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Spermatophores Development, Structure, Biochemical Attributes and Role in the Transfer of Spermatozoa

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Spermatophores Development, Structure, Biochemical Attributes and Role in the Transfer of Spermatozoa Thaddeus Mann Spermatophores Development, Structure, Biochemical Attributes and Role in the Transfer of Spermatozoa With 50 Figures Springer-Verlag Berlin Heidelberg New York Tokyo 1984 Zoophysiology Volume 15 Coordinating Editor: D. S. Farner Editors: B. Heinrich K. Johansen H. Langer G. Neuweiler D.J. Randall The l-m-Iong spennatophore of the Giant Octopus of North Pacific, Octopus dofleini martini, being pulled out manually from animals copulating in a sea­ water-filled observation tank. The upper, white portion of the spennatophore contains the spenn rppe with spennatozoa, and the lower, thin portion contains the ejaculatory apparatus; the junction between the two portions is located in the region pressed against the forefinger. Top right the head of the male, in profile; bottom right ventral aspect of the female's head. (Mann et al. 1969) Thaddeus Mann Spermatophores Development, Structure, Biochemical Attributes and Role in the Transfer of Spermatozoa With 50 Figures Springer-Verlag Berlin Heidelberg New York Tokyo 1984 Professor Dr. THADDEUS MANN 1, Courtney Way Cambridge CB42EE England The front cover illustrates the spermatophore of cuttlefish, as first seen by Swammerdam and described by him in Biblia Naturae ISBN -13: 978-3-642-82310-7 e-ISBN -13: 978-3-642-82308-4 DOl: 10.1007/978-3-642-82308-4 Library of Congress Cataloging in Publication Data. Mann, Thaddeus, 1908 - Spermato­ phores: development, structure, biochemical attributes, and role in the transfer of spermatozoa. (Zoophysiology; v. 15) Bibliography: p. Includes indexes. 1. Spermato­ phores. 2. Spermatozoa. I. Title. II. Series. QP255.M25 1984 592:01662 84-14181 This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically those of translation, reprinting, re-use of illustrations, broadcasting, reproduction by photocopying machine or similar means, and storage in data banks. Under § 54 of the German Copyright Law where copies are made for other than private use, a fee is payable to "Verwertungsgesellschaft Wort", Munich. © by Springer-Ver1a,g Berlin Heidelberg 1984 Softcover reprint of the hardcover I st edition 1984 The use of registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. 2131/3130-543210 Preface Physiology and biochemistry of male reproductive function and semen became the main area of my research in 1944, after my attention was finally diverted frorp. animal cells in general, to mammalian spermatozoa specifically~ Ever since, the interest has remained largely focussed on reproductive probletns in mammals, the work continuing mostly at the University of Cambridge, where I was privileged to hold also the Marshall­ Walton Professorship in Physiology of Reproduction. This work led to the publication of three books, The Biochemistry of Semen (Methuen 1954), The Biochemistry of Semen and of the Male Reproductive Tract (Methuen 1964) and lately, in co­ authorship with my wife, Dr. Cecilia Lutwak-Mann, Male Re­ productive Function and Semen - Themes and Trends in Phys­ iology, Biochemistry and Investigative Andrology (Springer­ Verlag 1981). In 1960, thanks to the Lalor Foundation, I was able to avail myself for the first time of a chance to visit the Marine Biological Laboratory at Woods Hole and there to take part in a study of reproduction in marine animals. Ever since, first as Visiting Professor of Biology at the State University of Florida, and later as the Walker Ames Professor and frequent visitor to the Department of Zoology at the University of Washington in Seattle, it has been my good fortune to sustain this pew interest and to pursue it further. The spermatophores of cephalopod molluscs aroused my special curiosity, not least because it puzzled me greatly why in contrast to all mammals, a male squid or octopus does not ejaculate semen in a liquid state, but chooses instead to pack the spermatozoa into the tube­ shaped capsule of a spermatophore, before transferring them to the female. Apart from the common American squid, Loligo pealii, and the common octopus, Octopus vulgaris, extensive use was made of the giant octopus of the North Pacific, Octopus dojleini martini. This creature's giant spermatosphores, each 1 m long, became the main object of a collaborative study with Dr. Arthur Martin, Dr. John Thiersch and several other colleagues. The study continued for many happy years and led to a number of new findings. We were able to demonstrate that the spermatophoric plasma, that is, the fluid which surrounds the spermatozoa inside the spermatophore, bears close chem- V ical similarity to mammalian epididymal plasma. We found that, unlike the spermatozoa of mammals, those of the octopus are unable to metabolize fructose to L( + )lactic acid, but instead survive at the expense of their glycogen, which they break down to D( - )lactic acid. We have shown that the so-called