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VetBooks.ir
Manabu Yoshida
Juan F. Asturiano Editors
Reproduction
in Aquatic
Animals
From Basic Biology to Aquaculture
Technology
Reproduction in Aquatic Animals
VetBooks.ir
Manabu Yoshida • Juan F. Asturiano
VetBooks.ir
Editors
Reproduction in Aquatic
Animals
From Basic Biology to Aquaculture
Technology
Editors
VetBooks.ir
This Springer imprint is published by the registered company Springer Nature Singapore Pte Ltd.
The registered company address is: 152 Beach Road, #21-01/04 Gateway East, Singapore 189721,
Singapore
Preface
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Even though there are many animals in terrestrial habitats, there is great biodiversity
to be found in aquatic ecosystems. Furthermore, aquatic animals show various
reproductive systems: many animals perform external fertilization, others show
internal fertilization without mating, some are viviparous, etc. This means that the
reproduction systems of aquatic animals are highly diverse, and they are excellent
models for studying adaptive evolution and species-specificity of fertilization. In
addition, many aquatic animals such as fish, crustaceans, and mollusks are impor-
tant as fishery and aquaculture resources. Nevertheless, their reproductive systems
are also diverse, resulting in difficulties in cultivation, especially in the production
of juveniles. Thus, comprehensive knowledge of the reproductive systems of vari-
ous aquatic animals will help us understand the systems of each animal, resulting in
breakthroughs in the research areas and aquaculture technologies. However, only a
few books overviewed the reproductive systems of aquatic animals from inverte-
brates to fishes since many researchers focused their animals of interest. Therefore,
our aim with this book was to overview the various reproductive systems of aquatic
animals.
The idea for this book was initially conceived in the International Symposium on
“AQUAGAMETE: Reproduction of Aquatic Animals” held in the Joint Meeting of
the 22nd International Congress of Zoology and the 87th meeting of the Zoological
Society of Japan, which was held from 14th to 19th November 2016 in Okinawa,
Japan. Three years have passed since the initial planning, and we have developed
the book ideation. In order to introduce up-to-date knowledge on the reproduction
systems of various aquatic animals from basic biology to aquaculture technology,
we invited up-and-coming researchers to contribute. This book consists of 17 chap-
ters and a foreword that details the history of spermatology to be read before the
main chapters. Finally, the book covers the reproductive systems of both sperm and
egg in cnidarians, annelids, arthropods, mollusks, echinoderms, ascidians, elasmo-
branchs, teleosts, and amphibians. Four chapters focus on the technological and
aquaculture aspects, in particular relating to fishes.
This book is designed for people who are neither experts/well-read/knowledge-
able in the field of reproductive biology nor aquaculture. The assumed readers are
v
vi Preface
graduate students and postgraduates in biology and agricultural sciences and also
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Part I Overview
1 Overview: Reproductive Systems in Aquatic Animals ������������������������ 13
Manabu Yoshida
vii
viii Contents
of Spermatology
Jacky Cosson
This foreword mostly aims to introduce, from a historical stand point, how the
notions of gametes emerged, and to describe the tortuous approach by the pioneer
scientists who first discovered and explored the functions and structure of aquatic
animal gametes and their interactions. Sperm cells most likely became of interest to
scientists due to the fact that they hold the key to life and have an incredible ability
to move, in spite of their small dimensions.
It is commonly acknowledged that spermatology is a scientific domain dealing
with the structure and function of spermatozoa. For this reason, it can be supposed
that the history of spermatology began in 1677 with Leeuwenhoek’s description of
the spermatozoon, the male entity, responsible for animal procreation and rendered
visible for the first time through his microscope. Therefore, it is considered that
spermatology starts at this date as biologists enjoy to attribute a structure to a func-
tion. For obvious reasons, this foreword mostly covers the last three-and-a-half cen-
turies, if we accept Leeuwenhoek to be the “inventor” of spermatozoa.
It is out of the present topic to discuss the history of human reproduction, in its
medical aspects. Instead, in this book, we will concentrate more specifically on the
gametes of aquatic animals with our main aim being to trace how the study of aquatic
animals can be so important in the understanding of the mechanisms of gamete
interaction.
