Table Of ContentADVISORY BOARD
DONALD P. ABBOTT
Stanford University
Hopkins Marine Station
Pacific Grove, California
DONALD P. COSTELLO
Department of Zoology
University of North Carolina
Chapel Hill, North Carolina
JOHN D. COSTLOW, JR.
Duke University Marine Laboratory
Beaufort, North Carolina
ROBERT L. FERNALD
University of Washington
Friday Harbor Laboratories
Friday Harbor, Washington
JEFFERSON J. GONOR
Oregon State University
Marine Science Center
Newport, Oregon
CADET HAND
University of California
Bodega Marine Laboratory
Bodega Bay, California
REPRODUCTION OF
MARINE INVERTEBRATES
Volume I
Acoelomate and Pseudocoelomate Metazoans
Edited by
Arthur C. Giese
Department of Biological Sciences and
Hopkins Marine Station
Stanford University
Stanford, California
John S. Pearse
Division of Natural Sciences
University of California
Santa Cruz, California
ACADEMIC PRESS New York and London 1974
A Subsidiary of Harcourt Brace Jovanovich, Publishers
COPYRIGHT © 1974, BY ACADEMIC PRESS, INC.
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LIBRARY OF CONGRESS CATALOG CARD NUMBER: 72-84365
PRINTED IN THE UNITED STATES OF AMERICA
LIST OF CONTRIBUTORS
Numbers in parentheses indicate the pages on which the authors' contributions begin.
Richard D. Campbell (133), Department of Developmental and Cell
Biology, University of California, Irvine, California
Paul E. Fell (51), Department of Zoology, Connecticut College, New
London, Connecticut
Arthur C. Giese (1), Department of Biological Sciences and Hopkins
Marine Station, Stanford University, Stanford, California
Catherine Henley (267), Department of Zoology and Laboratories
for Reproductive Biology, University of North Carolina, Chapel
Hill, North Carolina
Robert P. Higgins (507), Office of Environmental Sciences,
Smithsonian Institution, Washington, D. C.
W. D. Hope (391), Department of Invertebrate Zoology, Smithsonian
Institution, Washington, D. C.
William D. Hummon (485), Department of Zoology, Ohio University,
Athens, Ohio
John S. Pearse (1), Division of Natural Sciences, University of
California, Santa Cruz, California
Helen Dunlap Pianka (201),* Friday Harbor Laboratories and the
Department of Zoology, University of Washington, Seattle,
Washington
Nathan W. Riser (359), Marine Science Institute, Northeastern
University, East Point, Nahant, Massachusetts
Wolfgang Sterrer (345), Bermuda Biological Station, St. George's
West, Bermuda
Anne Thane (471), Zoological Institute, University of Aarhus, Aarhus
C, Denmark
♦Present address: 3221 Clearview Drive, Austin, Texas.
IX
PREFACE
The extensive and widely scattered information on reproduction in
marine invertebrates has never been summarized, and most books
covering comparative physiology and ecology of marine inverte-
brates omit consideration of reproduction for lack of such a summary.
Yet reproduction is one of the fundamental activities of organisms.
This was even pointed out by Aristotle in ancient times. This treatise
should be of particular interest because some of the marine inverte-
brates have remained relatively undifferentiated and even archaic in
their reproductive processes, while others have become specialized
and have changed considerably from their prototypes in this respect.
Thus they provide a unique perspective on the evolution of repro-
ductive mechanisms and behavior in the animal kingdom. During
the course of reproduction many invertebrates undergo profound
changes in anatomy, physiology, and behavior. Moreover, reproduc-
tive success is closely linked to environment so that reproductive
activities are often sensitive to, and synchronized by, environmental
changes. This treatise should therefore fill a need and be of use to
students of marine biology, ecology, and reproduction in general.
The work will consist of seven volumes. In the first six volumes,
specialists deal with particular marine invertebrate groups from a
similar vantage point to provide up-to-date coverage. All groups of
free-living marine invertebrates are considered rather than only
groups which have already received considerable attention. In
Volume VII the authors will deal with general aspects of reproductive
physiology and ecology.
We are indebted to our Advisory Board for suggestions on the
scope and organization of the treatise, to the Board and a larger
community of biologists for encouragement and suggestion of pro-
spective authors, and to all the authors who enthusiastically assumed
responsibility for chapters which required of them much effort and
time. Finally, we are indebted to Dr. Vicki Buchsbaum Pearse for
her painstaking editorial assistance and to the staff of Academic Press
for their advice and help with the development of the manuscript.
