 Smaragdia , 81 Strombus trumpets , 304 Solariella , 73 Struthiolaria , 123 Solariella luteola , 76 Struthiolariidae , 123 Solariella plicatula , 76 Subtidal , 39, 41, 46, 51, 61, 81, 89, 102, 113, Sole (of foot) , 17–19, 30, 31, 40, 93, 105, 118, 183, 187 120, 141, 146, 155, 171, 176, 181, 182, Sulphide , 63–65, 83 190, 220, 246 Sulphuric acid , 154, 155, 236, 240 Index 339

Symbiosis , 63, 231 Triviidae , 145–146 Symbols of status , 273, 291 Trochidae , 69, 123 Trochoidea , 60, 61, 68–77, 123 Trochophore , 27, 30, 31, 50, 76, 93, 136 T Trochus , 69, 77 T. giganteus see Triplofusus giganteus Trumpet shell , 158, 159, 308, 309, 311, 312, Talparia talpa , 141 315, 316 TBT see Tributyltin Trumpets , 97, 113, 153–159, 268, 277, 279, Teeth , 7, 14, 23, 24, 44–46, 55, 56, 79, 96, 288, 289, 307–316 152, 154, 161, 163, 164, 169, 174, 181, Trunk , 96, 109, 111, 113, 114, 116, 118, 119, 187, 190–192, 198, 216, 226, 229, 230, 124, 128, 134, 142, 151, 152, 154, 155, 243, 260, 261 157, 158, 160, 163–165, 168, 170, 171, Tegula funebralis , 72 174–179, 182, 183, 189, 192, 193, 224, Tekhelet , 300–303, 305 227, 308 Temperature , 31, 40, 42, 43, 50, 126, 128, 219, Tuns , 97, 153–159 260, 289 Turbans , 61, 68–77, 119 Tenagodus , 102, 103, 123 Turbinella pyrum , 277, 278, 283 Tentacle(s) , 11, 22, 30, 37–39, 44, 60, 61, 68, Turbinidae , 69 71–73, 75, 90–92, 100, 105, 117, 124, Turridae , 191, 193 145, 155, 162, 168, 175, 179, 204, 205, Turrids , 191–198 215, 225, 233, 236, 242–245, 251, Turritella , 100, 101, 105, 123, 197 262, 320 Turritella communis , 101 Terebra , 198 Turritellidae , 123 Terebridae , 197–198 Tylodina , 236 Territorial , 39, 42, 46–49 Territory , 42 Testis , 26, 90, 91, 169, 171, 173, 206 U Thecosomata , 208, 222–225 Umbilicus , 13, 77, 125, 159 Theodoxus , 83, 84 Umbonium , 73, 75, 77 Thiara , 103 Umbonium vestarium , 73, 74 Thyonicola , 173 Umbraculum , 236 Titiscania , 82 Urinary , 5, 56, 79, 85, 90 Tonna , 154 Urine , 56, 60, 72, 289 Tonnoidea , 97, 153–159 Urosalpinx , 182 Tooth , 23, 24, 45, 55, 56, 96, 143, 164, 174, Urosalpinx cinerea , 122, 182 190–193, 229 Top shells , 32, 49, 60, 68–77, 93 Torsion , 11, 28, 29, 31, 50, 56, 93, V 205, 261 Vagina , 207, 240 Toxic , 21, 103, 206, 218, 261, 319 Veliger , 8, 9, 27–31, 45, 47, 50, 56, 57, 62, 63, Trail-following , 19, 134 67, 68, 76, 82–84, 90, 93, 94, 101–103, Triassic , 64, 68, 79, 100 111, 113, 117, 119, 124, 136, 137, 142, Tributyltin (TBT) , 320, 322 143, 146, 157, 158, 164, 166, 169, Trichotropis , 123–125 171–173, 177, 189, 197, 206, 207, Tricolia , 69, 76 219–221, 225, 228, 235, 245, 251, 258, Trimusculus , 261 260–262 Triplofusus giganteus , 312, 314 see also Velum , 27, 136, 137 Pleuroploca gigantea Velutinoidea , 97, 145 Triplofusus princeps , 311 Venom , 143, 154, 157, 158, 183, 187, Triplofusus princeps formerly 191–194, 197, 198, 244, 246, 247 Pleuroploca princeps , 311 Vermetes triqueter , 105, 107 Trivia , 97, 145, 151 Vermetidae , 123 Trivia monacha , 146 Vermetoidea , 97, 104–107, 123 340 Index

