OTHER TITLES IN THE ZOOLOGY DIVISION Vol. 1. hveN-An Outline of Developmental Physiology Vol. 2. RhwN-Morphogenesis: The Analysis of Molluscan Development Vol. 3. SAVORY-Instinctive Living Vol. 4. KEmuT-Implications of Evolution Vol. 5. TARTAR-The Biology of Stentor Vol. 6. JENKIN-Animal Hormones-A Comparative Survey Vol. 7. ComIss-The Ciliated Protozoa Vol. 8. GEORGE-The Brain as a Computer Vol. 9. ARTnuR-Ticks and Disease Vol. 10. RAVEN-Oogenesis Vol. 11. MA"-Leeches (Hirudinea) OTHER DIVISIONS IN THE SERIES ON PURE AND APPLIED BIOLOGY B I 0 CHE M I S T RY BOTANY MODERN TRENDS IN PHYSIOLOGICAL SCIENCES PLANT PHYSIOLOGY 1W^ ϋ^ Frontispiece Metachronal waves of membranelles of Stentor polymorphus THE BIOLOGY OF CILIA AND FLAGELLA BY M. A. SLEIGH Department of Zoology. The University, Exeter PERGAMON PRESS OXFORD · LONDON · NEW YORK · PARIS 1962 PERGAMON PRESS LTD. Headington Hill Hall, Oxford 4 & 5 Fitzroy Square, London, W.l PERGAMON PRESS INC. 122 East 55th Street, Nezv York 22, N.Y. GAUTHIER-VILLARS 55 Quai des Grands-Augustins, Paris 6 PERGAMON PRESS G.m.b.H. Kaiserstrasse 75, Frankfurt am Main Copyright © 1962 PERGAMON PRESS LTD. Library of Congress Card No. 62-19269 Set in Imprint 11 on 12 pt. and printed in Great Britain by BELL AND BAIN, LTD. . . . the general existence of the ciliary motion in the Animal Kingdom is already sufficiently established, . . . whoever has opportunities and inclination to cultivate this field of inquiry will find his labour rewarded by much curious and interesting discovery. DR. W. SHARPEY, 1835 PREFACE IMPORTANT advances in our knowledge of the structure and physiology of cilia have been made since Gray's classical mono graph on Ciliary Movement was published in 1928. In particular, the improvement of techniques of electron microscopy in the last decade gave rise to a renewed interest in the structure of cilia which has been rewarded with the discovery of a widespread and consistent fibril pattern in all true cilia, flagella and sperm tails. A parallel growth of interest in the physiology of the beating and co-ordination of cilia has been taking place in these years, and has been given an added stimulus by the success of morphological studies. The primary purpose of this book is to review advances in these fields since 1928, for in these 34 years no attempt has been made to summarize fundamental work on cilia and flagella in a comprehensive way. A review by J. A. Rivera entitled Cilia, Ciliated Epithelium and Ciliary Activity was published while the present book was in the press; Rivera approached the subject in an entirely different way in summarizing the effects of various agents on ciliary activity from the point of view of the human physiologist, so that the two reviews scarcely overlap at all. In the present book modern ideas on structure are linked with modern ideas on physiology in an attempt to make a single coherent story. The field of study has been divided into four parts: ciliary structure, the effects of various agents on ciliary activity, the physiology of beating of cilia and the physiology of co-ordination. The second of these is intended for reference and for the intro duction of evidence used in the third and fourth parts. Summaries of the material included will be found at the beginning of Chapter II (structure of a typical cilium) and at the ends of Chapters IV (beating activity) and V (co-ordination). The literature contains many thousands of references to ciliary structure and functioning, and, in order not to overload the book with bibliography, some selection had to be made. Only vi some 400 references are mentioned here, recent work being cited more fully (well over half the references date within the last 10 years), while key works are quoted from older studies to enable interested students to follow up other references. While the review was written to satisfy the needs of the honours student of Zoology, students in other fields should also find it valuable. Research workers studying any topic related to ciliary organelles or their activity should find it useful as a fairly concise summary of the structure and physiology of cilia, particularly since most reviews tend to concentrate on either structure or physiology with little reference to the other part of the subject. Where good evidence is available I have tried to keep closely to established facts, but where our knowledge is very scanty I have tended to stray into the realms of speculation; I hope that the reader will be able to distinguish facts from speculative suggestions. Few can fail to be convinced of the need for such a review at this time, and I hope that this attempt at a summary of the present position will satisfy the requirements of as many people as possible. If any of the ideas presented here will lead others to further research, then the author will be well satisfied that he has not laboured in vain. ACKNOWLEDGEMENTS I AM pleased to record my thanks to Professor J. E. Harris and Dr. J. A. Kitching of the University of Bristol, both for introducing me to the study of ciliary activity and for valuable comments on parts