ARTHUR C. GIESE
JOHN S. PEARSE
xi
Chapter 1
INTRODUCTION: GENERAL PRINCIPLES
Arthur C. Giese
and
John S. Pearse
1.1 Basic Events and Terminology of Reproduction 2
1.2 Methods of Estimating Sexual Reproductive Activity 9
1.2.1 The Gonad Index 9
1.2.2 Observations of Spawning Animals 10
1.2.3 Gonadal Smears and Sections 11
1.2.4 Following Changes in Individual Animals 11
1.2.5 Sampling Eggs, Embryos, Larvae, and Juveniles 13
1.3 The Timing and Patterns of Reproduction 14
1.4 Endogenous Regulation of Gametogenesis 18
1.5 Exogenous Regulation of Gametogenesis 20
1.5.1 Temperature 21
1.5.2 Photoperiod 24
1.5.3 Salinity 26
1.5.4 Abundance of Food 28
1.5.5 Chemical Factors 30
1.6 Spawning 31
1.7 Ecological Considerations of Reproductive Cycles 34
1.8 Conclusion 36
Acknowledgments 38
1.9 References 38
On the basis of the number of phyla and classes, the most nu-
merous kinds of animals are invertebrate and marine. Marine inver-
tebrates thus provide the widest scope of diversity in animal life,
some relatively simple in organization (e.g., sponges, cnidarians, and
flatworms), and others much more complex (e.g., echinoderms, mol-
luscs, and arthropods). Most invertebrates probably originated and
became diversified in the sea; the sea is considered to have changed
little in physical and chemical properties since life began (Rubey,
1951; Robertson, 1953; Pearse and Gunter, 1957). In general, how-
1
2 GIESEANDPEARSE
ever, studies of reproduction in animals have been concerned mainly
with vertebrates, especially with particular classes of vertebrates.*
Reviews on invertebrates deal only with specialized aspects of repro-
duction.!
Coverage in this treatise of all groups of free-living marine
metazoans will focus attention on those groups of invertebrates for
which there is presently little or no information as well as on those
possessing unique features which might point to fundamental prob-
lems in reproductive biology and might be especially revealing for
an understanding of the regulation of reproduction. It is the intention
of the editors that this treatise may serve as a framework from which
further, more coordinated studies on reproductive biology will pro-
ceed.
Protozoans have been excluded because there has been little work
on reproduction of marine forms, and because many aspects of their
reproduction seem very different from those in metazoans (see
Fenchel, 1969). Work on parasites and nonmarine invertebrates**
is also excluded since these groups seem to mainly illustrate modi-
fications and specializations of general patterns seen in related free-
living marine forms.
Because reproduction is of such universal biological importance, it
is probably governed by general principles. Recognition, elucida-
tion, and formulation of such principles is therefore a central objec-
tive of this treatise.
1.1 Basic Events and Terminology of Reproduction
Reproduction occurs by sexual or asexual means (Fig. 1). In
asexual reproduction, which occurs by budding, fission, fragmenta-
*See, for example, general: Frazer, 1959; Bullough, 1961; Van Tienhoven, 1968; the
journal Biology of Reproduction; the series Advances in Reproductive Physiology; the
yearly chapter in the Annual Review of Physiology; fish: Götting, 1961; Breder and
Rosen, 1966; Nakano, 1968; Hoar, 1969; reptiles: Tinkle, 1969; Licht et al, 1969;
birds: Farner and Follett, 1966; Lack, 1967; Lofts and Murton, 1968; mammals: Mar-
shall and Parkes, 1950-1956; Asdel, 1964; Harrison, 1969; Sadlier, 1969.
fFor example, breeding cycles: Giese, 1959; sex determination: Bacci, 1965; Crew,
1965; genital morphology: Beklemishev, 1969;i hermaphroditism: Ghiselin, 1969; oo-
genesis: Raven, 1961; Schuetz, 1969a; Davidson, 1968; Busson-Mabillot, 1969; sper-
matogenesis: Roosen-Runge, 1969; fertilization: Austin, 1968; Franklin, 1970; devel-
opment: Kumé and Dan, 1968.
**See, for example, the recent reviews on insects: de Wilde, 1964; Davey, 1965;
Engelmann, 1970.
1. INTRODUCTION 3
FIG. 1. Diagram of the types of reproduction that can occur during the life cycle of
an animal.
tion, formation of reproductive bodies (e.g., gemmules, frustules,
statoblasts), polyembryony, or ameiotic (apomictic) parthenogenesis,
no recombination of genetic materials takes place (Vorontosova and
Liosner, 1960; Herlant-Meewis, 1965). Asexual reproduction may be
cyclic and may occur only at certain times of the year or during cer-
tain stages of the life cycle. Asexual reproduction enables organisms
to reproduce rapidly during favorable conditions, especially in un-
stable environments, or, as in some freshwater forms, it provides a
means of surviving adverse conditions. These topics will be dis-
cussed in the chapter on asexual reproduction in a future volume.