Vetigastropoda , 32, 52, 55, 56, 58, 60, 65, 66, Whorls , 13, 15, 31, 57, 60, 65–66, 69, 81, 93, 77, 89, 90, 123 99, 100, 102, 103, 105, 125, 138, 142, Vetigastropods , 55, 56, 60, 63, 64, 69, 79 144, 146, 152, 157, 159, 164, 177, 197, Violet shells , 97, 164–169, 174, 245 209, 279, 283, 309 Violets , 168, 289 Winkle(s) , 24, 32, 41, 97, 102, 125–138, Viscera , 5–7, 11, 12, 22, 27–29, 31, 57, 155, 258, 260 163, 172, 173, 205, 206, 209–211, 223, Winkle-come-ashore , 137 229, 235, 236, 241, 263 Worm snails , 97, 104–107 Visceral hump , 7, 11, 26, 29, 57, 235, 236 Vision , 39, 68, 94, 132, 162, 233, 314 Voluta , 178 X Xenophora , 114, 115 Xenophoroidea , 97, 114 W Wentletrap(s) , 97, 153, 164–169, 174 Whelk(s) , 97, 131, 153, 174–181, 185, Z 190, 193, 277, 282, 283, 288, 289, Zoila , 143 319, 320, 322 Zoo xanthellae , 245 Subject Index 1: Defence1

1. General list of groups Littorina fabalis , 134, 136, 138 Aeolidia papillosa , 245 Littorina obtusata , 128, 130 Aeolidina , 208, 237, 242–249 Lobiger , 236 Anthobranchia , 208, 237–242 Melibe , 251 Aplysia fasciata , 217, 220 Opisthobranchia , 32, 153, 203, Aporrhais , 108 205, 206, 208, 209, 245, 246, Aporrhais occidentalis , 109, 110 257, 258 Berthella martensi , 236 Ovulidae , 144–145 Berthellina , 236, 237 Oxynoe panamensis , 235 bubble shells , 208–214 Phasianellidae , 69 Bulla , 210, 212 Philinopsis , 212 Cantharidus , 70, 71, 77 Pleurobranchidea , 208, 236–237 Cephalaspidea , 208–214 Reticulida , 240 Chelidonura , 209, 212 Siphonaria , 259–261 Chlorostoma funebralis , 72, 75 Siphonarioidea , 259–261 Clanculus , 70, 71, 77 Smaragdia , 81 Clione antarctica , 228 Stomatella , 75–76 Cratena , 243 Stromboidea , 97, 108–116, 123 Cratena peregrina , 243 Titiscania , 82 Crepidula fornicata , 120–122 Trimusculus , 261 Dendronotina , 208, 237, 249–252 Discodoris planata , 240 Haminoea , 210, 211 2. Avoiding or deterring predators L. compressa see Littorina compressa Aeolidina , 242–249 L. fabalis see Littorina fabalis Aporrhais , 108 Laila cockerelli , 240 Aporrhais occidentalis , 109, 110 Lambis , 113, 115 Chlorostoma funebralis , 72 Littoraria irrorata , 132–134 Crepidula fornicata , 120–122 Littorina compressa , 130, 134, 136 Lambis , 113, 115

1 Sea snails’ shell and operculum form the basic, ancestral structures of defence (chapters 2.1, 6.3). This index offers a general list of groups in which defence is discussed. It then classifi es specifi c aspects and modes of defence: avoiding or deterring predators, camoufl age, autotomy, warning colouration, secretion of noxious chemicals; use of acquired spicules and stinging cells, and secretion of alarm substances.

Littoraria irrorata , 132, 133 6. Noxious chemicals Stromboidea , 108–116 6.1 acquisition of Anaspidea , 215–221 Anthobranchia , 237–242 3. Camouﬂ age Pleurobranchidea , 236, 237 Aeolidina , 242–249 6.2 self production of Anthobranchia , 237–242 Anthobranchia , 237–242 bubble shells , 209–214 Anaspidea , 217–218 Cephalaspidea , 209–214 Aplysia fasciata , 217 Haminoea , 210, 211 Berthellina , 236, 237 L. compressa see Littorina compressa Bulla , 210, 212 L. fabalis see Littorina fabalis Clione antarctica , 228 Littorina compressa , 128, 130 Discodoris planata , 240 Littorina fabalis , 128–131, 133 Oxynoe panamensis , 235 Littorina obtusata , 128–131, 134 Pleurobranchidea , 236–237 Opisthobranchia , 206, 246 Siphonaria , 259, 260 Ovulidae , 144–145 Siphonarioidea , 259–261 Phasianellidae , 69 Titiscania , 82 Smaragdia , 81 Trimusculus , 261

4. Autotomy 7. Acquired spicules Berthella martensi , 236 Anthobranchia , 240 Cantharidus , 71 Berthellina , 237 Clanculus , 71 Pleurobranchidea , 236 Dendronotina , 249–252 Lobiger , 236 Melibe , 251–252 8. Acquired stinging cells Oxynoe panamensis , 235–236 Aeolidia papillosa , 244 Pleurobranchidea , 236–237 Aeolidina , 243 Stomatella , 75–76 Cratena , 243–244 Cratena peregrina , 243

5. Warning colouration Anthobranchia , 235–242 9. Alarm substances Laila cockerelli , 240 Bubble shells , 211 Opisthobranchia , 206 Cephalaspidea , 211 Philinopsis , 212 Chelidonura , 212 Reticulida , 240 Haminoea , 211 Subject Index 2: Movement and Attachment1

