The. Cell Biology. Sponges

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1 The Cell Biology of Sponges

2 Tracy L. Simpson The Cell Biology of Sponges With 221 Figures Springer-Verlag New York Berlin Heidelberg Tokyo

3 Tracy L. Simpson Department of Biology and Health Science University of Hartford West Hartford, Connecticut Library of Congress Cataloging in Publication Data Simpson, Tracy L., The cell biology of sponges. Bibliography: p. Includes index. 1. Sponges-Cytology. 2. Porifera-Cytology. I. Title. QL371.S ' by Springer-Verlag New York Inc. Softcover reprint of the hardcover 1 st edition 1984 All rights reserved. No part of this book may be translated or reproduced in any form without written permission from Springer-Verlag, 175 Fifth Avenue, New York, New York 10010, U.S.A. The use of general descriptive names, trade names, trademarks, etc., in this publication, even if the former are not especially identified, is not to be taken as a sign that such names, as understood by the Trade Marks and Merchandise Marks Act, may accordingly be used freely by anyone. Typeset by BiComp, Inc., York, Pennsylvania ISBN -13 : DOl: / e-isbn-13:

4 In Memory of Rebecca (Rita) Simpson, Whose spontaneous magnetism for and joy in Nature will always be with those who knew her.

5 Foreword Modem biology owes much to the study of favorable model systems which facilitates the realization of critical experiments and results in the introduction of new concepts. Examples of such systems are numerous and studies of them are regularly recognized by the scientific community. The 1983 Nobel Prize in Medicine and Physiology is a magnificent example in which com plants served as the experimental model. In a manner somewhat more modest, other biological systems have attracted recognition due to their critical phylogenetic position, or indeed because of their uniqueness which distinguishes them from all other organisms. Assuredly, among the whole assemblage ofliving organisms, sponges stand out as worthy of interest by scientists: they are simultaneously models, an important group in evolution, and animals unlike others. As early as the beginning of this century, sponges appeared as exceptional models for the study of phenomena of cell recognition. Innumerable works have been dedicated to understanding the mechanisms which assure the reaggregation of dissociated cells and the reconstitution of a functional individual. Today, research on these phenomena is at the ultimate, molecular level. Through an assemblage of characteristics the sponges are, based upon all available evidence, the most primitive Metazoans. Their tissues-perhaps one can say their cell groups-are loosely assembled (they possess no tight or gap junctions), cell differentiation appears highly labile, and they do not develop any true organs. But, they are most certainly Metazoans. They contain an intercellular milieu rich in collagen and are capable of coordinating their cellular activities in order to attain a significant degree of integration. However, the sponges are des animaux a part. They are able to accumulate silica, to form gametes from somatic cells with digestive function, and to realize fantastic potentialities for asexual reproduction; one group even includes individuals which are syncytial! Most of these aspects of sponges generate interest among biologists, whether they are specialists in evolution, cell biologists, or molecular biologists. The goal which Tracy L. Simpson has wished to accomplish during his labors for the past nine years is to offer a comprehensive work on the structure and function of sponge cells which is for all scientists and at the same time completely up-to-date. In order to understand the originality of this work, perhaps it is necessary to consider two questions: what need does this book fulfill and how does it do so? There exist few reviews on sponges even though the literature is abundant-the author annotates almost 900 references. In some reviews, different research groups ignore the work of other groups (in particular in the field of cell aggregation) and literature citations are often incomplete. In certain general works,

6 viii Foreword previous research is reviewed, but without critique, and some of this data is even obsolete. Too many syntheses of specific areas are only bibliographic compilations without a true perspective. Finally, some excellent works are either focused only on a very specific subject or are published volumes based upon symposia. What is required, then, is a "critical synthesis" which is both broadly based and current. This need is becoming more acute as sponges begin to be considered as models, attracting, for example, molecular biologists whom, among others, need objective synthetic information. To respond to such a need has not been easy. T. L. Simpson has adopted an approach to each chapter which is most rewarding. He presents very complete analyses and I am sure that few papers have escaped his attention. But, he also presents a personal synthesis which makes the work highly interesting since for the most part this has not previously been accomplished. This synthesis is artfully supported by numerous tables which serve as mini-reviews. For example, one of the strong points of the book is a detailed consideration of the kinds of sponge cells. The published data permit the grouping of certain diverse cell types within one assemblage-"special cells." Each type is reviewed in the text and then all of the special cells are treated in a table which is extremely detailed, including numerous references. One will equally note numerous review tables, particularly in the chapters on mineralization and reproduction. Furthermore, this book is rendered unusual in the number and quality of its illustrations: almost 600 illustrations, of which more than 500 are photographs, the vast majority being electron micrographs. The tables and illustrations make this work very convenient to consult and give to it an exceptional, informative quality. While this book is most assuredly not a general presentation on the sponges, it permits the nonspecialist to grasp the nature of these primitive animals. Although it encompasses data corresponding to more than a century ofliterature, this volume is not a treatise; it presents numerous synthetic views which carry the mark of their author. The truth is that this work is unique and that it does not correspond even slightly to any other existent work. The basic morphological data which introduce this book will be very useful for all those who have an interest in sponges, both in research and teaching. The following chapters focus on the definition, the structure and-where known-the function of sponge cells. It has not been easy to clarify the diverse terminologies employed in the literature when reconsidering older views in light of the most recently available data. The result is, however, most satisfactory and extremely informative. A large place is given to biomineralization-it is without doubt due to a visible concern of the author for a subject which is dear to him. Beyond descriptions, sometimes complex, of diverse mineral forms encountered among the sponges, discussions are presented of general problems of the concentration or dissolution of minerals. A complete chapter is devoted to the aquiferous system-its organisation and its activities. At first sight this material appears to be of specific interest for spongologists, who will find there all of the detailed anatomical terminology. The fundamental analysis which is presented supports the view that sponges are animals capable of behavioral integration. This view is

