Biology of the Integument 1 Invertebrates

Edited by 1. Bereiter-Hahn . A.G. Matoltsy K. Sylvia Richards

With 298 Figures

Springer-Verlag Berlin Heidelberg New York Tokyo 1984

Prof. Dr. JURGEN BERElTER-HAHN Fachbereich Biologie der UniversiHit, Kinematische Zellforschung Postfach 111932, D-6000 Frankfurt a.M./FRG

Prof. Dr. A. GEDEON MATOLTSY Boston University School of Medicine, Department of Dermatology 80 East Concord Street, Boston, MA 02118/USA

Dr. K. SYLVIA RICHARDS Department of Biological Sciences, University of Keele Keele, Staffordshire ST5 5BG/GB

ISBN 978-3-642-51595-8 ISBN 978-3-642-51593-4 (eBook) 10.1007/978-3-642-51593-4 DOI

Library of Congress Cataloging in Publication Data; Library of Congress Catalog­ing in Publication Data. Main entry under title: Biology of the integument. Bibliog­raphy: p. Includes index. Contents: v. 1. Invertebrates. 1. Skin-Collected works. 2. Body covering (Anatomy)--Collected works. 1. Bereiter-Hahn, Jiirgen. II. Ma­toltsy, A. Gedeon. III. Richards, K. Sylvia. QP88.5.B565 1984 591.1'858 83-20351

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Preface

The integument plays an important role in the survival of meta­zoans by separating and protecting them from a hostile environ­ment. Its function ranges from protection against injury and in­fection; partlcipation in the regulation of body temperature and water balance, to respiratory activity, monitoring of the environ­ment and production of signals related to behaviour. All these result from specific structural, biochemical and physiological properties of intra- and extracellular components of the integu­ment. Thus its characterization can be best accomplished by a multidisciplinary approach with authors specialized in different fields of science.

This multi-author book, in two volumes, provides an up-to­date survey of the literature. The first volume deals with the integument of invertebrates, the second with that of vertebrates, both organized primarily on a phylum basis. As the level of knowledge on the integument of phyla differs considerably, the information provided is correspondingly either limited or con­densed. For some of the smaller groups of invertebrates little information is available, as often only a few electron micrographs are to be found in the literature; on the other hand, from the large body of knowledge existing for vertebrates, particularly for mammals, no complete overview can be provided, but publica­tions giving access to further information have been reviewed critically. A compilation of the knowlege on the animal integu­ment is at the same time a compilation of the gaps; it is hoped that this monograph will stimulate further research in skin biolo­gy. The articles were written primarily for researchers, but some background information is also included for interested students and teachers. No comparable text dealing with all the invertebrate phyla or even all the vertebrate classes exists in the literature.

A book on Skin biology was proposed originally by Dr. Czeschlik of Springer-Verlag. It has been an attractive and chal­lenging task for the editors to evaluate the literature and select subjects for these volumes. We received valuable advice from many colleagues, including Professors C. Arme (Keele), F.G. Barth (Frankfurt), D.T. Downing (Iowa City), R.M. Rieger

VI Preface

(Chapel Hill) and G.E. Rogers (Adelaide), to all of whom we are indebted as also to all the authors for their contributions to this work. The cooperation of the Publishers has been greatly appreciated.

J. BEREITER-HAHN

A.G. MATOLTSY

K.S. RICHARDS

Contents

I Introduction, Intercellular Junctions and Cilia

1 Introduction. K.S. RICHARDS 1

2 Intercellular Junctions. C.R. GREEN. (With 10 Figures) 5

2.1 Introduction 5 2.2 Desmosomes 6 2.3 Gap Junctions 8 2.4 Septate Junctions 10 2.5 Tricellular Junctions 12 2.6 Tight Junctions 14

3 Cilia. M.J. SANDERSON. (With 7 Figures) 17

3.1 Introduction 18 3.2 Ciliary Beat Patterns 19 3.3 Ciliary Structure 23 3.4 Mechanisms of Ciliary Motility 30 3.5 Control of Ciliary Activity 35