J. Cosson (*)
Faculty of Fisheries and Protection of Waters, Research Institute of Fish Culture and
Hydrobiology, University of South Bohemia in České Budějovice, Vodnany, Czech Republic
Long before the identification of the individual elements later called “spermatozoa,”
Leonardo da Vinci, by reference to Hippocrates, wrote: “The origin of our semen is
located in the brain and in the lungs and it is in the testis of ancestors that the final
mixing occurred.” This premonitory statement contains quite a lot of veracity that
modern science would finally establish as true: the brain definitely contributes
“psychologically” to the delivery of sperm to the female for reproduction; the lungs
constitute an organ making a large use of cilia which are homologue to flagella in
their constitution and the testis contributes to the efficient mixing of the ancestor’s
genomes during the meiotic process of spermatogenesis.
Already in 1623, L. Gardinius (L. du Gardin) assumed that there were fertilizing
particles in male semen, but it wasn’t until 1677 that they were in fact observed by
the human eye and described. However, the priority comes to Antonie van
Leeuwenhoek, who in that year found spermatozoa in the semen of fish, frogs, and
mammals, thanks to one of his rudimentary microscopes made of a single spheroi-
dal lens. His publication to the Royal Society De Natis E Semine Genitali Animalculis
(1678) remains famous and frequently cited.
In his letter (1677), he described that there are “living animalcules” in human
semen: “The size of animalcules is ten thousand times less than a water louse. They
move like a snake or like an eel swimming in water, have globule at the end, and are
very flexible.” He supported his letter with a drawn picture of what had been seen
under the microscope (see Fig. 1). He continued to observe many other animals in
his later works and showed that the animalcules were produced by the testes.
Leeuwenhoek knew his discovery was important to the understanding of reproduc-
tion and insisted that “a sperm cell was the only thing that made an embryo, and that
the egg and uterus merely nourished it as it grew.” At that time, the prevailing view
on reproduction was that the embryo grew from the egg alone, after the semen
added a “volatile spirit” to spark its development.
In the context of his epoch, he called them animalcula and interpreted them in
Aristotelean terms that could be considered nowadays as quite male chauvinist.
“Life comes from the male whereas the female produces nutrition for it in the egg.”
Two sentences from Leeuwenhoek’s letter read as follows: “What I investigate is
only what, without sinfully defiling myself, remains as a residue after conjugal
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coitus. And, if your Lordship should consider that these observations may disgust or
scandalize the learned, I earnestly beg your Lordship to regard them as private and
to publish or destroy them, as your Lordship thinks best.” Evidently, the Royal
Society did not regard the topic to be indecent as they published the letter. One
hundred years later, scientists were perhaps more prudish, as exemplified by this
statement by Herman Schützercranz, physician of the Swedish king: “You cannot
and ought not know whatever happens at fertilization,” which denotes a lack of
openness for a medical doctor. Whereas Leeuwenhoek’s famous letter undoubtedly
is the first description of spermatozoa, the events around his discovery are more
complex.
According to Cole (1930), Leeuwenhoek’s letter to the Royal Society in
November 1677 wasn’t published until 1679 and was preceded by a communication
to the Académie Française (French Academy) by Christiaan Huygens, dated July
30th 1678. Huygens describes in this communication small animals similar to tad-
poles in the semen of a dog. His comments, after translation into English read as this
premonitory sentence: “This discovery seems very important and should give
employment to those interested in the generation of animals,” predicting the advent
of artificial propagation of animals. Nevertheless, in a letter dated March 26th
1678, Huygens admits to having seen and read Leeuwenhoek’s letter of 1677. In
August 1678, Nicolas Hartsoeker published a letter in the Journal des Savants
(drafted by Huygens because of Hartsoeker’s inability to write in French), in which
he describes animals similar to little eels in the semen of the cock; the latter differed
thus in shape from the tadpole-like animalcula of the dog. It is amazing to note that
this is the first example of comparative spermatology! In conclusion, two investiga-
tors published data on spermatozoa in the year 1678; both did so during the time
span needed for Leeuwenhoek’s letter to be translated from Dutch to Latin (in three
different versions) and printed by the Royal Society. Such huge delay in the trans-
mission of information seems incredible in today’s internet era!