1. General list of groups Crepidula fecunda , 122 Acteon , 209 Creseis , 222, 227 Anaspidea , 208, 215–221 Crucibulum , 116, 117 Aplysia fasciata , 217, 220 Crysomallon squamiferum , 64 Aporrhais , 108 cup-and-saucer , 97, 116–122 Aporrhais occidentalis , 109, 110 Cymbulia , 223 Aporrhais pespelecani , 109, 110 Dendropoma , 123 Atlanta , 162, 163 Dendropoma maxima , 106 bubble shells , 208–214 Enteroxenos , 171–173 Bullia digitalis , 174, 175, 177 Epitonium millecostatum , 165 Cancellaria , 178, 180 Eulimoidea , 97, 153, 169–173 Cardiapoma , 163 false cowries , 97, 138–146 Carinaria , 163 Firoloida , 163 Cavolina , 222, 223, 225, 227 Glaucus , 245, 246 Cellana , 41, 42, 50–52 Gleba , 223 Cephalaspidea , 208–214 Gymnosomata , 208, 225–228 Cerithium , 101 H. australis see Hipponix australis Chelidonura , 209, 212 H. cranoides see Hipponix cranoides Chlorostoma funebralis , 72, 75 Haminoea , 210, 211 Clio , 222, 225–228 Heteropoda , 97, 153, 161–164 Clione antarctica , 228 Hexabranchus sanguineus , 237, 238 Clione limacina , 225, 226 Hipponix , 117–119 Colus stimpsoni , 109, 177 Hipponix australis , 119, 120 Coralliophila , 189 Hipponix cranoides , 118, 120 Crepidula , 120–123 hoof-snails , 117–119, 121

1 Sea snails’ basic mode of movement is by crawling over hard surfaces of the sea fl oor. Their basic mode of temporary attachment when inactive or in danger is to hard surfaces, by combining muscle contraction and mucus (chapters 2.2, 3.1). This index offers a general list of groups in which movement and attachment are discussed. It then classifi es specifi c modes of movement: rapid crawling, vertical climbing, locomotion over previously laid mucus trails, homing to territories, digging into soft sea fl oors, uprighting oneself if overturned, leaping, gliding over soft sea fl oors, occasional swimming, and permanent life and movement in the water column. It also presents aspects of attachment: adhering, sedentary behaviour and a sessile life.

hoverers , 97, 153, 161–164, 174, 204 2. Rapid crawling Janthina , 166, 303 bubble shells , 167 Janthina globosa , 169 Bullia digitalis , 174–175 Janthina janthina , 167, 169 Cancellaria , 180 Limacina , 222, 226, 227 Cellana , 50 Limacina inﬂ ata , 225 Cephalaspidea , 209 Limacina trochiformis , 224 Chelidonura , 212 limpets , 9, 19, 31, 32, 37–53, 55–57, 60–62, Chlorostoma funebralis , 75 68, 69, 72, 83, 90, 93, 96, 116, 259–261 Colus stimpsoni , 109 Littoraria , 128, 131, 135, 136 Haminoea , 211 Littoraria irrorata , 132–134 limpets , 49–52, 57 Littorina littorea , 128, 131, 132, 134, Littorina littorea , 131 320, 321 nutmegs , 178 Melibe , 251, 252 Patella oculus , 50 Monogamus , 170, 171 Stomatella , 75 Naticoidea , 97, 153, 159–161 surf whelk , 175, 176 Notarchus , 221 Notoacmaea petterdi , 42 Nutmegs , 97, 153, 174–180 3. Vertical climbing Opisthobranchia , 32, 153, 203, 205, 206, Littoraria , 128 208, 209, 245, 246, 257, 258 Ovulidae , 144–145 Oxygyrus , 162 4. Trail following Patella oculus , 49, 50 limpets , 40–49 Peraclis , 222, 224 Littorina littorea , 135 Phylliroe , 250, 251 Pneumodermopsis canephora , 227 Pneumodermopsis paucidens , 227 5. Homing Protatlanta , 162 Cellana , 41 Pterosoma , 163 limpets , 40, 41, 49, 51 Pterotrachea , 163 Notoacmaea petterdi , 42 Robillardia , 171 Siphonaria , 260 sea angels , 208, 225–228 Siphonarioidea , 259 sea butterﬂ ies , 163, 208, 222–225 shield slugs , 209–214 Siphonaria , 259–261, 263 6. Digging in Siphonarioidea , 259–261 Acteon , 209 slipper shells , 120, 121 Anaspidea , 219 Spanish dancer , 237, 238 Aplysia fasciata , 220 Stilifer , 171 Aporrhais , 108 Stomatella , 75, 76 Aporrhais occidentalis , 109 Stromboidea , 97, 108–116, 123 Aporrhais pespelecani , 109 Strombus maculatus , 112 Bullia digitalis , 174 surf whelk , 174–177 Cephalaspidea , 208–214 Tenagodus , 102, 103, 123 Cerithium , 101 Thecosomata , 208, 222–225 Opisthobranchia , 32, 153, 203, Titiscania , 82 205, 206, 208, 209, 245, 246, Tonna , 154 257, 258 Turritella , 100, 101, 105, 123, 197 Shield slugs , 208–214 Turritella communis , 101 Titiscania , 82 Umbonium , 73–75, 77, 123 Tonna , 154 Vermetes triqueter , 105, 107 Turritella , 100, 101 Vermetoidea , 97, 104–107, 123 Turritella communis , 101 violet shells , 97, 164–169, 174, 245 Umbonium , 73 Xenophora , 114, 115 Naticoidea , 160 Subject Index 2: Movement and Attachment 345

