Table Of ContentThaddeus 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
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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. . . . . . . . . . . . . . 16
Chapter 3. Mollusca
3.1 Gastropoda: Prosobranchia, Opisthobranchia, and
Pulmonata . . . . . . . . . . . . . . . . . . 18
3.1.1 Special Features of Reproduction in
Archaeogastropods, Mesogastropods, and
OtlJer Pro so branchs . . . . . . . . .. 18
3.1.2 Sporadic Occurrence of Spermatophores in
Cephalaspidean and Acochlidiacean
Opisthobranchs . . . . . . . . . 21
3.1.3 Love-Darts and Spermatophores in
Pulmonates. . . . . . . . . . . 22
VIII
3.2 Cephalopoda: Main Features of Male Reproductive
Function in Nautiloidea, Decapoda,
Vampyromorpha, and Octopoda. . . . . . .. 24
3.2.1 The Male Genital System of Cephalopoda 24
3.2.2 Modes of Spermatophore Transfer. . 26
3.2.3 Role of the Hectocotylus . . . . . . 27
3.3 Nautiloidea: Nautilus pompilius and Nautilus
macromphalus. . . . . . . . . . ~ . . . 29
3.4 Decapoda: Loligo pealii, Rossia macrosoma, Rossia
pacifica, Sepiola rondeletii, and Sepia officinalis 30
3.5 Small Octopoda: Octopus vulgaris, Octopus
hummelincki, Octopus bimaculatus, Other Small
Octopuses, Eledone moschata, and Eledone cirrhosa. 39
3.6 The Giant Octopus of the North Pacific, Octopus
dofleini martini . . . . . . . . . . . . 43
3.6.1 The Animal. . . . . . . . . . . . .. 43
3.6.2 Male Gonad and Accessory Organs . .. 44
3.6.3 Formation and Maturation of the Spermato-
phore in the Male Reproductive Tract . . . 46
3.6.4 The Mature Spermatophore. . . . . . . . 49
3.6.5 Osmoregulation as the Driving Force for the
Spermatophoric Reaction in Vitro . . 50
3.6.6 Copulation and the Mechanism of the
Spermatophoric Reaction in Vivo . . 56
3.7 Biochemistry of the Giant Octopus Spermatophore. 57
3.7.1 Outer Tunic and Its Permeability to Chemicals 57
3.7.2 The Gel Rod of the Ejaculatory Apparatus. 58
3.7.3 Cement Liquid and the Role of Glycosidases. 59
3.7.4 Main Physicochemical Properties of
Spermatophoric Semen. . . . . . . .. 59
3.7.5 Proteins, Peptides, Galactophosphopeptide,
and Certain Other Major Constituents of
Spermatophoric Plasma . . . . . . . . . 61
3.7.6 Distribution of Glycerylphosphorylcholine
and Carnitine Between Spermatophoric
Plasma and Spermatozoa. . . . 63
3.7.7 Glycogen and Glycogenolysis in
Spermatozoa . . . . . . . . . 64
3.7.8 D( - )Lactic Acid and D( - ) Lactate
Dehydrogenase . . . . . . . . . 65
3.7.9 Relation of Glycogen, Arginine Phosphate,
and Adenosine Polyphosphates to Sperm
Motility . . . . . . . . . . . . 66
3.7.10 The High Zinc Content of Octopus
Spermatozoa . . . . . . . . . . 68
3.7.11 Biochemical Changes Associated with the
Spermatophoric Reaction. . . . . . .. 68
IX
Description: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 probl