7 Foreword ix substantiated by observations on the water current which traverses these animals, on the effects of different factors on the current, and on studies of the anatomy and cellular structures which assure its regulation. There is no other equivalent synthesis of these data; such is essential for all researchers who are concerned with the evolutionary emergence of neuroid and muscular functions. The last sections of the volume deal with the developmental biology of sponges: gametogenesis and sexual reproduction, asexual reproduction, regeneration, cell recognition, and cell differentiation. A comprehensive view of this field has been needed for some time. Finally, I further like this book because more than assembling information, more than offering a focus on subjects of much interest, the book very often emphasizes the uncertainties and the obscurities; and it indicates possible paths which might be taken. What could be more stimulating when one has an interest in a discipline than to note that all is not known and that the questions which remain unanswered are still more passionate than those for which there have been-provisionally-a response? November, 1983 Villeurbanne, France ROBERT GARRONE Maitre de la Recherche, C.N.R.S. Laboratoire D'Histologie et Biologie Tissulaire Universite Claude Bernard

8 Preface The writing of this work was stimulated by discussions with colleagues in the fields of biochemistry, developmental biology, and physiology who expressed their, and other's, need for a current, critical review and analysis of sponge cell biology, and secondly by my own conviction that the field of sponge biology in general could benefit from such a synthesis and evaluation of the data. The major problem faced in writing this book was that of balancing the text relative to presenting, on the one hand, a review of the data and, on the other hand, a synthesis of it. A vigorous attempt has been made to be as uniform as possible in reviewing data but this, of course, is not always possible because some papers stand out as key advances in one or more areas. To the extent that it has been feasible to synthesize specific perspectives or to emphasize deficiencies in knowledge, these have been done. A major effort is made to review cellular structure per se since this has not previously been attempted. Some speculations are also to be found and these, hopefully, will not only stimulate new investigations but will also serve as respites from the unavoidable rigidity of data review. Much effort has been expended to avoid errors, although it is probably not possible in an undertaking of this scope to finally arrive at an error-free state. For such of those that do occur by omission or otherwise, I take full and sole responsibility. There are a number of important, recent monographs and symposial volumes which contain much information on sponge cell biology as well as other topics. Outstanding among them is Biologie des Spongiaires (C. Levi and N. Boury Esnault, Eds., Editions de CNRS, Paris). Others include Biology of the Porifera (W. G. Fry, Ed., Acad. Press), Aspects of Sponge Biology (F. W. Harrison and R. R. Cowden, Eds., Acad. Press), Phylogenesis of Connective Tissue. Morphological Aspects and Biosynthesis of Sponge Intercellular Matrix (by R. Garrone, S. Karger), Sponges (by P. R. Berquist, Univ. Calif. Press), Spongiaires (P-P. Grasse, Ed., Traite de Zoologie, Tome III, Fasc. I, Masson et Cie, Paris), and Living and Fossil Sponges (by W. D. Hartman, J. W. Wendt, and F. Wiedenmayer, Univ. Miami). Furthermore, there are numerous recent symposial volumes which include important contributions such as Nutrition in the Lower Metazoa, Phylogeny of Immunological Memory, Silicon and Siliceous Structures in Biological Systems, Cell-Cell Recognition, Biology and Systematics of Colonial Organisms, and Fourth European Marine Biology Symposium, among others. The demanding reader will doubtless want to refer to some of the above works as well as to the original literature for further details, particularly as concerns experimental technique.