7. Uprighting itself Pneumodermopsis canephora , 227 Aporrhais , 109 Pneumodermopsis paucidens , 227 Bullia digitalis , 174 Protatlanta , 162 surf whelk , 174 Pterotrachea , 163 sea angels , 225–227 sea butterfl ies , 163, 223, 225, 228 8. Leaping Thecosomata , 222 Aporrhais , 108, 109 violet shells , 164, 166–169 Stromboidea , 108 Strombus maculatus , 112 Xenophora , 114 12. Adhering limpets , 19, 39, 40, 50, 61 9. Gliding on sea fl oor Naticoidea , 82 13. Sedentary Coralliophila , 189 10. Occasional swimming Crucibulum , 116 Anaspidea , 215 Crysomallon squamiferum , 64 Aplysia fasciata , 220 cup-and-saucer , 116 Bullia digitalis , 175 Epitonium millecostatum , 165 Hexabranchus sanguineus , 237 Eulimoidea , 169 Melibe , 251 False cowries 97, 138–146 Notarchus , 221 H. australis see Hipponix australis Spanish dancer , 237 H. cranoides see Hipponix Cranoides Hipponix , 117, 118 Hipponix australis , 119 11. Movement in water column Hipponix conicus , 118, 119 Atlanta , 162 Hipponix cranoides , 118 Cardiapoma , 163 hoof-snails , 117, 119 Carinaria , 163 Ovulidae , 144 Cavolina , 227 Xenophora , 114 Clio , 227, 228 Clione antarctica , 228 Clione limacina , 225 14. Sessile Creseis , 227 Crepidula , 122, 123 Cymbulia , 223 Crepidula fecunda , 122 Firoloida , 163 Dendropoma , 123 Glaucus , 245 Dendropoma maxima , 106 Gleba , 224 Enteroxenos , 171 Gymnosomata , 225 Eulimoidea , 169 Heteropoda , 161 H. cranoides see Hipponix Cranoides hoverers , 162, 164 Hipponix , 117, 118 Janthina , 166 Hipponix australis , 119 Janthina globosa , 169 Hipponix cranoides , 118 Janthina janthina , 169 hoof-snails , 117, 119 Limacina , 226 Monogamus , 171 Limacina infl ata , 225 Robillardia , 171 Limacina trochiformis , 224 slipper shells , 72, 122 Oxygyrus , 162 Stilifer , 171 Peraclis , 222 Tenagodus , 102, 103 Pterosoma , 163 Vermetes triqueter , 105–106 Phylliroe , 250 Vermetoidea , 104 Subject Index 3: Food and Feeding1

1. Herbivores & detritivores H. australis see Hipponix australis 1.1 general list of groups Haminoea , 210, 211 abalones , 32, 60, 66–69, 75, 119, 183 Hipponix , 117–119 Aeolidia papillosa , 244, 245 Hipponix australis , 119, 120 Anaspidea , 208, 215–221 L. gordensis see Lepetodrilus Aporrhais pespelecani , 109, 110 gordensis Archimediella , 100, 105 Lepetodriloidea , 60, 63–65 bubble shells , 208–214 Lepetodrilus , 60, 63, 64 Buccinoidea , 97, 132, 153, Lepetodrilus fucensis , 63, 64 174–181, 311 Lepetodrilus gordensis , 63, 64 Bulla , 210, 212 limpets , 9, 19, 31, 32, 37–52, 55–57, Bullia digitalis , 174, 175, 177 60–62, 68, 69, 72, 83, 90, 93, 116, Caenogastropoda , 32, 89, 90, 96, 97, 259, 260 123, 152, 153 Littoraria , 128, 131, 134–136 Cephalaspidea , 208–214 Littorina littorea , 128, 131, 132, 134, Chlorostoma funebralis , 72, 75 135, 320, 321 Collisella scabra , 49 Littorina obtusata , 128–131, 134 Crepidula , 120–123 Lobtaus galeatus , 113, 114, 310 Crucibulum , 116, 117 Lottia gigantea , 44, 49 Crysomallon , 60, 63–65 Melibe , 251, 252 cup-and-saucer , 97, 116–122 Nerita , 80–82 Cypraeoidea , 97, 138–146 neritidae , 80, 81, 83, 84 Dendronotina , 208, 237, 249–252 Neritimorpha , 32, 79–85 Diodora , 59, 61, 62 Patella argenvillei , 46 Elysia timida , 234–235 Patella compressa , 46 Emarginula , 61 Patella granatina , 46