II The Diploblastic Level

4 Introduction to the Diploblastic Level. G.O. MACKIE 43

5 Cnidaria: Cell Types. M. HiiNDGEN. (With 5 Figures) 47

5.1 Introduction 47 5.2 Epithelial Cells 48 5.3 Mucous Cells 52 5.4 Nerve Cells 52 5.5 Sense Cells 54 5.6 Interstitial Cells 54

6 Cnidaria: Cnidae. R.N. MARISCAL. (With 8 Figures) 57

6.1 Introduction 57 6.2 Terminology 58 6.3 The Structure of Cnidae 59 6.4 The Functioning of Cnidae 62

VIII Contents

6.5 The Functions of Cnidae 64 6.6 The Chemistry of Cnidae 65 6.7 Conclusions. . . . . . 66

7 Cnidaria: Secreted Surface. J.G. TIDBALL 69

7.1 Introduction .......... 69 7.2 Settlement and Attachment . . . . 69 7.3 Food Capture and Surface Cleaning 71 7.4 Self-Recognition . . . . 73 7.5 Support and Protection . . . . . . 74 7.6 Conclusion and Questions . . . . . 76

8 Cnidaria: Permeability, Epidermal Transport and Related Phenomena. D. SCHLICHTER. (With 10 Figures) ........... 79

8.1 Introduction . . . . . . . . . . . 79 8.2 Permeability Properties of Apical Epidermal

Membranes . . . . . . . . . . . . . . 80 8.3 Other Phenomena Related to the Outer Epidermal

Surface . . . . . . . . . . . . . . . . . .. 91

9 Ctenophora. M.-L. HERNANDEZ-NICAISE. (With 7 Figures) 96

9.1 Introduction 96 9.2 Glandular Cells 97 9.3 Ciliated Cells (Other than Locomotory) 98 9.4 Single Sensory Cells 99 9.5 The Locomotory System ...... 101 9.6 Apical Organ . . . . . . . . . . . 103 9.7 The Integument of the Tentacles: the Colloblast 107 9.8 Other Cell Types ............. 109

ill Acoelomata

10 Turbellarian Platyhelminths. S. TYLER. (With 21 Figures) ..... . 112

10.1 Introduction . . . . . . 112 10.2 Morphology of Epidermal Cells 113 10.3 Cell Web . . . . . . . . . . 119 10.4 Intercellular Junctions .... 121 10.5 Ultrarhabdites and Other Secretory Products of

Epithelial Cells (" Epitheliosomes") 123 10.6 Extracellular Matrices ....... 125 10.7 Cilia . . . . . . . . . . . . . . . 126 10.8 Non-Epithelial Cells of the Body Wall 126 10.9 Epidermal Growth and Replacement 127 10.10 Phylogenetic Significance . . . . . . 128

Contents IX

11 Parasitic Platyhelminths. L.T. THREADGOLD. (With 25 Figures) .......... . 132

11.1 Introduction ............... 132 11.2 Trematoda: Larval Stages Monogenea, Digenea, and

Aspidogastrea . . . . 133 11.3 Trematoda: Adult . . 156 11.4 Cestoda: Larval Stages 163 11.5 Cestoda: Adult 178 11.6 Summary . . . . . . 184

12 Platyhelminth Host-Parasite Interface. A.D. BEFus and R.B. PODESTA . . . . . . . . . . . . . 192

12.1 Introduction ............... 192 12.2 The Structure and Function of Parasite Surfaces 193 12.3 Properties of the Surface Membrane and Interface 194 12.4 Host-Parasite Interface and Adhesiveness . . . . . 195 12.5 Survival Tactics of Parasites Confronted by Effectors

of Host Resistance . . . . . . . . . . . . . . . 196 12.6 The Host-Parasite Interface: Some New Directions 199 12.7 Conclusion . . . . . . . . . . . . . 200

13 Nemertea. R. GIBSON. (With 6 Figures)

13.1 Introduction ..... 13.2 Ciliated Supporting Cells 13.3 Gland Cells . . . . 13.4 Epidermal Enzymes 13.5 Sensory Cells 13.6 Basal Cells .... 13.7 Other Epidermal Features