Furthermore, Leeuwenhoek himself attributed the discovery of the animalcula to
a certain “Dominus Ham,” that is Mr. Ham, a person who never published anything
on semen nor its content. This man is commonly believed to be Ludwig van Hammen
of Danzig, but according to Cole (1930) it is more likely to be Johan Ham, a
Dutchman from Arnhem, born in 1650 or 1651, a student at the time of his discov-
ery, and who later became a Doctor in Arnhem. Apparently, Johan Ham was the first
person to see mammalian spermatozoa and Leeuwenhoek was informed by him;
thus, Huygens became the first to publish data on mammalian spermatozoa and
Hartsoeker the first to publish data on avian spermatozoa.
Leeuwenhoek later studied and described spermatozoa from other classes of
animals.
All observations on animalcula were met with great interest. Robert Hooke (the
first man to use the word “cell”) thus had to demonstrate the existence of spermato-
zoa to King Charles II, who expressed his delight to see the animalcula. Yet, the sig-
nificance of the animalcula remained obscure. To some philosophers, the huge
number of animalcula made no sense for any idea of conception. According to
4 J. Cosson
space of a sand grain size.” And after all, Leeuwenhoek had found a multitude of
small creatures when he examined scrapings from the teeth (probably bacteria). To
others, the existence of small swarming creatures validated the idea that offspring
comes from the male. The man-like homunculi depicted by Hartsoeker and
Dalenpatius are famous and classically used as illustrations in Fig. 2.
Some investigators went so far as to claim that they could see horse animalcula
in horse semen and donkey animalcula in donkey semen and that the donkey ani-
malcula had longer ears. Still others claimed that they could see male and female
animalcula and even mating and childbirth among these!
The humunculus also seemed to confirm the preformation concept, that is, the
belief that everything is present in the seed although in a miniaturized form and that
development merely consists of an increase in size. The preformationists could
either be animalculist or ovist; the latter believed that the animal is already formed
in the egg. An ovist would thus claim that he could see the chick in the unfertilized
egg. The preformationist theory has the merit that it explains original small men
were contained already in the organs of Adam and Eve. It also has the consequence
that the human race will become extinct when the stock of seed is exhausted.
The ovist school can be said to have begun with the publication by Harvey in
1651 of his influential book De Generatione with its prophetic quote on the frontis-
piece “Ex ovo omnia,” “all (animals) from eggs.” Harvey thus believed that the male
(semen) played no part in the formation of the fetus.
During an experimental dissection of a mated roe deer, he could find no sperma-
tozoa in the uterus. The debate between believers in epigenesis (i.e., the embryo and
its parts undergo differentiation of initially undifferentiated entities) and believers in
preformation went on for several centuries. If a vote had been taken in the seven-
teenth century, the preformationists would have won by a wide margin although
some thinkers, such as Descartes, were supporters of epigenesis.
Fig. 2 Drawing of
homunculi in sperm by
Hartsoeker. (Left: from
Essai de dioptrique 1694)
and by Dalenpatius (right:
from Nouvelles de la
République des Lettres,
1699). This figure is Public
Domain
Foreword: A Brief History of Spermatology 5
The structure and meaning of the animalcula was also debated at the end of that
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century. P. Dionis (1698) asked for further inquiries as he believed that they are
formed by minute fibers in semen exposed to air. M. Lister (1698) also inquiring
about the origin of the seminal animalcula concluded (free translation from Latin):
“Homunculi in great numbers: when I reflect upon it, I leave it to be cared for by
others, to me it is a fairy tale.”
Leeuwenhoek’s importance as a microscopist is widely recognized. Less known
is the fact that he also tried to investigate inheritance by an experiment. He mated a
gray rabbit buck with a white rabbit doe and noted that all the young were gray—
another “proof” of the validity of the “seed-dominant” concept. Evidently, he did
not perform—or at least did not report—a control, that is a cross between a white
male and a gray female.
The uncertainty continued into the eighteenth century. E. F. Geoffroy and C. du Cerf
(1704) observed numerous, but non “fully mature” animalcula in boys, well devel-
oped and active ones in adults, few and feeble ones in old men, and no animalcula
in sterile individuals. They would conclude that animalcula are needed for repro-
duction and can hence be considered the founders of andrological spermatology.