1 The ancestral mode of feeding among sea snails was perhaps of an algal grazer over rocks (Section 2.4). However, sea snails of today exploit a wide variety of foods. This index classiﬁ es sea snail diets into the following categories: herbivores and detritivores, suspension feeders, bacteria feeders, feeders on dissolved organic matter, and carnivores. For each of these food categories a general list of sea snail groups is given. The transition between grazers and detritivores, and between predators and scavengers, is somewhat continuous. These categories are further sub-classiﬁ ed into aspects of feeding, where relevant: functional morphology, energy balance, food detection, feeding behaviour, boring hard skeletons, and use of venom

Patella longicosta , 46, 48–49 2. Suspension feeders Patella oculus , 49–51 2.1 general list of groups Patella vulgata , 40, 43, 45 Atlanta , 162– 163 Sacoglossa , 208, 228–236, 245 Capuloidea , 123, 124 Scutellastra cochlear , 46–48 Crepidula , 120–122 Siphonaria , 259–261, 263 Crucibulum , 116–117 Solariella , 73, 76 Crysomallon , 60, 63–65 Stromboidea , 97, 108–116, 123 cup-and-saucer , 97, 116–122 Strombus , 111, 112, 114, 303, 304, Dendronotina , 208, 237, 310, 315 249–252 Tegula funebralis , 72 Dendropoma , 123 Thecosomata , 208, 222–225 Dendropoma maxima , 106 Trochoidea , 60, 68–77, 123 Gadinalea , 261 Vetigastropoda, 32, 52, 55–77, 89, 90, Glaucus , 246 123 L. gordensis see Lepetodrilus Xenophora , 97, 114, 115 gordensis 1.1.1 gardening Lepetodriloidea , 63–65 Patella longicostata , 48 Lepetodrilus , 60, 63, 64 Scutellastra cochlear , 46–48 Lepetodrilus fucensis , 63, 64 1.1.2 feeding on chloroplasts, Lepetodrilus gordensis , 63, 64 photosynthesis Melibe , 251–252 Aeolidina , 244–245 Tenagodus , 102–103 Phyllodesmium , 245 Trichotropis , 124–125 Phyllodesmium hyalinum , 245 Trimusculus , 261 Sacoglossa , 229–232 Turritella communis , 101 1.2 functional morphology concerning Umbonium vestarium , 73–75 1.2.1 shell, body Vermetes triqueter , 105–107 Anaspidea , 215 Vermetoidea , 96–97, 104–107, 123 Patella compressa , 46 2.2 functional morphology concerning Sacoglossa , 229, 230 2.2.1 gill 1.2.2 trunk gill ﬁ lter feeding: general Caenogastropoda , 95, 152–159 comments , 122–125 Stromboidea , 108–116 Calyptraeoidea , 96–97, 116–123 1.2.3 radula Cerithioidea , 96–97, Caenogastropoda , 96, 123, 124 99–103, 123 limpets , 38, 41, 44, 46, Dendropoma petraeum , 104 51, 52, 56 Tenagodus , 102–103, 123 Neritimorpha , 79–80 Umbonium vestarium , 73–75 Patella compressa , 46 2.2.2 digestive tract Sacoglossa , 229–230 gill ﬁ lter feeding: general Siphonaria , 260 comments , 122–125 Thecosomata , 224 Gadinalea , 261 Vetigastropoda , 55–56, 79, 124 Melibe , 251–252 1.2.4 digestive tract Thecosomata , 222–225 Anaspidea , 216–218 Trimusculus , 261 Lepetodrilus , 63–64 Vermetes triqueter , 105–106 Sacoglossa , 229–232 1.2.5 photosynthesis Aeolidia papillosa , 244–245 3. Bacteria feeders Phyllodesmium , 245 Lepetodriloidea , 63–65 Sacoglossa , 229–232 Lepetodrilus gordensis , 63, 64 1.3 grazing behaviour Lepetodrilus , 60 , 63, 64 Anaspidea , 216 Lepetodrilus fucensis, 63, 64 1.4 energy balance L. gordensis see Lepetodrilus gordensis abalones , 68 Phenacolepadidae , 80, 82–83 Subject Index 3: Food and Feeding 349