IV Pseudocoelomata

14 Nematoda. A.F. BIRD. (With 9 Figures)

14.1 Introduction 14.2 Cells 14.3 Cuticle 14.4 Conclusion

· 205

· 205 · 207 · 207 · 208 · 209 · 210 · 210

· 212

· 212 · 213

218 230

15 Acanthocephala. P.J. WHITFIELD. (With 2 Figures) 234

15.1 Introduction . . . . . . 234 15.2 Structural Organization . . . . . . . 235 15.3 Integumentary Nutrient Uptake . 238

16 Minor Pseudocoelomates. V. STORCH. (With 12 Figures)

16.1 Introduction 16.2 Gastrotricha

242

242 243

X Contents

16.3 Kinorhyncha · 247 16.4 Rotifera · 250 16.5 Priapulida · 254 16.6 Nematomorpha · 258 16.7 Kamptozoa (Entoprocta) 261 16.8 Gnathostomulida · 263

V Annelida

17 Epidermal Cells. U. WELSCH et al. (With 12 Figures) 269

17.1 Introduction 269 17.2 Supporting Cells 272 17.3 Basal Cells 278 17.4 Gland Cells 278 17.5 Sensory Cells · 284 17.6 Gills · 289 17.7 Clitellum · 290

18 Chaetae. P.C. SCHROEDER. (With 3 Figures) . 297

18.1 Introduction . 297 18.2 Structure . . . 299 18.3 Composition 301 18.4 Development 304

19 Cuticle. K.S. RICHARDS. (With 11 Figures) 310

19.1 Introduction 310 19.2 Ultrastructure . . . . . . 310 19.3 Histochemistry ..... 315 19.4 Biophysics and Biochemistry 315 19.5 Subcuticular Bacteria . . . 318 19.6 Function . . . . . . . . 319

20 Permeability and Epidermal Transport. J. GOMME . • . • • . . . . . 323

20.1 Introduction ........ 323 20.2 Terminology and Basic Concepts 324 20.3 Exchange of Respiratory Gases 325 20.4 Transpiration . . . . . . . . 326 20.5 Water Permeability in Aquatic Annelids 328 20.6 Monovalent Ion Transport in Freshwater Annelids 332 20.7 Ion Transport in Terrestrial Annelids? ..... 337 20.8 Monovalent Ion Transport in Brackish-Water and

Marine Annelids . . . . . . . . 338 20.9 Transport of Other Ions .... 345 20.10 Transport of Organic Compounds 346 20.11 Role of the Cuticle 355 20.12 Conclusion . . . . . . . . . . 358

Contents XI

VI Annelid-Related Phyla and Cuticle Evolution

21 Echiura and Sipuncula. V. STORCH. (With 3 Figures) 365

21.1 Echiura . 365 21.2 Sipuncula 372

22 Pogonophora. E.C. SOUTHWARD. (With 5 Figures) 376

22.1 Structure 376 22.2 Permeability 384

23 Evolution of the Cuticle in the Lower Eumetazoa. R.M. RmGER. (With 2 Figures) 389

23.1 Introduction and Definitions 389 23.2 On the Origin of True Cuticles 390 23.3 The Primitive Condition of True Cuticles 390 23.4 The Lines of Cuticle Specializations Within the

Cnidaria and the Lower Bilateria 391 23.5 The Function of Primitive Eumetazoan Cuticles 396

VII Mollusca

24 Epidermal Cells. A. BUBEL. (With 5 Figures) · 400 24.1 Introduction · 400 24.2 Epidermal Cell Types · 401 24.3 Wound Repair .420 24.4 Byssus · 421 24.5 Operculum · 431 24.6 Siphon Sheath · 432 24.7 Mucus · 433 24.8 Radula · 439 24.9 Beaks .440

25 Shell. N. WATABE. (With 9 Figures) · 448 25.1 Introduction · 448 25.2 Shell Structure .449 25.3 Chemical Constituents of Shells · 457 25.4 Cellular Aspects of Shell Formation · 464 25.5 Hinge System .472 25.6 Operculum · 475