spermato­ phoric or ejaculatory reaction which makes possible the release of spermatozoa from the spermatophore depends on influx of seawater and osmoregulation as the main driving force, but in the course of that reaction, not merely salt and water, hut also foreign chemicals can enter the interior of the spermatophore. Three centuries have passed since Swammerdam made the discovery of the first spermatophore in Sepia, 'and over the years that followed similar sperm-encompassing devices were shown to occur in phyla other than Mollusca, including Platyhelminthes, Aschelminthes, Phoronida, Annelida and many Arthropoda, such as Onychophora, Myriapoda, Insecta, Crustacea and Arachnida. They were also shown to be present in Chaetogmitha, Pogonophora and occasionally, in Verte­ brata, such as certain fishes and salamanders. Yet, as I became painfully aware during the pursuit of my own inquiries, no one seems to have made an attempt to collect and update informa­ tion about the various phyla so as to present it in the form of a single treatise. Hopefully, the present monograph, which in­ cludes references to about 770 publications, will meet that need even though it deals predominantly with problems of function and adaptation to environment. I have tried deliberately to shy away from phylogenetic speculations and have, left aside the various, sometimes rather wild, evolutional theories (which I distrust). I have made no attempt to tinker with problems of taxonomy (about which I know little), and as regards termin­ ology, I admit that apart from Lord Rothschild's (1965) Classification QfLiving Animals, I relied principally, partly for historical reasons, on the terms used by authors of the original publications. Those readers who might feel that I have accorded pre­ ferential treatment to cephalopod spermatophores, I would like to re"rnnd of a comment made by William Hoyle (1907) during his presidential address to the Zoological Section of the British Association for the Advancement of Science, on the subject of reproduction in Cephalopoda: "The impression left upon my mind by a score of Pre­ sidential Addresses to this Section, which it has been my privilege to hear, is that the speaker who treats of the subject matter of his own researches has the best prospect of making his remarks interesting and profitable to his audience." VI "What I have ventured to lay before you are a few fruits of the little garden plot in whose culture I have been privileged to take a humble share." "The plot I have tried to cultivate has been a very small one, and I have had but little leisure to peep over the fence and see what my neighbours were doing." The task of writing the monograph, which occupied a great deal of my time for about 2 years, could not have been accomplished without the support of the Royal Society, the help of Prof. A. Labhart and Mrs. A. Pfau during the search for early literature at the University of Zurich, and the gen­ erous assistance of those colleagues who either read parts of the text or gave permission to reproduce various figures: Drs. R. A. Brandon, J. Martan, L. D. Russell and E. J. Zalisko (Car­ bondale, Illinois), H. Breucker (Hamburg), R. Dallai (Siena), K. G. Davey (York University, Ontario), H. G. Drecktrah (University of Wisconsin Oshkosh), C. Erseus (Stockholm), W. H. Fahrenbach (Oregon Primate Research Center), D. S. Farner (Seattle), B. Feldman-Muhsam (Jerusalem), G. E. Gre­ gory (Rothamsted Experimental Station), W. Grewe (Anstalt Helgoland), R. Hartmann (Cologne), A. W. Martin (Seattle), W. G. Robison (National Institutes of Health, Bethesda), V. Storch (Heidelberg), P. Talbot and M. J. Kooda-Cisco (Riverside, California), H. E. Vistorin (Waiblingen, FRG), W. Westheide (Osnabrock), P. Weygoldt (Freiburg) and R. L. Zimmer (Harvard University). I take also great pleasure in expressing my thanks to Mrs. Carmen Frankl for drawing the figures, Mrs. Jennifer Constable for typing the manuscript, and Mr. Michael Jackson for patient guidance during the prepara­ tion· of the monograph for the Springer-Verlag. Indeed, the publishers and editors alike have gone far beyond normal obligations, and their assistance is gratefully acknowledged. Cambridge, August 1984 THADDEUS MANN VII Contents Chapter 1. General Considerations 1.1 Beginnings . .. 1 1.2 Definitions . .. 5 1.3 Spermatophore as Repository and Transport Vehicle for Spermatozoa. Certain Similarity to Epididymis. 6 1.4 Direct and Indirect Insemination Routes . .. 7 1.5 Role of Spermatophore in Fertilization and Nutrition 8 1.6 Common Features of Spermatophore, Copulatory Plug; and Sphragis. 10 1.7 Conflicting Views on the Origin and Purpose of Spermatophores. 11 Chapter 2. Platyhelminthes, Aschelminthes, and Phoronida 2.1 Early Observations on the Attachment of Spermatophores to the Skin of Turbellaria 14 2.2 Mechanisms of Sperm Transfer in Turbellaria and Monogenea. .. 14 2.3 Hypodermic Impregnation in Rotifera and Other Asche1minthes. .. 15 2.4 Spermatophores of Phoronis vancouverensis and Phoronopsis harmeri, and the Role of Lophophoral Organs in 'Phoronida.
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