FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. INSUFFICIENT INFORMATION FOR COVER Notice: © 1989 Stanford University Press. This manuscript is an author version with the final publication available and may be cited as: Lalli, C. M., & Gilmer, R. W. (1989). Pelagic snails: the biology of holoplanktonic gastropod mollusks. Stanford, CA: Stanford University Press. Pelagic Snails The Biology of Holoplanktonic Gastropod Mollusks Carol M. Lalli and Ronald W. Gilmer Stanford University Press Stanford, California 1989 Stanford University Press, Stanford, California © 1989 by the Board of Trustees of the Leland Stanford Junior University Printed in the United States of America CIP data appear at the end of the book Published with the assistance of the Harbor Branch Oceanographic Institute Preface The purpose of this book is to draw attention to some unusual and poorly known gastropods that are highly specialized for life in the open ocean. These mollusks, unlike most species in their phylum, live out their entire life cycles in an environment without solid substrates. Consequently, they have become adept at swimming or floating or attaching to drifting objects and, as members of the planktonic community, they have developed life styles quite different from those of their benthic relatives. Although these animals have been known and studied since the late sev­ enteenth century, much of the information has remained scattered in scien­ tific journals, expedition reports, or specialized monographs. Because this is particularly true of information relating to the biology and ecology of planktonic gastropods, the book concentrates on these topics. Less attention is given to taxonomy and distribution, since these areas have been consid­ ered fully in other works, but each chapter does conclude with a list of described species and references to published identification keys. Details of internal anatomy have also been neglected here, except where these are di­ rectly relevant to biological topics. We have often noticed, in working with students new to a scientific field, that many become overwhelmed by the sheer amount of literature that has accumulated and assume that there is nothing further to be discovered. To forestall this erroneous impression, we have tried to point out where pub­ lished observations are contradictory and where more research is needed. We have tried to use only photographs or drawings that accurately por­ tray living animals, to give the reader a more palpable sense of these unusual mollusks. Many previously published figures have represented pelagic mol­ lusks as they appear after collection by nets and rapid preservation in form­ aldehyde or alcohol; these often present distorted creatures that bear little or no resemblance to the live animals. Information on the biology of plank- vm Preface tonic gastropods often has been based upon interpretations of anatomical studies of preserved specimens. To correct or expand upon that earlier work, we have relied extensively upon recent and previously unpublished in situ biological observations of live animals. We hope that this book will prove useful to invertebrate zoologists, ma­ rine biologists, biological and geological oceanographers, zooplanktolo­ gists, and professional and amateur malacologists-and of interest to all those who appreciate the beauty and diversity of the adaptations of animals to their environments. We wish to acknowledge the generosity of Dr. T. R. Parsons and Dr. G. R. Harbison for providing space, technical facilities, and encouragement in this project. Some financial support for R.W.G. was provided by National Science Foundation grants OCE 82-09341 and OCE 85-16083 to G. R. Harbison. We also acknowledge the support of the Woods Hole Oceano­ graphic Institution, and we especially thank the Harbor Branch Oceano­ graphic Institution for providing publication expenses for the color figures. We thank Drs. M. Arai, P. Cornelius, and F. Boero for their helpful ad­ vice about the hydroids that grow on shelled pteropods, Dr. F. G. Hochberg for sharing his knowledge of the parasites that infect planktonic gastropods, and Dr. T. Pafort for discussions regarding her findings about reproduction in species of Clio. Dr. Catherine Thiriot very kindly supplied the scanning electron micrographs of radulae and larval shells of heteropods, and G. R. Harbison allowed us to use his unpublished observations and photographs of living Hydromyles. P. Linley provided technical assistance in preparing scanning electron mi­ crographs of radulae. B. Pratt, B. Rokeby, and E. Carefoot generously pro­ vided illustrative assistance, and T. Smoyer assisted in photographic re­ productions. Certain photographs were kindly