26 Permeability and Epidermal Transport. M.G. STEWART. (With 2 Figures) · 486

26.1 Introduction · 486 26.2 Permeability in Marine Molluscs · 487 26.3 Permeability in Freshwater Molluscs · 496 26.4 Permeability in Terrestrial Molluscs · 497 26.5 Conclusion · 498

XII

VIII Arthropoda

27 Epidermal Cells. M. LOCKE. (With 7 Figures)

27.1 Introduction ........... . 27.2 The Basic Structure of an Epidermal Cell 27.3 Epidermal Differentiation . . . . . . 27.4 The Cytoskeleton, Cell Movement and

Morphogenetic Shape Change . . . . 27.5 Cuticle Secretion and the Control of Cuticular

Contents

502

503 504 509

511

Compartments ............. 514 27.6 The IntermoultfMoult Sequence of Epidermal

Activity ................ 516 27.7 General Factors Controlling Epidermal Activity 518 27.8 Local Controlling Factors and Cell Communication 518 27.9 Summary and Conclusions ........... 520

28 Chemo-, Hygro-, and Thermoreceptors. R.A. STEINBRECHT. (With 6 Figures) 523

28.1 Introduction .......... ...... 523 28.2 General Morphology of Arthropod Exteroceptors 524 28.3 Structure and Function in Insect Olfactory Receptors 526 28.4 Structure and Function in Insect Gustatory

Receptors . . . . . . . . . . . . . . . . 534 28.5 Structure and Function in Insect Hygro- and

Thermoreceptors . . . . . . . . . 537 28.6 Sensilla in Other Arthropod Classes .... 543 28.7 Conclusions . . . . . . . . . . . . . . . 547

29 Mechanoreception. F.G. BARTH and R. BUCKHAN. (With8 Figures) . 554

29.1 Introduction 554 29.2 Hair Sensilla 555 29.3 Strain Detectors 564 29.4 Conclusion . . 577

30 Cuticle: Biochemistry. R.H. HACKMAN. (With 3 Figures) . . . 583

30.1 Introduction .... 30.2 Cuticular Components 30.3 Stabilization of Cuticles

31 Cuticle: Organization. A.C. NEVILLE.

(With 10 Figures) ... .

31.1 General Structure ... . 31.2 The Size Levels of Structure 31.3 Physical Colours . . . . .

583 584 597

. 611

611 612 623

Contents XIII

32 Cuticle: Mechanical Properties. J.E. HILLERTON. (With 2 Figures) 626

32.1 Introduction 626 32.2 Types of Mechanical Properties Important for

Cuticles 628 32.3 Relationship of Cuticular Structure to Mechanical

Properties . 631 32.4 Relationship of Composition to Mechanical

Properties . 632 32.5 Relationship of Mechanical Properties to Function 633 32.6 Mechanical Properties During Development 634 32.7 Effect of Calcification on Mechanical Properties 635

33 Cuticle: Formation, Moulting and Control. W. GNATZY and F. ROMER. (With 10 Figures) 638

33.1 Introduction 638 33.2 Formation of the Cuticle During Moult-Intermoult

Cycle. 639 33.3 Sequence of Events in the Epidermal Cells 649 33.4 Organogenesis and Moulting of Organules 651 33.5 Moulting Control 664

34 Cuticle: Ecological Significance. N.F. HADLEY. (With 2 Figures) 685

34.1 General Functions-An Overview 685 34.2 The Waterproofing Barrier 686 34.3 Cuticular Lipids and Transpiration 686 34.4 The Cuticle and Water Vapour Absorption 691

35 Cuticle and Insecticides. A.R. GILBY 694

35.1 Introduction 694 35.2 Experimental Techniques 695 35.3 Cuticular Structure 696 35.4 Aspects of Penetration by Insecticides 697

IX Arthropod-Related Phyla

36 Onychophora. V. STORCH. (With 3 Figures) 703

36.1 Introduction 703 36.2 The Cuticle 703 36.3 The Epidermis . 704 36.4 The Epidermal Glands 705 36.5 The Sensilla 705

37 Pentastomida. V. STORCH. (With 2 Figures) 709

37.1 Introduction 709 37.2 The Cuticle 709

XIV

37.3 The Gland Cells and Ionocytes 37.4 The Sensilla . . . . . . . . .

38 Tardigrada. H. GREVEN. (With 6 Figures) 38.1 Introduction ...... . 38.2 Integument . . . . . . . . 38.3 Integument and Anhydrobiosis 38.4 Encystation . . . . . . . 38.5 Integument and Systematics 38.6 Conclusion . . . . . . .