Genetic recombination occurs in sexual reproduction, almost al-
ways as a result of meiosis and the subsequent fusion (amphimixis)
of genetically different gametes. Genetic recombination also occurs
in meiotic or automictic parthenogenesis, in which meiosis takes
place and the haploid products recombine to form new diploid cells
(parthenogamy); in a strict sense, this should be considered a form of
sexual reproduction. Moreover, ameiotic diploid and meiotic haploid
forms of parthenogenesis are sometimes considered to be types of
sexual reproduction because they obviously are derived from sexual
reproductive processes (i.e., the process of oogenesis is modified).
The production of males by parthenogenesis is termed arrhenotoky,
while parthenogenetic production of females is termed thelytoky.
See White (1954), Bacci (1965), Crew (1965), and Engelmann (1970)
for more complete discussions on parthenogenesis.
Gametes are formed through gametogenesis, & process which is
markedly similar among most animals (Fig. 2). Generally, primordial
4 GIESEANDPEARSE
FIG. 2. Diagram of the general cellular changes that occur during gametogenesis.
germ cells (gonocytes) appear early in the development of an animal
and either migrate to, or form the locus of, the gonads. Primordial
germ cells multiply by mitosis and produce gonial cells. Gonial cells
(spermatogonia in males, oogonia in females) can sometimes be sepa-
rated into multiplying (primary) and terminal (secondary) stages.
Primary gonial cells usually go through a limited number of mitotic
divisions (usually 2-6), and the resulting secondary gonial cells
transform into primary spermatocytes (in males) or primary oocytes
(in females). In practice, primordial germ cells, primary and sec-
ondary gonial cells, and young primary spermatocytes and primary
oocytes are difficult to distinguish from each other; all are usually
relatively large cells, each containing a conspicuous large nucleus.
Both primary spermatocytes and primary oocytes undergo a
number of characteristic nuclear changes during prophase of the first
1. INTRODUCTION 5
meiotic division. These changes involve the duplication, pairing,
condensation, and partial separation of the homologous chromo-
somes, and the more or less discrete stages are termed leptotene,
zygotene, pachytene, diplotene, and diakinesis (see White, 1954;
Raven, 1961; Bacci, 1965). In spermatogenesis, these changes are fol-
lowed by the first meiotic division of the primary spermatocytes to
form the secondary spermatocytes. The second meiotic division oc-
curs soon after the secondary spermatocytes are formed, and pro-
duces haploid spermatids (four spermatids for each primary
spermatocyte). Differentiation of the spermatids into mature sperma-
tozoa (sperms) is termed spermiogenesis or spermateleosis. Spermi-
ogenesis is always completed, and usually large numbers of sperms
are accumulated, before the sperms are shed.
Nuclear changes are arrested when the diplotene stage is reached
in the primary oocytes, and the paired, partially separated, chromo-
somes are dispersed in the nuclear sap of the enlarged nucleus
(termed the germinal vesicle). Usually the nucleus contains one con-
spicuous nucleolus at this stage. Subsequent primary oocyte devel-
opment goes through two distinct phases (Raven, 1961; Schuetz,
1969a). First there is a period of intense RNA synthesis and the large
number of ribosomes accumulated typically cause the cytoplasm of
the cell to be strongly basophilic. This period is followed by growth
of the primary oocyte through the uptake and accumulation of nutri-
ents (vitellogenesis) (Schjeide et al., 1970), and often the cytoplasm
becomes weakly basophilic or even acidophilic. Primary oocyte
growth is usually assisted by accessory cells in the ovary called nutri-
ent, follicle or nurse cells (see Davidson, 1968, for distinction of
these cell types). Full-grown primary oocytes vary in size among
different species, but usually they range from about 75 μτη to several
millimeters in diameter. After reaching full size, the primary oocytes
may undergo the two meiotic divisions (maturation divisions) to form
haploid ova. Secondary oocytes, like secondary spermatocytes, are
usually very transitory and are not often encountered. Some inverte-
brates (e.g., many echinoids) accumulate ova in the ovaries and these
are shed during spawning. In many other invertebrates, however,
"eggs" are shed as full-grown, diploid, primary oocytes, and the
meiotic divisions are completed after spawning (e.g., asteroids) or
fertilization (e.g., platyhelminths). These differences in the timing of
the completion of meiosis with respect to fertilization have led to
considerable confusion in terminology (Schuetz, 1969a). In this trea-
tise, the term ova refers to haploid female gametes only; the more
general term, eggs, is used for female gametes (primary oocytes or
ova), zygotes, or embryos which are held or shed by the female.