4. Feeders on dissolved organic matter Lamellaria , 146 Bullia digitalis, 174–177 Melongena corona , 132–133 Mitridae , 188–189 Murexes , 174, 181–190 5. Carnivores Muricoidea , 181–190 5.1 general list of groups Naticoidea , 159–161 5.1.1 predating, scavenging Notocochilis gualteriana , 161 Acteon , 209 Nucella lapillus , 185, 319, 320 Aeolidia papillosa , 244, 245 Nudibranchia , 237–252 Aeolidina , 208, 237, 242–249 Onchidoris bilamellata , 240 Anthobranchia , 240 Ovulidae , 144–145 Archidoris pseudoargus , 240 Peltodoris atromaculata , 240 augers , 191–198 Philinopsis , 212 bubble shells , 209–214 Phylliroe , 250–251 Buccinoidea , 132, 153, 174–180 Phyllodesmium , 245 Buccinum undatum , 174, 177 Phyllodesmium hyalinum , 245 Caenogastropoda , 152, 153 Pleurotomarioidea , 65–66 Calliostoma , 76 Pneumodermopsis canephora , Calma glaucoides , 246 227–228 Carinaria , 163 Pneumodermopsis paucidens , Cassis , 154 227 C. geographus see Conus Stramonita , 183 geographus Terebridae , 197–198 Cephalaspidea , 209–214 Tonna , 154 Charonia , 158–159 Tonnoidea , 154–159 Chelidonura , 209, 212 Turridae , 191, 193 Colus stimpsoni , 109, 177 Urosalpinx , 122 Concholepas , 183 Voluta , 178 Cones , 153, 190–198 5.1.2 parasitising Conidae , 193, 197 Anthobranchia , 237–242 Conoidea , 191–198 Buccinoidea , 178 C. striatus see Conus striatus C. ungaricus see Capulus Conus , 193–196 ungaricus Conus geographus , 194–195 Cancellaria , 178 Conus striatus , 193–194 Capuloidea , 124 Conus textile , 111–112, 143, Capulus ungaricus , 124–125 193–194 Coralliophila , 189 Cratena , 243–244 Drupella , 187–188 Cratena peregrina , 243 Echineulima , 170 Cuthona nana , 244–245 Enteroxenos , 171–172 Cymatium , 157 Epitoniidae , 164–165 Dendronotina , 208, 237,249–252 Epitonium millecostatum , 164 Diodora , 61–62 Eulimoidea , 169–173 Drupella , 187–188 H. australis see Hipponix Favorinus branchialis , 246 australis Firoloida , 163 Heteropoda , 97, 153, 161–164 Hancockia , 249 Hipponix , 119 Hancockia schoeferti , 249 Hipponix australis , 119 Hancockia uncinata , 249 Marginellidae , 189 Harpa , 178 Melanella frieli , 170 Heteropoda , 161–164 Monogamus , 170–171 H. schoeferti see Hancockia Nutmegs , 178 schoeferti Ovulidae , 145 Hydatina , 210 Parenteroxenos doglieli , 173 350 Subject Index 3: Food and Feeding

Robillardia , 171 Eulimoidea , 169–172 Sabinella troglodytes , 170 Mitridae , 188–189 Stilifer , 171 Muricoidea , 181–190 Trichotropis , 125 Nutmegs , 174, 178–180 5.2 functional morphology concerning Tonnoidea , 154–159 5.2.1 shell, body 5.3 prey detection Predator functional morphology, Predator functional morphology, in in evolutionary perspective: evolutionary perspective: evolution evolution of predation of predation, 149–153 149–153 Bullia digitalis , 174–175 Clione limacina , 225–227 Drupella , 187–188 Enteroxenos , 171–172 Muricoidea , 181–190 Eulimoidea , 169–173 Urosalpinx , 122, 182–183 Gymnosomata , 225–228 violet shell , 166–168 Robillardia , 171 5.4 predatory behaviour Tonnoidea , 154–159 Acteon , 209 5.2.2 trunk Atlanta , 162–163 Predator functional morphology, Bullia digitalis , 174–175 in evolutionary perspective: Carinaria , 163 evolution of predation , Cassis , 154–155 149–153 Cladobranchia , 249 Buccinoidea , 174–180 Clione limacina , 228 Buccinum undatum , 177 Conus , 111–112, 193 Cymatium , 158 Cymatium , 157 Epitonium , 164 Drupella , 187–188 Pneumodermopsis , 227 Epitonium , 164–165 Robillardia , 171 Mitridae , 188–189 5.2.3 radula Naticoidea , 160–161 Predator functional morphology, Nutmegs , 178–180 in evolutionary perspective: Pneumodermopsis canephora , evolution of predation , 227–228 149–153 Tonna , 154 Buccinoidea , 174–176, 179 violet shell , 166–168 Conidae , 192, 193 5.5 attachment to prey Coralliophila , 189 Echineulima , 170 Epitonioidea , 164, 165 Heteropoda , 162, 163 Eulimoidea , 169 Gymnosomata , 227 Gymnosomata , 226 Monogamus , 170–171 Marginellidae , 190 Stilifer , 171 Muricoidea , 181–183, Pneumodermopsis , 227 187, 189, 190 5.6 boring hard skeletons Naticoidea , 160 Cassis , 154–155 Terebridae , 198 Naticoidea , 160–161 Tonna , 154 Muricoidea , 181–190 Turridae , 191 Stramonita , 183, 184, 290 5.2.4 digestive tract Urosalpinx , 182–183 Anthobranchia , 240 5.7 venom Buccinoidea , 174 Conidae , 192–193 Calma glaucoides , 246 Conoidea , 191–198 Cladobranchia , 249 Conus , 143, 193 Conidae , 193 Conus geographus , 193–195 Conus , 193 Conus purpurascens , 194 Gymnosomata , 225–228 Conus striatus , 193–194 Enteroxenos , 171–172 Stramonita , 183 Epitonium , 165 Terebridae , 197–198 Subject Index 4: Reproduction1