9 xii Preface A decision was made that one effective, useful, and accurate means of reviewing data is to include original illustrations contributed directly by researchers and this has been done extensively. In this way and textually throughout the volume an effort is made to convey appropriate recognition of the endeavors and dedication of all those who strive to more fully comprehend sponge cell structure and function. September, 1983 TRACY L. SIMPSON

10 Acknowledgments Numerous individuals have aided in this labor and for their help, assistance, and encouragement I am most grateful. Lynn D. Simpson, my wife, has freely and generously given of her time and efforts for typing substantial portions of the manuscript and for aiding in numerous technical problems and details. Fran Libbey, science librarian, has in many instances been instrumental in securing essential literature; Paula Stein has meticulously assisted with the compilation of the bibliography. Emily Barrett, department secretary, has been exceedingly helpful and offered assistance in numerous instances. Furthermore, I am very appreciative of the interest, tolerance, and support offered me during the preparation of this work by my colleagues in the Department of Biology and Health Sciences. I express my gratitude and thanks to the following researchers of sponges whose interest in this book is exemplified by the original photographic materials which they have generously provided: Roland M. Bagby, Nicole Boury-Esnault, Hagen Bretting, Max M. Burger, Marco Buscema, Dominique Carriere, Robert Connes, A. S. G. Curtis, Danielle DeSutter, Louis De Vos, Jean-Pierre Diaz, Claude Donadey, Ryan W. Drum, Clive W. Evans, Paul E. Fell, Marie-France Gallissian, Robert Garrone, John J. Gilbert, Willard D. Hartman, William H. Hildemann, Doris Hohr, Susie Humphreys, Tom Humphreys, M. FischelJohnson, W. Clifford Jones, Ernest F. Kilian, Paul-Friedrich Langenbruch, Philip W. Ledger, Claude Levi, Hideo Mukai, W. E. G. Miiller, Max Pavans de Ceccatty, Shirley A. Pomponi, Jacqueline Pottu-Boumendil, Henry M. Reiswig, Francine Rozenfeld, Klaus Rutzler, Michele Sara, Lidia Scalera-Liaci, llse Schmidt, Van Elliot Smith, Ole S. Tendal, Kenneth M. Towe, Jean Vacelet, Gysele Van de Vyver, Yoko Watanabe, Norbert Weissenfels, Clive R. Wilkinson, Craig E. Williamson, and Phillipe Willenz. I sincerely hope that their expectations are fulfilled. Aspects of this work have been discussed with numerous individuals. Most especially, Willard D. Hartman has taken a constant interest in its progress and revisions by offering his seemingly endless knowledge of sponges. I am indebted to Robert Garrone who has conscientiously and thoroughly read the manuscript and has suggested important revisions. In addition, I am particularly appreciative for discussions with Max Pavans de Ceccatty, Gysele Van de Vyver, Louis De Vos, Max M. Burger, Norbert Weissenfels, Philip W. Ledger, John J. Gilbert, William H. Kuhns, Robert S. Turner, and Paul Langenbruch, and Gideon A. Rodan. The University of Hartford generously provided support through its facilities and a small grant was made available through the Vincent Coffin Fund to aid in the final preparation of the bibliography. The final revisions and editing of this work were accomplished during a sabbatical leave from the University of

11 xiv Acknowledgments Hartford and an extended leave of absence as a Foreign Exchange Scientist in the U.S.-France Cooperation in Science Program sponsored jointly by the Centre National de la Recherche Scientifique (France) and the National Science Foundation (U.S.A.). Finally, to my father, George Simpson, I am indebted for his enthusiastic interest, suggestions, and most especially for his professional expertise in matters pertaining to book publication. September 1983 T. L. S.

12 Contents Morphology 1. FUNCTIONAL MORPHOLOGY AND MORPHOLOGICAL VARIATION 1 General Features 1 Functional Morphology 4 Variation in Morphology: The New Systematics 5 Skeletal Morphology 5 Spicule Geometry as a Major Morphological Feature 12 Other Morphological, Reproductive and Biochemical Features 15 Morphological Variation in the Phylum 15 Cellular Structure 2. THE EPITHELIA 42 Pinacocytes (Excluding Hexactinellids) 42 Choanocytes (Excluding Hexactinellids) 53 Variation in Cell Shape 61 Pinacoderm and Choanoderm in Hexactinellida 64 Contractile Vacuoles and Water Balance CELLULAR COMPONENTS OF THE MESOHYL 70 Cell Types and Structure 71 Archeocytes, Polyblasts, Thesocytes 74 Spongocytes, Gemmular Epithelium, Lophocytes, Trophocytes, Megasclerocytes 79 Histoblasts, Collencytes, Fiber Cells, Myocytes, Neuroid Cells 83 Microsclerocytes 89 Special Cells-Cellules a Inclusions 90 Summary of Special Cells 108 The Cortex 110 Cords of Cells 113 Symbionts 114 Cyanobacteria 114