of the text of this book. I am also grateful for the advice and criticism of Professor J. O. Corliss of the University of Illinois, who, while visiting Professor of Zoology at the University of Exeter, has read the whole text and spent much time in fruitful discussions. My wife Peggy has given invaluable help in correcting manuscripts and proofs and in innumerable other ways. The help of these kind people has improved this book considerably, but the author must bear the responsibility for the shortcomings that remain. The book was written at the suggestion of Dr. G. A. Kerkut, to whom I am sincerely indebted. My thanks are also due to Dr R. Barton, Professor J. T. Randall and Dr. K. Vickerman who have passed on valuable information for this book in discussions of their unpublished work. It is a pleasure to acknowledge the assistance of Mr. N. Barratt in preparing photographs of some of the illustrations, and of Miss B. Mortimer in typing parts of the script. The generosity of the following workers who have lent or given copies of electron micrographs is acknowledged with gratitude: Dr. B. A. Afzelius, Dr. W. Bernhard, Dr. E. De Robertis, Professor D. W. Fawcett, Dr. J. G. Gall, Dr. I. R. Gibbons, Dr. E. G. Gray, Dr. A. V. Grimstone, Dr. D. R. Pitelka, Professor J. T. Randall, Dr. L. E. Roth, Dr. J. E. Shapiro, Dr. K. Vickerman and Dr. E. Yamada. Professor P. P. Grasse, Professor I. Manton and Lord Rothschild have kindly given permission for electron micrographs to be copied from published work. Permission to reproduce material from books and periodicals has been given by Publishers and Journals as follows: Academic Press for Plate Vile (from the Proceedings of the viii First IUB/IUBS Symposium) ; Cambridge Philosophical Society for Plate Vlld (from Biological Reviews) ; Cambridge University Press for Fig. 3 (from Ciliary Movement by James Gray) ; Claren don Press, Oxford, for Plate IXa, b and c (from the Journal of Experimental Botany); The Company of Biologists Ltd. for Figs. 2a and 46 (from the Quarterly Journal of Microscopical Science), Figs. 19, 25, 29, 31, 33, 38, 41a, 41b, 42, 47, 49, 50, the figures in Plate XV and Table 6 (from the Journal of Experimental Biology); The Council of the Marine Biological Association of the United Kingdom for Plates VHIb, c and IXd, e and Table 8 (from the Journal of the Marine Biological Association) ; Macmillan and Co. Ltd. for Fig. 20 (from Nature) ; Nederlandse Vereniging voor Electronenmicroscopie for Fig. 5b (from the Proceedings of the Conference on Electron Microscopy, Delft, 1960) ; The Northern Association of Obstetricians and Gynaecologists for Fig. 10 (from Ada Obstetrica et Gynecologica Scandinavica); The Rockefeller Institute Press for Plates I, II, III, IV, V, Via, b, c, X, XIa, Xllb, XIII, XIVc and Figs. 5a, 7, 8, 15 and 17 (from the Journal of Biophysical and Biochemical Cytology); The Royal Entomological Society of London for Plate Xlb (from the Trans actions of the Royal Entomological Society) ; The Royal Society for Plates VId and XlVb and Fig. 9 (from the Philosophical Transactions of the Royal Society, Series B) and Figs. 11a, 18 and 24 (from the Proceedings of the Royal Society, Series B); Scientific American Inc. for Plate Xlla; the Society of Proto- zoologists for Plate Vila and b and Fig. 14 (from the Journal of Protozoology); The University of Chicago Press for Table 10 (from Physiological Zoology); Vaillant Carmanne, Liege, for Plate Vile (from Archives de Biologie); The Wistar Institute of Anatomy and Biology for Fig. 16 (from the Journal of Mor phology) and Fig. 21 (from the Journal of Cellular and Comparative Physiology) ; Yale University Press for Plate XlVa (from Frontiers in Cytology, Ed. S. L. Palay); The Zoological Society of Japan for Fig. 23 and Table 7 (from Annotationes Zoologicae Japo- nenses); The Zoological Society of London for Figs. 34 and 35 (from the Proceedings of the Zoological Society of London). ix LIST OF PLATES Frontispiece Metachronal waves of membranelles of Stentor polymorphus PL. I Transverse sections of flagella and basal bodies of Pseudo- trichonympha (E.M.). PL. II Sections of cilia and basal bodies of Anodonta (E.M.). PL. Ill Sections of flagella of hypermastigine flagellates (E.M.). PL. IV Sections of basal parts of the membranelles of Euplotes (E.M.). PL. V Sections of compound cilia (Euplotes and Mnemiopsis) (E.M.). PL. VI Sections of sensory cilia (E.M.). PL. VII Modifications of shaft structure of flagella and cilia (E.M.). PL. Vili Flagella of some phytoflagellates (E.M.). PL. IX Flagella and haptonemata from algae (E.M.). PL. X Sections of sperm tails of invertebrates (E.M.). PL. XI Transverse sections of sperm tails (E.M.). PL. XII Sections of some centrioles and basal bodies (E.M.). PL. XIII Basal bodies and root structures of some protozoa (E.M.) PL. XIV Striated roots of metazoan cilia (E.M.). PL. XV The movement of spermatozoa of the sea urchin and bull. PL. XVI The movement of two polyflagellate protozoa. PL. XVII The movement of two types of cilia from Mytilus gill filaments. PL. XVIII Metachronal waves and ciliary beating of Opalina. Xll