1. General list of groups Coralliophila , 189 Acmaea , 43 cowries , 32, 97, 138–145, 150, 156, 189, Acteon , 209 268–277 Aeolidiella glauca , 249 Crepidula aculeata , 120, 122 Aeolidina , 208, 237, 242–249 Crepidula convexa , 122 Alderia modesta , 233 Crepidula fecunda , 122 Amphibola crenata , 261–262 Crepidula fornicata , 120–122 Anaspidea , 208, 215–221 Crucibulum , 116, 117 Anthobranchia , 208, 237–242 cup-and-saucer , 97, 116–122 Austrocypraea , 143 Cuthona nana , 244 brush-snails , 32, 55–77, 89, 90, 96 Cymatium , 157, 158 bubble shells , 208–214 Cypraea , 139, 143, 268 Buccinum cyaneum , 177 Cypraeoidea , 97, 138–145 Buccinum undatum , 174, 177 Dendropoma petraeum , 104, 107 Bullia digitalis , 174, 175, 177 Diodora , 59, 61 C. aculeata see Crepidula aculeata Elysia timida , 234, 235 Calyptraeoidea , 97, 116–122 Enteroxenos , 171–173 Carychium , 263 Epitoniidae , 164–166 Cavolina , 222, 223, 225, 227 Eulimoidea , 97, 153, 169–173 Cephalaspidea , 209–214 Euspira catena , 161 Chelidonura , 209, 212 Haminoea , 210, 211 Chromodoris reticulata , 241 Hipponix , 117, 119 Clanculus bertheloti , 77 Hipponix australis , 119, 120 Colus stimpsoni , 109, 177 Hipponix cranoides , 118, 120 cones , 32, 97, 153, 190–198 Janthina , 166, 303 Conidae , 192, 193, 197 Janthina globosa , 169 Conuber , 161 Janthina janthina , 167, 169 Conus , 111, 143, 193–197 Jujubinus , 76

1 The ancestral mode of sea snail reproduction is of two sexes and of external fertilisation in the sea; the fertilised egg develops into the larval trochophore, which further develops into the larval veliger, which later metamorphoses to an adult (Section 2.5). This index classiﬁ es other modes of reproduction: internal fertilisation, sexual change from male to female (sequential hermaphroditism), simultaneous hermaphroditism, and imposex. It also classiﬁ es other reproductive aspects: courtship, parasperm, copulation, forms of egg laying, brooding, and direct embryonic development

Lacuna , 136 bubble shells , 212 Laevilittorina , 136 Cephalaspidea , 212 Limacina , 222, 224–227 Chelidonura , 212–213 Limacina inﬂ ata , 225 Elysia timida , 234 Limacina trochiformis , 224 Enteroxenos , 171 limpets , 9, 19, 32, 37–52, 55–57, 60–62, Haminoea , 210 69, 72, 83, 90, 93, 259–261 Navanax inermis , 212 Littorina littorea , 128, 132, 134, Palio , 240 136, 320, 321 Sacoglossa , 234 Littorinoidea , 97, 125–138 Turritella communis , 101 L. littorea see Littorina littorea Lobtus galeatus , 113, 310 murexes , 97, 153, 174, 181–190, 3. Copulation 193, 288, 303 Aeolidiella glauca , 249 Muricoidea , 97, 153, 174, 181–190 Aeolidina , 249 Naticoidea , 82, 97, 153, 159–161 Alderia modesta , 233 Navanax inermis , 212 Anaspidea , 217, 218 Neritidae , 80, 81, 83, 84 Anthobranchia , 240 Neritimorpha , 32, 79–85 bubble shells , 212 Notocypraea , 143 Cephalaspidea , 206, 212 Nucella lapillus , 185, 319, 320, 322 Chelidonura , 212–213 Opisthobranchia , 32, 153, 203, 205, 206, Chromodoris reticulata , 241–242 208, 209, 245, 246, 257, 258 Elysia timida , 234–235 Palio , 240, 241 Enteroxenos , 172 Polinices pulchellus , 161 Limacina trochiformis , 224 Pomatias , 137, 138 Littorina littorea , 134, 320–321 Pomatiidae , 137, 258 Littorinoidea , 136 Pulmonata , 32, 204, 205, 257, 258 Lobtaus galeatus , 113 Sacoglossa , 208, 228–237, 245 murexes , 190 S. gerula see Spectamen gerula Muricoidea , 190 Siphonaria , 259–261, 263 Navanax inermis , 212 Siphonaria serrata , 261 Opisthobranchia , 206, 245 Siphonarioidea , 259–261 Palio , 240 Siphopteron quadrispinosum , 213 Sacoglossa , 229 S. luteola see Solariella luteola Siphonaria , 261 Solariella luteola , 76 Siphonarioidea , 260 Solariella plicatula , 76 Siphopteron quadrispinosum , 213 Spectamen gerula , 76 Turritella communis , 101 Stilifer , 171 Stromboidea , 97, 108–116, 123 Tenagodus , 102–103, 123 4. Parasperm Trivia monacha , 146 Epitoniidae , 164–166 Trochus , 65, 69 Janthina globosa , 169 Turritella communis , 101 Vetigastropoda , 32, 52, 55, 56, 58, 60, 65, 66, 77, 89, 90, 123 5. Internal fertilisation Zoila , 143 Aeolidiella glauca , 249 Aeolidina , 242–249 Alderia modesta , 233 2. Courtship Anaspidea , 219 Aeolidiella glauca , 249 Buccinum undatum , 177 Aeolidina , 249 Bullia digitalis , 177 Alderia modesta , 233–235 cones , 194 Anaspidea , 234 Conidae , 193 Subject Index 4: Reproduction 353