13 xvi Contents Zooxanthellae Zoochlorellae Bacteria Some Problems in Symbiont-Host Relationships Pigment Cellular Functions CALCIFICATION, SILICIFICATION, BIOEROSION Calcareous Deposits: Morphology, Chemistry, Distribution Calcareous Spicules Calcareous Scales Cemented Calcareous Spicules Aspicular Calcareous Deposits The Secretion of Calcareous Spicules Factors Affecting Calcareous Spicule Secretion Morphogenetic and Developmental Aspects of Calcareous Spicule Secretion The Secretion of Other Calcareous Structures Siliceous Deposits: Morphology, Chemistry, Distribution Siliceous Spicules of Demosponges Siliceous Scales Siliceous Spicules of Hexactinellids Cemented Siliceous Spicules Entrapped Siliceous Spicules The Secretion of Siliceous Spicules Demosponges Hexactinellids Factors Affecting Siliceous Spicule Secretion Morphogenetic and Developmental Aspects of Siliceous Spicule Secretion The Secretion of Other Siliceous Structures Iron Containing Deposits Excavation of Calcareous Substrata General Features of Burrowing and the Species Involved Cellular Basis of Etching Mechanisms of Burrowing Morphogenetic Aspects of Burrowing COLLAGEN FIBRILS, SPONGIN, MATRIX SUBSTANCES Collagen: Morphology, Chemistry, Distribution Collagen Fibrils Spongin Fibers

14 Contents xvii Gemmule Coats 227 Collagen Synthesis and Secretion 232 Biochemical Aspects of Collagen Synthesis 232 Cellular Aspects of Collagen Secretion 235 Other Organic Products 244 Biochemical Studies 244 Cytochemical and Morphological Studies 245 Fibronectin 251 Morphogenetic and Developmental Aspects of Organic Matrix Substances CANAL SYSTEM STRUCTURE AND ACTIVITIES 255 Ostia 255 Structure in Calcarea 256 Structure in Demospongiae 257 Structure in Hexactinellida 258 Development 258 Incurrent Canals 260 Inhalant "Organs" 260 Papillae 264 Other Patterns 264 Cellular Features 266 Development 269 The Terms Prosopyles and Apopyles 269 Aphodal, Diplodal, Asconoid, and Syconoid Arrangements 271 Pinacocytic Prosopyles 271 Choanocytic Prosopyles 272 Choanocyte Chambers 273 Structural Heterogeneity of Chambers 276 Development 278 Choanocytic Apopyles 280 Pinacocytic Apopyles 283 Excurrent Canals 284 Structure 284 Development 285 Morphological Patterns 286 Oscules 288 Morphological Types 288 Cellular Features 289 Development 292 Canal System Elements in Reproductive Stages 292 Water Currents 294 Origin and Direction 294 Transport Rates and Velocities 299 Types of Changes in Water Transport 300

15 xviii Contents Effectors Which Directly Influence Water Currents Responses of Effectors to Experimental Stimuli Spontaneous Changes in Water Currents Environmental Factors Influencing Water Currents Intrinsic Control of Water Currents Coordination by Neuroid Cells Feeding Retention of Particulates Sites of Entrapment-Ingestion Distribution and Digestion Elimination Development GAMETE, EMBRYO, LARVAL DEVELOPMENT General Features of Sexual Reproduction Gametogenesis Spermatogenesis Oogenesis Nurse Cells Factors Influencing Gametogenesis Temperature Size of Animals Age and Other Factors Sex Determination Gamete Release Fertilization Cleavage Somatic Cells Associated with Embryos Polarity, Micromeres, Macromeres Larval Formation Larval Structure Processes in Larva Formation Reports of Asexually Formed Larvae Embryo and Larva Release Attachment of Larvae to the Substratum The Problem of the Polarity of the Larva Larval Metamorphosis Experimental Embryology BUDS, GEMMULES, TISSUES REGRESSION Buds Fragmentation: A Special Case of Budding

16 Contents XiX Budding 416 Gemmules 425 Occurrence of Gemmule Producing Species 427 Life Cycles Involving Gemmules 428 The Gemmule Envelope 428 The Gemmular Cells-Thesocytes 438 Gemmule Formation in Spongillids 445 Gemmule Formation in Marine Species 459 Determinants of Gemmule Formation 462 Gemmule Dormancy 467 Gemmule Germination 474 Gemmule Hatching 494 Tissue Regression 500 A Special Case of Tissue Regression: Reduction Bodies GROWTH, REGENERATION, CELL RECOGNITION, PERSPECTIVE ON CELL DIFFERENTIATION 510 Growth 510 Initiative Growth 511 Maturational Growth 513 Remodeling 517 Growth as an Increase in Size or Volume 523 Experimental Regeneration 526 Explants 527 Transection of Whole Animals 528 Tissue Ablation 529 Tissue Recognition 536 Reaggregation and Reconstitution of Dissociated Cells 551 Perspective on Cell Differentiation 577 REFERENCES 583 INDEX 627

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