X Minor Coelomate Phyla

Contents

· 711 · 712

· 714 714 715 724 725 725

· 726

39 Lophophorates. A. WILLIAMS. (With 30 Figures) 728 39.1 Introduction 728 39.2 Phoronida 728 39.3 Bryozoa 729 39.4 Brachiopoda 734 39.5 Conclusions . 744

40 Chaetognatha. P. AHNELT. (With 10 Figures) 746

40.1 Introduction ..... 746 40.2 Pluristratified Epidermis 747 40.3 Monolayered Epidermis 750 40.4 Nervous System and Receptors 752 40.5 Conclusion . . . . . . . . . 753

XI Echinodermata

41 Epidermal Cells. N.D. HOLLAND. (With 1 Figure) 756 41.1 Introduction and Definitions 756 41.2 Support Cells 758 41.3 Sensory Cells 761 41.4 Secretory Cells 762 41.5 Other Cell Types 765 41.6 Cuticle 768 41.7 Cell Proliferation and Epidermal Regeneration 769 41.8 Conclusion 770

42 Permeability and Epidermal Transport. D.R. BAMFORD · 775

42.1 Introduction · 775 42.2 The Integument and Osmotic Balance .777 42.3 Absorption of Organic Molecules · 779 42.4 Mechanisms of DOM Influx · 784 42.5 Conclusions · 786

Contents xv

xn The Protochordates

43 Hemichordata. U. WELSCH. (With 7 Figures) 790

43.1 Introduction 790 43.2 Pterobranchia . . . . . . . . . . . . . 790 43.3 Enteropneusta . . . . . . . . . . . . . 793

44 Urochordata. U. WELSCH. (With 8 Figures)

44.1 Introduction 44.2 Ascidiacea 44.3 Thaliacea . 44.4 Larvacea .

45 Cephalochordata. J. BERElTER-HAHN. (With 11 Figures) ....... .

45.1 Introduction . . . . . . . . 45.2 General Organization of the Integument 45.3 Epidermis . . . . . . . . . . 45.4 Cutis and Subcutis . . . . . . 45.5 Development and Regeneration

SUbject Index .

Index to Genera

Abbreviations

LM Light microscope/microscopy EM Electron microscope/microscopy TEM Transmission electron microscope/microscopy SEM Scanning electron microscope/microscopy RER Rough/granular endoplasmic reticulum SER Smooth endoplasmic reticulum MW Molecular weight

800 800 800 810 810

817

817 817 817 823 824

827

837

List of Contributors

You will find the addresses at the beginning of the respective contribution

Ahnelt, P. 746 Bamford, D.R. 775 Barth, F.G. 554 Befus, A.D. 192 Bereiter-Hahn, J. 817 Bird, A.F. 212 Blickhan, R. 554 Bubel, A. 400 Gibson, R. 205 Gilby, A.R. 694 Gnatzy, W. 638 Gomme, J. 323 Green, C.R. 5 Greven, H. 74 Hackman, R.H. 583 Hadley, N.F. 685 Hemandez-Nicaise, M.-L. 96 Hillerton, J.E. 626 Holland, N.D. 756 Hiindgen, M. 47 Locke, M. 502 Mackie, G.O. 43

Mariscal, R.N. 57 Neville, A.C. 611 Podesta, R.B. 192 Richards, K.S. 1, 269, 310 Rieger, R.M. 389 Romer, F. 638 Sanderson, M.J. 17 Schlichter, D. 79 Schroeder, P.C. 297 Southward, E.C. 376 Steinbrecht, R.A. 523 Stewart, M.G. 486 Storch, V. 242,269, 369,

703, 709 Threadgold, L.T. 132 Tidball, J.G. 69 Tyler, S. 112 Watabe, N. 448 Welsch, U. 269, 790, 800 Whitfield, P.J. 234 Williams, A. 728