Conus , 193 cowries, 142 cowries , 143 Crucibulum, 116, 117 Cypraeoidea , 142 cup-and-saucer, 97, 116–122 Limacina trochiformis , 224 Cymatium, 157, 158 Littorinoidea , 134 Cypraeoidea, 138 murexes , 190 Elysia timida , 134 Muricoidea , 190 Lacuna , 136 Naticoidea , 161 Laevilittorina, 136 Neritimorpha , 79 Limacina , 222 Opisthobranchia , 206, 207 Littorinoidea, 136 Palio , 240, 241 Lobtus galeatus, 113, 310 Tenagodus , 102, 103 Naticoidea, 97, 153, 159–161 Polinices pulchellus , 161 Pomatias, 137, 138 6. Eggs Pomatiidae, 137, 158 6.1 egg capsule Sacoglossa , 235 Anaspidea , 208, 215–221 6.4 nurse eggs Austrocypraea, 142 Buccinum cyaneum, 177 Bullia digitalis, 174, 175, 177 Colus stimpsoni, 109, 177 cones, 192–197 Conidae , 192, 193, 197 Conus, 192–197 7. Brooding cowries, 142, 146 Bullia digitalis , 177 Crepidula convexa, 122 C. aculeata see Crepidula aculeata Crepidula fecunda, 122 Clanculus bertheloti , 77 Cymatium, 157, 158 Coralliophila , 189 Cypraeoidea , 97, 138–146 Crepidula aculeata , 120, 122 Enteroxenos, 171–173 Crepidula convexa , 122 Epitoniidae , 164–166 Crucibulum , 117 Janthina globosa , 169 cup-and-saucer , 117 Littorinoidea, 136, 137 Dendropoma petraeum , 107 murexes, 189 Limacina inﬂ ata , 225 Muricoidea , 189 limpets , 51 Naticoidea , 161 Littorinoidea , 136 Neritidae , 81, 83, 84 S. gerula see Spectamen gerula Neritimorpha , 79, 81, 82 S. luteola see Solariella luteola Nucella lapillus, 185, 319, 320, 322 Solariella luteola , 76 Trivia monacha , 146 Solariella plicatula , 76 6.2 egg laying Spectamen gerula , 76 Anaspidea , 219 Tenagodus , 103 Coralliophila , 189 Trochus , 69, 70, 77 cowries, 144 Cymatium, 157, 158 Cypraeoidea , 142–144 8. Direct development Siphonaria, 259–263 Austrocypraea , 143 Siphonarioidea, 259–261 Buccinum undatum , 174, 177 6.3 egg mass Bullia digitalis , 174, 177 Acteon, 209 C. aculeate see Crepidula aculeata Anaspidea , 219 Carychium , 263 Austrocypraea, 143 Coralliophila , 189 cones, 195 cowries , 142 Conidae , 192, 193, 199 Crepidula aculeata , 120, 122 Conuber, 161 Crepidula convexa , 122 Conus , 194 Crucibulum , 116, 117 354 Subject Index 4: Reproduction

cup-and-saucer , 116, 117 Crepidula fornicata , 120–122 Cuthona nana , 244 Crucibulum , 116, 117 Cypraea , 143 cup-and-saucer , 116–122 Cypraeoidea , 143 Epitoniidae , 164–166 Dendropoma petraeum , 104, 105 Eulimoidea , 169–173 Elysia timida , 234 H. australis see Hipponix australis Euspira catena , 161 Hipponix , 117–119 H. australis see Hipponix australis Hipponix australis , 119, 120 H. cranoides see Hipponix cranoides Janthina , 166–169 Hipponix australis , 120 Limacina , 224 Hipponix cranoides , 120 Limacina inﬂ ata , 225 Janthina janthina , 166, 167 Limacina trochiformis , 224 Jujubinus , 76 limpets , 49, 259 Littorinoidea , 136 Stilifer , 171 Naticoidea , 161 Notocypraea , 143 Nucella lapillus , 322 10. Simultaneous hermaphrodites Pulmonata , 258 Acteon , 209 Sacoglossa , 231 Opisthobranchia , 206 Siphonaria , 259–261 Pulmonata , 257 Siphonaria serrata , 261 Sacoglossa , 228–236 Siphonarioidea , 259–261 Stromboidea , 112, 113 Tenagodus , 102, 103 Vetigastropoda , 32, 52, 55, 56, 58, 60, 65, Zoila , 143 66, 77, 89, 90, 123

9. Sequential hermaphrodites 11. Imposex Calyptraeoidea , 116–122 Littorina littorea , 320 Coralliophila , 189 L. littorea see Littorina littorea Crepidula fecunda , 122 Nucella lapillus , 319, 320, 322