provided by M. Jones, J. Carlton, and R. Reichelt. We also wish to thank the anonymous reviewer of the manuscript for the publisher. This work is contribution #61 5 of the Harbor Branch Oceanographic Institution. C.M.L. R.W.G. Contents I Introduction I References Cited 6 2 The Janthinid Snails Raft Builders 8 External Anatomy 9 Float Formation II Food and Feeding 12 Reproduction and Development 15 -- Epifauna and Parasites 20 Evolution 22 List of Recognized Species 23 References Cited 24 3 The Heteropods Visual Predators 27 External Anatomy 29 Swimming and Buoyancy 34 Food and Feeding 37 Reproduction and Development 44 Epifauna and Parasites 49 Shell Mineralogy and Sediments 50 Evolution 51 List of Recognized Species 52 References Cited 53 4 The Thecosomes Shelled Pteropods 58 External Anatomy 62 Swimming and Buoyancy 73 X Contents Food, Feeding, and Trophic Relationships 8o Reproduction and Development 100 Epifauna and Parasites 126 Pteropods as Ecological and Palaeoecological Indicators 13J Pteropods and the Carbonate Cycle 139 Evolution 145 List of Recognized Species 150 References Cited 152 5 The Gymnosomes Shell-less Pteropods 167 Swimming, External Anatomy, and Feeding Structures 168 Food and Feeding 178 Reproduction and Development 189 Parasites 199 Suborder Gymnoptera 199 Evolution 204 List of Recognized Species 208 References Cited 209 6 The Planktonic Nudibranchs Swimming Sea Slugs 214 Family Phylliroidae 215 Family Glaucidae 224 Family Fionidae 229 Evolution 232 List of Recognized Species 234 References Cited 234 Glossary 239 Systematic Index 249 Subject Index 253 Tables and Figures Tables I Major taxonomic divisions of the Phylum Mollusca 2 2 Major taxonomic divisions of the holoplanktonic gastropods 4 3 Characteristics of egg capsules and numbers of young produced by oviparous species of Janthina 20 4 Respiration rates of Cardiapoda placenta 4 3 5 In situ swimming rates of thecosomes 7 5 6 Relationship between shell length and the diameter of mucous feeding webs of euthecosomes 84 7 Gut-content analyses in the Limacinidae 8 5 8 Gut-content analyses in the Cavoliniidae 87 9 Gut-content analyses in the Pseudothecosomata 92 IO Chemical constituents of Euthecosomata 94 I I Minimal energy requirements and assimilation efficiency of carbon for Cavolinia longirostris 97 I 2 Respiration and ammonium-excretion rates of Corolla sp. and Gleba cordata 98 I 3 Numbers of egg masses and eggs deposited by Limacina helicina and L. retroversa I 04 14 Growth rates and times required to attain maturational stages in tropical species of Limacina I09 I 5 Size relationships of mating cavoliniids I IO I6 Hydrozoan epifauna associated with euthecosomes 128 I7 Infestation of euthecosomes by the parasitic copepod Cardiodectes medusaeus I30 I 8 Relative population densities of dominant euthecosomes in the plankton and in sediments off Barbados, West Indies I 3 6 I9 Sinking rates of euthecosomes under experimental conditions I 4 3 XII Tables and Figures 20 Feeding structures in gymnosome genera 174 21 Comparison of numbers of Limacina retroversa and L. helicina eaten by Clione limacina r8r 22 Growth and feeding rates for Clione limacina fed on either large or small Limacina retroversa 184 23 Prey species of gymnosomatous pteropods r88 24 Fecundity of Paedoclione doliiformis at different temperatures and food concentrations 193 25 Numbers of eggs produced by Clione limacina from the Denmark Strait and Labrador Sea 197 Figures I Janthinid snails IO 2 Radular teeth of Janthina prolongata 13 3 Reproductive anatomy of Janthina pal/ida 16 4 A spermatozeugma of Janthina pal/ida 17 5 Egg capsules of Janthina umbilicata 19 6 A janthinid veliger shell 21 7 Atlantid heteropods 29 8 Carinariid heteropods 31 9 Pigmentation in Cardiapoda species 32 IO Pterotracheid heteropods 33 II A quiescent atlantid heteropod with attached mucous strands 36 12 Heteropod radulae 38 13 Heteropod veliger larvae 46 14 Veliger shells of heteropods 47 15 Limacina retroversa 62 16 Limacina helicina 63 17 Cavoliniid thecosomes 64 18 Mantle appendages of Cavolinia uncinata 66 19 Peraclis reticulata 67 20 Comparative morphology of Limacina, Peraclis, and Cymbulia 68 21 Corolla sp. 70 22 Gleba cordata 71 23 Desmopterus papilio 73 24 Swimming in Limacina retroversa 74 25 Feeding in euthecosomes 81 26 Cavolinia uncinata feeding with a mucous web 82 27 Radular teeth of thecosomes 83 Tables and Figures Xlll 28 Feeding in pseudothecosomes 89 29 Gleba cordata in the feeding position 90 30 Particle-size distribution of food captured in the feeding webs of Gleba cordata 9I 31 Reproductive anatomy of Limacina IOI 32 Reproduction in Limacina helicina I02 33 Developmental stages of Limacina retroversa I05 34 The veliger of Limacina