Other opinions also prevailed; M. Schurig (1720) in his Spermatologia Historico
Medica considered the animalcula to be only an “active portion of the semen agi-
tated in a viscid mass.” A. Vallisnieri (1721) and P. L. M. de Maupertuis (1744)
admit that animalcula exist but claim that they have no direct relation to reproduc-
tion: they are entozoa (tapeworms) and keep the semen fluid. The philosopher
J. M. Gestner (1737) accepts seminal animalcula as a fact but claims that their dis-
covery is to be credited to Hippocrates who, according to Gesner, was able to see
them by his “enormous force of reason” rather than by using a microscope!
During this eighteenth century, the great naturalists were against the idea of ani-
malcula playing a role in reproduction. Carl Linnaeus (1746) believed them to be
inert “corpuscules,” P. Lyonet (1751) to be “entozoic” parasites, G. L. L. Buffon
(1752) and J. T. Needham (1749) to be aggregates of living organic molecules
derived from the mucilaginous part of the semen. The entozoa hypothesis seems to
have been very popular, and several attempts were made to include them in the clas-
sification of animals: according to Hill (1752), the animalcula are infusoria (pro-
tists) and deserve a genus name, Macrocercus, related to Vorticella and Euglena.
Spallanzani (1776) ranks them among the animals and Blumenbach (1779) again
among the “infusorial” animals, with the genus and species name Chaos spermati-
cum. Cuvier (1817) classifies them in the genus Cercaria. Bory de Saint-Vincent
(1827) similarly regards them as belonging to the family Cercariae and invents a
new genus name, Zoospermos. Carl Ernst von Baer (1827) modified that name to
Spermatozoon, a word that caught on and is still in use today.
6 J. Cosson
and that the outcome of such studies would influence the thinking on the role of
spermatozoa. The first such experiment in Europe was performed by M. Jacobi in
1763, when he discovered how to fertilize fish eggs with milt. It must be noted that
the artificial propagation of fish had been developed in China many years before by
Fan Li (born in 517 B.C.), with no understanding of the fact that sperm cells were
the fertilizing elements present in milt. Not long after Jacobi, Lazzaro Spallanzani
succeeded in performing artificial fertilization not only in fish and frogs but also in
a bitch (Gabriel and Vogel 1955; Castellani 1973; Sandler 1973). He also filtered the
semen in 1784 or 1785 and noted that frog eggs were fertilized by the seminal frac-
tion that could be squeezed out of the filter paper, but that no fertilization occurred
when the filtrate was added to the eggs.
Experiments of this kind would eventually become decisive to our understanding
of the role of spermatozoa. Yet, Spallanzani himself did not draw the correct conclu-
sion. He had previously performed some experiments where he had added frog
semen, which he supposed was devoid of spermatozoa, to eggs and these had then
developed. He concluded from his various experiments that it is the “seminal aura”
outside the animalcula that is capable of fertilization. It was only much later that this
type of experiment was repeated and that the correct conclusion was drawn. The
priority thus goes to Povost and Dumas, who in 1824 published their data and inter-
pretations. The technique of artificial insemination may have a much older history
however. There is a rumor that an Arabic person, named Hegira, in 1332 had a stal-
lion ejaculate on a cloth that he then inseminated in his mare’s vagina and that a foal
was born after the expected period (Adlam 1980). The funny part of the story is that
the stallion was not his own and the semen was a theft from a competitor and was
performed in the darkness of the night by exposing the stallion to the smell of a
mare’s vaginal secretion. There may even be records of artificial insemination in the
Talmudic books. These records may, however, refer to legends rather than to actual
experiments.
Not long after Spallanzani’s experiments, artificial insemination had even been
practiced in humans (reviewed in Adlam 1980). The first records are from the end
of the eighteenth century. More important from a scientific point of view were the
observations performed by Koelliker in 1844. He examined semen from many spe-
cies of marine animals and also performed some insemination experiments. He
could, among others, draw three fundamental conclusions: (1) semen of all animals
contain spermatozoa, (2) these are formed from cells in the testes, and (3) sperma-
tozoa have to come into contact with eggs for a fertile union to occur.
Fifteen years later, Koelliker could also conclude from more insemination exper-
iments that it is the sperm head that is essential for fertilization to occur and after yet
another 20 years, Hertwig (1892) made a statement in his doctoral thesis that made
Foreword: A Brief History of Spermatology 7
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Annesley Grayle meets the man who calls himself Nelson Smith
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[2]
WILSON, CAROLYN CROSBY. Fir trees and
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Poems on varied themes. Among the titles are: Mid winter; The
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